Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms

Journal of Neuroscience

Volumn 27, Issue 50, 2007, Pages 13635-13648

  Planel, Emmanuel ^a,d   Tatebayashi, Yoshitaka ^a,b   Miyasaka, Tomohiro ^a,c   Liu, Li ^d   Wang, Lili ^d   Herman, Mathieu ^d   Yu, W Haung ^d   Luchsinger, Jose A ^e   Wadzinski, Brian ^f   Duff, Karen E ^d   Takashima, Akihiko ^a  

^a INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d NewYork Presbyterian Hospital   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

amyloid precursor protein; Alzheimer's disease; CaMKII; Cdk5; Diabetes mellitus; GSK 3; Hypothermia; Insulin deficiency; JNK; Kinase; MAPK; PP2A; Serine threonine protein phosphatase; Streptozotocin; Tau hyperphosphorylation

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; INSULIN; PHOSPHOPROTEIN PHOSPHATASE 2A; STREPTOZOCIN; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HYPOTHERMIA; IN VIVO STUDY; INSULIN DEFICIENCY; MALE; MICROTUBULE; MOUSE; NERVE FIBER; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; STREPTOZOCIN DIABETES;

AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONS; BODY TEMPERATURE; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; EPITOPES; FEMALE; HIPPOCAMPUS; HYPOTHERMIA; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICROTUBULES; NEOCORTEX; NEUROPIL; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PHOSPHATASE 2; SOLUBILITY; STREPTOZOCIN; TAU PROTEINS; TIME FACTORS;

EID: 37249040432     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3949-07.2007     Document Type: Article

References (117)

