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  • Review Article
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Reconstitution of FoF1-ATPase-based biomimetic systems

Nature Reviews Chemistry volume 3, pages 361–374 (2019)Cite this article

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Abstract

Nature makes use of molecular machines to perform intricate functions in every significant biological process and to power macroscopic motion in organisms. Biomolecular motor proteins perform crucial tasks such as cell division, intracellular transport and mechanical actuation in biological cells. The rotary motor FoF1-ATPase is one of the most extensively studied biomolecular machines as a result of its vital physiological function. Research on the function of FoF1-ATPase can help to better understand the underlying biological processes and may also result in the development of biological molecular motor-based devices or even inspire the creative design and construction of artificial molecular machines. Recent advances in nanoscience and biotechnology have enabled engineering experiments with FoF1-ATPase that have achieved notable success. In this Review, we first outline the reconstitution of FoF1-ATPase into simple liposomes and polymersomes and then focus on recent progress in the reconstitution of FoF1-ATPase on layer-by-layer-assembled systems. The elaborate structural designs utilized in layer-by-layer-assembled systems to better mimic natural cell structures are introduced. The rational integration of functional components to achieve stimuli-responsive ATP syntheses from FoF1-ATPase-based biomimetic systems is highlighted. Finally, we address some remaining key challenges and speculate on future directions for the field.

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Fig. 1: Synthetic and natural molecular machines.
Fig. 2: The rotary motion of F1-ATPase.
Fig. 3: Biomimetic assemblies of FoF1-ATPase on different artificial architectures.
Fig. 4: A variety of stimuli-responsive ATP syntheses.
Fig. 5: Design and dynamic control of the photosynthetic artificial organelle.
Fig. 6: Improvement of the photophosphorylation efficiency of natural chloroplast.

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References

  1. Browne, W. R. & Feringa, B. L. Making molecular machines work. Nat. Nanotechnol. 1, 25–35 (2006).

    CAS  PubMed  Google Scholar 

  2. Balzani, V., Gómez-López, M. & Stoddart, J. F. Molecular machines. Acc. Chem. Res. 31, 405–414 (1998).

    CAS  Google Scholar 

  3. Yurke, B., Turberfield, A. J., Mills, A. P. Jr, Simmel, F. C. & Neumann, J. L. ADNA-fuelled molecular machine made of DNA. Nature 406, 605–608 (2000).

    CAS  PubMed  Google Scholar 

  4. Hernández, J. V., Kay, E. R. & Leigh, D. A. A reversible synthetic rotary molecular motor. Science 306, 1532–1537 (2004).

    PubMed  Google Scholar 

  5. Eelkema, R. et al. Nanomotor rotates microscale objects. Nature 440, 163 (2006).

    CAS  Google Scholar 

  6. van Leeuwen, T., Lubbe, A. S., Stacko, P., Wezenberg, S. J. & Feringa, B. L. Dynamic control of function by light-driven molecular motors. Nat. Rev. Chem. 1, 0096 (2017).

    Google Scholar 

  7. Warshel, A. Multiscale modeling of biological functions: from enzymes to molecular machines (Nobel Lecture). Angew. Chem. Int. Ed. 53, 10020–10031 (2014).

    CAS  Google Scholar 

  8. Kinbara, K. & Aida, T. Toward intelligent molecular machines: directed motions of biological and artificial molecules and assemblies. Chem. Rev. 105, 1377–1400 (2005).

    CAS  PubMed  Google Scholar 

  9. Pezzato, C., Cheng, C., Stoddart, J. F. & Astumian, R. D. Mastering the non-equilibrium assembly and operation of molecular machines. Chem. Soc. Rev. 46, 5491–5507 (2017).

    CAS  PubMed  Google Scholar 

  10. Berna, J. et al. Macroscopic transport by synthetic molecular machines. Nat. Mater. 4, 704–710 (2005).

    CAS  PubMed  Google Scholar 

  11. Sauvage, J.-P. From chemical topology to molecular machines (Nobel Lecture). Angew. Chem. Int. Ed. 56, 11080–11093 (2017).

    CAS  Google Scholar 

  12. Forgan, R. S., Sauvage, J.-P. & Stoddart, J. F. Chemical topology: complex molecular knots, links, and entanglements. Chem. Rev. 111, 5434–5464 (2011).

