Melatonin improves spermatogonial stem cells transplantation efficiency in azoospermic mice

Iranian Journal of Basic Medical Sciences

Volumn 17, Issue 2, 2014, Pages 93-99

  Gholami, Mohammadreza ^a   Saki, Ghasem ^b   Hemadi, Masoud ^b   Khodadadi, Ali ^b   Mohammadi Asl, Javad ^b  

^a LORESTAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b AHVAZ JUNDISHAPUR UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Cryopreservation; Melatonin; Spermatogonial stem cells; Transplantation

Indexed keywords

EID: 84894232584     PISSN: 20083866     EISSN: 20083874     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Geens M, Goossens E, De Block G, Ning L, Van Saen D, Tournaye H. Autologus spermatogonial stem cell transplantation in man: current obstacles for a future clinical application. Hum Reprod Update 2008; 14:121-129.
2. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis, 1st ed. Clearwater, FL:Cache River Press; 1990.
3. McLean DJ, Johnston D, Russell L, Griswold M. Germ cell transplantation and the study of testicular function. Trends Endocrinol Metab 2001; 12:16-21.
4. Nagano M, Avarbock MR, Brinster RL. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes. Biol Reprod 1999; 60:1429-1436.
5. Hermann B, Sukhwani M, Lin C, Sheng Y, Tomko J, Rodriguez M, Shuttleworth J, McFarland D, Hobbs R, Pandolfi P, Schatten G, Orwig K. Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem Cells 2007;25:2330-2338.
6. Brinster CJ, Ryu BY, Avarbock MR, Karagenc L, Brinster RL, Orwig KE. Restoration of fertility by germ cell transplantation requires effective recipient preparation. Biol Reprod 2003; 69:412-420.
7. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 1994; 91:11298-11302.
8. Honaramooz A, Behboodi E, Blash S, Megee SO, Dobrinski I. Germ cell transplantation in goats. Mol Reprod Dev 2003; 64:422-428.
9. Kim Y, Turner D, Nelson J, Dobrinski I, McEntee M, Travis AJ. Production of donor-derived sperm after spermatogonial stem cell transplantation in the dog. Reproduction 2008; 136:823-831.
10. Mikkola M, Sironen A, Kopp C, Taponen J, Sukura A, Vilkki J, et al. Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-tail sperm defect. Reprod Domest Anim 2006; 41:124-128.
11. Nagano M, Mccarrey JR, Brinster RL. Primate spermatogonial stem cells colonize mouse testes. Biol Reprod 2001; 64:1409-1416.
12. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med 2000; 6:29-34.
13. Orwig KE, Schlatt S. Cryopreservation and transplantation of spermatogonia and testicular tissue for preservation of male fertility. J Natl Cancer Inst Monogr 2005; 51-56.
14. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc Natl Acad Sci U S A 2001; 98:6186-6191.
15. Goossens E, Frederickx V, De Block G, Van Steirteghem AC, Tournaye H. Reproductive capacity of sperm obtained after germ cell transplantation in a mouse model. Hum Reprod 2003; 18:1874-1880.
16. Goossens E, Frederickx V, De Block G, Van Steirteghem A, Tournaye H. Evaluation of in vivo conception after testicular stem cell transplantation in a mouse model shows altered post-implantation development. Hum Reprod 2006; 21:2057-2060.
17. Goossens E, De Block G, Tournaye H. Computer-assisted motility analysis of spermatozoa obtained after spermatogonial stem cell transplantation in the mouse. Fertil Steril 2008a; 90:1411-1416.
18. Jung FJ, Yang L, Harter L, Inci I, Schneiter D, Lardinois D, et al. Melatonin in vivo prolongs cardiac allograft survival in rats. J Pineal Res 2004; 37:36-41.
