Volume 10 Issue 1
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Matthew T. J. Halma, Longfu Xu. Life under tension: the relevance of force on biological polymers. Biophysics Reports, 2024, 10(1): 48-56. doi: 10.52601/bpr.2023.230019
Citation: Matthew T. J. Halma, Longfu Xu. Life under tension: the relevance of force on biological polymers. Biophysics Reports, 2024, 10(1): 48-56. doi: 10.52601/bpr.2023.230019

Life under tension: the relevance of force on biological polymers

doi: 10.52601/bpr.2023.230019
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  • Corresponding author: m.t.j.halma@vu.nl (M. T. J. Halma)
  • Received Date: 11 October 2023
  • Accepted Date: 06 December 2023
  • Available Online: 26 February 2024
  • Publish Date: 29 February 2024
  • Optical tweezers have elucidated numerous biological processes, particularly by enabling the precise manipulation and measurement of tension. One question concerns the biological relevance of these experiments and the generalizability of these experiments to wider biological systems. Here, we categorize the applicability of the information garnered from optical tweezers in two distinct categories: the direct relevance of tension in biological systems, and what experiments under tension can tell us about biological systems, while these systems do not reach the same tension as the experiment, still, these artificial experimental systems reveal insights into the operations of biological machines and life processes.

  • Matthew Halma is employed by Lumicks B.V., a manufacturer of optical tweezers instruments. Longfu Xu declares that he has no conflict of interest.
    This article does not contain any studies with human or animal subjects performed by any of the authors.
    Matthew T.J. Halma and Longfu Xu contributed equally to this work.

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  • Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, Arellano-Santoyo H, Gonen T, Ranish JA, Asbury CL, Biggins S (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468: 576−579 doi: 10.1038/nature09594
    Bao C, Zhu M, Nykonchuk I, Wakabayashi H, Mathews DH, Ermolenko DN (2022) Specific length and structure rather than high thermodynamic stability enable regulatory mRNA stem-loops to pause translation. Nat Commun 13(1): 988. https://doi.org/10.1038/s41467-022-28600-5
    Bergamaschi G, Biebricher A, Wuite GJ (2019) From nuclei to artificial cells: probing the mechanics of minimal systems. Biophys J 116: 123a. https://doi.org/10.1016/j.bpj.2018.11.687
    Biebricher AS, Heller I, Roijmans RFH, Hoekstra TP, Peterman EJG, Wuite GJL (2015) The impact of DNA intercalators on DNA and DNA-processing enzymes elucidated through force-dependent binding kinetics. Nat Commun 6: 7304. https://doi.org/10.1038/ncomms8304
    Brower-Toland BD, Smith CL, Yeh RC, Lis JT, Peterson CL, Wang MD (2002) Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc Natl Acad Sci USA 99: 1960−1965 doi: 10.1073/pnas.022638399
    Bustamante C, Alexander L, Maciuba K, Kaiser CM (2020) Single-molecule studies of protein folding with optical tweezers. Annu Rev Biochem 89: 443−470 doi: 10.1146/annurev-biochem-013118-111442
    Bustamante C, Chemla YR, Forde NR, Izhaky D (2004) Mechanical processes in biochemistry. Annu Rev Biochem 73: 705−748 doi: 10.1146/annurev.biochem.72.121801.161542
