Skip to main content

This is a preview of improvements coming to the PMC website in October 2024. Learn more

Return to current site
PMC home page
Logo of The Journal of Cell Biology Link to view articles on publisher site
. 1991 Apr 1;113(1):173–185. doi: 10.1083/jcb.113.1.173

E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells

PMCID: PMC2288921  PMID: 2007622

Abstract

The ability of carcinomas to invade and to metastasize largely depends on the degree of epithelial differentiation within the tumors, i.e., poorly differentiated being more invasive than well-differentiated carcinomas. Here we confirmed this correlation by examining various human cell lines derived from bladder, breast, lung, and pancreas carcinomas. We found that carcinoma cell lines with an epithelioid phenotype were noninvasive and expressed the epithelium-specific cell- cell adhesion molecule E-cadherin (also known as Arc-1, uvomorulin, and cell-CAM 120/80), as visualized by immunofluorescence microscopy and by Western and Northern blotting, whereas carcinoma cell lines with a fibroblastoid phenotype were invasive and had lost E-cadherin expression. Invasiveness of these latter cells could be prevented by transfection with E-cadherin cDNA and was again induced by treatment of the transfected cells with anti-E-cadherin mAbs. These findings indicate that the selective loss of E-cadherin expression can generate dedifferentiation and invasiveness of human carcinoma cells, and they suggest further that E-cadherin acts as an invasion suppressor.

Full Text

The Full Text of this article is available as a PDF (3.9 MB).

