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Annual Review of Biophysics

Volume 52, 2023

Protein Diffusion Along Protein and DNA Lattices: Role of Electrostatics and Disordered Regions

Abstract

Diffusion is a pervasive process present in a broad spectrum of cellular reactions. Its mathematical description has existed for nearly two centuries and permits the construction of simple rules for evaluating the characteristic timescales of diffusive processes and some of their determinants. Although the term diffusion originally referred to random motions in three-dimensional (3D) media, several biological diffusion processes in lower dimensions have been reported. One-dimensional (1D) diffusions have been reported, for example, for translocations of various proteins along DNA or protein (e.g., microtubule) lattices and translation of helical peptides along the coiled-coil interface. Two-dimensional (2D) diffusion has been shown for dynamics of proteins along membranes. The microscopic mechanisms of these 1–3D diffusions may vary significantly depending on the nature of the diffusing molecules, the substrate, and the interactions between them. In this review, we highlight some key examples of 1–3D biomolecular diffusion processes and illustrate the roles that electrostatic interactions and intrinsic disorder may play in modulating these processes.

Keyword(s): diffusion coefficient, disordered regions, DNA search, electrostatics, microtubule, sliding
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2023-05-09
2024-05-01
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Literature Cited

  1. 1.
    Ando T, Skolnick J. 2014. Sliding of proteins non-specifically bound to DNA: Brownian dynamics studies with coarse-grained protein and DNA models. PLOS Comput. Biol. 10:e1003990
     [Google Scholar]
  2. 2.
    Bagchi B, Blainey PC, Xie XS. 2008. Diffusion constant of a nonspecifically bound protein undergoing curvilinear motion along DNA. J. Phys. Chem. B 112:6282–84
     [Google Scholar]
  3. 3.
    Bellesia G, Shea JE. 2007. Self-assembly of beta-sheet forming peptides into chiral fibrillar aggregates. J. Chem. Phys. 126:245104
     [Google Scholar]
  4. 4.
    Berg OG, von Hippel PH. 1985. Diffusion-controlled macromolecular interactions. Annu. Rev. Biophys. Biophys. Chem. 14:131–60
     [Google Scholar]
  5. 5.
    Berg OG, Winter RB, von Hippel PH. 1981. Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20:6929–48
     [Google Scholar]
  6. 6.
    Bhattacherjee A, Krepel D, Levy Y. 2016. Coarse-grained models for studying protein diffusion along DNA. Wiley Interdiscip. Rev. Comput. Mol. Sci. 6:515–31
     [Google Scholar]
  7. 7.
    Bhattacherjee A, Levy Y. 2014. Search by proteins for their DNA target site: 1. The effect of DNA conformation on protein sliding. Nucleic Acids Res. 42:12404–14
     [Google Scholar]
  8. 8.
    Bigman LS, Greenblatt HM, Levy Y. 2021. What are the molecular requirements for protein sliding along DNA?. J. Phys. Chem. B 125:3119–31
     [Google Scholar]
  9. 9.
    Bigman LS, Iwahara J, Levy Y. 2022. Negatively charged disordered regions are prevalent and functionally important across proteomes. J. Mol. Biol. 434:167660
     [Google Scholar]
  10. 10.
    Bigman LS, Levy Y. 2020. Protein diffusion on charged biopolymers: DNA versus microtubule. Biophys. J. 118:3008–18
     [Google Scholar]
  11. 11.
    Bigman LS, Levy Y. 2020. Proteins: molecules defined by their trade-offs. Curr. Opin. Struct. Biol. 60:50–56
     [Google Scholar]
  12. 12.
    Bigman LS, Levy Y. 2020. Tubulin tails and their modifications regulate protein diffusion on microtubules. PNAS 117:201914772
     [Google Scholar]
  13. 13.
    Bigman LS, Levy Y. 2021. Modulating microtubules: a molecular perspective on the effects of tail modifications. J. Mol. Biol. 433:166988
     [Google Scholar]
  14. 14.
    Blainey PC, Luo G, Kou SC, Mangel WF, Verdine GL et al. 2009. Nonspecifically bound proteins spin while diffusing along DNA. Nat. Struct. Mol. Biol. 16:1224–29
     [Google Scholar]
  15. 15.
