Microscopic insights into the protein-stabilizing effect of trimethylamine N-oxide (TMAO)

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 23, 2014, Pages 8476-8481

  Ma, Jianqiang ^a,b   Pazos, Ileana M ^a,b   Gai, Feng ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Ultrafast Optical Processes Laboratory   (United States)

Author keywords

2D IR; Crowding; Infrared; Linear response function

Indexed keywords

AMINO ACID; PEPTIDE; PHENYLALANINE DERIVATIVE; PROTEIN; SOLVENT; TRIMETHYLAMINE OXIDE; UREA; WATER;

ARTICLE; HYDRATION; HYDROGEN BOND; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULE; PHOTON; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; VIBRATION;

2D IR; CROWDING; INFRARED; LINEAR RESPONSE FUNCTION;

HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; METHYLAMINES; MICROFILAMENT PROTEINS; MUTATION; PEPTIDES; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN UNFOLDING; PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; UREA; WATER;

EID: 84902134138     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1403224111     Document Type: Article

References (76)

1. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208(Pt 15):2819-2830.
2. Wang A, Bolen DW (1997) A naturally occurring protective system in urea-rich cells: Mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 36(30):9101-9108. (Pubitemid 27329494)
3. Zou Q, Bennion BJ, Daggett V, Murphy KP (2002) The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. J Am Chem Soc 124(7):1192-1202. (Pubitemid 34169126)
4. Sharp KA, Madan B, Manas E, Vanderkooi JM (2001) Water structure changes induced by hydrophobic and polar solutes revealed by simulations and infrared spectroscopy. J Chem Phys 114(4):1791-1796. (Pubitemid 32168679)
5. Di Michele A, et al. (2006) Modulation of hydrophobic effect by cosolutes. J Phys Chem B 110(42):21077-21085.
6. Rezus YLA, Bakker HJ (2007) Observation of immobilized water molecules around hydrophobic groups. Phys Rev Lett 99(14):148301.
7. Rezus YLA, Bakker HJ (2009) Destabilization of the hydrogen-bond structure of water by the osmolyte trimethylamine N-oxide. J Phys Chem B 113(13):4038-4044.
8. Koga Y, Westh P, Nishikawa K, Subramanian S (2011) Is a methyl group always hydrophobic? Hydrophilicity of trimethylamine-N-oxide, tetramethyl urea and tetramethylammonium ion. J Phys Chem B 115(12):2995-3002.
9. Munroe KL, Magers DH, Hammer NI (2011) Raman spectroscopic signatures of noncovalent interactions between trimethylamine N-oxide (TMAO) and water. J Phys Chem B 115(23):7699-7707.
10. Sagle LB, et al. (2011) Methyl groups of trimethylamine N-oxide orient away from hydrophobic interfaces. J Am Chem Soc 133(46):18707-18712.
11. Bakulin AA, Pshenichnikov MS, Bakker HJ, Petersen C (2011) Hydrophobic molecules slow down the hydrogen-bond dynamics of water. J Phys Chem A 115(10):1821-1829.
12. Larini L, Shea J-E (2013) Double resolution model for studying TMAO/water effective interactions. J Phys Chem B 117(42):13268-13277.
13. Athawale MV, Dordick JS, Garde S (2005) Osmolyte trimethylamine-N-oxide does not affect the strength of hydrophobic interactions: Origin of osmolyte compatibility. Biophys J 89(2):858-866. (Pubitemid 41098972)
14. Auton M, Bolen DW (2005) Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc Natl Acad Sci USA 102(42):15065-15068. (Pubitemid 41513335)
15. Paul S, Patey GN (2007) Structure and interaction in aqueous urea-trimethylamine-N-oxide solutions. J Am Chem Soc 129(14):4476-4482. (Pubitemid 46595464)
