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Hyperosmotic stress response: comparison with other cellular stresses

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Abstract

Cellular responses induced by stress are essential for the survival of cells under adverse conditions. These responses, resulting in cell adaptation to the stress, are accomplished by a variety of processes at the molecular level. After an alteration in homeostatic conditions, intracellular signalling processes link the sensing mechanism to adaptive or compensatory changes in gene expression. The ability of cells to adapt to hyperosmotic stress involves early responses in which ions move across cell membranes and late responses characterized by increased synthesis of either membrane transporters essential for uptake of organic osmolytes or of enzymes involved in their synthesis. The goal of these responses is to return the cell to its normal size and maintain cellular homeostasis. The enhanced synthesis of molecular chaperones, such as heat shock proteins, is another important component of the adaptive process that contributes to cell survival. Some responses are common to different stresses, whereas others are specific. In the first part of the review, we illustrate the characteristic and specific features of adaptive response to hypertonicity; we then describe similarities to and differences from other cellular stresses, such as genotoxic agents, nutrient starvation and heat shock.

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References

  1. Abcouwer SF, Schwarz C, Meguid RA (1999) Glutamine deprivation induces the expression of GADD45 and GADD153 primarily by mRNA stabilization. J Biol Chem 274:28645–28651

    PubMed  CAS  Google Scholar 

  2. Akar F, Jiang G, Paul RJ, O’Neill WC (2001) Contractile regulation of the Na(+)–K(+)–2Cl(−) cotransporter in vascular smooth muscle. Am J Physiol 281:C579–C584

    CAS  Google Scholar 

  3. Alfieri R, Petronini PG, Urbani S, Borghetti AF (1996) Activation of heat-shock transcription factor 1 by hypertonic shock in 3T3 cells. Biochem J 319:601–606

    PubMed  CAS  Google Scholar 

  4. Alfieri RR, Petronini PG, Bonelli MA, Caccamo AE, Cavazzoni A, Borghetti AF, Wheeler KP (2001) Osmotic regulation of ATA2 mRNA expression and amino acid transport system A activity. Biochem Biophys Res Commun 283:174–178

    PubMed  CAS  Google Scholar 

  5. Alfieri RR, Cavazzoni A, Petronini PG, Bonelli MA, Caccamo AE, Borghetti AF, Wheeler KP (2002) Compatible osmolytes modulate the responses of porcine endothelial cells to hypertonicity and protect them from apoptosis. J Physiol 540:499–508

    PubMed  CAS  Google Scholar 

  6. Alfieri RR, Bonelli MA, Petronini PG, Borghetti AF (2002) Stabilization of hsp70 mRNA on prolonged cell exposure to hypertonicity. Biochim Biophys Acta 1592:135–140

    PubMed  CAS  Google Scholar 

  7. Alfieri RR, Petronini PG, Bonelli MA, Desenzani S, Cavazzoni A, Borghetti AF, Wheeler KP (2004) Roles of compatible osmolytes and heat shock protein 70 in the induction of tolerance to stresses in porcine endothelial cells. J Physiol 555:757–767

    PubMed  CAS  Google Scholar 

  8. Alfieri RR, Bonelli MA, Petronini PG, Desenzani S, Cavazzoni A, Borghetti AF, Wheeler KP (2005) Hypertonic stress and amino acid deprivation both increase expression of mRNA for amino acid transport system A. J Gen Physiol 125:37–39

    PubMed  CAS  Google Scholar 

  9. Alfieri RR, Bonelli MA, Cavazzoni A, Brigotti M, Fumarola C, Sestili P, Mozzoni P, De Palma G, Mutti A, Carnicelli D, Vacondio F, Silva C, Borghetti AF, Wheeler KP, Petronini PG (2006) Creatine as a compatible osmolyte in muscle cells exposed to hypertonic stress. J Physiol 576:391–401

    PubMed  CAS  Google Scholar 

  10. Alfieri RR, Bonelli MA, Pedrazzi G, Desenzani S, Ghillani M, Fumarola C, Ghibelli L, Borghetti AF, Petronini PG (2006) Increased levels of inducible HSP70 in cells exposed to electromagnetic fields. Radiat Res 165:95–104

    PubMed  CAS  Google Scholar 

  11. Anselmo AN, Earnest S, Chen W, Juang YC, Kim SC, Zhao Y, Cobb MH (2006) WNK1 and OSR1 regulate the Na+, K+, 2Cl− cotransporter in HeLa cells. Proc Natl Acad Sci USA 103:10883–10888

    PubMed  CAS  Google Scholar 

  12. Aramburu J, Drews-Elger K, Estrada-Gelonch A, Minguillon J, Morancho B, Santiago V, Lopez-Rodriguez C (2006) Regulation of the hypertonic stress response and other cellular functions by the Rel-like transcription factor NFAT5. Biochem Pharmacol 72(11):1597–1604

    PubMed  CAS  Google Scholar 

  13. Bader SB, Price BD, Mannheim-Rodman LA, Calderwood SK (1992) Inhibition of heat shock gene expression does not block the development of thermotolerance. J Cell Physiol 151:56–62

    PubMed  CAS  Google Scholar 

  14. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499–506

    PubMed  CAS  Google Scholar 

  15. Barbe MF, Tytell M, Gower DJ, Welch WJ (1988) Hyperthermia protects against light damage in the rat retina. Science 241:1817–1820

    PubMed  CAS  Google Scholar 

  16. Beck FX, Grunbein R, Lugmayr K, Neuhofer W (2000) Heat shock proteins and the cellular response to osmotic stress. Cell Physiol Biochem 10:303–306

