Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
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Single Nucleotide Polymorphism in Patients with Moyamoya Disease

  • Park, Young Seok (Department of Neurosurgery, Chungbuk National University College of Medicine, Chungbuk National University Hospital)
  • Received : 2015.02.22
  • Accepted : 2015.04.29
  • Published : 2015.06.28
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Abstract

Moyamoya disease (MMD) is a chronic, progressive, cerebrovascular occlusive disorder that displays various clinical features and results in cerebral infarct or hemorrhagic stroke. Specific genes associated with the disease have not yet been identified, making identification of at-risk patients difficult before clinical manifestation. Familial MMD is not uncommon, with as many as 15% of MMD patients having a family history of the disease, suggesting a genetic etiology. Studies of single nucleotide polymorphisms (SNPs) in MMD have mostly focused on mechanical stress on vessels, endothelium, and the relationship to atherosclerosis. In this review, we discuss SNPs studies targeting the genetic etiology of MMD. Genetic analyses in familial MMD and genome-wide association studies represent promising strategies for elucidating the pathophysiology of this condition. This review also discusses future research directions, not only to offer new insights into the origin of MMD, but also to enhance our understanding of the genetic aspects of MMD. There have been several SNP studies of MMD. Current SNP studies suggest a genetic contribution to MMD, but further reliable and replicable data are needed. A large cohort or family-based design would be important. Modern SNP studies of MMD depend on novel genetic, experimental, and database methods that will hopefully hasten the arrival of a consensus conclusion.

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References

  1. Achrol AS, Guzman R, Lee M, Steinberg GK : Pathophysiology and genetic factors in moyamoya disease. Neurosurg Focus 26 : E4, 2009
  2. Andreone V, Ciarmiello A, Fusco C, Ambrosanio G, Florio C, Linfante I : Moyamoya disease in Italian monozygotic twins. Neurology 53 : 1332-1335, 1999 https://doi.org/10.1212/WNL.53.6.1332
  3. Aoyagi M, Fukai N, Sakamoto H, Shinkai T, Matsushima Y, Yamamoto M, et al. : Altered cellular responses to serum mitogens, including platelet-derived growth factor, in cultured smooth muscle cells derived from arteries of patients with moyamoya disease. J Cell Physiol 147 : 191-198, 1991 https://doi.org/10.1002/jcp.1041470202
  4. Aoyagi M, Ogami K, Matsushima Y, Shikata M, Yamamoto M, Yamamoto K : Human leukocyte antigen in patients with moyamoya disease. Stroke 26 : 415-417, 1995 https://doi.org/10.1161/01.STR.26.3.415
  5. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, et al. : Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21 : 7724-7232, 2001 https://doi.org/10.1523/JNEUROSCI.21-19-07724.2001
  6. Baba T, Houkin K, Kuroda S : Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79 : 900-904, 2008 https://doi.org/10.1136/jnnp.2007.130666
  7. Bonduel M, Hepner M, Sciuccati G, Torres AF, Tenembaum S : Prothrombotic disorders in children with moyamoya syndrome. Stroke 32 : 1786-1792, 2001 https://doi.org/10.1161/01.STR.32.8.1786
  8. Burke GM, Burke AM, Sherma AK, Hurley MC, Batjer HH, Bendok BR : Moyamoya disease : a summary. Neurosurg Focus 26 : E11, 2009
  9. Cao Y, Hong A, Schulten H, Post MJ : Update on therapeutic neovascularization. Cardiovasc Res 65 : 639-648, 2005 https://doi.org/10.1016/j.cardiores.2004.11.020
  10. Cho HJ, Jung YH, Kim YD, Nam HS, Kim DS, Heo JH : The different infarct patterns between adulthood-onset and childhood-onset moyamoya disease. J Neurol Neurosurg Psychiatry 82 : 38-40, 2011 https://doi.org/10.1136/jnnp.2009.181487