    Bodakuntla S, Yuan XD, Genova M, Gadadhar S, Leboucher S et al. 2021. Distinct roles of α- and β-tubulin polyglutamylation in controlling axonal transport and in neurodegeneration. EMBO J. 40:e108498
     [Google Scholar]
  16. 16.
    Brackley C, Cates M, Marenduzzo D. 2013. Intracellular facilitated diffusion: searchers, crowders, and blockers. Phys. Rev. Lett. 111:108101
     [Google Scholar]
  17. 17.
    Brodsky S, Jana T, Barkai N 2021. Order through disorder: the role of intrinsically disordered regions in transcription factor binding specificity. Curr. Opin. Struct. Biol. 71:110–15
     [Google Scholar]
  18. 18.
    Brodsky S, Jana T, Mittelman K, Chapal M, Kumar DK et al. 2020. Intrinsically disordered regions direct transcription factor in vivo binding specificity. Mol. Cell. 79:459–71.e4
     [Google Scholar]
  19. 19.
    Carter AP, Cho C, Jin L, Vale RD 2011. Crystal structure of the dynein motor domain. Science 331:1159–65
     [Google Scholar]
  20. 20.
    Chen R, Wold MS. 2014. Replication protein A: single-stranded DNA's first responder: dynamic DNA-interactions allow replication protein A to direct single-strand DNA intermediates into different pathways for synthesis or repair. Bioessays 36:1156–61
     [Google Scholar]
  21. 21.
    Cooper JR, Wordeman L. 2009. The diffusive interaction of microtubule binding proteins. Curr. Opin. Cell Biol. 21:68–73
     [Google Scholar]
  22. 22.
    Croasdale R, Ivins FJ, Muskett F, Daviter T, Scott DJ et al. 2011. An undecided coiled coil: The leucine zipper of Nek2 kinase exhibits atypical conformational exchange dynamics. J. Biol. Chem. 286:27537–47
     [Google Scholar]
  23. 23.
    Cuculis L, Abil Z, Zhao H, Schroeder CM. 2016. TALE proteins search DNA using a rotationally decoupled mechanism. Nat. Chem. Biol. 12:831–37
     [Google Scholar]
  24. 24.
    Dahirel V, Paillusson F, Jardat M, Barbi M, Victor JM 2009. Nonspecific DNA-protein interaction: why proteins can diffuse along DNA. Phys. Rev. Lett. 102:228101
     [Google Scholar]
  25. 25.
    Daitchman D, Greenblatt HM, Levy Y. 2018. Diffusion of ring-shaped proteins along DNA: case study of sliding clamps. Nucleic Acids Res. 46:5935–49
     [Google Scholar]
  26. 26.
    del Rio A, Perez-Jimenez R, Liu RC, Roca-Cusachs P, Fernandez JM, Sheetz MP. 2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638–41
     [Google Scholar]
  27. 27.
    Doucleff M, Clore GM. 2008. Global jumping and domain-specific intersegment transfer between DNA cognate sites of the multidomain transcription factor Oct-1. PNAS 105:13871–76
     [Google Scholar]
  28. 28.
    Fan J, Pavletich NP. 2012. Structure and conformational change of a replication protein A heterotrimer bound to ssDNA. Genes Dev. 26:2337–47
     [Google Scholar]
  29. 29.
    Fersht AR, Tafvizi A, Huang F, Mirny LA, van Oijen AM. 2011. A single-molecule characterization of p53 search on DNA. PNAS 108:563–68
     [Google Scholar]
  30. 30.
    Forth S, Hsia KC, Shimamoto Y, Kapoor TM. 2014. Asymmetric friction of nonmotor MAPs can lead to their directional motion in active microtubule networks. Cell 157:420–32
     [Google Scholar]
  31. 31.
    Freedman H, Luchko T, Luduena RF, Tuszynski JA. 2011. Molecular dynamics modeling of tubulin C-terminal tail interactions with the microtubule surface. Proteins Struct. Funct. Bioinform. 79:2968–82
     [Google Scholar]
  32. 32.
    Gadadhar S, Viar GA, Hansen JN, Gong A, Kostarev A et al. 2021. Tubulin glycylation controls axonemal dynein activity, flagellar beat, and male fertility. Science 371:eabd4914
     [Google Scholar]
  33. 33.
