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Evaluation of Delta-Aminolevulinic Dehydratase Activity, Oxidative Stress Biomarkers, and Vitamin D Levels in Patients with Multiple Sclerosis

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Abstract

Multiple sclerosis (MS) is an autoimmune neurological disorder of unknown etiology. Oxidative stress and alterations in vitamin D levels have been implicated in the pathophysiology of MS. The aim of this study was to investigate δ-aminolevulinate dehydratase (δ-ALA-D) activity as well as the levels of vitamin D, lipid peroxidation levels, carbonyl protein content, DNA damage, superoxide dismutase (SOD) and catalase (CAT) activities, and the vitamin C, vitamin E, and non-protein thiol (NPSH) content in samples from patients with the relapsing-remitting form of MS (RRMS). The study population consisted of 29 RRMS patients and 29 healthy subjects. Twelve milliliters of blood was obtained from each individual and used for biochemical determinations. The results showed that δ-ALA-D and CAT activities were significantly increased, while SOD activity was decreased in the whole blood of RRMS patients compared to the control group (P < 0.05). In addition, we observed a significant increase in lipid peroxidation, carbonyl protein levels in serum and damaged DNA in leucocytes in RRMS patients compared with the control group (P < 0.05). Nonetheless, the levels of vitamin C, vitamin E, NPSH, and vitamin D were significantly decreased in RRMS patients in relation to the healthy individuals (P < 0.05). In conclusion, our results suggested that the increase in δ-ALA-D activity may be related to the inflammatory and immune process in MS in an attempt to maintain the cellular metabolism and reduce oxidative stress. Moreover, the alterations in the oxidant/antioxidant balance and lower vitamin D levels may contribute to the pathophysiology of MS.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  • Allen AC, Kelly S, Basdeo SA, Kinsella K, Mulready KJ, Mills KH, Tubridy N, Walsh C, Brady JJ, Hutchinson M, Fletcher JM (2012) A pilot study of the immunological effects of high-dose vitamin D in healthy volunteers. Mult Scler 18:1797–1800

    Article  PubMed  Google Scholar 

  • Ascherio A, Munger KL, Lünemann JD (2012) The initiation and prevention of multiple sclerosis. Nat Rev Neurol 8:602–612

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Benhusein GM, Mutch E, Aburawi S, Williams FM (2010) Genotoxic effect induced by hydrogen peroxide in human hepatoma cells using comet assay. Libyan J Med 5:1–6

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Correale J, Ysrraelit MC, Gaitán MI (2009) Immunomodulatory effects of vitamin D in multiple sclerosis. Brain 132:1146–1160

    Article  PubMed  Google Scholar 

  • Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A (2003) Protein carbonylation in human diseases. Trends Mol Med 9:169–176

    Article  PubMed  CAS  Google Scholar 

  • Djordjević VB, Zvezdanović L, Cosić V (2008) Oxidative stress in human diseases. Srp Arh Celok Lek 136:158–165

    Article  PubMed  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  PubMed  CAS  Google Scholar 

  • Fialkow L, Wang Y, Downey GP (2007) Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 42:153–164

    Article  PubMed  CAS  Google Scholar 

  • Friese MA, Schattling B, Fugger L (2014) Mechanisms of neurodegeneration and axonal in multiple sclerosis. Nat Rev Neurol 10:225–238

    Article  PubMed  CAS  Google Scholar 

  • Gianforcaro A, Hamadeh MJ (2014) Vitamin D as a potential therapy in amyotrophic lateral sclerosis. CNS Neurosci Ther 20:101–111

    Article  PubMed  CAS  Google Scholar 

  • Gilgun-Sherki Y, Melamed E, Offen D (2004) The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J Neurol 251:261–268

    Article  PubMed  CAS  Google Scholar 

  • Gonsette RE (2008) Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J Neurol Sci 274:48–53

    Article  PubMed  CAS  Google Scholar 

  • Gonzalo H, Brieva L, Tatzber F, Jové M, Cacabelos D, Cassanyé A, Lanau-Angulo L, Boada J, Serrano JC, González C, Hernández L, Peralta S, Pamplona R, Portero-Otin M (2012) Lipidome analysis in multiple sclerosis reveals protein lipoxidative damage as a potential pathogenic mechanism. J Neurochem 123:622–634

