Adrangi - 2013 - Biotech Advance - Review Quitinasas, Faltan EC 3.2.1.200-202 - No Las Agrega

JBA-06743; No of Pages 10
Biotechnology Advances xxx (2013) xxxxxx
Contents lists available at ScienceDirect
Biotechnology Advances
journal homepage: www.elsevier.com/locate/biotechadv
1 Research review paper
2Q2 From bacteria to human: A journey into the world of chitinases

3Q1 Sina Adrangi a, Mohammad Ali Faramarzi b,
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4 a
Department of Pharmaceutical Biotechnology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, Iran
5 b
Department of Pharmaceutical Biotechnology, Faculty of Pharmacy and Biotechnology Research Center, Tehran University of Medical Sciences, P.O. Box 14155-6451, Tehran 14176, Iran
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a r t i c l e i n f o a b s t r a c t
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8 Article history: Chitinases, the enzymes responsible for the biological degradation of chitin, are found in a wide range of 22
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9 Received 7 August 2012 organisms from bacteria to higher plants and animals. They participate in numerous physiological processes 23
10 Received in revised form 26 September 2013 such as nutrition, parasitism, morphogenesis and immunity. Many organisms, in addition to chitinases, produce 24
11 Accepted 28 September 2013
inactive chitinase-like lectins that despite lacking enzymatic activity are involved in several regulatory functions. 25
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12 Available online xxxx
Most known chitinases belong to families 18 and 19 of glycosyl hydrolases, however a few chitinases that belong 26
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16 Keywords:
to families 23 and 48 have also been identied in recent years. In this review, different aspects of chitinases and 27
17 Chitinase chi-lectins from bacteria, fungi, insects, plants and mammals are discussed. 28
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Chi-lectin
Gene evolution
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20 Biocontrol
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21 Biomarker
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34 Contents
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36 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
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37 2. Classication, structure and catalytic mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

38 3. Bacterial chitinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
39 4. Fungal chitinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
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40 5. Insect chitinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
41 6. Plant chitinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
42 7. Mammalian chitinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
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43 8. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
44 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
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46 1. Introduction chains. Chitinolytic enzymes are produced by a wide range of organisms 54

including bacteria, fungi, insects, plants and animals for different 55
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47 Chitin is the second most abundant natural carbohydrate polymer purposes such as nutrition, morphogenesis, and defense against chitin- 56
48 after cellulose and consists of -(1 4)-linked units of N- containing pathogens (Adrangi et al., 2010). Many of theses organisms 57
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49 acetylglucosamine (GlcNAc). It is a major component of fungal cell possess several genes that encode chitinolytic enzymes. For example, 58
50 walls and invertebrate exoskeletons. In nature, chitin occurs in two most lamentous fungi have 10 to 20 different chitinolytic genes, 59
51 different crystalline forms, and (Aam et al., 2010). -Chitin is the while in mycoparasitic species the number of such genes may reach 60
52 dominant form and it is composed of linear chains of GlcNAc arranged 30 or even higher (Hartl et al., 2012). These enzymes act in a synergetic 61
53 in an antiparallel manner. On the other hand, -chitin consists of parallel or successive manner to degrade chitin (Patil et al., 2000). Higher 62
organisms such as Arabidopsis have also been reported to contain a 63
large number of chitinolytic genes (Hossain et al., 2010). However, not 64
Abbreviations: AMCase, acidic mammalian chitinase; CBM, carbohydrate-binding all of these gene codes are for active enzymes. Many organisms 65
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module; GH, glycosyl hydrolase; GlcNAc, N-acetylglucosamine; IAD, innovation, amplica- including plants, invertebrates and higher animals express genes 66
tion, and divergence; ISP, ice structuring protein; MDN, mutation during non-functionality;
encoding so called chitinase-like lectins (chi-lectins) that are devoid of 67
PR, pathogenesis-related.
Corresponding author. Tel./fax: +98 21 66954712. chitinolytic activity due to substitutions in their key catalytic residues 68
E-mail address: faramarz@tums.ac.ir (M.A. Faramarzi). (Arakane and Muthukrishnan, 2010; Hossain et al., 2010; Vega and 69
0734-9750/$ see front matter 2013 Published by Elsevier Inc.

