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. 1983 Aug;3(8):1371–1380. doi: 10.1128/mcb.3.8.1371

Methylation and rearrangement of mouse intracisternal a particle genes in development, aging, and myeloma.

L L Mays-Hoopes, A Brown, R C Huang
PMCID: PMC369983  PMID: 6621530

Abstract

Sequences of DNA that hybridize on Southern blots with cloned intracisternal A-particle (IAP) sequences have been examined in genomic DNAs of neonatal mice, livers of adult mice (3, 6, 12, 18, 24, and 26 months old), and the solid myeloma tumor MOPC-315. The isoschizomers HpaII (CCGG or mCCGG) and MspI (CCGG or CmCGG) were used to assess methylation. All the DNAs produced a major 0.5-kilobase MspI fragment that hybridizes with IAP probe. Only the myeloma DNA, and to a much lesser degree DNA from senescent mouse liver, produced this fragment in HpaII digest; the other DNAs all had IAP sequences resistant to HpaII digestion. These sequences thus become fully methylated to CmCGG early and remain so in adult life, except in the myeloma cells that are expressing the IAP genes. An increase in MspI-sensitive sites in IAP gene-containing DNA was observed in aging mice. The probe used to assess methylation, a 0.8-kilobase fragment produced by BamHI-HindIII double digestion, is common to several cloned IAP genes and is part of a region of DNA which is conserved in genomes of all mouse tissues. The probe hybridized to 1.5- and 1.4-kilobase doublet bands produced by BamHI, HindIII, and EcoRI triple digestions of neonatal DNA. These two bands were found in neonatal livers of Swiss Webster, BALB/c, and C57BL/6J mouse strains, showed less in adult liver, and were barely detectable in senescent livers from C57BL/6J mice.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Breznik T., Cohen J. C. Altered methylation of endogenous viral promoter sequences during mammary carcinogenesis. Nature. 1982 Jan 21;295(5846):255–257. doi: 10.1038/295255a0. [DOI] [PubMed] [Google Scholar]
  2. Britten R. J., Graham D. E., Neufeld B. R. Analysis of repeating DNA sequences by reassociation. Methods Enzymol. 1974;29:363–418. doi: 10.1016/0076-6879(74)29033-5. [DOI] [PubMed] [Google Scholar]
  3. Calarco P. G., Szollosi D. Intracisternal A particles in ova and preimplantation stages of the mouse. Nat New Biol. 1973 May 16;243(124):91–93. [PubMed] [Google Scholar]
  4. Calvin H. I. Isolation of subfractionation of mammalian sperm heads and tails. Methods Cell Biol. 1976;13:85–104. doi: 10.1016/s0091-679x(08)61798-7. [DOI] [PubMed] [Google Scholar]
  5. Chase D. G., Pikó L. Expression of A- and C-type particles in early mouse embryos. J Natl Cancer Inst. 1973 Dec;51(6):1971–1975. doi: 10.1093/jnci/51.6.1971. [DOI] [PubMed] [Google Scholar]
  6. Christy B., Scangos G. Expression of transferred thymidine kinase genes is controlled by methylation. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6299–6303. doi: 10.1073/pnas.79.20.6299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cole M. D., Ono M., Huang R. C. Terminally redundant sequences in cellular intracisternal A-particle genes. J Virol. 1981 May;38(2):680–687. doi: 10.1128/jvi.38.2.680-687.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dackowski W., Morrison S. L. Two alpha heavy chain disease proteins with different genomic deletions demonstrate that nonexpressed alpha heavy chain genes contain methylated bases. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7091–7095. doi: 10.1073/pnas.78.11.7091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  10. Early P., Huang H., Davis M., Calame K., Hood L. An immunoglobulin heavy chain variable region gene is generated from three segments of DNA: VH, D and JH. Cell. 1980 Apr;19(4):981–992. doi: 10.1016/0092-8674(80)90089-6. [DOI] [PubMed] [Google Scholar]
