The Inheritance of Epigenetic Defects
10.1126/science.3310230
Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

Evidence from many sources shows that the control of gene expression in higher organisms is related to the methylation of cytosine in DNA, and that the pattern of methylation is inherited. Loss of methylation, which can result from DNA damage, will lead to heritable abnormalities in gene expression, and these may be important in oncogenesis and aging. Transformed permanent lines often lose gene activity through de novo methylation. It is proposed that epigenetic defects in germline cells due to loss of methylation can be repaired by recombination at meiosis but that some are transmitted to offspring.

Bibliography

Holliday, R. (1987). The Inheritance of Epigenetic Defects. Science, 238(4824), 163–170.

Authors 1
  1. Robin Holliday (first)
References 159 Referenced 835
  1. ADAMS RLP SPRINGER SERIES MOL (1985).
  2. ARLETT, C.F., BASIC LIFE SCI 23: 249 (1983). / BASIC LIFE SCI (1983)
  3. BAKER, R.M., BANBURY REPORT 2: 237 (1979). / BANBURY REPORT (1979)
  4. BARSKI, G, J NATL CANCER I 30: 869 (1963). / J NATL CANCER I (1963)
  5. BELL G MASTERPIECE NATURE E (1982).
  6. 10.1038/321209a0
  7. BRINK, R.A., PARAMUTATION, ANNUAL REVIEW OF GENETICS 7: 129 (1973). (10.1146/annurev.ge.07.120173.001021) / ANNUAL REVIEW OF GENETICS (1973)
  8. BURNET F.M. INTRINSIC MUTAGENESI (1974). (10.1007/978-94-011-6606-5)
  9. BUSSLINGER, M, DNA METHYLATION AND THE REGULATION OF GLOBIN GENE-EXPRESSION, CELL 34: 197 (1983). (10.1016/0092-8674(83)90150-2) / CELL (1983)
  10. CARR, B.I., THE TUMORIGENICITY OF 5-AZACYTIDINE IN THE MALE FISCHER RAT, CARCINOGENESIS 5: 1583 (1984). (10.1093/carcin/5.12.1583) / CARCINOGENESIS (1984)
  11. CATCHESIDE, DEA, A RESTRICTION AND MODIFICATION MODEL FOR THE INITIATION AND CONTROL OF RECOMBINATION IN NEUROSPORA, GENETICAL RESEARCH 47: 157 (1986). (10.1017/S0016672300023077) / GENETICAL RESEARCH (1986)
  12. CATTANACH, B.M., POSITION EFFECT VARIEGATION IN MOUSE, GENETICAL RESEARCH 23: 291 (1974). (10.1017/S0016672300014932) / GENETICAL RESEARCH (1974)
  13. CATTANACH, B.M., PARENTAL ORIGIN EFFECTS IN MICE, JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY 97: 137 (1986). / JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY (1986)
  14. CATTANACH, B.M., DIFFERENTIAL ACTIVITY OF MATERNALLY AND PATERNALLY DERIVED CHROMOSOME REGIONS IN MICE, NATURE 315: 496 (1985). (10.1038/315496a0) / NATURE (1985)
  15. CHANDLER, V.L., DNA MODIFICATION OF A MAIZE TRANSPOSABLE ELEMENT CORRELATES WITH LOSS OF ACTIVITY, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 1767 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)
  16. CHAPMAN, V.M., EVIDENCE FOR DNA MODIFICATION IN THE MAINTENANCE OF X-CHROMOSOME INACTIVATION OF ADULT-MOUSE TISSUES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 5357 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
  17. CHOMET, P.S., INACTIVATION OF THE MAIZE TRANSPOSABLE ELEMENT ACTIVATOR (AC) IS ASSOCIATED WITH ITS DNA MODIFICATION, EMBO JOURNAL 6: 295 (1987). (10.1002/j.1460-2075.1987.tb04753.x) / EMBO JOURNAL (1987)
  18. CHRISTMAN, J.K., FORMATION OF HIGHLY STABLE COMPLEXES BETWEEN 5-AZACYTOSINE-SUBSTITUTED DNA AND SPECIFIC NON-HISTONE NUCLEAR PROTEINS - IMPLICATIONS FOR 5-AZACYTIDINE-MEDIATED EFFECTS ON DNA METHYLATION AND GENE-EXPRESSION, JOURNAL OF BIOLOGICAL CHEMISTRY 260: 4059 (1985). (10.1016/S0021-9258(18)89231-6) / JOURNAL OF BIOLOGICAL CHEMISTRY (1985)
  19. CHRISTY, B, EXPRESSION OF TRANSFERRED THYMIDINE KINASE GENES IS CONTROLLED BY METHYLATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 6299 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
  20. 10.1126/science.6175023
  21. COLE, J, A COMPARISON OF THE AGAR CLONING AND MICROTITRATION TECHNIQUES FOR ASSAYING CELL-SURVIVAL AND MUTATION FREQUENCY IN L5178Y MOUSE LYMPHOMA-CELLS, MUTATION RESEARCH 111: 371 (1983). (10.1016/0027-5107(83)90034-9) / MUTATION RESEARCH (1983)