    Gibb B, Ye LF, Gergoudis SC, Kwon Y, Niu H et al. 2014. Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging. PLOS ONE 9:e87922
     [Google Scholar]
  34. 34.
    Givaty O, Levy Y. 2009. Protein sliding along DNA: dynamics and structural characterization. J. Mol. Biol. 385:1087–97
     [Google Scholar]
  35. 35.
    Gomez D, Gavrilov Y, Levy Y. 2019. Sliding mechanism at a coiled-coil interface. Biophys. J. 116:1228–38
     [Google Scholar]
  36. 36.
    Greenblatt HM, Rozenberg H, Daitchman D, Levy Y. 2020. Does PCNA diffusion on DNA follow a rotation-coupled translation mechanism?. Nat. Commun. 11:5000
     [Google Scholar]
  37. 37.
    Ha T, Kozlov AG, Lohman TM. 2012. Single-molecule views of protein movement on single-stranded DNA. Annu. Rev. Biophys. 41:295–319
     [Google Scholar]
  38. 38.
    Halford SE, Marko JF. 2004. How do site-specific DNA-binding proteins find their targets?. Nucleic Acids Res. 32:3040–52
     [Google Scholar]
  39. 39.
    Hazra MK, Levy Y. 2020. Charge pattern affects the structure and dynamics of polyampholyte condensates. Phys. Chem. Chem. Phys. 22:19368–75
     [Google Scholar]
  40. 40.
    Hazra MK, Levy Y. 2021. Biophysics of phase separation of disordered proteins is governed by balance between short- and long-range interactions. J. Phys. Chem. B 125:2202–11
     [Google Scholar]
  41. 41.
    Helenius J, Brouhard G, Kalaidzidis Y, Diez S, Howard J. 2006. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 441:115–19
     [Google Scholar]
  42. 42.
    Hinrichs MH, Jalal A, Brenner B, Mandelkow E, Kumar S, Scholz T. 2012. Tau protein diffuses along the microtubule lattice. J. Biol. Chem. 287:38559–68
     [Google Scholar]
  43. 43.
    Hummer G. 2005. Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular dynamics simulations. New J. Phys. 7:34
     [Google Scholar]
  44. 44.
    Itoh Y, Murata A, Takahashi S, Kamagata K. 2018. Intrinsically disordered domain of tumor suppressor p53 facilitates target search by ultrafast transfer between different DNA strands. Nucleic Acids Res. 46:7261–69
     [Google Scholar]
  45. 45.
    Iwahara J, Clore GM. 2006. Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440:1227–30
     [Google Scholar]
  46. 46.
    Iwahara J, Clore GM. 2006. Direct observation of enhanced translocation of a homeodomain between DNA cognate sites by NMR exchange spectroscopy. J. Am. Chem. Soc. 128:404–5
     [Google Scholar]
  47. 47.
    Iwahara J, Zweckstetter M, Clore GM. 2006. NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA. PNAS 103:15062–67
     [Google Scholar]
  48. 48.
    Jamecna D, Polidori J, Mesmin B, Dezi M, Levy D et al. 2019. An intrinsically disordered region in OSBP acts as an entropic barrier to control protein dynamics and orientation at membrane contact sites. Dev. Cell 49:220–34.e8
     [Google Scholar]
  49. 49.
    Jana T, Brodsky S, Barkai N. 2021. Speed-specificity trade-offs in the transcription factors search for their genomic binding sites. Trends Genet. 37:421–32
     [Google Scholar]
  50. 50.
    Janke C, Magiera MM. 2020. The tubulin code and its role in controlling microtubule properties and functions. Nat. Rev. Mol. Cell Biol. 21:307–26
     [Google Scholar]
  51. 51.
    Kabata H, Kurosawa O, Arai I, Washizu M, Margarson SA et al. 1993. Visualization of single molecules of RNA polymerase sliding along DNA. Science 262:1561–63
     [Google Scholar]
  52. 52.
    Kamagata K, Itoh Y, Subekti DRG. 2020. How p53 molecules solve the target DNA search problem: a review. Int. J. Mol. Sci. 21:1031
     [Google Scholar]
  53. 53.
    Kamagata K, Mano E, Ouchi K, Kanbayashi S, Johnson RC. 2018. High free-energy barrier of 1D diffusion along DNA by architectural DNA-binding proteins. J. Mol. Biol. 430:655–67
     [Google Scholar]
  54. 54.