16. O'Brien EP, Ziv G, Haran G, Brooks BR, Thirumalai D (2008) Effects of denaturants and osmolytes on proteins are accurately predicted by the molecular transfer model. Proc Natl Acad Sci USA 105(36):13403-13408.
17. Meersman F, Bowron D, Soper AK, Koch MHJ (2009) Counteraction of urea by trimethylamine N-oxide is due to direct interaction. Biophys J 97(9):2559-2566.
18. Hu CY, Lynch GC, Kokubo H, Pettitt BM (2010) Trimethylamine N-oxide influence on the backbone of proteins: An oligoglycine model. Proteins 78(3):695-704.
19. Wei H, Fan Y, Gao YQ (2010) Effects of urea, tetramethyl urea, and trimethylamine N-oxide on aqueous solution structure and solvation of protein backbones: A molecular dynamics simulation study. J Phys Chem B 114(1):557-568.
20. Rösgen J, Jackson-Atogi R (2012) Volume exclusion and H-bonding dominate the thermodynamics and solvation of trimethylamine-N-oxide in aqueous urea. J Am Chem Soc 134(7):3590-3597.
21. Fiore A, Venkateshwaran V, Garde S (2013) Trimethylamine N-oxide (TMAO) and tertbutyl alcohol (TBA) at hydrophobic interfaces: Insights from molecular dynamics simulations. Langmuir 29(25):8017-8024.
22. Macdonald RD, Khajehpour M (2013) Effects of the osmolyte TMAO (Trimethylamine-N-oxide) on aqueous hydrophobic contact-pair interactions. Biophys Chem 184:101-107.
23. Bruździak P, Panuszko A, Stangret J (2013) Influence of osmolytes on protein and water structure: A step to understanding the mechanism of protein stabilization. J Phys Chem B 117(39):11502-11508.
24. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: Evolution of osmolyte systems. Science 217(4566):1214-1222. (Pubitemid 13283134)
25. Uversky VN, Li J, Fink AL (2001) Trimethylamine-N-oxide-induced folding of alpha-synuclein. FEBS Lett 509(1):31-35.
26. Mello CC, Barrick D (2003) Measuring the stability of partly folded proteins using TMAO. Protein Sci 12(7):1522-1529. (Pubitemid 36759355)
27. Qu YX, Bolen DW (2003) Hydrogen exchange kinetics of RNase A and the urea:TMAO paradigm. Biochemistry 42(19):5837-5849.
28. Panuszko A, Bruździak P, Zielkiewicz J, Wyrzykowski D, Stangret J (2009) Effects of urea and trimethylamine-N-oxide on the properties of water and the secondary structure of hen egg white lysozyme. J Phys Chem B 113(44):14797-14809.
29. Auton M, Bolen DW, Rosgen J (2008) Structural thermodynamics of protein preferential solvation: Osmolyte solvation of proteins, aminoacids, and peptides. Proteins 73(4):802-813.
30. Hamm P, Zanni MT (2011) Concepts and Methods of 2D Infrared Spectroscopy (Cambridge Univ Pres, New York), p ix.
31. Kim YS, Liu L, Axelsen PH, Hochstrasser RM (2009) 2D IR provides evidence for mobile water molecules in β-amyloid fibrils. Proc Natl Acad Sci USA 106(42):17751-17756.
32. Ma J, et al. (2013) Intrinsic structural heterogeneity and long-term maturation of amyloid β peptide fibrils. ACS Chem Neurosci 4(8):1236-1243.
33. Kuroda DG, et al. (2013) Snapshot of the equilibrium dynamics of a drug bound to HIV-1 reverse transcriptase. Nat Chem 5(3):174-181.
34. Strasfeld DB, Ling YL, Shim S-H, Zanni MT (2008) Tracking fiber formation in human islet amyloid polypeptide with automated 2D-IR spectroscopy. J Am Chem Soc 130(21):6698-6699. (Pubitemid 351748393)
35. Strasfeld DB, Ling YL, Gupta R, Raleigh DP, Zanni MT (2009) Strategies for extracting structural information from 2D IR spectroscopy of amyloid: Application to islet amyloid polypeptide. J Phys Chem B 113(47):15679-15691.
