Pearls and pitfalls in genetic studies of migraine

Cephalalgia

Volumn 33, Issue 8, 2013, Pages 614-625

  Eising, Else ^a   De Vries, Boukje ^a   Ferrari, Michel D ^a   Terwindt, Gisela M ^a   Van Den Maagdenberg, Arn M J M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

association; gene; genome wide; linkage; Migraine; next generation sequencing

Indexed keywords

SODIUM CHANNEL NAV1.1;

ARTICLE; CLINICAL FEATURE; DISEASE MODEL; FAMILIAL HEMIPLEGIC MIGRAINE; GENE; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETICS; HERITABILITY; INHERITANCE; LINKAGE ANALYSIS; MIGRAINE; MIGRAINE AURA; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSGENIC MOUSE;

ASSOCIATION; GENE; GENOME-WIDE; LINKAGE; MIGRAINE; NEXT-GENERATION SEQUENCING;

GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; GENETIC RESEARCH; GENETIC TESTING; HUMANS; MIGRAINE DISORDERS; NERVE TISSUE PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PREVALENCE;

EID: 84877990291     PISSN: 03331024     EISSN: 14682982     Source Type: Journal    
DOI: 10.1177/0333102413484988     Document Type: Article

References (102)

1. The International Classification of Headache Disorders. 2nd ed. Cephalalgia. 2004 ; 24: 1-160
2. Lipton RB, Stewart WF, Diamond S, et al. Prevalence and burden of migraine in the United States: Data from the American Migraine Study II. Headache. 2001 ; 41: 646-657
3. Launer LJ, Terwindt GM, Ferrari MD. The prevalence and characteristics of migraine in a population-based cohort: The GEM Study. Neurology. 1999 ; 53: 537-542
4. Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain. 1994 ; 117: 199-210
5. 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
6. Bolay H, Reuter U, Dunn AK, et al. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med. 2002 ; 8: 136-142
7. Zhang X, Levy D, Noseda R, et al. Activation of meningeal nociceptors by cortical spreading depression: Implications for migraine with aura. J Neurosci. 2010 ; 30: 8807-8814
8. Zhang X, Levy D, Kainz V, et al. Activation of central trigeminovascular neurons by cortical spreading depression. Ann Neurol. 2011 ; 69: 855-865
9. Russell MB, Olesen J. Increased familial risk and evidence of genetic factor in migraine. BMJ. 1995 ; 311: 541-544
10. Stewart WF, Staffa J, Lipton RB, et al. Familial risk of migraine: A population-based study. Ann Neurol. 1997 ; 41: 166-172
11. Ulrich V, Gervil M, Fenger K, et al. The prevalence and characteristics of migraine in twins from the general population. Headache. 1999 ; 39: 173-180
12. Gervil M, Ulrich V, Kyvik KO, et al. Migraine without aura: A population-based twin study. Ann Neurol. 1999 ; 46: 606-611
13. Mulder EJ, Van Baal C, Gaist D, et al. Genetic and environmental influences on migraine: A twin study across six countries. Twin Res. 2003 ; 6: 422-431
14. 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
15. 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
16. 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
17. Van den Maagdenberg AM, Haan J, Terwindt GM, et al. Migraine: Gene mutations and functional consequences. Curr Opin Neurol. 2007 ; 20: 299-305
18. Stam AH, Luijckx GJ, Poll-Thé BT, et al. Early seizures and cerebral edema after trivial head trauma associated with the CACNA1A S218L mutation. J Neurol Neurosurg Psych. 2009 ; 80: 1125-1129
19. Le Fort D, Safran AB, Picard F, et al. Elicited repetitive daily blindness: A new familial disorder related to migraine and epilepsy. Neurology. 2004 ; 63: 348-350
20. Vahedi K, Depienne C, Le Fort D, et al. Elicited repetitive daily blindness: A new phenotype associated with hemiplegic migraine and SCN1A mutations. Neurology. 2009 ; 72: 1178-1183
21. Zhuchenko O, Bailey J, Bonnen P, et al. Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the alpha 1A-voltage-dependent calcium channel. Nat Genet. 1997 ; 15: 62-69
22. Gambardella A, Marini C. Clinical spectrum of SCN1A mutations. Epilepsia. 2009 ; 50 (Suppl 5). 20-23