    Kamagata K, Murata A, Itoh Y, Takahashi S. 2017. Characterization of facilitated diffusion of tumor suppressor p53 along DNA using single-molecule fluorescence imaging. J. Photochem. Photobiol. C 30:36–50
     [Google Scholar]
  55. 55.
    Katz M, Weinstein J, Eilon-Ashkenazy M, Gehring K, Cohen-Dvashi H et al. 2022. Structure and receptor recognition by the Lassa virus spike complex. Nature 603:174–79
     [Google Scholar]
  56. 56.
    Khazanov N, Levy Y. 2011. Sliding of p53 along DNA can be modulated by its oligomeric state and by cross-talks between its constituent domains. J. Mol. Biol. 408:335–55
     [Google Scholar]
  57. 57.
    Khazanov N, Marcovitz A, Levy Y. 2013. Asymmetric DNA-search dynamics by symmetric dimeric proteins. Biochemistry 52:5335–44
     [Google Scholar]
  58. 58.
    Koha HR, Kidwell MA, Ragunathand K, Doudnac JA, Myong S 2013. ATP-independent diffusion of double-stranded RNA binding proteins. PNAS 110:151–56
     [Google Scholar]
  59. 59.
    Kolomeisky A. 2011. Physics of protein-DNA interactions: mechanisms of facilitated target search. Phys. Chem. Chem. Phys. 13:2088–95
     [Google Scholar]
  60. 60.
    Komazin-Meredith G, Mirchev R, Golan DE, van Oijen AM, Coen DM. 2008. Hopping of a processivity factor on DNA revealed by single-molecule assays of diffusion. PNAS 10510721–26
  61. 61.
    Kon T, Imamula K, Roberts AJ, Ohkura R, Knight PJ et al. 2009. Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nat. Struct. Mol. Biol. 16:325–33
     [Google Scholar]
  62. 62.
    Kozlov AG, Lohman TM. 2002. Kinetic mechanism of direct transfer of Escherichia coli SSB tetramers between single-stranded DNA molecules. Biochemistry 41:11611–27
     [Google Scholar]
  63. 63.
    Krepel D, Gomez D, Klumpp S, Levy Y. 2016. Mechanism of facilitated diffusion during a DNA search in crowded environments. J. Phys. Chem. B 120:11113–22
     [Google Scholar]
  64. 64.
    Krepel D, Levy Y. 2016. Protein diffusion along DNA: on the effect of roadblocks and crowders. J. Phys. A 49:494003
     [Google Scholar]
  65. 65.
    Kunzelmann S, Morris C, Chavda AP, Eccleston JF, Webb MR. 2010. Mechanism of interaction between single-stranded DNA binding protein and DNA. Biochemistry 49:843–52
     [Google Scholar]
  66. 66.
    Kuznetsov SV, Kozlov AG, Lohman TM, Ansari A. 2006. Microsecond dynamics of protein-DNA interactions: direct observation of the wrapping/unwrapping kinetics of single-stranded DNA around the E. coli SSB tetramer. J. Mol. Biol. 359:55–65
     [Google Scholar]
  67. 67.
    Laurin Y, Eyer J, Robert CH, Prevost C, Sacquin-Mora S. 2017. Mobility and core-protein binding patterns of disordered C-terminal tails in β-tubulin isotypes. Biochemistry 56:1746–56
     [Google Scholar]
  68. 68.
    Leven I, Levy Y. 2019. Quantifying the two-state facilitated diffusion model of protein-DNA interactions. Nucleic Acids Res. 47:5530–38
     [Google Scholar]
  69. 69.
    Levine AJ, Oren M. 2009. The first 30 years of p53: growing ever more complex. Nat. Rev. Cancer 9:749–58
     [Google Scholar]
  70. 70.
    Li HL, DeRosier DJ, Nicholson WV, Nogales E, Downing KH. 2002. Microtubule structure at 8 Å resolution. Structure 10:1317–28
     [Google Scholar]
  71. 71.
    Lohman TM, Ferrari ME. 1994. Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem. 63:527–70
     [Google Scholar]
  72. 72.