Selected References

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

  1. Ahlering T. E., Dubeau L., Jones P. A. A new in vivo model to study invasion and metastasis of human bladder carcinoma. Cancer Res. 1987 Dec 15;47(24 Pt 1):6660–6665. [PubMed] [Google Scholar]
  2. Almoguera C., Shibata D., Forrester K., Martin J., Arnheim N., Perucho M. Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes. Cell. 1988 May 20;53(4):549–554. doi: 10.1016/0092-8674(88)90571-5. [DOI] [PubMed] [Google Scholar]
  3. Behrens J., Birchmeier W., Goodman S. L., Imhof B. A. Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin. J Cell Biol. 1985 Oct;101(4):1307–1315. doi: 10.1083/jcb.101.4.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Behrens J., Mareel M. M., Van Roy F. M., Birchmeier W. Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J Cell Biol. 1989 Jun;108(6):2435–2447. doi: 10.1083/jcb.108.6.2435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benchimol S., Fuks A., Jothy S., Beauchemin N., Shirota K., Stanners C. P. Carcinoembryonic antigen, a human tumor marker, functions as an intercellular adhesion molecule. Cell. 1989 Apr 21;57(2):327–334. doi: 10.1016/0092-8674(89)90970-7. [DOI] [PubMed] [Google Scholar]
  6. Blobel G. A., Moll R., Franke W. W., Vogt-Moykopf I. Cytokeratins in normal lung and lung carcinomas. I. Adenocarcinomas, squamous cell carcinomas and cultured cell lines. Virchows Arch B Cell Pathol Incl Mol Pathol. 1984;45(4):407–429. doi: 10.1007/BF02889883. [DOI] [PubMed] [Google Scholar]
  7. Bodmer W. F., Bailey C. J., Bodmer J., Bussey H. J., Ellis A., Gorman P., Lucibello F. C., Murday V. A., Rider S. H., Scambler P. Localization of the gene for familial adenomatous polyposis on chromosome 5. Nature. 1987 Aug 13;328(6131):614–616. doi: 10.1038/328614a0. [DOI] [PubMed] [Google Scholar]
  8. Boller K., Vestweber D., Kemler R. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J Cell Biol. 1985 Jan;100(1):327–332. doi: 10.1083/jcb.100.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bookstein R., Shew J. Y., Chen P. L., Scully P., Lee W. H. Suppression of tumorigenicity of human prostate carcinoma cells by replacing a mutated RB gene. Science. 1990 Feb 9;247(4943):712–715. doi: 10.1126/science.2300823. [DOI] [PubMed] [Google Scholar]
  10. Bos J. L., Fearon E. R., Hamilton S. R., Verlaan-de Vries M., van Boom J. H., van der Eb A. J., Vogelstein B. Prevalence of ras gene mutations in human colorectal cancers. 1987 May 28-Jun 3Nature. 327(6120):293–297. doi: 10.1038/327293a0. [DOI] [PubMed] [Google Scholar]
  11. Boyd D., Florent G., Kim P., Brattain M. Determination of the levels of urokinase and its receptor in human colon carcinoma cell lines. Cancer Res. 1988 Jun 1;48(11):3112–3116. [PubMed] [Google Scholar]
  12. Cailleau R., Olivé M., Cruciger Q. V. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro. 1978 Nov;14(11):911–915. doi: 10.1007/BF02616120. [DOI] [PubMed] [Google Scholar]
  13. Cailleau R., Young R., Olivé M., Reeves W. J., Jr Breast tumor cell lines from pleural effusions. J Natl Cancer Inst. 1974 Sep;53(3):661–674. doi: 10.1093/jnci/53.3.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cooper D., Schermer A., Sun T. T. Classification of human epithelia and their neoplasms using monoclonal antibodies to keratins: strategies, applications, and limitations. Lab Invest. 1985 Mar;52(3):243–256. [PubMed] [Google Scholar]
  15. Cunningham B. A., Leutzinger Y., Gallin W. J., Sorkin B. C., Edelman G. M. Linear organization of the liver cell adhesion molecule L-CAM. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5787–5791. doi: 10.1073/pnas.81.18.5787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  17. Daneker G. W., Jr, Piazza A. J., Steele G. D., Jr, Mercurio A. M. Relationship between extracellular matrix interactions and degree of differentiation in human colon carcinoma cell lines. Cancer Res. 1989 Feb 1;49(3):681–686. [PubMed] [Google Scholar]
  18. Edelman G. M., Gallin W. J., Delouvée A., Cunningham B. A., Thiery J. P. Early epochal maps of two different cell adhesion molecules. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4384–4388. doi: 10.1073/pnas.80.14.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Eidelman S., Damsky C. H., Wheelock M. J., Damjanov I. Expression of the cell-cell adhesion glycoprotein cell-CAM 120/80 in normal human tissues and tumors. Am J Pathol. 1989 Jul;135(1):101–110. [PMC free article] [PubMed] [Google Scholar]
