Redox requirements for ubiquitin-like urmylation of Ahp1, a 2-Cys peroxiredoxin from yeast

Wood, 2003, Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling, Science, 300, 650, 10.1126/science.1080405 Rhee, 2005, Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling, Free Radic. Biol. Med., 38, 1543, 10.1016/j.freeradbiomed.2005.02.026 Groitl, 2014, Thiol-based redox switches, Biochim. Biophys. Acta, 1844, 1335, 10.1016/j.bbapap.2014.03.007 Kumsta, 2011, Effects of oxidative stress on behavior, physiology, and the redox thiol proteome of Caenorhabditis elegans, Antioxidants Redox Signal., 14, 1023, 10.1089/ars.2010.3203 Lee, 2003, Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice, Blood, 101, 5033, 10.1182/blood-2002-08-2548 Neumann, 2003, Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression, Nature, 424, 561, 10.1038/nature01819 Morano, 2012, The response to heat shock and oxidative stress in Saccharomyces cerevisiae, Genetics, 190, 1157, 10.1534/genetics.111.128033 Fomenko, 2011, Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide, Proc. Natl. Acad. Sci. U. S. A., 108, 2729, 10.1073/pnas.1010721108 Delaunay, 2000, H2O2 sensing through oxidation of the Yap1 transcription factor, EMBO J., 19, 5157, 10.1093/emboj/19.19.5157 Delaunay, 2002, A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation, Cell, 111, 471, 10.1016/S0092-8674(02)01048-6 Lee, 1999, A new antioxidant with alkyl hydroperoxide defense properties in yeast, J. Biol. Chem., 274, 4537, 10.1074/jbc.274.8.4537 Trivelli, 2003, Characterization of the yeast peroxiredoxin Ahp1 in its reduced active and overoxidized inactive forms using NMR, Biochemistry, 42, 14139, 10.1021/bi035551r Munhoz, 2004, Cytosolic thioredoxin peroxidase I and II are important defenses of yeast against organic hydroperoxide insult: catalases and peroxiredoxins cooperate in the decomposition of H2O2 by yeast, J. Biol. Chem., 279, 35219, 10.1074/jbc.M313773200 Allan, 2016, Trapping redox partnerships in oxidant-sensitive proteins with a small, thiol-reactive cross-linker, Free Radic. Biol. Med., 101, 356, 10.1016/j.freeradbiomed.2016.10.506 Lian, 2012, Structural snapshots of yeast alkyl hydroperoxide reductase Ahp1 peroxiredoxin reveal a novel two-cysteine mechanism of electron transfer to eliminate reactive oxygen species, J. Biol. Chem., 287, 17077, 10.1074/jbc.M112.357368 Jeong, 1999, Purification and characterization of a second type thioredoxin peroxidase (type II TPx) from Saccharomyces cerevisiae, Biochemistry, 38, 776, 10.1021/bi9817818 Furukawa, 2000, A protein conjugation system in yeast with homology to biosynthetic enzyme reaction of prokaryotes, J. Biol. Chem., 275, 7462, 10.1074/jbc.275.11.7462 Goehring, 2003, Attachment of the ubiquitin-related protein Urm1p to the antioxidant protein Ahp1p, Eukaryot. Cell, 2, 930, 10.1128/EC.2.5.930-936.2003 Jüdes, 2016, Sulfur transfer and activation by ubiquitin-like modifier system Uba4*Urm1 link protein urmylation and tRNA thiolation in yeast, Microb Cell, 3, 554, 10.15698/mic2016.11.539 Jüdes, 2015, Urmylation and tRNA thiolation functions of ubiquitin-like Uba4.Urm1 systems are conserved from yeast to man, FEBS Lett., 589, 904, 10.1016/j.febslet.2015.02.024 Van der Veen, 2011, Role of the ubiquitin-like protein Urm1 as a noncanonical lysine-directed protein modifier, Proc. Natl. Acad. Sci. U. S. A., 108, 1763, 10.1073/pnas.1014402108 Wang, 2019, Urm1-mediated ubiquitin-like modification is required for oxidative stress adaptation during infection of the rice blast fungus, Front. Microbiol., 10, 2039, 10.3389/fmicb.2019.02039 Huang, 2005, An early step in wobble uridine tRNA modification requires the Elongator complex, RNA, 11, 424, 10.1261/rna.7247705 Schaffrath, 2017, Wobble uridine modifications-a reason to live, a reason to die?!, RNA Biol., 14, 1209, 10.1080/15476286.2017.1295204 Sokolowski, 2017, Cooperativity between different tRNA modifications and their modification pathways, Biochim. Biophys. Acta Shigi, 2018, Recent advances in our understanding of the biosynthesis of sulfur modifications in tRNAs, Front. Microbiol., 9, 2679, 10.3389/fmicb.2018.02679 Huang, 2008, A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2-thiouridine in Saccharomyces cerevisiae, RNA, 14, 2183, 10.1261/rna.1184108 Jablonowski, 2007, Zymocin, a composite chitinase and tRNase killer toxin from yeast, Biochem. Soc. Trans., 35, 1533, 10.1042/BST0351533 Termathe, 2018, The Uba4 domain interplay is mediated via a thioester that is critical for tRNA thiolation through Urm1 thiocarboxylation, Nucleic Acids Res., 46, 5171, 10.1093/nar/gky312 Pedrioli, 2008, Urm1 at the crossroad of modifications. 