Protein O-mannosylation in metazoan organisms

Current Protocols in Protein Science

Volumn 2014, Issue , 2014, Pages 12.12.1-12.12.29

  Panin, Vladislav M ^a   Wells, Lance ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Congenital muscular dystrophy; Drosophila; Dystroglycan; Mass spectrometry; O glycosylation; O mannose

Indexed keywords

ALPHA DYSTROGLYCAN; GLYCOPEPTIDE; MANNOSYLTRANSFERASE;

ARTICLE; DROSOPHILA; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME GLYCOSYLATION; ENZYME O MANNOSYLATION; ENZYME PURIFICATION; ENZYME RELEASE; ESCHERICHIA COLI; GENETIC ANALYSIS; GENETIC CONSERVATION; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; ION EXCHANGE CHROMATOGRAPHY; MASS SPECTROMETRY; MICROSOME; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; REGULATORY MECHANISM;

EID: 84949293407     PISSN: 19343655     EISSN: 19343663     Source Type: Journal    
DOI: 10.1002/0471140864.ps1212s75     Document Type: Article

References (78)

1. Abbott, K.L., Matthews, R.T., and Pierce, M. 2008. Receptor tyrosine phosphatase β (RPTPβ) activity and signaling are attenuated by glycosylation and subsequent cell surface galectin-1 binding. J. Biol. Chem. 283:33026-33035.
2. Akasaka-Manya, K., Manya, H., Nakajima, A., Kawakita, M., and Endo, T. 2006. Physical and functional association of human protein Omannosyltransferases 1 and 2. J. Biol. Chem. 281:19339-19345.
3. Anumula, K.R. and Taylor, P.B. 1992. A comprehensive procedure for preparation of partially methylated alditol acetates from glycoprotein carbohydrates. Anal. Biochem. 203:101-108.
4. Aoki, K., Porterfield, M., Lee, S.S., Dong, B., Nguyen, K., McGlamry, K.H., and Tiemeyer, M. 2008. The diversity of O-linked glycans expressed during Drosophila melanogaster development reflects stage-and tissue-specific requirements for cell signaling. J. Biol. Chem. 283:30385-30400.
5. Barone, R., Aiello, C., Race, V., Morava, E., Foulquier, F., Riemersma, M., Passarelli, C., Concolino, D., Carella, M., Santorelli, F., Vleugels, W., Mercuri, E., Garozzo, D., Sturiale, L., Messina, S., Jaeken, J., Fiumara, A., Wevers, R.A., Bertini, E., Matthijs, G., and Lefeber, D.J. 2012. DPM2-CDG: A muscular dystrophy-dystroglycanopathy syndrome with severe epilepsy. Ann. Neurol. 72: 550-558.
6. Barresi, R., Michele, D.E., Kanagawa, M., Harper, H.A., Dovico, S.A., Satz, J.S., Moore, S.A., Zhang, W., Schachter, H., Dumanski, J.P., Cohn, R.D., Nishino, I., and Campbell, K.P. 2004. LARGE can functionally bypass α-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat. Med. 10: 696-703.
7. Beedle, A.M., Turner, A.J., Saito, Y., Lueck, J.D., Foltz, S.J., Fortunato, M.J., Nienaber, P.M., and Campbell, K.P. 2012. Mouse fukutin deletion impairs dystroglycan processing and recapitulates muscular dystrophy. J. Clin. Invest. 122:3330-3342.
8. Beltran-Valero de Bernabe, D., Currier, S., Steinbrecher, A., Celli, J., van Beusekom, E., van der Zwaag, B., Kayserili, H., Merlini, L., Chitayat, D., Dobyns, W.B., Cormand, B., Lehesjoki, A.E., Cruces, J., Voit, T., Walsh, C.A., van Bokhoven, H., and Brunner, H.G. 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.
9. Bleckmann, C., Geyer, H., Lieberoth, A., Splittstoesser, F., Liu, Y., Feizi, T., Schachner, M., Kleene, R., Reinhold, V., and Geyer, R. 2009. O-Glycosylation pattern of CD24 from mouse brain. Biol. Chem. 390:627-645.
10. Brand, A.H., Manoukian, A.S., and Perrimon, N. 1994. Ectopic expression in Drosophila. Methods Cell Biol. 44:635-654.
