Sexually dimorphic effects of neonatal immune system activation with lipopolysaccharide on the behavioural response to a homotypic adult immune challenge

International Journal of Developmental Neuroscience

Volumn 26, Issue 3-4, 2008, Pages 331-338

  Tenk, Christine M ^a   Kavaliers, Martin ^a   Ossenkopp, Klaus Peter ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Endotoxin; Hypoactivity; Immune activation; Lipopolysaccharide; Locomotor activity; Neonatal; Open field; Sex differences; Sickness behaviour

Indexed keywords

LIPOPOLYSACCHARIDE; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNE SYSTEM; LOCOMOTION; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SEX DIFFERENCE;

AGING; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BODY WEIGHT; EXPLORATORY BEHAVIOR; FEMALE; GRAM-NEGATIVE BACTERIAL INFECTIONS; IMMUNE SYSTEM; IMMUNITY, ACTIVE; LIPOPOLYSACCHARIDES; MALE; MOTOR ACTIVITY; RATS; RATS, LONG-EVANS; SEX CHARACTERISTICS; WEIGHT LOSS;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; RATTUS;

EID: 41649119925     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2008.01.001     Document Type: Article

References (85)

1. Anisman H., Merali Z., and Hayley S. Sensitization associated with stressors and cytokine treatments. Brain Behav. Immun. 17 (2003) 86-93
2. Ashdown H., Poole S., Boksa P., and Luheshi G.N. 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. 292 (2007) R1667-R1674
3. Avitsur R., Pollak Y., and Yirmiya R. Different receptor mechanisms mediate the effects of endotoxin and interleukin-1 on female sexual behavior. Brain Res. 773 (1997) 149-161
4. Banasikowski T.J., Kavaliers M., and Ossenkopp K.-P. Repeated exposure of male mice to lipopolysaccharide: development of behavioral tolerance in an automated light-dark apparatus. Abstr. -Soc. Neurosci. 31 (2005) 202.6 (Abstract)
5. Becu-Villalobos D., Gonzalez I.A., Diaz-Torga G., Hockl P., and Libertun C. Brain sexual differentiation and gonadotropins secretion in the rat. Cell Mol. Neurobiol. 17 (1997) 699-715
6. 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
7. Boisse L., Mouihate A., Ellis S., and Pittman Q.J. Long-term alterations in neuroimmune responses after neonatal exposure to lipopolysaccharide. J. Neurosci. 24 (2004) 4928-4934
8. Boisse L., Spencer S.J., Mouihate A., Vergnolle N., and Pittman Q.J. Neonatal immune challenge alters nociception in the adult rat. Pain 119 (2005) 133-141
9. Boisse L., Van Sickle M.D., Sharkey K.A., and Pittman Q.J. Compromised neuroimmune status in rats with experimental colitis. J. Physiol. 548 (2003) 929-939
10. 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
11. 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
12. Dantzer R. Cytokine-induced sickness behavior: where do we stand?. Brain Behav. Immun. 15 (2001) 7-24
13. 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
14. Dunn A.J., and Swiergiel A.H. The role of cytokines in infection-related behavior. Ann. NY Acad. Sci. 840 (1998) 577-585
15. 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
16. 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
17. 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
18. 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
19. 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
20. Engeland C.G., Nielsen D.V., Kavaliers M., and Ossenkopp K.-P. Locomotor activity changes following lipopolysaccharide treatment in mice: a multivariate assessment of behavioral tolerance. Physiol. Behav. 72 (2001) 481-491
21. Fahmi H., Ancuta P., Perrier S., and Chaby R. Preexposure of mouse peritoneal macrophages to lipopolysaccharide and other stimuli enhances the nitric oxide response to secondary stimuli. Inflamm. Res. 45 (1996) 347-353
22. Franklin A.E., Engeland C.G., Kavaliers M., and Ossenkopp K.-P. The rate of behavioral tolerance development to repeated lipopolysaccharide treatments depends upon the time of injection during the light-dark cycle: a multivariable examination of locomotor activity. Behav. Brain Res. 180 (2007) 161-173
23. 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 (Berlin) 170 (2003) 399-408
24. Friedman D., Netti F., and Schreiber A.D. Effect of estradiol and steroid analogues on the clearance of immunoglobulin G-coated erythrocytes. J. Clin. Invest. 75 (1985) 162-167
25. 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
26. Gatti S., and Bartfai T. Induction of tumor necrosis factor-alpha mRNA in the brain after peripheral endotoxin treatment: comparison with interleukin-1 family and interleukin-6. Brain Res. 624 (1993) 291-294