36. Ghosh A, Qiu J, DeGrado WF, Hochstrasser RM (2011) Tidal surge in the M2 proton channel, sensed by 2D IR spectroscopy. Proc Natl Acad Sci USA 108(15):6115-6120.
37. Chung JK, Thielges MC, Fayer MD (2011) Dynamics of the folded and unfolded villin headpiece (HP35) measured with ultrafast 2D IR vibrational echo spectroscopy. Proc Natl Acad Sci USA 108(9):3578-3583.
38. Bagchi S, Boxer SG, Fayer MD (2012) Ribonuclease S dynamics measured using a nitrile label with 2D IR vibrational echo spectroscopy. J Phys Chem B 116(13):4034-4042.
39. Middleton CT, et al. (2012) Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor. Nat Chem 4(5):355-360.
40. Getahun Z, et al. (2003) Using nitrile-derivatized amino acids as infrared probes of local environment. J Am Chem Soc 125(2):405-411. (Pubitemid 36077861)
41. Waegele MM, Culik RM, Gai F (2011) Site-specific spectroscopic reporters of the local electric field, hydration, structure, and dynamics of biomolecules. J Phys Chem Lett 2(20):2598-2609.
42. Pazos IM, Gai F (2012) Solute's perspective on how trimethylamine oxide, urea, and guanidine hydrochloride affect water's hydrogen bonding ability. J Phys Chem B 116(41):12473-12478.
43. Bennion BJ, Daggett V (2004) Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: A chemical chaperone at atomic resolution. Proc Natl Acad Sci USA 101(17):6433-6438. (Pubitemid 38585991)
44. Cho SS, Reddy G, Straub JE, Thirumalai D (2011) Entropic stabilization of proteins by TMAO. J Phys Chem B 115(45):13401-13407.
45. Ghosh A, Remorino A, Tucker MJ, Hochstrasser RM (2009) 2D IR photon echo spectroscopy reveals hydrogen bond dynamics of aromatic nitriles. Chem Phys Lett 469(4-6):325-330.
46. Urbanek DC, Vorobyev DY, Serrano AL, Gai F, Hochstrasser RM (2010) The two dimensional vibrational echo of a nitrile probe of the villin HP35 protein. J Phys Chem Lett 1(23):3311-3315.
47. Park K-H, et al. (2013) Infrared probes based on nitrile-derivatized prolines: Thermal insulation effect and enhanced dynamic range. J. Phys. Chem. Lett 4(13):2105-2110.
48. Kwak K, Park S, Finkelstein IJ, Fayer MD (2007) Frequency-frequency correlation functions and apodization in two-dimensional infrared vibrational echo spectroscopy: A new approach. J Chem Phys 127(12):124503.
49. Mukamel S (1995) Principles of Nonlinear Optical Spectroscopy (Oxford Univ Press, New York), p xviii.
50. Cho M (2009) Two-Dimensional Optical Spectroscopy (CRC, Boca Raton, FL), p 378.
51. Volkov VV, Palmer DJ, Righini R (2007) Distinct water species confined at the interface of a phospholipid membrane. Phys Rev Lett 99(7):078302.
52. Ghosh A, Hochstrasser RM (2011) A peptide's perspective of water dynamics. Chem Phys 390(1):1-13.
53. Chung JK, Thielges MC, Fayer MD (2012) Conformational dynamics and stability of HP35 studied with 2D IR vibrational echoes. J Am Chem Soc 134(29):12118-12124.
54. Hochstrasser RM (2001) Two-dimensional IR-spectroscopy: Polarization anisotropy effects. Chem Phys 266(2-3):273-284.
55. Huang CY, Getahun Z, Wang T, DeGrado WF, Gai F (2001) Time-resolved infrared study of the helix-coil transition using (13)C-labeled helical peptides. J Am Chem Soc 123(48):12111-12112. (Pubitemid 33135053)
56. Wang T, Du DG, Gai F (2003) Helix-coil kinetics of two 14-residue peptides. Chem Phys Lett 370(5-6):842-848. (Pubitemid 36316498)
57. Lin YS, Shorb JM, Mukherjee P, Zanni MT, Skinner JL (2008) Empirical amide I vibrational frequency map: Application to 2D-IR line shapes for isotope-edited membrane peptide bundles. J Phys Chem B 113(3):592-602.
