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LTR Retroelement-Derived Protein-Coding Genes and Vertebrate Evolution

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Viruses: Essential Agents of Life

Abstract

During evolution, many cellular protein-coding genes have been formed from genes carried by long terminal repeat (LTR) retroelements (retroviruses and LTR retrotransposons). This phenomenon, called molecular domestication, has significantly impacted the emergence and diversification of the vertebrate lineage. LTR retroelements have contributed different types of coding regions to the gene repertoire of their host, including gag, envelope, integrase and protease genes. Genes derived from gag and envelope sequences are particularly well represented in vertebrate genomes. Retroelement-derived genes fulfil functions in important ­biological processes, particularly placenta formation and immunity against retro­elements, as well as cell proliferation and apoptosis. Of particular interest is the recurrent molecular domestication of retrovirus envelope genes, which has taken place several times independently in different mammalian sublineages to generate new genes involved in placenta formation. The function of most retroelement-derived genes remains unknown, and additional new genes are still to be identified particularly in “lower” vertebrates.

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References

  • Antony JM, Ellestad KK, Hammond R, Imaizumi K, Mallet F, Warren KG, Power C (2007) The human endogenous retrovirus envelope glycoprotein, syncytin-1, regulates neuroinflammation and its receptor expression in multiple sclerosis: a role for endoplasmic reticulum chaperones in astrocytes. J Immunol 179:1210–1224

    PubMed  CAS  Google Scholar 

  • Arnaud F, Caporale M, Varela M, Biek R, Chessa B, Alberti A, Golder M, Mura M, Zhang YP, Yu L, Pereira F, Demartini JC, Leymaster K, Spencer TE, Palmarini M (2007) A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog 3:e170

    Article  PubMed  Google Scholar 

  • Arnaud F, Varela M, Spencer TE, Palmarini M (2008) Coevolution of endogenous betaretroviruses of sheep and their host. Cell Mol Life Sci 65:3422–3432

    Article  PubMed  CAS  Google Scholar 

  • Baksh S, Tommasi S, Fenton S, Yu VC, Martins LM, Pfeifer GP, Latif F, Downward J, Neel BG (2005) The tumour suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death. Mol Cell 18:637–650

    Article  PubMed  CAS  Google Scholar 

  • Best S, Le Tissier P, Towers G, Stoye JP (1996) Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382:826–829

    Article  PubMed  CAS  Google Scholar 

  • Blaise S, de Parseval N, Bénit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100:13013–13018

    Article  PubMed  CAS  Google Scholar 

  • Böhne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN (2008) Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 16:203–215

    Article  PubMed  Google Scholar 

  • Bramham CR, Worley PF, Moore MJ, Guzowski JF (2008) The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J Neurosci 28:11760–11767

    Article  PubMed  CAS  Google Scholar 

  • Brandt J, Schrauth S, Veith AM, Froschauer A, Haneke T, Schultheis C, Gessler M, Leimeister C, Volff JN (2005) Transposable elements as a source of genetic innovation: expression and ­evolution of a family of retrotransposon-derived neogenes in mammals. Gene 345:101–111

    Article  PubMed  CAS  Google Scholar 

  • Butler M, Goodwin T, Simpson M, Singh M, Poulter R (2001) Vertebrate LTR retrotransposons of the Tf1/sushi group. J Mol Evol 52:260–274

    PubMed  CAS  Google Scholar 

  • Campillos M, Doerks T, Shah PK, Bork P (2006) Computational characterization of multiple Gag-like human proteins. Trends Genet 22:585–589

    Article  PubMed  CAS  Google Scholar 

  • Charlier C, Segers K, Wagenaar D, Karim L, Berghmans S, Jaillon O, Shay T, Weissenbach J, Cockett N, Gyapay G, Georges M (2001) Human-ovine comparative sequencing of a 250-kb imprinted domain encompassing the callipyge (clpg) locus and identification of six imprinted transcripts: DLK1, DAT, GTL2, PEG11, antiPEG11, and MEG8. Genome Res 11:850–862

    Article  PubMed  CAS  Google Scholar 

  • Chen HL, D’Mello SR (2010) Induction of neuronal cell death by paraneoplastic Ma1 antigen. J Neurosci Res 88:3508–3519

    Article  PubMed  CAS  Google Scholar 

  • Clark MB, Jänicke M, Gottesbühren U, Kleffmann T, Legge M, Poole ES, Tate WP (2007) Mammalian gene PEG10 expresses two reading frames by high efficiency −1 frameshifting in embryonic-associated tissues. J Biol Chem 282:37359–37369

    Article  PubMed  CAS  Google Scholar 

  • Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T (2012) Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci USA 109:E432–E441

