Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice

Environmental Health Perspectives

Volumn 116, Issue 3, 2008, Pages 355-361

  Leasure, J Leigh ^a,b   Giddabasappa, Anand ^b,c   Chaney, Shawntay ^b,c   Johnson Jr , Jerry E ^c,d   Pothakos, Konstantinos ^a   Lau, Yuen Sum ^a   Fox, Donald A ^a,b,c  

^a UNIVERSITY OF HOUSTON   (United States)

^b University of Houston   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

^d UNIVERSITY OF HOUSTON DOWNTOWN   (United States)

Author keywords

Aging; Amphetamine; Balance; Dopamine; Fetal; Gestation; Lead; Motor activity; Obesity; Sex

Indexed keywords

AMPHETAMINE; DOPAMINE; LEAD;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; COORDINATION DISORDER; FEMALE; FOREBRAIN; LEAD BLOOD LEVEL; LEAD POISONING; LOCOMOTION; MALE; MATING; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NEUROCHEMISTRY; NEUROTOXICITY; NONHUMAN; OBESITY; PREGNANCY; PRIORITY JOURNAL; RISK ASSESSMENT; ROTAROD TEST; SEX DIFFERENCE; TREADMILL;

ANIMALS; BODY WEIGHT; CORPUS STRIATUM; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; LEAD POISONING; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSENCEPHALON; SEX FACTORS; TIME FACTORS;

MURINAE; MUS;

EID: 40849130254     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.10862     Document Type: Article

References (75)

