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Medaka fish stem cells and their applications

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Abstract

Stem cells are present in developing embryos and adult tissues of multicellular organisms. Owing to their unique features, stem cells provide excellent opportunities for experimental analyses of basic developmental processes such as pluripotency control and cell fate decision and for regenerative medicine by stem cell-based therapy. Stem cell cultures have been best studied in 3 vertebrate organisms. These are the mouse, human and a small laboratory fish called medaka. Specifically, medaka has given rise to the first embryonic stem (ES) cells besides the mouse, the first adult testis-derived male stem cells spermatogonia capable of test-tube sperm production, and most recently, even haploid ES cells capable of producing Holly, a semi-cloned fertile female medaka from a mosaic oocyte created by microinjecting a haploid ES cell nucleus directly into a normal oocyte. These breakthroughs make medaka a favoring vertebrate model for stem cell research, the topic of this review.

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References

  1. Evans M J, Kaufman M H. Establishment in culture of pluripotential cells from mouse embryos. Nature, 1981, 292: 154–156 10.1038/292154a0, 1:STN:280:DyaL3M3itV2qsg%3D%3D, 7242681

    Article  PubMed  CAS  Google Scholar 

  2. Martin G R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA, 1981, 78: 7634–7638 10.1073/pnas.78.12.7634, 1:STN:280:DyaL387ltV2htg%3D%3D, 6950406

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  3. Thomson J A, Itskovitz-Eldor J, Shapiro S S, et al. Embryonic stem cell lines derived from human blastocysts. Science, 1998, 282: 1145–1147 10.1126/science.282.5391.1145, 1:CAS:528:DyaK1cXntleisLg%3D, 9804556

    Article  PubMed  CAS  Google Scholar 

  4. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 2006, 126: 663–676 10.1016/j.cell.2006.07.024, 1:CAS:528:DC%2BD28Xpt1aktbs%3D, 16904174

    Article  PubMed  CAS  Google Scholar 

  5. Yu J, Vodyanik M A, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science, 2007, 318: 1917–1920 10.1126/science.1151526, 1:CAS:528:DC%2BD2sXhsVGjsLbN, 18029452

    Article  PubMed  CAS  Google Scholar 

  6. Chen L, Liu L. Current progress and prospects of induced pluripotent stem cells. Sci China C Life Sci, 2009, 52: 622–636 10.1007/s11427-009-0092-6, 19641867

    Article  PubMed  Google Scholar 

  7. Bejar J, Hong Y, Alvarez M C. An ES-like cell line from the marine fish Sparus aurata: characterization and chimaera production. Transgenic Res, 2002, 11: 279–289 10.1023/A:1015678416921, 1:CAS:528:DC%2BD38XksVSntb0%3D, 12113460

    Article  PubMed  CAS  Google Scholar 

  8. Chen S, Ye H, Sha Q, et al. Derivation of a pluripotent embryonic cell line from red sea bream blastulas. J Fish Biol, 2003, 63: 795–805 10.1046/j.1095-8649.2003.00192.x

    Article  Google Scholar 

  9. Chen S, Sha Z, Ye H Q, et al. Pluripotency and chimera competence of an embryonic stem cell line from the sea perch (Lateolabrax japonicus). Mar Biotechnol, 2007, 9: 82–91 10.1007/s10126-006-6050-1, 1:CAS:528:DC%2BD2sXitlCrsb8%3D, 17136469

    Article  PubMed  CAS  Google Scholar 

  10. Parameswaran V, Shukla R, Bhonde R, et al. Development of a pluripotent ES-like cell line from Asian sea bass (Lates calcarifer)—an oviparous stem cell line mimicking viviparous ES cells. Mar Biotechnol, 2007, 9: 766–775 10.1007/s10126-007-9028-y, 1:CAS:528:DC%2BD2sXhtlyitLnE, 17704967

    Article  PubMed  CAS  Google Scholar 

  11. Wakamatsu Y, Ozato K, Sasado T. Establishment of a pluripotent cell line derived from a medaka (Oryzias latipes) blastula embryo. Mol Mar Biol Biotechnol, 1994, 3: 185–191 1:CAS:528:DyaK2MXit1yrsrk%3D, 8000476

