Hypervalent nonbonded interactions of a divalent sulfur atom. Implications in protein architecture and the functions

Molecules

Volumn 17, Issue 6, 2012, Pages 7266-7283

  Iwaoka, Michio ^a   Isozumi, Noriyoshi ^a  

^a TOKAI UNIVERSITY   (Japan)

Author keywords

Hole bonds; Chalcogen bonds; Drug design; Molecular assembly; Protein data bank; Protein engineering

Indexed keywords

ORGANIC COMPOUND; PROTEIN; SULFUR;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PROTEIN DATABASE; REVIEW;

ANIMALS; DATABASES, PROTEIN; HUMANS; MOLECULAR STRUCTURE; ORGANIC CHEMICALS; PROTEINS; SULFUR;

EID: 84862996200     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules17067266     Document Type: Review

References (75)

1. Ciuffarin, E.; Guaraldi, G. Nucleophilic substitution at dicoordinated sulfur. Effect of the leaving group on the reaction between triphenylmethyl sulfenyl derivatives and n-butylamine. J. Org. Chem. 1970, 35, 2006-2010.
2. Rosenfield, R. E., Jr.; Parthasarathy, R.; Dunitz, J. D. Directional preferences of nonbonded atomic contacts with divalent sulfur. 1. Electrophiles and nucleophiles. J. Am. Chem. Soc. 1977, 99, 4860-4862.
3. Row, T. N. G.; Parthasarathy, R. Directional preferences of nonbonded atomic contacts with divalent sulfur in terms of its orbital orientations. 2. S···S interactions and nonspherical shape of sulfur in crystals. J. Am. Chem. Soc. 1981, 103, 477-479.
4. Desiraju, G. R.; Nalini, V. Database analysis of crystal-structure- determining interactions involving sulphur: Implications for the design of organic metals. J. Mater. Chem. 1991, 1, 201-203.
5. Turbiez, M.; Frère, P.; Allain, M.; Videlot, C.; Ackermann, J.; Roncali, J. Design of organic semiconductors: Tuning the electronic properties of π-conjugated oligothiophenes with the 3, 4-ethylenedioxythiophene (EDOT) building block. Chem. Eur. J. 2005, 11, 3742-3752. (Pubitemid 40819454)
6. Réthoré, C.; Madalan, A.; Fourmigué, M.; Canadell, E.; Lopes, E. B.; Almeida, M,; Clérac, R.; Avarvari, N. O···S vs. N···S intramolecular nonbonded interactions in neutral and radical cation salts of TTF-oxazoline derivatives: synthesis, theoretical investigations, crystalline structures, and physical properties. New J. Chem. 2007, 31, 1468-1483. (Pubitemid 47174158)
7. Burling, F. T.; Goldstein, B. M. Computational studies of bonbonded sulfur-oxygen and seleniumoxygen interactions in the thiazole and selenazole nucleosides. J. Am. Chem. Soc. 1992, 114, 2313-2320.
8. Nagao, Y.; Hirata, T.; Goto, S.; Sano, S.; Kakehi, A.; Iizuka, K.; Shiro, M. Intramolecular nonbonded S···O interaction recognized in (acylimino) thiadiazoline derivatives as angiotensin II receptor antagonists and related compounds. J. Am. Chem. Soc. 1998, 120, 3104-3110. (Pubitemid 28204523)
9. Nakanishi, W.; Nakamoto, T.; Hayashi, S.; Sasamori, T.; Tokitoh, N. Atoms-in-molecules analysis of extended hypervalent five-center, six-electron (5c-6e) C2Z2O interactions at the 1, 8, 9-positions of anthraquinone and 9-methoxyanthracene systems. Chem. Eur. J. 2007, 13, 255-268. (Pubitemid 46033870)
10. Bleiholder, C.; Werz, D. B.; Köppel, H.; Gleiter, R. Theoretical investigations on chalcogenchalcogen interactions: What makes these nonbonded interactions bonding? J. Am. Chem. Soc. 2006, 128, 2666-2674. (Pubitemid 43327946)
