X chromosome inactivation, differentiation, and DNA methylation revisited, with a tribute to Susumu Ohno

Cytogenetic and Genome Research

Volumn 99, Issue 1-4, 2002, Pages 17-24

  Riggs, A D ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REPETITIVE DNA; SPACER DNA;

AUTOSOMAL INHERITANCE; CELL SPECIFICITY; CHROMATIN STRUCTURE; DEVELOPMENTAL GENETICS; DIFFERENTIATION; DNA METHYLATION; GENE CONTROL; GENE DUPLICATION; HUMAN; LABORATORY; MOLECULAR MODEL; NONHUMAN; POPULATION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; REVIEW; STOCHASTIC MODEL; X CHROMOSOME INACTIVATION;

MAMMALIA;

EID: 0344530960     PISSN: 14248581     EISSN: None     Source Type: Journal    
DOI: 10.1159/000071569     Document Type: Review

References (98)

1. Bachman KE, Rountree MR, Baylin SB: Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J biol Chem 276:32282-32287 (2001).
2. Bailey JA, Carrel L, Chakravarti A, Eichler EE: Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc natl Acad Sci, USA 97:6634-6639 (2000).
3. Bart ML, Bertram EG: A morphological distinction between neurons of the male and female. Nature 163:676-677 (1949).
4. Bell AC, Felsenfeld G: Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482-485 (2000).
5. Bestor TH: The DNA methyltransferases of mammals. Hum molec Genet 9:2395-2402 (2000).
6. Bird A: Does DNA methylation control transposition of selfish elements in the germline? Trends Genet 13:469-470 (1997).
7. Bird A: DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21 (2002).
8. Bird AP: Use of restriction enzymes to study eukaryotic DNA methylation. II. The symmetry of methylated sites supports semi-conservative copying of the methylation pattern. J molec Biol 118:49-60 (1978).
9. Boggs BA, Cheung P, Heard E, Spector DL, Chinault AC, Allis CD: Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nature Genet 30:73-76 (2002).
10. Brown CJ, Hendrich BD, Rupert JL, Lafrenière RG, Xing Y, Lawrence J, Willard HF: The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71:527-542 (1992).
11. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y: Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039-1043 (2002).
12. Chao W, Huynh KD, Spencer RJ, Davidow LS, Lee JT: CTCF, a candidate trans-acting factor for X-inactivation choice. Science 295:345-347 (2002).
13. Chen C, Yang MC, Yang TP: Evidence that silencing of the HPRT promoter by DNA methylation is mediated by critical CpG sites. J biol Chem 276:320-328 (2001).
14. Chong S, Riggs AD, Bonifer C: The chicken lysozyme chromatin domain contains a second, widely expressed gene. Nucl Acids Res 30:463-467 (2002).
15. Clark S J, Melki J: DNA methylation and gene silencing in cancer: which is the guilty party? Oncogene 21:5380-5387 (2002).
16. De Smet C, Lurquin C, Lethé B, Martelange V, Boon T: DNA methylation is the primary silencing mechanism for a set of germ line- and tumor-specific genes with a CpG-rich promoter. Mol Cell Biol 19:7327-7335 (1999).
17. Dernburg AF, Karpen GH: A chromosome RNAissance. Cell 111:159-162 (2002).
18. Ehrlich M, Ehrlich KC: Effect of DNA methylation on the binding of vertebrate and plant proteins to DNA, in Jost JP, Saluz HP (eds): DNA Methylation: Molecular Biology and Biological Significance, pp 145-168 (Birkhauser Verlag, Berlin 1993).
19. Epplen JT, Sutou S, McCarrey JR, Ohno S: Is sex-specifically arranged repetitive DNA involved in primary sex determination of vertebrates? Prog clin Biol Res 103(Pt A):317-326 (1982).
20. Feil R, Walter J, Allen ND, Reik W: Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development 120: 2933-2943 (1994).
21. Futscher BW, Oshiro MM, Wozniak R J, Holtan N, Hanigan CL, Duan H, Domann FE: Role for DNA methylation in the control of cell type specific maspin expression. Nature Genet 31:175-179 (2002).