  22. COMFORT A BIOL SENESCENCE (1979).
  23. COMPERE, S.J., DNA METHYLATION CONTROLS THE INDUCIBILITY OF THE MOUSE METALLOTHIONEIN-I GENE IN LYMPHOID-CELLS, CELL 25: 233 (1981). (10.1016/0092-8674(81)90248-8) / CELL (1981)
  24. CONKLIN, K.F., ROLE OF METHYLATION IN THE INDUCED AND SPONTANEOUS EXPRESSION OF THE AVIAN ENDOGENOUS VIRUS EV-1 - DNA-STRUCTURE AND GENE-PRODUCTS, MOLECULAR AND CELLULAR BIOLOGY 2: 638 (1982). / MOLECULAR AND CELLULAR BIOLOGY (1982)
  25. Creusot, F., Journal of Biological Chemistry 257: 2041 (1982). (10.1016/S0021-9258(19)68144-5) / Journal of Biological Chemistry (1982)
  26. CURTIS H.J. BIOL MECHANISMS AGEI (1966).
  27. DELERS, A, SPONTANEOUS AND 5-AZACYTIDINE-INDUCED REEXPRESSION OF ORNITHINE CARBAMOYL TRANSFERASE IN HEPATOMA-CELLS, MOLECULAR AND CELLULAR BIOLOGY 4: 809 (1984). / MOLECULAR AND CELLULAR BIOLOGY (1984)
  28. DEMARS, R, RESISTANCE OF CULTURED HUMAN FIBROBLASTS AND OTHER CELLS TO PURINE AND PYRIMIDINE ANALOGS IN RELATION TO MUTAGENESIS DETECTION, MUTATION RESEARCH 24: 335 (1974). (10.1016/0027-5107(74)90180-8) / MUTATION RESEARCH (1974)
  29. DEMPSEY, J.L., MEASUREMENT OF INVIVO MUTANT FREQUENCY IN LYMPHOCYTES IN THE MOUSE, ENVIRONMENTAL MUTAGENESIS 8: 385 (1986). (10.1002/em.2860080307) / ENVIRONMENTAL MUTAGENESIS (1986)
  30. DEOL, M.S., J MORPHOL 100: 345 (1957). (10.1002/jmor.1051000206) / J MORPHOL (1957)
  31. DEVRIES, P.J., SITE SPECIFICITY OF DNA METHYLATION AND EXPRESSION OF HERPES-SIMPLEX THYMIDINE KINASE GENE, SOMATIC CELL AND MOLECULAR GENETICS 12: 385 (1986). (10.1007/BF01570733) / SOMATIC CELL AND MOLECULAR GENETICS (1986)
  32. DIPAOLO, J.A., IN-VITRO TRANSFORMATION OF SYRIAN-HAMSTER EMBRYO CELLS BY DIVERSE CHEMICAL CARCINOGENS, NATURE 235: 278 (1972). (10.1038/235278a0) / NATURE (1972)
  33. DOERFLER, W, DNA METHYLATION AND GENE ACTIVITY, ANNUAL REVIEW OF BIOCHEMISTRY 52: 93 (1983). (10.1146/annurev.bi.52.070183.000521) / ANNUAL REVIEW OF BIOCHEMISTRY (1983)
  34. FAIRWEATHER, S, EXP CELL RES 168: 153 (1987). (10.1016/0014-4827(87)90424-1) / EXP CELL RES (1987)
  35. FESTING, M, MULTIVARIATE-ANALYSIS OF SUBLINE DIVERGENCE IN SHAPE OF MANDIBLE IN C57BL-GR MICE, GENETICAL RESEARCH 21: 121 (1973). (10.1017/S0016672300013306) / GENETICAL RESEARCH (1973)
  36. FLATAU, E, DNA METHYLATION IN 5-AZA-2'-DEOXYCYTIDINE-RESISTANT VARIANTS OF C3H 10T1/2 C18 CELLS, MOLECULAR AND CELLULAR BIOLOGY 4: 2098 (1984). / MOLECULAR AND CELLULAR BIOLOGY (1984)
  37. GASSON, J.C., ROLE OF DENOVO DNA METHYLATION IN THE GLUCOCORTICOID RESISTANCE OF A T-LYMPHOID CELL-LINE, NATURE 302: 621 (1983). (10.1038/302621a0) / NATURE (1983)
  38. GOSS, S.J., THE ASSOCIATED REACTIVATION OF 2 X-LINKED GENES - THE SPONTANEOUS AND AZACYTIDINE-INDUCED REEXPRESSION OF ORNITHINE TRANSCARBAMOYLASE AND GLUCOSE-6-PHOSPHATE-DEHYDROGENASE IN A RAT HEPATOMA, JOURNAL OF CELL SCIENCE 72: 241 (1984). (10.1242/jcs.72.1.241) / JOURNAL OF CELL SCIENCE (1984)
  39. Gounari, F., Genes & Development 1: 899 (1987). (10.1101/gad.1.9.899) / Genes & Development (1987)