  11. Groudine M., Eisenman R., Weintraub H. Chromatin structure of endogenous retroviral genes and activation by an inhibitor of DNA methylation. Nature. 1981 Jul 23;292(5821):311–317. doi: 10.1038/292311a0. [DOI] [PubMed] [Google Scholar]
  12. Harbers K., Schnieke A., Stuhlmann H., Jähner D., Jaenisch R. DNA methylation and gene expression: endogenous retroviral genome becomes infectious after molecular cloning. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7609–7613. doi: 10.1073/pnas.78.12.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hart R. W., D'Ambrosio S. M., Ng K. J., Modak S. P. Longevity, stability and DNA repair. Mech Ageing Dev. 1979 Feb;9(3-4):203–223. doi: 10.1016/0047-6374(79)90100-3. [DOI] [PubMed] [Google Scholar]
  14. Hart R. W., Setlow R. B. Correlation between deoxyribonucleic acid excision-repair and life-span in a number of mammalian species. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2169–2173. doi: 10.1073/pnas.71.6.2169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hawley R. G., Shulman M. J., Murialdo H., Gibson D. M., Hozumi N. Mutant immunoglobulin genes have repetitive DNA elements inserted into their intervening sequences. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7425–7429. doi: 10.1073/pnas.79.23.7425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Huebner R. J., Todaro G. J. Oncogenes of RNA tumor viruses as determinants of cancer. Proc Natl Acad Sci U S A. 1969 Nov;64(3):1087–1094. doi: 10.1073/pnas.64.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jones P. A., Taylor S. M. Cellular differentiation, cytidine analogs and DNA methylation. Cell. 1980 May;20(1):85–93. doi: 10.1016/0092-8674(80)90237-8. [DOI] [PubMed] [Google Scholar]
  18. Kuff E. L., Feenstra A., Lueders K., Smith L., Hawley R., Hozumi N., Shulman M. Intracisternal A-particle genes as movable elements in the mouse genome. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1992–1996. doi: 10.1073/pnas.80.7.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuff E. L., Lueders K. K., Scolnick E. M. Nucleotide sequence relationship between intracisternal type A particles of Mus musculus and an endogenous retrovirus (M432) of Mus cervicolor. J Virol. 1978 Oct;28(1):66–74. doi: 10.1128/jvi.28.1.66-74.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lueders K. K., Kuff E. L. Sequences associated with intracisternal A particles are reiterated in the mouse genome. Cell. 1977 Dec;12(4):963–972. doi: 10.1016/0092-8674(77)90161-1. [DOI] [PubMed] [Google Scholar]
  21. Lueders K. K., Segal S., Kuff E. L. RNA sequences specifically associated with mouse intracisternal A particles. Cell. 1977 May;11(1):83–94. doi: 10.1016/0092-8674(77)90319-1. [DOI] [PubMed] [Google Scholar]
  22. Mandel J. L., Chambon P. DNA methylation: organ specific variations in the methylation pattern within and around ovalbumin and other chicken genes. Nucleic Acids Res. 1979 Dec 20;7(8):2081–2103. doi: 10.1093/nar/7.8.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Max E. E., Seidman J. G., Leder P. Sequences of five potential recombination sites encoded close to an immunoglobulin kappa constant region gene. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3450–3454. doi: 10.1073/pnas.76.7.3450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McClelland M. The effect of sequence specific DNA methylation on restriction endonuclease cleavage. Nucleic Acids Res. 1981 Nov 25;9(22):5859–5866. doi: 10.1093/nar/9.22.5859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nakanishi Y., Dein R. A., Schneider E. L. Aging and sister chromatid exchange. V. The effect of post-embryonic development on mutagen-induced sister chromatid exchanges in mouse and rat bone marrow cells. Cytogenet Cell Genet. 1980;27(2-3):82–87. doi: 10.1159/000131469. [DOI] [PubMed] [Google Scholar]
