The ERM protein, Ezrin, regulates neutrophil transmigration by modulating the apical localization of MRP2 in response to the SipA effector protein during Salmonella Typhimurium infection

Cellular Microbiology

Volumn 13, Issue 12, 2011, Pages 2007-2021

  Agbor, Terence A ^a   Demma, Zachary C ^a   Mumy, Karen L ^a   Bien, Jeffrey D ^b   Mccormick, Beth A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EZRIN; MULTIDRUG RESISTANCE PROTEIN 2; PROTEIN KINASE C; PROTEIN KINASE C ALPHA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SALMONELLA TYPHIMURIUM; SALMONELLOSIS;

BACTERIAL PROTEINS; BENZOPHENANTHRIDINES; BLOTTING, WESTERN; CARBAZOLES; CELL LINE, TUMOR; CELL MOVEMENT; CYTOSKELETAL PROTEINS; HUMANS; INTESTINAL MUCOSA; MICROFILAMENT PROTEINS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEUTROPHILS; PHOSPHORYLATION; PROTEIN KINASE C-ALPHA; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; TRANSFECTION;

SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 81355154689     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01693.x     Document Type: Article

References (31)

1. Breitkreutz, D., Braiman-Wiksman, L., Daum, N., Denning, M.F., and Tennenbaum, T. (2007) Protein kinase C family: on the crossroads of cell signaling in skin and tumor epithelium. J Cancer Res Clin Oncol 133: 793-808.
2. Bretscher, A., Chambers, D., Nguyen, R., and Reczek, D. (2000) ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu Rev Cell Dev Biol 16: 113-143.
3. Cao, T.T., Deacon, H.W., Reczek, D., Bretscher, A., and von Zastrow, M. (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature 401: 286-290.
4. Cummins, E.P., Berra, E., Comerford, K.M., Ginouves, A., Fitzgerald, K.T., Seeballuck, F., etal. (2006) Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc Natl Acad Sci USA 103: 18154-18159.
5. Gewirtz, A.T., Siber, A.M., Madara, J.L., and McCormick, B.A. (1999) Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect Immun 67: 608-617.
6. Ito, K., Wakabayashi, T., and Horie, T. (2005) Mrp2/Abcc2 transport activity is stimulated by protein kinase Calpha in a baculo virus co-expression system. Life Sci 77: 539-550.
7. Kikuchi, S., Hata, M., Fukumoto, K., Yamane, Y., Matsui, T., Tamura, A., etal. (2002) Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nat Genet 31: 320-325.
8. Kohler, H., Sakaguchi, T., Hurley, B.P., Kase, B.A., Reinecker, H.C., and McCormick, B.A. (2007) Salmonella enterica serovar Typhimurium regulates intercellular junction proteins and facilitates transepithelial neutrophil and bacterial passage. Am J Physiol Gastrointest Liver Physiol 293: G178-G187.
9. Lee, C.A., Silva, M., Siber, A.M., Kelly, A.J., Galyov, E., and McCormick, B.A. (2000) A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci USA 97: 12283-12288.
10. Li, M., Wang, W., Soroka, C.J., Mennone, A., Harry, K., Weinman, E.J., etal. (2010) NHERF-1 binds to Mrp2 and regulates hepatic Mrp2 expression and function. J Biol Chem 285: 19299-19307.
11. Luciani, F., Molinari, A., Lozupone, F., Calcabrini, A., Lugini, L., Stringaro, A., etal. (2002) P-glycoprotein-actin association through Erm family proteins: a role in P-glycoprotein function in human cells of lymphoid origin. Blood 99: 641-648.
12. McCormick, B.A., Colgan, S.P., Delp-Archer, C., Miller, S.I., and Madara, J.L. (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907.
13. McCormick, B.A., Parkos, C.A., Colgan, S.P., Carnes, D.K., and Madara, J.L. (1998) Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J Immunol 160: 455-466.
14. Mrsny, R.J., Gewirtz, A.T., Siccardi, D., Savidge, T., Hurley, B.P., Madara, J.L., etal. (2004) Identification of hepoxilin A3 in inflammatory events: a required role in neutrophil migration across intestinal epithelia. Proc Natl Acad Sci USA 101: 7421-7426.
