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Signaling Events during Swelling and Regulatory Volume Decrease

Abstract

Brain cell swelling compromises neuronal function and survival by the risk of generation of ischemia episodes as compression of small vessels occurs due to the limits to expansion imposed by the rigid skull. External osmolarity reductions or intracellular accumulation of osmotically active solutes result in cell swelling which can be counteracted by extrusion of osmolytes through specific efflux pathways. Characterization of these pathways has received considerable attention, and there is now interest in the understanding of the intracellular signaling events involved in their activation and regulation. Calcium and calmodulin, phosphoinositides and cAMP may act as second messengers, carrying the information about a cell volume change into signaling enzymes. Small GTPases, protein tyrosine kinases and phospholipases, also appear to be part of the signaling cascades ultimately modulating the osmolyte efflux pathways. This review focus on i) the influence of hyposmotic and isosmotic swelling on these signaling events and molecules and ii) the effects of manipulating their function on the osmolyte fluxes, particularly K+, CI and amino acids, and on the consequent efficiency of cell volume adjustment.

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REFERENCES

  1. Lang, F., Busch, G. L., Ritter, M., Völkl, H., Waldegger, S., Gulbins, E., and Häussinger, D. 1998. Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78: 247-306.

    Google Scholar 

  2. Kimelberg, H. K. and Ransom, B. R. 1986. Physiological and pathological aspects of astrocytic swelling. Pages. 129-166, in Fedoroff, S., and Vernadakis, A. (eds.), Astrocytes. Orlando, Fl. Academic Press.

    Google Scholar 

  3. Häussinger, D., Lang, F., and Gerok, W. 1994. Regulation of cell function by the cellular hydration state. Am. J. Physiol. 267: E343-E355.

    Google Scholar 

  4. Lang, F., Lepple-Wienhues, A., Paulmichl, M., Szabó , I., Siemen, D., and Gulbins, E. 1998. Ion channels, cell volume, and apoptotic cell death. Cell. Physiol. Biochem. 8:285-292.

    Google Scholar 

  5. McManus, M. L. and Churchwell, K. B. 1994. Clinical significance of cellular osmoregulation. Pages 63-74, in Strange, K. (ed.), Cellular and Molecular Physiology of Cell Volume Regulation, CRC Press, Boca Rató n, Fl., U.S.A.

    Google Scholar 

  6. Kimelberg, H. K. 1995. Current concepts of brain edema. J. Neurosug. 83:1051-1059.

    Google Scholar 

  7. Hochman, D. W., Baraban, S. C., Owens, J. W. M., and Schwarzkroin, P. A. 1995. Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity. Science 270:99-102.

    Google Scholar 

  8. Hoffmann, E. K. and Simonsen, L. O. 1989. Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol. Rev. 69:315-382.

    Google Scholar 

  9. Pasantes-Morales, H. 1996. Volume regulation in brain cells: cellular and molecular mechanisms. Metab. Brain Dis. 11:187-203.

    Google Scholar 

  10. Okada, Y. 1997. Volume expansion-sensing outward-rectifier Cl-channel: fresh start to the molecular identity and volume sensor. Am. J. Physiol. 273:C755-C789.

    Google Scholar 

  11. Mills, J. W., Schiewebert, E. M., and Staton, B. A. 1994. The cytoskeleton and cell volume regulation. Pages 241-258, in Strange, K. (eds.), Cellular and Molecular Physiology of Cell Volume Regulation, CRC Press, Boca Rató n, Fl., U.S.A.

    Google Scholar 

  12. Summers, J. C., Trais, L., Lajvardi, R., Hergan, D., Buechler, R., Chang, H., Peñ a-Rasgado, C., and Rasgado-Flores, H. 1997. Role of concentration and size of intracellular macromolecules in cell volume regulation. Am. J. Physiol. 273: C360-C370.

    Google Scholar 

  13. Motais, R., Guizouarn, H., and Garcia-Romeu, F. 1991. Red cell volume regulation: the pivotal role of ionic strength in controlling swelling-dependent transport systems. Biochim. Biophys. Acta 1075:169-180.

