Interactions between Calcium and Alpha-Synuclein in Neurodegeneration
Abstract
:1. Introduction
1.1. Neurodegeneration and α-Synuclein
1.2. Parkinson’s Disease and α-Synuclein
1.3. Parkinson’s Disease and Environmental Factors
1.4. Pathology of Parkinson’s Disease and Multiple System Atrophy
1.5. Properties of α-Synuclein
1.6. α-Synuclein Oligomerization and Cytotoxicity
1.7. α-Synuclein Post-Translational Modifications
1.8. Exosomes and the Cell to Cell Spread of α-Synuclein
1.9. Oxidative Stress
2. Increased Intracellular Ca2+ Induces α-Synuclein Oligomers
2.1. The Role of Ca2+ in the Neuron and Age Related Changes
2.2. Increased Intracellular Ca2+ Induces α-Synuclein Oligomers
2.3. α-Synuclein Oligomerization Induces Raised Ca2+ and Oxidative Stress
2.4. Synergistic Effect of Ca2+ and Oxidative Stress
3. Conclusions: Targeting Calcium with Future Therapeutics
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Goedert, M.; Spillantini, M.G.; del Tredici, K.; Braak, H. 100 years of Lewy pathology. Nat. Rev. Neurol. 2013, 9, 13–24. [Google Scholar] [CrossRef]
- Eschbach, J.; Danzer, K.M. α-Synuclein in Parkinson’s disease: Pathogenic function and translation into animal models. Neurodegener. Dis. 2014, 14, 1–17. [Google Scholar] [CrossRef]
- Radford, R.; Wong, M.B.; Pountney, D.L. Neurodegenerative aspects of multiple system atrophy. In Handbook of Neurotoxicity; Kostrzewa, R.M., Ed.; Springer: New York, NY, USA, 2014; pp. 2157–2180. [Google Scholar]
- Krüger, R.; Kuhn, W.; Müller, T.; Woitalla, D.; Graeber, M.; Kösel, S.; Przuntek, H.; Epplen, J.T.; Schöls, L.; Riess, O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson’s disease. Nat. Genet. 1998, 18, 106–108. [Google Scholar]
- Polymeropoulos, M.H.; Lavedan, C.; Leroy, E.; Ide, S.E.; Dehejia, A.; Dutra, A.; Pike, B.; Root, H.; Rubenstein, J.; Boyer, R.; et al. Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease. Science 1997, 276, 2045–2047. [Google Scholar]
- Zarranz, J.J.; Alegre, J.; Gómez-Esteban, J.C.; Lezcano, E.; Ros, R.; Ampuero, I.; Vidal, L.; Hoenicka, J.; Rodriguez, O.; Atarés, B.; et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 2004, 55, 164–173. [Google Scholar] [CrossRef] [PubMed]
- Lesage, S.; Anheim, M.; Letournel, F.; Bousset, L.; Honore, A.; Rozas, N.; Pieri, L.; Madiona, K.; Durr, A.; Melki, R.; et al. G51D α-Synuclein mutation causes a novel parkinsonian-pyramidal syndrome. Ann. Neurol. 2013, 73, 459–471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Proukakis, C.; Dudzik, C.G.; Brier, T.; MacKay, D.S.; Cooper, J.M.; Millhauser, G.L.; Houlden, H.; Schapira, A.H. A novel α-synuclein missense mutation in Parkinson disease. Neurology 2013, 80, 1062–1064. [Google Scholar] [CrossRef] [PubMed]
- Kanda, S.; Bishop, J.F.; Eglitis, M.A.; Yang, Y.; Mouradian, M.M. Enhanced viability to oxidative stress by alpha-synuclein mutations and C-terminal truncation. Neuroscience 2000, 97, 279–284. [Google Scholar] [CrossRef] [PubMed]
- Narhi, L.; Wood, S.J.; Steavenson, S.; Jiang, Y.; Wu, G.M.; Anafi, D.; Kaufman, S.A.; Martin, F.; Sitney, K.; Denis, P.; et al. Both familial Parkinson’s disease mutations accelerate alpha-synuclein aggregation. J. Biol. Chem. 1999, 274, 9843–9846. [Google Scholar]
