NHE3 Regulatory Factor 1 (NHERF1) modulates intestinal sodium-dependent phosphate transporter (NaPi-2b) expression in apical microvilli

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35047-35056

  Giral, Hector ^a   Cranston, DeeAnn ^a   Lanzano, Luca ^b   Caldas, Yupanqui ^a   Sutherland, Eileen ^a   Rachelson, Joanna ^d   Dobrinskikh, Evgenia ^a   Weinman, Edward J ^c   Doctor, R Brian ^a   Gratton, Enrico ^b   Levi, Moshe ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Veterans Affairs Eastern Colorado Health Care System   (United States)

^c University of California at Irvine   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINUS; CO-EXPRESSION; CO-IMMUNOPRECIPITATIONS; CO-PRECIPITATES; DIETARY P; ENTEROCYTES; FLIM-FRET; FOUR AMINO ACIDS; MICROVILLI; PDZ BINDING MOTIF; PDZ DOMAINS; PHOSPHATE TRANSPORTERS; REGULATORY FACTORS; SEQUENCE ANALYSIS; SMALL INTESTINE; TAGGED PROTEINS;

AMINO ACIDS; PROTEINS; SODIUM;

RATS;

GREEN FLUORESCENT PROTEIN; NHE3 REGULATORY FACTOR 1; PDZ DOMAIN CONTAINING PROTEIN IN KIDNEY 1; PDZ PROTEIN; PHOSPHATE; SODIUM PHOSPHATE COTRANSPORTER 2B; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL STRAIN CACO 2; CELL STRAIN HEK293; CONTROLLED STUDY; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; INTESTINE BRUSH BORDER; INTESTINE CELL; MALE; MICROSCOPY; MOUSE; NONHUMAN; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SMALL INTESTINE ABSORPTION;

ANIMALS; CACO-2 CELLS; CARRIER PROTEINS; ENTEROCYTES; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; MICROVILLI; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; SODIUM-HYDROGEN ANTIPORTER; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE IIB;

EID: 84867429642     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.392415     Document Type: Article

References (57)

