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Mechanism of folding chamber closure in a group II chaperonin.

<div class='caption-title'>a. Top and side views of the cryo-EM density maps with one subunit colored blue (wild-type) and green (lidless) at 4.3 and 4.8 Å resolution respectively.</div>
<div class='caption-title'>a. Top and side views of the Mm-cpn density maps with one subunit colored yellow (wild-type) and orange (lidless) at 10 and 8 Å resolution respectively.</div>
<div class='caption-title'>a. Backbone models for two neighboring subunits of two states viewed from the central cavity with nucleotides as sphere models.</div>
Zhang J, Baker ML, Schr枚der GF, Douglas NR, Reissmann S, Jakana J, Dougherty M, Fu CJ, Levitt M, Ludtke SJ, Frydman J, Chiu W
OpenAccess logo Nature 463 379-83 (2010)
Cited: 138 times
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Abstract

Group II chaperonins are essential mediators of cellular protein folding in eukaryotes and archaea. These oligomeric protein machines, approximately 1 megadalton, consist of two back-to-back rings encompassing a central cavity that accommodates polypeptide substrates. Chaperonin-mediated protein folding is critically dependent on the closure of a built-in lid, which is triggered by ATP hydrolysis. The structural rearrangements and molecular events leading to lid closure are still unknown. Here we report four single particle cryo-electron microscopy (cryo-EM) structures of Mm-cpn, an archaeal group II chaperonin, in the nucleotide-free (open) and nucleotide-induced (closed) states. The 4.3 A resolution of the closed conformation allowed building of the first ever atomic model directly from the single particle cryo-EM density map, in which we were able to visualize the nucleotide and more than 70% of the side chains. The model of the open conformation was obtained by using the deformable elastic network modelling with the 8 A resolution open-state cryo-EM density restraints. Together, the open and closed structures show how local conformational changes triggered by ATP hydrolysis lead to an alteration of intersubunit contacts within and across the rings, ultimately causing a rocking motion that closes the ring. Our analyses show that there is an intricate and unforeseen set of interactions controlling allosteric communication and inter-ring signalling, driving the conformational cycle of group II chaperonins. Beyond this, we anticipate that our methodology of combining single particle cryo-EM and computational modelling will become a powerful tool in the determination of atomic details involved in the dynamic processes of macromolecular machines in solution.

