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Mouse Cell Surface : Nomenclature and Immunophenotyping1

Lily Lai,* Noosheen Alaverdi,* Lois Maltais,† and Herbert C. Morse III2‡

This paper reviews cell surface Ags expressed on hemopoietic and nonhemopoietic cells. The review will cover molecules included in the cluster of differentiation (CD) from CD1 to CD166 and 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 research. The Journal of Immunology, 1998, 160: 3861–3868. olecules on the surface of hemopoietic cells play im- ceptor, and blind (multilineage panels). More information can be portant roles in the development and function of these obtained from the HLDA website (http://mol.genes.nig.ac.jp/hlda) M cells and have permitted us to understand the immune or Reviews on the worldwide web (http://www.ncbi.nlm. system in increasingly great depth. In recent years, it has become nih.gov/prow). clear that there is a considerable amount of cross-talk between Over the years, the Committee on Standardized Genetic Nomen- cells of the hemopoietic system and nonhemopoietic cells, with clature for Mice has continued to assign new Ly and CD names to much of this interplay mediated by cell surface molecules. This novel and Ags. Since the last update (2), many new Ly review includes a discussion of cell surface Ags expressed on both designations have been assigned; for example, the F4/80 Ag, hemopoietic and nonhemopoietic cells. In addition to an update on whose has recently been cloned, was given the designation nomenclature, there will be a discussion of functions of the mol- Ly-71. (See Table I for an update of the Ly nomenclature.) The ecules, when known, and brief comments on the use of particular homologues of a number of mouse Ags or genes, including Ags for immunophenotyping cell subsets. The review will cover members of the Ly-6 and Ly-49 families, have not yet been de- molecules included in the cluster of differentiation (CD)3 and lym- finitively identified. When a mouse Ly Ag is identified as a human phocyte Ag (Ly) series as well as some new Ags without current CD homologue, the Ly number for the molecule is withdrawn and CD or Ly assignments. reassigned the appropriate CD number. If the mouse molecule was As discussed in previous reviews (1, 2), there is a need for encoded by a gene that is assigned a Ly number, that gene name is unifying mouse and human nomenclature to facilitate communi- withdrawn and reassigned a Cd number, unless another gene name cation between researchers studying these species. For mice, the was agreed on by the human and mouse nomenclature groups. As Ly nomenclature was originally devised to classify genes identified one example, the Ly-5 molecule of the mouse, encoded by Ly5, through serologic studies of inbred strains; for , the CD was assigned CD45 in the human nomenclature for Ags and the nomenclature originates from mAb reactivity to human Ags. Hu- gene name CD45. The mouse designations were changed to CD45 man leukocyte differentiation Ag (HLDA) workshops assign each for the Ag and, initially, Cd45 for the gene. More recently, the CD based on the same reactivity to one human Ag by at least two human and mouse nomenclature committees adopted the gene Pt- mAbs; provisional CDw are sometimes given to clusters not well prc for the genes encoding CD45 in both species. characterized or represented by only one mAb (3). The Sixth Multiple studies, including biochemical analysis, cloning, func- HLDA Workshop, which took place in 1996, resulted in the as- tional, and immunologic assays, are necessary to confirm homo- signment of novel CDs with new designations spanning CD131 to logues between species. In addition to differences in DNA se- CD166. mAb submitted to the workshop are tested by laboratories quence, evolutionary divergence between mice and humans may participating in the following sections: , , NK cell, also be manifested in Ag distribution. Notable examples include adhesion, endothelial, myeloid, nonlineage, , re- CD2, CD90 (Thy-1), and perhaps CD34. Table II reflects several novel mouse CD homologues that have been identified via cloning, Abs, or protein probes, such as the use of ligand-Ig fusion . † *PharMingen, San Diego, CA 92121; Nomenclature Coordinator/Mouse Genome, Some molecules are particularly useful as phenotyping markers The Jackson Laboratory, Bar Harbor, ME 04609; and ‡Laboratory of Immunopathol- ogy, National Institute of Allergy and Infectious Diseases, National Institutes of for different cell subpopulations. The large number of well-char- Health, Bethesda, MD 20892 acterized mAbs has facilitated identifying cell types based on their Received for publication September 26, 1997. Accepted for publication December surface phenotypes. For additional reference, a review of mAbs to 24, 1997. human and murine CD Ags has been made available (4). It should The costs of publication of this article were defrayed in part by the payment of page be noted that only a few Ags have restricted lineage distributions; charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. most cell surface molecules exhibit a broader distribution than ini- 1 The Mouse Genome Database Project is supported by National Institutes of Health tially reported. Multiparameter immunoanalysis, therefore, is re- Grant HG00330. quired to isolate different cell types. Below is a summary of rele- 2 Address correspondence and reprint requests to Dr. Dr. Herbert C. Morse III, Lab- vant Ags associated with cell lineages. oratory of Immunopathology, National Institute of Allergy and Infectious Diseases, Building 7, Room 304, National Institutes of Health, Bethesda, MD 20892–0760. B cells 3 Abbreviations used in this paper: CD, cluster of differentiation; Ly, lymphocyte ; HLDA, human leukocyte differentiation antigen; KIR, killing inhibitory re- In the mouse, one of the most commonly used pan-B cell markers ceptor; DC, . is identified by the mAb RA3-6B2 (CD45R/B220); however, this

