Increased susceptibility to cortical spreading depression in the mouse model of Familial hemiplegic migraine type 2

PLoS Genetics

Volumn 7, Issue 6, 2011, Pages

  Leo, Loredana ^a,b   Gherardini, Lisa ^c   Barone, Virginia ^a   de Fusco, Maurizio ^a   Pietrobon, Daniela ^d   Pizzorusso, Tommaso ^c,e   Casari, Giorgio ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) ALPHA SUBUNIT; GLUTAMIC ACID; UNCLASSIFIED DRUG; ATP1A2 PROTEIN, MOUSE;

AMINO ACID METABOLISM; AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ATP1A2 GENE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMBRYO; ENDOPLASMIC RETICULUM; FAMILIAL HEMIPLEGIC MIGRAINE; FAMILIAL HEMIPLEGIC MIGRAINE TYPE 2; FEMALE; GENE; GENE MUTATION; GENETIC TRANSFECTION; HETEROZYGOSITY; HOMOZYGOSITY; MALE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN DEGRADATION; SPREADING CORTICAL DEPRESSION; SYNAPSE; ANIMAL; DISEASE MODEL; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; HELA CELL; HUMAN; METABOLISM; MIGRAINE WITH AURA; PATHOLOGY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

MUS;

ANIMALS; ASTROCYTES; CORTICAL SPREADING DEPRESSION; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; FEMALE; GENE KNOCK-IN TECHNIQUES; GLUTAMIC ACID; HELA CELLS; HUMANS; MALE; MICE; MICE, TRANSGENIC; MIGRAINE WITH AURA; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SODIUM-POTASSIUM-EXCHANGING ATPASE; SYNAPTIC TRANSMISSION; TRANSFECTION;

EID: 79959847850     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002129     Document Type: Article

References (60)