22. Gartier SM, Goldman MA: Reactivation of inactive X-linked genes. Dev Genet 15:504-514 (1994).
23. Gilliland G, Perrin S, Bunn HF: Quantitative amplification of mRNA using polymerase chain reaction. J Cell Biochem 13E:270 (1989).
24. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI: Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237 (2002).
25. Han L, Lin IG, Hsieh CL: Protein binding protects sites on stable episomes and in the chromosome from de novo methylation. Mol Cell Biol 21:3416-3424 (2001).
26. Hansen RS, Wijmenga C, Luo P, Stanek AM, Canfield TK, Weemaes CMR, Gartler SM: The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc natl Acad Sci, USA 96:14412-14417 (1999).
27. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM: CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486-489 (2000).
28. Heard E, Clerc P, Avner P: X-chromosome inactivation in mammals. A Rev Genet 31:571-610 (1997).
29. Hershkovitz M, Riggs AD: Metaphase chromosome analysis by ligation-mediated PCR: heritable chromatin structure and a comparison of active and inactive X chromosomes. Proc natl Acad Sci, USA 92:2379-2383 (1995).
30. Holliday R: DNA methylation in eukaryotes: 20 years on, in Russo VEA, Martienssen RA, Riggs AD (eds): Epigenetic Mechanisms of Gene Regulation, pp 5-27 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1996).
31. Holliday R, Pugh JE: DNA modification mechanisms and gene activity during development. Science 187:226-232 (1975).
32. Hsieh CL: Evidence that protein binding specifies sites of DNA demethylation. Mol Cell Biol 19:46-56 (1999).
33. Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, Dausman J, Lee P, Wilson C, Lander E, Jaenisch R: Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nature Genet 27:31-39 (2001).
34. Jenuwein T, Allis CD: Translating the histone code. Science 293: 1074-1080 (2001).
35. Jeppesen P, Turner BM: The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74:281-289 (1993).
36. Jones PA: Gene activation by 5-azacytidine, in Razin A, Cedar H, Riggs AD (eds): DNA Methylation: Biochemistry and Biological Significance, pp 165-188 (Springer-Verlag, New York 1984).
37. Jones PA: DNA methylation and cancer. Oncogene 21:5358-5360 (2002).
38. Jones PL, Veenstra GJC, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP: Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nature Genet 19:187-191 (1998).
39. Kafri T, Ariel M, Brandeis M, Shemer R, Urven L, McCarrey J, Cedar H, Razin A: Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev 6:705-714 (1992).
40. Keohane AM, O'Neill L P, Belyaev ND, Lavender JS, Turner BM: X-inactivation and histone H4 acetylation in embryonic stem cells. Dev Biol 180:618-630 (1996).
41. Kondo T, Bobek MP, Kuick R, Lamb B, Zhu X, Narayan A, Bourc'his D, Viegas-Péquignot E, Ehrlich M, Hanash SM: Whole-genome methylation scan in ICF syndrome: hypomethylation of non-satellite DNA repeats D4Z4 and NBL2. Hum molec Genet 9:597-604 (2000).
42. Kuroda Y, Arai N, Arita M, Teranishi M, Hori T, Harata M, Mizuno S: Absence of Z-chromosome inactivation for five genes in male chickens. Chrom Res 9:457-468 (2001).
43. Lee JT, Davidow LS, Warshawsky D: Tsix, a gene antisense to Xist at the X-inactivation centre. Nature Genet 21:400-404 (1999).
44. Leonhardt H, Page AW, Weier HU, Bestor TH: A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71:865-873 (1992).
45. Li E, Beard C, Jaenisch R: Role for DNA methylation in genomic imprinting. Nature 366:362-365 (1993).
46. Li E, Bestor TH, Jaenisch R: Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915-926 (1992).
47. Lock LF, Takagi N, Martin GR: Methylation of the Hprt gene on the inactive X occurs after chromosome inactivation. Cell 48:39-46 (1987).
48. Lyon MF: Gene action in the X-chromosome of the mouse. Nature 190: 372-373 (1961).
