Converging Strategies in Expression of Human Complex Retroviruses
Abstract
:1. Introduction
2. Expression Strategies of HIV-1
3. Expression Strategies of HTLV-1
4. Expression Strategies of Other Human Complex Retroviruses
5. Open Questions and Perspectives
Acknowledgments
Conflict of Interest
References and Notes
- Goff, S.P. Retroviridae: The retroviruses and their replication. In Fields Virology, 5th ed.; Knipe, D.M., Howley, P.M., Eds.; Wolters Kluwer/Lippincott Williams and Wilkins: Philadelphia, PA, USA, 2007; Volume 2, pp. 1999–2070. [Google Scholar]
- Cullen, B.R. Human immunodeficiency virus as a prototypic complex retrovirus. J. Virol. 1991, 65, 1053–1056. [Google Scholar] [CrossRef]
- Mertz, J.A.; Simper, M.S.; Lozano, M.M.; Payne, S.M.; Dudley, J.P. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J. Virol. 2005, 79, 14737–14747. [Google Scholar] [CrossRef]
- Indik, S.; Gunzburg, W.H.; Salmons, B.; Rouault, F. A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 2005, 337, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Lower, R.; Tonjes, R.R.; Korbmacher, C.; Kurth, R.; Lower, J. Identification of a Rev-related protein by analysis of spliced transcripts of the human endogenous retroviruses HTDV/HERV-K. J. Virol. 1995, 69, 141–149. [Google Scholar] [CrossRef] [PubMed]
- Pasquinelli, A.E.; Ernst, R.K.; Lund, E.; Grimm, C.; Zapp, M.L.; Rekosh, D.; Hammarskjold, M.L.; Dahlberg, J.E. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J. 1997, 16, 7500–7510. [Google Scholar] [CrossRef] [PubMed]
- Young, L.S.; Rickinson, A.B. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 2004, 4, 757–768. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, S. HPV-16 RNA processing. Front. Biosci. 2008, 13, 5880–5891. [Google Scholar] [CrossRef]
- Moody, C.A.; Laimins, L.A. Human papillomavirus oncoproteins: Pathways to transformation. Nat. Rev. Cancer 2010, 10, 550–560. [Google Scholar] [CrossRef]
- Muesing, M.A.; Smith, D.H.; Cabradilla, C.D.; Benton, C.V.; Lasky, L.A.; Capon, D.J. Nucleic acid structure and expression of the human AIDS/lymphadenopathy retrovirus. Nature 1985, 313, 450–458. [Google Scholar] [CrossRef]
- Purcell, D.F.; Martin, M.A. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 1993, 67, 6365–6378. [Google Scholar] [CrossRef]
- Schwartz, S.; Felber, B.K.; Benko, D.M.; Fenyo, E.M.; Pavlakis, G.N. Cloning and functional analysis of multiply spliced mRNA species of human immunodeficiency virus type 1. J. Virol. 1990, 64, 2519–2529. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, S.; Felber, B.K.; Fenyo, E.M.; Pavlakis, G.N. Env and Vpu proteins of human immunodeficiency virus type 1 are produced from multiple bicistronic mRNAs. J. Virol. 1990, 64, 5448–5456. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, S.; Felber, B.K.; Pavlakis, G.N. Expression of human immunodeficiency virus type 1 vif and vpr mRNAs is Rev-dependent and regulated by splicing. Virology 1991, 183, 677–686. [Google Scholar] [CrossRef] [PubMed]
- Briquet, S.; Vaquero, C. Immunolocalization studies of an antisense protein in HIV-1-infected cells and viral particles. Virology 2002, 292, 177–184. [Google Scholar] [CrossRef] [PubMed]
- Stoltzfus, C.M. Chapter 1. Regulation of HIV-1 alternative RNA splicing and its role in virus replication. Adv. Virus Res. 2009, 74, 1–40. [Google Scholar] [PubMed]
- Tazi, J.; Bakkour, N.; Marchand, V.; Ayadi, L.; Aboufirassi, A.; Branlant, C. Alternative splicing: Regulation of HIV-1 multiplication as a target for therapeutic action. FEBS J. 2010, 277, 867–876. [Google Scholar] [CrossRef]
- Brady, J.; Kashanchi, F. Tat gets the "green" light on transcription initiation. Retrovirology 2005, 2, 69. [Google Scholar] [CrossRef]
