Ambient fine particulate matter induces apoptosis of endothelial progenitor cells through reactive oxygen species formation

Cellular Physiology and Biochemistry

Volumn 35, Issue 1, 2015, Pages 353-363

  Cui, Yuqi ^a   Xie, Xiaoyun ^c   Jia, Fengpeng ^a   He, Jianfeng ^a   Li, Zhihong ^a   Fu, Minghuan ^a   Hao, Hong ^a   Liu, Ying ^a   Liu, Jason Z ^a   Cowan, Peter J ^a   Zhu, Hua ^a,b   Sun, Qinghua ^a   Liu, Zhenguo ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Apoptosis; Endothelial progenitor cells; PM; ROS

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; EXTRACELLULAR SUPEROXIDE DISMUTASE; GLUTATHIONE PEROXIDASE 1; INTERLEUKIN 1BETA; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; ACETYLCYSTEINE; GLUTATHIONE PEROXIDASE; PARTICULATE MATTER; SOD3 PROTEIN, MOUSE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR;

ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIAL PROGENITOR CELL; FLOW CYTOMETRY; IN VIVO STUDY; INFLAMMATION; MALE; MOUSE; NONHUMAN; PARTICLE SIZE; PARTICULATE MATTER; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BLOOD; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; LUNG; METABOLISM; PATHOLOGY; TOXICITY;

MUS; MUS MUSCULUS;

ACETYLCYSTEINE; ANIMALS; APOPTOSIS; BONE MARROW CELLS; CELLS, CULTURED; ENDOTHELIAL PROGENITOR CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLUTATHIONE PEROXIDASE; INTERLEUKIN-1BETA; LUNG; MALE; MICE; MICE, INBRED C57BL; PARTICULATE MATTER; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84921358633     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000369701     Document Type: Article

References (49)

