Postnatal programming of the innate immune response

Integrative and Comparative Biology

Volumn 49, Issue 3, 2009, Pages 237-245

  Galic, Michael A ^a   Spencer, Sarah J ^a   Mouihate, Abdeslam ^a,b   Pittman, Quentin J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b KUWAIT UNIVERSITY   (Kuwait)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 76149124224     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icp025     Document Type: Article

References (87)

1. Akhtar M, Cheng Y, Magno RM, Ashktorab H, Smoot DT, Meltzer SJ, Wilson KT. 2001. Promoter methylation regulates Helicobacter pylori-stimulated cyclooxygenase-2 expression in gastric epithelial cells. Cancer Res 61: 2399-2403
2. Arancibia SA, Beltran CJ, Aguirre IM, Silva P, Peralta AL, Malinarich F, Hermoso MA. 2007. Toll-like receptors are key participants in innate immune responses. Biol Res 40:97-112.
3. Avishai-Eliner S, Brunson KL, Sandman CA, Baram TZ. 2002. Stressed-out, or in (utero)? Trends Neurosci 25:518-524
4. Beishuizen A, Thijs LG. 2003. Endotoxin and the hypothalamo-pituitary- adrenal (HPA) axis. J Endotoxin Res 9:3-24.
5. Beutler B. 2004. Inferences, questions and possibilities in toll-like receptor signalling. Nature 430:257-263
6. Bilbo SD, Biedenkapp JC, Der-Avakian A, Watkins LR, Rudy JW, Maier SF. 2005a. Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci 25:8000-8009
7. Bilbo SD, Levkoff LH, Mahoney JH, Watkins LR, Rudy JW, Maier SF. 2005b. Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav Neurosci 119:293-301.
8. Bilbo SD, Rudy JW, Watkins LR, Maier SF. 2006. A behavioural characterization of neonatal infectionfacilitated memory impairment in adult rats. Behav Brain Res 169:39-47.
9. Blatteis CM. 2003. Fever: pathological or physiological, injurious or beneficial? J Therm Biol 28:1-13.
10. Blatteis CM. 2007. The onset of fever: new insights into its mechanism. Prog Brain Res 162:3-14.
11. Blatteis CM, Li S, Li Z, Perlik V, Feleder C. 2004. Signaling the brain in systemic inflammation: The role of complement. Front Biosci 9:915-931
12. Blatteis CM, Sehic E, Li S. 2000. Pyrogen sensing and signaling: old views and new concepts. Clin Infect Dis 31(Suppl 5):S168-77.
13. Boisse L, Mouihate A, Ellis S, Pittman QJ. 2004. Long-term alterations in neuroimmune responses after neonatal exposure to lipopolysaccharide. J Neurosci 24:4928-4934
14. Boisse L, Spencer SJ, Mouihate A, Vergnolle N, Pittman QJ. 2005. Neonatal immune challenge alters nociception in the adult rat. Pain 119:133-141
15. Brake WG, Zhang TY, Diorio J, Meaney MJ, Gratton A. 2004. Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur J Neurosci 19:1863-1874
16. Breivik T, Stephan M, Brabant GE, Straub RH, Pabst R, von Horsten S. 2002. Postnatal lipopolysaccharide-induced illness predisposes to periodontal disease in adulthood. Brain Behav Immun 16:421-438
17. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ. 1998. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335-5340
18. Carlsen KH, Lodrup Carlsen KC. 2005. Parental smoking and childhood asthma: clinical implications. Treat Respir Med 4:337-346
19. Cartmell T, Ball C, Bristow AF, Mitchell D, Poole S. 2003. Endogenous interleukin-10 is required for the defervescence of fever evoked by local lipopolysaccharide-induced and Staphylococcus aureus-induced inflammation in rats. J Physiol 549:653-664
20. Cartmell T, Luheshi GN, Hopkins SJ, Rothwell NJ, Poole S. 2001. Role of endogenous interleukin-1 receptor antagonist in regulating fever induced by localised inflammation in the rat. J Physiol 531:171-180
21. Champagne F, Meaney MJ. 2001. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133: 287-302.
22. Conti B, Tabarean I, Andrei C, Bartfai T. 2004. Cytokines and fever. Front Biosci 9:1433-1449
23. Daniels WM, Pietersen CY, Carstens ME, Stein DJ. 2004. 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 19:3-14.
24. Dantzer R, Kelley KW. 2007. Twenty years of research on cytokine-induced sickness behavior. Brain Behav Immun 21:153-160
25. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. 2008. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46-56.
26. Dunn AJ. 2006. Effects of cytokines and infections on brain neurochemistry. Clin Neurosci Res 6:52-68.
27. Ellis S, Mouihate A, Pittman QJ. 2005. Early life immune challenge alters innate immune responses to lipopolysaccharide: implications for host defense as adults. FASEB J 19:1519-1521
28. Ellis S, Mouihate A, Pittman QJ. 2006. Neonatal programming of the rat neuroimmune response: stimulus specific changes elicited by bacterial and viral mimetics. J Physiol 571:695-701.
29. Francis D, Diorio J, Liu D, Meaney MJ. 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155-1158