  20. Engel L. W., Young N. A. Human breast carcinoma cells in continuous culture: a review. Cancer Res. 1978 Nov;38(11 Pt 2):4327–4339. [PubMed] [Google Scholar]
  21. Fearon E. R., Cho K. R., Nigro J. M., Kern S. E., Simons J. W., Ruppert J. M., Hamilton S. R., Preisinger A. C., Thomas G., Kinzler K. W. Identification of a chromosome 18q gene that is altered in colorectal cancers. Science. 1990 Jan 5;247(4938):49–56. doi: 10.1126/science.2294591. [DOI] [PubMed] [Google Scholar]
  22. Feinberg A. P., Gehrke C. W., Kuo K. C., Ehrlich M. Reduced genomic 5-methylcytosine content in human colonic neoplasia. Cancer Res. 1988 Mar 1;48(5):1159–1161. [PubMed] [Google Scholar]
  23. Feinberg A. P., Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature. 1983 Jan 6;301(5895):89–92. doi: 10.1038/301089a0. [DOI] [PubMed] [Google Scholar]
  24. Fogh J., Wright W. C., Loveless J. D. Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J Natl Cancer Inst. 1977 Feb;58(2):209–214. doi: 10.1093/jnci/58.2.209. [DOI] [PubMed] [Google Scholar]
  25. Forrester K., Almoguera C., Han K., Grizzle W. E., Perucho M. Detection of high incidence of K-ras oncogenes during human colon tumorigenesis. 1987 May 28-Jun 3Nature. 327(6120):298–303. doi: 10.1038/327298a0. [DOI] [PubMed] [Google Scholar]
  26. Gabbert H., Wagner R., Moll R., Gerharz C. D. Tumor dedifferentiation: an important step in tumor invasion. Clin Exp Metastasis. 1985 Oct-Dec;3(4):257–279. doi: 10.1007/BF01585081. [DOI] [PubMed] [Google Scholar]
  27. Gabbiani G., Kapanci Y., Barazzone P., Franke W. W. Immunochemical identification of intermediate-sized filaments in human neoplastic cells. A diagnostic aid for the surgical pathologist. Am J Pathol. 1981 Sep;104(3):206–216. [PMC free article] [PubMed] [Google Scholar]
  28. Gallin W. J., Edelman G. M., Cunningham B. A. Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1038–1042. doi: 10.1073/pnas.80.4.1038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gessler M., Poustka A., Cavenee W., Neve R. L., Orkin S. H., Bruns G. A. Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature. 1990 Feb 22;343(6260):774–778. doi: 10.1038/343774a0. [DOI] [PubMed] [Google Scholar]
  30. Giard D. J., Aaronson S. A., Todaro G. J., Arnstein P., Kersey J. H., Dosik H., Parks W. P. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst. 1973 Nov;51(5):1417–1423. doi: 10.1093/jnci/51.5.1417. [DOI] [PubMed] [Google Scholar]
  31. Haber D. A., Buckler A. J., Glaser T., Call K. M., Pelletier J., Sohn R. L., Douglass E. C., Housman D. E. An internal deletion within an 11p13 zinc finger gene contributes to the development of Wilms' tumor. Cell. 1990 Jun 29;61(7):1257–1269. doi: 10.1016/0092-8674(90)90690-g. [DOI] [PubMed] [Google Scholar]
  32. Harbour J. W., Lai S. L., Whang-Peng J., Gazdar A. F., Minna J. D., Kaye F. J. Abnormalities in structure and expression of the human retinoblastoma gene in SCLC. Science. 1988 Jul 15;241(4863):353–357. doi: 10.1126/science.2838909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hashimoto M., Niwa O., Nitta Y., Takeichi M., Yokoro K. Unstable expression of E-cadherin adhesion molecules in metastatic ovarian tumor cells. Jpn J Cancer Res. 1989 May;80(5):459–463. doi: 10.1111/j.1349-7006.1989.tb02336.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hastings R. J., Franks L. M. Cellular heterogeneity in a tissue culture cell line derived from a human bladder carcinoma. Br J Cancer. 1983 Feb;47(2):233–244. doi: 10.1038/bjc.1983.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hatta K., Nose A., Nagafuchi A., Takeichi M. Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J Cell Biol. 1988 Mar;106(3):873–881. doi: 10.1083/jcb.106.3.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Hatta K., Okada T. S., Takeichi M. A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation. Proc Natl Acad Sci U S A. 1985 May;82(9):2789–2793. doi: 10.1073/pnas.82.9.2789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hyafil F., Babinet C., Jacob F. Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell. 1981 Nov;26(3 Pt 1):447–454. doi: 10.1016/0092-8674(81)90214-2. [DOI] [PubMed] [Google Scholar]
