Human isotype-dependent inhibitory antibody responses against Mycobacterium tuberculosis

EMBO Molecular Medicine

Volumn 8, Issue 11, 2016, Pages 1325-1339

  Zimmermann, Natalie ^a,b   Thormann, Verena ^a   Hu, Bo ^a   Köhler, Anne Britta ^a   Imai Matsushima, Aki ^a   Locht, Camille ^c,d,e,f,g   Arnett, Eusondia ^h   Schlesinger, Larry S ^h   Zoller, Thomas ⁱ   Schürmann, Mariana ⁱ   Kaufmann, Stefan H E ^a   Wardemann, Hedda ^a,b  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIV LILLE   (France)

^d CNRS   (France)

^e INSERM U1019   (France)

^f LILLE UNIVERSITY HOSPITAL   (France)

^g INSTITUT PASTEUR DE LILLE   (France)

^h OHIO STATE UNIVERSITY   (United States)

ⁱ CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

antibodies; B cells; infection; isotype; Mycobacterium tuberculosis

Indexed keywords

BACTERIAL ANTIGEN; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; BACTERIUM ANTIBODY; IMMUNOGLOBULIN CLASS; MONOCLONAL ANTIBODY;

ADULT; ANTIBODY RESPONSE; ARTICLE; BACTERIAL VIRULENCE; CELL ISOLATION; CONTROLLED STUDY; HEALTH CARE PERSONNEL; HOST CELL; HUMAN; HUMAN CELL; INFECTION PREVENTION; LUNG TUBERCULOSIS; MAJOR CLINICAL STUDY; MEMORY CELL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OCCUPATIONAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANTIBODY PRODUCTION; B LYMPHOCYTE; IMMUNOLOGY; ISOLATION AND PURIFICATION;

ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; ANTIBODY FORMATION; B-LYMPHOCYTES; HUMANS; IMMUNOGLOBULIN ISOTYPES; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS, PULMONARY;

EID: 84991034085     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201606330     Document Type: Article

References (54)