30. Galic MA, Riazi K, Heida JG, Mouihate A, Fournier NM, Spencer SJ, Kalynchuk LE, Teskey GC, Pittman QJ. 2008. Postnatal inflammation increases seizure susceptibility in adult rats. J Neurosci 28:6904-6913
31. Gilmer WS, McKinney WT. 2003. Early experience and depressive disorders: human and non-human primate studies. J Affect Disord 75:97-113.
32. Gottlieb A, Keydar I, Epstein HT. 1977. Rodent brain growth stages: an analytical review. Biol Neonate 32:166-176
33. Harre EM, Galic MA, Mouihate A, Noorbakhsh F, Pittman QJ. 2008. Neonatal inflammation produces selective behavioural deficits and alters N-methyl-D-aspartate receptor subunit mRNA in the adult rat brain. Eur J Neurosci 27:644-653
34. Hart BL. 1988. Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12:123-137
35. Heida JG, Boisse L, Pittman QJ. 2004. Lipopolysaccharideinduced febrile convulsions in the rat: short-term sequelae. Epilepsia 45:1317-1329
36. Heim C, Nemeroff CB. 2001. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023-1039
37. Hodgson DM, Knott B. 2002. Potentiation of tumor metastasis in adulthood by neonatal endotoxin exposure: sex differences. Psychoneuroendocrinology 27:791-804.
38. Hodgson DM, Knott B, Walker FR. 2001. Neonatal endotoxin exposure influences HPA responsivity and impairs tumor immunity in Fischer 344 rats in adulthood. Pediatr Res 50:750-755
39. Hodyl NA, Krivanek KM, Lawrence E, Clifton VL, Hodgson DM. 2007. Prenatal exposure to a pro-inflammatory stimulus causes delays in the development of the innate immune response to LPS in the offspring. J Neuroimmunol 190:61-71.
40. Hood KE, Dreschel NA, Granger DA. 2003. Maternal behavior changes after immune challenge of neonates with developmental effects on adult social behavior. Dev Psychobiol 42:17-34.
41. Jiang Q, Cross AS, Singh IS, Chen TT, Viscardi RM, Hasday JD. 2000. Febrile core temperature is essential for optimal host defense in bacterial peritonitis. Infect Immun 68:1265-1270
42. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG. 2002. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 73:131-140
43. Kent S, Bluthe RM, Dantzer R, Hardwick AJ, Kelley KW, Rothwell NJ, Vannice JL. 1992. Different receptor mechanisms mediate the pyrogenic and behavioral effects of interleukin 1. Proc Natl Acad Sci USA 89:9117-9120
44. Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D. 1998. Role of fever in disease. Ann N Y Acad Sci 856:224-233
45. Konsman JP, Parnet P, Dantzer R. 2002. Cytokine-induced sickness behaviour: Mechanisms and implications. Trends Neurosci 25:154-159
46. Laye S, Parnet P, Goujon E, Dantzer R. 1994. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Brain Res Mol Brain Res 27:157-162
47. Lazarus M, Yoshida K, Coppari R, Bass CE, Mochizuki T, Lowell BB, Saper CB. 2007. EP3 prostaglandin receptors in the median preoptic nucleus are critical for fever responses. Nat Neurosci 10:1131-1133
48. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ. 2000. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3:799-806.
49. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. 1997. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659-1662
50. Luheshi G, Miller AJ, Brouwer S, Dascombe MJ, Rothwell NJ, Hopkins SJ. 1996. Interleukin-1 receptor antagonist inhibits endotoxin fever and systemic interleukin-6 induction in the rat. Am J Physiol 270:E91-5.
51. Marin MT, Planeta CS. 2004. Maternal separation affects cocaine-induced locomotion and response to novelty in adolescent, but not in adult rats. Brain Res 1013:83-90.
52. Matsumura K, Kobayashi S. 2004. Signaling the brain in inflammation: The role of endothelial cells. Front Biosci 9:2819-2826
53. McEwen BS. 2003. Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 9:149-154
54. Meaney MJ. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161-1192
55. Meaney MJ, Szyf M. 2005a. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci 7:103-123
56. Meaney MJ, Szyf M. 2005b. Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci 28:456-463
57. Meaney MJ, Szyf M, Seckl JR. 2007. Epigenetic mechanisms of perinatal programming of hypothalamicpituitary- adrenal function and health. Trends Mol Med 13:269-277
58. Morrison SF, Nakamura K, Madden CJ. 2008. Central control of thermogenesis in mammals. Exp Physiol 93: 773-797
59. Nadeau S, Rivest S. 2001. The complement system is an integrated part of the natural innate immune response in the brain. FASEB J 15:1410-1412
60. O'Connor JC, Lawson MA, Andre C, Moreau M, Lestage J, Castanon N, Kelley KW, Dantzer R. 2009. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry 14:511-522
61. Pittman QJ, Cooper KE, Veale WL, Van Petten GR. 1973. Fever in newborn lambs. Can J Physiol Pharmacol 51:868-872