    PubMed  CAS  Google Scholar 

  12. Nichols J, Evans E P, Smith A G. Establishment of germ-line-competent embryonic stem (ES) cells using differentiation inhibiting activity. Development, 1990, 110: 1341–1348 1:STN:280:DyaK3MzgtFSmug%3D%3D, 2129226

    PubMed  CAS  Google Scholar 

  13. Hong Y, Schartl M. Establishment and growth responses of early medakafish (Oryzias latipes) embryonic cells in feeder layer-free cultures. Mol Mar Biol Biotechnol, 1996, 5: 93–104 1:CAS:528:DyaK28XjtlOntLo%3D

    CAS  Google Scholar 

  14. Hong Y, Winkler C, Schartl M. Pluripotency and differentiation of embryonic stem cell lines from the medakafish (Oryzias latipes). Mech Dev, 1996, 60: 33–44 10.1016/S0925-4773(96)00596-5, 1:CAS:528:DyaK28Xnt1Oitrc%3D, 9025059

    Article  PubMed  CAS  Google Scholar 

  15. Hong Y, Winkler C, Schartl M. Efficiency of cell culture derivation from blastula embryos and of chimera formation in the medaka (Oryzias latipes) depends on donor genotype and passage number. Dev Genes Evol, 1998, 208: 595–602 10.1007/s004270050220, 1:STN:280:DyaK1M%2FjtVOnsg%3D%3D, 9811979

    Article  PubMed  CAS  Google Scholar 

  16. Wakamatsu Y, Ozato K, Hashimoto H, et al. Generation of germ-line chimeras in medaka (Oryzias latipes). Mol Mar Biol Biotechnol, 1993, 2: 325–332

    Google Scholar 

  17. Hong Y, Gui J, Chen S, et al. Embryonic stem cells in fish. Acta Zool Sin, 2003, 49: 281–294

    Google Scholar 

  18. Hong Y, Chen S, Gui J, et al. Retention of the developmental pluripotency in medaka embryonic stem cells after gene transfer and long-term drug selection for gene targeting in fish. Transgenic Res, 2004, 13: 41–50 10.1023/B:TRAG.0000017172.71391.fa, 1:CAS:528:DC%2BD2cXhsVOrt78%3D, 15070074

    Article  PubMed  CAS  Google Scholar 

  19. Hong Y, Winkler C, Schartl M. Production of medakafish chimeras from a stable embryonic stem cell line. Proc Natl Acad Sci USA, 1998, 95: 3679–3684 10.1073/pnas.95.7.3679, 1:CAS:528:DyaK1cXitlKjtr0%3D, 9520425

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. Iwamatsu T. Stages of normal development in the medaka Oryzias latipes. Mech Dev, 2004, 121: 605–618 10.1016/j.mod.2004.03.012, 1:CAS:528:DC%2BD2cXltVKns7Y%3D, 15210170

    Article  PubMed  CAS  Google Scholar 

  21. Schwartzberg P L, Goff S P, Robertson E J. Germ-line transmission of a c-abl mutation produced by targeted gene disruption in ES cells. Science, 1989, 246: 799–803 10.1126/science.2554496, 1:STN:280:DyaK3c%2FkvFajsw%3D%3D, 2554496

    Article  PubMed  CAS  Google Scholar 

  22. Ledermann B, Burki K. Establishment of a germ-line competent C57BL/6 embryonic stem cell line. Exp Cell Res, 1991, 197: 254–258 10.1016/0014-4827(91)90430-3, 1:STN:280:DyaK38%2FntVeqtQ%3D%3D, 1959560

    Article  PubMed  CAS  Google Scholar 

  23. Hong N, Li M, Zeng Z, et al. Accessibility of host cell lineages to medaka stem cells depends on genetic background and irradiation of recipient embryos. Cell Mol Life Sci, 2010, 67: 1189–1202 10.1007/s00018-009-0247-4, 1:CAS:528:DC%2BC3cXivFaktbw%3D, 20238480