    PubMed  CAS  Google Scholar 

  17. Beck FX, Neuhofer W (2005) Response of renal medullary cells to osmotic stress. Contrib Nephrol 148:21–34

    PubMed  Google Scholar 

  18. Bevilacqua E, Bussolati O, Dall’Asta V, Gaccioli F, Sala R, Gazzola GC, Franchi-Gazzola R (2005) SNAT2 silencing prevents the osmotic induction of transport system A and hinders cell recovery from hypertonic stress. FEBS Lett 579:3376–3380

    PubMed  CAS  Google Scholar 

  19. Bharadwaj S, Ali A, Ovsenek N (1999) Multiple components of the HSP90 chaperone complex function in regulation of heat shock factor 1 in vivo. Mol Cell Biol 19:8033–8041

    PubMed  CAS  Google Scholar 

  20. Bortner CD, Cidlowski JA (1996) Absence of volume regulatory mechanisms contributes to the rapid activation of apoptosis in thymocytes. Am J Physiol 271:C950–C961

    PubMed  CAS  Google Scholar 

  21. Bortner CD, Cidlowski JA (1998) A necessary role for cell shrinkage in apoptosis. Biochem Pharmacol 56:1549–1559

    PubMed  CAS  Google Scholar 

  22. Brigotti M, Petronini PG, Carnicelli D, Alfieri RR, Bonelli MA, Borghetti AF, Wheeler KP (2003) Effects of osmolarity, ions and compatible osmolytes on cell-free protein synthesis. Biochem J 369:369–374

    PubMed  CAS  Google Scholar 

  23. Bruhat A, Jousse C, Wang XZ, Ron D, Ferrara M, Fafournoux P (1997) Amino acid limitation induces expression of CHOP, a CCAAT/enhancer binding protein-related gene, at both transcriptional and post-transcriptional levels. J Biol Chem 272:17588–17593

    PubMed  CAS  Google Scholar 

  24. Bulavin DV, Higashimoto Y, Popoff IJ, Gaarde WA, Basrur V, Potapova O, Appella E, Fornace AJ Jr (2001) Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411:102–107

    PubMed  CAS  Google Scholar 

  25. Burg MB (1995) Molecular basis of osmotic regulation. Am J Physiol 268:F983–F996

    PubMed  CAS  Google Scholar 

  26. Burg MB, Kwon HM, Kultz D (1997) Regulation of gene expression by hypertonicity. Ann Rev Physiol 59:437–455

    CAS  Google Scholar 

  27. Bussolati O, Dall’Asta V, Franchi-Gazzola R, Sala R, Rotoli BM, Visigalli R, Casado J, Lopez-Fontanals M, Pastor-Anglada M, Gazzola GC (2001) The role of system A for neutral amino acid transport in the regulation of cell volume. Mol Membr Biol 18:27–38

    PubMed  CAS  Google Scholar 

  28. Cai Q, Michea L, Andrews P, Zhang Z, Rocha G, Dmitrieva N, Burg MB (2002) Rate of increase of osmolarity determines osmotic tolerance of mouse inner medullary epithelial cells. Am J Physiol 283:F792–F798

    Google Scholar 

  29. Cai Q, Ferraris JD, Burg MB (2004) Greater tolerance of renal medullary cells for a slow increase in osmolality is associated with enhanced expression of HSP70 and other osmoprotective genes. Am J Physiol 286:F58–F67

    CAS  Google Scholar 

  30. Cai Q, Ferraris JD, Burg MB (2005) High NaCl increases TonEBP/OREBP mRNA and protein by stabilizing its mRNA. Am J Physiol 289:F803–F807

    CAS  Google Scholar 

  31. Cai Q, Dmitrieva NI, Ferraris JD, Michea LF, Salvador JM, Hollander MC, Fornace AJ Jr, Fenton RA, Burg MB (2006) Effects of expression of p53 and Gadd45 on osmotic tolerance of renal inner medullary cells. Am J Physiol 291:F341–F349

    CAS  Google Scholar 

  32. Caruccio L, Bae S, Liu AY-C, Chen KY (1997) The heat-shock transcription factor HSF1 is rapidly activated by either hyper- or hypoosmotic stress in mammalian cells. Biochem J 327:341–347

    PubMed  CAS  Google Scholar 

  33. Cohen DM, Wasserman JC, Gullans SR (1991) Immediate early gene and HSP70 expression in hyperosmotic stress in MDCK cells. Am J Physiol 261:C594–C601

    PubMed  CAS  Google Scholar 

  34. Cohen DM (2005) SRC family in cell volume regulation. Am J Physiol 288:C483–C493

    CAS  Google Scholar 

  35. Colla E, Lee SD, Sheen MR, Woo SK, Kwon HM (2006) TonEBP is inhibited by RNA helicase A via interaction involving the E’F loop. Biochem J 3931:411–419

    Google Scholar 

  36. Copp J, Wiley S, Ward MW, van der Geer P (2005) Hypertonic shock inhibits growth factor receptor signaling, induces caspase-3 activation, and causes reversible fragmentation of the mitochondrial network. Am J Physiol 288:C403–C415

    CAS  Google Scholar 

  37. Dahl SC, Handler JS, Kwon HM (2001) Hypertonicity-induced phosphorylation and nuclear localization of the transcription factor TonEBP. Am J Physiol 280:C248–C253

