Arf6 anchors Cdr2 nodes at the cell cortex to control cell size at division
| dc.audience | Investigador | |
| dc.creator | Opalko, Hannah E. | |
| dc.creator | Miller, Kristi E. | |
| dc.creator | Kim, Hyun Soo | |
| dc.creator | Vargas Garcia, Cesar Augusto | |
| dc.creator | Singh, Abhyudai | |
| dc.creator | Keogh, Michael Christopher | |
| dc.creator | Moseley, James B. | |
| dc.date | 2024-02-23T14:18:20Z | |
| dc.date | 2024-02-23T14:18:20Z | |
| dc.date | 2021 | |
| dc.date | 2021 | |
| dc.date.accessioned | 2026-06-27T04:41:35Z | |
| dc.description | Fission yeast cells prevent mitotic entry until a threshold cell surface area is reached. The protein kinase Cdr2 contributes to this size control system by forming multiprotein nodes that inhibit Wee1 at the medial cell cortex. Cdr2 node anchoring at the cell cortex is not fully understood. Through a genomic screen, we identified the conserved GTPase Arf6 as a component of Cdr2 signaling. Cells lacking Arf6 failed to divide at a threshold surface area and instead shifted to volume-based divisions at increased overall size. Arf6 stably localized to Cdr2 nodes in its GTP-bound but not GDP-bound state, and its guanine nucleotide exchange factor (GEF), Syt22, was required for both Arf6 node localization and proper size at division. In arf6<U+0394> mutants, Cdr2 nodes detached from the membrane and exhibited increased dynamics. These defects were enhanced when arf6<U+0394> was combined with other node mutants. Our work identifies a regulated anchor for Cdr2 nodes that is required for cells to sense surface area. | |
| dc.format | application/pdf | |
| dc.format | application/pdf | |
| dc.identifier | https://doi.org/10.1083/jcb.202109152 | |
| dc.identifier | 0021-9525 | |
| dc.identifier | http://hdl.handle.net/20.500.12324/38936 | |
| dc.identifier | 10.1083/jcb.202109152 | |
| dc.identifier | reponame:Biblioteca Digital Agropecuaria de Colombia | |
| dc.identifier | instname:Corporación colombiana de investigación agropecuaria AGROSAVIA | |
| dc.identifier.uri | http://hdl.handle.net/123456789/35572 | |
| dc.language | spa | |
| dc.publisher | Rockfeller University Press | |
| dc.relation | Journal of Cell Biology | |
| dc.relation | 221 | |
| dc.relation | 2 | |
| dc.relation | 1 | |
| dc.relation | 16 | |
| dc.relation | Akamatsu, M., Y. Lin, J. Bewersdorf, and T.D. Pollard. 2017. Analysis of inter phase node proteins in fission yeast by quantitative and superresolution fluorescence microscopy. Mol. Biol. Cell. 28:3203–3214. https://doi.org/10 .1091/mbc.e16-07-0522 | |
| dc.relation | Allard, C.A.H., H.E. Opalko, K.-W. Liu, U. Medoh, and J.B. Moseley. 2018. Cell size-dependent regulation of Wee1 localization by Cdr2 cortical nodes. J. Cell Biol. 217:1589–1599. https://doi.org/10.1083/jcb.201709171 | |
| dc.relation | Allard, C.A.H., H.E. Opalko, and J.B. Moseley. 2019. Stable Pom1 clusters form a glucose-modulated concentration gradient that regulates mitotic en try. eLife. 8:e46003. https://doi.org/10.7554/eLife.46003 | |
| dc.relation | Almonacid, M., J.B. Moseley, J. Janvore, A. Mayeux, V. Fraisier, P. Nurse, and A. Paoletti. 2009. Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export. Curr. Biol. 19:961–966. https://doi.org/10 .1016/j.cub.2009.04.024 | |