    Google Scholar 

  14. Law, R. O. 1994. Taurine efflux and the regulation of cell volume in incubated slices of rat cerebral cortex. Biochim. Biophys. Acta 1221:21-28.

    Google Scholar 

  15. Nilius, B., Prenen, J., Voets, T., Eggermont, J., and Droogmans, G. 1998. Activation of volume-regulated chloride currents by reduction of intracellular ionic strength in bovine endothelial cells. J. Physiol. 506:353-361.

    Google Scholar 

  16. Cannon, C. L., Basavappa, S., and Strange, K. 1998. Intracellular ionic strength regulates the volume sensitivity of a swellingactivated anion channel. Am. J. Physiol. 275:C416-C422.

    Google Scholar 

  17. Voets, T., Droogmans, G., Raskin, G., Eggermont, J., and Nilius, B. 1999. Reduced intracellular ionic strength as the initial trigger for activation of endothelial volume-regulated anion channels. Proc. Natl. Acad. Sci. USA 96:5298-5303.

    Google Scholar 

  18. Cardin, V., Peñ a-Segura, C., and Pasantes-Morales, H. 1999. Activation and inactivation of taurine efflux in hyposmotic and isosmotic swelling in cortical astrocytes: role of ionic strength and cell volume decrease. J. Neurosci. Res. 56:659-667.

    Google Scholar 

  19. Thurston, J. H., Hauhart, R. E., and Nelson, J. S. 1987. Adaptive decreases in amino acids (taurine in particular) creatine and electrolytes, prevent cerebral edema in chronically hyponatremic mice: rapid correction (experimental model of central pontine myelinolysis) causes dehydration and shrinkage of brain. Metab. Brain Dis. 2:223-241.

    Google Scholar 

  20. Verbalis, J. G. and Gullans, S. R. 1991. Hyponatremia causes large sustained reductions in brain content of multiple organic osmolytes in rats. Brain Res. 567:274-282.

    Google Scholar 

  21. Nilius, B., Eggermont, J., Voets, T., Buyse, G., Manolopoulos, V., and Droogmans, G. 1997. Properties of volume-regulated anion channels in mammalian cells. Prog. Biophys. Molec. Biol. 68:69-119.

    Google Scholar 

  22. Sánchez-Olea, R., Morales-Mulia, M., Morán, J., and Pasantes-Morales, H. 1995. Inhibition by polyunsaturated fatty acids of regulatory volume decrease and osmolyte fluxes in astrocytes in culture. Am. J. Physiol. 269:C96-C102.

    Google Scholar 

  23. Jentsch, T. J. 1996. Chloride channels: a molecular perspective. Curr. Opin. Neurobiol. 6:303-310.

    Google Scholar 

  24. Duan, D., Cowley, S., Horowitz, B., and Hume, J. R. 1999. A serine residue in C1C-3 links phosphorylation-dephosphorylation to chloride channel regulation by cell volume. J. Gen. Physiol. 11:57-70.

    Google Scholar 

  25. von Weikersthal, S. F., Barrand, M. A., and Hladky, S. B. 1999. Functional and molecular characterization of a volumesensitive chloride current in rat brain endothelial cells. J. Physiol. 516:75-84.

    Google Scholar 

  26. Jackson, P. S. and Strange, K. 1995. Single-Channel properties of a volume-sensitive anion conductance. J. Gen. Physiol. 105:643-660.

    Google Scholar 

  27. Jackson, P. S. and Strange, K. 1995. Characterization of the voltage-dependent properties of a volume-sensitive anion conductance. J. Gen. Physiol. 105:661-676.

    Google Scholar 

  28. Patel, A. J., Lauritzen, I., Lazdunski, M., and Hornoré, E. 1998. Disruption of mitochondrial respiration inhibits volumeregulated anion channels and provokes neuronal cell swelling. J. Neurosci. 18:3117-3123.

    Google Scholar 

  29. Carpaneto, A., Accardi, A., Pisciotta, M., and Gambale, F. 1999. Chloride channels activated by hypotonicity in N2A neuroblastoma cell line. Exp. Brain Res. 124:193-199.

