Large induces functional glycans in an O-mannosylation dependent manner and targets glcnac terminals on alpha-dystroglycan

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Hu, Yihong ^a   Li, Zhi fang ^a   Wu, Xiaohua ^a   Lu, Qilong ^a  

^a CAROLINAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DYSTROGLYCAN; COMPLEMENTARY DNA; DOLICHOL PHOSPHATE MANNOSE BIOSYNTHESIS REGULATORY PROTEIN 2; GALACTOSYLTRANSFERASE; GLYCAN; LARGE PROTEIN; N ACETYLGLUCOSAMINE; REGULATOR PROTEIN; SIALIC ACID; UNCLASSIFIED DRUG; DYSTROGLYCAN; LARGE PROTEIN, MOUSE; MANNOSE; MANNOSYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE; NITROGEN; POLYSACCHARIDE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHO CELL; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; LIGAND BINDING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STABLE EXPRESSION; ANIMAL; CHEMISTRY; CRICETULUS; GENETICS; GLYCOSYLATION; HAMSTER; HUMAN; METABOLISM; MOUSE; MUTATION; PROTEIN BINDING;

CRICETULUS GRISEUS;

ACETYLGLUCOSAMINE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DYSTROGLYCANS; GLYCOSYLATION; HUMANS; MANNOSE; MANNOSYLTRANSFERASES; MICE; MUTATION; N-ACETYLGLUCOSAMINYLTRANSFERASES; NITROGEN; POLYSACCHARIDES; PROTEIN BINDING;

EID: 79951782427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016866     Document Type: Article

References (35)

1. Smalheiser NR, Schwartz NB, (1987) Cranin: a laminin-binding protein of cell membranes. Proc Natl Acad Sci U S A 84: 6457-6461.
2. Campbell KP, Kahl SD, (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338: 259-262.
3. Gorecki DC, Derry JM, Barnard EA, (1994) Dystroglycan: brain localisation and chromosome mapping in the mouse. Hum Mol Genet 3: 1589-1597.
4. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP, (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345: 315-319.
5. Kobayashi K, Nakahori Y, Miyake M, Matsumura K, Kondo-Iida E, et al. (1998) An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 394: 388-392.
6. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, et al. (2001) Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 1: 717-724.
7. Beltran-Valero de Bernabe D, Currier S, Steinbrecher A, Celli J, van Beusekom E, et al. (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.
8. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, 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.
9. van Reeuwijk J, Janssen M, van den Elzen C, Beltran-Valero de Bernabe D, Sabatelli P, et al. (2005) POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J Med Genet 42: 907-912.
10. Longman C, Brockington M, Torelli S, Jimenez-Mallebrera C, Kennedy C, et al. (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.
11. Manya H, Chiba A, Yoshida A, Wang X, Chiba Y, et al. (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.
12. Peyrard M, Seroussi E, Sandberg-Nordqvist AC, Xie YG, Han FY, et al. (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.
13. Grewal PK, McLaughlan JM, Moore CJ, Browning CA, Hewitt JE, (2005) Characterization of the LARGE family of putative glycosyltransferases associated with dystroglycanopathies. Glycobiology 15: 912-923.
14. Sgambato A, Migaldi M, Montanari M, Camerini A, Brancaccio A, et al. (2003) Dystroglycan expression is frequently reduced in human breast and colon cancers and is associated with tumor progression. Am J Pathol 162: 849-860.
15. Sgambato A, Camerini A, Faraglia B, Pavoni E, Montanari M, et al. (2004) Increased expression of dystroglycan inhibits the growth and tumorigenicity of human mammary epithelial cells. Cancer Biol Ther 3: 967-975.
16. Yamamoto T, Kato Y, Shibata N, Sawada T, Osawa M, et al. (2008) A role of fukutin, a gene responsible for Fukuyama type congenital muscular dystrophy, in cancer cells: a possible role to suppress cell proliferation. Int J Exp Pathol 89: 332-341.
17. Beltran-Valero de Bernabe D, Inamori KI, Yoshida-Moriguchi T, Weydert CJ, Harper HA, et al. (2009) Loss of alpha-dystroglycan laminin binding in epithelium-derived cancers is caused by silencing of large. J Biol Chem.
18. Barresi R, Michele DE, Kanagawa M, Harper HA, Dovico SA, et al. (2004) LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat Med 10: 696-703.
19. Patnaik SK, Stanley P, (2005) Mouse large can modify complex N- and mucin O-glycans on alpha-dystroglycan to induce laminin binding. J Biol Chem 280: 20851-20859.
20. Rojek JM, Spiropoulou CF, Campbell KP, Kunz S, (2007) Old World and clade C New World arenaviruses mimic the molecular mechanism of receptor recognition used by alpha-dystroglycan's host-derived ligands. J Virol 81: 5685-5695.
21. Aguilan JT, Sundaram S, Nieves E, Stanley P, (2009) Mutational and Functional Analysis of Large in a Novel CHO Glycosylation Mutant. Glycobiology.
22. Bao X, Kobayashi M, Hatakeyama S, Angata K, Gullberg D, et al. (2009) Tumor suppressor function of laminin-binding alpha-dystroglycan requires a distinct beta3-N-acetylglucosaminyltransferase. Proc Natl Acad Sci U S A 106: 12109-12114.
23. Patnaik SK, Stanley P, (2006) Lectin-resistant CHO glycosylation mutants. Methods Enzymol 416: 159-182.
24. 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.
25. Krieger M, Reddy P, Kozarsky K, Kingsley D, Hobbie L, et al. (1989) Analysis of the synthesis, intracellular sorting, and function of glycoproteins using a mammalian cell mutant with reversible glycosylation defects. Methods Cell Biol 32: 57-84.
26. Yoshida-Moriguchi T, Yu L, Stalnaker SH, Davis S, Kunz S,et al. O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 327: 88-92.
27. Stalnaker SH, Hashmi S, Lim JM, Aoki K, Porterfield 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.
28. Chiba A, Matsumura K, Yamada H, Inazu T, Shimizu T, et al. (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 alpha-dystroglycan with laminin. J Biol Chem 272: 2156-2162.
29. Sasaki T, Yamada H, Matsumura K, Shimizu T, Kobata A, et al. (1998) Detection of O-mannosyl glycans in rabbit skeletal muscle alpha-dystroglycan. Biochim Biophys Acta 1425: 599-606.
30. Smalheiser NR, Haslam SM, Sutton-Smith M, Morris HR, Dell A, (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.
31. Smalheiser NR, Kim E, (1995) Purification of cranin, a laminin binding membrane protein. Identity with dystroglycan and reassessment of its carbohydrate moieties. J Biol Chem 270: 15425-15433.
32. McDearmon EL, Combs AC, Sekiguchi K, Fujiwara H, Ervasti JM, (2006) Brain alpha-dystroglycan displays unique glycoepitopes and preferential binding to laminin-10/11. FEBS Lett 580: 3381-3385.
33. McDearmon EL, Combs AC, Ervasti JM, (2003) Core 1 glycans on alpha-dystroglycan mediate laminin-induced acetylcholine receptor clustering but not laminin binding. J Biol Chem 278: 44868-44873.
34. Ware FE, Lehrman MA, (1996) Expression cloning of a novel suppressor of the Lec15 and Lec35 glycosylation mutations of Chinese hamster ovary cells. J Biol Chem 271: 13935-13938.
35. Stoll J, Robbins AR, Krag SS, (1982) Mutant of Chinese hamster ovary cells with altered mannose 6-phosphate receptor activity is unable to synthesize mannosylphosphoryldolichol. Proc Natl Acad Sci U S A 79: 2296-2300.