Neuronal death induced by misfolded prion protein is due to NAD+ depletion and can be relieved in vitro and in vivo by NAD+ replenishment

Brain

Volumn 138, Issue 4, 2015, Pages 992-1008

  Zhou, Minghai ^a   Ottenberg, Gregory ^a   Sferrazza, Gian Franco ^a   Hubbs, Christopher ^a   Fallahi, Mohammad ^a   Rumbaugh, Gavin ^a   Brantley, Alicia F ^a   Lasmézas, Corinne I ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

neurodegeneration; neuroprotection; nicotinamide dinucleotide; prion; protein misfolding

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PRION PROTEIN; PRION;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; HIPPOCAMPAL NEURONAL CULTURE; IN VITRO STUDY; IN VIVO STUDY; MOTOR DYSFUNCTION; MOUSE; NERVE CELL; NERVE CELL DEGENERATION; NERVE DEGENERATION; NEUROBLASTOMA CELL; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FOLDING; ANIMAL; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DRUG EFFECTS; FEMALE; METABOLISM; PATHOLOGY; PRION; PRION DISEASES; TOXICITY;

ANIMALS; CELL DEATH; CELLS, CULTURED; FEMALE; MICE; MICE, INBRED C57BL; NAD; NEURONS; PRION DISEASES; PRIONS; PROTEIN FOLDING;

EID: 84929069363     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv002     Document Type: Article

References (84)