    CAS  Google Scholar 

  38. Dall’Asta V, Rossi PA, Bussolati O, Gazzola GC (1994) Response of human fibroblasts to hypertonic stress. Cell shrinkage is counteracted by an enhanced active transport of neutral amino acids. J Biol Chem 269:10485–10491

    PubMed  CAS  Google Scholar 

  39. De Angelis E, Petronini PG, Borghetti P, Borghetti AF, Wheeler KP (1999) Induction of betaine-γ-aminobutyric acid transport activity in porcine chondrocytes exposed to hypertonicity. J Physiol 518:187–194

    PubMed  Google Scholar 

  40. Denkert C, Warskulat U, Hensel F, Haussinger D (1998) Osmolyte strategy in human monocytes and macrophages: involvement of p38MAPK in hyperosmotic induction of betaine and myo-inositol transporters. Arch Biochem Biophys 354:172–180

    PubMed  CAS  Google Scholar 

  41. Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    PubMed  CAS  Google Scholar 

  42. Di Ciano-Oliveira C, Sirokmany G, Szaszi K, Arthur WT, Masszi A, Peterson M, Rotstein OD, Kapus A (2003) Hyperosmotic stress activates Rho: differential involvement in Rho kinase-dependent MLC phosphorylation and NKCC activation. Am J Physiol 285:C555–C566

    Google Scholar 

  43. Di Ciano-Oliveira C, Lodyga M, Fan L, Szaszi K, Hosoya H, Rotstein OD, Kapus A (2005) Is myosin light-chain phosphorylation a regulatory signal for the osmotic activation of the Na+–K+–2Cl− cotransporter? Am J Physiol 289:C68–C81

    Google Scholar 

  44. Di Ciano-Oliveira C, Thirone AC, Szaszi K, Kapus A (2006) Osmotic stress and the cytoskeleton: the R(h)ole of Rho GTPases. Acta Physiol 187:257–272

    Google Scholar 

  45. Didelot C, Schmitt E, Brunet M, Maingret L, Parcellier A, Garrido C (2006) Heat shock proteins: endogenous modulators of apoptotic cell death. Handb Exp Pharmacol 172:171–198

    Article  PubMed  CAS  Google Scholar 

  46. Dmitrieva N, Kultz D, Michea L, Ferraris J, Burg MB (2000) Protection of renal inner medullary epithelial cells from apoptosis by hypertonic stress-induced p53 activation. J Biol Chem 275:18243–18247

    PubMed  CAS  Google Scholar 

  47. Dmitrieva NI, Michea L, Burg MB (2001) p53 protects renal inner medullary cells from hypertonic stress by restricting DNA replication. Am J Physiol 281:F522–F530

    CAS  Google Scholar 

  48. Dmitrieva NI, Bulavin DV, Fornace AJ Jr, Burg MB (2002) Rapid activation of G2/M checkpoint after hypertonic stress in renal inner medullary epithelial (IME) cells is protective and requires p38 kinase. Proc Natl Acad Sci USA 99:184–189

    PubMed  CAS  Google Scholar 

  49. Dmitrieva NI, Bulavin DV, Burg MB (2003) High NaCl causes Mre11 to leave the nucleus, disrupting DNA damage signaling and repair. Am J Physiol 285:F266–F274

    CAS  Google Scholar 

  50. Dmitrieva NI, Cai Q, Burg MB (2004) Cells adapted to high NaCl have many DNA breaks and impaired DNA repair both in cell culture and in vivo. Proc Natl Acad Sci USA 101:2317–2322

    PubMed  CAS  Google Scholar 

  51. Dmitrieva NI, Burg MB (2005) Hypertonic stress response. Mutat Res 569:65–74

    PubMed  CAS  Google Scholar 

  52. Dmitrieva NI, Celeste A, Nussenzweig A, Burg MB (2005) Ku86 preserves chromatin integrity in cells adapted to high NaCl. Proc Natl Acad Sci USA 102:10730–10735

    PubMed  CAS  Google Scholar 

  53. Dowd BF, Forbush B (2003) PASK (proline-alanine-rich STE20-related kinase), a regulatory kinase of the Na–K–Cl cotransporter (NKCC1). J Biol Chem 278:27347–27353

    PubMed  CAS  Google Scholar 

  54. Franchi-Gazzola R, Visigalli R, Bussolati O, Dall’Asta V, Gazzola GC (1999) Adaptive increase of amino acid transport system A requires ERK1/2 activation. J Biol Chem 274:28922–28928

    PubMed  CAS  Google Scholar 

  55. Franchi-Gazzola R, Visigalli R, Dall’Asta V, Sala R, Woo SK, Kwon HM, Gazzola GC, Bussolati O (2001) Amino acid depletion activates TonEBP and sodium-coupled inositol transport. Am J Physiol 280:C1465–C1474

    CAS  Google Scholar 

  56. Franchi-Gazzola R, Sala R, Bussolati O, Visigalli R, Dall’Asta V, Ganapathy V, Gazzola GC (2001) The adaptive regulation of amino acid transport system A is associated to changes in ATA2 expression. FEBS Lett 490:11–14

    CAS  Google Scholar 

  57. Franchi-Gazzola R, Gaccioli F, Bevilacqua E, Visigalli R, Dall’Asta V, Sala R, Varoqui H, Erickson JD, Gazzola GC, Bussolati O (2004) The synthesis of SNAT2 transporters is required for the hypertonic stimulation of system A transport activity. Biochim Biophys Acta 1667:157–166

    Article  PubMed  CAS  Google Scholar 

  58. Franco DL, Nojek IM, Molinero L, Coso OA, Costas MA (2002) Osmotic stress sensitizes naturally resistant cells to TNF-alpha-induced apoptosis. Cell Death Differ 9:1090–1098

