Glycopeptidome of a heavily N-glycosylated cell surface glycoprotein of dictyostelium implicated in cell adhesion

Journal of Proteome Research

Volumn 9, Issue 7, 2010, Pages 3495-3510

  Feasley, Christa L ^a   Johnson, Jennifer M ^a   West, Christopher M ^a   Chia, Catherine P ^b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

Author keywords

Dictyostelium; glycobiology; glycopeptidome; gp130; mass spectrometry; N glycan

Indexed keywords

CELL SURFACE PROTEIN; GLYCOPEPTIDE; MONOSACCHARIDE; MEMBRANE PROTEIN; POLYSACCHARIDE; PROTOZOAL PROTEIN;

ANTIGEN BINDING; ARTICLE; CELL ADHESION; DICTYOSTELIUM; GLYCOBIOLOGY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; GLYCOSYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR GENETICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; TANDEM MASS SPECTROMETRY;

DICTYOSTELIUM;

AMINO ACID SEQUENCE; BASE SEQUENCE; CELL ADHESION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DICTYOSTELIUM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOMICS; GLYCOPEPTIDES; GLYCOSYLATION; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTOZOAN PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 77954355356     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr901195c     Document Type: Article

References (67)

1. Chadwick, C. M.; Ellison, J. E.; Garrod, D. R. Dual role for Dictyostelium contact site B in phagocytosis and developmental size regulation Nature 1984, 307, 646-647
2. 2+)-ATPase labelled with N-cyclohexyl-N-(4-dimethylamino-alpha-naphthyl)carbodiimide Biochim. Biophys. Acta 1984, 769, 291-296
3. Chia, C. P. A 130-kDa plasma membrane glycoprotein involved in Dictyostelium phagocytosis Exp. Cell Res. 1996, 227, 182-189
4. Chia, C. P.; Gomathinayagam, S.; Schmaltz, R. J.; Smoyer, L. K. Glycoprotein gp130 of Dictyostelium discoideum influences macropinocytosis and adhesion Mol. Biol. Cell 2005, 16, 2681-2693
5. Aiba, K.; Fang, H.; Yamaguchi, N.; Tanaka, Y.; Urushihara, H. Isoforms of gp138, a cell-fusion related protein in Dictyostelium discoideum J. Biochem. 1997, 121, 238-243
6. Fang, H.; Higa, M.; Suzuki, K.; Aiba, K.; Urushihara, H.; Yanagisawa, K. Molecular cloning and characterization of two genes encoding gp138, a cell surface glycoprotein involved in the sexual cell fusion of Dictyostelium discoideum Dev. Biol. 1993, 156, 201-208
7. Fang, H.; Aiba, K.; Higa, M.; Urushihara, H.; Yanagisawa, K. Antisense RNA inactivation of gp138 gene expression results in repression of sexual cell fusion in Dictyostelium discoideum J. Cell Sci. 1993, 106, 785-788
8. Hata, T.; Takahashi, M.; Tanaka, Y.; Urushihara, H. Total tetra knockout of GP138 multigene family implicated in cell interactions in Dictyostelium discoideum Gene 2001, 271, 33-42
9. Hata, T.; Yamaguchi, N.; Tanaka, Y.; Urushihara, H. A new member of the GP138 multigene family implicated in cell interactions in Dictyostelium discoideum Cell Struct. Funct. 1999, 24, 123-129
10. Dykstra, M. J.; Aldrich, H. C. Successful demonstration of an elusive cell coat in amebae J. Protozool. 1978, 25, 38-41
11. Sucgang, R.; Kuo, A.; Tian, X.; Salerno, W.; Parikh, A.; Feasley, C. L.; Dalin, E.; Tu, H.; Huang, E.; Barry, K.; Lindquist, E.; Shapiro, H.; Bruce, D.; Schmutz, J.; Fey, P.; Gaudet, P.; Anjard, C.; Mohan, M. B.; Basu, S.; Bushmanova, Y.; van der Wel, H.; Katoh, M.; Coutinho, P. M.; Saito, T.; Elias, M.; Schaap, P.; Kay, R. R.; Henrissat, B.; Eichinger, L.; Rivero-Crespo, F.; Putnam, N. H.; West, C. M.; Loomis, W. F.; Chisholm, R.; Shaulsky, G.; Strassmann, J. E.; Queller, D. C.; Kuspa, A.; Grigoriev, I. Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. 2010, submitted.
12. Boose, J. A.; Ziska, S. E.; Henderson, E. J. Defective intercellular cohesion in glycosylation mutants of Dictyostelium discoideum Dev. Genet. 1988, 9, 569-578
