Regulation of intestinal electroneutral sodium absorption and the brush border Na+H+ exchanger by intracellular calcium

Annals of the New York Academy of Sciences

Volumn 1165, Issue , 2009, Pages 240-248

  Zachos, Nicholas C ^a   Kovbasnjuk, Olga ^a   Donowitz, Mark ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Intracellular calcium; NHE3; NHERF

Indexed keywords

PDZ PROTEIN; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 3; SODIUM PROTON EXCHANGE REGULATORY FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BRUSH BORDER; CALCIUM CELL LEVEL; CALCIUM SIGNALING; DIARRHEA; ENDOCYTOSIS; INTESTINE EPITHELIUM CELL; PDZ DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SMALL INTESTINE; SODIUM ABSORPTION;

EID: 67249086093     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2009.04055.x     Document Type: Article

References (75)

1. Zachos, N.C.,M. Tse&M. Donowitz. 2005. Molecular physiology of intestinal Na+/H+ exchange. Annu. Rev. Physiol. 67: 411-443.
2. Maher, M.M. et al. 1997. The Na+/H+ exchange isoform NHE3 regulates basal canine ileal Na+ absorption in vivo. Gastroenterology 112: 174-183.
3. Maher, M.M. et al. 1996. Role of brush border Na+/H+ exchange in canine ileal absorption. Dig. Dis. Sci. 41: 651-659.
4. Donowitz, M. & C.M. Tse. 2001. Molecular physiology of mammalian epithelial Na/H exchangers NHE2 and NHE3. Curr. Topics Membr. 50: 437-498.
5. Donowitz, M. & M.J. Welsh. 1986. Ca2+ and cyclic AMP in regulation of intestinal Na, K, and Cl transport. Annu. Rev. Physiol. 48: 135-150.
6. Kachintorn, U. et al. 1993. Activation by calcium alone of chloride secretion in T84 epithelial cells. Br. J. Pharmacol. 109: 510-517.
7. Keely, S.J., J.M. Uribe & K.E. Barrett. 1998. Carbachol stimulates transactivation of epidermal growth factor receptor and mitogen-activated protein kinase in T84 cells. Implications for carbachol-stimulated chloride secretion. J. Biol. Chem. 273: 27111-27117.
8. Uribe, J.M. et al. 1996. Epidermal growth factor inhibits Ca(2+)-dependent Cl- transport in T84 human colonic epithelial cells. Am. J. Physiol. 271: C914-C922.
9. Uribe, J.M. et al. 1996. Phosphatidylinositol 3-kinase mediates the inhibitory effect of epidermal growth factor on calcium-dependent chloride secretion. J. Biol. Chem. 271: 26588-26595.
10. Kim, H.K. et al. 1991. PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254. Cell 65: 435-441.
11. Ronnstrand, L. et al. 1992. Identification of two C-terminal autophosphorylation sites in the PDGF beta-receptor: involvement in the interaction with phospholipase C-gamma. Embo. J. 11: 3911-3919.
12. Rotin, D. et al. 1992. SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma. Embo. J. 11: 559-567.
13. Wahl, M. & G. Carpenter. 1991. Selective phospholipase C activation. Bioessays 13: 107-113.
14. Caraveo, G. et al. 2006. Action of TFII-I outside the nucleus as an inhibitor of agonist-induced calcium entry. Science 314: 122-125.
15. Choi, J.H. et al. 2004. Phospholipase C-gamma1 is a guanine nucleotide exchange factor for dynamin-1 and enhances dynamin-1-dependent epidermal growth factor receptor endocytosis. J. Cell Sci. 117: 3785-3795.
16. Clapham, D.E. 2003. TRP channels as cellular sensors. Nature 426: 517-524.
17. Patterson, R.L. et al. 2005. Phospholipase C-gamma: diverse roles in receptor-mediated calcium signaling. Trends Biochem. Sci. 30: 688-697.
18. van Rossum, D.B. et al. 2005. Phospholipase Cgamma1 controls surface expression of TRPC3 through an intermolecular PH domain. Nature 434: 99-104.
19. Dolmetsch, R.E. et al. 1997. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855-858.
20. Hook, S.S. & A.R. Means. 2001. Ca(2+)/CaM-dependent kinases: from activation to function. Annu. Rev. Pharmacol. Toxicol. 41: 471-505.
21. Meyer, T. & L. Stryer. 1991. Calcium spiking. Annu. Rev. Biophys. Biophys. Chem. 20: 153-174.
22. Soderling, T.R. 1999. The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem. Sci. 24: 232-236.
23. Soderling, T.R. & J.T. Stull. 2001. Structure and regulation of calcium/calmodulin-dependent protein kinases. Chem. Rev. 101: 2341-2352.
24. Murakami, M. & I. Kudo. 2002. Phospholipase A2. J. Biochem. 131: 285-292.
25. Balboa, M.A. et al. 2002. Expression and function of phospholipase A(2) in brain. FEBS Lett. 531: 12-17.
26. Evans, J.H. et al. 2001. Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J. Biol. Chem. 276: 30150-30160.
