Artigo Revisado por pares

Astrocyte ERK phosphorylation precedes K+-induced swelling but follows hypotonicity-induced swelling

2010; Wiley; Volume: 31; Issue: 3 Linguagem: Inglês

10.1111/j.1440-1789.2010.01172.x

ISSN

1440-1789

Autores

Liping Cai, Ting Du, Dan Song, Baoman Li, Leif Hertz, Liang Peng,

Tópico(s)

Neuroscience and Neuropharmacology Research

Resumo

NeuropathologyVolume 31, Issue 3 p. 250-264 Astrocyte ERK phosphorylation precedes K+-induced swelling but follows hypotonicity-induced swelling Liping Cai, Liping Cai Department of Clinical Pharmacology, China Medical University Laboratory of Molecular Biology, Liaoning University of Traditional Chinese Medicine, Shenyang, ChinaSearch for more papers by this authorTing Du, Ting Du Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorDan Song, Dan Song Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorBaoman Li, Baoman Li Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorLeif Hertz, Leif Hertz Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorLiang Peng, Corresponding Author Liang Peng Department of Clinical Pharmacology, China Medical UniversityLiang Peng, MD PhD, College of Basic Medical Sciences, China Medical University, No. 92 Beier Road, Heping District, Shenyang 110001, China. Email: [email protected]Search for more papers by this author Liping Cai, Liping Cai Department of Clinical Pharmacology, China Medical University Laboratory of Molecular Biology, Liaoning University of Traditional Chinese Medicine, Shenyang, ChinaSearch for more papers by this authorTing Du, Ting Du Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorDan Song, Dan Song Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorBaoman Li, Baoman Li Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorLeif Hertz, Leif Hertz Department of Clinical Pharmacology, China Medical UniversitySearch for more papers by this authorLiang Peng, Corresponding Author Liang Peng Department of Clinical Pharmacology, China Medical UniversityLiang Peng, MD PhD, College of Basic Medical Sciences, China Medical University, No. 92 Beier Road, Heping District, Shenyang 110001, China. Email: [email protected]Search for more papers by this author First published: 01 December 2010 https://doi.org/10.1111/j.1440-1789.2010.01172.xCitations: 25 L. Cai and T. Du contributed equally to this article. Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Hypotonicity following water intoxication and/or salt loss leads to mainly astrocytic brain swelling. Astrocytic swelling also occurs following brain trauma or ischemia, together with an increase in extracellular K+ ([K+]o), stimulating a bumetanide/furosemide/ethacrynic acid-inhibitable cotransporter, NKCC1, that accumulates Na+ and K+ together with 2 Cl- and osmotically obliged water. Either type of swelling may become fatal and is associated with phosphorylation of extracellular regulated kinases 1 and 2 (ERK1/2). Only the swelling associated with elevated [K+]o, leads to an increase in astrocytic proliferation and in expression of the astrocytic marker, glial fibrillary acidic protein. These differences prompted us to investigate key aspects of the molecular pathways between hypotonicity-induced and high-K+-mediated swelling in primary cultures of mouse astrocytes. In the latter Ca2+-mediated, AG1478-inhibitable transactivation of the epidermal growth factor (EGF) receptor leads, via bumetanide-inhibitable activation of the mitogen activated protein (MAP) kinase pathway to ERK phosphorylation and to NKCC1-mediated swelling. In the former, inhibition of the MAP kinase pathway, but not of EGF receptor activation, abolishes ERK phosphorylation, but has no effect on swelling, indicating that activation of ERK is a result, not a cause, of the swelling. REFERENCES 1 Chvátal A, Anderová M, Hock M et al. Three-dimensional confocal morphometry reveals structural changes in astrocyte morphology in situ. J Neurosci Res 2007; 85: 260–271. 2 Nase G, Helm PJ, Enger R et al. Water entry into astrocytes during brain edema formation. Glia 2008; 56: 895–902. 