11. Breloy, I., Schwientek, T., Gries, B., Razawi, H., Macht, M., Albers, C., and Hanisch, F.G. 2008. Initiation of mammalian O-mannosylation in vivo is independent of a consensus sequence and controlled by peptide regions within and upstream of the α-dystroglycan mucin domain. J. Biol. Chem. 283:18832-18840.
12. Brockington, M., Blake, D.J., Prandini, P., Brown, S.C., Torelli, S., Benson, M.A., Ponting, C.P., Estournet, B., Romero, N.B., Mercuri, E., Voit, T., Sewry, C.A., Guicheney, P., and Muntoni, F. 2001a. Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin α2 deficiency and abnormal glycosylation of α-dystroglycan. Am. J. Hum. Genet. 69:1198-1209.
13. Brockington, M., Yuva, Y., Prandini, P., Brown, S.C., Torelli, S., Benson, M.A., Herrmann, R., Anderson, L.V., Bashir, R., Burgunder, J.M., Fallet, S., Romero, N., Fardeau, M., Straub, V., Storey, G., Pollitt, C., Richard, I., Sewry, C.A., Bushby, K., Voit, T., Blake, D.J., and Muntoni, F. 2001b. Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophyMDC1C. Hum. Mol. Genet. 10:2851-2859.
14. Brockington, M., Torelli, S., Prandini, P., Boito, C., Dolatshad, N.F., Longman, C., Brown, S.C., and Muntoni, F. 2005. Localization and functional analysis of the LARGE family of glycosyltransferases: Significance for muscular dystrophy. Hum. Mol. Genet. 14:657-665.
15. Buysse, K., Riemersma, M., Powell, G., van Reeuwijk, J., Chitayat, D., Roscioli, T., Kamsteeg, E.J., van den Elzen, C., van Beusekom, E., Blaser, S., Babul-Hirji, R., Halliday, W., Wright, G.J., Stemple, D.L., Lin, Y.Y., Lefeber, D.J., and van Bokhoven, H. 2013. Missense mutations in β-1, 3-N-acetylglucosaminyltransferase 1 (B3GNT1) cause Walker-Warburg syndrome. Hum. Mol. Genet. 22:1746-1754.
16. Chiba, A., Matsumura, K., Yamada, H., Inazu, T., Shimizu, T., Kusunoki, S., Kanazawa, I., Kobata, A., and Endo, T. 1997. Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve α-dystroglycan. The role of a novel O-mannosyl-type oligosaccharide in the binding of α-dystroglycan with laminin. J. Biol. Chem. 272:2156-2162.
17. de Bernabe, D.B., Inamori, K., Yoshida-Moriguchi, T., Weydert, C.J., Harper, H.A., Willer, T., Henry, M.D., and Campbell, K.P. 2009. Loss of α-dystroglycan laminin binding in epitheliumderived cancers is caused by silencing of LARGE. J. Biol. Chem. 284:11279-11284.
18. Dobzhansky, T. 1946. Genetics of Natural Populations. Xiii. Recombination and variability in populations of Drosophila pseudoobscura. Genetics 31:269-290.
19. Endo, T. and Manya, H. 2006. O-Mannosylation in mammalian cells. Methods Mol. Biol. 347:43-56.
20. Finne, J., Krusius, T., Margolis, R.K., and Margolis, R.U. 1979. Novel mannitol-containing oligosaccharides obtained by mild alkaline borohydride treatment of a chondroitin sulfate proteoglycan from brain. J. Biol. Chem. 254:10295-10300.
21. Fujimura, K., Sawaki, H., Sakai, T., Hiruma, T., Nakanishi, N., Sato, T., Ohkura, T., and Narimatsu, H. 2005. LARGE2 facilitates the maturation of α-dystroglycan more effectively than LARGE. Biochem. Biophys. Res. Commun. 329:1162-1171.
22. Greis, K.D., Hayes, B.K., Comer, F.I., Kirk, M., Barnes, S., Lowary, T.L., and Hart, G.W. 1996. Selective detection and site-analysis of O-GlcNAc-modified glycopeptides by β-elimination and tandem electrospray mass spectrometry. Anal. Biochem. 234:38-49.
