Imbalances emerge in cardiac autonomic cell signaling after neonatal exposure to terbutaline or chlorpyrifos, alone or in combination

Developmental Brain Research

Volumn 160, Issue 2, 2005, Pages 219-230

  Slotkin, Theodore A ^a   Tate, Charlotte A ^a   Cousins, Mandy M ^a   Seidler, Frederic J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adrenoceptor; Adenylyl cyclase; Autonomic function; Chlorpyrifos; Heart development; Muscarinic acetylcholine receptor; Organophosphorus insecticide; Preterm labor; Terbutaline

Indexed keywords

ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CHLORPYRIFOS; HEART RECEPTOR; MUSCARINIC M2 RECEPTOR; ORGANOPHOSPHATE PESTICIDE; TERBUTALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; CARDIOVASCULAR RESPONSE; CHOLINERGIC ACTIVITY; CHOLINERGIC STIMULATION; CHOLINESTERASE INHIBITION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVATION; ENZYME INHIBITION; EXCITABILITY; EXPOSURE; FEMALE; HEART DEVELOPMENT; MALE; NEUROTOXICITY; NEWBORN; NEWBORN PERIOD; NONHUMAN; PERINATAL DEVELOPMENT; PERINATAL PERIOD; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TOCOLYSIS;

ADENYLATE CYCLASE; ADRENERGIC BETA-AGONISTS; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CARBACHOL; CELL MEMBRANE; CHLORPYRIFOS; CHOLINERGIC AGONISTS; CHOLINESTERASE INHIBITORS; DRUG COMBINATIONS; DRUG INTERACTIONS; FEMALE; FORSKOLIN; HEART; ISOPROTERENOL; MALE; MYOCARDIUM; PREGNANCY; PROTEIN BINDING; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M2; RECEPTORS, ADRENERGIC, BETA; SEX FACTORS; SIGNAL TRANSDUCTION; TERBUTALINE;

ANIMALIA;

EID: 28444462888     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devbrainres.2005.09.006     Document Type: Article

References (84)

