Kinetic analysis of ribosome-bound fluorescent proteins reveals an early, stable, cotranslational folding intermediate

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2568-2578

  Kelkar, Devaki A ^a   Khushoo, Amardeep ^a   Yang, Zhongying ^a   Skach, William R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL PROPERTIES; C TERMINUS; COMPLEX ENVIRONMENTS; CYTOSOLIC; DIRECT ANALYSIS; FLUORESCENT PROTEIN; FOLDING INTERMEDIATES; FOLDING PATHWAY; FUSION PROTEINS; IN-VITRO; KINETIC ANALYSIS; MOLECULAR CROWDING; NON-NATIVE; PEPTIDYLTRANSFERASE; PROTEASE DIGESTION; RATE-LIMITING STEPS; SHARP THRESHOLD;

BIOSYNTHESIS; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; MACHINERY; PROTEIN FOLDING; PROTEINS; UREA;

MACROMOLECULES;

CHAPERONE; CYAN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PEPTIDYLTRANSFERASE; POLYPEPTIDE; PROTEINASE; RED FLUORESCENT PROTEIN; UREA;

ARTICLE; CYTOSOL; DENATURATION; FLUORESCENCE SPECTROSCOPY; IN VITRO STUDY; KINETICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; RIBOSOME;

GREEN FLUORESCENT PROTEINS; KINETICS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; RIBOSOMES;

EID: 84862972129     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.318766     Document Type: Article

References (75)