27. 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
28. Giglio T., Imro M.A., Filaci G., Scudeletti M., Puppo F., De Cecco L., Indiveri F., and Costantini S. Immune cell circulating subsets are affected by gonadal function. Life Sci. 54 (1994) 1305-1312
29. Grinevich V., Ma X.M., Herman J.P., Jezova D., Akmayev I., and Aguilera G. Effect of repeated lipopolysaccharide administration on tissue cytokine expression and hypothalamic-pituitary-adrenal axis activity in rats. J. Neuroendocrinol. 13 (2001) 711-723
30. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12 (1988) 123-137
31. Hayley S., Brebner K., Lacosta S., Merali Z., and Anisman H. Sensitization to the effects of tumor necrosis factor-alpha: neuroendocrine, central monoamine, and behavioral variations. J. Neurosci. 19 (1999) 5654-5665
32. Hayley S., Lacosta S., Merali Z., van Rooijen N., and Anisman H. Central monoamine and plasma corticosterone changes induced by a bacterial endotox: sensitisation cross-sensitization effects. Eur. J. Neurosci. 13 (2001) 1155-1165
33. Hayley S., Wall P., and Anisman H. Sensitization to the neuroendocrine, central monoamine and behavioural effects of murine tumor necrosis factor-alpha: peripheral and central mechanisms. Eur. J. Neurosci. 15 (2002) 1061-1076
34. Hodgson D.M., and Knott B. Potentiation of tumor metastasis in adulthood by neonatal endotoxin exposure: sex differences. Psychoneuroendocrinology 27 (2002) 791-804
35. 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
36. Inaba K., Suzuki S., Ihara H., Sakaguchi T., Baba S., Urano T., Konno H., and Nakamura S. Sexual dimorphism in endotoxin susceptibility after partial hepatectomy in rats. J. Hepatol. 42 (2005) 719-727
37. Johnson R.W., Propes M.J., and Shavit Y. Corticosterone modulates behavioral and metabolic effects of lipopolysaccharide. Am. J. Physiol. 270 (1996) R192-R198
38. Konsman J.P., Parnet P., and Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 25 (2002) 154-159
39. Kozak W., Conn C.A., and Kluger M.J. Lipopolysaccharide induces fever and depresses locomotor activity in unrestrained mice. Am. J. Physiol. 266 (1994) R125-R135
40. Kozak W., Zheng H., Conn C.A., Soszynski D., van der Ploeg L.H., and Kluger M.J. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1 beta-deficient mice. Am. J. Physiol. 269 (1995) R969-R977
41. Lacosta S., Merali Z., and Anisman H. Behavioral and neurochemical consequences of lipopolysaccharide in mice: anxiogenic-like effects. Brain Res. 818 (1999) 291-303
42. Lahita R.G. Gender and the immune system. J. Gend. Specif. Med. 3 (2000) 19-22
43. Langhans W., Balkowski G., and Savoldelli D. Differential feeding responses to bacterial lipopolysaccharide and muramyl dipeptide. Am. J. Physiol. 261 (1991) R659-R664
44. Laye S., Parnet P., Goujon E., and Dantzer R. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Brain Res. Mol. Brain Res. 27 (1994) 157-162
45. Levine S. Regulation of the hypothalamic-pituitary-adrenal axis in the neonatal rat: the role of maternal behavior. Neurotox. Res. 4 (2002) 557-564
46. Martin J.T. Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur. J. Pharmacol. 405 (2000) 251-261
47. Mead L.A., Hargeaves E.L., and Galea L.A. Sex differences in rodent spontaneous activity levels. In: Sanberg P., Ossenkopp K.-P., and Kavaliers M. (Eds). Motor Activity and Movement Disorders (1996), Humana Press, Totowa, NJ pp. 111-139
48. Meaney M.J., Aitken D.H., and Sapolsky R.M. Thyroid hormones influence the development of hippocampal glucocorticoid receptors in the rat: a mechanism for the effects of postnatal handling on the development of the adrenocortical stress response. Neuroendocrinology 45 (1987) 278-283
49. Murakami N., and Ono T. Sex-related differences in fever development of rats. Am. J. Physiol. 252 (1987) R284-R289
50. 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
51. Olsen N.J., Gu X., and Kovacs W.J. Bone marrow stromal cells mediate androgenic suppression of B lymphocyte development. J. Clin. Invest. 108 (2001) 1697-1704
52. Olsen N.J., and Kovacs W.J. Effects of androgens on T and B lymphocyte development. Immunol. Res. 23 (2001) 281-288
53. Opp M.R., and Toth L.A. Somnogenic and pyrogenic effects of interleukin-1beta and lipopolysaccharide in intact and vagotomized rats. Life Sci. 62 (1998) 923-936
