Low-level gestational lead exposure increases retinal progenitor cell proliferation and rod photoreceptor and bipolar cell neurogenesis in mice

Environmental Health Perspectives

Volumn 119, Issue 1, 2011, Pages 71-77

  Giddabasappa, Anand ^a   Ryan Hamilton, W ^a   Chaney, Shawntay ^a   Xiao, Weimin ^b   Johnson, Jerry E ^c   Mukherjee, Shradha ^a   Fox, Donald A ^a,b,d  

^a University of Houston   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

^c UNIVERSITY OF HOUSTON DOWNTOWN   (United States)

^d UNIVERSITY OF HOUSTON   (United States)

Author keywords

Bipolar cells; Development; Gestational exposure; Glia; Lead; Mice; Neurogenesis; Proliferation; Retina; Rod photoreceptors

Indexed keywords

BROXURIDINE; KI 67 ANTIGEN; LEAD;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL FATE; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; FEMALE; GESTATION PERIOD; IN VIVO STUDY; LEAD BLOOD LEVEL; MOUSE; MUELLER CELL; NERVE CELL DIFFERENTIATION; NEUROTOXICITY; NICK END LABELING; NONHUMAN; PHENOTYPE; PRENATAL EXPOSURE; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA INJURY; RETINA ROD; SIGNAL TRANSDUCTION; STEM CELL; WESTERN BLOTTING;

ANIMALS; CELL PROLIFERATION; ENVIRONMENTAL POLLUTANTS; FEMALE; LEAD; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; NEUROGENESIS; RETINA; RETINAL BIPOLAR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SIGNAL TRANSDUCTION; STEM CELLS;

ANIMALIA; MURINAE; MUS;

EID: 78751508086     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1002524     Document Type: Article

References (38)

