Diversity, cellular origin and autoreactivity of antibody-secreting cell population expansions in acute systemic lupus erythematosus

Nature Immunology

Volumn 16, Issue 7, 2015, Pages 755-765

  Tipton, Christopher M ^a   Fucile, Christopher F ^b   Darce, Jaime ^c   Chida, Asiya ^a   Ichikawa, Travis ^a   Gregoretti, Ivan ^c   Schieferl, Sandra ^c   Hom, Jennifer ^a   Jenks, Scott ^a   Feldman, Ron J ^a   Mehr, Ramit ^d   Wei, Chungwen ^a   Lee, F Eun Hyung ^e   Cheung, Wan Cheung ^c,f   Rosenberg, Alexander F ^b   Sanz, Iñaki ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c CELL SIGNALING TECHNOLOGY   (United States)

^d BAR ILAN UNIVERSITY   (Israel)

^e EMORY UNIVERSITY   (United States)

^f Pfizer Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN VARIABLE REGION; INFLUENZA VACCINE; PROTEOME; TETANUS TOXOID;

ACUTE DISEASE; ANTIBODY BLOOD LEVEL; ANTIBODY SECRETING CELL; ARTICLE; B LYMPHOCYTE; CD27 POSITIVE MEMORY T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL POPULATION; CLONAL VARIATION; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; DISEASE EXACERBATION; FLOW CYTOMETRY; GERMINAL CENTER; HUMAN; IMMUNE RESPONSE; LIQUID CHROMATOGRAPHY; MEMORY T LYMPHOCYTE; MUTATION RATE; PATHOGENESIS; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEOMICS; SINGLE CELL ANALYSIS; SOMATIC HYPERMUTATION; SYSTEMIC LUPUS ERYTHEMATOSUS; TANDEM MASS SPECTROMETRY; UPREGULATION; AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; BLOOD; CELL CLONE; CELL PROLIFERATION; CLINICAL TRIAL; GENETICS; IMMUNOGLOBULIN PRODUCING CELL; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MULTICENTER STUDY; NUCLEOTIDE SEQUENCE; PROCEDURES; SEQUENCE HOMOLOGY;

ACUTE DISEASE; AMINO ACID SEQUENCE; ANTIBODY DIVERSITY; ANTIBODY-PRODUCING CELLS; AUTOANTIBODIES; B-LYMPHOCYTES; BASE SEQUENCE; CELL PROLIFERATION; CLONE CELLS; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; INFLUENZA VACCINES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MOLECULAR SEQUENCE DATA; PROTEOME; PROTEOMICS; SEQUENCE HOMOLOGY, AMINO ACID; SINGLE-CELL ANALYSIS; TANDEM MASS SPECTROMETRY; TETANUS TOXOID;

EID: 84931424223     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3175     Document Type: Article

References (52)

