A role of the sodium pump in spreading ischemia in rats

Journal of Cerebral Blood Flow and Metabolism

Volumn 37, Issue 5, 2017, Pages 1687-1705

  Major, Sebastian ^a   Petzold, Gabor C ^b   Reiffurth, Clemens ^a   Windmüller, Olaf ^c   Foddis, Marco ^a   Lindauer, Ute ^d   Kang, Eun Jeung ^a   Dreier, Jens P ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c Ruppiner Kliniken GmbH   (Germany)

^d UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

inverse coupling; migraine; Na+ K+ ATPase; Spreading depolarization; spreading depression; stroke; subarachnoid hemorrhage; vasospasm

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM; OUABAIN; POTASSIUM; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CALCIUM EXCHANGE PROTEIN; THAPSIGARGIN; ATP1A2 PROTEIN, RAT; ATP1A3 PROTEIN, RAT; POTASSIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; BRAIN PERICYTE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CEREBROSPINAL FLUID; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; ENZYME ACTIVITY; EX VIVO STUDY; IN VIVO STUDY; LASER DOPPLER FLOWMETRY; MALE; MEMBRANE DEPOLARIZATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPECTROPHOTOMETRY; SPREADING CORTICAL DEPRESSION; VASOCONSTRICTION; ANIMAL; BRAIN CIRCULATION; CHEMISTRY; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; BRAIN ISCHEMIA; CALCIUM; CEREBROSPINAL FLUID; CEREBROVASCULAR CIRCULATION; CORTICAL SPREADING DEPRESSION; ELECTROCORTICOGRAPHY; LASER-DOPPLER FLOWMETRY; MALE; POTASSIUM CHLORIDE; RATS, WISTAR; SODIUM-POTASSIUM-EXCHANGING ATPASE; SPECTROPHOTOMETRY; VASOCONSTRICTION;

EID: 85018743167     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X16639059     Document Type: Article

References (87)

