Structural analysis of the regulation of the DYNLL/LC8 binding to Nek9 by phosphorylation

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 12283-12294

  Gallego, Pablo ^a   Velazquez Campoy, Adrian ^b,c   Regue, Laura ^d,e   Roig, Joan ^d   Reverter, David ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c FUNDACIÓN ARAID   (Spain)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHOSPHORYLATION; BINDING AFFINITIES; BINDING MOTIF; MULTIPLE INTERACTIONS; PROTEIN KINASE; PROTEIN-PROTEIN COMPLEXES; REGULATORY MECHANISM; SHEDDING LIGHT;

BINDING ENERGY; EXPERIMENTS; PEPTIDES; SIGNAL TRANSDUCTION; STRUCTURAL ANALYSIS;

PHOSPHORYLATION;

DYNEIN ADENOSINE TRIPHOSPHATASE; NEK9 PROTEIN; NIMA KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; BETA SHEET; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPLEX FORMATION; CRYSTAL STRUCTURE; DIMERIZATION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SPINDLE CELL;

AMINO ACID MOTIFS; BINDING SITES; CYTOPLASMIC DYNEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SERINE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84876891702     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.459149     Document Type: Article

References (48)

1. Roig, J., Mikhailov, A., Belham, C., and Avruch, J. (2002) Nercc1, a mammalian NIMA-family kinase, binds the Ran GTPase and regulates mitotic progression. Genes Dev. 16, 1640-1658
2. O'Connell, M. J., Krien, M. J., and Hunter, T. (2003) Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol. 13, 221-228
3. Quarmby, L. M., and Mahjoub, M. R. (2005) Caught Nek-ing: cilia and centrioles. J. Cell Sci. 118, 5161-5169
4. O'regan, L., Blot, J., and Fry, A. M. (2007) Mitotic regulation by NIMA-related kinases. Cell Div. 2, 25
5. Roig, J., Groen, A., Caldwell, J., and Avruch, J. (2005) Active Nercc1 protein kinase concentrates at centrosomes early in mitosis and is necessary for proper spindle assembly. Mol. Biol. Cell 16, 4827-4840
6. Bertran, M. T., Sdelci, S., Regué, L., Avruch, J., Caelles, C., and Roig, J. (2011) Nek9 is a Plk1-activated kinase that controls early centrosome separation through Nek6/7 and Eg5. EMBO J. 30, 2634-2647
7. Rapley, J., Nicolàs, M., Groen, A., Regué, L., Bertran, M. T., Caelles, C., Avruch, J., and Roig, J. (2008) The NIMA-family kinase Nek6 phosphoryl-ates the kinesin Eg5 at a novel site necessary for mitotic spindle formation. J. CellSci. 121, 3912-3921
8. Belham, C., Roig, J., Caldwell, J. A., Aoyama, Y., Kemp, B. E., Comb, M., and Avruch, J. (2003) A mitotic cascade of NIMA family kinases. Nercc1/Nek9 activates the Nek6 and Nek7 kinases. J. Biol. Chem. 278, 34897-34909
9. Sdelci, S., Bertran, M. T., and Roig J. (2011) Nek9, Nek6 and Nek7 and the separation of centrosomes. Cell Cycle 10, 3816-3817
10. Yissachar, N., Salem, H., Tennenbaum, T., and Motro, B. (2006) Nek7 kinase is enriched at the centrosome, and is required for proper spindle assembly and mitotic progression. FEBS Lett. 580, 6489-6495
11. Sdelci, S., Schütz, M., Pinyol, R., Bertran, M. T., Regue, L., Caelles, C., Vernos, I., and Roig, J. (2012) Nek9 phosphorylation of NEDD1/GCP-WD contributes to Plk1 control of gamma-tubulin recruitment to the mitotic centrosome. Curr. Biol. 22, 1516-1523
12. Regue, L., Sdelci, S., Bertran, M. T., Caelles, C., Reverter, D., and Roig, J. (2011) DYNLL/LC8 protein controls signal transduction through the Nek9/Nek6 signaling module by regulating Nek6 binding to Nek9. J. Biol. Chem. 286, 18118-18129
13. Rapali, P., Szenes, A., Radnai, L., Bakos, A., Pal, G., and Nyitray, L. (2011) DYNLL/LC8: a light chain subunit of the dynein motor complex and beyond. FEBS J. 278, 2980-2996
14. King, S. M., and Patel-King, R. S. (1995) The M (r) = 8, 000 and 11, 000 outer arm dynein light chains from Chlamydomonas flagella have cytoplasmic homologues. J. Biol. Chem. 270, 11445-11452
15. King, S. M., Barbarese, E., Dillman, J. F., 3rd, Benashski, S. E., Do, K. T., Patel-King, R. S., and Pfister, K. K. (1998) Cytoplasmic dynein contains a family of differentially expressed light chains. Biochemistry 37, 15033-15041
