Environmental Particulate Matter Induces Murine Intestinal Inflammatory Responses and Alters the Gut Microbiome

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Kish, Lisa ^a   Hotte, Naomi ^a   Kaplan, Gilaad G ^b   Vincent, Renaud ^c   Tso, Robert ^a   Gänzle, Michael ^a   Rioux, Kevin P ^b   Thiesen, Aducio ^a   Barkema, Herman W ^d   Wine, Eytan ^a   Madsen, Karen L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c HEALTH CANADA   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P35; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 5; LACTULOSE; MANNITOL; SHORT CHAIN FATTY ACID;

AIR POLLUTANT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL PROLIFERATION; COLON; CONTROLLED STUDY; CYTOKINE RELEASE; ENTERITIS; ENZYME ACTIVITY; FECES ANALYSIS; FEMALE; HISTOLOGY; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MICROBIOME; MOUSE; NONHUMAN; PARTICULATE MATTER; PROTEIN EXPRESSION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SPLEEN CELL; URINARY EXCRETION; WILD TYPE;

AIR POLLUTANTS; ANIMALS; COLON; CYTOKINES; ENVIRONMENTAL EXPOSURE; FATTY ACIDS, VOLATILE; FEMALE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; INFLAMMATION; INTESTINE, SMALL; INTESTINES; MICE; MICE, KNOCKOUT; MICROBIOTA; PARTICULATE MATTER; PERMEABILITY; SPLEEN; TIME FACTORS;

MURINAE; MUS;

EID: 84876545124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062220     Document Type: Article

References (72)