1. Alexiades MR, Cepko C. 1996. Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn 205:293-307.
2. Alkondon M, Costa AC, Radhakrishnan V, Aronstam RS, Albuquerque EX. 1990. Selective blockade of NMDA-activated channel currents may be implicated in learning defcits caused by lead. FEBS Lett 261:124-130.
3. Barton KM, Levine EM. 2008. Expression patterns and cell cycle profles of PCNA, MCM6, cyclin D1, cyclin A2, cyclin B1, and phosphorylated histone H3 in the developing mouse retina. Dev Dyn 237:672-682.
4. CDC (Centers for Disease Control and Prevention). 1991. Preventing Lead Poisoning in Young Children: A Statement by the Centers for Disease Control and Prevention. Atlanta, GA:CDC.
5. Chetty CS, Reddy GR, Murthy KS, Johnson J, Sajwan K, Desiah D. 2001. Perinatal lead exposure alters the expression of neuronal nitric oxide synthase in rat brain. Int J Toxicol 20:113-120.
6. Fox DA, Boyes WK. 2008. Toxic responses of the ocular and visual system. In: Casarett and Doull's Toxicology: The Science of Poisons (Klaassen CD, ed). 7th ed. New York:McGraw-Hill, 665-697.
7. Fox DA, Campbell ML, Blocker YS. 1997. Functional alterations and apoptotic cell death in the retina following developmental or adult lead exposure. Neurotoxicology 18:645-664.
8. Fox DA, Kala SV, Hamilton WR, Johnson JE, O'Callaghan JP. 2008. Low-level human equivalent gestational lead exposure produces supernormal scotopic electroretinograms, increased retinal neurogenesis and decreased dopamine utilization in rats. Environ Health Perspect 116:618-625.
9. Gilbert ME, Kelly ME, Samsam TE, Goodman JH. 2005. Chronic developmental lead exposure reduces neurogenesis in adult rat hippocampus but does not impair spatial learning. Toxicol Sci 86:365-374.
10. Grandjean P, Landrigan PJ. 2006. Developmental neurotoxicity of industrial chemicals. Lancet 368:2167-2178.
11. Green ES, Stubbs JL, Levine EM. 2003. Genetic rescue of cell number in a mouse model of microphthalmia: inter actions between Chx10 and G1-phase cell cycle regulators. Development 130:539-552.
12. He L, Perkins GA, Poblenz AT, Harris JB, Hung M, Ellisman MH, et al. 2003. Bcl-xL overexpression blocks bax-mediated mitochondrial contact site formation and apoptosis in rod photo receptors of lead-exposed mice. Proc Natl Acad Sci USA 100:1022-1027.
13. He L, Poblenz AT, Medrano CJ, Fox DA. 2000. Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J Biol Chem 275:12175-12184.
14. Jeon CJ, Strettoi E, Masland RH. 1998. The major cell populations of the mouse retina. J Neurosci 18:8936-8946.
15. 2+ dynamics in vertebrate rod and cone ribbon synapses. Mol Vis 13:887-919.
16. Leasure JL, Giddabasappa A, Chaney S, Johnson JE Jr, Pothakos K, Lau YS, et al. 2008. Low-level human equivalent gestational lead exposure produces sex-specifc motor and coordination abnormalities and late-onset obesity in year-old mice. Environ Health Perspect 116:355-361.
17. Lilienthal H, Kohler K, Turfeld M, Winneke G. 1994. Persistent increases in scotopic B-wave amplitudes after lead exposure in monkeys. Exp Eye Res 59:203-209.
18. Livesey FJ, Cepko CL. 2001. Vetebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2:109-118.
19. Lucocq JM. 2007. Effcient quantitative morphological pheno-typing of genetically altered organisms using stereology. Transgenic Res 16:133-145.
20. Magalhães CR, Socodato RE, Paes-de-Carvalho R. 2006. Nitric oxide regulates the proliferation of chick embryo retina cells by a cyclic GMP-independent mechanism. Int J Devel Neurosci 24:53-60.
21. Martins RA, Pearson RA. 2008. Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res 1192:37-60.
22. Mendola P, Selevan SG, Gutter S, Rice D. 2002. Environmental factors associated with a spectrum of neurodevelopmental defcits. Ment Retard Dev Disabil Res Rev 8:188-197.
23. Musshoff U, Madeja M, Binding N, Witting U, Speckmann EJ. 1995. Lead-induced blockage of kainate-sensitive receptor channels. Naunyn Schmiedebergs Arch Pharmacol 353:42-45.
24. Nagpal AG, Brodie SE. 2009. Supranormal electroretinogram in a 10-year-old girl with lead toxicity. Doc Ophthalmol 118:163-166.
25. NIH (National Institutes of Health). 2002. Public Health Service Policy on the Humane Care and Use of Laboratory Animals. Available: http://grants.nih.gov/grants/olaw/references/ phspol.htm [accessed 5 June 2010].
26. NIH (National Institutes of Health). 2009. ImageJ (version 1.38e). Available: http://rsb.info.nih.gov/ij/ [accessed 6 February 2010].
27. Portera-Cailliau C, Sung CH, Nathans J, Adler R. 1994. Apoptotic photoreceptor cell death in mouse models of retinitis pig-mentosa. Proc Natl Acad Sci USA 91:974-978.
28. Rachel RA, Dolen G, Hayes NL, Lu A, Erskine L, Nowakowski RS, et al. 2002. Spatiotemporal features of early neurono genesis differ in wild-type and albino mouse retina. J Neurosci 22:4249-4263.
29. 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.
30. Rice DS, Curran T. 2000. Disabled-1 is expressed in type AII ama-crine cells in the mouse retina. J Comp Neurol 424:327-338.
31. 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.
32. Strettoi E, Volpini M. 2002. Retinal organization in the bcl-2-overexpressing transgenic mouse. J Comp Neurol 446:1-10.
33. Tan E, Wang Q, Quiambao AB, Xu X, Qtaishat NM, Peachey NS, et al. 2001. The relationship between opsin overexpression and photoreceptor degeneration. Invest Ophthalmol Vis Sci 42:589-600.
34. Turner DL, Cepko CL. 1987. A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131-136.
35. Verina T, Rohde CA, Guilarte TR. 2007. Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats. Neuroscience 145:1037-1047.
36. Young RW. 1984. Cell death during differentiation of the retina in the mouse. J Comp Neurol 229:362-373.
37. Young RW. 1985. Cell differentiation in the retina of the mouse. Anat Rec 212:199-205.
38. Young RW. 1985. Cell proliferation during postnatal development of the retina in the mouse. Brain Res 353:229-239.