1932

Abstract

Single-molecule technologies have expanded our ability to detect biological events individually, in contrast to ensemble biophysical technologies, where the result provides averaged information. Recent developments in atomic force microscopy have not only enabled us to distinguish the heterogeneous phenomena of individual molecules, but also allowed us to view up to the resolution of a single covalent bond. Similarly, optical tweezers, due to their versatility and precision, have emerged as a potent technique to dissect a diverse range of complex biological processes, from the nanomechanics of ClpXP protease–dependent degradation to force-dependent processivity of motor proteins. Despite the advantages of optical tweezers, the time scales used in this technology were inconsistent with physiological scenarios, which led to the development of magnetic tweezers, where proteins are covalently linked with the glass surface, which in turn increases the observation window of a single biomolecule from minutes to weeks. Unlike optical tweezers, magnetic tweezers use magnetic fields to impose torque, which makes them convenient for studying DNA topology and topoisomerase functioning. Using modified magnetic tweezers, researchers were able to discover the mechanical role of chaperones, which support their substrate proteinsby pulling them during translocation and assist their native folding as a mechanical foldase. In this article, we provide a focused review of many of these new roles of single-molecule technologies, ranging from single bond breaking to complex chaperone machinery, along with the potential to design mechanomedicine, which would be a breakthrough in pharmacological interventions against many diseases.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-090420-083836
2021-05-06
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/biophys/50/1/annurev-biophys-090420-083836.html?itemId=/content/journals/10.1146/annurev-biophys-090420-083836&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ainavarapu SRK, Brujić J, Huang HH, Wiita AP, Lu H et al. 2007. Contour length and refolding rate of a small protein controlled by engineered disulfide bonds. Biophys. J. 92:1225–33
    [Google Scholar]
  2. 2. 
    Alegre-Cebollada J, Badilla CL, Fernández JM. 2010. Isopeptide bonds block the mechanical extension of pili in pathogenic Streptococcus pyogenes. J. Biol. Chem. 285:11235–42
    [Google Scholar]
  3. 3. 
    Alegre-Cebollada J, Kosuri P, Rivas-Pardo JA, Fernández JM. 2011. Direct observation of disulfide isomerization in a single protein. Nat. Chem. 3:882–87
    [Google Scholar]
  4. 4. 
    Allersma MW, Gittes F, DeCastro MJ, Stewart RJ, Schmidt CF. 1998. Two-dimensional tracking of ncd motility by back focal plane interferometry. Biophys. J. 74:21074–85
    [Google Scholar]
  5. 5. 
    Alonso-Caballero A, Echelman DJ, Tapia-Rojo R, Haldar S. 2019. Protein folding modulates the adhesion strategy of Gram positive pathogens. bioRxiv 743393. https://doi.org/10.1101/743393
    [Crossref]
  6. 6. 
    Andersson M, Björnham O, Svantesson M, Badahdah A, Uhlin BE, Bullitt E. 2012. A structural basis for sustained bacterial adhesion: biomechanical properties of CFA/I pili. J. Mol. Biol. 415:5918–28
    [Google Scholar]
  7. 7. 
    Ashkin A, Dziedzic JM, Bjorkholm JE, Chu S 1986. Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11:5288–90
    [Google Scholar]
  8. 8. 
    Aubin-Tam ME, Olivares AO, Sauer RT, Baker TA, Lang MJ. 2011. Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145:P257–67
    [Google Scholar]
  9. 9. 
    Badman RP, Ye F, Wang MD. 2019. Towards biological applications of nanophotonic tweezers. Curr. Opin. Chem. Biol. 53:158–66
    [Google Scholar]
  10. 10. 
    Bausch AR, Ziemann F, Boulbitch AA, Jacobson K, Sackmann E. 1998. Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophys. J. 75:42038–49
    [Google Scholar]
  11. 11. 
    Bhaumik P, Koski MK, Glumoff T, Hiltunen JK, Wierenga RK. 2005. Structural biology of the thioester-dependent degradation and synthesis of fatty acids. Curr. Opin. Struct. Biol. 15:621–28
    [Google Scholar]
  12. 12. 
    Binnig G, Quate CF, Gerber C. 1986. Atomic force microscope. Phys. Rev. Lett. 56:9930–33
    [Google Scholar]
  13. 13. 
    Block SM, Schnitzer MJ. 1997. Kinesin hydrolyses one ATP per 8-nm step. Nature 388:386–90
    [Google Scholar]
  14. 14. 