  11. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T : Increased expression of serum Matrix Metalloproteinase-9 in patients with moyamoya disease. Surg Neurol 72 : 476-480; discussion 480, 2009 https://doi.org/10.1016/j.surneu.2008.10.009
  12. Fukui M : Current state of study on moyamoya disease in Japan. Surg Neurol 47 : 138-143, 1997 https://doi.org/10.1016/S0090-3019(96)00358-8
  13. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, et al. : Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273 : 30336-30343, 1998 https://doi.org/10.1074/jbc.273.46.30336
  14. Guo DC, Papke CL, Tran-Fadulu V, Regalado ES, Avidan N, Johnson RJ, et al. : Mutations in smooth muscle alpha-actin (ACTA2) cause coronary artery disease, stroke, and Moyamoya disease, along with thoracic aortic disease. Am J Hum Genet 84 : 617-627, 2009 https://doi.org/10.1016/j.ajhg.2009.04.007
  15. Han DH, Kwon OK, Byun BJ, Choi BY, Choi CW, Choi JU, et al. : A co-operative study : clinical characteristics of 334 Korean patients with moyamoya disease treated at neurosurgical institutes (1976-1994). The Korean Society for Cerebrovascular Disease. Acta Neurochir (Wien) 142 : 1263-1273; discussion 1273-1274, 2000 https://doi.org/10.1007/s007010070024
  16. Han DH, Nam DH, Oh CW : Moyamoya disease in adults : characteristics of clinical presentation and outcome after encephalo-duro-arterio-synangiosis. Clin Neurol Neurosurg 99 Suppl 2 : S151-S155, 1997 https://doi.org/10.1016/S0303-8467(97)80015-7
  17. Han H, Pyo CW, Yoo DS, Huh PW, Cho KS, Kim DS : Associations of Moyamoya patients with HLA class I and class II alleles in the Korean population. J Korean Med Sci 18 : 876-880, 2003 https://doi.org/10.3346/jkms.2003.18.6.876
  18. Hojo M, Hoshimaru M, Miyamoto S, Taki W, Nagata I, Asahi M, et al. : Role of transforming growth factor-beta1 in the pathogenesis of moyamoya disease. J Neurosurg 89 : 623-629, 1998 https://doi.org/10.3171/jns.1998.89.4.0623
  19. Hong SH, Wang KC, Kim SK, Cho BK, Park MH : Association of HLA-DR and -DQ genes with familial Moyamoya disease in Koreans. J Korean Neurosurg Soc 46 : 558-563, 2009 https://doi.org/10.3340/jkns.2009.46.6.558
  20. Hoshimaru M, Takahashi JA, Kikuchi H, Nagata I, Hatanaka M : Possible roles of basic fibroblast growth factor in the pathogenesis of moyamoya disease : an immunohistochemical study. J Neurosurg 75 : 267-270, 1991 https://doi.org/10.3171/jns.1991.75.2.0267
  21. Ikeda E, Achen MG, Breier G, Risau W : Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 270 : 19761-19766, 1995 https://doi.org/10.1074/jbc.270.34.19761
  22. Ikeda H, Sasaki T, Yoshimoto T, Fukui M, Arinami T : Mapping of a familial moyamoya disease gene to chromosome 3p24.2-p26. Am J Hum Genet 64 : 533-537, 1999 https://doi.org/10.1086/302243
  23. Inoue TK, Ikezaki K, Sasazuki T, Matsushima T, Fukui M : Linkage analysis of moyamoya disease on chromosome 6. J Child Neurol 15 : 179-182, 2000 https://doi.org/10.1177/088307380001500307
  24. Inoue TK, Ikezaki K, Sasazuki T, Ono T, Kamikawaji N, Matsushima T, et al. : DNA typing of HLA in the patients with moyamoya disease. Jpn J Hum Genet 42 : 507-515, 1997 https://doi.org/10.1007/BF02767027
  25. Issa R, Krupinski J, Bujny T, Kumar S, Kaluza J, Kumar P : Vascular endothelial growth factor and its receptor, KDR, in human brain tissue after ischemic stroke. Lab Invest 79 : 417-425, 1999
  26. Jin KL, Mao XO, Nagayama T, Goldsmith PC, Greenberg DA : Induction of vascular endothelial growth factor and hypoxia-inducible factor-1alpha by global ischemia in rat brain. Neuroscience 99 : 577-585, 2000 https://doi.org/10.1016/S0306-4522(00)00207-4
  27. Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, et al. : A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet 56 : 34-40, 2011 https://doi.org/10.1038/jhg.2010.132