1. J.E. Aldridge, F.J. Seidler, and T.A. Slotkin Developmental exposure to chlorpyrifos elicits sex-selective alterations of serotonergic synaptic function in adulthood: critical periods and regional selectivity for effects on the serotonin transporter, receptor subtypes, and cell signaling Environ. Health Perspect. 112 2004 148 155
2. J.E. Aldridge, E.D. Levin, F.J. Seidler, and T.A. Slotkin Developmental exposure of rats to chlorpyrifos leads to behavioral alterations in adulthood, involving serotonergic mechanisms and resembling animal models of depression Environ. Health Perspect. 113 2005 527 531
3. J.E. Aldridge, A. Meyer, F.J. Seidler, and T.A. Slotkin Developmental exposure to terbutaline and chlorpyrifos: pharmacotherapy of preterm labor and an environmental neurotoxicant converge on serotonergic systems in neonatal rat brain regions Toxicol. Appl. Pharmacol. 203 2005 134 144
4. H.R. Andersen, A.M. Vinggaard, T.H. Rasmussen, I.M. Gjermandsen, and E.C. Bonefeld-Jorgensen Effects of currently used pesticides in assays for estrogenicity, androgenicity, and aromatase activity in vitro Toxicol. Appl. Pharmacol. 179 2002 1 12
5. C. Aprea, M. Strambi, M.T. Novelli, L. Lunghini, and N. Bozzi Biologic monitoring of exposure to organophosphorus pesticides in 195 Italian children Environ. Health Perspect. 108 2000 521 525
6. J.T. Auman, F.J. Seidler, and T.A. Slotkin Neonatal chlorpyrifos exposure targets multiple proteins governing the hepatic adenylyl cyclase signaling cascade: implications for neurotoxicity Dev. Brain Res. 121 2000 19 27
7. J.T. Auman, F.J. Seidler, and T.A. Slotkin Regulation of fetal cardiac and hepatic b-adrenoceptors and adenylyl cyclase signaling: terbutaline effects Am. J. Physiol. 281 2001 R1079 R1089
8. J.T. Auman, F.J. Seidler, C.A. Tate, and T.A. Slotkin β-Adrenoceptor-mediated cell signaling in the neonatal heart and liver: responses to terbutaline Am. J. Physiol. 281 2001 R1895 R1901
9. J.T. Auman, F.J. Seidler, and T.A. Slotkin β-Adrenoceptor control of G-protein function in the neonate: determinant of desensitization or sensitization Am. J. Physiol. 283 2002 R1236 R1244
10. D.J.P. Barker The developmental origins of adult disease Eur. J. Epidemiol. 18 2003 733 736
11. S. Barone, K.P. Das, T.L. Lassiter, and L.D. White Vulnerable processes of nervous system development: a review of markers and methods Neurotoxicology 21 2000 15 36
12. M. Baum, L. Ortiz, and A. Quan Fetal origins of cardiovascular disease Curr. Opin. Pediatr. 15 2003 166 170
13. B. Bergman, H. Bokström, O. Borga, L. Enk, T. Hedner, and B. Wängberg Transfer of terbutaline across the human placenta in late pregnancy Eur. J. Resp. Dis. 65 1984 81 86
14. M. Bey, A.C. Blanchard, J. Darnell, and K. Stephens Myocardial necrosis in a newborn after long-term maternal subcutaneous terbutaline for suppression of premature labor Am. J. Obstet. Gynecol. 167 1992 292
15. C.G. Campbell, F.J. Seidler, and T.A. Slotkin Chlorpyrifos interferes with cell development in rat brain regions Brain Res. Bull. 43 1997 179 189
16. S.N. Caritis, M.J. Darby, and L. Chan Pharmacologic treatment of preterm labor Clin. Obstet. Gynecol. 31 1988 635 651
17. J.E. Casida, and G.B. Quistad Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets Chem. Res. Toxicol. 17 2004 983 998
18. P.M. Clark Programming of the hypothalamo-pituitary-adrenal axis and the fetal origins of adult disease hypothesis Eur. J. Pediatr. 157 1998 S7 S10
19. K. Dam, S.J. Garcia, F.J. Seidler, and T.A. Slotkin Neonatal chlorpyrifos exposure alters synaptic development and neuronal activity in cholinergic and catecholaminergic pathways Dev. Brain Res. 116 1999 9 20
20. M.O. Enrique, V. Morales, E. Ngoumgna, R. Prescilla, E. Tan, E. Hernandez, G.B. Ramirez, H.L. Cifra, and M.L. Manlapaz Prevalence of fetal exposure to environmental toxins as determined by meconium analysis Neurotoxicology 23 2002 329 339
21. M.G.P. Feenstra Functional neuroteratology of drugs acting on adrenergic receptors Neurotoxicology 13 1992 55 63
22. R.A. Fenske, K.G. Black, K.P. Elkner, C. Lee, M.M. Methner, and R. Soto Potential exposure and health risks of infants following indoor residential pesticide applications Am. J. Publ. Health 80 1990 689 693