23. Grewal, P.K., McLaughlan, J.M., Moore, C.J., Browning, C.A., and Hewitt, J.E. 2005. Characterization of the LARGE family of putative glycosyltransferases associated with dystroglycanopathies. Glycobiology 15:912-923.
24. Haines, N., Seabrooke, S., and Stewart, B.A. 2007. Dystroglycan and protein Omannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles. Mol. Biol. Cell 18:4721-4730.
25. Harrison, R., Hitchen, P.G., Panico, M., Morris, H.R., Mekhaiel, D., Pleass, R.J., Dell, A., Hewitt, J.E., and Haslam, S.M. 2012. Glycoproteomic characterization of recombinant mouse α-dystroglycan. Glycobiology 22:662-675.
26. Haslam, S.M., North, S.J., and Dell, A. 2006. Mass spectrometric analysis of N-and Oglycosylation of tissues and cells. Curr. Opin. Struct. Biol. 16:584-591.
27. Hutzler, J., Schmid, M., Bernard, T., Henrissat, B., and Strahl, S. 2007. Membrane association is a determinant for substrate recognition by PMT4 protein O-mannosyltransferases. Proc. Natl. Acad. Sci. U.S.A. 104:7827-7832.
28. Ichimiya, T., Manya, H., Ohmae, Y., Yoshida, H., Takahashi, K., Ueda, R., Endo, T., and Nishihara, S. 2004. The twisted abdomen phenotype of Drosophila POMT1 and POMT2 mutants coincides with their heterophilic protein O-mannosyltransferase activity. J. Biol. Chem. 279:42638-42647.
29. Inamori, K., Yoshida-Moriguchi, T., Hara, Y., Anderson, M.E., Yu, L., and Campbell, K.P. 2012. Dystroglycan function requires xylosyland glucuronyltransferase activities of LARGE. Science 335:93-96.
30. Inamori, K.I., Hara, Y., Willer, T., Anderson, M.E., Zhu, Z., Yoshida-Moriguchi, T., and Campbell, K.P. 2013. Xylosyl-and glucuronyltransferase functions of LARGE in α-dystroglycan modification are conserved in LARGE2. Glycobiology 23:295-302.
31. Jae, L.T., Raaben, M., Riemersma, M., van Beusekom, E., Blomen, V.A., Velds, A., Kerkhoven, R.M., Carette, J.E., Topaloglu, H., Meinecke, P., Wessels, M.W., Lefeber, D.J., Whelan, S.P., van Bokhoven, H., and Brummelkamp, T.R. 2013. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Science 340:479-483.
32. Jang-Lee, J., Curwen, R.S., Ashton, P.D., Tissot, B., Mathieson, W., Panico, M., Dell, A., Wilson, R.A., and Haslam, S.M. 2007. Glycomics analysis of Schistosoma mansoni egg and cercarial secretions. Mol. Cell. Proteom. 6:1485-1499.
33. Jiang, X., Han, G., Feng, S., Jiang, X., Ye, M., Yao, X., and Zou, H. 2008. Automatic validation of phosphopeptide identifications by theMS2/MS3 target-decoy search strategy. J. Proteome Res. 7:1640-1649.
34. Jiao, J., Zhang, H., and Reinhold, V.N. 2011. High performance IT-MS sequencing of glycans (spatial resolution of ovalbumin isomers). Int. J. Mass Spectrom. 303:109-117.
35. Julenius, K., Molgaard, A., Gupta, R., and Brunak, S. 2005. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15:153-164.
36. Kobata, A. 1979. Use of endo-and exoglycosidases for structural studies of glycoconjugates. Anal. Biochem. 100:1-14.
37. Kobayashi, K., Nakahori, Y., Miyake, M., Matsumura, K., Kondo-Iida, E., Nomura, Y., Segawa, M., Yoshioka, M., Saito, K., Osawa, M., Hamano, K., Sakakihara, Y., Nonaka, I., Nakagome, Y., Kanazawa, I., Nakamura, Y., Tokunaga, K., and Toda, T. 1998. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 394:388-392.
38. Krusius, T., Finne, J., Margolis, R.K., and Margolis, R.U. 1986. Identification of an O-glycosidic mannose-linked sialylated tetrasaccharide and keratan sulfate oligosaccharides in the chondroitin sulfate proteoglycan of brain. J. Biol. Chem. 261:8237-8242.
