Allosteric transitions in biological nanomachines are described by robust normal modes of elastic networks

Current Protein and Peptide Science

Volumn 10, Issue 2, 2009, Pages 128-132

  Zheng, Wenjun ^a   Brooks, Bernard R ^b   Thirumalai, D ^c  

^a UNIVERSITY AT BUFFALO   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c Bldg 142   (United States)

Author keywords

Allostery; Chaperonin; Elastic network model; Myosin; Normal mode analysis; Polymerase

Indexed keywords

CHAPERONIN; DNA POLYMERASE; MYOSIN II;

ALLOSTERISM; BIOINFORMATICS; COMPUTER ANALYSIS; GENETIC CONSERVATION; MATHEMATICAL COMPUTING; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRUCTURAL GENOMICS; STRUCTURE ACTIVITY RELATION;

ALLOSTERIC REGULATION; CHAPERONIN 60; DNA-DIRECTED DNA POLYMERASE; ELASTICITY; MODELS, MOLECULAR; MYOSIN TYPE II; NANOSTRUCTURES; PROTEIN CONFORMATION;

EID: 65649154062     PISSN: 13892037     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920309787847608     Document Type: Review

References (44)

1. Tirion, M.M. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. (1996) Phys. Rev. Lett., 77, 1905-1908.
2. Hinsen, K. Analysis of domain motions by approximate normal mode calculations. (1998) Proteins, 33, 417-429.
3. Krebs, W.G., Alexandrov, V., Wilson, C.A., Echols, N., Yu, H. and Gerstein, M. Normal mode analysis of macromolecular motions in a database framework: developing mode concentration as a useful classifying statistic. (2002) Proteins, 48, 682-695.
4. Bahar, I. and Rader, A.J. Coarse-grained normal mode analysis in structural biology. (2005) Curr. Opin. Struct. Biol., 15, 586-592.
5. Ma, J. Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. (2005) Structure, 13, 373-380.
6. Tama, F. and Brooks, C.L. Symmetry, form, and shape: guiding principles for robustness in macromolecular machines. (2006) Annu. Rev. Biophys. Biomol. Struct., 35, 115-133.
7. Anfinsen, C.B. Principles that govern the folding of protein chains. ( 1973) Science, 181, 223-230.
8. Zheng, W., Brooks, B.R., Doniach, S. and Thirumalai, D. Network of dynamically important residues in the open/closed transition in polymerases is strongly conserved. (2005) Structure, 13, 565-577.
9. Zheng, W., Brooks, B.R. and Thirumalai, D. Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. (2006) Proc. Natl. Acad. Sci. USA, 103, 7664-7669.
10. Zheng, W., Brooks, B.R. and Thirumalai, D. Allosteric transitions in the chaperonin GroEL are captured by a dominant normal mode that is most robust to sequence variations. (2007) Biophys. J., 93, 2289-2299.
11. Ollis, D.L., Brick, P., Hamlin, R., Xuong, N.G. and Steitz, T.A. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. (1985) Nature, 313, 762-766.
12. Li, Y., Korolev, S. and Waksman, G. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. (1998) EMBO J., 17, 7514-7525.
13. Patel, P.H., Kawate, H., Adman, E., Ashbach, M. and Loeb, L.A. A single highly mutable catalytic site amino acid is critical for DNA polymerase fidelity. (2000) J. Biol. Chem., 276, 5044-5051.
14. Suzuki, M., Yoshida, S., Adman, E.T., Blank, A. and Loeb, L.A. Thermus aquaticus DNA polymerase I mutants with altered fidelity. Interacting mutations in the O-helix. (2000) J. Biol. Chem., 275, 32728-32735.
15. Suzuki, M., Avicola, A.K., Hood, L. and Loeb, L.A. Low fidelity mutants in the O-helix of Thermus aquaticus DNA polymerase I. (1997) J. Biol. Chem., 272, 11228-11235.
16. Kermekchiev, M.B., Tzekov, A. and Barnes, W.M. Cold-sensitive mutants of Taq DNA polymerase provide a hot start for PCR. (2003) Nucleic Acids Res., 31, 6139-6147.
17. Geeves, M.A. and Holmes, K.C. Structural mechanism of muscle contraction. (1999) Annu. Rev. Biochem., 68, 687-728.
18. Houdusse, A., Szent-Gyorgyi, A.G. and Cohen, C. Three conformational states of scallop myosin S1. (2000) Proc. Natl. Acad. Sci. USA, 97, 11238-11243.
19. Coureux, P.D., Wells, A.L., Menetrey, J., Yengo, C.M., Morris, C.A., Sweeney, H.L. and Houdusse, A. A structural state of the myosin V motor without bound nucleotide. (2003) Nature, 425, 419-423.
20. Reubold, T.F., Eschenburg, S., Becker, A., Kull, F.J. and Manstein, D.J. A structural model for actin-induced nucleotide release in myosin. ( 2003) Nat. Struct. Biol., 10, 826-830.
