Journal of Clinical Immunology

, Volume 5, Issue 2, pp 65–77 | Cite as

The role of c-myc in the proliferation of normal and neoplastic cells

  • Kathleen Kelly
  • Ulrich Siebenlist
Special Article

Key words

c-myc oncogenes Burkitt's lymphoma proliferation growth factors 

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References

  1. 1.
    Bishop JM: Cellular oncogenes and retroviruses. Annu Rev Biochem 52:301–354, 1983Google Scholar
  2. 2.
    Duesberg PH: Retroviral transforming genes in normal cells? Nature 304:219–226, 1983Google Scholar
  3. 3.
    Land H, Luis PF, Weinberg RA: Cellular oncogenes and multistep carcinogenesis. Science 222:771–778, 1983Google Scholar
  4. 4.
    Weinberg RA: Oncogenes of spontaneous and chemically-induced tumors. Adv Cancer Res 36:149–163, 1982Google Scholar
  5. 5.
    Lautenberger JA, Schulz RA, Garon CF, Tsichilis PN, Papas TS: Molecular cloning of avian myelocytomatosis virus (MC29) transforming sequences. Proc Natl Acad Sci USA 78:1518–1522, 1981Google Scholar
  6. 6.
    Goubin G, Goldman DS, Luce J, Neiman PE, Cooper GM: Molecular cloning and nucleotide sequence of a transforming gene detected by transfection of B-cell lymphoma DNA. Nature 302:114–119, 1983Google Scholar
  7. 7.
    Diamond A, Cooper GM, Ritz J, Lane MA: Identification and molecular cloning of the human Blym transforming gene activated in Burkitt's lymphomas. Nature 305:112–116, 1983Google Scholar
  8. 8.
    Lane MA, Sainten A, Doherty KM, Cooper GM: Isolation and characterization of a stage-specific transforming gene, Tlym-1, from T cell lymphomas. Proc Natl Acad Sci USA 81:227–2231, 1984Google Scholar
  9. 9.
    Lane MA, Stephens HAF, Doherty KM, Tobin MB: Tlym-1, a stage specific transforming gene shares homology with MHC I region genes.In Oncogenes in B-Cell Neoplasia, M Potter, F Melchers, M Weigert (eds). Heidelberg, Springer-Verlag, 1984, pp 31–33Google Scholar
  10. 10.
    Cooper CS, Park M, Blair DG, Tainsky MA, Huebner K, Croce CM, Vande Woude GF: Molecular cloning of a new transforming gene from a chemically transformed human cell line. Nature 311:29–33, 1984Google Scholar
  11. 11.
    Hayward WS, Neel BG, Astrin SM: Activation of cellular oncogenes by promoter insertion in ALV-induced lymphoid leukosis. Nature 296:475–479, 1981Google Scholar
  12. 12.
    Fung, YK, Lewis WG, Crittenden LB, Kung HJ: Activation of the cellular oncogene c-erbB by LTR insertion: MOlecular basis for induction of erythroblastosis by avian leukosis virus. Cell 33:357–368, 1983Google Scholar
  13. 13.
    Corcoran LM, Adams JM, Dunn AR, Cory S: Murine T lymphomas in which the cellular myc oncogene has been activated by retroviral insertion. Cell 37:113–122, 1984Google Scholar
  14. 14.
    Mushinski JF, Potter M, Bauer SR, Reddy EP: DNA rear-rangement and altered RNA expression of the c-myb oncogene in mouse plasmacytoid lymphosarcomas. Science 220:795–798, 1983Google Scholar
  15. 15.
    Shen-Ong GLC, Reddy EP, Potter M, Mushinski F: Disruption and activation of the c-myb locus by M-MuL V insertion in plasmacytoid lymphosarcomas induced by pristane and abelson viruses.In Oncogenes in B-cell Neoplasia, M Potter, F Melchers, M Weigert (eds). Heidelberg, Springer-Verlag, 1984, pp 41–46Google Scholar
