Capillary endothelial na+, k+, atpase transporter homeostasis and a new theory for migraine pathophysiology

Headache

Volumn 50, Issue 3, 2010, Pages 459-478

  Harrington, Michael G ^a   Fonteh, Alfred N ^a   Arakaki, Xianghong ^a   Cowan, Robert P ^a   Ecke, Laurel E ^a,c   Foster, Hailey ^a   Hühmer, Andreas F ^b   Biringer, Roger G ^b  

^a HMRI Molecular Neurology   (United States)

^b Thermo Fisher Scientific   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Capillary endothelial cell (CEC); Cerebrospinal fluid; K+ ATPase transporter (NKAT); Na+

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM ION; CANNABINOID; CHLORIDE ION; DOPAMINE; ESTROGEN; GLUTAMIC ACID; IONOTROPIC RECEPTOR; KAINIC ACID; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; NEUROTRANSMITTER; NORADRENALIN; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; POTASSIUM ION; SATURATED FATTY ACID; SEROTONIN 3 RECEPTOR; SODIUM CHANNEL; SODIUM ION; VOLTAGE GATED CALCIUM CHANNEL;

AGING; ALZHEIMER DISEASE; ANOXIA; APOPTOSIS; ASTROCYTE; ATAXIA; BLOOD BRAIN BARRIER; BLOOD VESSEL; BRAIN INFARCTION; CAPILLARY ENDOTHELIUM; CELL CULTURE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CIRCADIAN RHYTHM; DEHYDRATION; DEPOLARIZATION; ECTODERM; ELECTROLYTE METABOLISM; ENDOTHELIUM CELL; EXCITOTOXICITY; EYE MOVEMENT; GLIA CELL; HEADACHE; HUMAN; IN VIVO STUDY; INTERSTITIAL FLUID; LOCUS CERULEUS; MIGRAINE; MIGRAINE WITH AURA; NAUSEA; NERVE CELL; NERVE CELL EXCITABILITY; NEUROPATHIC PAIN; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PHONOPHOBIA; PHOTOPHOBIA; POTASSIUM BLOOD LEVEL; PRIORITY JOURNAL; REVIEW; SALIVARY GLAND; SALT INTAKE; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; SLEEP DISORDER; SODIUM CELL LEVEL; SODIUM TRANSPORT; SPINAL CORD INJURY; TELENCEPHALON; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; BRAIN; CEREBRAL ARTERIES; CEREBROSPINAL FLUID; CORTICAL SPREADING DEPRESSION; ENDOTHELIAL CELLS; HUMANS; MIGRAINE DISORDERS; POTASSIUM; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 77749305237     PISSN: 00178748     EISSN: 15264610     Source Type: Journal    
DOI: 10.1111/j.1526-4610.2009.01551.x     Document Type: Review

References (196)

1. May A, Goadsby PJ. The trigeminovascular system in humans: Pathophysiologic implications for primary headache syndromes of the neural influences on the cerebral circulation. J Cereb Blood Flow Metab. 1999 19 : 115 127.
2. Lance JW, Adams RW, Lambert GA. Bulbo-cortical pathways and their possible relevance to migraine and epilepsy. Funct Neurol. 1986 1 : 357 361.
3. Adams RW, Lambert GA, Lance JW. Stimulation of brainstem nuclei in the cat: Effect on neuronal activity in the primary visual cortex of relevance to cerebral blood flow and migraine. Cephalalgia. 1989 9 : 107 118.
4. Bartsch T, Levy MJ, Knight YE, Goadsby PJ. Inhibition of nociceptive dural input in the trigeminal nucleus caudalis by somatostatin receptor blockade in the posterior hypothalamus. Pain. 2005 117 : 30 39.
5. Burstein R, Yamamura H, Malick A, Strassman AM. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J Neurophysiol. 1998 79 : 964 982.
6. Drummond PD, Lance JW. Extracranial vascular changes and the source of pain in migraine headache. Ann Neurol. 1983 13 : 32 37.
7. Knight YE, Bartsch T, Kaube H, Goadsby PJ. P/Q-type calcium-channel blockade in the periaqueductal gray facilitates trigeminal nociception: A functional genetic link for migraine? J Neurosci. 2002 22 : RC213.
8. Malick A, Strassman RM, Burstein R. Trigeminohypothalamic and reticulohypothalamic tract neurons in the upper cervical spinal cord and caudal medulla of the rat. J Neurophysiol. 2000 84 : 2078 2112.
9. Strassman AM, Raymond SA, Burstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature. 1996 384 : 560 564.
10. Moskowitz MA. Defining a pathway to discovery from bench to bedside: The trigeminovascular system and sensitization. Headache. 2008 48 : 688 690.
11. 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.
12. Lauritzen M. Cortical spreading depression in migraine. Cephalalgia. 2001 21 : 757 760.
13. Bolay H, Reuter U, Dunn AK, Huang Z, Boas DA, Moskowitz MA. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med. 2002 8 : 136 142.
14. Silberstein SD. Topiramate in migraine prevention: Evidence-based medicine from clinical trials. Neurol Sci. 2004 25 (Suppl. 3 S244 S245.
