Intra-amygdala microinfusion of IL-6 impairs the auditory fear conditioning of rats via JAK/STAT activation

Behavioural Brain Research

Volumn 275, Issue , 2014, Pages 88-95

  Hao, Yongxin ^a   Jing, He ^a   Bi, Qiang ^a   Zhang, Jiaozhen ^a   Qin, Ling ^a   Yang, Pingting ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Auditory; Behavioral; Cognitive dysfunction; Cytokine; Fear memory

Indexed keywords

INTERLEUKIN 6; STAT3 PROTEIN; CUCURBITACIN I; ENZYME INHIBITOR; STAT PROTEIN; TRITERPENE;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY FEAR CONDITIONING; BEHAVIOR CHANGE; BODY TEMPERATURE; BRAIN REGION; CONDITIONING; FEAR; FREEZING; HABITUATION; IMMUNOREACTIVITY; LEARNING DISORDER; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; ADVERSE EFFECTS; ANALYSIS OF VARIANCE; ANIMAL; AUDITORY STIMULATION; CATALEPSY; CHEMICALLY INDUCED; CONDITIONED REFLEX; DOSE RESPONSE; DRUG ADMINISTRATION; DRUG EFFECTS; LEARNING DISORDERS; METABOLISM; MICROINJECTION; PHOSPHORYLATION; PHYSIOLOGY; REINFORCEMENT; TIME;

ACOUSTIC STIMULATION; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING, CLASSICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; ENZYME INHIBITORS; EXTINCTION, PSYCHOLOGICAL; FEAR; FREEZING REACTION, CATALEPTIC; INTERLEUKIN-6; LEARNING DISORDERS; MICROINJECTIONS; PHOSPHORYLATION; RATS; STAT TRANSCRIPTION FACTORS; TIME FACTORS; TRITERPENES;

EID: 84907164685     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.08.052     Document Type: Article

References (50)

