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

Neuropathology

Volumn 31, Issue 3, 2011, Pages 250-264

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

^a CHINA MEDICAL UNIVERSITY   (China)

^b LIAONING UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Bumetanide; Elevated potassium concentration; Hypotonicity; Na+,K+,2Cl cotransporter; Src; Transactivation

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; BUMETANIDE; COTRANSPORTER; EPIDERMAL GROWTH FACTOR RECEPTOR; ETACRYNIC ACID; FUROSEMIDE; ILOMASTAT; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POTASSIUM; SODIUM;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CELL SWELLING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE DELETION; IMMUNOPRECIPITATION; MOUSE; MUSCLE HYPOTONIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM DEPLETION; TRAUMATIC BRAIN INJURY; WATER INTOXICATION; WESTERN BLOTTING;

ADAM PROTEINS; ANIMALS; ASTROCYTES; BRAIN EDEMA; BUMETANIDE; CELL DIVISION; CELLS, CULTURED; CHELATING AGENTS; EGTAZIC ACID; HYPOTONIC SOLUTIONS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; POTASSIUM; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SRC-FAMILY KINASES; WATER INTOXICATION;

EID: 79957542880     PISSN: 09196544     EISSN: 14401789     Source Type: Journal    
DOI: 10.1111/j.1440-1789.2010.01172.x     Document Type: Article

References (74)

1. Chvátal A, Anderová M, Hock M etal. 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 etal. 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 etal. 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 etal. 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 etal. 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. 2+ 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 etal. 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 etal. 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 etal. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 2007; 6: 258-268.
15. Lu KT, Cheng NC, Wu CY etal. 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 etal. 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 etal. 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 etal. 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 etal. 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 etal. 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 etal. 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. + 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 etal. 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 etal. 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 etal. 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: Hertz L, ed. Non-neuronal Cells of the Nervous System: Function and Dysfunction. Amsterdam: Elsevier, 2004; 503-518.
30. Peng L, Li B, Du T etal. 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 etal. 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 etal. 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 etal. 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 etal. 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 etal. 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 etal. Glial swelling and astrogliosis produce diffusion barriers in the rat spinal cord. Glia 1999; 25: 56-70.
46. Favata MF, Horiuchi KY, Manos EJ etal. 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 etal. 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: Lajtha A, ed. Handbook of Neurochemistry. New York: Plenum Press, 1985; 603-661.
50. Deshmukh HS, Case LM, Wesselkamper SC etal. Metalloproteinases mediate mucin 5AC expression by epidermal growth factor receptor activation. Am J Respir Crit Care Med 2005; 171: 305-314.
51. 2B 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 etal. 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 etal. 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 etal. 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 etal. On the role of G-protein coupled receptors in cell volume regulation. Cell Physiol Biochem 2008; 21: 1-14.
58. - 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 etal. 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. - cotransporter. Am J Physiol 1999; 277: 1184-1193.
62. Vitari AC, Thastrup J, Rafiqi FH etal. 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 etal. Astrocyte swelling leads to membrane unfolding, not membrane insertion. J Neurochem 2006; 99: 514-523.
66. Rojas A, Ramos M, benaim G etal. 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 etal. Physiology of cell volume regulation in vertebrates. Physiol Rev 2009; 89: 193-277.
69. Schliess F, Sinning R, Fischer R etal. 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 etal. 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 etal. Role of raf in vascular protection from distinct apoptotic stimuli. Science 2003; 301: 94-96.
73. Xia F, Li J, Hickey GW etal. Raf activation is regulated by tyrosine 510 phosphorylation in Drosophila. PLoS Biol 2008; 6: e128.
74. Ahn S, Shenoy SK, Wei H etal. 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.