Copyright © 1998 by The American Association of Immunologists 0022-1767/98/$02.00 3862 MOUSE CELL SURFACE Ags

Table I. Mouse Ly molecules a

Ly Status Current CD Previous Designation Gene Symbol

Ly-1 Withdrawn CD5 Ly-35 Cd5 19 Ly-2 Withdrawn Cd8a Cd8a 6 Ly-3 Withdrawn CD8b CD8b 6 Ly-4 Withdrawn CD4 CD4 6 Ly-5 Withdrawn CD45 Ptprc 1 Ly-6A TAP, Sca-1, Ly-6D Ly6a 15 Ly-6B Ly6b 15 Ly-6C Ly6c 15 Ly-6D ThB, Ly-61 Ly6d 15 Ly-6E TSA-1, Sca-2, Ly-67 Ly6e 15 Ly-6F Ly6f 15 Ly-6G Ly6g 15 Ly-7 Ly7 16 Ly-8 Ly8 Unknown Ly-9 Ly9 1 Ly-10 Withdrawn CD98 CD98 19 Ly-11 Ly11 2 Ly-12 Withdrawn CD5 of Ly-1 Cd5 19 Ly-13 Ly13 Unknown Ly-14 Ly14 7 Ly-15 Withdrawn CD11a LFA-1 Itgal 7 Ly-16 Ly-18 Ly16 12 Ly-17 Withdrawn CD16/32 Fcgr2b 1 Ly-18 Ly-m18 Ly18 12 Ly-19 Withdrawn CD72 Ly-m19, Lyb-2 Cd72 4 Ly-20 Ly-22a Ly20 4 Ly-21 Withdrawn CD11a Allele of Ly-15, LFA-1 Itgal 7 Ly-22 Withdrawn CD62L L-, MEL-14 Sell 1 Ly-23 Ly23 2 Ly-24 Withdrawn CD44 Pgp-1 CD44 2 Ly-25 Ly25 2 Ly-26 Ly26 Unknown Ly-27 Withdrawn Ly-6 Ly6 15 Ly-28 Ly28 13 Ly-29 Ly29 4 Ly-30 Ly30 Unknown Ly-31 Ly31 4 Ly-32 Withdrawn CD72 Lyb-2 Cd72 4 Ly-33 Ly33 1 Ly-34 Ly34 13 Ly-35 Withdrawn CD8a Allele of Ly-2 Cd8a 6 Ly-36 Ly36 6 Ly-37 Withdrawn CD2 Cd2 3 Ly-38 Withdrawn CD1d Cd1d 3 Ly-39 Ly39 17 Ly-40 Withdrawn CD11b Mac-1 Itgam Unknown Ly-41 Npps 10 Ly-42 Withdrawn CD23 Fc⑀RIIa Fcer2a 8 Ly-43 Withdrawn CD25 IL-2Ra IL2ra 2 Ly-44 Withdrawn CD20 Cd20 19 Ly-45 Ly45 Unknown Ly-46 Ly46 Unknown Ly-47 Withdrawn CD54 ICAM-1 Icam1 9 Ly-48 Withdrawn CD43 leukosialin Spn 7 Ly-49A Withdrawn A1 Klra1 6 Ly-49B Withdrawn Klra2 6 Ly-49C Withdrawn 5E 6 Klra3 6 Ly-49D Withdrawn Klra4 6 Ly-49E Withdrawn Klra5 6 Ly-49F Withdrawn Klra6 6 Ly-49G Withdrawn LGL-1 Klra7 6 Ly-49H Withdrawn Klra8 6 Ly-49I Withdrawn Klra9 6 Ly-50 Fc⑀RI, high affinity Fcer1g 1 Ly-51 6C3/BP-1 Enpep 3 Ly-52 Withdrawn CD24a HSA Cd24a 10 Ly-53 Withdrawn CD80 B7-1 Cd80 16 Ly-54 Withdrawn CD79a mb-1, lg␣ Cd79a 7 Ly-55 Withdrawn CD161 NKR-P1A Klrb1 6 Ly-56 Withdrawn CD152 CTLA-4 Cd152 1 Ly-57 Lyw-57 Ly57 19 Ly-58 Withdrawn CD86 B7-2 CD86 16 Ly-59 Withdrawn NK1.1, NKR-P1C Klrb3 6 Ly-60 Withdrawn CD102 ICAM-2 Icam2 11