  26. Neel B. G., Hayward W. S., Robinson H. L., Fang J., Astrin S. M. Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion. Cell. 1981 Feb;23(2):323–334. doi: 10.1016/0092-8674(81)90128-8. [DOI] [PubMed] [Google Scholar]
  27. Ono M., Cole M. D., White A. T., Huang R. C. Sequence organization of cloned intracisternal A particle genes. Cell. 1980 Sep;21(2):465–473. doi: 10.1016/0092-8674(80)90483-3. [DOI] [PubMed] [Google Scholar]
  28. Payne G. S., Courtneidge S. A., Crittenden L. B., Fadly A. M., Bishop J. M., Varmus H. E. Analysis of avian leukosis virus DNA and RNA in bursal tumours: viral gene expression is not required for maintenance of the tumor state. Cell. 1981 Feb;23(2):311–322. doi: 10.1016/0092-8674(81)90127-6. [DOI] [PubMed] [Google Scholar]
  29. Razin A., Riggs A. D. DNA methylation and gene function. Science. 1980 Nov 7;210(4470):604–610. doi: 10.1126/science.6254144. [DOI] [PubMed] [Google Scholar]
  30. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  31. Schneider E. L., Kram D., Nakanishi Y., Monticone R. E., Tice R. R., Gilman B. A., Nieder M. L. The effect of aging on sister chromatid exchange. Mech Ageing Dev. 1979 Feb;9(3-4):303–311. doi: 10.1016/0047-6374(79)90107-6. [DOI] [PubMed] [Google Scholar]
  32. Shen-Ong G. L., Cole M. D. Differing populations of intracisternal A-particle genes in myeloma tumors and mouse subspecies. J Virol. 1982 May;42(2):411–421. doi: 10.1128/jvi.42.2.411-421.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shmookler Reis R. J., Goldstein S. Loss of reiterated DNA sequences during serial passage of human diploid fibroblasts. Cell. 1980 Oct;21(3):739–749. doi: 10.1016/0092-8674(80)90437-7. [DOI] [PubMed] [Google Scholar]
  34. Shmookler Reis R. J., Lumpkin C. K., Jr, McGill J. R., Riabowol K. T., Goldstein S. Extrachromosomal circular copies of an 'inter-Alu' unstable sequence in human DNA are amplified during in vitro and in vivo ageing. Nature. 1983 Feb 3;301(5899):394–398. doi: 10.1038/301394a0. [DOI] [PubMed] [Google Scholar]
  35. Singer J., Roberts-Ems J., Luthardt F. W., Riggs A. D. Methylation of DNA in mouse early embryos, teratocarcinoma cells and adult tissues of mouse and rabbit. Nucleic Acids Res. 1979 Dec 20;7(8):2369–2385. doi: 10.1093/nar/7.8.2369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sobieski D. A., Eden F. C. Clustering and methylation of repeated DNA: persistence in avian development and evolution. Nucleic Acids Res. 1981 Nov 25;9(22):6001–6015. doi: 10.1093/nar/9.22.6001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  38. Stuhlmann H., Jähner D., Jaenisch R. Infectivity and methylation of retroviral genomes is correlated with expression in the animal. Cell. 1981 Oct;26(2 Pt 2):221–232. doi: 10.1016/0092-8674(81)90305-6. [DOI] [PubMed] [Google Scholar]
  39. Vardimon L., Neumann R., Kuhlmann I., Sutter D., Doerfler W. DNA methylation and viral gene expression in adenovirus-transformed and -infected cells. Nucleic Acids Res. 1980 Jun 11;8(11):2461–2473. doi: 10.1093/nar/8.11.2461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weintraub H., Larsen A., Groudine M. Alpha-Globin-gene switching during the development of chicken embryos: expression and chromosome structure. Cell. 1981 May;24(2):333–344. doi: 10.1016/0092-8674(81)90323-8. [DOI] [PubMed] [Google Scholar]
  41. Wivel N. A., Smith G. H. Distribution of intracisternal A-particles in a variety of normal and neoplastic mouse tissues. Int J Cancer. 1971 Jan 15;7(1):167–175. doi: 10.1002/ijc.2910070119. [DOI] [PubMed] [Google Scholar]
  42. van der Ploeg L. H., Flavell R. A. DNA methylation in the human gamma delta beta-globin locus in erythroid and nonerythroid tissues. Cell. 1980 Apr;19(4):947–958. doi: 10.1016/0092-8674(80)90086-0. [DOI] [PubMed] [Google Scholar]

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