Autocrine production of insulin-like growth factor-I (IGF-I) affects paracellular transport across epithelial cells in vitro

Cell Communication and Adhesion

Volumn 14, Issue 2-3, 2007, Pages 85-98

  Paye, Julie M D ^a   Akers, R Michael ^b   Huckle, William R ^b   Forsten Williams, Kimberly ^a  

^a State University   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Autocrine; E cadherin; Epithelial; IGF I receptor (IGF IR); IGFBP 2; IGFBP 3; Insulin like growth factor I (IGF I); MAC T; Mammary alveolar cells large T antigen; Mammary epithelial cells

Indexed keywords

OCCLUDIN; PHENOLSULFONPHTHALEIN; SOMATOMEDIN C; UVOMORULIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; AUTOCRINE EFFECT; BREAST CELL; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL TRANSPORT; CONTROLLED STUDY; COW; EPITHELIUM CELL; GENETIC TRANSFECTION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION;

ADHERENS JUNCTIONS; ANIMALS; AUTOCRINE COMMUNICATION; BIOLOGICAL TRANSPORT; CATTLE; CELL COUNT; CELLS, CULTURED; COCULTURE TECHNIQUES; EPITHELIAL CELLS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR I; MEMBRANE PROTEINS; PARACRINE COMMUNICATION; PHENOLSULFONPHTHALEIN; RECEPTOR, IGF TYPE 1; TIGHT JUNCTIONS;

BOVINAE;

EID: 34547659869     PISSN: 15419061     EISSN: 15435180     Source Type: Journal    
DOI: 10.1080/15419060701463116     Document Type: Article

References (76)