    Google Scholar 

  30. Strange, K., Emma, F., and Jackson, P. S. 1996. Cellular and molecular physiology of volume-sensitive anion channels. Am. J. Physiol. 270:C711-C730.

    Google Scholar 

  31. Roy, G. 1994. Channels for amino acids and metabolites activated by cell volume regulation. Japanese J. Physiol. 44: S37-S42.

    Google Scholar 

  32. Moorman, J. R. and Jones, L. R. 1998. Phospholemman: a cardiac taurine channel involved in regulation of cell volume. Pages 219-228, in Schaffer, S., Lombardini, J. B., and Huxtable, R. J. (eds.), Taurine 3, Cellular and Regulatory mechanisms, Plenum Press, New York.

    Google Scholar 

  33. Morales-Mulia, M., Pasantes-Morales, H., and Morán, J. 2000. Volume sensitive efflux of taurine in HEK293 cells overexpressing phospholemann. Biochim. Biophys. Acta (in press).

  34. Lambert, I. H. and Hoffmann, E. K. 1994. Cell swelling activates separate taurine and chloride channels in eEhrlich mouse ascites tumor cells. J. Membr. Biol. 142:289-298.

    Google Scholar 

  35. Stutzin, A., Torres, R., Oporto, M., Pacheco, P., Eguiguren, A. L., Cid, L. P., and SepÚ lveda, F. V. 1999. Separate taurine and chloride efflux pathways activated during regulatory volume decrease. Am. J. Physiol. 277:C392-C402.

    Google Scholar 

  36. Pasantes-Morales, H. and Morales-Mulia, S. 2000. Influence of calcium on regulatory volume decrease: role of potassium channels. Nephron 336. (in press).

  37. Deutsch, C. and Chen, L. Q. 1993. Heterologous expression of specific K+ channels in T lymphocytes: Funcional consequences for volume regulation. Proc. Natl. Acad. Sci. USA 90:10036-10040.

    Google Scholar 

  38. Khanna, R., Chang, M. C., Joiner, W. J., Kaczmarek, L. K., and Schlichter, L. C. 1999. hSK4/hlK1, a calmodulin-binding KCa channel in human T lymphocytes. J. Biol. Chem. 274:14838-14849.

    Google Scholar 

  39. Baraban, S. C., Bellingham, M. C., Berger, A. J., and Schwartzkroin, P. A. 1997. Osmolarity modulates K+ channel function on rat hippocampal interneurons but no CA1 pyramidal neurons. J. Physiol. 498:679-689.

    Google Scholar 

  40. McCarty, N. A. and O'Neil, R. G. 1992. Calcium signaling in cell volume regulation. Physiol. Rev. 72:1037-1061.

    Google Scholar 

  41. Rubera, I., Tauc, M., Poujeol, C., Bohn, M. T., Bidet, M., de Renzis, G., and Poujeol, P. 1997. Cl- and K+ conductances activated by cell swelling in primary cultures of rabbit distal bright convoluted tubules. Am. J. Physiol. 273: F680-F697.

    Google Scholar 

  42. Verdon, B., Winpenny, J. P., Whitfield, K. J., Argent, B. E., and Gray, M. A. 1995. Volume-activated chloride currents in pancreatic duct cells. Membrane Biol. 147:173-183.

    Google Scholar 

  43. Galietta, L. J. V., Falzoni, S., Di Virgilio, F., Romeo, G., and Zegarra-Moran, O. 1997. Characterization of volume-sensitive taurine-and Cl- -permeable channels. Am. J. Physiol. 273:C57-C66.

    Google Scholar 

  44. Mastrocola, T., Lambert, I. H., Kramhoft, B., Rugolo, M., and Hoffmann, E. K. 1993. Volume regulation in human fibroblasts: role of Ca2+ and 5-lipoxygenase products in the activation of the Cl- efflux. J. Membrane Biol. 136:55-62.

    Google Scholar 

  45. Basavappa, S., Chartouni, V., Kirk, K., Prpic, V., Ellory, J. C., and Mangel, A. W. 1995. Swelling-induced chloride currents in neuroblastoma cells are calcium dependent. J. Neurosci. 15:3662-3666.