    Article  PubMed  CAS  Google Scholar 

  • Dalmau J, Gultekin SH, Voltz R, Hoard R, DesChamps T, Balmaceda C, Batchelor T, Gerstner E, Eichen J, Frennier J, Posner JB, Rosenfeld MR (1999) Ma1, a novel neuron- and testis-specific protein, is recognized by the serum of patients with paraneoplastic neurological disorders. Brain 122:27–39

    Article  PubMed  Google Scholar 

  • Darnell RB, Posner JB (2006) Paraneoplastic syndromes affecting the nervous system. Semin Oncol 33:270–298

    Article  PubMed  Google Scholar 

  • Davis E, Caiment F, Tordoir X, Cavaillé J, Ferguson-Smith A, Cockett N, Georges M, Charlier C (2005) RNAi-mediated allelic trans-interaction at the imprinted Rtl1/Peg11 locus. Curr Biol 15:743–749

    Article  PubMed  CAS  Google Scholar 

  • de la Chaux N, Wagner A (2011) BEL/Pao retrotransposons in metazoan genomes. BMC Evol Biol 11:154

    Article  PubMed  Google Scholar 

  • Dong H, Ge X, Shen Y, Chen L, Kong Y, Zhang H, Man X, Tang L, Yuan H, Wang H, Zhao G, Jin W (2009) Gene expression profile analysis of human hepatocellular carcinoma using SAGE and LongSAGE. BMC Med Genomics 2:5

    Article  PubMed  Google Scholar 

  • Dupressoir A, Marceau G, Vernochet C, Bénit L, Kanellopoulos C, Sapin V, Heidmann T (2005) Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci USA 102:725–730

    Article  PubMed  CAS  Google Scholar 

  • Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, Opolon P, Heidmann T (2009) Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endo­genous retrovirus-derived, envelope gene. Proc Natl Acad Sci USA 106:12127–12132

    Article  PubMed  CAS  Google Scholar 

  • Dupressoir A, Vernochet C, Harper F, Guégan J, Dessen P, Pierron G, Heidmann T (2011) A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc Natl Acad Sci USA 108:E1164–E1173

    Article  PubMed  CAS  Google Scholar 

  • Edelstein LC, Collins T (2005) The SCAN domain family of zinc finger transcription factors. Gene 359:1–17

    Article  PubMed  CAS  Google Scholar 

  • Eickbush TH (1997) Telomerase and retrotransposons: which came first? Science 277:911–912

    Article  PubMed  CAS  Google Scholar 

  • Emerson RO, Thomas JH (2011) Gypsy and the birth of the SCAN domain. J Virol 85:12043–12052

    Article  PubMed  CAS  Google Scholar 

  • Esnault C, Priet S, Ribet D, Vernochet C, Bruls T, Lavialle C, Weissenbach J, Heidmann T (2008) A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc Natl Acad Sci USA 105:17532–17537

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13:283–296

    Article  PubMed  CAS  Google Scholar 

  • Gaboli M, Kotsi PA, Gurrieri C, Cattoretti G, Ronchetti S, Cordon-Cardo C, Broxmeyer HE, Hromas R, Pandolfi PP (2001) Mzf1 controls cell proliferation and tumorigenesis. Genes Dev 15:1625–1630

    Article  PubMed  CAS  Google Scholar 

  • Georgiades P, Watkins M, Surani MA, Ferguson-Smith AC (2000) Parental origin-specific developmental defects in mice with uniparental disomy for chromosome 12. Development 127:4719–4728

    PubMed  CAS  Google Scholar 

  • Greiner EF, Kirfel J, Greschik H, Huang D, Becker P, Kapfhammer JP, Schüle R (2000) Differential ligand-dependent protein-protein interactions between nuclear receptors and a neuronal-specific cofactor. Proc Natl Acad Sci USA 97:7160–7165

    Article  PubMed  CAS  Google Scholar 

  • Heidmann O, Vernochet C, Dupressoir A, Heidmann T (2009) Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new “syncytin” in a third order of mammals. Retrovirology 6:107

    Article  PubMed  Google Scholar 

  • Herniou E, Martin J, Miller K, Cook J, Wilkinson M, Tristem M (1998) Retroviral diversity and distribution in vertebrates. J Virol 72:5955–5966

    PubMed  CAS  Google Scholar 

  • Hishida T, Naito K, Osada S, Nishizuka M, Imagawa M (2007) Peg10, an imprinted gene, plays a crucial role in adipocyte differentiation. FEBS Lett 581:4272–4278

