Prenatal exposure to a common organophosphate insecticide delays motor development in a mouse model of idiopathic autism

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  De Felice, Alessia ^a,b   Scattoni, Maria Luisa ^a   Ricceri, Laura ^a   Calamandrei, Gemma ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPYRIFOS; ORGANOPHOSPHATE INSECTICIDE; INSECTICIDE;

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; BODY GROWTH; COMPULSION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; FEMALE; GESTATION PERIOD; GROOMING; IDIOPATHIC DISEASE; LOCOMOTION; MALE; MOTOR DEVELOPMENT; MOTOR DEVELOPMENTAL DELAY; MOUSE; NERVE CELL DIFFERENTIATION; NEUROTOXICITY; NEWBORN; NONHUMAN; ONTOGENY; PATHOGENESIS; PRENATAL EXPOSURE; PROGENY; RIGHTING REFLEX; SEX DIFFERENCE; SEXUALITY; SOCIAL INTERACTION; VOCALIZATION; WEIGHT GAIN; ANIMAL; DRUG EFFECTS; HUMAN RELATION; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PREGNANCY; PSYCHOLOGY; REPRODUCTION;

MUS;

ANIMALS; ANIMALS, NEWBORN; AUTISTIC DISORDER; CHLORPYRIFOS; FEMALE; GROOMING; INSECTICIDES; INTERPERSONAL RELATIONS; MALE; MICE; MOTOR ACTIVITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REFLEX, RIGHTING; REPRODUCTION; VOCALIZATION, ANIMAL;

EID: 84925852697     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121663     Document Type: Article

References (79)

1. Abrahams BS, Geschwind DH. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet. 2008;9(5):341-55. doi: 10.1038/nrg2346 PMID: 18414403
2. Persico AM, Bourgeron T. Searching for ways out of the autism maze: genetic, epigenetic and environmental clues. Trends Neurosci. 2006;29(7):349-58. PMID: 16808981
3. Schwartzer JJ, Careaga M, Onore CE, Rushakoff JA, Berman RF, Ashwood P. Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice. Transl Psychiatry. 2013;3:e240. doi: 10.1038/tp. 2013.16 PMID: 23481627
4. Grandjean P, Landrigan PJ. Neurobehavioural effects of developmental toxicity. Lancet Neurol. 2014;13(3):330-8. doi: 10.1016/S1474-4422 (13) 70278-3 PMID: 24556010
5. Atladottir HO, Thorsen P, Ostergaard L, Schendel DE, Lemcke S, Abdallah M, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010;40(12):1423-30. doi: 10.1007/s10803-010-1006-y PMID: 20414802
6. Chess S. Autism in children with congenital rubella. J Autism Child Schizophr. 1971;1(1):33-47. PMID: 5172438
7. Chess S. Follow-up report on autism in congenital rubella. J Autism Child Schizophr. 1977;7(1):69-81. PMID: 576606
8. Mednick SA, Machon RA, Huttunen MO, Bonett D. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch Gen Psychiatry. 1988;45(2):189-92. PMID: 3337616
9. O'Roak BJ, Vives L, Girirajan S, Karakoc E, Krumm N, Coe BP, et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature. 2012;485(7397):246-50. doi: 10. 1038/nature10989 PMID: 22495309
10. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368(9553):2167-78. PMID: 17174709
11. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, et al. Genetic heritability and shared environmental factors among twin pairs with autism. Arch Gen Psychiatry. 2011;68(11):1095-102. doi: 10.1001/archgenpsychiatry.2011.76 PMID: 21727249
12. Rossignol DA, Genuis SJ, Frye RE. Environmental toxicants and autism spectrum disorders: a systematic review. Transl Psychiatry. 2014;4:e360. doi: 10.1038/tp. 2014.4 PMID: 24518398
13. Shelton JF, Hertz-Picciotto I, Pessah IN. Tipping the balance of autism risk: potential mechanisms linking pesticides and autism. Environ Health Perspect. 2012;120(7):944-51. doi: 10.1289/ehp. 1104553 PMID: 22534084
