Defective B cell ontogeny and humoral immune response in mice prematurely expressing human complement receptor 2 (CR2, CD21) is similar to that seen in aging wild type mice

Molecular Immunology

Volumn 46, Issue 10, 2009, Pages 2002-2013

  Twohig, Jason P ^b   Pappworth, Isabel Y ^a   Sivasankar, Baalasubramanian ^b   Kulik, Liudmila ^c   Bull, Melanie ^b   Holers, V Michael ^c   Wang, Eddie C Y ^b   Marchbank, Kevin J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

B lymphocytes; Complement; Transgenic knockout

Indexed keywords

ANTIGEN; COMPLEMENT COMPONENT C2 RECEPTOR; COMPLEMENT COMPONENT C3D RECEPTOR; COMPLEMENT RECEPTOR; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; MOUSE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEEP ERYTHROCYTE; TRANSGENIC MOUSE; WILD TYPE;

ADJUVANTS, IMMUNOLOGIC; AGING; ANIMALS; ANTIBODY FORMATION; ANTIGENS; B-LYMPHOCYTES; ERYTHROCYTES; GERMINAL CENTER; HUMANS; IMMUNE SYSTEM; IMMUNOGLOBULINS; LYMPHOCYTE SUBSETS; MICE; MICE, TRANSGENIC; PHENOTYPE; RECEPTORS, COMPLEMENT 3D; SHEEP; SPLEEN; TIME FACTORS;

MUS; MUS MUSCULUS;

EID: 67349200669     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.03.007     Document Type: Article

References (69)

