Arginine-aromatic interactions and their effects on arginine-induced solubilization of aromatic solutes and suppression of protein aggregation

Biotechnology Progress

Volumn 28, Issue 1, 2012, Pages 223-231

  Shah, Dhawal ^a,d   Li, Jianguo ^a,b   Shaikh, Abdul Rajjak ^a,c   Rajagopalan, Raj ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SINGAPORE EYE RESEARCH INSTITUTE   (Singapore)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^d MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

Author keywords

Arginine; Preferential interaction coefficient; Protein aggregation

Indexed keywords

ACIDIC RESIDUES; AROMATIC MOIETIES; AROMATIC RESIDUES; AROMATIC SOLUTES; MODEL SYSTEM; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR MECHANISM; PREFERENTIAL INTERACTION; PROTEIN AGGREGATION;

ARGININE; AROMATIZATION; ENZYMES; INSULIN; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PEPTIDES; SOLUBILITY;

AROMATIC COMPOUNDS;

ARGININE; AROMATIC AMINO ACID; INSULIN; LYSOZYME; PEPTIDE; PROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; MOLECULAR DYNAMICS; PROTEIN DENATURATION; SOLUBILITY; SOLUTION AND SOLUBILITY;

AMINO ACIDS, AROMATIC; ARGININE; INSULIN; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MURAMIDASE; PEPTIDES; PROTEIN DENATURATION; PROTEINS; SOLUBILITY; SOLUTIONS;

EID: 84856569138     PISSN: 87567938     EISSN: 15206033     Source Type: Journal    
DOI: 10.1002/btpr.710     Document Type: Article

References (66)

