Crystal structures of protein phosphatase-1 bound to motuporin and dihydromicrocystin-LA: Elucidation of the mechanism of enzyme inhibition by cyanobacterial toxins

Journal of Molecular Biology

Volumn 356, Issue 1, 2006, Pages 111-120

  Maynes, Jason T ^a   Luu, Hue A ^a   Cherney, Maia M ^a   Andersen, Raymond J ^b   Williams, David ^b   Holmes, Charles F B ^a   James, Michael N G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Crystal structure; Cyanobacteria; Microcystin; Nodularin

Indexed keywords

BACTERIAL TOXIN; CYANOGINOSIN; CYTOTOXIN; MOTUPORIN; NODULARIN; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME INHIBITION; HOST CELL; MICHAEL ADDITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); CYANOBACTERIA;

EID: 30344447686     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.11.019     Document Type: Article

References (42)

1. W.W. Carmichael Toxins of cyanobacteria Sci. Am. 270 1994 78 86
2. S. Yoshizawa, R. Matsushima, M.F. Watanabe, K. Harada, A. Ichihara, W.W. Carmichael, and H. Fujiki Inhibition of protein phosphatases by microcystis and nodularin associated with hepatotoxicity J. Cancer Res. Clin. Oncol. 116 1990 609 614
3. R.E. Honkanen, J. Zwiller, R.E. Moore, S.L. Daily, B.S. Khatra, M. Dukelow, and A.L. Boynton Characterization of microcystin-LR, a potent inhibitor of type-1 and type-2a protein phosphatases J. Biol. Chem. 265 1990 19401 19404
4. C. MacKintosh, K.A. Beattie, S. Klumpp, P. Cohen, and G.A. Codd Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants FEBS Letters 264 1990 187 192
5. R. Nishiwaki-Matsushima, S. Nishiwaki, T. Ohta, S. Yoshizawa, M. Suganuma, and K. Harada Structure-function-relationships of microcystins, liver-tumor promoters, in interaction with protein phosphatase Jpn. J. Cancer Res. 82 1991 993 996
6. C.F.B. Holmes, and M.P. Boland Inhibitors of protein phosphatase-1 and phosphatase-2a. Two of the major serine threonine protein phosphatases involved in cellular regulation Curr. Opin. Struct. Biol. 3 1993 934 943
7. J.E. Eriksson, D. Toivola, J.A.O. Meriluoto, H. Karaki, Y.G. Han, and D. Hartshorne Hepatocyte deformation induced by cyanobacterial toxins reflects inhibition of protein phosphatases Biochem. Biophys. Res. Commun. 173 1990 1347 1353
8. T. Ohta, R. Nishiwaki, J. Yatsunami, A. Komori, M. Suganuma, and H. Fujiki Hyperphosphorylation of cytokeratins 8 and 18 by microcystin-LR, a new liver-tumor promoter, in primary cultured rat hepatocytes Carcinogenesis 13 1992 2443 2447
9. M. Craig, T.L. McCready, H.A. Luu, M.A. Smillie, P. Dubord, and C.F.B. Holmes Identification and characterization of hydrophobic microcystins in Canadian fresh-water cyanobacteria Toxicon 31 1993 1541 1549
10. K.L. Rinehart, K. Harada, M. Namikoshi, C. Chen, and C.A. Harvis Nodularin, microcystin, and the configuration of adda J. Am. Chem. Soc. 110 1988 8557 8558
11. T. Ohta, R. Nishiwaki, M. Suganuma, J. Yatsunami, A. Komori, and S. Okabe Significance of the cyanobacterial cyclic peptide toxins, the microcystins and nodularin, in liver-cancer Mutat. Res. 292 1993 286 287
12. E.D. Desilva, D.E. Williams, R.J. Andersen, H. Klix, C.F.B. Holmes, and T.M. Allen Motuporin, a potent protein phosphatase inhibitor isolated from the Papua-New-Guinea sponge Theonella swinhoei Gray Tetrahedron Letters 33 1992 1561 1564
13. J.R. Bagu, F.D. Sonnichsen, D. Williams, R.J. Andersen, B.D. Sykes, and C.F.B. Holmes Comparison of the solution structures of microcystin-LR and motuporin Nature Struct. Biol. 2 1995 114 116
14. A. Annila, J. Lehtimaki, K. Mattila, J.E. Eriksson, K. Sivonen, T.T. Rantala, and T. Drakenberg Solution structure of nodularin. An inhibitor of serine/threonine-specific protein phosphatases J. Biol. Chem. 271 1996 16695 16702
15. J. Goldberg, H.B. Huang, Y.G. Kwon, P. Greengard, A.C. Nairn, and J. Kuriyan Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1 Nature 376 1995 745 753
16. C.F.B. Holmes, J.T. Maynes, K.R. Perreault, J.F. Dawson, and M.N.G. James Molecular enzymology underlying regulation of protein phosphatase-1 by natural toxins Curr. Med. Chem. 9 2002 1981 1989
17. M. Craig, H.A. Luu, T.L. McCready, D. Williams, R.J. Andersen, and C.F.B. Holmes Molecular mechanisms underlying he interaction of motuporin and microcystins with type-1 and type-2A protein phosphatases Biochem. Cell Biol. 74 1996 569 578