Continued The Journal of Immunology 3863

Table I. continued

Ly Status Current CD Previous Designation Gene Symbol Chromosome

Ly-61 Withdrawn ThB Ly6d 15 Ly-62 Withdrawn CD154 gp39 Cd401 X Ly-63 Withdrawn CD136 4-1BB Cd136 4 Ly-63L 4-1BB ligand Ly631 17 Ly-64 14/A10 Ly64 13 Ly-65 Withdrawn CD157 BP-3 Bp3 5 Ly-66 LAG3 Lag3 6 Ly-67 Withdrawn TSA-1, Sca-2 Ly6e 15 Ly-68 AA4.1 Ly68 Unknown Ly-69 Ly-69 Itgb7 15 Ly-70 Withdrawn CD134 OX-40 Txgp1 4 Ly-70L OX-40L Txgp1l 1 Ly-71 F4/80 Emr1 17 Ly-72 Withdrawn CD135 Flk-2/Flt3 Flt3 5 Ly-72L Flt3 L Flt3l 7 Ly-73 Flk-1 Flk1 5 Ly-74 Ep-CAM Ly74 Unknown Ly-75 DEC-205 Ly75 Unknown Ly-76 TER-119 Ly76 Unknown Ly-77 GL7 Ly77 Unknown Ly-78 RP-105 Ly78 Unknown Ly-79 33D1 Ly79 Unknown Ly-80 Mir Unknown Ly-81 Trail Unknown Lyb-2 Withdrawn CD72 Ly32 CD72 4 Lyb-3 Lyb3 Unknown Lyb-4 Lyb4 4 Lyb-5 Lyb5 Unknown Lyb-6 Lyb6 4 Lyb-7 Lyb7 12 Lyb-8 Withdrawn CD22 Cd22 7

a 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 CD152 (CTLA-4), CD154 (gp39), CD134 (OX-40), CD95L (Fas cell progenitors (6). The CD19 Ag appears to be more restricted to ligand), CD45R/B220, and Ly-6E (TSA, sca-2) (27). the B cell lineage and is not expressed by NK progenitor cells (6) or by LAK cells (N. Alaverdi, unpublished observation). Hence, NK cells Abs to mouse CD19 may be used more reliably to identify B cells. The official mouse and human genetic nomenclature for a substan- Although the mouse CD20 gene has been cloned (7), no mAb has tial number of the surface molecules expressed by NK cells will, been reported. While surface IgM and IgD are expressed by both most likely, soon be changed by consensus of those expert in the conventional (B-2) and unconventional (B-1) B cells, the expres- field. The provisional symbol for both the mouse and human no- sion of CD23 (8), CD5, and CD11b (9) can be used to distinguish menclature relating to the -like molecules would be Klr, for these subsets. Other markers identifying the B cell lineage and its killer cell lectin-like . This will be followed by the letters subsets include CD138 (Syndecan-1) (10), CD157 (BP-3) (11, 12), a through e to designate five distinct families and then a number to CD35 and CD21 (13), CD40 (14), CD72 (15), CD22 (16), Ly-68 specify each member of that family: Klra# will be used for the (AA4.1) (17), and Ly-78 (RP-105) (18, 19). CD86 (B7-2) and Ly49 family, Klrb# for the NKR-P1 family, Klrc# for the NKG2 CD80 (B7-1), although broadly expressed on APCs other than B family, klrd# for CD94 and related genes, and klre# for the MKAP cells, are useful markers for activated B cells. family. The Klra and Klre families have no human members to date. T cells The CD161c (NK1.1 Ly-59, NKR-P1C) Ag is the most widely While mAbs to Thy-1 (CD90) and TCR complex Ags have com- used pan-NK marker in mice. Since its expression is restricted to monly been used as pan-T cell markers in mice, Thy-1 is not re- CE, New Zealand Black, and C57BL/6-related strains, many com- stricted to T cells, while CD3e expression is correlated with T cell monly used strains do not express the Ag. In addition, like many maturation, similar to CD27 (20) and CD28 (21). In humans, CD2, NK cell markers, CD161c is also expressed on a subset of T cells CD5, and CD7 are preferred pan-T cell markers, although they are (23). Although CD56 (NCAM (neural molecule)) is also expressed on subsets of other cell types (3). The mouse CD7 used as the human NK cell marker, several existing Abs to mouse gene has been cloned recently (22); its Ag distribution remains to CD56 did not react with mouse NK cells (3); however, a novel be determined. The CD8 and CD4 molecules are generally used for mAb, DX5, exhibits similar reactivity to anti-CD161c Ab but re- identification of mainstream helper and cytotoxic T cells, respec- acts with NK cells in all strains of mice tested, including NK1.1- tively. A third class of T cells with both helper and cytotoxic negative strains (L. Lanier, unpublished observation). CD122 properties has been identified using the CD161c (NK1.1, previ- (IL-2R ␤-chain), which is constitutively expressed on NK cells and ously Ly-59 or NKR-P1C) (23). Reported markers a subset of T cells, can also be used to identify NK cells (V. include CD44 (24), CD62L (25), and CD45RB (26). Activated T Kumar, unpublished observation). A multitude of genes encoding cell markers include CD26, CD27, CD30, CDw137 (4-1BB), NK receptors, such as the newly cloned mouse gene CD94 (L. 3864 MOUSE CELL SURFACE Ags

