Effects of developmental stress and lead (Pb) on corticosterone after chronic and acute stress, brain monoamines, and blood Pb levels in rats

International Journal of Developmental Neuroscience

Volumn 29, Issue 1, 2011, Pages 45-55

  Graham, Devon L ^a,c   Grace, Curtis E ^a,c   Braun, Amanda A ^a,c   Schaefer, Tori L ^a,c   Skelton, Matthew R ^a,c   Tang, Peter H ^b,c   Vorhees, Charles V ^a,c   Williams, Michael T ^a,c  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Barren cage rearing; Corticosterone; Dopamine; Lead (Pb); Maternal stress; Serotonin

Indexed keywords

BRAIN MONOAMINE; CORTICOSTERONE; LEAD ACETATE;

ACUTE STRESS; ADRENAL GLAND; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DOPAMINE BRAIN LEVEL; DOPAMINE METABOLISM; ENTORHINAL CORTEX; FEMALE; GROWTH; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LEAD BLOOD LEVEL; MALE; MATERNAL STRESS; NEOSTRIATUM; NEWBORN; NONHUMAN; NORADRENALIN BRAIN LEVEL; ORGAN WEIGHT; PRIORITY JOURNAL; RAT; SEROTONIN BRAIN LEVEL; SEROTONIN METABOLISM; SPLEEN WEIGHT; THYMUS;

ANIMALS; BODY WEIGHT; BRAIN; CORTICOSTERONE; DOPAMINE; FEMALE; HUMANS; LEAD; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

RATTUS;

EID: 78650178909     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2010.09.008     Document Type: Article

References (142)

1. Aisa B., Tordera R., Lasheras B., Del Rio J., Ramirez M.J. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007, 32:256-266.
2. Alario P., Gamallo A., Beato M.J., Trancho G. Body weight gain, food intake and adrenal development in chronic noise stressed rats. Physiology and Behavior 1987, 40:29-32.
3. Andrews M.H., Matthews S.G. Programming of the hypothalamo-pituitary-adrenal axis: serotonergic involvement. Stress 2004, 7:15-27.
4. Anisman H., Zaharia M.D., Meaney M.J., Merali Z. Do early-life events permanently alter behavioral and hormonal responses to stressors?. International Journal of Developmental Neuroscience 1998, 16:149-164.
5. Avishai-Eliner S., Gilles E.E., Eghbal-Ahmadi M., Bar-El Y., Baram T.Z. Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. Journal of Neuroendocrinology 2001, 13:799-807.
6. Barros V.G., Duhalde-Vega M., Caltana L., Brusco A., Antonelli M.C. Astrocyte-neuron vulnerability to prenatal stress in the adult rat brain. Journal of Neuroscience Research 2006, 83:787-800.
7. Baum A., Garofalo J.P., Yali A.M. Socioeconomic status and chronic stress. Does stress account for SES effects on health?. Annals of the New York Academy of Science 1999, 896:131-144.
8. Bayer S.A., Altman J., Russo R.J., Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 1993, 14:83-144.
9. Bellinger D.C. Very low lead exposures and children's neurodevelopment. Current Opinion in Pediatrics 2008, 20:172-177.
10. Brydon L., Edwards S., Mohamed-Ali V., Steptoe A. Socioeconomic status and stress-induced increases in interleukin-6. Brain Behaviour and Immunity 2004, 18:281-290.
11. Bunn T.L., Parsons P.J., Kao E., Dietert R.R. Gender-based profiles of developmental immunotoxicity to lead in the rat: assessment in juveniles and adults. Journal of Toxicology and Environmental Health: Part A 2001, 64:223-240.
12. Bunn T.L., Parsons P.J., Kao E., Dietert R.R. Exposure to lead during critical windows of embryonic development: differential immunotoxic outcome based on stage of exposure and gender. Toxicological Science 2001, 64:57-66.
13. Burns J.M., Baghurst P.A., Sawyer M.G., McMichael A.J., Tong S.L. Lifetime low-level exposure to environmental lead and children's emotional and behavioral development at ages 11-13 years. The Port Pirie Cohort Study. American Journal of Epidemiology 1999, 149:740-749.
