Endoplasmic reticulum-mitochondria tethering in neurodegenerative diseases

Endoplasmic reticulum (ER) and mitochondria are tubular organelles with a characteristic “network structure” that facilitates the formation of inter-organellar connections. As a result, mitochondria-associated ER membranes (MAMs), a subdomain of the ER that is tightly linked to and communicates with mitochondria, serve multiple physiological functions including lipid synthesis and exchange, calcium signaling, bioenergetics, and apoptosis. Importantly, emerging evidence suggests that the abnormality and dysfunction of MAMs have been involved in various neurodegenerative disorders including Alzheimer’s disease, amyotrophic lateral sclerosis, and Parkinson’s disease. This review will focus on the architecture and function of MAMs and its involvement in the neurodegenerative diseases.

[1]  G. Knott,et al.  Parkin functionally interacts with PGC‐1&agr; to preserve mitochondria and protect dopaminergic neurons , 2017, Human molecular genetics.

[2]  Teruo Hayashi,et al.  Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. , 2007, Cell.

[3]  A. M. van der Bliek,et al.  Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. , 2001, Molecular biology of the cell.

[4]  J. Vance.  MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. , 2014, Biochimica et biophysica acta.

[5]  Teruo Hayashi,et al.  Sigma-1 Receptor Chaperones at the ER- Mitochondrion Interface Regulate Ca2+ Signaling and Cell Survival , 2007, Cell.

[6]  A. Negro,et al.  α-Synuclein Controls Mitochondrial Calcium Homeostasis by Enhancing Endoplasmic Reticulum-Mitochondria Interactions* , 2012, The Journal of Biological Chemistry.

[7]  T. Langer,et al.  Mitofusin 2 Builds a Bridge between ER and Mitochondria , 2008, Cell.

[8]  A. Luini,et al.  Presenilin 2 Modulates Endoplasmic Reticulum-Mitochondria Coupling by Tuning the Antagonistic Effect of Mitofusin 2. , 2016, Cell reports.

[9]  T. Meyer,et al.  Elementary calcium-release units induced by inositol trisphosphate. , 1997, Science.

[10]  I. Nabi,et al.  Distinct mechanisms controlling rough and smooth endoplasmic reticulum contacts with mitochondria , 2015, Journal of Cell Science.

[11]  P. Várnai,et al.  Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels , 2006, The Journal of cell biology.

[12]  A. Brice,et al.  The endoplasmic reticulum-mitochondria interface is perturbed in PARK2 knockout mice and patients with PARK2 mutations. , 2016, Human molecular genetics.

[13]  Yasushi Hiraoka,et al.  Autophagosomes form at ER–mitochondria contact sites , 2013, Nature.

[14]  E. Schon,et al.  α-Synuclein Is Localized to Mitochondria-Associated ER Membranes , 2014, The Journal of Neuroscience.

[15]  Elisa Greotti,et al.  Mitofusin 2 ablation increases endoplasmic reticulum–mitochondria coupling , 2015, Proceedings of the National Academy of Sciences.

[16]  M. Ankarcrona,et al.  Amyloid-β peptides are generated in mitochondria-associated endoplasmic reticulum membranes. , 2014, Journal of Alzheimer's disease : JAD.

[17]  A. Messina,et al.  VDAC1 selectively transfers apoptotic Ca2+ signals to mitochondria , 2011, Cell Death and Differentiation.

[18]  J. Vance,et al.  Phosphatidylserine Synthase-1 and -2 Are Localized to Mitochondria-associated Membranes* , 2000, The Journal of Biological Chemistry.

[19]  D. Chan.  Mitochondria: Dynamic Organelles in Disease, Aging, and Development , 2006, Cell.

[20]  L. Wan,et al.  PACS‐2 controls endoplasmic reticulum–mitochondria communication and Bid‐mediated apoptosis , 2005, The EMBO journal.

[21]  C. B. Pickett,et al.  Association between mitochondria and rough endoplasmic reticulum in rat liver , 1982, The Anatomical record.

[22]  A. Negro,et al.  The Parkinson disease-related protein DJ-1 counteracts mitochondrial impairment induced by the tumour suppressor protein p53 by enhancing endoplasmic reticulum-mitochondria tethering. , 2013, Human molecular genetics.

[23]  P. Agostinis,et al.  New functions of mitochondria associated membranes in cellular signaling. , 2014, Biochimica et biophysica acta.

[24]  Mark P Mattson,et al.  Alzheimer's Presenilin 1 Mutations Impair Kinesin-Based Axonal Transport , 2003, The Journal of Neuroscience.

[25]  David S. Park,et al.  Parkin is transcriptionally regulated by ATF4: evidence for an interconnection between mitochondrial stress and ER stress , 2011, Cell Death and Differentiation.

[26]  M. McNiven,et al.  Mammalian dynamin-like protein DLP1 tubulates membranes. , 2001, Molecular biology of the cell.

