HIV-1 Nef protein expression in human CD34+ progenitors impairs the differentiation of an early T/NK cell precursor

Virology

Volumn 377, Issue 1, 2008, Pages 207-215

  Dorival, Céline ^a   Brizzi, Fanny ^a   Lelièvre, Jean Daniel ^a,b   Sol Foulon, Nathalie ^c   Six, Emmanuelle ^a   Henry, Adeline ^a   André Schmutz, Isabelle ^d   Cavazzana Calvo, Marina ^d   Coulombel, Laure ^e   Estaquier, Jérôme ^a   Schwartz, Olivier ^c   Lévy, Yves ^a,b  

^a INSERM   (France)

^b HENRI MONDOR HOSPITAL   (France)

^c INSTITUT PASTEUR   (France)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e HÔPITAL PAUL BROUSSE   (France)

Author keywords

CD34+ cells; HIV 1; Nef; NK cells; OP9 DL1; T cell differentiation

Indexed keywords

NEF PROTEIN;

ARTICLE; B LYMPHOCYTE; CD34 SELECTION; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; T LYMPHOCYTE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 44849138169     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.04.009     Document Type: Article

References (57)

1. Baillou C., Simon A., Leclercq V., Azar N., Rosenzwajg M., Herson S., Klatzmann D., and Lemoine F.M. Highly active antiretroviral therapy corrects hematopoiesis in HIV-1 infected patients: interest for peripheral blood stem cell-based gene therapy. Aids 17 4 (2003) 563-574
2. Berkowitz R.D., Beckerman K.P., Schall T.J., and McCune J.M. CXCR4 and CCR5 expression delineates targets for HIV-1 disruption of T cell differentiation. J. Immunol. 161 7 (1998) 3702-3710
3. Bonyhadi M.L., Rabin L., Salimi S., Brown D.A., Kosek J., McCune J.M., and Kaneshima H. HIV induces thymus depletion in vivo. Nature 363 6431 (1993) 728-732
4. Brady H.J., Pennington D.J., Miles C.G., and Dzierzak E.A. CD4 cell surface downregulation in HIV-1 Nef transgenic mice is a consequence of intracellular sequestration. EMBO J. 12 13 (1993) 4923-4932
5. Deacon N.J., Tsykin A., Solomon A., Smith K., Ludford-Menting M., Hooker D.J., McPhee D.A., Greenway A.L., Ellett A., Chatfield C., Lawson V.A., Crowe S., Maerz A., Sonza S., Learmont J., Sullivan J.S., Cunningham A., Dwyer D., Dowton D., and Mills J. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270 5238 (1995) 988-9891
6. Deichmann M., Kronenwett R., and Haas R. Expression of the human immunodeficiency virus type-1 coreceptors CXCR-4 (fusin, LESTR) and CKR-5 in CD34+ hematopoietic progenitor cells. Blood 89 10 (1997) 3522-3528
7. Dion M.L., Poulin J.F., Bordi R., Sylvestre M., Corsini R., Kettaf N., Dalloul A., Boulassel M.R., Debre P., Routy J.P., Grossman Z., Sekaly R.P., and Cheynier R. HIV infection rapidly induces and maintains a substantial suppression of thymocyte proliferation. Immunity 21 6 (2004) 757-768
8. Douek D.C., Betts M.R., Hill B.J., Little S.J., Lempicki R., Metcalf J.A., Casazza J., Yoder C., Adelsberger J.W., Stevens R.A., Baseler M.W., Keiser P., Richman D.D., Davey R.T., and Koup R.A. Evidence for increased T cell turnover and decreased thymic output in HIV infection. J. immunol. 167 11 (2001) 6663-6668
9. Duus K.M., Miller E.D., Smith J.A., Kovalev G.I., and Su L. Separation of human immunodeficiency virus type 1 replication from nef-mediated pathogenesis in the human thymus. J. Virol. 75 8 (2001) 3916-3924
10. Fackler O.T., and Baur A.S. Live and let die: Nef functions beyond HIV replication. Immunity 16 4 (2002) 493-497
11. Garcia J.V., and Miller A.D. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350 6318 (1991) 508-511
