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. 1984 Jun 1;159(6):1762–1777. doi: 10.1084/jem.159.6.1762

Chromosomal translocations activating myc sequences and transduction of v-abl are critical events in the rapid induction of plasmacytomas by pristane and abelson virus

PMCID: PMC2187320  PMID: 6202819

Abstract

Plasmacytomas with short latent periods can be induced in BALB/c mice by a single intraperitoneal (i.p.) injection of 0.5 ml pristane followed 20-40 d later by an injection of Abelson virus. The karyotypes of 18 such tumors were determined; 10 of these had rcpt 12;15, 5 had rcpt 6;15 and 3 had no translocations, but two of these have been shown to have interstitial deletions of chromosome 15. The specific breakpoints were the same as described in pristane-induced plasmacytomas, i.e., at 15D2 /3, 6C2 , and 12F2 . Near diploid karyotypes and trisomy of chromosome 11 were frequently seen. All of the Abelson-plus-pristane-induced plasmacytomas (ABPC) were studied as transplanted tumors, contained integrated v- abl sequences, and actively transcribed v- abl mRNA. All but one of these tumors contained abundant myc RNA transcripts. The shortness of the latent periods of the ABPC suggests that the rcpt 12;15 and rcpt 6;15 occur soon after pristane administration and are present at the time Abelson virus is introduced. In this form of plasmacytomagenesis , activated v- abl genes appear to bypass other genetic changes that require a much longer period of time in pristane plasmacytomagenesis . Nonetheless, the consistent finding of chromosome-15 alterations and abundant myc expression in these plasmacytomas emphasize the apparent need for multiple events even in the genesis of some tumors induced by rapid transforming viruses.

