In utero and early life exposure to diesel exhaust air pollution increases adult susceptibility to heart failure in mice

Particle and Fibre Toxicology

Volumn 10, Issue 1, 2013, Pages

  Weldy, Chad S ^a   Liu, Yonggang ^a   Chang, Yu Chi ^b   Medvedev, Ivan O ^a   Fox, Julie R ^b   Larson, Timothy V ^b   Chien, Wei Ming ^a   Chin, Michael T ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Air pollution; Barker's hypothesis; Diesel exhaust; Fetal origins of adult disease; Heart failure

Indexed keywords

INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

AIR POLLUTION; AIR QUALITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE PREDISPOSITION; ECHOCARDIOGRAPHY; EXHAUST GAS; FEMALE; GENE EXPRESSION; GESTATION PERIOD; HEART FAILURE; HEART HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART VENTRICLE OVERLOAD; HISTOPATHOLOGY; LUNG CONGESTION; LUNG PARENCHYMA; MALE; MATING; MOUSE; NONHUMAN; PARTICULATE MATTER; PERINATAL PERIOD; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SYSTOLIC HEART FAILURE;

MUS;

ANIMALS; CYTOKINES; ENVIRONMENTAL EXPOSURE; FEMALE; HEART FAILURE; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; VEHICLE EMISSIONS;

EID: 84888187224     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-10-59     Document Type: Article

References (64)