1. Leopold, P. E., Montal, M., and Onuchic, J. N. (1992) Protein folding funnels. A kinetic approach to the sequence-structure relationship. Proc. Natl. Acad. Sci. U.S.A. 89, 8721-8725
2. Ozkan, S. B., Dill, K. A., and Bahar, I. (2002) Fast-folding protein kinetics, hidden intermediates, and the sequential stabilization model. Protein Sci. 11, 1958-1970 (Pubitemid 34791415)
3. Clark, P. L. (2004) Protein folding in the cell. Reshaping the folding funnel. Trends Biochem. Sci. 29, 527-534
4. Hartl, F. U., and Hayer-Hartl, M. (2009) Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16, 574-581
5. Kramer, G., Boehringer, D., Ban, N., and Bukau, B. (2009) The ribosome as a platform for cotranslational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597
6. Mankin, A. S. (2006) Nascent peptide in the "birth canal" of the ribosome. Trends Biochem. Sci. 31, 11-13
7. Fulle, S., and Gohlke, H. (2009) Statics of the ribosomal exit tunnel. Implications for cotranslational peptide folding, elongation regulation, and antibiotics binding. J. Mol. Biol. 387, 502-517
8. Matagne, A., and Dobson, C. M. (1998) The folding process of hen lysozyme. Aperspective from the "new view." Cell Mol. Life Sci. 54, 363-371 (Pubitemid 28192744)
9. Voss, N. R., Gerstein, M., Steitz, T. A., and Moore, P. B. (2006) The geometry of the ribosomal polypeptide exit tunnel. J. Mol. Biol. 360, 893-906 (Pubitemid 43993916)
10. Thulasiraman, V., Yang, C. F., and Frydman, J. (1999) In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 18, 85-95 (Pubitemid 29005026)
11. Etchells, S. A., Meyer, A. S., Yam, A. Y., Roobol, A., Miao, Y., Shao, Y., Carden, M. J., Skach, W. R., Frydman, J., and Johnson, A. E. (2005) The cotranslational contacts between ribosome-bound nascent polypeptides and the subunits of the hetero-oligomeric chaperonin TRiC probed by photocross-linking. J. Biol. Chem. 280, 28118-28126 (Pubitemid 41076930)
12. Hoffmann, A., Merz, F., Rutkowska, A., Zachmann-Brand, B., Deuerling, E., and Bukau, B. (2006) Trigger factor forms a protective shield for nascent polypeptides at the ribosome. J. Biol. Chem. 281, 6539-6545 (Pubitemid 43847587)
13. Krukenberg, K. A., Street, T. O., Lavery, L. A., and Agard, D. A. (2011) Conformational dynamics of the molecular chaperone Hsp90. Q. Rev. Biophys. 44, 229-255
14. Evans, M. S., Ugrinov, K. G., Frese, M. A., and Clark, P. L. (2005) Homogeneous stalled ribosome nascent chain complexes produced in vivo or in vitro. Nat. Methods 2, 757-762 (Pubitemid 41486207)
15. Schaffitzel, C., and Ban, N. (2007) Generation of ribosome nascent chain complexes for structural and functional studies. J. Struct. Biol. 158, 463-471 (Pubitemid 46764575)
16. Johnson, A. E. (2005) The cotranslational folding and interactions of nascent protein chains. A new approach using fluorescence resonance energy transfer. FEBS Lett. 579, 916-920
17. Fedorov, A. N., and Baldwin, T. O. (1995) Contribution of cotranslational folding to the rate of formation of native protein structure. Proc. Natl. Acad. Sci. U.S.A. 92, 1227-1231
18. Nicola, A. V., Chen, W., and Helenius, A. (1999) Cotranslational folding of an alphavirus capsid protein in the cytosol of living cells. Nat. Cell Biol. 1, 341-345 (Pubitemid 129493575)
19. Svetlov, M. S., Kommer, A., Kolb, V. A., and Spirin, A. S. (2006) Effective cotranslational folding of firefly luciferase without chaperones of the Hsp70 family. Protein Sci. 15, 242-247 (Pubitemid 43144996)
20. Ugrinov, K. G., and Clark, P. L. (2010) Cotranslational folding increases GFP folding yield. Biophys. J. 98, 1312-1320
21. Maggioni, M. C., Liscaljet, I. M., and Braakman, I. (2005) A critical step in the folding of influenza virus HA determined with a novel folding assay. Nat. Struct. Mol. Biol. 12, 258-263 (Pubitemid 43079368)
22. Kleizen, B., van Vlijmen, T., de Jonge, H. R., and Braakman, I. (2005) Folding of CFTR is predominantly cotranslational. Mol. Cell 20, 277-287 (Pubitemid 41484172)
23. Clark, P. L., and King, J. (2001) A newly synthesized, ribosome-bound polypeptide chain adopts conformations dissimilar from early in vitro refolding intermediates. J. Biol. Chem. 276, 25411-25420
24. Evans, M. S., Sander, I. M., and Clark, P. L. (2008) Cotranslational folding promotes beta-helix formation and avoids aggregation in vivo. J. Mol. Biol. 383, 683-692
