Inactivation of JAK2/STAT3 signaling axis and downregulation of m1 mAChR cause cognitive impairment in klotho mutant mice, a genetic model of aging

Neuropsychopharmacology

Volumn 38, Issue 8, 2013, Pages 1426-1437

  Park, Seok Joo ^a,b   Shin, Eun Joo ^a   Min, Sun Seek ^c   An, Jihua ^c   Li, Zhengyi ^a   Hee Chung, Yoon ^d   Hoon Jeong, Ji ^d   Bach, Jae Hyung ^a   Nah, Seung Yeol ^e   Kim, Won Ki ^f   Jang, Choon Gon ^g   Kim, Yong Sun ^b   Nabeshima, Yo Ichi ^h   Nabeshima, Toshitaka ⁱ   Kim, Hyoung Chun ^a  

^a Kangwon National University   (South Korea)

^b Hallym University   (South Korea)

^c Eulji University   (South Korea)

^d Chung Ang University   (South Korea)

^e Konkuk University   (South Korea)

^f Korea University College of Medicine   (South Korea)

^g Sungkyunkwan University   (South Korea)

^h INSTITUTE OF BIOMEDICAL RESEARCH AND INNOVATION   (Japan)

ⁱ MEIJO UNIVERSITY   (Japan)

Author keywords

cognitive impairment; JAK2 STAT3; klotho gene; long term potentiation; M1 mAChR; PKC ERK CREB BDNF

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLINE ACETYLTRANSFERASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; JANUS KINASE 2; KLOTHO PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MUSCARINIC M1 RECEPTOR; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOLIPASE C; PROTEIN KINASE C BETA; STAT3 PROTEIN;

AGING; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATIVE MEMORY; COGNITIVE DEFECT; CONTROLLED STUDY; DIMERIZATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE MUTATION; GENETIC MODEL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; LONG TERM POTENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VISUAL MEMORY;

AGING; ANIMALS; COGNITION DISORDERS; DOWN-REGULATION; GLUCURONIDASE; HIPPOCAMPUS; JANUS KINASE 2; MICE; MICE, MUTANT STRAINS; MODELS, ANIMAL; ORGAN CULTURE TECHNIQUES; RECEPTOR, MUSCARINIC M1; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84879415127     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.39     Document Type: Article

References (48)

