Arginylation Regulates Cytoskeleton Organization and Cell Division and Affects Mitochondria in Fission Yeast

REFERENCES

• Kashina AS. 2015. Protein arginylation: over 50 years of discovery. Methods Mol Biol 1337:1–11. https://doi.org/10.1007/978-1-4939-2935-1_1.
   PubMedGoogle Scholar
• Kashina A. 2014. Protein arginylation, a global biological regulator that targets actin cytoskeleton and the muscle. Anat Rec (Hoboken) 297:1630–1636. https://doi.org/10.1002/ar.22969.
   PubMedGoogle Scholar
• Rai R, Kashina A. 2005. Identification of mammalian arginyltransferases that modify a specific subset of protein substrates. Proc Natl Acad Sci USA 102:10123–10128. https://doi.org/10.1073/pnas.0504500102.
   PubMed Web of Science ®Google Scholar
• Kwon YT, Kashina AS, Varshavsky A. 1999. Alternative splicing results in differential expression, activity, and localization of the two forms of arginyl-tRNA-protein transferase, a component of the N-end rule pathway. Mol Cell Biol 19:182–193. and https://doi.org/10.1128/MCB.19.1.182.
   PubMed Web of Science ®Google Scholar
• Graciet E, Walter F, Ó'Maoiléidigh DS, Pollmann S, Meyerowitz EM, Varshavsky A, Wellmer F. 2009. The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. Proc Natl Acad Sci USA 106:13618–13623. https://doi.org/10.1073/pnas.0906404106.
   PubMed Web of Science ®Google Scholar
• Kwon YT, Kashina AS, Davydov IV, Hu R-G, An JY, Seo JW, Du F, Varshavsky A. 2002. An essential role of N-terminal arginylation in cardiovascular development. Science 297:96–99. https://doi.org/10.1126/science.1069531.
   PubMed Web of Science ®Google Scholar
• Kurosaka S, Leu NA, Zhang F, Bunte R, Saha S, Wang J, Guo C, He W, Kashina A. 2010. Arginylation-dependent neural crest cell migration is essential for mouse development. PLoS Genet 6:e1000878. https://doi.org/10.1371/journal.pgen.1000878.
   Google Scholar
• Leite FS, Minozzo FC, Kalganov A, Cornachione AS, Cheng Y-S, Leu NA, Han X, Saripalli C, Yates JR III, Granzier H, Kashina AS, Rassier DE. 2016. Reduced passive force in skeletal muscles lacking protein arginylation. Am J Physiol Cell Physiol 310:C127–C135. https://doi.org/10.1152/ajpcell.00269.2015.
   PubMed Web of Science ®Google Scholar
• de Souza Leite F, Kashina A, Rassier DE. 2016. Posttranslational arginylation regulates striated muscle function. Exerc Sport Sci Rev 44:98–103. https://doi.org/10.1249/JES.0000000000000079.
   PubMed Web of Science ®Google Scholar
• Wang J, Han X, Leu NA, Sterling S, Kurosaka S, Fina M, Lee VM, Dong DW, Yates JR III, Kashina A. 2017. Protein arginylation targets alpha synuclein, facilitates normal brain health, and prevents neurodegeneration. Sci Rep 7:11323. https://doi.org/10.1038/s41598-017-11713-z.
   PubMed Web of Science ®Google Scholar
• Cornachione AS, Leite FS, Wang J, Leu NA, Kalganov A, Volgin D, Han X, Xu T, Cheng Y-S, Yates JRR III, Rassier DE, Kashina A. 2014. Arginylation of myosin heavy chain regulates skeletal muscle strength. Cell Rep 8:470–476. https://doi.org/10.1016/j.celrep.2014.06.019.
   PubMed Web of Science ®Google Scholar
• Zhang F, Saha S, Kashina A. 2012. Arginylation-dependent regulation of a proteolytic product of talin is essential for cell-cell adhesion. J Cell Biol 197:819–836. https://doi.org/10.1083/jcb.201112129.
   PubMed Web of Science ®Google Scholar
• Saha S, Wong CCL, Xu T, Namgoong S, Zebroski H, Yates JR III, Kashina A. 2011. Arginylation and methylation double up to regulate nuclear proteins and nuclear architecture in vivo. Chem Biol 18:1369–1378. https://doi.org/10.1016/j.chembiol.2011.08.019.
   PubMedGoogle Scholar
• Wong CCL, Xu T, Rai R, Bailey AO, Yates JR III, Wolf YI, Zebroski H, Kashina A. 2007. Global analysis of posttranslational protein arginylation. PLoS Biol 5:e258. https://doi.org/10.1371/journal.pbio.0050258.
   Web of Science ®Google Scholar
• Balzi E, Choder M, Chen WN, Varshavsky A, Goffeau A. 1990. Cloning and functional analysis of the arginyl-tRNA-protein transferase gene ATE1 of Saccharomyces cerevisiae. J Biol Chem 265:7464–7471. https://doi.org/10.1016/S0021-9258(19)39136-7.