    Article  PubMed  CAS  Google Scholar 

  • Grecchi S, Mazzini G, Lisa A, Armentero MT, Bergamaschi R, Romani A, Blandini F, Di Perri C, Scovassi AI (2012) Search for cellular stress biomarkers in lymphocytes from patients with multiple sclerosis: a pilot study. PLoS One 7:e44935

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gröber U, Spitz J, Reichrath J, Kisters K, Holick MF (2013) Vitamin D: update 2013: from rickets prophylaxis to general preventive healthcare. Dermatoendocrinol 5:331–347

    Article  PubMed  PubMed Central  Google Scholar 

  • Haider L, Fischer MT, Frischer JM, Bauer J, Ho¨ftberger R, Botond G, Esterbauer H, Binder CJ, Witztum JL, Lassmann H (2011) Oxidative damage in multiple sclerosis lesions. Brain 134:1914–1924

    Article  PubMed  PubMed Central  Google Scholar 

  • Halliwell B (2012) Free radicals and antioxidants: updating a personal view. Nutr Rev 70:257–265

    Article  PubMed  Google Scholar 

  • Han X, Zhou DB, Xu CM, Yang Y, Duan MH, Wang X, Zhang JP, Zhao YQ, Shen T, Wu YJ (2011) Effect of erythropoietin on proinflammatory factors of human monocytes and its mechanisms. Zhongguo Shi Yan Xue Ye Xue Za Zhi 19(3):738–743

    PubMed  CAS  Google Scholar 

  • Hansen LG, Warwick WJ (1969) A fluorometric micromethod for serum vitamins A and E. Tech Bull Regist Med Technol 39:70–73

    PubMed  CAS  Google Scholar 

  • Hanwell HEC, Banwell B (2011) Assessment of evidence for a protective role of vitamin D in multiple sclerosis. Biochim Biophys Acta 1812:202–212

    Article  PubMed  CAS  Google Scholar 

  • Hartmann A, Agurell E, Beevers C, Brendler-Schwaab S, Burlinson B, Clay P, Collins A, Smith A, Speit G, Thybaud V, Tice RR (2003) Recommendations for conducting the in vivo alkaline Comet assay. Mutagenesis 18:45–51

    Article  PubMed  CAS  Google Scholar 

  • Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH, Weaver CM (2011) Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 96:1911–1930

    Article  PubMed  CAS  Google Scholar 

  • Jacques-Silva MC, Nogueira CW, Broch LC, Flores EM, Rocha JB (2001) Diphenyl diselenide and ascorbic acid changes deposition of selenium and ascorbic acid in liver and brain of mice. Pharmacol Toxicol 88:119–125

    Article  PubMed  CAS  Google Scholar 

  • Jentzsch AM, Bachmann H, Fürst P, Biesalski HK (1996) Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med 20:251–256

    Article  PubMed  CAS  Google Scholar 

  • Johansson SV, Strandberg PO (1972) Haem biosynthesis studied in patients with rheumatoid arthritis. J Clin Pathol 25:159–162

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson F, Giulivi C (2005) Superoxide dismutases and their impact upon human health. Mol Aspects Med 26:340–352

    Article  PubMed  CAS  Google Scholar 

  • Kang Z, Zhang J, Zhou J, Qi Q, Du G, Chen J (2012) Recent advances in microbial production of δ-aminolevulinic acid and vitamin B12. Biotechnol Adv 30:1533–1542

    Article  PubMed  CAS  Google Scholar 

  • Koch M, Ramsaransing GS, Arutjunyan AV, Stepanov M, Teelken A, Heersema DJ, De Keyser J (2006) Oxidative stress in serum and peripheral blood leukocytes in patients with different disease courses of multiple sclerosis. J Neurol 253:483–487

    Article  PubMed  CAS  Google Scholar 

  • Kopff M, Zakrzewska I, Czernicki J, Klem J, Strzelczyk M (1993) Red cell superoxide dismutase and catalase activity in multiple sclerosis. Acta Biochim Pol 40:154–157

