Human ISPD Is a Cytidyltransferase Required for Dystroglycan O-Mannosylation

Chemistry and Biology

Volumn 22, Issue 12, 2015, Pages 1643-1652

  Riemersma, Moniek ^a,b   Froese, D Sean ^c   Van Tol, Walinka ^a,b   Engelke, Udo F ^b   Kopec, Jolanta ^c   Van Scherpenzeel, Monique ^a,b   Ashikov, Angel ^a,b   Krojer, Tobias ^c   Von Delft, Frank ^c   Tessari, Marco ^d   Buczkowska, Anna ^e   Swiezewska, Ewa ^e   Jae, Lucas T ^f   Brummelkamp, Thijn R ^f   Manya, Hiroshi ^g   Endo, Tamao ^g   Van Bokhoven, Hans ^a   Yue, Wyatt W ^c   Lefeber, Dirk J ^a,b  

^a RADBOUD UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^e INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^f NETHERLANDS CANCER INSTITUTE   (Netherlands)

^g Tokyo Metropolitan Institute of Gerontology   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROGLYCAN; ISOPRENOID SYNTHASE; O MANNOSE GLYCAN; PENTOSE PHOSPHATE; RIBITOL 5 PHOSPHATE; RIBOSE 5 PHOSPHATE; RIBULOSE PHOSPHATE; SYNTHETASE; UNCLASSIFIED DRUG; CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; ISPD PROTEIN, HUMAN; NUCLEOTIDYLTRANSFERASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME MECHANISM; HETERONUCLEAR SINGLE QUANTUM COHERENCE; LIQUID CHROMATOGRAPHY; MISSENSE MUTATION; MUSCULAR DYSTROPHY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; TIME OF FLIGHT MASS SPECTROMETRY; CHEMISTRY; FIBROBLAST; GENE INACTIVATION; GENETICS; GLYCOSYLATION; HUMAN; METABOLISM; X RAY CRYSTALLOGRAPHY;

CELLS, CULTURED; CHOLINE-PHOSPHATE CYTIDYLYLTRANSFERASE; CRYSTALLOGRAPHY, X-RAY; DYSTROGLYCANS; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; GLYCOSYLATION; HUMANS; NUCLEOTIDYLTRANSFERASES;

EID: 84951569890     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.10.014     Document Type: Article

References (45)

1. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, and et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. R. Barone, C. Aiello, V. Race, E. Morava, F. Foulquier, M. Riemersma, C. Passarelli, D. Concolino, M. Carella, F. Santorelli, and et al. DPM2-CDG: a muscular dystrophy-dystroglycanopathy syndrome with severe epilepsy Ann. Neurol. 72 2012 550 558
3. S. Baur, J. Marles-Wright, S. Buckenmaier, R.J. Lewis, and W. Vollmer Synthesis of CDP-activated ribitol for teichoic acid precursors in Streptococcus pneumoniae J. Bacteriol. 191 2009 1200 1210
4. C. Bernal, C. Palacin, A. Boronat, and S. Imperial A colorimetric assay for the determination of 4-diphosphocytidyl-2-C-methyl-D-erythritol 4-phosphate synthase activity Anal. Biochem. 337 2005 55 61
5. V. Cantagrel, D.J. Lefeber, B.G. Ng, Z. Guan, J.L. Silhavy, S.L. Bielas, L. Lehle, H. Hombauer, M. Adamowicz, E. Swiezewska, and et al. SRD5A3 is required for converting polyprenol to dolichol and is mutated in a congenital glycosylation disorder Cell 142 2010 203 217
6. J.E. Carette, M. Raaben, A.C. Wong, A.S. Herbert, G. Obernosterer, N. Mulherkar, A.I. Kuehne, P.J. Kranzusch, A.M. Griffin, G. Ruthel, and et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1 Nature 477 2011 340 343
7. K.J. Carss, E. Stevens, A.R. Foley, S. Cirak, M. Riemersma, S. Torelli, A. Hoischen, T. Willer, M. van Scherpenzeel, S.A. Moore, and et al. Mutations in GDP-mannose pyrophosphorylase B cause congenital and limb-girdle muscular dystrophies associated with hypoglycosylation of alpha-dystroglycan Am. J. Hum. Genet. 93 2013 29 41
8. S.W. Coates, T. Gurney Jr., L.W. Sommers, M. Yeh, and C.B. Hirschberg Subcellular localization of sugar nucleotide synthetases J. Biol. Chem. 255 1980 9225 9229
9. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
10. A.C. Combs, and J.M. Ervasti Enhanced laminin binding by alpha-dystroglycan after enzymatic deglycosylation Biochem. J. 390 2005 303 309
11. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
12. J.M. Ervasti, and K.P. Campbell A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin J. Cell Biol 122 1993 809 823
13. A. Follens, M. Veiga-da-Cunha, R. Merckx, E. van Schaftingen, and J. van Eldere acs1 of Haemophilus influenzae type a capsulation locus region II encodes a bifunctional ribulose 5-phosphate reductase- CDP-ribitol pyrophosphorylase J. Bacteriol. 181 1999 2001 2007
14. T. Geis, K. Marquard, T. Rodl, C. Reihle, S. Schirmer, T. von Kalle, A. Bornemann, U. Hehr, and M. Blankenburg Homozygous dystroglycan mutation associated with a novel muscle-eye-brain disease-like phenotype with multicystic leucodystrophy Neurogenetics 14 2013 205 213
15. Y. Hara, B. Balci-Hayta, T. Yoshida-Moriguchi, M. Kanagawa, D. Beltran-Valero de Bernabe, H. Gundesli, T. Willer, J.S. Satz, R.W. Crawford, S.J. Burden, and et al. A dystroglycan mutation associated with limb-girdle muscular dystrophy N. Engl. J. Med. 364 2011 939 946
16. P. Holden, and W.A. Horton Crude subcellular fractionation of cultured mammalian cell lines BMC Res. Notes 2 2009 243
17. K. Inamori, T. Yoshida-Moriguchi, Y. Hara, M.E. Anderson, L. Yu, and K.P. Campbell Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE Science 335 2012 93 96
18. L.T. Jae, M. Raaben, M. Riemersma, E. van Beusekom, V.A. Blomen, A. Velds, R.M. Kerkhoven, J.E. Carette, H. Topaloglu, P. Meinecke, and et al. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry Science 340 2013 479 483
19. E.P. Kennedy, and S.B. Weiss The function of cytidine coenzymes in the biosynthesis of phospholipides J. Biol. Chem. 222 1956 193 214
20. D.J. Lefeber, J. Schonberger, E. Morava, M. Guillard, K.M. Huyben, K. Verrijp, O. Grafakou, A. Evangeliou, F.W. Preijers, P. Manta, and et al. Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies Am. J. Hum. Genet. 85 2009 76 86
21. D.J. Lefeber, A.P. de Brouwer, E. Morava, M. Riemersma, J.H. Schuurs-Hoeijmakers, B. Absmanner, K. Verrijp, W.M. van den Akker, K. Huijben, G. Steenbergen, and et al. Autosomal recessive dilated cardiomyopathy due to DOLK mutations results from abnormal dystroglycan O-mannosylation PLoS Genet. 7 2011 e1002427
22. M. Lommel, S. Cirak, T. Willer, R. Hermann, G. Uyanik, H. van Bokhoven, C. Körner, T. Voit, I. Barić, U. Hehr, and et al. Correlation of enzyme activity and clinical phenotype in POMT1-associated dystroglycanopathies Neurology 74 2010 157 164
23. J. Liu, and A. Mushegian Three monophyletic superfamilies account for the majority of the known glycosyltransferases Protein Sci. 12 2003 1418 1431
