Immune activation in the course of HIV-1 infection: Causes, phenotypes and persistence under therapy

HIV Medicine

Volumn 17, Issue 2, 2016, Pages 89-105

  Younas, M ^a   Psomas, C ^b,c   Reynes, J ^b,c,d   Corbeau, P ^a,d,e  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b MONTPELLIER UNIVERSITY HOSPITAL   (France)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^d UNIV MONTPELLIER   (France)

^e NÎMES UNIVERSITY HOSPITAL   (France)

Author keywords

Antiretroviral therapy; Cell activation; Coagulation; Endothelium; Inflammation; Microbial translocation

Indexed keywords

ANTIRETROVIRUS AGENT; CD27 ANTIGEN; CD28 ANTIGEN; CD4 ANTIGEN; CD57 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 22; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL STIMULATION; DENDRITIC CELL; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; ENDOTHELIUM CELL; GENETIC BACKGROUND; GENETIC POLYMORPHISM; HEREDITY; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE DYSREGULATION; IMMUNOREACTIVITY; IMMUNOSENESCENCE; IMMUNOSTIMULATION; INFLAMMATION; INTESTINE FLORA; LYMPHOCYTOPENIA; MACROPHAGE; MEMORY T LYMPHOCYTE; MIXED INFECTION; MONOCYTE; NATURAL KILLER CELL; NEUTROPHIL; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; UPREGULATION; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DISEASE COURSE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV INFECTIONS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; INTESTINE MUCOSA; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOPHYSIOLOGY; VIRUS LOAD;

ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BIOMARKERS; CD4-CD8 RATIO; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; HIV INFECTIONS; HIV-1; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; LYMPHOCYTE ACTIVATION; PHENOTYPE; VIRAL LOAD;

EID: 84956771902     PISSN: 14642662     EISSN: 14681293     Source Type: Journal    
DOI: 10.1111/hiv.12310     Document Type: Article

References (214)

1. Lawn SD, Butera ST, Folks TM. Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin Microbiol Rev 2001; 14: 753-777.
2. Beignon AS, McKenna K, Skoberne M et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 2005; 115: 3265-3275.
3. Doitsh G, Cavrois M, Lassen KG et al. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 2010; 143: 789-801.
4. 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: 749-759.
5. Ellis CL, Ma ZM, Mann SK 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.
6. Dillon SM, Lee EJ, Kotter CV et al. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol 2014; 7: 983-994.
7. Dinh DM, Volpe GE, Duffalo C et al. The intestinal microbiota, microbial translocation and systemic inflammation in chronic HIV infection. J Infect Dis 2015; 211: 19-27.
8. Somsouk M, Dunham RM, Cohen M et al. The immunologic effects of mesalamine in treated HIV-infected individuals with incomplete CD4+ T cell recovery: a randomized crossover trial. PLoS ONE 2014; 9: e116306.
9. Villar-Garcia J, Hernandez JJ, Guerri-Fernandez R et al. Effect of probiotics (Saccharomyces boulardii) on microbial translocation and inflammation in HIV-treated patients: a double-blind, randomized, placebo-controlled trial. J Acquir Immune Defic Syndr 2014; 68: 256-263.
10. Kovacs A, Al-Harthi L, Christensen S, Mack W, Cohen M, Landay A. CD8(+) T cell activation in women coinfected with human immunodeficiency virus type 1 and hepatitis C virus. J Infect Dis 2008; 197: 1402-1407.
11. Gonzalez VD, Falconer K, Blom KG et al. High levels of chronic immune activation in the T-cell compartments of patients coinfected with hepatitis C virus and human immunodeficiency virus type 1 and on highly active antiretroviral therapy are reverted by alpha interferon and ribavirin treatment. J Virol 2009;83:11407-11411.
12. Bautista-Amorocho H, Castellanos-Dominguez YZ, Rodriguez-Villamizar LA, Velandia-Cruz SA, Becerra-Pena JA, Farfan-Garcia AE. Epidemiology, risk factors and genotypes of HBV in HIV-infected patients in the Northeast region of Colombia: high prevalence of occult hepatitis B and F3 subgenotype dominance. PLoS ONE 2014; 9: e114272.
13. Sheth PM, Sunderji S, Shin LY et al. Coinfection with herpes simplex virus type 2 is associated with reduced HIV-specific T cell responses and systemic immune activation. J Infect Dis 2008; 197: 1394-1401.
14. Masia M, Robledano C, Ortiz de la Tabla V et al. Coinfection with human herpesvirus 8 is associated with persistent inflammation and immune activation in virologically suppressed HIV-infected patients. PLoS ONE 2014; 9: e105442.
15. Petrara MR, Cattelan AM, Zanchetta M et al. Epstein-Barr virus load and immune activation in human immunodeficiency virus type 1-infected patients. J Clin Virol 2012; 53: 195-200.
16. Gianella S, Strain MC, Rought SE et al. Associations between virologic and immunologic dynamics in blood and in the male genital tract. J Virol 2012; 86: 1307-1315.
17. Hunt P, Martin J, Sinclair E et al. Valganciclovir reduces CD8+ T cell activation among HIV-infected patients with suboptimal CD4+ T cell recovery during ART. 17th Conference on Retroviruses and Opportunistic Infections. San Francisco, CA, February 2010 [Abstract 380].
18. Ticona E, Huaman MA, Yanque O, Zunt JR. HIV and HTLV-1 coinfection: the need to initiate antiretroviral therapy. J Int Ass Provid AIDS Care 2013; 12: 373-374.
19. Zonios DI, Falloon J, Bennett JE et al. Idiopathic CD4+ lymphocytopenia: natural history and prognostic factors. Blood 2008; 112: 287-294.
