A repulsive electrostatic mechanism for protein export through the type III secretion apparatus

Biophysical Journal

Volumn 98, Issue 3, 2010, Pages 452-461

  Rathinavelan, Thenmalarchelvi ^a   Zhang, Lingling ^a   Picking, Wendy L ^a   Weis, David D ^a   De Guzman, Roberto N ^a   Im, Wonpil ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEGIBACTERIA; SHIGELLA;

EID: 76149140076     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.10.030     Document Type: Article

References (41)

1. Kotloff, K. L., J. P. Winickoff, M. M. Levine. 1999. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 77: 651-666.
2. Rotz, L. D., A. S. Khan, J. M. Hughes. 2002. Public health assessment of potential biological terrorism agents. Emerg. Infect. Dis. 8:225-230.
3. Cornelis, G. R. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811-825.
4. Yip, C. K., T. G. Kimbrough, N. C. Strynadka. 2005. Structural characterization of the molecular platform for type III secretion, system, assembly. Nature. 435:702-707. (Pubitemid 40825517)
5. Spreter, T., C. K. Yip, N. C. Strynadka. 2009. A conserved structural motif mediates formation of the periplasms rings in the type III secretion system. Nat. Struct. Mol. Biol. 16:468-476.
6. Deane, J. E., P. Roversi, S. M. Lea. 2006. Molecular model of a type III secretion, system needle: implications for host-cell sensing. Proc. Natl. Acad. Sci. USA. 103:12529-12533.
7. Wang, Y., A. N. Ouellette, R. N. De Guzman. 2007. Differences in the electrostatic surfaces of the type III secretion needle proteins PrgI, BsaL, and MxiH. J. Mol. Biol. 371:1304-1314. (Pubitemid 47208516)
8. Zhang, L., Y. Wang, R. N. De Guzman. 2006. Solution structure of monomeric BsaL, the type III secretion needle protein of Burkholderia pseudomallei. J. Mol. Biol. 359:322-330.
9. Johnson, S., P. Roversi, S. M. Lea. 2007. Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J. Biol. Chem. 282:4035-4044. (Pubitemid 47084440)
10. Broz, P., C. A. Mueller, G. R. Cornelis. 2007. Function and molecular architecture of the Yersinia injectisome tip complex. Mol, Microbiol. 65:1311-1320. (Pubitemid 47262832)
11. Paci, E., and M. Karplus. 1999. Forced unfolding of fibronectin type 3 modules: an analysis by biased molecular dynamics simulations. J. Mol. Biol. 288:441-459. (Pubitemid 29221813)
12. Hub, J. S., and B. L. de Groot. 2008. Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc. Natl. Acad. Sci. USA. 105: 1198-1203.
13. Jensen, M. O., S. Park, K. Schulten. 2002. Energetics of glycerol conduction, through, aquaglyceroporin Glpf Proc. Natl. Acad. Sci. USA. 99:6731-6736.
14. Peter, C., and G. Hummer. 2005. Ion transport through membrane-span-ning nanopores studied by molecular dynamics simulations and continuum electrostatics calculations. Biophys. J. 89:2222-2234. (Pubitemid 41401015)
15. Yeh, I. C., and G. Hummer. 2004. Nucleic acid transport through carbon nanotube membranes. Proc. Natl. Acad. Sci. USA. 101:1.2177-12182.
16. Im, W., S. Berneche, and B. Roux. 2001. Generalized solvent boundary potential for computer simulations. J. Chem. Phys. 114:2924-2937. (Pubitemid 32253408)
17. Im, W., M. S. Lee, and C. L. Brooks, 3rd. 2003. Generalized Bom model with a simple smoothing function. J. Comput. Chem. 24; 1691-1702.
18. Brooks, B. R., C. L. Brooks, 3rd, M. Karplus. 2009. CHARMM: the biomolecular simulation program. J. Comput. Chem. 30: 1545-1614.
19. Im, W., D. Beglov, and B. Roux. 1998. Continuum solvation model: computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation. Comput. Phys. Commun. 111:59-75. (Pubitemid 128400465)