49. Lyon MF: X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 80:133-137 (1998).
50. Mann JR, Szabo PE, Reed MR, Singer-Sam J: Methylated DNA sequences in genomic imprinting. Crit Rev eukaryot Gene Express 10:241-257 (2000).
51. McQueen HA, McBride D, Miele G, Bird AP, Clinton M: Dosage compensation in birds. Curr Biol 11:253-257 (2001).
52. Mermoud JE, Popova B, Peters AH, Jenuwein T, Brockdorff N: Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr Biol 12:247-251 (2002).
53. Monk M, Boubelik M, Lehnert S: Temporal and regional changes in DNA methylation in the embryonic, extraembryonic, and germ-cell lineages during mouse embryo development. Development 99:371-382 (1987).
54. Nan XS, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A: Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389 (1998).
55. Ohno S: Sex Chromosomes and Sex-linked Genes (Springer-Verlag, Heidelberg 1967).
56. Ohno S: Evolution of sex chromosomes in mammals. A Rev Genet 3:495-524 (1969).
57. Ohno S: Evolution by Gene Duplication (Springer-Verlag, Berlin 1970).
58. Ohno S: So much "junk" DNA in our genome. Brookhaven Symp Biol 23:366-370 (1972).
59. Ohno S, Stenius C, Christian LC, Harris C: Synchronous activation of both parental alleles at the 6-PGD locus of Japanese quail embryos. Biochem Genet 2:197-204 (1968).
60. Okano M, Bell DW, Haber DA, Li E: DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247-257 (1999).
61. Okano M, Xie SP, Li E: Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nature Genet 19:219-220 (1998).
62. Peters AH, Mermoud JE, O'Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T: Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nature Genet 30:77-80 (2002).
63. Pfeifer GP, Steigerwald SD, Hansen RS, Gartier SM, Riggs AD: Polymerase chain reaction-aided genomic sequencing of an X chromosome-linked CpG island: methylation patterns suggest clonal inheritance, CpG site autonomy, and an explanation of activity state stability. Proc natl Acad Sci, USA 87:8252-8256 (1990a).
64. Pfeifer GP, Steigerwald SD, Mueller PR, Wold B, Riggs AD: Genomic sequencing and methylation analysis by ligation mediated PCR. Science 246:810-813 (1989).
65. Pfeifer GP, Tanguay RL, Steigerwald SD, Riggs AD: In vivo footprint and methylation analysis by PCR-aided genomic sequencing: comparison of active and inactive X chromosomal DNA at the CpG island and promoter of human PGK-1. Genes Dev 4:1277-1287 (1990b).
66. Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R: Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc natl Acad Sci, USA 97:5237-5242 (2000).
67. Razin A, Riggs AD: DNA methylation and gene function. Science 210: 604-610 (1980).
68. Riggs AD: X inactivation, differentiation, and DNA methylation. Cytogenet Cell Genet 14:9-25 (1975).
69. Riggs AD: DNA methylation and late replication probably aid cell memory, and type I DNA reeling could aid chromosome folding and enhancer function. Phil Trans roy Soc Lond B Biol Sci 326:285-297 (1990).
70. Riggs AD, Bourgeois S: On the assay, isolation and characterization of the lac repressor. J molec Biol 34:361-364 (1968).
71. Riggs AD, Lin S, Wells RD: Lac repressor binding to synthetic DNAs of defined nucleotide sequence. Proc natl Acad Sci, USA 69:761-764 (1972).
72. Riggs AD, Pfeifer GP: X-chromosome inactivation and cell memory. Trends Genet 8:169-174 (1992).
73. Riggs AD, Porter TN: Overview of epigenetic mechanisms, in Russo E, Martienssen R, Riggs AD (eds): Epigenetics Mechanisms of Gene Regulation, pp 29-45 (Cold Spring Harbor Press, Cold Spring Harbor 1996).
74. Riggs AD, Singer SJ, Keith DH: Methylation of the PGK promoter region and an enhancer waystation model for X chromosome inactivation, in Cantoni GL, Razin A (eds): Biochemistry and Biology of DNA Methylation, pp 211-222 (Alan R Liss, New York 1985).
