Inhibition and Redistribution of NHE3, the Apical Na+/H + Exchanger, by Clostridium difficile Toxin B

Journal of General Physiology

Volumn 123, Issue 5, 2004, Pages 491-504

  Hayashi, Hisayoshi ^a   Szászi, Katalin ^a   Coady Osberg, Natasha ^a   Furuya, Wendy ^a   Bretscher, Anthony P ^b   Orlowski, John ^c   Grinstein, Sergio ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b Department of Obstetrics Gynecology   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Antiport; Ezrin; Na H exchange; pH regulation; Rho

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CLOSTRIDIUM DIFFICILE TOXIN B; DETERGENT; ENZYME INHIBITOR; EZRIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; SODIUM PROTON EXCHANGE PROTEIN;

ANIMAL CELL; ARTICLE; CLOSTRIDIUM DIFFICILE; DEPHOSPHORYLATION; ENZYME INACTIVATION; IMMUNOBLOTTING; INTESTINE EPITHELIUM; ION EXCHANGE; ION TRANSPORT; MEMBRANE BINDING; NONHUMAN; PH; PHOSPHORYLATION; PROTON SODIUM EXCHANGE; TIGHT JUNCTION;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL LINE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; PROTEIN ISOFORMS; SODIUM-HYDROGEN ANTIPORTER; TIGHT JUNCTIONS; TISSUE DISTRIBUTION;

EID: 2342586106     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200308979     Document Type: Article

References (64)