   PubMed Web of Science ®Google Scholar
• Varshavsky A. 1997. The N-end rule pathway of protein degradation. Genes Cells 2:13–28. https://doi.org/10.1046/j.1365-2443.1997.1020301.x.
   PubMed Web of Science ®Google Scholar
• Van V, Smith AT. 2020. ATE1-mediated post-translational arginylation is an essential regulator of eukaryotic cellular homeostasis. ACS Chem Biol 15:3073–3085. https://doi.org/10.1021/acschembio.0c00677.
   PubMed Web of Science ®Google Scholar
• Wiley DJ, D'Urso G, Zhang F. 2020. Posttranslational arginylation enzyme arginyltransferase1 shows genetic interactions with specific cellular pathways in vivo. Front Physiol 11:427. https://doi.org/10.3389/fphys.2020.00427.
   PubMed Web of Science ®Google Scholar
• Deka K, Saha S. 2021. Heat stress induced arginylation of HuR promotes alternative polyadenylation of Hsp70.3 by regulating HuR stability and RNA binding. Cell Death Differ 28:730–747. https://doi.org/10.1038/s41418-020-00619-5.
   PubMed Web of Science ®Google Scholar
• Deka K, Singh A, Chakraborty S, Mukhopadhyay R, Saha S. 2016. Protein arginylation regulates cellular stress response by stabilizing HSP70 and HSP40 transcripts. Cell Death Discov 2:16074. https://doi.org/10.1038/cddiscovery.2016.74.
   PubMed Web of Science ®Google Scholar
• Kumar A, Birnbaum MD, Patel DM, Morgan WM, Singh J, Barrientos A, Zhang F. 2016. Posttranslational arginylation enzyme Ate1 affects DNA mutagenesis by regulating stress response. Cell Death Dis 7:e2378. https://doi.org/10.1038/cddis.2016.284.
   Google Scholar
• Zhao Y, Lieberman HB. 1995. Schizosaccharomyces pombe: a model for molecular studies of eukaryotic genes. DNA Cell Biol 14:359–371. https://doi.org/10.1089/dna.1995.14.359.
   PubMed Web of Science ®Google Scholar
• Loiodice I, Staub J, Setty TG, Nguyen N-PT, Paoletti A, Tran PT. 2005. Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol Biol Cell 16:1756–1768. https://doi.org/10.1091/mbc.e04-10-0899.
   PubMed Web of Science ®Google Scholar
• Nabeshima K, Nakagawa T, Straight AF, Murray A, Chikashige Y, Yamashita YM, Hiraoka Y, Yanagida M. 1998. Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol Biol Cell 9:3211–3225. https://doi.org/10.1091/mbc.9.11.3211.
   PubMed Web of Science ®Google Scholar
• Tran PT, Marsh L, Doye V, Inoué S, Chang F. 2001. A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411. https://doi.org/10.1083/jcb.153.2.397.
   PubMed Web of Science ®Google Scholar
• Karakozova M, Kozak M, Wong CCL, Bailey AO, Yates JR III, Mogilner A, Zebroski H, Kashina A. 2006. Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science 313:192–196. https://doi.org/10.1126/science.1129344.
   PubMed Web of Science ®Google Scholar
• Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R. 2008. LifeAct: a versatile marker to visualize F-actin. Nat Methods 5:605–607. https://doi.org/10.1038/nmeth.1220.
   PubMed Web of Science ®Google Scholar
• Arai R, Mabuchi I. 2002. F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. J Cell Sci 115:887–898. https://doi.org/10.1242/jcs.115.5.887.
   PubMed Web of Science ®Google Scholar
• Martin SG, Arkowitz RA. 2014. Cell polarization in budding and fission yeasts. FEMS Microbiol Rev 38:228–253. https://doi.org/10.1111/1574-6976.12055.
   PubMed Web of Science ®Google Scholar
• EauClaire S, Guo W. 2003. Conservation and specialization. The role of the exocyst in neuronal exocytosis. Neuron 37:369–370. https://doi.org/10.1016/S0896-6273(03)00059-X.
   PubMed Web of Science ®Google Scholar
• He B, Guo W. 2009. The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21:537–542. https://doi.org/10.1016/j.ceb.2009.04.007.
   PubMed Web of Science ®Google Scholar
• Lacy MM, Ma R, Ravindra NG, Berro J. 2018. Molecular mechanisms of force production in clathrin-mediated endocytosis. FEBS Lett 592:3586–3605. https://doi.org/10.1002/1873-3468.13192.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Wu B, Guo W. 2019. The role of Exo70 in exocytosis and beyond. Small GTPases 10:331–335.
   PubMedGoogle Scholar
• Etienne-Manneville S. 2004. Cdc42—the centre of polarity. J Cell Sci 117:1291–1300. https://doi.org/10.1242/jcs.01115.
   PubMed Web of Science ®Google Scholar
• Rincon SA, Estravis M, Perez P. 2014. Cdc42 regulates polarized growth and cell integrity in fission yeast. Biochem Soc Trans 42:201–205. https://doi.org/10.1042/BST20130155.
