Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. (original) (raw)

• Journal List
• Proc Natl Acad Sci U S A
• v.79(24); 1982 Dec
• PMC347444

Proc Natl Acad Sci U S A. 1982 Dec; 79(24): 7837–7841.

Abstract

The consistent appearance of specific chromosomal translocations in human Burkitt lymphomas and murine plasmacytomas has suggested that these translocations might play a role in malignant transformation. Here we show that transformation of these cells is frequently accompanied by the somatic rearrangement of a cellular analogue of an avian retrovirus transforming gene, c-myc. Moreover, we map c-myc to human chromosome 8 band q24, the chromosomal segment involved in the reciprocal Burkitt translocations [t(8;14), t(8;22) and t(2;8)]. In two t(8;14) human Burkitt cell lines, c-myc appears to have been translocated directly into a DNA restriction fragment that also encodes the immunoglobulin mu chain gene. In the case of a specific cloned fragment of DNA derived from a mouse plasmacytoma, we demonstrate directly that c-myc has been translocated into the immunoglobulin alpha switch region. Our data provide a molecular basis for considering the role that specific translocations might play in malignant transformation.

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• Klein G. The role of gene dosage and genetic transpositions in carcinogenesis. Nature. 1981 Nov 26;294(5839):313–318. [PubMed] [Google Scholar]
• Rowley JD. Identification of the constant chromosome regions involved in human hematologic malignant disease. Science. 1982 May 14;216(4547):749–751. [PubMed] [Google Scholar]
• Manolov G, Manolova Y. Marker band in one chromosome 14 from Burkitt lymphomas. Nature. 1972 May 5;237(5349):33–34. [PubMed] [Google Scholar]
• Zech L, Haglund U, Nilsson K, Klein G. Characteristic chromosomal abnormalities in biopsies and lymphoid-cell lines from patients with Burkitt and non-Burkitt lymphomas. Int J Cancer. 1976 Jan 15;17(1):47–56. [PubMed] [Google Scholar]
• Manolova Y, Manolov G, Kieler J, Levan A, Klein G. Genesis of the 14q+ marker in Burkitt's lymphoma. Hereditas. 1979;90(1):5–10. [PubMed] [Google Scholar]
• Miyoshi I, Hamasaki K, Miyamoto K, Nagase K, Narahara K, Kitajima K, Kimura I, Sato J. Chromosome translocations in Burkitt's lymphoma. N Engl J Med. 1981 Mar 19;304(12):734–734. [PubMed] [Google Scholar]
• Bernheim A, Berger R, Lenoir G. Cytogenetic studies on African Burkitt's lymphoma cell lines: t(8;14), t(2;8) and t(8;22) translocations. Cancer Genet Cytogenet. 1981 Jun;3(4):307–315. [PubMed] [Google Scholar]
• Mitelman F. Marker chromosome 14q + in human cancer and leukemia. Adv Cancer Res. 1981;34:141–170. [PubMed] [Google Scholar]
• Lenoir GM, Preud'homme JL, Bernheim A, Berger R. Correlation between immunoglobulin light chain expression and variant translocation in Burkitt's lymphoma. Nature. 1982 Jul 29;298(5873):474–476. [PubMed] [Google Scholar]
• Miyoshi I, Hiraki S, Kimura I, Miyamoto K, Sato J. 2/8 translocation in a Japanese Burkitt's lymphoma. Experientia. 1979 Jun 15;35(6):742–743. [PubMed] [Google Scholar]
• Berger R, Bernheim A, Weh HJ, Flandrin G, Daniel MT, Brouet JC, Colbert N. A new translocation in Burkitt's tumor cells. Hum Genet. 1979;53(1):111–112. [PubMed] [Google Scholar]
• 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. [PubMed] [Google Scholar]
• Wiener F, Fenyö EM, Klein G, Davies AJ. Tumor-host cell hybrids in radiochimeras reconstituted with bone marrow and thymus grafts. Somatic Cell Genet. 1976 Mar;2(2):81–92. [PubMed] [Google Scholar]
• Kirsch IR, Morton CC, Nakahara K, Leder P. Human immunoglobulin heavy chain genes map to a region of translocations in malignant B lymphocytes. Science. 1982 Apr 16;216(4543):301–303. [PubMed] [Google Scholar]
