Impact of calcium on N1 influenza neuraminidase dynamics and binding free energy

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 11, 2010, Pages 2523-2532

  Lawrenz, Morgan ^a   Wereszczynski, Jeff ^a   Amaro, Rommie ^b,c   Walker, Ross ^d   Roitberg, Adrian ^e   McCammon, J Andrew ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Irvine   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF FLORIDA   (United States)

Author keywords

Bennett acceptance ratio; Force field comparison; Metal binding; Molecular dynamics; Oseltamivir; Thermodynamic integration

Indexed keywords

CALCIUM; OSELTAMIVIR; SIALIDASE; ANTIVIRUS AGENT; PROTEIN BINDING; VIRUS PROTEIN;

ARTICLE; CALCIUM BINDING; CALCULATION; DRUG DESIGN; DYNAMICS; INFLUENZA A (H1N1); MEDICAL LITERATURE; MEMBRANE STABILIZATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; SAMPLING; SIMULATION; THERMODYNAMICS; VIRUS STRAIN; CHEMISTRY; CLUSTER ANALYSIS; ENZYME ACTIVE SITE; ENZYMOLOGY; HYDROGEN BOND; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H5N1; METABOLISM;

ANTIVIRAL AGENTS; CALCIUM; CATALYTIC DOMAIN; CLUSTER ANALYSIS; HYDROGEN BONDING; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; MOLECULAR DYNAMICS SIMULATION; NEURAMINIDASE; OSELTAMIVIR; PROTEIN BINDING; THERMODYNAMICS; VIRAL PROTEINS;

EID: 77955813570     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22761     Document Type: Article

References (53)

1. Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 2006; 443:45-49.
2. Varghese JN, Laver WG, Colman PM. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 1983; 303:35-40.
3. Xu X, Zhu X, Dwek RA, Stevens J, Wilson IA. Structural characterization of the 1918 influenza virus H1N1 neuraminidase. J Virol 2008; 82:10493-10501.
4. Collins PJ, Haire LF, Lin YP, Liu J, Russell RJ, Walker PA, Skehel JJ, Martin SR, Hay AJ, Gamblin SJ. Crystal structures of oseltamivirresistant influenza virus neuraminidase mutants. Nature 2008; 453:1258-1261.
5. Taylor G, Garman E, Webster R, Saito T, Laver G. Crystallization and preliminary X-ray studies of influenza A virus neuraminidase of subtypes N5, N6, N8 and N9. J Mol Biol 1993; 230:345-348.
6. Chong AK, Pegg MS, von Itzstein M. Influenza virus sialidase: effect of calcium on steady-state kinetic parameters. Biochim Biophys Acta 1991; 1077:65-71.
7. Burmeister WP, Cusack S, Ruigrok RW. Calcium is needed for the thermostability of influenza B virus neuraminidase. J Gen Virol 1994;75(Part 2), 381-388.
8. Potier M, Mameli L, Bélisle M, Dallaire L, Melançon SB. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-alpha-D- N-acetylneuraminate) substrate. Anal Biochem 1979; 94:287-296.
9. Smith BJ, Huyton T, Joosten RP, McKimm-Breschkin JL, Zhang JG, Luo CS, Lou MZ, Labrou NE, Garrett TPJ. Structure of a calcium-deficient form of influenza virus neuraminidase: implications for substrate binding. Acta Crystallogr D Biol Crystallogr 2006; 62:947-952.
10. Amaro RE, Minh DDL, Cheng LS, Lindstrom WM, Olson AJ, Lin J-H, Li WW, McCammon JA. Remarkable loop flexibility in avian influenza N1 and its implications for antiviral drug design. J Am Chem Soc 2007; 129:7764-7765.
11. Amaro RE, Cheng X, Ivanov I, Xu D, McCammon JA. Characterizing loop dynamics and ligand recognition in human-and aviantype influenza neuraminidases via generalized born molecular dynamics and end-point free energy calculations. J Am Chem Soc 2009; 131:4702-4709.
12. Lawrenz M, Baron R, McCammon J. Independent-trajectories thermodynamic-integration free-energy changes for biomolecular systems: Determinants of H5N1 avian influenza virus neuraminidase inhibition by peramivir. J Chem Theory Comput 2009; 5:1106-1116.
13. Aruksakunwong O, Malaisree M, Decha P, Sompornpisut P, Parasuk V, Pianwanit S, Hannongbua S. On the Lower Susceptibility of Oseltamivir to Influenza Neuraminidase Subtype N1 than those in N2 and N9. Biophys J 2007; 92:798-807.
14. von Itzstein M. The war against influenza: discovery and development of sialidase inhibitors. Nat Rev Drug Discov 2007; 6:967-974.
15. Du Q-S, Wang S-Q, Huang R-B, Chou K-C. Chemi Phys Lett 2010; 485:191-195.
16. Wang S, Du Q, Huang R, Zhang D, Chou K. Insights from investigating the interaction of oseltamivir (Tamiflu) with neuraminidase of the 2009 H1N1 swine flu virus. Biochem Biophys Res Commun 2009; 432-436.
17. An J, Lee DCW, Law AHY, Yang CLH, Poon LLM, Lau ASY, Jones SJM. A novel small-molecule inhibitor of the avian influenza H5N1 virus determined through computational screening against the neuraminidase. J Med Chem 2009; 52:2667-2672.
18. Cheng LS, Amaro RE, Xu D, Li WW, Arzberger PW, McCammon JA. Ensemble-based virtual screening reveals potential novel antiviral compounds for avian influenza neuraminidase. J Med Chem 2008; 51:3878-3894.
19. Wang NX, Zheng JJ. Computational studies of H5N1 influenza virus resistance to oseltamivir. Protein Sci 2009; 432-436.
20. Masukawa KM, Kollman PA, Kuntz ID. Investigation of neuraminidase- substrate recognition using molecular dynamics and free energy calculations. J Med Chem 2003; 46:5628-5637.
21. Malaisree M, Rungrotmongkol T, Decha P, Intharathep P, Aruksakunwong O, Hannongbua S. Understanding of known drug-target interactions in the catalytic pocket of neuraminidase subtype N1. Proteins 2008; 1908-1918.
22. Christen M, Hünenberger PH, Bakowies D Baron R, Bürgi R, Geerke DP, Heinz TN, Kastenholz MA, Kräutler V, Oostenbrink C, Peter C, Trzesniak D, van Gunsteren WF. The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem 2005; 26:1719-1751.
23. Schuler LD, Daura X, van Gunsteren WF. An improved GRO-MOS96 force field for aliphatic hydrocarbons in the condensed phase. J Comput Chem 2001; 22:1205-1218.
24. Wang J, Cieplak P, Kollman PA. J Comput Chem 2000; 21:1049-1074.
25. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 2006; 65:712-725.
26. Case DA, Darden TA, Cheatham TE, III, Simmerling CL, Wang J, Duke RE, Luo R, Crowley M, Walker RC, Zhang W, Merz KM, Wang B, Hayik S, Roitberg A, Seabra G, Kolossváry I, Wong KF, Paesani F, Vanicek J, Wu X, Brozell SR, Steinbrecher T, Gohlke H, Yang L, Tan C, Mongan J, Hornak V, Cui G, Mathews DH, Seetin MG, Sagui C, Babin V, Kollman PA. AMBER 10. San Francisco: University of California; 2008.
27. Bowers KJ, Chow E, Xu H, Dror RO, Eastwood MP, Gregersen BA, Klepeis JL, Kolossváry I, Moraes MA, Sacerdoti FD, Salmon JK, Shan Y, Shaw DE. Scalable Algorithms for Molecular Dynamics Simulations on Commodity Clusters. Proceedings of the ACM/IEEE Conference on Supercomputing (SC06), 2006.
28. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996; 14:33-38, 27-28.
29. Daura X, van Gunsteren WF, Mark AE. Folding-unfolding thermodynamics of a beta-heptapeptide from equilibrium simulations. Proteins 1999; 34:269-80.
30. Gilson MK, Given JA, Bush BL, McCammon JA. The statisticalthermodynamic basis for computation of binding affinities: a critical review. Biophy J 1997; 72:1047-1069.
31. Hamelberg D, McCammon JA. Standard free energy of releasing a localized water molecule from the binding pockets of proteins: double-decoupling method. J Am Chem Soc 2004; 126:7683-7689.
32. Beutler TC, Mark AE, van Shaik RC, Gerber PR, van Gunsteren WF. Avoiding singularities and numerical instabilities in free energy calculations based on molecular simulations. Chem Phys Lett 1994; 529-539.
33. Chodera JD, Swope WC, Pitera JW, Seok C, Dill KA. J Chem Theory Comput 2007; 3:26-41.
34. Zagrovic B, van Gunsteren W. Computational Analysis of the Mechanism and Thermodynamics of Inhibition of Phosphodiesterase 5A by Synthetic Ligands. J Chem Theory Comput 2007; 3:301-311. doi: 10.1021/ct600322d.
35. Fujitani H, Tanida Y, Ito M, Jayachandran G, Snow CD, Shirts MR, Sorin EJ, Pande VS. Direct calculation of the binding free energies of FKBP ligands. J Chem Phys 2005; 123:084108.
36. Shirts MR, Chodera JD. Statistically optimal analysis of samples from multiple equilibrium states. J Chem Phys 2008; 129:124105.
37. Rueda M, Ferrer-Costa C, Meyer T, Pérez A, Camps J, Hospital A, Gelpí JL, Orozco M. A consensus view of protein dynamics. Proc Natl Acad Sci USA 2007; 104:796-801.
38. Caves LS, Evanseck JD, Karplus M. Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Protein Sci 1998; 7:649-666.
39. Monticelli L, Sorin EJ, Tieleman DP, Pande VS, Colombo G. Molecular simulation of multistate peptide dynamics: a comparison between microsecond timescale sampling and multiple shorter trajectories. J Comput Chem 2008; 29:1740-1752.
40. Stoll V, Stewart KD, Maring CJ, Muchmore S, Giranda V, Gu YY, Wang G, Chen Y, Sun M, Zhao C, Kennedy AL, Madigan DL, Xu Y, Saldivar A, Kati W, Laver G, Sowin T, Sham HL, Greer J, Kempf D. Influenza neuraminidase inhibitors: structure-based design of a novel inhibitor series. Biochemistry 2003; 42:718-727.
41. Kati WM, Montgomery D, Carrick R, Gubareva L, Maring C, McDaniel K, Steffy K, Molla A, Hayden F, Kempf D, Kohlbrenner W. In vitro characterization of A-315675, a highly potent inhibitor of A and B strain influenza virus neuraminidases and influenza virus replication. Antimicrob Agents Chemother 2002; 46:1014-1021.
42. Abed Y, Nehme B, Baz M, Boivin G. Activity of the neuraminidase inhibitor A-315675 against oseltamivir-resistant influenza neuraminidases of N1 and N2 subtypes. Antiviral Res 2008; 77:163-166.
43. Baz M, Abed Y, Boivin G. Characterization of drug-resistant recombinant influenza A/H1N1 viruses selected in vitro with peramivir and zanamivir. Antiviral Res 2007; 74:159-162.
44. Bantia S, Parker CD, Ananth SL, Horn LL, Andries K, Chand P, Kotian PL, Dehghani A, El-Kattan Y, Lin T, Hutchison TL, Montgomery JA, Kellog DL, Babu YS. Comparison of the anti-influenza virus activity of RWJ-270201 with those of oseltamivir and zanamivir. Antimicrob Agents Chemother 2001; 45:1162-1167.
45. Boivin G, Goyette N. Susceptibility of recent Canadian influenza A and B virus isolates to different neuraminidase inhibitors. Antiviral Res 2002; 54:143-147.
46. Gubareva LV, Webster RG, Hayden FG. Comparison of the activities of zanamivir, oseltamivir, and RWJ-270201 against clinical isolates of influenza virus and neuraminidase inhibitor-resistant variants. Antimicrob Agents Chemother 2001; 45:3403-3408.
47. Govorkova EA, Leneva IA, Goloubeva OG, Bush K, Webster RG. Comparison of efficacies of RWJ-270201, zanamivir, and oseltamivir against H5N1, H9N2, and other avian influenza viruses. Antimicrob Agents Chemother 2001; 45:2723-2732.
48. Hurt A, Selleck P, Komadina N, Shaw R, Brown L, Barr I. Susceptibility of highly pathogenic A (H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res 2007; 73:228-231.
49. McSharry JJ, McDonough AC, Olson BA, Drusano GL. Phenotypic drug susceptibility assay for influenza virus neuraminidase inhibitors. Clin Diagn Lab Immunol 2004; 11:21-28.
50. Mishin VP, Hayden FG, Gubareva LV. Susceptibilities of antiviralresistant influenza viruses to novel neuraminidase inhibitors. Antimicrob Agents Chemother 2005; 49:4515-4520.
51. Le QM, Kiso M, Someya K, Sakai YT, Nguyen TH, Nguyen KHL, Pham ND, Ngyen HH, Yamada S, Muramoto Y, Horimoto T, Takada A, Goto H, Suzuki T, Suzuki Y, Kawaoka Y. Avian flu: isolation of drug-resistant H5N1 virus. Nature 2005; 437:1108.
52. Shie J-J, Fang J-M, Wang S-Y, Tsai K-C, Cheng Y-SE, Yang A-S, Hsiao S-C, Su C-Y, Wong C-H. Synthesis of tamiflu and its phosphonate congeners possessing potent anti-influenza activity. J Am Chem Soc 2007; 129:11892-11893.
53. Yamashita M, Tomozawa T, Kakuta M, Tokumitsu A, Nasu H, Kubo S. CS-8958, a prodrug of the new neuraminidase inhibitor R-125489, shows long-acting anti-influenza virus activity. Antimicrob Agents Chemother 2009; 53:186-192.