ζ isoform of protein kinase C prevents oxidant-induced nuclear factor-κB activation and I-κBα degradation: A fundamental mechanism for epidermal growth factor protection of the microtubule cytoskeleton and intestinal barrier integrity

Journal of Pharmacology and Experimental Therapeutics

Volumn 307, Issue 1, 2003, Pages 53-66

  Banan, A ^a,b   Fields, J Z ^a   Zhang, L J ^a   Shaikh, M ^a   Farhadi, A ^a   Keshavarzian, A ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b RUSH MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL DERIVATIVE; EPIDERMAL GROWTH FACTOR; GLYCEROL 2 ACETATE 1 OLEATE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOENZYME; OXIDIZING AGENT; PROTEIN KINASE C ZETA; PROTEIN P50; SYNAPTOTAGMIN; TUBULIN;

ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; ENTERITIS; ENZYME ACTIVATION; FRACTIONATION; HUMAN; HUMAN CELL; INTESTINE; INTESTINE MUCOSA PERMEABILITY; MICROTUBULE; MOLECULAR CLONING; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ACTIVE TRANSPORT, CELL NUCLEUS; CACO-2 CELLS; CYTOSKELETON; CYTOSOL; EPIDERMAL GROWTH FACTOR; HUMANS; HYDROGEN PEROXIDE; I-KAPPA B PROTEINS; INTESTINES; MICROTUBULES; NF-KAPPA B; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; OXIDANTS; PHOSPHORYLATION; PROTEIN KINASE C; SERINE; TRANSFECTION; TUBULIN;

EID: 0141519513     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.103.053835     Document Type: Article

References (56)

