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Structural basis for reversible photobleaching of a green fluorescent protein homologue.

Henderson JN, Ai HW, Campbell RE, Remington SJ
Proc Natl Acad Sci U S A 104 6672-7 (2007)
Cited: 112 times
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Abstract

Fluorescent protein (FP) variants that can be reversibly converted between fluorescent and nonfluorescent states have proven to be a catalyst for innovation in the field of fluorescence microscopy. However, the structural basis of the process remains poorly understood. High-resolution structures of a FP derived from Clavularia in both the fluorescent and the light-induced nonfluorescent states reveal that the rapid and complete loss of fluorescence observed upon illumination with 450-nm light results from cis-trans isomerization of the chromophore. The photoinduced change in configuration from the well ordered cis isomer to the highly nonplanar and disordered trans isomer is accompanied by a dramatic rearrangement of internal side chains. Taken together, the structures provide an explanation for the loss of fluorescence upon illumination, the slow light-independent recovery, and the rapid light-induced recovery of fluorescence. The fundamental mechanism appears to be common to all of the photoactivatable and reversibly photoswitchable FPs reported to date.

Articles - 2otb mentioned but not cited (6)

  1. Henderson JN, Ai HW, Campbell RE, Remington SJ. Proc Natl Acad Sci U S A 104 6672-6677 (2007)
  2. Drobizhev M, Callis PR, Nifos矛 R, Wicks G, Stoltzfus C, Barnett L, Hughes TE, Sullivan P, Rebane A. Sci Rep 5 13223 (2015)
  3. Nottoli M, Nifos矛 R, Mennucci B, Lipparini F. J Chem Theory Comput 17 5661-5672 (2021)
  4. Burla MC, Carrozzini B, Cascarano GL, Giacovazzo C, Polidori G. Acta Crystallogr D Struct Biol 76 9-18 (2020)
  5. Chen C, Henderson JN, Ruchkin DA, Kirsh JM, Baranov MS, Bogdanov AM, Mills JH, Boxer SG, Fang C. Int J Mol Sci 24 11991 (2023)
  6. Carrozzini B, Cascarano GL, Giacovazzo C. Int J Mol Sci 24 6070 (2023)


Reviews citing this publication (34)

  1. Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA. Physiol Rev 90 1103-1163 (2010)
  2. Day RN, Davidson MW. Chem Soc Rev 38 2887-2921 (2009)
  3. Patterson G, Davidson M, Manley S, Lippincott-Schwartz J. Annu Rev Phys Chem 61 345-367 (2010)
  4. Newman RH, Fosbrink MD, Zhang J. Chem Rev 111 3614-3666 (2011)
  5. Nienhaus K, Nienhaus GU. Chem Soc Rev 43 1088-1106 (2014)
  6. Wiedenmann J, Oswald F, Nienhaus GU. IUBMB Life 61 1029-1042 (2009)
  7. Pakhomov AA, Martynov VI. Chem Biol 15 755-764 (2008)
  8. Meech SR. Chem Soc Rev 38 2922-2934 (2009)
  9. Remington SJ. Protein Sci 20 1509-1519 (2011)
  10. Miyawaki A. Nat Rev Mol Cell Biol 12 656-668 (2011)
  11. M眉ller-Taubenberger A, Anderson KI. Appl Microbiol Biotechnol 77 1-12 (2007)
  12. Subach FV, Verkhusha VV. Chem Rev 112 4308-4327 (2012)
  13. Stepanenko OV, Stepanenko OV, Shcherbakova DM, Kuznetsova IM, Turoverov KK, Verkhusha VV. Biotechniques 51 313-4, 316, 318 passim (2011)
  14. Bourgeois D, Adam V. IUBMB Life 64 482-491 (2012)
  15. Stepanenko OV, Stepanenko OV, Kuznetsova IM, Verkhusha VV, Turoverov KK. Int Rev Cell Mol Biol 302 221-278 (2013)
  16. Miyawaki A, Shcherbakova DM, Verkhusha VV. Curr Opin Struct Biol 22 679-688 (2012)
  17. Zhou X, Herbst-Robinson KJ, Zhang J. Methods Enzymol 504 317-340 (2012)
  18. Wiedenmann J, Gayda S, Adam V, Oswald F, Nienhaus K, Bourgeois D, Nienhaus GU. J Biophotonics 4 377-390 (2011)
  19. Shcherbakova DM, Verkhusha VV. Curr Opin Chem Biol 20 60-68 (2014)
  20. van de Meene AM, Doblin MS, Bacic A. Protoplasma 254 75-94 (2017)
  21. Ka艌a R. Photosynth Res 116 465-479 (2013)
  22. Abbruzzetti S, Bizzarri R, Luin S, Nifos矛 R, Storti B, Viappiani C, Beltram F. Photochem Photobiol Sci 9 1307-1319 (2010)
  23. Hedde PN, Nienhaus GU. Protoplasma 251 349-362 (2014)
  24. Bourgeois D, Regis-Faro A, Adam V. Biochem Soc Trans 40 531-538 (2012)
  25. Blum C, Subramaniam V. Anal Bioanal Chem 393 527-541 (2009)
  26. Adam V. Histochem Cell Biol 142 19-41 (2014)
  27. Horrocks MH, Palayret M, Klenerman D, Lee SF. Histochem Cell Biol 141 577-585 (2014)
  28. Tang L, Fang C. Int J Mol Sci 23 6459 (2022)
  29. Bourgeois D. Int J Mol Sci 18 E1187 (2017)
  30. Shkrob M, Mishin AS, Chudakov DM, Labas IuA, Luk'ianov KA. Bioorg Khim 34 581-590 (2008)
  31. Jeong S, Widengren J, Lee JC. Nanomaterials (Basel) 12 21 (2021)
  32. Kasuboski JM, Sigal YJ, Joens MS, Lillemeier BF, Fitzpatrick JA. Curr Protoc Cytom Chapter 2 Unit2.17 (2012)
  33. Bourigault Y, Chane A, Barbey C, Jafra S, Czajkowski R, Latour X. Microorganisms 9 295 (2021)
  34. Ilovitsh T, Zalevsky Z. Wiley Interdiscip Rev Nanomed Nanobiotechnol 8 439-448 (2016)