Table II. Mouse CD moleculesa

CD/Other name Mouse Gene Symbol Chromosome Comments ␤ ϩ CD1d Cd1d 3 Associates with 2m, Ag presentation, ligand for NK1 T cells CD2/LFA-2 Cd2 3 Ig superfamily, CD49 counter-receptor, adhesion, T cell activation CD3d Cd3d 9 TCR subunit, receptor complex assembly/traffic, signal transduction CD3e Cd3e 9 TCR subunit, receptor complex assembly/traffic, signal transduction CD3g Cd3g 9 TCR subunit, receptor complex assembly/traffic, signal transduction CD3z Cd3z 1 TCR subunit, receptor complex assembly/traffic, signal transduction CD4/L3T4/Ly-4 Cd4 6 TCR coreceptor, MHC class II receptor, signal transduction CD5/Ly-1 Cd5 19 CD72 counter-receptor, regulation of cellular activation CD6 Cd6 19 T cell activation, thymic development, CD166 counterreceptor CD7 Cd7 11 Early T cell marker (human) CD8a/Ly-2 Cd8a 6 TCR coreceptor, MHC class I receptor, signal transduction CD8b/Ly-3 Cd8b 6 TCR coreceptor, MHC class I receptor, signal transduction CD9 Cd9 6 TM4 superfamily, T cell costimulation CD10/CALLA, NEP Mme 3 Ectoenzyme, neutral endopeptidase, B cell development CD11a/Ly-15, LFA-1 ␣-chain Itgal 7 Associates with CD18, ICAM-1, and ICAM-2 counterreceptor CD11b/Ly-40, Mac-1 ␣-chain Itgam Unknown Associates with CD18, fibrinogen, and C3bi counterreceptor CD11c/ aX Itgax Unknown Associates with CD18 CD12 Not defined CD13 Lap1 9 Type II , aminopeptidase N CD14 Cd14 18 GPI-linked protein, LPS/LBP complex receptor CD15 Not defined Carbohydrate determinant: Lewis X (human); binds CD62E, CD62L, CD62P CD16/Fc␥R III Fcgr3 1 Low-affinity binding to IgG, ADCC CD17 Not defined Carbohydrate determinant: lactosylceramide (human) ␤ CD18/integrin 2 Itgb2 10 Adhesion, associates with CD11a, CD11b, CD11c CD19 Cd19 7 BCR co-receptor, signal transduction, pan B marker CD20/Ly-44 Cd20 19 B cell activation/differentiation, Type III transmembrane protein CD21/-2 Cr2 1 Cd 3 receptor, complex with BCR CD22/Lyb-8 Cd22 7 Adhesion, B cell activation CD23/Ly-42 Fcer2a 8 Low-affinity receptor for IgE CD24a/HSA Cd24a 10 T cell costimulation, adhesion, CD62P counterreceptor CD24b Cd24b 8 CD24c Cd24c 14 CD25/p55, IL-2R␣ chain Il2ra 2 Low-affinity binding to IL-2 by itself, associates with CD122 and CD132, lymphocyte differentiation and activation CD26/THAM Dpp4 2 Ectoenzyme, dipeptidyl peptidase, cellular activation CD27 Cd27 6 TNFR