15. Leith JL, Wilson AW, Donaldson LF, Lumb BM. Cyclooxygenase-1-derived prostaglandins in the periaqueductal gray differentially control C- versus A-fiber-evoked spinal nociception. J Neurosci. 2007 27 : 11296 11305.
16. Lipton RB, Baggish JS, Stewart WF, Codispoti JR, Fu M. Efficacy and safety of acetaminophen in the treatment of migraine: Results of a randomized, double-blind, placebo-controlled, population-based study. Arch Intern Med. 2000 160 : 3486 3492.
17. May A, Goadsby PJ. Pharmacological opportunities and pitfalls in the therapy of migraine. Curr Opin Neurol. 2001 14 : 341 345.
18. Olesen J, Diener HC, Husstedt IW, et al. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med. 2004 350 : 1104 1110.
19. Humphrey PP. The discovery and development of the triptans, a major therapeutic breakthrough. Headache. 2008 48 : 685 687.
20. Hansen AJ, Zeuthen T. Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol Scand. 1981 113 : 437 445.
21. Kraig RP, Nicholson C. Extracellular ionic variations during spreading depression. Neuroscience. 1978 3 : 1045 1059.
22. De Fusco M, Marconi R, Silvestri L, et al. Haploinsufficiency of ATP1A2 encoding the Na+/K+ pump alpha2 subunit associated with familial hemiplegic migraine type 2. Nat Genet. 2003 33 : 192 196.
23. Vanmolkot KR, Kors EE, Hottenga JJ, et al. Novel mutations in the Na+, K+-ATPase pump gene ATP1A2 associated with familial hemiplegic migraine and benign familial infantile convulsions. Ann Neurol. 2003 54 : 360 366.
24. Terwindt GM, Ophoff RA, Haan J, Sandkuijl LA, Frants RR, Ferrari MD. Migraine, ataxia and epilepsy: A challenging spectrum of genetically determined calcium channelopathies. Dutch Migraine Genetics Research Group. Eur J Hum Genet. 1998 6 : 297 307.
25. Dichgans M, Freilinger T, Eckstein G, et al. Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet. 2005 366 : 371 377.
26. Ducros A, Denier C, Joutel A, et al. The clinical spectrum of familial hemiplegic migraine associated with mutations in a neuronal calcium channel. N Engl J Med. 2001 345 : 17 24.
27. Moskowitz MA, Bolay H, Dalkara T. Deciphering migraine mechanisms: Clues from familial hemiplegic migraine genotypes. Ann Neurol. 2004 55 : 276 280.
28. de Vries B, Freilinger T, Vanmolkot KR, et al. Systematic analysis of three FHM genes in 39 sporadic patients with hemiplegic migraine. Neurology. 2007 69 : 2170 2176.
29. Harrington MG, Fonteh AN, Cowan RP, et al. Cerebrospinal fluid sodium increases in migraine. Headache. 2006 46 : 1128 1135.
30. Sweet WH, Brownell GL, Scholl JA, Bowsher DR, Benda P, Stickley EE. The formation, flow and absorption of cerebrospinal fluid; newer concepts based on studies with isotopes. Res Publ Assoc Res Nerv Ment Dis. 1955 34 : 101 159.
31. Somjen GG. Neuroglia and spinal fluids. J Exp Biol. 1981 95 : 129 133.
32. Bito LZ, Davson H. Local variations in cerebrospinal fluid composition and its relationship to the composition of the extracellular fluid of the cortex. Exp Neurol. 1966 14 : 264 280.
33. Olsen NS, Rudolph GG. Transfer of sodium and bromide ions between blood, cerebrospinal fluid and brain tissue. Am J Physiol. 1955 183 : 427 432.
34. Hodgkin AL, Katz B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 108 : 37 77.
35. Kuo CC, Liao SY. Facilitation of recovery from inactivation by external Na+ and location of the activation gate in neuronal Na+ channels. J Neurosci. 2000 20 : 5639 5646.
36. Van Huysse JW, Hou X. Pressor response to CSF sodium in mice: Mediation by a ouabain-like substance and renin-angiotensin system in the brain. Brain Res. 2004 1021 : 219 231.
37. Huang BS, Amin MS, Leenen FH. The central role of the brain in salt-sensitive hypertension. Curr Opin Cardiol. 2006 21 : 295 304.
38. Catterall WA, Dib-Hajj S, Meisler MH, Pietrobon D. Inherited neuronal ion channelopathies: New windows on complex neurological diseases. J Neurosci. 2008 28 : 11768 11777.
39. Hains BC, Klein JP, Saab CY, Craner MJ, Black JA, Waxman SG. Upregulation of sodium channel Nav1.3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci. 2003 23 : 8881 8892.
40. Iwamoto T, Watanabe Y, Kita S, Blaustein MP. Na+/Ca2+ exchange inhibitors: A new class of calcium regulators. Cardiovasc Hematol Disord Drug Targets. 2007 7 : 188 198.
41. Martinez F, Castillo J, Rodriguez JR, Leira R, Noya M. Neuroexcitatory amino acid levels in plasma and cerebrospinal fluid during migraine attacks. Cephalalgia. 1993 13 : 89 93. (Pubitemid 23116117)
42. Whittam R. The dependence of the respiration of brain cortex on active cation transport. Biochem J. 1962 82 : 205 212.