1. Antonio MT, Leret ML. 2000. Study of the neurochemical alterations produced in discrete brain areas by perinatal low-level lead exposure. Life Sci 67:635-642.
2. Baghurst PA, McMichael AJ, Tong S, Wigg NR, Vimpani GV, Robertson EF. 1995. Exposure to environmental lead and visual-motor integration at age 7 years: the Port Pirie Cohort Study. Epidemiology 6:104-109.
3. Baghurst PA, McMichael AJ, Wigg NR, Vimpani GV, Robertson EF, Roberts RJ, et al. 1992. Environmental exposure to lead and children's intelligence at the age of seven years. The Port Fine Cohort Study. N Engl J Med 327:1279-1284.
4. Baillio-Hamilton PF. 2002. Chemical toxins: a hypothesis to explain the global obesity epidemic. J Altern Complement Med 8:185-192.
5. Barkley RA, Grodzinsky G, DuPaul GJ. 1992. Frontal lobe functions in attention deficit disorder with and without hyperactivity: a review and research report. J Abnorm Child Psychol 20:163-186.
6. Barone S Jr, Stanton ME, Mundy WR. 1995. Neurotoxic effects of neonatal triethyltin (TET) exposure are exacerbated with aging. Neurobiol Aging 16:723-735.
7. Basha MR, Wei W, Bakheet SA, Benitez N, Siddiqi HK, Ge YW. et al. 2005. The fetal basis of amyloidogenesis: exposure to lead and latent overexpression of amyloid precursor protein and beta-amyloid in the aging brain. J Neurosci 25:823-829.
8. Bellinger D, Hu H, Titlebaum L, Needleman HL. 1994. Attentional correlates of dentin and bone lead levels in adolescents. Arch Environ Health 49:98-105.
9. Bhattacharya A, Shulkla R, Bornschein RL, Dietrich KN, Keith R. 1990. Lead effects on postural balance of children. Environ Health Perspect 89:35-42.
10. Bhattacharya A, Shukla R, Dietrich KN, Bornschein RL. 2006. Effect of early lead exposure on the maturation of children's postural balance: a longitudinal study. Neurotoxicol Teratol 28:376-385.
11. Boireau A, Dubedat P, Laduron PM, Doble A, Blanchard JC. 1990. Preferential decrease in dopamine utilization in profrontal cortex by zopiclone, diazepam and zolpidem in unstressed rats. J Pharm Pharmacol 42:562-565.
12. Bornschein RL, Fox DA, Michaelson IA. 1977. Estimation of daily exposure in neonatal rats receiving lead via dam's milk. Toxicol Appl Pharmacol 40:577-587.
13. Braun JM, Kahn RS, Froehlich T, Auinger P, Lanphear BP. 2006. Exposures to environmental toxicants and attention deficit hyperactivity disorder in U.S. children. Environ Health Perspect 114:1904-1909.
14. Calle EE, Kaaks R. 2004. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4:579-591.
15. Canfield RL, Henderson CR Jr, Cory-Slechta DA, Cox C, Jusko TA. Lanchear BP. 2003. Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N Engl J Med 348:1517-1526.
16. Carmichael NG, Winder C, Lewis PD. 1981. Dose response relationships during perinatal lead administration in the rat: a model for the study of lead effects on brain development. Toxicology 21:117-128.
17. CDC. 1991. Preventing Lead Poisoning in Young Children: a Statement by the Centers for Disease Control and Prevention. Atlanta, GA:Centers for Disease Control and Prevention.
18. Correa A, Min YI, Stewart PA, Lees PS, Breysse P, Dosemaci M, et al. 2006. Inter-rater agreement of assessed prenatal maternal occupational exposures to lead. Birth Defects Res A Clin Mol Teratol 76:811-824.
19. Cory-Slechta DA. 1997. Relationships between Pb-induced changes in neurotransmitter system function and behavioral toxicity. Neurotoxicology 18:673-688.
20. Cory-Slechta DA, Virgolini MB, Thiruchelvam M, Weston DD, Bauter MR. 2004. Maternal stress modulates the effects of developmental lead exposure. Environ Health Perspect 112:717-730.
21. Crofton KM, Taylor DH, Bull RJ, Sivulka DJ, Lutkenhoff SD. 1980. Developmental delays in exploration and locomotor activity in male rats exposed to low level lead. Life Sci 26:823-831.
22. Davis JM, Svendsgaard DJ. 1990, U-shaped dose-response curves: their occurrence and implications for risk assessment, J Toxicol Environ Health 30:71-83.
23. Dietrich KN, Succop PA, Berger OG, Keith RW. 1992. Lead exposure and the central auditory processing abilities and cognitive-development of urban children: the Cincinnati Lead Study cohort at age 5 years. Neurotoxicol Teratol 14:51-56.
24. Dobbing J, Sands,J.1979. Comparative aspects of the brain growth spurt. Early Hum Dev 3:79-83.
25. el-Refai MF, Chan TM. 1986. Possible involvement of a hypothalamic dopaminergic receptor in development of genetic obesity in mice. Biochim Biophys Acta 880:16-25.