1. Bondos SE, Bicknell A. Detection and prevention of protein aggregation before, during, and after purification. Anal Biochem. 2003; 316: 223-231.
2. Shastry BS. Neurodegenerative disorders of protein aggregation. Neurochem Int. 2003; 43: 1-7.
3. Taylor JP, Hardy J, Fischbeck KH. Toxic proteins in neurodegenerative disease. Science. 2002; 296: 1991-1995.
4. Wang W. Protein aggregation and its inhibition in biopharmaceutics. Int J Pharm. 2005; 289: 1-30.
5. Tsumoto K, Umetsu M, Kumagai I, Ejima D, Philo JS, Arakawa T. Role of arginine in protein refolding, solubilization, and purification. Biotechnol Prog. 2004; 20: 1301-1308.
6. Xie Q, Guo T, Lu J, Zhou H-M. The guanidine like effects of arginine on aminoacylase and salt-induced molten globule state. Int J Biochem Cell Biol. 2004; 36: 296-306.
7. Ishibashi M, Tsumoto K, Tokunaga M, Ejima D, Kita Y, Arakawa T. Is arginine a protein-denaturant? Protein Expr Purif. 2005; 42: 1-6.
8. Liu Y-D, Li J-J, Wang F-W, Chen J, Li P, Su Z-G. A newly proposed mechanism for arginine-assisted protein refolding-not inhibiting soluble oligomers although promoting a correct structure. Protein Expr Purif. 2007; 51: 235-242.
9. Kudou M, Ejima D, Sato H, Yumioka R, Arakawa T, Tsumoto K. Refolding single-chain antibody (scFv) using lauroyl-L-glutamate as a solubilization detergent and arginine as a refolding additive. Protein Expr Purif. 2011; 77: 68-74.
10. Golovanov AP, Hautbergue GM, Wilson SA, Lian L-Y. A simple method for improving protein solubility and long-term stability. J Am Chem Soc. 2004; 126: 8933-8939.
11. Tsumoto K, Abe R, Ejima D, Arakawa T. Non-denaturing solubilization of inclusion bodies. Curr Pharm Biotechnol. 2010; 11: 309-312.
12. Tsumoto K, Ejima D, Kita Y, Arakawa T. Review: why is arginine effective in suppressing aggregation? Protein Pept Lett. 2005; 12: 613-619.
13. Ignatova Z, Gierasch LM. Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant. Proc Natl Acad Sci USA. 2006; 103: 13357-13361.
14. Shukla D, Trout BL. Preferential interaction coefficients of proteins in aqueous arginine solutions and their molecular origins. J Phys Chem B. 2011; 115: 1243-1253.
15. Baier SK, Decker EA, McClements DJ. Impact of glycerol on thermostability and heat-induced gelation of bovine serum albumin. Food Hydrocoll. 2004; 18: 91-100.
16. Baier SK, McClements DJ. Impact of sorbitol on the thermostability and heat-induced gelation of bovine serum albumin. Food Res Int. 2003; 36: 1081-1087.
17. Shukla D, Shinde C, Trout BL. Molecular computations of preferential interaction coefficients of proteins. J Phys Chem B. 2009; 113: 12546-12554.
18. Schneider CP, Trout BL. Investigation of cosolute-protein preferential interaction coefficients: new insight into the mechanism by which arginine inhibits aggregation. J Phys Chem B. 2009; 113: 2050-2058.
19. Gekko K, Timasheff SN. Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry. 1981; 20: 4667-4676.
20. Lin TY, Timasheff SN. On the role of surface tension in the stabilization of globular proteins. Protein Sci. 1996; 5: 372-381.
21. Courtenay ES, Capp MW, Saecker RM, Record MT Jr. Thermodynamic analysis of interactions between denaturants and protein surface exposed on unfolding: interpretation of urea and guanidinium chloride m-values and their correlation with changes in accessible surface area (ASA) using preferential interaction coefficients and the local-bulk domain model. Proteins 2000; ( Suppl 4): 72-85.
22. Kita Y, Arakawa T, Lin T-Y, Timasheff SN. Contribution of the surface free energy perturbation to protein-solvent interactions. Biochemistry. 1994; 33: 15178-15189.
23. Hamada H, Arakawa T, Shiraki K. Effect of additives on protein aggregation. Curr Pharm Biotechnol. 2009; 10: 400-407.
24. Matsuoka T, Tomita S, Hamada H, Shiraki K. Amidated amino acids are prominent additives for preventing heat-induced aggregation of lysozyme. J Biosci Bioeng. 2007; 103: 440-443.
25. Hamada H, Shiraki K. L-Argininamide improves the refolding more effectively than L-arginine. J Biotechnol. 2007; 130: 153-160.
26. Baynes BM, Trout BL. Rational design of solution additives for the prevention of protein aggregation. Biophys J. 2004; 87: 1631-1639.
27. Das U, Hariprasad G, Ethayathulla AS, Manral P, Das TK, Pasha S, Mann A, Ganguli M, Verma AK, Bhat R, Chandrayan SK, Ahmed S, Sharma S, Kaur P, Singh TP, Srinivasan A. Inhibition of protein aggregation: supramolecular assemblies of arginine hold the key. PLoS One. 2007; 2: e1176.
28. Ghosh R, Sharma S, Chattopadhyay K. Effect of arginine on protein aggregation studied by fluorescence correlation spectroscopy and other biophysical methods. Biochemistry. 2009; 48: 1135-1143.
29. Arakawa T, Ejima D, Tsumoto K, Obeyama N, Tanaka Y, Kita Y, Timasheff SN. Suppression of protein interactions by arginine: a proposed mechanism of the arginine effects. Biophys Chem. 2007; 127: 1-8.
30. Ariki R, Hirano A, Arakawa T, Shiraki K. Arginine increases the solubility of alkyl gallates through interaction with the aromatic ring. J Biochem. 2011; 149: 389-394.
31. Hirano A, Kameda T, Arakawa T, Shiraki K. Arginine-assisted solubilization system for drug substances: solubility experiment and simulation. J Phys Chem B. 2010; 114: 13455-13462.
32. Hirano A, Arakawa T, Shiraki K. Arginine increases the solubility of coumarin: comparison with salting-in and salting-out additives. J Biochem. 2008; 144: 363-369.
33. Baynes BM, Trout BL. Protein in mixed solvents: a molecular-level perspective. J Phys Chem B. 2003; 107: 14058-14067.
