Hyperglycemia-induced tau cleavage in vitro and in vivo: A possible link between diabetes and alzheimer's disease

Journal of Alzheimer's Disease

Volumn 34, Issue 3, 2013, Pages 727-739

  Kim, Bhumsoo ^a   Backus, Carey ^a   Oh, Sangsu ^a   Feldman, Eva L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Alzheimer's disease; diabetes; hyperglycemia; tau

Indexed keywords

CASPASE 3; GLUCOSE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BRAIN CELL; CONCENTRATION (PARAMETERS); DIABETIC PATIENT; EMBRYO; ENZYME ACTIVATION; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; RAT;

EID: 84876389108     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-121669     Document Type: Article

References (73)

1. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: Prevalence estimates using the 2000 census. Arch Neurol 60, 1119-1122. (Pubitemid 36975801)
2. Feldman EL (2003) Oxidative stress and diabetic neuropathy: A new understanding of an old problem. J Clin Invest 111, 431-433. (Pubitemid 36227996)
3. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, BretelerMM(1999) Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 53, 1937-1942.
4. Peila R, Rodriguez BL, Launer LJ (2002) Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: The Honolulu-Asia Aging Study. Diabetes 51, 1256-1262. (Pubitemid 34438377)
5. Biessels GJ, Kappelle LJ (2005) Increased risk of Alzheimer's disease in Type II diabetes: Insulin resistance of the brain or insulin-induced amyloid pathology? Biochem Soc Trans 33, 1041-1044. (Pubitemid 41659109)
6. Cox DJ, Kovatchev BP, Gonder-Frederick LA, Summers KH, McCall A, Grimm KJ, Clarke WL (2005) Relationships between hyperglycemia and cognitive performance among adults with type 1 and type 2 diabetes. Diabetes Care 28, 71-77. (Pubitemid 40095785)
7. Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP (2005) The effects of type 1 diabetes on cognitive performance: A meta-analysis. Diabetes Care 28, 726-735. (Pubitemid 40315341)
8. Janson J, Laedtke T, Parisi JE, O'Brien P, Petersen RC, Butler PC (2004) Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53, 474-481. (Pubitemid 38174565)
9. Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117, 5721-5729. (Pubitemid 40123939)
10. Martin L, Latypova X, Terro F (2011) Post-translational modifications of tau protein: Implications for Alzheimer's disease. Neurochem Int 58, 458-471.
11. Cotman CW, Poon WW, Rissman RA, Blurton-Jones M (2005) The role of caspase cleavage of tau in Alzheimer disease neuropathology. J Neuropathol Exp Neurol 64, 104-112. (Pubitemid 40349308)
12. Zilka N, Kovacech B, Barath P, Kontsekova E, Novak M (2012) The self-perpetuating tau truncation circle. Biochem Soc Trans 40, 681-686.
13. Wang YP, Biernat J, Pickhardt M, Mandelkow E, Mandelkow EM (2007) Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proc Natl Acad Sci U S A 104, 10252-10257. (Pubitemid 47175295)
14. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, Lu M, FuY, Garcia-Sierra F, LaPointe N, Miller R, Berry RW, Binder LI, Cryns VL (2003) Caspase cleavage of tau: Linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci U S A 100, 10032-10037. (Pubitemid 37087063)
15. Yin H, Kuret J (2006) C-terminal truncation modulates both nucleation and extension phases of tau fibrillization. FEBS Lett 580, 211-215. (Pubitemid 43005338)
16. Zilka N, Filipcik P, Koson P, Fialova L, Skrabana R, Zilkova M, Rolkova G, Kontsekova E, NovakM(2006) Truncated tau from sporadic Alzheimer's disease suffices to drive neurofibrillary degeneration in vivo. FEBS Lett 580, 3582-3588. (Pubitemid 43902790)