1. Brook RD, Rajagopalan S, Pope CA, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, et al. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American heart association. Circulation 2010, 121:2331-2378. 10.1161/CIR.0b013e3181dbece1, 20458016.
2. Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, Amann M, Anderson HR, Andrews KG, Aryee M, et al. 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 2013, 380:2224-2260.
3. Hoek G, Krishnan RM, Beelen R, Peters A, Ostro B, Brunekreef B, Kaufman JD. Long-term air pollution exposure and cardio- respiratory mortality: a review. Environ Health 2013, 12:43. 10.1186/1476-069X-12-43, 3679821, 23714370.
4. Van Hee VC, Adar SD, Szpiro AA, Barr RG, Bluemke DA, Diez Roux AV, Gill EA, Sheppard L, Kaufman JD. Exposure to traffic and left ventricular mass and function: the multi-ethnic study of atherosclerosis. Am J Respir Crit Care Med 2009, 179:827-834. 10.1164/rccm.200808-1344OC, 2675567, 19164703.
5. Van Hee VC, Adar SD, Szpiro AA, Barr RG, Roux AD, Bluemke DA, Sheppard L, Gill EA, Bahrami H, Wassel C, et al. Common genetic variation, residential proximity to traffic exposure, and left ventricular mass: the multi-ethnic study of atherosclerosis. Environ Health Perspect 2010, 118:962-969. 10.1289/ehp.0901535, 2920916, 20308035.
6. Shah ASV, Langrish JP, Nair H, McAllister DA, Hunter AL, Donaldson K, Newby DE, MIlls NL. Global association of air pollution and heart failure: a systematic review and meta-analysis. Lancet 2013, 382:1039-1048. 10.1016/S0140-6736(13)60898-3, 3809511, 23849322.
7. Cherng TW, Campen MJ, Knuckles TL, Gonzalez Bosc L, Kanagy NL. Impairment of coronary endothelial cell ETB receptor function after short-term inhalation exposure to whole diesel emissions. Am J Physiol Regul Integr Comp Physiol 2009, 297:R640-R647. 10.1152/ajpregu.90899.2008, 2739797, 19535675.
8. Cherng TW, Paffett ML, Jackson-Weaver O, Campen MJ, Walker BR, Kanagy NL. Mechanisms of diesel-induced endothelial nitric oxide synthase dysfunction in coronary arterioles. Environ Health Perspect 2011, 119:98-103. 3018507, 20870565.
9. Knuckles TL, Lund AK, Lucas SN, Campen MJ. Diesel exhaust exposure enhances venoconstriction via uncoupling of eNOS. Toxicol Appl Pharmacol 2008, 230:346-351. 10.1016/j.taap.2008.03.010, 18455212.
10. Sun Q, Yue P, Ying Z, Cardounel AJ, Brook RD, Devlin R, Hwang J-S, Zweier JL, Chen LC, Rajagopalan S. Air pollution exposure potentiates hypertension through reactive oxygen species-mediated activation of Rho/ROCK. Arterioscler Thromb Vasc Biol 2008, 28:1760-1766. 10.1161/ATVBAHA.108.166967, 2739008, 18599801.
11. Bai N, Kido T, Kavanagh TJ, Kaufman JD, Rosenfeld ME, van Breemen C, van Eeden SF. Exposure to diesel exhaust up-regulates iNOS expression in ApoE knockout mice. Toxicol Appl Pharmacol 2011, 255:184-192. 10.1016/j.taap.2011.06.013, 21722660.
12. Bai N, Kido T, Suzuki H, Yang G, Kavanagh TJ, Kaufman JD, Rosenfeld ME, van Breemen C, van Eeden SF. Changes in atherosclerotic plaques induced by inhalation of diesel exhaust. Atherosclerosis 2011, 216:299-306. 10.1016/j.atherosclerosis.2011.02.019, 21435644.
13. Sun Q, Wang A, Jin X, Natanzon A, Duquaine D, Brook RD, Aguinaldo J-GS, Fayad ZA, Fuster V, Lippmann M, et al. Long-term air pollution exposure and acceleration of atherosclerosis and vascular inflammation in an animal model. JAMA 2005, 294:3003-3010. 10.1001/jama.294.23.3003, 16414948.
14. Quan C, Sun Q, Lippmann M, Chen L-C. Comparative effects of inhaled diesel exhaust and ambient fine particles on inflammation, atherosclerosis, and vascular dysfunction. Inhal Toxicol 2010, 22:738-753. 10.3109/08958371003728057, 3073494, 20462391.