14. CDC, 1991. Preventing Lead Poisoning in Young Children: A Statement by the Centers for Disease Control and Prevention, 4th revision. Vol. 1991. Centers for Disease Control and Prevention, Atlanta, GA.
15. Cecil K.M., Brubaker C.J., Adler C.M., Dietrich K.N., Altaye M., Egelhoff J.C., Wessel S., Elangovan I., Hornung R., Jarvis K., Lanphear B.P. Decreased brain volume in adults with childhood lead exposure. PLoS Medicine 2008, 5:e112.
16. Chaouloff F. Physiopharmacological interactions between stress hormones and central serotonergic systems. Brain Research Review 1993, 18:1-32.
17. Chiodo L.M., Covington C., Sokol R.J., Hannigan J.H., Jannise J., Ager J., Greenwald M., Delaney-Black V. Blood lead levels and specific attention effects in young children. Neurotoxicology and Teratology 2007, 29:538-546.
18. Choi D.C., Furay A.R., Evanson N.K., Ulrich-Lai Y.M., Nguyen M.M., Ostrander M.M., Herman J.P. The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology 2008, 33:659-669.
19. Clancy B., Kersh B., Hyde J., Darlington R.B., Anand K.J., Finlay B.L. Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 2007, 5:79-94.
20. Cohen S., Doyle W.J., Baum A. Socioeconomic status is associated with stress hormones. Psychosomatic Medicine 2006, 68:414-420.
21. Cooper, J.R., Bloom, F.E., Roth, R.H., 2003. The Biochemical Basis of Neuropharmacology, Vol. Oxford University Press, New York.
22. Cory-Slechta D.A., Weiss B., Cox C. Performance and exposure indices of rats exposed to low concentrations of lead. Toxicology and Applied Pharmacology 1985, 78:291-299.
23. Cory-Slechta D.A., Weiss B. Efficacy of the chelating agent CaEDTA in reversing lead-induced changes in behavior. Neurotoxicology 1989, 10:685-697.
24. Cory-Slechta D.A., Brockel B.J., O'Mara D.J. Lead exposure and dorsomedial striatum mediation of fixed interval schedule-controlled behavior. Neurotoxicology 2002, 23:313-327.
25. Cory-Slechta D.A., Virgolini M.B., Thiruchelvam M., Weston D.D., Bauter M.R. Maternal stress modulates the effects of developmental lead exposure. Environmental Health Perspectives 2004, 112:717-730.
26. Cory-Slechta D.A., Virgolini M.B., Rossi-George A., Weston D., Thiruchelvam M. Experimental manipulations blunt time-induced changes in brain monoamine levels and completely reverse stress, but not Pb+/-stress-related modifications to these trajectories. Behavioural Brain Research 2009, 205:76-87.
27. De Kloet E.R., Rosenfeld P., Van Eekelen J.A., Sutanto W., Levine S. Stress, glucocorticoids and development. Progress in Brain Research 1988, 73:101-120.
28. Dhabhar F.S., McEwen B.S. Stress-induced enhancement of antigen-specific cell-mediated immunity. Journal of Immunology 1996, 156:2608-2615.
29. Dhabhar F.S., McEwen B.S. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behaviour and Immunity 1997, 11:286-306.
30. Dhabhar F.S., McEwen B.S., Spencer R.L. Adaptation to prolonged or repeated stress-comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinolog 1997, 65:360-368.
31. Dietrich K.N., Ris M.D., Succop P.A., Berger O.G., Bornschein R.L. Early exposure to lead and juvenile delinquency. Neurotoxicological Teratology 2001, 23:511-518.
32. Ergurhan-Ilhan I., Cadir B., Koyuncu-Arslan M., Arslan C., Gultepe F.M., Ozkan G. Level of oxidative stress and damage in erythrocytes in apprentices indirectly exposed to lead. Pediatrics International 2008, 50:45-50.
