Giant protein kinases: Domain interactions and structural basis of autoregulation

EMBO Journal

Volumn 15, Issue 24, 1996, Pages 6810-6821

  Kobe, Bostjan ^a,b   Heierhorst, Jörg ^a,c   Feil, Susanne C ^a   Parker, Michael W ^a   Benian, Guy M ^d   Weiss, Klaudiusz R ^c   Kemp, Bruce E ^a  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Crystal structure; Immunoglobulin; Intrasteric regulation; Protein kinase; Twitchin

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALMODULIN; CONNECTIN; FIBRONECTIN; IMMUNOGLOBULIN; MYOSIN; PROTEIN KINASE;

APLYSIA; ARTICLE; AUTOREGULATION; BINDING SITE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 0030469482     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb01072.x     Document Type: Article

References (74)

1. Ayme-Southgate,A., Southgate,R., Saide,J., Benian,G.M. and Pardue, M.L. (1995) Both synchronous and asynchronous muscle isoforms of projectin (the Drosophila bent locus product) contain functional kinase domains. J. Cell Biol., 128, 393-403.
2. Babu,Y.S., Sack,J.S., Greenhough,T.J., Bugg,C.E., Means,A.R. and Cook,W.J. (1985) Three-dimensional structure of calmodulin. Nature, 315, 37-40.
3. Benian,G.M., Kiff,J.E., Neckleman,N., Moerman,D.G. and Waterston, R.H. (1989) Sequence of an unusually large protein implicated in regulation of myosin activity in C.elegans. Nature, 342, 45-50.
4. Benian,G.M., L'Hernault,S.W. and Morris,M.E. (1993) Additional sequence complexity in the muscle gene, unc-22, and its encoded protein, twitchin, of Caenorhabditis elegans. Genetics, 134, 1097-1104.
5. 2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J., 12, 849-859.
6. Brünger,A.T. (1990) Extension of molecular replacement: a new search strategy base on Patterson correlation coefficient. Acta Crysiallogr., A46, 46-57.
7. Brünger,A.T. (1992a) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-475.
8. Brünger,A.T. (1992b) X-PLOR Version 3.1. Yale University, New Haven, CT.
9. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Cryslallogr., D50, 760-763.
10. Dasgupta,M., Honeycutt,T. and Blumenthal,D.K. (1989) The γ-subunit of skeletal muscle phosphorylase kinase contains two noncontiguous domains that act in concert to bind calmodulin. J. Biol. Chem., 264, 17156-17163.
11. Dibb,N.J., Brown,D.M., Karn,J., Moerman,D.G., Bolten,S.L. and Waterston,R.H. (1985) Sequence analysis of mutations that affect the synthesis, assembly and enzymatic activity of the unc-54 myosin heavy chain of Caenorhabditis elegans. J. Mol. Biol., 183, 543-551.
12. Eisenberg,D. and McLachlan,A.D. (1986) Solvation energy in protein folding and binding. Nature, 319, 199-203.
13. Gautel,M., Castiglione Morelli,M.A., Pfuhl,M., Motta,A. and Pastore,A. (1995) A calmodulin-binding sequence in the C-terminus of human cardiac titin kinase. Eur. J. Biochem., 230, 752-759.
14. Gibbs,C.S., Knighton,D.R., Sowadski,J.M., Taylor,S.S. and Zoller,M.J. (1992) Systematic mutational analysis of cAMP-dependent protein kinase identifies unregulated catalytic subunits and defines regions important for the recognition of the regulatory subunit. J. Biol. Chem., 267, 4806-4814.
15. Goldberg,J., Nairn,A.C. and Kuriyan,J. (1996) Structural basis for the auto-inhibition of calcium/calmodulin-dependent protein kinase I. Cell, 84, 875-887.
16. Goldsmith,E.J. and Cobb,M.H. (1994) Protein kinases. Curr. Opin. Struct. Biol., 4, 833-840.
17. Haribabu,B., Hook,S.S., Selbert,M.A., Goldstein.E.G., Tomhave,E.D., Edelman,A.M., Snyderman,R. and Means,A.R. (1995) Human calcium-calmodulin dependent protein kinase 1: cDNA cloning, domain structure and activation by phosphorylation at threonine-177 by calcium-calmodulin dependent protein kinase I kinase. EMBO J., 14, 3679-3686.
18. Harpaz,Y. and Chothia,C. (1994) Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J. Mol. Biol., 238, 528-539.
19. Heierhorst,J., Probst,W.C., Vilim,F.S., Buku,A. and Weiss,K.R. (1994) Autophosphorylation of molluscan twitchin and interaction of its kinase domain with calcium/calmodulin. J. Biol. Chem., 269, 21086-21093.
