3‐Nitropropionic acid induces autophagy by forming mitochondrial permeability transition pores rather than activatiing the mitochondrial fission pathway

BACKGROUND AND PURPOSE Huntington's disease is a neurodegenerative process associated with mitochondrial alterations. Inhibitors of the electron–transport channel complex II, such as 3‐nitropropionic acid (3NP), are used to study the molecular and cellular pathways involved in this disease. We studied the effect of 3NP on mitochondrial morphology and its involvement in macrophagy.

[1]  J. Jordán,et al.  Mitochondria and calcium flux as targets of neuroprotection caused by minocycline in cerebellar granule cells. , 2010, Biochemical pharmacology.

[2]  H. Fujita,et al.  Mechanism of 3‐nitropropionic acid‐induced membrane permeability transition of isolated mitochondria and its suppression by L‐carnitine , 2008, Cell biochemistry and function.

[3]  A. Tolkovsky,et al.  Autophagy Is Activated by Apoptotic Signalling in Sympathetic Neurons: An Alternative Mechanism of Death Execution , 1999, Molecular and Cellular Neuroscience.

[4]  J. McCaffery,et al.  Dnm1 forms spirals that are structurally tailored to fit mitochondria , 2005, The Journal of cell biology.

[5]  J. Jordán,et al.  Methadone induces necrotic-like cell death in SH-SY5Y cells by an impairment of mitochondrial ATP synthesis. , 2010, Biochimica et biophysica acta.

[6]  Ana Maria Cuervo,et al.  Autophagy: Many paths to the same end , 2004, Molecular and Cellular Biochemistry.

[7]  James R. Burke,et al.  Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines , 2002, Nature Neuroscience.

[8]  J. Jordán,et al.  Reactive oxygen species induce swelling and cytochrome c release but not transmembrane depolarization in isolated rat brain mitochondria , 2003, British journal of pharmacology.

[9]  Françoise Condé,et al.  Replicating Huntington's disease phenotype in experimental animals , 1999, Progress in Neurobiology.

[10]  D. Andrews,et al.  Closing in on the link between apoptosis and autophagy , 2010, F1000 biology reports.

[11]  G. Miotto,et al.  Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. , 1999, Biophysical journal.

[12]  M Crompton,et al.  The mitochondrial permeability transition pore and its role in cell death. , 1999, The Biochemical journal.

[13]  M. Beal,et al.  Toxin-induced mitochondrial dysfunction. , 2002, International review of neurobiology.

[14]  D. Prou,et al.  Toxin-induced models of Parkinson’s disease , 2005, NeuroRX.

[15]  T. Kirchhausen,et al.  Constriction and Dnm1p recruitment are distinct processes in mitochondrial fission. , 2003, Molecular biology of the cell.

[16]  E. Bossy‐Wetzel,et al.  Complex II inhibition by 3-NP causes mitochondrial fragmentation and neuronal cell death via an NMDA- and ROS-dependent pathway , 2009, Cell Death and Differentiation.

[17]  E. Rugarli,et al.  Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. , 2004, The Journal of clinical investigation.

[18]  J. Shaw,et al.  Dnm1p Gtpase-Mediated Mitochondrial Fission Is a Multi-Step Process Requiring the Novel Integral Membrane Component Fis1p , 2000, The Journal of cell biology.

[19]  S. Frank,et al.  Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis , 2002, The Journal of cell biology.

[20]  R. Youle,et al.  Dynamics of mitochondrial morphology in healthy cells and during apoptosis , 2003, Cell Death and Differentiation.

[21]  R. Youle,et al.  A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis. , 2008, Molecular cell.

[22]  R. Youle,et al.  Endophilin B1 is required for the maintenance of mitochondrial morphology , 2004, The Journal of cell biology.

[23]  G. Kroemer,et al.  Autophagic cell death: the story of a misnomer , 2008, Nature Reviews Molecular Cell Biology.

[24]  J. Vasiliev,et al.  Thread-grain transition of mitochondrial reticulum as a step of mitoptosis and apoptosis , 2004, Molecular and Cellular Biochemistry.

[25]  A. M. van der Bliek,et al.  C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. , 1999, Molecular cell.

[26]  M. Schrader,et al.  6-Hydroxydopamine (6-OHDA) induces Drp1-dependent mitochondrial fragmentation in SH-SY5Y cells. , 2008, Free radical biology & medicine.

[27]  J. Puyal,et al.  Neuronal Autophagy as a Mediator of Life and Death , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[28]  Nuria Llecha,et al.  6‐Hydroxydopamine activates the mitochondrial apoptosis pathway through p38 MAPK‐mediated, p53‐independent activation of Bax and PUMA , 2008, Journal of neurochemistry.

[29]  S. Smaili,et al.  Bax translocation to mitochondria subsequent to a rapid loss of mitochondrial membrane potential , 2001, Cell Death and Differentiation.

[30]  S. Frank,et al.  The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. , 2001, Developmental cell.

[31]  T. Kuwana,et al.  Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. , 2008, Developmental cell.

[32]  A. Labrousse,et al.  elegans Dynamin-Related Protein DRP-1 Controls Severing of the Mitochondrial Outer , 1999 .

[33]  S. Schiffmann,et al.  Death of cortical and striatal neurons induced by mitochondrial defect involves differential molecular mechanisms , 2004, Neurobiology of Disease.

[34]  D. Chan,et al.  Functions and dysfunctions of mitochondrial dynamics , 2007, Nature Reviews Molecular Cell Biology.

[35]  R. Youle,et al.  How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? , 2006, Current opinion in cell biology.

[36]  Robert W. Taylor,et al.  Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. , 2002, Brain : a journal of neurology.

[37]  J. Thatcher,et al.  The Dynamin-related GTPase, Dnm1p, Controls Mitochondrial Morphology in Yeast , 1998, The Journal of cell biology.

[38]  R. Youle,et al.  Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. , 2004, Molecular biology of the cell.

[39]  J. Kordower,et al.  Cyclosporin A protects striatal neurons in vitro and in vivo from 3‐nitropropionic acid toxicity , 2000, The Journal of comparative neurology.

[40]  Joaquín Jordán,et al.  Lactacystin requires reactive oxygen species and Bax redistribution to induce mitochondria‐mediated cell death , 2009, British journal of pharmacology.

[41]  M. Gomez-Lazaro,et al.  Minocycline fails to protect cerebellar granular cell cultures against malonate-induced cell death , 2005, Neurobiology of Disease.

[42]  Kara L. Cerveny,et al.  Division of mitochondria requires a novel DNM1-interacting protein, Net2p. , 2001, Molecular biology of the cell.

[43]  K. Fukunaga,et al.  p53 mediates mitochondria dysfunction-triggered autophagy activation and cell death in rat striatum , 2009, Autophagy.

[44]  T. Kuwana,et al.  Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins , 2008, Proceedings of the National Academy of Sciences.

[45]  B. Hyman,et al.  Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  A. Godzik,et al.  Mitochondrial fission in apoptosis, neurodegeneration and aging. , 2003, Current opinion in cell biology.

[47]  Sudeshna Dutta,et al.  Autophagic programmed cell death by selective catalase degradation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[48]  J. Martinou,et al.  hFis1, a Novel Component of the Mammalian Mitochondrial Fission Machinery* , 2003, Journal of Biological Chemistry.

[49]  J. Jordán,et al.  Bcl‐xL blocks mitochondrial multiple conductance channel activation and inhibits 6‐OHDA‐induced death in SH‐SY5Y cells , 2004, Journal of neurochemistry.