A conserved interaction with the chromophore of fluorescent proteins

Protein Science

Volumn 21, Issue 2, 2012, Pages 171-177

  Choudhary, Amit ^a   Kamer, Kimberli J ^a   Raines, Ronald T ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Green fluorescent protein; Hyperconjugation; Imidazolidinone; N * interaction; Stereoelectronic effect

Indexed keywords

CARBONYL DERIVATIVE; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; OXYGEN; THREONINE;

ARTICLE; BIOGENESIS; CHROMATOPHORE; ELECTRON; ELECTROPHILICITY; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CHROMOGENIC COMPOUNDS; CONSERVED SEQUENCE; FLUORESCENCE; GREEN FLUORESCENT PROTEINS; HYDROGEN BONDING; IMIDAZOLIDINES; LUMINESCENT PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84856174363     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.762     Document Type: Article

References (54)

1. Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509-544.
2. Zimmer M (2002) Green fluorescent protein (GFP): applications, structure, and related photophysical behavior. Chem Rev 102:759-781.
3. Chalfie M (2009) GFP: Lighting up life (Nobel lecture). Angew Chem Int Ed 48:5603-5611.
4. Shimomura O (2009) Discovery of green fluorescent protein (GFP) (Nobel lecture). Angew Chem Int Ed 48: 5590-5602.
5. Tsien RY (2009) Constructing and exploiting the fluorescent protein paintbox (Nobel lecture). Angew Chem Int Ed 48:5612-5626.
6. Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA (2010) Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev 90: 1103-1163.
7. Remington SJ (2011) Green fluorescent protein: a perspective. Protein Sci 20:1508-1519.
8. Bartlett GJ, Choudhary A, Raines RT, Woolfson DN (2010) n→π*interactions in proteins. Nat Chem Biol 6: 615-620.
9. DeRider ML, Wilkens SJ, Waddell MJ, Bretscher LE, Weinhold F, Raines RT, Markley JL (2002) Collagen stability: insights from NMR spectroscopic and hybrid density functional computational investigations of the effect of electronegative substituents on prolyl ring conformations. J Am Chem Soc 124:2497-2505. (Pubitemid 34251763)
10. Hinderaker MP, Raines RT (2003) An electronic effect on protein structure. Protein Sci 12:1188-1194. (Pubitemid 36597505)
11. Hodges JA, Raines RT (2006) Energetics of an n→π* interaction that impacts protein structure. Org Lett 8: 4695-4697. (Pubitemid 44629438)
12. Choudhary A, Gandla D, Krow GR, Raines RT (2009) Nature of amide carbonyl-carbonyl interactions in proteins. J Am Chem Soc 131:7244-7246.
13. Choudhary A, Fry CG, Raines RT (2010) Modulation of an n→π*interaction with a-fluoro groups. ARKIVOC 8: 251-262.
14. Jakobsche CE, Choudhary A, Miller SJ, Raines RT (2010) n→π*interaction and n)(π Pauli repulsion are antagonistic for protein stability. J Am Chem Soc 132: 6651-6653.
15. Shoulders MD, Kotch FW, Choudhary A, Guzei IA, Raines RT (2010) The aberrance of the 4S diastereomer of 4-hydroxyproline. J Am Chem Soc 132:10857-10865.
16. Choudhary A, Raines RT (2011) Signature of n→π*interactions in α-helices. Protein Sci 20:1077-1081.
17. Bürgi HB, Dunitz JD, Shefter E (1973) Geometrical reaction coordinates. II. Nucleophilic addition to a carbonyl group. J Am Chem Soc 95:5065-5067.
18. Bürgi HB, Dunitz JD, Lehn JM, Wipff G (1974) Stereochemistry of reaction paths at carbonyl centres. Tetrahedron 30:1563-1572.
19. Bürgi HB, Lehn JM, Wipff G (1974) An ab initio study of nucleophilic addition to a carbonyl group. J Am Chem Soc 96:1965-1966.
20. Blanco S, López JC, Mata S, Alonso JL (2010) Conformations of γ-aminobutyric acid (GABA): the role of the n→π*interaction. Angew Chem Int Ed 49: 9187-9192.
21. Choudhary A, Kamer KJ, Raines RT (2011) An n→π*interaction in aspirin: implications for structure and reactivity. J Org Chem 76:7933-7937.
22. Gorske BC, Bastian BL, Geske GD, Blackwell HE (2007) Local and tunable n→π*interactions regulate amide isomerism in the peptoid backbone. J Am Chem Soc 129:8928-8929. (Pubitemid 47171818)
23. Gorske BC, Stringer JR, Bastian BL, Fowler SA, Blackwell HE (2009) New strategies for the design of folded peptoids revealed by a survey of noncovalent interactions in model systems. J Am Chem Soc 131: 16555-16567.
24. Choudhary A, Kamer KJ, Powner MW, Sutherland JD, Raines RT (2010) A stereoelectronic effect in prebiotic nucleotide synthesis. ACS Chem Biol 5:655-657.
25. Ormö M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273: 1392-1395. (Pubitemid 26296528)
26. Yang F, Moss LG, Phillips GN, Jr. (1996) The molecular structure of green fluorescent protein. Nat Biotechnol 14:1246-1251. (Pubitemid 26332784)
27. Berman H, Henrick K, Nakamura H, Markley JL (2007) The worldwide protein data bank (wwPDB): ensuring a single, uniform archive of PDB data. Nucleic Acids Res 35:D301-D303. (Pubitemid 46056219)