12. Geleziunas R., Xu W., Takeda K., Ichijo H., and Greene W.C. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature 410 6830 (2001) 834-838
13. Guatelli J.C., Gingeras T.R., and Richman D.D. Alternative splice acceptor utilization during human immunodeficiency virus type 1 infection of cultured cells. J. Virol. 64 9 (1990) 4093-4098
14. Hanna Z., Kay D.G., Cool M., Jothy S., Rebai N., and Jolicoeur P. Transgenic mice expressing human immunodeficiency virus type 1 in immune cells develop a severe AIDS-like disease. J. Virol. 72 1 (1998) 121-132
15. Hanna Z., Weng X., Kay D.G., Poudrier J., Lowell C., and Jolicoeur P. The pathogenicity of human immunodeficiency virus (HIV) type 1 Nef in CD4C/HIV transgenic mice is abolished by mutation of its SH3-binding domain, and disease development is delayed in the absence of Hck. J. Virol. 75 19 (2001) 9378-9392
16. Hatzakis A., Touloumi G., Karanicolas R., Karafoulidou A., Mandalaki T., Anastassopoulou C., Zhang L., Goedert J.J., Ho D.D., and Kostrikis L.G. Effect of recent thymic emigrants on progression of HIV-1 disease. Lancet 355 9204 (2000) 599-604
17. Itano A., Cado D., Chan F.K., and Robey E. A role for the cytoplasmic tail of the beta chain of CD8 in thymic selection. Immunity 1 4 (1994) 287-290
18. Jamieson B.D., Aldrovandi G.M., Planelles V., Jowett J.B., Gao L., Bloch L.M., Chen I.S., and Zack J.A. Requirement of human immunodeficiency virus type 1 nef for in vivo replication and pathogenicity. J. Virol. 68 6 (1994) 3478-3485
19. Janardhan A., Swigut T., Hill B., Myers M.P., and Skowronski J. HIV-1 Nef binds the DOCK2-ELMO1 complex to activate rac and inhibit lymphocyte chemotaxis. PLoS Biol. 2 1 (2004) E6
20. Kestler III H.W., Ringler D.J., Mori K., Panicali D.L., Sehgal P.K., Daniel M.D., and Desrosiers R.C. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65 4 (1991) 651-662
21. Knutsen A.P., Roodman S.T., Freeman J.J., Mueller K.R., and Bouhasin J.D. Inhibition of thymopoiesis of CD34+ cell maturation by HIV-1 in an in vitro CD34+ cell and thymic epithelial organ culture model. Stem Cells 17 6 (1999) 327-338
22. La Motte-Mohs R.N., Herer E., and Zuniga-Pflucker J.C. Induction of T-cell development from human cord blood hematopoietic stem cells by Delta-like 1 in vitro. Blood 105 4 (2005) 1431-1439
23. Lefort N., Benne C., Lelievre J.D., Dorival C., Balbo M., Sakano S., Coulombel L., and Levy Y. Short exposure to Notch ligand Delta-4 is sufficient to induce T-cell differentiation program and to increase the T cell potential of primary human CD34+ cells. Exp. Hematol. 34 12 (2006) 1720-1729
24. Levy Y. [Cytokine therapies in HIV infection]. Med. Sci. (Paris) 22 8-9 (2006) 751-754
25. Michel N., Allespach I., Venzke S., Fackler O.T., and Keppler O.T. The Nef protein of human immunodeficiency virus establishes superinfection immunity by a dual strategy to downregulate cell-surface CCR5 and CD4. Curr Biol 15 8 (2005) 714-723
26. Moanna A., Dunham R., Paiardini M., and Silvestri G. CD4+ T-cell depletion in HIV infection: killed by friendly fire?. Curr. HIV/AIDS Rep. 2 1 (2005) 16-23
27. Neal T.F., Holland H.K., Baum C.M., Villinger F., Ansari A.A., Saral R., Wingard J.R., and Fleming W.H. CD34+ progenitor cells from asymptomatic patients are not a major reservoir for human immunodeficiency virus-1. Blood 86 5 (1995) 1749-1756