17. Chong YH, Shin YJ, Lee EO, Kayed R, Glabe CG, Tenner AJ (2006) ERK1/2 activation mediates Abeta oligomer-induced neurotoxicity via caspase-3 activation and tau cleavage in rat organotypic hippocampal slice cultures. J Biol Chem 281, 20315-20325. (Pubitemid 44065806)
18. Oddo S (2008) The ubiquitin-proteasome system in Alzheimer's disease. J Cell Mol Med 12, 363-373. (Pubitemid 351555121)
19. ParkSY, Tournell C, Sinjoanu RC, FerreiraA(2007) Caspase-3- and calpain-mediated tau cleavage are differentially prevented by estrogen and testosterone in beta-amyloidtreated hippocampal neurons. Neuroscience 144, 119-127. (Pubitemid 44841997)
20. Reinecke JB, DeVos SL, McGrath JP, Shepard AM, Goncharoff DK, Tait DN, Fleming SR, Vincent MP, Steinhilb ML (2011) Implicating calpain in tau-mediated toxicity in vivo. PLoS ONE 6, e23865.
21. Figueroa-Romero C, Sadidi M, Feldman EL (2008) Mechanisms of disease: The oxidative stress theory of diabetic neuropathy. Rev Endocr Metab Disord 9, 301-314.
22. Sullivan KA, Hayes JM, Wiggin TD, Backus C, Su Oh S, Lentz SI, Brosius F 3rd, Feldman EL (2007) Mouse models of diabetic neuropathy. Neurobiol Dis 28, 276-285. (Pubitemid 350116599)
23. Vincent AM, Edwards JL, Sadidi M, Feldman EL (2008) The antioxidant response as a drug target in diabetic neuropathy. Curr Drug Targets 9, 94-100.
24. Kim B, Backus C, Oh S, Hayes JM, Feldman EL (2009) Increased tau phosphorylation and cleavage in mouse models of type 1 and type 2 diabetes. Endocrinology 150, 5294-5301.
25. Wiggin TD, Kretzler M, Pennathur S, Sullivan KA, Brosius FC, Feldman EL (2008) Rosiglitazone treatment reduces diabetic neuropathy in streptozotocin-treated DBA/2J mice. Endocrinology 149, 4928-4937.
26. Vincent AM, Russell JW, Sullivan KA, Backus C, Hayes JM, McLean LL, Feldman EL (2007) SOD2 protects neurons from injury in cell culture and animal models of diabetic neuropathy. Exp Neurol 208, 216-227. (Pubitemid 350101499)
27. Leventhal PS, Shelden EA, Kim B, Feldman EL (1997) Tyrosine phosphorylation of paxillin and focal adhesion kinase during insulin-like growth factor-I-stimulated lamellipodial advance. J Biol Chem 272, 5214-5218. (Pubitemid 27090081)
28. van Engeland M, Nieland LJ, Ramaekers FC, Schutte B, Reutelingsperger CP (1998) Annexin V-affinity assay: A review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1-9. (Pubitemid 28050057)
29. Andree HA, Reutelingsperger CP, Hauptmann R, Hemker HC, Hermens WT, Willems GM (1990) Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J Biol Chem 265, 4923-4928.
30. Leinninger GM, Backus C, Sastry AM, Yi YB, Wang CW, Feldman EL (2006) Mitochondria in DRG neurons undergo hyperglycemic mediated injury through Bim, Bax and the fission protein Drp1. Neurobiol Dis 23, 11-22. (Pubitemid 44192383)
31. Russell JW, Berent-Spillson A, Vincent AM, Freimann CL, Sullivan KA, Feldman EL (2008) Oxidative injury and neuropathy in diabetes and impaired glucose tolerance. Neurobiol Dis 30, 420-429.
32. Li ZG, ZhangW, Sima AA (2007) Alzheimer-like changes in rat models of spontaneous diabetes. Diabetes 56, 1817-1824. (Pubitemid 47025451)
33. Clodfelder-Miller BJ, Zmijewska AA, Johnson GV, Jope RS (2006) Tau is hyperphosphorylated at multiple sites in mouse brain in vivo after streptozotocin-induced insulin deficiency. Diabetes 55, 3320-3325. (Pubitemid 44923588)
