Resumption of HIV replication is associated with monocyte/macrophage derived cytokine and chemokine changes: Results from a large international clinical trial

AIDS

Volumn 25, Issue 9, 2011, Pages 1207-1217

  Cozzi Lepri, Alessandro ^a,b   French, Martyn A ^c,d   Baxter, John ^e   Okhuysen, Pablo ^f   Plana, Montserrat ^g   Neuhaus, Jacqueline ^b   Landay, Alan ^h  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d ROYAL PERTH HOSPITAL   (Australia)

^e UMDNJ Robert Wood Johnson Medical School at Camden   (United States)

^f UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF BARCELONA   (Spain)

^h RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

antiretroviral therapy; chemokines; clinical trial; cytokines; interruption

Indexed keywords

CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CLINICAL TRIAL (TOPIC); ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MONOCYTE; PRIORITY JOURNAL; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION;

EID: 85027941566     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e3283471f10     Document Type: Article

References (56)

1. Giorgi JV, Lyles RH, Matud JL, Yamashita TE, Mellors JW, Hultin LE, et al., Multicenter AIDS Cohort Study. Predictive value of immunologic and virologic markers after long or short duration of HIV-1 infection. J Acquir Immune Defic Syndr 2002; 29:346-355. (Pubitemid 34288887)
2. 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 Hum Retrovirol 1997; 16:83-92.
3. Bü rgisser P, Hammann C, Kaufmann D, Battegay M, Rutschmann OT. Expression of CD28 and CD38 by CD8R T lymphocytes in HIV-1 infection correlates with markers of disease severity and changes towards normalization under treatment. The Swiss HIV Cohort Study. Clin Exp Immunol 1999; 115:458-463. (Pubitemid 29130360)
4. Froebel KS, Raab GM, D'Alessandro C. A single measurement of CD38CD8 cells in HIVR, long-term surviving injecting drug users distinguishes those who will progress to AIDS from those who will remain stable. Clin Exp Immunol 2000; 122:72-78.
5. Giorgi JV, Liu Z, Hultin LE, Cumberland WG, Hennessey K, Detels R. Elevated levels of CD38R CD8R T cells in HIV infection add to the prognostic value of low CD4R 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. (Pubitemid 23207458)
6. Bofill M, Mocroft A, Lipman M, Medina E, Borthwick NJ, Sabin CA, et al. Increased numbers of primed activated CD8RCD38R CD45RORT cells predict the decline of CD4RT cells in HIV-1- infected patients. AIDS 1996; 10:827-834.
7. Wilson CM, Ellenberg JH, Douglas SD, Moscicki AB, Holland CA, Reach Project Of The Adolescent Medicine HIV/AIDS Research Network. CD8RCD38R T cells but not HIV type 1 RNA viral load predict CD4R T cell loss in a predominantly minority female HIVR adolescent population. AIDS Res Hum Retroviruses 2004; 20:263-269. (Pubitemid 38429397)
8. Hazenberg MD, Otto SA, Van Benthem BH, Roos MT, Coutinho RA, Lange JM, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17:1881-1888. (Pubitemid 37070273)
9. Fahey JL, Taylor JM, Detels R, Hofmann B, Melmed R, Nishanian P, Giorgi JV. The prognostic value of cellular and serologic markers in infection with human immunodeficiency virus type 1. N Engl J Med 1990; 322:166-172. (Pubitemid 20036390)
10. Mildvan D, Spritzler J, Grossberg SE, Fahey JL, Johnston DM, Schock BR, Kagan J. Serum neopterin, an immune activation marker, independently predicts disease progression in advanced HIV-1 infection. Clin Infect Dis 2005; 40:853-858. (Pubitemid 40365506)
11. Bedini JL, Garća F, Miró JM, Aznar E, Serrano J, Lozano L, et al. Serum levels of beta2-microglobulin, neopterin, TNF-alpha and soluble receptors of TNF-alpha and interleukin-2 in intravenous drug abusers according to HIV-1 status and stage of the HIV-1 infection. Clin Microbiol Infect 1998; 4:4-10. (Pubitemid 28059756)
12. Mart́nez-Brú C, Cortés M, Planella T, Barrio J, Cadafalch J, Domingo P, et al. Beta 2-microglobulin and immunoglobulins are more useful markers of disease progression in HIV than neopterin and adenosine deaminase. Ann Clin Biochem 1999; 36 (Pt 5):601-608. (Pubitemid 29410712)
13. Hunt PW, Martin JN, Sinclair E, Bredt B, Hagos E, Lampiris H, Deeks SG. T cell activation is associated with lower CD4R T cell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy. J Infect Dis 2003; 187:1534-1543. (Pubitemid 36578959)
14. 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 CD4R T cells. 1. J Infect Dis 2009; 200:1212-1215.
15. Valdez H, Connick E, Smith KY, Lederman MM, Bosch RJ, Kim RS. Limited immune restoration after 3 years' suppression of HIV-1 replication in patients with moderately advanced disease. AIDS 2002; 16:1859-1866.