58. Asbury JB, et al. (2004) Water dynamics: Vibrational echo correlation spectroscopy and comparison to molecular dynamics simulations. J Phys Chem A 108(7):1107-1119.
59. Canchi DR, Jayasimha P, Rau DC, Makhatadze GI, Garcia AE (2012) Molecular mechanism for the preferential exclusion of TMAO from protein surfaces. J Phys Chem B 116(40):12095-12104.
60. Hu KN, Havlin RH, Yau WM, Tycko R (2009) Quantitative determination of site-specific conformational distributions in an unfolded protein by solid-state nuclear magnetic resonance. J Mol Biol 392(4):1055-1073.
61. Chung JK, Thielges MC, Lynch SR, Fayer MD (2012) Fast dynamics of HP35 for folded and urea-unfolded conditions. J Phys Chem B 116(36):11024-11031.
62. Canchi DR, García AE (2013) Cosolvent effects on protein stability. Annu Rev Phys Chem 64(1):273-293.
63. Guinn EJ, Pegram LM, Capp MW, Pollock MN, Record MT, Jr. (2011) Quantifying why urea is a protein denaturant, whereas glycine betaine is a protein stabilizer. Proc Natl Acad Sci USA 108(41):16932-16937.
64. Cannon JG, Anderson CF, Record MT, Jr. (2007) Urea-amide preferential interactions in water: Quantitative comparison of model compound data with biopolymer results using water accessible surface areas. J Phys Chem B 111(32):9675-9685. (Pubitemid 47317896)
65. Zhang W, Capp MW, Bond JP, Anderson CF, Record MT, Jr. (1996) Thermodynamic characterization of interactions of native bovine serum albumin with highly excluded (glycine betaine) and moderately accumulated (urea) solutes by a novel application of vapor pressure osmometry. Biochemistry 35(32):10506-10516. (Pubitemid 26277310)
66. Lee S, Shek YL, Chalikian TV (2010) Urea interactions with protein groups: A volumetric study. Biopolymers 93(10):866-879.
67. Arakawa T, Timasheff SN (1982) Preferential interactions of proteins with salts in concentrated solutions. Biochemistry 21(25):6545-6552.
68. Hua L, Zhou R, Thirumalai D, Berne BJ (2008) Urea denaturation by stronger dispersion interactions with proteins than water implies a 2-stage unfolding. Proc Natl Acad Sci USA 105(44):16928-16933.
69. Kuffel A, Zielkiewicz J (2010) The hydrogen bond network structure within the hydration shell around simple osmolytes: Urea, tetramethylurea, and trimethylamine-N-oxide, investigated using both a fixed charge and a polarizable water model. J Chem Phys 133(3):035102.
70. King JT, Baiz CR, Kubarych KJ (2010) Solvent-dependent spectral diffusion in a hydrogen bonded "vibrational aggregate" J Phys Chem A 114(39):10590-10604.
71. Batchelor JD, Olteanu A, Tripathy A, Pielak GJ (2004) Impact of protein denaturants and stabilizers on water structure. J Am Chem Soc 126(7):1958-1961. (Pubitemid 38228875)
72. Doan-Nguyen V, Loria JP (2007) The effects of cosolutes on protein dynamics: The reversal of denaturant-induced protein fluctuations by trimethylamine N-oxide. Protein Sci 16(1):20-29. (Pubitemid 46036495)
73. Qu Y, Bolen DW (2002) Efficacy of macromolecular crowding in forcing proteins to fold. Biophys Chem 101-102:155-165. (Pubitemid 35462044)
74. Zangi R, Zhou R, Berne BJ (2009) Urea's action on hydrophobic interactions. J Am Chem Soc 131(4):1535-1541.
75. Kohlhoff KJ, et al. (2014) Cloud-based simulations on Google Exacycle reveal ligand modulation of GPCR activation pathways. Nat Chem 6(1):15-21.
76. Choi J-H, Cho M (2011) Vibrational solvatochromism and electrochromism of infrared probe molecules containing C≡O, C≡N, C=O, or C-F vibrational chromophore. J Chem Phys 134(15):154513.