Issues

 / 

2010

 / 

September

  

Reviews of topical problems


Molecular energy transducers of the living cell. Proton ATP synthase: a rotating molecular motor

,
Lomonosov Moscow State University, Department of Physics, Leninskie Gory 1 build. 2, Moscow, 119991, Russian Federation

The free energy released upon the enzymatic hydrolysis of adenosine triphosphate (ATP) is the main source of energy for the functioning of the living cell and all multicellular organisms. The overwhelming majority of ATP molecules are formed by proton ATP synthases, which are the smallest macromolecular electric motors in Nature. This paper reviews the modern concepts of the molecular structure and functioning of the proton ATP synthase, and real-time biophysical experiments on the rotation of the ’rotor’ of this macromolecular motor. Some mathematical models describing the operation of this nanosized macromolecular machine are described.

Fulltext is available at IOP
PACS: 87.10.−e, 87.15.−v, 87.16.−b (all)
DOI: 10.3367/UFNe.0180.201009b.0931
URL: https://ufn.ru/en/articles/2010/9/b/
Citation: Romanovsky Yu M, Tikhonov A N "Molecular energy transducers of the living cell. Proton ATP synthase: a rotating molecular motor" Phys. Usp. 53 893–914 (2010)
BibTexBibNote ® (generic)BibNote ® (RIS)MedlineRefWorks

Оригинал: Романовский Ю М, Тихонов А Н «Молекулярные преобразователи энергии живой клетки. Протонная АТФ-синтаза — вращающийся молекулярный мотор» УФН 180 931–956 (2010); DOI: 10.3367/UFNr.0180.201009b.0931

References (142) ↓ Cited by (37) Similar articles (20)

