A survey of the specificity and mechanism of 1,6 hexanediol-induced disruption of nuclear transport

References

• Dultz E, Wojtynek M, Medalia O, et al. The nuclear pore complex: birth, life, and death of a cellular behemoth. Cells. 2022;11(9):1–17. doi: 10.3390/cells11091456.
   Web of Science ®Google Scholar
• Javier F-M, Rout MP. One ring to rule them all? Structural and functional diversity in the nuclear pore complex. Trends Biochem Sci. 2021;46(7):595–607. doi: 10.1016/j.tibs.2021.01.003
   PubMed Web of Science ®Google Scholar
• Hampoelz B, Andres-Pons A, Kastritis P, et al. Structure and assembly of the nuclear pore complex. Annu Rev Biophys. 2019;48:515–536. doi: 10.1146/annurev-biophys-052118-115308
   PubMed Web of Science ®Google Scholar
• Wing CE, Yee Joyce Fung H, Min Chook Y. Karyopherin-mediated nucleocytoplasmic transport. Nat Rev Mol Cell Biol. 2022;23(5):307–328. doi: 10.1038/s41580-021-00446-7
   PubMed Web of Science ®Google Scholar
• Bayliss R, Littlewood T, Stewart M. Structural Basis for the Interaction between FxFG nucleoporin repeats and importin-β in nuclear trafficking. Cell. 2000;102(1):99–108. doi: 10.1016/S0092-8674(00)00014-3.
   PubMed Web of Science ®Google Scholar
• Giulia P, Caria J, Lemke EA. Cargo Transport through the Nuclear Pore Complex at a Glance. J Cell Sci. 2021 2;134. doi: 10.1242/jcs.247874
   Web of Science ®Google Scholar
• Kapinos LE, Schoch RL, Wagner RS, et al. Karyopherin-centric control of nuclear pores based on molecular occupancy and kinetic analysis of multivalent binding with FG Nucleoporins. Biophys J. 2014;106(8):1751–1762. doi: 10.1016/j.bpj.2014.02.021
   PubMed Web of Science ®Google Scholar
• Lowe AR, Tang JH, Yassif J, et al. Importin-β modulates the permeability of the nuclear pore complex in a ran-dependent manner. Elife. 2015;2015(4):1–24. doi: 10.7554/eLife.04052.
   Google Scholar
• Kim SJ, Fernandez-Martinez J, Nudelman I, et al. Integrative structure and functional anatomy of a nuclear pore complex. Nature. 2018;555(7697):475–482. doi: 10.1038/nature26003
   PubMed Web of Science ®Google Scholar
• Rajdeep C, Sau A, Musser SM. Super-resolved 3D tracking of cargo transport through nuclear pore complexes. Nat Cell Biol. 2022;24(1):112–122. doi: 10.1038/s41556-021-00815-6
   PubMed Web of Science ®Google Scholar
• Mattheyses AL, Kampmann M, Atkinson CE, et al. Fluorescence anisotropy reveals order and disorder of protein domains in the nuclear pore complex. Biophys J. 2010;99(6):1706–1717. doi: 10.1016/j.bpj.2010.06.075
   PubMed Web of Science ®Google Scholar
• Schnell SJ, Tingey M, Yang W. Speed microscopy: high-speed single molecule tracking and mapping of nucleocytoplasmic transport. Methods Mol Biol. 2022;2502:353–371. doi: 10.1007/978-1-0716-2337-4_23
   PubMedGoogle Scholar
• Yu M, Heidari M, Mikhaleva S, et al. Visualizing the disordered nuclear transport machinery in situ. Nature. 2023;617(7959):162–169. 10.1038/s41586-023-05990-0
   PubMed Web of Science ®Google Scholar
• Yusuke S, Mazur A, Kapinos LE, et al. Spatiotemporal dynamics of the nuclear pore complex transport barrier resolved by high-speed atomic force microscopy. Nature Nanotechnol. 2016;11(8):719–723. doi: 10.1038/nnano.2016.62
   PubMed Web of Science ®Google Scholar
