Unravelling the evolutionary origins of X chromosome inactivation in mammals: Insights from marsupials and monotremes

Chromosome Research

Volumn 17, Issue 5, 2009, Pages 671-685

  Deakin, Janine E ^a   Chaumeil, Julie ^b   Hore, Timothy A ^a   Marshall Graves, Jennifer A ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dosage compensation; Marsupial; Monotreme; X chromosome inactivation

Indexed keywords

ATR PROTEIN; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1; PROTEIN MSCI; UNCLASSIFIED DRUG;

CHROMATIN STRUCTURE; CPG ISLAND; EPIGENETICS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENOME IMPRINTING; MAMMAL; MARSUPIAL; MONOTREMATE; NONHUMAN; PATERNITY; PHYLOGENETIC TREE; PLATYPUS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SEX CHROMOSOME; X CHROMOSOME INACTIVATION;

ANIMALS; BIOLOGICAL EVOLUTION; EPIGENESIS, GENETIC; MARSUPIALIA; MONOTREMATA; SEX CHROMOSOMES; X CHROMOSOME INACTIVATION;

EUTHERIA; MAMMALIA; METATHERIA; MONOTREMATA;

EID: 70349665249     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-009-9058-6     Document Type: Review

References (100)

1. S Augui GJ Filion S Huart, et al. 2007 Sensing X chromosome pairs before X inactivation via a novel X-pairing region of the Xic Science 318 1632 1636 18063799 10.1126/science.1149420 (Pubitemid 350233663)
2. CP Bacher M Guggiari B Brors, et al. 2006 Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation Nat Cell Biol 8 293 299 16434960 10.1038/ncb1365 (Pubitemid 43336072)
3. OR Bininda-Emonds M Cardillo KE Jones, et al. 2007 The delayed rise of present-day mammals Nature 446 507 512 17392779 10.1038/nature05634 (Pubitemid 46514725)
4. N Brockdorff A Ashworth GF Kay, et al. 1991 Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome Nature 351 329 331 2034279 10.1038/351329a0
5. CJ Brown RG Lafreniere VE Powers, et al. 1991 Localization of the X inactivation centre on the human X chromosome in Xq13 Nature 349 82 84 1985270 10.1038/349082a0
6. L Carrel HF Willard 2005 X-inactivation profile reveals extensive variability in X-linked gene expression in females Nature 434 400 404 15772666 10.1038/nature03479 (Pubitemid 40469185)
7. L Carrel C Park S Tyekucheva, et al. 2006 Genomic environment predicts expression patterns on the human inactive X chromosome PLoS Genet 2 e151 17009873 10.1371/journal.pgen.0020151 (Pubitemid 44504798)
8. J Chaumeil I Okamoto M Guggiari E Heard 2002 Integrated kinetics of X chromosome inactivation in differentiating embryonic stem cells Cytogenet Genome Res 99 75 84 12900548 10.1159/000071577 (Pubitemid 37467827)
9. J Chaumeil P Le Baccon A Wutz E Heard 2006 A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced Genes Dev 20 2223 2237 16912274 10.1101/gad.380906 (Pubitemid 44244524)
10. DE Cohen LS Davidow JA Erwin, et al. 2007 The DXPas34 repeat regulates random and imprinted X inactivation Dev Cell 12 57 71 17199041 10.1016/j.devcel.2006.11.014 (Pubitemid 46002600)
11. DW Cooper 1971 Directed genetic change model for X chromosome inactivation in eutherian mammals Nature 230 292 294 5549404 10.1038/230292a0
12. DW Cooper JL VandeBerg GB Sharman WE Poole 1971 Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation Nat New Biol 230 155 157 5279474 10.1038/230292a0
13. DW Cooper PG Johnston JAM Graves 1993 X-inactivation in marsupials and monotremes Sem Dev Biol 4 117 128 10.1006/sedb.1993.1014
14. LS Davidow M Breen SE Duke, et al. 2007 The search for a marsupial XIC reveals a break with vertebrate synteny Chromosome Res 15 137 146 17333538 10.1007/s10577-007-1121-6 (Pubitemid 46354985)
15. JE Deakin TA Hore E Koina JAM Graves 2008 The status of dosage compensation in the multiple X chromosomes of the platypus PLoS Genet 4 e1000140 18654631 10.1371/journal.pgen.1000140
16. JE Deakin E Koina PD Waters, et al. 2008 Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals Chromosome Res 16 1159 1175 18987984 10.1007/s10577-008-1266-y
