Dysfunction of the PI3K-Akt-GSK-3 pathway is a common feature in cell culture and in vivo models of prion disease

Neuropathology and Applied Neurobiology

Volumn 40, Issue 3, 2014, Pages 311-326

  Simon, D ^a   Herva, M E ^b,c   Benitez, M J ^a,d   Garrido, J J ^e   Rojo, A I ^f   Cuadrado, A ^f   Torres, J M ^b   Wandosell, F ^a  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^b Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria   (Spain)

^c The Center for Brain Repair   (United Kingdom)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e CSIC   (Spain)

^f AUTONOMOUS UNIVERSITY OF MADRID   (Spain)

Author keywords

Akt; GSK 3; Neurotoxicity; Prion disease

Indexed keywords

CASPASE 12; CASPASE 3; GLYCOGEN SYNTHASE KINASE 3; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PRION PROTEIN; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CEREBELLUM; CLINICAL FEATURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; PARALLEL DESIGN; PRIMARY CELL CULTURE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

AKT; GSK-3; NEUROTOXICITY; PRION DISEASE;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASE; PRION DISEASES; PRIONS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84896028957     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12066     Document Type: Article

References (59)

1. Prusiner SB. The prion diseases. Brain Pathol 1998; 8: 499-513
2. Sailer A, Bueler H, Fischer M, Aguzzi A, Weissmann C. No propagation of prions in mice devoid of PrP. Cell 1994; 77: 967-968
3. Solomon IH, Schepker JA, Harris DA. Prion neurotoxicity: insights from prion protein mutants. Curr Issues Mol Biol 2010; 12: 51-61
4. Grenier C, Bissonnette C, Volkov L, Roucou X. Molecular morphology and toxicity of cytoplasmic prion protein aggregates in neuronal and non-neuronal cells. J Neurochem 2006; 97: 1456-1466
5. Castilla J, Hetz C, Soto C. Molecular mechanisms of neurotoxicity of pathological prion protein. Curr Mol Med 2004; 4: 397-403
6. Resenberger UK, Winklhofer KF, Tatzelt J. Neuroprotective and neurotoxic signaling by the prion protein. Top Curr Chem 2011; 305: 101-119
7. Forloni G, Angeretti N, Chiesa R, Monzani E, Salmona M, Bugiani O, Tagliavini F. Neurotoxicity of a prion protein fragment. Nature 1993; 362: 543-546
8. Mouillet-Richard S, Schneider B, Pradines E, Pietri M, Ermonval M, Grassi J, Richards JG, Mutel V, Launay JM, Kellermann O. Cellular prion protein signaling in serotonergic neuronal cells. Ann N Y Acad Sci 2007; 1096: 106-119
9. Corsaro A, Thellung S, Villa V, Principe DR, Paludi D, Arena S, Millo E, Schettini D, Damonte G, Aceto A, Schettini G, Florio T. Prion protein fragment 106-126 induces a p38 MAP kinase-dependent apoptosis in SH-SY5Y neuroblastoma cells independently from the amyloid fibril formation. Ann N Y Acad Sci 2003; 1010: 610-622
10. O'Donovan CN, Tobin D, Cotter TG. Prion protein fragment PrP-(106-126) induces apoptosis via mitochondrial disruption in human neuronal SH-SY5Y cells. J Biol Chem 2001; 276: 43516-43523
11. Hetz C, Russelakis-Carneiro M, Maundrell K, Castilla J, Soto C. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J 2003; 22: 5435-5445
12. Post K, Brown DR, Groschup M, Kretzschmar HA, Riesner D. Neurotoxicity but not infectivity of prion proteins can be induced reversibly in vitro. Arch Virol Suppl 2000; 16: 265-273
13. Ma J, Lindquist S. Conversion of PrP to a self-perpetuating PrPSc-like conformation in the cytosol. Science 2002; 298: 1785-1788
14. Saez-Valero J, Angeretti N, Forloni G. Caspase-3 activation by beta-amyloid and prion protein peptides is independent from their neurotoxic effect. Neurosci Lett 2000; 293: 207-210
15. King TD, Bijur GN, Jope RS. Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3beta and attenuated by lithium. Brain Res 2001; 919: 106-114
