Proliferation of small number of human spermatogonial stem cells obtained from azoospermic patients

Journal of Assisted Reproduction and Genetics

Volumn 29, Issue 9, 2012, Pages 957-967

  Koruji, Morteza ^a,b   Shahverdi, Abdulhossein ^b   Janan, Arghavan ^b   Piryaei, Abbas ^c   Lakpour, Mohammad Reza ^b   Sedighi, Mohammad Ali Gilani ^b,d  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Culture; Non obstructive azoospermia; Spermatogonial stem cells; Testicular biopsy

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LAMININ; LEUKEMIA INHIBITORY FACTOR;

ARTICLE; AZOOSPERMIA; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SPERMATOGONIUM; STEM CELL; TESTIS; TRANSMISSION ELECTRON MICROSCOPY; XENOTRANSPLANTATION;

ANALYSIS OF VARIANCE; ANIMALS; AZOOSPERMIA; BIOLOGICAL MARKERS; BIOPSY; BUSULFAN; CELL COUNT; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HUMANS; INFERTILITY, MALE; LAMININ; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERUM; SPERMATOGONIA; STEM CELL TRANSPLANTATION; STEM CELLS; TESTIS; TRANSPLANTATION, HETEROLOGOUS;

MUS;

EID: 84867402765     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-012-9817-8     Document Type: Article

References (57)

1. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11298-302.
2. Brinster RL. Male germline stem cells: from mice to men. Science (New York, NY). 2007;316(5823):404-5. doi:10.1126/science.1137741.
3. Radford J, Shalet S, Lieberman B. Fertility after treatment for cancer. Questions remain over ways of preserving ovarian and testicular tissue. BMJ. 1999;319(7215):935-6.
4. Honaramooz A, Behboodi E, Blash S, Megee SO, Dobrinski I. Germ cell transplantation in goats. Mol Reprod Dev. 2003;64(4):422-8.
5. Izadyar F, Den Ouden K, Stout TA, Stout J, Coret J, Lankveld DP, et al. Autologous and homologous transplantation of bovine spermatogonial stem cells. Reproduction. 2003;126(6):765-74.
6. Schlatt S, Kim SS, Gosden R. Spermatogenesisand steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts. Reproduction. 2002;124(3):339-46.
7. Lim JJ, Sung SY, Kim HJ, Song SH, Hong JY, Yoon TK, 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(4):405-17. doi:10.1111/j.1365-2184. 2010.00691.x.
8. 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.
9. Aponte PM, Soda T, Teerds KJ, Mizrak SC, van de Kant HJ, de Rooij DG. Propagation of bovine spermatogonial stem cells in vitro. Reproduction. 2008;136(5):543-57.
10. Brinster RL, Nagano M. Spermatogonial stem cell transplantation, cryopreservation and culture. Semin Cell Dev Biol. 1998;9(4):401-9.
11. Mirzapour T, Movahedin M, Ibrahim TABT, Haron AW, Makulati Z, Nowroozi M. Effect of donor cells concentration on colonization of human spermatogonial stem cells in recipient mouse testes. J Biol Sci. 2010;10:730-8.
12. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69(2):612-6.
13. Sadri-Ardekani H, Mizrak SC, van Daalen SK, Korver CM, Roepers-Gajadien HL, Koruji M, et al. Propagation of Human Spermatogonial Stem Cells In Vitro. JAMA. 2009;302(19):2127. doi:10.1001/jama.2009.1689
14. Anjamrooz SH, Movahedin M, Tiraihi T, Mowla SJ. Graft efficiency of co-cultured spermatogonial cells using sperm assay in epididymal lumen of recipient mice. Cell J (Yakhteh). 2006;7:242-9.
15. Kanatsu-Shinohara M, Inoue K, Lee J, Miki H, Ogonuki N, Toyokuni S, et al. Anchorage-independent growth of mouse male germline stem cells in vitro. Biol Reprod. 2006;74(3):522-9. doi:10.1095/biolreprod.105.046441.
16. Ebata KT, Yeh JR, Zhang X, Nagano MC. Soluble growth factors stimulate spermatogonial stem cell divisions that maintain a stem cell pool and produce progenitors in vitro. Exp Cell Res. 2011;317(10):1319-29. doi:10.1016/j.yexcr. 2011.03.013.
17. Kanatsu-Shinohara M, Miki H, Inoue K, Ogonuki N, Toyokuni S, Ogura A, et al. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol Reprod. 2005;72(4):985-91. doi:10.1095/biolreprod. 104.036400.
18. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA. 2004;101(47):16489-94.
19. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science (New York, NY). 2000;287(5457):1489-93.
20. Kuijk E, Colenbrander B, Roelen B. The effects of growth factors on in vitro-cultured porcine testicular cells. Reproduction. 2009. doi:10.1530/REP-09-0138.
21. Sadri-Ardekani H, Akhondi MA, van der Veen F, Repping S, van Pelt AM. In vitro propagation of human prepubertal spermatogonial stem cells. JAMA. 2011;305(23):2416-8. doi:10.1001/jama.2011.791.
22. Aponte PM, van Bragt MP, de Rooij DG, van Pelt AM. Spermatogonial stem cells: characteristics and experimental possibilities. APMIS. 2005;113(11-12):727-42.
23. Huang YH, Chin CC, Ho HN, Chou CK, Shen CN, Kuo HC, et al. Pluripotency of mouse spermatogonial stem cells maintained by IGF-1-dependent pathway. FASEB J. 2009;23(7):2076-87. doi:10.1096/fj.08-121939.
24. Kim J, Seandel M, Falciatori I, Wen D, Rafii S. CD34+ testicular stromal cells support long-term expansion of embryonic and adult stem and progenitor cells. Stem cells (Dayton, Ohio). 2008;26(10):2516-22. doi:10.1634/stemcells. 2008-0379.
25. Koruji M, Movahedin M, Mowla SJ, Gourabi H, Arfaee AJ. Efficiency of adult mouse spermatogonial stem cell colony formation under several culture conditions. Vitro Cell Dev Biol Anim. 2009;45(5-6):281-9. doi:10.1007/s11626- 008-9169-y.
26. Mohamadi SM, Movahedin M, Koruji SM, Jafarabadi MA, Makoolati Z. Comparison of colony formation in adult mouse spermatogonial stem cells developed in Sertoli and STO coculture systems. Andrologia. 2012;44(1):431-437. doi:10.1111/j.1439-0272.2011.01201.x.
27. Liu S, Tang Z, Xiong T, Tang W. Isolation and characterization of human spermatogonial stem cells. Reprod Biol Endocrinol. 2011;9:141. doi:10.1186/1477-7827-9-141.
28. Mirzapour T, Movahedin M, Tengku Ibrahim TA, Koruji M, Haron AW, Nowroozi MR, 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. doi:10.1111/j.1439-0272.2010.01135.x.
29. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11303-7.