14. Pessah IN, Seegal RF, Lein PJ, LaSalle J, Yee BK, Van De Water J, et al. Immunologic and neurodevelopmental susceptibilities of autism. Neurotoxicology. 2008;29(3):532-45. doi: 10.1016/j.neuro.2008. 02.006 PMID: 18394707
15. Mullen BR, Khialeeva E, Hoffman DB, Ghiani CA, Carpenter EM. Decreased reelin expression and organophosphate pesticide exposure alters mouse behaviour and brain morphology. ASN Neuro. 2012;5(1):e00106. doi: 10.1042/AN20120060 PMID: 23298182
16. Woods R, Vallero RO, Golub MS, Suarez JK, Ta TA, Yasui DH, et al. Long-lived epigenetic interactions between perinatal PBDE exposure and Mecp2308 mutation. Hum Mol Genet. 2012;21(11):2399-411. doi: 10.1093/hmg/dds046 PMID: 22343140
17. Bolivar VJ, Walters SR, Phoenix JL. Assessing autism-like behavior in mice: variations in social interactions among inbred strains. Behav Brain Res. 2007;176(1):21-6. PMID: 17097158
18. McFarlane HG, Kusek GK, Yang M, Phoenix JL, Bolivar VJ, Crawley JN. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 2008;7(2):152-63. PMID: 17559418
19. Moy SS, Nadler JJ, Young NB, Perez A, Holloway LP, Barbaro RP, et al. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res. 2007;176(1):4-20. PMID: 16971002
20. Yang M, Scattoni ML, Zhodzishsky V, Chen T, Caldwell H, Young WS, et al. Social approach behaviors are similar on conventional versus reverse lighting cycles, and in replications across cohorts, in BTBR T+ tf/J, C57BL/6J, and vasopressin receptor 1B mutant mice. Front Behav Neurosci. 2007;1:1. doi: 10. 3389/neuro.08.001.2007 PMID: 18958184
21. Yang M, Zhodzishsky V, Crawley JN. Social deficits in BTBR T+tf/J mice are unchanged by cross-fostering with C57BL/6J mothers. Int J Dev Neurosci. 2007;25(8):515-21. PMID: 17980995
22. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One. 2008;3(8):e3067. doi: 10.1371/journal.pone.0003067 PMID: 18728777
23. Scattoni ML, Ricceri L, Crawley JN. Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes Brain Behav. 2011;10(1):44-56. doi: 10.1111/j.1601-183X.2010.00623.x PMID: 20618443
24. Roullet FI, Wohr M, Crawley JN. Female urine-induced male mice ultrasonic vocalizations, but not scent-marking, is modulated by social experience. Behav Brain Res. 2010;216(1):19-28. doi: 10.1016/j.bbr.2010.06.004 PMID: 20540967
25. Wohr M, Moles A, Schwarting RK, D'Amato FR. Lack of social exploratory activation in male mu-opioid receptor KO mice in response to playback of female ultrasonic vocalizations. Soc Neurosci. 2010;6(1):76-87. doi: 10.1080/17470911003765560 PMID: 20503133
26. Jones-Davis DM, Yang M, Rider E, Osbun NC, da Gente GJ, Li J, et al. Quantitative trait loci for interhemispheric commissure development and social behaviors in the BTBR T (+) tf/J mouse model of autism. PLoS One. 2013;8(4):e61829. doi: 10.1371/journal.pone.0061829 PMID: 23613947
27. Cusco I, Medrano A, Gener B, Vilardell M, Gallastegui F, Villa O, et al. Autism-specific copy number variants further implicate the phosphatidylinositol signaling pathway and the glutamatergic synapse in the etiology of the disorder. Hum Mol Genet. 2009;18(10):1795-804. doi: 10.1093/hmg/ddp092 PMID: 19246517
28. Levitt P, Campbell DB. The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J Clin Invest. 2009;119(4):747-54. doi: 10.1172/JCI37934 PMID: 19339766
