Pathological and Evolutionary Implications of Retroviruses as Mobile Genetic Elements
Abstract
:1. Introduction
2. Retroviruses
2.2. Endogenous Retroviruses and Pathogenic Potentials
2.3. Effects of Reactivation
2.4. Oncological Implications
2.5. HERVs and Evolutionary Implications
2.6. Known Conserved Elements: Symbiotic Genomic Effects
2.7. Primate Evolution
3. Future Directions
Acknowledgments
Conflicts of Interest
References
- Frost, L.S.; Leplae, R.; Summers, A.O.; Toussaint, A. Mobile genetic elements: The agents of open source evolution. Nat. Rev. Microbiol. 2005, 3, 722–732. [Google Scholar] [CrossRef]
- Chenais, B.; Caruso, A.; Hiard, S.; Casse, N. The impact of transposable elements on eukaryotic genomes: From genome size increase to genetic adaptation to stressful environments. Gene 2012, 509, 7–15. [Google Scholar] [CrossRef]
- Buzdin, A.A. A functional analysis of retroviral endogenous inserts in view of human genome evolution. Bioorg. Khim. 2010, 36, 38–46. [Google Scholar]
- Kidwell, M.G.; Lisch, D. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 1997, 94, 7704–7711. [Google Scholar] [CrossRef]
- Finnegan, D.J. Eukaryotic transposable elements and genome evolution. Trends Genet. 1989, 5, 103–107. [Google Scholar] [CrossRef]
- Fischer, M.G.; Suttle, C.A. A virophage at the origin of large DNA transposons. Science 2011, 332, 231–234. [Google Scholar] [CrossRef]
- Momose, M.; Abe, Y.; Ozeki, Y. Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics 2010, 186, 59–66. [Google Scholar] [CrossRef]
- Lu, C.; Chen, J.; Zhang, Y.; Hu, Q.; Su, W.; Kuang, H. Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol. Biol. Evol. 2012, 29, 1005–1017. [Google Scholar] [CrossRef]
- Huang, C.R.; Burns, K.H.; Boeke, J.D. Active transposition in genomes. Annu. Rev. Genet. 2012, 46, 651–675. [Google Scholar] [CrossRef]
- O'Donnell, K.A.; Burns, K.H. Mobilizing diversity: Transposable element insertions in genetic variation and disease. Mob. DNA 2010, 1, 21. [Google Scholar] [CrossRef]
- Shukla, R.; Upton, K.R.; Munoz-Lopez, M.; Gerhardt, D.J.; Fischer, M.E.; Nguyen, T.; Brennan, P.M.; Baillie, J.K.; Collino, A.; Ghisletti, S.; et al. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell 2013, 153, 101–111. [Google Scholar] [CrossRef]
- Goodier, J.L.; Kazazian, H.H., Jr. Retrotransposons revisited: The restraint and rehabilitation of parasites. Cell 2008, 135, 23–35. [Google Scholar] [CrossRef]
- Deininger, P.L. SINEs: Short Interspersed Repeated DNA Elements in Higher Eucaryotes. In Mobie DNA; Berg, D.E., Howe, M.M., Eds.; American Society for Microbiology: Washington, DC, USA, 1989. [Google Scholar]
- Xiong, Y.; Eickbush, T.H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol. Biol. Evol. 1988, 5, 675–690. [Google Scholar]
- Varmus, H.; Brown, P. Retroviruses. In Mobile DNA; Berg, D.E., Howe, M.M., Eds.; American Society for Microbiology: Washington, DC, USA, 1989. [Google Scholar]
- Larsson, E.; Andersson, G. Beneficial role of human endogenous retroviruses: Facts and hypotheses. Scand. J. Immunol. 1998, 48, 329–338. [Google Scholar] [CrossRef]
- Lower, R. The pathogenic potential of endogenous retroviruses: Facts and fantasies. Trends Microbiol. 1999, 7, 350–356. [Google Scholar] [CrossRef]