    Google Scholar 

  46. Szücs, G., Heinke, S., Droggmans, G., and Nilius, B. 1996. Activation of the volume-sensitive chloride current in vascular endothelial cells requires a permissive intracellular Ca2+ concentration. Eur. J. Physiol. 431:467-469.

    Google Scholar 

  47. Basavappa, S., Huang, C. C., Mangel, A. W., Lebedev, D. V., Knauf, P. A., and Ellory, J. C. 1996. Swelling-activated amino acid efflux in the human neuroblastoma cell line CHP-100. J. Neurophysiol. 76:764-769.

    Google Scholar 

  48. Perry, P. B. and O'neill, W. C. 1994. Swelling-activated K+ fluxes in vascular endothelial cells: role of intracellular Ca2+. Am. J. Physiol. 267:C1535-C1542.

    Google Scholar 

  49. Bergeron, L. J., Stever, A. J., and Light, D. B. 1996. Potassium conductance activated during regulatory volume decrease by mudpuppy red blood cells. Am. J. Physiol. 270: R801-R810.

    Google Scholar 

  50. MacLeod, R. J. and Hamilton, J. R. 1999. Ca2+/calmodulin kinase II and decreases in intracellular pH are required to activate K+ channels after substantial swelling in villus epithelial cells. J. Membr. Biol. 172:59-66.

    Google Scholar 

  51. Vitarella, D., DiRisio, D. J., Kimelberg, H. K., and Aschner, M. 1994. Potassium and taurine release are highly correlated with regulatory volume decrease in neonatal primary rat astrocyte cultures. J. Neurochem. 63:1143-1149.

    Google Scholar 

  52. Jorgensen, N. K., Christensen, S., Harbak, H., Brown, A. M., Lambert, I. H., Hoffman, E. K., and Simonsen, L. O. 1997. On the role of calcium in the regulatory volume decrease (RVD) response in Ehrlich mouse ascites tumor cells. J. Membr. Biol. 157:281-299.

    Google Scholar 

  53. Lambert, I. H. 1998. Regulation of the taurine content in Ehrlich ascites tumour cells. Pages 269-276, in Schaffer, S., Lombardini, J. B., and Huxtable, R. J. (eds.), Taurine3, Cellular and Regulatory mechanisms, Plenum Press, New York.

    Google Scholar 

  54. Mongin, A. A., Cai, Z., and Kimelberg, H. K. 1999. Volume-dependent taurine release from cultured astrocytes requires permissive [Ca2+] and calmodulin. Am. J. Physiol. 277: C823-C832.

    Google Scholar 

  55. Kirk, J. and Kirk, K. 1994. Inhibition of volume-activated I- and taurine efflux from HeLa cells by P-glycoprotein blockers correlates with calmodulin inhibition. J. Biol. Chem. 269: 29389-29394.

    Google Scholar 

  56. Szücs, G., Heinke, S., De Greef, C., Raeymaekers, L., Eggermont, J., Droogmans, G., and Nilius, B. 1996. The volume-activated chloride current in endothelial cells from bovine pulmonary artery is not modulated by phosphorylation. Eur. J. Physiol. 431:540-548.

    Google Scholar 

  57. Leaney, J. L., Marsh, S. J., and Brown, D. A. 1997. A swelling-activated chloride current in rat sympathetic neurons. J. Physiol. 501:555-564.

    Google Scholar 

  58. Du, X. Y. and Sorota, S. 1999. Protein kinase C stimulates swelling-induced chloride current in canine atrial cells. Pflügers Arch. 437:227-234.

    Google Scholar 

  59. Vanoye, C. G., Castro, A. F., Pourcher, T., Reuss, L., and Altenberg, G. A. 1999. Phosphorylation of P-glycoprotein by PKA and PKC modulates swelling-activated Cl-Am. J. Physiol. 276:C370-C378.

    Google Scholar 

  60. Song, D., O'Regan, M. H., and Phillis, J. W. 1998. Protein kinase inhibitors attenuate cardiac swelling-induced amino acid release in the rat. J. Pharm. Pharmacol. 50:1280-1286.