    PubMed  CAS  Google Scholar 

  • Lassmann H, van Horssen J (2011) The molecular basis of neurodegeneration in multiple sclerosis. FEBS Lett 585:3715–3723

    Article  PubMed  CAS  Google Scholar 

  • Lee DH, Gold R, Linker RA (2012) Mechanisms of oxidative damage in multiple sclerosis and neurodegenerative diseases: therapeutic modulation via fumaric acid esters. Int J Mol Sci 13:11783–11803

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  PubMed  CAS  Google Scholar 

  • Li-Weber M, Weigand MA, Giaisi M, Süss D, Treiber MK, Baumann S, Ritsou E, Breitkreutz R, Krammer PH (2002) Vitamin E inhibits CD95 ligand expression and protects T cells from activation-induced cell death. J Clin Invest 110:681–690

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ljubisavljevic S, Stojanovic I, Vojinovic S, Stojanov D, Stojanovic S, Kocic G, Savic D, Cvetkovic T, Pavlovic D (2013) Cerebrospinal fluid and plasma oxidative stress biomarkers in different clinical phenotypes of neuroinflammatory acute attacks. Conceptual accession: from fundamental to clinic. Cell Mol Neurobiol 33:767–777

    Article  PubMed  CAS  Google Scholar 

  • Ljubisavljevic S, Stojanovic I, Cvetkovic T, Vojinovic S, Stojanov D, Stojanovic D, Stefanovic N, Pavlovic D (2014) Erythrocytes’ antioxidative capacity as a potential marker of oxidative stress intensity in neuroinflammation. J Neurol Sci 337:8–13

    Article  PubMed  CAS  Google Scholar 

  • Løken-Amsrud KI, Myhr KM, Bakke SJ, Beiske AG, Bjerve KS, Bjørnarå BT, Hovdal H, Lilleås F, Midgard R, Pedersen T, Benth JŠ, Torkildsen Ø, Wergeland S, Holmøy T (2013) Alpha-tocopherol and MRI outcomes in multiple sclerosis—association and prediction. PLoS One 8:e54417

    Article  PubMed  PubMed Central  Google Scholar 

  • Mao P, Reddy PH (2010) Is multiple sclerosis a mitochondrial disease? Biochim Biophys Acta 1802:66–79

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Matés JM, Sánchez-Jiménez F (1999) Antioxidant enzymes and their implications in pathophysiologic processes. Front Biosci 4:D339–D345

    Article  PubMed  Google Scholar 

  • Mazza M, Pomponi M, Janiri L, Bria P, Mazza S (2007) Omega-3 fatty acids and antioxidants in neurological and psychiatric diseases: an overview. Prog Neuropsychopharmacol Biol Psychiatry 31:12–26

    Article  PubMed  CAS  Google Scholar 

  • McCaddon A (2013) Vitamin B12 in neurology and ageing; clinical and genetic aspects. Biochimie 95:1066–1076

    Article  PubMed  CAS  Google Scholar 

  • McCord JM, Edeas MA (2005) SOD, oxidative stress and human pathologies: a brief history and a future vision. Biomed Pharmacother 59:139–142

    Article  PubMed  CAS  Google Scholar 

  • McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, Sandberg-Wollheim M, Sibley W, Thompson A, van den Noort S, Weinshenker BY, Wolinsky JS (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 50:121–127

    Article  PubMed  CAS  Google Scholar 

  • McKelvey-Martin VJ, Green MH, Schmezer P, Pool-Zobel BL, De Méo MP, Collins A (1993) The single cell gel electrophoresis assay (comet assay): a European review. Mutat Res 288:47–63

    Article  PubMed  CAS  Google Scholar 

  • Miller E, Mrowicka M, Malinowska K, Zołyński K, Kedziora J (2010) Effects of the whole-body cryotherapy on a total antioxidative status and activities of some antioxidative enzymes in blood of patients with multiple sclerosis-preliminary study. J Med Invest 57:168–173

