Features and regulation of non-enzymatic post-translational modifications.

Non-enzymatic post-translational modifications of proteins can occur when a nucleophilic or redox-sensitive amino acid side chain encounters a reactive metabolite. In many cases, the biological function of these modifications is limited by their irreversibility, and consequently these non-enzymatic modifications are often considered as indicators of stress and disease. Certain non-enzymatic post-translational modifications, however, can be reversed, which provides an additional layer of regulation and renders these modifications suitable for controlling a diverse set of cellular processes ranging from signaling to metabolism. Here we summarize recent examples of irreversible and reversible non-enzymatic modifications, with an emphasis on the latter category. We use two examples, lysine glutarylation and pyrophosphorylation, to highlight principles of the regulation of reversible non-enzymatic post-translational modifications in more detail. Overall, a picture emerges that goes well beyond nonspecific chemical reactions and cellular damage, and instead portrays multifaceted functions of non-enzymatic post-translational modifications.

[1]  D. Petersen,et al.  Prooxidant-initiated lipid peroxidation in isolated rat hepatocytes: detection of 4-hydroxynonenal- and malondialdehyde-protein adducts. , 1997, Chemical research in toxicology.

[2]  Paul J Thornalley,et al.  Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N alpha-acetylarginine, N alpha-acetylcysteine, and N alpha-acetyllysine, and bovine serum albumin. , 1994, The Journal of biological chemistry.

[3]  A. Napolitano,et al.  Glyoxal formation by Fenton-induced degradation of carbohydrates and related compounds. , 2006, Carbohydrate research.

[4]  M. Hirschey,et al.  Nonenzymatic protein acylation as a carbon stress regulated by sirtuin deacylases. , 2014, Molecular cell.

[5]  Anutosh Chakraborty,et al.  Inositol Pyrophosphates Inhibit Akt Signaling, Thereby Regulating Insulin Sensitivity and Weight Gain , 2010, Cell.

[6]  P. Ray,et al.  Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. , 2012, Cellular signalling.

[7]  T. Lyons,et al.  Accumulation of Maillard reaction products in skin collagen in diabetes and aging. , 1993, The Journal of clinical investigation.

[8]  Vidya Venkatraman,et al.  Cysteine oxidative posttranslational modifications: emerging regulation in the cardiovascular system. , 2013, Circulation research.

[9]  S. Snyder,et al.  H2S Signals Through Protein S-Sulfhydration , 2009, Science Signaling.

[10]  D. Fiedler,et al.  Establishing the Stability and Reversibility of Protein Pyrophosphorylation with Synthetic Peptides , 2015, Chembiochem : a European journal of chemical biology.

[11]  D. Fiedler,et al.  Elucidating diphosphoinositol polyphosphate function with nonhydrolyzable analogues. , 2014, Angewandte Chemie.

[12]  Yingming Zhao,et al.  Lysine glutarylation is a protein posttranslational modification regulated by SIRT5. , 2014, Cell metabolism.

[13]  W. Linehan,et al.  Discovering Targets of Non-enzymatic Acylation by Thioester Reactivity Profiling. , 2017, Cell chemical biology.

[14]  Kate S. Carroll,et al.  Cysteine-Mediated Redox Signaling: Chemistry, Biology, and Tools for Discovery , 2013, Chemical reviews.

[15]  A. Bhattacharjee,et al.  Dynamics of Protein Tyrosine Nitration and Denitration: A Review , 2016 .

[16]  H. Ciolino,et al.  Modification of proteins in endothelial cell death during oxidative stress. , 1997, Free radical biology & medicine.

[17]  H. Forman,et al.  Glutathione in Defense and Signaling , 2002 .

[18]  M. Tremblay,et al.  Regulation of Insulin-Like Growth Factor Type I (IGF-I) Receptor Kinase Activity by Protein Tyrosine Phosphatase 1B (PTP-1B) and Enhanced IGF-I-Mediated Suppression of Apoptosis and Motility in PTP-1B-Deficient Fibroblasts , 2002, Molecular and Cellular Biology.

[19]  Roberto Colombo,et al.  Protein carbonylation in human diseases. , 2003, Trends in molecular medicine.

[20]  J. Baynes,et al.  Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. , 1999, Diabetes.

[21]  J. Carlin,et al.  Identifying peroxidases and their oxidants in the early pathology of cystic fibrosis. , 2010, Free radical biology & medicine.

[22]  L. Aaltonen,et al.  Aberrant succination of proteins in fumarate hydratase‐deficient mice and HLRCC patients is a robust biomarker of mutation status , 2011, The Journal of pathology.

[23]  S. Snyder,et al.  Phosphorylation of Proteins by Inositol Pyrophosphates , 2004, Science.

