Testis formation in the fetal mouse: Dynamic and complex de novo tubulogenesis

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 6, 2012, Pages 847-859

  Cool, Jonah ^a   Defalco, Tony ^a   Capel, Blanche ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; FIBROBLAST GROWTH FACTOR 9; INHIBIN B; MUELLERIAN INHIBITING FACTOR; PLATELET DERIVED GROWTH FACTOR; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN;

CELL ADHESION; GERM CELL; GONAD; MALE; MOUSE; NONHUMAN; REVIEW; SEMINIFEROUS TUBULE; SERTOLI CELL; SERTOLI GERM CELL MASS; SEX DETERMINATION; TESTIS DEVELOPMENT; VASCULARIZATION;

ANIMALS; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GERM CELLS; GONADS; LEYDIG CELLS; MALE; MICE; SERTOLI CELLS; TESTIS;

EID: 84886253685     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.62     Document Type: Review

References (64)

1. Karl J, Capel B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev Biol 1998, 203:323-333.
2. Schmahl J, Eicher EM, Washburn LL, Capel B. Sry induces cell proliferation in the mouse gonad. Development 2000, 127:65-73.
3. Koopman P, Munsterberg A, Capel B, Vivian N, Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 1990, 348:450-452.
4. 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 2008, 105:7212-7217.
5. Brennan J, Karl J, Capel B. Divergent vascular mechanisms downstream of Sry establish the arterial system in the XY gonad. Dev Biol 2002, 244:418-428.
6. Di Carlo A, De Felici M. A role for E-cadherin in mouse primordial germ cell development. Dev Biol 2000, 226:209-219.
7. Wartenberg H, Kinsky I, Viebahn C, Schmolke C. Fine structural characteristics of testicular cord formation in the developing rabbit gonad. J Electron Microsc Tech 1991, 19:133-157.
8. Nel-Themaat L, Vadakkan TJ, Wang Y, Dickinson ME, Akiyama H, Behringer RR. Morphometric analysis of testis cord formation in Sox9-EGFP mice. Dev Dyn 2009, 238:1100-1110.
9. Nel-Themaat L, Jang CW, Stewart MD, Akiyama H, Viger RS, Behringer RR. Sertoli cell behaviors in developing testis cords and postnatal seminiferous tubules of the mouse. Biol Reprod 2011, 84:342-350.
10. Merchant H. Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol 1975, 44:1-21.
11. McLaren A. Relation of germ cell sex to gonadal differentiation. In: Halvorson HO, Monroy A, eds. The Origin and Evolution of Sex. New York: Liss; 1985, 289-300.
12. Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development 1998, 125:3323-3328.
13. Tung PS, Fritz IB. Interactions of Sertoli cells with myoid cells in vitro. Biol Reprod 1980, 23:207-217.
14. Skinner MK, Tung PS, Fritz IB. Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J Cell Biol 1985, 100:1941-1947.
15. Skinner MK, Fritz IB. Androgen stimulation of Sertoli cell function is enhanced by peritubular cells. Mol Cell Endocrinol 1985, 40:115-122.
16. Tung PS, Fritz IB. Extracellular matrix components and testicular peritubular cells influence the rate and pattern of sertoli cell migration in vitro. Dev Biol 1986, 113:119-134.
17. Tung PS, Skinner MK, Fritz IB. Cooperativity between Sertoli cells and peritubular myoid cells in the formation of the basal lamina in the seminiferous tubule. Ann N Y Acad Sci 1984, 438:435-446.
18. Jameson SA, Natarajan A, Cool J, Defalco T, Maatouk DM, Mork L, Munger SC, Capel B. Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet 2012, 8:e1002575.
19. Sang QX, Dym M, Byers SW. Secreted metalloproteinases in testicular cell culture. Biol Reprod 1990, 43:946-955.
20. Enders GC, Henson JH, Millette CF. Sertoli cell binding to isolated testicular basement membrane. J Cell Biol 1986, 103:1109-1119.