- Khalaf, O.; Fauvet, B.; Oueslati, A.; Dikiy, I.; Mahul-Mellier, A.L.; Ruggeri, F.S.; Mbefo, M.; Vercruysse, F.; Dietler, G.; Lee, S.J.; et al. The H50Q mutation enhances α-synuclein aggregation, secretion and toxicity. J. Biol. Chem. 2014. [Google Scholar] [CrossRef]
- Ibáñez, P.; Bonnet, A.M.; Débarges, B.; Lohmann, E.; Tison, F.; Pollak, P.; Agid, Y.; Dürr, A.; Brice, A. Causal relation between alpha-synuclein gene duplication and familial Parkinson’s disease. Lancet 2004, 364, 1169–1171. [Google Scholar]
- Singleton, A.B.; Farrer, M.; Johnson, J.; Singleton, A.; Hague, S.; Kachergus, J.; Hulihan, M.; Peuralinna, T.; Dutra, A.; Nussbaum, R.; et al. alpha-Synuclein locus triplication causes Parkinson’s disease. Science 2003. [Google Scholar] [CrossRef]
- Tanner, C.M.; Kamel, F.; Ross, W.; Hoppin, J.A.; Goldman, S.M.; Korell, M.; Marras, C.; Bhudhikanok, G.S.; Kasten, M.; Chade, A.R.; et al. Rotenone, paraquat, and Parkinson’s disease. Environ. Health Perspect. 2011, 119, 866–872. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Su, B.; Liu, W.; He, X.; Gao, Y.; Castellani, R.J.; Perry, G.; Smith, M.A.; Zhu, X. DLP1-dependent mitochondrial fragmentation mediates 1-methyl-4-phenylpyridinium toxicity in neurons: Implications for Parkinson’s disease. Ageing Cell. 2011, 10, 807–823. [Google Scholar] [CrossRef]
- Hernán, M.A.; Takkouche, B.; Caamaño-Isorna, F.; Gestal-Otero, J.J. A meta-analysis of coffee drinking, cigarette smoking, and the risk of Parkinson’s disease. Ann. Neurol. 2002, 52, 276–284. [Google Scholar]
- Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. Alpha-synuclein in Lewy bodies. Nature 1997, 388, 839–840. [Google Scholar] [CrossRef] [PubMed]
- Al-Chalabi, A.; Dürr, A.; Wood, N.W.; Parkinson, M.H.; Camuzat, A.; Hulot, J.S.; Morrison, K.E.; Renton, A.; Sussmuth, S.D.; Landwehrmeyer, B.G.; et al. Genetic variants of the alpha-synuclein gene SNCA are associated with multiple system atrophy. PLoS One 2009, 4, e7114. [Google Scholar]
- Hanna, P.A.; Jankovic, J.; Kirkpatrick, J.B. Multiple system atrophy: The putative causative role of environmental toxins. Arch. Neurol. 1999, 56, 90–94. [Google Scholar] [CrossRef] [PubMed]
- Vidal, J.S.; Vidailhet, M.; Elbaz, A.; Derkinderen, P.; Tzourio, C.; Alpérovitch, A. Risk factors of multiple system atrophy: A case-control study in French patients. Mov. Disord. 2008, 23, 797–803. [Google Scholar] [CrossRef] [PubMed]
- Iwai, A.; Masliah, E.; Yoshimoto, M.; Ge, N.; Fianagan, L.; Rohan de Silva, H.A.; Kittei, A.; Saitoh, T. The precursor protein of non-aβ component of Alzheimer’s disease amyloid is a presynaptic protein of the central nervous system. Neuron 1995, 14, 467–475. [Google Scholar] [CrossRef] [PubMed]
- Maroteaux, L.; Campanelli, J.T.; Scheller, R.H. Synuclein: A neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 1998, 8, 2804–2815. [Google Scholar]
- Clayton, D.F.; George, J.M. Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 1999, 58, 120–129. [Google Scholar] [CrossRef] [PubMed]
