Induced structural disorder as a molecular mechanism for enzyme dysfunction in phosphoglucomutase 1 deficiency

Journal of Molecular Biology

Volumn 428, Issue 8, 2016, Pages 1493-1505

  Stiers, Kyle M ^a   Kain, Bailee N ^a   Graham, Abigail C ^a   Beamer, Lesa J ^a  

^a University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; PHOSPHOGLUCOMUTASE; ARGININE; PEPTIDE; PGM1 PROTEIN, HUMAN;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME DEFICIENCY; ENZYME STRUCTURE; KINETIC PARAMETERS; METAL BINDING; MISSENSE MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; CHEMICAL STRUCTURE; CHEMISTRY; CYTOPLASM; GENETICS; GLYCOGEN STORAGE DISEASE; HUMAN; METABOLISM; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

ARGININE; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; GLYCINE; GLYCOGEN STORAGE DISEASE; HUMANS; MODELS, MOLECULAR; MUTATION; MUTATION, MISSENSE; PEPTIDES; PHOSPHOGLUCOMUTASE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; X-RAY DIFFRACTION;

EID: 84962175594     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.02.032     Document Type: Article

References (50)

1. L.C. Tegtmeyer, S. Rust, M. van Scherpenzeel, B.G. Ng, M.-E. Losfeld, S. Timal, and et al. Multiple phenotypes in phosphoglucomutase 1 deficiency N. Engl. J. Med. 370 2014 533 542
2. B. Pérez, C. Medrano, M.J. Ecay, P. Ruiz-Sala, M. Martínez-Pardo, M. Ugarte, and et al. A novel congenital disorder of glycosylation type without central nervous system involvement caused by mutations in the phosphoglucomutase 1 gene J. Inherit. Metab. Dis. 36 2012 535 542
3. S. Timal, A. Hoischen, L. Lehle, M. Adamowicz, K. Huijben, J. Sykut-Cegielska, and et al. Gene identification in the congenital disorders of glycosylation type I by whole-exome sequencing Hum. Mol. Genet. 21 2012 4151 4161
4. A. Kucukcongar, L. Tumer, F. Suheyl Ezgu, C. Seher Ksapkara, J. Jaeken, G. Matthijs, and et al. A case with rare type of congential-disorder of glycosylation: PGM1-CDG Genet. Couns. 26 2015 87 90
5. N. Ondruskova, T. Honzik, A. Vondrackova, M. Tesarova, J. Zeman, and H. Hansikova Glycogen storage disease-like phenotype with central nervous system involvement in a PGM1-CDG patient Neuro Endocrinol. Lett. 35 2014 137 141
6. S. Wong, L.J. Beamer, T. Gadomski, T. Honzik, M. Mohamed, S.B. Wortmann, et al., Defining the phenotype and assessing severity in Phosphoglucomutase-1 deficiency, J. Pediatr. Biochem. (in press).
7. N. Loewenthal, A. Haim, R. Parvari, and E. Hershkovitz Phosphoglucomutase-1 deficiency: intrafamilial clinical variability and common secondary adrenal insufficiency Am. J. Med. Genet. Part A. 167 2015 3139 3143
8. E. Morava Galactose supplementation in phosphoglucomutase-1 deficiency; review and outlook for a novel treatable CDG Mol. Genet. Metab. 112 2014 275 279
9. G.S. Shackelford, C.A. Regni, and L.J. Beamer Evolutionary trace analysis of the alpha-d-phosphohexomutase superfamily Protein Sci. 13 2004 2130 2138
10. W.J. Ray, J.W. Burgner, and C.B. Post Characterization of vanadate-based transition-state-analogue complexes of phosphoglucomutase by spectral and NMR techniques Biochemistry 29 1990 2770 2778
11. Y. Lee, K.M. Stiers, B.N. Kain, and L.J. Beamer Compromised catalysis and potential folding defects in in vitro studies of missense mutants associated with hereditary phosphoglucomutase 1 deficiency J. Biol. Chem. 289 2014 32010 32019
