OVEX1, a novel chicken endogenous retrovirus with sex-specific and left-right asymmetrical expression in gonads

Retrovirology

Volumn 6, Issue , 2009, Pages

  Carré Eusèbe, Danièle ^a,b   Coudouel, Noëlline ^c   Magre, Solange ^c  

^a Faculté de Médecine   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Groupe Hospitalier Pitié Salpêtrière   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GAG PROTEIN; MESSENGER RNA; POL PROTEIN; POLYPROTEIN; PROTEIN ORF3; PROTEIN OVEXI; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANIMAL VIRUS; ARTICLE; CELL LINEAGE; CHICKEN; CONTROLLED STUDY; DESQUAMATION; EMBRYO; ENDOGENOUS RETROVIRUS; ESTROGEN SYNTHESIS; FEMALE; FINCH; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE LOCUS; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; GONAD DEVELOPMENT; GRANULOSA CELL; IN SITU HYBRIDIZATION; LONG TERMINAL REPEAT; MALE; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OVARY FOLLICLE DEVELOPMENT; PHYLOGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES COMPARISON; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; TRANSIENT EXPRESSION; VERTICAL TRANSMISSION; VIRUS EXPRESSION; VIRUS TRANSMISSION; ANIMAL; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METHODOLOGY; MOLECULAR GENETICS; NUCLEIC ACID HYBRIDIZATION; OVARY; PHYSIOLOGY; TESTIS; VIROLOGY;

AVES; GALLUS GALLUS; TAENIOPYGIA GUTTATA;

ANIMALS; CHICKENS; CLUSTER ANALYSIS; ENDOGENOUS RETROVIRUSES; FEMALE; GENE EXPRESSION PROFILING; MALE; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; OPEN READING FRAMES; OVARY; PHYLOGENY; RNA, MESSENGER; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; TESTIS; VIRAL PROTEINS;

EID: 68449102355     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-6-59     Document Type: Article

References (91)