1. Babich M, Foti LR, and Mathias KL (1997) Protein kinase C modulator effects on parathyroid hormone-induced intracellular calcium and morphologic changes in UMR 106-H5 osteoblastic cells. J Cell Biochem 65:276-285.
2. Banan A, Choudhary S, Zhang Y, Fields JZ, and Keshavarzian A (1999) Ethanol-induced barrier dysfunction and its prevention by growth factors in human intestinal monolayers: evidence for oxidative and cytoskeletal mechanisms. J Pharmacol Exp Ther 291:1075-1085.
3. Banan A, Choudhary S, Zhang Y, Fields JZ, and Keshavarzian A (2000a) Role of the microtubule cytoskeleton in protection by epidermal growth factor and transforming growth factor-α against oxidant-induced barrier disruption in a human colonic cell line. Free Radical Biol Med 28:727-738.
4. Banan A, Farhadi A, Fields JZ, Zhang L, Mutlu E, and Keshavarzian A (2003a) Evidence that NF-κB activation is critical in oxidant disruption of the microtubule cytoskeleton and barrier integrity and that its inactivation is essential in protection of the monolayers of intestinal epithelia. J Pharmacol Exp Ther 306:13-28.
5. Banan A, Fields JZ, Farhadi A, Talmage DA, Zhang L, and Keshavarzian A (2002a) Activation of the PKC-delta (δ) isoform is required for oxidant-induced disruption of permeability barrier of intestinal epithelia. J Pharmacol Exp Ther 303:17-28.
6. Banan A, Fields JZ, Talmage DA, Zhang L, Farhadi A, and Keshavarzian A (2002b) The β1 isoform of protein kinase c mediates the protective effects of EGF on the dynamic assembly of the cytoskeleton through normalization of calcium homeostasis in human colonic cells. J Pharmacol Exp Ther 310:852-866.
7. Banan A, Fields JZ, Talmage DA, Zhang Y, and Keshavarzian A (2001a) The β1 isoform of protein kinase c in protection of the microtubules and barrier integrity of intestinal monolayers against oxidant damage. Am J Physiol 281:G833-G847.
8. Banan A, Fields JZ, Talmage DA, Zhang L, and Keshavarzian A (2002c) The Atypical PKC-ζ isoform is required for EGF protection of microtubules and intestinal barrier integrity. Am J Physiol 282:G794-G808.
9. Banan A, Fields JZ, Zhang Y, and Keshavarzian A (2000b) Nitric oxide and its metabolites mediate ethanol-induced microtubule disruption and intestinal barrier dysfunction. J Pharmacol Exp Ther 294:997-1008.
10. Banan A, Fields JZ, Zhang Y, and Keshavarzian A (2001b) Targeted molecular inhibition of phospholipase C-γ prevents EGF-mediated protection of the microtubule cytoskeleton and intestinal epithelial barrier function against oxidant injury. Am J Physiol 281:G412-G423.
11. Banan A, Fields JZ, Zhang Y, and Keshavarzian A (2001c) iNOS upregulation mediates oxidant-induced disruption of F-actin and the permeability barrier of intestinal monolayers. Am J Physiol 280:G1234-G1246.
12. Banan A, Fields JZ, Zhang Y, and Keshavarzian A (2001d) Key role of general protein kinase C activation in EGF-induced protection of the microtubule cytoskeleton and intestinal epithelial barrier against oxidant injury. Am J Physiol 280: G828-G843.
13. Banan A, McCormack SA, and Johnson LR (1998a) Polyamines are required for microtubule formation during mucosal ulcer healing. Am J Physiol 274:G879-G885.
14. Banan A, Shaikh M, Fields JZ, Farhadi A, Mutlu E, and Keshavarzian A (2003b) Upregulation of NF-κB and I-κBα phosphorylation and consequent cytoskeletal dysfunction in colonic mucosa of patients with inflammatory bowel disease (IBD) (Abstract). Gastroenterology, in press.
15. Banan A, Smith GS, Rickenberg C, Kokoska ER, and Miller TA (1998b) Protection against ethanol injury by prostaglandins in a human intestinal cell line: role of microtubules. Am J Physiol 274:G111-G121.
16. Banan A, Wang J-Y, McCormack SA, and Johnson LR (1996) Relationship between polyamines, cytoskeletal distribution and gastric mucosal ulcer healing in rats. Am J Physiol 34:G893-G903.
17. Banan A, Zhang Y, Hutte R, and Keshavarzian A (2000c) Increased oxidation injury in intestinal mucosa of patients with inflammatory bowel disease (Abstract). Gastroenterology 118:4266.
18. Banan A, Zhang Y, Losurdo J, and Keshavarzian A (2000d) Carbonylation and disassembly of the F-actin in oxidant-induced barrier dysfunction and its prevention by epidermal growth factor and transforming growth factor-α in a human intestinal cell line. Gut 46:830-837.
19. Baeuerle PA and Henkle T (1994) Function and activation of NF-κB in immune system. Annu Rev Immunol 12:141-179.
20. Barnes PJ and Karin M (1997) Nuclear factor-κB, a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 336:1066-1071.
21. Bradford MA (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye binding. Anal Biochem 72:224-254.
22. Chang Q and Tepperman BL (2001) The role of protein kinase C isozymes in TNF-alpha-induced cytotoxicity to a rat intestinal epithelial cell line. Am J Physiol 280:G572-G583.
23. Cho Y, Klein MG, and Talmage DA (1998) Distinct functions of protein kinase C-alpha and protein kinase C-beta during retinoic acid-induced differentiation of F9 cells. Cell Growth Differ 9:147-154.
24. Gilbert T, Le Bivic A, Quaroni A, and Rodreguez-Boulan E (1991) Microtubule organization and its involvement in the biogenic pathways of plasma membrane proteins in Caco-2 Intestinal epithelial cells. J Cell Biol 133:275-288.
25. Goodnight J, Mischak H, Kolch W, and Mushinski JF (1995) Immunocytochemical localization of eight PKC isoenzymes over-expressed in NIH 3T3 fibroblasts. J Biol Chem 270:9991-10001.
26. Gopalakrishna R and Jaken S (2000) Protein kinase C signaling and oxidative stress. Free Radical Biol Med 28:1349-1361.
27. Harter JL (1960) Critical values for Dunnett's new multiple range test. Biometrics 16:671-685.
28. Hermiston ML and Gordon JI (1995) Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science (Wash DC) 270:1203-1207.
