Human and simian immunodeficiency viruses deregulate early hematopoiesis through a Nef/PPARγ/STAT5 signaling pathway in macaques

Journal of Clinical Investigation

Volumn 118, Issue 5, 2008, Pages 1765-1775

  Prost, Stéphane ^a   Le Dantec, Mikael ^a   Augé, Sylvie ^b,c   Le Grand, Roger ^a   Derdouch, Sonia ^a   Auregan, Gwenaelle ^a,d   Déglon, Nicole ^d   Relouzat, Francis ^a   Aubertin, Anne Marie ^e   Maillere, Bernard ^f   Dusanter Fourt, Isabelle ^b,c   Kirszenbaum, Marek ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b INSTITUT COCHIN   (France)

^c INSERM   (France)

^d DIF   (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

^f CEA SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; [2 METHYL 4 [4 METHYL 2 (4 TRIFLUOROMETHYLPHENYL) 5 THIAZOLYLMETHYLTHIO]PHENOXY]ACETIC ACID; CIGLITAZONE; NEF PROTEIN; NETOGLITAZONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; PIOGLITAZONE; PROSTAGLANDIN J2; ROSIGLITAZONE; STAT5A PROTEIN; STAT5B PROTEIN; TROGLITAZONE; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DILUTION; DOWN REGULATION; DRUG ANTAGONISM; DRUG MECHANISM; EX VIVO STUDY; FEMALE; HEMATOPOIESIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VIVO STUDY; MACACA; MALE; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; TARGET CELL; VIRUS INFECTION; VIRUS REPLICATION; VIRUS VIRULENCE;

AMINO ACID SEQUENCE; ANIMALS; FEMALE; GENE PRODUCTS, NEF; HEMATOLOGIC DISEASES; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HIV-1; HUMANS; K562 CELLS; MACACA FASCICULARIS; MALE; MOLECULAR SEQUENCE DATA; PPAR GAMMA; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; STAT5 TRANSCRIPTION FACTOR;

EID: 43049118940     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI33037     Document Type: Article

References (61)

