Distinct and synergistic roles of FcγRIIB deficiency and 129 strain-derived SLAM family proteins in the development of spontaneous germinal centers and autoimmunity

Journal of Autoimmunity

Volumn 63, Issue , 2015, Pages 31-46

  Soni, Chetna ^a   Domeier, Phillip P ^a   Wong, Eric B ^a,b   Shwetank, ^a   Khan, Tahsin N ^a,c   Elias, Melinda J ^a   Schell, Stephanie L ^a   Lukacher, Aron E ^a   Cooper, Timothy K ^a   Rahman, Ziaur S M ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Autoimmunity; B cells; Germinal centers; Inhibitory IgG receptor Fc RIIB; Signaling lymphocyte activation molecules; Systemic lupus erythematosus

Indexed keywords

B CELL ACTIVATING FACTOR; CD40 LIGAND; COMPLEMENT COMPONENT C3; FC RECEPTOR IIB; INTERLEUKIN 21; MESSENGER RNA; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; CD150 ANTIGEN; CELL SURFACE RECEPTOR; FC RECEPTOR; FCGR2B PROTEIN, MOUSE; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY TITER; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; BONE MARROW DERIVED DENDRITIC CELL; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; ENERGY METABOLISM; FEMALE; GENE LOCUS; GERMINAL CENTER; HELPER CELL; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHOCYTE PROLIFERATION; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; 129 MOUSE; ANIMAL; DEFICIENCY; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD; AUTOIMMUNITY; B-LYMPHOCYTES; GERMINAL CENTER; IMMUNE TOLERANCE; MICE; MICE, 129 STRAIN; RECEPTORS, CELL SURFACE; RECEPTORS, IGG; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE FAMILY MEMBER 1; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84940898187     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2015.06.011     Document Type: Article

References (62)