1. Dreier JP and Reiffurth C. The stroke-migraine depolarization continuum. Neuron 2015; 86: 902-922.
2. Lauritzen M, Dreier JP, Fabricius M, et al. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 2011; 31: 17-35.
3. Piilgaard H and Lauritzen M. Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex. J Cereb Blood Flow Metab 2009; 29: 1517-1527.
4. Hadjikhani N, Sanchez Del Rio M, Wu O, et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 2001; 98: 4687-4692.
5. Dreier JP, Major S, Manning A, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009; 132(Pt 7): 1866-1881.
6. Woitzik J, Hecht N, Pinczolits A, et al. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology 2013; 80: 1095-1102.
7. Hinzman JM, Andaluz N, Shutter LA, et al. Inverse neurovascular coupling to cortical spreading depolarizations in severe brain trauma. Brain 2014; 137(Pt 11): 2960-2972.
8. Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011; 17: 439-447.
9. Dreier JP, Korner K, Ebert N, et al. Nitric oxide scavenging by hemoglobin or nitric oxide synthase inhibition by N-nitro-L-arginine induces cortical spreading ischemia when K+ is increased in the subarachnoid space. J Cereb Blood Flow Metab 1998; 18: 978-990.
10. Dreier JP, Ebert N, Priller J, et al. Products of hemolysis in the subarachnoid space inducing spreading ischemia in the cortex and focal necrosis in rats: a model for delayed ischemic neurological deficits after subarachnoid hemorrhage? J Neurosurg 2000; 93: 658-666.
11. Strong AJ, Anderson PJ, Watts HR, et al. Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain 2007; 130(Pt 4): 995-1008.
12. Shin HK, Dunn AK, Jones PB, et al. Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. J Cereb Blood Flow Metab 2006; 26: 1018-1030.
13. Bere Z, Obrenovitch TP, Bari F, et al. Ischemia-induced depolarizations and associated hemodynamic responses in incomplete global forebrain ischemia in rats. Neuroscience 2014; 260: 217-226.
14. Muller M and Somjen GG. Na(+) and K(+) concentrations, extra- and intracellular voltages, and the effect of TTX in hypoxic rat hippocampal slices. J Neurophysiol 2000; 83: 735-745.
15. Jiang HB, Yoneyama H, Furukawa A, et al. Effect of isosorbide dinitrate on nitric oxide synthase under hypoxia. Pharmacology 2001; 62: 10-16.
16. Windmuller O, Lindauer U, Foddis M, et al. Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 2005; 128(Pt 9): 2042-2051.
17. Petzold GC, Windmuller 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.
18. Dreier JP, Petzold G, Tille K, et al. Ischaemia triggered by spreading neuronal activation is inhibited by vasodilators in rats. J Physiol 2001; 531(Pt 2): 515-526.
19. Hajek I, Subbarao KV and Hertz L. Acute and chronic effects of potassium and noradrenaline on Na+, K+-ATPase activity in cultured mouse neurons and astrocytes. Neurochem Int 1996; 28: 335-342.
20. Levasseur JE, Wei EP, Raper AJ, et al. Detailed description of a cranial window technique for acute and chronic experiments. Stroke 1975; 6: 308-317.
21. Balestrino M, Young J and Aitken P. Block of (Na+,K+) ATPase with ouabain induces spreading depression-like depolarization in hippocampal slices. Brain Res 1999; 838: 37-44.
22. Dreier JP, Windmuller O, Petzold G, et al. Ischemia caused by inverse coupling between neuronal activation and cerebral blood flow in rats. In: Tomita M, Kanno I and Hamel E (eds). Brain activation and CBF control. Amsterdam: Elsevier, 2002, pp.487-492.
23. Sukhotinsky I, Dilekoz E, Moskowitz MA, et al. Hypoxia and hypotension transform the blood flow response to cortical spreading depression from hyperemia into hypoperfusion in the rat. J Cereb Blood Flow Metab 2008; 28: 1369-1376.
24. Petzold GC, Haack S, von Bohlen Und Halbach O, et al. Nitric oxide modulates spreading depolarization threshold in the human and rodent cortex. Stroke 2008; 39: 1292-1299.
25. Blaustein MP and Hamlyn JM. Signaling mechanisms that link salt retention to hypertension: endogenous ouabain, the Na(+) pump, the Na(+)/Ca(2+) exchanger and TRPC proteins. Biochim Biophys Acta 2010; 1802: 1219-1229.
26. Sagara Y, Fernandez-Belda F, de Meis L, et al. Characterization of the inhibition of intracellular Ca2+ transport ATPases by thapsigargin. J Biol Chem 1992; 267: 12606-12613.
27. Thastrup O, Cullen PJ, Drobak BK, et al. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA 1990; 87: 2466-2470.
28. Fabricius M, Akgoren N and Lauritzen M. Argininenitric oxide pathway and cerebrovascular regulation in cortical spreading depression. Am J Physiol 1995; 269(1 Pt 2): H23-H29.
29. Duckrow RB. A brief hypoperfusion precedes spreading depression if nitric oxide synthesis is inhibited. Brain Res 1993; 618: 190-195.
30. Ayata C and Lauritzen M. Spreading depression, spreading depolarizations, and the cerebral vasculature. Physiol Rev 2015; 95: 953-993.
31. Furchgott RF and Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980; 288: 373-376.