23. R.A. Fenske, J.C. Kissel, C. Lu, D.A. Kalman, N.J. Simcox, E.H. Allen, and M.C. Keifer Biological based pesticide dose estimates for children in an agricultural community Environ. Health Perspect. 108 2000 515 520
24. S.E. Fletcher, D.A. Fyfe, C.L. Case, H.B. Wiles, J.K. Upshur, and R.B. Newman Myocardial necrosis in a newborn after long-term maternal subcutaneous terbutaline infusion for suppression of preterm labor Am. J. Obstet. Gynecol. 165 1991 1401 1404
25. 2-adrenergic receptor overexpression Endocrinology 144 2003 4097 4105
26. M.C. Garofolo, F.J. Seidler, J.T. Auman, and T.A. Slotkin β-Adrenergic modulation of muscarinic cholinergic receptor expression and function in the developing heart Am. J. Physiol. 282 2002 R1356 R1363
27. M.C. Garofolo, F.J. Seidler, M.M. Cousins, C.A. Tate, D. Qiao, and T.A. Slotkin Developmental toxicity of terbutaline: critical periods for sex-selective effects on macromolecules and DNA synthesis in rat brain, heart, and liver Brain Res. Bull. 59 2003 319 329
28. R.L. Goldenberg The management of preterm labor Obstet. Gynecol. 100 2002 1020 1037
29. D.K. Guinn, A.R. Goepfert, J. Owen, K.D. Wenstrom, and J.C. Hauth Terbutaline pump maintenance therapy for prevention of preterm delivery: a double-blind trial Am. J. Obstet. Gynecol. 179 1998 874 878
30. R.C. Gupta Brain regional heterogeneity and toxicological mechanisms of organophosphates and carbamates Toxicol. Mech. Methods 14 2004 103 143
31. S. Gurunathan, M. Robson, N. Freeman, B. Buckley, A. Roy, R. Meyer, J. Bukowski, and P.J. Lioy Accumulation of chlorpyrifos on residential surfaces and toys accessible to children Environ. Health Perspect. 106 1998 9 16
32. M. Hadders-Algra, B.C. Touwen, and H.J. Huisjes Long-term follow-up of children prenatally exposed to ritodrine Br. J. Obstet. Gynæcol. 93 1986 156 161
33. K. Haram, J.H. Mortensen, and A.L. Wollen Preterm delivery: an overview Acta Obstet. Gynecol. Scand. 82 2003 687 704
34. U. Heudorf, J. Angerer, and H. Drexler Current internal exposure to pesticides in children and adolescents in Germany: urinary levels of metabolites of pyrethroid and organophosphorus insecticides Intl. Arch. Environ. Health 77 2004 67 72
35. R.A. Huff, J.J. Corcoran, J.K. Anderson, and M.B. Abou-Donia Chlorpyrifos oxon binds directly to muscarinic receptors and inhibits cAMP accumulation in rat striatum J. Pharmacol. Exp. Ther. 269 1994 329 335
36. R.A. Huff, A.W. Abu-Qare, and M.B. Abou-Donia Effects of sub-chronic in vivo chlorpyrifos exposure on muscarinic receptors and adenylate cyclase of rat striatum Arch. Toxicol. 75 2001 480 486
37. E.M. Kudlacz, H.A. Navarro, J.P. Eylers, S.S. Dobbins, S.E. Lappi, and T.A. Slotkin Selective linkage of β-adrenergic receptors to functional responses in developing rat lung and liver: phosphatidic acid phosphatase, ornithine decarboxylase and lung liquid reabsorption J. Dev. Physiol. 12 1989 129 134
38. E.M. Kudlacz, H.A. Navarro, and T.A. Slotkin Phosphatidic acid phosphatase in neonatal rat lung: effects of prenatal dexamethasone or terbutaline treatment on basal activity and on responsiveness to beta adrenergic stimulation J. Pharmacol. Exp. Ther. 250 1989 236 240
39. F. Lam, J. Elliott, J.S. Jones, M. Katz, R.A. Knuppel, J. Morrison, R. Newman, J. Phelan, and R. Willcourt Clinical issues surrounding the use of terbutaline sulfate for preterm labor Obstet. Gynecol. Surv. 53 1998 S85 S95
40. F. Lam, N.K. Bergauer, D. Jacques, S.K. Coleman, and G.J. Stanziano Clinical and cost-effectiveness of continuous subcutaneous terbutaline versus oral tocolytics for treatment of recurrent preterm labor in twin gestations J. Perinatol. 21 2001 444 450
41. F. Lam, N.B. Istwan, D. Jacques, S.K. Coleman, and G.J. Stanziano Managing perinatal outcomes: the clinical benefit and cost-effectiveness of pharmacologic treatment of recurrent preterm labor Managed Care 12 2003 39 46
42. S.C. Langley-Evans, D.S. Gardner, and S.J.M. Welham Intrauterine programming of cardiovascular disease by maternal nutritional status Nutrition 14 1998 39 47
43. D.R. Lenselink, R.S. Kuhlmann, J.M. Lawrence, and G.L. Kolesari Cardiovascular teratogenicity of terbutaline and ritodrine in the chick embryo Am. J. Obstet. Gynecol. 171 1994 501 506