29. Pearson BL, Bettis JK, Meyza KZ, Yamamoto LY, Blanchard DC, Blanchard RJ. Absence of social conditioned place preference in BTBR T+tf/J mice: relevance for social motivation testing in rodent models of autism. Behav Brain Res. 2012;233(1):99-104. doi: 10.1016/j.bbr.2012.04.040 PMID: 22562042
30. Amodeo DA, Jones JH, Sweeney JA, Ragozzino ME. Differences in BTBR T+ tf/J and C57BL/6J mice on probabilistic reversal learning and stereotyped behaviors. Behav Brain Res. 2012;227(1):64-72. doi: 10.1016/j.bbr.2011.10.032 PMID: 22056750
31. Yang M, Abrams DN, Zhang JY, Weber MD, Katz AM, Clarke AM, et al. Low sociability in BTBR T+tf/J mice is independent of partner strain. Physiol Behav. 2012;107(5):649-62. doi: 10.1016/j.physbeh. 2011.12.025 PMID: 22245067
32. Pearson BL, Pobbe RL, Defensor EB, Oasay L, Bolivar VJ, Blanchard DC, et al. Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism. Genes Brain Behav. 2011;10(2):228-35. doi: 10.1111/j.1601-183X.2010.00659.x PMID: 21040460
33. Silverman JL, Yang M, Turner SM, Katz AM, Bell DB, Koenig JI, et al. Low stress reactivity and neuroendocrine factors in the BTBR T+tf/J mouse model of autism. Neuroscience. 2010;171(4):1197-208. doi: 10.1016/j.neuroscience.2010.09.059 PMID: 20888890
34. Saunders M, Magnanti BL, Correia Carreira S, Yang A, Alamo-Hernandez U, Riojas-Rodriguez H, et al. Chlorpyrifos and neurodevelopmental effects: a literature review and expert elicitation on research and policy. Environ Health. 2012;11 Suppl 1:S5. doi: 10.1186/1476-069X-11-S1-S5 PMID: 22759505
35. Engel SM, Wetmur J, Chen J, Zhu C, Barr DB, Canfield RL, et al. Prenatal exposure to organophosphates, paraoxonase 1, and cognitive development in childhood. Environ Health Perspect. 2011;119(8):1182-8. doi: 10.1289/ehp. 1003183 PMID: 21507778
36. Eskenazi B, Marks AR, Bradman A, Harley K, Barr DB, Johnson C, et al. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ Health Perspect. 2007;115(5):792-8. PMID: 17520070
37. Rauh V, Arunajadai S, Horton M, Perera F, Hoepner L, Barr DB, et al. Seven-year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ Health Perspect. 2011;119(8):1196-201. doi: 10.1289/ehp. 1003160 PMID: 21507777
38. Eaton DL, Daroff RB, Autrup H, Bridges J, Buffler P, Costa LG, et al. Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol. 2008; 38 Suppl 2:1-125. doi: 10.1080/10408440802272158 PMID: 18726789
39. Slotkin TA, Seidler FJ. Prenatal chlorpyrifos exposure elicits presynaptic serotonergic and dopaminergic hyperactivity at adolescence: critical periods for regional and sex-selective effects. Reprod Toxicol. 2007;23(3):421-7. PMID: 17267174
40. Tait S, Ricceri L, Venerosi A, Maranghi F, Mantovani A, Calamandrei G. Long-term effects on hypothalamic neuropeptides after developmental exposure to chlorpyrifos in mice. Environ Health Perspect. 2009;117(1):112-6. doi: 10.1289/ehp. 11696 PMID: 19165396
41. Venerosi A, Ricceri L, Rungi A, Sanghez V, Calamandrei G. Gestational exposure to the organophosphate chlorpyrifos alters social-emotional behaviour and impairs responsiveness to the serotonin transporter inhibitor fluvoxamine in mice. Psychopharmacology (Berl). 2010;208(1):99-107. doi: 10.1007/s00213-009-1713-2 PMID: 19921154
42. Venerosi A, Ricceri L, Tait S, Calamandrei G. Sex dimorphic behaviors as markers of neuroendocrine disruption by environmental chemicals: the case of chlorpyrifos. Neurotoxicology. 2012;33(6):1420-6. doi: 10.1016/j.neuro.2012.08.009 PMID: 22947518
