Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 May 1;121(3):643–654. doi: 10.1083/jcb.121.3.643

Regulation of E-cadherin-mediated adhesion by muscarinic acetylcholine receptors in small cell lung carcinoma

PMCID: PMC2119556  PMID: 8387530

Abstract

We present the first evidence that adhesion mediated by a member of the cadherin gene family can be regulated by a G protein-coupled receptor. We show that activating the M3 muscarinic acetylcholine receptor (mAChR) rapidly induces E-cadherin-mediated adhesion in a small cell lung carcinoma (SCLC) cell line. This response is inhibited by E- cadherin antibodies, and does not occur in another SCLC cell line which expresses functional mAChR but reduced levels of E-cadherin. Protein kinase C may be involved, since phorbol 12-myristate 13-acetate also induces E-cadherin-mediated aggregation. Immunofluorescence analyses indicate that mAChR activation does not grossly alter E-cadherin surface expression or localization at areas of cell-cell contact, suggesting mAChR activation may increase E-cadherin binding activity. Our findings suggest that G protein-coupled receptors may regulate processes involving cadherin-mediated adhesion, such as embryonic development, neurogenesis, and cancer metastasis.

Full Text

The Full Text of this article is available as a PDF (2.4 MB).

Selected References

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

  1. Aletsee-Ufrecht M. C., Langley K., Rotsch M., Havemann K., Gratzl M. NCAM: a surface marker for human small cell lung cancer cells. FEBS Lett. 1990 Jul 16;267(2):295–300. doi: 10.1016/0014-5793(90)80948-i. [DOI] [PubMed] [Google Scholar]
  2. Andersson A. M., Moran N., Gaardsvoll H., Linnemann D., Bjerkvig R., Laerum O. D., Bock E. Characterization of NCAM expression and function in BT4C and BT4Cn glioma cells. Int J Cancer. 1991 Jan 2;47(1):124–129. doi: 10.1002/ijc.2910470122. [DOI] [PubMed] [Google Scholar]
  3. Ashkenazi A., Ramachandran J., Capon D. J. Acetylcholine analogue stimulates DNA synthesis in brain-derived cells via specific muscarinic receptor subtypes. Nature. 1989 Jul 13;340(6229):146–150. doi: 10.1038/340146a0. [DOI] [PubMed] [Google Scholar]
  4. Bailey C. H., Chen M., Keller F., Kandel E. R. Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth in Aplysia. Science. 1992 May 1;256(5057):645–649. doi: 10.1126/science.1585177. [DOI] [PubMed] [Google Scholar]
  5. Ball E. D., Sorenson G. D., Pettengill O. S. Expression of myeloid and major histocompatibility antigens on small cell carcinoma of the lung cell lines analyzed by cytofluorography: modulation by gamma-interferon. Cancer Res. 1986 May;46(5):2335–2339. [PubMed] [Google Scholar]
  6. Baxter G., Oto E., Daniel-Issakani S., Strulovici B. Constitutive presence of a catalytic fragment of protein kinase C epsilon in a small cell lung carcinoma cell line. J Biol Chem. 1992 Jan 25;267(3):1910–1917. [PubMed] [Google Scholar]
  7. Beckerle M. C. The adhesion plaque protein, talin, is phosphorylated in vivo in chicken embryo fibroblasts exposed to a tumor-promoting phorbol ester. Cell Regul. 1990 Jan;1(2):227–236. doi: 10.1091/mbc.1.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bepler G., Ostholt M., Neumann K., Holle R., Jaques G., Havemann K., Kalbfleisch H. Carcinoembryonic antigen as differentiation marker for small cell lung cancer in vitro and its clinical relevance. Anticancer Res. 1989 Nov-Dec;9(6):1525–1530. [PubMed] [Google Scholar]
  9. Bonner T. I. The molecular basis of muscarinic receptor diversity. Trends Neurosci. 1989 Apr;12(4):148–151. doi: 10.1016/0166-2236(89)90054-4. [DOI] [PubMed] [Google Scholar]
