Amelioration strategies fail to prevent tobacco smoke effects on neurodifferentiation: Nicotinic receptor blockade, antioxidants, methyl donors

Toxicology

Volumn 333, Issue , 2015, Pages 63-75

  Slotkin, Theodore A ^a   Skavicus, Samantha ^a   Card, Jennifer ^a   Levin, Edward D ^a   Seidler, Frederic J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Antioxidants; Methyl donors; Neurodifferentiation; Nicotine; PC12 cells; Tobacco smoke extract

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; CHOLINE; CYANOCOBALAMIN; FOLIC ACID; MECAMYLAMINE; NICOTINE TARTRATE; NICOTINIC RECEPTOR; TOBACCO SMOKE; NEUROPROTECTIVE AGENT; NICOTINE; NICOTINIC RECEPTOR BLOCKING AGENT; SMOKE;

ANTIOXIDANT ACTIVITY; ARTICLE; CARBON METABOLISM; CELL LOSS; NERVE CELL DIFFERENTIATION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ADVERSE EFFECTS; ANIMAL; CELL PROLIFERATION; CELL PROTECTION; CELL SIZE; CELL SURVIVAL; CHOLINERGIC NERVE CELL; DNA REPLICATION; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; DRUG POTENTIATION; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PC12 CELL LINE; RAT; SMOKE; SMOKING;

NICOTIANA TABACUM;

ANIMALS; ANTIOXIDANTS; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CHOLINERGIC NEURONS; CYTOPROTECTION; DNA REPLICATION; DOPAMINERGIC NEURONS; DRUG SYNERGISM; NEUROGENESIS; NEURONS; NEUROPROTECTIVE AGENTS; NICOTINE; NICOTINIC ANTAGONISTS; PC12 CELLS; PHENOTYPE; RATS; SMOKE; SMOKING;

EID: 84928265628     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2015.04.005     Document Type: Article

References (78)