3 Ayus JC, Achinger SG, Arieff A. Brain cell volume regulation in hyponatremia: role of sex, age, vasopressin, and hypoxia. Am J Physiol Renal Physiol 2008; 295: 619–624. 4 Cruz-Rangel S, Hernández-Benítez R, Vázquez-Juárez E et al. Potentiation by thrombin of hyposmotic glutamate and taurine efflux from cultured astrocytes: signalling chains. Neurochem Res 2008; 33: 1518–1524. 5 Lezama R, Ortega A, Ordaz B et al. Hyposmolarity-induced ErbB4 phosphorylation and its influence on the non-receptor tyrosine kinase network response in cultured cerebellar granule neurons. J Neurochem 2005; 93: 1189–1198. 6 Nedergaard M, Hansen AJ. Characterization of cortical depolarizations evoked in focal cerebral ischemia. J Cereb Blood Flow Metab 1993; 13: 568–574. 7 Petzold GC, Windmüller O, Haack S et al. Increased extracellular K+ concentration reduces the efficacy of N-methyl-D-aspartate receptor antagonists to block spreading depression-like depolarizations and spreading ischemia. Stroke 2005; 36: 1270–1277. 8 Klatzo I. Pathophysiological aspects of brain edema. Acta Neuropathol 1987; 72: 236–239. 9 Hansen AJ, Nedergaard M. Brain ion homeostasis in cerebral ischemia. Neurochem Pathol 1988; 9: 195–209. 10 Nilsson P, Hillered L, Olsson Y et al. Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J Cereb Blood Flow Metab 1993; 13: 183–192. 11 Gidö G, Kristián T, Siesjö BK. Extracellular potassium in a neocortical core area after transient focal ischemia. Stroke 1997; 28: 206–210. 12 Alessandrini A, Namura S, Moskowitz MA et al. MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc Natl Acad Sci USA 1999; 96: 12866–12869. 13 Reinert M, Khaldi A, Zauner A et al. High extracellular potassium and its correlates after severe head injury: relationship to high intracranial pressure. Neurosurg Focus 2000; 8: e10. 14 Simard JM, Kent TA, Chen M et al. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 2007; 6: 258–268. 15 Lu KT, Cheng NC, Wu CY et al. NKCC1-mediated traumatic brain injury-induced brain edema and neuron death via Raf/MEK/MAPK cascade. Crit Care Med 2008; 36: 917–922. 16 Li L, Xiong Y, Qu Y et al. The requirement of extracellular signal-related protein kinase pathway in the activation of hypoxia inducible factor 1 alpha in the developing rat brain after hypoxia-ischemia. Acta Neuropathol 2008; 115: 297–303. 17 Pedersen SF, O'Donnell ME, Anderson SE et al. Physiology and pathophysiology of Na+/H+ exchange and Na+ -K+ -2Cl- cotransport in the heart, brain, and blood. Am J Physiol Regul Integr Comp Physiol 2006; 291: 1–25. 18 Su G, Haworth RA, Dempsey RJ et al. Regulation of Na(+)-K(+)-Cl(−) cotransporter in primary astrocytes by dibutyryl cAMP and high [K(+)](o). Am J Physiol Cell Physiol 2000; 279: 1710–1721. 19 Zhao Z, Hertz L, Code WE. Effects of benzodiazepines on potassium-induced increase in free cytosolic calcium concentration in astrocytes: interactions with nifedipine and the peripheral-type benzodiazepine antagonist PK 11195. Can J Physiol Pharmacol 1996; 74: 273–277. 20 Kanaka C, Ohno K, Okabe A et al. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 2001; 104: 933–946. 21 Mikawa S, Wang C, Shu F et al. Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Dev Brain Res 2002; 136: 93–100. 22 Chen Y, McNeill JR, Hajek I et al. Effect of vasopressin on brain swelling at the cellular level: do astrocytes exhibit a furosemide-vasopressin-sensitive mechanism for volume regulation? Can J Physiol Pharmacol 1992; 70 (Suppl): 367–373. 23 Del Bigio MR, Omara F, Fedoroff S. Astrocyte proliferation in culture following exposure to potassium ion. Neuroreport 1994; 5: 639–641. 24 Kimelberg HK, Rutledge E, Goderie S et al. Astrocytic swelling due to hypotonic or high K+ medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 1995; 15: 409–416. 25 Su G, Kintner DB, Flagella M et al. Astrocytes from Na(+)-K(+)-Cl(−) cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am J Physiol Cell Physiol 2002; 282: 1147–1160. 26 Su G, Kintner DB, Sun D. Contribution of Na(+)-K(+)-Cl(−) cotransporter to high-[K(+)](o)- induced swelling and EAA release in astrocytes. Am J Physiol Cell Physiol 2002; 282: 1136–1146. 