SMAD proteins of oligodendroglial cells regulate transcription of JC virus early and late genes coordinately with the Tat protein of human immunodeficiency virus type 1

Journal of General Virology

Volumn 90, Issue 8, 2009, Pages 2005-2014

  Stettner, Michelle R ^a   Nance, Jonas A ^a   Wright, Clayton A ^a   Kinoshita, Yayoi ^b   Kim, Woong Kim ^a   Morgello, Susan ^b   Rappaport, Jay ^c   Khalili, Kamel ^c   Gordon, Jennifer ^c   Johnson, Edward M ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSACTIVATOR PROTEIN; VIRUS DNA;

ARTICLE; CELL STIMULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA REPLICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; JC VIRUS; NONHUMAN; OLIGODENDROGLIA; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; VIRUS TRANSCRIPTION; BRAIN; CELL LINE; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; JC POLYOMAVIRUS;

BRAIN; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DNA, VIRAL; GENE EXPRESSION REGULATION, VIRAL; HIV-1; HUMANS; JC VIRUS; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; OLIGODENDROGLIA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SMAD PROTEINS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC;

EID: 69449104035     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.011072-0     Document Type: Article

References (56)

1. Banks, W. A., Robinson, S. M. & Nath, A. (2005). Permeability of the blood-brain barrier to HIV-1 Tat. Exp Neurol 193, 218-227.
2. Barr, S. M. & Johnson, E. M. (2001). Ras-induced colony formation and anchorage-independent growth inhibited by elevated expression of Purα in NIH3T3 cells. J Cell Biochem 81, 621-638.
3. Bergemann, A. D., Ma, Z.-W. & Johnson, E. M. (1992). Sequence of cDNA comprising the human pur gene and sequence-specific single-stranded-DNA-binding properties of the encoded protein. Mol Cell Biol 12, 5673-5682.
4. Bottner, M., Krieglstein, K. & Unsicker, K. (2000). The transforming growth factor-βs: structure, signaling, and roles in nervous system development and functions. J Neurochem 75, 2227-2240.
5. Chepenik, L. G., Tretiakova, A. P., Krachmarov, C. P., Johnson, E. M. & Khalili, K. (1998). The single-stranded DNA binding protein, Pur-α, binds HIV-1 TAR RNA and activates HIV-1 transcription. Gene 210, 37-44.
6. Chowdhury, M., Taylor, J. P., Tada, H., Rappaport, J., Wong-Staal, F., Amini, S. & Khalili, K. (1990). Regulation of the human neurotropic virus promoter by JCV-T antigen and HIV-1 Tat protein. Oncogene 5, 1737-1742.
7. Chowdhury, M., Taylor, J. P., Chang, C. F., Rappaport, J. & Khalili, K. (1992). Evidence that a sequence similar to TAR is important for induction of the JC virus late promoter by human immunodeficiency virus type 1 Tat. J Virol 66, 7355-7361.
8. Cinque, P., Koralnik, I. J. & Clifford, D. B. (2003). The evolving face of human immunodeficiency virus-related progressive multifocal leukoencephalopathy: defining a consensus terminology. J Neurovirol 9 (Suppl. 1), 88-92.
9. Conant, K., Ma, M., Nath, A. & Major, E. O. (1996). Extracellular human immunodeficiency virus type 1 Tat protein is associated with an increase in both NF-κB binding and protein kinase C activity in primary human astrocytes. J Virol 70, 1384-1389.
10. Cupp, C., Taylor, J. P., Khalili, K. & Amini, S. (1993). Evidence for stimulation of the transforming growth factor β1 promoter by HIV-1 Tat in cells derived from CNS. Oncogene 8, 2231-2236.
11. Daniel, D. C., Wortman, M. J., Schiller, R. J., Liu, H., Gan, L., Mellen, J. S., Chang, C. F., Gallia, G. L., Rappaport, J. & other authors (2001). Coordinate effects of human immunodeficiency virus type 1 protein Tat and cellular protein Purα on DNA replication initiated at the JC virus origin. J Gen Virol 82, 1543-1553.
12. Daniel, D. C., Kinoshita, Y., Khan, M. A., Del Valle, L., Khalili, K., Rappaport, J. & Johnson, E. M. (2004). Internalization of exogenous human immunodeficiency virus-1 protein, Tat, by KG-1 oligodendroglioma cells followed by stimulation of DNA replication initiated at the JC virus origin. DNA Cell Biol 23, 858-867.
13. Darbinian, N., Gallia, G. L. & Khalili, K. (2001a). Helix-destabilizing properties of the human single-stranded DNA- and RNA-binding protein Purα. J Cell Biochem 80, 589-595.
