Gestational lead exposure selectively decreases retinal dopamine amacrine cells and dopamine content in adult mice

Toxicology and Applied Pharmacology

Volumn 256, Issue 3, 2011, Pages 258-267

  Fox, Donald A ^a,b,c   Hamilton, W Ryan ^b   Johnson, Jerry E ^d   Xiao, Weimin ^a   Chaney, Shawntay ^b   Mukherjee, Shradha ^b   Miller, Diane B ^e   O'Callaghan, James P ^e  

^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)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

Amacrine cells; Cell loss; Dopamine; Gestational exposure; Lead; Retina

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; CHOLINERGIC RECEPTOR; DOPAMINE; GLYCINE RECEPTOR; LEAD; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CIRCADIAN RHYTHM; DARK ADAPTATION; DOPAMINE RELEASE; FEMALE; GABAERGIC SYSTEM; GENE EXPRESSION; GESTATION PERIOD; GESTATIONAL LEAD EXPOSURE; IMMUNOCOMPETENT CELL; LIGHT ADAPTATION; MOUSE; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; PROTEIN EXPRESSION; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; STEREOLOGY;

AMACRINE CELLS; ANIMALS; BLOTTING, WESTERN; CELL COUNT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; LEAD POISONING, NERVOUS SYSTEM; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REAL-TIME POLYMERASE CHAIN REACTION;

MUS; RATTUS;

EID: 80855148201     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.05.021     Document Type: Article

References (69)