1. Aguzzi A, Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009; 64: 783-90.
2. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA. NAD + depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 2010; 30: 2967-78.
3. Andrabi SA, Kang HC, Haince JF, Lee YI, Zhang J, Chi Z, et al. Iduna protects the brain from glutamate excitotoxicity and stroke by interfering with poly(ADP-ribose) polymer-induced cell death. Nat Med 2011; 17: 692-9.
4. Benilova I, Karran E, De Strooper B. The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci 2012; 15: 349-57.
5. Bhoopathi P, Chetty C, Gujrati M, Dinh DH, Rao JS, Lakka S. Cathepsin B facilitates autophagy-mediated apoptosis in SPARC overexpressed primitive neuroectodermal tumor cells. Cell Death Different 2010; 17: 1529-39.
6. Biasini E, Unterberger U, Solomon IH, Massignan T, Senatore A, Bian H, et al. A mutant prion protein sensitizes neurons to glutamate-induced excitotoxicity. J Neurosci 2013; 33: 2408-18.
7. Billington RA, Genazzani AA, Travelli C, Condorelli F. NAD depletion by FK866 induces autophagy. Autophagy 2008; 4: 385-7.
8. Birkmayer W, Birkmayer JG, Vrecko K, Paletta B. The clinical benefit of NADH as stimulator of endogenous L-dopa biosynthesis in par-kinsonian patients. Adv Neurol 1990; 53: 545-9.
9. Blesa J, Phani S, Jackson-Lewis V, Przedborski S. Classic and new animal models of Parkinson's disease. J Biomed Biotechnol 2012; 2012: 845618.
10. Braidy N, Gai WP, Xu YH, Sachdev P, Guillemin GJ, Jiang XM, et al. Uptake and mitochondrial dysfunction of alpha-synuclein in human astrocytes, cortical neurons and fibroblasts. Transl Neurodegener 2013; 2: 20.
11. Bü eler H, Raeber A, Sailer A, Fischer M, Aguzzi A, Weissmann C. High prion and PrPsc levels but delayed onset of disease in scrapie-inoculated mice heterozygous for a disrupted PrP gene. Mol Med 1994; 1: 19-30.
12. Caughey B, Lansbury PT. Protofibrils, pores, fibrils, and neuro-degeneration: separating the responsible protein aggregates from the innocent bystanders. Ann Rev Neurosci 2003; 26: 267-98.
13. Cavallucci V, D'Amelio M, Cecconi F. Abeta toxicity in Alzheimer's disease. Mol Neurobiol 2012; 45: 366-78.
14. Crystal H, Dickson D, Fuld P, Masur D, Scott R, Mehler M, et al. Clinico-pathologic studies in dementia: nondemented subjects with pathologically confirmed Alzheimer's disease. Neurology 1988; 38: 1682-7.
15. Demarin V, Podobnik SS, Storga-Tomic D, Kay G. Treatment of Alzheimer's disease with stabilized oral nicotinamide adenine di-nucleotide: a randomized, double-blind study. Drugs Exp Clin Res 2004; 30: 27-33.
16. Di Girolamo M, Dani N, Stilla A, Corda D. Physiological relevance of the endogenous mono(ADP-ribosyl)ation of cellular proteins. FEBS J 2005; 272: 4565-75.
17. Di Girolamo M, Fabrizio G, Scarpa ES, Di Paola S. NAD(+)-dependent enzymes at the endoplasmic reticulum. Curr TopMed Chem 2013; 13: 3001-10.
18. Dorandeu A, Wingertsmann L, Chretien F, Delisle MB, Vital C, Parchi P, et al. Neuronal apoptosis in fatal familial insomnia. Brain Pathol 1998; 8: 531-7.
19. Eliasson MJ, Sampei K, Mandir AS, Hurn PD, Traystman RJ, Bao J, et al. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med 1997; 3: 1089-95.
20. Exner N, Lutz AK, Haass C, Winklhofer KF. Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J 2012; 31: 3038-62.
21. Feijs KL, Forst AH, Verheugd P, Luscher B. Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nature reviews. Mol Cell Biol 2013; 14: 443-51.
22. Friedman-Levi Y, Meiner Z, Canello T, Frid K, Kovacs GG, Budka H, et al. Fatal prion disease in a mouse model of genetic E200K Creutzfeldt-Jakob disease. PLoS Pathog 2011; 7: e1002350.
23. Garden GA, La Spada AR. Intercellular (mis)communication in neu-rodegenerative disease. Neuron 2012; 73: 886-901.
24. Graff CL, Pollack GM. Nasal drug administration: potential for targeted central nervous system delivery. J Pharm Sci 2005; 94: 1187-95.
25. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 2007; 8: 101-12.
26. Harris H, Rubinsztein DC. Control of autophagy as a therapy for neurodegenerative disease. Nat Rev Neurol 2012; 8: 108-17.
27. Hassa PO, Hottiger MO. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymer-ases. Front Biosci 2008; 13: 3046-82.
28. Heiseke A, Aguib Y, Schatzl HM. Autophagy, prion infection and their mutual interactions. Curr Issues Mol Biol 2009; 12: 87-98.
29. Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F. Toward a unified nomenclature for mammalian ADP-ribosyltrans-ferases. Trends Biochem Sci 2010; 35: 208-19.
30. Houtkooper RH, Canto C, Wanders RJ, Auwerx J. The secret life of NAD + : an old metabolite controlling new metabolic signaling pathways. Endocrine Rev 2010; 31: 194-223.
31. Jagtap P, Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 2005; 4: 421-40.
32. Kaneko S, Wang J, Kaneko M, Yiu G, Hurrell JM, Chitnis T, et al. Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J Neurosci 2006; 26: 9794-804.
33. Kauppinen TM, Swanson RA. The role of poly(ADP-ribose) polymer-ase-1 in CNS disease. Neuroscience 2007; 145: 1267-72.
34. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003; 300: 486-9.
35. Kletzien RF, Harris PK, Foellmi LA. Glucose-6-phosphate dehydrogen-ase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB J 1994; 8: 174-81.
36. Koh DW, Dawson TM, Dawson VL. Mediation of cell death by poly(ADP-ribose) polymerase-1. Pharmacol Res 2005; 52: 5-4.
37. Kristiansen M, Deriziotis P, Dimcheff DE, Jackson GS, Ovaa H, Naumann H, et al. Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol Cell 2007; 26: 175-88.
38. Kuhn W, Muller T, Winkel R, Danielczik S, Gerstner A, Hacker R, et al. Parenteral application of NADH in Parkinson's disease: clinical improvement partially due to stimulation of endogenous levodopa biosynthesis. J Neural Transm 1996; 103: 1187-93.
39. Kuzhandaivel A, Nistri A, Mladinic M. Kainate-mediated excitotoxi-city induces neuronal death in the rat spinal cord in vitro via a PARP-1 dependent cell death pathway (Parthanatos). Cell Mol Neurobiol 2010; 30: 1001-12.
40. Lasmézas CI, Deslys J-P, Demaimay R, Adjou KT, Hauw J-J, Dormont D. Strain specific and common pathogenic events in murine models of scrapie and bovine spongiform encephalopathy. J Gen Virol 1996; 77: 1601-9.
41. Lasmézas CI, Deslys J-P, Robain O, Jaegly A, Beringue V, Peyrin J-M, et al. Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 1997; 275: 402-5.
42. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010; 141: 1146-58.
43. Lepine S, Allegood JC, Edmonds Y, Milstien S, Spiegel S. Autophagy induced by deficiency of sphingosine-1-phosphate phosphohydrolase 1 is switched to apoptosis by calpain-mediated autophagy-related gene 5 (Atg5) cleavage. J Biol Chem 2011; 286: 44380-90.
44. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006; 440: 352-7.
45. Liberski PP, Brown P. Astrocytes in transmissible spongiform encepha-lopathies (prion diseases). Folia Neuropathol 2004; 42 (Suppl B): 71-88.
46. Liberski PP, Yanagihara R, Gibbs CJ, Gajdusek DC. Neuronal autop-hagic vacuoles in experimental scrapie and creutzfeldt-jakob disease. Acta Neuropathol 1992; 83: 134-9.
47. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ, et al. Pathological alpha-synuclein transmission initiates Parkinsonlike neurodegeneration in nontransgenic mice. Science 2012; 338: 949-53.
48. Ma J, Wollmann R, Lindquist S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 2002; 298: 1781-5.
49. Martinez-Vicente M, Cuervo AM. Autophagy and neurodegeneration: when the cleaning crew goes on strike. Lancet Neurol 2007; 6: 352-61.
50. Martinez-Vicente M, Talloczy Z, Wong E, Tang G, Koga H, Kaushik S, et al. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat Neurosci 2010; 13: 567-76.
51. Marzulli D, La Piana G, Fransvea E, Lofrumento NE. Modulation of cytochrome c-mediated extramitochondrial NADH oxidation by contact site density. Biochem Biophys Res Commun 1999; 259: 325-30.
52. McCormack JG, Denton RM. The role of Ca2+ in the regulation of intramitochondrial energy production in heart. Biomed Biochim Acta 1987; 46: S487-92.
53. Mindell JA. Lysosomal acidification mechanisms. Ann Rev Physiol 2012; 74: 69-86.
54. Moreno JA, Radford H, Peretti D, Steinert JR, Verity N, Martin MG, et al. Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 2012; 485: 507-11.
55. Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 2009; 324: 654-57.
56. Nikiforov A, Dolle C, Niere M, Ziegler M. Pathways and subcellular compartmentation of NAD biosynthesis in human cells: from entry of extracellular precursors to mitochondrial NAD generation. J Biol Chem 2011; 286: 21767-78.
57. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, et al. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 2005; 64: 113-22.
