Serine-47 phosphorylation of cytochrome c in the mammalian brain regulates cytochrome c oxidase and caspase-3 activity

Kalpage, Hasini A.; Vaishnav, Asmita; Liu, Jenney; Varughese, Ashwathy; Wan, Junmei; Turner, Alice A.; Ji, Qinqin; Zurek, Matthew P.; Kapralov, Alexandr A.; Kagan, Valerian E.; Brunzelle, Joseph S.; Recanati, Maurice-Andre; Grossman, Lawrence I.; Sanderson, Thomas H.; Lee, Icksoo; Salomon, Arthur R.; Edwards, Brian F.P.; Hüttemann, Maik

doi:10.1096/fj.201901120R

Title: Serine-47 phosphorylation of cytochrome c in the mammalian brain regulates cytochrome c oxidase and caspase-3 activity

Journal Article · Wed Jan 22 00:00:00 EST 2020 · FASEB J.

DOI:https://doi.org/10.1096/fj.201901120R· OSTI ID:1593444

Kalpage, Hasini A.; Vaishnav, Asmita; Liu, Jenney; Varughese, Ashwathy; Wan, Junmei; Turner, Alice A.; Ji, Qinqin; Zurek, Matthew P.; Kapralov, Alexandr A.; Kagan, Valerian E.; Brunzelle, Joseph S.; Recanati, Maurice-Andre; Grossman, Lawrence I.; Sanderson, Thomas H.; Lee, Icksoo; Salomon, Arthur R.; Edwards, Brian F.P.; Hüttemann, Maik ^[1]

Wayne State U

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1593444

Journal Information:: FASEB J., Vol. 33, Issue (12) ; 12, 2019

Country of Publication:: United States

Language:: ENGLISH

References (52)

Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state Piccoli, Claudia; Scrima, Rosella; Boffoli, Domenico Biochemical Journal, Vol. 396, Issue 3 https://doi.org/10.1042/BJ20060077	journal	May 2006
Control of Respiration by Cytochrome c Oxidase in Intact Cells : ROLE OF THE MEMBRANE POTENTIAL Dalmonte, Maria Elena; Forte, Elena; Genova, Maria Luisa Journal of Biological Chemistry, Vol. 284, Issue 47 https://doi.org/10.1074/jbc.M109.050146	journal	September 2009
Mechanistic stoichiometry of mitochondrial oxidative phosphorylation Hinkle, Peter C.; Kumar, M. Arun; Resetar, Andrea Biochemistry, Vol. 30, Issue 14 https://doi.org/10.1021/bi00228a031	journal	April 1991
The multiple functions of cytochrome c and their regulation in life and death decisions of the mammalian cell: From respiration to apoptosis Hüttemann, Maik; Pecina, Petr; Rainbolt, Matthew Mitochondrion, Vol. 11, Issue 3 https://doi.org/10.1016/j.mito.2011.01.010	journal	May 2011
Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors Kagan, Valerian E.; Tyurin, Vladimir A.; Jiang, Jianfei Nature Chemical Biology, Vol. 1, Issue 4 https://doi.org/10.1038/nchembio727	journal	August 2005
Cytochrome c/cardiolipin relations in mitochondria: a kiss of death Kagan, Valerian E.; Bayır, Hülya A.; Belikova, Natalia A. Free Radical Biology and Medicine, Vol. 46, Issue 11 https://doi.org/10.1016/j.freeradbiomed.2009.03.004	journal	June 2009
The biosynthesis and functional role of cardiolipin Schlame, Michael; Rua, Diego; Greenberg, Miriam L. Progress in Lipid Research, Vol. 39, Issue 3 https://doi.org/10.1016/S0163-7827(00)00005-9	journal	May 2000
Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine Kagan, Valerian E.; Borisenko, Grigory G.; Tyurina, Yulia Y. Free Radical Biology and Medicine, Vol. 37, Issue 12 https://doi.org/10.1016/j.freeradbiomed.2004.08.016	journal	December 2004
The “pro-apoptotic genies” get out of mitochondria: Oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes Kagan, V. E.; Tyurina, Y. Y.; Bayir, H. Chemico-Biological Interactions, Vol. 163, Issue 1-2 https://doi.org/10.1016/j.cbi.2006.04.019	journal	October 2006
Electron Transfer between Cytochrome c and p66Shc Generates Reactive Oxygen Species that Trigger Mitochondrial Apoptosis Giorgio, Marco; Migliaccio, Enrica; Orsini, Francesca Cell, Vol. 122, Issue 2 https://doi.org/10.1016/j.cell.2005.05.011	journal	July 2005
Cytochrome c, an ideal antioxidant Pereverzev, M. O.; Vygodina, T. V.; Konstantinov, A. A. Biochemical Society Transactions, Vol. 31, Issue 6 https://doi.org/10.1042/bst0311312	journal	December 2003
Tissue-specific regulation of cytochrome c by post-translational modifications: respiration, the mitochondrial membrane potential, ROS, and apoptosis Kalpage, Hasini A.; Bazylianska, Viktoriia; Recanati, Maurice A. The FASEB Journal, Vol. 33, Issue 2 https://doi.org/10.1096/fj.201801417R	journal	February 2019
New Prospects for an Old Enzyme: Mammalian Cytochrome c Is Tyrosine-Phosphorylated in Vivo † Lee, Icksoo; Salomon, Arthur R.; Yu, Kebing Biochemistry, Vol. 45, Issue 30 https://doi.org/10.1021/bi060585v	journal	August 2006
Mammalian liver cytochrome c is tyrosine-48 phosphorylated in vivo, inhibiting mitochondrial respiration Yu, Hong; Lee, Icksoo; Salomon, Arthur R. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 7-8 https://doi.org/10.1016/j.bbabio.2008.04.023	journal	July 2008
Phosphorylation of Cytochrome c Threonine 28 Regulates Electron Transport Chain Activity in Kidney : IMPLICATIONS FOR AMP KINASE Mahapatra, Gargi; Varughese, Ashwathy; Ji, Qinqin Journal of Biological Chemistry, Vol. 292, Issue 1 https://doi.org/10.1074/jbc.M116.744664	journal	October 2016
Cytochrome c Is Tyrosine 97 Phosphorylated by Neuroprotective Insulin Treatment Sanderson, Thomas H.; Mahapatra, Gargi; Pecina, Petr PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078627	journal	November 2013
Phosphoproteome Analysis of Functional Mitochondria Isolated from Resting Human Muscle Reveals Extensive Phosphorylation of Inner Membrane Protein Complexes and Enzymes Zhao, Xiaolu; León, Ileana R.; Bak, Steffen Molecular & Cellular Proteomics, Vol. 10, Issue 1 https://doi.org/10.1074/mcp.M110.000299	journal	September 2010
