Multiple sclerosis and air pollution exposure: Mechanisms toward brain autoimmunity

Medical Hypotheses

Volumn 100, Issue , 2017, Pages 23-30

  Esmaeil Mousavi, Sayed ^a   Heydarpour, Pouria ^b   Reis, Jacques ^c   Amiri, Masoud ^a   Sahraian, Mohammad Ali ^b  

^a SHAHREKORD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c HÔPITAL DE HAUTEPIERRE   (France)

Author keywords

Air pollution; Autoimmunity; Blood brain barrier; Multiple sclerosis; Neuroinflammation; Oxidative stress

Indexed keywords

NUCLEAR FACTOR; AIR POLLUTANT; FREE RADICAL; OXYGEN;

AIR POLLUTION; ARTICLE; AUTOIMMUNITY; BLOOD BRAIN BARRIER; CELL ACTIVATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL EXPOSURE; HEALTH HAZARD; HUMAN; HYPOTHESIS; IMMUNE RESPONSE; INCIDENCE; INFLAMMATION; LIFESTYLE MODIFICATION; MICROGLIA; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; VITAMIN D DEFICIENCY; ADVERSE EFFECTS; AIR POLLUTANT; ANIMAL; BRAIN; CHEMISTRY; DEGENERATIVE DISEASE; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; THEORETICAL MODEL;

AIR POLLUTANTS; ANIMALS; AUTOIMMUNITY; BLOOD-BRAIN BARRIER; BRAIN; ENVIRONMENTAL EXPOSURE; FREE RADICALS; HUMANS; INFLAMMATION; MODELS, THEORETICAL; MULTIPLE SCLEROSIS; NEURODEGENERATIVE DISEASES; OXYGEN; VITAMIN D DEFICIENCY;

EID: 85009836770     PISSN: 03069877     EISSN: 15322777     Source Type: Journal    
DOI: 10.1016/j.mehy.2017.01.003     Document Type: Article

References (86)