43. Astrup J, Sorensen PM, Sorensen HR. Oxygen and glucose consumption related to Na+-K+ transport in canine brain. Stroke. 1981 12 : 726 730.
44. Menna G, Tong CK, Chesler M. Extracellular pH changes and accompanying cation shifts during ouabain-induced spreading depression. J Neurophysiol. 2000 83 : 1338 1345.
45. Hertz L. An intense potassium uptake into astrocytes, its further enhancement by high concentrations of potassium, and its possible involvement in potassium homeostasis at the cellular level. Brain Res. 1978 145 : 202 208.
46. Geering K. Functional roles of Na,K-ATPase subunits. Curr Opin Nephrol Hypertens. 2008 17 : 526 532.
47. Betz AL, Firth JA, Goldstein GW. Polarity of the blood-brain barrier: Distribution of enzymes between the luminal and antiluminal membranes of brain capillary endothelial cells. Brain Res. 1980 192 : 17 28.
48. Eisenberg HM, Suddith RL. Cerebral vessels have the capacity to transport sodium and potassium. Science. 1979 206 : 1083 1085.
49. Praetorius J, Nielsen S. Distribution of sodium transporters and aquaporin-1 in the human choroid plexus. Am J Physiol Cell Physiol. 2006 291 : C59 C67.
50. Abbott NJ. Evidence for bulk flow of brain interstitial fluid: Significance for physiology and pathology. Neurochem Int. 2004 45 : 545 552.
51. Cserr HF. Physiology of the choroid plexus. Physiol Rev. 1971 51 : 273 311.
52. Go KG. The normal and pathological physiology of brain water. Adv Tech Stand Neurosurg. 1997 23 : 47 142.
53. Kimelberg HK. Water homeostasis in the brain: Basic concepts. Neuroscience. 2004 129 : 851 860.
54. Razmara A, Sunday L, Stirone C, et al. Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells. J Pharmacol Exp Ther. 2008 325 : 782 790.
55. Brust P, Friedrich A, Krizbai IA, et al. Functional expression of the serotonin transporter in immortalized rat brain microvessel endothelial cells. J Neurochem. 2000 74 : 1241 1248.
56. Takuwa Y, Takuwa N, Sugimoto N. The Edg family G protein-coupled receptors for lysophospholipids: Their signaling properties and biological activities. J Biochem. 2002 131 : 767 771.
57. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat Rev Neurosci. 2003 4 : 386 398.
58. Somjen GG, Muller M. Potassium-induced enhancement of persistent inward current in hippocampal neurons in isolation and in tissue slices. Brain Res. 2000 885 : 102 110.
59. Kager H, Wadman WJ, Somjen GG. Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J Neurophysiol. 2000 84 : 495 512.
60. Kiedrowski L. High activity of K+-dependent plasmalemmal Na+/Ca2+ exchangers in hippocampal CA1 neurons. Neuroreport. 2004 15 : 2113 2116.
61. Azin AL. Role of extracellular pO2 and pCO2 in membrane mechanisms regulating cerebral artery smooth muscle. Fiziol Zh SSSR Im I M Sechenova. 1981 67 : 1652 1660.
62. Ko EA, Han J, Jung ID, Park WS. Physiological roles of K+ channels in vascular smooth muscle cells. J Smooth Muscle Res. 2008 44 : 65 81.
63. Olesen SP, Munch E, Moldt P, Drejer J. Selective activation of Ca(2+)-dependent K+ channels by novel benzimidazolone. Eur J Pharmacol. 1994 251 : 53 59.
64. Hosoi R, Matsuda T, Asano S, et al. Isoform-specific up-regulation by ouabain of Na+,K+-ATPase in cultured rat astrocytes. J Neurochem. 1997 69 : 2189 2196.
65. Senatorov VV, Stys PK, Hu B. Regulation of Na+,K+-ATPase by persistent sodium accumulation in adult rat thalamic neurones. J Physiol. 2000 525 (Pt 2 343 353.
66. Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain. 1994 117 : 199 210.
67. Leão A. Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944 7 : 391 396.
68. Brennan KC, Beltran-Parrazal L, Lopez-Valdes HE, Theriot J, Toga AW, Charles AC. Distinct vascular conduction with cortical spreading depression. J Neurophysiol. 2007 97 : 4143 4151.
69. Iadecola C. From CSD to headache: A long and winding road. Nat Med. 2002 8 : 110 112.
70. Barrett CF, van den Maagdenberg AM, Frants RR, Ferrari MD. Familial hemiplegic migraine. Adv Genet. 2008 63 : 57 83.
71. Gulbenkian S, Uddman R, Edvinsson L. Neuronal messengers in the human cerebral circulation. Peptides. 2001 22 : 995 1007.
72. van den Maagdenberg AM, Pietrobon D, Pizzorusso T, et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron. 2004 41 : 701 710.
73. Taormino JP, Fambrough DM. Pre-translational regulation of the (Na+ + K+)-ATPase in response to demand for ion transport in cultured chicken skeletal muscle. J Biol Chem. 1990 265 : 4116 4123.
74. Smith LC, Harrington MG, Britten RJ, Davidson EH. The sea urchin profilin gene is specifically expressed in mesenchyme cells during gastrulation. Dev Biol. 1994 164 : 463 474.