Global Phosphoproteomic Analysis of Human Skeletal Muscle Reveals a Network of Exercise-Regulated Kinases and AMPK Substrates Hoffman, Nolan J.; Parker, Benjamin L.; Chaudhuri, Rima Cell Metabolism, Vol. 22, Issue 5 https://doi.org/10.1016/j.cmet.2015.09.001	journal	November 2015
Silencing, Positive Selection and Parallel Evolution: Busy History of Primate Cytochromes c Pierron, Denis; Opazo, Juan C.; Heiske, Margit PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026269	journal	October 2011
Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb-the counterpart to testes-specific cytochrome c ? : COX VIb TESTES Hüttemann, Maik; Jaradat, Saied; Grossman, Lawrence I. Molecular Reproduction and Development, Vol. 66, Issue 1 https://doi.org/10.1002/mrd.10327	journal	July 2003
Tissue- and Condition-Specific Isoforms of Mammalian Cytochrome c Oxidase Subunits: From Function to Human Disease Sinkler, Christopher A.; Kalpage, Hasini; Shay, Joseph Oxidative Medicine and Cellular Longevity, Vol. 2017 https://doi.org/10.1155/2017/1534056	journal	January 2017
Multiple phosphorylations of cytochrome c oxidase and their functions Helling, Stefan; Hüttemann, Maik; Ramzan, Rabia PROTEOMICS, Vol. 12, Issue 7 https://doi.org/10.1002/pmic.201100618	journal	April 2012
Molecular Mechanisms of Ischemia–Reperfusion Injury in Brain: Pivotal Role of the Mitochondrial Membrane Potential in Reactive Oxygen Species Generation Sanderson, Thomas H.; Reynolds, Christian A.; Kumar, Rita Molecular Neurobiology, Vol. 47, Issue 1 https://doi.org/10.1007/s12035-012-8344-z	journal	September 2012
High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria Korshunov, Sergey S.; Skulachev, Vladimir P.; Starkov, Anatoly A. FEBS Letters, Vol. 416, Issue 1 https://doi.org/10.1016/S0014-5793(97)01159-9	journal	October 1997
Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease Hüttemann, Maik; Lee, Icksoo; Pecinova, Alena Journal of Bioenergetics and Biomembranes, Vol. 40, Issue 5 https://doi.org/10.1007/s10863-008-9169-3	journal	October 2008
Membrane Potential Greatly Enhances Superoxide Generation by the Cytochrome bc 1 Complex Reconstituted into Phospholipid Vesicles Rottenberg, Hagai; Covian, Raul; Trumpower, Bernard L. Journal of Biological Chemistry, Vol. 284, Issue 29 https://doi.org/10.1074/jbc.M109.017376	journal	May 2009
Phosphomimetic Substitution of Cytochrome c Tyrosine 48 Decreases Respiration and Binding to Cardiolipin and Abolishes Ability to Trigger Downstream Caspase Activation Pecina, Petr; Borisenko, Grigory G.; Belikova, Natalia A. Biochemistry, Vol. 49, Issue 31 https://doi.org/10.1021/bi100486s	journal	August 2010
Remarkably high activities of testicular cytochrome c in destroying reactive oxygen species and in triggering apoptosis Liu, Z.; Lin, H.; Ye, S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 24 https://doi.org/10.1073/pnas.0603327103	journal	June 2006
Separation of mammalian cytochrome c oxidase into 13 polypeptides by a sodium dodecyl sulfate-gel electrophoretic procedure Kadenbach, Bernhard; Jarausch, Jochen; Hartmann, Renate Analytical Biochemistry, Vol. 129, Issue 2 https://doi.org/10.1016/0003-2697(83)90586-9	journal	March 1983
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Data processing and analysis with the autoPROC toolbox Vonrhein, Clemens; Flensburg, Claus; Keller, Peter Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007773	journal	March 2011
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/S2052252514009324	journal	May 2014
New ways to boost molecular dynamics simulations Krieger, Elmar; Vriend, Gert Journal of Computational Chemistry, Vol. 36, Issue 13 https://doi.org/10.1002/jcc.23899	journal	March 2015
Comparison of multiple Amber force fields and development of improved protein backbone parameters Hornak, Viktor; Abel, Robert; Okur, Asim Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 3 https://doi.org/10.1002/prot.21123	journal	November 2006
Isolation and properties of cytochrome c oxidase from rat liver and quantification of immunological differences between isozymes from various rat tissues with subunit-specific antisera Kuhn-Nentwig, Lucia; Kadenbach, Bernhard European Journal of Biochemistry, Vol. 149, Issue 1 https://doi.org/10.1111/j.1432-1033.1985.tb08905.x	journal	May 1985