    CAS  PubMed  Google Scholar 

  13. Feringa, B. L. The art of building small: from molecular switches to motors (Nobel Lecture). Angew. Chem. Int. Ed. 56, 11059–11078 (2017).

    Google Scholar 

  14. Stoddart, J. F. Mechanically interlocked molecules (MIM) — molecular shuttles, switches, and machines (NobelLecture). Angew. Chem. Int. Ed. 56, 11094–11125 (2017).

    CAS  Google Scholar 

  15. Guix, M., Mayorga-Martinez, C. C. & Merkoçi, A. Nano/micromotors in (bio)chemical science applications. Chem. Rev. 114, 6285–6322 (2014).

    CAS  PubMed  Google Scholar 

  16. Goel, A. & Vogel, V. Harnessing biological motors to engineer systems for nanoscale transport and assembly. Nat. Nanotechnol. 3, 465–475 (2008).

    CAS  PubMed  Google Scholar 

  17. van den Heuvel, M. G. L. & Dekker, C. Motor proteins at work for nanotechnology. Science 317, 333–336 (2007).

    PubMed  Google Scholar 

  18. Junge, W. & Müller, D. J. Seeing a molecular motor at work. Science 333, 704–705 (2011).

    CAS  PubMed  Google Scholar 

  19. Junge, W., Sielaff, H. & Engelbrecht, S. Torque generation and elastic power transmission in the rotary FoF1-ATPase. Nature 459, 364–370 (2009).

    CAS  PubMed  Google Scholar 

  20. Liu, H. et al. Control of a biomolecular motor-powered nanodevice with an engineered chemical switch. Nat. Mater. 1, 173–177 (2002).

    CAS  PubMed  Google Scholar 

  21. Boyer, P. D. The ATP synthase— a splendid molecular machine. Annu. Rev. Biochem. 66, 717–749 (1997).

    CAS  PubMed  Google Scholar 

  22. Boyer, P. D. Energy, life, and ATP (Nobel Lecture). Angew. Chem. Int. Ed. 37, 2297–2307 (1998).

    CAS  Google Scholar 

  23. Walker, J. E. ATP synthesis by rotary catalysis (Nobel Lecture). Angew. Chem. Int. Ed. 37, 2308–2319 (1998).

    CAS  Google Scholar 

  24. Skou, J. C. The identification of the sodium-potassium pump (Nobel Lecture). Angew. Chem. Int. Ed. 37, 2320–2328 (1998).

    CAS  Google Scholar 

  25. Bao, G. & Suresh, S. Cell and molecular mechanics of biological materials. Nat. Mater. 2, 715–725 (2003).

    CAS  PubMed  Google Scholar 

  26. Ueno, H., Suzuki, T., Kinosita, K. & Yoshida, M. ATP-driven stepwise rotation of FoF1-ATP synthase. Proc. Natl Acad. Sci. USA 102, 1333–1338 (2005).

    CAS  PubMed  Google Scholar 

  27. Abrahams, J. P., Leslie, A. G., Lutter, R. & Walker, J. E. Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621–628 (1994).

    CAS  PubMed  Google Scholar 

  28. Stock, D., Leslie, A. G. & Walker, J. E. Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700–1705 (1999).

    CAS  PubMed  Google Scholar 

  29. Junge, W. & Nelson, N. ATP synthase. Annu. Rev. Biochem. 84, 631–657 (2015).

    CAS  PubMed  Google Scholar 

  30. Uchihashi, T., Iino, R., Ando, T. & Noji, H. High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333, 755–758 (2011).

    CAS  PubMed  Google Scholar 

  31. Boyer, P. D. A perspective of the binding change mechanism for ATP synthesis. FASEB J. 3, 2164–2178 (1989).

    CAS  PubMed  Google Scholar 

  32. Li, J. et al. Direct measurement of single-molecule adenosine triphosphatase hydrolysis dynamics. ACS Nano 11, 12789–12795 (2017).

    CAS  PubMed  Google Scholar 

  33. Diez, M. et al. Proton-powered subunit rotation in single membrane-bound FoF1-ATP synthase. Nat. Struct. Mol. Biol. 11, 135–141 (2004).

    CAS  PubMed  Google Scholar 

  34. Noji, H., Yasuda, R., Yoshida, M. & Kinosita, K. Direct observation of the rotation of F1-ATPase. Nature 386, 299–302 (1997).

    CAS  PubMed  Google Scholar 

  35. Yasuda, R., Noji, H., Yoshida, M., Kinosita, K. & Itoh, H. Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature 410, 898–904 (2001).

