TonEBP stimulates multiple cellular pathways for adaptation to hypertonic stress: Organic osmolyte-dependent and -independent pathways

American Journal of Physiology - Renal Physiology

Volumn 300, Issue 3, 2011, Pages

  do Lee, Sang ^a,b   Youn Choi, Soo ^a   Woo Lim, Sun ^a   Todd Lamitina, S ^c   Ho, Steffan N ^d   Go, William Y ^d   Moo Kwon, H ^a  

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

^b Chungnam National University   (South Korea)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Asporin; Heat shock protein 70; Insulin like growth factor binding proteins; Lysophosphophatase D; Tonicity responsive enhancer binding protein

Indexed keywords

HEAT SHOCK PROTEIN 70; LYSOPHOSPHOLIPASE; SOMATOMEDIN BINDING PROTEIN 5; TONICITY RESPONSIVE ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL CELL; ARTICLE; EMBRYO; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; HYPEROSMOTIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

EID: 79954480118     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00227.2010     Document Type: Article

References (37)

1. Alfieri RR, Petronini PG, Bonelli MA, Desenzani S, Cavazzoni A, Borghetti AF, Wheeler KP. Roles of compaible osmolytes and heat shock protein 70 in the induction of tolerance to stresses in porcine endothelial cells. J Physiol 555.3: 757-767, 2004.
2. Aoki J, Taira A, Takenezawa Y, Kishi Y, Hama K, Kishimoto T, Mizuno K, Saku K, Taguchi R, Arai H. Serum lysophosphatitic acid is produced through diverse phospholiase pathways. J Biol Chem 277: 48734-48744, 2002.
3. Ashizawa N, Yoshida M, Aotsuka T. An enzymatic assay for myo-inositol in tissue samples. J Biochem Biophys Methods 44: 89-94, 2000.
4. Beck FX, Burger-Kentischer A, Müller E. Cellular response to osmotic stress in the renal medulla. Pflügers Arch Eur J Physiol 436: 814-827, 1998.
5. Burg M, Ferraris J, Dmitrieva N. Cellular response to hypertonic stress. Physiol Rev 87: 1441-1474, 2007.
6. Cai Q, Ferraris JD, Burg MB. Greater tolerance of renal medullary cells for a slow increse in osmolality is associated with enhanced expression of Hsp70 and other osmoprotective genes. Am J Physiol Renal Physiol 286: F58-F67, 2004.
7. Cai Q, Michea L, Andrews P, Zhang Z, Rocha G, Dmitrieva N, Burg MB. Rate of increase of osmolality determiens osmotic tolerance of mouse inner medullary epithelial cells. Am J Physiol Renal Physiol 283: F792-F798, 2002.
8. Cha JH, Woo SK, Han KH, Kim YH, Handler JS, Kim J, Kwon HM. Hydration status affects nuclear distribution of transcription factor tonicity responsive enhancer binding protein in rat kidney. J Am Soc Nephrol 12: 2221-2230, 2001.
9. Chen S, Grigsby CL, Law CS, Ni X, Nekrep N, Olsen K, Humphreys MH, Gardner DG. Tonicity-dependent induction of Sgk1 expression has a potential role in dehydration-induced natriuresis in rodents. J Clin Invest 119:1647-1658, 2009.
10. Foghsgaard L, Sissing D, Mauch D, Lademann U, Bastholm L, Boes M, Elling F, Leist M, Jäättelä M. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 153: 999-1009, 1999.
11. Garcia-Perez A, Burg MB. Renal medullary organic osmolytes. Physiol Rev 71: 1081-1115, 1991.
12. Go WY, Liu Z, Roti MA, Liu F, Ho SN. NFAT5/TonEBP mutant mice define osmotic stress a critical feature of the lymphoid microenviornment. Proc Natl Acad Sci USA 101: 10673-10678, 2004.
13. Kizawa H, Kou I, Iida A, Sudo A, Miyamoto Y, Fukuda A, Mabuchi A, Kotani A, Kawakami A, Yamamoto S, Uchida A, Nakamura K, Notoya K, Nakamura Y, Ikegawa S. An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat Genet 37: 138-144, 2005.
14. Klokkers J, Langehanenberg P, Kemper B, Kosmeier S, von Bally G, Riethmuller C, Wunder F, Sindie A, Ravenstadt H, Schlatter E, Edemir B. Atrial natriuretic peptide and nitric oxide signaling antagonizes vasporessin-mediated water permeability in inner medullary collecting duct cells. Am J Physiol Renal Physiol 297: F693-F703, 2009.
15. Kwon MS, Lim SW, Kwon HM. Hypertonic stress in the kidney: a necessary evil. Physiology 24: 186-191, 2009.