    Broadley SA, Hartl FU. 2009. The role of molecular chaperones in human misfolding diseases. FEBS Lett 583:162647–53
    [Google Scholar]
  15. 15. 
    Cordova JC, Olivares AO, Shin Y, Stinson BM, Calmat S et al. 2014. Stochastic but highly coordinated protein unfolding and translocation by the ClpXP proteolytic machine. Cell 158:647–58
    [Google Scholar]
  16. 16. 
    Cumpson PJ, Zhdan P, Hedley J. 2004. Calibration of AFM cantilever stiffness: a microfabricated array of reflective springs. Ultramicroscopy 100:3–4241–51
    [Google Scholar]
  17. 17. 
    Dierks T, Klappa P, Wiech H, Zimmermann R. 1993. The role of molecular chaperones in protein transport into the endoplasmic reticulum. Philos. Trans. R. Soc. Lond. B 339: 1289.335–41
    [Google Scholar]
  18. 18. 
    Douglas PM, Summers DW, Cyr DM. 2009. Molecular chaperones antagonize proteotoxicity by differentially modulating protein aggregation pathways. Prion 3:251–58
    [Google Scholar]
  19. 19. 
    Echelman DJ, Alegre-Cebollada J, Badilla CL, Chang C, Ton-That H, Fernández JM 2016. CnaA domains in bacterial pili are efficient dissipaters of large mechanical shocks. PNAS 113:2490–95
    [Google Scholar]
  20. 20. 
    Echelman DJ, Lee AQ, Fernández JM. 2017. Mechanical forces regulate the reactivity of a thioester bond in a bacterial adhesion. J. Biol. Chem. 292:8988–97
    [Google Scholar]
  21. 21. 
    Eckels EC, Echelman DJ, Rivas-Pardo JA, Fernández JM. 2018. Real-time detection of thiol chemistry in single proteins. Oxidative Folding of Proteins: Basic Principles, Cellular Regulation and Engineering MJ Feige 52–80 London: R. Soc. Chem.
    [Google Scholar]
  22. 22. 
    Eckels EC, Haldar S, Tapia-Rojo R, Rivas-Pardo JA, Fernández JM. 2019. The mechanical power of titin folding. Cell Rep 27:1836–47.e4
    [Google Scholar]
  23. 23. 
    Fisher JK, Cribb J, Desai KV, Vicci L, Wilde B et al. 2006. Thin-foil magnetic force system for high-numerical-aperture microscopy. Rev. Sci. Instrum. 77:2023702
    [Google Scholar]
  24. 24. 
    Gatsogiannis C, Balogh D, Merino F, Sieber SA, Raunser S. 2019. Cryo-EM structure of the ClpXP protein degradation machinery. Nat. Struct. Mol. Biol. 26:10946–54
    [Google Scholar]
  25. 25. 
    Gee MA, Heuser JE, Vallee RB. 1997. An extended microtubule-binding structure within the dynein motor domain. Nature 390:6660636–39
    [Google Scholar]
  26. 26. 
    Gennerich A, Carter AP, Reck-Peterson SL, Vale RD 2007. Force-induced bidirectional stepping of cytoplasmic dynein. Cell 131:952–65
    [Google Scholar]
  27. 27. 
    Gennerich A, Vale RD. 2009. Walking the walk: how kinesin and dynein coordinate their steps. Curr. Opin. Cell Biol. 21:59–67
    [Google Scholar]
  28. 28. 
    Giganti D, Yan K, Badilla CL, Fernandez JM, Alegre-Cebollada J. 2018. Disulfide isomerization reactions in titin immunoglobulin domains enable a mode of protein elasticity. Nat. Commun. 9:1185
    [Google Scholar]
  29. 29. 
    Glynn SE, Martin A, Nager AR, Baker TA, Sauer RT. 2009. Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139:P744–56
    [Google Scholar]
  30. 30. 
    Gosse C, Croquette V. 2002. Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys. J. 82:3314–29
    [Google Scholar]
  31. 31. 
    Grandbois M. 1999. How strong is a covalent bond?. Science 283:54081727–30
    [Google Scholar]
  32. 32. 
    Guydosh NR, Block SM 2006. Backsteps induced by nucleotide analogs suggest the front head of kinesin is gated by strain. PNAS 103:8054–59
    [Google Scholar]
  33. 33. 
    Haldar S, Eckels EC, Echelman DJ, Rivas-Pardo JA, Fernandez JM. 2018. DsbA is a switchable mechanical chaperone. bioRxiv 310169. https://doi.org/10.1101/310169
    [Crossref]
  34. 34. 