16. Philips AN, Carr A, Neuhaus J, Visnegarwala F, Prineas R, Burman WJ, et al. Interruption of antiretroviral therapy and risk of cardiovascular disease in persons with HIV-1 infection: exploratory analyses from the SMART trial. Antivir Ther 2008; 13:177-187. (Pubitemid 351535369)
17. Rodger AJ, Fox Z, Lundgren JD, Kuller LH, Boesecke C, Gey D, et al., INSIGHT Strategies for Management of Antiretroviral Therapy (SMART) Study Group. 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.
18. El-Sadr WM, Lundgren JD, Neaton JD, Gordin F, Abrams D, Arduino RC, et al., Strategies for Management of Antiretroviral Therapy (SMART) Study Group. CD4R count-guided interruption of antiretroviral treatment. N Engl J Med 2006; 355:2283-2296. (Pubitemid 44837777)
19. Kuller LH, Tracy R, Belloso W, De Wit S, Drummond F, Lane HC, et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 2008; 5:1496-1498.
20. Sandler NG, Wand H, Roque A, Law M, Nason MC, Nixon DE, et al., for the INSIGHT SMART Study Group. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 2011; 203:780-790.
21. Marchetti G, Cozzi-Lepri A, Bellistr̀ GM, Merlini E, Chiodera A, Soscia F, et al. for the Icona Foundation Study Group. Role of microbial translocation and immune hyperactivation in disease progression of HIVR patients with preserved CD4 count in the absence of ART [abstract 333]. In: 17th Conference on Retroviruses and Opportunistic Infections; 16-19 February 2010; San Francisco, California.
22. Mocroft A, Wyatt C, Szczech L, Neuhaus J, El-Sadr W, Tracy R, et al. Interruption of antiretroviral therapy is associated with increased plasma cystatin C. AIDS 2009; 23:71-82.
23. Lars P, Jacquie N, Amanda M, Vincent S, Juergen R, Greg D, et al. for the INSIGHT SMART Study Group. Interruption of ART and changes in hyaluronic acid as marker of liver fibrosis progression in strategies for management of ART viral hepatitis- co-infected participants and matched controls. Antivir Ther (in press).
24. Zhu J, Paul WE. Heterogeneity and plasticity of T helper cells. Cell Res 2010; 20:4-12.
25. Fantuzzi L, Belardelli F, Gessani S. Monocyte/macrophagederived CC chemokines and their modulation by HIV-1 and cytokines: a complex network of interactions influencing viral replicagtion and AIDS pathogenesis. J Leukoc Biol 2003; 74:719-725. (Pubitemid 38040348)
26. de Jager W, Rijkers GT. Solid-phase and bead-based cytokine immunoassay: a comparison. Methods 2006; 38:294-303.
27. Elshal MF, McCoy JP. Multiplex bead array assays: performance evaluation and comparison of sensitivity to ELISA. Methods 2006; 38:317-323.
28. Jenmalm MC, Malit M, Torrence J, Zhang A. Bio-plex cytokine immunoassays and ELISA: comparison of two methodologies in testing samples from asthmatic and healthy children. Cytokine assays, techinal note 305. Hercules, California: Bio-Rad Inc. http://www.biocompare.com/Articles/ApplicationNote/1156/Bio-Plex- Cytokine-Immunoassays-And-ELISA-Comparison-Of-Two-Methodologies-In-Testing- Samples-From-Asthmatic-And-Healthy-Children-Rev-A.html. [Accessed March 2011].
29. Marschner IC, Betensky RA, DeGruttola V, Hammer SM, Kuritzkes DR. Clinical trials using HIV-1 RNA-based primary endpoints: statistical analysis and potential biases. J Acquir Immune Defic Syndr Hum Retrovirol 1999; 20:220-227. (Pubitemid 29156958)
30. Hsu H, Xiong J, Goeddel DV. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 1995; 81:495-504.
31. Carpentier I, Coornaert B, Beyaert R. Function and regulation of tumor necrosis factor type 2. Curr Med Chem 2004; 11:2205-2212. (Pubitemid 38967740)
32. Aggarwal S, Gollapudi S, Gupta S. Increased TNF-alpha-induced apoptosis in lymphocytes from aged humans: changes in TNF-alpha receptor expression and activation of caspases. J Immunol 1999; 162:2154-2161. (Pubitemid 29288837)
33. Taylor JA, Cummins NW, Bren GD, Rizza SA, Kolbert CP, Behrens MD, et al. Casp8p41 expression in primary T cells induces a proinflammatory response. AIDS 2010; 24:1251-1258.
34. Haas DW, Geraghty DE, Andersen J, Mar J, Motsinger AA, D'Aquila RT, et al. Immunogenetics of CD4 lymphocyte count recovery during antiretroviral therapy: an AIDS Clinical Trials Group study. J Infect Dis 2006; 194:1098-1107. (Pubitemid 44547649)
35. Fernandez S, Rosenow AA, James IR, Roberts SG, Nolan RC, French MA, Price P. Recovery of CD4R T Cells in HIV patients with a stable virologic response to antiretroviral therapy is associated with polymorphisms of interleukin-6 and central major histocompatibility complex genes. J Acquir Immune Defic Syndr 2006; 41:1-5. (Pubitemid 41786012)