75. Tanaka Y, Ando S. Synaptic aging as revealed by changes in membrane potential and decreased activity of Na+,K(+)-ATPase. Brain Res. 1990 506 : 46 52.
76. Tanaka Y, Ando S. Age-related changes in [3H] ouabain binding to synaptic plasma membranes isolated from mouse brains. J Biochem. 1992 112 : 117 121.
77. Chauhan NB, Siegel GJ. In situ analysis of Na, K-ATPase alpha1- and alpha3-isoform mRNAs in aging rat hippocampus. J Neurochem. 1996 66 : 1742 1751.
78. Chauhan N, Siegel G. Na,K-ATPase: Increases in alpha1-messenger RNA and decreases in alpha3-messenger RNA levels in aging rat cerebral cortex. Neuroscience. 1997 78 : 7 11.
79. Chauhan N, Siegel G. Differential expression of Na,K-ATPase alpha-isoform mRNAs in aging rat cerebellum. J Neurosci Res. 1997 47 : 287 299.
80. Chauhan NB, Lee JM, Siegel GJ. Na,K-ATPase mRNA levels and plaque load in Alzheimer's disease. J Mol Neurosci. 1997 9 : 151 166.
81. Fraser CL, Arieff AI. Na-K-ATPase activity decreases with aging in female rat brain synaptosomes. Am J Physiol Renal Physiol. 2001 281 : F674 F678.
82. Fu YJ, Xiong S, Lovell MA, Lynn BC. Quantitative proteomic analysis of mitochondria in aging PS-1 transgenic mice. Cell Mol Neurobiol. 2009 29 : 649 664.
83. Alstadhaug KB. Periodicity of migraine. Headache. 2006 46 : 532 533.
84. Alstadhaug KB, Bekkelund S, Salvesen R. Circannual periodicity of migraine? Eur J Neurol. 2007 14 : 983 988.
85. Solomon GD. Circadian rhythms and migraine. Cleve Clin J Med. 1992 59 : 326 329.
86. Fox AW, Davis RL. Migraine chronobiology. Headache. 1998 38 : 436 441.
87. van Oosterhout F, Michel S, Deboer T, et al. Enhanced circadian phase resetting in R192Q Cav2.1 calcium channel migraine mice. Ann Neurol. 2008 64 : 315 324.
88. Wang HY, Huang RC. Diurnal modulation of the Na+/K+-ATPase and spontaneous firing in the rat retinorecipient clock neurons. J Neurophysiol. 2004 92 : 2295 2301.
89. Harrington MG, Oborina E, Pogoda J.M., et al. Circadian sodium rhythms in human cerebrospinal fluid. American Academy of Neurology Annual Meeting. 2008.
90. Denny PC, Ball WD, Redman RS. Salivary glands: A paradigm for diversity of gland development. Crit Rev Oral Biol Med. 1997 8 : 51 75.
91. Kurlansky M. Salt: A World History. New York : Penguin Books 2002.
92. Majumdar S, Faisal M, Madan V, Mallick BN. Increased turnover of Na-K ATPase molecules in rat brain after rapid eye movement sleep deprivation. J Neurosci Res. 2003 73 : 870 875.
93. Bignotto M, de Andrade UJ, de Carvalho JG, Benedito MA. Rapid eye movement sleep deprivation induces changes in the high-affinity binding of [3H]-ouabain to the rat cortical membranes. Neurosci Lett. 2006 396 : 143 147. (Pubitemid 43276429)
94. Wagner W, Nootbaar-Wagner U. Prophylactic treatment of migraine with gamma-linolenic and alpha-linolenic acids. Cephalalgia. 1997 17 : 127 130 discussion 102.
95. Harel Z, Gascon G, Riggs S, Vaz R, Brown W, Exil G. Supplementation with omega-3 polyunsaturated fatty acids in the management of recurrent migraines in adolescents. J Adolesc Health. 2002 31 : 154 161.
96. Pradalier A, Bakouche P, Baudesson G, et al. Failure of omega-3 polyunsaturated fatty acids in prevention of migraine: A double-blind study versus placebo. Cephalalgia. 2001 21 : 818 822.
97. Cohen GL. Migraine prophylactic drugs work via ion channels. Med Hypotheses. 2005 65 : 114 122.
98. Scarrone S, Podesta M, Cupello A, et al. Abnormalities of Na/K ATPase in migraine with aura. Cephalalgia. 2007 27 : 128 132.
99. Wu H, Riha GM, Yang H, Li M, Yao Q, Chen C. Differentiation and proliferation of endothelial progenitor cells from canine peripheral blood mononuclear cells. J Surg Res. 2005 126 : 193 198.
100. Horisberger JD, Lemas V, Kraehenbuhl JP, Rossier BC. Structure-function relationship of Na,K-ATPase. Annu Rev Physiol. 1991 53 : 565 584.
101. Trachtenberg MC, Packey DJ, Sweeney T. In vivo functioning of the Na+, K+-activated ATPase. Curr Top Cell Regul. 1981 19 : 159 217.
102. Blaustein MP, Zhang J, Chen L, Hamilton BP. How does salt retention raise blood pressure? Am J Physiol Regul Integr Comp Physiol. 2006 290 : R514 R523.