21. Matoba S, Hiramatsu R, Kanai-Azuma M, Tsunekawa N, Harikae K, Kawakami H, Kurohmaru M, Kanai Y. Establishment of testis-specific SOX9 activation requires high-glucose metabolism in mouse sex differentiation. Dev Biol 2008, 324:76-87.
22. Connelly JT, Gautrot JE, Trappmann B, Tan DW, Donati G, Huck WT, Watt FM. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat Cell Biol 2010, 12:711-718.
23. Nelson CM, Khauv D, Bissell MJ, Radisky DC. Change in cell shape is required for matrix metalloproteinase-induced epithelial-mesenchymal transition of mammary epithelial cells. J Cell Biochem 2008, 105:25-33.
24. Buehr M, Gu S, McLaren A. Mesonephric contribution to testis differentiation in the fetal mouse. Development 1993, 117:273-281.
25. 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 1993, 37:407-415.
26. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B. Male-specific cell migration into the developing gonad. Curr Biol 1997, 7:958-968.
27. Tilmann C, Capel B. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 1999, 126:2883-2890.
28. Brennan J, Tilmann C, Capel B. Pdgfr-α mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003, 17:800-810.
29. Colvin JS, Green RP, Schmahl J, Capel B, Ornitz DM. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 2001, 104:875-889.
30. Ross AJ, Tilman C, Yao H, MacLaughlin D, Capel B. AMH induces mesonephric cell migration in XX gonads. Mol Cell Endocrinol 2003, 211:1-7.
31. Yao HH, Aardema J, Holthusen K. Sexually dimorphic regulation of inhibin β B in establishing gonadal vasculature in mice. Biol Reprod 2006, 74:978-983.
32. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, Capel B, Swain A. Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 2003, 130:3663-3670.
33. Coveney D, Ross AJ, Slone JD, Capel B. A microarray analysis of the XX Wnt4 mutant gonad targeted at the identification of genes involved in testis vascular differentiation. Gene Expr Patterns 2007, 7:82-92.
34. Jeanes A, Wilhelm D, Wilson MJ, Bowles J, McClive PJ, Sinclair AH, Koopman P. Evaluation of candidate markers for the peritubular myoid cell lineage in the developing mouse testis. Reproduction 2005, 130:509-516.
35. Cool J, Carmona FD, Szucsik JC, Capel B. Peritubular myoid cells are not the migrating population required for testis cord formation in the XY gonad. Sex Dev 2008, 2:128-133.
36. Combes AN, Wilhelm D, Davidson T, Dejana E, Harley V, Sinclair A, Koopman P. Endothelial cell migration directs testis cord formation. Dev Biol 2009, 326:112-120.
37. DeFalco T, Takahashi S, Capel B. Two distinct origins for Leydig cell progenitors in the fetal testis. Dev Biol 2011, 352:14-26.
38. Poche RA, Larina IV, Scott ML, Saik JE, West JL, Dickinson ME. The Flk1-myr::mCherry mouse as a useful reporter to characterize multiple aspects of ocular blood vessel development and disease. Dev Dyn 2009, 238:2318-2326.
39. Kim Y, Bingham N, Sekido R, Parker KL, Lovell-Badge R, Capel B. Fibroblast growth factor receptor 2 regulates proliferation and Sertoli differentiation during male sex determination. Proc Natl Acad Sci U S A 2007, 104:16558-16563.
40. Cool J, DeFalco TJ, Capel B. Vascular-mesenchymal cross-talk through Vegf and Pdgf drives organ patterning. Proc Natl Acad Sci U S A 2011, 108:167-172.
41. Bott RC, McFee RM, Clopton DT, Toombs C, Cupp AS. Vascular endothelial growth factor and kinase domain region receptor are involved in both seminiferous cord formation and vascular development during testis morphogenesis in the rat. Biol Reprod 2006, 75:56-67.
42. Gnessi L, Basciani S, Mariani S, Arizzi M, Spera G, Wang C, Bondjers C, Karlsson L, Betsholtz C. Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 2000, 149:1019-1026.