13. Bozzaro, S.; Roseman, S. Adhesion of Dictyostelium discoideum cells to carbohydrates immobilized in polyacrylamide gels. II. Effect of D-glucoside derivatives on development J. Biol. Chem. 1983, 258, 13890-13897 (Pubitemid 14203796)
14. Loomis, W. F.; Wheeler, S. A.; Springer, W. R.; Barondes, S. H. Adhesion mutants of Dictyostelium discoideum lacking the saccharide determinant recognized by two adhesion-blocking monoclonal antibodies Dev. Biol. 1985, 109, 111-117
15. Bozzaro, S. Cell surface carbohydrates and cell recognition in Dictyostelium Cell Differen. 1985, 17, 67-82
16. Pang, T. L.; Wu, C. J.; Chen, P. A.; Weng, Y. L.; Chen, M. Y. Dictyostelium gnt15 encodes a protein with similarity to LARGE and plays an essential role in development Biochem. Biophys. Res. Commun. 2007, 360, 83-89
17. Chia, C. P.; Luna, E. J. Phagocytosis in Dictyostelium discoideum is inhibited by antibodies directed primarily against common carbohydrate epitopes of a major cell- surface plasma membrane glycoprotein Exp. Cell Res. 1989, 181, 11-26
18. Browning, D. D.; Lewis, K. E.; O'Day, D. H. Zygote giant cell differentiation in Dictyostelium discoideum: biochemical markers of specific stages of sexual development Biochem. Cell Biol. 1992, 70, 1200-1208
19. Browning, D. D.; O'Day, D. H. Concanavalin A and wheat germ agglutinin binding glycoproteins associated with cell fusion and zygote differentiation in Dictyostelium discoideum: effects of calcium ions and tunicamycin on glycoprotein profiles Biochem. Cell Biol. 1991, 69, 282-290
20. O'Day, D. H.; Rivera, J. Lectin binding and inhibition studies reveal the importance of D-glucose, D-mannose and N-acetylglucosamine during early sexual development of Dictyostelium discoideum Cell Differen. 1987, 20, 231-237
21. Freeze, H. H. Dicytostelium discoideum glycoproteins: using a model system for organismic glycobiology. In New Comprehensive Biochemistry; Montreul, J.; Vliegenthart, J. F. G.; Schachter, H., Eds.; Elsevier: New York, 1998; Vol. 29B, pp 89 - 121.
22. Schiller, B.; Hykollari, A.; Voglmeir, J.; Poltl, G.; Hummel, K.; Razzazi-Fazeli, E.; Geyer, R.; Wilson, I. B. H. Development of Dictyostelium discoideum is associated with alteration of fucosylated N-glycan structures Biochem. J. 2009, 423, 41-52
23. Zhang, Y.; Zhang, P.; West, C. M. A linking function for the cellulose-binding protein SP85 in the spore coat of Dictyostelium discoideum J. Cell Sci. 1999, 112, 4367-4377
24. van der Wel, H.; Ercan, A.; West, C. M. The Skp1 prolyl hydroxylase from Dictyostelium is related to the hypoxia-inducible factor-alpha class of animal prolyl 4-hydroxylases J. Biol. Chem. 2005, 280, 14645-14655
25. Huesgen, A.; Gerisch, G. Solubilized contact sites a from cell membranes of Dictyostelium discoideum FEBS Lett. 1975, 56, 46-49
26. Wang, F.; Metcalf, T.; van der Wel, H.; West, C. M. Initiation of mucin-type O- glycosylation in Dictyostelium is homologous to the corresponding step in animals and is important for spore coat function J. Biol. Chem. 2003, 278, 51395-51407
27. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins from silver-stained polyacrylaminde gels Anal. Chem. 1996, 68, 850-858
28. Faye, L.; Gomord, V.; Fitchette-Laine, A. C.; Chrispeels, M. J. Affinity purification of antibodies specific for Asn-linked glycans containing alpha 1 - >3 fucose or beta 1 - >2 xylose Anal. Biochem. 1993, 209, 104-108
29. Srikrishna, G.; Wang, L.; Freeze, H. H. Fucosebeta-1-P-Ser is a new type of glycosylation: using antibodies to identify a novel structure in Dictyostelium discoideum and study multiple types of fucosylation during growth and development Glycobiology 1998, 8, 799-811
30. Hardy, M. R.; Townsend, R. R. High-pH anion-exchange chromatography of glycoprotein-derived carbohydrates Methods Enzymol. 1994, 230, 208-225
