Foetal nicotine exposure causes PKCε gene repression by promoter methylation in rat hearts

Cardiovascular Research

Volumn 89, Issue 1, 2011, Pages 89-97

  Lawrence, Jennifer ^a   Chen, Man ^a   Xiong, Fuxia ^a   Xiao, Daliao ^a   Zhang, Haitao ^a   Buchholz, John N ^a   Zhang, Lubo ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA methylation; Heart; Nicotine; Norepinephrine; Protein kinase C

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; EARLY GROWTH RESPONSE FACTOR 1; MESSENGER RNA; NICOTINE; NORADRENALIN; PROTEIN KINASE C EPSILON;

ADRENERGIC TRANSMISSION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; EX VIVO STUDY; FEMALE; FETUS; FETUS HEART; GENE EXPRESSION; GENE REPRESSION; GESTATIONAL AGE; HYPOTHESIS; ISOLATED HEART; MALE; MATERNAL SMOKING; NONHUMAN; NORADRENALIN BLOOD LEVEL; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; PROTEIN METHYLATION; RAT;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; DNA METHYLATION; DNA PRIMERS; EARLY GROWTH RESPONSE PROTEIN 1; FEMALE; GENE EXPRESSION; HEART; MYOCARDIUM; NICOTINE; NOREPINEPHRINE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 78650479537     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq270     Document Type: Article

References (50)

