Pb2+: An endocrine disruptor in Drosophila?

Physiology and Behavior

Volumn 99, Issue 2, 2010, Pages 254-259

  Hirsch, Helmut V B ^a   Possidente, Debra ^b   Possidente, Bernard ^b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b SKIDMORE COLLEGE   (United States)

Author keywords

Drosophila; Endocrine disruptor; Model systems; Neural development; Pb2+; Synaptic function

Indexed keywords

CELL NUCLEUS RECEPTOR; ECDYSONE; ENDOCRINE DISRUPTOR; ESTRADIOL; LEAD; RETINOIC ACID; DROSOPHILA PROTEIN; LEAD ACETATE; ORGANOMETALLIC COMPOUND;

ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; CIRCADIAN RHYTHM; DROSOPHILA; ENVIRONMENTAL EXPOSURE; FATTY ACID OXIDATION; FERTILITY; GENETIC MODEL; GENETIC TRANSCRIPTION; HUMAN; LEAD POISONING; LIPID PEROXIDATION; LOCOMOTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; DROSOPHILA MELANOGASTER; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; REVIEW; SEXUAL DEVELOPMENT;

ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCRINE DISRUPTORS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOTOR ACTIVITY; ORGANOMETALLIC COMPOUNDS; SEX CHARACTERISTICS;

EID: 72649086553     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2009.09.014     Document Type: Article

References (131)

1. De Vleeschouwer F., Gerard L., Goormaghtigh C., Mattielli N., Le Roux G., and Fagel N. Atmospheric lead and heavy metal pollution records from a Belgian peat bog spanning the last two millenia: human impact on a regional to global scale. Sci Total Environ 377 2-3 (2007) 282-295
2. Caplun E., Petit D., and Picciotto E. Lead in petrol. Endeavour 8 3 (1984) 135-144
3. Lanphear B.P., Dietrich K.N., and Berger O. Prevention of lead toxicity in US children. Ambul Pediatr 3 1 (2003) 27-36
4. Iqbal S., Muntner P., Batuman V., and Rabito F.A. Estimated burden of blood lead levels 5 microg/dl in 1999-2002 and declines from 1988 to 1994. Environ Res 107 3 (2008) 305-311
5. Bellinger D.C. Very low lead exposures and children's neurodevelopment. Curr Opin Pediatr 20 2 (2008) 172-177
6. White L.D., Cory-Slechta D.A., Gilbert M.E., Tiffany-Castiglioni E., Zawia N.H., Virgolini M., et al. New and evolving concepts in the neurotoxicology of lead. Toxicol Appl Pharmacol 225 1 (2007) 1-27
7. Woolf A.D., Goldman R., and Bellinger D.C. Update on the clinical management of childhood lead poisoning. Pediatr Clin North Am 54 2 (2007) 271-294 viii
8. Needleman H. Lead poisoning. Annu Rev Med 55 (2004) 209-222
9. Nevin R., Jacobs D.E., Berg M., and Cohen J. Monetary benefits of preventing childhood lead poisoning with lead-safe window replacement. Environ Res 106 3 (2008) 410-419
10. Aschengrau A., Beiser A., Bellinger D., Copenhafer D., and Weitzman M. The impact of soil lead abatement on urban children's blood lead levels: phase II results from the Boston Lead-In-Soil Demonstration Project. Environ Res 67 2 (1994) 125-148
11. Clark H.F., Brabander D.J., and Erdil R.M. Sources, sinks, and exposure pathways of lead in urban garden soil. J Environ Qual 35 6 (2006) 2066-2074
12. Clark C.S., Rampal K.G., Thuppil V., Chen C.K., Clark R., and Roda S. The lead content of currently available new residential paint in several Asian countries. Environ Res 102 1 (2006) 9-12
13. Lin G.Z., Peng R.F., Chen Q., Wu Z.G., and Du L. Lead in housing paints: an exposure source still not taken seriously for children lead poisoning in China. Environ Res 109 1 (2009) 1-5
14. Huo X., Peng L., Xu X., Zheng L., Qiu B., Qi Z., et al. Elevated blood lead levels of children in Guiyu, an electronic waste recycling town in China. Environ Health Perspect 115 7 (2007) 1113-1117