    PubMed  CAS  Google Scholar 

  59. Friis MB, Friborg CR, Schneider L, Nielsen MB, Lambert IH, Christensen ST, Hoffmann EK (2005) Cell shrinkage as a signal to apoptosis in NIH 3T3 fibroblasts. J Physiol 567:427–443

    PubMed  CAS  Google Scholar 

  60. Fumarola C, Zerbini A, Guidotti GG (2001) Glutamine deprivation-mediated cell shrinkage induces ligand-independent CD95 receptor signaling and apoptosis. Cell Death Differ 8:1004–1013

    PubMed  CAS  Google Scholar 

  61. Gaccioli F, Huang CC, Wang C, Bevilacqua E, Franchi-Gazzola R, Gazzola GC, Bussolati O, Snider MD, Hatzoglou M (2006) Amino acid starvation induces the SNAT2 neutral amino acid transporter by a mechanism that involves eukaryotic initiation factor 2 alpha phosphorylation and cap-independent translation. J Biol Chem 281:17929–17940

    PubMed  Google Scholar 

  62. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286:433–442

    PubMed  CAS  Google Scholar 

  63. Go WY, Liu X, Roti MA, Liu F, Ho SN (2004) NFAT5/TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc Natl Acad Sci USA 101:10673–10678

    PubMed  CAS  Google Scholar 

  64. Heo JI, Lee MS, Kim JH, Lee JS, Kim J, Park JB, Lee JY, Han JA, Kim JI (2006) The role of tonicity responsive enhancer sites in the transcriptional regulation of human hsp70-2 in response to hypertonic stress. Exp Mol Med 38:295–301

    PubMed  CAS  Google Scholar 

  65. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372

    PubMed  CAS  Google Scholar 

  66. Holmberg CI, Hietakangas V, Mikhailov A, Rantanen JO, Kallio M, Meinander A, Hellman J, Morrice N, MacKintosh C, Morimoto RI, Eriksson JE, Sistonen L (2001) Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J 20:3800–3810

    PubMed  CAS  Google Scholar 

  67. Huang Z, Tunnacliffe A (2004) Response of human cells to desiccation: comparison with hyperosmotic stress response. J Physiol 558:181–191

    PubMed  CAS  Google Scholar 

  68. Huang Z, Tunnacliffe A (2005) Gene induction by desiccation stress in human cell cultures. FEBS Lett 579:4973–4977

    PubMed  CAS  Google Scholar 

  69. Irarrazabal CE, Liu JC, Burg MB, Ferraris JD (2004) ATM, a DNA damage-inducible kinase, contributes to activation by high NaCl of the transcription factor TonEBP/OREBP. Proc Natl Acad Sci USA 101:8809–8814

    PubMed  CAS  Google Scholar 

  70. Jacquier-Sarlin MR, Jornot L, Polla BS (1995) Differential expression and regulation of hsp70 and hsp90 by phorbol esters and heat shock. J Biol Chem 270:14094–14099

    PubMed  CAS  Google Scholar 

  71. Jeon US, Kim JA, Sheen MR, Kwon HM (2006) How tonicity regulates genes: story of TonEBP transcriptional activator. Acta Physiol 187:241–247

    CAS  Google Scholar 

  72. Jurivich DA, Sistonen L, Kroes RA, Morimoto RI (1992) Effect of sodium salicylate on the human heat shock response. Science 255:1243–1245

    PubMed  CAS  Google Scholar 

  73. Jurivich DA, Pachetti C, Qiu L, Welk JF (1995) Salicylate triggers heat shock factor differently than heat. J Biol Chem 270:24489–24495

    PubMed  CAS  Google Scholar 

  74. Kaarniranta K, Elo M, Sironen R, Lammi MJ, Goldring MB, Eriksson JE, Sistonen L, Helminen HJ (1998) Hsp70 accumulation in chondrocytic cells exposed to high continuous hydrostatic pressure coincides with mRNA stabilization rather than transcriptional activation. Proc Natl Acad Sci USA 95:2319–2324

    PubMed  CAS  Google Scholar 

  75. Kaarniranta K, Holmberg CI, Helminen HJ, Eriksson JE, Sistonen L, Lammi MJ (2000) Protein synthesis is required for stabilization of hsp70 mRNA upon exposure to both hydrostatic pressurization and elevated temperature. FEBS Lett 475:283–286

    PubMed  CAS  Google Scholar 

  76. Kabakov AE, Budagova KR, Latchman DS, Kampinga HH (2002) Stressful preconditioning and HSP70 overexpression attenuate proteotoxicity of cellular ATP depletion. Am J Physiol 283:C521–C534

    CAS  Google Scholar 

  77. Kabakov AE, Malyutina YV, Latchman DS (2006) Hsf1-mediated stress response can transiently enhance cellular radioresistance. Radiat Res 165:410–423

    PubMed  CAS  Google Scholar 

  78. Kitamura H, Yamauchi A, Nakanishi T, Takamitsu Y, Sugiura T, Akagi A, Moriyama T, Horio M, Imai E (1997) Effects of inhibition of myo-inositol transport on MDCK cells under hypertonic environment. Am J Physiol 272:F267–F272

    PubMed  CAS  Google Scholar 

  79. Klein JD, O’Neill WC (1995) Volume-sensitive myosin phosphorylation in vascular endothelial cells: correlation with Na–K–2Cl cotransport. Am J Physiol 269:C1524–C1531

