REVIEW PAPER
Air pollution, oxidative stress, and exacerbation of autoimmune diseases
Submission date: 2017-03-28
Final revision date: 2017-06-01
Acceptance date: 2017-06-01
Publication date: 2017-10-30
Cent Eur J Immunol 2017;42(3):305-312
KEYWORDS
ABSTRACT
A number of epidemiological studies have shown a strong association between exposure to ambient airborne particulate matter (PM 2.5, PM < 1.0) and lung or cardiovascular diseases characterised by high mortality and morbidity. However, much less is known about the role of air pollution in the pathogenesis of autoimmune diseases, which constitutes a significant problem in modern society.
This paper summarises the state of current research regarding the influence of PM on the development and/or progression of autoimmune diseases. A brief review of the great body of research concerning pathogenesis of autoimmune disorders is presented. Then, the scope of our review is narrowed to the research related to the impact of particulate matter on oxidative and nitrosative stress, as well as exacerbation of chronic inflammation, because they can contribute to the development of autoimmune diseases. Moreover, we discuss the impact of various components of PM (metal, organic compounds) on PM toxicity and the ability to generate oxidants.
This paper summarises the state of current research regarding the influence of PM on the development and/or progression of autoimmune diseases. A brief review of the great body of research concerning pathogenesis of autoimmune disorders is presented. Then, the scope of our review is narrowed to the research related to the impact of particulate matter on oxidative and nitrosative stress, as well as exacerbation of chronic inflammation, because they can contribute to the development of autoimmune diseases. Moreover, we discuss the impact of various components of PM (metal, organic compounds) on PM toxicity and the ability to generate oxidants.
REFERENCES (120)
1.
Liu S-K, Cai S, Chen Y, et al. (2016): The effect of pollutional haze on pulmonary function. J Thorac Dis 8: E41-E56.
2.
Valavanidis A, Fiotakis K, Vlachogianni T (2008): Airborne particulate matter and human health: Toxicological assessment and importance of size and composition of particles for oxidative damage and carcinogenic mechanisms. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev Part C 26: 339-362.
3.
Pope CA, Burnett RT, Thurston GD, et al. (2004): Cardiovascular mortality and long-term exposure to particulate air pollution. Circulation 109: 71.
4.
Ghio AJ, Carraway MS, Madden MC (2012): Composition of air pollution particles and oxidative stress in cells, tissues, and living systems. J Toxicol Environ Health B 15: 1-21.
5.
Kanazawa N, Tchernev G, Wollina U (2014): Autoimmunity versus autoinflammation – friend or foe? Wien Med Wochenschr 164: 274-277.
6.
Doria A, Zen M, Bettio S, et al. (2012): Autoinflammation and autoimmunity: Bridging the divide. Autoimmun Rev 12: 22-30.
7.
Touitou I (2012): New genetic interpretation of old diseases. Autoimmun Rev 12: 5-9.
8.
Anaya J-M (2012): Common mechanisms of autoimmune diseases (the autoimmune tautology). Autoimmun Rev 11: 781-784.
9.
Oliver JE, Silman AJ (2009): Why are women predisposed to autoimmune rheumatic diseases? Arthritis Res Ther 11: 252.
10.
Fairweather D, Frisancho-Kiss S, Rose NR (2008): Sex differences in autoimmune disease from a pathological perspective. Am J Pathol 173.
11.
Jäger A, Kuchroo VK (2010): Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand J Immunol 72: 173-184.
12.
Chowdhary VR, Dai C, Tilahun AY, et al. (2015): A central role for HLA-DR3 in anti-Smith antibody responses and glomerulonephritis in a transgenic mouse model of spontaneous lupus. J Immunol 195: 4660-4667.
13.
Pociot F, Lernmark Å Genetic risk factors for type 1 diabetes. Lancet 387: 2331-2339.
14.
Ray S, Sonthalia N, Kundu S, Ganguly S (2012): Autoimmune disorders: An overview of molecular and cellular basis in today’s perspective. Journal of Clinical & Cellular Immunology.
15.