[24]  V. Monnier,et al.  Mechanism of Protein Modification by Glyoxal and Glycolaldehyde, Reactive Intermediates of the Maillard Reaction (*) , 1995, The Journal of Biological Chemistry.

[25]  Philippe Gillery,et al.  Evaluation of nonenzymatic posttranslational modification-derived products as biomarkers of molecular aging of proteins. , 2010, Clinical chemistry.

[26]  L. Zhu,et al.  Insulin-stimulated Hydrogen Peroxide Reversibly Inhibits Protein-tyrosine Phosphatase 1B in Vivo and Enhances the Early Insulin Action Cascade* , 2001, The Journal of Biological Chemistry.

[27]  S. Hazen,et al.  Rapid and Selective Oxygen-regulated Protein Tyrosine Denitration and Nitration in Mitochondria* , 2004, Journal of Biological Chemistry.

[28]  Michael P. Myers,et al.  Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate , 2003, Nature.

[29]  S. Hirohashi,et al.  Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. , 2008, Cancer research.

[30]  David H Perlman,et al.  Unambiguous Identification of Serine and Threonine Pyrophosphorylation Using Neutral-Loss-Triggered Electron-Transfer/Higher-Energy Collision Dissociation. , 2017, Analytical chemistry.

[31]  D. Fiedler,et al.  Inositol hexakisphosphate kinase 1 (IP6K1) activity is required for cytoplasmic dynein-driven transport , 2016, The Biochemical journal.

[32]  G. R. Wagner,et al.  Widespread and Enzyme-independent Nϵ-Acetylation and Nϵ-Succinylation of Proteins in the Chemical Conditions of the Mitochondrial Matrix*♦ , 2013, The Journal of Biological Chemistry.

[33]  Zhihong Zhang,et al.  Identification of lysine succinylation as a new post-translational modification. , 2011, Nature chemical biology.

[34]  A. Saiardi,et al.  Inositol pyrophosphate mediated pyrophosphorylation of AP3B1 regulates HIV-1 Gag release , 2009, Proceedings of the National Academy of Sciences.

[35]  T. Lyons,et al.  S-(2-Succinyl)cysteine: a novel chemical modification of tissue proteins by a Krebs cycle intermediate. , 2006, Archives of biochemistry and biophysics.

[36]  J. Denu,et al.  Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. , 1998, Biochemistry.

[37]  A. Ninfa,et al.  Is acetyl phosphate a global signal in Escherichia coli? , 1993, Journal of bacteriology.

[38]  Roberto Colombo,et al.  Protein carbonylation, cellular dysfunction, and disease progression , 2006, Journal of cellular and molecular medicine.

[39]  T. Lyons,et al.  The Advanced Glycation End Product, N-(Carboxymethyl)lysine, Is a Product of both Lipid Peroxidation and Glycoxidation Reactions (*) , 1996, The Journal of Biological Chemistry.

[40]  F. G. van der Goot,et al.  Active and dynamic mitochondrial S-depalmitoylation revealed by targeted fluorescent probes , 2018, Nature Communications.

[41]  D. Butterfield,et al.  Protein oxidation in the brain in Alzheimer's disease , 2001, Neuroscience.

[42]  P. Bork,et al.  Evolution and functional cross‐talk of protein post‐translational modifications , 2013, Molecular systems biology.

[43]  Bryan C Dickinson,et al.  Chemistry and biology of reactive oxygen species in signaling or stress responses. , 2011, Nature chemical biology.

[44]  J. Denu,et al.  Site-Specific Reactivity of Nonenzymatic Lysine Acetylation , 2015, ACS chemical biology.

[45]  J. Baynes,et al.  Succination of Proteins by Fumarate , 2008, Annals of the New York Academy of Sciences.

[46]  Dustin E. Schones,et al.  High-Resolution Profiling of Histone Methylations in the Human Genome , 2007, Cell.

[47]  S. Rhee,et al.  Reversible Inactivation of Protein-tyrosine Phosphatase 1B in A431 Cells Stimulated with Epidermal Growth Factor* , 1998, The Journal of Biological Chemistry.

[48]  Sylvie Garneau-Tsodikova,et al.  Protein posttranslational modifications: the chemistry of proteome diversifications. , 2005, Angewandte Chemie.

[49]  E. Stadtman Protein oxidation and aging , 2006, Science.

[50]  T. Hunter,et al.  The Protein Kinase Complement of the Human Genome , 2002, Science.

[51]  T. Soga,et al.  Rare insights into cancer biology , 2014, Oncogene.

[52]  Hamid Mirzaei,et al.  Creation of allotypic active sites during oxidative stress. , 2006, Journal of proteome research.

[53]  D. Hajjar,et al.  Characterization of a cellular denitrase activity that reverses nitration of cyclooxygenase. , 2013, American journal of physiology. Heart and circulatory physiology.