44. E.D. Levin, N. Addy, N.C. Christopher, F.J. Seidler, and T.A. Slotkin Persistent behavioral consequences of neonatal chlorpyrifos exposure in rats Dev. Brain Res. 130 2001 83 89
45. A. Meyer, F.J. Seidler, J.E. Aldridge, C.A. Tate, M.M. Cousins, and T.A. Slotkin Critical periods for chlorpyrifos-induced developmental neurotoxicity: alterations in adenylyl cyclase signaling in adult rat brain regions after gestational or neonatal exposure Environ. Health Perspect. 112 2004 295 301
46. A. Meyer, F.J. Seidler, and T.A. Slotkin Developmental effects of chlorpyrifos extend beyond neurotoxicity: critical periods for immediate and delayed-onset effects on cardiac and hepatic cell signaling Environ. Health Perspect. 112 2004 170 178
47. A. Meyer, F.J. Seidler, J.E. Aldridge, and T.A. Slotkin Developmental exposure to terbutaline alters cell signaling in mature rat brain regions and augments the effects of subsequent neonatal exposure to the organophosphorus insecticide, chlorpyrifos Toxicol. Appl. Pharmacol. 203 2005 154 166
48. E. Mills Time course for development of vagal inhibition of the heart in neonatal rats Life Sci. 23 1978 2717 2720
49. H.A. Navarro, E.M. Kudlacz, and T.A. Slotkin Control of adenylate cyclase activity in developing rat heart and liver: effects of prenatal exposure to terbutaline or dexamethasone Biol. Neonate 60 1991 127 136
50. S. Padilla, J. Buzzard, and V.C. Moser Comparison of the role of esterases in the differential age-related sensitivity to chlorpyrifos and methamidophos Neurotoxicology 21 2000 49 56
51. F.P. Perera, V. Rauh, R.M. Whyatt, W.Y. Tsai, J.T. Bernert, Y.H. Tu, H. Andrews, J. Ramirez, L. Qu, and D. Tang Molecular evidence of an interaction between prenatal environmental exposures and birth outcomes in a multiethnic population Environ. Health Perspect. 223 2004 626 630
52. D.I.W. Phillips Endocrine programming and fetal origins of adult disease Trends Endocrinol. Metab. 13 2002 363
53. M. Pitzer, M.H. Schmidt, G. Esser, and M. Laucht Child development after maternal tocolysis with β-sympathomimetic drugs Child Psychiatry Hum. Dev. 31 2001 165 182
54. C.N. Pope Organophosphorus pesticides: do they all have the same mechanism of toxicity? J. Toxicol. Environ. Health 2 1999 161 181
55. A. Queisserluft, I. Eggers, G. Stolz, D. Kieningerbaum, and K. Schlaefer Serial examination of 20,248 newborn fetuses and infants: correlations between drug exposure and major malformations Am. J. Med. Genet. 63 1996 268 276
56. M.C. Rhodes, A. Nyska, F.J. Seidler, and T.A. Slotkin Does terbutaline damage the developing heart? Birth Defects Res. B 68 2003 449 455
57. M.C. Rhodes, F.J. Seidler, A. Abdel-Rahman, C.A. Tate, A. Nyska, H.L. Rincavage, and T.A. Slotkin Terbutaline is a developmental neurotoxicant: effects on neuroproteins and morphology in cerebellum, hippocampus and somatosensory cortex J. Pharmacol. Exp. Ther. 308 2004 529 537
58. M.C. Rhodes, F.J. Seidler, D. Qiao, C.A. Tate, M.M. Cousins, and T.A. Slotkin Does pharmacotherapy for preterm labor sensitize the developing brain to environmental neurotoxicants? Cellular and synaptic effects of sequential exposure to terbutaline and chlorpyrifos in neonatal rats Toxicol. Appl. Pharmacol. 195 2004 203 217
59. P.M. Rodier Structural-functional relationships in experimentally induced brain damage Prog. Brain Res. 73 1988 335 348
60. D.J. Selvage, and C. Rivier Importance of the paraventricular nucleus of the hypothalamus as a component of a neural pathway between the brain and the testes that modulates testosterone secretion independently of the pituitary Endocrinology 144 2003 594 598
61. T.A. Slotkin Endocrine control of synaptic development in the sympathetic nervous system: the cardiac-sympathetic axis P.M. Gootman Developmental Neurobiology of the Autonomic Nervous System 1986 Humana Press Clifton, NJ 97 133
62. T.A. Slotkin Developmental cholinotoxicants: nicotine and chlorpyrifos Environ. Health Perspect. 107 Suppl. 1 1999 71 80
63. T.A. Slotkin Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates Toxicol. Appl. Pharmacol. 198 2004 132 151