15. Wold LE, Ying Z, Hutchinson KR, Velten M, Gorr MW, Velten C, Youtz DJ, Wang A, Lucchesi PA, Sun Q, Rajagopalan S. Cardiovascular remodeling in response to long-term exposure to fine particulate matter air pollution. Circ Heart Fail 2012, 5:452-461. 10.1161/CIRCHEARTFAILURE.112.966580, 3617499, 22661498.
16. Ying Z, Yue P, Xu X, Zhong M, Sun Q, Mikolaj M, Wang A, Brook RD, Chen LC, Rajagopalan S. Air pollution and cardiac remodeling: a role for RhoA/Rho-kinase. Am J Physiol Heart Circ Physiol 2009, 296:H1540-H1550. 10.1152/ajpheart.01270.2008, 2685340, 19286943.
17. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ (Clinical Res Ed) 1989, 298:564-567.
18. Eriksson J, Forsén T, Tuomilehto J, Osmond C, Barker D. Fetal and childhood growth and hypertension in adult life. Hypertension 2000, 36:790-794. 10.1161/01.HYP.36.5.790, 11082144.
19. Feldt K, Räikkönen K, Eriksson JG, Andersson S, Osmond C, Barker DJP, Phillips DIW, Kajantie E. Cardiovascular reactivity to psychological stressors in late adulthood is predicted by gestational age at birth. J Hum Hypertens 2007, 21:401-410.
20. Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr 2001, 4:611-624.
21. Law CM, de Swiet M, Osmond C, Fayers PM, Barker DJ, Cruddas AM, Fall CH. Initiation of hypertension in utero and its amplification throughout life. BMJ (Clin Res Ed) 1993, 306:24-27.
22. Martyn CN, Barker DJ, Jespersen S, Greenwald S, Osmond C, Berry C. Growth in utero, adult blood pressure, and arterial compliance. Br Heart J 1995, 73:116-121. 10.1136/hrt.73.2.116, 483775, 7696018.
23. Vijayakumar M, Fall CH, Osmond C, Barker DJ. Birth weight, weight at one year, and left ventricular mass in adult life. Br Heart J 1995, 73:363-367. 10.1136/hrt.73.4.363, 483831, 7756071.
24. Dadvand P, Parker J, Bell ML, Bonzini M, Brauer M, Darrow LA, Gehring U, Glinianaia SV, Gouveia N, Ha E-H, et al. Maternal exposure to particulate air pollution and term birth weight: a multi-country evaluation of effect and heterogeneity. Environ Health Perspect 2013, 121:267-373. 10.1289/ehp.1205575, 3621183, 23384584.
25. Lewtas J. Air pollution combustion emissions: characterization of causative agents and mechanisms associated with cancer, reproductive, and cardiovascular effects. Mutat Res 2007, 636:95-133. 10.1016/j.mrrev.2007.08.003, 17951105.
26. Auten RL, Gilmour MI, Krantz QT, Potts EN, Mason SN, Foster WM. Maternal diesel inhalation increases airway hyperreactivity in ozone-exposed offspring. Am J Respir Cell Mol Biol 2012, 46:454-460. 10.1165/rcmb.2011-0256OC, 3359947, 22052876.
27. Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, Auten RL, Bilbo SD. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J 2012, 26:4743-4754. 10.1096/fj.12-210989, 22815382.
28. Campen MJ, Lund AK, Knuckles TL, Conklin DJ, Bishop B, Young D, Seilkop S, Seagrave J, Reed MD, Mcdonald JD. Inhaled diesel emissions alter atherosclerotic plaque composition in ApoE(-/-) mice. Toxicol Appl Pharmacol 2010, 242:310-317. 10.1016/j.taap.2009.10.021, 2813974, 19891982.
29. Wang J-F, Hu M-G, Xu C-D, Christakos G, Zhao Y. Estimation of citywide air pollution in Beijing. PloS one 2013, 8:e53400. 10.1371/journal.pone.0053400, 3539974, 23320082.
30. Miller KA, Siscovick DS, Sheppard L, Shepherd K, Sullivan JH, Anderson GL, Kaufman JD. Long-term exposure to air pollution and incidence of cardiovascular events in women. N Engl J Med 2007, 356:447-458. 10.1056/NEJMoa054409, 17267905.
31. Mills NL, Törnqvist H, Gonzalez MC, Vink E, Robinson SD, Söderberg S, Boon NA, Donaldson K, Sandström T, Blomberg A, Newby DE. Ischemic and thrombotic effects of dilute diesel-exhaust inhalation in men with coronary heart disease. N Engl J Med 2007, 357:1075-1082. 10.1056/NEJMoa066314, 17855668.
32. Mills NL, Törnqvist H, Robinson SD, Gonzalez M, Darnley K, MacNee W, Boon NA, Donaldson K, Blomberg A, Sandstrom T, Newby DE. Diesel exhaust inhalation causes vascular dysfunction and impaired endogenous fibrinolysis. Circulation 2005, 112:3930-3936. 10.1161/CIRCULATIONAHA.105.588962, 16365212.