43. Taketo T, Thau RB, Adeyemo O, Koide SS. Influence of adenosine 3′:5′-cyclic monophosphate analogues on testicular organization of fetal mouse gonads in vitro. Biol Reprod 1984, 30:189-198.
44. Tung PS, Fritz IB. Morphogenetic restructuring and formation of basement membranes by Sertoli cells and testis peritubular cells in co-culture: inhibition of the morphogenetic cascade by cyclic AMP derivatives and by blocking direct cell contact. Dev Biol 1987, 120:139-153.
45. Combes AN, Lesieur E, Harley VR, Sinclair AH, Little MH, Wilhelm D, Koopman P. Three-dimensional visualization of testis cord morphogenesis, a novel tubulogenic mechanism in development. Dev Dyn 2009, 238:1033-1041.
46. Bullejos M, Koopman P. Spatially dynamic expression of Sry in mouse genital ridges. Dev Dyn 2001, 221:201-205.
47. Moreno-Mendoza N, Harley V, Merchant-Larios H. Cell aggregation precedes the onset of Sox9-expressing preSertoli cells in the genital ridge of mouse. Cytogenet Genome Res 2003, 101:219-223.
48. Hiramatsu R, Harikae K, Tsunekawa N, Kurohmaru M, Matsuo I, Kanai Y. FGF signaling directs a center-to-pole expansion of tubulogenesis in mouse testis differentiation. Development 2010, 137:303-312.
49. Western PS, Ralli RA, Wakeling SI, Lo C, van den Bergen JA, Miles DC, Sinclair AH. Mitotic arrest in teratoma susceptible fetal male germ cells. PLoS One 2011, 6:e20736.
50. Yoshida S, Sukeno M, Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007, 317:1722-1726.
51. Nagano R, Tabata S, Nakanishi Y, Ohsako S, Kurohmaru M, Hayashi Y. Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat Rec 2000, 258:210-220.
52. 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.
53. Fahrioglu U, Murphy MW, Zarkower D, Bardwell VJ. mRNA expression analysis and the molecular basis of neonatal testis defects in Dmrt1 mutant mice. Sex Dev 2007, 1:42-58.
54. Kim S, Bardwell VJ, Zarkower D. Cell type-autonomous and non-autonomous requirements for Dmrt1 in postnatal testis differentiation. Dev Biol 2007, 307:314-327.
55. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011, 476:101-104.
56. Pierucci-Alves F, Clark AM, Russell LD. A developmental study of the Desert hedgehog-null mouse testis. Biol Reprod 2001, 65:1392-1402.
57. Tang H, Brennan J, Karl J, Hamada Y, Raetzman L, Capel B. Notch signaling maintains Leydig progenitor cells in the mouse testis. Development 2008, 135:3745-3753.
58. Yao HH, Whoriskey W, Capel B. Desert Hedgehog/patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 2002, 16:1433-1440.
59. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, Wegner M, Scherer G. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 2009, 327:301-312.
60. Chang H, Gao F, Guillou F, Taketo MM, Huff V, Behringer RR. Wt1 negatively regulates β-catenin signaling during testis development. Development 2008, 135:1875-1885.
61. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, Behringer RR, Lecureuil C, Guillou F, Huff V. The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc Natl Acad Sci U S A 2006, 103:11987-11992.
62. Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, van de Kant HJ, Wegner M, de Rooij DG, Behringer RR, Schedl A. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 2004, 131:1891-1901.
63. O'Bryan MK, Takada S, Kennedy CL, Scott G, Harada S, Ray MK, Dai Q, Wilhelm D, de Kretser DM, Eddy EM, et al. Sox8 is a critical regulator of adult Sertoli cell function and male fertility. Dev Biol 2008, 316:359-370.
64. Archambeault DR, Yao HH. Activin A, a product of fetal Leydig cells, is a unique paracrine regulator of Sertoli cell proliferation and fetal testis cord expansion. Proc Natl Acad Sci U S A 2010, 107:10526-10531.