O-mannose and O-N-acetyl galactosamine glycosylation of mammalian α-dystroglycan is conserved in a region-specific manner

Glycobiology

Volumn 22, Issue 11, 2012, Pages 1413-1423

  Gomez Toledo, Alejandro ^a   Raducu, Madalina ^b   Cruces, Jesús ^b   Nilsson, Jonas ^a   Halim, Adnan ^a   Larson, Göran ^a   Rüetschi, Ulla ^a   Grahn, Ammi ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b AUTONOMOUS UNIVERSITY OF MADRID   (Spain)

Author keywords

dystroglycan; glycoproteomics; mammalian; mass spectrometry; O glycosylation

Indexed keywords

ALPHA DYSTROGLYCAN; GALACTOSAMINE; MANNOSE; MUCIN; O MANNOSE; O N ACETYL GALACTOSAMINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHEMICAL STRUCTURE; GLYCOSYLATION; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RABBIT; SKELETAL MUSCLE;

ACETYLGALACTOSAMINE; ANIMALS; DYSTROGLYCANS; GLYCOSYLATION; HUMANS; MANNOSE; MICE; MUSCLE, SKELETAL; PROTEIN STRUCTURE, TERTIARY; RABBITS; SPECIES SPECIFICITY;

MAMMALIA; ORYCTOLAGUS CUNICULUS;

EID: 84868028000     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws109     Document Type: Article

References (33)