1. Wakeland E.K., Liu K., Graham R.R., Behrens T.W. Delineating the genetic basis of systemic lupus erythematosus. Immunity 2001, 15:397-408.
2. Fairhurst A.M., Wandstrat A.E., Wakeland E.K. Systemic lupus erythematosus: multiple immunological phenotypes in a complex genetic disease. Adv. Immunol. 2006, 92:1-69.
3. Wakeland E.K., Wandstrat A.E., Liu K., Morel L. Genetic dissection of systemic lupus erythematosus. Curr. Opin. Immunol. 1999, 11:701-707.
4. Morel L., Blenman K.R., Croker B.P., Wakeland E.K. The major murine systemic lupus erythematosus susceptibility locus, Sle1, is a cluster of functionally related genes. Proc. Natl. Acad. Sci. U S A 2001, 98:1787-1792.
5. Mohan C., Alas E., Morel L., Yang P., Wakeland E.K. Genetic dissection of SLE pathogenesis. Sle1 on murine chromosome 1 leads to a selective loss of tolerance to H2A/H2B/DNA subnucleosomes. J. Clin. Invest. 1998, 101:1362-1372.
6. Rozzo S.J., Vyse T.J., Drake C.G., Kotzin B.L. Effect of genetic background on the contribution of New Zealand black loci to autoimmune lupus nephritis. Proc. Natl. Acad. Sci. U S A 1996, 93:15164-15168.
7. Gubbels M.R., Jorgensen T.N., Metzger T.E., Menze K., Steele H., Flannery S.A., et al. Effects of MHC and gender on lupus-like autoimmunity in Nba2 congenic mice. J. Immunol. 2005, 175:6190-6196.
8. Wandstrat A.E., Nguyen C., Limaye N., Chan A.Y., Subramanian S., Tian X.H., et al. Association of extensive polymorphisms in the SLAM/CD2 gene cluster with murine lupus. Immunity 2004, 21:769-780.
9. Tsao B.P., Cantor R.M., Kalunian K.C., Chen C.J., Badsha H., Singh R., et al. Evidence for linkage of a candidate chromosome 1 region to human systemic lupus erythematosus. J. Clin. Invest. 1997, 99:725-731.
10. Moser K.L., Neas B.R., Salmon J.E., Yu H., Gray-McGuire C., Asundi N., et al. Genome scan of human systemic lupus erythematosus: evidence for linkage on chromosome 1q in African-American pedigrees. Proc. Natl. Acad. Sci. U S A 1998, 95:14869-14874.
11. Smith K.G., Clatworthy M.R. FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat. Rev. Immunol. 2010, 10:328-343.
12. Cannons J.L., Tangye S.G., Schwartzberg P.L. SLAM family receptors and SAP adaptors in immunity. Annu Rev. Immunol. 2011, 29:665-705.
13. Wang A., Batteux F., Wakeland E.K. The role of SLAM/CD2 polymorphisms in systemic autoimmunity. Curr. Opin. Immunol. 2010, 22:706-714.
14. Bolland S., Ravetch J.V. Inhibitory pathways triggered by ITIM-containing receptors. Adv. Immunol. 1999, 72:149-177.
15. Bolland S., Pearse R.N., Kurosaki T., Ravetch J.V. SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity 1998, 8:509-516.
16. Nimmerjahn F., Ravetch J.V. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 2008, 8:34-47.
17. Takai T., Ono M., Hikida M., Ohmori H., Ravetch J.V. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 1996, 379:346-349.
18. Bolland S., Ravetch J.V. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 2000, 13:277-285.
19. Tiller T., Kofer J., Kreschel C., Busse C.E., Riebel S., Wickert S., et al. Development of self-reactive germinal center B cells and plasma cells in autoimmune Fc gammaRIIB-deficient mice. J. Exp. Med. 2010, 207:2767-2778.
20. Sato-Hayashizaki A., Ohtsuji M., Lin Q., Hou R., Ohtsuji N., Nishikawa K., et al. Presumptive role of 129 strain-derived Sle16 locus in rheumatoid arthritis in a new mouse model with Fcgamma receptor type IIb-deficient C57BL/6 genetic background. Arthritis Rheum. 2011, 63:2930-2938.
21. Fujii T., Hou R., Sato-Hayashizaki A., Obata M., Ohtsuji M., Ikeda K., et al. Susceptibility loci for the defective foreign protein-induced tolerance in New Zealand Black mice: implication of epistatic effects of Fcgr2b and Slam family genes. Eur. J. Immunol. 2011, 41:2333-2340.
22. Jorgensen T.N., Alfaro J., Enriquez H.L., Jiang C., Loo W.M., Atencio S., et al. Development of murine lupus involves the combined genetic contribution of the SLAM and FcgammaR intervals within the Nba2 autoimmune susceptibility locus. J. Immunol. 2010, 184:775-786.