Kivity S, Agmon-Levin N, Blank M, Shoenfeld Y (2009): Infections and autoimmunity – friends or foes? Trends in Immunology 30: 409-414.
16.
Adams DD, Knight JG, Ebringer A (2010): Autoimmune diseases: Solution of the environmental, immunological and genetic components with principles for immunotherapy and transplantation. Autoimmunity Reviews 9: 525-530.
17.
Shoenfeld Y, Agmon-Levin N (2011): ‘Asia’ – autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun 36: 4-8.
18.
Israeli E, Agmon-Levin N, Blank M, Shoenfeld Y (2009): Adjuvants and autoimmunity. Lupus 18: 1217-1225.
19.
Sellner J, Kraus J, Awad A et al. (2011): The increasing incidence and prevalence of female multiple sclerosis – a critical analysis of potential environmental factors. Autoimmunity Reviews 10: 495-502.
20.
Gualtierotti R, Biggioggero M, Penatti AE, Meroni PL (2010): Updating on the pathogenesis of systemic lupus erythematosus. Autoimmunity Reviews 10: 3-7.
21.
Sies H (1997): Oxidative stress: Oxidants and antioxidants. Exp Physiol 82: 291-295.
22.
Klandorf H, Van Dyke K: Oxidative and nitrosative stresses: Their role in health and disease in man and birds. In: Oxidative Stress – Molecular Mechanisms and Biological Effects. Luschchak V, Semchyshyn HM (eds.). InTech, Rijeka 2012; 47-60.
23.
Wang X, Tao L, Hai CX (2012): Redox-regulating role of insulin: The essence of insulin effect. Mol Cell Endocrinol 349: 111-127.
24.
Balaban RS, Nemoto S, Finkel T (2005): Mitochondria, oxidants, and aging. Cell 120: 483-495.
25.
Taniyama Y, Griendling KK (2003): Reactive oxygen species in the vasculature. Molecular and Cellular Mechanisms 42: 1075-1081.
26.
Klebanoff SJ, Kettle AJ, Rosen H et al. (2013): Myeloperoxidase: A front-line defender against phagocytosed microorganisms. J Leukoc Biol 93: 185-198.
27.
Patel RP, Mcandrew J, Sellak H et al. (1999): Biological aspects of reactive nitrogen species. Biochim Biophys Acta Bioenergetics 1411: 385-400.
28.
Marcinkiewicz E, Marcinkiewicz J, Chłopicki S (2004): Nitric oxide – a pro-inflammatory and anti-inflammatory mediator. Central European Journal of Immunology 28: 74-78.
29.
Weinberg JB, Granger DL, Pisetsky DS et al. (1994): The role of nitric oxide in the pathogenesis of spontaneous murine autoimmune disease: Increased nitric oxide production and nitric oxide synthase expression in MRL-lpr/lpr mice, and reduction of spontaneous glomerulonephritis and arthritis by orally administered NG-monomethyl-L-arginine. The Journal of Experimental Medicine 179: 651-660.
30.
Wang G, Pierangeli SS, Papalardo E, et al. (2010): Markers of oxidative and nitrosative stress in systemic lupus erythematosus: Correlation with disease activity. Arthritis Rheum 62: 2064-2072.
31.
Xu X, Liu C, Xu Z, et al. (2011): Long-term exposure to ambient fine particulate pollution induces insulin resistance and mitochondrial alteration in adipose tissue. Toxicol Sci 124: 88-98.
32.
Wang J, Yi J (2008): Cancer cell killing via ROS: To increase or decrease, that is the question. Cancer Biol The 7: 1875-1884.
33.
Kurien BT, Hensley K, Bachmann M, Scofield RH (2006): Oxidatively modified autoantigens in autoimmune diseases. Free Radic Biol Med 41: 549-556.
34.
Frostegård J, Svenungsson E, Wu R, et al. (2005): Lipid peroxidation is enhanced in patients with systemic lupus erythematosus and is associated with arterial and renal disease manifestations. Arthritis Rheum 52: 192-200.
35.
Di Dalmazi G, Hirshberg J, Lyle D, et al. (2016): Reactive oxygen species in organ-specific autoimmunity. Autoimmunity Highlights 7: 11.
