Mouse Cell Surface Antigens: Nomenclature and Immunophenotyping

This information is current as of May 30, 2010 Lily Lai, Noosheen Alaverdi, Lois Maltais and Herbert C. Morse, III J. Immunol. 1998;160;3861-3868 http://www.jimmunol.org/cgi/content/full/160/8/3861 References This article cites 54 articles, 28 of which can be accessed free at: http://www.jimmunol.org/cgi/content/full/160/8/3861#BIBL 15 online articles that cite this article can be accessed at: http://www.jimmunol.org/cgi/content/full/160/8/3861#otherarticles Subscriptions Permissions Email Alerts Information about subscribing to The Journal of Immunology is online at http://www.jimmunol.org/subscriptions/ Submit copyright permission requests at http://www.aai.org/ji/copyright.html Receive free email alerts when new articles cite this article. Sign up at http://www.jimmunol.org/subscriptions/etoc.shtml

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The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 9650 Rockville Pike, Bethesda, MD 20814-3994. Copyright 1998 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606.

Mouse Cell Surface Antigens: Nomenclature and Immunophenotyping1

Lily Lai,* Noosheen Alaverdi,* Lois Maltais, and Herbert C. Morse III2
This paper reviews cell surface Ags expressed on mouse hemopoietic and nonhemopoietic cells. The review will cover molecules included in the cluster of differentiation (CD) from CD1 to CD166 and lymphocyte Ag (Ly) series from Ly-1 to Ly-81 as well as some new Ags without current CD or Ly assignments. In addition to an update on mouse nomenclature, there will be a discussion of some known functions of the molecules and brief comments on the use of particular Ags for immunophenotyping of cell subsets. Several novel markers mentioned may prove useful in mouse immunology research. The Journal of Immunology, 1998, 160: 38613868.

olecules on the surface of hemopoietic cells play important roles in the development and function of these cells and have permitted us to understand the immune system in increasingly great depth. In recent years, it has become clear that there is a considerable amount of cross-talk between cells of the hemopoietic system and nonhemopoietic cells, with much of this interplay mediated by cell surface molecules. This review includes a discussion of cell surface Ags expressed on both hemopoietic and nonhemopoietic cells. In addition to an update on nomenclature, there will be a discussion of functions of the molecules, when known, and brief comments on the use of particular Ags for immunophenotyping cell subsets. The review will cover molecules included in the cluster of differentiation (CD)3 and lymphocyte Ag (Ly) series as well as some new Ags without current CD or Ly assignments. As discussed in previous reviews (1, 2), there is a need for unifying mouse and human nomenclature to facilitate communication between researchers studying these species. For mice, the Ly nomenclature was originally devised to classify genes identied through serologic studies of inbred strains; for humans, the CD nomenclature originates from mAb reactivity to human Ags. Human leukocyte differentiation Ag (HLDA) workshops assign each CD based on the same reactivity to one human Ag by at least two mAbs; provisional CDw are sometimes given to clusters not well characterized or represented by only one mAb (3). The Sixth HLDA Workshop, which took place in 1996, resulted in the assignment of novel CDs with new designations spanning CD131 to CD166. mAb submitted to the workshop are tested by laboratories participating in the following sections: T cell, B cell, NK cell, adhesion, endothelial, myeloid, nonlineage, platelet, cytokine re-

*PharMingen, San Diego, CA 92121; Nomenclature Coordinator/Mouse Genome, The Jackson Laboratory, Bar Harbor, ME 04609; and Laboratory of Immunopathology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892 Received for publication September 26, 1997. Accepted for publication December 24, 1997. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1 The Mouse Genome Database Project is supported by National Institutes of Health Grant HG00330. 2 Address correspondence and reprint requests to Dr. Dr. Herbert C. Morse III, Laboratory of Immunopathology, National Institute of Allergy and Infectious Diseases, Building 7, Room 304, National Institutes of Health, Bethesda, MD 20892 0760.