    Chen G, Chang KY, Chou MY, Bustamante C, Tinoco I (2009) Triplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of -1 ribosomal frameshifting. Proc Natl Acad Sci USA 106: 12706−12711 doi: 10.1073/PNAS.0905046106/SUPPL_FILE/0905046106SI.PDF
    Clarke RJ, Högnason K, Brimacombe M, Townes-Anderson E (2008) Cone and rod cells have different target preferences in vitro as revealed by optical tweezers. Mol Vis 14: 706−720
    Cost A-L, Ringer P, Chrostek-Grashoff A, Grashoff C (2015) How to measure molecular forces in cells: a guide to evaluating genetically-encoded FRET-based tension sensors. Cell Mol Bioeng 8: 96−105 doi: 10.1007/s12195-014-0368-1
    Curtis ASG, Seehar GM (1978) The control of cell division by tension or diffusion. Nature 274: 52−53 doi: 10.1038/274052a0
    Dogterom M, Yurke B (1997) Measurement of the force-velocity relation for growing microtubules. Science 278: 856−860 doi: 10.1126/science.278.5339.856
    Forde NR, Izhaky D, Woodcock GR, Wuite GJL, Bustamante C (2002) Using mechanical force to probe the mechanism of pausing and arrest during continuous elongation by Escherichia coli RNA polymerase. Proc Natl Acad Sci USA 99: 11682−11687 doi: 10.1073/pnas.142417799
    Goel A, Astumian RD, Herschbach D (2003) Tuning and switching a DNA polymerase motor with mechanical tension. Proc Natl Acad Sci USA 100: 9699−9704 doi: 10.1073/pnas.1033134100
    Halma MTJ, Ritchie DB, Cappellano TR, Neupane K, Woodside MT (2019) Complex dynamics under tension in a high-efficiency frameshift stimulatory structure. Proc Natl Acad Sci USA 116: 19500−19505 doi: 10.1073/PNAS.1905258116/-/DCSUPPLEMENTAL
    Halma MTJ, Tuszynski JA, Wuite GJL (2022) Optical tweezers for drug discovery. Drug Discov Today 28(1): 103443. https://doi.org/10.1016/j.drudis.2022.103443
    Hamant O, Inoue D, Bouchez D, Dumais J, Mjolsness E (2019) Are microtubules tension sensors? Nat Commun 10: 1–12. https://doi.org/10.1038/s41467-019-10207-y
    Harrington HR, Zimmer MH, Chamness LM, Nash V, Penn WD, Miller TF, Mukhopadhyay S, Schlebach JP (2020) Cotranslational folding stimulates programmed ribosomal frameshifting in the alphavirus structural polyprotein. J Biol Chem 295: 6798−6808 doi: 10.1074/jbc.RA120.012706
    Hoekstra TP, Depken M, Lin SN, Cabanas-Danes J, Gross P, Dame RT, Peterman EJG, Wuite GJL (2017) Switching between exonucleolysis and replication by T7 DNA polymerase ensures high fidelity. Biophys J 112: 575−583 doi: 10.1016/j.bpj.2016.12.044
    Jun Y, Tripathy SK, Narayanareddy BR, Mattson-Hoss MK, Gross SP (2014) Calibration of optical tweezers for in vivo force measurements: how do different approaches compare? Biophys J 107(6): 1474−1484 doi: 10.1016/j.bpj.2014.07.033
    Kaiser CM, Goldman DH, Chodera JD, Tinoco I, Bustamante C (2011) The ribosome modulates nascent protein folding. Science 334: 1723−1727 doi: 10.1126/science.1209740
    Kaiser CM, Tinoco I (2014) Probing the mechanisms of translation with force. Chem Rev 114: 3266−3266 doi: 10.1021/CR400313X
    Keizer VIP, Grosse-Holz S, Woringer M, Zambon L, Aizel K, Bongaerts M, Delille F, Kolar-Znika L, Scolari VF, Hoffmann S, Banigan EJ, Mirny LA, Dahan M, Fachinetti D, Coulon A (2022) Live-cell micromanipulation of a genomic locus reveals interphase chromatin mechanics. Science 377: 489−495 doi: 10.1126/science.abi9810
