Single nucleotide polymorphisms associated with sporadic brain arteriovenous malformations: Where do we stand?

Brain

Volumn 136, Issue 2, 2013, Pages 665-681

  Sturiale, Carmelo Lucio ^a   Puca, Alfredo ^a   Sebastiani, Paola ^b   Gatto, Ilaria ^a   Albanese, Alessio ^a   Di Rocco, Concezio ^a   Maira, Giulio ^a   Pola, Roberto ^a,c  

^a CATHOLIC UNIVERSITY   (Italy)

^b BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

angiogenesis; brain arteriovenous malformation; genome wide association study; inflammation; single nucleotide polymorphism

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; APOLIPOPROTEIN E; ENDOGLIN; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B4; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 6; STROMELYSIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ALLELE; ANGIOGENESIS; ARTICLE; ATTENTION; BLEEDING; BRAIN ARTERIOVENOUS MALFORMATION; BRAIN HEMORRHAGE; CLINICAL FEATURE; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC SUSCEPTIBILITY; GENOTYPE; HUMAN; META ANALYSIS; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL SIGNIFICANCE; SYSTEMATIC REVIEW;

EID: 84874290488     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws180     Document Type: Article

References (91)

1. Acalovschi D, Wiest T, Hartmann M, Farahmi M, Mansmann U, Auffarth GU, et al. Multiple levels of regulation of the interleukin-6 system in stroke. Stroke 2003; 34: 1864-9.
2. Achrol AS, Kim H, Pawlikowska L, Trudy Poon KY, McCulloch CE, Ko NU, et al. Association of tumor necrosis factor-alpha-238G4A and apolipoprotein E2 polymorphisms with intracranial hemorrhage after brain arteriovenous malformation treatment. Neurosurgery 2007; 61: 731-9; discussion 740.
3. Achrol AS, Pawlikowska L, McCulloch CE, Poon KY, Ha C, Zaroff JG, et al. UCSF Barteriovenous malformation Study Project. Tumor necrosis factor-alpha-238G4A promoter polymorphism is associated with increased risk of new hemorrhage in the natural course of patients with brain arteriovenous malformations. Stroke 2006; 37: 231-4.
4. Armstrong C, Abilleira S, Sitzer M, Markus HS, Bevan S. Polymorphisms in MMP family and TIMP genes and carotid artery intima-media thickness. Stroke 2007; 38: 2895-9.
5. Biehle SJ, Carrozzella J, Shukla R, Popplewell J, Swann M, Freeman N, et al. Apolipoprotein E isoprotein-specific interactions with tissue plasminogen activator. Biochim Biophys Acta 2004; 1689: 244-51.
6. Broderick J, Lu M, Jackson C, Pancioli A, Tilley BC, Fagan SC, et al. Apolipoprotein E phenotype and the efficacy of intravenous tissue plasminogen activator in acute ischemic stroke. Ann Neurol 2001; 49: 736-44.
7. Brown RD Jr, Wiebers DO, Torner JC, O'Fallon WM. Incidence and prevalence of intracranial vascular malformations in Olmsted County, Minnesota, 1965 to 1992. Neurology 1996; 46: 949-52.
8. Brull DJ, Leeson CP, Montgomery HE, Mullen M, deDivitiis M, Humphries SE, et al. The effect of the interleukin-6-174G4C promoter gene polymorphism on endothelial function in healthy volunteers. Eur J Clin Invest 2002; 32: 153-7.
9. Brull DJ, Montgomery HE, Sanders J, Dhamrait S, Luong L, Rumley A, et al. Interleukin-6 gene-174G4C and-572G4C promoter polymorphisms are strong predictors of plasma interleukin-6 levels after coronary artery bypass surgery. Arterioscler Thromb Vasc Biol 2001; 21: 1458-63.
10. Cazes A, Galaup A, Chomel C, Bignon M, Brechot N, Le Jan S, et al. Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton. Circ Res 2006; 99: 1207-15.
11. Chen H, Gu Y, Wu W, Chen D, Li P, Fan W, et al. Polymorphisms of the vascular endothelial growth factor A gene and susceptibility to sporadic brain arteriovenous malformation in a Chinese population. J Clin Neurosci 2011; 18: 549-53.
12. Chen H, Wilkins LM, Aziz N, Cannings C, Wyllie DH, Bingle C, et al. Single nucleotide polymorphisms in the human interleukin-1B gene affect transcription according to haplotype context. Hum Mol Genet 2006; 15: 519-29.
