Manipulation of estrogen synthesis alters MIR202* expression in embryonic chicken gonads

Biology of Reproduction

Volumn 85, Issue 1, 2011, Pages 22-30

  Bannister, Stephanie C ^a,c   Smith, Craig A ^b,c   Roeszler, Kelly N ^b   Doran, Timothy J ^a   Sinclair, Andrew H ^b,c   Tizard, Mark L V ^a  

^a CSIRO   (Australia)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aromatase inhibitor; Chicken embryo; E2; Estradiol 17 ; Estradiol estradiol receptor; Estrogen; Gonad; MicroRNA MIR202*; Sex determination; Testis

Indexed keywords

AROMATASE; AROMATASE INHIBITOR; ESTRADIOL; MICRORNA; MICRORNA 202; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ESTROGEN SYNTHESIS; FEMALE; GONAD; MALE; MASCULINITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENTIATION; SEX TRANSFORMATION; TESTICULAR FEMINIZATION; UPREGULATION;

ANIMALS; CHICK EMBRYO; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; MALE; MICRORNAS; SEX DIFFERENTIATION; UP-REGULATION;

SPONDIAS PURPUREA; VERTEBRATA;

EID: 79960125227     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.088476     Document Type: Article

References (46)

1. Smith CA, Sinclair AH. Sex determination: insights from the chicken. Bioessays 2004; 26:120-132.
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. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009; 461:267-271.
4. 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.
5. Smith CA, McClive PJ, Western PS, Reed KJ, Sinclair AH. Conservation of a sex-determining gene. Nature 1999; 402:601-602.
6. Elbrecht A, Smith RG. Aromatase enzyme activity and sex determination in chickens. Science 1992; 255:467-470.
7. Vaillant S, Dorizzi M, Pieau C, Richard-Mercier N. Sex reversal and aromatase in chicken. J Exp Zool 2001; 290:727-740.
8. 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.
9. 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.
10. Shimada K. Gene expression of steroidogenic enzymes in chicken embryonic gonads. J Exp Zool 1998; 281:450-456.
11. Bruggeman V, Van As P, Decuypere E. Developmental endocrinology of the reproductive axis in the chicken embryo. Comp Biochem Physiol A Mol Integr Physiol 2002; 131:839-846.
12. Hudson QJ, Smith CA, Sinclair AH. Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Dev Dyn 2005; 233:1052-1055.
13. 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.
14. Willier BH, Gallagher TF, Koch FC. Sex-modification in the chick embryo resulting from injections of male and female hormones. Proc Natl Acad Sci U S A 1935; 21:625-631.
15. Akazome Y, Mori T. Evidence of sex reversal in the gonads of chicken embryos after oestrogen treatment as detected by expression of lutropin receptor. J Reprod Fertil 1999; 115:9-14.
16. Bannister SC, Tizard ML, Doran TJ, Sinclair AH, Smith CA. Sexually dimorphic microRNA expression during chicken embryonic gonadal development. Biol Reprod 2009; 81:165-176.
17. McFarlane L, Wilhelm D. Non-coding RNAs in mammalian sexual development. Sex Dev 2009; 3:302-316.
18. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75:843-854.
19. Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993; 75:855-862.
20. Shi Y, Jin Y. MicroRNA in cell differentiation and development. Sci China C Life Sci 2009; 52:205-211.
21. Yan N, Lu Y, Sun H, Qiu W, Tao D, Liu Y, Chen H, Yang Y, Zhang S, Li X, Ma Y. Microarray profiling of microRNAs expressed in testis tissues of developing primates. J Assist Reprod Genet 2009; 26:179-186.
22. Yan N, Lu Y, Sun H, Tao D, Zhang S, Liu W, Ma Y. A microarray for microRNA profiling in mouse testis tissues. Reproduction 2007; 134:73- 79.