    Article  PubMed  Google Scholar 

  • Miller E, Walczak A, Majsterek I, Kędziora J (2013) Melatonin reduces oxidative stress in the erythrocytes of multiple sclerosis patients with secondary progressive clinical course. J Neuroimmunol 257:97–101

    Article  PubMed  CAS  Google Scholar 

  • Mirshafiey A, Mohsenzadegan M (2009) Antioxidant therapy in multiple sclerosis. Immunopharmacol Immunotoxicol 31:13–29

    Article  PubMed  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    PubMed  CAS  Google Scholar 

  • Mitosek-Szewczyk K, Gordon-Krajcer W, Walendzik P, Stelmasiak Z (2010) Free radical peroxidation products in cerebrospinal fluid and serum of patients with multiple sclerosis after glucocorticoid therapy. Folia Neuropathol 48:116–122

    PubMed  CAS  Google Scholar 

  • Mora JR, Iwata M, von Andrian UH (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 8:685–698

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Morelli A, Ravera S, Calzia D, Panfoli I (2012) Impairment of heme synthesis in myelin as potential trigger of multiple sclerosis. Med Hypotheses 78:707–710

    Article  PubMed  CAS  Google Scholar 

  • Munger KL, Zhang SM, O’Reilly E, Hernán MA, Olek MJ, Willett WC, Ascherio A (2004) Vitamin D intake and incidence of multiple sclerosis. Neurology 62:60–65

    Article  PubMed  CAS  Google Scholar 

  • Nadin SB, Vargas-Roig LM, Ciocca DR (2001) A silver staining method for single-cell gel assay. J Histochem Cytochem 49:1183–1186

    Article  PubMed  CAS  Google Scholar 

  • Ortiz GG, Pacheco-Moisés FP, Bitzer-Quintero OK, Ramírez-Anguiano AC, Flores-Alvarado LJ, Ramírez-Ramírez V, Macias-Islas MA, Torres-Sánchez ED (2013) Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clin Dev Immunol 2013:708659

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozgocmen S, Bulut S, Ilhan N, Gulkesen A, Ardicoglu O, Ozkan Y (2005) Vitamin D deficiency and reduced bone mineral density in multiple sclerosis: effect of ambulatory status and functional capacity. J Bone Miner Metab 23:309–313

    Article  PubMed  Google Scholar 

  • Padh H (2005) Vitamin C: newer insights into its biochemical functions. Cell Mol Biol Lett 10:255–264

    Google Scholar 

  • Paniz C, Bairros A, Valentini J, Charão M, Bulcão R, Moro A, Grune T, Garcia SC (2007) The influence of the serum vitamin C levels on oxidative stress biomarkers in elderly women. Clin Biochem 40:1367–1372

    Article  PubMed  CAS  Google Scholar 

  • Pasquali L, Pecori C, Lucchesi C, LoGerfo A, Iudice A, Siciliano G, Bonuccelli U (2015) Plasmatic oxidative stress biomarkers in multiple sclerosis: relation with clinical and demographic characteristics. Clin Biochem 48:19–23

    Article  PubMed  CAS  Google Scholar 

  • Pekmezci D (2011) Vitamin E and Immunity. Vitam Horm 86:179–215

    Article  PubMed  CAS  Google Scholar 

  • Pierrot-Deseilligny C, Souberbielle JC (2013) Contribution of vitamin D insufficiency to the pathogenesis of multiple sclerosis. Ther Adv Neurol Disord 6:81–116

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Polachini CR, Spanevello RM, Casali EA, Zanini D, Pereira LB, Martins CC, Baldissareli J, Cardoso AM, Duarte MF, da Costa P, Prado AL, Schetinger MR, Morsch VM (2014) Alterations in the cholinesterase and adenosine deaminase activities and inflammation biomarker levels in patients with multiple sclerosis. Neuroscience 266:266–274

    Article  PubMed  CAS  Google Scholar 

  • Ramagopalan SV, Maugeri NJ, Handunnetthi L, Lincoln MR, Orton SM, Dyment DA, Deluca GC, Herrera BM, Chao MJ, Sadovnick AD, Ebers GC, Knight JC (2009) Expression of the multiple sclerosis associated MHC class II Allele HLA-DRB1*1501 is regulated by vitamin D. PLoS Genet 5:e1000369

