Establishment and applications of male germ cell and Sertoli cell lines

Reproduction

Volumn 152, Issue 2, 2016, Pages R31-R40

  Wang, Hong ^a   Wen, Liping ^a   Yuan, Qingqing ^a   Sun, Min ^a   Niu, Minghui ^a   He, Zuping ^a,b,c,d  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c Shanghai Key Laboratory of Assisted Reproduction and Reproductive Genetics   (China)

^d Shanghai Key Laboratory of Reproductive Medicine   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; SIMIAN VIRUS 40 LARGE T ANTIGEN; UNCLASSIFIED DRUG; VIRUS LARGE T ANTIGEN;

CELL IMMORTALIZATION; GENE; GENETIC TRANSFECTION; GERM CELL; HUMAN; MALE; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; RAT; REVIEW; SERTOLI CELL; SPERMATOCYTE; SPERMATOGONIUM; TELOMERASE REVERSE GENE; TEMPERATURE SENSITIVE MUTANT; TRANSGENIC ANIMAL; ANIMAL; CYTOLOGY; INFERTILITY, MALE; PHYSIOLOGY; SPERMATOGENESIS; STEM CELL;

ANIMALS; GERM CELLS; HUMANS; INFERTILITY, MALE; MALE; SERTOLI CELLS; SPERMATOGENESIS; STEM CELLS;

EID: 84979536797     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-15-0546     Document Type: Review

References (67)