1. Lee PS, Poh KK: Endothelial progenitor cells in cardiovascular diseases. World J Stem Cells 2014;6:355-366
2. Du F, Zhou J, Gong R, Huang X, Pansuria M, Virtue A, Li X, Wang H, Yang XF: Endothelial progenitor cells in atherosclerosis. Front Biosci 201247:2327-2349.
3. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Tang W, Gregg D, Ramaswami R, Pippen AM, Annex BH, Dong CM, Taylor DA: Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003408:457-463.
4. Urbich C, Dimmeler S: Endothelial progenitor cells: Characterization and role in vascular biology. Circ Res :2004;95 :343-353.
5. Werner N, Kosiol 5, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G: Circulating endothelial progenitor cells and cardiovascular outcomes. New EnglJ Med 2005;353:999-1007.
6. Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, Amann M, Anderson HR, Andrews KG, Aryee M, Atkinson C, Bacchus U, Bahalim AN, Balakrishnan K, Balmes L Barker-Collo S, Baxter A, Bell ML Blore JD, Blyth F, Bonner C, Borges G, Bourne R, Boussinesq M, Brauer M, Brooks P, Bruce NG, Brunekreef B, Bryan-Hancock C, Bucello C, Buchbinder R, Bull F, Burnett RT, Byers TE, Calabria B, Carapetis L Carnahan E, Chafe Z, Charlson F, Chen H, Chen JS, Cheng AT, Child JC, Cohen A, Colson KE, Cowie BC, Darby S, Darling S, Davis A, Degenhardt L Dentener F, Des Jarlais DC, Devries K, Dherani M, Ding EL Dorsey ER, Driscoll T, Edmond K, Ali SE, Engell RE, Erwin PJ, Fahimi S, Falder G, Farzadfar F, Ferrari A, Finucane MM, Flaxman S, Fowkes FG, Freedman G, Freeman MK, Gakidou E, Ghosh S, GioVannucci E, Gmel G, Graham K, Grainger R, Grant B, Gunnell D, Gutierrez HR, Hall W, Hoek HW, Hogan A, Hosgood HD, 3rd, Hoy D, Hu H, Hubbell BJ, Hutchings SJ, Ibeanusi SE, Jacklyn GL, Jasrasaria R, Jonas JB, Kan H, Kanis JA, Kassebaum N, Kawakami N, Khang YH, Khatibzadeh S, Khoo JP, Kok C, Laden F, Lalloo R, Lan Q, Lathlean T, Leasher JL, Leigh L Li Y, Lin JK, Lipshultz SE, London S, Lozano R, Lu Y, Mak L Malekzadeh R, Mallinger L Marcenes W, March L Marks R, Martin R, McGale P, McGrath L Mehta S, Mensah GA, Merriman TR, Micha R, Michaud C, Mishra V, Mohd Hanafiah K, Mokdad AA, Morawska L Mozaffarian D, Murphy T, Naghavi M, Neal B, Nelson PK, Nolla JM, Norman R, Olives C, Omer SB, Orchard L Osborne R, Ostro B, Page A, Pandey KD, Parry CD, Passmore E, Patra L Pearce N, Pelizzari PM, Petzold M, Phillips MR, Pope D, Pope CA, 3rd, Powles L Rao M, Razavi H, Rehfuess EA, Rehm JT, Ritz B, Rivara FP, Roberts T, Robinson C, Rodriguez-Portales JA, Romieu I, Room R, Rosenfeld LC, Roy A, Rushton L, Salomon JA, Sampson U, Sanchez-Riera L, Sanman E, Sapkota A, Seedat S, Shi P, Shield K, Shivakoti R, Singh GM, Sleet DA, Smith E, Smith KR, Stapelberg NJ, Steenland K, Stockl H, Stovner U, Straif K, Straney L Thurston GD, Tran JH, Van Dingenen R, Van Donkelaar A, Veerman JL, Vijayakumar L Weintraub R, Weissman MM, White RA, Whiteford H, Wiersma ST, Wilkinson JD, Williams HC, Williams W, Wilson N, Woolf AD, Yip P, Zielinski JM, Lopez AD, Murray CJ, Ezzati M, AlMazroa MA, Memish ZA: A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: A systematic analysis for the global burden of disease study 2010. Lancet 2012;380:2224-2260.
7. BrookRD, Rajagopalan 5, Pope CA, 3rd, BrookJR, BhatnagarA, Diez-RouxAV, Holguin F, HongY, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC, Jr., Whitsel L, Kaufman JD, American Heart Association Council on E, Prevention CotKiCD, Council on Nutrition PA, Metabolism: Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the american heart association. Circulation 2010421:2331-2378
8. Brunekreef B, Forsberg B: Epidemiological evidence of effects of coarse airborne particles on health. Europ RespirJ 2005;26:309-318.
9. Brook RD, Urch B, Dvonch JT, Bard RU, Speck M, Keeler G, Morishita M, Marsik FJ, Kamal AS, Kaciroti N, Harkema L Corey P, Silverman F, Gold DR, Wellenius G, Mittleman MA, Rajagopalan 5, Brook JR: Insights into the mechanisms and mediators of the effects of air pollution exposure on blood pressure and vascular function in healthy humans. Hypertension 2009;54:659-667.
10. Sun QH, Wang AX, Jin XM, Natanzon A, Duquaine D, Brook RD, Aguinaldo JGS, Fayad ZA, Fuster V, Lippmann M, Chen LC, Rajagopalan 5: Long-term air pollution exposure and acceleration of atherosclerosis and vascular inflammation in an animal model. Jama-J Am Med Assoc 2005;294:3003-3010.
