Home LiteratureArticle Details
PMID: 3049071 Published · ppublish English Journal Article

Ras-mediated cell cycle arrest is altered by nuclear oncogenes to induce Schwann cell transformation.

The EMBO journal ·Vol. 7 ·No. 6 ·1988-06-00 ·Pages 1635-45

Ridley AJ, Paterson HF, Noble M, Land H

Abstract

The cellular responses to ras and nuclear oncogenes were investigated in purified populations of rat Schwann cells. v-Ha-ras and SV40 large T cooperate to transform Schwann cells, inducing growth in soft agar and allowing proliferation in the absence of added mitogens. Expression of large T alone reduces their growth factor requirements but is insufficient to induce full transformation. In contrast, expression of v-Ha-ras leads to proliferation arrest in Schwann cells expressing a temperature-sensitive mutant of large T at the restrictive temperature. Cells arrest in either the G1 or G2/M phases of the cell cycle, and can re-enter cell division at the permissive temperature even after prolonged periods at the restrictive conditions. Oncogenic ras proteins also inhibit DNA synthesis when microinjected into Schwann cells. Adenovirus E1a and c-myc oncogenes behave similarly to SV40 large T. They cooperate with Ha-ras oncogenes to transform Schwann cells, and prevent ras-induced growth arrest. Thus nuclear oncogenes fundamentally alter the response of Schwann cells to a ras oncogene from cell cycle arrest to transformation.

