Decreases in IL-7 levels during antiretroviral treatment of HIV infection suggest a primary mechanism of receptor-mediated clearance

Blood

Volumn 118, Issue 12, 2011, Pages 3244-3253

  Hodge, Jessica N ^a   Srinivasula, Sharat ^b   Hu, Zonghui ^a   Read, Sarah W ^a   Porter, Brian O ^a   Kim, Insook ^b   Mican, JoAnn M ^a   Paik, Chang ^c   DeGrange, Paula ^a   Di Mascio, Michele ^a   Sereti, Irini ^a  

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

^b SAIC FREDERICK INC   (United States)

^c CLINICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CYCLE; CLINICAL ARTICLE; CONTROLLED STUDY; GROWTH RATE; HOMEOSTASIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNOPHENOTYPING; MATHEMATICAL MODEL; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REGULATORY MECHANISM; T LYMPHOCYTE SUBPOPULATION;

EID: 80053198653     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-12-323600     Document Type: Article

References (50)

1. Sansoni P, Cossarizza A, Brianti V, et al. Lymphocyte subsets and natural killer cell activity in healthy old people and centenarians. Blood. 1993;82(9):2767-2773. (Pubitemid 23318083)
2. Mazzucchelli R, Durum SK. Interleukin-7 receptor expression: intelligent design. Nat Rev Immunol. 2007;7(2):144-154. (Pubitemid 46178275)
3. Sasson SC, Zaunders JJ, Kelleher AD. The IL-7/IL-7 receptor axis: understanding its central role in T-cell homeostasis and the challenges facing its utilization as a novel therapy. Curr Drug Targets. 2006;7(12):1571-1582. (Pubitemid 44873719)
4. Fry TJ, Mackall CL. Interleukin-7: from bench to clinic. Blood. 2002;99(11):3892-3904. (Pubitemid 35332024)
5. Kondrack RM, Harbertson J, Tan JT, McBreen ME, Surh CD, Bradley LM. Interleukin 7 regulates the survival and generation of memory CD4 cells. J Exp Med. 2003;198(12):1797-1806. (Pubitemid 38032113)
6. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol. 2003;4(12):1191-1198. (Pubitemid 37540688)
7. Ozaki K, Leonard WJ. Cytokine and cytokine receptor pleiotropy and redundancy. J Biol Chem. 2002;277(33):29355-29358. (Pubitemid 41079217)
8. Reche PA, Soumelis V, Gorman DM, et al. Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol. 2001;167(1):336-343. (Pubitemid 32567797)
9. Guimond M, Veenstra RG, Grindler DJ, et al. Interleukin 7 signaling in dendritic cells regulates the homeostatic proliferation and niche size of CD4+ T cells. Nat Immunol. 2009;10(2):149-157.
10. Napolitano LA, Grant RM, Deeks SG, et al. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: implications for T-cell homeostasis. Nat Med. 2001;7(1):73-79. (Pubitemid 32095644)
11. Fry TJ, Connick E, Falloon J, et al. A potential role for interleukin-7 in T-cell homeostasis. Blood. 2001;97(10):2983-2990.
12. Bolotin E, Smogorzewska M, Smith S, Widmer M, Weinberg K. Enhancement of thymopoiesis after bone marrow transplant by in vivo interleukin-7. Blood. 1996;88(5):1887-1894. (Pubitemid 26307089)
13. Malaspina A, Moir S, Chaitt DG, et al. Idiopathic CD4+ T lymphocytopenia is associated with increases in immature/transitional B cells and serum levels of IL-7. Blood. 2007;109(5):2086-2088. (Pubitemid 46348209)
14. Pahwa R, McCloskey TW, Aroniadis OC, Strbo N, Krishnan S, Pahwa S. CD8+ T cells in HIV disease exhibit cytokine receptor perturbation and poor T cell receptor activation but are responsive to gamma-chain cytokine-driven proliferation. J Infect Dis. 2006;193(6):879-887.
15. Paiardini M, Cervasi B, Albrecht H, et al. Loss of CD127 expression defines an expansion of effector CD8+ T cells in HIV-infected individuals. J Immunol. 2005;174(5):2900-2909. (Pubitemid 40279708)