58. Nixon RA, Yang DS. Autophagy and neuronal cell death in neurological disorders. Cold Spring Harbor perspectives in biology 2012; 4. pii: a008839.
59. Olanow CW, Brundin P. Parkinson's disease and alpha synuclein: is Parkinson's disease a prion-like disorder? Mov Disord 2013; 28: 31-40.
60. Outeiro TF, Putcha P, Tetzlaff JE, Spoelgen R, Koker M, Carvalho F, et al. Formation of toxic oligomeric alpha-synuclein species in living cells. PLoS One 2008; 3: e1867.
61. Piccardo P, Manson JC, King D, Ghetti B, Barron RM. Accumulation of prion protein in the brain that is not associated with transmissible disease. Proc Natl Acad Sci USA 2007; 104: 4712-17.
62. Pittelli M, Felici R, Pitozzi V, Giovannelli L, Bigagli E, Cialdai F, et al. Pharmacological effects of exogenous NAD on mitochondrial bioenergetics, DNA repair, and apoptosis. Mol Pharmacol 2011; 80: 1136-46.
63. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982; 216: 136-44.
64. Puoti G, Bizzi A, Forloni G, Safar JG, Tagliavini F, Gambetti P. Sporadic human prion diseases: molecular insights and diagnosis. Lancet Neurol 2012; 11: 618-28.
65. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 2009; 324: 651-4.
66. Ross TM, Martinez PM, Renner JC, Thorne RG, Hanson LR, Frey WH, 2nd. Intranasal administration of interferon beta bypasses the blood-brain barrier to target the central nervous system and cervical lymph nodes: a non-invasive treatment strategy for multiple sclerosis. J Neuroimmunol 2004; 151: 66-77.
67. Rumbaugh G, Adams JP, Kim JH, Huganir RL. SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons. Proc Natl Acad Sci U S A 2006; 103: 4344-51.
68. Sandberg MK, Al-Doujaily H, Sharps B, Clarke AR, Collinge J. Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 2011; 470: 540-2.
69. Sasaki Y, Araki T, Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J Neurosci 2006; 26: 8484-91.
70. Siegel C, McCullough LD. NAD+ depletion or PAR polymer formation: which plays the role of executioner in ischaemic cell death? Acta Physiol (Oxf) 2011; 203: 225-34.
71. Sonati T, Reimann RR, Falsig J, Baral PK, O'Connor T, Hornemann S, et al. The toxicity of antiprion antibodies is mediated by the flexible tail of the prion protein. Nature 2013; 501: 102-6.
72. Soto C, Satani N. The intricate mechanisms of neurodegeneration in prion diseases. Trends Mol Med 2011; 17: 14-24.
73. Thellung S, Gatta E, Pellistri F, Corsaro A, Villa V, Vassalli M, et al. Excitotoxicity through NMDA receptors mediates cerebellar granule neuron apoptosis induced by prion protein 90-231 fragment. Neurotox Res 2013; 23: 301-14.
74. Trancikova A, Ramonet D, Moore DJ. Genetic mouse models of neu-rodegenerative diseases. Progr Mol Biol Transl Sci 2011; 100: 419-82.
75. Unterberger U, Voigtlander T, Budka H. Pathogenesis of prion diseases. Acta Neuropathol 2005; 109: 32-48.
76. Welsby I, Hutin D, Leo O. Complex roles of members of the ADP-ribosyl transferase super family in immune defences: looking beyond PARP1. Biochem Pharmacol 2012; 84: 11-20.
77. Winner B, Jappelli R, Maji SK, Desplats PA, Boyer L, Aigner S, et al. In vivo demonstration that alpha-synuclein oligomers are toxic. Proc Natl Acad Sci USA 2011; 108: 4194-9.
78. Winslow AR, Rubinsztein DC. The Parkinson disease protein alpha-synuclein inhibits autophagy. Autophagy 2011; 7: 429-31.
79. Yau L, Elliot T, Lalonde C, Zahradka P. Repression of phosphoenolpyruvate carboxykinase gene activity by insulin is blocked by 3-aminobenzamide but not by PD128763, a selective inhibitor of poly(ADP-ribose) polymerase. Eur J Biochem 1998; 253: 91-100.
80. Ying W, Wei G, Wang D, Wang Q, Tang X, Shi J, et al. Intranasal administration with NAD+ profoundly decreases brain injury in a rat model of transient focal ischemia. Front Biosci 2007; 12: 2728-34.
81. Zetterberg H, Blennow K. Biomarker evidence for uncoupling of amyloid build-up and toxicity in Alzheimer's disease. Alzheimer's Dement 2013; 9: 459-62.
82. Zhang J, Dawson VL, Dawson TM, Snyder SH. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 1994; 263: 687-89.
83. Zheng Z, Diamond MI. Huntington disease and the huntingtin protein. Prog Mol Biol Transl Sci 2012; 107: 189-214.
84. Zhou M, Ottenberg G, Sferrazza GF, Lasmezas CI. Highly neurotoxic monomeric alpha-helical prion protein. Proc Natl Acad Sci USA 2012; 109: 3113-18.