34. Planel E, Tatebayashi Y, Miyasaka T, Liu L, Wang L, Herman M, Yu WH, Luchsinger JA, Wadzinski B, Duff KE, Takashima A (2007) Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J Neurosci 27, 13635-13648. (Pubitemid 350278272)
35. Krieglstein K (2006) Cell death in the nervous system. Adv Exp Med Biol 557, 1-10.
36. Vincent AM, McLean LL, Backus C, Feldman EL (2005) Short-term hyperglycemia produces oxidative damage and apoptosis in neurons. FASEB J 19, 638-640. (Pubitemid 40471270)
37. Nelson TJ, AlkonDL(2007) Protection against beta-amyloidinduced apoptosis by peptides interacting with beta-amyloid. J Biol Chem 282, 31238-31249. (Pubitemid 350044852)
38. CorsettiV, Amadoro G, Gentile A, Capsoni S, CiottiMT, CencioniMT, Atlante A, Canu N, Rohn TT, Cattaneo A, Calissano P (2008) Identification of a caspase-derived N-terminal tau fragment in cellular and animal Alzheimer's disease models. Mol Cell Neurosci 38, 381-392.
39. Yoon S, Choi J, Huh JW, Hwang O, Kim D (2006) Calpain activation in okadaic-acid-induced neurodegeneration. Neuroreport 17, 689-692. (Pubitemid 43947924)
40. WenY,Yang S, Liu R, SimpkinsJW(2004) Transient cerebral ischemia induces site-specific hyperphosphorylation of tau protein. Brain Res 1022, 30-38. (Pubitemid 39194981)
41. Rissman RA, Poon WW, Blurton-Jones M, Oddo S, Torp R, Vitek MP, LaFerla FM, Rohn TT, Cotman CW (2004) Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J Clin Invest 114, 121-130. (Pubitemid 39071651)
42. Mondragon-Rodriguez S, Basurto-Islas G, Santa-Maria I, Mena R, Binder LI, Avila J, Smith MA, Perry G, Garcia- Sierra F (2008) Cleavage and conformational changes of tau protein follow phosphorylation during Alzheimer's disease. Int J Exp Pathol 89, 81-90. (Pubitemid 351365186)
43. Rametti A, Esclaire F, Yardin C, Terro F (2004) Linking alterations in tau phosphorylation and cleavage during neuronal apoptosis. J Biol Chem 279, 54518-54528. (Pubitemid 40053193)
44. Lee KY, Koh SH, Noh MY, Kim SH, Lee YJ (2008) Phosphatidylinositol-3- kinase activation blocks amyloid beta-induced neurotoxicity. Toxicology 243, 43-50. (Pubitemid 350250958)
45. Chen X, Huang T, Zhang J, Song J, Chen L, Zhu Y (2008) Involvement of calpain and p25 of CDK5 pathway in ginsenoside Rb1's attenuation of beta-amyloid peptide(25-35)-induced tau hyperphosphorylation in cortical neurons. Brain Res 1200C, 99-106.
46. Sorrentino G, Bonavita V (2007) Neurodegeneration and Alzheimer's disease: The lesson from tauopathies. Neurol Sci 28, 63-71. (Pubitemid 46681660)
47. ChunW, Johnson GV (2007) The role of tau phosphorylation and cleavage in neuronal cell death. Front Biosci 12, 733-756. (Pubitemid 46860209)
48. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M, McGowan E (2001) Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293, 1487-1491. (Pubitemid 32801551)
49. Gotz J, Chen F, van Dorpe J, Nitsch RM (2001) Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 293, 1491-1495. (Pubitemid 32807681)
50. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24, 1063-1070. (Pubitemid 37487883)
51. Quintanilla RA, Dolan PJ, Jin YN, Johnson GV (2012) Truncated tau and Abeta cooperatively impair mitochondria in primary neurons. Neurobiol Aging 33, 619 e625-e635.
52. Canu N, Dus L, Barbato C, Ciotti MT, Brancolini C, Rinaldi AM, Novak M, Cattaneo A, Bradbury A, Calissano P (1998) Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis. J Neurosci 18, 7061-7074. (Pubitemid 28425794)
53. Garcia-Sierra F, Mondragon-Rodriguez S, Basurto-Islas G (2008) Truncation of tau protein and its pathological significance in Alzheimer's disease. J Alzheimers Dis 14, 401-409.