• Fisher PDE, Shen Q, Akpinar B, et al. A programmable DNA origami platform for organizing intrinsically disordered nucleoporins within nanopore confinement. ACS Nano. 2018;12(2):1508–1518. doi: 10.1021/acsnano.7b08044
   PubMed Web of Science ®Google Scholar
• Tijana J-T, Tetenbaum-Novatt J, Sophia McKenney A, et al. Artificial nanopores that mimic the transport selectivity of the nuclear pore complex. Nature. 2009;457(7232):1023–1027. doi: 10.1038/nature07600
   PubMed Web of Science ®Google Scholar
• Kowalczyk SW, Kapinos L, Blosser TR, et al. Single-molecule transport across an individual biomimetic nuclear pore complex. Nature Nanotechnol. 2011;6(7):433–438. doi: 10.1038/nnano.2011.88
   PubMed Web of Science ®Google Scholar
• Ader C, Frey S, Maas W, et al. Amyloid-like Interactions within Nucleoporin FG Hydrogels. Proc Natl Acad Sci USA. 2010;107(14):6281–6285. doi: 10.1073/pnas.0910163107
   PubMed Web of Science ®Google Scholar
• Giorgia C, Paci G, Caria J, et al. The liquid state of FG-Nucleoporins mimics permeability barrier properties of nuclear pore complexes. J Cell Bio. 2020 1;219. doi: 10.1083/jcb.201907157
   Web of Science ®Google Scholar
• Steffen F, Richter RP, Görlich D. FG-Rich Repeats of Nuclear Pore Proteins Form a Three-Dimensional Meshwork with Hydrogel-like Properties. Science. 2006;314(5800):815–817. doi: 10.1126/science.1132516
   PubMed Web of Science ®Google Scholar
• Hayama R, Sparks S, Hecht LM, et al. Thermodynamic characterization of the multivalent interactions underlying rapid and selective translocation through the nuclear pore complex. J Biol Chem. 2018;293(12):4555–4563. doi: 10.1074/jbc.AC117.001649
   PubMed Web of Science ®Google Scholar
• Sparks S, Temel DB, Rout MP, et al. Deciphering thE ‘fuzzy’ interaction of FG nucleoporins and transport factors using small-angle neutron scattering. Structure. 2018;26(3):477–484.e4. doi: 10.1016/j.str.2018.01.010
   PubMed Web of Science ®Google Scholar
• Davis LK, Ford IJ, Hoogenboom BW. Crowding-induced phase separation of nuclear transport receptors in FG nucleoporin assemblies. Elife. 2022;11:1–20. doi: 10.7554/eLife.72627
   Web of Science ®Google Scholar
• Ghavami A, Veenhoff LM, Van Der Giessen E, et al. Probing The disordered domain of the nuclear pore complex through coarse-grained molecular dynamics simulations. Biophys J. 2014;107(6):1393–1402. doi: 10.1016/j.bpj.2014.07.060
   PubMed Web of Science ®Google Scholar
• Isgro TA, Schulten K. Association of Nuclear Pore FG-Repeat Domains to NTF2 Import and Export Complexes. J Mol Biol. 2007;366(1):330–345. doi: 10.1016/j.jmb.2006.11.048.
   PubMed Web of Science ®Google Scholar
• Popken P, Ghavami A, Onck PR, et al. Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex. ?Mol Biol Cell. 2015;26(7):1386–1394. doi: 10.1091/mbc.E14-07-1175
   Web of Science ®Google Scholar
• Zheng T, Zilman A. Self-regulation of the nuclear pore complex enables clogging-free crowded transport. PNAS. 2023;120(7). doi: 10.1073/pnas.2212874120
   Web of Science ®Google Scholar
• Hoogenboom BW, Hough LE, Lemke EA, et al. Physics of the nuclear pore complex: theory, modeling and experiment. Phys Rep. 2021;921:1–53. doi: 10.1016/j.physrep.2021.03.003
   PubMedGoogle Scholar
• Huang K, Szleifer I. Modeling the nucleoporins that form the hairy pores. Biochem Soc Trans. 2020;48(4):1447–1461. doi: 10.1042/BST20190941.
