Microbial translocation, immune activation, and HIV disease

Trends in Microbiology

Volumn 21, Issue 1, 2013, Pages 6-13

  Klatt, Nichole R ^a   Funderburg, Nicholas T ^b   Brenchley, Jason M ^a  

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

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

HIV; Immune activation; Microbial translocation; Mucosal immunity

Indexed keywords

ANTIRETROVIRUS AGENT; CYTOKINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COMORBIDITY; DENDRITIC CELL; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPATHOLOGY; IMMUNOSTIMULATION; INNATE IMMUNITY; LATENT VIRUS INFECTION; MICROBIAL ACTIVITY; MICROBIAL TRANSLOCATION; MORBIDITY; MORTALITY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ANIMALS; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL TRANSLOCATION; GASTROINTESTINAL TRACT; HIV INFECTIONS; HUMANS;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84871703067     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2012.09.001     Document Type: Review

References (105)

1. 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. 1999, 179:859-870.
2. Salazar-Gonzalez J.F., et al. Increased immune activation precedes the inflection point of CD4 T cells and the increased serum virus load in human immunodeficiency virus infection. J. Infect. Dis. 1998, 178:423-430.
3. + T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J. Infect. Dis. 2008, 197:126-133.
4. Kuller L.H., et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med. 2008, 5:e203.
5. Rodger A.J., et al. Activation and coagulation biomarkers are independent predictors of the development of opportunistic disease in patients with HIV infection. J. Infect. Dis. 2009, 200:973-983.
6. Lichtfuss G.F., et al. Biomarkers of immune dysfunction following combination antiretroviral therapy for HIV infection. Biomark. Med. 2011, 5:171-186.
7. Brenchley J.M., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 2006, 12:1365-1371.
8. Ancuta P., et al. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS ONE 2008, 3:e2516.
9. Balagopal A., et al. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology 2008, 135:226-233.
10. + T-cell reconstitution in HIV-infected patients on long-term highly active antiretroviral therapy. AIDS 2008, 22:2035-2038.
11. + subjects with <50 copies/ml HIV-1 RNA. J. Clin. Virol. 2009, 46:367-370.
12. Jiang W., 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, 199:1177-1185.
13. Arias J.F., et al. High systemic levels of interleukin-10, interleukin-22 and C-reactive protein in Indian patients are associated with low in vitro replication of HIV-1 subtype C viruses. Retrovirology 2010, 7:15.
14. Cassol E., et al. Persistent microbial translocation and immune activation in HIV-1-infected South Africans receiving combination antiretroviral therapy. J. Infect. Dis. 2010, 202:723-733.
15. + T cells decreases after prolonged anti-retroviral therapy and is associated with plasma LPS levels. Mucosal Immunol. 2010, 3:172-181.
16. Estes J.D., et al. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 2010, 6:e1001052.
17. Favre D., et al. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci. Transl. Med. 2010, 2:32ra36.
18. Funderburg N.T., et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood 2010, 115:161-167.
19. + T cell activation in HIV-infected individuals. J. Immunol. 2010, 185:5169-5179.
20. Kamat A., et al. Serological markers for inflammatory bowel disease in AIDS patients with evidence of microbial translocation. PLoS ONE 2010, 5:e15533.
21. Klatt N.R., et al. Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation, immune activation, and IL-17 production in the absence of SIV infection. Mucosal Immunol. 2010, 3:387-398.
22. Leinert C., et al. Microbial translocation in simian immunodeficiency virus (SIV)-infected rhesus monkeys (Macaca mulatta). J. Med. Primatol. 2010, 39:243-251.