75. Riggs AD, Xiong Z, Wang L, LeBon JM: Methylation dynamics, epigenetic fidelity and X chromosome structure. Novartis Found Symp 214:214-225 (1998).
76. Rodin SN, Riggs AD: Epigenetic silencing may aid evolution by gene duplication. J molec Evol (2003, in press).
77. Rountree MR, Bachman KE, Baylin SB: DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nature Genet 25:269-277 (2000).
78. Russo E, Martienssen R, Riggs AD: Epigenetics Mechanisms of Gene Regulation (Cold Spring Harbor Press, Cold Spring Harbor 1996).
79. Singer J, Roberts-Ems J, Luthardt FW, Riggs AD: Methylation of DNA in mouse early embryos, teratocarcinoma cells and adult tissues of mouse and rabbit. Nucl Acids Res 7:2369-2385 (1979).
80. Singer-Sam J, Grant M, LeBon JM, Okuyama K, Chapman V, Monk M, Riggs AD: Use of a HpalI-polymerase chain reaction assay to study DNA methylation in the Pgk-1 CpG island of mouse embryos at the time of X-chromosome inactivation. Mol Cell Biol 10:4987-4989 (1990a).
81. Singer-Sam J, LeBon JM, Tanguay RL, Riggs AD: A quantitative HpaII-PCR assay to measure methylation of DNA from a small number of cells. Nucl Acids Res 18:687 (1990b).
82. Singer-Sam J, Robinson M, Rossi JJ, Tanguay RL, Simon M, Riggs AD: Use of PCR for quantitative measurement of mRNA levels of X-linked genes during spermatogenesis and for a micro assay of DNA methylation. J Cell Biochem 13E: 306 (1989).
83. Smit AF: Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curt Opin Genet Dev 9:657-663 (1999).
84. Smit AF, Riggs AD: Tiggers and DNA transposon fossils in the human genome. Proc natl Acad Sci, USA 93:1443-1448 (1996).
85. Song JZ, Stirzaker C, Harrison J, Melki JR, Clark S J: Hypermethylation trigger of the glutathione-S-transferase gene (GSTP1) in prostate cancer cells. Oncogene 21:1048-1061 (2002).
86. Stoger R, Kajimura TM, Brown WT, Laird CD: Epigenetic variation illustrated by DNA methylation patterns of the fragile-X gene FMR1. Hum molec Genet 6:1791-1801 (1997).
87. Szabo P, Tang SH, Rentsendorj A, Pfeifer GP, Mann JR: Maternal-specific footprints at putative CTCF sites in the H19 imprinting control region give evidence for insulator function. Curr Biol 10:607-610 (2000).
88. Tamaru H, Selker EU: A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277-283 (2001).
89. Tommasi S, LeBon JM, Riggs AD, Singer-Sam J: Methylation analysis by genomic sequencing of 5′ region of mouse Pgk-1 gene and a cautionary note concerning the method. Somat Cell molec Genet 19:529-541 (1993).
90. Vertino PM, Sekowski JA, Coll JM, Applegren N, Han S, Hickey RJ, Malkas LH: DNMT1 is a component of a multiprotein DNA replication complex. Cell Cycle (2002, in press).
91. Volpe TA, Kidnet C, Hall IM, Teng G, Grewal SI, Martienssen RA: Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-1837 (2002).
92. Walsh CP, Bestor TH: Cytosine methylation and mammalian development. Genes Dev 13:26-34 (1999).
93. Wang J, Mager J, Chen Y, Schneider E, Cross JC, Nagy A, Magnuson T: Imprinted X inactivation maintained by a mouse Polycomb group gene. Nature Genet 28:371-375 (2001).
94. Wolffe AP, Matzke MA: Epigenetics: regulation through repression. Science 286:481-486 (1999).
95. Wutz A, Jaenisch R: A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5:695-705 (2000).
96. Wutz A, Rasmussen TP, Jaenisch R: Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nature Genet 30:167-174 (2002).
97. Yoder JA, Walsh CP, Bestor TH: Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335-340 (1997).
98. Zhu B, Benjamin D, Zheng Y, Angliker H, Thiry S, Siegmann M, Jost JP: Overexpression of 5-methylcytosine DNA glycosylase in human embryonic kidney cells EcR293 demethylates the promoter of a hormone-regulated reporter gene. Proc natl Acad Sci, USA 98:5031-5036 (2001).