Protective natural autoantibodies to apoptotic cells: Evidence of convergent selection of recurrent innate-like clones

Annals of the New York Academy of Sciences

Volumn 1362, Issue 1, 2015, Pages 164-175

  Silverman, Gregg J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptotic cell; Apoptotic clearance; B cell; Immunoregulation; Natural antibody

Indexed keywords

AUTOANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN RECEPTOR; PHOSPHORYLCHOLINE;

ANTIBODY RESPONSE; APOPTOSIS; ARTICLE; B CELL LEUKEMIA; B LYMPHOCYTE; CELL CLONE; HOMEOSTASIS; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; HUMAN; IMMUNOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; AUTOANTIBODIES; B-LYMPHOCYTE SUBSETS; HUMANS; IMMUNITY, INNATE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY;

EID: 84959545932     PISSN: 00778923     EISSN: 17496632     Source Type: Journal    
DOI: 10.1111/nyas.12788     Document Type: Article

References (77)

1. Avrameas, S. & C. Selmi. 2013. Natural autoantibodies in the physiology and pathophysiology of the immune system. J. Autoimmun. 41: 46-49.
2. Baumgarth, N. 2011. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11: 34-46.
3. Herzenberg, L.A. & L.A. Herzenberg. 1989. Toward a layered immune system. Cell 59: 953-954.
4. Hayakawa, K. et al. 1999. Positive selection of natural autoreactive B cells. Science 285: 113-116.
5. Cyster, J.G. et al. 1996. Regulation of B-lymphocyte negative and positive selection by tyrosine phosphatase CD45. Nature 381: 325-328.
6. Dighiero, G. et al. 1985. High frequency of natural autoantibodies in normal newborn mice. J. Immunol. 134: 765-771.
7. Merbl, Y. et al. 2007. Newborn humans manifest autoantibodies to defined self molecules detected by antigen microarray informatics. J. Clin. Invest. 117: 712-718.
8. -. J. Exp. Med. 208: 67-80.
9. Li, W., F. Batliwalla & T.L. Rothstein. 2013. Human B-1 cells are not preplasmablasts: analysis of microarray data and other issues. Blood 122: 3691-3693.
10. Cohn, M., G. Notani & S.A. Rice. 1969. Characterization of the antibody to the C-carbohydrate produced by a transplantable mouse plasmacytoma. Immunochemistry 6: 111-123.
11. Potter, M. & M.A. Leon. 1968. Three IgA myeloma immunoglobulins from the BALB/ mouse: precipitation with pneumococcal C polysaccharide. Science 162: 369-371.
12. Potter, M. 1972. Immunoglobulin-producing tumors and myeloma proteins of mice. Physiol. Rev. 52: 631-719.
13. Feeney, A.J. 1991. Predominance of the prototypic T15 anti-phosphorylcholine junctional sequence in neonatal pre-B cells. J. Immunol. 147: 4343-4350.
14. Vakil, M., D.E. Briles & J.F. Kearney. 1991. Antigen-independent selection of T15 idiotype during B-cell ontogeny in mice. Dev. Immunol. 1: 203-212.
15. Solvason, N. et al. 1992. The fetal omentum in mice and humans.A site enriched for precursors of CD5 B cells early in development. Ann. N. Y. Acad. Sci. 651: 10-20.
16. Feeney, A.J. 1992. Predominance of VH-D-JH junctions occurring at sites of short sequence homology results in limited junctional diversity in neonatal antibodies. J. Immunol. 149: 222-229.
17. Perlmutter, R.M. et al. 1985. Developmentally controlled expression of immunoglobulin VH genes. Science 227: 1597-1601.
18. Benedict, C.L. & J.F. Kearney. 1999. Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 10: 607-617.
19. + B lymphocytes. Int. Immunol. 2: 515-520.
20. Silverman, G.J. et al. 2000. Neo-self antigens and the expansion of B-1 cells: lessons from atherosclerosis-prone mice. Curr. Top. Microbiol. Immunol. 252: 189-200.
21. Kearney, J.F. 2005. Innate-like B cells. Springer Semin. Immunopathol. 26: 377-383.
22. Lieberman, R. et al. 1974. Genetics of a new IgVH (T15 idiotype) marker in the mouse regulating natural antibody to phosphorylcholine. J. Exp. Med. 139: 983-1001.
23. Chen, Y. et al. 2009. IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J. Immunol. 182: 6031-6043.
24. Satow, Y. et al. 1986. Phosphocholine binding immunoglobulin Fab McPC603. An X-ray diffraction study at 2.7 A. J. Mol. Biol. 190: 593-604.