1. [1] Feigin, V.L., Roth, G.A., Naghavi, M., et al. Global burden of stroke and risk factors in 188 countries, during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet Neurol, 2016.
2. [2] Hawkes, C.H., Del Tredici, K., Braak, H., Parkinson's disease: the dual hit theory revisited. Chemical senses, vol. 33, 2008, Oxford Univ Press Great Clarendon St, Oxford OX2 6DP, England.
3. [3] Calderon-Garciduenas, L., Maronpot, R.R., Torres-Jardon, R., et al. DNA damage in nasal and brain tissues of canines exposed to air pollutants is associated with evidence of chronic brain inflammation and neurodegeneration. Toxicol Pathol 31 (2003), 524–538.
4. [4] Ritz, B., Lee, P.-C., Hansen, J., et al. Traffic-related air pollution and parkinson's disease in Denmark: a case–control study. Environ Health Perspect, 124, 2016, 351.
5. [5] Grandjean, P., Landrigan, P.J., Neurobehavioural effects of developmental toxicity. Lancet Neurol 13 (2014), 330–338.
6. [6] Volk, H.E., Lurmann, F., Penfold, B., Hertz-Picciotto, I., McConnell, R., Traffic-related air pollution, particulate matter, and autism. JAMA Psychiatry 70 (2013), 71–77.
7. [7] Bellinger, D.C., Interpreting epidemiologic studies of developmental neurotoxicity: conceptual and analytic issues. Neurotoxicol Teratol 31 (2009), 267–274.
8. [8] Dutta, R., Trapp, B.D., Pathogenesis of axonal and neuronal damage in multiple sclerosis. Neurology 68 (2007), S22–S31.
9. [9] Calderón-Garcidueñas, L., Solt, A.C., Henríquez-Roldán, C., et al. Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain barrier, ultrafine particulate deposition, and accumulation of amyloid β-42 and α-synuclein in children and young adults. Toxicol Pathol 36 (2008), 289–310.
10. [10] Oikonen, M., Laaksonen, M., Laippala, P., et al. Ambient air quality and occurrence of multiple sclerosis relapse. Neuroepidemiology 22 (2003), 95–99.
11. [11] Oikonen, M.K., Erälinna, J.-P., Beta-interferon protects multiple sclerosis patients against enhanced susceptibility to infections caused by poor air quality. Neuroepidemiology 30 (2008), 13–19.
12. [12] Kaźmierski, R., Wender, M., Guzik, P., Zielonka, D., Association of influenza incidence with multiple sclerosis onset, Folia neuropathologica/Association of Polish Neuropathologists and Medical Research Centre. Pol Acad Sci 42 (2003), 19–23.
13. [13] Gregory, A.C., Shendell, D.G., Okosun, I.S., Gieseker, K.E., Multiple Sclerosis disease distribution and potential impact of environmental air pollutants in Georgia. Sci Total Environ 396 (2008), 42–51.
14. [14] Laura, A., Mirko, P., Tommaso, C., et al. Effects of particulate matter exposure on multiple sclerosis hospital admission in Lombardy region, Italy. Environ Res 145 (2016), 68–73.
15. [15] Leray, E., Le Pabic, E., Fermanian, C., Ongagna, J.-C., Bard, D., Seze, J., Does air pollution influence risk of relapse in multiple sclerosis?. Multiple Sclerosis 21 (2015), 742–743.
16. [16] Heydarpour, P., Amini, H., Khoshkish, S., Seidkhani, H., Sahraian, M.A., Yunesian, M., Potential impact of air pollution on multiple sclerosis in Tehran, Iran. Neuroepidemiology 43 (2014), 233–238.
17. [17] Vojinović, S., Savić, D., Lukić, S., Savić, L., Vojinović, J., Disease relapses in multiple sclerosis can be influenced by air pollution and climate seasonal conditions. Vojnosanit Pregl 72 (2015), 44–49.
18. [18] Calderon-Garciduenas, L., Cross, J.V., Franco-Lira, M., et al. Brain immune interactions and air pollution: macrophage inhibitory factor (MIF), prion cellular protein (PrPC), interleukin-6 (IL-6), interleukin 1 receptor antagonist (IL-1Ra), and interleukin-2 (IL-2) in cerebrospinal fluid and MIF in serum differentiate urban children exposed to severe vs. low air pollution. Front Neurosci, 7, 2013, 183.
19. [19] Liao, W., Lin, J.-X., Leonard, W.J., IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr Opin Immunol 23 (2011), 598–604.
