Short-term regulation of murine colonic NBCe1-B (electrogenic Na +/HCO3- cotransporter) membrane expression and activity by protein kinase C

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  May, Oliver ^a   Yu, Haoyang ^a   Riederer, Brigitte ^a   Manns, Michael P ^a   Seidler, Ursula ^a   Bachmann, Oliver ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE SODIUM COTRANSPORTER; NBCE1 B PROTEIN; PROTEIN KINASE C; UNCLASSIFIED DRUG; CHOLINERGIC RECEPTOR STIMULATING AGENT; SLC4A4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELL ISOLATION; CONTROLLED STUDY; CRYPT CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; PH MEASUREMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; PROTON TRANSPORT; ANIMAL; C57BL MOUSE; CELL MEMBRANE; COLON; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; CHOLINERGIC AGONISTS; COLON; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SODIUM-BICARBONATE SYMPORTERS;

EID: 84898622364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092275     Document Type: Article

References (46)

1. Romero MF, Fulton CM, Boron WF (2004) The SLC4 family of HCO 3 - transporters. Pflugers Arch 447: 495-509.
2. Bachmann O, Rossmann H, Berger UV, Colledge WH, Ratcliff R, et al. (2003) cAMP-mediated regulation of murine intestinal/pancreatic Na+/HCO3- cotransporter subtype pNBC1. Am J Phy (Pubitemid 36076248)
3. - cotransporter NBCn1 is a major pHi regulator in murine duodenum. J Physiol.
4. Jacob P, Christiani S, Rossmann H, Lamprecht G, Vieillard-Baron D, et al. (2000) Role of Na+HCO3- Cotransporter NBC1, Na+/H+ Exchanger NHE1, and Carbonic Anhydrase in Rabbit Duodenal Bicarbonate Secretion. Gastroenterology 119: 406-419.
5. Bachmann O, Franke K, Yu H, Riederer B, Li HC, et al. (2008) cAMPdependent and cholinergic regulation of the electrogenic intestinal/pancreatic Na+/HCO3- cotransporter pNBC1 in human embryonic kidney (HEK293) cells. BMC Cell Biol 9: 70.
6. Ruiz OS, Arruda JA (1992) Regulation of the renal Na-HCO3 cotransporter by cAMP and Ca-dependent protein kinases. Am J Physiol 262: F560-565.
7. Ruiz OS, Qiu YY, Cardoso LR, Arruda JA (1997) Regulation of the renal Na- HCO3 cotransporter: VII. Mechanism of the cholinergic stimulation. Kidney Int 51: 1069-1077. (Pubitemid 27186532)
8. Bachmann O, Reichelt D, Tuo B, Manns MP, Seidler U (2006) Carbachol increases Na+-HCO3- cotransport activity in murine colonic crypts in a M3-, Ca2+/calmodulin-, and PKC-dependent manner. Am J Physiol Gastrointest Liver Physiol 291: G650-657.
9. Abuladze N, Lee I, Newman D, Hwang J, Boorer K, et al. (1998) Molecular cloning, chromosomal localization, tissue distribution, and functional expression of the human pancreatic sodium bicarbonate cotransporter. J Biol Chem 273: 17689-17695. (Pubitemid 28355108)
10. Gross E, Fedotoff O, Pushkin A, Abuladze N, Newman D, et al. (2003) Phosphorylation-induced modulation of pNBC1 function: distinct roles for the amino- and carboxy-termini. J Physiol 549: 673-682. (Pubitemid 36889761)
11. Gross E, Kurtz I (2002) Structural determinants and significance of regulation of electrogenic Na(+)2HCO(3)(2) cotransporter stoichiometry. Am J Physiol Renal Physiol 283: F876-887. (Pubitemid 35192453)
12. Glaser S, Alvaro D, Roskams T, Phinizy JL, Stoica G, et al. (2003) Dopaminergic inhibition of secretin-stimulated choleresis by increased PKCgamma expression and decrease of PKA activity. Am J Physiol Gastrointest Liver Physiol 284: G683-694. (Pubitemid 36343218)
13. Orsenigo MN, Tosco M, Baroni MD, Bazzini C, Laforenza U, et al. (2002) Protein kinase C regulation of rat jejunal transport systems: mechanisms involved in bicarbonate absorption. Exp Physiol 87: 299-309. (Pubitemid 34498404)