33. Fietta P. Glucocorticoids and brain functions. Rivista di Biologia 2007, 100:403-418.
34. Fyhn M., Molden S., Witter M.P., Moser E.I., Moser M.B. Spatial representation in the entorhinal cortex. Science 2004, 305:1258-1264.
35. Gedeon Y., Ramesh G.T., Wellman P.J., Jadhav A.L. Changes in mesocorticolimbic dopamine and D1/D2 receptor levels after low level lead exposure: a time course study. Toxicology Letters 2001, 123:217-226.
36. Gilbert M.E., Kelly M.E., Samsam T.E., Goodman J.H. Chronic developmental lead exposure reduces neurogenesis in adult rat hippocampus but does not impair spatial learning. Toxicological Sciences 2005, 86:365-374.
37. Gilbert M.E., Lasley S.M. Developmental lead (Pb) exposure reduces the ability of the NMDA antagonist MK-801 to suppress long-term potentiation (LTP) in the rat dentate gyrus, in vivo. Neurotoxicology and Teratology 2007, 29:385-393.
38. Gilles E.E., Schultz L., Baram T.Z. Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatric Neurology 1996, 15:114-119.
39. Gos T., Bock J., Poeggel G., Braun K. Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse 2008, 62:229-232.
40. Goyer R.A. Results of lead research: prenatal exposure and neurological consequences. Environmental Health Perspectives 1996, 104:1050-1054.
41. Grace, C.E., Schaefer, T.L., Graham, D.L., Skelton, M.R., Williams, M.T., Vorhees, C.V., 2010. Effects of inhibiting neonatal methamphetamine-induced corticosterone release in rats by adrenal autotransplantation on later learning, memory, and plasma corticosterone levels. International Journal of Developmental Neuroscience, [Epub ahead of print].
42. Gruss M., Braun K., Frey J.U., Korz V. Maternal separation during a specific postnatal time window prevents reinforcement of hippocampal long-term potentiation in adolescent rats. Neuroscience 2008, 152:1-7.
43. Gruver A.L., Sempowski G.D. Cytokines, leptin, and stress-induced thymic atrophy. Journal of Leukocyte Biology 2008, 84:915-923.
44. Gump B.B., Stewart P., Reihman J., Lonky E., Darvill T., Matthews K.A., Parsons P.J. Prenatal and early childhood blood lead levels and cardiovascular functioning in 9(1/2) year old children. Neurotoxicology and Teratology 2005, 27:655-665.
45. Gump B.B., Stewart P., Reihman J., Lonky E., Darvill T., Parsons P.J., Granger D.A. Low-level prenatal and postnatal blood lead exposure and adrenocortical responses to acute stress in children. Environmental Health Perspectives 2008, 116:249-255.
46. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
47. Heidmets L.T., Zharkovsky T., Jurgenson M., Jaako-Movits K., Zharkovsky A. Early post-natal, low-level lead exposure increases the number of PSA-NCAM expressing cells in the dentate gyrus of adult rat hippocampus. Neurotoxicology 2006, 27:39-43.
48. Heo Y., Parsons P.J., Lawrence D.A. Lead differentially modifies cytokine production in vitro and in vivo. Toxicology and Applied Pharmacology 1996, 138:149-157.
49. Herman J.P., Watson S.J., Spencer R.L. Defense of adrenocorticosteroid receptor expression in rat hippocampus: effects of stress and strain. Endocrinology 1999, 140:3981-3991.
50. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Frontiers in Neuroendocrinology 2003, 24:151-180.
51. Hodges J.R., Mitchley S. Recovery of hypothalamo-pituitary-adrenal function in the rat after prolonged treatment with betamethasone. British Journal of Pharmacology 1970, 40:732-739.
52. Ivy A.S., Brunson K.L., Sandman C., Baram T.Z. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 2008, 154:1132-1142.
53. Jacobs D.E., Clickner R.P., Zhou J.Y., Viet S.M., Marker D.A., Rogers J.W., Zeldin D.C., Broene P., Friedman W. The prevalence of lead-based paint hazards in U.S. housing. Environmental Health Perspectives 2002, 110:A599-606.