superfamily, T cell costimulation, CD70 counterreceptor CD28 Cd28 1 T cell costimulation, CD80 and CD86 counterreceptor ␤ CD29/integrin 1, gplla Itgb1 Unknown VLAb, associates with CD49a, b, c, d, e, or f, adhesion CD30/Ki Cd30 4 TNFR superfamily, T cell activation/regulation CD31/PECAM-1 Pecam 6 Adhesion, signal transduction; counterreceptor to CD38 CD32/Ly-17/Fcg receptor II Fcgr2 1 Low-affinity binding to IgG, ADCC CD33 Cd33 7 CD34 Cd34 1 Multiple isoforms, CD62L counterreceptor (90 kD), hemopoiesis (human) CD35/complement receptor-1 Cr1 1 receptor, CD36 Cd36 5 receptor; oxidixed LDL receptor; collagen receptor CD37 Cd37 7 CD38 Cd38 5 Ectoenzyme, cyclase/hydrolase, cellular activation, CD31 counterreceptor (human) CD39 Not defined CD40 Cd40 2 TNFR superfamily, B cell activation/differentiation/survival CD154 (gp39) counterreceptor ␣ ␤ CD41/integrin llb Itga2b 11 Associates with integrin 3, adhesion; platelet marker CD42 Not defined CD43/leukosialin, Ly-48 Spn 7 Two isoforms; adhesion, signal transduction, binding to CD54 CD44/Pgp-1, Ly-24 Cd44 2 Receptor for hyaluronate, adhesion, homing, , T cell activation, marker for memory T cells CD45/LCA, Ly-5 Ptprc 1 /activation, tyrosine phosphatase pan-leukocyte marker CD45RA Ptprc 1 Cellular differentiation/activation, tyrosine phosphatase restricted expression, exon A dependent CD45RB Ptprc 1 Cellular differentiation/activation, tyrosine phosphatase restricted expression, exon B dependent CD45RC Ptprc 1 Cellular differentiation/activation, tyrosine phosphatase restricted expression, exon C dependent CD45RO Ptprc 1 Cellular differentiation/activation, tyrosine phosphatase, marker for naive T cells; restricted expression CD45R/B220 Ptprc 1 Cellular differentiation/activation, tyrosine phosphatase, marker for B cells and activated T and NK (LAK) cells CD46 Not defined Membrane protein (MCP) CD47/integrin-associated protein Itgp Unknown Activation and extravasation of PMN; Ig superfamily (IAP) CD48/Sgp-60, BCM-1, BLAST-1 Cd48 1 GPI-linked protein, T cell costimulation, adhesion, CD2 counterreceptor ␣ CD49a/integrin 1 Itga1 13 Associates with CD29, laminin/collagen receptor ␣ CD49b/integrin 2 Itga2 13 Associates with CD29, laminin/collagen/fibronectin receptor ␣ CD49c/integrin 3 Itga3 11 Associates with CD29, laminin/collagen/fibronectin receptor Continued The Journal of Immunology 3865