ceptor, and blind (multilineage panels). More information can be obtained from the HLDA website (http://mol.genes.nig.ac.jp/hlda) or Protein Reviews on the worldwide web (http://www.ncbi.nlm. nih.gov/prow). Over the years, the Committee on Standardized Genetic Nomenclature for Mice has continued to assign new Ly and CD names to novel genes and Ags. Since the last update (2), many new Ly designations have been assigned; for example, the F4/80 Ag, whose gene has recently been cloned, was given the designation Ly-71. (See Table I for an update of the Ly nomenclature.) The human homologues of a number of mouse Ags or genes, including members of the Ly-6 and Ly-49 families, have not yet been denitively identied. When a mouse Ly Ag is identied as a human CD homologue, the Ly number for the molecule is withdrawn and reassigned the appropriate CD number. If the mouse molecule was encoded by a gene that is assigned a Ly number, that gene name is withdrawn and reassigned a Cd number, unless another gene name was agreed on by the human and mouse nomenclature groups. As one example, the Ly-5 molecule of the mouse, encoded by Ly5, was assigned CD45 in the human nomenclature for Ags and the gene name CD45. The mouse designations were changed to CD45 for the Ag and, initially, Cd45 for the gene. More recently, the human and mouse nomenclature committees adopted the gene Ptprc for the genes encoding CD45 in both species. Multiple studies, including biochemical analysis, cloning, functional, and immunologic assays, are necessary to conrm homologues between species. In addition to differences in DNA sequence, evolutionary divergence between mice and humans may also be manifested in Ag distribution. Notable examples include CD2, CD90 (Thy-1), and perhaps CD34. Table II reects several novel mouse CD homologues that have been identied via cloning, Abs, or protein probes, such as the use of ligand-Ig fusion proteins. Some molecules are particularly useful as phenotyping markers for different cell subpopulations. The large number of well-characterized mAbs has facilitated identifying cell types based on their surface phenotypes. For additional reference, a review of mAbs to human and murine CD Ags has been made available (4). It should be noted that only a few Ags have restricted lineage distributions; most cell surface molecules exhibit a broader distribution than initially reported. Multiparameter immunoanalysis, therefore, is required to isolate different cell types. Below is a summary of relevant Ags associated with cell lineages. B cells In the mouse, one of the most commonly used pan-B cell markers is identied by the mAb RA3-6B2 (CD45R/B220); however, this
0022-1767/98/$02.00

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Abbreviations used in this paper: CD, cluster of differentiation; Ly, lymphocyte antigen; HLDA, human leukocyte differentiation antigen; KIR, killing inhibitory receptor; DC, dendritic cell. Copyright 1998 by The American Association of Immunologists

3862
Table I. Mouse Ly molecules a
Ly Status Current CD Previous Designation Gene Symbol

MOUSE CELL SURFACE Ags

Chromosome

Ly-1 Ly-2 Ly-3 Ly-4 Ly-5 Ly-6A Ly-6B Ly-6C Ly-6D Ly-6E Ly-6F Ly-6G Ly-7 Ly-8 Ly-9 Ly-10 Ly-11 Ly-12 Ly-13 Ly-14 Ly-15 Ly-16 Ly-17 Ly-18 Ly-19 Ly-20 Ly-21 Ly-22 Ly-23 Ly-24 Ly-25 Ly-26 Ly-27 Ly-28 Ly-29 Ly-30 Ly-31 Ly-32 Ly-33 Ly-34 Ly-35 Ly-36 Ly-37 Ly-38 Ly-39 Ly-40 Ly-41 Ly-42 Ly-43 Ly-44 Ly-45 Ly-46 Ly-47 Ly-48 Ly-49A Ly-49B Ly-49C Ly-49D Ly-49E Ly-49F Ly-49G Ly-49H Ly-49I Ly-50 Ly-51 Ly-52 Ly-53 Ly-54 Ly-55 Ly-56 Ly-57 Ly-58 Ly-59 Ly-60

Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn

CD5 Cd8a CD8b CD4 CD45

Ly-35

TAP, Sca-1, Ly-6D ThB, Ly-61 TSA-1, Sca-2, Ly-67

Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn

CD98 CD5 CD11a CD16/32 CD72 CD11a CD62L CD44 Ly-m18 Ly-m19, Lyb-2 Ly-22a Allele of Ly-15, LFA-1 L-selectin, MEL-14 Pgp-1 Ly-6 Allele of Ly-1 LFA-1 Ly-18

Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn

CD72 CD8a CD2 CD1d CD11b CD23 CD25 CD20 CD54 CD43

Lyb-2 Allele of Ly-2

Mac-1 Fc RIIa IL-2Ra

ICAM-1 leukosialin A1 5E 6

LGL-1 Fc RI, high afnity 6C3/BP-1 HSA B7-1 mb-1, lg NKR-P1A CTLA-4 Lyw-57 B7-2 NK1.1, NKR-P1C ICAM-2

CD24a CD80 CD79a CD161 CD152 CD86 CD102

Cd5 Cd8a CD8b CD4 Ptprc Ly6a Ly6b Ly6c Ly6d Ly6e Ly6f Ly6g Ly7 Ly8 Ly9 CD98 Ly11 Cd5 Ly13 Ly14 Itgal Ly16 Fcgr2b Ly18 Cd72 Ly20 Itgal Sell Ly23 CD44 Ly25 Ly26 Ly6 Ly28 Ly29 Ly30 Ly31 Cd72 Ly33 Ly34 Cd8a Ly36 Cd2 Cd1d Ly39 Itgam Npps Fcer2a IL2ra Cd20 Ly45 Ly46 Icam1 Spn Klra1 Klra2 Klra3 Klra4 Klra5 Klra6 Klra7 Klra8 Klra9 Fcer1g Enpep Cd24a Cd80 Cd79a Klrb1 Cd152 Ly57 CD86 Klrb3 Icam2