    Article  PubMed  PubMed Central  Google Scholar 

  • Ransohoff RM, Hafler DA, Lucchinetti CF (2015) Multiple sclerosis-a quiet revolution. Nat Rev Neurol 11:134–142

    Article  PubMed  Google Scholar 

  • Reinhardt K, Weiss S, Rosenbauer J, Gartnera J, von Kries R (2014) Multiple sclerosis in children and adolescents: incidence and clinical picture—new insights from the nationwide German surveillance (2009–2011). Eur J Neurol 21:654–659

    Article  PubMed  CAS  Google Scholar 

  • Reynolds R, Roncaroli F, Nicholas R, Radotra B, Gveric D, Howell O (2011) The neuropathological basis of clinical progression in multiple sclerosis. Acta Neuropathol 122:155–170

    Article  PubMed  Google Scholar 

  • Ricciarelli R, Argellati F, Pronzato MA, Domenicotti C (2007) Vitamin E and neurodegenerative diseases. Mol Aspects Med 28:591–606

    Article  PubMed  CAS  Google Scholar 

  • Rocha ME, Dutra F, Bandy B, Baldini RL, Gomes SL, Faljoni-Alario A, Liria CW, Miranda MT, Bechara EJ (2003) Oxidative damage to ferritin by 5-aminolevulinic acid. Arch Biochem Biophys 409:349–365

    Article  PubMed  CAS  Google Scholar 

  • Rocha JBT, Saraiva RA, Garcia SC, Gravina FS, Nogueira CW (2012) Aminolevulinate dehydratase (δ-ALA-D) as marker protein of intoxication with metals and other pro-oxidant situations. Toxicol Res 1:85–102

    Article  CAS  Google Scholar 

  • Rommer PS, Greilberger J, Salhofer-Polanyi S, Auff E, Leutmezer F, Herwig R (2014) Elevated levels of carbonyl proteins in cerebrospinal fluid of patients with neurodegenerative diseases. Tohoku J Exp Med 234:313–317

    Article  PubMed  Google Scholar 

  • Sadowska-Bartosz I, Adamczyk-Sowa M, Galiniak S, Mucha S, Pierzchala K, Bartosz G (2013) Oxidative modification of serum proteins in multiple sclerosis. Neurochem Int 63:507–516

    Article  PubMed  CAS  Google Scholar 

  • Salemi G, Gueli MC, Vitale F, Battaglieri F, Guglielmini E, Ragonese P, Trentacosti A, Massenti MF, Savettieri G, Bono A (2010) Blood lipids, homocysteine, stress factors, and vitamins in clinically stable multiple sclerosis patients. Lipids Health Dis 9:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Sassa S (1982) Delta-aminolevulinic acid dehydratase assay. Enzyme 28:133–145

    PubMed  CAS  Google Scholar 

  • Sassa S (1998) ALAD porphyria. Semin Liver Dis 18:95–101

    Article  PubMed  CAS  Google Scholar 

  • Schmatz R, Perreira LB, Stefanello N, Mazzanti C, Spanevello R, Gutierres J, Bagatini M, Martins CC, Abdalla FH, da Silva Daci, Serres J, Zanini D, Vieira JM, Cardoso AM, Schetinger MR, Morsch VM (2012) Effects of resveratrol on biomarkers of oxidative stress and on the activity of delta aminolevulinic acid dehydratase in liver and kidney of streptozotocin-induced diabetic rats. Biochimie 94:374–383

    Article  PubMed  CAS  Google Scholar 

  • Simpson S Jr, Taylor B, Blizzard L, Ponsonby AL, Pittas F, Tremlett H, Dwyer T, Gies P, van der Mei I (2010) Higher 25-hydroxyvitamin D is associated with lower relapse risk in multiple sclerosis. Ann Neurol 68:193–203

    PubMed  CAS  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantification of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  PubMed  CAS  Google Scholar 

