Single early prenatal lipopolysaccharide exposure impairs striatal monoamines and maternal care in female rats

Life Sciences

Volumn 92, Issue 14-16, 2013, Pages 852-858

  Soto, Ana M S ^a   Kirsten, Thiago B ^b   Reis Silva, Thiago M ^b   Martins, Maria F M ^a   Teodorov, Elisabeth ^c   Flório, Jorge C ^b   Palermo Neto, João ^b   Bernardi, Maria M ^a,b   Bondan, Eduardo F ^a  

^a PAULISTA UNIVERSITY   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSIDADE FEDERAL DO ABC   (Brazil)

Author keywords

Dopamine Maternal aggressive behavior Maternal immune activation Neuroinflammation Nucleus accumbens Serotonin Trans generational effects

Indexed keywords

DOPAMINE; LIPOPOLYSACCHARIDE; MONOAMINE; SEROTONIN;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BACTERIAL INFECTION; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; FEMALE; GESTATIONAL AGE; LACTATION; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MATING; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEUS ACCUMBENS; OPEN FIELD BEHAVIOR; PRENATAL EXPOSURE; PROGENY; PROTEIN EXPRESSION; RAT;

ANIMALS; BACTERIAL INFECTIONS; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; FEMALE; HYPOTHALAMUS; LIPOPOLYSACCHARIDES; MALE; MATERNAL BEHAVIOR; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEROTONIN;

BACTERIA (MICROORGANISMS); RATTUS;

EID: 84876169902     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2013.03.003     Document Type: Article

References (60)