27. Gijon, M.A. et al. 1999. Role of phosphorylation sites and the C2 domain in regulation of cytosolic phospholipase A2. J. Cell Biol. 145: 1219-1232.
28. Dickinson, K.E., R.A. Frizzell & M.C. Sekar. 1992. Activation of T84 cell chloride channels by carbachol involves a phosphoinositide-coupled muscarinic M3 receptor. Eur. J. Pharmacol. 225: 291-298.
29. Kasai, H. & G.J. Augustine. 1990. Cytosolic Ca2+ gradients triggering unidirectional fluid secretion from exocrine pancreas. Nature 348: 735-738.
30. Nathanson, M.H. et al. 1992. Mechanism of Ca2+ wave propagation in pancreatic acinar cells. J. Biol. Chem. 267: 18118-18121.
31. Thorn, P. et al. 1993. Ca2+ oscillations in pancreatic acinar cells: spatiotemporal relationships and functional implications. Cell Calcium 14: 746-757.
32. Kasai, H., Y.X. Li & Y. Miyashita. 1993. Subcellular distribution of Ca2 +release channels underlying Ca2+ waves and oscillations in exocrine pancreas. Cell 74: 669-677.
33. Nathanson, M.H. et al. 1994. Localization of the type 3 inositol 1,4,5-trisphosphate receptor in the Ca2+ wave trigger zone of pancreatic acinar cells. J. Biol. Chem. 269: 4693-4696.
34. Siefjediers, A. et al. 2007. Characterization of inositol 1,4,5-trisphosphate (IP3) receptor subtypes at rat colonic epithelium. Cell Calcium 41: 303-315.
35. Cohen, M.E. et al. 1991. Carbachol- and elevated Ca(2+)-induced translocation of functionally active protein kinase C to the brush border of rabbit ileal Na+ absorbing cells. J. Clin. Invest. 88: 855-863.
36. Emmer, E. et al. 1989. Role of calcium and calmod-ulin in the regulation of the rabbit ileal brush-border membrane Na+/H+ antiporter. J. Membr. Biol. 108: 207-215.
37. Khurana, S. et al. 1996. Asymmetric signal transduction in polarized ileal Na(+)-absorbing cells: carbachol activates brush-border but not basolateral-membrane PIP2-PLC and translocates PLC-gamma 1 only to the brush border. Biochem. J. 313(Pt 2): 509-518.
38. 2+/calmodulin and protein kinase C. J. Clin. Invest. 83: 1953-1962.
39. Morris, A.P. & M.K. Estes. 2001. Microbes and microbial toxins: paradigms for microbial-mucosal interactions. VIII. Pathological consequences of rotavirus infection and its enterotoxin. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G303-G310.
40. Khurana, S. et al. 1991. Studies on the mechanism of Salmonella typhimurium enterotoxin-induced diarrhoea. Biochim. Biophys. Acta 1097: 171-176.
41. Kanwar, R.K. et al. 1995. Calcium and protein kinase C play an important role in Campylobacter jejuni-induced changes in Na+ and Cl- transport in rat ileum in vitro. Biochim. Biophys. Acta 1270: 179-192.
42. Kaur, T. et al. 1995. Role of enteric nervous system in Shigella dysenteriae type 1 toxin-induced fluid secretion in rabbit ileum. J. Diarrhoeal Dis. Res. 13: 159-165.
43. Sullivan, S. et al. 2009. Downregulation of sodium transporters and NHERF proteins in IBD patients and mouse colitis models: potential contributors to IBD-associated diarrhea. Inflamm. Bowel Dis. 15: 261-274.
44. Khan, I. et al. 2003. Role of Na+/H +exchanger isoform-1 in human inflammatory bowel disease. Can. J. Gastroenterol. 17: 31-36.
45. Goyal, J. et al. 1989. Role of Ca2(+)-calmodulin and protein kinase C in the secretory action of heat-labile enterotoxin of Escherichia coli in mice. Biochem. Int. 19: 1007-1017.
46. Kim, J.H. et al. 2002. Ca(2+)-dependent inhibition of Na+/H+ exchanger 3 (NHE3) requires an NHE3-E3KARP-alpha-actinin-4 complex for oligomerization and endocytosis. J. Biol. Chem. 277: 23714-23724.
47. i. DDW 130: A332.
48. Akhter, S. et al. 2000. C-terminal domains of Na(+)/H(+) exchanger isoform 3 are involved in the basal and serum-stimulated membrane trafficking of the exchanger. Biochemistry 39: 1990-2000.
49. D'Souza, S. et al. 1998. The epithelial sodiumhydrogen antiporter Na+/H+ exchanger 3 accumulates and is functional in recycling endosomes. J. Biol. Chem. 273: 2035-2043.
50. Janecki, A.J. et al. 1998. Subcellular redistribution is involved in acute regulation of the brush border Na+/H+ exchanger isoform 3 in human colon adenocarcinoma cell line Caco-2. Protein kinase C-mediated inhibition of the exchanger. J. Biol. Chem. 273: 8790-8798.
51. Kurashima, K. et al. 1997. Identification of sites required for down-regulation of Na+/H+ exchanger NHE3 activity by cAMP-dependent protein kinase. Phosphorylation-dependent and -independent mechanisms. J. Biol. Chem. 272: 28672-28679.