- Burré, J.; Sharma, M.; Tsetsenis, T.; Buchman, V.; Etherton, M.R.; Südhof, T.C. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 2010, 329, 1663–1667. [Google Scholar]
- Nielsen, M.S.; Vorum, H.; Lindersson, E.; Jensen, P.H. Ca2+ binding to alpha-synuclein regulates ligand binding and oligomerization. J. Biol. Chem. 2001, 276, 22680–22684. [Google Scholar] [CrossRef] [PubMed]
- Giasson, B.I.; Murray, I.V.; Trojanowski, J.Q.; Lee, V.M. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J. Biol. Chem. 2001, 276, 2380–2386. [Google Scholar] [CrossRef] [PubMed]
- Eliezer, D.; Kutluay, E.; Bussell, R., Jr.; Browne, G. Conformational properties of alpha-synuclein in its free and lipid-associated states. J. Mol. Biol. 2001, 307, 1061–1073. [Google Scholar] [CrossRef] [PubMed]
- Davidson, W.S.; Jonas, A.; Clayton, D.F.; George, J.M. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 1998, 273, 9443–9449. [Google Scholar] [CrossRef] [PubMed]
- Wietek, J.; Haralampiev, I.; Amoussouvi, A.; Herrmann, A.; Stöckl, M. Membrane bound α-synuclein is fully embedded in the lipid bilayer while segments with higher flexibility remain. FEBS Lett. 2013, 587, 2572–2577. [Google Scholar] [CrossRef] [PubMed]
- Wood, S.J.; Wypych, J.; Steavenson, S.; Lousis, J-C.; Citron, M.; Biere, A.L. α-Synuclein fibrillogenesis is nucleation dependent: Implications for the pathogenesis of Parkinson’s disease. J. Biol. Chem. 1999, 274, 19509–19512. [Google Scholar] [CrossRef] [PubMed]
- Zibaee, S.; Jakes, R.; Fraser, G.; Serpell, L.C.; Crowther, R.A.; Goedert, M. Sequence determinants for amyloid fibrillogenesis of human alpha-synuclein. J. Mol. Biol. 2007, 374, 454–464. [Google Scholar] [CrossRef] [PubMed]
- Narayanan, V.; Scarlata, S. Membrane binding and self-association of alpha-synucleins. Biochemistry 2001, 40, 9927–9934. [Google Scholar] [CrossRef] [PubMed]
- Lokappa, S.B.; Suk, J.E.; Balasubramanian, A.; Samanta, S.; Situ, A.J.; Ulmer, T.S. Sequence and membrane determinants of the random coil-helix transition of α-synuclein. J. Mol. Biol. 2014, 426, 2130–2144. [Google Scholar] [CrossRef] [PubMed]
- McLean, P.J.; Kawamata, H.; Ribich, S.; Hyman, T. Membrane association and protein conformation of α-synuclein in intact neurons. J. Biol. Chem. 2000, 275, 8812–8816. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.H.; Wislet-Gendebien, S.; Samuel, F.; Visanji, N.P.; Zhang, G.; Marsilio, D.; Langman, T.; Fraser, P.E.; Tandon, A. α-Synuclein membrane association is regulated by the Rab3a recycling machinery and presynaptic activity. J. Biol. Chem. 2013, 288, 7438–7449. [Google Scholar] [CrossRef] [PubMed]
- Mak, S.R.; McCormack, A.L.; Langston, J.W.; Kordower, J.H.; di Monte, D.A. Decreased α-synuclein expression in the ageing mouse substantia nigra. Exp. Neurobiol. 2009, 220, 359–365. [Google Scholar] [CrossRef]
- Grundemann, J.; Schlaudraff, F.; Haeckel, O.; Liss, B. Elevated α-synuclein mRNA levels in individual UV-laser-microdissected dopaminergic substantia nigra neurons in Idiopathic Parkinson’s disease. Nucleic Acids Res. 2008, 36, e38. [Google Scholar] [CrossRef] [PubMed]
