Most animal genomes are diploid, and mammalian development depends on specific adaptations that have evolved secondary to diploidy. Genomic imprinting and dosage compensation restrict haploid development to early embryos. Recently, haploid mammalian development has been reinvestigated since the establishment of haploid embryonic stem cells (ESCs) from mouse embryos. Haploid cells possess one copy of each gene, facilitating the generation of loss-of-function mutations in a single step. Recessive mutations can then be assessed in forward genetic screens. Applications of haploid mammalian cell systems in screens have been illustrated in several recent publications. Haploid ESCs are characterized by a wide developmental potential and can contribute to chimeric embryos and mice. Different strategies for introducing genetic modifications from haploid ESCs into the mouse germline have been further developed. Haploid ESCs therefore introduce new possibilities in mammalian genetics and could offer an unprecedented tool for genome exploration in the future.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Allen ND, Barton SC, Hilton K, Norris ML, Surani MA. 1994. A functional analysis of imprinting in parthenogenetic embryonic stem cells. Development 120:1473–82 [Google Scholar]
  2. Andersson BS, Beran M, Pathak S, Goodacre A, Barlogie B, McCredie KB. 1987. Ph-positive chronic myeloid leukemia with near-haploid conversion in vivo and establishment of a continuously growing cell line with similar cytogenetic pattern. Cancer Genet. Cytogenet. 24:335–43 [Google Scholar]
  3. Aspberg F, Mertens F, Bauer HC, Lindholm J, Mitelman F, Mandahl N. 1995. Near-haploidy in two malignant fibrous histiocytomas. Cancer Genet. Cytogenet. 79:119–22 [Google Scholar]
  4. Beukeboom LW, Kamping A, Louter M, Pijnacker LP, Katju V. et al. 2007. Haploid females in the parasitic wasp Nasonia vitripennis. Science 315:206 [Google Scholar]
  5. Birsoy K, Wang T, Possemato R, Yilmaz OH, Koch CE. et al. 2013. MCT1-mediated transport of a toxic molecule is an effective strategy for targeting glycolytic tumors. Nat. Genet. 45:104–8 [Google Scholar]
  6. Braden AW, Austin CR. 1954. Reactions of unfertilized mouse eggs to some experimental stimuli. Exp. Cell Res. 7:277–80 [Google Scholar]
  7. Brandhorst BP, Corley-Smith GE. 2004. Production of haploid and diploid androgenetic zebrafish. Methods Mol. Biol. 254:255–70 [Google Scholar]
  8. Brickman JM, Tsakiridis A, To C, Stanford WL. 2010. A wider context for gene trap mutagenesis. Methods Enzymol. 477:271–95 [Google Scholar]
  9. Brodeur GM, Williams DL, Look AT, Bowman WP, Kalwinsky DK. 1981. Near-haploid acute lymphoblastic leukemia: A unique subgroup with a poor prognosis?. Blood 58:14–19 [Google Scholar]
  10. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B. et al. 2007. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191–95 [Google Scholar]
  11. Brown SD, Nolan PM. 1998. Mouse mutagenesis—systematic studies of mammalian gene function. Hum. Mol. Genet. 7:1627–33 [Google Scholar]
  12. Buehr M, Meek S, Blair K, Yang J, Ure J. et al. 2008. Capture of authentic embryonic stem cells from rat blastocysts. Cell 135:1287–98 [Google Scholar]
  13. Bürckstümmer T, Banning C, Hainzl P, Schobesberger R, Kerzendorfer C. et al. 2013. A reversible gene trap collection empowers haploid genetics in human cells. Nat. Methods 10:965–71 [Google Scholar]
  14. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I. et al. 2009. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326:1231–35 [Google Scholar]