20. Sereti I, Dunham RM, Spritzler J et al. IL-7 administration drives T cell-cycle entry and expansion in HIV-1 infection. Blood 2009; 113: 6304-6314.
21. Effros RB, Cai Z, Linton PJ. CD8 T cells and aging. Crit Rev Immunol 2003; 23: 45-64.
22. Deeks SG. HIV: how to escape treatment. Nature 2011; 477: 36-37.
23. Erikstrup C, Kallestrup P, Zinyama-Gutsire RB et al. Reduced mortality and CD4 cell loss among carriers of the interleukin-10 -1082G allele in a Zimbabwean cohort of HIV-1-infected adults. AIDS 2007; 21: 2283-2291.
24. Chang J, Lindsay RJ, Kulkarni S, Lifson JD, Carrington M, Altfeld M. Polymorphisms in interferon regulatory factor 7 reduce interferon-alpha responses of plasmacytoid dendritic cells to HIV-1. AIDS 2011; 25: 715-717.
25. Soria A, Guerini FR, Bandera A et al. KIR-HLA genotypes in HIV-infected patients lacking immunological recovery despite effective antiretroviral therapy. PLoS ONE 2011; 6: e27349.
26. Kanwar B, Favre D, McCune JM. Th17 and regulatory T cells: implications for AIDS pathogenesis. Curr Opin HIV AIDS 2010; 5: 151-157.
27. Chevalier MF, Petitjean G, Dunyach-Remy C et al. The Th17/Treg ratio, IL-1RA and sCD14 levels in primary HIV infection predict the T-cell activation set point in the absence of systemic microbial translocation. PLoS Pathog 2013; 9: e1003453.
28. Palmer S, Maldarelli F, Wiegand A et al. Low-level viremia persists for at least 7 years in patients on suppressive antiretroviral therapy. Proc Natl Acad Sci USA 2008; 105: 3879-3884.
29. 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;77:11708-11717.
30. Corbeau P, Reynes J. Immune reconstitution under antiretroviral therapy: the new challenge in HIV-1 infection. Blood 2011; 117: 5582-5590.
31. Stone SF, Price P, French MA. Dysregulation of CD28 and CTLA-4 expression by CD4 T cells from previously immunodeficient HIV-infected patients with sustained virological responses to highly active antiretroviral therapy. HIV Med 2005; 6: 278-283.
32. Lin RY, Nygren EJ, Valinsky JE, Ralph HE. T cell immunophenotypes and DR antigen expression in intravenous drug users. Relationship to human immunodeficiency virus serology. Int Arch Allergy Appl Immunol 1988;87:263-268.
33. Giorgi JV, Liu Z, Hultin LE, Cumberland WG, Hennessey K, Detels R. Elevated levels of CD38+ CD8+ T cells in HIV infection add to the prognostic value of low CD4+ T cell levels: results of 6 years of follow-up. The Los Angeles Center, Multicenter AIDS Cohort Study. J Acquir Immune Defic Syndr 1993; 6: 904-912.
34. Hazenberg MD, Otto SA, van Benthem BH et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17: 1881-1888.
35. Hazenberg MD, Stuart JW, Otto SA 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 2000; 95: 249-255.
36. Sachsenberg N, Perelson AS, Yerly S et al. Turnover of CD4+ and CD8+ T lymphocytes in HIV-1 infection as measured by Ki-67 antigen. J Exp Med 1998; 187: 1295-1303.
37. Gorochov G, Neumann AU, Kereveur A et al. Perturbation of CD4+ and CD8+ T-cell repertoires during progression to AIDS and regulation of the CD4+ repertoire during antiviral therapy. Nat Med 1998; 4: 215-221.
38. Hellerstein M, Hanley MB, Cesar D et al. Directly measured kinetics of circulating T lymphocytes in normal and HIV-1-infected humans. Nat Med 1999; 5: 83-89.
39. Wilson JD, Ogg GS, Allen RL et al. Oligoclonal expansions of CD8(+) T cells in chronic HIV infection are antigen specific. J Exp Med 1998; 188: 785-790.
40. Day CL, Kaufmann DE, Kiepiela P et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443: 350-354.
41. Kaufmann DE, Kavanagh DG, Pereyra F et al. Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat Immunol 2007; 8: 1246-1254.
42. Jones RB, Ndhlovu LC, Barbour JD et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 2008; 205: 2763-2779.
43. Wolthers KC, Bea G, Wisman A et al. T cell telomere length in HIV-1 infection: no evidence for increased CD4+ T cell turnover. Science 1996; 274: 1543-1547.
44. Gamberg J, Pardoe I, Bowmer MI, Howley C, Grant M. Lack of CD28 expression on HIV-specific cytotoxic T lymphocytes is associated with disease progression. Immunol Cell Biol 2004; 82: 38-46.
45. Lewis DE, Yang L, Luo W, Wang X, Rodgers JR. HIV-specific cytotoxic T lymphocyte precursors exist in a CD28-CD8+ T cell subset and increase with loss of CD4 T cells. AIDS 1999; 13: 1029-1033.
46. Appay V, Rowland-Jones SL. Premature ageing of the immune system: the cause of AIDS? Trends Immunol 2002; 23: 580-585.
47. Bucy RP, Hockett RD, Derdeyn CA et al. Initial increase in blood CD4(+) lymphocytes after HIV antiretroviral therapy reflects redistribution from lymphoid tissues. J Clin Invest 1999; 103: 1391-1398.
48. Hunt PW, Deeks SG, Rodriguez B et al. Continued CD4 cell count increases in HIV-infected adults experiencing 4 years of viral suppression on antiretroviral therapy. AIDS 2003; 17: 1907-1915.