    CAS  PubMed  Google Scholar 

  36. Nishizaka, T. et al. Chemomechanical coupling in F1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat. Struct. Mol. Biol. 11, 142–148 (2004).

    CAS  PubMed  Google Scholar 

  37. Shimabukuro, K. et al. Catalysis and rotation of F1 motor: cleavage of ATP at the catalytic site occurs in 1 ms before 40 degrees substep rotation. Proc. Natl Acad. Sci. USA 100, 14731–14736 (2003).

    CAS  PubMed  Google Scholar 

  38. Toyabe, S., Watanabe-Nakayama, T., Okamoto, T., Kudo, S. & Muneyuki, E. Thermodynamic efficiency and mechanochemical coupling of F1-ATPase. Proc. Natl Acad. Sci. USA 108, 17951–17956 (2011).

    CAS  PubMed  Google Scholar 

  39. Palanisami, A. & Okamoto, T. Torque-induced slip of the rotary motor F1-ATPase. Nano Lett. 10, 4146–4149 (2010).

    CAS  PubMed  Google Scholar 

  40. Soong, R. K. et al. Powering an inorganic nanodevice with a biomolecular motor. Science 290, 1555–1558 (2000).

    CAS  PubMed  Google Scholar 

  41. Suzuki, T., Tanaka, K., Wakabayashi, C., Saita, E.-i & Yoshida, M. Chemomechanical coupling of human mitochondrial F1-ATPase motor. Nat. Chem. Biol. 10, 930–936 (2014).

    CAS  PubMed  Google Scholar 

  42. York, J., Spetzler, D., Xiong, F. & Frasch, W. D. Single-molecule detection of DNA via sequence-specific links between F1-ATPase motors and gold nanorod sensors. Lab Chip 8, 415–419 (2008).

    CAS  PubMed  Google Scholar 

  43. Hayashi, S. et al. Molecular mechanism of ATP hydrolysis in F1-ATPase revealed by molecular simulations and single-molecule observations. J. Am. Chem. Soc. 134, 8447–8454 (2012).

    CAS  PubMed  Google Scholar 

  44. Itoh, H. et al. Mechanically driven ATP synthesis by F1-ATPase. Nature 427, 465–468 (2004).

    CAS  PubMed  Google Scholar 

  45. Rondelez, Y. et al. Highly coupled ATP synthesis by F1-ATPase single molecules. Nature 433, 773–777 (2005).

    CAS  PubMed  Google Scholar 

  46. Walde, P. & Ichikawa, S. Enzymes inside lipid vesicles: preparation, reactivity and applications. Biomol. Eng. 18, 143–177 (2001).

    CAS  PubMed  Google Scholar 

  47. Racker, E. & Stoeckenius, W. Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. J. Biol. Chem. 249, 662–663 (1974).

    CAS  PubMed  Google Scholar 

  48. Richard, P., Rigaud, J. L. & Gräber, P. Reconstitution of CFoF1 into liposomes using a new reconstitution procedure. Eur. J. Biochem. 193, 921–925 (1990).

    CAS  PubMed  Google Scholar 

  49. Pitard, B., Richard, P., Dunach, M., Girault, G. & Rigaud, J. L. ATP synthesis by the FoF1 ATP synthase from thermophilic Bacillus ps3 reconstituted into liposomes with bacteriorhodopsin.1. Factors defining the optimal reconstitution of ATP synthases with bacteriorhodopsin. Eur. J. Biochem. 235, 769–778 (1996).

    CAS  PubMed  Google Scholar 

  50. Rideau, E., Dimova, R., Schwille, P., Wurm, F. R. & Landfester, K. Liposomes and polymersomes: a comparative review towards cell mimicking. Chem. Soc. Rev. 47, 8572–8610 (2018).

    CAS  PubMed  Google Scholar 

  51. Marguet, M., Bonduelle, C. & Lecommandoux, S. Multicompartmentalized polymeric systems: towards biomimetic cellular structure and function. Chem. Soc. Rev. 42, 512–529 (2013).

    CAS  PubMed  Google Scholar 

  52. Choi, H.-J. & Montemagno, C. D. Artificial organelle: ATP synthesis from cellular mimetic polymersomes. Nano Lett. 5, 2538–2542 (2005).