24. H. Manya, A. Chiba, A. Yoshida, X. Wang, Y. Chiba, Y. Jigami, R.U. Margolis, and T. Endo Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 required for enzymatic activity Proc. Natl. Acad. Sci. USA 101 2004 500 505
25. P.T. Martin The dystroglycanopathies: the new disorders of O-linked glycosylation Semin. Pediatr. Neurol. 12 2005 152 158
26. D.E. Michele, R. Barresi, M. Kanagawa, F. Saito, R.D. Cohn, J.S. Satz, J. Dollar, I. Nishino, R.I. Kelley, H. Somer, and et al. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies Nature 418 2002 417 422
27. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
28. M.P. Pereira, and E.D. Brown Bifunctional catalysis by CDP-ribitol synthase: convergent recruitment of reductase and cytidylyltransferase activities in Haemophilus influenzae and Staphylococcus aureus Biochemistry 43 2004 11802 11812
29. S.B. Richard, M.E. Bowman, W. Kwiatkowski, I. Kang, C. Chow, A.M. Lillo, D.E. Cane, and J.P. Noel Structure of 4-diphosphocytidyl-2-C- methylerythritol synthetase involved in mevalonate- independent isoprenoid biosynthesis Nat. Struct. Biol. 8 2001 641 648
30. S.B. Richard, A.M. Lillo, C.N. Tetzlaff, M.E. Bowman, J.P. Noel, and D.E. Cane Kinetic analysis of Escherichia coli 2-C-methyl-D-erythritol-4-phosphate cytidyltransferase, wild type and mutants, reveals roles of active site amino acids Biochemistry 43 2004 12189 12197
31. M. Riemersma, J. Sandrock, T.J. Boltje, C. Bull, T. Heise, A. Ashikov, G.J. Adema, H. van Bokhoven, and D.J. Lefeber Disease mutations in CMP-sialic acid transporter SLC35A1 result in abnormal alpha-dystroglycan O-mannosylation, independent from sialic acid Hum. Mol. Genet. 24 2015 2241 2246
32. T. Roscioli, E.J. Kamsteeg, K. Buysse, I. Maystadt, J. van Reeuwijk, C. van den Elzen, E. van Beusekom, M. Riemersma, R. Pfundt, L.E. Vissers, and et al. Mutations in ISPD cause Walker-Warburg syndrome and defective glycosylation of alpha-dystroglycan Nat. Genet. 44 2012 581 585
33. N.E. Sanjana, L. Cong, Y. Zhou, M.M. Cunniff, G. Feng, and F. Zhang A transcription activator-like effector toolbox for genome engineering Nat. Protoc. 7 2012 171 192
34. S. Sugita, F. Saito, J. Tang, J. Satz, K. Campbell, and T.C. Sudhof A stoichiometric complex of neurexins and dystroglycan in brain J. Cell Biol 154 2001 435 445
35. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etzler Essentials of Glycobiology 2009 Cold Spring Harbor Laboratory Press
36. Q. Wang, Y. Xu, A.V. Perepelov, Y.A. Knirel, P.R. Reeves, A.S. Shashkov, P. Ding, X. Guo, and L. Feng Characterization of the CDP-D-mannitol biosynthetic pathway in Streptococcus pneumoniae 35A Glycobiology 22 2012 1760 1767
37. Q. Wang, Y. Xu, A.V. Perepelov, Y.A. Knirel, P.R. Reeves, A.S. Shashkov, X. Guo, P. Ding, and L. Feng Biochemical characterization of the CDP-D-arabinitol biosynthetic pathway in Streptococcus pneumoniae 17F J. Bacteriol. 194 2012 1868 1874
38. L. Wells The O-mannosylation pathway: glycosyltransferases and proteins implicated in congenital muscular dystrophy J. Biol. Chem. 288 2013 6930 6935
39. T. Willer, H. Lee, M. Lommel, T. Yoshida-Moriguchi, D.B. de Bernabe, D. Venzke, S. Cirak, H. Schachter, J. Vajsar, T. Voit, and et al. ISPD loss-of-function mutations disrupt dystroglycan O-mannosylation and cause Walker-Warburg syndrome Nat. Genet. 44 2012 575 580
40. M.C. Witschel, H.W. Hoffken, M. Seet, L. Parra, T. Mietzner, F. Thater, R. Niggeweg, F. Rohl, B. Illarionov, F. Rohdich, and et al. Inhibitors of the herbicidal target IspD: allosteric site binding Angew. Chem. Int. Ed. Engl. 50 2011 7931 7935
41. K.M. Wright, K.A. Lyon, H. Leung, D.J. Leahy, L. Ma, and D.D. Ginty Dystroglycan organizes axon guidance cue localization and axonal pathfinding Neuron 76 2012 931 944
42. A.C. Yang, B.G. Ng, S.A. Moore, J. Rush, C.J. Waechter, K.M. Raymond, T. Willer, K.P. Campbell, H.H. Freeze, and L. Mehta Congenital disorder of glycosylation due to DPM1 mutations presenting with dystroglycanopathy-type congenital muscular dystrophy Mol. Genet. Metab. 110 2013 345 351
43. A. Yoshida, K. Kobayashi, H. Manya, K. Taniguchi, H. Kano, M. Mizuno, T. Inazu, H. Mitsuhashi, S. Takahashi, M. Takeuchi, and et al. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1 Dev. Cell 1 2001 717 724
44. T. Yoshida-Moriguchi, L. Yu, S.H. Stalnaker, S. Davis, S. Kunz, M. Madson, M.B. Oldstone, H. Schachter, L. Wells, and K.P. Campbell O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding Science 327 2010 88 92
45. M. Zolli, D.J. Kobric, and E.D. Brown Reduction precedes cytidylyl transfer without substrate channeling in distinct active sites of the bifunctional CDP-ribitol synthase from Haemophilus influenzae Biochemistry 40 2001 5041 5048