1. Abbott L.C., Winzer-Serhan U.H. Smoking during pregnancy: lessons learned from epidemiological studies and experimental studies using animal models. Crit. Rev. Toxicol. 2012, 42:279-303.
2. Abreu-Villaça Y., Seidler F.J., Qiao D., Slotkin T.A. Modeling the developmental neurotoxicity of nicotine in vitro: cell acquisition, growth and viability in PC12 cells. Dev. Brain Res. 2005, 154:239-246.
3. Adigun A.A., Seidler F.J., Slotkin T.A. Disparate developmental neurotoxicants converge on the cyclic AMP signaling cascade, revealed by transcriptional profiles in vitro and in vivo. Brain Res. 2010, 1316:1-16.
4. Albuquerque C.A., Smith K.R., Johnson C., Chao R., Harding R. Influence of maternal tobacco smoking during pregnancy on uterine, umbilical and fetal cerebral artery blood flows. Early Hum. Dev. 2004, 80:31-42.
5. Araki W., Wurtman R.J. Control of membrane phosphatidylcholine biosynthesis by diacylglycerol levels in neuronal cells undergoing neurite outgrowth. Proc. Natl. Acad. Sci. 1997, 94:11946-11950.
6. Avila A.M., Davila-Garcia M.I., Ascarrunz V.S., Xiao Y., Kellar K.J. Differential regulation of nicotinic acetylcholine receptors in PC12 cells by nicotine and nerve growth factor. Mol. Pharmacol. 2003, 64:974-986.
7. Aycicek A., Ipek A. Maternal active or passive smoking causes oxidative stress in cord blood. Eur. J. Pediatr. 2008, 167:81-85.
8. Bell J.M., Whitmore W.L., Slotkin T.A. Effects of α-difluoromethylornithine, a specific irreversible inhibitor of ornithine decarboxylase, on nucleic acids and proteins in developing rat brain: critical perinatal periods for regional selectivity. Neuroscience 1986, 17:399-407.
9. Boeke C.E., Gillman M.W., Hughes M.D., Rifas-Shimanh S.L., Villamor E., Oken E. Choline intake during pregnancy and child cognition at age 7 years. Am. J. Epidemiol. 2013, 177:1338-1347.
10. Bruijnzeel A.W., Bauzo R.M., Munikoti V., Rodrick G.B., Yamada H., Fornal C.A., Ormerod B.K., Jacobs B.L. Tobacco smoke diminishes neurogenesis and promotes gliogenesis in the dentate gyrus of adolescent rats. Brain Res. 2011, 1413:32-42.
11. Bush P.G., Mayhew T.M., Abramovich D.R., Aggett P.J., Burke M.D., Page K.R. Maternal cigarette smoking and oxygen diffusion across the placenta. Placenta 2000, 21:824-833.
12. Carmines E.L., Rajendran N. Evidence for carbon monoxide as the major factor contributing to lower fetal weights in rats exposed to cigarette smoke. Toxicol. Sci. 2008, 102:383-391.
13. Clark K.E., Irion G.L. Fetal hemodynamic response to maternal intravenous nicotine administration. Am. J. Obstet. Gynecol. 1992, 167:1624-1631.
14. Coecke S., Goldberg A.M., Allen S., Buzanska L., Calamandrei G., Crofton K., Hareng L., Hartung T., Knaut H., Honegger P., Jacobs M., Lein P., Li A., Mundy W., Owen D., Schneider S., Silbergeld E., Reum T., Trnovec T., Monnet-Tschudi F., Bal-Price A. Workshop report: incorporating in vitro alternative methods for developmental neurotoxicity into international hazard and risk assessment strategies. Environ. Health Perspect. 2007, 115:924-931.
15. Cornelius M.D., Day N.L. Developmental consequences of prenatal tobacco exposure. Curr. Opin. Neurol. 2009, 22:121-125.
16. Costa L.G. Neurotoxicity testing: a discussion of in vitro alternatives. Environ. Health Perspect. 1998, 106(Suppl. 2):505-510.
17. DeLorenze G.N., Kharrazi M., Kaufman F.L., Eskenazi B., Bernert J.T. Exposure to environmental tobacco smoke in pregnant women: the association between self-report and serum cotinine. Environ. Res. 2002, 90:21-32.
18. DiFranza J.R., Lew R.A. Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome. J. Family Pract. 1995, 40:385-394.
19. Dreyfus C.F. Neurotransmitters and neurotrophins collaborate to influence brain development. Perspect. Dev. Neurobiol. 1998, 5:389-399.
20. Fayol L., Gulian J.M., Dalmasso C., Calaf R., Simeoni U., Millet V. Antioxidant status of neonates exposed in utero to tobacco smoke. Biol. Neonate 2005, 87:121-126.
21. Fujita K., Lazarovici P., Guroff G. Regulation of the differentiation of PC12 pheochromocytoma cells. Environ. Health Perspect. 1989, 80:127-142.