14. Saksena S, Gill RK, Syed IA, Tyagi S, Alrefai WA, et al. (2002) Inhibition of apical Cl-/OH- exchange activity in Caco-2 cells by phorbol esters is mediated by PKCepsilon. Am J Physiol Cell Physiol 283: C1492-1500. (Pubitemid 35178441)
15. Saksena S, Gill RK, Tyagi S, Alrefai WA, Sarwar Z, et al. (2005) Involvement of c-Src and protein kinase C delta in the inhibition of Cl(-)/OH- exchange activity in Caco-2 cells by serotonin. J Biol Chem 280: 11859-11868. (Pubitemid 40418500)
16. Tuo BG, Chow JY, Barrett KE, Isenberg JI (2004) Protein kinase C potentiates cAMP-stimulated mouse duodenal mucosal bicarbonate secretion in vitro. Am J Physiol Gastrointest Liver Physiol 286: G814-821. (Pubitemid 38506814)
17. Hegyi P, Rakonczay Z Jr, Tiszlavicz L, Varro A, Toth A, et al. (2005) Protein kinase C mediates the inhibitory effect of substance P on HCO3- secretion from guinea pig pancreatic ducts. Am J Physiol Cell Physiol 288: C1030-1041. (Pubitemid 40559379)
18. Odes HS, Reimer R, Muallem R, Schwenk M, Beil W, et al. (1996) Role of protein kinase C in duodenal mucosal bicarbonate secretion in the guinea pig. Pharmacology 53: 60-65. (Pubitemid 26275759)
19. Broughman JR, Sun L, Umar S, Scott J, Sellin JH, et al. (2006) Chronic PKCbeta activation in HT-29 Cl.19a colonocytes prevents cAMP-mediated ion secretion by inhibiting apical membrane current generation. Am J Physiol Gastrointest Liver Physiol 291: G318-330. (Pubitemid 44024692)
20. Qu F, Liu HJ, Xiang Y, Tan YR, Liu C, et al. (2011) Activation of CFTR trafficking and gating by vasoactive intestinal peptide in human bronchial epithelial cells. J Cell Biochem 112: 902-908.
21. Perry C, Baker OJ, Reyland ME, Grichtchenko II (2009) PKC{alpha}{beta}{- gamma}- and PKC{delta}-dependent endocytosis of NBCe1-A and NBCe1-B in salivary parotid acinar cells. Am J Physiol Cell Physiol 297: C1409-1423.
22. Ruiz OS, Wang LJ, Qiu YY, Kear F, Bernardo A, et al. (1996) Regulation of the renal Na-HCO3 cotransporter: VI. Mechanism of the stimulatory effect of protein kinase C. Kidney Int 49: 696-704.
23. Yamada H, Seki G, Taniguchi S, Uwatoko S, Nosaka K, et al. (1996) Roles of Ca2+ and PKC in regulation of acid/base transport in isolated proximal tubules. Am J Physiol 271: F1068-1076.
24. Yu H, Riederer B, Stieger N, Boron WF, Shull GE, et al. (2009) Secretagogue stimulation enhances NBCe1 (electrogenic Na(+)/HCO(3)(2) cotransporter) surface expression in murine colonic crypts. AmJPhysiol GastrointestLiver Physiol 297: G1223-G1231.
25. Espiritu DJ, Yang VL, Bernardo AA, Arruda JA (2004) Regulation of renal Na+/HCO3- cotransporter stimulation by CO2: role of phosphorylation, exocytosis and protein synthesis. J Membr Biol 199: 39-49. (Pubitemid 38766425)
26. Schmitt BM, Biemesderfer D, Romero MF, Boulpaep EL, Boron WF (1999) Immunolocalization of the electrogenic Na+-HCO-3 cotransporter in mammalian and amphibian kidney. Am J Physiol 276: F27-38. (Pubitemid 29061722)
27. Hillesheim J, Riederer B, Tuo B, Chen M, Manns M, et al. (2007) Down regulation of small intestinal ion transport in PDZK1- (CAP70/NHERF3) deficient mice. Pflugers Arch 454: 575-586. (Pubitemid 46872904)
28. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, et al. (1993) Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem 268: 9194-9197. (Pubitemid 23145960)
29. Espiritu DJD, Yang VL, Bernardo AA, Arruda JAL (2004) Regulation of Renal Na+/HCO32 Cotransporter Stimulation by CO2: Role of Phosphorylation, Exocytosis and Protein Synthesis. Journal of Membrane Biology 199: 39-49. (Pubitemid 38766425)
30. Perry C, Quissell D, Reyland M, Grichtchenko II (2008) Electrogenic NBCe1 (SLC4A4) but not electroneutral NBCn1 (SLC4A7) cotransporter undergoes cholinergic-stimulated endocytosis in salivary ParC5 cells. AmJPhysiol Cell Physiol.
