Effects of prenatal immune activation on amphetamine-induced addictive behaviors: Contributions from animal models

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 63, Issue , 2015, Pages 63-69

  Borçoi, Aline R ^a   Patti, Camilla L ^a   Zanin, Karina A ^a   Hollais, André W ^a   Santos Baldaia, Renan ^a   Ceccon, Liliane M B ^a   Berro, Laís F ^a   Wuo Silva, Raphael ^a   Grapiglia, Stephanie B ^a   Ribeiro, Luciana T C ^a   Lopes Silva, Leonardo B ^a   Frussa Filho, Roberto ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Addiction; Amphetamine; Mice; Poly(I:C); Schizophrenia

Indexed keywords

AMPHETAMINE; COCAINE; POLYINOSINIC POLYCYTIDYLIC ACID;

ADDICTION; ADULT; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIORAL SENSITIZATION; CONDITIONING; CONTROLLED STUDY; DOPAMINERGIC TRANSMISSION; ENVIRONMENTAL EXPOSURE; FEMALE; HABITUATION; IMMUNE RESPONSE; INNATE IMMUNITY; LOCOMOTION; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PLACE PREFERENCE; PRENATAL PERIOD; SCHIZOPHRENIA; SENSITIZATION; STEREOTYPY; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG ABUSE; DRUG EFFECTS; ETIOLOGY; EXPLORATORY BEHAVIOR; IMMUNOLOGY; MOTOR ACTIVITY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; TIME;

AMPHETAMINE-RELATED DISORDERS; ANIMALS; COCAINE; CONDITIONING (PSYCHOLOGY); DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; MALE; MICE; MOTOR ACTIVITY; POLY I-C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STEREOTYPED BEHAVIOR; TIME FACTORS;

EID: 84935857639     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2015.05.015     Document Type: Article

References (68)