  15. Carette JE, Guimaraes CP, Wuethrich I, Blomen VA, Varadarajan M. et al. 2011a. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nat. Biotechnol. 29:542–46 [Google Scholar]
  16. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G. et al. 2011b. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477:340–43 [Google Scholar]
  17. Cattanach BM, Kirk M. 1985. Differential activity of maternally and paternally derived chromosome regions in mice. Nature 315:496–98 [Google Scholar]
  18. Chen Z, Liu Z, Huang J, Amano T, Li C. et al. 2009. Birth of parthenote mice directly from parthenogenetic embryonic stem cells. Stem Cells 27:2136–45 [Google Scholar]
  19. Christiansen DG, Jakob C, Arioli M, Roethlisberger S, Reyer HU. 2010. Coexistence of diploid and triploid hybrid water frogs: Population differences persist in the apparent absence of differential survival. BMC Ecol. 10:14 [Google Scholar]
  20. Comai L. 2005. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6:836–46 [Google Scholar]
  21. Corley-Smith GE, Lim CJ, Brandhorst BP. 1996. Production of androgenetic zebrafish (Danio rerio). Genetics 142:1265–76 [Google Scholar]
  22. Corver WE, Ruano D, Weijers K, den Hartog WC, van Nieuwenhuizen MP. et al. 2012. Genome haploidisation with chromosome 7 retention in oncocytic follicular thyroid carcinoma. PLOS ONE 7:e38287 [Google Scholar]
  23. Debec A. 1978. Haploid cell cultures of Drosophila melanogaster. Nature 274:255–56 [Google Scholar]
  24. Debec A. 1984. Evolution of karyotype in haploid cell lines of Drosophila melanogaster. Exp. Cell Res. 151:236–46 [Google Scholar]
  25. Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T. 2005. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122:473–83 [Google Scholar]
  26. Elling U, Taubenschmid J, Wirnsberger G, O'Malley R, Demers SP. et al. 2011. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell 9:563–74 [Google Scholar]
  27. Freed JJ, Mezger-Freed L. 1970. Stable haploid cultured cell lines from frog embryos. Proc. Natl. Acad. Sci. USA 65:337–44 [Google Scholar]
  28. Friedel RH, Soriano P. 2010. Gene trap mutagenesis in the mouse. Methods Enzymol. 477:243–69 [Google Scholar]
  29. Fundele RH, Norris ML, Barton SC, Fehlau M, Howlett SK. et al. 1990. Temporal and spatial selection against parthenogenetic cells during development of fetal chimeras. Development 108:203–11 [Google Scholar]
  30. Gancberg D, Dargent JL, Verhest A, Kentos A, Feremans W. et al. 2001. Near haploid blast phase in a chronic myeloid leukemia detected by fluorescence in situ hybridization using a BCR-ABL probe. Cancer Genet. Cytogenet. 128:172–74 [Google Scholar]
  31. Ganesan S, Richardson AL, Wang ZC, Iglehart JD, Miron A. et al. 2005. Abnormalities of the inactive X chromosome are a common feature of BRCA1 mutant and sporadic basal-like breast cancer. Cold Spring Harb. Symp. Quant. Biol. 70:93–97 [Google Scholar]
  32. Gibbons B, MacCallum P, Watts E, Rohatiner AZ, Webb D. et al. 1991. Near haploid acute lymphoblastic leukemia: seven new cases and a review of the literature. Leukemia 5:738–43 [Google Scholar]
  33. Graham CF. 1966. The effect of cell size and DNA content on the cellular regulation of DNA synthesis in haploid and diploid embryos. Exp. Cell Res. 43:13–19 [Google Scholar]
  34. Graham CF. 1970. Parthenogenetic mouse blastocysts. Nature 226:165–67 [Google Scholar]
  35. Gribnau J, Grootegoed JA. 2012. Origin and evolution of X chromosome inactivation. Curr. Opin. Cell Biol. 24:397–404 [Google Scholar]