1. Beverdam A, Wilhelm D & Koopman P 2003 Molecular characterization of three gonad cell lines. Cytogenetic and Genome Research 101 242-249. (doi:10.1159/000074344)
2. Bourdon V, Lablack A, Abbe P, Segretain D & Pointis G 1998 Characterization of a clonal Sertoli cell line using adult PyLT transgenic mice. Biology of Reproduction 58 591-599. (doi:10.1095/biolreprod58.2.591)
3. Blagosklonova O, Joanne C, Roux C, Bittard H, Fellmann F & Bresson JL 2002 Absence of anti-Mullerian hormone (AMH) and M2A immunoreactivities in Sertoli cell-only syndrome and maturation arrest with and without AZF microdeletions. Human Reproduction 17 2062-2065. (doi:10.1093/humrep/17.8.2062)
4. Chen Z, Sun M, Yuan Q, Niu M, Yao C, Hou J, Wang H, Wen L, Liu Y, Li Z et al. 2016 Generation of functional hepatocytes from human spermatogonial stem cells. Oncotarget 7 8879-8895. (doi:10.18632/oncotarget.7092)
5. Chuang CK, Lee KH, Fan CT & Su YS 2007 FSH-sensitive murine sertoli cell lines immortalized by human telomerase gene hTERT express the androgen receptor in response to TNF-alpha stimulation. Bioscience Reports 27 403-411. (doi:10.1007/s10540-007-9063-y)
6. Dutertre M, Rey R, Porteu A, Josso N & Picard JY 1997 A mouse Sertoli cell line expressing anti-Mullerian hormone and its type II receptor. Molecular and Cellular Endocrinology 136 57-65. (doi:10.1016/S0303-7207(97)00214-1)
7. Feng LX, Chen Y, Dettin L, Pera RA, Herr JC, Goldberg E & Dym M 2002 Generation and in vitro differentiation of a spermatogonial cell line. Science 297 392-395. (doi:10.1126/science.1073162)
8. Fukasawa K, Sakoulas G, Pollack RE & Chen S 1991 Excess wild-type p53 blocks initiation and maintenance of simian virus 40 transformation. Molecular and Cellular Biology 11 3472-3483. (doi:10.1128/MCB.11.7.3472)
9. Golestaneh N, Kokkinaki M, Pant D, Jiang J, DeStefano D, Fernandez-Bueno C, Rone JD, Haddad BR, Gallicano GI & Dym M 2009 Pluripotent stem cells derived from adult human testes. Stem Cells and Devlopment 18 1115-1126. (doi:10.1089/scd.2008.0347)
10. Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W et al. 2006 Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440 1199-1203. (doi:10.1038/nature04697)
11. Guo Y, Hai Y, Yao C, Chen Z, Hou J, Li Z & He Z 2015 Long-term culture and significant expansion of human Sertoli cells whilst maintaining stable global phenotype and AKT and SMAD1/5 activation. Cell Communication and Signaling 13 20. (doi:10.1186/s12964-015-0101-2)
12. Hai Y, Hou J, Liu Y, Yang H, Li Z & He Z 2014 The roles and regulation of Sertoli cells in fate determinations of spermatogonial stem cells and spermatogenesis. Seminars in Cell & Developmental Biology 29 66-75. (doi:10.1016/j.semcdb.2014.04.007)
13. He Z, Jiang J, Hofmann MC & Dym M 2007 Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biology of Reproduction 77 723-733. (doi:10.1095/biolreprod.107.062513)
14. He Z, Jiang J, Kokkinaki M, Golestaneh N, Hofmann MC & Dym M 2008 Gdnf upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 26 266-278. (doi:10.1634/stemcells.2007-0436)
15. He Z, Jiang J, Kokkinaki M & Dym M 2009 Nodal signaling via an autocrine pathway promotes proliferation of mouse spermatogonial stem/progenitor cells through Smad2/3 and Oct-4 activation. Stem Cells 27 2580-2590. (doi:10.1002/stem.v27:10)
16. He Z, Kokkinaki M, Jiang J, Dobrinski I & Dym M 2010 Isolation, characterization, and culture of human spermatogonia. Biology of Reproduction 82 363-372. (doi:10.1095/biolreprod.109.078550)
17. Hofmann MC, Narisawa S, Hess RA & Millan JL 1992 Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Experimental Cell Research 201 417-435. (doi:10.1016/0014-4827(92)90291-F)
18. Hofmann MC, Hess RA, Goldberg E & Millan JL 1994 Immortalized germ cells undergo meiosis in vitro. PNAS 91 5533-5537. (doi:10.1073/pnas.91.12.5533)