23. Massanella M., et al. CD4 T-cell hyperactivation and susceptibility to cell death determine poor CD4 T-cell recovery during suppressive HAART. AIDS 2010, 24:959-968.
24. Nazli A., et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog. 2010, 6:e1000852.
25. Nowroozalizadeh S., et al. Microbial translocation correlates with the severity of both HIV-1 and HIV-2 infections. J. Infect. Dis. 2010, 201:1150-1154.
26. Rajasuriar R., et al. Biological determinants of immune reconstitution in HIV-infected patients receiving antiretroviral therapy: the role of interleukin 7 and interleukin 7 receptor alpha and microbial translocation. J. Infect. Dis. 2010, 202:1254-1264.
27. + T cell activation during HIV infection. Nat. Med. 2010, 16:452-459.
28. Smith A.J., et al. A role for syndecan-1 and claudin-2 in microbial translocation during HIV-1 infection. J. Acquir. Immune Defic. Syndr. 2010, 55:306-315.
29. Wallet M.A., et al. Microbial translocation induces persistent macrophage activation unrelated to HIV-1 levels or T-cell activation following therapy. AIDS 2010, 24:1281-1290.
30. Bukh A.R., et al. Endotoxemia is associated with altered innate and adaptive immune responses in untreated HIV-1 infected individuals. PLoS ONE 2011, 6:e21275.
31. Chege D., et al. Sigmoid Th17 populations, the HIV latent reservoir, and microbial translocation in men on long-term antiretroviral therapy. AIDS 2011, 25:741-749.
32. d'Ettorre G., et al. HIV persistence in the gut mucosa of HIV-infected subjects undergoing antiretroviral therapy correlates with immune activation and increased levels of LPS. Curr. HIV Res. 2011, 9:148-153.
33. Kramski M., et al. Novel sensitive real-time PCR for quantification of bacterial 16S rRNA genes in plasma of HIV-infected patients as a marker for microbial translocation. J. Clin. Microbiol. 2011, 49:3691-3693.
34. Lim A., et al. Antibody and B-cell responses may control circulating lipopolysaccharide in patients with HIV infection. AIDS 2011, 25:1379-1383.
35. + cell count. AIDS 2011, 25:1385-1394.
36. Merlini E., et al. Evidence for polymicrobic flora translocating in peripheral blood of HIV-infected patients with poor immune response to antiretroviral therapy. PLoS ONE 2011, 6:e18580.
37. Papasavvas E., et al. Increased microbial translocation in ≤180 days old perinatally human immunodeficiency virus-positive infants as compared with human immunodeficiency virus-exposed uninfected infants of similar age. Pediatr. Infect. Dis. J. 2011, 30:877-882.
38. Sandler N.G., et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J. Infect. Dis. 2011, 203:780-790.
39. + T cell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J. Clin. Invest. 2012, 122:62-69.
40. Pandrea I., et al. Coagulation biomarkers predict disease progression in SIV-infected nonhuman primates. Blood 2012, 120:1357-1366.
41. Pilakka-Kanthikeel S., et al. Increased gut microbial translocation in HIV-infected children persists in virologic responders and virologic failures after antiretroviral therapy. Pediatr. Infect. Dis. J. 2012, 31:583-591.
42. + lymphocytes is associated with mucosal damage in SIV infection. Mucosal Immunol. 2012, 5:646-657.
43. Papasavvas E., et al. Delayed loss of control of plasma lipopolysaccharide levels after therapy interruption in chronically HIV-1-infected patients. AIDS 2009, 23:369-375.
44. Harris L.D., et al. Mechanisms underlying γδ T cell subset perturbations in SIV-infected Asian rhesus macaques. Blood 2010, 116:4148-4157.
45. Troseid M., et al. Elevated plasma levels of lipopolysaccharide and high mobility group box-1 protein are associated with high viral load in HIV-1 infection: reduction by 2-year antiretroviral therapy. AIDS 2010, 24:1733-1737.
46. Ellis C.L., et al. Molecular characterization of stool microbiota in HIV-infected subjects by panbacterial and order-Level 16S ribosomal DNA (rDNA) quantification and correlations with immune activation. J. Acquir. Immune Defic. Syndr. 2011, 57:363-370.
