The effect of HIV infection on the host response to bacterial sepsis

The Lancet Infectious Diseases

Volumn 15, Issue 1, 2015, Pages 95-108

  Huson, Michaëla A M ^a   Grobusch, Martin P ^a   van der Poll, Tom ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CYTOKINE; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR; IMMUNOLOGIC FACTOR;

ANTIVIRAL THERAPY; B LYMPHOCYTE; BLOOD CLOTTING; COMPLEMENT SYSTEM; DENDRITIC CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; LYMPHOCYTE; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NEUTROPHIL; REVIEW; SEPSIS; T LYMPHOCYTE; COMPLICATION; DISEASE PREDISPOSITION; IMMUNE SYSTEM; IMMUNOLOGY; PATHOLOGY; PATHOPHYSIOLOGY;

DISEASE SUSCEPTIBILITY; HIV INFECTIONS; HUMANS; IMMUNE SYSTEM; IMMUNOLOGIC FACTORS; SEPSIS;

EID: 84918532541     PISSN: 14733099     EISSN: 14744457     Source Type: Journal    
DOI: 10.1016/S1473-3099(14)70917-X     Document Type: Review

References (160)

1. Kim JH, Psevdos G, Gonzalez E, Singh S, Kilayko MC, Sharp V All-cause mortality in hospitalized HIV-infected patients at an acute tertiary care hospital with a comprehensive outpatient HIV care program in New York City in the era of highly active antiretroviral therapy (HAART). Infection 2013, 41:545-551.
2. Gilks CF, Ojoo SA, Ojoo JC, et al. Invasive pneumococcal disease in a cohort of predominantly HIV-1 infected female sex-workers in Nairobi, Kenya. Lancet 1996, 347:718-723.
3. Huson MA, Stolp SM, van der Poll T, Grobusch MP Community-acquired bacterial bloodstream infections in HIV-infected patients: a systematic review. Clin Infect Dis 2014, 58:79-92.
4. Jordano Q, Falcó V, Almirante B, et al. Invasive pneumococcal disease in patients infected with HIV: still a threat in the era of highly active antiretroviral therapy. Clin Infect Dis 2004, 38:1623-1628.
5. Archibald LK, den Dulk MO, Pallangyo KJ, Reller LB Fatal Mycobacterium tuberculosis bloodstream infections in febrile hospitalized adults in Dar es Salaam, Tanzania. Clin Infect Dis 1998, 26:290-296.
6. Archibald LK, McDonald LC, Nwanyanwu O, et al. A hospital-based prevalence survey of bloodstream infections in febrile patients in Malawi: implications for diagnosis and therapy. J Infect Dis 2000, 181:1414-1420.
7. Arthur G, Nduba VN, Kariuki SM, Kimari J, Bhatt SM, Gilks CF Trends in bloodstream infections among human immunodeficiency virus-infected adults admitted to a hospital in Nairobi, Kenya, during the last decade. Clin Infect Dis 2001, 33:248-256.
8. Bell M, Archibald LK, Nwanyanwu O, et al. Seasonal variation in the etiology of bloodstream infections in a febrile inpatient population in a developing country. Int J Infect Dis 2001, 5:63-69.
9. Crump JA, Ramadhani HO, Morrissey AB, et al. Invasive bacterial and fungal infections among hospitalized HIV-infected and HIV-uninfected adults and adolescents in northern Tanzania. Clin Infect Dis 2011, 52:341-348.
10. Grant AD, Djomand G, Smets P, et al. Profound immunosuppression across the spectrum of opportunistic disease among hospitalized HIV-infected adults in Abidjan, CÔte d'Ivoire. AIDS 1997, 11:1357-1364.
11. Mayanja BN, Todd J, Hughes P, et al. Septicaemia in a population-based HIV clinical cohort in rural Uganda, 1996-2007: incidence, aetiology, antimicrobial drug resistance and impact of antiretroviral therapy. Trop Med Int Health 2010, 15:697-705.
12. Meremo A, Mshana SE, Kidenya BR, Kabangila R, Peck R, Kataraihya JB High prevalence of Non-typhoid salmonella bacteraemia among febrile HIV adult patients admitted at a tertiary Hospital, North-Western Tanzania. Int Arch Med 2012, 5:28.