    CAS  PubMed  Google Scholar 

  53. Choi, H.-J. & Montemagno, C. D. Biosynthesis within a bubble architecture. Nanotechnology 17, 2198–2202 (2006).

    CAS  Google Scholar 

  54. Beales, P. A., Khan, S., Muench, S. P. & Jeuken, L. J. C. Durable vesicles for reconstitution of membrane proteins in biotechnology. Biochem. Soc. Trans. 45, 15–26 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Barrera, N. P., Zhou, M. & Robinson, C. V. The role of lipids in defining membrane protein interactions: insights from mass spectrometry. Trends Cell Biol. 23, 1–8 (2013).

    CAS  PubMed  Google Scholar 

  56. Seneviratne, R. et al. A reconstitution method for integral membrane proteins in hybrid lipid-polymer vesicles for enhanced functional durability. Methods 147, 142–149 (2018).

    CAS  PubMed  Google Scholar 

  57. Matsusaki, M., Ajiro, H., Kida, T., Serizawa, T. & Akashi, M. Layer-by-layer assembly through weak interactions and their biomedical applications. Adv. Mater. 24, 454–474 (2012).

    CAS  PubMed  Google Scholar 

  58. De Cock, L. J. et al. Polymeric multilayer capsules in drug delivery. Angew. Chem. Int. Ed. 49, 6954–6973 (2010).

    Google Scholar 

  59. Jia, Y. & Li, J. Molecular assembly of Schiff base interactions: construction and application. Chem. Rev. 115, 1597–1621 (2015).

    CAS  PubMed  Google Scholar 

  60. Wang, H., Ishihara, S., Ariga, K. & Yamauchi, Y. All-metal layer-by-layer films: bimetallic alternate layers with accessible mesopores for enhanced electrocatalysis. J. Am. Chem. Soc. 134, 10819–10821 (2012).

    CAS  PubMed  Google Scholar 

  61. Ariga, K., Lvov, Y. M., Kawakami, K., Ji, Q. & Hill, J. P. Layer-by-layer self-assembled shells for drug delivery. Adv. Drug Deliv. Rev. 63, 762–771 (2011).

    CAS  PubMed  Google Scholar 

  62. Ariga, K., Li, J., Fei, J., Ji, Q. & Hill, J. P. Nanoarchitectonics for dynamic functional materials from atomic-/molecular-level manipulation to macroscopic action. Adv. Mater. 28, 1251–1286 (2016).

    CAS  PubMed  Google Scholar 

  63. Cui, W., Li, J. & Decher, G. Self-assembled smart nanocarriers for targeted drug delivery. Adv. Mater. 28, 1302–1311 (2016).

    CAS  PubMed  Google Scholar 

  64. Jia, Y., Duan, L. & Li, J. Hemoglobin-based nanoarchitectonic assemblies as oxygen carriers. Adv. Mater. 28, 1312–1318 (2016).

    CAS  PubMed  Google Scholar 

  65. He, Q., Cui, Y. & Li, J. Molecular assembly and application of biomimetic microcapsules. Chem. Soc. Rev. 38, 2292–2303 (2009).

    CAS  PubMed  Google Scholar 

  66. Shao, J. et al. Near-infrared-activated nanocalorifiers in microcapsules: vapor bubble generation for in vivo enhanced cancer therapy. Angew. Chem. Int. Ed. 54, 12782–12787 (2015).

    CAS  Google Scholar 

  67. Yang, Y., Liu, H., Han, M., Sun, B. & Li, J. Multilayer microcapsules for fret analysis and two-photon-activated photodynamic therapy. Angew. Chem. Int. Ed. 55, 13538–13543 (2016).

    CAS  Google Scholar 

  68. Xuan, M. et al. Magnetic mesoporous silica nanoparticles cloaked by red blood cell membranes: applications in cancer therapy. Angew. Chem. Int. Ed. 57, 6049–6053 (2018).

    CAS  Google Scholar 

  69. Duan, L. et al. Adenosine triphosphate biosynthesis catalyzed by FoF1 ATP synthase assembled in polymer microcapsules. Angew. Chem. Int. Ed. 46, 6996–7000 (2007).

    CAS  Google Scholar 

  70. Miller, M. D. & Bruening, M. L. Correlation of the swelling and permeability of polyelectrolyte multilayer films. Chem. Mater. 17, 5375–5381 (2005).

    CAS  Google Scholar 

  71. An, Z. H., Möhwald, H. & Li, J. B. pH controlled permeability of lipid/protein biomimetic microcapsules. Biomacromolecules 7, 580–585 (2006).

