Maternal cocaine administration causes an epigenetic modification of protein kinase Cε gene expression in fetal rat heart

Molecular Pharmacology

Volumn 71, Issue 5, 2007, Pages 1319-1328

  Zhang, Haitao ^a   Darwanto, Agus ^a   Linkhart, Thomas A ^a,b   Sowers, Lawrence C ^a   Zhang, Lubo ^a  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; MESSENGER RNA; PROTEIN C JUN; PROTEIN KINASE C EPSILON; SODIUM CHLORIDE; TRANSCRIPTION FACTOR AP 1;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; DNA METHYLATION; DOSE RESPONSE; DRUG MECHANISM; EPIGENETICS; FEMALE; FETUS HEART; GENE EXPRESSION; GESTATIONAL AGE; HEART MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT;

ANIMALS; BASE SEQUENCE; BINDING SITES; COCAINE; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPIGENESIS, GENETIC; FEMALE; FETAL HEART; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MATERNAL EXPOSURE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PREGNANCY; PROMOTER REGIONS (GENETICS); PROTEIN KINASE C-EPSILON; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTOR AP-1;

EID: 34247467479     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.106.032011     Document Type: Article

References (48)

1. Alikhani-Koopaei R, Fouladkou F, Frey FJ, and Frey BM (2004) Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression. J Clin Investig 114:1146-1157.
2. Bae S, Gilbert RD, Ducsay CA, and Zhang L (2005) Prenatal cocaine exposure increases heart susceptibility to ischemia/reperfusion injury in adult male but not female rats. J Physiol 565.1:149-158.
3. Bae S and Zhang L (2005a) Gender differences in cardioprotection against ischemia/reperfusion injury in adult rat hearts. J Pharmacol Exp Ther 315:1125-1135.
4. Bae S and Zhang L (2005b) Prenatal cocaine exposure increases apoptosis of neonatal rat heart and heart susceptibility to ischemia/reperfusion injury in one-month-old rat. Br J Pharmacol 144:900-907.
5. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, and Robinson JS (1993) Fetal nutrition and cardiovascular disease in adult life. Lancet 341:938-941.
6. Bogoyevitch MA, Parker PJ, and Sugden PH (1993) Characterization of protein kinase C isotype expression in adult rat heart. Protein kinase C-epsilon is a major isotype present, and it is activated by phorbol esters, epinephrine, and endothelin. Circ Res 72:757-767.
7. Campanero MR, Armstrong MI, and Flemington EK (2000) CpG methylation as a mechanism for the regulation of E2F activity. Proc Natl Acad Sci USA 97:481-6486.
8. Chen L, Hahn H, Wu G, Chen CH, Liron T, Schechtman D, Cavallaro G, Banci L, Guo Y, Bolli R, et al. (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci USA 98:11114-11119.
9. Dong Z, Wang X, and Evers BM (2000) Site-specific DNA methylation contributes to neurotensin/neuromedin N expression in colon cancers. Am J Physiol 279:G1139-G1147.
10. Fackler MJ, McVeigh M, Mehrotra J, Blum MA, Lange J, Lapides A, Garrett E, Argani P, and Sukumar S (2004) Quantitative multiplex methylation-specific PCR assay for the detection of promoter hypermethylation in multiple genes in breast cancer. Cancer Res 64:4442-4452.
11. Frassica JJ, Orav EJ, Walsh EP, and Lipshultz SE (1994) Arrhythmias in children prenatally exposed to cocaine. Arch Pediatr Adolesc Med 148:1163-1169.
12. Fujimoto M, Kitazawa R, Maeda S, and Kitazawa S (2005) Methylation adjacent to negatively regulating AP-1 site reactivates TrkA gene expression during cancer progression. Oncogene 24:5108-5118.
13. Gray MO, Zhou HZ, Schafhalter-Zoppoth I, Zhu P, Mochly-Rosen D, and Messing RO (2004) Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase Cε. J Biol Chem 279:3596-3604.
14. Heidcamp MC, Bayer AL, Martin JL, and Samarel AM (2001) Differential activation of mitogen-activated protein kinase cascades and apoptosis by protein kinase C epsilon and delta in neonatal rat ventricular myocytes. Circ Res 89:882-890.
15. Herman JG, Graff JR, Myohanen S, Nelkin BD, and Baylin SB (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 93:9821-9826.
16. Hoque MO, Begum S, Topaloglu O, Chatterjee A, Rosenbaum E, Van Criekinge W, Westra WH, Schoenberg M, Zahurak M, Goodman SN, et al. (2006) Quantitation of promoter methylation of multiple genes in urine DNA and bladder cancer detection. J Natl Cancer Inst 98:996-1004.
17. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, and Baylin SB (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7:536-540.
18. Jaenisch R and Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 (Suppl):245-254.
19. Javaid JI and Davis JM (1993) Cocaine disposition in discrete regions of rat brain. Biopharm Drug Dispos 14:357-364.
