A phosphorylation-controlled switch confers cell cycle-dependent protein relocalization.
Journal
Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575
Informations de publication
Date de publication:
29 Aug 2024
29 Aug 2024
Historique:
received:
29
06
2023
accepted:
31
07
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
29
8
2024
Statut:
aheadofprint
Résumé
Tools for acute manipulation of protein localization enable elucidation of spatiotemporally defined functions, but their reliance on exogenous triggers can interfere with cell physiology. This limitation is particularly apparent for studying mitosis, whose highly choreographed events are sensitive to perturbations. Here we exploit the serendipitous discovery of a phosphorylation-controlled, cell cycle-dependent localization change of the adaptor protein PLEKHA5 to develop a system for mitosis-specific protein recruitment to the plasma membrane that requires no exogenous stimulus. Mitosis-enabled anchor-away/recruiter system comprises an engineered, 15 kDa module derived from PLEKHA5 capable of recruiting functional protein cargoes to the plasma membrane during mitosis, either through direct fusion or via GFP-GFP nanobody interaction. Applications of the mitosis-enabled anchor-away/recruiter system include both knock sideways to rapidly extract proteins from their native localizations during mitosis and conditional recruitment of lipid-metabolizing enzymes for mitosis-selective editing of plasma membrane lipid content, without the need for exogenous triggers or perturbative synchronization methods.
Identifiants
pubmed: 39209962
doi: 10.1038/s41556-024-01495-8
pii: 10.1038/s41556-024-01495-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R01GM143367
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : T32GM138826
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R35GM141159
Organisme : Alfred P. Sloan Foundation
ID : Sloan Research Fellowship
Organisme : U.S. Department of Defense (United States Department of Defense)
ID : DURIP GRANT13710486
Organisme : U.S. Department of Defense (United States Department of Defense)
ID : DURIP GRANT13369767
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Grecco, H. E., Schmick, M. & Bastiaens, P. I. H. Signaling from the living plasma membrane. Cell 144, 897–909 (2011).
pubmed: 21414482
doi: 10.1016/j.cell.2011.01.029
Sunshine, H. & Iruela-Arispe, M. L. Membrane lipids and cell signaling. Curr. Opin. Lipidol. 28, 408–413 (2017).
pubmed: 28692598
pmcid: 5776726
doi: 10.1097/MOL.0000000000000443
Fegan, A., White, B., Carlson, J. C. T. & Wagner, C. R. Chemically controlled protein assembly: techniques and applications. Chem. Rev. 110, 3315–3336 (2010).
pubmed: 20353181
doi: 10.1021/cr8002888
Suzuki, S. et al. A chemogenetic platform for controlling plasma membrane signaling and synthetic signal oscillation. Cell Chem. Biol. 29, 1446–1464.e10 (2022).
pubmed: 35835118
doi: 10.1016/j.chembiol.2022.06.005
Kennedy, M. J. et al. Rapid blue-light–mediated induction of protein interactions in living cells. Nat. Methods 7, 973–975 (2010).
pubmed: 21037589
pmcid: 3059133
doi: 10.1038/nmeth.1524
Hannanta-Anan, P., Glantz, S. T. & Chow, B. Y. Optically inducible membrane recruitment and signaling systems. Curr. Opin. Struct. Biol. 57, 84–92 (2019).
pubmed: 30884362
pmcid: 6697567
doi: 10.1016/j.sbi.2019.01.017
Lin, Y. C. et al. Rapidly reversible manipulation of molecular activity with dual chemical dimerizers. Angew. Chem. Int. Ed. 52, 6450–6454 (2013).
doi: 10.1002/anie.201301219
Voß, S., Klewer, L. & Wu, Y. W. Chemically induced dimerization: reversible and spatiotemporal control of protein function in cells. Curr. Opin. Chem. Biol. 28, 194–201 (2015).
pubmed: 26431673
doi: 10.1016/j.cbpa.2015.09.003
Hu, J., Adebali, O., Adar, S. & Sancar, A. Dynamic maps of UV damage formation and repair for the human genome. Proc. Natl Acad. Sci. USA 114, 6758–6763 (2017).
pubmed: 28607063
pmcid: 5495279
doi: 10.1073/pnas.1706522114
Benman, W. et al. Temperature-responsive optogenetic probes of cell signaling. Nat. Chem. Biol. 18, 152–160 (2021).
pubmed: 34937907
pmcid: 9252025
doi: 10.1038/s41589-021-00917-0
Morgan, D. O. The Cell Cycle: Principles of Control (New Science Press Ltd, 2006).
