Neonatal immune system activation with lipopolysaccharide enhances behavioural sensitization to the dopamine agonist, quinpirole, in adult female but not male rats

Brain, Behavior, and Immunity

Volumn 21, Issue 7, 2007, Pages 935-945

  Tenk, Christine M ^a   Foley, Kelly A ^a   Kavaliers, Martin ^a   Ossenkopp, Klaus Peter ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Dopamine agonist; Drug addiction; Endotoxin; Immune activation; Lipopolysaccharide; Locomotor activity; Neonatal; Quinpirole; Sensitization; Sex differences

Indexed keywords

DOPAMINE 2 RECEPTOR STIMULATING AGENT; DOPAMINE 3 RECEPTOR STIMULATING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; LIPOPOLYSACCHARIDE; QUINPIROLE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG MECHANISM; DRUG SENSITIZATION; FEMALE; IMMUNE SYSTEM; IMMUNOSTIMULATION; LOCOMOTION; LONG EVANS RAT; MALE; NEWBORN; NEWBORN ASSESSMENT; NONHUMAN; POSTNATAL CARE; PRIORITY JOURNAL; RAT; SEX DIFFERENCE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; DOPAMINE AGONISTS; DRUG SYNERGISM; FEMALE; IMMUNE SYSTEM; LIPOPOLYSACCHARIDES; MALE; MOTOR ACTIVITY; QUINPIROLE; RATS; RATS, LONG-EVANS; SEX CHARACTERISTICS; SUBSTANCE-RELATED DISORDERS;

EID: 34548026766     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2007.03.001     Document Type: Article

References (105)

1. Abdulla D., Goralski K.B., and Renton K.W. The regulation of cytochrome P450 2E1 during LPS-induced inflammation in the rat. Toxicol. Appl. Pharmacol. 216 (2006) 1-10
2. Anderson S.M., and Pierce R.C. Cocaine-induced alterations in dopamine receptor signaling: implications for reinforcement and reinstatement. Pharmacol. Ther. 106 (2005) 389-403
3. Ashdown, H., Poole, S., Luheshi, G.N., in press. Interleukin-1 receptor antagonist as a modulator of gender differences in the febrile response to lipopolysaccharide in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol.
4. Bilbo S.D., and Nelson R.J. Sex steroid hormones enhance immune function in male and female Siberian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 (2001) R207-R213
5. Brake W.G., Zhang T.Y., Diorio J., Meaney M.J., and Gratton A. Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur. J. Neurosci. 19 (2004) 1863-1874
6. Breivik T., Stephan M., Brabant G.E., Straub R.H., Pabst R., and von Horsten S. Postnatal lipopolysaccharide-induced illness predisposes to periodontal disease in adulthood. Brain Behav. Immun. 16 (2002) 421-438
7. Crombag H.S., Badiani A., Chan J., Dell'Orco J., Dineen S.P., and Robinson T.E. The ability of environmental context to facilitate psychomotor sensitization to amphetamine can be dissociated from its effect on acute drug responsiveness and on conditioned responding. Neuropsychopharmacology 24 (2001) 680-690
8. Cross-Mellor S.K., Kent W.D., Kavaliers M., and Ossenkopp K.-P. Examining the effects of lipopolysaccharide and cholecystokinin on water ingestion: comparing intake and palatability. Brain Res. 861 (2000) 220-232
9. Daniels W.M., Pietersen C.Y., Carstens M.E., and Stein D.J. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab. Brain Dis. 19 (2004) 3-14
10. Deng X., Stachlewitz R.F., Liguori M.J., Blomme E.A., Waring J.F., Luyendyk J.P., Maddox J.F., Ganey P.E., and Roth R.A. Modest inflammation enhances diclofenac hepatotoxicity in rats: role of neutrophils and bacterial translocation. J. Pharmacol. Exp. Ther. 319 (2006) 1191-1199
11. Dent G.W., Smith M.A., and Levine S. The ontogeny of the neuroendocrine response to endotoxin. Brain Res. Dev. Brain Res. 117 (1999) 21-29
12. Di Paolo T., Bedard P.J., Dupont A., Poyet P., and Labrie F. Effects of estradiol on intact and denervated striatal dopamine receptors and on dopamine levels: a biochemical and behavioral study. Can. J. Physiol. Pharmacol. 60 (1982) 350-357
13. Di Paolo T., Falardeau P., and Morissette M. Striatal D-2 dopamine agonist binding sites fluctuate during the rat estrous cycle. Life Sci. 43 (1988) 665-672
14. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3 (1979) 79-83
15. Dunn A.J., and Swiergiel A.H. The role of cytokines in infection-related behavior. Ann. NY Acad. Sci. 840 (1998) 577-585
16. Eilam D., and Szechtman H. Biphasic effect of D-2 agonist quinpirole on locomotion and movements. Eur. J. Pharmacol. 161 (1989) 151-157
17. Ellis S., Mouihate A., and Pittman Q.J. Early life immune challenge alters innate immune responses to lipopolysaccharide: implications for host defense as adults. FASEB J. 19 (2005) 1519-1521
18. Ellis S., Mouihate A., and Pittman Q.J. Neonatal programming of the rat neuroimmune response: stimulus specific changes elicited by bacterial and viral mimetics. J. Physiol. 571 (2006) 695-701
19. Engeland C.G., Kavaliers M., and Ossenkopp K.-P. Sex differences in the effects of muramyl dipeptide and lipopolysaccharide on locomotor activity and the development of behavioral tolerance in rats. Pharmacol. Biochem. Behav. 74 (2003) 433-447
20. Engeland C.G., Kavaliers M., and Ossenkopp K.-P. The influence of photoperiod and sex on lipopolysaccharide-induced hypoactivity and behavioral tolerance development in meadow voles (Microtus pennsylvanicus). Psychoneuroendocrinology 28 (2003) 970-991
21. Engeland C.G., Kavaliers M., and Ossenkopp K.-P. Influence of the estrous cycle on tolerance development to LPS-induced sickness behaviors in rats. Psychoneuroendocrinology 31 (2006) 510-525
22. Fan L.W., Pang Y., Lin S., Tien L.T., Ma T., Rhodes P.G., and Cai Z. Minocycline reduces lipopolysaccharide-induced neurological dysfunction and brain injury in the neonatal rat. J. Neurosci. Res. 82 (2005) 71-82
23. Foley K.A., Fudge M.A., Kavaliers M., and Ossenkopp K.-P. Quinpirole-induced behavioral sensitization is enhanced by prior scheduled exposure to sucrose: A multi-variable examination of locomotor activity. Behav. Brain Res. 167 (2006) 49-56
24. Fortier M.E., Joober R., Luheshi G.N., and Boksa P. Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring. J. Psychiatr. Res. 38 (2004) 335-345
25. Franklin A.E., Engeland C.G., Kavaliers M., and Ossenkopp K.-P. Lipopolysaccharide-induced hypoactivity and behavioral tolerance development are modulated by the light-dark cycle in male and female rats. Psychopharmacology (Berl) 170 (2003) 399-408
26. Frantz K.J., and Van Hartesveldt C. The locomotor effects of quinpirole in rats depend on age and gender. Pharmacol. Biochem. Behav. 64 (1999) 821-826
27. Gaillard R.C., and Spinedi E. Sex- and stress-steroids interactions and the immune system: evidence for a neuroendocrine-immunological sexual dimorphism. Domest. Anim. Endocrinol. 15 (1998) 345-352
28. Gaykema R.P., Goehler L.E., Tilders F.J., Bol J.G., McGorry M., Fleshner M., Maier S.F., and Watkins L.R. Bacterial endotoxin induces fos immunoreactivity in primary afferent neurons of the vagus nerve. Neuroimmunomodulation 5 (1998) 234-240
29. Giannone P.J., Schanbacher B.L., Bauer J.A., and Reber K.M. Effects of prenatal lipopolysaccharide exposure on epithelial development and function in newborn rat intestine. J. Pediatr. Gastroenterol. Nutr. 43 (2006) 284-290
30. Gordon J.H., and Perry K.O. Pre- and postsynaptic neurochemical alterations following estrogen-induced striatal dopamine hypo- and hypersensitivity. Brain Res. Bull. 10 (1983) 425-428
31. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12 (1988) 123-137
32. Hodgson D.M., Knott B., and Walker F.R. Neonatal endotoxin exposure influences HPA responsivity and impairs tumor immunity in Fischer 344 rats in adulthood. Pediatr. Res. 50 (2001) 750-755
33. Hruska R.E. Elevation of striatal dopamine receptors by estrogen: dose and time studies. J. Neurochem. 47 (1986) 1908-1915
34. Hu X.T., Koeltzow T.E., Cooper D.C., Robertson G.S., White F.J., and Vezina P. Repeated ventral tegmental area amphetamine administration alters dopamine D1 receptor signaling in the nucleus accumbens. Synapse 45 (2002) 159-170