Articles citing this publication (72)

  1. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. Nat Methods 5 545-551 (2008)
  2. Grotjohann T, Testa I, Leutenegger M, Bock H, Urban NT, Lavoie-Cardinal F, Willig KI, Eggeling C, Jakobs S, Hell SW. Nature 478 204-208 (2011)
  3. Chudakov DM, Lukyanov S, Lukyanov KA. Nat Protoc 2 2024-2032 (2007)
  4. Lin MZ, McKeown MR, Ng HL, Aguilera TA, Shaner NC, Campbell RE, Adams SR, Gross LA, Ma W, Alber T, Tsien RY. Chem Biol 16 1169-1179 (2009)
  5. Andresen M, Stiel AC, F枚lling J, Wenzel D, Sch枚nle A, Egner A, Eggeling C, Hell SW, Jakobs S. Nat Biotechnol 26 1035-1040 (2008)
  6. Brakemann T, Stiel AC, Weber G, Andresen M, Testa I, Grotjohann T, Leutenegger M, Plessmann U, Urlaub H, Eggeling C, Wahl MC, Hell SW, Jakobs S. Nat Biotechnol 29 942-947 (2011)
  7. Wu J, Liu L, Matsuda T, Zhao Y, Rebane A, Drobizhev M, Chang YF, Araki S, Arai Y, March K, Hughes TE, Sagou K, Miyata T, Nagai T, Li WH, Campbell RE. ACS Chem Neurosci 4 963-972 (2013)
  8. Subach FV, Patterson GH, Renz M, Lippincott-Schwartz J, Verkhusha VV. J Am Chem Soc 132 6481-6491 (2010)
  9. Adam V, Lelimousin M, Boehme S, Desfonds G, Nienhaus K, Field MJ, Wiedenmann J, McSweeney S, Nienhaus GU, Bourgeois D. Proc Natl Acad Sci U S A 105 18343-18348 (2008)
  10. Snapp EL. Trends Cell Biol 19 649-655 (2009)
  11. Aoki K, Matsuda M. Nat Protoc 4 1623-1631 (2009)
  12. Stiel AC, Andresen M, Bock H, Hilbert M, Schilde J, Sch枚nle A, Eggeling C, Egner A, Hell SW, Jakobs S. Biophys J 95 2989-2997 (2008)
  13. Subach FV, Zhang L, Gadella TW, Gurskaya NG, Lukyanov KA, Verkhusha VV. Chem Biol 17 745-755 (2010)
  14. Mizuno H, Mal TK, W盲lchli M, Kikuchi A, Fukano T, Ando R, Jeyakanthan J, Taka J, Shiro Y, Ikura M, Miyawaki A. Proc Natl Acad Sci U S A 105 9227-9232 (2008)
  15. Zimmer M. Chem Soc Rev 38 2823-2832 (2009)
  16. Adam V, Moeyaert B, David CC, Mizuno H, Lelimousin M, Dedecker P, Ando R, Miyawaki A, Michiels J, Engelborghs Y, Hofkens J. Chem Biol 18 1241-1251 (2011)
  17. Andrews BT, Schoenfish AR, Roy M, Waldo G, Jennings PA. J Mol Biol 373 476-490 (2007)
  18. Botman D, de Groot DH, Schmidt P, Goedhart J, Teusink B. Sci Rep 9 2234 (2019)
  19. Mueller F, Morisaki T, Mazza D, McNally JG. Biophys J 102 1656-1665 (2012)
  20. Brakemann T, Weber G, Andresen M, Groenhof G, Stiel AC, Trowitzsch S, Eggeling C, Grubm眉ller H, Hell SW, Wahl MC, Jakobs S. J Biol Chem 285 14603-14609 (2010)
  21. Kuo CT, Thompson AM, Gallina ME, Ye F, Johnson ES, Sun W, Zhao M, Yu J, Wu IC, Fujimoto B, DuFort CC, Carlson MA, Hingorani SR, Paguirigan AL, Radich JP, Chiu DT. Nat Commun 7 11468 (2016)
  22. El Khatib M, Martins A, Bourgeois D, Colletier JP, Adam V. Sci Rep 6 18459 (2016)