1. Sarkar S, Khillare PS (2012) Profile of PAHs in the inhalable particulate fraction: source apportionment and associated health risks in a tropical megacity. Environ Monit Assess.
2. Brunekreef B, Holgate ST, (2002) Air pollution and health. Lancet 360: 1233-1242.
3. Vincent R, Bjarnason SG, Adamson IY, Hedgecock C, Kumarathasan P, et al. (1997) Acute pulmonary toxicity of urban particulate matter and ozone. Am J Pathol 151: 1563-1570.
4. Chen TM, Shofer S, Gokhale J, Kuschner WG, (2007) Outdoor air pollution: overview and historical perspective. Am J Med Sci 333: 230-234.
5. Hetland RB, Cassee FR, Lag M, Refsnes M, Dybing E, et al. (2005) Cytokine release from alveolar macrophages exposed to ambient particulate matter: heterogeneity in relation to size, city and season. Part Fibre Toxicol 2: 4.
6. Fujii T, Hayashi S, Hogg JC, Vincent R, Van Eeden SF, (2001) Particulate matter induces cytokine expression in human bronchial epithelial cells. Am J Respir Cell Mol Biol 25: 265-271.
7. Mills NL, Donaldson K, Hadoke PW, Boon NA, MacNee W, et al. (2009) Adverse cardiovascular effects of air pollution. Nat Clin Pract Cardiovasc Med 6: 36-44.
8. Brook RD, Rajagopalan S, (2010) Particulate matter air pollution and atherosclerosis. Curr Atheroscler Rep 12: 291-300.
9. Brook RD, Rajagopalan S, Pope CA, 3rd, Brook JR, Bhatnagar A, et al (2010) Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation 121: 2331-2378.
10. Samet JM, Zeger SL, Dominici F, Curriero F, Coursac I, et al. (2000) The National Morbidity, Mortality, and Air Pollution Study. Part II: Morbidity and mortality from air pollution in the United States. Res Rep Health Eff Inst 94: 5-70; discussion 71-79.
11. Beamish LA, Osornio-Vargas AR, Wine E, (2011) Air pollution: An environmental factor contributing to intestinal disease. J Crohns Colitis 5: 279-286.
12. Kaplan GG, Dixon E, Panaccione R, Fong A, Chen L, et al. (2009) Effect of ambient air pollution on the incidence of appendicitis. CMAJ 181: 591-597.
13. Orazzo F, Nespoli L, Ito K, Tassinari D, Giardina D, et al. (2009) Air pollution, aeroallergens, and emergency room visits for acute respiratory diseases and gastroenteric disorders among young children in six Italian cities. Environ Health Perspect 117: 1780-1785.
14. Kaplan GG, Hubbard J, Korzenik J, Sands BE, Panaccione R, et al. (2010) The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterol 105: 2412-2419.
15. Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K, (2011) Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm Bowel Dis 17: 1138-1145.
16. Guberan E, Usel M, Raymond L, Bolay J, Fioretta G, et al. (1992) Increased risk for lung cancer and for cancer of the gastrointestinal tract among Geneva professional drivers. Br J Ind Med 49: 337-344.
17. Moller W, Haussinger K, Winkler-Heil R, Stahlhofen W, Meyer T, et al. (2004) Mucociliary and long-term particle clearance in the airways of healthy nonsmoker subjects. J Appl Physiol 97: 2200-2206.
18. Leblanc JC, Guerin T, Noel L, Calamassi-Tran G, Volatier JL, et al. (2005) Dietary exposure estimates of 18 elements from the 1st French Total Diet Study. Food Addit Contam 22: 624-641.
19. De Brouwere K, Buekers J, Cornelis C, Schlekat CE, Oller AR, (2012) Assessment of indirect human exposure to environmental sources of nickel: oral exposure and risk characterization for systemic effects. Sci Total Environ 419: 25-36.
20. Mutlu EA, Engen PA, Soberanes S, Urich D, Forsyth CB, et al. (2011) Particulate matter air pollution causes oxidant-mediated increase in gut permeability in mice. Part Fibre Toxicol 8: 19.
21. Arrieta MC, Bistritz L, Meddings JB, (2006) Alterations in intestinal permeability. Gut 55: 1512-1520.
22. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W, (1993) Interleukin-10-deficient mice develop chronic enterocolitis.[comment]. Cell 75: 263-274.
23. Madsen KL, Fedorak RN, Tavernini MM, Doyle JS, (2002) Normal Breast Milk Limits the Development of Colitis in IL-10-Deficient Mice. Inflammatory Bowel Diseases 8: 390-398.
24. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, et al. (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121: 580-591.
25. Ewaschuk J, Diaz H, Meddings L, Diederichs B, Dmytrash A, et al. (2008) Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol 295: G1025-1034.
26. Arrieta MC, Madsen K, Doyle J, Meddings J, (2009) Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse. Gut 58: 41-48.
27. Ma BW, Bokulich NA, Castillo PA, Kananurak A, Underwood MA, et al. (2012) Routine habitat change: a source of unrecognized transient alteration of intestinal microbiota in laboratory mice. PLoS One 7: e47416.
28. Mage D, Ozolins G, Peterson P, Webster A, Orthofer RVV, et al. (1996) Urban air pollution in megacities of the world. Atmospheric Environment 30: 681-686.
29. Hotte NS, Salim SY, Tso RH, Albert EJ, Bach P, et al. (2012) Patients with inflammatory bowel disease exhibit dysregulated responses to microbial DNA. PLoS ONE 7: e37932.
30. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
31. Meddings JB, Gibbons I, (1998) Discrimination of site-specific alterations in gastrointestinal permeability in the rat. Gastroenterology 114: 83-92.
32. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN, (1999) Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice.[comment]. Gastroenterology 116: 1107-1114.
33. Liu WT, Marsh TL, Cheng H, Forney LJ, (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516-4522.
34. Shyu C, Soule T, Bent SJ, Foster JA, Forney LJ, (2007) MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA genes. Microb Ecol 53: 562-570.
35. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-145.
36. Kaplan GG, Szyszkowicz M, Fichna J, Rowe BH, Porada E, et al. (2012) Non-specific abdominal pain and air pollution: a novel association. PLoS One 7: e47669.
37. Soon IS, Molodecky NA, Rabi DM, Ghali WA, Barkema HW, et al. (2012) The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol 12: 51.
38. Donaldson K, Stone V, Borm PJ, Jimenez LA, Gilmour PS, et al. (2003) Oxidative stress and calcium signaling in the adverse effects of environmental particles (PM10). Free Radic Biol Med 34: 1369-1382.