11. Dahaoui, S.; Pichon-Pesme, V.; Howard, J. A. K.; Lecomte, C. CCD charge density study on crystals with large unit cell parameters: The case of hexagonal L-cystine. J. Phys. Chem. A 1999, 103, 6240-6250. (Pubitemid 129571114)
12. Nauser, T.; Jacoby, M.; Koppenol, W. H.; Squier, T. C.; Schöneich, C. Calmodulin methionine residues are targets for one-electron oxidation by hydroxyl radicals: Formation of S... N three-electron bonded radical complexes. Chem. Commun. 2005, 587-589. (Pubitemid 40299041)
13. Mishra, B.; Sharma, A.; Naumov, S.; Priyadarsini, K. I. Novel reactions of one-electron oxidized radicals of selenomethionine in comparison with methionine. J. Phys. Chem. B 2009, 113, 7709-7715.
14. Zhang, Y.; Wang, W. Z. The bifurcate chalcogen bond: Some theoretical observations. J. Mol. Struct. (Theochem) 2009, 916, 135-138.
15. Zhao, Q.; Feng, D. C.; Sun, Y. M.; Hao, J. C.; Cai, Z. T. Theoretical investigations on the weak nonbonded C=S···CH2 interactions: Chalcogen-bonded complexes with singlet carbene as an electron donor. Int. J. Quantum Chem. 2011, 111, 3881-3887.
16. Pal, D.; Chakrabarti, P. Non-hydrogen bond interactions involving the methionine sulfur atom. J. Biomol. Struct. Dynam. 2001, 19, 115-128. (Pubitemid 32844643)
17. Iwaoka, M.; Takemoto, S.; Okada, M.; Tomoda, S. Statistical characterization of nonbonded S···O interactions in proteins. Chem. Lett. 2001, 132-133.
18. Iwaoka, M.; Takemoto, S.; Okada, M.; Tomoda, S. Weak nonbonded S···X (X=O, N, and S) interactions in proteins. Statistical and theoretical studies. Bull. Chem. Soc. Jpn. 2002, 75, 1611-1625.
19. Iwaoka, M.; Takemoto, S.; Tomoda, S. Statistical and theoretical investigations on the directionality of nonbonded S···O interactions. Implications for molecular design and protein engineering. J. Am. Chem. Soc. 2002, 124, 10613-10620. (Pubitemid 34977414)
20. Iwaoka, M.; Isozumi, N. Possible roles of S···O and S···N interactions in the functions and evolution of phospholipase A Biophysics 2006, 2, 23-34.
21. Carugo, O. Stereochemistry of the interaction between methionine sulfur and the protein core. Biol. Chem. 1999, 380, 495-498. (Pubitemid 29204319)
22. Bhattacharyya, R.; Pal, D.; Chakrabarti, P. Disulfide bonds, their stereospecific environment and conservation in protein structures. Protein Eng. Des. Sel. 2004, 17, 795-808. (Pubitemid 40313673)
23. Lu, J. M.; Lu, Y. X.; Yang, S. B.; Zhu, W. L. Theoretical and crystallographic data investigations of noncovalent S···O interactions. Struct. Chem. 2011, 22, 757-763.
24. Murray, J. S.; Lane, P.; Politzer, P. Simultaneous s-hole and hydrogen bonding by sulfur-and selenium-containing heterocycles. Int. J. Quantum Chem. 2008, 108, 2770-2781.
25. Wang, W. Z.; Ji, B. M.; Zhang, Y. Chalcogen bond: A sister noncovalent bond to halogen bond. J. Phys. Chem. A 2008, 113, 8132-8135.
26. Allen, F. H. The Cambridge Structural Database: A quarter of a million crystal structures and rising. Acta Crystallogr. 2003, B58, 380-388. (Pubitemid 135702674)
