Pex30 undergoes phosphorylation and regulates peroxisome number in Saccharomyces cerevisiae

Springer Science and Business Media LLC - Tập 297 Số 2 - Trang 573-590 - 2022
Nayan Moni Deori1, Terence Infant1, Pradeep Kumar Sundaravadivelu2, Rajkumar P. Thummer2, Shirisha Nagotu1
1Organelle Biology and Cellular Ageing Lab, Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Assam, India
2Laboratory for Stem Cell Engineering and Regenerative Medicine, Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Assam, India

Tóm tắt

Từ khóa


Tài liệu tham khảo

Akşit A, van der Klei IJ (2018) Yeast peroxisomes: how are they formed and how do they grow? Int J Biochem Cell Biol 105:24–34. https://doi.org/10.1016/j.biocel.2018.09.019

Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H (2008) A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7:1389–1396. https://doi.org/10.1074/mcp.M700468-MCP200

Baerends RJ, Faber KN, Kram AM, Kiel JA, van der Klei IJ, Veenhuis M (2000) A stretch of positively charged amino acids at the N terminus of Hansenula polymorpha Pex3p is involved in incorporation of the protein into the peroxisomal membrane. J Biol Chem 275:9986–9995. https://doi.org/10.1074/jbc.275.14.9986

Balta E-A, Wittmann M-T, Jung M, Sock E, Haeberle BM, Heim B, von Zweydorf F, Heppt J, von Wittgenstein J, Gloeckner CJ, Lie DC (2018) Phosphorylation modulates the subcellular localization of SOX11. Front Mol Neurosci. https://doi.org/10.3389/fnmol.2018.00211

Cohen P (2002) The origins of protein phosphorylation. Nat Cell Biol 4:E127–E130. https://doi.org/10.1038/ncb0502-e127

David C, Koch J, Oeljeklaus S, Laernsack A, Melchior S, Wiese S, Schummer A, Erdmann R, Warscheid B, Brocard C (2013) A combined approach of quantitative interaction proteomics and live-cell imaging reveals a regulatory role for endoplasmic reticulum (ER) reticulon homology proteins in peroxisome biogenesis. Mol Cell Proteom 12:2408–2425. https://doi.org/10.1074/mcp.M112.017830

Deb R, Nagotu S (2017) Versatility of peroxisomes: an evolving concept. Tissue Cell 49:209–226. https://doi.org/10.1016/j.tice.2017.03.002

Deori NM, Kale A, Maurya PK, Nagotu S (2018) Peroxisomes: role in cellular ageing and age related disorders. Biogerontology 19:303–324. https://doi.org/10.1007/s10522-018-9761-9

Ferreira JV, Carvalho P (2021) Pex30-like proteins function as adaptors at distinct ER membrane contact sites. J Cell Biol 220:e202103176. https://doi.org/10.1083/jcb.202103176

Gietz RD, Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534. https://doi.org/10.1016/0378-1119(88)90185-0

Greenfield NJ (2006) Using circular dichroism spectra to estimate protein secondary structure. Nat Protoc 1:2876–2890. https://doi.org/10.1038/nprot.2006.202

Haridhasapavalan KK, Sundaravadivelu PK, Bhattacharyya S, Ranjan SH, Raina K, Thummer RP (2021) Generation of cell-permeant recombinant human transcription factor GATA4 from E. coli. Bioproc Biosyst Eng 44:1131–1146. https://doi.org/10.1007/s00449-021-02516-8

Hildebrand A, Remmert M, Biegert A, Söding J (2009) Fast and accurate automatic structure prediction with HHpred. Proteins 77(Suppl 9):128–132. https://doi.org/10.1002/prot.22499

Hunter T (2012) Why nature chose phosphate to modify proteins. Philos Trans R Soc Lond Ser B Biol Sci 367:2513–2516. https://doi.org/10.1098/rstb.2012.0013

Infant T, Deb R, Ghose S, Nagotu S (2021) Post-translational modifications of proteins associated with yeast peroxisome membrane: an essential mode of regulatory mechanism. Genes Cells 00:1–18. https://doi.org/10.1111/gtc.12892

Johnson LN, Barford D (1993) The effects of phosphorylation on the structure and function of proteins. Annu Rev Biophys Biomol Struct 22:199–232. https://doi.org/10.1146/annurev.bb.22.060193.001215

Joshi S, Agrawal G, Subramani S (2012) Phosphorylation-dependent Pex11p and Fis1p interaction regulates peroxisome division. Mol Biol Cell 23:1307–1315. https://doi.org/10.1091/mbc.E11-09-0782