  36. Guimaraes CP, Carette JE, Varadarajan M, Antos J, Popp MW. et al. 2011. Identification of host cell factors required for intoxication through use of modified cholera toxin. J. Cell Biol. 195:751–64 [Google Scholar]
  37. Horii T, Morita S, Kimura M, Kobayashi R, Tamura D. et al. 2013. Genome engineering of mammalian haploid embryonic stem cells using the Cas9/RNA system. Peer J. 1:e230 [Google Scholar]
  38. Horn C, Hansen J, Schnutgen F, Seisenberger C, Floss T. et al. 2007. Splinkerette PCR for more efficient characterization of gene trap events. Nat. Genet. 39:933–34 [Google Scholar]
  39. Ito M, Kaneko-Ishino T, Ishino F, Matsuhashi M, Yokoyama M, Katsuki M. 1991. Fate of haploid parthenogenetic cells in mouse chimeras during development. J. Exp. Zool. 257:178–83 [Google Scholar]
  40. Jae LT, Raaben M, Riemersma M, van Beusekom E, Blomen VA. et al. 2013. Deciphering the glycosylome of dystroglycanopathies using haploid screens for Lassa virus entry. Science 340:479–83 [Google Scholar]
  41. Jiang H, Sun B, Wang W, Zhang Z, Gao F. et al. 2007. Activation of paternally expressed imprinted genes in newly derived germline-competent mouse parthenogenetic embryonic stem cell lines. Cell Res. 17:792–803 [Google Scholar]
  42. Kaufman MH. 1978. Chromosome analysis of early postimplantation presumptive haploid parthenogenetic mouse embryos. J. Embryol. Exp. Morphol. 45:85–91 [Google Scholar]
  43. Kaufman MH, Barton SC, Surani MA. 1977. Normal postimplantation development of mouse parthenogenetic embryos to the forelimb bud stage. Nature 265:53–55 [Google Scholar]
  44. Kaufman MH, Robertson EJ, Handyside AH, Evans MJ. 1983. Establishment of pluripotential cell lines from haploid mouse embryos. J. Embryol. Exp. Morphol. 73:249–61 [Google Scholar]
  45. Kondrashov AS, Crow JF. 1991. Haploidy or diploidy: Which is better?. Nature 351:314–15 [Google Scholar]
  46. Kono T. 2009. Genetic modification for bimaternal embryo development. Reprod. Fertil. Dev. 21:31–36 [Google Scholar]
  47. Kono T, Obata Y, Wu Q, Niwa K, Ono Y. et al. 2004. Birth of parthenogenetic mice that can develop to adulthood. Nature 428:860–64 [Google Scholar]
  48. Kono T, Sotomaru Y, Sato Y, Nakahara T. 1993. Development of androgenetic mouse embryos produced by in vitro fertilization of enucleated oocytes. Mol. Reprod. Dev. 34:43–46 [Google Scholar]
  49. Koscielny G, Yaikhom G, Iyer V, Meehan TF, Morgan H. et al. 2014. The International Mouse Phenotyping Consortium Web Portal, a unified point of access for knockout mice and related phenotyping data. Nucleic Acids Res. 42:D802–9 [Google Scholar]
  50. Kotecki M, Reddy PS, Cochran BH. 1999. Isolation and characterization of a near-haploid human cell line. Exp. Cell Res. 252:273–80 [Google Scholar]
  51. Lawson HA, Cheverud JM, Wolf JB. 2013. Genomic imprinting and parent-of-origin effects on complex traits. Nat. Rev. Genet. 14:609–17 [Google Scholar]
  52. Lee CC, Carette JE, Brummelkamp TR, Ploegh HL. 2013. A reporter screen in a human haploid cell line identifies CYLD as a constitutive inhibitor of NF-κB. PLOS ONE 8:e70339 [Google Scholar]
  53. Leeb M, Dietmann S, Paramor M, Niwa H, Smith A. 2014. Genetic exploration of the exit from self-renewal using haploid embryonic stem cells. Cell Stem Cell 14:385–93 [Google Scholar]
  54. Leeb M, Walker R, Mansfield B, Nichols J, Smith A, Wutz A. 2012. Germline potential of parthenogenetic haploid mouse embryonic stem cells. Development 139:3301–5 [Google Scholar]