  40. GRAVES, JAM, X-CHROMOSOME ACTIVITY IN HETEROKARYONS AND HYBRIDS BETWEEN MOUSE FIBROBLASTS AND TERATOCARCINOMA STEM-CELLS, EXPERIMENTAL CELL RESEARCH 141: 87 (1982). (10.1016/0014-4827(82)90071-4) / EXPERIMENTAL CELL RESEARCH (1982)
  41. GREWAL, M.S., GENET RES 3: 226 (1982). / GENET RES (1982)
  42. GROUDINE, M, CHROMATIN STRUCTURE OF ENDOGENOUS RETROVIRAL GENES AND ACTIVATION BY AN INHIBITOR OF DNA METHYLATION, NATURE 292: 311 (1981). (10.1038/292311a0) / NATURE (1981)
  43. GRUNEBERG, H, IS THERE A VIRAL COMPONENT IN GENETIC BACKGROUND, NATURE 225: 39 (1970). (10.1038/225039a0) / NATURE (1970)
  44. GURDON, J.B., DEVELOPMENTAL CAPACITY OF NUCLEI TAKEN FROM INTESTINAL EPITHELIUM CELLS OF FEEDING TADPOLES, JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY 10: 622 (1962). / JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY (1962)
  45. 10.1038/2101240a0
  46. HARLAND, R.M., INHERITANCE OF DNA METHYLATION IN MICRO-INJECTED EGGS OF XENOPUS-LAEVIS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 2323 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
  47. HARRIS, M, INDUCTION OF THYMIDINE KINASE IN ENZYME-DEFICIENT CHINESE-HAMSTER CELLS, CELL 29: 483 (1982). (10.1016/0092-8674(82)90165-9) / CELL (1982)
  48. HARRIS, M, VARIANTS INDUCIBLE FOR GLUTAMINE-SYNTHETASE IN V79-56 CELLS, SOMATIC CELL AND MOLECULAR GENETICS 10: 275 (1984). (10.1007/BF01535249) / SOMATIC CELL AND MOLECULAR GENETICS (1984)
  49. HARRIS, M, HIGH-FREQUENCY INDUCTION BY 5-AZACYTIDINE OF PROLINE INDEPENDENCE IN CHO-K1 CELLS, SOMATIC CELL AND MOLECULAR GENETICS 10: 615 (1984). (10.1007/BF01535227) / SOMATIC CELL AND MOLECULAR GENETICS (1984)
  50. HARRIS, M, INDUCTION AND REVERSION OF ASPARAGINE AUXOTROPHS IN CHO-K1 AND V79 CELLS, SOMATIC CELL AND MOLECULAR GENETICS 12: 459 (1986). (10.1007/BF01539917) / SOMATIC CELL AND MOLECULAR GENETICS (1986)
  51. HAY, R.J., EXP GERONTOL 2: 123 (1967). (10.1016/0531-5565(67)90029-0) / EXP GERONTOL (1967)
  52. HAYFLICK, L, HDB BIOL AGING: 159 (1977). / HDB BIOL AGING (1977)
  53. HICKEY, I, AZACYTIDINE INDUCES REVERSION OF THYMIDINE KINASE-DEFICIENCY IN FRIEND-ERYTHROLEUKEMIA CELLS, EXPERIMENTAL CELL RESEARCH 164: 251 (1986). (10.1016/0014-4827(86)90472-6) / EXPERIMENTAL CELL RESEARCH (1986)
  54. HOISEN, Y, IS SUBLINE DIFFERENTIATION A CONTINUING PROCESS IN INBRED STRAINS OF MICE, GENETICAL RESEARCH 19: 53 (1972). (10.1017/S0016672300014269) / GENETICAL RESEARCH (1972)
  55. HOLLIDAY, R, BASIC LIFE SCI 35: 269 (1985). / BASIC LIFE SCI (1985)
  56. HOLLIDAY, R, NEW THEORY OF CARCINOGENESIS, BRITISH JOURNAL OF CANCER 40: 513 (1979). (10.1038/bjc.1979.216) / BRITISH JOURNAL OF CANCER (1979)
  57. HOLLIDAY, R, MECHANISMS FOR CHANGING GENE-EXPRESSION AND THEIR POSSIBLE RELATIONSHIP TO CARCINOGENESIS, CANCER SURVEYS 4: 557 (1985). / CANCER SURVEYS (1985)
  58. HOLLIDAY, R, CONTROLLING EVENTS E: 381 (1984). / CONTROLLING EVENTS E (1984)
  59. HOLLIDAY, R, STRONG EFFECTS OF 5-AZACYTIDINE ON THE INVITRO LIFE-SPAN OF HUMAN-DIPLOID FIBROBLASTS, EXPERIMENTAL CELL RESEARCH 166: 543 (1986). (10.1016/0014-4827(86)90499-4) / EXPERIMENTAL CELL RESEARCH (1986)