McLean, J. R., Chaix, D., Ohi, M. D. & Gould, K. L. State of the APC/C: organization, function, and structure. Crit. Rev. Biochem. Mol. Biol. 46, 118–136 (2011).
pubmed: 21261459
pmcid: 4856037
doi: 10.3109/10409238.2010.541420
Pomerening, J. R., Sun, Y. K. & Ferrell, J. E. Systems-level dissection of the cell-cycle oscillator: bypassing positive feedback produces damped oscillations. Cell 122, 565–578 (2005).
pubmed: 16122424
doi: 10.1016/j.cell.2005.06.016
Sakaue-Sawano, A. et al. Genetically encoded tools for optical dissection of the mammalian cell cycle. Mol. Cell 68, 626–640.e5 (2017).
pubmed: 29107535
doi: 10.1016/j.molcel.2017.10.001
Bajar, B. T. et al. Fluorescent indicators for simultaneous reporting of all four cell cycle phases. Nat. Methods 13, 993–996 (2016).
pubmed: 27798610
pmcid: 5548384
doi: 10.1038/nmeth.4045
Sakaue-Sawano, A. et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487–498 (2008).
pubmed: 18267078
doi: 10.1016/j.cell.2007.12.033
Cao, X., Shami Shah, A., Sanford, E. J., Smolka, M. B. & Baskin, J. M. Proximity labeling reveals spatial regulation of the anaphase-promoting complex/cyclosome by a microtubule adaptor. ACS Chem. Biol. 17, 2605–2618 (2022).
pubmed: 35952650
pmcid: 9933862
doi: 10.1021/acschembio.2c00527
Sluysmans, S. et al. PLEKHA5, PLEKHA6, and PLEKHA7 bind to PDZD11 to target the Menkes ATPase ATP7A to the cell periphery and regulate copper homeostasis. Mol. Biol. Cell 32, ar34 (2021).
pubmed: 34613798
pmcid: 8693958
doi: 10.1091/mbc.E21-07-0355
Sluysmans, S., Méan, I., Jond, L. & Citi, S. WW, PH and C-terminal domains cooperate to direct the subcellular localizations of PLEKHA5, PLEKHA6 and PLEKHA7. Front. Cell Dev. Biol. 9, 2522 (2021).
doi: 10.3389/fcell.2021.729444
Shami Shah, A. et al. PLEKHA4/kramer attenuates dishevelled ubiquitination to modulate wnt and planar cell polarity signaling. Cell Rep. 27, 2157–2170.e8 (2019).
pubmed: 31091453
doi: 10.1016/j.celrep.2019.04.060
Branon, T. C. et al. Efficient proximity labeling in living cells and organisms with TurboID. Nat. Biotechnol. 36, 880–887 (2018).
pubmed: 30125270
pmcid: 6126969
doi: 10.1038/nbt.4201
Kubala, M. H., Kovtun, O., Alexandrov, K. & Collins, B. M. Structural and thermodynamic analysis of the GFP:GFP–nanobody complex. Protein Sci. 19, 2389–2401 (2010).
pubmed: 20945358
pmcid: 3009406
doi: 10.1002/pro.519
Atilla-Gokcumen, G. E. et al. Dividing cells regulate their lipid composition and localization. Cell 156, 428 (2014).
pubmed: 24462247
pmcid: 3909459
doi: 10.1016/j.cell.2013.12.015
Li, J. et al. Grp1 plays a key role in linking insulin signaling to Glut4 recycling. Dev. Cell 22, 1286–1298 (2012).
pubmed: 22609160
pmcid: 3376201
doi: 10.1016/j.devcel.2012.03.004
Cho, E. A. et al. Phosphorylation of RIAM by src promotes integrin activation by unmasking the PH domain of RIAM. Structure 29, 320–329.e4 (2021).
pubmed: 33275877
doi: 10.1016/j.str.2020.11.011
Hornbeck, P. V. et al. PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 43, D512–D520 (2015).
pubmed: 25514926
doi: 10.1093/nar/gku1267
Kinoshita, E. & Kinoshita-Kikuta, E. Improved Phos-tag SDS–PAGE under neutral pH conditions for advanced protein phosphorylation profiling. Proteomics 11, 319–323 (2011).