1. Smith CA Sinclair AH Sex determination: Insights from the chicken Bioessays 2004, 26:120-132 14745830
2. Schmid M Nanda I Hoehn H Schartl M Haaf T Buerstedde JM Arakawa H Caldwell RB Weigend S Burt DW et al Second report on chicken genes and chromosomes 2005 Cytogenet Genome Res 2005, 109:415-479 15905640
3. Merchant-Larios HPL Reyss-Brion M Early morphogenesis of chick gonad in the absence of mesonephros Dev Growth Differ 1984, 26:403-417
4. Oreal E Mazaud S Picard JY Magre S Carre-Eusebe D Different patterns of anti-Mullerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads Dev Dyn 2002, 225:221-232 12412004
5. Kudo T Sutou S Molecular cloning of chicken FTZ-F1-related orphan receptors Gene 1997, 197:261-268 9332374
6. Smith CA Smith MJ Sinclair AH Expression of chicken steroidogenic factor-1 during gonadal sex differentiation Gen Comp Endocrinol 1999, 113:187-196 10082621
7. Oreal E Pieau C Mattei MG Josso N Picard JY Carre-Eusebe D Magre S Early expression of AMH in chicken embryonic gonads precedes testicular SOX9 expression Dev Dyn 1998, 212:522-532 9707325
8. Van Limborgh J Le premier indice de la differenciation sexuelle des gonades chez l'embryon de poulet Archives d Anatomie Microscopique et de Morphologie Experimentale 1968, 57:79-90 5691501
9. Andrews JE Smith CA Sinclair AH Sites of estrogen receptor and aromatase expression in the chicken embryo Gen Comp Endocrinol 1997, 108:182-190 9356214
10. Nakabayashi O Kikuchi H Kikuchi T Mizuno S Differential expression of genes for aromatase and estrogen receptor during the gonadal development in chicken embryos J Mol Endocrinol 1998, 20:193-202 9584834
11. Reed KJ Sinclair AH FET-1: A novel W-linked, female specific gene up-regulated in the embryonic chicken ovary Mech Dev 2002, 119(Suppl 1):S87-90 14516666
12. Hoshino A Koide M Ono T Yasugi S Sex-specific and left-right asymmetric expression pattern of Bmp7 in the gonad of normal and sex-reversed chicken embryos Dev Growth Differ 2005, 47:65-74 15771626
13. Smith CA Shoemaker CM Roeszler KN Queen J Crews D Sinclair AH Cloning and expression of R-Spondin1 in different vertebrates suggests a conserved role in ovarian development BMC Dev Biol 2008, 8:72 2519078 18651984
14. Guioli S Lovell-Badge R PITX2 controls asymmetric gonadal development in both sexes of the chick and can rescue the degeneration of the right ovary Development 2007, 134:4199-4208 17959721
15. Ishimaru Y Komatsu T Kasahara M Katoh-Fukui Y Ogawa H Toyama Y Maekawa M Toshimori K Chandraratna RA Morohashi K Yoshioka H Mechanism of asymmetric ovarian development in chick embryos Development 2008, 135:677-685 18199582
16. Rodriguez-Leon J Rodriguez Esteban C Marti M Santiago-Josefat B Dubova I Rubiralta X Izpisua Belmonte JC Pitx2 regulates gonad morphogenesis Proc Natl Acad Sci USA 2008, 105:11242-11247 2516275 18678914
17. Yoshioka H Meno C Koshiba K Sugihara M Itoh H Ishimaru Y Inoue T Ohuchi H Semina EV Murray JC et al Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry Cell 1998, 94:299-305 9708732
18. Morais da Silva S Hacker A Harley V Goodfellow P Swain A Lovell-Badge R Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds Nat Genet 1996, 14:62-68 8782821
19. Kent J Wheatley SC Andrews JE Sinclair AH Koopman P A male-specific role for SOX9 in vertebrate sex determination Development. 1996, 122(9):2813-2822 8787755
20. Shan Z Nanda I Wang Y Schmid M Vortkamp A Haaf T Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds Cytogenet Cell Genet 2000, 89:252-257 10965136
21. Raymond CS Kettlewell JR Hirsch B Bardwell VJ Zarkower D Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development Dev Biol 1999, 215:208-220 10545231
22. Nishikimi H Kansaku N Saito N Usami M Ohno Y Shimada K Sex differentiation and mRNA expression of P450c17, P450arom and AMH in gonads of the chicken Mol Reprod Dev 2000, 55:20-30 10602270
23. Yoshida K Shimada K Saito N Expression of P450(17 alpha) hydroxylase and P450 aromatase genes in the chicken gonad before and after sexual differentiation Gen Comp Endocrinol 1996, 102:233-240 8998967
24. Nomura O Nakabayashi O Nishimori K Yasue H Mizuno S Expression of five steroidogenic genes including aromatase gene at early developmental stages of chicken male and female embryos J Steroid Biochem Mol Biol 1999, 71:103-109 10659698
25. Scheib D Effects and role of estrogens in avian gonadal differentiation Differentiation 1983, 23(Suppl):S87-92 6444180
26. Elbrecht A Smith RG Aromatase enzyme activity and sex determination in chickens Science 1992, 255:467-470 1734525
27. Vaillant S Dorizzi M Pieau C Richard-Mercier N Sex reversal and aromatase in chicken J Exp Zool 2001, 290:727-740 11748621
28. Govoroun MS Pannetier M Pailhoux E Cocquet J Brillard JP Couty I Batellier F Cotinot C Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development Dev Dyn 2004, 231:859-870 15517586
29. Smith CA Roeszler KN Bowles J Koopman P Sinclair AH Onset of meiosis in the chicken embryo; evidence of a role for retinoic acid BMC Dev Biol 2008, 8:85 2564928 18799012