- Outeiro, T.F.; Putcha, P.; Tetzlaff, J.E.; Spoelgen, R.; Koker, M.; Carvalho, F.; Hyman, B.T.; McLean, P.J. Formation of toxic oligomeric alpha-synuclein species in living cells. PLoS One 2008, 3, e1867. [Google Scholar] [CrossRef] [PubMed]
- Esteves, A.R.; Arduíno, D.M.; Silva, D.F.; Oliveira, C.R.; Cardoso, S.M. Mitochondrial dysfunction: The Road to alpha-synuclein oligomerization in PD. Parkinsons Dis. 2011. [Google Scholar] [CrossRef]
- Kalia, L.V.; Kalia, S.K.; McLean, P.J.; Lozano, A.M.; Lang, A.E. α-Synuclein oligomers and clinical implications for Parkinson disease. Ann. Neurol. 2013, 73, 155–169. [Google Scholar] [CrossRef] [PubMed]
- Yasuda, T.; Nakata, Y.; Mochizuki, H. α-Synuclein and neuronal cell death. Mol. Neurobiol. 2013, 47, 466–483. [Google Scholar] [CrossRef] [PubMed]
- Luth, E.S.; Stavrovskaya, I.G.; Bartels, T.; Kristal, B.S.; Selkoe, D.J. Soluble, prefibrillar α-synuclein oligomers promote complex I-dependent, Ca2+-induced mitochondrial dysfunction. J. Biol. Chem. 2014. [Google Scholar] [CrossRef]
- Danzer, K.M.; Haasen, D.; Karow, A.R.; Moussaud, S.; habeck, M.; Giese, A.; Kretzschmar, H.; Hengerer, B.; Kostka, M. Different species of alpha-synuclein oligomers induce calcium influx and seeding. J. Neurosci. 2007, 27, 9220–9232. [Google Scholar] [CrossRef] [PubMed]
- Bartels, T.; Choi, J.C.; Selkoe, D.J. α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 2011, 477, 107–111. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Perovic, W.; Chittuluru, J.; Kaganovich, A.; Nguyen, L.T.T.; Liao, J.; Auclair, J.R.; Johnson, D.; Landeru, D.; Simorellis, A.K.; et al. A soluble α-synuclein construct forms a dynamic tetramer. Proc. Natl. Acad. Sci. USA 2011, 108, 17797–17802. [Google Scholar] [CrossRef] [PubMed]
- Smith, W.W.; Margolis, R.L.; Li, X.; Troncoso, J.C.; Lee, M.K.; Dawson, V.L.; Dawson, T.M.; Iwatsubo, T.; Ross, C.A. Alpha-synuclein phosphorylation enhances eosinophilic cytoplasmic inclusion formation in SH-SY5Y cells. J. Neurosci. 2005, 25, 5544–5552. [Google Scholar] [CrossRef] [PubMed]
- Lu, Y.; Prudent, M.; Fauvet, B.; Lashuel, H.A.; Girault, H.H. Phosphorylation of α-Synuclein at Y125 and S129 alters its metal binding properties: Implications for understanding the role of α-synuclein in the pathogenesis of Parkinson’s disease and related disorders. ACS Chem. Neurosci. 2011, 2, 667–675. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.L.; Franz, K.J. Phosphorylation of an alpha-synuclein peptide fragment enhances metal binding. J. Am. Chem. Soc. 2005, 127, 9662–9663. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.P.; Walker, D.E.; Goldstein, J.M.; de Laat, R.; Banducci, K.; Caccavello, R.J.; Barbour, R.; Huang, J.; Kling, K.; Lee, M.; et al. Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease. J. Biol. Chem. 2006, 281, 29739–29752. [Google Scholar] [CrossRef] [PubMed]
- Uversky, V.N.; Yamin, G.; Munishkina, L.A.; Karymov, M.A.; Millett, I.S.; Doniach, S.; Lyubchenko, Y.L.; Fink, A.L. Effects of nitration on the structure and aggregation of alpha-synuclein. Mol. Brain Res. 2005, 134, 84–102. [Google Scholar] [CrossRef] [PubMed]
