Spinophilin directs protein phosphatase 1 specificity by blocking substrate binding sites

Nature Structural and Molecular Biology

Volumn 17, Issue 4, 2010, Pages 459-464

  Ragusa, Michael J ^a,b   Dancheck, Barbara ^a   Critton, David A ^b   Nairn, Angus C ^c   Page, Rebecca ^b   Peti, Wolfgang ^a  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR 1; PHOSPHOPROTEIN PHOSPHATASE 1; SPINOPHILIN;

ARTICLE; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; PRIORITY JOURNAL; PROTEIN BINDING;

BINDING SITES; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN PHOSPHATASE 1; SUBSTRATE SPECIFICITY;

EID: 77950519767     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1786     Document Type: Article

References (42)

1. Ubersax, J.A. & Ferrell, J.E. Jr. Mechanisms of specifcity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 8, 530-541 (2007).
2. Cohen, P. The regulation of protein function by multisite phosphorylation\a 25 year update. Trends Biochem. Sci. 25, 596-601 (2000).
3. Alonso, A. et al. Protein tyrosine phosphatases in the human genome. Cell 117, 699-711 (2004). (Pubitemid 38748887)
4. Cohen, P.T. Protein phosphatase 1-targeted in many directions. J. Cell Sci. 115, 241-256 (2002).
5. Kelker, M.S., Page, R. & Peti, W. Crystal structures of protein phosphatase-1 bound to nodularin-R and tautomycin: a novel scaffold for structure-based drug design of serine/threonine phosphatase inhibitors. J. Mol. Biol. 385, 11-21 (2009).
6. Egloff, M.P., Cohen, P.T., Reinemer, P. & Barford, D. Crystal structure of the catalytic subunit of human protein phosphatase 1 and its complex with tungstate. J. Mol. Biol. 254, 942-959 (1995). (Pubitemid 26006861)
7. Goldberg, J. et al. Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature 376, 745-753 (1995).
8. Maynes, J.T. et al. Crystal structure of the tumor-promoter okadaic acid bound to protein phosphatase-1. J. Biol. Chem. 276, 44078-44082 (2001). (Pubitemid 37383979)
9. Hendrickx, A. et al. Docking motif-guided mapping of the interactome of protein phosphatase-1. Chem. Biol. 16, 365-371 (2009).
10. Ceulemans, H. & Bollen, M. Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 84, 1-39 (2004). (Pubitemid 38049874)
11. Bollen, M. Combinatorial control of protein phosphatase-1. Trends Biochem. Sci. 26, 426-431 (2001). (Pubitemid 32607484)
12. Egloff, M.P. et al. Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. EMBO J. 16, 1876-1887 (1997).
13. Dancheck, B., Nairn, A.C. & Peti, W. Detailed structural characterization of unbound protein phosphatase 1 inhibitors. Biochemistry 47, 12346-12356 (2008).
14. Hurley, T.D. et al. Structural basis for regulation of protein phosphatase 1 by inhibitor-2. J. Biol. Chem. 282, 28874-28883 (2007). (Pubitemid 47606030)
15. Terrak, M., Kerff, F., Langsetmo, K., Tao, T. & Dominguez, R. Structural basis of protein phosphatase 1 regulation. Nature 429, 780-784 (2004). (Pubitemid 38833131)
16. Allen, P.B., Ouimet, C.C. & Greengard, P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc. Natl. Acad. Sci. USA 94, 9956-9961 (1997). (Pubitemid 27408172)
17. Yan, Z. et al. Protein phosphatase 1 modulation of neostriatal AMPA channels: regulation by DARPP-32 and spinophilin. Nat. Neurosci. 2, 13-17 (1999). (Pubitemid 30488934)
18. Bielas, S.L. et al. Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell 129, 579-591 (2007).
19. Charlton, J.J. et al. Multiple actions of spinophilin regulate |i opioid receptor function. Neuron 58, 238-247 (2008).
20. Allen, P.B. et al. Distinct roles for spinophilin and neurabin in dopamine-mediated plasticity. Neuroscience 140, 897-911 (2006).
21. Brown, A.M., Baucum, A.J., Bass, M.A. & Colbran, R.J. Association of protein phosphatase 1 y 1 with spinophilin suppresses phosphatase activity in a Parkinson disease model. J. Biol. Chem. 283, 14286-14294 (2008).
22. Hsieh-Wilson, L.C., Allen, P.B., Watanabe, T., Nairn, A.C. & Greengard, P. Characterization of the neuronal targeting protein spinophilin and its interactions with protein phosphatase-1. Biochemistry 38, 4365-4373 (1999). (Pubitemid 129514703)
23. Dyson, H.J. & Wright, P.E. Intrinsically unstructured proteins and their functions. Nat Rev. Mol. Cell Biol. 6, 197-208 (2005). (Pubitemid 40314921)
24. Kita, A. et al. Crystal structure of the complex between calyculin A and the catalytic subunit of protein phosphatase 1. Structure 10, 715-724 (2002). (Pubitemid 34518712)
25. Fraczkiewicz, R. & Braun, W. Exact and effcient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19, 319-333 (1998). (Pubitemid 128592649)
26. Lo Conte, L, Chothia, C. & Janin, J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 2177-2198 (1999). (Pubitemid 29078179)
27. Dyson, H.J. & Wright, P.E. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 12, 54-60 (2002).
28. Tanaka, J. et al. Interaction of myosin phosphatase target subunit 1 with the catalytic subunit of type 1 protein phosphatase. Biochemistry 37, 16697-16703 (1998). (Pubitemid 28543930)
29. Hubbard, M.J. & Cohen, P. Regulation of protein phosphatase-1G from rabbit skeletal muscle. 2. Catalytic subunit translocation is a mechanism for reversible inhibition of activity toward glycogen-bound substrates. Eur. J. Biochem. 186, 711-716 (1989). (Pubitemid 20030126)
30. Zhang, J., Zhang, Z., Brew, K. & Lee, E.Y. Mutational analysis of the catalytic subunit of muscle protein phosphatase-1. Biochemistry 35, 6276-6282 (1996). (Pubitemid 26164057)
31. Ceulemans, H. et al. Binding of the concave surface of the Sds22 superhelix to the a 4/a 5/a 6-triangle of protein phosphatase-1. J. Biol. Chem. 277, 47331-47337 (2002). (Pubitemid 36159247)
32. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
33. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. & Read, R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 (2005).
34. Kelker, M.S. et al. Structural basis for spinophilin-neurabin receptor interaction. Biochemistry 46, 2333-2344 (2007). (Pubitemid 46362408)
35. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
36. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refnement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
37. Lamzin, V.S. & Wilson, K.S. Automated refnement of protein models. Acta Crystallogr. D Biol. Crystallogr. 49, 129-147 (1993).
38. Painter, J. & Merritt, E.A. TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111 (2006).
39. Davis, I.W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-83 (2007).
40. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).
41. Cohen, P. et al. Protein phosphatase-1 and protein phosphatase-2A from rabbit skeletal muscle. Methods Enzymol. 159, 390-408 (1988).
42. Jacques, A.M. et al. Myosin binding protein C phosphorylation in normal, hypertrophic and failing human heart muscle. J. Mol. Cell. Cardiol. 45, 209-216 (2008).