49. Cockerham LR, Jain V, Sinclair E et al. Programmed death-1 expression on CD4+ and CD8+ T cells in treated and untreated HIV disease. AIDS 2014; 28: 1749-1758.
50. Harari A, Petitpierre S, Vallelian F, Pantaleo G. Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 2004; 103: 966-972.
51. Kovacs JA, Lempicki RA, Sidorov IA et al. Identification of dynamically distinct subpopulations of T lymphocytes that are differentially affected by HIV. J Exp Med 2001; 194: 1731-1741.
52. Watanabe N, De Rosa SC, Cmelak A, Hoppe R, Herzenberg LA, Roederer M. Long-term depletion of naive T cells in patients treated for Hodgkin's disease. Blood 1997; 90: 3662-3672.
53. Dai Z, Lakkis FG. Cutting edge: secondary lymphoid organs are essential for maintaining the CD4, but not CD8, naive T cell pool. J Immunol 2001; 167: 6711-6715.
54. Widney D, Gundapp G, Said JW et al. Aberrant expression of CD27 and soluble CD27 (sCD27) in HIV infection and in AIDS-associated lymphoma. Clin Immunol 1999; 93: 114-123.
55. Sadeghi M, Susal C, Daniel V et al. Short communication: decreasing soluble CD30 and increasing IFN-gamma plasma levels are indicators of effective highly active antiretroviral therapy. AIDS Res Hum Retroviruses 2007; 23: 886-890.
56. Wolf K, Tsakiris DA, Weber R, Erb P, Battegay M. Antiretroviral therapy reduces markers of endothelial and coagulation activation in patients infected with human immunodeficiency virus type 1. J Infect Dis 2002; 185: 456-462.
57. Regidor DL, Detels R, Breen EC et al. Effect of highly active antiretroviral therapy on biomarkers of B-lymphocyte activation and inflammation. AIDS 2011; 25: 303-314.
58. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, Fauci AS. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 1983; 309: 453-458.
59. Ho J, Moir S, Malaspina A et al. Two overrepresented B cell populations in HIV-infected individuals undergo apoptosis by different mechanisms. Proc Natl Acad Sci USA 2006;103:19436-19441.
60. Moir S, Malaspina A, Ho J et al. Normalization of B cell counts and subpopulations after antiretroviral therapy in chronic HIV disease. J Infect Dis 2008; 197: 572-579.
61. Moir S, Malaspina A, Pickeral OK et al. Decreased survival of B cells of HIV-viremic patients mediated by altered expression of receptors of the TNF superfamily. J Exp Med 2004; 200: 587-599.
62. Fournier AM, Baillat V, Alix-Panabieres C et al. Dynamics of spontaneous HIV-1 specific and non-specific B-cell responses in patients receiving antiretroviral therapy. AIDS 2002; 16: 1755-1760.
63. Ng VL. B-lymphocytes and autoantibody profiles in HIV disease. Clin Rev Allergy Immunol 1996; 14: 367-384.
64. Biggar RJ. AIDS-related cancers in the era of highly active antiretroviral therapy. Oncology (Williston Park) 2001;15:439-448 discussion 48-49.
65. Malaspina A, Moir S, Kottilil S et al. Deleterious effect of HIV-1 plasma viremia on B cell costimulatory function. J Immunol 2003 Jun 15; 170: 5965-5972.
66. De Milito A, Morch C, Sonnerborg A, Chiodi F. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 2001; 15: 957-964.
67. Nagase H, Agematsu K, Kitano K et al. Mechanism of hypergammaglobulinemia by HIV infection: circulating memory B-cell reduction with plasmacytosis. Clin Immunol 2001; 100: 250-259.
68. Malaspina A, Moir S, Ho J et al. Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7. Proc Natl Acad Sci USA 2006; 103: 2262-2267.
69. 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.
70. 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.
71. 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: 2180-2186.
72. 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.
73. Yang OO, Wilson SB, Hultin LE et al. Delayed reconstitution of CD4+ iNKT cells after effective HIV type 1 therapy. AIDS Res Hum Retroviruses 2007 Jul; 23: 913-922.
74. Ibarrondo FJ, Yang OO, Chodon T et al. Natural killer T cells in advanced melanoma patients treated with tremelimumab. PLoS ONE 2013; 8: e76829.
75. Moll M, Kuylenstierna C, Gonzalez VD et al. Severe functional impairment and elevated PD-1 expression in CD1d-restricted NKT cells retained during chronic HIV-1 infection. Eur J Immunol 2009 Mar; 39: 902-911.
76. Snyder-Cappione JE, Loo CP, Carvalho KI et al. Lower cytokine secretion ex vivo by natural killer T cells in HIV-infected individuals is associated with higher CD161 expression. AIDS 2009; 23: 1965-1970.
77. Fogli M, Costa P, Murdaca G et al. Significant NK cell activation associated with decreased cytolytic function in peripheral blood of HIV-1-infected patients. Eur J Immunol 2004; 34: 2313-2321.
78. Kottilil S, Jackson JO, Reitano KN et al. Innate immunity in HIV infection: enhanced susceptibility to CD95-mediated natural killer cell death and turnover induced by HIV viremia. J Acquir Immune Defic Syndr 2007; 46: 151-159.
79. Norris S, Coleman A, Kuri-Cervantes L, Bower M, Nelson M, Goodier MR. PD-1 expression on natural killer cells and CD8(+) T cells during chronic HIV-1 infection. Viral Immunol 2012;25:329-332.
80. Hong HS, Eberhard JM, Keudel P et al. Phenotypically and functionally distinct subsets contribute to the expansion of CD56-/CD16+ natural killer cells in HIV infection. AIDS 2010; 24: 1823-1834.
