Phenotypic characterization and in vitro propagation and transplantation of the Nile tilapia (Oreochromis niloticus) spermatogonial stem cells

General and Comparative Endocrinology

Volumn 192, Issue , 2013, Pages 95-106

  Santos Nassif Lacerda, Samyra Maria ^a   Costa, Guilherme Mattos Jardim ^a   Da Silva, Mariana de Araújo ^a   Almeida Campos Junior, Paulo Henrique ^a   Segatelli, Tânia Mara ^a   Peixoto, Marco Túlio Diniz ^a   Resende, Rodrigo Ribeiro ^a   De França, Luiz Renato ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Gfra1; Nanos2; Nile tilapia (Oreochromis niloticus); Spermatogonial stem cells; Spermatogonial transplantation; Stem cell markers

Indexed keywords

DDX4 HELICASE; FISH PROTEIN; MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN GFRA1; PROTEIN NANOS2; RNA HELICASE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AQUACULTURE; ARTICLE; CELL ADHESION; CELL INTERACTION; CELL TRANSFORMATION; CELL VIABILITY; CONTROLLED STUDY; DMC1 GENE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC MANIPULATION; GENETIC SIMILARITY; GFRA1 GENE; IN VITRO PROPAGATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OREOCHROMIS NILOTICUS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SOX2 GENE; SPECIES CULTIVATION; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL EXPANSION; STEM CELL TRANSPLANTATION; TRANSGENIC ANIMAL; VASA GENE;

GFRA1; NANOS2; NILE TILAPIA (OREOCHROMIS NILOTICUS); SPERMATOGONIAL STEM CELLS; SPERMATOGONIAL TRANSPLANTATION; STEM CELL MARKERS;

ANIMALS; CICHLIDS; FISH PROTEINS; MALE; SPERMATOGONIA; STEM CELL TRANSPLANTATION; STEM CELLS; TESTIS;

EID: 84884413948     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.06.013     Document Type: Article

References (84)

