Calcineurin-NFATc signaling pathway regulates AQP2 expression in response to calcium signals and osmotic stress

American Journal of Physiology - Cell Physiology

Volumn 292, Issue 5, 2007, Pages

  Li, Song Zhe ^a   McDill, Bradley W ^a   Kovach, Paul A ^a   Ding, Li ^a   Go, William Y ^b   Ho, Steffan N ^b,c   Chen, Feng ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BIOGEN   (United States)

Author keywords

Aquaporin; Nuclear factor of activated T cells; Osmotic response; Tonicity responsive enhancer binding protein

Indexed keywords

AQUAPORIN 2; BINDING PROTEIN; CALCINEURIN; CALCIUM; HYPERTONIC SOLUTION; NUCLEAR FACTOR; TONICITY RESPONSIVE ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT5; TRANSCRIPTION FACTOR REL; UNCLASSIFIED DRUG; AQP2 PROTEIN, MOUSE; IONOMYCIN; IONOPHORE; NFAT5 PROTEIN, MOUSE; NFATC1 PROTEIN, MOUSE; PHORBOL 13 ACETATE 12 MYRISTATE; SODIUM CHLORIDE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; GENE MUTATION; HYPEROSMOTIC STRESS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ACTIVE TRANSPORT; ANIMAL; CALCIUM SIGNALING; CELL LINE; CYTOLOGY; DRUG EFFECT; ELECTROLYTE BALANCE; EPITHELIUM CELL; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; KIDNEY COLLECTING TUBULE; METABOLISM; MOUSE MUTANT; MUTATION; OSMOSIS; PATHOPHYSIOLOGY; STRESS; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; AQUAPORIN 2; CALCINEURIN; CALCIUM SIGNALING; CELL LINE; EPITHELIAL CELLS; IONOMYCIN; IONOPHORES; KIDNEY TUBULES, COLLECTING; MICE; MICE, KNOCKOUT; MUTATION; NFATC TRANSCRIPTION FACTORS; OSMOSIS; PROMOTER REGIONS (GENETICS); SALINE SOLUTION, HYPERTONIC; SIGNAL TRANSDUCTION; STRESS; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION; WATER-ELECTROLYTE BALANCE;

EID: 34250615503     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00588.2005     Document Type: Article

References (45)