- Chavarría, C.; Souza, J.M. Oxidation and nitration of α-synuclein and their implications in neurodegenerative diseases. Arch. Biochem. Biophys. 2013, 533, 25–32. [Google Scholar]
- Glaser, C.B.; Yamin, G.; Uversky, V.N.; Fink, A.L. Methionine oxidation, alpha-synuclein and Parkinson’s disease. Biochim. Biophys. Acta 2005, 1703, 157–169. [Google Scholar] [CrossRef]
- Uversky, V.N.; Yamin, G.; Souillac, P.O.; Goers, J.; Glaser, C.B.; Fink, A.L. Methionine oxidation inhibits fibrillation of human alpha-synuclein in vitro. FEBS Lett. 2002, 517, 239–244. [Google Scholar] [CrossRef] [PubMed]
- Feany, M.B.; Bender, W.W. A Drosophila model of Parkinson’s disease. Nature 2000, 404, 394–398. [Google Scholar] [CrossRef] [PubMed]
- Kaul, S.; Anantharam, V.; Kanthasamy, A.; Kanthasamy, A.G. Wild-type alpha-synuclein interacts with pro-apoptotic proteins PKCdelta and BAD to protect dopaminergic neuronal cells against MPP+-induced apoptotic cell death. Brain Res. Mol. Brain Res. 2005, 139, 137–152. [Google Scholar] [PubMed]
- Pham, C.L.; Cappai, R. The interplay between lipids and dopamine on α-synuclein oligomerization and membrane binding. Biosci. Rep. 2013, 33, e00074. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.J.; Bae, E.J.; Lee, S.J. Extracellular α-synuclein—A novel and crucial factor in Lewy body diseases. Nat. Rev. Neurol. 2014, 10, 92–98. [Google Scholar] [CrossRef] [PubMed]
- Alvarez-Erviti, L.; Seow, Y.; Schapira, A.H.; Gardiner, C.; Sargent, I.L.; Wood, M.J.; Cooper, J.M. Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission. Neurobiol. Dis. 2011, 42, 360–367. [Google Scholar]
- Danzer, K.M.; Kranich, L.R.; Ruf, W.P.; Cagsal-Getkin, O.; Winslow, A.R.; Zhu, L.; Vanderburg, C.R.; McLean, P.J. Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener. 2012. [Google Scholar] [CrossRef]
- Kovacs, G.G.; Breydo, L.; Green, R.; Kis, V.; Puska, G.; Lőrincz, P.; Perju-Dumbrava, L.; Giera, R.; Pirker, W.; Lutz, M.; et al. Intracellular processing of disease-associated α-synuclein in the human brain suggests prion-like cell-to-cell spread. Neurobiol. Dis. 2014. [Google Scholar] [CrossRef]
- Chang, C.; Lang, H.; Geng, N.; Wang, J.; Li, N.; Wang, X. Exosomes of BV-2 cells induced by alpha-synuclein: Important mediator of neurodegeneration in PD. Neurosci. Lett. 2013, 26, 190–195. [Google Scholar] [CrossRef]
- Kordower, J.H.; Chu, Y.; Hauser, R.A.; Freeman, T.B.; Olanow, C.W. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson’s disease. Nat. Med. 2008, 14, 504–506. [Google Scholar] [CrossRef] [PubMed]
- Li, J.Y.; Englund, E.; Holton, J.L.; Soulet, D.; Hagell, P.; Lees, A.J.; Lashley, T.; Quinn, N.P.; Rehncrona, S.; Bjorklund, A.; et al. Lewy bodies in grafted neurons in subjects with Parkinson’s disease suggest host-to-graft disease propagation. Nat. Med. 2008, 14, 501–503. [Google Scholar] [CrossRef] [PubMed]
- Sims-Robertson, C.; Hur, J.; Hayes, J.M.; Dauch, J.R.; Keller, P.J.; Brooks, S.V.; Feldman, E.L. The role of oxidative stress in nervous system aging. PLoS One 2013, 8, e68011. [Google Scholar]