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  1. Lopez T, Dalton K, Frydman J. J. Mol. Biol. 427 2919-2930 (2015)
  2. Latorre V, Mattenberger F, Geller R. Viruses 10 (2018)
  3. Gestaut D, Limatola A, Joachimiak L, Frydman J. Curr. Opin. Struct. Biol. 55 50-58 (2019)

Articles - 3iyf mentioned but not cited (15)

  1. Zhang J, Baker ML, Schr枚der GF, Douglas NR, Reissmann S, Jakana J, Dougherty M, Fu CJ, Levitt M, Ludtke SJ, Frydman J, Chiu W. Nature 463 379-383 (2010)
  2. Zhang J, Ma B, DiMaio F, Douglas NR, Joachimiak LA, Baker D, Frydman J, Levitt M, Chiu W. Structure 19 633-639 (2011)
  3. Baker ML, Baker MR, Hryc CF, Ju T, Chiu W. Biopolymers 97 655-668 (2012)
  4. Hoersch D, Roh SH, Chiu W, Kortemme T. Nat Nanotechnol 8 928-932 (2013)
  5. Afonine PV, Klaholz BP, Moriarty NW, Poon BK, Sobolev OV, Terwilliger TC, Adams PD, Urzhumtsev A. Acta Crystallogr D Struct Biol 74 814-840 (2018)
  6. Wu X, Subramaniam S, Case DA, Wu KW, Brooks BR. J. Struct. Biol. 183 429-440 (2013)
  7. Zhang J, Minary P, Levitt M. Proc. Natl. Acad. Sci. U.S.A. 109 9845-9850 (2012)
  8. Joseph AP, Lagerstedt I, Patwardhan A, Topf M, Winn M. J. Struct. Biol. 199 12-26 (2017)
  9. Lee BH, Seo S, Kim MH, Kim Y, Jo S, Choi MK, Lee H, Choi JB, Kim MK. PLoS One 12 e0185658 (2017)
  10. Lee H, Seo S, Kim M, Choi Jb, Kim SM, Jeon TJ, Kim MK. Protein Sci. 23 703-713 (2014)
  11. Kuzu G, Keskin O, Nussinov R, Gursoy A. Acta Crystallogr D Struct Biol 72 1137-1148 (2016)
  12. Morita K, Yamamoto YY, Hori A, Obata T, Uno Y, Shinohara K, Noguchi K, Noi K, Ogura T, Ishii K, Kato K, Kikumoto M, Arranz R, Valpuesta JM, Yohda M. Int J Mol Sci 19 (2018)
  13. Burger V, Chennubhotla C. Biopolymers 97 732-741 (2012)
  14. Peck A, Chang HY, Dujardin A, Ramalingam D, Uervirojnangkoorn M, Wang Z, Mancuso A, Poitevin F, Yoon CH. J Appl Crystallogr 55 1002-1010 (2022)
  15. Ritterson RS, Hoersch D, Barlow KA, Kortemme T. Methods Mol. Biol. 1414 197-211 (2016)


Reviews citing this publication (27)

  1. Saibil H. Nat. Rev. Mol. Cell Biol. 14 630-642 (2013)
  2. Lindquist SL, Kelly JW. Cold Spring Harb Perspect Biol 3 (2011)
  3. Roth DM, Balch WE. Curr. Opin. Cell Biol. 23 126-134 (2011)
  4. Zhou ZH. Adv Protein Chem Struct Biol 82 1-35 (2011)
  5. Clare DK, Saibil HR. Biopolymers 99 846-859 (2013)
  6. Penczek PA. Meth. Enzymol. 482 1-33 (2010)
  7. Zhang X, Zhou ZH. J. Struct. Biol. 175 253-263 (2011)
  8. Jarrell KF, Walters AD, Bochiwal C, Borgia JM, Dickinson T, Chong JP. Microbiology (Reading, Engl.) 157 919-936 (2011)
  9. Ludtke SJ. Meth. Enzymol. 579 159-189 (2016)
  10. Rother M, Nussbaumer MG, Renggli K, Bruns N. Chem Soc Rev 45 6213-6249 (2016)