- Temin, H.M. Origin of retroviruses from cellular moveable genetic elements. Cell 1980, 21, 599–600. [Google Scholar] [CrossRef]
- Temin, H.M.; Mizutani, S. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 1970, 226, 1211–1213. [Google Scholar] [CrossRef]
- Temin, H.M. Reprint of Temin’s 1971 Paper Proposing the Protovirus Hypothesis. In The DNA Provirus: Howard Temin’s Scientific Legacy; Geoffrey, C.M., Sugden, B., Eds.; American Society for Microbiology: Washington, DC, USA, 1971; pp. 55–60. [Google Scholar]
- Xiong, Y.; Eickbush, T.H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990, 9, 3353–3362. [Google Scholar]
- Lower, R.; Lower, J.; Kurth, R. The viruses in all of us: Characteristics and biological significance of human endogenous retrovirus sequences. Proc. Natl. Acad. Sci. USA 1996, 93, 5177–5184. [Google Scholar] [CrossRef]
- Best, S.; le Tissier, P.R.; Stoye, J.P. Endogenous retroviruses and the evolution of resistance to retroviral infection. Trends Microbiol. 1997, 5, 313–318. [Google Scholar] [CrossRef]
- Smith, R.G.; Gallo, R.C. Agents which inhibit reverse transcriptases. Life Sci. 1974, 15, 1711–1730. [Google Scholar] [CrossRef]
- Oricchio, E.; Sciamanna, I.; Beraldi, R.; Tolstonog, G.V.; Schumann, G.G.; Spadafora, C. Distinct roles for LINE-1 and HERV-K retroelements in cell proliferation, differentiation and tumor progression. Oncogene 2007, 26, 4226–4233. [Google Scholar] [CrossRef]
- Orgel, L.E.; Crick, F.H. Selfish DNA: The ultimate parasite. Nature 1980, 284, 604–607. [Google Scholar] [CrossRef]
- Temin, H.M. Origin and General Nature of Retroviruses. In The retroviridae; Levy, J.A., Ed.; Plenum Press: New York, NY, USA, 1992; pp. 1–18. [Google Scholar]
- Bock, M.; Stoye, J.P. Endogenous retroviruses and the human germline. Curr. Opin. Genet. Dev. 2000, 10, 651–655. [Google Scholar] [CrossRef]
- Belshaw, R.; Pereira, V.; Katzourakis, A; Talbot, G.; Paces, J.; Burt, A.; Tristem, M. Long-term reinfection of the human genome by endogenous retroviruses. Proc. Natl. Acad. Sci. USA 2004, 101, 4894–4899. [Google Scholar]
- Connolly, J.B. Lentiviruses in gene therapy clinical research. Gene Ther. 2002, 9, 1730–1734. [Google Scholar] [CrossRef]
- Schanab, O.; Humer, J.; Gleiss, A.; Mikula, M.; Sturlan, S.; Grunt, S.; Okamoto, I.; Muster, T.; Pehamberger, H.; Waltenberger, A. Expression of human endogenous retrovirus K is stimulated by ultraviolet radiation in melanoma. Pigment Cell Melanoma Res. 2011, 24, 656–665. [Google Scholar] [CrossRef]
- Loiacono, C.M.; Taus, N.S.; Mitchell, W.J. The herpes simplex virus type 1 ICP0 promoter is activated by viral reactivation stimuli in trigeminal ganglia neurons of transgenic mice. J. Neurovirol. 2003, 9, 336–345. [Google Scholar]
- Johnson, T.P.; Frey, R.; Modugno, M.; Brennan, T.P.; Margulies, B.J. Development of an aciclovir implant for the effective long-term control of herpes simplex virus type-1 infection in Vero cells and in experimentally infected SKH-1 mice. Int. J. Antimicrob. Agents 2007, 30, 428–435. [Google Scholar] [CrossRef]
- Florl, A.R.; Lower, R.; Schmitz-Drager, B.J.; Schulz, W.A. DNA methylation and expression of LINE-1 and HERV-K provirus sequences in urothelial and renal cell carcinomas. Br. J. Cancer 1999, 80, 1312–1321. [Google Scholar] [CrossRef]