    CAS  PubMed  Google Scholar 

  72. Duan, L. et al. Proton gradients produced by glucose oxidase microcapsules containing motor FoF1-ATPase for continuous ATP biosynthesis. J. Phys. Chem. B113, 395–399 (2008).

    Google Scholar 

  73. Feng, X., Jia, Y., Cai, P., Fei, J. & Li, J. Coassembly of photosystem II and ATPase as artificial chloroplast for light-driven ATP synthesis. ACS Nano 10, 556–561 (2016).

    CAS  PubMed  Google Scholar 

  74. Köper, I. & Vockenroth, I. in Surface Design: Applications in Bioscience and Nanotechnology (eds Förch, R., Schönherr, H. & Jenkins, A. T. A.)221–232 (John Wiley & Sons, 2009).

  75. Tanaka, M. & Sackmann, E. Polymer-supported membranes as models of the cell surface. Nature 437, 656–663 (2005).

    CAS  PubMed  Google Scholar 

  76. Naumann, R. et al. Incorporation of membrane proteins in solid-supported lipid layers. Angew. Chem. Int. Ed. 34, 2056–2058 (1995).

    CAS  Google Scholar 

  77. Naumann, R. et al. Proton transport through a peptide-tethered bilayer lipid membrane by the H+-ATP synthase from chloroplasts measured by impedance spectroscopy. Biosens. Bioelectron. 17, 25–34 (2002).

    CAS  PubMed  Google Scholar 

  78. Naumann, R. et al. Coupling of proton translocation through ATPase incorporated into supported lipid bilayers to an electrochemical process. Bioelectrochem. Bioenerg. 42, 241–247 (1997).

    CAS  Google Scholar 

  79. Li, G., Fei, J., Xu, Y., Li, Y. & Li, J. Bioinspired assembly of hierarchical light-harvesting architectures for improved photophosphorylation. Adv. Funct. Mater. 28, 1706557 (2018).

    Google Scholar 

  80. Li, Y. et al. Supramolecular assembly of photosystem II and adenosine triphosphate synthase in artificially designed honeycomb multilayers for photophosphorylation. ACS Nano 12, 1455–1461 (2018).

    CAS  PubMed  Google Scholar 

  81. Xu, Y., Fei, J., Li, G., Yuan, T. & Li, J. Compartmentalized assembly of motor protein reconstituted on protocell membrane toward highly efficient photophosphorylation. ACS Nano 11, 10175–10183 (2017).

    CAS  PubMed  Google Scholar 

  82. Bunz, U. H. F. Breath figures as a dynamic templating method for polymers and nanomaterials. Adv. Mater. 18, 973–989 (2006).

    CAS  Google Scholar 

  83. Turina, P., Samoray, D. & Gräber, P. H+/ATP ratio of proton transport-coupled ATP synthesis and hydrolysis catalysed by CFoF1—liposomes. EMBO J. 22, 418–426 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Qi, W. et al. Motor protein CFoF1 reconstituted in lipid-coated hemoglobin microcapsules for ATP synthesis. Adv. Mater. 20, 601–605 (2008).

    CAS  Google Scholar 

  85. Li, J. H. et al. Cyclodextrin-based microcapsules as bioreactors for ATP biosynthesis. Biomacromolecules 14, 2984–2988 (2013).

    CAS  PubMed  Google Scholar 

  86. Otrin, L. et al. Toward artificial mitochondrion: mimicking oxidative phosphorylation in polymer and hybrid membranes. Nano Lett. 17, 6816–6821 (2017).

    CAS  PubMed  Google Scholar 

  87. Qi, W., Duan, L. & Li, J. B. Fabrication of glucose-sensitive protein microcapsules and their applications. Soft Matter 7, 1571–1576 (2011).

    CAS  Google Scholar 

  88. Qi, W. et al. Triggered release of insulin from glucose-sensitive enzyme multilayer shells. Biomaterials 30, 2799–2806 (2009).

    CAS  PubMed  Google Scholar 

  89. Babcock, G. T. & Wikström, M. Oxygen activation and the conservation of energy in cell respiration. Nature 356, 301–309 (1992).