1. Alonso AC, Zaidi T, Grundke-Iqbal I, Iqbal K (1994) Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc Natl Acad Sci USA 91:5562-5566.
2. Alonso AC, Zaidi T, Novak M, Grundke-Iqbal I, Iqbal K (2001) Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA 98:6923-6928.
3. Alonso AC, Mederlyova A, Novak M, Grundke-Iqbal I, Iqbal K (2004) Promotion of hyperphosphorylation by frontotemporal dementia tau mutations. J Biol Chem 279:34873-34881.
4. Andorfer C, Kress Y, Espinoza M, de Silva R, Tucker KL, Barde YA, Duff K, Davies P (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J Neurochem 86:582-590.
5. Arvanitakis Z, Wilson RS, Bienias JL, Evans DA, Bennett DA (2004) Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch Neurol 61:661-666.
6. Avila J, Lucas JJ, Perez M, Hernandez F (2004) Role of tau protein in both physiological and pathological conditions. Physiol Rev 84:361-384.
7. Baharians Z, Schonthal AH (1998) Autoregulation of protein phosphatase type 2A expression. J Biol Chem 273:19019-19024.
8. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, Seitelberger F, Grundke-Iqbal I, Iqbal K, Wisniewski HM (1989) Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 477:90-99.
9. Bhardwaj SK, Kaur G (1999) Effect of diabetes on calcium/calmodulin dependent protein kinase-II from rat brain. Neurochem Int 35:329-335.
10. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P (2006) Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 5:64-74.
11. Blurton-Jones M, Laferla FM (2006) Pathways by which Abeta facilitates tau pathology. Curr Alzheimer Res 3:437-448.
12. Braak E, Braak H, Mandelkow EM (1994) A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 87:554-567.
13. Burns M, Gaynor K, Olm V, Mercken M, LaFrancois J, Wang L, Mathews PM, Noble W, Matsuoka Y, Duff K (2003) Presenilin redistribution associated with aberrant cholesterol transport enhances β-amyloid production in vivo. J Neurosci 23:5645-5649.
14. Bussiere T, Hof PR, Mailliot C, Brown CD, Caillet-Boudin ML, Perl DP, Buee L, Delacourte A (1999) Phosphorylated serine422 on tau proteins is a pathological epitope found in several diseases with neurofibrillary degeneration. Acta Neuropathol (Berl) 97:221-230.
15. Chohan MO, Haque N, Alonso A, El-Akkad E, Grundke-Iqbal I, Grover A, Iqbal K (2005) Hyperphosphorylation-induced self assembly of murine tau: a comparison with human tau. J Neural Transm 112:1035-1047.
16. 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.
17. Cohen P (1989) The structure and regulation of protein phosphatases. Annu Rev Biochem 58:453-508.
18. Cole GM, Frautschy SA (2007) The role of insulin and neurotrophic factor signaling in brain aging and Alzheimer's Disease. Exp Gerontol 42:10-21.
19. Craft S, Peskind E, Schwartz MW, Schellenberg GD, Raskind M, Porte Jr D (1998) Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology 50:164-168.
20. Cuthbertson RA, Koulmanda M, Mandel TE (1988) Detrimental effect of chronic diabetes on growth and function of fetal islet isografts in mice. Transplantation 46:650-654.
21. DeFronzo RA (2004) Pathogenesis of type 2 diabetes mellitus. Med Clin North Am 88:787-835, ix.
22. Ebneth A, Drewes G, Mandelkow EM, Mandelkow E (1999) Phosphorylation of MAP2c and MAP4 by MARK kinases leads to the destabilization of microtubules in cells. Cell Motil Cytoskeleton 44:209-224.
23. Feinstein SC, Wilson L (2005) Inability of tau to properly regulate neuronal microtubule dynamics: a loss-of-function mechanism by which tau might mediate neuronal cell death. Biochim Biophys Acta 1739:268-279.
24. Festa A, Williams K, D'Agostino Jr R, Wagenknecht LE, Haffner SM (2006) The natural course of beta-cell function in nondiabetic and diabetic individuals: the Insulin Resistance Atherosclerosis Study. Diabetes 55:1114-1120.
25. Figlewicz DP, Dorsa D, Ikeda H, Stein LJ, Baskin D, Woods SC (1983) Brain insulin binding and contents are altered by streptozotocin treatment in rats. Diabetes 32:134a.
26. Finch CE, Cohen DM (1997) Aging, metabolism, and Alzheimer disease: review and hypotheses. Exp Neurol 143:82-102.
27. Frank HJ, Pardridge WM, Jankovic-Vokes T, Vinters HV, Morris WL (1986) Insulin binding to the blood-brain barrier in the streptozotocin diabetic rat. J Neurochem 47:405-411.
28. Frolich L, Blum-Degen D, Riederer P, Hoyer S (1999) A disturbance in the neuronal insulin receptor signal transduction in sporadic Alzheimer's disease. Ann NY Acad Sci 893:290-293.
29. Gasparini L, Netzer WJ, Greengard P, Xu H (2002) Does insulin dysfunction play a role in Alzheimer's disease? Trends Pharmacol Sci 23:288-293.
30. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
31. Goedert M, Cohen ES, Jakes R, Cohen P (1992) p42 MAP kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A1. Implications for Alzheimer's disease. FEBS Lett [Erratum (1992) 313:203] 312:95-99.