19. Hofmann MC, Van Der Wee KS, Dargart JL, Dirami G, Dettin L & Dym M 2003 Establishment and characterization of neonatal mouse sertoli cell lines. Journal of Andrololgy 24 120-130.
20. Hofmann MC, Braydich-Stolle L, Dettin L, Johnson E & Dym M 2005 Immortalization of mouse germ line stem cells. Stem Cells 23 200-210. (doi:10.1634/stemcells.2003-0036)
21. Hou J, Niu M, Liu L, Zhu Z, Wang X Sun M, Yuan Q, Yang S, Zeng W, Liu Y et al. 2015 Establishment and characterization of human germline stem cell line with unlimited proliferation potentials and no tumor formation. Scientific Reports 5 16922. (doi:10.1038/srep16922)
22. Jiang C, Hall SJ & Boekelheide K 1997 Development and characterization of a prepubertal rat Sertoli cell line, 93RS2. Journal of Andrology 18 393-399.
23. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, Miki H, Baba S, Kato T, Kazuki Y, Toyokuni S et al. 2004 Generation of pluripotent stem cells from neonatal mouse testis. Cell 119 1001-1012. (doi:10.1016/j.cell.2004.11.011)
24. Kanatsu-Shinohara M, Inoue K, Takashima S, Takehashi M, Ogonuki N, Morimoto H, Nagasawa T, Ogura A & Shinohara T 2012 Reconstitution of mouse spermatogonial stem cell niches in culture. Cell Stem Cell 11 567-578. (doi:10.1016/j.stem.2012.06.011)
25. Katakura Y, Alam S & Shirahata S 1998 Immortalization by gene transfection. Methods in Cell Biology 57 69-91. (doi:10.1016/S0091-679X(08)61573-3)
26. Kaur G, Thompson LA, Pasham M, Tessanne K, Long CR & Dufour JM 2014 Sustained expression of insulin by a genetically engineered sertoli cell line after allotransplantation in diabetic BALB/c mice. Biology of Reproduction 90 109. (doi:10.1095/biolreprod.113.115600)
27. Ko K, Tapia N, Wu G, Kim JB, Bravo MJ, Sasse P, Glaser T, Ruau D, Han DW, Greber B et al. 2009 Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 5 87-96. (doi:10.1016/j.stem.2009.05.025)
28. Konrad L, Munir Keilani M, Cordes A, Völck-Badouin E, Laible L, Albrecht M, Renneberg H & Aumüller G 2005 Rat Sertoli cells express epithelial but also mesenchymal genes after immortalization with SV40. Biochimica et Biophysica Acta 1722 6-14. (doi:10.1016/j.bbagen.2004.10.015)
29. Lee J, Kanatsu-Shinohara M, Morimoto H, Kazuki Y, Takashima S, Oshimura M, Toyokuni S & Shinohara T 2009 Genetic reconstruction of mouse spermatogonial stem cell self-renewal in vitro by Ras-cyclin D2 activation. Cell Stem Cell 5 76-86. (doi:10.1016/j.stem.2009.04.020)
30. Liang ZG, Shelton JA & Goldberg E 1986 Non-cross-reactivity of antibodies to murine LDH-C4 with LDH-A4 and LDH-B4. Journal of Experimental Zoology 240 377-384. (doi:10.1002/(ISSN)1097-010X)
31. Mather JP 1980 Establishment and characterization of two distinct mouse testicular epithelial cell lines. Biology of Reproduction 23 243-252. (doi:10.1095/biolreprod23.1.243)
32. McCarrey JR, Kumari M, Aivaliotis MJ, Wang Z, Zhang P, Marshall F & Vandeberg JL 1996 Analysis of the cDNA and encoded protein of the human testis-specific PGK-2 gene. Developmental Genetics 19 321-332. (doi:10.1002/(ISSN)1520-6408)
33. Morales CP, Holt SE, Ouellette M, Kaur KJ, Yan Y, Wilson KS, White MA, Wright WE & Shay JW 1999 Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nature Genetics 21 115-118. (doi:10.1038/5063)
34. Paquis-Flucklinger V, Michiels JF, Vidal F, Alquier C, Pointis G, Bourdon V, Cuzin F & Rassoulzadegan M 1993 Expression in transgenic mice of the large T antigen of polyomavirus induces Sertoli cell tumours and allows the establishment of differentiated cell lines. Oncogene 8 2087-2094.
35. Pognan F, Masson MT, Lagelle F & Charuel C 1997 Establishment of a rat Sertoli cell line that displays the morphological and some of the functional characteristics of the native cell. Cell Biology and Toxicology 13 453-463. (doi:10.1023/A:1007475928452)