36.
Gomez-Mejiba SE, Zhai Z, Akram H, et al. (2009): Inhalation of environmental stressors & chronic inflammation: Autoimmunity and neurodegeneration. Mutat Res Genetic Toxicology and Environmental Mutagenesis 674: 62-72.
37.
Farhat SCL, Silva CA, Orione MM, et al. (2011): Air pollution in autoimmune rheumatic diseases: A review. Autoimmun Rev 11: 14-21.
38.
Brook RD, Franklin B, Cascio W, et al. (2004): Air pollution and cardiovascular disease. Circulation 109: 2655-2671.
39.
Sierra-Vargas MP, Teran LM (2012): Air pollution: Impact and prevention. Respirology 17: 1031-1038.
40.
Grzela K, Zagórska W, Grzela T (2012): Mechanisms of the innate immunity in the respiratory system. Centr Eur J Immunol 37: 280-285.
41.
Doran MF, Pond GR, Crowson CS et al. (2002): Trends in incidence and mortality in rheumatoid arthritis in Rochester, Minnesota, over a forty-year period. Arthritis Rheum 46: 625-631.
42.
Oikonen M, Laaksonen M, Laippala P, et al. (2003): Ambient air quality and occurrence of multiple sclerosis relapse. Neuroepidemiology 22: 95-99.
43.
Crispin JC, Hedrich CM, Tsokos GC (2013): Gene-function studies in systemic lupus erythematosus. Nat Rev Rheumatol 9: 476-484.
45.
Hatron PY, Plouvier B, François M, et al. (1982): Association of lupus erythematosus and silicosis. Rev Med Interne 3: 245-246.
46.
Parks CG, Cooper GS, Nylander-French LA, et al. (2002): Occupational exposure to crystalline silica and risk of systemic lupus erythematosus: A population-based, case-control study in the southeastern United States. Arthritis Rheum 46: 1840-1850.
47.
Balluz L, Philen R, Ortega L, et al. (2001): Investigation of systemic lupus erythematosus in Nogales, Arizona. Am J Epidemiol 154: 1029-1036.
48.
Cooper GS, Parks CG, Treadwell EL, et al. (2004): Occupational risk factors for the development of systemic lupus erythematosus. J Rheumatol 31: 1928-1933.
49.
Cooper GS, Wither J, Bernatsky S, et al. (2010): Occupational and environmental exposures and risk of systemic lupus erythematosus: Silica, sunlight, solvents. Rheumatology (Oxford) 49: 2172-2180.
50.
Bernatsky S, Hudson M, Panopalis P, et al. (2009): The cost of systemic sclerosis. Arthritis Care Res 61: 119-123.
51.
Olokoba AB, Obateru OA, Olokoba LB (2012): Type 2 diabetes mellitus: A review of current trends. Oman Medical Journal 27: 269-273.
52.
Hathout EH, Beeson WL, Nahab F, et al. (2002): Role of exposure to air pollutants in the development of type 1 diabetes before and after 5 yr of age. Pediatric Diabetes 3: 184-188.
53.
Hathout EH, Beeson WL, Ischander M, et al. (2006): Air pollution and type 1 diabetes in children. Pediatric Diabetes 7: 81-87.
54.
Dales RE, Cakmak S, Vidal CB, Rubio MA (2012): Air pollution and hospitalization for acute complications of diabetes in Chile. Environment International 46: 1-5.
55.
Brook RD, Jerrett M, Brook JR, et al. (2008): The relationship between diabetes mellitus and traffic-related air pollution. J Occup Environ Med 50: 32-38.
56.
Kan H, Jia J, Chen B (2004): The association of daily diabetes mortality and outdoor air pollution in Shanghai, China. J Environ Health 67: 21-26.
57.
Pearson JF, Bachireddy C, Shyamprasad S, et al. (2010): Association between fine particulate matter and diabetes prevalence in the U.S. Diabetes Care 33: 2196-2201.
58.
Callaghan R, Prabu A, Allan RB, et al. (2007): Direct healthcare costs and predictors of costs in patients with primary Sjögren’s syndrome. Rheumatology (Oxford) 46: 105-111.