15. Mumy, K.L., Bien, J.D., Pazos, M.A., Gronert, K., Hurley, B.P., and McCormick, B.A. (2008) Distinct isoforms of phospholipase A2 mediate the ability of Salmonella enterica serotype typhimurium and Shigella flexneri to induce the transepithelial migration of neutrophils. Infect Immun 76: 3614-3627.
16. Nakano, T., Sekine, S., Ito, K., and Horie, T. (2009) Correlation between apical localization of Abcc2/Mrp2 and phosphorylation status of ezrin in rat intestine. Drug Metab Dispos 37: 1521-1527.
17. Parkos, C.A., Colgan, S.P., Delp, C., Arnaout, M.A., and Madara, J.L. (1992) Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways. J Cell Biol 117: 757-764.
18. Pazos, M., Siccardi, D., Mumy, K.L., Bien, J.D., Louie, S., Shi, H.N., etal. (2008) Multidrug resistance-associated transporter 2 regulates mucosal inflammation by facilitating the synthesis of hepoxilin A3. J Immunol 181: 8044-8052.
19. Rasmussen, M., Alexander, R.T., Darborg, B.V., Mobjerg, N., Hoffmann, E.K., Kapus, A., and Pedersen, S.F. (2008) Osmotic cell shrinkage activates ezrin/radixin/moesin (Erm) proteins: activation mechanisms and physiological implications. Am J Physiol Cell Physiol 294: 197-212.
20. Reczek, D., Berryman, M., and Bretscher, A. (1997) Identification of EBP50: a PDZ-containing phosphoprotein that associates with members of the ezrin-radixin-moesin family. J Cell Biol 139: 169-179.
21. Saotome, I., Curto, M., and McClatchey, A.I. (2004) Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell 6: 855-864.
22. Shiue, H., Musch, M.W., Wang, Y., Chang, E.B., and Turner, J.R. (2005) Akt2 phosphorylates ezrin to trigger NHE3 translocation and activation. J Biol Chem 280: 1688-1695.
23. Silva, M., Song, C., Nadeau, W.J., Matthews, J.B., and McCormick, B.A. (2004) Salmonella typhimurium SipA-induced neutrophil transepithelial migration: involvement of a PKC-alpha-dependent signal transduction pathway. Am J Physiol Gastrointest Liver Physiol 286: G1024-G1031.
24. Srikanth, C.V., Wall, D.M., Maldonado-Contreras, A., Shi, H.N., Zhou, D., Demma, Z., etal. (2010) Salmonella pathogenesis and processing of secreted effectors by caspase-3. Science 330: 390-393.
25. Strohmeier, G.R., Lencer, W.I., Patapoff, T.W., Thompson, L.F., Carlson, S.L., Moe, S.J., etal. (1997) Surface expression, polarization, and functional significance of CD73 in human intestinal epithelia. J Clin Invest 99: 2588-2601.
26. Wakusawa, S., Machida, I., Suzuki, S., Hayashi, H., Yano, M., and Yoshioka, K. (2003) Identification of a novel 2026G->C mutation of the MRP2 gene in a Japanese patient with Dubin-Johnson syndrome. J Hum Genet 48: 425-429.
27. Wald, F.A., Oriolo, A.S., Mashukova, A., Fregien, N.L., Langshaw, A.H., and Salas, P.J. (2008) Atypical protein kinase C (iota) activates ezrin in the apical domain of intestinal epithelial cells. J Cell Sci 121: 644-654.
28. Wang, W., Soroka, C.J., Mennone, A., Rahner, C., Harry, K., Pypaert, M., etal. (2006) Radixin is required to maintain apical canalicular membrane structure and function in rat hepatocytes. Gastroenterology 131: 878-884.
29. Weinman, E.J., Steplock, D., Wang, Y., and Shenolikar, S. (1995) Characterization of a protein cofactor that mediates protein kinase A regulation of the renal brush border membrane Na(+)-H+ exchanger. J Clin Invest 95: 2143-2149.
30. Yang, Q., Onuki, R., Nakai, C., and Sugiyama, Y. (2007) Ezrin and radixin both regulate the apical membrane localization of ABCC2 (MRP2) in human intestinal epithelial Caco-2 cells. Exp Cell Res 313: 3517-3525.
31. Zhao, H., Shiue, H., Palkon, S., Wang, Y., Cullinan, P., Burkhardt, J.K., etal. (2004) Ezrin regulates NHE3 translocation and activation after Na+-glucose cotransport. Proc Natl Acad Sci USA 101: 9485-9490.