Haploid genomes illustrate epigenetic constraints and gene dosage effects in mammals

Epigenetics and Chromatin

Volumn 6, Issue 1, 2013, Pages

  Leeb, Martin ^a   Wutz, Anton ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

Development; Epigenetics; Evolution; Haploid cells; Stem cells; Tumor

Indexed keywords

ADULTHOOD; DIPLOIDY; EPIGENETICS; GENE CONTROL; GENE DOSAGE; GENETIC SCREENING; GENOME; GENOME IMPRINTING; HAPLOIDY; HUMAN; INSECT; MAMMAL; MAMMAL CELL; MITE; MOUSE EMBRYO; NONHUMAN; PLOIDY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; VERTEBRATE; X CHROMOSOME INACTIVATION;

ANIMALIA; MAMMALIA;

EID: 84888997604     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-6-41     Document Type: Review

References (97)

1. The evolution of alternative genetic systems in insects. Normark BB, Annu Rev Entomol 2003 48 397 423 10.1146/annurev.ento.48.091801.112703 12221039 (Pubitemid 37365398)
2. A mite species that consists entirely of haploid females. Weeks AR, Marec F, Breeuwer JA, Science 2001 292 2479 2482 10.1126/science.1060411 11431565 (Pubitemid 32601658)
3. Haploid females in the parasitic wasp Nasonia vitripennis. Beukeboom LW, Kamping A, Louter M, Pijnacker LP, Katju V, Ferree PM, Werren JH, Science 2007 315 206 10.1126/science.1133388 17218519 (Pubitemid 46166359)
4. Evolution of karyotype in haploid cell lines of Drosophila melanogaster. Debec A, Exp Cell Res 1984 151 236 246 10.1016/0014-4827(84)90371-9 6421610 (Pubitemid 14156919)
5. Coexistence of diploid and triploid hybrid water frogs: population differences persist in the apparent absence of differential survival. Christiansen DG, Jakob C, Arioli M, Roethlisberger S, Reyer HU, BMC Ecol 2010 10 14 10.1186/1472-6785-10-14 20507575
6. Laboratory synthesis of an independently reproducing vertebrate species. Lutes AA, Baumann DP, Neaves WB, Baumann P, Proc Natl Acad Sci U S A 2011 108 9910 9915 10.1073/pnas.1102811108 21543715
7. A bisexually reproducing all-triploid vertebrate. Stock M, Lamatsch DK, Steinlein C, Epplen JT, Grosse WR, Hock R, Klapperstuck T, Lampert KP, Scheer U, Schmid M, Schartl M, Nat Genet 2002 30 325 328 10.1038/ng839 11836500
8. The advantages and disadvantages of being polyploid. Comai L, Nat Rev Genet 2005 6 836 846 16304599
9. Adult triploids in a rainbow trout family. Thorgaard GH, Gall GA, Genetics 1979 93 961 973 546676 (Pubitemid 10077477)
10. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Ohno S, Semin Cell Dev Biol 1999 10 517 522 10.1006/scdb.1999.0332 10597635 (Pubitemid 129513238)
11. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Nakatani Y, Takeda H, Kohara Y, Morishita S, Genome Res 2007 17 1254 1265 10.1101/gr.6316407 17652425 (Pubitemid 47360900)
12. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Freeling M, Thomas BC, Genome Res 2006 16 805 814 10.1101/gr.3681406 16818725 (Pubitemid 43992905)
13. Stable haploid cultured cell lines from frog embryos. Freed JJ, Mezger-Freed L, Proc Natl Acad Sci U S A 1970 65 337 344 10.1073/pnas.65.2.337 5263768
14. A genetic linkage map for the zebrafish. Postlethwait JH, Johnson SL, Midson CN, Talbot WS, Gates M, Ballinger EW, Africa D, Andrews R, Carl T, Eisen JS, et al. Science 1994 264 699 703 10.1126/science.8171321 8171321 (Pubitemid 24185879)
15. Production of haploid and diploid androgenetic zebrafish. Brandhorst BP, Corley-Smith GE, Methods Mol Biol 2004 254 255 270 15041767
