Multiple alternative splicing and differential expression of dmrt1 during gonad transformation of the rice field eel

Biology of Reproduction

Volumn 73, Issue 5, 2005, Pages 1017-1024

  Huang, Xiao ^a   Guo, Yiqing ^a   Shui, Yi ^a   Gao, Shang ^a   Yu, Hongshi ^a   Cheng, Hanhua ^a   Zhou, Rongjia ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Alternative splicing; Developmental biology; dsx; Fish; Ovary; Sexual development; Testis

Indexed keywords

ISOPROTEIN; PROTEIN; PROTEIN DMRT1; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EEL; EPITHELIUM CELL; EVOLUTION; GENETIC TRANSCRIPTION; GONAD; HUMAN; LIFE CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE FIELD EEL; SEX DIFFERENCE; SEXUAL DEVELOPMENT; TELEOST; TESTIS;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; EELS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; MALE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; OVARY; SEQUENCE HOMOLOGY, AMINO ACID; SEX REVERSAL, GONADAL; TESTIS; TRANSCRIPTION FACTORS;

ANIMALIA; MONOPTERUS ALBUS; TELEOSTEI;

EID: 27144548432     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.105.041871     Document Type: Article

References (55)

1. Zarkower D. Establishing sexual dimorphism: conservation amidst diversity? Nature Rev Genet 2001; 2:175-185.
2. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990; 346:240-244.
3. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badgc R. Male development of chromosomally female mice transgenic for SRY. Nature 1991: 351:117-121.
4. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. A male-specific role for SOX9 in vertebrate sex determination. Development 1996; 122:2813-2822.
5. Morals da Silva S, Hacker A, Harlcy V, Goodfellow P, Swain A, Lovell-Badge R. Sox9 expression during gonudal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 1996; 14:62-68.
6. Western PS, Harry JL, Graves JA, Sinclair AH. Temperature-dependent sex determination: upregulation of SOX9 expression after commitment to male development. Dev Dyn 1999; 214:171-177.
7. Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harrison WR, Behringer RR, Overbeek PA. A transgenic insertion upstream of Sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet 2000; 26:490-494.
8. Vidai VP, Chaboissier MC, De Rooij DG, Schedl A. Sox9 induces testis development in XX transgenic mice. Nat Genet 2001; 28:216-217.
9. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. Evidence for evolutionary conservation of sex-determining genes. Nature 1998; 391:691-695.
10. Nanda I, Shan Z, Schartl M, Burl DW, Koehler M, Nothwang H, Grutzner F, Paton IR, Windsor D, Dunn I, Engel W, Staeheli P, Mizuno S, Haaf T, Schmid M. 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 1999; 21:258-259.
11. Raymond CS, Parker ED, Kettlewell JR, Brown LG, Page DC, Kusz K, Jaruzelska J, Reinbcrg Y, Flejter WL, Bardwell VJ, Hirsch B, Zarkower D. A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 1999; 8:989-996.
12. Smith CA, McClive PJ, Western PS, Reed KJ, Sinclair AH. Conservation of a sex-determining gene. Nature 1999; 402:601-602.
13. Guan G, Kobayashi T, Nagahama Y. Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domnin genes in a teleost fish, the Tilapia (Oreochromis niloticus). Biochem Biophys Res Commun 2000; 272:662-666.
14. Kettlewell JR, Raymond CS, Zarkower D. Temperature-dependent expression of turtle Dmrt1 before sexual differentiation. Genesis 2000; 26:174-178.
15. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre J, Bernot A, Laudet V, Guiguen Y. DMRT1 expression during gonadal differentiation and spennatogenesis in the rainbow trout. Oncorhynchus mykiss. Biochim Biophys Acta 2000; 1493:180-187.
16. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 2000; 14:2587-2595.
17. Ohbayashi F, Suzuki MG, Mita K, Okano K, Shimada T. A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp Biochem Phys B 2001; 128:145-158.
18. Hodgkin J. The remarkable ubiquity of DM domain factors as regulators of sexual phenotype: ancestry or aptitude? Gen Dev 2002; 16: 2322-2326.
19. Shihata K, Takase M, Nakamura M. The Dmrt1 expression in sex-reversed gonuds of amphibians. Gen Comp Endocrinol 2002; 127: 232-241.
20. Ottolenghi C, Veitia R, Quintuna-Murci L, Torchard D, Scapoli L, Souleyreau-Therville N, Beckmann J, Fellous M, McElreavey K. The region on 9p associated with 46. XY sex reversal contains several transcripts expressed in the urogenital system and a novel doublesex-related domain. Genomics 2000; 64:170-178.
21. Flejter WL, Fergestad J, Gorski J, Varvill T Chandrasekharappa S. A gene involved in XY sex reversal is located on chromosome 9, distal to marker D9SI779. Am J Hum Genet 1998; 63:794-802.
22. Guioli S, Schmitt K, Critcher R, Bouzyk M, Spurr NK, Ogata T, Hoo JJ, Pinsky L, Gimelli G, Pasztor L, Goodlellow PN. Molecular analysis of 9p deletions associated with XY sex reversal: refining the localization of a sex-determining gene to the tip of the chromosome. Am J Hum Genet 1998; 63:905-908.
23. Moniot B, Berta P, Scherer G, Sudbeck P, Poulat F. Male specific-expression suggests role of DMRT1 in human sex determination. Mech Dev 2000; 91:323-325.
24. 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.