15. Hu H., Shih R., Rothenberg S., and Schwartz B.S. The epidemiology of lead toxicity in adults: measuring dose and consideration of other methodologic issues. Environ Health Perspect 115 3 (2007) 455-462
16. Nie H., Sanchez B.N., Wilker E., Weisskopf M.G., Schwartz J., Sparrow D., et al. Bone lead and endogenous exposure in an environmentally exposed elderly population: the normative aging study. J Occup Environ Med 51 7 (2009) 848-857
17. Shih R.A., Hu H., Weisskopf M.G., and Schwartz B.S. Cumulative lead dose and cognitive function in adults: a review of studies that measured both blood lead and bone lead. Environ Health Perspect 115 3 (2007) 483-492
18. Theppeang K., Glass T.A., Bandeen-Roche K., Todd A.C., Rohde C.A., and Schwartz B.S. Gender and race/ethnicity differences in lead dose biomarkers. Am J Public Health 98 7 (2008) 1248-1255
19. Weuve J., Korrick S.A., Weisskopf M.A., Ryan L.M., Schwartz J., Nie H., et al. Cumulative exposure to lead in relation to cognitive function in older women. Environ Health Perspect 117 4 (2009) 574-580
20. Kosnett M.J., Wedeen R.P., Rothenberg S.J., Hipkins K.L., Materna B.L., Schwartz B.S., et al. Recommendations for medical management of adult lead exposure. Environ Health Perspect 115 3 (2007) 463-471
21. Perlstein T., Weuve J., Schwartz J., Sparrow D., Wright R., Litonjua A., et al. Cumulative community-level lead exposure and pulse pressure: the normative aging study. Environ Health Perspect 115 12 (2007) 1696-1700
22. Gulson B.L., Mizon K.J., Korsch M.J., Palmer J.M., and Donnelly J.B. Mobilization of lead from human bone tissue during pregnancy and lactation-a summary of long-term research. Sci Total Environ 303 1-2 (2003) 79-104
23. Bellinger D.C., Stiles K.M., and Needleman H.L. Low-level lead exposure, intelligence and academic achievement: a long-term follow-up study. Pediatrics 90 6 (1992) 855-861
24. Canfield R.L., Henderson Jr. C.R., Cory-Slechta D.A., Cox C., Jusko T.A., and Lanphear B.P. Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N Engl J Med 348 16 (2003) 1517-1526
25. Jusko T.A., Henderson C.R., Lanphear B.P., Cory-Slechta D.A., Parsons P.J., and Canfield R.L. Blood lead concentrations < 10 microg/dL and child intelligence at 6 years of age. Environ Health Perspect 116 2 (2008) 243-248
26. Lanphear B.P., Hornung R., Khoury J., Yolton K., Baghurst P., Bellinger D.C., et al. Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ Health Perspect 113 7 (2005) 894-899
27. Needleman H.L., Schell A., Bellinger D., Leviton A., and Allred E.N. The long-term effects of exposure to low doses of lead in childhood. An 11-year follow-up report. N Engl J Med 322 2 (1990) 83-88
28. Nevin R. Trends in preschool lead exposure, mental retardation, and scholastic achievement: association or causation?. Environ Res 109 3 (2009) 301-310
29. Surkan P.J., Zhang A., Trachtenberg F., Daniel D.B., McKinlay S., and Bellinger D.C. Neuropsychological function in children with blood lead levels < 10 microg/dL. Neurotoxicology 28 6 (2007) 1170-1177
30. Dietrich K.N., Ris M.D., Succop P.A., Berger O.G., and Bornschein R.L. Early exposure to lead and juvenile delinquency. Neurotoxicol Teratol 23 6 (2001) 511-518
31. Nevin R. Understanding international crime trends: the legacy of preschool lead exposure. Environ Res 104 3 (2007) 315-336
32. Wright J.P., Dietrich K.N., Ris M.D., Hornung R.W., Wessel S.D., Lanphear B.P., et al. Association of prenatal and childhood blood lead concentrations with criminal arrests in early adulthood. PLoS Med 5 5 (2008) e101
33. Braun J.M., Kahn R.S., Froehlich T., Auinger P., and Lanphear B.P. Exposures to environmental toxicants and attention deficit hyperactivity disorder in U.S. children. Environ Health Perspect 114 12 (2006) 1904-1909