25. Khushoo, A., Yang, Z., Johnson, A. E., and Skach, W. R. (2011) Ligand-driven vectorial folding of ribosome-bound human CFTR NBD1. Mol. Cell 41, 682-692
26. Woolhead, C. A., McCormick, P. J., and Johnson, A. E. (2004) Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116, 725-736 (Pubitemid 38326730)
27. Eichmann, C., Preissler, S., Riek, R., and Deuerling, E. (2010) Cotranslational structure acquisition of nascent polypeptides monitored by NMR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 107, 9111-9116
28. Cabrita, L. D., Hsu, S. T., Launay, H., Dobson, C. M., and Christodoulou, J. (2009) Probing ribosome-nascent chain complexes produced in vivo by NMR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 106, 22239-22244
29. Jansens, A., van Duijn, E., and Braakman, I. (2002) Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 298, 2401-2403 (Pubitemid 36014216)
30. Xia, K., Manning, M., Hesham, H., Lin, Q., Bystroff, C., and Colón, W. (2007) Identifying the subproteome of kinetically stable proteins via diagonal two-dimensional SDS/PAGE. Proc. Natl. Acad. Sci. U.S.A. 104, 17329-17334 (Pubitemid 350219842)
31. Yang, F., Moss, L. G., and Phillips, G. N., Jr. (1996) The molecular structure of green fluorescent protein. Nat. Biotechnol. 14, 1246-1251 (Pubitemid 26332784)
32. Ormö, M., Cubitt, A. B., Kallio, K., Gross, L. A., Tsien, R. Y., and Remington, S. J. (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273, 1392-1395 (Pubitemid 26296528)
33. Yarbrough, D., Wachter, R. M., Kallio, K., Matz, M. V., and Remington, S. J. (2001) Refined crystal structure of DsRed. A red fluorescent protein from coral, at 2.0-A resolution. Proc. Natl. Acad. Sci. U.S.A. 98, 462-467 (Pubitemid 32105064)
34. Huang, J. R., Craggs, T. D., Christodoulou, J., and Jackson, S. E. (2007) Stable intermediate states and high energy barriers in the unfolding of GFP. J. Mol. Biol. 370, 356-371 (Pubitemid 46829211)
35. Reid, B. G., and Flynn, G. C. (1997) Chromophore formation in green fluorescent protein. Biochemistry 36, 6786-6791 (Pubitemid 27242339)
36. Andrews, B. T., Schoenfish, A. R., Roy, M., Waldo, G., and Jennings, P. A. (2007) The rough energy landscape of superfolder GFP is linked to the chromophore. J. Mol. Biol. 373, 476-490 (Pubitemid 47445575)
37. Andrews, B. T., Roy, M., and Jennings, P. A. (2009) Chromophore packing leads to hysteresis in GFP. J. Mol. Biol. 392, 218-227
38. Kamagata, K., Arai, M., and Kuwajima, K. (2004) Unification of the folding mechanisms of non-two-state and two-state proteins. J. Mol. Biol. 339, 951-965 (Pubitemid 38686356)
39. Cormack, B. P., Valdivia, R. H., and Falkow, S. (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33-38 (Pubitemid 26239677)
40. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A., and Tsien, R. Y. (2001) Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188-29194
41. Shaner, N. C., Steinbach, P. A., and Tsien, R. Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909 (Pubitemid 43108726)
42. Hasegawa, H., Skach, W., Baker, O., Calayag, M. C., Lingappa, V., and Verkman, A. S. (1992) A multifunctional aqueous channel formed by CFTR. Science 258, 1477-1479 (Pubitemid 23011001)
43. Oberdorf, J., and Skach, W. R. (2002) In vitro reconstitution of CFTR biogenesis and degradation. Methods Mol. Med. 70, 295-310
44. McCormick, P. J., Miao, Y., Shao, Y., Lin, J., and Johnson, A. E. (2003) Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell 12, 329-341 (Pubitemid 37238920)
45. Sadlish, H., Pitonzo, D., Johnson, A. E., and Skach, W. R. (2005) Sequential triage of transmembrane segments by Sec61α during biogenesis of a native multispanning membrane protein. Nat. Struct. Mol. Biol. 12, 870-878 (Pubitemid 41486710)
46. Pokrovskaya, I. D., and Gurevich, V. V. (1994) In vitro transcription. Preparative RNA yields in analytical scale reactions. Anal. Biochem. 220, 420-423 (Pubitemid 24261191)
47. Devaraneni, P. K., Conti, B., Matsumura, Y., Yang, Z., Johnson, A. E., and Skach, W. R. (2011) Stepwise insertion and inversion of a type II signal anchor sequence in the ribosome-Sec61 translocon complex. Cell 146, 134-147
48. Kowarik, M., Küng, S., Martoglio, B., and Helenius, A. (2002) Protein folding during cotranslational translocation in the Endoplasmic Reticulum. Mol. Cell 10, 769-778 (Pubitemid 35335632)
49. 2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887
