HIV disease progression despite suppression of viral replication is associated with exhaustion of lymphopoiesis

Blood

Volumn 117, Issue 19, 2011, Pages 5142-5151

  Sauce, Delphine ^a   Larsen, Martin ^a,b   Fastenackels, Solène ^a   Pauchard, Michèle ^a,b   Ait Mohand, Hocine ^a,b   Schneider, Luminita ^a,b   Guihot, Amélie ^a   Boufassa, Faroudy ^c   Zaunders, John ^d   Iguertsira, Malika ^a   Bailey, Michelle ^d   Gorochov, Guy ^a,b   Duvivier, Claudine ^e,f,g   Carcelain, Guislaine ^a   Kelleher, Anthony D ^d   Simon, Anne ^a   Meyer, Laurence ^c,h   Costagliola, Dominique ^a,b   Deeks, Steven G ⁱ   Lambotte, Olivier ^b,h   Autran, Brigitte ^a   Hunt, Peter W ^a,b   Katlama, Christine ^a,b   Appay, Victor ^a   more..

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b INSERM   (France)

^c CENTRE FOR RESEARCH IN EPIDEMIOLOGY AND POPULATION HEALTH   (France)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g INSTITUT PASTEUR   (France)

^h BICÊTRE HOSPITAL   (France)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN;

ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DRUG RESPONSE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOPOIESIS; PRIORITY JOURNAL; VIRUS PATHOGENESIS; VIRUS REPLICATION;

EID: 79955962732     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-01-331306     Document Type: Article

References (55)

