IgG3 regulates tissue-like memory B cells in HIV-infected individuals

Nature Immunology

Volumn 19, Issue 9, 2018, Pages 1001-1012

  Kardava, Lela ^a   Sohn, Haewon ^a   Youn, Christine ^a   Austin, James W ^a   Wang, Wei ^a   Buckner, Clarisa M ^a   Justement, J Shawn ^a   Melson, Valerie A ^a   Roth, Gwynne E ^a   Hand, Marissa A ^a   Gittens, Kathleen R ^b   Kwan, Richard W ^b   Sneller, Michael C ^a   Li, Yuxing ^c,d   Chun, Tae Wook ^a   Sun, Peter D ^a   Pierce, Susan K ^a   Moir, Susan ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; B LYMPHOCYTE ANTIGEN RECEPTOR; C REACTIVE PROTEIN; COMPLEMENT COMPONENT C1Q; FC RECEPTOR IIB; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M; LYMPHOCYTE ANTIGEN RECEPTOR; UNCLASSIFIED DRUG; FC RECEPTOR; IMMUNOGLOBULIN G; PROTEIN BINDING;

ADULT; ANTIRETROVIRAL THERAPY; ARTICLE; CELL EXPANSION; CELL POPULATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MEMORY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; B LYMPHOCYTE; CAPPING PHENOMENON; CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; MIDDLE AGED; PHYSIOLOGY; YOUNG ADULT;

ADULT; B-LYMPHOCYTES; C-REACTIVE PROTEIN; CELLS, CULTURED; COMPLEMENT C1Q; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOLOGIC MEMORY; IMMUNOMODULATION; MALE; MIDDLE AGED; PROTEIN BINDING; RECEPTOR AGGREGATION; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, IGG; YOUNG ADULT;

EID: 85051945031     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/s41590-018-0180-5     Document Type: Article

References (53)