| dc.relation | Amodeo, A.A., and J.M. Skotheim. 2016. Cell-Size Control. Cold Spring Harb. Perspect. Biol. 8:a019083. https://doi.org/10.1101/cshperspect.a019083 | |
| dc.relation | Bahler, J., and J.R. Pringle. 1998. Pom1p, a fission yeast protein kinase that ¨ provides positional information for both polarized growth and cytoki nesis. Genes Dev. 12:1356–1370. https://doi.org/10.1101/gad.12.9.1356 | |
| dc.relation | Bahler, J., J.Q. Wu, M.S. Longtine, N.G. Shah, A. McKenzie III, A.B. Steever, A. ¨ Wach, P. Philippsen, and J.R. Pringle. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosacchar omyces pombe. Yeast. 14:943–951. https://doi.org/10.1002/(SICI)1097 -0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y | |
| dc.relation | Bhatia, P., O. Hachet, M. Hersch, S.A. Rincon, M. Berthelot-Grosjean, S. Dalessi, L. Basterra, S. Bergmann, A. Paoletti, and S.G. Martin. 2014.Distinct levels in Pom1 gradients limit Cdr2 activity and localization to time and position division. Cell Cycle. 13:538–552. https://doi.org/10 .4161/cc.27411 | |
| dc.relation | Breeding, C.S., J. Hudson, M.K. Balasubramanian, S.M. Hemmingsen, P.G. Young, and K.L. Gould. 1998. The cdr2(+) gene encodes a regulator of G2/M progression and cytokinesis in Schizosaccharomyces pombe. Mol. Biol. Cell. 9:3399–3415. https://doi.org/10.1091/mbc.9.12.3399 | |
| dc.relation | Breslow, D.K., D.M. Cameron, S.R. Collins, M. Schuldiner, J. Stewart-Orn stein, H.W. Newman, S. Braun, H.D. Madhani, N.J. Krogan, and J.S. Weissman. 2008. A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat. Methods. 5:711–718. https:// doi.org/10.1038/nmeth.1234 | |
| dc.relation | Celton-Morizur, S., V. Racine, J.-B. Sibarita, and A. Paoletti. 2006. Pom1 ki nase links division plane position to cell polarity by regulating Mid1p cortical distribution. J. Cell Sci. 119:4710–4718. https://doi.org/10.1242/ jcs.03261 | |
| dc.relation | Chang, F., A. Woollard, and P. Nurse. 1996. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J. Cell Sci. 109:131–142. https://doi.org/10.1242/jcs .109.1.131 | |
| dc.relation | Cherfils, J. 2014. Arf GTPases and their effectors: assembling multivalent membrane-binding platforms. Curr. Opin. Struct. Biol. 29:67–76. https:// doi.org/10.1016/j.sbi.2014.09.007 | |
| dc.relation | Coleman, T.R., Z. Tang, and W.G. Dunphy. 1993. Negative regulation of the wee1 protein kinase by direct action of the nim1/cdr1 mitotic inducer. Cell. 72:919–929. https://doi.org/10.1016/0092-8674(93)90580-J | |
| dc.relation | Deng, L., S. Baldissard, A.N. Kettenbach, S.A. Gerber, and J.B. Moseley. 2014. Dueling kinases regulate cell size at division through the SAD kinase Cdr2. Curr. Biol. 24:428–433. https://doi.org/10.1016/j.cub.2014.01.009 | |
| dc.relation | Eng, K., N.I. Naqvi, K.C. Wong, and M.K. Balasubramanian. 1998. Rng2p, a protein required for cytokinesis in fission yeast, is a component of the actomyosin ring and the spindle pole body. Curr. Biol. 8:611–621. https:// doi.org/10.1016/S0960-9822(98)70248-9 | |
| dc.relation | Facchetti, G., B. Knapp, I. Flor-Parra, F. Chang, and M. Howard. 2019. Re programming Cdr2-Dependent Geometry-Based Cell Size Control in Fission Yeast. Curr. Biol. 29:350–358.e4. https://doi.org/10.1016/j.cub .2018.12.017 | |