1. Berndt, T., and Kumar, R. (2009) Novel mechanisms in the regulation of phosphorus homeostasis. Physiology 24, 17-25
2. Alizadeh Naderi, A. S., and Reilly, R. F. (2010) Hereditary disorders of renal phosphate wasting. Nat. Rev. Nephrol. 6, 657-665
3. Farrow, E. G., and White, K. E. (2010) Recent advances in renal phosphate handling. Nat. Rev. Nephrol. 6, 207-217
4. Tonelli, M., Sacks, F., Pfeffer, M., Gao, Z., and Curhan, G. (2005) Relation between serum phosphate level and cardiovascular event rate in people with coronary disease. Circulation 112, 2627-2633 (Pubitemid 41532599)
5. Dhingra, R., Sullivan, L. M., Fox, C. S., Wang, T. J., D'Agostino, R. B., Sr., Gaziano, J. M., and Vasan, R. S. (2007) Relations of serum phosphorus and calcium levels to the incidence of cardiovascular disease in the community. Arch. Intern. Med. 167, 879-885 (Pubitemid 46762749)
6. Shuto, E., Taketani, Y., Tanaka, R., Harada, N., Isshiki, M., Sato, M., Nashiki, K., Amo, K., Yamamoto, H., Higashi, Y., Nakaya, Y., and Takeda, E. (2009) Dietary phosphorus acutely impairs endothelial function. J. Am. Soc. Nephrol. 20, 1504-1512
7. Kempson, S. A., Lötscher, M., Kaissling, B., Biber, J., Murer, H., and Levi, M. (1995) Parathyroid hormone action on phosphate transporter mRNA and protein in rat renal proximal tubules. Am. J. Physiol. 268, F784-791
8. Segawa, H., Yamanaka, S., Onitsuka, A., Tomoe, Y., Kuwahata, M., Ito, M., Taketani, Y., and Miyamoto, K. (2007) Parathyroid hormone-dependent endocytosis of renal type IIc NaPi cotransporter. Am. J. Physiol. Renal Physiol. 292, F395-403 (Pubitemid 46105277)
9. Segawa, H., Kawakami, E., Kaneko, I., Kuwahata, M., Ito, M., Kusano, K., Saito, H., Fukushima, N., and Miyamoto, K. (2003) Effect of hydrolysis-resistant FGF23-R179Q on dietary phosphate regulation of the renal type-II Na/Pi transporter. Pflugers Arch. 446, 585-592 (Pubitemid 37070215)
10. Sabbagh, Y., O'Brien, S. P., Song, W., Boulanger, J. H., Stockmann, A., Arbeeny, C., and Schiavi, S. C. (2009) Intestinal npt2b plays a major role in phosphate absorption and homeostasis. J. Am. Soc. Nephrol. 20, 2348-2358
11. Marks, J., Srai, S. K., Biber, J., Murer, H., Unwin, R. J., and Debnam, E. S. (2006) Intestinal phosphate absorption and the effect of vitamin D. A comparison of rats with mice. Exp. Physiol. 91, 531-537
12. Giral, H., Caldas, Y., Sutherland, E., Wilson, P., Breusegem, S., Barry, N., Blaine, J., Jiang, T., Wang, X. X., and Levi, M. (2009) Regulation of rat intestinal sodium-dependent phosphate transporters by dietary phosphate. Am. J. Physiol. Renal Physiol 297, F1466-1475
13. i type IIb cotransporter by dietary phosphate intake. Am. J. Physiol. Gastrointest. Liver Physiol. 277, G756-762
14. Forster, I. C., Hernando, N., Biber, J., and Murer, H. (2006) Proximal tubular handling of phosphate. A molecular perspective. Kidney Int. 70, 1548-1559 (Pubitemid 44606989)
15. Miyamoto, K., Ito, M., Tatsumi, S., Kuwahata, M., and Segawa, H. (2007) New aspect of renal phosphate reabsorption. The type IIc sodium-dependent phosphate transporter. Am. J. Nephrol. 27, 503-515 (Pubitemid 47482008)
16. Nourry, C., Grant, S. G., and Borg, J. P. (2003) PDZ domain proteins. Plug and play! Sci. STKE 2003, RE7
17. Sugiura, T., Shimizu, T., Kijima, A., Minakata, S., and Kato, Y. (2011) PDZ adaptors. Their regulation of epithelial transporters and involvement in human diseases. J. Pharm. Sci. 100, 3620-3635
18. Lee, H. J., and Zheng, J. J. (2010) PDZ domains and their binding partners. Structure, specificity, and modification. Cell Commun. Signal. 8, 8
19. i cotransporter with PDZ proteins. J. Biol. Chem. 276, 9206-9213
