Anesthetics and tau protein: Animal model studies

Journal of Alzheimer's Disease

Volumn 22, Issue SUPPL. 3, 2010, Pages

  Run, Xiaoqin ^a,b   Liang, Zhihou ^a,b   Gong, Cheng Xin ^b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

Alzheimer's disease; anesthesia; phosphorylation; tau

Indexed keywords

ANESTHETIC AGENT; CHLORAL HYDRATE; HALOTHANE; ISOFLURANE; PENTOBARBITAL; TAU PROTEIN;

ALZHEIMER DISEASE; COGNITIVE DEFECT; GENERAL ANESTHESIA; NERVE DEGENERATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW;

EID: 78650456123     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100813     Document Type: Review

References (85)

1. Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM (2007) Forecasting the global burden of Alzheimer's disease. Alzheimers Dement 3, 186-191.
2. Alzheimer's Association. Home page. Available at: http://www.alz.org. Accessed March 2009.
3. Evered LA, Silbert BS, Scott DA, Maruff P, Laughton KM, Volitakis I, Cowie T, Cherny RA, Masters CL, Li QX (2009) Plasma amyloid beta42 and amyloid beta40 levels are associated with early cognitive dysfunction after cardiac surgery. Ann Thorac Surg 88, 1426-1432.
4. Culley DJ, Xie Z, Crosby G (2007) General anesthetic-induced neurotoxicity: an emerging problem for the young and old? Curr Opin Anaesthesiol 20, 408-413.
5. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 19, 353-356.
6. Francis PT, Palmer AM , Snape M, Wilcock GK (1999) The cholinergic hypothesis of Alzheimer's disease: a review of progress. J Neurol Neurosurg Psychiatry 66, 137-147.
7. Iqbal K, Grundke-Iqbal I (2005) Metabolic/signal transduction hypothesis of Alzheimer's disease and other tauopathies. Acta Neuropathol 109, 25-31.
8. Gong CX, Liu F, Grundke-Iqbal I, Iqbal K (2006) Impaired brain glucose metabolism leads to Alzheimer neurofibrillary degeneration through a decrease in tau O-GlcNAcylation. J Alzheimers Dis 9, 1-12.
9. Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23, 134-147.
10. Zhu X, Raina AK, Perry G, Smith MA (2004) Alzheimer's disease: the two-hit hypothesis. Lancet Neurol 3, 219-226.
11. Maragos WF, Greenamyre JT, Penney Jr JB,Young AB (1987) Glutamate dysfunction in Alzheimer's disease: an hypothesis. Trends Neurosci 10, 65-68.
12. Supnet C, Bezprozvanny I (2010) The dysregulation of intracellular calcium in Alzheimer disease. Cell Calcium 47, 183-189.
13. Hardy J (2009) The amyloid hypothesis for Alzheimer's disease: acritical reappraisal. JNeurochem 110, 1129-1134.
14. Iqbal K, Liu F, Gong CX, Alonso Adel C, Grundke-Iqbal I (2009) Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 118, 53-69.
15. Grundke-Iqbal I, Iqbal K, Ting YC, Quinlan M, Wisniews-ki HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83, 4913-4917.
16. Goeder M (1996) Tau protein and the neurofibrillary pathology of Alzheimer's disease. Ann NY Acad Sci 777, 121-131.
17. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Titani K, Ihara Y (1995) Proline-directed and non-proline-directed phosphorylation of PHF-tau. J Biol Chem 270, 823-829.
18. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS,Wisniewski HM (1986) Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 261, 6084-6089.
19. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofib-rillary tangles of Alzheimer's disease. Neuron 3, 519-526.
20. Spillantini MG, Goedert M (1998) Tau protein pathology in neurodegenerative diseases. TrendsNeurosci 21, 428-433.
21. Yu Y, Run X, Liang Z, Li Y, Liu F, Liu Y, Iqbal K, Grundke-Iqbal I, Gong CX (2009) Developmental regulation of tau phosphorylation, tau kinases, and tau phosphatases. J Neurochem 108, 1480-1494.
22. Bramblett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ, Lee VM (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099.
