Ischemia-induced stimulation of cerebral microvascular endothelial cell Na-K-Cl cotransport involves p38 and JNK MAP kinases

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 3, 2012, Pages

  Wallace, Breanna K ^a   Jelks, Karen A ^a   O'Donnell, Martha E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Blood brain barrier; Bumetanide; Cerebral edema; SB 239063; SP 600125; Stroke

Indexed keywords

4 [4 (4 FLUOROPHENYL) 5 (2 METHOXY 4 PYRIMIDINYL) 1 IMIDAZOLYL]CYCLOHEXANOL; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BUMETANIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; RUBIDIUM 86; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOFLUORESCENCE; MALE; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING;

ANIMALS; ANTHRACENES; BLOOD-BRAIN BARRIER; BRAIN; BRAIN ISCHEMIA; BUMETANIDE; CATTLE; CELL HYPOXIA; CELLS, CULTURED; ENDOTHELIAL CELLS; IMIDAZOLES; INFARCTION, MIDDLE CEREBRAL ARTERY; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICROCIRCULATION; MICROVESSELS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIMIDINES; RUBIDIUM; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; STROKE;

RATTUS;

EID: 84856287555     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00261.2011     Document Type: Article

References (64)

1. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, Badger AM, Legos JJ, Erhardt JA, Ohlstein EH, Hunter AJ, Harrison DC, Philpott K, Smith BR, Adams JL, Parsons AA. Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med Res Rev 21: 129-145, 2001.
2. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, Badger AM, White RF, McVey MJ, Legos JJ, Erhardt JA, Nelson AH, Ohlstein EH, Hunter AJ, Ward K, Smith BR, Adams JL, Parsons AA. SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia. J Pharmacol Exp Ther 296: 312-321, 2001.
3. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, Bhagwat SS, Manning AM, Anderson DW. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 98: 13681-13686, 2001.
4. Betz AL. Alterations in cerebral endothelial cell function in ischemia. Adv Neurol 71: 301-313, 1996.
5. Bogoyevitch MA, Gillespie-Brown J, Ketterman AJ, Fuller SJ, Ben-Levy R, Ashworth A, Marshall CJ, Sugden PH. Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart-p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion. Circ Res 79: 162-173, 1996.
6. Borsello T, Clarke PGH, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9: 1180-1186, 2003.
7. Bourke RS, Kimelberg HK, Nelson LR, Barron KD, Auen EL, Popp AJ, Waldman JB. Biology of glial swelling in experimental brain edema. Adv Neurol 28: 99-109, 1980.
8. Brillault J, Lam TI, Rutkowsky JM, Foroutan S, O'Donnell ME. Hypoxia effects on cell volume and ion uptake of cerebral microvascular endothelial cells. Am J Physiol Cell Physiol 294: C88-C96, 2008.
9. Bronner LL, Kanter DS, Manson JE. Primary prevention of stroke. N Engl J Med 333: 1392-1400, 1995.
10. Carling D. The AMP-activated protein kinase cascade-a unifying system for energy control. Trends Biochem Sci 29: 18-24, 2004.
11. Chen YJ, Anderson SE, O'Donnell ME. Bumetanide and HOE642 administered after initiation of middle cerebral artery occlusion effectively reduce rat brain Na uptake and infarct (Abstract). FASEB J 23: A614.613, 2009.
12. Chen YJ, Lam TI, Anderson SE, Walton JH, O'Donnell ME. Bloodbrain barrier Na-K-Cl cotransporter and Na/H exchanger: therapeutic targets for ischemia-induced Na uptake and edema formation (Abstract). J Cereb Blood Flow Metab 29: S489, 2008.
13. Cowan KJ, Storey KB. Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J Exp Biol 206: 1107-1115, 2003.
14. - cotransport in primary afferent neurons. J Physiol 588: 3365-3373, 2010.
15. Ennis SR, Ren XD, Betz AL. Mechanisms of sodium transport at the blood-brain barrier studied with in situ perfusion of rat brain. J Neurochem 66: 756-763, 1996.
16. Ferrer I, Ballabriga J, Pozas E. Transient forebrain ischemia in the adult gerbil is associated with a complex c-Jun response. Neuroreport 8: 2483-2487, 1997.
17. Ferrer I, Friguls B, Dalfo E, Planas AM. Early modifications in the expression of mitogen-activated protein kinase (MAPK/ERK), stressactivated kinases SAPK/JNK and p38, and their phosphorylated substrates following focal cerebral ischemia. Acta Neuropathol (Berl) 105: 425-437, 2003.
