Paraoxonase 1 and 2 gene variants and the ischemic stroke risk in Gran Canaria population: an association study and meta-analysis

References

• Feigin VL, Forouzanfar MH, Krishnamurthi R, Mensah GA, Connor M, Bennett DA, et al. Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet 2014;383(9913):245–54.
   PubMed Web of Science ®Google Scholar
• Adams HP, Jr., Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 1993;24(1):35–41.
   PubMed Web of Science ®Google Scholar
• Bevan S, Traylor M, Adib-Samii P, Malik R, Paul NL, Jackson C, et al. Genetic heritability of ischemic stroke and the contribution of previously reported candidate gene and genomewide associations. Stroke 2012;43(12):3161–7.
   PubMed Web of Science ®Google Scholar
• Schulz UG, Flossmann E, Rothwell PM. Heritability of ischemic stroke in relation to age, vascular risk factors, and subtypes of incident stroke in population-based studies. Stroke 2004;35(4):819–24.
   PubMed Web of Science ®Google Scholar
• Billecke S, Draganov D, Counsell R, Stetson P, Watson C, Hsu C, et al. Human serum paraoxonase (PON1) isozymes Q and R hydrolyze lactones and cyclic carbonate esters. Drug Metab Dispos 2000;28(11):1335–42.
   PubMed Web of Science ®Google Scholar
• Mackness MI, Arrol S, Durrington PN. Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein. FEBS Lett 1991;286(1–2):152–4.
   PubMed Web of Science ®Google Scholar
• Adkins S, Gan KN, Mody M, La Du BN. Molecular basis for the polymorphic forms of human serum paraoxonase/arylesterase: glutamine or arginine at position 191, for the respective A or B allozymes. Am J Hum Genet 1993;52(3):598–608.
   PubMed Web of Science ®Google Scholar
• Garin MC, James RW, Dussoix P, Blanche H, Passa P, Froguel P, et al. Paraoxonase polymorphism Met-Leu54 is associated with modified serum concentrations of the enzyme. A possible link between the paraoxonase gene and increased risk of cardiovascular disease in diabetes. J Clin Invest 1997;99(1):62–6.
   PubMed Web of Science ®Google Scholar
• Humbert R, Adler DA, Disteche CM, Hassett C, Omiecinski CJ, Furlong CE. The molecular basis of the human serum paraoxonase activity polymorphism. Nat Genet 1993;3(1):73–6.
   PubMed Web of Science ®Google Scholar
• Mackness B, Mackness MI, Arrol S, Turkie W, Durrington PN. Effect of the human serum paraoxonase 55 and 192 genetic polymorphisms on the protection by high density lipoprotein against low density lipoprotein oxidative modification. FEBS Lett 1998;423(1):57–60.
   PubMed Web of Science ®Google Scholar
• Richard SA, Frank EA, D'Souza CJ. Correlation between cholinesterase and paraoxonase 1 activities: case series of pesticide poisoning subjects. Bioimpacts 2013;3(3):119–22.
   PubMedGoogle Scholar
• Benmoyal-Segal L, Vander T, Shifman S, Bryk B, Ebstein RP, Marcus EL, et al. Acetylcholinesterase/paraoxonase interactions increase the risk of insecticide-induced Parkinson's disease. FASEB J 2005;19(3):452–4.
   PubMed Web of Science ®Google Scholar
• Ng CJ, Wadleigh DJ, Gangopadhyay A, Hama S, Grijalva VR, Navab M, et al. Paraoxonase-2 is a ubiquitously expressed protein with antioxidant properties and is capable of preventing cell-mediated oxidative modification of low density lipoprotein. J Biol Chem 2001;276(48):44444–9.
   PubMed Web of Science ®Google Scholar
• Mochizuki H, Scherer SW, Xi T, Nickle DC, Majer M, Huizenga JJ, et al. Human PON2 gene at 7q21.3: cloning, multiple mRNA forms, and missense polymorphisms in the coding sequence. Gene 1998;213(1–2):149–57.
