Reactive oxygen species in organ-specific autoimmunity

Autoimmunity Highlights

Volumn 7, Issue 1, 2016, Pages

  Di Dalmazi, Giulia ^a,b   Hirshberg, Jason ^c   Lyle, Daniel ^c   Freij, Joudeh B ^c   Caturegli, Patrizio ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHIETI   (Italy)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Autoimmunity; Hashimoto thyroiditis; Monoamine oxidase (MAO); Oxidative stress; Reactive oxygen species (ROS); Smoking

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING); NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; AUTOIMMUNITY; HASHIMOTO DISEASE; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; MULTIPLE SCLEROSIS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; RHEUMATOID ARTHRITIS; SMOKING; TISSUE INJURY; VITILIGO;

EID: 84982822232     PISSN: 20380305     EISSN: 20383274     Source Type: Journal    
DOI: 10.1007/s13317-016-0083-0     Document Type: Review

References (110)

1. Fenton HJJ (1894) Oxidation of tartaric acid in presence of iron. J Chem Soc 65:899–910
2. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11(3):298–300
3. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95. doi:10.1152/physrev.00018.2001
4. Poncin S, Van Eeckoudt S, Humblet K, Colin IM, Gerard AC (2010) Oxidative stress: a required condition for thyroid cell proliferation. Am J Pathol 176(3):1355–1363. doi:10.2353/ajpath.2010.090682
5. Wang X, Hai C (2016) Novel insights into redox system and the mechanism of redox regulation. Mol Biol Rep. doi:10.1007/s11033-016-4022-y
6. Jackson MJ (2016) Reactive oxygen species in sarcopenia: should we focus on excess oxidative damage or defective redox signalling? Mol Asp Med. doi:10.1016/j.mam.2016.05.002
7. Panieri E, Santoro MM (2016) ROS homeostasis and metabolism: a dangerous liason in cancer cells. Cell Death Dis 7(6):e2253. doi:10.1038/cddis.2016.105
8. Miller EW, Dickinson BC, Chang CJ (2010) Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci USA 107(36):15681–15686. doi:10.1073/pnas.1005776107
9. Hippeli S, Elstner EF (1999) Transition metal ion-catalyzed oxygen activation during pathogenic processes. FEBS Lett 443(1):1–7
10. Taniyama Y, Griendling KK (2003) Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42(6):1075–1081. doi:10.1161/01.hyp.0000100443.09293.4f
11. Karlenius TC, Tonissen KF (2010) Thioredoxin and cancer: a role for thioredoxin in all states of tumor oxygenation. Cancers 2(2):209–232. doi:10.3390/cancers2020209
12. Wang X, Tao L, Hai CX (2012) Redox-regulating role of insulin: the essence of insulin effect. Mol Cell Endocrinol 349(2):111–127. doi:10.1016/j.mce.2011.08.019
13. Li JM, Shah AM (2003) ROS generation by nonphagocytic NADPH oxidase: potential relevance in diabetic nephropathy. J Am Soc Nephrol JASN 14(8 Suppl 3):S221–S226
14. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88(1):287–332. doi:10.1152/physrev.00015.2007
15. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4):483–495. doi:10.1016/j.cell.2005.02.001
16. Hausenloy D, Wynne A, Duchen M, Yellon D (2004) Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 109(14):1714–1717. doi:10.1161/01.cir.0000126294.81407.7d
17. Pitkanen S, Robinson BH (1996) Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J Clin Investig 98(2):345–351. doi:10.1172/jci118798
