ER Stress Induced by Tunicamycin Triggers α-Synuclein Oligomerization, Dopaminergic Neurons Death and Locomotor Impairment: a New Model of Parkinson’s Disease

Molecular Neurobiology

Volumn 54, Issue 8, 2017, Pages 5798-5806

  Cóppola Segovia, Valentín ^a   Cavarsan, Clarissa ^a   Maia, Flavia G ^a   Ferraz, Anete C ^a   Nakao, Lia S ^a   Lima, Marcelo Ms ^a   Zanata, Silvio M ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

ER stress; Parkinson s disease; Tunicamycin; Synuclein oligomerization

Indexed keywords

ALPHA SYNUCLEIN; OXIDOPAMINE; TUNICAMYCIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CLINICAL FEATURE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENDOPLASMIC RETICULUM STRESS; IN VIVO STUDY; MACROGLIA; MALE; MOTOR DYSFUNCTION; NERVE CELL NECROSIS; NONHUMAN; OLIGOMERIZATION; PARKINSON DISEASE; PATHOPHYSIOLOGY; PHENOTYPE; RAT; SUBSTANTIA NIGRA PARS COMPACTA; UNFOLDED PROTEIN RESPONSE; ANIMAL; DRUG EFFECT; LOCOMOTION; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; SUBSTANTIA NIGRA; WISTAR RAT;

ALPHA-SYNUCLEIN; ANIMALS; DOPAMINERGIC NEURONS; ENDOPLASMIC RETICULUM STRESS; LOCOMOTION; MALE; OXIDATIVE STRESS; PARKINSON DISEASE; RATS, WISTAR; SUBSTANTIA NIGRA; TUNICAMYCIN;

EID: 84988692340     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-016-0114-x     Document Type: Article

References (72)

