Role of hydration in collagen recognition by bacterial adhesins

Biophysical Journal

Volumn 100, Issue 9, 2011, Pages 2253-2261

  Vitagliano, Luigi ^a   Berisio, Rita ^a   De Simone, Alfonso ^b  

^a CNR   (Italy)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 79959717409     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.03.033     Document Type: Article

References (65)

1. Ball, P. 2008. Water as an active constituent in cell biology. Chem. Rev. 108:74-108. (Pubitemid 351187472)
2. Levy, Y., and J. N. Onuchic. 2006. Water mediation in protein folding and molecular recognition. Annu. Rev. Biophys. Biomol. Struct. 35:389-415. (Pubitemid 43877384)
3. Chandler, D. 2005. Interfaces and the driving force of hydrophobic assembly. Nature. 437:640-647. (Pubitemid 41486526)
4. Pal, S. K., J. Peon, and A. H. Zewail. 2002. Biological water at the protein surface: dynamical solvation probed directly with femtosecond resolution. Proc. Natl. Acad. Sci. USA. 99:1763-1768. (Pubitemid 34168964)
5. Zong, C., G. A. Papoian,..., P. G. Wolynes. 2006. Role of topology, nonadditivity, and water-mediated interactions in predicting the structures of a/b proteins. J. Am. Chem. Soc. 128:5168-5176.
6. Abel, R., T. Young,..., R. A. Friesner. 2008. Role of the active-site solvent in the thermodynamics of factor Xa ligand binding. J. Am. Chem. Soc. 130:2817-2831. (Pubitemid 351416242)
7. Papoian, G. A., J. Ulander, and P. G. Wolynes. 2003. Role of water mediated interactions in protein-protein recognition landscapes. J. Am. Chem. Soc. 125:9170-9178. (Pubitemid 36903833)
8. Fuxreiter, M., M. Mezei,..., R. Osman. 2005. Interfacial water as a "hydration fingerprint" in the noncognate complex of BamHI. Biophys. J. 89:903-911. (Pubitemid 41098977)
9. Fischer, S., and C. S. Verma. 1999. Binding of buried structural water increases the flexibility of proteins. Proc. Natl. Acad. Sci. USA. 96:9613-9615. (Pubitemid 29398779)
10. Hamelberg, D., T. Shen, and J. A. McCammon. 2006. Insight into the role of hydration on protein dynamics. J. Chem. Phys. 125:094905.
11. De Simone, A., G. G. Dodson,..., F. Fraternali. 2005. Prion and water: tight and dynamical hydration sites have a key role in structural stability. Proc. Natl. Acad. Sci. USA. 102:7535-7540. (Pubitemid 40741006)
12. Silva, J. L., and D. Foguel. 2009. Hydration, cavities and volume in protein folding, aggregation and amyloid assembly. Phys. Biol. 6:015002.
13. Choudhury, N., and B. M. Pettitt. 2007. The dewetting transition and the hydrophobic effect. J. Am. Chem. Soc. 129:4847-4852. (Pubitemid 46648785)
14. Cramer, C. J., and D. G. Truhlar. 2008. A universal approach to solvation modeling. Acc. Chem. Res. 41:760-768.
15. Despa, F., A. Fernández, and R. S. Berry. 2004. Dielectric modulation of biological water. Phys. Rev. Lett. 93:228104.
16. Fernández, A., and L. R. Scott. 2003. Adherence of packing defects in soluble proteins. Phys. Rev. Lett. 91:018102.
17. Myllyharju, J., and K. I. Kivirikko. 2004. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20:33-43. (Pubitemid 38032818)
18. Brodsky, B., and A. V. Persikov. 2005. Molecular structure of the collagen triple helix. Adv. Protein Chem. 70:301-339. (Pubitemid 40544786)
19. Okuyama, K. 2008. Revisiting the molecular structure of collagen. Connect. Tissue Res. 49:299-310.
20. Berisio, R., A. De Simone,..., L. Vitagliano. 2009. Role of side chains in collagen triple helix stabilization and partner recognition. J. Pept. Sci. 15:131-140.
21. Shoulders, M. D., and R. T. Raines. 2009. Collagen structure and stability. Annu. Rev. Biochem. 78:929-958.
22. Leitinger, B., and E. Hohenester. 2007. Mammalian collagen receptors. Matrix Biol. 26:146-155. (Pubitemid 46401227)
23. Emsley, J. 2010. Convergent recognition of a triple helical hydrophobic motif in collagen. Structure. 18:1-2.