54. Ossenkopp K.-P., Macrae L.K., and Teskey G.C. Automated multivariate measurement of spontaneous motor activity in mice: time course and reliabilities of the behavioral measures. Pharmacol. Biochem. Behav. 27 (1987) 565-568
55. 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
56. 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
57. Ozanne S.E., and Hales C.N. Early programming of glucose-insulin metabolism. Trends Endocrinol. Metab. 13 (2002) 368-373
58. Packard G.C., and Boardman T.J. The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort?. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 122 (1999) 37-44
59. Pezeshki G., Pohl T., and Schobitz B. Corticosterone controls interleukin-1 beta expression and sickness behavior in the rat. J. Neuroendocrinol. 8 (1996) 129-135
60. Pierpaoli W. Integrated phylogenetic and ontogenic evolution of neuroendocrine and identity-defense, immune functions. In: Ader R., and Cohen N. (Eds). Psychoneuroimmunology (1981), Academic Press, San Diego 575-607
61. Plata-Salaman C.R., and Borkoski J.P. Centrally administered bacterial lipopolysaccharide depresses feeding in rats. Pharmacol. Biochem. Behav. 46 (1993) 787-791
62. Roden A.C., Moser M.T., Tri S.D., Mercader M., Kuntz S.M., Dong H., Hurwitz A.A., McKean D.J., Celis E., Leibovich B.C., Allison J.P., and Kwon E.D. Augmentation of T cell levels and responses induced by androgen deprivation. J. Immunol. 173 (2004) 6098-6108
63. Schmidt E.D., Janszen A.W., Wouterlood F.G., and Tilders F.J. Interleukin-1-induced long-lasting changes in hypothalamic corticotropin-releasing hormone (CRH)-neurons and hyperresponsiveness of the hypothalamus-pituitary-adrenal axis. J. Neurosci. 15 (1995) 7417-7426
64. Schuurs A.H., and Verheul H.A. Effects of gender and sex steroids on the immune response. J. Steroid Biochem. 35 (1990) 157-172
65. 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
66. 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
67. 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
68. 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. U.S.A. 97 (2000) 5645-5650
69. Spencer S.J., Heida J.G., and Pittman Q.J. Early life immune challenge-effects on behavioural indices of adult rat fear and anxiety. Behav. Brain Res. 164 (2005) 231-238
70. 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 31 (2006) 1910-1918
71. Spinedi E., Gaillard R.C., and Chisari A. Sexual dimorphism of neuroendocrine-immune interactions. Front. Horm. Res. 29 (2002) 91-107
72. Swiergiel A.H., and Dunn A.J. Effects of interleukin-1beta and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests. Pharmacol. Biochem. Behav. 86 (2007) 651-659
73. Takemura T., Makino S., Takao T., Asaba K., Suemaru S., and Hashimoto K. Hypothalamic-pituitary-adrenocortical responses to single vs. repeated endotoxin lipopolysaccharide administration in the rat. Brain Res. 767 (1997) 181-191
74. 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
75. van Dam A.M., Brouns M., Louisse S., and Berkenbosch F. Appearance of interleukin-1 in macrophages and in ramified microglia in the brain of endotoxin-treated rats: a pathway for the induction of non-specific symptoms of sickness?. Brain Res. 588 (1992) 291-296
76. Viselli S.M., Reese K.R., Fan J., Kovacs W.J., and Olsen N.J. Androgens alter B cell development in normal male mice. Cell Immunol. 182 (1997) 99-104
77. 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
78. Walker F.R., Hodyl N.A., Krivanek K.M., and Hodgson D.M. Early life host-bacteria relations and development: long-term individual differences in neuroimmune function following neonatal endotoxin challenge. Physiol. Behav. 87 (2006) 126-134
79. 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
80. Washburn T.C., Medearis Jr. D.N., and Childs B. Sex differences in susceptibility to infections. Pediatrics 35 (1965) 57-64
81. West M.A., Bennet T., Seatter S.C., Clair L., and Bellingham J. LPS pretreatment reprograms macrophage LPS-stimulated TNF and IL-1 release without protein tyrosine kinase activation. J. Leukoc. Biol. 61 (1997) 88-95
82. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res. 711 (1996) 163-174
83. 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
84. Zuckerman S.H., Ahmari S.E., Bryan-Poole N., Evans G.F., Short L., and Glasebrook A.L. Estriol: a potent regulator of TNF and IL-6 expression in a murine model of endotoxemia. Inflammation 20 (1996) 581-597
85. Zuk M., and McKean K.A. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26 (1996) 1009-1023