16. Pietri M, Caprini A, Mouillet-Richard S, Pradines E, Ermonval M, Grassi J, Kellermann O, Schneider B. Overstimulation of PrPC signaling pathways by prion peptide 106-126 causes oxidative injury of bioaminergic neuronal cells. J Biol Chem 2006; 281: 28470-28479
17. Perez M, Rojo AI, Wandosell F, Diaz-Nido J, Avila J. Prion peptide induces neuronal cell death through a pathway involving glycogen synthase kinase 3. Biochem J 2003; 372: 129-136
18. Gavin R, Braun N, Nicolas O, Parra B, Urena JM, Mingorance A, Soriano E, Torres JM, Aguzzi A, del Rio JA. PrP(106-126) activates neuronal intracellular kinases and Egr1 synthesis through activation of NADPH-oxidase independently of PrPc. FEBS Lett 2005; 579: 4099-4106
19. Shi SH, Cheng T, Jan LY, Jan YN. APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr Biol 2004; 14: 2025-2032
20. Jiang H, Guo W, Liang X, Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 2005; 120: 123-135
21. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, Greenberg ME. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 1997; 275: 661-665
22. Perez M, Wandosell F, Colaco C, Avila J. Sulphated glycosaminoglycans prevent the neurotoxicity of a human prion protein fragment. Biochem J 1998; 335: 369-374
23. Coghlan MP, Culbert AA, Cross DA, Corcoran SL, Yates JW, Pearce NJ, Rausch OL, Murphy GJ, Carter PS, Roxbee Cox L, Mills D, Brown MJ, Haigh D, Ward RW, Smith DG, Murray KJ, Reith AD, Holder JC. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem Biol 2000; 7: 793-803
24. Bhat R, Xue Y, Berg S, Hellberg S, Ormo M, Nilsson Y, Radesater AC, Jerning E, Markgren PO, Borgegard T, Nylof M, Gimenez-Cassina A, Hernandez F, Lucas JJ, Diaz-Nido J, Avila J. Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J Biol Chem 2003; 278: 45937-45945
25. Sanchez Martin C, Diaz-Nido J, Avila J. Regulation of a site-specific phosphorylation of the microtubule- associated protein 2 during the development of cultured neurons. Neuroscience 1998; 87: 861-870
26. Sanchez Martin C, Ledesma D, Dotti CG, Avila J. Microtubule-associated protein-2 located in growth regions of rat hippocampal neurons is highly phosphorylated at its proline-rich region. Neuroscience 2000; 101: 885-893
27. Mattson MP, Barger SW, Begley JG, Mark RJ. Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol 1995; 46: 187-216
28. Salinas M, Martin D, Alvarez A, Cuadrado A. Akt1/PKBalpha protects PC12 cells against the parkinsonism-inducing neurotoxin 1-methyl-4-phenylpyridinium and reduces the levels of oxygen-free radicals. Mol Cell Neurosci 2001; 17: 67-77
29. Fischer M, Rulicke T, Raeber A, Sailer A, Moser M, Oesch B, Brandner S, Aguzzi A, Weissmann C. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 1996; 15: 1255-1264
30. Zlotnik I, Rennie JC. Further observations on the experimental transmission of scrapie from sheep and goats to laboratory mice. J Comp Pathol 1963; 73: 150-162
31. Giese A, Kretzschmar HA. Prion-induced neuronal damage - the mechanisms of neuronal destruction in the subacute spongiform encephalopathies. Curr Top Microbiol Immunol 2001; 253: 203-217
32. Nicolas O, Gavin R, Braun N, Urena JM, Fontana X, Soriano E, Aguzzi A, del Rio JA. Bcl-2 overexpression delays caspase-3 activation and rescues cerebellar degeneration in prion-deficient mice that overexpress amino-terminally truncated prion. FASEB J 2007; 21: 3107-3117
33. Pap M, Cooper GM. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3- Kinase/Akt cell survival pathway. J Biol Chem 1998; 273: 19929-19932
34. Cohen P, Frame S. The renaissance of GSK-3. Nat Rev Mol Cell Biol 2001; 2: 769-776
35. Lopes JP, Oliveira CR, Agostinho P. Role of cyclin-dependent kinase 5 in the neurodegenerative process triggered by amyloid-Beta and prion peptides: implications for Alzheimer's disease and prion-related encephalopathies. Cell Mol Neurobiol 2007; 27: 943-957
