L2pB1: A new player in autoimmunity

Molecular Immunology

Volumn 48, Issue 11, 2011, Pages 1292-1300

  Zhong, Xuemei ^a   Rothstein, Thomas L ^b,c  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

Author keywords

Autoimmunity; B1 B cells; PD L2

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN M; PROGRAMMED DEATH 1 LIGAND 2;

AUTOIMMUNITY; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; DENDRITIC CELL; GERMINAL CENTER; HUMAN; IMMUNOGLOBULIN PRODUCTION; MACROPHAGE; NONHUMAN; PATHOPHYSIOLOGY; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE; TH17 CELL;

ANIMALS; ANTIGENS, CD80; AUTOANTIGENS; AUTOIMMUNITY; B-LYMPHOCYTE SUBSETS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; RNA, DOUBLE-STRANDED; T-LYMPHOCYTES; TH17 CELLS;

MURINAE;

EID: 79956324551     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.12.006     Document Type: Review

References (97)

1. Amel Kashipaz M.R., Huggins M.L., Lanyon P., Robins A., Powell R.J., Todd I. Assessment of Be1 and Be2 cells in systemic lupus erythematosus indicates elevated interleukin-10 producing CD5+ B cells. Lupus 2003, 12:356-363.
2. Ansel K.M., Harris R.B., Cyster J.G. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 2002, 16:67-76.
3. Baudino L., Nimmerjahn F., Azeredo da Silveira S., Martinez-Soria E., Saito T., Carroll M., Ravetch J.V., Verbeek J.S., Izui S. Differential contribution of three activating IgG Fc receptors (FcgammaRI, FcgammaRIII, and FcgammaRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice. J. Immunol. 2008, 180:1948-1953.
4. Baumgarth N., Herman O.C., Jager G.C., Brown L.E., Herzenberg L.A., Chen J. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J. Exp. Med. 2000, 192:271-280.
5. Becker H., Weber C., Storch S., Federlin K. Relationship between CD5+ B lymphocytes and the activity of systemic autoimmunity. Clin. Immunol. Immunopathol. 1990, 56:219-225.
6. Binder C.J., Silverman G.J. Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin. Immunopathol. 2005, 26:385-404.
7. Blenman K.R., Duan B., Xu Z., Wan S., Atkinson M.A., Flotte T.R., Croker B.P., Morel L. IL-10 regulation of lupus in the NZM2410 murine model. Lab. Invest. 2006, 86:1136-1148.
8. Boes M., Prodeus A.P., Schmidt T., Carroll M.C., Chen J. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J. Exp. Med. 1998, 188:2381-2386.
9. Bouaziz J.D., Yanaba K., Tedder T.F. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol. Rev. 2008, 224:201-214.
10. Cabral A.R., Cabiedes J., Alarcon-Segovia D. Hemolytic anemia related to an IgM autoantibody to phosphatidylcholine that binds in vitro to stored and to bromelain-treated human erythrocytes. J. Autoimmun. 1990, 3:773-787.
11. Chong W.P., Ip W.K., Wong W.H., Lau C.S., Chan T.M., Lau Y.L. Association of interleukin-10 promoter polymorphisms with systemic lupus erythematosus. Genes Immun. 2004, 5:484-492.
12. Crispin J.C., Tsokos G.C. Interleukin-17-producing T cells in lupus. Curr. Opin. Rheumatol. 2010, 22:499-503.
13. Cunningham A.J. Large numbers of cells in normal mice produce antibody components of isologous erythrocytes. Nature 1974, 252:749-751.
14. Dauphinee M., Tovar Z., Talal N. B cells expressing CD5 are increased in Sjogren's syndrome [see comments]. Arthritis Rheum. 1988, 31:642-647.
15. El-behi M., Rostami A., Ciric B. Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J. Neuroimmun. Pharmacol. 2010, 5:189-197.
16. Evans J.G., Chavez-Rueda K.A., Eddaoudi A., Meyer-Bahlburg A., Rawlings D.J., Ehrenstein M.R., Mauri C. Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. 2007, 178:7868-7878.
17. Fillatreau S., Sweenie C.H., McGeachy M.J., Gray D., Anderton S.M. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002, 3:944-950.