1. Ameen, N.A., and P.J. Salas. 2000. Microvillus inclusion disease: a genetic defect affecting apical membrane protein traffic in intestinal epithelium. Traffic. 1:76-83.
2. Benais-Pont, G., Punn A., C. Flores-Maldonado, J. Eckert, G. Raposo, T.P. Fleming, M.S. Balda and K. Matter. 2003. Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability. J. Cell Biol. 160:729-740.
3. Biemesderfer, D., B. DeGray, and P.S. Aronson. 1998. Membrane topology of NHE3. Epitopes within the carboxyl-terminal hydrophilic domain are exoplasmic. J. Biol. Chem. 273:12391-12396.
4. + exchanger isoform of renal brush border. Am. J. Physiol. 265:F736-F742.
5. Biemesderfer, D., P.A. Rutherford, T. Nagy, J.H. Pizzonia, A.K. Abu-Alfa, and P.S. Aronson. 1997. Monoclonal antibodies for high-resolution localization of NHE3 in adult and neonatal rat kidney. Am. J. Physiol. 273:F289-F299.
6. Botelho, R.J., M. Teruel, R. Dierckman, R. Anderson, A. Wells, J.D. York, T. Meyer, and S. Grinstein. 2000. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151:1353-1368.
7. Bretscher, A. 1989. Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes induced in A-431 cells by epidermal growth factor. J. Cell Biol. 108:921-930.
8. Bretscher, A., K. Edwards, and R.G. Fehon. 2002. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3:586-599.
9. Brown, D.A., and J.K. Rose. 1992. Sorting of GP1-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
10. + exchanger NHE3 isoform. J. Biol. Chem. 271:3590-3599.
11. Cano, A., P. Preisig, and R.J. Alpern. 1993. Cyclic adenosine monophosphate acutely inhibits and chronically stimulates Na/H anti-porter in OKP cells. J. Clin. Invest. 92:1632-1638.
12. + exchanger NHE3 by parathyroid hormone via NHE3 phosphorylation and dynamin-dependent endocytosis. J. Biol. Chem. 275:31601-31608.
13. Doughman, R.L., A.J. Firestone, and R.A. Anderson. 2003. Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place. J. Membr. Biol. 194:77-89.
14. + exchanger 3 accumulates and is functional in recycling endosomes. J. Biol. Chem. 273:2035-2043.
15. Gao, L., G. Joberty, and I.G. Macara. 2002. Assembly of epithelial tightjunctions is negatively regulated by Par6. Curr. Biol. 12:221-225.
16. Gaullier, J.M., A. Simonsen, A. D'Arrigo, B. Bremnes, and H. Stenmark. 1999. FYVE finger proteins as effectors of phosphatidyl-inositol 3-phosphate. Chem. Phys. Lipids. 98:87-94.
17. Gawenis, L.R., X. Stien, G.E. Shull, P.J. Schultheis, A.L. Woo, N.M. Walker, and L.L. Clarke. 2002. Intestinal NaCl transport in NHE2 and NHE3 knockout mice. Am. J. Physiol. Gastrointest. Liver Physiol. 282:G776-G784.
18. Ghosh, S., S. Gepstein, J.J. Heikkila, and E.B. Dumbroff. 1988. Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissues. Anal. Biochem. 169:227-233.
19. + exchanger-3 isoform. J. Biol. Chem. 277:11090-11096.
20. He, D., S.J. Hagen, C. Pothoulakis, M. Chen, N.D. Medina, M. Warny, and J.T. LaMont. 2000. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology. 119:139-150.
21. Hecht, G., A. Koutsouris, C. Pothoulakis, J.T. LaMont, and J.L. Madara. 1992. Clostridium difficile toxin B disrupts the barrier function of T84 monolayers. Gastroenterology. 102:416-423.
22. Helmle-Kolb, C., L. Counillon, D. Roux, J. Pouyssegur, B. Mrkic, and H. Murer. 1993. Na/H exchange activities in NHE1-transfected OK-cells: cell polarity and regulation. Pflugers Arch. 425: 34-40.
23. + exchange in opossum kidney cells: polarity and mechanisms. Pflugers Arch. 416:615-623.
24. Hirao, M., N. Sato, T. Kondo, S. Yonemura, M. Monden, T. Sasaki, Y. Takai, and S. Tsukita. 1996. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway. J. Cell Biol. 135:37-51.
25. + exchange through distinct Cdc42-dependent and RhoA-dependent pathways. J. Biol. Chem. 271:6152-6158.
26. + exchanger (NHE3) endocytosis via clathrin-coated vesicles: dependence on protein kinase A-mediated NHE3 phosphorylation. J. Biol. Chem. 276:26906-26915.
27. + 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.
28. Just, I., J. Selzer, M. Wilm, C. von Eichel-Streiber, M. Mann, and K. Aktories. 1995a. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature. 375:500-503.
29. Just, I., M. Wilm, J. Selzer, G. Rex, C. von Eichel-Streiber, M. Mann, and K. Aktories. 1995b. The enterotoxin from Clostridium difficile (ToxA) monoglucosylates the Rho proteins. J. Biol. Chem. 270: 13932-13936.
30. + exchanger stably expressed in Chinese hamster ovary cells. ATP dependence, osmotic sensitivity, and role in cell proliferation. J. Biol. Chem. 269:23544-23552.
31. Kelly, C.P., and J.T. LaMont. 1998. Clostridium difficile infection. Annu. Rev. Med. 49:375-390.