32. Goedert M, Jakes R, Crowther RA, Cohen P, Vanmechelen E, Vandermeeren M, Cras P (1994) Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein. Biochem J 301:871-877.
33. Goedert M, Jakes R, Vanmechelen E (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 189:167-169.
34. Gong CX, Singh TJ, Grundke-Iqbal I, Iqbal K (1993) Phosphoprotein phosphatase activities in Alzheimer disease brain. J Neurochem 61:921-927.
35. Gong CX, Grundke-Iqbal I, Damuni Z, Iqbal K (1994) Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and -2C and its implication in Alzheimer disease. FEBS Lett 341:94-98.
36. Gong CX, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K (1995) Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer disease brain. J Neurochem 65:732-738.
37. 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.
38. Greenberg SG, Davies P (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87:5827-5831.
39. Grunblatt E, Salkovic-Petrisic M, Osmanovic J, Riederer P, Hoyer S (2007) Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem 101:757-770.
40. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83:4913-4917.
41. Harman D (2002) Alzheimer's disease: role of aging in pathogenesis. Ann NY Acad Sci 959:384-395; discussion 463-465.
42. Hasegawa M, Jakes R, Crowther RA, Lee VM, Ihara Y, Goedert M (1996) Characterization of mAb AP422, a novel phosphorylation-dependent monoclonal antibody against tau protein. FEBS Lett 384:25-30.
43. Heininger K (2000) A unifying hypothesis of Alzheimer's disease. IV. Causation and sequence of events. Rev Neurosci 11:213-328.
44. Ho L, Qin W, Pompl PN, Xiang Z, Wang J, Zhao Z, Peng Y, Cambareri G, Rocher A, Mobbs CV, Hof PR, Pasinetti GM (2004) Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J 18:902-904.
45. Hong M, Lee VM (1997) Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J Biol Chem 272:19547-19553.
46. Howarth FC, Jacobson M, Naseer O, Adeghate E (2005) Short-term effects of streptozotocin-induced diabetes on the electrocardiogram, physical activity and body temperature in rats. Exp Physiol 90:237-245.
47. Hoyer S (2000) Brain glucose and energy metabolism abnormalities in sporadic Alzheimer disease. Causes and consequences: an update. Exp Gerontol 35:1363-1372.
48. Hoyer S (2002) The aging brain. Changes in the neuronal insulin/insulin receptor signal transduction cascade trigger late-onset sporadic Alzheimer disease (SAD). A mini-review. J Neural Transm 109:991-1002.
49. Hoyer S (2004) Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur J Pharmacol 490:115-125.
50. Ito M, Kondo Y, Nakatani A, Naruse A (1999) New model of progressive non-insulin-dependent diabetes mellitus in mice induced by streptozotocin. Biol Pharm Bull 22:988-989.
51. Itoh N, Arai H, Urakami K, Ishiguro K, Ohno H, Hampel H, Buerger K, Wiltfang J, Otto M, Kretzschmar H, Moeller HJ, Imagawa M, Kohno H, Nakashima K, Kuzuhara S, Sasaki H, Imahori K (2001) Large-scale, multicenter study of cerebrospinal fluid tau protein phosphorylated at serine 199 for the antemortem diagnosis of Alzheimer's disease. Ann Neurol 50:150-156.
52. Janke C, Beck M, Stahl T, Holzer M, Brauer K, Bigl V, Arendt T (1999) Phylogenetic diversity of the expression of the microtubule-associated protein tau: implications for neurodegenerative disorders. Brain Res Mol Brain Res 68:119-128.
53. Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417-439.
54. Kilgour RD, Williams PA (1996) Effects of diabetes and food deprivation on shivering activity during progressive hypothermia in the rat. Comp Biochem Physiol A Physiol 114:159-165.
55. Kilgour RD, Williams PA (1998) Diabetes affects blood pressure and heart rate responses during acute hypothermia. Acta Physiol Scand 162:27-32.
56. Lamberts SW, van den Beld AW, van der Lely AJ (1997) The endocrinology of aging. Science 278:419-424.
57. Leibson CL, Rocca WA, Hanson VA, Cha R, Kokmen E, O'Brien PC, Palumbo PJ (1997) Risk of dementia among persons with diabetes mellitus: a population-based cohort study. Am J Epidemiol 145:301-308.
58. Lesort M, Johnson GV (2000) Insulin-like growth factor-1 and insulin mediate transient site-selective increases in tau phosphorylation in primary cortical neurons. Neuroscience 99:305-316.
59. Lesort M, Jope RS, Johnson GV (1999) Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J Neurochem 72:576-584.
60. Lester-Coll N, Rivera EJ, Soscia SJ, Doiron K, Wands JR, de la Monte SM (2006) Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer's disease. J Alzheimers Dis 9:13-33.
61. Litersky JM, Johnson GV, Jakes R, Goedert M, Lee M, Seubert P (1996) Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356. Biochem J 316:655-660.
