Systemic antibody responses to gut commensal bacteria during chronic HIV-1 infection

Gut

Volumn 60, Issue 11, 2011, Pages 1506-1519

  Haas, Anna ^a   Zimmermann, Kathrin ^a   Graw, Frederik ^a   Slack, Emma ^b   Rusert, Peter ^c   Ledergerber, Bruno ^d   Bossart, Walter ^c   Weber, Rainer ^d   Thurnheer, Maria C ^b   Battegay, Manuel ^e   Hirschel, Bernard ^f   Vernazza, Pietro ^g   Patuto, Nicola ^b   Macpherson, Andrew J ^b   Günthard, Huldrych F ^d   Oxenius, Annette ^a   Barth, J ^h   Bernasconi, E ^h   Boni J ^h   Brazzola, P ^h   Bucher, H C ^h   Burgisser P ^h   Burton Jeangros, C ^h   Calmy, A ^h   Cavassini, M ^h   Cheseaux, J J ^h   Drack, G ^h   Dubs, R ^h   Duppenthaler, A ^h   Egger, M ^h   Elzi, L ^h   Fehr, J ^h   Fischer, M ^h   Flepp, M ^h   Francioli, P ^h   Furrer, H ^h   Fux, C A ^h   Gorgievski, M ^h   Grawe, C ^h   Gunthard H ^h   Gyr, T ^h   Hasse, B ^h   Hirsch, H H ^h   Hosli I ^h   Kahlert, C ^h   Kaiser, L ^h   Keiser, O ^h   Kind, C ^h   Klimkait, T ^h   Kovari, H ^h   Martinetti, G ^h   Martinez De Tejada, B ^h   Muller N ^h   Nadal, D ^h   Pantaleo, G ^h   Posfay Barbe, K ^h   Raio, L ^h   Rauch, A ^h   Regenass, S ^h   Rickenbach, M ^h   Rudin, C ^h   Schmid, P ^h   Schultze, D ^h   Schoni Affolter F ^h   Schupbach J ^h   Speck, R ^h   Taffe P ^h   Telenti, A ^h   Trkola, A ^h   Vernazza, P ^h   Von Wyl, V ^h   Wyler, C A ^h   Yerly, S ^h   more..

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e UNIVERSITY OF BASEL   (Switzerland)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^g CANTONAL HOSPITAL ST GALLEN   (Switzerland)

^h NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; ENDOTOXIN ANTIBODY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; LIPOPOLYSACCHARIDE; POLIOMYELITIS VACCINE; TETANUS TOXOID; VIRUS ANTIBODY;

ADULT; AGED; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL TRANSLOCATION; BACTEROIDES FRAGILIS; BLOOD SAMPLING; BRADYRHIZOBIUM JAPONICUM; CANDIDA ALBICANS; COMMENSAL; CONTROLLED STUDY; CROHN DISEASE; DIARRHEA; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HYPERGAMMAGLOBULINEMIA; IMMUNOGLOBULIN BLOOD LEVEL; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LEGIONELLA PNEUMOPHILA; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES; STAPHYLOCOCCUS EPIDERMIDIS; ULCERATIVE COLITIS;

ADULT; AGED; ANTI-RETROVIRAL AGENTS; ANTIBODIES, BACTERIAL; ANTIBODY SPECIFICITY; B-LYMPHOCYTES; CHRONIC DISEASE; COINFECTION; FEMALE; FLOW CYTOMETRY; HIV ENTEROPATHY; HIV-1; HUMANS; HYPERGAMMAGLOBULINEMIA; IMMUNITY, MUCOSAL; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MALE; MIDDLE AGED;

EID: 80053563346     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gut.2010.224774     Document Type: Article

References (81)

1. Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science 2005;308:1635-8. (Pubitemid 40807514)
2. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65.
3. Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 2010;10:159-69.
4. Nazli A, Chan O, Dobson-Belaire WN, et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 2010;6:-1000852.
5. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008;1:23-30.
6. Mehandru S, Dandekar S. Role of the gastrointestinal tract in establishing infection in primates and humans. Curr Opin HIV AIDS 2008;3:22-7. (Pubitemid 351339925)
7. Mehandru S, Poles MA, Tenner-Racz K, et al. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004;200:761-70. (Pubitemid 39299462)
8. Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004;200:749-59. (Pubitemid 39299461)
9. Guadalupe M, Reay E, Sankaran S, et al. Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 2003;77:11708-17. (Pubitemid 37271669)
10. Kotler DP, Gaetz HP, Lange M, et al. Enteropathy associated with the acquired immunodeficiency syndrome. Ann Inter Med 1984;101:421-8. (Pubitemid 14018034)
11. McGowan I, Elliott J, Fuerst M, et al. Increased HIV-1 mucosal replication is associated with generalized mucosal cytokine activation. J Acquir Immune Defic Syndr 2004;37:1228-36. (Pubitemid 39281503)
12. Weber R, Ledergerber B, Zbinden R, et al. Enteric infections and diarrhea in human immunodeficiency virus-infected persons: prospective community-based cohort study. Swiss HIV Cohort Study. Arch Intern Med 1999;159:1473-80. (Pubitemid 29302888)
13. Keating J, Bjarnason I, Somasundaram S, et al. Intestinal absorptive capacity, intestinal permeability and jejunal histology in HIV and their relation to diarrhoea. Gut 1995;37:623-9.
14. Sharpstone D, Neild P, Crane R, et al. Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut 1999;45:70-6. (Pubitemid 29301848)
15. Stein TP, Koerner B, Schluter MD, et al. Weight loss, the gut and the inflammatory response in AIDS patients. Cytokine 1997;9:143-7. (Pubitemid 27116890)
16. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006;12:1365-71. (Pubitemid 44924494)
17. Clark EC, Patel SD, Chadwick PR, et al. Glutamine deprivation facilitates tumour necrosis factor induced bacterial translocation in Caco-2 cells by depletion of enterocyte fuel substrate. Gut 2003;52:224-30. (Pubitemid 36115063)
18. Clark E, Hoare C, Tanianis-Hughes J, et al. Interferon gamma induces translocation of commensal Escherichia coli across gut epithelial cells via a lipid raft-mediated process. Gastroenterology 2005;128:1258-67. (Pubitemid 40712177)
19. Macpherson AJ, Slack E. The functional interactions of commensal bacteria with intestinal secretory IgA. Curr Opin Gastroenterol 2007;23:673-8. (Pubitemid 47508799)
20. Lane HC, Masur H, Edgar LC, et al. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 1983;309:453-8. (Pubitemid 13041485)
21. Cagigi A, Nilsson A, De Milito A, et al. B cell immunopathology during HIV-1 infection: lessons to learn for HIV-1 vaccine design. Vaccine 2008;26:3016-25.
22. Moir S, Fauci AS. B cells in HIV infection and disease. Nat Rev Immunol 2009;9:235-45.
23. De Milito A, Nilsson A, Titanji K, et al. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood 2004;103:2180-6. (Pubitemid 38326236)
24. Malaspina A, Moir S, Orsega Susan M, et al. Compromised B cell responses to influenza vaccination in HIV-infected individuals. Journal of Infectious Diseases 2005;191:1442-50. (Pubitemid 40563355)
25. Nilssen DE, Oktedalen O, Brandtzaeg P. Intestinal B cell hyperactivity in AIDS is controlled by highly active antiretroviral therapy. Gut 2004;53:487-93. (Pubitemid 38372971)
26. Levesque MC, Moody MA, Hwang K-K, et al. Polyclonal B cell differentiation and loss of gastrointestinal tract germinal centers in the earliest stages of HIV-1 infection. PLoS Med 2009;6:-1000107.
27. Xu W, Santini PA, Sullivan JS, et al. HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Immunol 2009;10:1008-17.
28. Slack E, Hapfelmeier S, Stecher B, et al. Innate and adaptive immunity cooperate flexibly to maintain hostemicrobiota mutualism. Science 2009;325:617-20.
29. Schoeni-Affolter F, Ledergerber B, Rickenbach M, et al. Cohort profile: the Swiss HIV Cohort study. Int J Epidemiol 2010;39:1179-89.