23. Thomsen LL, Ostergaard E, Olesen J, et al. Evidence for a separate type of migraine with aura: Sporadic hemiplegic migraine. Neurology. 2003 ; 60: 595-601
24. 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
25. Terwindt G, Kors E, Haan J, et al. Mutation analysis of the CACNA1A calcium channel subunit gene in 27 patients with sporadic hemiplegic migraine. Arch Neurol. 2002 ; 59: 1016-1018
26. Thomsen LL, Oestergaard E, Bjornsson A, et al. Screen for CACNA1A and ATP1A2 mutations in sporadic hemiplegic migraine patients. Cephalalgia. 2008 ; 28: 914-921
27. Gallanti A, Cardin V, Tonelli A, et al. The genetic features of 24 patients affected by familial and sporadic hemiplegic migraine. Neurol Sci. 2011 ; 32: S141 - S142
28. Riant F, Ducros A, Ploton C, et al. De novo mutations in ATP1A2 and CACNA1A are frequent in early-onset sporadic hemiplegic migraine. Neurology. 2010 ; 75: 967-972
29. De Sanctis S, Grieco GS, Breda L, et al. Prolonged sporadic hemiplegic migraine associated with a novel de novo missense ATP1A2 gene mutation. Headache. 2011 ; 51: 447-450
30. Russell MB, Ducros A. Sporadic and familial hemiplegic migraine: Pathophysiological mechanisms, clinical characteristics, diagnosis, and management. Lancet Neurol. 2011 ; 10: 457-470
31. Stam AH, Louter MA, Haan J, et al. A long-term follow-up study of 18 patients with sporadic hemiplegic migraine. Cephalalgia. 2011 ; 31: 199-205
32. Nyholt DR, LaForge KS, Kallela M, et al. A high-density association screen of 155 ion transport genes for involvement with common migraine. Hum Mol Genet. 2008 ; 17: 3318-3331
33. Cavalleri GL, Weale ME, Shianna KV, et al. Multicentre search for genetic susceptibility loci in sporadic epilepsy syndrome and seizure types: A case-control study. Lancet Neurol. 2007 ; 6: 970-980
34. Pietrobon D. Insights into migraine mechanisms and CaV2.1 calcium channel function from mouse models of familial hemiplegic migraine. J Physiol. 2010 ; 588: 1871-1878
35. Cao YQ, Piedras-Rentería ES, Smith GB, et al. Presynaptic Ca2+ channels compete for channel type-preferring slots in altered neurotransmission arising from Ca2+ channelopathy. Neuron. 2004 ; 43: 387-400
36. Tao J, Liu P, Xiao Z, et al. Effects of familial hemiplegic migraine type 1 mutation T666M on voltage-gated calcium channel activities in trigeminal ganglion neurons. J Neurophysiol. 2012 ; 107: 1666-1680
37. Tavraz NN, Friedrich T, Dürr KL, et al. Diverse functional consequences of mutations in the Na+/K+-ATPase alpha2-subunit causing familial hemiplegic migraine type 2. J Biol Chem. 2008 ; 283: 31097-31106
38. Kahlig KM, Rhodes TH, Pusch M, et al. Divergent sodium channel defects in familial hemiplegic migraine. Proc Natl Acad Sci USA. 2008 ; 105: 9799-9804
39. Cestele S, Scalmani P, Rusconi R, et al. Self-limited hyperexcitability: Functional effect of a familial hemiplegic migraine mutation of the Nav1.1 (SCN1A) Na+ channel. J Neurosci. 2008 ; 28: 7273-7283
40. Castro MJ, Stam AH, Lemos C, et al. First mutation in the voltage-gated Nav1.1 subunit gene SCN1A with co-occurring familial hemiplegic migraine and epilepsy. Cephalalgia. 2009 ; 29: 308-313
41. Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev. 2001 ; 81: 1065-1096
42. 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
43. Van den Maagdenberg AM, Pizzorusso T, Kaja S, et al. High CSD susceptibility and migraine-associated symptoms in CaV2.1 S218L mice. Ann Neurol. 2010 ; 67: 85-98
44. Langford DJ, Bailey AL, Chanda ML, et al. Coding of facial expressions of pain in the laboratory mouse. Nat Methods. 2010 ; 7: 447-449
45. Eikermann-Haerter K, Dilekoz E, Kudo C, et al. Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest. 2009 ; 119: 99-109
46. Tottene A, Conti R, Fabbro A, et al. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron. 2009 ; 61: 762-773
47. 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 ;: e1002129 - e1002129
48. 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
49. Anttila V, Stefansson H, Kallela M, et al. Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat Genet. 2010 ; 42: 869-873