13. Chen Y, Zhu W, Bollen AW, Lawton MT, Barbaro NM, Dowd CF, et al. Evidence for inflammatory cell involvement in brain arteriovenous malformations. Neurosurgery 2008; 62: 1340-9.
14. Choi M, Scholl UI, Ji W, Liu T, Tikhonova IR, Zumbo P, et al. Genetic diagnosis by whole exome capture and massively parallel DNA sequencing. Proc Natl Acad Sci USA 2009; 106: 19096-101.
15. Chomel C, Cazes A, Faye C, Bignon M, Gomez E, Ardidie-Robouant C, et al. Interaction of the coiled-coil domain with glycosaminoglycans protects angiopoietinlike 4 from proteolysis and regulates its antiangiogenic activity. FASEB J 2009; 23: 940-9.
16. Clark JF, Huri DA, Carrozzella J, Jauch EC, Mehta P, Heaton D, et al. Isoforms of apolipoprotein E can modulate tPA-induced clot lysis in vitro. Front Biosci 2002; 7: a163-8.
17. Dasu MR, Barrow RE, Spies M, Herndon DN. Matrix metalloproteinase expression in cytokine stimulated human dermal fibroblasts. Burns 2003; 29: 527-31.
18. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, et al. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 1996; 87: 1161-9.
19. Deguara J, Burnand KG, Berg J, Green P, Lewis CM, Chinien G, et al. An increased frequency of the 5A allele in the promoter region of the MMP-3 gene is associated with abdominal aortic aneurysms. Hum Mol Genet 2007; 16: 3002-7.
20. Di Rocco C, Tamburrini G. Sturge-Weber syndrome. Childs Nerv Syst 2006; 22: 909-21.
21. Feuerstein GZ, Liu T, Barone FC. Cytokines, inflammation, and brain injury: role of tumor necrosis factor-alpha. Cerebrovasc Brain Metab Rev 1994; 6: 341-60.
22. Fishman D, Faulds G, Jeffery R, Mohamed-Ali V, Yudkin JS, Humphries S, et al. The effect of novel polymorphisms in the interleukin-6 (IL6) gene on IL6 transcription and plasma IL6 levels, and an association with systemic-onset juvenile chronic arthritis. J Clin Invest 1998; 102: 1369-76.
23. Flex A, Gaetani E, Pola R, Santoliquido A, Aloi F, Papaleo P, et al. The-174 G/C polymorphism of the interleukin-6 gene promoter is associated with peripheral artery occlusive disease. Eur J Vasc Endovasc Surg 2002; 24: 264-8.
24. Folsom AR, Peacock JM, Demerath E, Boerwinkle E. Variation in ANGPTL4 and risk of coronary heart disease: the Atherosclerosis Risk in Communities Study. Metabolism 2008; 57: 1591-6.
25. Fontanella M, Rubino E, Crobeddu E, Gallone S, Gentile S, Garbossa D, et al. Brain arteriovenous malformations are associated with interleukin-1 cluster gene polymorphisms. Neurosurgery 2012; 70: 12-17.
26. Fujimura M, Watanabe M, Shimizu H, Tominaga T. Expression of matrix metalloproteinases (MMPs) and tissue inhibitor of metalloproteinase (TIMP) in cerebral cavernous malformations: immunohistochemical analysis of MMP-2,-9 and TIMP-2. Acta Neurochir (Wien) 2007; 149: 179-83.
27. Galaup A, Cazes A, Le Jan S, Philippe J, Connault E, Le Coz E, et al. Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness. Proc Natl Acad Sci USA 2006; 103: 18721-6.
28. Gaetani P, Rodriguez y Baena R, Tartara F, Messina AL, Tancioni F, Schiavo R, et al. Metalloproteases and intracranial vascular lesions. Neurol Res 1999; 21: 385-90.
29. Gaudino M, Andreotti F, Zamparelli R, Di Castelnuovo A, Nasso G, Burzotta F, et al. The-174G/C interleukin-6 polymorphism influences postoperative interleukin-6 levels and postoperative atrial fibrillation. Is atrial fibrillation an inflammatory complication? Circulation 2003; 108 (Suppl 1): II195-9.
30. Gealekman O, Burkart A, Chouinard M, Nicoloro SM, Straubhaar J, Corvera S. Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production. Am J Physiol Endocrinol Metab 2008; 295: E1056-64.
31. Georges JL, Loukaci V, Poirier O, Evans A, Luc G, Arveiler D, et al. Interleukin-6 gene polymorphisms and susceptibility to myocardial infarction: the ECTIM study. Etude Cas-Temoin de l'Infarctus du Myocarde. J Mol Med 2001; 79: 300-5.