[54]  Anne Dawnay,et al.  Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. , 2003, The Biochemical journal.

[55]  J. Peschek,et al.  Methionine oxidation activates a transcription factor in response to oxidative stress , 2013, Proceedings of the National Academy of Sciences.

[56]  V. Gladyshev,et al.  Regulation of protein function by reversible methionine oxidation and the role of selenoprotein MsrB1. , 2015, Antioxidants & redox signaling.

[57]  Lan Huang,et al.  Quantitative analysis of global ubiquitination in HeLa cells by mass spectrometry. , 2008, Journal of proteome research.

[58]  S. Snyder,et al.  Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  H. Forman,et al.  An overview of mechanisms of redox signaling. , 2014, Journal of molecular and cellular cardiology.

[60]  Johan Auwerx,et al.  Sirt5 Is a NAD-Dependent Protein Lysine Demalonylase and Desuccinylase , 2011, Science.

[61]  V. Gladyshev,et al.  Methionine sulfoxide reduction in mammals: characterization of methionine-R-sulfoxide reductases. , 2003, Molecular biology of the cell.

[62]  M. Keller,et al.  The widespread role of non-enzymatic reactions in cellular metabolism , 2015, Current opinion in biotechnology.

[63]  Nessar Ahmed,et al.  Advanced glycation endproducts--role in pathology of diabetic complications. , 2005, Diabetes research and clinical practice.

[64]  A. Saiardi,et al.  Protein polyphosphorylation of lysine residues by inorganic polyphosphate. , 2015, Molecular cell.

[65]  A. Wolfe,et al.  The Intracellular Concentration of Acetyl Phosphate in Escherichia coli Is Sufficient for Direct Phosphorylation of Two-Component Response Regulators , 2007, Journal of bacteriology.

[66]  M. Tominaga,et al.  Nitric oxide activates TRP channels by cysteine S-nitrosylation , 2006, Nature chemical biology.

[67]  B. Cravatt,et al.  Functional Lysine Modification by an Intrinsically Reactive Primary Glycolytic Metabolite , 2013, Science.

[68]  D. Stuehr,et al.  Dynamics of protein nitration in cells and mitochondria. , 2004, American journal of physiology. Heart and circulatory physiology.

[69]  J. Baynes,et al.  Succination of proteins in diabetes , 2011, Free radical research.

[70]  Laura G. Dubois,et al.  A Class of Reactive Acyl-CoA Species Reveals the Non-enzymatic Origins of Protein Acylation. , 2017, Cell metabolism.

[71]  S. Hazen,et al.  Protein Carbamylation and Cardiovascular Disease , 2015, Kidney international.

[72]  P. Carmeliet,et al.  Renal Cyst Formation in Fh1-Deficient Mice Is Independent of the Hif/Phd Pathway: Roles for Fumarate in KEAP1 Succination and Nrf2 Signaling , 2011, Cancer cell.

[73]  W. MacNee,et al.  4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. , 2002, American journal of respiratory and critical care medicine.

[74]  A. Berg,et al.  Protein carbamylation in kidney disease: pathogenesis and clinical implications. , 2014, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[75]  Santiago Lamas,et al.  Hydrogen peroxide signaling in vascular endothelial cells , 2014, Redox biology.

[76]  Huanchen Wang,et al.  Cellular Cations Control Conformational Switching of Inositol Pyrophosphate Analogues. , 2016, Chemistry.

[77]  Troels Z. Kristiansen,et al.  Protein pyrophosphorylation by inositol pyrophosphates is a posttranslational event , 2007, Proceedings of the National Academy of Sciences.

[78]  F. Regnier,et al.  Proteomic identification of carbonylated proteins and their oxidation sites. , 2010, Journal of proteome research.

[79]  Miles Congreve,et al.  Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B , 2003, Nature.

[80]  A. Barden,et al.  Advanced Glycation End Products: A Review , 2013 .

[81]  Hening Lin,et al.  Protein lysine acylation and cysteine succination by intermediates of energy metabolism. , 2012, ACS chemical biology.

[82]  A. Kraus,et al.  Carbamoylation of amino acids and proteins in uremia. , 2001, Kidney international. Supplement.

[83]  Adrian Drazic,et al.  The physiological role of reversible methionine oxidation. , 2014, Biochimica et biophysica acta.

[84]  Joanne I. Yeh,et al.  Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. , 1999, Biochemistry.

[85]  James E. Ferrell,et al.  Mechanisms of specificity in protein phosphorylation , 2007, Nature Reviews Molecular Cell Biology.

[86]  E. Topol,et al.  Protein carbamylation links inflammation, smoking, uremia and atherogenesis , 2007, Nature Medicine.