hSOD1 Promotes Tau Phosphorylation and Toxicity in the Drosophila Model

Journal of Alzheimer's Disease

Volumn 45, Issue 1, 2015, Pages 235-244

  Huang, Yunpeng ^a   Wu, Zhihao ^a   Zhou, Bing ^a,b  

^a TSINGHUA UNIVERSITY   (China)

^b BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

Drosophila; hSOD1; hyperphosphorylation; tau

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; TAU PROTEIN; DROSOPHILA PROTEIN; SUPEROXIDE DISMUTASE;

ARTICLE; CONTROLLED STUDY; FRUIT FLY MODEL; IMMUNOBLOTTING; LIFESPAN; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; AGE; ANIMAL; DISEASE MODEL; DROSOPHILA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LOCOMOTION; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; TAUOPATHY; TRANSGENIC ANIMAL;

AGE FACTORS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; HUMANS; LOCOMOTION; MUTATION; PHOSPHORYLATION; SUPEROXIDE DISMUTASE; TAU PROTEINS; TAUOPATHIES;

EID: 84924162125     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-141608     Document Type: Article

References (47)

1. Drechsel DN, Hyman A, Cobb MH, Kirschner M (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3, 1141-1154.
2. Gustke N, Trinczek B, Biernat J, Mandelkow E-M, Mandelkow E (1994) Domains of tau protein and interactions with microtubules. Biochemistry (Mosc) 33, 9511-9522.
3. Buée L, Bussiere T, Buée-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33, 95-130.
4. Lindwall G, Cole RD (1984) Phosphorylation affects the ability of tau protein to promote microtubule assembly. J Biol Chem 259, 5301-5305.
5. Biernat J, Gustke N, Drewes G, Mandelkow E, Mandelkow E (1993) Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: Distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163.
6. Timm T, Matenia D, Li X-Y, Griesshaber B, Mandelkow E-M (2006) Signaling fromMARKto tau: Regulation, cytoskeletal crosstalk, and pathological phosphorylation. Neurodegener Dis 3, 207-217.
7. Ploia C, Antoniou X, Sclip A, Grande V, Cardinetti D, Colombo A, Canu N, Benussi L, Ghidoni R, Forloni G (2011) JNK plays a key role in tau hyperphosphorylation in Alzheimer's disease models. J Alzheimers Dis 26, 315-329.
8. Wang D, Fu Q, Zhou Y, Xu B, Shi Q, Igwe B, Matt L, Hell JW, WiselyEV, Oddo S (2013) β2 adrenergic receptor, protein kinase A (PKA) and c-Jun N-terminal kinase (JNK) signaling pathways mediate tau pathology in Alzheimer disease models. J Biol Chem 288, 10298-10307.
9. Mondragón-Rodr?guez S, Perry G, Luna-Münoz J, Acevedo-Aquino M, Williams S (2013) Phosphorylation of tau protein at sites Ser396-404 is one of the earliest events in Alzheimer's disease and Down syndrome. Neuropathol Appl Neurobiol 40, 121-135.
10. Shankar SK, Yanagihara R, Garruto RM, Grundke-Iqbal I, Kosik KS, Gajdusek DC (1989) Immunocytochemical characterization of neurofibrillary tangles in amyotrophic lateral sclerosis and parkinsonism-dementia of guam. Ann Neurol 25, 146-151.
11. Delacourte A, Defossez A (1986) Biochemical characterization of an immune serum which specifically marks neurons in neurofibrillary degeneration in Alzheimer's disease. C R Acad Sci III 303, 439-444.
12. Grundke-Iqbal I, Iqbal K, Tung Y-C, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A 83, 4913-4917.
13. KoSIK, Joachim KS, Selkoe CL, DJ (1986) Microtubuleassociated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci U S A 83, 4044-4048.