- Landry, S.; Halin, M.; Lefort, S.; Audet, B.; Vaquero, C.; Mesnard, J.M.; Barbeau, B. Detection, characterization and regulation of antisense transcripts in HIV-1. Retrovirology 2007, 4, 71. [Google Scholar] [CrossRef]
- Berro, R.; Kehn, K.; de la Fuente, C.; Pumfery, A.; Adair, R.; Wade, J.; Colberg-Poley, A.M.; Hiscott, J.; Kashanchi, F. Acetylated Tat regulates human immunodeficiency virus type 1 splicing through its interaction with the splicing regulator p32. J. Virol. 2006, 80, 3189–3204. [Google Scholar] [CrossRef]
- Berro, R.; Pedati, C.; Kehn-Hall, K.; Wu, W.; Klase, Z.; Even, Y.; Geneviere, A.M.; Ammosova, T.; Nekhai, S.; Kashanchi, F. CDK13, a new potential human immunodeficiency virus type 1 inhibitory factor regulating viral mRNA splicing. J. Virol. 2008, 82, 7155–7166. [Google Scholar] [CrossRef]
- Kammler, S.; Otte, M.; Hauber, I.; Kjems, J.; Hauber, J.; Schaal, H. The strength of the HIV-1 3′ splice sites affects Rev function. Retrovirology 2006, 3, 89. [Google Scholar] [CrossRef] [PubMed]
- Cullen, B.R. Nuclear mRNA export: Insights from virology. Trends Biochem. Sci. 2003, 28, 419–424. [Google Scholar] [CrossRef] [PubMed]
- Groom, H.C.; Anderson, E.C.; Lever, A.M. Rev: Beyond nuclear export. J. Gen. Virol. 2009, 90, 1303–1318. [Google Scholar] [CrossRef] [PubMed]
- Rosen, C.A.; Terwilliger, E.; Dayton, A.; Sodroski, J.G.; Haseltine, W.A. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 2071–2075. [Google Scholar] [CrossRef] [PubMed]
- Maldarelli, F.; Martin, M.A.; Strebel, K. Identification of posttranscriptionally active inhibitory sequences in human immunodeficiency virus type 1 RNA: Novel level of gene regulation. J. Virol. 1991, 65, 5732–5743. [Google Scholar] [CrossRef]
- Nasioulas, G.; Zolotukhin, A.S.; Tabernero, C.; Solomin, L.; Cunningham, C.P.; Pavlakis, G.N.; Felber, B.K. Elements distinct from human immunodeficiency virus type 1 splice sites are responsible for the Rev dependence of env mRNA. J. Virol. 1994, 68, 2986–2993. [Google Scholar] [CrossRef]
- Schwartz, S.; Felber, B.K.; Pavlakis, G.N. Distinct RNA sequences in the gag region of human immunodeficiency virus type 1 decrease RNA stability and inhibit expression in the absence of Rev protein. J. Virol. 1992, 66, 150–159. [Google Scholar] [CrossRef]
- Fischer, U.; Meyer, S.; Teufel, M.; Heckel, C.; Luhrmann, R.; Rautmann, G. Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J. 1994, 13, 4105–4112. [Google Scholar] [CrossRef]
- Schwartz, S.; Campbell, M.; Nasioulas, G.; Harrison, J.; Felber, B.K.; Pavlakis, G.N. Mutational inactivation of an inhibitory sequence in human immunodeficiency virus type 1 results in Rev-independent gag expression. J. Virol. 1992, 66, 7176–7182. [Google Scholar] [CrossRef]
- Berthold, E.; Maldarelli, F. cis-acting elements in human immunodeficiency virus type 1 RNAs direct viral transcripts to distinct intranuclear locations. J. Virol. 1996, 70, 4667–4682. [Google Scholar] [CrossRef]
- Kim, S.Y.; Byrn, R.; Groopman, J.; Baltimore, D. Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: Evidence for differential gene expression. J. Virol. 1989, 63, 3708–3713. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, N.; Maitra, R.K.; Venkatesan, S. Rev-induced modulation of Nef protein underlies temporal regulation of human immunodeficiency virus replication. Proc. Natl. Acad. Sci. U. S. A. 1989, 86, 6111–6115. [Google Scholar] [CrossRef] [PubMed]
- Weinberger, L.S.; Burnett, J.C.; Toettcher, J.E.; Arkin, A.P.; Schaffer, D.V. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell 2005, 122, 169–182. [Google Scholar] [CrossRef] [PubMed]
- Weinberger, L.S.; Dar, R.D.; Simpson, M.L. Transient-mediated fate determination in a transcriptional circuit of HIV. Nat. Genet. 2008, 40, 466–470. [Google Scholar] [CrossRef] [PubMed]
