Membrane β-catenin and adherens junctions in early gonadal patterning

Developmental Dynamics

Volumn 241, Issue 11, 2012, Pages 1782-1798

  Fleming, Alice ^a   Ghahramani, Negar ^a   Zhu, Maggie Xiaoming ^a,b   Délot, Emmanuèle C ^a   Vilain, Eric ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

catenin; Adherens junction; Cadherin; Gonad; P120 catenin; Patterning; Sex development; Wnt4

Indexed keywords

BETA CATENIN; CADHERIN; MEMBRANE PROTEIN;

ARTICLE; CELL ADHESION; CELL JUNCTION; CELL SELECTION; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO; GONAD DEVELOPMENT; MORPHOGENESIS; MOUSE; NONHUMAN; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENTIATION; TESTIS DEVELOPMENT;

ADHERENS JUNCTIONS; ANIMALS; BETA CATENIN; FEMALE; GONADS; IMMUNOHISTOCHEMISTRY; MALE; MICE; WNT4 PROTEIN;

MAMMALIA;

EID: 84867692332     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23870     Document Type: Article

References (62)

1. Bendel-Stenzel MR, Gomperts M, Anderson R, Heasman J, Wylie C. 2000. The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91: 143-152.
2. Bernard P, Harley VR. 2007. Wnt4 action in gonadal development and sex determination. Int J Biochem Cell Biol 39: 31-43.
3. Bernard P, Fleming A, Lacombe A, Harley VR, Vilain E. 2008. Wnt4 inhibits beta-catenin/TCF signalling by redirecting beta-catenin to the cell membrane. Biol Cell 100: 167-177.
4. Birk OS, Casiano DE, Wassif CA, Cogliati T, Zhao L, Zhao Y, Grinberg A, Huang S, Kreidberg JA, Parker KL, Porter FD, Westphal H. 2000. The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 403: 909-913.
5. Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD. 1989. Genetically haploid spermatids are phenotypically diploid. Nature 337: 373-376.
6. Brembeck FH, Rosario M, Birchmeier W. 2006. Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr Opin Genet Dev 16: 51-59.
7. Brennan J, Tilmann C, Capel B. 2003. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 17: 800-810.
8. Bullejos M, Bowles J, Koopman P. 2002. Extensive vascularization of developing mouse ovaries revealed by caveolin-1 expression. Dev Dyn 225: 95-99.
9. Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E. 2003. The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 162: 1111-1122.
10. Chang H, Gao F, Guillou F, Taketo MM, Huff V, Behringer RR. 2008. Wt1 negatively regulates beta-catenin signaling during testis development. Development 135: 1875-1885.
11. Chassot AA, Ranc F, Gregoire EP, Roepers-Gajadien HL, Taketo MM, Camerino G, de Rooij DG, Schedl A, Chaboissier MC. 2008. Activation of beta-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Hum Mol Genet 17: 1264-1277.
12. Combes AN, Wilhelm D, Davidson T, Dejana E, Harley V, Sinclair A, Koopman P. 2009. Endothelial cell migration directs testis cord formation. Dev Biol 326: 112-120.
13. Cool J, DeFalco TJ, Capel B. 2011. Vascular-mesenchymal cross-talk through Vegf and Pdgf drives organ patterning. Proc Natl Acad Sci U S A 108: 167-172.
14. Coveney D, Cool J, Oliver T, Capel B. 2008. Four-dimensional analysis of vascularization during primary development of an organ, the gonad. Proc Natl Acad Sci U S A 105: 7212-7217.
15. DeFalco T, Capel B. 2009. Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu Rev Cell Dev Biol 25: 457-482.
16. DeFalco T, Takahashi S, Capel B. 2011. Two distinct origins for Leydig cell progenitors in the fetal testis. Dev Biol 352: 14-26.