  16. 16.
    Nusse R, Varmus HE: Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31:99–109, 1982Google Scholar
  17. 17.
    Peters G, Brookes S, Smith R, Dickson C: Tumorigenesis by mouse mammary tumor virus: Evidence for a common region for provirus integration in mammary tumors. Cell 33:369–377, 1983Google Scholar
  18. 18.
    Cuypers HT, Selten G, Quint W, Zijlstra M, Maandag ER, Boelens W, van Wezenbeck P, Melief C, Berns A: Murine leukemia virus-induced T cell lymphomagenesis: Integration of proviruses in a distinct chromosomal region. Cell 37:141–150, 1984Google Scholar
  19. 19.
    Hoffman-Falk H, Einat P, Shilo BZ, Hoffmann FM: Drosophila melanogaster DNA clones homologous to vertebrate oncogenes: Evidence for a common ancestor to the src and abl cellular genes. Cell 32:589–598, 1983Google Scholar
  20. 20.
    Powers S, Kataoka T, Fasano O, Goldfarb M, Strathern J, Broach J, Wigler M: Genes in S. cerevisiae encoding proteins with domains homologous to the mammalian ras proteins. Cell 36:607–612, 1984Google Scholar
  21. 21.
    Hanafusa H: Cell Transformation by RNA tumor viruses.In Comprehensive Virology10, Fraenkel-Conrant, R Wagner (eds). New York, Academic Press, 1982, pp 401–483.Google Scholar
  22. 22.
    Quade K: Transformation of mammalian cells by avian myelocytomatosis virus and avian erythroblastosis virus. Virology 98:461–465, 1979Google Scholar
  23. 23.
    Mladenov Z, Heine J, Beard D, Beard JW: Strain MC29 avian leukosis virus. Myelocytoma, endothelioma, and renal growths: Pathomorphological and ultrastructural aspects. J Natl Cancer Inst 38:251–285, 1967Google Scholar
  24. 24.
    Persson H, Leder P: Nuclear localization and DNA binding properties of protein expressed by human c-myc oncogene. Science 225:718–721, 1984Google Scholar
  25. 25.
    Muller R, Slamon DJ, Trmblay JM, Cline MJ, Verma IM: Differential expression of cellular oncogenes during pre- and postnatal development of the mouse. Nature 299:640–644, 1982Google Scholar
  26. 26.
    Gonda RJ, Bishop JM: Structure and transcription of the cellular homolog (c-myb) of the avian myeloblastosis virus transforming gene (v-myb). J Virol 46:212–220, 1982Google Scholar
  27. 27.
    Cantrell DA, Smith KA: The interleukin-2 T-cell system: A new cell growth model. Science 224:1312–1316, 1984Google Scholar
  28. 28.
    Pardee AB: A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci USA 80:5592–5596, 1974Google Scholar
  29. 29.
    Waterfield MD, Scrace GT, Whittle N, Stroobant P, Johnson A, Wasteson A, Westermark B, Heldin CH, Huang JS, Deuel TF: Platelet-derived growth factor is structurally related to the putative transforming protein p28sis of simian sarcoma virus. Nature 304:35–39, 1983Google Scholar
  30. 30.
    Doolittle RF, Hunkapiller MW, Hood LE, Devare SG, Robbins KC, Aaronson SA, and Antoniades HN: Simian sarcoma virus oncogene, v-sis, is derived from the gene (or genes) encoding a platelet-derived growth factor. Science 221:275–277, 1983Google Scholar
  31. 31.
    Downward J, Yarden Y, Mayes E, Scrace G, Fotty N, Stockwell G, Ullrich A, Schlessinger J, Waterfield MD: Close similarity of epidermal growth factor receptor and v-erbB oncogenic protein sequences. Nature 307:521–527, 1984Google Scholar