59.
Bernatsky S, Renoux C, Suissa S (2010): Demyelinating events in rheumatoid arthritis after drug exposures. Ann Rheum Dis 69: 1691-1693.
60.
Aghdassi E, Zhang W, St-Pierr Y, et al. (2011): Healthcare cost and loss of productivity in a Canadian population of patients with and without lupus nephritis. J Rheumatol 38: 658-666.
61.
Bernatsky S, Smargiassi A, Johnson M, et al. (2015): Fine particulate air pollution, nitrogen dioxide, and systemic autoimmune rheumatic disease in Calgary, Alberta. Environ Res 140: 474-478.
62.
Arnson Y, Shoenfeld Y, Amital H (2010): Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34: J258-J265.
63.
Olsson ÅR, Skogh T, Wingren G (2001): Comorbidity and lifestyle, reproductive factors, and environmental exposures associated with rheumatoid arthritis. Ann Rheum Dis 60: 934-939.
64.
Silman AJ, Newman J, Macgregor AJ (1996): Cigarette smoking increases the risk of rheumatoid arthritis: Results from a nationwide study of disease-discordant twins. Arthritis Rheum 39: 732-735.
65.
Sluis-Cremer GK, Hessel PA, Hnizdo E, Churchill AR (1986): Relationship between silicosis and rheumatoid arthritis. Thorax 41: 596-601.
66.
Klockars M, Koskela RS, Järvinen E, et al. (1987): Silica exposure and rheumatoid arthritis: A follow up study of granite workers 1940-81. Br Med J (Clin Res Ed) 294: 997-1000.
67.
Zeft AS, Prahalad S, Lefevre S, et al. (2009): Juvenile idiopathic arthritis and exposure to fine particulate air pollution. Clin Exp Rheumatol 27: 877-884.
68.
Bernatsky S, Smargiassi A, Barnabe C, et al. (2016): Fine particulate air pollution and systemic autoimmune rheumatic disease in two Canadian provinces. Environ Res 146: 85-91.
69.
Hart JE, Laden F, Puett RC, et al. (2009): Exposure to traffic pollution and increased risk of rheumatoid arthritis. Environ Health Perspect 117: 1065-1069.
70.
Gregory Ii AC, Shendell DG, Okosun IS, Gieseker KE (2008): Multiple sclerosis disease distribution and potential impact of environmental air pollutants in Georgia. Sci Total Environ 396: 42-51.
71.
Heydarpour P, Amini H, Khoshkish S, et al. (2014): Potential impact of air pollution on multiple sclerosis in Tehran, Iran. Neuroepidemiology 43: 233-238.
72.
Vojinović S, Savić D, Lukić S, et al. (2015): Disease relapses in multiple sclerosis can be influenced by air pollution and climate seasonal conditions. Vojnosanit Pregl 72: 44-49.
73.
Leray E, Le Pabic E, Fermanian C, et al. (2015): Does air pollution influence risk of relapse in multiple sclerosis? Mult Scler 21: 742-743.
74.
Angelici L, Piola M, Cavalleri T, et al. (2016): Effects of particulate matter exposure on multiple sclerosis hospital admission in Lombardy region, Italy. Environ Res 145: 68-73.
75.
Ritz SA (2010): Air pollution as a potential contributor to the ‘epidemic’ of autoimmune disease. Med Hypotheses 74: 110-117.
76.
Prokopowicz ZM, Arce F, Biedron R, et al. (2010): Hypochlorous acid: A natural adjuvant that facilitates antigen processing, cross-priming, and the induction of adaptive immunity. J Immunol 184: 824-835.
77.
Davies KJA (1995): Oxidative stress: The paradox of aerobic life. Biochemical Society Symposium 61: 1-31.
78.
Negre-Salvayre A, Coatrieux C, Ingueneau C, Salvayre R (2008): Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 153: 6-20.
79.
Grune T, Davies KJ (2003): The proteasomal system and HNE-modified proteins. Mol Aspects Med 24: 195-204.
80.