    Article  PubMed  CAS  Google Scholar 

  • Ikeda H, Sugimura H (1989) Fv-4 resistance gene: a truncated endogenous murine leukemia virus with ecotropic interference properties. J Virol 63:5405–5412

    PubMed  CAS  Google Scholar 

  • Ivanov D, Stone JR, Maki JL, Collins T, Wagner G (2005) Mammalian SCAN domain dimer is a domain-swapped homolog of the HIV capsid C-terminal domain. Mol Cell 17:137–143

    Article  PubMed  CAS  Google Scholar 

  • Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20:1313–1326

    Article  PubMed  CAS  Google Scholar 

  • Kagami M, Yamazawa K, Matsubara K, Matsuo N, Ogata T (2008) Placentomegaly in paternal uniparental disomy for human chromosome 14. Placenta 29:760–761

    Article  PubMed  CAS  Google Scholar 

  • Kainz B, Shehata M, Bilban M, Kienle D, Heintel D, Krömer-Holzinger E, Le T, Kröber A, Heller G, Schwarzinger I, Demirtas D, Chott A, Döhner H, Zöchbauer-Müller S, Fonatsch C, Zielinski C, Stilgenbauer S, Gaiger A, Wagner O, Jäger U (2007) Overexpression of the paternally expressed gene 10 (PEG10) from the imprinted locus on chromosome 7q21 in high-risk B-cell chronic lymphocytic leukemia. Int J Cancer 121:1984–1993

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3:e181

    Article  PubMed  Google Scholar 

  • Krylov DM, Koonin EV (2001) A novel family of predicted retroviral-like aspartyl proteases with a possible key role in eukaryotic cell cycle control. Curr Biol 11:R584–R587

    Article  PubMed  CAS  Google Scholar 

  • Kuroiwa Y, Kaneko-Ishino T, Kagitani F, Kohda T, Li LL, Tada M, Suzuki R, Yokoyama M, Shiroishi T, Wakana S, Barton SC, Ishino F, Surani MA (1996) Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nat Genet 12:186–190

    Article  PubMed  CAS  Google Scholar 

  • Li LL, Szeto IY, Cattanach BM, Ishino F, Surani MA (2000) Organization and parent-of-origin-specific methylation of imprinted Peg3 gene on mouse proximal chromosome 7. Genomics 63:333–340

    Article  PubMed  CAS  Google Scholar 

  • Li CM, Margolin AA, Salas M, Memeo L, Mansukhani M, Hibshoosh H, Szabolcs M, Klinakis A, Tycko B (2006) PEG10 is a c-MYC target gene in cancer cells. Cancer Res 66:665–672

    Article  PubMed  CAS  Google Scholar 

  • Linggi MS, Burke TL, Williams BB, Harrington A, Kraemer R, Hempstead BL, Yoon SO, Carter BD (2005) Neurotrophin receptor interacting factor (NRIF) is an essential mediator of apoptotic signaling by the p75 neurotrophin receptor. J Biol Chem 280:13801–13808

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Bei D, Parmar H, Matus A (2000) Activity-regulated, cytoskeleton-associated protein (Arc) is essential for visceral endoderm organization during early embryogenesis. Mech Dev 92:207–215

    Article  PubMed  CAS  Google Scholar 

  • Lloréns C, Marín I (2001) A mammalian gene evolved from the integrase domain of an LTR retrotransposon. Mol Biol Evol 18:1597–1600

    Article  PubMed  Google Scholar 

  • Lux A, Beil C, Majety M, Barron S, Gallione CJ, Kuhn HM, Berg JN, Kioschis P, Marchuk DA, Hafner M (2005) Human retroviral gag- and gag-pol-like proteins interact with the transforming growth factor-beta receptor activin receptor-like kinase 1. J Biol Chem 280:8482–8493

    Article  PubMed  CAS  Google Scholar 

  • Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14:433–445

    Article  PubMed  CAS  Google Scholar 

  • Malik HS (2012) Retroviruses push the envelope for mammalian placentation. Proc Natl Acad Sci USA 109:2184–2185

    Article  PubMed  CAS  Google Scholar 

  • Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318

    Article  PubMed  CAS  Google Scholar 

  • Mangeney M, Renard M, Schlecht-Louf G, Bouallaga I, Heidmann O, Letzelter C, Richaud A, Ducos B, Heidmann T (2007) Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc Natl Acad Sci USA 104:20534–20539

    Article  PubMed  CAS  Google Scholar 

  • Manktelow E, Shigemoto K, Brierley I (2005) Characterization of the frameshift signal of Edr, a mammalian example of programmed −1 ribosomal frameshifting. Nucleic Acids Res 33:1553–1563

