Prenatal cocaine exposure impairs cognitive function of progeny via insulin growth factor II epigenetic regulation

Neurobiology of Disease

Volumn 82, Issue , 2015, Pages 54-65

  Zhao, Qian ^a   Hou, Jing ^a   Chen, Bo ^a   Shao, Xue ^a   Zhu, Ruiming ^a   Bu, Qian ^a   Gu, Hui ^a   Li, Yan ^a   Zhang, Baolai ^a   Du, Changman ^a   Fu, Dengqi ^a   Kong, Jueying ^a   Luo, Li ^a   Long, Hailei ^a   Li, Hongyu ^a   Deng, Yi ^a   Zhao, Yinglan ^a   Cen, Xiaobo ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

CaMKII ; Cognitive function; DNA methylation; DNMTs; IGF II; L Methionine; Prenatal cocaine exposure

Indexed keywords

COCAINE; DINUCLEOTIDE; DNA METHYLTRANSFERASE; MESSENGER RNA; METHIONINE; SOMATOMEDIN B; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DOWN REGULATION; EPIGENETICS; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; IGF II GENE; MALE; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPATIAL MEMORY; UPREGULATION; ANIMAL; COGNITION; DNA METHYLATION; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; MAZE TEST; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PREGNANCY; PSYCHOLOGY;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; COCAINE; COGNITION; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR II; MAZE LEARNING; MICE; PHOSPHORYLATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84930942565     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.05.014     Document Type: Article

References (47)