  10. Boyd A. W., Dunn S. M., Fecondo J. V., Culvenor J. G., Dührsen U., Burns G. F., Wawryk S. O. Regulation of expression of a human intercellular adhesion molecule (ICAM-1) during lymphohematopoietic differentiation. Blood. 1989 May 15;73(7):1896–1903. [PubMed] [Google Scholar]
  11. Boyd A. W., Wawryk S. O., Burns G. F., Fecondo J. V. Intercellular adhesion molecule 1 (ICAM-1) has a central role in cell-cell contact-mediated immune mechanisms. Proc Natl Acad Sci U S A. 1988 May;85(9):3095–3099. doi: 10.1073/pnas.85.9.3095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bussemakers M. J., van Moorselaar R. J., Giroldi L. A., Ichikawa T., Isaacs J. T., Takeichi M., Debruyne F. M., Schalken J. A. Decreased expression of E-cadherin in the progression of rat prostatic cancer. Cancer Res. 1992 May 15;52(10):2916–2922. [PubMed] [Google Scholar]
  13. Carter W. G., Wayner E. A., Bouchard T. S., Kaur P. The role of integrins alpha 2 beta 1 and alpha 3 beta 1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol. 1990 Apr;110(4):1387–1404. doi: 10.1083/jcb.110.4.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chen W. C., Obrink B. Cell-cell contacts mediated by E-cadherin (uvomorulin) restrict invasive behavior of L-cells. J Cell Biol. 1991 Jul;114(2):319–327. doi: 10.1083/jcb.114.2.319. [DOI] [PMC free article] [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. Cunningham J. M., Lennon V. A., Lambert E. H., Scheithauer B. Acetylcholine receptors in small cell carcinomas. J Neurochem. 1985 Jul;45(1):159–167. doi: 10.1111/j.1471-4159.1985.tb05488.x. [DOI] [PubMed] [Google Scholar]
  17. Diamond M. S., Staunton D. E., de Fougerolles A. R., Stacker S. A., Garcia-Aguilar J., Hibbs M. L., Springer T. A. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol. 1990 Dec;111(6 Pt 2):3129–3139. doi: 10.1083/jcb.111.6.3129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Doherty P., Ashton S. V., Moore S. E., Walsh F. S. Morphoregulatory activities of NCAM and N-cadherin can be accounted for by G protein-dependent activation of L- and N-type neuronal Ca2+ channels. Cell. 1991 Oct 4;67(1):21–33. doi: 10.1016/0092-8674(91)90569-k. [DOI] [PubMed] [Google Scholar]
  19. Dustin M. L., Springer T. A. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 1989 Oct 19;341(6243):619–624. doi: 10.1038/341619a0. [DOI] [PubMed] [Google Scholar]
  20. Edelman G. M., Crossin K. L. Cell adhesion molecules: implications for a molecular histology. Annu Rev Biochem. 1991;60:155–190. doi: 10.1146/annurev.bi.60.070191.001103. [DOI] [PubMed] [Google Scholar]
  21. Feldman L. E., Shin K. C., Natale R. B., Todd R. F., 3rd Beta 1 integrin expression on human small cell lung cancer cells. Cancer Res. 1991 Feb 15;51(4):1065–1070. [PubMed] [Google Scholar]
  22. Friedlander D. R., Mège R. M., Cunningham B. A., Edelman G. M. Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7043–7047. doi: 10.1073/pnas.86.18.7043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Frixen U. H., Behrens J., Sachs M., Eberle G., Voss B., Warda A., Löchner D., Birchmeier W. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol. 1991 Apr;113(1):173–185. doi: 10.1083/jcb.113.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fujisawa M., Sasaki M., Fujii H., Okamura K., Miyata M., Hashimoto H., Yachiku S., Yamauchi K., Yamaguchi S., Inagaki N. [Treatment of urinary tract infection with cefixime]. Hinyokika Kiyo. 1989 Nov;35(11):1989–1992. [PubMed] [Google Scholar]
  25. Grove D. S., Mastro A. M. Prevention of the TPA-mediated down-regulation of protein kinase C. Biochem Biophys Res Commun. 1988 Feb 29;151(1):94–99. doi: 10.1016/0006-291x(88)90563-3. [DOI] [PubMed] [Google Scholar]