14. Joachim CL, Morris JH, Kosik KS, Selkoe DJ (1987) Tau antisera recognize neurofibrillary tangles in a range of neurodegenerative disorders. Ann Neurol 22, 514-520.
15. Kadota M, Nishigaki R, Wang C, Toda T, Shirayoshi Y, Inoue T, Gojobori T, Ikeo K, Rogers M, Oshimura M (2004) Proteomic signatures and aberrations of mouse embryonic stem cells containing a single human chromosome 21 in neuronal differentiation: An in vitro model of down syndrome. Neuroscience 129, 325-335.
16. Epstein CJ, Avraham KB, Lovett M, Smith S, Elroy-Stein O, Rotman G, Bry C, Groner Y (1987) Transgenic mice with increased Cu/Zn-superoxide dismutase activity: Animal model of dosage effects in Down syndrome. Proc Natl Acad Sci U S A 84, 8044-8048.
17. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng H-X (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62.
18. Cudkowicz M, McKenna-Yasek D, Sapp P, Chin W, Geller B, Hayden D, Schoenfeld D, Hosler B, Horvitz H, Brown R (1997) Epidemiology of mutations in superoxide dismutase in amyotrophic lateal sclerosis. Ann Neurol 41, 210-221.
19. Sago H, Carlson EJ, Smith DJ, Rubin EM, Crnic LS, Huang T-T, Epstein CJ (2000) Genetic dissection of region associated with behavioral abnormalities in mouse models for Down syndrome. Pediatr Res 48, 606-613.
20. Gahtan E, Auerbach J, Groner Y, Segal M (1998) Reversible impairment of long-term potentiation in transgenic Cu/Zn-SOD mice. Eur J Neurosci 10, 538-544.
21. Jaarsma D, Haasdijk ED, Grashorn J, Hawkins R, Van Duijn W, Verspaget HW, London J, Holstege JC (2000) Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 7, 623-643.
22. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2, 806-819.
23. Nishimura I, Yang Y, Lu B (2004) PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116, 671-682.
24. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB (2001) Tauopathy in Drosophila: Neurodegeneration without neurofibrillary tangles. Science 293, 711-714.
25. Steinhilb ML, Dias-Santagata D, Fulga TA, Felch DL, Feany MB (2007) Tau phosphorylation sites work in concert to promote neurotoxicity in vivo. Mol Biol Cell 18, 5060-5068.
26. Zhang B, Higuchi M, Yoshiyama Y, Ishihara T, Forman MS, Martinez D, Joyce S, Trojanowski JQ, Lee VM-Y (2004) Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J Neurosci 24, 4657-4667.
27. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Anderton BH (2000) Phosphorylation sites on tau identified by nanoelectrospray mass spectrometry. J Neurochem 74, 1587-1595.
28. Bond D, Foley E (2009) A quantitative RNAi screen for JNK modifiers identifies Pvr as a novel regulator of Drosophila immune signaling. PLoS Pathogens 5, e1000655.
29. Jarvis BW, Schaefer EM, Miller DT (1997) Detection of JNK, p38 and MAPK enzyme activation using anti-dualphosphopeptide antibodies: Coordinated signaling of the extracellular signal-regulated protein kinase (ERK) superfamily. Promega Notes Mag 63, 2-7.
30. KhokhlatchevA, Xu S, English J, Wu P, Schaefer E, CobbMH (1997) Reconstitution of mitogen-activated protein kinase phosphorylation cascades in Bacteria efficient synthesis of active protein kinase. J Biol Chem 272, 11057-11062.
31. Xiong H, Zheng C, Wang J, Song J, Zhao G, Shen H, Deng Y (2013) The neuroprotection of Liraglutide on Alzheimerlike learning and memory impairment by modulating the hyperphosphorylation of tau and neurofilament proteins and insulin signaling pathways in mice. J Alzheimers Dis 37, 623-635.