  60. HOLLIDAY R GENES PROTEINS CELLU (1986).
  61. HOLLIDAY, R, MECHANISM FOR GENE CONVERSION IN FUNGI, GENETICAL RESEARCH 5: 282 (1964). (10.1017/S0016672300001233) / GENETICAL RESEARCH (1964)
  62. HOLLIDAY, R, PREDICTIONS OF THE SOMATIC MUTATION AND MORTALIZATION THEORIES OF CELLULAR AGING ARE CONTRARY TO EXPERIMENTAL-OBSERVATIONS, JOURNAL OF THEORETICAL BIOLOGY 93: 627 (1981). (10.1016/0022-5193(81)90225-3) / JOURNAL OF THEORETICAL BIOLOGY (1981)
  63. HOLLIDAY, R, MONOGR DEV BIOL 17: 60 (1984). / MONOGR DEV BIOL (1984)
  64. HOLLIDAY, R, REPLICATION RECOMBIN: 157 (1968). / REPLICATION RECOMBIN (1968)
  65. 10.1126/science.187.4173.226
  66. HOLLIDAY R unpublished data.
  67. HOOPES, LLM, MOL CELL BIOL 3: 1371 (1983). / MOL CELL BIOL (1983)
  68. HUBERMAN, E, MUTAGENESIS AND TRANSFORMATION OF NORMAL CELLS BY CHEMICAL CARCINOGENS, NATURE 264: 360 (1976). (10.1038/264360a0) / NATURE (1976)
  69. HUSCHTSCHA L.I. unpublished data.
  70. IVARIE, R, ACTIVATION OF A NONEXPRESSED HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE ALLELE IN MUTANT H23 HELA-CELLS BY AGENTS THAT INHIBIT DNA METHYLATION, MOLECULAR AND CELLULAR BIOLOGY 6: 97 (1986). / MOLECULAR AND CELLULAR BIOLOGY (1986)
  71. IVARIE, R.D., INDUCTION OF PROLACTIN-DEFICIENT VARIANTS OF GH3 RAT PITUITARY-TUMOR CELLS BY ETHYL METHANESULFONATE - REVERSION BY 5-AZACYTIDINE, A DNA METHYLATION INHIBITOR, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 2967 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
  72. JAHNER, D, DENOVO METHYLATION AND EXPRESSION OF RETROVIRAL GENOMES DURING MOUSE EMBRYOGENESIS, NATURE 298: 623 (1982). (10.1038/298623a0) / NATURE (1982)
  73. JEGGO, P.A., AZACYTIDINE-INDUCED REACTIVATION OF A DNA-REPAIR GENE IN CHINESE-HAMSTER OVARY CELLS, MOLECULAR AND CELLULAR BIOLOGY 6: 2944 (1986). / MOLECULAR AND CELLULAR BIOLOGY (1986)
  74. JONES, P.A., DNA METHYLATION AND CANCER, CANCER RESEARCH 46: 461 (1986). / CANCER RESEARCH (1986)
  75. 10.1016/0092-8674(80)90237-8
  76. JONES, P.A., HEMIMETHYLATED DUPLEX DNAS PREPARED FROM 5-AZACYTIDINE-TREATED CELLS, NUCLEIC ACIDS RESEARCH 9: 2933 (1981). (10.1093/nar/9.12.2933) / NUCLEIC ACIDS RESEARCH (1981)
  77. KENNEDY, A.R., RELATIONSHIP BETWEEN X-RAY-EXPOSURE AND MALIGNANT TRANSFORMATION IN C3H 10T1/2 CELLS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 7262 (1980). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1980)
  78. KIRKWOOD, TBL, STABILITY OF THE CELLULAR TRANSLATION PROCESS, INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY 92: 93 (1984). / INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY (1984)
  79. KONDO, S, CARCINOGENESIS IN RELATION TO THE STEM-CELL-MUTATION HYPOTHESIS, DIFFERENTIATION 24: 1 (1983). (10.1111/j.1432-0436.1983.tb01294.x) / DIFFERENTIATION (1983)
  80. KRAEMER, P.M., SPONTANEOUS IMMORTALIZATION RATE OF CULTURED CHINESE-HAMSTER CELLS, JOURNAL OF THE NATIONAL CANCER INSTITUTE 76: 703 (1986). (10.1093/jnci/76.4.703) / JOURNAL OF THE NATIONAL CANCER INSTITUTE (1986)
  81. LANDOLPH, J.R., MUTAGENICITY OF 5-AZACYTIDINE AND RELATED NUCLEOSIDES IN C3H-10T1/2 CLONE-8 AND V79 CELLS, CANCER RESEARCH 42: 817 (1982). / CANCER RESEARCH (1982)
  82. LASKEY, R.A., J EMBRYOL EXP MORPHO 24: 227 (1970). / J EMBRYOL EXP MORPHO (1970)