1. D. Agrati, A. Fernandez-Guasti, M. Ferreno, and A. Ferreira Coexpression of sexual behavior and maternal aggression: the ambivalence of sexually active mother rats toward male intruders Behav Neurosci 125 3 2011 446 451
2. A.A. Agrawal, C. Laforsch, and R. Tollrian Transgenerational induction of defences in animals and plants Nature 401 1999 60 63
3. H. Ashdown, Y. Dumont, M. Ng, S. Poole, P. Boksa, and G.N. Luheshi The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia Mol Psychiatry 11 1 2006 47 55
4. A. Aubert Sickness and behaviour in animals: a motivational perspective Neurosci Biobehav Rev 23 7 1999 1029 1036
5. A. Aubert, G. Goodall, R. Dantzer, and G. Gheusi Differential effects of lipopolysaccharide on pup retrieving and nest building in lactating mice Brain Behav Immun 11 2 1997 107 118
6. R. Avitsur, Y. Pollak, and R. Yirmiya Different receptor mechanisms mediate the effects of endotoxin and interleukin-1 on female sexual behavior Brain Res 773 1-2 1997 149 161
7. M.M. Bernardi, T.B. Kirsten, S.M. Matsuoka, E. Teodorov, S.F. Habr, and S.H. Penteado Prenatal lipopolysaccharide exposure affects maternal behavior and male offspring sexual behavior in adulthood Neuroimmunomodulation 17 1 2010 47 55
8. A. Bjorklung, and E. Lindvall Dopamine-containing systems in the CNS A. Bjorklund, T. Hokfelt, Handbook of chemical neuroanatomy Classical transmitters in the CNS, part I vol. 2 1984 Elsevier Amsterdam 55 111
9. P. Boksa Effects of prenatal infection on brain development and behavior: a review of findings from animal models Brain Behav Immun 24 6 2010 881 897
10. E.F. Bondan, M.A. Lallo, M.L. Dagli, M. Sanchez, and D.L. Graca Investigation into the astrocytic immunoreactivity to GFAP and vimentin in the brainstem of Wistar rats submitted to the ethidium bromide gliotoxic model Arq Neuropsiquiatr 61 3A 2003 642 649
11. W.G. Brake, M.B. Noel, P. Boksa, and A. Gratton Influence of perinatal factors on the nucleus accumbens dopamine response to repeated stress during adulthood: an electrochemical study in the rat Neuroscience 77 4 1997 1067 1076
12. P.L. Broadhurst Experiments in psychogenetics: applications of biometrical genetics to the inheritance of behaviour H.J. Eysenck, Experiments in personality 1960 Routledge & Kegan Paul London 1 256
13. Z. Cai, Z.L. Pan, Y. Pang, O.B. Evans, and P.G. Rhodes Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration Pediatr Res 47 1 2000 64 72
14. R. Causon Validation of chromatographic methods in biomedical analysis. Viewpoint and discussion J Chromatogr B Biomed Sci Appl 689 1 1997 175 180
15. O. Curno, J.M. Behnke, A.G. McElligott, T. Reader, and C.J. Barnard Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy Proc Biol Sci 276 1659 2009 1047 1054
16. M.A. Elovitz, A.G. Brown, K. Breen, L. Anton, M. Maubert, and I. Burd Intrauterine inflammation, insufficient to induce parturition, still evokes fetal and neonatal brain injury Int J Dev Neurosci 29 6 2011 663 671
17. L.F. Felicio, J.C. Florio, L.H. Sider, P.E. Cruz-Casallas, and R.S. Bridges Reproductive experience increases striatal and hypothalamic dopamine levels in pregnant rats Brain Res Bull 40 4 1996 253 256
18. O. Gaffori, and M. Le Moal Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmentum lesions Physiol Behav 23 2 1979 317 323
19. D.A. Gayle, R. Beloosesky, M. Desai, F. Amidi, S.E. Nunez, and M.G. Ross Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain Am J Physiol Regul Integr Comp Physiol 286 6 2004 R1024 R1029
20. C.A. Ghiani, N.S. Mattan, H. Nobuta, J.S. Malvar, J. Boles, and M.G. Ross Early effects of lipopolysaccharide-induced inflammation on foetal brain development in rat ASN Neuro 3 4 2011
21. A.L. Giordano, A.E. Johnson, and J.S. Rosenblatt Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats Physiol Behav 48 1 1990 211 214
22. H.M. Golan, V. Lev, M. Hallak, Y. Sorokin, and M. Huleihel Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy Neuropharmacology 48 6 2005 903 917
23. V.E. Grimm, and B. Frieder Differential vulnerability of male and female rats to the timing of various perinatal insults Int J Neurosci 27 3-4 1985 155 164
24. J.L. Grindstaff, D. Hasselquist, J.K. Nilsson, M. Sandell, H.G. Smith, and M. Stjernman Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity Proc Biol Sci 273 1600 2006 2551 2557
25. S. Hansen Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit Physiol Behav 55 4 1994 615 620
26. S. Ikemoto Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex Brain Res Rev 56 1 2007 27 78
27. S.E. Keer, and J.M. Stern Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats Physiol Behav 67 5 1999 659 669
28. T.B. Kirsten, M. Taricano, J.C. Florio, J. Palermo-Neto, and M.M. Bernardi Prenatal lipopolysaccharide reduces motor activity after an immune challenge in adult male offspring Behav Brain Res 211 1 2010 77 82
29. T.B. Kirsten, M. Taricano, P.C. Maiorka, J. Palermo-Neto, and M.M. Bernardi Prenatal lipopolysaccharide reduces social behavior in male offspring Neuroimmunomodulation 17 4 2010 240 251
