Monogenic causes of stroke: now and the future

Journal of Neurology

Volumn 262, Issue 12, 2015, Pages 2601-2616

  Tan, Rhea Y Y ^a   Markus, Hugh S ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

CADASIL; CARASIL; COL4A1; Genetics; Next generation sequencing; Retinal vasculopathy with cerebral leukodystrophy; Small vessel disease; Stroke

Indexed keywords

COLLAGEN TYPE 4; COLLAGEN TYPE 4 ALPHA1; COLLAGEN TYPE 4 ALPHA2; EXODEOXYRIBONUCLEASE III; NOTCH3 RECEPTOR; PITTSBURGH COMPOUND B; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TRANSCRIPTION FACTOR FOXC1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VITRONECTIN;

ALZHEIMER DISEASE; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CADASIL; CEREBROVASCULAR ACCIDENT; CEREBROVASCULAR DISEASE; CEREBROVASCULAR MALFORMATION; CLINICAL PRACTICE; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DEMENTIA; DNA REPAIR; ENZYME ACTIVITY; ENZYME REPLACEMENT; FABRY DISEASE; GENE DELETION; GENE MUTATION; HUMAN; HYDROCEPHALUS; HYPERTENSION; KIDNEY FUNCTION; LEUKOENCEPHALOPATHY; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSON DISEASE; PATHOGENESIS; PERIVENTRICULAR HETEROTOPIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; VASCULAR AMYLOIDOSIS; VASCULAR DISEASE; ALOPECIA; BRAIN INFARCTION; COMPLICATION; DEMYELINATING DISEASE; DNA SEQUENCE; GENETICS; RETINA DISEASE; SPINE DISEASE; STROKE; TRENDS;

ALOPECIA; CADASIL; CEREBRAL INFARCTION; CEREBRAL SMALL VESSEL DISEASES; HEREDITARY CENTRAL NERVOUS SYSTEM DEMYELINATING DISEASES; HUMANS; LEUKOENCEPHALOPATHIES; RETINAL DISEASES; SEQUENCE ANALYSIS, DNA; SPINAL DISEASES; STROKE; VASCULAR DISEASES;

EID: 84947868819     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-015-7794-4     Document Type: Review

References (81)

1. Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701
2. Joutel A, Corpechot C, Ducros A et al (1996) Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 383:707–710
3. Razvi SSM, Davidson R, Bone I, Muir KW (2005) The prevalence of cerebral autosomal dominant arteriopathy with subcortical infarcts and leucoencephalopathy (CADASIL) in the west of Scotland. J Neurol Neurosurg Psychiatry 76:739–741
4. Narayan SK, Gorman G, Kalaria RN et al (2012) The minimum prevalence of CADASIL in northeast England. Neurology 78:1025–1027
5. Rutten-Jacobs LC, Kilarski LL, Bevan S et al (2015) Abstract 26: Prevalence of CADASIL and Fabry Disease in a Large Cohort of MRI defined Younger onset Lacunar Stroke. Stroke 46:A26
6. Adib-Samii P, Brice G, Martin RJ, Markus HS (2010) Clinical spectrum of CADASIL and the effect of cardiovascular risk factors on phenotype: study in 200 consecutively recruited individuals. Stroke 41:630–634
7. Dichgans M, Mayer M, Uttner I et al (1998) The phenotypic spectrum of CADASIL: clinical findings in 102 cases. Ann Neurol 44:731–739
8. Desmond DW, Moroney JT, Lynch T et al (1999) The natural history of CADASIL: a pooled analysis of previously published cases. Stroke 30:1230–1233
9. Roine S, Pöyhönen M, Timonen S et al (2005) Neurologic symptoms are common during gestation and puerperium in CADASIL. Neurology 64:1441–1443
10. Hinze S, Goonasekera M, Nannucci S et al (2015) Longitudinally extensive spinal cord infarction in CADASIL. Pract Neurol 15:60–62
11. Tournier-Lasserve E, Joutel A, Melki J et al (1993) Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy maps to chromosome 19q12. Nat Genet 3:256–259
12. O’Sullivan M, Jarosz JM, Martin RJ et al (2001) MRI hyperintensities of the temporal lobe and external capsule in patients with CADASIL. Neurology 56:628–634
13. Lesnik Oberstein SA, van den Boom R, van Buchem MA et al (2001) Cerebral microbleeds in CADASIL. Neurology 57:1066–1070
14. Morroni M, Marzioni D, Ragno M et al (2013) Role of electron microscopy in the diagnosis of cadasil syndrome: a study of 32 patients. PLoS One 8:e65482
15. Singhal S, Bevan S, Barrick T et al (2004) The influence of genetic and cardiovascular risk factors on the CADASIL phenotype. Brain 127:2031–2038
16. Opherk C, Peters N, Holtmannspötter M et al (2006) Heritability of MRI lesion volume in CADASIL: evidence for genetic modifiers. Stroke 37:2684–2689
17. Fukutake T (2011) Cerebral autosomal recessive arteriopathy with subcortical infarcts and leukoencephalopathy (CARASIL): from discovery to gene identification. J Stroke Cerebrovasc Dis 20:85–93
18. Mendioroz M, Fernández-Cadenas I, Del Río-Espinola A et al (2010) A missense HTRA1 mutation expands CARASIL syndrome to the Caucasian population. Neurology 75:2033–2035
19. Fukutake T, Hirayama K (1995) Familial young-adult-onset arteriosclerotic leukoencephalopathy with alopecia and lumbago without arterial hypertension. Eur Neurol 35:69–79
20. Yanagawa S, Ito N, Arima K, Ikeda S-IS (2002) Cerebral autosomal recessive arteriopathy with subcortical infarcts and leukoencephalopathy. Neurology 58:817–820
21. Arima K, Yanagawa S, Ito N, Ikeda S (2003) Cerebral arterial pathology of CADASIL and CARASIL (Maeda syndrome). Neuropathology 23:327–334
22. Richards A, van den Maagdenberg AMJM, Jen JC et al (2007) C-terminal truncations in human 3′-5′ DNA exonuclease TREX1 cause autosomal dominant retinal vasculopathy with cerebral leukodystrophy. Nat Genet 39:1068–1070
23. Ophoff RA, DeYoung J, Service SK et al (2001) Hereditary vascular retinopathy, cerebroretinal vasculopathy, and hereditary endotheliopathy with retinopathy, nephropathy, and stroke map to a single locus on chromosome 3p21.1–p21.3. Am J Hum Genet 69:447–453
24. DiFrancesco JC, Novara F, Zuffardi O et al (2014) TREX1 C-terminal frameshift mutations in the systemic variant of retinal vasculopathy with cerebral leukodystrophy. Neurol Sci. doi:10.1007/s10072-014-1944-9
25. Kavanagh D, Spitzer D, Kothari PH et al (2008) New roles for the major human 3′-5′ exonuclease TREX1 in human disease. Cell Cycle 7:1718–1725
26. Pelzer N, de Vries B, Boon EMJ et al (2013) Heterozygous TREX1 mutations in early-onset cerebrovascular disease. J Neurol 260:2188–2190