1. Russell MB, Iversen HK, Olesen J, (1994) Improved description of the migraine aura by a diagnostic aura diary. Cephalalgia 14: 107-117.
2. Goadsby PJ, Lipton RB, Ferrari MD, (2002) Migraine-current understanding and treatment. N Engl J Med 346: 257-270.
3. Pietrobon D, Striessnig J, (2003) Neurobiology of migraine. Nat Rev Neurosci 4: 386-398.
4. Pietrobon D, (2005) Migraine: new molecular mechanisms. Neuroscientist 11: 373-386.
5. Lauritzen M, (1994) Pathophysiology of the migraine aura. The spreading depression theory. Brain 117: 199-210.
6. Cutrer FM, Sorensen AG, Weisskoff RM, Ostergaard L, Sanchez del Rio M, et al. (1998) Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann Neurol 43: 25-31.
7. Hadjikhani N, Sanchez Del Rio M, Wu O, Schwartz D, Bakker D, et al. (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proceedings of the National Academy of Sciences of the United States of America 98: 4687-4692.
8. Bowyer SM, Aurora KS, Moran JE, Tepley N, Welch KM, (2001) Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann Neurol 50: 582-587.
9. Milner PM, (1958) Note on a possible correspondence between the scotomas of migraine and spreading depression of Leao. Electroencephalogr Clin Neurophysiol 10: 705.
10. Bolay H, Reuter U, Dunn AK, Huang Z, Boas DA, et al. (2002) Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med 8: 136-142.
11. Dalkara T, Zervas NT, Moskowitz MA, (2006) From spreading depression to the trigeminovascular system. Neurol Sci 27 (Suppl 2): S86-90.
12. Zhang X, Levy D, Noseda R, Kainz V, Jakubowski M, et al. (2010) Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J Neurosci 30: 8807-8814.
13. Ayata C, Jin H, Kudo C, Dalkara T, Moskowitz MA, (2006) Suppression of cortical spreading depression in migraine prophylaxis. Ann Neurol 59: 652-661.
14. Wessman M, Kaunisto MA, Kallela M, Palotie A, (2004) The molecular genetics of migraine. Ann Med 36: 462-473.
15. Ferrari MD, (2008) Migraine genetics: a fascinating journey towards improved migraine therapy. Headache 48: 697-700.
16. Ophoff RA, Terwindt GM, Vergouwe MN, van Eijk R, Mohrenweiser H, et al. (1996) A 3-Mb region for the familial hemiplegic migraine locus on 19p13.1-p13.2: exclusion of PRKCSH as a candidate gene. Dutch Migraine Genetic Research Group. Eur J Hum Genet 4: 321-328.
17. De Fusco M, Marconi R, Silvestri L, Atorino L, Rampoldi L, et al. (2003) Haploinsufficiency of ATP1A2 encoding the Na+/K+ pump alpha2 subunit associated with familial hemiplegic migraine type 2. Nat Genet 33: 192-196.
18. Dichgans M, Freilinger T, Eckstein G, Babini E, Lorenz-Depiereux B, et al. (2005) Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet 366: 371-377.
19. Riant F, De Fusco M, Aridon P, Ducros A, Ploton C, et al. (2005) ATP1A2 mutations in 11 families with familial hemiplegic migraine. Hum Mutat 26: 281.
20. Jurkat-Rott K, Freilinger T, Dreier JP, Herzog J, Gobel H, et al. (2004) Variability of familial hemiplegic migraine with novel A1A2 Na+/K+-ATPase variants. Neurology 62: 1857-1861.
21. Kaunisto MA, Harno H, Vanmolkot KR, Gargus JJ, Sun G, et al. (2004) A novel missense ATP1A2 mutation in a Finnish family with familial hemiplegic migraine type 2. Neurogenetics 5: 141-146.
22. Pierelli F, Grieco GS, Pauri F, Pirro C, Fiermonte G, et al. (2006) A novel ATP1A2 mutation in a family with FHM type II. Cephalalgia 26: 324-328.
23. Spadaro M, Ursu S, Lehmann-Horn F, Veneziano L, Antonini G, et al. (2004) A G301R Na+/K+-ATPase mutation causes familial hemiplegic migraine type 2 with cerebellar signs. Neurogenetics 5: 177-185.
24. Vanmolkot KR, Kors EE, Hottenga JJ, Terwindt GM, Haan J, et al. (2003) Novel mutations in the Na+, K+-ATPase pump gene ATP1A2 associated with familial hemiplegic migraine and benign familial infantile convulsions. Annals of Neurology 54: 360-366.
25. Deprez L, Weckhuysen S, Peeters K, Deconinck T, Claeys KG, et al. (2008) Epilepsy as part of the phenotype associated with ATP1A2 mutations. Epilepsia 49: 500-508.
26. Vanmolkot KR, Stroink H, Koenderink JB, Kors EE, van den Heuvel JJ, et al. (2006) Severe episodic neurological deficits and permanent mental retardation in a child with a novel FHM2 ATP1A2 mutation. Ann Neurol 59: 310-314.
27. Ambrosini A, D'Onofrio M, Grieco GS, Di Mambro A, Montagna G, et al. (2005) Familial basilar migraine associated with a new mutation in the ATP1A2 gene. Neurology 65: 1826-1828.
28. Todt U, Dichgans M, Jurkat-Rott K, Heinze A, Zifarelli G, et al. (2005) Rare missense variants in ATP1A2 in families with clustering of common forms of migraine. Hum Mutat 26: 315-321.
29. Blanco G, Mercer RW, (1998) Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol 275: F633-650.
30. Hu YK, Kaplan JH, (2000) Site-directed chemical labeling of extracellular loops in a membrane protein. The topology of the Na,K-ATPase alpha-subunit. J Biol Chem 275: 19185-19191.