32. Ishiguro M, Morielli AD, Zvarova K, et al. Oxyhemoglobin-induced suppression of voltage-dependent K+ channels in cerebral arteries by enhanced tyrosine kinase activity. Circ Res 2006; 99: 1252-1260.
33. Koide M, Penar PL, Tranmer BI, et al. Heparin-binding EGF-like growth factor mediates oxyhemoglobininduced suppression of voltage-dependent potassium channels in rabbit cerebral artery myocytes. Am J Physiol Heart Circ Physiol 2007; 293: H1750-H1759.
34. Asano T. Oxyhemoglobin as the principal cause of cerebral vasospasm: a holistic view of its actions. Crit Rev Neurosurg 1999; 9: 303-318.
35. Forstermann U and Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 2012; 33: 829-837, 837 a-837 d.
36. Dietz RM, Weiss JH and Shuttleworth CW. Zn2+ influx is critical for some forms of spreading depression in brain slices. J Neurosci 2008; 28: 8014-8024.
37. Carvajal JA, Germain AM, Huidobro-Toro JP, et al. Molecular mechanism of cGMP-mediated smooth muscle relaxation. J Cell Physiol 2000; 184: 409-420.
38. Robertson BE, Schubert R, Hescheler J, et al. cGMPdependent protein kinase activates Ca-activated K channels in cerebral artery smooth muscle cells. Am J Physiol 1993; 265(1 Pt 1): C299-C303.
39. Archer SL, Huang JM, Hampl V, et al. Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin- sensitive K channel by cGMP-dependent protein kinase. Proc Natl Acad Sci USA 1994; 91: 7583-7587.
40. Ishikawa T, Hume JR and Keef KD. Regulation of Ca2+ channels by cAMP and cGMP in vascular smooth muscle cells. Circ Res 1993; 73: 1128-1137.
41. Tewari K and Simard JM. Sodium nitroprusside and cGMP decrease Ca2+ channel availability in basilar artery smooth muscle cells. Pflugers Arch 1997; 433: 304-311.
42. Ji J, Benishin CG and Pang PK. Nitric oxide selectively inhibits intracellular Ca++ release elicited by inositol trisphosphate but not caffeine in rat vascular smooth muscle. J Pharmacol Exp Ther 1998; 285: 16-21.
43. Yu JZ, Zhang DX, Zou AP, et al. Nitric oxide inhibits Ca(2+) mobilization through cADP-ribose signaling in coronary arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 2000; 279: H873-H881.
44. Li N, Zou AP, Ge ZD, et al. Effect of nitric oxide on calcium-induced calcium release in coronary arterial smooth muscle. Gen Pharmacol 2000; 35: 37-45.
45. Iadecola C and Zhang F. Permissive and obligatory roles of NO in cerebrovascular responses to hypercapnia and acetylcholine. Am J Physiol 1996; 271(4 Pt 2): R990-R1001.
46. Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014; 508: 55-60.
47. Petzold GC, Scheibe F, Braun JS, et al. Nitric oxide modulates calcium entry through P/Q-type calcium channels and N-methyl-d-aspartate receptors in rat cortical neurons. Brain Res 2005; 1063: 9-14.
48. Ulmer HJ, de Lima VM and Hanke W. Effects of nitric oxide on the retinal spreading depression. Brain Res 1995; 691: 239-242.
49. Leo L, Gherardini L, Barone V, et al. Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Genet 2011; 7: e1002129.
50. Pavlovic D, Hall AR, Kennington EJ, et al. Nitric oxide regulates cardiac intracellular Na(+) and Ca(2)(+) by modulating Na/K ATPase via PKCepsilon and phospholemman- dependent mechanism. J Mol Cell Cardiol 2013; 61: 164-171.
51. Jamme I, Barbey O, Trouve P, et al. Focal cerebral ischaemia induces a decrease in activity and a shift in ouabain affinity of Na+, K+-ATPase isoforms without modifications in mRNA and protein expression. Brain Res 1999; 819: 132-142.
52. Mishra OP and Delivoria-Papadopoulos M. Cellular mechanisms of hypoxic injury in the developing brain. Brain Res Bull 1999; 48: 233-238.
53. Lingrel JB. The physiological significance of the cardiotonic steroid/ouabain-binding site of the Na,K-ATPase. Annu Rev Physiol 2010; 72: 395-412.
54. Blanco G and Mercer RW. Isozymes of the Na-KATPase: heterogeneity in structure, diversity in function. Am J Physiol 1998; 275(5 Pt 2): F633-F650.
55. Juhaszova M and Blaustein MP. Distinct distribution of different Na+ pump alpha subunit isoforms in plasmalemma. Physiological implications. Ann NY Acad Sci 1997; 834: 524-536.
56. Pulina MV, Zulian A, Berra-Romani R, et al. Upregulation of Na+ and Ca2+ transporters in arterial smooth muscle from ouabain-induced hypertensive rats. Am J Physiol Heart Circ Physiol 2010; 298: H263-H274.
57. Blaustein MP. Physiological effects of endogenous ouabain: control of intracellular Ca2+ stores and cell responsiveness. Am J Physiol 1993; 264(6 Pt 1): C1367-C1387.
58. Reuter H, Pott C, Goldhaber JI, et al. Na(+)-Ca2+ exchange in the regulation of cardiac excitation-contraction coupling. Cardiovasc Res 2005; 67: 198-207.
59. James PF, Grupp IL, Grupp G, et al. Identification of a specific role for the Na,K-ATPase alpha 2 isoform as a regulator of calcium in the heart. Mol Cell 1999; 3: 555-563.
60. Arnon A, Hamlyn JM and Blaustein MP. Ouabain augments Ca(2+) transients in arterial smooth muscle without raising cytosolic Na(+). Am J Physiol Heart Circ Physiol 2000; 279: H679-H691.