43. Ricceri L, Venerosi A, Capone F, Cometa MF, Lorenzini P, Fortuna S, et al. Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice. Toxicol Sci. 2006;93(1):105-13. PMID: 16760416
44. Venerosi A, Cutuli D, Colonnello V, Cardona D, Ricceri L, Calamandrei G. Neonatal exposure to chlorpyrifos affects maternal responses and maternal aggression of female mice in adulthood. Neurotoxicol Teratol. 2008;30(6):468-74. doi: 10.1016/j.ntt.2008.07.002 PMID: 18674613
45. Dam K, Seidler FJ, Slotkin TA. Chlorpyrifos exposure during a critical neonatal period elicits gender-selective deficits in the development of coordination skills and locomotor activity. Brain Res Dev Brain Res. 2000;121(2):179-87. PMID: 10876030
46. Venerosi A, Ricceri L, Scattoni ML, Calamandrei G. Prenatal chlorpyrifos exposure alters motor behavior and ultrasonic vocalization in CD-1 mouse pups. Environ Health. 2009;8:12. doi: 10.1186/1476-069X-8-12 PMID: 19331648
47. Picker JD, Yang R, Ricceri L, Berger-Sweeney J. An altered neonatal behavioral phenotype in Mecp2 mutant mice. Neuroreport. 2006;17(5):541-4. PMID: 16543822
48. Moreira EG, Yu X, Robinson JF, Griffith W, Hong SW, Beyer RP, et al. Toxicogenomic profiling in maternal and fetal rodent brains following gestational exposure to chlorpyrifos. Toxicol Appl Pharmacol. 2010;245(3):310-25. doi: 10.1016/j.taap. 2010.03.015 PMID: 20350560
49. Brunelli SA, Hofer MA. Selective breeding for infant rat separation-induced ultrasonic vocalizations: developmental precursors of passive and active coping styles. Behav Brain Res. 2007;182(2):193-207. PMID: 17543397
50. Zimmerberg B, Rosenthal AJ, Stark AC. Neonatal social isolation alters both maternal and pup behaviors in rats. Dev Psychobiol. 2003;42(1):52-63. PMID: 12471636
51. Romano E, Michetti C, Caruso A, Laviola G, Scattoni ML. Characterization of neonatal vocal and motor repertoire of reelin mutant mice. PLoS One. 2013;8(5):e64407. doi: 10.1371/journal.pone.0064407 PMID: 23700474
52. Chadman KK, Gong S, Scattoni ML, Boltuck SE, Gandhy SU, Heintz N, et al. Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res. 2008;1(3):147-58. doi: 10.1002/aur.22 PMID: 19360662
53. Branchi I, Santucci D, Alleva E. Ultrasonic vocalisation emitted by infant rodents: a tool for assessment of neurobehavioural development. Behav Brain Res. 2001;125(1-2):49-56. PMID: 11682119
54. Cirulli F, Alleva E. Effects of repeated administrations of EGF and TGF-alpha on mouse neurobehavioral development. Neurotoxicology. 1994;15(4):819-25. PMID: 7715853
55. De Filippis B, Ricceri L, Laviola G. Early postnatal behavioral changes in the Mecp2-308 truncation mouse model of Rett syndrome. Genes Brain Behav. 2010;9(2):213-23. doi: 10.1111/j.1601-183X.2009.00551.x PMID: 19958389
56. Spear LP, Penson J, Linville DG. GABA and behavioral inhibition in the neonatal rat pup. Psychopharmacology (Berl). 1986;90(1):106-11. PMID: 3094052
57. Branchi I, Santucci D, Puopolo M, Alleva E. Neonatal behaviors associated with ultrasonic vocalizations in mice (mus musculus): A slow-motion analysis. Dev Psychobiol. 2004;44(1):37-44. PMID: 14704988
58. Hofer MA, Shair H. Ultrasonic vocalization during social interaction and isolation in 2-weeek-old rats. Dev Psychobiol. 1978;11(5):495-504. PMID: 689298
59. Wohr M, Schwarting RK. Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat. Behav Neurosci. 2008;122(2):310-30. doi: 10.1037/0735-7044.122.2.310 PMID: 18410171