39. Donaldson K, Tran L, Jimenez LA, Duffin R, Newby DE, et al. (2005) Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Part Fibre Toxicol 2: 10.
40. Hirota JA, Hirota SA, Warner SM, Stefanowicz D, Shaheen F, et al. (2012) The airway epithelium nucleotide-binding domain and leucine-rich repeat protein 3 inflammasome is activated by urban particulate matter. J Allergy Clin Immunol 129: 1116-1125 e1116.
41. Kooter I, Pennings J, Opperhuizen A, Cassee F, (2005) Gene expression pattern in spontaneously hypertensive rats exposed to urban particulate matter (EHC-93). Inhal Toxicol 17: 53-65.
42. Sarkar S, Song Y, Kipen HM, Laumbach RJ, Zhang J, et al. (2012) Suppression of the NF-kappaB pathway by diesel exhaust particles impairs human antimycobacterial immunity. J Immunol 188: 2778-2793.
43. Yin XJ, Dong CC, Ma JY, Roberts JR, Antonini JM, et al. (2007) Suppression of phagocytic and bactericidal functions of rat alveolar macrophages by the organic component of diesel exhaust particles. J Toxicol Environ Health A 70: 820-828.
44. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the human intestinal microbial flora.[see comment]. Science 308: 1635-1638.
45. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, et al. (2002) Mucosal flora in inflammatory bowel disease.[see comment]. Gastroenterology 122: 44-54.
46. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, et al. (2006) Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach.[see comment]. Gut 55: 205-211.
47. Frank D, Amand AL, Feldman RA, Boedeker EC, Harpaz N, et al. (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. PNAS 104: 13780-13785.
48. Sepehri S, Kotlowski R, Bernstein CN, Krause DO (2007) Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflammatory Bowel Diseases.
49. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H, (2005) Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. Journal of Clinical Microbiology 43: 3380-3389.
50. Li XY, Donaldson K, Rahman I, MacNee W, (1994) An investigation of the role of glutathione in increased epithelial permeability induced by cigarette smoke in vivo and in vitro. Am J Respir Crit Care Med 149: 1518-1525.
51. Madara JL, (2000) Modulation of tight junctional permeability. Advanced Drug Delivery Reviews 41: 251-253.
52. Hall J, Bouladoux N, Sun C, Wohlfert EA, Blank RB, et al. (2008) Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29: 1-13.
53. Ivanov, II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, et al. (2008) Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host & Microbe 4: 337-349.
54. Madsen KL, Doyle JS, Tavernini MM, Jewell LD, Rennie RP, et al. (2000) Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology 118: 1094-1105.
55. Campeau JL, Salim SY, Albert EJ, Hotte N, Madsen KL, (2012) Intestinal epithelial cells modulate antigen-presenting cell responses to bacterial DNA. Infect Immun 80: 2632-2644.
56. Kitts CL, (2001) Terminal restriction fragment patterns: a tool for comparing microbial communities and assessing community dynamics. Curr Issues Intest Microbiol 2: 17-25.
57. Zhang R, Thiyagarajan V, Qian PY, (2008) Evaluation of terminal-restriction fragment length polymorphism analysis in contrasting marine environments. FEMS Microbiol Ecol 65: 169-178.
58. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, et al. (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27: 104-119.
59. Solano AF, Leipnitz G, De Bortoli GM, Seminotti B, Amaral AU, et al. (2008) Induction of oxidative stress by the metabolites accumulating in isovaleric acidemia in brain cortex of young rats. Free Radic Res 42: 707-715.
60. Sunkara LT, Achanta M, Schreiber NB, Bommineni YR, Dai G, et al. (2011) Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS ONE 6: e27225.
61. Willemsen LE, Koetsier MA, van Deventer SJ, van Tol EA, (2003) Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut 52: 1442-1447.
62. Becker S, Soukup JM, Gilmour MI, Devlin RB, (1996) Stimulation of human and rat alveolar macrophages by urban air particulates: effects on oxidant radical generation and cytokine production. Toxicol Appl Pharmacol 141: 637-648.
63. Adamson IY, Prieditis H, Vincent R, (1999) Pulmonary toxicity of an atmospheric particulate sample is due to the soluble fraction. Toxicol Appl Pharmacol 157: 43-50.
64. Vincent R, Goegan P, Johnson G, Brook JR, Kumarathasan P, et al. (1997) Regulation of promoter-CAT stress genes in HepG2 cells by suspensions of particles from ambient air. Fundam Appl Toxicol 39: 18-32.
65. Carter JD, Ghio AJ, Samet JM, Devlin RB, (1997) Cytokine production by human airway epithelial cells after exposure to an air pollution particle is metal-dependent. Toxicol Appl Pharmacol 146: 180-188.
66. Kennedy T, Ghio AJ, Reed W, Samet J, Zagorski J, et al. (1998) Copper-dependent inflammation and nuclear factor-kappaB activation by particulate air pollution. Am J Respir Cell Mol Biol 19: 366-378.
67. Ghio AJ, Carter JD, Richards JH, Brighton LE, Lay JC, et al. (1998) Disruption of normal iron homeostasis after bronchial instillation of an iron-containing particle. Am J Physiol 274: L396-403.
68. Mukae H, Hogg JC, English D, Vincent R, van Eeden SF, (2000) Phagocytosis of particulate air pollutants by human alveolar macrophages stimulates the bone marrow. Am J Physiol Lung Cell Mol Physiol 279: L924-931.
69. Semmler-Behnke M, Takenaka S, Fertsch S, Wenk A, Seitz J, et al. (2007) Efficient elimination of inhaled nanoparticles from the alveolar region: evidence for interstitial uptake and subsequent reentrainment onto airways epithelium. Environ Health Perspect 115: 728-733.
70. Lomer MC, Thompson RP, Powell JJ, (2002) Fine and ultrafine particles of the diet: influence on the mucosal immune response and association with Crohn's disease. Proc Nutr Soc 61: 123-130.
71. Urbanski SJ AA, Green FH, Haber G, (1989) Pigment resembling atmospheric dust in Peyer's patches. Mod Pathol 2: 222-226.
72. Lomer MC, Hutchinson C, Volkert S, Greenfield SM, Catterall A, et al. (2004) Dietary sources of inorganic microparticles and their intake in healthy subjects and patients with Crohn's disease. Br J Nutr 92: 947-955.