36. Aukrust P, Mü ller F, Lien E, Nordoy I, Liabakk NB, Kvale D, 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. (Pubitemid 29028341)
37. Reddy MM, Sorrell SJ, Lange M, Grieco MH. Tumor necrosis factor and HIV P24 antigen levels in serum of HIV-infected populations. J Acquir Immune Defic Syndr 1988; 1:436-440. (Pubitemid 19129850)
38. Godfried MH, Van der Poll T, Jansen J, Romijin JA, Schattenkerk JK, Endert E, et al. Soluble receptors for tumor necrosis factor are markers for clinical course but not for major metabolic changes in human immunodeficiency virus infection. Metabolism 1995; 44:1564-1569. (Pubitemid 26102595)
39. Stein DS, Lyles RH, Graham NM, Tassoni CJ, Margolick JB, Phair JP, et al. Predicting clinical progression or death in subjects with early-stage human immunodeficiency virus (HIV) infection: a comparative analysis of quantification of HIV RNA, soluble tumor necrosis factor type II receptors, neopterin, and beta2-microglobulin. Multicenter AIDS Cohort Study. J Infect Dis 1997; 176:1161-1167. (Pubitemid 27460979)
40. Fahey JL, Taylor JM, Manna B, Nishanian P, Aziz N, Giorgi JV, Detels R. Prognostic significance of plasma markers of immune activation, HIV viral load and CD4 T-cell measurements. AIDS 1998; 12:1581-1590. (Pubitemid 28418327)
41. Kalayjian RC, Machekano RN, Rizk N, Robbins GK, Gandhi RT, Rodriguez BA, 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.
42. Parish ST, Wu JE, Effros RB. Modulation of T lymphocyte replicative senescence via TNF-{alpha} inhibition: role of caspase-.3. J Immunol 2009; 182:4237-4243.
43. Burton DG, Matsubara H, Ikeda K. Pathophysiology of vascular calcification: pivotal role of cellular senescence in vascular smooth muscle cells. Exp Gerontol 2010; 45:819-824.
44. Norris PJ, Pappalardo BL, Custer B, Spotts G, Hecht FM, Busch MP. Elevations in IL-10, TNF-alpha, and IFN-gamma from the earliest point of HIV Type 1 infection. AIDS Res Hum Retroviruses 2006; 22:757-762. (Pubitemid 44735002)
45. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, Heitman J, et al. Induction of a striking systemic cytokine cascade prior to peak viremia 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.
46. Rychert J, Strick D, Bazner S, Robinson J, Rosenberg E. Detection of HIV gp120 in plasma during early HIV infection is associated with increased proinflammatory and immunoregulatory cytokines. AIDS Res Hum Retroviruses 2010; 26:1139-1145.
47. Stylianou E, Aukrust P, Bendtzen K, Mü ller F, Frøland SS. Interferons and interferon (IFN)-inducible protein 10 during highly active antiretroviral therapy (HAART)-possible immunosuppressive role of IFN-a in HIV infection. Clin Exp Immunol 2000; 119:479-485. (Pubitemid 30146344)
48. Gu Y, Yang J, Ouyang X, Liu W, Li H, Yang J, et al. Interleukin 10 suppresses Th17 cytokines secreted by macrophages and T cells. Eur J Immunol 2008; 38:1807-1813.
49. Mills KH. Induction, function and regulation of IL-17-producing T cells. Eur J Immunol 2008; 38:2636-2649.
50. Heo YJ, Joo YB, Oh HJ, Park MK, Heo YM, Cho ML, et al. IL-10 suppresses Th17 cells and promotes regulatory T cells in the CD4R T cell population of rheumatoid arthritis patients. Immunol Lett 2010; 127:150-156.
51. Naundorf S, Schröder M, Höflich C, Suman N, Volk HD, Grü tz G. IL-10 interferes directly with TCR-induced IFN-gamma but not IL-17 production in memory T cells. Eur J Immunol 2009; 39:1066-1077.
52. Klatt NR, Brenchley JM. Th17 cell dynamics in HIV infection. Curr Opin HIV AIDS 2010; 5:135-140.
53. McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, Huston G, et al. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J Immunol 2009; 182:7353-7363.
54. Roe B, Coughlan S, Hassan J, Grogan A, Farrell G, Norris S, et al. Elevated serum levels of interferon-gamma-inducible protein-10 in patients coinfected with hepatitis C virus and HIV. J Infect Dis 2007; 196:1053-1057. (Pubitemid 47580300)
55. Stone SF, Price P, Brochier J, French MA. Plasma bioavailable interleukin-6 is elevated in human immunodeficiency virusinfected patients who experience herpesvirus-associated immune restoration disease after start of highly active antiretroviral therapy. J Infect Dis 2001; 184:1073-1077. (Pubitemid 32955127)
56. Flandre P, Durier C, Descamps D, Launay O, Joly V. On the use of magnitude of reduction in HIV-1 RNA in clinical trials: statistical analysis and potential biases. J Acquir Immune Defic Syndr 2002; 30:59-64. (Pubitemid 34506687)