Impaired structural and functional development of cerebellum following gestational exposure of deltamethrin in rats: Role of reelin

Cellular and Molecular Neurobiology

Volumn 33, Issue 5, 2013, Pages 731-746

  Kumar, Kamendra ^a   Patro, Nisha ^a   Patro, Ishan ^a  

^a JIWAJI UNIVERSITY   (India)

Author keywords

Cerebellum; Deltamethrin; Granule cell migration; Prenatal toxicity; Purkinje cells; Reelin

Indexed keywords

DELTAMETHRIN; REELIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; NITRILE; PYRETHROID; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BERGMANN GLIAL FIBER; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL DENSITY; CELL MIGRATION; CELL STRUCTURE; CEREBELLUM; CONTROLLED STUDY; DENDRITIC SPINE; DENDRITIC SPINE DENSITY; ENVIRONMENTAL EXPOSURE; EXTERNAL GRANULE CELL LAYER; FEMALE; GESTATION PERIOD; GRANULE CELL; MALE; NERVE FIBER; NERVE FIBER GROWTH; NEUROANATOMY; NEUROTOXICITY; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PURKINJE CELL; RAT; ANIMAL; BODY WEIGHT; DENDRITE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; MOTOR ACTIVITY; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PREGNANCY; ROTAROD TEST; TOXICITY; WISTAR RAT;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CELL ADHESION MOLECULES, NEURONAL; CEREBELLUM; DENDRITES; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MALE; MATERNAL EXPOSURE; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEUROGENESIS; NITRILES; PHENOTYPE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PURKINJE CELLS; PYRETHRINS; RATS; RATS, WISTAR; ROTAROD PERFORMANCE TEST; SERINE ENDOPEPTIDASES;

EID: 84878695763     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-013-9942-7     Document Type: Article

References (64)