23. Yoshida H, Ihara Y (1993) Tau in paired helical filaments is functionally distinct from fetal tau: assembly incompetence of paired helical filament-tau. J Neurochem 61, 1183-1186.
24. Gong CX, Liu F, Grundke-Iqbal I, Iqbal K (2005) Post-translational modifications of tau protein in Alzheimer's disease. J Neural Transm 112, 813-838. (Pubitemid 40655573)
25. Alonso AC, Grundke-Iqbal I, Iqbal K (1996) Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat Med 2, 783-787.
26. Alonso AD, Grundke-Iqbal I, Barra HS, Iqbal K (1997) Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of micro-tubules by the abnormal tau. Proc Natl Acad Sci U S A 94, 298-303.
27. Hernandez F, Avila J (2008) Tau aggregates and tau pathology. JAlzheimers Dis 14, 449-452.
28. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingels-son M, Guimaraes A, Deture M, Ramsden M, McGowan E, Forster C, Yue M, Orne J, Janus C, Mariash A, Kuskowski M, Hyman B, Hutton M, Ashe KH (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476-481.
29. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M (2000) Neurofibrillary tangles, amy-otrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25, 402-405.
30. Gotz J, Chen F, Barmettler R, Nitsch RM (2001) Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 276, 529-534.
31. Tanemura K, Murayama M, Akagi T, Hashikawa T, Tomina-ga T, Ichikawa M, Yamaguchi H, Takashima A (2002) Neu-rodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. JNeurosci 22, 133-141.
32. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615622.
33. Gong CX, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K (1995) Phosphatase activity toward abnormally phosphory-lated tau: decrease in Alzheimer disease brain. J Neurochem 65, 732-738.
34. Gong CX, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K (1995) Phosphatase activity toward abnormally phosphory-lated tau: decrease in Alzheimer disease brain. J Neurochem 65, 732-738.
35. Loring JF, Wen X, Lee JM, Seilhamer J, Somogyi R (2001)A gene expression profile of Alzheimer's disease. DNA Cell Biol 20, 683-695.
36. Sontag E, Luangpirom A, Hladik C, Mudrak I, Ogris E, Spe-ciale S, White CL 3rd (2004) Altered expression levels of the protein phosphatase 2A ABalphaC enzyme are associated with Alzheimer disease pathology. J Neuropathol Exp Neurol 63, 287-301.
37. Liu F, Grundke-Iqbal I, Iqbal K, Gong CX (2005) Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur J Neurosci 22, 1942-1950.
38. Liu F, Iqbal K, Grundke-Iqbal I, Hart GW, Gong CX (2004) O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease. Proc Natl Acad Sci U S A 101, 10804-10809.
39. Li X, Lu F, Wang JZ, Gong CX (2006) Concurrent alterations of O-GlcNAcylation and phosphorylation of tau in mouse brains during fasting. Eur J Neurosci 23, 2078-2086.
40. Liu F, Shi J, Tanimukai H, Gu J, Gu J, Grundke-Iqbal I, Iqbal K, Gong CX (2009) Reduced O-GlcNAcylation links lower brain glucose metabolism and tau pathology in Alzheimer's disease. Brain 132, 1820-1832.
41. Goldbaum O, Richter-Landsberg C (2002) Activation of PP2A-like phosphatase and modulation of tau phosphoryla-tion accompany stress-induced apoptosis in cultured oligoden-drocytes. Glia 40, 271-282.
42. Rissman RA (2009) Stress-induced tau phosphorylation: functional neuroplasticity or neuronal vulnerability? J Alzheimers Dis 18, 453-457.
43. Rissman RA, Lee KF, Vale W, Sawchenko PE (2007) Corticotropin-releasing factor receptors differentially regulate stress-induced tau phosphorylation. J Neurosci 27, 6552-6562.
44. Geschwind DH (2003) Tau phosphorylation, tangles, and neu-rodegeneration: the chicken or the egg? Neuron 40, 457-460.
45. Bulbarelli A, Lonati E, Cazzaniga E, Gregori M, Masserini M (2009) Pin1 affects Tau phosphorylation in response to Abeta oligomers. Mol Cell Neurosci 42, 75-80.
46. Ballatore C, Lee VM, Trojanowski JQ (2007) Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 8, 663-672.