24. Zong, Y., Y. Xu,..., S. V. Narayana. 2005. A 'collagen hug' model for Staphylococcus aureus CNA binding to collagen. EMBO J. 24:4224-4236. (Pubitemid 41828898)
25. Emsley, J., C. G. Knight,..., R. C. Liddington. 2000. Structural basis of collagen recognition by integrin a2b1. Cell. 101:47-56.
26. Hohenester, E., T. Sasaki,..., H. P. Bächinger. 2008. Structural basis of sequence-specific collagen recognition by SPARC. Proc. Natl. Acad. Sci. USA. 105:18273-18277.
27. Carafoli, F., D. Bihan,..., E. Hohenester. 2009. Crystallographic insight into collagen recognition by discoidin domain receptor 2. Structure. 17:1573-1581.
28. De Simone, A., L. Vitagliano, and R. Berisio. 2008. Role of hydration in collagen triple helix stabilization. Biochem. Biophys. Res. Commun. 372:121-125.
29. Kang, H. J., F. Coulibaly,..., E. N. Baker. 2007. Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Science. 318:1625-1628. (Pubitemid 350233661)
30. Inouye, K., S. Sakakibara, and D. J. Prockop. 1976. Effects of the stereo-configuration of the hydroxyl group in 4-hydroxyproline on the triple-helical structures formed by homogenous peptides resembling collagen. Biochim. Biophys. Acta. 420:133-141.
31. Berisio, R., L. Vitagliano,..., A. Zagari. 2002. Recent progress on collagen triple helix structure, stability and assembly. Protein Pept. Lett. 9:107-116. (Pubitemid 34432246)
32. Doi, M., Y. Nishi,..., Y. Kobayashi. 2005. Collagen-like triple helix formation of synthetic (Pro-Pro-Gly) 10 analogues: (4 (S)-hydroxyprolyl-4 (R)-hydroxyprolyl-Gly) 10, (4 (R)-hydroxyprolyl-4 (R)-hydroxyprolyl-Gly) 10 and (4 (S)-fluoroprolyl-4 (R)-fluoroprolyl-Gly) 10. J. Pept. Sci. 11:609-616.
33. Holmgren, S. K., L. E. Bretscher,..., R. T. Raines. 1999. A hyperstable collagen mimic. Chem. Biol. 6:63-70. (Pubitemid 29363157)
34. Hess, B., C. Kutzner,..., E. Lindahl. 2008. GROMACS 4: algorithms for highly efficient, loadβalanced, and scalable molecular simulation. J. Chem. Theory Comput. 4:435-447.
35. Hornak, V., R. Abel,..., C. Simmerling. 2006. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 65:712-725. (Pubitemid 44583220)
36. Sorin, E. J., and V. S. Pande. 2005. Exploring the helix-coil transition via all-atom equilibrium ensemble simulations. Biophys. J. 88:2472-2493. (Pubitemid 40976118)
37. Horn, H. W., W. C. Swope,..., T. Head-Gordon. 2004. Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. J. Chem. Phys. 120:9665-9678.
38. Wickstrom, L., A. Okur, and C. Simmerling. 2009. Evaluating the performance of the ff99SB force field based on NMR scalar coupling data. Biophys. J. 97:853-856.
39. Makarov, V. A., B. K. Andrews,..., B. M. Pettitt. 2000. Residence times of water molecules in the hydration sites of myoglobin. Biophys. J. 79:2966-2974.
40. Colombo, G., M. Meli, and A. De Simone. 2008. Computational studies of the structure, dynamics and native content of amyloid-like fibrils of ribonuclease A. Proteins. 70:863-872. (Pubitemid 351161945)
41. De Simone, A., J. E. Corrie,..., F. Fraternali. 2008. Conformation and dynamics of a rhodamine probe attached at two sites on a protein: implications for molecular structure determination in situ. J. Am. Chem. Soc. 130:17120-17128.
42. Hamelberg, D., and J. A. McCammon. 2004. Standard free energy of releasing a localized water molecule from the binding pockets of proteins: double-decoupling method. J. Am. Chem. Soc. 126:7683-7689. (Pubitemid 38781502)
43. Jenkins, C. L., and R. T. Raines. 2002. Insights on the conformational stability of collagen. Nat. Prod. Rep. 19:49-59. (Pubitemid 34140332)
44. Stultz, C. M. 2002. Localized unfolding of collagen explains collagenase cleavage near imino-poor sites. J. Mol. Biol. 319:997-1003. (Pubitemid 34729413)
45. Raman, S. S., R. Parthasarathi,..., T. Ramasami. 2006. Role of aspartic acid in collagen structure and stability: a molecular dynamics investigation. J. Phys. Chem. B. 110:20678-20685. (Pubitemid 44797501)