  26. Gutkind J. S., Novotny E. A., Brann M. R., Robbins K. C. Muscarinic acetylcholine receptor subtypes as agonist-dependent oncogenes. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4703–4707. doi: 10.1073/pnas.88.11.4703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Haimovich B., Aneskievich B. J., Boettiger D. Cellular partitioning of beta-1 integrins and their phosphorylated forms is altered after transformation by Rous sarcoma virus or treatment with cytochalasin D. Cell Regul. 1991 Apr;2(4):271–283. doi: 10.1091/mbc.2.4.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hemler M. E., Elices M. J., Chan B. M., Zetter B., Matsuura N., Takada Y. Multiple ligand binding functions for VLA-2 (alpha 2 beta 1) and VLA-3 (alpha 3 beta 1) in the integrin family. Cell Differ Dev. 1990 Dec 2;32(3):229–238. doi: 10.1016/0922-3371(90)90035-u. [DOI] [PubMed] [Google Scholar]
  29. Hibbs M. L., Jakes S., Stacker S. A., Wallace R. W., Springer T. A. The cytoplasmic domain of the integrin lymphocyte function-associated antigen 1 beta subunit: sites required for binding to intercellular adhesion molecule 1 and the phorbol ester-stimulated phosphorylation site. J Exp Med. 1991 Nov 1;174(5):1227–1238. doi: 10.1084/jem.174.5.1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hibbs M. L., Xu H., Stacker S. A., Springer T. A. Regulation of adhesion of ICAM-1 by the cytoplasmic domain of LFA-1 integrin beta subunit. Science. 1991 Mar 29;251(5001):1611–1613. doi: 10.1126/science.1672776. [DOI] [PubMed] [Google Scholar]
  31. Hirano S., Kimoto N., Shimoyama Y., Hirohashi S., Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell. 1992 Jul 24;70(2):293–301. doi: 10.1016/0092-8674(92)90103-j. [DOI] [PubMed] [Google Scholar]
  32. Hirst R., Horwitz A., Buck C., Rohrschneider L. Phosphorylation of the fibronectin receptor complex in cells transformed by oncogenes that encode tyrosine kinases. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6470–6474. doi: 10.1073/pnas.83.17.6470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hulme E. C., Birdsall N. J., Buckley N. J. Muscarinic receptor subtypes. Annu Rev Pharmacol Toxicol. 1990;30:633–673. doi: 10.1146/annurev.pa.30.040190.003221. [DOI] [PubMed] [Google Scholar]
  34. Hynes R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. doi: 10.1016/0092-8674(92)90115-s. [DOI] [PubMed] [Google Scholar]
  35. Johnson J. P. Cell adhesion molecules of the immunoglobulin supergene family and their role in malignant transformation and progression to metastatic disease. Cancer Metastasis Rev. 1991 May;10(1):11–22. doi: 10.1007/BF00046840. [DOI] [PubMed] [Google Scholar]
  36. Julius D., Huang K. N., Livelli T. J., Axel R., Jessell T. M. The 5HT2 receptor defines a family of structurally distinct but functionally conserved serotonin receptors. Proc Natl Acad Sci U S A. 1990 Feb;87(3):928–932. doi: 10.1073/pnas.87.3.928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Julius D., Livelli T. J., Jessell T. M., Axel R. Ectopic expression of the serotonin 1c receptor and the triggering of malignant transformation. Science. 1989 Jun 2;244(4908):1057–1062. doi: 10.1126/science.2727693. [DOI] [PubMed] [Google Scholar]
  38. Kawamoto S., Bengur A. R., Sellers J. R., Adelstein R. S. In situ phosphorylation of human platelet myosin heavy and light chains by protein kinase C. J Biol Chem. 1989 Feb 5;264(4):2258–2265. [PubMed] [Google Scholar]
  39. Kibbelaar R. E., Moolenaar C. E., Michalides R. J., Bitter-Suermann D., Addis B. J., Mooi W. J. Expression of the embryonal neural cell adhesion molecule N-CAM in lung carcinoma. Diagnostic usefulness of monoclonal antibody 735 for the distinction between small cell lung cancer and non-small cell lung cancer. J Pathol. 1989 Sep;159(1):23–28. doi: 10.1002/path.1711590108. [DOI] [PubMed] [Google Scholar]