27 Zwick E, Daub H, Aoki N et al. Critical role of calcium-dependent epidermal growth factor receptor transactivation in PC12 cell membrane depolarization and bradykinin signaling. J Biol Chem 1997; 272: 24767–24770. 28 Pierce KL, Tohgo A, Ahn S et al. Epidermal growth factor (EGF) receptor-dependent ERK activation by G protein-coupled receptors: a co-culture system for identifying intermediates upstream and downstream of heparin-binding EGF shedding. J Biol Chem 2001; 276: 23155–23160. 29 Peng L. Transactivation in astrocytes as a novel mechanism of neuroprotection. In: L Hertz, ed. Non-neuronal Cells of the Nervous System: Function and Dysfunction. Amsterdam: Elsevier, 2004; 503–518. 30 Peng L, Li B, Du T et al. Astrocytic transactivation by alpha(2)-adrenergic and 5-HT(2B) serotonergic signaling. Neurochem Int 2010; 57: 421–431. 31 Grobelny D, Poncz L, Galardy RE. Inhibition of human skin fibroblast collagenase, thermolysin, and Pseudomonas aeruginosa elastase by peptide hydroxamic acids. Biochemistry 1992; 31: 7152–7154. 32 Levitzki A, Gazit A. Tyrosine kinase inhibition: an approach to drug development. Science 1995; 267: 1782–1788. 33 Li B, Du T, Li H et al. Signaling pathways for EGFR transactivation in astrocytes by dexmedetomidine, an alpha2-adrenergic agonist, and its paracrine neuronal effect. Br J Pharmacol 2008; 154: 191–203. 34 Luttrell LM, Daaka Y, Della Rocca GJ et al. G protein-coupled receptors mediate two functionally distinct pathways of tyrosine phosphorylation in rat 1a fibroblasts. Shc phosphorylation and receptor endocytosis correlate with activation of Erk kinases. J Biol Chem 1997; 272: 31648–31656. 35 Häussinger D, Kurz AK, Wettstein M et al. Involvement of integrins and Src in tauroursodeoxycholate-induced and swelling-induced choleresis. Gastroenterology 2003; 124: 1476–1487. 36 Amoui M, Dráber P, Dráberová L. Src family-selective tyrosine kinase inhibitor, PP1, inhibits both Fc epsilonRI- and Thy-1-mediated activation of rat basophilic leukemia cells. Eur J Immunol 1997; 27: 1881–1886. 37 Kimelberg HK, O'Connor E. Swelling of astrocytes causes membrane potential depolarization. Glia 1988; 1: 219–224. 38 Del Bigio MR, Fedoroff S. Swelling of astroglia in vitro and the effect of arginine vasopressin and atrial natriuretic peptide. Acta Neurochir Suppl (Wien) 1990; 51: 14–16. 39 Sarfaraz D, Fraser CL. Effects of arginine vasopressin on cell volume regulation in brain astrocyte in culture. Am J Physiol 1999; 276: 596–601. 40 Hertz L, Chen Y, Spatz M. Involvement of non-neuronal brain cells in AVP-mediated regulation of water space at the cellular, organ, and whole-body level. J Neurosci Res 2000; 62: 480–490. 41 Du T, Song D, Li H et al. Stimulation by vasopressin of ERK phosphorylation and vector-driven water flux in astrocytes is transactivation-dependent. Eur J Pharmacol 2008; 587: 73–77. 42 Kimelberg HK, Frangakis MV. Furosemide- and bumetanide-sensitive ion transport and volume control in primary astrocyte cultures from rat brain. Brain Res 1985; 361: 125–134. 43 Walz W, Hertz L. Intense furosemide-sensitive potassium accumulation in astrocytes in the presence of pathologically high extracellular potassium levels. J Cereb Blood Flow Metab 1984; 4: 301–304. 44 Tas PW, Massa PT, Kress HG et al. Characterization of an Na+/K+/Cl- co-transport in primary cultures of rat astrocytes. Biochim Biophys Acta 1987; 903: 411–416. 45 Syková E, Vargová L, Prokopová S et al. Glial swelling and astrogliosis produce diffusion barriers in the rat spinal cord. Glia 1999; 25: 56–70. 46 Favata MF, Horiuchi KY, Manos EJ et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 1998; 273: 18623–18632. 47 Hertz L, Schousboe A, Boechler N et al. Kinetic characteristics of the glutamate uptake into normal astrocytes in cultures. Neurochem Res 1978; 3: 1–14. 48 Hertz L, Peng L, Lai JC. Functional studies in cultured astrocytes. Methods 1998; 16: 293–310. 49 Hertz L, Juurlink BHJ, Szuchet S. Cell cultures. In: A Lajtha, ed. Handbook of Neurochemistry. New York: Plenum Press, 1985; 603–661. 