22. Fuller B.F., Cortes D.F., Landis M.K., Yohannes H., Griffin H.E., Stafflinger J.E., Bowers M.S., Lewis M.H., Fox M.A., Ottens A.K. Exposure of rats to environmental tobacco smoke during cerebellar development alters behavior and perturbs mitochondrial energetics. Environ. Health Perspect. 2012, 120:1684-1691.
23. Gaysina D., Fergusson D.M., Leve L.D., Horwood J., Reiss D., Shaw D.S., Elam K.K., Natsuaki M.N., Neiderhiser J.M., Harold G.T. Maternal smoking during pregnancy and offspring conduct problems: evidence from three independent genetically-sensitive research designs. JAMA Psychiatry 2013, 70:956-963.
24. Gitto E., Reiter R.J., Karbownik M., Tan D.X., Gitto P., Barberi S., Barberi I. Causes of oxidative stress in the pre- and perinatal period. Biol. Neonate 2002, 81:146-157.
25. Golub M.S., Slotkin T.A., Pinkerton K.E. Visual recognition memory and auditory brainstem response in infant rhesus monkeys exposed perinatally to environmental tobacco smoke. Brain Res. 2007, 1151:102-106.
26. Gospe S.M., Joyce J.A., Siebert J.R., Jack R.M., Pinkerton K.E. Exposure to environmental tobacco smoke during pregnancy in rats yields less effect on indices of brain cell number and size than does postnatal exposure. Reprod. Toxicol. 2009, 27:22-27.
27. Guan Z.Z., Yu W.F., Nordberg A. Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells. Neurochem. Int. 2003, 43:243-249.
28. Gueorguiev V.D., Zeman R.J., Meyer E.M., Sabban E.L. Involvement of α7 nicotinic acetylcholine receptors in activation of tyrosine hydroxylase and dopamine β-hydroxylase gene expression in PC12 cells. J. Neurochem. 2000, 75:1997-2005.
29. Hohmann C.F. A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci. Biobehav. Rev. 2003, 27:351-363.
30. Jameson R.R., Seidler F.J., Qiao D., Slotkin T.A. Adverse neurodevelopmental effects of dexamethasone modeled in PC12 cells: identifying the critical stages and concentration thresholds for the targeting of cell acquisition, differentiation and viability. Neuropsychopharmacology 2006, 31:1647-1658.
31. Jameson R.R., Seidler F.J., Qiao D., Slotkin T.A. Chlorpyrifos affects phenotypic outcomes in a model of mammalian neurodevelopment: critical stages targeting differentiation in PC12 cells. Environ. Health Perspect. 2006, 114:667-672.
32. Katoh S., Mitsui Y., Kitani K., Suzuki T. Hyperoxia induces the differentiated neuronal phenotype of PC12 cells by producing reactive oxygen species. Biochem. Biophys. Res. Commun. 1997, 241:347-351.
33. Knapp S., Wurtman R.J. Enhancement of free fatty acid incorporation into phospholipids by choline plus cytidine. Brain Res. 1999, 822:52-59.
34. Koren G., Eliopoulos C., Klein J. Measuring fetal exposure to nicotine. Nicotine Safety and Toxicity 1998, 99-106. Oxford University Press, New York. N.L. Benowitz (Ed.).
35. Lassiter T.L., MacKillop E.A., Ryde I.T., Seidler F.J., Slotkin T.A. Is fipronil safer than chlorpyrifos? Comparative developmental neurotoxicity modeled in PC12 cells. Brain Res. Bull. 2009, 78:313-322.
36. Lauder J.M. Roles for neurotransmitters in development: possible interaction with drugs during the fetal and neonatal periods. Prevention of Physical and Mental Congenital Defects 1985, 375-380. Alan R. Liss, New York. M. Marois (Ed.).
37. Lee J.E., Park J.H., Shin I.C., Koh H.C. Reactive oxygen species regulated mitochondria-mediated apoptosis in PC12 cells exposed to chlorpyrifos. Toxicol. Appl. Pharmacol. 2012, 263:148-162.
38. Lobo Torres L.H., Moreira W.L., Tamborelli Garcia R.C., Annoni R., Nicoletti Carvalho A.L., Teixeira S.A., Pacheco-Neto M., Muscara M.N., Camarini R., de Melo Loureiro A.P., Yonamine M., Mauad T., Marcourakis T. Environmental tobacco smoke induces oxidative stress in distinct brain regions of infant mice. J. Toxicol. Environ. Health A 2012, 75:971-980.
39. Luck W., Nau H., Hansen R., Steldinger R. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev. Pharmacol. Ther. 1985, 8:384-395.