20. Dobrinskikh, E., Giral, H., Caldas, Y. A., Levi, M., and Doctor, R. B. (2010) Shank2 redistributes with NaPilla during regulated endocytosis. Am. J. Physiol. Cell Physiol. 299, C1324-1334
21. i cotransporter at the apical membrane of proximal tubule cells. Am. J. Physiol. Cell Physiol. 289, C1042-1051
22. Villa-Bellosta, R., Barac-Nieto, M., Breusegem, S. Y., Barry, N. P., Levi, M., and Sorribas, V. (2008) Interactions of the growth-related, type IIc renal sodium/phosphate cotransporter with PDZ proteins. Kidney Int. 73, 456-464 (Pubitemid 351186289)
23. Giral, H., Lanzano, L., Caldas, Y., Blaine, J., Verlander, J. W., Lei, T., Gratton, E., and Levi, M. (2011) Role of PDZK1 protein in apical membrane expression of renal sodium-coupled phosphate transporters. J. Biol. Chem. 286, 15032-15042
24. Shenolikar, S., Voltz, J. W., Minkoff, C. M., Wade, J. B., and Weinman, E. J. (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. U.S.A. 99, 11470-11475 (Pubitemid 34920949)
25. i-IIa in a mouse model deficient for the PDZ protein PDZK1. Pflugers Arch. 449, 392-402
26. Lan, D., and Silver, D. L. (2005) Fenofibrate induces a novel degradation pathway for scavenger receptor B-I independent of PDZK1. J. Biol. Chem. 280, 23390-23396 (Pubitemid 40853253)
27. Caldas, Y. A., Giral, H., Cortazar, M. A., Sutherland, E., Okamura, K., Blaine, J., Sorribas, V., Koepsell, H., and Levi, M. (2011) Liver X receptor-activating ligands modulate renal and intestinal sodium-phosphate transporters. Kidney Int. 80, 535-544
28. Peterson, M. D., and Mooseker, M. S. (1992) Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J. Cell Sci. 102, 581-600
29. Colyer, R. A., Lee, C., and Gratton, E. (2008) A novel fluorescence lifetime imaging system that optimizes photon efficiency. Microsc. Res. Tech. 71, 201-213 (Pubitemid 351374447)
30. + exchanger 3 (NHE3) activity in NHE regulatory factor 1 (NHERF1) adaptor protein-deficient mice. Pflugers Arch. 457, 1079-1091
31. Redford, G. I., and Clegg, R. M. (2005) Polar plot representation for frequency-domain analysis of fluorescence lifetimes. J. Fluoresc. 15, 805-815 (Pubitemid 41795606)
32. Lanzano, L., Digman, M. A., Fwu, P., Giral, H., Levi, M., and Gratton, E. (2011) Nanometer-scale imaging by the modulation tracking method. J. Biophotonics 4, 415-424
33. Lamprecht, G., and Seidler, U. E. (1998) The emerging role of PDZ adapter proteins for regulation of intestinal ion transport. J. Biol. Chem. 273, 29972-29978
34. + pump activity. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G909-919
35. Zachos, N. C., Li, X., Kovbasnjuk, O., Hogema, B., Sarker, R., Lee, L. J., Li, M., de Jonge, H., and Donowitz, M. (2009) NHERF3 (PDZK1) contributes to basal and calcium inhibition of NHE3 activity in Caco-2BBe cells. J. Biol. Chem. 284, 23708-23718
36. + exchange regulatory factor 2-dependent process. Gastroenterology 140, 560-571
37. Fujiya, M., Inaba, Y., Musch, M. W., Hu, S., Kohgo, Y., and Chang, E. B. (2011) Cytokine regulation of OCTN2 expression and activity in small and large intestine. Inflamm. Bowel Dis. 17, 907-916
38. Peterson, M. D., Bement, W. M., and Mooseker, M. S. (1993) An in vitro model for the analysis of intestinal brush border assembly. II. Changes in expression and localization of brush border proteins during cell contact-induced brush-border assembly in Caco-2BBe cells. J. Cell Sci. 105, 461-472 (Pubitemid 23234164)
39. Peterson, M. D., and Mooseker, M. S. (1993) An in vitro model for the analysis of intestinal brush-border assembly. I. Ultrastructural analysis of cell contact-induced brush-border assembly in Caco-2BBe cells. J. Cell Sci. 105, 445-460 (Pubitemid 23234163)
