Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression

AIDS

Volumn 24, Issue 6, 2010, Pages 819-831

  Roberts, Lindi ^a   Passmore, Jo Ann S ^a,b   Williamson, Carolyn ^a,c   Little, Francesca ^a   Bebell, Lisa M ^c,d   Mlisana, Koleka ^c   Burgers, Wendy A ^a   Van Loggerenberg, Francois ^c   Walzl, Gerhard ^e   Djoba Siawaya, Joel F ^e   Abdool Karim, Quarraisha ^c,d   Abdool Karim, Salim S ^c,d  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Acute infection; Cytokines; Disease progression; HIV 1; Viral load

Indexed keywords

EOTAXIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 7;

ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; CLINICAL ARTICLE; DISEASE COURSE; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SEXUALLY TRANSMITTED DISEASE; VIRUS LOAD;

ADULT; BIOLOGICAL MARKERS; CD4 LYMPHOCYTE COUNT; CYTOKINES; DISEASE PROGRESSION; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; PREDICTIVE VALUE OF TESTS; RECEPTORS, CYTOKINE; YOUNG ADULT;

EID: 77949565615     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e3283367836     Document Type: Article

References (62)

1. Deeks SG, Kitchen CMR, Liu L, Guo H, Gascon R, Narvaez AB, et al. Immune activation set point during early HIV infection predicts subsequent CD4R T-cell changes independent of viral load. Blood 2004; 104:942-947.
2. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, et al. CD4R T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200:749-759.
3. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C, et al. Primary HIV-1 infection is associated with preferential depletion of CD4R T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004; 200:761-770.
4. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, Heitman J, et al. Induction of a striking systemic cytokine cascade prior to peak viraemia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 2009; 83:3719-3733.
5. Hazenberg MD, Otto SA, van Benthem BHB, Roos MTL, Cou-tinho RA, Lange JMA, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17:1881-1888.
6. 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.
7. Alter G, Malenfant JM, Delabre RM, Burgett NC, Yu XG, Lichterfeld M, et al. Increased natural killer cell activity in viremic HIV-1 infection. J Immunol 2004; 173:5305-5311.
8. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12:1365-1371.
9. Catalfamo M, Mascio MD, Hu Z, Srinivasula S, Thaker V, Adelsberger J, et al. HIV infection-associated immune activation occurs by two distinct pathways that differentially affect CD4 and CD8 T cells. Proc Natl Acad Sci USA 2008; 105:19851-19856.
10. Norris PJ, Pappalardo BL, Custer B, Spotts G, Hecht FM, Busch MP. Elevations in IL-10, TNF-a and IFN-g from the earliest point of HIV type 1 infection. AIDS Res Hum Retroviruses 2006; 22:757-762.
11. Bebell LM, Passmore JA, Williamson C, Mlisana K, Iriogbe I, van Loggerenberg F, et al. Relationship between levels of inflammatory cytokines in the genital tract and CD4R cell counts in women with acute HIV-1 infection. J Infect Dis 2008; 198:710-714.
12. Osborne L, Kunkel S, Nabel GJ. Tumor necrosis factor-alpha and interleukin-1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc Natl Acad Sci USA 1989; 86:2336-2340.
13. Lin RH, Hwang YW, Yang BC, Lin CS. TNF receptor-2-triggered apoptosis is associated with the down-regulation of BclxL on activated T cells and can be prevented by CD28 costimulation. J Immunol 1997; 158:598-603.
14. Swingler S, Mann A, Jacque JM, Brichacek B, Sasseville VG, Williams K, et al. HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat Med 1999; 5:997-1003.
15. Mascola JR, Nabel GJ. Vaccines for the prevention of HIV-1 disease. Curr Opinion Immunol 2001; 13:489-495.
16. Goujard C, Bonarek M, Meyer L, BonnetF, Chaix ML, Deveau C, et al. CD4 cell count and HIV DNA level are independent predictors of disease progression after primary HIV type 1 infectioninuntreated patients. Clin Infect Dis 2006;42:709-715.
17. Mellors JW, Munoz A, Giorgi JV, Margolick JB, Tassoni CJ, Gupta P, et al. Plasma viral load and CD4R lymphocytes as prognostic markers of HIV-1 infection. Ann Intern Med 1997; 126:946-954.