'Protein modifications: beyond the usual suspects' review series, EMBO Rep., 9, 1196, 10.1038/embor.2008.209 Petroski, 2011, Urm1 couples sulfur transfer to ubiquitin-like protein function in oxidative stress, Proc. Natl. Acad. Sci. U. S. A., 108, 1749, 10.1073/pnas.1019043108 Khoshnood, 2016, Urm1: an essential regulator of JNK signaling and oxidative stress in Drosophila melanogaster, Cell. Mol. Life Sci., 73, 1939, 10.1007/s00018-015-2121-x Hleihel, 2018, The HTLV-1 oncoprotein Tax is modified by the ubiquitin related modifier 1 (Urm1), Retrovirology, 15, 33, 10.1186/s12977-018-0415-4 Nakai, 2012, Arabidopsis molybdopterin biosynthesis protein Cnx5 collaborates with the ubiquitin-like protein Urm11 in the thio-modification of tRNA, J. Biol. Chem., 287, 30874, 10.1074/jbc.M112.350090 Anjum, 2015, Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius, Nat. Commun., 6, 8163, 10.1038/ncomms9163 Maupin-Furlow, 2014, Prokaryotic ubiquitin-like protein modification, Annu. Rev. Microbiol., 68, 155, 10.1146/annurev-micro-091313-103447 Shigi, 2012, Posttranslational modification of cellular proteins by a ubiquitin-like protein in bacteria, J. Biol. Chem., 287, 17568, 10.1074/jbc.M112.359844 Hochstrasser, 2009, Origin and function of ubiquitin-like proteins, Nature, 458, 422, 10.1038/nature07958 Iwai, 2010, Peroxiredoxin Ahp1 acts as a receptor for alkylhydroperoxides to induce disulfide bond formation in the Cad1 transcription factor, J. Biol. Chem., 285, 10597, 10.1074/jbc.M109.090142 Verdoucq, 1999, In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family, J. Biol. Chem., 274, 19714, 10.1074/jbc.274.28.19714 Prouzet-Mauleon, 2002, Identification in Saccharomyces cerevisiae of a new stable variant of alkyl hydroperoxide reductase 1 (Ahp1) induced by oxidative stress, J. Biol. Chem., 277, 4823, 10.1074/jbc.M109614200 Igloi, 1988, Interaction of tRNAs and of phosphorothioate-substituted nucleic acids with an organomercurial. Probing the chemical environment of thiolated residues by affinity electrophoresis, Biochemistry, 27, 3842, 10.1021/bi00410a048 Loberg, 2019, Aromatic residues at the dimer-dimer interface in the peroxiredoxin Tsa1 facilitate decamer formation and biological function Cappadocia, 2018, Ubiquitin-like protein conjugation: structures, chemistry, and mechanism, Chem. Rev., 118, 889, 10.1021/acs.chemrev.6b00737 Schmitz, 2008, The sulfurtransferase activity of Uba4 presents a link between ubiquitin-like protein conjugation and activation of sulfur carrier proteins, Biochemistry, 47, 6479, 10.1021/bi800477u Leidel, 2009, Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA, Nature, 458, 228, 10.1038/nature07643 Nakai, 2008, Thio-modification of yeast cytosolic tRNA requires a ubiquitin-related system that resembles bacterial sulfur transfer systems, J. Biol. Chem., 283, 27469, 10.1074/jbc.M804043200 Noma, 2009, Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions, Nucleic Acids Res., 37, 1335, 10.1093/nar/gkn1023 Schlieker, 2008, A functional proteomics approach links the ubiquitin-related modifier Urm1 to a tRNA modification pathway, Proc. Natl. Acad. Sci. U. S. A., 105, 18255, 10.1073/pnas.0808756105 Rudolph, 2001, Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation, Nat. Struct. Biol., 8, 42, 10.1038/87531 Wang, 2001, Solution structure of ThiS and implications for the evolutionary roots of ubiquitin, Nat. Struct. Biol., 8, 47, 10.1038/83041 Wang, 2011, The dual role of ubiquitin-like protein Urm1 as a protein modifier and sulfur carrier, Protein Cell, 2, 612, 10.1007/s13238-011-1074-6 Ho, 2018, Unification of protein abundance datasets yields a quantitative Saccharomyces cerevisiae proteome, Cell Syst, 6, 192, 10.1016/j.cels.2017.12.004 Sadowski, 2010, Mechanisms of mono- and poly-ubiquitination: ubiquitination specificity depends on compatibility between the E2 catalytic core and amino acid residues proximal to the lysine, Cell Div., 5, 19, 10.1186/1747-1028-5-19 Haynes, 2013, Molecular basis for the resistance of human mitochondrial 2-Cys peroxiredoxin 3 to hyperoxidation, J. Biol. Chem., 288, 29714, 10.1074/jbc.M113.473470 Randall, 2014, Nitration transforms a sensitive peroxiredoxin 2 into a more active and robust peroxidase, J. Biol. Chem., 289, 15536, 10.1074/jbc.M113.539213 Perkins, 2014, Tuning of peroxiredoxin catalysis for various