1. Adams, T. E., Epa, V. C., Garrett, T. P. and Ward, C. W. (2000) Structure and function of the type 1 insulin-like growth factor receptor. Cell Mol Life Sci, 57, pp. 1050-1093.
2. Andre, F., Rigot, V., Thimonier, J., Montixi, C., Parat, F., Pommier, G., Marvaldi, J. and Luis, J. (1999) Integrins and E-cadherin cooperate with IGF-I to induce migration of epithelial colonic cells. Int J Cancer, 83, pp. 497-505.
3. Baker, K. M., Chernin, M. I., Schreiber, T., Sanghi, S., Haiderzaidi, S., Booz, G. W., Dostal, D. E. and Kumar, R. (2004) Evidence of a novel intracrine mechanism in angiotensin II-induced cardiac hypertrophy. Regul Pept, 120, pp. 5-13.
4. Baumrucker, C. R. (2005) Intracrine signaling in the mammary gland. Livestock Production Science, 98, pp. 47-56.
5. Bayne, M. L., Applebaum, J., Chicchi, G. G., Miller, R. E. and Cascieri, M. A. (1990) The roles of tyrosines 24, 31, and 60 in the high affinity binding of insulin-like growth factor-I to the type 1 insulin-like growth factor receptor. J Biol Chem, 265, pp. 15648-15652.
6. Beavon, I. R. (2000) The E-cadherin-catenin complex in tumour metastasis: Structure, function and regulation. Eur J Cancer, 36, pp. 1607-1620.
7. Berry, S. D., McFadden, T. B., Pearson, R. E. and Akers, R. M. (2001) A local increase in the mammary IGF-I: IGFBP-3 ratio mediates the mammogenic effects of estrogen and growth hormone. Domest Anim Endocrinol, 21, pp. 39-53.
8. Bilak, M. M., Hossain, W. A. and Morest, D. K. (2003) Intracellular fibroblast growth factor produces effects different from those of extracellular application on development of avian cochleovestibular ganglion cells in vitro. J Neurosci Res, 71, pp. 629-647.
9. Braga, V. (2002) Cell-cell adhesion and signalling. Curr Opin Cell Biol, 14, p. 546.
10. Bremnes, R. M., Veve, R., Hirsch, F. R. and Franklin, W. A. (2002) The E-cadherin cell-cell adhesion complex and lung cancer invasion, metastasis, and prognosis. Lung Cancer, 36, pp. 115-124.
11. Burke, J. M. and Hong, J. (2006) Fate of E-cadherin in early RPE cultures: Transient accumulation of truncated peptides at nonjunctional sites. Invest Ophthalmol Vis Sci, 47, pp. 3635-3643.
12. Burroughs, K. D., Barrett, J. C. and DiAugustine, R. P. (2003) Phosphatidylinositol 3-kinase and mek1/2 are necessary for insulin-like growth factor-I-induced vascular endothelial growth factor synthesis in prostate epithelial cells: A role for hypoxia-inducible factor-1?. Mol Cancer Res, 1, pp. 312-322.
13. Cohick, W. S. and Turner, J. D. (1998) Regulation of IGF binding protein synthesis by a bovine mammary epithelial cell line. J Endocrinol, 157, pp. 327-336.
14. Conacci-Sorrell, M., Zhurinsky, J. and Ben-Ze'ev, A. (2002) The cadherin-catenin adhesion system in signaling and cancer. J Clin Invest, 109, pp. 987-991.
15. DeWitt, A. E., Dong, J. Y., Wiley, H. S. and Lauffenburger, D. A. (2001) Quantitative analysis of the EGF receptor autocrine system reveals cryptic regulation of cell response by ligand capture. J Cell Sci, 114, pp. 2301-2313.
16. Dietrich, C., Scherwat, J., Faust, D. and Oesch, F. (2002) Subcellular localization of beta-catenin is regulated by cell density. Biochem Biophys Res Commun, 292, pp. 195-199.
17. Dubois, V., Couissi, D., Schonne, E., Schneider, Y. J., Remacle, C. and Trouet, A. (1993) Estrogen and insulin modulation of intracellular insulin-like growth factor binding proteins in human breast cancer cells: Possible involvement in lysosomal hydrolases oversecretion. Biochem Biophys Res Commun, 192, pp. 295-301.
18. Dunn, S. E., Ehrlich, M., Sharp, N. J., Reiss, K., Solomon, G., Hawkins, R., Baserga, R. and Barrett, J. C. (1998) A dominant negative mutant of the insulin-like growth factor-I receptor inhibits the adhesion, invasion, and metastasis of breast cancer. Cancer Res, 58, pp. 3353-3361.
19. Ericson, L. E. and Nilsson, M. (1996) Effects of insulin-like growth factor I on growth, epithelial barrier and iodide transport in polarized pig thyrocyte monolayers. Eur J Endocrinol, 135, pp. 118-127.