32. Klussmann, E., G. Tamma, D. Lorenz, B. Wiesner, K. Maric, F. Hofmann, K. Aktories, G. Valenti, and W. Rosenthal. 2001. An inhibitory role of Rho in the vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J. Biol. Chem. 276:20451-20457.
33. Kotani, H., K. Takaishi, T. Sasaki, and Y. Takai. 1997. Rho regulates association of both the ERM family and vinculin with the plasma membrane in MDCK cells. Oncogene. 14:1705-1713.
34. + exchanger NHE3 isoform is regulated by the phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 273:20828-20836.
35. Matsui, T., M. Maeda, Y. Doi, S. Yonemura, M. Amano, K. Kaibuchi, and S. Tsukita. 1998. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140:647-657.
36. Matsui, T., S. Yonemura, and S. Tsukita. 1999. Activation of ERM proteins in vivo by Rho involves phosphatidyl-inositol 4-phosphate 5-kinase and not ROCK kinases. Curr. Biol. 9:1259-1262.
37. Mukherjee, S., R.N. Ghosh, and ER. Maxfield. 1997. Endocytosis. Physiol. Rev. 77:759-803.
38. Mukherjee, S., T.T. Soe, and F.R. Maxfield. 1999. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J. Cell Biol. 144:1271-1284.
39. Mylonakis, E., E.T. Ryan, and S.B. Caldenvood. 2001. Clostridium difficile-associated diarrhea: a review. Arch. Intern. Med. 161:525-533.
40. Niggli, V., C. Andreoli, C. Roy, and P. Mangeat. 1995. Identification of a phosphatidylinositol-4,5-bisphosphate-binding domain in the N-terminal region of ezrin. FEBS Lett. 376:172-176.
41. Orlowski, J. 1993. Heterologous expression and functional properties of amiloride high affinity (NHE-1) and low affinity (NHE-3) isoforms of the rat Na/H exchanger. J. Biol. Chem. 268:16369-16377.
42. + exchangers of mammalian cells. J. Biol. Chem. 272:22373-22376.
43. Pothoulakis, C. 2000. Effects of Clostridium difficile toxins on epithelial cell barrier. Ann NY Acad Sci. 915:347-356.
44. Pothoulakis, C., and J.T. Lamont. 2001. Microbes and microbial toxins: paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G178-G183.
45. Raiborg, C., and H. Stenmark. 2002. Hrs and endocytic sorting of ubiquitinated membrane proteins. Cell Struct. Funct. 27:403-408.
46. + exchangers NHE2 and NHE3 in rat intestine and human Caco-2/bbe cells. Am J. Physiol. Cell Physiol. 280:C1224-C1232.
47. Roos, A., and W.F. Boron. 1981. Intracellular pH. Physiol. Rev. 61: 296-434.
48. Scaduto, R.C., Jr., and L.W. Grotyohann. 1999. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys. J. 76:469-477.
49. + exchanger. Nat. Genet. 19:282-285.
50. Shenolikar, S., J.W. Voltz., C.M. Minkoff, J.B. Wade, and E.J. Weinman. 2002. Targeted disruption of the mouse NHERF-1 gene promotes internalization of proximal tubule sodium-phosphate cotransporter type IIa and renal phosphate wasting. Proc. Natl. Acad. Sci. USA. 99:11470-11475.
51. Shenolikar, S., and E.J. Weinman. 2001. NHERF: targeting and trafficking membrane proteins. Am. J. Physiol. Renal Physiol. 280: F389-F395.
52. + exchanger in human choriocarcinoma (BeWo) cells. Pflugers Arch. 433:792-802.
53. Stauffer, T.P., S. Ahn, and T. Meyer. 1998. Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr. Biol. 8:343-346.
54. + exchanger NHE3. Role of mysoin light chain phosphorylation. J. Biol. Chem. 275:28599-28606.
55. Thomas, J.A., R.N. Buchsbaum, A. Zimniak, and E. Racker. 1979. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry. 18: 2210-2218.
56. Tominaga, T., and D.L. Barber. 1998. Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading. Mol. Biol. Cell. 9:2287-2303.
57. Uehata, M., T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya. 1997. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 389:990-994.
58. Vega-Salas, D.E., P.J. Salas, and E. Rodriguez-Boulan. 1987. Modulation of the expression of an apical plasma membrane protein of Madin-Darby canine kidney epithelial cells: cell-cell interactions control the appearance of a novel intracellular storage compartment. J. Cell Biol. 104:1249-1259.
59. + exchangers. Physiol. Rev. 77:51-74.
60. + exchanger in rabbit kidney brush-border membranes. Am. J. Physiol. 252:F19-F25.
61. Weinman, E.J., D. Steplock, and S. Shenolikar. 2003. NHERF-1 uniquely transduces the cAMP signals that inhibit sodium-hydrogen exchange in mouse renal apical membranes. FEBS Lett. 536: 141-144.
62. Yonemura, S., M. Hirao, Y. Doi, N. Takahashi, T. Kondo, and S. Tsukita. 1998. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J. Cell Biol. 140: 885-895.
63. Yonemura, S., T. Matsui, and S. Tsukita. 2002. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115:2569-2580.
64. + exchanger gene family: structure and function studies. Am. J. Physiol. 269:G1-G11.