Spermatogonial stem cells alone are not sufficient to re-initiate spermatogenesis in the rat testis following adjudin-induced infertility

International Journal of Andrology

Volumn 35, Issue 1, 2012, Pages 86-101

  Mok, K W ^a   Mruk, D D ^a   Lee, W M ^b   Cheng, C Y ^a  

^a POPULATION COUNCIL   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Adjudin; Blood testis barrier; Seminiferous epithelial cycle; Spermatogonia; Spermatogonial stem cells; Testis

Indexed keywords

ADJUDIN; MALE CONTRACEPTIVE AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD TESTIS BARRIER; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; EPIDIDYMIS; FEMALE; IMMUNOFLUORESCENCE; MALE; MALE FERTILITY; MALE INFERTILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOGONIUM;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; HYDRAZINES; INDAZOLES; MALE; RATS; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS;

EID: 84855669276     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2011.01183.x     Document Type: Article

References (54)

1. Allrad EK & Boekelheide K. (1996) Fate of germ cells in 2, 5-hexanedione-induced testicular injury. II. Atrophy persists due to a reduced stem cell mass and ongoing apoptosis. Toxicol Appl Pharmacol 137, 149-156.
2. Bascian S, De Luca G, Dolci S, Brama M, Arizzi M, Mariani S, Rosano G, Spera G & Gnessi L. (2008) Platelet-derived growth factor receptor beta-subtype regulates proliferation and migration of gonocytes. Endocrinology 149, 6226-6235.
3. Boekelheide K & Hall SJ. (1991) 2, 5-Hexanedione exposure in the rat results in long-term testicular atrophy despite the presence of residual spermatogonia. J Androl 12, 18-26.
4. van den Boom V, Kooistra SM, Boesjes M, Geverts B, Houtsmuller AB, Monzen K, Komuro I, Essers J, Drenth-Diephuis LJ & Eggen BJ. (2007) UTF1 is a chromatin-associated protein involved in ES cell differentiation. J Cell Biol 178, 913-924.
5. van Bragt MP, Roepers-Gajadien HL, Korver CM, Bogerd J, Okuda A, Eggen BJ, de Rooij DG & van Pelt AM. (2008) Expression of the pluripotency marker UTF1 is restricted to a subpopulation of early A spermatogonia in rat testis. Reproduction 136, 33-40.
6. Brawley C & Matunis E. (2004) Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304, 1331-1334.
7. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG & Braun RE. (2004) Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36, 647-652.
8. Cheng CY & Mruk DD. (2010) A local autocrine axis in the testes that regulates spermatogenesis. Nature Rev Endocrinol 6, 380-395.
9. Cheng CY, Silvestrini B, Grima J, Mo MY, Zhu LJ, Johansson E, Saso L, Leone MG, Palmery M & Mruk DD. (2001) Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol Reprod 65, 449-461.
10. Cheng CY, Mruk DD, Silvestrini B, Bonanomi M, Wong CH, Siu MKY, Lee NPY & Mo MY. (2005) AF-2364 [1-(2, 4-dichlorobenzyl)-1H-indazole-3-carbohydrazide] is a potential male contraceptive: a review of recent data. Contraception 72, 251-261.
11. Clermont Y & Perry B. (1957) Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 100, 241-267.
12. Dann CT, Alvarado AL, Molyneux LA, Denard BS, Garbers DL & Porteus MH. (2008) Spermatogonial stem cell self-renewal requires OCT4, a factor downregulated during retinoic acid-induced differentiation. Stem Cells 26, 2928-2937.
13. Ehmcke J, Wistuba J & Schlatt S. (2006) Spermatogonial stem cells: questions, models and perspectives. Human Reprod Update 12, 275-282.
14. Fink C, Weigel R, Hembes T, Lauke-Wettwer H, Kliesch S, Bergmann M & Brehm RH. (2006) 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, 1019-1027.
