Pdgfr-α mediates testis cord organization and fetal Leydig cell development in the XY gonad

Genes and Development

Volumn 17, Issue 6, 2003, Pages 800-810

  Brennan, Jennifer ^a   Tilmann, Christopher ^b   Capel, Blanche ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Endothelial cells; Leydig cells; Platelet derived growth factor; Sex determination

Indexed keywords

LIGAND; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; FEMALE; FETUS; GONAD DEVELOPMENT; INTERSTITIUM; LEYDIG CELL; MALE; MORPHOLOGY; MOUSE; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SEX DETERMINATION; SIGNAL TRANSDUCTION; SRY GENE; TESTIS; TESTIS DEVELOPMENT; VASCULARIZATION;

ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL DIVISION; GENOTYPE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LEYDIG CELLS; LIGANDS; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MUTATION; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SEX DETERMINATION (GENETICS); TESTIS; TIME FACTORS; X CHROMOSOME; Y CHROMOSOME;

ANIMALIA;

EID: 0345700294     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1052503     Document Type: Article

References (40)

1. Ariyaratne, S., Mendis-Handagama, C., Hales, B., and Mason, I. 2000. Studies on the onset of Leydig precursor cell differentiation in the prepubertal rat testis. Biol. Reprod. 63: 165-171.
2. Betsholtz, C., Karlsson, L., and Lindahlm P. 2001. Developmental roles of platelet-derived growth factors. Bioessays. 23:494-507.
3. Bostrom, H., Willetts, K., Pekny, M., Leveen, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellstrom, M., Gebre-Medhin, S., Schalling, M., et al. 1996. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85: 863-873.
4. Brennan, J., Karl, J., and Capel, B. 2002. Divergent vascular mechanisms downstream of Sry establish the arterial system in the XY gonad. Dev. Biol. 244: 418-428.
5. Buehr, M., Gu, S., and McLaren, A. 1993. Mesonephric contribution to testis differentiation in the fetal mouse. Development 117: 273-281.
6. Capel, B., Albrecht, K.H., Washburn, L.L., and Eicher, E.M. 1999. Migration of mesonephric cells into the mammalian gonad depends on Sry. Mech. Dev. 84: 127-131.
7. Chai, Y., Jiang, X., Ito, Y., Bringas Jr., P., Han, J., Rowitch, D.H., Soriano, P., McMahon, A.P., and Sucov, H.M. 2000. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127: 1671-1679.
8. Darnell, D.K., Garcia-Martinez, V., Lopez-Sanchez, C., Yuan, S., and Schoenwolf, G.C. 2000. Dynamic labeling techniques for fate mapping, testing cell commitment, and following living cells in avian embryos. Methods Mol. Biol. 135: 305-321.
9. Ding, H., Wu, X., Kim, I., Tam, P.P., Koh, G.Y., and Nagy, A. 2000. The mouse Pdgfc gene: Dynamic expression in embryonic tissues during organogenesis. Mech. Dev. 96: 209-213.
10. Gnessi, L., Emidi, A., Jannini, E.A., Carosa, E., Maroder, M., Arizzi, M., Ulisse, S., and Spera, G. 1995. Testicular development involves the spatiotemporal control of PDGFs and PDGF receptors gene expression and action. J. Cell Biol. 131:1105-1121.
11. Gnessi, L., Basciani, S., Mariani, S., Arizzi, M., Spera, G., Wang, C., Bondjers, C., Karlsson, L., and Betsholtz, C. 2000. Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A deficient mice. J. Cell Biol. 149: 1019-1025.
12. Hacker, A., Capel, B., Goodfellow, P., and Lovell-Badge, R. 1995. Expression of Sry, the mouse sex determining gene. Development 121: 1603-1614.
13. Hadjantonakis, A.K., Gertsenstein, M., Ikawa, M., Okabe, M., and Nagy, A. 1998. Non-invasive sexing of preimplantation stage mammalian embryos. Nat. Genet. 19: 220-222.
14. Hatano, O., Takakusu, A., Nomura, M., and Morohashi, K. 1996. Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF1. Genes Cells 1: 663-671.
15. Heikkila, M., Peltoketo, H., Leppaluoto, J., Ilves, M., Vuolteenaho, O., and Vaino, S. 2002. Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology 143: 4358-4365.
16. Heldin, C.H. and Westermark, B. 1999. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79: 1283-1316.