81. Portales P, Reynes J, Pinet V et al. Interferon-alpha restores HIV-induced alteration of natural killer cell perforin expression in vivo. AIDS 2003; 17: 495-504.
82. 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.
83. Brenner BG, Dascal A, Margolese RG, Wainberg MA. Natural killer cell function in patients with acquired immunodeficiency syndrome and related diseases. J Leukoc Biol 1989; 46: 75-83.
84. Mavilio D, Lombardo G, Benjamin J et al. Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci USA 2005; 102: 2886-2891.
85. Sondergaard SR, Aladdin H, Ullum H, Gerstoft J, Skinhoj P, Pedersen BK. Immune function and phenotype before and after highly active antiretroviral therapy. J Acquir Immune Defic Syndr 1999; 21: 376-383.
86. Lichtfuss GF, Cheng WJ, Farsakoglu Y et al. Virologically suppressed HIV patients show activation of NK cells and persistent innate immune activation. J Immunol 2012; 189: 1491-1499.
87. Fontaine J, Chagnon-Choquet J, Valcke HS, Poudrier J, Roger M. High expression levels of B lymphocyte stimulator (BLyS) by dendritic cells correlate with HIV-related B-cell disease progression in humans. Blood 2011; 117: 145-155.
88. Almeida M, Cordero M, Almeida J, Orfao A. Different subsets of peripheral blood dendritic cells show distinct phenotypic and functional abnormalities in HIV-1 infection. AIDS 2005; 19: 261-271.
89. Sabado RL, O'Brien M, Subedi A et al. Evidence of dysregulation of dendritic cells in primary HIV infection. Blood 2010;116:3839-3852.
90. 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.
91. 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.
92. Lehmann C, Harper JM, Taubert D et al. Increased interferon alpha expression in circulating plasmacytoid dendritic cells of HIV-1-infected patients. J Acquir Immune Defic Syndr 2008; 48: 522-530.
93. Tilton JC, Manion MM, Luskin MR et al. Human immunodeficiency virus viremia induces plasmacytoid dendritic cell activation in vivo and diminished alpha interferon production in vitro. J Virol 2008; 82: 3997-4006.
94. Papagno L, Spina CA, Marchant A et al. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol 2004; 2: E20.
95. 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.
96. Laforge M, Campillo-Gimenez L, Monceaux V et al. HIV/SIV infection primes monocytes and dendritic cells for apoptosis. PLoS Pathog 2011; 7: e1002087.
97. Lehmann C, Jung N, Forster K et al. Longitudinal analysis of distribution and function of plasmacytoid dendritic cells in peripheral blood and gut mucosa of HIV infected patients. J Infect Dis 2014; 209: 940-949.
98. Elbim C, Pillet S, Prevost MH et al. Redox and activation status of monocytes from human immunodeficiency virus-infected patients: relationship with viral load. J Virol 1999; 73: 4561-4566.
99. Almeida M, Cordero M, Almeida J, Orfao A. Relationship between CD38 expression on peripheral blood T-cells and monocytes, and response to antiretroviral therapy: a one-year longitudinal study of a cohort of chronically infected ART-naive HIV-1+ patients. Cytometry B Clin Cytom 2007; 72: 22-33.
100. Fischer-Smith T, Tedaldi EM, Rappaport J. CD163/CD16 coexpression by circulating monocytes/macrophages in HIV: potential biomarkers for HIV infection and AIDS progression. AIDS Res Hum Retroviruses 2008; 24: 417-421.
101. Kedzierska K, Azzam R, Ellery P, Mak J, Jaworowski A, Crowe SM. Defective phagocytosis by human monocyte/macrophages following HIV-1 infection: underlying mechanisms and modulation by adjunctive cytokine therapy. J Clin Virol 2003; 26: 247-263.
102. Smith PD, Ohura K, Masur H, Lane HC, Fauci AS, Wahl SM. Monocyte function in the acquired immune deficiency syndrome. Defective chemotaxis. J Clin Invest 1984; 74: 2121-2128.
103. Poli G, Bottazzi B, Acero R et al. Monocyte function in intravenous drug abusers with lymphadenopathy syndrome and in patients with acquired immunodeficiency syndrome: selective impairment of chemotaxis. Clin Exp Immunol 1985; 62: 136-142.
104. Wahl SM, Allen JB, Gartner S et al. HIV-1 and its envelope glycoprotein down-regulate chemotactic ligand receptors and chemotactic function of peripheral blood monocytes. J Immunol 1989; 142: 3553-3559.
105. Kedzierska K, Ellery P, Mak J, Lewin SR, Crowe SM, Jaworowski A. HIV-1 down-modulates gamma signaling chain of Fc gamma R in human macrophages: a possible mechanism for inhibition of phagocytosis. J Immunol 2002; 168: 2895-2903.
106. Musher DM, Watson DA, Nickeson D, Gyorkey F, Lahart C, Rossen RD. The effect of HIV infection on phagocytosis and killing of Staphylococcus aureus by human pulmonary alveolar macrophages. Am J Med Sci 1990; 299: 158-163.
107. Weiss L, Haeffner-Cavaillon N, Laude M, Gilquin J, Kazatchkine MD. HIV infection is associated with the spontaneous production of interleukin-1 (IL-1) in vivo and with an abnormal release of IL-1 alpha in vitro. AIDS 1989; 3: 695-699.
108. Emilie D, Peuchmaur M, Maillot MC et al. Production of interleukins in human immunodeficiency virus-1-replicating lymph nodes. J Clin Invest 1990; 86: 148-159.