54. Jett D.A., Kuhlmann A.C., Farmer S.J., Guilarte T.R. Age-dependent effects of developmental lead exposure on performance in the Morris water maze. Pharmacology, Biochemistry and Behavior 1997, 57:271-279.
55. Johnson E.A., O'Callaghan J.P., Miller D.B. Chronic treatment with supraphysiological levels of corticosterone enhances D-MDMA-induced dopaminergic neurotoxicity in the C57BL/6J female mouse. Brain Research 2002, 933:130-138.
56. Jusko T.A., Henderson C.R., Lanphear B.P., Cory-Slechta D.A., Parsons P.J., Canfield R.L. Blood lead concentrations<10μg/dL and child intelligence at 6 years of age. Environmental Health Perspectives 2008, 116:243-248.
57. Karatsoreos I.N., Bhagat S.M., Bowles N.P., Weil Z.M., Pfaff D.W., McEwen B.S. Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 2010, 151:2117-2127.
58. Kwon M.S., Seo Y.J., Lee J.K., Lee H.K., Jung J.S., Jang J.E., Park S.H., Suh H.W. The repeated immobilization stress increases IL-1beta immunoreactivities in only neuron, but not astrocyte or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neuroscience Letters 2008, 430:258-263.
59. Lanphear B.P., Byrd R.S., Auinger P., Schaffer S.J. Community characteristics associated with elevated blood lead levels in children. Pediatrics 1998, 101:264-271.
60. Lanphear B.P., Dietrich K., Auinger P., Cox C. Cognitive deficits associated with blood lead concentrations<10μg/dL in US children and adolescents. Public Health Reports 2000, 115:521-529.
61. Lee J.E., Dietert R.R. Developmental immunotoxicity of lead: impact on thymic function. Birth Defects Research Part A: Clinical and Molecular Teratology 2003, 67:861-867.
62. Levin R., Brown M.J., Kashtock M.E., Jacobs D.E., Whelan E.A., Rodman J., Schock M.R., Padilla A., Sinks T. Lead exposures in U.S. Children, 2008: implications for prevention. Environmental Health Perspectives 2008, 116:1285-1293.
63. Lindahl L.S., Bird L., Legare M.E., Mikeska G., Bratton G.R., Tiffany-Castiglioni E. Differential ability of astroglia and neuronal cells to accumulate lead: dependence on cell type and on degree of differentiation. Toxicological Sciences 1999, 50:236-243.
64. Lupien S.J., Nair N.P., Briere S., Maheu F., Tu M.T., Lemay M., McEwen B.S., Meaney M.J. Increased cortisol levels and impaired cognition in human aging: implication for depression and dementia in later life. Reviews Neuroscience 1999, 10:117-139.
65. Lupien S.J., King S., Meaney M.J., McEwen B.S. Child's stress hormone levels correlate with mother's socioeconomic status and depressive state. Biological Psychiatry 2000, 48:976-980.
66. Lupien S.J., King S., Meaney M.J., McEwen B.S. Can poverty get under your skin? basal cortisol levels and cognitive function in children from low and high socioeconomic status. Development and Psychopathology 2001, 13:653-676.
67. Lutz P.M., Wilson T.J., Ireland J., Jones A.L., Gorman J.S., Gale N.L., Johnson J.C., Hewett J.E. Elevated immunoglobulin E (IgE) levels in children with exposure to environmental lead. Toxicology 1999, 134:63-78.
68. Ma T., Chen H.H., Ho I.K. Effects of chronic lead (Pb) exposure on neurobehavioral function and dopaminergic neurotransmitter receptors in rats. Toxicology Letters 1999, 105:111-121.
69. Mantovani M., Matteussi A.S., Rodrigues A.L. Antidepressant-like effect of lead in adult mice. Brazilian Journal of Medical and Biological Research 1999, 32:1555-1560.
70. Massaro E.J., Miller G.D., Massaro T.F. Multiple dose exposure effects on the tissue distribution of lead in the preweanling rat. Neurotoxicology 1984, 5:333-351.