50. Verkhusha, V. V., Chudakov, D. M., Gurskaya, N. G., Lukyanov, S., and Lukyanov, K. A. (2004) Common pathway for the red chromophore formation in fluorescent proteins and chromoproteins. Chem. Biol. 11, 845-854 (Pubitemid 38836900)
51. Shu, X., Shaner, N. C., Yarbrough, C. A., Tsien, R. Y., and Remington, S. J. (2006) Novel chromophores and buried charges control color in mFruits. Biochemistry 45, 9639-9647 (Pubitemid 44257411)
52. Remington, S. J. (2006) Fluorescent proteins, maturation, photochemistry, and photophysics. Curr. Opin. Struct. Biol. 16, 714-721
53. Ward, W. W., Prentice, H. J., Roth, A. F., Cody, C. W., and Reeves, S. C. (1982) Spectral perturbation of the Aqueorea green fluorescent protein. Photochem. Photobiol. 35, 803-808
54. Tsien, R. Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544
55. Sniegowski, J. A., Phail, M. E., and Wachter, R. M. (2005) Maturation efficiency, trypsin sensitivity, and optical properties of Arg-96, Glu-222, and Gly-67 variants of green fluorescent protein. Biochem. Biophys. Res. Commun. 332, 657-663 (Pubitemid 40745165)
56. Hsu, S. T., Blaser, G., and Jackson, S. E. (2009) The folding, stability, and conformational dynamics of β-barrel fluorescent proteins. Chem. Soc. Rev. 38, 2951-2965
57. Kosolapov, A., and Deutsch, C. (2009) Tertiary interactions within the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 16, 405-411
58. Picking, W. D., Picking, W. L., Odom, O. W., and Hardesty, B. (1992) Fluorescence characterization of the environment encountered by nascent polyalanine and polyserine as they exit Escherichia coli ribosomes during translation. Biochemistry 31, 2368-2375
59. Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4-Å resolution. Science 289, 905-920 (Pubitemid 30659939)
60. Lu, J., and Deutsch, C. (2005) Folding zones inside the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 12, 1123-1129 (Pubitemid 41746784)
61. Gajewski, C., Dagcan, A., Roux, B., and Deutsch, C. (2011) Biogenesis of the pore architecture of a voltage-gated potassium channel. Proc. Natl. Acad. Sci. U.S.A. 108, 3240-3245
62. Daniel, C. J., Conti, B., Johnson, A. E., and Skach, W. R. (2008) Control of translocation through the Sec61 translocon by nascent polypeptide structure within the ribosome. J. Biol. Chem. 283, 20864-20873
63. Ziv, G., Haran, G., and Thirumalai, D. (2005) Ribosome exit tunnel can entropically stabilize α-helices. Proc. Natl. Acad. Sci. U.S.A. 102, 18956-18961 (Pubitemid 43049548)
64. O'Brien, E. P., Stan, G., Thirumalai, D., and Brooks, B. R. (2008) Factors governing helix formation in peptides confined to carbon nanotubes. Nano Lett. 8, 3702-3708
65. Li, X., Zhang, G., Ngo, N., Zhao, X., Kain, S. R., and Huang, C. C. (1997) Deletions of the Aequorea victoria green fluorescent protein define the minimal domain required for fluorescence. J. Biol. Chem. 272, 28545-28549 (Pubitemid 27517805)
66. Cabantous, S., and Waldo, G. S. (2006) In vivo and in vitro protein solubility assays using split GFP. Nat. Methods 3, 845-854 (Pubitemid 44445833)
67. O'Brien, E. P., Hsu, S. T., Christodoulou, J., Vendruscolo, M., and Dobson, C. M. (2010) Transient tertiary structure formation within the ribosome exit port. J. Am. Chem. Soc. 132, 16928-16937
68. 13C assignments of yellow fluorescent protein (YFP) Venus. Biomol. NMR Assign 3, 67-72
69. Fukuda, H., Arai, M., and Kuwajima, K. (2000) Folding of green fluorescent protein and the cycle 3 mutant. Biochemistry 39, 12025-12032
70. Enoki, S., Saeki, K., Maki, K., and Kuwajima, K. (2004) Acid denaturation and refolding of green fluorescent protein. Biochemistry 43, 14238-14248 (Pubitemid 39482773)
71. Huang, J. R., Hsu, S. T., Christodoulou, J., and Jackson, S. E. (2008) The extremely slow-exchanging core and acid-denatured state of green fluorescent protein. HFSP J. 2, 378-387
72. Bertz, M., Kunfermann, A., and Rief, M. (2008) Navigating the folding energy landscape of green fluorescent protein. Angew. Chem. Int. Ed. 47, 8192-8195
73. Reeder, P. J., Huang, Y. M., Dordick, J. S., and Bystroff, C. (2010) A rewired green fluorescent protein. Folding and function in a nonsequential, non-circular GFP permutant. Biochemistry 49, 10773-10779
74. Kent, K. P., and Boxer, S. G. (2011) Light-activated reassembly of split green fluorescent protein. J. Am. Chem. Soc. 133, 4046-4052
75. Kent, K. P., Childs, W., and Boxer, S. G. (2008) Deconstructing green fluorescent protein. J. Am. Chem. Soc. 130, 9664-9665