62. Pittman QJ, Cooper KE, Veale WL, Van Petten GR. 1974. Observations on the development of the febrile response to pyrogens in sheep. Clin Sci Mol Med 46:591-602.
63. Rakyan VK, Preis J, Morgan HD, Whitelaw E. 2001. The marks, mechanisms and memory of epigenetic states in mammals. Biochem J 356:1-10.
64. Rivest S. 2001. How circulating cytokines trigger the neural circuits that control the hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 26:761-788
65. Roberts NJ Jr. 1991. Impact of temperature elevation on immunologic defenses. Rev Infect Dis 13:462-472
66. Schafers M, Sorkin L. 2008. Effect of cytokines on neuronal excitability. Neurosci Lett 437:188-193
67. Shanks N, Larocque S, Meaney MJ. 1995. Neonatal endotoxin exposure alters the development of the hypothalamicpituitary- adrenal axis: early illness and later responsivity to stress. J Neurosci 15:376-384
68. Shanks N, Windle RJ, Perks PA, Harbuz MS, Jessop DS, Ingram CD, Lightman SL. 2000. Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation. Proc Natl Acad Sci USA 97:5645-5650
69. Spencer SJ, Auer RN, Pittman QJ. 2006a. Rat neonatal immune challenge alters adult responses to cerebral ischaemia. J Cereb Blood Flow Metab 26:456-467
70. Spencer SJ, Boisse L, Mouihate A, Pittman QJ. 2006b. Long term alterations in neuroimmune responses of female rats after neonatal exposure to lipopolysaccharide. Brain Behav Immun 20:325-330
71. Spencer SJ, Heida JG, Pittman QJ. 2005. Early life immune challenge-effects on behavioural indices of adult rat fear and anxiety. Behav Brain Res 164:231-238
72. Spencer SJ, Hyland NP, Sharkey KA, Pittman QJ. 2007a. Neonatal immune challenge exacerbates experimental colitis in adult rats: potential role for TNF-alpha. Am J Physiol Regul Integr Comp Physiol 292:R308-15.
73. Spencer SJ, Martin S, Mouihate A, Pittman QJ. 2006c. Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology 31:1910-8.
74. Spencer SJ, Mouihate A, Galic MA, Ellis SL, Pittman QJ. 2007b. Neonatal immune challenge does not affect body weight regulation in rats. Am J Physiol Regul Integr Comp Physiol 293:R581-89.
75. Spencer SJ, Mouihate A, Galic MA, Pittman QJ. 2008. Central and peripheral neuroimmune responses: hyporesponsiveness during pregnancy. J Physiol 586:399-406.
76. Spencer SJ, Mouihate A, Pittman QJ. 2007c. Peripheral inflammation exacerbates damage after global ischemia independently of temperature and acute brain inflammation. Stroke 38:1570-1577
77. Spencer SJ, Tilbrook A. 2009. Neonatal overfeeding alters adult anxiety and stress responsiveness. Psychoneuroendocrinology.
78. Thibeault I, Laflamme N, Rivest S. 2001. Regulation of the gene encoding the monocyte chemoattractant protein 1 (MCP-1) in the mouse and rat brain in response to circulating LPS and proinflammatory cytokines. J Comp Neurol 434:461-477
79. Thornhill J, Asselin J. 1998. Increased neural damage to global hemispheric hypoxic ischemia (GHHI) in febrile but not nonfebrile lipopolysaccharide Escherichia coli injected rats. Can J Physiol Pharmacol 76:1008-1016
80. Turrin NP, Rivest S. 2004. Unraveling the molecular details involved in the intimate link between the immune and neuroendocrine systems. Exp Biol Med (Maywood) 229: 996-1006.
81. Walker FR, Brogan A, Smith R, Hodgson DM. 2004. A profile of the immediate endocrine, metabolic and behavioural responses following a dual exposure to endotoxin in early life. Physiol Behav 83:495-504.
82. Walker FR, Hodyl NA, Hodgson DM. 2009. Neonatal bacterial endotoxin challenge interacts with stress in the adult male rat to modify KLH specific antibody production but not KLH stimulated ex vivo cytokine release. J Neuroimmunol 207:57-65.
83. Walker FR, Hodyl NA, Krivanek KM, Hodgson DM. 2006. Early life host-bacteria relations and development: long-term individual differences in neuroimmune function following neonatal endotoxin challenge. Physiol Behav 87:126-134
84. Wang Y, McCusker C. 2006. Neonatal exposure with LPS and/or allergen prevents experimental allergic airways disease: development of tolerance using environmental antigens. J Allergy Clin Immunol 118:143-151
85. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR., Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854
86. Zampetaki A, Xiao Q, Zeng L, Hu Y, Xu Q. 2006. TLR4 expression in mouse embryonic stem cells and in stem cell-derived vascular cells is regulated by epigenetic modifications. Biochem Biophys Res Commun 347:89-99.
87. Zhang TY, Bagot R, Parent C, Nesbitt C, Bredy TW, Caldji C, Fish E, Anisman H, Szyf M, Meaney MJ. 2006. Maternal programming of defensive responses through sustained effects on gene expression. Biol Psychol 73:72-89.