  32. 32.
    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 3:307–315, 1981Google Scholar
  33. 33.
    Leder P, Battey J, Lenoir G, Moulding C, Murphy W, Potter H, Stewart T, Taub R: Translocations among antibody genes in human cancer. Science 222:765–771, 1983Google Scholar
  34. 34.
    Geser A, Lenior GM, Anvret M, Bornkaurm G, Klein G, Williams EM, Wright DM, De-The G: Epstein-Barr virus markers in a series of Burkitt's lymphomas from the West Nile District, Uganda. Eur J Cancer Clin Oncol 19:1393–1404, 1983Google Scholar
  35. 35.
    Lenoir GM, Land H, Parada LF, Cunningham JM, Weinberg RA: Activated oncogenes in Burkitt's lymphoma.In Oncogenes in B-cell Neoplasia, M Potter, F Melchers, M Weigert (eds). Heidelberg, Springer, 1983, pp 6–14.Google Scholar
  36. 36.
    Taub R, Kelly K, Battey J, Latt S, Lenoir GM, Tantrahavi U, Tu Z, Leder P: A novel alteration in the structure of an activated c-myc gene in a variant t(2;8) Burkitt lymphoma. Cell 37:511–520, 1984Google Scholar
  37. 37.
    Hollis GF, Mitchell KF, Battey J, Potter J, Taub R, Lenoir GM, Leder P: A variant translocation places the lambda immunoglobulin genes 3′ to the c-myc oncogene in Burkitt's lymphoma. Nature 307:752–755, 1984Google Scholar
  38. 38.
    Davis M, Malcolm S, Rabbitts TH: Chromosome translocation can occur on either side of the c-myc oncogene in Burkitt lymphoma cells. Nature 308:286–288, 1984Google Scholar
  39. 39.
    Erikson J, Nishikura K, ar-Rushdi A, Finan J, Emanuel B, Lenoir G, Nowell PC, Croce CM: Translocation of an immunoglobulin kappa locus to a region 3' of an unrearranged c-myc oncogene enhances c-myc transcription. Proc Natl Acad Sci USA 80:7581–7585, 1983Google Scholar
  40. 40.
    Croce CM, Thierfelder W, Erikson J, Nishikura K, Finan J, Lenoir GM, Nowell PD: Transcriptional activation of an unrearranged and untranslocated c-myc oncogene by translocation of a C lambda locus in Burkitt lymphoma. Proc Natl Acad Sci USA 80:6922–6926, 1983Google Scholar
  41. 41.
    Westin EH, Wong-Staal F, Gelmann EP, Dalla-Favera R, Papas T, Lautenberger JA, Eva A, Reddy EP, Tronick SR, Aaronson SA, Gallo RC: Expression of cellular homologs of retroviral onc genes in human hematopoietic cells. Proc Natl Acad Sci USA 79:2490–2494, 1982Google Scholar
  42. 42.
    Keath EJ, Kelekar A, Cole MD: Transcriptional activation of the translocated c-myc oncogene in mouse plasmacytomas: Similar RNA levels in tumor and proliferating normal cells. Cell 37:521–528, 1984Google Scholar
  43. 43.
    Bernard O, Cory S, Gerondakis S, Weff E, Adams JM: Sequence of the murine and human cellular myc oncogenes and two modes of myc transcription resulting from chromosome translocation in B lymphoid tumors. EMBO J 2:2375–2383, 1983Google Scholar
  44. 44.
    Erikson J, ar-Rushdi A, Drwinga HL, Nowell PC, Croce CM: Transcriptional activation of the translocated c-myc oncogene in Burkitt lymphoma. Proc Natl Acad Sci USA 80:820–824, 1983Google Scholar
  45. 45.
    Hamlyn PH, Rabbitts TH: Translocation joins c-myc and immunoglobulin gamma-1 genes in a Burkitt lymphoma revealing a third exon in the c-myc oncogene. Nature 304:135–139, 1983Google Scholar
  46. 46.