18. Forster I., Gu H., Muller W., Schmitt M., Tarlinton D., Rajewsky K. CD5 B cells in the mouse. Curr. Top. Microbiol. Immunol. 1991, 173:247-251.
19. Giorgini A., Brown H.J., Lock H.R., Nimmerjahn F., Ravetch J.V., Verbeek J.S., Sacks S.H., Robson M.G. Fc gamma RIII and Fc gamma RIV are indispensable for acute glomerular inflammation induced by switch variant monoclonal antibodies. J. Immunol. 2008, 181:8745-8752.
20. Good-Jacobson K.L., Szumilas C.G., Chen L., Sharpe A.H., Tomayko M.M., Shlomchik M.J. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 2010, 11:535-542.
21. Greenwald R.J., Tumang J.R., Sinha A., Currier N., Cardiff R.D., Rothstein T.L., Faller D.V., Denis G.V. E mu-BRD2 transgenic mice develop B-cell lymphoma and leukemia. Blood 2004, 103:1475-1484.
22. Haas K.M., Poe J.C., Steeber D.A., Tedder T.F. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 2005, 23:7-18.
23. Hamaguchi Y., Uchida J., Cain D.W., Venturi G.M., Poe J.C., Haas K.M., Tedder T.F. The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J. Immunol. 2005, 174:4389-4399.
24. Hardy R.R. B-1 B cell development. J. Immunol. 2006, 177:2749-2754.
25. Hardy R.R., Carmack C.E., Shinton S.A., Riblet R.J., Hayakawa K. A single VH gene is utilized predominantly in anti-BrMRBC hybridomas derived from purified Ly-1 B cells. Definition of the VH11 family. J. Immunol. 1989, 142:3643-3651.
26. Hardy R.R., Wei C.J., Hayakawa K. Selection during development of VH11+ B cells: a model for natural autoantibody-producing CD5+ B cells. Immunol. Rev. 2004, 197:60-74.
27. Holodick N.E., Tumang J.R., Rothstein T.L. Continual signaling is responsible for constitutive ERK phosphorylation in B-1a cells. Mol. Immunol. 2009, 46:3029-3036.
28. Ishikawa S., Matsushima K. Aberrant B1 cell trafficking in a murine model for lupus. Front. Biosci. 2007, 12:1790-1803.
29. Ito T., Ishikawa S., Sato T., Akadegawa K., Yurino H., Kitabatake M., Hontsu S., Ezaki T., Kimura H., Matsushima K. Defective B1 cell homing to the peritoneal cavity and preferential recruitment of B1 cells in the target organs in a murine model for systemic lupus erythematosus. J. Immunol. 2004, 172:3628-3634.
30. Jamin C., Morva A., Lemoine S., Daridon C., de Mendoza A.R., Youinou P. Regulatory B lymphocytes in humans: a potential role in autoimmunity. Arthritis Rheum. 2008, 58:1900-1906.
31. Kaku H., Rothstein T.L. Octamer binding protein 2 (Oct2) regulates PD-L2 gene expression in B-1 cells through lineage-specific activity of a unique, intronic promoter. Genes Immun. 2010, 11:55-66.
32. Kanno K., Okada T., Abe M., Hirose S., Shirai T. CD5+ B cells as precursors of CD5- IgG anti-DNA antibody-producing B cells in autoimmune-prone NZB/W F1 mice. Ann. N.Y. Acad. Sci. 1992, 651:576-578.
33. Kantor A.B., Herzenberg L.A. Origin of murine B cell lineages. Annu. Rev. Immunol. 1993, 11:501-538.
34. Klinman D.M., Holmes K.L. Differences in the repertoire expressed by peritoneal and splenic Ly-1 (CD5)+ B cells. J. Immunol. 1990, 144:4520-4525.
35. Kroese F.G., Ammerlaan W.A., Deenen G.J. Location and function of B-cell lineages. Ann. N.Y. Acad. Sci. 1992, 651:44-58.
36. Latchman Y., Wood C.R., Chernova T., Chaudhary D., Borde M., Chernova I., Iwai Y., Long A.J., Brown J.A., Nunes R., Greenfield E.A., Bourque K., Boussiotis V.A., Carter L.L., Carreno B.M., Malenkovich N., Nishimura H., Okazaki T., Honjo T., Sharpe A.H., Freeman G.J. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2001, 2:261-268.
37. Lenert P., Brummel R., Field E.H., Ashman R.F. TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J. Clin. Immunol. 2005, 25:29-40.