39. Kunz, S., Rojek, J.M., Kanagawa, M., Spiropoulou, C.F., Barresi, R., Campbell, K.P., and Oldstone, M.B. 2005. Posttranslational modification of α-dystroglycan, the cellular receptor for arenaviruses, by the glycosyltransferase LARGE is critical for virus binding. J. Virol. 79:14282-14296.
40. Lefeber, D.J., Schonberger, J., Morava, E., Guillard, M., Huyben, K.M., Verrijp, K., Grafakou, O., Evangeliou, A., Preijers, F.W., Manta, P., Yildiz, J., Grunewald, S., Spilioti, M., vandenElzen, C., Klein, D., Hess, D., Ashida, H., Hofsteenge, J., Maeda, Y., van den Heuvel, L., Lammens, M., Lehle, L., and Wevers, R.A. 2009. Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. Am. J. Hum. Genet. 85:76-86.
41. Lommel, M. and Strahl, S. 2009. Protein Omannosylation: Conserved from bacteria to humans. Glycobiology 19:816-828.
42. Longman, C., Brockington, M., Torelli, S., Jimenez-Mallebrera, C., Kennedy, C., Khalil, N., Feng, L., Saran, R.K., Voit, T., Merlini, L., Sewry, C.A., Brown, S.C., and Muntoni, F. 2003. Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of α-dystroglycan. Hum. Mol. Genet. 12:2853-2861.
43. Lyalin, D., Koles, K., Roosendaal, S.D., Repnikova, E., Van Wechel, L., and Panin, V.M. 2006. The twisted gene encodes Drosophila protein O-mannosyltransferase 2 and genetically interacts with the rotated abdomen gene encoding Drosophila protein O-mannosyltransferase 1. Genetics 172:343-353.
44. Manya, H., Chiba, A., Yoshida, A., Wang, X., Chiba, Y., Jigami, Y., Margolis, R.U., and Endo, T. 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.
45. Manya, H., Suzuki, T., Akasaka-Manya, K., Ishida, H.K., Mizuno, M., Suzuki, Y., Inazu, T., Dohmae, N., and Endo, T. 2007. Regulation of mammalian proteinO-mannosylation: Preferential amino acid sequence for O-mannose modification. J. Biol. Chem. 282:20200-20206.
46. Manya, H., Bouchet, C., Yanagisawa, A., Vuillaumier-Barrot, S., Quijano-Roy, S., Suzuki, Y., Maugenre, S., Richard, P., Inazu, T., Merlini, L., Romero, N.B., Leturcq, F., Bezier, I., Topaloglu, H., Estournet, B., Seta, N., Endo, T., and Guicheney, P. 2008. Protein Omannosyltransferase activities in lymphoblasts from patients with α-dystroglycanopathies. Neuromuscul. Disord. 18:45-51.
47. Manya, H., Akasaka-Manya, K., Nakajima, A., Kawakita, M., and Endo, T. 2010. Role of Nglycans in maintaining the activity of protein O-mannosyltransferases POMT1 and POMT2. J. Biochem. 147:337-344.
48. Manzini, M.C., Tambunan, D.E., Hill, R.S., Yu, T.W., Maynard, T.M., Heinzen, E.L., Shianna, K.V., Stevens, C.R., Partlow, J.N., Barry, B.J., Rodriguez, J., Gupta, V.A., Al-Qudah, A.K., Eyaid, W.M., Friedman, J.M., Salih, M.A., Clark, R., Moroni, I., Mora, M., Beggs, A.H., Gabriel, S.B., and Walsh, C.A. 2012. Exome sequencing and functional validation in zebrafish identifyGTDC2 mutations as a cause of Walker-Warburg syndrome. Am. J. Hum. Genet. 91:541-547.
49. Martinez, T., Pace, D., Brady, L., Gerhart, M., and Balland, A. 2007. Characterization of a novel modification on IgG2 light chain. Evidence for the presence of O-linked mannosylation. J. Chromatogr. A 1156:183-187.
50. Mikesh, L.M., Ueberheide, B., Chi, A., Coon, J.J., Syka, J.E., Shabanowitz, J., and Hunt, D.F. 2006. The utility of ETD mass spectrometry in proteomic analysis. Biochim. Biophys. Acta 1764:1811-1822.