26. Frayling TM, Timpson NJ, Weedon MN, Zeggini E, Freathy RM, Lindgren CM, et al. 2007. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316(5826):880-894.
27. Gilbert SG, Weiss B, 2006. A rationale for lowering the blood lead action level from 10 to 2 microg/dL. Neurotoxicology 27:693-701.
28. Glick SD, Milloy S. 1973. Rate-dependent effects of d-amphetamine on locomotor activity in mice: possible relationship to paradoxical amphetamine sedation in minimal brain dysfunction. Eur J Pharmacol 24:266-268.
29. Govoni S, Lucchi L, Battaini F, Spano PF, Trabucchi M. 1984. Chronic lead treatment affects dopaminergic control of prolactin secretion in rat pituitary. Toxicol Lett 20:237-241.
30. Grun F, Watanabe H, Zamanian Z, Maeda L, Arima K, Cubacha R, et al. 2006. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol 20:2141-2155.
31. He L, Perkins GA, Poblenz AT, Harris JB, Ellisman MH, Fox DA. 2003. Bcl-xL overexpression blocks bax-mediated mitochondrial contact site formation and apoptosis in rod photoreceptors of lead-exposed mice. Proc Natl Acad Sci USA 100:1022-1027.
32. Hadley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. 2004. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. JAMA 291:2847-2850.
33. Heindel JJ 2003. Endocrine disruptors and the obesity epidemic. Toxicol Sci 76:247-249.
34. Hu H, Tellez-Rojo MM, Bellinger D, Smith D, Ettinger AS, Lamadrid-Figueroa H, et al. 2006, Fetal lead exposure at each stage of pregnancy as a predictor of infant mental development. Environ Health Perspect 114:1730-1735.
35. Jadhav AL, Ramesh GT. 1997, Pb-induced alterations in tyrosine hydroxylase activity in rat brain. Mol Cell Biochem 175:137-141.
36. Kelley BM, Middaugh LD. 1996. Ethanol self-administration and motor deficits in adults C57BL/6J mice exposed prenatally to cocaine. Pharmacol Biochem Behav 55:575-584.
37. Kessler RC, Adler L, Barkley R, Biederman J, Conners CK, Demler O, et al. 2006 The prevalence and correlates of adult ADHD in the United States: results from the National Comorbidity Survey Replication. Am J Psychiatry 163:716-723.
38. Korpela H, Loueniva R, Yrjanheikki E, Kauppila A. 1986. Lead and cadmium concentrations in maternal and umbilical cord blood, amniotic fluid, placenta, and amniotic membranes. Am J Obstet Gynecol 155:1086-1089.
39. Kuhlmann AC, McGlothan JL, Guilarte TR. 1997. Developmental lead exposure causes spatial learning deficits in adult rats. Neurosci Lett 233:101-104.
40. Landrigan PJ, Sonawane B, Butler RN, Trasande L, Callan R, Droller D. 2005. Early environmental origins of neurodegenerative disease in later life. Environ Health Perspect 113:1230-1233.
41. Lanphear BP, Hornung R, Khoury J, Yolton K, Baghurst P, Bellinger DC, et al. 2005. Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ Health Perspect 113:894-899.
42. Ma T, Chen HH, Ho IK. 1999. Effects of chronic lead exposure on neurobehavioral function and dopaminergic neurotransmitter receptors in rats. Toxicol Lett 105:111-121.
43. Madras BK, Miller GM, Fischman AJ. 2005. The dopamine transporter and attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1397-1409.
44. Manton WI, Angle CR, Stanek KL, Kuntzelman D, Reese YR, Kuehnemann TJ. 2003. Release of lead from bone in pregnancy and lactation. Environ Res 92:139-151.
45. McNamara RK, Levant B, Taylor B, Ahlbrand R, Liu Y, Sullivan JR, et al. 2006. C57BL/6J mice exhibit reduced dopamine D3 receptor-mediated locomotor-inhibitory function relative to DBA/2J mice. Neuroscience 143:141-153.
46. Middaugh LD, Randall GL, Favara JP. 1988. Prenatal ethanol exposure in C57 mice: effects on pregnancy and offspring development. Neurotoxicol Teratol 10:175-180.
47. Min YI, Correa-Villasenor A, Stewart PA. 1996. Parental occupational lead exposure and low birth weight. Am J Ind Med 30:569-578.
48. Minnema DJ, Greenland RD, Michaelson IA. 1986. Effect of in vitro inorganic lead on dopamine release from superfused rat striatal synaptosomes. Toxicol Appl Pharmacol 84:400-411.
49. Moreira EG, Vassilieff I, Vassilieff VS. 2001. Developmental lead exposure: behavioral alterations in the short and long term. Neurotoxicol Teratol 23:489-495.
50. Newland MC, Rasmussen EB. 2000. Aging unmasks adverse effects of gestational exposure to methylmercury in rats. Neurotoxicol Teratol 22:819-828.
51. NIH. 2002. Public Health Service Policy on Humane Care and Use of Laboratory Animals. Bethesda, MD:National Institutes of Health.