1. Aoki Y., Nakamura S., Ishikawa Y., Tanaka M. Expression and syntenic analyses of four nanos genes in medaka. Zool. Sci. 2009, 26:112-118.
2. Aponte P.M., Soda T., Teerds K.J., Mizrak S.C., van de Kant H.J., de Rooij D.G. Propagation of bovine spermatogonial stem cells in vitro. Reproduction 2008, 136:543-557.
3. Baloh R.H., Enomoto H., Johnson E.M., Milbrandt J. The GDNF family ligands and receptors - implications for neural development. Curr. Opin. Neurobiol. 2000, 10:103-110.
4. Barrios F., Filipponi D., Pellegrini M., Paronetto M.P., Di Siena S., Geremia R., Rossi P., De Felici M., Jannini E.A., Dolci S. Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J. Cell Sci. 2010, 123:871-880.
5. Beer R.L., Draper B.W. Nanos3 maintains germline stem cells and expression of the conserved germline stem cell gene nanos2 in the zebrafish ovary. Dev. Biol. 2012, 374:308-318.
6. Buageaw A., Sukhwani M., Ben-Yehudah A., Ehmcke J., Rawe V.Y., Pholpramool C., Orwig K.E., Schlatt S. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol. Reprod. 2005, 73:1011-1016.
7. Campos-Junior P.H., Costa G.M., Lacerda S.M., Rezende-Neto J.V., de Paula A.M., Hofmann M.C., de França L.R. The spermatogonial stem cell niche in the collared peccary (Tayassu tajacu). Biol. Reprod. 2012, 86:1-10.
8. Cnaani A., Lee B.Y., Ozouf-Costaz C., Bonillo C., Baroiller J.F., D'Cotta H., Kocher T. Mapping of sox2 and sox14 in tilapia (Oreochromis spp.). Sex Dev. 2007, 1:207-210.
9. Conrad S., Renninger M., Hennenlotter J., Wiesner T., Just L., Bonin M., Aicher W., Bühring H.J., Mattheus U., Mack A., Wagner H.J., Minger S., Matzkies M., Reppel M., Hescheler J., Sievert K.D., Stenzl A., Skutella T. Generation of pluripotent stem cells from adult human testis. Nature 2008, 456:344-349.
10. Costa G.M., Avelar G.F., Rezende-Neto J.V., Campos-Junior P.H., Lacerda S.M., Andrade B.S., Thomé R.G., Hofmann M.C., Franca L.R. Spermatogonial stem cell markers and niche in equids. PLoS One 2012, 7:e44091.
11. de Rooij D.G., Russell L.D. All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 2000, 21:776-798.
12. Dettin L., Ravindranath N., Hofmann M.C., Dym M. Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. Biol. Reprod. 2003, 69:1565-1571.
13. Draper B.W., McCallum C.M., Moens C.B. Nanos1 is required to maintain oocyte production in adult zebrafish. Dev. Biol. 2007, 305:589-598.
14. Froschauer A., Khatun M.M., Sprott D., Franz A., Rieger C., Pfennig F., Gutzeit H.O. Oct4-EGFP reporter gene expression marks the stem cells in embryonic development and in adult gonads of transgenic medaka. Mol. Reprod. Dev. 2013, 80:48-58.
15. Fujimura K., Conte M.A., Kocher T.D. Circular DNA intermediate in the duplication of Nile tilapia vasa genes. PLoS One 2011, 6:e29477.
16. Gassei K., Ehmcke J., Schlatt S. Efficient enrichment of undifferentiated GFRalpha1+ spermatogonia from immature rat testis by magnetic activated cell sorting. Cell Tissue Res. 2009, 337:177-183.
17. Gassei K., Ehmcke J., Dhir R., Schlatt S. Magnetic activated cell sorting allows isolation of spermatogonia from adult primate testes and reveals distinct GFRa1-positive subpopulations in men. J. Med. Primatol. 2010, 39:83-91.
18. Grisanti L., Falciatori I., Grasso M., Dovere L., Fera S., Muciaccia B., Fuso A., Berno V., Boitani C., Stefanini M., Vicini E. Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells 2009, 27:3043-3052.
19. Gustafson E.A., Wessel G.M. Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 2010, 32:626-637.
20. Hayashi M., Sato M., Iwasaki Y., Terasawa M., Tashiro M., Yokoyama S., Katayama N., Sadaie S., Miwa M., Yoshizaki G. Combining next-generation sequencing with microarray for transcriptome analysis in rainbow trout gonads. Mol. Reprod. Dev. 2012, 79:870-878.
21. He Z., Kokkinaki M., Jiang J., Dobrinski I., Dym M. Isolation, characterization, and culture of human spermatogonia. Biol. Reprod. 2010, 82:363-372.
