Computational insights into the interaction of the anthrax lethal factor with the N-terminal region of its substrates

Proteins: Structure, Function and Bioinformatics

Volumn 75, Issue 2, 2009, Pages 323-335

  Joshi, Manali ^a   Ebalunode, Jerry Osagie ^a   Briggs, James M ^a  

^a University of Houston   (United States)

Author keywords

Anthrax lethal factor; Molecular dynamics; Substrate recognition

Indexed keywords

ANTHRAX LETHAL FACTOR; ANTHRAX TOXIN; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ZINC; BACTERIAL ANTIGEN; BACTERIAL TOXIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ARTICLE; BACILLUS ANTHRACIS; BETA SHEET; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME BINDING; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SIMULATION; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ENZYME SPECIFICITY; METABOLISM; PROTEIN BINDING; PROTEIN DOMAIN; THERMODYNAMICS;

BACILLUS ANTHRACIS;

ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; COMPUTER SIMULATION; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 66149128826     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22241     Document Type: Article

References (45)

1. Mock M, Foucet A. Anthrax. Annu Rev Microbiol 2001;55:647-671.
2. Milne JC, Furlong D, Hanna PC, Wall JS, Collier RJ. Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J Biol Chem 1994;269:20607-20612.
3. Leppla SH. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci USA 1982;79:3162-3166.
4. Klimpel KR, Arora N, Leppla SH. Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol Microbiol 1994;13:1093-1100.
5. Moayeri M, Haines D, Young HA, Leppla SH. Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J Clin Invest 2003;112:670-682.
6. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, Copeland TD, Ahn NG, Oskarsson MK, Fukasawa K, Paull KD, Vande Woude GF. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 1998;280:734-737.
7. Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M, Monte-cucco C. Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem Biophys Res Commun 1998;248:706-711.
8. Duesbery NS, Vande Woude GF. Anthrax lethal factor causes pro-teolytic inactivation of mitogen-activated protein kinase kinase. J Appl Microbiol 1999;87:289-293.
9. Vitale G, Bernardi L, Napolitani G, Mock M, Montecucco C. Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem J 2000; 352:739-745.
10. Egan SE, Weinberg RA. The pathway to signal achievement. Nature 1993;365:781-783.
11. Abrami L, Reig N, van der Goot FG. Anthrax toxin: the long and winding road that leads to the kill. Trends Microbiol 2005;13:72-78.
12. Pannifer AD, Wong TY, Schwarzenbacher R, Renatus M, Petosa C, Bienkowska J, Lacy DB, Collier RJ, Park S, Leppla SH, Hanna P, Liddington RC. Crystal structure of the anthrax lethal factor. Nature 2001;414:229-233.
13. Hammond SE, Hanna PC. Lethal factor active-site mutations affect catalytic activity in vitro. Infect Immun 1998;66:2374-2378.
14. Turk BE, Wong TY, Schwarzenbacher R, Jarrell ET, Leppla SH, Collier RJ, Liddington RC, Cantley LC. The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor. Nat Struct Mol Biol 2004;11:60-66.
15. Chopra AP, Boone SA, Liang X, Duesbery NS. Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J Biol Chem 2003;278:9402-9406.
16. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comp Chem 1983;4:187-217.
17. MacKerell AD, Jr, Bashford D, Bellott M, Dunbrack RL, Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102:3586-3616.
18. Antosiewicz J, Briggs JM, Elcock AH, Gilson MK, McCammon JA. Computing the ionization states of proteins with a detailed charge model. J Comp Chem 1996;17:1633-1644.
19. Antosiewicz J, McCammon JA, Gilson MK. Prediction of pH-dependent properties of proteins. J Mol Biol 1994;6:238:415-436.