  38. Imhof B. A., Vollmers H. P., Goodman S. L., Birchmeier W. Cell-cell interaction and polarity of epithelial cells: specific perturbation using a monoclonal antibody. Cell. 1983 Dec;35(3 Pt 2):667–675. doi: 10.1016/0092-8674(83)90099-5. [DOI] [PubMed] [Google Scholar]
  39. Kearney J. F., Radbruch A., Liesegang B., Rajewsky K. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J Immunol. 1979 Oct;123(4):1548–1550. [PubMed] [Google Scholar]
  40. Klimpfinger M., Beham A., Denk H. Der pathologische Befund bei kolorektalen Karzinomen und Diskussion seiner Bedeutung für die stadiengerechte Tumortherapie. Wien Klin Wochenschr. 1987 Jul 17;99(14):488–493. [PubMed] [Google Scholar]
  41. Knowles M. A., Franks L. M. Stages in neoplastic transformation of adult epithelial cells by 7,12-dimethylbenz(a)anthracene in vitro. Cancer Res. 1977 Nov;37(11):3917–3924. [PubMed] [Google Scholar]
  42. Koch P. J., Walsh M. J., Schmelz M., Goldschmidt M. D., Zimbelmann R., Franke W. W. Identification of desmoglein, a constitutive desmosomal glycoprotein, as a member of the cadherin family of cell adhesion molecules. Eur J Cell Biol. 1990 Oct;53(1):1–12. [PubMed] [Google Scholar]
  43. Kok K., Osinga J., Carritt B., Davis M. B., van der Hout A. H., van der Veen A. Y., Landsvater R. M., de Leij L. F., Berendsen H. H., Postmus P. E. Deletion of a DNA sequence at the chromosomal region 3p21 in all major types of lung cancer. Nature. 1987 Dec 10;330(6148):578–581. doi: 10.1038/330578a0. [DOI] [PubMed] [Google Scholar]
  44. Kovacs G., Erlandsson R., Boldog F., Ingvarsson S., Müller-Brechlin R., Klein G., Sümegi J. Consistent chromosome 3p deletion and loss of heterozygosity in renal cell carcinoma. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1571–1575. doi: 10.1073/pnas.85.5.1571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lee E. Y., To H., Shew J. Y., Bookstein R., Scully P., Lee W. H. Inactivation of the retinoblastoma susceptibility gene in human breast cancers. Science. 1988 Jul 8;241(4862):218–221. doi: 10.1126/science.3388033. [DOI] [PubMed] [Google Scholar]
  46. Leibovitz A., Stinson J. C., McCombs W. B., 3rd, McCoy C. E., Mazur K. C., Mabry N. D. Classification of human colorectal adenocarcinoma cell lines. Cancer Res. 1976 Dec;36(12):4562–4569. [PubMed] [Google Scholar]
  47. Leppert M., Dobbs M., Scambler P., O'Connell P., Nakamura Y., Stauffer D., Woodward S., Burt R., Hughes J., Gardner E. The gene for familial polyposis coli maps to the long arm of chromosome 5. Science. 1987 Dec 4;238(4832):1411–1413. doi: 10.1126/science.3479843. [DOI] [PubMed] [Google Scholar]
  48. Lieber M., Smith B., Szakal A., Nelson-Rees W., Todaro G. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer. 1976 Jan 15;17(1):62–70. doi: 10.1002/ijc.2910170110. [DOI] [PubMed] [Google Scholar]
  49. Mansouri A., Spurr N., Goodfellow P. N., Kemler R. Characterization and chromosomal localization of the gene encoding the human cell adhesion molecule uvomorulin. Differentiation. 1988 Jun;38(1):67–71. doi: 10.1111/j.1432-0436.1988.tb00593.x. [DOI] [PubMed] [Google Scholar]
  50. Mareel M. M., Van Roy F. M., De Baetselier P. The invasive phenotypes. Cancer Metastasis Rev. 1990 Jul;9(1):45–62. doi: 10.1007/BF00047588. [DOI] [PubMed] [Google Scholar]
  51. Mege R. M., Matsuzaki F., Gallin W. J., Goldberg J. I., Cunningham B. A., Edelman G. M. Construction of epithelioid sheets by transfection of mouse sarcoma cells with cDNAs for chicken cell adhesion molecules. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7274–7278. doi: 10.1073/pnas.85.19.7274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mentges B. Kolonkarzinom. Präoperatives CEA, Tumordifferenzierung und Prognose. Dtsch Med Wochenschr. 1987 Aug 14;112(33):1245–1249. doi: 10.1055/s-2008-1068229. [DOI] [PubMed] [Google Scholar]
  53. Miyatani S., Shimamura K., Hatta M., Nagafuchi A., Nose A., Matsunaga M., Hatta K., Takeichi M. Neural cadherin: role in selective cell-cell adhesion. Science. 1989 Aug 11;245(4918):631–635. doi: 10.1126/science.2762814. [DOI] [PubMed] [Google Scholar]
  54. Moll R., Achtstätter T., Becht E., Balcarova-Ständer J., Ittensohn M., Franke W. W. Cytokeratins in normal and malignant transitional epithelium. Maintenance of expression of urothelial differentiation features in transitional cell carcinomas and bladder carcinoma cell culture lines. Am J Pathol. 1988 Jul;132(1):123–144. [PMC free article] [PubMed] [Google Scholar]