    PubMed  CAS  Google Scholar 

  80. Klein JD, Lamitina ST, O’Neill WC (1999) JNK is a volume-sensitive kinase that phosphorylates the Na–K–2Cl cotransporter in vitro. Am J Physiol 277:C425–C431

    PubMed  CAS  Google Scholar 

  81. Kojima R, Randall J, Brenner BM, Gullans SR (1996) Osmotic stress protein 94 (Osp94). A new member of the Hsp110/SSE gene subfamily. J Biol Chem 271:12327–12332

    PubMed  CAS  Google Scholar 

  82. Kojima R, Randall JD, Ito E, Manshio H, Suzuki Y, Gullans SR (2004) Regulation of expression of the stress response gene, Osp94: identification of the tonicity response element and intracellular signalling pathways. Biochem J 380:783–794

    PubMed  CAS  Google Scholar 

  83. Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J App Physiol 92:2177–2186

    CAS  Google Scholar 

  84. Kultz D, Madhany S, Burg MB (1998) Hyperosmolality causes growth arrest of murine kidney cells. Induction of GADD45 and GADD153 by osmosensing via stress-activated protein kinase 2. J Biol Chem 273:13645–13651

    PubMed  CAS  Google Scholar 

  85. Kultz D, Chakravarty D (2001) Hyperosmolality in the form of elevated NaCl but not urea causes DNA damage in murine kidney cells. Proc Natl Acad Sci USA 98:1999–2004

    PubMed  CAS  Google Scholar 

  86. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78:247–306

    PubMed  CAS  Google Scholar 

  87. Lang F, Madlung J, Bock J, Lukewille U, Kaltenbach S, Lang KS, Belka C, Wagner CA, Lang HJ, Gulbins E, Lepple-Wienhues A (2000) Inhibition of Jurkat-T-lymphocyte Na+/H+-exchanger by CD95(Fas/Apo-1)-receptor stimulation. Pflugers Arch 440:902–907

    PubMed  CAS  Google Scholar 

  88. Lang KS, Fillon S, Schneider D, Rammensee HG, Lang F (2002) Stimulation of TNF alpha expression by hyperosmotic stress. Pflugers Arch 443:798–803

    PubMed  CAS  Google Scholar 

  89. Lee SD, Colla E, Sheen MR, Na KY, Kwon HM (2003) Multiple domains of TonEBP cooperate to stimulate transcription in response to hypertonicity. J Biol Chem 278:47571–47577

    PubMed  CAS  Google Scholar 

  90. Lee JS, Lee JJ, Seo JS (2005) HSP70 deficiency results in activation of c-Jun N-terminal Kinase, extracellular signal-regulated kinase, and caspase-3 in hyperosmolarity-induced apoptosis. J Biol Chem 280:6634–6641

    PubMed  CAS  Google Scholar 

  91. Lepore DA, Knight KR, Anderson RL, Morrison WA (2001) Role of priming stresses and Hsp70 in protection from ischemia-reperfusion injury in cardiac and skeletal muscle. Cell Stress Chaperones 6:93–96

    PubMed  CAS  Google Scholar 

  92. Lezama R, Diaz-Tellez A, Ramos-Mandujano G, Oropeza L, Pasantes-Morales H (2005) Epidermal growth factor receptor is a common element in the signaling pathways activated by cell volume changes in isosmotic, hyposmotic or hyperosmotic conditions. Neurochem Res 30:1589–1597

    PubMed  CAS  Google Scholar 

  93. Li GC, Werb Z (1982) Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster ovary cells. Proc Natl Acad Sci USA 79:3218–3222

    PubMed  CAS  Google Scholar 

  94. Lindquist S, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22:631–677

    PubMed  CAS  Google Scholar 

  95. López-Fontanals M, Rodríguez-Mulero S, Casado FJ, Dérijard B, Pastor-Anglada M (2003) The osmoregulatory and the amino acid-regulated responses of system A are mediated by different signal transduction pathways. J Gen Physiol 122:5–16

    PubMed  Google Scholar 

  96. Lytle C, McManus T (2002) Coordinate modulation of Na–K–2Cl cotransport and K–Cl cotransport by cell volume and chloride. Am J Physiol 283:C1422–C1431

    CAS  Google Scholar 

  97. Maallem S, Berod A, Mutin M, Kwon HM, Tappaz ML (2006) Large discrepancies in cellular distribution of the tonicity-induced expression of osmoprotective genes and their regulatory transcription factor TonEBP in rat brain. Neuroscience 142:355–368

    PubMed  CAS  Google Scholar 

  98. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 97:9487–9492

    PubMed  CAS  Google Scholar 

  99. Mak SK, Kultz D (2004) Gadd45 proteins induce G2/M arrest and modulate apoptosis in kidney cells exposed to hyperosmotic stress. J Biol Chem 279:39075–39084

    PubMed  CAS  Google Scholar 

  100. Matsuoka Y, Yamauchi A, Nakanishi T, Sugiura T, Kitamura H, Horio M, Takamitsu Y, Ando A, Imai E, Hori M (1999) Response to hypertonicity in mesothelial cells: role of Na+/myo-inositol co-transporter. Nephrol Dial Transplant 14:1217–1223

    PubMed  CAS  Google Scholar 

  101. Mackenzie B, Erickson JD (2004) Sodium-coupled neutral amino acid (system N/A) transporters of the SLC38 gene family. Pflügers Arch 447:784–795

