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. 1982 Dec;79(24):7842–7846. doi: 10.1073/pnas.79.24.7842

Two human c-onc genes are located on the long arm of chromosome 8.

B G Neel, S C Jhanwar, R S Chaganti, W S Hayward
PMCID: PMC347445  PMID: 6961456

Abstract

We have used in situ chromosome hybridization techniques to map the human cellular counterparts (c-onc genes) of the transforming genes of two RNA tumor viruses on human meiotic pachytene and somatic metaphase chromosomes. We find that the human c-mos gene is located on chromosome 8 at a position corresponding to band 8q22 on the somatic map. The human c-myc gene is found on chromosome 8 at position 8q24. These regions on the long arm of chromosome 8 have been previously reported to be involved in specific translocations found in the M-2 subset of acute nonlymphoblastic leukemias. Burkitt lymphoma, and other forms of non-Hodgkin lymphoma, and a familial abnormality that predisposes to renal cell carcinoma. These results suggest that translocations of the human c-mos or c-myc genes may be causally related to neoplastic transformation.

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Selected References

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  1. Berger R., Bernheim A., Weh H. J., Flandrin G., Daniel M. T., Brouet J. C., Colbert N. A new translocation in Burkitt's tumor cells. Hum Genet. 1979;53(1):111–112. doi: 10.1007/BF00289460. [DOI] [PubMed] [Google Scholar]
  2. Blair D. G., Oskarsson M., Wood T. G., McClements W. L., Fischinger P. J., Vande Woude G. G. Activation of the transforming potential of a normal cell sequence: a molecular model for oncogenesis. Science. 1981 May 22;212(4497):941–943. doi: 10.1126/science.7233190. [DOI] [PubMed] [Google Scholar]
  3. Chandler M. E., Yunis J. J. A high resolution in situ hybridization technique for the direct visualization of labeled G-banded early metaphase and prophase chromosomes. Cytogenet Cell Genet. 1978;22(1-6):352–356. doi: 10.1159/000130970. [DOI] [PubMed] [Google Scholar]
  4. Chang E. H., Furth M. E., Scolnick E. M., Lowy D. R. Tumorigenic transformation of mammalian cells induced by a normal human gene homologous to the oncogene of Harvey murine sarcoma virus. Nature. 1982 Jun 10;297(5866):479–483. doi: 10.1038/297479a0. [DOI] [PubMed] [Google Scholar]
  5. Cohen A. J., Li F. P., Berg S., Marchetto D. J., Tsai S., Jacobs S. C., Brown R. S. Hereditary renal-cell carcinoma associated with a chromosomal translocation. N Engl J Med. 1979 Sep 13;301(11):592–595. doi: 10.1056/NEJM197909133011107. [DOI] [PubMed] [Google Scholar]
  6. 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. doi: 10.1038/298679a0. [DOI] [PubMed] [Google Scholar]
  7. Cooper G. M., Neiman P. E. Two distinct candidate transforming genes of lymphoid leukosis virus-induced neoplasms. Nature. 1981 Aug 27;292(5826):857–858. doi: 10.1038/292857a0. [DOI] [PubMed] [Google Scholar]
  8. Croce C. M., Shander M., Martinis J., Cicurel L., D'Ancona G. G., Dolby T. W., Koprowski H. Chromosomal location of the genes for human immunoglobulin heavy chains. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3416–3419. doi: 10.1073/pnas.76.7.3416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dalla-Favera R., Franchini G., Martinotti S., Wong-Staal F., Gallo R. C., Croce C. M. Chromosomal assignment of the human homologues of feline sarcoma virus and avian myeloblastosis virus onc genes. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4714–4717. doi: 10.1073/pnas.79.15.4714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dalla-Favera R., Wong-Staal F., Gallo R. C. 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. doi: 10.1038/299061a0. [DOI] [PubMed] [Google Scholar]
  11. DeFeo D., Gonda M. A., Young H. A., Chang E. H., Lowy D. R., Scolnick E. M., Ellis R. W. Analysis of two divergent rat genomic clones homologous to the transforming gene of Harvey murine sarcoma virus. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3328–3332. doi: 10.1073/pnas.78.6.3328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Der C. J., Krontiris T. G., Cooper G. M. Transforming genes of human bladder and lung carcinoma cell lines are homologous to the ras genes of Harvey and Kirsten sarcoma viruses. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3637–3640. doi: 10.1073/pnas.79.11.3637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Erikson J., Martinis J., Croce C. M. Assignment of the genes for human lambda immunoglobulin chains to chromosome 22. Nature. 1981 Nov 12;294(5837):173–175. doi: 10.1038/294173a0. [DOI] [PubMed] [Google Scholar]