  83. LIEBERMAN, M.W., ULTRAVIOLET RADIATION-INDUCED METALLOTHIONEIN-I GENE ACTIVATION IS ASSOCIATED WITH EXTENSIVE DNA DEMETHYLATION, CELL 35: 207 (1983). (10.1016/0092-8674(83)90223-4) / CELL (1983)
  84. LILLIS, M, MU-TRANSPOSONS IN MAIZE, TRENDS IN GENETICS 2: 183 (1986). (10.1016/0168-9525(86)90221-0) / TRENDS IN GENETICS (1986)
  85. LINDOP, P.J., SHORTENING OF LIFE AND CAUSES OF DEATH IN MICE EXPOSED TO A SINGLE WHOLE-BODY DOSE OF RADIATION, NATURE 189: 645 (1961). (10.1038/189645a0) / NATURE (1961)
  86. LINDOP, P.J., P R SOC LONDON B 154: 332 (1960). / P R SOC LONDON B (1960)
  87. LISKAY, R.M., INACTIVE X-CHROMOSOME DNA DOES NOT FUNCTION IN DNA-MEDIATED CELL-TRANSFORMATION FOR THE HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE GENE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 4895 (1980). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1980)
  88. LITEPLO, R.G., 5-AZACYTIDINE INDUCTION OF THYMIDINE KINASE IN A SPONTANEOUSLY ENZYME-DEFICIENT MURINE TUMOR LINE, EXPERIMENTAL CELL RESEARCH 150: 499 (1984). (10.1016/0014-4827(84)90596-2) / EXPERIMENTAL CELL RESEARCH (1984)
  89. MAYNARDSMITH, J, NATURE 184: 956 (1959). (10.1038/184956a0) / NATURE (1959)
  90. MCCLINTOCK, B, ANN REV GENET 8: 15 (1974). (10.1146/annurev.ge.08.120174.000311) / ANN REV GENET (1974)
  91. MESELSON, M.S., GENERAL MODEL FOR GENETIC RECOMBINATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 72: 358 (1975). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1975)
  92. Holliday R. The Evolution of Sex (1988).
  93. MILO, G.E., CHARACTERIZATION OF HUMAN-CELLS TRANSFORMED BY CHEMICAL AND PHYSICAL CARCINOGENS INVITRO, IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION 17: 719 (1981). / IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION (1981)
  94. 10.1126/science.6164095
  95. MONK, M, METHYLATION AND THE X-CHROMOSOME, BIOESSAYS 4: 204 (1986). (10.1002/bies.950040505) / BIOESSAYS (1986)
  96. MORLEY, A.A., MEASUREMENT OF INVIVO MUTATIONS IN HUMAN-LYMPHOCYTES, NATURE 302: 155 (1983). (10.1038/302155a0) / NATURE (1983)
  97. NAKAMURA, N, MUTATIONS RESISTANT TO BROMODEOXYURIDINE IN MOUSE LYMPHOMA-CELLS SELECTED BY REPEATED EXPOSURE TO EMS - CHARACTERISTICS OF PHENOTYPIC INSTABILITY AND REVERSION TO HAT RESISTANCE BY 5-AZACYTIDINE, MUTATION RESEARCH 111: 353 (1983). (10.1016/0027-5107(83)90032-5) / MUTATION RESEARCH (1983)
  98. NAMBA, M, MULTISTEP PROCESS OF NEOPLASTIC TRANSFORMATION OF NORMAL HUMAN-FIBROBLASTS BY CO-60 GAMMA-RAYS AND HARVEY SARCOMA-VIRUSES, INTERNATIONAL JOURNAL OF CANCER 37: 419 (1986). (10.1002/ijc.2910370314) / INTERNATIONAL JOURNAL OF CANCER (1986)
  99. NIWA, O, 5-AZACYTIDINE INDUCTION OF MOUSE ENDOGENOUS TYPE-C VIRUS AND SUPPRESSION OF DNA METHYLATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 78: 6290 (1981). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1981)
  100. NOMURA, T, PARENTAL EXPOSURE TO X-RAYS AND CHEMICALS INDUCES HERITABLE TUMORS AND ANOMALIES IN MICE, NATURE 296: 575 (1982). (10.1038/296575a0) / NATURE (1982)
  101. ORGEL, L.E., NATURE 243: 441 (1973). (10.1038/243441a0) / NATURE (1973)
  102. ORGEL, L.E., CORRECTION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 67: 1476 (1970). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1970)