19 6 6 6 1 15 15 15 15 15 15 15 16 Unknown 1 19 2 19 Unknown 7 7 12 1 12 4 4 7 1 2 2 2 Unknown 15 13 4 Unknown 4 4 1 13 6 6 3 3 17 Unknown 10 8 2 19 Unknown Unknown 9 7 6 6 6 6 6 6 6 6 6 1 3 10 16 7 6 1 19 16 6 11

Continued

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The Journal of Immunology

Table I. continued
Ly Status Current CD Previous Designation Gene Symbol Chromosome

3863

Ly-61 Ly-62 Ly-63 Ly-63L Ly-64 Ly-65 Ly-66 Ly-67 Ly-68 Ly-69 Ly-70 Ly-70L Ly-71 Ly-72 Ly-72L Ly-73 Ly-74 Ly-75 Ly-76 Ly-77 Ly-78 Ly-79 Ly-80 Ly-81 Lyb-2 Lyb-3 Lyb-4 Lyb-5 Lyb-6 Lyb-7 Lyb-8
a

Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn Withdrawn

CD154 CD136 CD157

CD134 CD135

ThB gp39 4-1BB 4-1BB ligand 14/A10 BP-3 LAG3 TSA-1, Sca-2 AA4.1 Ly-69 OX-40 OX-40L F4/80 Flk-2/Flt3 Flt3 L Flk-1 Ep-CAM DEC-205 TER-119 GL7 RP-105 33D1 Ly32

Withdrawn

CD72

Withdrawn

CD22

Ly6d Cd401 Cd136 Ly631 Ly64 Bp3 Lag3 Ly6e Ly68 Itgb7 Txgp1 Txgp1l Emr1 Flt3 Flt3l Flk1 Ly74 Ly75 Ly76 Ly77 Ly78 Ly79 Mir Trail CD72 Lyb3 Lyb4 Lyb5 Lyb6 Lyb7 Cd22

15 X 4 17 13 5 6 15 Unknown 15 4 1 17 5 7 5 Unknown Unknown Unknown Unknown Unknown Unknown Unknown Unknown 4 Unknown 4 Unknown 4 12 7

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References for all Ly molecules have been entered into the Mouse Genome Database (http://www.informatics.jax.org).

epitope is also expressed on activated T and NK cells (5) and NK cell progenitors (6). The CD19 Ag appears to be more restricted to the B cell lineage and is not expressed by NK progenitor cells (6) or by LAK cells (N. Alaverdi, unpublished observation). Hence, Abs to mouse CD19 may be used more reliably to identify B cells. Although the mouse CD20 gene has been cloned (7), no mAb has been reported. While surface IgM and IgD are expressed by both conventional (B-2) and unconventional (B-1) B cells, the expression of CD23 (8), CD5, and CD11b (9) can be used to distinguish these subsets. Other markers identifying the B cell lineage and its subsets include CD138 (Syndecan-1) (10), CD157 (BP-3) (11, 12), CD35 and CD21 (13), CD40 (14), CD72 (15), CD22 (16), Ly-68 (AA4.1) (17), and Ly-78 (RP-105) (18, 19). CD86 (B7-2) and CD80 (B7-1), although broadly expressed on APCs other than B cells, are useful markers for activated B cells. T cells While mAbs to Thy-1 (CD90) and TCR complex Ags have commonly been used as pan-T cell markers in mice, Thy-1 is not restricted to T cells, while CD3e expression is correlated with T cell maturation, similar to CD27 (20) and CD28 (21). In humans, CD2, CD5, and CD7 are preferred pan-T cell markers, although they are also expressed on subsets of other cell types (3). The mouse CD7 gene has been cloned recently (22); its Ag distribution remains to be determined. The CD8 and CD4 molecules are generally used for identication of mainstream helper and cytotoxic T cells, respectively. A third class of T cells with both helper and cytotoxic properties has been identied using the CD161c (NK1.1, previously Ly-59 or NKR-P1C) (23). Reported memory T cell markers include CD44 (24), CD62L (25), and CD45RB (26). Activated T cell markers include CD26, CD27, CD30, CDw137 (4-1BB),