52. Yip, K.P. et al. 1998. Redistribution of Na+/H+ exchanger isoform NHE3 in proximal tubules induced by acute and chronic hypertension. Am. J. Physiol. 275: F565-F575.
53. Janecki, A.J. et al. 2000. Quantitation of plasma membrane expression of a fusion protein of Na/H exchanger NHE3 and green fluorescence protein (GFP) in living PS120 fibroblasts. J. Histochem. Cytochem. 48: 1479-1492.
54. Li, X. et al. 2001. Na+-H+ exchanger 3 (NHE3) is present in lipid rafts in the rabbit ileal brush border: a role for rafts in trafficking and rapid stimulation of NHE3. J. Physiol. 537: 537-552.
55. Hu, M.C. et al. 2001. Dopamine acutely stimulates Na+/H+ exchanger (NHE3) endocytosis via clathrin-coated vesicles: dependence on protein kinase A-mediated NHE3 phosphorylation. J. Biol. Chem. 276: 26906-26915.
56. Donowitz, M. et al. 2000. Short-term regulation of NHE3 by EGF and protein kinase C but not protein kinase A involves vesicle trafficking in epithelial cells and fibroblasts. Epithelial Transport and Barrier Function 915: 30-42.
57. Li, Y. et al. 2007. Regulation of insulin secretion and GLUT4 trafficking by the calcium sensor synaptotagmin VII. Biochem. Biophys. Res. Commun. 362: 658-664.
58. 2+ in insulin-stimulated glucose transport in 3T3-L1 cells. J. Biol. Chem. 276: 27816-27824.
59. Bommert, K. et al. 1993. Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature 363: 163-165.
60. DeBello, W.M., H. Betz & G.J. Augustine. 1993. Synaptotagmin and neurotransmitter release. Cell 74: 947-950.
61. Li, X. et al. 2004. Carbachol regulation of rabbit ileal brush border Na+-H+ exchanger 3 (NHE3) occurs through changes in NHE3 trafficking and complex formation and is Src dependent. J. Physiol. 556: 791-804.
62. Zachos, N.C. et al. 2008. Phospholipase Cgamma (PLCg) directly binds to the Na+/H+ exchanger 3 (NHE3) C-terminus which is necessary for basal and calcium-mediated inhibition of NHE3 activity. DDW 134: A744.
63. Donowitz, M. et al. 2005. NHERF family and NHE3 regulation. J. Physiol. 567: 3-11.
64. Murtazina, R. et al. 2007. Tissue-specific regulation of sodium/proton exchanger isoform 3 activity in Na(+)/H(+) exchanger regulatory factor 1 (NHERF1) null mice. cAMP inhibition is differentially dependent on NHERF1 and exchange protein directly activated by cAMP in ileum versus proximal tubule. J. Biol. Chem. 282: 25141-25151.
65. Yun, C.H. et al. 1997. cAMP-mediated inhibition of the epithelial brush border Na+/H+ exchanger, NHE3, requires an associated regulatory protein. Proc. Natl. Acad. Sci. USA 94: 3010-3015.
66. Murtazina, R. et al. 2008. NHERF2 is necessary for basal and all second messenger regulation of NHE3 activity in intact mouse ileal Na absorptive cells. DDW 134: A749.
67. Cinar, A. et al. 2007. NHE3 inhibition by cAMP and Ca2+ is abolished in PDZ-domain protein PDZK1-deficient murine enterocytes. J. Physiol. 581: 1235-1246.
68. Hillesheim, J. et al. 2007. Down regulation of small intestinal ion transport in PDZK1- (CAP70/NHERF3) deficient mice. Pflugers Arch. 454: 575-586.
69. 2+: inhibition with PDZK1 and stimulation with IKEPP. DDW 128: A177.
70. Morales, F.C. et al. 2004. Ezrin-radixin-moesin (ERM)-binding phosphoprotein 50 organizes ERM proteins at the apical membrane of polarized epithelia. Proc. Natl. Acad. Sci. USA 101: 17705-17710.
71. Donowitz, M. et al. 2008. Proteome of the small intestinal brush border of the NHERF1 knock out mouse: regulation of transporters and pro-proliferation molecules. Gastroenterology 134: S1770.
72. Murtazina, R. et al. 2008. NHERF2 is necessary for basal and all second messenger regulation of NHE3 activity in intact mouse ileal Na absorptive cells. Gastroenterology 134: A749.
73. Donowitz, M. & X. Li. 2007. Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87: 825-872.
74. Cha, B. et al. 2004. The lateral mobility of NHE3 on the apical membrane of renal epithelial OK cells is limited by the PDZ domain proteins NHERF1/2, but is dependent on an intact actin cytoskeleton as determined by FRAP. J. Cell Sci. 117: 3353-3365.
75. Lee-Kwon, W. et al. 2003. Lysophosphatidic acid stimulates brush border Na+/H+ exchanger 3 (NHE3) activity by increasing its exocytosis by an NHE3 kinase A regulatory protein-dependent mechanism. J. Biol. Chem. 278: 16494-16501.