103. Lebel CP, Schatz RA. Altered synaptosomal phospholipid metabolism after toluene: Possible relationship with membrane fluidity, Na+,K(+)-adenosine triphosphatase and phospholipid methylation. J Pharmacol Exp Ther. 1990 253 : 1189 1197.
104. Liu XL, Miyakawa A, Aperia A, Krieger P. Na,K-ATPase generates calcium oscillations in hippocampal astrocytes. Neuroreport. 2007 18 : 597 600.
105. Xie Z. Molecular mechanisms of Na/K-ATPase-mediated signal transduction. Ann N Y Acad Sci. 2003 986 : 497 503.
106. Berrebi-Bertrand I, Maixent JM, Christe G, Lelievre LG. Two active Na+/K+-ATPases of high affinity for ouabain in adult rat brain membranes. Biochim Biophys Acta. 1990 1021 : 148 156.
107. Blanco G, Mercer RW. Isozymes of the Na-K-ATPase: Heterogeneity in structure, diversity in function. Am J Physiol. 1998 275 : F633 F650.
108. Jewell EA, Lingrel JB. Comparison of the substrate dependence properties of the rat Na,K-ATPase alpha 1, alpha 2, and alpha 3 isoforms expressed in HeLa cells. J Biol Chem. 1991 266 : 16925 16930.
109. Lingrel JB, Williams MT, Vorhees CV, Moseley AE. Na,K-ATPase and the role of alpha isoforms in behavior. J Bioenerg Biomembr. 2007 39 : 385 389.
110. McGrail KM, Phillips JM, Sweadner KJ. Immunofluorescent localization of three Na,K-ATPase isozymes in the rat central nervous system: Both neurons and glia can express more than one Na,K-ATPase. J Neurosci. 1991 11 : 381 391.
111. Segall L, Daly SE, Blostein R. Mechanistic basis for kinetic differences between the rat alpha 1, alpha 2, and alpha 3 isoforms of the Na,K-ATPase. J Biol Chem. 2001 276 : 31535 31541.
112. Peng L, Martin-Vasallo P, Sweadner KJ. Isoforms of Na,K-ATPase alpha and beta subunits in the rat cerebellum and in granule cell cultures. J Neurosci. 1997 17 : 3488 3502.
113. Watts AG, Sanchez-Watts G, Emanuel JR, Levenson R. Cell-specific expression of mRNAs encoding Na+,K(+)-ATPase alpha- and beta-subunit isoforms within the rat central nervous system. Proc Natl Acad Sci USA. 1991 88 : 7425 7429.
114. Magyar JP, Bartsch U, Wang ZQ, et al. Degeneration of neural cells in the central nervous system of mice deficient in the gene for the adhesion molecule on glia, the beta 2 subunit of murine Na,K-ATPase. J Cell Biol. 1994 127 : 835 845.
115. Martin-Vasallo P, Wetzel RK, Garcia-Segura LM, Molina-Holgado E, Arystarkhova E, Sweadner KJ. Oligodendrocytes in brain and optic nerve express the beta3 subunit isoform of Na,K-ATPase. Glia. 2000 31 : 206 218.
116. Feschenko MS, Donnet C, Wetzel RK, Asinovski NK, Jones LR, Sweadner KJ. Phospholemman, a single-span membrane protein, is an accessory protein of Na,K-ATPase in cerebellum and choroid plexus. J Neurosci. 2003 23 : 2161 2169.
117. Arystarkhova E, Sweadner KJ. Splice variants of the gamma subunit (FXYD2) and their significance in regulation of the Na, K-ATPase in kidney. J Bioenerg Biomembr. 2005 37 : 381 386.
118. Bell JR, Kennington E, Fuller W, et al. Characterization of the phospholemman knockout mouse heart: Depressed left ventricular function with increased Na-K-ATPase activity. Am J Physiol Heart Circ Physiol. 2008 294 : H613 H621.
119. Cairo ER, Friedrich T, Swarts HG, et al. Impaired routing of wild type FXYD2 after oligomerisation with FXYD2-G41R might explain the dominant nature of renal hypomagnesemia. Biochim Biophys Acta. 2008 1778 : 398 404.
120. Meij IC, Koenderink JB, van Bokhoven H, et al. Dominant isolated renal magnesium loss is caused by misrouting of the Na(+),K(+)-ATPase gamma-subunit. Nat Genet. 2000 26 : 265 266.
121. Jones DH, Li TY, Arystarkhova E, et al. Na,K-ATPase from mice lacking the gamma subunit (FXYD2) exhibits altered Na+ affinity and decreased thermal stability. J Biol Chem. 2005 280 : 19003 19011.
122. Yamaguchi F, Yamaguchi K, Tai Y, Sugimoto K, Tokuda M. Molecular cloning and characterization of a novel phospholemman-like protein from rat hippocampus. Brain Res Mol Brain Res. 2001 86 : 189 192.
123. Crambert G, Beguin P, Uldry M, et al. FXYD7, the first brain- and isoform-specific regulator of Na,K-ATPase: Biosynthesis and function of its posttranslational modifications. Ann N Y Acad Sci. 2003 986 : 444 448.
124. Sweadner KJ, Rael E. The FXYD gene family of small ion transport regulators or channels: cDNA sequence, protein signature sequence, and expression. Genomics. 2000 68 : 41 56.
125. Ophoff RA, Terwindt GM, Vergouwe MN, et al. Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell. 1996 87 : 543 552.
