Dystroglycan glycosylation and muscular dystrophy

Glycoconjugate Journal

Volumn 26, Issue 3, 2009, Pages 349-357

  Moore, Christopher J ^a   Hewitt, Jane E ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Dystroglycan; Glycosylation; Glycosyltransferase; Muscle; Muscular dystrophy

Indexed keywords

ALPHA DYSTROGLYCAN; GENE PRODUCT; GLYCOSYLTRANSFERASE; PROTEIN LARGE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CONFERENCE PAPER; ENZYME ACTIVITY; GENE; GENE IDENTIFICATION; GENE MUTATION; GLYCOSYLATION; HUMAN; LARGE GENE; MUSCULAR DYSTROPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; DYSTROGLYCANS; EVOLUTION, MOLECULAR; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; MUSCULAR DYSTROPHIES; N-ACETYLGLUCOSAMINYLTRANSFERASES;

EID: 62449178402     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-008-9182-0     Document Type: Conference Paper

References (82)

1. D.J. Blake A. Weir S.E. Newey K.E. Davies 2002 Function and genetics of dystrophin and dystrophin-related proteins in muscle Physiol. Rev. 82 291 329
2. R.A. Williamson M.D. Henry K.J. Daniels R.F. Hrstka C.J. Lee Y. Sunada 1997 Dystroglycan is essential for early embryonic development: disruption of Reichart's membrane in Dag1-null mice Hum. Mol. Genet. 6 831 841
3. P.D. Côté H. Moukhles M. Lindebaum S. Carbonetto 1999 Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses Nat. Genet. 23 338 342
4. O. Ibraghimov-Beskrovnaya J.M. Ervasti C.J. Leveille C.A. Slaughter S.W. Sernett K.P. Campbell 1992 Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix Nature. 355 696 702
5. S.J. Winder 2001 The complexities of dystroglycan Trends Biochem. Sci. 26 118 124
6. J.M. Ervasti K.P. Campbell 1993 A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin J. Cell Biol. 122 809 823
7. J. Campanelli S. Roberds K. Campbell R. Scheller 1994 A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AchR clustering Cell. 77 663 674
8. S. Sugita F. Saito J. Tang J. Satz K. Campbell T.C. Südhof 2001 A stoichiometric complex of neurexins and dystroglycan in brain J. Cell Biol. 154 435 445
9. F. Muntoni M. Brockington S. Torelli S.C. Brown 2004 Defective glycosylation in congenital muscular dystrophies Curr. Opin. Neurol. 17 205 209
10. P.K. Grewal J.E. Hewitt 2002 Mutation of Large, which encodes a putative glycosyltransferase, in an animal model of muscular dystrophy Biochim. Biophys. Acta. 1573 216 224
11. M. Brockington S. Torelli P. Prandini C. Boito N.F. Dolatshad C. Longman 2005 Localization and functional analysis of the LARGE family of glycosyltransferases: significance for muscular dystrophy Hum. Mol. Genet. 15 657 665
12. K. Fujimura H. Sawaki T. Sakai T. Hiruma N. Nakanishi T. Sato 2005 LARGE2 facilitates the maturation of alpha-dystroglycan more effectively than LARGE Biochem. Biophys. Res. Commun. 329 1162 1171
13. P.K. Grewal J.M. McLaughlan C.J. Moore C.A. Browning J.E. Hewitt 2005 Characterisation of the LARGE family of putative glycosyltransferases associated with dystroglycanopathies Glycobiology. 15 912 923
14. myd mouse defines a natural model for glycosylation-deficient muscle-eye-brain disorders Hum. Mol. Genet. 11 2673 2687
15. D.E. Michele R. Barresi M. Kanagawa F. Saito R.D. Cohn J.S. Satz 2002 Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies Nature. 418 417 422
16. M. Kanagawa D.E. Michele J.S. Satz R. Barresi H. Kusano T. Sasaki 2005 Disruption of perlecan binding and matrix assembly by post-translational or genetic disruption of dystroglycan function FEBS Lett. 579 4792 4796
17. S.A. Moore F. Saito J. Chen D.E. Michele M.D. Henry A. Messing 2002 Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy Nature. 418 422 425
18. R.D. Cohn 2005 Dystroglycan: important player in skeletal muscle and beyond Neuromusc. Dis. 15 207 217
19. A. Sgambato A. Brancaccio 2005 The dystroglycan complex: From biology to cancer J. Cell. Physiol. 205 163 169