14. Derynck, R., Zhang, Y. & Feng, X. H. (1998). Smads: transcriptional activators of TGF-β responses. Cell 95, 737-740.
15. Dingwall, C., Ernberg, I., Gait, M. J., Green, S. M., Heaphy, S., Karn, J., Lowe, A. D., Singh, M. & Skinner, M. A. (1990). HIV-1 tat protein stimulates transcription by binding to a U-rich bulge in the stem of the TAR RNA structure. EMBO J 9, 4145-4153.
16. Enam, S., Sweet, T. M., Amini, S., Khalili, K. & Del Valle, L. (2004). Evidence for involvement of transforming growth factor β1 signaling pathway in activation of JC virus in human immunodeficiency virus 1-associated progressive multifocal leukoencephalopathy. Arch Pathol Lab Med 128, 282-291.
17. Ensoli, B., Barillari, G., Salahuddin, S. Z., Gallo, R. C. & Wong-Staal, F. (1990). Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 345, 84-86.
18. 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 in cell growth and viral transactivation. J Virol 67, 277-287.
19. Ezhevsky, S. A., Nagahara, H., Vocero-Akbani, A.M., Gius, D. R., Wei, M. C. & Dowdy, S. F. (1997). Hypo-phosphorylation of the retinoblastoma protein (pRb) by cyclin D:Cdk4/6 complexes results in active pRb. Proc Natl Acad Sci U S A 94, 10699-10704.
20. Feng, X. H. & Derynck, R. (2005). Specificity and versatility in TGF-β signaling through Smads. Annu Rev Cell Dev Biol 21, 659-693.
21. Frankel, A. D. & Pabo, C. O. (1988). Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55, 1189-1193.
22. Fujinaga, K., Taube, R., Wimmer, J., Cujec, T. P. & Peterlin, B. M. (1999). Interactions between human cyclin T, Tat, and the transactivation response element (TAR) are disrupted by a cysteine to tyrosine substitution found in mouse cyclin T. Proc Natl Acad Sci U S A 96, 1285-1290.
23. Gallia, G. L., Safak, M. & Khalili, K. (1998). Interaction of the single-stranded DNA-binding protein Purα with the human polyomavirus JC virus early protein T-antigen. J Biol Chem 273, 32662-32669.
24. Gallia, G. L., Darbinian, N., Tretiakova, A., Ansari, S. A., Rappaport, J., Brady, J., Wortman, M. J., Johnson, E. M. & Khalili, K. (1999). Association of HIV-1 Tat with the cellular protein, Purα, is mediated by RNA. Proc Natl Acad Sci U S A 96, 11572-11577.
25. Gallia, G. L., Johnson, E. M. & Khalili, K. (2000). Purα: a multifunctional single-stranded DNA- and RNA-binding protein. Nucleic Acids Res 28, 3197-3205.
26. Garber, M. E., Wei, P. & Jones, K. A. (1998a). HIV-1 Tat interacts with cyclin T1 to direct the P-TEFb CTD kinase complex to TAR RNA. Cold Spring Harb Symp Quant Biol 63, 371-380.
27. Garber, M. E., Wei, P., KewalRamani, V. N., Mayall, T. P., Herrmann, C. H., Rice, A. P., Littman, D. R. & Jones, K. A. (1998b). The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev 12, 3512-3527.
28. Gold, M. O., Yang, X., Herrmann, C. H. & Rice, A. P. (1998). PITALRE, the catalytic subunit of TAK, is required for human immunodeficiency virus Tat transactivation in vivo. J Virol 72, 4448-4453.
29. Haas, S., Thatikunta, P., Steplewski, A., Johnson, E. M., Khalili, K. & Amini, S. (1995). A 39-kD DNA-binding protein from mouse brain stimulates transcription of myelin basic protein gene in oligodendrocytic cells. J Cell Biol 130, 1171-1179.
30. Itoh, H., Wortman, M. J., Kanovsky, M., Uson, R.R., Gordon, R.E., Alfano, N. & Johnson, E. M. (1998). Alterations in Purα levels and intracellular localization in the CV-1 cell cycle. Cell Growth Differ 9, 651-665.
31. Johnson, E. M. (2003). The Pur protein family: clues to function from recent studies on cancer and AIDS. Anticancer Res 23, 2093-2100.
32. Johnson, E. M., Kinoshita, Y.,Weinreb, D. B., Wortman, M. J., Simon, R., Khalili, K., Winckler, B. & Gordon, J. (2006). Role of Purα in targeting mRNA to sites of translation in hippocampal neuronal dendrites. J Neurosci Res 83, 929-943.
33. Karn, J. (1991). Control of human immunodeficiency virus replication by the tat, rev, nef and protease genes. Curr Opin Immunol 3, 526-536.
34. Kinoshita, Y. & Johnson, E. M. (2004). Site-specific loading of an MCM protein complex in a DNA replication initiation zone upstream of the c-MYC gene in the HeLa cell cycle. J Biol Chem 279, 35879-35889.