    Maffeo C, Aksimentiev A. 2017. Molecular mechanism of DNA association with single-stranded DNA binding protein. Nucleic Acids Res. 45:12125–39
     [Google Scholar]
  73. 73.
    Magiera MM, Bodakuntla S, Ziak J, Lacomme S, Sousa PM et al. 2018. Excessive tubulin polyglutamylation causes neurodegeneration and perturbs neuronal transport. EMBO J. 37:e100440
     [Google Scholar]
  74. 74.
    Magiera MM, Singh P, Gadadhar S, Janke C. 2018. Tubulin posttranslational modifications and emerging links to human disease. Cell 173:1323–27
     [Google Scholar]
  75. 75.
    Marcovitz A, Levy Y. 2011. Frustration in protein-DNA binding influences conformational switching and target search kinetics. PNAS 108:17957–62
     [Google Scholar]
  76. 76.
    Marcovitz A, Levy Y. 2012. Sliding dynamics along DNA: a molecular perspective. Innovations in Biomolecular Modeling and Simulations, Vol. 2 T Schlick 237–62. London: R. Soc. Chem.
     [Google Scholar]
  77. 77.
    Marcovitz A, Levy Y. 2013. Obstacles may facilitate and direct DNA search by proteins. Biophys. J. 104:2042–50
     [Google Scholar]
  78. 78.
    Marcovitz A, Levy Y. 2013. Weak frustration regulates sliding and binding kinetics on rugged protein-DNA landscapes. J. Phys. Chem. B 117:13005–14
     [Google Scholar]
  79. 79.
    Marklund EG, Mahmutovic A, Berg OG, Hammar P, van der Spoel D et al. 2013. Transcription-factor binding and sliding on DNA studied using micro- and macroscopic models. PNAS 110:19796–801
     [Google Scholar]
  80. 80.
    Metzler R, Klafter J. 2000. The random walk's guide to anomalous diffusion: a fractional dynamics approach. Phys. Rep. 339:1–77
     [Google Scholar]
  81. 81.
    Mika JT, Poolman B. 2011. Macromolecule diffusion and confinement in prokaryotic cells. Curr. Opin. Biotechnol. 22:117–26
     [Google Scholar]
  82. 82.
    Mirny L, Slutsky M, Wunderlich Z, Tafvizi A, Leith J, Kosmrlj A. 2009. How a protein searches for its site on DNA: the mechanism of facilitated diffusion. J. Phys. A 42:434013
     [Google Scholar]
  83. 83.
    Mishra G, Bigman LS, Levy Y. 2020. ssDNA diffuses along replication protein A via a reptation mechanism. Nucleic Acids Res. 48:1701–14
     [Google Scholar]
  84. 84.
    Mishra G, Levy Y. 2015. Molecular determinants of the interactions between proteins and ssDNA. PNAS 112:5033–38
     [Google Scholar]
  85. 85.
    Mukherjee G, Pal A, Levy Y. 2017. Mechanism of the formation of the RecA-ssDNA nucleoprotein filament structure: a coarse-grained approach. Mol. Biosyst. 13:2697–703
     [Google Scholar]
  86. 86.
    Murugan R. 2021. A lattice model on the rate of in vivo site-specific DNA-protein interactions. Phys. Biol. 18:016005
     [Google Scholar]
  87. 87.
    Nguyen B, Sokoloski J, Galletto R, Elson EL, Wold MS, Lohman TM. 2014. Diffusion of human replication protein A along single-stranded DNA. J. Mol. Biol. 426:3246–61
     [Google Scholar]
  88. 88.
    Nogales E. 2000. Structural insights into microtubule function. Annu. Rev. Biochem. 69:277–302
     [Google Scholar]
  89. 89.
    Nogales E, Kellogg EH. 2017. Challenges and opportunities in the high-resolution cryo-EM visualization of microtubules and their binding partners. Curr. Opin. Struct. Biol. 46:65–70
     [Google Scholar]
  90. 90.
    Oshea EK, Klemm JD, Kim PS, Alber T. 1991. X-ray structure of the Gcn4 leucine zipper, a 2-stranded, parallel coiled coil. Science 254:539–44
     [Google Scholar]
  91. 91.
    Pal A, Greenblatt HM, Levy Y. 2020. Prerecognition diffusion mechanism of human DNA mismatch repair proteins along DNA: Msh2-Msh3 versus Msh2-Msh6. Biochemistry 59:4822–32
     [Google Scholar]
  92. 92.