  103. ORGEL, L.E., MAINTENANCE OF ACCURACY OF PROTEIN SYNTHESIS AND TIS RELEVANCE TO AGEING, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 49: 517 (1963). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1963)
  104. PATERNO, G.D., X-CHROMOSOME REACTIVATION IN MOUSE EMBRYONAL CARCINOMA-CELLS, MOLECULAR AND CELLULAR BIOLOGY 5: 2705 (1985). / MOLECULAR AND CELLULAR BIOLOGY (1985)
  105. PEMBREY, M.E., A PRE-MUTATION THAT GENERATES A DEFECT AT CROSSING OVER EXPLAINS THE INHERITANCE OF FRAGILE X MENTAL RETARDATION, AMERICAN JOURNAL OF MEDICAL GENETICS 21: 709 (1985). (10.1002/ajmg.1320210413) / AMERICAN JOURNAL OF MEDICAL GENETICS (1985)
  106. PETO, R, ORIGINS HUMAN CANCER 4: 1403 (1977). / ORIGINS HUMAN CANCER (1977)
  107. RATTAN, SIS, OPTIMUM CONDITIONS FOR GROWTH AND LONGEVITY OF CHICK-EMBRYO FIBROBLASTS IN CULTURE, MECHANISMS OF AGEING AND DEVELOPMENT 19: 1 (1982). (10.1016/0047-6374(82)90043-4) / MECHANISMS OF AGEING AND DEVELOPMENT (1982)
  108. RATTAN SIS unpublished data.
  109. RAZIN, A, DNA METHYLATION IN EUKARYOTIC CELLS, INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY 92: 159 (1984). / INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY (1984)
  110. RAZIN A SPRINGER SERIES MOL (1984).
  111. RIGGS, A.D., 5-METHYLCYTOSINE, GENE-REGULATION, AND CANCER, ADVANCES IN CANCER RESEARCH 40: 1 (1983). (10.1016/S0065-230X(08)60678-8) / ADVANCES IN CANCER RESEARCH (1983)
  112. RIGGS, A.D., BIOCH BIOL DNA METHY: 211 (1985). / BIOCH BIOL DNA METHY (1985)
  113. RIGGS, A.D., X-INACTIVATION, DIFFERENTIATION, AND DNA METHYLATION, CYTOGENETICS AND CELL GENETICS 14: 9 (1975). (10.1159/000130315) / CYTOGENETICS AND CELL GENETICS (1975)
  114. RYAN, J.M., KINETICS OF CHICK CELL-POPULATION AGING INVITRO, JOURNAL OF CELLULAR PHYSIOLOGY 99: 67 (1979). (10.1002/jcp.1040990109) / JOURNAL OF CELLULAR PHYSIOLOGY (1979)
  115. SACHER, G.A., GENETICS AGING: 151 (1978). / GENETICS AGING (1978)
  116. 10.1126/science.189.4201.426
  117. SALUZ, H.P., GENOMIC SEQUENCING REVEALS A POSITIVE CORRELATION BETWEEN THE KINETICS OF STRAND-SPECIFIC DNA DEMETHYLATION OF THE OVERLAPPING ESTRADIOL GLUCOCORTICOID RECEPTOR-BINDING SITES AND THE RATE OF AVIAN VITELLOGENIN MESSENGER-RNA SYNTHESIS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 7167 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)
  118. SANTI, D.V., COVALENT BOND FORMATION BETWEEN A DNA-CYTOSINE METHYLTRANSFERASE AND DNA CONTAINING 5-AZACYTOSINE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 81: 6993 (1984). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1984)
  119. SCARANO, E, ADV CYTOPHARMACOL 1: 13 (1971). / ADV CYTOPHARMACOL (1971)
  120. SCHWARTZ, D, TRANSPOSASE ACTIVITY OF THE AC CONTROLLING ELEMENT IN MAIZE IS REGULATED BY ITS DEGREE OF METHYLATION, MOLECULAR & GENERAL GENETICS 205: 476 (1986). (10.1007/BF00338085) / MOLECULAR & GENERAL GENETICS (1986)
  121. SILINSKAS, K.C., INDUCTION OF ANCHORAGE-INDEPENDENT GROWTH IN HUMAN-FIBROBLASTS BY PROPANE SULTONE, CANCER RESEARCH 41: 1620 (1981). / CANCER RESEARCH (1981)
  122. SIMINOVITCH, L, NATURE OF HEREDITABLE VARIATION IN CULTURED SOMATIC-CELLS, CELL 7: 1 (1976). (10.1016/0092-8674(76)90249-X) / CELL (1976)
