HIV-1 TAT represses transcription of the bone morphogenic protein receptor-2 in U937 monocytic cells

Journal of Leukocyte Biology

Volumn 79, Issue 1, 2006, Pages 192-201

  Caldwell, Robert L ^a,b,c   Gadipatti, Radhika ^a   Lane, Kirk B ^a   Shepherd, Virginia L ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

AIDS; Cell surface molecules; Gene regulation; Lung; Monocytes macrophages

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; SMAD6 PROTEIN; TRANSACTIVATOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN U937; CELL TYPE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE IDENTIFICATION; GENE MUTATION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; MACROPHAGE ACTIVATION; MONOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PULMONARY HYPERTENSION; TARGET CELL; TRANSCRIPTION REGULATION;

BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; DOWN-REGULATION; ENDOTHELIAL CELLS; GENE PRODUCTS, TAT; HIV INFECTIONS; HIV-1; HUMANS; HYPERTENSION, PULMONARY; LECTINS, C-TYPE; MACROPHAGES; MANNOSE-BINDING LECTINS; MUTATION; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, CELL SURFACE; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SMAD6 PROTEIN; U937 CELLS;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 30144435554     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0405194     Document Type: Article

References (76)

1. Jeang, K. T., Chang, Y., Berkhout, B., Hammarskjold, M. L., Rekosh, D. (1991) Regulation of HIV expression: mechanisms of action of Tat and Rev. AIDS 5 (Suppl. 2), S3-14.
2. Jones, K. A., Peterlin, B. M. (1994) Control of RNA initiation and elongation at the HIV-1 promoter. Annu. Rev. Biochem. 63, 717-743.
3. Kanazawa, S., Okamoto, T., Peterlin, B. M. (2000) Tat competes with CHTA for the binding to P-TEFb and blocks the expression of MHC class II genes in HIV infection. Immunity 12, 61-70.
4. Darbinian, N., Sawaya, B. E., Khalili, K., Jaffe, N., Wortman, B., Giordano, A., Amini, S. (2001) Functional interaction between cyclin T1/cdk9 and Pura determines the level of TNFa promoter activation by Tat in glial cells. J. Neuroimmunol. 121, 3-11.
5. Karn, J. (1999) Tackling Tat. J. Mol. Biol. 293, 235-254.
6. Frankel, A. D., Pabo, C. O. (1988) Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55, 1189-1193.
7. Subramanyam, M., Gutheil, W. G., Bachovchin, W. W., Huber, B. T. (1993) Mechanism of HIV-1 Tat induced inhibition of antigen-specific T cell responsiveness. J. Immunol. 150, 2544-2553.
8. Conaldi, P. G., Bottelli, A., Baj, A., Serra, C., Fiore, L., Federico, G., Bussolati, B., Camussi, G. (2002) Human immunodeficiency virus-1 Tat induces hyperproliferation and dysregulation of renal glomerular epithelial cells. Am. J. Pathol. 161, 53-61.
9. Zauli, G., Gibellini, D., Celeghini, C., Mischiati, C., Bassini, A., La Placa, M., Capitani, S. (1996) Pleiotropic effects of immobilized versus soluble recombinant HIV-1 Tat protein on CD3-mediated activation, induction of apoptosis, and HIV-1 long terminal repeat transactivation in purified CD4+ T lymphocytes. J. Immunol. 157, 2216-2224.
10. Chen, P., Mayne, M., Power, C., Nath, A. (1997) The Tat protein of HIV-1 induces tumor necrosis factor-α production. Implications for HIV-1-associated neurological diseases. J. Biol. Chem. 272, 22385-22388.
11. Ito, M., Ishida, T., He, L., Tanabe, F., Rongge, Y., Miyakawa, Y., Terunuma, H. (1998) HIV type 1 Tat protein inhibits interleukin 12 production by human peripheral blood mononuclear cells. AIDS Res. Hum. Retroviruses 14, 845-849.