18. de Wolf F, Spijkerman I, Schellekens PT, Langendam M, Kuiken C, Bakker M, etal. AIDS prognosis basedonHIV-1 RNA, CD4R T-cell count and function: markers with reciprocal predictive value over time after seroconversion. AIDS 1997; 11:1799-1806.
19. Lepri AC, Katzenstein TL, Ullum H, Phillips AN, Skinhøj P, Gerstoft J, et al. The relative prognostic value of plasma HIV RNA levels and CD4 lymphocyte counts in advanced HIV infection. AIDS 1998; 12:1639-1643.
20. Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, Giorgi JV. Elevated CD38 antigen expression on CD8R T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4R cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J Acquir Immune Defic Syndr 1997; 16:83-92.
21. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, 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.
22. Fahey JL, Taylor JMG, Manna B, Nishanian P, Aziz N, Giorgi JV, et al. Prognostic significance of plasma markers of immune activation, HIV viral load and CD4 T-cell measurements. AIDS 1998; 12:1581-1590.
23. Zangerle R, Steinhuber S, Sarcletti M, Dierich MP, Wachter H, Fuchs D, 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.
24. van Loggerenberg F, Mlisana K, Williamson C, Auld SC, Morris L, Gray CM, et al. Establishing a cohort at high risk of HIV infection in South Africa: challenges and experiences of the CAPRISA 002 acute infection study. PLoS ONE 2008; 3:e1954.
25. Siawaya JF, Roberts T, Babb C, Black G, Golakai HJ, Stanley K, et al. An evaluation of commercial fluorescent bead-based luminex cytokine assays. PLoS ONE 2008; 3:e2535.
26. Columb MO, Sagadai S. Multiple comparisons. Curr Anaesth Crit Care 2006; 17:233-236.
27. Lee JS, Dixon DO, Kantarjian HM, Keating MJ, Talpaz M. Prognosis of chronic lymphocytic leukaemia: a multivariate regression analysisof325 untreated patients.Blood 1987;69:929-936.
28. Meier A, Alter G, Frahm N, Sidhu H, Li B, Bagchi A, et al. MyD88-dependent immune activation mediated by human immunodeficiency virus type 1-encoded Toll-like receptor ligands. J Virol 2007; 81:8180-8191.
29. Centlivre M, Sala M, Wain-Hobson S, Berkhout B. In HIV-1 pathogenesis the die is cast during primary infection. AIDS 2007; 21:1-11.
30. Kubin M, Kamoun M, Trinchieri G. Interleukin 12 synergizes with B7/CD28 interaction in inducing efficient proliferation and cytokine production of human T cells. J Exp Med 1994; 180:211-222.
31. Flesch IE, Hess JH, Huang S, Aguet M, Rothe J, Bluethmann H, et al. Early interleukin 12 production by macrophages in response to mycobacterial infection depends on interferon g and tumor necrosis factor a. J Exp Med 1995; 181:1615-1621.
32. Gazzinelli RT, Hieny S, Wynn TA, Wolf S, Sher A. Interleukin-12is required for the T-lymphocyte independent induction of inter-feron-g by an intracellular parasite and induces resistance in T-deficient hosts. Proc Natl Acad Sci USA 1993; 90:6115-6119.
33. Tripp CS, Wolf SF, Unanue ER. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc Natl Acad Sci USA 1993; 90:3725-3729.
34. Manetti R, Gerosa F, Giudizi MG, Biagiotti R, Parronchi P, Piccinni M, et al. Interleukin 12 induces stable priming for interferon-g (IFN-g) production during differentiation of human T helper (Th) cells and transient IFN-g production in established Th2 cell clones. J Exp Med 1994; 179:1273-1283.
35. Manetti R, Parronchi P, Giudizi MG, Piccinni MP, Maggi E, Trinchieri G, et al. Natural killer cell stimulator-y factor (NKSF/ IL-12) induces Thl-type specific immune responses and inhibits the development of IL-4 producing Th cells. J Exp Med 1993; 177:1199-1204.
36. Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-g. Annu Rev Immunol 1997; 15:749-795.
37. Ullum H, Lerri AC, Bendtzen K, Victor J, Gùtzsche PC, Philips AN, et al. Low production of interferon-g is related to disease progression in HIV infection: evidence from a cohort of 347 HIV-infected individuals. AIDS Res Hum Retrovir 1997; 13:1039-1046.
38. Bailer RT, Holloway A, Sun J, Margolick JB, Martin M, Kostman J, et al. IL-13 and IFN-g secretion by activated T cells in HIV-1 infection associated with viral suppression and a lack of disease progression. J Immunol 1999; 162:7534-7542.
39. Ansari AA, Mayne AE, Sundstrom JB, Bostik P, Grimm B, Altman JD, et al. Administration of recombinant rhesus interleukin-12 during acute simian immunodeficiency virus (SIV) infection leads to decreased viral loads associated with prolonged survival in SIVmac251-infected rhesus macaques. J Virol 2002; 76:1731-2174.