33. Arck PC, Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nature medicine 2013, 19:548-556.
34. Ward JM, Elmore SA, Foley JF. Pathology methods for the evaluation of embryonic and perinatal developmental defects and lethality in genetically engineered mice. Vet Pathol 2012, 49:71-84. 10.1177/0300985811429811, 22146849.
35. Auten RL, Potts EN, Mason SN, Fischer B, Huang Y, Foster WM. Maternal exposure to particulate matter increases postnatal ozone-induced airway hyperreactivity in juvenile mice. Am J Respir Crit Care Med 2009, 180:1218-1226. 10.1164/rccm.200901-0116OC, 2796733, 19762564.
36. Janssen BG, Munters E, Pieters N, Smeets K, Cox B, Cuypers A, Fierens F, Penders J, Vangronsveld J, Gyselaers W, Nawrot TS. Placental mitochondrial DNA content and particulate air pollution during in utero life. Environ Health Perspect 2012, 120:1346-1352. 10.1289/ehp.1104458, 3440109, 22626541.
37. Janssen BG, Godderis L, Pieters N, Poels K, Kici Ski M, Cuypers A, Fierens F, Penders J, Plusquin M, Gyselaers W, Nawrot TS. Placental DNA hypomethylation in association with particulate air pollution in early life. Part Fibre Toxicol 2013, 10:22. 10.1186/1743-8977-10-22, 3686623, 23742113.
38. Andersen KV, Hermann N. Placenta flow reduction in pregnant smokers. Acta Obstet Gynecol Scand 1984, 63:707-709. 10.3109/00016348409154668, 6524306.
39. Burton GJ, Palmer ME, Dalton KJ. Morphometric differences between the placental vasculature of non-smokers, smokers and ex-smokers. Br J Obstet Gynaecol 1989, 96:907-915. 10.1111/j.1471-0528.1989.tb03344.x, 2775688.
40. Demir R, Demir AY, Yinanc M. Structural changes in placental barrier of smoking mother. A quantitative and ultrastructural study. Pathol Res Pract 1994, 190:656-667. 10.1016/S0344-0338(11)80744-2, 7808964.
41. Larsen LG, Clausen HV, Jønsson L. Stereologic examination of placentas from mothers who smoke during pregnancy. Am J Obstet Gynecol 2002, 186:531-537. 10.1067/mob.2002.120481, 11904619.
42. MacLennan NK, James SJ, Melnyk S, Piroozi A, Jernigan S, Hsu JL, Janke SM, Pham TD, Lane RH. Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol Genomics 2004, 18:43-50. 10.1152/physiolgenomics.00042.2004, 15084713.
43. Bussey ME, Finley S, LaBarbera A, Ogata ES. Hypoglycemia in the newborn growth-retarded rat: delayed phosphoenolpyruvate carboxykinase induction despite increased glucagon availability. Pediatr Res 1985, 19:363-367. 10.1203/00006450-198519040-00010, 3889814.
44. Economides DL, Nicolaides KH. Blood glucose and oxygen tension levels in small-for-gestational-age fetuses. Am J Obstet Gynecol 1989, 160:385-389. 10.1016/0002-9378(89)90453-5, 2916623.
45. Economides DL, Nicolaides KH, Gahl WA, Bernardini I, Bottoms S, Evans M. Cordocentesis in the diagnosis of intrauterine starvation. Am J Obstet Gynecol 1989, 161:1004-1008. 10.1016/0002-9378(89)90772-2, 2679098.
46. Ogata ES, Bussey ME, Finley S. Altered gas exchange, limited glucose and branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism 1986, 35:970-977. 10.1016/0026-0495(86)90064-8, 3531762.
47. Ogata ES, Bussey ME, LaBarbera A, Finley S. Altered growth, hypoglycemia, hypoalaninemia, and ketonemia in the young rat: postnatal consequences of intrauterine growth retardation. Pediatr Res 1985, 19:32-37. 10.1203/00006450-198501000-00010, 3881726.
48. Lane RH, Kelley DE, Ritov VH, Tsirka AE, Gruetzmacher EM. Altered expression and function of mitochondrial beta-oxidation enzymes in juvenile intrauterine-growth-retarded rat skeletal muscle. Pediatr Res 2001, 50:83-90. 10.1203/00006450-200107000-00016, 11420423.
