Developmental role of nuclear factor E2-related factor 2 in mitigating methamphetamine fetal toxicity and postnatal neurodevelopmental deficits

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 620-631

  Ramkissoon, Annmarie ^a   Wells, Peter G ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

DNA oxidation; E2 related factor 2; Fetal toxicity; Free radicals; Methamphetamine; Neurodevelopmental deficits; Nrf2; Nuclear factor

Indexed keywords

DNA; GLUTAMATE DECARBOXYLASE 65; GLYCOSYLTRANSFERASE; HEME OXYGENASE 1; MESSENGER RNA; METHAMPHETAMINE; OXOGUANINE GLYCOSYLASE 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; CENTRAL STIMULANT AGENT; NFE2L2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DISEASE EXACERBATION; DNA DAMAGE; FEMALE; FETOTOXICITY; FETUS; FETUS WEIGHT; GABAERGIC SYSTEM; LONG TERM EXPOSURE; MACROMOLECULE; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLFACTORY BULB; OXIDATION; OXIDATIVE STRESS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; SINGLE DRUG DOSE; SMELLING; WILD TYPE; ANIMAL; BRAIN; DRUG EFFECTS; EMBRYOLOGY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION;

MUS;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; FEMALE; FETUS; IMMUNOHISTOCHEMISTRY; METHAMPHETAMINE; MICE; MICE, KNOCKOUT; NEUROGENESIS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84882778791     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.07.043     Document Type: Article

References (41)