18. Treberg JR, Quinlan CL, Brand MD (2011) Evidence for two sites of superoxide production by mitochondrial NADH-ubiquinone oxidoreductase (complex I). J Biol Chem 286(31):27103–27110. doi:10.1074/jbc.M111.252502
19. Paddenberg R, Ishaq B, Goldenberg A, Faulhammer P, Rose F, Weissmann N, Braun-Dullaeus RC, Kummer W (2003) Essential role of complex II of the respiratory chain in hypoxia-induced ROS generation in the pulmonary vasculature. Am J Physiol Lung Cell Mol Physiol 284(5):L710–L719. doi:10.1152/ajplung.00149.2002
20. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, Brand MD (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem 287(32):27255–27264. doi:10.1074/jbc.M112.374629
21. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122(2):221–233. doi:10.1016/j.cell.2005.05.011
22. Babior BM, Lambeth JD, Nauseef W (2002) The neutrophil NADPH oxidase. Arch Biochem Biophys 397(2):342–344. doi:10.1006/abbi.2001.2642
23. Lambeth JD, Cheng G, Arnold RS, Edens WA (2000) Novel homologs of gp91phox. Trends Biochem Sci 25(10):459–461
24. Zalba G, San Jose G, Moreno MU, Fortuno MA, Fortuno A, Beaumont FJ, Diez J (2001) Oxidative stress in arterial hypertension: role of NAD(P)H oxidase. Hypertension 38(6):1395–1399
25. Radeke HH, Cross AR, Hancock JT, Jones OT, Nakamura M, Kaever V, Resch K (1991) Functional expression of NADPH oxidase components (alpha- and beta-subunits of cytochrome b558 and 45-kDa flavoprotein) by intrinsic human glomerular mesangial cells. J Biol Chem 266(31):21025–21029
26. Jones SA, Hancock JT, Jones OT, Neubauer A, Topley N (1995) The expression of NADPH oxidase components in human glomerular mesangial cells: detection of protein and mRNA for p47phox, p67phox, and p22phox. J Am Soc Nephrol JASN 5(7):1483–1491
27. Griendling KK, Sorescu D, Ushio-Fukai M (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86(5):494–501
28. Brown DI, Griendling KK (2009) Nox proteins in signal transduction. Free Radic Biol Med 47(9):1239–1253. doi:10.1016/j.freeradbiomed.2009.07.023
29. Li WG, Miller FJ Jr, Zhang HJ, Spitz DR, Oberley LW, Weintraub NL (2001) H(2)O(2)-induced O(2) production by a non-phagocytic NAD(P)H oxidase causes oxidant injury. J Biol Chem 276(31):29251–29256. doi:10.1074/jbc.M102124200
30. Kovacic HN, Irani K, Goldschmidt-Clermont PJ (2001) Redox regulation of human Rac1 stability by the proteasome in human aortic endothelial cells. J Biol Chem 276(49):45856–45861. doi:10.1074/jbc.M107925200
31. Maejima Y, Kuroda J, Matsushima S, Ago T, Sadoshima J (2011) Regulation of myocardial growth and death by NADPH oxidase. J Mol Cell Cardiol 50(3):408–416. doi:10.1016/j.yjmcc.2010.12.018
32. Forstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33(7):829–837a-d. doi:10.1093/eurheartj/ehr304
33. Dimmeler S, Zeiher AM (2000) Reactive oxygen species and vascular cell apoptosis in response to angiotensin II and pro-atherosclerotic factors. Regul Pept 90(1–3):19–25
34. Rodriguez MJ, Saura J, Billett EE, Finch CC, Mahy N (2001) Cellular localization of monoamine oxidase A and B in human tissues outside of the central nervous system. Cell Tissue Res 304(2):215–220
35. Huang YH, Ito A, Arai R (2005) Immunohistochemical localization of monoamine oxidase type B in pancreatic islets of the rat. J Histochem Cytochem Off J Histochem Soc 53(9):1149–1158. doi:10.1369/jhc.5A6658.2005