34. Padich R.A., Dietrich K.N., and Pearson D.T. Attention, activity level, and lead exposure at 18 months. Environ Res 38 1 (1985) 137-143
35. Altmann L., Sveinsson K., Kramer U., Weishoff-Houben M., Turfeld M., Winneke G., et al. Visual functions in 6-year-old children in relation to lead and mercury levels. Neurotoxicol Teratol 20 1 (1998) 9-17
36. Buchanan L.H., Counter S.A., Ortega F., and Laurell G. Distortion product oto-acoustic emissions in Andean children and adults with chronic lead intoxication. Acta Otolaryngol 119 6 (1999) 652-658
37. Counter S.A., Vahter M., Laurell G., Buchanan L.H., Ortega F., and Skerfving S. High lead exposure and auditory sensory-neural function in Andean children. Environ Health Perspect 105 5 (1997) 522-526
38. Jones L.G., Prins J., Park S., Walton J.P., Luebke A.E., and Lurie D.I. Lead exposure during development results in increased neurofilament phosphorylation, neuritic beading, and temporal processing deficits within the murine auditory brainstem. J Comp Neurol 506 6 (2008) 1003-1017
39. Lengyel Z., Lukacs A., Szabo A., and Institoris L. Neurotoxic and general effects of combined subchronic exposure of rats to insecticides and heavy metals. Acta Biol Hung 57 4 (2006) 423-432
40. Liang G.H., Jarlebark L., Ulfendahl M., Bian J.T., and Moore E.J. Lead (Pb2+) modulation of potassium currents of guinea pig outer hair cells. Neurotoxicol Teratol 26 2 (2004) 253-260
41. Cory-Slechta D.A., and Pokora M.J. Lead-induced changes in muscarinic cholinergic sensitivity. Neurotoxicology 16 2 (1995) 337-347
42. Tang M., Luo L., Zhu D., Wang M., Luo Y., Wang H., et al. Muscarinic cholinergic modulation of synaptic transmission and plasticity in rat hippocampus following chronic lead exposure. Naunyn Schmiedebergs Arch Pharmacol 379 1 (2009) 37-45
43. Wang L., Luo L., Luo Y.Y., Gu Y., and Ruan D.Y. Effects of Pb2+ on muscarinic modulation of glutamatergic synaptic transmission in rat hippocampal CA1 area. Neurotoxicology 28 3 (2007) 499-507
44. Gilbert M.E., and 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. Neurotoxicol Teratol 29 3 (2007) 385-393
45. Guilarte T.R. Pb2+ inhibits NMDA receptor function at high and low affinity sites: developmental and regional brain expression. Neurotoxicology 18 1 (1997) 43-51
46. Yan D., Wang L., Ma F.L., Deng H., Liu J., Li C., et al. Developmental exposure to lead causes inherent changes on voltage-gated sodium channels in rat hippocampal CA1 neurons. Neuroscience 153 2 (2008) 436-445
47. Audesirk G., and Audesirk T. Effects of in vitro lead exposure on voltage-sensitive calcium channels differ among cell types in central neurons of Lymnaea stagnalis. Neurotoxicology 10 4 (1989) 659-669
48. Busselberg D. Calcium channels as target sites of heavy metals. Toxicol Lett 82-83 (1995) 255-261
49. Sandhir R., and Gill K.D. Alterations in calcium homeostasis on lead exposure in rat synaptosomes. Mol Cell Biochem 131 1 (1994) 25-33
50. Suszkiw J.B. Presynaptic disruption of transmitter release by lead. Neurotoxicology 25 4 (2004) 599-604
51. Vazquez A., and Pena de Ortiz S. Lead (Pb(+ 2)) impairs long-term memory and blocks learning-induced increases in hippocampal protein kinase C activity. Toxicol Appl Pharmacol 200 1 (2004) 27-39
52. Zhang H.S., Song L.H., Wang L., and Qin Y.H. Lead can inhibit NMDA-, K(+)-, QA/KA-induced increases in intracellular free Ca2+ in cultured rat hippocampal neurons. Biomed Environ Sci 15 4 (2002) 330-340
53. He T, Singh V, Hirsch HVB, Ruden DM, Lnenicka GA. Chronic lead exposure alters calcium regulation at presynaptic terminals in Drosophila larvae. Neurotoxicology in press. Available online 2 September 2009.
