Evolution and gene capture in ancient endogenous retroviruses - insights from the crocodilian genomes

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Chong, Amanda Y ^a   Kojima, Kenji K ^b   Jurka, Jerzy ^b   Ray, David A ^c,d   Smit, Arian F ^e   Isberg, Sally R ^a,f   Gongora, Jaime ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b Genetic Information Research Institute   (United States)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

^d TEXAS TECH UNIVERSITY   (United States)

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^f Centre for Crocodile Research   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; MESSENGER RNA; NECTIN 3; STEM CELL FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; CROCODILIAN; ENDOGENOUS RETROVIRUS; ENDOGENOUS RETROVIRUS 3; ENDOGENOUS RETROVIRUS 4; EVOLUTION; GENE CAPTURE; GENE EXPRESSION; GENETIC PARAMETERS; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; HOST RANGE; NONHUMAN; PHYLOGENY; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; TURTLE; VIRUS CLASSIFICATION; VIRUS REPLICATION; ANIMAL; BIOLOGY; CLASSIFICATION; CLUSTER ANALYSIS; GENETIC RECOMBINATION; GENETICS; GENOME; MOLECULAR EVOLUTION; VIROLOGY;

CROCODYLIDAE (ALL CROCODILES); MAMMALIA; TESTUDINES; VERTEBRATA;

ALLIGATORS AND CROCODILES; ANIMALS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; ENDOGENOUS RETROVIRUSES; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME; PHYLOGENY; RECOMBINATION, GENETIC; SEQUENCE HOMOLOGY; TURTLES;

EID: 84924230064     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0071-2     Document Type: Article

References (76)