36. Pizzinat N, Copin N, Vindis C, Parini A, Cambon C (1999) Reactive oxygen species production by monoamine oxidases in intact cells. Naunyn Schmiedeberg’s Arch Pharmacol 359(5):428–431
37. Kaludercic N, Carpi A, Menabo R, Di Lisa F, Paolocci N (2011) Monoamine oxidases (MAO) in the pathogenesis of heart failure and ischemia/reperfusion injury. Biochim Biophys Acta 1813(7):1323–1332. doi:10.1016/j.bbamcr.2010.09.010
38. Santin Y, Sicard P, Vigneron F, Guilbeau-Frugier C, Dutaur M, Lairez O, Couderc B, Manni D, Korolchuk VI, Lezoualc’h F, Parini A, Mialet-Perez J (2016) Oxidative stress by monoamine oxidase-a impairs transcription factor EB activation and autophagosome clearance, leading to cardiomyocyte necrosis and heart failure. Antioxid Redox Signal. doi:10.1089/ars.2015.6522
39. Benson CA, Wong G, Tenorio G, Baker GB, Kerr BJ (2013) The MAO inhibitor phenelzine can improve functional outcomes in mice with established clinical signs in experimental autoimmune encephalomyelitis (EAE). Behav Brain Res 252:302–311. doi:10.1016/j.bbr.2013.06.019
40. Namazi MR (2005) Phenytoin as a novel anti-vitiligo weapon. J Autoimmune Dis 2:11. doi:10.1186/1740-2557-2-11
41. Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82(2):291–295
42. Xie H, Zhou F, Liu L, Zhu G, Li Q, Li C, Gao T (2016) Vitiligo: how do oxidative stress-induced autoantigens trigger autoimmunity? J Dermatol Sci 81(1):3–9. doi:10.1016/j.jdermsci.2015.09.003
43. Salzano S, Checconi P, Hanschmann EM, Lillig CH, Bowler LD, Chan P, Vaudry D, Mengozzi M, Coppo L, Sacre S, Atkuri KR, Sahaf B, Herzenberg LA, Herzenberg LA, Mullen L, Ghezzi P (2014) Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal. Proc Natl Acad Sci USA 111(33):12157–12162. doi:10.1073/pnas.1401712111
44. Holmdahl R, Sareila O, Olsson LM, Backdahl L, Wing K (2016) Ncf1 polymorphism reveals oxidative regulation of autoimmune chronic inflammation. Immunol Rev 269(1):228–247. doi:10.1111/imr.12378
45. Ahsan H, Ali A, Ali R (2003) Oxygen free radicals and systemic autoimmunity. Clin Exp Immunol 131(3):398–404
46. Kienhofer D, Boeltz S, Hoffmann MH (2016) Reactive oxygen homeostasis—the balance for preventing autoimmunity. Lupus 25(8):943–954. doi:10.1177/0961203316640919
47. Kolypetri P, King J, Larijani M, Carayanniotis G (2015) Genes and environment as predisposing factors in autoimmunity: acceleration of spontaneous thyroiditis by dietary iodide in NOD. H2(h4) mice. Int Rev Immunol 34(6):542–556. doi:10.3109/08830185.2015.1065828
48. Braley-Mullen H, Yu S (2015) NOD.H-2h4 mice: an important and underutilized animal model of autoimmune thyroiditis and Sjogren’s syndrome. Adv Immunol 126:1–43. doi:10.1016/bs.ai.2014.11.001
49. Burek CL, Rose NR (2008) Autoimmune thyroiditis and ROS. Autoimmun Rev 7(7):530–537. doi:10.1016/j.autrev.2008.04.006
50. Sharma R, Traore K, Trush MA, Rose NR, Burek CL (2008) Intracellular adhesion molecule-1 up-regulation on thyrocytes by iodine of non-obese diabetic. H2(h4) mice is reactive oxygen species-dependent. Clin Exp Immunol 152(1):13–20. doi:10.1111/j.1365-2249.2008.03590.x
51. Kolypetri P, Carayanniotis G (2014) Apoptosis of NOD. H2 h4 thyrocytes by low concentrations of iodide is associated with impaired control of oxidative stress. Thyroid Off J Am Thyroid Assoc 24(7):1170–1178. doi:10.1089/thy.2013.0676