  55. Moll R., Cowin P., Kapprell H. P., Franke W. W. Desmosomal proteins: new markers for identification and classification of tumors. Lab Invest. 1986 Jan;54(1):4–25. [PubMed] [Google Scholar]
  56. Moll R. Epitheliale Tumormarker. Verh Dtsch Ges Pathol. 1986;70:28–50. [PubMed] [Google Scholar]
  57. Nagafuchi A., Shirayoshi Y., Okazaki K., Yasuda K., Takeichi M. Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature. 1987 Sep 24;329(6137):341–343. doi: 10.1038/329341a0. [DOI] [PubMed] [Google Scholar]
  58. Natt E., Magenis R. E., Zimmer J., Mansouri A., Scherer G. Regional assignment of the human loci for uvomorulin (UVO) and chymotrypsinogen B (CTRB) with the help of two overlapping deletions on the long arm of chromosome 16. Cytogenet Cell Genet. 1989;50(2-3):145–148. doi: 10.1159/000132745. [DOI] [PubMed] [Google Scholar]
  59. Nigro J. M., Baker S. J., Preisinger A. C., Jessup J. M., Hostetter R., Cleary K., Bigner S. H., Davidson N., Baylin S., Devilee P. Mutations in the p53 gene occur in diverse human tumour types. Nature. 1989 Dec 7;342(6250):705–708. doi: 10.1038/342705a0. [DOI] [PubMed] [Google Scholar]
  60. Noguchi P., Wallace R., Johnson J., Earley E. M., O'Brien S., Ferrone S., Pellegrino M. A., Milstien J., Needy C., Browne W. Characterization of the WIDR: a human colon carcinoma cell line. In Vitro. 1979 Jun;15(6):401–408. doi: 10.1007/BF02618407. [DOI] [PubMed] [Google Scholar]
  61. Nose A., Nagafuchi A., Takeichi M. Expressed recombinant cadherins mediate cell sorting in model systems. Cell. 1988 Sep 23;54(7):993–1001. doi: 10.1016/0092-8674(88)90114-6. [DOI] [PubMed] [Google Scholar]
  62. Osborn M., Franke W. W., Weber K. Visualization of a system of filaments 7-10 nm thick in cultured cells of an epithelioid line (Pt K2) by immunofluorescence microscopy. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2490–2494. doi: 10.1073/pnas.74.6.2490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Osborn M., Weber K. Tumor diagnosis by intermediate filament typing: a novel tool for surgical pathology. Lab Invest. 1983 Apr;48(4):372–394. [PubMed] [Google Scholar]
  64. Owens R. B., Smith H. S., Nelson-Rees W. A., Springer E. L. Epithelial cell cultures from normal and cancerous human tissues. J Natl Cancer Inst. 1976 Apr;56(4):843–849. doi: 10.1093/jnci/56.4.843. [DOI] [PubMed] [Google Scholar]
  65. Ozawa M., Baribault H., Kemler R. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 1989 Jun;8(6):1711–1717. doi: 10.1002/j.1460-2075.1989.tb03563.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Peyriéras N., Hyafil F., Louvard D., Ploegh H. L., Jacob F. Uvomorulin: a nonintegral membrane protein of early mouse embryo. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6274–6277. doi: 10.1073/pnas.80.20.6274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Rigby C. C., Franks L. M. A human tissue culture cell line from a transitional cell tumour of the urinary bladder: growth, chromosone pattern and ultrastructure. Br J Cancer. 1970 Dec;24(4):746–754. doi: 10.1038/bjc.1970.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Ringwald M., Schuh R., Vestweber D., Eistetter H., Lottspeich F., Engel J., Dölz R., Jähnig F., Epplen J., Mayer S. The structure of cell adhesion molecule uvomorulin. Insights into the molecular mechanism of Ca2+-dependent cell adhesion. EMBO J. 1987 Dec 1;6(12):3647–3653. doi: 10.1002/j.1460-2075.1987.tb02697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Rosengard A. M., Krutzsch H. C., Shearn A., Biggs J. R., Barker E., Margulies I. M., King C. R., Liotta L. A., Steeg P. S. Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development. Nature. 1989 Nov 9;342(6246):177–180. doi: 10.1038/342177a0. [DOI] [PubMed] [Google Scholar]
  70. Semple T. U., Quinn L. A., Woods L. K., Moore G. E. Tumor and lymphoid cell lines from a patient with carcinoma of the colon for a cytotoxicity model. Cancer Res. 1978 May;38(5):1345–1355. [PubMed] [Google Scholar]
  71. Shimoyama Y., Hirohashi S., Hirano S., Noguchi M., Shimosato Y., Takeichi M., Abe O. Cadherin cell-adhesion molecules in human epithelial tissues and carcinomas. Cancer Res. 1989 Apr 15;49(8):2128–2133. [PubMed] [Google Scholar]