1. Giorgi JV, Hultin LE, McKeating JA, 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(4):859-870. (Pubitemid 29159331)
2. Hazenberg MD, Hamann D, Schuitemaker H, Miedema F. T cell depletion in HIV-1 infection: how CD4+ T cells go out of stock. Nat Immunol. 2000;1(4):285-289.
3. Grossman Z, Meier-Schellersheim M, Sousa AE, Victorino RM, Paul WE. CD4+ T-cell depletion in HIV infection: are we closer to understanding the cause? Nat Med. 2002;8(4):319-323.
4. 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(13):1881-1888. (Pubitemid 37070273)
5. Deeks SG, Kitchen CM, Liu L, et al. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood. 2004;104(4):942-947. (Pubitemid 39038012)
6. Appay V, Sauce D. Immune activation and inflammation in HIV-1 infection: causes and consequences. J Pathol. 2008;214(2):231-241. (Pubitemid 351160160)
7. Roederer M, Dubs JG, Anderson MT, Raju PA, Herzenberg LA. CD8 naive T cell counts decrease progressively in HIV-infected adults. J Clin Invest. 1995;95(5):2061-2066.
8. Hazenberg MD, Borghans JA, de Boer RJ, Miedema F. Thymic output: a bad TREC record. Nat Immunol. 2003;4(2):97-99. (Pubitemid 36193005)
9. Dion ML, Poulin JF, Bordi R, et al. HIV infection rapidly induces and maintains a substantial suppression of thymocyte proliferation. Immunity. 2004;21(6):757-768. (Pubitemid 39626667)
10. Vrisekoop N, den Braber I, de Boer AB, et al. Sparse production but preferential incorporation of recently produced naive T cells in the human peripheral pool. Proc Natl Acad Sci U S A. 2008; 105(16):6115-6120. (Pubitemid 351758408)
11. Vrisekoop N, van Gent R, de Boer AB, et al. Restoration of the CD4 T cell compartment after longterm highly active antiretroviral therapy without phenotypical signs of accelerated immunological aging. J Immunol. 2008;181(2):1573-1581.
12. Douek DC, McFarland RD, Keiser PH, et al. Changes in thymic function with age and during the treatment of HIV infection. Nature. 1998; 396(6712):690-695.
13. Douek DC, Betts MR, Hill BJ, et al. Evidence for increased T cell turnover and decreased thymic output in HIV infection. J Immunol. 2001;167(11): 6663-6668. (Pubitemid 33081605)
14. Dion ML, Bordi R, Zeidan J, et al. Slow disease progression and robust therapy-mediated CD4+ T-cell recovery are associated with efficient thymopoiesis during HIV-1 infection. Blood. 2007; 109(7):2912-2920. (Pubitemid 46482088)
15. Kalayjian RC, Landay A, Pollard RB, et al. Age-related immune dysfunction in health and in human immunodeficiency virus (HIV) disease: association of age and HIV infection with naive CD8+ cell depletion, reduced expression of CD28 on CD8+ cells, and reduced thymic volumes. J Infect Dis. 2003;187(12):1924-1933. (Pubitemid 36724491)
16. Stanley SK, McCune JM, Kaneshima H, et al. Human immunodeficiency virus infection of the human thymus and disruption of the thymic microenvironment in the SCID-hu mouse. J Exp Med. 1993;178(4):1151-1163. (Pubitemid 23277349)
17. 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(8): 1797-1805.
18. Marandin A, Katz A, Oksenhendler E, et al. Loss of primitive hematopoietic progenitors in patients with human immunodeficiency virus infection. Blood. 1996;88(12):4568-4578. (Pubitemid 26419139)
19. Jenkins M, Hanley MB, Moreno MB, Wieder E, McCune JM. Human immunodeficiency virus-1 infection interrupts thymopoiesis and multilineage hematopoiesis in vivo. Blood. 1998;91(8):2672-2678. (Pubitemid 28227515)
20. Moses A, Nelson J, Bagby GC Jr. The influence of human immunodeficiency virus-1 on hematopoiesis. Blood. 1998;91(5):1479-1495. (Pubitemid 28110310)
21. Thiebot H, Vaslin B, Derdouch S, et al. Impact of bone marrow hematopoiesis failure on T-cell generation during pathogenic simian immunodeficiency virus infection in macaques. Blood. 2005; 105(6):2403-2409. (Pubitemid 40387038)
22. Effros RB, Globerson A. Hematopoietic cells and replicative senescence. Exp Gerontol. 37(2-3): 191-196, 2002. (Pubitemid 34073534)
23. Terstappen LW, Huang S, Safford M, Lansdorp PM, Loken MR. Sequential generations of hematopoietic colonies derived from single nonlineage-committed CD34+CD38- progenitor cells. Blood. 1991;77(6):1218-1227.
24. Galy A, Travis M, Cen D, Chen B. Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity. 1995;3(4):459-473.
25. Miettinen M, Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl Immunohistochem Mol Morphol. 2005;13(3): 205-220. (Pubitemid 41209013)
26. Six EM, Bonhomme D, Monteiro M, et al. A human postnatal lymphoid progenitor capable of circulating and seeding the thymus. J Exp Med. 2007;204(13):3085-3093.
27. De Luca A, Teofili L, Antinori A, et al. Haemopoietic CD34+ progenitor cells are not infected by HIV-1 in vivo but show impaired clonogenesis. Br J Haematol. 1993;85(1):20-24. (Pubitemid 23291468)
28. Carter CC, Onafuwa-Nuga A, McNamara LA, et al. HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat Med. 2010;16(4):446-451.
29. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med. 1997; 185(1):111-120. (Pubitemid 27039446)