1. Abreu MT, Carvalheiro H, Rodrigues-Sousa T, Domingos A, Segorbe-Luis A, Rodrigues-Santos P, Souto-Carneiro MM (2014) Alterations in the peripheral blood B cell subpopulations of multidrug-resistant tuberculosis patients. Clin Exp Med 14: 423–429
2. Achkar JM, Chan J, Casadevall A (2015) B cells and antibodies in the defense against Mycobacterium tuberculosis infection. Immunol Rev 264: 167–181
3. Andersen P, Kaufmann SH (2014) Novel vaccination strategies against tuberculosis. Cold Spring Harbor Perspect Med 4: a018523
4. Bakema JE, van Egmond M (2011) The human immunoglobulin A Fc receptor FcalphaRI: a multifaceted regulator of mucosal immunity. Mucosal Immunol 4: 612–624
5. Balu S, Reljic R, Lewis MJ, Pleass RJ, McIntosh R, van Kooten C, van Egmond M, Challacombe S, Woof JM, Ivanyi J (2011) A novel human IgA monoclonal antibody protects against tuberculosis. J Immunol 186: 3113–3119
6. Berkowska MA, Schickel JN, Grosserichter-Wagener C, de Ridder D, Ng YS, van Dongen JJ, Meffre E, van Zelm MC (2015) Circulating human CD27-IgA+ memory B cells recognize bacteria with polyreactive Igs. J Immunol 195: 1417–1426
7. Bermudez LE, Goodman J (1996) Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect Immun 64: 1400–1406
8. Bosio CM, Gardner D, Elkins KL (2000) Infection of B cell-deficient mice with CDC 1551, a clinical isolate of Mycobacterium tuberculosis: delay in dissemination and development of lung pathology. J Immunol 164: 6417–6425
9. Bournazos S, DiLillo DJ, Ravetch JV (2015) The role of Fc-FcgammaR interactions in IgG-mediated microbial neutralization. J Exp Med 212: 1361–1369
10. Brandtzaeg P, Jahnsen FL, Farstad IN, Haraldsen G (1997) Mucosal immunology of the upper airways: an overview. Ann N Y Acad Sci 830: 1–18
11. Brown RM, Cruz O, Brennan M, Gennaro ML, Schlesinger L, Skeiky YA, Hoft DF (2003) Lipoarabinomannan-reactive human secretory immunoglobulin A responses induced by mucosal bacille Calmette-Guerin vaccination. J Infect Dis 187: 513–517
12. Buccheri S, Reljic R, Caccamo N, Ivanyi J, Singh M, Salerno A, Dieli F (2007) IL-4 depletion enhances host resistance and passive IgA protection against tuberculosis infection in BALB/c mice. Eur J Immunol 37: 729–737
13. Castro-Garza J, King CH, Swords WE, Quinn FD (2002) Demonstration of spread by Mycobacterium tuberculosis bacilli in A549 epithelial cell monolayers. FEMS Microbiol Lett 212: 145–149
14. Chambers MA, Gavier-Widen D, Hewinson RG (2004) Antibody bound to the surface antigen MPB83 of Mycobacterium bovis enhances survival against high dose and low dose challenge. FEMS Immunol Med Microbiol 41: 93–100
15. Cooper AM (2009) Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 27: 393–422
16. Demkow U, Filewska M, Michalowska-Mitczuk D, Kus J, Jagodzinski J, Zielonka T, Zwolska Z, Wasik M, Rowinska-Zakrzewska E (2007) Heterogeneity of antibody response to mycobacterial antigens in different clinical manifestations of pulmonary tuberculosis. J Physiol Pharmacol 58(Suppl 5): 117–127
17. van Egmond M, van Vuuren AJ, Morton HC, van Spriel AB, Shen L, Hofhuis FM, Saito T, Mayadas TN, Verbeek JS, van de Winkel JG (1999) Human immunoglobulin A receptor (FcalphaRI, CD89) function in transgenic mice requires both FcR gamma chain and CR3 (CD11b/CD18). Blood 93: 4387–4394
18. Falero-Diaz G, Challacombe S, Rahman D, Mistry M, Douce G, Dougan G, Acosta A, Ivanyi J (2000) Transmission of IgA and IgG monoclonal antibodies to mucosal fluids following intranasal or parenteral delivery. Int Arch Allergy Immunol 122: 143–150
19. Glatman-Freedman A, Casadevall A (1998) Serum therapy for tuberculosis revisited: reappraisal of the role of antibody-mediated immunity against Mycobacterium tuberculosis. Clin Microbiol Rev 11: 514–532
20. Guirado E, Schlesinger LS, Kaplan G (2013) Macrophages in tuberculosis: friend or foe. Semin Immunopathol 35: 563–583
21. Hamasur B, Haile M, Pawlowski A, Schroder U, Kallenius G, Svenson SB (2004) A mycobacterial lipoarabinomannan specific monoclonal antibody and its F(ab') fragment prolong survival of mice infected with Mycobacterium tuberculosis. Clin Exp Immunol 138: 30–38
22. Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, DesJardin LE, Schlesinger LS (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202: 987–999
23. Kohama H, Umemura M, Okamoto Y, Yahagi A, Goga H, Harakuni T, Matsuzaki G, Arakawa T (2008) Mucosal immunization with recombinant heparin-binding haemagglutinin adhesin suppresses extrapulmonary dissemination of Mycobacterium bovis bacillus Calmette-Guerin (BCG) in infected mice. Vaccine 26: 924–932
24. Li GM, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng NY, Lee JH, Huang M, Qu X, Edupuganti S et al (2012) Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci USA 109: 9047–9052
25. Locht C, Hougardy JM, Rouanet C, Place S, Mascart F (2006) Heparin-binding hemagglutinin, from an extrapulmonary dissemination factor to a powerful diagnostic and protective antigen against tuberculosis. Tuberculosis 86: 303–309
26. Lopez Y, Yero D, Falero-Diaz G, Olivares N, Sarmiento ME, Sifontes S, Solis RL, Barrios JA, Aguilar D, Hernandez-Pando R et al (2009) Induction of a protective response with an IgA monoclonal antibody against Mycobacterium tuberculosis 16 kDa protein in a model of progressive pulmonary infection. Int J Med Microbiol 299: 447–452
