Abstract
Psoriasis is a chronic, autoimmune skin disease. In psoriasis, PON1 activity is diminished and peroxidation biomarkers are elevated. The most studied PON1 polymorphisms are rs662 (A > G) and rs854560 (A > T), which have been associated with the antioxidant activity of PON1, risk of cardiovascular diseases and psoriasis development. The aim of this study, was to determine the association of rs662 (A > G) and rs854560 (A > T) PON1 polymorphisms with psoriasis susceptibility in Western Mexico population. In this case-control study, we included 104 psoriasis patients and 124 control subjects. The genotyping of polymorphisms rs662 (A > G) and rs854560 (A > T) of PON1 was carried out by PCR-RFLPs. The lipid profiles were quantified by enzymatic colorimetric method, and PON1 activity was determined by spectrophotometry. The lipid profile levels, except HDL-C and atherogenic index, were higher in patients vs. controls. Patients presented lower paraoxonase and arylesterase activity. The G allele of rs662 (A > G) is associated with risk for psoriasis, while the T allele of rs854560 (A > T) is associated with low susceptibility to psoriasis. The AG haplotype was more frequent within the patient group (p < 0.05). The AA and AG genotypes of rs662 (A > G) and TT and AA genotypes of rs854560 (A > T) are associated with lower PONase and ARE activity in patients vs. controls. Patients with the G allele of rs662 (G > A) and T alleles of rs854560 (A > T) show significant differences in the lipid levels in comparison to controls. These results suggest that carriers of G allele of rs662 (A > G) present a greater susceptibility to psoriasis.
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References
Davidson A, Diamond B (2001) Autoimmune diseases. N Engl J Med 345(5):340–350
Gu W-J, Weng C-L, Zhao Y-T, Liu Q-H, Yin R-X (2013) Psoriasis and risk of cardiovascular disease: a meta-analysis of cohort studies. Int J Cardiol 168(5):4992–4996
Zhou Q, Mrowietz U, Rostami-Yazdi M (2009) Oxidative stress in the pathogenesis of psoriasis. Free Radical Biol Med 47(7):891–905
Kural BV, Örem A, Çimşit G, Yandı YE, Calapoǧlu M (2003) Evaluation of the atherogenic tendency of lipids and lipoprotein content and their relationships with oxidant–antioxidant system in patients with psoriasis. Clin Chim Acta 328(1–2):71–82
Mallbris L, Granath F, Hamsten A, Ståhle M (2006) Psoriasis is associated with lipid abnormalities at the onset of skin disease. J Am Acad Dermatol 54(4):614–621
Miller I, Skaaby T, Ellervik C, Jemec G (2013) Quantifying cardiovascular disease risk factors in patients with psoriasis: a meta-analysis. Br J Dermatol 169(6):1180–1187
Mackness MI, Arrol S, Abbott C, Durrington PN (1993) Protection of low-density lipoprotein against oxidative modification by high-density lipoprotein associated paraoxonase. Atherosclerosis 104(1):129–135
Mata C, Lares M, Hernández P (2013) Enzima Paraoxonasa 1 y modulación del Estrés Oxidativo/Enzyme paraoxonase 1 and Modulation of Oxidative Stress. Síndrome Cardiometabólico 3(1):6
Jakubowski H (2000) Calcium-dependent human serum homocysteine thiolactone hydrolase a protective mechanism against proteinn-homocysteinylation. J Biol Chem 275(6):3957–3962
Aviram M, Rosenblat M (2004) Paraoxonases 1, 2, and 3, oxidative stress, and macrophage foam cell formation during atherosclerosis development. Free Radical Biol Med 37(9):1304–1316
Mackness MI, Harty D, Bhatnagar D et al (1991) Serum paraoxonase activity in familial hypercholesterolaemia and insulin-dependent diabetes mellitus. Atherosclerosis 86(2):193–199
Baskol G, Demir H, Baskol M et al (2005) Assessment of paraoxonase 1 activity and malondialdehyde levels in patients with rheumatoid arthritis. Clin Biochem 38(10):951–955
Toker A, Kadı M, Yıldırım AK, Aksoy H, Akçay F (2009) Serum lipid profile paraoxonase and arylesterase activities in psoriasis. Cell Biochem Funct 27(3):176–180
Huen K, Richter R, Furlong C, Eskenazi B, Holland N (2009) Validation of PON1 enzyme activity assays for longitudinal studies. Clin Chim Acta 402(1–2):67–74
Grubiša I, Otašević P, Dimković N, Nedeljković I, Toljić B, Vučinić N (2013) Genetic polymorphisms of paraoxonase 1 and susceptibility to atherogenesis. Srp Arh Celok Lek 141(9–10):629–633
Bae S-C, Lee YH (2019) Associations between paraoxonase 1 (PON1) polymorphisms and susceptibility and PON1 activity in rheumatoid arthritis patients, and comparison of PON1 activity in patients and controls: a meta-analysis. Clin Rheumatol 38(8):2141–2149