126. Therien AG, Blostein R. Mechanisms of sodium pump regulation. Am J Physiol Cell Physiol. 2000 279 : C541 C566.
127. Kassardjian A, Kreydiyyeh SI. JNK modulates the effect of caspases and NF-kappaB in the TNF-alpha-induced down-regulation of Na+/K+ATPase in HepG2 cells. J Cell Physiol. 2008 216 : 615 620.
128. Namekata K, Harada C, Kohyama K, Matsumoto Y, Harada T. Interleukin-1 stimulates glutamate uptake in glial cells by accelerating membrane trafficking of Na+/K+-ATPase via actin depolymerization. Mol Cell Biol. 2008 28 : 3273 3280.
129. Banerjee B, Chaudhury S. Thyroidal regulation of different isoforms of NaKATPase in the primary cultures of neurons derived from fetal rat brain. Life Sci. 2002 71 : 1643 1654.
130. Phakdeekitcharoen B, Phudhichareonrat S, Pookarnjanamorakot C, et al. Thyroid hormone increases mRNA and protein expression of Na+-K+-ATPase alpha2 and beta1 subunits in human skeletal muscles. J Clin Endocrinol Metab. 2007 92 : 353 358.
131. Thompson SM, Prince DA. Activation of electrogenic sodium pump in hippocampal CA1 neurons following glutamate-induced depolarization. J Neurophysiol. 1986 56 : 507 522.
132. Dunham ET, Glynn IM. Adenosinetriphosphatase activity and the active movements of alkali metal ions. J Physiol. 1961 156 : 274 293.
133. Lingrel JB, Kuntzweiler T. Na+,K(+)-ATPase. J Biol Chem. 1994 269 : 19659 19662.
134. Donnet C, Sweadner KJ. The mechanism of Na-K interaction on Na,K-ATPase. Ann N Y Acad Sci. 2003 986 : 249 251.
135. Morth JP, Pedersen BP, Toustrup-Jensen MS, et al. Crystal structure of the sodium-potassium pump. Nature. 2007 450 : 1043 1049.
136. Fleidervish IA, Friedman A, Gutnick MJ. Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol. 1996 493 : 83 97.
137. Johnson SW, Seutin V, North RA. Burst firing in dopamine neurons induced by N-methyl-D-aspartate: Role of electrogenic sodium pump. Science. 1992 258 : 665 667.
138. Flashner MS, Robinson JD. Effects of Mg(2+) on activation of the (Na(+) + K(+)-dependent ATPase by Na(+1). Arch Biochem Biophys. 1979 192 : 584 591.
139. Strugatsky D, Gottschalk KE, Goldshleger R, Karlish SJ. D443 of the N domain of Na+,K+-ATPase interacts with the ATP-Mg2+ complex, possibly via a second Mg2+ ion. Biochemistry (Mosc). 2005 44 : 15961 15969.
140. Jacobsen MD, Pedersen PA, Jorgensen PL. Importance of Na,K-ATPase residue alpha 1-Arg544 in the segment Arg544-Asp567 for high-affinity binding of ATP, ADP, or MgATP. Biochemistry (Mosc). 2002 41 : 1451 1456.
141. Meij IC, Koenderink JB, De Jong JC, et al. Dominant isolated renal magnesium loss is caused by misrouting of the Na+,K+-ATPase gamma-subunit. Ann N A Acad Sci. 2003 986 : 437 443.
142. Dietz RM, Weiss JH, Shuttleworth CW. Zn2+ influx is critical for some forms of spreading depression in brain slices. J Neurosci. 2008 28 : 8014 8024.
143. Hiatt A, McDonough AA, Edelman IS. Assembly of the (Na+ + K+)-adenosine triphosphatase. Post-translational membrane integration of the alpha subunit. J Biol Chem. 1984 259 : 2629 2635.
144. Palasis M, Kuntzweiler TA, Arguello JM, Lingrel JB. Ouabain interactions with the H5-H6 hairpin of the Na,K-ATPase reveal a possible inhibition mechanism via the cation binding domain. J Biol Chem. 1996 271 : 14176 14182.
145. Kyte J. Molecular considerations relevant to the mechanism of active transport. Nature. 1981 292 : 201 204.
146. Yoda A, Yoda S. Interaction between ouabain and the phosphorylated intermediate of Na,K-ATPase. Mol Pharmacol. 1982 22 : 700 705.
147. Greef K, Schadewaldt H. Introduction and Remarks on the History of Cardiac Glycosides. New York : Springer-Verlag 1981.
148. Sole MJ, Benedict CR, Versteeg DH, de Kloet ER. Digitoxin therapy partially restores cardiac catecholamine and brain serotonin metabolism in congestive heart failure. J Mol Cell Cardiol. 1985 17 : 1055 1063.
149. Balestrino M, Young J, Aitken P. Block of (Na+,K+)ATPase with ouabain induces spreading depression-like depolarization in hippocampal slices. Brain Res. 1999 838 : 37 44.
150. Haglund MM, Schwartzkroin PA. Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. J Neurophysiol. 1990 63 : 225 239.
151. Durakovic Z, Plavsic F, Smalcelj A, Grgic V Blue color vision as a sign of digitalis poisoning Lijec Vjesn. 1992 114 : 132 134.