32. Gong ZP, Qiao ND, Gu YX, Song JP, Li PL, Qiu HJ, et al. Polymorphisms of VEGFA gene and susceptibility to hemorrhage risk of brain arteriovenous malformations in a Chinese population. Acta Pharmacol Sin 2011; 32: 1071-7.
33. Hashimoto T, Lawton MT, Wen G, Yang GY, Chaly T Jr, Stewart CL, et al. Gene microarray analysis of human brain arteriovenous malformations. Neurosurgery 2004; 54: 410-25.
34. Hashimoto T, Meng H, Young WL. Intracranial aneurysms: links between inflammation, hemodynamics and vascular remodeling. Neurol Res 2006; 28: 372-80.
35. Hashimoto T, Wen G, Lawton MT, Boudreau NJ, Bollen AW, Yang GY, et al. Abnormal expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in brain arteriovenous malformations. Stroke 2003; 34: 925-31.
36. Hato T, Tabata M, Oike Y. The role of angiopoietin-like proteins in angiogenesis and metabolism. Trends Cardiovasc Med 2008; 18: 6-14.
37. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003; 374: 1-20.
38. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, et al. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci USA 2009; 106: 9362-7.
39. Iacoviello L, Di Castelnuovo A, Gattone M, Pezzini A, Assanelli D, Lorenzet R, et al. Polymorphisms of the interleukin-1beta gene affect the risk of myocardial infarction and ischemic stroke at young age and the response of mononuclear cells to stimulation in vitro. Arterioscler Thromb Vasc Biol 2005; 25: 222-7.
40. Inoue S, Liu W, Inoue K, Mineharu Y, Takenaka K, Yamakawa H, et al. Combination of linkage and association studies for brain arteriovenous malformation. Stroke 2007; 38: 1368-1370.
41. Ito Y, Oike Y, Yasunaga K, Hamada K, Miyata K, Matsumoto S, et al. Inhibition of angiogenesis and vascular leakiness by angiopoietin related protein 4. Cancer Res 2003; 63: 6651-7.
42. Ivanov AI, Romanovsky AA. Putative dual role of ephrin-Eph receptor interactions in inflammation. IUBMB Life 2006; 58: 389-94.
43. Jiang N, Li X, Qi T, Guo S, Liang F, Huang Z. Susceptible gene single nucleotide polymorphism and hemorrhage risk in patients with brain arteriovenous malformation. J Clin Neurosci 2011; 18: 1279-81.
44. Jones KG, Brull DJ, Brown LC, Sian M, Greenhalgh RM, Humphries SE, et al. Interleukin-6 (IL6) and the prognosis of abdominal aortic aneurysms. Circulation 2001; 103: 2260-5.
45. Kim H, Hysi PG, Pawlikowska L, Choudhry S, Gonzá lez Burchard E, Kwok PY, et al. Population stratification in a case-control study of brain arteriovenous malformation in Latinos. Neuroepidemiology 2008a; 31: 224-8.
46. Kim H, Hysi PG, Pawlikowska L, Poon A, Burchard EG, Zaroff JG, et al. Common variants in interleukin-1-beta gene are associated with intracranial hemorrhage and susceptibility to brain arteriovenous malformation. Cerebrovasc Dis 2009a; 27: 176-82.
47. Kim I, Kim HG, Kim H, Kim HH, Park SK, Uhm CS, et al. Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem J 2000; 346: 603-10.
48. Kim H, Marchuk DA, Pawlikowska L, Chen Y, Su H, Yang GY, et al. Genetic considerations relevant to intracranial hemorrhage and brain arteriovenous malformations. Acta Neurochir Suppl 2008b; 105: 199-206.
49. Kim H, Pawlikowska L, Chen Y, Su H, Yang GY, Young WL. Brain arteriovenous malformation biology relevant to hemorrhage and implication for therapeutic development. Stroke 2009b; 40 (3 Suppl): S95-7.
50. Kimura R, Nishioka T, Soemantri A, Ishida T. Cis-acting effect of the IL1B C-31T polymorphism on IL-1 beta mRNA expression. Genes Immun 2004; 5: 572-5.
51. Koistinaho M, Koistinaho J. Interactions between Alzheimer's disease and cerebral ischemia-focus on inflammation. Brain Res Brain Res Rev 2005; 48: 240-50.
52. Lawton MT, Du R, Tran M, Achrol AS, McCulloch CE, Johnston SC, et al. Effect of presenting hemorrhage on outcome after microsurgical resection of brain arteriovenous malformations. Neurosurgery 2005; 56: 485-93.