18. - cotransporter. Am J Physiol Cell Physiol 289: C1492-C1501, 2005.
19. Gamba G, Garbarini NJ, Delpire E. Regulation of cation-chloride cotransproters. In: Physiology and Pathology of Chloride Transporters and Channels in the Nervous System: From Molecular to Diseases, edited by Alvarez-Leefmans FJ, Delpire E. London: Academic, 2009, p. 357-381.
20. Giménez K. Molecular mechanism and regulation of furosemide-sensitive Na-K-Cl cotransporters. Curr Opin Nephrol Hypertens 15: 517-523, 2006.
21. Gotoh O, Asano T, Koide T, Takakura K. Ischemic brain edema following occlusion of the middle cerebral artery in the rat. I. The time courses of the brain water, sodium and potassium contents and blood-brain barrier permeability to 125I-albumin. Stroke 16: 101-109, 1985.
22. Guo Y, Signore AP, Yin W, Cao G, Yin XM, Sun F, Luo Y, Graham SH, Chen J. Neuroprotection against focal ischemic brain injury by inhibition of c-Jun N-terminal kinase and attenuation of the mitochondrial apoptosis-signaling pathway. J Cereb Blood Flow Metab 25: 694-712, 2005.
23. Hardie DG. The AMP-activated protein kinase pathway-new players upstream and downstream. J Cell Sci 117: 5479-5487, 2004.
24. Hardie DG. The AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144: 5179-5183, 2003.
25. Hatashita S, Hoff JT. Brain edema and cerebrovascular permeability during cerebral ischemia in rats. Stroke 21: 582-588, 1990.
26. Herdegen T, Claret FX, Martin-Villalba A, Winter C, Hunter T, Karin M. Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury. J Neurosci 18: 5124-5135, 1998.
27. Hu BR, Liu CL, Park DJ. Alteration of MAP kinase pathways after transient forebrain ischemia. J Cereb Blood Flow Metab 20: 1089-1095, 2000.
28. Iadecola C. Mechanisms of cerebral ischemic damage. In: Cerebral Ischemia: Molecular and Cellular Pathophysiology, edited by Walz W. Totowa, NJ: Humana, 1999, p. 3-34.
29. Irving EA, Bamford M. Role of mitogen-and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab 22: 631-647, 2002.
30. Irving EA, Barone FC, Reith AD, Hadingham SJ, Parsons AA. Differential activation of MAPK/ERK and p38/SAPK in neurones and glia following focal cerebral ischaemia in the rat. Brain Res Mol Brain Res 77: 65-75, 2000.
31. Kahle KT, Rinehart J, Lifton RP. Phosphoregulation of the Na-K-2Cl and K-Cl cotransporters by the WNK kinases. Biochim Biophys Acta 1802: 1150-1158, 2010.
32. - flux by altering the phosphorylation state of the Na-K-Cl and K-Cl cotransporters. Physiology (Bethesda) 21: 326-335, 2006.
33. - cotransport in cultured brain capillary endothelial cells of the rat. J Neurochem 66: 2572-2579, 1996.
34. Keep RF. Potassium transport at the blood-brain and blood-CSF barriers. In: Frontiers in Cerebral Vascular Biology: Transport and Its Regulation, edited by Drewes LR, Betz AL. New York: Plenum, 1993, p. 43-54.
35. Kimelberg HK. Current concepts of brain edema. Rev Lab Invest J Neurosurg 83: 1051-1059, 1995.
36. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81: 807-869, 2001.
37. Lam TI, Wise PM, O'Donnell ME. Cerebral microvascular endothelial cell Na/H exchange: evidence for the presence of NHE1 and NHE2 isoforms and regulation by arginine vasopressin. Am J Physiol Cell Physiol 297: C278-C289, 2009.
38. Lee SR, Lo EH. Interactions between p38 mitogen-activated protein kinase and caspase-3 in cerebral endothelial cell death after hypoxiareoxygenation. Stroke 34: 2704-2709, 2003.
39. Legos JL, McLaughlin B, Skaper SD, Strijbos PJLM, Parsons AA, Aizenman E, Herin GA, Barone FC, Erhardt JA. The selective p38 inhibitor SB-239063 protects primary neurons from mild to moderate excitotoxic injury. Eur J Pharmacol 447: 37-42, 2002.
40. Li J, McCullough LD. Effects of AMP-activated protein kinase in cerebral ischemia. J Cereb Blood Flow Metab 30: 480-492, 2010.
41. Li J, Zeng Z, Viollet B, Ronnett GV, McCullough LD. Neuroprotective effects of adenosine monophosphate-activated protein kinase inhibition and gene deletion in stroke. Stroke 38: 2992-2999, 2007.
42. Li Y, Hu J, Vita R, Sun B, Tabata H, Altman A. SPAK kinase is a substrate and target of PKCθ in T-cell receptor-induced AP-1 activation pathway. EMBO J 23: 1112-1122, 2004.
