B in TB: B Cells as Mediators of Clinically Relevant Immune Responses in Tuberculosis

Clinical Infectious Diseases

Volumn 61, Issue , 2015, Pages S225-S234

  Rao, Martin ^a   Valentini, Davide ^a,b   Poiret, Thomas ^a   Dodoo, Ernest ^a   Parida, Shreemanta ^a   Zumla, Alimuddin ^c   Brighenti, Susanna ^a   Maeurer, Markus ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

antibodies; B cells; cytokines; host directed therapy; Tuberculosis

Indexed keywords

EPITOPE; IMMUNOGLOBULIN G; PEPTIDE; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY; CYTOKINE; PEPTIDE LIBRARY;

ANTIBODY RESPONSE; ANTIGENICITY; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BONE MARROW CELL; DISEASE COURSE; GRANULOMA; HUMAN; HUMORAL IMMUNITY; IMMUNOTHERAPY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MICROARRAY; SERODIAGNOSIS; SPUTUM; TUBERCULOSIS; CELLULAR IMMUNITY; IMMUNOLOGY; PEPTIDE LIBRARY; PHYSIOLOGY;

ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; B-LYMPHOCYTES; CYTOKINES; EPITOPES, B-LYMPHOCYTE; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; MYCOBACTERIUM TUBERCULOSIS; PEPTIDE LIBRARY; TUBERCULOSIS;

EID: 84943383932     PISSN: 10584838     EISSN: 15376591     Source Type: Journal    
DOI: 10.1093/cid/civ614     Document Type: Article

References (71)