1. Altmann L., Sveinsson K., Krämer U., Weishoff-Hoube'n M., Turfeld M., Winneke G., Wiegand H. Visual functions in 6-year-old children in relation to lead and mercury levels. Neurotoxicol. Teratol. 1998, 20:9-17.
2. Boireau A., Dubedat P., Laduron P.M., Doble A., Blanchard J.C. Preferential decrease in dopamine utilization in prefrontal cortex by zopiclone, diazepam and zolpidem in unstressed rats. J. Pharm. Pharmacol. 1990, 42:562-565.
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
4. Canfield R.L., Henderson C.R., Cory-Slechta D.A., Cox C., Jusko T.A., Lanphear B.P. Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N. Engl. J. Med. 2003, 348:1517-1526.
5. Cellerino A., Kohler K. Brain-derived neurotrophic factor/neurotrophin-4 receptor TrkB is localized on ganglion cells and dopaminergic amacrine cells in the vertebrate retina. J. Comp. Neurol. 1997, 386:149-160.
6. Cellerino A., Pinzón-Duarte G., Carroll P., Kohler K. Brain-derived neurotrophic factor modulates the development of the dopaminergic network in the rodent retina. J. Neurosci. 1998, 18:3351-3362.
7. Chadderton T., Wilson C., Bewick M., Glück S. Evaluation of three rapid RNA extraction reagents: relevance for use in RT-PCR's and measurement of low level gene expression in clinical samples. Cell. Mol. Biol. 1997, 43:1227-1234.
8. Contini M., Raviola E. GABAergic synapses made by a retinal dopaminergic neuron. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1358-1363.
9. Dacey D.M. The dopaminergic amacrine cell. J. Comp. Neurol. 1990, 301:461-489.
10. Fernandez de Arriba A., Balsa D., Tipton K.F., Unzeta M. Monoamine oxidase and semicarbazide-sensitive amine oxidase activities in bovine eye. J. Neural. Transm. Suppl. 1990, 32:327-330.
11. Fox D.A., Campbell M.L., Blocker Y.S. Functional alterations and apoptotic cell death in the retina following developmental or adult lead exposure. Neurotoxicology 1997, 18:645-664.
12. Fox D.A., Boyes W.K. Toxic responses of the ocular and visual system. Casarett & Doull's Toxicology: The Science of Poisons 2007, 565-596. McGraw-Hill, New York. C.D. Klaassen (Ed.).
13. Fox D.A., Kala S.V., Hamilton W.R., Johnson J.E., O'Callaghan J.P. Low-level human equivalent gestational lead exposure produces supernormal scotopic electroretinograms, increased retinal neurogenesis and decreased dopamine utilization in rats. Environ. Health Perspect. 2008, 116:618-625.
14. Frank-Cannon T.C., Tran T., Ruhn K.A., Martinez T.N., Hong J., et al. Parkin deficiency increases vulnerability to inflammation-related nigral degeneration. J. Neurosci. 2008, 28:10825-10834.
15. Ghai K., Zelinka C., Fischer A.J. Serotonin released from amacrine neurons is scavenged and degraded in bipolar neurons in the retina. J. Neurochem. 2009, 111:1-14.
16. Giddabasappa A., Hamilton W.R., Chaney S., Xiao W., Johnson J.E., Mukherjee S., Fox D.A. Low-level gestational lead exposure increases retinal progenitor cell proliferation and rod photoreceptor and bipolar cell neurogenesis in mice. Environ. Health Perspect. 2011, 119:71-77.
17. Gustincich S., Feigenspan A., Wu D.K., Koopman L.J., Raviola E. Control of dopamine release in the retina: a transgenic approach to neural networks. Neuron 1997, 18:723-736.
18. Gustincich S., Feigenspan A., Sieghart W., Raviola E. Composition of the GABA(A) receptors of retinal dopaminergic neurons. J. Neurosci. 1999, 19:7812-7822.
19. Haverkamp S., Wässle H. Immunocytochemical analysis of the mouse retina. J. Comp. Neurol. 2000, 424:1-23.
20. Haycock J.W., Waymire J.C. Activating antibodies to tyrosine hydroxylase. J. Biol. Chem. 1982, 257:9416-9423.
21. He L., Perkins G.A., Poblenz A.T., Harris J.B., Hung M., Ellisman M.H., Fox D.A. Bcl-xL overexpression blocks bax-mediated mitochondrial contact site formation and apoptosis in rod photoreceptors of lead-exposed mice. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1022-1027.
22. Ilia M., Jeffery G. Retinal mitosis is regulated by dopa, a melanin precursor that may influence the time at which cells exit the cell cycle: analysis of patterns of cell production in pigmented and albino retinae. J. Comp. Neurol. 1999, 405:394-405.