71. Massaro T.F., Miller G.D., Massaro E.J. Low-level lead exposure affects latent learning in the rat. Neurobehavioral Toxicology and Teratology 1986, 8:109-113.
72. McEwen B.S., Weiss J.M., Schwartz L.S. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968, 220:911-912.
73. McEwen B.S., Angulo J., Cameron H., Chao H.M., Daniels D., Gannon M.N., Gould E., Mendelson S., Sakai R., Spencer R., et al. Paradoxical effects of adrenal steroids on the brain: protection versus degeneration. Biological Psychiatry 1992, 31:177-199.
74. McEwen B.S., Stellar E. Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine 1993, 153:2093-2101.
75. McEwen B.S. Stress, adaptation, and disease. Allostasis and allostatic load. Annals of New York Academy Sciences 1998, 840:33-44.
76. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews 2007, 87:873-904.
77. Melnyk L.J., Berry M.R., Sheldon L.S., Freeman N.C., Pellizzari E.D., Kinman R.N. Dietary exposure of children in lead-laden environments. Journal of Exposure Analysis and Environmental Epidemiology 2000, 10:723-731.
78. Mendez-Gomez J., Garcia-Vargas G.G., Lopez-Carrillo L., Calderon-Aranda E.S., Gomez A., Vera E., Valverde M., Cebrian M.E., Rojas E. Genotoxic effects of environmental exposure to arsenic and lead on children in region Lagunera, Mexico. Annals of the New York Academy of Sciences 2008, 1140:358-367.
79. Mendola P., Selevan S.G., Gutter S., Rice D. Environmental factors associated with a spectrum of neurodevelopmental deficits. Mental Retardation and Developmental Disabilities Research Reviews 2002, 8:188-197.
80. Menke A., Muntner P., Batuman V., Silbergeld E.K., Guallar E. Blood lead below 0.48μmol/L (10μg/dL) and mortality among US adults. Circulation 2006, 114:1388-1394.
81. Merrett D.L., Kirkland S.W., Metz G.A. Synergistic effects of age and stress in a rodent model of stroke. Behavioural Brain Research 2010, 214:55-59.
82. Meyer P.A., McGeehin M.A., Falk H. A global approach to childhood lead poisoning prevention. International Journal of Hygiene and Environmental Health 2003, 206:363-369.
83. Miller A.H., Spencer R.L., Trestman R.L., Kim C., McEwen B.S., Stein M. Adrenal steroid receptor activation in vivo and immune function. American Journal of Physiology 1991, 261:E126-E131.
84. Miller D.B., O'Callaghan J.P. Neuroendocrine aspects of the response to stress. Metabolism 2002, 51:5-10.
85. Min M.O., Singer L.T., Kirchner H.L., Minnes S., Short E., Hussain Z., Nelson S. Cognitive development and low-level lead exposure in poly-drug exposed children. Neurotoxicology and Teratology 2009, 31:225-231.
86. Mineur Y.S., Prasol D.J., Belzung C., Crusio W.E. Agonistic behavior and unpredictable chronic mild stress in mice. Behavioral Genetics 2003, 33:513-519.
87. Mineur Y.S., Belzung C., Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behavioural Brain Research 2006, 175:43-50.
88. Mitchell J.B., Betito K., Rowe W., Boksa P., Meaney M.J. Serotonergic regulation of type II corticosteroid receptor binding in hippocampal cell cultures: evidence for the importance of serotonin-induced changes in cAMP levels. Neuroscience 1992, 48:631-639.
89. Morford L.L., Inman-Wood S.L., Gudelsky G.A., Williams M.T., Vorhees C.V. Impaired spatial and sequential learning in rats treated neonatally with D-fenfluramine. European Journal of Neuroscience 2002, 16:491-500.
90. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
91. Muntner P., Menke A., DeSalvo K.B., Rabito F.A., Batuman V. Continued decline in blood lead levels among adults in the United States: the National Health and Nutrition Examination Surveys. Archives of Internal Medicine 2005, 165:2155-2161.