- Castro, R.; Suarez, E.; Kraiselburd, E.; Isidro, A.; Paz, J.; Ferder, L.; Ayala-Torres, S. Aging increases mitochondrial DNA damage and oxidative stress in liver of rhesus monkeys. Exp. Gerentol. 2012, 47, 29–37. [Google Scholar] [CrossRef]
- Quilty, M.C.; King, A.E.; Gai, W.P.; Pountney, D.L.; West, A.K.; Vickers, J.C.; Dickson, T.C. Alpha-synuclein is upregulated in neurons in response to chronic oxidative stress and is associated with neuroprotection. Exp. Neurol. 2006, 199, 249–256. [Google Scholar] [CrossRef] [PubMed]
- Surmeier, D.J.; Schumacker, P.T. Calcium, bioenergetics, and neuronal vulnerability in Parkinson’s disease. J. Biol. Chem. 2013, 288, 10736–10741. [Google Scholar] [CrossRef] [PubMed]
- Fairless, R.; Williams, S.K.; Diem, R. Dysfunction of neuronal calcium signalling in neuroinflammation and neurodegeneration. Cell Tissue Res. 2013. [Google Scholar] [CrossRef]
- Lowe, R.; Pountney, D.L.; Jensen, P.H.; Gai, W.P.; Voelcker, N.H. Calcium(II) selectively induces alpha-synuclein annular oligomers via interaction with the C-terminal domain. Protein Sci. 2004, 13, 3245–3252. [Google Scholar] [CrossRef] [PubMed]
- Brini, M.; Calì, T.; Ottolini, D.; Carafoli, E. Neuronal calcium signaling: Function and dysfunction. Cell. Mol. Life Sci. 2014. [Google Scholar] [CrossRef]
- Michaelis, M.L.; Bigelow, D.J.; Schöneich, C.; Williams, T.D.; Ramonda, L.; Yin, D.; Hühmer, A.F.; Yao, Y.; Gao, J.; Squier, T.C. Decreased plasma membrane calcium transport activity in aging brain. Life Sci. 1996, 59, 405–412. [Google Scholar] [CrossRef] [PubMed]
- Duckles, S.P.; Tsai, H.; Buchholz, J.N. Evidence for decline in intracellular calcium buffering in adrenergic nerves of aged rats. Life Sci. 1996, 58, 2029–2035. [Google Scholar] [CrossRef] [PubMed]
- Schwaller, B. Calretinin: From a “simple” Ca2+ buffer to a multifunctional protein implicated in many biological processes. Front. Neuroanat. 2014. [Google Scholar] [CrossRef]
- Perier, C.; Vila, M. Mitochondrial biology and Parkinson’s disease. Cold Spring Harb. Prospect. Med. 2012. [Google Scholar] [CrossRef]
- Bu, J.; Sathyendra, V.; Nagykery, N.; Geula, C. Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp. Neurol. 2003, 182, 220–231. [Google Scholar] [CrossRef] [PubMed]
- German, D.C.; Manaye, K.F.; Sonsalla, P.K.; Brooks, B.A. Midbrain dopaminergic cell loss in Parkinson’s disease and MPTP-induced Parkinsonism: Sparing of calbindin-D 28K containing cells. Ann. NY Acad. Sci. 1992, 648, 42–62. [Google Scholar] [CrossRef] [PubMed]
- Tsuboi, K.; Kimber, T.A.; Shults, C.W. Calretinin-containing axon and neurons are resistant to intrastriatal 6-hydroxydopamine. Brain Res. 2000, 866, 55–64. [Google Scholar] [CrossRef] [PubMed]
- Kim, B.G.; Shin, D.H.; Jeon, G.S.; Seo, J.H.; Kim, Y.W.; Jeon, B.S.; Cho, S.S. Relative sparing of calretinin containin neurons in the substantia nigra of 6-OHDA treated rat Parkinsonian model. Brain Res. 2000, 7, 162–165. [Google Scholar] [CrossRef]
- Yamada, T.; McGeer, P.L.; Bainbridge, K.G.; McGeer, E.C. Relative sparing in Parkinson’s disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res. 1990, 526, 303–307. [Google Scholar] [CrossRef] [PubMed]