[27]  L. Scorrano,et al.  Mitofusin 2 tethers endoplasmic reticulum to mitochondria , 2008, Nature.

[28]  Victor S. Van Laar,et al.  Glutamate excitotoxicity in neurons triggers mitochondrial and endoplasmic reticulum accumulation of Parkin, and, in the presence of N-acetyl cysteine, mitophagy , 2015, Neurobiology of Disease.

[29]  F. Striggow,et al.  The regulation of OXPHOS by extramitochondrial calcium. , 2010, Biochimica et biophysica acta.

[30]  C. Tacchetti,et al.  Mitochondria and Melanosomes Establish Physical Contacts Modulated by Mfn2 and Involved in Organelle Biogenesis , 2014, Current Biology.

[31]  Xiaodi A Deng,et al.  Association of Active Caspase 8 with the Mitochondrial Membrane during Apoptosis: Potential Roles in Cleaving BAP31 and Caspase 3 and Mediating Mitochondrion-Endoplasmic Reticulum Cross Talk in Etoposide-Induced Cell Death , 2004, Molecular and Cellular Biology.

[32]  E. Valente,et al.  PINK1 and BECN1 relocalize at mitochondria-associated membranes during mitophagy and promote ER-mitochondria tethering and autophagosome formation , 2017, Autophagy.

[33]  L. Petrucelli,et al.  ER–mitochondria associations are regulated by the VAPB–PTPIP51 interaction and are disrupted by ALS/FTD-associated TDP-43 , 2014, Nature Communications.

[34]  I. Nishimoto,et al.  Characterization of Amyotrophic Lateral Sclerosis-linked P56S Mutation of Vesicle-associated Membrane Protein-associated Protein B (VAPB/ALS8)* , 2006, Journal of Biological Chemistry.

[35]  D. Voelker,et al.  Synthesis and Intracellular Transport of Aminoglycerophospholipids in Permeabilized Cells of the Yeast, Saccharomyces cerevisiae(*) , 1995, The Journal of Biological Chemistry.

[36]  H. Kiyama,et al.  Mitochondria‐associated membrane collapse is a common pathomechanism in SIGMAR1‐ and SOD1‐linked ALS , 2016, EMBO molecular medicine.

[37]  G. Hajnóczky,et al.  Old players in a new role: mitochondria-associated membranes, VDAC, and ryanodine receptors as contributors to calcium signal propagation from endoplasmic reticulum to the mitochondria. , 2002, Cell calcium.

[38]  M. Ankarcrona,et al.  Mitofusin‐2 knockdown increases ER–mitochondria contact and decreases amyloid β‐peptide production , 2016, Journal of cellular and molecular medicine.

[39]  V. Mootha,et al.  Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter , 2011, Nature.

[40]  H. Bose,et al.  Mitochondria-associated Endoplasmic Reticulum Membrane (MAM) Regulates Steroidogenic Activity via Steroidogenic Acute Regulatory Protein (StAR)-Voltage-dependent Anion Channel 2 (VDAC2) Interaction* , 2014, The Journal of Biological Chemistry.

[41]  Luca Scorrano,et al.  Critical reappraisal confirms that Mitofusin 2 is an endoplasmic reticulum–mitochondria tether , 2016, Proceedings of the National Academy of Sciences.

[42]  T. Pozzan,et al.  Calcium Elevation in Mitochondria Is the Main Ca2+ Requirement for Mitochondrial Permeability Transition Pore (mPTP) Opening , 2009, The Journal of Biological Chemistry.

[43]  T. M. Lewin,et al.  Acyl-CoA Synthetase Isoforms 1, 4, and 5 Are Present in Different Subcellular Membranes in Rat Liver and Can Be Inhibited Independently* , 2001, The Journal of Biological Chemistry.

[44]  D. Voelker.  Bridging gaps in phospholipid transport. , 2005, Trends in biochemical sciences.

[45]  H. McBride,et al.  MAPL SUMOylation of Drp1 Stabilizes an ER/Mitochondrial Platform Required for Cell Death. , 2015, Molecular cell.

[46]  C. Thompson,et al.  The endoplasmic reticulum gateway to apoptosis by Bcl-XL modulation of the InsP3R , 2005, Nature Cell Biology.

[47]  F. Al-Mohanna,et al.  A mutation in sigma‐1 receptor causes juvenile amyotrophic lateral sclerosis , 2011, Annals of neurology.

[48]  M. Birnbaum,et al.  Essential Regulation of Cell Bioenergetics by Constitutive InsP3 Receptor Ca2+ Transfer to Mitochondria , 2010, Cell.

[49]  G. Shore,et al.  Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol , 2003, The Journal of cell biology.

[50]  Lawrence M. Lifshitz,et al.  Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. , 1998, Science.

[51]  Hong Qi,et al.  Optimal microdomain crosstalk between endoplasmic reticulum and mitochondria for Ca2+ oscillations , 2015, Scientific Reports.