25. Mi, Q.S. et al. 2000. Highly reduced protection against Streptococcus pneumoniae after deletion of a single heavy chain gene in mouse. Proc. Natl. Acad. Sci. U. S. A. 97: 6031-6036.
26. McDaniel, L.S. et al. 1984. Blood clearance by anti-phosphocholine antibodies as a mechanism of protection in experimental pneumococcal bacteremia. J. Immunol. 133: 3308-3312.
27. Claflin, J.L., R. Lieberman & J.M. Davie. 1974. Clonal nature of the immune response to phosphorylcholine. I. Specificity, class, and idiotype of phosphorylcholine-binding receptors on lymphoid cells. J. Exp. Med. 139: 58-73.
28. Leon, M.A. & N.M. Young. 1971. Specificity for phosphorylcholine of six murine myeloma proteins reactive with Pneumococcus C polysaccharide and beta-lipoprotein. Biochemistry 10: 1424-1429.
29. Claflin, J.L. & J. Berry. 1988. Genetics of the phosphocholine-specific antibody response to Streptococcus pneumoniae. Germ-line but not mutated T15 antibodies are dominantly selected. J. Immunol. 141: 4012-4019.
30. Clark, S.E. & J.N. Weiser. 2013. Microbial modulation of host immunity with the small molecule phosphorylcholine. Infect. Immun. 81: 392-401.
31. Schenkein, H.A. et al. 2001. Phosphorylcholine-dependent cross-reactivity between dental plaque bacteria and oxidized low-density lipoproteins. Infect. Immun. 69: 6612-6617.
32. Sigal, N.H. et al. 1977. Expression of phosphorylcholine-specific B cells during murine development. J. Exp. Med. 146: 933-948.
33. Sigal, N.H., P.J. Gearhart & N.R. Klinman. 1975. The frequency of phosphorylcholine-specific B cells in conventional and germfree BALB/C mice. J. Immunol. 114: 1354-1358.
34. Palinski, W. et al. 1996. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J. Clin. Invest. 98: 800-814.
35. Shaw, P.X. et al. 2000. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 105: 1731-1740.
36. Binder, C.J. & G.J. Silverman. 2005. Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin. Immunopathol. 26: 385-404.
37. Boullier, A. et al. 2000. The binding of oxidized low density lipoprotein to mouse CD36 is mediated in part by oxidized phospholipids that are associated with both the lipid and protein moieties of the lipoprotein. J. Biol. Chem. 275: 9163-9169.
38. Chou, M.Y. et al. 2009. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Invest. 119: 1335-1349.
39. Wang, C. et al. 2013. Natural antibodies of newborns recognize oxidative stress-related malondialdehyde acetaldehyde adducts on apoptotic cells and atherosclerotic plaques. Int. Immunol. 25: 575-587.
40. Binder, C.J. et al. 2003. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 9: 736-743.
41. Shaw, P.X. et al. 2003. The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neo-antigens and apoptotic cells. J. Immunol. 170: 6151-6157.
42. Friedman, P. et al. 2002. Correlation of antiphospholipid antibody recognition with the structure of synthetic oxidized phospholipids. Importance of Schiff base formation and aldol condensation. J. Biol. Chem. 277: 7010-7020.
43. Korb, L.C. & J.M. Ahearn. 1997. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158: 4525-4528.
44. Ogden, C.A. et al. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194: 781-795.
45. Paidassi, H. et al. 2008. C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition. J. Immunol. 180: 2329-2338.
46. Fraser, D.A. et al. 2009. C1q differentially modulates phagocytosis and cytokine responses during ingestion of apoptotic cells by human monocytes, macrophages, and dendritic cells. J. Immunol. 183: 6175-6185.
47. Matsushita, M. et al. 2004. Origin of the classical complement pathway: lamprey orthologue of mammalian C1q acts as a lectin. Proc. Natl. Acad. Sci. U. S. A. 101: 10127-10131.
48. Stuart, L.M. et al. 2005. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J. Immunol. 174: 3220-3226.
49. Quartier, P. et al. 2005. Predominant role of IgM-dependent activation of the classical pathway in the clearance of dying cells by murine bone marrow-derived macrophages in vitro. Eur. J. Immunol. 35: 252-260.
50. Chen, Y. et al. 2009. Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis. J. Immunol. 183: 1346-1359.