20. Heierhorst,J., Probst,W.C., Kohanski,R.A., Buku,A. and Weiss,K.R. (1995) Phosphorylation of myosin regulatory light chains by the molluscan twitchin kinase. Eur. J. Biochem., 233, 426-431.
21. 2+/S100 regulation of giant protein kinases. Nature, 380, 636-639.
22. Holden,H.M., Ito,M., Hartshorne,D.J. and Rayment,I. (1992) X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase at 2.8 Å resolution. J. Mol. Biol., 227, 840-851.
23. Houmeida,A., Holt,J., Tskhovrebova,L. and Trinick,J. (1995) Studies of the interaction between titin and myosin. J. Cell Biol., 131, 1471-1481.
24. Hu,S.-H., Parker,M.W., Lei,J.Y., Wilce,M.C.J., Benian,G.M. and Kemp.B.E. (1994) Insights into autoregulation from the crystal structure of twitchin kinase. Nature, 369, 581-584.
25. Hubbard,S.R., Wei,L., Ellis,L. and Hendrickson,W.A. (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature, 372, 746-754.
26. Ikura,M., Clore,G.M., Gronenborn,A.M., Zhu,G., Klee,C.B. and Bax,A. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science, 256, 632-638.
27. Improta,S., Politou,A.S. and Pastore,A. (1996) Immunoglobulin-like modules from titin I-band: extensible components of muscle elasticity. Structure, 4, 323-337.
28. Jancarik,J. and Kim,S.-H. (1991) Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallogr., 24, 409-411.
29. Janin,J. (1995) Elusive affinities. Proteins, 21, 30-39.
30. Jeffrey,P.D., Russo,A.A., Polyak,K., Gibbs,E., Hurwitz,G., Massague,J. and Pavletich,N.P. (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature, 376, 313-320.
31. Jones,T.A., Bergdoll,M. and Kjeldgaard,M. (1990) O: a macromolecule modeling environment. In Bugg,C.E. and Ealick,S.E. (eds), Crystallographic and Modeling Methods in Molecular Design. Springer-Verlag, New York, pp. 189-195.
32. Jones,T.A., Zou,J.-Y., Cowan,S.W. and Kjeldgaard,M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A47, 110-119.
33. Kabsch,W. and Sander,C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
34. Kamm,K.E. and Stull,J.T. (1985) The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu. Rev. Pharmacol. Toxicol., 25, 593-620.
35. Kanoh,S., Ito,M., Niwa,E., Kawano,Y. and Hartshorne,D.J. (1993) Actin-binding peptide from smooth muscle myosin light chain kinase. Biochemistry, 32, 8902-8907.
36. Katoh,T. and Fujisawa,H. (1991) Calmodulin-dependent protein kinase II. Kinetic studies on the interaction with substrates and calmodulin. Biochim. Biophys. Acta, 1091, 205-212.
37. Kemp,B.E., Faux,M.C., Means,A.R., House,C., Tiganis,T., Hu,S.-H. and Mitchelhill,K.I. (1994) Structural aspects: pseudosubstrate and substrate interactions. In Woodgett,J.R. (ed.), Protein Kinases. IRL Press at Oxford University Press, Oxford, pp. 30-67.
38. Kennely,P.J., Colburn,J.C., Lorenzen,J., Edelman,A.M., Stull,J.T. and Krebs,E.G. (1991) Activation mechanism of rabbit skeletal muscle myosin light chain kinase. FEBS Lett., 286, 217-220.
39. Kleywegt,G.J. and Jones,T.A. (1995) Where freedom is given, liberties are taken. Structure, 3, 535-540.
40. Kleywegt,G.J., Bergfors,T., Senn,H., Le Motte,P., Gsell,B., Shudo,K. and Jones,T.A. (1994) Crystal structures of cellular retinoic acid binding proteins I and II in complex with all-trans-retinoic acid and a synthetic retinoid. Structure, 2, 1241-1258.
41. Knighton,D.R., Zheng,J., Eyck,L.F.T., Ashford,V.A., Xuong,N.-H., Taylor,S.S. and Sowadski,J.M. (1991) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science, 253, 407-414.
42. Kraulis,P. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
43. Krueger,J.K., Padre,R.C. and Stull,J.T. (1995) Intrasteric regulation of myosin light chain kinase. J. Biol. Chem., 270, 16848-16853.
44. Labeit,S. and Kolmerer,B. (1995) Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science, 270, 293-296.
45. Labeit,S., Gautel,M., Lakey,A. and Trinick,J. (1992) Towards a molecular understanding of titin. EMBO J., 11, 1711-1716.
46. Laskowski,R.A., MacArthur,M.W., Moss,D.S. and Thornton,J.M. (1993) PROCHECK, a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
47. Lawrence,M.C. and Colman,P.M. (1993) Shape complementarity at protein-protein interfaces. J. Mol. Biol., 234, 946-950.
48. Leahy,D.J., Aukhil,I. and Erickson,H.P. (1996) 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell, 84, 155-164.