16. Production of androgenetic zebrafish (Danio rerio). Corley-Smith GE, Lim CJ, Brandhorst BP, Genetics 1996 142 1265 1276 8846903 (Pubitemid 26115506)
17. Generation of medaka fish haploid embryonic stem cells. Yi M, Hong N, Hong Y, Science 2009 326 430 433 10.1126/science.1175151 19833967
18. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, et al. Nature 2004 431 946 957 10.1038/nature03025 15496914 (Pubitemid 39434410)
19. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Meyer A, Van de Peer Y, Bioessays 2005 27 937 945 10.1002/bies.20293 16108068 (Pubitemid 41415948)
20. Parthenogenetic mouse blastocysts. Graham CF, Nature 1970 226 165 167 10.1038/226165a0 5437002
21. Experimental partheonogenesis in the mouse. Tarkowski AK, Witkowska A, Nowicka J, Nature 1970 226 162 165 10.1038/226162a0 5437001
22. Reactions of unfertilized mouse eggs to some experimental stimuli. Braden AW, Austin CR, Exp Cell Res 1954 7 277 280 10.1016/0014-4827(54)90063-4 13200528
23. Development of androgenetic mouse embryos produced by in vitro fertilization of enucleated oocytes. Kono T, Sotomaru Y, Sato Y, Nakahara T, Mol Reprod Dev 1993 34 43 46 10.1002/mrd.1080340107 8418815 (Pubitemid 23014501)
24. Haploid mouse blastocysts developed from bisected zygotes. Tarkowski AK, Rossant J, Nature 1976 259 663 665 10.1038/259663a0 1250417
25. Haploid mouse embryos obtained by microsurgical removal of one pronucleus. Modlinski JA, J Embryol Exp Morphol 1975 33 897 905 1176880
26. Chromosome analysis of early postimplantation presumptive haploid parthenogenetic mouse embryos. Kaufman MH, J Embryol Exp Morphol 1978 45 85 91 670867 (Pubitemid 8375672)
27. Parental imprinting of the mouse insulin-like growth factor II gene. DeChiara TM, Robertson EJ, Efstratiadis A, Cell 1991 64 849 859 10.1016/0092-8674(91)90513-X 1997210 (Pubitemid 121001171)
28. Parental imprinting of the mouse H19 gene. Bartolomei MS, Zemel S, Tilghman SM, Nature 1991 351 153 155 10.1038/351153a0 1709450 (Pubitemid 21896555)
29. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Barlow DP, Stoger R, Herrmann BG, Saito K, Schweifer N, Nature 1991 349 84 87 10.1038/349084a0 1845916 (Pubitemid 21912022)
30. Differential imprinting and expression of maternal and paternal genomes. Solter D, Annu Rev Genet 1988 22 127 146 10.1146/annurev.ge.22.120188.001015 3071246 (Pubitemid 19156666)
31. Completion of mouse embryogenesis requires both the maternal and paternal genomes. McGrath J, Solter D, Cell 1984 37 179 183 10.1016/0092-8674(84)90313-1 6722870 (Pubitemid 14079849)
32. Differential activity of maternally and paternally derived chromosome regions in mice. Cattanach BM, Kirk M, Nature 1985 315 496 498 10.1038/315496a0 4000278 (Pubitemid 15232865)
33. A rheostat model for a rapid and reversible form of imprinting-dependent evolution. Beaudet AL, Jiang YH, Am J Hum Genet 2002 70 1389 1397 10.1086/340969 11992247 (Pubitemid 34533887)
34. Genomic imprinting in mammalian development: a parental tug-of-war. Moore T, Haig D, Trends Genet 1991 7 45 49 2035190 (Pubitemid 121001901)
35. Growth effects of uniparental disomies and the conflict theory of genomic imprinting. Hurst LD, McVean GT, Trends Genet 1997 13 436 443 10.1016/S0168-9525(97)01273-0 9385840 (Pubitemid 27479902)
36. Mechanisms and consequences of widespread random monoallelic expression. Chess A, Nat Rev Genet 2012 13 421 428 22585065