    Article  PubMed  CAS  Google Scholar 

  24. Raz E. Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet, 2003, 4: 690–700 10.1038/nrg1154, 1:CAS:528:DC%2BD3sXmvVWlsrk%3D, 12951570

    Article  PubMed  CAS  Google Scholar 

  25. Yoon C, Kawakami K, Hopkins N. Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development, 1997, 124: 3157–3165 1:CAS:528:DyaK2sXlvVehs7Y%3D, 9272956

    PubMed  CAS  Google Scholar 

  26. Shinomiya A, Tanaka M, Kobayashi T, et al. The vasa-like gene, olvas, identifies the migration path of primordial germ cells during embryonic body formation stage in the medaka, Oryzias latipes. Dev Growth Differ, 2000, 42: 317–326 10.1046/j.1440-169x.2000.00521.x, 1:CAS:528:DC%2BD3cXmvVegsLw%3D, 10969731

    Article  PubMed  CAS  Google Scholar 

  27. Xu H, Li M, Gui J, et al. Fish germ cells. Sci China Life Sci, 2010, 53: 435–446 20596909

    Article  PubMed  Google Scholar 

  28. Herpin A, Rohr S, Riedel D, et al. Specification of primordial germ cells in medaka (Oryzias latipes). BMC Dev Biol, 2007, 7: 3 10.1186/1471-213X-7-3, 17217535, 1:CAS:528:DC%2BD2sXhvFCgtbo%3D

    Article  PubMed  PubMed Central  Google Scholar 

  29. Nagano M, Brinster C J, Orwig K E, et al. Transgenic mice produced by retroviral transduction of male germ-line stem cells. Proc Natl Acad Sci USA, 2001, 98: 13090–13095 10.1073/pnas.231473498, 1:CAS:528:DC%2BD3MXosFygsLs%3D, 11606778

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Hofmann M C, Hess R A, Goldberg E, et al. Immortalized germ cells undergo meiosis in vitro. Proc Natl Acad Sci USA, 1994, 91: 5533–5537 10.1073/pnas.91.12.5533, 1:STN:280:DyaK2c3mtFKhsg%3D%3D, 8202522

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Wolkowicz M J, Coonrod S A, Reddi P P, et al. Refinement of the differentiated phenotype of the spermatogenic cell line GC-2spd(ts). Biol Reprod, 1996, 55: 923–932 10.1095/biolreprod55.4.923, 1:CAS:528:DyaK28Xls1Grsro%3D, 8879510

    Article  PubMed  CAS  Google Scholar 

  32. Feng L, Chen Y, Dettin L, et al. Generation and in vitro differentiation of a spermatogonial cell line. Science, 2002, 297: 392–395 10.1126/science.1073162, 1:CAS:528:DC%2BD38Xls1CisLo%3D, 12077424

    Article  PubMed  CAS  Google Scholar 

  33. Kanatsu-Shinohara M, Muneto T, Lee J, et al. Long-term culture of male germline stem cells from hamster testes. Biol Reprod, 2008, 78: 611–617 10.1095/biolreprod.107.065615, 1:CAS:528:DC%2BD1cXjvVaitbg%3D, 18094355

    Article  PubMed  CAS  Google Scholar 

  34. Miura T, Yamauchi K, Takahashi H, et al. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proc Natl Acad Sci USA, 1991, 88: 5774–5778 10.1073/pnas.88.13.5774, 1:CAS:528:DyaK3MXltFWjs7Y%3D, 2062857

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. Saiki A, Tamura M, Matsumoto M, et al. Establishment of in vitro spermatogenesis from spermatocytes in the medaka, Oryzias latipes. Dev Growth Differ, 1997, 39: 337–344 10.1046/j.1440-169X.1997.t01-2-00009.x, 1:STN:280:DyaK2szntFKrtA%3D%3D, 9227900