    Haldar S, Tapia-Rojo R, Eckels EC, Valle-Orero J, Fernandez JM. 2017. Trigger factor chaperone acts as a mechanical foldase. Nat. Commun. 8:1668
    [Google Scholar]
  35. 35. 
    Hartl FU. 2017. Protein misfolding diseases. Annu. Rev. Biochem. 86:21–26
    [Google Scholar]
  36. 36. 
    Hashemi Shabestari M, Meijering AEC, Roos WH, Wuite GJL, Peterman EJG. 2017. Recent advances in biological single-molecule applications of optical tweezers and fluorescence microscopy. Methods Enzymol. 582:85–119
    [Google Scholar]
  37. 37. 
    Health W. 1983. Mechanisms in enteropathogenic Escherichia coli diarrhoea. Lancet 321:83361254–56
    [Google Scholar]
  38. 38. 
    Hishiya A, Takayama S. 2008. Molecular chaperones as regulators of cell death. Oncogene 27:506489–506
    [Google Scholar]
  39. 39. 
    Hoffstrom BG, Kaplan A, Letso R, Schmid RS, Turmel GJ et al. 2010. Inhibitors of protein disulfide isomerase suppress apoptosis induced by misfolded proteins. Nat. Chem. Biol. 6:12900–6
    [Google Scholar]
  40. 40. 
    Iosefson O, Nager AR, Baker TA, Sauer RT. 2015. Coordinated gripping of substrate by subunits of a AAA+ proteolytic machine. Nat. Chem. Biol. 11:201–6
    [Google Scholar]
  41. 41. 
    Isojima H, Iino R, Niitani Y, Noji H, Tomishige M. 2016. Direct observation of intermediate states during the stepping motion of kinesin-1. Nat. Chem. Biol. 12:4290–97
    [Google Scholar]
  42. 42. 
    Jing P, Wu J, Liu GW, Keeler EG, Pun SH, Lin LY. 2016. Photonic crystal optical tweezers with high efficiency for live biological samples and viability characterization. Sci. Rep. 6:19924
    [Google Scholar]
  43. 43. 
    Johnston CL, Marzano NR, van Oijen AM, Ecroyd H. 2018. Using single-molecule approaches to understand the molecular mechanisms of heat-shock protein chaperone function. J. Mol. Biol. 430:224525–46
    [Google Scholar]
  44. 44. 
    Keller M, Schilling J, Sackmann E. 2001. Oscillatory magnetic bead rheometer for complex fluid microrheometry. Rev. Sci. Instrum. 72:3626
    [Google Scholar]
  45. 45. 
    Kim D, Lim S, Haque MM, Ryoo N, Hong HS et al. 2015. Identification of disulfide cross-linked tau dimer responsible for tau propagation. Sci. Rep. 5:115231
    [Google Scholar]
  46. 46. 
    Klumpp LM, Hoenger A, Gilbert SP 2004. Kinesin's second step. PNAS 101:103444–49
    [Google Scholar]
  47. 47. 
    Kosuri P, Alegre-Cebollada J, Feng J, Kaplan A, Inglés-Prieto A et al. 2012. Protein folding drives disulfide formation. Cell 151:4794–806
    [Google Scholar]
  48. 48. 
    Lang MJ, Asbury CL, Shaevitz JW, Block SM. 2002. An automated two-dimensional optical force clamp for single molecule studies. Biophys. J. 83:491–501
    [Google Scholar]
  49. 49. 
    Langer T. 2000. AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem. Sci. 25:247–51
    [Google Scholar]
  50. 50. 
    Li X, Liu C, Chen S, Wang Y, Cheng SH, Sun D. 2017. In vivo manipulation of single biological cells with an optical tweezers-based manipulator and a disturbance compensation controller. IEEE Trans. Robot. 33:1200–12
    [Google Scholar]
  51. 51. 
    Liang J, Fernández JM. 2009. Mechanochemistry: one bond at a time. ACS Nano 3:1628–45
    [Google Scholar]
  52. 52. 
    Liang J, Fernández JM. 2011. Kinetic measurements on single-molecule disulfide bond cleavage. J. Am. Chem. Soc. 133:103528–34
    [Google Scholar]
  53. 53. 
    Lipfert J, Hao X, Dekker NH. 2009. Quantitative modeling and optimization of magnetic tweezers. Biophys. J. 96:5040–49
    [Google Scholar]
  54. 54. 
