NHERF2 protein mobility rate is determined by a unique C-terminal domain that is also necessary for its regulation of NHE3 protein in OK cells

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16960-16974

  Yang, Jianbo ^a   Singh, Varsha ^a   Cha, Boyoung ^a   Chen, Tian E ^a   Sarker, Rafiquel ^a   Murtazina, Rakhilya ^a   Jin, Shi ^a   Zachos, Nicholas C ^a   Patterson, George H ^b   Tse, C Ming ^a   Kovbasnjuk, Olga ^a   Li, Xuhang ^a   Donowitz, Mark ^a  

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

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; FLUORESCENCE RECOVERY; INTESTINAL EPITHELIAL CELLS; LYSOPHOSPHATIDIC ACID; MULTIPROTEIN SIGNALING; REGULATORY FACTORS; SCAFFOLDING PROTEINS; TRANS-MEMBRANE PROTEINS;

BIOLOGICAL MEMBRANES; CELL CULTURE; DIFFUSION; MOLECULAR BIOLOGY; PHOSPHOLIPIDS; PROTEINS; WELL STIMULATION;

SCAFFOLDS (BIOLOGY);

REGULATOR PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 3; SODIUM PROTON EXCHANGER REGULATOR 1 PROTEIN; SODIUM PROTON EXCHANGER REGULATOR 2 PROTEIN; SODIUM PROTON EXCHANGER REGULATOR 3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DIFFUSION COEFFICIENT; HUMAN; HUMAN CELL; KIDNEY CELL; MICROVILLUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSPORT KINETICS;

EPITHELIAL CELL; EXOCYTOSIS; MOBILITY; SCAFFOLD PROTEINS; SODIUM PROTON EXCHANGE; TRAFFICKING;

ANIMALS; CACO-2 CELLS; CALCIMYCIN; CALCIUM IONOPHORES; CYTOSKELETAL PROTEINS; HUMANS; KIDNEY TUBULES, PROXIMAL; LYSOPHOSPHOLIPIDS; MULTIPROTEIN COMPLEXES; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RABBITS; RATS; SODIUM-HYDROGEN ANTIPORTER;

EID: 84878749405     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.470799     Document Type: Article

References (55)

