Concise review: Spermatogenesis in an artificial three-dimensional system

Stem Cells

Volumn 30, Issue 11, 2012, Pages 2355-2360

  Mahmoud, Huleihel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Cytokines; Pluripotent stem cells; Spermatogenesis; Spermatogonial stem cells; Stem cell microenvironment; Three dimension system

Indexed keywords

GELATIN;

CELL CULTURE; CELL MATURATION; GERM CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MICROENVIRONMENT; NONHUMAN; REVIEW; SEMINIFEROUS TUBULE; SPERM; SPERMATOGENESIS; SPERMATOGONIAL STEM CELL; STEM CELL; TESTIS CELL; THREE DIMENSIONAL CULTURE SYSTEM;

AGAR; ANIMALS; CELLS, CULTURED; CULTURE MEDIA; ENDONUCLEASES; HUMANS; MALE; SEMINIFEROUS TUBULES; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS; TISSUE CULTURE TECHNIQUES;

EID: 84867903820     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1238     Document Type: Review

References (71)

1. De Kretser DM, de Loveland KL, Meinhardt A et al. Spermatogenesis. Hum Reprod 1998;13:1-8. (Pubitemid 28310435)
2. Ogawa T. Spermatogonial transplantation: The principle and possible applications. J Mol Med 2001;79:368-374. (Pubitemid 32692632)
3. Huleihel M, AbuElhija M, Lunenfeld E. In vitro culture of testicular germ cells: Regulatory factors and limitations. Growth Factors 2007; 25:236-251.
4. de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000;21:776-798.
5. Ehmcke J, Wistuba J, Schlatt S. Spermatogonial stem cells. Questions, models and perspectives. Hum Reprod Update 2006;12:275-282.
6. Clermont Y. Renewal spermatogenesis in man. Am J Anat 1996;118: 509-524.
7. Ramaswamy S, Marshall GR, McNeilly AS et al. Dynamics of the fol-licle- stimulating hormone (FSH)-inhibin B feedback loop and its role in regulating spermatogenesis in the adult male rhesus monkey (Macaca mulatta) as revealed by unilateral orchidectomy. Endocrinology 2000;141:18-27. (Pubitemid 32260341)
8. De Rooij DG, van de Kant HJ, Dol R et al. Long-term effects of irradiation before adulthood on reproductive function in the male rhesus monkey. Biol Reprod 2002;66:486-494. (Pubitemid 34101848)
9. Ehmcke JCM, Luetjens CM, Schlatt S. Clonal organization of proliferating spermatogonial stem cells in adult males of two species of nonhuman primates, Macaca mulatta and Callithrix jacchus. Biol Reprod 2005;72:293-300. (Pubitemid 40129704)
10. De Rooij D, Grootegoed J. Spermatogonial stem cells. Cur Opin Cell Biol 1998;10:694-701. (Pubitemid 28561012)
11. Dettin L, Ravindranath N, Hofmann MC et al. Morphological characterization of spermatogonial subtypes in the neonatal mouse testis. Biol Reprod 2003;69:1565-1571. (Pubitemid 37362839)
12. Luetjens CM, Weinbauer GF, Wistuba J. Primate spermatogenesis. New insights into comparative testicular organization, spermatogenic efficiency and endocrine control. Biol Rev Comb Philos Soc 2005;80: 475-488. (Pubitemid 41081468)
13. Sofikitis N, Pappas E, Kawatani A et al. Efforts to create an artificial testis: Culture systems of male germ cells under biochemical conditions resembling the seminiferous tubular biochemical environment. Hum Reprod Update 2005;11:229-259. (Pubitemid 40668110)
14. Tesarik J, Greco E, Mendoza C. Assisted reproduction with in vitro cultured testicular spermatozoa in cases of severe germ cell apoptosis: A pilot study. Hum Reprod 2001;16:2640-2645. (Pubitemid 34007484)
15. Sousa M, Cremades N, Alves C et al. Developmental potential of human spermatogenic cells co-cultured with Sertoli cells. Hum Reprod 2002;17:161-172. (Pubitemid 34130281)
16. Nagano M, Ryu BY, Brinster CJ et al. Maintenance of mouse male germ line stem cells in vitro. Biol Reprod 2003;68:2207-2214. (Pubitemid 36687013)
17. Skinner MK. Cell-cell interaction in the testis. Endocr Rev 1991;12: 45-77.
18. Kierszenbaum AL. Mammalian spermatogenesis in vivo and in vitro: A partnership of spermatogenic and somatic cell lineages. Endocr Rev 1994;15:116-134. (Pubitemid 24058599)
19. Saez JM. Leydig cells: Endocrine, paracrine, and autocrine regulation. Endocr Rev 1994;15:574-626. (Pubitemid 24328208)
20. Lee JH, Kim HJ, Kim H et al. In vitro spermatogenesis by threedimensional culture of rat testicular cells in collagen gel matrix. Biomaterials 2006;27:2845-2853. (Pubitemid 43165753)