27. Lorin V, Mouquet H (2015) Efficient generation of human IgA monoclonal antibodies. J Immunol Methods 422: 102–110
28. Maglione PJ, Xu J, Chan J (2007) B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis. J Immunol 178: 7222–7234
29. Maglione PJ, Xu J, Casadevall A, Chan J (2008) Fc gamma receptors regulate immune activation and susceptibility during Mycobacterium tuberculosis infection. J Immunol 180: 3329–3338
30. Masungi C, Temmerman S, Van Vooren JP, Drowart A, Pethe K, Menozzi FD, Locht C, Mascart F (2002) Differential T and B cell responses against Mycobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J Infect Dis 185: 513–520
31. Menozzi FD, Rouse JH, Alavi M, Laude-Sharp M, Muller J, Bischoff R, Brennan MJ, Locht C (1996) Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 184: 993–1001
32. Menozzi FD, Reddy VM, Cayet D, Raze D, Debrie AS, Dehouck MP, Cecchelli R, Locht C (2006) Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions. Microbes Infect 8: 1–9
33. Pethe K, Alonso S, Biet F, Delogu G, Brennan MJ, Locht C, Menozzi FD (2001) The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412: 190–194
34. Pukazhvanthen P, Anbarasu D, Basirudeen SA, Raja A, Singh M (2014) Assessing humoral immune response of 4 recombinant antigens for serodiagnosis of tuberculosis. Tuberculosis 94: 622–633
35. Ravetch JV, Clynes RA (1998) Divergent roles for Fc receptors and complement in vivo. Ann Rev Immunol 16: 421–432
36. Rojas R, Apodaca G (2002) Immunoglobulin transport across polarized epithelial cells. Nature Rev Mol Cell Biol 3: 944–955
37. Roy E, Stavropoulos E, Brennan J, Coade S, Grigorieva E, Walker B, Dagg B, Tascon RE, Lowrie DB, Colston MJ et al (2005) Therapeutic efficacy of high-dose intravenous immunoglobulin in Mycobacterium tuberculosis infection in mice. Infect Immun 73: 6101–6109
38. Ryndak MB, Singh KK, Peng Z, Laal S (2015) Transcriptional profile of Mycobacterium tuberculosis replicating in type II alveolar epithelial cells. PLoS ONE 10: e0123745
39. Sato K, Tomioka H, Shimizu T, Gonda T, Ota F, Sano C (2002) Type II alveolar cells play roles in macrophage-mediated host innate resistance to pulmonary mycobacterial infections by producing proinflammatory cytokines. J Infect Dis 185: 1139–1147
40. Schlesinger LS, Hull SR, Kaufman TM (1994) Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J Immunol 152: 4070–4079
41. Small PM, Hopewell PC, Singh SP, Paz A, Parsonnet J, Ruston DC, Schecter GF, Daley CL, Schoolnik GK (1994) The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med 330: 1703–1709
42. Smith P, DiLillo DJ, Bournazos S, Li F, Ravetch JV (2012) Mouse model recapitulating human Fcgamma receptor structural and functional diversity. Proc Natl Acad Sci USA 109: 6181–6186
43. Spiekermann GM, Finn PW, Ward ES, Dumont J, Dickinson BL, Blumberg RS, Lencer WI (2002) Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J Exp Med 196: 303–310
44. Suprynowicz FA, Upadhyay G, Krawczyk E, Kramer SC, Hebert JD, Liu X, Yuan H, Cheluvaraju C, Clapp PW, Boucher RC Jr et al (2012) Conditionally reprogrammed cells represent a stem-like state of adult epithelial cells. Proc Natl Acad Sci USA 109: 20035–20040
45. Teitelbaum R, Glatman-Freedman A, Chen B, Robbins JB, Unanue E, Casadevall A, Bloom BR (1998) A mAb recognizing a surface antigen of Mycobacterium tuberculosis enhances host survival. Proc Natl Acad Sci USA 95: 15688–15693
46. Tiller T, Tsuiji M, Yurasov S, Velinzon K, Nussenzweig MC, Wardemann H (2007) Autoreactivity in human IgG+ memory B cells. Immunity 26: 205–213
47. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, Wardemann H (2008) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329: 112–124
48. Torrelles JB, Knaup R, Kolareth A, Slepushkina T, Kaufman TM, Kang P, Hill PJ, Brennan PJ, Chatterjee D, Belisle JT et al (2008) Identification of Mycobacterium tuberculosis clinical isolates with altered phagocytosis by human macrophages due to a truncated lipoarabinomannan. J Biol Chem 283: 31417–31428
49. Tsuiji M, Yurasov S, Velinzon K, Thomas S, Nussenzweig MC, Wardemann H (2006) A checkpoint for autoreactivity in human IgM+ memory B cell development. J Exp Med 203: 393–400
50. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC (2003) Predominant autoantibody production by early human B cell precursors. Science 301: 1374–1377
51. Williams A, Reljic R, Naylor I, Clark SO, Falero-Diaz G, Singh M, Challacombe S, Marsh PD, Ivanyi J (2004) Passive protection with immunoglobulin A antibodies against tuberculous early infection of the lungs. Immunology 111: 328–333
52. Wrammert J, Smith K, Miller J, Langley WA, Kokko K, Larsen C, Zheng NY, Mays I, Garman L, Helms C et al (2008) Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453: 667–671
53. Zimmermann N, Saiga H, Houthuys E, Moura-Alves P, Koehler A, Bandermann S, Dorhoi A, Kaufmann SH (2016) Syndecans promote mycobacterial internalization by lung epithelial cells. Cell Microbiol. doi: 10.1111/cmi.12627
54. Zumla A, George A, Sharma V, Herbert N, Baroness Masham of I (2013) WHO's 2013 global report on tuberculosis: successes, threats, and opportunities. Lancet 382: 1765–1767