Overexpression of protein kinase C-δ increases tight junction permeability in LLC-PK1 epithelia

American Journal of Physiology - Cell Physiology

Volumn 275, Issue 2 44-2, 1998, Pages

  Mullin, James M ^a   Kampherstein, Jennifer A ^a   Laughlin, Kathleen V ^a   Clarkin, Cheryl E K ^a,d   Miller, R Daniel ^a   Szallasi, Zoltan ^b   Kachar, Bechara ^c   Soler, Alejandro Peralta ^a   Rosson, Dan ^a  

^a LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cytoskeleton; Dextran; Freeze fracture; Mannitol; Paracellular; Phorbol ester; Resistance; Transepithelial

Indexed keywords

CALCIUM ION; PHORBOL ESTER; PROTEIN KINASE C; TETRACYCLINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENZYME POLYMORPHISM; FREEZE FRACTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SWINE; TIGHT JUNCTION;

ANIMALIA; SUS SCROFA;

EID: 0031843583     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.1998.275.2.c544     Document Type: Article

References (71)

1. 1 cells. Am. J. Physiol. 270 (Cell Physiol. 39): C332-C340, 1996.
2. Anderson, J. M., and C. M. Van Itallie. Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J. Physiol. 269 (Gastrointest. Liver Physiol. 32): G467-G475, 1995.
3. Assert, R., H. Schatz, and A. Pfeiffer. Upregulation of PKC-δ and downregulation of PKC-α mRNA and protein by a phorbol ester in human T84 cells. FEBS Lett. 388: 195-199, 1996.
4. Bakker, R., and J. A. Groot. Further evidence for the regulation of the tight junction ion selectivity by cAMP in goldfish intestinal mucosa. J. Membr. Biol. 111: 25-35, 1989.
5. Balda, M. S., L. González-Mariscal, R. G. Contreras, M. Macias-Silva, M. E. Torres-Marquez, J. A. García Sáinz, and M. Cereijido. Assembly and sealing of tight junctions: possible participation of G-proteins, phospholipase C, protein kinase C and calmodulin. J. Membr. Biol. 122: 193-202, 1991.
6. Barnard, J. A., R. D. Beauchamp, W. E. Russell, R. N. DuBois, and R. J. Coffey. Epidermal growth factor related peptides and their relevance to gastrointestinal pathophysiology. Gastroenterology 108: 564-580, 1995.
7. Bishop, W. P., and J. T. Wen. Regulation of Caco-2 cell proliferation by basolateral membrane epidermal growth factor receptors. Am. J. Physiol. 267 (Gastrointest. Liver Physiol. 30): G892-G900, 1994.
8. Blumberg, P. M., G. Acs, L. B. Areces, M. G. Kazanietz, N. E. Lewin, and Z. Szallasi. Protein kinase C in signal transduction and carcinogenesis. Prog. Clin. Biol. Res. 387: 3-19, 1994.
9. Bornancin, F., and P. J. Parker. Phosphorylation of threonine-638 critically controls the dephosphorylation and inactivation of protein kinase C-α. Curr. Biol. 6: 1114-1123, 1996.
10. Borner, C., S. N. Guadagno, D. Fabbro, and I. B. Weinstein. Expression of four protein kinase C isoforms in rat fibroblasts. J. Biol. Chem. 267: 12892-12899, 1992.
11. Boutwell, R. K. The function and mechanism of promoters of carcinogenesis. Crit. Rev. Toxicol. 2: 419-443, 1974.
12. Cazaubon, S., F. Bornancin, and P. J. Parker. Threonine-497 is a critical site for permissive activation of protein kinase C-α. Biochem. J. 301: 443-448, 1994.
13. Citi, S. The molecular organization of tight junctions. J. Cell Biol. 121: 485-489, 1993.
14. Craven, P. A., and F. R. DeRubertis. Alterations in protein kinase C in 1,2-dimethylhydrazine induced colonic carcinogenesis. Cancer Res. 52: 2216-2221, 1992.
15. Craven, P.A., and F. R. DeRubertis. Loss of protein kinase C-δ isozyme immunoreactivity in human adenocarcinomas. Dig. Dis. Sci. 39: 481-489, 1994.