17. SV Dindot KC Kent B Evers, et al. 2004 Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine Mamm Genome 15 966 974 15599555 10.1007/s00335-004-2407-z (Pubitemid 40100902)
18. L Duret C Chureau S Samain J Weissenbach P Avner 2006 The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene Science 312 1653 1655 16778056 10.1126/science.1126316 (Pubitemid 43902664)
19. EA Elisaphenko NN Kolesnikov AI Shevchenko, et al. 2008 A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements PLoS ONE 3 e2521 18575625 10.1371/journal.pone.0002521
20. H Ellegren L Hultin-Rosenberg B Brunstrom, et al. 2007 Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes BMC Biol 5 40 17883843 10.1186/1741-7007-5-40 (Pubitemid 350226887)
21. A Gimelbrant JN Hutchinson BR Thompson A Chess 2007 Widespread monoallelic expression on human autosomes Science 318 1136 1140 18006746 10.1126/science.1148910 (Pubitemid 350134896)
22. JAM Graves 1967 DNA synthesis in chromosomes of cultured leucocytes from two marsupial species Exp Cell Res 46 37 57 6025285 10.1016/0014-4827(67)90407-7
23. JAM Graves 1982 5-azacytidine-induced re-expression of alleles on the inactive X chromosome in a hybrid mouse cell line Exp Cell Res 141 99 105 6180921 10.1016/0014-4827(82)90072-6 (Pubitemid 13219186)
24. JAM Graves 1995 The evolution of mammalian sex chromosomes and the origin of sex determining genes Philos Trans R Soc Lond B Biol Sci 350 305 311 8570696 10.1098/rstb.1995.0166 discussion 311-2
25. JAM Graves 2008 Weird animal genomes and the evolution of vertebrate sex and sex chromosomes Annu Rev Genet 42 565 586 10.1146/annurev.genet.42.110807. 091714
26. JAM Graves GW Dawson 1988 The relationship between position and expression of genes on the kangaroo X chromosome suggests a tissue-specific spread of inactivation from a single control site Genet Res 51 103 109 3410313 10.1017/S0016672300024113
27. JAM Graves SM Gartler 1986 Mammalian X chromosome inactivation: testing the hypothesis of transcriptional control Somat Cell Mol Genet 12 275 280 3459256 10.1007/BF01570786
28. JAM Graves E Koina N Sankovic 2006 How the gene content of human sex chromosomes evolved Curr Opin Genet Dev 16 219 224 16650758 10.1016/j.gde.2006. 04.007
29. F Grützner J Deakin W Rens N El-Mogharbel JAM Graves 2003 The monotreme genome: a patchwork of reptile, mammal and unique features? Comp Biochem Physiol A Mol Integr Physiol 136 867 881 14667850 10.1016/j.cbpb.2003. 09.014 (Pubitemid 37510335)
30. F Grützner W Rens E Tsend-Ayush, et al. 2004 In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes Nature 432 913 917 15502814 10.1038/nature03021 (Pubitemid 40037154)
31. DL Hayman PG Martin 1965 Sex chromosome mosaicism in the marsupial genera Isoodon and Perameles Genetics 52 1201 1206 5882195
32. Hayman DL, Martin PG (1974) Mammalia I: Monotremata and Marsupialia. In: John B (ed) Animal Cytogenetics 4: Chordata. Gebruder Borntraeger, Berlin/Stuttgart, pp 1-110
33. E Heard 2005 Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome Curr Opin Genet Dev 15 482 489 16107314 10.1016/j.gde.2005.08.009 (Pubitemid 41262403)
34. E Heard C Rougeulle D Arnaud, et al. 2001 Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation Cell 107 727 738 11747809 10.1016/S0092-8674(01)00598-0 (Pubitemid 34033666)
35. TA Hore E Koina JAM Graves 2007 The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals Chromosome Res 15 147 161 17333539 10.1007/s10577-007-1119-0 (Pubitemid 46357427)
36. JL Hornecker PB Samollow ES Robinson JL Vandeberg JR McCarrey 2007 Meiotic sex chromosome inactivation in the marsupial Monodelphis domestica Genesis 45 696 708 17987663 10.1002/dvg.20345
37. Human Genome Sequencing Center at Baylor College of Medicine (2009) Internet references. Retrieved from http://www.hgsc.bcm.tmc.edu/projects/wallaby 28/2/2009.