30. Wallenburg J [Macroscopy, light and electron microscopy studies on the genesis and function of the gonads after experimental sex-reversal following left-side ovariectomy of hen chicks (Gallus domesticus)] Gegenbaurs Morphol Jahrb 1982, 128:463-529 6891351
31. ICGSC Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution Nature 2004, 432:695-716 15592404
32. Huda A Polavarapu N Jordan IK McDonald JF Endogenous retroviruses of the chicken genome Biol Direct 2008, 3:9 2329609 18361801
33. Jern P Coffin JM Effects of retroviruses on host genome function Annu Rev Genet 2008, 42:709-732 18694346
34. Gifford R Kabat P Martin J Lynch C Tristem M Evolution and distribution of class II-related endogenous retroviruses J Virol 2005, 79:6478-6486 1091674 15858031
35. 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 1224870 16092962
36. 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 16093699
37. Diatchenko L Lukyanov S Lau YF Siebert PD Suppression subtractive hybridization: A versatile method for identifying differentially expressed genes Methods Enzymol 1999, 303:349-380 10349654
38. Haas NB Grabowski JM Sivitz AB Burch JB Chicken repeat 1 (CR1) elements, which define an ancient family of vertebrate non-LTR retrotransposons, contain two closely spaced open reading frames Gene 1997, 197:305-309 9332379
39. Schattner P Brooks AN Lowe TM The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs Nucleic Acids Res 2005, 33:W686-689 1160127 15980563
40. Amendt BA Sutherland LB Semina EV Russo AF The molecular basis of Rieger syndrome. Analysis of Pitx2 homeodomain protein activities J Biol Chem 1998, 273:20066-20072 9685346
41. Kozak M Pushing the limits of the scanning mechanism for initiation of translation Gene 2002, 299:1-34 12459250
42. Hart D Frerichs GN Rambaut A Onions DE Complete nucleotide sequence and transcriptional analysis of snakehead fish retrovirus J Virol 1996, 70:3606-3616 190236 8648695
43. Benit L De Parseval N Casella JF Callebaut I Cordonnier A Heidmann T Cloning of a new murine endogenous retrovirus, MuERV-L, with strong similarity to the human HERV-L element and with a gag coding sequence closely related to the Fv1 restriction gene J Virol 1997, 71:5652-5657 191811 9188643
44. Hicks GR Raikhel NV Protein import into the nucleus: An integrated view Annu Rev Cell Dev Biol 1995, 11:155-188 8689555
45. Lupas A Van Dyke M Stock J Predicting coiled coils from protein sequences Science. 1991, 252(5010):1162-1164
46. Yoshinaka Y Katoh I Copeland TD Oroszlan S Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon Proc Natl Acad Sci USA 1985, 82:1618-1622 397323 3885215
47. Tristem M Myles T Hill F A highly divergent retroviral sequence in the tuatara (Sphenodon) Virology 1995, 210:206-211 7540785
48. Doolittle RF Feng DF Johnson MS McClure MA Origins and evolutionary relationships of retroviruses Q Rev Biol 1989, 64:1-30 2469098
49. 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 112974 10516048
50. Jacobo-Molina A Ding J Nanni RG Clark AD Jr Lu X Tantillo C Williams RL Kamer G Ferris AL Clark P et al Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA Proc Natl Acad Sci USA 1993, 90:6320-6324 46920 7687065
51. Johnson MS McClure MA Feng DF Gray J Doolittle RF Computer analysis of retroviral pol genes: Assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes Proc Natl Acad Sci USA 1986, 83:7648-7652 386778 2429313
52. Malik HS Eickbush TH Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses Genome Res 2001, 11:1187-1197 11435400
53. Kulkosky J Jones KS Katz RA Mack JP Skalka AM Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases Mol Cell Biol 1992, 12:2331-2338 364405 1314954
54. Dimcheff DE Krishnan M Mindell DP Evolution and characterization of tetraonine endogenous retrovirus: A new virus related to avian sarcoma and leukosis viruses J Virol 2001, 75:2002-2009 115148 11160701
55. de Parseval N Lazar V Casella JF Benit L Heidmann T Survey of human genes of retroviral origin: Identification and transcriptome of the genes with coding capacity for complete envelope proteins J Virol 2003, 77:10414-10422 228468 12970426
56. Benit L Dessen P Heidmann T Identification, phylogeny, and evolution of retroviral elements based on their envelope genes J Virol 2001, 75:11709-11719 114757 11689652
57. Cordonnier A Casella JF Heidmann T Isolation of novel human endogenous retrovirus-like elements with foamy virus-related pol sequence J Virol 1995, 69:5890-5897 189468 7543594
58. Xiong Y Eickbush T Origin and evolution of retroelements based upon their reverse transcriptase sequences Embo J 1990, 9:3353-3362 552073 1698615
59. Herniou E Martin J Miller K Cook J Wilkinson M Tristem M Retroviral diversity and distribution in vertebrates J Virol 1998, 72:5955-5966 110400 9621058
60. Acloque H Risson V Birot AM Kunita R Pain B Samarut J Identification of a new gene family specifically expressed in chicken embryonic stem cells and early embryo Mech Dev 2001, 103:79-91 11335114
61. Mazaud S Oreal E Guigon CJ Carre-Eusebe D Magre S Lhx9 expression during gonadal morphogenesis as related to the state of cell differentiation Gene Expr Patterns 2002, 2:373-377 12617828