31. Crambert G, Hasler U, Beggah AT, Yu C, Modyanov NN, et al. (2000) Transport and pharmacological properties of nine different human Na, K-ATPase isozymes. J Biol Chem 275: 1976-1986.
32. de Carvalho Aguiar P, Sweadner KJ, Penniston JT, Zaremba J, Liu L, et al. (2004) Mutations in the Na+/K+-ATPase alpha3 gene ATP1A3 are associated with rapid-onset dystonia parkinsonism. Neuron 43: 169-175.
33. McGrail KM, Phillips JM, Sweadner KJ, (1991) 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 11: 381-391.
34. Pietrobon D, (2007) Familial hemiplegic migraine. Neurotherapeutics 4: 274-284.
35. Tavraz NN, Friedrich T, Durr KL, Koenderink JB, Bamberg E, et al. (2008) Diverse functional consequences of mutations in the Na+/K+-ATPase alpha2-subunit causing familial hemiplegic migraine type 2. J Biol Chem 283: 31097-31106.
36. Tavraz NN, Durr KL, Koenderink JB, Freilinger T, Bamberg E, et al. (2009) Impaired plasma membrane targeting or protein stability by certain ATP1A2 mutations identified in sporadic or familial hemiplegic migraine. Channels (Austin) 3: 82-87.
37. Jorgensen PL, Hakansson KO, Karlish SJ, (2003) Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol 65: 817-849.
38. Koenderink JB, Zifarelli G, Qiu LY, Schwarz W, De Pont JJ, et al. (2005) Na,K-ATPase mutations in familial hemiplegic migraine lead to functional inactivation. Biochim Biophys Acta 1669: 61-68.
39. James PF, Grupp IL, Grupp G, Woo AL, Askew GR, et al. (1999) Identification of a specific role for the Na,K-ATPase alpha 2 isoform as a regulator of calcium in the heart. Mol Cell 3: 555-563.
40. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, et al. (1997) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 8: 711-713.
41. van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, et al. (2010) High cortical spreading depression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice. Ann Neurol 67: 85-98.
42. Ikeda K, Onaka T, Yamakado M, Nakai J, Ishikawa TO, et al. (2003) Degeneration of the amygdala/piriform cortex and enhanced fear/anxiety behaviors in sodium pump alpha2 subunit (Atp1a2)-deficient mice. J Neurosci 23: 4667-4676.
43. Moseley AE, Lieske SP, Wetzel RK, James PF, He S, et al. (2003) The Na,K-ATPase alpha 2 isoform is expressed in neurons, and its absence disrupts neuronal activity in newborn mice. J Biol Chem 278: 5317-5324.
44. Onimaru H, Homma I, (2007) Spontaneous oscillatory burst activity in the piriform-amygdala region and its relation to in vitro respiratory activity in newborn rats. Neuroscience 144: 387-394.
45. Moseley AE, Williams MT, Schaefer TL, Bohanan CS, Neumann JC, et al. (2007) Deficiency in Na,K-ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. J Neurosci 27: 616-626.
46. van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, et al. (2004) A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 41: 701-710.
47. Eikermann-Haerter K, Dilekoz E, Kudo C, Savitz SI, Waeber C, et al. (2009) Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 119: 99-109.
48. Moskowitz MA, Bolay H, Dalkara T, (2004) Deciphering migraine mechanisms: clues from familial hemiplegic migraine genotypes. Ann Neurol 55: 276-280.
49. D'Ambrosio R, Gordon DS, Winn HR, (2002) Differential role of KIR channel and Na(+)/K(+)-pump in the regulation of extracellular K(+) in rat hippocampus. J Neurophysiol 87: 87-102.
50. Ransom CB, Ransom BR, Sontheimer H, (2000) Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps. J Physiol 522 Pt 3: 427-442.
51. Somjen GG, (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81: 1065-1096.
52. Haglund MM, Schwartzkroin PA, (1990) Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. J Neurophysiol 63: 225-239.
53. Clapcote SJ, Duffy S, Xie G, Kirshenbaum G, Bechard AR, et al. (2009) Mutation I810N in the alpha3 isoform of Na+,K+-ATPase causes impairments in the sodium pump and hyperexcitability in the CNS. Proc Natl Acad Sci U S A 106: 14085-14090.
54. Pellerin L, Magistretti PJ, (1997) Glutamate uptake stimulates Na+,K+-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J Neurochem 69: 2132-2137.
55. Cholet N, Pellerin L, Magistretti PJ, Hamel E, (2002) Similar perisynaptic glial localization for the Na+,K+-ATPase alpha 2 subunit and the glutamate transporters GLAST and GLT-1 in the rat somatosensory cortex. Cereb Cortex 12: 515-525.
56. Rose EM, Koo JC, Antflick JE, Ahmed SM, Angers S, et al. (2009) Glutamate transporter coupling to Na,K-ATPase. J Neurosci 29: 8143-8155.
57. Tzingounis AV, Wadiche JI, (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8: 935-947.
58. Anttila V, Stefansson H, Kallela M, Todt U, Terwindt GM, et al. Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat Genet 42: 869-873.
59. Jen JC, Wan J, Palos TP, Howard BD, Baloh RW, (2005) Mutation in the glutamate transporter EAAT1 causes episodic ataxia, hemiplegia, and seizures. Neurology 65: 529-534.
60. Tottene A, Conti R, Fabbro A, Vecchia D, Shapovalova M, et al. (2009) Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 61: 762-773.