1. Abramowicz D, Wissing KM, Broeders N. Nephrotoxicity of calcineurin inhibitors: new therapeutic approaches. Transplant Proc 32: 3S-5S, 2000.
2. Akool el-S, Doller A, Muller R, Gutwein P, Xin C, Huwiler A, Pfeilschifter J, Eberhardt W. Nitric oxide induces TIMP-1 expression by activating the transforming growth factor beta-Smad signaling pathway. J Biol Chem 280: 39403-39416, 2005.
3. Brenner B, Rector F. The Kidney. Philadelphia, PA: Saunders, 2004.
4. Chang CP, McDill BW, Neilson JR, Joist HE, Epstein JA, Crabtree GR, Chen F. Calcineurin is required in urinary tract mesenchyme for the development of the pyeloureteral peristaltic machinery. J Clin Invest 113: 1051-1058, 2004.
5. Clipstone NA, Crabtree GR. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357: 695-697, 1992.
6. Crabtree GR, Olson EN. NFAT signaling: choreographing the social lives of cells. Cell 109, Suppl: S67-S79, 2002.
7. Dahl SC, Handler JS, Kwon HM. Hypertonicity-induced phosphorylation and nuclear localization of the transcription factor TonEBP. Am J Physiol Cell Physiol 280: C248-C253, 2001.
8. Dascalu A, Matithyou A, Oron Y, Korenstein R. A hyperosmotic stimulus elevates intracellular calcium and inhibits proliferation of a human keratinocyte cell line. J Invest Dermatol 115: 714-718, 2000.
9. Ferraris JD, Garcia-Perez A. Osmotically responsive genes: the mammalian osmotic response element (ORE). Am Zool 41: 734-742, 2001.
10. Ferraris JD, Williams CK, Ohtaka A, Garcia-Perez A. Functional consensus for mammalian osmotic response elements. Am J Physiol Cell Physiol 276: C667-C673, 1999.
11. Go WY, Liu X, Roti MA, Liu F, Ho SN. NFAT5/TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc Natl Acad Sci USA 101: 10673-10678, 2004.
12. Grinyo JM, Cruzado JM. Cyclosporine nephrotoxicity. Transplant Proc 36: 240S-242S, 2004.
13. Hasler U, Jeon US, Kim JA, Mordasini D, Kwon HM, Feraille E, Martin PY. Tonicity-responsive enhancer binding protein is an essential regulator of aquaporin-2 expression in renal collecting duct principal cells. J Am Soc Nephrol 17: 1521-1531, 2006.
14. Hasler U, Vinciguerra M, Vandewalle A, Martin PY, Feraille E. Dual effects of hypertonicity on aquaporin-2 expression in cultured renal collecting duct principal cells. J Am Soc Nephrol 16: 1571-1582, 2005.
15. Ho SN. Intracellular water homeostasis and the mammalian cellular osmotic stress response. J Cell Physiol 206: 9-15, 2005.
16. Ho SN. The role of NFAT5/TonEBP in establishing an optimal intracellular environment. Arch Biochem Biophys 413: 151-157, 2003.
17. Hogan PG, Chen L, Nardone J, Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17: 2205-2232, 2003.
18. Jenq W, Mathieson IM, Ihara W, Ramirez G. Aquaporin-1: an osmoinducible water channel in cultured mIMCD-3 cells. Biochem Biophys Res Commun 245: 804-809, 1998.
19. Jo I, Ward DT, Baum MA, Scott JD, Coghlan VM, Hammond TG, Harris HW. AQP2 is a substrate for endogenous PP2B activity within an inner medullary AKAP-signaling complex. Am J Physiol Renal Physiol 281: F958-F965, 2001.
20. Kasono K, Saito T, Saito T, Tamemoto H, Yanagidate C, Uchida S, Kawakami M, Sasaki S, Ishikawa SE. Hypertonicity regulates the aquaporin-2 promoter independently of arginine vasopressin. Nephrol Dial Transplant 20: 509-515, 2005.
21. King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5: 687-698, 2004.
22. Klee CB, Ren H, Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273: 13367-13370, 1998.
23. Knoers NV, Deen PM. Molecular and cellular defects in nephrogenic diabetes insipidus. Pediatr Nephrol 16: 1146-1152, 2001.
24. Krumschnabel G, Gstir R, Manzl C, Prem C, Pafundo D, Schwarzbaum PJ. Metabolic and ionic responses of trout hepatocytes to anisosmotic exposure. J Exp Biol 206: 1799-1808, 2003.
25. Lim SW, Li C, Sun BK, Han KH, Kim WY, Oh YW, Lee JU, Kador PF, Knepper MA, Sands JM, Kim J, Yang CW. Long-term treatment with cyclosporine decreases aquaporins and urea transporters in the rat kidney. Am J Physiol Renal Physiol 287: F139-F151, 2004.
26. Lopez-Rodriguez C, Antos CL, Shelton JM, Richardson JA, Lin F, Novobrantseva TI, Bronson RT, Igarashi P, Rao A, Olson EN. Loss of NFAT5 results in renal atrophy and lack of tonicity-responsive gene expression. Proc Natl Acad Sci USA 101: 2392-2397, 2004.
27. Lopez-Rodriguez C, Aramburu J, Jin L, Rakeman AS, Michino M, Rao A. Bridging the NFAT and NF-kappaB families: NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity 15: 47-58, 2001.
28. Lopez-Rodriguez C, Aramburu J, Rakeman AS, Copeland NG, Gilbert DJ, Thomas S, Disteche C, Jenkins NA, Rao A. NF-AT5: the NF-AT family of transcription factors expands in a new direction. Cold Spring Harb Symp Quant Biol 64: 517-526, 1999.
29. Lopez-Rodriguez C, Aramburu J, Rakeman AS, Rao A. NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc Natl Acad Sci USA 96: 7214-7219, 1999.
30. Matsuzaki T, Suzuki T, Takata K. Hypertonicity-induced expression of aquaporin 3 in MDCK cells. Am J Physiol Cell Physiol 281: C55-C63, 2001.
31. Miyakawa H, Rim JS, Handler JS, Kwon HM. Identification of the second tonicity-responsive enhancer for the betaine transporter (BGT1) gene. Biochim Biophys Acta 1446: 359-364, 1999.
32. Miyakawa H, Woo SK, Chen CP, Dahl SC, Handler JS, Kwon HM. Cis- and trans-acting factors regulating transcription of the BGT1 gene in response to hypertonicity. Am J Physiol Renal Physiol 274: F753-F761, 1998.
33. Miyakawa H, Woo SK, Dahl SC, Handler JS, Kwon HM. Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA 96: 2538-2542, 1999.
34. Myers BD, Ross J, Newton L, Luetscher J, Perlroth M. Cyclosporineassociated chronic nephropathy. N Engl J Med 311: 699-705, 1984.
35. Nielsen S, Frokiaer J, Marples D, Kwon TH, Agre P, Knepper MA. Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82: 205-244, 2002.
36. Paemeleire K, de Hemptinne A, Leybaert L. Chemically, mechanically, and hyperosmolarity-induced calcium responses of rat cortical capillary endothelial cells in culture. Exp Brain Res 126: 473-481, 1999.
37. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15: 707-747, 1997.
38. Sanchez JC, Wilkins RJ. Changes in intracellular calcium concentration in response to hypertonicity in bovine articular chondrocytes. Comp Biochem Physiol A 137: 173-182, 2004.
39. Shapiro L, Dinarello CA. Hyperosmotic stress as a stimulant for proin-flammatory cytokine production. Exp Cell Res 231: 354-362, 1997.
40. Shapiro L, Dinarello CA. Osmotic regulation of cytokine synthesis in vitro. Proc Natl Acad Sci USA 92: 12230-12234, 1995.
41. Sheikh-Hamad D, Nadkarni V, Choi YJ, Truong LD, Wideman C, Hodjati R, Gabbay KH. Cyclosporine A inhibits the adaptive responses to hypertonicity: a potential mechanism of nephrotoxicity. J Am Soc Nephrol 12: 2732-2741, 2001.
42. Storm R, Klussmann E, Geelhaar A, Rosenthal W, Maric K. Osmolality and solute composition are strong regulators of AQP2 expression in renal principal cells. Am J Physiol Renal Physiol 284: F189-F198, 2003.
43. Trama J, Lu Q, Hawley RG, Ho SN. The NFAT-related protein NFATL1 (TonEBP/NFAT5) is induced upon T cell activation in a calcineurin-dependent manner. J Immunol 165: 4884-4894, 2000.
44. Umenishi F, Yoshihara S, Narikiyo T, Schrier RW. Modulation of hypertonicity-induced aquaporin-1 by sodium chloride, urea, betaine, and heat shock in murine renal medullary cells. J Am Soc Nephrol 16: 600-607, 2005.
45. Vandewalle A. Immortalized renal proximal and collecting duct cell lines derived from transgenic mice harboring L-type pyruvate kinase promoters as tools for pharmacological and toxicological studies. Cell Biol Toxicol 18: 321-328, 2002.