1887

Journal of General Virology header logo

Volume 94, Issue 3

Effects of Tat proteins and Tat mutants of different human immunodeficiency virus type 1 clades on glial JC virus early and late gene transcription Free

Abstract

Polyomavirus JC (JCV) is the aetiological agent of progressive multifocal leukoencephalopathy (PML), a frequently fatal infection of the brain afflicting nearly 4 % of AIDS patients in the USA. Human immunodeficiency virus type 1 (HIV-1) Tat, acting together with cellular proteins at the JCV non-coding control region (NCCR), can stimulate JCV DNA transcription and replication. Tat in the brain is secreted by HIV-1-infected cells and incorporated by oligodendroglia, cells capable of infection by JCV. Thus far the effects of Tat on JCV have been studied primarily with protein encoded by the HIV-1 B clade most common in North America. Here, we determine the abilities of Tat from different HIV-1 clades to alter JCV early and late gene transcription and DNA replication initiated at the JCV origin. Tat from all clades tested stimulates both JCV early and late gene promoters, with clade B Tat being significantly most effective. Tat proteins from the HIV-1 clades display parallel patterns of differences in their effects on HIV-1 and JCV transcription, suggesting that Tat effects in both cases are mediated by the same cellular proteins. Clade B Tat is most effective at directing Smad mediators of tumour growth factor beta and cellular partner Purα to the NCCR. Tat proteins from all non-B clades inhibit initiation of JCV DNA replication. The effectiveness of HIV-1 clade B Tat at promoting JCV transcriptional and replicative processes highlights a need for further investigation to determine which molecular aspects of Tat from distinct HIV-1 substrains can contribute to the course of PML development in neuroAIDS.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.047902-0
2013-03-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/3/514.html?itemId=/content/journal/jgv/10.1099/vir.0.047902-0&mimeType=html&fmt=ahah