18. R.W. MacKintosh, K.N. Dalby, D.G. Campbell, P.T. Cohen, P. Cohen, and C. MacKintosh The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase 1 FEBS Letters 371 1995 236 240
19. M. Runnegar, N. Berndt, S.M. Kong, E.Y.C. Lee, and L.F. Zhang In vivo and in vitro binding of microcystin to protein phosphatase-1 and phosphatase-2a Biochem. Biophys. Res. Commun. 216 1995 162 169
20. J.F. Dawson, and C.F.B. Holmes Molecular mechanisms underlying inhibition of protein phosphatases by marine toxins Front. Biosci. 4 1999 D646 D658
21. A. McCluskey, A.T.R. Sim, and J.A. Sakoff Serine-threonine protein phosphatase inhibitors: development of potential therapeutic strategies J. Med. Chem. 45 2002 1151 1175
22. M.P. Egloff, P.T. Cohen, P. Reinemer, and D. Barford Crystal structure of the catalytic subunit of human protein phosphatase 1 and its complex with tungstate J. Mol. Biol. 254 1995 942 959
23. D. Barford Molecular mechanisms of the protein serine threonine phosphatases Trends Biochem. Sci. 21 1996 407 412
24. A. Kita, S. Matsunaga, A. Takai, H. Kataiwa, T. Wakimoto, and N. Fusetani Crystal structure of the complex between calyculin A and the catalytic subunit of protein phosphatase 1 Structure 10 2002 715 724
25. J.T. Maynes, K.S. Bateman, M.M. Cherney, A.K. Das, H.A. Luu, C.F.B. Holmes, and M.N.G. James Crystal structure of the tumor-promoter okadaic acid bound to protein phosphatase-1 J. Biol. Chem. 276 2001 44078 44082
26. L. Zhang, Z. Zhang, F. Long, and E.Y. Lee Tyrosine-272 is involved in the inhibition of protein phosphatase-1 by multiple toxins Biochemistry 35 1996 1606 1611
27. H.B. Burgi, J.D. Dunitz, and E. Shefter Geometrical reaction coordinates. 2. Nucleophilic addition to a carbonyl group J. Am. Chem. Soc. 95 1973 5065 5067
28. C. Drahl, B.F. Cravatt, and E.J. Sorensen Protein-reactive natural products Angew Chem. Int. Ed. Engl. 44 2005 5788 5809
29. J.T. Maynes, K.R. Perreault, M.M. Cherney, H.A. Luu, M.N.G. James, and C.F.B. Holmes Crystal structure and mutagenesis of a protein phosphatase-1: calcineurin hybrid elucidate the role of the beta 12-beta 13 loop in inhibitor binding J. Biol. Chem. 279 2004 43198 43206
30. G. Moorhead, R.W. MacKintosh, N. Morrice, T. Gallagher, and C. MacKintosh Purification of type 1 protein (serine/threonine) phosphatases by microcystin-Sepharose affinity chromatography FEBS Letters 356 1994 46 50
31. F. Kondo, Y. Ikai, H. Oka, M. Okumura, N. Ishikawa, and K. Harada Formation, characterization, and toxicity of the glutathione and cysteine conjugates of toxic heptapeptide microcystins Chem. Res. Toxicol. 5 1992 591 596
32. D.E. Williams, M. Craig, S.C. Dawe, M.L. Kent, C.F.B. Holmes, and R.J. Andersen Evidence for a covalently bound form of microcystin-LR in salmon liver and dungeness crab larvae Chem. Res. Toxicol. 10 1997 1293
33. D.E. Williams, S.C. Dawe, M.L. Kent, R.J. Andersen, M. Craig, and C.F. Holmes Bioaccumulation and clearance of microcystins from salt water mussels, Mytilus edulis, and in vivo evidence for covalently bound microcystins in mussel tissues Toxicon 35 1997 1617 1625
34. W.J. Fischer, B.C. Hitzfeld, F. Tencalla, J.E. Eriksson, A. Mikhailov, and D.R. Dietrich Microcystin-LR toxicodynamics, induced pathology, and immunohistochemical localization in livers of blue-green algae exposed rainbow trout (oncorhynchus mykiss) Toxicol. Sci. 54 2000 365 373
35. C.J. Hastie, E.B. Borthwick, L.F. Morrison, G.A. Codd, and P.T. Cohen Inhibition of several protein phosphatases by a non-covalently interacting microcystin and a novel cyanobacterial peptide, nostocyclin Biochim. Biophys. Acta 18 2005 18
36. H.R. Powell The Rossmann Fourier autoindexing algorithm in MOSFLM Acta Crystallog. sect. D 55 1999 1690 1695
37. S. Bailey The CCP4 suite - programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
38. J. Navaza, and P. Saludjian AMoRe: an automated molecular replacement program package Macromolecular Crystallography, Part A vol. 276 1997 pp. 581-594
39. D.E. McRee XtalView Xfit - a versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 125 1999 156 165
40. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallog. sect. D 53 1997 240 255
41. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
42. R.W. Hooft, G. Vriend, C. Sander, and E.E. Abola Errors in protein structures Nature 381 1996 272