43. McCullough LD, Zeng Z, Li H, Landree LE, McFadden J, Ronnett GV. Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke. J Biol Chem 280: 20493-204502, 2005.
44. Menzies SA, Betz AL, Hoff JT. Contributions of ions and albumin to the formation and resolution of ischemic brain edema. J Neurosurg 78: 257-266, 1993.
45. Menzies SA, Hoff JT, Betz AL. Extravasation of albumin in ischaemic brain oedema. Acta Neurochir (Wien) 51: 220-222, 1990.
46. Neuwelt EA, Bauer B, Fahlke C, Fricker G, Iadecola C, Janigro D, Leybaert L, Molnár Z, O'Donnell ME, Povlishock JT, Saunders NR, Sharp F, Stanimirovic D, Watts RJ, Drewed LR. Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 12: 169-182, 2011.
47. Nito C, Kamada H, Endo H, Niizuma K, Myer DJ, Chan PH. Role of the p38 mitogen-activated protein kinase/cytosolic phospholipase A2 signaling pathway in blood-brain barrier disruption after focal cerebral ischemia and reperfusion. J Cereb Blood Flow Metab 28: 1686-1696, 2008.
48. O'Donnell ME. Ion and water transport across the blood-brain barrier. In: Physiology and Pathology of Chloride Transporters and Channels in the Nervous System, edited by Alvarez-Leefmans FJ, Delpire E. London: Academic, 2009, p. 585-606.
49. O'Donnell ME, Duong V, Suvatne J, Foroutan S, Johnson DM. Arginine vasopressin stimulation of cerebral microvascular endothelial cell Na-K-Cl cotransporter activity is V1 receptor and [Ca] dependent. Am J Physiol Cell Physiol 289: C283-C292, 2005.
50. O'Donnell ME, Martinez A, Sun D. Cerebral microvascular endothelial cell Na-K-Cl cotransport: regulation by astrocyte-conditioned medium. Am J Physiol Cell Physiol 268: C747-C754, 1995.
51. O'Donnell ME, Tran L, Lam TI, Liu XB, Anderson SE. Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J Cereb Blood Flow Metab 24: 1046-1056, 2004.
52. - cotransporter in the nervous system. Evidence for a scaffolding role of the kinase. J Biol Chem 278: 52848-52856, 2003.
53. Schielke GP, Moises HC, Betz AL. Blood to brain sodium transport and interstitial fluid potassium concentration during focal ischemia in the rat. J Cereb Blood Flow Metab 11: 466-471, 1991.
54. Smith L, Smallwood N, Altman A, Liedtke CM. PKCθ acts upstream of SPAK in the activation of NKCC1 by hyperosmotic stress in human airway epithelial cells. J Biol Chem 283: 22147-22156, 2008.
55. Strassburger M, Braun H, Reymann KG. Anti-inflammatory treatment with the p38 mitogen-activated protein kinase inhibitor SB239063 is neuroprotective, decreases the number of activated microglia and facilitates neurogenesis in oxygen-glucose-deprived hippocampal slice cultures. Eur J Pharmacol 592: 55-61, 2008.
56. Sugino T, Nozaki K, Takagi Y, Hattori I, Hashimoto N, Moriguchi T, Nishida E. Activation of mitogen-activated protein kinases after transient forebrain ischemia in gerbil hippocampus. J Neurosci 20: 4506-4514, 2000.
57. Takagi Y, Nozaki K, Sugino T, Hattori I, Hashimoto N. Phosphorylation of c-Jun NH2-terminal kinase and p38 mitogen-activated protein kinase after transient forebrain ischemia in mice. Neurosci Lett 294: 117-120, 2000.
58. Tian D, Litvak V, Lev S. Cerebral ischemia and seizures induce tyrosine phosphorylation of PYK2 in neurons and microglial cells. J Neurosci 20: 6478-6487, 2000.
59. Waetzig V, Herdegen T. Context-specific inhibition of JNKx: overcoming the dilemma or protection and damage. Trends Pharmacol Sci 26: 454-461, 2005.
60. Wallace BK, Foroutan S, O'Donnell ME. Ischemia-induced stimulation of Na-K-Cl cotransport in cerebral microvascular endothelial cells involves AMP kinase. Am J Physiol Cell Physiol 301: C316-C326, 2011.
61. Wu DC, Ye W, Che XM, Yang GY. Activation of mitogen-activated protein kinases after permanent cerebral artery occlusion in mouse brain. J Cereb Blood Flow Metab 20: 1320-1330, 2000.
62. Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH. Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res 85: 1436-1448, 2007.
63. Zhu Y, Mao XO, Sun Y, Xia Z, Greenberg DA. p38 Mitogen-activated protein kinase mediates hypoxic regulation of Mdm2 and p53 in neurons. J Biol Chem 277: 22909-22914, 2002.
64. Zhu Y, Sun Y, Xie L, Jin K, Sheibani N, Greenberg DA. Hypoxic induction of endoglin via mitogen-activated protein kinases in mouse brain microvascular endothelial cells. Stroke 34: 2483-2488, 2003.