- Santourlidis, S.; Florl, A.; Ackermann, R.; Wirtz, H.C.; Schulz, W.A. High. frequency of alterations in DNA methylation in adenocarcinoma of the prostate. Prostate 1999, 39, 166–174. [Google Scholar] [CrossRef]
- Pagano, J.S.; Blaser, M.; Buendia, M.A.; Damania, B.; Khalili, K.; Raab-Traub, N.; Roizman, B. Infectious agents and cancer: Criteria for a causal relation. Semin. Cancer Biol. 2004, 14, 453–471. [Google Scholar] [CrossRef]
- Liang, Q.; Xu, Z.; Xu, R.; Wu, L.; Zheng, S. Expression patterns of non-coding spliced transcripts from human endogenous retrovirus HERV-H elements in colon cancer. PLoS One 2012, 7, e29950. [Google Scholar] [CrossRef]
- Cegolon, L.; Salata, C.; Weiderpass, E.; Vineis, P.; Palu, G.; Mastrangelo, G. Human endogenous retroviruses and cancer prevention: Evidence and prospects. BMC Cancer 2013, 13, 4. [Google Scholar] [CrossRef]
- Contreras-Galindo, R.; Kaplan, M.H.; Leissner, P.; Verjat, T.; Ferlenghi, I.; Bagnoli, F.; Giusti, F.; Dosik, M.H.; Hayes, D.F.; Gitlin, S.D.; et al. Human endogenous retrovirus K (HML-2) elements in the plasma of people with lymphoma and breast cancer. J. Virol. 2008, 82, 9329–9336. [Google Scholar] [CrossRef]
- Maeda, N.; Fan, H.; Yoshikai, Y. Oncogenesis by retroviruses: Old and new paradigms. Rev. Med. Virol. 2008, 18, 387–405. [Google Scholar] [CrossRef]
- Fan, H.; Johnson, C. Insertional oncogenesis by non-acute retroviruses: Implications for gene therapy. Viruses 2011, 3, 398–422. [Google Scholar] [CrossRef]
- Serafino, A.; Balestrieri, E.; Pierimarchi, P.; Matteucci, C.; Moroni, G.; Oricchio, E.; Rasi, G.; Mastino, A.; Spadafora, C.; Garaci, E.; et al. The activation of human endogenous retrovirus K (HERV-K) is implicated in melanoma cell malignant transformation. Exp. Cell Res. 2009, 315, 849–862. [Google Scholar] [CrossRef]
- Schmitt, K.; Reichrath, J.; Roesch, A.; Meese, E.; Mayer, J. Transcriptional profiling of human endogenous retrovirus group HERV-K(HML-2) loci in melanoma. Genome Biol. Evol. 2013, 5, 307–328. [Google Scholar] [CrossRef]
- Iskow, R.C.; McCabe, M.T.; Mills, R.E.; Torene, S.; Pittard, W.S.; Neuwald, A.F.; van Meir, E.G.; Vertino, P.M.; Devine, S.E. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 2010, 141, 1253–1261. [Google Scholar] [CrossRef]
- Wilkins, A.S. The enemy within: An epigenetic role of retrotransposons in cancer initiation. Bioessays 2010, 32, 856–865. [Google Scholar] [CrossRef]
- Medstrand, P.; van de Lagemaat, L.N.; Dunn, C.A.; Landry, J.R.; Svenback, D.; Mager, D.L. Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenet. Genome Res. 2005, 110, 342–352. [Google Scholar] [CrossRef]
- Ting, C.N.; Rosenberg, M.P.; Snow, C.M.; Samuelson, L.C.; Meisler, M.H. Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes Dev. 1992, 6, 1457–1465. [Google Scholar] [CrossRef]
- Samuelson, L.C.; Wiebauer, K.; Snow, C.M.; Meisler, M.H. Retroviral and pseudogene insertion sites reveal the lineage of human salivary and pancreatic amylase genes from a single gene during primate evolution. Mol. Cell. Biol. 1990, 10, 2513–2520. [Google Scholar]
- Di Cristofano, A.; Strazzullo, M.; Longo, L.; La Mantia, G. Characterization and genomic mapping of the ZNF80 locus: Expression of this zinc-finger gene is driven by a solitary LTR of ERV9 endogenous retroviral family. Nucleic Acids Res. 1995, 23, 2823–2830. [Google Scholar] [CrossRef]
