Microbial translocation is a cause of systemic immune activation in chronic HIV infection

Nature Medicine

Volumn 12, Issue 12, 2006, Pages 1365-1371

  Brenchley, Jason M ^a   Price, David A ^a   Schacker, Timothy W ^b   Asher, Tedi E ^a   Silvestri, Guido ^c   Rao, Srinivas ^a   Kazzaz, Zachary ^a   Bornstein, Ethan ^a   Lambotte, Olivier ^d   Altmann, Daniel ^e   Blazar, Bruce R ^f   Rodriguez, Benigno ^g   Teixeira Johnson, Leia ^g   Landay, Alan ^h   Martin, Jeffrey N ⁱ   Hecht, Frederick M ⁱ   Picker, Louis J ^j   Lederman, Michael M ^g   Deeks, Steven G ⁱ   Douek, Daniel C ^a  

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

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d BICÊTRE HOSPITAL   (France)

^e HAMMERSMITH HOSPITAL   (United Kingdom)

^f UNIVERSITY OF MINNESOTA   (United States)

^g UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^h RUSH MEDICAL COLLEGE   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; BACTERIUM LIPOPOLYSACCHARIDE; CEFOTAXIME; METRONIDAZOLE; NEOMYCIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL TRANSLOCATION; CERCOCEBUS; CHRONIC DISEASE; CONTROLLED STUDY; CORRELATION ANALYSIS; FECES MICROFLORA; GASTROINTESTINAL MUCOSA; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPATHOGENESIS; IN VIVO STUDY; INNATE IMMUNITY; MAJOR CLINICAL STUDY; NONHUMAN; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; RETROVIRUS INFECTION; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS LOAD;

ANIMALS; ANTI-HIV AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BACTERIAL TRANSLOCATION; CERCOCEBUS ATYS; CHRONIC DISEASE; ENTEROBACTERIACEAE; FECES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNE SYSTEM; LIPOPOLYSACCHARIDES; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 33845532053     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm1511     Document Type: Article

References (50)

