Interleukin17A promotes postoperative cognitive dysfunction by triggering β-amyloid accumulation via the transforming growth factor-β (TGFβ)/Smad signaling pathway

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Tian, Ayong ^a   Ma, Hong ^a   Zhang, Rongwei ^a   Tan, Wenfei ^a   Wang, Xiaolong ^a   Wu, Binyang ^a   Wang, Jun ^a   Wan, Chengfu ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; INTERLEUKIN 17; SMAD PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; AMYLOID PRECURSOR PROTEIN; BIOLOGICAL MARKER; CYTOKINE; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MOLECULAR PATHOLOGY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; POSTOPERATIVE COGNITIVE DYSFUNCTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ADVERSE EFFECTS; ANIMAL; ANTAGONISTS AND INHIBITORS; COGNITION DISORDERS; DISEASE MODEL; LIVER RESECTION; MAZE TEST; METABOLISM; PATHOLOGY; PHOSPHORYLATION; POSTOPERATIVE COMPLICATION; SHORT TERM MEMORY; SPATIAL MEMORY;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIBODIES, MONOCLONAL; ASTROCYTES; BIOMARKERS; COGNITION DISORDERS; CYTOKINES; DISEASE MODELS, ANIMAL; HEPATECTOMY; HIPPOCAMPUS; INTERLEUKIN-17; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; PHOSPHORYLATION; POSTOPERATIVE COMPLICATIONS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SPATIAL MEMORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84949921501     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141596     Document Type: Article

References (58)

1. Rasmussen LS (1988) Defining postoperative cognitive dysfunction. Eur J Anesthesiol 15: 761-764.
2. Moller JT, Cluitmans P, Rasmussen LS, Houx P, Rasmussen H, Canet J et al (1998) Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction. Lancet 351: 857-861. PMID: 9525362
3. Chen X, Zhao M, White PF, Li S, Tang J, Wender RH, et al (2001) The recovery of cognitive function after general anaesthesia in elderly patients: a comparison of desflurane and sevoflurane. Anaesth Analg 93: 1489-94.
4. Newman MF, Kirchner JL, Phillips-Bute B, Gaver V, Grocott H, Jones R H, et al (2001) Neurological Outcome Research Group and the Cardiothoracic Anesthesiology Research Endeavors InvestigatorsLongitudinal assessment of neurocognitive function after coronary-artery bypass surgery. N Engl J Med 344: 395-402. PMID: 11172175
5. Cao XZ, Ma H, Wang JK, Liu F, Wu BY, Tian AY, et al (2010) Postoperative cognitive deficits and neuroinflammation in the hippocampus triggered by surgical trauma are exacerbated in aged rats.Prog Neuropsychopharmacol Biol Psychi 34: 1426-1432.
6. Cibelli M, Fidalgo AR, Terrando N, Ma D, Monaco C, Feldmann M, et al (2010) Role of interleukin-1beta in postoperative cognitive dysfunction. Ann Neuro 68: 360-368.
7. Kamer AR, Galoyan SM, Haile M, Kline R, Boutajangout A, Li YS, et al (2012) Meloxicam improves object recognition memory and modulates glial activation after splenectomy in mice. Eur J Anaesthes 29: 332-337.
8. Rosczyk HA, Sparkman NL, Johnson RW (2008) Neuroinflammation and cognitive function in aged mice following minor surgery. Exp Geron 43:840-846.
9. McGeer PL, McGeer EG (1995) The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res Rev 21:195-218 PMID: 8866675
10. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21: 383-421. PMID: 10858586
11. Zhao J, O'Connor T, Vassar R (2011) The contribution of activated astrocytes to Aβ production: implications for Alzheimer's disease pathogenesis. J Neuroinflammation 8: 150. doi: 10.1186/1742-2094-8-150 PMID: 22047170
12. Flanders KC, Lippa CF, Smith TW, Pollen DA, Sporn MB (1995) Altered expression of transforming growth factor-beta in Alzheimer's disease. Neurology 45: 1561-1569. PMID: 7543987
13. Lesné S, Docagne F, Gabriel C, Liot G, Lahiri DK, Buée L, et al (2003) Transforming growth factor-beta 1 potentiates amyloid-beta generatiaon in astrocytes and in transgenic mice. J Biol Chem 278: 18408-18418. PMID: 12626500
14. Vawter MP, Dillon-Carter O, Tourtellotte WW, Carvey P, Freed WJ (1996) TGFbeta1 and TGFbeta2 concentrations are elevated in Parkinson's disease in ventricular cerebrospinal fluid. Exp Neurol 142: pp. 313-322. PMID: 8934562