27. Kucsman, A.; Kapovits, I. Nonbonded Sulfur-Oxygen Interaction in Organic Sulfur Compounds. In Organic Sulfur Chemistry; Bernardi, F., Csizmadia, I. G., Mangini, A., Eds.; Elsevier: Amsterdam, The Netherlands, 1985; pp. 191-245.
28. Zauhar, R. J.; Colbert, C. L.; Morgan, R. S.; Welsh, W. J. Evidence for a strong sulfur-aromatic interaction derived from crystallographic data. Biopolymers 2000, 53, 233-248. (Pubitemid 30082310)
29. Cozzolino, A. F.; Vargas-Baca, I.; Mansour, S.; Mahmoudkhani, A. H. The nature of the supramolecular association of 1, 2, 5-chalcogenadiazoles. J. Am. Chem. Soc. 2005, 127, 3184-3190.
30. Nakanishi, W.; Hayashi, S.; Narahara, K. Atoms-in-molecules dual parameter analysis of weak to strong interactions: Behaviors of electronic energy densities versus Laplacian of electron densities at bond critical points. J. Phys. Chem. A 2008, 112, 13593-13599.
31. Scheiner, S. On the properties of X···N noncovalent interactions for first-, second-, and third-row X atoms. J. Chem. Phys. 2011, 134, 164313.
32. Adhikari, U.; Scheiner, S. The S···N noncovalent interaction: Comparison with hydrogen and halogen bonds. Chem. Phys. Lett. 2011, 514, 36-39.
33. Nagao, Y.; Honjo, T.; Iimori, H.; Goto, S.; Sano, S.; Shiro, M.; Yamaguchi, K.; Sei, Y. Intramolecular nonbonded S···O interaction in acetazolamide and thiadiazolinethione molecules in their dimeric crystalline structures and complex crystalline structures with enzymes. Tetrahedron Lett. 2004, 45, 8757-8761. (Pubitemid 39421490)
34. Esparza-Ruiz, A.; Peña-Hueso, A.; Hernández-Díaz, J.; Flores-Parra, A.; Contreras, R. Effect of weak sulfur interactions and hydrogen bonds in the folded or unfolded conformation of bis 2-(1H-benzimidazol-2-yl) phenyl disulfide derivatives. Cryst. Growth Des. 2007, 7, 2031-2040.
35. González, F. V.; Jain, A.; Rodríguez, S.; Sáez, J. A.; Vicent, C.; Peris, G. Stereoisomerization of β-hydroxy-α- sulfenyl-γ-butyrolactones controlled by two concomitant 1, 4-Type nonbonded sulfur-oxygen interactions as analyzed by X-ray crystallography. J. Org. Chem. 2010, 75, 5888-5894.
36. Shishkin, O. V.; Omelchenko, I. V.; Kalyuzhny, A. L.; Paponov, B. V. Intramolecular S···O chalcogen bond in thioindirubin. Struct. Chem. 2010, 21, 1005-1011.
37. Dobson, C. M.; Sali, A.; Karplus, M. Protein folding: A perspective from theory and experiment. Angew. Chem. Int. Ed. Engl. 1998, 37, 869-893.
38. Derewenda, Z. S.; Lee, L.; Derewenda, U. The occurrence of C-H···O hydrogen bonds in proteins. J. Mol. Biol. 1995, 252, 248-262.
39. α-H···O=C hydrogen bonds in a collagen triple helix. J. Mol. Biol. 1996, 264, 734-742. (Pubitemid 27013557)
40. α-H···O=C hydrogen bond? J. Am. Chem. Soc. 2000, 122, 4750-4755. (Pubitemid 30331692)
41. Flocco, M. M.; Mowbray, S. L. Planar stacking interactions of arginine and aromatic side-chains in proteins. J. Mol. Biol. 1994, 235, 709-717. (Pubitemid 24063588)
42. Gallivan, J. P.; Dougherty, D. A. Cation-p interactions in structural biology. Proc. Natl. Acad. Sci. USA 1999, 96, 9459-9464.
43. Gallivan, J. P.; Dougherty, D. A. A computational study of cation-p interactions vs salt bridges in aqueous media: Implications for protein engineering. J. Am. Chem. Soc. 2000, 122, 870-874. (Pubitemid 30094396)