12. Y. Liu, W.J. Ray, and S. Baranidharan Structure of rabbit muscle phosphoglucomutase refined at 2.4 Å resolution Acta Crystallogr. Sect. D 53 1997 392 405
13. J.-B. Dai, W.J. Ray, and M. Konno The crystal structure of muscle phosphoglucomutase refined at 2.7 Å resolution J. Biol. Chem. 267 1992 6322 6337
14. J. Dundas, Z. Ouyang, J. Tseng, A. Binkowski, Y. Turpaz, and J. Liang CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues Nucleic Acids Res. 34 2006 116 118
15. L.J. Beamer Mutations in hereditary phosphoglucomutase 1 deficiency map to key regions of enzyme structure and function J. Inherit. Metab. Dis. 38 2015 243 256
16. Y. Lee, R. Mehra-Chaudhary, C. Furdui, and L.J. Beamer Identification of an essential active-site residue in the alpha-d-phosphohexomutase enzyme superfamily FEBS J. 280 2013 2622 2632
17. R. Mehra-Chaudhary, J. Mick, J.J. Tanner, M.T. Henzl, and L.J. Beamer Crystal structure of a bacterial phosphoglucomutase, an enzyme involved in the virulence of multiple human pathogens Proteins 79 2011 1215 1229
18. C. Regni, L. Naught, P.A. Tipton, and L.J. Beamer Structural basis of diverse substrate recognition by the enzyme PMM/PGM from P. aeruginosa Structure 12 2004 55 63
19. A. Hawe, M. Sutter, and W. Jiskoot Extrinsic fluorescent dyes as tools for protein characterization Pharm. Res. 25 2008 1487 1499
20. R.A. Laskowski, and M.B. Swindells LigPlot +: multiple ligand-protein interaction diagrams for drug discovery J. Chem. Inf. Model. 51 2011 2778 2786
21. D.N. Cooper, P.D. Stenson, and N.A. Chuzhanova The Human Gene Mutation Database (HGMD) and its exploitation in the study of mutational mechanisms. Curr. Protoc. Bioinformatics 2006 Chapter 1. (Unit 1.13)
22. P. Yue, Z. Li, and J. Moult Loss of protein structure stability as a major causative factor in monogenic disease J. Mol. Biol. 353 2005 459 473 10.1016/j.jmb.2005.08.020
23. N. Tokuriki, and D.S. Tawfik Stability effects of mutations and protein evolvability Curr. Opin. Struct. Biol. 19 2009 596 604
24. S. Stefl, H. Nishi, M. Petukh, A.R. Panchenko, and E. Alexov Molecular mechanisms of disease-causing missense mutations J. Mol. Biol. 425 2013 3919 3936
25. M. Petukh, T.G. Kucukkal, and E. Alexov On human disease-causing amino acid variants: statistical study of sequence and structural patterns Hum. Mutat. 36 2015 524 534
26. T.A. Peterson, E. Doughty, and M.G. Kann Towards precision medicine: advances in computational approaches for the analysis of human variants J. Mol. Biol. 425 2013 4047 4063
27. J.-H. Han, S. Batey, A.A. Nickson, S.A. Teichmann, and J. Clarke The folding and evolution of multidomain proteins Nat. Rev. Mol. Cell Biol. 8 2007 319 330
28. A.M. Schramm, D. Karr, R. Mehra-Chaudhary, S.R. Van Doren, C.M. Furdui, and L.J. Beamer Breaking the covalent connection: chain connectivity and the catalytic reaction of PMM/PGM Protein Sci. 19 2010 1235 1242
29. Y. Wei, T.C. Marcink, J. Xu, A.G. Sirianni, A.V.S. Sarma, S.H. Prior, and et al. Chemical shift assignments of domain 4 from the phosphohexomutase from pseudomonas aeruginosa suggest that freeing perturbs its coevolved domain interface Biomol. NMR Assign. 8 2014 329 333
30. D. Ekman, A.K. Björklund, J. Frey-Skött, and A. Elofsson Multi-domain proteins in the three kingdoms of life: orphan domains and other unassigned regions J. Mol. Biol. 348 2005 231 243