16. Benashski, S. E., Harrison, A., Patel-King, R. S., and King, S. M. (1997) Dimerization of the highly conserved light chain shared by dynein and myosin V. J. Biol. Chem. 272, 20929-20935
17. Kaiser, F. J., Tavassoli, K., Van den Bemd, G. J., Chang, G. T., Horsthemke, B., Moroy, T., and Lüdecke, H. J. (2003) Nuclear interaction of the dynein light chain LC8a with the TRPS1 transcription factor suppresses the transcriptional repression activity of TRPS1. Hum. Mol. Genet. 12, 1349-1358
18. Puthalakath, H., Huang, D. C, 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
19. Jaffrey, S. R., and Snyder, S. H. (1996) PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science 274, 774-777
20. 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
21. Barbar, E. (2008) Dynein light chain LC8 is a dimerization hub essential in diverse protein networks. Biochemistry 47, 503-508
22. 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
23. Fan, J., Zhang, Q., Tochio, H., Li, M., and Zhang, M. (2001) Structural basis of diverse sequence-dependent target recognition by the 8 kDa dynein light chain. J. Mol. Biol. 306, 97-108
24. 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. 384, 954-966
25. Lightcap, C. M., Sun, S., Lear, J. D., Rodeck, U., Polenova, T., and Williams, J. C. (2008) Biochemical and structural characterization of the Pak1-LC8 interaction. J. Biol. Chem. 283, 27314-27324
26. 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
27. 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 LC8 from Drosophila. Protein Sci. 13, 727-734
28. 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
29. 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
30. Jung, Y., Kim, H., Min, S. H., Rhee, S. G., and Jeong, W. (2008) Dynein light chain LC8 negatively regulates NF-κB through the redox-dependent interaction with IκBα. J. Biol. Chem. 283, 23863-23871
31. 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
32. Lo, K. W., Naisbitt, S., Fan, J. S., Sheng, M., and Zhang, M. (2001) The 8-kDa dynein light chain binds to its targets via a conserved (K/R) XTQT motif. J. Biol. Chem. 276, 14059-14066
33. Rodríguez-Crespo, I., Yelamos, B., Roncal, F., Albar, J. P., Ortiz de Mon-tellano, P. R., and Gavilanes, F. (2001) Identification of novel cellular proteins that bind to the LC8 dynein light chain using a pepscan technique. FEBSLett. 503, 135-141
34. Radnai, L., Rapali, P., Hodi, Z., Süveges, D., Molnar, T., Kiss, B., Becsi, B., Erdodi, F., Buday, L., Kardos, J., Kovacs, M., and Nyitray, L. (2010) Affinity, avidity, and kinetics of target sequence binding to LC8 dynein light chain isoforms. J. Biol. Chem. 285, 38649-38657
35. Gomez, J., and Freire, E. (1995) Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin. J. Mol. Biol. 252, 337-350
36. Velazquez-Campoy, A., Luque, I., Todd, M. J., Milutinovich, M., Kiso, Y., and Freire, E. (2000) Thermodynamic dissection of the binding energetics of KNI-272, a potent HIV-1 protease inhibitor. Protein Sci. 9, 1801-1809
37. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
38. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
39. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
40. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
41. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3, Schrödinger, LLC, New York
42. 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
43. Murphy, K. P., and Freire, E. (1992) Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv. Protein Chem. 43, 313-361
44. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934
45. Lei, K., and Davis, R. J. (2003) JNK phosphorylation of Bim-related members ofthe Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. U. S. A. 100, 2432-2437
46. 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
47. 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
48. Benison, G., Nyarko, A., and Barbar, E. (2006) Heteronuclear NMR identifies a nascent helix in intrinsically disordered dynein intermediate chain: implications for folding and dimerization. J. Mol. Biol. 362, 1082-1093