1. Lange, K. (2011) Fundamental role of microvilli in the main functions of differentiated cells: Outline of an universal regulating and signaling system at the cell periphery. J. Cell. Physiol. 226, 896-927
2. + exchanger isoform, NHE3. Am. J. Physiol. 269, C198-C206
3. + exchanger. Nat. Genet. 19, 282-285
4. Donowitz, M., and Li, X. (2007) Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87, 825-872 (Pubitemid 47086280)
5. + exchange regulatory factors. Pharmacol. Rev. 63, 882-900
6. Romero, G., von Zastrow, M., and Friedman, P. A. (2011) Role of PDZ proteins in regulating trafficking, signaling, and function of GPCRs: means, motif, and opportunity. Adv. Pharmacol. 62, 279-314
7. + exchanger. J. Clin. Invest. 95, 2143-2149
8. Sarker, R., Valkhoff, V. E., Zachos, N. C., Lin, R., Cha, B., Chen, T. E., Guggino, S., Zizak, M., de Jonge, H., Hogema, B., and Donowitz, M. (2011) NHERF1 and NHERF2 are necessary for multiple but usually separate aspects of basal and acute regulation of NHE3 activity. Am. J. Physiol. Cell Physiol. 300, C771-C782
9. Murtazina, R., Kovbasnjuk, O., Chen, T. E., Zachos, N. C., Chen, Y., Kocinsky, H. S., Hogema, B. M., Seidler, U., de Jonge, H. R., and Donowitz, M. (2011) NHERF2 is necessary for basal activity, second messenger inhibition, and LPA stimulation of NHE3 in mouse distal ileum. Am. J. Physiol. Cell Physiol. 301, C126-C136
10. + exchanger 3 and fluid absorption via LPA(5) and NHERF2. Gastroenterology 138, 649-658
11. + exchanger isoform 3 revisited. The roles of SGK1 and NHERF2. J. Biol. Chem. 277, 7676-7683
12. 2+ is abolished in PDZ-domain protein PDZK1-deficient murine enterocytes. J. Physiol. 581, 1235-1246
13. Zachos, N. C., Hodson, C., Kovbasnjuk, O., Li, X., Thelin, W. R., Cha, B., Milgram, S., and Donowitz, M. (2008) Elevated intracellular calcium stimulates NHE3 activity by an IKEPP (NHERF4)-dependent mechanism. Cell. Physiol. Biochem. 22, 693-704
14. Wade, J. B., Liu, J., Coleman, R. A., Cunningham, R., Steplock, D. A., Lee-Kwon, W., Pallone, T. L., Shenolikar, S., and Weinman, E. J. (2003) Localization and interaction of NHERF isoforms in the renal proximal tubule of the mouse. Am. J. Physiol. Cell Physiol. 285, C1494-C1503 (Pubitemid 37429624)
15. Cotton, L. M., Rodriguez, C. M., Suzuki, K., Orgebin-Crist, M. C., and Hinton, B. T. (2010) Organic cation/carnitine transporter, OCTN2, transcriptional activity is regulated by osmotic stress in epididymal cells. Mol. Reprod. Dev. 77, 114-125
16. 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 (Pubitemid 41167297)
17. Cha, B., Zhu, X. C., Chen, W., Jones, M., Ryoo, S., Zachos, N. C., Chen, T. E., Lin, R., Sarker, R., Kenworthy, A. K., Tse, M., Kovbasnjuk, O., and Donowitz, M. (2010) NHE3 mobility in brush borders increases upon NHERF2-dependent stimulation by lysophosphatidic acid. J. Cell Sci. 123, 2434-2443
18. Brown, J. W., and McKnight, C. J. (2010) Molecular model of the microvillar cytoskeleton and organization of the brush border. PLoS One 5, e9406
19. 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 (Pubitemid 39139919)
20. + exchange regulatory factor 2-dependent process. Gastroenterology 140, 560-571
21. Zhu, X., Cha, B., Zachos, N. C., Sarker, R., Chakraborty, M., Chen, T. E., Kovbasnjuk, O., and Donowitz, M. (2011) Elevated calcium acutely regulates dynamic interactions of NHERF2 and NHE3 in OK cell microvilli. J. Biol. Chem. 286, 34486-34496
22. Seidler, U., Singh, A. K., Cinar, A., Chen, M., Hillesheim, J., Hogema, B., and Riederer, B. (2009) The role of the NHERF family of PDZ scaffolding proteins in the regulation of salt and water transport. Ann. N.Y. Acad. Sci. 1165, 249-260
23. + exchanger NHE3 and the cytoskeletal protein ezrin. J. Biol. Chem. 273, 25856-25863
24. + exchanger NHE3 activity and trafficking are lipid Raft-dependent. J. Biol. Chem. 281, 17845-17855
25. McKinney, S. A., Murphy, C. S., Hazelwood, K. L., Davidson, M. W., and Looger, L. L. (2009) A bright and photostable photoconvertible fluorescent protein. Nat. Methods 6, 131-133
26. Ellenberg, J., Siggia, E. D., Moreira, J. E., Smith, C. L., Presley, J. F., Worman, H. J., and Lippincott-Schwartz, J. (1997) Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol. 138, 1193-1206 (Pubitemid 27415047)
27. Mavrakis, M., Rikhy, R., Lilly, M., and Lippincott-Schwartz, J. (2008) Fluorescence imaging techniques for studying Drosophila embryo development. Curr. Protoc. Cell Biol. Chapter 4, Unit 4.18
28. + 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
29. + exchanger 3 (NHE3) occurs through changes in NHE3 trafficking and complex formation and is Src-dependent. J. Physiol. 556, 791-804