92. Naitoh Y., Fukata J., Tominaga T., Nakai Y., Tamai S., Mori K., Imura H. Interleukin-6 stimulates the secretion of adrenocorticotropic hormone in conscious, freely-moving rats. Biochemical and Biophysical Research Communications 1988, 155:1459-1463.
93. Navarra P., Tsagarakis S., Faria M.S., Rees L.H., Besser G.M., Grossman A.B. Interleukins-1 and -6 stimulate the release of corticotropin-releasing hormone-41 from rat hypothalamus in vitro via the eicosanoid cyclooxygenase pathway. Endocrinology 1991, 128:37-44.
94. Needleman H.L., Gunnoe C., Leviton A., Reed R., Peresie H., Maher C., Barrett P. Deficits in psychologic and classroom performance of children with elevated dentine lead levels. New England Journal of Medicine 1979, 300:689-695.
95. Nigg J.T., Knottnerus G.M., Martel M.M., Nikolas M., Cavanagh K., Karmaus W., Rappley M.D. Low blood lead levels associated with clinically diagnosed attention-deficit/hyperactivity disorder and mediated by weak cognitive control. Biological Psychiatry 2008, 63:325-331.
96. Nihei M.K., Desmond N.L., McGlothan J.L., Kuhlmann A.C., Guilarte T.R. N-methyl-d-aspartate receptor subunit changes are associated with lead-induced deficits of long-term potentiation and spatial learning. Neuroscience 2000, 99:233-242.
97. Patel A., Athawale A. Blood lead levels in children with encephalopathy. Indian Pediatrics 2009, 46:845-848.
98. Path G., Bornstein S.R., Ehrhart-Bornstein M., Scherbaum W.A. Interleukin-6 and the interleukin-6 receptor in the human adrenal gland: expression and effects on steroidogenesis. Journal of Clinical Endocrinology and Metabolism 1997, 82:2343-2349.
99. Path G., Scherbaum W.A., Bornstein S.R. The role of interleukin-6 in the human adrenal gland. European Journal of Clinical Investigation 2000, 30(3 Suppl):91-95.
100. Plusquellec P., Muckle G., Dewailly E., Ayotte P., Jacobson S.W., Jacobson J.L. The relation of low-level prenatal lead exposure to behavioral indicators of attention in Inuit infants in Arctic Quebec. Neurotoxicology and Teratology 2007, 29:527-537.
101. Pruett S., Hebert P., Lapointe J.M., Reagan W., Lawton M., Kawabata T.T. Characterization of the action of drug-induced stress responses on the immune system: evaluation of biomarkers for drug-induced stress in rats. Journal of Immunotoxicology 2007, 4:25-38.
102. Rabinowitz M.B., Wetherill G.W., Kopple J.D. Kinetic analysis of lead metabolism in healthy humans. Journal of Clinical Investigation 1976, 58:260-270.
103. Reiter L.W., Anderson G.E., Laskey J.W., Cahill D.F. Developmental and behavioral changes in the rat during chronic exposure to lead. Environmental Health Perspectives 1975, 12:119-123.
104. Rice C.J., Sandman C.A., Lenjavi M.R., Baram T.Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 2008, 149:4892-4900.
105. Rice D.C. Chronic low-lead exposure from birth produces deficits in discrimination reversal in monkeys. Toxicology and Applied Pharmacology 1985, 77:201-210.
106. Rossi-George A., Virgolini M.B., Weston D., Cory-Slechta D.A. Alterations in glucocorticoid negative feedback following maternal Pb, prenatal stress and the combination: a potential biological unifying mechanism for their corresponding disease profiles. Toxicology and Applied Pharmacology 2009, 234:117-127.
107. Sahu J.K., Sharma S., Kamate M., Kumar A., Gulati S., Kabra M., Kalra V. Lead encephalopathy in an infant mimicking a neurometabolic disorder. Journal of Child Neurology 2010, 25:390-392.
108. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research 1986, 396:64-76.