152. Beller GA, Smith TW, Abelmann WH, Haber E, Hood WB Jr. Digitalis intoxication. A prospective clinical study with serum level correlations. N Engl J Med. 1971 284 : 989 997.
153. Johansson BW. Migraine: Effect of digoxin. J R Soc Med. 1982 75 : 215 216.
154. Tanaka R, Strickland KP. Role of phospholipid in the activation of Na+, Ka+-activated adenosine triphosphatase of beef brain. Arch Biochem Biophys. 1965 111 : 583 592.
155. Goldman SS, Albers RW. Sodium-potassium-activated adenosine triphosphatase. IX. The role of phospholipids. J Biol Chem. 1973 248 : 867 874.
156. Plataras C, Tsakiris S, Angelogianni P. Effect of CDP-choline on brain acetylcholinesterase and Na(+), K(+)-ATPase in adult rats. Clin Biochem. 2000 33 : 351 357.
157. Hanson MA, Cherezov V, Griffith MT, et al. A specific cholesterol binding site is established by the 2.8: A structure of the human beta2-adrenergic receptor. Structure. 2008 16 : 897 905.
158. Maier GA, Robinson JD. Effects of local anesthetics and cholesterol on the (Na+ +K+)-dependent ATPase. Biochem Pharmacol. 1977 26 : 791 793.
159. Tian D, Dmitrieva RI, Doris PA, et al. Protein kinase M zeta regulation of Na/K ATPase: A persistent neuroprotective mechanism of ischemic preconditioning in hippocampal slice cultures. Brain Res. 2008 1213 : 127 139.
160. Fisone G, Snyder GL, Aperia A, Greengard P. Na+,K(+)-ATPase phosphorylation in the choroid plexus: Synergistic regulation by serotonin/protein kinase C and isoproterenol/cAMP-PK/PP-1 pathways. Mol Med. 1998 4 : 258 265.
161. Das G, Gopalakrishnan A, Faisal M, Mallick BN. Stimulatory role of calcium in rapid eye movement sleep deprivation-induced noradrenaline-mediated increase in Na-K-ATPase activity in rat brain. Neuroscience. 2008 155 : 76 89.
162. Fienberg AA, Hiroi N, Mermelstein PG, et al. DARPP-32: Regulator of the efficacy of dopaminergic neurotransmission. Science. 1998 281 : 838 842.
163. Hazelwood LA, Free RB, Cabrera DM, Skinbjerg M, Sibley DR. Reciprocal modulation of function between the D1 and D2 dopamine receptors and the Na+,K+-ATPase. J Biol Chem. 2008 283 : 36441 36453.
164. Nishi A, Fisone G, Snyder GL, et al. Regulation of Na+, K+-ATPase isoforms in rat neostriatum by dopamine and protein kinase C. J Neurochem. 1999 73 : 1492 1501.
165. Das G, Mallick BN. Noradrenaline acting on alpha1-adrenoceptor mediates REM sleep deprivation-induced increased membrane potential in rat brain synaptosomes. Neurochem Int. 2008 52 : 734 740.
166. Mallick BN, Adya HV. Norepinephrine induced alpha-adrenoceptor mediated increase in rat brain Na-K ATPase activity is dependent on calcium ion. Neurochem Int. 1999 34 : 499 507.
167. Mallick BN, Adya HV, Faisal M. Norepinephrine-stimulated increase in Na+, K+-ATPase activity in the rat brain is mediated through alpha1A-adrenoceptor possibly by dephosphorylation of the enzyme. J Neurochem. 2000 74 : 1574 1578.
168. Aperia A, Ibarra F, Svensson LB, Klee C, Greengard P. Calcineurin mediates alpha-adrenergic stimulation of Na+,K(+)-ATPase activity in renal tubule cells. Proc Natl Acad Sci USA. 1992 89 : 7394 7397.
169. Antonelli MC, Costa Lieste M, Mercado R, Hernandez RJ. Serotonin modulation of low-affinity ouabain binding in rat brain determined by quantitative autoradiography. Neurochem Res. 1998 23 : 939 944.
170. Pena-Rangel MT, Mercado R, Hernandez-Rodriguez J. Regulation of glial Na+/K+-ATPase by serotonin: Identification of participating receptors. Neurochem Res. 1999 24 : 643 649.
171. Matlhagela K, Taub M. Regulation of the Na-K-ATPase beta(1)-subunit promoter by multiple prostaglandin-responsive elements. Am J Physiol Renal Physiol. 2006 291 : F635 F646.
172. Pascual J, Sterin-Borda L, Wald M, Borda ES. TXB2: Cardiostimulant effect that involves beta-adrenoceptor and Na+ + K+-ATPase activity. Prostaglandins Leukot Essent Fatty Acids. 1988 33 : 53 59.
173. Foley TD. 5-HPETE is a potent inhibitor of neuronal Na+, K(+)-ATPase activity. Biochem Biophys Res Commun. 1997 235 : 374 376.
174. Olesen J. The role of nitric oxide (NO) in migraine, tension-type headache and cluster headache. Pharmacol Ther. 2008 120 : 157 171.
175. McQueen JK, Wilson H, Sumner BE, Fink G. Serotonin transporter (SERT) mRNA and binding site densities in male rat brain affected by sex steroids. Brain Res Mol Brain Res. 1999 63 : 241 247.