http://dx.doi.org/10.1016/j.biotechadv.2013.09.012
Please cite this article as: Adrangi S, Faramarzi MA, From bacteria to human: A journey into the world of chitinases, Biotechnol Adv (2013), http://
dx.doi.org/10.1016/j.biotechadv.2013.09.012
2 S. Adrangi, M.A. Faramarzi / Biotechnology Advances xxx (2013) xxxxxx
70 Kalkum, 2012). Despite lacking catalytic activity, these proteins retain provide the necessary environment for the exible binding and move- 119
71 the capacity to bind chitin. Owing to their widespread presence and ment of the substrate through the active site. Although processivity 120
72 diverse biological functions, chitinolytic enzymes have found several comprises an efcient strategy for the hydrolysis of insoluble substrates, 121
73 applications. For example they can be used in the production of it is usually associated with reduced activity towards soluble or more 122
74 single-cell proteins, isolation of fungal protoplasts, estimation of accessible polymeric substrates (Aam et al., 2010). 123
75 fungal biomass, development of 3D cell culture scaffolds, biocontrol Like other glycosyl hydrolases, chitinolytic enzymes generally cata- 124
76 of plant-pathogenic fungi and insect vectors, and the production of lyze the depolymerization of their substrate through one of the two 125
77 chitooligosaccharides, glucosamine, GlcNAc, neoglycoproteins and arti- pathways known as single- and double-displacement mechanisms 126
78 cial polysaccharides (Adrangi et al., 2010; Jamialahmadi et al., 2011; Li (Aam et al., 2010; Andersen et al., 2005; Cantarel et al., 2009; Li and 127
79 et al., 2008; Lu et al., 2012; Ortiz-Rodriguez et al., 2010; Tajdini et al., Greene, 2010; Slamova et al., 2010; Tang et al., 2004; Udaya Prakash 128
80 2010; Zakariassen et al., 2011). Recent studies in the eld of chitinolytic et al., 2010). In both pathways, two distinct catalytic groups are 129
81 enzymes have demonstrated that both the diversity and the physiolog- involved. One of these is a carboxyl group that acts as a proton donor 130
82 ical roles of these enzymes are far beyond those previously recognized. and is usually provided by a conserved glutamate residue at the active 131
site of the enzyme, although in some cases, for example in family 132
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83 2. Classication, structure and catalytic mechanism GH84, an aspartate residue may fulll this role (Table 1). The second 133
catalytic group may act either as a base (as in the single-displacement 134
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84 Based on their mode of action, chitinolytic enzymes are classied into mechanism) or a nucleophile (as in the double-displacement mecha- 135
85 two categories: chitinases (EC 3.2.1.14) that cleave the chitin chain at nism). This group may be a carboxyl moiety provided by a conserved 136
86 internal sites in a random manner, and -N-acetylhexosaminidases glutamate or aspartate residue, or it may be the N-acetyl group of the 137
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87 (EC 3.2.1.52) that catalyze the successive removal of GlcNAc residues sugar positioned in the 1 subsite of the enzyme (Aam et al., 2010; 138
88 from the non-reducing end of the chain (Adrangi et al., 2010). Chitinases Udaya Prakash et al., 2010). Subsites are numbered from n to +n, 139
89 occur in families 18, 19, 23, and 48 of glycosyl hydrolases (GH), while where negative sign represents the non-reducing end of the chain with 140
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90 -N-acetylhexosaminidases are included in GH3, GH18, GH20, and cleavage occurring between the 1 and +1 subsites (Davies et al., 141
91 GH84 (Table 1). The classication of GH families is based on sequence 1997). Since the single-displacement mechanism results in the inversion 142
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92 homology and a continuously updated list of these families is available of the anomeric conguration of the hydrolyzed GlcNAc residue, it is also 143
93 through the CAZy database (Cantarel et al., 2009). The catalytic domains known as the inverting mechanism. On the other hand, in the double- 144
94 of members of each GH family fold into a common three-dimensional displacement mechanism, also referred to as the retaining mechanism,
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95 structure (Fig. 1). Families GH18, GH20, and GH84 all have similar the anomeric conguration is retained. 146
96 (/)8 barrel domains (Sumida et al., 2011). On the other hand, GH19
97 and GH23 enzymes adopt an + structure, while the catalytic domain 3. Bacterial chitinases 147
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98 of GH3 enzymes has a bipartite structure comprising a (/)8 barrel
99 followed by an (/)6 sandwich (Wohlkonig et al., 2010; Yoshida Bacterial chitinases occur in families GH18, GH19, and GH23 (Dahiya 148
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100 et al., 2010). Some GH3 enzymes, however, lack the (/)6 sandwich et al., 2006; Udaya Prakash et al., 2010; Ueda et al., 2009). Most bacterial 149
101 (Yoshida et al., 2010). Finally, GH48 enzymes have an (/)6 barrel chitinases belong to the GH18 family (Larsen et al., 2011) (Fig. 3). Based 150
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102 structure characterized by six central -helices surrounded by six exter- on sequence homology, bacterial GH18 chitinases are classied into 151
103 nal -helices (Yennamalli et al., 2011). Most chitinases are modular pro- three subfamilies A, B and C (Li and Greene, 2010). It should be noted 152
104 teins that, in addition to a catalytic domain, contain auxiliary domains that the nomenclature of bacterial chitinases does not follow this classi- 153
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105 such as the carbohydrate-binding module (CBM) (Guillen et al., 2010). cation; for example, chitinase B from Serratia marcescens belongs to 154
106 The CBM enhances the activity of the enzyme towards insoluble sub- subfamily A while Bacillus circulans chitinase D is classied in subfamily 155
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107 strates by anchoring the enzyme to the substrate and disrupting the B (Watanabe et al., 1999). Some bacterial GH18 chitinases besides 156
108 crystalline structure of the substrate resulting in the formation of free catalytic and CBM domains contain a bronectin type III-like domain 157
109 chain ends (Guillen et al., 2010; Vaaje-Kolstad et al., 2005). Like catalytic which plays a role in substrate binding (Horn et al., 2006a). On the 158
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110 modules, CBMs are classied into families of homologous proteins which other hand, the distribution of GH19 chitinases among bacteria appears 159
111 may be accessed at the CAZy database. A second feature that helps to to be restricted to actinobacteria and purple bacteria (Udaya Prakash 160
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112 overcome the low accessibility of insoluble substrates is the presence et al., 2010). It has been proposed that actinobacteria and purple bacte- 161
113 of a deep and narrow substrate-binding cleft lined with aromatic ria may have acquired GH19 chitinase genes from plants and, in turn, 162
114 residues in some chitinolytic enzymes (Fig. 2) (Horn et al., 2006a,b; transferred them to arthropods and nematodes (Udaya Prakash et al., 163
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115 Zakariassen et al., 2010). Such enzymes act in a processive manner, 2010). To date, only one GH23 chitinase has been identied in bacteria 164
116 meaning once attached to a substrate chain, they thread the chain (Ueda et al., 2009). This enzyme was isolated from Ralstonia sp. 165
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117 through their catalytic cleft performing several hydrolytic cuts instead A-471 and comprises an N-terminal chitin-binding domain linked to 166
118 of releasing the substrate after each cleavage. The aromatic residues a C-terminal catalytic domain that shows homology to goose-type 167
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t1:1 Table 1
t1:2 Characteristics of chitinolytic enzymes belonging to different GH families.
t1:3 Family Catalytic mechanism Proton donor Base/nucleophile Structure Reference
t1:4 Chitinases
t1:5 GH18 Retaining Glu Substrate acetamido group (/)8 CAZY; Sumida et al. (2011)
t1:6 GH19 Inverting Glu Glu/asp + CAZY; Wohlkonig et al. (2010)
t1:7 GH23 Inverting Glu Not known + CAZY; Wohlkonig et al. (2010);
Arimori et al. (2013)
t1:8 GH48 Inverting Glu Not known (/)6 CAZY; Yennamalli et al. (2011)
t1:9
t1:10 -N-acetylhexosaminidases
t1:11 GH3 Retaining Glu Asp (/)8 + (/)6 CAZY; Yoshida et al. (2010)
t1:12 GH18 Retaining Glu Substrate acetamido group (/)8 CAZY; Sumida et al. (2011)