23. Boross P., Arandhara V.L., Martin-Ramirez J., Santiago-Raber M.L., Carlucci F., Flierman R., et al. The inhibiting Fc receptor for IgG, FcgammaRIIB, is a modifier of autoimmune susceptibility. J. Immunol. 2011, 187:1304-1313.
24. Li F., Smith P., Ravetch J.V. Inhibitory Fcgamma receptor is required for the maintenance of tolerance through distinct mechanisms. J. Immunol. 2014, 192:3021-3028.
25. Shlomchik M.J., Marshak-Rothstein A., Wolfowicz C.B., Rothstein T.L., Weigert M.G. The role of clonal selection and somatic mutation in autoimmunity. Nature 1987, 328:805-811.
26. Meffre E., Wardemann H. B-cell tolerance checkpoints in health and autoimmunity. Curr. Opin. Immunol. 2008, 20:632-638.
27. Wong E.B., Khan T.N., Mohan C., Rahman Z.S. The lupus-prone NZM2410/NZW strain-derived Sle1b sublocus alters the germinal center checkpoint in female mice in a B cell-intrinsic manner. J. Immunol. 2012, 189:5667-5681.
28. Soni C., Wong E.B., Domeier P.P., Khan T.N., Satoh T., Akira S., et al. B cell-intrinsic TLR7 signaling is essential for the development of spontaneous germinal centers. J. Immunol. 2014, 193:4400-4414.
29. Jackson S.W., Scharping N.E., Kolhatkar N.S., Khim S., Schwartz M.A., Li Q.Z., et al. Opposing impact of B cell-intrinsic TLR7 and TLR9 signals on autoantibody repertoire and systemic inflammation. J. Immunol. May 2014, 192:4525-4532.
30. Brink R. The imperfect control of self-reactive germinal center B cells. Curr. Opin. Immunol. 2014, 28:97-101.
31. Li F., Ravetch J.V. Inhibitory Fcgamma receptor engagement drives adjuvant and anti-tumor activities of agonistic CD40 antibodies. Science 2011, 333:1030-1034.
32. Smith P., DiLillo D.J., Bournazos S., Li F., Ravetch J.V. Mouse model recapitulating human Fcgamma receptor structural and functional diversity. Proc. Natl. Acad. Sci. U S A 2012, 109:6181-6186.
33. Heltemes-Harris L., Liu X., Manser T. Progressive surface B cell antigen receptor down-regulation accompanies efficient development of antinuclear antigen B cells to mature, follicular phenotype. J. Immunol. 2004, 172:823-833.
34. Notidis E., Heltemes L., Manser T. Dominant, hierarchical induction of peripheral tolerance during foreign antigen-driven B cell development. Immunity 2002, 17:317-327.
35. Rahman Z.S., Alabyev B., Manser T. FcgammaRIIB regulates autoreactive primary antibody-forming cell, but not germinal center B cell, activity. J. Immunol. 2007, 178:897-907.
36. Nojima T., Haniuda K., Moutai T., Matsudaira M., Mizokawa S., Shiratori I., et al. In-vitro derived germinal centre B cells differentially generate memory B or plasma cells in vivo. Nat. Commun. 2011, 2:465.
37. Wong E.B., Khan T.N., Mohan C., Rahman Z.S. The lupus-prone NZM2410/NZW strain-derived Sle1b sublocus alters the germinal center checkpoint in female mice in a B cell-intrinsic manner. J. Immunol. 2012, 189:5667-5681.
38. Rahman Z.S., Manser T. Failed up-regulation of the inhibitory IgG Fc receptor Fc gamma RIIB on germinal center B cells in autoimmune-prone mice is not associated with deletion polymorphisms in the promoter region of the Fc gamma RIIB gene. J. Immunol. 2005, 175:1440-1449.
39. Rahman Z.S., Niu H., Perry D., Wakeland E., Manser T., Morel L. Expression of the autoimmune Fcgr2b NZW allele fails to be upregulated in germinal center B cells and is associated with increased IgG production. Genes. Immun. 2007, 8:604-612.
40. Jackson S.W., Kolhatkar N.S., Rawlings D.J. B cells take the front seat: dysregulated B cell signals orchestrate loss of tolerance and autoantibody production. Curr. Opin. Immunol. 2015, 33C:70-77.
41. Crotty S. T follicular helper cell differentiation, function, and roles in disease. Immunity 2014, 41:529-542.
42. Zotos D., Tarlinton D.M. Determining germinal centre B cell fate. Trends Immunol. 2012, 33:281-288.
43. Liu D., Xu H., Shih C., Wan Z., Ma X., Ma W., et al. T-B-cell entanglement and ICOSL-driven feed-forward regulation of germinal centre reaction. Nature 2015, 517:214-218.