38. Leung S., Liu X., Fang L., Chen X., Guo T., Zhang J. The cytokine milieu in the interplay of pathogenic Th1/Th17 cells and regulatory T cells in autoimmune disease. Cell. Mol. Immunol. 2010, 7:182-189.
39. Liang S.C., Latchman Y.E., Buhlmann J.E., Tomczak M.F., Horwitz B.H., Freeman G.J., Sharpe A.H. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur. J. Immunol. 2003, 33:2706-2716.
40. Liang Z., Xie C., Chen C., Kreska D., Hsu K., Li L., Zhou X.J., Mohan C. Pathogenic profiles and molecular signatures of antinuclear autoantibodies rescued from NZM2410 lupus mice. J. Exp. Med. 2004, 199:381-398.
41. Loke P., Allison J.P. PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5336-5341.
42. Lubberts E. Th17 cytokines and arthritis. Semin. Immunopathol. 2010, 32:43-53.
43. Lundy S.K., Boros D.L. Fas ligand-expressing B-1a lymphocytes mediate CD4(+)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and IL-10. Infect. Immun. 2002, 70:812-819.
44. Mai J., Wang H., Yang X.F. Th 17 cells interplay with Foxp3+ Tregs in regulation of inflammation and autoimmunity. Front. Biosci. 2010, 15:986-1006.
45. Marcos M.A., Huetz F., Pereira P., Andreu J.L., Martinez A.C., Coutinho A. Further evidence for coelomic-associated B lymphocytes. Eur. J. Immunol. 1989, 19:2031-2035.
46. Markeljevic J., Batinic D., Uzarevic B., Bozikov J., Cikes N., Babic-Naglic D., Horvat Z., Marusic M. Peripheral blood CD5+ B cell subset in the remission phase of systemic connective tissue diseases. J. Rheumatol. 1994, 21:2225-2230.
47. Matsushita T., Horikawa M., Iwata Y., Tedder T.F. Regulatory B cells (B10 Cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J. Immunol. 2010, 185:2240-2252.
48. Mauri C., Gray D., Mushtaq N., Londei M. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 2003, 197:489-501.
49. Mercolino T.J., Arnold L.W., Hawkins L.A., Haughton G. Normal mouse peritoneum contains a large population of Ly-1+ (CD5) B cells that recognize phosphatidyl choline. Relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J. Exp. Med. 1988, 168:687-698.
50. Mohan C., Morel L., Yang P., Wakeland E.K. Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum. 1998, 41:1652-1662.
51. Mond J.J., Lees A., Snapper C.M. T cell-independent antigens type 2. Annu. Rev. Immunol. 1995, 13:655-692.
52. Mond J.J., Vos Q., Lees A., Snapper C.M. T cell independent antigens. Curr. Opin. Immunol. 1995, 7:349-354.
53. Montecino-Rodriguez E., Dorshkind K. Evolving patterns of lymphopoiesis from embryogenesis through senescence. Immunity 2006, 24:659-662.
54. Morel L., Croker B.P., Blenman K.R., Mohan C., Huang G., Gilkeson G., Wakeland E.K. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:6670-6675.
55. Morris D.L., Rothstein T.L. Abnormal transcription factor induction through the surface immunoglobulin M receptor of B-1 lymphocytes. J. Exp. Med. 1993, 177:857-861.
56. Murakami M., Nakajima K., Yamazaki K., Muraguchi T., Serikawa T., Honjo T. Effects of breeding environments on generation and activation of autoreactive B-1 cells in anti-red blood cell autoantibody transgenic mice. J. Exp. Med. 1997, 185:791-794.
57. Murphy T.P., Kolber D.L., Rothstein T.L. Elevated expression of Pgp-1 (Ly-24) by murine peritoneal B lymphocytes. Eur. J. Immunol. 1990, 20:1137-1142.
58. Nguyen L.T., Ciric B., Ure D.R., Zhou B., Tamada K., Tseng S.Y., Shin T., Chen L., Dong H., Kyle R.A., Rodriguez M., Pease L.R. Retraction: Naturally occurring human IgM antibody that binds B7-DC and potentiates T cell stimulation by dendritic cells. J. Immunol. 2010, 184:6552.
59. Nguyen L.T., Ciric B., Van Keulen V.P., Pease L.R. Retraction: B7-DC/PD-L2 cross-linking induces NF-kappaB-dependent protection of dendritic cells from cell death. J. Immunol. 2010, 184:6554.