    Maillard RA, Chistol G, Sen M, Righini M, Tan J et al. 2011. ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145:P459–69
    [Google Scholar]
  55. 55. 
    Maître J-L, Heisenberg C-P. 2011. The role of adhesion energy in controlling cell-cell contacts. Curr. Opin. Cell Biol. 23:5508–14
    [Google Scholar]
  56. 56. 
    Mallik R. 2019. From physics to physiology at the membrane-motor interface. Nat. Rev. Mol. Cell Biol. 21:61–62
    [Google Scholar]
  57. 57. 
    Mallik R, Carter BC, Lex SA, King SJ, Gross SP. 2004. Cytoplasmic dynein functions as a gear in response to load. Nature 427:6975649–52
    [Google Scholar]
  58. 58. 
    Mallik R, Rai AK, Barak P, Rai A, Kunwar A. 2013. Teamwork in microtubule motors. Trends Cell Biol 23:11575–82
    [Google Scholar]
  59. 59. 
    Mashaghi A, Bezrukavnikov S, Minde DP, Wentink AS, Kityk R et al. 2016. Alternative modes of client binding enable functional plasticity of Hsp70. Nature 539:448–51
    [Google Scholar]
  60. 60. 
    Mashaghi A, Kramer G, Bechtluft P, Zachmann-Brand B, Driessen AJM et al. 2013. Reshaping of the conformational search of a protein by the chaperone trigger factor. Nature 500:746098–101
    [Google Scholar]
  61. 61. 
    Meunier L, Usherwood YK, Tae Chung K, Hendershot LM 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13:4456–69
    [Google Scholar]
  62. 62. 
    Mitchell CA, Shi C, Aldrich CC, Gulick AM. 2012. Structure of PA1221, a non-ribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains. Biochemistry 51:3252–63
    [Google Scholar]
  63. 63. 
    Moreno DF, Parisi E, Yahya G, Vaggi F, Csikász-Nagy A, Aldea M. 2019. Competition in the chaperone-client network subordinates cell-cycle entry to growth and stress. Life Sci. Alliance 2:2e201800277
    [Google Scholar]
  64. 64. 
    Mori T, Vale RD, Tomishige M. 2007. How kinesin waits between steps. Nature 450:750–54
    [Google Scholar]
  65. 65. 
    Mortezaei N, Singh B, Zakrisson J, Bullitt E, Andersson M. 2015. Biomechanical and structural features of CS2 fimbriae of enterotoxigenic Escherichia coli. Biophys. J. 109:149–56
    [Google Scholar]
  66. 66. 
    Mossuto MF. 2013. Disulfide bonding in neurodegenerative misfolding diseases. Int. J. Cell Biol. 2013.318319
    [Google Scholar]
  67. 67. 
    Neuman KC, Block SM. 2004. Optical trapping. Rev. Sci. Instrum. 75:92787–809
    [Google Scholar]
  68. 68. 
    Neuman KC, Lionnet T, Allemand J-F. 2007. Single-molecule micromanipulation techniques. Annu. Rev. Mater. Res. 37:33–67
    [Google Scholar]
  69. 69. 
    Neuman KC, Nagy A. 2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5:6491–505
    [Google Scholar]
  70. 70. 
    Nicholas MP, Höök P, Brenner S, Wynne CL, Vallee RB, Gennerich A. 2015. Control of cytoplasmic dynein force production and processivity by its C-terminal domain. Nat. Commun. 6:16206
    [Google Scholar]
  71. 71. 
    Nuccitelli A, Cozzi R, Gourlay LJ, Donnarumma D, Necchi F et al. 2011. Structure-based approach to rationally design a chimeric protein for an effective vaccine against Group B Streptococcus infections. PNAS 108:2510278–83
    [Google Scholar]
  72. 72. 
    Olivares AO, Baker TA, Sauer RT. 2018. Mechanical protein unfolding and degradation. Annu. Rev. Physiol. 80:413–29
    [Google Scholar]
  73. 73. 
    Pan S, Malik IT, Thomy D, Henrichfreise B, Sass P. 2019. The functional ClpXP protease of Chlamydia trachomatis requires distinct clpP genes from separate genetic loci. Sci. Rep. 9:114129
    [Google Scholar]
  74. 74. 
    Pasinelli P, Brown RH. 2006. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 7:710–23
    [Google Scholar]
  75. 75. 
    Pointon JA, Smith WD, Saalbach G, Crow A, Kehoe MA, Banfield MJ. 2010. A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. J. Biol. Chem. 285:33858–66
    [Google Scholar]
  76. 76. 