44. Naito Y., Takematsu H., Koyama S., Miyake S., Yamamoto H., Fujinawa R., et al. Germinal center marker GL7 probes activation-dependent repression of N-glycolylneuraminic acid, a sialic acid species involved in the negative modulation of B-cell activation. Mol. Cell. Biol. 2007, 27:3008-3022.
45. Wong E.B., Soni C., Chan A.Y., Domeier P.P., Shwetank, Abraham T., et al. B Cell-Intrinsic CD84 and Ly108 Maintain Germinal Center B Cell Tolerance. J. Immunol. 2015, 194:4130-4143.
46. Doughty C.A., Bleiman B.F., Wagner D.J., Dufort F.J., Mataraza J.M., Roberts M.F., et al. Antigen receptor-mediated changes in glucose metabolism in B lymphocytes: role of phosphatidylinositol 3-kinase signaling in the glycolytic control of growth. Blood 2006, 107:4458-4465.
47. Dufort F.J., Bleiman B.F., Gumina M.R., Blair D., Wagner D.J., Roberts M.F., et al. Cutting edge: IL-4-mediated protection of primary B lymphocytes from apoptosis via Stat6-dependent regulation of glycolytic metabolism. J. Immunol. 2007, 179:4953-4957.
48. Lee S.K., Silva D.G., Martin J.L., Pratama A., Hu X., Chang P.P., et al. Interferon-gamma excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 2012, 37:880-892.
49. Alabyev B., Rahman Z.S., Manser T. Quantitatively reduced participation of anti-nuclear antigen B cells that down-regulate B cell receptor during primary development in the germinal center/memory B cell response to foreign antigen. J. Immunol. 2007, 178:5623-5634.
50. Vuyyuru R., Mohan C., Manser T., Rahman Z.S. The lupus susceptibility locus Sle1 breaches peripheral B cell tolerance at the antibody-forming cell and germinal center checkpoints. J. Immunol. 2009, 183:5716-5727.
51. Carlucci F., Cortes-Hernandez J., Fossati-Jimack L., Bygrave A.E., Walport M.J., Vyse T.J., et al. Genetic dissection of spontaneous autoimmunity driven by 129-derived chromosome 1 Loci when expressed on C57BL/6 mice. J. Immunol. 2007, 178:2352-2360.
52. Nimmerjahn F., Ravetch J.V. Fcgamma receptors: old friends and new family members. Immunity 2006, 24:19-28.
53. Veillette A. SLAM Family Receptors Regulate Immunity with and without SAP-related adaptors. J. Exp. Med. 2004, 199:1175-1178.
54. Veillette A., Latour S. The SLAM family of immune-cell receptors. Curr. Opin. Immunol. 2003, 15:277-285.
55. Bygrave A.E., Rose K.L., Cortes-Hernandez J., Warren J., Rigby R.J., Cook H.T., et al. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2004, 2:E243.
56. Erickson L.D., Lin L.L., Duan B., Morel L., Noelle R.J. A genetic lesion that arrests plasma cell homing to the bone marrow. Proc. Natl. Acad. Sci. U S A 2003, 100:12905-12910.
57. Kanari Y., Sugahara-Tobinai A., Takahashi H., Inui M., Nakamura A., Hirose S., et al. Dichotomy in FcgammaRIIB deficiency and autoimmune-prone SLAM haplotype clarifies the roles of the Fc receptor in development of autoantibodies and glomerulonephritis. BMC Immunol. 2014, 15:47.
58. Van Montfoort N., t Hoen P.A., Mangsbo S.M., Camps M.G., Boross P., Melief C.J., et al. Fcgamma receptor IIb strongly regulates Fcgamma receptor-facilitated T cell activation by dendritic cells. J. Immunol. 2012, 189:92-101.
59. Cannons J.L., Qi H., Lu K.T., Dutta M., Gomez-Rodriguez J., Cheng J., et al. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010, 32:253-265.
60. Goenka R., Matthews A.H., Zhang B., O'Neill P.J., Scholz J.L., Migone T.S., et al. Local BLyS production by T follicular cells mediates retention of high affinity B cells during affinity maturation. J. Exp. Med. 2013, 211:45-56.
61. Caro-Maldonado A., Wang R., Nichols A.G., Kuraoka M., Milasta S., Sun L.D., et al. Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J. Immunol. 2014, 192:3626-3636.
62. Sharp P.E., Martin-Ramirez J., Mangsbo S.M., Boross P., Pusey C.D., Touw I.P., et al. FcgammaRIIb on myeloid cells and intrinsic renal cells rather than B cells protects from nephrotoxic nephritis. J. Immunol. 2013, 190:340-348.