21. Caires K, Broady J, McLean D. Maintaining the male germline: Regulation of spermatogonial stem cells. J Endocrinol 2010;205:133-145.
22. Chiarini-Garcia H, Hornick JR, Griswold MD et al. Distribution of type A spermatogonia in the mouse is not random. Biol Reprod 2001; 65:1179-1185. (Pubitemid 32927585)
23. Chiarini-Garcia H, Raymer AM, Russell LD. Non-random distribution of spermatogonia in rats: Evidence of niches in the seminiferous tubules. Reproduction 2003;126:669-680. (Pubitemid 37540628)
24. Yoshida S, Sukeno M, Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007; 317:1722-1726. (Pubitemid 47461832)
25. Yoshida S. Stem cells in mammalian spermatogenesis. Develop Growth Differ 2010;52:311-317.
26. Reece WQ, Male reproduction. In: Functional anatomy and physiology of domestic animals. 4th Ed. Wiley, 2009:432-457.
27. Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 2006;7:211-224.
28. He Z, Kokkinaki M, Dym M. Signaling molecules and pathways regulating the fate of spermatogonial stem cells. Microsc Res Tech 2009; 72:586-595.
29. Meachem S, von Schonfeldt V, Schlatt S. Spermatogonia: Stem cells with a great perspective. Reproduction 2001;121:825-834. (Pubitemid 32547311)
30. Brinster RL. Germline stem cell transplantation and transgenesis. Science 2002;296:2174-2176. (Pubitemid 34680289)
31. Creemers LB, den Ouden K, van Pelt AMM et al. Maintenance of adult mouse type A spermatogonia in vitro: Influence of serum and growth factors and comparison with prepubertal spermatogonial cell culture. Reproduction 2002;124:791-799. (Pubitemid 36104525)
32. Sofikitis N, Pappas E, Kawatani A et al. Efforts to create an artificial testis: Culture systems of male germ cells under biochemical conditions resembling the seminiferous tubular biochemical environment. Hum Reprod Update 2005;11:229-259. (Pubitemid 40668110)
33. Aslam I, Fishel S. Short-term in-vitro culture and cryopreservation of spermatogenic cells used for human in-vitro conception. Hum Reprod 1998;13:634-638. (Pubitemid 28171960)
34. Tesarik J, Greco E, Rienzi L et al. Differentiation of spermatogenic cells during in-vitro culture of testicular biopsy samples from patients with obstructive azoospermia effect of recombinant follicle stimulating hormone. Hum Reprod 1998;13:2772-2781. (Pubitemid 28482725)
35. Tanaka A, Nagayoshi M, Awata S et al. Completion of meiosis in human primary spermatocytes through in vitro coculture with Vero cells. Fertil Steril 2003;79:795-801. (Pubitemid 36279686)
36. Stukenborg J-B, Schlatt S, Simoni M et al. New horizons for in vitro spermatogenesis? An update on novel three-dimensional culture systems as tools for meiotic and post-meiotic differentiation of testicular germ cells. Mol Hum Reprod 2009;15:521-529.
37. Nagano M, Avarbock MR, Leonida EB et al. Culture of mouse spermatogonial stem cells. Tissue Cell 1998;30:389-397. (Pubitemid 28444790)
38. Steinberger A, Steinberger E, Perloff WH. Mammalian testes in organ culture. Exp Cell Res 1964;36:19-27.
39. Steinberger A, Steinberger E. Factors affecting spermatogenesis in organ cultures of mammalian testes. J Reprod Fertil 1967;2:117-124.
40. Ogawa T. In vitro spermatogenesis: The dawn of a new era in the study of male infertility. Int J Urol 2012;19:282-283.
41. Sato T, Katagiri K, Gohbara A et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature 2011;471:504-508.
42. Shinohara T, Avarbock MR, Brinster RL. Functional analysis of spermatogonial stem cells in steel and cryptorchid infertile mouse models. Dev Biol 2000;220:401-411. (Pubitemid 30228163)
43. Kikuchi K, Nakai M, Kashiwazaki N et al. Xenografting of gonadal tissues into mice as a possible method for conservation and utilization of porcine genetic resources. Anim Sci J 2011;82:495-503.
44. Jahnukainen K, Ehmcke J, Hou M et al. Testicular function and fertility preservation in male cancer patients. Best Pract Res Clin Endocrinol Metab 2011;25:287-302.
45. Hofmann MC, Narisawa S, Hess RA et al. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp Cell Res 1992;201:417-435.