28. Rahemtulla A., Fung-Leung W.P., Schilham M.W., Kundig T.M., Sambhara S.R., Narendran A., Arabian A., Wakeham A., Paige C.J., Zinkernagel R.M., et al. Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353 6340 (1991) 180-184
29. Reynaud D., Lefort N., Manie E., Coulombel L., and Levy Y. In vitro identification of human pro-B cells that give rise to macrophages, natural killer cells, and T cells. Blood 101 11 (2003) 4313-4321
30. Richardson M.W., Sverstiuk A., Hendel H., Cheung T.W., Zagury J.F., and Rappaport J. Analysis of telomere length and thymic output in fast and slow/non-progressors with HIV infection. Biomed. Pharmacother. 54 1 (2000) 21-31
31. Robert-Guroff M., Popovic M., Gartner S., Markham P., Gallo R.C., and Reitz M.S. Structure and expression of tat-, rev-, and nef-specific transcripts of human immunodeficiency virus type 1 in infected lymphocytes and macrophages. J. Virol. 64 7 (1990) 3391-3398
32. Ruiz M.E., Cicala C., Arthos J., Kinter A., Catanzaro A.T., Adelsberger J., Holmes K.L., Cohen O.J., and Fauci A.S. Peripheral blood-derived CD34+ progenitor cells: CXC chemokine receptor 4 and CC chemokine receptor 5 expression and infection by HIV. J. Immunol. 161 8 (1998) 4169-4176
33. Schmitt T.M., and Zuniga-Pflucker J.C. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17 6 (2002) 749-756
34. Schnittman S.M., Denning S.M., Greenhouse J.J., Justement J.S., Baseler M., Kurtzberg J., Haynes B.F., and Fauci A.S. Evidence for susceptibility of intrathymic T-cell precursors and their progeny carrying T-cell antigen receptor phenotypes TCR alpha beta + and TCR gamma delta + to human immunodeficiency virus infection: a mechanism for CD4+ (T4) lymphocyte depletion. Proc. Natl. Acad. Sci. U. S. A. 87 19 (1990) 7727-7731
35. Schrager J.A., and Marsh J.W. HIV-1 Nef increases T cell activation in a stimulus-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 96 14 (1999) 8167-8172
36. Schwartz O., Marechal V., Le Gall S., Lemonnier F., and Heard J.M. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2 3 (1996) 338-342
37. Simmons A., Aluvihare V., and McMichael A. Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 14 6 (2001) 763-777
38. Sirven A., Ravet E., Charneau P., Zennou V., Coulombel L., Guetard D., Pflumio F., and Dubart-Kupperschmitt A. Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol. Ther. 3 4 (2001) 438-448
39. Skowronski J., Parks D., and Mariani R. Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J. 12 2 (1993) 703-713
40. Sol-Foulon N., Moris A., Nobile C., Boccaccio C., Engering A., Abastado J.P., Heard J.M., van Kooyk Y., and Schwartz O. HIV-1 Nef-induced upregulation of DC-SIGN in dendritic cells promotes lymphocyte clustering and viral spread. Immunity 16 1 (2002) 145-155
41. Sol-Foulon N., Esnault C., Percherancier Y., Porrot F., Metais-Cunha P., Bachelerie F., and Schwartz O. The effects of HIV-1 Nef on CD4 surface expression and viral infectivity in lymphoid cells are independent of rafts. J. Biol. Chem. 279 30 (2004) 31398-31408
42. Stanley S.K., Kessler S.W., Justement J.S., Schnittman S.M., Greenhouse J.J., Brown C.C., Musongela L., Musey K., Kapita B., and Fauci A.S. CD34+ bone marrow cells are infected with HIV in a subset of seropositive individuals. J. Immunol. 149 2 (1992) 689-697
43. Stoddart C.A., Geleziunas R., Ferrell S., Linquist-Stepps V., Moreno M.E., Bare C., Xu W., Yonemoto W., Bresnahan P.A., McCune J.M., and Greene W.C. Human immunodeficiency virus type 1 Nef-mediated downregulation of CD4 correlates with Nef enhancement of viral pathogenesis. J. Virol. 77 3 (2003) 2124-2133