  40. Knudsen K. A., Wheelock M. J. Plakoglobin, or an 83-kD homologue distinct from beta-catenin, interacts with E-cadherin and N-cadherin. J Cell Biol. 1992 Aug;118(3):671–679. doi: 10.1083/jcb.118.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lagunowich L. A., Grunwald G. B. Tissue and age-specificity of post-translational modifications of N-cadherin during chick embryo development. Differentiation. 1991 May;47(1):19–27. doi: 10.1111/j.1432-0436.1991.tb00217.x. [DOI] [PubMed] [Google Scholar]
  42. Lagunowich L. A., Schneider J. C., Chasen S., Grunwald G. B. Immunohistochemical and biochemical analysis of N-cadherin expression during CNS development. J Neurosci Res. 1992 Jun;32(2):202–208. doi: 10.1002/jnr.490320209. [DOI] [PubMed] [Google Scholar]
  43. Leoncini P., Bellizzi de Marco E., Bugnoli M., Mencarelli C., Vindigni C., Cintorino M. Expression of phosphorylated and non-phosphorylated neurofilament subunits and cytokeratins in neuroendocrine lung tumors. Pathol Res Pract. 1989 Dec;185(6):848–855. doi: 10.1016/S0344-0338(89)80285-7. [DOI] [PubMed] [Google Scholar]
  44. Litchfield D. W., Ball E. H. Phosphorylation of the cytoskeletal protein talin by protein kinase C. Biochem Biophys Res Commun. 1986 Feb 13;134(3):1276–1283. doi: 10.1016/0006-291x(86)90388-8. [DOI] [PubMed] [Google Scholar]
  45. Makgoba M. W., Sanders M. E., Ginther Luce G. E., Dustin M. L., Springer T. A., Clark E. A., Mannoni P., Shaw S. ICAM-1 a ligand for LFA-1-dependent adhesion of B, T and myeloid cells. Nature. 1988 Jan 7;331(6151):86–88. doi: 10.1038/331086a0. [DOI] [PubMed] [Google Scholar]
  46. Maneckjee R., Minna J. D. Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines. Proc Natl Acad Sci U S A. 1990 May;87(9):3294–3298. doi: 10.1073/pnas.87.9.3294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Matsunaga M., Hatta K., Nagafuchi A., Takeichi M. Guidance of optic nerve fibres by N-cadherin adhesion molecules. Nature. 1988 Jul 7;334(6177):62–64. doi: 10.1038/334062a0. [DOI] [PubMed] [Google Scholar]
  48. Matsuyoshi N., Hamaguchi M., Taniguchi S., Nagafuchi A., Tsukita S., Takeichi M. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J Cell Biol. 1992 Aug;118(3):703–714. doi: 10.1083/jcb.118.3.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Mayford M., Barzilai A., Keller F., Schacher S., Kandel E. R. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science. 1992 May 1;256(5057):638–644. doi: 10.1126/science.1585176. [DOI] [PubMed] [Google Scholar]
  50. McCrea P. D., Gumbiner B. M. Purification of a 92-kDa cytoplasmic protein tightly associated with the cell-cell adhesion molecule E-cadherin (uvomorulin). Characterization and extractability of the protein complex from the cell cytostructure. J Biol Chem. 1991 Mar 5;266(7):4514–4520. [PubMed] [Google Scholar]
  51. McNeill H., Ozawa M., Kemler R., Nelson W. J. Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity. Cell. 1990 Jul 27;62(2):309–316. doi: 10.1016/0092-8674(90)90368-o. [DOI] [PubMed] [Google Scholar]
  52. Montgomery K. F., Osborn L., Hession C., Tizard R., Goff D., Vassallo C., Tarr P. I., Bomsztyk K., Lobb R., Harlan J. M. Activation of endothelial-leukocyte adhesion molecule 1 (ELAM-1) gene transcription. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6523–6527. doi: 10.1073/pnas.88.15.6523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Nagafuchi A., Takeichi M. Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regul. 1989 Nov;1(1):37–44. doi: 10.1091/mbc.1.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Nagafuchi A., Takeichi M., Tsukita S. The 102 kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell. 1991 May 31;65(5):849–857. doi: 10.1016/0092-8674(91)90392-c. [DOI] [PubMed] [Google Scholar]