47. Ikeda Y, Ishiguro K, Fujita SC (2007) Ether stress-induced Alzheimer-like tau phosphorylation in the normal mouse brain. FEBSLett 581, 891-897. (Pubitemid 46282719)
48. Planel E, Richter KE, Nolan CE, Finley JE, Liu L, Wen Y, Krishnamurthy P, Herman M, Wang L, Schachter JB, Nelson RB, Lau LF, Duff KE (2007) Anesthesia leads to tau hyper-phosphorylation through inhibition of phosphatase activity by hypothermia. J Neurosci 27, 3090-3097.
49. Planel E, Krishnamurthy P, Miyasaka T, Liu L, Herman M, Kumar A, Bretteville A, Figueroa HY, Yu WH, Whitting-ton RA, Davies P, Takashima A, Nixon RA, Duff KE (2008) Anesthesia-induced hyperphosphorylation detaches 3-repeat tau from microtubules without affecting their stability in vivo. JNeurosci 28, 12798-12807.
50. Planel E, Bretteville A, Liu L, Virag L, Du AL, Yu WH, Dickson DW, Whittington RA, Duff KE (2009) Acceleration and persistence of neurofibrillary pathology in a mouse model oftauopathy following anesthesia. FASEB J 23, 2595-2604.
51. Run X, Liang Z, Zhang L, Iqbal K, Grundke-Iqbal I, Gong CX (2009) Anesthesia induces phosphorylation of tau. J Alzheimers Dis 16, 619-626.
52. Cook DM, Kendall JW, Greer MA, Kramer RM (1973) The effect of acute or chronic ether stress on plasma ACTH concentration in the rat. Endocrinology 93, 1019-1024.
53. Emmert ME, Herman JP (1999) Differential forebrain c-fos mRNA induction by ether inhalation and novelty: evidence for distinctive stress pathways. Brain Res 845, 60-67.
54. Gibson A, Hart SL, Shabib A (1980) Leucine-enkephalin and methionine-enkephalin produce opposing effects on plasma corticosterone levels in ether-stressed mice. Br J Pharmacol 70, 509-511.
55. Rivier C, Vale W (1983) Modulation of stress-induced ACTH release by corticotropin-releasing factor, catecholamines and vasopressin. Nature 305, 325-327. (Pubitemid 13010928)
56. Nakane T, Audhya T, Kanie N, Hollander CS (1985) Evidence for a role of endogenous corticotropin-releasing factor in cold, ether, immobilization, and traumatic stress. Proc Natl Acad Sci USA 82, 1247-1251.
57. Lim YW, Yoon SY, Choi JE, Kim SM, Lee HS, Choe H, Lee SC, Kim DH (2010) Maintained activity of glycogen syn-thase kinase-3beta despite of its phosphorylation at serine-9 in okadaic acid-induced neurodegenerative model. Biochem Biophys Res Commun 395, 207-212.
58. Goedert M, Jakes R, Qi Z, Wang JH, Cohen P (1995) Protein phosphatase 2A is the major enzyme in brain that dephospho-rylates tau protein phosphorylated by proline-directed protein kinases or cyclic AMP-dependent protein kinase. J Neurochem 65, 2804-2807.
59. Gong CX, Lidsky T, Wegiel J, Zuck L, Grundke-Iqbal I, Iqbal K (2000) Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J Biol Chem 275, 5535-5544.
60. Sontag E, Nunbhakdi-Craig V, Lee G, Bloom GS, Mumby MC (1996) Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron 17, 1201-1207.
61. Vogelsberg-Ragaglia V, Schuck T, Trojanowski JQ, Lee VM (2001) PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus. Exp Neurol 168, 402-412.
62. Tanimukai H, Grundke-Iqbal I, Iqbal K (2005) Up-regulation of inhibitors of protein phosphatase-2A in Alzheimer's disease. AmJ Pathol 166, 1761-1771. (Pubitemid 40734399)
63. Gong CX, Iqbal K (2008) Hyperphosphorylation of microtubule-associated protein tau: a promising therapeutic target for Alzheimer disease. CurrMed Chem 15, 2321-2328.
64. Bone I, Rosen M (2000) Alzheimer's disease and anaesthesia. Anaesthesia 55, 592-593.
65. Baranov D, Bickler PE, Crosby GJ, Culley DJ, Eckenhoff MF, Eckenhoff RG, Hogan KJ, Jevtovic-Todorovic V, Palotas A, Perouansky M, Planel E, Silverstein JH, Wei H, Whittington RA, Xie Z, Zuo Z; First International Workshop on Anesthetics and Alzheimer's Disease (2009) Consensus statement: First International Workshop on Anesthetics and Alzheimer's disease. AnesthAnalg 108, 1627-30.