30. Scott H, Rognum TO, Midtvedt T, et al. Age-related changes of human serum antibodies to dietary and colonic bacterial antigens measured by an enzyme-linked immunosorbent assay. Acta Pathol Microbiol Immunol Scand C 1985;93:65-70. (Pubitemid 15044139)
31. Fonzi WA, Irwin MY. Isogenic strain construction and gene mapping in Candida albicans. Genetics 1993;134:717-28. (Pubitemid 23193572)
32. Haas A, Rehr M, Graw F, et al. HIV-1 replication activates CD4+ T cells with specificities for persistent herpes viruses. EMBO Mol Med 2010;2:231-44.
33. Rusert P, Kuster H, Joos B, et al. Virus isolates during acute and chronic human immunodeficiency virus type 1 infection show distinct patterns of sensitivity to entry inhibitors. J Virol 2005;79:8454-69. (Pubitemid 40853547)
34. Allan E, Poxton IR, Barclay GR. Anti-bacteroides lipopolysaccharide IgG levels in healthy adults and sepsis patients. FEMS Immunol Med Microbiol 1995;11:5-12.
35. Galili U, Mandrell RE, Hamadeh RM, et al. Interaction between human natural anti-alpha-galactosyl immunoglobulin G and bacteria of the human flora. Infect Immun 1988;56:1730-7.
36. Lee HK, Woo MK, Ju YI, et al. Prevalence of antibodies in response to Legionella species, analysis of a healthy population from Jeollanam-do Province, Korea. J Microbiol 2008;46:160-4. (Pubitemid 351840303)
37. Sanchez JL, Polyak CS, Kolavic SA, et al. Investigation of a cluster of Legionella pneumophila infections among staff at a federal research facility. Mil Med 2001;166:753-8. (Pubitemid 32939152)
38. Zoetendal EG, Akkermans ADL, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 1998;64:3854-9. (Pubitemid 28462983)
39. Springer GF. Blood-group and Forssman antigenic determinants shared between microbes and mammalian cells. Prog Allergy 1971;15:9-77.
40. Castro G, Martinez R. Relationship between serum and saliva antibodies to Candida and isolation of Candida species from the mucosa of HIV-infected individuals. Mycoses 2009;52:246-50.
41. Pomarico L, De Souza IP, Castro GF, et al. Levels of salivary IgA antibodies to Candida spp. in HIV-infected adult patients: a systematic review. J Dent 2010;38:10-15.
42. Gardiner KR, Halliday MI, Barclay GR, et al. Significance of systemic endotoxaemia in inflammatory bowel disease. Gut 1995;36:897-901.
43. Oriishi T, Sata M, Toyonaga A, et al. Evaluation of intestinal permeability in patients with inflammatory bowel disease using lactulose and measuring antibodies to lipid A. Gut 1995;36:891-6.
44. Adams RJ, Heazlewood SP, Gilshenan KS, et al. IgG antibodies against common gut bacteria are more diagnostic for Crohn's disease than IgG against mannan or flagellin. Am J Gastroenterol 2008;103:386-96. (Pubitemid 351248712)
45. Lodes MJ, Cong Y, Elson CO, et al. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 2004;113:1296-306. (Pubitemid 39069929)
46. Furrie E, Macfarlane S, Cummings JH, et al. Systemic antibodies towards mucosal bacteria in ulcerative colitis and Crohn's disease differentially activate the innate immune response. Gut 2004;53:91-8. (Pubitemid 38083016)
47. Pastor Rojo O, Lopez San Roman A, Albeniz Arbizu E, et al. Serum lipopolysaccharide-binding protein in endotoxemic patients with inflammatory bowel disease. Inflamm Bowel Dis 2007;13:269-77.
48. Caradonna L, Amati L, Magrone T, et al. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 2000;6:205-14.
49. Pinching AJ. Antibody responses in HIV infection. Clin Exp Immunol 1991;84:181-4.
50. Hart M, Steel A, Clark SA, et al. Loss of discrete memory B cell subsets is associated with impaired immunization responses in HIV-1 infection and may be a risk factor for invasive pneumococcal disease. J Immunol 2007;178:8212-20. (Pubitemid 46898094)
51. Flo RW, Nilsen A, Voltersvik P, et al. Serum antibodies to viral pathogens and Toxoplasma gondii in HIV-infected individuals. APMIS 1993;101:946-52. (Pubitemid 24063736)
52. Quesnel A, Pozzetto B, Touraine F, et al. Antibodies to Epstein-Barr virus and cytomegalovirus in relation to CD4 cell number in human immunodeficiency virus 1 infection. J Med Virol 1992;36:60-4.
53. Bussmann BM, Reiche S, Bieniek B, et al. Loss of HIV-specific memory B-cells as a potential mechanism for the dysfunction of the humoral immune response against HIV. Virology 2010;397:7-13.
54. Konrad A, Cong Y, Duck W, et al. Tight mucosal compartmentation of the murine immune response to antigens of the enteric microbiota. Gastroenterology 2006;130:2050-9. (Pubitemid 43816958)
55. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004;303:1662-5. (Pubitemid 38338323)
56. Cohen IR, Norins LC. Natural human antibodies to Gram-negative bacteria: immunoglobulins G, A, and M. Science 1966;152:1257-9.
57. Jiang W, Lederman MM, Hunt P, et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis 2009;199:1177-85.
58. Malaspina A, Moir S, DiPoto AC, et al. CpG oligonucleotides enhance proliferative and effector responses of B cells in HIV-infected individuals. J Immunol 2008;181:1199-206.
59. Hunziker L, Recher M, Macpherson AJ, et al. Hypergammaglobulinemia and autoantibody induction mechanisms in viral infections. Nat Immunol 2003;4:343-9. (Pubitemid 36432316)
60. Moir S, Malaspina A, Li Y, et al. B cells of HIV-1-infected patients bind virions through CD21ecomplement interactions and transmit infectious virus to activated T cells. J Exp Med 2000;192:637-46.
61. Rappocciolo G, Piazza P, Fuller CL, et al. DC-SIGN on B lymphocytes is required for transmission of HIV-1 to T lymphocytes. PLoS Pathog 2006;2:-70.
62. Rieckmann P, Poli G, Fox CH, et al. Recombinant gp120 specifically enhances tumor necrosis factor-alpha production and Ig secretion in B lymphocytes from HIV-infected individuals but not from seronegative donors. J Immunol 1991;147:2922-7.
63. He B, Qiao X, Klasse PJ, et al. HIV-1 envelope triggers polyclonal Ig class switch recombination through a CD40-independent mechanism involving BAFF and C-type lectin receptors. J Immunol 2006;176:3931-41. (Pubitemid 44264370)
64. Qiao X, He B, Chiu A, et al. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol 2006;7:302-10.
65. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002;298:2199-202. (Pubitemid 35471246)
66. Bernasconi NL, 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 2003;101:4500-4. (Pubitemid 36857820)
67. Wagner M, Poeck H, Jahrsdoerfer B, et al. IL-12p70-dependent Th1 induction by human B cells requires combined activation with CD40 ligand and CpG DNA. J Immunol 2004;172:954-63. (Pubitemid 38113754)
68. Muller F, Aukrust P, Nordoy I, et al. Possible role of interleukin-10 (IL-10) and CD40 ligand expression in the pathogenesis of hypergammaglobulinemia in human immunodeficiency virus infection: modulation of IL-10 and Ig production after intravenous Ig infusion. Blood 1998;92:3721-9. (Pubitemid 28525199)
69. Fecteau JF, Neron S. CD40 stimulation of human peripheral B lymphocytes: distinct response from naive and memory cells. J Immunol 2003;171:4621-9. (Pubitemid 37310578)
70. Hapfelmeier S, Lawson MA, Slack E, et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010;328:1705-9.
71. Macpherson A, Khoo UY, Forgacs I, et al. Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut 1996;38:365-75. (Pubitemid 26074316)
72. Lee PI, Ciccone EJ, Read SW, et al. Evidence for translocation of microbial products in patients with idiopathic CD4 lymphocytopenia. J Infect Dis 2009;199:1664-70.
73. Nowroozalizadeh S, Mansson F, Da Silva Z, et al. Microbial translocation correlates with the severity of both HIV-1 and HIV-2 infections. J Infect Dis 2010;201:1150-4.
74. Balagopal A, Philp FH, Astemborski J, et al. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology 2008;135:226-33. (Pubitemid 351899010)
75. MacLennan CA, Gilchrist JJ, Gordon MA, et al. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 2010;328:508-12.
76. Redd AD, Dabitao D, Bream JH, et al. Microbial translocation, the innate cytokine response, and HIV-1 disease progression in Africa. Proc Natl Acad Sci USA 2009;106:6718-23.
77. Cassol E, Malfeld S, Mahasha P, et al. Persistent microbial translocation and immune activation in HIV-1-infected South Africans receiving combination antiretroviral therapy. J Infect Dis 2010;202:723-33.
78. Lien E, Aukrust P, Sundan A, et al. Elevated levels of serum-soluble CD14 in human immunodeficiency virus type 1 (HIV-1) infection: correlation to disease progression and clinical events. Blood 1998;92:2084-92. (Pubitemid 28446698)
79. Bazil V, Strominger JL. Shedding as a mechanism of down-modulation of CD14 on stimulated human monocytes. J Immunol 1991;147:1567-74.
80. Brown WR, Kloppel TM. The liver and IgA: immunological, cell biological and clinical implications. Hepatology 1989;9:763-84. (Pubitemid 19123527)
81. van Egmond M, van Garderen E, van Spriel AB, et al. FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat Med 2000;6:680-5.