21. Holmes, K.C., Angert, I., Kull, F.J., Jahn, W. and Schroder, R.R. Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. (2003) Nature, 425, 423-427.
22. Fujita, H., Sugiura, S., Momomura, S., Sugi, H. and Sutoh, K. Functional characterization of Dictyostelium discoideum mutant myosins equivalent to human familial hypertrophic cardiomyopathy. (1998) Adv. Exp. Med. Biol., 453, 131-137.
23. Zeng, W., Conibear, P.B., Dickens, J.L., Cowie, R.A., Wakelin, S., Malnasi-Csizmadia, A. and Bagshaw, C.R. Dynamics of actomyosin interactions in relation to the cross-bridge cycle. (2004) Philos. Trans. R. Soc. Lond. B. Biol. Sci., 359, 1843-1855.
24. Patterson, B. and Spudich, J.A. Cold-sensitive mutations of Dictyostelium myosin heavy chain highlight functional domains of the myosin motor. (1996) Genetics, 143, 801-810.
25. Batra, R., Geeves, M.A. and Manstein, D.J. Kinetic analysis of Dictyostelium discoideum myosin motor domains with glycine-to-alanine mutations in the reactive thiol region. (1999) Biochemistry, 38, 6126-3614.
26. Patterson, B., Ruppel, K.M., Wu, Y. and Spudich, J.A. Cold-sensitive mutants G680V and G691C of Dictyostelium myosin II confer dramatically different biochemical defects. (1997) J. Biol. Chem., 272, 27612-27617.
27. Ruppel, K.M. and Spudich, J.A. Structure-function analysis of the motor domain of myosin. (1996) Annu. Rev. Cell Dev. Biol., 12, 543-573.
28. Tsiavaliaris, G., Fujita-Becker, S., Batra, R., Levitsky, D.I., Kull, F.J., Geeves, M.A. and Manstein, D.J. Mutations in the relay loop region result in dominant-negative inhibition of myosin II function in Dictyostelium. (2002) EMBO Rep., 3, 1099-1105.
29. Sigler, P.B., Xu, Z., Rye, H.S., Burston, S.G., Fenton, W.A. and Horwich, A.L. Structure and function in GroEL-mediated protein folding. (1998) Annu. Rev. Biochem., 67, 581-608.
30. Thirumalai, D. and Lorimer, G.H. Chaperonin-mediated protein folding. (2001) Annu. Rev. Biophys. Biomol. Struct., 30, 245-269.
31. Horovitz, A., Fridmann, Y., Kafri, G. and Yifrach, O. Review: Allostery in chaperonins. (2001) J. Struct. Biol., 135, 104-114.
32. Fenton, W.A., Kashi, Y., Furtak, K. and Horwich, A.L. Residues in chaperonin GroEL required for polypeptide binding and release. (1999) Nature, 371, 614-619.
33. Klein, G. and Georgopoulos, C. Identification of important amino acid residues that modulate binding of Escherichia coli GroEL to its various cochaperones. (2001) Genetics, 158, 507-517.
34. Murai, N., Makino, Y. and Yoshida, M. GroEL locked in a closed conformation by an interdomain cross-link can bind ATP and polypeptide but cannot process further reaction steps. (1996) J. Biol. Chem., 271, 28229-28234.
35. Xu, Z., Horwich, A.L., Sigler, P.B. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. (1997) Nature, 388, 741-750.
36. Buckle, A.M., Zahn, R., and Fersht, A.R. A structural model for GroEL-polypeptide recognition. (1997) Proc. Natl. Acad. Sci. USA, 94, 3571-3575.
37. Chen, L. and Sigler, P.B. The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. (1999) Cell, 99, 757-768.
38. Danziger, O., Shimon, L. and Horovitz, A. Glu257 in GroEL is a sensor involved in coupling polypeptide substrate binding to stimulation of ATP hydrolysis. (2006) Protein Sci., 15, 1270-1276.
39. Stan, G., Brooks, B.R. and Thirumalai, D. Probing the "annealing" mechanism of GroEL minichaperone using molecular dynamics simulations. (2005) J. Mol. Biol., 350, 817-829.
40. Kass, I. and Horovitz, A. Mapping pathways of allosteric communication in GroEL by analysis of correlated mutations. (2002) Proteins, 48, 611-617.
41. Sun, Z., Scott, D.J. and Lund, P.A. Isolation and characterization of mutants of GroEL that are fully functional as single rings. (2003) J. Mol. Biol., 332, 715-728.
42. Ranson, N.A., Farr, G.W., Roseman, A.M., Gowen, B., Fenton, W.A., Horwich, A.L. and Saibil, H.R. ATP-bound states of GroEL captured by cryo-electron microscopy. (2001) Cell, 107, 869-879.
43. Lockless, S.W. and Ranganathan, R. Evolutionarily conserved pathways of energetic connectivity in protein families. (1999) Science, 286, 295-299.
44. Suel, G.M., Lockless, S.W., Wall, M.A. and Ranganathan, R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. (2003) Nat. Struct. Biol., 10, 59-69.