Protein kinase C activation downregulates the expression and function of the basolateral Na+/K+/2Cl- cotransporter

Journal of Cellular Physiology

Volumn 181, Issue 3, 1999, Pages 489-498

  Farokhzad, Omid C ^a   Vivek Sagar, G D ^a   Mun, Edward C ^a   Sicklick, Jason K ^a   Lotz, Margaret ^a   Smith, Jeremy A ^a   Song, Jaekyung C ^a   O'brien, Timothy C ^a   Pal Sharma, C ^b,c   Bernard Kinane, T ^b   Hodin, Richard A ^a   Matthews, Jeffrey B ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN KINASE C;

ARTICLE; CHLORIDE TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME REGULATION; HUMAN; HUMAN CELL; POTASSIUM TRANSPORT; PRIORITY JOURNAL; RNA ANALYSIS; SODIUM TRANSPORT;

CARRIER PROTEINS; CELL DIVISION; CELL LINE; DOWN-REGULATION; ENZYME ACTIVATION; HUMANS; PROTEIN KINASE C; RNA, MESSENGER; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; TETRADECANOYLPHORBOL ACETATE;

EID: 0032741026     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199912)181:3<489::AID-JCP13>3.3.CO;2-Z     Document Type: Article

References (54)

1. Assert R, Schatz H, Pfeiffer A. 1996. Upregulation of PKC d- and downregulation of PKC a-mRNA and protein by a phorbol ester in human T84 cells. FEBS Lett 388:195-199.
2. Bargon J, Loitsch S, Dauletbaev N, von Mallinckrodt C, Buhl R. 1998. Modulation of cystic fibrosis transmembrane conductance regulator gene-expression by elevation of intracellular cyclic AMP. Eur J Med Res 3:256-262.
3. Beron J, Forster I, Beguin P, Geering K, Verrey F. 1997. Phorbol 12-myristate 13-acetate down-regulates Na,K-ATPase independent of its protein kinase C site: decrease in basolateral cell surface area. Mol Biol Cell 8:387-398.
4. Caloca MJ, Fernandez N, Lewin NE, Ching D, Modali R, Blumberg PM, Kazanietz MG. 1997. b2-chimaerin is a high affinity receptor for the phorbol ester tumor promoters. J Biol Chem 272:26488- 26496.
5. Castagna M, Takai Y, Kaibuchi K, Sano K, Kikkawa U, Nishizuka Y. 1982. Direct activation of calcium-activated, phospholipid dependent protein kinase by tumor-promoting phorbol ester. J Biol Chem 257:7847-7851.
6. D'Andrea LC, Lytle C, Matthews JB, Hofman P, Forbush B III, Madara JL. 1996. Na/K/2Cl cotransporter protein of intestinal epithelial cells: surface distribution, immunoprecipitation as a protein complex and surface expression in response to cAMP. J Biol Chem 271:28969-28976.
7. Davidson LA, Jiang YH, Derr JN, Aukema HM, Lupton JR, Chapkin RS. 1994. Protein kinase C isoforms in human and rat colonic mucosa. Arch Biochem Biophys 312:547-553.
8. Doi S, Goldstein D, Hug H, Weinstein IB. 1994. Expression of multiple isoforms of protein kinase C in normal human colon mucosa and colon tumors and decreased levels of protein kinase Cb and h mRNAs in the tumors. Mol Carcinog 11:197-203.
9. Downey GP, Chan CK, Lea P, Takai A, Grinstein S. 1992. Phorbol ester-induced actin assembly in neutrophils: role of protein kinase C. J Cell Biol 116:695-706.
10. Farokhzad OC, Mun EC, Sicklick JK, Smith JA, Matthews JB. 1998. Effects of bryostatin 1, a novel anti-cancer agent, on intestinal transport and barrier function: role of protein kinase C. Surgery 124:380-387.
11. Fuller CM, Benos DJ. 1992. CFTR! Am J Physiol 263:C267-286.
12. Gamba G, Miyanoshita A, Lombardi M, Lytton J, Lee W-S, Hediger MA, Hebert SC. 1994. Molecular cloning, primary structure, and characterization of two members of the mammalian electroneutral sodium-(potassium)-chloride cotransporter family expressed in kidney. Proc Acad Natl Sci USA 269:17713-17722.
13. Haas M, Schmidt WF III, McManus TJ. 1982. Catecholamine-stimulated ion transport in duck red cells. Gradient effects in electrically neutral [Na1K12Cl] co-transport. J Gen Physiol 80:125-147.
14. Haas M. 1994. The Na-K-Cl cotransporters. Am J Physiol 267:C869- 885.