    Popa I, Rivas-Pardo JA, Eckels EC, Echelman DJ, Badilla CL et al. 2016. A HaloTag anchored ruler for week-long studies of protein dynamics. J. Am. Chem. Soc. 138:3310546–53
    [Google Scholar]
  77. 77. 
    Rai A, Pathak D, Thakur S, Singh S, Dubey AK, Mallik R. 2016. Dynein clusters into lipid microdomains on phagosomes to drive rapid transport toward lysosomes. Cell 164:4722–34
    [Google Scholar]
  78. 78. 
    Rao L, Berger F, Nicholas MP, Gennerich A. 2019. Molecular mechanism of cytoplasmic dynein tension sensing. Nat. Commun. 10:13332
    [Google Scholar]
  79. 79. 
    Reck-Peterson SL, Yildiz A, Carter AP, Gennerich A, Zhang N, Vale RD. 2006. Single-molecule analysis of dynein processivity and stepping behavior. Cell 126:2335–48
    [Google Scholar]
  80. 80. 
    Rief M. 1997. Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 275:53041295–97
    [Google Scholar]
  81. 81. 
    Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:53151109–12
    [Google Scholar]
  82. 82. 
    Rivas-Pardo JA, Badilla CL, Tapia-Rojo R, Alonso-Caballero Á, Fernández JM 2018. Molecular strategy for blocking isopeptide bond formation in nascent pilin proteins. PNAS 115:9222–27
    [Google Scholar]
  83. 83. 
    Roberts AJ, Kon T, Knight PJ, Sutoh K, Burgess SA. 2013. Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol. 14:11713–26
    [Google Scholar]
  84. 84. 
    Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P et al. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59–62
    [Google Scholar]
  85. 85. 
    Rosenfeld SS, Fordyce PM, Jefferson GM, King PH, Block SM. 2003. Stepping and stretching: how kinesin uses internal strain to walk processively. J. Biol. Chem. 278:18550–56
    [Google Scholar]
  86. 86. 
    Sarkar R, Rybenkov VV. 2016. A guide to magnetic tweezers and their applications. Front. Phys. 4:48
    [Google Scholar]
  87. 87. 
    Schönfelder J, Alonso-Caballero A, De Sancho D, Perez-Jimenez R. 2018. The life of proteins under mechanical force. Chem. Soc. Rev. 47:3558–73
    [Google Scholar]
  88. 88. 
    Selvaggi L, Pasakarnis L, Brunner D, Aegerter CM. 2018. Magnetic tweezers optimized to exert high forces over extended distances from the magnet in multicellular systems. Rev. Sci. Instrum. 89:045106
    [Google Scholar]
  89. 89. 
    Sen M, Maillard RA, Nyquist K, Rodriguez-Aliaga P, Pressé S et al. 2013. The ClpXP protease unfolds substrates using a constant rate of pulling but different gears. Cell 155:P636–46
    [Google Scholar]
  90. 90. 
    Sevier CS, Kaiser CA. 2002. Formation and transfer of disulphide bonds in living cells. Nat. Rev. Mol. Cell Biol. 3:836–47
    [Google Scholar]
  91. 91. 
    Shao Z, Yang J, Somlyo AP 1995. Biological atomic force microscopy: from microns to nanometers and beyond. Annu. Rev. Cell Dev. Biol. 11:241–65
    [Google Scholar]
  92. 92. 
    Singh B, Mortezaei N, Savarino SJ, Uhlin BE, Bullitt E, Andersson M. 2017. Antibodies damage the resilience of fimbriae, causing them to be stiff and tangled. J. Bacteriol. 199:1e00665–16
    [Google Scholar]
  93. 93. 
    Singh B, Mortezaei N, Uhlin BE, Savarino SJ, Bullitt E, Andersson M. 2015. Antibody-mediated disruption of the mechanics of CS20 fimbriae of enterotoxigenic Escherichia coli. Sci. Rep. 5:13678
    [Google Scholar]
  94. 94. 
    Smith WD, Pointon JA, Abbot E, Kang HJ, Baker EN et al. 2010. Roles of minor pilin subunits Spy0125 and Spy0130 in the serotype M1 Streptococcus pyogenes strain SF370. J. Bacteriol. 192:184651–59
    [Google Scholar]
  95. 95. 
    Stinson BM, Nager AR, Glynn SE, Schmitz KR, Baker TA, Sauer RT. 2013. Nucleotide binding and conformational switching in the hexameric ring of a AAA+ machine. Cell 153:628–39
    [Google Scholar]
  96. 96. 