52. Duthoit C, Estienne V, Giraud A, Durand-Gorde JM, Rasmussen AK, Feldt-Rasmussen U, Carayon P, Ruf J (2001) Hydrogen peroxide-induced production of a 40 kDa immunoreactive thyroglobulin fragment in human thyroid cells: the onset of thyroid autoimmunity? Biochem J 360(Pt 3):557–562
53. Poncin S, Colin IM, Decallonne B, Clinckspooor I, Many MC, Denef JF, Gerard AC (2010) N-acetylcysteine and 15 deoxy-{delta}12,14-prostaglandin J2 exert a protective effect against autoimmune thyroid destruction in vivo but not against interleukin-1{alpha}/interferon {gamma}-induced inhibitory effects in thyrocytes in vitro. Am J Pathol 177(1):219–228. doi:10.2353/ajpath.2010.091253
54. Ates I, Yilmaz FM, Altay M, Yilmaz N, Berker D, Guler S (2015) The relationship between oxidative stress and autoimmunity in Hashimoto’s thyroiditis. Eur J Endocrinol Eur Fed Endocr Soc 173(6):791–799. doi:10.1530/eje-15-0617
55. Baser H, Can U, Baser S, Yerlikaya FH, Aslan U, Hidayetoglu BT (2015) Assesment of oxidative status and its association with thyroid autoantibodies in patients with euthyroid autoimmune thyroiditis. Endocrine 48(3):916–923. doi:10.1007/s12020-014-0399-3
56. Ruggeri RM, Vicchio TM, Cristani M, Certo R, Caccamo D, Alibrandi A, Giovinazzo S, Saija A, Campenni A, Trimarchi F, Gangemi S (2016) Oxidative stress and advanced glycation end products in hashimoto’s thyroiditis. Thyroid Off J Am Thyroid Assoc 26(4):504–511. doi:10.1089/thy.2015.0592
57. Zhu H, Li YR (2012) Oxidative stress and redox signaling mechanisms of inflammatory bowel disease: updated experimental and clinical evidence. Exp Biol Med (Maywood, NJ) 237(5):474–480. doi:10.1258/ebm.2011.011358
58. Graff LA, Walker JR, Bernstein CN (2009) Depression and anxiety in inflammatory bowel disease: a review of comorbidity and management. Inflamm Bowel Dis 15(7):1105–1118. doi:10.1002/ibd.20873
59. Mikocka-Walus AA, Turnbull DA, Moulding NT, Wilson IG, Andrews JM, Holtmann GJ (2006) Antidepressants and inflammatory bowel disease: a systematic review. Clin Pract Epidemiol Ment Health CP EMH 2:24. doi:10.1186/1745-0179-2-24
60. Kast RE (1998) Crohn’s disease remission with phenelzine treatment. Gastroenterology 115(4):1034–1035
61. Magro F, Vieira-Coelho MA, Fraga S, Serrao MP, Veloso FT, Ribeiro T, Soares-da-Silva P (2002) Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci 47(1):216–224
62. 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(3):261–268. doi:10.1007/s00415-004-0348-9
63. Oliveira SR, Kallaur AP, Reiche EM, Kaimen-Maciel DR, Panis C, Lozovoy MA, Morimoto HK, Maes M, Dichi I, Simao AN (2016) Albumin and protein oxidation are predictors that differentiate relapsing-remitting from progressive clinical forms of multiple sclerosis. Mol Neurobiol. doi:10.1007/s12035-016-9860-z
64. Gonsette RE (2008) Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J Neurol Sci 274(1–2):48–53. doi:10.1016/j.jns.2008.06.029
65. Ortiz GG, Pacheco-Moises FP, Bitzer-Quintero OK, Ramirez-Anguiano AC, Flores-Alvarado LJ, Ramirez-Ramirez V, Macias-Islas MA, Torres-Sanchez ED (2013) Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clin Dev Immunol 2013:708659. doi:10.1155/2013/708659