    Kellermayer MS, Smith SB, Granzier HL, Bustamante C (1997) Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276: 1112−1116 doi: 10.1126/science.276.5315.1112
    Kelly JA, Woodside MT, Dinman JD (2021) Programmed−1 ribosomal frameshifting in coronaviruses: a therapeutic target. Virology 554: 75−82 doi: 10.1016/j.virol.2020.12.010
    King GA, Gross P, Bockelmann U, Modesti M, Wuite GJL Peterman EJG (2013) Revealing the competition between peeled ssDNA, melting bubbles, and S-DNA during DNA overstretching using fluorescence microscopy. Proc Natl Acad Sci USA 110: 3859−3864 doi: 10.1073/pnas.1213676110
    Laan L, Husson J, Munteanu EL, Kerssemakers JWJ, Dogterom M (2008) Force-generation and dynamic instability of microtubule bundles. Proc Natl Acad Sci USA 105: 8920−8925 doi: 10.1073/pnas.0710311105
    Leick MB, Silva H, Scarfò I, Larson R, Choi BD, Bouffard AA, Gallagher K, Schmidts A, Bailey SR, Kann MC, Jan M, Wehrli M, Grauwet K, Horick N, Frigault MJ, Maus MV (2022) Non-cleavable hinge enhances avidity and expansion of CAR-T cells for acute myeloid leukemia. Cancer Cell 40: 494−508.e5 doi: 10.1016/j.ccell.2022.04.001
    Li JH, Lin WX, Zhang B, Nong DG, Ju HP, Ma JB, Xu CH, Ye FF, Xi XG, Li M, Lu Y, Dou SX (2016) Pif1 is a force-regulated helicase. Nucleic Acids Res 44: 4330−4339 doi: 10.1093/NAR/GKW295
    Liu K, Maciuba K, Kaiser CM (2019) The ribosome cooperates with a chaperone to guide multi-domain protein folding. Mol Cell 74: 310−319.e7 doi: 10.1016/j.molcel.2019.01.043
    Luo Y, Chang J, Yang D, Bryan JSI, MacIsaac M, Pressé S, Wong WP (2023) Resolving Molecular Heterogeneity with Single-Molecule Centrifugation. J Am Chem Soc 145: 3276−3282 doi: 10.1021/jacs.2c11450
    Meijering AEC, Sarlós K, Nielsen CF, Witt H, Harju J, Kerklingh E, Haasnoot GH, Bizard AH, Heller I, Broedersz CP, Liu Y, Peterman EJG, Hickson ID, Wuite GJL (2022) Nonlinear mechanics of human mitotic chromosomes. Nature 605(7910): 545−550 doi: 10.1038/s41586-022-04666-5
    Newton MD, Taylor BJ, Driessen RPC, Roos L, Cvetesic N, Allyjaun S, Lenhard B, Cuomo ME, Rueda DS (2019) DNA stretching induces Cas9 off-target activity. Nat Struct Mol Biol 26(3): 185−192 doi: 10.1038/s41594-019-0188-z
    O’Neil NJ, Bailey ML, Hieter P (2017) Synthetic lethality and cancer. Nat Rev Genet 18: 613−623 doi: 10.1038/nrg.2017.47
    Otake M, Ukita Y (2019) Force analysis method of single-molecule interaction using centrifugal force. Jpn J Appl Phys 58: SIIC03. https://doi.org/10.7567/1347-4065/ab1b5e
    Punnoose JA, Hayden A, Zhou L, Halvorsen K (2020) Wi-Fi live-streaming centrifuge force microscope for benchtop single-molecule experiments. Biophys J 119: 2231−2239 doi: 10.1016/j.bpj.2020.10.017
    Ren Y, Yang J, Jin H, Zhang Y, Berro J (2023) Force redistribution in clathrin-mediated endocytosis revealed by phase-separating force sensors. Sci Adv 9(41): eadi1535. https://doi.org/10.1126/sciadv.adi1535
    Ribeck N, Saleh OA (2013) DNA unwinding by ring-shaped T4 helicase gp41 is hindered by tension on the occluded strand. PLoS One 8: e79237. https://doi.org/10.1371/journal.pone.0079237
    Sarkar R, Rybenkov VV (2016) A guide to magnetic tweezers and their applications. Front Physics 4. https://doi.org/10.3389/fphy.2016.00048