16. Davidson, L. A., Y.-H. Jiang, J. N. Derr, H. M. Aukema, J. R. Lupton, and R. S. Chapkin. Protein kinase C isoforms in human and rat colonic mucosa. Arch. Biochem. Biophys. 312: 547-553, 1994.
17. Davies, R. J., R. Joseph, H. Asbun, and M. Sedwitz. Detection of the cancer-prone colon, using transepithelial impedance analysis. Arch. Surg. 124: 480-484, 1989.
18. Denning, M. F., A. A. Dlugosz, M. K. Howett, and S. H. Yuspa. Expression of an oncogenic rasHa gene in murine keratinocytes induces tyrosine phosphorylation and reduced activity of protein kinase C-δ. J. Biol. Chem. 268: 26079-26081, 1993.
19. Diamond, L., T. G. O'Brien, and W. M. Baird. Tumor promoters and the mechanism of tumor promotion. Adv. Cancer Res. 32: 1-63, 1980.
20. Dodane, V., and B. Kachar. Identification of isoforms of G proteins and PKC that colocalize with tight junctions. J. Membr. Biol. 149: 199-209, 1996.
21. Ellis, B., E. E. Schneeberger, and C. A. Rabito. Cellular variability in the development of tight junctions after activation of protein kinase C. Am. J. Physiol. 263 (Renal Fluid Electrolyte Physiol. 32): F293-F300, 1992.
22. Flamion, B., K. R. Spring, and M. Abramow. Adaptation of inner medullary collecting duct to dehydration involves a paracellular pathway. Am. J. Physiol. 268 (Renal Fluid Electrolyte Physiol. 37): F53-F63, 1995.
23. Frizzell, R. A., and S. G. Schultz. Ionic conductances of extracellular shunt pathway in rabbit ileum. J. Gen. Physiol. 59: 318-346, 1972.
24. Gossen, M., and H. Bujard. Tight control of gene expression in mammalian cells by tetracycline responsive promoters. Proc. Natl. Acad. Sci. USA 89: 5547-5551, 1992.
25. Gschwendt, M., K. Kielbassa, W. Kittstein, and F. Marks. Tyrosine phosphorylation and stimulation of protein kinase C-δ from porcine spleen by src in vitro: dependence on the activated state of protein kinase C-δ. FEBS Lett. 347: 85-89, 1994.
26. Haleem-Smith, H., E.-Y. Chang, Z. Szallasi, P. M. Blumberg, and J. Rivera. Tyrosine phosphorylation of protein kinase C-δ in response to the activation of the high-affinity receptor for immunoglobulin E modifies its substrate recognition. Proc. Natl. Acad. Sci. USA 92: 9112-9116, 1995.
27. Hazen-Martin, D. J., M. A. Sens, C. J. Detrisac, J. G. Blackburn, and D. A. Sens. Elevated glucose alters paracellular transport of cultured human proximal tubule cells. Kidney Int. 35: 31-39, 1989.
28. Hecht, G., B. Robinson, and A. Koutsouris. Reversible disassembly of an intestinal epithelial monolayer by prolonged exposure to phorbol ester. Am. J. Physiol. 266 (Gastrointest. Liver Physiol. 29): G214-G221, 1994.
29. Hollander, D. Crohn's disease - a permeability disorder of the tight junction. Gut 29: 1621-1624, 1988.
30. 1. In Vitro 12: 670-677, 1976.
31. Jaeger, M. M., V. Dodane, and B. Kachar. Modulation of tight junction morphology and permeability by an epithelial factor. J. Membr. Biol. 139: 41-48, 1994.
32. Jorgensen, P. E., A.-L. Kamper, O. Munck, S. Strandgaard, and E. Nexo. Urinary excretion of epidermal growth factor in living human kidney donors and their recipients. Eur. J. Clin. Invest. 25: 442-446, 1995.
33. Kahl-Rainer, P., J. Karner-Hanusch, W. Weiss, and B. Marian. Five of six protein kinase C isoenzymes present in normal mucosa show reduced protein levels during tumor development in the human colon. Carcinogenesis 15: 779-782, 1994.
34. Kazanietz, M. G., L. B. Areces, A. Bahador, H. Mischak, J. Goodnight, J. F. Mushinski, and P. M. Blumberg. Characterization of ligand and substrate specificity for the calcium-dependent and calcium-independent protein kinase C isozymes. Mol. Pharmacol. 44: 298-307, 1993.
