The Journal of Immunology, 1998, 160: 3861-3868.
Copyright © 1998 by The American Association of Immunologists
Mouse Cell Surface Antigens: Nomenclature and Immunophenotyping1
Lily Lai*,
Noosheen Alaverdi*,
Lois Maltais
and
Herbert C. Morse, III2,
*
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
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Abstract
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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.
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Introduction
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Molecules
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 identified
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 receptor, 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 definitively identified. When a mouse Ly Ag is
identified 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 confirm 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 reflects several novel mouse CD homologues that have
been identified 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.
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B cells
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In the mouse, one of the most commonly used pan-B cell markers is
identified by the mAb RA3-6B2 (CD45R/B220); however, this 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.
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T cells
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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 identification of mainstream helper and
cytotoxic T cells, respectively. A third class of T cells with both
helper and cytotoxic properties has been identified 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).
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NK cells
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The official 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 field.
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 five 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 NK1.1-negative strains (L. Lanier, unpublished
observation). CD122 (IL-2R ß-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. 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 suggest 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).
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Macrophages/monocytes
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The anti-Ly-71 (F4/80) mAb has been used extensively in
determining the distribution and function of mouse tissue macrophages
(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, rmC5–3, 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 identification of macrophage/monocyte
subsets are MOMA-1, MOMA-2 (33), Mac-2, Mac-3, and the macrophage
scavenger receptor.
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Dendritic cells
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DC display surface phenotype heterogeneity depending on their
microenvironment and state of activation. Their ill-defined 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 specifically 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 identified by mAb CRMF-44 have
recently been identified as novel markers for DC (3, 36). Other Abs
useful for the identification of DCs include Ly-79 (33D1) (37), 4F7
(38), and Ly-74 (Ep-CAM, gp40), a homologue of human epithelial growth
factor (39).
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Granulocytes
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Expression of Ly-6G is reported to be primarily limited to
granulocytes; mAbs specific to this molecule, also known as the Gr-1
Ag, have been used successfully to separate mouse granulocyte lineage
cells (40).
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Erythroid cells
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The Ly-76 Ag detected by the mAb TER-119 has been used to identify
cells of the erythroid lineage (41, 42).
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Endothelial cells
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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).
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Platelets
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CD41 (integrin 
IIb) is the best marker for platelets; other
surface proteins expressed by platelets include CD61 (integrin ß3)
(45) and CD9 (46). Activated platelets express CD62P (27).
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Progenitor cells
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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 (Mac-1), 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 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 identified 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 (Thy-1), 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).
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Activation Ags
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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,
reflecting 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 defined to be restricted to specific 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 fibroblasts 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 flow 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
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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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Footnotes
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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.
3 Abbreviations used in this paper: CD, cluster of differentiation; Ly, lymphocyte antigen; HLDA, human leukocyte differentiation antigen; KIR, killing inhibitory receptor; DC, dendritic cell.
Received for publication September 26, 1997.
Accepted for publication December 24, 1997.
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Top
Abstract
Introduction