[52]  B. Winblad,et al.  Modulation of the endoplasmic reticulum–mitochondria interface in Alzheimer’s disease and related models , 2013, Proceedings of the National Academy of Sciences.

[53]  K. Mikoshiba,et al.  IRBIT controls apoptosis by interacting with the Bcl-2 homolog, Bcl2l10, and by promoting ER-mitochondria contact , 2016, eLife.

[54]  S. Grimm.  The ER-mitochondria interface: the social network of cell death. , 2012, Biochimica et biophysica acta.

[55]  H. Higgs,et al.  An Actin-Dependent Step in Mitochondrial Fission Mediated by the ER-Associated Formin INF2 , 2013, Science.

[56]  E. Schon,et al.  Presenilins are enriched in endoplasmic reticulum membranes associated with mitochondria. , 2009, The American journal of pathology.

[57]  M. Bortolozzi,et al.  Presenilin 2 modulates endoplasmic reticulum (ER)–mitochondria interactions and Ca2+ cross-talk , 2011, Proceedings of the National Academy of Sciences.

[58]  M. Hall,et al.  mTOR complex 2-Akt signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology , 2013, Proceedings of the National Academy of Sciences.

[59]  J. Vance.  Phospholipid synthesis in a membrane fraction associated with mitochondria. , 1990, The Journal of biological chemistry.

[60]  P. Pinton,et al.  Mitochondria-associated membranes (MAMs) as hotspot Ca(2+) signaling units. , 2012, Advances in experimental medicine and biology.

[61]  A. Terrin,et al.  The Mitochondrial Calcium Uniporter (MCU): Molecular Identity and Physiological Roles* , 2013, The Journal of Biological Chemistry.

[62]  Matthew West,et al.  ER Tubules Mark Sites of Mitochondrial Division , 2011, Science.

[63]  E. Schon,et al.  Upregulated function of mitochondria-associated ER membranes in Alzheimer disease , 2012, The EMBO journal.

[64]  E. Schon,et al.  ApoE4 upregulates the activity of mitochondria‐associated ER membranes , 2015, EMBO reports.

[65]  C. Mannella,et al.  Structural and functional features and significance of the physical linkage between ER and mitochondria , 2006, The Journal of cell biology.

[66]  H. McBride,et al.  MITOL regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. , 2013, Molecular cell.

[67]  E. Schon,et al.  Is Alzheimer's disease a disorder of mitochondria-associated membranes? , 2010, Journal of Alzheimer's disease : JAD.

[68]  S. Grimm,et al.  Fis1 and Bap31 bridge the mitochondria–ER interface to establish a platform for apoptosis induction , 2011, The EMBO journal.

[69]  G. Voeltz,et al.  Endoplasmic reticulum–mitochondria contacts: function of the junction , 2012, Nature Reviews Molecular Cell Biology.

[70]  P. Pinton,et al.  Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis , 2008, Oncogene.

[71]  Chenglong Xia,et al.  Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes , 2012, Proceedings of the National Academy of Sciences.

[72]  S. Snyder,et al.  Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis , 2003, Nature Cell Biology.

[73]  A. Negro,et al.  Enhanced parkin levels favor ER-mitochondria crosstalk and guarantee Ca(2+) transfer to sustain cell bioenergetics. , 2013, Biochimica et biophysica acta.

[74]  S. Buch,et al.  The sigma-1 receptor chaperone as an inter-organelle signaling modulator. , 2010, Trends in pharmacological sciences.

[75]  C. B. Pickett,et al.  The physical association between rat liver mitochondria and rough endoplasmic reticulum. I. Isolation, electron microscopic examination and sedimentation equilibrium centrifugation analyses of rough endoplasmic reticulum-mitochondrial complexes. , 1980, Experimental cell research.

[76]  B. Kornmann,et al.  The molecular hug between the ER and the mitochondria. , 2013, Current opinion in cell biology.

[77]  I. Nabi,et al.  Calcium Regulates the Association between Mitochondria and a Smooth Subdomain of the Endoplasmic Reticulum , 2000, The Journal of cell biology.

[78]  G. Shore,et al.  Fis1, Bap31 and the kiss of death between mitochondria and endoplasmic reticulum , 2011, The EMBO journal.

[79]  Carlotta Giorgi,et al.  Calcium signaling around Mitochondria Associated Membranes (MAMs) , 2011, Cell Communication and Signaling.

[80]  T. M. Lewin,et al.  Rat liver acyl-CoA synthetase 4 is a peripheral-membrane protein located in two distinct subcellular organelles, peroxisomes, and mitochondrial-associated membrane. , 2002, Archives of biochemistry and biophysics.

[81]  C. Shaw,et al.  VAPB interacts with the mitochondrial protein PTPIP51 to regulate calcium homeostasis , 2011, Human molecular genetics.