1. World Health Organization. Global tuberculosis report 2014. Geneva, Switzerland: WHO, 2014.
2. Zumla A, Rao M, Parida SK, et al. Inflammation and tuberculosis: hostdirected therapies. J Intern Med 2015; 277:373-87.
3. Zumla A, Maeurer M. Rational development of adjunct immune-based therapies for drug-resistant tuberculosis: hypotheses and experimental designs. J Infect Dis 2012; 205(suppl 2):S335-9.
4. Brighenti S, Andersson J. Local immune responses in human tuberculosis: learning from the site of infection. J Infect Dis 2012; 205(suppl 2): S316-24.
5. Achkar JM, Chan J, Casadevall A. Role of B cells and antibodies in acquired immunity against Mycobacterium tuberculosis. Cold Spring Harb Perspect Med 2014; 5:a018432.
6. O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MP. The immune response in tuberculosis. Annu Rev Immunol 2013; 31:475-527.
7. Ehlers S, Schaible UE. The granuloma in tuberculosis: dynamics of a host-pathogen collusion. Front Immunol 2012; 3:411.
8. Das B, Kashino SS, Pulu I, et al. CD271(+) bone marrow mesenchymal stem cells may provide a niche for dormant Mycobacterium tuberculosis. Sci Transl Med 2013; 5:170-13.
9. Kozakiewicz L, Phuah J, Flynn J, Chan J. The role of B cells and humoral immunity in Mycobacterium tuberculosis infection. Adv Exp Med Biol 2013; 783:225-50.
10. Chan J, Mehta S, Bharrhan S, et al. The role of B cells and humoral immunity in Mycobacterium tuberculosis infection. Semin Immunol 2014; 26:588-600.
11. Bao Y, Liu X, Han C, et al. Identification of IFN-gamma-producing innate B cells. Cell Res 2014; 24:161-76.
12. Lund FE. Cytokine-producing B lymphocytes-key regulators of immunity. Curr Opin Immunol 2008; 20:332-8.
13. Zhang M, Zheng X, Zhang J, et al. CD19(+)CD1d(+)CD5(+) B cell frequencies are increased in patients with tuberculosis and suppress Th17 responses. Cell Immunol 2012; 274:89-97.
14. Olivares N, Marquina B, Mata-Espinoza D, et al. The protective effect of immunoglobulin in murine tuberculosis is dependent on IgG glycosylation. Pathog Dis 2013; 69:176-83.
15. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature 1985; 314:537-9.
16. Abbas AK, Lichtman AH, Pillai S. Basic immunology: functions and disorders of the immune system. 4th ed. Philadelphia: Elsevier Saunders, 2014:320.
17. Achkar JM, Casadevall A. Antibody-mediated immunity against tuberculosis: implications for vaccine development. Cell Host Microbe 2013; 13:250-62.
18. Rodriguez A, Tjarnlund A, Ivanji J, et al. Role of IgA in the defense against respiratory infections IgA deficient mice exhibited increased susceptibility to intranasal infection with Mycobacterium bovis BCG. Vaccine 2005; 23:2565-72.
19. Manivannan S, Rao NV, Ramanathan VD. Role of complement activation and antibody in the interaction between Mycobacterium tuberculosis and human macrophages. Indian J Exp Biol 2012; 50:542-50.
20. Clemenceau B, Vivien R, BerthomeM, et al. Effector memory alphabeta T lymphocytes can express FcgammaRIIIa and mediate antibodydependent cellular cytotoxicity. J Immunol 2008; 180:5327-34.
21. Alvarez N, Infante JF, Borrero R, et al. Histopathological study of the lungs of mice receiving human secretory IgA and challenged with Mycobacterium tuberculosis. Malays J Med Sci 2014; 21:31-7.
22. Legesse M, Ameni G, Medhin G, et al. IgA response to ESAT-6/CFP-10 and Rv2031 antigens varies in patients with culture-confirmed pulmonary tuberculosis, healthy Mycobacterium tuberculosis-infected and non-infected individuals in a tuberculosis endemic setting, Ethiopia. Scand J Immunol 2013; 78:266-74.
23. McEwan WA, Tam JC, Watkinson RE, Bidgood SR, Mallery DL, James LC. Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21. Nat Immunol 2013; 14:327-36.
24. Sabbatini P, Tsuji T, Ferran L, et al. Phase I trial of overlapping long peptides from a tumor self-antigen and poly-ICLC shows rapid induction of integrated immune response in ovarian cancer patients. Clin Cancer Res 2012; 18:6497-508.
25. Morris D, Nguyen T, Kim J, et al. An elucidation of neutrophil functions against Mycobacterium tuberculosis infection. Clin Dev Immunol 2013; 2013:959650.