20. W.B. Dobyns R.A. Pagon D. Armstrong C.J. Curry F. Greenberg A. Grix 1989 Diagnostic criteria for Walker-Warburg syndrome Am. J. Med. Genet. 32 195 210
21. J. van Reeuwijk H.G. Brunner H. van Bokhoven 2005 Glyc-O-genetics of Walker-Warburg syndrome Clin. Genet. 67 281 289
22. D. Beltrán-Valero de Bernabé S. Currier A. Steinbrecher J. Celli E. van Beusekom B. van der Zwaag 2002 Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome Am. J. Hum. Genet. 71 1033 1043
23. J. van Reeuwijk M. Janssen C. van den Elzen D. Beltran-Valero de Bernabe P. Sabatelli L. Merlini 2005 POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker Warburg syndrome J. Med. Genet. 42 907 912
24. D. Beltrán-Valero de Bernabé H. van Bokhovan E. van Beusekom W. Van den Akker S. Kant W.B. Dobyns 2003 A homozygous nonsense mutation in the Fukutin gene causes a Walker-Warburg Syndrome phenotype J. Med. Genet. 40 845 848
25. D. Beltrán-Valero de Bernabé T. Voit C. Longman A. Steinbrecher V. Straub Y. Yuva 2004 Mutations in the FKRP gene can cause muscle-eye-brain disease and Walker-Warburg syndrome J. Med. Genet. 41 e61
26. J. van Reeuwijk P.K. Grewal M.A.M. Salih D.B.V. de Bernabe J.M. McLaughlan C.B. Michielse 2007 Intragenic deletion in the LARGE gene causes Walker-Warburg syndrome Hum. Genet. 121 685 690
27. P. Santavuori H. Somer K. Sainio J. Rapola S. Kruus T. Nikitin 1989 Muscle-eye-brain disease (MEB) Brain Dev. 11 147 153
28. A. Yoshida K. Kobayashi H. Manya K. Taniguchi H. Kano M. Mizuno 2001 Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1 Dev. Cell. 1 717 724
29. E. Mercuri A. D'Amico A. Tessa A. Berardinelli M. Pane S. Messina 2006 POMT2 mutations in a patient with 'MEB-like' phenotype Neuromusc. Dis. 16 446 448
30. T. Toda K. Kobayashi E. Kondo-Iida J. Sasaki Y. Nakamura 2000 The Fukuyama congenital muscular dystrophy story Neuromusc. Dis. 10 153 159
31. K. Kobayashi Y. Nakahori M. Miyake K. Matsumura E. Kondo-Iida Y. Nomura 1998 An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy Nature 394 388 392
32. L. Aravind E.V. Koonin 1999 The fukutin protein family-Predicted enzymes modifying cell-surface molecules Curr. Biol. 9 R836 R837
33. C. Godfrey E. Clement R. Mein M. Brockington J. Smith B. Talim 2007 Refining genotype-phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan Brain 130 2725 2735
34. R.P. Cotarelo M.C. Valero B. Prados A. Pena L. Rodriguez O. Fano 2008 Two new patients bearing mutations in the fukutin gene confirm the relevance of this gene in Walker-Warburg syndrome Clin. Genet. 73 139 145
35. M. Brockington D.J. Blake P. Prandini S.C. Brown S. Torelli M.A. Benson 2001 Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin alpha 2 deficiency and abnormal glycosylation of alpha-dystroglycan Am. J. Hum. Genet. 69 1198 1209
36. M. Brockington Y. Yuva P. Prandini S.C. Brown S. Torelli M.A. Benson 2001 Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophy MDC1C Hum. Mol. Genet. 10 2851 2859
37. S.C. Brown S. Torelli Y. Yuva C. Jimenez L. Feng L. Anderson 2004 Abnormalities in alpha-dystroglycan expression in MDC1C and LGMD21 muscular dystrophies Am. J. Pathol. 164 727 737
38. E. Mercuri M. Brockington V. Straub S. Quijano-Roy Y. Yuva R. Herrmann 2003 Phenotypic spectrum associated with mutations in the fukutin-related protein gene Ann. Neurol. 53 537 542
39. Y.K. Hayashi M. Ogawa K. Tagawa S. Noguchi T. Ishihara I. Nonaka 2001 Selective deficiency of α-dystroglycan in Fukuyama-type congenital muscular dystrophy Neurology. 57 115 121
40. H. Kano K. Kobayashi R. Herrmann M. Tachikawa H. Manya I. Nishino 2002 Deficiency of α-dystroglycan in muscle-eye-brain disease Biochem. Biophys. Res. Commun. 291 1283 1286
41. P.K. Grewal P.J. Holzfeind R.E. Bittner J.E. Hewitt 2001 Mutant glycosyltransferase and altered glycosylation of α-dystroglycan in the myodystrophy mouse Nat. Genet. 28 151 154
42. E.M. Clement C. Godfrey J. Tan M. Brockington S. Torelli L. Feng 2008 Mild POMGnT1 mutations underlie a novel limb-girdle muscular dystrophy variant Arch. Neurol. 65 137 141