  11. Glaeser RM, Hall RJ. Biophys. J. 100 2331-2337 (2011)
  12. Lin L, Xu J. Biotechnol. Adv. 31 827-837 (2013)
  13. Faruqi AR, McMullan G. Q. Rev. Biophys. 44 357-390 (2011)
  14. Gabizon R, Friedler A. Front Chem 2 9 (2014)
  15. Skj忙rven L, Cuellar J, Martinez A, Valpuesta JM. FEBS Lett. 589 2522-2532 (2015)
  16. Chang J, Liu X, Rochat RH, Baker ML, Chiu W. Adv. Exp. Med. Biol. 726 49-90 (2012)
  17. Sander B, Golas MM. Microsc. Res. Tech. 74 642-663 (2011)
  18. Serysheva II. Cell Calcium 56 125-132 (2014)
  19. Hutt DM, Balch WE. Cold Spring Harb Perspect Biol 5 (2013)
  20. Zhang Q, Bettadapura R, Bajaj C. Biopolymers 97 709-731 (2012)
  21. Baker MR, Fan G, Serysheva II. Eur J Transl Myol 25 4803 (2015)
  22. Moiseenkova-Bell V, Wensel TG. Adv. Exp. Med. Biol. 704 25-40 (2011)
  23. Lund P. Biochem. Soc. Trans. 39 94-98 (2011)
  24. Conway de Macario E, Robb FT, Macario AJ. Front Mol Biosci 3 84 (2016)
  25. Faber S, Roepman R. Genes (Basel) 10 (2019)
  26. Conway de Macario E, Yohda M, Macario AJL, Robb FT. Commun Biol 2 103 (2019)
  27. Chang WH, Huang SH, Lin HH, Chung SC, Tu IP. Front Bioinform 1 788308 (2021)

Articles citing this publication (93)

  1. Li X, Mooney P, Zheng S, Booth CR, Braunfeld MB, Gubbens S, Agard DA, Cheng Y. Nat. Methods 10 584-590 (2013)
  2. Fujii T, Iwane AH, Yanagida T, Namba K. Nature 467 724-728 (2010)
  3. other Henderson R, Sali A, Baker ML, Carragher B, Devkota B, Downing KH, Egelman EH, Feng Z, Frank J, Grigorieff N, Jiang W, Ludtke SJ, Medalia O, Penczek PA, Rosenthal PB, Rossmann MG, Schmid MF, Schr枚der GF, Steven AC, Stokes DL, Westbrook JD, Wriggers W, Yang H, Young J, Berman HM, Chiu W, Kleywegt GJ, Lawson CL. Structure 20 205-214 (2012)
  4. Zhang X, Ge P, Yu X, Brannan JM, Bi G, Zhang Q, Schein S, Zhou ZH. Nat. Struct. Mol. Biol. 20 105-110 (2013)
  5. Leitner A, Joachimiak LA, Bracher A, M枚nkemeyer L, Walzthoeni T, Chen B, Pechmann S, Holmes S, Cong Y, Ma B, Ludtke S, Chiu W, Hartl FU, Aebersold R, Frydman J. Structure 20 814-825 (2012)
  6. Lawson CL, Baker ML, Best C, Bi C, Dougherty M, Feng P, van Ginkel G, Devkota B, Lagerstedt I, Ludtke SJ, Newman RH, Oldfield TJ, Rees I, Sahni G, Sala R, Velankar S, Warren J, Westbrook JD, Henrick K, Kleywegt GJ, Berman HM, Chiu W. Nucleic Acids Res. 39 D456-64 (2011)
  7. Kalisman N, Adams CM, Levitt M. Proc. Natl. Acad. Sci. U.S.A. 109 2884-2889 (2012)
  8. Mu帽oz IG, Y茅benes H, Zhou M, Mesa P, Serna M, Park AY, Bragado-Nilsson E, Beloso A, de C谩rcer G, Malumbres M, Robinson CV, Valpuesta JM, Montoya G. Nat. Struct. Mol. Biol. 18 14-19 (2011)
  9. Allegretti M, Mills DJ, McMullan G, K眉hlbrandt W, Vonck J. Elife 3 e01963 (2014)