13. Nadjm B, Mtove G, Amos B, et al. Severe febrile illness in adult hospital admissions in Tanzania: a prospective study in an area of high malaria transmission. Trans R Soc Trop Med Hyg 2012, 106:688-695.
14. Peters RP, Zijlstra EE, Schijffelen MJ, et al. A prospective study of bloodstream infections as cause of fever in Malawi: clinical predictors and implications for management. Trop Med Int Health 2004, 9:928-934.
15. Ssali FN, Kamya MR, Wabwire-Mangen F, et al. A prospective study of community-acquired bloodstream infections among febrile adults admitted to Mulago Hospital in Kampala, Uganda. J Acquir Immune Defic Syndr Hum Retrovirol 1998, 19:484-489.
16. Angus DC, van der Poll T Severe sepsis and septic shock. N Engl J Med 2013, 369:840-851.
17. Hotchkiss RS, Monneret G, Payen D Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis 2013, 13:260-268.
18. Appay V, Sauce D Immune activation and inflammation in HIV-1 infection: causes and consequences. J Pathol 2008, 214:231-241.
19. Stearns-Kurosawa DJ, Osuchowski MF, Valentine C, Kurosawa S, Remick DG The pathogenesis of sepsis. Annu Rev Pathol 2011, 6:19-48.
20. Akira S, Uematsu S, Takeuchi O Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
21. van der Poll T, Opal SM Host-pathogen interactions in sepsis. Lancet Infect Dis 2008, 8:32-43.
22. Mancuso G, Gambuzza M, Midiri A, et al. Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells. Nat Immunol 2009, 10:587-594.
23. Cavassani KA, Ishii M, Wen H, et al. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 2008, 205:2609-2621.
24. Murphy KM Janeway's immunobiology 2012, Garland Science, New York. 8th edn.
25. Chiche L, Forel JM, Thomas G, et al. The role of natural killer cells in sepsis. J Biomed Biotechnol 2011, 986491.
26. Souza-Fonseca-Guimaraes F, Adib-Conquy M, Cavaillon JM Natural killer (NK) cells in antibacterial innate immunity: angels or devils?. Mol Med 2012, 18:270-285.
27. Leung B, Harris HW NKT cells: the culprits of sepsis?. J Surg Res 2011, 167:87-95.
28. Nathan C Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 2006, 6:173-182.
29. de Jong HK, van der Poll T, Wiersinga WJ The systemic pro-inflammatory response in sepsis. J Innate Immun 2010, 2:422-430.
30. Yang H, Antoine DJ, Andersson U, Tracey KJ The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J Leukoc Biol 2013, 93:865-873.
31. Epple HJ, Zeitz M HIV infection and the intestinal mucosal barrier. Ann N Y Acad Sci 2012, 1258:19-24.
32. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
33. Sanders CM, Cruse JM, Lewis RE Toll-like receptors, cytokines and HIV-1. Exp Mol Pathol 2008, 84:31-36.
34. Scagnolari C, Selvaggi C, Chiavuzzo L, et al. Expression levels of TLRs involved in viral recognition in PBMCs from HIV-1-infected patients failing antiretroviral therapy. Intervirology 2009, 52:107-114.
35. Hernández JC, Stevenson M, Latz E, Urcuqui-Inchima S HIV type 1 infection up-regulates TLR2 and TLR4 expression and function in vivo and in vitro. AIDS Res Hum Retroviruses 2012, 28:1313-1328.
36. Heggelund L, Müller F, Lien E, et al. Increased expression of toll-like receptor 2 on monocytes in HIV infection: possible roles in inflammation and viral replication. Clin Infect Dis 2004, 39:264-269.
37. Gordon SB, Jagoe RT, Jarman ER, et al. The alveolar microenvironment of patients infected with human immunodeficiency virus does not modify alveolar macrophage interactions with Streptococcus pneumoniae. Clin Vaccine Immunol 2013, 20:882-891.
38. Lester RT, Yao XD, Ball TB, et al. Toll-like receptor expression and responsiveness are increased in viraemic HIV-1 infection. AIDS 2008, 22:685-694.
39. Schuitemaker H, Kootstra NA, Fouchier RA, Hooibrink B, Miedema F Productive HIV-1 infection of macrophages restricted to the cell fraction with proliferative capacity. EMBO J 1994, 13:5929-5936.