1. Moses, A., Nelson, J., and Bagby, G.C., Jr. 1998. The influence of human immunodeficiency virus-1 on hematopoiesis. Blood. 91:1479-1495.
2. Zon, L.I., Arkin, C., and Groopman, J.E. 1987. Haematologic manifestations of the human immune deficiency virus (HIV). Br. J. Haematol. 66:251-256.
3. Koka, P.S., and Reddy, S.T. 2004. Cytopenias in HIV infection: mechanisms and alleviation of hematopoietic inhibition. Curr. HIV Res. 2:275-282.
4. Levine, A.M., Scadden, D.T., Zaia, J.A., and Krishnan, A. 2001. Hematologic aspects of HIV/AIDS. Hematology Am. Soc. Hematol. Educ. Program. 2001:463-478.
5. Marandin, A., et al. 1996. Loss of primitive hematopoietic progenitors in patients with human immunodeficiency virus infection. Blood. 88:4568-4578.
6. Sloand, E.M., et al. 1997. Secondary colony formation after long-term bone marrow culture using peripheral blood and bone marrow of HIV-infected patients. AIDS. 11:1547-1553.
7. Thiebot, H., et al. 2005. Impact of bone marrow hematopoiesis failure on T-cell generation during pathogenic simian immunodeficiency virus infection in macaques. Blood. 105:2403-2409.
8. Burstein, Y., et al. 1992. Alterations in human fetal hematopoiesis are associated with maternal HIV infection. Pediatr. Res. 32:155-159.
9. Bieniasz, P.D. 2007. An intrinsic host defense against HIV-1 integration? J. Clin. Invest. 117:302-304.
10. De Luca, A., et al. 1993. Haemopoietic CD34+ progenitor cells are not infected by HIV-1 in vivo but show impaired clonogenesis. Br. J. Haematol. 85:20-24.
11. Koka, P.S., Jamieson, B.D., Brooks, D.G., and Zack, J.A. 1999. Human immunodeficiency virus type 1-induced hematopoietic inhibition is independent of productive infection of progenitor cells in vivo. J. Virol. 73:9089-9097.
12. Molina, J.M., et al. 1990. Lack of evidence for infection of or effect on growth of hematopoietic progenitor cells after in vivo or in vitro exposure to human immunodeficiency virus. Blood. 76:2476-2482.
13. Jenkins, M., Hanley, M.B., Moreno, M.B., Wieder, E., and McCune, J.M. 1998. Human immunodeficiency virus-1 infection interrupts thymopoiesis and multilineage hematopoiesis in vivo. Blood. 91:2672-2678.
14. Moses, A.V., et al. 1996. Human immunodeficiency virus infection of bone marrow endothelium reduces induction of stromal hematopoietic growth factors. Blood. 87:919-925.
15. Calenda, V., Graber, P., Delamarter, J.F., and Chermann, J.C. 1994. Involvement of HIV nef protein in abnormal hematopoiesis in AIDS: in vitro study on bone marrow progenitor cells. Eur. J. Haematol. 52:103-107.
16. Rameshwar, P., Denny, T.N., and Gascon, P. 1996. Enhanced HIV-1 activity in bone marrow can lead to myelopoietic suppression partially contributed by gag p24. J. Immunol. 157:4244-4250.
17. Reinhold, D., Wrenger, S., Kahne, T., and Ansorge, S. 1999. HIV-1 Tat: immunosuppression via TGF-beta1 induction. Immunol. Today. 20:384-385.
18. Sugiura, K., Oyaizu, N., Pahwa, R., Kalyanaraman, V.S., and Pahwa, S. 1992. Effect of human immunodeficiency virus-1 envelope glycoprotein on in vitro hematopoiesis of umbilical cord blood. Blood. 80:1463-1469.
19. Zauli, G., Re, M.C., Furlini, G., Giovannini, M., and La Placa, M. 1992. Human immunodeficiency virus type 1 envelope glycoprotein gp120- mediated killing of human haematopoietic progenitors (CD34+ cells). J. Gen. Virol. 73:417-421.
20. Maciejewski, J.P., Weichold, F.F., and Young, N.S. 1994. HIV-1 suppression of hematopoiesis in vitro mediated by envelope glycoprotein and TNF-alpha. J. Immunol. 153:4303-4310.
21. Hillyer, C.D., et al. 1993. CD34+ and CFU-GM progenitors are significantly decreased in SIVsmm9 infected rhesus macaques with minimal evidence of direct viral infection by polymerase chain reaction. Am. J. Hematol. 43:274-278.
22. Thiebot, H., et al. 2001. 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. 75:11594-11602.
23. Bradley, T.R., and Metcalf, D. 1966. The growth of mouse bone marrow cells in vitro. Aust. J. Exp. Biol. Med. Sci. 44:287-299.
24. Stein, M.I., Zhu, J., and Emerson, S.G. 2004. Molecular pathways regulating the self-renewal of hematopoietic stem cells. Exp. Hematol. 32:1129-1136.
25. Hou, S.X., Zheng, Z., Chen, X., and Perrimon, N. 2002. The Jak/STAT pathway in model organisms: emerging roles in cell movement. Dev. Cell. 3:765-778.
26. Ihle, J.N., et al. 1998. The roles of Jaks and Stats in cytokine signaling. Cancer J. Sci. Am. 4(Suppl. 1):S84-S91.
27. Baskiewicz-Masiuk, M., Paczkowski, M., and Machalinski, B. 2004. The influence of antisense oligonucleotides against STAT5 on the regulation of normal haematopoiesis in a bone marrow model. Cell Prolif. 37:231-245.
28. Bradley, H.L., Couldrey, C., and Bunting, K.D. 2004. Hematopoietic- repopulating defects from STAT5-deficient bone marrow are not fully accounted for by loss of thrombopoietin responsiveness. Blood. 103:2965- 2972.
29. Bradley, H.L., Hawley, T.S., and Bunting, K.D. 2002. Cell intrinsic defects in cytokine responsiveness of STAT5-deficient hematopoietic stem cells. Blood. 100:3983-3989.
30. Kyba, M., et al. 2003. Enhanced hematopoietic differentiation of embryonic stem cells conditionally expressing Stat5. Proc. Natl. Acad. Sci. U. S. A. 100(Suppl. 1):11904-11910.
31. Nosaka, T., et al. 1999. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 18:4754-4765.
32. Yao, Z., et al. 2006. Stat5a/b are essential for normal lymphoid development and differentiation. Proc. Natl. Acad. Sci. U. S. A. 103:1000-1005.