    Google Scholar 

  61. Estevez, A. Y., O'Regan, M. H., Song, D., and Phillis, J. W. 1999. Hyposmotically induced amino acid release from the rat cerebral cortex: role of phospholipases and protein kinases. Brain Res. 844:1-9.

    Google Scholar 

  62. Deleuze, C., Duvoid, A., Moos, F. C., and Hussy, N. 2000. Tyrosine phosphorylation modulates the osmosensitivity of volume-dependent taurine efflux from glial cells in the rat supraoptic nucleus. J. Physiol. 523:291-299.

    Google Scholar 

  63. Morales-Mulia, S., Cardin, V., Torres-Márquez, M. E., Crevenna, A., and Pasantes-Morales, H. 2000. Influence of protein kinases on the osmosensitive release of taurine from cerebellar granule neurons. Nerochem. Int. (in press).

  64. Chung, I. and Schlichter, L. C. 1997. Native Kv1.3 channels are upregulated by protein kinase C. J. Membr. Biol. 156:73-85.

    Google Scholar 

  65. Bender, A. S. and Norenberg, M. D. 1994. Calcium dependence of hypoosmotically induced potassium release in cultured astrocytes. J. Neurosci. 14:4237-4243.

    Google Scholar 

  66. Hall, S. K., Zhang, J., and Lieberman, M. 1995. Cyclic AMP prevents activation of a swelling-induced chloride-sensitive conductance in chick heart cells. J. Physiol. 488:359-369.

    Google Scholar 

  67. Du, X. Y. and Sorota, S. 1997. Modulation of dog atrial swelling-induced chloride current by cAMP: protein kinase A-dependent and independent pathways. J. Physiol. 500: 111-122.

    Google Scholar 

  68. Nagasaki, M., Ye, L., Duan, D., Horowitz, B., and Hume, J. R. 2000. Intracellular cyclic AMP inhibits native and recombinant volume-regulated chloride channels from mammalian heart. J. Physiol. 15:705-717.

    Google Scholar 

  69. Klaerke, D. A. 1997. Regulation of Ca2+-activated K+ channels from rabbit distal colon. Comp. Biochem. Physiol. A. Physiol. 118:215-217.

    Google Scholar 

  70. Bringmann, A., Faude, F., and Reichenbach, A. 1997. Mammalian retinal glial Müller cells express large-conductance Ca2+-activated K+ channels that are modulated by Mg2+ and pH and activated by protein kinase A. Glia. 19:311-323.

    Google Scholar 

  71. Oz, M. C. and Sorota, S. 1995. Forskolin stimulates swellinginduced chloride current, not cardiac cystic fibrosis transmembrane-conductance regulator current, in human cardiac myocytes. Circ. Res. 76:1063-1070.

    Google Scholar 

  72. Jackson, P. S. and Strange, K. 1993. Volume-sensitive anion channels mediate swelling-activated inositol and taurine efflux. Am. J. Physiol. 265:C1489-C1500.

    Google Scholar 

  73. Tilly, B. C., van den Berghe, N., Tertoolen, L. G. J., Edixhoven, M. J., and de Jonge, H. R. 1993. Protein tyrosine phosphorylation is involved in osmoregulation of ionic conductances. J. Biol. Chem. 268:19919-19922.

    Google Scholar 

  74. Sadoshima, J., Qiu, Z., Morgan, J. P., and Izumo, S. 1996. Tyrosine kinase activation is an immediate and essential step in hypotonic cell swelling-induced ERK activation and c-fos gene expression in cardiac myocytes. EMBO J. 15:5535-5546.

    Google Scholar 

  75. Crépel, V., Panenka, W., Kelly, M. E. M., and MacVicar, B. A. 1998. Mitogen-activated protein and tyrosine kinases in the activation of astrocyte volume-activated chloride current. J. Neurosci. 18:1196-1206.

    Google Scholar 

  76. Lepple-Wienhues, A., Szabo, I., Laun, T., Kaba, N. K., Gulbins, E., and Lang, F. 1998. The tyrosine kinase p56lck mediates activation of swelling-induced chloride channels in lymphocytes. J. Cell Biol. 141:281-286.

