Peritubular myoid cells participate in male mouse spermatogonial stem cell maintenance

Endocrinology

Volumn 155, Issue 12, 2014, Pages 4964-4974

  Chen, Liang Yu ^a   Brown, Paula R ^a   Willis, William B ^a   Eddy, Edward M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; TESTOSTERONE;

ADULT STEM CELL; ANIMAL; C57BL MOUSE; COCULTURE; CYTOLOGY; MALE; METABOLISM; PHYSIOLOGY; SPERMATOGONIUM; TESTIS; TRANSPLANTATION;

ADULT STEM CELLS; ANIMALS; COCULTURE TECHNIQUES; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MALE; MICE, INBRED C57BL; SPERMATOGONIA; TESTIS; TESTOSTERONE;

EID: 84914132766     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1406     Document Type: Article

References (69)

1. Oatley JM, Brinster RL. The germline stem cell niche unit in mammalian testes. Physiol Rev. 2012;92(2):577-595.
2. Ross MH. The fine structure and development of the peritubular contractile cell component in the seminiferous tubules of the mouse. Am J Anat. 1967;121(3):523-557.
3. Ogawa T, Ohmura M, Ohbo K. The niche for spermatogonial stem cells in the mammalian testis. Int J Hematol. 2005;82(5):381-388.
4. de Rooij DG, van Beek ME. Computer simulation of the rodent spermatogonial stem cell niche. Biol Reprod. 2013;88(5):131.
5. Yang QE, Kim D, Kaucher A, Oatley MJ, Oatley JM. CXCL12-CXCR4 signaling is required for the maintenance of mouse spermatogonial stem cells. J Cell Sci. 2012;126(Pt 4):1009-1020.
6. Ishii K, Kanatsu-Shinohara M, Toyokuni S, Shinohara T. FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activation. Development. 2012;139(10):1734-1743.
7. Caires KC, de Avila JM, Cupp AS, McLean DJ. VEGFA family isoforms regulate spermatogonial stem cell homeostasis in vivo. Endocrinology. 2012;153(2):887-900.
8. Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development. 2009;136(7): 1191-1199.
9. Jijiwa M, Kawai K, Fukihara J, et al. GDNF-mediated signaling via RET tyrosine 1062 is essential for maintenance of spermatogonial stem cells. Genes Cells. 2008;13(4):365-374.
10. Meng X, Lindahl M, Hyvönen ME, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science. 2000;287(5457):1489-1493.
11. Creemers LB, Meng X, den Ouden K, et al. Transplantation of germ cells from glial cell line-derived neurotrophic factor-overexpressing mice to host testes depleted of endogenous spermatogenesis by fractionated irradiation. Biol Reprod. 2002;66(6):1579-1584.
12. Nagano MC. Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice. Biol Reprod. 2003;69(2):701-707.
13. Kanatsu-Shinohara M, Ogonuki N, Inoue K, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69(2):612-616.
14. Buageaw A, Sukhwani M, Ben-Yehudah A, et al. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod. 2005;73(5):1011-1016.
15. 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. 2008;26(1):266-278.
16. Hofmann MC. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol Cell Endocrinol. 2008;288(1-2):95-103.
17. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod. 2006;74(2):314-321.
18. Fouchécourt S, Godet M, Sabido O, Durand P. Glial cell-line-derived neurotropic factor and its receptors are expressed by germinal and somatic cells of the rat testis. J Endocrinol. 2006;190(1):59-71.
19. Katoh-Semba R, Tsuzuki M, Miyazaki N, et al. Distribution and immunohistochemical localization of GDNF protein in selected neural and non-neural tissues of rats during development and changes in unilateral 6-hydroxydopamine lesions. Neurosci Res. 2007;59(3):277-287.
20. Johnston DS, Olivas E, DiCandeloro P, Wright WW. Stage-specific changes in GDNF expression by rat Sertoli cells: a possible regulator of the replication and differentiation of stem spermatogonia. Biol Reprod. 2011;85(4):763-769.
21. Sato T, Aiyama Y, Ishii-Inagaki M, et al. Cyclical and patch-like GDNF distribution along the basal surface of Sertoli cells in mouse and hamster testes. PLoS One. 2011;6(12):e28367.
22. Crépieux P, Marion S, Martinat N, et al. The ERK-dependent signalling is stage-specifically modulated by FSH, during primary Sertoli cell maturation. Oncogene. 2001;20(34):4696-4709.
23. Makela JA, Toppari J, Rivero-Muller A, Ventela S. Reconstruction of mouse testicular cellular microenvironments in long-term seminiferous tubule culture. PLoS One. 2014;9(3):e90088.
