Analysis of gene function in cultured embryonic mouse gonads using nucleofection

Sexual Development

Volumn 5, Issue 1, 2011, Pages 7-15

  Ryan, J ^a,b   Ludbrook, L ^a   Wilhelm, D ^c   Sinclair, A ^d   Koopman, P ^c   Bernard, P ^a   Harley, V R ^a  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

Author keywords

DNA delivery; Nucleofection; Organ culture; Sex determination; SOX9; SRY gonads

Indexed keywords

MAMMALIA;

FORKHEAD TRANSCRIPTION FACTOR; FOXL2 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; SOX9 PROTEIN, MOUSE; SRY PROTEIN, MOUSE; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR SOX9;

ANIMAL; ARTICLE; DRUG ANTAGONISM; EMBRYO CULTURE; FEMALE; GENDER AND SEX; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; MOUSE; OVARY; PRENATAL DEVELOPMENT; SEX DIFFERENTIATION; SRY GENE; TESTIS;

ANIMALS; EMBRYO CULTURE TECHNIQUES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GENES, SRY; GREEN FLUORESCENT PROTEINS; MALE; MICE; OVARY; RECOMBINANT FUSION PROTEINS; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; SEX-DETERMINING REGION Y PROTEIN; SOX9 TRANSCRIPTION FACTOR; TESTIS; TRANSFECTION;

EID: 79551529473     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000322162     Document Type: Article

References (41)

