Age-associated B cells: A T-bet-dependent effector with roles in protective and pathogenic immunity

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 1933-1937

  Rubtsova, Kira ^a,b,c   Rubtsov, Anatoly V ^a,b,c   Cancro, Michael P ^d   Marrack, Philippa ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b DEPARTMENT OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BREAKPOINT CLUSTER REGION PROTEIN; CD23 ANTIGEN; CD5 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; COMPLEMENT COMPONENT C3D RECEPTOR; FAS ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SYNDECAN 1; TOLL LIKE RECEPTOR 7; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR ALPHA; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

ADAPTIVE IMMUNITY; AGE ASSOCIATED B CELL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN PRESENTATION; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL FATE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOLOGY; IMMUNOREACTIVITY; INNATE IMMUNITY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENESCENCE; TH17 CELL; UPREGULATION; VIRAL CLEARANCE; VIRUS INFECTION; VIRUS LOAD; AGING; ANIMAL; BIOLOGICAL MODEL; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

AGING; ANIMALS; AUTOIMMUNITY; B-LYMPHOCYTE SUBSETS; HUMANS; INFLAMMATION; MICE; MODELS, IMMUNOLOGICAL; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

EID: 84940118728     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501209     Document Type: Review

References (55)

1. Ben-Yehuda, A., and M. E. Weksler. 1992. Immune senescence: mechanisms and clinical implications. Cancer Invest. 10: 525-531.
2. Pawelec, G. 2003. Immunosenescence and human longevity. Biogerontology 4: 167-170.
3. Miller, R. A. 1996. The aging immune system: primer and prospectus. Science 273: 70-74.
4. Doria, G., and D. Frasca. 1997. Genes, immunity, and senescence: looking for a link. Immunol. Rev. 160: 159-170.
5. Franceschi, C., M. Passeri, G. De Benedictis, and L. Motta. 1998. Immunosenescence. Aging (Milano) 10: 153-154.
6. Johnson, S. A., and J. C. Cambier. 2004. Ageing, autoimmunity and arthritis: senescence of the B cell compartment - implications for humoral immunity. Arthritis Res. Ther. 6: 131-139.
7. Franceschi, C., and M. Bonafè. 2003. Centenarians as a model for healthy aging. Biochem. Soc. Trans. 31: 457-461.
8. Franceschi, C., and J. Campisi. 2014. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol. A Biol. Sci. Med. Sci. 69(Suppl. 1): S4-S9.
9. Dolcetti, R., and M. Boiocchi. 1996. Cellular and molecular bases of B-cell clonal expansions. Clin. Exp. Rheumatol. 14(Suppl. 14): S3-S13.
10. LeMaoult, J., S. Delassus, R. Dyall, J. Nikolić-Zugić, P. Kourilsky, and M. E. Weksler. 1997. Clonal expansions of B lymphocytes in old mice. J. Immunol. 159: 3866-3874.
11. LeMaoult, J., I. Messaoudi, J. S. Manavalan, H. Potvin, D. Nikolich-Zugich, R. Dyall, P. Szabo, M. E. Weksler, and J. Nikolich-Zugich. 2000. Age-related dysregulation in CD8 T cell homeostasis: kinetics of a diversity loss. J. Immunol. 165: 2367-2373.
12. Eaton-Bassiri, A. S., L. Mandik-Nayak, S. J. Seo, M. P. Madaio, M. P. Cancro, and J. Erikson. 2000. Alterations in splenic architecture and the localization of antidouble-stranded DNA B cells in aged mice. Int. Immunol. 12: 915-926.
13. Zediak, V. P., I. Maillard, and A. Bhandoola. 2007. Multiple prethymic defects underlie age-related loss of T progenitor competence. Blood 110: 1161-1167.
14. Miller, J. P., and D. Allman. 2003. The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J. Immunol. 171: 2326-2330.
15. Labrie, J. E., III, A. P. Sah, D. M. Allman, M. P. Cancro, and R. M. Gerstein. 2004. Bone marrow microenvironmental changes underlie reduced RAG-mediated recombination and B cell generation in aged mice. J. Exp. Med. 200: 411-423.
16. Sherwood, E. M., B. B. Blomberg, W. Xu, C. A. Warner, and R. L. Riley. 1998. Senescent BALB/c mice exhibit decreased expression of lambda5 surrogate light chains and reduced development within the pre-B cell compartment. J. Immunol. 161: 4472-4475.