40. Michailidis C, Giannopoulos G, Vigklis V, Armenis K, Tsakris A, Gargalianos P Impaired phagocytosis among patients infected by the human immunodeficiency virus: implication for a role of highly active anti-retroviral therapy. Clin Exp Immunol 2012, 167:499-504.
41. Trial J, Birdsall HH, Hallum JA, et al. Phenotypic and functional changes in peripheral blood monocytes during progression of human immunodeficiency virus infection. Effects of soluble immune complexes, cytokines, subcellular particulates from apoptotic cells, and HIV-1-encoded proteins on monocytes phagocytic function, oxidative burst, transendothelial migration, and cell surface phenotype. J Clin Invest 1995, 95:1690-1701.
42. Nottet HS, de Graaf L, de Vos NM, et al. Phagocytic function of monocyte-derived macrophages is not affected by human immunodeficiency virus type 1 infection. J Infect Dis 1993, 168:84-91.
43. Bandres JC, Trial J, Musher DM, Rossen RD Increased phagocytosis and generation of reactive oxygen products by neutrophils and monocytes of men with stage 1 human immunodeficiency virus infection. J Infect Dis 1993, 168:75-83.
44. Brown JN, Kohler JJ, Coberley CR, Sleasman JW, Goodenow MM HIV-1 activates macrophages independent of Toll-like receptors. PLoS One 2008, 3:e3664.
45. Gekonge B, Giri MS, Kossenkov AV, et al. Constitutive gene expression in monocytes from chronic HIV-1 infection overlaps with acute Toll-like receptor induced monocyte activation profiles. PLoS One 2012, 7:e41153.
46. Dutertre CA, Amraoui S, DeRosa A, et al. Pivotal role of M-DC8+ monocytes from viremic HIV-infected patients in TNFα overproduction in response to microbial products. Blood 2012, 120:2259-2268.
47. Haissman JM, Vestergaard LS, Sembuche S, et al. Plasma cytokine levels in Tanzanian HIV-1-infected adults and the effect of antiretroviral treatment. J Acquir Immune Defic Syndr 2009, 52:493-497.
48. Keating SM, Golub ET, Nowicki M, et al. The effect of HIV infection and HAART on inflammatory biomarkers in a population-based cohort of women. AIDS 2011, 25:1823-1832. the Women's Interagency HIV Study.
49. Kuritzkes DR Neutropenia, neutrophil dysfunction, and bacterial infection in patients with human immunodeficiency virus disease: the role of granulocyte colony-stimulating factor. Clin Infect Dis 2000, 30:256-260.
50. Silva JM, dos Santos SS Sepsis in AIDS patients: clinical, etiological and inflammatory characteristics. J Int AIDS Soc 2013, 16:17344.
51. Amancio RT, Japiassu AM, Gomes RN, et al. The innate immune response in HIV/AIDS septic shock patients: a comparative study. PLoS One 2013, 8:e68730.
52. Lester RT, Yao XD, Ball TB, et al. HIV-1 RNA dysregulates the natural TLR response to subclinical endotoxemia in Kenyan female sex-workers. PLoS One 2009, 4:e5644.
53. Tachado SD, Zhang J, Zhu J, Patel N, Koziel H HIV impairs TNF-alpha release in response to Toll-like receptor 4 stimulation in human macrophages in vitro. Am J Respir Cell Mol Biol 2005, 33:610-621.
54. Nicol MQ, Mathys JM, Pereira A, Ollington K, Ieong MH, Skolnik PR Human immunodeficiency virus infection alters tumor necrosis factor alpha production via Toll-like receptor-dependent pathways in alveolar macrophages and U1 cells. J Virol 2008, 82:7790-7798.
55. Gordon SB, Jarman ER, Kanyanda S, et al. Reduced interleukin-8 response to StreptococcuS pneumoniae by alveolar macrophages from adults with HIV/AIDS. AIDS 2005, 19:1197-1200.
56. Denis M, Ghadirian E Dysregulation of interleukin 8, interleukin 10, and interleukin 12 release by alveolar macrophages from HIV type 1-infected subjects. AIDS Res Hum Retroviruses 1994, 10:1619-1627.