47. Lyons J.L., et al. Plasma sCD14 is a biomarker associated with impaired neurocognitive test performance in attention and learning domains in HIV infection. J. Acquir. Immune Defic. Syndr. 2011, 57:371-379.
48. Chaoul N., et al. Default in plasma and intestinal IgA responses during acute infection by simian immunodeficiency virus. Retrovirology 2012, 9:43.
49. Dyavar Shetty R., et al. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. J. Clin. Invest. 2012, 122:1712-1716.
50. Mohan M., et al. Focused examination of the intestinal lamina propria yields greater molecular insight into mechanisms underlying SIV induced immune dysfunction. PLoS ONE 2012, 7:e34561.
51. Funderburg N., et al. Toll-like receptor ligands induce human T cell activation and death, a model for HIV pathogenesis. PLoS ONE 2008, 3:e1915.
52. Brenchley J.M., Douek D.C. HIV infection and the gastrointestinal immune system. Mucosal Immunol. 2008, 1:23-30.
53. Douek D.C., et al. T cell dynamics in HIV-1 infection. Annu. Rev. Immunol. 2003, 21:265-304.
54. + T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J. Immunol. 2007, 179:3026-3034.
55. Paiardini M., et al. Lessons learned from the natural hosts of HIV-related viruses. Annu. Rev. Med. 2009, 60:485-495.
56. + T Cells and HIV: a paradoxical pas de deux. Sci. Transl. Med. 2012, 4:123ps124.
57. + T cells depleted?. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15572-15577.
58. Paiardini M., et al. Cell-cycle dysregulation in the immunopathogenesis of AIDS. Immunol. Res. 2004, 29:253-268.
59. + memory T cells in rapidly progressive simian immunodeficiency virus infection. J. Exp. Med. 2004, 200:1299-1314.
60. - natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 2010, 115:4439-4446.
61. Alter G., et al. Increased natural killer cell activity in viremic HIV-1 infection. J. Immunol. 2004, 173:5305-5311.
62. Moir S., Fauci A.S. B cells in HIV infection and disease. Nat. Rev. Immunol. 2009, 9:235-245.
63. Kwa S., et al. Plasmacytoid dendritic cells are recruited to the colorectum and contribute to immune activation during pathogenic SIV infection in rhesus macaques. Blood 2011, 118:2763-2773.
64. Reeves R.K., et al. SIV infection induces accumulation of plasmacytoid dendritic cells in the gut mucosa. J. Infect. Dis. 2012, 206:1462-1468.
65. Connolly N.C., et al. Proinflammatory cytokines in HIV disease - a review and rationale for new therapeutic approaches. AIDS Rev. 2005, 7:168-180.
66. + T cells and limiting reconstitution in HIV-1 and SIV infections through damage to the secondary lymphoid organ niche. Semin. Immunol. 2008, 20:181-186.
67. Sodora D.L., Silvestri G. Immune activation and AIDS pathogenesis. AIDS 2008, 22:439-446.
68. Appay V., Sauce D. Immune activation and inflammation in HIV-1 infection: causes and consequences. J. Pathol. 2008, 214:231-241.
69. Alter G., et al. Single-stranded RNA derived from HIV-1 serves as a potent activator of NK cells. J. Immunol. 2007, 178:7658-7666.
70. Iannello A., et al. Role of interleukin-18 in the development and pathogenesis of AIDS. AIDS Rev. 2009, 11:115-125.
71. Klatt N.R., Brenchley J.M. Th17 cell dynamics in HIV infection. Curr. Opin. HIV AIDS 2010, 5:135-140.
72. Hooper L.V., et al. Interactions between the microbiota and the immune system. Science 2012, 336:1268-1273.
73. Macpherson A.J., et al. Homeland security: IgA immunity at the frontiers of the body. Trends Immunol. 2012, 33:160-167.
74. Brenchley J.M., Douek D.C. Microbial translocation across the GI tract. Annu. Rev. Immunol. 2012, 30:149-173.
75. Lester R.T., et al. HIV-1 RNA dysregulates the natural TLR response to subclinical endotoxemia in Kenyan female sex-workers. PLoS ONE 2009, 4:e5644.
76. + blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 2007, 81:584-592.
77. Kim W.K., et al. Monocyte heterogeneity underlying phenotypic changes in monocytes according to SIV disease stage. J. Leukoc. Biol. 2009, 87:557-567.