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Selected References

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  1. Abelson H. T., Rabstein L. S. Lymphosarcoma: virus-induced thymic-independent disease in mice. Cancer Res. 1970 Aug;30(8):2213–2222. [PubMed] [Google Scholar]
  2. Abrams H. D., Rohrschneider L. R., Eisenman R. N. Nuclear location of the putative transforming protein of avian myelocytomatosis virus. Cell. 1982 Jun;29(2):427–439. doi: 10.1016/0092-8674(82)90159-3. [DOI] [PubMed] [Google Scholar]
  3. Adams J. M., Gerondakis S., Webb E., Corcoran L. M., Cory S. Cellular myc oncogene is altered by chromosome translocation to an immunoglobulin locus in murine plasmacytomas and is rearranged similarly in human Burkitt lymphomas. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1982–1986. doi: 10.1073/pnas.80.7.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Adams J. M., Gerondakis S., Webb E., Mitchell J., Bernard O., Cory S. Transcriptionally active DNA region that rearranges frequently in murine lymphoid tumors. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6966–6970. doi: 10.1073/pnas.79.22.6966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Alitalo K., Ramsay G., Bishop J. M., Pfeifer S. O., Colby W. W., Levinson A. D. Identification of nuclear proteins encoded by viral and cellular myc oncogenes. Nature. 1983 Nov 17;306(5940):274–277. doi: 10.1038/306274a0. [DOI] [PubMed] [Google Scholar]
  6. Anderson P. N., Potter M. Induction of plasma cell tumours in BALB-c mice with 2,6,10,14-tetramethylpentadecane (pristane). Nature. 1969 Jun 7;222(5197):994–995. doi: 10.1038/222994a0. [DOI] [PubMed] [Google Scholar]
  7. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  8. Calame K., Kim S., Lalley P., Hill R., Davis M., Hood L. Molecular cloning of translocations involving chromosome 15 and the immunoglobulin C alpha gene from chromosome 12 in two murine plasmacytomas. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6994–6998. doi: 10.1073/pnas.79.22.6994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cancro M., Potter M. The requirement of an adherent cell substratum for the growth of developing plasmacytoma cells in vivo. J Exp Med. 1976 Dec 1;144(6):1554–1567. doi: 10.1084/jem.144.6.1554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cooper G. M., Neiman P. E. Transforming genes of neoplasms induced by avian lymphoid leukosis viruses. Nature. 1980 Oct 16;287(5783):656–659. doi: 10.1038/287656a0. [DOI] [PubMed] [Google Scholar]
  11. Crews S., Barth R., Hood L., Prehn J., Calame K. Mouse c-myc oncogene is located on chromosome 15 and translocated to chromosome 12 in plasmacytomas. Science. 1982 Dec 24;218(4579):1319–1321. doi: 10.1126/science.7146913. [DOI] [PubMed] [Google Scholar]
  12. Dalla-Favera R., Martinotti S., Gallo R. C., Erikson J., Croce C. M. Translocation and rearrangements of the c-myc oncogene locus in human undifferentiated B-cell lymphomas. Science. 1983 Feb 25;219(4587):963–967. doi: 10.1126/science.6401867. [DOI] [PubMed] [Google Scholar]
  13. Donner P., Bunte T., Greiser-Wilke I., Moelling K. Decreased DNA-binding ability of purified transformation-specific proteins from deletion mutants of the acute avian leukemia virus MC29. Proc Natl Acad Sci U S A. 1983 May;80(10):2861–2865. doi: 10.1073/pnas.80.10.2861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Erikson J., ar-Rushdi A., Drwinga H. L., Nowell P. C., Croce C. M. Transcriptional activation of the translocated c-myc oncogene in burkitt lymphoma. Proc Natl Acad Sci U S A. 1983 Feb;80(3):820–824. doi: 10.1073/pnas.80.3.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goubin G., Goldman D. S., Luce J., Neiman P. E., Cooper G. M. Molecular cloning and nucleotide sequence of a transforming gene detected by transfection of chicken B-cell lymphoma DNA. Nature. 1983 Mar 10;302(5904):114–119. doi: 10.1038/302114a0. [DOI] [PubMed] [Google Scholar]
  16. Grunwald D. J., Dale B., Dudley J., Lamph W., Sugden B., Ozanne B., Risser R. Loss of viral gene expression and retention of tumorigenicity by Abelson lymphoma cells. J Virol. 1982 Jul;43(1):92–103. doi: 10.1128/jvi.43.1.92-103.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Harris L. J., D'Eustachio P., Ruddle F. H., Marcu K. B. DNA sequence associated with chromosome translocations in mouse plasmacytomas. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6622–6626. doi: 10.1073/pnas.79.21.6622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Harris L. J., Lang R. B., Marcu K. B. Non-immunoglobulin-associated DNA rearrangements in mouse plasmacytomas. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4175–4179. doi: 10.1073/pnas.79.13.4175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Klein G., Ohno S., Rosenberg N., Wiener F., Spira J., Baltimore D. Cytogenetic studies on abelson-virus-induced mouse leukemias. Int J Cancer. 1980 Jun 15;25(6):805–811. doi: 10.1002/ijc.2910250617. [DOI] [PubMed] [Google Scholar]
  20. Land H., Parada L. F., Weinberg R. A. Cellular oncogenes and multistep carcinogenesis. Science. 1983 Nov 18;222(4625):771–778. doi: 10.1126/science.6356358. [DOI] [PubMed] [Google Scholar]