  23. Brenner MD, Zhou R, Conway DE, Lanzano L, Gratton E, Schwartz MA, Ha T. Nano Lett 16 2096-2102 (2016)
  24. Alford SC, Wu J, Zhao Y, Campbell RE, Kn枚pfel T. Biol Cell 105 14-29 (2013)
  25. Kim H, Zou T, Modi C, D枚rner K, Grunkemeyer TJ, Chen L, Fromme R, Matz MV, Ozkan SB, Wachter RM. Structure 23 34-43 (2015)
  26. Peddie CJ, Domart MC, Snetkov X, O'Toole P, Larijani B, Way M, Cox S, Collinson LM. J Struct Biol 199 120-131 (2017)
  27. Kent KP, Boxer SG. J Am Chem Soc 133 4046-4052 (2011)
  28. Woodhouse J, Nass Kovacs G, Coquelle N, Uriarte LM, Adam V, Barends TRM, Byrdin M, de la Mora E, Bruce Doak R, Feliks M, Field M, Fieschi F, Guillon V, Jakobs S, Joti Y, Macheboeuf P, Motomura K, Nass K, Owada S, Roome CM, Ruckebusch C, Schir貌 G, Shoeman RL, Thepaut M, Togashi T, Tono K, Yabashi M, Cammarata M, Foucar L, Bourgeois D, Sliwa M, Colletier JP, Schlichting I, Weik M. Nat Commun 11 741 (2020)
  29. Olsen S, McKenzie RH. J Chem Phys 130 184302 (2009)
  30. Faro AR, Carpentier P, Jonasson G, Pompidor G, Arcizet D, Demachy I, Bourgeois D. J Am Chem Soc 133 16362-16365 (2011)
  31. Hoi H, Howe ES, Ding Y, Zhang W, Baird MA, Sell BR, Allen JR, Davidson MW, Campbell RE. Chem Biol 20 1296-1304 (2013)
  32. Vogt A, D'Angelo C, Oswald F, Denzel A, Mazel CH, Matz MV, Ivanchenko S, Nienhaus GU, Wiedenmann J. PLoS One 3 e3766 (2008)
  33. Pletnev S, Subach FV, Dauter Z, Wlodawer A, Verkhusha VV. J Mol Biol 417 144-151 (2012)
  34. Faro AR, Adam V, Carpentier P, Darnault C, Bourgeois D, de Rosny E. Photochem Photobiol Sci 9 254-262 (2010)
  35. Stuhlm眉ller M, Schwarz-Finsterle J, Fey E, Lux J, Bach M, Cremer C, Hinderhofer K, Hausmann M, Hildenbrand G. Nanoscale 7 17938-17946 (2015)
  36. Datta BK, Thiyagarajan D, Samanta S, Ramesh A, Das G. Org Biomol Chem 12 4975-4982 (2014)
  37. Hughes AJ, Tentori AM, Herr AE. J Am Chem Soc 134 17582-17591 (2012)
  38. Morisaki T, McNally JG. PLoS One 9 e107730 (2014)
  39. Fredj A, Pasquier H, Demachy I, Jonasson G, Levy B, Derrien V, Bousmah Y, Manoussaris G, Wien F, Ridard J, Erard M, Merola F. PLoS One 7 e49149 (2012)
  40. Nosrati M, Berbasova T, Vasileiou C, Borhan B, Geiger JH. J Am Chem Soc 138 8802-8808 (2016)
  41. Gayda S, Nienhaus K, Nienhaus GU. Biophys J 103 2521-2531 (2012)
  42. Burghardt TP. PLoS One 6 e16772 (2011)
  43. Ablikim U, Bomme C, Xiong H, Savelyev E, Obaid R, Kaderiya B, Augustin S, Schnorr K, Dumitriu I, Osipov T, Bilodeau R, Kilcoyne D, Kumarappan V, Rudenko A, Berrah N, Rolles D. Sci Rep 6 38202 (2016)
  44. Scott BL, Hoppe AD. Sci Rep 5 10270 (2015)
  45. Galanzha EI, Nedosekin DA, Sarimollaoglu M, Orza AI, Biris AS, Verkhusha VV, Zharov VP. J Biophotonics 8 81-93 (2015)
  46. Roebroek T, Vandenberg W, Sipieter F, Hugelier S, Stove C, Zhang J, Dedecker P. Nat Commun 12 2005 (2021)