53. Legry V, Bokor S, Cottel D, Beghin L, Catasta G, Nagy E, et al. Associations between common genetic polymorphisms in angiopoietin-like proteins 3 and 4 and lipid metabolism and adiposity in European adolescents and adults. J Clin Endocrinol Metab 2009; 94: 5070-7.
54. Lenk GM, Tromp G, Weinsheimer S, Gatalica Z, Berguer R, Kuivaniemi H. Whole genome expression profiling reveals a significant role for immune function in human abdominal aortic aneurysms. BMC Genomics 2007; 8: 237.
55. Leung CH, Poon WS, Yu LM, Wong GK, Ng HK. Apolipoprotein e genotype and outcome in aneurysmal subarachnoid hemorrhage. Stroke 2002; 33: 548-52.
56. Li C. Genetics and regulation of angiopoietin-like proteins 3 and 4. Curr Opin Lipidol 2006; 17: 152-6.
57. Limaye N, Wouters V, Uebelhoer M, Tuominen M, Wirkkala R, Mulliken JB, et al. Somatic mutations in angiopoietin receptor gene TEK cause solitary and multiple sporadic venous malformations. Nat Genet 2009; 41: 118-24.
58. Manolio TA. Genomewide association studies and assessment of the risk of disease. N Engl J Med 2010; 363: 166-76.
59. McCarron MO, Weir CJ, Muir KW, Hoffmann KL, Graffagnino C, Nicoll JA, et al. Effect of apolipoprotein E genotype on in-hospital mortality following intracerebral haemorrhage. Acta Neurol Scand 2003; 107: 106-9.
60. Miida T, Hirayama S. Impacts of angiopoietin-like proteins on lipoprotein metabolism and cardiovascular events. Curr Opin Lipidol 2010; 21: 70-5.
61. Miljkovic D, Trajkovic V. Inducible nitric oxide synthase activation by interleukin-17. Cytokine Growth Factor Rev 2004; 15: 21-32.
62. Mikhak B, Weinsheimer S, Pawlikowska L, Poon A, Kwok PY, Lawton MT, et al. Angiopoietin-like 4 (ANGPTL4) gene polymorphisms and risk of brain arteriovenous malformations. Cerebrovasc Dis 2011; 31: 338-45.
63. Moftakhar P, Hauptman JS, Malkasian D, Martin NA. Cerebral arteriovenous malformations. Part 1: cellular and molecular biology. Neurosurg Focus 2009; 26: E10.
64. Morgan L, Cooper J, Montgomery H, Kitchen N, Humphries SE. The interleukin-6 gene-174G4C and-572G4C promoter polymorphisms are related to cerebral aneurysms. J Neurol Neurosurg Psychiatry 2006; 77: 915-17.
65. Niki D, Katsu K, Yokouchi Y. Ontogeny of angiopoietin-like protein 1, 2, 3, 4, 5, and 7 genes during chick embryonic development. Dev Growth Differ 2009; 51: 821-32.
66. O'Donnell HC, Rosand J, Knudsen KA, Furie KL, Segal AZ, Chiu RI, et al. Apolipoprotein E genotype and the risk of recurrent lobar intracranial hemorrhage. N Engl J Med 2000; 342: 240-5.
67. Oikawa M, Kuniba H, Kondoh T, Kinoshita A, Nagayasu T, Niikawa N, et al. Familial brain arteriovenous malformation maps to 5p13-q14, 15q11-q13 or 18p11: linkage analysis with clipped fingernail DNA on high-density SNP array. Eur J Med Genet 2010; 53: 244-9.
68. Pawlikowska L, Poon KY, Achrol AS, McCulloch CE, Ha C, Lum K, et al. Apolipoprotein E epsilon 2 is associated with new hemorrhage risk in brain arteriovenous malformations. Neurosurgery 2006; 58: 838-43; discussion 838-43.
69. Pawlikowska L, Tran MN, Achrol AS, Ha C, Burchard E, Choudhry S, et al. UCSF Barteriovenous malformation Study Project. Polymorphisms in transforming growth factor-beta-related genes ALK1 and ENG are associated with sporadic brain arteriovenous malformations. Stroke 2005; 36: 2278-80.
70. Pawlikowska L, Tran MN, Achrol AS, McCulloch CE, Ha C, Lind DL, et al. UCSF Barteriovenous malformation Study Project. Polymorphisms in genes involved in inflammatory and angiogenic pathways and the risk of hemorrhagic presentation of brain arteriovenous malformations. Stroke 2004; 35: 2294-300.
71. Pola R, Flex A, Gaetani E, Flore R, Serricchio M, Pola P. Synergistic effect of-174 G/C polymorphism of the interleukin-6 gene promoter and 469 E/K polymorphism of the intercellular adhesion molecule-1 gene in Italian patients with history of ischemic stroke. Stroke 2003; 34: 881-5.