109. Canque B, Rosenzwajg M, Gey A, Tartour E, Fridman WH, Gluckman JC. Macrophage inflammatory protein-1alpha is induced by human immunodeficiency virus infection of monocyte-derived macrophages. Blood 1996; 87: 2011-2019.
110. Cotter RL, Zheng J, Che M et al. Regulation of human immunodeficiency virus type 1 infection, beta-chemokine production, and CCR5 expression in CD40L-stimulated macrophages: immune control of viral entry. J Virol 2001; 75: 4308-4320.
111. Thieblemont N, Weiss L, Sadeghi HM, Estcourt C, Haeffner-Cavaillon N. CD14lowCD16high: a cytokine-producing monocyte subset which expands during human immunodeficiency virus infection. Eur J Immunol 1995; 25: 3418-3424.
112. Pulliam L, Gascon R, Stubblebine M, McGuire D, McGrath MS. Unique monocyte subset in patients with AIDS dementia. Lancet 1997; 349: 692-695.
113. Chen TP, Roberts RL, Wu KG, Ank BJ, Stiehm ER. Decreased superoxide anion and hydrogen peroxide production by neutrophils and monocytes in human immunodeficiency virus-infected children and adults. Pediatr Res 1993; 34: 544-550.
114. Pittis MG, Prada F, Mangano A et al. Monocyte phagolysosomal fusion in children born to human immunodeficiency virus-infected mothers. Pediatr Infect Dis J 1997; 16: 24-28.
115. Palmer CS, Anzinger JJ, Zhou J et al. Glucose transporter 1-expressing proinflammatory monocytes are elevated in combination antiretroviral therapy-treated and untreated HIV+ subjects. J Immunol 2014; 193: 5595-5603.
116. Cassol E, Cassetta L, Alfano M, Poli G. Macrophage polarization and HIV-1 infection. J Leukoc Biol 2010;87:599-608.
117. Burdo TH, Lentz MR, Autissier P et al. Soluble CD163 made by monocyte/macrophages is a novel marker of HIV activity in early and chronic infection prior to and after anti-retroviral therapy. J Infect Dis 2011; 204: 154-163.
118. Rajasuriar R, Booth D, Solomon A 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.
119. Wallet MA, Rodriguez CA, Yin L et al. Microbial translocation induces persistent macrophage activation unrelated to HIV-1 levels or T-cell activation following therapy. AIDS 2010; 24: 1281-1290.
120. Kamat A, Lyons JL, Misra V et al. Monocyte Activation Markers in Cerebrospinal Fluid Associated With Impaired Neurocognitive Testing in Advanced HIV Infection. J Acquir Immune Defic Syndr 2012; 60: 234-243.
121. Kedzierska K, Mak J, Jaworowski A et al. nef-deleted HIV-1 inhibits phagocytosis by monocyte-derived macrophages in vitro but not by peripheral blood monocytes in vivo. AIDS 2001; 15: 945-955.
122. Bowers NL, Helton ES, Huijbregts RP, Goepfert PA, Heath SL, Hel Z. Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog 2014; 10: e1003993.
123. 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.
124. Cassone A, Chiani P, Quinti I, Torosantucci A. Possible participation of polymorphonuclear cells stimulated by microbial immunomodulators in the dysregulated cytokine patterns of AIDS patients. J Leukoc Biol 1997; 62: 60-66.
125. Schwartz R, Lu Y, Villines D, Sroussi HY. Effect of human immunodeficiency virus infection on S100A8/A9 inhibition of peripheral neutrophils oxidative metabolism. Biomed Pharmacother 2010; 64: 572-575.
126. Flo RW, Naess A, Nilsen A, Harthug S, Solberg CO. A longitudinal study of phagocyte function in HIV-infected patients. AIDS 1994; 8: 771-777.
127. Wenisch C, Parschalk B, Zedwitz-Liebenstein K, Graninger W, Rieger A. Dysregulation of the polymorphonuclear leukocyte-Candida spp. interaction in HIV-positive patients. AIDS 1996; 10: 983-987.
128. Baldelli F, Preziosi R, Francisci D, Tascini C, Bistoni F, Nicoletti I. Programmed granulocyte neutrophil death in patients at different stages of HIV infection. AIDS 2000; 14: 1067-1069.
129. Pitrak DL, Tsai HC, Mullane KM, Sutton SH, Stevens P. Accelerated neutrophil apoptosis in the acquired immunodeficiency syndrome. J Clin Invest 1996; 98: 2714-2719.
130. Salmen S, Teran G, Borges L et al. Increased Fas-mediated apoptosis in polymorphonuclear cells from HIV-infected patients. Clin Exp Immunol 2004; 137: 166-172.
131. Mastroianni CM, d'Ettorre G, Forcina G et al. Interleukin-15 enhances neutrophil functional activity in patients with human immunodeficiency virus infection. Blood 2000;96:1979-1984.
132. Perskvist N, Long M, Stendahl O, Zheng L. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 2002; 168: 6358-6365.
133. Gasperini S, Zambello R, Agostini C et al. Impaired cytokine production by neutrophils isolated from patients with AIDS. AIDS 1998; 12: 373-379.
134. Campillo-Gimenez L, Casulli S, Dudoit Y et al. Neutrophils in antiretroviral therapy-controlled HIV demonstrate hyperactivation associated with a specific IL-17/IL-22 environment. J Allergy Clin Immunol 2014;134:1142-1152 e5.
135. Zietz C, Hotz B, Sturzl M, Rauch E, Penning R, Lohrs U. Aortic endothelium in HIV-1 infection: chronic injury, activation, and increased leukocyte adherence. Am J Pathol 1996; 149: 1887-1898.
