Prenatal environmental tobacco smoke exposure promotes adult atherogenesis and mitochondrial damage in apolipoprotein E-/- mice fed a chow diet

Circulation

Volumn 110, Issue 24, 2004, Pages 3715-3720

  Yang, Zhen ^a   Knight, Cynthia A ^a   Mamerow, Madonna M ^c   Vickers, Kasey ^a   Penn, Arthur ^d   Postlethwait, Edward M ^b   Ballinger, Scott W ^a,e  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d LOUISIANA STATE UNIVERSITY   (United States)

^e Department of Pathology   (United States)

Author keywords

Atherosclerosis; Mitochondria; Pregnancy; Prenatal exposure delayed effects; Smoking

Indexed keywords

ACONITATE HYDRATASE; APOLIPOPROTEIN E; FUMARATE HYDRATASE; SUPEROXIDE DISMUTASE; TOBACCO SMOKE;

ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ATHEROGENESIS; CELL DAMAGE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HYPERLIPOPROTEINEMIA TYPE 3; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; WEANING;

ANIMALS; ANTIOXIDANTS; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; DIETARY FATS; FEMALE; MALE; MICE; MITOCHONDRIA; OXIDANTS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; TOBACCO SMOKE POLLUTION;

EID: 10844232037     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000149747.82157.01     Document Type: Article

References (60)

