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. 1988 Feb;62(2):580–585. doi: 10.1128/jvi.62.2.580-585.1988

Tumorigenicity of adenovirus-transformed cells: collagen interaction and cell surface laminin are controlled by the serotype origin of the E1A and E1B genes.

F J Bober 1, D E Birk 1, T Shenk 1, K Raska Jr 1
PMCID: PMC250571  PMID: 3275789

Abstract

A library of cells transformed with recombinant adenoviruses was used to study tumorigenicity and interaction with extracellular matrix. Cells expressing the complete E1 region of highly oncogenic adenovirus type 12 (Ad12) are tumorigenic, adhere preferentially to type IV collagen, and express cell surface laminin. Weakly tumorigenic cells, which express the E1A oncogene of Ad12 and the E1B genes of Ad5, also attach preferentially to type IV collagen but do not contain laminin on their surface. Cells which express the E1A oncogene of Ad5 and the E1B genes of Ad12 are nontumorigenic and do not preferentially attach to type IV versus type I collagen but have laminin on their surface. There is no significant difference in the amounts of laminin secreted into the culture medium among cells expressing the E1B genes of Ad5 or Ad12. In vitro assays show that cells which express the E1B genes of Ad12, irrespective of the origin of the E1A genes, can bind three times more exogenously added laminin than cells expressing the E1B genes of nononcogenic Ad5. The interaction of adenovirus-transformed cells with collagen is controlled by the serotype origin of the E1A oncogene, whereas cell surface laminin is controlled by the serotype origin of the E1B genes.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berk A. J., Sharp P. A. Structure of the adenovirus 2 early mRNAs. Cell. 1978 Jul;14(3):695–711. doi: 10.1016/0092-8674(78)90252-0. [DOI] [PubMed] [Google Scholar]
  2. Bernards R., Schrier P. I., Houweling A., Bos J. L., van der Eb A. J., Zijlstra M., Melief C. J. Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. 1983 Oct 27-Nov 2Nature. 305(5937):776–779. doi: 10.1038/305776a0. [DOI] [PubMed] [Google Scholar]
  3. Bober F. J., Birk D. E., Raska K., Jr Expression of varying portions of the adenovirus 12 early region 1 in transformed cells affects tumorigenicity and interaction with extracellular matrix components. Lab Invest. 1987 Jan;56(1):37–43. [PubMed] [Google Scholar]
  4. Gallimore P. H., Byrd P. J., Whittaker J. L., Grand R. J. Properties of rat cells transformed by DNA plasmids containing adenovirus type 12 E1 DNA or specific fragments of the E1 region: comparison of transforming frequencies. Cancer Res. 1985 Jun;45(6):2670–2680. [PubMed] [Google Scholar]
  5. Gallimore P. H., McDougall J. K., Chen L. B. In vitro traits of adenovirus-transformed cell lines and their relevance to tumorigenicity in nude mice. Cell. 1977 Apr;10(4):669–678. doi: 10.1016/0092-8674(77)90100-3. [DOI] [PubMed] [Google Scholar]
  6. Gallimore P. H. Viral DNA in transformed cells. II. A study of the sequences of adenovirus 2 DNA IN NINE LINES OF TRANSFORMED RAT CELLS USING SPECIFIC FRAGMENTS OF THE VIRAL GENOME;. J Mol Biol. 1974 Oct 15;89(1):49–72. doi: 10.1016/0022-2836(74)90162-4. [DOI] [PubMed] [Google Scholar]
  7. Jochemsen H., Daniëls G. S., Hertoghs J. J., Schrier P. I., van den Elsen P. J., van der EB A. J. Identification of adenovirus-type 12 gene products involved in transformation and oncogenesis. Virology. 1982 Oct 15;122(1):15–28. doi: 10.1016/0042-6822(82)90373-7. [DOI] [PubMed] [Google Scholar]