1. Slotkin TA. Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther 1998;285:931-945.
2. Beratis NG, Panagoulias D, Varvarigou A. Increased blood pressure in neonates and infants whose mothers smoked during pregnancy. J Pediatr 1996;128:806-812.
3. Blake KV, Gurrin LC, Evans SF, Beilin LJ, Landau LI, Stanley FJ et al. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev 2000;57:137-147.
4. Xiao D, Huang X, Lawrence J, Yang S, Zhang L. Fetal and neonatal nicotine exposure differentially regulates vascular contractility in adult male and female offspring. J Pharmacol Exp Ther 2007;320:654-661.
5. Lawrence J, Xiao D, Xue Q, Rejali M, Yang S, Zhang L. Prenatal nicotine exposure increases heart susceptibility to ischemia/reperfusion injury in adult offspring. J Pharmacol Exp Ther 2008;324:331-341. (Pubitemid 350294154)
6. Xiao D, Xu Z, Huang X, Longo LD, Yang S, Zhang L. Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension 2008;51:1239-1247. (Pubitemid 351398971)
7. Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986;1:1077-1081.
8. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA et al. Developmental plasticity and human health. Nature 2004;430:419-421.
9. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008;359:61-73.
10. Xue Q, Zhang L. Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: Role of PKC1. J Pharmacol Exp Ther 2009;330:624-632.
11. Meyer K, Zhang H, Zhang L. Prenatal cocaine exposure abolished ischemic preconditioning-induced protection in adult male rat hearts: role of PKC1. Am J Physiol Heart Circ Physiol 2009;296:H1566-H1576.
12. Patterson AJ, Chen M, Xue Q, Xiao D, Zhang L. Chronic hypoxia induces epigenetic programming of PKC1 gene repression in fetal rat heart. Circ Res 2010; [Epub ahead of print, 10 June].
13. Chen L, Hahn H, Wu G, Chen CH, Liron T, Schechtman D et al. Opposing cardio-protective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci USA 2001;98:11114-11119.
14. Ping P, Zhang J, Pierce WM Jr, Bolli R. Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ Res 2001;88:59-62.
15. Murriel CL, Mochly-Rosen D. Opposing roles of delta and epsilonPKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch Biochem Biophys 2003;420:246-254.
16. Gray MO, Zhou HZ, Schafhalter-Zoppoth I, Zhu P, Mochly-Rosen D, Messing RO. Preservation of base-line hemodynamic function and loss of inducible cardioprotec-tion in adult mice lacking protein kinase C epsilon. J Biol Chem 2004;279:3596-3604.
17. Bogdarina I, Welham S, King PJ, Burns SP, Clark AJL. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ Res 2007; 100:520-526.
18. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001;293:1068-1070.
19. Jones PA, Laird PW. Cancer epigenetics comes of age. Nat Genet 1999;21:163-167.
20. Wade PA. Methyl CpG-binding proteins and transcriptional repression. Bioessays 2001;23:1131-1137.
21. Campanero MR, Armstrong MI, Flemington EK. CpG methylation as a mechanism for the regulation of E2F activity. Proc Natl Acad Sci USA 2000;97:6481-6486.
22. Zhu WG, Srinivasan K, Dai Z, Duan W, Druhan LJ, Ding H et al. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21Cip1 promoter. Mol Cell Biol 2003;23:4056-4065.
23. Fujimoto M, Kitazawa R, Maeda S, Kitazawa S. Methylation adjacent to negatively regulating AP-1 site reactivates TrkA gene expression during cancer progression. Onco-gene 2005;24:5108-5118.
24. Meyer K, Zhang H, Zhang L. Direct effect of cocaine on epigenetic regulation of PKCepsilon gene repression in the fetal rat heart. J Mol Cell Cardiol 2009;47:504-511.
25. Zhang H, Meyer KD, Zhang L. Fetal exposure to cocaine causes programming of prkce gene repression in the left ventricle of adult rat offspring. Biol Reprod 2009; 80:440-448.
26. Li Z, Barrios V, Buchholz JN, Glenn TC, Duckles SP. Chronic nicotine administration does not affect peripheral vascular reactivity in the rat. J Pharmacol Exp Ther 1994;271: 1135-1142.
27. Figliola R, Busanello A, Vaccarello G, Maione R. Regulation of p57KIP2 during muscle differentiation: role of Egr1, Sp1 and DNA hypomethylation. J Mol Biol 2008;380: 265-277.
28. Lambers DS, Clark KE. The maternal and fetal physiologic effects of nicotine. Semin Perinatol 1996;20:115-126.
29. Koren G. Fetal toxicology of environmental tobacco smoke. Curr Opin Pediatr 1995;7: 128-131.
30. Onal A, Uysal A, Ulker S, Delen Y, Yurtseven ME, Evinç A. Alterations of brain tissue in fetal rats exposed to nicotine in utero: possible involvement of nitric oxide and cat-echolamines. Neurotoxicol Teratol 2004;26:103-112.
31. Greenberg RE, Lind J. Catecholamines in tissues of the human fetus. Pediatrics 1961; 27:904-911.
32. Wehrwein EA, Parker LM, Wright AA, Spitsbergen JM, Novotny M, Babankova D et al. Cardiac norepinephrine transporter protein expression is inversely correlated to chamber norepinephrine content. Am J Physiol Regul Integr Comp Physiol 2008; 295:R857-R863.
33. Giussani DA, Gardner DS, Cox DT, Fletcher AJ. Purinergic contribution to circulatory, metabolic, and adrenergic responses to acute hypoxemia in fetal sheep. Am J Physiol Regul Integr Comp Physiol 2001;280:R678-R685.
34. Gagnon R, Murotsuki J, Challis JR, Fraher L, Richardson BS. Fetal sheep endocrine responses to sustained hypoxemic stress after chronic fetal placental embolization. Am J Physiol 1997;272:E817-E823.
35. Compere SJ, Palmiter RD. DNA methylation controls the inducibility of the mouse metallothionein-I gene in lymphoid cells. Cancer Cell 1980;25:233-240.
36. ′-deoxycytidine. Mol Cancer Ther 2005;4:1515-1520.
37. ′-deoxycytidine. Cancer Res 2002;62: 6456-6461.
38. ′-deoxycytidine suppresses the growth of human tumor cell lines. Cancer Res 1998;58:95-101.
39. Lee BH, Yegnasubramanian S, Lin X, Nelson WG. Procainamide is a specific inhibitor of DNA methyltransferase 1. J Biol Chem 2005;280:40749-40756.
40. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 2008;135:2128-2140. 2140 e2121-2128.
41. Franco R, Schoneveld O, Georgakilas AG, Panayiotidis MI. Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett 2008;266:6-11.
42. Min JY, Lim SO, Jung G. Downregulation of catalase by reactive oxygen species via hypermethylation of CpG island II on the catalase promoter. FEBS Lett 2010;584: 2427-2432.
43. Fu YC, Chi CS, Yin SC, Hwang B, Chiu YT, Hsu SL. Norepinephrine induces apoptosis in neonatal rat cardiomyocytes through a reactive oxygen species-TNF alpha-caspase signaling pathway. Cardiovasc Res 2004;62:558-567.
44. Kuster GM, Pimentel DR, Adachi T, Ido Y, Brenner DA, Cohen RA et al. Alpha-adrenergic receptor-stimulated hypertrophy in adult rat ventricular myocytes is mediated via thioredoxin-1-sensitive oxidative modification of thiols on Ras. Circulation 2005;111:1192-1198.
45. Amin JK, Xiao L, Pimental DR, Pagano PJ, Singh K, Sawyer DB et al. Reactive oxygen species mediate alpha-adrenergic receptor-stimulated hypertrophy in adult rat ventricular myocytes. J Mol Cell Cardiol 2001;33:131-139. (Pubitemid 32127790)
46. Xiao L, Pimentel DR, Wang J, Singh K, Colucci WS, Sawyer DB. Role of reactive oxygen species and NAD(P)H oxidase in alpha(1)-adrenoceptor signaling in adult rat cardiac myocytes. Am J Physiol Cell Physiol 2002;282:C926-C934.
47. Bae S, Gilbert RD, Ducsay CA, Zhang L. Prenatal cocaine exposure increases heart susceptibility to ischemia/reperfusion injury in adult male but not female rats. J Physiol 2005;565:149-158. (Pubitemid 40723698)
48. Do Carmo Pinho Franco M, Nigro D, Fortes ZB, Tostes RC, Carvalho MH, Lucas SR et al. Intrauterine undernutrition-renal and vascular origin of hypertension. Cardio-vasc Res 2003;60:228-234.
49. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005;85:571-633.
50. Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G et al. Mechanisms of estrogen action. Physiol Rev 2001;81:1535-1565.