15. Van Horssen J, Bo L, Dijkstra CD, de Vries HE (2006) Extensive extracellular matrix depositions in active multiple sclerosis lesions Neurobiol Dis 24: pp. 484-491. PMID: 17005408
16. Tesseur I, Zou K, Esposito L, Bard F, Berber E, Can JV, et al (2006) Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J Clin Invest 116: 3060-3069. PMID: 17080199
17. Martinez GJ, Nurieva RI, Yang XO, Dong C (2008) Regulation and function of proinflammatory TH17 cells. Ann N Y Acad Sci 1143: 188-211. doi: 10.1196/annals.1443.021 PMID: 19076351
18. Dong C (2008) TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 8: 337-348. doi: 10.1038/nri2295 PMID: 18408735
19. Onishi RM, Gaffen SL (2010) Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 129: 311-321. doi: 10.1111/j.1365-2567.2009.03240.x PMID: 20409152
20. Miossec P (2009) IL-17 and Th17 cells in human inflammatory diseases. Microbes Infect 11: 625-630. doi: 10.1016/j.micinf.2009.04.003 PMID: 19371791
21. Qian Y, Kang Z, Liu C, Li X (2010) IL-17 signaling in host defense and inflammatory diseases. Cell Mol Immunol 7: 328-333. doi: 10.1038/cmi.2010.27 PMID: 20514051
22. Reynolds AD, Stone DK, Hutter JA, Benner EJ, Mosley RL, Gendelman HE, et al (2010) cells attenuate Th17 cell-mediated nigrostriatal dopaminergic neurodegeneration in a model of Parkinson's disease. J Immunol 184: 2261-71. doi: 10.4049/jimmunol.0901852 PMID: 20118279
23. Christensen JR, Börnsen L, Ratzer R, Piehl F, Khademi M, Olsson T, et al (2013) Systemic Inflammation in Progressive Multiple Sclerosis Involves Follicular T-Helper, Th17-and Activated B-Cells and Correlates with Progression. PLoS One 8:5782014.
24. Zhang J, Ke KF, Liu Z, Qiu YH, Peng YP (2013) Th17 Cell-Mediated Neuroinflammation Is Involved in Neurodegeneration of Aβ1-42-Induced Alzheimer's Disease Model Rats. PLoS One 8: e75786. doi: 10. 1371/journal.pone.0075786 PMID: 24124514
25. Abraham J, Jang S, Godbout JP, Chen J, Kelley KW, Dantzer R (2008) Aging sensitizes mice to behavioral deficits induced by central HIV-1 gp120. Neurobiol Aging 29: 614-621. PMID: 17174449
26. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1: 848-58. PMID: 17406317
27. Deacon RM, Rawlins JN (2006) T-maze alternation in the rodent. Nat Protoc 1: 7-12. PMID: 17406205
28. Qin H, Niyongere SA, Lee SJ, Baker BJ, Benveniste EN (2008) Expression and functional significance of SOCS-1 and SOCS-3 in astrocytes. J Immunol 181:3167-3176. PMID: 18713987
29. Mandybur TI, Chuirazzi BA (1990) Astrocytes and the plaques of Alzheimer's disease. Neurology 40: 635-639. PMID: 1690867
30. Gaffen SL (2009) Structure and signaling in the IL-17 receptor family. Nat Rev Immunol 9: 556-567. doi: 10.1038/nri2586 PMID: 19575028
31. Das Sarma J, Ciric B, Marek R, Sadhukhan S, Caruso ML, Shafagh J (2009) Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. J Neuroinflammation 6: 14. doi: 10.1186/1742-2094-6-14 PMID: 19400960
32. Docagne F, Gabriel C, Lebeurrier N, Lesné S, Hommet Y, Plawinski L, et al (2004) Sp1 and Smad trnscription factors co-operate to mediate TGF-beta-dependent activation of amyloid-beta precursor protein gene transcription. Biochem J 383: 393-399. PMID: 15242331
33. Wyss-Coray T, Lin C, Sanan DA, Mucke L, Masliah E (2000) Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am J Pathol 156: 139-150. PMID: 10623661
34. Steinmetz J, Christensen KB, Lund T, Lohse N, Rasmussen LS (2009) ISPOCD Group. Long-term consequences of postoperative cognitive dysfunction. Anesthesiology 110: 548-55. doi: 10.1097/ALN. 0b013e318195b569 PMID: 19225398
35. Rasmussen LS, Johnson T, Kuipers HM, Kristensen D, Siersma VD, Vila P, et al (2003) Does anaesthesia cause postoperative cognitive dysfunction? A randomised study of regional versus general anaesthesia in 438 elderly patients. Acta Anaesthesiol Scand 47: 260-66 PMID: 12648190
36. Bettelli E, Korn T, Oukka M, Kuchroo VK (2008) Induction and effector functions of T(H)17 cells. Nature 453: 1051-1057. doi: 10.1038/nature07036 PMID: 18563156
37. Korn T, Bettelli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 Cells. Annu Rev Immunol 27: 485-517. doi: 10.1146/annurev.immunol.021908.132710 PMID: 19132915