CD152 (CTLA-4), CD154 (gp39), CD134 (OX-40), CD95L (Fas ligand), CD45R/B220, and Ly-6E (TSA, sca-2) (27). NK cells The ofcial mouse and human genetic nomenclature for a substantial number of the surface molecules expressed by NK cells will, most likely, soon be changed by consensus of those expert in the eld. The provisional symbol for both the mouse and human nomenclature relating to the lectin-like molecules would be Klr, for killer cell lectin-like receptor. This will be followed by the letters a through e to designate ve distinct families and then a number to specify each member of that family: Klra# will be used for the Ly49 family, Klrb# for the NKR-P1 family, Klrc# for the NKG2 family, klrd# for CD94 and related genes, and klre# for the MKAP family. The Klra and Klre families have no human members to date. The CD161c (NK1.1 Ly-59, NKR-P1C) Ag is the most widely used pan-NK marker in mice. Since its expression is restricted to CE, New Zealand Black, and C57BL/6-related strains, many commonly used strains do not express the Ag. In addition, like many NK cell markers, CD161c is also expressed on a subset of T cells (23). Although CD56 (NCAM (neural cell adhesion molecule)) is used as the human NK cell marker, several existing Abs to mouse CD56 did not react with mouse NK cells (3); however, a novel mAb, DX5, exhibits similar reactivity to anti-CD161c Ab but reacts with NK cells in all strains of mice tested, including NK1.1negative strains (L. Lanier, unpublished observation). CD122 (IL-2R -chain), which is constitutively expressed on NK cells and a subset of T cells, can also be used to identify NK cells (V. Kumar, unpublished observation). A multitude of genes encoding NK receptors, such as the newly cloned mouse gene CD94 (L.

3864
Table II. Mouse CD moleculesa
CD/Other name Mouse Gene Symbol Chromosome

MOUSE CELL SURFACE Ags

Comments

CD1d CD2/LFA-2 CD3d CD3e CD3g CD3z CD4/L3T4/Ly-4 CD5/Ly-1 CD6 CD7 CD8a/Ly-2 CD8b/Ly-3 CD9 CD10/CALLA, NEP CD11a/Ly-15, LFA-1 -chain CD11b/Ly-40, Mac-1 -chain CD11c/integrin aX CD12 CD13 CD14 CD15 CD16/Fc R III CD17 CD18/integrin 2 CD19 CD20/Ly-44 CD21/complement receptor-2 CD22/Lyb-8 CD23/Ly-42 CD24a/HSA CD24b CD24c CD25/p55, IL-2R chain CD26/THAM CD27 CD28 CD29/integrin 1, gplla CD30/Ki CD31/PECAM-1 CD32/Ly-17/Fcg receptor II CD33 CD34 CD35/complement receptor-1 CD36 CD37 CD38 CD39 CD40 CD41/integrin llb CD42 CD43/leukosialin, Ly-48 CD44/Pgp-1, Ly-24 CD45/LCA, Ly-5 CD45RA CD45RB CD45RC CD45RO CD45R/B220 CD46 CD47/integrin-associated protein (IAP) CD48/Sgp-60, BCM-1, BLAST-1 CD49a/integrin 1 CD49b/integrin 2 CD49c/integrin 3

Cd1d Cd2 Cd3d Cd3e Cd3g Cd3z Cd4 Cd5 Cd6 Cd7 Cd8a Cd8b Cd9 Mme Itgal Itgam Itgax Not dened Lap1 Cd14 Not dened Fcgr3 Not dened Itgb2 Cd19 Cd20 Cr2 Cd22 Fcer2a Cd24a Cd24b Cd24c Il2ra Dpp4 Cd27 Cd28 Itgb1 Cd30 Pecam Fcgr2 Cd33 Cd34 Cr1 Cd36 Cd37 Cd38 Not dened Cd40 Itga2b Not dened Spn Cd44 Ptprc Ptprc Ptprc Ptprc Ptprc Ptprc Not dened Itgp Cd48 Itga1 Itga2 Itga3

3 3 9 9 9 1 6 19 19 11 6 6 6 3 7 Unknown Unknown 9 18 1 10 7 19 1 7 8 10 8 14 2

Associates with 2m, Ag presentation, ligand for NK1 T cells Ig superfamily, CD49 counter-receptor, adhesion, T cell activation TCR subunit, receptor complex assembly/trafc, signal transduction TCR subunit, receptor complex assembly/trafc, signal transduction TCR subunit, receptor complex assembly/trafc, signal transduction TCR subunit, receptor complex assembly/trafc, signal transduction TCR coreceptor, MHC class II receptor, signal transduction CD72 counter-receptor, regulation of cellular activation T cell activation, thymic development, CD166 counterreceptor Early T cell marker (human) TCR coreceptor, MHC class I receptor, signal transduction TCR coreceptor, MHC class I receptor, signal transduction TM4 superfamily, T cell costimulation Ectoenzyme, neutral endopeptidase, B cell development Associates with CD18, ICAM-1, and ICAM-2 counterreceptor Associates with CD18, brinogen, and C3bi counterreceptor Associates with CD18 Type II transmembrane protein, aminopeptidase N GPI-linked protein, LPS/LBP complex receptor Carbohydrate determinant: Lewis X (human); binds CD62E, CD62L, CD62P Low-afnity binding to IgG, ADCC Carbohydrate determinant: lactosylceramide (human) Adhesion, associates with CD11a, CD11b, CD11c BCR co-receptor, signal transduction, pan B marker B cell activation/differentiation, Type III transmembrane protein Cd 3 receptor, complex with BCR Adhesion, B cell activation Low-afnity receptor for IgE T cell costimulation, adhesion, CD62P counterreceptor