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. Hellerstein, M. et al. Directly measured kinetics of circulating T lymphocytes in normal and HIV-1-infected humans. Nat. Med. 5, 83-89 (1999).
3. Hazenberg, M.D. et al. T-cell division in human immunodeficiency virus (HIV)-1 infection is mainly due to immune activation: a longitudinal analysis in patients before and during highly active antiretroviral therapy (HAART). Blood 95, 249-255 (2000).
4. Valdez, H. & Lederman, M.M. Cytokines and cytokine therapies in HIV infection. AIDS Clin. Rev. 187-228 (1997).
5. Giorgi, J.V. et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179, 859-870 (1999).
6. Brenchley, J.M., Price, D.A. & Douek, D.C. HIV disease: fallout from a mucosal catastrophe? Nat. Immunol. 7, 235-239 (2006).
7. Grossman, Z., Meier-Schellersheim, M., Paul, W.E. & Picker, L.J. Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat. Med. 12, 289-295 (2006).
8. + T cells in multiple tissues during acute SIV infection. Nature 434, 1093-1097 (2005).
9. + T cell depletion and viral replication in SIV infection. Science 280, 427-431 (1998).
10. + 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. 77, 11708-11717 (2003).
11. + T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200, 749-759 (2004).
12. + T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200, 761-770 (2004).
13. + memory T cells in rapidly progressive simian immunodeficiency virus infection. J. Exp. Med. 200, 1299-1314 (2004).
14. + T-cell restoration and enhanced gene expression regulating mucosal repair and regeneration. J. Virol. 79, 2709-2719 (2005).
15. Kotler, D.P. HIV infection and the gastrointestinal tract. AIDS 19, 107-117 (2005).
16. Sharpstone, D. et al. Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut 45, 70-76 (1999).
17. Macpherson, A.J. & Harris, N.L. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4, 478-485 (2004).
18. Cooke, K.R., Olkiewicz, K., Erickson, N. & Ferrara, J.L. The role of endotoxin and the innate immune response in the pathophysiology of acute graft versus host disease. J. Endotoxin Res. 8, 441-448 (2002).
19. Caradonna, L. et al. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J. Endotoxin Res. 6, 205-214 (2000).
20. Takeda, K., Kaisho, T. & Akira, S. Toll-like receptors. Annu. Rev. Immunol. 21, 335-376 (2003).
21. Hill, G.R. et al. Differential roles of IL-1 and TNF-α on graft-versus-host disease and graft versus leukemia. J. Clin. Invest. 104, 459-467 (1999).
22. Schietroma, M. et al. Intestinal and systemic endotoxaemia after laparotomic or laparoscopic cholecystectomy. Chir. Ital. 58, 171-177 (2006).
23. Wellmann, W., Fink, P.C., Benner, F. & Schmidt, F.W. Endotoxaemia in active Crohn's disease. Treatment with whole gut irrigation and 5-aminosalicylic acid. Gut 27, 814-820 (1986).
24. Wyatt, J., Vogelsang, H., Hubl, W., Waldhoer, T. & Lochs, H. Intestinal permeability and the prediction of relapse in Crohn's disease. Lancet 341, 1437-1439 (1993).
25. Schietroma, M., Carlei, F., Cappelli, S. & Amicucci, G. Intestinal permeability and systemic endotoxemia after laparotomic or laparoscopic cholecystectomy. Ann. Surg. 243, 359-363 (2006).
26. Kitchens, R.L. & Thompson, P.A. Modulatory effects of sCD14 and LBP on LPS-host cell interactions. J. Endotoxin Res. 11, 225-229 (2005).
27. Lien, E. 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 92, 2084-2092 (1998).
28. Nomura, F. et al. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J. Immunol. 164, 3476-3479 (2000).
29. Strutz, F., Heller, G., Krasemann, K., Krone, B. & Muller, G.A. Relationship of antibodies to endotoxin core to mortality in medical patients with sepsis syndrome. Intensive Care Med. 25, 435-444 (1999).
30. Cohen, I.R. & Norins, L.C. Natural human antibodies to gram-negative bacteria: immunoglobulins G, A, and M. Science 152, 1257-1259 (1966).
31. Barclay, G.R. Endogenous endotoxin-core antibody (EndoCAb) as a marker of endotoxin exposure and a prognostic indicator: a review. Prog. Clin. Biol. Res. 392, 263-272 (1995).
32. Titanji, K. et al. Loss of memory B cells impairs maintenance of long-term serological memory during HIV-1 infection. Blood 108, 1580-1587 (2006).
33. Ito, T., Kanzler, H., Duramad, O., Cao, W. & Liu, Y.J. Specialization, kinetics, and repertoire of type 1 interferon responses by human plasmacytoid predendritic cells. Blood 107, 2423-2431 (2006).
34. Aziz, N. et al. Stability of plasma levels of cytokines and soluble activation markers in patients with human immunodeficiency virus infection. J. Infect. Dis. 179, 843-848 (1999).
35. Haas, D.W. et al. Proinflammatory cytokine and human immunodeficiency virus RNA levels during early Mycobacterium avium complex bacteremia in advanced AIDS. J. Infect. Dis. 177, 1746-1749 (1998).
36. MacArthur, R.D. et al. Effects of mycobacterium avium complex-infection treatment on cytokine expression in human immunodeficiency virus-infected persons: results of AIDS clinical trials group protocol 853. J. Infect. Dis. 181, 1486-1490 (2000).
37. Beignon, A.S. et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J. Clin. Invest. 115, 3265-3275 (2005).
38. + T cells. J. Immunol. 175, 1551-1557 (2005).
39. Kovacs, J.A. et al. Identification of dynamically distinct subpopulations of T lymphocytes that are differentially affected by HIV. J. Exp. Med. 194, 1731-1741 (2001).
40. Lederman, M.M. et al. Immunologic responses associated with 12 weeks of combination antiretroviral therapy consisting of zidovudine, lamivudine, and ritonavir: results of AIDS clinical trials group protocol 315. J. Infect. Dis. 178, 70-79 (1998).
41. Bafica, A., Scanga, C.A., Schito, M., Chaussabel, D. & Sher, A. Influence of coinfecting pathogens on HIV expression: evidence for a role of Toll-like receptors. J. Immunol. 172, 7229-7234 (2004).
42. Morris, L. et al. HIV-1 antigen-specific and -nonspecific B cell responses are sensitive to combination antiretroviral therapy. J. Exp. Med. 188, 233-245 (1998).
43. Emu, B. et al. Phenotypic, functional, and kinetic parameters associated with apparent T-cell control of human immunodeficiency virus replication in individuals with and without antiretroviral treatment. J. Virol. 79, 14169-14178 (2005).
44. Holmes, C.L., Russell, J.A. & Walley, K.R. Genetic polymorphisms in sepsis and septic shock: role in prognosis and potential for therapy. Chest 124, 1103-1115 (2003).
45. Sankaran, S. et al. Gut mucosal T cell responses and gene expression correlate with protection against disease in long-term HIV-1-infected nonprogressors. Proc. Natl. Acad. Sci. USA 102, 9860-9865 (2005).
46. Silvestri, G. et al. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18, 441-452 (2003).
47. Zaunders, J.J. et al. Increased turnover of CCR5+ and redistribution of CCR5- CD4 T lymphocytes during primary human immunodeficiency virus type 1 infection. J. Infect. Dis. 183, 736-743 (2001).
48. Skoner, D.P., Gentile, D.A., Patel, A. & Doyle, W.J. Evidence for cytokine mediation of disease expression in adults experimentally infected with influenza A virus. J. Infect. Dis. 180, 10-14 (1999).
49. Veazey, R.S. et al. Protection of macaques from vaginal SHIV challenge by vaginally delivered inhibitors of virus-cell fusion. Nature 438, 99-102 (2005).
50. Fort, M.M. et al. A synthetic TLR4 antagonist has anti-inflammatory effects in two murine models of inflammatory bowel disease. J. Immunol. 174, 6416-6423 (2005).