57. Smed-Sörensen A, Loré K, Walther-Jallow L, Andersson J, Spetz AL HIV-1-infected dendritic cells up-regulate cell surface markers but fail to produce IL-12 p70 in response to CD40 ligand stimulation. Blood 2004, 104:2810-2817.
58. Frleta D, Ochoa CE, Kramer HB, et al. HIV-1 infection-induced apoptotic microparticles inhibit human DCs via CD44. J Clin Invest 2012, 122:4685-4697.
59. Benlahrech A, Gotch F, Kelleher P, Patterson S Loss of NK stimulatory capacity by plasmacytoid and monocyte-derived DC but not myeloid DC in HIV-1 infected patients. PLoS One 2011, 6:e17525.
60. Donaghy H, Gazzard B, Gotch F, Patterson S Dysfunction and infection of freshly isolated blood myeloid and plasmacytoid dendritic cells in patients infected with HIV-1. Blood 2003, 101:4505-4511.
61. Feldman S, Stein D, Amrute S, et al. Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin Immunol 2001, 101:201-210.
62. Chougnet C, Cohen SS, Kawamura T, et al. Normal immune function of monocyte-derived dendritic cells from HIV-infected individuals: implications for immunotherapy. J Immunol 1999, 163:1666-1673.
63. Sabado RL, O'Brien M, Subedi A, et al. Evidence of dysregulation of dendritic cells in primary HIV infection. Blood 2010, 116:3839-3852.
64. Dillon SM, Lee EJ, Bramante JM, Barker E, Wilson CC The natural killer cell interferon-gamma response to bacteria is diminished in untreated HIV-1 infection and defects persist despite viral suppression. J Acquir Immune Defic Syndr 2014, 65:259-267.
65. Vasan S, Tsuji M A double-edged sword: the role of NKT cells in malaria and HIV infection and immunity. Semin Immunol 2010, 22:87-96.
66. Ostrowski MA, Gu JX, Kovacs C, Freedman J, Luscher MA, MacDonald KS Quantitative and qualitative assessment of human immunodeficiency virus type 1 (HIV-1)-specific CD4+ T cell immunity to gag in HIV-1-infected individuals with differential disease progression: reciprocal interferon-gamma and interleukin-10 responses. J Infect Dis 2001, 184:1268-1278.
67. Kim CJ, McKinnon LR, Kovacs C, et al. Mucosal Th17 cell function is altered during HIV infection and is an independent predictor of systemic immune activation. J Immunol 2013, 191:2164-2173.
68. Jambo KC, Banda DH, Kankwatira AM, et al. Small alveolar macrophages are infected preferentially by HIV and exhibit impaired phagocytic function. Mucosal Immunol 2014, 7:1116-1126.
69. van der Poll T, Keogh CV, Buurman WA, Lowry SF Passive immunization against tumor necrosis factor-alpha impairs host defense during pneumococcal pneumonia in mice. Am J Respir Crit Care Med 1997, 155:603-608.
70. Olliver M, Hiew J, Mellroth P, Henriques-Normark B, Bergman P Human monocytes promote Th1 and Th17 responses to Streptococcus pneumoniae. Infect Immun 2011, 79:4210-4217.
71. Dockrell DH, Marriott HM, Prince LR, et al. Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J Immunol 2003, 171:5380-5388.
72. Patel NR, Zhu J, Tachado SD, et al. HIV impairs TNF-alpha mediated macrophage apoptotic response to Mycobacterium tuberculosis. J Immunol 2007, 179:6973-6980.
73. Dillon SM, Robertson KB, Pan SC, et al. Plasmacytoid and myeloid dendritic cells with a partial activation phenotype accumulate in lymphoid tissue during asymptomatic chronic HIV-1 infection. J Acquir Immune Defic Syndr 2008, 48:1-12.
74. Donaghy H, Pozniak A, Gazzard B, et al. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 2001, 98:2574-2576.
75. Loré K, Sönnerborg A, Broström C, et al. Accumulation of DC-SIGN+CD40+ dendritic cells with reduced CD80 and CD86 expression in lymphoid tissue during acute HIV-1 infection. AIDS 2002, 16:683-692.
76. Dillon SM, Friedlander LJ, Rogers LM, et al. Blood myeloid dendritic cells from HIV-1-infected individuals display a proapoptotic profile characterized by decreased Bcl-2 levels and by caspase-3+ frequencies that are associated with levels of plasma viremia and T cell activation in an exploratory study. J Virol 2011, 85:397-409.