  55. Leeb M, Wutz A. 2011. Derivation of haploid embryonic stem cells from mouse embryos. Nature 479:131–34 [Google Scholar]
  56. Leeb M, Wutz A. 2012. Establishment of epigenetic patterns in development. Chromosoma 121:251–62 [Google Scholar]
  57. Lefebvre L. 2012. Engineering of large deletions and duplications in vivo. Methods Mol. Biol. 925:137–46 [Google Scholar]
  58. Leitch HG, McEwen KR, Turp A, Encheva V, Carroll T. et al. 2013. Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 20:311–16 [Google Scholar]
  59. Li MA, Pettitt SJ, Eckert S, Ning Z, Rice S. et al. 2013a. The piggyBac transposon displays local and distant reintegration preferences and can cause mutations at noncanonical integration sites. Mol. Cell. Biol. 33:1317–30 [Google Scholar]
  60. Li MA, Pettitt SJ, Yusa K, Bradley A. 2010. Genome-wide forward genetic screens in mouse ES cells. Methods Enzymol. 477:217–42 [Google Scholar]
  61. Li W, Li X, Li T, Jiang MG, Wan H. et al. 2013b. Genetic modification and screening in rat using haploid embryonic stem cells. Cell Stem Cell 14:404–14 [Google Scholar]
  62. Li W, Shuai L, Wan H, Dong M, Wang M. et al. 2012. Androgenetic haploid embryonic stem cells produce live transgenic mice. Nature 490:407–11 [Google Scholar]
  63. Liu A, Eggenschwiler J. 2014. Identifying essential genes in mouse development via an ENU-based forward genetic approach. Methods Mol. Biol. 1092:95–118 [Google Scholar]
  64. Liu Z, Hu Z, Pan X, Li M, Togun TA. et al. 2011. Germline competency of parthenogenetic embryonic stem cells from immature oocytes of adult mouse ovary. Hum. Mol. Genet. 20:1339–52 [Google Scholar]
  65. Lutes AA, Baumann DP, Neaves WB, Baumann P. 2011. Laboratory synthesis of an independently reproducing vertebrate species. Proc. Natl. Acad. Sci. USA 108:9910–15 [Google Scholar]
  66. Ma SK, Chan GC, Wan TS, Lam CK, Ha SY. et al. 1998. Near-haploid common acute lymphoblastic leukaemia of childhood with a second hyperdiploid line: a DNA ploidy and fluorescence in-situ hybridization study. Br. J. Haematol. 103:750–55 [Google Scholar]
  67. Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R. 1997. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 11:156–66 [Google Scholar]
  68. Marks H, Kalkan T, Menafra R, Denissov S, Jones K. et al. 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149:590–604 [Google Scholar]
  69. McGrath J, Solter D. 1983. Nuclear transplantation in the mouse embryo by microsurgery and cell fusion. Science 220:1300–2 [Google Scholar]
  70. McGrath J, Solter D. 1984. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–83 [Google Scholar]
  71. Modlinski JA. 1975. Haploid mouse embryos obtained by microsurgical removal of one pronucleus. J. Embryol. Exp. Morphol. 33:897–905 [Google Scholar]
  72. Mott R, Yuan W, Kaisaki P, Gan X, Cleak J. et al. 2014. The architecture of parent-of-origin effects in mice. Cell 156:332–42 [Google Scholar]
  73. Ng K, Daigle N, Bancaud A, Ohhata T, Humphreys P. et al. 2011. A system for imaging the regulatory noncoding Xist RNA in living mouse embryonic stem cells. Mol. Biol. Cell 22:2634–45 [Google Scholar]
  74. Obata Y, Ono Y, Akuzawa H, Kwon OY, Yoshizawa M, Kono T. 2000. Post-implantation development of mouse androgenetic embryos produced by in-vitro fertilization of enucleated oocytes. Hum. Reprod. 15:874–80 [Google Scholar]
  75. Onodera N, McCabe NR, Nachman JB, Johnson FL, Le Beau MM. et al. 1992. Hyperdiploidy arising from near-haploidy in childhood acute lymphoblastic leukemia. Genes Chromosom. Cancer 4:331–36 [Google Scholar]