27. Vahedi K, Alamowitch S (2011) Clinical spectrum of type IV collagen (COL4A1) mutations: a novel genetic multisystem disease. Curr Opin Neurol 24:63–68
28. Lanfranconi S, Markus HS (2010) COL4A1 mutations as a monogenic cause of cerebral small vessel disease: a systematic review. Stroke 41:e513–e518
29. Gould DB, Phalan FC, van Mil SE et al (2006) Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med 354:1489–1496
30. Vahedi K, Boukobza M, Massin P et al (2007) Clinical and brain MRI follow-up study of a family with COL4A1 mutation. Neurology 69:1564–1568
31. Alamowitch S, Plaisier E, Favrole P et al (2009) Cerebrovascular disease related to COL4A1 mutations in HANAC syndrome. Neurology 73:1873–1882
32. Verbeek E, Meuwissen MEC, Verheijen FW et al (2012) COL4A2 mutation associated with familial porencephaly and small-vessel disease. Eur J Hum Genet 20:844–851
33. Renard D, Miné M, Pipiras E et al (2014) Cerebral small-vessel disease associated with COL4A1 and COL4A2 gene duplications. Neurology 83:1029–1031
34. Garman SC, Garboczi DN (2004) The molecular defect leading to Fabry disease: structure of human alpha-galactosidase. J Mol Biol 337:319–335
35. Clarke JTR (2007) Narrative review: Fabry disease. Ann Intern Med 146:425–433
36. Orteu CH, Jansen T, Lidove O et al (2007) Fabry disease and the skin: data from FOS, the Fabry outcome survey. Br J Dermatol 157:331–337
37. Viana-Baptista M (2012) Stroke and Fabry disease. J Neurol 259:1019–1028
38. Crutchfield KE, Patronas NJ, Dambrosia JM et al (1998) Quantitative analysis of cerebral vasculopathy in patients with Fabry disease. Neurology 50:1746–1749
39. Rolfs A, Böttcher T, Zschiesche M et al (2005) Prevalence of Fabry disease in patients with cryptogenic stroke: a prospective study. Lancet 366:1794–1796
40. Baptista MV, Ferreira S, Pinho-E-Melo T et al (2010) Mutations of the GLA gene in young patients with stroke: the PORTYSTROKE study––screening genetic conditions in Portuguese young stroke patients. Stroke 41:431–436
41. Wilcox WR, Oliveira JP, Hopkin RJ et al (2008) Females with Fabry disease frequently have major organ involvement: lessons from the Fabry Registry. Mol Genet Metab 93:112–128
42. Linthorst GE, Vedder AC, Aerts JMFG, Hollak CEM (2005) Screening for Fabry disease using whole blood spots fails to identify one-third of female carriers. Clin Chim Acta 353:201–203
43. Schiffmann R, Kopp JB, Austin HA et al (2001) Enzyme replacement therapy in Fabry disease: a randomized controlled trial. JAMA 285:2743–2749
44. Siegenthaler JA, Choe Y, Patterson KP et al (2013) Foxc1 is required by pericytes during fetal brain angiogenesis. Biol Open 2:647–659
45. Tümer Z, Bach-Holm D (2009) Axenfeld-Rieger syndrome and spectrum of PITX2 and FOXC1 mutations. Eur J Hum Genet 17:1527–1539
46. Delahaye A, Khung-Savatovsky S, Aboura A et al (2012) Pre- and postnatal phenotype of 6p25 deletions involving the FOXC1 gene. Am J Med Genet A 158A:2430–2438
47. Cellini E, Disciglio V, Novara F et al (2012) Periventricular heterotopia with white matter abnormalities associated with 6p25 deletion. Am J Med Genet A 158A:1793–1797
48. French CR, Seshadri S, Destefano AL et al (2014) Mutation of FOXC1 and PITX2 induces cerebral small-vessel disease. J Clin Invest 124:4877–4881
49. Revesz T, Holton JL, Lashley T et al (2009) Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol 118:115–130
50. Di Fede G, Giaccone G, Tagliavini F (2013) Hereditary and sporadic beta-amyloidoses. Front Biosci (Landmark Ed) 18:1202–1226
51. Biffi A, Greenberg SM (2011) Cerebral amyloid angiopathy: a systematic review. J Clin Neurol 7:1–9
52. Linn J, Halpin A, Demaerel P et al (2010) Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 74:1346–1350
53. Greenberg SM, Vernooij MW, Cordonnier C et al (2009) Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 8:165–174
54. Bacskai BJ, Frosch MP, Freeman SH et al (2007) Molecular imaging with Pittsburgh Compound B confirmed at autopsy: a case report. Arch Neurol 64:431–434
55. Baron J-C, Farid K, Dolan E et al (2014) Diagnostic utility of amyloid PET in cerebral amyloid angiopathy-related symptomatic intracerebral hemorrhage. J Cereb Blood Flow Metab 34:753–758