MeSH Terms
Animals Antigens, Polyomavirus Transforming/physiology Cell Cycle Cell Division Cell Nucleus Cell Transformation, Neoplastic/pathology Cell Transformation, Viral Cells, Cultured Growth Substances/pharmacology Oncogene Protein p21(ras) Oncogene Proteins, Viral/physiology Oncogenes Proto-Oncogene Proteins/physiology Proto-Oncogene Proteins c-myc Rats Rats, Inbred Strains Schwann Cells/pathology
Chemicals
Antigens, Polyomavirus Transforming Growth Substances Oncogene Proteins, Viral Proto-Oncogene Proteins Proto-Oncogene Proteins c-myc Oncogene Protein p21(ras)
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ridley A J
Imperial Cancer Research Fund, London, UK.
Paterson H F
Noble M
Land H
References (79)
79 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. A new technique for the assay of infectivity of human adenovirus 5 DNA.
    Virology. 1973 Apr;52(2):456-67 PMID: 4705382
  3. Role of simian virus 40 gene A function in maintenance of transformation.
    J Virol. 1975 Mar;15(3):619-35 PMID: 163376
  4. Deletion loop mutagenesis: a novel method for the construction of point mutations using deletion mutants.
    Nucleic Acids Res. 1982 Sep 11;10(17):5161-71 PMID: 6292832
  5. Are all the neuronal nuclei polyploid?
    Histochemistry. 1975;43(1):59-61 PMID: 1141026
  6. Transformation of BALB/c-3T3 cells by tsA mutants of simian virus 40: temperature sensitivity of the transformed phenotype and retransofrmation by wild-type virus.
    J Virol. 1978 Mar;25(3):860-70 PMID: 205675
  7. Transformation parameters in chicken fibroblasts transformed by AEV and MC29 avian leukemia viruses.
    Cell. 1978 Apr;13(4):751-60 PMID: 207439
  8. Animal cell cycle.
    Annu Rev Biochem. 1978;47:715-50 PMID: 354504
  9. Schwann cell growth factors.
    Cell. 1978 Nov;15(3):813-22 PMID: 215315
  10. Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve.
    Brain Res. 1979 Apr 6;165(1):105-18 PMID: 371755
  11. Cell-type-specific markers for distinguishing and studying neurons and the major classes of glial cells in culture.
    Brain Res. 1979 Oct 5;174(2):283-308 PMID: 385109
  12. Production and characterization of cytotoxic Thy-1 antibody-secreting hybrid cell lines. Detection of T cell subsets.
    Eur J Immunol. 1979 Nov;9(11):875-86 PMID: 393521
  13. Autocrine secretion and malignant transformation of cells.
    N Engl J Med. 1980 Oct 9;303(15):878-80 PMID: 7412807
  14. Kirsten murine sarcoma virus transformed cell lines and a spontaneously transformed rat cell-line produce transforming factors.
    J Cell Physiol. 1980 Oct;105(1):163-80 PMID: 6253509
  15. Studies on cultured rat Schwann cells. III. Assays for peripheral myelin proteins.
    J Neurocytol. 1980 Feb;9(1):67-77 PMID: 7009795
  16. Cytophotometric evidence of non-S-phase extra-DNA in human neuronal nuclei.
    Cell Tissue Kinet. 1981 Jul;14(4):433-44 PMID: 7261027
  17. Isolation of a transforming sequence from a human bladder carcinoma cell line.
    Cell. 1982 May;29(1):161-9 PMID: 6286138
  18. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter.
    J Mol Appl Genet. 1982;1(4):327-41 PMID: 6286831
  19. Monoclonal antibodies to the p21 products of the transforming gene of Harvey murine sarcoma virus and of the cellular ras gene family.
    J Virol. 1982 Jul;43(1):294-304 PMID: 6287003
  20. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium.
    Nature. 1983 Jun 2-8;303(5916):390-6 PMID: 6304520
  21. In vivo and in vitro observations on laminin production by Schwann cells.
    Proc Natl Acad Sci U S A. 1983 Jun;80(12):3850-4 PMID: 6344090
  22. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes.
    Nature. 1983 Aug 18-24;304(5927):596-602 PMID: 6308472
  23. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture.
    Nature. 1983 Aug 18-24;304(5927):602-6 PMID: 6308473
  24. Biosynthesis of type IV collagen by cultured rat Schwann cells.
    J Cell Biol. 1983 Aug;97(2):473-9 PMID: 6885907
  25. Microinjection of tissue culture cells.
    Methods Enzymol. 1983;101:482-92 PMID: 6310338
  26. The G1 distribution of "G1-less" V79 Chinese hamster cells.
    Exp Cell Res. 1983 Oct;148(1):127-42 PMID: 6628553
  27. Cellular oncogenes and multistep carcinogenesis.
    Science. 1983 Nov 18;222(4625):771-8 PMID: 6356358
  28. Identification and purification of glial growth factor.
    J Neurosci. 1984 Jan;4(1):75-83 PMID: 6693948
  29. G proteins and dual control of adenylate cyclase.
    Cell. 1984 Mar;36(3):577-9 PMID: 6321035
  30. Construction and applications of a highly transmissible murine retrovirus shuttle vector.
    Cell. 1984 Jul;37(3):1053-62 PMID: 6331674
  31. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus.
    Cell. 1983 May;33(1):153-9 PMID: 6678608
  32. Microinjection of the oncogene form of the human H-ras (T-24) protein results in rapid proliferation of quiescent cells.
    Cell. 1984 Aug;38(1):109-17 PMID: 6380758
  33. Functional role for c-myc in mitogenic response to platelet-derived growth factor.
    Nature. 1984 Aug 23-29;310(5979):655-60 PMID: 6088986
  34. The product of ras is a GTPase and the T24 oncogenic mutant is deficient in this activity.
    Nature. 1984 Sep 20-26;311(5983):273-5 PMID: 6148703
  35. Intrinsic GTPase activity distinguishes normal and oncogenic ras p21 molecules.
    Proc Natl Acad Sci U S A. 1984 Sep;81(18):5704-8 PMID: 6148751
  36. Biological activities of v-myc and rearranged c-myc oncogenes in rat fibroblast cells in culture.
    Proc Natl Acad Sci U S A. 1984 Sep;81(18):5758-62 PMID: 6091107
  37. High-efficiency gene transfer into mammalian cells: generation of helper-free recombinant retrovirus with broad mammalian host range.
    Proc Natl Acad Sci U S A. 1984 Oct;81(20):6349-53 PMID: 6093098
  38. Inositol trisphosphate, a novel second messenger in cellular signal transduction.
    Nature. 1984 Nov 22-28;312(5992):315-21 PMID: 6095092
  39. Harvey murine sarcoma virus p21 ras protein: biological and biochemical significance of the cysteine nearest the carboxy terminus.