1. Lee, F.E. et al. Circulating human antibody-secreting cells during vaccinations and respiratory viral infections are characterized by high specificity and lack of bystander effect. J. Immunol. 186, 5514-5521 (2011).
2. Wrammert, J. et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453, 667-671 (2008).
3. Odendahl, M. et al. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J. Immunol. 165, 5970-5979 (2000).
4. Cappione, A. III et al. Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus. J. Clin. Invest. 115, 3205-3216 (2005).
5. Isenberg, D.A. et al. Correlation of 9G4 idiotope with disease activity in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 57, 566-570 (1998).
6. Jackson, K.J. et al. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16, 105-114 (2014).
7. Palanichamy, A. et al. Immunoglobulin class-switched B cells form an active immune axis between CNS and periphery in multiple sclerosis. Sci. Transl. Med. 6, 248ra106 (2014).
8. Stern, J.N. et al. B cells populating the multiple sclerosis brain mature in the draining cervical lymph nodes. Sci. Transl. Med. 6, 248ra107 (2014).
9. Boyd, S.D. et al. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med. 1, 12ra23 (2009).
10. Moody, M.A. et al. HIV-1 gp120 vaccine induces affinity maturation in both new and persistent antibody clonal lineages. J. Virol. 86, 7496-7507 (2012).
11. Dogan, I. et al. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10, 1292-1299 (2009).
12. Breden, F. et al. Comparison of antibody repertoires produced by HIV-1 infection, other chronic and acute infections, and systemic autoimmune disease. PLoS ONE 6, e16857 (2011).
13. Richardson, C. et al. Molecular basis of 9G4 B cell autoreactivity in human systemic lupus erythematosus. J. Immunol. 191, 4926-4939 (2013).
14. Jenks, S.A. et al. 9G4+ autoantibodies are an important source of apoptotic cell reactivity associated with high levels of disease activity in systemic lupus erythematosus. Arthritis Rheum. 65, 3165-3175 (2013).
15. Klinman, D.M. & Steinberg, A.D. Systemic autoimmune disease arises from polyclonal B cell activation. J. Exp. Med. 165, 1755-1760 (1987).
16. Pugh-Bernard, A.E. et al. Regulation of inherently autoreactive VH4-34 B cells in the maintenance of human B cell tolerance. J. Clin. Invest. 108, 1061-1070 (2001).
17. William, J., Euler, C., Christensen, S. & Shlomchik, M.J. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 297, 2066-2070 (2002).
18. Shlomchik, M.J. Sites and stages of autoreactive B cell activation and regulation. Immunity 28, 18-28 doi:10.1016/j.immuni.2007.12.004 (2008).
19. Sweet, R.A., Lee, S.K. & Vinuesa, C.G. Developing connections amongst key cytokines and dysregulated germinal centers in autoimmunity. Curr. Opin. Immunol. 24, 658-664 (2012).
20. Wirths, S. & Lanzavecchia, A. ABCB1 transporter discriminates human resting naive B cells from cycling transitional and memory B cells. Eur. J. Immunol. 35, 3433-3441 (2005).
21. Sims, G.P. et al. Identification and characterization of circulating human transitional B cells. Blood 105, 4390-4398 (2005).
22. Masilamani, M., Kassahn, D., Mikkat, S., Glocker, M.O. & Illges, H. B cell activation leads to shedding of complement receptor type II (CR2/CD21). Eur. J. Immunol. 33, 2391-2397 (2003).
23. Wehr, C. et al. A new CD21low B cell population in the peripheral blood of patients with SLE. Clin. Immunol. 113, 161-171 (2004).
24. William, J., Euler, C. & Shlomchik, M.J. Short-lived plasmablasts dominate the early spontaneous rheumatoid factor response: differentiation pathways, hypermutating cell types, and affinity maturation outside the germinal center. J. Immunol. 174, 6879-6887 (2005).
25. Barak, M., Zuckerman, N.S., Edelman, H., Unger, R. & Mehr, R. IgTree: creating Immunoglobulin variable region gene lineage trees. J. Immunol. Methods 338, 67-74 (2008).
26. 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 328, 805-811 (1987).
27. Cheung, W.C. et al. A proteomics approach for the identification and cloning of monoclonal antibodies from serum. Nat. Biotechnol. 30, 447-452 (2012).