- Weinberger, L.S.; Shenk, T. An HIV feedback resistor: Auto-regulatory circuit deactivator and noise buffer. PLoS Biol. 2007, 5, e9. [Google Scholar] [CrossRef]
- Kirchhoff, F. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 2010, 8, 55–67. [Google Scholar] [CrossRef]
- Malim, M.H.; Emerman, M. HIV-1 accessory proteins—Ensuring viral survival in a hostile environment. Cell Host Microbe 2008, 3, 388–398. [Google Scholar] [CrossRef]
- 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.; et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 1995, 270, 988–991. [Google Scholar] [CrossRef]
- Lindwasser, O.W.; Chaudhuri, R.; Bonifacino, J.S. Mechanisms of CD4 downregulation by the Nef and Vpu proteins of primate immunodeficiency viruses. Curr. Mol. Med. 2007, 7, 171–184. [Google Scholar] [CrossRef]
- Lama, J.; Mangasarian, A.; Trono, D. Cell-surface expression of CD4 reduces HIV-1 infectivity by blocking Env incorporation in a Nef- and Vpu-inhibitable manner. Curr. Biol. 1999, 9, 622–631. [Google Scholar] [CrossRef]
- Ross, T.M.; Oran, A.E.; Cullen, B.R. Inhibition of HIV-1 progeny virion release by cell-surface CD4 is relieved by expression of the viral Nef protein. Curr. Biol. 1999, 9, 613–621. [Google Scholar] [CrossRef] [PubMed]
- Neil, S.J.; Zang, T.; Bieniasz, P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451, 425–430. [Google Scholar] [CrossRef] [PubMed]
- Geleziunas, R.; Xu, W.; Takeda, K.; Ichijo, H.; Greene, W.C. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature 2001, 410, 834–838. [Google Scholar] [CrossRef] [PubMed]
- Harris, R.S.; Liddament, M.T. Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol. 2004, 4, 868–877. [Google Scholar] [CrossRef]
- Kogan, M.; Rappaport, J. HIV-1 accessory protein Vpr: Relevance in the pathogenesis of HIV and potential for therapeutic intervention. Retrovirology 2011, 8, 25. [Google Scholar] [CrossRef]
- Schoborg, R.V. Analysis of caprine arthritis encephalitis virus (CAEV) temporal gene expression in infected cells. Virus Res. 2002, 90, 37–46. [Google Scholar] [CrossRef]
- Sargan, D.R.; Roy, D.J.; Dalziel, R.G.; Watt, N.J.; McConnell, I. A temporal study of RNAs produced in maedi-visna virus infection of choroid plexus cells. Vet. Microbiol. 1994, 39, 369–378. [Google Scholar] [CrossRef]
- Martarano, L.; Stephens, R.; Rice, N.; Derse, D. Equine infectious anemia virus trans-regulatory protein Rev controls viral mRNA stability, accumulation, and alternative splicing. J. Virol. 1994, 68, 3102–3111. [Google Scholar] [CrossRef]
- Ciminale, V.; Pavlakis, G.N.; Derse, D.; Cunningham, C.P.; Felber, B.K. Complex splicing in the human T-cell leukemia virus (HTLV) family of retroviruses: Novel mRNAs and proteins produced by HTLV type I. J. Virol. 1992, 66, 1737–1745. [Google Scholar] [CrossRef]
- Koralnik, I.J.; Gessain, A.; Klotman, M.E.; Lo Monico, A.; Berneman, Z.N.; Franchini, G. Protein isoforms encoded by the pX region of human T-cell leukemia/lymphotropic virus type I. Proc. Natl. Acad. Sci. U. S. A. 1992, 89, 8813–8817. [Google Scholar] [CrossRef]
- Larocca, D.; Chao, L.A.; Seto, M.H.; Brunck, T.K. Human T-cell leukemia virus minus strand transcription in infected T-cells. Biochem. Biophys. Res. Commun. 1989, 163, 1006–1013. [Google Scholar] [CrossRef] [PubMed]
- Gaudray, G.; Gachon, F.; Basbous, J.; Biard-Piechaczyk, M.; Devaux, C.; Mesnard, J.M. The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J. Virol. 2002, 76, 12813–12822. [Google Scholar] [CrossRef] [PubMed]
- Felber, B.K.; Paskalis, H.; Kleinman-Ewing, C.; Wong-Staal, F.; Pavlakis, G.N. The pX protein of HTLV-I is a transcriptional activator of its long terminal repeats. Science 1985, 229, 675–679. [Google Scholar] [CrossRef] [PubMed]