  1. Blyumenfel’d L A Problemy Biologicheskoi Fiziki (M.: Nauka, 1974); Blumenfeld L A Problems Of Biological Physics (Heidelberg: Springer-Verlag, 1981)
  2. Blumenfeld L A, Tikhonov A N Biophysical Thermodynamics Of Intracellular Processes: Molecular Machines Of The Living Cell (New-York: Springer-Verlag, 1994)
  3. Chernavskii D S, Chernavskaya N M Belok-mashina: Biologicheskie Makromolekulyarnye Konstruktsii (M.: Yanus-K, 1999)
  4. Chernavskii D S, Khurgin Yu I, Shnol’ S E Mol. Biol. 1 419 (1967)
  5. Romanovskii Yu M, Ebeling V (Red.) Molekulyarnaya Dinamika Fermentov (M.: Izd-vo Moskovskogo universiteta, 2000)
  6. Rubin A B Biofizika Vol. 1, 2 (M.: Izd-vo Moskovskogo universiteta, 2004)
  7. Asbury C L Curr. Opin. Cell Biol. 17 89 (2005)
  8. Carter N J, Cross R A Curr. Opin. Cell Biol. 18 61 (2006)
  9. Westermann S, Drubin D G, Barnes G Annu. Rev. Biochem. 76 563 (2007)
  10. Borgia A, Williams P M, Clarke J Annu. Rev. Biochem. 77 101 (2008)
  11. Marshall R A et al. Annu. Rev. Biochem. 77 177 (2008)
  12. Joo Ch et al. Annu. Rev. Biochem. 77 51 (2008)
  13. Herbert K M, Greenleaf W J, Block S M Annu. Rev. Biochem. 77 149 (2008)
  14. Hamdan S M, Richardson C C Annu. Rev. Biochem. 78 205 (2009)
  15. Gennerich A, Vale R D Curr. Opin. Cell Biol. 21 59 (2009)
  16. Moffitt J R et al. Annu. Rev. Biochem. 77 205 (2008)
  17. Block S M, Goldstein L S, Schnapp B J Nature 348 348 (1990)
  18. Svoboda K et al. Nature 365 721 (1993)
  19. Finer J T, Simmons R M, Spudich J A Nature 368 113 (1994)
  20. Vale R D Cell 112 467 (2003)
  21. Howard J, Hudspeth A J, Vale R D Nature 342 154 (1989)
  22. Rice S et al. Nature 402 778 (1999)
  23. Yildiz A et al. Science 303 676 (2004)
  24. Kon T et al. Nature Struct. Mol. Biol. 12 513 (2005)
  25. Grishchuk E L et al. Nature 438 384 (2005)
  26. McIntosh J et al. Cell 135 322 (2008)
  27. Block S M Biophys. J. 92 2986 (2007)
  28. Shiroguchi K, Kinosita K (Jr.) Science 316 1208 (2007)
  29. Ebeling W, Schimansky-Gaier L, Romanovsky Yu M Stochastic Dynamics Of Reacting Biomolecules (River Edgee, N.J.: World Scientific, 2002)
  30. Shaitan K V Stochastic Dynamics Of Reacting Biomolecules (River Edgee, N.J.: World Scientific, 2002) p. 285
  31. Oster G, Wang H Biochim. Biophys. Acta (BBA) — Bioenergetics 1458 482 (2000)
  32. Oster G, Wang H Trends Cell Biol. 13 114 (2003)
  33. Keller D, Bustamante C Biophys. J. 78 541 (2000)
  34. Bustamante C, Keller D, Oster G Acc. Chem. Res. 34 412 (2001)
  35. Xing J et al. Proc. Natl. Acad. Sci. USA 103 1260 (2006)
  36. Boyer P D Biochim. Biophys. Acta (BBA) — Bioenergetics 1140 215 (1993)
  37. Boyer P D Annu. Rev. Biochem. 66 717 (1997)
  38. Junge W, Lill H, Engelbrecht S Trends Biochem. Sci. 22 420 (1997)
  39. Stock D et al. Curr. Opin. Struct. Biol. 10 672 (2000)
  40. Walker J (Ed.) Biochim. Biophys. Acta 1458 (2-3) (2000), Special Issue, Guest
  41. Walker J (Ed.) J. Bioenerg. Biomembr. 32 (4-5) (2000), Minireview Series, ATP Synthesis in the Year 2000: Current Views about Structure, Motor Components, Energy Interconversions and Catalytic Mechanisms, Pt. 1, 2
  42. Harvey W R, Boutilier R G, Nelson N (Eds) J. Exp. Biol. 203 (1) (2000), Special issue
  43. Capaldi R A, Aggeler R Trends Biochem. Sci. 27 154 (2002)
  44. Von Ballmoos C, Wiedenmann A, Dimroth P Annu. Rev. Biochem. 78 649 (2009)
  45. Von Ballmoos C, Cook G M, Dimroth P Annu. Rev. Biophys. 37 43 (2008)
  46. Mitchell P Theor. Exp. Biophys. 2 159 (1969)