    Maguire RT, Robins TS, Thorgeirsson S, Heilman CA: Expression of cellular myc and mos genes in undifferentiated B cell lymphomas of Burkitt and non-Burkitt types. Proc Natl Acad Sci USA 80:1947–1950, 1983Google Scholar
  47. 47.
    Taub R, Moulding C, Battey J, Murphy W, Vasicek T, Lenoir GM, Leder P: Activation and somatic mutation of the translocated c-myc gene in Burkitt lymphoma cells. Cell 36:339–348, 1984Google Scholar
  48. 48.
    Gillies SD, Morrison SL, Oi VT, Tonegawa S: A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell 33:717–728, 1983Google Scholar
  49. 49.
    Banerji J, Olson L, Schaffner W: A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell 33:729–740, 1983Google Scholar
  50. 50.
    Battey J, Moulding C, Taub R, Murphy W, Stewart T, Potter H, Lenoir G, Leder P: The human c-myc oncogene: Structural consequences of translocation into the IgH in Burkitt lymphoma. Cell 34:779–789, 1983Google Scholar
  51. 51.
    Rabbitts TH, Hamlyn PH, Baer R: Altered nucleotide sequence of a translocated c-myc gene in Burkitt lymphoma. Nature 306:760–765, 1983Google Scholar
  52. 52.
    Rabbitts TH, Forster A, Hamlyn P, Baer R: Effect of somatic mutation within translocated c-myc genes in Burkitt's lymphoma. Nature 309:592–597, 1983Google Scholar
  53. 53.
    Saito H, Hayday AC, Wiman K, Hayward WS, Tonegawa S: Activation of the c-myc gene by translocation: A model for translational control. Proc Natl Acad Sci USA 80:7476–7480, 1983Google Scholar
  54. 54.
    Nishikura K, ar-Rushdi A, Erikson J, Watt R, Rovera G, Croce CM: Differential expression of the normal and of the translocated human c-myc oncogenes in B cells. Proc Natl Acad Sci USA 80:4822–4826, 1983Google Scholar
  55. 55.
    ar-Rushdi A, Nishikura K, Erikson J, Watt R, Rovera G, Croce CM: Differential expression of the translocated and the untranslocated c-myc oncogene in Burkitt lymphoma. Science 222:390–393, 1983Google Scholar
  56. 56.
    Gelman EP, Psallidopoulos MC, Papas TS, Dalla-Favera R: Identification of reciprocal translocation sites within the c-myc oncogene and immunoglobulin mu locus in a Burkitt lymphoma. Nature 306:799–803, 1983Google Scholar
  57. 57.
    Siebenlist U, Hennighausen L, Battey J, Leder P: Chromatin structure and protein binding in the putative regulatory region of the c-myc gene in Burkitt lymphoma. Cell 37:381–391, 1984Google Scholar
  58. 58.
    Della-Favera R, Martinotti S, Gallo RC, Erikson J, Croce CM: Translocation and rearrangements of the c-myc oncogene locus in human undifferentiated B-cell lymphomas. Science 219:963–967, 1983Google Scholar
  59. 59.
    Erikson J, Finan J, Nowell P, Croce CM: Translocation of immunoglobulin VH genes in Burkitt lymphoma. Proc Natl Acad Sci USA 79:5611–5615, 1982Google Scholar
  60. 60.
    Hayday A, Gillies S, Saito H, Wood C, Wiman K, Hayward W, Tonegawa S: Activation of a translocated human c-myc gene by an enhancer in the immunoglobulin heavy chain locus. Nature 307:334–340, 1984Google Scholar
  61. 61.
    Cereghini S, Herbomel P, Jouanneau J, Saragosti S, Katinka M, Bourachot B, de Crombrugghe B, Yaniv M: Structure and function of the promoter-enhancer region of polyoma and SV40. Cold Spring Harbor Symp Quant Biol 47:935–944, 1983Google Scholar
  62. 62.