- Hidaka, M.; Inoue, J.; Yoshida, M.; Seiki, M. Post-transcriptional regulator (rex) of HTLV-1 initiates expression of viral structural proteins but suppresses expression of regulatory proteins. EMBO J. 1988, 7, 519–523. [Google Scholar] [CrossRef]
- Inoue, J.; Seiki, M.; Yoshida, M. The second pX product p27 chi-III of HTLV-1 is required for gag gene expression. FEBS Lett. 1986, 209, 187–190. [Google Scholar] [CrossRef]
- Bogerd, H.P.; Fridell, R.A.; Madore, S.; Cullen, B.R. Identification of a novel cellular cofactor for the Rev/Rex class of retroviral regulatory proteins. Cell 1995, 82, 485–494. [Google Scholar] [CrossRef]
- Hanly, S.M.; Rimsky, L.T.; Malim, M.H.; Kim, J.H.; Hauber, J.; Duc Dodon, M.; Le, S.Y.; Maizel, J.V.; Cullen, B.R.; Greene, W.C. Comparative analysis of the HTLV-I Rex and HIV-1 Rev trans-regulatory proteins and their RNA response elements. Genes Dev. 1989, 3, 1534–1544. [Google Scholar] [CrossRef]
- Saiga, A.; Orita, S.; Minoura-Tada, N.; Maeda, M.; Aono, Y.; Asakawa, M.; Nakahara, K.; Kubota, R.; Osame, M.; Igarashi, H. cis-Acting inhibitory elements within the pol-env region of human T-cell leukemia virus type 1 possibly involved in viral persistence. J. Virol. 1997, 71, 4485–4494. [Google Scholar] [CrossRef]
- Li, M.; Green, P.L. Detection and quantitation of HTLV-1 and HTLV-2 mRNA species by real-time RT-PCR. J. Virol. Meth. 2007, 142, 159–168. [Google Scholar] [CrossRef]
- Li, M.; Kesic, M.; Yin, H.; Yu, L.; Green, P.L. Kinetic analysis of human T-cell leukemia virus type 1 gene expression in cell culture and infected animals. J. Virol. 2009, 83, 3788–3797. [Google Scholar] [CrossRef]
- Rende, F.; Cavallari, I.; Corradin, A.; Silic-Benussi, M.; Toulza, F.; Toffolo, G.M.; Tanaka, Y.; Jacobson, S.; Taylor, G.P.; D’Agostino, D.M.; et al. Kinetics and intracellular compartmentalization of HTLV-1 gene expression: nuclear retention of HBZ mRNA. Blood 2011. [CrossRef] [PubMed]
- Corradin, A.; Di Camillo, B.; Ciminale, V.; Toffolo, G.; Cobelli, C. Sensitivity analysis of retrovirus HTLV-1 transactivation. J. Comput. Biol. 2011, 18, 183–193. [Google Scholar] [CrossRef] [PubMed]
- Marriott, S.J.; Semmes, O.J. Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene 2005, 24, 5986–5995. [Google Scholar] [CrossRef] [PubMed]
- Boxus, M.; Twizere, J.C.; Legros, S.; Dewulf, J.F.; Kettmann, R.; Willems, L. The HTLV-1 Tax interactome. Retrovirology 2008, 5, 76. [Google Scholar] [CrossRef] [PubMed]
- Saggioro, D.; Silic-Benussi, M.; Biasiotto, R.; D’Agostino, D.M.; Ciminale, V. Control of cell death pathways by HTLV-1 proteins. Front. Biosci. 2009, 14, 3338–3351. [Google Scholar] [CrossRef]
- D’Agostino, D.M.; Ciminale, V.; Zotti, L.; Rosato, A.; Chieco-Bianchi, L. The human T-cell lymphotropic virus type 1 Tof protein contains a bipartite nuclear localization signal that is able to functionally replace the amino-terminal domain of Rex. J. Virol. 1997, 71, 75–83. [Google Scholar] [CrossRef]
- Nicot, C.; Dundr, M.; Johnson, J.M.; Fullen, J.R.; Alonzo, N.; Fukumoto, R.; Princler, G.L.; Derse, D.; Misteli, T.; Franchini, G. HTLV-1-encoded p30(II) is a post-transcriptional negative regulator of viral replication. Nat. Med. 2004, 10, 197–201. [Google Scholar] [CrossRef]
- Younis, I.; Khair, L.; Dundr, M.; Lairmore, M.D.; Franchini, G.; Green, P.L. Repression of human T-cell leukemia virus type 1 and type 2 replication by a viral mRNA-encoded posttranscriptional regulator. J. Virol. 2004, 78, 11077–11083. [Google Scholar] [CrossRef]
- Zhang, W.; Nisbet, J.W.; Albrecht, B.; Ding, W.; Kashanchi, F.; Bartoe, J.T.; Lairmore, M.D. Human T-lymphotropic virus type 1 p30(II) regulates gene transcription by binding CREB binding protein/p300. J. Virol. 2001, 75, 9885–9895. [Google Scholar] [CrossRef]
