Quantifying Steric and Hydrophobic Influence of Non-Standard Amino Acids in Proteins That Undergo Post-Translational Modifications
Non-standard amino acids in protein post-translational modifications aid in a wide variety of biological functions and processes, furnishing expansion from the genome to the proteome. First, from structural examinations in unmodified proteins with only standard amino acids, this work empirically obtains numeric relations that reveal how instruction transfers occur between native-state structures. Next, from these relations, the influence of non-standard amino acids inside post-translationally modified proteins is quantified by successfully predicting the contents of large and hydrophobic residues in helices and β-strands for 210 inspections performed. This suggests a twofold molecular mechanism by the fundamental biophysicochemical properties (residue volume and hydrophobicity), and concludes that the utilized non-standard amino acids have limited global influence at the residue level. Our prediction method provides a better underlying understanding of molecular interactions and mechanisms, and is particularly promising in terms of surveying further modified proteins.
Luiz F. O. Rocha,
Quantifying Steric and Hydrophobic Influence of Non-Standard Amino Acids in Proteins That Undergo Post-Translational Modifications, Biochemistry and Molecular Biology.
Vol. 2, No. 2,
2017, pp. 12-24.
C. T. Walsh, S. Garneau-Tsodikova, G. J. Gatto Jr., Protein Posttranslational Modifications: The Chemistry of Proteome Diversifications, Angew. Chem. Int. Ed. 44, 2005, 7342–7372.
Y. Tweedie-Cullen, I. M. Mansuy, Towards a better understanding of nuclear processes based on proteomics, Amino Acids 39, 2010, 1117–1130.
O. N. Jensen, Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry, Curr. Opin. Chem. Biol. 8, 2004, 33–41.
J. Seo, K. J. Lee, Post-translational Modifications and Their Biological Functions: Proteomic Analysis and Systematic Approaches, J. Biochem. Mol. Biol. 37, 2004, 35–44.
E. S. Groban, A. Narayanan, M. P. Jacobson, Conformational Changes in Protein Loops and Helices Induced by Post-Translational Phosphorylation, PLoS Comput. Biol. 2, 2006, 0238–0250.
J. H. McKerrow, E. Sun, P. J. Rosenthal, The proteases and pathogenicity of parasitic protozoa, Annu. Rev. Microbiol. 47, 1993, 821–853.
C. Drouet, A. Désormeaux, J. Robillard, D. Ponard, L. Bouillet, L. Martin, G. Kanny, D. A. M. Vautrin, J. L. Bosson, J. L. Quesada, M. L. Trascasa, A. Adam, Metallopeptidase activities in hereditary angioedema: Effect of androgen prophylaxis on plasma aminopeptidase P, J. Allergy Clin. Immunol. 121, 2008, 429–433.
S. J. Dunne, R. B. Cornell, J. E. Johnson, N. R. Glove, A. S. Tracey, Structure of the membrane binding domain of CTP: Phosphocholine Cytidylyltransferase, Biochemistry 35, 1996, 11975–11984.
P. Savarin, R. Romi-Lebrun, S. Zinn-Justin, B. Lebrun, T. Nakajima, B. Gilquin, A. Ménez, Structural and functional consequences of the presence of a fourth disulfide bridge in the scorpion short toxins: Solution structure of the potassium channel inhibitor HsTX1, Prot. Scien. 8, 1999, 2672–2685.
K. D. Hapner, P. E. Wilcox, Fragmentation of bovine chymotrypsinogen A and chymotrypsin A. Specific cleavage at arginine and methionine residues and separation of peptides, including B and C chains of chymotrypsin, Biochemistry 9, 1970, 4470–4480.
V. Serval, T. Galli, A. Cheramy, J. Glowinski, S. Lavielle, In vitro and in vivo inhibition of N-acetyl-L-aspartyl-L-glutamate catabolism by N-acylated L-glutamate analogs, J. Pharmacol. Exp. Ther. 260, 1992, 1093–1100.
M. W. Pennington, M. D. Lanigan, K. Kalman, V. M. Mahnir, H. Rauer, C. T. McVaugh, D. Behm, D. Donaldson, K. G. Chandy, W. R. Kem, R. S. Norton, Role of disulfide bonds in the structure and potassium channel blocking activity of ShK toxin, Biochemistry 38, 1999, 14549–14558.
L. Carrega, A. Mosbah, G. Ferrat, C. Beeton, N. Andreotti, P. Mansuelle, H. Darbon, M. D. Waard, J. M. Sabatier, The impact of the fourth disulfide bridge in scorpion toxins of the α-KTx6 subfamily, Proteins 61, 2005, 1010–1023.