t1:13 GH20 Retaining Glu Substrate acetamido group (/)8 CAZY
t1:14 GH84 Retaining Asp Substrate acetamido group (/)8 CAZY
S. Adrangi, M.A. Faramarzi / Biotechnology Advances xxx (2013) xxxxxx 3
Fig. 1. Three-dimensional structure of representative GH enzymes. (A) A GH18 chitinase from Aspergillus fumigatus showing a (/)8 barrel (PDB ID: 2XVP). (B) A GH19 chitinase from
Carica papaya showing + structure (PDB ID: 3CQL). In most cases, like this example, the regions are actually composed of isolated bridges rather than extended strands (residues
shown in stick representation). (C) A GH3 glucohydrolase from Hordeum vulgare showing a bipartite domain consisting of a (/)8 barrel (lower right) and an (/)6 sandwich (upper
left) (PDB ID: 1IEQ). (D) A GH48 cellobiohydrolase from Clostridium thermocellum showing an (/)6 barrel (PDB ID: 1L1Y). All gures were prepared using VMD (Humphrey et al., 1996).
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168 lysozyme. The gene encoding this enzyme also appears to be acquired membrane (Chandler et al., 2011; Killiny et al., 2010). However, even 197
169 via horizontal gene transfer (Ueda et al., 2009). in non-chitinous hosts, chitinases may directly contribute to bacterial 198
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170 Bacteria produce chitinases for different purposes such as nutrition virulence, probably by binding to alternative substrates such as the 199
171 and parasitism (Dahiya et al., 2006; Faramarzi et al., 2009). For some carbohydrate moieties of glycoproteins involved in the host's immune 200
172 species, chitinases may play an essential role in providing the bacterium response (Chaudhuri et al., 2010). In the human pathogen Listeria 201
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173 with required nutrients or precursors. The spirochete Borrelia burgdorferi, monocytogenes, the virulence gene regulator PrfA induces, among other 202
174 for example, is unable to produce GlcNAc required for cell wall synthesis genes, chitinase expression indicating that the biological functions of 203
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175 and in an environment such as the tick midgut where free GlcNAc is not this enzyme are not limited to the external environment (Larsen et al., 204
176 available, the ability to degrade the chitin-rich peritrophic membrane 2010). Chitinase production is also stimulated by the quorum-sensing 205
177 would allow the bacterium to obtain the necessary GlcNAc (Rhodes LuxRLuxI homologous system that is involved in virulence, biolm
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178 et al., 2010). It has also been shown that the chitinase system of formation and surface motility in some pathogens such as Pseudomonas 207
179 Pseudoalteromonas is involved in nitrogen metabolism (Delpin and aeruginosa and Chromobacterium violaceum (Alipour et al., 2010; Stauff 208
180 Goodman, 2009). However, for many other heterotrophic bacteria and Bassler, 2011). Clostridium difcile produces a bifunctional protein 209
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181 chitinases are probably not crucial in this respect since in most habitats with chitinase and peroxiredoxin activities that appears to be partly 210
182 different nutrient sources are available (Cottrell et al., 2000). On the responsible for the symptoms of C. difcile infection (Permpoonpattana 211
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183 other hand, autotrophic microorganisms such as the cyanobacterium et al., 2011). 212
184 Anabaena probably produces chitinolytic enzymes as part of their allelo- Bacteria also produce chitin-binding proteins comprised exclusively 213
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185 pathic system to inhibit the growth of competitor organisms such as of non-catalytic CBMs. For example, S. marcescens secretes a protein 214
186 fungi (Prasanna et al., 2010). Chitinases are also involved in bacterial named CBP21 that belongs to CBM family 33 and seems to be involved 215
187 pathogenesis. In cases where the host is known to contain chitin, such in chitin digestion despite lacking hydrolytic activity (Vaaje-Kolstad 216
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188 as in insects, the mechanism seems straightforward. For example, the et al., 2005). CBP21 probably promotes the degradation of insoluble 217
189 entomopathogenic bacterium Yersinia entomophaga produces an ABC- chitin via non-enzymatic disruption of the crystalline structure of the 218
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190 type protein toxin complex that can kill the host within 72 h of infection substrate. Nevertheless, recent studies suggest that CBP21 may actually 219
191 (Busby et al., 2012; Landsberg et al., 2011). It has been shown that this possess oxidoreductase activity (Tran et al., 2011; Vaaje-Kolstad et al., 220
192 complex includes two subunits with chitinase activity that anchor the 2010). The majority of bacterial CBM proteins belong to the CBM33 221
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193 complex to, and facilitate its penetration through the peritrophic family while their eukaryotic counterparts mostly belong to CBM fami- 222
194 membrane (Busby et al., 2012). Vector-borne bacterial pathogens of lies 14 and 18 (Purushotham et al., 2012; Tran et al., 2011). 223
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195 non-chitinous organisms such as mammals and plants also produce It has been shown that some bacteria such as Streptomyces and 224
196 chitinases to colonize the insect vector by digesting the peritrophic Bacillus licheniformis produce different chitinase inhibitors; however 225
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Fig. 2. Substrate-binding cleft of processive and non-processive chitinases. (A) A processive chitinase from Serratia marcescens (PDB ID: 1E6N). (B) A non-processive chitinase from Hevea
brasiliensis (PDB ID: 1KQY). Cocrystallized substrates are shown in stick representation.
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Fig. 3. A cladogram showing the relationship of selected chitinases from all bacterial genera represented with at least one GH18 chitinase sequence in the NCBI RefSeq database. Chitinase D
from Bacillus circulans (Swiss-Prot Accession: P27050) was used as query for a BLAST search against the RefSeq database. A total number of 439 chitinase sequences from 68 bacterial
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genera were obtained (E value b 0.01) and aligned using MEGA5 (Tamura et al., 2011). For each genus, the entry showing the highest degree of similarity to the query sequence was
selected and included in the cladogram. It should be noted that most of these genera are represented in RefSeq with several species and each species with more than one chitinase;
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as a result, depending on the selected sequences, the topology of the resulting tree may vary.
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226 the biological functions of these inhibitors are not completely claried bacteriophage and bacterial cell wall degrading enzymes as a substrate 253
227 (Kumar and Rao, 2010; Suzuki et al., 2008). Allosamidin is a (peptidoglycan) binding domain (Bateman and Bycroft, 2000). It was 254
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228 pseudotrisaccharide produced by some Streptomyces species that later shown to bind other glycans such as chitooligosaccharides as 255
229 mimics the structure of chitin and competitively inhibits GH18 well (Buist et al., 2008). In plants, specic LysM-containing cell surface 256
230 chitinases. Although allosamidin can suppress chitinase activity in receptors (known as LysM-RLK) are involved in the perception of rhizo- 257
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231 allosamidin-nonproducer strains, it is not secreted to the medium by bial nodulation (Nod) factors (Radutoiu et al., 2003). Nod factors are 258
232 the producer strain and rather tends to accumulate in the mycelia lipochitooligosaccharide signaling molecules secreted by Rhizobium 259
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233 where it probably acts as a signal molecule for chitinase production bacteria that induce the formation of symbiotic root nodules in legumi- 260
234 (Suzuki et al., 2008). The peptidic aspartic protease inhibitor of nous plants (Knogge and Scheel, 2006). Since these molecules are 261
235 B. licheniformis, on the other hand, is secreted to the medium and subjected to species-specic substitutions, they are believed to play a 262
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236 shows a non-competitive inhibition pattern (Kumar and Rao, 2010). major role in the specic recognition of Rhizobium species by the host 263