20. Forsten, K. E. and Lanffenburger, D. A. (1992) Autocrine ligands binding to cell receptors. Mathematical analysis of competition by solution "decoys". Biophys J, 61, pp. 518-529.
21. Forsten, K. E. and Lanffenburger, D. A. (1992) Interrupting autocrine ligand-receptor binding: Comparison between receptor blockers and ligand decoys. Biophys J, 63, pp. 857-861.
22. Forsythe, R. M., Xu, D. Z. and Deitch, E. A. (2002) Lipopolysaccharide-induced enterocyte-derived nitric oxide induces intestinal monolayer permeability in an autocrine fashion. Shock, 17, pp. 180-184.
23. Friedl, J., Puhlmann, M., Bartlett, D. L., Libutti, S. K., Turner, E. N., Gnant, M. F. and Alexander, H. R. (2002) Induction of permeability across endothelial cell monolayers by tumor necrosis factor (TNF) occurs via a tissue factor-dependent mechanism: Relationship between the procoagulant and permeability effects of TNF. Blood, 100, pp. 1334-1339.
24. Gottardi, C. J. and Gumbiner, B. M. (2001) Adhesion signaling: How beta-catenin interacts with its partners. Curr Biol, 11, pp. R792-R794.
25. Grande, M., Franzen, A., Karlsson, J. O., Ericson, L. E., Heldin, N. E. and Nilsson, M. (2002) Transforming growth factor-beta and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes. J Cell Sci, 115, pp. 4227-4236.
26. Grill, C. J. and Cohick, W. S. (2000) Insulin-like growth factor binding protein-3 mediates IGF-I action in a bovine mammary epithelial cell line independent of an IGF interaction. J Cell Physiol, 183, pp. 273-283.
27. Grill, C. J., Sivaprasad, U. and Cohick, W. S. (2002) Constitutive expression of IGF-binding protein-3 by mammary epithelial cells alters signaling through Akt and p70S6 kinase. J Mol Endocrinol, 29, pp. 153-162.
28. Guvakova, M. A. and Surmacz, E. (1997) Overexpressed IGF-I receptors reduce estrogen growth requirements, enhance survival, and promote E-cadherin-mediated cell-cell adhesion in human breast cancer cells. Exp Cell Res, 231, pp. 149-162.
29. Hellawell, G. O., Turner, G. D., Davies, D. R., Poulsom, R., Brewster, S. F. and Macaulay, V. M. (2002) Expression of the type 1 insulin-like growth factor receptor is up-regulated in primary prostate cancer and commonly persists in metastatic disease. Cancer Res, 62, pp. 2942-2950.
30. Hossenlopp, P., Seurin, D., Segovia-Quinson, B., Hardouin, S. and Binoux, M. (1986) Analysis of serum insulin-like growth factor binding proteins using western blotting: Use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem, 154, pp. 138-143.
31. Huynh, H. T., Robitaille, G. and Turner, J. D. (1991) Establishment of bovine mammary epithelial cells (MAC-T): An in vitro model for bovine lactation. Exp Cell Res, 197, pp. 191-199.
32. Jiang, W. G., Martin, T. A., Matsumoto, K., Nakamura, T. and Mansel, R. E. (1999) Hepatocyte growth factor/scatter factor decreases the expression of occludin and transendothelial resistance (TER) and increases paracellular permeability in human vascular endothelial cells. J Cell Physiol, 181, pp. 319-329.
33. Jones, S. M. and Kazlauskas, A. (2001) Growth factor-dependent signaling and cell cycle progression. Chem Rev, 101, pp. 2413-2423.
34. Kleeff, J., Shi, X., Bode, H. P., Hoover, K., Shrikhande, S., Bryant, P. J., Korc, M., Buchler, M. W. and Friess, H. (2001) Altered expression and localization of the tight junction protein ZO-1 in primary and metastatic pancreatic cancer. Pancreas, 23, pp. 259-2565.
35. Kolodziejczyk, J., Gertler, A., Leibovich, H., Rzasa, J. and Gregoraszczuk, E. L. (2003) Synergistic action of growth hormone and insulin-like growth factor I (IGF-I) on proliferation and estradiol secretion in porcine granulosa and theca cells cultured alone or in coculture. Theriogenology, 60, pp. 559-570.
36. Lauffenburger, D. A., Oehrtman, G. T., Walker, L. and Wiley, H. S. (1998) Real-time quantitative measurement of autocrine ligand binding indicates that autocrine loops are spatially localized. Proc Natl Acad Sci USA, 95, pp. 15368-15373.
37. Schaider, H., Satyamoorthy, K., Hanakawa, Y., Hashimoto, K. and Herlyn, M. (2001) Downregulation of E-cadherin and Desmoglein 1 by autocrine hepatocyte growth factor during melanoma development. Oncogene, 20, pp. 8125-8135.