35. Kiley, S. C., P. J. Parker, D. Fabbro, and S. Jaken. Selective redistribution of protein kinase C isozymes by thapsigargin and staurosporine. Carcinogenesis 13: 1997-2001, 1992.
36. 2+. I. Microscopic and general electrophysiological observations. Pflügers Arch. 425: 528-534, 1993.
37. Kuranami, M., C. T. Powell, H. Hug, Z. Zeng, A. M. Cohen, and J. G. Guillem. Differential expression of protein kinase C isoforms in human colorectal cancers. J. Surg. Res. 58: 233-239, 1995.
38. Lee, H. W., L. Smith, G. R. Pettit, and J. B. Smith. Dephosphorylation of activated protein kinase C contributes to downregulation by bryostatin. Am. J. Physiol. 271 (Cell Physiol. 40): C304-C311, 1996.
39. Lee, H. W., L. Smith, G. R. Pettit, A. Vinitsky, and J. B. Smith. Ubiquitination of protein kinase C-α and degradation by the proteasome. J. Biol. Chem. 271: 20973-20976, 1996.
40. Li, W., H. Mischak, J.-C. Yu, L.-M. Wang, J. F. Mushinski, M. A. Heidaran, and J. H. Pierce. Tyrosine phosphorylation of protein kinase C-δ in response to its activation. J. Biol. Chem. 269: 2349-2352, 1994.
41. Liu, F., and R. A. Roth. Insulin-stimulated tyrosine phosphorylation of protein kinase C-α: evidence for direct interaction of the insulin receptor and protein kinase C in cells. Biochem. Biophys. Res. Commun. 200: 1570-1577, 1994.
42. Liu, J. P. Protein kinase C and its substrates. Mol. Cell. Endocrinol. 116: 1-29, 1996.
43. Lum, H., and A. B. Malik. Regulation of vascular endothelial barrier function. Am. J. Physiol. 267 (Lung Cell. Mol. Physiol. 11): L223-L241, 1994.
44. Madara, J. L., and J. R. Pappenheimer. Structural basis for physiological regulation of paracellular pathways in intestinal epithelia. J. Membr. Biol. 100: 149-164, 1987.
45. 1 transepithelial permeability. Biochem. Biophys. Res. Commun. 209: 669-676, 1995.
46. Martinez-Palomo, A. Ultrastructural modifications of intercellular junctions between tumor cells. In Vitro 6: 15-20, 1970.
47. Mischak, H., J. Goodnight, W. Kolch, G. Martiny-Baron, C. Schaechtle, M. G. Kazanietz, P. M. Blumberg, J. H. Pierce, and J. F. Mushinski. Overexpression of protein kinase C-δ and -ε in NIH/3T3 cells induces opposite effects on growth, morphology, anchorage dependence, and tumorigenicity. J. Biol. Chem. 268: 6090-6096, 1993.
48. Mullin, J. M. Potential interplay between luminal growth factors and increased tight junction permeability in epithelial carcinogenesis. J. Exp. Zool. 279: 484-489, 1997.
49. 1 renal epithelial cells. Biochim. Biophys. Acta 885: 233-239, 1986.
50. Mullin, J. M., J. A. Kampherstein, K. V. Laughlin, D. T. Saladik, and A. P. Soler. Transepithelial paracellular leakiness induced by chronic phorbol ester exposure correlates with polyp-like foci and redistribution of protein kinase C-α. Carcinogenesis 18: 2339-2345, 1997.
51. 1 renal epithelia: similarity to phorbol ester tumor promoters. J. Cell. Physiol. 134: 357-366, 1988.
52. Mullin, J. M., and M. T. McGinn. The phorbol ester, TPA, increases transepithelial epidermal growth factor flux. FEBS Lett. 221: 359-364, 1987.
53. 1 renal epithelial tight junctions and transepithelial fluxes. Am. J. Physiol. 251 (Cell Physiol. 20): C597-C602, 1986.
54. Mullin, J. M., K. V. Snock, R. D. Shurina, J. Noe, K. George, L. Misner, S. Imaizumi, and T. G. O'Brien. Effects of acute vs. chronic phorbol ester exposure on transepithelial permeability and epithelial morphology. J. Cell. Physiol. 152: 35-47, 1992.
55. 1 epithelia to the phorbol ester TPA produces polyp-like foci with leaky tight junctions and altered protein kinase C-α expression and localization. Exp. Cell Res. 227: 12-22, 1996.