Liu T, Zhang X, Zhang J et al (2014) Association between PON1 rs662 polymorphism and coronary artery disease. Eur J Clin Nutr 68(9):1029–1035
Mackness B, Mackness MI, Arrol S, Turkie W, Durrington PN (1998) 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 423(1):57–60
Luo Z, Pu L, Muhammad I, Chen Y, Sun X (2018) Associations of the PON1 rs662 polymorphism with circulating oxidized low-density lipoprotein and lipid levels: a systematic review and meta-analysis. Lipids Health Dis 17(1):281
Mackness MI, Mackness B, Durrington PN, Connelly PW, Hegele RA (1996) Paraoxonase: biochemistry, genetics and relationship to plasma lipoproteins. Curr Opin Lipidol 7(2):69–76
Li W-F, Costa LG, Richter RJ et al (2000) Catalytic efficiency determines the in-vivo efficacy of PON1 for detoxifying organophosphorus compounds. Pharmacogenet Genomics 10(9):767–779
Kuremoto K, Watanabe Y, Ohmura H, Shimada K, Mokuno H, Daida H (2003) R/R genotype of human paraoxonase (PON1) is more protective against lipoprotein oxidation and coronary artery disease in Japanese subjects. J Atheroscleros Thromb 10(2):85–92
Asefi M, Vaisi-Raygani A, Bahrehmand F et al (2012) Paraoxonase 1 (PON1) 55 polymorphism, lipid profiles and psoriasis. Br J Dermatol 167(6):1279–1286
Kalkan G, Seçkin HY, Benli I et al (2019) Association of paraoxonase 1 (PON1) L55M and PON1 Q192R gene polymorphisms and risk of psoriasis. Giornale Italan Dermatol Venereol 154(3):321–326
Rangel-Villalobos H, Muñoz-Valle J, González-Martín A, Gorostiza A, Magaña M, Páez-Riberos L (2008) Genetic admixture, relatedness, and structure patterns among Mexican populations revealed by the Y-chromosome. Am J Phys Anthropol 135(4):448–461
Castelli W (1984) Epidemiology of coronary heart disease: the Framingham study. Am J Med 76(2):4–12
Gamboa R, Regalado JC, Huesca-Gómez C et al (2008) Actividades paraoxonasa y arilesterasa bajas en sujetos mexicanos con enfermedad arterial coronaria. Arch Cardiol Méx 78(4):360–368
Miller S, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16(3):1215
Ergen A, Kılıcoglu O, Ozger H, Agachan B, Isbir T (2011) Paraoxonase 1 192 and 55 polymorphisms in osteosarcoma. Mol Biol Rep 38(6):4181–4184
Dursun A, Cicek S, Keni FM, Karakas-Celik S, Sezer T, Altinyazar CH (2014) The relation of PON1-L55M gene polymorphism and clinical manifestation of Behcet’s disease. Acta Biochim Pol 61(2):271–274
Yong Y, He L (2005) SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res 15(2):97
Langan SM, Seminara NM, Shin DB et al (2012) Prevalence of metabolic syndrome in patients with psoriasis: a population-based study in the United Kingdom. J Invest Dermatol 132(3):556–562
Ferretti G, Bacchetti T, Campanati A, Simonetti O, Liberati G, Offidani A (2012) Correlation between lipoprotein (a) and lipid peroxidation in psoriasis: role of the enzyme paraoxonase-1. Br J Dermatol 166(1):204–207
Solak Tekin N, Tekin IO, Barut F, Yilmaz Sipahi E (2007) Accumulation of oxidized low-density lipoprotein in psoriatic skin and changes of plasma lipid levels in psoriatic patients. Mediators Inflamm. https://doi.org/10.1155/2007/78454
Gate L, Paul J, Ba GN, Tew K, Tapiero H (1999) Oxidative stress induced in pathologies: the role of antioxidants. Biomed Pharmacother 53(4):169–180
Detection NCEPEPo, Adults ToHBCi, Program NCE (1993) Second report of the expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel II). National Cholesterol Education Program, National Institute of Health
Owczarczyk-Saczonek AB, Nowicki RJ (2015) Prevalence of cardiovascular disease risk factors, and metabolic syndrome and its components in patients with psoriasis aged 30 to 49 years. Adv Dermatol Allergol 32(4):290
McElveen J, Mackness M, Colley C, Peard T, Warner S, Walker C (1986) Distribution of paraoxon hydrolytic activity in the serum of patients after myocardial infarction. Clin Chem 32(4):671–673
Tang WW, Hartiala J, Fan Y et al (2012) Clinical and genetic association of serum paraoxonase and arylesterase activities with cardiovascular risk. Arterioscler Thromb Vasc Biol 32(11):2803–2812
Gaál K, Tarr T, Lőrincz H et al (2016) High-density lipopoprotein antioxidant capacity, subpopulation distribution and paraoxonase-1 activity in patients with systemic lupus erythematosus. Lipids Health Dis 15(1):60