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Low-afnity binding to IL-2 by itself, associates with CD122 and CD132, lymphocyte differentiation and activation 2 Ectoenzyme, dipeptidyl peptidase, cellular activation 6 TNFR superfamily, T cell costimulation, CD70 counterreceptor 1 T cell costimulation, CD80 and CD86 counterreceptor Unknown VLAb, associates with CD49a, b, c, d, e, or f, adhesion 4 TNFR superfamily, T cell activation/regulation 6 Adhesion, signal transduction; counterreceptor to CD38 1 Low-afnity binding to IgG, ADCC 7 1 Multiple isoforms, CD62L counterreceptor (90 kD), hemopoiesis (human) 1 C3b receptor, phagocytosis 5 Thrombospondin receptor; oxidixed LDL receptor; collagen receptor 7 5 Ectoenzyme, cyclase/hydrolase, cellular activation, CD31 counterreceptor (human) 2 11 7 2 TNFR superfamily, B cell activation/differentiation/survival CD154 (gp39) counterreceptor Associates with integrin 3, adhesion; platelet marker

Two isoforms; adhesion, signal transduction, binding to CD54 Receptor for hyaluronate, adhesion, homing, metastasis, T cell activation, marker for memory T cells 1 Cellular differentiation/activation, tyrosine phosphatase pan-leukocyte marker 1 Cellular differentiation/activation, tyrosine phosphatase restricted expression, exon A dependent 1 Cellular differentiation/activation, tyrosine phosphatase restricted expression, exon B dependent 1 Cellular differentiation/activation, tyrosine phosphatase restricted expression, exon C dependent 1 Cellular differentiation/activation, tyrosine phosphatase, marker for naive T cells; restricted expression 1 Cellular differentiation/activation, tyrosine phosphatase, marker for B cells and activated T and NK (LAK) cells Membrane cofactor protein (MCP) Unknown Activation and extravasation of PMN; Ig superfamily 1 13 13 11 GPI-linked protein, T cell costimulation, adhesion, CD2 counterreceptor Associates with CD29, laminin/collagen receptor Associates with CD29, laminin/collagen/bronectin receptor Associates with CD29, laminin/collagen/bronectin receptor
Continued

The Journal of Immunology

Table II. continued
CD/Other name Mouse Gene Symbol Chromosome Comments

3865

CD49d/integrin 4 CD49e/integrin 5 CD49f/integrin 6 CD50/ICAM-3 CD51/integrin aV CD52 CD53 CD54/ICAM-1, Ly-47 CD55 CD56/NCAM-1 CD57 CD58 CD59 CD60 CD61/integrin 3 CD62E/E-selectin, ELAM CD62L/L-selectin, LECAM-1 CD62P/P-selectin, PADGEM CD63 CD64/Fc RI CD65 CD66 CD67 CD68/macrosialin CD69/very early activation Ag CD70 CD71/transferrin receptor CD72/Lyb-2 CD73 CD74/invariant chain CD75 CD76 CD77 CD78 CD79a/Ig CD79b/Ig CD80/B7-1 CD81/TAPA-1 CD82/KAI1 CD83 CD84 CD85 CD86/B7-2 CD87 CD88 CD89 CD90/Thy-1 CD91/ 2 macroglobulin receptor CD92 CD93 CD94 CD95/Fas CD96 CD97 CD98/4F2, Ly-10 CD99 CD100 CD101 CD102/ICAM-2 CD103/integrin IEL CD104/integrin 4 CD105/endoglin CD106/VCAM-1 CD107a/LAMP-1 CD107b/LAMP-2 CDw108 CDw109 CD110 CD111 CD112 CD113 CD114

Itga4 Itga5 Itga6 Icam3 Itgav Not dened Cd53 Icam1 Daf1 Ncam Not dened Not dened Cd59 Not dened Itgb3 Sele Sell Selp Cd63 Fcgr1 Not dened Not dened Cd68 Cd69 Cd70 Trfr Cd72 Nt5 Ii Not dened Not dened Not dened Not dened Cd79a Cd79b Cd80 CD81 Cd82 Cd83 Not dened Not dened Cd86 Not dened Not dened Not dened Thy1 Lrp Not dened Not dened Not dened Fas Not dened Not dened Cd98 Not dened Not dened Not dened Icam2 Itgae Itgb4 Eng Vcam1 Lamp1 Lamp2 Not dened Reserved Reserved Reserved Reserved Not dened