  28. Kastrup A, Schulz JB, Mader I, Dichgans J, Küker W : Diffusion-weighted MRI in patients with symptomatic internal carotid artery disease. J Neurol 249 : 1168-1174, 2002 https://doi.org/10.1007/s00415-002-0793-2
  29. Kim SH, Hwang H, Chae JH, Kim KJ, Hwang YS, Lim BC : Ischemic stroke in a 7-month-old infant with antiphospholipid antibody and homozygous C677T methylenetetrahydrofolate reductase (MTHFR) polymorphism. J Child Neurol 25 : 1047-1050, 2010 https://doi.org/10.1177/0883073809356710
  30. Kim SK, Yoo JI, Cho BK, Hong SJ, Kim YK, Moon JA, et al. : Elevation of CRABP-I in the cerebrospinal fluid of patients with Moyamoya disease. Stroke 34 : 2835-2841, 2003 https://doi.org/10.1161/01.STR.0000100159.43123.D7
  31. Kitahara T, Okumura K, Semba A, Yamaura A, Makino H : Genetic and immunologic analysis on moya-moya. J Neurol Neurosurg Psychiatry 45 : 1048-1052, 1982 https://doi.org/10.1136/jnnp.45.11.1048
  32. Kraemer M, Horn PA, Roder C, Khan N, Diehl RR, Berlit P, et al. : Analysis of human leucocyte antigen genes in Caucasian patients with idiopathic moyamoya angiopathy. Acta Neurochir (Wien) 154 : 445-454, 2012 https://doi.org/10.1007/s00701-011-1261-5
  33. Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y; Research Committee on Moyamoya Disease in Japan : Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease : results of multicenter survey in Japan. Stroke 38 : 1430-1435, 2007 https://doi.org/10.1161/STROKEAHA.106.478297
  34. Kuroda S, Houkin K : Moyamoya disease : current concepts and future perspectives. Lancet Neurol 7 : 1056-1066, 2008 https://doi.org/10.1016/S1474-4422(08)70240-0
  35. Lee CZ, Xu B, Hashimoto T, McCulloch CE, Yang GY, Young WL : Doxycycline suppresses cerebral matrix metalloproteinase-9 and angiogenesis induced by focal hyperstimulation of vascular endothelial growth factor in a mouse model. Stroke 35 : 1715-1719, 2004 https://doi.org/10.1161/01.STR.0000129334.05181.b6
  36. Lee SR, Lo EH : Induction of caspase-mediated cell death by matrix metalloproteinases in cerebral endothelial cells after hypoxia-reoxygenation. J Cereb Blood Flow Metab 24 : 720-727, 2004 https://doi.org/10.1097/01.WCB.0000122747.72175.47
  37. Li H, Zhang ZS, Liu W, Yang WZ, Dong ZN, Ma MJ, et al. : Association of a functional polymorphism in the MMP-3 gene with Moyamoya Disease in the Chinese Han population. Cerebrovasc Dis 30 : 618-625, 2010 https://doi.org/10.1159/000319893
  38. Liu C, Roder C, Schulte C, Kasuya H, Akagawa H, Nishizawa T, et al. : Analysis of TGFB1 in European and Japanese Moyamoya disease patients. Eur J Med Genet 55 : 531-534, 2012 https://doi.org/10.1016/j.ejmg.2012.05.002
  39. Liu W, Hashikata H, Inoue K, Matsuura N, Mineharu Y, Kobayashi H, et al. : A rare Asian founder polymorphism of Raptor may explain the high prevalence of moyamoya disease among East Asians and its low prevalence among Caucasians. Environ Health Prev Med 15 : 94-104, 2010 https://doi.org/10.1007/s12199-009-0116-7
  40. Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. : Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One 6 : e22542, 2011 https://doi.org/10.1371/journal.pone.0022542
  41. Liu W, Senevirathna ST, Hitomi T, Kobayashi H, Roder C, Herzig R, et al. : Genomewide association study identifies no major founder variant in Caucasian moyamoya disease. J Genet 92 : 605-609, 2013 https://doi.org/10.1007/s12041-013-0304-5
  42. Lo EH, Dalkara T, Moskowitz MA : Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4 : 399-415, 2003
  43. Malek AM, Connors S, Robertson RL, Folkman J, Scott RM : Elevation of cerebrospinal fluid levels of basic fibroblast growth factor in moyamoya and central nervous system disorders. Pediatr Neurosurg 27 : 182-189, 1997 https://doi.org/10.1159/000121249