77. Izmailova E, Bertley FM, Huang Q, et al. HIV-1 Tat reprograms immature dendritic cells to express chemoattractants for activated T cells and macrophages. Nat Med 2003, 9:191-197.
78. Granelli-Piperno A, Golebiowska A, Trumpfheller C, Siegal FP, Steinman RM HIV-1-infected monocyte-derived dendritic cells do not undergo maturation but can elicit IL-10 production and T cell regulation. Proc Natl Acad Sci USA 2004, 101:7669-7674.
79. Yonkers NL, Rodriguez B, Asaad R, Lederman MM, Anthony DD Systemic immune activation in HIV infection is associated with decreased MDC responsiveness to TLR ligand and inability to activate naive CD4 T-cells. PLoS One 2011, 6:e23884.
80. Funke J, Dürr R, Dietrich U, Koch J Natural killer cells in HIV-1 infection: a double-edged sword. AIDS Rev 2011, 13:67-76.
81. Azzoni L, Papasavvas E, Chehimi J, et al. Sustained impairment of IFN-gamma secretion in suppressed HIV-infected patients despite mature NK cell recovery: evidence for a defective reconstitution of innate immunity. J Immunol 2002, 168:5764-5770.
82. Jost S, Altfeld M Evasion from NK cell-mediated immune responses by HIV-1. Microbes Infect 2012, 14:904-915.
83. Mavilio D, Lombardo G, Kinter A, et al. Characterization of the defective interaction between a subset of natural killer cells and dendritic cells in HIV-1 infection. J Exp Med 2006, 203:2339-2350.
84. Kottilil S, Chun TW, Moir S, et al. Innate immunity in human immunodeficiency virus infection: effect of viremia on natural killer cell function. J Infect Dis 2003, 187:1038-1045.
85. Kottilil S, Shin K, Planta M, et al. Expression of chemokine and inhibitory receptors on natural killer cells: effect of immune activation and HIV viremia. J Infect Dis 2004, 189:1193-1198.
86. Mavilio D, Benjamin J, Daucher M, et al. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci USA 2003, 100:15011-15016.
87. Munyazesa E, Emile I, Mutimura E, et al. Assessment of haematological parameters in HIV-infected and uninfected Rwandan women: a cross-sectional study. BMJ Open 2012, 2:e001600.
88. Rubinstein DB, Farrington GK, O'Donnell C, Hartman KR, Wright DG Autoantibodies to leukocyte alphaMbeta2 integrin glycoproteins in HIV infection. Clin Immunol 1999, 90:352-359.
89. Elbim C, Prevot MH, Bouscarat F, et al. Polymorphonuclear neutrophils from human immunodeficiency virus-infected patients show enhanced activation, diminished fMLP-induced L-selectin shedding, and an impaired oxidative burst after cytokine priming. Blood 1994, 84:2759-2766.
90. Mauss S, Steinmetz HT, Willers R, et al. Induction of granulocyte colony-stimulating factor by acute febrile infection but not by neutropenia in HIV-seropositive individuals. J Acquir Immune Defic Syndr Hum Retrovirol 1997, 14:430-434.
91. Meddows-Taylor S, Pendle S, Tiemessen CT Altered expression of CD88 and associated impairment of complement 5a-induced neutrophil responses in human immunodeficiency virus type 1-infected patients with and without pulmonary tuberculosis. J Infect Dis 2001, 183:662-665.
92. Meddows-Taylor S, Martin DJ, Tiemessen CT Reduced expression of interleukin-8 receptors A and B on polymorphonuclear neutrophils from persons with human immunodeficiency virus type 1 disease and pulmonary tuberculosis. J Infect Dis 1998, 177:921-930.
93. Hofman P, Fischer F, Far DF, et al. Impairment of HIV polymorphonuclear leukocyte transmigration across T84 cell monolayers: an alternative mechanisms for increased intestinal bacterial infections in AIDS?. Eur Cytokine Netw 1999, 10:373-382.
94. Pos O, Stevenhagen A, Meenhorst PL, Kroon FP, Van Furth R Impaired phagocytosis of StaphylococcuS aureus by granulocytes and monocytes of AIDS patients. Clin Exp Immunol 1992, 88:23-28.