   PubMed Web of Science ®Google Scholar
• Fragasso A, de Vries HW, Andersson J, et al. Transport receptor occupancy in nuclear pore complex mimics. Nano Res. 2022;15(11):9689–9703. doi: 10.1007/s12274-022-4647-1
   Web of Science ®Google Scholar
• Kalita J, Kapinos LE, Zheng T, et al. Karyopherin enrichment and compensation fortifies the nuclear pore complex against nucleocytoplasmic leakage. J Cell Bio. 2022 3;221. doi: 10.1083/jcb.202108107
   PubMed Web of Science ®Google Scholar
• Kapinos LE, Huang B, Rencurel C, et al. Karyopherins regulate nuclear pore complex barrier and transport function. J Cell Bio. 2017;216(11):3609–3624. doi: 10.1083/jcb.201702092
   PubMed Web of Science ®Google Scholar
• Ribbeck K, Görlich D. The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. Embo J. 2002;21(11):2664–2671. doi: 10.1093/emboj/21.11.2664
   PubMed Web of Science ®Google Scholar
• Nataliya S, Goldfarb DS. Binding dynamics of structural nucleoporins govern nuclear pore complex permeability and may mediate channel gating. Mol Cell Biol. 2003;23(2):534–542. doi: 10.1128/mcb.23.2.534-542.2003
   PubMed Web of Science ®Google Scholar
• Patel SS, Belmont BJ, Sante JM, et al. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell. 2007;129(1):83–96. doi: 10.1016/j.cell.2007.01.044
   PubMed Web of Science ®Google Scholar
• Schmidt HBR, Görlich D. Nup98 FG domains from diverse species spontaneously phase-separate into particles with nuclear pore-like permselectivity. Elife. 2015;4:1–30. doi: 10.7554/eLife.04251
   Web of Science ®Google Scholar
• Jäggi RD, Franco-Obregón A, Mühlhäusser P, et al. Modulation of Nuclear Pore Topology by Transport Modifiers. Biophys J. 2003;84(1):665–670. doi: 10.1016/S0006-3495(03)74886-3
   PubMed Web of Science ®Google Scholar
• Onischenko E, Tang JH, Andersen KR, et al. Natively Unfolded FG repeats stabilize the structure of the nuclear pore complex. Cell. 2017;171(4):904–917.e19. doi: 10.1016/j.cell.2017.09.033
   PubMed Web of Science ®Google Scholar
• Kroschwald S, Maharana S, Simon A. Hexanediol: a chemical probe to investigate the material properties of membrane-less compartments. Matters. 2017;1–7. doi: 10.19185/matters.201702000010
   Google Scholar
• Molliex A, Temirov J, Lee J, et al. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell. 2015;163(1):123–133. doi: 10.1016/j.cell.2015.09.015
   PubMed Web of Science ®Google Scholar
• Shi KY, Mori E, Nizami ZF, et al. Toxic PRn Poly-dipeptides encoded by the C9orf72 repeat expansion block nuclear import and export. Proc Natl Acad Sci USA. 2017;114(7):E1111–17. doi: 10.1073/pnas.1620293114
   PubMed Web of Science ®Google Scholar
• Lin Y, Mori E, Kato M, et al. Toxic PR Poly-Dipeptides Encoded by the C9orf72 repeat expansion target LC domain polymers. Cell. 2016;167(3):789–802.e12. doi: 10.1016/j.cell.2016.10.003
   PubMed Web of Science ®Google Scholar
• Van Lindt J, Lazar T, Pakravan D, et al. F/YGG-Motif is an intrinsically disordered nucleic-acid binding motif. RNA Biol. 2022;19(1):622–635. doi: 10.1080/15476286.2022.2066336.
   PubMed Web of Science ®Google Scholar
• Wheeler JR, Matheny T, Jain S, et al. Distinct stages in stress granule assembly and disassembly. Elife. 2016;5(Se):1–25. doi: 10.7554/eLife.18413.
   Google Scholar
• Meinema AC, Poolman B, Veenhoff LM. Quantitative analysis of membrane protein transport across the nuclear pore complex. Traffic. 2013;14(5):487–501. doi: 10.1111/tra.12048.
   PubMed Web of Science ®Google Scholar
• Timney BL, Tetenbaum-Novatt J, Agate DS, et al. Simple kinetic relationships and nonspecific competition govern nuclear import rates in vivo. J Cell Bio. 2006;175(4):579–593. doi: 10.1083/jcb.200608141
   PubMed Web of Science ®Google Scholar
• Timney BL, Raveh B, Mironska R, et al. Simple rules for passive diffusion through the nuclear pore complex. J Cell Bio. 2016;215(1):57–76. doi: 10.1083/jcb.201601004
   PubMed Web of Science ®Google Scholar
• Hiromi I, Huynh Nhat KP, Togawa H, et al. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Nat Acad Sci. 2009;106(37):15651–15656. doi: 10.1073/pnas.0904764106
   PubMed Web of Science ®Google Scholar
• Miesenböck G, De Angelis DA, Rothman JE. Visualizing Secretion and Synaptic Transmission with PH-Sensitive Green Fluorescent Proteins. Nature. 1998;394(July):192–195. https://www.nature.com/articles/BF28190
   PubMedGoogle Scholar
• Mouton SN, Thaller DJ, Crane MM, et al. A Physicochemical Perspective of Aging from Single-Cell Analysis of Ph, Macromolecular and Organellar Crowding in Yeast. Elife. 2020;9:1–42. doi: 10.7554/ELIFE.54707
   Web of Science ®Google Scholar
• Bösl B, Grimminger V, Walter S. The Molecular Chaperone Hsp104-A Molecular Machine for Protein Disaggregation. J Struct Biol. 2006;156(1):139–148. doi: 10.1016/j.jsb.2006.02.004
   PubMed Web of Science ®Google Scholar
• Glover JR, Lindquist S. Hsp104, Hsp70, and Hsp40: A Novel Chaperone System That Rescues Previously Aggregated Proteins. Cell. 1998;94(1):73–82. doi: 10.1016/S0092-8674(00)81223-4.