- Zhang, W.; Nisbet, J.W.; Bartoe, J.T.; Ding, W.; Lairmore, M.D. Human T-lymphotropic virus type 1 p30(II) functions as a transcription factor and differentially modulates CREB-responsive promoters. J. Virol. 2000, 74, 11270–11277. [Google Scholar] [CrossRef]
- Michael, B.; Nair, A.M.; Hiraragi, H.; Shen, L.; Feuer, G.; Boris-Lawrie, K.; Lairmore, M.D. Human T lymphotropic virus type-1 p30II alters cellular gene expression to selectively enhance signaling pathways that activate T lymphocytes. Retrovirology 2004, 1, 39. [Google Scholar] [CrossRef]
- Taylor, J.M.; Ghorbel, S.; Nicot, C. Genome wide analysis of human genes transcriptionally and post-transcriptionally regulated by the HTLV-I protein p30. BMC Genomics 2009, 10, 311. [Google Scholar] [CrossRef] [PubMed]
- Sinha-Datta, U.; Datta, A.; Ghorbel, S.; Dodon, M.D.; Nicot, C. Human T-cell lymphotrophic virus type I rex and p30 interactions govern the switch between virus latency and replication. J. Biol. Chem. 2007, 282, 14608–14615. [Google Scholar] [CrossRef] [PubMed]
- Datta, A.; Sinha-Datta, U.; Dhillon, N.K.; Buch, S.; Nicot, C. The HTLV-I p30 interferes with TLR4 signaling and modulates the release of pro- and anti-inflammatory cytokines from human macrophages. J. Biol. Chem. 2006, 281, 23414–23424. [Google Scholar] [CrossRef] [PubMed]
- Heger, P.; Rosorius, O.; Hauber, J.; Stauber, R.H. Titration of cellular export factors, but not heteromultimerization, is the molecular mechanism of trans-dominant HTLV-1 rex mutants. Oncogene 1999, 18, 4080–4090. [Google Scholar] [CrossRef] [PubMed]
- Kubota, S.; Hatanaka, M.; Pomerantz, R.J. Nucleo-cytoplasmic redistribution of the HTLV-I Rex protein: Alterations by coexpression of the HTLV-I p21x protein. Virology 1996, 220, 502–507. [Google Scholar] [CrossRef]
- Ciminale, V.; Zotti, L.; D’Agostino, D.M.; Ferro, T.; Casareto, L.; Franchini, G.; Bernardi, P.; Chieco-Bianchi, L. Mitochondrial targeting of the p13II protein coded by the x-II ORF of human T-cell leukemia/lymphotropic virus type I (HTLV-I). Oncogene 1999, 18, 4505–4514. [Google Scholar] [CrossRef]
- D’Agostino, D.M.; Silic-Benussi, M.; Hiraragi, H.; Lairmore, M.D.; Ciminale, V. The human T-cell leukemia virus type 1 p13II protein: effects on mitochondrial function and cell growth. Cell Death Differ. 2005, 12, 905–915. [Google Scholar] [CrossRef]
- Silic-Benussi, M.; Cavallari, I.; Zorzan, T.; Rossi, E.; Hiraragi, H.; Rosato, A.; Horie, K.; Saggioro, D.; Lairmore, M.D.; Willems, L.; et al. Suppression of tumor growth and cell proliferation by p13II, a mitochondrial protein of human T cell leukemia virus type 1. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 6629–6634. [Google Scholar] [CrossRef]
- Hiraragi, H.; Michael, B.; Nair, A.; Silic-Benussi, M.; Ciminale, V.; Lairmore, M. Human T-lymphotropic virus type 1 mitochondrion-localizing protein p13II sensitizes Jurkat T cells to Ras-mediated apoptosis. J. Virol. 2005, 79, 9449–9457. [Google Scholar] [CrossRef]
- Silic-Benussi, M.; Cavallari, I.; Vajente, N.; Vidali, S.; Chieco-Bianchi, L.; Di Lisa, F.; Saggioro, D.; D’Agostino, D.M.; Ciminale, V. Redox regulation of T-cell turnover by the p13 protein of human T-cell leukemia virus type 1: Distinct effects in primary versus transformed cells. Blood 2010, 116, 54–62. [Google Scholar] [CrossRef] [PubMed]
- Silic-Benussi, M.; Biasiotto, R.; Andresen, V.; Franchini, G.; D’Agostino, D.M.; Ciminale, V. HTLV-1 p13, a small protein with a busy agenda. Mol. Aspect. Med. 2010, 31, 350–358. [Google Scholar] [CrossRef] [PubMed]
- Andresen, V.; Pise-Masison, C.A.; Sinha-Datta, U.; Bellon, M.; Valeri, V.; Washington Parks, R.; Cecchinato, V.; Fukumoto, R.; Nicot, C.; Franchini, G. Suppression of HTLV-1 replication by Tax-mediated re-routing of the p13 viral protein to nuclear speckles. Blood 2011. [CrossRef]