23. Kim GJ, Georg I, Scherthan H, Merkenschlager M, Guillou F, Scherer G, Barrionuevo F. Dicer is required for Sertoli cell function and survival. Int J Dev Biol 2009; 54:867-875.
24. Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, Schaad O, Vejnar CE, Kuhne F, Descombes P, Zdobnov EM, McManus MT, Guillou F, Harfe BD, Yan W, Jegou B, Nef S. Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 2009; 326:250-259.
25. Huang CC, Yao HH. Inactivation of Dicer1 in steroidogenic factor 1-positive cells reveals tissue-specific requirement for Dicer1 in adrenal, testis, and ovary. BMC Dev Biol 2010; 10:66.
26. Mishima T, Takizawa T, Luo SS, Ishibashi O, Kawahigashi Y, Mizuguchi Y, Ishikawa T, Mori M, Kanda T, Goto T, Takizawa T. MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 2008; 136:811-822.
27. Ro S, Park C, Sanders KM, McCarrey JR, Yan W. Cloning and expression profiling of testis-expressed microRNAs. Dev Biol 2007; 311:592-602.
28. Ro S, Song R, Park C, Zheng H, Sanders KM, Yan W. Cloning and expression profiling of small RNAs expressed in the mouse ovary. RNA 2007; 13:2366-2380.
29. Takada S, Berezikov E, Choi YL, Yamashita Y, Mano H. Potential role of miR-29b in modulation of Dnmt3a and Dnmt3b expression in primordial germ cells of female mouse embryos. RNA 2009; 15:1507-1514.
30. Huang P, Gong Y, Peng X, Li S, Yang Y, Feng Y. Cloning, identification, and expression analysis at the stage of gonadal sex differentiation of chicken miR-363 and 363*. Acta Biochim Biophys Sin (Shanghai) 2010; 42:522-529.
31. Gasc JM. Estrogen target cells in gonads of the chicken embryo during sexual differentiation. J Embryol Exp Morphol 1980; 55:331-342.
32. 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.
33. Clinton M, Haines L, Belloir B, McBride D. Sexing chick embryos: a rapid and simple protocol. Br Poult Sci 2001; 42:134-138.
34. Shi R, Chiang VL. Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 2005; 39:519-525.
35. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3:1101-1108.
36. Andrews JE, Smith CA, Sinclair AH. Sites of estrogen receptor and aromatase expression in the chicken embryo. Gen Comp Endocrinol 1997; 108:182-190.
37. Ason B, Darnell DK, Wittbrodt B, Berezikov E, Kloosterman WP, Wittbrodt J, Antin PB, Plasterk RH. Differences in vertebrate microRNA expression. Proc Natl Acad Sci U S A 2006; 103:14385-14389.
38. Ro S, Park C, Young D, Sanders KM, Yan W. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res 2007; 35:5944-5953.
39. Liang Y, Ridzon D, Wong L, Chen C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 2007; 8:166.
40. Michalak P, Malone JH. Testis-derived microRNA profiles of African clawed frogs (Xenopus) and their sterile hybrids. Genomics 2008; 91:158- 164.
41. Murchison EP, Tovar C, Hsu A, Bender HS, Kheradpour P, Rebbeck CA, Obendorf D, Conlan C, Bahlo M, Blizzard CA, Pyecroft S, Kreiss A, Kellis M, Stark A, Harkins TT, Marshall Graves JA, Woods GM, Hannon GJ, Papenfuss AT. The Tasmanian devil transcriptome reveals Schwann cell origins of a clonally transmissible cancer. Science 2010; 327:84-87.
42. Mittwoch U. Phenotypic manifestations during the development of the dominant and default gonads in mammals and birds. J Exp Zool 1998; 281:466-471.
43. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. A malespecific role for SOX9 in vertebrate sex determination. Development 1996; 122:2813-2822.
44. 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.
45. Smith CA, McClive PJ, Hudson Q, Sinclair AH. Male-specific cell migration into the developing gonad is a conserved process involving PDGF signalling. Dev Biol 2005; 284:337-350.
46. 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.