30. Haggie, P. M., Stanton, B. A., and Verkman, A. S. (2004) Increased diffusional mobility of CFTR at the plasma membrane after deletion of its C-terminal PDZ-binding motif. J. Biol. Chem. 279, 5494-5500 (Pubitemid 38220574)
31. + exchanger regulatory factor-1 association and dissociation regulate parathyroid hormone receptor trafficking at membrane microdomains. J. Biol. Chem. 286, 35020-35029
32. Garbett, D., and Bretscher, A. (2012) PDZ interactions regulate rapid turnover of the scaffolding protein EBP50 in microvilli. J. Cell Biol. 198, 195-203
33. Cole, J. A., Forte, L. R., Krause, W. J., and Thorne, P. K. (1989) Clonal sublines that are morphologically and functionally distinct from parental OK cells. Am. J. Physiol. 256, F672-F679
34. 2+ pump 2B variants in polarized epithelial cells. J. Biol. Chem. 285, 31704-31712
35. Lee, H. J., and Zheng, J. J. (2010) PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun. Signal. 8, 8
36. + exchanger regulatory factor interaction with the β2 adrenergic and platelet-derived growth factor receptors. J. Biol. Chem. 277, 18973-18978
37. Weinman, E. J., Wang, Y., Wang, F., Greer, C., Steplock, D., and Shenolikar, S. (2003) A C-terminal PDZ motif in NHE3 binds NHERF-1 and enhances cAMP inhibition of sodium-hydrogen exchange. Biochemistry 42, 12662-12668 (Pubitemid 37337557)
38. 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 (Pubitemid 38559829)
39. Terawaki, S., Maesaki, R., and Hakoshima, T. (2006) Structural basis for NHERF recognition by ERM proteins. Structure 14, 777-789
40. Morales, F. C., Takahashi, Y., Momin, S., Adams, H., Chen, X., and Georgescu, M. M. (2007) NHERF1/EBP50 head-to-tail intramolecular interaction masks association with PDZ domain ligands. Mol. Cell. Biol. 27, 2527-2537 (Pubitemid 46581344)
41. + exchange in OK cells. Am. J. Physiol. Renal Physiol. 281, F374-F380
42. Itoh, K., Sakakibara, M., Yamasaki, S., Takeuchi, A., Arase, H., Miyazaki, M., Nakajima, N., Okada, M., and Saito, T. (2002) Cutting edge: negative regulation of immune synapse formation by anchoring lipid raft to cytoskeleton through Cbp-EBP50-ERM assembly. J. Immunol. 168, 541-544 (Pubitemid 34049551)
43. Lissner, S., Nold, L., Hsieh, C. J., Turner, J. R., Gregor, M., Graeve, L., and Lamprecht, G. (2010) Activity and PI3-kinase-dependent trafficking of the intestinal anion exchanger down-regulated in adenoma depend on its PDZ interaction and on lipid rafts. Am. J. Physiol. Gastrointest. Liver Physiol. 299, G907-G920
44. Berryman, M., Gary, R., and Bretscher, A. (1995) Ezrin oligomers are major cytoskeletal components of placental microvilli: a proposal for their involvement in cortical morphogenesis. J. Cell Biol. 131, 1231-1242
45. + exchanger 3 (NHE3) activity by increasing its exocytosis by an NHE3 kinase A regulatory protein-dependent mechanism. J. Biol. Chem. 278, 16494-16501
46. 2+-dependent inhibition of NHE3 requires PKCα, which binds to E3KARP to decrease surface NHE3 containing plasma membrane complexes. Am. J. Physiol. Cell Physiol. 285, C1527-C1536
47. Coscoy, S., Waharte, F., Gautreau, A., Martin, M., Louvard, D., Mangeat, P., Arpin, M., and Amblard, F. (2002) Molecular analysis of microscopic ezrin dynamics by two-photon FRAP. Proc. Natl. Acad. Sci. U.S.A. 99, 12813-12818
48. Waharte, F., Brown, C. M., Coscoy, S., Coudrier, E., and Amblard, F. (2005) A two-photon FRAP analysis of the cytoskeleton dynamics in the microvilli of intestinal cells. Biophys. J. 88, 1467-1478 (Pubitemid 40975973)
49. Tyska, M. J., and Mooseker, M. S. (2002) MYO1A (brush border myosin I) dynamics in the brush border of LLC-PK1-CL4 cells. Biophys. J. 82, 1869-1883 (Pubitemid 34280803)
50. Weinman, E. J., Steplock, D., Cha, B., Kovbasnjuk, O., Frost, N. A., Cunningham, R., Shenolikar, S., Blanpied, T. A., and Donowitz, M. (2009) PTH transiently increases the percent mobile fraction of Npt2a in OK cells as determined by FRAP. Am. J. Physiol. Renal Physiol. 297, F1560-F1565
51. Cha, B., Tse, M., Yun, C., Kovbasnjuk, O., Mohan, S., Hubbard, A., Arpin, M., and Donowitz, M. (2006) The NHE3 juxtamembrane cytoplasmic domain directly binds ezrin: dual role in NHE3 trafficking and mobility in the brush border. Mol. Biol. Cell 17, 2661-2673 (Pubitemid 43825503)
52. + exchanger 3. J. Biol. Chem. 281, 1461-1469
53. + exchanger 3 (NHE3) requires an NHE3-E3KARP-α- actinin-4 complex for oligomerization and endocytosis. J. Biol. Chem. 277, 23714-23724
54. + exchanger 3 in murine intestine. J. Physiol. 588, 5049-5063
55. LaLonde, D. P., Garbett, D., and Bretscher, A. (2010) A regulated complex of the scaffolding proteins PDZK1 and EBP50 with ezrin contribute to microvillar organization. Mol. Biol. Cell 21, 1519-1529