95. Schaumann R, Krosing J, Shah PM Phagocytosis of Escherichia coli and StaphylococcuS aureus by neutrophils of human immunodeficiency virus-infected patients. Eur J Med Res 1998, 3:546-548.
96. Roilides E, Mertins S, Eddy J, Walsh TJ, Pizzo PA, Rubin M Impairment of neutrophil chemotactic and bactericidal function in children infected with human immunodeficiency virus type 1 and partial reversal after in vitro exposure to granulocyte-macrophage colony-stimulating factor. J Pediatr 1990, 117:531-540.
97. Meddows-Taylor S, Kuhn L, Meyers TM, Sherman G, Tiemessen CT Defective neutrophil degranulation induced by interleukin-8 and complement 5a and down-regulation of associated receptors in children vertically infected with human immunodeficiency virus type 1. Clin Diagn Lab Immunol 2001, 8:21-30.
98. Saitoh T, Komano J, Saitoh Y, et al. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 2012, 12:109-116.
99. Keating SM, Jacobs ES, Norris PJ Soluble mediators of inflammation in HIV and their implications for therapeutics and vaccine development. Cytokine Growth Factor Rev 2012, 23:193-206.
100. Nowak P, Barqasho B, Sönnerborg A Elevated plasma levels of high mobility group box protein 1 in patients with HIV-1 infection. AIDS 2007, 21:869-871.
101. Bjerk SM, Baker JV, Emery S, et al. Biomarkers and bacterial pneumonia risk in patients with treated HIV infection: a case-control study. PLoS one 2013, 8:e56249. the INSIGHT SMART Study Group.
102. Vanham G, Penne L, Devalck J, et al. Decreased CD40 ligand induction in CD4 T cells and dysregulated IL-12 production during HIV infection. Clin Exp Immunol 1999, 117:335-342.
103. Kelly-Scumpia KM, Scumpia PO, Weinstein JS, et al. B cells enhance early innate immune responses during bacterial sepsis. J Exp Med 2011, 208:1673-1682.
104. Kasten KR, Tschöp J, Adediran SG, Hildeman DA, Caldwell CC T cells are potent early mediators of the host response to sepsis. Shock 2010, 34:327-336.
105. Boomer JS, To K, Chang KC, et al. Immunosuppression in patients who die of sepsis and multiple organ failure. JAMA 2011, 306:2594-2605.
106. Gougeon ML To kill or be killed: how HIV exhausts the immune system. Cell Death Differ 2005, 12(suppl 1):845-854.
107. Piguet V, Schwartz O, Le Gall S, Trono D The downregulation of CD4 and MHC-I by primate lentiviruses: a paradigm for the modulation of cell surface receptors. Immunol Rev 1999, 168:51-63.
108. Daigneault M, De Silva TI, Bewley MA, et al. Monocytes regulate the mechanism of T-cell death by inducing Fas-mediated apoptosis during bacterial infection. PLoS Pathog 2012, 8:e1002814.
109. Klatt NR, Brenchley JM Th17 cell dynamics in HIV infection. Curr Opin HIV AIDS 2010, 5:135-140.
110. Leeansyah E, Ganesh A, Quigley MF, et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 2013, 121:1124-1135.
111. Cosgrove C, Ussher JE, Rauch A, et al. Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood 2013, 121:951-961.
112. Greathead L, Metcalf R, Gazzard B, Gotch F, Steel A, Kelleher P CD8+/CD161++ mucosal-associated invariant T-cell levels in the colon are restored on long-term antiretroviral therapy and correlate with CD8+ T-cell immune activation. AIDS 2014, 28:1690-1692.
113. Gold MC, Lewinsohn DM Co-dependents: MR1-restricted MAIT cells and their antimicrobial function. Nat Rev Microbiol 2013, 11:14-19.
114. Rubino SJ, Geddes K, Girardin SE Innate IL-17 and IL-22 responses to enteric bacterial pathogens. Trends Immunol 2012, 33:112-118.
115. Zhang Z, Clarke TB, Weiser JN Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 2009, 119:1899-1909.
116. Catalfamo M, Wilhelm C, Tcheung L, et al. CD4 and CD8 T cell immune activation during chronic HIV infection: roles of homeostasis, HIV, type I IFN, and IL-7. J Immunol 2011, 186:2106-2116.