    Article  PubMed  CAS  Google Scholar 

  36. Sakai N. Transmeiotic differentiation of zebrafish germ cells into functional sperm in culture. Development, 2002, 129: 3359–3365 1:CAS:528:DC%2BD38XmtFars7c%3D, 12091306

    PubMed  CAS  Google Scholar 

  37. Hong Y, Liu T, Zhao H, et al. Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proc Natl Acad Sci USA, 2004, 101: 8011–8016 10.1073/pnas.0308668101, 1:CAS:528:DC%2BD2cXkslCisb8%3D, 15141090

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  38. Guan K, Nayernia K, Maier L S, et al. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature, 2006, 440: 1199–1203 10.1038/nature04697, 1:CAS:528:DC%2BD28XjvVGltbw%3D, 16565704

    Article  PubMed  CAS  Google Scholar 

  39. Li M, Hong N, Xu H, et al. Medaka vasa is required for migration but not survival of primordial germ cells. Mech Dev, 2009, 126: 366–381 10.1016/j.mod.2009.02.004, 1:CAS:528:DC%2BD1MXlslWqu7o%3D, 19249358

    Article  PubMed  CAS  Google Scholar 

  40. Liu L, Hong N, Xu H, et al. Medaka dead end encodes a cytoplasmic protein and identifies embryonic and adult germ cells. Gene Expr Patterns, 2009, 9: 541–548 10.1016/j.gep.2009.06.008, 1:CAS:528:DC%2BD1MXhtFGqs7nI, 19577665

    Article  PubMed  CAS  Google Scholar 

  41. Xu H, Li Z, Li M, et al. Boule is present in fish and bisexually expressed in adult and embryonic germ cells of medaka. PLoS One, 2009, 4: e6097. doi: 10.1371/journal.pone.0006097 10.1371/journal.pone.0006097, 19564913, 1:CAS:528:DC%2BD1MXot1SnsL8%3D

    Article  PubMed  PubMed Central  Google Scholar 

  42. Xu H, Li M, Gui J, et al. Cloning and expression of medaka dazl during embryogenesis and gametogenesis. Gene Expr Patterns, 2007, 7: 332–338 10.1016/j.modgep.2006.08.001, 1:CAS:528:DC%2BD28Xht12ksbvK, 16979959

    Article  PubMed  CAS  Google Scholar 

  43. Sette C, Dolci S, Geremia R, et al. The role of stem cell factor and of alternative c-kit gene products in the establishment, maintenance and function of germ cells. Int J Dev Biol, 2000, 44: 599–608 1:CAS:528:DC%2BD3cXotlyrtb4%3D, 11061423

    PubMed  CAS  Google Scholar 

  44. Yan Y, Du J, Chen T, et al. Establishment of medakafish as a model for stem cell-based gene therapy: Efficient gene delivery and potential chromosomal integration by baculoviral vectors. Exp Cell Res, 2009, 315: 2322–2331 10.1016/j.yexcr.2009.04.015, 1:CAS:528:DC%2BD1MXnt1yiurY%3D, 19406120

    Article  PubMed  CAS  Google Scholar 

  45. Muller U. Ten years of gene targeting: Targeted mouse mutants, from vector design to phenotype analysis. Mech Dev, 1999, 82: 3–21 10.1016/S0925-4773(99)00021-0, 1:CAS:528:DyaK1MXisFCku7w%3D, 10354467

    Article  PubMed  CAS  Google Scholar 

  46. Thomas K R, Capecchi M R. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell, 1987, 51: 503–512 10.1016/0092-8674(87)90646-5, 1:CAS:528:DyaL1cXhsFGg, 2822260

    Article  PubMed  CAS  Google Scholar 

  47. Kanatsu-Shinohara M, Ikawa M, Takehashi M, et al. Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells. Proc Natl Acad Sci USA, 2006, 103: 8018–8023 10.1073/pnas.0601139103, 1:CAS:528:DC%2BD28Xlt1ChsbY%3D, 16679411

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  48. Takehashi M, Kanatsu-Shinohara M, Miki H, et al. Production of knockout mice by gene targeting in multipotent germline stem cells. Dev Biol, 2007, 312: 344–352 10.1016/j.ydbio.2007.09.029, 1:CAS:528:DC%2BD2sXhtlyks7bI, 17959167