| dc.relation | Fujita, A. 2008. ADP-ribosylation factor arf6p may function as a molecular switch of new end take off in fission yeast. Biochem. Biophys. Res. Commun. 366:193–198. https://doi.org/10.1016/j.bbrc.2007.11.117 | |
| dc.relation | Fujita, A., and Y. Misumi. 2009. Fission yeast syt22 protein, a putative Arf guanine nucleotide exchange factor, is necessary for new end take off. FEMS Microbiol. Lett. 294:191–197. https://doi.org/10.1111/j.1574-6968 .2009.01566.x | |
| dc.relation | Fujita, A., and Y. Misumi. 2011. Fission yeast ucp3 gene encodes a putative Arf6 GTPase-activating protein. Mol. Biol. Rep. 38:3875–3882. https:// doi.org/10.1007/s11033-010-0503-6 | |
| dc.relation | Gillingham, A.K., and S. Munro. 2007. The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23:579–611. https://doi .org/10.1146/annurev.cellbio.23.090506.123209 | |
| dc.relation | Gould, K.L., and P. Nurse. 1989. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature. 342:39–45. https://doi.org/10.1038/342039a0 | |
| dc.relation | Hagan, I., and M. Yanagida. 1995. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. J. Cell Biol. 129:1033–1047. https://doi.org/10.1083/jcb.129.4 .1033 | |
| dc.relation | Harashima, H., N. Dissmeyer, and A. Schnittger. 2013. Cell cycle control across the eukaryotic kingdom. Trends Cell Biol. 23:345–356. https://doi .org/10.1016/j.tcb.2013.03.002 | |
| dc.relation | Hashimoto, S., Y. Onodera, A. Hashimoto, M. Tanaka, M. Hamaguchi, A. Yamada, and H. Sabe. 2004. Requirement for Arf6 in breast cancer invasive activities. Proc. Natl. Acad. Sci. USA. 101:6647–6652. https://doi .org/10.1073/pnas.0401753101 | |
| dc.relation | Kanoh, J., and P. Russell. 1998. The protein kinase Cdr2, related to Nim1/Cdr1 mitotic inducer, regulates the onset of mitosis in fission yeast. Mol. Biol. Cell. 9:3321–3334. https://doi.org/10.1091/mbc.9.12.3321 | |
| dc.relation | Keifenheim, D., X.-M. Sun, E. D’Souza, M.J. Ohira, M. Magner, M.B. Mayhew, S. Marguerat, and N. Rhind. 2017. Size-Dependent Expression of the Mitotic Activator Cdc25 Suggests a Mechanism of Size Control in Fis sion Yeast. Curr. Biol. 27:1491–1497.e4. https://doi.org/10.1016/j.cub.2017 .04.016 | |
| dc.relation | Kim, H.-S., V. Vanoosthuyse, J. Fillingham, A. Roguev, S. Watt, T. Kislinger, A. Treyer, L.R. Carpenter, C.S. Bennett, A. Emili, et al. 2009. An acetylated form of histone H2A.Z regulates chromosome architecture in Schizosaccharomyces pombe. Nat. Struct. Mol. Biol. 16:1286–1293. https://doi.org/10.1038/nsmb.1688 | |
| dc.relation | Kim, D.-U., J. Hayles, D. Kim, V. Wood, H.-O. Park, M. Won, H.-S. Yoo, T. Duhig, M. Nam, G. Palmer, et al. 2010. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 28:617–623. https://doi.org/10.1038/nbt.1628 | |
| dc.relation | Le Goff, X., F. Motegi, E. Salimova, I. Mabuchi, and V. Simanis. 2000. The S. pombe rlc1 gene encodes a putative myosin regulatory light chain that binds the type II myosins myo3p and myo2p. J. Cell Sci. 113:4157–4163. https://doi.org/10.1242/jcs.113.23.4157 | |
| dc.relation | Li, R., C. Peng, X. Zhang, Y. Wu, S. Pan, and Y. Xiao. 2017. Roles of Arf6 in cancer cell invasion, metastasis and proliferation. Life Sci. 182:80–84. https://doi.org/10.1016/j.lfs.2017.06.008 | |