51. Arnold, J.N. et al. 2005. Human serum IgM glycosylation: identification of glycoforms that can bind to mannan-binding lectin. J. Biol. Chem. 280: 29080-29087.
52. Grönwall, C. et al. 2012. MAPK phosphatase-1 is required for regulatory natural autoantibody-mediated inhibition of TLR responses. Proc. Natl. Acad. Sci. U. S. A. 109: 19745-19750.
53. Vas, J. et al. 2012. Natural antibody to apoptotic cell membranes inhibits the proinflammatory properties of lupus autoantibody immune complexes. Arthritis Rheum. 64: 3388-3398.
54. Terato, K. et al. 1992. Induction of arthritis with monoclonal antibodies to collagen. J. Immunol. 148: 2103-2108.
55. Kleinau, S., P. Martinsson & B. Heyman. 2000. Induction and suppression of collagen-induced arthritis is dependent on distinct fcgamma receptors. J. Exp. Med. 191: 1611-1616.
56. Brown, M., G. Schiffman & M.B. Rittenberg. 1984. Subpopulations of antibodies to phosphocholine in human serum. J. Immunol. 132: 1323-1328.
57. Grönwall, C. et al. 2012. IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE. Clin. Immunol. 142: 390-398.
58. Silverman, G.J. et al. 2008. Genetic imprinting of autoantibody repertoires in systemic lupus erythematosus patients. Clin. Exp. Immunol. 153: 102-116.
59. Padilla, N.D. et al. 2004. Levels of natural IgM antibodies against phosphorylcholine in healthy individuals and in patients undergoing isolated limb perfusion. J. Immunol. Methods 293: 1-11.
60. Su, J. et al. 2008. Natural antibodies against phosphorylcholine as potential protective factors in SLE. Rheumatology (Oxford). 47: 1144-1150.
61. deFaire, U. et al. 2010. Low levels of IgM antibodies to phosphorylcholine predict cardiovascular disease in 60-year old men: effects on uptake of oxidized LDL in macrophages as a potential mechanism. J. Autoimmun. 34: 73-79.
62. Fiskesund, R. et al. 2010. Low levels of antibodies against phosphorylcholine predict development of stroke in a population-based study from northern Sweden. Stroke 41: 607-612.
63. Grönwall, C., J. Vas & G.J. Silverman. 2012. Protective Roles of Natural IgM Antibodies. Front. Immunol. 3: 66.
64. Grönwall, C. et al. 2014. Relation of carotid plaque with natural IgM antibodies in patients with systemic lupus erythematosus. Clin. Immunol. 157: 1-7.
65. Smith, G.P. 1985. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228: 1315-1317.
66. Grönwall, C. et al. 2014. Selection of apoptotic cell specific human antibodies from adult bone marrow. PLoS One 9: e95999.
67. Asma, G.E., R.L. vanden Bergh & J.M. Vossen. 1986. Characterization of early lymphoid precursor cells in the human fetus using monoclonal antibodies and anti-terminal deoxynucleotidyl transferase. Clin. Exp. Immunol. 64: 356-363.
68. Ehrenstein, M.R. & C.A. Notley. 2010. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10: 778-786.
69. Fiskesund, R. et al. 2014. Naturally occurring human phosphorylcholine antibodies are predominantly products of affinity-matured B cells in the adult. J. Immunol. 192: 4551-4559.
70. Catera, R. et al. 2008. Chronic lymphocytic leukemia cells recognize conserved epitopes associated with apoptosis and oxidation. Mol. Med. 14: 665-674.
71. Chu, C.C. et al. 2008. Chronic lymphocytic leukemia antibodies with a common stereotypic rearrangement recognize nonmuscle myosin heavy chain IIA. Blood 112: 5122-5129.
72. Silverman, G.J. et al. 1995. Repertoire cloning of human lupus autoantibodies. Ann. N. Y. Acad. Sci. 764: 565-566.
73. Roben, P. et al. 1996. Repertoire cloning of lupus anti-DNA autoantibodies. J. Clin. Invest. 98: 2827-2837.
74. Wang, C. et al. 2015. B-cell repertoire responses to varicella-zoster vaccination in human identical twins. Proc. Natl. Acad. Sci. U. S. A. 112: 500-505.
75. Parameswaran, P. et al. 2013. Convergent antibody signatures in human dengue. Cell Host Microbe 13: 691-700.
76. Jackson, K.J. et al. 2014. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16: 105-114.
77. Xu, J.L. & M.M. Davis. 2000. Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity 13: 37-45.