- Mulloy, J.C.; Crownley, R.W.; Fullen, J.; Leonard, W.J.; Franchini, G. The human T-cell leukemia/lymphotropic virus type 1 p12I proteins bind the interleukin-2 receptor beta and gammac chains and affects their expression on the cell surface. J. Virol. 1996, 70, 3599–3605. [Google Scholar] [CrossRef]
- Nicot, C.; Mulloy, J.C.; Ferrari, M.G.; Johnson, J.M.; Fu, K.; Fukumoto, R.; Trovato, R.; Fullen, J.; Leonard, W.J.; Franchini, G. HTLV-1 p12(I) protein enhances STAT5 activation and decreases the interleukin-2 requirement for proliferation of primary human peripheral blood mononuclear cells. Blood 2001, 98, 823–829. [Google Scholar] [CrossRef]
- Johnson, J.M.; Nicot, C.; Fullen, J.; Ciminale, V.; Casareto, L.; Mulloy, J.C.; Jacobson, S.; Franchini, G. Free major histocompatibility complex class I heavy chain is preferentially targeted for degradation by human T-cell leukemia/lymphotropic virus type 1 p12(I) protein. J. Virol. 2001, 75, 6086–6094. [Google Scholar] [CrossRef]
- Ding, W.; Albrecht, B.; Luo, R.; Zhang, W.; Stanley, J.R.; Newbound, G.C.; Lairmore, M.D. Endoplasmic reticulum and cis-Golgi localization of human T-lymphotropic virus type 1 p12(I): Association with calreticulin and calnexin. J. Virol. 2001, 75, 7672–7682. [Google Scholar] [CrossRef]
- Ding, W.; Albrecht, B.; Kelley, R.E.; Muthusamy, N.; Kim, S.J.; Altschuld, R.A.; Lairmore, M.D. Human T-cell lymphotropic virus type 1 p12(I) expression increases cytoplasmic calcium to enhance the activation of nuclear factor of activated T cells. J. Virol. 2002, 76, 10374–10382. [Google Scholar] [CrossRef]
- Albrecht, B.; D’Souza, C.D.; Ding, W.; Tridandapani, S.; Coggeshall, K.M.; Lairmore, M.D. Activation of nuclear factor of activated T cells by human T-lymphotropic virus type 1 accessory protein p12(I). J. Virol. 2002, 76, 3493–3501. [Google Scholar] [CrossRef]
- Kim, S.J.; Ding, W.; Albrecht, B.; Green, P.L.; Lairmore, M.D. A conserved calcineurin-binding motif in human T lymphotropic virus type 1 p12I functions to modulate nuclear factor of activated T cell activation. J. Biol. Chem. 2003, 278, 15550–15557. [Google Scholar] [CrossRef]
- Nicot, C.; Harrod, R.L.; Ciminale, V.; Franchini, G. Human T-cell leukemia/lymphoma virus type 1 nonstructural genes and their functions. Oncogene 2005, 24, 6026–6034. [Google Scholar] [CrossRef] [PubMed]
- Van Prooyen, N.; Andresen, V.; Gold, H.; Bialuk, I.; Pise-Masison, C.; Franchini, G. Hijacking the T-cell communication network by the human T-cell leukemia/lymphoma virus type 1 (HTLV-1) p12 and p8 proteins. Mol. Aspect. Med. 2010, 31, 333–343. [Google Scholar] [CrossRef]
- Van Prooyen, N.; Gold, H.; Andresen, V.; Schwartz, O.; Jones, K.; Ruscetti, F.; Lockett, S.; Gudla, P.; Venzon, D.; Franchini, G. Human T-cell leukemia virus type 1 p8 protein increases cellular conduits and virus transmission. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 20738–20743. [Google Scholar] [CrossRef] [PubMed]
- Xu, W.; Santini, P.A.; Sullivan, J.S.; He, B.; Shan, M.; Ball, S.C.; Dyer, W.B.; Ketas, T.J.; Chadburn, A.; Cohen-Gould, L.; et al. HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat. Immunol. 2009, 10, 1008–1017. [Google Scholar] [CrossRef]
- Matsuoka, M.; Green, P.L. The HBZ gene, a key player in HTLV-1 pathogenesis. Retrovirology 2009, 6, 71. [Google Scholar] [CrossRef] [PubMed]
- Clerc, I.; Polakowski, N.; Andre-Arpin, C.; Cook, P.; Barbeau, B.; Mesnard, J.M.; Lemasson, I. An interaction between the human T cell leukemia virus type 1 basic leucine zipper factor (HBZ) and the KIX domain of p300/CBP contributes to the down-regulation of tax-dependent viral transcription by HBZ. J. Biol. Chem. 2008, 283, 23903–23913. [Google Scholar] [CrossRef]