Table II. continued

CD/Other name Mouse Gene Symbol Chromosome Comments ␣ CD49d/integrin 4 Itga4 2 Associates with CD29 ␣ CD49e/integrin 5 Itga5 15 Associates with CD29, fibronectin/laminin receptor ␣ CD49f/integrin 6 Itga6 2 Associates with CD29, laminin receptor CD50/ICAM-3 Icam3 Unknown Adhesion/signaling CD51/integrin aV Itgav 2 Associates with ␤ , vitronectin and fibronectin receptor CD52 Not defined Campath (human) CD53 Cd53 3 CD54/ICAM-1, Ly-47 Icam1 9 Adhesion, T cell costimulation, CD11a, CD11b, and CD43 counterreceptor CD55 Daf1 1 CD56/NCAM-1 Ncam 9 Adhesion, nervous system CD57 Not defined HNK1 (human) CD58 Not defined LFA-3 (human) CD59 Cd59 2 CD60 Not defined ␤ CD61/integrin 3 Itgb3 11 Associates with CD41 and CD51, extracellular adhesion CD62E/E-selectin, ELAM Sele 1 Adhesion, leukocyte rolling/migration, binds to sialyl Lewis X (CD15) CD62L/L-selectin, LECAM-1 Sell 1 Adhseion, leukocyte rolling/migration, binds to sialyl Lewis X (CD15) CD34 counterreceptor CD62P/P-selectin, PADGEM Selp 1 Adhesion, leukocyte rolling/migration, binds to CD15 and CD24 CD63 Cd63 18 Platelet activation Ag (TM4 superfamily) CD64/Fc␥RI Fcgr1 3 High-affinity binding to IgG, ADCC CD65 Not defined Ceremide dodecasaccharide (human) CD66 Not defined CD67 Withdrawn, now CD66b CD68/macrosialin Cd68 Unknown Type I transmembrane, lysosomal-associated protein CD69/very early activation Ag Cd69 6 Leukocyte activation; early lymphocyte activation marker CD70 Cd70 CD27 counter-receptor CD71/ Trfr Unknown Type II transmembrane protein, activation, iron metabolism CD72/Lyb-2 Cd72 4 Cd5 counter-receptor, B cell costimulation CD73 Nt5 Ecto-5Ј nucleotidase; B and T cell subsets (human) CD74/invariant chain Ii 18 MCH class II folding/trafficking, Ag presentation CD75 Not defined CD76 Not defined CD77 Not defined CD78 Not defined CD79a/Ig␣ Cd79a 7 Ig superfamily, signal transduction CD79b/Ig␤ Cd79b Unknown Ig superfamily, signal transduction CD80/B7-1 Cd80 16 B cell costimulation, T/B interaction CD28 and CE152 counterreceptor CD81/TAPA-1 CD81 7 TM4 superfamily, signal transduction, T cell costimulation CD82/KAI1 Cd82 2 TM4 superfamily, signal transduction, T cell costimulation CD83 Cd83 Unknown Marker for dendritic and activated T and B (human; mouse cloned, no mAb) CD84 Not defined CD85 Not defined CD86/B7-2 Cd86 16 B cell costimulation, T/B interactions, CD28 and CD152 counterreceptor CD87 Not defined CD88 Not defined (human) CD89 Not defined Receptor for IgA CD90/Thy-1 Thy1 9 GPI-linked transmembrane protein, signal transduction, T cell activation ␣ CD91/ 2 macroglobulin receptor Lrp 15 Lipoprotein metabolism CD92 Not defined CD93 Not defined CD94 Not defined NK cell receptor for HLA-class I molecules CD95/Fas Fas 19 TNFR superfamily , T cell costimulation, lpr mutation CD96 Not defined Ig superfamily, T cell activation, increased late expression CD97 Not defined CD98/4F2, Ly-10 Cd98 19 Cellular activation, calcium flux CD99 Not defined CD100 Not defined CD101 Not defined V7 , Ig superfamily, CD3-dependent T cell activation (human) CD102/ICAM-2 Icam2 11 Ig superfamily, adhesion to CD11a ␣ ␤ CD103/integrin IEL Itgae Unknown Associates with integrin 7, adhesion ␤ ␣ CD104/integrin 4 Itgb4 11 Associates with integrin 6, adhesion CD105/ Eng 2 Adhesion, ligand for TGF-␤ CD106/VCAM-1 Vcam1 3 Signaling, adhesion to CD49d/CD29 (VLA-4) CD107a/LAMP-1 Lamp1 8 Lysosomal-associated , adhesion/metastasis CD107b/LAMP-2 Lamp2 X Lysosomal-associated membrane protein, adhesion/metastasis CDw108 Not defined CDw109 Sialomucin CD110 Reserved CD111 Reserved CD112 Reserved CD113 Reserved CD114 Not defined