    Svoboda K, Block SM. 1994. Force and velocity measured for single kinesin molecules. Cell 77:5773–84
    [Google Scholar]
  97. 97. 
    Svoboda K, Schmidt CF, Schnapp BJ, Block SM. 1993. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365:721–27
    [Google Scholar]
  98. 98. 
    Sweeney HL, Holzbaur ELF. 2018. Motor proteins. Cold Spring Harb. Perspect. Biol. 10:5a021931
    [Google Scholar]
  99. 99. 
    Tapia-Rojo R, Eckels EC, Fernández JM 2019. Ephemeral states in protein folding under force captured with a magnetic tweezers design. PNAS 116:167873–78
    [Google Scholar]
  100. 100. 
    Toba S, Watanabe TM, Yamaguchi-Okimoto L, Toyoshima YY, Higuchi H 2006. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. PNAS 103:5741–45
    [Google Scholar]
  101. 101. 
    Tsai M-Y, Morfini G, Szebenyi G, Brady ST. 2000. Release of kinesin from vesicles by hsc70 and regulation of fast axonal transport. Mol. Biol. Cell. 11:62161–73
    [Google Scholar]
  102. 102. 
    Uehara T, Nakamura T, Yao D, Shi Z-Q, Gu Z et al. 2006. S-Nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441:7092513–17
    [Google Scholar]
  103. 103. 
    Uemura S, Ishiwata S. 2003. Loading direction regulates the affinity of ADP for kinesin. Nat. Struct. Mol. Biol. 10:4308–11
    [Google Scholar]
  104. 104. 
    Uemura S, Kawaguchi K, Yajima J, Edamatsu M, Yano Toyoshima Y, Ishiwata S 2002. Kinesin-microtubule binding depends on both nucleotide state and loading direction. PNAS 99:5977–81
    [Google Scholar]
  105. 105. 
    Walden M, Edwards JM, Dziewulska AM, Bergmann R, Saalbach G et al. 2015. An internal thioester in a pathogen surface protein mediates covalent host binding. eLife 4:e06638
    [Google Scholar]
  106. 106. 
    Wang B, Xiao S, Edwards SA, Gräter F. 2013. Isopeptide bonds mechanically stabilize Spy0128 in bacterial pili. Biophys. J. 104:2051–57
    [Google Scholar]
  107. 107. 
    Webb RC. 2003. Smooth muscle contraction and relaxation. Adv. Physiol. Educ. 27:4201–6
    [Google Scholar]
  108. 108. 
    Wiita AP, Ainavarapu SRK, Huang HH, Fernandez JM 2006. Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques. PNAS 103:7222–27
    [Google Scholar]
  109. 109. 
    Willaert R, Kasas S, Devreese B, Dietler G. 2016. Yeast nanobiotechnology. Fermentation 2:18
    [Google Scholar]
  110. 110. 
    Wruck F, Avellaneda MJ, Koers EJ, Minde DP, Mayer MP et al. 2018. Protein folding mediated by trigger factor and Hsp70: new insights from single-molecule approaches. J. Mol. Biol. 430:438–49
    [Google Scholar]
  111. 111. 
    Wruck F, Katranidis A, Nierhaus KH, Büldt G, Hegner M 2017. Translation and folding of single proteins in real time. PNAS 114:22E4399–407
    [Google Scholar]
  112. 112. 
    Wu W, Zhu X, Song C. 2019. Single-molecule technique: a revolutionary approach to exploring fundamental questions in plant science. New Phytol 223:2508–10
    [Google Scholar]
  113. 113. 
    Xu S, Wang J, Wang J-H, Springer TA 2017. Distinct recognition of complement iC3b by integrins αXβ2 and αMβ2. PNAS 114:4303–8
    [Google Scholar]
  114. 114. 
    Yan J, Skoko D, Marko JF. 2004. Near-field-magnetic-tweezer manipulation of single DNA molecules. Phys. Rev. E 70:1011905
    [Google Scholar]
  115. 115. 
    Yildiz A, Tomishige M, Gennerich A, Vale RD. 2008. Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134:1030–41
    [Google Scholar]
  116. 116. 
    Zacchia NA, Valentine MT. 2015. Design and optimization of arrays of neodymium iron boron-based magnets for magnetic tweezers applications. Rev. Sci. Instrum. 86:5053704
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-090420-083836
Loading
/content/journals/10.1146/annurev-biophys-090420-083836
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error