1. Alkam T, Nitta A, Furukawa-Hibi Y, Niwa M, Mizoguchi H, Yamada K et al (2010). Oral supplementation with Leu-Ile, a hydrophobic dipeptide, prevents the impairment of memory induced by amyloid beta in mice via restraining the hyperpho-sphorylation of extracellular signal-regulated kinase. Behav Brain Res 210: 184-190.
2. Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, Rahnama NP, Nathanson NM et al (2003). Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice. Nat Neurosci 6: 51-58. (Pubitemid 36026332)
3. Asanuma M, Nishibayashi S, Iwata E, Kondo Y, Nakanishi T, Vargas MG et al (1996). Alterations of cAMP response element-binding activity in the aged rat brain in response to administration of rolipram, a cAMP-specific phosphodiesterase inhibitor. Brain Res Mol Brain Res 41: 210-215. (Pubitemid 26288163)
4. Bach JH, Chung YH, Park SJ, Jin CH, Shin EJ, Jeong JH et al (2010). Klotho gene plays an important role in attenuating cognitive dysfunction in aging organism. Society for Neuroscience: San Diego, USA.
5. Berkeley JL, Gomeza J, Wess J, Hamilton SE, Nathanson NM, Levey AI (2001). M1 muscarinic acetylcholine receptors activate extracellular signal-regulated kinase in CA1 pyramidal neurons in mouse hippocampal slices. Mol Cell Neurosci 18: 512-524. (Pubitemid 34008391)
6. Bursa R, Gamalero SR, Genazzani E, Eva C (1995). In primary neuronal cultures muscarinic m1 and m3 receptor mRNA levels are regulated by agonists, partial agonists and antagonists. Eur J Pharmacol 289: 9-16.
7. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G (1998). Endogenous ACh enhances striatal NMDA-responses via M1-like muscarinic receptors and PKC activation. Eur J Neurosci 10: 2887-2895. (Pubitemid 29073961)
8. Cattaneo E, Conti L, De-Fraja C (1999). Signalling through the JAK-STAT pathway in the developing brain. Trends Neurosci 22: 365-369. (Pubitemid 29339250)
9. Chao LP, Wolfgram F (1972). Spectrophotometric assay for choline acetyltransferase. Anal Biochem 46: 114-118.
10. Chiba T, Yamada M, Sasabe J, Terashita K, Shimoda M, Matsuoka M et al (2009). Amyloid-beta causes memory impairment by disturbing the JAK2/STAT3 axis in hippocampal neurons. Mol Psychiatry 14: 206-222.
11. Chou H, Ogawa N, Asanuma M, Hirata H, Kondo Y, Mori A (1993). Rapid response of striatal muscarinic M1-receptor mRNA to muscarinic cholinergic agents in rat brain. Mol Brain Res 19: 211-214.
12. Chung YH, Kim EJ, Shin CM, Joo KM, Kim MJ, Woo HW et al (2002). Age-related changes in CREB binding protein immunor-eactivity in the cerebral cortex and hippocampus of rats. Brain Res 956: 312-318. (Pubitemid 35351398)
13. De-Fraja C, Conti L, Magrassi L, Govoni S, Cattaneo E (1998). Members of the JAK/STAT proteins are expressed and regulated during development in the mammalian forebrain. J Neurosci Res 54: 320-330. (Pubitemid 28493942)
14. Fisher A, Pittel Z, Haring R, Bar-Ner N, Kliger-Spatz M, Natan N et al (2003). M1 muscarinic agonists can modulate some of the hallmarks in Alzheimer's disease: implications in future therapy. J Mol Neurosci 20: 349-356. (Pubitemid 38146993)
15. Franklin KBJ, Paxinos G (2008). The Mouse Brain in Stereotaxic Coordinates. 3rd edn. Academic Press: San Diego, CA.
16. Gurwitz D, Haring R, Haring R, Heldman E, Fraser CM, Manor D et al (1994). Duscrete activation of transduction pathways associated with acetylcholine m1 receptor by several muscarinic ligands. Eur J Pharmacol 267: 21-31.
17. Hoyer D, Boddeke HW (1993). Partial agonists, full agonists, antagonists: dilemmas of definition. Trends Pharmacol Sci 14: 270-275. (Pubitemid 23204245)
18. Ihle JN, Witthuhn BA, Quelle FW, Yamamoto K, Silvennoinen O (1995). Signaling through the hematopoietic cytokine receptors. Annu Rev Immunol 13: 369-398.
19. Jin CH, Shin EJ, Park JB, Jang CG, Li Z, Kim MS et al (2009). Fustin flavonoid attenuates beta-amyloid (1-42)-induced learning impairment. J Neurosci Res 87: 3658-3670.
20. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T et al (1997). Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390: 45-51. (Pubitemid 27494749)
21. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P et al (2005). Suppression of aging in mice by the hormone Klotho. Science 309: 1829-1833. (Pubitemid 41325087)
22. Li SA, Watanabe M, Yamada H, Nagai A, Kinuta M, Takei K (2004). Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct Funct 29: 91-99. (Pubitemid 40260033)
23. Liu N, Varma S, Shooter EM, Tolwani RJ (2005). Enhancement of Schwann cell myelin formation by K252a in the Trembler-J mouse dorsal root ganglion explant culture. J Neurosci Res 79: 310-317. (Pubitemid 40278345)
24. Lu WY, Xiong ZG, Lei S, Orser BA, Dudek E, Browning MD et al (1999). G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat Neurosci 2: 331-338. (Pubitemid 30491275)