    Scarpa E, Finet C, Blanchard GB, Sanson B (2018) Actomyosin-driven tension at compartmental boundaries orients cell division independently of cell geometry in vivo. Dev Cell 47: 727−740.e6 doi: 10.1016/j.devcel.2018.10.029
    Schaich MA, Schnable BL, Kumar N, Roginskaya V, Jakielski RC, Urban R, Zhong Z, Kad NM, Van Houten B (2023) Single-molecule analysis of DNA-binding proteins from nuclear extracts (SMADNE). Nucleic Acids Res 51: e39. https://doi.org/10.1093/nar/gkad095
    Siahaan V, Tan R, Humhalova T, Libusova L, Lacey SE, Tan T, Dacy M, Ori-McKenney KM, McKenney RJ, Braun M, Lansky Z (2022) Microtubule lattice spacing governs cohesive envelope formation of tau family proteins. Nat Chem Biol 18: 1224−1235 doi: 10.1038/s41589-022-01096-2
    Sitters G, Kamsma D, Thalhammer G, Ritsch-Marte M, Peterman EJG, Wuite GJL (2015) Acoustic force spectroscopy. Nat Methods 12: 47−50 doi: 10.1038/nmeth.3183
    Skinner GM, Kalafut BS, Visscher K (2011) Downstream DNA tension regulates the stability of the T7 RNA polymerase initiation complex. Biophys J 100: 1034−1041 doi: 10.1016/j.bpj.2010.11.092
    ter Keurs HE, Iwazumi T, Pollack GH (1978) The sarcomere length-tension relation in skeletal muscle. J Gen Physiol 72: 565−592 doi: 10.1085/jgp.72.4.565
    Tskhovrebova L, Trinick J, Sleep JA, Simmons RM (1997) Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387: 308−312 doi: 10.1038/387308a0
    Visscher K (2016) −1 Programmed ribosomal frameshifting as a force-dependent process. Prog Mol Biol Transl Sci 139: 45−72 doi: 10.1016/bs.pmbts.2015.11.003
    Wang MD, Schnitzer MJ, Yin H, Landick R, Gelles J, Block SM (1998) Force and velocity measured for single molecules of RNA polymerase. Science 282: 902−907 doi: 10.1126/science.282.5390.902
    Wee LM, Tong AB, Ariza AJF, Cañari-Chumpitaz C, Grob P, Nogales E, Bustamante CJ (2023) A trailing ribosome speeds up RNA polymerase at the expense of transcript fidelity via force and allostery. Cell 186: 1244−1262.e34 doi: 10.1016/j.cell.2023.02.008
    Witt H, Harju J, Chameau EMJ, Bruinsma CMA, Clement TVM, Nielsen CF, Hickson ID, Peterman EJG, Broedersz CP, Wuite GJL (2023) Ion-mediated condensation controls the mechanics of mitotic chromosomes. bioRxiv 2023.04. 11.536423. https://doi.org/10.1101/2023.04.11.536423
    Woodside MT, Behnke-Parks WM, Larizadeh K, Travers K, Herschlag D, Block SM (2006) Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins. Proc Natl Acad Sci USA 103: 6190−6195 doi: 10.1073/pnas.0511048103
    Wuite GJ, Smith SB, Young M, Keller D, Bustamante C (2000) Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404: 103−106 doi: 10.1038/35003614
    Xu L, Cabanas-Danés J, Halma MTJ, Heller I, Stratmann SA, van Oijen AM, Lee S-J, Peterman EJG, Wuite GJL (2023a) Regulation of T7 gp2.5 binding dynamics by its C-terminal tail, template conformation and sequence. Nucleic Acids Res 51(13): 6540−6553 doi: 10.1093/nar/gkad485
    Xu L, Halma MTJ, Wuite GJL (2023b) Unravelling how single-stranded DNA binding protein coordinates DNA metabolism using single-molecule approaches. Int J Mol Sci 24: 2806. https://doi.org/10.3390/ijms24032806
    Yin H, Wang MD, Svoboda K, Landick R, Block SM, Gelles J (1995) Transcription against an applied force. Science 270: 1653−1657 doi: 10.1126/science.270.5242.1653
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