22. He Z., Kokkinaki M., Jiang J., Zeng W., Dobrinski I., Dym M. Isolation of human male germ-line stem cells using enzymatic digestion and magnetic-activated cell sorting. Methods Mol. Biol. 2012, 825:45-57.
23. Hermann B.P., Sukhwani M., Hansel M.C., Orwig K.E. Spermatogonial stem cells in higher primates: are there differences from those in rodents?. Reproduction 2010, 139:479-493.
24. Hofmann M.C. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol. Cell Endocrinol. 2008, 288:95-103.
25. Hofmann M.C., Braydich-Stolle L., Dym M. Isolation of male germ-line stem cells; influence of GDNF. Dev. Biol. 2005, 279:114-124.
26. Honaramooz, A., Yang, Y., 2010. Recent advances in application of male germ cell transplantation in farm animals. Vet. Med. Int. Pii 657860.
27. Hong Y., Liu T., Zhao H., Xu H., Wang W., Liu R., Chen T., Deng J., Gui J. Establishment of a normal medaka fish spermatogonial cell line capable of sperm production in vitro. Proc. Natl. Acad. Sci. USA 2004, 101:8011-8016.
28. Hong Y., Winkler C., Schartl M. Pluripotency and differentiation of embryonic stem cell lines from the medaka fish (Oryzias latipes). Mech. Dev. 1996, 60:33-44.
29. Hong Y., Schartl M. Isolation and differentiation of medaka embryonic stem cells. Embryonic Stem Cell Protocols. Methods in Molecular Biology 1996, 5-16. Humana Press Inc, New Jersey. K. Turksen (Ed.).
30. Izadyar F., Spierenberg G.T., Creemers L.B., den Ouden K., de Rooij D.G. Isolation and purification of type A spermatogonia from the bovine testis. Reproduction 2002, 124:85-94.
31. Jaruzelska J., Kotecki M., Kusz K., Spik A., Firpo M., Reijo Pera R.A. Conservation of a Pumilio-Nanos complex from Drosophila germ plasm to human germ cells. Dev. Genes Evol. 2003, 213:120-126.
32. Jijiwa M., Kawai K., Fukihara J., Nakamura A., Hasegawa M., Suzuki C., Sato T., Enomoto A., Asai N., Murakumo Y., Takahashi M. GDNF-mediated signaling via RET tyrosine 1062 is essential for maintenance of spermatogonial stem cells. Genes Cells 2008, 13:365-374.
33. Jing S., Wen D., Yu Y., Holst P.L., Luo Y., Fang M., Tamir R., Antonio L., Hu Z., Cupples R., Louis J.C., Hu S., Altrock B.W., Fox G.M. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell 1996, 85:1113-1124.
34. Kajiura-Kobayashi H., Kobayashi T., Nagahama Y. Cloning of cDNAs and the differential expression of A-type cyclins and Dmc1 during spermatogenesis in the Japanese eel, a teleost fish. Dev. Dyn. 2005, 232:1115-1123.
35. Kala S., Kaushik R., Singh K.P., Kadam P.H., Singh M.K., Manik R.S., Singla S.K., Palta P., Chauhan M.S. In vitro culture and morphological characterization of prepubertal buffalo (Bubalus bubalis) putative spermatogonial stem cell. J. Assist. Reprod. Genet. 2012, 29:1335-1342.
36. Kawasaki T., Saito K., Sakai C., Shinya M., Sakai N. Production of zebrafish offspring from cultured spermatogonial stem cells. Genes Cells 2012, 17:316-325.
37. Kobayashi T., Kajiura-Kobayashi H., Nagahama Y. A novel stage-specific antigen is expressed only in early stages of spermatogonia in Japanese eel, Anguilla japonica testis. Mol. Reprod. Dev. 1998, 51:355-361.
38. Kobayashi T., Kajiura-Kobayashi H., Nagahama Y. Two isoforms of vasa homologs in a teleost fish: their differential expression during germ cell differentiation. Mech. Dev. 2002, 111:167-171.
39. Kolasa A., Misiakiewicz K., Marchlewicz M., Wiszniewska B. The generation of spermatogonial stem cells and spermatogonia in mammals. Reprod. Biol. 2012, 12:5-23.
40. Kuijk E.W., Colenbrander B., Roelen B.A. The effects of growth factors on in vitro-cultured porcine testicular cells. Reproduction 2009, 138:721-731.
41. Lacerda S.M., Aponte P.M., Costa G.M., Campos-Junior P.H., Segatelli T.M., Silva M.A., França L.R. An overview of spermatogonial stem cell physiology, niche and transplantation in fish. Anim. Reprod. 2012, 9:798-808.