17. Frasca, D., E. Van Der Put, R. L. Riley, and B. B. Blomberg. 2004. Age-related differences in the E2A-encoded transcription factor E47 in bone marrow-derived B cell precursors and in splenic B cells. Exp. Gerontol. 39: 481-489.
18. Stephan, R. P., D. A. Lill-Elghanian, and P. L. Witte. 1997. Development of B cells in aged mice: decline in the ability of pro-B cells to respond to IL-7 but not to other growth factors. J. Immunol. 158: 1598-1609.
19. Stephan, R. P., V. M. Sanders, and P. L. Witte. 1996. Stage-specific alterations in murine B lymphopoiesis with age. Int. Immunol. 8: 509-518.
20. Kline, G. H., T. A. Hayden, and N. R. Klinman. 1999. B cell maintenance in aged mice reflects both increased B cell longevity and decreased B cell generation. J. Immunol. 162: 3342-3349.
21. Tsukamoto, H., K. Clise-Dwyer, G. E. Huston, D. K. Duso, A. L. Buck, L. L. Johnson, L. Haynes, and S. L. Swain. 2009. Age-associated increase in lifespan of naive CD4 T cells contributes to T-cell homeostasis but facilitates development of functional defects. Proc. Natl. Acad. Sci. USA 106: 18333-18338.
22. Hao, Y., P. O'Neill, M. S. Naradikian, J. L. Scholz, and M. P. Cancro. 2011. A B-cell subset uniquely responsive to innate stimuli accumulates in aged mice. Blood 118: 1294-1304.
23. Rubtsov, A. V., K. Rubtsova, A. Fischer, R. T. Meehan, J. Z. Gillis, J. W. Kappler, and P. Marrack. 2011. Toll-like receptor 7 (TLR7)-driven accumulation of a novel CD11c+ B-cell population is important for the development of autoimmunity. Blood 118: 1305-1315.
24. Birjandi, S. Z., J. A. Ippolito, A. K. Ramadorai, and P. L. Witte. 2011. Alterations in marginal zone macrophages and marginal zone B cells in old mice. J. Immunol. 186: 3441-3451.
25. Rubtsova, K., A. V. Rubtsov, L. F. Van Dyk, J. W. Kappler, and P. Marrack. 2013. T-box transcription factor T-bet, a key player in a unique type of B-cell activation essential for effective viral clearance. Proc. Natl. Acad. Sci. USA 110: E3216-E3224.
26. Ehrhardt, G. R., A. Hijikata, H. Kitamura, O. Ohara, J. Y. Wang, and M. D. Cooper. 2008. Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 205: 1807-1817.
27. Ratliff, M., S. Alter, D. Frasca, B. B. Blomberg, and R. L. Riley. 2013. In senescence, age-associated B cells secrete TNFα and inhibit survival of B-cell precursors. Aging Cell 12: 303-311.
28. Gerth, A. J., L. Lin, and S. L. Peng. 2003. T-bet regulates T-independent IgG2a class switching. Int. Immunol. 15: 937-944.
29. Ehlers, M., H. Fukuyama, T. L. McGaha, A. Aderem, and J. V. Ravetch. 2006. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J. Exp. Med. 203: 553-561.
30. Carrel, L., and H. F. Willard. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
31. Wang, N. S., L. J. McHeyzer-Williams, S. L. Okitsu, T. P. Burris, S. L. Reiner, and M. G. McHeyzer-Williams. 2012. Divergent transcriptional programming of classspecific B cell memory by T-bet and RORa. Nat. Immunol. 13: 604-611.
32. Peng, S. L., S. J. Szabo, and L. H. Glimcher. 2002. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. USA 99: 5545-5550.
33. Rubtsov, A. V., K. Rubtsova, J. W. Kappler, J. Jacobelli, R. S. Friedman, and P. Marrack. 2015. CD11c-expressing B cells are located at the T cell/B cell border in spleen and are potent APCs. J. Immunol. 195: 71-79.
34. Keren, Z., S. Naor, S. Nussbaum, K. Golan, T. Itkin, Y. Sasaki, M. Schmidt- Supprian, T. Lapidot, and D. Melamed. 2011. B-cell depletion reactivates B lymphopoiesis in the BM and rejuvenates the B lineage in aging. Blood 117: 3104-3112.
35. Goenka, R., J. L. Scholz, M. S. Naradikian, and M. P. Cancro. 2014. Memory B cells form in aged mice despite impaired affinity maturation and germinal center kinetics. Exp. Gerontol. 54: 109-115.
36. Lefebvre, J. S., A. C. Maue, S. M. Eaton, P. A. Lanthier, M. Tighe, and L. Haynes. 2012. The aged microenvironment contributes to the age-related functional defects of CD4 T cells in mice. Aging Cell 11: 732-740.