66. Eckenhoff RG, Johansson JS, Wei H, Carnini A, Kang B, Wei W, Pidikiti R, Keller JM, Eckenhoff MF (2004) Inhaled anesthetic enhancement of amyloid-beta oligomerization and cytotoxicity. Anesthesiology 101, 703-709.
67. Bianchi SL, Tran T, Liu C, Lin S, Li Y, Keller JM, Ecken-hoff RG, Eckenhoff MF (2008) Brain and behavior changes in 12-month-old Tg2576 and nontransgenic mice exposed to anesthetics. Neurobiol Aging 29, 1002-1010.
68. Xie Z, Dong Y, Maeda U, Moir RD, Xia W, Culley DJ, Crosby G, Tanzi RE (2007) The inhalation anesthetic isoflurane induces a vicious cycle of apoptosis and amyloid beta-protein accumulation. J Neurosci 27, 1247-1254.
69. Fodale V, Quattrone D, Trecroci C, Caminiti V, Santamaria LB (2006) Alzheimer's disease and anaesthesia: implications for the central cholinergic system. Br J Anaesth 97, 445-452.
70. Wei H, Xie Z (2009) Anesthesia, calcium homeostasis and Alzheimer's disease. Curr Alzheimer Res 6, 30-35.
71. Zhang G, Dong Y, Zhang B, Ichinose F, Wu X, Culley DJ, Crosby G, Tanzi RE, Xie Z (2008) Isoflurane-induced caspase-3 activation is dependent on cytosolic calcium and can be attenuated by memantine. J Neurosci 28, 4551-4560.
72. Yang H, Liang G, Hawkins BJ, Madesh M, Pierwola A, Wei H (2008) Inhalational anesthetics induce cell damage by disruption of intracellular calcium homeostasis with different potencies. Anesthesiology 109, 243-250.
73. Ma D, Williamson P, Januszewski A, Nogaro MC, Hossain M, Ong LP, Shu Y, Franks NP, Maze M (2007) Xenon mitigates isofluraneinduced neuronal apoptosis in the developing rodent brain. Anesthesiology 106, 746-753.
74. Zhang G, Dong Y, Zhang B, Ichinose F, Wu X, Culley DJ, Crosby G, Tanzi RE, Xie Z (2009) Isoflurane-induced caspase-3 activation is dependent on cytosolic calcium and can be attenuated by memantine. J Neurosci 28, 4551-4560.
75. Wei H, Liang G, Yang H, Wang Q, Hawkins B, Madesh M, Wang S, Eckenhoff RG (2008) The common inhalational anesthetic isoflurane induces apoptosis via activation of inositol 1,4,5-trisphosphate receptors. Anesthesiology 108, 251-260.
76. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, Olney JW, Wozniak DF (2003) Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 23, 876-882.
77. Kuehn BM (2007) Anesthesia-Alzheimer disease link probed. JAMA 297, 1760.
78. Mandal PK, Pettegrew JW (2008) Abeta peptide interactions with isoflurane, propofol, thiopental and combined thiopental with halothane: a NMR study. Biochim Biophys Acta 1778, 2633-2639.
79. Mandal PK, Fodale V (2009) Isoflurane and desflurane at clinically relevant concentrations induce amyloid beta-peptide oligomerization: an NMR study. Biochem Biophys Res Com-mun 379, 716-720.
80. Mandal PK, Fodale V (2009) Smaller molecular-sized anaesthetics oligomerize Abeta peptide simulating Alzheimer's disease: a relevant issue. Eur J Anaesthesiol 26, 805-806.
81. Mandal PK, Simplaceanu V, Fodale V (2010) Intravenous anesthetic diazepam does not induce amyloid-beta peptide oligomerization but diazepam co-administered with halothane oligomerizes amyloid-beta peptide: an NMR study. J Alzh-eimers Dis 20, 127-34.
82. Williams AS (2009) Perianesthesia care of the Alzheimer's patient. J Perianesth Nurs 24, 343-347.
83. Bohnen NI, Warner MA, Kokmen E, Beard CM, Kurland LT (1994) Alzheimer's disease and cumulative exposure to anesthesia: a case-control study. J Am Geriatr Soc 42, 198-201. (Pubitemid 24057360)
84. Gasparini M, Vanacore N, Schiaffini C, Brusa L, Panella M, Talarico G, Bruno G, Meco G, Lenzi GL (2002) A case-control study on Alzheimer's disease and exposure to anesthesia. Neurol Sci 23, 11-14.
85. Avidan MS, Searleman AC, Storandt M, Barnett K, Vannucci A, Saager L, Xiong C, Grant EA, Kaiser D, Morris JC, Evers AS (2009) Long-term cognitive decline in older subjects was not attributable to noncardiac surgery or major illness. Anesthesiology 111, 964-970.