117. Sachdeva M, Fischl MA, Pahwa R, Sachdeva N, Pahwa S Immune exhaustion occurs concomitantly with immune activation and decrease in regulatory T cells in viremic chronically HIV-1-infected patients. J Acquir Immune Defic Syndr 2010, 54:447-454.
118. Larsson M, Shankar EM, Che KF, et al. Molecular signatures of T-cell inhibition in HIV-1 infection. Retrovirology 2013, 10:31.
119. Champagne P, Ogg GS, King AS, et al. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 2001, 410:106-111.
120. Appay V, Nixon DF, Donahoe SM, et al. HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J Exp Med 2000, 192:63-75.
121. Andersson J, Behbahani H, Lieberman J, et al. Perforin is not co-expressed with granzyme A within cytotoxic granules in CD8 T lymphocytes present in lymphoid tissue during chronic HIV infection. AIDS 1999, 13:1295-1303.
122. Lange CG, Valdez H, Medvik K, Asaad R, Lederman MM CD4+ T-lymphocyte nadir and the effect of highly active antiretroviral therapy on phenotypic and functional immune restoration in HIV-1 infection. Clin Immunol 2002, 102:154-161.
123. Moir S, Fauci AS Insights into B cells and HIV-specific B-cell responses in HIV-infected individuals. Immunol Rev 2013, 254:207-224.
124. 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, 178:8212-8220.
125. Qiao X, He B, Chiu A, Knowles DM, Chadburn A, Cerutti A Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol 2006, 7:302-310.
126. Nielsen H, Kvinesdal B, Benfield TL, Lundgren JD, Konradsen HB Rapid loss of specific antibodies after pneumococcal vaccination in patients with human immunodeficiency virus-1 infection. Scand J Infect Dis 1998, 30:597-601.
127. Malaspina A, Moir S, Kottilil S, et al. Deleterious effect of HIV-1 plasma viremia on B cell costimulatory function. J Immunol 2003, 170:5965-5972.
128. Pensieroso S, Galli L, Nozza S, et al. B-cell subset alterations and correlated factors in HIV-1 infection. AIDS 2013, 27:1209-1217.
129. Moir S, Ho J, Malaspina A, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med 2008, 205:1797-1805.
130. Moir S, Buckner CM, Ho J, et al. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy. Blood 2010, 116:5571-5579.
131. Jacobson MA, Khayam-Bashi H, Martin JN, Black D, Ng V Effect of long-term highly active antiretroviral therapy in restoring HIV-induced abnormal B-lymphocyte function. J Acquir Immune Defic Syndr 2002, 31:472-477.
132. Iwajomo OH, Finn A, Moons P, et al. Deteriorating pneumococcal-specific B-cell memory in minimally symptomatic African children with HIV infection. J Infect Dis 2011, 204:534-543.
133. Moja P, Jalil A, Quesnel A, et al. Humoral immune response within the lung in HIV-1 infection. Clin Exp Immunol 1997, 110:341-348.
134. Gordon SB, Miller DE, Day RB, et al. Pulmonary immunoglobulin responses to StreptococcuS pneumoniae are altered but not reduced in human immunodeficiency virus-infected Malawian adults. J Infect Dis 2003, 188:666-670.
135. Takahashi H, Oishi K, Yoshimine H, et al. Decreased serum opsonic activity against StreptococcuS pneumoniae in human immunodeficiency virus-infected Ugandan adults. Clin Infect Dis 2003, 37:1534-1540.
136. MacLennan CA, Gilchrist JJ, Gordon MA, et al. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 2010, 328:508-512.
137. Matta F, Yaekoub AY, Stein PD Human immunodeficiency virus infection and risk of venous thromboembolism. Am J Med Sci 2008, 336:402-406.
138. Jong E, Louw S, van Gorp EC, Meijers JC, ten Cate H, Jacobson BF The effect of initiating combined antiretroviral therapy on endothelial cell activation and coagulation markers in South African HIV-infected individuals. Thromb Haemost 2010, 104:1228-1234.
139. Koppel K, Bratt G, Schulman S, Bylund H, Sandström E Hypofibrinolytic state in HIV-1-infected patients treated with protease inhibitor-containing highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2002, 29:441-449.