Continued 3866 MOUSE CELL SURFACE Ags

Table II. continued

CD/Other name Mouse Gene Symbol Chromosome Comments

CD115/M-CSFR, CSF-1R Csfmr 18 Tyrosine kinase receptor family, signal transduction, cell differentiation CD116 Csfgmra 19 Receptor for GM-CSF, associates with CDw131 CD117/c-KIT, steel factor receptor Kit 5 Tyrosine kinase receptor family, signal transduction, cell differentiation, CD118/IFN-␣␤ receptor Ifnar 16 Wr mutation IFN-␣␤ receptor, signal transduction CD119/IFN-␥ receptor Ifngr 1 13 High-affinity binding to IFN-␥, signal transduction CD120a/TNF receptor ␣-chain Tnfr1 6 Type I, TNFR superfamily, signal transduction, apoptosis CD120b/TNF receptor ␤-chain Thfr2 4 Type II, TNFR superfamily, signal transduction, apoptosis CD121a/IL-1 receptor ␣-chain Il1r1 1 Ig superfamily, IL-1 binding, signal transduction CD121b/IL-1 receptor ␤-chain IL1r2 1 Ig superfamily, IL-1 binding CD122/IL-2 receptor ␤-chain Il2rb 15 Associates with CD25 and CD132 for high-affinity binding to IL-2, signal transduction CD123/IL-3 receptor ␣-chain II3ra 14 Low-affinity binding to IL-3, associates with CDw131 for high-affinity binding CD124/IL-4 receptor ␣-chain Il4ra 7 Associates with CD132 for high-affinity binding to IL-4 CD125/IL-5 receptor ␣-chain Il5ra 6 Low-affinity binding to IL-5, associates with CDw131 for high-affinity binding CD126/IL-6 receptor ␣-chain Il6ra 3 Low-affinity binding to IL-6, associates with CD130 for high-affinity binding CD127/IL-7 receptor ␣-chain Il7ra 15 Associates with CD132 for high-affinity binding to IL-7 CD128/IL-8 receptor ␣-chain Cmkar2 1 Binding to mouse MIP-2 CD129 Reserved CD130/gp 130 Il6st Unknown Signal transduction, common ␤ chain of IL-6R, IL-11R, LIFR, OSMR CDw131/common ␤-chain II3rb 1/II3rb2 15 Signal transduction, member of IL-3R, IL-5R, and GM-CSFR complexes CD132/common ␥-chain Il2rg X Signal transduction, member of IL-2R, IL-4R, IL-7R, IL-13R, and IL-15R complexes CD133 Reserved CD134/OX-40, Ly-70 Txgp2 4 TNFR superfamily, T cell costimulation CD135/Flk-1/flt3, Ly-72 Flt3 5 Tyrosine kinase receptor family myeloid and lymphoid progenitor development CD136/4-1BB, Ly-63 Cd136 TNFR superfamily, T cell costimulation CD137/MSPR, RON Not defined 4 Receptor for -stimulating protein (MSP) (human) CD138/syndecan-1 Synd-1 12 B cell development/differentiation CD139 Not defined CD140a/PDGF-R ␣-chain Pdgfra 5 Tyrosine kinase receptor family, binds to PDGF a and b, signal transduction CD140b/PDGF-R ␤-chain Pdgfrb 18 Tyrosine kinase receptor family, binds only to PDGF b, signal transduction CD141/ Thbd 2 CD142 Not defined Unknown , receptor for cofactor VII (human) CD143 Ace 11 Angiotesin converting CD144/VE- Cdh5 8 Adhesion CDw145 Pan endothelial marker (defined by mAbs E036, E037) CD146/MUC 18/s-endo Not defined CD147/neurothelin, Bsg 10 Ig superfamily, -brain barrier, expressed on activated leukocytes CD148/M4, M56 Not defined CD149/MEM-133 Not defined CDw 150/IPO-3; SLAM Not defined Ig superfamily, T cell stimulation (human) CD151/PETA Not defined TM4 family; signaling CD152/CTLA-4, Ly-56 Cd152 1 T cell activation/regulation, CD80 and CD86 counter-receptor CD153/CD30 ligand Cd153 4 TNF family, activated , CD30 counter-receptor CD154/CD40 ligand (gp39), Ly-62 Cd154 X TNF family, T cell activation, transient expression CD155 Not defined Poliovirus receptor (human) CD156/ADAM8 Cd156 7 CD157/BST-1, Mo-5, Ly-65 Bp3 5 Ectoenzyme, B and T cell development CD158a/p58.1 Not defined NK receptor (human) CD159b/p58.2 Not defined NK receptor (human) CD160 Reserved CD161a Klrb1 6 NK cell activation/regulation; NKR-P1A CD161b CD161c Klrb3 Mouse NK1.1, pan NK marker; NKR-P1C CD162/PSGL-1 Cd162 P-selectin ligand protein one P11, P12 (human) CD163 Not defined CD164/MGC-24, A115, A25 Not defined

CD165/Ad2/gp37 Not defined CD166/ALCAM Cd166 CD6 counter-receptor, activated leukocyte-, thymic development, T/B interaction, nervous system (human)

a CD1-CD130 are cited in ref. 4; references for CD131–CD166 have been entered into the Mouse Genome Database (http://www.informatics.jax.org).

Lanier, unpublished observation), CD161a, and the Klra family gest that gp49 is unlikely to be the mouse equivalent of human members, have been characterized (28). The MHC class I ligands KIR (29). It is likely that Klra family members serve as KIR and of these NK receptors and their inhibitory or activating functions KAR functional equivalents in mice (28). 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 The anti-Ly-71 (F4/80) mAb has been used extensively in deter- been cloned from mouse mast cells (29). The available data sug- mining the distribution and function of mouse tissue macrophages The Journal of Immunology 3867