pubmed: 21204258
doi: 10.1002/pmic.201000472
Johnson, J. L. et al. An atlas of substrate specificities for the human serine/threonine kinome. Nature 613, 759–766 (2023).
pubmed: 36631611
pmcid: 9876800
doi: 10.1038/s41586-022-05575-3
Bumpus, T. W. & Baskin, J. M. Clickable substrate mimics enable imaging of phospholipase d activity. ACS Cent. Sci. 3, 1070–1077 (2017).
pubmed: 29104923
pmcid: 5658752
doi: 10.1021/acscentsci.7b00222
Hardman, C. et al. Synthesis and evaluation of designed PKC modulators for enhanced cancer immunotherapy. Nat. Commun. 11, 1–11 (2020).
doi: 10.1038/s41467-020-15742-7
Gschwendt, M. et al. Inhibition of protein kinase C μ by various inhibitors. Inhibition from protein kinase c isoenzymes. FEBS Lett. 392, 77–80 (1996).
pubmed: 8772178
doi: 10.1016/0014-5793(96)00785-5
Young, L. H., Balin, B. J. & Weis, M. T. Gö 6983: a fast acting protein kinase C inhibitor that attenuates myocardial ischemia/reperfusion injury. Cardiovasc. Drug Rev. 23, 255–272 (2005).
pubmed: 16252018
doi: 10.1111/j.1527-3466.2005.tb00170.x
Evenou, J. P. et al. The potent protein kinase c-selective inhibitor AEB071 (Sotrastaurin) represents a new class of immunosuppressive agents affecting early T-cell activation. J. Pharmacol. Exp. Ther. 330, 792–801 (2009).
pubmed: 19491325
doi: 10.1124/jpet.109.153205
Bibian, M. et al. Development of highly selective casein kinase 1δ/1ε (CK1δ/ε) inhibitors with potent antiproliferative properties. Bioorg. Med. Chem. Lett. 23, 4374 (2013).
pubmed: 23787102
pmcid: 3783656
doi: 10.1016/j.bmcl.2013.05.075
Bernatík, O. et al. Functional analysis of dishevelled-3 phosphorylation identifies distinct mechanisms driven by casein kinase 1ε and Frizzled5. J. Biol. Chem. 289, 23520–23533 (2014).
pubmed: 24993822
pmcid: 4156093
doi: 10.1074/jbc.M114.590638
Meng, Q. J. et al. Entrainment of disrupted circadian behavior through inhibition of casein kinase 1 (CK1) enzymes. Proc. Natl Acad. Sci. USA 107, 15240–15245 (2010).
pubmed: 20696890
pmcid: 2930590
doi: 10.1073/pnas.1005101107
Rena, G., Bain, J., Elliott, M. & Cohen, P. D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Rep. 5, 60–65 (2004).
pubmed: 14710188
doi: 10.1038/sj.embor.7400048
Moura, M. & Conde, C. Phosphatases in mitosis: roles and regulation. Biomolecules 9, 55 (2019).
pubmed: 30736436
pmcid: 6406801
doi: 10.3390/biom9020055
Kastian, R. F. et al. Dephosphorylation of neural wiring protein shootin1 by PP1 phosphatase regulates netrin-1-induced axon guidance. J. Biol. Chem. 299, 104687 (2023).
pubmed: 37044214
pmcid: 10196999
doi: 10.1016/j.jbc.2023.104687
Swingle, M., Ni, L. & Honkanen, R. E. Small-molecule inhibitors of Ser/Thr protein phosphatases. Methods Mol. Biol. 365, 23–38 (2007).
pubmed: 17200551
pmcid: 2709456
Bastan, R., Eskandari, N., Ardakani, H. J. & Peachell, P. T. Effects of fostriecin on β2-adrenoceptor-driven responses in human mast cells. J. Immunotoxicol. 14, 60–65 (2017).
pubmed: 28090813
doi: 10.1080/1547691X.2016.1259277
McKinley, K. L. & Cheeseman, I. M. Polo-like kinase 1 licenses CENP-a deposition at centromeres. Cell 158, 397–411 (2014).