38. Lin, S. B., Hsieh, S. H., Hsu, H. L., Lai, M. Y., Kan, L. S. and Au, L. C. (1997) Antisense oligodeoxynucleotides of IGF-II selectively inhibit growth of human hepatoma cells overproducing IGF-II. J Biochem (Tokyo), 122, pp. 717-722.
39. Liou, G. I., Matragoon, S., Samuel, S., Behzadian, M. A., Tsai, N. T., Roon, P., Hunt, D. M., Hunt, R. C., Caldwell, R. B. and Marcus, D. M. (2002) MAP kinase and beta-catenin signaling in HGF induced RPE migration. Mol Vis, 8, pp. 483-493.
40. Lui, W. Y., Wong, C. H., Mruk, D. D. and Cheng, C. Y. (2003) TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: An in vivo study. Endocrinology, 144, pp. 1139-1142.
41. Mauro, L., Bartucci, M., Morelli, C., Ando, S. and Surmacz, E. (2001) Igf-I receptor-induced cell-cell adhesion of mcf-7 breast cancer cells requires the expression of junction protein zo-1. J Biol Chem, 276, pp. 39892-39897.
42. Mauro, L., Salerno, M., Morelli, C., Boterberg, T., Bracke, M. E. and Surmacz, E. (2003) Role of the IGF-I receptor in the regulation of cell-cell adhesion: Implications in cancer development and progression. J Cell Physiol, 194, pp. 108-116.
43. McRoberts, J. A. and Riley, N. E. (1992) Regulation of T84 cell monolayer permeability by insulin-like growth factors. American Journal of Physiology, 262, pp. C207-C213.
44. Monine, M. I., Berezhkovskii, A. M., Joslin, E. J., Wiley, H. S., Lauffenburger, D. A. and Shvartsman, S. Y. (2005) Ligand accumulation in autocrine cell cultures. Biophys J, 88, pp. 2384-2390.
45. Nguyen, D. A. and Neville, M. C. (1998) Tight junction regulation in the mammary gland. Journal of Mammary Gland Biology and Neoplasia, 3, pp. 233-246.
46. Nugent, M. A. and Edelman, E. R. (1992) Kinetics of basic fibroblast growth factor binding to its receptor and heparan sulfate proteoglycan: a mechanism for cooperactivity. Biochemistry, 31, pp. 8876-8883.
47. Nwariaku, F. E., Liu, Z., Zhu, X., Turnage, R. H., Sarosi, G. A. and Terada, L. S. (2002) Tyrosine phosphorylation of vascular endothelial cadherin and the regulation of microvascular permeability. Surgery, 132, pp. 180-185.
48. Peixoto, E. B. and Collares-Buzato, C. B. (2005) Protamine-induced epithelial barrier disruption involves rearrangement of cytoskeleton and decreased junction-associated protein expression in cultured MDCK strains. Cell Struct. Funct., 29, pp. 165-178.
49. Pennisi, P. A., Barr, V., Nunez, N. P., Stannard, B. and Roith, D Le (2002) Reduced expression of insulin-like growth factor I receptors in MCF-7 breast cancer cells leads to a more metastatic phenotype. Cancer Res, 62, pp. 6529-65237.
50. Playford, M. P., Bicknell, D., Bodmer, W. F. and Macaulay, V. M. (2000) Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of beta-catenin. Proc Natl Acad Sci USA, 97, pp. 12103-12108.
51. Pollak, M. (2000) Insulin-like growth factor physiology and cancer risk. Eur J Cancer, 36, pp. 1224-1228.
52. Re, R. N. (2002) Toward a theory of intracrine hormone action. Regul Pept, 106, pp. 1-6.
53. Reuss, B., Dono, R. and Unsicker, K. (2003) Functions of fibroblast growth factor (FGF)-2 and FGF-5 in astroglial differentiation and blood-brain barrier permeability: Evidence from mouse mutants. J Neurosci, 23, pp. 6404-6412.
54. Romagnolo, D., Akers, R. M., Byatt, J. C., Wong, E. A. and Turner, J. D. (1994) Regulation of expression of IGF-I-induced IGFBP-3 and IGF-I-receptor by constitutive vs regulated expression of recombinant IGF-I in transfected mammary epithelial cells. Endocrine J, 2, pp. 375-384.
55. Sachdev, D. and Yee, D. (2007) Disrupting insulin-like growth factor signaling as a potential cancer therapy. Mol Cancer Ther, 6, pp. 1-12.
56. Sachdev, D., Hartell, J. S., Lee, A. V., Zhang, X. and Yee, D. (2004) A dominant negative type I insulin-like growth factor receptor inhibits metastasis of human cancer cells. J Biol Chem, 279, pp. 5017-5024.
57. Shvartsman, S. Y., Hagan, M. P., Yacoub, A., Dent, P., Wiley, H. S. and Lauffenburger, D. A. (2002) Autocrine loops with positive feedback enable context-dependent cell signaling. Am J Physiol Cell Physiol, 282, pp. C545-C559.