    Article  PubMed  CAS  Google Scholar 

  49. Chen S, Hong Y, Schartl M. Cloning, structural analysis and construction of homologous recombination vector of p53 gene in medaka fish (Oryzias latipes). Acta Zool Sin, 2002, 48: 519–526 1:CAS:528:DC%2BD2cXitlGntLY%3D

    CAS  Google Scholar 

  50. Hong Y, Winkler C, Liu T, et al. Activation of the mouse Oct4 promoter in medaka embryonic stem cells and its use for ablation of spontaneous differentiation. Mech Dev, 2004, 121: 933–943 10.1016/j.mod.2004.03.028, 1:CAS:528:DC%2BD2cXltVKntrs%3D, 15210197

    Article  PubMed  CAS  Google Scholar 

  51. Chen S, Hong Y, Scherer S J, et al. Lack of ultraviolet-light inducibility of the medakafish (Oryzias latipes) tumor suppressor gene p53. Gene, 2001, 264: 197–203 10.1016/S0378-1119(01)00340-7, 1:CAS:528:DC%2BD3MXhsleksrY%3D, 11250074

    Article  PubMed  CAS  Google Scholar 

  52. Bejar J, Hong Y, Schartl M. Mitf expression is sufficient to direct differentiation of medaka blastula derived stem cells to melanocytes. Development, 2003, 130: 6545–6553 10.1242/dev.00872, 1:CAS:528:DC%2BD2cXitlCitw%3D%3D, 14660543

    Article  PubMed  CAS  Google Scholar 

  53. Wakamatsu Y, Pristyazhnyuk S, Kinoshita M, et al. The see-through medaka: A fish model that is transparent throughout life. Proc Natl Acad Sci USA, 2001, 98: 10046–10050 10.1073/pnas.181204298, 1:CAS:528:DC%2BD3MXmvFWitr8%3D, 11526229

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  54. Freed J J, Mezger-Freed L. Stable haploid cultured cell lines from frog embryos. Proc Natl Acad Sci USA, 1970, 65: 337–344 10.1073/pnas.65.2.337, 1:STN:280:DyaE3c7htFCnug%3D%3D, 5263768

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  55. Yan H, Papadopoulos N, Marra G, et al. Conversion of diploidy to haploidy. Nature, 2000, 403: 723–724 10.1038/35002251, 1:CAS:528:DC%2BD3cXns1CjtA%3D%3D, 10693791

    Article  PubMed  CAS  Google Scholar 

  56. Kaufman M H, Robertson E J, Handyside A H, et al. Establishment of pluripotential cell lines from haploid mouse embryos. J Embryol Exp Morphol, 1983, 73: 249–261 1:STN:280:DyaL3s3mslehtg%3D%3D, 6875460

    PubMed  CAS  Google Scholar 

  57. Araki K, Okamoto H, Graveson A C, et al. Analysis of haploid development based on expression patterns of developmental genes in the medaka Oryzias latipes. Dev Growth Differ, 2001, 43: 591–599 10.1046/j.1440-169X.2001.00601.x, 1:CAS:528:DC%2BD3MXotlylt7c%3D, 11576176

    Article  PubMed  CAS  Google Scholar 

  58. Yi M, Hong N, Hong Y. Generation of medaka fish haploid embryonic stem cells. Science, 2009, 326: 430–433 10.1126/science.1175151, 1:CAS:528:DC%2BD1MXht1GgtLfI, 19833967

    Article  PubMed  CAS  Google Scholar 

  59. Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: Its biology and applications in humans and animals. Reprod Biomed Online, 2005, 10: 247–288 15823233, 10.1016/S1472-6483(10)60947-9

    Article  PubMed  Google Scholar 

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Yi, M., Hong, N., Li, Z. et al. Medaka fish stem cells and their applications. Sci. China Life Sci. 53, 426–434 (2010). https://doi.org/10.1007/s11427-010-0079-3

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