    PubMed  CAS  Google Scholar 

  102. McDowell HE, Eyers PA, Hundal HS (1998) Regulation of system A amino acid transport in L6 rat skeletal muscle cells by insulin, chemical and hyperthermic stress. FEBS Lett 441:15–19

    PubMed  CAS  Google Scholar 

  103. McGivan JD, Pastor-Anglada M (1994) Regulatory and molecular aspects of mammalian amino acid transport. Biochem J 299:321–334

    PubMed  CAS  Google Scholar 

  104. McManus ML, Churchwell KB, Strange K (1995) Regulation of cell volume in health and disease. N Engl J Med 333:1260–1266

    PubMed  CAS  Google Scholar 

  105. Michea L, Combs C, Andrews P, Dmitrieva N, Burg MB (2002) Mitochondrial dysfunction is an early event in high-NaCl-induced apoptosis of mIMCD3 cells. Am J Physiol 282:F981–F990

    CAS  Google Scholar 

  106. Miyakawa H, Woo SK, Dahl SC, Handler JS, Kwon HM (1999) Tonicity-responsive enhancer binding protein, a Rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA 96:2538–2542

    PubMed  CAS  Google Scholar 

  107. Mongin AA, Orlov SN (2001) Mechanisms of cell volume regulation and possible nature of the cell volume sensor. Pathophysiology 8:77–88

    PubMed  CAS  Google Scholar 

  108. Morimoto RI, Tissieres A, Georgopoulos C (1990) The stress response, function of the proteins and perspectives. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 1–36

    Google Scholar 

  109. Morimoto RI, Milarski KL (1990) Expression and function of vertebrate hsp70 genes. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 323–359

    Google Scholar 

  110. Morishima N (2005) Control of cell fate by Hsp70: more than an evanescent meeting. J Biochem 137:449–453

    PubMed  CAS  Google Scholar 

  111. Mow VC, Wang CC, Hung CT (1999) The extracellular matrix, interstitial fluid and ions as a mechanical signal transducer in articular cartilage. Osteoarthr Cartil 7:41–58

    PubMed  CAS  Google Scholar 

  112. Na KY, Woo SK, Lee SD, Kwon HM (2003) Silencing of TonEBP/NFAT5 transcriptional activator by RNA interference. J Am Soc Nephrol 14:283–288

    PubMed  CAS  Google Scholar 

  113. Nahm O, Woo SK, Handler JS, Kwon M (2002) Involvement of multiple kinase pathways in stimulation of gene transcription by hypertonicity. Am J Physiol 282:C49–C58

    CAS  Google Scholar 

  114. Neuhofer W, Müller E, Burger-Kentischer A, Frack ML, Thurau K, Beck FX (1998) Pretreatment with hypertonic NaCl protects MDCK cells against high urea concentrations. Pflugers Arch 435:407–414

    PubMed  CAS  Google Scholar 

  115. Neuhofer W, Muller E, Burger-Kentischer A, Fraek ML, Thurau K, Beck FX (1999) Inhibition of NaCl-induced heat shock protein 72 expression renders MDCK cells susceptible to high urea concentrations. Pflugers Arch 437:611–616

    PubMed  CAS  Google Scholar 

  116. Neuhofer W, Fraek ML, Ouyang N, Beck FX (2005) Differential expression of heat shock protein 27 and 70 in renal papillary collecting duct and interstitial cells—implications for urea resistance. J Physiol 564:715–722

    PubMed  CAS  Google Scholar 

  117. Neuhofer W, Beck FX (2006) Survival in hostile environments: strategies of renal medullary cells. Physiology 21:171–180

    PubMed  CAS  Google Scholar 

  118. Nylandsted J, Jaattela M, Hoffmann EK, Pedersen SF (2004) Heat shock protein 70 inhibits shrinkage-induced programmed cell death via mechanisms independent of effects on cell volume-regulatory membrane transport proteins. Pflugers Arch 449:175–185

    PubMed  CAS  Google Scholar 

  119. Olsen M, Sarup A, Larsson OM, Schousboe A (2005) Effect of hyperosmotic conditions on the expression of the betaine-GABA-transporter (BGT-1) in cultured mouse astrocytes. Neurochem Res 30:855–865

    PubMed  CAS  Google Scholar 

  120. Oxender DL, Christensen HN (1963) Distinct mediating systems for the transport of neutral amino acids by the Ehrlich cell. J Biol Chem 238:3686–3699

    PubMed  CAS  Google Scholar 

  121. Padda R, Wamsley-Davis AM, Gustin MC, Ross R, Yu C, Sheikh-Hamad D (2006) MEKK3-mediated signaling to p38 kinase and TonE in hypertonically stressed kidney cells. Am J Physiol 291:F874–F881

    CAS  Google Scholar 

  122. Palii SS, Thiaville MM, Pan YX, Zhong C, Kilberg MS (2006) Characterization of the amino acid response element within the human sodium-coupled neutral amino acid transporter 2 (SNAT2) system A transporter gene. Biochem J 395:517–527

    PubMed  CAS  Google Scholar 

  123. Parsell DA, Taulien J, Lindquist S (1993) The role of heat-shock proteins in thermotolerance. Philos Trans R Soc Lond B Biol Sci 339:279–285

    PubMed  CAS  Google Scholar 

  124. Petronini PG, Tramacere R, Kay JE, Borghetti AF (1986) Adaptive response of cultured fibroblasts to hyperosmolarity. Exp Cell Res 165:180–190

    PubMed  CAS  Google Scholar 

  125. Petronini PG, Tramacere M, Wheeler KP, Borghetti AF (1990) Induction of amino acid transport activity in chick embryo fibroblasts by replacement of extracellular sodium chloride with disaccharide. Biochim Biophys Acta 1053:144–150

