Protein O-mannosylation is crucial for E-cadherin-mediated cell adhesion

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 52, 2013, Pages 21024-21029

  Lommel, Mark ^a   Winterhalter, Patrick R ^a   Willer, Tobias ^a,c   Dahlhoff, Maik ^b   Schneider, Marlon R ^b   Bartels, Markus F ^a   Renner Müller, Ingrid ^b   Ruppert, Thomas ^a   Wolf, Eckhard ^b   Strahl, Sabine ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Mouse preimplantation development; O glycans; POMT1; POMT2; Protein glycosylation

Indexed keywords

EPITOPE; GLYCAN; MANNOSE; MANNOSYLTRANSFERASE; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLASTOCYST; BLASTOMA; CELL ADHESION; CELL AGGREGATION; CELL CONTACT; CELL JUNCTION; CONTROLLED STUDY; EMBRYO; LETHALITY; MASS SPECTROMETRY; MORULA; MOUSE; MOUSE EMBRYO; NONHUMAN; O MANNOSYLATION; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN PROCESSING; TIGHT JUNCTION;

EID: 84891363796     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316753110     Document Type: Article

References (44)

1. Lommel M, Strahl S (2009) Protein O-mannosylation: Conserved from bacteria to humans. Glycobiology 19(8): 816-828.
2. Godfrey C, Foley AR, Clement E, Muntoni F (2011) Dystroglycanopathies: Coming into focus. Curr Opin Genet Dev 21(3): 278-285.
3. Barresi R, Campbell KP (2006) Dystroglycan: From biosynthesis to pathogenesis of human disease. J Cell Sci 119(Pt 2): 199-207.
4. Willer T, et al. (2004) Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci USA 101(39): 14126-14131.
5. Michele DE, et al. (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418(6896): 417-422.
6. Chai W, et al. (1999) High prevalence of 2-mono- and 2, 6-di-substituted manol-terminating sequences among O-glycans released from brain glycopeptides by reductive alkaline hydrolysis. Eur J Biochem 263(3): 879-888.
7. Stalnaker SH, et al. (2011) Glycomic analyses of mouse models of congenital muscular dystrophy. J Biol Chem 286(24): 21180-21190.
8. Bleckmann C, et al. (2009) O-glycosylation pattern of CD24 from mouse brain. Biol Chem 390(7): 627-645.
9. Trinidad JC, Schoepfer R, Burlingame AL, Medzihradszky KF (2013) N- and O-glycosylation in the murine synaptosome. Mol Cell Proteomics, 10.1074/mcp.M113.030007. Available at www.mcponline.org/content/early/2013/07/ 01/mcp.M113.030007.long.
10. Pacharra S, Hanisch FG, Breloy I (2012) Neurofascin 186 is O-mannosylated within and outside of the mucin domain. J Proteome Res 11(8): 3955-3964.
11. Pacharra S, et al. (2013) The lecticans of mammalian brain perineural net are O-mannosylated. J Proteome Res 12(4): 1764-1771.
12. Manya H, et al. (2004) Demonstration of mammalian protein O-mannosyltransferase activity: Coexpression of POMT1 and POMT2 required for enzymatic activity. Proc Natl Acad Sci USA 101(2): 500-505.
13. Avsar-Ban E, et al. (2010) Protein O-mannosylation is necessary for normal embryonic development in zebrafish. Glycobiology 20(9): 1089-1102.
14. Haines N, Seabrooke S, Stewart BA (2007) Dystroglycan and protein O-mannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles. Mol Biol Cell 18(12): 4721-4730.
15. Halbleib JM, Nelson WJ (2006) Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20(23): 3199-3214.
16. Meng W, Takeichi M (2009) Adherens junction: Molecular architecture and regulation. Cold Spring Harb Perspect Biol 1(6):a002899.
17. Hulpiau P, van Roy F (2009) Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 41(2): 349-369.
18. Brasch J, Harrison OJ, Honig B, Shapiro L (2012) Thinking outside the cell: How cadherins drive adhesion. Trends Cell Biol 22(6): 299-310.
19. Larue L, Ohsugi M, Hirchenhain J, Kemler R (1994) E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA 91(17): 8263-8267.