Joshi AS, Huang X, Choudhary V, Levine TP, Hu J, Prinz WA (2016) A family of membrane-shaping proteins at ER subdomains regulates pre-peroxisomal vesicle biogenesis. J Cell Biol 215:515–529. https://doi.org/10.1083/jcb.201602064

Joshi AS, Nebenfuehr B, Choudhary V, Satpute-Krishnan P, Levine TP, Golden A, Prinz WA (2018) Lipid droplet and peroxisome biogenesis occur at the same ER subdomains. Nat Commun 9:2940. https://doi.org/10.1038/s41467-018-05277-3

Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589. https://doi.org/10.1038/s41586-021-03819-2

Kelly SM, Jess TJ, Price NC (2005) How to study proteins by circular dichroism. BBA-Proteins Proteomics 1751:119–139. https://doi.org/10.1016/j.bbapap.2005.06.005

Kinoshita E, Kinoshita-Kikuta E, Koike T (2009) Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc 4:1513–1521. https://doi.org/10.1038/nprot.2009.154

Knoblach B, Rachubinski RA (2010) Phosphorylation-dependent activation of peroxisome proliferator protein PEX11 controls peroxisome abundance. J Biol Chem 285:6670–6680. https://doi.org/10.1074/jbc.M109.094805

Kunau W-H, Dommes V, Schulz H (1995) β-Oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog Lipid Res 34:267–342. https://doi.org/10.1016/0163-7827(95)00011-9

Kuravi K, Nagotu S, Krikken AM, Sjollema K, Deckers M, Erdmann R, Veenhuis M, van der Klei IJ (2006) Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J Cell Sci 119:3994–4001. https://doi.org/10.1242/jcs.03166

Lanz MC, Yugandhar K, Gupta S, Sanford EJ, Faça VM, Vega S, Joiner AMN, Fromme JC, Yu H, Smolka MB (2021) In-depth and 3-dimensional exploration of the budding yeast phosphoproteome. EMBO Rep 22:e51121. https://doi.org/10.15252/embr.202051121

Léger J, Kempf M, Lee G, Brandt R (1997) Conversion of serine to aspartate imitates phosphorylation-induced changes in the structure and function of microtubule-associated protein Tau *. J Biol Chem 272:8441–8446. https://doi.org/10.1074/jbc.272.13.8441

Lowry O, Rosebrough N, Farr AL, Randall R (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/S0021-9258(19)52451-6

Mast FD, Jamakhandi A, Saleem RA, Dilworth DJ, Rogers RS, Rachubinski RA, Aitchison JD (2016) Peroxins Pex30 and Pex29 dynamically associate with reticulons to regulate peroxisome biogenesis from the endoplasmic reticulum. J Biol Chem 291:15408–15427. https://doi.org/10.1074/jbc.M116.728154

Metzger MB, Maurer MJ, Dancy BM, Michaelis S (2008) Degradation of a cytosolic protein requires endoplasmic reticulum-associated degradation machinery. J Biol Chem 283:32302–32316. https://doi.org/10.1074/jbc.M806424200

Micsonai A, Wien F, Kernya L, Lee YH, Goto Y, Réfrégiers M, Kardos J (2015) Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy. Proc Natl Acad Sci USA 112:E3095-3103. https://doi.org/10.1073/pnas.1500851112

Micsonai A, Wien F, Bulyáki É, Kun J, Moussong É, Lee YH, Goto Y, Réfrégiers M, Kardos J (2018) BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucleic Acids Res 46:W315–W322. https://doi.org/10.1093/nar/gky497

Nishi H, Hashimoto K, Panchenko Anna R (2011) Phosphorylation in protein-protein binding: effect on stability and function. Structure 19:1807–1815. https://doi.org/10.1016/j.str.2011.09.021

Oeljeklaus S, Schummer A, Mastalski T, Platta HW, Warscheid B (2016) Regulation of peroxisome dynamics by phosphorylation. BBA-Mol Cell Res 1863:1027–1037. https://doi.org/10.1016/j.bbamcr.2015.12.022

Okumoto K, El Shermely M, Natsui M, Kosako H, Natsuyama R, Marutani T, Fujiki Y (2020) The peroxisome counteracts oxidative stresses by suppressing catalase import via Pex14 phosphorylation. Elife. https://doi.org/10.7554/eLife.55896

Olsen JV, de Godoy LMF, Li G, Macek B, Mortensen P, Pesch R, Makarov A, Lange O, Horning S, Mann M (2005) Parts per million mass accuracy on an orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 4:2010–2021. https://doi.org/10.1074/mcp.T500030-MCP200

Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK (2006) Peroxisomal β-oxidation—a metabolic pathway with multiple functions. BBA-Mol Cell Res 1763:1413–1426. https://doi.org/10.1016/j.bbamcr.2006.08.034

Saleem RA, Rogers RS, Ratushny AV, Dilworth DJ, Shannon PT, Shteynberg D, Wan Y, Moritz RL, Nesvizhskii AI, Rachubinski RA, Aitchison JD (2010) Integrated phosphoproteomics analysis of a signaling network governing nutrient response and peroxisome induction. Mol Cell Proteomics 9:2076–2088. https://doi.org/10.1074/mcp.M000116-MCP201

Schummer A, Maier R, Gabay-Maskit S, Hansen T, Mühlhäuser WWD, Suppanz I, Fadel A, Schuldiner M, Girzalsky W, Oeljeklaus S, Zalckvar E, Erdmann R, Warscheid B (2020) Pex14p Phosphorylation modulates import of citrate synthase 2 into peroxisomes in saccharomyces cerevisiae. Front Cell Dev Biol 8:955. https://doi.org/10.3389/fcell.2020.549451

Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75

Smaczynska-de Rooij Iwona I, Marklew Christopher J, Allwood Ellen G, Palmer Sarah E, Booth Wesley I, Mishra R, Goldberg Martin W, Ayscough Kathryn R (2016) Phosphorylation regulates the endocytic function of the yeast dynamin-related protein Vps1. Mol Cell Biol 36:742–755. https://doi.org/10.1128/MCB.00833-15

Subramani S, Koller A, Snyder WB (2000) Import of peroxisomal matrix and membrane proteins. Annu Rev Biochem 69:399–418. https://doi.org/10.1146/annurev.biochem.69.1.399

Sula A, Cole AR, Yeats C, Orengo C, Keep NH (2014) Crystal structures of the human dysferlin inner DYSF domain. BMC Struct Biol 14:3–3. https://doi.org/10.1186/1472-6807-14-3

Swaney DL, Beltrao P, Starita L, Guo A, Rush J, Fields S, Krogan NJ, Villén J (2013) Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods 10:676–682. https://doi.org/10.1038/nmeth.2519

Taylor SS, Keshwani MM, Steichen JM, Kornev AP (2012) Evolution of the eukaryotic protein kinases as dynamic molecular switches. Philos Trans R Soc Lond Ser B Biol Sci 367:2517–2528. https://doi.org/10.1098/rstb.2012.0054

Thomas AS, Krikken AM, van der Klei IJ, Williams CP (2015) Phosphorylation of Pex11p does not regulate peroxisomal fission in the yeast Hansenula polymorpha. Sci Rep 5:11493. https://doi.org/10.1038/srep11493

Vizeacoumar FJ, Torres-Guzman JC, Bouard D, Aitchison JD, Rachubinski RA (2004) Pex30p, Pex31p, and Pex32p form a family of peroxisomal integral membrane proteins regulating peroxisome size and number in Saccharomyces cerevisiae. Mol Biol Cell 15:665–677. https://doi.org/10.1091/mbc.e03-09-0681

Vlastaridis P, Kyriakidou P, Chaliotis A, Van de Peer Y, Oliver SG, Amoutzias GD (2017) Estimating the total number of phosphoproteins and phosphorylation sites in eukaryotic proteomes. GigaScience 6:1–11. https://doi.org/10.1093/gigascience/giw015

Wang W, Malcolm BA (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using quikchange site-directed mutagenesis. Biotechniques 26:680–682. https://doi.org/10.2144/99264st03

Wang S, Idrissi F-Z, Hermansson M, Grippa A, Ejsing CS, Carvalho P (2018) Seipin and the membrane-shaping protein Pex30 cooperate in organelle budding from the endoplasmic reticulum. Nat Commun 9:2939. https://doi.org/10.1038/s41467-018-05278-2

Zhang J, Tripathi DN, Jing J, Alexander A, Kim J, Powell RT, Dere R, Tait-Mulder J, Lee JH, Paull TT, Pandita RK, Charaka VK, Pandita TK, Kastan MB, Walker CL (2015) ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat Cell Biol 17:1259–1269. https://doi.org/10.1038/ncb3230

Zutphen T, Veenhuis M, van der Klei IJ (2008) Pex14 is the sole component of the peroxisomal translocon that is required for pexophagy. Autophagy 4:63–66. https://doi.org/10.4161/auto.5076