37. Yates, J. L., R. Racine, K. M. McBride, and G. M. Winslow. 2013. T celldependent IgM memory B cells generated during bacterial infection are required for IgG responses to antigen challenge. J. Immunol. 191: 1240-1249.
38. Kipps, T. J., P. Parham, J. Punt, and L. A. Herzenberg. 1985. Importance of immunoglobulin isotype in human antibody-dependent, cell-mediated cytotoxicity directed by murine monoclonal antibodies. J. Exp. Med. 161: 1-17.
39. Coutelier, J. P., J. T. van der Logt, F. W. Heessen, A. Vink, and J. van Snick. 1988. Virally induced modulation of murine IgG antibody subclasses. J. Exp. Med. 168: 2373-2378.
40. Nimmerjahn, F., P. Bruhns, K. Horiuchi, and J. V. Ravetch. 2005. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23: 41-51.
41. Markine-Goriaynoff, D., and J. P. Coutelier. 2002. Increased efficacy of the immunoglobulin G2a subclass in antibody-mediated protection against lactate dehydrogenase-elevating virus-induced polioencephalomyelitis revealed with switch mutants. J. Virol. 76: 432-435.
42. Larson, J. D., J. M. Thurman, A. V. Rubtsov, D. Claypool, P. Marrack, L. F. Van Dyk, R. M. Torres, and R. Pelanda. 2012. Murine gammaherpesvirus 68 infection protects lupus-prone mice from the development of autoimmunity. Proc. Natl. Acad. Sci. USA 109: E1092-E1100.
43. Rakhmanov, M., B. Keller, S. Gutenberger, C. Foerster, M. Hoenig, G. Driessen, M. van der Burg, J. J. van Dongen, E. Wiech, M. Visentini, et al. 2009. Circulating CD21low B cells in common variable immunodeficiency resemble tissue homing, innate-like B cells. Proc. Natl. Acad. Sci. USA 106: 13451-13456.
44. Isnardi, I., Y. S. Ng, L. Menard, G. Meyers, D. Saadoun, I. Srdanovic, J. Samuels, J. Berman, J. H. Buckner, C. Cunningham-Rundles, and E. Meffre. 2010. Complement receptor 2/CD21- human naive B cells contain mostly autoreactive unresponsive clones. Blood 115: 5026-5036.
45. Warnatz, K., C. Wehr, R. Dräger, S. Schmidt, H. Eibel, M. Schlesier, and H. H. Peter. 2002. Expansion of CD19(hi)CD21(lo/neg) B cells in common variable immunodeficiency (CVID) patients with autoimmune cytopenia. Immunobiology 206: 502-513.
46. Wehr, C., H. Eibel, M. Masilamani, H. Illges, M. Schlesier, H. H. Peter, and K. Warnatz. 2004. A new CD21low B cell population in the peripheral blood of patients with SLE. Clin. Immunol. 113: 161-171.
47. Moir, S., J. Ho, A. Malaspina, W. Wang, A. C. DiPoto, M. A. O'Shea, G. Roby, S. Kottilil, J. Arthos, M. A. Proschan, et al. 2008. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 205: 1797-1805.
48. Wherry, E. J., S. J. Ha, S. M. Kaech, W. N. Haining, S. Sarkar, V. Kalia, S. Subramaniam, J. N. Blattman, D. L. Barber, and R. Ahmed. 2007. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
49. Giltiay, N. V., C. P. Chappell, X. Sun, N. Kolhatkar, T. H. Teal, A. E. Wiedeman, J. Kim, L. Tanaka, M. B. Buechler, and J. A. Hamerman, et al. 2013. Over-expression of TLR7 promotes cell-intrinsic expansion and autoantibody production by transitional T1 B cells. J. Exp. Med. 210: 2773-2789.
50. Allman, D., and S. Pillai. 2008. Peripheral B cell subsets. Curr. Opin. Immunol. 20: 149-157.
51. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
52. Jacob, C. O., P. H. van der Meide, and H. O. McDevitt. 1987. In vivo treatment of (NZB X NZW)F1 lupus-like nephritis with monoclonal antibody to gamma interferon. J. Exp. Med. 166: 798-803.
53. Balomenos, D., R. Rumold, and A. N. Theofilopoulos. 1998. Interferon-gamma is required for lupus-like disease and lymphoaccumulation in MRL-lpr mice. J. Clin. Invest. 101: 364-371.
54. Ytterberg, S. R., and T. J. Schnitzer. 1982. Serum interferon levels in patients with systemic lupus erythematosus. Arthritis Rheum. 25: 401-406.
55. Christensen, S. R., J. Shupe, K. Nickerson, M. Kashgarian, R. A. Flavell, and M. J. Shlomchik. 2006. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 25: 417-428.