    Google Scholar 

  77. Musch, M. W., Hubert, E. M., and Goldstein, L. 1999. Volume expansion stimulates p72syk and p56lyn in skates. J. Biol. Chem. 274:7923-7928.

    Google Scholar 

  78. Niisato, N., Post, M., Van Driessche, W., and Marunaka, Y. 1999. Cell swelling activates stress-activated protein kinases, p38 MAP kinase and JNK, in renal epithelial A6 cells. Biochem. Biophys. Res. Commun. 266:547-550.

    Google Scholar 

  79. Mongin, A. A., Redd, J. M., Charniga, C., and Kimelberg, H. K. 1999. [3H]taurine and D-[3H]aspartate release from astrocyte cultures are differently regulated by tyrosine kinases. Am. J. Physiol. 276:C1226-C1230.

    Google Scholar 

  80. van der Wijk, T., Dorrestijn, J., Narumiya, S., Maassen, J. A., de Jonge, H. R., and Tilly, B. C. 1998. Osmotic swelling-induced activation of the extracellular-signal-regulated protein kinases Erk-1 and Erk-2 in intestine 407 cells involves the Ras/Raf-signalling pathway. Biochem. J. 331:863-869.

    Google Scholar 

  81. Tilly, B. C., Gaestel, M., Engel, K., Edixhoven, M. J., and de Jonge, H. R. 1996. Hypoosmotic cell swelling activates the p38 MAP kinase signalling cascade. FEBS Lett. 395:133-136.

    Google Scholar 

  82. Häussinger, D., Schliess, F., Dombrowski, F., and Vom Dahl, S. 1999. Involvement of p38 MAPK in the regulation of proteolysis by liver cell hydration. Gastroenterology 116:921-935.

    Google Scholar 

  83. Tilly, B. C., van der Wijk, T., and de Jonge, H. R. 1998. Activation of cellular signalling pathways by hypotonicity. Pages 59-66, in Okada, Y. (ed.), Cell Volume Regulation: The Molecular Mechanism and Volume Sensing Machinery, Elsevier Science B.V., Amsterdam.

    Google Scholar 

  84. Kurz, A. K., Schliess, F., and Häussinger, D. 1998. Osmotic regulation of the heat shock response in primary rat hepatocytes. Hepatology 28:774-781.

    Google Scholar 

  85. Nilius, B., Voets, T., Prenen, J., Barth, H., Aktories, K., Kaibuchi, K., Droogmans, G., and Eggermont, J. 1999. Role of Rho and Rho kinase in the activation of volume-regulated anion channels in bovine endothelial cells. J. Physiol. 516:67-74.

    Google Scholar 

  86. Symons, M. 1996. Rho family GTPases: the cytoskeleton and beyond. TIBS. 2:78-181.

    Google Scholar 

  87. Kjoller, L. and Hall, A. 1999. Signaling to Rho GTPases. Exp. Cell. Res. 253:66-179.

    Google Scholar 

  88. Nilius, B., Gerke, V., Prenen, J., Szücs, G., Heinke, S., Weber, K., and Droogmans, G. 1996. Annexin II modulates volume-activated chloride currents in vascular endothelial cells. J. Biol. Chem. 271:30631-30636.

    Google Scholar 

  89. Ding, M., Eliasson, C., Betsholtz, C., Hamberger, A., and Pekni, M. 1998. Altered taurine release following hypotonic stress in astrocytes from mice deficient for GFAP and vimentin. Mol. Brain Res. 62:77-81.

    Google Scholar 

  90. Krause, U., Rider, H., and Hue, L. 1996. Protein kinase signaling pathway triggered by call swelling and involved in the activation of glycogen synthase and acetyl-CoA carboxylase in isolated rat hepatocytes. J. Biol. Chem. 271:16668-16673.

    Google Scholar 

  91. Feranchak, A. P., Roman, R. M., Schwiebert, E. M., and Fitz, J. G. 1998. Phosphatidylinositol 3-kinase contributes to cell volume regulation through effects on ATP release. J. Biol. Chem. 273:14906-14911.

    Google Scholar 

  92. Wymann, M. P. and Pirola, L. 1998. Structure and function of phosphoinositide3-kinases. Biochim. Biophys. Acta 436: 127-150.

