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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
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
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
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
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
Best S, Le Tissier P, Towers G, Stoye JP (1996) Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382:826–829
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
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
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
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
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
Campillos M, Doerks T, Shah PK, Bork P (2006) Computational characterization of multiple Gag-like human proteins. Trends Genet 22:585–589
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
Chen HL, D’Mello SR (2010) Induction of neuronal cell death by paraneoplastic Ma1 antigen. J Neurosci Res 88:3508–3519
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
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
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
Darnell RB, Posner JB (2006) Paraneoplastic syndromes affecting the nervous system. Semin Oncol 33:270–298
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
de la Chaux N, Wagner A (2011) BEL/Pao retrotransposons in metazoan genomes. BMC Evol Biol 11:154
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
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
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
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
Edelstein LC, Collins T (2005) The SCAN domain family of zinc finger transcription factors. Gene 359:1–17
Eickbush TH (1997) Telomerase and retrotransposons: which came first? Science 277:911–912
Emerson RO, Thomas JH (2011) Gypsy and the birth of the SCAN domain. J Virol 85:12043–12052
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
Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13:283–296
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
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
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
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
Herniou E, Martin J, Miller K, Cook J, Wilkinson M, Tristem M (1998) Retroviral diversity and distribution in vertebrates. J Virol 72:5955–5966
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
Ikeda H, Sugimura H (1989) Fv-4 resistance gene: a truncated endogenous murine leukemia virus with ecotropic interference properties. J Virol 63:5405–5412
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
Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20:1313–1326
Kagami M, Yamazawa K, Matsubara K, Matsuo N, Ogata T (2008) Placentomegaly in paternal uniparental disomy for human chromosome 14. Placenta 29:760–761
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
Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3:e181
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
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
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
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
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
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
Lloréns C, Marín I (2001) A mammalian gene evolved from the integrase domain of an LTR retrotransposon. Mol Biol Evol 18:1597–1600
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
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
Malik HS (2012) Retroviruses push the envelope for mammalian placentation. Proc Natl Acad Sci USA 109:2184–2185
Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318
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
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
Marco A, Marín I (2009) CGIN1: a retroviral contribution to mammalian genomes. Mol Biol Evol 26:2167–2170
Marín I (2010) GIN transposons: genetic elements linking retrotransposons and genes. Mol Biol Evol 27:1903–1911
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
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
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
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
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
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
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
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
Poulter RT, Goodwin TJ (2005) DIRS-1 and the other tyrosine recombinase retrotransposons. Cytogenet Genome Res 110:575–588
Prudhomme S, Bonnaud B, Mallet F (2005) Endogenous retroviruses and animal reproduction. Cytogenet Genome Res 110:353–364
Rawn SM, Cross JC (2008) The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol 24:159–181
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
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
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
Schüller M, Jenne D, Voltz R (2005) The human PNMA family: novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol 169:172–176
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
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
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
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
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
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
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
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
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
Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28:913–922
Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C (2003) Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678
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
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
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
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
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
Acknowledgements
Our work is supported by grants from the Agence Nationale de la Recherche (ANR).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
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
Download citation
DOI: https://doi.org/10.1007/978-94-007-4899-6_13
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-4898-9
Online ISBN: 978-94-007-4899-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)