  47. Deng Y, Sun M, Lin PH, Ma J, Shaevitz JW. PLoS One 9 e94807 (2014)
  48. Don Paul C, Kiss C, Traore DA, Gong L, Wilce MC, Devenish RJ, Bradbury A, Prescott M. PLoS One 8 e75835 (2013)
  49. Olsen S, McKenzie RH. J Chem Phys 137 164319 (2012)
  50. Sirimuthu NM, Syme CD, Cooper JM. Chem Commun (Camb) 47 4099-4101 (2011)
  51. Wang Q, Byrnes LJ, Shui B, R枚hrig UF, Singh A, Chudakov DM, Lukyanov S, Zipfel WR, Kotlikoff MI, Sondermann H. PLoS One 6 e23513 (2011)
  52. Serra F, Terentjev EM. J Chem Phys 128 224510 (2008)
  53. Burghardt TP, Li J, Ajtai K. Biochemistry 48 754-765 (2009)
  54. Wachter RM. Int J Mol Sci 18 E1792 (2017)
  55. Hutchison CDM, Cordon-Preciado V, Morgan RML, Nakane T, Ferreira J, Dorlhiac G, Sanchez-Gonzalez A, Johnson AS, Fitzpatrick A, Fare C, Marangos JP, Yoon CH, Hunter MS, DePonte DP, Boutet S, Owada S, Tanaka R, Tono K, Iwata S, van Thor JJ. Int J Mol Sci 18 E1918 (2017)
  56. Malo GD, Wang M, Wu D, Stelling AL, Tonge PJ, Wachter RM. J Mol Biol 378 871-886 (2008)
  57. Vegh RB, Bloch DA, Bommarius AS, Verkhovsky M, Pletnev S, Iwa茂 H, Bochenkova AV, Solntsev KM. Phys Chem Chem Phys 17 12472-12485 (2015)
  58. Ilovitsh T, Danan Y, Meir R, Meiri A, Zalevsky Z. Sci Rep 5 8244 (2015)
  59. Vigano MA, Bieli D, Schaefer JV, Jakob RP, Matsuda S, Maier T, Pl眉ckthun A, Affolter M. Biol Open 7 bio036749 (2018)
  60. Kiefer HV, Lattouf E, Persen NW, Bochenkova AV, Andersen LH. Phys Chem Chem Phys 17 20056-20060 (2015)
  61. Danan Y, Yariv I, Zalevsky Z, Sinvani M. Materials (Basel) 10 E203 (2017)
  62. Ilovitsh T, Danan Y, Meir R, Meiri A, Zalevsky Z. Sci Rep 5 10965 (2015)
  63. Duw茅 S, Moeyaert B, Dedecker P. Curr Protoc Chem Biol 7 27-41 (2015)
  64. Srivastava S, Thakur N, Singh A, Shukla P, Maikhuri VK, Garg N, Prasad A, Pandey R. RSC Adv 9 29856-29863 (2019)
  65. Ikejiri M, Kojima H, Fugono Y, Fujisaka A, Chihara Y, Miyashita K. Org Biomol Chem 16 2397-2401 (2018)
  66. Wang D, Merz T, van Gunsteren WF. Phys Chem Chem Phys 12 11051-11061 (2010)
  67. Zhang L, Gurskaia NG, Kopantseva EE, Mudrik NN, Vagner LL, Luk'ianov KA, Chudakov DM. Bioorg Khim 36 187-192 (2010)
  68. Ilovitsh T, Ilovitsh A, Weiss A, Meir R, Zalevsky Z. Sci Rep 5 15473 (2015)
  69. Wu T, Kumar M, Zhang J, Zhao S, Drobizhev M, McCollum M, Anderson CT, Wang Y, Pokorny A, Tian X, Zhang Y, Tzounopoulos T, Ai HW. Sci Adv 9 eadd2058 (2023)
  70. Glazachev YI, Orlova DY, 艠ezn铆膷kov谩 P, B谩rtov谩 E. Phys Biol 15 036008 (2018)
  71. Zhang N, Li K, Xie BB, Chen XL, Zhou BC, Su HN, Zhang YZ. Mar Life Sci Technol 3 427-433 (2021)
  72. Kirk W, Allen T, Atanasova E, Wessels W, Yao J, Prendergast F. J Fluoresc 27 895-919 (2017)


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