20. Jones PA and Laird PW (1999) Cancer epigenetics comes of age. Nat Genet 21:163-167.
21. Jones PA and Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science (Wash DC) 293:1068-1070.
22. Kaneda R, Ueno S, Yamashita Y, Choi YL, Koinuma K, Takada S, Wada T, Shimada K, and Mano H (2005) Genome-wide screening for target regions of histone deacetylases in cardiomyocytes. Circ Res 97:210-218.
23. Kim MH, Jung YS, Moon CH, Jeong EM, Lee SH, Baik EJ, and Moon CK (2003) Isoform-specific induction of PKC-ε by high glucose protects heart-derived H9c2 cells against hypoxic injury. Biochem Biophys Res Commun 309:1-6.
24. Li G, Xiao YH, and Zhang L (2005) Cocaine induces apoptosis in fetal rat myocardial cells through the p38 MAPK and mitochondrial/cytochrome c pathways. J Pharmacol Exp Ther 312:112-119.
25. Lipshultz SE, Frassica JJ, and Orav EJ (1991) Cardiovascular abnormalities in infants prenatally exposed to cocaine. J Pediatr 118:44-51.
26. Mehta SK, Finkelhor RS, Anderson RL, Harcar-Sevcik RA, Wasser TE, and Bahler RC (1993) Transient myocardial ischemia in infants prenatally exposed to cocaine. J Pediatr 122:945-949.
27. Mone SM, Gillman MW, Miller TL, Herman EH, and Lipshultz SE (2004) Effects of environmental exposures on the cardiovascular system: prenatal period through adolescence. Pediatrics 113:1058-1069.
28. Murriel CL and Mochly-Rosen D (2003) Opposing roles of delta and epsilon PKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch Biochem Biophys 420:246-254.
29. Nguyen CT, Gonzales FA, and Jones PA (2001) Altered chromatin structure associated with methylation-induced gene silencing in cancer cells: correlation of accessibility, methylation, MeCP2 binding and acetylation. Nucleic Acids Res 29:4598-4606.
30. Norris MK and Hill CS (1992) Assessing congenital heart defects in the cocaine-exposed neonate. Dimens Crit Care Nurs 11:6-12.
31. Reik W, Constancia M, Fowden A, Anderson N, Dean W, Ferguson-Smith A, Tycko B, and Sibley C (2003) Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 547:35-44.
32. Reik W, Dean W, and Walter J (2001) Epigenetic reprogramming in mammalian development. Science (Wash DC) 293:1089-1093.
33. Rogstad DK, Liu P, Burdzy A, Lin SS, and Sower LC (2002) Endogenous DNA lesions can inhibit the binding of the AP-1 (c-Jun) transcription factor. Biochemistry 41:8093-8102.
34. Rybin VO and Steinberg SF (1994) Protein kinase C isoform expression and regulation in the developing rat heart. Circ Res 74:299-309.
35. Shaulian E and Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131-E136.
36. Shaw GM, Malcoe LH, Lammer EJ, and Swan SH (1991) Maternal use of cocaine during pregnancy and congenital cardiac anomalies. J Pediatr 118:167-168.
37. Soto U, Das BC, Lengert M, Finzer P, zur Hausen H, and Rösl F (1999) Conversion of HPV-18-positive non-tumorigenic HeLa-fibroblast hybrids to invasive growth involves loss of TNF-mediated repression of viral transcription and modification of the AP-1-transcription complex. Oncogene 18:3187-3198.
38. Spear LP, Frambes NA, and Kirstein CL (1989) Fetal and maternal brain and plasma levels of cocaine and benzoylecgonine following chronic subcutaneous administration of cocaine during gestation in rats. Psychopharmacology (Berl) 97:427-431.
39. van de Bor M, Walther FJ, and Ebrahimi M (1990) Decreased cardiac output in infants of mothers who abused cocaine. Pediatrics 85:30-32.
40. van den Veyver IB (2002) Genetic effects of methylation diets. Annu Rev Nutr 22:255-282.
41. van Riggelen J, Buchwalter G, Soto U, De-Castro AJ, Hausen HZ, Wasylyk B, and Rosl F (2005) Loss of net as repressor leads to constitutive increased c-fos transcription in cervical cancer cells. J Biol Chem 280:3286-3294.
42. Wade PA (2001) Methyl CpG-binding proteins and transcriptional repression. Bioessays 23:1131-1137.
43. Wiggins RC (1992) Pharmacokinetics of cocaine in pregnancy and effects on fetal maturation. Clin Pharmacokinet 22:85-93.
44. Xiao Y, He J, Gilbert RD, and Zhang L (2000) Cocaine induces apoptosis in fetal myocardial cells through a mitochondria-dependent pathway. J Pharmacol Exp Ther 292:8-14.
45. Xiao Y, Xiao D, He J, and Zhang L (2001) Maternal cocaine administration during pregnancy induces apoptosis in fetal rat heart. J Cardiovasc Pharmacol 37:639-648.
46. Zhang H, Xiao D, Longo LD, and Zhang L (2006) Regulation of α1-adrenoceptor-mediated contractions of uterine arteries by PKC: effect of pregnancy. Am J Physiol 291:H2282-H2289.
47. Zhang L, Xiao Y, and He J (1999) Cocaine and apoptosis in myocardial cells. Anat Rec 257:208-216.
48. Cip1 promoter. Mol Cell Biol 23:4056-4065.