The NHE3 juxtamembrane cytoplasmic domain directly binds ezrin: Dual role in NHE3 trafficking and mobility in the brush border

Molecular Biology of the Cell

Volumn 17, Issue 6, 2006, Pages 2661-2673

  Cha, Boyoung ^a   Tse, Ming ^a   Yun, Chris ^a,c   Kovbasnjuk, Olga ^a   Mohan, Sachin ^a   Hubbard, Ann ^a   Arpin, Monique ^b   Donowitz, Mark ^a  

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

^b CNRS   (France)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EZRIN; PDZ PROTEIN; PROTEIN NHERF1; PROTEIN NHERF2; SODIUM PROTON EXCHANGE PROTEIN 3; UNCLASSIFIED DRUG;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BRUSH BORDER; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; MICROVILLUS; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL MEMBRANE; CONSERVED SEQUENCE; CYTOPLASM; CYTOSKELETAL PROTEINS; HUMANS; JUXTAGLOMERULAR APPARATUS; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM-HYDROGEN ANTIPORTER;

EID: 33744779069     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-09-0843     Document Type: Article

References (54)

1. - salvage mechanisms in model systems and the mouse pancreatic duct. J. Biol. Chem. 276, 17236-17243.
2. Akhter, S., Cavet, M. E., Tse, C. M., and Donowitz, M. (2002). 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.
3. Alexander, R. T., Furuya, W., Szaszi, K., Orlowski, J., and Grinstein, S. (2005). Rho GTPases dictate the mobility of the Na/H exchanger NHE3 in epithelia: role in apical retention and targeting. Proc. Natl. Acad. Sci. USA 102, 12253-12258.
4. Bader, M.-F., Doussau, F., Chasserot-Golaz, S., Vitale, N., and Gasman, S. (2004). Coupling actin and membrane dynamics during calcium-regulated exocytosis: a role for Rho and ARF GTPases. Biochim. Biophys. Acta 1742, 37-49.
5. Bader, M.-F., Holz, R. W., Kumakura, K., and Vitale, N. (2002). Exocytosis: the chromaffin cell as a model system. Ann. NY Acad. Sci. 971, 178-183.
6. Baumgartner, M., Patel, H., and Barber, D. L. (2004). Na(+)/H(+) exchanger NHE1 as plasma membrane scaffold in the assembly of signaling complexes. Am. J. Physiol. Cell 287, C844-C850.
7. Biemesderfer, M., Mentone, S. A., Mooseker, M., and Hasson, T. (2002). Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules Am. J. Physiol. 282, F785-F794.
8. Bretscher, A., Edwards, K., and Fehon, R. G. (2002). ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell. Biol. 3, 586-599.
9. + exchanger NHE3 isoform. J. Biol. Chem. 271, 3590-3599.
10. Cavet, M. E., Akhter, S., Murtazina, R., Sanchez de Medina, F., Tse, C. M., and Donowitz, M. (2001). Half-lives of plasma membrane Na(+)/H(+) exchangers NHE1-3, plasma membrane NHE2 has a rapid rate of degradation. Am. J. Physiol. 281, C2039-C2048.
11. Cha, B., Kenworthy, A., Murtazina, R., and Donowitz, M. (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.
12. + antiporter 3 (NHE3) requires PDZ domain adapter NHERF2, a broad specificity protein kinase G-anchoring protein. J. Biol. Chem. 280, 16642-16650.
13. + exchanger isoform 3 (NHE3) determine the set point. J. Membr. Biol. 191, 49-58.
14. Chambers, D. N., and Bretscher, A. (2005). Ezrin mutants affecting dimerization and activation. Biochemistry 44, 3926-3932.
15. Denker, S. P., and Barber, D. L. (2002). Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J. Cell Biol. 159, 1087-1096.