20. Madura JD, Briggs JM, Wade RC, Davis ME, Luty BA, Ilin A, Anto-siewicz J, Gilson MK, Bagheri B, Scott LR, McCammon JA. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian dynamics program. Comp Phys Commun 1995;91:57-95.
21. Humphrey W, Dalke A, Schulten K. VMD-visual molecular dynamics. J Mol Graph 1996;14:33-38.
22. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. Scalable molecular dynamics with NAMD. J Comput Chem 2005;26:1781-1802.
23. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79:926-935.
24. Essman U, Perela L, Berkowitz ML, Darden T, Lee H, Pederson L. A smooth particle mesh Ewald method. J Chem Phys 1995;103: 8577-8593.
25. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
26. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. GROMACS: fast, flexible, and free. J Comput Chem 2005;26:1701-1718.
27. Srinivasan J, Miller J, Kollman PA, Case DA. Continuum solvent studies of the stability of RNA hairpin loops and helices. J Biomol Struct Dyn 1998;16:671-682.
28. Masukawa KM, Kollman PA, Kuntz ID. Investigation of neuramini-dase- substrate recognition using molecular dynamics and free energy calculations. J Med Chem 2003;46:5628-5637.
29. Wang J, Morin P, Wang W, Kollman PA. Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. J Am Chem Soc 2001;123:5221-5230.
30. Sitkoff D, Sharp KA, Honig B. Accurate calculation of hydration free energies using macroscopic solvent models. J Phys Chem 1994;98:1978-1988.
31. Caves LS, Evanseck JD, Karplus M. Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Protein Sci 1998;7:649-666.
32. Elofsson A, Nilsson L. How consistent are molecular dynamics simulations? Comparing structure and dynamics in reduced and oxidized Escherichia coli thioredoxin. J Mol Biol 1993;233:766-780.
33. Grossfield A, Feller SE, Pitman MC. Convergence of molecular dynamics simulations of membrane proteins Proteins 2007;67:31-40.
34. Pandini A, Bonati L. Conservation and specialization in PAS domain dynamics. Protein Eng Des Sel 2005;18:127-137.
35. Shoop WL, Xiong Y, Wiltsie J, Woods A, Guo J, Pivnichny JV, Fel-cetto T, Michael BF, Bansal A, Cummings RT, Cunningham BR, Friedlander AM, Douglas CM, Patel SB, Wisniewski D, Scapin G, Salowe SP, Zaller DM, Chapman KT, Scolnick EM, Schmatz DM, Bartizal K, MacCoss M, Hermes JD. Anthrax Lethal Factor Inhibition. Proc Natl Acad Sci USA 2005;102:7958-7963.
36. Tyndall JD, Nall T, Fairlie DP. Proteases universally recognize beta strands in their active sites. Chem Rev 2005;105:973-999.
37. Hutchinson EG, Sessions RB, Thornton JM, Woolfson DN. Determinants of strand register in antiparallel beta-sheets of proteins. Protein Sci 1998;7:2287-2300.
38. Sakharov DV, Lim C. Zn protein simulations including charge transfer and local polarization effects. J Am Chem Soc 2005;127: 4921-929.
39. Li W, Zhang J, Wang J, Wang W. Metal-coupled folding of Cys2His2 zinc-finger. J Am Chem Soc 2008;130:892-900.
40. Zoete V, Meuwly M, Karplus M. Study of the insulin dimerization: binding free energy calculations and per-residue free energy decomposition. Proteins 2005;61:79-93.
41. Noskov SY, Lim C. Free energy decomposition of protein-protein interactions. Biophys J 2001;81:737-750.
42. Tonello F, Ascenzi P, Montecucco C. The metalloproteolytic activity of the anthrax lethal factor is substrate-inhibited. J Biol Chem 2003;278:40075-40078.
43. Bodart JF, Chopra A, Liang X, Duesbery N. Anthrax. MEK Cancer Cell Cycle 2002;1:10-15.
44. Tanami H, Imoto I, Hirasawa A, Yuki Y, Sonoda I, Inoue J, Yasui K, Misawa-Furihata A, Kawakami Y, Inazawa J. Involvement of overexpressed wild-type BRAF in the growth of malignant melanoma cell lines. Oncogene 2004;23:8796-8804.
45. Abi-Habib RJ, Singh R, Leppla SH, Greene JJ, Ding Y, Berghuis B, Duesbery NS, Frankel AE. Systemic anthrax lethal toxin therapy produces regressions of subcutaneous human melanoma tumors in athymic nude mice. Clin Cancer Res 2006;12:7437-7443.