2 15 2 Unknown 2 3 9 1 9 2 11 1 1 1 18 3

Associates with CD29 Associates with CD29, bronectin/laminin receptor Associates with CD29, laminin receptor Adhesion/signaling Associates with integrins, vitronectin and bronectin receptor Campath (human) Adhesion, T cell costimulation, CD11a, CD11b, and CD43 counterreceptor Adhesion, nervous system HNK1 (human) LFA-3 (human) Associates with CD41 and CD51, extracellular adhesion Adhesion, leukocyte rolling/migration, binds to sialyl Lewis X (CD15) Adhseion, leukocyte rolling/migration, binds to sialyl Lewis X (CD15) CD34 counterreceptor Adhesion, leukocyte rolling/migration, binds to CD15 and CD24 Platelet activation Ag (TM4 superfamily) High-afnity binding to IgG, ADCC Ceremide dodecasaccharide (human)

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Withdrawn, now CD66b Unknown Type I transmembrane, lysosomal-associated protein 6 Leukocyte activation; early lymphocyte activation marker CD27 counter-receptor Unknown Type II transmembrane protein, activation, iron metabolism 4 Cd5 counter-receptor, B cell costimulation Ecto-5 nucleotidase; B and T cell subsets (human) 18 MCH class II folding/trafcking, Ag presentation

7 Unknown 16 7 2 Unknown 16

Ig superfamily, signal transduction Ig superfamily, signal transduction B cell costimulation, T/B interaction CD28 and CE152 counterreceptor TM4 superfamily, signal transduction, T cell costimulation TM4 superfamily, signal transduction, T cell costimulation Marker for dendritic and activated T and B (human; mouse cloned, no mAb) B cell costimulation, T/B interactions, CD28 and CD152 counterreceptor C5a receptor (human) Receptor for IgA GPI-linked transmembrane protein, signal transduction, T cell activation Lipoprotein metabolism NK cell receptor for HLA-class I molecules TNFR superfamily apoptosis, T cell costimulation, lpr mutation Ig superfamily, T cell activation, increased late expression Cellular activation, calcium ux V7 glycoprotein, Ig superfamily, CD3-dependent T cell activation (human) Ig superfamily, adhesion to CD11a Associates with integrin 7, adhesion Associates with integrin 6, adhesion Adhesion, ligand for TGFSignaling, adhesion to CD49d/CD29 (VLA-4) Lysosomal-associated membrane protein, adhesion/metastasis Lysosomal-associated membrane protein, adhesion/metastasis Sialomucin

9 15

19 19

11 Unknown 11 2 3 8 X

Continued

3866
Table II. continued
CD/Other name Mouse Gene Symbol Chromosome

MOUSE CELL SURFACE Ags

Comments

CD115/M-CSFR, CSF-1R CD116 CD117/c-KIT, steel factor receptor receptor CD118/IFNCD119/IFN- receptor CD120a/TNF receptor -chain CD120b/TNF receptor -chain CD121a/IL-1 receptor -chain CD121b/IL-1 receptor -chain CD122/IL-2 receptor -chain CD123/IL-3 receptor -chain CD124/IL-4 receptor -chain CD125/IL-5 receptor -chain CD126/IL-6 receptor -chain CD127/IL-7 receptor -chain CD128/IL-8 receptor -chain CD129 CD130/gp 130 CDw131/common -chain CD132/common -chain CD133 CD134/OX-40, Ly-70 CD135/Flk-1/t3, Ly-72 CD136/4-1BB, Ly-63 CD137/MSPR, RON CD138/syndecan-1 CD139 CD140a/PDGF-R -chain CD140b/PDGF-R -chain CD141/thrombomodulin CD142 CD143 CD144/VE-cadherin CDw145 CD146/MUC 18/s-endo CD147/neurothelin, basigin CD148/M4, M56 CD149/MEM-133 CDw 150/IPO-3; SLAM CD151/PETA CD152/CTLA-4, Ly-56 CD153/CD30 ligand CD154/CD40 ligand (gp39), Ly-62 CD155 CD156/ADAM8 CD157/BST-1, Mo-5, Ly-65 CD158a/p58.1 CD159b/p58.2 CD160 CD161a CD161b CD161c CD162/PSGL-1 CD163 CD164/MGC-24, A115, A25 CD165/Ad2/gp37 CD166/ALCAM
a

Csfmr Csfgmra Kit Ifnar Ifngr 1 Tnfr1 Thfr2 Il1r1 IL1r2 Il2rb II3ra Il4ra Il5ra Il6ra Il7ra Cmkar2 Reserved Il6st II3rb 1/II3rb2 Il2rg Reserved Txgp2 Flt3 Cd136 Not dened Synd-1 Not dened Pdgfra Pdgfrb Thbd Not dened Ace Cdh5 Not dened Bsg Not dened Not dened Not dened Not dened Cd152 Cd153 Cd154 Not dened Cd156 Bp3 Not dened Not dened Reserved Klrb1 Klrb3 Cd162 Not dened Not dened Not dened Cd166

