Interleukin-15 receptor is essential to facilitate GABA transmission and hippocampal-dependent memory

Journal of Neuroscience

Volumn 30, Issue 13, 2010, Pages 4725-4734

  He, Yi ^a   Hsuchou, Hung ^a   Wu, Xiaojun ^a   Kastin, Abba J ^a   Khan, Reas S ^a   Pistell, Paul J ^a   Wang, Wei Hsung ^b   Feng, Jiming ^c   Li, Zengbiao ^d   Guo, Xiaochuan ^d   Pan, Weihong ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b Department of Physics ^*  (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d Drumetix Laboratories   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; 4 AMINOBUTYRIC ACID UPTAKE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION RESPONSE; CONDITIONING; CONTROLLED STUDY; FEAR; FOREBRAIN; GABAERGIC TRANSMISSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; MEMORY; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE; SYNAPTOSOME; TURNOVER TIME; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; CELLS, CULTURED; CONDITIONING (PSYCHOLOGY); FEAR; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; INTERLEUKIN-15; INTERLEUKIN-15 RECEPTOR ALPHA SUBUNIT; MAZE LEARNING; MEMORY; MICE; MICE, KNOCKOUT; NEURONS; NEUROTRANSMITTER AGENTS; SYNAPSES; SYNAPTOSOMES;

EID: 77950680176     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6160-09.2010     Document Type: Article

References (46)