43. Jimenez-Mallebrera, C., Torelli, S., Feng, L., Kim, J., Godfrey, C., Clement, E., et al. A comparative study of α-dystroglycan glycosylation in dystroglycanopathies suggests that hypoglycosyation of α-dystroglycan does not consistently correlate with clinical severity. Brain Pathol. (2008) (in press). doi: 10.1111/j.1750-3639.2008.00198.x
44. P.T. Martin 2003 Dystroglycan glycosylation and its role in matrix binding in skeletal muscle Glycobiology 13 55R 66R
45. C.T. Esapa G.R.B. Bentham J.E. Schroder S. Kroger D.J. Blake 2003 The effects of post-translational processing on dystroglycan synthesis and trafficking FEBS Lett. 555 209 216
46. K. Matsumura A. Chiba H. Yamada H. Fukuta-Ohi S. Fujita T. Endo 1997 A role of dystroglycan in Schwannoma cell adhesion to laminin J. Biol. Chem. 272 13904 13910
47. J.M. Ervasti K.P. Campbell 1991 Membrane organization of the dystrophin-glycoprotein complex Cell 66 1121 1131
48. A. Brancaccio T. Schulthess M. Gesemann J. Engel 1995 Electron microscopic evidence for a mucin-like region in chick muscle α-dystroglycan FEBS Lett. 368 139 142
49. M.D. Henry K.P. Campbell 1999 Dystroglycan inside and out Curr. Opin. Cell Biol. 11 602 607
50. J.M. Ervasti K.P. Campbell 1993 A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin J. Cell Biol. 122 809 823
51. S.C. Brown A. Fassati L. Popplewell A.M. Page M.D. Henry K.P. Campbell 1999 Dystrophic phenotype induced by antibody blockade of muscle α-dystroglycan-laminin interaction J. Cell Sci. 112 209 216
52. A.K. Chiba H. Matsumura T. Yamada T. Inazu S. Shimizu I. Kusunoki 1997 Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve a-dystroglycan. The role of a novel O-mannosyl-type oligosaccharide in binding of α-dystroglycan with laminin J. Biol. Chem. 272 2156 2162
53. J.M. Ervasti A.L. Burwell A.L. Geissler 1997 Tissue-specific heterogeneity in α-dystroglycan sialoglycosylation. Skeletal muscle α-dystroglycan is a latent receptor for Vicia villosa agglutinin b4 masked by sialic acid modification J. Biol. Chem. 272 22315 22321
54. A.C. Combs J.M. Ervasti 2005 Enhanced laminin binding by α-dystrogycan after enzymatic deglycosylation Biochem. J. 390 303 309
55. T. Sasaki H. Yamada K. Matsumura T. Shimizu A. Kobata T. Endo 1998 Detection of O-mannosyl glycans in rabbit skeletal muscle α-dystroglycan Biochim. Biophys. Acta. 1425 599 606
56. N.R. Smalheiser S.M. Haslam M. Sutton-Smith H.R. Morris A. Dell 1998 Structural analysis of sequences O-linked to mannose reveals a novel Lewis X structure in cranin (dystroglycan) purified from sheep brain J. Biol. Chem. 273 23698 23703
57. H. Manya A. Chiba A. Yoshida X. Wang Y. Chiba Y. Jigami 2004 Demonstration of mammalian protein O-mannosyltransferase activity: Coexpression of POMT1 and POMT2 required for enzymatic activity Proc. Natl. Acad. Sci. U. S. A. 101 500 505
58. W.L. Zhang C. Betel H. Schachter 2002 Cloning and expression of a novel UDP-GlcNAc:alpha-d-mannoside beta 1,2-N-acetylglucosaminyltransferase homologous to UDP-GlcNAc:alpha-3-d-mannoside beta 1,2-N-acetylglucosaminyltransferase I Biochem. J. 361 153 162
59. H. Xiong K. Kobayashi M. Tachikawa H. Manya S. Takeda T. Chiyonobu 2006 Molecular interaction between fukutin and POMGnT1 in the glycosylation pathway of α-dystroglycan Biochem. Biophys. Res. Commun. 350 935 941
60. C. Longman M. Brockington S. Torelli C. Jimenez-Mallebrera C. Kennedy N. Khalil 2003 Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan Hum. Mol. Genet. 12 2853 2861
61. M. Peyrard E. Seroussi A.C. Sandberg-Nordqvist Y.G. Xie F.Y. Han I. Fransson 1999 The human LARGE gene from 22q12,3-q13.1 is a new, distinct member of the glycosyltransferase gene family Proc. Natl. Acad. Sci. U. S. A. 96 598 603
62. P.M. Coutinho E. Deleury G.J. Davies B. Henrissat 2003 An evolving hierarchical family classification for glycosyltransferases J. Mol. Biol. 328 307 317