  8. Levine E. L., Birk D. E., Raska K., Jr Attachment to and degradation of collagen substrata by adenovirus-transformed cells of varying tumorigenicity. Coll Relat Res. 1984 Jan;4(1):49–61. doi: 10.1016/s0174-173x(84)80028-x. [DOI] [PubMed] [Google Scholar]
  9. Lewis A. M., Jr, Cook J. L. A new role for DNA virus early proteins in viral carcinogenesis. Science. 1985 Jan 4;227(4682):15–20. doi: 10.1126/science.3843807. [DOI] [PubMed] [Google Scholar]
  10. Liotta L. A. Tumor invasion and metastases--role of the extracellular matrix: Rhoads Memorial Award lecture. Cancer Res. 1986 Jan;46(1):1–7. [PubMed] [Google Scholar]
  11. Malinoff H. L., McCoy J. P., Jr, Varani J., Wicha M. S. Metastatic potential of murine fibrosarcoma cells is influenced by cell surface laminin. Int J Cancer. 1984 May 15;33(5):651–655. doi: 10.1002/ijc.2910330516. [DOI] [PubMed] [Google Scholar]
  12. Mellow G. H., Föhring B., Dougherty J., Gallimore P. H., Raska K., Jr Tumorigenicity of adenovirus-transformed rat cells and expression of class I major histocompatibility antigen. Virology. 1984 Apr 30;134(2):460–465. doi: 10.1016/0042-6822(84)90313-1. [DOI] [PubMed] [Google Scholar]
  13. Murray J. C., Liotta L., Rennard S. I., Martin G. R. Adhesion characteristics of murine metastatic and nonmetastatic tumor cells in vitro. Cancer Res. 1980 Feb;40(2):347–351. [PubMed] [Google Scholar]
  14. Raska K., Jr, Gallimore P. H. An inverse relation of the oncogenic potential of adenovirus-transformed cells and their sensitivity to killing by syngeneic natural killer cells. Virology. 1982 Nov;123(1):8–18. doi: 10.1016/0042-6822(82)90290-2. [DOI] [PubMed] [Google Scholar]
  15. Sawada Y., Föhring B., Shenk T. E., Raska K., Jr Tumorigenicity of adenovirus-transformed cells: region E1A of adenovirus 12 confers resistance to natural killer cells. Virology. 1985 Dec;147(2):413–421. doi: 10.1016/0042-6822(85)90143-6. [DOI] [PubMed] [Google Scholar]
  16. Sawada Y., Urbanelli D., Raskova J., Shenk T. E., Raska K., Jr Adenovirus tumor-specific transplantation antigen is a function of the E1A early region. J Exp Med. 1986 Mar 1;163(3):563–572. doi: 10.1084/jem.163.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Terranova V. P., Liotta L. A., Russo R. G., Martin G. R. Role of laminin in the attachment and metastasis of murine tumor cells. Cancer Res. 1982 Jun;42(6):2265–2269. [PubMed] [Google Scholar]
  18. Terranova V. P., Rao C. N., Kalebic T., Margulies I. M., Liotta L. A. Laminin receptor on human breast carcinoma cells. Proc Natl Acad Sci U S A. 1983 Jan;80(2):444–448. doi: 10.1073/pnas.80.2.444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Varani J., Lovett E. J., 3rd, McCoy J. P., Jr, Shibata S., Maddox D. E., Goldstein I. J., Wicha M. Differential expression of a lamininlike substance by high- and low-metastatic tumor cells. Am J Pathol. 1983 Apr;111(1):27–34. [PMC free article] [PubMed] [Google Scholar]
  20. Yurchenco P. D., Furthmayr H. Self-assembly of basement membrane collagen. Biochemistry. 1984 Apr 10;23(8):1839–1850. doi: 10.1021/bi00303a040. [DOI] [PubMed] [Google Scholar]
  21. de Leij L., Smets L. A., Jochemsen H., van der Eb A. J. Tumor- and growth-related membrane changes caused by transformation with different fragments of the adenovirus 12 genome. Virology. 1982 Oct 15;122(1):210–214. doi: 10.1016/0042-6822(82)90392-0. [DOI] [PubMed] [Google Scholar]

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