    CAS  PubMed  Google Scholar 

  90. Richard, P., Pitard, B. & Rigaud, J.-L. ATP synthesis by the FoF1-ATPase from the thermophilic Bacillus ps3 co-reconstituted with bacteriorhodopsin into liposomes evidence for stimulation of ATP synthesis by ATP bound to a noncatalytic binding site. J. Biol. Chem. 270, 21571–21578 (1995).

    CAS  PubMed  Google Scholar 

  91. Pitard, B., Richard, P., Dunach, M. & Rigaud, J. L. ATP synthesis by the FoF1 ATP synthase from thermophilic Bacillus ps3 reconstituted into liposomes with bacteriorhodopsin.2. Relationships between proton motive force and ATP synthesis. Eur. J. Biochem. 235, 779–788 (1996).

    CAS  PubMed  Google Scholar 

  92. Luo, T.-J. M., Soong, R., Lan, E., Dunn, B. & Montemagno, C. Photo-induced proton gradients and ATP biosynthesis produced by vesicles encapsulated in a silica matrix. Nat. Mater. 4, 220–224 (2005).

    CAS  PubMed  Google Scholar 

  93. Wendell, D., Todd, J. & Montemagno, C. Artificial photosynthesis in ranaspumin-2 based foam. Nano Lett. 10, 3231–3236 (2010).

    CAS  PubMed  Google Scholar 

  94. Wang, W., Chen, J., Li, C. & Tian, W. Achieving solar overall water splitting with hybrid photosystems of photosystem II and artificial photocatalysts. Nat. Commun. 5, 4647 (2014).

    CAS  PubMed  Google Scholar 

  95. Kato, M., Zhang, J. Z., Paul, N. & Reisner, E. Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem. Soc. Rev. 43, 6485–6497 (2014).

    CAS  PubMed  Google Scholar 

  96. Cai, P. et al. Co-assembly of photosystem II/reduced graphene oxide multilayered biohybrid films for enhanced photocurrent. Nanoscale 7, 10908–10911 (2015).

    CAS  PubMed  Google Scholar 

  97. Li, Z. et al. Biomimetic electron transport via multiredox shuttles from photosystem II to a photoelectrochemical cell for solar water splitting. Energy Environ. Sci. 10, 765–771 (2017).

    CAS  Google Scholar 

  98. Wang, W. Y. et al. Spatially separated photosystem II and a silicon photoelectrochemical cell for overall water splitting: a natural-artificial photosynthetic hybrid. Angew. Chem. Int. Ed. 55, 9229–9233 (2016).

    CAS  Google Scholar 

  99. Ritzmann, N. et al. Fusion domains guide the oriented insertion of light-driven proton pumps into liposomes. Biophys. J. 113, 1181–1186 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Goers, R. et al. Optimized reconstitution of membrane proteins into synthetic membranes. Commun. Chem. 1, 35 (2018).

    Google Scholar 

  101. Harder, D. et al. Engineering a chemical switch into the light-driven proton pump proteorhodopsin by cysteine mutagenesis and thiol modification. Angew. Chem. Int. Ed. 55, 8846–8849 (2016).

    CAS  Google Scholar 

  102. Lee, K. Y. et al. Photosynthetic artificial organelles sustain and control ATP-dependent reactions in a protocellular system. Nat. Biotechnol. 36, 530–535 (2018).

    CAS  PubMed  Google Scholar 

  103. Xu, Y. et al. Enhanced photophosphorylation of a chloroplast-entrapping long-lived photoacid. Angew. Chem. Int. Ed. 56, 12903–12907 (2017).

    CAS  Google Scholar 

  104. Xu, Y. et al. Optically matched semiconductor quantum dots improve photophosphorylation performed by chloroplasts. Angew. Chem. Int. Ed. 57, 6532–6535 (2018).

    CAS  Google Scholar 

  105. Steinberg-Yfrach, G. et al. Conversion of light energy to proton potential in liposomes by artificial photosynthetic reaction centres. Nature 385, 239–241 (1997).

    CAS  Google Scholar 

  106. Steinberg-Yfrach, G. et al. Light-driven production of ATP catalysed by FoF1-ATP synthase in an artificial photosynthetic membrane. Nature 392, 479–482 (1998).

    CAS  PubMed  Google Scholar 

  107. Gust, D., Moore, T. A. & Moore, A. L. Mimicking photosynthetic solar energy transduction. Acc. Chem. Res. 34, 40–48 (2001).

