Isolation of enriched carp spermatogonial stem cells from Labeo rohita testis for in vitro propagation

Theriogenology

Volumn 76, Issue 2, 2011, Pages 241-251

  Panda, R P ^a   Barman, H K ^a   Mohapatra, C ^a  

^a CENTRAL INSTITUTE OF FRESHWATER AQUACULTURE   (India)

Author keywords

Labeo rohita; Magnetic activated cell sorting; Rohu; Spermatogenesis; Spermatogonial stem cell; Testis

Indexed keywords

ANIMAL; ANIMAL DISEASE; AQUACULTURE; ARTICLE; CARP; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CLASSIFICATION; CYTOLOGY; DENSITY GRADIENT CENTRIFUGATION; IMMUNOMAGNETIC SEPARATION; MALE; METHODOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATOGONIUM; TESTIS;

ANIMALS; AQUACULTURE; CARPS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; CENTRIFUGATION, DENSITY GRADIENT; IMMUNOMAGNETIC SEPARATION; MALE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPERMATOGONIA; TESTIS;

BOVINAE; CYPRINIDAE; LABEO ROHITA;

EID: 79958847570     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2011.01.031     Document Type: Article

References (45)

1. Schulz R.W., Menting S., Bogerd J., Franca L.R., Vilela D.A., Godinho H.P. Sertoli cell proliferation in the adult testis--evidence from two fish species belonging to different orders. Biol Reprod 2005, 73:891-898.
2. Vilela D.A.R., Silva S.G.B., Peixoto M.T.D., Godinho H.P., Franca L.R. Spermatogenesis in teleost: insights from the nile tilapia (Oreochromis niloticus) model. Fish Physiol Biochem 2003, 28:187-190.
3. Kubota H., Avarbock M.R., Brinster R.L. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci USA 2003, 100:6487-6492.
4. 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, 72:985-991.
5. Shen F., Zhang C., Zheng H., Xiong Y., Wang X., Liao W., et al. Long-term culture and transplantation of spermatogonial stem cells from BALB/c mice. Cells Tissues Organs 2010, 191:372-381.
6. Kanatsu-Shinohara M., Muneto T., Lee J., Takenaka M., Chuma S., Nakatsuji N., et al. Long-term culture of male germline stem cells from hamster testes. Biol Reprod 2008, 78:611-617.
7. 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, 456:344-349.
8. He Z., Kokkinaki M., Jiang J., Dobrinski I., Dym M. Isolation, characterization, and culture of human spermatogonia. Biol Reprod 2010, 82:363-372.
9. Hermann B.P., Sukhwani M., Simorangkir D.R., Chu T., Plant T.M., Orwig K.E. Molecular dissection of the male germ cell lineage identifies putative spermatogonial stem cells in rhesus macaques. Hum Reprod 2009, 24:1704-1716.
10. Muller T., Eildermann K., Dhir R., Schlatt S., Behr R. Glycan stem-cell markers are specifically expressed by spermatogonia in the adult non-human primate testis. Hum Reprod 2008, 23:2292-2298.
11. 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.
12. Rodriguez-Sosa J.R., Dobson H., Hahnel A. Isolation and transplantation of spermatogonia in sheep. Theriogenology 2006, 66:2091-2103.
13. 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.
14. Kurita K., Burgess S.M., Sakai N. Transgenic zebrafish produced by retroviral infection of in vitro-cultured sperm. Proc Natl Acad Sci USA 2004, 101:1263-1267.
15. Sakai N. Transmeiotic differentiation of zebrafish germ cells into functional sperm in culture. Development 2002, 129:3359-3365.
16. Hong Y., Liu T., Zhao H., Xu H., Wang W., Liu R., et al. Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proc Natl Acad Sci U S A 2004, 101:8011-8016.
17. Saiki A., Tamura M., Matsumoto M., Katowgi J., Watanabe A., Onitake K. Establishment of in vitro spermatogenesis from spermatocytes in the medaka, Oryzias latipes. Dev Growth Differ 1997, 39:337-344.
18. Song M., Gutzeit H.O. Primary culture of medaka (Oryzias latipes) testis: a test system for the analysis of cell proliferation and differentiation. Cell Tissue Res 2003, 313:107-115.
19. Song M., Gutzeit H.O. Effect of 17-alpha-ethynylestradiol on germ cell proliferation in organ and primary culture of medaka (Oryzias latipes) testis. Dev Growth Differ 2003, 45:327-337.
20. 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.
21. 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.
22. Loppion G., Crespel A., Martinez A.S., Auvray P., Sourdaine P. Study of the potential spermatogonial stem cell compartment in dogfish testis, Scyliorhinus canicula L. Cell Tissue Res 2008, 332:533-542.