  76. Orndal C, Mandahl N, Carlen B, Willen H, Wennerberg J. et al. 1992. Near-haploid clones in a malignant fibrous histiocytoma. Cancer Genet. Cytogenet. 60:147–51 [Google Scholar]
  77. Otto SP, Jarne P. 2001. Evolution. Haploids—hapless or happening?. Science 292:2441–43 [Google Scholar]
  78. Papatheodorou P, Carette JE, Bell GW, Schwan C, Guttenberg G. et al. 2011. Lipolysis-stimulated lipoprotein receptor (LSR) is the host receptor for the binary toxin Clostridium difficile transferase (CDT). Proc. Natl. Acad. Sci. USA 108:16422–27 [Google Scholar]
  79. Paquin C, Adams J. 1983. Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302:495–500 [Google Scholar]
  80. Perrot V, Richerd S, Valero M. 1991. Transition from haploidy to diploidy. Nature 351:315–17 [Google Scholar]
  81. Pettitt SJ, Rehman FL, Bajrami I, Brough R, Wallberg F. et al. 2013. A genetic screen using the PiggyBac transposon in haploid cells identifies Parp1 as a mediator of olaparib toxicity. PLOS ONE 8:e61520 [Google Scholar]
  82. Philippe C, Landureau JC. 1975. Culture de cellules embryonnaires et d'hemocytes de blatte d'origine parthenogenetique. Exp. Cell Res. 96:287–96 [Google Scholar]
  83. Pollex T, Heard E. 2012. Recent advances in X-chromosome inactivation research. Curr. Opin. Cell Biol. 24:825–32 [Google Scholar]
  84. Reiling JH, Clish CB, Carette JE, Varadarajan M, Brummelkamp TR, Sabatini DM. 2011. A haploid genetic screen identifies the major facilitator domain containing 2A (MFSD2A) transporter as a key mediator in the response to tunicamycin. Proc. Natl. Acad. Sci. USA 108:11756–65 [Google Scholar]
  85. Reiling JH, Olive AJ, Sanyal S, Carette JE, Brummelkamp TR. et al. 2013. A CREB3-ARF4 signalling pathway mediates the response to Golgi stress and susceptibility to pathogens. Nat. Cell Biol. 15:1473–85 [Google Scholar]
  86. Rosmarin DM, Carette JE, Olive AJ, Starnbach MN, Brummelkamp TR, Ploegh HL. 2012. Attachment of Chlamydia trachomatis L2 to host cells requires sulfation. Proc. Natl. Acad. Sci. USA 109:10059–64 [Google Scholar]
  87. Safavi S, Forestier E, Golovleva I, Barbany G, Nord KH. et al. 2013. Loss of chromosomes is the primary event in near-haploid and low-hypodiploid acute lymphoblastic leukemia. Leukemia 27:248–50 [Google Scholar]
  88. Schnutgen F, Hansen J, De-Zolt S, Horn C, Lutz M. et al. 2008. Enhanced gene trapping in mouse embryonic stem cells. Nucleic Acids Res. 36:e133 [Google Scholar]
  89. Silk AD, Zasadil LM, Holland AJ, Vitre B, Cleveland DW, Weaver BA. 2013. Chromosome missegregation rate predicts whether aneuploidy will promote or suppress tumors. Proc. Natl. Acad. Sci. USA 110:E4134–41 [Google Scholar]
  90. Solter D. 1988. Differential imprinting and expression of maternal and paternal genomes. Annu. Rev. Genet. 22:127–46 [Google Scholar]
  91. Spencer HG, Clark AG. 2014. Non-conflict theories for the evolution of genomic imprinting. Heredity 113112–18 [Google Scholar]
  92. Stark B, Jeison M, Gobuzov R, Krug H, Glaser-Gabay L. et al. 2001. Near haploid childhood acute lymphoblastic leukemia masked by hyperdiploid line: detection by fluorescence in situ hybridization. Cancer Genet. Cytogenet. 128:108–13 [Google Scholar]
  93. Stock M, Lamatsch DK, Steinlein C, Epplen JT, Grosse WR. et al. 2002. A bisexually reproducing all-triploid vertebrate. Nat. Genet. 30:325–28 [Google Scholar]
