Conditioned taste aversion with lipopolysaccharide and peptidoglycan does not activate cytokine gene expression in the spleen and hypothalamus of mice

Brain, Behavior, and Immunity

Volumn 18, Issue 2, 2004, Pages 186-200

  Mormède, Cécile ^a   Palin, Karine ^b   Kelley, Keith W ^c   Castanon, Nathalie ^a   Dantzer, Robert ^a  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Conditioned taste aversion; Cytokine; Innate immunity; Lipopolysaccharide; Macroarray; MAPK; Mouse; NF B; Real time PCR; Taqman

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDOGLYCAN; SACCHARIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE ACTIVATION; HYPOTHALAMUS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPLEEN; TASTE AVERSION;

EID: 0842306091     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0889-1591(03)00133-8     Document Type: Article

References (69)

1. Ader R., Cohen N. Conditioning and immunity. Ader R., Felten D., Cohen N. Psychoneuroimmunology. 2001;3-34 Academic Press, San Diego.
2. Alheim K., Chai Z., Fantuzzi G., Hasanvan H., Malinowsky D., Di Santo E., Ghezzi P., Dinarello C.A., Bartfai T. Hyperresponsive febrile reactions to interleukin (IL) 1alpha and IL-1beta, and altered brain cytokine mRNA and serum cytokine levels, in IL-1beta-deficient mice. Proc. Natl. Acad. Sci. USA. 94:1997;2681-2686.
3. Baltathakis I., Alcantara O., Boldt D.H. Expression of different NF-kappaB pathway genes in dendritic cells (DCs) or macrophages assessed by gene expression profiling. J. Cell. Biochem. 83:2001;281-290.
4. Berman D.E., Hazvi S., Neduva V., Dudai Y. The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: activation of ERK1-2 and formation of a memory trace. J. Neurosci. 20:2000;7017-7023.
5. Berman D.E., Hazvi S., Rosenblum K., Seger R., Dudai Y. Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J. Neurosci. 18:1998;10037-10044.
6. Biberstine K.J., Rosenthal R.S. Peptidoglycan fragments decrease food intake and body weight gain in rats. Infect. Immun. 62:1994;3276-3281.
7. Blalock E.M., Chen K.C., Sharrow K., Herman J.P., Porter N.M., Foster T.C., Landfield P.W. Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J. Neurosci. 23:2003;3807-3819.
8. Bluthé R.M., Michaud B., Poli V., Dantzer R. Role of IL-6 in cytokine-induced sickness behaviour: a study with IL-6 deficient mice. Physiol. Behav. 70:2000;367-373.
9. Brasier A.R., Han Y., Sherman C.T. Transcriptional regulation of angiotensinogen gene expression. Vitam. Horm. 57:1999;217-247.
10. Bull D.F., Brown R., King M.G., Husband A.J. Modulation of body temperature through taste aversion conditioning. Physiol. Behav. 49:1991;1229-1233.
11. Burrell R. Human responses to bacterial endotoxin. Circ. Shock. 43:1994;137-153.
12. Bustin S.A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25:2000;169-193.
13. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature. 410:2001;37-40.
14. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
15. Cohen N., Moynihan J.A., Ader R. Pavlovian conditioning of the immune system. Int. Arch. Allergy Immunol. 105:1994;101-106.
16. Daemen M.A., Heemskerk V.H., van't Veer C., Denecker G., Wolfs T.G., Vandenabeele P., Buurman W.A. Functional protection by acute phase proteins alpha(1)-acid glycoprotein and alpha(1)-antitrypsin against ischemia/ reperfusion injury by preventing apoptosis and inflammation. Circulation. 102:2000;1420-1426.
17. Dantzer R. Cytokine-induced sickness behavior: where do we stand? Brain Behav. Immun. 15:2001;7-24.
18. Dantzer R., Bluthé R., Castanon N., Chauvet N., Capuron L., Goodall G., Kelley K., Konsman J., Layé S., Parnet P., Pousset F. Cytokine effects on behavior. Ader R., Felten D., Cohen N. Psychoneuroimmunology. 3rd ed. 2001;703-727 Academic Press, San Diego.
19. Dziarski R., Jin Y.P., Gupta D. Differential activation of extracellular signal-regulated kinase (ERK) 1, ERK2, p38, and c-Jun NH2-terminal kinase mitogen-activated protein kinases by bacterial peptidoglycan. J. Infect. Dis. 174:1996;777-785.
20. Exton M.S., Bull D.F., King M.G. Behavioral conditioning of lipopolysaccharide-induced anorexia. Physiol. Behav. 57:1995;401-405.
21. Exton M.S., Gierse C., Meier B., Mosen M., Xie Y., Frede S., Goebel M.U., Limmroth V., Schedlowski M. Behaviorally conditioned immunosuppression in the rat is regulated via noradrenaline and beta-adrenoceptors. J. Neuroimmunol. 131:2002;21-30.