51. Muntoni, F., Torelli, S., Wells, D.J., and Brown, S.C. 2011. Muscular dystrophies due to glycosylation defects: Diagnosis and therapeutic strategies. Curr. Opin. Neurol. 24:437-442.
52. Nakamura, N., Lyalin, D., and Panin, V.M. 2010a. Protein O-mannosylation in animal development and physiology: From human disorders to Drosophila phenotypes. Semin. Cell Dev. Biol. 21:622-630.
53. Nakamura, N., Stalnaker, S.H., Lyalin, D., Lavrova, O., Wells, L., and Panin, V.M. 2010b. Drosophila dystroglycan is a target of Omannosyltransferase activity of two protein O-mannosyltransferases, rotated abdomen and twisted. Glycobiology 20:381-394.
54. OMIM. 2012. Online Mendelian Inheritance in Man. McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD), URL: http://omim.org/.
55. Pacharra, S., Hanisch, F.G., and Breloy, I. 2012. Neurofascin 186 is O-mannosylated within and outside of the mucin domain. J. Proteome Res. 11:3955-3964.
56. Rademaker, G.J., Pergantis, S.A., Blok-Tip, L., Langridge, J.I., Kleen, A., and Thomas-Oates, J.E. 1998. Mass spectrometric determination of the sites of O-glycan attachment with low picomolar sensitivity. Anal. Biochem. 257: 149-160.
57. Roberts, D.B. 1998. Drosophila: A Practical Approach, 2nd ed. Oxford University Press, New York.
58. Sharma, R.C. and Schimke, R.T. 1996. Preparation of electro-competent E. coli using salt-free growth medium. BioTechniques 20:42-44.
59. Shcherbata, H.R., Yatsenko, A.S., Patterson, L., Sood, V.D., Nudel, U., Yaffe, D., Baker, D., and Ruohola-Baker, H. 2007. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J. 26:481-493.
60. Spradling, A.C. and Rubin, G.M. 1982. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341-347.
61. Stalnaker, S.H., Hashmi, S., Lim, J.M., Aoki, K., Porterfield, M., Gutierrez-Sanchez, G., Wheeler, J., Ervasti, J.M., Bergmann, C., Tiemeyer, M., and Wells, L. 2010. Site mapping and characterization of O-glycan structures on α-dystroglycan isolated from rabbit skeletal muscle. J. Biol. Chem. 285:24882-24891.
62. Stalnaker, S.H., Aoki, K., Lim, J.M., Porterfield, M., Liu, M., Satz, J.S., Buskirk, S., Xiong, Y., Zhang, P., Campbell, K.P., Hu, H., Live, D., Tiemeyer, M., and Wells, L. 2011a. Glycomic analyses of mouse models of congenital muscular dystrophy. J. Biol. Chem. 286:21180-21190.
63. Stalnaker, S.H., Stuart, R., and Wells, L. 2011b. Mammalian O-mannosylation: Unsolved questions of structure/function. Curr. Opin. Struct. Biol. 21:603-609.
64. Tran, D.T., Lim, J.M., Liu, M., Stalnaker, S.H., Wells, L., Ten Hagen, K.G., and Live, D. 2012. Glycosylation of α-dystroglycan: OMannosylation influences the subsequent addition of GalNAc by UDP-GalNAc polypeptide N-acetylgalactosaminyltransferases. J. Biol. Chem. 287:20967-20974.
65. van Reeuwijk, J., Janssen, M., van den Elzen, C., Beltran-Valero de Bernabe, D., Sabatelli, P., Merlini, L., Boon, M., Scheffer, H., Brockington, M., Muntoni, F., Huynen, M.A., Verrips, A., Walsh, C.A., Barth, P.G., Brunner, H.G., and van Bokhoven, H. 2005. POMT2 mutations cause α-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J. Med. Genet. 42:907-912.
66. Vester-Christensen, M.B., Halim, A., Joshi, H.J., Steentoft, C., Bennett, E.P., Levery, S.B., Vakrushev, S.Y., and Clausen, H. 2013. Mining the O-mannose glycoproteome reveals cadherins as major O-mannosylated glycoproteins. Proc. Natl. Acad. Sci. U.S.A. 110:21018-20123.
67. Vosseller, K., Hansen, K.C., Chalkley, R.J., Trinidad, J.C., Wells, L., Hart, G.W., and Burlingame, A.L. 2005. Quantitative analysis of both protein expression and serine/threonine post-translational modifications through stable isotope labeling with dithiothreitol. Proteomics 5:388-398.
