BMP4 promotes human sertoli cell proliferation via Smad1/5 and ID2/3 pathway and its abnormality is associated with azoospermia

Discovery Medicine

Volumn 19, Issue 105, 2015, Pages 311-325

  Hai, Yanan ^a   Sun, Min ^a   Niu, Minghui ^a   Yuan, Qingqing ^a   Guo, Ying ^a   Li, Zheng ^a   He, Zuping ^a,b,c  

^a School of Medicine   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c Shanghai Key Laboratory of Assisted Reproduction and Reproductive Genetics ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; SMAD1 PROTEIN; SMAD5 PROTEIN; BMP4 PROTEIN, HUMAN; CHOLECYSTOKININ OCTAPEPTIDE; ID2 PROTEIN, HUMAN; ID3 PROTEIN, HUMAN; INHIBITOR OF DIFFERENTIATION 2; INHIBITOR OF DIFFERENTIATION PROTEIN; SMAD1 PROTEIN, HUMAN; SMAD5 PROTEIN, HUMAN; SMALL INTERFERING RNA; TUMOR PROTEIN;

ARTICLE; AZOOSPERMIA; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CELL TRANSFER; CONTROLLED STUDY; GENE THERAPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA INTERFERENCE; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS BIOPSY; WESTERN BLOTTING; ADULT; BIOPSY; CYTOLOGY; GENE EXPRESSION REGULATION; MALE; METABOLISM; SPERMATOZOON; TESTIS;

ADULT; AZOOSPERMIA; BIOPSY; BONE MORPHOGENETIC PROTEIN 4; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INHIBITOR OF DIFFERENTIATION PROTEINS; MALE; NEOPLASM PROTEINS; RNA, SMALL INTERFERING; SERTOLI CELLS; SINCALIDE; SMAD1 PROTEIN; SMAD5 PROTEIN; SPERMATOZOA; TESTIS;

EID: 84940477946     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (43)