22. Exton M.S., von Auer A.K., Buske-Kirschbaum A., Stockhorst U., Gobel U., Schedlowski M. Pavlovian conditioning of immune function: animal investigation and the challenge of human application. Behav. Brain Res. 110:2000;129-141.
23. Exton M.S., von Horsten S., Schult M., Voge J., Strubel T., Donath S., Steinmuller C., Seeliger H., Nagel E., Westermann J., Schedlowski M. Behaviorally conditioned immunosuppression using cyclosporine A: central nervous system reduces IL-2 production via splenic innervation. J. Neuroimmunol. 88:1998;182-191.
24. Fitzsimons J.T. Angiotensin, thirst, and sodium appetite. Physiol. Rev. 78:1998;583-686.
25. Fuseler J.W., Conner E.M., Davis J.M., Wolf R.E., Grisham M.B. Cytokine and nitric oxide production in the acute phase of bacterial cell wall-induced arthritis. Inflammation. 21:1997;113-131.
26. Gatti S., 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. Geschwind D.H., Gregg J.P. Microarrays for the Neurosciences: An Essential Guide. 2002;The MIT press, Cambridge.
28. Goujon E., Parnet P., Aubert A., Goodall G., Dantzer R. Corticosterone regulates behavioral effects of lipopolysaccharide and interleukin-1 beta in mice. Am. J. Physiol. 269:1995;R154-R159.
29. Goujon E., Parnet P., Layé S., Combe C., Dantzer R. Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain of mice in response to lipopolysaccharide. Mol. Brain Res. 36:1996;53-62.
30. Gupta D., Wang Q., Vinson C., Dziarski R. Bacterial peptidoglycan induces CD14-dependent activation of transcription factors CREB/ATF and AP-1. J. Biol. Chem. 274:1999;14012-14020.
31. Hellman J., Roberts J.D. Jr., Tehan M.M., Allaire J.E., Warren H.S. Bacterial peptidoglycan-associated lipoprotein is released into the bloodstream in gram-negative sepsis and causes inflammation and death in mice. J. Biol. Chem. 277:2002;14274-14280.
32. Hiramoto R.N., Ghanta V.K., Rogers C.F., Hiramoto N.S. Conditioning the elevation of body temperature, a host defensive reflex response. Life Sci. 49:1991;93-99.
33. Hochepied T., Van Molle W., Berger F.G., Baumann H., Libert C. Involvement of the acute phase protein alpha 1-acid glycoprotein in nonspecific resistance to a lethal gram-negative infection. J. Biol. Chem. 275:2000;14903-14909.
34. Hochepied T., Wullaert A., Berger F.G., Baumann H., Brouckaert P., Steidler L., Libert C. Overexpression of alpha(1)-acid glycoprotein in transgenic mice leads to sensitisation to acute colitis. Gut. 51:2002;398-404.
35. Hoijer M.A., Melief M.J., Debets R., Hazenberg M.P. Inflammatory properties of peptidoglycan are decreased after degradation by human N-acetylmuramyl-L-alanine amidase. Eur. Cytokine Netw. 8:1997;375-381.
36. Janssens S., Beyaert R. A universal role for MyD88 in TLR/IL-1R-mediated signaling. Trends Biochem. Sci. 27:2002;474-482.
37. Janz L.J., Green-Johnson J., Murray L., Vriend C.Y., Nance D.M., Greenberg A.H., Dyck D.G. Pavlovian conditioning of LPS-induced responses: effects on corticosterone, splenic NE, and IL-2 production. Physiol. Behav. 59:1996;1103-1109.
38. Konsman J.P., Parnet P., Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 25:2002;154-159.
39. Lamprecht R., Hazvi S., Dudai Y. cAMP response element-binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory. J. Neurosci. 17:1997;8443-8450.
40. Layé S., Parnet P., Goujon E., Dantzer R. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Mol. Brain Res. 27:1994;157-162.
41. Liège S., Moze E., Kelley K.W., Parnet P., Neveu P.J. Activation of the hypothalamic-pituitary-adrenal axis in IL-1 beta-converting enzyme-deficient mice. Neuroimmunomodulation. 7:2000;189-194.
42. Matzinger P. The danger model: a renewed sense of self. Science. 296:2002;301-305.
43. Medzhitov R., Preston-Hurlburt P., Janeway C.A. Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 388:1997;394-397.
44. Mengozzi M., Fantuzzi G., Faggioni R., Marchant A., Goldman M., Orencole S., Clark B.D., Sironi M., Benigni F., Ghezzi P. Chlorpromazine specifically inhibits peripheral and brain TNF production, and up-regulates IL-10 production, in mice. Immunology. 82:1994;207-210.
45. Minami M., Kuraishi Y., Yamaguchi T., Nakai S., Hirai Y., Satoh M. Immobilization stress induces interleukin-1 beta mRNA in the rat hypothalamus. Neurosci. Lett. 123:1991;254-256.