30. Sarris AH, Broxmeyer HE, Wirthmueller U, et al. Human interferon-inducible protein 10: expression and purification of recombinant protein demonstrate inhibition of early human hematopoietic progenitors. J Exp Med. 1993;178(3):1127-1132. (Pubitemid 23260454)
31. Schwartz GN, Liao F, Gress RE, Farber JM. Suppressive effects of recombinant human monokine induced by IFN-gamma (rHuMig) chemokine on the number of committed and primitive hemopoietic progenitors in liquid cultures of CD34+ human bone marrow cells. J Immunol. 1997;159(2): 895-904. (Pubitemid 127484243)
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(12):1365-1371. (Pubitemid 44924494)
33. Hunt PW, Brenchley J, Sinclair E, et al. Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis. 2008;197(1):126-133. (Pubitemid 351263476)
34. 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(5): 587-599. (Pubitemid 39258308)
35. Clark DR, Ampel NM, Hallett CA, Yedavalli VR, Ahmad N, DeLuca D. Peripheral blood from human immunodeficiency virus type 1-infected patients displays diminished T cell generation capacity. J Infect Dis. 1997;176(3):649-654. (Pubitemid 27360529)
36. Clark DR, Repping S, Pakker NG, et al. T-cell progenitor function during progressive human immunodeficiency virus-1 infection and after antiretroviral therapy. Blood. 2000;96(1):242-249. (Pubitemid 30456477)
37. Nielsen SD, Jeppesen DL, Kolte L, et al. Impaired progenitor cell function in HIV-negative infants of HIV-positive mothers results in decreased thymic output and low CD4 counts. Blood. 2001;98(2): 398-404.
38. Dorival C, Brizzi F, Lelievre JD, et al. HIV-1 Nef protein expression in human CD34+ progenitors impairs the differentiation of an early T/NK cell precursor. Virology. 2008;377(1):207-215. (Pubitemid 351799836)
39. Prost S, Le Dantec M, Auge S, et al. Human and simian immunodeficiency viruses deregulate early hematopoiesis through a Nef/PPARgamma/ STAT5 signaling pathway in macaques. J Clin Invest. 2008;118(5):1765-1775. (Pubitemid 351632379)
40. Moses AV, Williams S, Heneveld ML, et al. Human immunodeficiency virus infection of bone marrow endothelium reduces induction of stromal hematopoietic growth factors. Blood. 1996;87(3): 919-925. (Pubitemid 26043522)
41. Mandl JN, Barry AP, Vanderford TH, et al. Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med. 2008; 14(10):1077-1087.
42. Jacquelin B, Mayau V, Targat B, et al. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest. 2009;119(12):3544-3555.
43. Nagai Y, Garrett KP, Ohta S, et al. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity. 2006;24(6):801-812. (Pubitemid 43867369)
44. Blackwell SE, Krieg AM. CpG-A-induced monocyte IFN-gamma-inducible protein-10 production is regulated by plasmacytoid dendritic cell-derived IFN-alpha. J Immunol. 2003;170(8):4061-4068.
45. Jiang W, Lederman MM, Hunt P, et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis. 2009;199(8):1177-1185.
46. Binder D, Fehr J, Hengartner H, Zinkernagel RM. Virus-induced transient bone marrow aplasia: major role of interferon-alpha/beta during acute infection with the noncytopathic lymphocytic choriomeningitis virus. J Exp Med. 1997;185(3):517-530. (Pubitemid 27078370)
47. Lin Q, Dong C, Cooper MD. Impairment of T and B cell development by treatment with a type I interferon. J Exp Med. 1998;187(1):79-87. (Pubitemid 28044822)
48. Dam Nielsen S, Kjaer Ersboll A, Mathiesen L, Nielsen JO, Hansen JE. Highly active antiretroviral therapy normalizes the function of progenitor cells in human immunodeficiency virus-infected patients. J Infect Dis. 1998;178(5):1299-1305. (Pubitemid 28523266)
49. Adams GB, Pym AS, Poznansky MC, McClure MO, Weber JN. The in vivo effects of combination antiretroviral drug therapy on peripheral blood CD34+ cell colony-forming units from HIV type 1-infected patients. AIDS Res Hum Retroviruses. 1999;15(6):551-559. (Pubitemid 29177851)
50. Baillou C, Simon A, Leclercq V, et al. Highly active antiretroviral therapy corrects hematopoiesis in HIV-1 infected patients: interest for peripheral blood stem cell-based gene therapy. AIDS. 2003; 17(4):563-574. (Pubitemid 36293110)
51. Thiebot H, Louache F, Vaslin B, et al. Early and persistent bone marrow hematopoiesis defect in simian/human immunodeficiency virus-infected macaques despite efficient reduction of viremia by highly active antiretroviral therapy during primary infection. J Virol. 2001;75(23):11594-11602. (Pubitemid 33063251)
52. Isgro A, Leti W, De Santis W, et al. Altered clonogenic capability and stromal cell function characterize bone marrow of HIV-infected subjects with low CD4+ T cell counts despite viral suppression during HAART. Clin Infect Dis. 2008;46(12):1902-1910.
53. French RA, Broussard SR, Meier WA, et al. Age-associated loss of bone marrow hematopoietic cells is reversed by GH and accompanies thymic reconstitution. Endocrinology. 2002;143(2):690-699. (Pubitemid 34107225)
54. Hanley MB, Napolitano LA, McCune JM. Growth hormone-induced stimulation of multilineage human hematopoiesis. Stem Cells. 2005;23(8): 1170-1179. (Pubitemid 41377732)
55. Napolitano LA, Schmidt D, Gotway MB, et al. Growth hormone enhances thymic function in HIV-1-infected adults. J Clin Invest. 2008;118(3): 1085-1098. (Pubitemid 351364616)