40. McEvoy C.T., Schilling D., Clay N., Jackson K., Go M.D., Spitale P., Bunten C., Leiva M., Gonzales D., Hollister-Smith J., Durand M., Frei B., Buist A.S., Peters D., Morris C.D., Spindel E.R. Vitamin C supplementation for pregnant smoking women and pulmonary function in their newborn infants: a randomized clinical trial. J. Am. Med. Assoc. 2014, 311:2074-2082.
41. Orhon F.S., Ulukol B., Kahya D., Cengiz B., Baskan S., Tezcan S. The influence of maternal smoking on maternal and newborn oxidant and antioxidant status. Eur. J. Pediatr. 2009, 168:975-981.
42. Panchision D.M. The role of oxygen in regulating neural stem cells in development and disease. J. Cell Physiol. 2009, 220:562-568.
43. Pauly J.R., Slotkin T.A. Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatr. 2008, 97:1331-1337.
44. Pettigrew A.R., Logan R.W., Willocks J. Smoking in pregnancy: effect on birth weight and on cyanide and thiocyanate levels in mother and baby. Br. J. Obstet. Gynaecol. 1977, 84:31-34.
45. Powers C.M., Badireddy A.R., Ryde I.T., Seidler F.J., Slotkin T.A. Silver nanoparticles compromise neurodevelopment in PC12 cells: critical contributions of silver ion, particle size, coating and composition. Environ. Health Perspect. 2010, 119:37-44.
46. Powers C.M., Wrench N., Ryde I.T., Smith A.M., Seidler F.J., Slotkin T.A. Silver impairs neurodevelopment: studies in PC12 cells. Environ. Health Perspect. 2010, 118:73-79.
47. Proskocil B.J., Sekhon H.S., Clark J.A., Lupo S.L., Jia Y., Hull W.M., Whitsett J.A., Starcher B.C., Spindel E.R. Vitamin C prevents the effects of prenatal nicotine on pulmonary function in newborn monkeys. Am. J. Respir. Crit. Care Med. 2005, 171:1032-1039.
48. Qiao D., Seidler F.J., Slotkin T.A. Developmental neurotoxicity of chlorpyrifos modeled in vitro: comparative effects of metabolites and other cholinesterase inhibitors on DNA synthesis in PC12 and C6 cells. Environ. Health Perspect. 2001, 109:909-913.
49. Qiao D., Seidler F.J., Slotkin T.A. Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicol. Appl. Pharmacol. 2005, 206:17-26.
50. Qiao D., Seidler F.J., Violin J.D., Slotkin T.A. Nicotine is a developmental neurotoxicant and neuroprotectant: stage-selective inhibition of DNA synthesis coincident with shielding from effects of chlorpyrifos. Dev. Brain Res. 2003, 147:183-190.
51. Radio N.M., Breier J.M., Shafer T.J., Mundy W.R. Assessment of chemical effects on neurite outgrowth in PC12 cells using high content screening. Toxicol. Sci. 2008, 105:106-118.
52. Robkin M.A. Carbon monoxide and the embryo. Int. J. Dev. Biol. 1997, 41:283-289.
53. Rossner P., Milcova A., Libalova H., Novakova Z., Topinka J., Balascak I., Sram R.J. Biomarkers of exposure to tobacco smoke and environmental pollutants in mothers and their transplacental transfer to the foetus. Part II. Oxidative damage. Mutation Res. 2009, 669:20-26.
54. Savelkoul P.J.M., Janickova H., Kuipers A.A.M., Hageman R.J.J., Kamphuis P.J., Dolezal V., Broerson L.M. A specific multi-nutrient formulation enhances M1 muscarinic acetylcholine receptor responses in vitro. J. Neurochem. 2012, 120:631-640.
55. Sekizawa S., Chen C.Y., Bechtold A.G., Tabor J.M., Bric J.M., Pinkerton K.E., Joad J.P., Bonham A.C. Extended second-hand tobacco smoke exposure induces plasticity in nucleus tractus solitarius second-order lung afferent neurons in young guinea pigs. Eur. J. Neurosci. 2008, 28:771-781.
56. Slikker W., Xu Z.A., Levin E.D., Slotkin T.A. Mode of action: disruption of brain cell replication, second messenger, and neurotransmitter systems during development leading to cognitive dysfunction - developmental neurotoxicity of nicotine. Crit. Rev. Toxicol. 2005, 35:703-711.
57. Slotkin T.A. Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 2004, 198:132-151.
58. Slotkin T.A. If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents?. Neurotoxicol. Teratol. 2008, 30:1-19.
59. Slotkin T.A., Card J., Seidler F.J. Adverse benzo[a]pyrene effects on neurodifferentiation are altered by other neurotoxicant coexposures: interactions with dexamethasone, chlorpyrifos, or nicotine in PC12 cells. Environ. Health Perspect. 2013, 121:825-831.