1. Baleato RM, Aitken RJ, Roman SD. Vitamin A regulation of BMP4 expression in the male germ line. Dev Biol 286(1):78-90, 2005.
2. Belville C, Jamin SP, Picard JY, Josso N, Di Clemente N. Role of type I receptors for anti-Mullerian hormone in the SMAT-1 Sertoli cell line. Oncogene 24(31):4984-4992, 2005.
3. Blaudeau TE, Hunter GR, Sirikul B. Intra-abdominal adipose tissue deposition and parity. Int J Obes (Lond) 30(7):1119-1124, 2006.
4. Carlomagno G, Van Bragt MP, Korver CM, Repping S, De Rooij DG, Van Pelt AM. BMP4-induced differentiation of a rat spermatogonial stem cell line causes changes in its cell adhesion properties. Biol Reprod 83(5):742-749, 2010.
5. Cheng CY, Mruk DD. The blood-testis barrier and its implications for male contraception. Pharmacol Rev 64(1):16-64, 2012.
6. Chiu CY, Kuo KK, Kuo TL, Lee KT, Cheng KH. The activation of MEK/ERK signaling pathway by bone morphogenetic protein 4 to increase hepatocellular carcinoma cell proliferation and migration. Mol Cancer Res 10(3):415-427, 2012.
7. Chui K, Trivedi A, Cheng CY, Cherbavaz DB, Dazin PF, Huynh AL, Mitchell JB, Rabinovich GA, Noble-Haeusslein LJ, John CM. Characterization and functionality of proliferative human Sertoli cells. Cell Transplant 20(5):619-635, 2011.
8. De Rooij DG. The spermatogonial stem cell niche. Microsc Res Techniq 72(8):580-585, 2009.
9. De Winter JP, Vanderstichele HM, Timmerman MA, Blok LJ, Themmen AP, De Jong FH. Activin is produced by rat Sertoli cells in vitro and can act as an autocrine regulator of Sertoli cell function. Endocrinology 132(3):975-982, 1993.
10. Ding X, Zhang X, Mu Y, Li Y, Hao J. Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via up-regulation of Sohlh2 and c-kit. Mol Reprod Dev 80(1):70-78, 2013.
11. Fink C, Weigel R, Hembes T, Lauke-Wettwer H, Kliesch S, Bergmann M, Brehm RH. Altered expression of ZO-1 and ZO-2 in Sertoli cells and loss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 8(12):1019-1027, 2006.
12. Frank NY, Kho AT, Schatton T, Murphy GF, Molloy MJ, Zhan Q, Ramoni MF, Frank MH, Kohane IS, Gussoni E. Regulation of myogenic progenitor proliferation in human fetal skeletal muscle by BMP4 and its antagonist Gremlin. J Cell Biol 175(1):99-110, 2006.
13. Hai Y, Hou J, Liu Y, Yang H, Li Z, He Z. The roles and regulation of Sertoli cells in fate determinations of spermatogonial stem cells and spermatogenesis. Semin Cell Dev Biol 29C:66-75, 2014.
14. Hasegawa K, Saga Y. Retinoic acid signaling in Sertoli cells regulates organization of the blood-testis barrier through cyclical changes in gene expression. Development 139(23):4347-4355, 2012.
15. He Z, Jiang J, Hofmann MC, Dym M. Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biol Reprod 77(4):723-733, 2007.
16. He Z, Jiang J, Kokkinaki M, Golestaneh N, Hofmann MC, Dym M. Gdnf upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 26(1):266-278, 2008.
17. He Z, Kokkinaki M, Jiang J, Dobrinski I, Dym M. Isolation, characterization, and culture of human spermatogonia. Biol Reprod 82(2):363-372, 2010.
18. Hu J, Shima H, Nakagawa H. Glial cell line-derived neurotropic factor stimulates sertoli cell proliferation in the early postnatal period of rat testis development. Endocrinology 140(8):3416-3421, 1999.
19. Hua H, Zhang YQ, Dabernat S, Kritzik M, Dietz D, Sterling L, Sarvetnick N. BMP4 regulates pancreatic progenitor cell expansion through Id2. J Biol Chem 281(19):13574-13580, 2006.
20. Jeffery TK, Upton PD, Trembath RC, Morrell NW. BMP4 inhibits proliferation and promotes myocyte differentiation of lung fibroblasts via Smad1 and JNK pathways. Am J Physiol Lung Cell Mol Physiol 288(2):L370-L378, 2005.
21. Kiyono M, Shibuya M. Bone morphogenetic protein 4 mediates apoptosis of capillary endothelial cells during rat pupillary membrane regression. Mol Cell Biol 23(13):4627-4636, 2003.
22. Lie PP, Cheng CY, Mruk DD. Signalling pathways regulating the blood-testis barrier. Int J Biochem Cell Biol 45(3):621-625, 2013.
23. Lui WY, Lee WM. Molecular mechanisms by which hormones and cytokines regulate cell junction dynamics in the testis. J Mol Endocrinol 43(2):43-51, 2009.