37. Role and control of X chromosome dosage in mammalian development. Schulz EG, Heard E, Curr Opin Genet Dev 2013 23 109 115 10.1016/j.gde.2013.01.008 23465885
38. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Wutz A, Rasmussen TP, Jaenisch R, Nat Genet 2002 30 167 174 10.1038/ng820 11780141
39. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R, Genes Dev 1997 11 156 166 10.1101/gad.11.2.156 9009199 (Pubitemid 27081893)
40. The chromosome make-up of mouse embryonic stem cells is predictive of somatic and germ cell chimaerism. Longo L, Bygrave A, Grosveld FG, Pandolfi PP, Transgenic Res 1997 6 321 328 10.1023/A:1018418914106 9322369 (Pubitemid 27422816)
41. Allograft theory: transmission of devil facial-tumour disease. Pearse AM, Swift K, Nature 2006 439 549 10.1038/439549a 16452970 (Pubitemid 43185372)
42. Chromosome studies of a transplanted and a primary canine venereal sarcoma. Weber WT, Nowell PC, Hare WC, J Natl Cancer Inst 1965 35 537 547 5897386
43. Ph-positive chronic myeloid leukemia with near-haploid conversion in vivo and establishment of a continuously growing cell line with similar cytogenetic pattern. Andersson BS, Beran M, Pathak S, Goodacre A, Barlogie B, McCredie KB, Cancer Genet Cytogenet 1987 24 335 343 10.1016/0165-4608(87)90116-6 3466682 (Pubitemid 17231521)
44. Near-haploid acute lymphoblastic leukemia: a unique subgroup with a poor prognosis? Brodeur GM, Williams DL, Look AT, Bowman WP, Kalwinsky DK, Blood 1981 58 14 19 6940627 (Pubitemid 11064454)
45. Near haploid blast phase in a chronic myeloid leukemia detected by fluorescence in situ hybridization using a BCR-ABL probe. Gancberg D, Dargent JL, Verhest A, Kentos A, Feremans W, Lohrisch C, Kornreich A, Cancer Genet Cytogenet 2001 128 172 174 10.1016/S0165-4608(01)00403-4 11478300 (Pubitemid 32706594)
46. Near haploid acute lymphoblastic leukemia: seven new cases and a review of the literature. Gibbons B, MacCallum P, Watts E, Rohatiner AZ, Webb D, Katz FE, Secker-Walker LM, Temperley IJ, Harrison CJ, Campbell RH, et al. Leukemia 1991 5 738 743 1943226
47. Isolation and characterization of a near-haploid human cell line. Kotecki M, Reddy PS, Cochran BH, Exp Cell Res 1999 252 273 280 10.1006/excr.1999.4656 10527618 (Pubitemid 29530258)
48. Near haploid childhood acute lymphoblastic leukemia masked by hyperdiploid line: detection by fluorescence in situ hybridization. Stark B, Jeison M, Gobuzov R, Krug H, Glaser-Gabay L, Luria D, El-Hasid R, Harush MB, Avrahami G, Fisher S, Stein J, Zaizov R, Yaniv I, Cancer Genet Cytogenet 2001 128 108 113 10.1016/S0165-4608(01)00411-3 11463448 (Pubitemid 32706582)
49. Adult acute lymphoblastic leukemia with near haploidy, hyperdiploidy and Ph positive lines: a rare entity with poor prognosis. Sunil SK, Prakash PN, Hariharan S, Vinod G, Preethi RT, Geetha N, Ankathil R, Leuk Lymphoma 2006 47 561 563 10.1080/10428190500361094 16396782 (Pubitemid 43102108)
50. Near-haploidy in two malignant fibrous histiocytomas. Aspberg F, Mertens F, Bauer HC, Lindholm J, Mitelman F, Mandahl N, Cancer Genet Cytogenet 1995 79 119 122 10.1016/0165-4608(94)00124-T 7889501
51. Near-haploid clones in a malignant fibrous histiocytoma. Orndal C, Mandahl N, Carlen B, Willen H, Wennerberg J, Heim S, Mitelman F, Cancer Genet Cytogenet 1992 60 147 151 10.1016/0165-4608(92)90007-U 1318780