  14. Fung Y. K., Fadly A. M., Crittenden L. B., Kung H. J. On the mechanism of retrovirus-induced avian lymphoid leukosis: deletion and integration of the proviruses. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3418–3422. doi: 10.1073/pnas.78.6.3418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gerhard D. S., Kawasaki E. S., Bancroft F. C., Szabo P. Localization of a unique gene by direct hybridization in situ. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3755–3759. doi: 10.1073/pnas.78.6.3755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hanafusa H. Cellular origin of transforming genes of RNA tumor viruses. Harvey Lect. 1979 1980;75:255–275. [PubMed] [Google Scholar]
  17. Harper M. E., Saunders G. F. Localization of single copy DNA sequences of G-banded human chromosomes by in situ hybridization. Chromosoma. 1981;83(3):431–439. doi: 10.1007/BF00327364. [DOI] [PubMed] [Google Scholar]
  18. Harper M. E., Ullrich A., Saunders G. F. Localization of the human insulin gene to the distal end of the short arm of chromosome 11. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4458–4460. doi: 10.1073/pnas.78.7.4458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Henderson A. S., Yu M. T., Atwood K. C. The localization of mouse globin genes: a test of the effectiveness of hybridization in situ. Cytogenet Cell Genet. 1978;21(4):231–240. doi: 10.1159/000130899. [DOI] [PubMed] [Google Scholar]
  21. Hobart M. J., Rabbitts T. H., Goodfellow P. N., Solomon E., Chambers S., Spurr N., Povey S. Immunoglobulin heavy chain genes in humans are located on chromosome. Ann Hum Genet. 1981 Oct;45(Pt 4):331–335. doi: 10.1111/j.1469-1809.1981.tb00346.x. [DOI] [PubMed] [Google Scholar]
  22. Jhanwar S. C., Burns J. P., Alonso M. L., Hew W., Chaganti R. S. Mid-pachytene chromomere maps of human autosomes. Cytogenet Cell Genet. 1982;33(3):240–248. doi: 10.1159/000131760. [DOI] [PubMed] [Google Scholar]
  23. Jhanwar S. C., Chaganti R. S. Pachytene chromomere maps of Chinese hamster autosomes. Cytogenet Cell Genet. 1981;31(2):70–76. doi: 10.1159/000131627. [DOI] [PubMed] [Google Scholar]
  24. Jhanwar S. C., Prensky W., Chaganti R. S. Localization and metabolic activity of ribosomal genes in Chinese hamster meiotic and mitotic chromosomes. Cytogenet Cell Genet. 1981;30(1):39–46. doi: 10.1159/000131586. [DOI] [PubMed] [Google Scholar]
  25. Kirsch I. R., Morton C. C., 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. doi: 10.1126/science.6801764. [DOI] [PubMed] [Google Scholar]
  26. Klein G. The role of gene dosage and genetic transpositions in carcinogenesis. Nature. 1981 Nov 26;294(5839):313–318. doi: 10.1038/294313a0. [DOI] [PubMed] [Google Scholar]
  27. Lautenberger J. A., Schulz R. A., Garon C. F., Tsichlis P. N., Papas T. S. Molecular cloning of avian myelocytomatosis virus (MC29) transforming sequences. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1518–1522. doi: 10.1073/pnas.78.3.1518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lenoir G. M., Preud'homme J. L., 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. doi: 10.1038/298474a0. [DOI] [PubMed] [Google Scholar]
  29. Malcolm S., Barton P., Murphy C., Ferguson-Smith M. A., Bentley D. L., Rabbitts T. H. 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. doi: 10.1073/pnas.79.16.4957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Manolov G., Manolova Y. Marker band in one chromosome 14 from Burkitt lymphomas. Nature. 1972 May 5;237(5349):33–34. doi: 10.1038/237033a0. [DOI] [PubMed] [Google Scholar]
  32. 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. doi: 10.1111/j.1601-5223.1979.tb01288.x. [DOI] [PubMed] [Google Scholar]
  33. Mitelman F. Marker chromosome 14q + in human cancer and leukemia. Adv Cancer Res. 1981;34:141–170. [PubMed] [Google Scholar]
  34. 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. doi: 10.1007/BF01968217. [DOI] [PubMed] [Google Scholar]