136. de Gaetano Donati K, Rabagliati R, Iacoviello L, Cauda R. HIV infection, HAART, and endothelial adhesion molecules: current perspectives. Lancet Infect Dis 2004;4:213-222.
137. Krishnaswamy G, Kelley J, Yerra L, Smith JK, Chi DS. Human endothelium as a source of multifunctional cytokines: molecular regulation and possible role in human disease. J Interferon Cytokine Res 1999; 19: 91-104.
138. Bussolino F, Mitola S, Serini G, Barillari G, Ensoli B. Interactions between endothelial cells and HIV-1. Int J Biochem Cell Biol 2001; 33: 371-390.
139. 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.
140. Graham SM, Rajwans N, Tapia KA et al. A prospective study of endothelial activation biomarkers, including plasma angiopoietin-1 and angiopoietin-2, in Kenyan women initiating antiretroviral therapy. BMC Infect Dis 2013; 13: 263.
141. Graham SM, Rajwans N, Jaoko W et al. Endothelial activation biomarkers increase after HIV-1 acquisition: plasma vascular cell adhesion molecule-1 predicts disease progression. AIDS 2013; 27: 1803-1813.
142. Arildsen H, Sorensen KE, Ingerslev JM, Ostergaard LJ, Laursen AL. Endothelial dysfunction, increased inflammation, and activated coagulation in HIV-infected patients improve after initiation of highly active antiretroviral therapy. HIV Med 2013; 14: 1-9.
143. Beltran LM, Munoz Hernandez R, de Pablo Bernal RS et al. Reduced sTWEAK and increased sCD163 levels in HIV-infected patients: modulation by antiretroviral treatment, HIV replication and HCV co-infection. PLoS ONE 2014; 9: e90541.
144. de Larranaga 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.
145. Chi D, Henry J, Kelley J, Thorpe R, Smith JK, Krishnaswamy G. The effects of HIV infection on endothelial function. Endothelium 2000; 7: 223-242.
146. Seigneur M, Constans J, Blann A et al. Soluble adhesion molecules and endothelial cell damage in HIV infected patients. Thromb Haemost 1997; 77: 646-649.
147. Nordoy I, Aukrust P, Muller F, Froland SS. Abnormal levels of circulating adhesion molecules in HIV-1 infection with characteristic alterations in opportunistic infections. Clin Immunol Immunopathol 1996; 81: 16-21.
148. Ross AC, Rizk N, O'Riordan MA et al. Relationship between inflammatory markers, endothelial activation markers, and carotid intima-media thickness in HIV-infected patients receiving antiretroviral therapy. Clin Infect Dis 2009; 49: 1119-1127.
149. 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.
150. Aukrust P, Bjornsen S, Lunden B et al. Persistently elevated levels of von Willebrand factor antigen in HIV infection. Downregulation during highly active antiretroviral therapy. Thromb Haemost 2000; 84: 183-187.
151. Kristoffersen US, Kofoed K, Kronborg G, Giger AK, Kjaer A, Lebech AM. Reduction in circulating markers of endothelial dysfunction in HIV-infected patients during antiretroviral therapy. HIV Med 2009; 10: 79-87.
152. Francisci D, Giannini S, Baldelli F et al. HIV type 1 infection, and not short-term HAART, induces endothelial dysfunction. AIDS 2009; 23: 589-596.
153. Ronsholt FF, Ullum H, Katzenstein TL, Gerstoft J, Ostrowski SR. Persistent inflammation and endothelial activation in HIV-1 infected patients after 12 years of antiretroviral therapy. PLoS ONE 2013; 8: e65182.
154. Shi B, De Girolami U, He J et al. Apoptosis induced by HIV-1 infection of the central nervous system. J Clin Invest 1996; 98: 1979-1990.
155. Laurence J, Mitra D, Steiner M, Staiano-Coico L, Jaffe E. Plasma from patients with idiopathic and human immunodeficiency virus-associated thrombotic thrombocytopenic purpura induces apoptosis in microvascular endothelial cells. Blood 1996; 87: 3245-3254.
156. Baker JV, Brummel-Ziedins K, Neuhaus J et al. HIV replication alters the composition of extrinsic pathway coagulation factors and increases thrombin generation. J Am Heart Assoc 2013; 2: e000264.
157. 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.
158. Kuller LH, Tracy R, Belloso W et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 2008; 5: e203.
159. Rodger AJ, Fox Z, Lundgren JD 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.
160. Neuhaus J, Jacobs DR Jr, Baker JV et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J Infect Dis 2010; 201: 1788-1795.
161. Baker JV, Huppler Hullsiek K, Bradford RL, Prosser R, Tracy RP, Key NS. Circulating levels of tissue factor microparticle procoagulant activity are reduced with antiretroviral therapy and are associated with persistent inflammation and coagulation activation among HIV-positive patients. J Acquir Immune Defic Syndr 2013;63:367-371.
162. 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.
163. Hileman CO, Longenecker CT, Carman TL et al. Elevated D-dimer is independently associated with endothelial dysfunction: a cross-sectional study in HIV-infected adults on antiretroviral therapy. Antivir Ther 2012; 17: 1345-1349.
164. Baker J, Quick H, Hullsiek KH et al. Interleukin-6 and d-dimer levels are associated with vascular dysfunction in patients with untreated HIV infection. HIV Med 2010; 11: 608-609.
165. Musselwhite LW, Sheikh V, Norton TD et al. Markers of endothelial dysfunction, coagulation and tissue fibrosis independently predict venous thromboembolism in HIV. AIDS 2011; 25: 787-795.
166. Funderburg NT, Zidar DA, Shive C et al. Shared monocyte subset phenotypes in HIV-1 infection and in uninfected subjects with acute coronary syndrome. Blood 2012;120:4599-4608.