plants (Gressent et al., 2002; Streng et al., 2011). In fact, it has been 264
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237 4. Fungal chitinases shown that the heterologous expression of the enzymes involved in 265
the acylation of Nod factors may be used to extend the host range of 266
238 Fungal chitinases are members of the GH18 family (Hartl et al., Rhizobium bacteria (Pacios Bras et al., 2000). Plant LysM-RLKs also 267
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239 2012). They can be further divided into three subgroups, namely A, B, play a role in defense against fungal pathogens (Brotman et al., 2012; 268
240 and C (not to be confused with bacterial GH18 chitinase subfamilies). Petutschnig et al., 2010). Based on these ndings, as well as the observa- 269
241 This classication scheme primarily makes use of sequence similarity tion that subgroup C chitinases are present at higher numbers in 270
242 but other distinctive features have also been described (Seidl, 2008). mycoparasitic fungi, it was hypothesized that it may be possible to 271
243 Subgroup A chitinases contain a single catalytic domain and no CBMs. categorize fungal chitinases as self- and non-self degrading enzymes 272
244 These are processive enzymes with a deep substrate-binding cleft. Sub- (Gruber and Seidl-Seiboth, 2012). However, detailed analysis of the 273
245 group B chitinases are non-processive and in addition to their catalytic expression prole of subgroup C chitinases from several mycoparasitic 274
246 domain comprise either a C-terminal CBM or an unstructured serine/ Trichoderma species revealed that these enzymes are not expressed in 275
247 threonine-rich domain. Subgroup C chitinases consist of an N-terminal a mycoparasitism-specic manner suggesting that they are involved in 276
248 CBM linked to a C-terminal catalytic domain. Like subgroup A, subgroup the degradation of both self and non-self cell walls (Gruber and Seidl- 277
249 C chitinases have a deep narrow substrate-binding cleft that indicates Seiboth, 2012; Gruber et al., 2011a,b). The protection of the fungus's 278
250 a processive nature. An interesting feature of subgroup C chitinases is own cell wall is probably achieved by limiting the accessibility of 279
251 the presence of several LysM (lysin motif; also known as CBM50) chitin by cell wall proteins rather than the speciation of individual 280
252 domains (Hartl et al., 2012). The LysM domain was rst identied in chitinases (Gruber and Seidl-Seiboth, 2012). In situations where self 281
282 cell wall degradation is required, e.g. in hyphal branching, a localized Insect chitinases play an important role in chitin turnover especially 345
283 de-protection of chitin occurs. In addition to mycoparasitic fungi, non- during molting. However, their expression should be tightly controlled 346
284 mycoparasitic fungi have also been shown to secret proteins with since premature exposure can lead to growth inhibition and mortality 347
285 chitinolytic activity in order to inhibit the growth of competitive fungi. (H. Zhang et al., 2011). To achieve such a control, insects produce several 348
286 For example, the subunit of Kluyveromyces lactis killer toxin, which functionally specialized chitinases that are differentially expressed 349
287 is essential for the antifungal activity of the toxin, is actually a through the various stages of metamorphosis (Zhu et al., 2008). At 350
288 chitinolytic enzyme (Colussi et al., 2005). least some of these enzymes are regulated by hormonal control 351
289 In nature, entomopathogenic fungi play an important role in control- (Merzendorfer and Zimoch, 2003; Royer et al., 2002; Takahashi et al., 352
290 ling insect pests, especially those that are resistant to viral and bacterial 2002; Zheng et al., 2003). For example, in Tribolium castaneum, TcCHT5 353
291 infections (Fang et al., 2012; Schrank and Vainstein, 2010). Since is required for pupaladult molting only while TcCHT10 is involved in 354
292 chitinases are an important part of the enzymatic arsenal of these larvallarval, larvalpupal and pupaladult molting (Zhu et al., 2008). 355
293 fungi, improved strains overexpressing native or engineered chitinases Since during a normal molting cycle the synthesis of the new cuticle 356
294 have been produced and demonstrated to exhibit increased virulence and the degradation of the old cuticle occur simultaneously, it is also 357
295 against insects (Fan et al., 2007; Fang et al., 2005). Such improved important to protect the nascent cuticle from chitinases and other 358
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296 strains can potentially be used in the biocontrol of pest and disease molting enzymes (Chaudhari et al., 2011). This is mainly achieved 359
297 vector insects (Fang et al., 2012; Jami Al Ahmadi et al., 2008; through the action of specic proteins that colocalize and directly inter- 360
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298 Tasharro et al., 2011). An alternative approach is to use fungal or act with newly synthesized chitin and organize it into laminae confer- 361
299 bacterial chitinases directly as biopesticides (Binod et al., 2007; Kim ring resistance to chitinolytic enzymes (Chaudhari et al., 2011; Petkau 362
300 and Je, 2010; Martinez et al., 2012). The insecticidal activity of such et al., 2012). Knickkopf is one such protein that shows homology to 363
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301 preparations may be improved by the addition of adjuvants such as the CBM9 family (Chaudhari et al., 2011; Iyer et al., 2007). The 364
302 polyoxyethylene-(3)-isotridecyl ether that promote the penetration of colocalization of Knickkopf with chitin appears to be controlled by yet 365
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303 the enzymes through epicuticle (Kim et al., 2010). In practice, however, another protein known as Obstructor-A which is encoded by a member 366
304 the applicability of this method is limited by several factors including of the obstructor multigene family (Petkau et al., 2012). The obstructor 367
305 the rapid evaporation of the aqueous phase especially under drying family was rst identied in Drosophila melanogaster and shown to 368
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306 conditions. Nematode-pathogenic fungi such as Clonostachys rosea code for putative chitin-binding proteins (Behr and Hoch, 2005). 369
307 that produce several proteases and chitinases to target eggs and larvae Chitinases (and chi-lectins) are also produced by the venom and salivary 370
308 have also been exploited as biological control agents to suppress glands of some insect species (Arakane and Muthukrishnan, 2010).
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309 plant or even animal parasitic nematodes (Baloyi et al., 2012; Zou In endoparasitoid wasps such as Chelonus inanitus and Toxoneuron 372
310 et al., 2010). nigriceps the venom chitinases are probably involved in the degradation 373
311 Invasive fungal infections are a major cause of mortality in immuno- of the host cuticle facilitating the egression or ingression of parasitoid 374
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312 suppressed patients mostly due to the fact that current diagnostic larvae through such barriers (Consoli et al., 2005; Vincent et al., 2010). 375
313 methods usually fail to detect fungal infections at early stages (Vega However, it has been shown that the venom of ectoparasitoid species 376
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314 and Kalkum, 2012). It has been proposed that radiolabeled chitinases like Nasonia vitripennis also contains chitinases (Danneels et al., 2010). 377
315 and chitin-binding proteins may be used for the early detection Since in ectoparasitoids no larval egression or ingression occurs, other 378
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316 of such infections (Lupetti et al., 2011). Other methods that detect functions should be ascribed to these enzymes (Danneels et al., 2010). 379
317 the host responses to fungal infections such as the use of immuno- The physiological role of chi-lectins found in the saliva of some insects 380
318 uorescence stains for chitinase have also been investigated (Guo such as the anopheline mosquito is not well understood either. It 381
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319 et al., 2012). Nevertheless, further studies are needed before these has been proposed that these chi-lectins may be involved in the self- 382
320 approaches are ready for clinical use. defense mechanism of the anopheline mosquito against malaria 383
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parasites through a complex sequence of events (Owhashi et al., 384