30. T.B. Kirsten, G.P. Chaves, M. Taricano, D.O. Martins, J.C. Florio, and L.R. Britto Prenatal LPS exposure reduces olfactory perception in neonatal and adult rats Physiol Behav 104 3 2011 417 422
31. T.B. Kirsten, G.P. Chaves-Kirsten, L.M. Chaible, A.C. Silva, D.O. Martins, and L.R. Britto Hypoactivity of the central dopaminergic system and autistic-like behavior induced by a single early prenatal exposure to lipopolysaccharide J Neurosci Res 90 10 2012 1903 1912
32. S.J. Larson, and A.J. Dunn Behavioral effects of cytokines Brain Behav Immun 15 4 2001 371 387
33. A. Lee, M. Li, J. Watchus, and A.S. Fleming Neuroanatomical basis of maternal memory in postpartum rats: selective role for the nucleus accumbens Behav Neurosci 113 3 1999 523 538
34. Y.C. Liu, B.D. Sachs, and J.D. Salamone Sexual behavior in male rats after radiofrequency or dopamine-depleting lesions in nucleus accumbens Pharmacol Biochem Behav 60 2 1998 585 592
35. D. Maestripieri, S.G. Lindell, and J.D. Higley Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms Dev Psychobiol 49 2 2007 165 171
36. U. Meyer, M. Nyffeler, A. Engler, A. Urwyler, M. Schedlowski, and I. Knuesel The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology J Neurosci 26 18 2006 4752 4762
37. U. Meyer, B.K. Yee, and J. Feldon The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse? Neuroscientist 13 3 2007 241 256
38. U. Meyer, J. Feldon, and S.H. Fatemi In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders Neurosci Biobehav Rev 33 7 2009 1061 1079
39. M. Numan Motivational systems and the neural circuitry of maternal behavior in the rat Dev Psychobiol 49 1 2007 12 21
40. M. Numan, and D.S. Stolzenberg Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats Front Neuroendocrinol 30 1 2009 46 64
41. Y. Pang, B. Zheng, L.R. Campbell, L.W. Fan, Z. Cai, and P.G. Rhodes IGF-1 can either protect against or increase LPS-induced damage in the developing rat brain Pediatr Res 67 6 2010 579 584
42. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates 4 ed. 1998 Academic Press San Diego
43. C.A. Pedersen, S.V. Vadlamudi, M.L. Boccia, and J.A. Amico Maternal behavior deficits in nulliparous oxytocin knockout mice Genes Brain Behav 5 3 2006 274 281
44. M. Pereira, and J.I. Morrell Functional mapping of the neural circuitry of rat maternal motivation: effects of site-specific transient neural inactivation J Neuroendocrinol 23 11 2011 1020 1035
45. D.L. Robinson, D.L. Zitzman, and S.K. Williams Mesolimbic dopamine transients in motivated behaviors: focus on maternal behavior Front Psychiatry 2 2011 23
46. H. Rosengarten, and A.J. Friedhoff Enduring changes in dopamine receptor cells of pups from drug administration to pregnant and nursing rats Science 203 4385 1979 1133 1135
47. W. Saltzman, and D. Maestripieri The neuroendocrinology of primate maternal behavior Prog Neuropsychopharmacol Biol Psychiatry 35 5 2011 1192 1204
48. J. Saluk-Juszczak, and B. Wachowicz The proinflammatory activity of lipopolysaccharide Postepy Biochem 51 3 2005 280 287
49. A.M. Samuelsson, E. Jennische, H.A. Hansson, and A. Holmang Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning Am J Physiol Regul Integr Comp Physiol 290 5 2006 R1345 R1356
50. L. Shi, S.H. Fatemi, R.W. Sidwell, and P.H. Patterson Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring J Neurosci 23 1 2003 297 302
51. S.J. Spencer, A. Mouihate, M.A. Galic, S.L. Ellis, and Q.J. Pittman Neonatal immune challenge does not affect body weight regulation in rats Am J Physiol Regul Integr Comp Physiol 293 2 2007 R581 R589
52. J.M. Stern Multisensory regulation of maternal behavior and masculine sexual behavior: a revised view Neurosci Biobehav Rev 14 2 1990 183 200
53. J.M. Stern, and J.S. Lonstein Neural mediation of nursing and related maternal behaviors Prog Brain Res 133 2001 263 278
54. J.M. Stern, and M. Protomastro Effects of low dosages of apomorphine on maternal responsiveness in lactating rats Pharmacol Biochem Behav 66 2 2000 353 359
55. D.S. Stolzenberg, K.Y. Zhang, K. Luskin, L. Ranker, J. Bress, and M. Numan Dopamine D(1) receptor activation of adenylyl cyclase, not phospholipase C, in the nucleus accumbens promotes maternal behavior onset in rats Horm Behav 57 1 2010 96 104
56. B. Svare, C. Betteridge, D. Katz, and O. Samuels Some situational and experiential determinants of maternal aggression in mice Physiol Behav 26 2 1981 253 258
57. A. Urakubo, L.F. Jarskog, J.A. Lieberman, and J.H. Gilmore Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain Schizophr Res 47 1 2001 27 36
58. X. Wang, C.I. Rousset, H. Hagberg, and C. Mallard Lipopolysaccharide- induced inflammation and perinatal brain injury Semin Fetal Neonatal Med 11 5 2006 343 353
59. Z.M. Weil, S.L. Bowers, E.R. Dow, and R.J. Nelson Maternal aggression persists following lipopolysaccharide-induced activation of the immune system Physiol Behav 87 4 2006 694 699
60. C. Zhao, and M. Li Neuroanatomical substrates of the disruptive effect of olanzapine on rat maternal behavior as revealed by c-Fos immunoreactivity Pharmacol Biochem Behav 103 2 2012 174 180