1. Barker D. Fetal origins of coronary heart disease. BMJ. 1995;311:171-174.
2. Palinski W, D'Armiento FP, Witztum JL, de Nigris F, Casanada F, Condorelli M, Silvestre M, Napoli C. Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ Res. 2001;89:991-996.
3. Napoli C, Glass CK, Witztum JL, Deutsch R, D'Armiento FP, Palinski W. Influence of maternal hypercholesterolemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet. 1999;354:1234-1241.
4. Napoli C, D'Armiento FP, Mancini FP, Postiglione A, Witztum JL, Palumbo G, Palinski W. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. J Clin Invest. 1997;100:2680-2690.
5. Napoli C, de Nigris F, Welch JS, Calara FB, Stuart RO, Glass CK, Palinski W. Maternal hypercholesterolemia during pregnancy promotes early atherogenesis in LDL receptor-deficient mice and alters aortic gene expression determined by microarray. Circulation. 2002;105:1360-1367.
6. Napoli C, Witztum JL, Calara FB, de Nigris F, Palinski W. Maternal hypercholesterolemia enhances atherogenesis in normocholesterolemic rabbits, which is inhibited by antioxidant or lipid-lowering intervention during pregnancy. Circ Res. 2000;87:946-952.
7. Godfrey K, Barker D. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71:1344S-1352S.
8. Witschi H, Joad JP, Pinkerton K. The toxicology of environmental tobacco smoke. Annu Rev Pharmacol Toxicol. 1997;37:29-52.
9. Cunningham J, Dockery DW, Speizer FE. Maternal smoking during pregnancy as a predictor of lung function in children. Am J Epidemiol. 1994;139:1139-1152.
10. Taylor AE, Johnson DC, Kazemi H. Environmental tobacco smoke and cardiovascular disease. Circulation. 1992;86:1-4.
11. Glantz S, Parmley W. Passive smoking and heart disease: epidemiology, physiology, and biochemistry. Circulation. 1991;83:1-12.
12. Glantz S, Parmley W. Passive smoking and heart disease. JAMA. 1995;273:1047-1053.
13. Steenland K. Passive smoking and the risk of heart disease. JAMA. 1992;267:94-99.
14. Steenland K, Thun M, Lally C, Heath C. Environmental tobacco smoke and coronary heart disease in the American Cancer Society CPS-II cohort. Circulation. 1996;94:622-628.
15. Wells AJ. Heart disease from passive smoking in the workplace. J Am Coll Cardiol. 1998;31:1-9.
16. Kawachi I, Colditz G, Speizer FE, Manson J, Stampfer M, Willet W, Hennekens C. A prospective study of passive smoking and coronary heart disease. Circulation. 1997;95:2374-2379.
17. American Heart Association. 2000 Heart and Stroke Statistical Update. Dallas, Tex: American Heart Association; 1999:1-29.
18. Davis J, Shelton L, Watnabe I, Arnold J. Passive smoking affects endothelium and platelets. Arch Intern Med. 1989;149:386-389.
19. Knight-Lozano CA, Young CG, Burow DL, Hu Z, Uyeminami D, Pinkerton K, Ischiropoulos H, Ballinger SW. Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues. Circulation. 2002;105:849-854.
20. Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking apoE: evaluation of lesional development and progression. Arterioscler Thromb. 1994;14:141-147.
21. Hausladen A, Fridovich I. Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Methods Enzymol. 1996;269:37-41.
22. Flohe L, Otting F. Superoxide dismutase assays. Methods Enzymol. 1984;105:93-104.
23. Calleja L, Paris M, Paul A, Vilella E, Joven J, Jimenez A, Beltran G, Uceda M, Maeda N, Osada J. Low cholesterol and high fat diets reduce atherosclerotic lesion development in apoE knockout mice. Arterioscler Thromb Vasc Biol. 1999;19:2368-2375.
24. Bourassa P, Milos P, Gaynor B, Breslow J, Aiello R. Estrogen reduces atherosclerotic lesion development in apolipoprolein E deficient mice. Proc Natl Acad Sci USA. 1996;93:10022-10027.
25. -/- mice. Atherosclerosis. 2001;156:49-55.
26. Ronchetti R, Bonci E, Cutrera R, De Castro G, Indinnimeo L, Midulla F, Tancredi G, Martinez F. Enhanced allergic sensitization related to parental smoking. Arch Dis Child. 1992;67:496-500.
27. Tangirala RK, Rubin EM, Palinski W. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apolipoprotein E-deficient mice. J Lipid Res. 1995; 36:2320-2328.
28. American Heart Association. Heart Disease and Stroke Statistics: 2003 Update. Dallas, Tex: American Heart Association; 2002:25-27.
29. Rubin D, Krasilnikoff P, Levanthai J, Weile B, Berget A. Effect of passive smoking on birth-weight. Lancet. 1986;2:415-417.
30. Martinez F, Antognoni G, Macri F, Bonci E, Midulla F, De Castro G, Ronchetti R. Parental smoking enhances bronchial responsiveness in nine-year-old children. Am Rev Respir Dis. 1988;138:518-523.
31. Hanrahan JP, Tager IB, Segal MR, Tosteson TD, Castile RG, Van Vunakis H, Weiss ST, Speizer FE. The effect of maternal smoking during pregnancy on early infant lung function. Am Rev Respir Dis. 1992;145:1129-1135.
32. Chen Y. Environmental tobacco smoke, low birth weight, and hospitalization for respiratory disease. Am J Respir Crit Care Med. 1994;150:54-58.