17. Derycke LD, Bracke ME. 2004. N-cadherin in the spotlight of cell-cell adhesion, differentiation, embryogenesis, invasion and signalling. Int J Dev Biol 48: 463-476.
18. Di Carlo A, De Felici M. 2000. A role for E-cadherin in mouse primordial germ cell development. Dev Biol 226: 209-219.
19. Duncan GS, Andrew DP, Takimoto H, Kaufman SA, Yoshida H, Spellberg J, Luis de la Pompa J, Elia A, Wakeham A, Karan-Tamir B, Muller WA, Senaldi G, Zukowski MM, Mak TW. 1999. Genetic evidence for functional redundancy of Platelet/Endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J Immunol 162: 3022-3030.
20. Fleming A, Vilain E. 2005. The endless quest for sex determination genes. Clin Genet 67: 15-25.
21. Foty RA, Steinberg MS. 2004. Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int J Dev Biol 48: 397-409.
22. Gassei K, Ehmcke J, Schlatt S. 2008. Initiation of testicular tubulogenesis is controlled by neurotrophic tyrosine receptor kinases in a three-dimensional Sertoli cell aggregation assay. Reproduction 136: 459-469.
23. Gumbiner BM. 2005. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6: 622-634.
24. Hacker A, Capel B, Goodfellow P, Lovell-Badge R. 1995. Expression of Sry, the mouse sex determining gene. Development 121: 1603-1614.
25. Halbleib JM, Nelson WJ. 2006. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-3214.
26. Harris TJ, Tepass U. 2010. Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11: 502-514.
27. Hartsock A, Nelson WJ. 2008. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778: 660-669.
28. Heuberger J, Birchmeier W. 2010. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2: a002915.
29. Hinck L, Nelson WJ, Papkoff J. 1994. Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing beta-catenin binding to the cell adhesion protein cadherin. J Cell Biol 124: 729-741.
30. Ilan N, Madri JA. 2003. PECAM-1: old friend, new partners. Curr Opin Cell Biol 15: 515-524.
31. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, Capel B, Swain A. 2003. Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130: 3663-3670.
32. Jeays-Ward K, Dandonneau M, Swain A. 2004. Wnt4 is required for proper male as well as female sexual development. Dev Biol 276: 431-440.
33. Kim KA, Wagle M, Tran K, Zhan X, Dixon MA, Liu S, Gros D, Korver W, Yonkovich S, Tomasevic N, Binnerts M, Abo A. 2008. R-Spondin family members regulate the Wnt pathway by a common mechanism. Mol Biol Cell 19: 2588-2596.
34. Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier MC, Poulat F, Behringer RR, Lovell-Badge R, Capel B. 2006. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 4: e187.
35. Kimura T, Nakamura T, Murayama K, Umehara H, Yamano N, Watanabe S, Taketo MM, Nakano T. 2006. The stabilization of beta-catenin leads to impaired primordial germ cell development via aberrant cell cycle progression. Dev Biol 300: 545-553.
36. Kopera IA, Bilinska B, Cheng CY, Mruk DD. 2010. Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 365: 1593-1605.
37. Lecuit T, Lenne PF. 2007. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8: 633-644.
38. Lee HJ, Pazin DE, Kahlon RS, Correa SM, Albrecht KH. 2009. Novel markers of early ovarian pre-granulosa cells are expressed in an Sry-like pattern. Dev Dyn 238: 812-825.
39. Lien WH, Klezovitch O, Vasioukhin V. 2006. Cadherin-catenin proteins in vertebrate development. Curr Opin Cell Biol 18: 499-506.
40. Lin LH, DePhilip RM. 1996. Sex-dependent expression of placental (P)-cadherin during mouse gonadogenesis. Anat Rec 246: 535-544.