  10. Wang Z, Hryc CF, Bammes B, Afonine PV, Jakana J, Chen DH, Liu X, Baker ML, Kao C, Ludtke SJ, Schmid MF, Adams PD, Chiu W. Nat Commun 5 4808 (2014)
  11. Douglas NR, Reissmann S, Zhang J, Chen B, Jakana J, Kumar R, Chiu W, Frydman J. Cell 144 240-252 (2011)
  12. Baker ML, Zhang J, Ludtke SJ, Chiu W. Nat Protoc 5 1697-1708 (2010)
  13. Bammes BE, Rochat RH, Jakana J, Chen DH, Chiu W. J. Struct. Biol. 177 589-601 (2012)
  14. Ge P, Zhou ZH. Proc. Natl. Acad. Sci. U.S.A. 108 9637-9642 (2011)
  15. Baker ML, Abeysinghe SS, Schuh S, Coleman RA, Abrams A, Marsh MP, Hryc CF, Ruths T, Chiu W, Ju T. J. Struct. Biol. 174 360-373 (2011)
  16. Pereira JH, Ralston CY, Douglas NR, Meyer D, Knee KM, Goulet DR, King JA, Frydman J, Adams PD. J. Biol. Chem. 285 27958-27966 (2010)
  17. Gopal A, Zhou ZH, Knobler CM, Gelbart WM. RNA 18 284-299 (2012)
  18. Cong Y, Schr枚der GF, Meyer AS, Jakana J, Ma B, Dougherty MT, Schmid MF, Reissmann S, Levitt M, Ludtke SL, Frydman J, Chiu W. EMBO J. 31 720-730 (2012)
  19. Chan KY, Gumbart J, McGreevy R, Watermeyer JM, Sewell BT, Schulten K. Structure 19 1211-1218 (2011)
  20. DiMaio F, Zhang J, Chiu W, Baker D. Protein Sci. 22 865-868 (2013)
  21. Lasker K, Sali A, Wolfson HJ. Proteins 78 3205-3211 (2010)
  22. Chan KY, Trabuco LG, Schreiner E, Schulten K. Biopolymers 97 678-686 (2012)
  23. Sergeeva OA, Chen B, Haase-Pettingell C, Ludtke SJ, Chiu W, King JA. J. Biol. Chem. 288 17734-17744 (2013)
  24. Boudiaf-Benmammar C, Cresteil T, Melki R. PLoS ONE 8 e60895 (2013)
  25. Huo Y, Hu Z, Zhang K, Wang L, Zhai Y, Zhou Q, Lander G, Zhu J, He Y, Pang X, Xu W, Bartlam M, Dong Z, Sun F. Structure 18 1270-1279 (2010)
  26. R眉脽mann F, Stemp MJ, M枚nkemeyer L, Etchells SA, Bracher A, Hartl FU. Proc. Natl. Acad. Sci. U.S.A. 109 21208-21215 (2012)
  27. Wang Z, Schr枚der GF. Biopolymers 97 687-697 (2012)
  28. Mills DJ, Vitt S, Strauss M, Shima S, Vonck J. Elife 2 e00218 (2013)
  29. Stone JE, McGreevy R, Isralewitz B, Schulten K. Faraday Discuss. 169 265-283 (2014)
  30. Pereira JH, Ralston CY, Douglas NR, Kumar R, Lopez T, McAndrew RP, Knee KM, King JA, Frydman J, Adams PD. EMBO J. 31 731-740 (2012)
  31. Si D, Ji S, Nasr KA, He J. Biopolymers 97 698-708 (2012)
  32. Plimpton RL, Cu茅llar J, Lai CW, Aoba T, Makaju A, Franklin S, Mathis AD, Prince JT, Carrascosa JL, Valpuesta JM, Willardson BM. Proc. Natl. Acad. Sci. U.S.A. 112 2413-2418 (2015)
  33. Schwander P, Giannakis D, Yoon CH, Ourmazd A. Opt Express 20 12827-12849 (2012)
  34. Knee KM, Sergeeva OA, King JA. Cell Stress Chaperones 18 137-144 (2013)
  35. Zhang X, Zhang X, Zhou ZH. J. Struct. Biol. 172 400-406 (2010)