(30), although eosinophils and dendritic cells (DC) have been re- monoclonal Abs to mouse CD34 (49–50) have demonstrated that ported to react with this mAb (31, 32). To date, no human homo- CD34 is expressed on a small subset of cells. In logue of Ly-71 (F4/80) has been reported. CD11b (Mac-1), an- humans, the populations are identified by the expression other commonly used marker for the /macrophage of CD34. A recent report with one anti-mouse CD34 mAb, 49E8 lineage, is expressed on NK cells, granulocytes, a T cell subset, (RAM34), however, suggests that primitive hemopoietic stem cells and peritoneal B-1 B cells. CD14 is widely perceived as the best capable of long term repopulation are contained in the CD34-neg- marker for the human macrophage/monocyte population. In mice, ative/low fraction, whereas the CD34-positive cells are committed the level of CD14, as recognized by an anti-CD14 mAb, rmC5–3, progenitor cells lacking self-renewal capability (51). Other rele- was low or undetectable on resting blood monocytes. It remains to vant Ags expressed by progenitor cells include CD25, CD90 (Thy- be determined whether other newly generated Abs to mouse CD14 1), ER-MP12 (52), CD135 (Flk-2/Flt-3) (53), Ly-6E (TSA-1, will recognize a distribution similar to that in humans. Other mAbs Sca-2) (54), Ly-51 (BP-1, 6C3), and CD157 (BP-3). used for identification of macrophage/monocyte subsets are MOMA-1, MOMA-2 (33), Mac-2, Mac-3, and the macrophage Activation Ags scavenger receptor. An important feature of cellular activation is the de novo expres- sion of surface molecules or up-regulation of the Ags expressed Dendritic cells constitutively. The mode of stimulation, kinetics, and expression DC display surface phenotype heterogeneity depending on their pattern of any given marker may imply its role in the immune microenvironment and state of activation. Their ill-defined surface response. Surface molecules, including CD71 (transferrin recep- phenotypes in addition to their low numbers in tissues have made tor), CD98 (4F2), and CD69, are expressed by a wide range of the isolation of these cells rather cumbersome. DC express many activated cell types, reflecting their general role in cellular prolif- adhesion and costimulatory molecules and myeloid lineage mark- eration. CD69 is useful as a lymphocyte activation marker because ers (32). Although several Ags have been reported to be expressed of its expression in the very early stage of activation (55). It is specifically by DC, mAb to these Ags often react with other cell noteworthy that although some markers were initially defined to be types or only recognize subsets of DC. For separation of DC from restricted to specific types of activated cells, their distributions other cell types, multicolor analysis or prior enrichment protocols were subsequently found to be more general. For example, CD25 such as plastic adherence methods are necessary. The Ly-75 (IL-2R ␣-chain), often used as a T cell activation marker, is (DEC-205) Ag (34) and CD11c (35) have proved to be more re- present on activated T, B, and NK cells and is expressed during stricted markers for DC, although they may not be expressed on all ontogeny on pre-B and pre-T cells. CD80 and CD86, initially re- DC, and they may also be expressed on other cell types. In hu- ported as B cell activation markers, are constitutively expressed by mans, CD83 and the Ag identified by mAb CRMF-44 have re- macrophages, DCs, and fibroblasts and can be induced on acti- cently been identified as novel markers for DC (3, 36). Other Abs vated T cells (56, 57). Further, sensitivity of the detection method useful for the identification of DCs include Ly-79 (33D1) (37), 4F7 may be a limiting factor when studying low density Ags. Other (38), and Ly-74 (Ep-CAM, gp40), a homologue of human epithe- molecules reported to be expressed by activated lymphocytes in- lial growth factor (39). clude CD152 (CTLA-4), CDw137 (4-1BB), CD134 (OX-40), DATK44 Ag (TABS), Ly-77 (GL7), CD45R (B220), CD30, CD95 Granulocytes ligand, CD43, Ly-6 family members, CD106, cytokine receptors, Expression of Ly-6G is reported to be primarily limited to gran- and the family of very late Ag adhesion molecules. ulocytes; mAbs specific to this molecule, also known as the Gr-1 In this communication, we provide an update on mouse cell Ag, have been used successfully to separate mouse granulocyte surface molecules, including lists of surface markers that, in com- lineage cells (40). bination with multiparameter flow cytometric analysis, can be used to trace cell lineages and activation state. Several novel markers Erythroid cells mentioned here may prove useful in mouse immunology research. The Ly-76 Ag detected by the mAb TER-119 has been used to Most of the reported mAbs and their respective Ags are compiled identify cells of the erythroid lineage (41, 42). in the CD and Ly charts. Undoubtedly, many molecules have not been included here. Scientists are encouraged to contact the au- Endothelial cells thors and the Committee on Standardized Genetic Nomenclature MECA-32 appears to be most restricted marker for for Mice to submit novel molecules for their inclusion in the future (43). Other Ags expressed by endothelial cells include CD106 reports. In addition to this communication, information on the (vascular cell adhesion molecule-1), CD31, CD34, Ly-73 (Flk-1), mouse genome and genetic markers is available on the worldwide and CD105. CD62E is expressed by activated endothelial web. The Mouse Genome Database can be accessed via http:// cells (27, 44). 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. CD41 (integrin ␣IIb) is the best marker for platelets; other surface proteins expressed by platelets include CD61 (integrin ␤3) (45) Acknowledgments and CD9 (46). Activated platelets express CD62P (27). We thank M. A. Reyes and Drs. C. Shih, K. Holmes, and V. Kumar for Progenitor cells their helpful assistance with this manuscript, and B. R. Marshall for ex- cellent editorial assistance. The classic method for identifying mouse stem/pluripotent cells in total bone marrow cells has included the use of a combination of References Abs; cells negative for CD4, CD8, CD11b (Mac- 1), CD45/B220, Ly-6G (Gr-1), and Ly-76 (Ter-119) and positive 1. Holmes, K. L., and H. C. Morse III. 1988. Cell surface antigen expression in murine hematopoietic cell differentiation. Immunol. 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