54. McMillan PJ, Kraemer BC, Robinson L, Leverenz JB, Raskind M, Schellenberg G (2011) Truncation of tau at E391 promotes early pathologic changes in transgenic mice. J Neuropathol Exp Neurol 70, 1006-1019.
55. Park SY, Ferreira A (2005) The generation of a 17 kDa neurotoxic fragment: An alternative mechanism by which tau mediates beta-amyloid-induced neurodegeneration. J Neurosci 25, 5365-5375. (Pubitemid 40770916)
56. de Calignon A, Fox LM, Pitstick R, Carlson GA, Bacskai BJ, Spires-Jones TL, Hyman BT (2010) Caspase activation precedes and leads to tangles. Nature 464, 1201-1204.
57. Chung CW, Song YH, Kim IK, Yoon WJ, Ryu BR, Jo DG, Woo HN, Kwon YK, Kim HH, Gwag BJ, Mook-Jung IH, Jung YK (2001) Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol Dis 8, 162-172.
58. Gamblin TC, Berry RW, Binder LI (2003) Tau polymerization: Role of the amino terminus. Biochemistry 42, 2252-2257. (Pubitemid 36258700)
59. Saito K, Elce JS, Hamos JE, Nixon RA (1993) Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: A potential molecular basis for neuronal degeneration. Proc Natl Acad SciUS A 90, 2628-2632. (Pubitemid 23113469)
60. Adamec E, Mohan P, Vonsattel JP, Nixon RA (2002) Calpain activation in neurodegenerative diseases: Confocal immunofluorescence study with antibodies specifically recognizing the active form of calpain 2. Acta Neuropathol 104, 92-104. (Pubitemid 36075364)
61. David DC, Layfield R, Serpell L, Narain Y, Goedert M, SpillantiniMG(2002) Proteasomal degradation of tau protein. J Neurochem 83, 176-185.
62. Feuillette S, Blard O, Lecourtois M, Frebourg T, Campion D, Dumanchin C (2005) Tau is not normally degraded by the proteasome. J Neurosci Res 80, 400-405. (Pubitemid 40780828)
63. Freude S, Plum L, Schnitker J, Leeser U, UdelhovenM, Krone W, Bruning JC, Schubert M (2005) Peripheral hyperinsulinemia promotes tau phosphorylation in vivo. Diabetes 54, 3343-3348. (Pubitemid 43334322)
64. Bruce KD, Hanson MA (2010) The developmental origins, mechanisms, and implications of metabolic syndrome. J Nutr 140, 648-652.
65. Petersen KF, Shulman GI (2006) Etiology of insulin resistance. Am J Med 119, S10-S16.
66. Taubes G (2009) Insulin resistance Prosperity's plague. Science 325, 256-260.
67. Kim B, Feldman EL (2012) Insulin resistance in the nervous system. Trends Endocrinol Metab 23, 133-141.
68. Kim B, McLean LL, Philip SS, Feldman EL (2011) Hyperinsulinemia induces insulin resistance in dorsal root ganglion neurons. Endocrinology 152, 3638-3647.
69. Kim B, Sullivan KA, Backus C, Feldman EL (2011) Cortical neurons develop insulin resistance and blunted Akt signaling: A potential mechanism contributing to enhanced ischemic injury in diabetes. Antioxid Redox Signal 14, 1829-1839.
70. Hay N (2011) Akt isoforms and glucose homeostasis - the leptin connection. Trends Endocrinol Metab 22, 66-73.
71. Zdychova J, Komers R (2005) Emerging role of Akt kinase/protein kinase B signaling in pathophysiology of diabetes and its complications. Physiol Res 54, 1-16. (Pubitemid 40363649)
72. Son SM, Song H, Byun J, Park KS, Jang HC, Park YJ, Mook-Jung I (2012) Accumulation of autophagosomes contributes to enhanced amyloidogenic APP processing under insulinresistant conditions. Autophagy 8, 1842-1844.
73. Son SM, Song H, Byun J, Park KS, Jang HC, Park YJ, Mook- Jung I (2012) Altered APP processing in insulin-resistant conditions is mediated by autophagosome accumulation via the inhibition of mammalian target of rapamycin pathway. Diabetes 61, 3126-3138.