11. Liberda EN, Cuevas AK, Gillespie PA, Grunig G, Qu QS, Chen LC: Exposure to inhaled nickel nanoparticles causes a reduction in number and function of bone marrow endothelial progenitor cells. Inhal Toxicol 2010;22;95-99
12. Brook RD, Bard RL Kaplan ML Yalavarthi 5, Morishita M, Dvonch JT, Wang L, Yang HY, Spino C, Mukherjee B, Oral EA, Sun QH, BrookJR, Harkema L Rajagopalan 5: The effect of acute exposure to coarse particulate matter air pollution in a rural location on circulating endothelial progenitor cells: Results from a randomized controlled study. Inhal Toxicol 2013; 25:587-592.
13. Khurshid SS, Siegel JA, Kinney KA: Indoor particulate reactive oxygen species concentrations. Envir Res; 2014;43; 2; 46-53
14. Nocun MS, Schantz MM: Determination of selected oxygenated polycyclic aromatic hydrocarbons (oxypahs) in diesel and air particulate matter standard reference materials (srms). Anal Bioanal Chem;2013; 405;5583-5593
15. Mutlu GM, Green D, Bellmeyer A, Baker CM, Burgess Z, Rajamannan N, Christman JW, Foiles N, Kamp DW, Ghio AL Chandel NS, Dean DA, Sznajder JI, Budinger GR: Ambient particulate matter accelerates coagulation via an il-6-dependent pathway. J Clin Invest 2007417:2952-2961.
16. Shadie AM, Herbert C, Kumar RK: Ambient particulate matter induces an exacerbation of airway inflammation in experimental asthma: Role of interleukin-33. Clin Exp Immunol 2014477:491-499.
17. Arantes-Costa FM, Lopes FD, Toledo AC, Magliarelli-Filho PA, Moriya HT, Carvalho-Oliveira R, Mauad T, Saldiva PH, Martins MA: Effects of residual oil fly ash (rofa) in mice with chronic allergic pulmonary inflammation. Toxicol Pathol 2008;36:680-686.
18. Ferraro SA, Yakisich JS, Gallo FT, Tasat DR: Simvastatin pretreatment prevents ambient particle-induced lung injury in mice. Inhal Toxicol 2011;23:889-896.
19. Alberg T, Nilsen A, Hansen JS, Nygaard UC, Lovik M: Nitrogen dioxide: No influence on allergic sensitization in an intranasal mouse model with ovalbumin and diesel exhaust particles. Inhal Toxicol 2011;23:268-276.
20. Mysore TB, Shinkel TA, Collins L Salvaris EL Fisicaro N, Murray-Segal U, Johnson LE, Lepore DA, Walters SN, Stokes R, Chandra AP, OConnell PJ, dApice AL Cowan PJ: Overexpression of glutathione peroxidase with two isoforms of superoxide dismutase protects mouse islets from oxidative injury and improves islet graft function. Diabetes 2005;54:2109-2116.
21. Mital R, Zhang W, Cai M, Huttinger ZM, Goodman LA, Wheeler DG, Ziolo MT, Dwyer KM, dApice AL Zweier JL He G, Cowan L Gumina RJ: Antioxidant network expression abrogates oxidative posttranslational modifications in mice. Am J Physiol Heart Circul Physiol 2011;300:H1960-1970.
22. Rosenkranz AR, Schmaldienst 5, Stuhlmeier KM, Chen WL Knapp W, Zlabinger GJ: A microplate assay for the detection of oxidative products using 2,7-dichlorofluorescin-diacetate. J Immunol Methods; 1992;156; 3;9-45;215639-45.
23. Jurczyszyn A, Zebzda A, Czepiel L Perucki W, Bazan-Socha 5, Cibor D, Owczarek D, Majka M: Geldanamycin and its derivatives inhibit the growth of myeloma cells and reduce the expression of the met receptor Cancer 2014;5:480-490.
24. Traverse JH: Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction: The time randomized trial (vol 308, pg 2380, 2012). Jama-J Am Med Assoc 2013;309:343-343.
25. Gunther C, Martini E, Wittkopf N, Amann K, Weigmann B, Neumann H, Waldner ML Hedrick SM, Tenzer 5, Neurath MF, Becker C: Caspase-8 regulates tnf-Alpha-induced epithelial necroptosis and terminal ileitis. Nature 2011;477:335-339.
26. Wang XL Kong KM, Qi WU, Ye WU, Song PS: Interleukin-1 beta induction of neuron apoptosis depends on p38 mitogen-Activated protein kinase activity after spinal cord injury. Acta Pharmacol Sinica 2005;26:934-942
27. Brucker N, Moro AM, Charao MF, Durgante J, Freitas F, Baierle M, Nascimento 5, Gauer B, Bulcao RP, Bubols GB, Ferrari PD, Thiesen FV, Gioda A, Duarte MM, de Castro L Saldiva PH, Garcia SC: Biomarkers of occupational exposure to air pollution, inflammation and oxidative damage in taxi drivers. Sci Total Environ 2013;463-464:884-893.
28. Ryan KA, Smith M Sanders MK, Ernst PB: Reactive oxygen and nitrogen species differentially regulate toll-like receptor 4-mediated activation of nf-kappa b and interleukin-8 expression. Infect Immun;2004;72;2123-2130
29. Di Stefano R, Barsotti MC, Felice F, Magera A, Lekakis J, Leone A, Balbarini A: Smoking and endothelial progenitor cells: A revision of literature. Curr Pharm Des 2 010;16 :2559-2566.