62. 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 USA 101:10804-10809.
63. Luchsinger JA, Mayeux R (2007) Adiposity and Alzheimer's disease. Curr Alzheimer Res 4:127-134.
64. Luchsinger JA, Tang MX, Stern Y, Shea S, Mayeux R (2001) Diabetes mellitus and risk of Alzheimer's disease and dementia with stroke in a multiethnic cohort. Am J Epidemiol 154:635-641.
65. Luchsinger JA, Reitz C, Honig LS, Tang MX, Shea S, Mayeux R (2005) Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 65:545-551.
66. Maas T, Eidenmuller J, Brandt R (2000) Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J Biol Chem 275:15733-15740.
67. Maccioni RB, Otth C, Concha II, Munoz JP (2001) The protein kinase Cdk5. Structural aspects, roles in neurogenesis and involvement in Alzheimer's pathology. Eur J Biochem 268:1518-1527.
68. Mathews PM, Jiang Y, Schmidt SD, Grbovic OM, Mercken M, Nixon RA (2002) Calpain activity regulates the cell surface distribution of amyloid precursor protein. Inhibition of clapains enhances endosomal generation of beta-cleaved C-terminal APP fragments. J Biol Chem 277:36415-36424.
69. Matsuo ES, Shin RW, Billingsley ML, Van deVoorde A, O'Connor M, Trojanowski JQ, Lee VM (1994) Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13:989-1002.
70. Maurage CA, Sergeant N, Ruchoux MM, Hauw JJ, Delacourte A (2003) Phosphorylated serine 199 of microtubule-associated protein tau is a neuronal epitope abundantly expressed in youth and an early marker of tau pathology. Acta Neuropathol (Berl) 105:89-97.
71. Meier-Ruge W, Bertoni-Freddari C (1996) The significance of glucose turnover in the brain in the pathogenetic mechanisms of Alzheimer's disease. Rev Neurosci 7:1-19.
72. Mi K, Johnson GV (2006) The role of tau phosphorylation in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res 3:449-463.
73. Mosconi L (2005) Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. FDG-PET studies in MCI and AD. Eur J Nucl Med Mol Imaging 32:486-510.
74. Neil HA, Dawson JA, Baker JE (1986) Risk of hypothermia in elderly patients with diabetes. Br Med J (Clin Res Ed) 293:416-418.
75. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Burns M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlijanian M, Lau LF, Duff K (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38:555-565.
76. Noble W, Planel E, Zehr C, Olm V, Meyerson J, Suleman F, Gaynor K, Wang L, LaFrancois J, Feinstein B, Burns M, Krishnamurthy P, Wen Y, Bhat R, Lewis J, Dickson D, Duff K (2005) Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci USA 102:6990-6995.
77. O'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007-4021.
78. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM (1999) Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 53:1937-1942.
79. Pacold ST, Blackard WG (1979) Central nervous system insulin receptors in normal and diabetic rats. Endocrinology 105:1452-1457.
80. 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.
81. Pezzino V, Costantino A, Russo P, Gullo D, Papa V (1996) Insulin receptor content in tissues of normal and diabetic rats measured by radioimmunoassay. J Endocrinol Invest 19:593-597.
82. Planel E, Yasutake K, Fujita SC, Ishiguro K (2001) Inhibition of protein phosphatase 2A overrides Tau protein kinase I/glycogen synthase kinase 3beta and Cyclin-dependant kinase 5 inhibition and results in tau hyperphosphorylation in the hippocampus of starved mouse. J Biol Chem 276:34298-34306.
83. Planel E, Sun X, Takashima A (2002) Role of GSK-3 beta in Alzheimer's disease pathology. Drug Development Res 56:491-510.
84. Planel E, Miyasaka T, Launey T, Chui DH, Tanemura K, Sato S, Murayama O, Ishiguro K, Tatebayashi Y, Takashima A (2004) Alterations in glucose metabolism induce hypothermia leading to tau hyperphosphorylation through differential inhibition of kinase and phosphatase activities: implications for Alzheimer's disease. J Neurosci 24:2401-2411.
85. Planel E, Richter KEG, Nolan CE, Finley JE, Liu L, Wen Y, Krishnamurthy P, Herman M, Wang L, Schachter JB, Nelson RB, Lau L-F, Duff KE (2007) Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia. J Neurosci 27:3090-3097.
86. Price NE, Wadzinski B, Mumby MC (1999) An anchoring factor targets protein phosphatase 2A to brain microtubules. Brain Res Mol Brain Res 73:68-77.
87. Rivera EJ, Goldin A, Fulmer N, Tavares R, Wands JR, de la Monte SM (2005) Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J Alzheimers Dis 8:247-268.
88. Salehi A, Swaab DF (1999) Diminished neuronal metabolic activity in Alzheimer's disease. Review article. J Neural Transm 106:955-986.
89. Sato S, Tatebayashi Y, Akagi T, Chui DH, Murayama M, Miyasaka T, Planel E, Tanemura K, Sun X, Hashikawa T, Yoshioka K, Ishiguro K, Takashima A (2002) Aberrant tau phosphorylation by glycogen synthase kinase-3beta and JNK3 induces oligomeric tau fibrils in COS-7 cells. J Biol Chem 277:42060-42065.