60. Nishimura H., Nose M., Hiai H., Minato N., Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999, 11:141-151.
61. Nishimura H., Okazaki T., Tanaka Y., Nakatani K., Hara M., Matsumori A., Sasayama S., Mizoguchi A., Hiai H., Minato N., Honjo T. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001, 291:319-322.
62. O'Garra A., Chang R., Go N., Hastings R., Haughton G., Howard M. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur. J. Immunol. 1992, 22:711-717.
63. Ochsenbein A.F., Fehr T., Lutz C., Suter M., Brombacher F., Hengartner H., Zinkernagel R.M. Control of early viral and bacterial distribution and disease by natural antibodies. Science 1999, 286:2156-2159.
64. Oflazoglu E., Swart D.A., Anders-Bartholo P., Jessup H.K., Norment A.M., Lawrence W.A., Brasel K., Tocker J.E., Horan T., Welcher A.A., Fitzpatrick D.R. Paradoxical role of programmed death-1 ligand 2 in Th2 immune responses in vitro and in a mouse asthma model in vivo. Eur. J. Immunol. 2004, 34:3326-3336.
65. Pages J., Bussard A.E. Precommitment of normal mouse peritoneal cells by erythrocyte antigens in relation to auto-antibody production. Nature 1975, 257:316-317.
66. Radhakrishnan S., Nguyen L.T., Ciric B., Ure D.R., Zhou B., Tamada K., Dong H., Tseng S.Y., Shin T., Pardoll D.M., Chen L., Kyle R.A., Rodriguez M., Pease L.R. Naturally occurring human IgM antibody that binds B7-DC and potentiates T cell stimulation by dendritic cells. J. Immunol. 2003, 170:1830-1838.
67. Radhakrishnan S., Nguyen L.T., Ciric B., Van Keulen V.P., Pease L.R. B7-DC/PD-L2 cross-linking induces NF-kappaB-dependent protection of dendritic cells from cell death. J. Immunol. 2007, 178:1426-1432.
68. Reap E.A., Sobel E.S., Cohen P.L., Eisenberg R.A. The role of CD5+ B cells in the production of autoantibodies in murine systemic lupus erythematosus. Ann. N.Y. Acad. Sci. 1992, 651:588-590.
69. Reininger L., Kaushik A., Izui S., Jaton J.C. A member of a new VH gene family encodes antibromelinized mouse red blood cell autoantibodies. Eur. J. Immunol. 1988, 18:1521-1526.
70. Rothstein T.L., Kolber D.L. Peritoneal B cells respond to phorbol esters in the absence of co- mitogen. J. Immunol. 1988, 140:2880-2885.
71. Sato T., Ishikawa S., Akadegawa K., Ito T., Yurino H., Kitabatake M., Yoneyama H., Matsushima K. Aberrant B1 cell migration into the thymus results in activation of CD4 T cells through its potent antigen-presenting activity in the development of murine lupus. Eur. J. Immunol. 2004, 34:3346-3358.
72. Shin T., Yoshimura K., Crafton E.B., Tsuchiya H., Housseau F., Koseki H., Schulick R.D., Chen L., Pardoll D.M. In vivo costimulatory role of B7-DC in tuning T helper cell 1 and cytotoxic T lymphocyte responses. J. Exp. Med. 2005, 201:1531-1541.
73. Singh A.K., Stock P., Akbari O. Role of PD-L1 and PD-L2 in allergic diseases and asthma. Allergy 2010, Article first published online: 17 AUG 2010, doi:10.1111/j.1398-9995.2010.02458.x.
74. Sun C.M., Deriaud E., Leclerc C., Lo-Man R. Upon TLR9 signaling, CD5+ B cells control the IL-12-dependent Th1-priming capacity of neonatal DCs. Immunity 2005, 22:467-477.
75. Tesmer L.A., Lundy S.K., Sarkar S., Fox D.A. Th17 cells in human disease. Immunol. Rev. 2008, 223:87-113.
76. Tseng S.Y., Otsuji M., Gorski K., Huang X., Slansky J.E., Pai S.I., Shalabi A., Shin T., Pardoll D.M., Tsuchiya H. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J. Exp. Med. 2001, 193:839-846.
77. Tumang J.R., Frances R., Yeo S.G., Rothstein T.L. Cutting edge: Spontaneously Ig-secreting B-1 cells violate the accepted paradigm for expression of differentiation-associated transcription factors. J. Immunol. 2005, 174:3173-3177.