18 19 5 16 13 6 4 1 1 15 14 7 6 3 15 1

Tyrosine kinase receptor family, signal transduction, cell differentiation Receptor for GM-CSF, associates with CDw131 Tyrosine kinase receptor family, signal transduction, cell differentiation, Wr mutation IFNreceptor, signal transduction High-afnity binding to IFN- , signal transduction Type I, TNFR superfamily, signal transduction, apoptosis Type II, TNFR superfamily, signal transduction, apoptosis Ig superfamily, IL-1 binding, signal transduction Ig superfamily, IL-1 binding Associates with CD25 and CD132 for high-afnity binding to IL-2, signal transduction Low-afnity binding to IL-3, associates with CDw131 for high-afnity binding Associates with CD132 for high-afnity binding to IL-4 Low-afnity binding to IL-5, associates with CDw131 for high-afnity binding Low-afnity binding to IL-6, associates with CD130 for high-afnity binding Associates with CD132 for high-afnity binding to IL-7 Binding to mouse MIP-2

Unknown Signal transduction, common chain of IL-6R, IL-11R, LIFR, OSMR 15 Signal transduction, member of IL-3R, IL-5R, and GM-CSFR complexes X Signal transduction, member of IL-2R, IL-4R, IL-7R, IL-13R, and IL-15R complexes 4 5 4 12 5 18 2 Unknown 11 8 10 TNFR superfamily, T cell costimulation Tyrosine kinase receptor family myeloid and lymphoid progenitor development TNFR superfamily, T cell costimulation Receptor for macrophage-stimulating protein (MSP) (human) B cell development/differentiation Tyrosine kinase receptor family, binds to PDGF a and b, signal transduction Tyrosine kinase receptor family, binds only to PDGF b, signal transduction Tissue factor, receptor for cofactor VII (human) Angiotesin converting enzyme Adhesion Pan endothelial marker (dened by mAbs E036, E037) Ig superfamily, blood-brain barrier, expressed on activated leukocytes Ig superfamily, T cell stimulation (human) TM4 family; signaling T cell activation/regulation, CD80 and CD86 counter-receptor TNF family, activated lymphocytes, CD30 counter-receptor TNF family, T cell activation, transient expression Poliovirus receptor (human) Ectoenzyme, B and T cell development NK receptor (human) NK receptor (human) NK cell activation/regulation; NKR-P1A Mouse NK1.1, pan NK marker; NKR-P1C P-selectin ligand protein one P11, P12 (human)

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1 4 X 7 5

CD6 counter-receptor, activated leukocyte-cell adhesion molecule, thymic development, T/B interaction, nervous system (human)

CD1-CD130 are cited in ref. 4; references for CD131CD166 have been entered into the Mouse Genome Database (http://www.informatics.jax.org).

Lanier, unpublished observation), CD161a, and the Klra family members, have been characterized (28). The MHC class I ligands of these NK receptors and their inhibitory or activating functions are being elucidated. To date, no mouse homologues of the killing inhibitory receptor (KIR) and killing-activating receptor (KAR) Ig superfamily members have been discovered, although two mouse genes related to human KIR, gp49A and gp49B (B1 and B2), have been cloned from mouse mast cells (29). The available data sug-

gest that gp49 is unlikely to be the mouse equivalent of human KIR (29). It is likely that Klra family members serve as KIR and KAR functional equivalents in mice (28). Macrophages/monocytes The anti-Ly-71 (F4/80) mAb has been used extensively in determining the distribution and function of mouse tissue macrophages