1. Barresi R, Campbell KP. 2006. Dystroglycan: From biosynthesis to pathogenesis of human disease. J Cell Sci. 119:199-207.
2. Beltran-Valero de Bernabe D, Voit T, Longman C, Steinbrecher A, Straub V, Yuva Y, Herrmann R, Sperner J, Korenke C, Diesen C, et al. 2004. Mutations in the FKRP gene can cause muscle-eye-brain disease and Walker-Warburg syndrome. J Med Genet. 41:e61.
3. Breloy I, Schwientek T, Gries B, Razawi H, Macht M, Albers C, Hanisch FG. 2008. Initiation of mammalian O-mannosylation in vivo is independent of a consensus sequence and controlled by peptide regions within and upstream of the alpha-dystroglycan mucin domain. J Biol Chem. 283:18832-18840.
4. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, Benson MA, Ponting CP, Estournet B, Romero NB, Mercuri E, et al. 2001. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin alpha2 deficiency and abnormal glycosylation of alpha-dystroglycan. Am J Hum Genet. 69:1198-1209.
5. Chiba A, Matsumura K, Yamada H, Inazu T, Shimizu T, Kusunoki S, Kanazawa I, Kobata A, Endo T. 1997. Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve alpha-dystroglycan. The role of a novel O-mannosyl-type oligosaccharide in the binding of alphadystroglycan with laminin. J Biol Chem. 272:2156-2162.
6. Combs AC, Ervasti JM. 2005. Enhanced laminin binding by alphadystroglycan after enzymatic deglycosylation. Biochem J. 390:303-309.
7. Dincer P, Balci B, Yuva Y, Talim B, Brockington M, Dincel D, Torelli S, Brown S, Kale G, Haliloglu G, et al. 2003. A novel form of recessive limb girdle muscular dystrophy with mental retardation and abnormal expression of alpha-dystroglycan. Neuromuscul Disord. 13:771-778.
8. Endo T, Manya H. 2006. O-mannosylation in mammalian cells. Methods Mol Biol. 347:43-56.
9. Ervasti JM, Campbell KP. 1993. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol. 122:809-823.
10. Furukawa J, Shinohara Y, Kuramoto H, Miura Y, Shimaoka H, Kurogochi M, Nakano M, Nishimura S. 2008. Comprehensive approach to structural and functional glycomics based on chemoselective glycoblotting and sequential tag conversion. Anal Chem. 80:1094-1101.
11. Godfrey C, Clement E, Mein R, Brockington M, Smith J, Talim B, Straub V, Robb S, Quinlivan R, Feng L, et al. 2007. Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain. 130:2725-2735.
12. Hara Y, Balci-Hayta B, Yoshida-Moriguchi T, Kanagawa M, Beltran-Valero de Bernabe D, Gundesli H, Willer T, Satz JS, Crawford RW, Burden SJ, et al. 2011. A dystroglycan mutation associated with limb-girdle muscular dystrophy. N Engl J Med. 364:939-946.
13. Hara Y, Kanagawa M, Kunz S, Yoshida-Moriguchi T, Satz JS, Kobayashi YM, Zhu Z, Burden SJ, Oldstone MB, Campbell KP. 2011. Like- acetylglucosaminyltransferase (LARGE)-dependent modification of dystroglycan at Thr-317/319 is required for laminin binding and arenavirus infection. Proc Natl Acad Sci USA. 108:17426-17431.
14. Harrison R, Hitchen PG, Panico M, Morris HR, Mekheil D, Pleass RJ, Dell A, Hewitt JE, Haslam SM. 2012. Glycoproteomic characterisation of recombinant mouse alpha-dystroglycan. Glycobiology. 22:662-675.
15. Huddleston MJ, Bean MF, Carr SA. 1993. Collisional fragmentation of glycopeptides by electrospray ionization LC/MS and LC/MS/MS: Methods for selective detection of glycopeptides in protein digests. Anal Chem. 65:877-884.
16. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP. 1992. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 355: 696-702.
17. Ibraghimov-Beskrovnaya O, Milatovich A, Ozcelik T, Yang B, Koepnick K, Francke U, Campbell KP. 1993. Human dystroglycan: Skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet. 2:1651-1657.
18. Inamori K, Yoshida-Moriguchi T, Hara Y, Anderson ME, Yu L, Campbell KP. 2012. Dystroglycan function requires xylosyl-and glucuronyltransferase activities of LARGE. Science. 335:93-96.
19. Jimenez-Mallebrera C, Torelli S, Feng L, Kim J, Godfrey C, Clement E, Mein R, Abbs S, Brown SC, Campbell KP, et al. 2009. A comparative study of alpha-dystroglycan glycosylation in dystroglycanopathies suggests that the hypoglycosylation of alpha-dystroglycan does not consistently correlate with clinical severity. Brain Pathol. 19:596-611.
20. Kanagawa M, Saito F, Kunz S, Yoshida-Moriguchi T, Barresi R, Kobayashi YM, Muschler J, Dumanski JP, Michele DE, Oldstone MB, et al. 2004. Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell. 117:953-964.
21. Leschziner A, Moukhles H, Lindenbaum M, Gee SH, Butterworth J, Campbell KP, Carbonetto S. 2000. Neural regulation of alpha-dystroglycan biosynthesis and glycosylation in skeletal muscle. J Neurochem. 74:70-80.
22. Manya H, Suzuki T, Akasaka-Manya K, Ishida HK, Mizuno M, Suzuki Y, Inazu T, Dohmae N, Endo T. 2007. Regulation of mammalian protein O-mannosylation: Preferential amino acid sequence for O-mannose modification. J Biol Chem. 282:20200-20206.
23. Mercuri E, Brockington M, Straub V, Quijano-Roy S, Yuva Y, Herrmann R, Brown SC, Torelli S, Dubowitz V, Blake DJ, et al. 2003. Phenotypic spectrum associated with mutations in the fukutin-related protein gene. Ann Neurol. 53:537-542.
24. Mercuri E, D'Amico A, Tessa A, Berardinelli A, Pane M, Messina S, van Reeuwijk J, Bertini E, Muntoni F, Santorelli FM. 2006. POMT2 mutation in a patient with 'MEB-like' phenotype. Neuromuscul Disord. 16: 446-448.
25. Mercuri E, Topaloglu H, Brockington M, Berardinelli A, Pichiecchio A, Santorelli F, Rutherford M, Talim B, Ricci E, Voit T, et al. 2006. Spectrum of brain changes in patients with congenital muscular dystrophy and FKRP gene mutations. Arch Neurol. 63:251-257.
26. Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, Dollar J, Nishino I, Kelley RI, Somer H, et al. 2002. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature. 418:417-422.
27. Nilsson J, Nilsson J, Larson G, Grahn A. 2010. Characterization of sitespecific O-glycan structures within the mucin-like domain of alphadystroglycan from human skeletal muscle. Glycobiology. 20:1160-1169.
28. Poppe M, Cree L, Bourke J, Eagle M, Anderson LV, Birchall D, Brockington M, Buddles M, Busby M, Muntoni F, et al. 2003. The phenotype of limbgirdle muscular dystrophy type 2I. Neurology. 60:1246-1251.
29. Stalnaker SH, Hashmi S, Lim JM, Aoki K, Porterfield M, Gutierrez-Sanchez G, Wheeler J, Ervasti JM, Bergmann C, Tiemeyer M, et al. 2010. Site mapping and characterization of O-glycan structures on alpha-dystroglycan isolated from rabbit skeletal muscle. J Biol Chem. 285:24882-24891.
30. Tran DT, Lim JM, Liu M, Stalnaker SH, Wells L, Ten Hagen KG, Live D. 2012. Glycosylation of alpha-dystroglycan: O-mannosylation influences the subsequent addition of GalNAc by the UDP-GalNAc polypeptide N- acetylgalactosaminyltransferases. J Biol Chem. 287:20967-20974.
31. Wuhrer M, Deelder AM, van der Burgt YE. 2011. Mass spectrometric glycan rearrangements. Mass Spectrom Rev. 30:664-680.
32. Yamada H, Shimizu T, Tanaka T, Campbell KP, Matsumura K. 1994. Dystroglycan is a binding protein of laminin and merosin in peripheral nerve. FEBS Lett. 352:49-53.
33. Yoshida-Moriguchi T, Yu L, Stalnaker SH, Davis S, Kunz S, Madson M, Oldstone MB, Schachter H, Wells L, Campbell KP. 2010. O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science. 327:88-92.