Defective mucin-type glycosylation on α-dystroglycan in COG-deficient cells increases its susceptibility to bacterial proteases

Journal of Biological Chemistry

Volumn 293, Issue 37, 2018, Pages 14534-14544

  Yu, Seok Ho ^a   Zhao, Peng ^a   Prabhakar, Pradeep K ^a   Sun, Tiantian ^a   Beedle, Aaron ^a   Boons, Geert Jan ^a   Moremen, Kelley W ^a   Wells, Lance ^a   Steet, Richard ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CYTOLOGY; GLYCOPROTEINS; POLYSACCHARIDES; PROTEINS; PROTEOLYSIS;

BLOTTING ANALYSIS; CHINESE HAMSTER OVARY; CONGENITAL DISORDERS; CONSERVED OLIGOMERIC GOLGI COMPLEXES; METABOLIC LABELING; PROTEIN STABILITY; RAPID DEGRADATION; SURFACE GLYCOPROTEINS;

GLYCOSYLATION;

ALPHA DYSTROGLYCAN; ALPHA SARCOGLYCAN; CELL PROTEIN; CONSERVED OLIGOMERIC GOLGI COMPLEX; GLYCOPROTEIN; MUCIN; PROTEINASE; SIALIDASE; UNCLASSIFIED DRUG; DYSTROGLYCAN; HYALURONATE LYASE; PEPTIDE HYDROLASE; POLYSACCHARIDE LYASE;

ANIMAL CELL; ARTICLE; CELL SURFACE; CHO CELL LINE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN STABILITY; VIBRIO CHOLERAE; WESTERN BLOTTING; WILD TYPE; ANIMAL; BACTERIUM; CRICETULUS; ENZYMOLOGY; GLYCOSYLATION; HALF LIFE TIME; METABOLISM;

ANIMALS; BACTERIA; CHO CELLS; CRICETULUS; DYSTROGLYCANS; GLYCOPROTEINS; GLYCOSYLATION; HALF-LIFE; MUCINS; PEPTIDE HYDROLASES; POLYSACCHARIDE-LYASES;

EID: 85053338058     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.RA118.003014     Document Type: Article

References (45)