  123. SMITH J.M. EVOLUTION SEX (1978).
  124. SMITH, J.M., P R SOC LONDON B 157: 115 (1961). / P R SOC LONDON B (1961)
  125. STALLINGS, R.L., 5-AZACYTIDINE-INDUCED CONVERSION TO CADMIUM RESISTANCE CORRELATES WITH EARLY S-PHASE REPLICATION OF INACTIVE METALLOTHIONEIN GENES IN SYNCHRONIZED CHO CELLS, SOMATIC CELL AND MOLECULAR GENETICS 12: 423 (1986). (10.1007/BF01539913) / SOMATIC CELL AND MOLECULAR GENETICS (1986)
  126. STEGLICH, C, CHINESE-HAMSTER CELLS DEFICIENT IN ORNITHINE DECARBOXYLASE ACTIVITY - REVERSION BY GENE AMPLIFICATION AND BY AZACYTIDINE TREATMENT, SOMATIC CELL AND MOLECULAR GENETICS 11: 11 (1985). (10.1007/BF01534730) / SOMATIC CELL AND MOLECULAR GENETICS (1985)
  127. STELLWAGEN R unpublished data.
  128. STEWART, C.L., DENOVO METHYLATION, EXPRESSION, AND INFECTIVITY OF RETROVIRAL GENOMES INTRODUCED INTO EMBRYONAL CARCINOMA-CELLS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 4098 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
  129. SUGIYAMA, R.H., PROPERTIES OF ASPARAGINE SYNTHETASE IN ASPARAGINE-INDEPENDENT VARIANTS OF JENSEN RAT SARCOMA-CELLS INDUCED BY 5-AZACYTIDINE, MOLECULAR AND CELLULAR BIOLOGY 3: 1937 (1983). / MOLECULAR AND CELLULAR BIOLOGY (1983)
  130. SUTHERLAND, B.M., ULTRAVIOLET LIGHT-INDUCED TRANSFORMATION OF HUMAN-CELLS TO ANCHORAGE-INDEPENDENT GROWTH, CANCER RESEARCH 40: 1934 (1980). / CANCER RESEARCH (1980)
  131. SUTHERLAND, G.R., THE ENIGMA OF THE FRAGILE-X CHROMOSOME, TRENDS IN GENETICS 1: 108 (1985). (10.1016/0168-9525(85)90042-3) / TRENDS IN GENETICS (1985)
  132. SZILARD, L, ON THE NATURE OF THE AGING PROCESS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 45: 30 (1959). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1959)
  133. SZOSTAK, J.W., THE DOUBLE-STRAND-BREAK REPAIR MODEL FOR RECOMBINATION, CELL 33: 25 (1983). (10.1016/0092-8674(83)90331-8) / CELL (1983)
  134. TAYLOR, S.M., MECHANISM OF ACTION OF EUKARYOTIC DNA METHYLTRANSFERASE - USE OF 5-AZACYTOSINE-CONTAINING DNA, JOURNAL OF MOLECULAR BIOLOGY 162: 679 (1982). (10.1016/0022-2836(82)90395-3) / JOURNAL OF MOLECULAR BIOLOGY (1982)
  135. THACKER, J, MUTAT RES 42: 311 (1977). / MUTAT RES (1977)
  136. THURIAUX, P, IS RECOMBINATION CONFINED TO STRUCTURAL GENES ON EUKARYOTIC GENOME, NATURE 268: 460 (1977). (10.1038/268460a0) / NATURE (1977)
  137. TODARO, G.J., QUANTITATIVE STUDIES OF GROWTH OF MOUSE EMBRYO CELLS IN CULTURE AND THEIR DEVELOPMENT INTO ESTABLISHED LINES, JOURNAL OF CELL BIOLOGY 17: 299 (1963). (10.1083/jcb.17.2.299) / JOURNAL OF CELL BIOLOGY (1963)
  138. TOMATIS, L, NATIONAL CANCER INSTITUTE MONOGRAPHS 51: 159 (1979). / NATIONAL CANCER INSTITUTE MONOGRAPHS (1979)
  139. 10.1038/302575a0
  140. TONIOLO, D, SPECIFIC METHYLATION PATTERN AT THE 3' END OF THE HUMAN HOUSEKEEPING GENE FOR GLUCOSE-6-PHOSPHATE-DEHYDROGENASE, EMBO JOURNAL 3: 1987 (1984). (10.1002/j.1460-2075.1984.tb02080.x) / EMBO JOURNAL (1984)
  141. 10.1086/413059
  142. VENOLIA, L, COMPARISON OF TRANSFORMATION EFFICIENCY OF HUMAN ACTIVE AND INACTIVE X-CHROMOSOMAL DNA, NATURE 302: 82 (1983). (10.1038/302082a0) / NATURE (1983)
  143. VENOLIA, L, TRANSFORMATION WITH DNA FROM 5-AZACYTIDINE-REACTIVATED X-CHROMOSOMES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 2352 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