20. Cavallaro U, Christofori G (2004) Cell adhesion and signalling by cadherins and Ig- CAMs in cancer. Nat Rev Cancer 4(2): 118-132.
21. Lommel M, et al. (2010) Correlation of enzyme activity and clinical phenotype in POMT1-associated dystroglycanopathies. Neurology 74(2): 157-164.
22. Hu H, et al. (2011) Conditional knockout of protein O-mannosyltransferase 2 reveals tissue-specific roles of O-mannosyl glycosylation in brain development. J Comp Neurol 519(7): 1320-1337.
23. Orchard MG, et al. (2004) Rhodanine-3-acetic acid derivatives as inhibitors of fungal protein mannosyl transferase 1 (PMT1). Bioorg Med Chem Lett 14(15): 3975-3978.
24. Argyros R, et al. (2013) A phenylalanine to serine substitution within an O-protein mannosyltransferase led to strong resistance to PMT-inhibitors in Pichia pastoris. PLoS ONE 8(5):e62229.
25. Arroyo J, et al. (2011) Functional and genomic analyses of blocked protein O-mannosylation in baker's yeast. Mol Microbiol 79(6): 1529-1546.
26. Fleming TP, et al. (1994) Molecular maturation of cell adhesion systems during mouse early development. Histochemistry 101(1): 1-7.
27. Wang H, et al. (2008) Zonula occludens-1 (ZO-1) is involved in morula to blastocyst transformation in the mouse. Dev Biol 318(1): 112-125.
28. Kan NG, et al. (2007) Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm. Development 134(1): 31-41.
29. Ohsugi M, Larue L, Schwarz H, Kemler R (1997) Cell-junctional and cytoskeletal organization in mouse blastocysts lacking E-cadherin. Dev Biol 185(2): 261-271.
30. Pinho SS, et al. (2011) Modulation of E-cadherin function and dysfunction by N-glycosylation. Cell Mol Life Sci 68(6): 1011-1020.
31. Harrison OJ, et al. (2011) The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19(2): 244-256.
32. Vester-Christensen MB, Halim A, Joshi HJ, Steentoft C, Bennett EP, et al. (2013) Mining the O-mannose glycoproteome reveals cadherins as major O-mannosylated glycoproteins. Proc Natl Acad Sci USA 110: 21018-21023.
33. Winterhalter PR, Lommel M, Ruppert T, Strahl S (2013) O-glycosylation of the noncanonical T-cadherin from rabbit skeletal muscle by single mannose residues. FEBS Lett 587(22): 3715-3721.
34. Boterberg T, Bracke ME, Bruyneel EA, Mareel MM (2001) Cell aggregation assays. Methods Mol Med 58: 33-45.
35. Stewart DB, Barth AI, Nelson WJ (2000) Differential regulation of endogenous cadherin expression in Madin-Darby canine kidney cells by cell-cell adhesion and activation of beta -catenin signaling. J Biol Chem 275(27): 20707-20716.
36. Jia L, Liu F, Hansen SH, Ter Beest MB, Zegers MM (2011) Distinct roles of cadherin-6 and E-cadherin in tubulogenesis and lumen formation.Mol Biol Cell 22(12): 2031-2041.
37. Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6(8): 622-634.
38. Liu J, et al. (2010) Cellular and molecular characterization of abnormal brain development in protein o-mannose N-acetylglucosaminyltransferase 1 knockout mice. Methods Enzymol 479: 353-366.
39. Thornhill P, Bassett D, Lochmüller H, Bushby K, Straub V (2008) Developmental defects in a zebrafish model for muscular dystrophies associated with the loss of fukutin- related protein (FKRP). Brain 131(Pt 6): 1551-1561.
40. Gupta V, et al. (2011) The zebrafish dag1 mutant: A novel genetic model for dystroglycanopathies. Hum Mol Genet 20(9): 1712-1725.
41. Babb SG, et al. (2005) Zebrafish R-cadherin (Cdh4) controls visual system development and differentiation. Dev Dyn 233(3): 930-945.
42. Erdmann B, Kirsch FP, Rathjen FG, Moré MI (2003) N-cadherin is essential for retinal lamination in the zebrafish. Dev Dyn 226(3): 570-577.
43. Kadowaki M, et al. (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304(1): 22-33.
44. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45.