52. Nearly identical near-haploid karyotype in a peritoneal mesothelioma and a retroperitoneal malignant peripheral nerve sheath tumor. Sukov WR, Ketterling RP, Wei S, Monaghan K, Blunden P, Mazzara P, Raghavan R, Oliviera AM, Wiktor AE, Keeney GL, Van Dyke DL, Cancer Genet Cytogenet 2010 202 123 128 10.1016/j.cancergencyto.2010.07.120 20875874
53. Loss of chromosomes is the primary event in near-haploid and low-hypodiploid acute lymphoblastic leukemia. Safavi S, Forestier E, Golovleva I, Barbany G, Nord KH, Moorman AV, Harrison CJ, Johansson B, Paulsson K, Leukemia 2013 27 248 250 10.1038/leu.2012.227 22889820
54. Genome haploidisation with chromosome 7 retention in oncocytic follicular thyroid carcinoma. Corver WE, Ruano D, Weijers K, den Hartog WC, van Nieuwenhuizen MP, de Miranda N, van Eijk R, Middeldorp A, Jordanova ES, Oosting J, Kapiteijn E, Hovens G, Smit J, van Wezel T, Morreau H, PLoS One 2012 7 38287 10.1371/journal.pone.0038287 22675538
55. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, Mulherkar N, Kuehne AI, Kranzusch PJ, Griffin AM, Ruthel G, Dal Cin P, Dye JM, Whelan SP, Chandran K, Brummelkamp TR, Nature 2011 477 340 343 10.1038/nature10348 21866103
56. Establishment of pluripotential cell lines from haploid mouse embryos. Kaufman MH, Robertson EJ, Handyside AH, Evans MJ, J Embryol Exp Morphol 1983 73 249 261 6875460 (Pubitemid 13160101)
57. Normal postimplantation development of mouse parthenogenetic embryos to the forelimb bud stage. Kaufman MH, Barton SC, Surani MA, Nature 1977 265 53 55 10.1038/265053a0 556803 (Pubitemid 8004307)
58. Post-implantation development of mouse androgenetic embryos produced by in-vitro fertilization of enucleated oocytes. Obata Y, Ono Y, Akuzawa H, Kwon OY, Yoshizawa M, Kono T, Hum Reprod 2000 15 874 880 10.1093/humrep/15.4.874 10739836 (Pubitemid 30192739)
59. Birth of parthenogenetic mice that can develop to adulthood. Kono T, Obata Y, Wu Q, Niwa K, Ono Y, Yamamoto Y, Park ES, Seo JS, Ogawa H, Nature 2004 428 860 864 10.1038/nature02402 15103378 (Pubitemid 38529501)
60. Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Csankovszki G, Panning B, Bates B, Pehrson JR, Jaenisch R, Nat Genet 1999 22 323 324 10.1038/11887 10431231 (Pubitemid 29369518)
61. Loss of Xist imprinting in diploid parthenogenetic preimplantation embryos. Nesterova TB, Barton SC, Surani MA, Brockdorff N, Dev Biol 2001 235 343 350 10.1006/dbio.2001.0295 11437441 (Pubitemid 32661175)
62. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Elling U, Taubenschmid J, Wirnsberger G, O'Malley R, Demers SP, Vanhaelen Q, Shukalyuk AI, Schmauss G, Schramek D, Schnuetgen F, von Melchner H, Ecker JR, Stanford WL, Zuber J, Stark A, Penninger JM, Cell Stem Cell 2011 9 563 574 10.1016/j.stem.2011.10.012 22136931
63. Derivation of haploid embryonic stem cells from mouse embryos. Leeb M, Wutz A, Nature 2011 479 131 134 10.1038/nature10448 21900896
64. Androgenetic haploid embryonic stem cells produce live transgenic mice. Li W, Shuai L, Wan H, Dong M, Wang M, Sang L, Feng C, Luo GZ, Li T, Li X, Wang L, Zheng QY, Sheng C, Wu HJ, Liu Z, Liu L, Wang L, Wang XJ, Zhao XY, Zhou Q, Nature 2012 490 407 411 10.1038/nature11435 23023130
65. Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Yang H, Shi L, Wang BA, Liang D, Zhong C, Liu W, Nie Y, Liu J, Zhao J, Gao X, Li D, Xu GL, Li J, Cell 2012 149 605 617 10.1016/j.cell.2012.04.002 22541431