    Article  PubMed  CAS  Google Scholar 

  • Marco A, Marín I (2009) CGIN1: a retroviral contribution to mammalian genomes. Mol Biol Evol 26:2167–2170

    Article  PubMed  CAS  Google Scholar 

  • Marín I (2010) GIN transposons: genetic elements linking retrotransposons and genes. Mol Biol Evol 27:1903–1911

    Article  PubMed  Google Scholar 

  • Matsui T, Kinoshita-Ida Y, Hayashi-Kisumi F, Hata M, Matsubara K, Chiba M, Katahira-Tayama S, Morita K, Miyachi Y, Tsukita S (2006) Mouse homologue of skin-specific retroviral-like aspartic protease involved in wrinkle formation. J Biol Chem 281:27512–27525

    Article  PubMed  CAS  Google Scholar 

  • Matsui T, Miyamoto K, Kubo A, Kawasaki H, Ebihara T, Hata K, Tanahashi S, Ichinose S, Imoto I, Inazawa J, Kudoh J, Amagai M (2011) SASPase regulates stratum corneum hydration through profilaggrin-to-filaggrin processing. EMBO Mol Med 3:320–333

    Article  PubMed  CAS  Google Scholar 

  • Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang XY, Edouard P, Howes S, Keith JC Jr, McCoy JM (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789

    Article  PubMed  CAS  Google Scholar 

  • Mura M, Murcia P, Caporale M, Spencer TE, Nagashima K, Rein A, Palmarini M (2004) Late viral interference induced by transdominant Gag of an endogenous retrovirus. Proc Natl Acad Sci USA 101:11117–11122

    Article  PubMed  CAS  Google Scholar 

  • Okabe H, Satoh S, Furukawa Y, Kato T, Hasegawa S, Nakajima Y, Yamaoka Y, Nakamura Y (2003) Involvement of PEG10 in human hepatocellular carcinogenesis through interaction with SIAH1. Cancer Res 63:3043–3048

    PubMed  CAS  Google Scholar 

  • Ono R, Kobayashi S, Wagatsuma H, Aisaka K, Kohda T, Kaneko-Ishino T, Ishino F (2001) A ­retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73:232–237

    Article  PubMed  CAS  Google Scholar 

  • Ono R, Nakamura K, Inoue K, Naruse M, Usami T, Wakisaka-Saito N, Hino T, Suzuki-Migishima R, Ogonuki N, Miki H, Kohda T, Ogura A, Yokoyama M, Kaneko-Ishino T, Ishino F (2006) Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet 38:101–106

    Article  PubMed  CAS  Google Scholar 

  • Ono R, Kuroki Y, Naruse M, Ishii M, Iwasaki S, Toyoda A, Fujiyama A, Shaw G, Renfree MB, Kaneko-Ishino T, Ishino F (2011) Identification of tammar wallaby SIRH12, derived from a marsupial-specific retrotransposition event. DNA Res 18:211–219

    Article  PubMed  CAS  Google Scholar 

  • Poulter RT, Goodwin TJ (2005) DIRS-1 and the other tyrosine recombinase retrotransposons. Cytogenet Genome Res 110:575–588

    Article  PubMed  CAS  Google Scholar 

  • Prudhomme S, Bonnaud B, Mallet F (2005) Endogenous retroviruses and animal reproduction. Cytogenet Genome Res 110:353–364

    Article  PubMed  CAS  Google Scholar 

  • Rawn SM, Cross JC (2008) The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol 24:159–181

    Article  PubMed  CAS  Google Scholar 

  • Ribet D, Harper F, Dupressoir A, Dewannieux M, Pierron G, Heidmann T (2008) An infectious progenitor for the murine IAP retrotransposon: emergence of an intracellular genetic parasite from an ancient retrovirus. Genome Res 18:597–609

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld MR, Eichen JG, Wade DF, Posner JB, Dalmau J (2001) Molecular and clinical diversity in paraneoplastic immunity to Ma proteins. Ann Neurol 50:339–348

    Article  PubMed  CAS  Google Scholar 

  • Sander TL, Stringer KF, Maki JL, Szauter P, Stone JR, Collins T (2003) The SCAN domain defines a large family of zinc finger transcription factors. Gene 310:29–38

    Article  PubMed  CAS  Google Scholar 

  • Schüller M, Jenne D, Voltz R (2005) The human PNMA family: novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol 169:172–176

    Article  PubMed  Google Scholar 

  • Seitz H, Youngson N, Lin SP, Dalbert S, Paulsen M, Bachellerie JP, Ferguson-Smith AC, Cavaillé J (2003) Imprinted microRNA genes transcribed antisense to a reciprocally imprinted ­retrotransposon-like gene. Nat Genet 34:261–262