  55. 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]
  56. Patarroyo M., Clark E. A., Prieto J., Kantor C., Gahmberg C. G. Identification of a novel adhesion molecule in human leukocytes by monoclonal antibody LB-2. FEBS Lett. 1987 Jan 5;210(2):127–131. doi: 10.1016/0014-5793(87)81321-2. [DOI] [PubMed] [Google Scholar]
  57. Patel K., Moore S. E., Dickson G., Rossell R. J., Beverley P. C., Kemshead J. T., Walsh F. S. Neural cell adhesion molecule (NCAM) is the antigen recognized by monoclonal antibodies of similar specificity in small-cell lung carcinoma and neuroblastoma. Int J Cancer. 1989 Oct 15;44(4):573–578. doi: 10.1002/ijc.2910440402. [DOI] [PubMed] [Google Scholar]
  58. Peifer M., McCrea P. D., Green K. J., Wieschaus E., Gumbiner B. M. The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J Cell Biol. 1992 Aug;118(3):681–691. doi: 10.1083/jcb.118.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Reichardt L. F., Bixby J. L., Hall D. E., Ignatius M. J., Neugebauer K. M., Tomaselli K. J. Integrins and cell adhesion molecules: neuronal receptors that regulate axon growth on extracellular matrices and cell surfaces. Dev Neurosci. 1989;11(4-5):332–347. doi: 10.1159/000111910. [DOI] [PubMed] [Google Scholar]
  60. Roubin R., Deagostini-Bazin H., Hirsch M. R., Goridis C. Modulation of NCAM expression by transforming growth factor-beta, serum, and autocrine factors. J Cell Biol. 1990 Aug;111(2):673–684. doi: 10.1083/jcb.111.2.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Ruggeri B., Caamano J., Slaga T. J., Conti C. J., Nelson W. J., Klein-Szanto A. J. Alterations in the expression of uvomorulin and Na+,K(+)-adenosine triphosphatase during mouse skin tumor progression. Am J Pathol. 1992 May;140(5):1179–1185. [PMC free article] [PubMed] [Google Scholar]
  62. Rygaard K., Møller C., Bock E., Spang-Thomsen M. Expression of cadherin and NCAM in human small cell lung cancer cell lines and xenografts. Br J Cancer. 1992 Apr;65(4):573–577. doi: 10.1038/bjc.1992.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schubert D. The possible role of adhesion in synaptic modification. Trends Neurosci. 1991 Apr;14(4):127–130. doi: 10.1016/0166-2236(91)90078-9. [DOI] [PubMed] [Google Scholar]
  64. Sefton M., Johnson M. H., Clayton L. Synthesis and phosphorylation of uvomorulin during mouse early development. Development. 1992 May;115(1):313–318. doi: 10.1242/dev.115.1.313. [DOI] [PubMed] [Google Scholar]
  65. Shaw L. M., Messier J. M., Mercurio A. M. The activation dependent adhesion of macrophages to laminin involves cytoskeletal anchoring and phosphorylation of the alpha 6 beta 1 integrin. J Cell Biol. 1990 Jun;110(6):2167–2174. doi: 10.1083/jcb.110.6.2167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. 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]
  67. Sorenson G. D., Pettengill O. S., Cate C. C., Ghatei M. A., Molyneux K. E., Gosselin E. J., Bloom S. R. Bombesin and calcitonin secretion by pulmonary carcinoma is modulated by cholinergic receptors. Life Sci. 1983 Nov 7;33(19):1939–1944. doi: 10.1016/0024-3205(83)90679-3. [DOI] [PubMed] [Google Scholar]
  68. Symington B. E., Symington F. W., Rohrschneider L. R. Phorbol ester induces increased expression, altered glycosylation, and reduced adhesion of K562 erythroleukemia cell fibronectin receptors. J Biol Chem. 1989 Aug 5;264(22):13258–13266. [PubMed] [Google Scholar]