2008). Plasmodium falciparum, the causative parasite of malaria, during 385
321 5. Insect chitinases its sporogonic cycle in the midgut of the anopheline vector, produces a 386
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chitinase that disrupts the peritrophic membrane and allows the 387
322 With the exception of a GH48 chitinase identied in the leaf beetle parasite to migrate to the salivary glands of the vector (Giansanti et al., 388
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323 Gastrophysa atrocyanea (Fujita et al., 2006), all known insect chitinases 2007). Inhibition of this enzyme results in complete disruption of 389
324 belong to the family GH18 (J. Zhang et al., 2011). Based on sequence sporogonic development (Bhatnagar et al., 2003; Isaacs et al., 2012). 390
325 homology and domain architecture, GH18 insect chitinases have been Following a mosquito bite, the mosquito saliva proteins including 391
C
326 assigned into eight distinct groups denoted by Roman numerals IVIII chi-lectins are introduced to the immune system of the host where 392
327 (Arakane and Muthukrishnan, 2010; H. Zhang et al., 2011). Group I they induce antibody production. Such anti-chitinase antibodies are 393
N
328 are characterized by the presence of an N-terminal catalytic domain frequently encountered in the sera of residents of malaria-endemic 394
329 joined to a CBM14 domain via a serine/threonine-rich linker. The linker areas (Owhashi et al., 2008). Ingestion of these antibodies from blood 395
330 region serves as a site for glycosylation which increases the stability of meals may contribute to the defense mechanism of mosquitoes by 396
U
331 the enzyme against proteases. Group II are much larger proteins with inhibiting the chitinolytic activity of malaria parasites (Owhashi et al., 397
332 45 catalytic domains and 47 CBMs. Some catalytic domains of group 2008). Insect chi-lectins have been shown to contribute to other 398
333 II chitinases seem to be enzymatically inactive as their catalytic aspartic processes such as growth regulation and immunity as well (Aronstein 399
334 acid residue is replaced by other residues such as histidine or serine et al., 2010; Nakabachi et al., 2010). 400
335 (Arakane and Muthukrishnan, 2010). Group III chitinases consist of
336 two catalytic domains and a single CBM. Groups IV, V, VII and VIII have 6. Plant chitinases 401
337 a single catalytic domain and usually no CBM, and are distinguished
338 from each other by sequence homology. Group V includes chitinase- Based on sequence similarity, plant chitinases are classied into 402
339 like proteins such as the imaginal disk growth factors (IDGFs) that lack seven classes IVII (Kasprzewska, 2003; Patil et al., 2009; Sarma et al., 403
340 chitinase activity and are involved in growth regulation and immunity. 2012). Class I, II, IV, VI, and VII chitinases belong to the GH19 family 404
341 Group VI chitinases have one catalytic domain, one CBM and a long while class III and V chitinases are members of the GH18 family 405
342 C-terminal stretch with a high percentage of serine and threonine (Ohnuma et al., 2011, 2012). Chitinases comprise an important part of 406
343 residues. Other features such as transmembrane and signal regions pathogenesis-related (PR) proteins; a group of proteins including 407
344 may also be present in all groups. hydrolytic enzymes, enzyme inhibitors, and membrane-permeabilizing 408
409 peptides that are produced by plants in response to invading pathogens 7. Mammalian chitinases 475
410 and abiotic factors (Ebrahim et al., 2011; Edreva, 2005; Li and Yi, 2012;
411 Sels et al., 2008). It should be noted that although this denition includes All known mammalian chitinases belong to the GH18 family 476
412 abiotic factors, induction by such factors alone is not a sufcient criterion (Shuhui et al., 2009). The rst human chitinase to be identied was a 477
413 for categorizing a particular protein as a PR protein (Edreva, 2005). PR chitotriosidase produced by macrophages of Gaucher patients (Boot 478
414 proteins show antifungal, antibacterial, insecticidal, nematicidal, and et al., 1995). Since this enzyme showed antifungal properties, it was 479
415 antiviral effects and participate in the systemic acquired resistance proposed that it may be involved in defense against chitin-containing 480
416 (SAR) of plants against a broad range of pathogens. PR proteins are pathogens. This observation was supported by other studies (Bussink 481
417 currently classied into 17 families with chitinases occurring in families et al., 2006). In contrast to these ndings, later studies revealed that 482
418 PR-3, PR-4, PR-8, and PR-11 (Sels et al., 2008). Considering the impor- about 5% of Caucasian populations are completely decient in active 483
419 tant role of chitinases in plant defense against chitin-containing patho- chitotriosidase suggesting that this enzyme may no longer be a direct 484
420 gens, efforts have been made to produce transgenic plants expressing effector of the innate immune response (Boot et al., 2005). This deciency 485
421 several chitinases or a combination of chitinases and other PR proteins results from a 24-bp duplication in the CHIT1 gene (the gene encoding 486
422 to increase their resistance against such pathogens and promising human chitotriosidase) that leads to aberrant splicing and, consequently, 487
F
423 results have been achieved (Al Ahmadi et al., 2008; Amian et al., 2011; the production of an enzymatically inactive protein. Despite the fact 488
424 Ramana Rao et al., 2011). An alternative approach is to clone chitinase that the relatively high incidence of this polymorphism precludes a 489
O
425 genes in symbiotic rhizobacteria such as Burkholderia vietnamiensis direct defensive function for chitotriosidase, this enzyme still appears 490
426 (Zhang et al., 2012). There are legitimate concerns about the environ- to affect the host's defense system through other mechanisms. In a 491
427 mental consequences of using such procedures; nevertheless eld stud- recent study, it was shown that the aforementioned duplication event 492
O
428 ies have demonstrated that these methods do not negatively affect is strongly associated with an increased rate of decline in the lung func- 493
429 the decomposition dynamics of the plants or the soil fungal biomass tion of smokers with chronic obstructive pulmonary disease (COPD) 494
430 (Duc et al., 2011; Stefani et al., 2010). (Aminuddin et al., 2011). This suggests a protective role against rapid 495
R
431 In addition to their role in defense against pathogens, plant disease progression for human chitotriosidase although the underlying 496
432 chitinases also serve several other physiological functions that may mechanism still remains to be elucidated. Chitotriosidase may also 497
P