20. [20] Phillips, G., Guo, S., Bender, R., Havrdová, E., Proskorovsky, I., Vollmer, T., Assessing the impact of multiple sclerosis disease activity and daclizumab HYP treatment on patient-reported outcomes: results from the SELECT trial. Multiple Sclerosis Relat Disord 6 (2016), 66–72.
21. [21] Gold, R., Giovannoni, G., Selmaj, K., et al. Daclizumab high-yield process in relapsing-remitting multiple sclerosis (SELECT): a randomised, double-blind, placebo-controlled trial. Lancet 381 (2013), 2167–2175.
22. [22] Li, J., Baud, O., Vartanian, T., Volpe, J.J., Rosenberg, P.A., Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Nat Acad Sci U.S.A. 102 (2005), 9936–9941.
23. [23] Van Horssen, J., Witte, M.E., Schreibelt, G., De Vries, H.E., Radical changes in multiple sclerosis pathogenesis. Biochim. Biophys. Acta (BBA)-Molecular Basis of Disease 1812 (2011), 141–150.
24. [24] Calderón-Garcidueñas, L., Mora-Tiscareño, A., Ontiveros, E., et al. Air pollution, cognitive deficits and brain abnormalities: a pilot study with children and dogs. Brain Cognition 68 (2008), 117–127.
25. [25] Miller, E., Wachowicz, B., Majsterek, I., Advances in antioxidative therapy of multiple sclerosis. Curr Med Chem 20 (2013), 4720–4730.
26. [26] Levesque, S., Taetzsch, T., Lull, M.E., et al. Diesel exhaust activates and primes microglia: air pollution, neuroinflammation, and regulation of dopaminergic neurotoxicity. Environ Health Perspect, 119, 2011, 1149.
27. [27] Karpus, W.J., Kennedy, K.J., MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J Leukocyte Biol 62 (1997), 681–687.
28. [28] Losy, J., Michałowska-Wender, G., Wender, M., Chemokines MIP-1 and MCP-1 and patients with multiple sclerosis treated with interferon beta-1a. Neurol Neurochir Pol 35 (2000), 583–588.
29. [29] Katsavos, S., Anagnostouli, M., Biomarkers in multiple sclerosis: an up-to-date overview. Multiple Sclerosis Int, 2013, 2013.
30. [30] Levesque, S., Surace, M.J., McDonald, J., Block, M.L., Air pollution & the brain: subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease. J Neuroinflammation, 8, 2011, 1.
31. [31] Ortiz, G.G., Pacheco-Moisés, F.P., Bitzer-Quintero, O.K., et al. Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clin Dev Immunol, 2013, 2013.
32. [32] Calderón-Garcidueñas, L., Kavanaugh, M., Block, M., et al. Neuroinflammation, hyperphosphorylated tau, diffuse amyloid plaques, and down-regulation of the cellular prion protein in air pollution exposed children and young adults. J Alzheimer's Dis 28 (2012), 93–107.
33. [33] van Berlo, D., Albrecht, C., Knaapen, A.M., et al. Comparative evaluation of the effects of short-term inhalation exposure to diesel engine exhaust on rat lung and brain. Arch Toxicol 84 (2010), 553–562.
34. [34] Farina, F., Sancini, G., Battaglia, C., et al. Milano summer particulate matter (PM10) triggers lung inflammation and extra pulmonary adverse events in mice. PLoS One, 8, 2013, e56636.
35. [35] Harris, V.K., Sadiq, S.A., Disease biomarkers in multiple sclerosis. Mol Diagn Ther 13 (2009), 225–244.
36. [36] Liu, J.S.-H., Zhao, M.-L., Brosnan, C.F., Lee, S.C., Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am J Pathol 158 (2001), 2057–2066.
37. [37] Dutta, K., Ghosh, D., Nazmi, A., Kumawat, K.L., Basu, A., A common carcinogen benzo [a] pyrene causes neuronal death in mouse via microglial activation. PLoS One, 5, 2010, e9984.
38. [38] Calderón-Garcidueñas, L., Azzarelli, B., Acuna, H., et al. Air pollution and brain damage. Toxicol Pathol 30 (2002), 373–389.
39. [39] Oppenheim, H.A., Lucero, J., Guyot, A.-C., et al. Exposure to vehicle emissions results in altered blood brain barrier permeability and expression of matrix metalloproteinases and tight junction proteins in mice. Particle Fibre Toxicol, 10, 2013, 1.
40. [40] Hartz, A.M., Bauer, B., Block, M.L., Hong, J.-S., Miller, D.S., Diesel exhaust particles induce oxidative stress, proinflammatory signaling, and P-glycoprotein up-regulation at the blood-brain barrier. FASEB J 22 (2008), 2723–2733.
41. [41] Hametner, S., Wimmer, I., Haider, L., Pfeifenbring, S., Brück, W., Lassmann, H., Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 74 (2013), 848–861.