16. Kwon MS, Na KY, Moeckel G, Lee SD, Kwon HM. Urea promotes TonEBP expression and cellular adaptation to extreme hypertonicity. Pflügers Arch Eur J Physiol 459: 183-189, 2009.
17. Lam AKM, Ko BCB, Tam S, Morris R, Yang JY, Chung SK, Chung SSM. Osmotic response element-binding protein is an essential regulator of the urine conentrating mechanism. J Biol Chem 279: 48048-48054, 2004.
18. Lamitina T, Huan CG, Strange K. Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression. Proc Natl Acad Sci USA 103: 12173-12178, 2006.
19. Lee JS, Lee JJ, Seo JS. Hsp70 deficiency results in activation of JNK, ERK, and caspase-3 in hyperosmolality-induced apoptosis. J Biol Chem 280: 6634-6641, 2005.
20. López-Rodríguez 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.
21. Mehlen P, Kretz-Remy C, Preville X, Arrigo AP. Human Hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective acitivity of these proteins agains TNFalpha-induced cell death. EMBO J 15:2695-2706, 1996.
22. Michl M, Ouyang N, Fraek ML, Beck FX, Neuhofer W. Expression and regulation of alphaB-crystallin in the kidney in vivo and in vitro. Pflügers Arch Eur J Physiol 452: 387-395, 2006.
23. Mills GB, Moolenaar WH. The emerging role of lysophosphoatidic acid in cancer. Nature Rev 3:582-591, 2003.
24. Miyakoshi N, Richman C, Kasukawa Y, Linkhart TA, Baylink DJ, Mohan S. Evidence for IGF-binding protein-5 as a growth factor. J Clin Invest 107:73-81, 2001.
25. Nakajima M, Kizawa H, Saitoh M, Kou I, Miyazono K, Ikegawas S. Mechanisms for asporin function and regulation in articular cartilage. J Biol Chem 282: 32185-32192, 2007.
26. Nylandsted J, Jäättelä M, Hoffmann EK, Pedersen SF. Heat shock protein 70 inhibits shrinkage-induced programmed cell death via mechanisms independent of effects on cell volume-regulatory membrane transport proteins. Pflügers Arch Eur J Physiol 449: 175-185, 2004.
27. Ousman SS, Tomooka BH, va Noort JM, Wawrousek ER, O'Connor KC, Hafler DA, Sobel RA, Robinson WH, Steinman L. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448: 474-479, 2007.
28. Rohlfing AK, Miteva Y, Hannenhalli S, Lamitina T. Genetic and physiological activation of osmosensitive gene expression mimics tran-scriptional signatures of pathogen infection in C. elegans PLoS ONE 5(2): e9010, 2010.
29. Salih DAM, Tripathi G, Holding C, Szestak TAM, Gonzalez MI, Carter EJ, Cobb LJ, Esenmann JE, Pell JM. Insulin-like growth factor-binding protein 5 compromises cell survival, growth, muscle development, and fertility in mice. Proc Natl Acad Sci USA 101: 4314-4319, 2004.
30. Sheen MR, Kim JA, Lim SW, Jung JY, Han KH, Jeon US, Park SH, Kim J, Kwon HM. Interstitial tonicity controls TonEBP expression in the renal medulla. Kidney Int 75: 518-525, 2009.
31. Shim EH, Kim JI, Band ES, Heon JS, Lee JS, Kim EY, Lee JE, Park WY, Kim SH, Kim HS, Smithies O, Jang JJ, Jin DI, Seon JS. Targeted disruption of hsp70.1 sensitizes to osmotic stress. EMBP Reports 3: 857-861, 2002.
32. Terada Y, Inoshita S, Hanada S, Shimamura H, Kuwahara M, Ogawa W, Kasuga M, Sasaki S, Marumo F. Hyperosmolality activates Akt and regulates apoptosis inrenal tubular cells. Kidney Int 60: 553-567, 2000.
33. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. Onco-genic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132:363-374, 2008.
34. Woo SK, Lee SD, Na KY, Park WK, Kwon HM. TonEBP/NFAT5 stimulates transcription of HSP70 in response to hypertonicity. Mol Cell Biol 22: 5753-5760, 2002.
35. Yamauchi A, Uchida S, Kwon HM, Preston AS, Robey RB, Garcia-Perez A, Burg MB, Handler JS. Cloning of a Na- and Cl-dependent betaine transporter that is regulated by hypertonicity. J Biol Chem 267: 649-652, 1992.
36. Zhang Z, Cai Q, Michea L, Dmitrieva NI, Andrews P, Burg MB. Proliferation and osmotic tolerance of renal inner medullary epithelial cells in vivo and in cell culture. Am J Physiol Renal Physiol 283: F302-F308, 2002.
37. Zhu Y, Bogomolovas J, Labelt S, Granzier H. Single molecule force spectroscopy of the cardiac titin N2B element: effects of the moleular chaperone alphaB-crystallin with disease-causing mutations. J Biol Chem 284: 13914-13923, 2009.