33. Michael, N.L., et al. 1999. Development of calibrated viral load standards for group M subtypes of human immunodeficiency virus type 1 and performance of an improved AMPLICOR HIV-1 MONITOR test with isolates of diverse subtypes. J. Clin. Microbiol. 37:2557-2563.
34. Geyer, M., Fackler, O.T., and Peterlin, B.M. 2001. Structure - function relationships in HIV-1 Nef. EMBO Rep. 2:580-585.
35. Pandori, M.W., et al. 1996. Producer-cell modification of human immunodeficiency virus type 1: Nef is a virion protein. J. Virol. 70:4283-4290.
36. Fujii, Y., Otake, K., Tashiro, M., and Adachi, A. 1996. Soluble Nef antigen of HIV-1 is cytotoxic for human CD4+ T cells. FEBS Lett. 393:93-96.
37. Chakrabarti, L., et al. 1995. Limited viral spread and rapid immune response in lymph nodes of macaques inoculated with attenuated simian immunodeficiency virus. Virology. 213:535-548.
38. Hanna, Z., et al. 2001. 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. 75:9378-9392.
39. Couillin, I., Letourneur, F., Lefebvre, P., Guillet, J.G., and Martinon, F. 2001. DNA vaccination of macaques with several different Nef sequences induces multispecific T cell responses. Virology. 279:136-145.
40. Sutherland, H.J., Lansdorp, P.M., Henkelman, D.H., Eaves, A.C., and Eaves, C.J. 1990. Functional characterization of individual human hematopoietic stem cells cultured at limiting dilution on supportive marrow stromal layers. Proc. Natl. Acad. Sci. U. S. A. 87:3584-3588.
41. Lehrke, M., and Lazar, M.A. 2005. The many faces of PPARgamma. Cell. 123:993-999.
42. Otake, K., et al. 2004. HIV-1 Nef protein in the nucleus influences adipogenesis as well as viral transcription through the peroxisome proliferator-activated receptors. AIDS. 18:189-198.
43. Hoelbl, A., et al. 2006. Clarifying the role of Stat5 in lymphoid development and Abelson-induced transformation. Blood. 107:4898-4906.
44. Schuringa, J.J., Wu, K., Morrone, G., and Moore, M.A. 2004. Enforced activation of STAT5A facilitates the generation of embryonic stem-derived hematopoietic stem cells that contribute to hematopoiesis in vivo. Stem Cells. 22:1191-1204.
45. Bunting, K.D., et al. 2002. Reduced lymphomyeloid repopulating activity from adult bone marrow and fetal liver of mice lacking expression of STAT5. Blood. 99:479-487.
46. Snow, J.W., et al. 2002. STAT5 promotes multilineage hematolymphoid development in vivo through effects on early hematopoietic progenitor cells. Blood. 99:95-101.
47. Kryworuchko, M., et al. 2004. Defective interleukin-2-dependent STAT5 signalling in CD8 T lymphocytes from HIV-positive patients: restoration by antiretroviral therapy. AIDS. 18:421-426.
48. Pericle, F., et al. 1998. HIV-1 infection induces a selective reduction in STAT5 protein expression. J. Immunol. 160:28-31.
49. Geleziunas, R., Xu, W., Takeda, K., Ichijo, H., and Greene, W.C. 2001. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature. 410:834-838.
50. Qiao, X., et al. 2006. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat. Immunol. 7:302-310.
51. Alessandrini, L., et al. 2000. T-tropic human immunodeficiency virus (HIV) type 1 Nef protein enters human monocyte-macrophages and induces resistance to HIV replication: a possible mechanism of HIV T-tropic emergence in AIDS. J. Gen. Virol. 81:2905-2917.
52. Mangino, G., et al. 2007. In vitro treatment of human monocytes/macrophages with myristoylated recombinant Nef of human immunodeficiency virus type 1 leads to the activation of mitogen-activated protein kinases, IkappaB kinases, and interferon regulatory factor 3 and to the release of beta interferon. J. Virol. 81:2777-2791.
53. Olivetta, E., et al. 2003. HIV-1 Nef induces the release of inflammatory factors from human monocyte/ macrophages: involvement of Nef endocytotic signals and NF-kappa B activation. J. Immunol. 170:1716-1727.
54. Varin, A., et al. 2003. Exogenous Nef protein activates NF-kappa B, AP-1, and c-Jun N-terminal kinase and stimulates HIV transcription in promonocytic cells. Role in AIDS pathogenesis. J. Biol. Chem. 278:2219-2227.
55. Olsen, H., and Haldosen, L.A. 2006. Peroxisome proliferator-activated receptor gamma regulates expression of signal transducer and activator of transcription 5A. Exp. Cell Res. 312:1371-1380.
56. Nagasawa, E., et al. 2005. Pivotal role of peroxisome proliferator-activated receptor gamma (PPARgamma) in regulation of erythroid progenitor cell proliferation and differentiation. Exp. Hematol. 33:857-864.
57. Berria, R., et al. 2007. Reduction in hematocrit and hemoglobin following pioglitazone treatment is not hemodilutional in type II diabetes mellitus. Clin. Pharmacol. Ther. 82:275-281.
58. Wang, T., Xu, J., Yu, X., Yang, R., and Han, Z.C. 2005. Peroxisome proliferator-activated receptor gamma in malignant diseases. Crit. Rev. Oncol. Hematol. 58:1-14.
59. Geyer, M., and Peterlin, B.M. 2001. Domain assembly, surface accessibility and sequence conservation in full length HIV-1 Nef. FEBS Lett. 496:91-95.
60. Hofmann-Lehmann, R., et al. 2000. Sensitive and robust one-tube real-time reverse transcriptase-polymerase chain reaction to quantify SIV RNA load: comparison of one- versus two-enzyme systems. AIDS Res. Hum. Retroviruses. 16:1247-1257.
61. Hottinger, A.F., Azzouz, M., Deglon, N., Aebischer, P., and Zurn, A.D. 2000. Complete and long-term rescue of lesioned adult motoneurons by lentiviral-mediated expression of glial cell line-derived neurotrophic factor in the facial nucleus. J. Neurosci. 20:5587-5593.