42. [42] Mehindate, K., Sahlas, D., Frankel, D., et al. Proinflammatory cytokines promote glial heme oxygenase-1 expression and mitochondrial iron deposition: implications for multiple sclerosis. J Neurochem 77 (2001), 1386–1395.
43. [43] Rose, J.W., Hill, K.E., Watt, H.E., Carlson, N.G., Inflammatory cell expression of cyclooxygenase-2 in the multiple sclerosis lesion. J Neuroimmunol 149 (2004), 40–49.
44. [44] Minagar, A., Alexander, J.S., Blood-brain barrier disruption in multiple sclerosis. Multiple Sclerosis 9 (2003), 540–549.
45. [45] Haorah, J., Ramirez, S.H., Schall, K., Smith, D., Pandya, R., Persidsky, Y., Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood–brain barrier dysfunction. J Neurochem 101 (2007), 566–576.
46. [46] Lassmann, H., Van Horssen, J., Mahad, D., Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol 8 (2012), 647–656.
47. [47] Haufschild, T., Shaw, S.G., Kesselring, J., Flammer, J., Increased endothelin-1 plasma levels in patients with multiple sclerosis. J Neuroophthalmol 21 (2001), 37–38.
48. [48] Kouwenhoven, M., Özenci, V., Gomes, A., et al. Multiple sclerosis: elevated expression of matrix metalloproteinases in blood monocytes. J Autoimmun 16 (2001), 463–470.
49. [49] Avolio, C., Ruggieri, M., Giuliani, F., et al. Serum MMP-2 and MMP-9 are elevated in different multiple sclerosis subtypes. J Neuroimmunol 136 (2003), 46–53.
50. [50] Felts, P.A., Woolston, A.-M., Fernando, H.B., et al. Inflammation and primary demyelination induced by the intraspinal injection of lipopolysaccharide. Brain 128 (2005), 1649–1666.
51. [51] Lossinsky, A., Shivers, R., Structural pathways for macromolecular and cellular transport across the blood-brain barrier during inflammatory conditions. Review. Histol Histopathol 19 (2004), 535–564.
52. [52] Myers, C.L., Wertheimer, S.J., Schembri-King, J., Parks, T., Wallace, R.W., Induction of ICAM-1 by TNF-alpha, IL-1 beta, and LPS in human endothelial cells after downregulation of PKC. Am J Physiol-Cell Physiol 263 (1992), C767–C772.
53. [53] Kooij, G., van Horssen, J., de Lange, E.C., et al. T lymphocytes impair P-glycoprotein function during neuroinflammation. J Autoimmun 34 (2010), 416–425.
54. [54] Lassmann, H., Brück, W., Lucchinetti, C., Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy. Trends Mol Med 7 (2001), 115–121.
55. [55] Goldmann, T., Prinz, M., Role of microglia in CNS autoimmunity. Clin Dev Immunol, 2013, 2013.
56. [56] Xiao, B.-G., Link, H., Is there a balance between microglia and astrocytes in regulating Th1/Th2-cell responses and neuropathologies?. Immunol Today 20 (1999), 477–479.
57. [57] Oeckinghaus, A., Hayden, M.S., Ghosh, S., Crosstalk in NF-[kappa]B signaling pathways. Nat Immunol 12 (2011), 695–708.
58. [58] Mc Guire, C., Prinz, M., Beyaert, R., van Loo, G., Nuclear factor kappa B (NF-κB) in multiple sclerosis pathology. Trends Mol Med 19 (2013), 604–613.
59. [59] Block, M.L., Hong, J.-S., Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76 (2005), 77–98.
60. [60] Cox, G.M., Kithcart, A.P., Pitt, D., et al. Macrophage migration inhibitory factor potentiates autoimmune-mediated neuroinflammation. J Immunol 191 (2013), 1043–1054.
61. [61] Hagman, S., Raunio, M., Rossi, M., Dastidar, P., Elovaara, I., Disease-associated inflammatory biomarker profiles in blood in different subtypes of multiple sclerosis: prospective clinical and MRI follow-up study. J Neuroimmunol 234 (2011), 141–147.
62. [62] Witte, M.E., Mahad, D.J., Lassmann, H., van Horssen, J., Mitochondrial dysfunction contributes to neurodegeneration in multiple sclerosis. Trends Mol Med 20 (2014), 179–187.
63. [63] Su, K., Bourdette, D., Forte, M., Mitochondrial dysfunction and neurodegeneration in multiple sclerosis. Front Physiol, 4, 2013, 169.
64. [64] Yan, W., Ji, X., Shi, J., Li, G., Sang, N., Acute nitrogen dioxide inhalation induces mitochondrial dysfunction in rat brain. Environ Res 138 (2015), 416–424.