78. Tumang J.R., Hastings W.D., Bai C., Rothstein T.L. Peritoneal and splenic B-1 cells are separable by phenotypic, functional, and transcriptomic characteristics. Eur. J. Immunol. 2004, 34:2158-2167.
79. Turner J.E., Paust H.J., Steinmetz O.M., Panzer U. The Th17 immune response in renal inflammation. Kidney Int. 2010, 77:1070-1075.
80. van Zelm M.C., Szczepanski T., van der Burg M., van Dongen J.J. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J. Exp. Med. 2007, 204:645-655.
81. Viau M., Zouali M. B-lymphocytes, innate immunity, and autoimmunity. Clin. Immunol. 2005, 114:17-26.
82. Viau M., Zouali M. Effect of the B cell superantigen protein A from S. aureus on the early lupus disease of (NZBxNZW) F1 mice. Mol. Immunol. 2005, 42:849-855.
83. Wang S.C., Lin C.H., Ou T.T., Wu C.C., Tsai W.C., Hu C.J., Liu H.W., Yen J.H. Ligands for programmed cell death 1 gene in patients with systemic lupus erythematosus. J. Rheumatol. 2007, 34:721-725.
84. Wofsy D., Chiang N.Y. Proliferation of Ly-1 B cells in autoimmune NZB and (NZB x NZW)F1 mice. Eur. J. Immunol. 1987, 17:809-814.
85. Wolf S.D., Dittel B.N., Hardardottir F., Janeway C.A. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med. 1996, 184:2271-2278.
86. Wong S.C., Chew W.K., Tan J.E., Melendez A.J., Francis F., Lam K.P. Peritoneal CD5+ B-1 cells have signaling properties similar to tolerant B cells. J. Biol. Chem. 2002, 277:30707-30715.
87. Xu Z., Duan B., Croker B.P., Wakeland E.K., Morel L. Genetic dissection of the murine lupus susceptibility locus Sle2: contributions to increased peritoneal B-1a cells and lupus nephritis map to different loci. J. Immunol. 2005, 175:936-943.
88. Yamazaki T., Akiba H., Iwai H., Matsuda H., Aoki M., Tanno Y., Shin T., Tsuchiya H., Pardoll D.M., Okumura K., Azuma M., Yagita H. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 2002, 169:5538-5545.
89. Yanaba K., Bouaziz J.D., Haas K.M., Poe J.C., Fujimoto M., Tedder T.F. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008, 28:639-650.
90. Yang H., Kala M., Scott B.G., Goluszko E., Chapman H.A., Christadoss P. Cathepsin S is required for murine autoimmune myasthenia gravis pathogenesis. J. Immunol. 2005, 174:1729-1737.
91. Yeo S.G., Tumang J.R., Rothstein T.L. Characteristic features of B cells in murine cervical lymph nodes. Acta Otolaryngol. 2006, 126:56-61.
92. Yin Z., Bahtiyar G., Zhang N., Liu L., Zhu P., Robert M.E., McNiff J., Madaio M.P., Craft J. IL-10 regulates murine lupus. J. Immunol. 2002, 169:2148-2155.
93. Youinou P., Mackenzie L., Katsikis P., Merdrignac G., Isenberg D.A., Tuaillon N., Lamour A., Le Goff P., Jouquan J., Drogou A., et al. The relationship between CD5-expressing B lymphocytes and serologic abnormalities in rheumatoid arthritis patients and their relatives. Arthritis Rheum. 1990, 33:339-348.
94. Zhang M., Takahashi K., Alicot E.M., Vorup-Jensen T., Kessler B., Thiel S., Jensenius J.C., Ezekowitz R.A., Moore F.D., Carroll M.C. Activation of the lectin pathway by natural IgM in a model of ischemia/reperfusion injury. J. Immunol. 2006, 177:4727-4734.
95. Zhong X., Gao W., Degauque N., Bai C., Lu Y., Kenny J., Oukka M., Strom T.B., Rothstein T.L. Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur. J. Immunol. 2007, 37:2400-2404.
96. Zhong X., Lau S., Bai C., Degauque N., Holodick N.E., Steven S.J., Tumang J., Gao W., Rothstein T.L. A novel subpopulation of B-1 cells is enriched with autoreactivity in normal and lupus-prone mice. Arthritis Rheum. 2009, 60:3734-3743.
97. Zhong X., Tumang J.R., Gao W., Bai C., Rothstein T.L. PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for V(H)11/V(H)12 and phosphatidylcholine binding. Eur. J. Immunol. 2007, 37:2405-2410.