46. Ravikumar, K. M., and W. Hwang. 2008. Region-specific role of water in collagen unwinding and assembly. Proteins. 72:1320-1332.
47. Bella, J., B. Brodsky, and H. M. Berman. 1995. Hydration structure of a collagen peptide. Structure. 3:893-906.
48. Berisio, R., L. Vitagliano,..., A. Zagari. 2000-2001. Crystal structure of a collagen-like polypeptide with repeating sequence Pro-Hyp-Gly at 1.4 A resolution: implications for collagen hydration. Biopolymers 56:8-13.
49. Okuyama, K., C. Hongo,..., N. Nishino. 2004. Crystal structures of collagen model peptides with Pro-Hyp-Gly repeating sequence at 1.26 A resolution: implications for proline ring puckering. Biopolymers. 76:367-377. (Pubitemid 39540531)
50. Melacini, G., A. M. Bonvin,..., R. Kaptein. 2000. Hydration dynamics of the collagen triple helix by NMR. J. Mol. Biol. 300:1041-1049.
51. Hua, L., X. Huang,..., B. J. Berne. 2006. Dynamics of water confined in the interdomain region of a multidomain protein. J. Phys. Chem. B. 110:3704-3711.
52. De Simone, A., R. Spadaccini,..., F. Fraternali. 2006. Toward the understanding of MNEI sweetness from hydration map surfaces. Biophys. J. 90:3052-3061.
53. Despa, F., and R. S. Berry. 2007. The origin of long-range attraction between hydrophobes in water. Biophys. J. 92:373-378. (Pubitemid 46145771)
54. Meyer, E. E., Q. Lin,..., J. N. Israelachvili. 2005. Origin of the longrange attraction between surfactant-coated surfaces. Proc. Natl. Acad. Sci. USA. 102:6839-6842. (Pubitemid 40675403)
55. Berisio, R., V. Granata,..., A. Zagari. 2004. Imino acids and collagen triple helix stability: characterization of collagen-like polypeptides containing Hyp-Hyp-Gly sequence repeats. J. Am. Chem. Soc. 126:11402-11403. (Pubitemid 39244932)
56. Murphy, 4th, F. V., R. M. Sweet, and M. E. Churchill. 1999. The structure of a chromosomal high mobility group protein-DNA complex reveals sequence-neutral mechanisms important for non-sequencespecific DNA recognition. EMBO J. 18:6610-6618.
57. Engel, J., and D. J. Prockop. 1998. Does bound water contribute to the stability of collagen? Matrix Biol. 17:679-680. (Pubitemid 29017235)
58. Nishi, Y., S. Uchiyama,..., Y. Kobayashi. 2005. Different effects of 4-hydroxyproline and 4-fluoroproline on the stability of collagen triple helix. Biochemistry. 44:6034-6042. (Pubitemid 40570697)
59. Holmgren, S. K., K. M. Taylor,..., R. T. Raines. 1998. Code for collagen's stability deciphered. Nature. 392:666-667.
60. Schumacher, M., K. Mizuno, and H. P. Bächinger. 2005. The crystal structure of the collagen-like polypeptide (glycyl-4 (R)-hydroxyprolyl-4 (R)-hydroxyprolyl) 9 at 1.55 A resolution shows up-puckering of the proline ring in the Xaa position. J. Biol. Chem. 280:20397-20403. (Pubitemid 40776739)
61. Shoulders, M. D., K. A. Satyshur,..., R. T. Raines. 2010. Stereoelectronic and steric effects in side chains preorganize a protein main chain. Proc. Natl. Acad. Sci. USA. 107:559-564.
62. Tame, J. R., G. N. Murshudov,..., A. J. Wilkinson. 1994. The structural basis of sequence-independent peptide binding by OppA protein. Science. 264:1578-1581. (Pubitemid 24227710)
63. Autenrieth, F., E. Tajkhorshid,..., Z. Luthey-Schulten. 2004. Role of water in transient cytochrome c2 docking. J. Phys. Chem. B. 108:20376-20378.
64. Keskin, O., B. Ma, and R. Nussinov. 2005. Hot regions in protein-protein interactions: the organization and contribution of structurally conserved hot spot residues. J. Mol. Biol. 345:1281-1294. (Pubitemid 40092239)
65. Li, X., O. Keskin,..., J. Liang. 2004. Protein-protein interactions: hot spots and structurally conserved residues often locate in complemented pockets that pre-organized in the unbound states: implications for docking. J. Mol. Biol. 344:781-795. (Pubitemid 39469220)