46. Miyahara S., Komori T., Fujiwara R., Shizuya K., Yamamoto M., Ohmori M., Okazaki Y. Effects of repeated stress on expression of interleukin-6 (IL-6) and IL-6 receptor mRNAs in rat hypothalamus and midbrain. Life Sci. 66:2000;L93-98.
47. Mormede C., Castanon N., Medina C., Dantzer R. Conditioned place aversion with interleukin-1beta in mice is not associated with activation of the cytokine network. Brain, Behav. Immun. 17:2003;110-120.
48. Murphy B.E. Some studies of the protein-binding of steroids and their application to the routine micro and ultramicro measurement of various steroids in body fluids by competitive protein-binding radioassay. J. Clin. Endocrinol. Metab. 27:1967;973-990.
49. Nguyen K.T., Deak T., Owens S.M., Kohno T., Fleshner M., Watkins L.R., Maier S.F. Exposure to acute stress induces brain interleukin-1beta protein in the rat. J. Neurosci. 18:1998;2239-2246.
50. O'Neill L.A., Dinarello C.A. The IL-1 receptor/toll-like receptor superfamily: crucial receptors for inflammation and host defense. Immunol. Today. 21:2000;206-209.
51. Reichhart J.M., Imler J.L. Toll story. médecine/sciences. 16:2000;1439-1442.
52. Reilly S. The parabrachial nucleus and conditioned taste aversion. Brain Res. Bull. 48:1999;239-254.
53. Rivier C., Chizzonite R., Vale W. In the mouse, the activation of the hypothalamic-pituitary-adrenal axis by a lipopolysaccharide (endotoxin) is mediated through interleukin-1. Endocrinology. 125:1989;2800-2805.
54. Selcher J.C., Weeber E.J., Varga A.W., Sweatt J.D., Swank M. Protein kinase signal transduction cascades in mammalian associative conditioning. Neuroscientist. 8:2002;122-131.
55. Simpson C.S., Morris B.J. Regulation of neuronal cell adhesion molecule expression by NF-kappa B. J. Biol. Chem. 275:2000;16879-16884.
56. Smotherman W.P., Hennessy J.W., Levine S. Plasma corticosterone levels during recovery from LiCl produced taste aversions. Behav. Biol. 16:1976;401-412.
57. Solvason H.B., Ghanta V.K., Lorden J.F., Soong S.J., Hiramoto R.N. A behavioral augmentation of natural immunity: odor specificity supports a Pavlovian conditioning model. Int. J. Neurosci. 61:1991;277-288.
58. Solvason H.B., Ghanta V.K., Soong S.J., Rogers C.F., Hsueh C.M., Hiramoto N.S., Hiramoto R.N. A simple, single, trial-learning paradigm for conditioned increase in natural killer cell activity. Proc. Soc. Exp. Biol. Med. 199:1992;199-203.
59. Swank M.W. Pharmacological antagonism of tyrosine kinases and MAP kinase in brainstem blocks taste aversion learning in mice. Physiol. Behav. 69:2000;499-503.
60. Swank M.W. Phosphorylation of MAP kinase and CREB in mouse cortex and amygdala during taste aversion learning. Neuroreport. 11:2000;1625-1630.
61. Swank M.W., Sweatt J.D. Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. J. Neurosci. 21:2001;3383-3391.
62. Takano M., Yokoyama K., Yayama K., Itoh N., Okamoto H. Endotoxin-induced enhancement of angiotensinogen synthesis in the liver: decreased response following repeated endotoxin exposure. Biol. Pharm. Bull. 16:1993;917-920.
63. Takeuchi O., Akira S. Toll-like receptors; their physiological role and signal transduction system. Int. Immunopharmacol. 1:2001;625-635.
64. Terao A., Apte-Deshpande A., Dousman L., Morairty S., Eynon B.P., Kilduff T.S., Freund Y.R. Immune response gene expression increases in the aging murine hippocampus. J. Neuroimmunol. 132:2002;99-112.
65. Wang Q., Dziarski R., Kirschning C.J., Muzio M., Gupta D. Micrococci and peptidoglycan activate TLR2. → MyD88 → IRAK → TRAF → NIK → IKK → NF-kappaB signal transduction pathway that induces transcription of interleukin-8 Infect. Immun. 69:2001;2270-2276.
66. Wang Z.M., Liu C., Dziarski R. Chemokines are the main proinflammatory mediators in human monocytes activated by Staphylococcus aureus, peptidoglycan, and endotoxin. J. Biol. Chem. 275:2000;20260-20267.
67. Xu Z., Dziarski R., Wang Q., Swartz K., Sakamoto K.M., Gupta D. Bacterial peptidoglycan-induced tnf-alpha transcription is mediated through the transcription factors Egr-1, Elk-1, and NF-kappaB. J. Immunol. 167:2001;6975-6982.
68. Yamamoto T., Shimura T., Sako N., Yasoshima Y., Sakai N. Neural substrates for conditioned taste aversion in the rat. Behav. Brain Res. 65:1994;123-137.
69. Yang H., Wang L., Huang C.S., Ju G. Plasticity of GAP-43 innervation of the spleen during immune response in the mouse. Evidence for axonal sprouting and redistribution of the nerve fibers. Neuroimmunomodulation. 5:1998;53-60.