Loss of Smad4 in sertoli and leydig cells leads to testicular dysgenesis and hemorrhagic tumor formation in mice

Biology of Reproduction

Volumn 90, Issue 3, 2014, Pages

  Archambeault, Denise R ^a,c   Yao, Humphrey Hung Chang ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Azoospermia; Hemorrhage; Leydig cell hyperplasia; Mouse; Smad; Teratoma; Testicular dysgenesis; Testis

Indexed keywords

SMAD4 PROTEIN;

ADENOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL POPULATION; GENE EXPRESSION; GONADAL DYSGENESIS; HORMONE DETERMINATION; KNOCKOUT MOUSE; LEYDIG CELL; MALE; MOUSE; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SEMEN ANALYSIS; SEMINIFEROUS TUBULE; SERTOLI CELL; SOMATIC CELL; SPERM; SPERMATOGENESIS; TESTIS; TESTIS DEVELOPMENT; TESTIS SIZE; TESTIS TUMOR;

AZOOSPERMIA; HEMORRHAGE; LEYDIG CELL HYPERPLASIA; MOUSE; SMAD; TERATOMA; TESTICULAR DYSGENESIS; TESTIS;

ADENOMA; AGING; ANIMALS; GONADAL DYSGENESIS; HEMORRHAGE; IMMUNOHISTOCHEMISTRY; LEYDIG CELLS; MALE; MICE; MICE, KNOCKOUT; ORGAN SIZE; SEMINIFEROUS TUBULES; SERTOLI CELLS; SMAD4 PROTEIN; TESTICULAR NEOPLASMS; TESTIS;

EID: 84899905846     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.111393     Document Type: Article

References (45)

1. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 2008; 1782:197-228.
2. Govani FS, Shovlin CL. Hereditary haemorrhagic telangiectasia: a clinical and scientific review. Eur J Hum Genet 2009; 17:860-871.
3. Wu MY, Hill SC. TGF-b superfamily signaling in embryonic development and homeostasis. Dev Cell 2009; 16:329-343.
4. Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-beta superfamily signaling. Genes Cells 2002; 7: 1191-1204.
5. Lagna G, Hata A, Hemmati-Brivanlou A, Massagué J. Partnership between DPC4 and SMAD proteins in TGF-b signaling pathways. Nature 1996; 383:832-836.
6. Zhang Y, Feng X, We RY, Derynck R. Receptor associated Mad homologues synergize as effectors of the TGF-b response. Nature 1996; 383:168-172.
7. Behringer RR, Finegold MJ, Cate RL. Mü llerian-inhibiting substance function during mammalian sexual development. Cell 1994; 79:415-425.
8. Vassalli A, Matzuk MM, Gardner HA, Lee KF, Jaenisch R. Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev 1994; 8:414-427.
9. Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R, Bradley A. Functional analysis of activins during mammalian development. Nature 1995; 374:354-356.
10. Yao HH, Aardema J, Holthusen K. Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol Reprod 2006; 74:978-983.
11. Memon MA, Anway MD, Covert TR, Uzumcu M, Skinner MK. Transforming growth factor beta (TGFb1, TGFb2, TGFb3) null-mutant phenotypes in embryonic gonadal development. Mol Cell Endocrinol 2008; 294:70-80.
12. Archambeault DR, Yao HHC. Activin A, a product of fetal Leydig cells, is a unique paracrine regulator of Sertoli cell proliferation and testis cord expansion. Proc Natl Acad Sci U S A 2010; 107:10526-10531.
13. Itman C, Loveland KL. SMAD expression in the testis: an insight into BMP regulation of spermatogenesis. Dev Dyn 2008; 237:97-111.
14. Hussein N, Lu J, Casse H, Fontaniére S, Morera AM, Guittot SM, Calender A, Di Clemente N, Zhang CX. Deregulation of anti-Mü llerian hormone/BMP and transforming growth factor-beta pathways in Leydig cell lesions developed in male heterozygous multiple endocrine neoplasia type 1 mutant mice. Endocr Relat Cancer 2008; 15:217-227.
15. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. Requirement of Bmpr1a for Mü llerian duct regression during male sexual development. Nat Genet 2002; 32:408-410.
16. Bingham NC, Verma-Kurvari S, Parada LF, Parker KL. Development of a steroidogenic factor 1/Cre transgenic mouse line. Genesis 2006; 44: 419-424.
17. Yang X, Li C, Herrera PL, Deng CX. Generation of Smad4/Dpc4 conditional knockout mice. Genesis 2002; 32:80-81.
18. Joyce KL, Porcelli J, Cooke PS. Neonatal goitrogen treatment increases adult testis size and sperm production in the mouse. J Androl 1993; 14: 448-455.
19. Itman C, Mendis S, Barakat B, Loveland KL. All in the family: TGF-beta family action in testis development. Reproduction 2006; 132:233-246.
20. Jeyasuria P, Ikeda Y, Jamin SP, Zhao L, De Rooij DG, Themmen AP, Behringer RR, Parker KL. Cell-specific knockout of steroidogenic factor 1 reveals its essential roles in gonadal function. Mol Endocrinol 2004; 18: 1610-1619.
21. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, Behringer RR. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev 1996; 10:2577-2587.
22. Mouse Genome Informatics (MGI). Bar Harbor, ME: The Jackson Laboratory. http://www.informatics.jax.org/reference/allele/MGI:3042214. Accessed January 15, 2014.
23. Mouse Genome Informatics (MGI). Bar Harbor, ME: The Jackson Laboratory. http://www.informatics.jax.org/reference/allele/MGI:3042214. Accessed January 15, 2014.
24. Liu CF, Bingham N, Parker K, Yao HH. Sex-specific roles of beta-catenin in mouse gonadal development. Hum Mol Genet 2009; 18:405-417.
25. Huang CC, Miyagawa S, Matsumaru D, Parker KL, Yao HH. Progenitor cell expansion and organ size of mouse adrenal is regulated by sonic hedgehog. Endocrinology 2010; 151:1119-1128.
26. 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.
27. Liu CF, Parker K, Yao HH. WNT4/beta-catenin pathway maintains female germ cell survival by inhibiting activin betaB in the mouse fetal ovary. PLoS One 2010; 5:e10382.
28. Archambeault DR, Tomaszewski J, Childs AJ, Anderson RA, Yao HH. Testicular somatic cells, not gonocytes, are the major source of functional activin A during testis morphogenesis. Endocrinology 2011; 152: 4358-4367.
29. Huang CC, Liu C, Yao HH. Investigating the role of adrenal cortex in organization and differentiation of the adrenal medulla in mice. Mol Cell Endocrinol 2012; 361:165-171.
30. De Gendt K, Verhoeven G. Tissue- and cell-specific functions of the androgen receptor revealed through conditional knockout models in mice. Mol Cell Endocrinol 2012; 352:13-25.
31. Lécureuil C, Fontaine I, Crepieux P, Guillou F. Sertoli and granulosa cellspecific Cre recombinase activity in transgenic mice. Genesis 2002; 33: 114-118.
32. Cool J, Capel B. Mixed signals: development of the testis. Semin Reprod Med 2009; 27:5-13.
33. Brennan J, Tilmann C, Capel B. Pdgrf-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003; 17:800-810.
34. Sato Y, Baba T, Zubair M, Miyabayashi K, Toyama Y, Maekawa M, Owaki A, Mizusaki H, Sawamura T, Toshimori K, Morohashi K, Katoh- Fukui Y. Importance of forkhead transcription factor Fkhl18 for development of testicular vasculature. Mol Reprod Dev 2008; 75: 1361-1371.
35. Chen X, Rubock MJ, Whitman M. A transcriptional partner for MAD proteins in TGF-beta signaling. Nature 1996; 383:691-696.
36. Chen X, Weisberg E, Fridmacher V, Watanabe M, Naco G, Whitman M. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 1997; 389:85-89.
37. Accili D, Arden KC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004; 117:421-426.
38. Owens P, Engelking E, Han G, Haeger SM, Wang XJ. Epidermal Smad4 deletion results in aberrant wound healing. Am J Pathol 2010; 176: 122-133.
39. Schwarte-Waldhoff I, Volpert OV, Bouck NP, Sipos B, Hahn SA, Klein- Scory S, Lü ttges J, Klöppel G, Graeven U, Eilert-Micus C, Hintelmann A, Schmiegel W. Smad4/DPC4-mediated tumor suppression through suppression of angiogenesis. Proc Natl Acad Sci U S A 2000; 97:9624-9629.
40. Golat BT, Cameron DF. Sertoli cells enhance formation of capillary-like structures in vitro. Cell Transplant 2008; 17:1135-1144.
41. Collin O, Bergh A. Leydig cells secrete factors which increase vascular permeability and endothelial cell proliferation. Int J Androl 1996; 19: 221-228.
42. Yoshida S, Sukeno M, Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007; 317: 1722-1726.
43. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM. Conditional deletion of Smad1 and Smad5 in somatic cells of the male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 2008; 28:248-257.
44. Stevens, LC Jr, Little CC. Spontaneous testicular teratomas in an inbred strain of mice. Proc Natl Acad Sci U S A 1954; 40:1080-1087.
45. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 1998; 4:415-428.