35. Krachmarov, C. P., Chepenik, L. G., Barr-Vagell, S., Khalili, K. & Johnson, E. M. (1996). Activation of the JC virus Tat-responsive transcriptional control element by association of the Tat protein of human immunodeficiency virus 1 with cellular protein Purα. Proc Natl Acad Sci U S A 93, 14112-14117.
36. Liu, H., Barr, S. M., Chu, C., Kohtz, D. S., Kinoshita, Y. & Johnson, E. M. (2005). Functional interaction of Purα with the Cdk2 moiety of cyclin A/Cdk2. Biochem Biophys Res Commun 328, 851-857.
37. Ma, M. & Nath, A. (1997). Molecular determinants for cellular uptake of Tat protein of human immunodeficiency virus type 1 in brain cells. J Virol 71, 2495-2499.
38. Marzocchetti, A., Wuthrich, C., Tan, C. S., Tompkins, T., Bernal-Cano, F., Bhargava, P., Ropper, A. H. & Koralnik, I. J. (2008). Rearrangement of the JC virus regulatory region sequence in the bone marrow of a patient with rheumatoid arthritis and progressive multifocal leukoencephalopathy. J Neurovirol 14, 455-458.
39. McKinnon, R. D., Piras, G., Ida, J. A., Jr & Dubois-Dalcq, M. (1993). A role for TGF-β in oligodendrocyte differentiation. J Cell Biol 121, 1397-1407.
40. Rasty, S., Thatikunta, P., Gordon, J., Khalili, K., Amini, S. & Glorioso, J. C. (1996). Human immunodeficiency virus tat gene transfer to the murine central nervous system using a replication-defective herpes simplex virus vector stimulates transforming growth factor β1 gene expression. Proc Natl Acad Sci U S A 93, 6073-6078.
41. Reinhold, D., Wrenger, S., Kahne, T. & Ansorge, S. (1999). HIV-1 Tat: immunosuppression via TGF-β1 induction. Immunol Today 20, 384-385.
42. Rice, A. P. & Mathews, M. B. (1988). Transcriptional but not translational regulation of HIV-1 by the tat gene product. Nature 332, 551-553.
43. Romano, G., Kasten, M., De Falco, G., Micheli, P., Khalili, K. & Giordano, A. (1999). Regulatory functions of Cdk9 and of cyclin T1 in HIV Tat transactivation pathway gene expression. J Cell Biochem 75, 357-368.
44. Ross, S., Cheung, E., Petrakis, T. G., Howell, M., Kraus, W. L. & Hill, C. S. (2006). Smads orchestrate specific histone modifications and chromatin remodeling to activate transcription. EMBO J 25, 4490-4502.
45. Sadaie, M. R., Benter, T. & Wong-Staal, F. (1988). Site-directed mutagenesis of two trans-regulatory genes (tat-III,trs) of HIV-1. Science 239, 910-913.
46. Sawaya, B. E., Thatikunta, P., Denisova, L., Brady, J., Khalili, K. & Amini, S. (1998). Regulation of TNFα and TGFβ-1 gene transcription by HIV-1 Tat in CNS cells. J Neuroimmunol 87, 33-42.
47. Schmierer, B. & Hill, C. S. (2007). TGFβ-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8, 970-982.
48. Schuster, N., Bender, H., Philippi, A., Subramaniam, S., Strelau, J., Wang, Z. & Krieglstein, K. (2002). TGF-β induces cell death in the oligodendroglial cell line OLI-neu. Glia 40, 95-108.
49. Shi, Y. & Massague, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700.
50. Silvestri, C., Narimatsu, M., von Both, I., Liu, Y., Tan, N. B., Izzi, L., McCaffery, P., Wrana, J. L. & Attisano, L. (2008). Genome-wide identification of Smad/Foxh1 targets reveals a role for Foxh1 in retinoic acid regulation and forebrain development. Dev Cell 14, 411-423.
51. Tanaka, N., Nagao, S., Tohgo, A., Sekiguchi, F., Kohno, M., Ogawa, H., Matsui, T. & Matsutani, M. (1983). Effects of human fibroblast interferon on human gliomas transplanted into nude mice. Gann 74, 308-316.
52. Thatikunta, P., Sawaya, B. E., Denisova, L., Cole, C., Yusibova, G., Johnson, E. M., Khalili, K. & Amini, S. (1997). Identification of a cellular protein that binds to Tat-responsive element of TGF β-1 promoter in glial cells. J Cell Biochem 67, 466-477.
53. 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.
54. Wortman, M. J., Krachmarov, C. P., Kim, J. H., Gordon, R. G., Chepenik, L. G., Brady, N. N., Gallia, G. L., Khalili, K. & Johnson, E. M. (2000). Interaction of HIV-Tat with Pur-α in nuclei of human glial cells: characterization of RNA-mediated protein-protein binding. J Cell Biochem 77, 65-74.
55. Wortman, M. J., Johnson, E. M. & Bergemann, A. D. (2005). Mechanism of DNA binding and localized strand separation by Purα and comparison with Pur family member, Purβ. Biochim Biophys Acta 1743, 64-78.
56. Zhang, Y., Feng, X., We, R. & Derynck, R. (1996). Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383, 168-172.