40. Nathan CF, Murray HW, Wiebe ME, Rubin BY. Identification of interferon-g as the lymphokine that activates human macro-phage oxidative metabolism and antimicrobial activity. J Exp Med 1983; 158:670-689.
41. Metcalf D. The molecular biology and functions of the gran-ulocyte-macrophage colony-stimulating factors. Blood 1986; 67:257-267.
42. Jana M, Dasgupta S, Saha RN, Liu X, Pahan K. Induction of tumor necrosis factor-alpha (TNF-alpha) by interleukin-12 p40 monomer and homodimer in microglia and macrophages. J Neurochem 2003; 86:519-528.
43. Cooper AM, Khader SA. IL-12p40: an inherently agonistic cytokine. Trends Immunol 2007; 28:33-38.
44. Miossec P, Yu CL. Lymphocyte chemotactic activity of human interleukin 1. J Immunol 1984; 133:2007-2011.
45. Gerber BO, Zanni MP, Uguccioni M, Loetscher M, Mackay CR, Pichler WJ, et al. Functional expression of the eotaxin receptor CCR3 in T lymphocytes co-localizing with eosinophils. Curr Biol 1997; 7:836-843.
46. Niu J, Li Z, Peng B, Chiao PJ. Identification of an auto-regulatory feedback pathway involving IL-1a in induction of constitutive NF-kB activation in pancreatic cancer cells. J Biol Chem 2004; 279:16452-16462.
47. Fry TJ, Mackall CL. The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J Immunol 2005; 174:6571-6576.
48. Picker LJ, Reed-Inderbitzin EF, Hagen SI, Edgar JB, Hansen SG, Legasse A, et al. IL-15 induces CD4R effector memory T cell production and tissue emigration in nonhuman primates. J Clin Invest 2006; 116:1514-1524.
49. Okoye A, Meier-Schellersheim M, Brenchley JM, Hagen SI, Walker JM, Rohankhedkar M, et al. Progressive CD4R central-memory T cell decline results in CD4R effector-memory insufficiency and overt disease in chronic SIV infection. J Exp Med 2007; 204:2171-2185.
50. Napolitano LA, Grant RM, Deeks SG, Schmidt D, De Rosa SC, Herzenberg LA, et al. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: implications for T-cell homeostasis. Nat Med 2001; 7:73-79.
51. Geginat J, Sallusto F, Lanzavecchia A. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(R) T cells. J Exp Med 2001; 194: 1711-1719.
52. Eberly MD, Kader M, Hassan W, Rogers KA, Zhou J, Mueller YM, et al. Increased IL-15 production is associated with higher susceptibility of memory CD4 T cells to simian immunodeficiency virus during acute infection. J Immunol 2009; 182:1439-1448.
53. Burgers WA, Riou C, Mlotshwa M,de Assis Rosa D, Maenetje P, Brenchley JM, et al. Association of HIV-specific and total CD8R T memory phenotypes in subtype C HIV-1 infection with viral set point. J Immunol 2009; 182:4751-4761.
54. Kacani L, Sprinzl GM, Erdei A, Dierich MP. Interleukin-15 enhances HIV-1-driven polyclonal B-cell response in vitro. Exp Clin Immunogenet 1999; 16:162-172.
55. Levesque MC, Moody MA, Hwang KK, Marshall DJ, Whitesides JF, Amos JD, et al. Polyclonal B cell differentiation and loss of gastrointestinal tract germinal centers in the earliest stages of HIV-1 infection. PLOS Med 2009; 6:e1000107.
56. Akridge RE, Oyafuso LK, Reed SG. IL-10 is induced during HIV-1 infection and is capable of decreasing viral replication in human macrophages. J Immunol 1994; 153:5782-5789.
57. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, Oldstone MB. Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 2006; 12:1301-1309.
58. Ejrnaes M, Filippi CM, Martinic MM, Ling EM, Togher LM, Crotty S, et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J Exp Med 2006; 203:2461-2472.
59. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon-g-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 1993; 178:1041-1048.
60. Stylianou E, Aukrust P, Kvale D, Muller F, Froland SS. IL-10 in HIV infection: increasing serum IL-10 levels with disease progression-down- regulatory effect of potent antiretroviral therapy. Clin Exp Immunol 1999; 116:115-120.
61. Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection. J Immunol 2008; 180:5771-5777.
62. Estes JD, Li Q, Reynolds MR, Wietgrefe S, Duan L, Schacker T, et al. Premature induction of immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J Infect Dis 2006; 193:703-712.