- Nath, S.; Goodwin, J.; Engelborghs, Y.; Pountney, D.L. Raised calcium promotes α-synuclein aggregate formation. Mol. Cell. Neurosci. 2011, 46, 516–526. [Google Scholar] [CrossRef] [PubMed]
- Follett, J.; Darlow, B.; Wong, M.B.; Goodwin, J.; Pountney, D.L. Potassium depolarization and raised calcium induces α-synuclein aggregates. Neurotox. Res. 2013, 23, 378–392. [Google Scholar] [CrossRef] [PubMed]
- Kopecky, B.J.; Liang, R.; Bao, J. T-type calcium channel blockers as neuroprotective agents. Eur. J. Physiol. 2014, 466, 757–765. [Google Scholar] [CrossRef]
- Chan, S.C.; Guzman, J.N.; Ilijic, E.; Mecer, J.N.; Rick, C.; Tkatch, T.; Meredith, G.E.; Surmeier, D.J. “Rejuvenation” protects neurons in mouse models of Parkinson’s disease. Nature 2007, 447, 1081–1089. [Google Scholar] [CrossRef] [PubMed]
- Gasper, P.; Ben Jelloun, N.; Febvret, A. Sparing of the dopaminergic neurons containing calbindin-D28k and the loss of dopaminergic mesocortical projections in weaver mice. Neuroscience 1994, 61, 293–305. [Google Scholar] [CrossRef] [PubMed]
- Weetman, J.; Wong, M.B.; Sharry, S.; Rcom-H’cheo-Gauthier, A.; Gai, W.P.; Meedeniya, A.; Pountney, D.L. Increased SUMO-1 expression in the unilateral rotenone-lesioned mouse model of Parkinson’s disease. Neurosci. Lett. 2013, 544, 119–124. [Google Scholar] [CrossRef] [PubMed]
- Rcom-H’cheo-Gauthier, A.; Meedeniya, A.; Pountney, D.L.; School of Medical Science, Griffith University, Gold Coast, Australia. Unpublished work. 2014.
- Goodwin, J.; Nath, S.; Engelborghs, Y.; Pountney, D.L. Raised calcium and oxidative stress cooperatively promote alpha-synuclein aggregate formation. Neurochem. Int. 2013, 62, 703–711. [Google Scholar] [CrossRef] [PubMed]
- Hettiarachchi, N.T.; Parker, A.; Dallas, M.L.; Pennington, K.; Hung, C.C.; Pearson, H.A.; Boyle, J.P.; Robinson, P.; Peers, C. α-Synuclein modulation of Ca2+ signaling in human neuroblastoma (SH-SY5Y) cells. J. Neurochem. 2009, 111, 1192–1201. [Google Scholar] [CrossRef] [PubMed]
- Melachroinou, K.; Xilouri, M.; Emmanouilidou, E.; Masgrau, R.; Papazafiri, P.; Stefanis, L.; Vekrellis, K. Deregulation of calcium homeostasis mediates secreted alpha-synuclein-induced neurotoxicity. Neurobiol. Aging 2013, 34, 2853–2865. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reznichenko, L.; Cheng, Q.; Nizar, K.; Gratiy, S.L.; Saisan, P.A.; Rockenstein, E.M.; González, T.; Patrick, C.; Spencer, B.; Desplats, P.; et al. In vivo alterations in calcium buffering capacity in transgenic mouse model of synucleinopathy. J. Neurosci. 2012, 32, 9992–9998. [Google Scholar] [CrossRef] [PubMed]
- Cali, T.; Ottolini, D.; Negro, A.; Brini, M. alpha-Synuclein controls mitochondrial calcium homeostasis by enhancing endoplasmic reticulum-mitochondria interactions. J. Biol. Chem. 2012, 287, 17914–17929. [Google Scholar] [CrossRef] [PubMed]
- Dryanovski, D.I.; Guzman, J.N.; Xie, Z.; Galteri, D.J.; Volpicelli-Daley, L.A.; Lee, V.M.; Miller, R.J.; Scumacker, P.T.; Surmeier, D.J. Calcium entry and alpha-synuclein inclusions elevate dendritic mitochondrial oxidant stress in dopaminergic neurons. J. Neurosci. 2013, 33, 10154–10164. [Google Scholar] [CrossRef] [PubMed]