12. Nath, A., Conant, K., Chen, P., Scott, C., Major, E. O. (1999) Transient exposure to HIV-1 Tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon. J. Biol. Chem. 274, 17098-17102.
13. Weiss, J. M., Nath, A., Major, E. O., Berman, J. W. (1999) HIV-1 Tat induces monocyte chemoattractant protein-1-mediated monocyte transmigration across a model of the human blood-brain barrier and up-regulates CCR5 expression on human monocytes. J. Immunol. 163, 2953-2959.
14. Secchiero, P., Zella, D., Capitani, S., Gallo, R. C., Zauli, G. (1999) Extracellular HIV-1 Tat protein up-regulates the expression of surface CXC-chemokine receptor 4 in resting CD4+ T cells. J. Immunol. 162, 2427-2431.
15. Vene, R., Benelli, R., Noonan, D. M., Albini, A. (2000) HIV-Tat-dependent chemotaxis and invasion, key aspects of Tat-mediated pathogenesis. Clin. Exp. Metastasis 18, 533-538.
16. Park, I. W., Ullrich, C. K., Schoenberger, E., Ganju, R. K., Groopman, J. E. (2001) HIV-1 Tat induces microvascular endothelial apoptosis through caspase activation. J. Immunol. 167, 2766-2771.
17. Park, I. W., Wang, J. F., Groopman, J. E. (2001) HIV-1 Tat promotes monocyte chemoattractant protein-1 secretion followed by transmigration of monocytes. Blood 97, 352-358.
18. Stahl, P. D., Ezekowitz, R. A. (1998) The mannose receptor is a pattern recognition receptor involved in host defense. Curr. Opin. Immunol. 10, 50-55.
19. Caldwell, R. L., Egan, B. S., Shepherd, V. L. (2000) HIV-1 Tat represses transcription from the mannose receptor promoter. J. Immunol. 165, 7035-7041.
20. Lane, K. B., Machado, R. D., Pauciulo, M. W., Thomson, J. R., Phillips III, J. A., Loyd, J. E., Nichols, W. C., Trembath, R. C. (2000) Heterozygous germline mutations in BMPR2, encoding a TGF-β receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat. Genet. 26, 81-84.
21. Machado, R. D., Pauciulo, M. W., Thomson, J. R., Lane, K. B., Morgan, N. V., Wheeler, L., Phillips III, J. A., Newman, J., Williams, D., Galie, N., Manes, A., McNeil, K., Yacoub, M., Mikhail, G., Rogers, P., Corns, P., Humbert, M., Donnai, D., Martensson, G., Tranebjaerg, L., Loyd, J. E., Trembath, R. C., Nichols, W. C. (2001) BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am. J. Hum. Genet. 68, 92-102.
22. Deng, Z., Morse, J. H., Slager, S. L., Cuervo, N., Moore, K. J., Venetos, G., Kalachikov, S., Cayanis, E., Fischer, S. G., Barst, R. J., Hodge, S. E., Knowles, J. A. (2000) Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am. J. Hum. Genet, 67, 737-744.
23. Hogan, B. L. (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
24. Balemans, W., Van Hul, W. (2002) Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol, 250, 231-250.
25. Tsuneizumi, K., Nakayama, T., Kamoshida, Y., Kornberg, T. B., Christian, J. L., Tabata, T. (1997) Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 389, 627-631.
26. Wozney, J. M., Rosen, V., Celeste, A. J., Mitsock, L. M., Whitters, M. J., Kriz, R. W., Hewick, R. M., Wang, E. A. (1988) Novel regulators of bone formation: molecular clones and activities. Science 242, 1528-1534.
27. Morrell, N. W., Yang, X., Upton, P. D., Jourdan, K. B., Morgan, N., Sheares, K. K., Trembath, R. C. (2001) Altered growth responses of pulmonary artery smooth muscle cells from patients with primary pulmonary hypertension to transforming growth factor-β(1) and bone morphogenetic proteins. Circulation 104, 790-795.