36. Dorandeu A, Wingertsmann L, Chretien F, Delisle MB, Vital C, Parchi P, Montagna P, Lugaresi E, Ironside JW, Budka H, Gambetti P, Gray F. Neuronal apoptosis in fatal familial insomnia. Brain Pathol 1998; 8: 531-537
37. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998; 281: 1312-1316
38. Mehmet H. Caspases find a new place to hide. Nature 2000; 403: 29-30
39. Forloni G, Bugiani O, Tagliavini F, Salmona M. Apoptosis-mediated neurotoxicity induced by beta-amyloid and PrP fragments. Mol Chem Neuropathol 1996; 28: 163-171
40. Carimalo J, Cronier S, Petit G, Peyrin JM, Boukhtouche F, Arbez N, Lemaigre-Dubreuil Y, Brugg B, Miquel MC. Activation of the JNK-c-Jun pathway during the early phase of neuronal apoptosis induced by PrP106-126 and prion infection. Eur J Neurosci 2005; 21: 2311-2319
41. Giese A, Groschup MH, Hess B, Kretzschmar HA. Neuronal cell death in scrapie-infected mice is due to apoptosis. Brain Pathol 1995; 5: 213-221
42. Ma J, Wollmann R, Lindquist S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 2002; 298: 1781-1785
43. Hetz C, Russelakis-Carneiro M, Walchli S, Carboni S, Vial-Knecht E, Maundrell K, Castilla J, Soto C. The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci 2005; 25: 2793-2802
44. Ferrer I. Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease. Cerebellum 2002; 1: 213-222
45. Steele AD, Hetz C, Yi CH, Jackson WS, Borkowski AW, Yuan J, Wollmann RH, Lindquist S. Prion pathogenesis is independent of caspase-12. Prion 2007; 1: 243-247
46. Zanata SM, Lopes MH, Mercadante AF, Hajj GN, Chiarini LB, Nomizo R, Freitas AR, Cabral AL, Lee KS, Juliano MA, de Oliveira E, Jachieri SG, Burlingame A, Huang L, Linden R, Brentani RR, Martins VR. Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J 2002; 21: 3307-3316
47. Caetano FA, Lopes MH, Hajj GN, Machado CF, Pinto Arantes C, Magalhaes AC, Vieira Mde P, Americo TA, Massensini AR, Priola SA, Vorberg I, Gomez MV, Linden R, Prado VF, Martins VR, Prado MA. Endocytosis of prion protein is required for ERK1/2 signaling induced by stress-inducible protein 1. J Neurosci 2008; 28: 6691-6702
48. Uppington KM, Brown DR. Resistance of cell lines to prion toxicity aided by phospho-ERK expression. J Neurochem 2008; 105: 842-852
49. Rapoport M, Ferreira A. PD98059 prevents neurite degeneration induced by fibrillar beta-amyloid in mature hippocampal neurons. J Neurochem 2000; 74: 125-133
50. Medina MG, Ledesma MD, Dominguez JE, Medina M, Zafra D, Alameda F, Dotti CG, Navarro P. Tissue plasminogen activator mediates amyloid-induced neurotoxicity via Erk1/2 activation. EMBO J 2005; 24: 1706-1716
51. Brunet A, Datta SR, Greenberg ME. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 2001; 11: 297-305
52. van der Heide LP, Ramakers GM, Smidt MP. Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol 2006; 79: 205-221
53. Alessi DR, Deak M, Casamayor A, Caudwell FB, Morrice N, Norman DG, Gaffney P, Reese CB, MacDougall CN, Harbison D, Ashworth A, Bownes M. 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr Biol 1997; 7: 776-789
54. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005; 307: 1098-1101
55. Brognard J, Sierecki E, Gao T, Newton AC. PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol Cell 2007; 25: 917-931
56. Gasparini L, Xu H. Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci 2003; 26: 404-406
57. Townsend M, Mehta T, Selkoe DJ. Soluble Abeta inhibits specific signal transduction cascades common to the insulin receptor pathway. J Biol Chem 2007; 282: 33305-33312
58. Lee HK, Kumar P, Fu Q, Rosen KM, Querfurth HW. The insulin/Akt signaling pathway is targeted by intracellular beta-amyloid. Mol Biol Cell 2009; 20: 1533-1544
59. Morales R, Duran-Aniotz C, Castilla J, Estrada LD, Soto C. De novo induction of amyloid-beta deposition in vivo. Mol Psychiatry 2012; 17: 1347-1353