Buzea C, Pacheco II, Robbie K (2007): Nanomaterials and nanoparticles: Sources and toxicity. Biointerphases 2: MR17-71.
81.
Harrison RM, Yin J (2000): Particulate matter in the atmosphere: Which particle properties are important for its effects on health? Sci Total Environ 249: 85-101.
82.
Shi T, Schins RP, Knaapen AM, et al. (2003): Hydroxyl radical generation by electron paramagnetic resonance as a new method to monitor ambient particulate matter composition. Journal of Environmental Monitoring : JEM 5: 550-556.
83.
Davis GS, Pfeiffer LM, Hemenway DR (1998): Persistent overexpression of interleukin-1beta and tumor necrosis factor-alpha in murine silicosis. J Environ Pathol Toxicol Oncol 17: 99-114.
84.
Davis GS, Holmes CE, Pfeiffer LM, Hemenway DR (2001): Lymphocytes, lymphokines, and silicosis. J Environ Pathol Toxicol Oncol 20: 14.
85.
Costantini LM, Gilberti RM, Knecht DA (2011): The phagocytosis and toxicity of amorphous silica. PLoS ONE 6: e14647.
86.
Lim Y, Kim JH, Kim KA, et al. (1999): Silica-induced apoptosis in vitro and in vivo. Toxicol Lett 108: 335-339.
87.
Joshi GN, Knecht DA (2013): Silica phagocytosis causes apoptosis and necrosis by different temporal and molecular pathways in alveolar macrophages. Apoptosis 18: 271-285.
88.
Brown JM, Archer AJ, Pfau JC, Holian A (2003): Silica accelerated systemic autoimmune disease in lupus-prone New Zealand mixed mice. Clin Exp Immunol 131: 415-421.
89.
Pfau JC, Brown JM, Holian A (2004): Silica-exposed mice generate autoantibodies to apoptotic cells. Toxicology 195: 167-176.
90.
Brown JM, Pfau JC, Holian A (2004): Immunoglobulin and lymphocyte responses following silica exposure in new zealand mixed mice. Inhal Toxicol 16: 133-139.
91.
Firestein GS, Mcinnes IB (2017): Immunopathogenesis of rheumatoid arthritis. Immunity 46: 183-196.
92.
Noonan CW, Pfau JC, Larson TC, Spence MR (2006): Nested case-control study of autoimmune disease in an asbestos-exposed population. Environ Health Perspect 114: 1243-1247.
93.
Bernatsky SM, Pfau JC, Fritzler MJ (2017): Environmental exposures and biomarkers predictive of rheumatoid arthritis and the pathway to precision medicine. J Laboratory and Precision Medicine 2.
95.
Nemmar A, Hoet PHM, Vanquickenborne B, et al. (2002): Passage of inhaled particles into the blood circulation in humans. Circulation 105: 411-414.
96.
Pope CA, Dockery DW (2006): Health effects of fine particulate air pollution: Lines that connect. J Air Waste Manag Assoc 56: 709-742.
97.
Eeden SFV, Hogg JC (2002): Systemic inflammatory response induced by particulate matter air pollution: The importance of bone-marrow stimulation. J Toxicol Environ Health A 65: 1597-1613.
98.
Ghio AJ, Huang Y-CT (2004): Exposure to concentrated ambient particles (caps): A review. Inhal Toxicol 16: 53-59.
99.
Stenfors N, Nordenhäll C, Salvi SS, et al. (2004): Different airway inflammatory responses in asthmatic and healthy humans exposed to diesel. Eur Respir J 23: 82-86.
100.
Behndig AF, Mudway IS, Brown JL, et al. (2006): Airway antioxidant and inflammatory responses to diesel exhaust exposure in healthy humans. Eur Respir J 27: 359-365.
101.
Takano H, Ichinose T, Miyabara Y, et al. (1998): Inhalation of diesel exhaust enhances allergen-related eosinophil recruitment and airway hyperresponsiveness in mice. Toxicol Appl Pharmacol 150: 328-337.
102.
Salvi, Holgate (1999): Mechanisms of particulate matter toxicity. Clin Exp Allergy 29: 1187-1194.