The Journal of Immunology (30), although eosinophils and dendritic cells (DC) have been reported to react with this mAb (31, 32). To date, no human homologue of Ly-71 (F4/80) has been reported. CD11b (Mac-1), another commonly used marker for the monocyte/macrophage lineage, is expressed on NK cells, granulocytes, a T cell subset, and peritoneal B-1 B cells. CD14 is widely perceived as the best marker for the human macrophage/monocyte population. In mice, the level of CD14, as recognized by an anti-CD14 mAb, rmC53, was low or undetectable on resting blood monocytes. It remains to be determined whether other newly generated Abs to mouse CD14 will recognize a distribution similar to that in humans. Other mAbs used for identication of macrophage/monocyte subsets are MOMA-1, MOMA-2 (33), Mac-2, Mac-3, and the macrophage scavenger receptor. Dendritic cells DC display surface phenotype heterogeneity depending on their microenvironment and state of activation. Their ill-dened surface phenotypes in addition to their low numbers in tissues have made the isolation of these cells rather cumbersome. DC express many adhesion and costimulatory molecules and myeloid lineage markers (32). Although several Ags have been reported to be expressed specically by DC, mAb to these Ags often react with other cell types or only recognize subsets of DC. For separation of DC from other cell types, multicolor analysis or prior enrichment protocols such as plastic adherence methods are necessary. The Ly-75 (DEC-205) Ag (34) and CD11c (35) have proved to be more restricted markers for DC, although they may not be expressed on all DC, and they may also be expressed on other cell types. In humans, CD83 and the Ag identied by mAb CRMF-44 have recently been identied as novel markers for DC (3, 36). Other Abs useful for the identication of DCs include Ly-79 (33D1) (37), 4F7 (38), and Ly-74 (Ep-CAM, gp40), a homologue of human epithelial growth factor (39). Granulocytes Expression of Ly-6G is reported to be primarily limited to granulocytes; mAbs specic to this molecule, also known as the Gr-1 Ag, have been used successfully to separate mouse granulocyte lineage cells (40). Erythroid cells The Ly-76 Ag detected by the mAb TER-119 has been used to identify cells of the erythroid lineage (41, 42). Endothelial cells MECA-32 appears to be most restricted marker for endothelium (43). Other Ags expressed by endothelial cells include CD106 (vascular cell adhesion molecule-1), CD31, CD34, Ly-73 (Flk-1), and CD105. CD62E is expressed by activated endothelial cells (27, 44). Platelets CD41 (integrin IIb) is the best marker for platelets; other surface proteins expressed by platelets include CD61 (integrin 3) (45) and CD9 (46). Activated platelets express CD62P (27). Progenitor cells The classic method for identifying mouse stem/pluripotent cells in total bone marrow cells has included the use of a combination of Abs; cells negative for lineage markers CD4, CD8, CD11b (Mac1), CD45/B220, Ly-6G (Gr-1), and Ly-76 (Ter-119) and positive for CD117 (c-kit), and Ly-6A (Sca-1), which are greatly enriched for capacity to reconstitute hemopoiesis (47, 48). Polyclonal and

3867 monoclonal Abs to mouse CD34 (49 50) have demonstrated that CD34 is expressed on a small subset of bone marrow cells. In humans, the stem cell populations are identied by the expression of CD34. A recent report with one anti-mouse CD34 mAb, 49E8 (RAM34), however, suggests that primitive hemopoietic stem cells capable of long term repopulation are contained in the CD34-negative/low fraction, whereas the CD34-positive cells are committed progenitor cells lacking self-renewal capability (51). Other relevant Ags expressed by progenitor cells include CD25, CD90 (Thy1), ER-MP12 (52), CD135 (Flk-2/Flt-3) (53), Ly-6E (TSA-1, Sca-2) (54), Ly-51 (BP-1, 6C3), and CD157 (BP-3). Activation Ags An important feature of cellular activation is the de novo expression of surface molecules or up-regulation of the Ags expressed constitutively. The mode of stimulation, kinetics, and expression pattern of any given marker may imply its role in the immune response. Surface molecules, including CD71 (transferrin receptor), CD98 (4F2), and CD69, are expressed by a wide range of activated cell types, reecting their general role in cellular proliferation. CD69 is useful as a lymphocyte activation marker because of its expression in the very early stage of activation (55). It is noteworthy that although some markers were initially dened to be restricted to specic types of activated cells, their distributions were subsequently found to be more general. For example, CD25 (IL-2R -chain), often used as a T cell activation marker, is present on activated T, B, and NK cells and is expressed during ontogeny on pre-B and pre-T cells. CD80 and CD86, initially reported as B cell activation markers, are constitutively expressed by macrophages, DCs, and broblasts and can be induced on activated T cells (56, 57). Further, sensitivity of the detection method may be a limiting factor when studying low density Ags. Other molecules reported to be expressed by activated lymphocytes include CD152 (CTLA-4), CDw137 (4-1BB), CD134 (OX-40), DATK44 Ag (TABS), Ly-77 (GL7), CD45R (B220), CD30, CD95 ligand, CD43, Ly-6 family members, CD106, cytokine receptors, and the family of very late Ag adhesion molecules. In this communication, we provide an update on mouse cell surface molecules, including lists of surface markers that, in combination with multiparameter ow cytometric analysis, can be used to trace cell lineages and activation state. Several novel markers mentioned here may prove useful in mouse immunology research. Most of the reported mAbs and their respective Ags are compiled in the CD and Ly charts. Undoubtedly, many molecules have not been included here. Scientists are encouraged to contact the authors and the Committee on Standardized Genetic Nomenclature for Mice to submit novel molecules for their inclusion in the future reports. In addition to this communication, information on the mouse genome and genetic markers is available on the worldwide web. The Mouse Genome Database can be accessed via http:// www.informatics.jax.org. Information on germ-line disruptions of Ly/CD-encoding loci can be obtained at www.bioscience.org/ knockout/knochome.htm or TBASE at www.gdb.org/dan/tbase.html.

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Acknowledgments
We thank M. A. Reyes and Drs. C. Shih, K. Holmes, and V. Kumar for their helpful assistance with this manuscript, and B. R. Marshall for excellent editorial assistance.

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