1. Abuse S. Mental health services administration: results from the 2009 National Survey on Drug Use and Health: volume I. Summary of National Findings. NSDUH Series H-38A, HHS Publication No. SMA 2010.
2. Agis-Balboa R.C., Arcos-Diaz D., et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J. 2011, 30(19):4071-4083.
3. Alberini C.M., Chen D.Y. Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends Neurosci. 2012, 35(5):274-283.
4. Bashkatova V., Meunier J., et al. Memory impairments and oxidative stress in the hippocampus of in-utero cocaine-exposed rats. Neuroreport 2005, 16(11):1217-1221.
5. Beck S., Olek A. The Epigenome: Molecular Hide and Seek 2006, John Wiley & Sons.
6. Beckonert O., Keun H.C., et al. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat. Protoc. 2007, 2(11):2692-2703.
7. Benarroch E.E. Insulin-like growth factors in the brain and their potential clinical implications. Neurology 2012, 79(21):2148-2153.
8. Bernal A.J., Jirtle R.L. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res. A Clin. Mol. Teratol. 2010, 88(10):938-944.
9. Bestor T.H. The DNA methyltransferases of mammals. Hum. Mol. Genet. 2000, 9(16):2395-2402.
10. Broughton S., Partridge L. Insulin/IGF-like signalling, the central nervous system and aging. Biochem. J. 2009, 418:1-12.
11. Capel E., Flejou J., et al. Assessment of MLH1 promoter methylation in relation to gene expression requires specific analysis. Oncogene 2007, 26(54):7596-7600.
12. Chao W., D'Amore P.A. IGF2: epigenetic regulation and role in development and disease. Cytokine Growth Factor Rev. 2008, 19(2):111-120.
13. Chen D.Y., Stern S.A., et al. A critical role for IGF-II in memory consolidation and enhancement. Nature 2011, 469(7331):491-497.
14. Cone-Wesson B. Prenatal alcohol and cocaine exposure: influences on cognition, speech, language, and hearing. J. Commun. Disord. 2005, 38(4):279-302.
15. Ding G.-L., Wang F.-F., et al. Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 2012, 61(5):1133-1142.
16. Fuso A., Cavallaro R.A., et al. Gene silencing by S-adenosylmethionine in muscle differentiation. FEBS Lett. 2001, 508(3):337-340.
17. Gapp K., von Ziegler L., et al. Early life epigenetic programming and transmission of stress-induced traits in mammals. Bioessays 2014, 36(5):491-502.
18. Govorko D., Bekdash R.A., et al. Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol. Psychiatry 2012, 72(5):378-388.
19. Hawkes C., Kar S. The insulin-like growth factor-II/mannose-6-phosphate receptor: structure, distribution and function in the central nervous system. Brain Res. Rev. 2004, 44(2):117-140.
20. Hermann A., Gowher H., et al. Biochemistry and biology of mammalian DNA methyltransferases. Cell. Mol. Life Sci. CMLS 2004, 61(19-20):2571-2587.
21. Kalhan S., Edmison J., et al. Methionine and protein metabolism in non-alcoholic steatohepatitis: evidence for lower rate of transmethylation of methionine. Clin. Sci. 2011, 121:179-189.
22. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3(6):453-462.
23. Kovacheva V.P., Mellott T.J., et al. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J. Biol. Chem. 2007, 282(43):31777-31788.
24. Li H., Bu Q., et al. Mechanisms of metabonomic for a gateway drug: nicotine priming enhances behavioral response to cocaine with modification in energy metabolism and neurotransmitter level. PLoS One 2014, 9(1):e87040.
25. Lisman J., Schulman H., et al. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 2002, 3(3):175-190.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 2001, 25(4):402-408.
27. Lopes S., Lewis A., et al. Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum. Mol. Genet. 2003, 12(3):295-305.
28. Murphy S.K., Adigun A., et al. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene 2012, 494(1):36-43.
29. Nolan T., Hands R.E., et al. Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 2006, 1(3):1559-1582.
30. Novikova S.I., He F., et al. Maternal cocaine administration in mice alters DNA methylation and gene expression in hippocampal neurons of neonatal and prepubertal offspring. PLoS One 2008, 3(4):e1919.
31. Oka M., Meacham A.M., et al. De novo DNA methyltransferases Dnmt3a and Dnmt3b primarily mediate the cytotoxic effect of 5-aza-2'-deoxycytidine. Oncogene 2005, 24(19):3091-3099.
32. O'Reilly R.C., Rudy J.W. Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol. Rev. 2001, 108(2):311.
33. Ostrovsky O., Ahmed N.T., et al. The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Mol. Biol. Cell 2009, 20(6):1855-1864.
34. Paoloni-Giacobino A., Chaillet J. The role of DMDs in the maintenance of epigenetic states. Cytogenet. Genome Res. 2006, 113(1-4):116-121.
35. Pfalzer A.C., Choi S.-W., et al. S-adenosylmethionine mediates inhibition of inflammatory response and changes in DNA methylation in human macrophages. Physiol. Genomics 2014, 46(17):617-623.
36. Reik W., Dean W., et al. Epigenetic reprogramming in mammalian development. Science 2001, 293(5532):1089-1093.
37. Reinhart B., Paoloni-Giacobino A., et al. Specific differentially methylated domain sequences direct the maintenance of methylation at imprinted genes. Mol. Cell. Biol. 2006, 26(22):8347-8356.
38. Robert M.-F., Morin S., et al. DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat. Genet. 2002, 33(1):61-65.
39. Robertson K.D., Ait-Si-Ali S., et al. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 2000, 25(3):338-342.
40. Rountree M.R., Bachman K.E., et al. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat. Genet. 2000, 25(3):269-277.
41. Salas-Ramirez K.Y., Frankfurt M., et al. Prenatal cocaine exposure increases anxiety, impairs cognitive function and increases dendritic spine density in adult rats: influence of sex. Neuroscience 2010, 169(3):1287-1295.
42. Sananbenesi F., Fischer A., et al. A hippocampal Cdk5 pathway regulates extinction of contextual fear. Nat. Neurosci. 2007, 10(8):1012-1019.
43. Singer L.T., Minnes S., et al. Cognitive outcomes of preschool children with prenatal cocaine exposure. JAMA 2004, 291(20):2448-2456.
44. Ulrey C.L., Liu L., et al. The impact of metabolism on DNA methylation. Hum. Mol. Genet. 2005, 14(Suppl. 1):R139-R147.
45. Vassoler F.M., White S.L., et al. Epigenetic inheritance of a cocaine-resistance phenotype. Nat. Neurosci. 2013, 16(1):42-47.
46. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 2006, 1(2):848-858.
47. Waterland R.A., Lin J.-R., et al. Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum. Mol. Genet. 2006, 15(5):705-716.