15. Fink C, Weigel R, Fink L, Wilhelm J, Kliesch S, Zeiler M, Bergmann M & Brehm R. (2009) Claudin-11 is over-expressed and dislocated from the blood-testis barrier in Sertoli cells associated with testicular intraepithelial neoplasia in men. Histochem Cell Biol 131, 755-764.
16. Forgione N, Vogl AW & Varmuza S. (2010) Loss of protein phosphatase 1c {gamma} (PPP1CC) leads to impaired spermatogenesis associated with defects in chromatin condensation and acrosome development: an ultrastructural analysis defects in chromatin condensation and acrosome development: an ultrastructural analysis. Reproduction 139, 1021-1029.
17. Gow A, Southwood C, Li J, Pariali M, Riordan G, Brodie S, Danias J, Bronstein J, Kachar B & Lazzarini R. (1999) CNS myelin and Sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99, 649-659.
18. Howell SJ & Shalet SM. (2005) Spermatogenesis after cancer treatment: damage and recovery. J Natl Cancer Inst Monogr 2005, 12-17.
19. Hubert MF, Laroque P, Gillet JP & Keenan KP. (2000) The effects of diet, ad libitum feeding, and moderate and severe dietary restriction on body weight, survival, clinical pathology parameters, and cause of death in control Sprague-Dawley rats. Toxicol Sci 58, 195-207.
20. Kangasniemi M, Huhtaniemi I & Meistrich ML. (1996) Failure of spermatogenesis to recover despite the presence of A spermatogonia in the irradiated LBNF1 rat. Biol Reprod 54, 1200-1208.
21. Koksal IT, Ishak Y, Usta M, Danisman A, Guntekin E, Bassorgun IC & Citftcioglu A. (2007) Varicocele-induced testicular dysfunction may be associated with disruption of blood-testis barrier. Arch Androl 53, 43-48.
22. Kubota H, Avarbock MR & Brinster RL. (2003) Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci U S A 100, 6487-6492.
23. Landon GV & Pryor JP. (1981) The blood-testis barrier in men of diverse fertility status: an ultrastructural study. Virchows Arch A Pathol Anat Histol 392, 355-364.
24. Li MWM, Xia W, Mruk DD, Wang CQF, Yan HHY, Siu MKY, Lui WY, Lee WM & Cheng CY. (2006) TNFa reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol 190, 313-329.
25. Lie PPY, Chan AYN, Mruk DD, Lee WM & Cheng CY. (2010a) Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 107, 11411-11416.
26. Lie PPY, Cheng CY & Mruk DD. (2010b) Crosstalk between desmoglein-2/desmocollin-2/Src kinase and coxsackie and adenovirus receptor/ZO-1 protein complexes, regulates blood-testis barrier dynamics. Int J Biochem Cell Biol 42, 975-986.
27. Mazaud-Guittot S, Meugnier E, Pesenti S, Wu X, Vidal H, Gow A & Le Magueresse-Battistoni B. (2010) Claudin 11 deficiency in mice results in loss of the Sertoli cell epithelial phenotype in the testis. Biol Reprod 82, 202-213.
28. Meinhardt A & Hedger MP. (2010) Immunological, paracrine and endocrine aspects of testicular immune privilege. Mol Cell Endocrinol 335, 60-68.
29. Meistrich ML. (1986) Critical components of testicular function and sensitivity to disruption. Biol Reprod 34, 17-28.
30. Meistrich ML, Wilson G & Huhtaniemi I. (1999) Hormonal treatment after cytotoxic therapy stimulates recovery of spermatogenesis. Cancer Res 59, 3557-3560.
31. Meistrich ML, Wilson G, Porter KL, Huhtaniemi I, Shetty G & Shuttlesworth GA. (2003) Restoration of spermatogenesis in dibromochloropropane (DBCP)-treated rats by hormone suppression. Toxicol Sci 76, 418-426.
32. Mok KW, Mruk DD, Lie PPY, Lui WY & Cheng CY. (2011) Adjudin, a potential male contraceptive, exerts its effects locally in the seminiferous epithelium of mammalian testes. Reproduction 141, 571-580.
