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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Hong Y, Gui J, Chen S, et al. Embryonic stem cells in fish. Acta Zool Sin, 2003, 49: 281–294
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
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
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
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
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
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
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
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
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
Xu H, Li M, Gui J, et al. Fish germ cells. Sci China Life Sci, 2010, 53: 435–446 20596909
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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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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DOI: https://doi.org/10.1007/s11427-010-0079-3