32. Lénért N, Szegedi V, Juhész G, Kasztner A, Horváth J, Bereczki E, Tóth ME, Penke B, Sántha M (2012) Increased tau phosphorylation and impaired presynaptic function in hypertriglyceridemic ApoB-100 transgenic mice. PloS One 7, e46007.
33. Ryoo S-R, Jeong HK, Radnaabazar C, Yoo J-J, Cho H-J, Lee H-W, Kim I-S, Cheon Y-H, Ahn YS, Chung S-H (2007) DYRK1A-mediated hyperphosphorylation of tau. A functional link between Down syndrome and Alzheimer disease. J Biol Chem 282, 34850-34857.
34. Cárdenas AM, Ardiles AO, Barraza N, Baéz-Matus X, Caviedes P (2012) Role of tau protein in neuronal damage in Alzheimer's disease and Down syndrome. Arch Med Res 43, 645-654.
35. Hanger D, Brion JP, Gallo J, Cairns N, Luthert P, Anderton B (1991) Tau in Alzheimer's disease and Down's syndrome is insoluble and abnormally phosphorylated. Biochem J 275, 99-104.
36. Ball M, Nuttall K (1980) Neurofibrillary tangles, granulovacuolar degeneration, and neuron loss in Down syndrome: Quantitative comparison with Alzheimer dementia. Ann Neurol 7, 462-465.
37. Juneja T, Pericak-Vance MA, Laing NG, Dave S, Siddique T (1997) Prognosis in familial amyotrophic lateral sclerosis progression and survival in patients with Glu100gly and Ala4val mutations in Cu, Zn superoxide dismutase. Neurology 48, 55-57.
38. Saeed M, Yang Y, Deng H, HungW, Siddique N, Dellefave L, Gellera C, Andersen PM, Siddique T (2009) Age and founder effect of SOD1 A4V mutation causing ALS. Neurology 72, 1634-1639.
39. Oyanagi K, Makifuchi T, Ohtoh T, Chen KM, Van Der Schaaf T, Gajdusek DC, Chase TN, Ikuta F (1994) Amyotrophic lateral sclerosis of Guam: The nature of the neuropathological findings. Acta Neuropathol (Berl) 88, 405-412.
40. Wang X, Blanchard J, Grundke-Iqbal I, Wegiel J, Deng H-X, Siddique T, Iqbal K (2014) Alzheimer disease and amyotrophic lateral sclerosis: An etiopathogenic connection. Acta Neuropathol 127, 243-256.
41. Strong M, YangW, StrongW, Leystra-Lantz C, Jaffe H, Pant H (2006) Tau protein hyperphosphorylation in sporadic ALS with cognitive impairment. Neurology 66, 1770-1771.
42. Lomoio S, Scherini E, Necchi D (2009) β-Amyloid overload does not directly correlate with SAPK/JNK activation and tau protein phosphorylation in the cerebellar cortex of Ts65Dn mice. Brain Res 1297, 198-206.
43. Shen C, Chen Y, Liu H, Zhang K, Zhang T, Lin A, Jing N (2008) Hydrogen peroxide promotes Aβ production through JNK-dependent activation of β-secretase. J Biol Chem 283, 17721-17730.
44. Inanami O, Takahashi K, Yoshito A, Kuwabara M (1999) Hydrogen peroxide-induced activation of SAPK/JNK regulated by phosphatidylinositol 3-kinase in Chinese hamster V79 cells. Antioxid Redox Signal 1, 113-121.
45. Krishnan U, Son M, Rajendran B, Elliott JL (2006) Novel mutations that enhance or repress the aggregation potential of SOD1. Mol Cell Biochem 287, 201-211.
46. Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, Fukutomi H, Noguchi T, Matsuzawa A, Takeda K, Ichijo H (2008) ALS-linked mutant SOD1 induces ER stress and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22, 1451-1464.
47. Dias-Santagata D, Fulga TA, Duttaroy A, Feany MB (2007) Oxidative stress mediates tau-induced neurodegeneration in Drosophila. The Journal of Clinical Investigation 117, 236-245.