23. Innis M.A., Gelfand D.H., Sninsky J.J., White T.J. PCR Protocols: a Guide to Methods and Applications 1990, Academic Press, New York.
24. Iuvone P.M., Galli C.L., Garrison-Gund C.K., Neff N.H. Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons. Science 1978, 202:901-902.
25. Jacoby R., Zhang A.J., Wu S.M. Light- and dopamine-regulated receptive field plasticity in primate horizontal cells. J. Comp. Neurol. 2011, [Epub ahead of print]. 10.1002/cne.22604.
26. Jadhav A.L., Ramesh G.T. Pb-induced alterations in tyrosine hydroxylase activity in rat brain. Mol. Cell. Biochem. 1997, 175:137-141.
27. Jeon C.J., Strettoi E., Masland R.H. The major cell populations of the mouse retina. J. Neurosci. 1998, 18:8936-8946.
28. 2+ dynamics in vertebrate rod and cone ribbon synapses. Mol. Vis. 2007, 13:887-919.
29. Jones D.C., Miller G.W. The effects of environmental neurotoxicants on the dopaminergic system: a possible role in drug addiction. Biochem. Pharmacol. 2008, 76:569-581.
30. Kohler K., Lilienthal H., Guenther E., Winneke G., Zrenner E. Persistent decrease of the dopamine-synthesizing enzyme tyrosine hydroxylase in the rhesus monkey retina after chronic lead exposure. Neurotoxicology 1997, 18:623-632.
31. Kothmann W.W., Massey S.C., O'Brien J. Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. J. Neurosci. 2009, 29:14903-14911.
32. Leasure J.L., Giddabasappa A., Chaney S., Johnson J.E., Pothakos K., Lau Y.S., Fox D.A. Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ. Health Perspect. 2008, 115:355-361.
33. Lee J.Y., Choi J.S., Ahn C.H., Kim I.S., Ha J.H., Jeon C.J. Calcium-binding protein calretinin immunoreactivity in the dog superior colliculus. Acta Histochem. Cytochem. 2006, 39:125-138.
34. Lilienthal H., Lenaerts C., Winneke G., Hennekes R. Alteration of the visual evoked potential and the electroretinogram in lead-treated monkeys. Neurotoxicol. Teratol. 1988, 10:417-422.
35. Lilienthal H., Kohler K., Turfeld M., Winneke G. Persistent increases in scotopic B-wave amplitudes after lead exposure in monkeys. Exp. Eye Res 1994, 59:203-209.
36. Loeliger M., Briscoe T., Lambert G., Caddy J., Rehn A., Dieni S., Rees S. Invest. Ophthalmol. Vis. Sci. 2004, 45:2361-2367.
37. Ming M., Li X., Fan X., Yang D., Li L., Chen S., Gu Q., Le W. Retinal pigment epithelial cells secrete neurotrophic factors and synthesize dopamine: possible contribution to therapeutic effects of RPE cell transplantation in Parkinson's disease. J. Transl. Med. 2009, 7:53.
38. Minnema D.J., Greenland R.D., Michaelson I.A. Effect of in vitro inorganic lead on dopamine release from superfused rat striatal synaptosomes. Toxicol. Appl. Pharmacol. 1986, 84:400-411.
39. Nagpal A.G., Brodie S.E. Supranormal electroretinogram in a 10-year-old girl with lead toxicity. Doc. Ophthalmol. 2009, 118:163-166.
40. Nakajima J., Stuart M., Kani K., Maeda T. Monoamine oxidase-A-positive retinal ganglion cells projecting to the superior colliculus and dorsolateral geniculate nucleus of the rat brain. Exp. Eye Res. 1998, 66:591-598.
41. Neal A.P., Stansfield K.H., Worley P.F., Thompson R.E., Guilarte T.R. Lead exposure during synaptogenesis alters vesicular proteins and impairs vesicular release: potential role of NMDA receptor-dependent BDNF signaling. Toxicol. Sci. 2010, 116:249-263.
42. Nguyen-Legros J., Krieger M., Simon A. Immunohistochemical localization of L.-dopa and aromatic L.-amino acid-decarboxylase in the rat retina. Invest. Ophthalmol. Vis. Sci. 1994, 35:2906-2915.
43. Nguyen-Legros J., Versaux-Botteri C., Savy C. Dopaminergic and GABAergic retinal cell populations in mammals. Microsc. Res. Tech. 1997, 36:26-42.
44. Ohtani N., Goto T., Waeber C., Bhide P.G. Dopamine modulates cell cycle in the lateral ganglionic eminence. J. Neurosci. 2003, 23:2840-2850.
45. Oliver P., Jolicoeur F.B., Lafond G., Drumheller A.L., Brunette J.R. Dose related effects of 6-OHDA on rabbit retinal dopamine concentrations and ERG b-wave amplitudes. Brain Res. Bull. 1986, 16:751-753.
46. Osman K., Pawlas K., Schütz A., Gazdzik M., Sokal J.A., Vahter M. Lead exposure and hearing effects in children in Katowice, Poland. Eviron. Res. 1999, 80:1-8.
