1932

Abstract

Many enzymes appear to diffuse faster in the presence of substrate and to drift either up or down a concentration gradient of their substrate. Observations of these phenomena, termed enhanced enzyme diffusion (EED) and enzyme chemotaxis, respectively, lead to a novel view of enzymes as active matter. Enzyme chemotaxis and EED may be important in biology and could have practical applications in biotechnology and nanotechnology. They are also of considerable biophysical interest; indeed, their physical mechanisms are still quite uncertain. This review provides an analytic summary of experimental studies of these phenomena and of the mechanisms that have been proposed to explain them and offers a perspective on future directions for the field.

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2020-05-06
2024-04-25
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Literature Cited

  1. 1. 
    Agudo-Canalejo J, Adeleke-Larodo T, Illien P, Golestanian R 2018. Enhanced diffusion and chemotaxis at the nanoscale. Acc. Chem. Res. 51:2365–72
    [Google Scholar]
  2. 2. 
    Agudo-Canalejo J, Illien P, Golestanian R 2018. Phoresis and enhanced diffusion compete in enzyme chemotaxis. Nano Lett. 18:2711–17
    [Google Scholar]
  3. 3. 
    Anderson JL 1989. Colloid transport by interfacial forces. Annu. Rev. Fluid Mech. 21:61–99
    [Google Scholar]
  4. 4. 
    Astumian RD 2014. Enhanced diffusion, chemotaxis, and pumping by active enzymes: progress toward an organizing principle of molecular machines. ACS Nano 8:11917–24
    [Google Scholar]
  5. 5. 
    Astumian RD, Mukherjee S, Warshel A 2016. The physics and physical chemistry of molecular machines. ChemPhysChem 17:1719–41
    [Google Scholar]
  6. 6. 
    Bai X, Wolynes PG 2015. On the hydrodynamics of swimming enzymes. J. Chem. Phys. 143:165101
    [Google Scholar]
  7. 7. 
    Burrows JA, Goward CR 1992. Purification and properties of DNA polymerase from Bacillus caldotenax. Biochem. J. 287:971–77
    [Google Scholar]
  8. 8. 
    Brsch M, Turina P, Eggeling C, Fries JR, Seidel CA 1998. Conformational changes of the H+-ATPase from Escherichia coli upon nucleotide binding detected by single molecule fluorescence. FEBS Lett. 437:251–54
    [Google Scholar]
  9. 9. 
    Challberg MD, Englund PT 1979. Purification and properties of the deoxyribonucleic acid polymerase induced by vaccinia virus. J. Biol. Chem. 254:7812–19
    [Google Scholar]
  10. 10. 
    Colberg PH, Kapral R 2014. Ångström-scale chemically powered motors. Europhys. Lett. 106:30004
    [Google Scholar]
  11. 11. 
    de la Torre JG, Huertas ML, Carrasco B 2000. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 78:719–30
    [Google Scholar]
  12. 12. 
    Dey KK, Das S, Poyton MF, Sengupta S, Butler PJ 2014. Chemotactic separation of enzymes. ACS Nano 8:11941–49
    [Google Scholar]
  13. 13. 
    Dey KK, Sen A 2017. Chemically propelled molecules and machines. J. Am. Chem. Soc. 139:7666–76
    [Google Scholar]
  14. 14. 
    Elgeti J, Winkler RG, Gompper G 2015. Physics of microswimmers—single particle motion and collective behavior: a review. Rep. Prog. Phys. 78:056601
    [Google Scholar]
  15. 15. 
    Ey PL, Ferber E 1977. Calf thymus alkaline phosphatase: I. Properties of the membrane-bound enzyme. Biochim. Biophys. Acta Enzymol. 480:403–16
    [Google Scholar]
  16. 16. 
    Farago O, Grønbech-Jensen N 2014. Fluctuation–dissipation relation for systems with spatially varying friction. J. Stat. Phys. 156:1093–110
    [Google Scholar]
  17. 17. 
    Feng M, Gilson MK 2019. A thermodynamic limit on the role of self-propulsion in enhanced enzyme diffusion. Biophys. J. 116:1898–906
    [Google Scholar]
  18. 18. 