433 not be directly related to their hydrolytic activity. For example, some exert some protective effects against atherosclerosis (Kitamoto et al., 498
434 plant chitinases show ice structuring activity (Goni et al., 2010; Yaish 2013). A few years after the discovery of chitotriosidase, a second 499
435 et al., 2006). Ice structuring proteins (ISPs) are a group of proteins chitinase named acidic mammalian chitinase (AMCase) was isolated
D 500
436 produced by different organisms including plants that bind ice crystals and shown to be expressed primarily in the gastrointestinal tract and 501
437 and affect their growth and morphology providing cold or freezing lung of both mouse and human (Boot et al., 2001). Based on its expres- 502
438 tolerance for the organism (Hassas-Roudsari and Goff, 2012). ISPs sion prole, a dual function in innate immunity and chitin digestion was 503
E
439 probably interact with crystals through an ice binding surface composed proposed for AMCase (Bussink et al., 2007). Recent studies performed 504
440 of charge-conserved amino acids located apart from the enzyme's on several bat species suggest that AMCase may actually be involved 505
T
441 active site (Yaish et al., 2006). Plant chitinases are also up-regulated in chitin digestion in insectivorous mammals (Strobel et al., 2013). 506
442 by certain heavy metals such as lead and cadmium (Cai et al., 2011; This is probably not the case for humans, however, as AMCase expres- 507
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443 Walliwalagedara et al., 2010). This may simply represent a common sion level in the human gastrointestinal tract is signicantly lower 508
444 stress response, although there is some evidence that chitinases may than that observed in mouse (Ohno et al., 2013). In the respiratory 509
445 counteract oxidative stress (Walliwalagedara et al., 2010). It has also tract, AMCase also appears to be involved in Th2-mediated inamma- 510
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446 been shown that chitinases can act as calcium storage proteins. Yang tion (Kawada et al., 2007). Originally, it was hypothesized that in 511
447 et al. (2011) have isolated a class III chitinase from Punica granatum response to Th2 cytokines such as IL-13, airway epithelial cells and 512
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448 seeds that binds calcium ions with high capacity. Although the presence macrophages produce AMCase that in turn induces the production of 513
449 of calcium improves the stability of P. granatum seed chitinase, it has several chemokines resulting in the recruitment of T cells, eosinophils 514
450 negligible effect on its activity. The subcellular localization pattern of and macrophages (Lee, 2009; Shuhui et al., 2009; Zhu et al., 2004). 515
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451 this enzyme is also in agreement with a role in calcium storage. This assumption was based on the observation that neutralizing 516
452 Chi-lectins are produced by a broad range of plants and, like active AMCase with anti-AMCase serum or chitinase inhibitors reduced 517
O
453 chitinases, appear to be involved in different physiological processes inammatory inltration in mouse asthma models (Shuhui et al., 518
454 (Van Damme et al., 2007). In Arabidopsis thaliana and Oryza sativa 2009). However, a recent study has shown that AMCase may act 519
455 chi-lectins play an essential role in cellulose biosynthesis (Sanchez- through altering the Th1/Th2 balance in lungs (Fitz et al., 2012). One 520
C
456 Rodriguez et al., 2012; Wu et al., 2012). The underlying mechanism of should note that some of the physiological functions of AMCase are 521
457 this observation is not completely understood but evidence suggests independent from its enzymatic activity (Hartl et al., 2009), hence, 522
N
458 that chi-lectins bind to emerging cellulose microbrils and affect their considering the different nature of the neutralizing agents used in 523
459 crystallinity or the association of crystalline and amorphous regions these studies, it can be assumed that these two proposed mechanisms 524
460 (Sanchez-Rodriguez et al., 2012). In another study it was demonstrated may represent two different pathways through which AMCase exerts 525
U
461 that chi-lectins affect root structure architecture in A. thaliana through its effects. AMCase and/or chitotriosidase may also be implicated in 526
462 similar mechanisms (Hermans et al., 2010). On the other hand, studies conjunctivitis, nasal polyp pathogenesis, adenoid hypertrophy, neuro- 527
463 on fruit ripening in banana have shown that some chi-lectins may myelitis, and gastritis (Bucolo et al., 2011; Correale and Fiol, 2011; 528
464 serve as storage proteins to support the synthesis of ripening- Cozzarini et al., 2009; Heo et al., 2011; Park et al., 2011). Both AMCase 529
465 associated proteins by providing the required amino acids (Peumans and chitotriosidase, in addition to an N-terminal catalytic domain, con- 530
466 et al., 2002). Plant chi-lectins also show antifungal and insecticidal activ- tain a C-terminal CBM that belongs to the CBM14 family (Funkhouser 531
467 ity (Vasconcelos et al., 2011; Wasano et al., 2009). It has been proposed and Aronson, 2007), and the genes coding for both enzymes have 532
468 that the antifungal activity of chi-lectins results from their ability to been identied in all mammals for which complete genome data are 533
469 inhibit fungal glycosidases such as xylanases, however other mecha- available (Bussink et al., 2007). 534
470 nisms may also be involved (Vasconcelos et al., 2011). With regard to In addition to active chitinolytic enzymes, mammalian genomes 535
471 their insecticidal activity, chi-lectins probably exert their toxic effect by also code for enzymatically inactive chi-lectins (Shuhui et al., 2009). In 536
472 disrupting the formation of the peritrophic membrane (Wasano et al., humans three chi-lectins have been identied: human chitinase 3-like 537
473 2009). Plant chi-lectins are up-regulates in response to abiotic stresses protein 1 (CHI3L1; also known as YKL-40), human chitinase 3-like pro- 538
474 such as drought, heat, and high salinity as well (Kwon et al., 2007). tein 2 (CHI3L2; also known as YKL-39), and oviductin (OVGP1) (Bussink 539
540 et al., 2007; Shuhui et al., 2009). The mouse genome contains at least model indicates that gene duplication precedes the acquisition of new 604
541 seven chi-lectin genes. The physiological function of chi-lectins is not functions and, in order to prevent the loss of the newly duplicated 605
542 completely understood but they appear to be involved in different pro- gene due to drift or other processes, some selective pressure must be 606
543 cesses such as tissue remodeling, fertilization, and innate immunity present. Several mechanisms such as the protective effect of redundancy, 607