15. Haas M, McBrayer D, Lytle C. 1995. [Cl2]i-dependent phosphorylation of the Na-K-Cl cotransport protein of dog tracheal epithelial cells. J Biol Chem 270:28955-28961.
16. Halm DR, Frizzell RA. 1990. Intestinal chloride secretion. In: Lebenthal E, Duffey ME, editors. Textbook of secretory diarrhea. New York: Raven Press, p 47-58.
17. Hecht G, Robinson B, Koutsouris A. 1994. Reversible disassembly of an intestinal epithelial monolayer by prolonged exposure to phorbol ester. Am J Physiol 266:G214-221.
18. Hong DH, Forstner JF, Forstner GG. 1997. Protein kinase C-e is the likely mediator of mucin exocytosis in human colonic cell lines. Am J Physiol 272:G31-37.
19. Isenring P, Forbush B III. 1997. Ion and bumetanide binding by the Na-K-Cl cotransporter. Importance of transmembrane domains. J Biol Chem 272:24556-24562.
20. Isenring P, Jacoby SC, Payne JA, Forbush B III. 1998a. Comparison of Na-K-Cl cotransporters. NKCC1, NKCC2, and the HEK cell Na-K-Cl cotransporter. J Biol Chem 273:11295-11301.
21. Isenring P, Jacoby SC, Forbush B III. 1998b. The role of transmembrane domain 2 in cation transport by the Na-K-Cl cotransporter. Proc Natl Acad Sci USA 95:7179-7184.
22. Jia Y, Mathews CJ, Hanrahan JW. 1997. Phosphorylation by protein kinase C is required for acute activation of cystic fibrosis conductance regulator by protein kinase A. J Biol Chem 272:4978-4984.
23. Kachintorn U, Vongkovit P, Vajanaphanich M, Dinh S, Barrett KE, Dharmsathaphorn K. 1992. Dual effects of a phorbol ester on calcium- dependent chloride secretion by T84 epithelial cells. Am J Physiol 262:C15-22.
24. Kahl-Rainer P, Karner-Hanusch J, Weiss W, Marian B. 1994. Five of six protein kinase C isozymes present in normal mucosa show reduced protein levels during tumor development in the human colon. Carcinogenesis 15:779-782.
25. Liedtke CM, Thomas L. 1996. Phorbol ester and okadaic acid regulation of Na-2Cl-K cotransport in rabbit tracheal epithelial cells. Am J Physiol 271:C338-346.
26. Liedtke CM, Cole T. 1997. Antisense oligonucleotide to PKC-delta blocks alpha-1 adrenergic activation of Na-K-2Cl cotransport. Am J Physiol 273:C1632-1640.
27. Lytle C, Forbush B III. 1992. The Na-K-Cl cotransport protein of shark rectal gland: regulation by direct phosphorylation. J Biol Chem 267:25438-25443.
28. Lytle C, Xu J-C, Biemesderfer D, Forbush B III. 1995. Distribution and diversity of Na-K-Cl cotransport proteins: a study with monoclonal antibodies. Am J Physiol 269:C1496-C1505.
29. Mosior M, Newton AC. 1995. Mechanism of interaction of protein kinase C with phorbol esters. Reversibility and nature of membrane association. J Biol Chem 270:25526-25533.
30. Matthews JB, Awtrey CS, Madara JL. 1992. Microfilament-dependent activation of Na1/K1/2Cl2 cotransport by cAMP in intestinal epithelial monolayers. J Clin Invest 90:1608-1613.
31. Matthews JB, Awtrey CS, Hecht G, Tally KJ, Thompson RS, Mardara JL. 1993. Phorbol ester sequentially downregulates cAMP-regulated basolateral and apical Cl2 transport pathways in T84 cells. Am J Physiol 265:C1109-1117.
32. Matthews JB, Smith JA, Tally KJ, Awtrey CS, Nguyen H, Rich J, Madara JL. 1994. Na-K-2Cl cotransport in intestinal epithelial cells. Influence of chloride efflux and F-actin on regulation of cotransporter activity and bumetanide binding. J Biol Chem 269: 15703-15709.
33. Matthews JB, Smith JA, Nguyen H. 1995. Modulation of intestinal chloride secretion at basolateral transport sites: opposing effects of cyclic adenosine monophosphate and phorbol ester. Surgery 118: 147-153.
34. Matthews JB, Hassan I, Meng S, Archer SY, Hrnjez BJ, Hodin RA. 1998. Na-K-2Cl cotransporter gene expression and function during enterocyte differentiation. J Clin Invest 101:2072-2079.
35. Newton AC. 1995. Protein kinase C: structure, function, and regulation. J Biol Chem 270:28495-28498.
36. O'Grady SM, Palfrey HC, Field M. 1987. Characteristics and function of Na-K-Cl cotransport in epithelial tissues. Am J Physiol 253: C177-192.