    Google Scholar 

  93. Rodriguez-Viciana, P., Warne, P. H., Khwaja, A., Marte, B. M., Pappin, D., Das, P., Waterfield, M. D., Ridley, A., and Downward, J. 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by ras. Cell 89:457-467.

    Google Scholar 

  94. Hoffmann, E. K., Simonsen, L. O., and Lambert, I. H. 1993. Cell volume regulation: intracellular transmission. Chap. 7, in Gilles, R., (ed.), Interaction, Cell Volume, Cell Function, ACEP Series, Springer, Heidelberg.

    Google Scholar 

  95. Tilly, B. C., Edixhoven, M. J., Tertoolen, G. J., Morii, N., Saitoh, Y., Narumiya, S., and de Jonge, H. R. 1996. Activation of the osmo-sensitive chloride conductance involves P21rho and is accompanied by a transient reorganization of the F-actin cytoskeleton. Mol. Biol. Cell. 7:1419-1427.

    Google Scholar 

  96. Lambert, I. H. 1994. Eicosanoids and cell volume regulation. Pages 279-298, in Strange, K. (ed.), Cellular and Molecular Physiology of Cell Volume Regulation, CRC Press, Boca Rató n, Fl., U.S.A.

    Google Scholar 

  97. Thoroed, S. M., Lauritzen, L., Lambert, I. H., Hansen, H. S., and Hoffmann, E. K. 1997. Cell swelling activates phospholipase A2 in Ehrlich ascites tumor cells. J. Membr. Biol. 160:47-58.

    Google Scholar 

  98. Basavappa, S., Pedersen, S. F., Jorgensen, N. K., Ellory, J. C., and Hoffman, E. K. 1998. Swelling-induced arachidonic acid release via the 85-kDa cPLA2 in human neuroblastoma cells. J. Neurophysiol. 79:1441-1449.

    Google Scholar 

  99. Mitchell, C. H., Zhang, J. J., Wang, L., and Jacob, T. J. C. 1997. Volume-sensitive chloride current in pigmented ciliary epithelial cells: role of phospholipases. Am. J. Physiol. 272: C212-C222.

    Google Scholar 

  100. von Weikersthal, S. F., Hickman, M. E., Hladky, S. B., and Barrand, M. A. 1997. Hypotonicity-induced changes in anion permeability of cultured rat brain endothelial cells. Biochim. Biophys. Acta 1325:99-107.

    Google Scholar 

  101. Borsch-Haubold, A. G., Bartoli, F., Asselin, J., Dudler, T., Kramer, R. M., Apitz-Castro, R., Watson, S. P., and Gelb, M. H. 1998. Identification of the phosphorylation sites of cytosolic phopholipase A2 in agonist-stimulated platelets and HeLa cells. J. Biol. Chem. 273:19277-19282.

    Google Scholar 

  102. Hernández, M., Bayon, Y., Sánchez-Crespo, M., and Nieto, M. L. 1999. Signaling mechanisms involved in the activation of arachidonic acid metabolism in human astrocytoma cells by tumor necrosis factor-alpha: phosphorylation of cytosolic phospholipase A2 and transactivation of cyclooxygenase-2. J. Neurochem. 73:1641-1649.

    Google Scholar 

  103. Muthalif, M. M., Benter, I. F., Karzoun, N., Fatima, S., Harper, J., Uddin, M. R., and Malik, K. U. 1998. 20-Hydroxyeicosatetraenoic acid mediates calcium/calmodulin-dependent protein kinase II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA 95:12701-12706.

    Google Scholar 

  104. Lehtonen, J. Y. A. and Kinnunen, P. J. 1995. Phospholipase A2 as a mechanosensor. Biophys. J. 68:1888-1894.

    Google Scholar 

  105. Trouet, D., Nilius, B., Jacobs, A., Remacle, C., Droogmans, G., and Eggermont, J. 1999. Caveolin-1 modulates the activity of the volume-regulated chloride channel. J. Physiol. 520:113-119.