38. KD Huynh JT Lee 2003 Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos Nature 426 857 862 14661031 10.1038/nature02222 (Pubitemid 38056873)
39. KD Huynh JT Lee 2005 X-chromosome inactivation: a hypothesis linking ontogeny and phylogeny Nat Rev Genet 6 410 418 15818384 10.1038/nrg1604 (Pubitemid 40577184)
40. Y Itoh E Melamed X Yang, et al. 2007 Dosage compensation is less effective in birds than in mammals J Biol 6 2 17352797 10.1186/jbiol53 (Pubitemid 46474683)
41. PG Johnston ES Robinson 1987 X chromosome inactivation in female embryos of a marsupial mouse (Antechinus stuartii) Chromosoma 95 419 423 2824142 10.1007/BF00333993
42. PG Johnston CM Watson M Adams DJ Paull 2002 Sex chromosome elimination, X chromosome inactivation and reactivation in the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae) Cytogenet Genome Res 99 119 124 12900554 10.1159/000071583 (Pubitemid 37467833)
43. CM Johnston FL Lovell DA Leongamornlert, et al. 2008 Large-scale population study of human cell lines indicates that dosage compensation is virtually complete PLoS Genet 4 e9 18208332 10.1371/journal.pgen.0040009 (Pubitemid 351230877)
44. DC Kaslow BR Migeon 1987 DNA methylation stabilizes X chromosome inactivation in eutherians but not in marsupials: evidence for multistep maintenance of mammalian X dosage compensation Proc Natl Acad Sci U S A 84 6210 6214 3476942 10.1073/pnas.84.17.6210
45. AM Keohane LP O'Neill ND Belyaev JS Lavender BM Turner 1996 X-Inactivation and histone H4 acetylation in embryonic stem cells Dev Biol 180 618 630 8954732 10.1006/dbio.1996.0333 (Pubitemid 27037368)
46. AM Keohane JS Lavender LP O'Neill BM Turner 1998 Histone acetylation and X inactivation Dev Genet 22 65 73 9499581 10.1002/(SICI)1520-6408(1998)22: 1<65::AID-DVG7>3.0.CO;2-5 (Pubitemid 28114776)
47. JAW Kirsch FJ Lapointe MS Springer 1997 DNA-hybridisation studies of marsupials and their implications for metatherian classification Australian Journal of Zoology 45 211 280 10.1071/ZO96030
48. A Kohlmaier F Savarese M Lachner, et al. 2004 A chromosomal memory triggered by Xist regulates histone methylation in X inactivation PLoS Biol 2 E171 15252442 10.1371/journal.pbio.0020171 (Pubitemid 39234412)
49. E Koina MJ Wakefield C Walcher, et al. 2005 Isolation, X location and activity of the marsupial homologue of SLC16A2, an XIST-flanking gene in eutherian mammals Chromosome Res 13 687 698 16235118 10.1007/s10577-005-1006-5 (Pubitemid 41476505)
50. Koina E, Chaumeil J, Greaves IK, Tremethick DJ, Graves JAM (2009) Specific patterns of histone marks accompany X chromosome inactivation in a marsupial. Chromosome Res
51. BR Lawton BR Carone CJ Obergfell, et al. 2008 Genomic imprinting of IGF2 in marsupials is methylation dependent BMC Genomics 9 205 18454865 10.1186/1471-2164-9-205 (Pubitemid 351712567)
52. E Lifschytz DL Lindsley 1972 The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation) Proc Natl Acad Sci U S A 69 182 186 4621547 10.1073/pnas.69.1.182
53. LF Lock N Takagi GR Martin 1987 Methylation of the Hprt gene on the inactive X occurs after chromosome inactivation Cell 48 39 46 3791414 10.1016/0092-8674(87)90353-9
54. DA Loebel PG Johnston 1993 Analysis of DNase 1 sensitivity and methylation of active and inactive X chromosomes of kangaroos (Macropus robustus) by in situ nick translation Chromosoma 102 81 87 8381740 10.1007/BF00356024 (Pubitemid 23040890)
55. DA Loebel PG Johnston 1996 Methylation analysis of a marsupial X-linked CpG island by bisulfite genomic sequencing Genome Res 6 114 123 8919690 10.1101/gr.6.2.114
56. MF Lyon 1961 Gene action in the X-chromosome of the mouse (Mus musculus L.) Nature 190 372 373 13764598 10.1038/190372a0
57. MF Lyon 1998 X-chromosome inactivation: a repeat hypothesis Cytogenet Cell Genet 80 133 137 9678347 10.1159/000014969
58. W Mak TB Nesterova M de Napoles, et al. 2004 Reactivation of the paternal X chromosome in early mouse embryos Science 303 666 669 14752160 10.1126/science.1092674 (Pubitemid 38141631)
