Mutations that reduce its specific DNA binding inhibit high NaCl-induced nuclear localization of the osmoprotective transcription factor NFAT5

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 10, 2012, Pages

  Izumi, Yuichiro ^a   Li, Jinxi ^a   Villers, Courtney ^a   Hashimoto, Kosuke ^b   Burg, Maurice B ^a   Ferraris, Joan D ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

High NaCl; Leptomycin B; NUP88; XPO1

Indexed keywords

ALANINE; ASPARTIC ACID; EXPORTIN 1; NUCLEOPORIN; SODIUM CHLORIDE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NUCLEAR FACTOR OF ACTIVATED T CELL 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING; DNA RESPONSIVE ELEMENT; GENE MUTATION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REGULATORY MECHANISM;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE; DNA; GENE EXPRESSION REGULATION; HUMANS; KARYOPHERINS; MICE; MUTATION; OSMOTIC PRESSURE; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SODIUM CHLORIDE; TRANSCRIPTION FACTORS;

EID: 84869204418     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00265.2012     Document Type: Article

References (36)

1. Andres-Hernando A, Lanaspa MA, Rivard CJ, Berl T. Nucleoporin 88 (Nup88) is regulated by hypertonic stress in kidney cells to retain the transcription factor tonicity enhancer-binding protein (TonEBP) in the nucleus. J Biol Chem 283: 25082-25090, 2008.
2. Burg MB, Ferraris JD, Dmitrieva NI. Cellular response to hyperosmotic stresses. Physiol Rev 87: 1441-1474, 2007.
3. Eisenhaber B, Sammer M, Lua WH, Benetka W, Liew LL, Yu W, Lee HK, Koranda M, Eisenhaber F, Adhikari S. Nuclear import of a lipid-modified transcription factor: mobilization of NFAT5 isoform a by osmotic stress. Cell Cycle 10: 3897-3911, 2011.
4. Estrada-Gelonch A, Aramburu J, Lopez-Rodriguez C. Exclusion of NFAT5 from mitotic chromatin resets its nucleo-cytoplasmic distribution in interphase. PLos One 4: e7036, 2009.
5. Fagerlund R, Kinnunen L, Kohler M, Julkunen I, Melen K. NF-κB is transported into the nucleus by importin α3 and importin α4. J Biol Chem 280: 15942-15951, 2005.
6. Ferraris JD, Burg MB. Tonicity-regulated gene expression. Methods Enzymol 428: 279-296, 2007.
7. Ferraris JD, Williams CK, Jung KY, Bedford JJ, Burg MB, Garcia-Perez A. ORE, a eukaryotic minimal essential osmotic response element. The aldose reductase gene in hyperosmotic stress. J Biol Chem 271: 18318-18321, 1996.
8. Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051-1060, 1997.
9. Gallazzini M, Heussler GE, Kunin M, Izumi Y, Burg MB, Ferraris JD. High NaCl-induced activation of CDK5 increases phosphorylation of the osmoprotective transcription factor TonEBP/OREBP at threonine 135, which contributes to its rapid nuclear localization. Mol Biol Cell 22: 703-714, 2011.
10. Gallazzini M, Yu MJ, Gunaratne R, Burg MB, Ferraris JD. c-Abl mediates high NaCl-induced phosphorylation and activation of the transcription factor TonEBP/OREBP. FASEB J 24: 4325-4335, 2010.
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. Herrington J, Rui L, Luo G, Yu-Lee LY, Carter-Su C. A functional DNA binding domain is required for growth hormone-induced nuclear accumulation of Stat5B. J Biol Chem 274: 5138-5145, 1999.
13. Irarrazabal CE, Gallazzini M, Schnetz MP, Kunin M, Simons BL, Williams CK, Burg MB, Ferraris JD. Phospholipase C-g1 is involved in signaling the activation by high NaCl of the osmoprotective transcription factor TonEBP/OREBP. Proc Natl Acad Sci USA 107: 906-911, 2010.
14. Irarrazabal CE, Liu JC, Burg MB, Ferraris JD. ATM, a DNA damageinducible kinase, contributes to activation by high NaCl of the transcription factor TonEBP/OREBP. Proc Natl Acad Sci USA 101: 8809-8814, 2004