- Suzuki, H.; Hosokawa, Y.; Toda, H.; Nishikimi, M.; Ozawa, T. Common protein-binding sites in the 5'-flanking regions of human genes for cytochrome c1 and ubiquinone-binding protein. J. Biol. Chem. 1990, 265, 8159–8163. [Google Scholar]
- Kjellman, C.; Sjogren, H.O.; Salford, L.G.; Widegren, B. HERV-F (XA34) is a full-length human endogenous retrovirus expressed in placental and fetal tissues. Gene 1999, 239, 99–107. [Google Scholar] [CrossRef]
- Kammerer, U.; Germeyer, A.; Stengel, S.; Kapp, M.; Denner, J. Human endogenous retrovirus K (HERV-K) is expressed in villous and extravillous cytotrophoblast cells of the human placenta. J. Reprod. Immunol. 2011, 91, 1–8. [Google Scholar]
- Venables, P.J.; Brookes, S.M.; Griffiths, D.; Weiss, R.A.; Boyd, M.T. Abundance of an endogenous retroviral envelope protein in placental trophoblasts suggests a biological function. Virology 1995, 211, 589–592. [Google Scholar] [CrossRef]
- Ober, C. The maternal-fetal relationship in human pregnancy: An immunogenetic perspective. Exp. Clin. Immunogenet. 1992, 9, 1–14. [Google Scholar]
- Linscheid, C.; Petroff, M.G. Minor histocompatibility antigens and the maternal immune response to the fetus during pregnancy. Am. J. Reprod. Immunol. 2013, 69, 304–314. [Google Scholar] [CrossRef]
- Holder, B.S.; Tower, C.L.; Forbes, K.; Mulla, M.J.; Aplin, J.D.; Abrahams, V.M. Immune cell activation by trophoblast-derived microvesicles is mediated by syncytin 1. Immunology 2012, 136, 184–191. [Google Scholar] [CrossRef]
- Villareal, L.P. On viruses, sex, and motherhood. J. Virol. 1997, 71, 859–865. [Google Scholar]
- Mangeney, M.; Renard, M.; Schlecht-Louf, G.; Bouallaga, I.; Heidmann, O.; Letzelter, C.; Richaud, A.; Ducos, B.; Heidmann, T. Placental syncytins: Genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc. Natl. Acad. Sci. USA 2007, 104, 20534–20539. [Google Scholar] [CrossRef]
- Conrad, B.; Weissmahr, R.N.; Boni, J.; Arcari, R.; Schupbach, J.; Mach, B. A human endogenous retroviral superantigen as candidate autoimmune gene in type I diabetes. Cell 1997, 90, 303–313. [Google Scholar] [CrossRef]
- Lee, Y.K.; Chew, A.; Phan, H.; Greenhalgh, D.G.; Cho, K. Genome-wide expression profiles of endogenous retroviruses in lymphoid tissues and their biological properties. Virology 2008, 373, 263–273. [Google Scholar] [CrossRef]
- Sverdlov, E.D. Retroviruses and primate evolution. Bioessays 2000, 22, 161–171. [Google Scholar] [CrossRef]
- Kim, H.S. Genomic impact, chromosomal distribution and transcriptional regulation of HERV elements. Mol. Cells 2012, 33, 539–544. [Google Scholar] [CrossRef]
© 2013 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Hayes, M.; Whitesell, M.; Brown, M.A. Pathological and Evolutionary Implications of Retroviruses as Mobile Genetic Elements. Genes 2013, 4, 573-582. https://doi.org/10.3390/genes4040573
Hayes M, Whitesell M, Brown MA. Pathological and Evolutionary Implications of Retroviruses as Mobile Genetic Elements. Genes. 2013; 4(4):573-582. https://doi.org/10.3390/genes4040573
Chicago/Turabian StyleHayes, Madeline, Mackenzie Whitesell, and Mark A. Brown. 2013. "Pathological and Evolutionary Implications of Retroviruses as Mobile Genetic Elements" Genes 4, no. 4: 573-582. https://doi.org/10.3390/genes4040573