66. Germline potential of parthenogenetic haploid mouse embryonic stem cells. Leeb M, Walker R, Mansfield B, Nichols J, Smith A, Wutz A, Development 2012 139 3301 3305 10.1242/dev.083675 22912412
67. Establishment of epigenetic patterns in development. Leeb M, Wutz A, Chromosoma 2012 121 251 262 10.1007/s00412-012-0365-x 22427185
68. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C, Shimotohno K, Ishikawa F, Li E, Ueda HR, Nakayama J, Okano M, Genes Cells 2006 11 805 814 10.1111/j.1365-2443.2006.00984.x 16824199 (Pubitemid 43923351)
69. Polycomb complexes act redundantly to repress genomic repeats and genes. Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, Wutz A, Genes Dev 2010 24 265 276 10.1101/gad.544410 20123906
70. Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Kim Y, Sharov AA, McDole K, Cheng M, Hao H, Fan CM, Gaiano N, Ko MS, Zheng Y, Science 2011 334 1706 1710 10.1126/science.1211222 22116031
71. The ground state of embryonic stem cell self-renewal. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A, Nature 2008 453 519 523 10.1038/nature06968 18497825 (Pubitemid 351733324)
72. Nanog safeguards pluripotency and mediates germline development. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A, Nature 2007 450 1230 1234 10.1038/nature06403 18097409
73. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, Kemler R, Smith A, Nat Cell Biol 2011 13 838 845 10.1038/ncb2267 21685889
74. The transcriptional and epigenomic foundations of ground state pluripotency. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H, Nichols J, Kranz A, Stewart AF, Smith A, Stunnenberg HG, Cell 2012 149 590 604 10.1016/j.cell.2012.03.026 22541430
75. Naive pluripotency is associated with global DNA hypomethylation. Leitch HG, McEwen KR, Turp A, Encheva V, Carroll T, Grabole N, Mansfield W, Nashun B, Knezovich JG, Smith A, Surani MA, Hajkova P, Nat Struct Mol Biol 2013 20 311 316 10.1038/nsmb.2510 23416945
76. Influence of in vitro manipulation on the stability of methylation patterns in the Snurf/Snrpn-imprinting region in mouse embryonic stem cells. Schumacher A, Doerfler W, Nucleic Acids Res 2004 32 1566 1576 10.1093/nar/gkh322 15004243 (Pubitemid 38864684)
77. Establishment of a tetraploid cell line from mouse H-1 (ES) cells highly polyploidized with demecolcine. Fujikawa-Yamamoto K, Miyagoshi M, Yamagishi H, Cell Prolif 2007 40 327 337 10.1111/j.1365-2184.2007.00442.x 17531078 (Pubitemid 46802191)
78. Haploid genetic screens in human cells identify host factors used by pathogens. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I, Godarova A, Kotecki M, Cochran BH, Spooner E, Ploegh HL, Brummelkamp TR, Science 2009 326 1231 1235 10.1126/science.1178955 19965467
79. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Carette JE, Guimaraes CP, Wuethrich I, Blomen VA, Varadarajan M, Sun C, Bell G, Yuan B, Muellner MK, Nijman SM, Ploegh HL, Brummelkamp TR, Nat Biotechnol 2011 29 542 546 10.1038/nbt.1857 21623355
80. Attachment of Chlamydia trachomatis L2 to host cells requires sulfation. Rosmarin DM, Carette JE, Olive AJ, Starnbach MN, Brummelkamp TR, Ploegh HL, Proc Natl Acad Sci U S A 2012 109 10059 10064 10.1073/pnas.1120244109 22675117
81. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Jae LT, Raaben M, Riemersma M, van Beusekom E, Blomen VA, Velds A, Kerkhoven RM, Carette JE, Topaloglu H, Meinecke P, Wessels MW, Lefeber DJ, Whelan SP, van Bokhoven H, Brummelkamp TR, Science 2013 340 479 483 10.1126/science.1233675 23519211