| dc.relation | Lucena, R., M. Alcaide-Gavilan, S.D. Anastasia, and D.R. Kellogg. 2017. Wee1 ´ and Cdc25 are controlled by conserved PP2A-dependent mechanisms in fission yeast. Cell Cycle. 16:428–435. https://doi.org/10.1080/15384101 .2017.1281476 | |
| dc.relation | Martin, S.G., and M. Berthelot-Grosjean. 2009. Polar gradients of the DYRK family kinase Pom1 couple cell length with the cell cycle. Nature. 459: 852–856. https://doi.org/10.1038/nature08054 | |
| dc.relation | McCollum, D., M.K. Balasubramanian, L.E. Pelcher, S.M. Hemmingsen, and K.L. Gould. 1995. Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis. J. Cell Biol. 130:651–660. https://doi.org/10.1083/jcb.130.3.651 | |
| dc.relation | Miller, K.E., J.O. Magliozzi, N.A. Picard, and J.B. Moseley. 2021. Sequestration of the exocytic SNARE Psy1 into multiprotein nodes reinforces polar ized morphogenesis in fission yeast. Mol. Biol. Cell. 32:ar7. https://doi .org/10.1091/mbc.E20-05-0277 | |
| dc.relation | Moreno, S., P. Nurse, and P. Russell. 1990. Regulation of mitosis by cyclic accumulation of p80cdc25 mitotic inducer in fission yeast. Nature. 344: 549–552. https://doi.org/10.1038/344549a0 | |
| dc.relation | Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795–823. https://doi.org/10.1016/0076-6879(91)94059-L | |
| dc.relation | Morrell, J.L., C.B. Nichols, and K.L. Gould. 2004. The GIN4 family kinase, Cdr2p, acts independently of septins in fission yeast. J. Cell Sci. 117: 5293–5302. https://doi.org/10.1242/jcs.01409 | |
| dc.relation | Moseley, J.B., A. Mayeux, A. Paoletti, and P. Nurse. 2009. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature. 459: 857–860. https://doi.org/10.1038/nature08074 | |
| dc.relation | Naqvi, N.I., K.C. Wong, X. Tang, and M.K. Balasubramanian. 2000. Type II myosin regulatory light chain relieves auto-inhibition of myosin heavy-chain function. Nat. Cell Biol. 2:855–858. https://doi.org/10.1038/ 35041107 | |
| dc.relation | Opalko, H.E., I. Nasa, A.N. Kettenbach, and J.B. Moseley. 2019. A mechanism for how Cdr1/Nim1 kinase promotes mitotic entry by inhibiting Wee1. Mol. Biol. Cell. 30:3015–3023. https://doi.org/10.1091/mbc.E19-08-0430 | |
| dc.relation | Pan, K.Z., T.E. Saunders, I. Flor-Parra, M. Howard, and F. Chang. 2014. Cortical regulation of cell size by a sizer cdr2p. eLife. 3:e02040. https:// doi.org/10.7554/eLife.02040 | |
| dc.relation | Parker, L.L., S.A. Walter, P.G. Young, and H. Piwnica-Worms. 1993. Phos phorylation and inactivation of the mitotic inhibitor Wee1 by the nim1/ cdr1 kinase. Nature. 363:736–738. https://doi.org/10.1038/363736a0 | |
| dc.relation | Patterson, J.O., P. Rees, and P. Nurse. 2019. Noisy Cell-Size-Correlated Ex pression of Cyclin B Drives Probabilistic Cell-Size Homeostasis in Fis sion Yeast. Curr. Biol. 29:1379–1386.e4. https://doi.org/10.1016/j.cub .2019.03.011 | |
| dc.relation | Rincon, S.A., P. Bhatia, C. Bicho, M. Guzman-Vendrell, V. Fraisier, W.E. Borek, F.L. Alves, F. Dingli, D. Loew, J. Rappsilber, et al. 2014. Pom1 regulates the assembly of Cdr2-Mid1 cortical nodes for robust spatial control of cytokinesis. J. Cell Biol. 206:61–77. https://doi.org/10.1083/jcb .201311097 | |