    Article  PubMed  CAS  Google Scholar 

  • Sekita Y, Wagatsuma H, Nakamura K, Ono R, Kagami M, Wakisaka N, Hino T, Suzuki-Migishima R, Kohda T, Ogura A, Ogata T, Yokoyama M, Kaneko-Ishino T, Ishino F (2008) Role of ­retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet 40:243–248

    Article  PubMed  CAS  Google Scholar 

  • Smallwood A, Papageorghiou A, Nicolaides K, Alley MK, Jim A, Nargund G, Ojha K, Campbell S, Banerjee S (2003) Temporal regulation of the expression of syncytin (HERV-W), maternally imprinted PEG10, and SGCE in human placenta. Biol Reprod 69:286–293

    Article  PubMed  CAS  Google Scholar 

  • Søe K, Andersen TL, Hobolt-Pedersen AS, Bjerregaard B, Larsson LI, Delaissé JM (2011) Involvement of human endogenous retroviral syncytin-1 in human osteoclast fusion. Bone 48:837–846

    Article  PubMed  Google Scholar 

  • Steplewski A, Krynska B, Tretiakova A, Haas S, Khalili K, Amini S (1998) MyEF-3, a developmentally controlled brain-derived nuclear protein which specifically interacts with myelin basic protein proximal regulatory sequences. Biochem Biophys Res Commun 243:295–301

    Article  PubMed  CAS  Google Scholar 

  • Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, Wang C, Kohda T, Alsop AE, Marshall Graves JA, Kohara Y, Ishino F, Renfree MB, Kaneko-Ishino T (2007) Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 3:e55

    Article  PubMed  Google Scholar 

  • Tan KO, Tan KM, Chan SL, Yee KS, Bevort M, Ang KC, Yu VC (2001) MAP-1, a novel proapoptotic protein containing a BH3-like motif that associates with Bax through its Bcl-2 homology domains. J Biol Chem 276:2802–2807

    Article  PubMed  CAS  Google Scholar 

  • Tan KO, Fu NY, Sukumaran SK, Chan SL, Kang JH, Poon KL, Chen BS, Yu VC (2005) MAP-1 is a mitochondrial effector of Bax. Proc Natl Acad Sci USA 102:14623–14628

    Article  PubMed  CAS  Google Scholar 

  • Vernochet C, Heidmann O, Dupressoir A, Cornelis G, Dessen P, Catzeflis F, Heidmann T (2011) A syncytin-like endogenous retrovirus envelope gene of the guinea pig specifically expressed in the placenta junctional zone and conserved in Caviomorpha. Placenta 32:885–892

    Article  PubMed  CAS  Google Scholar 

  • Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28:913–922

    Article  PubMed  CAS  Google Scholar 

  • Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C (2003) Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678

    Article  PubMed  CAS  Google Scholar 

  • Voltz R, Gultekin SH, Rosenfeld MR, Gerstner E, Eichen J, Posner JB, Dalmau J (1999) A serologic marker of paraneoplastic limbic and brain-stem encephalitis in patients with testicular cancer. N Engl J Med 340:1788–1795

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Xiao Y, Hu Z, Chen Y, Liu N, Hu G (2008) PEG10 directly regulated by E2Fs might have a role in the development of hepatocellular carcinoma. FEBS Lett 582:2793–2798

    Article  PubMed  CAS  Google Scholar 

  • Wills NM, Moore B, Hammer A, Gesteland RF, Atkins JF (2006) A functional −1 ribosomal frameshift signal in the human paraneoplastic Ma3 gene. J Biol Chem 281:7082–7088

    Article  PubMed  CAS  Google Scholar 

  • Zdobnov EM, Campillos M, Harrington ED, Torrents D, Bork P (2005) Protein coding potential of retroviruses and other transposable elements in vertebrate genomes. Nucleic Acids Res 33:946–954

    Article  PubMed  CAS  Google Scholar 

  • Zhou QY, Huang JN, Xiong YZ, Zhao SH (2007) Imprinting analyses of the porcine GATM and PEG10 genes in placentas on days 75 and 90 of gestation. Genes Genet Syst 82:265–269

    Article  PubMed  CAS  Google Scholar 

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Our work is supported by grants from the Agence Nationale de la Recherche (ANR).

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Chalopin, D., Tomaszkiewicz, M., Galiana, D., Volff, JN. (2012). LTR Retroelement-Derived Protein-Coding Genes and Vertebrate Evolution. In: Witzany, G. (eds) Viruses: Essential Agents of Life. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4899-6_13

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