1. Akaneya Y., Takahashi M., Hatanaka H. Interleukin-1 beta enhances survival and interleukin-6 protects against MPP+ neurotoxicity in cultures of fetal rat dopaminergic neurons. Exp Neurol 1995, 136:44-52.
2. Alcaro A., Huber R., Pankseep J. Behavioral functions of the mesolimbic dopaminergic system: an affective neuroethological perspective. Brain Res Rev 2007, 56:283-321.
3. Bardo M.T., Bervins R.A. Conditioned place preference: what does it add to our preclinical understanding of drug reward?. Psychopharmacology (Berl) 2000, 153:31-43.
4. Bellack A.S., Bennett M.E., Gearon J.S., Brown C.H., Yang M.S. A randomized clinical trial of a new behavioral treatment for drug abuse in people with severe and persistent mental illness. Arch Gen Psychiatry 2006, 63:426-432.
5. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Rev 1998, 28:309-369.
6. Berro L.F., Hollais A.W., Patti C.L., Fukushiro D.F., Mári-Kawamoto E., Talhati F., et al. Sleep deprivation impairs the extinction of cocaine-induced environmental conditioning in mice. Pharmacol Biochem Behav 2014, 124:13-18.
7. Betts K.S., Williams G.M., Najman J.M., Scott J., Alati R. Maternal prenatal infection, early susceptibility to illness and adult psychotic experiences: a birth cohort study. Schizophr Res 2014, 156:161-167.
8. Blanchard J.J., Brown S.A., Horan W.P., Sherwood A.R. Substance use disorders in schizophrenia: review, integration, and a proposed model. Clin Psychol Rev 2000, 20:207-234.
9. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 2010, 24:881-897.
10. Bonate P.T., Swann A., Silverman P.B. Context-dependent cross-sensitization between cocaine and amphetamine. Life Sci 1997, 60:PL1-PL7.
11. Brown A.S., Derkits E.J. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 2010, 167:261-280.
12. Buka S.L., Tsuang M.T., Torrey E.F., Klebanoff M.A., Wagner R.L., Yolken R.H. Maternal cytokine levels during pregnancy and adult psychosis. Brain Behav Immun 2001, 15:411-420.
13. Canales J.J., Graybiel A.M. A measure of striatal function predicts motor stereotypy. Nat Neurosci 2000, 3:377-383.
14. Canetta S.E., Brown A.S. Prenatal infection, maternal immune activation and risk for schizophrenia. Transl Neurosci 2012, 3:320-327.
15. Carvalho R.C., Fukushiro D.F., Helfer D.C., Callegaro-Filho D., Trombin T.F., Zanlorenci L.H.F., et al. Long-term haloperidol treatment (but not risperidone) enhances addiction-related behaviors in mice: role of dopamine D2 receptors. Addict Biol 2009, 14:283-293.
16. Carvey P.M., Ling Z.D., Sortwell C.E., Pitzer M.R., McGuire S.O., Storch A., et al. A clonal line of mesencephalic progenitor cells converted to dopamine neurons by hematopoietic cytokines: a source of cells for transplantation in Parkinson's disease. Exp Neurol 2001, 171:98-108.
17. Chinen C.C., Faria R.R., Frussa-Filho R. Characterization of the rapid-onset type of behavioral sensitization to amphetamine in mice: role of drug-environment conditioning. Neuropsychopharmacology 2006, 31:151-159.
18. Costa F.G., Frussa-Filho R., Canteras N.S., Valera A.G., Felicio L.F. Blockade of neurotensin receptors during amphetamine discontinuation indicates individual variability. Neuropeptides 2007, 41:83-91.
19. Fortier M.E., Kent S., Ashdown H., Poole S., Boksa P., Luheshi G.N. The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism. Am J Physiol 2004, 287:R759-R766.
20. Fukushiro D.F., Alvarez J., do N., Tatsu J.A., Castro J.P., Chinen C.C., et al. Haloperidol (but not ziprasidone) withdrawal enhances cocaine-induced locomotor activation and conditioned place preference in mice. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:867-872.
21. Fukushiro D.F., Carvalho R.C., Ricardo V.P., Alvarez J., do N., Ribeiro L.T.C., et al. Haloperidol (but not ziprasidone) withdrawal potentiates sensitization to the hyperlocomotor effect of cocaine in mice. Brain Res Bull 2008, 77:124-128.
22. Gilmore J.H., Jarskog L.F., Vadlamudi S., Lauder J.M. Prenatal infection and risk for schizophrenia: IL-1b, IL-6, and TNFa inhibit cortical neuron dendrite development. Neuropsychopharmacology 2004, 29:1221-1229.
23. Gilmore J.H., Jarskog L.F., Vadlamudi S. Maternal poly I:C exposure during pregnancy regulates TNF alpha, BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. J Neuroimmunol 2005, 159:106-112.
24. Green A.I. Schizophrenia and comorbid substance use disorder: effects of antipsychotics. J Clin Psychiatry 2005, 66:21-26.
25. Gregg L., Barrowclough C., Haddock G. Reasons for increased substance use in psychosis. Clin Psychol Rev 2007, 27:494-510.
26. Ibi D., Nagai T., Kitahara Y., Mizoguchi H., Koike H., Shiraki A., et al. Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood. Neurosci Res 2009, 64:297-305.
27. Insel T.R. Rethinking esquizofrenia. Nature 2010, 468:187-193.
28. Jones C.A., Watson D.J.G., Fone K.C.F. Animal models of schizophrenia. Br J Pharmacol 2011, 164:1162-1194.
29. Kalivas P.W. Neurocircuitry of addiction. Neuropsychopharmacology, the fifth generation of progress 2002, 1357-1366. Lippincott Williams & Wilkins, Philadelphia.
30. Kalivas P.W., O'brien C. Drug addiction as a pathology of staged neuroplasticity. Neuropsychopharmacol 2008, 33:166-180.
31. Koob G.F. Neural mechanisms of drug reinforcement. Ann N Y Acad Sci 1992, 54:171-191.
32. Kosten T.R., Ziedonis D.M. Substance abuse and schizophrenia: editors' introduction. Schizophr Bull 1997, 23:181-186.
33. Ling Z.D., Potter E.D., Lipton J.W., Carvey P.M. Differentiation of mesencephalic progenitor cells into dopaminergic neurons by cytokines. Exp Neurol 1998, 149:411-423.
34. Marinho E.A.V., Oliveira-Lima A.J., Wuo-Silva R., Santos R., Baldaia M.A., Hollais A.W., et al. Selective action of an atypical neuroleptic on the mechanisms related to the development of cocaine addiction: a pre-clinical behavioural study. Int J Neuropsychopharmacol 2014, 17:613-623.