  144. WADDINGTON C.H. PRINCIPLES EMBRYOLOG (1956). (10.5962/bhl.title.7217)
  145. WADDINGTON, C.H., EPIGENETICS AND EVOLUTION, SYMPOSIA OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY 7: 186 (1953). / SYMPOSIA OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY (1953)
  146. WAREHAM, K.A., AGE-RELATED REACTIVATION OF AN X-LINKED GENE, NATURE 327: 725 (1987). (10.1038/327725a0) / NATURE (1987)
  147. 10.1016/0092-8674(85)90267-3
  148. WHITEHOUSE, HLK, ANALYSIS OF GENETIC RECOMBINATION ON POLARON HYBRID DNA MODEL, GENETICAL RESEARCH 6: 27 (1965). (10.1017/S0016672300003955) / GENETICAL RESEARCH (1965)
  149. WHITEHOUSE, HLK, AN OPERATOR MODEL OF CROSSING-OVER, NATURE 211: 708 (1966). (10.1038/211708a0) / NATURE (1966)
  150. WIGLER, M, THE SOMATIC REPLICATION OF DNA METHYLATION, CELL 24: 33 (1981). (10.1016/0092-8674(81)90498-0) / CELL (1981)
  151. WIGLER, M.H., THE INHERITANCE OF METHYLATION PATTERNS IN VERTEBRATES, CELL 24: 285 (1981). (10.1016/0092-8674(81)90317-2) / CELL (1981)
  152. WILLIAMS G.C. MONOGRAPHS POPULATIO 8 (1974).
  153. WILSON, V.L., INHIBITION OF DNA METHYLATION BY CHEMICAL CARCINOGENS INVITRO, CELL 32: 239 (1983). (10.1016/0092-8674(83)90514-7) / CELL (1983)
  154. 10.1126/science.6844925
  155. WOLF, S.F., COMPLETE CONCORDANCE BETWEEN GLUCOSE-6-PHOSPHATE-DEHYDROGENASE ACTIVITY AND HYPOMETHYLATION OF 3' CPG CLUSTERS - IMPLICATIONS FOR X-CHROMOSOME DOSAGE COMPENSATION, NUCLEIC ACIDS RESEARCH 12: 9333 (1984). (10.1093/nar/12.24.9333) / NUCLEIC ACIDS RESEARCH (1984)
  156. WOLF, S.F., METHYLATION OF THE HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE LOCUS ON THE HUMAN X-CHROMOSOME - IMPLICATIONS FOR X-CHROMOSOME INACTIVATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 81: 2806 (1984). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1984)
  157. YEN, P.H., DIFFERENTIAL METHYLATION OF HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE GENES ON ACTIVE AND INACTIVE HUMAN X-CHROMOSOMES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 81: 1759 (1984). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1984)
  158. YEN, P.H., STABILITY OF DNA METHYLATION OF THE HUMAN HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE GENE, SOMATIC CELL AND MOLECULAR GENETICS 12: 153 (1986). (10.1007/BF01560662) / SOMATIC CELL AND MOLECULAR GENETICS (1986)
  159. YISRAELI, J, MUSCLE-SPECIFIC ACTIVATION OF A METHYLATED CHIMERIC ACTIN GENE, CELL 46: 409 (1986). (10.1016/0092-8674(86)90661-6) / CELL (1986)
Dates
Type When
Created 18 years, 10 months ago (Oct. 5, 2006, 4:28 p.m.)
Deposited 1 year, 6 months ago (Feb. 6, 2024, 10:19 p.m.)
Indexed 2 days, 1 hour ago (Aug. 31, 2025, 6:12 a.m.)
Issued 37 years, 10 months ago (Oct. 9, 1987)
Published 37 years, 10 months ago (Oct. 9, 1987)
Published Print 37 years, 10 months ago (Oct. 9, 1987)
Funders 0

None

@article{Holliday_1987, title={The Inheritance of Epigenetic Defects}, volume={238}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.3310230}, DOI={10.1126/science.3310230}, number={4824}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Holliday, Robin}, year={1987}, month=oct, pages={163–170} }