544 (Bussink et al., 2006; Vega and Kalkum, 2012). For example, it has stabilization by subfunctionalization, and the effect of increased gene 608
545 been shown that CHI3L1 mediates mammary tissue remodeling during dosage participate in the maintenance of the duplicated gene, among 609
546 involution possibly by inhibiting epithelial cell differentiation and which the latter may have played an important role in the evolution of 610
547 polarization and inducing cell motility (Scully et al., 2011). However, chitinases. As described in Section 1, many organisms such as fungi con- 611
548 elevated levels of CHI3L1 are also associated with pathologic conditions tain several chitinase genes that might have provided them competitive 612
549 such as breast malignancies which are characterized by poor differenti- advantage. Once a duplicated gene has been stabilized, it may, over 613
550 ation (Scully et al., 2011). In fact, the murine homologue of CHI3L1 was time, acquire the rare mutations that provide a new function. On the 614
551 rst discovered in breast cancer cells and named breast regression other hand, according to the IAD model, innovation (acquisition of 615
552 protein 39 (BRP-39) (Lee et al., 2009). In Th2-dependent immune minor side activities) occurs before gene duplication. These activities 616
553 responses, on the other hand, CHI3L1 appears to be involved in macro- are neither benecial nor detrimental per se, but they may become 617
F
554 phage and dendritic cell activation and apoptosis prevention (Lee et al., valuable following a change in the surrounding environment that favors 618
555 2009), and thus it is not surprising that increased expression of one of these newly acquired functions. In this instance, the new 619
O
556 chi-lectins has been reported in several inammatory diseases such as function may act as a selectable trait. Such non-enzymatic side activities 620
557 neuromyelitis (Correale and Fiol, 2011), colitis (Aomatsu et al., 2011), have been documented for mammalian and plant chitinases, as 621
558 COPD (Sakazaki et al., 2011), and hepatitis (Lebensztejn et al., 2007). discussed in Sections 6 and 7. The IAD model can also explain the 622
O
559 CHI3L1 appears to exert its effect by binding to interleukin-13 receptor emergence of chi-lectins. It can be hypothesized that with the elimina- 623
560 2 (He et al., 2013). It has been proposed that chi-lectins may be used tion of the need for active chitinases, the selective pressure preventing 624
forbidden mutations in critical regions such as the catalytic active
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561 as biomarkers to evaluate the stage, prognosis and therapeutic response 625
562 of different diseases (Agapov et al., 2009; Roslind and Johansen, 2009). site of the enzyme was removed. However, these genes were still 626
563 For example, CHI3L1 plasma level may be used to estimate the severity selectively maintained for their (previously) side activities, giving rise 627
P
564 of preeclampsia (Seol et al., 2009), to evaluate the prognosis of chronic to new non-enzymatic proteins with regulatory functions. Other exam- 628
565 heart failure (Bilim et al., 2010), or to monitor the therapeutic response ples of such dead enzymes with regulatory functions have also been 629
566 of psoriasis (Imai et al., 2011). A limitation to this strategy is that in identied (Adrain and Freeman, 2012). Since young proteins evolve
D 630
567 many cases the plasma concentration of the chi-lectin does not directly more quickly than old proteins (Vishnoi et al., 2010), it is not surprising 631
568 correlate with the clinical parameters of the disease under investigation that the number and diversity of chi-lectin genes in mammalian 632
569 (Lebensztejn et al., 2007; Mathiasen et al., 2011). It may also be possible genomes appear to be higher than their active counterparts (refer to 633
E
570 to use chi-lectins as diagnostic biomarkers. However, since chi-lectins Section 7). 634
571 are overexpressed in a wide range of inammatory and oncogenic In recent years, chitinase research has made fast progress especially 635
T
572 pathologies, they are of little diagnostic value when used alone. The at molecular levels and chitinolytic activity, once considered to be 636
573 sensitivity and selectivity of diagnosis can be increased by measuring limited to GH18 and GH19 families, and has been identied in other 637
C
574 a panel of biomarkers at the same time (Chang et al., 2009). Chang GH families suggesting that the diversity of chitinases may be greater 638
575 et al. (2009) have developed a multiplex proximity ligation assay than previously anticipated. In a foreseeable future, with the elucidation 639
576 using three biomarkers (CHI3L1, osteopontin, and carbohydrate antigen of the different mechanisms through which they exert their physiolog- 640
E
577 19-9) for the diagnosis of pancreatic cancer. In another study, a similar ical effects, chitinases and chi-lectins may found several medical, phar- 641
578 approach was used to improve the accuracy of ovarian cancer diagnosis maceutical, and agricultural applications. As discussed in Section 7, 642
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579 (Fredriksson et al., 2008). Further studies are required before these chi-lectins can potentially be used as biomarkers for the diagnosis of 643
580 methods can be exploited in clinic. different types of cancers or for the evaluation of the therapeutic 644
response and prognosis of several diseases in humans. Chitinase- 645
R
581 8. Concluding remarks producing microorganisms, on the other hand, have successfully been 646
exploited in the treatment of veterinary parasites (Section 4). The 647
O
582 Chitinases and/or chi-lectins are ubiquitous proteins that are widely possibility of the direct application of parenteral chitinase preparations 648
583 distributed among all kingdoms of life. These proteins take part in a in the treatment of systemic fungal infections has also been investigated 649
584 wide range of physiological processes including nutrition, morphogen- and promising results have been achieved (van Eijk et al., 2005). Alter- 650
C
585 esis, pathogenesis, parasitism, growth regulation, and immunity. In natively, it may be possible to control fungal infections using chitinase 651
586 microorganisms, they are primarily involved in the metabolism of inhibitors such as methylxanthines (Tsirilakis et al., 2012). However it 652
N
587 chitin, both endogenous (e.g. in fungi) and exogenous (e.g. in bacteria). should be noted that these compounds may not be effective against all 653
588 However, in higher organisms, their regulatory function seems to be known fungal pathogens. Chitinases can also be used in the biocontrol 654