50 Deshmukh HS, Case LM, Wesselkamper SC et al. Metalloproteinases mediate mucin 5AC expression by epidermal growth factor receptor activation. Am J Respir Crit Care Med 2005; 171: 305–314. 51 Kong EK, Peng L, Chen Y et al. Up-regulation of 5-HT2B receptor density and receptor-mediated glycogenolysis in mouse astrocytes by long-term fluoxetine administration. Neurochem Res 2002; 27: 113–120. 52 Majka S, McGuire PG, Das A. Regulation of matrix metalloproteinase expression by tumor necrosis factor in a murine model of retinal neovascularization. Invest Ophthalmol Vis Sci 2002; 43: 260–266. 53 Marjou AE, Delouvée A, Thiery JP et al. Involvement of epidermal growth factor receptor in chemically induced mouse bladder tumour progression. Carcinogenesis 2000; 21: 2211–2218. 54 Solenov E, Watanabe H, Manley GT et al. Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 2004; 286: 426–432. 55 Petito CK, Juurlink BH, Hertz L. In vitro models differentiating between direct and indirect effects of ischemia on astrocytes. Exp Neurol 1991; 113: 364–372. 56 Benesova J, Hock M, Butenko O et al. Quantification of astrocyte volume changes during ischemia in situ reveals two populations of astrocytes in the cortex of GFAP/EGFP mice. J Neurosci Res 2009; 87: 96–111. 57 Vázquez-Juárez E, Ramos-Mandujano G, Hernández-Benítez R et al. On the role of G-protein coupled receptors in cell volume regulation. Cell Physiol Biochem 2008; 21: 1–14. 58 Panet R, Eliash M, Atlan H. Na+/K+/Cl- cotransporter activates MAP-kinase cascade downstream to protein kinase C, and upstream to MEK. J Cell Physiol 2006; 206: 578–585. 59 Meyer M, Maly K, Uberall F et al. Stimulation of K+ transport systems by Ha-ras. J Biol Chem 1991; 266: 8230–8235. 60 Lytle C, Forbush B 3rd. The Na–K–Cl cotransport protein of shark rectal gland. II. Regulation by direct phosphorylation. J Biol Chem 1992; 267: 25438–25443. 61 Kurihara K, Moore-Hoon ML, Saitoh M et al. Characterization of a phosphorylation event resulting in upregulation of the salivary Na+–K+–2Cl- cotransporter. Am J Physiol 1999; 277: 1184–1193. 62 Vitari AC, Thastrup J, Rafiqi FH et al. Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 2006; 397: 223–231. 63 Delpire E, Gagnon KB. SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem J 2008; 409: 321–331. 64 Fischer R, Schliess F, Häussinger D. Characterization of the hypo-osmolarity-induced Ca2+ response in cultured rat astrocytes. Glia 1997; 20: 51–58. 65 Pangrsic T, Potokar M, Haydon PG et al. Astrocyte swelling leads to membrane unfolding, not membrane insertion. J Neurochem 2006; 99: 514–523. 66 Rojas A, Ramos M, benaim G et al. The activity of the Na+/Ca2+ exchanger largely modulates the Ca2+i signal induced by hypo-osmotic stress in rat cerebellar astrocytes. The effect of osmolarity on exchange activity. J Physiol Sci 2008; 58: 277–279. 67 Pasantes-Morales H, Lezama RA, Ramos-Mandujano G. Tyrosine kinases and osmolyte fluxes during hyposmotic swelling. Acta Physiol (Oxf) 2006; 187: 93–102. 68 Hoffmann EK, Lambert IH, Pedersen SF et al. Physiology of cell volume regulation in vertebrates. Physiol Rev 2009; 89: 193–277. 69 Schliess F, Sinning R, Fischer R et al. Calcium-dependent activation of Erk-1 and Erk-2 after hypo-osmotic astrocyte swelling. Biochem J 1996; 320: 167–171. 70 Crépel V, Panenka W, Kelly Me et al. Mitogen-activated protein and tyrosine kinases in the activation of astrocyte volume-activated chloride current. J Neurosci 1998; 18: 1196–1206. 71 Stokoe D, McCormick F. Activation of c-Raf-1 by Ras and Src through different mechanisms: activation in vivo and in vitro. EMBO J 1997; 16: 2384–2396. 72 Alavi A, Hood JD, Frausto R et al. Role of raf in vascular protection from distinct apoptotic stimuli. Science 2003; 301: 94–96. 73 Xia F, Li J, Hickey GW et al. Raf activation is regulated by tyrosine 510 phosphorylation in Drosophila. PLoS Biol 2008; 6: e128. 74 Ahn S, Shenoy SK, Wei H et al. Differential kinetic and spatial patterns of beta-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J Biol Chem 2004; 279: 35518–35525. Citing Literature Volume31, Issue3June 2011Pages 250-264 ReferencesRelatedInformation

Referência(s)
Altmetric
PlumX