36. Rassoulzadegan M, Paquis-Flucklinger V, Bertino B, Sage J, Jasin M, Miyagawa K, van Heyningen V, Besmer P & Cuzin F 1993 Transmeiotic differentiation of male germ cells in culture. Cell 75 997-1006. (doi:10.1016/0092-8674(93)90543-Y)
37. Regadera J, Martinez-Garcia F, Gonzalez-Peramato P, Serrano A, Nistal M & Suarez-Quian C 2001 Androgen receptor expression in sertoli cells as a function of seminiferous tubule maturation in the human cryptorchid testis. Journal of Clinical Endocrinology & Metabolism 86 413-421.
38. Roberts KP, Banerjee PP, Tindall JW & Zirkin BR 1995 Immortalization and characterization of a Sertoli cell line from the adult rat. Biology of Reproduction 53 1446-1453. (doi:10.1095/biolreprod53.6.1446)
39. Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y & Ogawa T 2011 In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471 504-507. (doi:10.1038/nature09850)
40. Sato Y, Yoshida K, Nozawa S, Yoshiike M, Arai M, Otoi T & Iwamoto T 2013 Establishment of adult mouse Sertoli cell lines by using the starvation method. Reproduction 145 505-516. (doi:10.1530/REP-12-0086)
41. Schlegel PN 2009 Evaluation of male infertility. Minerva Ginecologica 61 261-283.
42. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, Chavala S Scherr DS, Zhang F, Torres R, Gale NW et al. 2007 Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449 346-350. (doi:10.1038/nature06129)
43. Sette C, Dolci S, Geremia R & Rossi P 2000 The role of stem cell factor and of alternative c-kit gene products in the establishment, maintenance and function of germ cells. International Journal of Developmental Biology 44 599-608.
44. Sharpe RM, McKinnell C, Kivlin C & Fisher JS 2003 Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125 769-784. (doi:10.1530/rep.0.1250769)
45. Sheng C, Zheng Q, Wu J, Xu Z, Sang L, Wang L, Guo C, Zhu W, Tong M, Liu L et al. 2012 Direct reprogramming of Sertoli cells into multipotent neural stem cells by defined factors. Cell Research 22 208-218. (doi:10.1038/cr.2011.175)
46. Simon L, Ekman GC, Kostereva N, Zhang Z, Hess RA, Hofmann MC & Cooke PS 2009 Direct transdifferentiation of stem/progenitor spermatogonia into reproductive and nonreproductive tissues of all germ layers. Stem Cells 27 1666-1675. (doi:10.1002/stem.v27:7)
47. Sneddon SF, Walther N & Saunders PT 2005 Expression of androgen and estrogen receptors in sertoli cells: studies using the mouse SK11 cell line. Endocrinology 146 5304-5312. (doi:10.1210/en.2005-0914)
48. Sun H, Zhang G, Dong F, Wang F & Cao W 2014 Reprogramming sertoli cells into pluripotent stem cells. Cell Reprogram 16 196-205. (doi:10.1089/cell.2013.0083)
49. Sze KL, Lee WM & Lui WY 2008 Expression of CLMP, a novel tight junction protein, is mediated via the interaction of GATA with the Kruppel family proteins, KLF4 and Sp1, in mouse TM4 Sertoli cells. Journal of Cellular Physiology 214 334-344.
50. Tabuchi Y, Ohta S, Yanai N, Obinata M, Kondo T, Fuse H & Asano S 2002 Development of the conditionally immortalized testicular Sertoli cell line TTE3 expressing Sertoli cell specific genes from mice transgenic for temperature sensitive simian virus 40 large T antigen gene. Journal of Urology 167 1538-1545. (doi:10.1016/S0022-5347(05)65359-1)
51. Tabuchi Y, Takahashi R, Ueda M & Obinata M 2003 Development of a conditionally immortalized testicular Sertoli cell line RTS3-3 from adult transgenic rats harboring temperature-sensitive simian virus 40 large T-antigen gene. Cell Structure and Function 28 87-95. (doi:10.1247/csf.28.87)
52. Tascou S, Nayernia K, Samani A, Schmidtke J, Vogel T, Engel W & Burfeind P 2000 Immortalization of murine male germ cells at a discrete stage of differentiation by a novel directed promoter-based selection strategy. Biology of Reproduction 63 1555-1561. (doi:10.1095/biolreprod63.5.1555)