    Emerson BM, Felsenfeld G: Specific factor conferring nuclease hypersensitivity at the 5' end of the chicken adult beta-globin gene. Proc Natl Acad Sci USA 81:95–99, 1984Google Scholar
  63. 63.
    Parslow T, Granner D: Structure of a nuclease-sensitive region inside the immunoglobulin kappa gene: Evidence for a role in gene regulation. Nucl Acids Res 11:4775–4792, 1983Google Scholar
  64. 64.
    Mills F, Fisher M, Kuroda R, Ford A, Gould H: DNAase I hypersensitive sites in the chromatin of human mu immunoglobulin heavy-chain genes. Nature 306:809–812, 1983Google Scholar
  65. 65.
    Shermoen AW, Beckendorf SK: A complex of interacting DNAase I-hypersensitive sites near the Drosophila glue protein gene,Sgs4. Cell 29:601–607, 1982Google Scholar
  66. 66.
    Emanuel BS, Selden JR, Chaganti RS, Jhanwar S, Nowell PC, Croce CM: The 2p breakpoint of a 2;8 translocation in Burkitt lymphoma interrupts the V kappa locus. Proc Natl Acad Sci USA 81:2444–2446, 1984Google Scholar
  67. 67.
    Smith KA: T-cell growth factor.In T Cell Stimulating Growth Factors, Immunological Reviews 51, G Moller (ed). Copenhagen, Munksgaard, 1980, pp 337–357Google Scholar
  68. 68.
    Kehrl JH, Muraguchi A, Butler JL, Falkoff JM, Fauci AS: Human B cell activation, proliferation and differentiation.In B Cell Growth and Differentiation Factors, Immunological Reviews 78, G Moller (ed). Copenhagen, Munksgaard, 1984, pp 75–96Google Scholar
  69. 69.
    Pledger WJ, Stiles CD, Antoniades HN, Scher CD: An ordered sequence of events is required before BALB/c-3T3 cells become committed to DNA synthesis. Proc Natl Acad Sci USA 75:2839–2843, 1978Google Scholar
  70. 70.
    Kelly K, Cochran B, Stiles CD, Leder P: Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell 35:603–610, 1983Google Scholar
  71. 71.
    Campisi J, Gray HE, Pardee AB, Dean M, Sonnenshein GE: Cell-cycle control of c-myc but not c-ras expression is lost following chemical transformation. Cell 36:241–247, 1984Google Scholar
  72. 72.
    Greenberg ME, Ziff EB: Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature 311:433–438Google Scholar
  73. 73.
    Muller R, Bravo R, Burckhardt J, Curran T: Immediate dramatic induction of c-fos by growth factors precedes activation of c-myc. Nature (in press)Google Scholar
  74. 74.
    Makino R, Hayashi K, Sugimura T: c-myc transcript is induced in rat liver at a very early stage of regeneration or by cycloheximide treatment. Nature 310:697–698, 1984Google Scholar
  75. 75.
    Pfeifer-Ohlsson S, Goustin AS, Rydnert J, Wahlstrom T, Bjersing L, Stehelin D, Ohlsson R: Spatial and temporal pattern of cellular myc oncogene expression in developing human placenta: Implications for embryonic cell proliferation. Cell 38:585–596, 1984Google Scholar
  76. 76.
    Armelin HA, Armelin MCS, Kelly K, Stewart T, Leder P, Cochran BH, Stiles CD: A functional role for c-myc in the mitogenic response to platelet-derived growth factor. Nature 310:655–660, 1984Google Scholar
  77. 77.
    Goyette M, Petropoulous CJ, Shank PR, Fausto N: Expression of a cellular oncogene during liver regeneration. Science 219:510–512, 1983Google Scholar
  78. 78.
    Reitsma PH, Rothberg PG, Astrin SM, Trial J, Bar-Shavit Z, Hall A, Teitelbaum SL, Kahn AJ: Regulation of myc gene expression in HL-60 leukaemia cells by a vitamin D metabolite. Nature 306:492–494, 1983Google Scholar