  47. Skulachev V P Membrane Bioenergetics (New York: Springer-Verlag, 1988)
  48. Nicholls D G, Ferguson S J Bioenergetics 3 (San Diego, Calif.: Academic Press, 2002)
  49. Nelson D L, Cox M M Lehninger Principles Of Biochemistry 4th ed. (New York: W.H. Freeman, 2005)
  50. Alberty R A J. Biol. Chem. 244 3290 (1969)
  51. Gräber P Curr. Topics Membr. Transp. 16 215 (1982)
  52. Kramer D M, Sacksteder C A, Cruz J A Photosynth. Res. 60 151 (1999)
  53. Trubitsin B V, Tikhonov A N J. Magn. Res. 163 257 (2003)
  54. Tikhonov A N et al. Biochim. Biophys. Acta 1777 285 (2008)
  55. Abrahams J P et al. Nature 370 621 (1994)
  56. Leslie A G W, Walker J E Philos. Trans. R. Soc. Lond. B 355 465 (2000)
  57. Groth G, Pohl E J. Biol. Chem. 276 1345 (2001)
  58. Seelert H et al. Nature 405 418 (2000)
  59. Stock D, Leslie A G W, Walker J E Science 286 1700 (1999)
  60. Menz R I, Walker J E, Leslie A G Cell 106 331 (2001)
  61. Kabaleeswaran V et al. EMBO J. 25 5433 (2006)
  62. Oster G, Wang H Encyclopedia Of Molecular Biology (Ed. T Creighton) (New York: Wiley, 1999) p. 211
  63. Shirakihara Y et al. Structure 5 825 (1997)
  64. Grubmeyer C, Cross R L, Penefsky H S J. Biol. Chem. 257 12092 (1982)
  65. Cunningham D, Cross R L J. Biol. Chem. 263 18850 (1988)
  66. Senior A E J. Bioenerg. Biomem. 24 479 (1992)
  67. Milgrom Y M, Murataliev M B, Boyer P D Biochem. J. 330 1037 (1998)
  68. Penefsky H S, Cross R L Adv. Enzymol. Relat. Areas Mol. Biol. 64 173 (1991)
  69. Antes D et al. Biophys. J. 85 695 (2003)
  70. Sun S et al. Eur. Biophys. J. 32 676 (2003)
  71. Vinogradov A D J. Exp. Biol. 203 41 (2000)
  72. Duncan T M et al. Proc. Natl. Acad. Sci. USA 92 10964 (1995)
  73. Zhou Y et al. Biochim. Biophys. Acta (BBA) — Bioenergetics 1275 96 (1996)
  74. Zhou Y, Duncan T M, Cross R L Proc. Natl. Acad. Sci. USA 94 10583 (1997)
  75. Sabbert D, Engelbrecht S, Junge W Nature 381 623 (1996)
  76. Sabbert D, Engelbrecht S, Junge W Proc. Natl. Acad. Sci. USA 94 4401 (1997)
  77. Häsler K, Engelbrecht S, Junge W FEBS Lett. 426 301 (1998)
  78. Noji H et al. Nature 386 299 (1997)
  79. Yasuda R et al. Cell 93 1117 (1998)
  80. Kinosita K et al. Philos. Trans. R. Soc. Lond. B 355 473 (2000)
  81. Sambongi Y et al. Science 286 1722 (1999)
  82. Tanabe M et al. J. Biol. Chem. 276 15269 (2001)
  83. Yasuda R et al. Nature 410 898 (2001)
  84. Shimabukuro K et al. Proc. Natl. Acad. Sci. USA 100 14731 (2003)
  85. Nishizaka T et al. Nature Struct. Mol. Biol. 11 142 (2004)
  86. Kinosita K, Adachi K, Itoh H Annu. Rev. Biophys. Biomol. Struct. 33 245 (2004)
  87. Ueno H et al. Proc. Natl. Acad. Sci. USA 102 1333 (2005)
  88. Sakaki N et al. Biophys. J. 88 2047 (2005)
  89. Adachi K et al. Cell 130 309 (2007)
  90. Boyer P D FEBS Lett. 512 29 (2002)
  91. Weber J, Senior A E Biochim. Biophys. Acta (BBA) — Bioenergetics 1319 19 (1997)
  92. Weber J, Senior A E Biochim. Biophys. Acta (BBA) — Bioenergetics 1458 300 (2000)
  93. Senior A, Nadanaciva S, Weber J Biochim. Biophys. Acta (BBA) — Bioenergetics 1553 188 (2002)
  94. Weber J, Senior A E J. Biol. Chem. 276 35422 (2001)
  95. Itoh H et al. Nature 427 465 (2004)
  96. Yasuda R et al. Proc. Natl. Acad. Sci. USA 100 9314 (2003)
  97. Diez M et al. Nature Struct. Mol. Biol. 11 135 (2004)
  98. Ma J et al. Structure 10 921 (2002)
  99. Furuike S et al. Science 319 955 (2008)
  100. Hossain M D et al. Biophys. J. 95 4837 (2008)
  101. Suzuki T et al. J. Biol. Chem. 277 13281 (2002)
  102. Elston T, Wang H, Oster G Nature 391 510 (1998)
