Home LiteratureArticle Details
PMID: 1594587 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Loss of tumorigenicity of rat glioblastoma directed by episome-based antisense cDNA transcription of insulin-like growth factor I.

Trojan J, Blossey BK, Johnson TR, Rudin SD, Tykocinski M, Ilan J, Ilan J

Abstract

Malignant glioma is the most common brain tumor. The molecular basis of glioma tumorigenicity has not been defined. Cultured glioma cells accumulate high levels of insulin-like growth factor I (IGF-I) transcripts. We asked whether IGF-I expression is coupled to tumorigenicity, using a combined in vivo/in vitro system employing antisense RNA for IGF-I. An antisense IGF-I expression construct in an expression vector that incorporates Epstein-Barr virus replicative signals and the ZnSO4-inducible metallothionein I transcriptional promoter was assembled. Stable glioma transfectants were derived from C6 glioma cells, which constitutively express IGF-I. B-104 neuroblastoma cells, derived originally from the same tumor but not expressing IGF-I, were also transfected as controls. In the absence of ZnSO4, the C6 transfectants expressed high levels of IGF-I mRNA and protein as detected by in situ hybridization and immunocytochemistry, respectively. Addition of ZnSO4 in the culture medium resulted in high levels of antisense transcript accumulation and dramatically decreased levels of endogenous IGF-I mRNA and IGF-I protein. Subcutaneous injection of either nontransfected C6 parental cells or C6 cells transfected with vector without IGF-I sequences into rats resulted in large tumors after 2 weeks, as did transfected and nontransfected B-104 cells. However, the rats injected with transfected C6 cells yielded no tumors after 40 weeks of observation. Two weeks after injection of the transfected C6 cells a small cyst was apparent in six rats. Histologic sections revealed a few glioma cells infiltrated by a large number of mononuclear cells. No infiltration of mononuclear cells was apparent in the glioma tumors resulting from injection of parental (nontransfected) cells, suggesting that the parental cells, but not the antisense IGF-I transfectants, escape the host immune response.