    Google Scholar 

  106. Rizzo, V., Sung, A., Oh, P., and Schnitzer, J. E. 1998. Rapid mechanotransduction in situ at the luminal cell surface of vascular endothelium and its caveolae. J. Biol. Chem. 273: 26323-26329.

    Google Scholar 

  107. Häussinger, D. and Lang, F. 1991. Cell volume in the regulation of hepatic function: a new mechanism for metabolic control. Biochim. Biophys. Acta 1071:331-350.

    Google Scholar 

  108. MacLeod, R. J., Lembessis, P., and Hamilton, J. R. 1992. Effect of protein kinase C inhibitors on Cl-conductance required for volume regulation after L-alanine cotransport. Am. J. Physiol. 262:C950-C955.

    Google Scholar 

  109. Lydofsky, S. D. and Roman, R. M. 1997. Alanine uptake activates hepatocellular chloride channels. Am. J. Physiol. 273: G849-G853.

    Google Scholar 

  110. MacLeod, R. J., Lembessis, P., and Hamilton, J. R. 1992. Differences in Ca2+-mediation of hypotonic and Na+-nutrient regulatory volume decrease in suspensions of jejunal enterocytes. J. Membr. Biol. 130:23-31.

    Google Scholar 

  111. Andrew, R. D. and Macvicar, B. A. 1994. Imaging cell volume changes and neuronal excitation in the hippocampal slice. Neuroscience. 62:371-383.

    Google Scholar 

  112. Albrecht, J. 1998. Roles of neuroactive amino acids in ammonia neurotoxicity. J. Neurosci. Res. 51:133-138.

    Google Scholar 

  113. Choi, D. W. 1992. Excitotoxic cell death. J. Neurobiol. 23: 1261-1276.

    Google Scholar 

  114. Torp, R., Andiné, P., Hagberg, H., Karagulle, T., Blackstad, T. W., and Ottersen, O. P. 1991. Cellular and subcellular redistribution of glutamate-, glutamine-and taurine-like immunoreactivities during forebrain ischemia: a semiquantitative electron microscopic study in rat hippocampus. Neuroscience 41:433-447.

    Google Scholar 

  115. Walz, W. 1987. Swelling and potassium uptake in cultured astrocytes. Can. J. Physiol. Pharmacol. 65:1051-1057.

    Google Scholar 

  116. Rossi, D. J., Oshima, T., and Attwell, D. 2000. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321.

    Google Scholar 

  117. Phillis, J. W., Song, D., and O'Regan, M. H. 1997. Inhibition by anion channel blockers of ischemia-evoked release of excitotoxic and other amino acids from rat cerebral cortex. Brain Res. 758:9-16.

    Google Scholar 

  118. Rutledge, E. M., Aschner, M., and Kimelberg, H. K. 1998. Pharmacological characterization of swelling-induced D-[3H]aspartate release from primary astrocyte cultures. Am. J. Physiol. 274:C1511-C1520.

    Google Scholar 

  119. Kempski, O., Staub, F., Schneider, G. H., Weigt, H., and Baethmann, A. 1992. Swelling of C6 glioma cells and astrocytes from glutamate, high K+concentrations or acidosis. Prog. Brain Res. 94:69-75.

    Google Scholar 

  120. Gotoh, M. and Davies, S. E., and Obrenovitch, T. P. 1997. Brain tissue acidosis: effects on the extracellular concentration of N-acetylaspartate. J. Neurochem. 69:655-661.

    Google Scholar 

  121. Phillis, J. W. and O'Regan, M. H. 1996. Mechanisms of glutamate and aspartate release in the ischemic rat cerebral cortex. Brain Res. 730:150-164.

    Google Scholar 

  122. Newsome, W. P., Warskulat, U., Noe, B., Wettstein, M., Stoll, B., Gerok, W., and Häausssinger, D. 1994. Modulation of phosphoenolpyruvate carboxykinase mRNA levels by the hepatocellular hydration state. Biochem. J. 304:555-560.

    Google Scholar 

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Pasantes-Morales, H., Cardin, V. & Tuz, K. Signaling Events during Swelling and Regulatory Volume Decrease. Neurochem Res 25, 1301–1314 (2000). https://doi.org/10.1023/A:1007652330703

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