35. Juarez I., Silva-Gomez A.B., Peralta F., and Flores G. Anoxia at birth induced hyperresponsiveness to amphetamine and stress in postpubertal rats. Brain Res. 992 (2003) 281-287
36. Kalitsky-Szirtes J., Shayeganpour A., Brocks D.R., and Piquette-Miller M. Suppression of drug-metabolizing enzymes and efflux transporters in the intestine of endotoxin-treated rats. Drug Metab. Dispos. 32 (2004) 20-27
37. Kalivas P.W. Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res. Brain Res. Rev. 18 (1993) 75-113
38. Kalivas P.W., and Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Brain Res. Rev. 16 (1991) 223-244
39. Kant G.J., Lenox R.H., Bunnell B.N., Mougey E.H., Pennington L.L., and Meyerhoff J.L. Comparison of stress response in male and female rats: pituitary cyclic AMP and plasma prolactin, growth hormone and corticosterone. Psychoneuroendocrinology 8 (1983) 421-428
40. Kehoe P., Shoemaker W.J., Triano L., Callahan M., and Rappolt G. Adult rats stressed as neonates show exaggerated behavioral responses to both pharmacological and environmental challenges. Behav. Neurosci. 112 (1998) 116-125
41. Kikusui T., Faccidomo S., and Miczek K.A. Repeated maternal separation: differences in cocaine-induced behavioral sensitization in adult male and female mice. Psychopharmacology (Berl) 178 (2005) 202-210
42. Kosten T.A., Miserendino M.J., and Kehoe P. Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience. Brain Res. 875 (2000) 44-50
43. Kosten T.A., Sanchez H., Zhang X.Y., and Kehoe P. Neonatal isolation enhances acquisition of cocaine self-administration and food responding in female rats. Behav. Brain Res. 151 (2004) 137-149
44. Kosten T.A., Zhang X.Y., and Kehoe P. Neurochemical and behavioral responses to cocaine in adult male rats with neonatal isolation experience. J. Pharmacol. Exp. Ther. 314 (2005) 661-667
45. Kozlov A.V., Gille L., Miller I., Piskernik C., Haindl S., Staniek K., Nohl H., Bahrami S., Ohlinger W., Gemeiner M., and Redl H. Opposite effects of endotoxin on mitochondrial and endoplasmic reticulum functions. Biochem. Biophys. Res. Commun. 352 (2007) 91-96
46. Kuhn C.M., Pauk J., and Schanberg S.M. Endocrine responses to mother-infant separation in developing rats. Dev. Psychobiol. 23 (1990) 395-410
47. Lahita R.G. Gender and the immune system. J. Gend. Specif. Med. 3 (2000) 19-22
48. Langhans W., Balkowski G., and Savoldelli D. Differential feeding responses to bacterial lipopolysaccharide and muramyl dipeptide. Am. J. Physiol. 261 (1991) R659-R664
49. Lehmann J., Pryce C.R., Bettschen D., and Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 64 (1999) 705-715
50. Levine S., Berkenbosch F., Suchecki D., and Tilders F.J. Pituitary-adrenal and interleukin-6 responses to recombinant interleukin-1 in neonatal rats. Psychoneuroendocrinology 19 (1994) 143-153
51. Li Y., Acerbo M.J., and Robinson T.E. The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur. J. Neurosci. 20 (2004) 1647-1654
52. Li Y., Kolb B., and Robinson T.E. The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen. Neuropsychopharmacology 28 (2003) 1082-1085
53. Li Y., Robinson T.E., and Bhatnagar S. Effects of maternal separation on behavioural sensitization produced by repeated cocaine administration in adulthood. Brain Res. 960 (2003) 42-47
54. Liu D., Caldji C., Sharma S., Plotsky P.M., and Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J. Neuroendocrinol. 12 (2000) 5-12
55. Lomanowska A., Gormley S., and Szechtman H. Presynaptic stimulation and development of locomotor sensitization to the dopamine agonist quinpirole. Pharmacol. Biochem. Behav. 77 (2004) 617-622
56. Lynch W.J. Sex differences in vulnerability to drug self-administration. Exp. Clin. Psychopharmacol. 14 (2006) 34-41
57. Magid J., Bobbin M.D., and Zalcman S. Interleukin-2 enhances the expression of stereotypic behavior associated with dopamine D1 receptor stimulation. ([Abstract]) Abstr. Soc. Neurosci. 31 (2005) 907.8
58. Magid J., Bobbin M.D., and Zalcman S. Behavioral changes induced by a dopamine receptor D2 receptor agonist are augmented by interleukin-2. ([Abstract]) Abstr. Soc. Neurosci. 32 (2006) 384.11