1. Herniou E, Martin J, Miller K, Cook J, Wilkinson M, Tristem M: Retroviral diversity and distribution in vertebrates. J Virol 1998, 72:5955-5966.
2. Jaratlerdsiri W, Rodríguez-Zárate CJ, Isberg SR, Damayanti CS, Miles LG, Chansue N, Moran C, Melville L, Gongora J: Distribution of Endogenous Retroviruses in Crocodilians. J Virol 2009, 83:10305-10308.
3. Martin J, Herniou E, Cook J, O'Neill RW, Tristem M: Interclass transmission and phyletic host tracking in murine leukemia virus-related retroviruses. J Virol 1999, 73:2442-2449.
4. Chong AYY, Atkinson SJ, Isberg S, Gongora J: Strong purifying selection in endogenous retroviruses in the saltwater crocodile ( Crocodylus porosus ) in the Northern Territory of Australia. Mobile DNA 2012, 3:20.
5. Martin J, Kabat P, Herniou E, Tristem M: Characterization and complete nucleotide sequence of an unusual reptilian retrovirus recovered from the Order Crocodylia. J Virol 2002, 76:4651-4654.
6. St John JA, Braun EL, Isberg SR, Miles LG, Chong AY, Gongora J, Dalzell P, Moran C, Bed'hom B, Abzhanov A, Burgess SC, Cooksey AM, Castoe TA, Crawford NG, Densmore LD, Drew JC, Edwards SV, Faircloth BC, Fujita MK, Greenwold MJ, Hoffmann FG, Howard JM, Iguchi T, Janes DE, Khan SY, Kohno S, de Koning AJ, Lance SL, McCarthy FM, McCormack JE, et al: Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes. Genome Biol 2012, 13:415.
7. Hugall AF, Foster R, Lee MSY: Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Syst Biol 2007, 56:543-563.
8. Roos J, Aggarwal RK, Janke A: Extended mitogenomic phylogenetic analyses yield new insight into crocodylian evolution and their survival of the Cretaceous-Tertiary boundary. Mol Phylogenet Evol 2007, 45:663-673.
9. Jern P, Sperber GO, Blomberg J: Use of endogenous retroviral sequences (ERVs) and structural markers for retroviral phylogenetic inference and taxonomy. Retrovirology 2005, 2:50.
10. Blomberg J, Benachenhou F, Blikstad V, Sperber G, Mayer J: Classification and nomenclature of endogenous retroviral sequences (ERVs): problems and recommendations. Gene 2009, 448:115-123.
11. Polavarapu N, Bowen N, McDonald J: Identification, characterization and comparative genomics of chimpanzee endogenous retroviruses. Genome Biol 2006, 7:R51.
12. Bannert N, Kurth R: The evolutionary dynamics of human endogenous retroviral families. Annu Rev Genomics Hum Genet 2006, 7:149-173.
13. 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 U S A 2004, 101:4894-4899.
14. Katzourakis A, Rambaut A, Pybus OG: The evolutionary dynamics of endogenous retroviruses. Trends Microbiol 2005, 13:463-468.
15. Belshaw R, Katzourakis A, Paces J, Burt A, Tristem M: High copy number in human endogenous retrovirus families is associated with copying mechanisms in addition to reinfection. Mol Biol Evol 2005, 22:814-817.
16. Gifford R, Tristem M: The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 2003, 26:291-316.
17. Jurka J, Bao W, Kojima KK: Families of transposable elements, population structure and the origin of species. Biol Direct 2011, 6:1-16.
18. Muriaux D, Rein A: Encapsidation and transduction of cellular genes by retroviruses. Front Biosci 2003, 8:D135-D142.
19. Katz RA, Skalka AM: Generation of diversity in retroviruses. Annu Rev Genet 1990, 24:409-445.
20. LaPierre LA, Casey JW, Holzschu DL: Walleye Retroviruses Associated with Skin Tumors and Hyperplasias Encode Cyclin D Homologs. J Virol 1998, 72:8765-8771.
21. Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, Vandewege MW, St John JA, Capella-Gutiérrez S, Castoe TA, Kern C, Fujita MK, Opazo JC, Jurka J, Kojima KK, Caballero J, Hubley RM, Smit AF, Platt RN, Lavoie CA, Ramakodi MP, Finger JW Jr, Suh A, Isberg SR, Miles L, Chong AY, Jaratlerdsiri W, Gongora J, Moran C, Iriarte A, et al: Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science. Submitted.
22. Blikstad V, Benachenhou F, Sperber GO, Blomberg J: Evolution of human endogenous retroviral sequences: a conceptual account. Cell Mol Life Sci 2008, 65:3348-3365.
23. Harshman J, Huddleston CJ, Bollback JP, Parsons TJ, Braun MJ: True and false gharials: A nuclear gene phylogeny of Crocodylia. Syst Biol 2003, 52:386-402.