    CAS  PubMed  Google Scholar 

  108. Rögner, M., Ohno, K., Hamamoto, T., Sone, N. & Kagawa, Y. Net ATP synthesis in H+-ATPase macroliposomes by an external electric field. Biochem. Biophys. Res. Commun. 91, 362–367 (1979).

    PubMed  Google Scholar 

  109. Hamamoto, T., Ohno, K. & Kagawa, Y. Net adenosine triphosphate synthesis driven by an external electric field in rat liver mitochondria. J. Biochem. 91, 1759–1766 (1982).

    CAS  PubMed  Google Scholar 

  110. Vinkler, C. & Korenstein, R. Characterization of external electric field-driven ATP synthesis in chloroplasts. Proc. Natl Acad. Sci. USA 79, 3183–3187 (1982).

    CAS  PubMed  Google Scholar 

  111. Gutierrez-Sanz, O. et al. H2-fueled ATP synthesis on an electrode: mimicking cellular respiration. Angew. Chem. Int. Ed. 55, 6216–6220 (2016).

    CAS  Google Scholar 

  112. Adachi, K., Oiwa, K., Yoshida, M., Nishizaka, T. & Kinosita, K. Jr. Controlled rotation of the F1-ATPase reveals differential and continuous binding changes for ATP synthesis. Nat. Commun. 3, 1022 (2012).

    PubMed  PubMed Central  Google Scholar 

  113. Hirono-Hara, Y., Ishuzuka, K., Kinosita, K., Yoshida, M. & Noji, H. Activation of pausing F1 motor by external force. Proc. Natl Acad. Sci. USA 102, 4288–4293 (2005).

    CAS  PubMed  Google Scholar 

  114. Saita, E.-i, Suzuki, T., Kinosita, K. Jr & Yoshida, M. Simple mechanism whereby the F1-ATPase motor rotates with near-perfect chemomechanical energy conversion. Proc. Natl Acad. Sci. USA 112, 9626–9631 (2015).

    CAS  PubMed  Google Scholar 

  115. Daum, B., Nicastro, D., Austin, J., McIntosh, J. R. & Kühlbrandt, W. Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22, 1299–1312 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Daum, B., Walter, A., Horst, A., Osiewacz, H. D. & Kühlbrandt, W. Age-dependent dissociation of ATP synthase dimers and loss of inner-membrane cristae in mitochondria. Proc. Natl Acad. Sci. USA 110, 15301–15306 (2013).

    CAS  PubMed  Google Scholar 

  117. Hahn, A. et al. Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology. Mol. Cell 63, 445–456 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Tunuguntla, R. et al. Lipid bilayer composition can influence the orientation of proteorhodopsin in artificial membranes. Biophys. J. 105, 1388–1396 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Barrera, N. P. et al. Mass spectrometry of membrane transporters reveals subunit stoichiometry and interactions. Nat. Methods 6, 585–587 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Schmidt, C. et al. Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation. Nat. Commun. 4, 1985 (2013).

    PubMed  PubMed Central  Google Scholar 

  121. Zhou, M. et al. Mass spectrometry of intact V-type ATPases reveals bound lipids and the effects of nucleotide binding. Science 334, 380–385 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Zhou, M. et al. Ion mobility-mass spectrometry of a rotary ATPase reveals ATP-induced reduction in conformational flexibility. Nat. Chem. 6, 208–215 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Jia, Y., Dong, W., Feng, X., Li, J. & Li, J. A self-powered kinesin-microtubule system for smart cargo delivery. Nanoscale 7, 82–85 (2015).

    CAS  PubMed  Google Scholar 

  124. Li, J. et al. Transporting a tube in a tube. Nano Lett. 14, 6160–6164 (2014).

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge financial support from the National Natural Science Foundation of China (project nos 21433010, 21872151 and 21320102004).

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Authors and Affiliations

  1. Beijing National Laboratory for Molecular Sciences, CAS Key Laboratory of Colloid, Interface and Chemical Thermodynamics, Institute of Chemistry, Chinese Academy of Sciences, Beijing, China

    Yi Jia & Junbai Li

  2. University of Chinese Academy of Sciences, Beijing, China

    Junbai Li

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  1. Yi Jia
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  2. Junbai Li
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Both authors contributed to all stages of manuscript research, writing and editing.

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Correspondence to Junbai Li.

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Jia, Y., Li, J. Reconstitution of FoF1-ATPase-based biomimetic systems. Nat Rev Chem 3, 361–374 (2019). https://doi.org/10.1038/s41570-019-0100-8

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