  44. McKasson MJ, Golomb MR : Two children with both arm ischemia and arterial ischemic stroke during the perinatal period. J Child Neurol 26 : 1548-1554, 2011 https://doi.org/10.1177/0883073811413277
  45. Mineharu Y, Liu W, Inoue K, Matsuura N, Inoue S, Takenaka K, et al. : Autosomal dominant moyamoya disease maps to chromosome 17q25.3. Neurology 70 (24 Pt 2) : 2357-2363, 2008 https://doi.org/10.1212/01.wnl.0000291012.49986.f9
  46. Miyatake S, Miyake N, Touho H, Nishimura-Tadaki A, Kondo Y, Okada I, et al. : Homozygous c.14576G>A variant of RNF213 predicts early-onset and severe form of moyamoya disease. Neurology 78 : 803-810, 2012 https://doi.org/10.1212/WNL.0b013e318249f71f
  47. Miyatake S, Touho H, Miyake N, Ohba C, Doi H, Saitsu H, et al. : Sibling cases of moyamoya disease having homozygous and heterozygous c.14576G>A variant in RNF213 showed varying clinical course and severity. J Hum Genet 57 : 804-806, 2012 https://doi.org/10.1038/jhg.2012.105
  48. Miyawaki S, Imai H, Takayanagi S, Mukasa A, Nakatomi H, Saito N : Identification of a genetic variant common to moyamoya disease and intracranial major artery stenosis/occlusion. Stroke 43 : 3371-3374, 2012 https://doi.org/10.1161/STROKEAHA.112.663864
  49. Moncada S, Higgs A : The L-arginine-nitric oxide pathway. N Engl J Med 329 : 2002-2012, 1993 https://doi.org/10.1056/NEJM199312303292706
  50. Mukhopadhyay D, Tsiokas L, Zhou XM, Foster D, Brugge JS, Sukhatme VP : Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature 375 : 577-581, 1995 https://doi.org/10.1038/375577a0
  51. Nanba R, Kuroda S, Tada M, Ishikawa T, Houkin K, Iwasaki Y : Clinical features of familial moyamoya disease. Childs Nerv Syst 22 : 258-262, 2006 https://doi.org/10.1007/s00381-005-1230-5
  52. Nanba R, Tada M, Kuroda S, Houkin K, Iwasaki Y : Sequence analysis and bioinformatics analysis of chromosome 17q25 in familial moyamoya disease. Childs Nerv Syst 21 : 62-68, 2005 https://doi.org/10.1007/s00381-004-1005-4
  53. Park YS, Jeon YJ, Kim HS, Chae KY, Oh SH, Han IB, et al. : The role of VEGF and KDR polymorphisms in moyamoya disease and collateral revascularization. PLoS One 7 : e47158, 2012 https://doi.org/10.1371/journal.pone.0047158
  54. Park YS, Jeon YJ, Kim HS, Han IB, Choi JU, Kim DS, et al. : The roles of methylenetetrahydrofolate reductase 677C>T and 1298A>C polymorphisms in moyamoya disease patients. Childs Nerv Syst 30 : 1687-1695, 2014 https://doi.org/10.1007/s00381-014-2495-3
  55. Park YS, Jeon YJ, Kim HS, Han IB, Oh SH, Kim DS, et al. : The GC + CC genotype at position -418 in TIMP-2 promoter and the -1575GA/-1306CC genotype in MMP-2 is genetic predisposing factors for prevalence of moyamoya disease. BMC Neurol 14 : 180, 2014 https://doi.org/10.1186/s12883-014-0180-5
  56. Park YS, Min KT, Kim TG, Lee YH, Cheong HJ, Yeom IS, et al. : Age-specific eNOS polymorphisms in moyamoya disease. Childs Nerv Syst 27 : 1919-1926, 2011 https://doi.org/10.1007/s00381-011-1504-z
  57. Roder C, Peters V, Kasuya H, Nishizawa T, Wakita S, Berg D, et al. : Analysis of ACTA2 in European Moyamoya disease patients. Eur J Paediatr Neurol 15 : 117-122, 2011 https://doi.org/10.1016/j.ejpn.2010.09.002
  58. Roder C, Peters V, Kasuya H, Nishizawa T, Takehara Y, Berg D, et al. : Common genetic polymorphisms in moyamoya and atherosclerotic disease in Europeans. Childs Nerv Syst 27 : 245-252, 2011 https://doi.org/10.1007/s00381-010-1241-8
  59. Roder C, Peters V, Kasuya H, Nishizawa T, Takehara Y, Berg D, et al. : Polymorphisms in TGFB1 and PDGFRB are associated with Moyamoya disease in European patients. Acta Neurochir (Wien) 152 : 2153-2160, 2010 https://doi.org/10.1007/s00701-010-0711-9
  60. Ruel M, Khan TA, Voisine P, Bianchi C, Sellke FW : Vasomotor dysfunction after cardiac surgery. Eur J Cardiothorac Surg 26 : 1002-1014, 2004 https://doi.org/10.1016/j.ejcts.2004.07.040