1. Ahearn J.M., Fischer M.B., Croix D., Goerg S., Ma M., Xia J., Zhou X., Howard R.G., Rothstein T.L., and Carroll M.C. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity 4 (1996) 251-262
2. Bates J.T., Honko A.N., Graff A.H., Kock N.D., and Mizel S.B. Mucosal adjuvant activity of flagellin in aged mice. Mech. Ageing Dev. 129 (2008) 271-281
3. Birrell L., Kulik L., Morgan B.P., Holers V.M., and Marchbank K.J. B cells from mice prematurely expressing human complement receptor type 2 are unresponsive to T-dependent antigens. J. Immunol. 174 (2005) 6974-6982
4. Bouaziz J.D., Yanaba K., and Tedder T.F. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol. Rev. 224 (2008) 201-214
5. Bovbjerg D.H., Kim Y.T., Schwab R., Schmitt K., DeBlasio T., and Weksler M.E. "Cross-wiring" of the immune response in old mice: increased autoantibody response despite reduced antibody response to nominal antigen. Cell. Immunol. 135 (1991) 519-525
6. Bradbury L.E., Kansas G.S., Levy S., Evans R.L., and Tedder T.F. The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J. Immunol. 149 (1992) 2841-2850
7. Carroll M.C. The role of complement in B cell activation and tolerance. Adv. Immunol. 74 (2000) 61-88
8. Doria G., D'Agostaro G., and Poretti A. Age-dependent variations of antibody avidity. Immunology 35 (1978) 601-611
9. Fearon D.T., and Carter R.H. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu. Rev. Immunol. 13 (1995) 127-149
10. Fischer M.B., Ma M., Goerg S., Zhou X., Xia J., Finco O., Han S., Kelsoe G., Howard R.G., Rothstein T.L., Kremmer E., Rosen F.S., and Carroll M.C. Regulation of the B cell response to T-dependent antigens by classical pathway complement. J. Immunol. 157 (1996) 549-556
11. Franceschi C., Monti D., Sansoni P., and Cossarizza A. The immunology of exceptional individuals: the lesson of centenarians. Immunol. Today 16 (1995) 12-16
12. Fulop Jr. T. Signal transduction changes in granulocytes and lymphocytes with ageing. Immunol. Lett. 40 (1994) 259-268
13. Fulop Jr. T., Gagne D., Goulet A.C., Desgeorges S., Lacombe G., Arcand M., and Dupuis G. Age-related impairment of p56lck and ZAP-70 activities in human T lymphocytes activated through the TcR/CD3 complex. Exp. Gerontol. 34 (1999) 197-216
14. Gahring L.C., and Weigle W.O. The effect of aging on the induction of humoral and cellular immunity and tolerance in two long-lived mouse strains. Cell. Immunol. 128 (1990) 142-151
15. Gajewski T.F., Qian D., Fields P., and Fitch F.W. Anergic T-lymphocyte clones have altered inositol phosphate, calcium, and tyrosine kinase signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 38-42
16. Ghosh J., and Miller R.A. Rapid tyrosine phosphorylation of Grb2 and Shc in T cells exposed to anti-CD3, anti-CD4, and anti-CD45 stimuli: differential effects of aging. Mech. Ageing Dev. 80 (1995) 171-187
17. Goidl E.A., Innes J.B., and Weksler M.E. Immunological studies of aging. II. Loss of IgG and high avidity plaque-forming cells and increased suppressor cell activity in aging mice. J. Exp. Med. 144 (1976) 1037-1048
18. Gustavsson S., Kinoshita T., and Heyman B. Antibodies to murine complement receptor 1 and 2 can inhibit the antibody response in vivo without inhibiting T helper cell induction. J. Immunol. 154 (1995) 6524-6528
19. Haas K.M., Hasegawa M., Steeber D.A., Poe J.C., Zabel M.D., Bock C.B., Karp D.R., Briles D.E., Weis J.H., and Tedder T.F. Complement receptors CD21/35 link innate and protective immunity during Streptococcus pneumoniae infection by regulating IgG3 antibody responses. Immunity 17 (2002) 713-723
20. Hayashi Y., Kurashima C., Utsuyama M., and Hirokawa K. An animal model of autoimmune sialadenitis in aged mice. Pathol. Immunopathol. Res. 8 (1989) 118-124
21. Hebell T., Ahearn J.M., and Fearon D.T. Suppression of the immune response by a soluble complement receptor of B lymphocytes. Science 254 (1991) 102-105
22. Heyman B., Wiersma E.J., and Kinoshita T. In vivo inhibition of the antibody response by a complement receptor-specific monoclonal antibody. J. Exp. Med. 172 (1990) 665-668
23. Holers V.M. Complement receptors and the shaping of the natural antibody repertoire. Springer Semin. Immunopathol. 26 (2005) 405-423
24. Hu A., Ehleiter D., Ben-Yehuda A., Schwab R., Russo C., Szabo P., and Weksler M.E. Effect of age on the expressed B cell repertoire: role of B cell subsets. Int. Immunol. 5 (1993) 1035-1039
