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. 1982 May;42(2):411–421. doi: 10.1128/jvi.42.2.411-421.1982

Differing populations of intracisternal A-particle genes in myeloma tumors and mouse subspecies.

G L Shen-Ong, M D Cole
PMCID: PMC256867  PMID: 6283165

Abstract

Intracisternal A-particle genes form a family of endogenous retrovirus-like genetic elements that are transcribed in mouse plasmacytomas (myeloma tumors). Two types of A-particle genes that can be differentiated by a sequence of 0.5 kilobase found in one type but not the other have been identified. Quantitative Southern blot analysis was used to measure the populations of different A-particle genes in DNAs from BALB/c mice, the Japanese subspecies Mus musculus subsp. molossinus, and myeloma tumors. The majority of the genes (715 copies per haploid genome or 76%) were found to be nearly identical except for small changes in conserved restriction enzyme sites. The second type of A-particle gene was much less abundant with 90 copies representing approximately 10%. The A-particle RNA in MOPC104E and MOPC315 was found to be colinear with a small portion of this latter type, comprising only 2% of the endogenous intracisternal A-particle sequences. Myeloma tumor DNA was found to have a two- to fourfold increase in the number of these genes, suggesting that the intracellular viruses have been activated to produce a double-stranded complementary DNA which subsequently integrated into the tumor genome. Analysis of M. musculus subsp. molossinus DNA revealed similar but shifted populations of A-particle genes, when compared with BALB/c DNA, except for the absence of a prominent EcoRI-HindIII band at 3.9 kilobases. This latter band, representing approximately 15% of the A-particle genes in BALB/c DNA, was shown to be a deletion variant of the most abundant gene family.