16. Denker, S. P., Huang, D. C., Orlowski, J., Furthmayr, H., and Barber, D. L. (2000). Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H(+) translocation. Mol. Cell 6, 1425-1436.
17. Donowitz, M., Cha, B., Zachos, N. C., Brett, C. L., Sharma, A., Tse, C. M., and Li, X. (2005). NHERF family and NHE3 regulation. J. Physiol. 567, 3-11.
18. + exchanger 3 accumulates and is functional in recycling endosomes. J. Biol. Chem. 273, 2035-2043.
19. Finnerty, C. M., Chambers, D., Ingraffea, J., Faber, H. R., Karplus, P. A., and Bretscher, A. (2004). The EBP50-moesin interaction involves a binding site regulated by direct masking on the FERM domain. J. Cell Sci. 117, 1547-1552.
20. Gautreau, A., Poullet, P., Louvard, D., and Arpin, M. (1999). Ezrin, a plasma membrane-microfilament linker, signals cell survival through the phosphati dylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. USA 96, 7300-7305.
21. + exchange. Nature 392, 626-630.
22. Hamada, K., Shimizu, T. L., Matsui, T., Tsukita, M., Tsukita, S., and Hakoshima, T. (2000). Structural basis of the membrane-targeting and unmasking mechanisms of the radixin PERM domain. EMBO J. 22, 502-514.
23. Hamada, K., Shimizu, T., Yonemura, S., Tsukita, S., Tsukita, S., and Hakoshima, T. (2003). Structural basis of adhesion-molecule recognition by ERM proteins revealed by the crystal structure of the radixin-ICAM-2 complex. EMBO J. 22, 502-514.
24. Hasson, T. (2003). Myosin VI: two distinct roles in endocytosis. J. Cell Sci. 226, 3453-3461.
25. Heiska, L., Alfthan, K., Gronholm, M., Vilja, P., Vaheri, A., and Carpen, O. (1998). Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM2). Regulation by phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 273, 21893-21900.
26. Helander, T. S., Carpen, O., Turunen, O., Kovanen, P. E., Vaheri, A., and Timonon, T. (1996). ICAM-2 redistributed by ezrin as a target for killer cells. Nature 382, 265-268.
27. + exchanger (NHE1): pH-maintenance, ATP-sensitive, and flexible loop domains. J. Biochem. 121, 295-303.
28. + exchanger 3 (NHE3) requires an NHE3-E3KARP-alpha-actinin-4 complex for oligomerization and endocytosis. J. Biol. Chem. 277, 23714-23724.
29. + exchanger 3 (NHE3) activity by increasing its exocytosis by an NHE3 kinase A regulatory protein-dependent mechanism. J. Biol. Chem. 278, 16494-16501.
30. + exchanger isoform NHE3 are involved in stimulation and inhibition by protein kinases/growth factors. J. Biol. Chem. 270, 13716-13725.
31. + exchanger 3 (NHE3) occurs through changes in NHE3 trafficking and complex formation and is Src dependent. J. Physiol. 556, 791-804.
32. Lozupone, F., Lugini, L., Matarrese, P., Luciani, F., Federici, C., Iessi, E., Margutti, P., Stassi, G., Malorni, W., and Fais, S. (2004). Identification and relevance of the CD95-binding domain in the N-terminal region of ezrin. J. Biol. Chem. 279, 9199-9207.
33. Pearson, M. A., Reczek, D., Bretscher, A., and Karplus, P. A. (2000). Structure of the ERM protein moesin reveals the PERM domain fold masked by an extended actin binding tail domain. Cell 101, 259-270.
34. + antiport activity in hamster fibroblasts precludes growth at neural and acidic pH. Proc. Natl. Acad. Sci. USA 81, 4833-4837.
35. Reczek, D., and Bretscher, A. (1998). The carboxyl-terminal region of EBP50 binds to a site in the amino-terminal domain of ezrin that is masked in the dormant molecule. J. Biol. Chem. 273, 18452-18458.