59. Martin J.T. Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur. J. Pharmacol. 405 (2000) 251-261
60. Matthews K., Robbins T.W., Everitt B.J., and Caine S.B. Repeated neonatal maternal separation alters intravenous cocaine self-administration in adult rats. Psychopharmacology (Berl) 141 (1999) 123-134
61. Matthews K., Wilkinson L.S., and Robbins T.W. Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol. Behav. 59 (1996) 99-107
62. McIntosh J., Anisman H., and Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res. Dev. Brain Res. 113 (1999) 97-106
63. Meaney M.J., Brake W., and Gratton A. Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse?. Psychoneuroendocrinology 27 (2002) 127-138
64. Nakano K., Suzuki S., and Oh C. Significance of increased secretion of glucocorticoids in mice and rats injected with bacterial endotoxin. Brain Behav. Immun. 1 (1987) 159-172
65. Ossenkopp K.-P., and Kavaliers M. Measuring spontaneous locomotor activity in small mammals. In: Ossenkopp K.P., Kavaliers M., and Sanberg P. (Eds). Measuring Movement and Locomotion: from Invertebrates to Humans (1996), Landes Company, Georgetown TX 33-59
66. Ossenkopp K.-P., and Mazmanian D.S. The measurement and integration of behavioral variables: aggregation and complexity as important issues. Neurobehav. Toxicol. Teratol. 7 (1985) 95-100
67. Ossenkopp K.-P., Zaki K., and Engeland C.G. Sensitization of locomotor behaviors with repeated quinpirole treatments: a model of compulsive behavior?. ([Abstract]) Abstr. Int. Behav. Neurosci. Soc. 10 (2001) 36
68. Pang Y., Cai Z., and Rhodes P.G. Disturbance of oligodendrocyte development, hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide. Brain Res. Dev. Brain Res. 140 (2003) 205-214
69. Pierce R.C., and Kalivas P.W. Amphetamine produces sensitized increases in locomotion and extracellular dopamine preferentially in the nucleus accumbens shell of rats administered repeated cocaine. J. Pharmacol. Exp. Ther. 275 (1995) 1019-1029
70. Plata-Salaman C.R., and Borkoski J.P. Centrally administered bacterial lipopolysaccharide depresses feeding in rats. Pharmacol. Biochem. Behav. 46 (1993) 787-791
71. Plotsky P.M., and Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 18 (1993) 195-200
72. Raff H., Lee J.J., Widmaier E.P., Oaks M.K., and Engeland W.C. Basal and adrenocorticotropin-stimulated corticosterone in the neonatal rat exposed to hypoxia from birth: modulation by chemical sympathectomy. Endocrinology 145 (2004) 79-86
73. Ramos J.A., Pais J.R., Cebeira M., and Fernandez-Ruiz J. Role of estrogens on striatal dopaminergic activity. J. Steroid Biochem. 27 (1987) 683-689
74. Robinson T.E., and 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. 396 (1986) 157-198
75. Robinson T.E., and Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 18 (1993) 247-291
76. Robinson T.E., and Berridge K.C. The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95 Suppl 2 (2000) S91-S117
77. Robinson T.E., and Kolb B. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J. Neurosci. 17 (1997) 8491-8497
78. Savageau M.M., and Beatty W.W. Gonadectomy and sex differences in the behavioral responses to amphetamine and apomorphine of rats. Pharmacol. Biochem. Behav. 14 (1981) 17-21
79. Schindler C.W., and Carmona G.N. Effects of dopamine agonists and antagonists on locomotor activity in male and female rats. Pharmacol. Biochem. Behav. 72 (2002) 857-863
80. Schuurs A.H., and Verheul H.A. Effects of gender and sex steroids on the immune response. J. Steroid Biochem. 35 (1990) 157-172
81. Shanks N., Larocque S., and Meaney M.J. Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: early illness and later responsivity to stress. J. Neurosci. 15 (1995) 376-384
82. Shanks N., McCormick C.M., and Meaney M.J. Sex differences in hypothalamic-pituitary-adrenal responding to endotoxin challenge in the neonate: reversal by gonadectomy. Brain Res. Dev. Brain Res. 79 (1994) 260-266