28. Chikazu, D., Li, X., Kawaguchi, H., Sakuma, Y., Voznesensky, O. S., Adams, D. J., Xu, M., Hoshio, K., Katavic, V., Herschman, H. R., Raisz, L. G., Pilbeam, C. C. (2002) Bone morphogenetic protein 2 induces cyclo-oxygenase 2 in osteoblasts via a Cbfal-binding site: role in effects of bone morphogenetic protein 2 in vitro and in vivo. J. Bone Miner. Res. 17, 1430-1440.
29. Olschewski, H., Rose, F., Grunig, E., Ghofrani, H. A., Walmrath, D., Schulz, R., Schermuly, R., Grimminger, F., Seeger, W. (2001) Cellular pathophysiology and therapy of pulmonary hypertension. J. Lab. Clin. Med. 138, 367-377.
30. Adatia, I. (2002) Recent advances in pulmonary vascular disease. Curr. Opin, Pediatr. 14, 292-297.
31. Petrosillo, N., Pefficelli, A. M., Boumis, E., Ippolito, G. (2001) Clinical manifestation of HIV-related pulmonary hypertension. Ann. N. Y. Acad. Sci. 946, 223-235.
32. Opravil, M., Pechere, M., Speich, R., Joller-Jemelka, H. I., Jenni, R., Russi, E. W., Hirschel, B., Luthy, R. (1997) HIV-associated primary pulmonary hypertension. A case control study. Swiss HIV Cohort Study, Am. J. Respir. Crit. Care Med. 155, 990-995.
33. Frankel, A. D., Young, J. A. (1998) HIV-1: fifteen proteins and an RNA. Annu. Rev. Biochem. 67, 1-25.
34. Massague, J., Chen, Y. G. (2000) Controlling TGF-β signaling. Genes Dev. 14, 627-644.
35. von Bubnoff, A., Cho, K. W. (2001) Intracellular BMP signaling regulation in vertebrates: pathway or network? Dev, Biol. 239, 1-14.
36. Lagna, G., Hata, A., Hemmati-Brivanlou, A., Massague, J. (1996) Partnership between DPC4 and SMAD proteins in TGF-β signaling pathways. Nature 383, 832-836.
37. Liu, F., Hata, A., Baker, J. C., Doody, J., Carcamo, J., Harland, R. M., Massague, J. (19%) A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381, 620-623.
38. Zhang, Y., Feng, X., We, R., Derynck, R. (1996) Receptor-associated Mad homologues synergize as effectors of the TGF- response. Nature 383, 168-172.
39. Zhang, Y., Musci, T., Derynck, R. (1997) The tumor suppressor Smad4/DPC 4 as a central mediator of Smad function. Curr. Biol. 7, 270-276.
40. Imamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J., Kawabata, M., Miyazono, K. (1997) Smad6 inhibits signalling by the TGF-β superfamily. Nature 389, 622-626.
41. Inoue, H., Imamura, T., Ishidou, Y., Takase, M., Udagawa, Y., Oka, Y., Tsuneizumi, K., Tabata, T., Miyazono, K., Kawabata, M. (1998) Interplay of signal mediators of decapentaplegic (Dpp): molecular characterization of mothers against dpp, Medea, and daughters against dpp. Mol. Biol. Cell 9, 2145-2156.
42. Hata, A., Lagna, G., Massague, J., Hemmati-Brivanlou, A. (1998) Smad6 inhibits BMP/Smadl signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev. 12, 186-197.
43. Nishimura, R., Kato, Y., Chen, D., Harris, S. E., Mundy, G. R., Yoneda, T. (1998) Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J. Biol Chem. 273, 1872-1879.
44. Ishida, W., Hamamoto, T., Kusanagi, K., Yagi, K., Kawabata, M., Takehara, K., Sampath, T. K., Kato, M., Miyazono, K. (2000) Smad6 is a Smad1/5-induced smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter. J. Biol. Chem. 275, 6075-6079.