49. Lei,J., Tang,X., Chamber,T.C., Pohl,J. and Benian,G.M. (1994) The protein kinase domain of twitchin has protein kinase activity and an autoinhibitory region. J. Biol. Chem., 269, 21078-21085.
50. Luzzati,P.V. (1952) Traitements statistique des erreurs dans la détermination des structures cristallines. Acta Crystallogr., 5, 802-810.
51. Lüthy,R., Bowie,J.U. and Eisenberg,D. (1992) Assessment of protein models with three-dimensional profiles. Nature, 356, 83-85.
52. McPherson,A. (1982) Preparation and Analysis of Protein Crystals. John Wiley and Sons, New York.
53. Meador,W.E., Means,A.R. and Quiocho,F.A. (1992) Target enzyme recognition by calmodulin: 2.4 Å structure of a calmodulin-peptide complex. Science, 257, 1251-1255.
54. Meador,W.E., Means,A.R. and Quiocho,F.A. (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of X-ray structures. Science, 262, 1718-1721.
55. Navaza,J. (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr., A50, 157-163.
56. Nicholls,A., Sharp,K.A. and Honig,B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
57. 2+calmodulin-dependent protein kinase Gr and calspermin: a gene within a gene. Proc. Natl Acad. Sci. USA, 88, 5784-5788.
58. Okagaki,T., Weber,F.E., Fischman,D.A., Vaughan,K.T., Mikawa,T. and Reinach,F.C. (1993) The major myosin-binding domain of skeletal muscle MyBP-C (C protein) resides in the COOH-terminal, immunoglobulin C2 motif. J. Cell Biol., 123, 619-626.
59. Olson,N.J., Pearson,R.B., Needleman,D.S., Hurwitz,M.Y., Kemp,B.E. and Means,A.R. (1990) Regulatory and structural motifs of chicken gizzard myosin light chain kinase. Proc. Natl Acad. Sci. USA, 87, 2284-2288.
60. Otwinowski,Z. (1993) Data collection and processing. In Sawyer,L., Isaacs,N. and Bailey,S. (eds). Proceedings of the CCP4 Study Weekend. SERC, Daresbury Laboratory, Daresbury, UK, pp. 56-62.
61. Pfuhl,M. and Pastore,A. (1995) Tertiary structure of an immunoglobulin-like domain from the giant muscle protein titin: a new member of the I set. Structure, 3, 391-401.
62. Pfuhl,M., Winder,S.J., Castiglione Morelli,M.A., Labeit,S. and Pastore,A. (1996) Correlation between conformational and binding properties of nebulin repeats. J. Mol. Biol., 257, 367-384.
63. Politou,A.S., Gautel,M., Improta,S., Vangelista,L. and Pastore,A. (1996) The elastic I-band region of titin is assembled in a 'modular' fashion by weakly interacting Ig-like domains. J. Mol. Biol., 255, 604-616.
64. 2+-binding proteins. Nature Struct. Biol., 2, 790-796.
65. Read,R.J. (1986) Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr., A42, 140-149.
66. Rice,L.M. and Brünger,A.T. (1994) Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refinement. Proteins, 19, 277-290.
67. Sakabe,N. (1991) X-ray diffraction data collection system for modern protein crystallography with a Weissenberg camera and an imaging plate using synchrotron radiation. Nucl. Instr. Methods Phys. Res., A303, 448-463.
68. Schäfer,B.W. and Heizmann,C.W. (1996) The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem. Sci., 21, 134-140.
69. Shirinsky,V.P., Vorotnikov,A.V., Birukov,K.G., Nanaev,A.K., Collinge,M., Lukas,T.J., Sellers,J.R. and Watterson,D.M. (1993) A kinase-related protein stabilizes unphosphorylated smooth muscle myosin minifilaments in the presence of ATP. J. Biol. Chem., 268, 16578-16583.
70. Taylor,S.S. and Radzio-Andzelm,E. (1994) Cyclic AMP-dependent protein kinase. In Woodgett,J.R. (ed.). Protein Kinases. IRL Press at Oxford University Press, Oxford, pp. 1-29.
71. Trinick,J. (1994) Titin and nebulin: protein rulers in muscle. Trends Biochem. Sci., 19, 405-409.
72. Waterston,R.H., Thomson,J.N. and Brenner,S. (1980) Mutants with altered muscle structure of Caenorhabditis elegans. Dev. Biol., 77, 271-302.
73. Wilson,A.J.C. (1949) The probability distribution of X-ray intensities. Acta Crystallogr., 2, 318-321.
74. Yokokura,H., Picciotto,M.R., Nairn,A.C. and Hidaka,H. (1995) The regulatory region of calcium/calmodulin-dependent protein kinase I contains closely associated autoinhibitory and calmodulin-binding domains. J. Biol. Chem., 270, 23851-23859.