1. Hirano T., Yasukawa K., Harada H., Taga T., Watanabe Y., Matsuda T., et al. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 1998, 324:73-76.
2. Kishimoto T. Interleukin-6: from basic science to medicine-40 years in immunology. Annu Rev Immunol 2005, 23:1-21.
3. Kishimoto T. IL-6: from its discovery to clinical applications. Int Immunol 2010, 22:347-352.
4. Erta M., Quintana A., Hidalgo J. Interleukin-6, a major cytokine in the central nervous system. Int J Biol Sci 2012, 8:1254-1266.
5. Scho¨bitz B., de Kloet E.R., Sutanto W., Holsboer F. Cellular localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. Eur J Neurosci 1993, 5:1426-1435.
6. Vallie`res L., Rivest S. Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1beta. J Neurochem 1997, 69:1668-1683.
7. Anisman H., Merali Z. Cytokines, stress, and depressive illness. Brain Behav Immun 2002, 16:513-524.
8. Gao Y., Ng Y.K., Lin J.Y., Ling E.A. Expression of immunoregulatory cytokines in neurons of the lateral hypothalamic area and amygdaloid nuclear complex of rats immunized against human IgG. Brain Res 2000, 859:364-368.
9. Lehtima¨ki K.A., Peltola J., Koskikallio E., Kera¨nen T., Honkaniemi J. Expression of cytokines and cytokine receptors in the rat brain after kainic acid-induced seizures. Brain Res Mol Brain Res 2003, 110:253-260.
10. Scho¨bitz B., De Kloet E.R., Holsboer F. Gene expression and function of interleukin 1, interleukin 6 and tumor necrosis factor in the brain. Prog Neurobiol 1994, 44:397-432.
11. Song C., Merali Z., Anisman H. Variations of nucleus accumbens dopamine and serotonin following systemic interleukin-1, interleukin-2 or interleukin-6 treatment. Neuroscience 1999, 88:823-836.
12. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., et al. A meta-analysis of cytokines in major depression. Biol Psychiatry 2010, 67:446-457.
13. Kim Y.-K., Na K.-S., Shin K.-H., Jung H.-Y., Choi S.-H., Kim J.-B. Cytokine imbalance in the pathophysiology of major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:1044-1053.
14. Grassi-Oliveira R., Bauer M.E., Pezzi J.C., Teixeira A.L., Brietzke E. Interleukin-6 and verbal memory in recurrent major depressive disorder. Neuro Endocrinol Lett 2011, 32:540-544.
15. Rizzo S.J.S., Neal S.J., Hughes Z.A., Beyna M., Moss S.J., Brandon N.J., et al. Evidence for sustained elevation of IL-6 in the CNS as a key contributor of depressive-like phenotypes. Transl Psychiatry 2012, 2:e199.
16. Ye S.M., Johnson R.W. Increased interleukin-6 expression by microglia from brain of aged mice. J Neuroimmunol 1999, 93:139-148.
17. Tha K.K., Okuma Y., Miyazaki H., Murayama T., Uehara T., Hatakeyama R., et al. Changes in expressions of proinflammatory cytokines IL-1beta, TNF-alpha and IL-6 in the brain of senescence accelerated mouse (SAM) P8. Brain Res 2000, 885:25-31.
18. Braida D., Sacerdote P., Panerai A.E., Bianchi M., Aloisi A.M., Iosue` S., et al. Cognitive function in young and adult IL (interleukin)-6 deficient mice. Behav Brain Res 2004, 153:423-429.
19. Balschun D., Wetzel W., Del Rey A., Pitossi F., Schneider H., Zuschratter W., et al. Interleukin-6: a cytokine to forget. FASEB J 2004, 18:1788-1790.
20. Oitzl M.S., van Oers H., Scho¨bitz B., de Kloet E.R. Interleukin-1 beta, but not interleukin-6, impairs spatial navigation learning. Brain Res 1993, 613:160-163.
21. Bianchi M., Ferrario P., Clavenna A., Panerai A.E. Interleukin-6 affects scopolamine-induced amnesia, but not brain amino acid levels in mice. Neuroreport 1997, 8:1775-1778.
22. Brennan F.X., Beck K.D., Servatius R.J. Proinflammatory cytokines differentially affect leverpress avoidance acquisition in rats. Behav Brain Res 2004, 153:351-355.
23. Marsland A.L., Petersen K.L., Sathanoori R., Muldoon M.F., Neumann S.A., Ryan C., et al. Interleukin-6 covaries inversely with cognitive performance among middle-aged community volunteers. Psychosom Med 2006, 68:895-903.
24. Elwan O., Madkour O., Elwan F., Mostafa M., Abbas Helmy A., Abdel-Naseer M., et al. Brain aging in normal Egyptians: cognition, education, personality, genetic and immunological study. J Neurol Sci 2003, 211:15-22.
25. Dik M.G., Jonker C., Hack C.E., Smit J.H., Comijs H.C., Eikelenboom P. Serum inflammatory proteins and cognitive decline in older persons. Neurology 2005, 64:1371-1377.
26. Baune B.T., Ponath G., Golledge J., Varga G., Arolt V., Rothermundt M., et al. Association between IL-8 cytokine and cognitive performance in an elderly general population-the MEMO-Study. Neurobiol Aging 2008, 29:937-944.
27. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 2001, 24:897-931.
28. Kim J.J., Jung M.W. Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 2006, 30:188-202.
29. Pare´ D. Mechanisms of Pavlovian fear conditioning: has the engram been located?. Trends Neurosci 2002, 25:436-437. discussion 437-8.
30. Burton M.D., Johnson R.W. Interleukin-6 trans-signaling in the senescent mouse brain is involved in infection-related deficits in contextual fear conditioning. Brain Behav Immun 2012, 26:732-738.
31. D'Arcangelo G., Tancredi V., Onofri F., D'Antuono M., Giovedi` S., Benfenati F. Interleukin-6 inhibits neurotransmitter release and the spread of excitation in the rat cerebral cortex. Eur J Neurosci 2000, 12:1241-1252.
32. Sun J., Blaskovich M.A., Jove R., Livingston S.K., Coppola D., Sebti S.M. Cucurbitacin Q: a selective STAT3 activation inhibitor with potent antitumor activity. Oncogene 2005, 24:3236-3245.
33. Donegan J.J., Girotti M., Weinberg M.S., Morilak D.A. A novel role for brain interleukin-6: facilitation of cognitive flexibility in rat orbitofrontal cortex. J Neurosci 2014, 34:953-962.
34. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, New York.
35. Blanchard R.J., Blanchard D.C. Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 1969, 68:129-135.
36. Pare´ D., Quirk G.J., Ledoux J.E. New vistas on amygdala networks in conditioned fear. J Neurophysiol 2004, 92:1-9.
37. Nicolas C.S., Amici M., Bortolotto Z.A., Doherty A., Csaba Z., Fafouri A., et al. The role of JAK-STAT signaling within the CNS. JAK-STAT 2013, 2:e22925.
38. Heyser C.J., Masliah E., Samimi A., Campbell I.L., Gold L.H. Progressive decline in avoidance learning paralleled by inflammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc Natl Acad Sci U S A 1997, 94:1500-1505.
39. Kozora E., Laudenslager M., Lemieux A., West S.G. Inflammatory and hormonal measures predict neuropsychological functioning in systemic lupus erythematosus and rheumatoid arthritis patients. J Int Neuropsychol Soc 2001, 7:745-754.
40. Mihara M., Hashizume M., Yoshida H., Suzuki M., Shiina M. IL-6/IL-6 receptor system and its role in physiological and pathological conditions. Clin Sci 2011, 122:143-159.
41. Tanaka T., Kishimoto T. Targeting interleukin-6: all the way to treat autoimmune and inflammatory diseases. Int J Biol Sci 2012, 8:1227-1236.
42. Chiba T., Yamada M., Sasabe J., Terashita K., Shimoda M., Matsuoka M., et al. Amyloid-beta causes memory impairment by disturbing the JAK2/STAT3 axis in hippocampal neurons. Mol Psychiatry 2009, 14:206-222.
43. Park S.-J., Shin E.-J., Min S.S., An J., Li Z., Hee Chung Y., et al. Inactivation of JAK2/STAT3 signaling axis and downregulation of M1 mAChR cause cognitive impairment in klotho mutant mice, a genetic model of aging. Neuropsychopharmacology 2013, 38:1426-1437.
44. Malenka R.C., Nicoll R.A. Long-term potentiation-a decade of progress?. Science 1999, 285:1870-1874.
45. Nicolas C.S., Peineau S., Amici M., Csaba Z., Fafouri A., Javalet C., et al. The Jak/STAT pathway is involved in synaptic plasticity. Neuron 2012, 73:374-390.
46. Tancredi V., D'Antuono M., Cafe` C., Giovedi` S., Bue` M.C., D'Arcangelo G., et al. The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogen-activated protein kinase ERK. J Neurochem 2000, 75:634-643.
47. Murray P.J. The JAK-STAT signaling pathway: input and output integration. J Immunol 2007, 178:2623-2629.
48. Ihle J.N. The Stat family in cytokine signaling. Curr Opin Cell Biol 2001, 13:211-217.
49. Neurath M.F., Finotto S. IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev 2011, 22:83-89.
50. Hirohata S., Kanai Y., Mitsuo A., Tokano Y., Hashimoto H. Accuracy of cerebrospinal fluid IL-6 testing for diagnosis of lupus psychosis. A multicenter retrospective study. Clin Rheumatol 2009, 28:1319-1323.