25. Johnson K.M., Owen K., and Witte P.L. Aging and developmental transitions in the B cell lineage. Int. Immunol. 14 (2002) 1313-1323
26. Johnson S.A., and Cambier J.C. Ageing, autoimmunity and arthritis: senescence of the B cell compartment-implications for humoral immunity. Arthritis Res. Ther. 6 (2004) 131-139
27. Johnson S.A., Rozzo S.J., and Cambier J.C. Aging-dependent exclusion of antigen-inexperienced cells from the peripheral B cell repertoire. J. Immunol. 168 (2002) 5014-5023
28. Kirman I., Zhao K., Wang Y., Szabo P., Telford W., and Weksler M.E. Increased apoptosis of bone marrow pre-B cells in old mice associated with their low number. Int. Immunol. 10 (1998) 1385-1392
29. Kishimoto S., Takahama T., and Mizumachi H. In vitro immune response to the 2,4,6-trinitrophenyl determinant in aged C57BL/6J mice: changes in the humoral immune response to, avidity for the TNP determinant and responsiveness to LPS effect with aging. J. Immunol. 116 (1976) 294-300
30. Kline G.H., Hayden T.A., and Klinman N.R. B cell maintenance in aged mice reflects both increased B cell longevity and decreased B cell generation. J. Immunol. 162 (1999) 3342-3349
31. Koch S., Solana R., Dela Rosa O., and Pawelec G. Human cytomegalovirus infection and T cell immunosenescence: a mini review. Mech. Ageing Dev. 127 (2006) 538-543
32. Krogsrud R.L., and Perkins E.H. Age-related changes in T cell function. J. Immunol. 118 (1977) 1607-1611
33. Kulik L., Marchbank K.J., Lyubchenko T., Kuhn K.A., Liubchenko G.A., Haluszczak C., Gibson M.G., Boackle S.A., and Holers V.M. Intrinsic B cell hypo-responsiveness in mice prematurely expressing human CR2/CD21 during B cell development. Eur. J. Immunol. 37 (2007) 623-633
34. Maletto B., Ropolo A., Moron V., and Pistoresi-Palencia M.C. CpG-DNA stimulates cellular and humoral immunity and promotes Th1 differentiation in aged BALB/c mice. J. Leukoc. Biol. 72 (2002) 447-454
35. Marchbank K.J., Kulik L., Gipson M.G., Morgan B.P., and Holers V.M. Expression of human complement receptor type 2 (CD21) in mice during early B cell development results in a reduction in mature B cells and hypogammaglobulinemia. J. Immunol. 169 (2002) 3526-3535
36. Marchbank K.J., Watson C.C., Ritsema D.F., and Holers V.M. Expression of human complement receptor 2 (CR2, CD21) in Cr2-/-mice restores humoral immune function. J. Immunol. 165 (2000) 2354-2361
37. Matsumoto A.K., Kopicky-Burd J., Carter R.H., Tuveson D.A., Tedder T.F., and Fearon D.T. Intersection of the complement and immune systems: a signal transduction complex of the B lymphocyte-containing complement receptor type 2 and CD19. J. Exp. Med. 173 (1991) 55-64
38. Matsushita T., Yanaba K., Bouaziz J.D., Fujimoto M., and Tedder T.F. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118 (2008) 3420-3430
39. Miller C., and Kelsoe G. Ig VH hypermutation is absent in the germinal centers of aged mice. J. Immunol. 155 (1995) 3377-3384
40. Miller R.A. The aging immune system: primer and prospectus. Science 273 (1996) 70-74
41. Miller R.A. Effect of aging on T lymphocyte activation. Vaccine 18 (2000) 1654-1660
42. Molina H., Holers V.M., Li B., Fung Y., Mariathasan S., Goellner J., Strauss-Schoenberger J., Karr R.W., and Chaplin D.D. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 3357-3361
43. Nel A.E. T-cell activation through the antigen receptor. Part 1. Signaling components, signaling pathways, and signal integration at the T-cell antigen receptor synapse. J. Allergy Clin. Immunol. 109 (2002) 758-770
44. Nel A.E., and Slaughter N. T-cell activation through the antigen receptor. Part 2. Role of signaling cascades in T-cell differentiation, anergy, immune senescence, and development of immunotherapy. J. Allergy Clin. Immunol. 109 (2002) 901-915
45. Nicoletti C., Borghesi-Nicoletti C., Yang X.H., Schulze D.H., and Cerny J. Repertoire diversity of antibody response to bacterial antigens in aged mice. II. Phosphorylcholine-antibody in young and aged mice differ in both VH/VL gene repertoire and in specificity. J. Immunol. 147 (1991) 2750-2755
46. Pappworth I.Y., Kulik L., Haluszczak C., Reuter J.W., Holers V.M., and Marchbank K.J. Increased B cell deletion and significantly reduced auto-antibody titre due to premature expression of human complement receptor 2 (CR2, CD21). Mol. Immunol. (2009)