167. 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.
168. Madden E, Lee G, Kotler DP et al. Association of antiretroviral therapy with fibrinogen levels in HIV-infection. AIDS 2008; 22: 707-715.
169. Pretorius E, Oberholzer HM, Smit E, Steyn E, Briedenhann S, Franz CR. Ultrastructural changes in platelet aggregates of HIV patients: a scanning electron microscopy study. Ultrastruct Pathol 2008; 32: 75-79.
170. Karpatkin S, Nardi M, Green D. Platelet and coagulation defects associated with HIV-1-infection. Thromb Haemost 2002; 88: 389-401.
171. Holme PA, Muller F, Solum NO, Brosstad F, Froland 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.
172. Corrales-Medina VF, Simkins J, Chirinos JA et al. Increased levels of platelet microparticles in HIV-infected patients with good response to highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2010; 54: 217-218.
173. Ahmad R, Iannello A, Samarani S et al. Contribution of platelet activation to plasma IL-18 concentrations in HIV-infected AIDS patients. AIDS 2006; 20: 1907-1909.
174. Baker JV, Neuhaus J, Duprez D et al. Changes in inflammatory and coagulation biomarkers: a randomized comparison of immediate versus deferred antiretroviral therapy in patients with HIV infection. J Acquir Immune Defic Syndr 2011; 56: 36-43.
175. Singh MV, Davidson DC, Kiebala M, Maggirwar SB. Detection of circulating platelet-monocyte complexes in persons infected with human immunodeficiency virus type-1. J Virol Methods 2012; 181: 170-176.
176. Landro L, Ueland T, Otterdal K, Froland SS, Aukrust P. Persistently raised plasma levels of platelet-derived inflammatory mediators in HIV-infected patients during highly active anti-retroviral therapy. J Thromb Haemost 2011; 9: 1075-1077.
177. Satchell CS, Cotter AG, O'Connor EF et al. Platelet function and HIV: a case-control study. AIDS 2010; 24: 649-657.
178. Haugaard AK, Lund TT, Birch C et al. Discrepant coagulation profile in HIV infection: elevated D-dimer but impaired platelet aggregation and clot initiation. AIDS 2013; 27: 2749-2758.
179. Breen EC, Rezai AR, Nakajima K et al. Infection with HIV is associated with elevated IL-6 levels and production. J Immunol 1990; 144: 480-484.
180. Corasaniti MT, Bellizzi C, Russo R, Colica C, Amantea D, Di Renzo G. Caspase-1 inhibitors abolish deleterious enhancement of COX-2 expression induced by HIV-1 gp120 in human neuroblastoma cells. Toxicol Lett 2003; 139: 213-219.
181. Ilyin SE, Plata-Salaman CR. HIV-1 envelope glycoprotein 120 regulates brain IL-1beta system and TNF-alpha mRNAs in vivo. Brain Res Bull 1997; 44: 67-73.
182. Poli G, Kinter AL, Fauci AS. Interleukin 1 induces expression of the human immunodeficiency virus alone and in synergy with interleukin 6 in chronically infected U1 cells: inhibition of inductive effects by the interleukin 1 receptor antagonist. Proc Natl Acad Sci USA 1994; 91: 108-112.
183. Roux-Lombard P, Modoux C, Cruchaud A, Dayer JM. Purified blood monocytes from HIV 1-infected patients produce high levels of TNF alpha and IL-1. Clin Immunol Immunopathol 1989; 50: 374-384.
184. Lathey JL, Kanangat S, Rouse BT. Differential expression of tumor necrosis factor alpha and interleukin 1 beta compared with interleukin 6 in monocytes from human immunodeficiency virus-positive individuals measured by polymerase chain reaction. J Acquir Immune Defic Syndr 1994; 7: 109-115.
185. Berman MA, Sandborg CI, Calabia BS, Andrews BS, Friou GJ. Interleukin 1 inhibitor masks high interleukin 1 production in acquired immunodeficiency syndrome (AIDS). Clin Immunol Immunopathol 1987; 42: 133-140.
186. Clouse KA, Cosentino LM, Weih KA et al. The HIV-1 gp120 envelope protein has the intrinsic capacity to stimulate monokine secretion. J Immunol 1991; 147: 2892-2901.
187. Lore K, Sonnerborg A, Olsson J et al. HIV-1 exposed dendritic cells show increased pro-inflammatory cytokine production but reduced IL-1ra following lipopolysaccharide stimulation. AIDS 1999; 13: 2013-2021.
188. Corasaniti MT, Turano P, Bilotta A et al. Evidence that increases of mitochondrial immunoreactive IL-1beta by HIV-1 gp120 implicate in situ cleavage of pro-IL-1beta in the neocortex of rat. J Neurochem 2001; 78: 611-618.
189. Ullum H, Victor J, Katzenstein TL et al. Decreased short-term production of tumor necrosis factor-alpha and interleukin-1beta in human immunodeficiency virus-seropositive subjects. J Infect Dis 1997; 175: 1507-1510.
190. Bergamini A, Bolacchi F, Bongiovanni B et al. Human immunodeficiency virus type 1 infection modulates the interleukin (IL)-1beta and IL-6 responses of human macrophages to CD40 ligand stimulation. J Infect Dis 2000; 182: 776-784.
191. Baqui AA, Jabra-Rizk MA, Kelley JI, Zhang M, Falkler WA Jr, Meiller TF. Enhanced interleukin-1beta, interleukin-6 and tumor necrosis factor-alpha production by LPS stimulated human monocytes isolated from HIV+ patients. Immunopharmacol Immunotoxicol 2000; 22: 401-421.