   PubMed Web of Science ®Google Scholar
• Sanghera DK, Aston CE, Saha N, Kamboh MI. DNA polymorphisms in two paraoxonase genes (PON1 and PON2) are associated with the risk of coronary heart disease. Am J Hum Genet 1998;62(1):36–44.
   PubMed Web of Science ®Google Scholar
• Li BH, Zhang LL, Yin YW, Pi Y, Yang QW, Gao CY, et al. Association between paraoxonase 2 Ser311Cys polymorphism and ischemic stroke risk: a meta-analysis involving 5,008 subjects. Mol Biol Rep 2012;39(5):5623–30.
   PubMed Web of Science ®Google Scholar
• Slowik A, Wloch D, Szermer P, Wolkow P, Malecki M, Pera J, et al. Paraoxonase 2 gene C311S polymorphism is associated with a risk of large vessel disease stroke in a Polish population. Cerebrovasc Dis 2007;23(5-6):395–400.
   PubMed Web of Science ®Google Scholar
• Wang XY, Xue YM, Wen SJ, Zhang NL, Ji Z, Pan SY. The association of paraoxonase 2 gene C311S variant with ischemic stroke in Chinese type 2 diabetes mellitus patients. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2003;20(3):215–9.
   PubMedGoogle Scholar
• Rodriguez-Perez JC, Rodriguez-Esparragon F, Hernandez-Perera O, Anabitarte A, Losada A, Medina A, et al. Association of angiotensinogen M235T and A(-6)G gene polymorphisms with coronary heart disease with independence of essential hypertension: the PROCAGENE study. Prospective Cardiac Gene. J Am Coll Cardiol 2001;37(6):1536–42.
   PubMed Web of Science ®Google Scholar
• Worek F, Eyer P, Thiermann H. Determination of acetylcholinesterase activity by the Ellman assay: a versatile tool for in vitro research on medical countermeasures against organophosphate poisoning. Drug Test Anal 2012;4(3–4):282–91.
   PubMed Web of Science ®Google Scholar
• R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2008.
   Google Scholar
• Wolfgang V. Conducting meta-analyses in R with the metafor package. J Stat Soft 2010;36(3):1–48.
   Web of Science ®Google Scholar
• Mahdy AK, Wonnerth A, Huber K, Wojta J. Cardiovascular disease risk reduction by raising HDL cholesterol–current therapies and future opportunities. Br J Pharmacol 2012;167(6):1177–94.
   PubMed Web of Science ®Google Scholar
• Markus HS, Bevan S. Mechanisms and treatment of ischaemic stroke-insights from genetic associations. Nat Rev Neurol 2014; 10:723–730
   PubMed Web of Science ®Google Scholar
• Menini T, Gugliucci A. Paraoxonase 1 in neurological disorders. Redox Rep 2014;19(2):49–58.
   PubMed Web of Science ®Google Scholar
• Shenhar-Tsarfaty S, Waiskopf N, Ofek K, Shopin L, Usher S, Berliner S, et al. Atherosclerosis and arteriosclerosis parameters in stroke patients associate with paraoxonase polymorphism and esterase activities. Eur J Neurol 2013;20(6):891–8.
   PubMed Web of Science ®Google Scholar
• Mahrooz A, Gohari G, Hashemi MB, Zargari M, Musavi H, Abedini M, et al. R-carrying genotypes of serum paraoxonase (PON1) 192 polymorphism and higher activity ratio are related to susceptibility against ischemic stroke. Mol Biol Rep 2012;39(12):11177–85.
   PubMed Web of Science ®Google Scholar
• Voetsch B, Benke KS, Panhuysen CI, Damasceno BP, Loscalzo J. The combined effect of paraoxonase promoter and coding region polymorphisms on the risk of arterial ischemic stroke among young adults. Arch Neurol 2004;61(3):351–6.
   PubMedGoogle Scholar
• Dahabreh IJ, Kitsios GD, Kent DM, Trikalinos TA. Paraoxonase 1 polymorphisms and ischemic stroke risk: a systematic review and meta-analysis. Genet Med 2010 Oct;12(10):606–15.