23. Sanchez-Sanchez A.V., Camp E., Garcia-Espana 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.
24. Mohapatra C., Barman H.K., Panda R.P., Sunil K., Das V., Mohanta R., et al. Cloning of cDNA and prediction of peptide structure of Plzf expressed in the spermatogonial cells of Labeo rohita. Marine Genomics 2010, 3:157-163.
25. Gassei K., Ehmcke J., Schlatt S. Efficient enrichment of undifferentiated GFR alpha 1+ spermatogonia from immature rat testis by magnetic activated cell sorting. Cell Tissue Res 2009, 337:177-183.
26. Kossack N., Meneses J., Shefi S., Nguyen H.N., Chavez S., Nicholas C., et al. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells 2009, 27:138-149.
27. Yuan Z., Hou R., Wu J. Generation of mice by transplantation of an adult spermatogonial cell line after cryopreservation. Cell Prolif 2009, 42:123-131.
28. Fishery and Aquaculture Statistics 2009, FAO, FAO.
29. Barman H.K., Barat A., Yadav B.M., Banerjee S., Meher P.K., Reddy P.V.G.K., et al. Genetic variation between four species of Indian major carps as revealed by random amplified polymorphic DNA assay. Aquaculture Research 2003, 217:115-123.
30. Jena J.K. Cultured Aquatic Species Information Programme - Labeo rohita 2006, FAO.
31. Mohamet L., Lea M.L., Ward C.M. Abrogation of E-cadherin-mediated cellular aggregation allows proliferation of pluripotent mouse embryonic stem cells in shake flask bioreactors. PLoS One 2010, 5:e12921.
32. Barman H.K., Takami Y., Ono T., Nishijima H., Sanematsu F., Shibahara K., et al. Histone acetyltransferase 1 is dispensable for replication-coupled chromatin assembly but contributes to recover DNA damages created following replication blockage in vertebrate cells. Biochem Biophys Res Commun 2006, 345:1547-1557.
33. Kubota H., Avarbock M.R., Brinster R.L. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 2004, 71:722-731.
34. Reding S.C., Stepnoski A.L., Cloninger E.W., Oatley J.M. THY1 is a conserved marker of undifferentiated spermatogonia in the pre-pubertal bull testis. Reproduction 2010, 139:893-903.
35. Bashamboo A., Taylor A.H., Samuel K., Panthier J.J., Whetton A.D., Forrester L.M. The survival of differentiating embryonic stem cells is dependent on the SCF-KIT pathway. J Cell Sci 2006, 119:3039-3046.
36. Dash S.N., Routray P., Dash C., Guru B.C., Swain P., Sarangi N. Use of the non-toxic cryoprotectant trehalose enhances recovery and function of fish embryonic stem cells following cryogenic storage. Curr Stem Cell Res Ther 2008, 3:277-287.
37. Filipponi D., Hobbs R.M., Ottolenghi S., Rossi P., Jannini E.A., Pandolfi P.P., et al. Repression of kit expression by Plzf in germ cells. Mol Cell Biol 2007, 27:6770-6781.
38. Scholer H.R., Ruppert S., Suzuki N., Chowdhury K., Gruss P. New type of POU domain in germ line-specific protein Oct-4. Nature 1990, 344:435-439.
39. Solter D., Knowles B.B. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci U S A 1978, 75:5565-5569.
40. Xu H., Gui J., Hong Y. Differential expression of vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp (Carassius auratus gibelio), a bisexually and gynogenetically reproducing vertebrate. Dev Dyn 2005, 233:872-882.
41. Goel S., Fujihara M., Tsuchiya K., Takagi Y., Minami N., Yamada M., et al. Multipotential ability of primitive germ cells from neonatal pig testis cultured in vitro. Reprod Fertil Dev 2009, 21:696-708.
42. Lee Y.M., Jung J.G., Kim J.N., Park T.S., Kim T.M., Shin S.S., et al. A testis-mediated germline chimera production based on transfer of chicken testicular cells directly into heterologous testes. Biol Reprod 2006, 75:380-386.
43. Burgess S., Reim G., Chen W., Hopkins N., Brand M. The zebrafish spiel-ohne-grenzen (spg) gene encodes the POU domain protein Pou2 related to mammalian Oct4 and is essential for formation of the midbrain and hindbrain, and for pre-gastrula morphogenesis. Development 2002, 129:905-916.
44. Lacerda S.M., Batlouni S.R., Costa G.M., Segatelli T.M., Quirino B.R., Queiroz B.M., et al. 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.
45. Nakamura S., Kobayashi K., Nishimura T., Higashijima S., Tanaka M. Identification of germline stem cells in the ovary of the teleost medaka. Science 2010, 328:1561-1563.