26. Ashenafi S, Aderaye G, Zewdie M, et al. BCG-specific IgG-secreting peripheral plasmablasts as a potential biomarker of active tuberculosis in HIV negative and HIV positive patients. Thorax 2013; 68:269-76.
27. Welch RJ, Lawless KM, Litwin CM. Antituberculosis IgG antibodies as a marker of active Mycobacterium tuberculosis disease. Clin Vaccine Immunol 2012; 19:522-6.
28. Demkow U, Filewska M, Michalowska-Mitczuk D, et al. Heterogeneity of antibody response to mycobacterial antigens in different clinical manifestations of pulmonary tuberculosis. J Physiol Pharmacol 2007; 58(suppl 5 pt 1):117-27.
29. Rahman S, Rehn A, Rahman J, Andersson J, Svensson M, Brighenti S. Pulmonary tuberculosis patients with a vitamin D deficiency demonstrate low local expression of the antimicrobial peptide LL-37 but enhanced FoxP3 regulatory T cells and IgG-secreting cells. Clin Immunol 2014; 156:85-97.
30. Subbian S, Tsenova L, Yang G, et al. Chronic pulmonary cavitary tuberculosis in rabbits: a failed host immune response. Open Biol 2011; 1:110016.
31. Hussain R, Dockrell HM, Chiang TJ. Dominant recognition of a cross-reactive B-cell epitope in Mycobacterium leprae 10 K antigen by immunoglobulin G1 antibodies across the disease spectrum in leprosy. Immunology 1999; 96:620-7.
32. Li Y, Zeng Q, Ellis MK, Xiong T, Balen J, McManus DP. CD4+ T-cell counts, CD4+/CD8+ T-cell count ratios, and antibody levels in migrant fishermen infected with Schistosoma japonicum in the Dongting Lake, China. Am J Trop Med Hyg 2006; 75:910-3.
33. Torrado E, Fountain JJ, Robinson RT, et al. Differential and site specific impact of B cells in the protective immune response to Mycobacterium tuberculosis in the mouse. PLoS One 2013; 8:e61681.
34. Farhat M, Greenaway C, Pai M, Menzies D. False-positive tuberculin skin tests: what is the absolute effect of BCG and non-tuberculous mycobacteria Int J Tuberc Lung Dis 2006; 10:1192-204.
35. Steingart KR, Henry M, Laal S, et al. Commercial serological antibody detection tests for the diagnosis of pulmonary tuberculosis: a systematic review. PLoS Med 2007; 4:e202.
36. Slifka MK, Antia R, Whitmire JK, Ahmed R. Humoral immunity due to long-lived plasma cells. Immunity 1998; 8:363-72.
37. Verma RK, Jain A. Antibodies to mycobacterial antigens for diagnosis of tuberculosis. FEMS Immunol Med Microbiol 2007; 51:453-61.
38. Bothamley GH. Serological diagnosis of tuberculosis. Eur Respir J Suppl 1995; 20:676s-88.
39. Maekura R, Okuda Y, Nakagawa M, et al. Clinical evaluation of antituberculous glycolipid immunoglobulin G antibody assay for rapid serodiagnosis of pulmonary tuberculosis. J Clin Microbiol 2001; 39:3603-8.
40. Raqib R, Kamal SM, Rahman MJ, et al. Use of antibodies in lymphocyte secretions for detection of subclinical tuberculosis infection in asymptomatic contacts. Clin Diagn Lab Immunol 2004; 11:1022-7.
41. Raqib R, Mondal D, Karim MA, et al. Detection of antibodies secreted from circulating Mycobacterium tuberculosis-specific plasma cells in the diagnosis of pediatric tuberculosis. Clin Vaccine Immunol 2009; 16:521-7.
42. Schierloh P, Landoni V, Balboa L, et al. Human pleural B-cells regulate IFN-gamma production by local T-cells and NK cells in a Mycobacterium tuberculosis-induced delayed hypersensitivity reaction. Clin Sci (Lond) 2014; 127:391-403.
43. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008; 28:639-50.
44. Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011; 117:530-41.
45. Blair PA, Norena LY, Flores-Borja F, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010; 32:129-40.
46. Flores-Borja F, Bosma A, Ng D, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med 2013; 5:173ra23.
47. Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, Fallon PG. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 2010; 125:1114-24.e8.
48. Watanabe R, Ishiura N, Nakashima H, et al. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol 2010; 184:4801-9.
49. Zhang M, Zeng G, Yang Q, et al. Anti-tuberculosis treatment enhances the production of IL-22 through reducing the frequencies of regulatory B cell. Tuberculosis 2014; 94:238-44.
50. Pagan AJ, Ramakrishnan L. Immunity and immunopathology in the tuberculous granuloma. Cold Spring Harb Perspect Med 2014; doi:10.1101/cshperspect.a018499.