  79. 79.
    Grosso LE, Pitot HC: Modulation of c-myc expression in the HL-60 cell line. Biochem Biophys Res Commun 119:473–480, 1984Google Scholar
  80. 80.
    Westaway D, Payne G, Varmus HE: Proviral deletions and oncogene base-substitutions in insertionally mutagenized c-myc alleles may contribute to the progression of avian bursal tumors. Proc Natl Acad Sci USA 81:843–847, 1984Google Scholar
  81. 81.
    Croce CM, Erikson J, ar-Rushdi A, Aden D, Nishikura K: Translocated c-myc oncogene of Burkitt lymphoma is transcribed in plasma cells and repressed in lymphoblastoid cells. Proc Natl Acad Sci USA 81:3170–3174, 1984Google Scholar
  82. 82.
    Tonegawa S: Somatic generation of antibody diversity. Nature 302:575–581, 1983Google Scholar
  83. 83.
    Mullins JI, Brody DS, Binari RC Jr, Cotter SM: Viral transduction of c-myc gene in naturally occurring feline leukaemias. Nature 308:856–858, 1984Google Scholar
  84. 84.
    Levy LS, Gardner MB, Casey JW: Isolation of feline leukaemia provirus containing the oncogene myc from a feline lymphosarcoma. Nature 308:853–856, 1984Google Scholar
  85. 85.
    Yanagi Y, Yoshikai Y, Leggett K, Clark SP, Aleksander J, Mak TW: A human T cell specific cDNA clone encodes a protein having extensive homology to immunoglobulin chains. Nature 308:145–149, 1984Google Scholar
  86. 86.
    Dalla-Favera R, Wong-Staal F, Gallo RC: Onc gene amplification in promyelocytic leukemia cell line HL-60 and primary leukaemic cells of the same patient. Nature 299:61–63, 1982.Google Scholar
  87. 87.
    Alitalo K, Schwab M, Lin CC, Varmus HE, Bishop JM: Homogeneously staining chromosomal regions contain amplified copies of an abundantly expressed cellular oncogene (c-myc) in malignant neuroendocrine cells from a human colon carcinoma. Proc Natl Acad Sci USA 80:1707–1711, 1983Google Scholar
  88. 88.
    Little CD, Nau MM, Carney DN, Gazdar AF, Minna JD: Amplification and expression of the c-myc oncogene in human lung cancer cell lines. Nature 306:194–196, 1983Google Scholar
  89. 89.
    Stewart TA, Pattengale PK, Leder P: Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38:627–637, 1984Google Scholar
  90. 90.
    Ralston R, Bishop JM: The protein products of the myc and myb oncogenes and adenovirus E1A are structurally related. Nature 306:803–806, 1983Google Scholar
  91. 91.
    Nevins JR: Mechanism of activation of early viral transcription by the adenovirus E1A gene product. Cell 26:213–220, 1981Google Scholar
  92. 92.
    Murray MJ, Cunningham JM, Parada LF, Dautry F, Lebowitz P, Weinberg RA: The HL-60 transforming sequence: A ras oncogene coexisting with altered myc genes in hematopoietic tumors. Cell 33:749–757, 1983Google Scholar
  93. 93.
    Land H, Parada LF, Weinberg RA: Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304:596–602, 1983Google Scholar

Copyright information

© Plenum Publishing Corporation 1985

Authors and Affiliations

  • Kathleen Kelly
    • 1
  • Ulrich Siebenlist
    • 2
  1. 1.Immunology BranchNCIBethesda
  2. 2.Laboratory of ImmunoregulationNational Institute of Allergy and Infectious DiseasesBethesda

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