31. Geyer, H.; Schmitt, S.; Wuhrer, M.; Geyer, R. Structural analysis of glycoconjugates by on-target enzymatic digestion and MALDI-TOF-MS Analyt. Chem. 1999, 71, 476-482
32. Mechref, Y.; Novotny, M. Mass spectrometric mapping and sequencing of N-linked oligosaccharides derived from submicrogram amounts of glycoproteins Analyt. Chem. 1998, 3, 455-463
33. Colangelo, J.; Orlando, R. On-target exoglycosidase digestions/MALDI-MS for determining the primary structures of carbohydrate chains Anal. Chem. 1999, 71, 1479-1482
34. Bigge, J. C.; Patel, T. P.; Bruce, J. A.; Goulding, P. N.; Charles, S. M.; Parekh, R. B. Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid Anal. Biochem. 1995, 230, 229-238
35. Kang, P.; Mechref, Y.; Novotny, M. V. High-throughput solid-phase permethylation of glycans prior to mass spectrometry Rapid Commun. Mass Spectrom. 2008, 22, 721-734
36. Lei, M.; Mechref, Y.; Novotny, M. V. Structural analysis of sulfated glycans by sequential double-permethylation using methyl iodide and deuteromethyl iodide J. Am. Soc. Mass Spectrom. 2009, 20, 1660-1671
37. Dell, A.; Chalabi, S.; Easton, R. L.; Haslam, S. M.; Sutton-Smith, M.; Patankar, M. S.; Lattanzio, F.; Panico, M.; Morris, H. R.; Clark, G. F. Murine and human zona pellucida 3 derived from mouse eggs express identical O-glycans Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 15631-15636
38. Kang, P.; Mechref, Y.; Klouckova, I.; Novotny, M. V. Solid-phase permethylation of glycans for mass spectrometric analysis Rapid Commun. Mass Spectrom. 2005, 19, 3421-3428
39. Babu, P.; North, S. J.; Jang-Lee, J.; Chalabi, S.; Mackerness, K.; Stowell, S. R.; Cummings, R. D.; Rankin, S.; Dell, A.; Haslam, S. M. Structural characterisation of neutrophil glycans by ultra sensitive mass spectrometric glycomics methodology Glycoconj. J. 2008, 26, 975-986
40. Huang, Y.; Mechref, Y.; Novotny, M. V. Microscale nonreductive release of O-linked glycans for subsequent analysis through MALDI mass spectrometry and capillary electrophoresis Anal. Chem. 2001, 73, 6063-6069
41. Makino, Y.; Omichi, K.; Hase, S. Analysis of oligosaccharide structures from the reducing end terminal by combining partial acid hydrolysis and a two-dimensional sugar map Anal. Biochem. 1998, 264, 172-179
42. Gonzalez-Yanes, B.; Mandell, R. B.; Girard, M.; Henry, S.; Aparicio, O.; Gritzali, M.; Brown, R. D., Jr.; Erdos, G. W.; West, C. M. The spore coat of a fucosylation mutant in Dictyostelium discoideum Dev. Biol. 1989, 133, 576-587
43. Aparicio, J. G.; Erdos, G. W.; West, C. M. Spore coat is altered in modB glycosylation mutants of Dictyostelium discoideum J. Cell. Biochem. 1990, 42, 255-266
44. Herscovics, A. Structure and function of Class I alpha 1,2-mannosidases involved in glycoprotein synthesis and endoplasmic reticulum quality control Biochimie 2001, 83, 757-762
45. Couso, R.; van Halbeek, H.; Reinhold, V.; Kornfeld, S. The high mannose oligosaccharides of Dictyostelium discoideum glycoproteins contain a novel intersecting N-acetylglucosamine residue J. Biol. Chem. 1987, 262, 4521-4527
46. Faye, L.; Johnson, K. D.; Chrispeels, M. J. Oligosaccharide side chains of glycoproteinsthat remain in the high-mannose form are not accessible to glycosidases Plant Physiol. 1986, 81, 206-211
47. Sharkey, D. J.; Kornfeld, R. Developmental regulation of asparagine-linked oligosaccharide synthesis in Dictyostelium discoideum J. Biol. Chem. 1991, 266, 18485-18497
48. Sharkey, D. J.; Kornfeld, R. Identification of an N- acetylglucosaminyltransferase in Dictyostelium discoideum that transfers an 'intersecting' N-acetylglucosamine residue tohigh mannose oligosaccharides J. Biol. Chem. 1989, 264, 10411-10419
49. Domon, B.; Costello, C. E. A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates Glycoconj. J. 1988, 5, 397-409