78. Burdo T.H., et al. Soluble CD163, a novel marker of activated macrophages, is elevated and associated with noncalcified coronary plaque in HIV-infected patients. J. Infect. Dis. 2011, 204:1227-1236.
79. Mayne E., et al. Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression. J. Acquir. Immune Defic. Syndr. 2012, 59:340-346.
80. Favre D., et al. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog. 2009, 5:e1000295.
81. + T cell depletion. J. Immunol. 2008, 181:6687-6691.
82. Lee P.I., et al. Evidence for translocation of microbial products in patients with idiopathic CD4 lymphocytopenia. J. Infect. Dis. 2009, 199:1664-1670.
83. Sharpstone D., et al. Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut 1999, 45:70-76.
84. + mucosal NK cells during SIV infection. Blood 2011, 118:3321-3330.
85. Klatt N.R., et al. SIV infection of rhesus macaques results in dysfunctional T- and B-cell responses to neo and recall Leishmania major vaccination. Blood 2011, 118:5803-5812.
86. Pierson T., et al. Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu. Rev. Immunol. 2000, 18:665-708.
87. Page E.E., et al. HIV and hepatitis C coinfection: pathogenesis and microbial translocation. Curr. Opin. HIV AIDS 2011, 6:472-477.
88. Anselmi A., et al. Immune reconstitution in human immunodeficiency virus type 1-infected children with different virological responses to anti-retroviral therapy. Clin. Exp. Immunol. 2007, 150:442-450.
89. Pitrak D.L., et al. Discordant CD4 T lymphocyte responses to antiretroviral therapy for HIV infection are associated with ex-vivo rates of apoptosis. AIDS 2001, 15:1317-1319.
90. + T cell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy. J. Infect. Dis. 2003, 187:1534-1543.
91. Valdez H., et al. Limited immune restoration after 3 years' suppression of HIV-1 replication in patients with moderately advanced disease. AIDS 2002, 16:1859-1866.
92. Marchetti G., et al. Comparative analysis of T-cell turnover and homeostatic parameters in HIV-infected patients with discordant immune-virological responses to HAART. AIDS 2006, 20:1727-1736.
93. Tincati C., et al. Early initiation of highly active antiretroviral therapy fails to reverse immunovirological abnormalities in gut-associated lymphoid tissue induced by acute HIV infection. Antivir. Ther. 2009, 14:321-330.
94. + T-cell counts during antiretroviral therapy. AIDS 2010, 24:1991-2000.
95. Li Q., et al. Functional genomic analysis of the response of HIV-1-infected lymphatic tissue to antiretroviral therapy. J. Infect. Dis. 2004, 189:572-582.
96. Dyavar Shetty R.D., et al. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. J. Clin. Invest. 2012, 122:1712-1716.
97. Madsen K.L. The use of probiotics in gastrointestinal disease. Can. J. Gastroenterol. 2001, 15:817-822.
98. Hummelen R., et al. Effect of 25 weeks probiotic supplementation on immune function of HIV patients. Gut Microbes 2011, 2:80-85.
99. Hummelen R., et al. Altered host-microbe interaction in HIV: a target for intervention with pro- and prebiotics. Int. Rev. Immunol. 2010, 29:485-513.
100. + T cell effector responses via retinoic acid receptor alpha. Immunity 2011, 34:435-447.
101. Ivanov I.I., Littman D.R. Segmented filamentous bacteria take the stage. Mucosal Immunol. 2010, 3:209-212.
102. Cani P.D., et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009, 58:1091-1103.
103. Fuller D.H., et al. Therapeutic DNA vaccine induces broad T cell responses in the gut and sustained protection from viral rebound and AIDS in SIV-infected rhesus macaques. PLoS ONE 2012, 7:e33715.
104. Rainone V., et al. CCL28 induces mucosal homing of HIV-1-specific IgA-secreting plasma cells in mice immunized with HIV-1 virus-like particles. PLoS ONE 2011, 6:e26979.
105. Pegu P., et al. Induction of strong anti-HIV cellular immunity by a combination of Clostridium perfringens expressing HIV gag and virus like particles. Curr. HIV Res. 2011, 9:613-622.