28. Gray HB. 1965. Electrons and chemical bonding. New York: W. A. Benjamin.
29. Raber DJ, Raber NK, Chandrasekhar J, Scheleyer PvR (1984) Geometries and energies of complexes between formaldehyde and first- and second-row cations. A theoretical study. Inorg Chem 23:4076-4080.
30. Laing M (1987) No rabbit ears on water. J Chem Educ 64:124-128.
31. Weinhold F. Natural bond orbital methods. In: Schleyer PvR, Allinger NL, Clark T, Gasteiger J, Kollman PA, Shaefer HF, III, Schreiner PR, editors. (1998) Encyclopedia of computational chemistry. Chichester, UK: Wiley, pp 1792-1811.
32. Glendening ED, Badenhoop JK, Reed AE, Carpenter JE, Bohmann JA, Morales CM, Weinhold F (2001) NBO 5.0. NBO 50.
33. Weinhold F, Landis CR (2005) Valency and bonding: a natural bond orbital donor-acceptor perspective. Cambridge, UK: Cambridge University Press.
34. Shinobu A, Palm GJ, Schierbeek AJ, Agmon N (2010) Visualizing proton antenna in a high-resolution greenfluorescent protein structure. J Am Chem Soc 132: 11093-11102.
35. Stoner-Ma D, Melief EH, Nappa J, Ronayne KL, Tonge PJ, Meech SR (2006) Proton relay reaction in green fluorescent protein (GFP): polarization-resolved ultrafast vibrational spectroscopy of isotopically edited GFP. J Phys Chem B 110:22009-22018. (Pubitemid 44797314)
36. Niwa H, Inouye S, Hirano T, Matsuno T, Kojima S, Kubota M, Ohashi M, Tsuji FI (1996) Chemical nature of the light emitter of the Aequorea green fluorescent protein. Proc Natl Acad Sci USA 93:13617-13622. (Pubitemid 26424168)
37. Wu L, Burgess K (2008) Synthesis of highly fluorescent GFP-chromophore analogues. J Am Chem Soc 130: 4089-4096. (Pubitemid 351429879)
38. Voityuk AA, Michel-Beyerle M-B, Rösch N (1998) Quantum chemical modeling of structure and absorption spectra of the chromophore in green fluorescent proteins. Chem Phys 231:13-25.
39. Weber W, Helms V, McCammon JA, Langhoff PW (1999) Shedding light on the dark and weakly fluorescent states of green fluorescent proteins. Proc Natl Acad Sci USA 96:6177-6182. (Pubitemid 29256639)
40. Litvinenko KL, Webber NM, Meech SR (2001) An ultrafast polarisation spectroscopy study of internal conversion and orientational relaxation of the chromophore of the green fluorescent protein. Chem Phys Lett 346:47-53. (Pubitemid 33396313)
41. Webber NM, Litvinenko KL, Meech SR (2001) Radiationless relaxation in a synthetic analogue of the green fluorescent protein chromophore. J Phys Chem B 105: 8036-8039. (Pubitemid 35338873)
42. Brandl M, Weiss MS, Jabs A, Suhnel J, Hilgenfeld R (2001) C-H⋯π interactions in proteins. J Mol Biol 307: 357-377.
43. Paige JS, Wu KY, Jaffrey SR (2011) RNA mimics of green fluorescent protein. Science 333:642-646.
44. Remington SJ (2006) Fluorescent proteins: maturation, photochemistry and photophysics. Curr Opin Struct Biol 16:714-721.
45. Wachter RM (2007) Chromogenic cross-link formation in green fluorescent protein. Acc Chem Res 40: 120-127.
46. Barondeau DP, Putnam CD, Kassmann CJ, Taines JA, Getzoff ED (2003) Mechanism and energetics of green fluorescent protein chromophore synthesis revealed by trapped intermediate structures. Proc Natl Acad Sci USA 100:12111-12116. (Pubitemid 37271523)
47. Rosenow MA, Huffman HA, Phail ME, Wachter RM (2004) The crystal structure of the Y66L variant of green fluorescent protein supports a cyclization-oxidation-dehydration mechanism for chromophore maturation. Biochemistry 43:4464-4472. (Pubitemid 38500575)
48. Barondeau DP, Kassmann CJ, Tainer JA, Getzoff ED (2005) Understanding GFP chromophore biosynthesis: controlling backbone cyclization and modifying posttranslational chemistry. Biochemistry 44:1960-1970. (Pubitemid 40223625)
49. Wood TI, Barondeau DP, Hitomi C, Kassmann CJ, Tainer JA, Getzoff ED (2005) Defining the role of arginine 96 in green fluorescent protein fluorophore biosynthesis. Biochemistry 44:16211-16220. (Pubitemid 41785819)
50. Barondeau DP, Tainer JA, Getzoff ED (2006) Structural evidence for an enolate intermediate in GFP fluorophore biosynthesis. J Am Chem Soc 128:3166-3168.
51. Pletneva NV, Pletnev VZ, Lukyanov KA, Gurskaya NG, Goryacheva EA, Martynov VI, Wlodawer A, Dauter Z, Pletnev S (2010) Structural evidence for a dehydrated intermediate in green fluorescent protein chromophore biosynthesis. J Biol Chem 285:15978-15984.
52. Olsen S, Smith SC (2007) Radiationless decay of red fluorescent protein chromophore models via twisted intramolecular charge-transfer states. J Am Chem Soc 129:2054-2065.
53. Olsen S, Smith SC (2008) Bond selection in the photoisomerization reaction of anionic green fluorescent protein and kindling fluorescent protein chromophore models. J Am Chem Soc 130:8677-8689. (Pubitemid 351962501)
54. Meech SR (2009) Excited state reactions in fluorescent proteins. Chem Soc Rev 38:2922-2934.