50. Dallas M, Boycott HE, Atkinson L, et al. Hypoxia suppresses glutamate transport in astrocytes. J Neurosci. 2007 ; 27: 3946-3955
51. Sarkar D, Park ES, Emdad L, et al. Molecular basis of nuclear factor-kappaB activation by astrocyte elevated gene-1. Cancer Res. 2008 ; 68: 1478-1484
52. Kang DC, Su ZZ, Sarkar D, et al. Cloning and characterization of HIV-1-inducible astrocyte elevated gene-1, AEG-1. Gene. 2005 ; 353: 8-15
53. Boycott HE, Wilkinson JA, Boyle JP, et al. Differential involvement of TNF alpha in hypoxic suppression of astrocyte glutamate transporters. Glia. 2008 ; 56: 998-1004
54. Andreou AP, Goadsby PJ. Therapeutic potential of novel glutamate receptor antagonists in migraine. Expert Opin Investig Drugs. 2009 ; 18: 789-803
55. Chasman DI, Schürks M, Anttila V, et al. Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat Genet. 2011 ; 43: 695-698
56. Peier AM, Moqrich A, Hergarden AC, et al. A TRP channel that senses cold stimuli and menthol. Cell. 2002 ; 108: 705-715
57. Proudfoot CJ, Garry EM, Cottrell DF, et al. Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Curr Biol. 2006 ; 16: 1591-1605
58. Dray A. Neuropathic pain: Emerging treatments. Br J Anaesth. 2008 ; 101: 48-58
59. Cassé F, Bardou I, Danglot L, et al. Glutamate controls tPA recycling by astrocytes, which in turn influences glutamatergic signals. J Neurosci. 2012 ; 32: 5186-5199
60. Seale P, Bjork B, Yang W, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008 ; 454: 961-967
61. Kinameri E, Inoue T, Aruga J, et al. Prdm proto-oncogene transcription factor family expression and interaction with the Notch-Hes pathway in mouse neurogenesis. PLoS One. 2008 ; 3: e3859 - e3859
62. Endo K, Karim MR, Taniguchi H, et al. Chromatin modification of Notch targets in olfactor receptor neuron diversification. Nat Neurosci. 2011 ; 15: 224-233
63. Freilinger T, Anttila V, de Vries B, et al. Genome-wide association analysis identifies susceptibility loci for migraine without aura. Nat Genet. 2012 ; 44: 777-782
64. Flavell SW, Kim TK, Gray JM, et al. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron. 2008 ; 60: 1022-1038
65. Schytz HW, Birk S, Wienecke T, et al. PACAP38 induces migraine-like attacks in patients with migraine without aura. Brain. 2009 ; 132: 16-25
66. Law C, Bunyan D, Castle B, et al. Clinical features in a family with an R460H mutation in transforming growth factor beta receptor 2 gene. J Med Genet. 2006 ; 43: 908-916
67. Jarray R, Allain B, Borriello L, et al. Depletion of the novel protein PHACTR-1 from human endothelial cells abolishes tube formation and induces cell death receptor apoptosis. Biochimie. 2011 ; 93: 1668-1675
68. Wang K, Li M, Hakonarson H. Analysing biological pathways in genome-wide association studies. Nat Rev Genet. 2010 ; 11: 843-854
69. Müller B, Grossniklaus U. Model organisms - A historical perspective. J Proteomics. 2010 ; 73: 2054-2063
70. Brennand KJ, Gage FH. Concise review: The promise of human induced pluripotent stem cell-based studies of schizophrenia. Stem Cells. 2011 ; 29: 1915-1922
71. De Vries B, Frants RR, Ferrari MD, et al. Molecular genetics of migraine. Hum Genet. 2009 ; 126: 115-132
72. Wessman M, Kallela M, Kaunisto MA, et al. Susceptibility locus for migraine with aura, on chromosome 4q24. Am J Hum Genet. 2002 ; 70: 652-662
73. Björnsson A, Gudmundsson G, Gudfinnsson E, et al. Localization of a gene for migraine without aura to chromosome 4q21. Am J Hum Genet. 2003 ; 73: 986-993
74. Nyholt DR, Morley KI, Ferreira MA, et al. Genomewide significant linkage to migrainous headache on chromosome 5q21. Am J Hum Genet. 2005 ; 77: 500-512
75. Anttila V, Kallela M, Oswell G, et al. Trait components provide tools to dissect the genetic susceptibility of migraine. Am J Hum Genet. 2006 ; 79: 85-99
76. Anttila V, Nyholt DR, Kallela M, et al. Consistently replicating locus linked to migraine on 10q22-q23. Am J Hum Genet. 2008 ; 82: 1051-1063