19. Fildes JE, Yonan N, Keevil BG. Melatonin--a pleiotropic molecule involved in pathophysiological processes following organ transplantation. Immunology 2009; 127:443-449.
20. Hemadi M, Abolhassani F, Akbari M, Sobhani A, Pasbakhsh P, Ahrlund-Richter L, et al. Melatonin promotes the cumulus-oocyte complexes quality of vitrified-thawed murine ovaries; with increased mean number of follicles survival and ovary size following heterotopic transplantation. Eur J Pharmacol 2009; 618:84-90.
21. Hemadi M, Zargar M, Sobhani A. Assessment of morphological and functional changes in neonate vitrified testis grafts after host treatment with melatonin. Folia Morphol (Warsz) 2011; 70:95-102.
22. Hardeland R, Cardinali DP, Srinivasan V, Spence DW, Brown GM, Pandi-Perumal SR. Melatonin--a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 2011; 93:350-384.
23. Zawilska JB, Skene DJ, Arendt J. Physiology and pharmacology of melatonin in relation to biological rhythms. Pharmacol Rep 2009; 61:383-410.
24. Ahmad R, Haldar C. Melatonin and androgen receptor expression interplay modulates cell-mediated immunity in tropical rodent Funambulus pennanti: an in vivo and in vitro study. Scand J Immunol 2010; 71:420-430.
25. Dasilva CM, Macias-garcia B, Miro-moran A, González-Fernández L, Morillo-Rodriguez A, Ortega-Ferrusola C, et al. Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. J Pineal Res 2011; 51:172-179.
26. Martin-renedo J, Mauriz JL, Jorquera F, Ruiz-Andrés O, González P, González-Gallego J. Melatonin induces cell cycle arrest and apoptosis in hepatocarcinoma HepG2 cell line. J Pineal Res 2008; 45:532-540.
27. Millan-plano S, Piedrafita E, Miana-mena FJ, Fuentes-Broto L, Martínez-Ballarín E, López-Pingarrón L, et al. Melatonin and structurally-related compounds protect synaptosomal membranes from free radical damage. Int J Mol Sci 2010; 11:312-328.
28. Radogna F, Cristofanon S, Paternoster L, D'Alessio M, De Nicola M, Cerella C, et al. Melatonin antagonizes the intrinsic pathway of apoptosis via mitochondrial targeting of Bcl-2. J Pineal Res 2008; 44:316-325.
29. Radogna F, Paternoster L, Albertini MC, Accorsi A, Cerella C, D'Alessio M, et al. Melatonin as an apoptosis antagonist. Ann N Y Acad Sci 2006; 1090:226-233.
30. Radogna F, Paternoster L, Albertini MC, Cerella C, Accorsi A, Bucchini A, et al. Melatonin antagonizes apoptosis via receptor interaction in U937 monocytic cells. J Pineal Res 2007; 43:154-162.
31. Reiter RJ, Tan DX, Manchester LC, Paredes SD, Mayo JC, Sainz RM. Melatonin and reproduction revisited. Biol Reprod 2009; 81:445-456.
32. Zhao Y, Qi LW, Wang WM, Saxena PK, Liu CZ. Melatonin improves the survival of cryopreserved callus of Rhodiola crenulata. J Pineal Res 2010; 50:83-88.
33. Gholami M, Saki G, Hemadi M, Khodadadi A, Mohammadi-asl J. Supplementation vitrified-thawed media with melatonin do not protecting immature mouse testicular tissue from vitrified-thawed induced injury. Asian J Anim Veterinary Advances 2012; 7:940-949.
34. Milazzo JP, Vaudreuil L, Cauliez B, Gruel E, Massé L, Mousset-Siméon N, et al. Comparison of conditions for cryopreservation of testicular tissue from immature mice. Hum Reprod 2008; 23:17-28.
35. Shinohara K, Avarbock MR, Brinster RL. beta1-and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA 1999; 96:5504-5509.
36. Ogawa T, Arechaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 1997; 41:111-122.