64. T.A. Slotkin, E.C. McCook, C.B. Nemeroff, and F.J. Seidler Species differences in a2-adrenergic regulation of platelet adenylate cyclase Res. Comm. Chem. Pathol. Pharmacol. 72 1991 259 271
65. T.A. Slotkin, M.M. Cousins, C.A. Tate, and F.J. Seidler Persistent cholinergic presynaptic deficits after neonatal chlorpyrifos exposure Brain Res. 902 2001 229 243
66. T.A. Slotkin, C.A. Tate, M.M. Cousins, and F.J. Seidler β-Adrenoceptor signaling in the developing brain: sensitization or desensitization in response to terbutaline Dev. Brain Res. 131 2001 113 125
67. T.A. Slotkin, C.A. Tate, M.M. Cousins, and F.J. Seidler Functional alterations in CNS catecholamine systems in adolescence and adulthood after neonatal chlorpyrifos exposure Dev. Brain Res. 133 2002 163 173
68. T.A. Slotkin, J.T. Auman, and F.J. Seidler Ontogenesis of β-adrenoceptor signaling: implications for perinatal physiology and for fetal effects of tocolytic drugs J. Pharmacol. Exp. Ther. 306 2003 1 7
69. T.A. Slotkin, K.K. Brown, and F.J. Seidler Developmental exposure of rats to chlorpyrifos elicits sex-selective hyperlipidemia and hyperinsulinemia in adulthood Environ. Health Perspect. 113 2005 1291 1294
70. T.A. Slotkin, C.A. Oliver, and F.J. Seidler Critical periods for the role of oxidative stress in the developmental neurotoxicity of chlorpyrifos and terbutaline, alone or in combination Dev. Brain Res. 157 2005 172 180
71. G.W. Snedecor, and W.G. Cochran Statistical Methods 6th ed. 1967 Iowa State Univ. Press Ames, Iowa 593 pp.
72. X. Song, F.J. Seidler, J.L. Saleh, J. Zhang, S. Padilla, and T.A. Slotkin Cellular mechanisms for developmental toxicity of chlorpyrifos: targeting the adenylyl cyclase signaling cascade Toxicol. Appl. Pharmacol. 145 1997 158 174
73. K. Tegner, H.T. Nilsson, C.G.A Persson, K. Persson, and Å. Ryrfeldt Elimination pathways of terbutaline Eur. J. Respir. Dis. 65 Suppl. 134 1984 93 100
74. K.A. Usmani, R.L. Rose, and E. Hodgson Inhibition and activation of the human liver microsomal and human cytochrome P450 3A4 metabolism of testosterone by deployment-related chemicals Drug Metab. Dispos. 31 2003 384 391
75. sα prevents full expression of catecholamine desensitization despite increased β-adrenergic receptor kinase J. Clin. Invest. 101 1998 1916 1922
76. V.M. Vizgirda, G.M. Wahler, K.L. Sondgeroth, M.T. Ziolo, and D.W. Schwertz Mechanisms of sex differences in rat cardiac myocyte response to β-adrenergic stimulation Am. J. Physiol. 282 2002 H256 H263
77. D. Wessels, D.B. Barr, and P. Mendola Use of biomarkers to indicate exposure of children to organophosphate pesticides: implications for a longitudinal study of children's environmental health Environ. Health Perspect. 111 2003 1939 1946
78. K.D. Whitney, F.J. Seidler, and T.A. Slotkin Developmental neurotoxicity of chlorpyrifos: cellular mechanisms Toxicol. Appl. Pharmacol. 134 1995 53 62
79. R.M. Whyatt, D.E. Camann, P.L. Kinney, A. Reyes, J. Ramirez, J. Dietrich, D. Diaz, D. Holmes, and F.P. Perera Residential pesticide use during pregnancy among a cohort of urban minority women Environ. Health Perspect. 110 2002 507 514
80. R.M. Whyatt, D.B. Barr, D.E. Camann, P.L. Kinney, J.R. Barr, H.F. Andrews, L.A. Hoepner, R. Garfinkel, Y. Hazi, A. Reyes, J. Ramirez, Y. Cosme, and F.P. Perera Contemporary-use pesticides in personal air samples during pregnancy and blood samples at delivery among urban minority mothers and newborns Environ. Health Perspect. 111 2003 749 756
81. J.L. Zeiders, F.J. Seidler, and T.A. Slotkin Ontogeny of regulatory mechanisms for β-adrenoceptor control of rat cardiac adenylyl cyclase: targeting of G-proteins and the cyclase catalytic subunit J. Mol. Cell. Cardiol. 29 1997 603 615
82. J.L. Zeiders, F.J. Seidler, G. Iaccarino, W.J. Koch, and T.A. Slotkin Ontogeny of cardiac b-adrenoceptor desensitization mechanisms: agonist treatment enhances receptor/G-protein transduction rather than eliciting uncoupling J. Mol. Cell. Cardiol. 31 1999 413 423
83. J.L. Zeiders, F.J. Seidler, and T.A. Slotkin Ontogeny of G-protein expression: control by β-adrenoceptors Dev. Brain Res. 120 2000 125 134
84. H.S. Zhang, J. Liu, and C.N. Pope Age-related effects of chlorpyrifos on muscarinic receptor-mediated signaling in rat cortex Arch. Toxicol. 75 2002 676 684