40. Digman, M. A., Caiolfa, V. R., Zamai, M., and Gratton, E. (2008) The phasor approach to fluorescence lifetime imaging analysis. Biophys. J. 94, L14-16
41. i cotransporters in vitamin D receptor- and 1αOHase-deficient mice. Am. J. Physiol. Cell Physiol. 288, C429-434
42. Hung, A. Y., and Sheng, M. (2002) PDZ domains. Structural modules for protein complex assembly. J. Biol. Chem. 277, 5699-5702 (Pubitemid 34968344)
43. + exchanger requires a dissociable phosphoprotein cofactor. J. Clin. Invest. 92, 1781-1786
44. 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 (Pubitemid 27444089)
45. + exchanger. J. Clin. Invest. 95, 2143-2149
46. + exchanger regulatory factor family of PDZ proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 8496-8501
47. Hegedüs, T., Sessler, T., Scott, R., Thelin, W., Bakos, E., Váradi, A., Szabó, K., Homolya, L., Milgram, S. L., and Sarkadi, B. (2003) C-terminal phosphorylation of MRP2 modulates its interaction with PDZ proteins. Biochem. Biophys. Res. Commun. 302, 454-461 (Pubitemid 36279550)
48. Weinman, E. J., Boddeti, A., Cunningham, R., Akom, M., Wang, F., Wang, Y., Liu, J., Steplock, D., Shenolikar, S., and Wade, J. B. (2003) NHERF-1 is required for renal adaptation to a low-phosphate diet. Am. J. Physiol. Renal Physiol. 285, F1225-1232 (Pubitemid 37421058)
49. Biber, J., Gisler, S. M., Hernando, N., and Murer, H. (2005) Protein/protein interactions (PDZ) in proximal tubules. J. Membr. Biol. 203, 111-118 (Pubitemid 40933559)
50. Hilfiker, H., Hattenhauer, O., Traebert, M., Forster, I., Murer, H., and Biber, J. (1998) Characterization of a murine type II sodium-phosphate cotransporter expressed in mammalian small intestine. Proc. Natl. Acad. Sci. U.S.A. 95, 14564-14569 (Pubitemid 28549407)
51. +/phosphate cotransport and cotransporter gene expression. J. Clin. Invest. 104, 679-686
52. Ohkido, I., Segawa, H., Yanagida, R., Nakamura, M., and Miyamoto, K. (2003) Cloning, gene structure, and dietary regulation of the type-IIc Na/Pi cotransporter in the mouse kidney. Pflugers Arch. 446, 106-115 (Pubitemid 36539539)
53. Lanaspa, M. A., Giral, H., Breusegem, S. Y., Halaihel, N., Baile, G., Catalán, J., Carrodeguas, J. A., Barry, N. P., Levi, M., and Sorribas, V. (2007) Interaction of MAP17 with NHERF3/4 induces translocation of the renal Na/Pi IIa transporter to the trans-Golgi. Am. J. Physiol. Renal Physiol. 292, F230-242 (Pubitemid 46105263)
54. Sugiura, T., Kato, Y., Wakayama, T., Silver, D. L., Kubo, Y., Iseki, S., and Tsuji, A. (2008) PDZK1 regulates two intestinal solute carriers (Slc15a1 and Slc22a5) in mice. Drug Metab. Dispos. 36, 1181-1188 (Pubitemid 351717477)
55. Singh, A. K., Riederer, B., Krabbenhoft, A., Rausch, B., Bonhagen, J., Lehmann, U., de Jonge, H. R., Donowitz, M., Yun, C., Weinman, E. J., Kocher, O., Hogema, B. M., and Seidler, U. (2009) Differential roles of NHERF1, NHERF2, and PDZK1 in regulating CFTR-mediated intestinal anion secretion in mice. J. Clin. Invest. 119, 540-550
56. + exchanger 3 regulatory factor 1 (NHERF-1)- but not NHERF-2-deficient mice. J. Biol. Chem. 282, 37575-37584
57. Donowitz, M., Singh, S., Singh, P., Salahuddin, F. F., Chen, Y., Chakraborty, M., Murtazina, R., Gucek, M., Cole, R. N., Zachos, N. C., Kovbasnjuk, O., Broere, N., Smalley-Freed, W. G., Reynolds, A. B., Hubbard, A. L., Seidler, U., Weinman, E., de Jonge, H. R., Hogema, B. M., and Li, X. (2010) Alterations in the proteome of the NHERF1 knockout mouse jejunal brush-border membrane vesicles. Physiol. Genomics 42A, 200-210