    PubMed  CAS  Google Scholar 

  126. Petronini PG, Alfieri RR, De Angelis E, Campanini C, Borghetti AF, Wheeler KP (1993) Different HSP70 expression and cell survival during adaptive responses of 3T3 and transformed 3T3 cells to osmotic stress. Brit J Cancer 67:493–499

    PubMed  CAS  Google Scholar 

  127. Petronini PG, Alfieri RR, Losio MN, Caccamo AE, Cavazzoni A, Bonelli MA, Borghetti AF, Wheeler KP (2000) Induction of BGT1 and amino acid system A transport activities in endothelial cells exposed to hyperosmolarity. Am J Physiol 279:R1580–R1589

    CAS  Google Scholar 

  128. Petronini PG, Caccamo AE, Alfieri RR, Bonelli MA, Borghetti AF (2001) The effect of heat shock on amino acid transport and cell volume in 3T3 cells. Amino Acids 20:363–380

    PubMed  CAS  Google Scholar 

  129. Piechotta K, Lu J, Delpire E (2002) Cation chloride cotransporters interact with the stress-related kinases Ste20-related proline-alanine-rich kinase (SPAK) and oxidative stress response 1 (OSR1). J Biol Chem 277:50812–50819

    PubMed  CAS  Google Scholar 

  130. Plumier JC, Currie RW (1996) Heat shock-induced myocardial protection against ischemic injury: a role for Hsp70? Cell Stress Chaperones 1:13–17

    PubMed  CAS  Google Scholar 

  131. Proft M, Mas G, de Nadal E, Vendrell A, Noriega N, Struhl K, Posas F (2006) The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress. Mol Cell 23:241–250

    PubMed  CAS  Google Scholar 

  132. Qu Y, Bolen CL, Bolen DW (1998) Osmolyte-driven contraction of a random coil protein. Proc Natl Acad Sci USA 95:9268–9273

    PubMed  CAS  Google Scholar 

  133. Reimer RJ, Chaudhry FA, Gray AT, Edwards RH (2000) Amino acid transport system A resembles system N in sequence but differs in mechanism. Proc Natl Acad Sci USA 97:7715–7720

    PubMed  CAS  Google Scholar 

  134. Reyna SV, Ensenat D, Johnson FK, Wang H, Schafer AI, Durante W (2004) Cyclic strain stimulates l-proline transport in vascular smooth muscle cells. Am J Hypertens 17:712–717

    PubMed  CAS  Google Scholar 

  135. Santos BC, Chevaile A, Kojima R, Gullans SR (1998) Characterization of the Hsp110/SSE gene family response to hyperosmolality and other stresses. Am J Physiol 274:F1054–F1061

    PubMed  CAS  Google Scholar 

  136. Santos BC, Pullman JM, Chevaile A, Welch WJ, Gullans SR (2003) Chronic hyperosmolarity mediates constitutive expression of molecular chaperones and resistance to injury. Am J Physiol 284:F564–F574

    CAS  Google Scholar 

  137. Shamovsky I, Ivannikov M, Kandel ES, Gershon D, Nudler E (2006) RNA-mediated response to heat shock in mammalian cells. Nature 440:556–560

    PubMed  CAS  Google Scholar 

  138. Sheikh-Hamad D, Garcia-Perez A, Ferraris JD, Peters EM, Burg MB (1994) Induction of gene expression by heat shock versus osmotic stress. Am J Physiol 267:F28–F34

    PubMed  CAS  Google Scholar 

  139. Sheikh-Hamad D, Gustin MC (2004) MAP kinases and the adaptive response to hypertonicity: functional preservation from yeast to mammals. Am J Physiol 287:F1102–F1110

    CAS  Google Scholar 

  140. Shim EH, Kim JI, Bang ES, Heo JS, Lee JS, Kim EY, Lee JE, Park WY, Kim SH, Kim HS, Smithies O, Jang JJ, Jin DI, Seo JS (2002) Targeted disruption of hsp70.1 sensitizes to osmotic stress. EMBO Rep 3:857–861

    PubMed  CAS  Google Scholar 

  141. Strange K (2004) Cellular volume homeostasis. Adv Physiol Educ 28:155–159

    PubMed  Google Scholar 

  142. Sugawara M, Nakanishi T, Fei Y-J, Huang W, Ganapathy ME, Leibach FH, Ganapathy V (2000) Cloning of an amino acid transporter with functional characteristics and tissue expression pattern identical to that of system A. J Biol Chem 275:16473–16477

    PubMed  CAS  Google Scholar 

  143. Takanaga H, Tokuda N, Ohtsuki S, Hosoya KI, Terasaki T (2002) ATA2 is predominantly expressed as system A at the blood–brain barrier and acts as brain-to-blood efflux transport for l-proline. Mol Pharmacol 61:1289–1296

    PubMed  CAS  Google Scholar 

  144. Trama J, Go WY, Ho SN (2002) The osmoprotective function of the NFAT5 transcription factor in T cell development and activation. J Immunol 169:5477–5488

    PubMed  CAS  Google Scholar 

  145. Tramacere M, Petronini PG, Severini A, Borghetti AF (1984) Osmoregulation of amino acid transport activity in cultured fibroblasts. Exp Cell Res 151:70–79

    PubMed  CAS  Google Scholar 

  146. Tsai TT, Danielson KG, Guttapalli A, Oguz E, Albert TJ, Shapiro IM, Risbud MV (2006) TonEBP/OREBP is a regulator of nucleus pulposus cell function and survival in the intervertebral disc. J Biol Chem 281:25416–25424