20. Nina, M., W. Im, and B. Roux. 1999. Optimized atomic radii for protein continuum electrostatics solvation forces. Biophys. Chem. 78:89-96. (Pubitemid 29206659)
21. Levy, R. M., L. Y. Zhang, A. K. Felts. 2003. On the nonpolar hydration free energy of proteins: surface area and continuum solvent models for the solute-solvent interaction energy. J. Am. Chem. Soc. 125:9523-9530.
22. Banavali, N. K., W. Im, and B. Roux. 2002. Electrostatic free energy calculations using the generalized solvent boundary potential method. J. Chem. Phys. 117:7381-7388.
23. Im, W., and B. Roux. 2002. Ion permeation and selectivity of OmpF porin: a theoretical study based on molecular dynamics, Brownian dynamics, and continuum, electrodiffusion theory. J. Mol. Biol. 322:851-869.
24. Im, W., S. Seefeld, and B. Roux. 2000. A grand canonical Monte CarloBrownian dynamics algorithm for simulating ion channels. Biophys. J. 79:788-801. (Pubitemid 30626174)
25. Cordes, F. S., K. Komoriya, S. M. Lea. 2003. Helical structure of the needle of the type III secretion system of Shigella flexneri, J. Biol. Chem. 278:17103-17107.
26. Schirmer, T., T. A. Keller, J. P. Rosenbusch. 1995. Structural basis for sugar translocation through, maltoporin channels at 3.1 Å resolution. Science. 267:512-514.
27. Dutzler, R., Y. F. Wang, T. Schirmer. 1996. Crystal structures of various maltooligosaccharides bound to maltoporin reveal a specific sugar translocation pathway. Structure. 4:127-134. (Pubitemid 126658976)
28. Van Gelder, P., F. Dumas, T. Schirmer. 2002. Sugar transport through maltoporin of Escherichia coli: role of the greasy slide. J. Bacterial. 184:2994-2999. (Pubitemid 34517822)
29. Hummer, G., and A. Szabo. 2005. Free energy surfaces from singlemolecule force spectroscopy. Act: Chem. Res. 38:504-513. (Pubitemid 41128402)
30. Jensen, M. O., E. Tajkhorshid, and K. Schulten. 2001. The mechanism of glycerol conduction in aquaglyceroporins. Structure. 9:1083-1093.
31. André, I., P. Bradley, D. Baker. 2007. Prediction of the structure of symmetrical protein assemblies. Proc: Natl, Acad. Sci. USA. 104: 17656-17661. (Pubitemid 350210890)
32. Zarivach, R., M. Vuckovic, N. C. Strynadka. 2007. Structural analysis of a prototypical ATPase from the type III secretion system. Nat. Struct. Mol. Biol. 14:131-137. (Pubitemid 46245809)
33. Wilharm, G., V. Lehmann, K. Trülzsch. 2004. Yersinia enterocoli- tica type III secretion depends on the proton, motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72:4004-4009. (Pubitemid 38821915)
34. Blocker, A. J., J. E. Deane, S. M. Lea. 2008. What's the point of the type III secretion system needle? Prot: Natl. Acad. Sci. USA. 105:6507-6513. (Pubitemid 351754539)
35. Samatey, F. A., H. Matsunami, K. Namba. 2004. Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature. 431:1062-1068.
36. Yonekura, K., S. Maki-Yonekura, and K. Namba. 2003. Complete atomic model of the bacterial, flagellar filament by electron cryomicroscopy. Nature. 424:643-650. (Pubitemid 36987983)
37. Paul, K., M. Erhardt, K. T. Hughes. 2008. Energy source of flagellar type III secretion. Nature. 451:489-492. (Pubitemid 351158887)
38. Galán, J. E. 2008. Energizing type III secretion machines: what is the fuel? Nat. Struct. Mol. Biol. 15:127-128.
39. Minamino, T., and K. Namba. 2008. Distinct roles of the FliL ATPase and proton motive force in bacterial flagellar protein export. Nature. 451:485-488. (Pubitemid 351158881)
40. Johnson, S., J. E. Deane, and S. M. Lea. 2005. The type III needle and the damage done. Curr. Opin, Struct. Biol. 15:700-707. (Pubitemid 41668527)
41. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA. http://www.pymol.org.