63. K. Sasaki K. Kurata-Miura M. Ujita K. Angata S. Nakagawa S. Sekine 1997 Expression cloning of cDNA encoding a human β-1,3-N- acetylglucosaminyltransferase that is essential for poly-N-acetyllactosamine synthesis Proc. Natl. Acad. Sci. U. S. A. 94 14294 14299
64. C.R. Wiggins S. Munro 1998 Activity of the yeast MNN1 α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases Proc. Natl. Acad. Sci. U. S. A. 95 7945 7950
65. R. Barresi D.E. Michele M. Kanagawa H.A. Harper S.A. Dovico J.S. Satz 2004 LARGE can functionally bypass α-dystroglycan glycosylation defect in distinct congenital muscular dystrophy Nat. Med. 10 696 703
66. S.K. Patnaik P. Stanley 2005 Mouse Large can modify complex N- and mucin O-glycans on α-dystroglycan to induce laminin binding J. Biol. Chem. 280 20851 20859
67. C.G. Giraudo H.J.F. Maccioni 2003 Endoplasmic reticulum export of glycosyltransferases depends on interaction of a cytoplasmic dibasic motif with sar1 Mol. Biol. Cell. 14 3753 3766
68. Sutton-Smith, M., Morris, H.R., Grewal, P.K., Hewitt, J.E., Bittner, R.E., Goldin, E., et al: (2002) MS screening strategies: investigating the glycomes of knockout and myodystrophic mice and leukodystrophic human brains. Glycogenomics: The impact of Genomics and Informatics on Glycobiology, pp. 105-115
69. K. Jabbari E. Rayko G. Bernardi 2003 The major shifts of human duplicated genes Gene. 317 203 208
70. E. Rayko K. Jabbari G. Bernardi 2006 The evolution of introns in human duplicated genes; the major shifts in human duplicated genes Gene. 365 41 47
71. Y. Lee S. Kameya G.A. Cox J. Hsu W. Hicks T.R. Maddatu 2005 Ocular abnormalities in Large(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases Mol. Cell. Neurosci. 30 160 172
72. N. Haines S. Seabrooke B.A. Stewart 2007 Dystroglycan and protein O-mannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles Mol. Biol. Cell. 18 4721 4730
73. M. Schneider A.A. Khalil M. Poulton C. Castillejo-Lopez D. Egger-Adam A. Wodarz 2006 Perlecan and dystroglycan act as the basal side of the Drosophila follicular epithelium to maintain epithelial organisation Development. 133 3805 3815
74. P. Thornhill D. Bassett H. Lochmüller K. Bushby V. Straub 2008 Developmental defects in a zebrafish model for muscular dystrophies associated with the loss of fukutin-related protein (FKRP) Brain. 131 1551 1561
75. C.J. Moore H.T. Goh J.E. Hewitt 2008 Genes required for functional glycosylation of dystroglycan are conserved in zebrafish Genomics 92 159 167
76. T.L. Pang C.J. Wu P.A. Chen Y.L. Weng M.Y. Chen 2007 Dictyostelium gnt15 encodes a protein with similarity to LARGE and plays an essential role in development Biochem. Biophys. Res. Commun. 360 83 89
77. C. Borchiellini M. Manuel E. Alivon N. Boury-Esnault J. Vacelet Y. Le Parco 2001 Sponge paraphyly and the origin of Metazoa J. Evol. Biol. 14 171 179
78. J. van Reeuwijk S. Maugenre C. van den Elzen A. Verrips E. Bertini F. Muntoni 2006 The expanding phenotype of POMT1 mutations: From Walker-Warburg syndrome to congenital muscular dystrophy, microcephaly, and mental retardation Hum. Mutat. 27 453 459
79. B. Balci G. Uyanik P. Dincer C. Gross T. Willer B. Talim 2005 An autosomal recessive limb girdle muscular dystrophy (LGMD2) with mild mental retardation is allelic to Walker-Warburg syndrome (WWS) caused by a mutation in the POMT1 gene Neuromuscul. Dis. 15 271 275
80. R. Biancheri A. Falace A. Tessa M. Pedernonte S. Scapolan D. Cassandrini 2007 POMT2 gene mutation in limb-girdle muscular dystrophy with inflammatory changes Biochem. Biophys. Res. Commun. 363 1033 1037
81. C. Godfrey D. Escolar M. Brockington E.M. Clement R. Mein C. Jimenez-Mallebrera 2006 Fukutin gene mutations in steroid-responsive limb girdle muscular dystrophy Ann. Neurol. 60 603 610
82. H. Topaloglu M. Brockington Y. Yuva B. Talim G. Haliloglu D. Blake 2003 FKRP gene mutations cause congenital muscular dystrophy, mental retardation, and cerebellar cysts Neurol. (Tokyo). 60 988 992