  69. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 1991 Mar 22;251(5000):1451–1455. doi: 10.1126/science.2006419. [DOI] [PubMed] [Google Scholar]
  70. Valent P., Bevec D., Maurer D., Besemer J., Di Padova F., Butterfield J. H., Speiser W., Majdic O., Lechner K., Bettelheim P. Interleukin 4 promotes expression of mast cell ICAM-1 antigen. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3339–3342. doi: 10.1073/pnas.88.8.3339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Valmu L., Autero M., Siljander P., Patarroyo M., Gahmberg C. G. Phosphorylation of the beta-subunit of CD11/CD18 integrins by protein kinase C correlates with leukocyte adhesion. Eur J Immunol. 1991 Nov;21(11):2857–2862. doi: 10.1002/eji.1830211130. [DOI] [PubMed] [Google Scholar]
  72. Vestweber D., Kemler R. Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 1985 Dec 16;4(13A):3393–3398. doi: 10.1002/j.1460-2075.1985.tb04095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Vleminckx K., Vakaet L., Jr, Mareel M., Fiers W., van Roy F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell. 1991 Jul 12;66(1):107–119. doi: 10.1016/0092-8674(91)90143-m. [DOI] [PubMed] [Google Scholar]
  74. Wanke E., Ferroni A., Malgaroli A., Ambrosini A., Pozzan T., Meldolesi J. Activation of a muscarinic receptor selectively inhibits a rapidly inactivated Ca2+ current in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4313–4317. doi: 10.1073/pnas.84.12.4313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Weynants P., Humblet Y., Canon J. L., Symann M. Biology of small cell lung cancer: an overview. Eur Respir J. 1990 Jun;3(6):699–714. [PubMed] [Google Scholar]
  76. Wheelock M. J., Jensen P. J. Regulation of keratinocyte intercellular junction organization and epidermal morphogenesis by E-cadherin. J Cell Biol. 1992 Apr;117(2):415–425. doi: 10.1083/jcb.117.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Wilkins J. A., Stupack D., Stewart S., Caixia S. Beta 1 integrin-mediated lymphocyte adherence to extracellular matrix is enhanced by phorbol ester treatment. Eur J Immunol. 1991 Feb;21(2):517–522. doi: 10.1002/eji.1830210239. [DOI] [PubMed] [Google Scholar]
  78. Williams C. L., Hay J. E., Huiatt T. W., Lennon V. A. Paraneoplastic IgG striational autoantibodies produced by clonal thymic B cells and in serum of patients with myasthenia gravis and thymoma react with titin. Lab Invest. 1992 Mar;66(3):331–336. [PubMed] [Google Scholar]
  79. Williams C. L., Lennon V. A. Activation of M3 muscarinic acetylcholine receptors inhibits voltage-dependent calcium influx in small cell lung carcinoma. J Biol Chem. 1990 Jan 25;265(3):1443–1447. [PubMed] [Google Scholar]
  80. Williams C. L., Lennon V. A. Activation of muscarinic acetylcholine receptors inhibits cell cycle progression of small cell lung carcinoma. Cell Regul. 1991 May;2(5):373–381. doi: 10.1091/mbc.2.5.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Winkel G. K., Ferguson J. E., Takeichi M., Nuccitelli R. Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. Dev Biol. 1990 Mar;138(1):1–15. doi: 10.1016/0012-1606(90)90171-e. [DOI] [PubMed] [Google Scholar]
  82. Young D., Waitches G., Birchmeier C., Fasano O., Wigler M. Isolation and characterization of a new cellular oncogene encoding a protein with multiple potential transmembrane domains. Cell. 1986 Jun 6;45(5):711–719. doi: 10.1016/0092-8674(86)90785-3. [DOI] [PubMed] [Google Scholar]
  83. Zhu D. Z., Cheng C. F., Pauli B. U. Mediation of lung metastasis of murine melanomas by a lung-specific endothelial cell adhesion molecule. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9568–9572. doi: 10.1073/pnas.88.21.9568. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES