Differences in dynamic structure of LC8 monomer, dimer, and dimer-peptide complexes

Biochemistry

Volumn 47, Issue 46, 2008, Pages 11940-11952

  Hall, Justin ^a   Hall, Andrea ^a   Pursifull, Nathan ^a   Barbar, Elisar ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; BINDING ENERGY; BIOCHEMISTRY; CHEMICAL REACTIONS; CONCENTRATION (PROCESS); CONFORMATIONS; DIMERIZATION; DISSOCIATION; DYNAMICS; LIGANDS; MONOMERS; PHOSPHORYLATION;

BACKBONE DYNAMICS; BINDING CAPABILITIES; BINDING MODES; CONFORMATIONAL DYNAMICS; CONFORMATIONAL HETEROGENEITIES; DEGREE OF ORDERINGS; DIMER INTERFACES; DYNAMIC STRUCTURES; HETEROGENEOUS DYNAMICS; IN VITRO; LIGAND BINDINGS; LIGHT CHAINS; NEUTRAL PH; PEPTIDE COMPLEXES; PROTEIN CONCENTRATIONS; REDUCED COMPLEXITIES;

BINDING SITES;

DIMER; DYNEIN ADENOSINE TRIPHOSPHATASE; MONOMER; PEPTIDE;

ARTICLE; DIMERIZATION; ENTROPY; LIGAND BINDING; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ANIMALS; CARRIER PROTEINS; DIMERIZATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HYDROGEN-ION CONCENTRATION; LIGANDS; MODELS, MOLECULAR; MUTATION; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; RNA-BINDING PROTEINS;

EID: 56249116551     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801093k     Document Type: Article

References (52)

1. King, S. M., Barbarese, E., Dillman, J. F., PatelKing, R. S., Carson, J. H., and Pfister, K. K. (1996) Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved M(r) 8,000 light chain. J. Biol. Chem. 271, 19358-19366.
2. Makokha, M., Hare, M., Li, M. G., Hays, T., and Barbar, E. (2002) Interactions of cytoplasmic dynein light chains Tctex-1 and LC8 with the intermediate chain IC74. Biochemistry 41, 4302-4311.
3. Lo, K. W. H., Naisbitt, S., Fan, J. S., Sheng, M., and Zhang, M. J. (2001) The 8-kDa dynein light chain binds to its targets via a conserved (K/R)XTQT motif. J. Biol. Chem. 276, 14059-14066.
4. Jaffrey, S. R., and Snyder, S. H. (1996) PIN: An associated protein inhibitor of neuronal nitric oxide synthase. Science 274, 774.
5. Puthalakath, H., Huang, D. C. S., O'Reilly, L. A., King, S. M., and Strasser, A. (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3, 287-296.
6. Wang, L., Hare, M., Hays, T. S., and Barbar, E. (2004) Dynein light chain LC8 promotes assembly of the coiled-coil domain of swallow protein. Biochemistry 43, 4611-4620.
7. Schnorrer, F., Bohmann, K., and Nusslein-Volhard, C. (2000) The molecular motor dynein is involved in targeting Swallow and bicoid RNA to the anterior pole of Drosophila oocytes. Nat. Cell Biol. 2, 185-190.
8. Tan, G. S., Preuss, M. A., Williams, J. C., and Schnell, M. J. (2007) The dynein light chain 8 binding motif of rabies virus phosphoprotein promotes efficient viral transcription. Proc. Natl. Acad. Sci. U.S.A. 104, 7229-7234.
9. Stelter, P., Kunze, R., Flemming, D., Hopfner, D., Diepholz, M., Philippsen, P., Bottcher, B., and Hurt, E. (2007) Molecular basis for the functional interaction of dynein light chain with the nuclear-pore complex. Nat. Cell Biol. 9, 788-796.
10. Benison, G., Karplus, P. A., and Barbar, E. (2007) Structure and dynamics of LC8 complexes with KXTQT-motif peptides: Swallow and dynein intermediate chain compete for a common site. J. Mol. Biol. 371, 457-468.
11. Williams, J. C., Roulhac, P. L., Roy, A. G., Vallee, R. B., Fitzgerald, M. C., and Hendrickson, W. A. (2007) Structural and thermodynamic characterization of a cytoplasmic dynein light chain-intermediate chain complex. Proc. Natl. Acad. Sci. U.S.A. 104, 10028-10033.
12. Liang, J., Jaffrey, S. R., Guo, W., Snyder, S. H., and Clardy, J. (1999) Structure of the PIN/LC8 dimer with a bound peptide. Nat. Struct. Biol. 6, 735-740.
13. Fan, J. S., Zhang, Q., Tochio, H., Li, M., and Zhang, M. J. (2001) Structural basis of diverse sequence-dependent target recognition by the 8 kDa dynein light chain. J. Mol. Biol. 306, 97-108.
14. Barbar, E. (2008) Dynein light chain LC8 is a dimerization hub essential in diverse protein networks. Biochemistry 47, 503-508.
15. Nyarko, A., Hare, M., Hays, T. S., and Barbar, E. (2004) The intermediate chain of cytoplasmic dynein is partially disordered and gains structure upon binding to light-chain LC8. Biochemistry 43, 15595-15603.
16. Benison, G., Karplus, P. A., and Barbar, E. (2008) The interplay of ligand binding and quaternary structure in the diverse interactions of dynein light chain LC8. J. Mol. Biol. (in press).
17. Barbar, E., Kleinman, B., Imhoff, D., Li, M. G., Hays, T. S., and Hare, M. (2001) Dimerization and folding of LC8, a highly conserved light chain of cytoplasmic dynein. Biochemistry 40, 1596-1605.
18. Makokha, M., Huang, Y. J., Montelione, G., Edison, A. S., and Barbar, E. (2004) The solution structure of the pH induced monomer of dynein light chain from Drosophila. Protein Sci. 13, 727-734.
19. Wang, W., Lo, K. W., Kan, H. M., Fan, J. S., and Zhang, M. (2003) Structure of the monomeric 8-kDa dynein light chain and mechanism of the domain-swapped dimer assembly. J. Biol. Chem. 278, 41491-41499.
20. Song, C., Wen, W., Rayala, S. K., Chen, M., Ma, J., Zhang, M., and Kumar, R. (2008) Serine 88 phosphorylation of the 8-kDa dynein light chain 1 is a molecular switch for its dimerization status and functions. J. Biol. Chem. 283, 4004-4013.
21. Song, Y., Benison, G., Nyarko, A., Hays, T. S., and Barbar, E. (2007) Potential role for phosphorylation in differential regulation of the assembly of dynein light chains. J. Biol. Chem. 282, 17272-17279.
22. Nyarko, A., Cochrun, L., Norwood, S., Pursifull, N., Voth, A., and Barbar, E. (2005) Ionization of His 55 at the dimer interface of dynein light-chain LC8 is coupled to dimer dissociation. Biochemistry 44, 14248-14255.
23. Barbar, E., and Hare, M. (2004) Characterization of the cargo attachment complex of cytoplasmic dynein using NMR and mass spectrometry. Methods Enzymol. 380, 219-241.
24. Fan, J. S., Zhang, Q. A., Li, M., Tochio, H., Yamazaki, T., Shimizu, M., and Zhang, M. J. (1998) Protein inhibitor of neuronal nitric-oxide synthase, PIN, binds to a 17-amino acid residue fragment of the enzyme. J. Biol. Chem. 273, 33472-33481.
25. Cheng, X., Gonzalez, M. L., and Lee, J. C. (1993) Energetics of intersubunit and intrasubunit interactions of Escherichia coli adenosine cyclic 3′,5′-phosphate receptor protein. Biochemistry 32, 8130-8139.
26. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068.
27. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6, 135-140.
28. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J. Biomol. NMR 4, 727-734.
29. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
30. Benison, G., Berkholz, D. S., and Barbar, E. (2007) Protein assignments without peak lists using higher-order spectra. J. Magn. Reson. 189, 173-181.
31. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647-1651.
32. Clore, G. M., Szabo, A., Bax, A., Kay, L. E., Driscoll, P. C., and Gronenborn, A. M. (1990) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112, 4989-4991.
33. Lipari, G., and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104, 4546.
34. Dosset, P., Hus, J. C., Marion, D., and Blackledge, M. (2001) A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings. J. Biomol. NMR 20, 223-231.
35. 15N NMR relaxation. J. Am. Chem. Soc. 117, 12562-12566.
36. Mandel, A. M., Akke, M., and Palmer, A. G., III. (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163.
37. Hwang, T. L., van Zijl, P. C., and Mori, S. (1998) Accurate quantitation of water-amide proton exchange rates using the phase-modulated CLEAN chemical Exchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme. J. Biomol. NMR 11, 221-226.
38. Turnbull, W. B., and Daranas, A. H. (2003) On the value of c: can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866.
39. Mohan, P. M., Barve, M., Chatterjee, A., and Hosur, R. V. (2006) pH driven conformational dynamics and dimer-to-monomer transition in DLC8. Protein Sci. 15, 335-342.
40. Schlunegger, M. P., Bennett, M. J., and Eisenberg, D. (1997) Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. Adv. Protein Chem. 50, 61-122.
41. Chatterjee, A., Krishna Mohan, P. M., Prabhu, A., Ghosh-Roy, A., and Hosur, R. V. (2007) Equilibrium unfolding of DLC8 monomer by urea and guanidine hydrochloride: Distinctive global and residue level features. Biochimie 89, 117-134.
42. Krishna Mohan, P. M., Barve, M., Chatterjee, A., Ghosh-Roy, A., and Hosur, R. V. (2008) NMR comparison of the native energy landscapes of DLC8 dimer and monomer. Biophys. Chem. 134, 10-19.
43. Krishna Mohan, P. M. (2007) Unfolding energetics and conformational stability of DLC8 monomer. Biochimie 89, 1409-1415.
44. Fan, J. S., Zhang, Q., Tochio, H., and Zhang, M. (2002) Backbone dynamics of the 8 kDa dynein light chain dimer reveals molecular basis of the protein's functional diversity. J. Biomol. NMR 23, 103-114.
45. Mohan, P. M., and Hosur, R. V. (2008) NMR characterization of structural and dynamics perturbations due to a single point mutation in Drosophila DLC8 dimer: functional implications. Biochemistry 47, 6251-6259.
46. Rodriguez-Crespo, I., Yelamos, B., Roncal, F., Albar, J. P., Ortiz de Montellano, P. R., and Gavilanes, F. (2001) Identification of novel cellular proteins that bind to the LC8 dynein light chain using a pepscan technique. FEBS Lett. 503, 135-141.
47. Frederick, K. K., Marlow, M. S., Valentine, K. G., and Wand, A. J. (2007) Conformational entropy in molecular recognition by proteins. Nature 448, 325-329.
48. Dunker, A. K., Cortese, M. S., Romero, P., Iakoucheva, L. M., and Uversky, V. N. (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J. 272, 5129-5148.
49. Lee, A. L., Kinnear, S. A., and Wand, A. J. (2000) Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex. Nat. Struct. Biol. 7, 72-77.
50. Leung, D. H., Bergman, R. G., and Raymond, K. N. (2008) Enthalpy-entropy compensation reveals solvent reorganization as a driving force for supramolecular encapsulation in water. J. Am. Chem. Soc. 130, 2798-2805.
51. Vadlamudi, R. K., Bagheri-Yarmand, R., Yang, Z., Balasenthil, S., Nguyen, D., Sahin, A. A., den Hollander, P., and Kumar, R. (2004) Dynein light chain 1, a p21-activated kinase 1-interacting substrate, promotes cancerous phenotypes. Cancer Cell 5, 575-585.
52. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.