44. Umezawa, Y.; Nishio, M. CH/π interactions as demonstrated in the crystal structure of guaninenucleotide binding proteins, Src homology-2 domains and human growth hormone in complex with their specific ligands. Bioorg. Med. Chem. 1998, 6, 493-504. (Pubitemid 28179589)
45. Takahashi, O.; Kohno, Y.; Nishio, M. Relevance of weak hydrogen bonds in the conformation of organic compounds and bioconjugates: Evidence from recent experimental data and high-level ab initio MO calculations. Chem. Rev. 2010, 110, 6049-6076.
46. Brandl, M.; Weiss, M. S.; Jabs, A.; Sühnel, J.; Hilgenfeld, R. C-H···π-interactions in proteins. J. Mol. Biol. 2001, 307, 357-377.
47. Chakrabarti, P.; Bhattacharyya, R. Geometry of nonbonded interactions involving planar groups in proteins. Prog. Biophys. Mol. Biol. 2007, 95, 83-137. (Pubitemid 47513187)
48. Ippolito, J. A.; Alexander, R. S.; Christianson, D. W. Hydrogen bond stereochemistry in protein structure and function. J. Mol. Biol. 1990, 215, 457-471. (Pubitemid 20364477)
49. Morgan, R. S.; Tatsch, C. E.; Gushard, R. H.; McAdon, J. M. Warme, P. K. Chains of alternating sulfur and p-bonded atoms in eight small proteins. Int. J. Peptide Protein Res. 1978, 11, 209-217. (Pubitemid 8323034)
50. Reid, K. S. C.; Lindley, P. F.; Thornton, J. M. Sulfur-aromatic interactions in proteins. FEBS Lett. 1985, 190, 209-213.
51. Viguera, A. R.; Serrano, L. Side-chain interactions between sulfur-containing amino acids and phenylalanine in α-helices. Biochemistry 1995, 34, 8771-8779.
52. Cheney, B. V.; Schulz, M. W.; Cheney, J. Complexes of benzene with formamide and methanethiol as models for interactions of protein substructures. Biochim. Biophys. Acta 1989, 996, 116-124.
53. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The protein data bank. Nucl. Acids Res. 2000, 28, 235-242. (Pubitemid 30047768)
54. Møller, C.; Plesset, M. S. Note on the approximation treatment for many-electron systems. Phys. Rev. 1934, 46, 618-622.
55. Taylor, J. C.; Markham, G. D. The bifunctional active site of S-adenosylmethionine synthetase-Roles of the active site aspartates. J. Biol. Chem. 1999, 274, 32909-32914. (Pubitemid 129535328)
56. Brandt, W.; Golbraikh, A.; Täger, M.; Lendeckel, U. A molecular mechanism for the cleavage of a disulfide bond as the primary function of agonist binding to G-protein-coupled receptors based on theoretical calculations supported by experiments. Eur. J. Biochem. 1999, 261, 89-97. (Pubitemid 29166072)
57. Palenchar, J. B.; Crocco, J. M.; Colman, R. F. The characterization of mutant Bacillus subtilis adenylosuccinate lyases corresponding to severe human adenylosuccinate lyase deficiencies. Protein Sci. 2003, 12, 1694-1705. (Pubitemid 36910050)
58. Singh, A. K.; Singh, N.; Sharma, S.; Shin, K.; Takase, M.; Kaur, P.; Srinivasan, A.; Singh, T. P. Inhibition of lactoperoxidase by its own catalytic product: Crystal structure of the hypothiocyanate-inhibited bovine lactoperoxidase at 2.3-. resolution. Biophys. J. 2009, 96, 646-654.
59. Nakamura, T.; Yamamoto, T.; Abe, M.; Matsumura, H.; Hagihara, Y.; Goto, T.; Yamaguchi, T.; Inoue, T. Oxidation of archaeal peroxiredoxin involves a hypervalent sulfur intermediate. Proc. Nat. Acad. Sci. USA 2008, 105, 6238-6242. (Pubitemid 351758330)