K. Kalman, M. W. Pennington, M. D. Lanigan, A. Nguyen, H. Rauer, V. Mahniri, K. Paschetto, W. R. Kem, S. Grissmer, G. A. Gutman, E. P. Christian, M. D. Cahalan, R. S. Norton, K. G. Chandy, ShK-Dap22, a potent Kv1.3-specific immunosuppressive polypeptide, J. Biol. Chem. 273, 1998, 32697–32707.
J. Venkatraman, G. A. N. Gowda, P. Balaram, Design and construction of an open multistranded β-sheet polypeptide stabilized by a disulfide bridge, J. Am. Chem. Soc. 124, 2002, 4987–4994.
P. B. Harbury, J. J. Plecs, B. Tidor, T. Alber, P. S. Kim, high-resolution protein design with backbone freedom, Science 282, 1998, 1462–1467.
T. K. Chiu, J. Kubelka, R. Herbst-Irmer, W. A. Eaton, J. Hofrichter, D. R. Davies, High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein, Proc. Natl. Acad. Sci. USA 102, 2005, 7517–7522.
J. I. Fletcher, A. J. Dingley, R. Smith, M. Connor, M. J. Christie, G. F. King, High-resolution solution structure of gurmarin, a sweet-taste-suppressing plant polypeptide, Eur. J. Biochem. 264, 1999, 525–533.
Y. C. Lou, Y. C. Huang, Y. R. Pan, C. Chen, Y. D. Liao, Roles of N-terminal pyroglutamate in maintaining structural integrity and pKa values of catalytic histidine residues in bullfrog ribonuclease 3, J. Mol. Biol. 355, 2006, 409–421.
E. S. Witze, W. M. Old, K. A. Resing, N. G. Ahn, Mapping protein post-translational modifications with mass spectrometry, Nat. Methods 4(10), 2007, 798–806.
F. C. Bernstein, T. F. Koetzle, G. J. B. Williams, E. F. Meyer Jr., M. D. Brice, J. R. Rodgers, O. Kennard, T. Shimanouchi, M. Tasumi, The protein data bank: A computer-based archival file for macromolecular structures, Eur. J. Biochem. 80, 1977, 319–324.
M. I. Sadowski, D. T. Jones, The sequence–structure relationship and protein function prediction, Curr. Opin. Struct. Biol. 19, 2009, 357–362.
W. Taylor, The classification of amino acid conservation, J. Theor. Biol. 119, 1986, 205–218.
G. E. Schulz, R. H. Schirmer, Noncovalent forces determining protein structure, in: C. R. Cantor (Ed.), Principles of Protein Structure, Springer-Verlag, New York, 1990, 27–45.
R. Srinivasan, G. D. Rose, LINUS: A hierarchic procedure to predict the fold of a protein, Proteins 19, 1995, 81–99.
L. F. O. Rocha, I. R. Silva, A. Caliri, Distinct conformational properties determined by implicit and explicit representation of protein-solvent interactions. An analytical and computer simulation study, Phys. A 388, 2009, 4097–4104.
H. Goodarzi, A. Katanforoush, N. Torabi, H. S. Najafabadi, Solvent accessibility, residue charge and residue volume, the three ingredients of a robust amino acid substitution matrix, J. Theor. Biol. 245, 2007, 715–725.
A. A. Zamyatnin, Protein volume in solution, Progr. Biophys. Mol. Biol. 24, 1972, 107–123.
C. Chothia, Structural invariants in protein folding, Nature 254, 1975, 304–308.
S. Moelbert, E. Emberly, C. Tang, Correlation between sequence hydrophobicity and surface-exposure pattern of database proteins, Protein Sci. 13, 2004, 752–762.
L. F. O. Rocha, M. E. P. Tarragó, A. Caliri, The water factor in the protein-folding problem, Braz. J. Phys. 34, 2004, 90–101.
E. G. Hutchinson, J. M. Thornton, PROMOTIF-A program to identify and analyze structural motifs in proteins, Protein Sci. 5, 1996, 212–220.
N. Bhardwaj, M. Gerstein, Relating protein conformational changes to packing efficiency and disorder, Prot. Sci. 18, 2009, 1230–1240.
R. Sreekanth, S. S. Rajan, The study of helical distortions due to environmental changes: Choice of parameters, Biophys. Chem. 125, 2007, 191–200.
T. Haltia, E. Freire, Forces and factors that contribute to the structural stability of membrane proteins, Biochim. Biophys. Acta 1228, 1995, 1–27.
K. E. Kawulka, T. Sprules, C. M. Diaper, R. M. Whittal, R. T. McKay, P. Mercier, P. Zuber, J. C. Vederas, Structure of subtilosin A, a cyclic antimicrobial peptide from bacillus subtilis with unusual sulfur to α-carbon cross-links: Formation and reduction of α-thio-α-amino acid derivatives, Biochemistry 43, 2004, 3385–3395.
H. Takahashi, J. I. Kim, H. J. Min, K. S. Kenton, J. Swartz, I. Shimada, Solution structure of hanatoxin1, a gating modifier of voltage-dependent K+ channels: Common surface features of gating modifier toxins, J. Mol. Biol. 297, 2000, 771–780.