34. Humphrey W, Dalke A, Schulten K. VMD - Visual Molecular Dynamics. J Mol Graph. 1996; 14: 33-38.
35. Arakawa T, Tsumoto K. The effects of arginine on refolding of aggregated proteins: not facilitate refolding, but suppress aggregation. Biochem Biophys Res Commun. 2003; 304: 148-152.
36. Tantipolphan R, Romeijn S, Engelsman Jd, Torosantucci R, Rasmussen T, Jiskoot W. Elution behavior of insulin on high-performance size exclusion chromatography at neutral pH. J Pharma Biomed Anal. 2010; 52: 195-202.
37. Baynes BM, Wang DIC, Trout BL. Role of arginine in the stabilization of proteins against aggregation. Biochemistry. 2005; 44: 4919-4925.
38. Li J, Garg M, Shah D, Rajagopalan R. Solubilization of aromatic and hydrophobic moieties by arginine in aqueous solutions. J Chem Phys. 2010; 133: 054902.
39. Timasheff SN, Xie G. Preferential interactions of urea with lysozyme and their linkage to protein denaturation. Biophys Chem. 2003; 105: 421-448.
40. Parsegian VA, Rand RP, Rau DC. Osmotic stress, crowding, preferential hydration, and binding: a comparison of perspective. Proc Natl Acad Sci USA. 2000; 97: 3987-3992.
41. Tateno M, Hagiwara Y. Evaluation of stabilization energies in π-π and cation-π interactions involved in biological macromolecules by ab initio calculations. J Phys Condens Matter. 2009; 21: 064243.
42. Stumpe MC, Grubmuller H. Interaction of urea with amino acids: implications for urea-induced protein denaturation. J Am Chem Soc. 2007; 129: 16126-16131.
43. Lyutova EM, Kasakov AS, Gurvits BY. Effects of arginine on kinetics of protein aggregation studied by dynamic laser light scattering and tubidimetry techniques. Biotechnol Prog. 2007; 23: 1411-1416.
44. Okanojo M, Shiraki K, Kudou M, Nishikori S, Takagi M. Diamines prevent thermal aggregation and inactivation of lysozyme. J Biosci Bioeng. 2005; 100: 556-561.
45. Melo A, Ramos MJ, Floriano WB, Gomes JANF, Leão JFR, Magalhães AL, Maigret B, Nascimento MC, Reuter N. Theoretical study of arginine-carboxylate interactions. J Mol Struct Theochem. 1999; 463: 81-90.
46. Shah D, Shaikh AR, Peng X, Rajagopalan R. Effects of arginine on heat-induced aggregation of concentrated protein solutions. Biotechnol Prog. 2011; 27: 513-520.
47. Shukla D, Trout BL. Interaction of arginine with proteins and the mechanism by which it inhibits aggregation. J Phys Chem B. 2010; 114: 13426-13438.
48. Dhe-Paganon S, Werner ED, Nishi M, Hansen L, Chi Y-I, Shoelson SE. A phenylalanine zipper mediates APS dimerization. Nat Struct Mol Biol. 2004; 11: 968-974.
49. Liu J, Yong W, Deng Y, Kallenbach NR, Lu M. Atomic structure of a tryptophan-zipper pentamer. Proc Natl Acad Sci USA. 2004; 101: 16156-16161.
50. Ma B, Nussinov R. Trp/Met/Phe Hot spots in protein-protein interactions: potential targets in drug design. Curr Top Med Chem. 2007; 7: 999-1005.
51. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, Thompson MJ, Balbirnie M, Wiltzius JJW, McFarlane HT, Madsen AO, Riekel C, Eisenberg D. Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature. 2007; 447: 453-457.
52. Wang W, Nema S, Teagarden D. Protein aggregation-pathways and influencing factors. Int J Pharm. 2010; 390: 89-99.
53. Flocco MM, Mowbray SL. Planar stacking interactions of arginine and aromatic side-chains in proteins. J Mol Biol. 1994; 235: 709-717.
54. Martis RL, Singh SK, Gromiha MM, Santhosh C. Role of cation-π interactions in single chain 'all-alpha' proteins. J Theor Biol. 2008; 250: 655-662.
55. Beene DL, Brandt GS, Zhong WG, Zacharias NM, Lester HA, Dougherty DA. Cation-pi interactions in ligand recognition by serotonergic (5-HT3A) and nicotinic acetylcholine receptors: the anomalous binding properties of nicotine. Biochemistry. 2002; 41: 10262-10269.
56. Beene DL, Price KL, Lester HA, Dougherty DA, Lummis SCR. Tyrosine residues that control binding and gating in the 5-hydroxytryptamine(3) receptor revealed by unnatural amino acid mutagenesis. J Neurosci. 2004; 24: 9097-9104.
57. Dougherty DA. Cation-π interactions involving aromatic amino acids. J Nutr. 2007; 137: 1504S-1508S.
58. Gallivan JP, Dougherty DA. Can lone pairs bind to a pi system? The water center dot center dot center dot hexafluorobenzene interaction. Org Lett. 1999; 1: 103-105.
59. Gallivan JP, Dougherty DA. Cation-pi interactions in structural biology. Proc Natl Acad Sci USA. 1999; 96: 9459-9464.
60. Gallivan JP, Dougherty DA. A computational study of cation-pi interactions vs salt bridges in aqueous media: implications for protein engineering. J Am Chem Soc. 2000; 122: 870-874.
61. Crowley PB, Golovin A. Cation-pi interactions in protein-protein interfaces. Prot Struct Funct Bioinform. 2005; 59: 231-239.
62. Dempsey CE, Piggot TJ, Mason PE. Dissecting contributions to the denaturant sensitivities of proteins. Biochemistry. 2004; 44: 775-781.
63. Mason PE, Brady JW, Neilson GW, Dempsey CE. The interaction of guanidinium ions with a model peptide. Biophys J. 2007; 93: L04-L06.
64. Mason PE, Neilson GW, Enderby JE, Saboungi M-L, Dempsey CE, MacKerell AD, Brady JW. The structure of aqueous guanidinium chloride solutions. J Am Chem Soc. 2004; 126: 11462-11470.
65. Vondrasek J, Mason PE, Heyda J, Collins KD, Jungwirth P. The molecular origin of like-charge arginine-arginine pairing in water. J Phys Chem B. 2009; 113: 9041-9045.
66. Arakawa T, Bhat R, Timasheff SN. Why preferential hydration does not always stabilize the native structure of globular proteins. Biochemistry. 1990; 29: 1924-1931.