24. Llorens C, Fares M, Moya A: Relationships of gag-pol diversity between Ty3/Gypsy and Retroviridae LTR retroelements and the three kings hypothesis. BMC Evol Biol 2008, 8:276.
25. Carré-Eusèbe D, Coudouel N, Magre S: OVEX1, a novel chicken endogenous retrovirus with sex-specific and left-right asymmetrical expression in gonads. Retrovirology 2009, 6:59.
26. Tristem M, Myles T, Hill F: A Highly Divergent Retroviral Sequence in the Tuatara ( Sphenodon ). Virology 1995, 210:206-211.
27. Kojima KK, Jurka J: LTR retrotransposons from the western painted turtle. Rep Base Reports 2013, 13:1931-1934.
28. Kapitonov VV, Jurka J, Kapitonov VV, Jurka J: A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 2008, 9:411-412. author reply 414.
29. Rebollo R, Horard B, Hubert B, Vieira C: Jumping genes and epigenetics: Towards new species. Gene 2010, 454:1-7.
30. Oliver KR, Greene WK: Transposable elements: powerful facilitators of evolution. Bioessays 2009, 31:703-714.
31. Benit L, Lallemand JB, Casella JF, Philippe H, Heidmann T: ERV-L elements: a family of endogenous retrovirus-like elements active throughout the evolution of mammals. J Virol 1999, 73:3301-3308.
32. Barrio AM, Ekerljung M, Jern P, Benachenhou F, Sperber GO, Bongcam-Rudloff E, Blomberg J, Andersson G: The first sequenced carnivore genome shows complex host-endogenous retrovirus relationships. PLoS One 2011, 6.
33. Alfoldi J, Di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, Russell P, Lowe CB, Glor RE, Jaffe JD, Ray DA, Boissinot S, Shedlock AM, Botka C, Castoe TA, Colbourne JK, Fujita MK, Moreno RG, ten Hallers BF, Haussler D, Heger A, Heiman D, Janes DE, Johnson J, de Jong PJ, Koriabine MY, Lara M, Novick PA, Organ CL, Peach SE, et al: The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 2011, 477:587-591.
34. Garcia-Etxebarria K, Jugo BM: Genome-wide detection and characterization of endogenous retroviruses in Bos taurus. J Virol 2010, 84:10852-10862.
35. Huda A, Polavarapu N, Jordan IK, McDonald JF: Endogenous retroviruses of the chicken genome. Biol Direct 2008, 3.
36. Mandal PK, Kazazian HH Jr: SnapShot: vertebrate transposons. Cell 2008, 135:192-192. e191.
37. Gentles AJ, Wakefield MJ, Kohany O, Gu W, Batzer MA, Pollock DD, Jurka J: Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res 2007, 17:992-1004.
38. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, et al: The genome of the western clawed frog Xenopus tropicalis. Science 2010, 328:633-636.
39. Kim H-S, Takenaka O, Crow TJ: Isolation and phylogeny of endogenous retrovirus sequences belonging to the HERV-W family in primates. J Gen Virol 1999, 80:2613-2619.
40. Johnson WE, Coffin JM: Constructing primate phylogenies from ancient retrovirus sequences. Proc Natl Acad Sci U S A 1999, 96:10254-10260.
41. Xiong Y, Eickbush TH: Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol 1988, 5:675-690.
42. Xiong Y, Eickbush TH: Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 1990, 9:3353-3362.
43. King AM, Adams MJ, Lefkowitz EJ, Carstens EB: Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. London: Elsevier; 2012.
44. Butler M, Goodwin T, Simpson M, Singh M, Poulter R: Vertebrate LTR retrotransposons of the Tf1/Sushi group. J Mol Evol 2001, 52:260-274.
45. Schwartz DE, Tizard R, Gilbert W: Nucleotide sequence of rous sarcoma virus. Cell 1983, 32:853-869.
46. Swanstrom R, Parker RC, Varmus HE, Bishop JM: Transduction of a cellular oncogene: the genesis of Rous sarcoma virus. Proc Natl Acad Sci U S A 1983, 80:2519-2523.
47. LaPierre LA, Holzschu DL, Bowser PR, Casey JW: Sequence and transcriptional analyses of the fish retroviruses walleye epidermal hyperplasia virus types 1 and 2: evidence for a gene duplication. J Virol 1999, 73:9393-9403.
48. Huang E, Nocka K, Beier DR, Chu T-Y, Buck J, Lahm H-W, Wellner D, Leder P, Besmer P: The hematopoietic growth factor KL is encoded by the SI locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell 1990, 63:225-233.
49. Williams DE, Eisenman J, Baird A, Rauch C, Van Ness K, March CJ, Park LS, Martin U, Mochizukl DY, Boswell HS: Identification of a ligand for the c-kit proto-oncogene. Cell 1990, 63:167-174.
50. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, Atkins HL, Hsu R-Y, Birkett NC, Okino KH, Murdock DC: Stem cell factor is encoded at the SI locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 1990, 63:213-224.
51. Huang EJ, Nocka KH, Buck J, Besmer P: Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol Biol Cell 1992, 3:349-362.
52. Kanetsky PA, Mitra N, Vardhanabhuti S, Li M, Vaughn DJ, Letrero R, Ciosek SL, Doody DR, Smith LM, Weaver J, Albano A, Chen C, Starr JR, Rader DJ, Godwin AK, Reilly MP, Hakonarson H, Schwartz SM, Nathanson KL: Common variation in KITLG and at 5q31.3 predisposes to testicular germ cell cancer. Nat Genet 2009, 41:811-815.
53. Rapley EA, Turnbull C, Al Olama AA, Dermitzakis ET, Linger R, Huddart RA, Renwick A, Hughes D, Hines S, Seal S, Morrison J, Nsengimana J, Deloukas P, Testicular Cancer Collaboration UK, Rahman N, Bishop DT, Easton DF, Stratton MR: A genome-wide association study of testicular germ cell tumor. Nat Genet 2009, 41:807-810.
54. Karyadi DM, Karlins E, Decker B, Von Holdt BM, Carpintero-Ramirez G, Parker HG, Wayne RK, Ostrander EA: A copy number variant at the KITLG locus likely confers risk for canine squamous cell carcinoma of the digit. PLoS Genet 2013, 9:e1003409.
55. Besmer P, Murphy JE, George PC, Qiu F, Bergold PJ, Lederman L, Snyder HW, Brodeur D, Zuckerman EE, Hardy WD: A new acute transforming feline retrovirus and relationship of its oncogene v-kit with the protein kinase gene family. Nature 1986, 320:415-421.
56. Hultman KA, Bahary N, Zon LI, Johnson SL: Gene duplication of the zebrafish kit ligand and partitioning of melanocyte development functions to kit ligand a. PLoS Genet 2007, 3:e17.
57. Reymond N, Borg JP, Lecocq E, Adelaide J, Campadelli-Fiume G, Dubreuil P, Lopez M: Human nectin3/PRR3: a novel member of the PVR/PRR/nectin family that interacts with afadin. Gene 2000, 255:347-355.
58. Fabre S, Reymond N, Cocchi F, Menotti L, Dubreuil P, Campadelli-Fiume G, Lopez M: Prominent role of the Ig-like V domain in trans-interactions of nectins. Nectin3 and nectin 4 bind to the predicted C-C'-C"-D beta-strands of the nectin1 V domain. J Biol Chem 2002, 277:27006-27013.
59. Sperber GO, Airola T, Jern P, Blomberg J: Automated recognition of retroviral sequences in genomic data-RetroTector©. Nucleic Acids Res 2007, 35:4964-4976.
60. Bao Z, Eddy SR: Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 2002, 12:1269-1276.
61. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
62. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
63. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL: NCBI BLAST: a better web interface. Nucleic Acids Res 2008, 36:W5-W9.
64. Kohany O, Gentles A, Hankus L, Jurka J: Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 2006, 7:474.
65. Martin J, Herniou E, Cook J, Oneill RW, Tristem M: Human endogenous retrovirus type I-related viruses have an apparently widespread distribution within vertebrates. J Virol 1997, 71:437-443.
66. Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33:511-518.
67. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
68. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
69. Bolisetty M, Blomberg J, Benachenhou F, Sperber G, Beemon K: Unexpected diversity and expression of avian endogenous retroviruses. MBio 2012, 3.
70. Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, Aguilar-Rodríguez J, Vicente-Ripolles M, Fuster G, Bernet GP: The Gypsy Database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res 2011, 39:D70-D74.
71. Dimmic MW, Rest JS, Mindell DP, Goldstein RA: rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J Mol Evol 2002, 55:65-73.
72. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
73. Anisimova M, Gascuel O: Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006, 55:539-552.
74. Kimura M: A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980, 16:111-120.
75. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
76. Wan Q-H, Pan S-K, Hu L, Zhu Y, Xu P-W, Xia J-Q, Chen H, He G-Y, He J, Ni X-W, et al: Genome analysis and signature discovery for diving and sensory properties of the endangered Chinese alligator. Cell Res 2013, 23:1091-1105.