1. Freeze, H. H. (2007) Congenital disorders of glycosylation: CDG-I, CDGII, and beyond. Curr. Mol. Med. 7, 389-396 CrossRef Medline.
2. Jaeken, J. (2010) Congenital disorders of glycosylation. Ann. N.Y. Acad. Sci. 1214, 190-198 CrossRef Medline.
3. Jaeken, J., and Matthijs, G. (2007) Congenital disorders of glycosylation: A rapidly expanding disease family. Annu. Rev. Genomics Hum. Genet. 8, 261-278 CrossRef Medline.
4. Haeuptle, M. A., and Hennet, T. (2009) Congenital disorders of glycosylation: An update on defects affecting the biosynthesis of dolichol-linked oligosaccharides. Hum. Mutat. 30, 1628-1641 CrossRef Medline.
5. Kim, Y. M., Seo, G. H., Jung, E., Jang, J. H., Kim, S. Z., and Lee, B. H. (2018) Characteristic dysmorphic features in congenital disorders of glycosylation type IIb. J. Hum. Genet. 63, 383-386 CrossRef Medline.
6. Krasnewich, D., O'Brien, K., and Sparks, S. (2007) Clinical features in adults with congenital disorders of glycosylation type Ia (CDG-Ia). Am. J. Med. Genet. C Semin. Med. Genet. 145C, 302-306 CrossRef Medline.
7. Marques-da-Silva, D., Dos Reis Ferreira, V., Monticelli, M., Janeiro, P., Videira, P. A., Witters, P., Jaeken, J., and Cassiman, D. (2017) Liver involvement in congenital disorders of glycosylation (CDG): A systematic review of the literature. J. Inherit. Metab. Dis. 40, 195-207 CrossRef Medline.
8. Marques-da-Silva, D., Francisco, R., Webster, D., Dos Reis Ferreira, V., Jaeken, J., and Pulinilkunnil, T. (2017) Cardiac complications of congenital disorders of glycosylation (CDG): A systematic review of the literature. J. Inherit. Metab. Dis. 40, 657-672 CrossRef Medline.
9. Barone, R., Fiumara, A., and Jaeken, J. (2014) Congenital disorders of glycosylation with emphasis on cerebellar involvement. Semin. Neurol. 34, 357-366 CrossRef Medline.
10. Hennet, T. (2012) Diseases of glycosylation beyond classical congenital disorders of glycosylation. Biochim. Biophys. Acta 1820, 1306-1317 CrossRef Medline.
11. Wu, X., Steet, R. A., Bohorov, O., Bakker, J., Newell, J., Krieger, M., Spaapen, L., Kornfeld, S., and Freeze, H. H. (2004) Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder. Nat. Med. 10, 518-523 CrossRef Medline.
12. Ungar, D., Oka, T., Brittle, E. E., Vasile, E., Lupashin, V. V., Chatterton, J. E., Heuser, J. E., Krieger, M., and Waters, M. G. (2002) Characterization of a mammalian Golgi-localized protein complex, COG, that is required for normal Golgi morphology and function. J. Cell Biol. 157, 405-415 CrossRef Medline.
13. Zolov, S. N., and Lupashin, V. V. (2005) Cog3p depletion blocks vesiclemediated Golgi retrograde trafficking in HeLa cells. J. Cell Biol. 168, 747-759 CrossRef Medline.
14. Oka, T., Ungar, D., Hughson, F. M., and Krieger, M. (2004) The COG and COPI complexes interact to control the abundance of GEARs, a subset of Golgi integral membrane proteins. Mol. Biol. Cell 15, 2423-2435 CrossRef Medline.
15. Shestakova, A., Zolov, S., and Lupashin, V. (2006) COG complex-mediated recycling of Golgi glycosyltransferases is essential for normal protein glycosylation. Traffic 7, 191-204 CrossRef Medline.
16. Foulquier, F., Vasile, E., Schollen, E., Callewaert, N., Raemaekers, T., Quelhas, D., Jaeken, J., Mills, P., Winchester, B., Krieger, M., Annaert, W., and Matthijs, G. (2006) Conserved oligomeric Golgi complex subunit 1 deficiency reveals a previously uncharacterized congenital disorder of glycosylation type II. Proc. Natl. Acad. Sci. U.S.A. 103, 3764-3769 CrossRef Medline.