140. Holme PA, Müller F, Solum NO, Brosstad F, Frøland SS, Aukrust P Enhanced activation of platelets with abnormal release of RANTES in human immunodeficiency virus type 1 infection. FASEB J 1998, 12:79-89.
141. Mayne E, Funderburg NT, Sieg SF, 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.
142. Funderburg NT, Mayne E, Sieg SF, 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.
143. Lafeuillade A, Alessi MC, Poizot-Martin I, et al. Endothelial cell dysfunction in HIV infection. J Acquir Immune Defic Syndr 1992, 5:127-131.
144. Ross AC, Armentrout R, O'Riordan MA, et al. Endothelial activation markers are linked to HIV status and are independent of antiretroviral therapy and lipoatrophy. J Acquir Immune Defic Syndr 2008, 49:499-506.
145. Solages A, Vita JA, Thornton DJ, et al. Endothelial function in HIV-infected persons. Clin Infect Dis 2006, 42:1325-1332.
146. Zietz C, Hotz B, Stürzl M, Rauch E, Penning R, Löhrs U Aortic endothelium in HIV-1 infection: chronic injury, activation, and increased leukocyte adherence. Am J Pathol 1996, 149:1887-1898.
147. Joshi VV, Pawel B, Connor E, et al. Arteriopathy in children with acquired immune deficiency syndrome. Pediatr Pathol 1987, 7:261-275.
148. Mankhambo LA, Banda DL, Jeffers G, et al. The role of angiogenic factors in predicting clinical outcome in severe bacterial infection in Malawian children. Crit Care Med 2010, 14:R91. the IPD Study Group.
149. de Larrañaga GF, Bocassi AR, Puga LM, Alonso BS, Benetucci JA Endothelial markers and HIV infection in the era of highly active antiretroviral treatment. Thromb Res 2003, 110:93-98.
150. de Gaetano Donati K, Rabagliati R, Tumbarello M, et al. Increased soluble markers of endothelial dysfunction in HIV-positive patients under highly active antiretroviral therapy. AIDS 2003, 17:765-768.
151. Rittirsch D, Redl H, Huber-Lang M Role of complement in multiorgan failure. Clin Dev Immunol 2012, 2012:962927.
152. Huber G, Bánki Z, Lengauer S, Stoiber H Emerging role for complement in HIV infection. Curr Opin HIV AIDS 2011, 6:419-426.
153. Yefenof E, Asjö B, Klein E Alternative complement pathway activation by HIV infected cells: C3 fixation does not lead to complement lysis but enhances NK sensitivity. Int Immunol 1991, 3:395-401.
154. Dellinger RP, Levy MM, Rhodes A, et al. Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit Care Med 2013, 41:580-637. the Surviving Sepsis Campaign Guidelines Committee including the Pediatric Subgroup.
155. Hutchins NA, Unsinger J, Hotchkiss RS, Ayala A The new normal: immunomodulatory agents against sepsis immune suppression. Trends Mol Med 2014, 20:224-233.
156. Fagard C, Le Braz M, Günthard H, et al. A controlled trial of granulocyte macrophage-colony stimulating factor during interruption of HAART. AIDS 2003, 17:1487-1492. the Swiss HIV Cohort Study.
157. Porichis F, Hart MG, Zupkosky J, et al. Differential impact of PD-1 and/or interleukin-10 blockade on HIV-1-specific CD4 T cell and antigen-presenting cell functions. J Virol 2014, 88:2508-2518.
158. Vanham G, Van Gulck E Can immunotherapy be useful as a "functional cure" for infection with Human Immunodeficiency Virus-1?. Retrovirology 2012, 9:72.
159. Zhou H, Ji X, Wu Y, et al. A dual-role of Gu-4 in suppressing HMGB1 secretion and blocking HMGB1 pro-inflammatory activity during inflammation. PLoS one 2014, 9:e89634.
160. Vincent JL, Ramesh MK, Ernest D, et al. A randomized, double-blind, placebo-controlled, Phase 2b study to evaluate the safety and efficacy of recombinant human soluble thrombomodulin, ART-123, in patients with sepsis and suspected disseminated intravascular coagulation. Crit Care Med 2013, 41:2069-2079.