    Pal A, Levy Y. 2019. Structure, stability and specificity of the binding of ssDNA and ssRNA with proteins. PLOS Comput. Biol. 15:e1006768
     [Google Scholar]
  93. 93.
    Pal A, Levy Y. 2020. Balance between asymmetry and abundance in multi-domain DNA-binding proteins may regulate the kinetics of their binding to DNA. PLOS Comput. Biol. 16:e1007867
     [Google Scholar]
  94. 94.
    Piatt SC, Loparo JJ, Price AC. 2019. The role of noncognate sites in the 1D search mechanism of EcoRI. Biophys. J. 116:2367–77
     [Google Scholar]
  95. 95.
    Pokhrel N, Origanti S, Davenport EP, Gandhi D, Kaniecki K et al. 2017. Monitoring replication protein A (RPA) dynamics in homologous recombination through site-specific incorporation of non-canonical amino acids. Nucleic Acids Res. 45:9413–26
     [Google Scholar]
  96. 96.
    Reichheld SE, Muiznieks LD, Keeley FW, Sharpe S. 2017. Direct observation of structure and dynamics during phase separation of an elastomeric protein. PNAS 114:E4408–15
     [Google Scholar]
  97. 97.
    Rodriguez G, Esadze A, Weiser BP, Schonhoft JD, Cole PA, Stivers JT. 2017. Disordered N-terminal domain of human uracil DNA glycosylase (hUNG2) enhances DNA translocation. ACS Chem. Biol. 12:2260–63
     [Google Scholar]
  98. 98.
    Roll-Mecak A. 2015. Intrinsically disordered tubulin tails: complex tuners of microtubule functions?. Semin. Cell Dev. Biol. 37:11–19
     [Google Scholar]
  99. 99.
    Roy R, Kozlov AG, Lohman TM, Ha T. 2007. Dynamic structural rearrangements between DNA binding modes of E. coli SSB protein. J. Mol. Biol. 369:1244–57
     [Google Scholar]
  100. 100.
    Roy R, Kozlov AG, Lohman TM, Ha T. 2009. SSB protein diffusion on single-stranded DNA stimulates RecA filament formation. Nature 461:1092–97
     [Google Scholar]
  101. 101.
    Rudolph J, Mahadevan J, Dyer P, Luger K. 2018. Poly(ADP-ribose) polymerase 1 searches DNA via a “monkey bar” mechanism. eLife 7:e37818
     [Google Scholar]
  102. 102.
    Saxton MJ. 1997. Single-particle tracking: the distribution of diffusion coefficients. Biophys. J. 72:1744–53
     [Google Scholar]
  103. 103.
    Schavemaker PE, Boersma AJ, Poolman B. 2018. How important is protein diffusion in prokaryotes?. Front. Mol. Biosci. 5:93
     [Google Scholar]
  104. 104.
    Schmidt H, Zalyte R, Urnavicius L, Carter AP. 2015. Structure of human cytoplasmic dynein-2 primed for its power stroke. Nature 518:435–38
     [Google Scholar]
  105. 105.
    Schoch RL, Brown FLH, Haran G. 2021. Correlated diffusion in lipid bilayers. PNAS 118:e2113202118
     [Google Scholar]
  106. 106.
    Schreiber G, Haran G, Zhou HX. 2009. Fundamental aspects of protein-protein association kinetics. Chem. Rev. 109:839–60
     [Google Scholar]
  107. 107.
    Schurr JM. 1979. One-dimensional diffusion-coefficient of proteins absorbed on DNA—hydrodynamic considerations. Biophys. Chem. 9:413–14
     [Google Scholar]
  108. 108.
    Shayegan M, Tahvildari R, Metera K, Kisley L, Michnick SW, Leslie SR. 2019. Probing inhomogeneous diffusion in the microenvironments of phase-separated polymers under confinement. J. Am. Chem. Soc. 141:7751–57
     [Google Scholar]
  109. 109.
    Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL. 2008. SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43:289–318
     [Google Scholar]
  110. 110.
    Shi Y, Zhang W, Yang Y, Murzin AG, Falcon B et al. 2021. Structure-based classification of tauopathies. Nature 598:359–63
     [Google Scholar]
  111. 111.