58. Shvartsman, S. Y., Wiley, H. S., Deen, W. M. and Lauffenburger, D. A. (2001) Spatial range of autocrine signaling: Modeling and computational analysis. Biophys J, 81, pp. 1854-1867.
59. Sinaga, E., Jois, S. D., Avery, M., Makagiansar, I. T., Tambunan, U. S., Audus, K. L. and Siahaan, T. J. (2002) Increasing paracellular porosity by E-cadherin peptides: Discovery of bulge and groove regions in the EC1-domain of E-cadherin. Pharm Res, 19, pp. 1170-1179.
60. Soler, A. P., Miller, R. D., Laughlin, K. V., Carp, N. Z., Klurfeld, D. M. and Mullin, J. M. (1999) Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis, 20, pp. 1425-1431.
61. Spoerri, P. E., Afzal, A., Calzi, S Li, Shaw, L. C., Cai, J., Pan, H., Boulton, M. and Grant, M. B. (2006) Effects of VEGFR-1, VEGFR-2, IGF-IR hammerhead ribozymes on glucose-mediated tight junction expression in cultured human retinal endothelial cells. Mol Vis., 12, pp. 32-42.
62. Sporn, M. B. and Roberts, A. B. (1992) Autocrine secretion-10 years later. Ann Intern Med, 117, pp. 408-414.
63. Stachowiak, M. K., Moffett, J., Maher, P., Tucholski, J. and Stachowiak, E. K. (1997) Growth factor regulation of cell growth and proliferation in the nervous system. A new intracrine nuclear mechanism. Mol Neurobiol, 15, pp. 257-283.
64. Stevenson, B. R. and Keon, B. H. (1998) The tight junction: Morphology to molecules. Annu Rev Cell Dev Biol, 14, pp. 89-109.
65. Surmacz, E. (2000) Function of the IGF-I receptor in breast cancer. J Mammary Gland Biol Neoplasia, 5, pp. 95-105.
66. Suzuki, K., Saito, J., Yanai, R., Yamada, N., Chikama, T., Seki, K. and Nishida, T. (2003) Cell-matrix and cell-cell interactions during corneal epithelial wound healing. Prog Retin Eye Res, 22, pp. 113-133.
67. Tan, X. D., Chang, H., Qu, X. W., Caplan, M., Gonzalez-Crussi, F. and Hsueh, W. (2000) Platelet-activating factor increases mucosal permeability in rat intestine via tyrosine phosphorylation of E-cadherin. Brit J Pharmacol, 129, pp. 1522-1529.
68. Toropainen, E., Lipponen, P. and Syrjanen, K. (1995) Expression of insulin-like growth factor I (IGF-I) in female breast cancer as related to established prognostic factors and long-term prognosis. Eur J Cancer, 9, pp. 1443-1448.
69. Van, d er, Ven, L. T., Van Buul-Offers, S. C., Gloudemans, T., Roholl, P. J., Sussenbach, J. S. and Otter, W Den (1997) Histamine-stimulated expression of insulin-like growth factors in human glioma cells. Br J Cancer, 75, pp. 1091-1097.
70. Venkiteswaran, K., Xiao, K., Summers, S., Calkins, C. C., Vincent, P. A., Pumiglia, K. and Kowalczyk, A. P. (2002) Regulation of endothelial barrier function and growth by VE-cadherin, plakoglobin, and beta-catenin. Am J Physiol, 283, pp. C811-C821.
71. Vleminckx, K. and Kemler, R. (1999) Cadherins and tissue formation: integrating adhesion and signaling. Bioessays, 21, pp. 211-220.
72. Ward, C. W., Garrett, T. P., McKern, N. M., Lou, M., Cosgrove, L. J., Sparrow, L. G., Frenkel, M. J., Hoyne, P. A., Elleman, T. C., Adams, T. E., Lovrecz, G. O., Lawrence, L. J. and Tulloch, P. A. (2001) The three dimensional structure of the type I insulin-like growth factor receptor. Mol Pathol, 54, pp. 125-132.
73. West, M. R., Ferguson, D. J., Hart, V. J., Sanjar, S. and Man, Y. (2002) Maintenance of the epithelial barrier in a bronchial epithelial cell line is dependent on functional E-cadherin local to the tight junctions. Cell Commun Adhes, 9, pp. 29-44.
74. Wiley, H. S., Woolf, M. F., Opresko, L. K., Burke, P. M., Will, B., Morgan, J. R. and Lauffenburger, D. A. (1998) Removal of the membrane-anchoring domain of epidermal growth factor leads to intracrine signaling and disruption of mammary epithelial cell organization. J Cell Biol, 143, pp. 1317-1328.
75. Wills, N. K. (1996) Epithelial cell culture. Epithelial Transport: A guide to methods and experimental analysis, pp. 236-255. Chapman & Hall, London
76. Zabner, J., Winter, M. C., Shasby, S., Ries, D. and Shasby, D. M. (2003) Histamine decreases E-cadherin-based adhesion to increase permeability of human airway epithelium. Chest, 123, p. 385S.