1. Lane, H. C. et al. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 309, 453–458 (1983).
2. Moir, S. & Fauci, A. S. B-cell responses to HIV infection. Immunol. Rev. 275, 33–48 (2017).
3. Moir, S. et al. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy. Blood 116, 5571–5579 (2010).
4. Moir, S. et al. 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 (2008).
5. Ho, J. et al. Two overrepresented B cell populations in HIV-infected individuals undergo apoptosis by different mechanisms. Proc. Natl. Acad. Sci. USA 103, 19436–19441 (2006).
6. Meffre, E. et al. Maturational characteristics of HIV-specific antibodies in viremic individuals. JCI Insight 1, e84610 (2016).
7. + B cells in human health and disease. Cell. Immunol. 321, 40–45 (2017).
8. Naradikian, M. S., Hao, Y. & Cancro, M. P. Age-associated B cells: key mediators of both protective and autoreactive humoral responses. Immunol. Rev. 269, 118–129 (2016).
9. Portugal, S., Obeng-Adjei, N., Moir, S., Crompton, P. D. & Pierce, S. K. Atypical memory B cells in human chronic infectious diseases: An interim report. Cell. Immunol. 321, 18–25 (2017).
10. Pupovac, A. & Good-Jacobson, K. L. An antigen to remember: regulation of B cell memory in health and disease. Curr. Opin. Immunol. 45, 89–96 (2017).
11. Knox, J. J., Kaplan, D. E. & Betts, M. R. T-bet-expressing B cells during HIV and HCV infections. Cell. Immunol. 321, 26–34 (2017).
12. Barnett, B. E. et al. Cutting edge: B cell-intrinsic T-bet expression is required to control chronic viral infection. J. Immunol. 197, 1017–1022 (2016).
13. + B-cell population is important for the development of autoimmunity. Blood 118, 1305–1315 (2011).
14. Rubtsova, K. et al. B cells expressing the transcription factor T-bet drive lupus-like autoimmunity. J. Clin. Invest. 127, 1392–1404 (2017).
15. Peng, S. L., Szabo, S. J. & Glimcher, L. H. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. USA 99, 5545–5550 (2002).
16. Pekkarinen, P. T. et al. Dysregulation of adaptive immune responses in complement C3-deficient patients. Eur. J. Immunol. 45, 915–921 (2015).
17. Mortensen, R. et al. Adaptive immunity against Streptococcus pyogenes in adults involves increased IFN-γ and IgG3 responses compared with children. J. Immunol. 195, 1657–1664 (2015).
18. + B cells are induced by human viral infections and dominate the HIV gp140 response. JCI Insight 2, e92943 (2017).
19. Buckner, C. M. et al. Characterization of plasmablasts in the blood of HIV-infected viremic individuals: evidence for nonspecific immune activation. J. Virol. 87, 5800–5811 (2013).
20. Roux, K. H., Strelets, L. & Michaelsen, T. E. Flexibility of human IgG subclasses. J. Immunol. 159, 3372–3382 (1997).
21. Lefranc, M. P. & Lefranc, G. Human Gm, Km, and Am allotypes and their molecular characterization: a remarkable demonstration of polymorphism. Methods Mol. Biol. 882, 635–680 (2012).
22. Michaelsen, T. E., Sandlie, I., Bratlie, D. B., Sandin, R. H. & Ihle, O. Structural difference in the complement activation site of human IgG1 and IgG3. Scand. J. Immunol. 70, 553–564 (2009).
23. Morell, A., Terry, W. D. & Waldmann, T. A. Metabolic properties of IgG subclasses in man. J. Clin. Invest. 49, 673–680 (1970).
24. Dugast, A. S. et al. Independent evolution of Fc- and Fab-mediated HIV-1-specific antiviral antibody activity following acute infection. Eur. J. Immunol. 44, 2925–2937 (2014).
25. Chung, A. W. et al. Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology. Cell 163, 988–998 (2015).
26. Scharf, O. et al. Immunoglobulin G3 from polyclonal human immunodeficiency virus (HIV) immune globulin is more potent than other subclasses in neutralizing HIV type 1. J. Virol. 75, 6558–6565 (2001).
27. Yates, N. L. et al. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 6, 228ra39 (2014).
28. Yates, N. L. et al. Multiple HIV-1-specific IgG3 responses decline during acute HIV-1: implications for detection of incident HIV infection. AIDS 25, 2089–2097 (2011).
29. Wesemann, D. R. et al. Immature B cells preferentially switch to IgE with increased direct Sμ to Sε recombination. J. Exp. Med. 208, 2733–2746 (2011).
30. Depoil, D. et al. CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nat. Immunol. 9, 63–72 (2008).
31. Lu, J. et al. Structural recognition and functional activation of FcγR by innate pentraxins. Nature 456, 989–992 (2008).
32. Bang, R. et al. Analysis of binding sites in human C-reactive protein for FcγRI, FcγRIIA, and C1q by site-directed mutagenesis. J. Biol. Chem. 280, 25095–25102 (2005).
33. Bharadwaj, D., Stein, M. P., Volzer, M., Mold, C. & Du Clos, T. W. The major receptor for C-reactive protein on leukocytes is Fcgγ receptor II. J. Exp. Med. 190, 585–590 (1999).
34. Bruhns, P. et al. Specificity and affinity of human Fcγ receptors and their polymorphic variants for human IgG subclasses. Blood 113, 3716–3725 (2009).
35. Seeling, M., Brückner, C. & Nimmerjahn, F. Differential antibody glycosylation in autoimmunity: sweet biomarker or modulator of disease activity? Nat. Rev. Rheumatol. 13, 621–630 (2017).
36. Sjögren, J. et al. EndoS2 is a unique and conserved enzyme of serotype M49 group A Streptococcus that hydrolyses N-linked glycans on IgG and α1-acid glycoprotein. Biochem. J. 455, 107–118 (2013).
37. Noto, A. & Pantaleo, G. B-cell abnormalities and impact on antibody response in HIV infection. Curr. Opin. HIV AIDS 12, 203–208 (2017).
38. Pallikkuth, S., de Armas, L., Rinaldi, S. & Pahwa, S. T follicular helper Cells and B cell dysfunction in aging and HIV-1 infection. Front. Immunol. 8, 1380 (2017).
39. Pierce, S. K. & Liu, W. The tipping points in the initiation of B cell signalling: how small changes make big differences. Nat. Rev. Immunol. 10, 767–777 (2010).
40. Liu, W., Won Sohn, H., Tolar, P., Meckel, T. & Pierce, S. K. Antigen-induced oligomerization of the B cell receptor is an early target of FcγRIIB inhibition. J. Immunol. 184, 1977–1989 (2010).
41. + naive B cells. J. Immunol. 188, 3332–3341 (2012).
42. Sörman, A., Zhang, L., Ding, Z. & Heyman, B. How antibodies use complement to regulate antibody responses. Mol. Immunol. 61, 79–88 (2014).
43. Ugurlar, D. et al. Structures of C1-IgG1 provide insights into how danger pattern recognition activates complement. Science 359, 794–797 (2018).
44. Hogarth, P. M. & Pietersz, G. A. Fc receptor-targeted therapies for the treatment of inflammation, cancer and beyond. Nat. Rev. Drug Discov. 11, 311–331 (2012).
45. Xu, L. et al. Impairment on the lateral mobility induced by structural changes underlies the functional deficiency of the lupus-associated polymorphism FcγRIIB-T232. J. Exp. Med. 213, 2707–2727 (2016).
46. Clatworthy, M. R. et al. Systemic lupus erythematosus-associated defects in the inhibitory receptor FcγRIIb reduce susceptibility to malaria. Proc. Natl. Acad. Sci. USA 104, 7169–7174 (2007).
47. Willcocks, L. C. et al. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 107, 7881–7885 (2010).
48. Son, M., Diamond, B. & Santiago-Schwarz, F. Fundamental role of C1q in autoimmunity and inflammation. Immunol. Res. 63, 101–106 (2015).
49. Nezlin, R., & Ghetie, V. Interactions of immunoglobulins outside the antigen-combining site. Adv. Immunol. 82, 155–215 (2004).
50. Molinos-Albert, L. M., Clotet, B., Blanco, J. & Carrillo, J. Immunologic insights on the membrane proximal external region: a major human immunodeficiency virus type-1 vaccine target. Front. Immunol. 8, 1154 (2017).
51. Sohn, H. W., Krueger, P. D., Davis, R. S. & Pierce, S. K. FcRL4 acts as an adaptive to innate molecular switch dampening BCR signaling and enhancing TLR signaling. Blood 118, 6332–6341 (2011).
52. + B cell line. J. Immunol. 160, 2145–2157 (1998).
53. Brunner, M. & Sigal, L. H. Immune complexes from serum of patients with Lyme disease contain Borrelia burgdorferi antigen and antigen-specific antibodies: potential use for improved testing. J. Infect. Dis. 182, 534–539 (2000).