59. JE Mank H Ellegren 2009 All dosage compensation is local: Gene-by-gene regulation of sex-biased expression on the chicken Z chromosome Heredity 102 312 320 18985062 10.1038/hdy.2008.116
60. Y Marahrens B Panning J Dausman W Strauss R Jaenisch 1997 Xist-deficient mice are defective in dosage compensation but not spermatogenesis Genes Dev 11 156 166 9009199 10.1101/gad.11.2.156
61. JR McCarrey C Watson J Atencio, et al. 2002 X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse Genesis 34 257 266 12434336 10.1002/gene.10163 (Pubitemid 35470700)
62. LM McKay JM Wrigley JA Graves 1987 Evolution of mammalian X-chromosome inactivation: sex chromatin in monotremes and marsupials Aust J Biol Sci 40 397 404 3453040
63. E Melamed AP Arnold 2007 Regional differences in dosage compensation on the chicken Z chromosome Genome Biol 8 R202 17900367 10.1186/gb-2007-8-9-r202 (Pubitemid 351895463)
64. TS Mikkelsen MJ Wakefield B Aken, et al. 2007 Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences Nature 447 167 177 17495919 10.1038/nature05805 (Pubitemid 46763085)
65. S Mlynarczyk-Evans M Royce-Tolland MK Alexander, et al. 2006 X chromosomes alternate between two states prior to random X-inactivation PLoS Biol 4 e159 16669701 10.1371/journal.pbio.0040159 (Pubitemid 43909450)
66. T Mohandas RS Sparkes LJ Shapiro 1981 Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation Science 211 393 396 6164095 10.1126/science.6164095
67. V Monesi 1965 Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse Chromosoma 17 11 21 5833946 10.1007/BF00285153
68. K Monkhorst I Jonkers E Rentmeester F Grosveld J Gribnau 2008 X inactivation counting and choice is a stochastic process: evidence for involvement of an X-linked activator Cell 132 410 421 18267073 10.1016/j.cell.2007.12.036 (Pubitemid 351191999)
69. CE Murtagh 1977 A unique cytogenetic system in monotremes Chromosoma 65 37 57 10.1007/BF00293129
70. SH Namekawa JL VandeBerg JR McCarrey JT Lee 2007 Sex chromosome silencing in the marsupial male germ line Proc Natl Acad Sci U S A 104 9730 9735 17535928 10.1073/pnas.0700323104 (Pubitemid 47175335)
71. DP Norris N Brockdorff S Rastan 1991 Methylation status of CpG-rich islands on active and inactive mouse X chromosomes Mamm Genome 1 78 83 1799791 10.1007/BF02443782
72. R Ohlsson A Paldi JAM Graves 2001 Did genomic imprinting and X chromosome inactivation arise from stochastic expression? Trends Genet 17 136 141 11226606 10.1016/S0168-9525(00)02211-3 (Pubitemid 32171948)
73. Ohno S (1967) Sex Chromosomes and Sex Linked Genes. Springer, Berlin
74. I Okamoto AP Otte CD Allis D Reinberg E Heard 2004 Epigenetic dynamics of imprinted X inactivation during early mouse development Science 303 644 649 14671313 10.1126/science.1092727 (Pubitemid 38141624)
75. I Okamoto D Arnaud P Le Baccon, et al. 2005 Evidence for de novo imprinted X-chromosome inactivation independent of meiotic inactivation in mice Nature 438 369 373 16227973 10.1038/nature04155 (Pubitemid 41643954)
76. Patrat C, Okamoto I, Diabangouaya P et al. (2009) Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proc Natl Acad Sci U S A
77. W Rens F Grutzner PC O'Brien, et al. 2004 Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution Proc Natl Acad Sci U S A 101 16257 16261 15534209 10.1073/pnas.0405702101 (Pubitemid 39552832)
78. W Rens PC O'Brien F Grützner, et al. 2007 The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z Genome Biol 8 R243 18021405 10.1186/gb-2007-8- 11-r243 (Pubitemid 351917501)
79. BJ Richardson AB Czuppon GB Sharman 1971 Inheritance of glucose-6-phosphate dehydrogenase variation in kangaroos Nat New Biol 230 154 155 5279473
80. T Sado M Okano E Li H Sasaki 2004 De novo DNA methylation is dispensable for the initiation and propagation of X chromosome inactivation Development 131 975 982 14973270 10.1242/dev.00995 (Pubitemid 38380452)