589 dominant. This is especially true for mammals since, as stated in of plant pathogens and insect vectors of human diseases as described 655
U
590 Section 7, preliminary evidence suggests that mammalian chitinases in Sections 6 and 4, respectively. Finally, chitinases have been utilized 656
591 do not directly participate in defense against chitinous pathogens. A in the production of neoglycoproteins (Li et al., 2008) and synthetic 657
592 similar argument can be made for plants. Although plant chitinases polysaccharides (Faijes and Planas, 2007). Neoglycoproteins are valu- 658
593 are classied as PR proteins, it is not clear whether their increased able tools for structure-function studies (Kent, 2004) while synthetic 659
594 expression in response to infections is a pathogen-specic process or polysaccharides offer promising opportunities for the development of 660
595 it simply reects a general stress-induced response in which chitinases prophylactic and therapeutic agents (Boltje et al., 2009). From an indus- 661
596 act as signaling intermediates (refer to Section 6). In this context, it is trial viewpoint, screening alternative sources such as extreme habitats 662
597 tempting to look at chitinases as living examples of gene evolution. for chitinolytic enzymes may be advantageous as related glycosyl 663
598 This idea becomes particularly attractive when we consider that hydrolases obtained from extremophiles often demonstrate superior 664
599 the acquisition of (new) regulatory functions by chitinases can be characteristics when catalytic reactions are performed under non- 665
600 explained by both the mutation during non-functionality (MDN) and physiologic conditions such as high salinity and low water activity 666
601 innovation, amplication, and divergence (IAD) models of gene evolu- (Karan et al., 2012; Moshfegh et al., 2013; Niknejad et al., 2013). This 667
602 tion (Bergthorsson et al., 2007). Both models are based on the assump- may also be the case for chitinases. For example, such conditions may 668
603 tion that new genes always emerge from duplicated genes. The MDN be encountered in cases where chitinases are used as biocontrol agents 669
670 (Barranco-Florido et al., 2002). Similarly, thermostable chitinases may Busby JN, Landsberg MJ, Simpson RM, Jones SA, Hankamer B, Hurst MR, et al. Structural 751
analysis of Chi1 chitinase from Yen-Tc: the multisubunit insecticidal ABC toxin 752
671 offer considerable advantages for the production of oligosaccharides at complex of Yersinia entomophaga. J Mol Biol 2012;415:35971. 753
672 high temperature and low pH (Hobel et al., 2005). Bussink AP, van Eijk M, Renkema GH, Aerts JM, Boot RG. The biology of the Gaucher cell: 754
the cradle of human chitinases. Int Rev Cytol 2006;252:71128. 755
Bussink AP, Speijer D, Aerts JM, Boot RG. Evolution of mammalian chitinase(-like) 756
members of family 18 glycosyl hydrolases. Genetics 2007;177:95970. 757
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675 chitooligosaccharides and their potential applications in medicine. Mar Drugs Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate- 761
676 2010;8:1482517. Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids 762
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678 by iRhoms. Nat Rev Mol Cell Biol 2012;13:48998. Chandler JC, Molins CR, Petersen JM, Belisle JT. Differential chitinase activity and produc- 764
679 Adrangi S, Faramarzi MA, Shahverdi AR, Sepehrizadeh Z. Purication and characterization tion within Francisella species, subspecies, and subpopulations. J Bacteriol 2011;193: 765
680 of two extracellular endochitinases from Massilia timonae. Carbohydr Res 2010;345: 326575. 766
681 4027. Chang ST, Zahn JM, Horecka J, Kunz PL, Ford JM, Fisher GA, et al. Identication of a 767
682 Agapov E, Battaile JT, Tidwell R, Hachem R, Patterson GA, Pierce RA, et al. Macrophage biomarker panel using a multiplex proximity ligation assay improves accuracy of 768
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687 isolated: Aeromonas sp. Biotechnology 2008;7:26672. Chaudhuri S, Bruno JC, Alonzo III F, Xayarath B, Cianciotto NP, Freitag NE. Contribution of 773
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690 Paenibacillus chitinolyticus JK2 from Iran. Res J Microbiol 2008;3:395404. Colussi PA, Specht CA, Taron CH. Characterization of a nucleus-encoded chitinase from the 776
691 Alipour M, Suntres ZE, Lafrenie RM, Omri A. Attenuation of Pseudomonas aeruginosa yeast Kluyveromyces lactis. Appl Environ Microbiol 2005;71:28629. 777
692 virulence factors and biolms by co-encapsulation of bismuth-ethanedithiol with Consoli FL, Brandt SL, Coudron TA, Vinson SB. Host regulation and release of parasitism- 778
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695 L.) resistance against fungal diseases through stacking of two antifungal genes Correale J, Fiol M. Chitinase effects on immune cell response in neuromyelitis optica and 781
696 (chitinase and glucanase). GM Crops 2011;2:1049. multiple sclerosis. Mult Scler 2011;17:52131. 782
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697 Aminuddin F, Akhabir L, Stefanowicz D, Pare PD, Connett JE, Anthonisen NR, et al. Genetic Cottrell MT, Wood DN, Yu L, Kirchman DL. Selected chitinase genes in cultured and 783
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721 family in invertebrates. FEBS Lett 2005;579:682733. glycosynthases. Carbohydr Res 2007;342:158194. 807
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723 continuous selection. Proc Natl Acad Sci U S A 2007;104:170049. bassiana strains overexpressing an engineered chitinase. Appl Environ Microbiol 809
724 Bhatnagar RK, Arora N, Sachidanand S, Shahabuddin M, Keister D, Chauhan VS. Synthetic 2007;73:295302. 810
725 propeptide inhibits mosquito midgut chitinase and blocks sporogonic development Fang W, Leng B, Xiao Y, Jin K, Ma J, Fan Y, et al. Cloning of Beauveria bassiana chitinase 811
726 of malaria parasite. Biochem Biophys Res Commun 2003;304:7837. gene Bbchit1 and its application to improve fungal strain virulence. Appl Environ 812
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JBA-06743; No of Pages 10

Biotechnology Advances xxx (2013) xxxxxx

Contents lists available at ScienceDirect

1 Research review paper

2Q2 From bacteria to human: A journey into the world of chitinases

37 2. Classication, structure and catalytic mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

46 1. Introduction chains. Chitinolytic enzymes are produced by a wide range of organisms 54

0734-9750/$ see front matter 2013 Published by Elsevier Inc.

t1:3 Family Catalytic mechanism Proton donor Base/nucleophile Structure Reference

parasites through a complex sequence of events (Owhashi et al., 384

Opin Biotechnol 2004;15:60714. 2011;25:124.

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