66. Fiorini A, Koudriavtseva T, Bucaj E, Coccia R, Foppoli C, Giorgi A, Schinina ME, Di Domenico F, De Marco F, Perluigi M (2013) Involvement of oxidative stress in occurrence of relapses in multiple sclerosis: the spectrum of oxidatively modified serum proteins detected by proteomics and redox proteomics analysis. PLoS One 8(6):e65184. doi:10.1371/journal.pone.0065184
67. Fischer MT, Sharma R, Lim JL, Haider L, Frischer JM, Drexhage J, Mahad D, Bradl M, van Horssen J, Lassmann H (2012) NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain J Neurol 135(Pt 3):886–899. doi:10.1093/brain/aws012
68. 2) accumulation in the epidermis of patients with vitiligo and its successful removal by a UVB-activated pseudocatalase. J Investig Dermatol Symp Proc Soc Investig Dermatol Inc Eur Soc Dermatol Res 4(1):91–96
69. Hann SK, Chang JH, Lee HS, Kim SM (2000) The classification of segmental vitiligo on the face. Yonsei Med J 41(2):209–212. doi:10.3349/ymj.2000.41.2.209
70. Schallreuter KU, Wood JM, Ziegler I, Lemke KR, Pittelkow MR, Lindsey NJ, Gutlich M (1994) Defective tetrahydrobiopterin and catecholamine biosynthesis in the depigmentation disorder vitiligo. Biochim Biophys Acta 1226(2):181–192
71. Schallreuter KU, Wood JM, Pittelkow MR, Buttner G, Swanson N, Korner C, Ehrke C (1996) Increased monoamine oxidase A activity in the epidermis of patients with vitiligo. Arch Dermatol Res 288(1):14–18
72. Laddha NC, Dwivedi M, Mansuri MS, Singh M, Gani AR, Yeola AP, Panchal VN, Khan F, Dave DJ, Patel A, Madhavan SE, Gupta R, Marfatia Z, Marfatia YS, Begum R (2014) Role of oxidative stress and autoimmunity in onset and progression of vitiligo. Exp Dermatol 23(5):352–353. doi:10.1111/exd.12372
73. Schallreuter KU, Wood JM, Berger J (1991) Low catalase levels in the epidermis of patients with vitiligo. J Invest Dermatol 97(6):1081–1085
74. Sravani PV, Babu NK, Gopal KV, Rao GR, Rao AR, Moorthy B, Rao TR (2009) Determination of oxidative stress in vitiligo by measuring superoxide dismutase and catalase levels in vitiliginous and non-vitiliginous skin. Indian J Dermatol Venereol Leprol 75(3):268–271. doi:10.4103/0378-6323.48427
75. Farahi-Jahromy A, Fallahzadeh MK, Ashkani-Esfahani S, Hamidizadeh N, Ghavipisheh M, Namazi MR (2014) Decreased glucose-6-phosphate dehydrogenase levels in vitiligo patients: further evidence of oxidative stress. Adv Biomed Res 3:34. doi:10.4103/2277-9175.124686
76. Jian Z, Li K, Liu L, Zhang Y, Zhou Z, Li C, Gao T (2011) Heme oxygenase-1 protects human melanocytes from H2O2-induced oxidative stress via the Nrf2-ARE pathway. J Invest Dermatol 131(7):1420–1427. doi:10.1038/jid.2011.56
77. Domej W, Oettl K, Renner W (2014) Oxidative stress and free radicals in COPD–implications and relevance for treatment. Int J Chronic Obstr Pulm Dis 9:1207–1224. doi:10.2147/copd.s51226
78. Hitchon CA, El-Gabalawy HS (2004) Oxidation in rheumatoid arthritis. Arthritis Res Ther 6(6):265–278. doi:10.1186/ar1447
79. Staron A, Makosa G, Koter-Michalak M (2012) Oxidative stress in erythrocytes from patients with rheumatoid arthritis. Rheumatol Int 32(2):331–334. doi:10.1007/s00296-010-1611-2
80. Mapp PI, Grootveld MC, Blake DR (1995) Hypoxia, oxidative stress and rheumatoid arthritis. Br Med Bull 51(2):419–436