1. Altman J, Bayer S (1995) Atlas of prenatal brain development. CRC Press, Boca Raton
2. Amweg EL, Weston DP, Ureda NM (2005) Use and toxicity of pyrethroid pesticides in the Central Valley, California, USA. Environ Toxicol Chem 24(4):966-972
3. Beffert U, Weeber EJ, Durudas A, Qiu S, Masiulis I, Sweatt JD, Li WP, Adelmann G, Frotscher M, Hammer RE, Herz J (2005) Modulation of synaptic plasticity and memory by reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47(4):567-579
4. Beffert U, Durudas A, Weeber EJ, Stolt PC, Giehl KM, Sweatt JD, Hammer RE, Herz J (2006) Functional dissection of reelin signaling by site-directed disruption of disabled-1 adaptor binding to apolipoprotein E receptor 2: distinct roles in development and synaptic plasticity. J Neurosci 26(7):2041-2052
5. Berkowitz GS, Obel J, Deych E, Lapinski R, Godbold J, Liu Z, Landrigan PJ, Wolff MS (2003) Exposure to indoor pesticides during pregnancy in a multiethnic, urban cohort. Environ Health Perspect 111(1):79-84
6. Botella-Lopez A, Burgaya F, Gavin R, Garcia-Ayllon MS, Gomez-Tortosa E, Pena-Casanova J, Urena JM, Del Rio JA, Blesa R, Soriano E, Saez-Valero J (2006) Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc Natl Acad Sci USA 103(14):5573-5578
7. Campo CG, Sinagra M, Verrier D, Manzoni OJ, Chavis P (2009) Reelin secreted by GABAergic neurons regulates glutamate receptor homeostasis. PLoS ONE 4(5):e5505
8. Chizhikov VV, Lindgren AG, Currle DS, Rose MF, Monuki ES, Millen KJ (2006) The roof plate regulates cerebellar cell-type specification and proliferation. Development 133(15):2793-2804
9. Choi BH, Yee S, Robles M (1996) The effects of glutathione glycoside in methyl mercury poisoning. Toxicol Appl Pharmacol 141(2):357-364
10. D'Arca D, Zhao X, Xu W, Ramirez-Martinez NC, Iavarone A, Lasorella A (2010) Huwe1 ubiquitin ligase is essential to synchronize neuronal and glial differentiation in the developing cerebellum. Proc Natl Acad Sci USA 107(13):5875-5880
11. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374(6524):719-723
12. Durakoglugil MS, Chen Y, White CL, Kavalali ET, Herz J (2009) Reelin signaling antagonizes beta-amyloid at the synapse. Proc Natl Acad Sci USA 106(37):15938-15943
13. Duveau V, Madhusudan A, Caleo M, Knuesel I, Fritschy JM (2011) Impaired reelin processing and secretion by Cajal-Retzius cells contributes to granule cell dispersion in a mouse model of temporal lobe epilepsy. Hippocampus 21(9):935-944
14. Forster E, Bock HH, Herz J, Chai X, Frotscher M, Zhao S (2010) Emerging topics in reelin function. Eur J Neurosci 31(9):1511-1518
15. Frotscher M (2010) Role for reelin in stabilizing cortical architecture. Trends Neurosci 33(9):407-414
16. Frotscher M, Haas CA, Forster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13(6):634-640
17. Gohlke JM, Armant O, Parham FM, Smith MV, Zimmer C, Castro DS, Nguyen L, Parker JS, Gradwohl G, Portier CJ, Guillemot F (2008) Characterization of the proneural gene regulatory network during mouse telencephalon development. BMC Biol 6:15
18. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR, Impagnatiello F, Pandey G, Pesold C, Sharma R, Uzunov D, Costa E (2000) Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatr 57(11):1061-1069
19. Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Gotz M (2003) Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130(19):4597-4609
20. Hatten ME, Alder J, Zimmerman K, Heintz N (1997) Genes involved in cerebellar cell specification and differentiation. Curr Opin Neurobiol 7(1):40-47
21. Herz J, Chen Y (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 7(11):850-859
22. Heudorf U, Angerer J, Drexler H (2004) Current internal exposure to pesticides in children and adolescents in Germany: urinary levels of metabolites of pyrethroid and organophosphorus insecticides. Int Arch Occup Environ Health 77(1):67-72
23. Hevner RF (2008) Reelin and the cerebellum. In: Fatemi SH (ed) Reelin glycoprotein. Springer, Heidelberg, pp 141-158
24. Hevner RF, Hodge RD, Daza RA, Englund C (2006) Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res 55(3):223-233
25. Hibi T, Mizutani M, Baba A, Hattori M (2009) Splicing variations in the ligand-binding domain of ApoER2 results in functional differences in the binding properties to reelin. Neurosci Res 63(4):251-258
26. Hunter-Schaedle KE (1997) Radial glial cell development and transformation are disturbed in reeler forebrain. J Neurobiol 33(4):459-472
27. Knuesel I, Nyffeler M, Mormede C, Muhia M, Meyer U, Pietropaolo S, Yee BK, Pryce CR, LaFerla FM, Marighetto A, Feldon J (2009) Age-related accumulation of reelin in amyloid-like deposits. Neurobiol Aging 30(5):697-716
28. Matsuki T, Pramatarova A, Howell BW (2008) Reduction of Crk and CrkL expression blocks reelin-induced dendritogenesis. J Cell Sci 121(Pt 11):1869-1875
29. Miller MW, Robertson S (1993) Prenatal exposure to ethanol alters the postnatal development and transformation of radial glia to astrocytes in the cortex. J Comp Neurol 337(2):253-266
30. Mohn AR, Gainetdinov RR, Caron MG, Koller BH (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98(4):427-436
31. Narahashi T (2000) Neuroreceptors and ion channels as the basis for drug action: past, present, and future. J Pharmacol Exp Ther 294(1):1-26