38. Graber JJ, Allie SR, Mullen KM, Jones MV, Wang T, Krishnan C, et al (2008) Interleukin-17 in transverse myelitis and multiple sclerosis. J Neuroimmunol 196: 124-132. doi: 10.1016/j.jneuroim.2008.02. 008 PMID: 18417225
39. Inoue D, Numasaki M, Watanabe M, Kubo H, Sasaki T, Yasuda H, et al (2006) IL-17A promotes the growth of airway epithelial cells through ERK-dependent signaling pathway.Biochem. Biophys. Res Commun 347: 852-858. PMID: 16859642
40. Toy D, Kugler D, Wolfson M, Vanden Bos T, Gurgel J, Derry J, et al (2006) Cutting edge: interleukin 17 signals through a heteromeric receptor complex. J Immunol 177: 36-39. PMID: 16785495
41. Schultz J, Schwarz A, Neidhold S, Burwinkel M, Riemer C, Simon D, et al (2004) Role of interleukin-1 in prion disease-associated astrocyte activation. Am. J Pathol 165: 671-678. PMID: 15277240
42. Masters CL, Cappai R, Barnham KJ, Villemagne VL (2006) Molecular mechanisms for Alzheimer's disease: implications for neuroimaging and therapeutics. J Neurochem 97: 1700-1725. PMID: 16805778
43. Griffin WS, Sheng JG, Royston MC, Gentleman SM, McKenzie JE, Graham DI, et al (1998) Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol 8: 65-72. PMID: 9458167
44. Forloni G, Chiesa R, Smiroldo S, Verga L, Salmona M, Tagliavini F, et al (1993) Apoptosis mediated neurotoxicity induced by chronic application of beta amyloid fragment 25-35. Neuroreport 4: 523-526. PMID: 8513131
45. Loo DT, Copani A, Pike CJ, Whittemore ER, Walencewicz AJ, Cotman CW (1993) Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc Natl Acad Sci U S A 90: 7951-7955. PMID: 8367446
46. Mattson MP, Partin J, Begley JG (1998) Amyloid beta-peptide induces apoptosis-related events in synapses and dendrites. Brain Res 807: 167-176. PMID: 9757026
47. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, et al (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23: 8692-8700. PMID: 14507968
48. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, et al (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410: 471-475. PMID: 11260714
49. Massagué J (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6: 597-641. PMID: 2177343
50. Massagué J,Wotton D (2000) Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 19: 1745-1754. PMID: 10775259
51. Baig S, van Helmond Z, Love S (2009) Tau hyperphosphorylation affects Smad 2/3 translocation. Neuroscience 163: 561-570. doi: 10.1016/j.neuroscience.2009.06.045 PMID: 19555739
52. Servi B, La Porta CA, Bontempelli M, Comolli R (2002) Decrease of TGF-beta1 plasma levels and increase of nitric oxide synthase activity in leukocytes as potential biomarkers of Alzheimer's disease. Exp Gerontol 37:813-821. PMID: 12175481
53. Lee HG, Ueda M, Zhu X, Perry G, Smith MA (2006) Ectopic expression of phospho-Smad2 in Alzheimer's disease: uncoupling of the transforming growth factor-beta pathway? J Neurosci Res 84: 1856-1861. PMID: 16998902
54. Blasko I, Veerhuis R, Stampfer-Kountchev M, Saurwein-Teissl M, Eikelenboom P, Grubeck-Loebenstein B (2000) Costimulatory effects of interferon-gamma and interleukin-1beta or tumor necrosis factor alpha on the synthesis of Abeta1-40 and Abeta1-42 by human astrocytes. Neurobiol Dis 7: 682-689. PMID: 11114266
55. Hu J, Akama KT, Krafft GA, Chromy BA, Van Eldik LJ (1998) Amyloid-beta peptide activates cultured astrocytes: morphological alterations, cytokine induction and nitric oxide release. Brain Res 785: 195-206. PMID: 9518610
56. White JA, Manelli AM, Holmberg KH, Van Eldik LJ, Ladu MJ (2005) Differential effects of oligomeric and fibrillar amyloid-beta 1-42 on astrocyte-mediated inflammation. Neurobiol Dis 18:459-465. PMID: 15755672
57. Akama KT, Van Eldik LJ (2000) Beta-amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1beta-and tumor necrosis factor-alpha (TNFalpha)-dependent, and involves a TNFalpha receptor-associated factor-and NFkappaB-inducing kinase-dependent signaling mechanism. J Biol Chem 275: 7918-7924. PMID: 10713108
58. Craft JM, Watterson DM, Frautschy SA, Van Eldik LJ (2004) Aminopyridazines inhibit beta-amyloidinduced glial activation and neuronal damage in vivo. Neurobiol Aging 25: 1283-1292. PMID: 15465624