Altered N-glycan expression profile in epithelial-to-mesenchymal transition of NMuMG cells revealed by an integrated strategy using mass spectrometry and glycogene and lectin microarray analysis

Journal of Proteome Research

Volumn 13, Issue 6, 2014, Pages 2783-2795

  Tan, Zengqi ^a   Lu, Wei ^a   Li, Xiang ^b   Yang, Ganglong ^a   Guo, Jia ^a   Yu, Hanjie ^c   Li, Zheng ^c   Guan, Feng ^a  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b JIANGNAN UNIVERSITY   (China)

^c NORTHWEST UNIVERSITY   (China)

Author keywords

gene microarray; glycogene; high throughput; lectin microarray; mass spectrometry; N glycan

Indexed keywords

GLYCAN; LECTIN; N ACETYLGLUCOSAMINE; TRANSFORMING GROWTH FACTOR BETA1; GLYCOPROTEIN; POLYSACCHARIDE; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA;

ALG9 GENE; ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FUCOSYLATION; GENE; GENE EXPRESSION; GLYCOBIOLOGY; GLYCOGENE; GLYCOSYLATION; HISTOCHEMISTRY; MAMMARY GLAND; MASS SPECTROMETRY; MGAT3 GENE; MGAT4B GENE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; CARBOHYDRATE ANALYSIS; CELL LINE; CHEMISTRY; CONFORMATION; DNA MICROARRAY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN PROCESSING;

ANIMALS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CELL LINE; EPITHELIAL-MESENCHYMAL TRANSITION; GLYCOPROTEINS; GLYCOSYLATION; LECTINS; MICE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYSACCHARIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA;

EID: 84902096317     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401185z     Document Type: Article

References (46)