25. De Grandi A, Calvari V, Bertini V, Bulfone A, Peverali G, Camerino G, Borsani G, Guioli S. The expression pattern of a mouse doublesex-related gene is consistent with a role in gonadal differentiation. Mech Dev 2000; 90:323-326.
26. Matsuda M, Nagahama Y, Shinotniya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the nicdaka fish. Nature 2002; 417: 559-563.
27. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shun Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 2002;99:1778-11783.
28. Zhang J. Evolution of DMY, a newly emergent male sex-determination gene of medaka fish. Genetics 2004; 166:1887-1895.
29. Nanda I, Zend-Ajusch E, Shan Z, Grutzner F, Schartl M, Burt DW, Koehler M, Fowler VM, Goodwin G, Schneider WJ, Mizuno S, Dechant G, Haaf T, Schmid M. Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRTI: a comparative (re)view on avian sex determination. Cytogenet Cell Genet 2000; 89:67-78.
30. Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T. Sex-specific expression of an evolutionary conserved male regulatory gene, DMRTI, in birds. Cytogenet Cell Genet 2000; 89:252-257.
31. Huang X, Cheng H, Guo Y, Liu L, Gui J, Zhou R. A conserved family of doublescx-related genes from fishes. J Exp Zool 2002; 294:63-67.
32. Chcng H, Guo Y, Yu Q, Zhou R. The rice field eel as a model system for vertebrate sexual development. Cytogenet Genome Res 2003; 101: 274-277.
33. Burtis KC, Baker BS. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 1989; 56:997-1010.
34. Narendra U, Zhu L, Li B, Wilken J, Weiss MA. Sex-specific gene-regulation. The doublesex DM motif is a bipartite DNA-binding domain. J Biol Chem 2002; 277:43463-43473.
35. Guo Y, Cheng H, Huang X, Gao S, Yu H, Zhou R. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem Biophys Res Commun 2005; 330:950-957.
36. Kriventseva EV, Koch I, Apweiler R, Vingron M, Bork P, Gelfand MS, Sunyaev S. Increase of functional diversity by alternative splicing. Trends Genet 2003; 19:124-128.
37. Ottolenghi C, Veitia R, Barbieri M, Fellous M, McElreavey K. The human doublesex-related gene, DMRT2, is homologous to a gene involved in somitogenesis and encodes a potential bicistronic transcript. Genomics 2000; 64:179-186.
38. Sreenivasulu K, Ganesh S, Raman R. Evolutionarily conserved, DMRTl, encodes alternatively spliced transcripts and shows dimorphic expression during gonadal differentiation in the lizard, Caloles versicolor. Gene Expr Patterns 2002; 2:51-60.
39. Lulfalla G, Roest Crollius H, Brunet FG, Laudet V, Robinson-Rechavi M. Inventing a sex-specific gene: a conserved role of DMRT1 in teleost fishes plus a recent duplication in the medaka Oryzias latipes resulted in DMY. J Mol Evol 2003; 57(Suppl 1):S148-S153.
40. Miller SW, Hayward DC, Bunch TA, Miller DJ, Ball EE, Bardwell VJ, Zarkower D, Brower DL. A DM domain protein from a coral, Acropora millepom, homologous to proteins important for sex determination. Evol Dev 2003; 5:251-258.
41. Suzuki MG, Ohbayashi F, Mita K, Shimada T. The mechanism of sex-specific splicing at the doublesex gene is different between Drosophila melanogaster and Bombyx mori. Insect Biochem Mol Biol 2001; 31: 1201-1211.
42. Yi W, Zarkower D. Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 1999; 126:873-881.
43. Yi W, Ross JM, Zarkower D. Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 2000; 127:4469-4480.
44. Burtis KC, Coschigano KT, Baker BS, Wensink PC. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J 1991; 10:2577-2582.
45. Coschigano KT, Wensink PC. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev 1993; 7:42-54.
46. Christiansen AE, Keisman EL, Ahmad SM, Baker BS. Sex comes in from the cold: the integration of sex and pattern. Trends Genet 2002; 18:510-516.
47. Garrett-Engele CM, Siegal ML, Manoli DS, Williams BC, Li H, Baker BS. Intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation. Development 2002; 129: 4661-4675.
48. Chen JK, Heckert LL. Dmrt1 expression is regulated by follicle-stimulating hormone and phorbol esters in postnatal Sertoli cells. Endocrinology 2001; 142:1167-1178.
49. Lei N, Heckert LL. Sp1 and Egr1 regulate transcription of the Dmrt1 gene in Sertoli cells. Biol Reprod 2002: 66:675-684.
50. Larsson SH, Charlieu JP, Miyagawa K, Engelkamp D, Rassoulzadegan M, Ross A, Cuzin F, van Heyningen V, Hastie ND. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell 1995; 81:391-401.
51. Davies RC, Calvio C, Bratt E, Larsson SH, Lainond AI, Hastie ND. WT1 interacts with the splicing factor U2AF65 in an isoform-dependent manner and can be incorporated into spliceosomes. Genes Dev 1998; 12:3217-3225.
52. Little NA, Hastie ND, Davies RC. Identification of WTAP, a novel Wilms' tumour 1-associating protein. Hum Mol Genet 2000; 9:2231-2239.
53. Ohe K, Lalli E, Sassone-Corsi P. A direct role of SRY and SOX proteins in pre-mRNA splicing. Proc Natl Acad Sci U S A 2002; 99: 1146-1151.
54. Zhou Z, Licklider LJ, Gygi SP, Reed R. Comprehensive proteomic analysis of the human spliceosome. Nature 2002; 419:182-185.
55. Lalli E, Ohe K, Latorre E, Bianchi ME, Sassone-Corsi P. Sexy splicing: regulatory interplays governing sex determination from Drosophilla to mammals. J Cell Science 2003; 116:441-445.