51. Tully G, Kortsik C, Hohn H, et al. Highly focused T cell responses in latent human pulmonary Mycobacterium tuberculosis infection. J Immunol 2005; 174:2174-84.
52. Lee SH, Min JW, Lee CH, et al. Impact of parenchymal tuberculosis sequelae on mediastinal lymph node staging in patients with lung cancer. J Korean Med Sci 2011; 26:67-70.
53. Ochsenbein AF, Pinschewer DD, Sierro S, Horvath E, Hengartner H, Zinkernagel RM. Protective long-term antibody memory by antigendriven and T help-dependent differentiation of long-lived memory B cells to short-lived plasma cells independent of secondary lymphoid organs. Proc Natl Acad Sci USA 2000; 97:13263-8.
54. Paramithiotis E, Cooper MD. Memory B lymphocytes migrate to bone marrow in humans. Proc Natl Acad Sci USA 1997; 94:208-12.
55. Lausen BF, Hougs L, Schejbel L, Heilmann C, Barington T. Human memory B cells transferred by allogenic bone marrow transplantation contribute significantly to the antibody repertoire of the recipient. J Immunol 2004; 172:3305-18.
56. Scheid JF, Mouquet H, Kofer J, Yurasov S, Nussenzweig MC, Wardemann H. Differential regulation of self-reactivity discriminates between IgG+ human circulating memory B cells and bone marrow plasma cells. Proc Natl Acad Sci USA 2011; 108:18044-8.
57. Lay JC, Peden DB, Alexis NE. Flow cytometry of sputum: assessing inflammation and immune response elements in the bronchial airways. Inhal Toxicol 2011; 23:392-406.
58. Willis VC, Demoruelle MK, Derber LA, et al. Sputum autoantibodies in patients with established rheumatoid arthritis and subjects at risk of future clinically apparent disease. Arthritis Rheum 2013; 65:2545-54.
59. Aanaes K, Johansen HK, Poulsen SS, Pressler T, Buchwald C, Hoiby N. Secretory IgA as a diagnostic tool for Pseudomonas aeruginosa respiratory colonization. J Cyst Fibros 2013; 12:81-7.
60. Valentini D, Gaseitsiwe S, Maeurer M. Humoral 'reactome' profiles using peptide microarray chips. Trends Immunol 2010; 31:399-400.
61. Ambati A, Poiret T, Svahn BM, et al. Increased beta-haemolytic group A streptococcal M6 serotype and streptodornase B-specific cellular immune responses in Swedish narcolepsy cases. J Intern Med 2015; doi:10.1111/joim.12355.
62. Aditya A, Valentini D, Montomoli E, et al. H1N1 viral proteome peptide microarray predicts individuals at risk for H1N1 infection and segregates infection versus pandemrix-vaccination. Immunology 2015; 143:357-66.
63. Gaseitsiwe S, Valentini D, Mahdavifar S, et al. Pattern recognition in pulmonary tuberculosis defined by high content peptide microarray chip analysis representing 61 proteins from M. tuberculosis. PLoS One 2008; 3:e3840.
64. Britschgi M, Olin CE, Johns HT, et al. Neuroprotective natural antibodies to assemblies of amyloidogenic peptides decrease with normal aging and advancing Alzheimer's disease. Proc Natl Acad Sci USA 2009; 106:12145-50.
65. Nimmerjahn F, Ravetch JV. The antiinflammatory activity of IgG: the intravenous IgG paradox. J Exp Med 2007; 204:11-5.
66. Aktas O, Waiczies S, Grieger U, Wendling U, Zschenderlein R, Zipp F. Polyspecific immunoglobulins (IVIg) suppress proliferation of human (auto)antigen-specific T cells without inducing apoptosis. J Neuroimmunol 2001; 114:160-7.
67. Orange JS, Hossny EM, Weiler CR, et al. Use of intravenous immunoglobulin in human disease: a review of evidence by members of the Primary Immunodeficiency Committee of the American Academy of Allergy, Asthma and Immunology. J Allergy Clin Immunol 2006; 117(4 suppl):S525-53.
68. Latov N, Chaudhry V, Koski CL, et al. Use of intravenous gamma globulins in neuroimmunologic diseases. J Allergy Clin Immunol 2001; 108 (4 suppl):S126-32.
69. Barry W, Hudgins L, Donta ST, Pesanti EL. Intravenous immunoglobulin therapy for toxic shock syndrome. JAMA 1992; 267:3315-6.
70. Intravenous immune globulin for the prevention of bacterial infections in children with symptomatic human immunodeficiency virus infection. The National Institute of Child Health and Human Development Intravenous Immunoglobulin Study Group. N Engl J Med 1991; 325:73-80.
71. Winston DJ, Ho WG, Rasmussen LE, et al. Use of intravenous immune globulin in patients receiving bone marrow transplants. J Clin Immunol 1982; 2(2 suppl):42S-7.