  36. Tracy CM, Gray AJ, Cu茅llar J, Shaw TS, Howlett AC, Taylor RM, Prince JT, Ahn NG, Valpuesta JM, Willardson BM. J. Biol. Chem. 289 4490-4502 (2014)
  37. Kmiecik S, Kolinski A. J. Am. Chem. Soc. 133 10283-10289 (2011)
  38. Gupta AJ, Haldar S, Mili膷i膰 G, Hartl FU, Hayer-Hartl M. J. Mol. Biol. 426 2739-2754 (2014)
  39. Baker ML, Baker MR, Hryc CF, Dimaio F. Meth. Enzymol. 483 1-29 (2010)
  40. Chapman MS, Trzynka A, Chapman BK. J. Struct. Biol. 182 10-21 (2013)
  41. Kabir MA, Uddin W, Narayanan A, Reddy PK, Jairajpuri MA, Sherman F, Ahmad Z. J Amino Acids 2011 843206 (2011)
  42. Sekiguchi H, Nakagawa A, Moriya K, Makabe K, Ichiyanagi K, Nozawa S, Sato T, Adachi S, Kuwajima K, Yohda M, Sasaki YC. PLoS ONE 8 e64176 (2013)
  43. Techtmann SM, Robb FT. Proc. Natl. Acad. Sci. U.S.A. 107 20269-20274 (2010)
  44. Tjioe E, Lasker K, Webb B, Wolfson HJ, Sali A. Nucleic Acids Res. 39 W167-70 (2011)
  45. Baker MR, Rees I, Ludtke SJ, Chiu W, Baker ML. Structure 20 450-463 (2012)
  46. Roh SH, Hryc CF, Jeong HH, Fei X, Jakana J, Lorimer GH, Chiu W. Proc. Natl. Acad. Sci. U.S.A. 114 8259-8264 (2017)
  47. Luo H, Robb FT. Arch. Biochem. Biophys. 512 111-118 (2011)
  48. Zang Y, Jin M, Wang H, Cui Z, Kong L, Liu C, Cong Y. Nat. Struct. Mol. Biol. 23 1083-1091 (2016)
  49. Renggli K, Nussbaumer MG, Urbani R, Pfohl T, Bruns N. Angew. Chem. Int. Ed. Engl. 53 1443-1447 (2014)
  50. Chen M, Baldwin PR, Ludtke SJ, Baker ML. J. Struct. Biol. 196 289-298 (2016)
  51. Knee KM, Goulet DR, Zhang J, Chen B, Chiu W, King JA. Protein Sci. 20 30-41 (2011)
  52. Nussbaumer MG, Duskey JT, Rother M, Renggli K, Chami M, Bruns N. Adv Sci (Weinh) 3 1600046 (2016)
  53. Bammes BE, Rochat RH, Jakana J, Chiu W. J. Struct. Biol. 175 384-393 (2011)
  54. Baker MR, Fan G, Serysheva II. Eur J Transl Myol 25 35-48 (2015)
  55. Pereira JH, McAndrew RP, Sergeeva OA, Ralston CY, King JA, Adams PD. Sci Rep 7 3673 (2017)
  56. Pilak O, Harrop SJ, Siddiqui KS, Chong K, De Francisci D, Burg D, Williams TJ, Cavicchioli R, Curmi PM. Environ. Microbiol. 13 2232-2249 (2011)
  57. Peng S, Chu Z, Lu J, Li D, Wang Y, Yang S, Zhang Y. Cell Stress Chaperones 21 477-484 (2016)
  58. Zhang K, Wang L, Liu Y, Chan KY, Pang X, Schulten K, Dong Z, Sun F. Protein Cell 4 432-444 (2013)
  59. Nakagawa A, Moriya K, Arita M, Yamamoto Y, Kitamura K, Ishiguro N, Kanzaki T, Oka T, Makabe K, Kuwajima K, Yohda M. J. Mol. Biol. 426 447-459 (2014)
  60. Comment Woolley GA. Nat Nanotechnol 8 892-893 (2013)
  61. Chaston JJ, Smits C, Arag茫o D, Wong AS, Ahsan B, Sandin S, Molugu SK, Molugu SK, Bernal RA, Stock D, Stewart AG. Structure 24 364-374 (2016)
  62. Biswas A, Ranjan D, Zubair M, Zeil S, Nasr KA, He J. IEEE/ACM Trans Comput Biol Bioinform 14 578-586 (2017)