52. Opler MG, Brown AS, Graziano J, Desai M, Zheng W, Schaefer C, et al. 2004. Prenatal lead exposure, δ-aminolevulinic acid, and schizophrenia. Environ Health Perspect 112:548-552.
53. Petroske E, Meredith GE, Callen S, Totterdell S, Lau YS. 2001. Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 106:589-601.
54. Pizzi WJ, Barnhart JE. 1976. Effects of monosodium glutamate on somatic development, obesity and activity in the mouse. Pharmacol Biochem Behav 5:55-557.
55. Raedler A, Sievers J. 1975. The development of the visual system of the albino rat. Adv Anat Embryol Cell Biol 50:3-88.
56. Ramsay PB, Krigman MR, Morell P. 1980. Developmental studies of the uptake of choline, GABA and dopamine by crude synaptosomal preparations after in vivo or in-vitro lead treatment. Brain Res 187:383-402.
57. Rezende VB, Barbosa F Jr, Montenegro MF, Sandrim VC, Gerlach RF, Tanus-Santos JE. 2008. Haplotypes of vitamin D receptor modulate the circulating levels of lead in exposed subjects. Arch Toxicol 82:29-36.
58. Rice D, Barone S Jr. 2000. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(suppl 3):511-533.
59. Ris MD, Dietrich KN, Succop PA, Berger OG, Bornschein RL. 2004. Early exposure to lead and neuropsychological outcome in adolescence. J Int Neuropsychol Soc 10:261-270.
60. Rothenberg SJ, Poblano A, Schnaas L. 2000. Brainstem auditory evoked response at five years and prenatal and postnatal blood lead. Neurotoxicol Teratol 22:503-510.
61. Rothenberg SJ, Schnaas L, Salgado-Valladares M, Casanueva E, Geller AM, Hudnell HK, et al. 2002. Increased ERG a- and b-wave amplitudes in 7- to 10-year-old children resulting from prenatal lead exposure. Invest Ophthalmol Vis Sci 43:2036-2044.
62. Schanne FA, Gupta RK, Rosen JF. 1992. Lead inhibits 1,25-dihydroxyvitamin D-3 regulation of calcium metabolism in osteoblastic osteosarcoma cells (ROS 17/2.8). Biochim Biophys Acta 1180:187-194.
63. Schnaas L, Rothenberg SJ, Flores MF, Martinez S, Hernandez C, Osorio E, et al. 2006. Reduced intellectual development in children with prenatal lead exposure. Environ Health Perspect 114:791-797.
64. Schwartz BS, Lee BK, Lee GS, Stewart WF, Simon D, Kelsey K, et al. 2000. Associations of blood lead dimercaptosuccinic acid-chelatable lead, and tibia lead with polymorphisms in the vitamin D receptor and δ-aminolevulinic acid dehydratase genes. Environ Health Perspect 108:949-954.
65. Vahter M, Akesson A, Liden C, Ceccatelli S, Berglund M. 2007. Gender differences in the disposition and toxicity of metals. Environ Res 104:85-95.
66. Verlangieri AJ. 1979. Prenatal and postnatal chronic lead intoxication and running wheel activity in the rat. Pharmacol Biochem Behav 11:95-98.
67. Virgolini MB, Volosin M, Fulginiti AS, Cancela LM. 2004. Amphetamine and stress responses in developmentally lead-exposed rats. Neurotoxicol Teratol 26:291-303.
68. Wasserman GA, Liu X, Popovac D, Factor-Litvak P, Kline J, Waternaux C, et al. 2000. The Yugoslavia Prospective Lead Study: contributions of prenatal and postnatal lead exposure to early intelligence. Neurotoxicol Teratol 22:811-818.
69. Weiss B. 1990. Risk assessment: the insidious nature of neurotoxicity and the aging brain. Neurotoxicology 11:305-313.
70. Weiss B, Clarkson TW, Simon W. 2002. Silent latency periods in methylmercury poisoning and in neurodegenerative disease. Environ Health Perspect 110(suppl 5):851-854.
71. Weiss B, Stern S, Cox C, Balys M. 2005. Perinatal and lifetime exposure to methylmercury in the mouse: behavioral effects. Neurotoxicology 26:675-690.
72. Winneke G, Brockhaus A, Ewers U, Kramer U, Neuf M. 1990. Results from the European multicenter study on lead neurotoxicity in children: implications for risk assessment. Neurotoxicol Teratol 12:553-559.
73. Ye WZ, Reis AF, Dubois-Laforgue D, Bellanne-Chantelot C, Timsit J, Velho G. 2001. Vitamin D receptor gene polymorphisms are associated with obesity in type 2 diabetic subjects with early age of onset. Eur J Endocrinol 145:181-186.
74. Yuan W, Holland SK, Cecil KM, Dietrich KN, Wessel SD, Altaye M, et al. 2006. The impact of early childhood lead exposure on brain organization: a functional magnetic resonance imaging study of language function. Pediatrics 118:971-977.
75. Zhu HJ, Wang JS, DeVane CL, Williard RL, Donovan JL, Middaugh LD, et al. 2006. The role of the polymorphic efflux transporter P-glycoprotein on the brain accumulation of d-methylphenidate and d-amphetamine. Drug Metab Dispos 34:1116-1121.