  103. Wang H, Oster G Nature 396 279 (1998)
  104. Grabe M , Wang H, Oster G Biophys. J. 78 2798 (2000)
  105. Wang H, Oster G Europhys. Lett. 57 134 (2002)
  106. Jain S, Nath S FEBS Lett. 476 113 (2000)
  107. Sun S X, Wang H, Oster G Biophys. J. 86 1373 (2004)
  108. Dittrich M, Hayashi S, Schulten K Biophys. J. 85 2253 (2003)
  109. Böckmann R A, Grubmüller H Nature Struct. Biol. 9 198 (2002)
  110. Böckmann R A , Grubmüller H Biophys. J. 85 1482 (2003)
  111. Yang W et al. Proc. Natl. Acad. Sci. USA 100 874 (2003)
  112. Strajbl M, Shurki A, Warshel A Proc. Natl. Acad. Sci. USA 100 14834 (2003)
  113. Gao Y Q et al. Proc. Natl. Acad. Sci. USA 100 11339 (2003)
  114. Romanovskii Yu M, Kargovskii A V Nelineinye Volny 2008 (Pod red. A V Gaponova, V I Nekorkina) (N. Novgorod: IPF RAN, 2009) p. 223
  115. Nartsissov Ya R, Mashkovtseva E V Biofizika 50 1048 (2005); Nartsissov Ya R, Mashkovtseva E V Biophysics 50 905 (2005)
  116. Nartsissov Y R, Mashkovtseva E V J. Theor. Biol. 242 300 (2006)
  117. Pänke O, Rumberg B Biochim. Biophys. Acta (BBA) — Bioenergetics 1412 118 (1999)
  118. Cherepanov D A, Mulkidjanian A Y, Junge W FEBS Lett. 449 1 (1999)
  119. Pänke O et al. Biophys. J. 81 1220 (2001)
  120. Rastogi V K, Girvin M V Nature 402 263 (1999)
  121. Fillingame R H et al. Biochim. Biophys. Acta (BBA) — Bioenergetics 1458 387 (2000)
  122. Fillingame R H, Angevine C M, Dmitriev O Y Biochim. Biophys. Acta (BBA) — Bioenergetics 1555 29 (2002)
  123. Fillingame R H, Dmitriev O Y Biochim. Biophys. Acta (BBA) — Bioenergetics 1565 232 (2002)
  124. Xing J, Wang H, Oster G Biophys. J. 89 1551 (2005)
  125. Xing J et al. Biophys. J. 87 2148 (2004)
  126. Xing J, Liao J-C, Oster G Proc. Natl. Acad. Sci. USA 102 16539 (2005)
  127. Tikhonov A N, Pogrebnaya A F, Romanovskii Yu M Biofizika 48 1052 (2003); Tikhonov A N, Pogrebnaya A F, Romanovsky Yu M Biophysics 48 970 (2003)
  128. Pogrebnaya A F, Romanovsky Y M, Tikhonov A N Proc. SPIE 5068 27 (2003)
  129. Pogrebnaya A F, Romanovsky Y M, Tikhonov A N Proc. SPIE 5330 120 (2004)
  130. Pogrebnaya A, Romanovsky Y, Tikhonov A Fluct. Noise Lett. 5 L217 (2005)
  131. Pogrebnaya A F Disc. ... kand. fiz.-mat. nauk (M.: MGU im. M.V. Lomonosova. Biol. fak., 2005)
  132. Pogrebnaya A F Komp’yuternye Issledovaniya Modelirovanie 1 217 (2009)
  133. Kargovskii A V, Romanovskii Yu M, Tikhonov A N Biofizika 54 5 (2009); Kargovsky A V, Romanovsky Yu M, Tikhonov A N Biophysics 54 1 (2009)
  134. Kargovskii A V i dr. Dinamicheskie Modeli Protsessov v Kletkakh i Subkletochnykh Nanostrukturakh (Pod obshch. red. G Yu Riznichenko, A B Rubina) (M. - Izhevsk: RKhD, 2009) p. 69
  135. Fiasconaro A, Ebeling W, Gudowska-Nowak E Eur. Phys. J. B 65 403 (2008)
  136. Nekorkin V I Usp. Fiz. Nauk 178 313 (2008); Nekorkin V I Phys. Usp. 51 295 (2008)
  137. Ivanitskii G R, Krinskii V I, Sel’kov E E Matematicheskaya Biofizika Kletki (M.: Nauka, 1978)
  138. Borisyuk G N i dr. Usp. Fiz. Nauk 172 1189 (2002); Borisyuk G N et al. Phys. Usp. 45 1073 (2002)
  139. Plusnina T Yu et al. J. Biol. Syst. 16 197 (2008)
  140. Murray J D Mathematical Biology I. An Introduction (Berlin: Springer-Verlag, 2002); Myurrei Dzh Matematicheskaya Biologiya. T. 1. Vvedenie (M. - Izhevsk: RKhD. In-t komp’yut. issled., 2009)
  141. Elston T C, Oster G Biophys. J. 73 703 (1997)
  142. Kinosita K (Jr.) et al. Cell 93 21 (1998)

© 1918–2021 Uspekhi Fizicheskikh Nauk
Email: ufn@ufn.ru Editorial office contacts About the journal Terms and conditions