  61. Sakamoto S, Kiura Y, Yamasaki F, Shibukawa M, Ohba S, Shrestha P, et al. : Expression of vascular endothelial growth factor in dura mater of patients with moyamoya disease. Neurosurg Rev 31 : 77-81; discussion 81, 2008
  62. Sakurai K, Horiuchi Y, Ikeda H, Ikezaki K, Yoshimoto T, Fukui M, et al. : A novel susceptibility locus for moyamoya disease on chromosome 8q23. J Hum Genet 49 : 278-281, 2004 https://doi.org/10.1007/s10038-004-0143-6
  63. Schork NJ, Fallin D, Lanchbury JS : Single nucleotide polymorphisms and the future of genetic epidemiology. Clin Genet 58 : 250-264, 2000
  64. Scott RM : Arteriovenous malformation and moyamoya disease. Childs Nerv Syst 13 : 357, 1997 https://doi.org/10.1007/s003810050097
  65. Skardoutsou A, Voudris KA, Mastroyianni S, Vagiakou E, Magoufis G, Koukoutsakis P : Moya moya syndrome in a child with pyruvate kinase deficiency and combined prothrombotic factors. J Child Neurol 22 : 474-478, 2007 https://doi.org/10.1177/0883073807301934
  66. Sonobe S, Fujimura M, Niizuma K, Nishijima Y, Ito A, Shimizu H, et al. : Temporal profile of the vascular anatomy evaluated by 9.4-T magnetic resonance angiography and histopathological analysis in mice lacking RNF213 : a susceptibility gene for moyamoya disease. Brain Res 1552 : 64-71, 2014 https://doi.org/10.1016/j.brainres.2014.01.011
  67. Starke RM, Komotar RJ, Connolly ES : Optimal surgical treatment for moyamoya disease in adults : direct versus indirect bypass. Neurosurg Focus 26 : E8, 2009
  68. Takekawa Y, Umezawa T, Ueno Y, Sawada T, Kobayashi M : Pathological and immunohistochemical findings of an autopsy case of adult moyamoya disease. Neuropathology 24 : 236-242, 2004 https://doi.org/10.1111/j.1440-1789.2004.00550.x
  69. Thomas KA : Vascular endothelial growth factor, a potent and selective angiogenic agent. J Biol Chem 271 : 603-606, 1996 https://doi.org/10.1074/jbc.271.2.603
  70. Wakai K, Tamakoshi A, Ikezaki K, Fukui M, Kawamura T, Aoki R, et al. : Epidemiological features of moyamoya disease in Japan : findings from a nationwide survey. Clin Neurol Neurosurg 99 Suppl 2 : S1-S5, 1997 https://doi.org/10.1016/S0303-8467(97)00031-0
  71. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH : Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269 : 26988-26995, 1994
  72. Wang X, Zhang Z, Liu W, Xiong Y, Sun W, Huang X, et al. : Impacts and interactions of PDGFRB, MMP-3, TIMP-2, and RNF213 polymorphisms on the risk of Moyamoya disease in Han Chinese human subjects. Gene 526 : 437-442, 2013 https://doi.org/10.1016/j.gene.2013.05.083
  73. Weinberg DG, Arnaout OM, Rahme RJ, Aoun SG, Batjer HH, Bendok BR : Moyamoya disease : a review of histopathology, biochemistry, and genetics. Neurosurg Focus 30 : E20, 2011 https://doi.org/10.3171/2011.3.FOCUS1151
  74. Wu Z, Jiang H, Zhang L, Xu X, Zhang X, Kang Z, et al. : Molecular analysis of RNF213 gene for moyamoya disease in the Chinese Han population. PLoS One 7 : e48179, 2012 https://doi.org/10.1371/journal.pone.0048179
  75. Yamamoto M, Aoyagi M, Fukai N, Matsushima Y, Yamamoto K : Differences in cellular responses to mitogens in arterial smooth muscle cells derived from patients with moyamoya disease. Stroke 29 : 1188-1193, 1998 https://doi.org/10.1161/01.STR.29.6.1188
  76. Yamashita M, Oka K, Tanaka K : Histopathology of the brain vascular network in moyamoya disease. Stroke 14 : 50-58, 1983 https://doi.org/10.1161/01.STR.14.1.50
  77. Yamauchi T, Tada M, Houkin K, Tanaka T, Nakamura Y, Kuroda S, et al. : Linkage of familial moyamoya disease (spontaneous occlusion of the circle of Willis) to chromosome 17q25. Stroke 31 : 930-935, 2000 https://doi.org/10.1161/01.STR.31.4.930
  78. Yoshimoto T, Houkin K, Takahashi A, Abe H : Angiogenic factors in moyamoya disease. Stroke 27 : 2160-2165, 1996 https://doi.org/10.1161/01.STR.27.12.2160

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