72. Reich K, Mossner R, Konig IR, Westphal G, Ziegler A, Neumann C. Promoter polymorphisms of the genes encoding tumor necrosis factor-alpha and interleukin-1beta are associated with different subtypes of psoriasis characterized by early and late disease onset. J Invest Dermatol 2002; 118: 155-63.
73. Romeo S, Pennacchio LA, Fu Y, Boerwinkle E, Tybjaerg-Hansen A, Hobbs HH, et al. Population-based resequencing of ANGPTL4 uncovers variations that reduce triglycerides and increase HDL. Nat Genet 2007; 39: 513-16.
74. Rosenberg GA. Matrix metalloproteinases in neuroinflammation. Glia 2002; 39: 279-91.
75. Rundek T, Elkind MS, Pittman J, Boden-Albala B, Martin S, Humphries SE, et al. Carotid intima-media thickness is associated with allelic variants of stromelysin-1, interleukin-6, and hepatic lipase genes: the Northern Manhattan Prospective Cohort Study. Stroke 2002; 33: 1420-3.
76. Schmidt D, Pache M, Schumacher M. The congenital unilateral retinocephalic vascular malformation syndrome (Bonnet-Dechaume-Blanc syndrome or Wyburn-Mason syndrome): review of the literature. Surv Ophthalmol 2008; 53: 227-49.
77. Erratum in: Surv Ophthalmol 2009; 54: 165.
78. Selmaj KW, Farooq M, Norton WT, Raine CS, Brosnan CF. Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor. J Immunol 1990; 144: 129-35.
79. Shenkar R, Shi C, Check IJ, Lipton HL, Awad IA. Concepts and hypotheses: inflammatory hypothesis in the pathogenesis of cerebral cavernous malformations. Neurosurgery 2007; 61: 693-702; discussion 702-3.
80. Simon M, Franke D, Ludwig M, Aliashkevich AF, Köster G, Oldenburg J, et al. Association of a polymorphism of the ACVRL1 gene with sporadic arteriovenous malformations of the central nervous system. J Neurosurg 2006; 104: 945-9.
81. Slowik A, Borratynska A, Turaj W, Pera J, Dziedzic T, Wloch D, et al. Interleukin 1beta-511 C/T polymorphism and risk of aneurismal subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 2006; 77: 279-80.
82. Suzuki K, Enghild JJ, Morodomi T, Salvesen G, Nagase H. Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 1990; 29: 10261-70.
83. Tian L, Zhou J, Casimiro MC, Liang B, Ojeifo JO, Wang M, et al. Activating peroxisome proliferator-activated receptor gamma mutant promotes tumor growth in vivo by enhancing angiogenesis. Cancer Res 2009; 69: 9236-44.
84. Tu J, Stoodley MA, Morgan MK, Storer KP, Smee R. Different responses of cavernous malformations and arteriovenous malformations to radiosurgery. J Clin Neurosci 2009; 16: 945-9.
85. Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000; 14: 2123-33.
86. Weinsheimer S, Kim H, Pawlikowska L, Chen Y, Lawton MT, Sidney S, et al. EPHB4 gene polymorphisms and risk of intracranial hemorrhage in patients with brain arteriovenous malformations. Circ Cardiovasc Genet 2009; 2: 476-82.
87. Xu B, Wu YQ, Huey M, Arthur HM, Marchuk DA, Hashimoto T, et al. Vascular endothelial growth factor induces abnormal microvasculature in the endoglin heterozygous mouse brain. J Cereb Blood Flow Metab 2004; 24: 237-44.
88. Young WL, Kwok PY, Pawlikowska L, Lawton MT, Kim H, Hysi PG, et al. Arteriovenous malformation. J Neurosurg 2007; 106: 731-2; author reply 732-3.
89. Young WL, Yang GY. Are there genetic influences on sporadic brain arteriovenous malformations? Stroke 2004; 35 (11 Suppl 1): 2740-5.
90. Zhao Y, Li P, Fan W, Chen D, Gu Y, Lu D, et al. The rs522616 polymorphism in the matrix metalloproteinase-3 (MMP-3) gene is associated with sporadic brain arteriovenous malformation in a Chinese population. Cerebrovasc Dis 2009; 27: 176-82.
91. Zhang HL, Wu J, Zhu J. The role of apolipoprotein E in Guillain-Barré syndrome and experimental autoimmune neuritis. J Biomed Biotechnol 2010; 2010: 357412.