42. Lacerda S.M., Batlouni S.R., Costa G.M., Segatelli T.M., Quirino B.R., Queiroz B.M., Kalapothakis E., França L.R. A new and fast technique to generate offspring after germ cells transplantation in adult fish: the Nile tilapia (Oreochromis niloticus) model. PLoS One 2010, 5:e10740.
43. Lacerda S.M., Batlouni S.R., Silva S.B., Homem C.S., França L.R. Germ cells transplantation in fish: the Nile-tilapia model. Anim. Reprod. 2006, 3:146-159.
44. Lacerda S.M., Costa G.M., Campos-Junior P.H., Segatelli T.M., Yazawa R., Takeuchi Y., Morita T., Yoshizaki G., França L.R. Germ cell transplantation as a potential biotechnological approach to fish reproduction. Fish Physiol. Biochem. 2013, 39:3-11.
45. Leal M.C., Cardoso E.R., Nóbrega R.H., Batlouni S.R., Bogerd J., França L.R., Schulz R.W. Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol. Reprod. 2009, 81:177-187.
46. Lok D., Weenk D., De Rooij D.G. Morphology, proliferation, and differentiation of undifferentiated spermatogonia in the Chinese hamster and the ram. Anat. Rec. 1982, 203:83-99.
47. Mirzapour T., Movahedin M., Tengku Ibrahim T.A., Koruji M., Haron A.W., Nowroozi M.R., Rafieian S.H. 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.
48. Mochizuki K., Sano H., Kobayashi S., Nishimiya-Fujisawa C., Fujisawa T. Expression and evolutionary conservation of nanos-related genes in Hydra. Dev. Genes Evol. 2000, 210:591-602.
49. Nagano M.C., Yeh J.R. The identity and fate decision control of spermatogonial stem cells: where is the point of no return?. Curr. Top. Dev. Biol. 2013, 102:61-95.
50. Nagasawa K., Miwa M., Yazawa R., Morita T., Takeuchi Y., Yoshizaki G. Characterization of lymphocyte antigen 75 (Ly75/CD205) as a potential cell-surface marker on spermatogonia in Pacific bluefin tuna Thunnus orientalis. Fish Sci. 2012, 78:791-800.
51. Nagasawa K., Shikina S., Takeuchi Y., Yoshizaki G. Lymphocyte antigen 75 (Ly75/CD205) is a surface marker on mitotic germ cells in rainbow trout. Biol. Reprod. 2010, 83:597-606.
52. Nakagawa T., Sharma M., Nabeshima Y., Braun R.E., Yoshida S. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 2010, 328:62-67.
53. Naughton C.K., Jain S., Strickland A.M., Gupta A., Milbrandt J. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol. Reprod. 2006, 74:314-321.
54. Nóbrega R.H., Greebe C.D., van de Kant H., Bogerd J., de França L.R., Schulz R.W. Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PLoS One 2010, 5:e12808.
55. Oatley J.M., Brinster R.L. The germline stem cell niche unit in mammalian testes. Physiol. Rev. 2012, 92:577-595.
56. Oatley M.J., Kaucher A.V., Racicot K.E., Oatley J.M. Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol. Reprod. 2011, 85:347-356.
57. Okutsu T., Suzuki K., Takeuchi Y., Takeuchi T., Yoshizaki G. Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc. Natl. Acad. Sci. USA 2006, 103:2725-2729.
58. Onichtchouk D. Pou5f1/oct4 in pluripotency control: insights from zebrafish. Genesis 2012, 50:75-85.
59. Ozaki Y., Saito K., Shinya M., Kawasaki T., Sakai N. Evaluation of Sycp3, Plzf and Cyclin B3 expression and suitability as spermatogonia and spermatocyte markers in zebrafish. Gene Expr. Patterns 2011, 11:309-315.
60. Pfennig F., Kurth T., Meissner S., Standke A., Hoppe M., Zieschang F., Reitmayer C., Göbel A., Kretzschmar G., Gutzeit H.O. The social status of the male Nile tilapia (Oreochromis niloticus) influences testis structure and gene expression. Reproduction 2012, 143:71-84.
61. Phillips B.T., Gassei K., Orwig K.E. Spermatogonial stem cell regulation and spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365:1663-1678.
62. Powell R.H., Biancardi M.N., Galiguis J., Qin Q., Pope C.E., Leibo S.P., Wang G., Gómez M.C. 286 expression of pluripotent stem cell markers in domestic cat spermatogonial cells. Reprod. Fertil. Dev. 2012, 25:290-291.
63. Sada A., Hasegawa K., Pin P.H., Saga Y. NANOS2 acts downstream of glial cell line-derived neurotrophic factor signaling to suppress differentiation of spermatogonial stem cells. Stem Cells 2012, 30:280-291.