54. Denham M., Schell L.M., Deane G., Gallo M.V., Ravenscroft J., and DeCaprio A.P. Relationship of lead, mercury, mirex, dichlorodiphenyldichloroethylene, hexachlorobenzene, and polychlorinated biphenyls to timing of menarche among Akwesasne Mohawk girls. Pediatrics 115 2 (2005) e127-e134
55. Selevan S.G., Rice D.C., Hogan K.A., Euling S.Y., Pfahles-Hutchens A., and Bethel J. Blood lead concentration and delayed puberty in girls. N Engl J Med 348 16 (2003) 1527-1536
56. Staessen J.A., Nawrot T., Hond E.D., Thijs L., Fagard R., Hoppenbrouwers K., et al. Renal function, cytogenetic measurements, and sexual development in adolescents in relation to environmental pollutants: a feasibility study of biomarkers. Lancet 357 9269 (2001) 1660-1669
57. Wu T., Buck G.M., and Mendola P. Blood lead levels and sexual maturation in U.S. girls: the Third National Health and Nutrition Examination Survey, 1988-1994. Environ Health Perspect 111 5 (2003) 737-741
58. Wolff M.S., Britton J.A., Boguski L., Hochman S., Maloney N., Serra N., et al. Environmental exposures and puberty in inner-city girls. Environ Res 107 3 (2008) 393-400
59. Winder C. Lead, reproduction and development. Neurotoxicology 14 2-3 (1993) 303-317
60. Bonde J.P., Joffe M., Apostoli P., Dale A., Kiss P., Spano M., et al. Sperm count and chromatin structure in men exposed to inorganic lead: lowest adverse effect levels. Occup Environ Med 59 4 (2002) 234-242
61. Gennart J.P., Buchet J.P., Roels H., Ghyselen P., Ceulemans E., and Lauwerys R. Fertility of male workers exposed to cadmium, lead, or manganese. Am J Epidemiol 135 11 (1992) 1208-1219
62. Hsu P.C., Chang H.Y., Guo Y.L., Liu Y.C., and Shih T.S. Effect of smoking on blood lead levels in workers and role of reactive oxygen species in lead-induced sperm chromatin DNA damage. Fertil Steril 91 4 (2009) 1096-1103
63. Kasperczyk A., Kasperczyk S., Horak S., Ostalowska A., Grucka-Mamczar E., Romuk E., et al. Assessment of semen function and lipid peroxidation among lead exposed men. Toxicol Appl Pharmacol 228 3 (2008) 378-384
64. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87 3 (2007) 905-931
65. McCarthy M.M. Estradiol and the developing brain. Physiol Rev 88 1 (2008) 91-124
66. Mermelstein P.G., and Micevych P.E. Nervous system physiology regulated by membrane estrogen receptors. Rev Neurosci 19 6 (2008) 413-424
67. Micevych P.E., and Mermelstein P.G. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol 38 1 (2008) 66-77
68. Huttenlocher P.R., and Dabholkar A.S. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387 2 (1997) 167-178
69. Cooper G.P., and Manalis R.S. Influence of heavy metals on synaptic transmission: a review. Neurotoxicology 4 4 (1983) 69-83
70. Morley E.J., Hirsch H.V., Hollocher K., and Lnenicka G.A. Effects of chronic lead exposure on the neuromuscular junction in Drosophila larvae. Neurotoxicology 24 1 (2003) 35-41
71. Toscano C.D., and Guilarte T.R. Lead neurotoxicity: from exposure to molecular effects. Brain Res Brain Res Rev 49 3 (2005) 529-554
72. Schantz S.L., and Widholm J.J. Cognitive effects of endocrine-disrupting chemicals in animals. Environ Health Perspect 109 12 (2001) 1197-1206
73. Crews D., Willingham E., and Skipper J.K. Endocrine disruptors: present issues, future directions. Q Rev Biol 75 3 (2000) 243-260