56. Nigam, S. K., N. Denisenko, E. Rodriguez-Boulan, and S. Citi. The role of phosphorylation in development of tight junctions in cultured renal epithelial (MDCK) cells. Biochem. Biophys. Res. Commun. 181: 548-553, 1991.
57. Parkos, C. A., S. P. Colgan, C. Delp, M. A. Arnaout, and J. L. Madara. Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways. J. Cell Biol. 117: 757-764, 1992.
58. Playford, R. J., A. M. Hanby, S. Gschmeissner, L. P. Peiffer, N. A. Wright, and T. McGarrity. The epidermal growth factor receptor (EGF-R) is present on the basolateral, but not the apical, surface of enterocytes in the human gastrointestinal tract. Gut 39: 262-266, 1996.
59. 1 epithelial cell line. J. Biol. Chem. 272: 14950-14953, 1997.
60. Saito, T. Ultrastructural changes on the junctional complexes in the human urinary bladder carcinoma by thin sectioning and freeze fracture. J. Clin. Electron Microsc. 17: 201-209, 1984.
61. Saxon, M. L., X. Zhao, and J. D. Black. Activation of protein kinase C isozymes is associated with post-mitotic events in intestinal epithelial cells in situ. J. Cell Biol. 126: 747-763, 1994.
62. Scheving, L. A., R. A. Shiurba, T. D. Nguyen, and G. M. Gray. Epidermal growth factor receptor of the intestinal enterocyte. Localization to laterobasal but not brush border membrane. J. Biol. Chem. 264: 1735-1741, 1989.
63. Schneeberger, E. E., and R. D. Lynch. Structure, function, and regulation of cellular tight junctions. Am. J. Physiol. 262 (Lung Cell. Mol. Physiol. 6): L647-L661, 1992.
64. Stenson, W. F., R. A. Easom, T. E. Riehl, and J. Turk. Regulation of paracellular permeability in Caco-2 cell monolayers by protein kinase C. Am. J. Physiol. 265 (Gastrointest. Liver Physiol. 28): G955-G962, 1993.
65. Stoddard, J. S., and L. Reuss. Voltage and time dependence of apical membrane conductance during current clamp in Necturus gallbladder epithelium. J. Membr. Biol. 103: 191-204, 1988.
66. Szallasi, Z., M. F. Denning, E.-Y. Chang, J. Rivera, S. H. Yuspa, C. Lehel, Z. Olah, W. B. Anderson, and P. M. Blumberg. Development of a rapid approach to identification of tyrosine phosphorylation sites: application to PKC-δ phosphorylated upon activation of the high-affinity receptor for IgE in rat basophilic leukemia cells. Biochem. Biophys. Res. Commun. 214: 888-894, 1995.
67. Traumeni, J. F., R. N. Hoover, S. S. Devesa, and L. J. Kinlen. Epidemiology of cancer. In: Cancer: Principles and Practice of Oncology. Philadelphia, PA: Lippincott, 1989, p. 196-209.
68. Watanabe, T., Y. Ono, Y. Taniyama, K., Hazama, K. Igarashi, K. Ogita, U. Kikkawa, and Y. Nishizuka. Cell division arrest induced by phorbol ester in CHO cells overexpressing protein kinase C-δ subspecies. Proc. Natl. Acad. Sci. USA 89: 10159-10163, 1992.
69. Ways, D. K., C. A. Kukoly, J. DeVente, J. L. Hooker, W. O. Bryant, K. J. Posekany, D. J. Fletcher, P. P. Cook, and P. J. Parker. MCF-7 breast cancer cells transfected with protein kinase C-α exhibit altered expression of other protein kinase C isoforms and display a more aggressive neoplastic phenotype. J. Clin. Invest. 95: 1906-1915, 1995.
70. 2+ transport in the cortical thick ascending limb of Henle's loop of the mouse: evidence for a change in the paracellular pathway permeability. Pflügers Arch. 423: 387-396, 1993.
71. Wright, N. A., C. Pike, and G. Elia. Induction of a novel epidermal growth factor-secreting cell lineage by mucosal ulceration in human gastrointestinal stem cells. Nature 343: 82-85, 1990.