64. Sada A., Suzuki A., Suzuki H., Saga Y. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 2009, 325:1394-1398.
65. Sánchez-Sánchez A.V., Camp E., García-España A., Leal-Tassias A., Mullor J.L. Medaka Oct4 is expressed during early embryo development, and in primordial germ cells and adult gonads. Dev. Dyn. 2010, 239:672-679.
66. Sato T., Aiyama Y., Ishii-Inagaki M., Hara K., Tsunekawa N., Harikae K., Uemura-Kamata M., Shinomura M., Zhu X.B., Maeda S., Kuwahara-Otani S., Kudo A., Kawakami H., Kanai-Azuma M., Fujiwara M., Miyamae Y., Yoshida S., Seki M., Kurohmaru M., Kanai Y. Cyclical and patch-like GDNF distribution along the basal surface of Sertoli cells in mouse and hamster testes. PLoS One 2011, 6:e28367.
67. Schulz R.W., de França L.R., Lareyre J.J., Le Gac F., Chiarini-Garcia H., Nobrega R.H., Miura T. Spermatogenesis in fish. Gen. Comp. Endocrinol. 2010, 165:390-411.
68. Shikina S., Yoshizaki G. Improved in vitro culture conditions to enhance the survival, mitotic activity, and transplantability of rainbow trout type a spermatogonia. Biol. Reprod. 2010, 83:268-276.
69. Shikina S., Ihara S., Yoshizaki G. Culture conditions for maintaining the survival and mitotic activity of rainbow trout transplantable type A spermatogonia. Mol. Reprod. Dev. 2008, 75:529-537.
70. Silva R.C., Costa G.M., Lacerda S.M., Batlouni S.R., Soares J.M., Avelar G.F., Böttger K.B., Silva S.F., Nogueira M.S., Andrade L.M., França L.R. Germ cell transplantation in felids: a potential approach to preserving endangered species. J. Androl. 2012, 33:264-276.
71. Suzuki H., Sada A., Yoshida S., Saga Y. 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. 2009, 336:222-231.
72. Takehashi M., Tada M., Kanatsu-Shinohara M., Morimoto H., Kazuki Y., Oshimura M., Tada T., Shinohara T. Hybridization of testis-derived stem cells with somatic cells and embryonic stem cells in mice. Biol. Reprod. 2012, 86:178. 10.1095/biolreprod.112.098988.
73. Takeuchi Y., Yoshizaki G., Takeuchi T. Biotechnology: surrogate broodstock produces salmonids. Nature 2004, 430:629-630.
74. Tang L., Rodriguez-Sosa J.R., Dobrinski I. Germ cell transplantation and testis tissue xenografting in mice. J. Vis. Exp. 2012, 6(60). pii: 3545. 10.3791/3545.
75. Thoma E.C., Wagner T.U., Weber I.P., Herpin A., Fischer A., Schartl M. Ectopic expression of single transcription factors directs differentiation of a medaka spermatogonial cell line. Stem Cells Dev. 2011, 20:1425-1438.
76. Tokuda M., Kadokawa Y., Kurahashi H., Marunouchi T. CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biol. Reprod. 2007, 76:130-141.
77. van der Wee K.S., Johnson E.W., Dirami G., Dym T.M., Hofmann M.C. Immunomagnetic isolation and long-term culture of mouse type A spermatogonia. J. Androl. 2001, 22:696-704.
78. von Schonfeldt V., Wistuba J., Schlatt S. Notch-1, c-kit and GFRalpha-1 are developmentally regulated markers for premeiotic germ cells. Cytogenet. Genome Res. 2004, 105:235-239.
79. Wang D., Manali D., Wang T., Bhat N., Hong N., Li Z., Wang L., Yan Y., Liu R., Hong Y. Identification of pluripotency genes in the fish medaka. Int. J. Biol. Sci. 2011, 7:440-451.
80. Wang Z., Lin H. Nanos maintains germline stem cell self-renewal by preventing differentiation. Science 2004, 303:2016-2019.
81. Westerfield, M., 1995. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), third ed. Eugene, OR.
82. Yano A., von Schalburg K., Cooper G., Koop B.F., Yoshizaki G. Identification of a molecular marker for type A spermatogonia by microarray analysis using gonadal cells from pvasa-GFP transgenic rainbow trout (Oncorhynchus mykiss). Mol. Reprod. Dev. 2009, 76:246-254.
83. Yoshida S., Sukeno M., Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007, 317:1722-1726.
84. Yoshizaki G., Okutsu T., Morita T., Terasawa M., Yazawa R., Takeuchi Y. Biological characteristics of fish germ cells and their application to developmental biotechnology. Reprod. Domest. Anim. 2012, 47:187-192.