74. Diamanti-Kandarakis E., Bourguignon J.P., Giudice L.C., Hauser R., Prins G.S., Soto A.M., et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30 4 (2009) 293-342
75. Hotchkiss A.K., Rider C.V., Blystone C.R., Wilson V.S., Hartig P.C., Ankley G.T., et al. Fifteen years after "Wingspread"-environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci 105 2 (2008) 235-259
76. McLachlan J.A. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev 22 3 (2001) 319-341
77. Witorsch R.J. Endocrine disruptors: can biological effects and environmental risks be predicted?. Regul Toxicol Pharmacol 36 1 (2002) 118-130
78. Iavicoli I., Fontana L., and Bergamaschi A. The effects of metals as endocrine disruptors. J Toxicol Environ Health B Crit Rev 12 3 (2009) 206-223
79. Hirsch H.V., Mercer J., Sambaziotis H., Huber M., Stark D.T., Torno-Morley T., et al. Behavioral effects of chronic exposure to low levels of lead in Drosophila melanogaster. Neurotoxicology 24 3 (2003) 435-442
80. Hirsch H.V., Possidente D., Averill S., Despain T.P., Buytkins J., Thomas V., et al. Variations at a quantitative trait locus (QTL) affect development of behavior in lead-exposed Drosophila melanogaster. Neurotoxicology 30 2 (2009) 305-311
81. Ruden D.M., Chen L., Possidente D., Possidente B., Rasouli P., Wang L., et al. Genetical toxicogenomics in Drosophila identifies master modulatory loci that are regulated by developmental exposure to lead. Neurotoxicology 30 (2009) 898-914
82. Yepiskoposyan H., Egli D., Fergestad T., Selvaraj A., Treiber C., Multhaup G., et al. Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res 34 17 (2006) 4866-4877
83. Akins J.M., Schroeder J.A., Brower D.L., and Aposhian H.V. Evaluation of Drosophila melanogaster as an alternative animal for studying the neurotoxicity of heavy metals. Biometals 5 2 (1992) 111-120
84. Balamurugan K., Hua H., Georgiev O., and Schaffner W. Mercury and cadmium trigger expression of the copper importer Ctr1B, which enables Drosophila to thrive on heavy metal-loaded food. Biol Chem 390 2 (2009) 109-113
85. Lauverjat S., Ballan-Dufrancais C., and Wegnez M. Detoxification of cadmium. Ultrastructural study and electron-probe microanalysis of the midgut in a cadmium-resistant strain of Drosophila melanogaster. Biol Met 2 2 (1989) 97-107
86. Rand M.D.., Dao J.C., and Clason T.A. Methylmercury disruption of embryonic neural development in Drosophila. Neurotoxicology 30 (2009) 794-802
87. deFur P.L. Use and role of invertebrate models in endocrine disruptor research and testing. Ilar J 45 4 (2004) 484-493
88. Riddiford L.M. Hormones and Drosophila development. In: Bate M., and Arias A. (Eds). The development of Drosophila melanogaster (1993), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York USA 899-939
89. Bardet P.L., Laudet V., and Vanacker J.M. Studying non-mammalian models? Not a fool's ERRand!. Trends Endocrinol Metab 17 4 (2006) 166-171
90. King-Jones K., and Thummel C.S. Nuclear receptors-a perspective from Drosophila. Nat Rev Genet 6 4 (2005) 311-323
91. Flatt T., and Kawecki T.J. Pleiotropic effects of methoprene-tolerant (Met), a gene involved in juvenile hormone metabolism, on life history traits in Drosophila melanogaster. Genetica 122 2 (2004) 141-160
92. Liu Z., Li X., Prasifka J.R., Jurenka R., and Bonning B.C. Overexpression of Drosophila juvenile hormone esterase binding protein results in anti-JH effects and reduced pheromone abundance. Gen Comp Endocrinol 156 1 (2008) 164-172