56. Rannikmäe K, Davies G, Thomson PA et al (2015) Common variation in COL4A1/COL4A2 is associated with sporadic cerebral small vessel disease. Neurology. doi:10.1212/WNL.0000000000001309
57. Schmidt H, Zeginigg M, Wiltgen M et al (2011) Genetic variants of the NOTCH3 gene in the elderly and magnetic resonance imaging correlates of age-related cerebral small vessel disease. Brain 134:3384–3397
58. Oka C, Tsujimoto R, Kajikawa M et al (2004) HtrA1 serine protease inhibits signaling mediated by Tgfbeta family proteins. Development 131:1041–1053
59. Shiga A, Nozaki H, Yokoseki A et al (2011) Cerebral small-vessel disease protein HTRA1 controls the amount of TGF-1 via cleavage of proTGF- 1. Hum Mol Genet 20:1800–1810
60. Ruiz-Ortega M, Rodríguez-Vita J, Sanchez-Lopez E et al (2007) TGF-beta signaling in vascular fibrosis. Cardiovasc Res 74:196–206
61. Gunda B, Mine M, Kovács T et al (2014) COL4A2 mutation causing adult onset recurrent intracerebral hemorrhage and leukoencephalopathy. J Neurol 261:500–503
62. Farrall AJ, Wardlaw JM (2009) Blood-brain barrier: ageing and microvascular disease––systematic review and meta-analysis. Neurobiol Aging 30:337–352
63. Kopan R, Ilagan MXG (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233
64. Joutel A, Vahedi K, Corpechot C et al (1997) Strong clustering and stereotyped nature of Notch3 mutations in CADASIL patients. Lancet 350:1511–1515
65. Rutten JW, Boon EMJ, Liem MK et al (2013) Hypomorphic NOTCH3 alleles do not cause CADASIL in humans. Hum Mutat 34:1486–1489
66. Ruchoux MM, Domenga V, Brulin P et al (2003) Transgenic mice expressing mutant Notch3 develop vascular alterations characteristic of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Am J Pathol 162:329–342
67. Joutel A, Andreux F, Gaulis S et al (2000) The ectodomain of the Notch3 receptor accumulates within the cerebrovasculature of CADASIL patients. J Clin Invest 105:597–605
68. Duering M, Karpinska A, Rosner S et al (2011) Co-aggregate formation of CADASIL-mutant NOTCH3: a single-particle analysis. Hum Mol Genet 20:3256–3265
69. Arboleda-Velasquez JF, Manent J, Lee JH et al (2011) Hypomorphic Notch 3 alleles link Notch signaling to ischemic cerebral small-vessel disease. Proc Natl Acad Sci 108:E128–E135
70. Monet-Leprêtre M, Haddad I, Baron-Menguy C et al (2013) Abnormal recruitment of extracellular matrix proteins by excess Notch3 ECD: a new pathomechanism in CADASIL. Brain 136:1830–1845
71. Jucker M, Walker LC (2013) Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501:45–51
72. Kast J, Hanecker P, Beaufort N et al (2014) Sequestration of latent TGF-β binding protein 1 into CADASIL-related Notch3-ECD deposits. Acta Neuropathol Commun 2:96
73. Ng SB, Buckingham KJ, Lee C et al (2010) Exome sequencing identifies the cause of a mendelian disorder. Nat Genet 42:30–35
74. Boycott KM, Vanstone MR, Bulman DE, MacKenzie AE (2013) Rare-disease genetics in the era of next-generation sequencing: discovery to translation. Nat Rev Genet 14:681–691
75. Low WC, Junna M, Börjesson-Hanson A et al (2007) Hereditary multi-infarct dementia of the Swedish type is a novel disorder different from NOTCH3 causing CADASIL. Brain 130:357–367
76. Nannucci S, Pescini F, Bertaccini B et al (2015) Clinical, familial, and neuroimaging features of CADASIL-like patients. Acta Neurol Scand 131:30–36
77. Foo J-N, Liu J-J, Tan E-K (2012) Whole-genome and whole-exome sequencing in neurological diseases. Nat Rev Neurol 8:508–517
78. Vrijenhoek T, Kraaijeveld K, Elferink M et al (2015) Next-generation sequencing-based genome diagnostics across clinical genetics centers: implementation choices and their effects. Eur J Hum Genet. doi:10.1038/ejhg.2014.279
79. Genomics England Ltd Genomics England|100,000 genomes project. http://www.genomicsengland.co.uk/. Accessed 3 May 2015
80. Bamshad MJ, Ng SB, Bigham AW et al (2011) Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet 12:745–755
81. Guerreiro R, Brás J, Hardy J, Singleton A (2014) Next generation sequencing techniques in neurological diseases: redefining clinical and molecular associations. Hum Mol Genet 44:1–7