44. Stove V., Naessens E., Stove C., Swigut T., Plum J., and Verhasselt B. Signaling but not trafficking function of HIV-1 protein Nef is essential for Nef-induced defects in human intrathymic T-cell development. Blood 102 8 (2003) 2925-2932
45. Stove V., Van de Walle I., Naessens E., Coene E., Stove C., Plum J., and Verhasselt B. Human immunodeficiency virus Nef induces rapid internalization of the T-cell coreceptor CD8alphabeta. J. Virol. 79 17 (2005) 11422-11433
46. Stumptner-Cuvelette P., Morchoisne S., Dugast M., Le Gall S., Raposo G., Schwartz O., and Benaroch P. HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc. Natl. Acad. Sci. U. S. A. 98 21 (2001) 12144-12149
47. Su L., Kaneshima H., Bonyhadi M., Salimi S., Kraft D., Rabin L., and McCune J.M. HIV-1-induced thymocyte depletion is associated with indirect cytopathogenicity and infection of progenitor cells in vivo. Immunity 2 1 (1995) 25-36
48. Swigut T., Shohdy N., and Skowronski J. Mechanism for down-regulation of CD28 by Nef. EMBO J. 20 7 (2001) 1593-1604
49. Tolstrup M., Ostergaard L., Laursen A.L., Pedersen S.F., and Duch M. HIV/SIV escape from immune surveillance: focus on Nef. Curr. HIV Res. 2 2 (2004) 141-151
50. Valentin H., Nugeyre M.T., Vuillier F., Boumsell L., Schmid M., Barre-Sinoussi F., and Pereira R.A. Two subpopulations of human triple-negative thymic cells are susceptible to infection by human immunodeficiency virus type 1 in vitro. J. Virol. 68 5 (1994) 3041-3050
51. Verhasselt B., Naessens E., Verhofstede C., De Smedt M., Schollen S., Kerre T., Vanhecke D., and Plum J. Human immunodeficiency virus nef gene expression affects generation and function of human T cells, but not dendritic cells. Blood 94 8 (1999) 2809-2818
52. von Laer D., Hufert F.T., Fenner T.E., Schwander S., Dietrich M., Schmitz H., and Kern P. CD34+ hematopoietic progenitor cells are not a major reservoir of the human immunodeficiency virus. Blood 76 7 (1990) 1281-1286
53. Weichold F.F., Zella D., Barabitskaja O., Maciejewski J.P., Dunn D.E., Sloand E.M., and Young N.S. Neither human immunodeficiency virus-1 (HIV-1) nor HIV-2 infects most-primitive human hematopoietic stem cells as assessed in long-term bone marrow cultures. Blood 91 3 (1998) 907-915
54. Xu X.N., Laffert B., Screaton G.R., Kraft M., Wolf D., Kolanus W., Mongkolsapay J., McMichael A.J., and Baur A.S. Induction of Fas ligand expression by HIV involves the interaction of Nef with the T cell receptor zeta chain. J. Exp. Med. 189 9 (1999) 1489-1496
55. Zaitseva M.B., Lee S., Rabin R.L., Tiffany H.L., Farber J.M., Peden K.W., Murphy P.M., and Golding H. CXCR4 and CCR5 on human thymocytes: biological function and role in HIV-1 infection. J. Immunol. 161 6 (1998) 3103-3113
56. Zauli G., Vitale M., Re M.C., Furlini G., Zamai L., Falcieri E., Gibellini D., Visani G., Davis B.R., Capitani S., et al. In vitro exposure to human immunodeficiency virus type 1 induces apoptotic cell death of the factor-dependent TF-1 hematopoietic cell line. Blood 83 1 (1994) 167-175
57. Zauli G., Gibellini D., Secchiero P., Dutartre H., Olive D., Capitani S., and Collette Y. Human immunodeficiency virus type 1 Nef protein sensitizes CD4(+) T lymphoid cells to apoptosis via functional upregulation of the CD95/CD95 ligand pathway. Blood 93 3 (1999) 1000-1010