93. Belgacem Y.H., and Martin J.R. Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila. Proc Natl Acad Sci U S A 99 23 (2002) 15154-15158
94. Meunier N., Belgacem Y.H., and Martin J.R. Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J Exp Biol 210 Pt 8 (2007) 1424-1434
95. Wilson T.G., DeMoor S., and Lei J. Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the Methoprene-tolerant (27) mutant phenotype. Insect Biochem Mol Biol 33 12 (2003) 1167-1175
96. Christopherson K.S., Mark M.R., Bajaj V., and Godowski P.J. Ecdysteroid-dependent regulation of genes in mammalian cells by a Drosophila ecdysone receptor and chimeric transactivators. Proc Natl Acad Sci U S A 89 14 (1992) 6314-6318
97. Goodwin B., Jones S.A., Price R.R., Watson M.A., McKee D.D., Moore L.B., et al. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol Cell 6 3 (2000) 517-526
98. Lu T.T., Makishima M., Repa J.J., Schoonjans K., Kerr T.A., Auwerx J., et al. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol Cell 6 3 (2000) 507-515
99. Marvin K.A., Reinking J.L., Lee A.J., Pardee K., Krause H.M., and Burstyn J.N. Nuclear receptors homo sapiens Rev-erbbeta and Drosophila melanogaster E75 are thiolate-ligated heme proteins which undergo redox-mediated ligand switching and bind CO and NO. Biochemistry 48 29 (2009) 7056-7071
100. Ostberg T., Jacobsson M., Attersand A., Mata de Urquiza A., and Jendeberg L. A triple mutant of the Drosophila ERR confers ligand-induced suppression of activity. Biochemistry 42 21 (2003) 6427-6435
101. Palanker L., Necakov A.S., Sampson H.M., Ni R., Hu C., Thummel C.S., et al. Dynamic regulation of Drosophila nuclear receptor activity in vivo. Development 133 18 (2006) 3549-3562
102. Pardee K., Reinking J., and Krause H. Nuclear hormone receptors, metabolism, and aging: what goes around comes around. Transcription factors link lipid metabolism and aging-related processes. Sci Aging Knowledge Environ 2004 47 (2004) re8
103. Thackray V.G., Young R.H., Hooper J.E., and Nordeen S.K. Estrogen agonist and antagonist action on the human estrogen receptor in Drosophila. Endocrinology 141 10 (2000) 3912-3915
104. Bajraktari I.S.G., Marinkovic D., and Hajrizi A. The influence of heavy metals on the duration of Drosophila melanogaster preadult development. Acta Biol Med Exp 12 (1987) 57-66
105. Cohn J., Widzowski D.V., and Cory-Slechta D.A. Lead retards development of Drosophila melanogaster. Comp Biochem Physiol C 102 1 (1992) 45-49
106. Massie H.R., Aiello V.R., and Whitney S.J.P. Lead accumulation during aging of Drosophila and effect of dietary lead on life span. Age 15 (1992) 47-49
107. Uysal H., and Bahceci Z. Effect of lead acetate and mercury chloride on offspring production in Drosophila melanogaster. Drosoph Inf Serv 77 (July 1996) 102-103
108. Calabrese E.J., and Baldwin L.A. Hormesis: the dose-response revolution. Annu Rev Pharmacol Toxicol 43 (2003) 175-197
109. Nuzhdin S.V., Pasyukova E.G., Dilda C.L., Zeng Z.B., and Mackay T.F. Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc Natl Acad Sci U S A 94 18 (1997) 9734-9739
110. Gurer H., and Ercal N. Can antioxidants be beneficial in the treatment of lead poisoning?. Free Radic Biol Med 29 10 (2000) 927-945