  63. Lopez T, Dalton K, Tomlinson A, Pande V, Frydman J. Nat. Struct. Mol. Biol. 24 726-733 (2017)
  64. Anthony KC, You C, Piehler J, Pomeranz Krummel DA. Structure 22 628-635 (2014)
  65. An YJ, Rowland SE, Na JH, Spigolon D, Hong SK, Yoon YJ, Lee JH, Robb FT, Cha SS. Nat Commun 8 827 (2017)
  66. Chandramouli P, Hernandez-Lopez R, Wang HW, Leschziner AE. J. Struct. Biol. 175 85-96 (2011)
  67. Hoersch D, Kortemme T. Structure 24 576-584 (2016)
  68. Rochat RH, Hecksel CW, Chiu W. Methods Mol. Biol. 1144 265-281 (2014)
  69. Bajaj C, Goswami S, Zhang Q. J. Struct. Biol. 177 367-381 (2012)
  70. Iizuka R, Ueno T, Morone N, Funatsu T. PLoS ONE 6 e22253 (2011)
  71. Willison KR. Structure 19 754-755 (2011)
  72. Dalton KM, Frydman J, Pande VS. PLoS ONE 10 e0117724 (2015)
  73. Enriquez AS, Rojo HM, Bhatt JM, Molugu SK, Hildenbrand ZL, Bernal RA. Cell Cycle 16 1309-1319 (2017)
  74. Congresses Bromberg S, Chiu W, Ferrin TE. Structure 18 1261-1265 (2010)
  75. Sergeeva OA, Yang J, King JA, Knee KM. Protein Sci. 23 693-702 (2014)
  76. Paul DM, Beuron F, Sessions RB, Brancaccio A, Bigotti MG. Sci Rep 6 20696 (2016)
  77. Hiller S. J Biomol NMR 75 1-8 (2021)
  78. Rao Z. Structure 18 1221-1222 (2010)
  79. Bhatt JM, Enriquez AS, Wang J, Rojo HM, Molugu SK, Hildenbrand ZL, Bernal RA. Front Mol Biosci 5 42 (2018)
  80. Mas G, Guan JY, Crublet E, Debled EC, Moriscot C, Gans P, Schoehn G, Macek P, Schanda P, Boisbouvier J. Sci Adv 4 eaau4196 (2018)
  81. Jin M, Han W, Liu C, Zang Y, Li J, Wang F, Wang Y, Cong Y. Proc. Natl. Acad. Sci. U.S.A. 116 19513-19522 (2019)
  82. Ecoffet A, Woollard G, Kushner A, Poitevin F, Duc KD. AIMS Math 7 986-999 (2022)
  83. Zhao Y, Schmid MF, Frydman J, Chiu W. Nat Commun 12 4754 (2021)
  84. Kommera PR, Ramakrishnaiah V, Sweeney C, Donatelli J, Zwart PH. J Appl Crystallogr 54 1179-1188 (2021)
  85. Yang LD, Chu ZM, Zhang Y, Yang SL. Biotechnol. Lett. 33 1649-1655 (2011)
  86. Zhang PF, Su JG. J Chem Phys 151 045101 (2019)
  87. Shoemark DK, Sessions RB, Brancaccio A, Bigotti MG. FASEB J. 32 2223-2234 (2018)
  88. Araki K, Watanabe-Nakayama T, Sasaki D, Sasaki YC, Mio K. Int J Mol Sci 24 14850 (2023)
  89. Ding J, Li J, Yang D, Yang F, Nie H, Huo Z, Yan X. Cell Stress Chaperones 23 179-187 (2018)
  90. Moriya T, Mio K, Sato C. Microscopy (Oxf) 62 491-513 (2013)
  91. F枚rster F. J Struct Biol X 6 100063 (2022)
  92. Ogawa N, Yamamoto YY, Abe K, Sekiguchi H, Sasaki YC, Ishikawa A, Frydman J, Yohda M. Int J Mol Sci 19 (2018)
  93. Pretto C, van Hest JCM. Bioconjug. Chem. 30 3069-3077 (2019)


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