32. Niu S, Renfro A, Quattrocchi CC, Sheldon M, D'Arcangelo G (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41(1):71-84
33. Niu S, Yabut O, D'Arcangelo G (2008) The reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J Neurosci 28(41):10339-10348
34. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14(5):899-912
35. Olson EC, Kim S, Walsh CA (2006) Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J Neurosci 26(6):1767-1775
36. Pang T, Atefy R, Sheen V (2008) Malformations of cortical development. Neurologist 14(3):181-191
37. Patro N, Patro IK (2005) Effects of deltamethrin on granule cell migration during postnatal development of rat cerebellum. Indian J Exp Biol 43(2):158-162
38. Patro N, Mishra S, Chattopadhyay M, Patro I (1997) Neurotoxicological effects of deltamethrin on the postnatal development of cerebellum of rat. J Biosci 22(2):117-130
39. Patro N, Shrivastava M, Tripathi S, Patro IK (2009) S100beta upregulation: a possible mechanism of deltamethrin toxicity and motor coordination deficits. Neurotoxicol Teratol 31(3):169-176
40. Perez-Garcia CG, Tissir F, Goffinet AM, Meyer G (2004) Reelin receptors in developing laminated brain structures of mouse and human. Eur J Neurosci 20(10):2827-2832
41. Pinto-Lord MC, Evrard P, Caviness VS Jr (1982) Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Brain Res 256(4):379-393
42. Pujadas L, Gruart A, Bosch C, Delgado L, Teixeira CM, Rossi D, de Lecea L, Martinez A, Delgado-Garcia JM, Soriano E (2010) Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J Neurosci 30(13):4636-4649
43. Rakic P (1977) Genesis of the dorsal lateral geniculate nucleus in the rhesus monkey: site and time of origin, kinetics of proliferation, routes of migration and pattern of distribution of neurons. J Comp Neurol 176(1):23-52
44. Ramos-Moreno T, Galazo MJ, Porrero C, Martinez-Cerdeno V, Clasca F (2006) Extracellular matrix molecules and synaptic plasticity: immunomapping of intracellular and secreted reelin in the adult rat brain. Eur J Neurosci 23(2):401-422
45. Ray DE, Fry JR (2006) A reassessment of the neurotoxicity of pyrethroid insecticides. Pharmacol Ther 111(1):174-193
46. Rice DS, Curran T (1999) Mutant mice with scrambled brains: understanding the signaling pathways that control cell positioning in the CNS. Genes Dev 13(21):2758-2773
47. Rice DS, Curran T (2001) Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24:1005-1039
48. Roper SN, Abraham LA, Streit WJ (1997) Exposure to in utero irradiation produces disruption of radial glia in rats. Dev Neurosci 19(6):521-528
49. Sergaki MC, Guillemot F, Matsas R (2010) Impaired cerebellar development and deficits in motor coordination in mice lacking the neuronal protein BM88/Cend1. Mol Cell Neurosci 44(1):15-29
50. Shafer TJ, Meyer DA, Crofton KM (2005) Developmental neurotoxicity of pyrethroid insecticides: critical review and future research needs. Environ Health Perspect 113(2):123-136
51. Sinagra M, Gonzalez Campo C, Verrier D, Moustie O, Manzoni OJ, Chavis P (2008) Glutamatergic cerebellar granule neurons synthesize and secrete reelin in vitro. Neuron Glia Biol 4(3):189-196
52. Soderlund DM (2010) State-dependent modification of voltage-gated sodium channels by pyrethroids. Pestic Biochem Physiol 97(2):78-86
53. Soderlund DM, Clark JM, Sheets LP, Mullin LS, Piccirillo VJ, Sargent D, Stevens JT, Weiner ML (2002) Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 171(1):3-59
54. Spalice A, Parisi P, Nicita F, Pizzardi G, Del Balzo F, Iannetti P (2009) Neuronal migration disorders: clinical, neuroradiologic and genetics aspects. Acta Paediatr 98(3):421-433
55. Stensaas LJ (1967) The development of hippocampal and dorsolateral pallial region of the cerebral hemisphere in fetal rabbits. V. Sixty millimeter stage, glial cell morphology. J Comp Neurol 131(1967):423-436
56. Tabata H, Nakajima K (2002) Neurons tend to stop migration and differentiate along the cortical internal plexiform zones in the reelin signal-deficient mice. J Neurosci Res 69(6):723-730
57. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4(6):496-505
58. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97(6):689-701
59. Verrotti A, Agostinelli S, Mohn A, Manco R, Coppola G, Franzoni E, Cerminara C, Parisi P, Iannetti P, Spalice A (2009) Clinical features of psychogenic non-epileptic seizures in prepubertal and pubertal patients with idiopathic epilepsy. Neurol Sci 30(4):319-323
60. Verschoyle RD, Aldridge WN (1980) Structure-activity relationships of some pyrethroids in rats. Arch Toxicol 45(4):325-329
61. Vijverberg HP, van den Bercken J (1990) Neurotoxicological effects and the mode of action of pyrethroid insecticides. Crit Rev Toxicol 21(2):105-126
62. Weeber EJ, Beffert U, Jones C, Christian JM, Forster E, Sweatt JD, Herz J (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277(42):39944-39952
63. Wolansky MJ, Gennings C, DeVito MJ, Crofton KM (2009) Evidence for dose-additive effects of pyrethroids on motor activity in rats. Environ Health Perspect 117(10):1563-1570
64. Yoshiki A, Kusakabe M (1998) Cerebellar histogenesis as seen in identified cells of normal-reeler mouse chimeras. Int J Dev Biol 42(5):695-700