31. Song JC, Hrnjez BJ, Farokhzad OC, Matthews JB (1999) PKC-epsilon regulates basolateral endocytosis in human T84 intestinal epithelia: role of F-actin and MARCKS. AmJPhysiol 277: C1239-C1249. (Pubitemid 30045981)
32. Liu J, Kesiry R, Periyasamy SM, Malhotra D, Xie Z, et al. (2004) Ouabain induces endocytosis of plasmalemmal Na/K-ATPase in LLC-PK1 cells by a clathrin-dependent mechanism. Kidney Int 66: 227-241. (Pubitemid 38870098)
33. Perry C, Blaine J, Le H, Grichtchenko II (2006) PMA- and ANG II-induced PKC regulation of the renal Na+-HCO3- cotransporter (hkNBCe1). Am J Physiol Renal Physiol 290: F417-427. (Pubitemid 43724995)
34. Parekh DB, Ziegler W, Parker PJ (2000) Multiple pathways control protein kinase C phosphorylation. EMBO J 19: 496-503. (Pubitemid 30093722)
35. Durgan J, Cameron AJ, Saurin AT, Hanrahan S, Totty N, et al. (2008) The identification and characterization of novel PKCepsilon phosphorylation sites provide evidence for functional cross-talk within the PKC superfamily. Biochem J 411: 319-331. (Pubitemid 351580184)
36. Carriere A, Romeo Y, Acosta-Jaquez HA, Moreau J, Bonneil E, et al. (2011) ERK1/2 phosphorylate Raptor to promote Ras-dependent activation of mTOR complex 1 (mTORC1). J Biol Chem 286: 567-577.
37. Leontieva OV, Black JD (2004) Identification of two distinct pathways of protein kinase Calpha down-regulation in intestinal epithelial cells. J Biol Chem 279: 5788-5801. (Pubitemid 38220610)
38. Kim HW, Ha SH, Lee MN, Huston E, Kim DH, et al. (2010) Cyclic AMP controls mTOR through regulation of the dynamic interaction between Rheb and phosphodiesterase 4D. Mol Cell Biol 30: 5406-5420.
39. Edelstein J, Hao T, Cao Q, Morales L, Rockwell P (2011) Crosstalk between VEGFR2 and muscarinic receptors regulates the mTOR pathway in serum starved SK-N-SH human neuroblastoma cells. Cell Signal 23: 239-248.
40. Del Castillo IC, Fedor-Chaiken M, Song JC, Starlinger V, Yoo J, et al. (2005) Dynamic regulation of Na(+)-K(+)-2Cl(2) cotransporter surface expression by PKC-{epsilon} in Cl(-)-secretory epithelia. Am J Physiol Cell Physiol 289: C1332-1342. (Pubitemid 41456850)
41. Tang J, Bouyer P, Mykoniatis A, Buschmann M, Matlin KS, et al. (2010) Activated PKC{delta} and PKC{epsilon} inhibit epithelial chloride secretion response to cAMP via inducing internalization of the Na+-K+-2Cl2 cotransporter NKCC1. J Biol Chem 285: 34072-34085.
42. Matthews JB, Awtrey CS, Hecht G, Tally KJ, Thompson RS, et al. (1993) Phorbol ester sequentially downregulates cAMP-regulated basolateral and apical Cl- transport pathways in T84 cells. Am J Physiol 265: C1109-1117.
43. Singh AK, Xia W, Riederer B, Juric M, Li J, et al. (2013) Essential role of the electroneutral Na+HCO32 cotransporter NBCn1 in murine duodenal acid/ base balance and colonic mucus layer build-up in vivo. J Physiol.
44. Damkier HH, Nielsen S, Praetorius J (2007) Molecular expression of SLC4- derived Na+-dependent anion transporters in selected human tissues. Am J Physiol Regul Integr Comp Physiol 293: R2136-2146. (Pubitemid 350085692)
45. Alvarez BV, Vilas GL, Casey JR (2005) Metabolon disruption: a mechanism that regulates bicarbonate transport. Embo Journal 24: 2499-2511. (Pubitemid 41076307)
46. Hong JH, Yang D, Shcheynikov N, Ohana E, Shin DM, et al. (2013) Convergence of IRBIT, phosphatidylinositol (4,5) bisphosphate, and WNK/ SPAK kinases in regulation of the Na+-HCO32 cotransporters family. Proc Natl Acad Sci U S A 110: 4105-4110.