35. Meyer U., Feldon J., Schedlowski M., Yee B.K. Towards an immunoprecipitated neurodevelopmental animal model of schizophrenia. Neurosci Biobehav Rev 2005, 29:913-947.
36. Meyer U., Schwendener S., Feldon J., Yee B.K. Prenatal and postnatal maternal contributions in the infection model of schizophrenia. Exp Brain Res 2006, 173:243-257.
37. Meyer U., Nyffeler M., Engler A., Urwyler A., Schedlowski M., Knuesel I., et al. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 2006, 26:4752-4762.
38. Meyer U., Yee B.K., Feldon J. The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse?. Neuroscientist 2007, 13:241-256.
39. Meyer U., Murray P.J., Urwyler A., Yee B.K., Schedlowski M., Feldon J. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated antiinflammatory signaling. Mol Psychiatry 2008, 13:208-221.
40. Meyer U., Nyffeler M., Yee B.K., Knuesel I., Feldon J. Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 2008, 22:469-486.
41. Meyer U., Engler A., Weber L., Schedlowski M., Feldon J. Preliminary evidence for a modulation of fetal dopaminergic development by maternal immune activation during pregnancy. Neuroscience 2008, 154:701-709.
42. Meyer U., Feldon J., Fatemi S.H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci Biobehav Rev 2009, 33:1061-1079.
43. Moy S.S., Riddick N.V., Nikolova V.D., Teng B.L., Agster K.L., Nonneman R.J., et al. Repetitive behavior profile and supersensitivity to amphetamine in the C58/J mouse model of autism. Behav Brain Res 2014, 259:200-214.
44. Nagai T., Ibi D., Yamada K. Animal model for schizophrenia that reflects gene-environment interactions. Translational research in neurodevelopmental disorders: development of etiology-based animal models. Biol Pharm Bull 2011, 34:1364-1368.
45. Ozawa K., Kenji H., Takashi K., Eiji S., Hiroshi I., Masaomi I. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol Psychiatry 2006, 59:546-554.
46. Pettersen H., Ruud T., Ravndal E., Landheim A. Walking the fine line: self-reported reasons for substance use in persons with severe mental illness. Int J Qual Stud Health Well-being 2013, 8:21968.
47. Piontkewitz M.A., Arad M., Weiner I. Risperidone administered during asymptomatic period of adolescence prevents the emergence of brain structural pathology and behavioral abnormalities in an animal model of schizophrenia. Schizophr Bull 2011, 37:1257-1269.
48. Potter E.D., Ling Z.D., Carvey P.M. Cytokine-induced conversion of mesencephalic-derived progenitor cells into dopamine neurons. Cell Tissue Res 1999, 296:235-246.
49. Rapoport J.L., Addington A.M., Frangou S., Psych M.R. The neurodevelopmental model of schizophrenia: update. Mol Psychiatry 2005, 10:434-449.
50. Richtand N.M., Ahlbrand R., Hom P.S., Chambers B., Davis J., Benoit S. Effects of prenatal immune activation and peri-adolescent stress on amphetamine-induced conditioned place preference in the rat. Psychopharmacology (Berl) 2012, 222:313-324.
51. Robinson T.E., Becker J.B. Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res 1986, 396:157-198.
52. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 1993, 18:247-291.
53. Robinson T.E., Berridge K.C. Incentive-sensitization and addiction. Addiction 2001, 96:103-114.
54. Robinson T.E., Berridge K.C. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci 2008, 363:3137-3146.
55. Romero E., Guaza C., Castellano B., Borrell J. Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia. Mol Psychiatry 2010, 15:372-383.
56. Saito L.P., Fukushiro D.F., Hollais A.W., Mári-Kawamoto E., Costa J.M., Berro L.F., et al. Acute total sleep deprivation potentiates amphetamine-induced locomotor-stimulant effects and behavioral sensitization in mice. Pharmacol Biochem Behav 2014, 117:7-16.
57. Saka E., Goodrich C., Harlan P., Madras B.K., Graybiel A.M. Repetitive behaviors in monkeys are linked to specific striatal activation patterns. J Neurosci 2004, 24:7557-7565.
58. Sanchis-Segura C., Spanagel R. Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict Biol 2006, 11:2-38.
59. Setler P., Sarau H., Mckenzie G. Differential attenuation of some effects of haloperidol in rats given scopolamine. Eur J Pharmacol 1976, 39:117-126.
60. Van Os J., Kenis G., Rutten B.P.F. The environment and schizophrenia. Nature 2010, 468:203-212.
61. Vezina P. Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci Biobehav Rev 2004, 27:827-839.
62. Vorhees C.V., Graham D.L., Braun A.A., Schaefer T.L., Skelton M.R., Richtand N.M., et al. Prenatal immune challenge in rats: altered responses to dopaminergic and glutamatergic agents, prepulse inhibition of acoustic startle, and reduced route-based learning as a function of maternal body weight gain after prenatal exposure to poly IC. Synapse 2012, 66:725-737.
63. Vorhees C.V., Graham D.L., Braun A.A., Schaefer T.L., Skelton M.R., Richtand N.M., et al. Prenatal immune challenge in rats: effects of polyinosinic-polycytidylic acid on spatial learning, prepulse inhibition, conditioned fear, and responses to MK-801 and amphetamine. Neurotoxicol Teratol 2015, 47:54-65.
64. Wise R.A., Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol Rev 1987, 94:469-492.
65. Wuo-Silva R., Fukushiro D.F., Borçoi A.R., Fernandes H.A., Procópio-Souza R., Hollais A.W., et al. Addictive potential of modafinil and cross-sensitization with cocaine: a pre-clinical study. Addict Biol 2011, 16:565-579.
66. Zager A., Mennecier G., Palermo-Neto J. Maternal immune activation in late gestation enhances locomotor response to acute but not chronic amphetamine treatment in male mice offspring: role of the D1 receptor. Behav Brain Res 2012, 232:30-36.
67. Zuckerman L., Weiner I. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J Psychiatr Res 2005, 39:311-323.
68. Zuckerman L., Rehavi M., Nachman R., Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 2003, 28:1778-1789.