1. Bagheri-Fam S, Sim H, Bernard P, Jayakody I, Taketo MM, Scherer G, Harley VR: Loss of Fgfr2 leads to partial XY sex reversal. Dev Biol 314:71-83 (2008).
2. Barrionuevo F, Bagheri-Fam S, Klattig J, Kist R, Taketo MM, Englert C, Scherer G: Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod 74:195-201 (2006).
3. Behringer RR, Finegold MJ, Cate RL: Mullerianinhibiting substance function during mammalian sexual development. Cell 79:415-425 (1994).
4. Bernard P, Sim H, Knower K, Vilain E, Harley V: Human SRY inhibits beta-catenin-mediated transcription. Int J Biochem Cell Biol 40:2889-2900 (2008).
5. Chassot AA, Ranc F, Gregoire EP, Roepers-Gajadien HL, Taketo MM, et al: Activation of beta-catenin signaling by RSPO1 controls differentiation of the mammalian ovary. Hum Mol Genet 17:1264-1277 (2008).
6. Coveney D, Cool J, Oliver T, Capel B: Four-dimensional analysis of vascularization during primary development of an organ, the gonad. Proc Natl Acad Sci U S A 105:7212-7217 (2008).
7. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, et al: The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/ epicanthus inversus syndrome. Nat Genet 27:159-166 (2001).
8. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, et al: Direct Interaction of SRY-Related Protein SOX9 and Steroidogenic Factor 1 Regulates Transcription of the Human Anti-Müllerian Hormone Gene. Mol Cell Biol 18:6653-6665 (1998).
9. Forbes K, Desforges M, Garside R, Aplin JD, Westwood M: Methods for siRNA-mediated reduction of mRNA and protein expression in human placental explants, isolated primary cells and cell lines. Placenta 30:124-129 (2009).
10. Hersmus R, de Leeuw BH, Stoop H, Bernard P, van Doorn HC, et al: A novel SRY missense mutation affecting nuclear import in a 46, XY female patient with bilateral gonadoblastoma. Eur J Hum Genet 17:1642-1649 (2009).
11. Hughes IA, Houk C, Ahmed SF, Lee PA: Consensus statement on management of intersex disorders. J Pediatr Urol 2:148-162 (2006).
12. Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, et al: FGF9 and WNT4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 4: e187 (2006).
13. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R: Male development of chromosomally female mice transgenic for Sry. Nature 351:117-121 (1991).
14. Lau YF, Li Y: The human and mouse sex-determining SRY genes repress the Rspol/betacatenin signaling. J Genet Genomics 36:193-202 (2009).
15. Maatouk DM, DiNapoli L, Alvers A, Parker KL, Taketo MM, Capel B: Stabilization of betacatenin in XY gonads causes male-to-female sex-reversal. Hum Mol Genet 17:2949-2955 (2008).
16. Malki S, Nef S, Notarnicola C, Thevenet L, Gasca S, et al: Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J 24:1798-1809 (2005).
17. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B: Male-specific cell migration into the developing gonad. Curr Biol 7:958-968 (1997).
18. McLaren A, Buehr M: Development of mouse germ cells in cultures of fetal gonads. Cell Differ Dev 31:185-195 (1990).
19. Meachem SJ, Ruwanpura SM, Ziolkowski J, Ague JM, Skinner MK, Loveland KL: Developmentally distinct in vivo effects of FSH on proliferation and apoptosis during testis maturation. J Endocrinol 186:429-446 (2005).
20. Merchant-Larios H, Moreno-Mendoza N, Buehr M: The role of the mesonephros in cell differentiation and morphogenesis of the mouse fetal testis. Int J Dev Biol 37:407-415 (1993).
21. Merkerova M, Klamova H, Brdicka R, Bruchova H: Targeting of gene expression by siRNA in CML primary cells. Mol Biol Rep 34:27-33 (2007).
22. Nakamura Y, Yamamoto M, Matsui Y: Introduction and expression of foreign genes in cultured mouse embryonic gonads by electroporation. Reprod Fertil Dev 14:259-265 (2002).
23. Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, et al: Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet 14:2053-2062 (2005).
24. Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, et al: Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 16:2795-2804 (2007).
25. Palmer SJ, Burgoyne PS: In situ analysis of fetal, prepuberal and adult XX-XY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112:265-268 (1991).
26. Ross AJ, Capel B: Signaling at the crossroads of gonad development. Trends Endocrinol Metab 16:19-25 (2005).
27. Ross AJ, Tilman C, Yao H, MacLaughlin D, Capel B: AMH induces mesonephric cell migration in XX gonads. Mol Cell Endocrinol 211:1-7 (2003).
28. Schmahl J, Kim Y, Colvin JS, Ornitz DM, Capel B: Fgf9 induces proliferation and nuclear localization of FGFR2 in Sertoli precursors during male sex determination. Development 131:3627-3636 (2004).
29. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier AC, Treier M: The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131:933-942 (2004).
30. Seiffert M, Stilgenbauer S, Dohner H, Lichter P: Efficient nucleofection of primary human B cells and B-CLL cells induces apoptosis, which depends on the microenvironment and on the structure of transfected nucleic acids. Leukemia 21:1977-1983 (2007).
31. Sekido R, Lovell-Badge R: Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930-934 (2008).
32. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, et al: A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240-244 (1990).
33. Svingen T, Wilhelm D, Combes AN, Hosking B, Harley VR, Sinclair AH, Koopman P: Ex vivo magnetofection: A novel strategy for the study of gene function in mouse organogenesis. Dev Dyn 238:956-964 (2009).
34. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, et al: Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139:1130-1142 (2009).
35. Wilhelm D, Martinson F, Bradford S, Wilson MJ, Combes AN, et al: Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev Biol 287:111-124 (2005).
36. Wilhelm D, Hiramatsu R, Mizusaki H, Widjaja L, Combes AN, Kanai Y, Koopman P: SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 282:10553-10560 (2007).
37. Wilhelm D, Washburn LL, Truong V, Fellous M, Eicher EM, Koopman P: Antagonism of the testis-and ovary-determining pathways during ovotestis development in mice. Mech Dev 126:324-336 (2009).
38. Xiao WL, Shi B, Zheng Q, Wang Y, Huang L, et al: Nucleofection is highly efficient for transfecting genes into murine embryonic palatal mesenchymal cells in primary culture. Int J Oral Maxillofac Surg 36:429-434 (2007).
39. Zaragosi LE, Billon N, Ailhaud G, Dani C: Nucleofection is a valuable transfection method for transient and stable transgene expression in adipose tissue-derived stem cells. Stem Cells 25:790-797 (2007).
40. Zeitelhofer M, Vessey JP, Xie Y, Tubing F, Thomas S, Kiebler M, Dahm R: High-efficiency transfection of mammalian neurons via nucleofection. Nat Protoc 2:1692-1704 (2007).
41. Zheng W, Izaki J, Furusawa S, Yoshimura Y: A sensitive non-radioactive in situ hybridization method for the detection of chicken IgG gamma-chain mRNA: A technique suitable for detecting of variety of mRNAs in tissue sections. Biol Proced Online 3:1-7 (2001).