Mitochondrion- and Endoplasmic Reticulum-Induced SK Channel Dysregulation as a Potential Origin of the Selective Neurodegeneration in Parkinson’s Disease

Mitochondrial dysfunction and metabolic issues are known to have strong implications in the pathogenesis of Parkinson’s disease (PD). But it is also known that the neuronal loss leading to PD symptoms is selective for particular areas of the brain (see Chap. 1). In particular, the characteristic motor symptoms of PD are mainly due to abnormal neuronal activity in the basal ganglia, through the degeneration of substantia nigra pars compacta (SNc), but not ventral tegmental area (VTA), dopaminergic (DA) neurons. How a metabolic dysfunction triggers such a selective loss is considered from a range of perspectives in several contributions to this volume. The aim of this chapter is to investigate the potential role of small conductance calcium-activated potassium (SK) channels in this selective degeneration.

[1]  Eugene M. Izhikevich,et al.  Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting , 2006 .

[2]  F. Sterky,et al.  Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons in vivo , 2011, Proceedings of the National Academy of Sciences.

[3]  U. Misgeld,et al.  Two pathways for the activation of small-conductance potassium channels in neurons of substantia nigra pars reticulata , 2005, Neuroscience.

[4]  J. Brotchie,et al.  The serotonergic system in Parkinson's disease , 2011, Progress in Neurobiology.

[5]  B. Bunney,et al.  Repetitive firing properties of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca2+-activated K+ conductance , 2004, Experimental Brain Research.

[6]  M. Farrer,et al.  Missing pieces in the Parkinson's disease puzzle , 2010, Nature Medicine.

[7]  Y. Kagawa,et al.  Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. , 1989, Biochemical and biophysical research communications.

[8]  E. Hirsch,et al.  Regional vulnerability of mesencephalic dopaminergic neurons prone to degenerate in Parkinson's disease: A post-mortem study in human control subjects , 2006, Neurobiology of Disease.

[9]  Jean-François Liégeois,et al.  SK channels control the firing pattern of midbrain dopaminergic neurons in vivo , 2005, The European journal of neuroscience.

[10]  J. Bonnar,et al.  Letter: Prostaglandins and pre-eclampsia. , 1974, Lancet.

[11]  Todd B. Sherer,et al.  Chronic systemic pesticide exposure reproduces features of Parkinson's disease , 2000, Nature Neuroscience.

[12]  B. Bean,et al.  Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons , 2007, The Journal of Neuroscience.

[13]  Eric L. Schwartz,et al.  Computational Neuroscience , 1993, Neuromethods.

[14]  D. Johnston,et al.  Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. , 1995, Science.

[15]  B. Hille,et al.  Ionic channels of excitable membranes , 2001 .

[16]  A. H. V. Schapira,et al.  MITOCHONDRIAL COMPLEX I DEFICIENCY IN PARKINSON'S DISEASE , 1989, The Lancet.

[17]  D. Surmeier,et al.  A molecular basis for the increased vulnerability of substantia nigra dopamine neurons in aging and Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

[18]  D James Surmeier,et al.  What causes the death of dopaminergic neurons in Parkinson's disease? , 2010, Progress in brain research.

[19]  M. Ungless,et al.  Hyperexcitable substantia nigra dopamine neurons in PINK1- and HtrA2/Omi-deficient mice. , 2010, Journal of neurophysiology.

[20]  A. Noma.  Ionic mechanisms of the cardiac pacemaker potential. , 1996, Japanese heart journal.

[21]  C. Marsden,et al.  MITOCHONDRIAL-FUNCTION IN PARKINSONS-DISEASE , 1992 .

[22]  Terina N. Martinez,et al.  Toxin models of mitochondrial dysfunction in Parkinson's disease. , 2012, Antioxidants & redox signaling.

[23]  Ted M. Dawson,et al.  Genetic Animal Models of Parkinson's Disease , 2010, Neuron.

[24]  D. James Surmeier,et al.  ‘Rejuvenation’ protects neurons in mouse models of Parkinson’s disease , 2007, Nature.

[25]  D. Surmeier,et al.  Calcium, ageing, and neuronal vulnerability in Parkinson's disease , 2007, The Lancet Neurology.