D. J. Taylor, J. Nilsson, A. R. Merrill, G. R. Andersen, P. Nissen, J. Frank, Structures of modified eEF2.80S ribosome complexes reveal the role of GTP hydrolysis in translocation, Embo J. 26, 2007, 2421–2431.
K. Peng, Q. Shu, Z. Liu, S. Liang, Function and solution structure of huwentoxin-IV, a potent neuronal tetrodotoxin (TTX)-sensitive sodium channel antagonist from chinese bird spider celenocosmia huwena, J. Biol. Chem. 277, 2002, 47564–47571.
S. Borra, A. D. Ciaccio, Measuring the prediction error. A comparison of cross-validation, bootstrap and covariance penalty methods, Comput. Statist. Dat. Analys. 54, 2010, 2976–2989.
L. F. O. Rocha, Analysis of molecular structures and mechanisms for toxins derived from venomous animals, Comput. Biol. Chem. 61, 2016, 8–14.
L. F. O. Rocha, Toward a better understanding of structural divergences in proteins using different secondary structure assignment methods, J. Mol. Struct. 1063, 2014, 242–250.
R. M. Hanson, Jmol – a paradigm shift in crystallographic visualization, J. Appl. Cryst. 43, 2010, 1250–1260.
J. M. Thornton, Protein structures: The end point of the folding pathway, in: T. E. Creighton (Ed.), Protein Folding, W. H. Freeman and Company, New York, 1992, 59–81.
B. Li, M. Lin, Q. Liu, Y. Li, C. Zhou, Protein folding optimization based on 3D off-lattice model via an improved artificial bee colony algorithm, J. Mol. Model. 21, 2015, 261–1–15.
F. L. Custódio, H. J. C. Barbosa, L. E. Dardenne, A multiple minima genetic algorithm for protein structure prediction, Appl. Soft Comput. 15, 2014, 88–99.
J. Santos, P. Villot, M. Diéguez, Emergent Protein Folding Modeled with Evolved Neural Cellular Automata Using the 3D HP Model, J. Comp. Biol. 21, 2014, 823–845.
A. Irbäck, J. Wessén, Thermodynamics of amyloid formation and the role of intersheet interactions, J. Chem. Phys. 143, 2015, 105104–1–9.
H. I. Ingólfsson, C. A. Lopez, J. J. Uusitalo, D. H. Jong, S. M. Gopal, X. Periole, S. J. Marrink, The power of coarse graining in biomolecular simulations, WIREs Comput. Mol. Sci. 4, 2014, 225–248.
W. Li, H. Yoshii, N. Hori, T. Kameda, S. Takada, Multiscale methods for protein folding simulations, Methods 52, 2010, 106–114.
T. J. Richmond, Solvent accessible surface area and excluded volume in proteins: Analytical equations for overlapping spheres and implications for the hydrophobic effect, J. Mol. Biol. 178, 1984, 63–89.
E. Kussell, J. Shimada, E. I. Shakhnovich, Excluded volume in protein side-chain packing, J. Mol. Biol. 311, 2001, 183–193.
L. R. Pratt, Molecular Theory of hydrophobic effects:“She is too mean to have her name repeated.”, Annu. Rev. Phys. Chem. 53, 2002, 409–436.
G. E. Crooks, J. Wolfe, S. E. Brenner, Measurements of protein sequence–structure correlations. Proteins, Proteins 57, 2004, 804–810.
K. Sobha, C. Kanakaraju, K. S. K. Yadav, Is protein structure prediction still an enigma?, Afr. J. Biotechnol. 7, 2008, 4687–4693.
C. Benros, A. G. Brevern, S. Hazout, Analyzing the sequence-structure relationship of a library of local structural prototypes, J. Theor. Biol. 256, 2009, 215–226.
A. M. Gutin, V. I. Abkevich, E. I. Shakhnovich, Is burst hydrophobic collapse necessary for protein folding?, Biochemistry 34, 1995, 3066–3076.
B. Nölting, D. A. Agard, How general is the nucleation–condensation mechanism? Proteins 73, 2008, 754–764.
D. R. Livesay, S. Dallakyan, G. G. Wood, D. J. Jacobs, A flexible approach for understanding protein stability, FEBS Lett. 576, 2004, 468–476.
K. Fan, W. Wang, What is the minimum number of letters required to fold a protein?, J. Mol. Biol. 328, 2003, 921–926.
A. Yamaguchi, K. Iida, N. Matsui, S. Tomoda, K. Yura, M. Go, Het-PDB Navi.: A database for protein–small molecule interactions, J. Biochem. 135, 2004, 79–84.
G. J. Kleywegt, Crystallographic refinement of ligand complexes, Acta Cryst. D63, 2007, 94–100.