81. Newkirk MM, Goldbach-Mansky R, Lee J, Hoxworth J, McCoy A, Yarboro C, Klippel J, El-Gabalawy HS (2003) Advanced glycation end-product (AGE)-damaged IgG and IgM autoantibodies to IgG-AGE in patients with early synovitis. Arthritis Res Ther 5(2):R82–R90
82. Ostrakhovitch EA, Afanas’ev IB (2001) Oxidative stress in rheumatoid arthritis leukocytes: suppression by rutin and other antioxidants and chelators. Biochem Pharmacol 62(6):743–746
83. Davies MJ, Hawkins CL, Pattison DI, Rees MD (2008) Mammalian heme peroxidases: from molecular mechanisms to health implications. Antioxid Redox Signal 10(7):1199–1234. doi:10.1089/ars.2007.1927
84. Cacciapaglia F, Anelli MG, Rizzo D, Morelli E, Scioscia C, Mazzotta D, Iannone F, Lapadula G (2015) Influence of TNF-alpha inhibition on oxidative stress of rheumatoid arthritis patients. Reumatismo 67(3):97–102. doi:10.4081/reumatismo.2015.829
85. Jia Z, He J (2016) Paeoniflorin ameliorates rheumatoid arthritis in rat models through oxidative stress, inflammation and cyclooxygenase 2. Exp Ther Med 11(2):655–659. doi:10.3892/etm.2015.2908
86. Umar S, Zargan J, Umar K, Ahmad S, Katiyar CK, Khan HA (2012) Modulation of the oxidative stress and inflammatory cytokine response by thymoquinone in the collagen induced arthritis in Wistar rats. Chem Biol Interact 197(1):40–46. doi:10.1016/j.cbi.2012.03.003
87. van der Toorn M, Rezayat D, Kauffman HF, Bakker SJ, Gans RO, Koeter GH, Choi AM, van Oosterhout AJ, Slebos DJ (2009) Lipid-soluble components in cigarette smoke induce mitochondrial production of reactive oxygen species in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 297(1):L109–L114. doi:10.1152/ajplung.90461.2008
88. MacNee W (2001) Oxidative stress and lung inflammation in airways disease. Eur J Pharmacol 429(1–3):195–207
89. Repine JE, Bast A, Lankhorst I (1997) Oxidative stress in chronic obstructive pulmonary disease. Oxidative Stress Study Group. Am J Respir Crit Care Med 156(2 Pt 1):341–357. doi:10.1164/ajrccm.156.2.9611013
90. Florou AN, Gkiozos IC, Tsagouli SK, Souliotis KN, Syrigos KN (2014) Clinical significance of smoking cessation in subjects with cancer: a 30-year review. Respir Care 59(12):1924–1936. doi:10.4187/respcare.02559
91. Sasco AJ, Secretan MB, Straif K (2004) Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer (Amsterdam, Netherlands) 45(Suppl 2):S3–S9. doi:10.1016/j.lungcan.2004.07.998
92. Boyko EJ, Perera DR, Koepsell TD, Keane EM, Inui TS (1988) Effects of cigarette smoking on the clinical course of ulcerative colitis. Scand J Gastroenterol 23(9):1147–1152
93. Calabrese E, Yanai H, Shuster D, Rubin DT, Hanauer SB (2012) Low-dose smoking resumption in ex-smokers with refractory ulcerative colitis. J Crohn’s Colitis 6(7):756–762. doi:10.1016/j.crohns.2011.12.010
94. Fraga XF, Vergara M, Medina C, Casellas F, Bermejo B, Malagelada JR (1997) Effects of smoking on the presentation and clinical course of inflammatory bowel disease. Eur J Gastroenterol Hepatol 9(7):683–687
95. Mokbel M, Carbonnel F, Beaugerie L, Gendre JP, Cosnes J (1998) Effect of smoking on the long-term course of ulcerative colitis. Gastroenterol Clin Biol 22(11):858–862
96. Schmeltz LR, Blevins TC, Aronoff SL, Ozer K, Leffert JD, Goldberg MA, Horowitz BS, Bertenshaw RH, Troya P, Cohen AE, Lanier RK, Ct Wright (2014) Anatabine supplementation decreases thyroglobulin antibodies in patients with chronic lymphocytic autoimmune (Hashimoto’s) thyroiditis: a randomized controlled clinical trial. J Clin Endocrinol Metab 99(1):E137–E142. doi:10.1210/jc.2013-2951