24. Caires K, Broady J, McLean D. Maintaining the male germline: regulation of spermatogonial stem cells. J Endocrinol. 2010;205(2):133-145.
25. Savitt J, Singh D, Zhang C, et al. The in vivo response of stem and other undifferentiated spermatogonia to the reversible inhibition of glial cell line-derived neurotrophic factor signaling in the adult. Stem Cells. 2012;30(4):732-740.
26. Kanatsu-Shinohara M, Inoue K, Takashima S, et al. Reconstitution of mouse spermatogonial stem cell niches in culture. Cell Stem Cell. 2012;11(4):567-578.
27. Huckins C. The spermatogonial stem cell population in adult rats. 3. Evidence for a long-cycling population. Cell Tissue Kinet. 1971;4(4):335-349.
28. Caires KC, de Avila J, McLean DJ. Endocrine regulation of spermatogonial stem cells in the seminiferous epithelium of adult mice. Biores Open Access. 2012;1(5):222-230.
29. Bremner WJ, Millar MR, Sharpe RM, Saunders PT. Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens. Endocrinology. 1994;135(3):1227-1234.
30. Bhattacharya I, Pradhan BS, Sarda K, Gautam M, Basu S, Majumdar SS. A switch in Sertoli cell responsiveness to FSH may be responsible for robust onset of germ cell differentiation during prepubartal testicular maturation in rats. Am J Physiol Endocrinol Metab. 2012;303(7):E886-E898.
31. de Rooij DG, Okabe M, Nishimune Y. Arrest of spermatogonial differentiation in jsd/jsd, Sl17H/Sl17H, and cryptorchid mice. Biol Reprod. 1999;61(3):842-847.
32. Zhou W, Wang G, Small CL, et al. Gene expression alterations by conditional knockout of androgen receptor in adult sertoli cells of Utp14b(jsd/jsd) (jsd) mice. Biol Reprod. 2010;83(5):759-766.
33. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G. Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature. 1977;269(5626):338-340.
34. Scott IS, Charlton HM, Cox BS, Grocock CA, Sheffield JW, O'Shaughnessy PJ. Effect of LH injections on testicular steroidogenesis, cholesterol side-chain cleavage P450 mRNA content and Leydig cell morphology in hypogonadal mice. Journal of Endocrinology. 1990;125(1):131-138.
35. O'Shaughnessy PJ, Verhoeven G, De Gendt K, Monteiro A, Abel MH. Direct action through the sertoli cells is essential for androgen stimulation of spermatogenesis. Endocrinology. 2010;151(5): 2343-2348.
36. Sharpe RM. Sertoli cell endocrinology and signal transduction: androgen regulation. In: Skinner MK, Griswold MD, eds. Sertoli Cell Biology. San Diego, CA: Academic Press; 2005:199-216.
37. Tripiciano A, Filippini A, Giustiniani Q, Palombi F. Direct visualization of rat peritubular myoid cell contraction in response to endothelin. Biol Reprod. 1996;55(1):25-31.
38. Losinno AD, Morales A, Fernandez D, Lopez LA. Peritubular myoid cells from rat seminiferous tubules contain actin and myosin filaments distributed in two independent layers. Biol Reprod. 2012;86(5):150, 151-158.
39. 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(6):1941-1947.
40. Spinnler K, Köhn FM, Schwarzer U, Mayerhofer A. Glial cell linederived neurotrophic factor is constitutively produced by human testicular peritubular cells and may contribute to the spermatogonial stem cell niche in man. Hum Reprod. 2010;25(9):2181-2187.
41. Welsh M, Saunders PT, Atanassova N, Sharpe RM, Smith LB. Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J. 2009;23(12):4218-4230.
42. Oatley JM, Brinster RL. Spermatogonial stem cells. Methods Enzymol. 2006;419:259-282.
43. Palombi F FD, De Cesaris P, Stefanini M. Characterization of peritubular myoid cells in highly enriched in vitro cultures. In: Cooke BA, Sharpe RM, eds. Molecular and Cellular Endocrinology of the Testis. Serono Symposia. 50th ed. New York, NY: Raven Press; 1988:11-317.
44. Kanatsu-Shinohara M, Takashima S, Shinohara T. Transmission distortion by loss of p21 or p27 cyclin-dependent kinase inhibitors following competitive spermatogonial transplantation. Proc Natl Acad Sci U S A. 2010;107(14):6210-6215.
45. Dobrinski I, Ogawa T, Avarbock MR, Brinster RL. Computer assisted image analysis to assess colonization of recipient seminiferous tubules by spermatogonial stem cells from transgenic donor mice. Mol Reprod Dev. 1999;53(2):142-148.