  35. Neel B. G., Gasic G. P., Rogler C. E., Skalka A. M., Ju G., Hishinuma F., Papas T., Astrin S. M., Hayward W. S. Molecular analysis of the c-myc locus in normal tissue and in avian leukosis virus-induced lymphomas. J Virol. 1982 Oct;44(1):158–166. doi: 10.1128/jvi.44.1.158-166.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Oskarsson M., McClements W. L., Blair D. G., Maizel J. V., Vande Woude G. F. Properties of a normal mouse cell DNA sequence (sarc) homologous to the src sequence of Moloney sarcoma virus. Science. 1980 Mar 14;207(4436):1222–1224. doi: 10.1126/science.6243788. [DOI] [PubMed] [Google Scholar]
  38. Parada L. F., Tabin C. J., Shih C., Weinberg R. A. Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature. 1982 Jun 10;297(5866):474–478. doi: 10.1038/297474a0. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Prakash K., McBride O. W., Swan D. C., Devare S. G., Tronick S. R., Aaronson S. A. Molecular cloning and chromosomal mapping of a human locus related to the transforming gene of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5210–5214. doi: 10.1073/pnas.79.17.5210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Reichmann A., Martin P., Levin B. Chromosomal banding patterns in human large bowel cancer. Int J Cancer. 1981 Oct 15;28(4):431–440. doi: 10.1002/ijc.2910280407. [DOI] [PubMed] [Google Scholar]
  42. Robins D. M., Ripley S., Henderson A. S., Axel R. Transforming DNA integrates into the host chromosome. Cell. 1981 Jan;23(1):29–39. doi: 10.1016/0092-8674(81)90267-1. [DOI] [PubMed] [Google Scholar]
  43. 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. doi: 10.1128/jvi.41.2.635-642.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Rowley J. D. Identificaton of a translocation with quinacrine fluorescence in a patient with acute leukemia. Ann Genet. 1973 Jun;16(2):109–112. [PubMed] [Google Scholar]
  45. Santos E., Tronick S. R., Aaronson S. A., Pulciani S., Barbacid M. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature. 1982 Jul 22;298(5872):343–347. doi: 10.1038/298343a0. [DOI] [PubMed] [Google Scholar]
  46. Swan D. C., McBride O. W., Robbins K. C., Keithley D. A., Reddy E. P., Aaronson S. A. Chromosomal mapping of the simian sarcoma virus onc gene analogue in human cells. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4691–4695. doi: 10.1073/pnas.79.15.4691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tereba A., Lai M. M., Murti K. G. Chromosome 1 contains the endogenous RAV-0 retrovirus sequences in chicken cells. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6486–6490. doi: 10.1073/pnas.76.12.6486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wahl G. M., Vitto L., Padgett R. A., Stark G. R. Single-copy and amplified CAD genes in Syrian hamster chromosomes localized by a highly sensitive method for in situ hybridization. Mol Cell Biol. 1982 Mar;2(3):308–319. doi: 10.1128/mcb.2.3.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Watson R., Oskarsson M., Vande Woude G. F. Human DNA sequence homologous to the transforming gene (mos) of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4078–4082. doi: 10.1073/pnas.79.13.4078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Westin E. H., Wong-Staal F., Gelmann E. P., Dalla-Favera R., Papas T. S., Lautenberger J. A., Eva A., Reddy E. P., Tronick S. R., Aaronson S. A. Expression of cellular homologues of retroviral onc genes in human hematopoietic cells. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2490–2494. doi: 10.1073/pnas.79.8.2490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Whang-Peng J., Kao-Shan C. S., Lee E. C., Bunn P. A., Carney D. N., Gazdar A. F., Minna J. D. Specific chromosome defect associated with human small-cell lung cancer; deletion 3p(14-23). Science. 1982 Jan 8;215(4529):181–182. doi: 10.1126/science.6274023. [DOI] [PubMed] [Google Scholar]
  52. Yunis J. J., Bloomfield C. D., Ensrud K. All patients with acute nonlymphocytic leukemia may have a chromosomal defect. N Engl J Med. 1981 Jul 16;305(3):135–139. doi: 10.1056/NEJM198107163050304. [DOI] [PubMed] [Google Scholar]
  53. 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. doi: 10.1002/ijc.2910170108. [DOI] [PubMed] [Google Scholar]

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