176. Fink G, Sumner B, Rosie R, Wilson H, McQueen J. Androgen actions on central serotonin neurotransmission: Relevance for mood, mental state and memory. Behav Brain Res. 1999 105 : 53 68.
177. Chang HH, Michaelis EK. Effects of L-glutamic acid on synaptosomal and synaptic membrane Na+ fluxes and (Na+-K+)-ATPase. J Biol Chem. 1980 255 : 2411 2417.
178. Chang HH, Michaelis EK. L-glutamate stimulation of Na+ efflux from brain synaptic membrane vesicles. J Biol Chem. 1981 256 : 10084 10087.
179. Nathanson JA, Scavone C, Scanlon C, McKee M. The cellular Na+ pump as a site of action for carbon monoxide and glutamate: A mechanism for long-term modulation of cellular activity. Neuron. 1995 14 : 781 794.
180. Araya KA, David Pessoa Mahana C, Gonzalez LG. Role of cannabinoid CB1 receptors and Gi/o protein activation in the modulation of synaptosomal Na+,K+-ATPase activity by WIN55,212-2 and delta(9)-THC. Eur J Pharmacol. 2007 572 : 32 39.
181. Steffens M, Feuerstein TJ. Receptor-independent depression of DA and 5-HT uptake by cannabinoids in rat neocortex - Involvement of Na(+)/K(+)-ATPase. Neurochem Int. 2004 44 : 529 538.
182. Mahadik SP, Hawver DB, Hungund BL, Li YS, Karpiak SE. GM1 ganglioside treatment after global ischemia protects changes in membrane fatty acids and properties of Na+, K+-ATPase and Mg2+-ATPase. J Neurosci Res. 1989 24 : 402 412.
183. Zhou G, Dada LA, Chandel NS, et al. Hypoxia-mediated Na-K-ATPase degradation requires von Hippel Lindau protein. FASEB J. 2008 22 : 1335 1342.
184. Malfatti CR, Royes LF, Francescato L, et al. Intrastriatal methylmalonic acid administration induces convulsions and TBARS production, and alters Na+,K+-ATPase activity in the rat striatum and cerebral cortex. Epilepsia. 2003 44 : 761 767.
185. Morel P, Tallineau C, Pontcharraud R, Piriou A, Huguet F. Effects of 4-hydroxynonenal, a lipid peroxidation product, on dopamine transport and Na+/K+ ATPase in rat striatal synaptosomes. Neurochem Int. 1998 33 : 531 540.
186. Lu C, Chan SL, Fu W, Mattson MP. The lipid peroxidation product 4-hydroxynonenal facilitates opening of voltage-dependent Ca2+ channels in neurons by increasing protein tyrosine phosphorylation. J Biol Chem. 2002 277 : 24368 24375.
187. Lu C, Chan SL, Haughey N, Lee WT, Mattson MP. Selective and biphasic effect of the membrane lipid peroxidation product 4-hydroxy-2,3-nonenal on N-methyl-D-aspartate channels. J Neurochem. 2001 78 : 577 589.
188. Matsuda T, Murata Y, Kawamura N, et al. Selective induction of alpha 1 isoform of (Na+ + K+)-ATPase by insulin/insulin-like growth factor-I in cultured rat astrocytes. Arch Biochem Biophys. 1993 307 : 175 182.
189. Sweeney G, Klip A. Regulation of the Na+/K+-ATPase by insulin: Why and how? Mol Cell Biochem. 1998 182 : 121 133.
190. Kawai N, Yamamoto T, Yamamoto H, McCarron RM, Spatz M. Endothelin 1 stimulates Na+,K(+)-ATPase and Na(+)-K(+)-Cl- cotransport through ETA receptors and protein kinase C-dependent pathway in cerebral capillary endothelium. J Neurochem. 1995 65 : 1588 1596.
191. Krishnamoorthy RR, Prasanna G, Dauphin R, et al. Regulation of Na,K-ATPase expression by endothelin-1 in transformed human ciliary non-pigmented epithelial (HNPE) cells. J Ocul Pharmacol Ther. 2003 19 : 465 481. (Pubitemid 37315134)
192. Spatz M, Kawai N, Merkel N, Bembry J, McCarron RM. Functional properties of cultured endothelial cells derived from large microvessels of human brain. Am J Physiol. 1997 272 : C231 C239.
193. Amann R, Donnerer J, Lembeck F. Ruthenium red selectively inhibits capsaicin-induced release of calcitonin gene-related peptide from the isolated perfused guinea pig lung. Neurosci Lett. 1989 101 : 311 315.
194. Andersen SL, Clausen T. Calcitonin gene-related peptide stimulates active Na(+)-K+ transport in rat soleus muscle. Am J Physiol. 1993 264 : C419 C429.
195. Mahmmoud YA. Capsazepine, a synthetic vanilloid that converts the Na,K-ATPase to Na-ATPase. Proc Natl Acad Sci USA. 2008 105 : 1757 1761.
196. Tria E, Luly P, Tomasi V, Trevisani A, Barnabei O. Modulation by cyclic AMP in vitro of liver plasma membrane (Na+-K+)-ATPase and protein kinases. Biochim Biophys Acta. 1974 343 : 297 306.