47. Peppe A., Stanzione P., Pierantozzi M., Semprini R., Bassi A., et al. Does pattern electroretinogram spatial tuning alteration in Parkinson's disease depend on motor disturbances or retinal dopaminergic loss?. Electroencephalogr. Clin. Neurophysiol. 1998, 106:374-382.
48. Proll M.A., Kamp C.W., Morgan W.W. Use of liquid chromatography with electrochemistry to measure effects of varying intensities of white light on DOPA accumulation in rat retinas. Life Sci. 1982, 30:11-19.
49. Ramsay P.B., Krigman M.R., Morell P. Developmental studies of the uptake of choline GABA and dopamine by crude synaptosomal preparations after in vivo or in vitro lead treatment. Brain Res. 1980, 187:383-402.
50. Reiner P.B., Vincent S.R. Topographic relations of cholinergic and noradrenergic neurons in the feline pontomesencephalic tegmentum: an immunohistochemical study. Brain Res. Bull. 1987, 19:705-714.
51. Rice D.S., Curran T. Disabled-1 is expressed in type AII amacrine cells in the mouse retina. J. Comp. Neurol. 2000, 424:327-338.
52. Rothenberg S.J., Poblano A., Schnaas L. Brainstem auditory evoked response at five years and prenatal and postnatal blood lead. Neurotoxicol. Teratol. 2000, 22:503-510.
53. Rothenberg S.J., Schnaas L., Salgado-Valladares M., Casanueva E., Geller A.M., Hudnell H.K., Fox D.A. Increased ERG a- and b-wave amplitudes in 7- to 10-year-old children resulting from prenatal lead exposure. Invest. Ophthalmol. Vis. Sci. 2002, 43:2036-2044.
54. Ruan G.X., Allen G.C., Yamazaki S., McMahon D.G. An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS Biol. 2008, 6:e249.
55. Shulman L.M., Fox D.A. Dopamine inhibits mammalian photoreceptor Na+, K+-ATPase activity via a selective effect on the alpha3 isozyme. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:8034-8039.
56. Sriram K., Matheson J.M., Benkovic S.A., Miller D.B., Luster M.I., O'Callaghan J.P. Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: implications for Parkinson's disease. FASEB. 2002, 16:1474-1476.
57. Strettoi E., Volpini M. Retinal organization in the bcl-2-overexpressing transgenic mouse. J. Comp. Neurol. 2002, 446:1-10.
58. Skrandies W., Wässle H. Dopamine and serotonin in cat retina, electroretinography and histology. Exp. Brain Res. 1988, 71:231-240.
59. Todd R.D. Neural development is regulated by classical neurotransmitters: dopamine D2 receptor stimulation enhances neurite outgrowth. Biol. Psychiatry 1992, 31:794-807.
60. Versaux-Botteri C., Nguyen-Legros J., Vigny A., Raoux N. Morphology, density and distribution of tyrosine hydroxylase immunoreactive cells in the retina of mice. Brain Res. 1984, 301:192-197.
61. Voigt T., Wassle H. Dopaminergic innervation of AII amacrine cells in mammalian retina. J. Neurosci. 1987, 7:4115-4128.
62. Volpicelli F., Caiazzo M., Greco D., Consales C., Leone L., Perrone-Capano C., D.'Amato L.Colucci, di Porzio U. Bdnf gene is a downstream target of Nurr1 transcription factor in rat midbrain neurons in vitro. J. Neurochem. 2007, 102:441-453.
63. Wall M.A., Socolich M., Ranganathan R. The structural basis for red fluorescence in the tetrameric GFP homolog DsRed. Nat. Struct. Biol. 2000, 7:1133-1138.
64. Wasserman G.A., Musabegovic A., Liu X., Kline J., Factor-Litvak P., Graziano J.H. Lead exposure and motor functioning in 4(1/2)-year-old children: the Yugoslavia prospective study. J. Pediatr. 2000, 137:555-561.
65. Witkovsky P. Dopamine and retinal function. Doc. Ophthalmol. 2004, 108:17-40.
66. Wyatt R.J., Murphy D.L., Belmaker R., Cohen S., Donnelly C.H., Pollin W. Reduced monoamine oxidase activity in platelets: a possible genetic marker for vulnerability to schizophrenia. Science 1973, 179:916-918.
67. Xiao W., Liu W., Li Z., Liang D., Li L., White L.D., Fox D.A., Overbeek P.A., Chen Q. Gene expression profiling in embryonic mouse lenses. Mol. Vision 2006, 12:1692-1698.
68. Yuan J.S., Wang D., Stewart C.N. Statistical methods for efficiency adjusted real-time PCR quantification. Biotechnol. J. 2008, 3:112-123.
69. Zhang D.Q., Stone J.F., Zhou T., Ohta H., McMahon D.G. Characterization of genetically labeled catecholamine neurons in the mouse retina. Neuroreport 2004, 15:1761-1765.