• Malcolm S, Barton P, Murphy C, Ferguson-Smith MA, Bentley DL, Rabbitts TH. Localization of human immunoglobulin kappa light chain variable region genes to the short arm of chromosome 2 by in situ hybridization. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4957–4961. [PMC free article] [PubMed] [Google Scholar]
• Kirsch IR, Ravetch JV, Kwan SP, Max EE, Ney RL, Leder P. Multiple immunoglobulin switch region homologies outside the heavy chain constant region locus. Nature. 1981 Oct 15;293(5833):585–587. [PubMed] [Google Scholar]
• Robins T, Bister K, Garon C, Papas T, Duesberg P. Structural relationship between a normal chicken DNA locus and the transforming gene of the avian acute leukemia virus MC29. J Virol. 1982 Feb;41(2):635–642. [PMC free article] [PubMed] [Google Scholar]
• Lautenberger JA, Schulz RA, Garon CF, Tsichlis PN, Papas TS. Molecular cloning of avian myelocytomatosis virus (MC29) transforming sequences. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1518–1522. [PMC free article] [PubMed] [Google Scholar]
• Lenoir GM, Preud'homme JL, Bernheim A, Berger R. Correlation between immunoglobulin light chain expression and variant translocation in Burkitt's lymphoma. Nature. 1982 Jul 29;298(5873):474–476. [PubMed] [Google Scholar]
• Harper ME, Saunders GF. Localization of single copy DNA sequences of G-banded human chromosomes by in situ hybridization. Chromosoma. 1981;83(3):431–439. [PubMed] [Google Scholar]
• Hieter PA, Hollis GF, Korsmeyer SJ, Waldmann TA, Leder P. Clustered arrangement of immunoglobulin lambda constant region genes in man. Nature. 1981 Dec 10;294(5841):536–540. [PubMed] [Google Scholar]
• Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [PubMed] [Google Scholar]
• Harris LJ, Lang RB, Marcu KB. Non-immunoglobulin-associated DNA rearrangements in mouse plasmacytomas. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4175–4179. [PMC free article] [PubMed] [Google Scholar]
• Hayward WS, Neel BG, Astrin SM. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. [PubMed] [Google Scholar]
• Meo T, Johnson J, Beechey CV, Andrews SJ, Peters J, Searle AG. Linkage analyses of murine immunoglobulin heavy chain and serum prealbumin genes establish their location on chromosome 12 proximal to the T (5;12) 31H breakpoint in band 12F1. Proc Natl Acad Sci U S A. 1980 Jan;77(1):550–553. [PMC free article] [PubMed] [Google Scholar]
• Eva A, Robbins KC, Andersen PR, Srinivasan A, Tronick SR, Reddy EP, Ellmore NW, Galen AT, Lautenberger JA, Papas TS, et al. Cellular genes analogous to retroviral onc genes are transcribed in human tumour cells. Nature. 1982 Jan 14;295(5845):116–119. [PubMed] [Google Scholar]
• Dalla-Favera R, Wong-Staal F, Gallo RC. Onc gene amplification in promyelocytic leukaemia cell line HL-60 and primary leukaemic cells of the same patient. Nature. 1982 Sep 2;299(5878):61–63. [PubMed] [Google Scholar]
• Collins S, Groudine M. Amplification of endogenous myc-related DNA sequences in a human myeloid leukaemia cell line. Nature. 1982 Aug 12;298(5875):679–681. [PubMed] [Google Scholar]
• Ravetch JV, Siebenlist U, Korsmeyer S, Waldmann T, Leder P. Structure of the human immunoglobulin mu locus: characterization of embryonic and rearranged J and D genes. Cell. 1981 Dec;27(3 Pt 2):583–591. [PubMed] [Google Scholar]
• Ramsay G, Graf T, Hayman MJ. Mutants of avian myelocytomatosis virus with smaller gag gene-related proteins have an altered transforming ability. Nature. 1980 Nov 13;288(5787):170–172. [PubMed] [Google Scholar]
• Dalla-Favera R, Bregni M, Erikson J, Patterson D, Gallo RC, Croce CM. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7824–7827. [PMC free article] [PubMed] [Google Scholar]

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