References

  1. Bachis A., Biggio F., Major E. O., Mocchetti I. 2009; M- and T-tropic HIVs promote apoptosis in rat neurons. J Neuroimmune Pharmacol 4:150–160 [View Article][PubMed]
     [Google Scholar]
  2. 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[PubMed]
     [Google Scholar]
  3. Berger J. R., Major E. O. 1999; Progressive multifocal leukoencephalopathy. Semin Neurol 19:193–200 [View Article][PubMed]
     [Google Scholar]
  4. Campbell G. R., Watkins J. D., Loret E. P., Spector S. A. 2011; Differential induction of rat neuronal excitotoxic cell death by human immunodeficiency virus type 1 clade B and C tat proteins. AIDS Res Hum Retroviruses 27:647–654 [View Article][PubMed]
     [Google Scholar]
  5. Chang C.-F., Tada H., Khalili K. 1994; The role of a pentanucleotide repeat sequence, AGGGAAGGGA, in the regulation of JC virus DNA replication. Gene 148:309–314 [View Article][PubMed]
     [Google Scholar]
  6. Chang C. F., Gallia G. L., Muralidharan V., Chen N. N., Zoltick P., Johnson E. M., Khalili K. 1996; Evidence that replication of human neurotropic JC virus DNA in glial cells is regulated by the sequence-specific single-stranded DNA-binding protein Pur α. J Virol 70:4150–4156[PubMed]
     [Google Scholar]
  7. Chen N. N., Chang C.-F., Gallia G. L., Kerr D. A., Johnson E. M., Krachmarov C. P., Barr S. M., Frisque R. J., Bollag B., Khalili K. 1995; Cooperative action of cellular proteins YB-1 and Pur α with the tumor antigen of the human JC polyomavirus determines their interaction with the viral lytic control element. Proc Natl Acad Sci U S A 92:1087–1091 [View Article][PubMed]
     [Google Scholar]
  8. 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 [View Article][PubMed]
     [Google Scholar]
  9. 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. 188–92[PubMed] [CrossRef]
     [Google Scholar]
  10. Clifford D. B. 1999; Opportunistic viral infections in the setting of human immunodeficiency virus. Semin Neurol 19:185–192 [View Article][PubMed]
     [Google Scholar]
  11. Daniel D. C., Johnson E. M. 1989; Selective initiation of replication at origin sequences of the rDNA molecule of Physarum polycephalum using synchronous plasmodial extracts. Nucleic Acids Res 17:8343–8362 [View Article][PubMed]
     [Google Scholar]
  12. 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[PubMed]
     [Google Scholar]
  13. Daniel D. C., Kinoshita Y., Khan M. A., Valle L. D., 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 [View Article][PubMed]
     [Google Scholar]
  14. 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[PubMed]
     [Google Scholar]
  15. Frankel A. D., Pabo C. O. 1988; Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55:1189–1193 [View Article][PubMed]
     [Google Scholar]
  16. Frankel A. D., Bredt D. S., Pabo C. O. 1988; Tat protein from human immunodeficiency virus forms a metal-linked dimer. Science 240:70–73 [View Article][PubMed]
     [Google Scholar]
  17. Frisque R. J., Bream G. L., Cannella M. T. 1984; Human polyomavirus JC virus genome. J Virol 51:458–469[PubMed]
     [Google Scholar]
  18. Gallia G. L., Safak M., Khalili K. 1998; Interaction of the single-stranded DNA-binding protein Puralpha with the human polyomavirus JC virus early protein T-antigen. J Biol Chem 273:32662–32669 [View Article][PubMed]
     [Google Scholar]
  19. 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 [View Article][PubMed]
     [Google Scholar]
  20. 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 [View Article][PubMed]
     [Google Scholar]
  21. Garber M. E., Wei P., Jones K. A. 1998; 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 [View Article][PubMed]
     [Google Scholar]
  22. Gurwell J. A., Nath A., Sun Q., Zhang J., Martin K. M., Chen Y., Hauser K. F. 2001; Synergistic neurotoxicity of opioids and human immunodeficiency virus-1 Tat protein in striatal neurons in vitro. Neuroscience 102:555–563 [View Article][PubMed]
     [Google Scholar]
  23. Heaton R. K., Clifford D. B., Franklin D. R. Jr, Woods S. P., Ake C., Vaida F., Ellis R. J., Letendre S. L., Marcotte T. D. other authors 2010; HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: charter study. Neurology 75:2087–2096 [View Article][PubMed]
     [Google Scholar]
  24. Heaton R. K., Franklin D. R., Ellis R. J., McCutchan J. A., Letendre S. L., Leblanc S., Corkran S. H., Duarte N. A., Clifford D. B. other authors 2011; HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17:3–16 [View Article][PubMed]
     [Google Scholar]
  25. Johnson E. M. 2003; The Pur protein family: clues to function from recent studies on cancer and AIDS. Anticancer Res 23:3A2093–2100[PubMed]
     [Google Scholar]
  26. Johnson E. M., Kinoshita Y., Weinreb D. B., Wortman M. J., Simon R., Khalili K., Winckler B., Gordon J. 2006; Role of Pur α in targeting mRNA to sites of translation in hippocampal neuronal dendrites. J Neurosci Res 83:929–943 [View Article][PubMed]
     [Google Scholar]
  27. Jones K. A. 1997; Taking a new TAK on tat transactivation. Genes Dev 11:2593–2599 [View Article][PubMed]
     [Google Scholar]
  28. Karn J. 1991; Control of human immunodeficiency virus replication by the tat, rev, nef and protease genes. Curr Opin Immunol 3:526–536 [View Article][PubMed]