192. Brazille P, Dereuddre-Bosquet N, Leport C et al. Decreases in plasma TNF-alpha level and IFN-gamma mRNA level in peripheral blood mononuclear cells (PBMC) and an increase in IL-2 mRNA level in PBMC are associated with effective highly active antiretroviral therapy in HIV-infected patients. Clin Exp Immunol 2003; 131: 304-311.
193. Aukrust P, Muller F, Lien E et al. Tumor necrosis factor (TNF) system levels in human immunodeficiency virus-infected patients during highly active antiretroviral therapy: persistent TNF activation is associated with virologic and immunologic treatment failure. J Infect Dis 1999; 179: 74-82.
194. 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.
195. Biswas P, Cozzi-Lepri A, Delfanti F et al. Significant link between sCD30 changes and HIV viremia in patients treated with HAART. J Med Virol 2006; 78: 1513-1519.
196. Calmy A, Gayet-Ageron A, Montecucco F et al. HIV increases markers of cardiovascular risk: results from a randomized, treatment interruption trial. AIDS 2009; 23: 929-939.
197. Giron-Gonzalez JA, Lopez-Sanchez A, Elvira J, Perez E, Fernandez-Gutierrez C. Effect of patient adherence to antiretroviral therapy on CD4+ cell count, HIV-1 RNA, and serum concentrations of tumor necrosis factor and its soluble receptors. Eur J Clin Microbiol Infect Dis 2000; 19: 852-858.
198. Aukrust P, Liabakk NB, Muller F, Lien E, Espevik T, Froland SS. Serum levels of tumor necrosis factor-alpha (TNF alpha) and soluble TNF receptors in human immunodeficiency virus type 1 infection-correlations to clinical, immunologic, and virologic parameters. J Infect Dis 1994; 169: 420-424.
199. Thea DM, Porat R, Nagimbi K et al. Plasma cytokines, cytokine antagonists, and disease progression in African women infected with HIV-1. Ann Intern Med 1996; 124: 757-762.
200. Zangerle R, Gallati H, Sarcletti M et al. Increased serum concentrations of soluble tumor necrosis factor receptors in HIV-infected individuals are associated with immune activation. J Acquir Immune Defic Syndr 1994; 7: 79-85.
201. Kalayjian RC, Machekano RN, Rizk N et al. Pretreatment levels of soluble cellular receptors and interleukin-6 are associated with HIV disease progression in subjects treated with highly active antiretroviral therapy. J Infect Dis 2010; 201: 1796-1805.
202. Fahey JL, Taylor JM, Manna B et al. Prognostic significance of plasma markers of immune activation, HIV viral load and CD4 T-cell measurements. AIDS 1998; 12: 1581-1590.
203. Mildvan D, Spritzler J, Grossberg SE et al. Serum neopterin, an immune activation marker, independently predicts disease progression in advanced HIV-1 infection. Clin Infect Dis 2005; 40: 853-858.
204. Zangerle R, Steinhuber S, Sarcletti M et al. Serum HIV-1 RNA levels compared to soluble markers of immune activation to predict disease progression in HIV-1-infected individuals. Int Arch Allergy Immunol 1998; 116: 228-239.
205. Hober D, Benyoucef S, Delannoy AS et al. Plasma levels of sTNFR p75 and IL-8 in patients with HIV-1 infection. Immunol Lett 1996; 52: 57-60.
206. Godfried MH, van der Poll T, Weverling GJ et al. Soluble receptors for tumor necrosis factor as predictors of progression to AIDS in asymptomatic human immunodeficiency virus type 1 infection. J Infect Dis 1994; 169: 739-745.
207. French MA, King MS, Tschampa JM, da Silva BA, Landay AL. Serum immune activation markers are persistently increased in patients with HIV infection after 6 years of antiretroviral therapy despite suppression of viral replication and reconstitution of CD4+ T cells. J Infect Dis 2009; 200: 1212-1215.
208. Neaton JD, Neuhaus J, Emery S. Soluble biomarkers and morbidity and mortality among people infected with HIV: summary of published reports from 1997 to 2010. Curr Opin HIV AIDS 2010; 5: 480-490.
209. Lau B, Sharrett AR, Kingsley LA et al. C-reactive protein is a marker for human immunodeficiency virus disease progression. Arch Intern Med 2006; 166: 64-70.
210. Guimaraes MM, Greco DB, Figueiredo SM, Foscolo RB, Oliveira AR Jr, Machado LJ. High-sensitivity C-reactive protein levels in HIV-infected patients treated or not with antiretroviral drugs and their correlation with factors related to cardiovascular risk and HIV infection. Atherosclerosis 2008; 201: 434-439.
211. van Vonderen MG, Hassink EA, van Agtmael MA et al. Increase in carotid artery intima-media thickness and arterial stiffness but improvement in several markers of endothelial function after initiation of antiretroviral therapy. J Infect Dis 2009; 199: 1186-1194.
212. Funderburg N, Kalinowska M, Eason J et al. Effects of maraviroc and efavirenz on markers of immune activation and inflammation and associations with CD4+ cell rises in HIV-infected patients. PLoS ONE 2010;5:e13188.
213. Shikuma CM, Ribaudo HJ, Zheng Y et al. Change in high-sensitivity c-reactive protein levels following initiation of efavirenz-based antiretroviral regimens in HIV-infected individuals. AIDS Res Hum Retroviruses 2011; 27: 461-468.
214. Hosaka N, Oyaizu N, Kaplan MH, Yagita H, Pahwa S. Membrane and soluble forms of Fas (CD95) and Fas ligand in peripheral blood mononuclear cells and in plasma from human immunodeficiency virus-infected persons. J Infect Dis 1998; 178: 1030-1039.