47. Pawelec G., Hirokawa K., and Fulop T. Altered T cell signalling in ageing. Mech. Ageing Dev. 122 (2001) 1613-1637
48. Pillai S., Cariappa A., and Moran S.T. Marginal zone B cells. Annu. Rev. Immunol. 23 (2005) 161-196
49. Prodeus A.P., Goerg S., Shen L.M., Pozdnyakova O.O., Chu L., Alicot E.M., Goodnow C.C., and Carroll M.C. A critical role for complement in maintenance of self-tolerance. Immunity 9 (1998) 721-731
50. Riley S.C., Froscher B.G., Linton P.J., Zharhary D., Marcu K., and Klinman N.R. Altered VH gene segment utilization in the response to phosphorylcholine by aged mice. J. Immunol. 143 (1989) 3798-3805
51. Schwab R., Walters C.A., and Weksler M.E. Host defense mechanisms and aging. Semin. Oncol. 16 (1989) 20-27
52. Sen G., Chen Q., and Snapper C.M. Immunization of aged mice with a pneumococcal conjugate vaccine combined with an unmethylated CpG-containing oligodeoxynucleotide restores defective immunoglobulin G antipolysaccharide responses and specific CD4+-T-cell priming to young adult levels. Infect. Immun. 74 (2006) 2177-2186
53. Sherwood E.M., Xu W., King A.M., Blomberg B.B., and Riley R.L. The reduced expression of surrogate light chains in B cell precursors from senescent BALB/c mice is associated with decreased E2A proteins. Mech. Ageing Dev. 118 (2000) 45-59
54. Sherwood E.M., Xu W., and Riley R.L. B cell precursors in senescent mice exhibit decreased recruitment into proliferative compartments and altered expression of Bcl-2 family members. Mech. Ageing Dev. 124 (2003) 147-153
55. Srivastava B., Quinn III W.J., Hazard K., Erikson J., and Allman D. Characterization of marginal zone B cell precursors. J. Exp. Med. 202 (2005) 1225-1234
56. Szakal A.K., Taylor J.K., Smith J.P., Kosco M.H., Burton G.F., and Tew J.J. Kinetics of germinal center development in lymph nodes of young and aging immune mice. Anat. Rec. 227 (1990) 475-485
57. Takahashi K., Kozono Y., Waldschmidt T.J., Berthiaume D., Quigg R.J., Baron A., and Holers V.M. Mouse complement receptors type 1 (CR1; CD35) and type 2 (CR2; CD21): expression on normal B cell subpopulations and decreased levels during the development of autoimmunity in MRL/lpr mice. J. Immunol. 159 (1997) 1557-1569
58. Tedder T.F., Clement L.T., and Cooper M.D. Expression of C3d receptors during human B cell differentiation: immunofluorescence analysis with the HB-5 monoclonal antibody. J. Immunol. 133 (1984) 678-683
59. Tedder T.F., Zhou L.J., and Engel P. The CD19/CD21 signal transduction complex of B lymphocytes. Immunol. Today 15 (1994) 437-442
60. Thyphronitis G., Kinoshita T., Inoue K., Schweinle J.E., Tsokos G.C., Metcalf E.S., Finkelman F.D., and Balow J.E. Modulation of mouse complement receptors 1 and 2 suppresses antibody responses in vivo. J. Immunol. 147 (1991) 224-230
61. Twohig J., Kulik L., Haluszczak C., Reuter J., Rossbach A., Bull M., Holers V.M., and Marchbank K.J. Defective B cell ontogeny and immune response in human complement receptor 2 (CR2, CD21) transgenic mice is partially recovered in the absence of C3. Mol. Immunol. 44 (2007) 3434-3444
62. Weksler M.E. Changes in the B-cell repertoire with age. Vaccine 18 (2000) 1624-1628
63. Weksler M.E., Russo C., and Siskind G.W. Peripheral T cells select the B-cell repertoire in old mice. Immunol. Rev. 110 (1989) 173-185
64. Wessels M.R., Butko P., Ma M., Warren H.B., Lage A.L., and Carroll M.C. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 11490-11494
65. Wu X., Jiang N., Fang Y.F., Xu C., Mao D., Singh J., Fu Y.X., and Molina H. Impaired affinity maturation in Cr2-/- mice is rescued by adjuvants without improvement in germinal center development. J. Immunol. 165 (2000) 3119-3127
66. Yanaba K., Bouaziz J.D., Haas K.M., Poe J.C., Fujimoto M., and Tedder T.F. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28 (2008) 639-650
67. Yang X., Stedra J., and Cerny J. Relative contribution of T and B cells to hypermutation and selection of the antibody repertoire in germinal centers of aged mice. J. Exp. Med. 183 (1996) 959-970
68. Zhao K.S., Wang Y.F., Gueret R., and Weksler M.E. Dysregulation of the humoral immune response in old mice. Int. Immunol. 7 (1995) 929-934
69. Zharhary D., Segev Y., and Gershon H. The affinity and spectrum of cross reactivity of antibody production in senescent mice: the IgM response. Mech. Ageing Dev. 6 (1977) 385-392