1. A.M. Arria, C. Derauf, L.L. Lagasse, P. Grant, R. Shah, L. Smith, W. Haning, M. Huestis, A. Strauss, S. Della Grotta, J. Liu, and B. Lester Methamphetamine and other substance use during pregnancy: preliminary estimates from the Infant Development, Environment, and Lifestyle (IDEAL) study Matern. Child Health J. 10 2006 293 302 (Pubitemid 43898985)
2. M.A. Plessinger Prenatal exposure to amphetamines: risks and adverse outcomes in pregnancy Obstet. Gynecol. Clin. North Am. 25 1998 119 138 (Pubitemid 28141704)
3. L.M. Smith, L.L. LaGasse, C. Derauf, P. Grant, R. Shah, A. Arria, M. Huestis, W. Haning, A. Strauss, S. Della Grotta, J. Liu, and B.M. Lester The infant development, environment, and lifestyle study: effects of prenatal methamphetamine exposure, polydrug exposure, and poverty on intrauterine growth Pediatrics 118 2006 1149 1156 (Pubitemid 46090058)
4. W. Jeng, A.W. Wong, A.K.R. Ting, and P.G. Wells Methamphetamine-enhanced embryonic oxidative DNA damage and neurodevelopmental deficits Free Radic. Biol. Med. 39 2005 317 326 (Pubitemid 40910188)
5. A.W. Wong, G.P. McCallum, W. Jeng, and P.G. Wells Oxoguanine glycosylase 1 protects against methamphetamine-enhanced fetal brain oxidative DNA damage and neurodevelopmental deficits J. Neurosci. 28 2008 9047 9054
6. K.D. Acuff-Smith, M.A. Schilling, J.E. Fisher, and C.V. Vorhees Stage-specific effects of prenatal d-methamphetamine exposure on behavioral and eye development in rats Neurotoxicol. Teratol. 18 1996 199 215 (Pubitemid 26115055)
7. X. Deng, B. Ladenheim, S. Jayanthi, and J.L. Cadet Methamphetamine administration causes death of dopaminergic neurons in the mouse olfactory bulb Biol. Psychiatry 61 2007 1235 1243 (Pubitemid 46735929)
8. W. Jeng, A. Ramkissoon, T. Parman, and P.G. Wells Prostaglandin H synthase-catalyzed bioactivation of amphetamines to free radical intermediates that cause CNS regional DNA oxidation and nerve terminal degeneration FASEB J 20 2006 638 650 (Pubitemid 44933308)
9. L. Nguyen, J.M. Rigo, V. Rocher, S. Belachew, B. Malgrange, B. Rogister, P. Leprince, and G. Moonen Neurotransmitters as early signals for central nervous system development Cell Tissue Res. 305 2001 187 202 (Pubitemid 32684574)
10. M.J. Calkins, R.J. Jakel, D.A. Johnson, K. Chan, Y.W. Kan, and J.A. Johnson Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription Proc. Natl. Acad. Sci. USA 102 2005 244 249 (Pubitemid 40094460)
11. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 1999 76 86 (Pubitemid 29045117)
12. A. Dhenaut, S. Hollenbach, I. Eckert, B. Epe, S. Boiteux, and J.P. Radicella Characterization of hOGG1 promoter structure, expression during cell cycle and overexpression in mammalian cells Adv. Exp. Med. Biol. 500 2001 613 616 (Pubitemid 34107060)
13. J.M. Lee, M.J. Calkins, K. Chan, Y.W. Kan, and J.A. Johnson Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis J. Biol. Chem. 278 2003 12029 12038 (Pubitemid 36800179)
14. A.Y. Shih, D.A. Johnson, G. Wong, A.D. Kraft, L. Jiang, H. Erb, J.A. Johnson, and T.H. Murphy Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress J. Neurosci. 23 2003 3394 3406 (Pubitemid 36531981)
15. K. Chan, R. Lu, J.C. Chang, and Y.W. Kan NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development Proc. Natl. Acad. Sci. USA 93 1996 13943 13948 (Pubitemid 26424225)
16. A. Ramkissoon, and P.G. Wells Methamphetamine-initiated oxidative stress, neurotoxicity and functional deficits are modulated by nuclear factor-E2-related factor 2 (Nrf2) Toxicol. Sci. 108 1 2009 448 (Suppl.)
17. A.M. Pacchioni, J. Vallone, R.I. Melendez, A. Shih, T.H. Murphy, and P.W. Kalivas Nrf2 gene deletion fails to alter psychostimulant-induced behavior or neurotoxicity Brain Res. 1127 2007 26 35 (Pubitemid 44856721)
18. N. Granado, I. Lastres-Becker, S. Ares-Santos, I. Oliva, E. Martin, A. Cuadrado, and R. Moratalla Nrf2 deficiency potentiates methamphetamine-induced dopaminergic axonal damage and gliosis in the striatum Glia 59 2011 1850 1863
19. S. Jayanthi, M.T. McCoy, G. Beauvais, B. Ladenheim, K. Gilmore, W. Wood 3rd, K. Becker, and J.L. Cadet Methamphetamine induces dopamine D1 receptor-dependent endoplasmic reticulum stress-related molecular events in the rat striatum PLoS One 4 2009 e6092
20. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