   PubMed Web of Science ®Google Scholar
• Chiou J-G, Balasubramanian MK, Lew DJ. 2017. Cell polarity in yeast. Annu Rev Cell Dev Biol 33:77–101. https://doi.org/10.1146/annurev-cellbio-100616-060856.
   PubMed Web of Science ®Google Scholar
• Estravis M, Rincon S, Perez P. 2012. Cdc42 regulation of polarized traffic in fission yeast. Commun Integr Biol 5:370–373. https://doi.org/10.4161/cib.19977.
   PubMedGoogle Scholar
• Fukuda T, Ebi Y, Saigusa T, Furukawa K, Yamashita S-i, Inoue K, Kobayashi D, Yoshida Y, Kanki T. 2020. Atg43 tethers isolation membranes to mitochondria to promote starvation-induced mitophagy in fission yeast. eLife 9:e61245. https://doi.org/10.7554/eLife.61245.
   PubMed Web of Science ®Google Scholar
• Wu J-Q, Pollard TD. 2005. Counting cytokinesis proteins globally and locally in fission yeast. Science 310:310–314. https://doi.org/10.1126/science.1113230.
   PubMed Web of Science ®Google Scholar
• Wang J, Yates JR III, Kashina A. 2019. Biochemical analysis of protein arginylation. Methods Enzymol 626:89–113. https://doi.org/10.1016/bs.mie.2019.07.028.
   PubMed Web of Science ®Google Scholar
• Xu T, Wong CCL, Kashina A, Yates JR III. 2009. Identification of N-terminally arginylated proteins and peptides by mass spectrometry. Nat Protoc 4:325–332. https://doi.org/10.1038/nprot.2008.248.
   PubMed Web of Science ®Google Scholar
• Futcher B, Latter GI, Monardo P, McLaughlin CS, Garrels JI. 1999. A sampling of the yeast proteome. Mol Cell Biol 19:7357–7368. https://doi.org/10.1128/MCB.19.11.7357.
   PubMed Web of Science ®Google Scholar
• Saha S, Mundia MM, Zhang F, Demers RW, Korobova F, Svitkina T, Perieteanu AA, Dawson JF, Kashina A. 2010. Arginylation regulates intracellular actin polymer level by modulating actin properties and binding of capping and severing proteins. Mol Biol Cell 21:1350–1361. https://doi.org/10.1091/mbc.e09-09-0829.
   PubMed Web of Science ®Google Scholar
• McNally FJ, Roll-Mecak A. 2018. Microtubule-severing enzymes: from cellular functions to molecular mechanism. J Cell Biol 217:4057–4069. https://doi.org/10.1083/jcb.201612104.
   PubMed Web of Science ®Google Scholar
• Pidoux AL, LeDizet M, Cande WZ. 1996. Fission yeast pkl1 is a kinesin-related protein involved in mitotic spindle function. Mol Biol Cell 7:1639–1655. https://doi.org/10.1091/mbc.7.10.1639.
   PubMed Web of Science ®Google Scholar
• Marks J, Hagan IM, Hyams JS. 1986. Growth polarity and cytokinesis in fission yeast: the role of the cytoskeleton. J Cell Sci Suppl 5:229–241. https://doi.org/10.1242/jcs.1986.supplement_5.15.
   PubMedGoogle Scholar
• Sawin KE, Tran PT. 2006. Cytoplasmic microtubule organization in fission yeast. Yeast 23:1001–1014. https://doi.org/10.1002/yea.1404.
   PubMed Web of Science ®Google Scholar
• Jiang C, Moorthy BT, Patel DM, Kumar A, Morgan WM, Alfonso B, Huang J, Lampidis TJ, Isom DG, Barrientos A, Fontanesi F, Zhang F. 2020. Regulation of mitochondrial respiratory chain complex levels, organization, and function by arginyltransferase 1. Front Cell Dev Biol 8:603688. https://doi.org/10.3389/fcell.2020.603688.
   PubMed Web of Science ®Google Scholar
• Heo AJ, Kim SB, Ji CH, Han D, Lee SJ, Lee SH, Lee MJ, Lee JS, Ciechanover A, Kim BY, Kwon YT. 2021. The N-terminal cysteine is a dual sensor of oxygen and oxidative stress. Proc Natl Acad Sci USA 118:e2107993118. https://doi.org/10.1073/pnas.2107993118.
   Google Scholar
• Okamoto K, Shaw JM. 2005. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu Rev Genet 39:503–536. https://doi.org/10.1146/annurev.genet.38.072902.093019.
   PubMed Web of Science ®Google Scholar
• Westermann B. 2010. Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11:872–884. https://doi.org/10.1038/nrm3013.
   PubMed Web of Science ®Google Scholar
• Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795–823. https://doi.org/10.1016/0076-6879(91)94059-l.
   PubMed Web of Science ®Google Scholar
• Tran PT, Paoletti A, Chang F. 2004. Imaging green fluorescent protein fusions in living fission yeast cells. Methods 33:220–225. https://doi.org/10.1016/j.ymeth.2003.11.017.
   PubMed Web of Science ®Google Scholar