60. Iwaoka, M.; Tomoda, S. The SAAP force field. A simple approach to a new all-atom protein force field by using single amino acid potential (SAAP) functions in various solvents. J. Comput. Chem. 2003, 24, 1192-1200.
61. Iwaoka, M.; Kimura, N.; Yosida, D.; Minezaki, T. The SAAP force field: Development of the single amino acid potentials for 20 proteinogenic amino acids and Monte Carlo molecular simulation for short peptides. J. Comput. Chem. 2009, 30, 2039-2055.
62. Dennis, E. A. Diversity of group types, regulation, and function of phospholipase A 2. J. Biol. Chem. 1994, 269, 13057-13060. (Pubitemid 24206060)
63. Jain, M. K.; Gelb, M. H.; Rogers, J.; Berg, O. G. Kinetic basis for interfacial catalysis by phospholipase A2. Methods Enzymol. 1995, 249, 567-614.
64. Yu, B. Z.; Pan, Y. H.; Janssen, M. J. W.; Bahnson, B. J.; Jain, M. K. Kinetic and structural properties of disulfide engineered phospholipase A2: Insight into the role of disulfide bonding patterns. Biochemistry 2005, 44, 3369-3379. (Pubitemid 40322007)
65. Ohno, M.; Chijiwa, T.; Oda-Ueda, N.; Ogawa, T.; Hattori, S. Molecular evolution of myotoxic phospholipase A2 from snake venom. Toxicon 2003, 42, 841-854. (Pubitemid 38201487)
66. Raines, R. T. Ribonuclease A. Chem. Rev. 1998, 98, 1045-1065. (Pubitemid 128632236)
67. Rothwarf, D. M.; Li, Y. J.; Scheraga, H. A. Regeneration of bovine pancreatic ribonuclease A: Identification of two nativelike three-disulfide intermediates involved in separate pathways. Biochemistry 1998, 37, 3760-3766. (Pubitemid 28162931)
68. Welker, E.; Narayan, M.; Wedemeyer, W. J.; Scheraga, H. A. Structural determinants of oxidative folding in proteins. Proc. Natl. Acad. Sci. USA 2001, 98, 2312-2316. (Pubitemid 32209479)
69. Xu, X.; Rothwarf, D. M.; Scheraga, H. A. Nonrandom distribution of the one-disulfide intermediates in the regeneration of ribonuclease A. Biochemistry 1996, 35, 6406-6417. (Pubitemid 26164075)
70. Li, Y. J.; Rothwarf, D. M.; Scheraga, H. A. Mechanism of reductive protein unfolding. Nat. Struct. Mol. Biol. 1995, 2, 489-494.
71. Nachman, J.; Miller, M.; Gilliland, G. L.; Carty, R.; Pincus, M.; Wlodawer, A. Crystal structure of two covalent nucleoside derivatives of ribonuclease A. Biochemistry 1990, 29, 928-937. (Pubitemid 20053803)
72. Leonidas, D. D.; Shapiro, R.; Irons, L. I.; Russo, N.; Acharya, K. R. Crystal structures of ribonuclease A complexes with 5'-diphosphoadenosine 3'-phosphate and 5'-diphosphoadenosine 2'-phosphate at 1.7. resolution. Biochemistry 1997, 36, 5578-5588. (Pubitemid 27200056)
73. Leonidas, D. D.; Shapiro, R.; Irons, L. I.; Russo, N.; Acharya, K. R. Toward rational design of ribonuclease inhibitors: High-resolution crystal structure of a ribonuclease A complex with a potent 3', 5'-pyrophosphate-linked dinucleotide inhibitor. Biochemistry 1999, 38, 10287-10297.
74. de Meyts, P. Insulin and its receptor: Structure, function and evolution. BioEssays 2004, 26, 1351-1362. (Pubitemid 39664629)
75. Merlini, G.; Bellotti, V. Lysozyme: A paradigmatic molecule for the investigation of protein structure, function and misfolding. Clin. Chim. Acta 2005, 357, 168-172. (Pubitemid 40884596)