physiological roles, Biochemistry, 53, 7693, 10.1021/bi5013222 Kumar, 2011, Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control, EMBO J., 30, 2044, 10.1038/emboj.2011.105 Perkins, 2015, Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling, Trends Biochem. Sci., 40, 435, 10.1016/j.tibs.2015.05.001 Bodvard, 2017, Light-sensing via hydrogen peroxide and a peroxiredoxin, Nat. Commun., 8, 14791, 10.1038/ncomms14791 Goehring, 2003, Urmylation: a ubiquitin-like pathway that functions during invasive growth and budding in yeast, Mol. Biol. Cell, 14, 4329, 10.1091/mbc.e03-02-0079 Cadwell, 2005, Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase, Science, 309, 127, 10.1126/science.1110340 Cadwell, 2008, The specificities of Kaposi's sarcoma-associated herpesvirus-encoded E3 ubiquitin ligases are determined by the positions of lysine or cysteine residues within the intracytoplasmic domains of their targets, J. Virol., 82, 4184, 10.1128/JVI.02264-07 Williams, 2007, A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p, J. Biol. Chem., 282, 22534, 10.1074/jbc.M702038200 Hall, 2010, Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization, J. Mol. Biol., 402, 194, 10.1016/j.jmb.2010.07.022 Malins, 2014, Recent extensions to native chemical ligation for the chemical synthesis of peptides and proteins, Curr. Opin. Chem. Biol., 22, 70, 10.1016/j.cbpa.2014.09.021 Tam, 1995, Peptide synthesis using unprotected peptides through orthogonal coupling methods, Proc. Natl. Acad. Sci. U. S. A., 92, 12485, 10.1073/pnas.92.26.12485 Tam, 2001, Methods and strategies of peptide ligation, Biopolymers, 60, 194, 10.1002/1097-0282(2001)60:3<194::AID-BIP10031>3.0.CO;2-8 Ju, 2006, Identification of the preferential ubiquitination site and ubiquitin-dependent degradation signal of Rpn4, J. Biol. Chem., 281, 10657, 10.1074/jbc.M513790200 Sadowski, 2010, Molecular basis for lysine specificity in the yeast ubiquitin-conjugating enzyme Cdc34, Mol. Cell Biol., 30, 2316, 10.1128/MCB.01094-09 Suryadinata, 2013, Molecular and structural insight into lysine selection on substrate and ubiquitin lysine 48 by the ubiquitin-conjugating enzyme Cdc34, Cell Cycle, 12, 1732, 10.4161/cc.24818 Manganelli, 2002, Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression, Mol. Microbiol., 45, 365, 10.1046/j.1365-2958.2002.03005.x Biteau, 2003, ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin, Nature, 425, 980, 10.1038/nature02075 Sherman, 1991, Getting started with yeast, Methods Enzymol., 194, 3, 10.1016/0076-6879(91)94004-V Gueldener, 2002, A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast, Nucleic Acids Res., 30, e23, 10.1093/nar/30.6.e23 Knop, 1999, Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines, Yeast, 15, 963, 10.1002/(SICI)1097-0061(199907)15:10B<963::AID-YEA399>3.0.CO;2-W Jacobus, 2015, Optimal cloning of PCR fragments by homologous recombination in Escherichia coli, PloS One, 10, 10.1371/journal.pone.0119221 Edelheit, 2009, Simple and efficient site-directed mutagenesis using two single-primer reactions in parallel to generate mutants for protein structure-function studies, BMC Biotechnol., 9, 61, 10.1186/1472-6750-9-61 Zheng, 2004, An efficient one-step site-directed and site-saturation mutagenesis protocol, Nucleic Acids Res., 32, e115, 10.1093/nar/gnh110 Gietz, 1988, New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites, Gene, 74, 527, 10.1016/0378-1119(88)90185-0 Christianson, 1992, Multifunctional yeast high-copy-number shuttle vectors, Gene, 110, 119, 10.1016/0378-1119(92)90454-W Gietz, 2002, Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method, Methods Enzymol., 350, 87, 10.1016/S0076-6879(02)50957-5 Chen, 1992, One-step transformation of yeast in stationary phase, Curr. Genet., 21, 83, 10.1007/BF00318659 Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 Lämmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 Kinsland, 1998, Overexpression of recombinant proteins with a C-terminal thiocarboxylate: implications for protein semisynthesis and thiamin biosynthesis, Protein Sci., 7, 1839, 10.1002/pro.5560070821 West, 2011, Enhanced toxicity of the protein cross-linkers divinyl sulfone and diethyl acetylenedicarboxylate in comparison to related monofunctional electrophiles, Chem. Res. Toxicol., 24, 1457, 10.1021/tx200302w Spencer, 2013, Pronounced toxicity differences between homobifunctional protein cross-linkers and analogous monofunctional electrophiles, Chem. Res. Toxicol., 26, 1720, 10.1021/tx400290j