- Arnold, J.; Zimmerman, B.; Li, M.; Lairmore, M.D.; Green, P.L. Human T-cell leukemia virus type-1 antisense-encoded gene, Hbz, promotes T-lymphocyte proliferation. Blood 2008, 112, 3788–3797. [Google Scholar] [CrossRef] [PubMed]
- Satou, Y.; Yasunaga, J.; Yoshida, M.; Matsuoka, M. HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 720–725. [Google Scholar] [CrossRef] [PubMed]
- Derse, D.; Hill, S.A.; Princler, G.; Lloyd, P.; Heidecker, G. Resistance of human T cell leukemia virus type 1 to APOBEC3G restriction is mediated by elements in nucleocapsid. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 2915–2920. [Google Scholar] [CrossRef]
- Linial, M. Foamy viruses. In Fields Virology, 5th ed.; Knipe, D., Howley, P., Eds.; Lippincott Williams and Wilkins: Philadelphia, PA, USA, 2007; Volume 2, pp. 2245–2262. [Google Scholar]
- Linial, M.L. Foamy viruses are unconventional retroviruses. J. Virol. 1999, 73, 1747–1755. [Google Scholar] [CrossRef]
- Rethwilm, A. Molecular biology of foamy viruses. Med. Microbiol. Immunol. 2010, 199, 197–207. [Google Scholar] [CrossRef] [PubMed]
- Lochelt, M.; Flugel, R.M.; Aboud, M. The human foamy virus internal promoter directs the expression of the functional Bel 1 transactivator and Bet protein early after infection. J. Virol. 1994, 68, 638–645. [Google Scholar] [CrossRef] [PubMed]
- Keller, A.; Partin, K.M.; Lochelt, M.; Bannert, H.; Flugel, R.M.; Cullen, B.R. Characterization of the transcriptional trans activator of human foamy retrovirus. J. Virol. 1991, 65, 2589–2594. [Google Scholar] [CrossRef] [PubMed]
- Meiering, C.D.; Rubio, C.; May, C.; Linial, M.L. Cell-type-specific regulation of the two foamy virus promoters. J. Virol. 2001, 75, 6547–6557. [Google Scholar] [CrossRef] [PubMed]
- Jordan, I.; Enssle, J.; Guttler, E.; Mauer, B.; Rethwilm, A. Expression of human foamy virus reverse transcriptase involves a spliced pol mRNA. Virology 1996, 224, 314–319. [Google Scholar] [CrossRef]
- Bodem, J.; Lochelt, M.; Winkler, I.; Flower, R.P.; Delius, H.; Flugel, R.M. Characterization of the spliced pol transcript of feline foamy virus: The splice acceptor site of the pol transcript is located in gag of foamy viruses. J. Virol. 1996, 70, 9024–9027. [Google Scholar] [CrossRef] [PubMed]
- Yu, S.F.; Edelmann, K.; Strong, R.K.; Moebes, A.; Rethwilm, A.; Linial, M.L. The carboxyl terminus of the human foamy virus Gag protein contains separable nucleic acid binding and nuclear transport domains. J. Virol. 1996, 70, 8255–8262. [Google Scholar] [CrossRef] [PubMed]
- Yu, S.F.; Sullivan, M.D.; Linial, M.L. Evidence that the human foamy virus genome is DNA. J. Virol. 1999, 73, 1565–1572. [Google Scholar] [CrossRef]
- Russell, R.A.; Wiegand, H.L.; Moore, M.D.; Schafer, A.; McClure, M.O.; Cullen, B.R. Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J. Virol. 2005, 79, 8724–8731. [Google Scholar] [CrossRef]
- Lochelt, M.; Romen, F.; Bastone, P.; Muckenfuss, H.; Kirchner, N.; Kim, Y.B.; Truyen, U.; Rosler, U.; Battenberg, M.; Saib, A.; et al. The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 7982–7987. [Google Scholar] [CrossRef]
- Lee, A.H.; Lee, H.Y.; Sung, Y.C. The gene expression of human foamy virus does not require a post-transcriptional transactivator. Virology 1994, 204, 409–413. [Google Scholar] [CrossRef] [PubMed]
- Bodem, J.; Schied, T.; Gabriel, R.; Rammling, M.; Rethwilm, A. Foamy virus nuclear RNA export is distinct from that of other retroviruses. J. Virol. 2011, 85, 2333–2341. [Google Scholar] [CrossRef] [PubMed]
- Turner, G.; Barbulescu, M.; Su, M.; Jensen-Seaman, M.I.; Kidd, K.K.; Lenz, J. Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr. Biol. 2001, 11, 1531–1535. [Google Scholar] [CrossRef] [PubMed]
- Bannert, N.; Kurth, R. Retroelements and the human genome: New perspectives on an old relation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 14572–14579. [Google Scholar] [CrossRef]