[26]  J. Duda.  Olfactory system pathology as a model of Lewy neurodegenerative disease , 2010, Journal of the Neurological Sciences.

[27]  H. Braak,et al.  Staging of brain pathology related to sporadic Parkinson’s disease , 2003, Neurobiology of Aging.

[28]  C. Marsden,et al.  Brain, skeletal muscle and platelet homogenate mitochondrial function in Parkinson's disease. , 1992, Brain : a journal of neurology.

[29]  J. Tepper,et al.  GABAergic Afferents Activate Both GABAA and GABAB Receptors in Mouse Substantia Nigra Dopaminergic Neurons In Vivo , 2008, The Journal of Neuroscience.

[30]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: burst firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Steven W. Johnson,et al.  Apamin increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons , 1993, Brain Research.

[32]  G. Westbrook,et al.  SK channel regulation of dendritic excitability and dendrodendritic inhibition in the olfactory bulb. , 2005, Journal of neurophysiology.

[33]  M. Stocker.  Ca2+-activated K+ channels: molecular determinants and function of the SK family , 2004, Nature Reviews Neuroscience.

[34]  J. Parks,et al.  Abnormalities of the electron transport chain in idiopathic parkinson's disease , 1989, Annals of neurology.

[35]  N. Wood,et al.  Expanding insights of mitochondrial dysfunction in Parkinson's disease , 2006, Nature Reviews Neuroscience.

[36]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[37]  D. Turnbull,et al.  MITOCHONDRIAL FUNCTION IN PARKINSON'S DISEASE , 1989, The Lancet.

[38]  P. Sah,et al.  Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. , 1992, Journal of neurophysiology.

[39]  D. James Surmeier,et al.  Robust Pacemaking in Substantia Nigra Dopaminergic Neurons , 2009, The Journal of Neuroscience.

[40]  I. Engberg,et al.  Nifedipine‐ and omega‐conotoxin‐sensitive Ca2+ conductances in guinea‐pig substantia nigra pars compacta neurones. , 1993, The Journal of physiology.

[41]  M. Bevan,et al.  Cellular Mechanisms Underlying Burst Firing in Substantia Nigra Dopamine Neurons , 2009, The Journal of Neuroscience.

[42]  T. Takeuchi,et al.  Expression of Ca(2+)-activated K(+) channels, SK3, in the interstitial cells of Cajal in the gastrointestinal tract. , 2001, American journal of physiology. Cell physiology.

[43]  K. H. Lee,et al.  Pregnenolone sulfate enhances spontaneous glutamate release by inducing presynaptic Ca2+-induced Ca2+ release , 2010, Neuroscience.

[44]  T. González-Hernández,et al.  Vulnerability of Mesostriatal Dopaminergic Neurons in Parkinson's Disease , 2010, Front. Neuroanat..

[45]  Charles J. Wilson,et al.  Apamin-Sensitive Small Conductance Calcium-Activated Potassium Channels, through their Selective Coupling to Voltage-Gated Calcium Channels, Are Critical Determinants of the Precision, Pace, and Pattern of Action Potential Generation in Rat Subthalamic Nucleus Neurons In Vitro , 2003, The Journal of Neuroscience.

[46]  R. Takahashi,et al.  Expanding insights on the involvement of endoplasmic reticulum stress in Parkinson's disease. , 2007, Antioxidants & redox signaling.

[47]  D. Surmeier,et al.  Calcium homeostasis, selective vulnerability and Parkinson's disease , 2009, Trends in Neurosciences.

[48]  C. Oliveira,et al.  Endoplasmic reticulum and mitochondria interplay mediates apoptotic cell death: Relevance to Parkinson's disease , 2009, Neurochemistry International.

[49]  D. Bourdette,et al.  Mitochondrial calcium and its regulation in neurodegeneration induced by oxidative stress , 2011, The European journal of neuroscience.

[50]  Jean-François Liégeois,et al.  SK channel blockade promotes burst firing in dorsal raphe serotonergic neurons , 2008, The European journal of neuroscience.

[51]  M. Brini,et al.  Mitochondria, calcium, and endoplasmic reticulum stress in Parkinson's disease. , 2011, BioFactors.

[52]  Paul T. Schumacker,et al.  Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1 , 2010, Nature.