49. Lane RH, Kelley DE, Gruetzmacher EM, Devaskar SU. Uteroplacental insufficiency alters hepatic fatty acid-metabolizing enzymes in juvenile and adult rats. Am J Physiol Regul Integr Comp Physiol 2001, 280:R183-R190.
50. Bagley HN, Wang Y, Campbell MS, Yu X, Lane RH, Joss-Moore LA. Maternal docosahexaenoic acid increases adiponectin and normalizes IUGR-induced changes in rat adipose deposition. J Obes 2013, 2013:312153. 3606778, 23533720.
51. Tsirka AE, Gruetzmacher EM, Kelley DE, Ritov VH, Devaskar SU, Lane RH. Myocardial gene expression of glucose transporter 1 and glucose transporter 4 in response to uteroplacental insufficiency in the rat. J Endocrinol 2001, 169:373-380. 10.1677/joe.0.1690373, 11312153.
52. Ke X, Lei Q, James SJ, Kelleher SL, Melnyk S, Jernigan S, Yu X, Wang L, Callaway CW, Gill G, et al. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics 2006, 25:16-28. 10.1152/physiolgenomics.00093.2005, 16380407.
53. Patterson AJ, Chen M, Xue Q, Xiao D, Zhang L. Chronic prenatal hypoxia induces epigenetic programming of PKC{epsilon} gene repression in rat hearts. Circ Res 2010, 107:365-373. 10.1161/CIRCRESAHA.110.221259, 2919213, 20538683.
54. Patterson AJ, Xiao D, Xiong F, Dixon B, Zhang L. Hypoxia-derived oxidative stress mediates epigenetic repression of PKCε{lunate} gene in foetal rat hearts. Cardiovasc Res 2012, 93:302-310. 10.1093/cvr/cvr322, 3258654, 22139554.
55. Proietti E, Röösli M, Frey U, Latzin P. Air pollution during pregnancy and neonatal outcome: a review. J Aerosol Med Pulm Drug Deliv 2013, 26:9-23. 10.1089/jamp.2011.0932, 22856675.
56. Gauderman WJ, Avol E, Gilliland F, Vora H, Thomas D, Berhane K, McConnell R, Kuenzli N, Lurmann F, Rappaport E, et al. The effect of air pollution on lung development from 10 to 18 years of age. N Engl J Med 2004, 351:1057-1067. 10.1056/NEJMoa040610, 15356303.
57. Van Eeden S, Leipsic J, Paul Man SF, Sin DD. The relationship between lung inflammation and cardiovascular disease. Am J Respir Crit Care Med 2012, 186:11-16. 10.1164/rccm.201203-0455PP, 22538803.
58. Liu Y, Chien W-M, Medvedev IO, Weldy CS, Luchtel DL, Rosenfeld ME, Chin MT. Inhalation of diesel exhaust does not exacerbate cardiac hypertrophy or heart failure in two mouse models of cardiac hypertrophy. Part Fibre Toxicol 2013, 10:49. 10.1186/1743-8977-10-49, 24093778.
59. Gould T, Larson T, Stewart J, Kaufman JD, Slater D, Mcewen N. A controlled inhalation diesel exhaust exposure facility with dynamic feedback control of PM concentration. Inhal Toxicol 2008, 20:49-52. 10.1080/08958370701758478, 18236222.
60. Weldy CS, Luttrell IP, White CC, Morgan-Stevenson V, Cox DP, Carosino CM, Larson TV, Stewart JA, Kaufman JD, Kim F, et al. Glutathione (GSH) and the GSH synthesis gene Gclm modulate plasma redox and vascular responses to acute diesel exhaust inhalation in mice. Inhal Toxicol 2013, 25:444-454. 10.3109/08958378.2013.801004, 23808636.
61. Yin F, Lawal A, Ricks J, Fox JR, Larson T, Navab M, Fogelman AM, Rosenfeld ME, Araujo JA. Diesel exhaust induces systemic lipid peroxidation and development of dysfunctional pro-oxidant and pro-inflammatory high-density lipoprotein. Arterioscler Thromb Vasc Biol 2013, 33:1153-1161. 10.1161/ATVBAHA.112.300552, 23559632.
62. Liu Y, Yu M, Wu L, Chin MT. The bHLH transcription factor CHF1/Hey2 regulates susceptibility to apoptosis and heart failure after pressure overload. Am J Physiol Heart Circ Physiol 2010, 298:H2082-H2092. 10.1152/ajpheart.00747.2009, 2886641, 20382855.
63. Yu M, Liu Y, Xiang F, Li Y, Cullen D, Liao R, Beyer RP, Bammler TK, Chin MT. CHF1/Hey2 promotes physiological hypertrophy in response to pressure overload through selective repression and activation of specific transcriptional pathways. OMICS 2009, 13:501-511. 10.1089/omi.2009.0086, 3145963, 20001863.
64. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif) 2001, 25:402-408.