109. Schaefer T.L., Ehrman L.A., Gudelsky G.A., Vorhees C.V., Williams M.T. Comparison of monoamine and corticosterone levels 24h following (+)methamphetamine, (+/-)3, 4-methylenedioxymethamphetamine, cocaine, (+)fenfluramine or (+/-)methylphenidate administration in the neonatal rat. Journal of Neurochemistry 2006, 98:1369-1378.
110. Schnaas L., Rothenberg S.J., Flores M.F., Martinez S., Hernandez C., Osorio E., Perroni E. Blood lead secular trend in a cohort of children in Mexico City (1987-2002). Environmental Health Perspectives 2004, 112:1110-1115.
111. Selye H. The significance of the adrenals for adaptation. Science 1937, 85:247-248.
112. Shih R.A., Glass T.A., Bandeen-Roche K., Carlson M.C., Bolla K.I., Todd A.C., Schwartz B.S. Environmental lead exposure and cognitive function in community-dwelling older adults. Neurology 2006, 67:1556-1562.
113. Singh V.B., Hao-Phan T., Corley K.C., Boadle-Biber M.C. Increase in cortical and midbrain tryptophan hydroxylase activity by intracerebroventricular administration of corticotropin releasing factor: block by adrenalectomy, by RU 38486 and by bilateral lesions to the central nucleus of the amygdala. Neurochemistry International 1992, 20:81-92.
114. Skelton M.R., Williams M.T., Schaefer T.L., Vorhees C.V. Neonatal (+)-methamphetamine increases brain derived neurotrophic factor, but not nerve growth factor, during treatment and results in long-term spatial learning deficits. Psychoneuroendocrinology 2007, 32:734-745.
115. Solomon M.B., Jones K., Packard B.A., Herman J.P. The medial amygdala modulates body weight but not neuroendocrine responses to chronic stress. Journal of Neuroendocrinology 2010, 22:13-23.
116. Stewart W.F., Schwartz B.S., Davatzikos C., Shen D., Liu D., Wu X., Todd A.C., Shi W., Bassett S., Youssem D. Past adult lead exposure is linked to neurodegeneration measured by brain MRI. Neurology 2006, 66:1476-1484.
117. Stewart W.F., Schwartz B.S. Effects of lead on the adult brain: a 15-year exploration. American Journal Industrial Medicine 2007, 50:729-739.
118. Struzynska L., Dabrowska-Bouta B., Koza K., Sulkowski G. Inflammation-like glial response in lead-exposed immature rat brain. Toxicological Science 2007, 95:156-162.
119. Sun H.W., Ma D.J., Chao C.Y., Liu S., Yuan Z.B. Lead distribution in blood and organs of mice exposed to lead by vein injection. Environmental Technology 2009, 30:1051-1057.
120. Surkan P.J., Zhang A., Trachtenberg F., Daniel D.B., McKinlay S., Bellinger D.C. Neuropsychological function in children with blood lead levels<10mug/dL. Neurotoxicology 2007, 28:1170-1177.
121. Szczerbak G., Nowak P., Kostrzewa R.M., Brus R. Maternal lead exposure produces long-term enhancement of dopaminergic reactivity in rat offspring. Neurochemical Research 2007, 32:1791-1798.
122. Talcott P.A., Koller L.D. The effect of inorganic lead and/or a polychlorinated biphenyl on the developing immune system of mice. Journal of Toxicology and Environmental Health 1983, 12:337-352.
123. Tong S., McMichael A.J., Baghurst P.A. Interactions between environmental lead exposure and sociodemographic factors on cognitive development. Archives of Environmental Health 2000, 55:330-335.
124. Toscano C.D., Guilarte T.R. Lead neurotoxicity: from exposure to molecular effects. Brain Research Brain Research Review 2005, 49:529-554.
125. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C., Herman J.P. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. American Journal of Physiology, Endocrinology and Metabolism 2006, 291:E965-E973.
126. van Wijngaarden E., Campbell J.R., Cory-Slechta D.A. Bone lead levels are associated with measures of memory impairment in older adults. Neurotoxicology 2009, 30:572-580.