pubmed: 25036634
pmcid: 4192726
doi: 10.1016/j.cell.2014.06.016
Selvy, P. E., Lavieri, R. R., Lindsley, C. W. & Brown, H. A. Phospholipase D: enzymology, functionality, and chemical modulation. Chem. Rev. 111, 6064–6119 (2011).
pubmed: 21936578
pmcid: 3233269
doi: 10.1021/cr200296t
Tei, R. & Baskin, J. M. Spatiotemporal control of phosphatidic acid signaling with optogenetic, engineered phospholipase Ds. J. Cell Biol. 219, e201907013 (2020).
pubmed: 31999306
pmcid: 7054994
doi: 10.1083/jcb.201907013
Tei, R., Bagde, S. R., Fromme, J. C. & Baskin, J. M. Activity-based directed evolution of a membrane editor in mammalian cells. Nat. Chem. 15, 1030–1039 (2023).
pubmed: 37217787
pmcid: 10525039
doi: 10.1038/s41557-023-01214-0
Balla, T. Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93, 1019–1137 (2013).
pubmed: 23899561
pmcid: 3962547
doi: 10.1152/physrev.00028.2012
Idevall-Hagren, O., Dickson, E. J., Hille, B., Toomre, D. K. & De Camilli, P. Optogenetic control of phosphoinositide metabolism. Proc. Natl Acad. Sci. USA 109, E2316–E2323 (2012).
pubmed: 22847441
pmcid: 3435206
doi: 10.1073/pnas.1211305109
Cauvin, C. & Echard, A. Phosphoinositides: lipids with informative heads and mastermind functions in cell division. Biochim. Biophys. Acta 1851, 832–843 (2015).
pubmed: 25449648
doi: 10.1016/j.bbalip.2014.10.013
Toyoshima, F., Matsumura, S., Morimoto, H., Mitsushima, M. & Nishida, E. PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells. Dev. Cell 13, 796–811 (2007).
pubmed: 18061563
doi: 10.1016/j.devcel.2007.10.014
Kotak, S., Busso, C. & Gönczy, P. NuMA interacts with phosphoinositides and links the mitotic spindle with the plasma membrane. EMBO J. 33, 1815–1830 (2014).
pubmed: 24996901
pmcid: 4195763
doi: 10.15252/embj.201488147
Bordhan, P., Razavi Bazaz, S., Jin, D. & Ebrahimi Warkiani, M. Advances and enabling technologies for phase-specific cell cycle synchronisation. Lab Chip 22, 445–462 (2022).
pubmed: 35076046
doi: 10.1039/D1LC00724F
Fiume, R. et al. Involvement of nuclear PLCβl in lamin B1 phosphorylation and G 2 /M cell cycle progression. FASEB J. 23, 957–966 (2009).
pubmed: 19028838
doi: 10.1096/fj.08-121244
Goss, V. L. et al. Identification of nuclear pII protein kinase C as a mitotic lamin kinase. J. Biol. Chem. 269, 19074–19080 (1994).
pubmed: 8034666
doi: 10.1016/S0021-9258(17)32276-7
Sun, B., Murray, N. R. & Fields, A. P. A role for nuclear phosphatidylinositol-specific phospholipase C in the G2/M phase transition. J. Biol. Chem. 272, 26313–26317 (1997).
pubmed: 9334202
doi: 10.1074/jbc.272.42.26313
Lim, S. et al. BioPROTACs as versatile modulators of intracellular therapeutic targets including proliferating cell nuclear antigen (PCNA). Proc. Natl Acad. Sci. USA 117, 5791–5800 (2020).
pubmed: 32123106
pmcid: 7084165
doi: 10.1073/pnas.1920251117
Ludwicki, M. B. et al. Broad-spectrum proteome editing with an engineered bacterial ubiquitin ligase mimic. ACS Cent. Sci. 5, 852–866 (2019).
pubmed: 31139721
pmcid: 6535771
doi: 10.1021/acscentsci.9b00127
Siriwardena, S. U. et al. Phosphorylation-inducing chimeric small molecules. J. Am. Chem. Soc. 142, 14052–14057 (2020).
pubmed: 32787262
doi: 10.1021/jacs.0c05537
Chen, P. H. et al. Modulation of phosphoprotein activity by phosphorylation targeting chimeras (PhosTACs). ACS Chem. Biol. 16, 2808–2815 (2021).