83. Shanks N., and Meaney M.J. Hypothalamic-pituitary-adrenal activation following endotoxin administration in the developing rat: a CRH-mediated effect. J. Neuroendocrinol. 6 (1994) 375-383
84. Shanks N., Windle R.J., Perks P.A., Harbuz M.S., Jessop D.S., Ingram C.D., and Lightman S.L. Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation. Proc. Natl. Acad. Sci. USA 97 (2000) 5645-5650
85. Slotten H.A., Kalinichev M., Hagan J.J., Marsden C.A., and Fone K.C. Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res. 1097 (2006) 123-132
86. Sorg B.A., and Steketee J.D. Mechanisms of cocaine-induced sensitization. Prog. Neuropsychopharmacol. Biol. Psychiatry 16 (1992) 1003-1012
87. Spencer S.J., Martin S., Mouihate A., and Pittman Q.J. Early-life immune challenge: Defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology (2006)
88. Stewart J., and Badiani A. Tolerance and sensitization to the behavioral effects of drugs. Behav. Pharmacol. 4 (1993) 289-312
89. Szechtman H., Dai H., Mustafa S., Einat H., and Sullivan R.M. Effects of dose and interdose interval on locomotor sensitization to the dopamine agonist quinpirole. Pharmacol. Biochem. Behav. 48 (1994) 921-928
90. Szechtman H., Talangbayan H., Canaran G., Dai H., and Eilam D. Dynamics of behavioral sensitization induced by the dopamine agonist quinpirole and a proposed central energy control mechanism. Psychopharmacology (Berl) 115 (1994) 95-104
91. Szumlinski K.K., Allan M., Talangbayan H., Tracey A., and Szechtman H. Locomotor sensitization to quinpirole: environment-modulated increase in efficacy and context-dependent increase in potency. Psychopharmacology (Berl) 134 (1997) 193-200
92. Szumlinski K.K., Goodwill A.M., and Szechtman H. Locomotor sensitization to quinpirole in rats: effects of drug abstinence and sex. Psychopharmacology (Berl) 152 (2000) 304-311
93. Tenk C.M., Kavaliers M., and Ossenkopp K.-P. Neonatal exposure to lipopolysaccharide alters anxiety-related behaviors in adult rats: evidence for sex differences. ([Abstract]) Abstr. Soc. Neurosci. 31 (2005) 795.9
94. Tollner B., Roth J., Storr B., Martin D., Voigt K., and Zeisberger E. The role of tumor necrosis factor (TNF) in the febrile and metabolic responses of rats to intraperitoneal injection of a high dose of lipopolysaccharide. Pflugers Arch. 440 (2000) 925-932
95. Walker F.R., Brogan A., Smith R., and Hodgson D.M. A profile of the immediate endocrine, metabolic and behavioural responses following a dual exposure to endotoxin in early life. Physiol. Behav. 83 (2004) 495-504
96. Walker F.R., March J., and Hodgson D.M. Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat. Behav. Brain Res. 154 (2004) 63-69
97. Washburn T.C., Medearis Jr. D.N., and Childs B. Sex differences in susceptibility to infections. Pediatrics 35 (1965) 57-64
98. Wigger A., and Neumann I.D. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 66 (1999) 293-302
99. Wise R.A., and Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol. Rev. 94 (1987) 469-492
100. Yeh S.Y., and Haertzen C.A. Cocaine-induced locomotor activity in rats. Pharmacol. Biochem. Behav. 39 (1991) 723-727
101. Yirmiya R., Rosen H., Donchin O., and Ovadia H. Behavioral effects of lipopolysaccharide in rats: involvement of endogenous opioids. Brain Res. 648 (1994) 80-86
102. Zalcman S., Savina I., and Wise R.A. Interleukin-6 increases sensitivity to the locomotor-stimulating effects of amphetamine in rats. Brain Res. 847 (1999) 276-283
103. Zolfaghari R., Cifelli C.J., Lieu S.O., Chen Q., Li N.Q., and Ross A.C. Lipopolysaccharide opposes the induction of CYP26A1 and CYP26B1 gene expression by retinoic acid in the rat liver in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 292 (2007) G1029-G1036
104. Zuckerman L., Rehavi M., Nachman R., and 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 28 (2003) 1778-1789
105. Zuk M., and McKean K.A. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26 (1996) 1009-1023