62. Tsunekawa N Naito M Sakai Y Nishida T Noce T Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells Development 2000, 127:2741-2750 10821771
63. Hudson QJ Smith CA Sinclair AH Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary Dev Dyn 2005, 233:1052-1055 15830351
64. Oulad-Abdelghani M Bouillet P Decimo D Gansmuller A Heyberger S Dolle P Bronner S Lutz Y Chambon P Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene J Cell Biol 1996, 135:469-477 2121034 8896602
65. Ch'in Suang H Gaginskaia ER Kalinina EI [Characteristics of oogenesis in the chick. I. The extrafollicular period in the development of the oocytes] Ontogenez 1979, 10:340-349 481849
66. Vaillant S Magre S Dorizzi M Pieau C Richard-Mercier N Expression of AMH, SF1, and SOX9 in gonads of genetic female chickens during sex reversal induced by an aromatase inhibitor Dev Dyn 2001, 222:228-237 11668600
67. Smith CA Katz M Sinclair AH DMRT1 is upregulated in the gonads during female-to-male sex reversal in ZW chicken embryos Biol Reprod 2003, 68:560-570 12533420
68. Pereira SL Baker AJ A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock Mol Biol Evol 2006, 23:1731-1740 16774978
69. Wang Z Miyake T Edwards SV Amemiya CT Tuatara (Sphenodon) genomics: BAC library construction, sequence survey, and application to the DMRT gene family J Hered 2006, 97:541-548 17135461
70. Villesen P Aagaard L Wiuf C Pedersen FS Identification of endogenous retroviral reading frames in the human genome Retrovirology 2004, 1:32 524368 15476554
71. Nei M Gojobori T Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions Mol Biol Evol 1986, 3:418-426 3444411
72. Mank JE Axelsson E Ellegren H Fast-X on the Z: Rapid evolution of sex-linked genes in birds Genome Res 2007, 17:618-624 1855182 17416747
73. Motta PM Makabe S Nottola SA The ultrastructure of human reproduction. I. The natural history of the female germ cell: Origin, migration and differentiation inside the developing ovary Hum Reprod Update 1997, 3:281-295 9322103
74. Shen CH Steiner LA Genome structure and thymic expression of an endogenous retrovirus in zebrafish J Virol 2004, 78:899-911 368747 14694121
75. Wang-Johanning F Liu J Rycaj K Huang M Tsai K Rosen DG Chen DT Lu DW Barnhart KF Johanning GL Expression of multiple human endogenous retrovirus surface envelope proteins in ovarian cancer Int J Cancer 2007, 120:81-90 17013901
76. Lee YK Chew A Phan H Greenhalgh DG Cho K Genome-wide expression profiles of endogenous retroviruses in lymphoid tissues and their biological properties Virology 2008, 373:263-273 2427371 18187179
77. Mi S Lee X Li X Veldman GM Finnerty H Racie L LaVallie E Tang XY Edouard P Howes S et al Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis Nature 2000, 403:785-789 10693809
78. Blaise S de Parseval N Benit L Heidmann T Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution Proc Natl Acad Sci USA 2003, 100:13013-13018 240736 14557543
79. Dupressoir A Marceau G Vernochet C Benit L Kanellopoulos C Sapin V Heidmann T Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae Proc Natl Acad Sci USA 2005, 102:725-730 545540 15644441
80. Dunlap KA Palmarini M Varela M Burghardt RC Hayashi K Farmer JL Spencer TE Endogenous retroviruses regulate periimplantation placental growth and differentiation Proc Natl Acad Sci USA 2006, 103:14390-14395 1599973 16980413
81. Yang KT Lin CY Huang HL Liou JS Chien CY Wu CP Huang CW Ou BR Chen CF Lee YP et al Expressed transcripts associated with high rates of egg production in chicken ovarian follicles Mol Cell Probes 2008, 22:47-54 17692502
82. Hamburger V Hamilton HL A series of normal stages in the development of the chick embryo. 1951 Dev Dyn 1992, 195:231-272 1304821
83. Eusebe D di Clemente N Rey R Pieau C Vigier B Josso N Picard JY Cloning and expression of the chick anti-Mullerian hormone gene J Biol Chem 1996, 271:4798-4804 8617748
84. 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 308517 7984417
85. Saitou N Nei M The neighbor-joining method: A new method for reconstructing phylogenetic trees Mol Biol Evol 1987, 4:406-425 3447015
86. Howe K Bateman A Durbin R QuickTree: Building huge Neighbour-Joining trees of protein sequences Bioinformatics 2002, 18:1546-1547 12424131
87. Perriere G Gouy M WWW-query: An on-line retrieval system for biological sequence banks Biochimie 1996, 78:364-369 8905155
88. Kyte J Doolittle RF A simple method for displaying the hydropathic character of a protein J Mol Biol 1982, 157:105-132 7108955
89. Marck C 'DNA Strider': A 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers Nucleic Acids Res 1988, 16:1829-1836 338177 2832831
90. Korber B HIV Signature and Sequence Variation Analysis. Computational Analysis of HIV Molecular Sequences Kluwer Academic Publishers. Dordrecht, Netherlands Allen G Rodrigo, Gerald H Learn 2000.
91. Pereira SL Baker AJ A molecular timescale for galliform birds accounting for uncertainty in time estimates and heterogeneity of rates of DNA substitutions across lineages and sites Mol Phylogenet Evol 2006, 38:499-509 16112881