  • Smolders J, Menheere P, Kessels A, Damoiseaux J, Hupperts R (2008) Association of vitamin D metabolite levels with relapse rate and disability in multiple sclerosis. Mult Scler 14:1220–1224

    Article  PubMed  CAS  Google Scholar 

  • Souza JB, Rocha JB, Nogueira CW, Borges VC, Kaizer RR, Morsch VM, Dressler VL, Martins AF, Flores EM, Schetinger MR (2007) Delta-aminolevulinate dehydratase (δ-ALA-D) activity in diabetes and hypothyroidism. Clin Biochem 40:321–325

    Article  PubMed  CAS  Google Scholar 

  • Tavazzi B, Batocchi AP, Amorini AM, Nociti V, D’Urso S, Longo S, Gullotta S, Picardi M, Lazzarino G (2011) Serum metabolic profile in multiple sclerosis patients. Mult Scler Int 2011:167156

    PubMed  PubMed Central  Google Scholar 

  • Trapp BD, Nave KA (2008) Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 31:247–269

    Article  PubMed  CAS  Google Scholar 

  • Valentini J, Grotto D, Paniz C, Roehrs M, Burg G, Garcia SC (2008) The influence of the hemodialysis treatment time under oxidative stress biomarkers in chronic renal failure patients. Biomed Pharmacother 62:378–382

    Article  PubMed  CAS  Google Scholar 

  • van Horssen J, Schreibelt G, Drexhage J, Hazes T, Dijkstra CD, van der Valk P, de Vries HE (2008) Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 45:1729–1737

    Article  PubMed  Google Scholar 

  • van Horssen J, Witte ME, Schreibelt G, Helga E, de Vries HE (2011) Radical changes in multiple sclerosis pathogenesis. Biochim Biophys Acta 1812:141–150

    Article  PubMed  Google Scholar 

  • Van Laer K, Hamilton CJ, Messens J (2013) Low-molecular-weight thiols in thiol-disulfide exchange. Antioxid Redox Signal 18:1642–1653

    Article  PubMed  Google Scholar 

  • Villacorta L, Azzi A, Zingg JM (2007) Regulatory role of vitamins E and C on extracellular matrix components of the vascular system. Mol Aspects Med 8:507–537

    Article  Google Scholar 

  • Wacker M, Holick MF (2013) Vitamin D effects on skeletal and extraskeletal health and the need for supplementation. Nutrients 5:111–148

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yousefi B, Ahmadi Y, Ghorbanihaghjo A, Faghfoori Z, Irannejad VS (2014) Serum arsenic and lipid peroxidation levels in patients with multiple sclerosis. Biol Trace Elem Res 158:276–279

    Article  PubMed  CAS  Google Scholar 

  • Zanini D, Pelinson LP, Schmatz R, Belmonte PL, Curry MC, Baldissareli J, Pires AG, Antunes SFA, Brenner RLG, Araújo MC, Chiesa J, Morsch VM, Bitencourt RLD, Schetinger MR (2014) δ-Aminolevulinate dehydratase activity in lung cancer patients and its relationship with oxidative stress. Biomed Pharmacother 68:603–609

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank the neurologist Juarez Lopes and the MS patients and healthy subjects that contributed to the realization of this study. We also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS), FAPERGS/PPSUS 1279-2551/13-7, Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Instituto Brasileiro de Neurociência (IBN-Net), INCT for Excitotoxicity and Neuroprotection, and the Federal University of Santa Maria, RS, Brazil for financial support.

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Correspondence to Carla Roberta Nunes Polachini or Vera Maria Morsch.

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This work is original and is not under consideration by another journal. All of the patients provided written consent, and the work was approved by the Human Ethical Committee from the Federal University of Santa Maria Hospital. Finally, this manuscript has been approved by all of the authors, and none of the authors have a conflict of interest.

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Polachini, C.R.N., Spanevello, R.M., Zanini, D. et al. Evaluation of Delta-Aminolevulinic Dehydratase Activity, Oxidative Stress Biomarkers, and Vitamin D Levels in Patients with Multiple Sclerosis. Neurotox Res 29, 230–242 (2016). https://doi.org/10.1007/s12640-015-9584-2

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