97. Dorn HF (1959) Tobacco consumption and mortality from cancer and other diseases. Public Health Rep 74(7):581–593
98. Thiriez C, Villafane G, Grapin F, Fenelon G, Remy P, Cesaro P (2011) Can nicotine be used medicinally in Parkinson’s disease? Expert Rev Clin Pharmacol 4(4):429–436. doi:10.1586/ecp.11.27
99. Shao D, Oka S, Brady CD, Haendeler J, Eaton P, Sadoshima J (2012) Redox modification of cell signaling in the cardiovascular system. J Mol Cell Cardiol 52(3):550–558. doi:10.1016/j.yjmcc.2011.09.009
100. Perricone C, Versini M, Ben-Ami D, Gertel S, Watad A, Segel MJ, Ceccarelli F, Conti F, Cantarini L, Bogdanos DP, Antonelli A, Amital H, Valesini G, Shoenfeld Y (2016) Smoke and autoimmunity: the fire behind the disease. Autoimmun Rev 15(4):354–374. doi:10.1016/j.autrev.2016.01.001
101. Tsai CC, Cheng CY, Liu CY, Kao SC, Kau HC, Hsu WM, Wei YH (2009) Oxidative stress in patients with Graves’ ophthalmopathy: relationship between oxidative DNA damage and clinical evolution. Eye (London, England) 23(8):1725–1730. doi:10.1038/eye.2008.310
102. Cao C, Lai T, Li M, Zhou H, Lv D, Deng Z, Ying S, Chen Z, Li W, Shen H (2016) Smoking-promoted oxidative DNA damage response is highly correlated to lung carcinogenesis. Oncotarget. doi:10.18632/oncotarget.7810
103. Steinmaus C, Miller MD, Howd R (2007) Impact of smoking and thiocyanate on perchlorate and thyroid hormone associations in the 2001–2002 national health and nutrition examination survey. Environ Health Perspect 115(9):1333–1338. doi:10.1289/ehp.10300
104. Pathak KV, Bellamri M, Wang Y, Langouet S, Turesky RJ (2015) 2-Amino-9H-pyrido[2,3-b]indole (AalphaC) adducts and thiol oxidation of serum albumin as potential biomarkers of tobacco smoke. J Biol Chem 290(26):16304–16318. doi:10.1074/jbc.M115.646539
105. Fowler JS, Volkow ND, Wang GJ, Pappas N, Logan J, Shea C, Alexoff D, MacGregor RR, Schlyer DJ, Zezulkova I, Wolf AP (1996) Brain monoamine oxidase A inhibition in cigarette smokers. Proc Natl Acad Sci USA 93(24):14065–14069
106. Herraiz T, Chaparro C (2005) Human monoamine oxidase is inhibited by tobacco smoke: beta-carboline alkaloids act as potent and reversible inhibitors. Biochem Biophys Res Commun 326(2):378–386. doi:10.1016/j.bbrc.2004.11.033
107. Leroy C, Bragulat V, Berlin I, Gregoire MC, Bottlaender M, Roumenov D, Dolle F, Bourgeois S, Penttila J, Artiges E, Martinot JL, Trichard C (2009) Cerebral monoamine oxidase A inhibition in tobacco smokers confirmed with PET and [11C]befloxatone. J Clin Psychopharmacol 29(1):86–88. doi:10.1097/JCP.0b013e31819e98f
108. Hogg RC (2016) Contribution of monoamine oxidase inhibition to tobacco dependence: a review of the evidence. Nicotine Tob Res Off J Soc Res Nicotine Tob 18(5):509–523. doi:10.1093/ntr/ntv245
109. Khalil AA, Davies B, Castagnoli N Jr (2006) Isolation and characterization of a monoamine oxidase B selective inhibitor from tobacco smoke. Bioorgan Med Chem 14(10):3392–3398. doi:10.1016/j.bmc.2005.12.057
110. Malczewska-Jaskola K, Jasiewicz B, Mrowczynska L (2016) Nicotine alkaloids as antioxidant and potential protective agents against in vitro oxidative haemolysis. Chem Biol Interact 243:62–71. doi:10.1016/j.cbi.2015.11.030