    EMBO J. 1984 Nov;3(11):2581-5 PMID: 6096132
  40. Requirement for ras proto-oncogene function during serum-stimulated growth of NIH 3T3 cells.
    Nature. 1985 Jan 17-23;313(5999):241-3 PMID: 3918269
  41. Distinctive effects of the viral oncogenes myc, erb, fps, and src on the differentiation program of quail myogenic cells.
    Proc Natl Acad Sci U S A. 1985 Jan;82(2):426-30 PMID: 2982156
  42. Nerve growth factor-treated, neurite-bearing PC12 cells continue to synthesize DNA.
    J Neurosci. 1985 Feb;5(2):343-51 PMID: 3973669
  43. Myeloid cell transformation by ras-containing murine sarcoma viruses.
    Mol Cell Biol. 1985 Apr;5(4):667-74 PMID: 2985965
  44. Nonmyelin-forming Schwann cells coexpress surface proteins and intermediate filaments not found in myelin-forming cells: a study of Ran-2, A5E3 antigen and glial fibrillary acidic protein.
    J Neurocytol. 1984 Dec;13(6):923-34 PMID: 6398831
  45. Viral oncogenes.
    Cell. 1985 Aug;42(1):23-38 PMID: 2990725
  46. Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells.
    Proc Natl Acad Sci U S A. 1985 Aug;82(16):5365-9 PMID: 3860868
  47. A neuronal cell surface heparan sulfate proteoglycan is required for dorsal root ganglion neuron stimulation of Schwann cell proliferation.
    J Cell Biol. 1985 Sep;101(3):744-54 PMID: 3161898
  48. Glial cells express N-CAM/D2-CAM-like polypeptides in vitro.
    Nature. 1985 Aug 22-28;316(6030):725-8 PMID: 2412126
  49. Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation.
    Cell. 1985 Oct;42(3):841-8 PMID: 2996779
  50. Individual adenovirus type 5 early region 1A gene products elicit distinct alterations of cellular morphology and gene expression.
    J Virol. 1985 Nov;56(2):404-13 PMID: 4057356
  51. The action of oncogenes in the cytoplasm and nucleus.
    Science. 1985 Nov 15;230(4727):770-6 PMID: 2997917
  52. An immunoaffinity purification procedure for SV40 large T antigen.
    Virology. 1985 Jul 15;144(1):88-100 PMID: 2998049
  53. Phorbol ester enhances deoxynucleoside incorporation while inhibiting proliferation of K-562 cells.
    Cytometry. 1985 Nov;6(6):591-6 PMID: 2415311
  54. Specific growth response of ras-transformed embryo fibroblasts to tumour promoters.
    Nature. 1985 Dec 5-11;318(6045):472-5 PMID: 4069218
  55. Three restriction points in the cell cycle of activated murine B lymphocytes.
    Proc Natl Acad Sci U S A. 1985 Nov;82(22):7681-5 PMID: 3877931
  56. ras-transformed cells: altered levels of phosphatidylinositol-4,5-bisphosphate and catabolites.
    Science. 1986 Jan 24;231(4736):407-10 PMID: 3001936
  57. Growth factors and cancer.
    Cancer Res. 1986 Mar;46(3):1015-29 PMID: 3002607
  58. In vitro establishment is not a sufficient prerequisite for transformation by activated ras oncogenes.
    Cell. 1986 Feb 14;44(3):409-18 PMID: 3510745
  59. v-erbA cooperates with sarcoma oncogenes in leukemic cell transformation.
    Cell. 1986 May 9;45(3):349-56 PMID: 3009024
  60. Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment.
    Nature. 1986 Apr 24-30;320(6064):760-3 PMID: 3458027
  61. v-ras genes from Harvey and BALB murine sarcoma viruses can act as initiators of two-stage mouse skin carcinogenesis.
    Cell. 1986 Aug 1;46(3):447-56 PMID: 3015415
  62. Infection of immune mast cells by Harvey sarcoma virus: immortalization without loss of requirement for interleukin-3.
    Mol Cell Biol. 1985 Sep;5(9):2257-64 PMID: 3016524
  63. Normal p21N-ras couples bombesin and other growth factor receptors to inositol phosphate production.
    Nature. 1986 Sep 11-17;323(6084):173-6 PMID: 3018591
  64. Early signals in the mitogenic response.
    Science. 1986 Oct 10;234(4773):161-6 PMID: 3018928
  65. Schwann cells stimulated to proliferate in the absence of neurons retain full functional capability.
    J Neurosci. 1986 Oct;6(10):3070-8 PMID: 3760949
  66. Differential responsiveness of myc- and ras-transfected cells to growth factors: selective stimulation of myc-transfected cells by epidermal growth factor.
    Mol Cell Biol. 1986 Mar;6(3):870-7 PMID: 3022135
  67. Regulation of tumor antigen synthesis by simain virus 40 gene A.
    J Virol. 1975 Jul;16(1):168-78 PMID: 166203
  68. Microinjection of the ras oncogene protein into nonestablished rat embryo fibroblasts.
    Cancer Res. 1986 Dec;46(12 Pt 1):6427-32 PMID: 3536079
  69. Recombinant retroviruses encoding simian virus 40 large T antigen and polyomavirus large and middle T antigens.
    Mol Cell Biol. 1986 Apr;6(4):1204-17 PMID: 3023876
  70. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts.
    Mol Cell Biol. 1986 Jun;6(6):1917-25 PMID: 3785184
  71. The molecular genetics of cancer.
    Science. 1987 Jan 16;235(4786):305-11 PMID: 3541204
  72. Biochemical and biological properties of the human N-ras p21 protein.
    Mol Cell Biol. 1987 Jan;7(1):541-4 PMID: 3550423
  73. Expression of human class II major histocompatibility complex antigens using retrovirus vectors.
    Proc Natl Acad Sci U S A. 1987 Apr;84(8):2150-4 PMID: 3031667
  74. ras genes.
    Annu Rev Biochem. 1987;56:779-827 PMID: 3304147
  75. Mutational analysis of the adenovirus E1a gene: the role of transcriptional regulation in transformation.
    EMBO J. 1987 Jul;6(7):2053-60 PMID: 2820718
  76. Oncogenes and transcriptional control.
    Science. 1987 Dec 4;238(4832):1337-9 PMID: 2825348
  77. Immortalization by c-myc, H-ras, and Ela oncogenes induces differential cellular gene expression and growth factor responses.
    Mol Cell Biol. 1987 Nov;7(11):3899-907 PMID: 2963209
  78. Involvement of functional protein kinase C in the mitogenic response to the H-ras oncogene product.
    Mol Cell Biol. 1987 Nov;7(11):4146-9 PMID: 3323889
  79. Tetraploid DNA content of Purkinje neurons of human cerebellar cortex.
    Science. 1968 Jan 19;159(3812):310-2 PMID: 5634498
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1988-06-00
Pages
1635-45
Language
English
Region
England
NLM ID
8208664
PMCID
PMC457147
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com