1. Lang AE, Lozano AM (1998) Parkinson's disease. N Engl J Med 339:1044–1053
2. Shiba M, Bower JH, Maraganore DM, McDonnell SK, Peterson BJ, Ahlskog JE, Schaid DJ, Rocca WA (2000) Anxiety disorders and depressive disorders preceding Parkinson’s disease: a case-control study. Mov Disord 15(4):669–677
3. Lima MM, Andersen ML, Reksidler AB, Ferraz AC, Vital MA, Tufik S (2012) Paradoxical sleep deprivation modulates tyrosine hydroxylase expression in the nigrostriatal pathway and attenuates motor deficits induced by dopaminergic depletion. CNS & Neurol Disord Drug Targets 11(4):359–368
4. Dauer W, Przedborski S (2003) Parkinson ’ s disease: mechanisms and models. Neuron 39:889–909
5. Przedborski S (2010) Inflammation and Parkinson’s disease pathogenesis. Mov Disord 25(1):S55–S57
6. Tieu K (2011) A guide to neurotoxic animal models of Parkinson’s disease. Cold Spring Harb Perspect Med 1(1):a009316. doi:10.1101/cshperspect.a009316
7. Perier C, Vila M (2012) Mitochondrial biology and Parkinson’s disease. Cold Spring Harbor perspectives in medicine 2(2):a009332
8. Jellinger KA (2012) Interaction between pathogenic proteins in neurodegenerative disorders. J Cell Mol Med 16(6):1166–1183
9. Dettmer U, Selkoe D, Bartels T (2016) New insights into cellular α-synuclein homeostasis in health and disease. Curr Opin Neurobiol 36:15–22
10. Danzer KM, Haasen D, Karow AR, Moussaud S, Habeck M, Giese A, Kretzschmar H, Hengerer B, Kostka M (2007) Different species of alpha-synuclein oligomers induce calcium influx and seeding. J Neurosci 27(34):9220–9232
11. Hettiarachchi NT, Parker A, Dallas ML, Pennington K, Hung CC, Pearson HA, Boyle JP, Robinson P, Peers C (2009) α-Synuclein modulation of Ca2+ signaling in human neuroblastoma (SH-SY5Y) cells. J. Neurochem 111(5):1192–1201
12. Winklhofer KF, Haass C (2010) Mitochondrial dysfunction in Parkinson’s disease. Biochim Biophys Acta 1802(1):29–44
13. Tsang AH, Chung KK (2009) Oxidative and nitrosative stress in Parkinson’s disease. Biochim Biophys Acta 1792(7):643–650
14. Chen L, Jin J, Davis J, Zhou Y, Wang Y, Liu J, Lockhart PJ, Zhang J (2007) Oligomeric alpha-synuclein inhibits tubulin polymerization. Biochem Biophys Res Commun 356(3):548–553
15. Qian L, Flood PM, Hong JS (2010) Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J Neural Transm 117(8):971–979
16. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M (1998) alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci U S A 95(11):6469–6473
17. Roberts HL, Brown DR (2015) Seeking a mechanism for the toxicity of oligomeric α-synuclein. Biomolecules 5(2):282–305
18. Kim YM, Jang WH, Quezado MM, Oh Y, Chung KC, Junn E, Mouradian MM (2011) Proteasome inhibition induces α-synuclein SUMOylation and aggregate formation. J Neurol Sci 307(1–2):157–161
19. Krumova P, Meulmeester E, Garrido M, Tirard M, Hsiao HH, Bossis G, Urlaub H, Zweckstetter M, Kügler S, Melchior F, Bähr M, Weishaupt JH (2011) Sumoylation inhibits α-synuclein aggregation and toxicity. J Cell Biol 194(1):49–60
20. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R, Wu DC, Follenzi A, Dauer W, Przedborski S, Ischiropoulos H, Lansbury PT, Sulzer D, Cuervo AM (2008) Dopamine-modified α-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118(2):777–788
21. Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13(2):89–102
22. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7(12):1013–1030
23. Boyce M, Yuan J (2006) Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13(3):363–373
24. Yoshida H (2007) ER stress and diseases. FEBS J 274(3):630–658
25. Hoozemans JJM, Scheper W (2012) Endoplasmic reticulum: the unfolded protein response is tangled in neurodegeneration. Int J Biochem Cell Biol 44(8):1295–1298
26. Hetz C, Mollereau B (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci 15(4):233–249
27. Mercado G, Castillo V, Soto P, Sidhu A (2016) ER stress and Parkinson's disease: pathological inputs that converge into the secretory pathway. Brain Res. doi:10.1016/j.brainres.2016.04.042
28. Hoozemans JJM, Van Haastert ES, Eikelenboom P, Vos D, R. al, Rozemuller JM, Scheper W (2007) Activation of the unfolded protein response in Parkinson’s disease. Biochem Biophys Res Commun 354(3):707–711
29. Holtz WA, O’Malley KL (2003) Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J Biol Chem 278(21):19367–19377
30. Tanaka K, Fukuoka S, Kawahara S, Kimoto N, Ogawa N (2013) Effect of cabergoline on increase of several ER stress-related molecules in 6-OHDA-lesioned mice. Neurol Sci 34(2):259–261
31. Silva RM, Ries V, Oo TF, Yarygina O, Jackson- V, Ryu EJ, Lu PD, Marciniak SJ, Ron D, Przedborski S, Kholodilov N, Greene LA, Burke RE (2005) CHOP/GADD153 is a mediator of apoptotic death in substantia nigra dopamine neurons in an in vivo neurotoxin model of parkinsonism. J Neurochem 95(4):974–986
32. Ryu EJ, Harding HP, Angelastro JM, Vitolo OV, Ron D, Greene LA (2002) Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson’ s disease. J Neurosci 22(24):10690–10698
33. Credle JJ, Forcelli PA, Delannoy M, Oaks AW, Permaul E, Berry DL, Duka V, Wills J, Sidhu A (2015) Alpha-synuclein-mediated inhibition of ATF6 processing into COPII vesicles disrupts UPR signaling in Parkinson's disease. NeurobiolDis 76:112–125
34. Egawa N, Yamamoto K, Inoue H, Hikawa R, Nishi K, Mori K, Takahashi R (2011) The endoplasmic reticulum stress sensor, ATF6alpha, protects against neurotoxin-induced dopaminergic neuronal death. J Biol Chem 286(10):7947–7957
35. Valdés P, Mercado G, Vidal RL, Molina C, Parsons G, Court FA, Martinez A, Galleguillos D, Armentano D, Schneider BL, Hetz C (2014) Control of dopaminergic neuron survival by the unfolded protein response transcription factor XBP1. Proc Natl Acad Sci U S A 111(18):6804–6809
36. Leaver DD, Schneider KM, Rand MJ, Anderson RM, Gage PW, Malbon R (1988) The neurotoxicity of tunicamycin. Toxicology 49:179–187