15. Irarrazabal CE, Williams CK, Ely MA, Birrer MJ, Garcia-Perez A, Burg MB, Ferraris JD. Activator protein-1 contributes to high NaClinduced increase in tonicity-responsive enhancer/osmotic response element-binding protein transactivating activity. J Biol Chem 283: 2554-2563, 2008.
16. Jans DA, Hubner S. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol Rev 76: 651-685, 1996.
17. Ko BC, Turck CW, Lee KW, Yang Y, Chung SS. Purification, identification, and characterization of an osmotic response element binding protein. Biochem Biophys Res Commun 270: 52-61, 2000.
18. Ko BCB, Ruepp B, Bohren KM, Gabbay KH, Chung SS. Identification and characterization of multiple osmotic response sequences in the human aldose reductase gene. J Biol Chem 272: 16431-16437, 1997.
19. Kwon MS, Lee SD, Kim JA, Colla E, Choi YJ, Suh PG, Kwon HM. Novel nuclear localization signal regulated by ambient tonicity in vertebrates. J Biol Chem 283: 22400-22409, 2008.
20. Lammers PE, Beck JA, Chu S, Kempson SA. Hypertonic upregulation of betaine transport in renal cells is blocked by a proteasome inhibitor. Cell Biochem Funct 23: 315-324, 2005.
21. 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.
22. McBride KM, McDonald C, Reich NC. Nuclear export signal located within theDNA-binding domain of the STAT1transcription factor. EMBO J 19: 6196-6206, 2000.
23. Melen K, Kinnunen L, Julkunen I. Arginine/lysine-rich structural element is involved in interferon-induced nuclear import of STATs. J Biol Chem 276: 16447-16455, 2001.
24. Miyakawa H, Woo SK, Dahl SC, Handler JS, Kwon HM. Tonicityresponsive enhancer binding protein, a Rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA 96: 2538-2542, 1999.
25. Neuhofer W. Role of NFAT5 in inflammatory disorders associated with osmotic stress. Curr Genomics 11: 584-590, 2010.
26. Obenauer JC, Cantley LC, Yaffe MB. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31: 3635-3641, 2003.
27. Ossareh-Nazari B, Bachelerie F, Dargemont C. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278: 141-144, 1997
28. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L. The FoldX web server: an online force field. Nucleic Acids Res 33: W382-W388, 2005.
29. Stroud JC, Lopez-Rodriguez C, Rao A, Chen L. Structure of a TonEBP-DNA complex reveals DNA encircled by a transcription factor. Nat Struct Biol 9: 90-94, 2002.
30. Tong EH, Guo JJ, Huang AL, Liu H, Hu CD, Chung SS, Ko BC. Regulation of nucleocytoplasmic trafficking of transcription factor OREBP/TonEBP/NFAT5. J Biol Chem 281: 23870-23879, 2006.
31. Tzivion G, Dobson M, Ramakrishnan G. FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta 1813: 1938-1945, 2011.
32. Woo SK, Dahl SC, Handler JS, Kwon HM. Bidirectional regulation of tonicity-responsive enhancer binding protein in response to changes in tonicity. Am J Physiol Renal Physiol 278: F1006-F1012, 2000.
33. Woo SK, Maouyo D, Handler JS, Kwon HM. Nuclear redistribution of tonicity-responsive enhancer binding protein requires proteasome activity. Am J Physiol Cell Physiol 278: C323-C330, 2000.
34. Xu SX, Wong CC, Tong EH, Chung SS, Yates JR III, Yin YB, Ko BC. Phosphorylation by casein kinase 1 regulates tonicity-induced OREBP/ TonEBP nucleocytoplasmic trafficking. J Biol Chem 283: 17624-17634, 2008
35. Zhang Z, Ferraris J, Irarrazabal CE, Dmitireva NI, Park JH, Burg MB. Ataxia-telangiectasia mutated (ATM), a DNA damage-inducible kinase, contributes to high NaCl-induced nuclear localization of the transcription factor TonEBP/OREBP. Am J Physiol Renal Physiol 289: F506-F511, 2005.
36. Zhou X, Gallazzini M, Burg MB, Ferraris JD. Contribution of SHP-1 protein tyrosine phosphatase to osmotic regulation of the transcription factor TonEBP/OREBP. Proc Natl Acad Sci USA 107: 7072-7077, 2010.