33. Mruk DD, Wong CH, Silvestrini B & Cheng CY. (2006) A male contraceptive targeting germ cell adhesion. Nat Med 12, 1323-1328.
34. Nah WH, Lee JE, Park HJ, Park NC & Gye MC. (2010) Claudin-11 expression increased in spermatogenic defect in human testes. Fertil Steril 95, 385-388.
35. Nakagawa T, Nabeshima Y & Yoshida S. (2007) Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 12, 195-206.
36. Oatley JM & Brinster RL. (2006) Spermatogonial stem cells. Methods Enzymol 419, 259-282.
37. Pan J, Eckardt S, Leu NA, Buffone MG, Zhou J, Gerton GL, McLaughlin KJ & Wang PJ. (2009) Inactivation of Nxf2 causes defects in male meiosis and age-dependent depletion of spermatogonia. Dev Biol 330, 167-174.
38. Phillips BT, Gassei K & Orwig KE. (2010) Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365, 1663-1678.
39. de Rooij DG. (2009) The spermatogonial stem cell niche. Microsc Res Tech 72, 580-585.
40. de Rooij DG & Russell LD. (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21, 776-798.
41. Saitou M, Furuse M, Sasaki H, Schulzke J, Fromm M, Takano H, Noda T & Tsukita S. (2000) Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11, 4131-4142.
42. Setchell BP & Waites GMH. (1970) Changes in the permeability of the testicular capillaries and of the "blood-testis barrier" after injection of cadmium chloride in the rat. J Endocrinol 47, 81-86.
43. Setchell BP & Waites GMB. (1975) The blood-testis barrier. In: The Handbook of Physiology. Section 7, Vol. V. Male Reproductive System, (eds DW Hamilton & RO Greep), pp. 143-172. American Physiological Society, Washington, DC.
44. Shuttlesworth GA, De Rooij DG, Huhtaniemi I, Reissmann T, Russell LD, Shetty G, Wilson G & Meistrich ML. (2000) Enhancement of A spermatogonial proliferation and differentiation in irradiated rats by gonadotropin-releasing hormone antagonist administration. Endocrinology 141, 37-49.
45. Slutsky M, Levin JL & Levy BS. (1999) Azoospermia and oligospermia among a large cohort of DBCP applicators in 12 countries. Int J Occup Environ Health. 5, 116-122.
46. Su L, Cheng CY & Mruk DD. (2010) Adjudin-mediated Sertoli-germ cell junction disassembly affects Sertoli cell barrier function in vitro and in vivo. Int J Biochem Cell Biol 42, 1864-1875.
47. Suzuki H, Sada A, Yoshida S & Saga Y. (2009) The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev Biol 336, 222-231.
48. Takehashi M, Kanatsu-Shinohara M, Miki H, Lee J, Kazuki Y, Inoue K et al. (2007) Production of knockout mice by gene targeting in multipotent germline stem cells. Dev Biol 312, 344-352.
49. Tegelenbosch RA & de Rooij DG. (1993) A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101F1 hybrid mouse. Mutat Res 290, 193-200.
50. Toyama Y, Ohkawa M, Oku R, Maekawa M & Yuasa S. (2001) Neonatally administered diethylstilbestrol retards the development of the blood-testis barrier in the rat. J Androl 22, 413-423.
51. Wikström AM, Raivio T, Hadziselimovic F, Wikström S, Tuuri T & Dunkel L. (2004) Klinefelter syndrome in adolescence: onset of puberty is associated with accelerated germ cell depletion. J Clin Endocrinol Metab 89, 2263-2270.
52. Wong CH, Mruk DD, Lui WY & Cheng CY. (2004) Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 117, 783-798.
53. Wong EWP, Mruk DD & Cheng CY. (2008) Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim Biophys Acta 1778, 692-708.
54. Yan HHN, Mruk DD, Lee WM & Cheng CY. (2008) Blood-testis barrier dynamics are regulated by testosterone and cytokines via their differential effects on the kinetics of protein endocytosis and recycling in Sertoli cells. FASEB J 22, 1945-1959.