28. Tan, E.M. Antinuclear antibodies: diagnostic markers for autoimmune diseases and probes for cell biology. Adv. Immunol. 44, 93-151 (1989).
29. Sanz, I. & Lee, F.E. B cells as therapeutic targets in SLE. Nat. Rev. Rheumatol 6, 326-337 (2010).
30. Bernasconi, N.L., Traggiai, E. & Lanzavecchia, A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298, 2199-2202 (2002).
31. Gharavi, A.E., Chu, J.L. & Elkon, K.B. Autoantibodies to intracellular proteins in human systemic lupus erythematosus are not due to random polyclonal B cell activation. Arthritis Rheum. 31, 1337-1345 (1988).
32. Choi, J., Kim, S.T. & Craft, J. The pathogenesis of systemic lupus erythematosus-an update. Curr. Opin. Immunol. 24, 651-657 (2012).
33. Bernasconi, N.L., Onai, N. & Lanzavecchia, A. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101, 4500-4504 (2003).
34. Zubler, R.H. & Kanagawa, O. Requirement for three signals in B cell responses. II. Analysis of antigen-and Ia-restricted T helper cell-B cell interaction. J. Exp. Med. 156, 415-429 (1982).
35. Palanichamy, A. et al. Novel human transitional B cell populations revealed by B cell depletion therapy. J. Immunol. 182, 5982-5993 (2009).
36. Hanten, J.A. et al. Comparison of human B cell activation by TLR7 and TLR9 agonists. BMC Immunol. 9, 39 (2008).
37. Yokota, A. et al. Two species of human Fc ε receptor II (FcεRII/CD23): tissue-specific and IL-4-specific regulation of gene expression. Cell 55, 611-618 (1988).
38. Delespesse, G., Sarfati, M. & Peleman, R. Influence of recombinant IL-4, IFN-α, and IFN-γ on the production of human IgE-binding factor (soluble CD23). J. Immunol. 142, 134-138 (1989).
39. Stern, J.N.H. et al. B cells populating the multiple sclerosis brain mature in the draining cervical lymph nodes. Sci. Transl. Med. 6, 248ra107 (2014).
40. Palanichamy, A. et al. Immunoglobulin class-switched B cells form an active immune axis between CNS and periphery in multiple sclerosis. Sci. Transl. Med. 6, 248ra106 (2014).
41. Joo, H. et al. Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation. J. Exp. Med. 209, 1335-1348 (2012).
42. Wardemann, H. et al. Predominant autoantibody production by early human B cell precursors. Science 301, 1374-1377 (2003).
43. Sabouri, Z. et al. Redemption of autoantibodies on anergic B cells by variable-region glycosylation and mutation away from self-reactivity. Proc. Natl. Acad. Sci. USA 111, E2567-E2575 (2014).
44. Mietzner, B. et al. Autoreactive IgG memory antibodies in patients with systemic lupus erythematosus arise from nonreactive and polyreactive precursors. Proc. Natl. Acad. Sci. USA 105, 9727-9732 (2008).
45. Chevrier, S., Kratina, T., Emslie, D., Karnowski, A. & Corcoran, L.M. Germinal center-independent, IgM-mediated autoimmunity in sanroque mice lacking Obf1. Immunol. Cell Biol. 92, 12-19 (2014).
46. Fulcher, D.A. & Basten, A. B cell life span: A review. Immunol. Cell Biol. 75, 446-455 (1997).
47. Cyster, J.G. & Goodnow, C.C. Antigen-induced exclusion from follicles and anergy are separate and complementary processes that influence peripheral B cell fate. Immunity 3, 691-701 (1995).
48. Macallan, D.C. et al. B-cell kinetics in humans: rapid turnover of peripheral blood memory cells. Blood 105, 3633-3640 (2005).
49. Stohl, W. et al. Belimumab reduces autoantibodies, normalizes low complement levels, and reduces select B cell populations in patients with systemic lupus erythematosus. Arthritis Rheum. 64, 2328-2337 (2012).
50. Infantino, S. et al. The tyrosine kinase Lyn limits the cytokine responsiveness of plasma cells to restrict their accumulation in mice. Sci. Signal. 7, 77 (2014).
51. Thaunat, O. et al. Asymmetric segregation of polarized antigen on B cell division shapes presentation capacity. Science 335, 475-479 (2012).
52. Jacobi, A.M. et al. Differential effects of epratuzumab on peripheral blood B cells of patients with systemic lupus erythematosus versus normal controls. Ann. Rheum. Dis. 67, 450-457 (2008).