77. Nyholt DR, Gillespie NG, Heath AC, et al. Latent class and genetic analysis does not support migraine with aura and migraine without aura as separate entities. Genet Epidemiol. 2004 ; 26: 231-244
78. Tuulio-Henriksson A, Haukka J, Partonen T, et al. Heritability and number of quantitative trait loci of neurocognitive functions in families with schizophrenia. Am J Med Genet. 2002 ; 114: 483-490
79. Rommelse NN, Altink ME, Martin NC, et al. Neuropsychological measures probably facilitate heritability research of ADHD. Arch Clin Neuropsychol. 2008 ; 23: 579-591
80. Rubino E, Ferrero M, Rainero I, et al. Association of the C677T polymorphism in the MTHFR gene with migraine: A meta-analysis. Cephalalgia. 2009 ; 29: 818-825
81. Schurks M, Rist PM, Kurth T. MTHFR 677C>T and ACE D/I polymorphisms in migraine: A systematic review and meta-analysis. Headache. 2010 ; 50: 588-599
82. Kaunisto MA, Kallela M, Hamalainen E, et al. Testing of variants of the MTHFR and ESR1 genes in 1798 Finnish individuals fails to confirm the association with migraine with aura. Cephalalgia. 2006 ; 26: 1462-1472
83. Todt U, Freudenberg J, Goebel I, et al. MTHFR C677T polymorphism and migraine with aura. Ann Neurol. 2006 ; 60: 621-622
84. Goyette P, Sumner JS, Milos R, et al. Human methylenetetrahydrofolate reductase: Isolation of cDNA, mapping and mutation identification. Nat Genet. 1994 ; 7: 195-200
85. Oterino A, Toriello M, Valle N, et al. The relationship between homocysteine and genes of folate-related enzymes in migraine patients. Headache. 2010 ; 50: 99-168
86. Suzuki M, Van Paesschen W, Stalmans I, et al. Defective membrane expression of the Na(+)-HCO(3)(-) cotransporter NBCe1 is associated with familial migraine. Proc Natl Acad Sci USA. 2010 ; 107: 15963-15968
87. Igarashi T, Sekine T, Watanabe H. Molecular basis of proximal renal tubular acidosis. J Nephrol. 2002 ; (Suppl 5). S135 - S141
88. Lafrenière RG, Cader MZ, Poulin JF, et al. A dominant-negative mutation in the TRESK potassium channel is linked to familial migraine with aura. Nat Med. 2010 ; 16: 1157-1160
89. Andres-Enguix I, Shang L, Stansfeld PJ, et al. Functional analysis of missense variants in the TRESK (KCNK18) K channel. Sci Rep. 2012 ; 2: 237-237
90. Bamshad MJ, Ng SB, Bigham AW, et al. Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet. 2011 ; 12: 745-755
91. Lafrenière RG, Rouleau GA. Migraine: Role of the TRESK two-pore potassium channel. Int J Biochem Cell Biol. 2011 ; 43: 1533-1536
92. Tulleuda A, Cokic B, Callejo G, et al. TRESK channel contribution to nociceptive sensory neurons excitability: Modulation by nerve injury. Mol Pain. 2011 ; 7: 30-30
93. Stam AH, Luijckx GJ, Poll-Thé BT, et al. Early seizures and cerebral oedema after trivial head trauma associated with the CACNA1A S218L mutation. J Neurol Neurosurg Psychiatry. 2009 ; 80: 1125-1129
94. Kuhlenbäumer G, Hullmann J, Appenzeller S. Novel genomic techniques open new avenues in the analysis of monogenic disorders. Hum Mutat. 2011 ; 32: 144-151
95. Ng SB, Buckingham KJ, Lee C, et al. Exome sequencing identifies the cause of a mendelian disorder. Nat Genet. 2010 ; 42: 30-35
96. Bourgeois M, Aicardi J, Goutieres F. Alternating hemiplegia of childhood. J Pediatr. 1993 ; 122: 673-679
97. Heinzen EL, Swoboda KJ, Hitomi Y, et al. De novo mutations in ATP1A3 cause alternating hemiplegia of childhood. Nat Genet. 2012 ; 44: 1030-1034
98. Rosewich H, Thiele H, Ohlenbusch A, et al. Heterozygous de-novo mutations in ATP1A3 in patients with alternating hemiplegia of childhood: A whole-exome sequencing gene-identification study. Lancet Neurol. 2012 ; 11: 764-773.
99. Manolio TA, Collins FS, Cox NJ, et al. Finding the missing heritability of complex diseases. Nature. 2009 ; 461: 747-753
100. Thomsen LL, Olesen J. Nitric oxide in primary headaches. Curr Opin Neurol. 2001 ; 14: 315-321
101. Walsh T, McClellan JM, McCarthy SE, et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science. 2008 ; 320: 539-543
102. Klein RJ, Zeiss C, Chew EY, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005 ; 308: 385-389