25. MacDonald JF, Kotecha SA, Lu WY, Jackson MF (2001). Convergence of PKC-dependent kinase signal cascades on NMDA receptors. Curr Drug Targets 2: 299-312. (Pubitemid 32821472)
26. Marino MJ, Rouse ST, Levey AI, Potter LT, Conn PJ (1998). Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci USA 95: 11465-11470. (Pubitemid 28450152)
27. Mehler MF, Kessler JA (1997). Hematolymphopoietic and inflammatory cytokines in neural development. Trends Neurosci 20: 357-365. (Pubitemid 27319848)
28. Min SS, Quan HY, Ma J, Han JS, Jeon BH, Seol GH (2009). Chronic brain inflammation impairs two forms of long-term potentiation in the rat hippocampal CA1 area. Neurosci Letters 456: 20-24.
29. Mizuno M, Yamada K, Takei N, Tran MH, He J, Nakajima A et al (2003). Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol Psychiatry 8: 217-224. (Pubitemid 36315230)
30. Nagai T, Yamada K, Kim HC, Kim YS, Noda Y, Imura A et al (2003). Cognition impairment in the genetic model of aging klotho gene mutant mice: a role of oxidative stress. FASEB J 17: 50-52.
31. Nicolas CS, Peineau S, Amici M, Csaba Z, Fafouri A, Javalet C et al (2012). The Jak/STAT pathway is involved in synaptic plasticity. Neuron 73: 374-390.
32. Nomura Y, Kitamura Y, Ohnuki T, Arima T, Yamanaka Y, Sasaki K et al (1997). Alterations in acetylcholine, NMDA, benzodiazepine receptors and protein kinase C in the brain of the senescence-accelerated mouse: an animal model useful for studies on cognitive enhancers. Behav Brain Res 83: 51-55. (Pubitemid 27086614)
33. O'Neil C, Marcusson J, Nordberg A, Winblad B (1987). The influence of age on neurotransmitters in the human brain. In: Govoni SBattaini F (eds) NATO Advanced Research Workshop on Modifications of Cell to Cell Signals during Normal and Pathological Aging. Springer-Verlag: Salò, Garda Lake, Italy. Vol 9, pp 183-198.
34. Orellana DI, Quintanilla RA, Gonzalez-Billault C, Maccioni RB (2005). Role of the JAKs/STATs pathway in the intracellular calcium changes induced by interleukin-6 in hippocampal neurons. Neurotox Res 8: 295-304.
35. Pepitoni S, Wood IC, Buckley NJ (1997). Structure of the m1 muscarinic acetylcholine receptor gene and its promoter. J Biol Chem 272: 17112-17117. (Pubitemid 27289820)
36. Sgambato V, Vanhoutte P, Pages C, Rogard M, Hipskind R, Besson MJ et al (1998). In vivo expression and regulation of Elk-1, a target of the extracellular-regulated kinase signaling pathway, in the adult rat brain. J Neuroscience 18: 214-226. (Pubitemid 28046783)
37. Shaulian E, Karin M (2001). AP-1 in cell proliferation and survival. Oncogene 20: 2390-2400. (Pubitemid 32531297)
38. Shin EJ, Chae JS, Park SJ, Kim SC, Koo KH, Yamada K et al (2009). Growth hormone-releaser diet attenuates beta-amyloid(1-42)-induced cognitive impairment via stimulation of the insulin-like growth factor (IGF)-1 receptor in mice. J Pharmacol Sci 109: 139-143.
39. Sun MK, Alkon DL (2005). Protein kinase C isozymes: memory therapeutic potential. Curr Drug Targets CNS Neurol Disord 4: 541-552. (Pubitemid 41448380)
40. Svedberg MM, Bednar I, Nordberg A (2004). Effect of subchronic galantamine treatment on neuronal nicotinic and muscarinic receptor subtypes in transgenic mice overexpressing human acetylcholinesterase. Neuropharmacology 47: 558-571. (Pubitemid 39221778)
41. Wall PM, Flinn J, Messier C (2001). Infralimbic muscarinic M1 receptors modulate anxiety-like behaviour and spontaneous working memory in mice. Psychopharmacology (Berl) 155: 58-68. (Pubitemid 32295770)
42. Walland A, Pieper MP (1998). Central activation of the sympathetic nervous system including the adrenals in anaesthetized guinea pigs by the muscarinic agonist talsaclidine. Naunyn-Schmiedeberg's Arch Pharmacol 357: 426-430. (Pubitemid 28188321)
43. Wang Q, Zengin A, Ying W, Newell KA, Wang P, Yeo W et al (2008). Chronic treatment with simvastatin upregulates mus-carinic M1/4 receptor binding in the rat brain. Neuroscience 154: 1100-1106.
44. Wayman GA, Impey S, Marks D, Saneyoshi T, Grant WF, Derkach V et al (2006). Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50: 897-909. (Pubitemid 43850689)
45. Weeber EJ, Atkins CM, Selcher JC, Varga AW, Mirnikjoo B, Paylor R et al (2000). A role for the beta isoform of protein kinase C in fear conditioning. J Neurosci 20: 5906-5914. (Pubitemid 30658381)
46. Williams CM, El Mohsen MA, Vauzour D, Rendeiro C, Butler LT, Ellis JA et al (2008). Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med 45: 295-305.
47. Zhang LC, Buccafusco JJ (2000). Adaptive changes in M1 muscarinic receptors localized to specific rostral brain regions during and after morphine withdrawal. Neuropharmacology 39: 1720-1731. (Pubitemid 30398477)
48. Zola-Morgan S, Squire LR, Amaral DG (1986). Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6: 2950-2967. (Pubitemid 16026076)