60. Rugh R. The Mouse: Its reproduction and development. Oxford University Press; Oxford:. 1990.
61. Holy TE, Guo Z. Ultrasonic songs of male mice. PLoS Biol. 2005;3(12):e386. PMID: 16248680
62. Altman J, Sudarshan K. Postnatal development of locomotion in the laboratory rat. Anim Behav. 1975;23(4):896-920. PMID: 1200422
63. Cazalets JR, Gardette M, Hilaire G. Locomotor network maturation is transiently delayed in the MAOAdeficient mouse. J Neurophysiol. 2000;83(4):2468-70. PMID: 10758149
64. Aldridge JE, Seidler FJ, Slotkin TA. Developmental exposure to chlorpyrifos elicits sex-selective alterations of serotonergic synaptic function in adulthood: critical periods and regional selectivity for effects on the serotonin transporter, receptor subtypes, and cell signaling. Environ Health Perspect. 2004;112(2):148-55. PMID: 14754568
65. Gould GG, Hensler JG, Burke TF, Benno RH, Onaivi ES, Daws LC. Density and function of central serotonin (5-HT) transporters, 5-HT1A and 5-HT2A receptors, and effects of their targeting on BTBR T+tf/J mouse social behavior. J Neurochem. 2011;116(2):291-303. doi: 10.1111/j.1471-4159.2010.07104. x PMID: 21070242
66. Dierssen M, Fotaki V, Martinez de Lagran M, Gratacos M, Arbones M, Fillat C, et al. Neurobehavioral development of two mouse lines commonly used in transgenic studies. Pharmacol Biochem Behav. 2002;73(1):19-25. PMID: 12076721
67. Fox WM. Reflex-ontogeny and behavioural development of the mouse. Anim Behav. 1965;13(2):234-41. PMID: 5835840
68. Santos M, Silva-Fernandes A, Oliveira P, Sousa N, Maciel P. Evidence for abnormal early development in a mouse model of Rett syndrome. Genes Brain Behav. 2007;6(3):277-86. PMID: 16848781
69. Shu W, Cho JY, Jiang Y, Zhang M, Weisz D, Elder GA, et al. Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Natl Acad Sci U S A. 2005;102(27):9643-8. PMID: 15983371
70. Whyatt RM, Rauh V, Barr DB, Camann DE, Andrews HF, Garfinkel R, et al. Prenatal insecticide exposures and birth weight and length among an urban minority cohort. Environ Health Perspect. 2004;112(10):1125-32. PMID: 15238288
71. Young JG, Eskenazi B, Gladstone EA, Bradman A, Pedersen L, Johnson C, et al. Association between in utero organophosphate pesticide exposure and abnormal reflexes in neonates. Neurotoxicology. 2005;26(2):199-209. PMID: 15713341
72. Leonard HC, Bedford R, Charman T, Elsabbagh M, Johnson MH, Hill EL. Motor development in children at risk of autism: a follow-up study of infant siblings. Autism. 2014;18(3):281-91. doi: 10.1177/1362361312470037 PMID: 24101718
73. Bhat AN, Galloway JC, Landa RJ. Relation between early motor delay and later communication delay in infants at risk for autism. Infant Behav Dev. 2012;35(4):838-46. doi: 10.1016/j.infbeh.2012.07.019 PMID: 22982285
74. Esposito G, Venuti P, Apicella F, Muratori F. Analysis of unsupported gait in toddlers with autism. Brain Dev. 2011;33(5):367-73. doi: 10.1016/j.braindev. 2010.07.006 PMID: 20708861
75. Leary MR, Hill DA. Moving on: autism and movement disturbance. Ment Retard. 1996;34(1):39-53. PMID: 8822025
76. Laviola G, Adriani W, Gaudino C, Marino R, Keller F. Paradoxical effects of prenatal acetylcholinesterase blockade on neuro-behavioral development and drug-induced stereotypies in reeler mutant mice. Psychopharmacology (Berl). 2006;187(3):331-44. PMID: 16783542
77. Venerosi A, Calamandrei G, Ricceri L. A social recognition test for female mice reveals behavioral effects of developmental chlorpyrifos exposure. Neurotoxicol Teratol. 2006;28(4):466-71. PMID: 16814983
78. Ricceri L, Markina N, Valanzano A, Fortuna S, Cometa MF, Meneguz A, et al. Developmental exposure to chlorpyrifos alters reactivity to environmental and social cues in adolescent mice. Toxicol Appl Pharmacol. 2003;191(3):189-201. PMID: 13678652
79. Timofeeva OA, Roegge CS, Seidler FJ, Slotkin TA, Levin ED. Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicol Teratol. 2008;30(1):38-45. PMID: 18096363