16. Read SW, Higgins J, Metcalf JA, et al. Decreased CD127 expression on T Cells in HIV-1-infected adults receiving antiretroviral therapy with or without intermittent IL-2 therapy. J Acquir Immune Defic Syndr. 2006;42(5):537-544. (Pubitemid 44162421)
17. Sasson SC, Zaunders JJ, Zanetti G, et al. Increased plasma interleukin-7 level correlates with decreased CD127 and Increased CD132 extracellular expression on T cell subsets in patients with HIV-1 infection. J Infect Dis. 2006;193(4):505-514. (Pubitemid 43202741)
18. Hakim FT, Memon SA, Cepeda R, et al. Age-dependent incidence, time course, and consequences of thymic renewal in adults. J Clin Invest. 2005;115(4):930-939. (Pubitemid 40489397)
19. Bosco N, Agenes F, Ceredig R. Effects of increasing IL-7 availability on lymphocytes during and after lymphopenia-induced proliferation. J Immunol. 2005;175(1):162-170. (Pubitemid 40884313)
20. Foxwell BM, Woerly G, Ryffel B. Inhibition of interleukin 4 receptor expression on human lymphoid cells by cyclosporin. Eur J Immunol. 1990;20(5):1185-1188. (Pubitemid 20206077)
21. Foxwell BM, Taylor-Fishwick DA, Simon JL, Page TH, Londei M. Activation induced changes in expression and structure of the IL-7 receptor on human T cells. Int Immunol. 1992;4(2):277-282.
22. Dower SK, Ozato K, Segal DM. The interaction of monoclonal antibodies with MHC class I antigens on mouse spleen cells, I: analysis of the mechanism of binding. J Immunol. 1984;132(2):751-758. (Pubitemid 14183672)
23. Gil PE, Murray W, Wright MH. Practical Optimization. London, United Kingdom: Academic Press; 1981:136-137.
24. Wu HL, Zhang JT. Local polynomial mixed-effects models for longitudinal data. J Am Stat Assoc. 2002;97(459):883-897.
25. Zhou L, Huang JZ, Carroll RJ. Joint modelling of paired sparse functional data using principal components. Biometrika. 2008;95(3):601-619.
26. Tzafriri AR, Wu D, Edelman ER. Analysis of compartmental models of ligand-induced endocytosis. J Theor Biol. 2004;229(1):127-138. (Pubitemid 38721256)
27. Beckmann MP, Schooley KA, Gallis B, et al. Monoclonal antibodies block murine IL-4 receptor function. J Immunol. 1990;144(11):4212-4217. (Pubitemid 20187759)
28. 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(25):6304- 6314.
29. Carini C, McLane MF, Mayer KH, Essex M. Dysregulation of interleukin-7 receptor may generate loss of cytotoxic T cell response in human immunodeficiency virus type 1 infection. Eur J Immunol. 1994;24(12):2927-2934.
30. Mohri H, Perelson AS, Tung K, et al. Increased turnover of T lymphocytes in HIV-1 infection and its reduction by antiretroviral therapy. J Exp Med. 2001;194(9):1277-1287. (Pubitemid 33055046)
31. Di Mascio M, Paik CH, Carrasquillo JA, et al. Noninvasive in vivo imaging of CD4 cells in simian-human immunodeficiency virus (SHIV)-infected nonhuman primates. Blood. 2009;114(2):328-337.
32. Anthony KB, Yoder C, Metcalf JA, et al. Incomplete CD4 T cell recovery in HIV-1 infection after 12 months of highly active antiretroviral therapy is associated with ongoing increased CD4 T cell activation and turnover. J Acquir Immune Defic Syndr. 2003;33(2):125-133. (Pubitemid 36793144)
33. Di Mascio M, Sereti I, Matthews LT, et al. Naive T-cell dynamics in human immunodeficiency virus type 1 infection: effects of highly active antiretroviral therapy provide insights into the mechanisms of naive T-cell depletion. J Virol. 2006;80(6):2665-2674. (Pubitemid 43346362)