1. Asada H, Kawamura Y, Maruyama K, Kume H, Ding R, Ji FY, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K (1996) Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem Biophys Res Commun 229:891-895. (Pubitemid 27035813)
2. Barrientos RM, Higgins EA, Sprunger DB, Watkins LR, Rudy JW, Maier SF (2002) Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav Brain Res 134:291-298.
3. Beck RD Jr, Wasserfall C, Ha GK, Cushman JD, Huang Z, Atkinson MA, Petitto JM (2005) Changes in hippocampal IL-15, related cytokines, and neurogenesis in IL-2 deficient mice. Brain Res 1041:223-230. (Pubitemid 40501335)
4. Bergado-Acosta JR, Sangha S, Narayanan. RT, Obata K, Pape HC, Stork O (2008) Critical role of the 65-kDa isoform of glutamic acid decarboxylase in consolidation and generalization of Pavlovian fear memory. Learn Mem 15:163-171. (Pubitemid 351439146)
5. Bryant CD, Zhang NN, Sokoloff G, Fanselow MS, Ennes HS, Palmer AA, McRoberts JA (2008) Behavioral differences among C57BL/6 substrains: implications for transgenic and knockout studies. J Neurogenet 22:315-331.
6. Budagian V, Bulanova E, Paus R, Bulfone-Paus S (2006) IL-15/IL-15 receptor biology: a guided tour through, an expanding universe. Cytokine Growth Factor Rev 17:259-280. (Pubitemid 44038618)
7. Burman MA, Gewirtz JC (2007) Hippocampal activity, but not plasticity, is required for early consolidation of fear conditioning with a short trace interval. Eur J Neurosci 25:2483-2490.
8. Corcoran KA, Desmond TJ, Frey KA, Maren S (2005) Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J Neurosci 25:8978-8987.
9. Del Arco A, Segovia G, Garrido P, de Blas M, Mora F (2007) Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 176:267-273. (Pubitemid 44880088)
10. Fukuda T, Aika Y, Heizmann CW, Kosaka T (1998) GABAergic axon terminals at perisomatic and dendritic inhibitory sites show different immunoreact.iv.iti.es against two GAD isoforms, GAD67 and GAD65, in the mouse hippocampus: a digitized quantitative analysis. J Comp Neurol 395:177-194. (Pubitemid 28234596)
11. Goshen I, Kreisel T, Ounallah-Saad H, Renbaum P, Zalzstein Y, Ben-Hur T, Levy-Lahad E, Yirmiya R (2007) A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 32:1106-1115. (Pubitemid 350086829)
12. Hanisch UK, Lyons SA, Prinz M, Noite C, Weber JR, Kettenmann H, Kirchhoff F (1997) Mouse brain microglia express interleukin-15 and its multimeric receptor complex functionally coupled to Janus kinase activity. J Biol Chem 272:28853-28860. (Pubitemid 27498165)
13. HeY, Kastin AJ, Hsuchou H, Pan W (2009) The Cdk5/p35 kinases modulate leptin-induced STAT3 signaling. J MoI Neurosci 39:49-58.
14. Heldt SA, Green A, Ressler KJ (2004) Prepulse inhibition deficits in GAD65 knockout mice and the effect of antipsychotic treatment. Neuropsychopharmacology 29:1610-1619. (Pubitemid 39150102)
15. Hsuchou H, He Y, Kastin AJ, Tu H, Markadakis EN, Rogers RC, Fossier PB, Pan W (2009a) Obesity induces functional astrocytic leptin receptors in hypothalamus. Brain 132:889-902.
16. Hsuchou H, Pan W, Wu X, Kastin AJ (2009b) Cessation of blood-to-brain influx of interleukin-15 during development of EAE. J Cereb Blood Flow Metab 29:1568-1578.
17. Ingram DK (1988) Complex maze learning in rodents as a model of agerelated memory impairment. Neurobiol Aging 9:475-485.
18. Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17:749-758. (Pubitemid 47493456)
19. Kobayashi H, Carrasquillo JA, Paik CH, Waldmann TA, Tagaya Y (2000) Differences of biodistribution, pharmacokinetics, and tumor targeting between interleukins 2 and 15. Cancer Res 60:3577-3583. (Pubitemid 30482179)
20. Koo JW, Duman RS (2009) Interleukin-1 receptor null mutant mice show decreased anxiety-like behavior and enhanced fear memory. Neurosci Lett 456:39-43.
21. Kubota T, Brown RA, Fang J, Krueger JM (2001) Interleukin-15 and interleukin-2 enhance non-REM sleep in rabbits. Am J Physiol Regul Integr Comp Physiol 281:R1004-R1012. (Pubitemid 32885117)
22. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
23. Lee YB, Satoh J, Walker DG, Kim SU ( 1996) Interleukin-15 gene expression in human astrocytes and microglia in culture. Neuroreport 7:1062-1066. (Pubitemid 26194481)
24. Locchi F, Dall'Olio R, Gandolfi O, Rimondini R (2007) Water T-maze, an improved method to assess spatial working memory in rats: pharmacological validation. Neurosci Lett 422:213-216. (Pubitemid 47077603)
25. Lodolce JP, Boone DL, Chai S, Swain RE, Dassopoulos T, Trettin. S, Ma A (1998) IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9:669-676. (Pubitemid 28557595)
26. Málińska D (2001) The cytokine network and interleukin-15 (IL-15) in brain development. Folia Neuropathol 39:43-47.
27. McInnes IB, Leung BP, Sturrock RD, Field M, Liew FY (1997) Interleukin-15 mediates T cell-dependent regulation of tumor necrosis factor-alpha production in rheumatoid arthritis. Nat Med. 3:189-195. (Pubitemid 27064704)
28. Myers KM, Davis M (2002) Behavioral and neural analysis of extinction. Neuron 36:567-584.
29. Pan W, Kastin AJ (2001) Upregulation of the transport system for TNFa at the blood-brain barrier. Arch Physiol Biochem 109:350-353. (Pubitemid 35216881)
30. Pan W, Banks WA, Kennedy MK, Gutierrez EG, Kastin AJ (1996) Differential permeability of the BBB in acute EAE: enhanced transport of TNF-a. Am J Physiol 271:E636-E642. (Pubitemid 126757742)
31. Pan W, Zadina JE, Harlan RE, Weber JT, Banks WA, Kastin AJ (1997) Tumor necrosis factor a: a neuromodulator in the CNS. Neurosci Biobehav Rev 21:603-613. (Pubitemid 27458802)
32. Pan W, Kastin AJ, Bell RL, Olson RD (1999) Upregulation of tumor necrosis factor ∞ transport across the blood-brain barrier after acute compressive spinal cord injury. J Neurosci 19:3649-3655. (Pubitemid 29203143)
33. Pan W, Kastin AJ, Rigai T, McLay R, Pick CG (2003) Increased hippocampal uptake of TNFa and behavioral changes in mice. Exp Brain Res 149:195-199.
34. Pan W, Ding Y, Yu Y, Ohtaki H, Nakamachi T, Kastin AJ (2006) Stroke upregulates TNF alpha transport across the blood-brain barrier. Exp Neurol 198:222-233. (Pubitemid 43243760)
35. Pan W, Kastin AJ, Daniel J, Yu C, Baryshnikova LM, von Bartheld CS (2007) TNF alpha trafficking in cerebral vascular endothelial cells. J Neuroim- munol 185:47-56. (Pubitemid 46497436)
36. Pan W, Hsuchou H, He Y, Sakharkar A, Cain C, Yu C, Kastin AJ (2008a) Astrocyte leptin receptor (ObR) and leptin transport in adult-onset obese mice. Endocrinology 149:2798-2806. (Pubitemid 351724513)
37. Pan W, Hsuchou H, Yu C, Kastin AJ (2008b) Permeation of blood-borne IL15 across the blood-brain barrier and the effect of LPS. J Neurochem 106:313-319. (Pubitemid 351840214)
38. Pan W, Yu C, Hsuchou H, Khan RS, Kastin AJ (2009) Cerebral microvascular IL15 is a novel mediator of TNF action. J Neurochem 111:819-827.
39. Pistell PJ, Ingram DK (2010) Development of a water escape-motivated version of the Stone T-maze for mice. Neuroscience 166:61-72.
40. Pugh CR, Kumagawa K, Fleshner M, Watkins LR, Maier SF, Rudy JW (1998) Selective effects of peripheral lipopolysacchari.de administration on contextual and auditory-cue fear conditioning. Brain Behav Immun 12:212-229. (Pubitemid 28520001)
41. Rachal Pugh C, Fleshner M, Watkins LR, Maier SF, Rudy JW (2001) The immune system, and memory consolidation: a role for the cytokine ILlbeta. Neurosci Biobehav Rev 25:29-41. (Pubitemid 32101387)
42. Rentzos M, Cambouri C, Rombos A, Nikolaou C, Anagnostouli M, Tsoutsou A, Dimitrakopoulos A, Triantafyllou N, Vassilopoulos D (2006) IL-15 is elevated in serum and cerebrospinal fluid of patients with multiple sclerosis. J Neurol Sci 241:25-29. (Pubitemid 43112512)
43. Satoh J, Kurohara K, Yukitake M, Kuroda Y ( 1998) Interleukin-15, a T-cell growth, factor, is expressed in human neural cell lines and tissues. J Neurol Sci 155:170-177. (Pubitemid 28139016)
44. Sutch RJ, Davies CC, Bowery NG (1999) GABA release and uptake measured in crude synaptosomes from genetic absence epilepsy rats from Strasbourg (GAERS). Neurochem Int 34:415-425.
45. Wang QP, Guan JL, Pan W, Kastin AJ, Shioda S (2008) A diffusion barrier between the area postrema and nucleus tractus solitarius. Neurochem Res 33:2035-2043.
46. Yirmiya R, Winocur G, Goshen I (2002) Brain interleukin-1 is involved in spatial memory and passive avoidance conditioning. Neurobiol Learn Mem 78:379-389. (Pubitemid 35366017)