- Buttner, S.; Faes, L.; Reichelt, W.N.; Broeskamp, F.; Habernig, L.; Benke, S.; Kourtis, N.; Ruli, D.; Carmona-Gutierrez, D.; Eisenberg, T.; et al. The Ca2+/Mn2+ ion-pump PMR1 links elevation of cytosolic Ca2+ levels to alpha-synuclein toxicity in Parkinson’s disease models. Cell Death Differ. 2013, 20, 465–477. [Google Scholar] [CrossRef] [PubMed]
- Parihar, M.S.; Parihar, A.; Fujita, M.; Hashimoto, M.; Ghafourifar, P. Mitochondrial association of alpha-synuclein causes oxidative stress. Cell. Mol. Life Sci. 2008, 65, 1272–1284. [Google Scholar] [CrossRef] [PubMed]
- Hashimoto, M.; Hsu, L.J.; Rockenstein, E.; Takenouchi, T.; Mallory, M.; Masliah, E. α-Synuclein protects against oxidative stress via inactivation of the c-Jun N-terminal kinase stress-signalling pathway in neuronal cells. J. Biol. Chem. 2002, 277, 11465–11472. [Google Scholar] [CrossRef] [PubMed]
- Stefanova, N.; Reindl, M.; Neumann, M.; Haass, C.; Poewe, W.; Kahle, P.J.; Wenning, G.K. Oxidative stress in transgenic mice with oligodendroglial α-synuclein overexpression replicates the characteristic neuropathology of multiple system atrophy. Am. J. Pathol. 2005, 166, 869–876. [Google Scholar] [CrossRef] [PubMed]
- Nath, S.; Meuvis, J.; Hendrix, J.; Carl, S.A.; Engelborghs, Y. Early aggregation steps in alpha-synuclein as measured by FCS and FRET: Evidence for a contagious conformational change. Biophys. J. 2010, 98, 1302–1311. [Google Scholar] [CrossRef] [PubMed]
- Krishnan, S.; Chi, E.Y.; Wood, S.J.; Kendrick, B.S.; Li, C.; Garzon-Rodrigues, W.; Wypych, J.; Randolph, T.W.; Narhi, L.O.; Biere, A.L.; et al. Oxidative dimer formation is the critical rate-limiting step for Parkinson’s disease α-synuclein fibrillogenesis. Biochemistry 2003, 42, 829–837. [Google Scholar] [CrossRef] [PubMed]
- Goldberg, J.A.; Guzman, J.N.; Estep, C.M.; Ilijic, E.; Kondapalli, J.; Sanchez-Padilla, J.; Surmerier, D.J. Calcium entry induces mitochondrial oxidant stress in vagal neurons at risk in Parkinson’s disease. Nat. Neurosci. 2012, 15, 1414–1421. [Google Scholar] [CrossRef] [PubMed]
- Schapira, A.H.; Olanow, C.W.; Greenamyre, J.T.; Bezard, E. Slowing of neurodegeneration in Parkinson’s disease and Huntington’s disease: Future therapeutic perspectives. Lancet 2014. [Google Scholar] [CrossRef]
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Rcom-H'cheo-Gauthier, A.; Goodwin, J.; Pountney, D.L. Interactions between Calcium and Alpha-Synuclein in Neurodegeneration. Biomolecules 2014, 4, 795-811. https://doi.org/10.3390/biom4030795
Rcom-H'cheo-Gauthier A, Goodwin J, Pountney DL. Interactions between Calcium and Alpha-Synuclein in Neurodegeneration. Biomolecules. 2014; 4(3):795-811. https://doi.org/10.3390/biom4030795
Chicago/Turabian StyleRcom-H'cheo-Gauthier, Alex, Jacob Goodwin, and Dean L. Pountney. 2014. "Interactions between Calcium and Alpha-Synuclein in Neurodegeneration" Biomolecules 4, no. 3: 795-811. https://doi.org/10.3390/biom4030795