21. V.P. Sah, L.D. Attardi, G.J. Mulligan, B.O. Williams, R.T. Bronson, and T. Jacks A subset of p53-deficient embryos exhibit exencephaly Nat. Genet. 10 1995 175 180
22. J.L. Ravanat, T. Douki, P. Duez, E. Gremaud, K. Herbert, T. Hofer, L. Lasserre, C. Saint-Pierre, A. Favier, and J. Cadet Cellular background level of 8-oxo-7,8-dihydro-2′-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up Carcinogenesis 23 2002 1911 1918 (Pubitemid 35355940)
23. L.L. Goncalves, A. Ramkissoon, and P.G. Wells Prostaglandin H synthase-1-catalyzed bioactivation of neurotransmitters, their precursors, and metabolites: oxidative DNA damage and electron spin resonance spectroscopy studies Chem. Res. Toxicol. 22 2009 842 852
24. J.L. Tillerson, W.M. Caudle, J.M. Parent, C. Gong, T. Schallert, and G.W. Miller Olfactory discrimination deficits in mice lacking the dopamine transporter or the D2 dopamine receptor Behav. Brain. Res. 172 2006 97 105 (Pubitemid 44037817)
25. S. Parrish-Aungst, M.T. Shipley, F. Erdelyi, G. Szabo, and A.C. Puche Quantitative analysis of neuronal diversity in the mouse olfactory bulb J. Comp. Neurol. 501 2007 825 836 (Pubitemid 46797133)
26. J.P. Abramov, and P.G. Wells Embryonic catalase protects against endogenous and phenytoin-enhanced DNA oxidation and embryopathies in acatalasemic and human catalase-expressing mice FASEB J 25 2011 2188 2200
27. S. el-Hage, and S.M. Singh Temporal expression of genes encoding free radical-metabolizing enzymes is associated with higher mRNA levels during in utero development in mice Dev. Genet 11 1990 149 159 (Pubitemid 20230592)
28. L.M. Winn, and P.G. Wells Maternal administration of superoxide dismutase and catalase in phenytoin teratogenicity Free Radic. Biol. Med. 26 1999 266 274 (Pubitemid 29013456)
29. T. Yamamoto, K. Yoh, A. Kobayashi, Y. Ishii, S. Kure, A. Koyama, T. Sakamoto, K. Sekizawa, H. Motohashi, and M. Yamamoto Identification of polymorphisms in the promoter region of the human NRF2 gene Biochem. Biophys. Res. Commun. 321 2004 72 79 (Pubitemid 39055607)
30. X. Wang, D.J. Tomso, B.N. Chorley, H.Y. Cho, V.G. Cheung, S.R. Kleeberger, and D.A. Bell Identification of polymorphic antioxidant response elements in the human genome Hum. Mol. Genet 16 2007 1188 1200 (Pubitemid 47062715)
31. R.O. Bost, P. Kemp, and V. Hnilica Tissue distribution of methamphetamine and amphetamine in premature infants J. Anal. Toxicol. 13 1989 300 302 (Pubitemid 19231667)
32. L. Won, N. Bubula, H. McCoy, and A. Heller Methamphetamine concentrations in fetal and maternal brain following prenatal exposure Neurotoxicol. Teratol. 23 2001 349 354 (Pubitemid 32727366)
33. R. Venugopal, and A.K. Jaiswal Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes Oncogene 17 1998 3145 3156 (Pubitemid 29020810)
34. J.Y. Chan, M. Kwong, R. Lu, J. Chang, B. Wang, T.S. Yen, and Y.W. Kan Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice EMBO J. 17 1998 1779 1787 (Pubitemid 28119131)
35. N. Wakabayashi, K. Itoh, J. Wakabayashi, H. Motohashi, S. Noda, S. Takahashi, S. Imakado, T. Kotsuji, F. Otsuka, D.R. Roop, T. Harada, J.D. Engel, and M. Yamamoto Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation Nat. Genet. 35 2003 238 245 (Pubitemid 37363177)
36. J. Dong, K.K. Sulik, and S.Y. Chen Nrf2-mediated transcriptional induction of antioxidant response in mouse embryos exposed to ethanol in vivo: implications for the prevention of fetal alcohol spectrum disorders Antioxid. Redox Signaling 10 2008 2023 2033
37. G. Gheusi, H. Cremer, H. McLean, G. Chazal, J.D. Vincent, and P.M. Lledo Importance of newly generated neurons in the adult olfactory bulb for odor discrimination Proc. Natl. Acad. Sci. USA 97 2000 1823 1828 (Pubitemid 30118527)
38. R.L. Doty, and D.A. Deems Stellar, S. Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration Neurology 38 1988 1237 1244
39. M. Larsson, A. Lundin, and T.B. Robins Wahlin Olfactory functions in asymptomatic carriers of the Huntington disease mutation J. Clin. Exp. Neuropsychol. 28 2006 1373 1380 (Pubitemid 44578243)
40. J.W. Hinds, and P.L. Hinds Synapse formation in the mouse olfactory bulb. I. Quantitative studies J. Comp. Neurol. 169 1976 15 40
41. E. Enwere, T. Shingo, C. Gregg, H. Fujikawa, S. Ohta, and S. Weiss Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination J. Neurosci. 24 2004 8354 8365 (Pubitemid 39280814)