17. Kranz, C., Ng, B. G., Sun, L., Sharma, V., Eklund, E. A., Miura, Y., Ungar, D., Lupashin, V., Winkel, R. D., Cipollo, J. F., Costello, C. E., Loh, E., Hong, W., and Freeze, H. H. (2007) COG8 deficiency causes new congenital disorder of glycosylation type IIh. Hum. Mol. Genet. 16, 731-741 CrossRef Medline.
18. Palmigiano, A., Bua, R. O., Barone, R., Rymen, D., Régal, L., Deconinck, N., Dionisi-Vici, C., Fung, C. W., Garozzo, D., Jaeken, J., and Sturiale, L. (2017) MALDI-MS profiling of serum O-glycosylation and N-glycosylation in COG5-CDG. J. Mass Spectrom. 52, 372-377 CrossRef Medline.
19. Xia, B., Zhang, W., Li, X., Jiang, R., Harper, T., Liu, R., Cummings, R. D., and He, M. (2013) Serum N-glycan and O-glycan analysis by mass spectrometry for diagnosis of congenital disorders of glycosylation. Anal. Biochem. 442, 178-185 CrossRef Medline.
20. Frappaolo, A., Sechi, S., Kumagai, T., Robinson, S., Fraschini, R., Karimpour-Ghahnavieh, A., Belloni, G., Piergentili, R., Tiemeyer, K. H., Tiemeyer, M., and Giansanti, M. G. (2017)COG7deficiency in Drosophila generates multifaceted developmental, behavioral and protein glycosylation phenotypes. J. Cell Sci. 130, 3637-3649 CrossRef Medline.
21. Kingsley, D. M., Kozarsky, K. F., Segal, M., and Krieger, M. (1986) Three types of low density lipoprotein receptor-deficient mutant have pleiotropic defects in the synthesis of N-linked, O-linked, and lipid-linked carbohydrate chains. J. Cell Biol. 102, 1576-1585 CrossRef Medline.
22. Kingsley, D. M., and Krieger, M. (1984) Receptor-mediated endocytosis of low density lipoprotein: Somatic cell mutants define multiple genes required for expression of surface-receptor activity. Proc. Natl. Acad. Sci. U.S.A. 81, 5454-5458 CrossRef Medline.
23. Kozarsky, K. F., Brush, H. A., and Krieger, M. (1986) Unusual forms of low density lipoprotein receptors in hamster cell mutants with defects in the receptor structural gene. J. Cell Biol. 102, 1567-1575 CrossRef Medline.
24. Deng, W. M., Schneider, M., Frock, R., Castillejo-Lopez, C., Gaman, E. A., Baumgartner, S., and Ruohola-Baker, H. (2003) Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130, 173-184 CrossRef Medline.
25. Moremen, K. W., Ramiah, A., Stuart, M., Steel, J., Meng, L., Forouhar, F., Moniz, H. A., Gahlay, G., Gao, Z., Chapla, D., Wang, S., Yang, J. Y., Prabhakar, P. K., Johnson, R., Rosa, M. D., et al. (2018) Expression system for structural and functional studies of human glycosylation enzymes. Nat. Chem. Biol. 14, 156-162 Medline.
26. Schneider, M., Khalil, A. A., Poulton, J., Castillejo-Lopez, C., Egger-Adam, D., Wodarz, A., Deng, W. M., and Baumgartner, S. (2006) Perlecan and Dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization. Development 133, 3805-3815 CrossRef Medline.
27. Friscourt, F., Ledin, P. A., Mbua, N. E., Flanagan-Steet, H. R., Wolfert, M. A., Steet, R., and Boons, G. J. (2012) Polar dibenzocyclooctynes for selective labeling of extracellular glycoconjugates of living cells. J. Am. Chem. Soc. 134, 5381-5389 CrossRef Medline.
28. Burnet, F. M., and Stone, J. D. (1947) Desquamation of intestinal epithelium in vitro by V. cholerae filtrates: Characterization of mucinase and tissue disintegrating enzymes. Aust. J. Exp. Biol. Med. Sci. 25, 219-226 CrossRef Medline.
29. Crennell, S., Garman, E., Laver, G., Vimr, E., and Taylor, G. (1994) Crystal structure of Vibrio cholera neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure 2, 535-544 CrossRef Medline.
30. Schneider, D. R., and Parker, C. D. (1982) Purification and characterization of the mucinase of Vibrio cholerae. J. Infect. Dis. 145, 474-482 CrossRef Medline.
31. Stewart-Tull, D. E., Ollar, R. A., and Scobie, T. S. (1986) Studies on the Vibrio cholerae mucinase complex: I. enzymic activities associated with the complex. J. Med. Microbiol. 22, 325-333 CrossRef Medline.