  21. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  22. Marcu K. B., Harris L. J., Stanton L. W., Erikson J., Watt R., Croce C. M. Transcriptionally active c-myc oncogene is contained within NIARD, a DNA sequence associated with chromosome translocations in B-cell neoplasia. Proc Natl Acad Sci U S A. 1983 Jan;80(2):519–523. doi: 10.1073/pnas.80.2.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mushinski J. F., Bauer S. R., Potter M., Reddy E. P. Increased expression of myc-related oncogene mRNA characterizes most BALB/c plasmacytomas induced by pristane or Abelson murine leukemia virus. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1073–1077. doi: 10.1073/pnas.80.4.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mushinski J. F., Potter M., Bauer S. R., Reddy E. P. DNA rearrangement and altered RNA expression of the c-myb oncogene in mouse plasmacytoid lymphosarcomas. Science. 1983 May 20;220(4599):795–798. doi: 10.1126/science.6687762. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Nesbitt M. N., Francke U. A system of nomenclature for band patterns of mouse chromosomes. Chromosoma. 1973;41(2):145–158. doi: 10.1007/BF00319691. [DOI] [PubMed] [Google Scholar]
  27. Ohno S., Babonits M., Wiener F., Spira J., Klein G., Potter M. Nonrandom chromosome changes involving the Ig gene-carrying chromosomes 12 and 6 in pristane-induced mouse plasmacytomas. Cell. 1979 Dec;18(4):1001–1007. doi: 10.1016/0092-8674(79)90212-5. [DOI] [PubMed] [Google Scholar]
  28. POTTER M., MACCARDLE R. C. HISTOLOGY OF DEVELOPING PLASMA CELL NEOPLASIA INDUCED BY MINERAL OIL IN BALB/C MICE. J Natl Cancer Inst. 1964 Sep;33:497–515. [PubMed] [Google Scholar]
  29. Payne G. S., Bishop J. M., Varmus H. E. Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas. Nature. 1982 Jan 21;295(5846):209–214. doi: 10.1038/295209a0. [DOI] [PubMed] [Google Scholar]
  30. Polsky F., Edgell M. H., Seidman J. G., Leder P. High capacity gel preparative electrophoresis for purification of fragments of genomic DNA. Anal Biochem. 1978 Jul 1;87(2):397–410. doi: 10.1016/0003-2697(78)90689-9. [DOI] [PubMed] [Google Scholar]
  31. Potter M., Sklar M. D., Rowe W. P. Rapid viral induction of plasmacytomas in pristane-primed BALB-c mice. Science. 1973 Nov 9;182(4112):592–594. doi: 10.1126/science.182.4112.592. [DOI] [PubMed] [Google Scholar]
  32. Potter M., Wax J. S. Peritoneal plasmacytomagenesis in mice: comparison of different pristane dose regimens. J Natl Cancer Inst. 1983 Aug;71(2):391–395. [PubMed] [Google Scholar]
  33. Rechavi G., Givol D., Canaani E. Activation of a cellular oncogene by DNA rearrangement: possible involvement of an IS-like element. Nature. 1982 Dec 16;300(5893):607–611. doi: 10.1038/300607a0. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Risser R., Potter M., Rowe W. P. Abelson virus-induced lymphomagenesis in mice. J Exp Med. 1978 Sep 1;148(3):714–726. doi: 10.1084/jem.148.3.714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Risser R. The pathogenesis of Abelson virus lymphomas of the mouse. Biochim Biophys Acta. 1982 Jun 28;651(4):213–244. doi: 10.1016/0304-419x(82)90013-0. [DOI] [PubMed] [Google Scholar]
  37. Rosenberg N. Abelson leukemia virus. Curr Top Microbiol Immunol. 1982;101:95–126. doi: 10.1007/978-3-642-68654-2_5. [DOI] [PubMed] [Google Scholar]
  38. Ruley H. E. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature. 1983 Aug 18;304(5927):602–606. doi: 10.1038/304602a0. [DOI] [PubMed] [Google Scholar]
  39. Shen-Ong G. L., Keath E. J., Piccoli S. P., Cole M. D. Novel myc oncogene RNA from abortive immunoglobulin-gene recombination in mouse plasmacytomas. Cell. 1982 Dec;31(2 Pt 1):443–452. doi: 10.1016/0092-8674(82)90137-4. [DOI] [PubMed] [Google Scholar]
  40. Srinivasan A., Reddy E. P., Aaronson S. A. Abelson murine leukemia virus: molecular cloning of infectious integrated proviral DNA. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2077–2081. doi: 10.1073/pnas.78.4.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stanton L. W., Watt R., Marcu K. B. Translocation, breakage and truncated transcripts of c-myc oncogene in murine plasmacytomas. Nature. 1983 Jun 2;303(5916):401–406. doi: 10.1038/303401a0. [DOI] [PubMed] [Google Scholar]
  42. Sümegi J., Spira J., Bazin H., Szpirer J., Levan G., Klein G. Rat c-myc oncogene is located on chromosome 7 and rearranges in immunocytomas with t(6:7) chromosomal translocation. Nature. 1983 Dec 1;306(5942):497–498. doi: 10.1038/306497a0. [DOI] [PubMed] [Google Scholar]
  43. Wang H. C., Fedoroff S. Banding in human chromosomes treated with trypsin. Nat New Biol. 1972 Jan 12;235(54):52–54. doi: 10.1038/newbio235052a0. [DOI] [PubMed] [Google Scholar]
  44. Wiener F., Babonits M., Spira J., Klein G., Potter M. Cytogenetic studies on IgA/lambda-producing murine plasmacytomas: regular occurrence of a T(12;15) translocation. Somatic Cell Genet. 1980 Nov;6(6):731–738. doi: 10.1007/BF01538972. [DOI] [PubMed] [Google Scholar]
  45. Wiener F., Ohno S., Babonits M., Sümegi J., Wirschubsky Z., Klein G., Mushinski J. F., Potter M. Hemizygous interstitial deletion of chromosome 15 (band D) in three translocation-negative murine plasmacytomas. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1159–1163. doi: 10.1073/pnas.81.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yoshida M. C., Moriwaki K., Migita S. Specificity of the deletion of chromosome No. 15 in mouse plasmacytoma: brief communication. J Natl Cancer Inst. 1978 Jan;60(1):235–238. doi: 10.1093/jnci/60.1.235. [DOI] [PubMed] [Google Scholar]
  47. Yu R. L., Aronson M. M., Nichols W. W. High-resolution bands in human fibroblast chromosomes induced by actinomycin D. Cytogenet Cell Genet. 1981;31(2):111–114. doi: 10.1159/000131634. [DOI] [PubMed] [Google Scholar]

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