30. Haberzettl P, Lee J, Duggineni D, McCracken J, Bolanowski D, OToole TE, Bhatnagar A, Conklin DJ: Exposure to ambient air fine particulate matter prevents vegf-induced mobilization of endothelial progenitor cells from the bone marrow. Environ Health Persp 2012;120:848-856.
31. Heiss C, Amabile N, Lee AC, Real WM, Schick SF, Lao D, Wong ML Jahn 5, Angeli FS, Minasi P, Springer ML Hammond SK, Glantz SA, Grossman W, Balmes JR, Yeghiazarians Y: Brief secondhand smoke exposure depresses endothelial progenitor cells activity and endothelial function. JAm Coll Cardiol 2008;51:1760-1771.
32. Zhu EQ Heeschen C, Sievers RE, Karliner JS, Parmley WW, Glantz SA, Cooke JP: Second hand smoke stimulates tumor angiogenesis and growth. Cancer Cell 2003;4:191-196.
33. OToole TE, Hellmann L Wheat L, Haberzettl P, Lee L Conklin DL Ehatnagar A, Pope CA: Episodic exposure to fine particulate air pollution decreases circulating levels of endothelial progenitor cells. Circ Res;2010; 407; 200-203
34. Shafer MM, Perkins DA, Antkiewicz DS, Stone EA, Quraishi TA, Schauer JJ: Reactive oxygen species activity and chemical speciation of size-fractionated atmospheric particulate matter from lahore, pakistan: An important role for transition metals. Journal of environmental monitoring: JEM 201042:704-715.
35. Xiao GG, Wang MY, Li N, Loo JA, Nel AE: Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line. J Biol Chem 2003;278:50781-5 07 90.
36. Deng X, Zhang F, Wang L Rui W, Long F, Zhao Y, Chen D, Ding W: Airborne fine particulate matter induces multiple cell death pathways in human lung epithelial cells. Apoptosis 201449:1099-1112.
37. Xu Z, Xu X, Zhong M, Hotchkiss IP, Lewandowski RP, Wagner JG, Bramble LA, Yang Y, Wang A, Harkema JR, Lippmann M, Rajagopalan 5, Chen LC, Sun Q: Ambient particulate air pollution induces oxidative stress and alterations of mitochondria and gene expression in brown and white adipose tissues. Part Fibre Toxicol; 2011;8;20
38. Delfino RJ, Staimer N, Tjoa T, Gillen DL, Schauer JJ, Shafer MM: Airway inflammation and oxidative potential of air pollutant particles in a pediatric asthma panel. J Exp Sci Envir Epidem 2013;23:466-473.
39. Tonne C, Yanosky JD, Beevers 5, Wilkinson P, Kelly FJ: Pm mass concentration and pm oxidative potential in relation to carotid intima-media thickness. Epidemiology 2012;23:486-494.
40. Godri KJ, Green DC, Fuller GW, DallOsto M, Beddows DC, Kelly FL Harrison RM, Mudway IS: Particulate oxidative burden associated with firework activity. Envir Scie Technol 2010;44:8295-8301.
41. Strak M, Janssen NAH, Godri KJ, Gosens I, Mudway IS, Cassee FR, Lebret E, Kelly FL Harrison RM, Brunekreef B, Steenhof M, Hoek G: Respiratory health effects of airborne particulate matter: The role of particle size, composition, and oxidative potential-The raptes project. Environ Health Perspect;2012;420;1183-1189
42. Ardestani 5, Deskins DL, Young PP: Membrane tnf-Alpha-Activated programmed necrosis is mediated by ceramide-induced reactive oxygen species. Journal of molecular signaling 2013;8:12.
43. Mokgobu ML Cholo MC, Anderson R, Steel HC, Motheo MP, Hlatshwayo TN, Tintinger GR, Theron AJ: Oxidative induction of pro-inflammatory cytokine formation by human monocyte-derived macrophages following exposure to manganese in vitro. J Immunotoxicol 2014
44. Lee IT, Yang CM: Role of nadph oxidase/ros in pro-inflammatory mediators-induced airway and pulmonary diseases. Biochem Pharmacol 2012;84:581-590.
45. Santee SM, OwenSchaub LB: Human tumor necrosis factor receptor p75/80 (cdl2ObJ gene structure and promoter characterization. J Biol Chem 1996;271:21151-21159.
46. Koike E, Hirano 5, Furuyama A, Kobayashi T: Cdna microarray analysis of rat alveolar epithelial cells following exposure to organic extract of diesel exhaust particles. Toxicol Appl Pharm 2004;201:178-185.
47. Romieu I, Tellez-Rojo MM, Lazo M, Manzano-Patino A, Cortez-Lugo M, Julien P, Belanger MC, HernandezAvila M, Holguin F: Omega-3 fatty acid prevents heart rate variability reductions associated with particulate matter Am J Respir Critical Care Med 2005472:1534-1540.
48. Tashakkor AY, Chow KS, Carlsten C: Modification by antioxidant supplementation of changes in human lung function associated with air pollutant exposure: A systematic review. Bmc Public Health 201141:532.
49. Turgeon J, Dussault 5, Haddad P, Groleau J, Menard C, Michaud SE, Maingrette F, Rivard A: Probucol and antioxidant vitamins rescue ischemia-induced neovascularization in mice exposed to cigarette smoke: Potential role of endothelial progenitor cells. Atherosclerosis 2010; 208:342-349.