17. Henrique, D., Adam, J., Myat, A., Chitnis, A., Lewis, J., and Ish-Horowicz, D. 1995. Expression of a Delta homologue in prospective neurons in the chick. Nature 375: 787-790.
18. Karl, J. and Capel, B. 1998. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol. 203: 323-333.
19. Karlsson, L., Lindahl, P., Heath, J.K., and Betsholtz, C. 2000. Abnormal gastrointestinal development in PDGF-A and PDGFR-α deficient mice implicates a novel mesenchymal structure with putative instructive properties in villus morphogenesis. Development 127: 3457-3466.
20. Kitamura, K., Yanazawa, M., Sugiyama, N., Miura, H., Iizuka-Kogo, A., Kusaka, M., Omichi, K., Suzuki, R., Kato-Fukui, Y., Kamiirisa, K., et al. 2002. Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat. Genet. 32: 359-369.
21. Klinghoffer, R.A., Mueting-Nelsen, P.F., Faerman, A., Shani, M., and Soriano, P. 2001. The two PDGF receptors maintain conserved signaling in vivo despite divergent embryological functions. Mol. Cell 7: 343-354.
22. Lammert, E., Cleaver, O., and Melton, D. 2001. Induction of pancreatic differentiation by signals from blood vessels. Science 294: 564-567.
23. Lindahl, P., Hellstrom, M., Kalen, M., Karlsson, L., Pekny, M., Pekna, M., Soriano, P., and Betsholtz, C. 1998. Paracrine PDGF-B/PDGF-Rβ signaling controls mesangial cell development in kidney glomeruli. Development 125: 3313-3322.
24. Martineau, J., Nordqvist, K., Tilmann, C., Lovell-Badge, R., and Capel, B. 1997. Male-specific cell migration into the developing gonad. Curr. Biol. 7: 958-968.
25. Matsumoto, K., Yoshitomi, H., Rossant, J., and Zaret, K.S. 2001. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294: 559-563.
26. Mayerhofer, A., Lahr, G., Seidl, K., Eusterschulte, B., Christoph, A., and Gratzl, M. 1996. The neural cell adhesion molecule (NCAM) provides clues to the development of testicular Leydig cells. J. Andrology 17: 223-230.
27. Merchant-Larios, H. and Moreno-Mendoza, N. 1998. Mesonephric stromal cells differentiate into Leydig cells in the mouse fetal testis. Exp. Cell Res. 244: 230-238.
28. Merchant-Larios, H., Moreno-Mendoza, N., and Buehr, M. 1993. The role of the mesonephros in cell differentiation and morphogenesis of the mouse fetal testis. Intl. J. Dev. Biol. 37:407-415.
29. Middendorff, R., Davidoff, M., and Holstein, A.F. 1993. Neuroendocrine marker substances in human Leydig cells -Changes by disturbances of testicular function. Andrologia 25: 257-262.
30. Morohashi, K. 1997. The ontogenesis of the steroidogenic tissues. Genes to Cells 2: 95-106.
31. Nishino, K., Yamanouchi, K., Naito, K., and Tojo, H. 2001. Characterization of mesonephric cells that migrate into the XY gonad during testis differentiation. Exp. Cell Res. 267:225-232.
32. Palmer, S.J. and Burgoyne, P.S. 1991. In situ analysis of fetal, prepubertal and adult XX-XY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112:265-268.
33. Schmahl, J., Eicher, E.M., Washburn, L.L., and Capel, B. 2000. Sry induces cell proliferation in the mouse gonad. Development 127: 65-73.
34. Soriano, P. 1994. Abnormal kidney development and hematological disorders in PDGF β-receptor mutant mice. Genes & Dev. 8: 1888-1896.
35. -. 1997. The PDGF α receptor is required for neural crest cell development and for normal patterning of the somites. Development 124:2691-2700.
36. Tilmann, K. and Capel, B. 1999. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126: 2883-2890.
37. Uzumcu, M., Dirks, K.A., and Skinner, M.K. 2002. Inhibition of platelet-derived growth factor actions in the embryonic testis influences normal cord development and morphology. Biol. Reprod. 66: 745-753.
38. Vanio, S., Heikkila, M., Kispert, A., Chin, N., and McMahon, A. 1999. Female development in mammals is regulated by Wnt-4 signaling. Nature 397: 405-409.
39. Yamauchi, Y., Abe, K., Mantani, A., Hitoshi, Y., Suzuki, M., Osuzu, F., Kuratani, S., and Yamamura, K. 1999. A novel transgenic technique that allows specific marking of the neural crest cell lineage in mice. Dev. Biol. 212: 191-203.
40. Yao, H.H., Whoriskey, W., and Capel, B. 2002. Desert hedgehog/patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes & Dev. 16: 1433-1440.