61. Zlokovic BV, Mackic JB, Wang L, et al. Differential expression of Na,K-ATPase alpha and beta subunit isoforms at the blood-brain barrier and the choroid plexus. J Biol Chem 1993; 268: 8019-8025.
62. Iadecola C and Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci 2007; 10: 1369-1376.
63. Filosa JA, Bonev AD, Straub SV, et al. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 2006; 9: 1397-1403.
64. Girouard H, Bonev AD, Hannah RM, et al. Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 2010; 107: 3811-3816.
65. Horrigan FT and Aldrich RW. Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels. J Gen Physiol 2002; 120: 267-305.
66. Koide M, Bonev AD, Nelson MT, et al. Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. Proc Natl Acad Sci USA 2012; 109: E1387-E1395.
67. Harder DR, Gebremedhin D, Narayanan J, et al. Formation and action of a P-450 4A metabolite of arachidonic acid in cat cerebral microvessels. Am J Physiol 1994; 266(5 Pt 2): H2098-H2107.
68. Fordsmann JC, Ko RW, Choi HB, et al. Increased 20-HETE synthesis explains reduced cerebral blood flow but not impaired neurovascular coupling after cortical spreading depression in rat cerebral cortex. J Neurosci 2013; 33: 2562-2570.
69. Crago EA, Thampatty BP, Sherwood PR, et al. Cerebrospinal fluid 20-HETE is associated with delayed cerebral ischemia and poor outcomes after aneurysmal subarachnoid hemorrhage. Stroke 2011; 42: 1872-1877.
70. Dreier JP, Woitzik J, Fabricius M, et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006; 129(Pt 12): 3224-3237.
71. Bosche B, Graf R, Ernestus RI, et al. Recurrent spreading depolarizations after SAH decrease oxygen availability in human cerebral cortex. Ann Neurol 2010; 67: 607-617.
72. Borysova L, Wray S, Eisner DA, et al. How calcium signals in myocytes and pericytes are integrated across in situ microvascular networks and control microvascular tone. Cell Calcium 2013; 54: 163-174.
73. McNeish AJ, Dora KA and Garland CJ. Possible role for K+ in endothelium-derived hyperpolarizing factor-linked dilatation in rat middle cerebral artery. Stroke 2005; 36: 1526-1532.
74. Brayden JE and Wellman GC. Endothelium-dependent dilation of feline cerebral arteries: role of membrane potential and cyclic nucleotides. J Cereb Blood Flow Metab 1989; 9: 256-263.
75. Vergouwen MD, Etminan N, Ilodigwe D, et al. Lower incidence of cerebral infarction correlates with improved functional outcome after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab 2011; 31: 1545-1553.
76. Sakowitz OW, Wolfrum S, Sarrafzadeh AS, et al. Relation of cerebral energy metabolism and extracellular nitrite and nitrate concentrations in patients after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab 2001; 21: 1067-1076.
77. Macdonald RL, Pluta RM and Zhang JH. Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol 2007; 3: 256-263.
78. Terpolilli NA, Feiler S, Dienel A, et al. Nitric oxide inhalation reduces brain damage, prevents mortality, and improves neurological outcome after subarachnoid hemorrhage by resolving early pial microvasospasms. J Cereb Blood Flow Metab 2016; 36(12): 2096-2107.
79. Dreier J, Körner K, Back T, et al. Cortical spreading ischemia (CSI): A novel phenomenon induced by cortical spreading depression (CSD), NOS inhibition and elevated extracellular potassium. Soc Neurosci Abstr 1995; 21(Part 1): 225.
80. Dreier JP, Windmuller O, Petzold G, et al. Ischemia triggered by red blood cell products in the subarachnoid space is inhibited by nimodipine administration or moderate volume expansion/hemodilution in rats. Neurosurgery 2002; 51: 1457-1465. (discussion 1465-1467.
81. Allen GS, Ahn HS, Preziosi TJ, et al. Cerebral arterial spasm-a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N Engl J Med 1983; 308: 619-624.
82. Dirnagl U, Hakim A, Macleod M, et al. A concerted appeal for international cooperation in preclinical stroke research. Stroke 2013; 44: 1754-1760.
83. Feuerstein D, Takagaki M, Gramer M, et al. Detecting tissue deterioration after brain injury: regional blood flow level versus capacity to raise blood flow. J Cereb Blood Flow Metab 2014; 34: 1117-1127.
84. Ostergaard L, Dreier JP, Hadjikhani N, et al. Neurovascular coupling during cortical spreading depolarization and -depression. Stroke 2015; 46: 1392-1401.
85. Pluta RM, Dejam A, Grimes G, et al. Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. JAMA 2005; 293: 1477-1484.
86. Ehlert A, Schmidt C, Wolfer J, et al. Molsidomine for the prevention of vasospasm-related delayed ischemic neurological deficits and delayed brain infarction and the improvement of clinical outcome after subarachnoid hemorrhage: a single-center clinical observational study. J Neurosurg 2016; 124: 51-58.
87. Jakobsen CM, Denmeade SR, Isaacs JT, et al. Design, synthesis, and pharmacological evaluation of thapsigargin analogues for targeting apoptosis to prostatic cancer cells. J Med Chem 2001; 44: 4696-4703.