| dc.relation | Roguev, A., M. Wiren, J.S. Weissman, and N.J. Krogan. 2007. High throughput genetic interaction mapping in the fission yeast Schiz osaccharomyces pombe. Nat. Methods. 4:861–866. https://doi.org/10 .1038/nmeth1098 | |
| dc.relation | Roguev, A., S. Bandyopadhyay, M. Zofall, K. Zhang, T. Fischer, S.R. Collins, H. Qu, M. Shales, H.-O. Park, J. Hayles, et al. 2008. Conservation and re wiring of functional modules revealed by an epistasis map in fission yeast. Science. 322:405–410. https://doi.org/10.1126/science.1162609 | |
| dc.relation | Rupes, I. 2002. Checking cell size in yeast. Trends Genet. 18:479–485. https:// doi.org/10.1016/S0168-9525(02)02745-2 | |
| dc.relation | Russell, P., and P. Nurse. 1987a. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell. 49:559–567. https://doi .org/10.1016/0092-8674(87)90458-2 | |
| dc.relation | Russell, P., and P. Nurse. 1987b. The mitotic inducer nim1+ functions in a regulatory network of protein kinase homologs controlling the initia tion of mitosis. Cell. 49:569–576. https://doi.org/10.1016/0092-8674(87) 90459-4 | |
| dc.relation | Schweitzer, J.K., A.E. Sedgwick, and C. D’Souza-Schorey. 2011. ARF6- mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin. Cell Dev. Biol. 22:39–47. https://doi.org/10 .1016/j.semcdb.2010.09.002 | |
| dc.relation | Villar-Tajadura, M.A., P.M. Coll, M. Madrid, J. Cansado, B. Santos, and P. Perez. 2008. Rga2 is a Rho2 GAP that regulates morphogenesis and cell ´ integrity in S. pombe. Mol. Microbiol. 70:867–881. https://doi.org/10 .1111/j.1365-2958.2008.06447.x | |
| dc.relation | Wood, E., and P. Nurse. 2015. Sizing up to divide: mitotic cell-size control in fission yeast. Annu. Rev. Cell Dev. Biol. 31:11–29. https://doi.org/10.1146/ annurev-cellbio-100814-125601 | |
| dc.relation | Wu, L., and P. Russell. 1993. Nim1 kinase promotes mitosis by inactivating Wee1 tyrosine kinase. Nature. 363:738–741. https://doi.org/10.1038/363738a0 | |
| dc.relation | Young, P.G., and P.A. Fantes. 1987. Schizosaccharomyces pombe mutants affected in their division response to starvation. J. Cell Sci. 88:295–304. https://doi.org/10.1242/jcs.88.3.295 | |
| dc.rights | Attribution-ShareAlike 4.0 International | |
| dc.rights | http://creativecommons.org/licenses/by-sa/4.0/ | |
| dc.source | Journal of Cell Biology; Vol. 221, Núm. 2 (2021):Journal of Cell Biology;p. 1 -16. | |
| dc.subject | Investigación agropecuaria - A50 | |
| dc.subject | Genética molecular | |
| dc.subject | Ciclo celular | |
| dc.subject | División celular | |
| dc.subject | Procesos biológicos | |
| dc.subject | Transversal | |
| dc.subject | http://aims.fao.org/aos/agrovoc/c_27577 | |
| dc.subject | http://aims.fao.org/aos/agrovoc/c_37218 | |
| dc.subject | http://aims.fao.org/aos/agrovoc/c_1413 | |
| dc.subject | http://aims.fao.org/aos/agrovoc/c_330999 | |
| dc.thumbnail | https://repository.agrosavia.co/bitstreams/8394ab20-57b8-4370-a653-e21440ec643b/download | |
| dc.title | Arf6 anchors Cdr2 nodes at the cell cortex to control cell size at division | |
| dc.title | Arf6 anchors Cdr2 nodes at the cell cortex to control cell size at division | |
| dc.type | Artículo científico |