65. [65] Hou, L., Zhu, Z.-Z., Zhang, X., et al. Airborne particulate matter and mitochondrial damage: a cross-sectional study. Environ Health, 9, 2010, 1.
66. [66] Migliore, L., Coppedè, F., Environmental-induced oxidative stress in neurodegenerative disorders and aging. Mutat Res 674 (2009), 73–84.
67. [67] Witte, M.E., Bø, L., Rodenburg, R.J., et al. Enhanced number and activity of mitochondria in multiple sclerosis lesions. J Pathol 219 (2009), 193–204.
68. [68] Parihar, A., Vaccaro, P., Ghafourifar, P., Nitric oxide irreversibly inhibits cytochrome oxidase at low oxygen concentrations: evidence for inverse oxygen concentration-dependent peroxynitrite formation. IUBMB Life 60 (2008), 64–67.
69. [69] Engelhardt, S., Al-Ahmad, A.J., Gassmann, M., Ogunshola, O.O., Hypoxia selectively disrupts brain microvascular endothelial tight junction complexes through a hypoxia-inducible factor-1 (HIF-1) dependent mechanism. J Cell Physiol 229 (2014), 1096–1105.
70. [70] Munger, K.L., Levin, L.I., Hollis, B.W., Howard, N.S., Ascherio, A., Serum 25-hydroxyvitamin D levels and risk of multiple sclerosis. JAMA 296 (2006), 2832–2838.
71. [71] Correale, J., Ysrraelit, M.C., Gaitán, M.I., Immunomodulatory effects of Vitamin D in multiple sclerosis. Brain, 2009 p. awp033.
72. [72] Barrea, L., Savastano, S., Di Somma, C., et al. Low serum vitamin D-status, air pollution and obesity: a dangerous liaison. Rev Endocr Metab Disord, 2016, 1–8.
73. [73] Wacker, M., Holick, M.F., Sunlight and Vitamin D: a global perspective for health. Dermato-endocrinology 5 (2013), 51–108.
74. [74] Manicourt, D.-H., Devogelaer, J.-P., Urban tropospheric ozone increases the prevalence of vitamin D deficiency among Belgian postmenopausal women with outdoor activities during summer. J Clin Endocrinol Metab 93 (2008), 3893–3899.
75. [75] Hosseinpanah, F., Sima, H., Heibatollahi, M., Moghbel, N., Asefzade, S., Azizi, F., The effects of air pollution on vitamin D status in healthy women: a cross sectional study. BMC Public Health, 10, 2010, 519.
76. [76] Kelishadi, R., Moeini, R., Poursafa, P., Farajian, S., Yousefy, H., Okhovat-Souraki, A.-A., Independent association between air pollutants and vitamin D deficiency in young children in Isfahan, Iran. Paediatrics Int Child Health 34 (2014), 50–55.
77. [77] Agarwal, K., Mughal, M., Upadhyay, P., Berry, J., Mawer, E., Puliyel, J., The impact of atmospheric pollution on vitamin D status of infants and toddlers in Delhi, India. Arch Dis Childhood 87 (2002), 111–113.
78. [78] Patsopoulos, N.A., Barcellos, L.F., Hintzen, R.Q., et al. Fine-mapping the genetic association of the major histocompatibility complex in multiple sclerosis: HLA and non-HLA effects. PLoS Genet, 9, 2013, e1003926.
79. [79] Ramagopalan, S.V., Maugeri, N.J., Handunnetthi, L., et al. Expression of the multiple sclerosis-associated MHC class II Allele HLA-DRB1* 1501 is regulated by vitamin D. PLoS Genet, 5, 2009, e1000369.
80. [80] I.M.S.G. Consortium, Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat Genet 45 (2013), 1353–1360.
81. [81] Libbey, J.E., McCoy, L.L., Fujinami, R.S., Molecular mimicry in multiple sclerosis. Int Rev Neurobiol 79 (2007), 127–147.
82. [82] Calderón-Garcidueñas, L., Vojdani, A., Blaurock-Busch, E., et al. Air pollution and children: neural and tight junction antibodies and combustion metals, the role of barrier breakdown and brain immunity in neurodegeneration. J Alzheimer's Dis 43 (2015), 1039–1058.
83. [83] Vojdani, A., A potential link between environmental triggers and autoimmunity. Autoimmune Dis, 2014, 2014.
84. [84] Jangi, S., Gandhi, R., Cox, L.M., et al. Alterations of the human gut microbiome in multiple sclerosis. Nat Commun, 7, 2016.
85. [85] Beamish, L.A., Osornio-Vargas, A.R., Wine, E., Air pollution: an environmental factor contributing to intestinal disease. J Crohn's Colitis 5 (2011), 279–286.
86. [86] Tankou, S., Bry, L., Gerber, G., et al. Effect of Vitamin D level in the gut microbiome of MS patients (P2. 206). Neurology, 84, 2015 p. P2. 206.