34. Camargo JF, Kulkarni H, Agan BK, et al. Responsiveness of T cells to interleukin-7 is associated with higher CD4+ T cell counts in HIV-1-positive individuals with highly active antiretroviral therapy-induced viral load suppression. J Infect Dis. 2009;199(12):1872-1882.
35. Benito JM, Lopez M, Lozano S, Gonzalez-Lahoz J, Soriano V. Down-regulation of interleukin-7 receptor (CD127) in HIV infection is associated with T cell activation and is a main factor influencing restoration of CD4(+) cells after antiretroviral therapy. J Infect Dis. 2008;198(10):1466-1473.
36. Mussini C, Pinti M, Borghi V, et al. Features of 'CD4-exploders', HIV-positive patients with an optimal immune reconstitution after potent antiretroviral therapy. AIDS. 2002;16(12):1609-1616. (Pubitemid 34921106)
37. Schacker TW, Nguyen PL, Beilman GJ, et al. Collagen deposition in HIV-1 infected lymphatic tissues and T cell homeostasis. J Clin Invest. 2002;110(8):1133-1139. (Pubitemid 35215894)
38. Ariel A, Hershkoviz R, Cahalon L, et al. Induction of T cell adhesion to extracellular matrix or endothelial cell ligands by soluble or matrix-bound interleukin-7. Eur J Immunol. 1997;27(10):2562-2570. (Pubitemid 27453845)
39. Moniuszko M, Edghill-Smith Y, Venzon D, et al. Decreased number of CD4+ and CD8+ T cells that express the interleukin-7 receptor in blood and tissues of SIV-infected macaques. Virology. 2006;356(1-2):188-197. (Pubitemid 44750035)
40. Mastroianni CM, Forcina G, d'Ettorre G, et al. Circulating levels of interleukin-7 in antiretroviral-naive and highly active antiretroviral therapy-treated HIV-infected patients. HIV Clin Trials. 2001;2(2):108-112. (Pubitemid 32331419)
41. Correa R, Resino S, Munoz-Fernandez MA. Increased interleukin-7 plasma levels are associated with recovery of CD4+ T cells in HIV-infected children. J Clin Immunol. 2003;23(5):401-406. (Pubitemid 37083194)
42. 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(8):1254-1264.
43. Darcissac EC, Vidal V, De La Tribonniere X, Mouton Y, Bahr GM. Variations in serum IL-7 and 90K/Mac-2 binding protein (Mac-2 BP) levels analysed in cohorts of HIV-1 patients and correlated with clinical changes following antiretroviral therapy. Clin Exp Immunol. 2001;126(2):287-294.
44. Lederman MM, McKinnis R, Kelleher D, et al. Cellular restoration in HIV infected persons treated with abacavir and a protease inhibitor: age inversely predicts naive CD4 cell count increase. AIDS. 2000;14(17):2635-2642. (Pubitemid 32118716)
45. Kalayjian RC, Spritzler J, Pu M, et al. Distinct mechanisms of T cell reconstitution can be identified by estimating thymic volume in adult HIV-1 disease. J Infect Dis. 2005;192(9):1577-1587. (Pubitemid 41504693)
46. Engram JC, Cervasi B, Borghans JA, et al. Lineage- specific T-cell reconstitution following in vivo CD4+ and CD8+ lymphocyte depletion in nonhuman primates. Blood. 2010;116(5):748-758.
47. Catalfamo M, Di Mascio M, Hu Z, et al. HIV infection- associated immune activation occurs by two distinct pathways that differentially affect CD4 and CD8 T cells. Proc Natl Acad Sci U S A. 2008;105(50):19851-19856.
48. Adleman LM, Wofsy D. Blind T-cell homeostasis in CD4-deficient mice. J Acquir Immune Defic Syndr Hum Retrovirol. 1996;11(4):334-340. (Pubitemid 26103061)
49. De Bruin HG, Astaldi A, Leupers T, et al. T lymphocyte characteristics in bone marrow-transplanted patients, II: analysis with monoclonal antibodies. J Immunol. 1981;127(1):244-251. (Pubitemid 11075487)
50. Grossman Z, Herberman RB. T-cell homeostasis in HIV infection is neither failing nor blind: modified cell counts reflect an adaptive response of the host. Nat Med. 1997;3(5):486-490. (Pubitemid 27198637)