Husni ME, Wilson Tang W, Lucke M, Chandrasekharan U, Brennan DM, Hazen SL (2018) Correlation of high-density lipoprotein-associated paraoxonase 1 activity with systemic inflammation, disease activity, and cardiovascular risk factors in psoriatic disease. Arthrit Rheumatol 70(8):1240–1250
Shih DM, Lusis AJ (2009) The roles of PON1 and PON2 in cardiovascular disease and innate immunity. Curr Opin Lipidol. https://doi.org/10.1097/MOL.0b013e32832ca1ee
Fuhrman B, Volkova N, Aviram M (2005) Paraoxonase 1 (PON1) is present in postprandial chylomicrons. Atherosclerosis 180(1):55–61
Deakin S, Moren X, James RW (2005) Very low density lipoproteins provide a vector for secretion of paraoxonase-1 from cells. Atherosclerosis 179(1):17–25
Otocka-Kmiecik A, Orlowska-Majdak M (2009) The role of genetic (PON1 polymorphism) and environmental factors, especially physical activity, in antioxidant function of paraoxonase. Postepy Hig Med Dosw 63:668–677
Wadhwa D, Mahajan VK, Mehta KS et al (2019) Malondialdehyde, lipoprotein-a, lipoprotein ratios, comprehensive lipid tetrad index and atherogenic index as surrogate markers for cardiovascular disease in patients with psoriasis: a case–control study. Arch Dermatol Res 311(4):287–297
Qujeq D, Mahrooz A, Alizadeh A, Masoumi P, Annemohammadzadeh S, Boorank R (2018) Genotype and phenotype of salt-stimulated paraoxonase 1 (PON1) is associated with atherogenic indices in type 2 diabetes. J Diabet Metabol Disord 17(1):1–10
Jarvik GP, Rozek LS, Brophy VH et al (2000) Paraoxonase (PON1) phenotype is a better predictor of vascular disease than is PON1 192 or PON1 55 genotype. Arterioscler Thromb Vasc Biol 20(11):2441–2447
Mackness B, Davies GK, Turkie W et al (2001) Paraoxonase status in coronary heart disease: are activity and concentration more important than genotype? Arterioscler Thromb Vasc Biol 21(9):1451–1457
Fridman O, Gariglio L, Riviere S, Porcile R, Fuchs A, Potenzoni M (2016) Paraoxonase 1 gene polymorphisms and enzyme activities in coronary artery disease and its relationship to serum lipids and glycemia. Arch Cardiol Mex 86(4):350–357
Aviram M, Hardak E, Vaya J et al (2000) Human serum paraoxonases (PON1) Q and R selectively decrease lipid peroxides in human coronary and carotid atherosclerotic lesions: PON1 esterase and peroxidase-like activities. Circulation 101(21):2510–2517
Flekač M, Škrha J, Zidkova K, Lacinova Z, Hilgertova J (2008) Paraoxonase 1 gene polymorphisms and enzyme activities in diabetes mellitus. Physiol Res 57(5):717–726
Garin M, James RW, Dussoix P et al (1997) 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 Investig 99(1):62–66
Esparragón FR, Trujillo YH, Reyes AM, Ortega EH, Medina A, Pérez JCR (2006) Sobre los genes paraoxonasa-1 y SR-B1, y su importancia en la aterosclerosis. Rev Españ Cardiol 59(2):154–164
Mackness B, Mackness MI, Arrol S, Turkie W, Durrington PN (1997) Effect of the molecular polymorphisms of human paraoxonase (PON1) on the rate of hydrolysis of paraoxon. Br J Pharmacol 122(2):265
Christophers E (2007) Comorbidities in psoriasis. Clin Dermatol 25(6):529–534
Acknowledgments
We would like to acknowledge the students in our lab that collaborated in the process, especially Karla Elizabeth Díaz de León Romero, Felipe de Jesús Tachiquin Alvarez, Saúl Ceja Reyes and Néstor Oswaldo Alvarado López, who assisted the different parts of the methods. We recognize the work and help provided by Francisco Arturo Miranda-Gomez, Teresa Valencia Ponce and Maria Isabel Medina-Ortega who collected the samples for our study.
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AAH-C: Conceptualization, Investigation, Data curation and Writing-Original draft preparation. OP-M, VL-O and VD-R: Methodology, Resources and Validation. JFM-V: Writing-Original draft preparation and Resources. EM-L, MF-M: Methodology and Resources. DGV-Q: Methodology and Resource. CD-D: Writing-Original draft preparation. AA-N: Conceptualization, Visualization, Formal analysis, resource, Supervision, Methodology, Writing-Original draft preparation, Project administration. She is responsible of writing review and editing the document.
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Hernández-Collazo, A.A., Pérez-Méndez, O., López-Olmos, V. et al. Association between rs662 (A > G) and rs854560 (A > T) polymorphisms in PON1 gene and the susceptibility for psoriasis in mestizo population of Western Mexico. Mol Biol Rep 48, 183–194 (2021). https://doi.org/10.1007/s11033-020-06031-z
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DOI: https://doi.org/10.1007/s11033-020-06031-z