31. A.L. Pey, F. Stricher, L. Serrano, and A. Martinez Predicted effects of missense mutations on native-state stability account for phenotypic outcome in phenylketonuria, a paradigm of misfolding diseases Am. J. Hum. Genet. 81 2007 1006 1024
32. U. Ohto, K. Usui, T. Ochi, K. Yuki, Y. Satow, and T. Shimizu Crystal structure of human β-galactosidase: structural basis of G M1 gangliosidosis and morquio B diseases J. Biol. Chem. 287 2012 1801 1812
33. K. Fulop, L. Barna, O. Symmons, P. Zavodsky, and A. Varadi Clustering of disease-causing mutations on the domain-domain interfaces of ABCC6 Biochem. Biophys. Res. Commun. 379 2009 706 709
34. M. Bozzi, A. Cassetta, S. Covaceuszach, M.G. Bigotti, S. Bannister, W. Hübner, and et al. The structure of the T190M mutant of murine α-dystroglycan at high resolution: insight into the molecular basis of a primary dystroglycanopathy PLoS ONE 10 2015 e0124277
35. M.S. Lee, R. Green, S.M. Marsillac, N. Coquelle, R.S. Williams, T. Yeung, and et al. Comprehensive analysis of missense variations in the BRCT domain of BRCA1 by structural and functional assays Cancer Res. 70 2010 4880 4890
36. E. Bjørgo, P.M. Knappskog, A. Martinez, R.C. Stevens, and T. Flatmark Partial characterization and three-dimensional-structural localization of eight mutations in exon 7 of the human phenylalanine hydroxylase gene associated with phenylketonuria Eur. J. Biochem. 257 1998 1 10
37. A.C. Muntau, J. Leandro, M. Staudigl, F. Mayer, and S.W. Gersting Innovative strategies to treat protein misfolding in inborn errors of metabolism: pharmacological chaperones and proteostasis regulators J. Inherit. Metab. Dis. 37 2014 505 523
38. B.M. Kroncke, C.G. Vanoye, J. Meiler, A.L. George, and C.R. Sanders Personalized biochemistry and biophysics Biochemistry 54 2015 2551 2559
39. E. Alexov Advances in human biology: combining genetics and molecular biophysics to pave the way for personalized diagnostics and medicine Adv. Biol. 2014 2014
40. W. Kabsch Software XDS for image rotation, recognition and crystal symmetry assignment Acta Crystallogr. Sect. D: Biol. Crystallogr. 66 2010 125 132
41. P.R. Evans, and G.N. Murshudov How good are my data and what is the resolution? Acta Crystallogr. Sect. D Biol. Crystallogr. 69 2013 1204 1214
42. E. Potterton, P. Briggs, M. Turkenburg, and E. Dodson A graphical user interface to the CCP 4 program suite Acta Crystallogr. Sect. D: Biol. Crystallogr. 59 2003 1131 1137
43. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
44. M.S. Weiss Global indicators of X-ray data quality J. Appl. Crystallogr. 34 2001 130 135
45. G.N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, and et al. REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. Sect. D: Biol. Crystallogr. 67 2011 355 367
46. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, and et al. PHENIX: A comprehensive python-based system for macromolecular structure solution Acta Crystallogr. Sect. D: Biol. Crystallogr. 66 2010 213 221
47. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D: Biol. Crystallogr. 60 2004 2126 2132
48. A. Vagin, and A. Teplyakov Molecular replacement with MOLREP Acta Crystallogr. Sect. D: Biol. Crystallogr. 66 2010 22 25
49. V.B. Chen, W.B. Arendall, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, and et al. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. Sect. D Biol. Crystallogr. 66 2010 12 21
50. W.L. DeLano The PyMOL Molecular Graphics System, Schrödinger LLC Wwwpymolorg. Version 1 2002