   PubMed Web of Science ®Google Scholar
• Liu H, Xia P, Liu M, Ji XM, Sun HB, Tao L, et al. PON gene polymorphisms and ischaemic stroke: a systematic review and meta analysis. Int J Stroke 2013;8(2):111–23.
   PubMed Web of Science ®Google Scholar
• Ranade K, Kirchgessner TG, Iakoubova OA, Devlin JJ, DelMonte T, Vishnupad P, et al. Evaluation of the paraoxonases as candidate genes for stroke: Gln192Arg polymorphism in the paraoxonase 1 gene is associated with increased risk of stroke. Stroke 2005;36(11):2346–50.
   PubMed Web of Science ®Google Scholar
• Banerjee I. Relationship between Paraoxonase 1 (PON1) gene polymorphisms and susceptibility of stroke: a meta-analysis. Eur J Epidemiol 2010;25(7):449–58.
   PubMed Web of Science ®Google Scholar
• Zhang G, Li W, Li Z, Lv H, Ren Y, Ma R, et al. Association between paraoxonase gene and stroke in the Han Chinese population. BMC Med Genet 2013;14:16.
   PubMed Web of Science ®Google Scholar
• Kim DS, Crosslin DR, Auer PL, Suzuki SM, Marsillach J, Burt AA, et al. Rare coding variation in paraoxonase-1 is associated with ischemic stroke in the NHLBI Exome Sequencing Project. J Lipid Res 2014;55(6):1173–8.
   PubMed Web of Science ®Google Scholar
• Cozzi L, Campolo J, Parolini M, De MR, Patrosso MC, Marocchi A, et al. Paraoxonase 1 L55M, Q192R and paraoxonase 2 S311C alleles in atherothrombosis. Mol Cell Biochem 2013;374(1–2):233–8.
   PubMed Web of Science ®Google Scholar
• Ellison CA, Crane AL, Bonner MR, Knaak JB, Browne RW, Lein PJ, et al. PON1 status does not influence cholinesterase activity in Egyptian agricultural workers exposed to chlorpyrifos. Toxicol Appl Pharmacol 2012;265(3):308–15.
   PubMed Web of Science ®Google Scholar
• Sirivarasai J, Kaojarern S, Yoovathaworn K, Sura T. Paraoxonase (PON1) polymorphism and activity as the determinants of sensitivity to organophosphates in human subjects. Chem Biol Interact 2007;168(3):184–92.
   PubMed Web of Science ®Google Scholar
• Sunay SZ, Kayaalti Z, Bayrak T, Soylemezoglu T. Effect of paraoxonase 1 192 Q/R polymorphism on paraoxonase and acetylcholinesterase enzyme activities in a Turkish population exposed to organophosphate. Toxicol Ind Health 2015;31(12):1061–8.
   PubMed Web of Science ®Google Scholar
• Fregel R, Gomes V, Gusmao L, Gonzalez AM, Cabrera VM, Amorim A, et al. Demographic history of Canary Islands male gene-pool: replacement of native lineages by European. BMC Evol Biol 2009;9:181.
   PubMed Web of Science ®Google Scholar
• Maca-Meyer N, Villar J, Perez-Mendez L, Cabrera de LA, Flores C. A tale of aborigines, conquerors and slaves: Alu insertion polymorphisms and the peopling of Canary Islands. Ann Hum Genet 2004;68(Pt 6):600–5.
   PubMed Web of Science ®Google Scholar
• Fregel R, Betancor E, Suarez NM, Cabrera VM, Pestano J, Larruga JM, et al. Temporal evolution of the ABO allele frequencies in the Canary Islands: the impact of the European colonization. Immunogenetics 2009;61(9):603–10.
   PubMed Web of Science ®Google Scholar
• Gonzalez HA, Fabre PO, Lopez Fernandez JC, Diaz NS, Cabrera HA. Risk factors, etiology and prognosis in patients with ischemic stroke and diabetes mellitus. Rev Clin Esp 2008;208(11):546–50.
   PubMed Web of Science ®Google Scholar