37. Zheng J, Xia X, Ding H, Yan A, Hu S, Gong X, Zong S, Zhang Y, Sheng HZ. Erasure of the paternal transcription program during spermiogenesis: the first step in the reprogramming of sperm chromatin for zygotic development. Dev Dyn 2008; 237:1463-1476.
38. Lewis-Johnes DI, Kerrigan DD. A modified johnsen's count for evaluation of Spermatogenesis in the rat. IRCS Med Sci 1985; 13:510-511.
39. Anjamrooz SH, Movahedin M, Mowla SJ, Anvand SP. Assessment of morphological and functional changes in the mouse testis and epididymal sperms following busulfan treatment. Iran Biomed J 2007; 11:15-22.
40. Sanchez-hidalho M, De La Lastra CA, Carrascosa-salmoral M, P et al. Age-related changes in melatonin synthesis in rat extrapineal tissues. Exp Gerontol 2009; 44:328-334.
41. Aziz A, Metwally DH, Halla GB. The effect of stem cell therapy versus melatonin on the changes induced by busulfan in the testes of adult rat: histological and immunohistochemical studies. Egypt J Histol 2013; 36:175-184.
42. Mohammadghasemi F, Faghani M, Khajeh S. The protective effects of melatonin on the histological changes of testis in busulfan-treated adult mice. J Reprod Infertil 2010; 11:67-76.
43. Atessahin A, Sahna E, Turk G, Ceribaşi AO, Yilmaz S, Yüce A, et al. Chemoprotective effect of melatonin against cisplatin-induced testicular toxicity in rats. J Pineal Res 2006; 41:21-27.
44. Gunelie E, Tugyan K, Ozturk H, Gumustekin M, Cilaker S, Uysal N. Effect of melatonin on testicular damage in streptozotocin-induced diabetes rats. Eur Surg Res 2008; 40:354-360.
45. Ji YL, Wang H, Meng C, Zhao XF, Zhang C, Zhang Y, et al. Melatonin alleviates cadmium-induced cellular stress and germ cell apoptosis in testes. J Pineal Res 2012; 52:71-79.
46. Davanipour Z, Poulsen HE, Weimann A, Sobel E. Endogenous melatonin and oxidatively damaged guanine in DNA. BMC Endocr Disord 2009; 9:22.
47. Take G, Erdogan D, Helvacioglu F, Göktas G, Ozbey G, Uluoglu C, et al. Effect of melatonin and time of administration on irradiation-induced damage to rat testes. Braz J Med Biol Res 2009; 42:621-628.
48. Lissoni P, Chilelli M, Villa S, Cerizza L, Tancini G. Five years survival in metastatic non-small cell lung cancer patients treated with chemotherapy alone or chemotherapy and melatonin: a randomized trial. J Pineal Res 2003; 35:12-15.
49. Vijayalaxmi, Thpmas CR, Reiter RJ, Herman TS. Melatonin: from basic research to cancer treatment clinics. J Clin Oncol 2002; 20:2575-2601.
50. Mohammadghasemi F, Faghani M, Falahkarkan M. The protective effect of melatonin on sperm parameters, epididymis and seminal vesicle morphology in adult mouse treated with busulfan. J Iran Anatomi Sci 2010; 8:25-36.
51. D'istria M, Serino I, Izzo G, Ferrara D, De Rienzo G, Minucci S. Effects of melatonin treatment on Leydig cell activity in the testis of the frog Rana esculenta. Zygote 2004; 12:293-299.
52. Pizarro JG, Yeste-velasco M, Esparza JL, Verdaguer E, Pallàs M, Camins A, et al. The antiproliferative activity of melatonin in B65 rat dopaminergic neuroblastoma cells is related to the downregulation of cell cycle-related genes. J Pineal Res 2008; 45:8-16.
53. Tam CW, Chan KW, Liu VW, Pang B, Yao KM, Shiu SY. Melatonin as a negative mitogenic hormonal regulator of human prostate epithelial cell growth: potential mechanisms and clinical significance. J Pineal Res 2008; 45:403-412.
54. Gholami M, Saki G, Hemadi M, Khodadadi A, Mohamma-di-Asl J. Melatonin effect on expression apoptotic genes in vitrified-thawed 6-old-days mouse spermatogonial stem cells type A. Iran J Basic Med Sci 2013; 16:906-909.