111. Wills E.D. Mechanisms of lipid peroxide formation in tissues. Role of metals and haematin proteins in the catalysis of the oxidation unsaturated fatty acids. Biochim Biophys Acta 98 (1965) 238-251
112. Yiin S.J., and Lin T.H. Lead-catalyzed peroxidation of essential unsaturated fatty acid. Biol Trace Elem Res 50 2 (1995) 167-172
113. Gerber G., Maes J., and Deroo J. Effect of dietary lead on placental blood flow and on fetal uptake of alpha-amino isobutyrate. Arch Toxicol 41 2 (1978) 125-131
114. Sandhir R., Julka D., and Gill K.D. Lipoperoxidative damage on lead exposure in rat brain and its implications on membrane bound enzymes. Pharmacol Toxicol 74 2 (1994) 66-71
115. Shafiq Ur R. Lead-induced regional lipid peroxidation in brain. Toxicol Lett 21 3 (1984) 333-337
116. Shafiq ur R., and Chandra O. Regional interrelationships of zinc, copper, and lead in the brain following lead intoxication. Bull Environ Contam Toxicol 32 2 (1984) 157-165
117. Drysdale R. FlyBase: a database for the Drosophila research community. Methods Mol Biol 420 (2008) 45-59
118. Li H., and Cooper R.L. Effects of the ecdysoneless mutant on synaptic efficacy and structure at the neuromuscular junction in Drosophila larvae during normal and prolonged development. Neuroscience 106 1 (2001) 193-200
119. Lai C.Q., Parnell L.D., Lyman R.F., Ordovas J.M., and Mackay T.F. Candidate genes affecting Drosophila life span identified by integrating microarray gene expression analysis and QTL mapping. Mech Ageing Dev 128 3 (2007) 237-249
120. Lai C.Q., Leips J., Zou W., Roberts J.F., Wollenberg K.R., Parnell L.D., et al. Speed-mapping quantitative trait loci using microarrays. Nat Methods 4 10 (2007) 839-841
121. Mackay T.F., and Anholt R.R. Of flies and man: Drosophila as a model for human complex traits. Annu Rev Genomics Hum Genet 7 (2006) 339-367
122. Takahashi J.S., Shimomura K., and Kumar V. Searching for genes underlying behavior: lessons from circadian rhythms. Science 322 5903 (2008) 909-912
123. Hooven L.A., Sherman K.A., Butcher S., and Giebultowicz J.M. Does the clock make the poison? Circadian variation in response to pesticides. PLoS One 4 7 (2009) e6469
124. Ayroles J.F., Carbone M.A., Stone E.A., Jordan K.W., Lyman R.F., Magwire M.M., et al. Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41 3 (2009) 299-307
125. Ruden D.M., and Lu X. Evolutionary conservation of metabolism explains how Drosophila nutrigenomics can help us understand human nutrigenomics. Genes Nutr 1 2 (2006) 75-83
126. Ruden D.M. Personalized medicine and quantitative trait transcripts. Nat Genet 39 2 (2007) 144-145
127. Dinan L., Bourne P., Whiting P., Dhadialla T.S., and Hutchinson T.H. Screening of environmental contaminants for ecdysteroid agonist and antagonist activity using the Drosophila melanogaster B(II) cell in vitro assay. Environ Toxicol Chem 20 9 (2001) 2038-2046
128. Magnusson J., and Ramel C. Genetic variation in the susceptibility to mercury and other metal compounds in Drosophila melanogaster. Teratog Carcinog Mutagen 6 4 (1986) 289-305
129. Nassar R. Genetics of resistance to tetraethyllead. Aust J Biol Sci 32 1 (1979) 127-132
130. Flatt T., and Kawecki T.J. Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophila melanogaster. Evolution 61 8 (2007) 1980-1991
131. Morgan T.J., and Mackay T.F. Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96 3 (2006) 232-242