    Shvets AA, Kochugaeva MP, Kolomeisky AB. 2018. Mechanisms of protein search for targets on DNA: theoretical insights. Molecules 23:2106
     [Google Scholar]
  112. 112.
    Sirajuddin M, Rice LM, Vale RD. 2014. Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat. Cell Biol. 16:335–44
     [Google Scholar]
  113. 113.
    Slutsky M, Mirny LA. 2004. Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys. J. 87:4021–35
     [Google Scholar]
  114. 114.
    Snoberger A, Brettrager EJ, Smith DM. 2018. Conformational switching in the coiled-coil domains of a proteasomal ATPase regulates substrate processing. Nat. Commun. 9:2374
     [Google Scholar]
  115. 115.
    Spenkelink LM, Lewis JS, Jergic S, Xu ZQ, Robinson A et al. 2019. Recycling of single-stranded DNA-binding protein by the bacterial replisome. Nucleic Acids Res. 47:4111–23
     [Google Scholar]
  116. 116.
    Stewart CM, Buffalo CZ, Valderrama JA, Henningham A, Cole JN et al. 2016. Coiled-coil destabilizing residues in the group A Streptococcus M1 protein are required for functional interaction. PNAS 113:9515–20
     [Google Scholar]
  117. 117.
    Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. 2017. Phase separation drives heterochromatin domain formation. Nature 547:241–45
     [Google Scholar]
  118. 118.
    Subekti DRG, Murata A, Itoh Y, Takahashi S, Kamagata K. 2020. Transient binding and jumping dynamics of p53 along DNA revealed by sub-millisecond resolved single-molecule fluorescence tracking. Sci. Rep. 10:13697
     [Google Scholar]
  119. 119.
    Sudhof TC, Rothman JE. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–77
     [Google Scholar]
  120. 120.
    Suksombat S, Khafizov R, Kozlov AG, Lohman TM, Chemla YR. 2015. Structural dynamics of E. coli single-stranded DNA binding protein reveal DNA wrapping and unwrapping pathways. eLife 4:e08193
     [Google Scholar]
  121. 121.
    Tafvizi A, Huang F, Fersht AR, Mirny LA, van Oijen AM. 2011. A single-molecule characterization of p53 search on DNA. PNAS 108:563–68
     [Google Scholar]
  122. 122.
    Takayama Y, Clore GM. 2011. Intra- and intermolecular translocation of the bi-domain transcription factor Oct1 characterized by liquid crystal and paramagnetic NMR. PNAS 108:E169–76
     [Google Scholar]
  123. 123.
    Taylor NO, Wei MT, Stone HA, Brangwynne CP. 2019. Quantifying dynamics in phase-separated condensates using fluorescence recovery after photobleaching. Biophys. J. 117:1285–300
     [Google Scholar]
  124. 124.
    Terakawa T, Kenzaki H, Takada S. 2012. p53 searches on DNA by rotation-uncoupled sliding at C-terminal tails and restricted hopping of core domains. J. Am. Chem. Soc. 134:14555–62
     [Google Scholar]
  125. 125.
    Vasquez JK, Chantranuvatana K, Giardina DT, Coffman MD, Knight JD. 2014. Lateral diffusion of proteins on supported lipid bilayers: additive friction of synaptotagmin 7 C2A-C2B tandem domains. Biochemistry 53:7904–13
     [Google Scholar]
  126. 126.
    Veksler A, Kolomeisky AB. 2013. Speed-selectivity paradox in the protein search for targets on DNA: Is it real or not?. J. Phys. Chem. B 117:12695–701
     [Google Scholar]
  127. 127.
    von Hippel PH, Berg OG. 1989. Facilitated target location in biological systems. J. Biol. Chem. 264:675–78
     [Google Scholar]
  128. 128.
    Vousden KH, Prives C. 2009. Blinded by the light: the growing complexity of p53. Cell 137:413–31
     [Google Scholar]
  129. 129.
    Vuzman D, Azia A, Levy Y. 2010. Searching DNA via a “monkey bar” mechanism: the significance of disordered tails. J. Mol. Biol. 396:674–84
     [Google Scholar]
  130. 130.
    Vuzman D, Levy Y. 2010. DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail. PNAS 107:21004–9
     [Google Scholar]
  131. 131.