46. Lee JH, Gye MC, Choi KW et al. In vitro differentiation of germ cells from nonobstructive azoospermic patients using three-dimensional culture in a collagen gel matrix. Fertil Steril 2007;84:824-833. (Pubitemid 46566356)
47. Stukenborg JB, Wistuba J, Luetjens CM et al. Coculture of spermatogonia with somatic cells in a novel three-dimensional soft-agar-cul-ture- system. J Androl 2008;29:312-329. (Pubitemid 351669021)
48. Parent-Massin D. Relevance of clonogenic assays in hematotoxicology. Cell Biol Toxicol 2001;17:87-94. (Pubitemid 32681045)
49. Weinbauer GF, Wessels J. Paracrine control of spermatogenesis. Andrologia 1999;31:249-262.
50. Grisswold MD. The central role of sertoli cells in spermatogenesis. Semin Cell Dev Biol 1998;9:411-416.
51. Salanova M, Stefanini M, De Curtis I et al. Integrin receptor alpha 6 beta 1 is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol Reprod 1995;52:79-87.
52. Giebel J, Loster K, Rune GM. Localization of integrin beta 1, alpha 1, alpha 5 and alpha 9 subunits in the rat testis. Int J Androl 1997;20: 3-9. (Pubitemid 27280934)
53. Hue D, Staub C, Perrard-Sapori MH et al. Meiotic differentiation of germinal cells in three-week cultures of whole cell population from rat seminiferous tubules. Biol Reprod 1998;59:379-387. (Pubitemid 28354880)
54. Lee DR, Kaproth MT, Parks JE. In vitro production of haploid germ cells from fresh or frozen-thawed testicular cells of neonatal bulls. Biol Reprod 2001;65:873-878. (Pubitemid 32777375)
55. Spradling A, Drummond-Barbosa D, Toshie K. Stem cells find their niche. Nature 2001;414:98-104. (Pubitemid 33041633)
56. Nayernia K, Nolte J, Michelmann HW et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell 2006;11:125-132. (Pubitemid 43960802)
57. Toyooka Y, Tsunekawa N, Akasu R et al. Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci USA 2003;100: 11457-11462. (Pubitemid 37205957)
58. Geijsen N, Horoschak M, Kim K et al. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 2004;427: 148-154. (Pubitemid 38094954)
59. Weaver VM, Peterson OW, Wang F et al. Revision of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997;137:231-245. (Pubitemid 27167310)
60. Zhang S. Beyond the Petri dish. Nat Biotechnol 2004;22:151-152. (Pubitemid 38160524)
61. Abu Elhija M, Lunenfeld E, Schlatt S et al. Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. Asian J Androl 2012;14:285-293.
62. Lin HS, Kuhn C, Kuo T. Clonal growth of hamster free alveolar cells in soft agar. J Exp Med 1975;142:877-886.
63. Quaroni A, Wands J, Trelstad RL et al. Epithelioid cell cultures from rat small intestine. Characterization by morphologic and immunologic criteria. J Cell Biol 1979;80:248-265. (Pubitemid 9091502)
64. Huleihel M, Douvdevani A, Segal S et al. Different regulatory levels involved in the generation of hemopoietic cytokines (CSFs and IL-6) in fibroblasts by inflammatory products. Cytokine 1993;5:47-56. (Pubitemid 23098834)
65. Horowitz D, King AG. Colorimetric determination of inhibition of hematopoietic progenitor cells in soft agar. J Immunol Methods 2000; 244:49-58.
66. Sadri-Ardekani H, Mizrak SC, van Daalen SK et al. Propagation of human spermatogonial stem cells in vitro. JAMA 2009;302: 2127-2134.
67. Sadri-Ardekani H, Akhondi MA, van der Veen F et al. In vitro propagation of human prepubertal spermatogonial stem cells. JAMA 2011; 305:2416-2418.
68. Koruji M, Shahverdi A, Janan A et al. Proliferation of small number of human spermatogonial stem cells obtained from azoospermic patients. J Assist Reprod Genet 2012 (in press).
69. Mirzapour T, Movahedin M, Tengku Ibrahim TA et al. Effects of basic fibroblast growth factor and leukaemia inhibitory factor on proliferation and short-term culture of human spermatogonial stem cells. Andrologia 2012;44:41-55.
70. Lim JJ, Sung SY, Kim HJ et al. Long-term proliferation and characterization of human spermatogonial stem cells obtained from obstructive and non-obstructive azoospermia under exogenous feeder-free culture conditions. Cell Prolif 2010;43:405-417.
71. Huleihel M, Lunenfeld E. Regulation of spermatogenesis by paracrine/ autocrine testicular factors. Asian J Androl 2004;6:259-268. (Pubitemid 39207284)