32. Brancaccio, A., Schulthess, T., Gesemann, M., and Engel, J. (1997) The N-terminal region of -dystroglycan is an autonomous globular domain. Eur. J. Biochem. 246, 166-172 CrossRef Medline.
33. Heng, S., Paule, S. G., Li, Y., Rombauts, L. J., Vollenhoven, B., Salamonsen, L. A., and Nie, G. (2015) Posttranslational removal of α dystroglycan N terminus by PC5/6 cleavage is important for uterine preparation for embryo implantation in women. FASEB J. 29, 4011-4022 CrossRef Medline.
34. Szabady, R. L., Yanta, J. H., Halladin, D. K., Schofield, M. J., and Welch, R. A. (2011) TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins. Microbiology 157, 516 -525 CrossRef Medline.
35. Jae, L. T., Raaben, M., Herbert, A. S., Kuehne, A. I., Wirchnianski, A. S., Soh, T. K., Stubbs, S. H., Janssen, H., Damme, M., Saftig, P., Whelan, S. P., Dye, J. M., and Brummelkamp, T. R. (2014) Virus entry: Lassa virus entry requires a trigger-induced receptor switch. Science 344, 1506-1510 CrossRef Medline.
36. 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 CrossRef Medline.
37. Aguilan, J. T., Sundaram, S., Nieves, E., and Stanley, P. (2009) Mutational and functional analysis of Large in a novel CHO glycosylation mutant. Glycobiology 19, 971-986 CrossRef Medline.
38. Lübbehusen, J., Thiel, C., Rind, N., Ungar, D., Prinsen, B. H., de Koning, T. J., van Hasselt, P. M., and Körner, C. (2010) Fatal outcome due to deficiency of subunit 6 of the conserved oligomeric Golgi complex leading to a new type of congenital disorders of glycosylation. Hum. Mol. Genet. 19, 3623-3633 CrossRef Medline.
39. Paesold-Burda, P., Maag, C., Troxler, H., Foulquier, F., Kleinert, P., Schnabel, S., Baumgartner, M., and Hennet, T. (2009) Deficiency in COG5 causes a moderate form of congenital disorders of glycosylation. Hum. Mol. Genet. 18, 4350-4356 CrossRef Medline.
40. Rymen, D., Keldermans, L., Race, V., Régal, L., Deconinck, N., Dionisi-Vici, C., Fung, C. W., Sturiale, L., Rosnoblet, C., Foulquier, F., Matthijs, G., and Jaeken, J. (2012) COG5-CDG: Expanding the clinical spectrum. Orphanet J. Rare Dis. 7, 94 CrossRef Medline.
41. Rymen, D., Winter, J., Van Hasselt, P. M., Jaeken, J., Kasapkara, C., Gokçay, G., Haijes, H., Goyens, P., Tokatli, A., Thiel, C., Bartsch, O., Hecht, J., Krawitz, P., Prinsen, H. C., Mildenberger, E., et al. (2015) Key features and clinical variability of COG6-CDG. Mol. Genet. Metab. 116, 163-170 CrossRef Medline.
42. Lefeber, D. J., Schönberger, J., Morava, E., Guillard, M., Huyben, K. M., Verrijp, K., Grafakou, O., Evangeliou, A., Preijers, F. W., Manta, P., Yildiz, J., Grünewald, S., Spilioti, M., van den Elzen, C., Klein, D., et al. (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 CrossRef Medline.
43. Mbua, N. E., Guo, J., Wolfert, M. A., Steet, R., and Boons, G. J. (2011) Strain-promoted alkyne-azide cycloadditions (SPAAC) reveal new features of glycoconjugate biosynthesis. Chembiochem 12, 1912-1921 CrossRef Medline.
44. Yu, S. H., Zhao, P., Sun, T., Gao, Z., Moremen, K. W., Boons, G. J., Wells, L., and Steet, R. (2016) Selective exo-enzymatic labeling detects increased cell surface sialoglycoprotein expression upon megakaryocytic differentiation. J. Biol. Chem. 291, 3982-3989 CrossRef Medline.
45. Fortunato, M. J., Ball, C. E., Hollinger, K., Patel, N. B., Modi, J. N., Rajasekaran, V., Nonneman, D. J., Ross, J. W., Kennedy, E. J., Selsby, J. T., and Beedle, A. M. (2014) Development of rabbit monoclonal antibodies for detection of dystroglycan in normal and dystrophic tissue. PLoS One 9, e97567 CrossRef Medline.