  72. Shimoyama Y., Yoshida T., Terada M., Shimosato Y., Abe O., Hirohashi S. Molecular cloning of a human Ca2+-dependent cell-cell adhesion molecule homologous to mouse placental cadherin: its low expression in human placental tissues. J Cell Biol. 1989 Oct;109(4 Pt 1):1787–1794. doi: 10.1083/jcb.109.4.1787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Shirayoshi Y., Okada T. S., Takeichi M. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell. 1983 Dec;35(3 Pt 2):631–638. doi: 10.1016/0092-8674(83)90095-8. [DOI] [PubMed] [Google Scholar]
  74. Slamon D. J., Clark G. M., Wong S. G., Levin W. J., Ullrich A., McGuire W. L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987 Jan 9;235(4785):177–182. doi: 10.1126/science.3798106. [DOI] [PubMed] [Google Scholar]
  75. Slamon D. J., Godolphin W., Jones L. A., Holt J. A., Wong S. G., Keith D. E., Levin W. J., Stuart S. G., Udove J., Ullrich A. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science. 1989 May 12;244(4905):707–712. doi: 10.1126/science.2470152. [DOI] [PubMed] [Google Scholar]
  76. Sluyser M. Steroid/thyroid receptor-like proteins with oncogenic potential: a review. Cancer Res. 1990 Feb 1;50(3):451–458. [PubMed] [Google Scholar]
  77. Sommers C. L., Walker-Jones D., Heckford S. E., Worland P., Valverius E., Clark R., McCormick F., Stampfer M., Abularach S., Gelmann E. P. Vimentin rather than keratin expression in some hormone-independent breast cancer cell lines and in oncogene-transformed mammary epithelial cells. Cancer Res. 1989 Aug 1;49(15):4258–4263. [PubMed] [Google Scholar]
  78. Soule H. D., Vazguez J., Long A., Albert S., Brennan M. A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst. 1973 Nov;51(5):1409–1416. doi: 10.1093/jnci/51.5.1409. [DOI] [PubMed] [Google Scholar]
  79. Steele J. G., Rowlatt C., Sandall J. K., Franks L. M. Identification of exposed surface glycoproteins of four human bladder carcinoma cell lines. Biochim Biophys Acta. 1983 Jul 13;732(1):219–228. doi: 10.1016/0005-2736(83)90206-7. [DOI] [PubMed] [Google Scholar]
  80. Sun T. T., Green H. Immunofluorescent staining of keratin fibers in cultured cells. Cell. 1978 Jul;14(3):469–476. doi: 10.1016/0092-8674(78)90233-7. [DOI] [PubMed] [Google Scholar]
  81. Takahashi T., Nau M. M., Chiba I., Birrer M. J., Rosenberg R. K., Vinocour M., Levitt M., Pass H., Gazdar A. F., Minna J. D. p53: a frequent target for genetic abnormalities in lung cancer. Science. 1989 Oct 27;246(4929):491–494. doi: 10.1126/science.2554494. [DOI] [PubMed] [Google Scholar]
  82. Tsai Y. C., Nichols P. W., Hiti A. L., Williams Z., Skinner D. G., Jones P. A. Allelic losses of chromosomes 9, 11, and 17 in human bladder cancer. Cancer Res. 1990 Jan 1;50(1):44–47. [PubMed] [Google Scholar]
  83. Tsuda H., Zhang W. D., Shimosato Y., Yokota J., Terada M., Sugimura T., Miyamura T., Hirohashi S. Allele loss on chromosome 16 associated with progression of human hepatocellular carcinoma. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6791–6794. doi: 10.1073/pnas.87.17.6791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Vestweber D., Kemler R. Rabbit antiserum against a purified surface glycoprotein decompacts mouse preimplantation embryos and reacts with specific adult tissues. Exp Cell Res. 1984 May;152(1):169–178. doi: 10.1016/0014-4827(84)90241-6. [DOI] [PubMed] [Google Scholar]
  85. Volk T., Geiger B. A-CAM: a 135-kD receptor of intercellular adherens junctions. I. Immunoelectron microscopic localization and biochemical studies. J Cell Biol. 1986 Oct;103(4):1441–1450. doi: 10.1083/jcb.103.4.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Weidner K. M., Behrens J., Vandekerckhove J., Birchmeier W. Scatter factor: molecular characteristics and effect on the invasiveness of epithelial cells. J Cell Biol. 1990 Nov;111(5 Pt 1):2097–2108. doi: 10.1083/jcb.111.5.2097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Weinstein R. S., Merk F. B., Alroy J. The structure and function of intercellular junctions in cancer. Adv Cancer Res. 1976;23:23–89. doi: 10.1016/s0065-230x(08)60543-6. [DOI] [PubMed] [Google Scholar]
  88. Yunis A. A., Arimura G. K., Russin D. J. Human pancreatic carcinoma (MIA PaCa-2) in continuous culture: sensitivity to asparaginase. Int J Cancer. 1977 Jan;19(1):128–135. doi: 10.1002/ijc.2910190118. [DOI] [PubMed] [Google Scholar]
  89. Zbar B., Brauch H., Talmadge C., Linehan M. Loss of alleles of loci on the short arm of chromosome 3 in renal cell carcinoma. 1987 Jun 25-Jul 1Nature. 327(6124):721–724. doi: 10.1038/327721a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES

-