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Selected References

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

  1. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  2. Biczysko W., Pienkowski M., Solter D., Koprowski H. Virus particles in early mouse embryos. J Natl Cancer Inst. 1973 Sep;51(3):1041–1050. doi: 10.1093/jnci/51.3.1041. [DOI] [PubMed] [Google Scholar]
  3. Blattner F. R., Williams B. G., Blechl A. E., Denniston-Thompson K., Faber H. E., Furlong L., Grunwald D. J., Kiefer D. O., Moore D. D., Schumm J. W. Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. Science. 1977 Apr 8;196(4286):161–169. doi: 10.1126/science.847462. [DOI] [PubMed] [Google Scholar]
  4. 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]
  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. Cohen J. C. Methylation of milk-borne and genetically transmitted mouse mammary tumor virus proviral DNA. Cell. 1980 Mar;19(3):653–662. doi: 10.1016/s0092-8674(80)80042-0. [DOI] [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. Cordell B., Weiss S. R., Varmus H. E., Bishop J. M. At least 104 nucleotides are transposed from the 5' terminus of the avian sarcoma virus genome to the 5' termini of smaller viral mRNAs. Cell. 1978 Sep;15(1):79–91. doi: 10.1016/0092-8674(78)90084-3. [DOI] [PubMed] [Google Scholar]
  9. DALTON A. J., POTTER M., MERWIN R. M. Some ultrastructural characteristics of a series of primary and transplanted plasma-cell tumors of the mouse. J Natl Cancer Inst. 1961 May;26:1221–1267. [PubMed] [Google Scholar]
  10. DE HARVEN E., FRIEND C. Electron microscope study of a cell-free induced leukemia of the mouse: a preliminary report. J Biophys Biochem Cytol. 1958 Mar 25;4(2):151–156. doi: 10.1083/jcb.4.2.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Eisen H. N., Simms E. S., Potter M. Mouse myeloma proteins with antihapten antibody acitivity. The protein produced by plasma cell tumor MOPC-315. Biochemistry. 1968 Nov;7(11):4126–4134. doi: 10.1021/bi00851a048. [DOI] [PubMed] [Google Scholar]
  13. FRIEDLAENDER M., MOORE D. H. Occurrence of bodies within endoplasmic reticulum of Ehrlich ascites tumor cells. Proc Soc Exp Biol Med. 1956 Aug-Sep;92(4):828–831. doi: 10.3181/00379727-92-22627. [DOI] [PubMed] [Google Scholar]
  14. Hall W. T., Hartley J. W., Sanford K. K. Characteristics of and relationship between C particles and intracisternal A particles in cloned cell strains. J Virol. 1968 Mar;2(3):238–247. doi: 10.1128/jvi.2.3.238-247.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  16. Hayward W. S. Size and genetic content of viral RNAs in avian oncovirus-infected cells. J Virol. 1977 Oct;24(1):47–63. doi: 10.1128/jvi.24.1.47-63.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  18. Kakefuda T., Roberts E., Suntzeff V. Electron microscopic study of methylcholanthrene-induced epidermal carcinogenesis in mice: mitochondrial dense bodies and intracisternal A-particles. Cancer Res. 1970 Apr;30(4):1011–1019. [PubMed] [Google Scholar]
  19. Kuff E. L., Smith L. A., Lueders K. K. Intracisternal A-particle genes in Mus musculus: a conserved family of retrovirus-like elements. Mol Cell Biol. 1981 Mar;1(3):216–227. doi: 10.1128/mcb.1.3.216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kuff E. L., Wivel N. A., Lueders K. K. The extraction of intracisternal A-particles from a mouse plasma-cell tumor. Cancer Res. 1968 Oct;28(10):2137–2148. [PubMed] [Google Scholar]
  21. Lueders K. K., Kuff E. L. Intracisternal A-particle genes: identification in the genome of Mus musculus and comparison of multiple isolates from a mouse gene library. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3571–3575. doi: 10.1073/pnas.77.6.3571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Lueders K. K., Kuff E. L. Synthesis and turnover of intracisternal A-particle structural protein in cultured neuroblastoma cells. J Biol Chem. 1975 Jul 10;250(13):5192–5199. [PubMed] [Google Scholar]
  24. McCarthy B. J., Nishiura J. T., Doenecke D., Nasser D. S., Johnson C. B. Transcription and chromatin structure. Cold Spring Harb Symp Quant Biol. 1974;38:763–771. doi: 10.1101/sqb.1974.038.01.081. [DOI] [PubMed] [Google Scholar]
  25. McIntimif K. R., Asofsky R. M., Potter M., Kuff E. L. Macroglobulin-Producing Plasma-Cell Tumor in Mice: Identification of a New Light Chain. Science. 1965 Oct 15;150(3694):361–363. doi: 10.1126/science.150.3694.361. [DOI] [PubMed] [Google Scholar]
  26. Minna J. D., Lueders K. K., Kuff E. L. Expression of genes for intracisternal A-particle antigen in somatic cell hybrids. J Natl Cancer Inst. 1974 Apr;52(4):1211–1217. doi: 10.1093/jnci/52.4.1211. [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. Potter M. Immunoglobulin-producing tumors and myeloma proteins of mice. Physiol Rev. 1972 Jul;52(3):631–719. doi: 10.1152/physrev.1972.52.3.631. [DOI] [PubMed] [Google Scholar]
  29. Potter S. S., Brorein W. J., Jr, Dunsmuir P., Rubin G. M. Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell. 1979 Jun;17(2):415–427. doi: 10.1016/0092-8674(79)90168-5. [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. Schimke R. T., Alt F. W., Kellems R. E., Kaufman R. J., Bertino J. R. Amplification of dihydrofolate reductase genes in methotrexate-resistant cultured mouse cells. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):649–657. doi: 10.1101/sqb.1978.042.01.067. [DOI] [PubMed] [Google Scholar]
  32. Shank P. R., Hughes S. H., Kung H. J., Majors J. E., Quintrell N., Guntaka R. V., Bishop J. M., Varmus H. E. Mapping unintegrated avian sarcoma virus DNA: termini of linear DNA bear 300 nucleotides present once or twice in two species of circular DNA. Cell. 1978 Dec;15(4):1383–1395. doi: 10.1016/0092-8674(78)90063-6. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Sternberg N., Tiemeier D., Enquist L. In vitro packaging of a lambda Dam vector containing EcoRI DNA fragments of Escherichia coli and phage P1. Gene. 1977 May;1(3-4):255–280. doi: 10.1016/0378-1119(77)90049-x. [DOI] [PubMed] [Google Scholar]
  35. Weiss S. R., Varmus H. E., Bishop J. M. The size and genetic composition of virus-specific RNAs in the cytoplasm of cells producing avian sarcoma-leukosis viruses. Cell. 1977 Dec;12(4):983–992. doi: 10.1016/0092-8674(77)90163-5. [DOI] [PubMed] [Google Scholar]
  36. Wilson S. H., Kuff E. L. A novel DNA polymerase activity found in association with intracisternal A-type particles. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1531–1536. doi: 10.1073/pnas.69.6.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]

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