1. Li, M.; Song, L.; Qin, X. Glycan changes: cancer metastasis and anti-cancer vaccines J. Biosciences 2010, 35, 665-673
2. Dube, D. H.; Bertozzi, C. R. Glycans in cancer and inflammation-potential for therapeutics and diagnostics Nat. Rev. Drug Discovery 2005, 4, 477-488
3. Ruhaak, L. R.; Miyamoto, S.; Lebrilla, C. B. Developments in the identification of glycan biomarkers for the detection of cancer Mol. Cell. Proteomics 2013, 12, 846-855
4. Alley, W. R., Jr.; Madera, M.; Mechref, Y.; Novotny, M. V. Chip-based reversed-phase liquid chromatography-mass spectrometry of permethylated N-linked glycans: a potential methodology for cancer-biomarker discovery Anal. Chem. 2010, 82, 5095-5106
5. Hamid, U. M. A.; Royle, L.; Saldova, R.; Radcliffe, C. M.; Harvey, D. J.; Storr, S. J.; Pardo, M.; Antrobus, R.; Chapman, C. J.; Zitzmann, N. A strategy to reveal potential glycan markers from serum glycoproteins associated with breast cancer progression Glycobiology 2008, 18, 1105-1118
6. Saldova, R.; Royle, L.; Radcliffe, C. M.; Hamid, U. M. A.; Evans, R.; Arnold, J. N.; Banks, R. E.; Hutson, R.; Harvey, D. J.; Antrobus, R. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG Glycobiology 2007, 17, 1344-1356
7. Ito, Y.; Miyauchi, A.; Yoshida, H.; Uruno, T.; Nakano, K.; Takamura, Y.; Miya, A.; Kobayashi, K.; Yokozawa, T.; Matsuzuka, F. Expression of α1, 6-fucosyltransferase (FUT8) in papillary carcinoma of the thyroid: its linkage to biological aggressiveness and anaplastic transformation Cancer Lett. 2003, 200, 167-172
8. Taniguchi, N.; Gu, J.; Takahashi, M.; Miyoshi, E. Functional glycomics and evidence for gain-and loss-of-functions of target proteins for glycosyltransferases involved in N-glycan biosynthesis: their pivotal roles in growth and development, cancer metastasis and antibody therapy against cancer Proc. Jpn. Acad., Ser. B. 2004, 80, 82-91
9. Wu, S. L.; Taylor, A. D.; Lu, Q.; Hanash, S. M.; Im, H.; Snyder, M.; Hancock, W. S. Identification of potential glycan cancer markers with sialic acid attached to sialic acid and up-regulated fucosylated galactose structures in epidermal growth factor receptor secreted from A431 cell line Mol. Cell. Proteomics 2013, 12, 1239-1249
10. Landers, K. A.; Burger, M. J.; Tebay, M. A.; Purdie, D. M.; Scells, B.; Samaratunga, H.; Lavin, M. F.; Gardiner, R. A. Use of multiple biomarkers for a molecular diagnosis of prostate cancer Int. J. Cancer 2005, 114, 950-956
11. Battula, V. L.; Shi, Y.; Evans, K. W.; Wang, R. Y.; Spaeth, E. L.; Jacamo, R. O.; Guerra, R.; Sahin, A. A.; Marini, F. C.; Hortobagyi, G. Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis J. Clin. Invest. 2012, 122, 2066-2078
12. Liang, Y. J.; Ding, Y.; Levery, S. B.; Lobaton, M.; Handa, K.; Hakomori, S. Differential expression profiles of glycosphingolipids in human breast cancer stem cells vs. cancer non-stem cells Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 4968-4973
13. Guan, F.; Schaffer, L.; Handa, K.; Hakomori, S. Functional role of gangliotetraosylceramide in epithelial-to-mesenchymal transition process induced by hypoxia and by TGF-β FASEB. J. 2010, 24, 4889-4903
14. Guan, F.; Handa, K.; Hakomori, S. Specific glycosphingolipids mediate epithelial-to-mesenchymal transition of human and mouse epithelial cell lines Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 7461-7466
15. Kalluri, R. EMT: when epithelial cells decide to become mesenchymal-like cells J. Clin. Invest. 2009, 119, 1417-1419
16. Willis, B. C.; Borok, Z.; TGF-β-induced, E. M. T. mechanisms and implications for fibrotic lung disease Am. J. Physiol.: Lung Cell. Mol. Physiol. 2007, 293, L525-L534
17. Li, S.; Mo, C.; Peng, Q.; Kang, X.; Sun, C.; Jiang, K.; Huang, L.; Lu, Y.; Sui, J.; Qin, X. Cell Surface Glycan Alterations in Epithelial Mesenchymal Transition Process of Huh7 Hepatocellular Carcinoma Cell PloS One 2013, 8, e71273
18. Maupin, K. A.; Sinha, A.; Eugster, E.; Miller, J.; Ross, J.; Paulino, V.; Keshamouni, V. G.; Tran, N.; Berens, M.; Webb, C. Glycogene expression alterations associated with pancreatic cancer epithelial-mesenchymal transition in complementary model systems PloS One 2010, 5, e13002
19. Pinho, S. S.; Oliveira, P.; Cabral, J.; Carvalho, S.; Huntsman, D.; Gärtner, F.; Seruca, R.; Reis, C. A.; Oliveira, C. Loss and recovery of Mgat3 and GnT-III Mediated E-cadherin N-glycosylation is a mechanism involved in epithelial-mesenchymal-epithelial transitions PLoS One 2012, 7, e33191
20. Xu, Q.; Isaji, T.; Lu, Y.; Gu, W.; Kondo, M.; Fukuda, T.; Du, Y.; Gu, J. Roles of N-acetylglucosaminyltransferase III in epithelial-to-mesenchymal transition induced by transforming growth factorβ1 (TGF-β1) in epithelial cell lines J. Biol. Chem. 2012, 287, 16563-16574
21. Terao, M.; Ishikawa, A.; Nakahara, S.; Kimura, A.; Kato, A.; Moriwaki, K.; Kamada, Y.; Murota, H.; Taniguchi, N.; Katayama, I. Enhanced epithelial-mesenchymal transition-like phenotype in N- acetylglucosaminyltransferase V transgenic mouse skin promotes wound healing J. Biol. Chem. 2011, 286, 28303-28311
22. Lockhart, D. J.; Dong, H.; Byrne, M. C.; Follettie, M. T.; Gallo, M. V.; Chee, M. S.; Mittmann, M.; Wang, C.; Kobayashi, M.; Norton, H. Expression monitoring by hybridization to high-density oligonucleotide arrays Nat. Biotechnol. 1996, 14, 1675-1680
23. Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat. Appl. Genet. Mol. 2004, 3, 3
24. - ΔΔCT Method Methods 2001, 25, 402-408
25. Yu, H.; Zhu, M.; Qin, Y.; Zhong, Y.; Yan, H.; Wang, Q.; Bian, H.; Li, Z. Analysis of glycan-related genes expression and glycan profiles in mice with liver fibrosis J. Proteome Res. 2012, 11, 5277-5285
26. Qin, Y.; Zhong, Y.; Dang, L.; Zhu, M.; Yu, H.; Chen, W.; Cui, J.; Bian, H.; Li, Z. Alteration of protein glycosylation in human hepatic stellate cells activated with transforming growth factor-β1 J. Proteomics 2012, 75, 4114-4123
27. Yang, G.; Cui, T.; Wang, Y.; Sun, S.; Ma, T.; Wang, T.; Chen, Q.; Li, Z. Selective isolation and analysis of glycoprotein fractions and their glycomes from hepatocellular carcinoma sera Proteomics 2013, 13, 1481-1498
28. Gil, G. C.; Iliff, B.; Cerny, R.; Velander, W. H.; Van Cott, K. E. High throughput quantification of N-glycans using one-pot sialic acid modification and matrix assisted laser desorption ionization time-of-flight mass spectrometry Anal. Chem. 2010, 82, 6613-6620
29. Ceroni, A.; Maass, K.; Geyer, H.; Geyer, R.; Dell, A.; Haslam, S. M. GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans J. Proteome Res. 2008, 7, 1650-1659
30. Gu, J.; Isaji, T.; Xu, Q.; Kariya, Y.; Gu, W.; Fukuda, T.; Du, Y. Potential roles of N-glycosylation in cell adhesion Glycoconjugate J. 2012, 29, 599-607
31. Fukuda, M. N. i.; Sasaki, H.; Lopez, L.; Fukuda, M. Survival of recombinant erythropoietin in the circulation: the role of carbohydrates Blood 1989, 73, 84-89
32. Balog, C. I.; Stavenhagen, K.; Fung, W. L.; Koeleman, C. A.; McDonnell, L. A.; Verhoeven, A.; Mesker, W. E.; Tollenaar, R. A.; Deelder, A. M.; Wuhrer, M. N-glycosylation of colorectal cancer tissues: a liquid chromatography and mass spectrometry-based investigation Mol. Cell. Proteomics 2012, 11, 571-585
33. Mehta, A.; Norton, P.; Liang, H.; Comunale, M. A.; Wang, M.; Rodemich-Betesh, L.; Koszycki, A.; Noda, K.; Miyoshi, E.; Block, T. Increased levels of tetra-antennary N-linked glycan but not core fucosylation are associated with hepatocellular carcinoma tissue Cancer Epidemiol., Biomarkers Prev. 2012, 21, 925-933
34. Frank, C. G.; Grubenmann, C. E.; Eyaid, W.; Berger, E. G.; Aebi, M.; Hennet, T. Identification and functional analysis of a defect in the human ALG9 gene: definition of congenital disorder of glycosylation type I L Am. J. Hum. Genet. 2004, 75, 146-150
35. Goldman, R.; Ressom, H. W.; Varghese, R. S.; Goldman, L.; Bascug, G.; Loffredo, C. A.; Abdel-Hamid, M.; Gouda, I.; Ezzat, S.; Kyselova, Z. Detection of hepatocellular carcinoma using glycomic analysis Clin. Cancer Res. 2009, 15, 1808-1813
36. Kyselova, Z.; Mechref, Y.; Kang, P.; Goetz, J. A.; Dobrolecki, L. E.; Sledge, G. W.; Schnaper, L.; Hickey, R. J.; Malkas, L. H.; Novotny, M. V. Breast cancer diagnosis and prognosis through quantitative measurements of serum glycan profiles Clin. Chem. 2008, 54, 1166-1175
37. Chandrasekaran, E. V.; Xue, J.; Xia, J.; Chawda, R.; Piskorz, C.; Locke, R. D.; Neelamegham, S.; Matta, K. L. Analysis of the specificity of sialyltransferases toward mucin core 2, globo, and related structures. identification of the sialylation sequence and the effects of sulfate, fucose, methyl, and fluoro substituents of the carbohydrate chain in the biosynthesis of selectin and siglec ligands, and novel sialylation by cloned alpha2,3(O)sialyltransferase Biochem. J. 2005, 44, 15619-15635
38. Chen, C. Y.; Jan, Y. H.; Juan, Y. H.; Yang, C. J.; Huang, M. S.; Yu, C. J.; Yang, P. C.; Hsiao, M.; Hsu, T. L.; Wong, C. H. Fucosyltransferase 8 as a functional regulator of nonsmall cell lung cancer Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 630-635
39. Gu, W.; Fukuda, T.; Isaji, T.; Hashimoto, H.; Wang, Y.; Gu, J. α1, 6-Fucosylation regulates neurite formation via the activin/phospho-Smad2 pathway in PC12 cells: the implicated dual effects of Fut8 for TGF-β/activin- mediated signaling FASEB. J. 2013, 27, 3947-3958
40. Bernardi, C.; Soffientini, U.; Piacente, F.; Tonetti, M. G. Effects of MicroRNAs on Fucosyltransferase 8 (FUT8) Expression in Hepatocarcinoma Cells PloS One 2013, 8, e76540
41. Silver, H. K.; Rangel, D. M.; Morton, D. L. Serum sialic acid elevations in malignant melanoma patients Cancer 1978, 41, 1497-1499
42. Kökoǧlu, E.; Sönmez, H.; Uslu, E.; Uslu, I. Sialic acid levels in various types of cancer Cancer Biochem. Biophys. 1992, 13, 57-64
43. Toyoda, M.; Ito, H.; Matsuno, Y. K.; Narimatsu, H.; Kameyama, A. Quantitative derivatization of sialic acids for the detection of sialoglycans by MALDI MS Anal. Chem. 2008, 80, 5211-5218
44. Frank, C. G.; Aebi, M. ALG9 mannosyltransferase is involved in two different steps of lipid-linked oligosaccharide biosynthesis Glycobiology 2005, 15, 1156-1163
45. Jaeken, J.; Matthijs, G. Congenital disorders of glycosylation: a rapidly expanding disease family Annu. Rev. Genomics Hum. Genet. 2007, 8, 261-278
46. Stanley, P. Biological consequences of overexpressing or eliminating N-acetylglucosaminyltransferase-TIII in the mouse Biochim. Biophys. Acta 2002, 1573, 363-368