Definition of the Interaction Domain for Cytochrome c on Cytochrome c Oxidase : III. PREDICTION OF THE DOCKED COMPLEX BY A COMPLETE, SYSTEMATIC SEARCH Roberts, Victoria A.; Pique, Michael E. Journal of Biological Chemistry, Vol. 274, Issue 53 https://doi.org/10.1074/jbc.274.53.38051	journal	December 1999
A near atomic structure of the active human apoptosome Cheng, Tat Cheung; Hong, Chuan; Akey, Ildikó V. eLife, Vol. 5 https://doi.org/10.7554/eLife.17755	journal	October 2016
Alternative Conformations of Cytochrome c : Structure, Function, and Detection Hannibal, Luciana; Tomasina, Florencia; Capdevila, Daiana A. Biochemistry, Vol. 55, Issue 3 https://doi.org/10.1021/acs.biochem.5b01385	journal	January 2016
Appraising the brain's energy budget Raichle, M. E.; Gusnard, D. A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 16 https://doi.org/10.1073/pnas.172399499	journal	July 2002
The pig as an animal model for human pathologies: A proteomics perspective Bassols, Anna; Costa, Cristina; Eckersall, P. David PROTEOMICS - Clinical Applications, Vol. 8, Issue 9-10 https://doi.org/10.1002/prca.201300099	journal	October 2014
In vivo Phosphoproteome of Human Skeletal Muscle Revealed by Phosphopeptide Enrichment and HPLC−ESI−MS/MS Højlund, Kurt; Bowen, Benjamin P.; Hwang, Hyonson Journal of Proteome Research, Vol. 8, Issue 11 https://doi.org/10.1021/pr9007267	journal	November 2009
How Cytochrome c Folds, and Why: Submolecular Foldon Units and their Stepwise Sequential Stabilization Maity, Haripada; Maity, Mita; Walter Englander, S. Journal of Molecular Biology, Vol. 343, Issue 1 https://doi.org/10.1016/j.jmb.2004.08.005	journal	October 2004
Increased dynamics in the 40–57 Ω-loop of the G41S variant of human cytochrome c promote its pro-apoptotic conformation Karsisiotis, Andreas Ioannis; Deacon, Oliver M.; Wilson, Michael T. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30447	journal	July 2016
Naturally Occurring Disease-Related Mutations in the 40–57 Ω-Loop of Human Cytochrome c Control Triggering of the Alkaline Isomerization Deacon, Oliver M.; Svistunenko, Dimitri A.; Moore, Geoffrey R. Biochemistry, Vol. 57, Issue 29 https://doi.org/10.1021/acs.biochem.8b00520	journal	June 2018
The low ionic strength crystal structure of horse cytochrome c at 2.1 å resolution and comparison with its high ionic strength counterpart Sanishvili, R.; Volz, Kw; Westbrook, Em Structure, Vol. 3, Issue 7 https://doi.org/10.1016/S0969-2126(01)00205-2	journal	July 1995
Structural and functional characterization of phosphomimetic mutants of cytochrome c at threonine 28 and serine 47 Guerra-Castellano, Alejandra; Díaz-Moreno, Irene; Velázquez-Campoy, Adrián Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 4 https://doi.org/10.1016/j.bbabio.2016.01.011	journal	April 2016
The role of key residues in structure, function, and stability of cytochrome-c Zaidi, Sobia; Hassan, Md. Imtaiyaz; Islam, Asimul Cellular and Molecular Life Sciences, Vol. 71, Issue 2 https://doi.org/10.1007/s00018-013-1341-1	journal	April 2013
Isolation and sequence of the human cytochrome c oxidase subunit VIIaL gene Hüttemann, Maik; Mühlenbein, Nicole; Schmidt, Timothy R. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1492, Issue 1 https://doi.org/10.1016/S0167-4781(00)00087-7	journal	June 2000
Tissue-Specific Expression and Mapping of theCox7ahGene in Mouse Jaradat, Saied A.; Ko, Minoru S. H.; Grossman, Lawrence I. Genomics, Vol. 49, Issue 3 https://doi.org/10.1006/geno.1998.5279	journal	May 1998
Localization of PTP-1B, SHP-2, and Src Exclusively in Rat Brain Mitochondria and Functional Consequences Arachiche, Amal; Augereau, Olivier; Decossas, Marion Journal of Biological Chemistry, Vol. 283, Issue 36 https://doi.org/10.1074/jbc.M709217200	journal	June 2008
The Whole Structure of the 13-Subunit Oxidized Cytochrome c Oxidase at 2.8 A Tsukihara, T.; Aoyama, H.; Yamashita, E. Science, Vol. 272, Issue 5265 https://doi.org/10.1126/science.272.5265.1136	journal	May 1996

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