    PubMed  CAS  Google Scholar 

  147. Tong EH, Guo JJ, Huang AL, Liu H, Hu CD, Chung SS, Ko BC (2006) Regulation of nucleocytoplasmic trafficking of transcription factor OREBP/TonEBP/NFAT5. J Biol Chem 281:23870–23879

    PubMed  CAS  Google Scholar 

  148. Urban JP, Hall AC, Gehl KA (1993) Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J Cell Physiol 154:262–270

    PubMed  CAS  Google Scholar 

  149. Valkova N, Kultz D (2006) Constitutive and inducible stress proteins dominate the proteome of the murine inner medullary collecting duct-3 (mIMCD3) cell line. Biochim Biophys Acta 1764:1007–1020

    PubMed  CAS  Google Scholar 

  150. Walter L, Rauh F, Gunther E (1994) Comparative analysis of the three major histocompatibility complex-linked heat shock protein 70 (Hsp70) genes of the rat. Immunogenetics 40:325–330

    PubMed  CAS  Google Scholar 

  151. Wang YH, Borkan SC (1996) Prior heat stress enhances survival of renal epithelial cells after ATP depletion. Am J Physiol 270:F1057–F1065

    PubMed  CAS  Google Scholar 

  152. Wang YH, Knowlton AA, Li FH, Borkan SC (2002) Hsp72 expression enhances survival in adenosine triphosphate-depleted renal epithelial cells. Cell Stress Chaperones 7:137–145

    PubMed  CAS  Google Scholar 

  153. Warskulat U, Reinen A, Grether-Beck S, Krutmann J, Haussinger D (2004) The osmolyte strategy of normal human keratinocytes in maintaining cell homeostasis. J Invest Dermatol 123:516–521

    PubMed  CAS  Google Scholar 

  154. Welch WJ, Brown CR (1996) Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1:109–115

    PubMed  CAS  Google Scholar 

  155. Woo SK, Dahl SC, Handler JS, Kwon HM (2000) Bidirectional regulation of tonicity-responsive enhancer binding protein in response to changes in tonicity. Am J Physiol 278:F1006–F1012

    CAS  Google Scholar 

  156. Woo SK, Lee SD, Kwon HM (2002a) TonEBP transcriptional activator in the cellular response to increased osmolality. Pflugers Arch 444:579–585

    PubMed  CAS  Google Scholar 

  157. Woo SK, Lee SD, Na KY, Park WK, Kwon HM (2002b) TonEBP/NFAT5 stimulates transcription of HSP70 in response to hypertonicity. Mol Cell Biol 22:5753–5760

    PubMed  CAS  Google Scholar 

  158. Wu KL, Khan S, Lakhe-Reddy S, Wang L, Jarad G, Miller RT, Konieczkowski M, Brown AM, Sedor JR, Schelling JR (2003) Renal tubular epithelial cell apoptosis is associated with caspase cleavage of the NHE1 Na+/H+ exchanger. Am J Physiol 284:F829–F839

    CAS  Google Scholar 

  159. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222

    PubMed  CAS  Google Scholar 

  160. Yao D, Mackenzie B, Ming H, Varoqui H, Zhu H, Hediger MA, Erickson JD (2000) A novel system A isoform mediating Na+/neutral amino acid cotransport. J Biol Chem 275:22790–22797

    PubMed  CAS  Google Scholar 

  161. Zhan Q, Antinore MJ, Wang XW, Carrier F, Smith ML, Harris CC, Fornace AJ Jr (1999) Association with Cdc2 and inhibition of Cdc2/cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene 18:2892–2900

    PubMed  CAS  Google Scholar 

  162. Zhang Z, Ferraris JD, Brooks HL, Brisc I, Burg MB (2003) Expression of osmotic stress-related genes in tissues of normal and hyposmotic rats. Am J Physiol 285:F688–F693

    CAS  Google Scholar 

  163. Zhang Z, Ferraris JD, Irarrazabal CE, Dmitrieva NI, Park JH, Burg MB (2005) Ataxia telangiectasia-mutated, a DNA damage-inducible kinase, contributes to high NaCl-induced nuclear localization of transcription factor TonEBP/OREBP. Am J Physiol 289:F506–F511

    Article  CAS  Google Scholar 

  164. Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408:433–439

    PubMed  CAS  Google Scholar 

  165. Zhou C, Li Z, Diao H, Yu Y, Zhu W, Dai Y, Chen FF, Yang J (2006) DNA damage evaluated by gammaH2AX foci formation by a selective group of chemical/physical stressors. Mutat Res 604:8–18

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Dr. K.P. Wheeler and Dr. A.F. Borghetti for carefully reading and for the constructive criticism of this manuscript.

We apologize to the colleagues whose works have not been cited in the present review because of space limitations and our inability to find their work in the literature search.

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  1. Dipartimento di Medicina Sperimentale, Sezione di Patologia Molecolare e Immunologia, Universita` degli Studi di Parma, 43100, Parma, Italy

    Roberta R. Alfieri & Pier Giorgio Petronini

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  1. Roberta R. Alfieri
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  2. Pier Giorgio Petronini
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Correspondence to Roberta R. Alfieri.

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Alfieri, R.R., Petronini, P.G. Hyperosmotic stress response: comparison with other cellular stresses. Pflugers Arch - Eur J Physiol 454, 173–185 (2007). https://doi.org/10.1007/s00424-006-0195-x

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