36. Rudich, A., and Klip, A. (2003). Push/pull mechanisms of GLUT4 traffic in muscle cells. Acta Physiol. Scand. 178, 297-308.
37. Schmieder, S., Nagai, M., Orlando, R. A., Takeda, T., and Farquhar, M. G. (2004). Podocalyxin activates RhoA and induces actin reorganization through NHERF1 and Ezrin in MDCK cells. J. Am. Soc. Nephrol. 15, 2289-2298.
38. Shenolikar, S., Voltz, J. W., Cunningham, R., and Weinman, E. J. (2004). Regulation of ion transport by the NHERF family of PDZ proteins. Physiology 19, 362-369.
39. Smith, W. J., and Cerione, R. A. (2002). Crystallization and preliminary crystallographic analysis of the ezrin FERM domain. Acta Crystallogr. D. Biol. Crystallogr. 58, 1359-1361.
40. Smith, W. J., Nassar, N., Bretscher, A., Cerione, R. A., and Karplus, P. A. (2003). Structure of the active N-terminal domain of Ezrin. Conformational and mobility changes identify keystone interactions. J. Biol. Chem. 278, 4949-4956.
41. Sun, F., Hug, M. J., Lewarchik, C. M., Yun, C. H., Bradbury, N. A., and Frizzell, R. A. (2000). E3KARP mediates the association of ezrin and protein kinase A with the cystic fibrosis transmembrane conductance regulator in airway cells. J. Biol. Chem. 275, 539-546.
42. Tsukita, S., Oishi, K., Sato, N., Sagara, J., Kawai, A., and Tsukita, S. (1994). ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 226, 391-401.
43. Valentijn, K., Valentijn, J. A., and Jamieson, J. D. (1999). Role of actin in regulated exocytosis and compensatory membrane retrieval: insights from an old acquaintance. Biochem. Biophys. Res. Commun. 266, 652-661.
44. + antiporter cytoplasmic domain mediates growth factor signals and controls "H(+)-sensing". Proc. Natl. Acad. Sci. USA 89, 2424-2428.
45. + exchangers by measurement of reverse mode reaction. J. Biol. Chem. 278, 43580-43585.
46. Wang, S., Raab, R. W., Schatz, P. J., Guggino, W. B., and Li, M. (1998). Peptide binding consensus of the NHE-RF-PDZ1 domain matches the C-terminal sequence of cystic fibrosis transmembrane conductance regulator (CFTR). FEBS Lett. 427, 103-108.
47. Ward, R. E., IV, Schweizer, L., Lamb, R. S., and Fehon, R. G. (2001). The protein 4.1, ezrin, radixin, moesin (PERM) domain of Drosophila Coracle, a cytoplasmic component of the septate junction, provides functions essential for embryonic development and imaginal cell proliferation. Genetics 159, 219-228.
48. Weinman, E. J., Steplock, D., Donowitz, M., and Shenolikar, S. (2000). NHERF associations with sodium-hydrogen exchanger isoform 3 (NHE3) and ezrin are essential for cAMP-mediated phosphorylation and inhibition of NHE3. Biochemistry 23, 6123-6129.
49. Wenk, M. R., and Camilli, P. (2004). Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. USA 101, 8262-8269.
50. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., Tsukita, S., and Tsukita, S. (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.
51. + exchanger NHE3 and the cytoskeletal protein ezrin. J. Biol. Chem. 273, 25856-25863.
52. + exchanger, NHE3, requires an associated regulatory protein. Proc. Natl. Acad. Sci. USA 94, 3010-3015.
53. + exchange. Annu. Rev. Physiol. 67, 411-443.
54. Zizak, M., Lamprecht, G., Steplock, D., Tariq, N., Shenolikar, S., Donowitz, M., Yun, C.H.C., and Weinman, E. J. (1999). cAMP-induced phosphorylation and inhibition of Na(+)/H(+) exchanger 3 (NHE3) are dependent on the presence but not the phosphorylation of NHE regulatory factor. J. Biol. Chem. 274, 24753-24758.