33. Asmussen I. Ultrastructure of human umbilical arteries from newborn children of smoking and non-smoking mothers. Acta Pathol Microbiol Immunol Scand [A]. 1982;90:375-383.
34. Guyer B, Hoyert DL, Martin JC, Ventura SJ, MacDorman MF, Strobino DM. Annual summary of statistics: 1998. Pediatrics. 1999;104:1229-1246.
35. Mulcahy R. Effect of age, parity, and cigarette smoking on outcome of pregnancy. Am J Obstet Gynecol. 1968;101:844-849.
36. Butler N, Goldstein H, Ross E. Cigarette smoking in pregnancy: its influence on birth weight and perinatal mortality. BMJ. 1972;806:127-130.
37. van der Velde W, Treffers P. Smoking in pregnancy: the influence on percentile birth weight, mean birth weight, placental weight, menstrual age, perinatal mortality and maternal diastolic blood pressure. Gynecol Obstet Invest. 1985;19:57-63.
38. Wang X, Tager I, van Vunakis H, Speizer F, Hanrahan J. Maternal smoking during pregnancy, urine cotinine concentrations, and birth outcomes. Int J Epidemol. 1997;26:978-988.
39. England L, Kendrick J, Gargiullo P, Zahniser S, Hannon W. Measures of maternal tobacco exposure and infant birth weight at term. Am J Epidemol. 2001;153:954-960.
40. Power C, Jefferis B. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemol. 2002;31:413-419.
41. van der Meulen J. Maternal smoking during pregnancy and obesity in the offspring. Int J Epidemol. 2002;31:420-421.
42. von Kries R, Toschke A, Koletzko B, Slikker W. Maternal smoking during pregnancy and childhood obesity. Am J Epidemol. 2002;156:954-961.
43. Iscan A, Yigitoglu R, Ece A, Ari Z, Akyildiz M. The effect of cigarette smoking during pregnancy on cord blood lipid, lipoprotein and apolipoprotein levels. Jpn Heart J. 1997;38:497-502.
44. Metcoff J, Costiloe P, Crosby WM, Sandstead HH, Milne D. Smoking in pregnancy: relation of birth weight to maternal plasma carotene and cholesterol levels. Obstet Gynecol. 1989;74:302-309.
45. Agostini C, Marangoni F, Grandi F, Lammardo AM, Giovannini M, Riva E, Galli C. Earlier smoking habits are associated with higher serum lipids and lower milk fat and polyunsaturated fatty acid content in the first 6 months of lactation. Ear J Clin Nutr. 2003;57:1466-1472.
46. Adam B, Cetinkaya F, Malatyalioglu E, Gurses N. Cigarette smoking and lipids and lipoproteins in cord plasma. Jpn Heart J. 1993;34:759-762.
47. 32P-postlabeling assay in mice of transplacental DNA damage induced by the environmental carcinogens safrole, 4-aminobiphenyl, and benzo(a)pyrene. Cancer Res. 1986;46:3046-3054.
48. Bandy B, Davison AJ. Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radic Biol Med. 1990;8:523-539.
49. Ballinger SW, Bouder TG, Davis GS, Judice SA, Nicklas JA, Albertini RJ. Mitochondrial genome damage associated with cigarette smoking. Cancer Res. 1996;56:5692-5697.
50. Jones DP, Lash LH. Criteria for assessing normal and abnormal mitochondrial function. In: Lash LH, Jones DP, eds. Methods in Toxicology: Mitochondrial Dysfunction. San Diego, Calif: Academic Press; 1993:1-7.
51. Couch NP. On the arterial consequences of smoking. J Vasc Surg. 1986;3:807-812.
52. Asmussen I, Kjeldsen K. Intimai ultrastructure of human umbilical arteries. Circ Res. 1975;36:579-589.
53. Gerschenson M, Erhart S, Paik C, St Claire M, Nagashima K, Skopets B, Harbaugh S, Harbaugh J, Quan W, Poirier M. Fetal mitochondrial heart and skeletal muscle damage in Erythrocebus patas monkeys exposed in utero to 3-azido-3-deoxythymidine. AIDS Res Hum Retroviruses. 2000;16:635-644.
54. Bialkowska A, Bialkowski K, Gerschenson M, Diwan B, Jones A, Olivero O, Poirier M, Anderson L, Kasprzak K, Sipowicz M. Oxidative DNA damage in fetal tissues after transplacental exposure to 3-azido-3-deoxythymidine (AZT). Carcinogenesis. 2000;21:1059-1062.
55. Radi R, Rodriguez M, Castro L, Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys. 1994;308:89-95.
56. Cassina A, Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys. 1996;328:309-316.
57. Gow A, Duran D, Thom S, Ischiropoulos H. Carbon dioxide enhancement of peroxynitrite mediated protein tyrosine nitration. Arch Biochem Biophys. 1996;333:42-48.
58. MacMillan-Crow LA, Crow JP, Thompson JA. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical gyrosine residues. Biochemistry. 1998;37:1613-1622.
59. Ballinger SW, Patterson WC, Yan C-N, Doan R, Burow DL, Young CG, Yakes FM, Van Houten B, Ballinger CA, Freeman BA, Runge MS. Hydrogen peroxide and peroxynitrite induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ Res. 2000;86:960-966.
60. Ballinger SW, Patterson C, Knight-Lozano CA, Burow DL, Conklin CA, Hu Z, Reuf J, Horaist C, Lebovitz RM, Hunter GC, McIntyre K, Runge MS. Mitochondrial integrity and function in atherogenesis. Circulation. 2002;106:544-549.