    Follmer C, Pereira FV, da Silveira NP, Carlini CR 2004. Jack bean urease (EC 3.5.1.5) aggregation monitored by dynamic and static light scattering. Biophys. Chem. 111:79–87
    [Google Scholar]
  19. 19. 
    Froede HC, Wilson IB 1984. Direct determination of acetyl-enzyme intermediate in the acetylcholinesterase-catalyzed hydrolysis of acetylcholine and acetylthiocholine. J. Biol. Chem. 259:11010–13
    [Google Scholar]
  20. 20. 
    Golestanian R 2015. Enhanced diffusion of enzymes that catalyze exothermic reactions. Phys. Rev. Lett. 115:108102
    [Google Scholar]
  21. 21. 
    Günther JP, Börsch M, Fischer P 2018. Diffusion measurements of swimming enzymes with fluorescence correlation spectroscopy. Acc. Chem. Res. 51:1911–20
    [Google Scholar]
  22. 22. 
    Günther JP, Majer G, Fischer P 2019. Absolute diffusion measurements of active enzyme solutions by NMR. J. Chem. Phys. 150:124201
    [Google Scholar]
  23. 23. 
    Iino R, Hasegawa R, Tabata KV, Noji H 2009. Mechanism of inhibition by C-terminal-helices of the subunit of Escherichia coli FoF1-ATP synthase. J. Biol. Chem. 284:17457–64
    [Google Scholar]
  24. 24. 
    Illien P, Adeleke-Larodo T, Golestanian R 2017. Diffusion of an enzyme: the role of fluctuation-induced hydrodynamic coupling. Europhys. Lett. 119:40002
    [Google Scholar]
  25. 25. 
    Illien P, Zhao X, Dey KK, Butler PJ, Sen A, Golestanian R 2017. Exothermicity is not a necessary condition for enhanced diffusion of enzymes. Nano Lett 17:4415–20
    [Google Scholar]
  26. 26. 
    Jee AY, Chen K, Tlusty T, Zhao J, Granick S 2019. Enhanced diffusion and oligomeric enzyme dissociation. J. Am. Chem. Soc 141:20062–68
    [Google Scholar]
  27. 27. 
    Jee AY, Cho YK, Granick S, Tlusty T 2018. Catalytic enzymes are active matter. PNAS 115:E10812–21
    [Google Scholar]
  28. 28. 
    Jee AY, Dutta S, Cho YK, Tlusty T, Granick S 2018. Enzyme leaps fuel antichemotaxis. PNAS 115:14–18
    [Google Scholar]
  29. 29. 
    Jiang L, Santiago I, Foord J 2017. Observation of nanoimpact events of catalase on diamond ultramicroelectrodes by direct electron transfer. Chem. Commun. 53:8332–35
    [Google Scholar]
  30. 30. 
    Khair AS 2013. Diffusiophoresis of colloidal particles in neutral solute gradients at finite Péclet number. J. Fluid Mech. 731:64–94
    [Google Scholar]
  31. 31. 
    Kondrat S, Popescu MN 2019. Brownian dynamics assessment of enhanced diffusion exhibited by fluctuating-dumbbell enzymes. Phys. Chem. Chem. Phys. 21:18811–15
    [Google Scholar]
  32. 32. 
    Landauer R 1983. Stability and relative stability in nonlinear driven systems. Helv. Phys. Acta 56:847–61
    [Google Scholar]
  33. 33. 
    Lauga E 2011. Enhanced diffusion by reciprocal swimming. Phys. Rev. Lett. 106:178101
    [Google Scholar]
  34. 34. 
    Lauga E 2011. Life around the scallop theorem. Soft Matter 7:3060–65
    [Google Scholar]
  35. 35. 
    Lauga E, Powers TR 2009. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72:096601
    [Google Scholar]
  36. 36. 
    Lee TC, Alarcón-Correa M, Miksch C, Hahn K, Gibbs JG, Fischer P 2014. Self-propelling nanomotors in the presence of strong Brownian forces. Nano Lett. 14:2407–12
    [Google Scholar]
  37. 37. 
    Lighthill MJ 1952. On the squirming motion of nearly spherical deformable bodies through liquids at very small Reynolds numbers. Commun. Pure Appl. Math. 5:109–18
    [Google Scholar]
  38. 38. 