81. GB Sharman 1971 Late DNA replication in the paternally derived X chromosome of female kangaroos Nature 230 231 232 4926712 10.1038/230231a0
82. AI Shevchenko IS Zakharova EA Elisaphenko, et al. 2007 Genes flanking Xist in mouse and human are separated on the X chromosome in American marsupials Chromosome Res 15 127 136 17333537 10.1007/s10577-006-1115-9 (Pubitemid 46354982)
83. J Silva W Mak I Zvetkova, et al. 2003 Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes Dev Cell 4 481 495 12689588 10.1016/S1534-5807(03)00068-6 (Pubitemid 36437556)
84. N Takagi M Sasaki 1975 Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse Nature 256 640 642 1152998 10.1038/256640a0
85. P Temple-Smith T Grant 2001 Uncertain breeding: a short history of reproduction in monotremes Reprod Fertil Dev 13 487 497 11999298 10.1071/RD01110
86. M Teranishi Y Shimada T Hori, et al. 2001 Transcripts of the MHM region on the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the DMRT1 locus Chromosome Res 9 147 165 11321370 10.1023/A:1009235120741 (Pubitemid 32269987)
87. JM Turner SK Mahadevaiah DJ Elliott, et al. 2002 Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist J Cell Sci 115 4097 4105 12356914 10.1242/jcs.00111 (Pubitemid 35446806)
88. JM Turner O Aprelikova X Xu, et al. 2004 BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation Curr Biol 14 2135 2142 15589157 10.1016/j.cub.2004.11.032 (Pubitemid 39623196)
89. F Veyrunes PD Waters P Miethke, et al. 2008 Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes Genome Res 18 965 973 18463302 10.1101/gr.7101908 (Pubitemid 351793069)
90. N Wake N Takagi M Sasaki 1976 Non-random inactivation of X chromosome in the rat yolk sac Nature 262 580 581 958416 10.1038/262580a0
91. MJ Wakefield AM Keohane BM Turner JAM Graves 1997 Histone underacetylation is an ancient component of mammalian X chromosome inactivation Proc Natl Acad Sci U S A 94 9665 9668 9275180 10.1073/pnas.94.18.9665 (Pubitemid 27408119)
92. WC Warren LW Hillier JAM Graves, et al. 2008 Genome analysis of the platypus reveals unique signatures of evolution Nature 453 175 183 18464734 10.1038/nature06936 (Pubitemid 351667983)
93. PD Waters ML Delbridge JE Deakin, et al. 2005 Autosomal location of genes from the conserved mammalian X in the platypus (Ornithorhynchus anatinus): implications for mammalian sex chromosome evolution Chromosome Res 13 401 410 15973504 10.1007/s10577-005-0978-5 (Pubitemid 40853834)
94. D Watson AS Jacombs DA Loebel ES Robinson PG Johnston 2000 Single nucleotide primer extension (SNuPE) analysis of the G6PD gene in somatic cells and oocytes of a kangaroo (Macropus robustus) Genet Res 75 269 274 10893863 10.1017/S0016672300004523 (Pubitemid 30398382)
95. JR Weidman SK Murphy CM Nolan FS Dietrich RL Jirtle 2004 Phylogenetic footprint analysis of IGF2 in extant mammals Genome Res 14 1726 1732 15342558 10.1101/gr.2774804 (Pubitemid 39276430)
96. JD West WI Frels VM Chapman VE Papaioannou 1977 Preferential expression of the maternally derived X chromosome in the mouse yolk sac Cell 12 873 882 597862 10.1016/0092-8674(77)90151-9
97. JM Wrigley JAM Graves 1988 Sex chromosome homology and incomplete, tissue-specific X-inactivation suggest that monotremes represent an intermediate stage of mammalian sex chromosome evolution J Hered 79 115 118 3403957
98. N Xu CL Tsai JT Lee 2006 Transient homologous chromosome pairing marks the onset of X inactivation Science 311 1149 1152 16424298 10.1126/science. 1122984 (Pubitemid 43305953)
99. SM Zeng J Yankowitz 2003 X-inactivation patterns in human embryonic and extra-embryonic tissues Placenta 24 270 275 12566254 10.1053/plac.2002.0889 (Pubitemid 37184722)
100. KR Zenger LM McKenzie DW Cooper 2002 The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii) Genetics 162 321 330 12242243