30. Rowley MJ, Berlin JD, Heller CG. The ultrastructure of four types of human spermatogonia. Z Zellforsch Mikrosk Anat. 1971;112(2):139-57.
31. Hofmann MC, Braydich-Stolle L, Dym M. Isolation of male germline stem cells; influence of GDNF. Dev Biol. 2005;279(1):114-24.
32. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116(6):769-78.
33. Li L, Xie T. Stem cell niche: structure and function. Annu Rev CellDev Biol. 2005;21:605-31. doi:10.1146/annurev. cellbio.21.012704.131525.
34. Simon L, Ekman GC, Tyagi G, Hess RA, Murphy KM, Cooke PS. Common and distinct factors regulate expression of mRNA for ETV5 and GDNF, Sertoli cell proteins essential for spermatogonial stem cell maintenance. Exp Cell Res. 2007;313(14):3090-9. doi:10.1016/j.yexcr.2007.05.002.
35. Aponte P, de Rooij D. Biomanipulation of bovine spermatogonial stem cells. Anim Reprod. 2008;5:16-22.
36. Dirami G, Ravindranath N, Pursel V, Dym M. Effects of stem cell factor and granulocyte macrophage-colony stimulating factor on survival of porcine type A spermatogonia cultured in KSOM. Biol Reprod. 1999;61(1):225-30.
37. Shinohara T, Avarbock MR, Brinster RL. beta1-and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA. 1999;96(10):5504-9.
38. Orwig KE, Shinohara T, Avarbock MR, Brinster RL. Functional analysis of stem cells in the adult rat testis. Biol Reprod. 2002;66(4):944-9.
39. Shinohara T, Avarbock MR, Brinster RL. Functional analysis of spermatogonial stem cells in Steel and cryptorchid infertile mouse models. Dev Biol. 2000;220(2):401-11. doi:10.1006/dbio.2000.9655.
40. Kokil SN, Patil PR, Mahadik KR, Paradkar AR. Effect of molecular weight of hydrolyzed gelatin on its binding properties in tablets: a technical note. AAPS PharmSciTech. 2004;5(3):38-42. doi:10.1208/pt050341.
41. Conrad S, Renninger M, Hennenlotter J, Wiesner T, Just L, Bonin M, et al. Generation of pluripotent stem cells from adult human testis. Nature. 2008;456(7220):344-9.
42. Kanatsu-Shinohara M, Lee J, Inoue K, Ogonuki N, Miki H, Toyokuni S, et al. Pluripotency of a single spermatogonial stem cell in mice. Biol Reprod. 2008;78(4):681-7. doi:10.1095/biolreprod.107.066068.
43. Hermann B, Sukhwani M, Hansel M, Orwig K. Spermatogonial stem cells in higher primates: are there differences to those in rodents? Reproduction. 2009. doi:10.1530/REP-09-0255.
44. Ohbo K, Yoshida S, Ohmura M, Ohneda O, Ogawa T, Tsuchiya H, et al. Identification and characterization of stem cells in prepubertal spermatogenesis in mice small star, filled. Dev Biol. 2003;258(1):209-25.
45. Ohmura M, Yoshida S, Ide Y, Nagamatsu G, Suda T, Ohbo K. Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch Histol Cytol. 2004;67(4):285-96.
46. Bhartiya D, Kasiviswanathan S, Unni SK, Pethe P, Dhabalia JV, Patwardhan S, et al. Newer insights into premeiotic development of germ cells in adult human testis using Oct-4 as astem cell marker. J Histochem Cytochem. 2010;58(12):1093-106. doi:10.1369/jhc.2010.956870.
47. Izadyar F, Wong J, Maki C, Pacchiarotti J, Ramos T, Howerton K, et al. Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Hum Reprod. 2011;26(6):1296-306. doi:10.1093/humrep/der026.
48. Dann CT, Alvarado AL, Molyneux LA, Denard BS, Garbers DL, Porteus MH. Spermatogonial stem cell self-renewal requires OCT4, a factor downregulated during retinoic acid-induced differentiation. Stem cells (Dayton, Ohio). 2008;26(11):2928-37. doi:10.1634/stemcells.2008-0134.
49. Kubota H, Avarbock MR, Brinster RL. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci USA. 2003;100(11):6487-92.
50. Reijo R, Seligman J, Dinulos MB, Jaffe T, Brown LG, Disteche CM, et al. Mouse autosomal homolog of DAZ, a candidate male sterility gene in humans, is expressed in male germ cells before and after puberty. Genomics. 1996;35(2):346-52. doi:10.1006/geno. 1996.0366.
51. Hermann BP, Sukhwani M, Lin CC, Sheng Y, Tomko J, Rodriguez M, et al. Characterization, cryopreservation, and ablation of spermatogonial stem cells in adult rhesus macaques. Stem cells (Dayton, Ohio). 2007;25(9):2330-8. doi:10.1634/stemcells.2007-0143.
52. Brinster RL. Germline stem cell transplantation and transgenesis. Science (New York, NY. 2002;296(5576):2174-6.
53. McLean DJ. Spermatogonial stem cell transplantation, testicular function, and restoration of male fertility in mice. Methods Mol Biol (Clifton, NJ). 2008;450:149-62.
54. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci USA. 2000;97(15):8346-51.
55. Bellve AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol. 1977;74(1):68-85.
56. Chiarini-Garcia H, Russell LD. High-resolution light microscopic characterization of mouse spermatogonia. Biol Reprod. 2001;65(4):1170-8.
57. Morena AR, Boitani C, Pesce M, De Felici M, Stefanini M. Isolation of highly purified type A spermatogonia from prepubertal rat testis. J Androl. 1996;17(6):708-17.