29. Hollander D (1992) The intestinal permeability barrier: a hypothesis as to its regulation and involvement in Crohn's disease. Scand J Gastroenterol 27:721-726.
30. Hollander D (1998) Crohn's disease-a permeability disorder of the tight junction? Gut 26:1621-1624.
31. Housey GM, Johnson MD, Hsiao WLW, O'Brian CA, Murphy JP, Kirschmeier P, and Weinstein IB (1998) Overproduction of protein kinase C causes disordered growth control in rat fibroblasts. Cell 52:343-354.
32. Jobin C, Bradham CA, Russo MP, Juma B, Narula AS, Brenner DA, and Sartor B (1999) Curcumin blocks cytokine-mediated NF-κB activation and proinflammatory gene expression by inhibiting inhibitory factor I-κB kinase activity. J Immunol 163:3474-3483.
33. Kennedy M, Denenberg AG, Szabo C, and Salzman AL (1998) Poly (ADP-ribose) synthetase activation mediates increased permeability induced by peroxynitrite in Caco-2BBe cells. Gastroenterology 114:510-518.
34. Keshavarzian A, Banan A, Kommandori S, Zhang Y, and Fields JZ (2003) Increased colonic free radicals and oxidative injury to key cytoskeletal proteins in inflammatory bowel disease. Gut 52:720-728.
35. Keshavarzian A, Holmes EW, Patel M, Iber F, and Pethkar S (1999) Leaky gut in alcoholic cirrhosis: a possible mechanism for alcohol induced liver damage. Am J Gastroenterol 94:200-207.
36. Keshavarzian A, Sedghi S, Kanofsky J, List T, Robinson C, Ibrahim C, and Winship D (1992) Excessive production of reactive oxygen metabolites by inflamed colon: analysis by chemiluminescence probe. Gastroenterology 103:177-185.
37. Kimura H, Hokari R, Miura S, Shigematsu T, Hirokawa M, Akiba Y, Kurose I, Higuchi H, Fujimori H, Tsuzuki Y, et al. (1998) Increased expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in colonic mucosa of patients with active ulcerative colitis. Gut 42:180-187.
38. Maruvada P and Levine AE (1999) Increased transforming growth factor-alpha levels in human colon carcinoma cell lines over-expressing protein kinase C. Int J Cancer 80:72-77.
39. McKenizie SJ, Baker MS, Buffington GD, and Doe WF (1996) Evidence for Oxidant-induced injury to epithelial cells during inflammatory bowel disease. J Clin Investig 98:136-141.
40. McKenna JP, Williams JM, and Hanson PJ (1995) The alpha isoform of protein kinase C inhibits histamine-stimulated adenylate cyclase activity in a particulate fraction of the human gastric cancer cell line HGT-1. Inflamm Res 44:66-69.
41. Melloni E, Pontremoli S, Sparatore B, Patrone M, Grossi F, Marks PA, and Rifkind RA (1990) Introduction of the β isozyme of protein kinase C accelerates induced differentiation of murine erythroleukemia cells. Proc Natl Acad Sci USA 87:4417-4420.
42. Menon SD, Qin S, Guy RG, and Tan YH (1993) Differential Induction of Nuclear NF-κB protein phosphatase inhibitors in primary and transformed human cells. J Biol Chem 268:26805-26812.
43. Meunier VM, Bourrie Y, Berger Y, and Fabre G (1995) The human intestinal epithelial cell line Caco-2: pharmacological and pharmacokinetics applications. Cell Biol Toxicol 11:187-194.
44. Mischak H, Goodnight J, Kolch W, Martiny-Baron G, Schaechtle C, Kazanietz MG, Blumberg PM, Pierce JH, and Mushinski JF (1993) Protein kinase C-α and -β in NIH 3T3 cells induce opposite effects on growth morphology, anchorage dependence and tumorigenicity. J Biol Chem 268:6090-6096.
45. Moon RM, Parikh AA, Pritts TA, Fischer JE, Cottongim S, Szabo C, Salzman AL, and Hasselgren PO (1999) Complement component C3 production in IL-1 beta-stimulated human intestinal epithelial cells is blocked by NF-κB inhibitors and by transfection with Ser 32/36 mutant I kappa B alpha. J Surg Res 82:48-55.
46. Mullin JM, Kampherstein JA, Laughlin KV, Clarkin CE, Miller RD, Szallasi Z, Kachar B, Soler AP, and Rosson D (1998) Protein kinase C-delta increases tight junction permeability in LLC-PK1 cells. Am J Physiol 275:C544-C554.
47. Neurath MF, Pettersson S, Buscheneedle KMZ, and Strober W (1999) Local Administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-κB abrogates established experimental colitis in mice. Nat Med 9:998-1004.
48. Persons DA, Wilkison WO, Bell RM, and Finn O (1988) Altered growth regulation and enhanced tumorigenicity of NIH 3T3 fibroblasts by protein kinase C. Cell 52:447-458.
49. Ponzoni M, Lacarelli E, Corrias MV, and Cornaglia-Ferraris P (1993) Protein kinase C isoenzymes in human neuroblasts: involvement of PKC-α in cell differentiation. FEBS Lett 322:120-124.
50. Renard P, Ernest I, Houbion A, Art M, Le Calvez H, Raes M, and Remacle J (2001) Development of a sensitive multi-well colorimetric assay for active NF-κB. Nucleic Acid Res 29:1-5.
51. Rogler G, Brand K, Vogl D, Page S, Hofmeister R, Andus T, Knuechel R, Baeuerle PA, Scholrerich J, and Gross V (1998) Nuclear factor κB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 115:357-369.
52. Sanders SE, Madara JL, Mcgurick DK, Gelman DS, and Colgan SP (1995) Assessment of inflammatory events in epithelial permeability: a rapid screening method using fluorescein dextrans. Epithelial Cell Biol 4:25-34.
53. Schreiber S, Nikolaus S, and Hampe J (1998) Activation of nuclear factor κB in inflammatory bowel disease. Gut 42:477-484.
54. Tang G and Leppla SH (1999) Proteasome activity is required for anthrax lethal toxin to kill macrophages. Infect Immun 67:3055-3060.
55. Wang L, Wilson EJ, Osburn J, and DelValle J (1996) Epidermal growth factor inhibits carbachol stimulated canine parietal cell function via protein kinase C. Gastroenterology 110:469-477.
56. Yamada T, Sarto RB, Marshall S, Special RD, and Grisham MB (1993) Mucosal injury and inflammation in a model of chronic granulomatous colitis in rats. Gastroenterology 104:759-771.