50. Lei, M.; Mechref, Y.; Novotny, M. V. Structural analysis of sulfated glycans by sequential double-permethylation using methyl iodide and deuteromethyl iodide J. Am. Soc. Mass Spectrom. 2009, 20, 1660-1671
51. Murakami, T.; Natsuka, S.; Nakakita, S.; Hase, S. Structure determination of a sulfated N- glycans, candidate for a precursor of the selectin ligand in bovine lung Glycoconj. J. 2007, 24, 195-206
52. Song, X.; Lasanajak, Y.; Xia, B.; Smith, D. F.; Cummings, R. D. Fluorescent glycosylamides produced by microscale derivatization of free glycans for natural glycan microarrays ACS Chem. Biol. 2009, 4, 741-750
53. Song, X.; Lasanajak, Y.; Olson, L. J.; Boonen, M.; Dahms, N. M.; Kornfeld, S.; Cummings, R. D.; Smith, D. F. Glycan microarray analysis of P-type lectins reveals distinct phospho- mannose glycan recognition J. Biol. Chem. 2009, 284, 35201-35214
54. Freeze, H. H.; Wolgast, D. Structural analysis of N-linked oligosaccharides from glycoproteins secreted by Dictyostelium discoideum. Identification of mannose 6-sulfate J. Biol. Chem. 1986, 261, 127-34
55. Freeze, H. H.; Hindsgaul, O.; Ichikawa, M. A novel pathway for phosphorylated oligosaccharide biosynthesis. Identification of an oligosaccharide-specific phosphate methyltransferase in Dictyostelium discoideum J. Biol. Chem. 1992, 267, 4431-4439
56. Freeze, H. H.; Yeh, R.; Miller, A. L.; Kornfeld, S. Structural analysis of the asparagine-linked oligosaccharides from three lysosomal enzymes of Dictyostelium discoideum. Evidence for an unusual acid-stable phosphodiester J. Biol. Chem. 1983, 258, 14874-14879
57. Ivatt, R. L.; Das, O. P.; Henderson, E. J.; Robbins, P. W. Glycoprotein biosynthesis in Dictyostelium discoideum: developmental regulation of the protein-linked glycans Cell 1984, 38, 561-567
58. Tschursin, E.; Riley, G. R.; Henderson, E. J. Differential regulation of glycoprotein sulfation and fucosylation during growth of Dictyostelium discoideum Differentiation 1989, 40, 1-9
59. West, C. M.; van der Wel, H.; Coutinho, P. M.; Henrissat, B. Glycosyltransferase genomics in Dictyostelium discoideum. In Dictyostelium Genomics; Loomis, W. F.; Kuspa, A., Eds.; Horizon Scientific Press: Norfolk, U.K., 2005; pp 235 - 264.
60. GCG Sequence Analysis Software Program, 2001; Acclerys (http://accelrys.com/, San Diego, CA).
61. Aiba, K.; Yanagisawa, K.; Urushihara, H. Distribution of gp138, a cell surface protein responsible for sexual cell fusion, among cellular slime moulds J. Gen. Microbiol. 1993, 139, 279-285
62. Sternfeld, J. Evidence for differential cellular adhesion as the mechanism of sorting-out of various cellular slime mold species J. Embryol. Exp. Morphol. 1979, 53, 163-178
63. Mehdiabadi, N. J.; Jack, C. N.; Farnham, T. T.; Platt, T. G.; Kalla, S. E.; Shaulsky, G.; Queller, D. C.; Strassmann, J. E. Social evolution: kin preference in a social microbe Nature 2006, 442, 881-882
64. Banerjee, S.; Vishwanath, P.; Cui, J.; Kelleher, D. J.; Gilmore, R.; Robbins, P. W.; Samuelson, J. The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 11676-11681
65. West, M. B.; Segu, Z.; Feasley, C. L.; Kang, P.; Klouckova, I.; Novotny, M.; West, C. M.; Mechref, Y.; Hanigan, M. H. Analysis of site-specific glycosylation of renal and hepatic -glutamyltranspeptidase from normal human tissue. Submitted.
66. Alvarez-Manilla, G.; Warren, N. L.; Atwood, J. A.; Dalton, S.; Orlando, R.; Pierce, M. Glycoproteomic analysis of embryonic stem cells: identification of potential glycobiomarkers using lectin affinity chromatography of glycopeptides J. Proteome. Res. 2010, 9, 2062-2075
67. Satomaa, T.; Heiskanen, A.; Mikkola, M.; Olsson, C.; Blomqvist, M.; Tiittanen, M.; Jaatinen, T.; Aitio, O.; Olonen, A.; Helin, J.; Hiltunen, J.; Natunen, J.; Tuuri, T.; Otonkoski, T.; Saarinen, J.; Laine, J. The N-glycome of human embryonic stem cells BMC Cell Biol. 2009, 10, 42