41. Liu CF, Bingham N, Parker K, Yao HH. 2009. Sex-specific roles of beta-catenin in mouse gonadal development. Hum Mol Genet 18: 405-417.
42. Liu CF, Parker K, Yao HH. 2010. WNT4/beta-catenin pathway maintains female germ cell survival by inhibiting activin betaB in the mouse fetal ovary. PLoS One 5: e10382.
43. Loffler KA, Koopman P. 2002. Charting the course of ovarian development in vertebrates. Int J Dev Biol 46: 503-510.
44. Maatouk DM, DiNapoli L, Alvers A, Parker KL, Taketo MM, Capel B. 2008. Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum Mol Genet 17: 2949-2955.
45. Mackay S, Nicholson CL, Lewis SP, Brittan M. 1999. E-cadherin in the developing mouse gonad. Anat Embryol (Berl) 200: 91-102.
46. Manuylov NL, Smagulova FO, Leach L, Tevosian SG. 2008. Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 135: 3731-3743.
47. Murphy G, Gavrilovic J. 1999. Proteolysis and cell migration: creating a path? Curr Opin Cell Biol 11: 614-621.
48. Naillat F, Prunskaite-Hyyrylainen R, Pietila I, Sormunen R, Jokela T, Shan J, Vainio SJ. 2010. Wnt4/5a signalling coordinates cell adhesion and entry into meiosis during presumptive ovarian follicle development. Hum Mol Genet 19: 1539-1550.
49. Nelson WJ, Nusse R. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303: 1483-1487.
50. Panda DK, Miao D, Lefebvre V, Hendy GN, Goltzman D. 2001. The transcription factor SOX9 regulates cell cycle and differentiation genes in chondrocytic CFK2 cells. J Biol Chem 276: 41229-41236.
51. Pepling ME, Spradling AC. 1998. Female mouse germ cells form synchronously dividing cysts. Development 125: 3323-3328.
52. Perez-Moreno M, Fuchs E. 2006. Catenins: keeping cells from getting their signals crossed. Dev Cell 11: 601-612.
53. Radice GL, Ferreira-Cornwell MC, Robinson SD, Rayburn H, Chodosh LA, Takeichi M, Hynes RO. 1997. Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol 139: 1025-1032.
54. Rowlands TM, Symonds JM, Farookhi R, Blaschuk OW. 2000. Cadherins: crucial regulators of structure and function in reproductive tissues. Rev Reprod 5: 53-61.
55. Salomon D, Sacco PA, Roy SG, Simcha I, Johnson KR, Wheelock MJ, Ben-Ze'ev A. 1997. Regulation of beta-catenin levels and localization by overexpression of plakoglobin and inhibition of the ubiquitin-proteasome system. J Cell Biol 139: 1325-1335.
56. Steinberg MS. 2007. Differential adhesion in morphogenesis: a modern view. Curr Opin Genet Dev 17: 281-286.
57. Tepass U, Godt D, Winklbauer R. 2002. Cell sorting in animal development: signalling and adhesive mechanisms in the formation of tissue boundaries. Curr Opin Genet Dev 12: 572-582.
58. Tevosian SG, Manuylov NL. 2008. To beta or not to beta: canonical beta-catenin signaling pathway and ovarian development. Dev Dyn 237: 3672-3680.
59. Tomizuka K, Horikoshi K, Kitada R, Sugawara Y, Iba Y, Kojima A, Yoshitome A, Yamawaki K, Amagai M, Inoue A, Oshima T, Kakitani M. 2008. R-spondin1 plays an essential role in ovarian development through positively regulating Wnt-4 signaling. Hum Mol Genet 17: 1278-1291.
60. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP. 1999. Female development in mammals is regulated by Wnt-4 signalling. Nature 397: 405-409.
61. Wilhelm D, Englert C. 2002. The Wilms tumor suppressor WT1 regulates early gonad development by activation of Sf1. Genes Dev 16: 1839-1851.
62. Wilhelm D, Palmer S, Koopman P. 2007. Sex determination and gonadal development in mammals. Physiol Rev 87: 1-28.