37. Ebert DA, Hann HJ, Bohn MC (2008) Progressive degeneration of dopamine neurons in 6-hydroxydopamine rat model of Parkinson’s disease does not involve activation of caspase-9 and caspase-3. J Neurosci Res 86:317–325
38. Hsieh T-H, Chen J-JJ, Chen L-H, Chiang P-T, Lee H-Y (2011) Time-course gait analysis of hemiparkinsonian rats following 6-hydroxydopamine lesion. Behav Brain Res 222(1):1–9
39. Carter, R. J., Morton J., Dunnet, S. B. (2001). Motor coordination and balance in rodents. Curr Protoc Neurosci, Chapter 8: Unit 8.12. doi: 10.1002/0471142301.ns0812s15
40. Pallier PN, Drew CJG, Morton AJ (2009) The detection and measurement of locomotor deficits in a transgenic mouse model of Huntington’s disease are task- and protocol-dependent: influence of non-motor factors on locomotor function. Brain Res Bull 78(6):347–355
41. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, et al. (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington’ s disease mutation. J Neurosci 19(8):3248–3257
42. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35
43. Kikuchi H, Almer G, Yamashita S, Guégan C, Nagai M, Xu Z, Sosunov A a, et al. (2006) Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model. Proc Natl Acad Sci U S A 103(15):6025–6030
44. Jiang P, Gan M, Ebrahim AS, Lin W-L, Melrose HL, Yen S-HC (2010) ER stress response plays an important role in aggregation of α-synuclein. Mol Neurodegener 5(1):56. doi:10.1186/1750-1326-5-56
45. Colla E, Coune P, Liu Y, Pletnikova O, Troncoso JC, Iwatsubo T, Schneider BL, et al. (2012) Endoplasmic reticulum stress is important for the manifestations of α-synucleinopathy in vivo. J Neurosci 32(10):3306–3320
46. Dawson TM, Dawson VL (2003) Molecular pathways of neurodegeneration in Parkinson’s disease. Science 302:819–822
47. Mori K (2000) Tripartite management of unfolded Proteins in the endoplasmic reticulum. Cell 101:451–454
48. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529
49. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P (2013) Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5(3):a013169
50. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13(3):184–190
51. Hoozemans JJM, Van Haastert ES, Nijholt D a T, Rozemuller AJM, Scheper W (2012) Activation of the unfolded protein response is an early event in Alzheimer’s and Parkinson's disease. Neurodegener Dis 10(1–4):212–215
52. Bové J, Prou D, Perier C, Przedborski S (2005) Toxin-induced models of Parkinson’s disease. NeuroRx 2(3):484–494
53. Liu ZC, Fu ZQ, Song J, Zhang JY, Wei YP, Chu J, Han L, Qu N, Wang JZ, Tian Q (2012) Bip enhanced the association of GSK-3b with tau during ER stress both in vivo and in vitro. J Alzheimers Disease 29(4):727–740
54. Okada T, Yoshida H, Akazawa R, Negishi M, Mori K (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366:585–594
55. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11(4):381–389
56. Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14(1):20–28
57. Lu W, Hagiwara D, Morishita Y, Tochiya M, Azuma Y, Suga H, Goto M, Banno R, Sugimura Y, Oyadomari S, Mori K, Arima H (2016) Unfolded protein response in hypothalamic cultures of wild-type and ATF6α-knockout mice. Neurosci Lett 612:199–203
58. Rutkowski DT, Arnold SM, Miller CN, Wu J, Li J, Gunnison KM, Mori K, et al. (2006) Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 4(11):e374
59. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982–995
60. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, et al. (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18(24):3066–3077
61. Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, Cregan SP (2010) Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of Bcl-2 homology 3-only member PUMA. J Neurosci 30(50):16938–16948
62. Zhang W, Wang T, Pei Z, Miller DS, Wu X, Block ML, Wilson B, Zhang W, Zhou Y, Hong JS, Zhang J (2005) Aggregated α-synuclein activates microglia: a process leading to disease progression in Parkinson’s disease. FASEB J 19(6):533–542
63. Winner B, Jappelli R, Maji S, K. D, P. A, Boyer L, Aigner S, Hetzer C, Loher T, Vilar M, Campioni S, Tzitzilonis C, Soragni A, Jessberger S, Mira H, Consiglio A, Pham E, Masliah E, Gage FH, Riek R (2011) In vivo demonstration that α-syniclein oligomers are toxic. Proc Natl Acad Sci U S A 108(10):4194–4199
64. Jiang P, Gan M, Lin W-L, Yen S-HC (2014) Nutrient deprivation induces α-synuclein aggregation through endoplasmic reticulum stress response and SREBP2 pathway. Front Aging Neurosci 6:268. doi:10.3389/fnagi.2014.00268
65. Heneka MT, Rodríguez JJ, Verkhratsky A (2010) Neuroglia in neurodegeneration. Brain Res Rev 63(1–2):189–211
66. Papadeas ST, Kraig SE, O’Banion C, Lepore AC, Maragakis NJ (2011) Astrocytes carrying the superoxide dismutase 1 (SOD1G93A) mutation induce wild-type motor neuron degeneration in vivo. Proc Natl Acad Sci U S A 108(43):17803–17808
67. Díaz-Amarilla P, Olivera-Bravo S, Trias E, Cragnolini A, Martínez-Palma L, Cassina P, Beckman J, Barbeito L (2011) Phenotypically aberrant astrocytes that promote motoneuron damage in a model of inherited amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 108(44):18126–18131
68. Langston JW, Forno LS, Tetrud J, Reeves AG, Kaplan JA, Karluk D (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann Neurol 46(4):598–605
69. Damier P, Hirsch CE, Zhang P, Agid Y, Javoy-Agid F (1993) Glutathione peroxidase, glial cells and Parkinson’s disease. Neuroscience 52(1):1–6
70. Kondo S, Murakami T, Tatsumi K, Ogata M, Kanemoto S, Otori K, Iseki K, et al. (2005) OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat Cell Biol 7(2):186–194
71. Matsui H, Ito H, Taniguchi Y, Takeda S, Takahashi R (2010) Ammonium chloride and tunicamycin are novel toxins for dopaminergic neurons and induce Parkinson’s disease-like phenotypes in medaka fish. J Neurochem 115(5):1150–1160
72. Fouillet A, Levet C, Virgone A, Robin M, Dourlen P, Rieusset J, Belaidi E, Ovize M, Touret M, Nataf S, Mollereau B (2012) ER stress inhibits neuronal death by promoting autophagy. Autophagy 8(6):915–926