   PubMed Web of Science ®Google Scholar
• Harari A, Zoltsman G, Levin T, et al. Hsp104 N-Terminal Domain Interaction with Substrates Plays a Regulatory Role in Protein Disaggregation. FEBS J. 2022;289(17):5359–5377. doi: 10.1111/febs.16441
   PubMed Web of Science ®Google Scholar
• Yolanda S, Lindquist SL. HSP104 Required for Induced Thermotolerance. Science. 1990;248(4959):1112–1115. doi: 10.1126/science.2188365
   PubMed Web of Science ®Google Scholar
• Joanna K, Kapinos LE, Lim RYH. On the Asymmetric Partitioning of Nucleocytoplasmic Transport – Recent Insights and Open Questions. J Cell Sci. 2021;134(7). doi: 10.1242/jcs.240382
   Web of Science ®Google Scholar
• Hough LE, Dutta K, Sparks S, et al. The Molecular Mechanism of Nuclear Transport Revealed by Atomic-Scale Measurements. Elife. 2015;4(September):1–23. doi: 10.7554/eLife.10027.
   Google Scholar
• Milles S, Mercadante D, Valle Aramburu I, et al. Plasticity of an Ultrafast Interaction between Nucleoporins and Nuclear Transport Receptors. Cell. 2015;163(3):734–745. doi: 10.1016/j.cell.2015.09.047
   PubMed Web of Science ®Google Scholar
• Thaller DJ, Tong D, Marklew CJ, et al. Direct Binding of ESCRT Protein Chm7 to phosphatidic acid-rich membranes at nuclear envelope herniations. J Cell Bio. 2021 3;220. doi: 10.1083/JCB.202004222
   Web of Science ®Google Scholar
• Thaller DJ, Allegretti M, Borah S, et al. An escrt-lem protein surveillance system is poised to directly monitor the nuclear envelope and nuclear transport system. Elife. 2019;8:1–36. doi: 10.7554/eLife.45284
   Web of Science ®Google Scholar
• Webster BM, Thaller DJ, Jäger J, et al. Chm7 and Heh1 collaborate to link nuclear pore complex quality control with nuclear envelope sealing. Embo J. 2016;35(22):2447–2467. doi: 10.15252/embj.201694574
   PubMed Web of Science ®Google Scholar
• Semmelink MFW, Jafarinia H, Wolters JC, et al. 2022. “Nuclear Transport under Stress Phenocopies Transport Defects in Models of C9Orf72 ALS,” 1–38. bioRxiv 2022.04.13.488135; doi: 10.1101/2022.04.13.488135
   Google Scholar
• Rempel IL, Crane MM, Thaller DJ, et al. Age-dependent deterioration of nuclear pore assembly in mitotic cells decreases transport dynamics. Elife. 2019;8(June):1–26. doi: 10.7554/eLife.48186
   Google Scholar
• Huh WK, Falvo JV, Gerke LC, et al. Global analysis of protein localization in budding yeast. Nature. 2003;425(6959):686–691. http://yeastgfp.ucsf.edu.
   PubMed Web of Science ®Google Scholar
• Janke C, Magiera MM, Rathfelder N, et al. A Versatile Toolbox for PCR-Based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 2004;21(11):947–962. doi: 10.1002/yea.1142
   PubMed Web of Science ®Google Scholar
• Kuiper EFE, Gallardo P, Bergsma T, et al. The chaperone DNAJB6 Surveils FG-Nucleoporins and is required for interphase nuclear pore complex biogenesis. Nat Cell Biol. 2022;24(11):1584–1594. doi: 10.1038/s41556-022-01010-x
   PubMed Web of Science ®Google Scholar
• Springhower CE, Rosen MK, Min Chook Y. Karyopherins and Condensates. Curr Opinion Cell Biol. 2020;64:112–123. doi: 10.1016/j.ceb.2020.04.003
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nature Methods. 2012;9(7):676–682. doi: 10.1038/nmeth.2019
   PubMed Web of Science ®Google Scholar