82. A haploid genetic screen identifies the major facilitator domain containing 2A (MFSD2A) transporter as a key mediator in the response to tunicamycin. Reiling JH, Clish CB, Carette JE, Varadarajan M, Brummelkamp TR, Sabatini DM, Proc Natl Acad Sci U S A 2011 108 11756 11765 10.1073/pnas. 1018098108 21677192
83. A Genetic Screen Using the PiggyBac Transposon in Haploid Cells Identifies Parp1 as a Mediator of Olaparib Toxicity. Pettitt SJ, Rehman FL, Bajrami I, Brough R, Wallberg F, Kozarewa I, Fenwick K, Assiotis I, Chen L, Campbell J, Lord CJ, Ashworth A, PLoS One 2013 8 61520 10.1371/journal.pone. 0061520 23634208
84. Combined haploid and insertional mutation screen in the zebrafish. Wiellette E, Grinblat Y, Austen M, Hirsinger E, Amsterdam A, Walker C, Westerfield M, Sive H, Genesis 2004 40 231 240 10.1002/gene.20090 15593329 (Pubitemid 40110708)
85. High-frequency generation of viable mice from engineered bi-maternal embryos. Kawahara M, Wu Q, Takahashi N, Morita S, Yamada K, Ito M, Ferguson-Smith AC, Kono T, Nat Biotechnol 2007 25 1045 1050 10.1038/nbt1331 17704765 (Pubitemid 47517640)
86. Dosage compensation of the active X chromosome in mammals. Nguyen DK, Disteche CM, Nat Genet 2006 38 47 53 10.1038/ng1705 16341221 (Pubitemid 43011881)
87. Mammalian X upregulation is associated with enhanced transcription initiation, RNA half-life, and MOF-mediated H4K16 acetylation. Deng X, Berletch JB, Ma W, Nguyen DK, Hiatt JB, Noble WS, Shendure J, Disteche CM, Dev Cell 2013 25 55 68 10.1016/j.devcel.2013.01.028 23523075
88. Expression reduction in mammalian X chromosome evolution refutes Ohno's hypothesis of dosage compensation. Lin F, Xing K, Zhang J, He X, Proc Natl Acad Sci U S A 2012 109 11752 11757 10.1073/pnas.1201816109 22753487
89. Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Birchler JA, Veitia RA, Proc Natl Acad Sci U S A 2012 109 14746 14753 10.1073/pnas.1207726109 22908297
90. The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics. Levasseur A, Pontarotti P, Biol Direct 2011 6 11 10.1186/1745-6150-6-11 21333002
91. Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Pessia E, Makino T, Bailly-Bechet M, McLysaght A, Marais GA, Proc Natl Acad Sci U S A 2012 109 5346 5351 10.1073/pnas.1116763109 22392987
92. Abnormalities of the inactive X chromosome are a common feature of BRCA1 mutant and sporadic basal-like breast cancer. Ganesan S, Richardson AL, Wang ZC, Iglehart JD, Miron A, Feunteun J, Silver D, Livingston DM, Cold Spring Harb Symp Quant Biol 2005 70 93 97 10.1101/sqb.2005.70.045 16869742 (Pubitemid 44124860)
93. Xist RNA is a potent suppressor of hematologic cancer in mice. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, Scadden DT, Lee JT, Cell 2013 152 727 742 10.1016/j.cell.2013.01.034 23415223
94. Haploid plants produced by centromere-mediated genome elimination. Ravi M, Chan SW, Nature 2010 464 615 618 10.1038/nature08842 20336146
95. Derivation of oocytes from mouse embryonic stem cells. Hubner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF 3rd, Boiani M, Scholer HR, Science 2003 300 1251 1256 10.1126/science.1083452 12730498 (Pubitemid 36618231)
96. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M, Science 2012 338 971 975 10.1126/science.1226889 23042295
97. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M, Cell 2011 146 519 532 10.1016/j.cell.2011.06.052 21820164