103.
Poniedziałek B, Rzymski P, Wiktorowicz K (2012): In vitro effect of cadmium on the function of human lymphocytes and neutrophils. Centr Eur J Immunol 37: 110-113.
104.
Araujo JA, Barajas B, Kleinman M, et al. (2008): Ambient particulate pollutants in the ultrafine range promote early atherosclerosis and systemic oxidative stress. Circ Res 102: 589-596.
105.
Barregard L, Sällsten G, Gustafson P, et al. (2006): Experimental exposure to wood-smoke particles in healthy humans: Effects on markers of inflammation, coagulation, and lipid peroxidation. Inhal Toxicol 18: 845-853.
106.
Goto Y, Ishii H, Hogg JC, et al. (2004): Particulate matter air pollution stimulates monocyte release from the bone marrow. Am J Respir Crit Care Med 170: 891-897.
107.
Fujii T, Hayashi S, Hogg JC, et al. (2002): Interaction of alveolar macrophages and airway epithelial cells following exposure to particulate matter produces mediators that stimulate the bone marrow. Am J Respir Cell Mol Biol 27: 34-41.
108.
Liao D, Heiss G, Chinchilli VM, et al. (2004): Association of criteria pollutants with plasma hemostatic//inflammatory markers: A population-based study. J Expo Anal Environ Epidemiol 15: 319-328.
109.
Eeden SFV, Tan WC, Suwa T, et al. (2001): Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM10). Am J Respir Crit Care Med 164: 826-830.
110.
Verstraelen S, Van Den Heuvel R, Nelissen I, et al. (2005): Flow cytometric characterisation of antigen presenting dendritic cells after in vitro exposure to diesel exhaust particles. Toxicology In Vitro 19: 903-907.
111.
Becker S, Soukup J (2003): Coarse(PM 2.5-10), fine(PM 2.5), and ultrafine air pollution particles induce/increase immune costimulatory receptors on human blood-derived monocytes but not on alveolar macrophages. J Toxicol Environ Health, A 66: 847-859.
112.
Bleck B, Tse DB, Curotto De Lafaille MA, et al. (2008): Diesel exhaust particle-exposed human bronchial epithelial cells induce dendritic cell maturation and polarization via thymic stromal lymphopoietin. J Clin Immunol 28: 147-156.
113.
Hamilton RF, Holian A, Morandi MT (2004): A comparison of asbestos and urban particulate matter in the in vitro modification of human alveolar macrophage antigen-presenting cell function. Exp Lung Res 30: 147-162.
114.
Kantengwa S, Jornot L, Devenoges C, Nicod LP (2003): Superoxide anions induce the maturation of human dendritic cells. Am J Respir Crit Care Med 167: 431-437.
115.
Alderman CJJ, Shah S, Foreman JC, et al. (2002): The role of advanced oxidation protein products in regulation of dendritic cell function. Free Radic Biol Med 32: 377-385.
116.
Rutault K, Alderman C, Chain BM, Katz DR (1999): Reactive oxygen species activate human peripheral blood dendritic cells. Free Radic Biol Med 26: 232-238.
117.
Granum B, Gaarder PI, Groeng EC, et al. (2001): Fine particles of widely different composition have an adjuvant effect on the production of allergen-specific antibodies. Toxicol Lett 118: 171-181.
118.
Takano H, Yoshikawa T, Ichinose T, et al. (1997): Diesel exhaust particles enhance antigen-induced airway inflammation and local cytokine expression in mice. Am J Respir Crit Care Med 156: 36-42.
119.
Van Zijverden M, Van Der Pijl A, Bol M, et al. (2000): Diesel exhaust, carbon black, and silica particles display distinct Th1/Th2 modulating activity. Toxicol Appl Pharmacol 168: 131-139.
120.
Yi L, Wen C, Fan W (2017): Fine particulate matter (PM2.5), a risk factor of rat gestational diabetes with altered blood glucose and pancreatic GLUT2 expression. Gynecol Endocrinol: 1-6.
Share
RELATED ARTICLE
| eISSN: | 1644-4124 |
| ISSN: | 1426-3912 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