pubmed: 34780684
pmcid: 10437008
doi: 10.1021/acschembio.1c00693
Ramirez, D. H. et al. Engineering a proximity-directed O-GlcNAc transferase for selective protein O-GlcNAcylation in cells. ACS Chem. Biol. 15, 1059–1066 (2020).
pubmed: 32119511
pmcid: 7296736
doi: 10.1021/acschembio.0c00074
Ge, Y. et al. Target protein deglycosylation in living cells by a nanobody-fused split O-GlcNAcase. Nat. Chem. Biol. 17, 593–600 (2021).
pubmed: 33686291
pmcid: 8085020
doi: 10.1038/s41589-021-00757-y
Wang, W. et al. A light- and calcium-gated transcription factor for imaging and manipulating activated neurons. Nat. Biotechnol. 35, 864–871 (2017).
pubmed: 28650461
pmcid: 5595644
doi: 10.1038/nbt.3909
Barnea, G. et al. The genetic design of signaling cascades to record receptor activation. Proc. Natl Acad. Sci. USA 105, 64–69 (2008).
pubmed: 18165312
doi: 10.1073/pnas.0710487105
Kim, M. W. et al. Time-gated detection of protein-protein interactions with transcriptional readout. eLife 6, e30233 (2017).
pubmed: 29189201
pmcid: 5708895
doi: 10.7554/eLife.30233
Gao, X. J., Chong, L. S., Kim, M. S. & Elowitz, M. B. Programmable protein circuits in living cells. Science 361, 1252–1258 (2018).
pubmed: 30237357
pmcid: 7176481
doi: 10.1126/science.aat5062
Fink, T. et al. Design of fast proteolysis-based signaling and logic circuits in mammalian cells. Nat. Chem. Biol. 15, 115–122 (2018).
pubmed: 30531965
pmcid: 7069760
doi: 10.1038/s41589-018-0181-6
Yuan, J. et al. Multi-responsive self-healing metallo-supramolecular gels based on ‘click’ ligand. J. Mater. Chem. 22, 11515–11522 (2012).
doi: 10.1039/c2jm31347b
Alamudi, S. H. et al. Development of background-free tame fluorescent probes for intracellular live cell imaging. Nat. Commun. 7, 1–9 (2016).
doi: 10.1038/ncomms11964
Shami Shah, A., Cao, X., White, A. C. & Baskin, J. M. PLEKHA4 promotes Wnt/b-catenin signaling-mediated G 1-S transition and proliferation in melanoma. Cancer Res. 81, 2029–2043 (2021).
pubmed: 33574086
pmcid: 8137570
doi: 10.1158/0008-5472.CAN-20-2584
Cao, X. & Baskin, J. M. Applying the mitosis-enabled anchor-away/recruiter system (MARS) for conditional protein recruitment to the plasma membrane during mitosis. https://doi.org/10.17504/protocols.io.n2bvjnzypgk5/v1 (2024).
McIntire, L. B. J. et al. Reduction of synaptojanin 1 ameliorates synaptic and behavioral impairments in a mouse model of alzheimer’s disease. J. Neurosci. 32, 15271–15276 (2012).
pubmed: 23115165
pmcid: 3711720
doi: 10.1523/JNEUROSCI.2034-12.2012
Nasuhoglu, C. et al. Nonradioactive analysis of phosphatidylinositides and other anionic phospholipids by anion-exchange high-performance liquid chromatography with suppressed conductivity detection. Anal. Biochem. 301, 243–254 (2002).
pubmed: 11814295
doi: 10.1006/abio.2001.5489
Deutsch, E. W. et al. Trans-proteomic pipeline: robust mass spectrometry-based proteomics data analysis suite. J. Proteome Res. 22, 615–624 (2023).
pubmed: 36648445
pmcid: 10166710
doi: 10.1021/acs.jproteome.2c00624
Eng, J. K., Jahan, T. A. & Hoopmann, M. R. Comet: an open-source MS/MS sequence database search tool. Proteomics 13, 22–24 (2013).
pubmed: 23148064
doi: 10.1002/pmic.201200439
Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).
pubmed: 34723319
doi: 10.1093/nar/gkab1038
Nagy, Z., Comer, S. & Smolenski, A. Analysis of protein phosphorylation using phos-tag gels. Curr. Protoc. Protein Sci. 93, e64 (2018).
pubmed: 30044546
doi: 10.1002/cpps.64