60. Slotkin T.A., Card J., Stadler A., Levin E.D., Seidler F.J. Effects of tobacco smoke on PC12 cell neurodifferentiation are distinct from those of nicotine or benzo[a]pyrene. Neurotoxicol. Teratol. 2014, 43:19-24.
61. Slotkin T.A., Lobner D., Seidler F.J. Transcriptional profiles for glutamate transporters reveal differences between organophosphates but similarities with unrelated neurotoxicants. Brain Res. Bull. 2010, 83:76-83.
62. Slotkin T.A., MacKillop E.A., Ryde I.T., Seidler F.J. Ameliorating the developmental neurotoxicity of chlorpyrifos: a mechanisms-based approach in PC12 cells. Environ. Health Perspect. 2007, 115:1306-1313.
63. Slotkin T.A., MacKillop E.A., Ryde I.T., Tate C.A., Seidler F.J. Screening for developmental neurotoxicity using PC12 cells: comparisons of organophosphates with a carbamate, an organochlorine and divalent nickel. Environ. Health Perspect. 2007, 115:93-101.
64. Slotkin T.A., Persons D., Slepetis R.J., Taylor D., Bartolome J. Control of nucleic acid and protein synthesis in developing brain, kidney, and heart of the neonatal rat: effects of α-difluoromethylornithine, a specific, irreversible inhibitor of ornithine decarboxylase. Teratology 1984, 30:211-224.
65. Slotkin T.A., Pinkerton K.E., Seidler F.J. Perinatal environmental tobacco smoke exposure in Rhesus monkeys: critical periods and regional selectivity for effects on brain cell development and lipid peroxidation. Environ. Health Perspect. 2006, 114:34-39.
66. Slotkin T.A., Pinkerton K.E., Tate C.A., Seidler F.J. Alterations of serotonin synaptic proteins in brain regions of neonatal Rhesus monkeys exposed to perinatal environmental tobacco smoke. Brain Res. 2006, 1111:30-35.
67. Slotkin T.A., Seidler F.J. Oxidative and excitatory mechanisms of developmental neurotoxicity: transcriptional profiles for chlorpyrifos, diazinon, dieldrin and divalent nickel in PC12 cells. Environ. Health Perspect. 2009, 117:587-596.
68. Slotkin T.A., Seidler F.J. Oxidative stress from diverse developmental neurotoxicants: antioxidants protect against lipid peroxidation without preventing cell loss. Neurotoxicol. Teratol. 2010, 32:124-131.
69. Slotkin T.A., Seidler F.J., Qiao D., Aldridge J.E., Tate C.A., Cousins M.M., Proskocil B.J., Sekhon H.S., Clark J.A., Lupo S.L., Spindel E.R. Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of Rhesus monkeys. Neuropsychopharmacology 2005, 30:129-144.
70. Slotkin T.A., Seidler F.J., Spindel E.R. Prenatal nicotine exposure in rhesus monkeys compromises development of brainstem and cardiac monoamine pathways involved in perinatal adaptation and sudden infant death syndrome: amelioration by vitamin C. Neurotoxicol. Teratol. 2011, 33:431-434.
71. Song X., Violin J.D., Seidler F.J., Slotkin T.A. Modeling the developmental neurotoxicity of chlorpyrifos in vitro: macromolecule synthesis in PC12 cells. Toxicol. Appl. Pharmacol. 1998, 151:182-191.
72. Steegers-Theunissen R.P., Twigt J., Pestinger V., Sinclair V. The periconceptional period, reproduction and long-term health of offspring: the importance of one-carbon metabolism. Hum. Reprod. Update 2013, 19:640-655.
73. Teng K.K., Greene L.A. Cultured PC 12 cells: a model for neuronal function and differentiation. Cell Biology: A Laboratory Handbook 1994, 218-224. Academic Press, San Diego. J.E. Celis (Ed.).
74. Vieira H.A., Alves P., Vercelli A. Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog. Neurobiol. 2011, 93:444-455.
75. Wakschlag L.S., Lahey B.B., Loeber R., Green S.M., Gordon R.A., Leventhal B.L. Maternal smoking during pregnancy and the risk of conduct disorder in boys. Arch. Gen. Psychiat. 1997, 54:670-676.
76. Winick M., Noble A. Quantitative changes in DNA, RNA and protein during prenatal and postnatal growth in the rat. Dev. Biol. 1965, 12:451-466.
77. Yamashita H., Nakamura S. Nicotine rescues PC12 cells from death induced by nerve growth factor deprivation. Neurosci. Lett. 1996, 213:145-147.
78. Yildiz D., Liu Y.S., Ercal N., Armstrong D.W. Comparison of pure nicotine- and smokeless tobacco extract-induced toxicities and oxidative stress. Arch. Environ. Contam. Toxicol. 1999, 37:434-439.