53. van Pelt AM, Roepers-Gajadien HL, Gademan IS, Creemers LB, de Rooij DG & van Dissel-Emiliani FM 2002 Establishment of cell lines with rat spermatogonial stem cell characteristics. Endocrinology 143 1845-1850. (doi:10.1210/endo.143.5.8806)
54. Walther N, Jansen M, Ergun S, Kascheike B & Ivell R 1996 Sertoli cell lines established from H-2Kb-tsA58 transgenic mice differentially regulate the expression of cell-specific genes. Experimental Cell Research 225 411-421. (doi:10.1006/excr.1996.0192)
55. Wang X, Qin J, Zhao RC & Zenke M 2014 Reduced immunogenicity of induced pluripotent stem cells derived from Sertoli cells. PLoS ONE 9 e106110. (doi:10.1371/journal.pone.0106110)
56. West FD, Roche-Rios MI, Abraham S, Rao RR, Natrajan MS, Bacanamwo M & Stice SL 2010 KIT ligand and bone morphogenetic protein signaling enhances human embryonic stem cell to germ-like cell differentiation. Human Reproduction 25 168-178. (doi:10.1093/humrep/dep338)
57. Wolkowicz MJ, Coonrod SA, Reddi PP, Millan JL, Hofmann MC & Herr JC 1996 Refinement of the differentiated phenotype of the spermatogenic cell line GC-2spd(ts). Biology of Reproduction 55 923-932. (doi:10.1095/biolreprod55.4.923)
58. Wosnitzer M, Goldstein M & Hardy MP 2014 Review of Azoospermia. Spermatogenesis 4 e28218.
59. Wu L, Dong H, Zhao J, Wang Y, Yang Q, Jia C & Ma J 2015 Diosgenin stimulates rat TM4 cell proliferation through activating plasma membrane translocation and transcriptional activity of estrogen receptors. Biology of Reproduction 92 24. (doi:10.1095/biolreprod.114.124206)
60. Yang S, Ping P, Ma M, Li P, Tian R, Yang H, Liu Y, Gong Y, Zhang Z, Li Z et al. 2014a Generation of haploid spermatids with fertilization and development capacity from human spermatogonial stem cells of cryptorchid patients. Stem Cell Reports 3 663-675. (doi:10.1016/j.stemcr.2014.08.004)
61. Yang L, Wang Y, Zhang Q, Lai Y, Li C, Huang W, Duan Y, Jiang Z, Li X, Cai Z et al. 2014b Identification of Hsf1 as a novel androgen receptor-regulated gene in mouse Sertoli cells. Molecular Reproduction and Development 81 514-523. (doi:10.1002/mrd.22318)
62. Yang H, Liu Y, Hai Y, Guo Y, Yang S, Li Z, Gao WQ & He Z 2015 Efficient Conversion of spermatogonial stem cells to phenotypic and functional dopaminergic neurons via the PI3K/Akt and P21/Smurf2/Nolz1 pathway. Molecular Neurobiology 52 1654-1669. (doi:10.1007/s12035-014-8966-4)
63. Yao C, Liu Y, Sun M, Niu M, Yuan Q, Hai Y, Guo Y, Chen Z, Hou J & He Z 2015 MicroRNAs and DNA methylation as epigenetic regulators of mitosis, meiosis and spermiogenesis. Reproduction 150 R25-R34. (doi:10.1530/REP-14-0643)
64. Yao C, Sun M, Yuan Q, Niu M, Chen Z, Hou J, Wang H, Wen L, Liu Y, Li Z et al. 2016 MiRNA-133b promotes the proliferation of human Sertoli cells through targeting GLI3. Oncotarget 7 2201-2219. (doi:10.18632/oncotarget.6876)
65. Zhang Z, Gong Y, Guo Y, Hai Y, Yang H, Yang S, Liu Y, Ma M, Liu L, Li Z et al. 2013 Direct transdifferentiation of spermatogonial stem cells to morphological, phenotypic and functional hepatocyte-like cells via the ERK1/2 and Smad2/3 signaling pathways and the inactivation of cyclin A, cyclin B and cyclin E. Cell Communication and Signaling 11 67. (doi:10.1186/1478-811X-11-67)
66. Zhang L, Chen M, Wen Q, Li Y, Wang Y, Qin Y, Qin Y, Cui X, Yang L, Huff V et al. 2015 Reprogramming of Sertoli cells to fetal-like Leydig cells by Wt1 ablation. PNAS 112 4003-4008. (doi:10.1073/pnas.1422371112)
67. Zhou Q, Wang M, Yuan Y, Wang XP, Fu R, Wan HF, Xie MM, Liu MX, Guo XJ, Zheng Y et al. 2016 Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 18 330-340. (doi:10.1016/j.stem.2016.01.017)