  94. Sukov WR, Ketterling RP, Wei S, Monaghan K, Blunden P. et al. 2010. Nearly identical near-haploid karyotype in a peritoneal mesothelioma and a retroperitoneal malignant peripheral nerve sheath tumor. Cancer Genet. Cytogenet. 202:123–28 [Google Scholar]
  95. Sunil SK, Prakash PN, Hariharan S, Vinod G, Preethi RT. et al. 2006. Adult acute lymphoblastic leukemia with near haploidy, hyperdiploidy and Ph positive lines: a rare entity with poor prognosis. Leuk. Lymphoma 47:561–63 [Google Scholar]
  96. Tarkowski AK, Rossant J. 1976. Haploid mouse blastocysts developed from bisected zygotes. Nature 259:663–65 [Google Scholar]
  97. Tarkowski AK, Witkowska A, Nowicka J. 1970. Experimental partheonogenesis in the mouse. Nature 226:162–65 [Google Scholar]
  98. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP. et al. 2007. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196–99 [Google Scholar]
  99. Thompson SL, Compton DA. 2008. Examining the link between chromosomal instability and aneuploidy in human cells. J. Cell Biol. 180:665–72 [Google Scholar]
  100. Thorgaard GH, Gall GA. 1979. Adult triploids in a rainbow trout family. Genetics 93:961–73 [Google Scholar]
  101. Timms RT, Duncan LM, Tchasovnikarova IA, Antrobus R, Smith DL. et al. 2013. Haploid genetic screens identify an essential role for PLP2 in the downregulation of novel plasma membrane targets by viral E3 ubiquitin ligases. PLOS Pathog. 9:e1003772 [Google Scholar]
  102. Uren AG, Mikkers H, Kool J, van der Weyden L, Lund AH. et al. 2009. A high-throughput splinkerette-PCR method for the isolation and sequencing of retroviral insertion sites. Nat. Protoc. 4:789–98 [Google Scholar]
  103. Wan H, He Z, Dong M, Gu T, Luo GZ. et al. 2013. Parthenogenetic haploid embryonic stem cells produce fertile mice. Cell Res. 23:1330–33 [Google Scholar]
  104. Wang T, Wei JJ, Sabatini DM, Lander ES. 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343:80–84 [Google Scholar]
  105. Wang W, Bradley A, Huang Y. 2009. A piggyBac transposon-based genome-wide library of insertionally mutated Blm-deficient murine ES cells. Genome Res. 19:667–73 [Google Scholar]
  106. Weeks AR, Marec F, Breeuwer JA. 2001. A mite species that consists entirely of haploid females. Science 292:2479–82 [Google Scholar]
  107. White M. 1984. Chromosomal mechanisms in animal reproduction. Boll. Zool. 51:1–23 [Google Scholar]
  108. Wiellette E, Grinblat Y, Austen M, Hirsinger E, Amsterdam A. et al. 2004. Combined haploid and insertional mutation screen in the zebrafish. Genesis 40:231–40 [Google Scholar]
  109. Yamauchi Y, Riel JM, Stoytcheva Z, Ward MA. 2013. Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse. Science 343:69–72 [Google Scholar]
  110. Yang H, Liu Z, Ma Y, Zhong C, Yin Q. et al. 2013. Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes. Cell Res. 23:1187–200 [Google Scholar]
  111. Yang H, Shi L, Wang BA, Liang D, Zhong C. et al. 2012. Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Cell 149:605–17 [Google Scholar]
  112. Yi M, Hong N, Hong Y. 2009. Generation of medaka fish haploid embryonic stem cells. Science 326:430–33 [Google Scholar]
  113. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI. et al. 2013. Xist RNA is a potent suppressor of hematologic cancer in mice.. Cell 152:727–42 [Google Scholar]
  114. Yuan Y, Huang X, Zhang L, Zhu Y, Huang Y. et al. 2013. Medaka haploid embryonic stem cells are susceptible to Singapore grouper iridovirus as well as to other viruses of aquaculture fish species. J. Gen. Vir. 94:2352–59 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error