45. Carroll, I. R., Wang, J., Howcroft, T. K., Singer, D. S. (1998) HIV Tat represses transcription of the β 2-microglobulin promoter. Mol. Immunol. 35, 1171-1178.
46. Verhoef, K., Bauer, M., Meyerhans, A., Berkhout, B. (1998) On the role of the second coding exon of the HIV-1 Tat protein in virus replication and MHC class I downregulation. AIDS Res. Hum. Retroviruses 14, 1553-1559.
47. Howcroft, T. K., Palmer, L. A., Brown, J., Rellahan, B., Kashanchi, F., Brady, J. N., Singer, D. S. (1995) HIV Tat represses transcription through Sp1-like elements in the basal promoter. Immunity 3, 127-138.
48. Weissman, J. D., Brown, J. A., Howcroft, T. K., Hwang, J., Chawla, A., Roche, P. A., Schiltz, L., Nakatani, Y., Singer, D. S. (1998) HIV-1 Tat binds TAFH250 and represses TAFH250-dependent transcription of major histocompatibility class I genes. Proc. Natl. Acad. Sci. USA 95, 11601-11606.
49. Howcroft, T. K., Strebel, K., Martin, M. A., Singer, D. S. (1993) Repression of MHC class I gene promoter activity by two-exon Tat of HIV. Science 260, 1320-1322.
50. Rudarakanchana, N., Flanagan, J. A., Chen, H., Upton, P. D., Machado, R., Patel, D., Trembath, R. C., Morrell, N. W. (2002) Functional analysis of bone morphogenetic protein type II receptor mutations underlying primary pulmonary hypertension. Hum. Mol. Genet. 11, 1517-1525.
51. Kretzschmar, M., Liu, F., Hata, A., Doody, J., Massague, J. (1997) The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev, 11, 984-995.
52. Korchynskyi, O., ten Dijke, P. (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Idl promoter. J. Biol, Chem. 277, 4883-4891.
53. Zhang, M., Li, X., Pang, X., Ding, L., Wood, O., Clouse, K. A., Hewlett, I., Dayton, A. I. (2002) Bcl-2 upregulation by HIV-1 Tat during infection of primary human macrophages in culture. J. Biomed. Sci. 9, 133-139.
54. Mangasarian, A., Trono, D. (1997) The multifaceted role of HIV Nef. Res. Virol 148, 30-33.
55. Le Gall, S., Heard, J. M., Schwartz, O. (1997) Analysis of Nef-induced MHC-I endocytosis. Res. Virol. 148, 43-47.
56. De Caestecker, M., Meyrick, B. (2001) Bone morphogenetic proteins, genetics and the pathophysiology of primary pulmonary hypertension. Respir. Res. 2, 193-197.
57. Bellusci, S., Henderson, R., Winnier, G., Oikawa, T., Hogan, B. L. (1996) Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122, 1693-1702.
58. Miyazono, K., Kusanagi, K., Inoue, H. (2001) Divergence and convergence of TGF-β/BMP signaling. J. Cell. Physiol. 187, 265-276.
59. Cujec, T. P., Cho, H., Maldonado, E., Meyer, J., Reinberg, D., Peterlin, B. M. (1997) The human immunodeficiency virus transactivator Tat interacts with the RNA polymerase II holoenzyme. Mol. Cell. Biol. 17, 1817-1823.
60. Mavankal, G., Ignatius Ou, S. H., Oliver, H., Sigman, D., Gaynor, R. B. (1996) Human immunodeficiency virus type 1 and 2 Tat proteins specifically interact with RNA polymerase H. Proc. Natl. Acad. Sci. USA 93, 2089-2094.
61. Chiang, C. M., Roeder, R. G. (1995) Cloning of an intrinsic human TFHD subunit that interacts with multiple transcriptional activators. Science 267, 531-536.
62. Blau, J., Xiao, H., McCracken, S., O'Hare, P., Greenblatt, J., Bentley, D. (1996) Three functional classes of transcriptional activation domain. Mol. Cell. Biol. 16, 2044-2055.