24. Lui WY, Mruk D, Lee WM, Cheng CY. Sertoli cell tight junction dynamics: their regulation during spermatogenesis. Biol Reprod 68(4):1087-1097, 2003.
25. Ma M, Yang S, Zhang Z, Li P, Gong Y, Liu L, Zhu Y, Tian R, Liu Y, Wang X, Liu F, He L, Yang H, Li Z, He Z. Sertoli cells from non-obstructive azoospermia and obstructive azoospermia patients show distinct morphology, Raman spectrum and biochemical phenotype. Hum Reprod 28(7):1863-1873, 2013.
26. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25(5):747-806, 2004.
27. Nicholls PK, Harrison CA, Gilchrist RB, Farnworth PG, Stanton PG. Growth differentiation factor 9 is a germ cell regulator of Sertoli cell function. Endocrinology 150(5):2481-2490, 2009.
28. Nicholls PK, Harrison CA, Rainczuk KE, Wayne Vogl A, Stanton PG. Retinoic acid promotes Sertoli cell differentiation and antagonises activin-induced proliferation. Mol Cell Endocrinol 377(1-2):33-43, 2013.
29. Nishimura YV, Shikanai M, Hoshino M, Ohshima T, Nabeshima Y, Mizutani K, Nagata K, Nakajima K, Kawauchi T. Cdk5 and its substrates, Dcx and p27kip1, regulate cytoplasmic dilation formation and nuclear elongation in migrating neurons. Development 141(18):3540-3550, 2014.
30. Pallares J, Bussaglia E, Martinez-Guitarte JL, Dolcet X, Llobet D, Rue M, Sanchez-Verde L, Palacios J, Prat J, Matias-Guiu X. Immunohistochemical analysis of PTEN in endometrial carcinoma: a tissue microarray study with a comparison of four commercial antibodies in correlation with molecular abnormalities. Mod Pathol 18(5):719-727, 2005.
31. Pellegrini M, Grimaldi P, Rossi P, Geremia R, Dolci S. Developmental expression of BMP4/ALK3/SMAD5 signaling pathway in the mouse testis: a potential role of BMP4 in spermatogonia differentiation. J Cell Sci 116(Pt 16):3363-3372, 2003.
32. Perez CV, Sobarzo CM, Jacobo PV, Pellizzari EH, Cigorraga SB, Denduchis B, Lustig L. Loss of occludin expression and impairment of blood-testis barrier permeability in rats with autoimmune orchitis: effect of interleukin 6 on Sertoli cell tight junctions. Biol Reprod 87(5):122, 2012.
33. Qi X, Li TG, Hao J, Hu J, Wang J, Simmons H, Miura S, Mishina Y, Zhao GQ. BMP4 supports self-renewal of embryonic stem cells by inhibiting mitogen-activated protein kinase pathways. Proc Natl Acad Sci U S A 101(16):6027-6032, 2004.
34. Rebourcet D, O'shaughnessy PJ, Pitetti JL, Monteiro A, O'hara L, Milne L, Tsai YT, Cruickshanks L, Riethmacher D, Guillou F, Mitchell RT, Van't Hof R, Freeman TC, Nef S, Smith LB. Sertoli cells control peritubular myoid cell fate and support adult Leydig cell development in the prepubertal testis. Development 141(10):2139-2149, 2014.
35. Rossi P, Dolci S. Paracrine mechanisms involved in the control of early stages of Mammalian spermatogenesis. Front Endocrinol (Lausanne) 4:181, 2013.
36. Sharpe RM, Mckinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125(6):769-784, 2003.
37. Shimasaki S, Moore RK, Otsuka F, Erickson GF. The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25(1):72-101, 2004.
38. Wada T, Yamashita Y, Saga Y, Takahashi K, Koinuma K, Choi YL, Kaneda R, Fujiwara S, Soda M, Watanabe H, Kurashina K, Hatanaka H, Enomoto M, Takada S, Mano H, Suzuki M. Screening for genetic abnormalities involved in ovarian carcinogenesis using retroviral expression libraries. Int J Oncol 35(5):973-976, 2009.
39. Yang Y, Han C. GDNF stimulates the proliferation of cultured mouse immature Sertoli cells via its receptor subunit NCAM and ERK1/2 signaling pathway. BMC Cell Biol 11:78, 2010.
40. Ying QL, Nichols J, Chambers I, Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115(3):281-292, 2003.
41. Yoon MK, Mitrea DM, Ou L, Kriwacki RW. Cell cycle regulation by the intrinsically disordered proteins p21 and p27. Biochem Soc Trans 40(5):981-988, 2012.
42. Yu PB, Deng DY, Beppu H, Hong CC, Lai C, Hoyng SA, Kawai N, Bloch KD. Bone morphogenetic protein (BMP) type II receptor is required for BMP-mediated growth arrest and differentiation in pulmonary artery smooth muscle cells. J Biol Chem 283(7):3877-3888, 2008.
43. Zhang Y, Wang S, Wang X, Liao S, Wu Y, Han C. Endogenously produced FGF2 is essential for the survival and proliferation of cultured mouse spermatogonial stem cells. Cell Res 22(4):773-776, 2012.