    Vuzman D, Levy Y. 2012. Intrinsically disordered regions as affinity tuners in protein-DNA interactions. Mol. Biosyst. 8:45–57
     [Google Scholar]
  132. 132.
    Vuzman D, Levy Y. 2014. The “monkey-bar” mechanism for searching for the DNA target site: the molecular determinants. Isr. J. Chem. 54:1374–81
     [Google Scholar]
  133. 133.
    Vuzman D, Polonsky M, Levy Y. 2010. Facilitated DNA search by multidomain transcription factors: cross talk via a flexible linker. Biophys. J. 99:1202–11
     [Google Scholar]
  134. 134.
    Wall KP, Hart H, Lee T, Page C, Hawkins TL, Hough LE. 2020. C-terminal tail polyglycylation and polyglutamylation alter microtubule mechanical properties. Biophys. J. 119:2219–30
     [Google Scholar]
  135. 135.
    Walshaw J, Woolfson DN. 2001. SOCKET: a program for identifying and analysing coiled-coil motifs within protein structures. J. Mol. Biol. 307:1427–50
     [Google Scholar]
  136. 136.
    Wang X, Bigman LS, Greenblatt HM, Yu B, Levy Y, Iwahara J. 2023. Negatively charged, intrinsically disordered regions can accelerate target search by DNA-binding proteins. Nucleic Acids Res. In press
    [Google Scholar]
  137. 137.
    Wehenkel A, Janke C. 2014. Towards elucidating the tubulin code. Nat. Cell Biol. 16:303–5
     [Google Scholar]
  138. 138.
    Wiggers F, Wohl S, Dubovetskyi A, Rosenblum G, Zheng WW, Hofmann H. 2021. Diffusion of a disordered protein on its folded ligand. PNAS 118:e2106690118
     [Google Scholar]
  139. 139.
    Woringer M, Izeddin I, Favard C, Berry H. 2020. Anomalous subdiffusion in living cells: bridging the gap between experiments and realistic models through collaborative challenges. Front. Phys. 8:134
     [Google Scholar]
  140. 140.
    Xi ZQ, Gao Y, Sirinakis G, Guo HL, Zhang YL. 2012. Single-molecule observation of helix staggering, sliding, and coiled coil misfolding. PNAS 109:5711–16
     [Google Scholar]
  141. 141.
    Zandarashvili L, Esadze A, Vuzman D, Kemme CA, Levy Y, Iwahara J. 2015. Balancing between affinity and speed in target DNA search by zinc-finger proteins via modulation of dynamic conformational ensemble. PNAS 112:E5142–49
     [Google Scholar]
  142. 142.
    Zandarashvili L, Vuzman D, Esadze A, Takayama Y, Sahu D et al. 2012. Asymmetrical roles of zinc fingers in dynamic DNA-scanning process by the inducible transcription factor Egr-1. PNAS 109:E1724–32
     [Google Scholar]
  143. 143.
    Zhou HX. 2011. Rapid search for specific sites on DNA through conformational switch of nonspecifically bound proteins. PNAS 108:8651–56
     [Google Scholar]
  144. 144.
    Zhou R, Kozlov AG, Roy R, Zhang J, Korolev S et al. 2011. SSB functions as a sliding platform that migrates on DNA via reptation. Cell 146:222–32
     [Google Scholar]
  145. 145.
    Ziemba BP, Knight JD, Falke JJ. 2012. Assembly of membrane-bound protein complexes: detection and analysis by single molecule diffusion. Biochemistry 51:1638–47
     [Google Scholar]
  146. 146.
    Zou Y, Liu YY, Wu XM, Shell SM. 2006. Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J. Cell. Physiol. 208:267–73
     [Google Scholar]
  147. 147.
    Zwanzig R. 1988. Diffusion in a rough potential. PNAS 85:2029–30
     [Google Scholar]
/content/journals/10.1146/annurev-biophys-111622-091220
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Protein Diffusion Along Protein and DNA Lattices: Role of Electrostatics and Disordered Regions
Annual Review of Biophysics 52, 463 (2023); https://doi.org/10.1146/annurev-biophys-111622-091220
/content/journals/10.1146/annurev-biophys-111622-091220
/content/journals/10.1146/annurev-biophys-111622-091220
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