63. Cujec, T. P., Okamoto, H., Fujinaga, K., Meyer, J., Chamberlin, H., Morgan, D. O., Peterlin, B. M. (1997) The HIV transactivator TAT binds to the CDK-activating kinase and activates the phosphorylation of the carboxy-terminal domain of RNA polymerase H. Genes Dev. 11, 2645-2657.
64. Jeang, K. T., Chun, R., Lin, N. H., Gatignol, A., Glabe, C. G., Fan, H. (1993) In vitro and in vivo binding of human immunodeficiency virus type 1 Tat protein and SpI transcription factor. J. Virol 67, 6224-6233.
65. Macian, F., Rao, A. (1999) Reciprocal modulatory interaction between human immunodeficiency virus type 1 Tat and transcription factor NFAT1. Mol. Cell. Biol. 19, 3645-3653.
66. Wei, P., Garber, M. E., Fang, S. M., Fischer, W. H., Jones, K. A. (1998) A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92, 451-462.
67. Zauli, G., La Placa, M., Vignoli, M., Re, M. C., Gibellini, D., Furlini, G., Milani, D., Marchisio, M., Mazzoni, M., Capitani, S. (1995) An autocrine loop of HIV type-1 Tat protein responsible for the improved survival/ proliferation capacity of permanently Tat-transfected cells and required for optimal HIV-1 LTR transactivating activity. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 10, 306-316.
68. Ensoli, B., Buonaguro, L., Barillari, G., Fiorelli, V., Gendelman, R., Morgan, R. A., Wingfield, P., Gallo, R. C. (1993) Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J. Virol, 67, 277-287.
69. Ehret, Á., Li-Weber, M., Frank, R., Krammer, P. H. (2001) The effect of HIV-1 regulatory proteins on cellular genes: derepression of the IL-2 promoter by Tat. Eur. J. Immunol. 31, 1790-1799.
70. Sharma, V., Knobloch, T. J., Benjamin, D. (1995) Differential expression of cytokine genes in HIV-1 Tat-transfected T and B cell lines. Biochem. Biophys. Res. Commun. 208, 704-713.
71. Gibellini, D., Caputo, A., Capitani, S., La Placa, M., Zauli, G. (1997) Upregulation of c-Fos in activated T lymphoid and monocytic cells by human immunodeficiency virus-1 Tat protein. Blood 89, 1654-1664.
72. Willette, R. N., Gu, J. L., Lysko, P. G., Anderson, K. M., Minehart, H., Yue, T. (1999) BMP-2 gene expression and effects on human vascular smooth muscle cells. J. Vasc. Res. 36, 120-125.
73. Nakaoka, T., Gonda, K., Ogita, T., Otawara-Hamamoto, Y., Okabe, F., Kira, Y., Harii, K., Miyazono, K., Takuwa, Y., Fujita, T. (1997) Inhibition of rat vascular smooth muscle proliferation in vitro and in vivo by bone morphogenetic protein-2. J, Clin, Invest. 100, 2824-2832.
74. Shitara, Y., Yokozaki, H., Yasui, W., Takenoshita, S., Nagamachi, Y., Tahara, E. (1998) Mutation of the transforming growth factor-β type II receptor gene is a rare event in human sporadic gastric carcinomas. Int. J. Oncol. 12, 1061-1065.
75. Clark, K. J., Gary, N. R., Grace, A. A., Metcalfe, J. C. (2001) Microsatellite mutation of type II transforming growth factor-β receptor is rare in atherosclerotic plaques. Arterioscler. Thromb. Vasc. Biol. 21, 555-559.
76. Yeager, M. E., Halley, G. R., Golpon, H. A., Voelkel, N. F., Tuder, R. M. (2001) Microsatellite instability of endothelial cell growth and apoptosis genes within plexiform lesions in primary pulmonary hypertension. Circ. Res. 88, E2-E11.