90. Schechter R, Beju D, Miller KE (2005) The effect of insulin deficiency on tau and neurofilament in the insulin knockout mouse. Biochem Biophys Res Commun 334:979-986.
91. Schmidt SD, Nixon RA, Mathews PM (2005) ELISA method for measurement of amyloid-beta levels. Methods Mol Biol 299:279-297.
92. Schnedl WJ, Ferber S, Johnson JH, Newgard CB (1994) STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 43:1326-1333.
93. Schubert M, Brazil DP, Burks DJ, Kushner JA, Ye J, Flint CL, Farhang-Fallah J, Dikkes P, Warot XM, Rio C, Corfas G, White MF (2003) Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J Neurosci 23:7084-7092.
94. Schubert M, Gautam D, Surjo D, Ueki K, Baudler S, Schubert D, Kondo T, Alber J, Galldiks N, Kustermann E, Arndt S, Jacobs AH, Krone W, Kahn CR, Bruning JC (2004) Role for neuronal insulin resistance in neurodegenerative diseases. Proc Natl Acad Sci USA 101:3100-3105.
95. Scott AR, Bennett T, Macdonald IA (1987) Diabetes mellitus and thermoregulation. Can J Physiol Pharmacol 65:1365-1376.
96. Sechi LA, Griffin CA, Grady EF, Grunfeld C, Kalinyak JE, Schambelan M (1992) Tissue-specific regulation of insulin receptor mRNA levels in rats with STZ-induced diabetes mellitus. Diabetes 41:1113-1118.
97. Seydoux J, Chinet A, Schneider-Picard G, Bas S, Imesch E, Assimacopoulos-Jeannet F, Giacobino JP, Girardier L (1983) Brown adipose tissue metabolism in streptozotocin-diabetic rats. Endocrinology 113:604-610.
98. Shalaby TH, Yousef MK, Dupre RK (1989) Thermoregulatory responses of diabetic rats. Comp Biochem Physiol A 94:153-157.
99. Simpson IA, Appel NM, Hokari M, Oki J, Holman GD, Maher F, Koehler-Stec EM, Vannucci SJ, Smith QR (1999) Blood-brain barrier glucose transporter: effects of hypo- and hyperglycemia revisited. J Neurochem 72:238-247.
100. Sironi JJ, Yen SH, Gondal JA, Wu Q, Grundke-Iqbal I, Iqbal K (1998) Ser-262 in human recombinant tau protein is a markedly more favorable site for phosphorylation by CaMKII than PKA or PhK. FEBS Lett 436:471-475.
101. Smith OL, Davidson SB (1982) Shivering thermogenesis and glucose uptake by muscles of normal or diabetic rats. Am J Physiol 242:R109-R115.
102. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White III CL, Mumby MC, Bloom GS (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 274:25490-25498.
103. Strack S, Zaucha JA, Ebner FF, Colbran RJ, Wadzinski BE (1998) Brain protein phosphatase 2A: developmental regulation and distinct cellular and subcellular localization by B subunits. J Comp Neurol 392:515-527.
104. Su JH, Cummings BJ, Cotman CW (1993) Identification and distribution of axonal dystrophic neurites in Alzheimer's disease. Brain Res 625:228-237.
105. Su JH, Cummings BJ, Cotman CW (1994) Early phosphorylation of tau in Alzheimer's disease occurs at Ser-202 and is preferentially located within neurites. NeuroReport 5:2358-2362.
106. Szendrei GI, Lee VM, Otvos Jr L (1993) Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location. J Neurosci Res 34:243-249.
107. Tanimukai H, Grundke-Iqbal I, Iqbal K (2005) Up-regulation of inhibitors of protein phosphatase-2A in Alzheimer's disease. Am J Pathol 166:1761-1771.
108. Tian Q, Wang J (2002) Role of serine/threonine protein phosphatase in Alzheimer's disease. Neurosignals 11:262-269.
109. Tjalve H (1983) Streptozotocin: distribution, metabolism and mechanisms of action. Uppsala J Med Sci Suppl 39:145-157.
110. Trojanowski JQ, Lee VM (1994) Paired helical filament tau in Alzheimer's disease. The kinase connection. Am J Pathol 144:449-453.
111. 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.
112. Wang JZ, Grundke-Iqbal I, Iqbal K (2007) Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 25:59-68.
113. Watson GS, Craft S (2003) The role of insulin resistance in the pathogenesis of Alzheimer's disease: implications for treatment. CNS Drugs 17:27-45.
114. Weber C, Pernis B, Ting W, Rosenkrantz K, Reemtsma K (1984) Murine streptozotocin diabetes: influences of the major histocompatibility complex, genetic background and blood transfusion. Diabetologia 27 [Suppl]:160-162.
115. Williams SK, Howarth NL, Devenny JJ, Bitensky MW (1982) Structural and functional consequences of increased tubulin glycosylation in diabetes mellitus. Proc Natl Acad Sci USA 79:6546-6550.
116. Zhao YM, Pei JJ, Ji ZJ, Zhao ZW, Qian YY, Sheng SL (2003) Effect of amyloid precursor protein 17mer peptide on microtubule structure and tau protein hyperphosphorylation in hippocampal neurons of experimental diabetic mice. NeuroReport 14:61-66.
117. Zhu X, Lee HG, Raina AK, Perry G, Smith MA (2002) The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11:270-281.