[53]  D. Noble,et al.  The surprising heart: a review of recent progress in cardiac electrophysiology. , 1984, The Journal of physiology.

[54]  H. Pape,et al.  Burst discharges in neurons of the thalamic reticular nucleus are shaped by calcium-induced calcium release. , 2009, Cell calcium.

[55]  J. Adelman,et al.  Regional distribution of SK3 mRNA‐containing neurons in the adult and adolescent rat ventral midbrain and their relationship to dopamine‐containing cells , 2004, Synapse.

[56]  H. Braak,et al.  Gastric α-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology , 2006, Neuroscience Letters.

[57]  G. Deuschl,et al.  Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. , 2008, Journal of neurophysiology.

[58]  J. Adelman,et al.  Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin , 2001, Nature.

[59]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: single spike firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  C. Marsden,et al.  Anatomic and Disease Specificity of NADH CoQ1 Reductase (Complex I) Deficiency in Parkinson's Disease , 1990, Journal of neurochemistry.

[61]  N. Marrion,et al.  Small-Conductance, Calcium-Activated Potassium Channels from Mammalian Brain , 1996, Science.

[62]  S. Snyder,et al.  Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6 -tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Adelman,et al.  Small conductance Ca2+‐activated K+ channels and calmodulin , 2004, The Journal of physiology.

[64]  B. Sabatini,et al.  SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines , 2005, Nature Neuroscience.

[65]  D. Surmeier,et al.  The L-type channel antagonist isradipine is neuroprotective in a mouse model of Parkinson's disease , 2011, Neurobiology of Disease.

[66]  D. Surmeier,et al.  Calcium, cellular aging, and selective neuronal vulnerability in Parkinson's disease. , 2010, Cell calcium.

[67]  T. González-Hernández,et al.  Phenotype, compartmental organization and differential vulnerability of nigral dopaminergic neurons. , 2009, Journal of neural transmission. Supplementum.

[68]  E. Bézard,et al.  A tale on animal models of Parkinson's disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

[69]  Jochen Roeper,et al.  K-ATP channels promote the differential degeneration of dopaminergic midbrain neurons , 2005, Nature Neuroscience.

[70]  A. Lees,et al.  Ageing and Parkinson's disease: substantia nigra regional selectivity. , 1991, Brain : a journal of neurology.

[71]  B. Lancaster,et al.  SK channels and the varieties of slow after‐hyperpolarizations in neurons , 2003, The European journal of neuroscience.

[72]  Rodolphe Sepulchre,et al.  How Modeling Can Reconcile Apparently Discrepant Experimental Results: The Case of Pacemaking in Dopaminergic Neurons , 2011, PLoS Comput. Biol..

[73]  Zhaoyang Feng,et al.  Dysregulated LRRK2 Signaling in Response to Endoplasmic Reticulum Stress Leads to Dopaminergic Neuron Degeneration in C. elegans , 2011, PloS one.

[74]  Interplay between ER Ca2+ uptake and release fluxes in neurons and its impact on [Ca2+] dynamics. , 2004, Biological research.

[75]  P. Christophersen,et al.  Pharmacological modulation of the gating properties of small conductance Ca2+-activated K+ channels alters the firing pattern of dopamine neurons in vivo. , 2010, Journal of neurophysiology.

[76]  J. Obeso,et al.  Functional organization of the basal ganglia: Therapeutic implications for Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[77]  A. Schapira.  Mitochondria in the aetiology and pathogenesis of Parkinson's disease , 2008, The Lancet Neurology.

[78]  Charles J. Wilson,et al.  A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons. , 2010, Journal of neurophysiology.

[79]  John P. Horn,et al.  Cav1.3 Channel Voltage Dependence, Not Ca2+ Selectivity, Drives Pacemaker Activity and Amplifies Bursts in Nigral Dopamine Neurons , 2009, The Journal of Neuroscience.

[80]  D. Jacobowitz,et al.  A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[81]  B. Bunney,et al.  Effects of apamin on the discharge properties of putative dopamine-containing neurons in vitro , 1988, Brain Research.

[82]  Jochen Roeper,et al.  Differential Expression of the Small-Conductance, Calcium-Activated Potassium Channel SK3 Is Critical for Pacemaker Control in Dopaminergic Midbrain Neurons , 2001, The Journal of Neuroscience.