127. Vega-Dienstmaier J.M., Salinas-Pielago J.E., Gutierrez-Campos Mdel R., Mandamiento-Ayquipa R.D., Yara-Hokama Mdel C., Ponce-Canchihuaman J., Castro-Morales J. Lead levels and cognitive abilities in Peruvian children. Revista Brasileira de Psiquiatria 2006, 28:33-39.
128. Verina T., Rohde C.A., Guilarte T.R. Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats. Neuroscience 2007, 145:1037-1047.
129. Virgolini M.B., Chen K., Weston D.D., Bauter M.R., Cory-Slechta D.A. Interactions of chronic lead exposure and intermittent stress: consequences for brain catecholamine systems and associated behaviors and HPA axis function. Toxicological Science 2005, 87:469-482.
130. Virgolini M.B., Bauter M.R., Weston D.D., Cory-Slechta D.A. Permanent alterations in stress responsivity in female offspring subjected to combined maternal lead exposure and/or stress. Neurotoxicology 2006, 27:11-21.
131. Virgolini M.B., Rossi-George A., Lisek R., Weston D.D., Thiruchelvam M., Cory-Slechta D.A. CNS effects of developmental Pb exposure are enhanced by combined maternal and offspring stress. Neurotoxicology 2008, 29:812-827.
132. Virgolini M.B., Rossi-George A., Weston D., Cory-Slechta D.A. Influence of low level maternal Pb exposure and prenatal stress on offspring stress challenge responsivity. Neurotoxicology 2008, 29:928-939.
133. Wang L., Xu S.E., Zhang G.D., Wang W.Y. Study of lead absorption and its effect on children's development. Biomedical and Environmental Sciences 1989, 2:325-330.
134. Williams M.T., Inman-Wood S.L., Morford L.L., McCrea A.E., Ruttle A.M., Moran M.S., Rock S.L., Vorhees C.V. Preweaning treatment with methamphetamine induces increases in both corticosterone and ACTH in rats. Neurotoxicology and Teratology 2000, 22:751-759.
135. Williams M.T., Blankenmeyer T.L., Schaefer T.L., Brown C.A., Gudelsky G.A., Vorhees C.V. Long-term effects of neonatal methamphetamine exposure in rats on spatial learning in the Barnes maze and on cliff avoidance, corticosterone release, and neurotoxicity in adulthood. Brain Research Developmental Brain Research 2003, 147:163-175.
136. Wilson D.R., Warise L. Cytokines and their role in depression. Perspectives in Psychiatric Care 2008, 44:285-289.
137. Winneke G., Beginn U., Ewert T., Havestadt C., Kraemer U., Krause C., Thron H.L., Wagner H.M. Comparing the effects of perinatal and later childhood lead exposure on neuropsychological outcome. Environmental Research 1985, 38:155-167.
138. Wright J.P., Dietrich K.N., Ris M.D., Hornung R.W., Wessel S.D., Lanphear B.P., Ho M., Rae M.N. Association of prenatal and childhood blood lead concentrations with criminal arrests in early adulthood. PLoS Medicines 2008, 5:e101.
139. Yuan W., Holland S.K., Cecil K.M., Dietrich K.N., Wessel S.D., Altaye M., Hornung R.W., Ris M.D., Egelhoff J.C., Lanphear B.P. The impact of early childhood lead exposure on brain organization: a functional magnetic resonance imaging study of language function. Pediatrics 2006, 118:971-977.
140. Yun S., Lannert H., Hoyer S. Chronic exposure to low-level lead impairs learning ability during aging and energy metabolism in aged rat brain. Archives of Gerontology and Geriatrics 2000, 30:199-213.
141. Zhou M., Suszkiw J.B. Nicotine attenuates spatial learning deficits induced in the rat by perinatal lead exposure. Brain Research 2004, 999:142-147.
142. Zhu Z.W., Yang R.L., Dong G.J., Zhao Z.Y. Study on the neurotoxic effects of low-level lead exposure in rats. Journals of Zhejiang University Science B 2005, 6:686-692.