37. Payne JA, Xu J-C, Haas M, Lytle C, Ward D, Forbush B III. 1995. Primary structure, functional expression, and chromosomal localization of the bumetanide-sensitive Na-K-Cl cotransporter in human colon. J Biol Chem 270:17977-17985.
38. Perletti GP, Folini M, Lin HC, Mischak H, Piccinini F, Tashjian H Jr. 1996. Overexpression of protein kinase C epsilon is oncogenic in rat colonic epithelial cells. Oncogene 12:847-854.
39. Perletti GP, Concari P, Brusaferri S, Marras E, Piccinini F, Tashjian AH Jr. 1998. Protein kinase Ce is oncogenic in colon epithelial cells by interaction with the ras signal transduction pathway. Oncogene 16:3345-3348.
40. Perletti GP, Marras E, Concari P, Piccinini F, Tashjian AH Jr. 1999. PKC delta acts as a growth and tumor suppressor in rat colonic epithelial cells. Oncogene 18:1251-1256.
41. Pewitt EB, Hegde RS, Haas M, Palfrey HC. 1990. The regulation of Na/K/2Cl cotransport and bumetanide binding in avian erythrocytes by protein phosphorylation and dephosphorylation: effects of kinase inhibitors and okadaic acid. J Biol Chem 265:20747-20756.
42. Plotkin MD, Snyder EY, Hebert SC, Delpire E. 1997. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J. Neurobiol 33:781-795.
43. Randall J, Thorne T, Delpire E. 1997. Partial cloning and characterization of Slc12a2: the gene encoding the secretory Na1-K1-2Cl2 cotransporter. Am J Physiol 273:C1267-C1277.
44. Reenstra W. 1993. Inhibition of cAMP- and Ca-dependent Cl2 secretion by phorbol esters: inhibition of basolateral K1 channels. Am J Physiol 264:C161-168.
45. Schonhorn JE, Akompong T, Wessling-Resnick M. 1995. Mechanism of transferrin receptor down-regulation in K562 cells in response to protein kinase C activation. J Biol Chem 270:3698-3705.
46. Song JC, Hrnjez BJ, Farokhzad OC, Matthews JB. 1999. Protein Kinase Ce selectively regulates basolateral membrane endocytosis in polarized human epithelia: role of F-actin and MARCKS. Am J Physiol (Cell). In press.
47. Topper TN, Wasserman SM, Anderson KR, Cai J, Falb D, Gimbrone MA Jr. 1997. Expression of the bumetanide-sensitive Na-K-Cl cotransporter BSC2 is differentially regulated by fluid mechanical and inflammatory cytokine stimuli in vascular endothelium. J Clin Invest 99:2941-2949.
48. Trapnell BC, Zeitlin PL, Chu C-S, Yoshimura K, Nakamura H, Guggino WB, Bargon J, Banks TC, Dalemans W, Pavirani A, Lecocq J-P, Crystal RC. 1991. Down-regulation of cystic fibrosis gene mRNA transcript levels and induction of the cystic fibrosis phenotype in epithelial cells by phorbol ester. J Biol Chem 266:10319-10323.
49. Traynor-Kaplan AE, Buranawuti T, Vajanaphanich M, Barrett KE. 1994. Protein kinase C activity does not mediate the inhibitory effect of carbachol on chloride secretion by T84cells. Am J Physiol 267:C1224-1230.
50. Vaandrager AB, van den Berghe N, Bot AGM, Jonge HR. 1992. Phorbol esters stimulate and inhibit Cl2 secretion by different mechanisms in a colonic cell line. Am J Physiol 262:G249-256
51. Verstovsek G, Byrd A, Frey MR, Petrelli NJ, Black JD. 1998. Colonocyte differentiation is associated with increased expression and altered distribution of protein kinase C isozymes. Gastroenterology 115:75-85.
52. Whorwood CB, Stewart PM. 1995. Transcriptional regulation of Na/ K-ATPase by corticosteroids, glycyrrhetinic acid and second messenger pathways in rat kidney epithelial cells. J Mol Endocrinol 15:93-103.
53. Wu MS, Bens M, Cluzeaud F, van Dewalle A. 1994. Role of F-actin in the activation of Na1-K1-2Cl2 cotransport by forskolin and vasopressin in mouse kidney cultured thick ascending limb cells. J Membrane Biol 142:323-326.
54. Xu J-C, Lytle C, Zhu TT, Payne JA, Benz E Jr, Forbush B III. 1994. Molecular cloning and functional expression of the bumetanidesensitive Na-K-Cl cotransporter. Proc Natl Acad Sci 91:2201- 2205.