    Lilie H, Bar D, Kettner K, Weininger U, Balbach J 2011. Yeast hexokinase isoenzyme ScHxk2: stability of a two-domain protein with discontinuous domains. Protein Eng. Des. Select. 24:79–87
    [Google Scholar]
  39. 39. 
    Martin CT, Coleman JE 1987. Kinetic analysis of T7 RNA polymerase-promoter interactions with small synthetic promoters. Biochemistry 26:2690–96
    [Google Scholar]
  40. 40. 
    Mikhailov AS, Kapral R 2015. Hydrodynamic collective effects of active protein machines in solution and lipid bilayers. PNAS 112:E3639–44
    [Google Scholar]
  41. 41. 
    Mohajerani F, Zhao X, Somasundar A, Velegol D, Sen A 2018. A theory of enzyme chemotaxis: from experiments to modeling. Biochemistry 57:6256–63
    [Google Scholar]
  42. 42. 
    Moran JL, Posner JD 2017. Phoretic self-propulsion. Annu. Rev. Fluid Mech. 49:511–40
    [Google Scholar]
  43. 43. 
    Muddana HS, Sengupta S, Mallouk TE, Sen A, Butler PJ 2010. Substrate catalysis enhances single-enzyme diffusion. J. Am. Chem. Soc. 132:2110–11
    [Google Scholar]
  44. 44. 
    Ortega A, Amorós D, García de la Torre J 2011. Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models. Biophys. J. 101:892–98
    [Google Scholar]
  45. 45. 
    Pantarotto D, Browne WR, Feringa BL 2008. Autonomous propulsion of carbon nanotubes powered by a multienzyme ensemble. Chem. Commun. 13:1533–35
    [Google Scholar]
  46. 46. 
    Riedel C, Gabizon R, Wilson CAM, Hamadani K, Tsekouras K 2014. The heat released during catalytic turnover enhances the diffusion of an enzyme. Nature 517:227–30
    [Google Scholar]
  47. 47. 
    Rieger F, Bon S, Massoulie J, Cartaud J, Benda P 1976. Torpedo marmorata acetylcholinesterase; a comparison with the Electrophorus electricus enzyme. Molecular forms, subunits, electron microscopy, immunological relationship. Eur. J. Biochem. 68:513–21
    [Google Scholar]
  48. 48. 
    Sabass B, Seifert U 2010. Efficiency of surface-driven motion: Nanoswimmers beat microswimmers. Phys. Rev. Lett. 105:218103
    [Google Scholar]
  49. 49. 
    Sabass B, Seifert U 2012. Dynamics and efficiency of a self-propelled, diffusiophoretic swimmer. J. Chem. Phys. 136:064508
    [Google Scholar]
  50. 50. 
    Sanchez S, Solovev AA, Mei Y, Schmidt OG 2010. Dynamics of biocatalytic microengines mediated by variable friction control. J. Am. Chem. Soc. 132:13144–45
    [Google Scholar]
  51. 51. 
    Santiago I 2018. Nanoscale active matter matters: challenges and opportunities for self-propelled nanomotors. Nano Today 19:11–15
    [Google Scholar]
  52. 52. 
    Schnitzer MJ, Block SM, Berg HC 1990. Strategies for chemotaxis. Biol. Chemotactic Response 46:15–34
    [Google Scholar]
  53. 53. 
    Schurr JM, Fujimoto BS, Huynh L, Chiu DT 2013. A theory of macromolecular chemotaxis. J. Phys. Chem. B 117:7626–52
    [Google Scholar]
  54. 54. 
    Sengupta S, Dey KK, Muddana HS, Tabouillot T, Ibele ME 2013. Enzyme molecules as nanomotors. J. Am. Chem. Soc. 135:1406–14
    [Google Scholar]
  55. 55. 
    Sengupta S, Spiering MM, Dey KK, Duan W, Patra D 2014. DNA polymerase as a molecular motor and pump. ACS Nano 8:2410–18
    [Google Scholar]
  56. 56. 
    Slochower DR, Gilson MK 2018. Motor-like properties of nonmotor enzymes. Biophys. J. 114:2174–79
    [Google Scholar]
  57. 57. 
    Sokolov I 2010. Ito, Stratonovich, Hnggi and all the rest: the thermodynamics of interpretation. Chem. Phys. 375:359–63
    [Google Scholar]
  58. 58. 
    Sousa R, Chung YJ, Rose JP, Wang BC 1993. Crystal structure of bacteriophage T7 RNA polymerase at 3.3 Å resolution. Nature 364:593–99
    [Google Scholar]
  59. 59. 
    Stone HA, Samuel AD 1996. Propulsion of microorganisms by surface distortions. Phys. Rev. Lett. 77:4102
    [Google Scholar]
  60. 60. 
    Tsekouras K, Riedel C, Gabizon R, Marqusee S, Pressé S, Bustamante C 2016. Comment on “Enhanced diffusion of enzymes that catalyze exothermic reactions” by R. Golestanian. arXiv:1608.05433 [physics.bio-ph]
    [Google Scholar]
  61. 61. 
    Tupper PF, Yang X 2012. A paradox of state-dependent diffusion and how to resolve it. Proc. R. Soc. A 468:3864–81
    [Google Scholar]
  62. 62. 
    Wang H 2005. Chemical and mechanical efficiencies of molecular motors and implications for motor mechanisms. J. Phys. Condens. Matt. 17:S3997–4014
    [Google Scholar]
  63. 63. 
    Wang H, Oster G 2002. Ratchets, power strokes, and molecular motors. Appl. Phys. A 75:315–23
    [Google Scholar]
  64. 64. 
    Wang H, Oster G 2002. The Stokes efficiency for molecular motors and its applications. Europhys. Lett. 57:134–40
    [Google Scholar]
  65. 65. 
    Weistuch C, Pressé S 2018. Spatiotemporal organization of catalysts driven by enhanced diffusion. J. Phys. Chem. B 122:5286–90
    [Google Scholar]
  66. 66. 
    Wheat PM 2011. Collective behavior of swimming bimetallic motors in chemical concentration gradients Ph.D. thesis, Arizona State Univ., Tempe
  67. 67. 
    Wilkinson PC 1998. Assays of leukocyte locomotion and chemotaxis. J. Immunol. Methods 216:139–53
    [Google Scholar]
  68. 68. 
    Woodfin BM 1967. Substrate-induced dissociation of rabbit muscle aldolase into active subunits. Biochem. Biophys. Res. Commun. 29:288–93
    [Google Scholar]
  69. 69. 
    Wu F, Pelster LN, Minteer SD 2015. Krebs cycle metabolon formation: Metabolite concentration gradient enhanced compartmentation of sequential enzymes. Chem. Commun. 51:1244–47
    [Google Scholar]
  70. 70. 
    Xu M, Ross JL, Valdez L, Sen A 2019. Direct single molecule imaging of enhanced enzyme diffusion. Phys. Rev. Lett. 123:128101
    [Google Scholar]
  71. 71. 
    Yu H, Jo K, Kounovsky KL, de Pablo JJ, Schwartz DC 2009. Molecular propulsion: chemical sensing and chemotaxis of DNA driven by RNA polymerase. J. Am. Chem. Soc. 131:5722–23
    [Google Scholar]
  72. 72. 
    Zhang Y, Armstrong MJ, Bassir Kazeruni NM, Hess H 2018. Aldolase does not show enhanced diffusion in dynamic light scattering experiments. Nano Lett. 18:8025–29
    [Google Scholar]
  73. 73. 
    Zhang Y, Hess H 2019. Enhanced diffusion of catalytically active enzymes. ACS Cent. Sci. 5:939–48
    [Google Scholar]
  74. 74. 
    Zhao X, Dey KK, Jeganathan S, Butler PJ, Córdova-Figueroa UM, Sen A 2017. Enhanced diffusion of passive tracers in active enzyme solutions. Nano Lett. 17:4807–12
    [Google Scholar]
  75. 75. 
    Zhao X, Palacci H, Yadav V, Spiering MM, Gilson MK 2017. Substrate-driven chemotactic assembly in an enzyme cascade. Nat. Chem. 10:311–17
    [Google Scholar]
  76. 76. 
    Zwanzig R 2001. Nonequilibrium Statistical Mechanics Oxford, UK: Oxford Univ. Press
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