46. Campagnolo L, Russo MA, Puglianiello A, Favale A, Siracusa G. Mesenchymal cell precursors of peritubular smooth muscle cells of the mouse testis can be identified by the presence of the p75 neurotrophin receptor. Biol Reprod. 2001;64(2):464-472.
47. Ohbo K, Yoshida S, Ohmura M, et al. Identification and characterization of stem cells in prepubertal spermatogenesis in mice. Dev Biol. 2003;258(1):209-225.
48. Haider SG, Servos G. Ultracytochemistry of 3beta-hydroxysteroid dehydrogenase in Leydig cell precursors and vascular endothelial cells of the postnatal rat testis. Anat Embryol (Berl). 1998;198(2): 101-110.
49. Laurich VM, Trbovich AM, O'Neill FH, et al. Müllerian inhibiting substance blocks the protein kinase A-induced expression of cytochrome p450 17alpha-hydroxylase/C(17-20) lyase mRNA in a mouse Leydig cell line independent of cAMP responsive element binding protein phosphorylation. Endocrinology. 2002;143(9): 3351-3360.
50. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. Amalespecific role for SOX9 in vertebrate sex determination. Development. 1996;122(9):2813-2822.
51. Maekawa M, Kamimura K, Nagano T. Peritubular myoid cells in the testis: their structure and function. Arch Histol Cytol. 1996;59(1):1-13.
52. 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. 2007;77(4):723-733.
53. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci U S A. 2000;97(15):8346-8351.
54. Kubota H, Avarbock MR, Brinster RL. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod. 2004;71(3):722-731.
55. Johnston DS, Russell LD, Friel PJ, Griswold MD. Murine germ cells do not require functional androgen receptors to complete spermatogenesis following spermatogonial stem cell transplantation. Endocrinology. 2001;142(6):2405-2408.
56. Turner TT, Jones CE, Howards SS, Ewing LL, Zegeye B, Gunsalus GL. On the androgen microenvironment of maturing spermatozoa. Endocrinology. 1984;115(5):1925-1932.
57. Tegelenbosch RA, de Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 1993;290(2):193-200.
58. Zhang C, Yeh S, Chen YT, et al. Oligozoospermia with normal fertility in male mice lacking the androgen receptor in testis peritubular myoid cells. Proc Natl Acad Sci U S A. 2006;103(47):17718-17723.
59. Frutkin AD, Shi H, Otsuka G, Levéen P, Karlsson S, Dichek DA. A critical developmental role for tgfbr2 in myogenic cell lineages is revealed in mice expressing SM22-Cre, not SMMHC-Cre. J Mol Cell Cardiol. 2006;41(4):724-731.
60. O'Shaughnessy PJ, Monteiro A, Abel M. Testicular development in mice lacking receptors for follicle stimulating hormone and androgen. PLoS One. 2012;7(4):e35136.
61. Tadokoro Y, Yomogida K, Ohta H, Tohda A, Nishimune Y. Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech Dev. 2002;113(1):29-39.
62. Ding LJ, Yan GJ, Ge QY, et al. FSH acts on the proliferation of type A spermatogonia via Nur77 that increases GDNF expression in the Sertoli cells. FEBS Lett. 2011;585(15):2437-2444.
63. Ebata KT, Zhang X, Nagano MC. Expression patterns of cell-surface molecules on male germ line stem cells during postnatal mouse development. Mol Reprod Dev. 2005;72(2):171-181.
64. Schmidt JA, de Avila JM, McLean DJ. Effect of vascular endothelial growth factor and testis tissue culture on spermatogenesis in bovine ectopic testis tissue xenografts. Biol Reprod. 2006;75(2):167-175.
65. Kanatsu-Shinohara M, Inoue K, Ogonuki N, et al. Leukemia inhibitory factor enhances formation of germ cell colonies in neonatal mouse testis culture. Biol Reprod. 2007;76(1):55-62.
66. Skinner MK, Takacs K, Coffey RJ. Transforming growth factoralpha gene expression and action in the seminiferous tubule: peritubular cell-Sertoli cell interactions. Endocrinology. 1989;124(2):845-854.
67. Skinner MK, Moses HL. Transforming growth factor beta gene expression and action in the seminiferous tubule: peritubular cell-Sertoli cell interactions. Mol Endocrinol. 1989;3(4):625-634.
68. Welsh M, Moffat L, Jack L, et al. Deletion of androgen receptor in the smooth muscle of the seminal vesicles impairs secretory function and alters its responsiveness to exogenous testosterone and estradiol. Endocrinology. 2010;151(7):3374-3385.
69. Oatley JM, Avarbock MR, Brinster RL. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. J Biol Chem. 2007;282(35):25842-25851.