MeSH Terms
Animals Cell Transformation, Neoplastic/genetics Glioma/genetics,pathology In Vitro Techniques Insulin-Like Growth Factor I/genetics,metabolism Plasmids RNA, Antisense Rats Transfection Tumor Cells, Cultured
Chemicals
RNA, Antisense Insulin-Like Growth Factor I
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Trojan J
Department of Anatomy, Case Western Reserve University, School of Medicine, Cleveland, OH 44106.
Blossey B K
Johnson T R
Rudin S D
Tykocinski M
Ilan J
Ilan J
References (44)
44 references, click to expand
  1. Growth factors as transforming proteins.
    Eur J Biochem. 1989 Oct 1;184(3):487-96 PMID: 2680482
  2. RNA complementary to herpes simplex virus type 1 ICP0 gene demonstrated in neurons of human trigeminal ganglia.
    J Virol. 1988 May;62(5):1832-5 PMID: 2451758
  3. National survey of patterns of care for brain-tumor patients.
    J Neurosurg. 1989 Dec;71(6):826-36 PMID: 2585073
  4. Grading of astrocytomas. A simple and reproducible method.
    Cancer. 1988 Nov 15;62(10):2152-65 PMID: 3179928
  5. Evidence for autocrine mitogenic stimulation by somatomedin-C/insulin-like growth factor I on an established human lung cancer cell line.
    Cancer Res. 1988 Jul 1;48(13):3716-9 PMID: 3378214
  6. Immunocytochemical quantitative study of alpha-fetoprotein in normal and neoplastic neural development.
    Dev Neurosci. 1983-1984;6(4-5):251-9 PMID: 6083861
  7. A 12-base-pair DNA motif that is repeated several times in metallothionein gene promoters confers metal regulation to a heterologous gene.
    Proc Natl Acad Sci U S A. 1984 Dec;81(23):7318-22 PMID: 6095286
  8. Secretion of an insulin-like growth factor-I-related protein by human breast cancer cells.
    Cancer Res. 1986 Sep;46(9):4613-9 PMID: 3731113
  9. Appearance of H and B antigens in primary sensory cells of the rat olfactory apparatus and inner ear.
    Brain Res. 1985 Jan;349(1-2):275-9 PMID: 3986592
  10. N-myc mRNA forms an RNA-RNA duplex with endogenous antisense transcripts.
    Mol Cell Biol. 1990 Aug;10(8):4180-91 PMID: 1695323
  11. BCL2-mediated tumorigenicity of a human T-lymphoid cell line: synergy with MYC and inhibition by BCL2 antisense.
    Proc Natl Acad Sci U S A. 1990 May;87(10):3660-4 PMID: 1692620
  12. Assumptions in the radiotherapy of glioblastoma.
    Neurology. 1980 Sep;30(9):907-11 PMID: 6252514
  13. Production of an insulin-like growth factor by osteosarcoma.
    Biochem Biophys Res Commun. 1984 Aug 30;123(1):373-6 PMID: 6383381
  14. Sequence of cDNA encoding human insulin-like growth factor I precursor.
    Nature. 1983 Dec 8-14;306(5943):609-11 PMID: 6358902
  15. Metallothionein-human GH fusion genes stimulate growth of mice.
    Science. 1983 Nov 18;222(4625):809-14 PMID: 6356363
  16. Effects of actinomycin D and cycloheximide on transcript levels of IGF-I, actin, and albumin in hepatocyte primary cultures treated with growth hormone and insulin.
    Mol Reprod Dev. 1991 Oct;30(2):95-9 PMID: 1720008
  17. Experimental therapy of human glioma by means of a genetically engineered virus mutant.
    Science. 1991 May 10;252(5007):854-6 PMID: 1851332
  18. A genetic tool used to identify thioredoxin as a mediator of a growth inhibitory signal.
    Science. 1991 Apr 5;252(5002):117-20 PMID: 1901424
  19. Episome-generated N-myc antisense RNA restricts the differentiation potential of primitive neuroectodermal cell lines.
    Mol Cell Biol. 1991 Mar;11(3):1360-71 PMID: 1996098
  20. Antisense RNA inhibition of HPRT synthesis.
    Somat Cell Mol Genet. 1990 Jul;16(4):369-82 PMID: 2218724
  21. Antisense RNA of the latent period gene (MER5) inhibits the differentiation of murine erythroleukemia cells.
    Gene. 1990 Jul 16;91(2):261-5 PMID: 2210385
  22. Antisense RNA inhibits splicing of pre-mRNA in vitro.
    EMBO J. 1988 Aug;7(8):2523-32 PMID: 2461296
  23. Insulin-like growth factor-I messenger ribonucleic acid in the developing human placenta and in term placenta of diabetics.
    Mol Endocrinol. 1988 Mar;2(3):217-29 PMID: 3398851
  24. Expression of insulin-like growth factor II in human placentas from normal and diabetic pregnancies.
    Proc Natl Acad Sci U S A. 1986 Dec;83(23):9179-82 PMID: 3466182
  25. Rat C6 glial cells synthesize insulin-like growth factor I (IGF-I) and express IGF-I receptors and IGF-II/mannose 6-phosphate receptors.
    Endocrinology. 1989 Apr;124(4):1727-36 PMID: 2538309
  26. Antisense RNA-induced reduction in murine TIMP levels confers oncogenicity on Swiss 3T3 cells.
    Science. 1989 Feb 17;243(4893):947-50 PMID: 2465572
  27. Constitutive and conditional suppression of exogenous and endogenous genes by anti-sense RNA.
    Science. 1985 Jul 26;229(4711):345-52 PMID: 2990048
  28. Nuclear-organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants.
    Cell. 1988 Nov 18;55(4):673-81 PMID: 3052855
  29. Epstein-Barr virus episome-based promoter function in human myeloid cells.
    Nucleic Acids Res. 1989 Mar 11;17(5):1989-2003 PMID: 2538801
  30. Stable reduction of thymidine kinase activity in cells expressing high levels of anti-sense RNA.
    Cell. 1985 Aug;42(1):129-38 PMID: 2410135
  31. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells.
    Nature. 1985 Feb 28-Mar 6;313(6005):812-5 PMID: 2983224
  32. Intragenic pausing and anti-sense transcription within the murine c-myc locus.
    EMBO J. 1986 Nov;5(11):2859-65 PMID: 3024965
  33. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  34. The effect of antisense RNA to fibronectin on the malignancy of hybrids between melanoma cells and normal fibroblasts.
    J Cell Sci. 1989 Jul;93 ( Pt 3):515-24 PMID: 2481681
  35. Nuclear and cytoplasmic sites for anti-sense control.
    Nucleic Acids Res. 1989 Sep 25;17(18):7203-9 PMID: 2477795
  36. An antisense RNA involved in p53 mRNA maturation in murine erythroleukemia cells induced to differentiate.
    EMBO J. 1989 Dec 20;8(13):4107-14 PMID: 2480234
  37. Directional antisense and sense cDNA cloning using Epstein-Barr virus episomal expression vectors.
    Gene. 1989 Sep 30;81(2):285-94 PMID: 2478421
  38. An antisense mRNA directs the covalent modification of the transcript encoding fibroblast growth factor in Xenopus oocytes.
    Cell. 1989 Nov 17;59(4):687-96 PMID: 2479482
  39. Alpha-fetoprotein (AFP) in granulomatous inflammation of the mouse.
    Br J Exp Pathol. 1989 Aug;70(4):469-78 PMID: 2475155
  40. Conversion of normal behavior to shiverer by myelin basic protein antisense cDNA in transgenic mice.
    Science. 1988 Jul 29;241(4865):593-5 PMID: 2456614
  41. The interleukin 2 gene is expressed in the syncytiotrophoblast of the human placenta.
    Proc Natl Acad Sci U S A. 1989 Jan;86(2):656-60 PMID: 2463636
  42. Isolation of an insulin-like growth factor II cDNA with a unique 5' untranslated region from human placenta.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1947-51 PMID: 2450353
  43. Use of an Epstein-Barr virus episomal replicon for anti-sense RNA-mediated gene inhibition in a human cytotoxic T-cell clone.
    Proc Natl Acad Sci U S A. 1988 Jun;85(11):4010-4 PMID: 2453884
  44. Expression of insulin-like growth factor I in cultured rat hepatocytes: effects of insulin and growth hormone.
    Mol Endocrinol. 1989 Mar;3(3):580-7 PMID: 2664476
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1992-06-01
Pages
4874-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC49190
Subset
IM
Grants
NCI NIH HHS · CA-43703 · United States
NICHD NIH HHS · HD-18271 · United States
NICHD NIH HHS · HD-25004 · United States
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