68. Wada, Y., Dell, A., Haslam, S.M., Tissot, B., Canis, K., Azadi, P., Backstrom, M., Costello, C.E., Hansson, G.C., Hiki, Y., Ishihara, M., Ito, H., Kakehi, K., Karlsson, N., Hayes, C.E., Kato, K., Kawasaki, N., Khoo, K.H., Kobayashi, K., Kolarich, D., Kondo, A., Lebrilla, C., Nakano, M., Narimatsu, H., Novak, J., Novotny, M.V., Ohno, E., Packer, N.H., Palaima, E., Renfrow, M.B., Tajiri, M., Thomsson, K.A., Yagi, H., Yu, S.Y., and Taniguchi, N. 2010. Comparison of methods for profiling O-glycosylation: Human Proteome Organisation Human Disease Glycomics/Proteome Initiative multi-institutional study of IgA1. Mol. Cell. Proteom. 9:719-727.
69. Wairkar, Y.P., Fradkin, L.G., Noordermeer, J.N., and DiAntonio, A. 2008. Synaptic defects in a Drosophila model of congenital muscular dystrophy. J. Neurosci. 28:3781-3789.
70. Wells, L., Vosseller, K., Cole, R.N., Cronshaw, J.M., Matunis, M.J., and Hart, G.W. 2002. Mapping sites of O-GlcNAc modification using affinity tags for serine and threonine post-translational modifications. Mol. Cell. Proteom. 1:791-804.
71. Willer, T., Lee, H., Lommel, M., Yoshida-Moriguchi, T., de Bernabe, D.B., Venzke, D., Cirak, S., Schachter, H., Vajsar, J., Voit, T., Muntoni, F., Loder, A.S., Dobyns, W.B., Winder, T.L., Strahl, S., Mathews, K.D., Nelson, S.F., Moore, S.A., and Campbell, K.P. 2012. ISPD loss-of-function mutations disrupt dystroglycan O-mannosylation and cause Walker-Warburg syndrome. Nat. Genet. 44:575-580.
72. Wing, D.R., Rademacher, T.W., Schmitz, B., Schachner, M., and Dwek, R.A. 1992. Comparative glycosylation in neural adhesion molecules. Biochem. Soc. Trans. 20:386-390.
73. Winterhalter, P.R., Lommel, M., Ruppert, T., and Strahl, S. 2013. O-Glycosylation of the noncanonical T-cahderin from rabbit skeletal muscle by single mannose residues. FEBS Lett. 587:3715-3721.
74. Yoshida, A., Kobayashi, K., Manya, H., Taniguchi, K., Kano, H., Mizuno, M., Inazu, T., Mitsuhashi, H., Takahashi, S., Takeuchi, M., Herrmann, R., Straub, V., Talim, B., Voit, T., Topaloglu, H., Toda, T., and Endo, T. 2001. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev. Cell 1:717-724.
75. Yoshida-Moriguchi, T., Yu, L., Stalnaker, S.H., Davis, S., Kunz, S., Madson, M., Oldstone, M.B., Schachter, H., Wells, L., and Campbell, K.P. 2010. O-Mannosyl phosphorylation of α-dystroglycan is required for laminin binding. Science 327:88-92.
76. Yoshida-Morguchi, T., Willer, T., Anderson, M.E., Venzke, D., Whyte, T., Muntoni, F., Lee, H., Nelson, S.F., Yu, L., and Campbell, K.P. 2013. SGK196 is a glycosylation-specific O-mannose kinase required for dystroglycan function. Science 341:896-899.
77. Yuen, C.T., Chai, W., Loveless, R.W., Lawson, A.M., Margolis, R.U., and Feizi, T. 1997. Brain contains HNK-1 immunoreactive O-glycans of the sulfoglucuronyl lactosamine series that terminate in 2-linked or 2, 6-linked hexose (mannose). J. Biol. Chem. 272:8924-8931.
78. Zhao, P., Viner, R., Teo, C.F., Boons, G.J., Horn, D., and Wells, L. 2011. Combining high-energy C-trap dissociation and electron transfer dissociation for protein O-GlcNAc modification site assignment. J. Proteome Res. 10:4088-4104.