     [Google Scholar]
  29. Kashanchi F., Khleif S. N., Duvall J. F., Sadaie M. R., Radonovich M. F., Cho M., Martin M. A., Chen S. Y., Weinmann R., Brady J. N. 1996; Interaction of human immunodeficiency virus type 1 Tat with a unique site of TFIID inhibits negative cofactor Dr1 and stabilizes the TFIID-TFIIA complex. J Virol 70:5503–5510[PubMed]
     [Google Scholar]
  30. Khalili K., Del Valle L., Muralidharan V., Gault W. J., Darbinian N., Otte J., Meier E., Johnson E. M., Daniel D. C. other authors 2003; Purα is essential for postnatal brain development and developmentally coupled cellular proliferation as revealed by genetic inactivation in the mouse. Mol Cell Biol 23:6857–6875 [View Article][PubMed]
     [Google Scholar]
  31. Khalili K., Gordon J., White M. K. 2006; The polyomavirus, JCV and its involvement in human disease. Adv Exp Med Biol 577:274–287 [View Article][PubMed]
     [Google Scholar]
  32. 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 [View Article][PubMed]
     [Google Scholar]
  33. 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 Pur α. Proc Natl Acad Sci U S A 93:14112–14117 [View Article][PubMed]
     [Google Scholar]
  34. Liner K. J. II, Hall C. D., Robertson K. R. 2007; Impact of human immunodeficiency virus (HIV) subtypes on HIV-associated neurological disease. J Neurovirol 13:291–304 [View Article][PubMed]
     [Google Scholar]
  35. Major E. O., Amemiya K., Tornatore C. S., Houff S. A., Berger J. R. 1992; Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin Microbiol Rev 5:49–73[PubMed]
     [Google Scholar]
  36. Mancebo H. S., Lee G., Flygare J., Tomassini J., Luu P., Zhu Y., Peng J., Blau C., Hazuda D. other authors 1997; P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev 11:2633–2644 [View Article][PubMed]
     [Google Scholar]
  37. Padgett B. L., Zurhein G. M., Walker D. L., Eckroade R. J., Dessel B. H. 1971; Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 297:1257–1260 [View Article][PubMed]
     [Google Scholar]
  38. Price R. W. 1996; Neurological complications of HIV infection. Lancet 348:445–452 [View Article][PubMed]
     [Google Scholar]
  39. Rahimi R. A., Leof E. B. 2007; TGF-β signaling: a tale of two responses. J Cell Biochem 102:593–608 [View Article][PubMed]
     [Google Scholar]
  40. Robertson K. R., Hall C. D. 2007; Assessment of neuroAIDS in the international setting. J Neuroimmune Pharmacol 2:105–111 [View Article][PubMed]
     [Google Scholar]
  41. Robertson K., Liner J., Hakim J., Sankalé J. L., Grant I., Letendre S., Clifford D., Diop A. G., Jaye A. other authors 2010; NeuroAIDS in Africa. J Neurovirol 16:189–202 [View Article][PubMed]
     [Google Scholar]
  42. Rotta I., Almeida S. M. 2011; Genotypical diversity of HIV clades and central nervous system impairment. Arq Neuropsiquiatr 69:964–972 [View Article][PubMed]
     [Google Scholar]
  43. Ruben S., Perkins A., Purcell R., Joung K., Sia R., Burghoff R., Haseltine W. A., Rosen C. A. 1989; Structural and functional characterization of human immunodeficiency virus Tat protein. J Virol 63:1–8[PubMed]
     [Google Scholar]
  44. 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 [View Article][PubMed]
     [Google Scholar]
  45. Shankar S. K., Satishchandra P., Mahadevan A., Yasha T. C., Nagaraja D., Taly A. B., Prabhakar S., Nath A. 2003; Low prevalence of progressive multifocal leukoencephalopathy in India and Africa: is there a biological explanation?. J Neurovirol 9:Suppl. 159–67[PubMed] [CrossRef]
     [Google Scholar]
  46. Stettner M. R., Nance J. A., Wright C. A., Kinoshita Y., Kim W. K., Morgello S., Rappaport J., Khalili K., Gordon J., Johnson E. M. 2009; 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. J Gen Virol 90:2005–2014 [View Article][PubMed]
     [Google Scholar]
  47. Tada H., Rappaport J., Lashgari M., Amini S., Wong-Staal F., Khalili K. 1990; Trans-activation of the JC virus late promoter by the tat protein of type 1 human immunodeficiency virus in glial cells. Proc Natl Acad Sci U S A 87:3479–3483 [View Article][PubMed]
     [Google Scholar]
  48. Tahirov T. H., Babayeva N. D., Varzavand K., Cooper J. J., Sedore S. C., Price D. H. 2010; Crystal structure of HIV-1 Tat complexed with human P-TEFb. Nature 465:747–751 [View Article][PubMed]
     [Google Scholar]
  49. 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[PubMed]
     [Google Scholar]
  50. White M. K., Johnson E. M., Khalili K. 2009; Multiple roles for Pur-α in cellular and viral regulation. Cell Cycle 8:414–420 [View Article][PubMed]
     [Google Scholar]
  51. Wortman M. J., Krachmarov C. P., Kim J. H., Gordon R. G., Chepenik L. G., Brady J. N., Gallia G. L., Khalili K., Johnson E. M. 2000; Interaction of HIV-1 Tat with Pur-α in nuclei of human glial cells: characterization of RNA-mediated protein-protein binding. J Cell Biochem 77:65–74 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.047902-0
Loading
Effects of Tat proteins and Tat mutants of different human immunodeficiency virus type 1 clades on glial JC virus early and late gene transcription
J. Gen. Virol. 94, 514 (2013); https://doi.org/10.1099/vir.0.047902-0
/content/journal/jgv/10.1099/vir.0.047902-0
/content/journal/jgv/10.1099/vir.0.047902-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error