- Magin, C.; Lower, R.; Lower, J. cORF and RcRE, the Rev/Rex and RRE/RxRE homologues of the human endogenous retrovirus family HTDV/HERV-K. J. Virol. 1999, 73, 9496–9507. [Google Scholar] [CrossRef]
- Boese, A.; Sauter, M.; Galli, U.; Best, B.; Herbst, H.; Mayer, J.; Kremmer, E.; Roemer, K.; Mueller-Lantzsch, N. Human endogenous retrovirus protein cORF supports cell transformation and associates with the promyelocytic leukemia zinc finger protein. Oncogene 2000, 19, 4328–4336. [Google Scholar] [CrossRef]
- Armbruester, V.; Sauter, M.; Krautkraemer, E.; Meese, E.; Kleiman, A.; Best, B.; Roemer, K.; Mueller-Lantzsch, N. A novel gene from the human endogenous retrovirus K expressed in transformed cells. Clin. Cancer Res. 2002, 8, 1800–1807. [Google Scholar]
- Wang-Johanning, F.; Frost, A.R.; Johanning, G.L.; Khazaeli, M.B.; LoBuglio, A.F.; Shaw, D.R.; Strong, T.V. Expression of human endogenous retrovirus k envelope transcripts in human breast cancer. Clin. Cancer Res. 2001, 7, 1553–1560. [Google Scholar]
- Lairmore, M.; Franchini, G. Human T-cell leukemia virus types 1 and 2. In Fields Virology, 5th ed.; Knipe, D., Howley, P., Eds.; Lippincott Williams and Wilkins: Philadelphia, PA, USA, 2007; Volume 2, pp. 2071–2106. [Google Scholar]
PROTEIN | LOCALIZATION | FUNCTION |
---|---|---|
Nef | cytoplasm, nucleus, virion | enhances clathrin-mediated endocytosis and degradation of CD4; downregulates surface expression of MHC class I and T cell receptor (TCR)-CD3 complexes |
Vpu | cytoplasm, nucleus | favors CD4 retention in the endoplasmic reticulum and proteasomal degradation; promotes release of nascent virions from infected cells by inhibiting tetherin |
Vif | cytoplasm, virion | induces proteasomal degradation of the APOBEC3G restriction factor |
Vpr | nucleus mitochondria, virion | exerts cytopathic effects through its ability to affect mitochondrial function; increases viral transcription and induces cell-cycle arrest in the G2 phase |
PROTEIN | LOCALIZATION | FUNCTION |
---|---|---|
p30Tof | nucleolus, nucleus | inhibits nuclear export of the tax/rex mRNA; affects Tax-mediated transcription; affects the expression of cellular genes; interacts with Rex; interferes with TLR4 signaling |
p21Rex | cytoplasm | represses Rex in some experimental systems |
p13 | mitochondrial inner membrane, nucleus | alters mitochondrial K+ permeability and increases mitochondrial ROS production; activates normal resting T-cells while promoting death of transformed cells; exerts antitumor effects in vivo; inhibits Tax function in the nucleus |
p12 | endoplasmic reticulum, Golgi apparatus | binds to the IL-2R β and γ chains; sequesters free MHC-I heavy chains; interacts with calreticulin and calnexin resulting in Ca2+ release from the ER and NFAT activation |
p8 | cell surface, immunological synapse | recruited to the immunological synapse; increases T-cell contacts through LFA1 and intercellular conduits |
HBZ | nucleus | HBZ protein: inhibits Tax, Jun-B and c-Jun; stimulates Jun-D; HBZ RNA: growth-promoting effects in T-cells |
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Cavallari, I.; Rende, F.; D'Agostino, D.M.; Ciminale, V. Converging Strategies in Expression of Human Complex Retroviruses. Viruses 2011, 3, 1395-1414. https://doi.org/10.3390/v3081395
Cavallari I, Rende F, D'Agostino DM, Ciminale V. Converging Strategies in Expression of Human Complex Retroviruses. Viruses. 2011; 3(8):1395-1414. https://doi.org/10.3390/v3081395
Chicago/Turabian StyleCavallari, Ilaria, Francesca Rende, Donna M. D'Agostino, and Vincenzo Ciminale. 2011. "Converging Strategies in Expression of Human Complex Retroviruses" Viruses 3, no. 8: 1395-1414. https://doi.org/10.3390/v3081395