N-glycosylation of colorectal cancer tissues: A liquid chromatography and mass spectrometry-based investigation

Molecular and Cellular Proteomics

Volumn 11, Issue 9, 2012, Pages 571-585

  Balog, Crina I A ^a   Stavenhagen, Kathrin ^a   Fung, Wesley L J ^a   Koeleman, Carolien A ^a   McDonnell, Liam A ^a   Verhoeven, Aswin ^a   Mesker, Wilma E ^a   Tollenaar, Rob A E M ^a   Deelder, André M ^a   Wuhrer, Manfred ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRANILIC ACID; EPITOPE; GLYCAN;

ADULT; AGED; ARTICLE; CANCER TISSUE; CLINICAL ARTICLE; COLON; COLORECTAL CANCER; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME PURIFICATION; ENZYME RELEASE; FEMALE; FLUORESCENCE; GLYCOSYLATION; HUMAN; HUMAN TISSUE; HYDROPHILIC INTERACTION CHROMATOGRAPHY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PARTIAL LEAST SQUARES REGRESSION; PREDICTION; PRIORITY JOURNAL;

ADULT; AGED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLORECTAL NEOPLASMS; FEMALE; GLYCOSYLATION; HUMANS; MALE; MANNOSE; MIDDLE AGED; POLYSACCHARIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUMOR MARKERS, BIOLOGICAL;

EID: 84864378010     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.011601     Document Type: Article

References (71)

1. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Murray, T., and Thun, M. J. (2008) Cancer statistics. CA-Cancer J. Clin. 58, 71-96
2. Davies, R. J., Miller, R., and Coleman, N. (2005) Colorectal cancer screening: Prospects for molecular stool analysis. Nat. Rev. Cancer 5, 199-209
3. Levin, B., Brooks, D., Smith, R. A., and Stone, A. (2003) Emerging technologies in screening for colorectal cancer: CT colonography, immunochemical fecal occult blood tests, and stool screening using molecular markers. CA-Cancer J. Clin. 53, 44-55
4. Terdiman, J. P. (2005) Colonoscopy is superior to flexible sigmoidoscopy for colorectal cancer screening: Now beyond a reasonable doubt? Gastroenterology 129, 1793-1794
5. Nakazato, M., Yamano, H., Matsushita, H., Sato, K., Fujita, K., Yamanaka, Y., and Imai, Y. (2006) Immunologic fecal occult blood test for colorectal cancer screening. Jpn. Med. Assoc. J. 49, 203-207
6. Saussez, S., Marchant, H., Nagy, N., Decaestecker, C., Hassid, S., Jortay, A., Schüring, M. P., Gabius, H. J., Danguy, A., Salmon, I., and Kiss, R. (1998) Quantitative glycohistochemistry defines new prognostic markers for cancers of the oral cavity. Cancer 82, 252-260
7. Turner, G. A. (1992) N-Glycosylation of serum proteins in disease and its investigation using lectins. Clin. Chim. Acta 208, 149-171
8. Hakomori, S. I. (1989) Aberrant glycosylation in tumors and tumor-associated carbohydrate antigens. Adv. Cancer Res. 52, 257-331
9. Hakomori, S. (2001) Tumor-associated carbohydrate antigens defining tumor malignancy: Basis for development of anti-cancer vaccines. Adv. Exp. Med. Biol. 491, 369-402
10. An, H. J., Kronewitter, S. R., de Leoz, M. L., and Lebrilla, C. B. (2009) Glycomics and disease markers. Curr. Opin. Chem. Biol. 13, 601-607
11. Chandrasekaran, E. V., Xue, J., Neelamegham, S., and Matta, K. L. (2006) The pattern of glycosyl- and sulfotransferase activities in cancer cell lines: A predictor of individual cancer-associated distinct carbohydrate structures for the structural identification of signature glycans. Carbohydr. Res. 341, 983-994
12. Szajda, S. D., Snarska, J., Puchalski, Z., and Zwierz, K. (2008) Lysosomal exoglycosidases in serum and urine of patients with colon adenocarcinoma. Hepatogastroenterology 55, 921-925
13. Arnold, J. N., Saldova, R., Galligan, M. C., Murphy, T. B., Mimura-Kimura, Y., Telford, J. E., Godwin, A. K., and Rudd, P. M. (2011) Novel glycan biomarkers for the detection of lung cancer. J. Proteome Res. 10, 1755-1764
14. Abd Hamid, U. M., Royle, L., Saldova, R., Radcliffe, C. M., Harvey, D. J., Storr, S. J., Pardo, M., Antrobus, R., Chapman, C. J., Zitzmann, N., Robertson, J. F., Dwek, R. A., and Rudd, P. M. (2008) A strategy to reveal potential glycan markers from serum glycoproteins associated with breast cancer progression. Glycobiology 18, 1105-1118
15. de Leoz, M. L., Young, L. J., An, H. J., Kronewitter, S. R., Kim, J., Miyamoto, S., Borowsky, A. D., Chew, H. K., and Lebrilla, C. B. (2011) High-mannose glycans are elevated during breast cancer progression. Mol. Cell. Proteomics 10, 10.1074/mcp.M110.002717
16. Arnold, J. N., Saldova, R., Hamid, U. M., and Rudd, P. M. (2008) Evaluation of the serum N-linked glycome for the diagnosis of cancer and chronic inflammation. Proteomics 8, 3284-3293
17. 1-Acid glycoprotein fucosylation as a marker ofcarcinoma progression and prognosis. Cancer 101, 2825-2836
18. x predict multilevel N2 disease in non-small-cell lung cancer. Ann. Surg. Oncol. 13, 1010-1018
19. x and cytokeratin 19 fragment as predictive factors for recurrence in patients with stage I non-small cell lung cancer. Lung Cancer 58, 369-375
20. Gu, J., Sato, Y., Kariya, Y., Isaji, T., Taniguchi, N., and Fukuda, T. (2009) A mutual regulation between cell-cell adhesion and N-glycosylation: Implication of the bisecting GlcNAc for biological functions. J. Proteome Res. 8, 431-435
21. Li, M., Song, L., and Qin, X. (2010) Glycan changes: Cancer metastasis and anti-cancer vaccines. J. Biosci. 35, 665-673
22. Vercoutter-Edouart, A. S., Slomianny, M. C., Dekeyzer-Beseme, O., Haeuw, J. F., and Michalski, J. C. (2008) Glycoproteomics and glycomics investigation of membrane N-glycosylproteins from human colon carcinoma cells. Proteomics 8, 3236-3256
23. Qiu, Y., Patwa, T. H., Xu, L., Shedden, K., Misek, D. E., Tuck, M., Jin, G., Ruffin, M. T., Turgeon, D. K., Synal, S., Bresalier, R., Marcon, N., Brenner, D. E., and Lubman, D. M. (2008) Plasma glycoprotein profiling for colorectal cancer biomarker identification by lectin glycoarray and lectin blot. J. Proteome Res. 7, 1693-1703
24. Ahn, Y. H., Kim, Y. S., Ji, E. S., Lee, J. Y., Jung, J. A., Ko, J. H., and Yoo, J. S. (2010) Comparative quantitation of aberrant glycoforms by lectinbased glycoprotein enrichment coupled with multiple-reaction monitoring mass spectrometry. Anal. Chem. 82, 4441-4447
25. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70
26. Friedman, D. B., Hill, S., Keller, J. W., Merchant, N. B., Levy, S. E., Coffey, R. J., and Caprioli, R. M. (2004) Proteome analysis of human colon cancer by two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics 4, 793-811
27. Ma, Y., Peng, J., Liu, W., Zhang, P., Huang, L., Gao, B., Shen, T., Zhou, Y., Chen, H., Chu, Z., Zhang, M., and Qin, H. (2009) Proteomics identification of desmin as a potential oncofetal diagnostic and prognostic biomarker in colorectal cancer. Mol. Cell. Proteomics 8, 1878-1890
28. Contessa, J. N., Bhojani, M. S., Freeze, H. H., Ross, B. D., Rehemtulla, A., and Lawrence, T. S. (2010) Molecular imaging of N-linked glycosylation suggests glycan biosynthesis is a novel target for cancer therapy. Clin. Cancer Res. 16, 3205-3214
29. nd Ed., pp. 580-670, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
30. Dierssen, J. W., de Miranda, N. F., Ferrone, S., van, P. M., Cornelisse, C. J., Fleuren, G. J., van, W. T., and Morreau, H. (2007) HNPCC versus sporadic microsatellite-unstable colon cancers follow different routes toward loss of HLA class I expression. BMC Cancer 7, 33
31. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
32. Wuhrer, M., Koeleman, C. A., Deelder, A. M., and Hokke, C. H. (2006) Repeats of LacdiNAc and fucosylated LacdiNAc on N-glycans of the human parasite Schistosoma mansoni. FEBS J. 273, 347-361
33. Ruhaak, L. R., Steenvoorden, E., Koeleman, C. A., Deelder, A. M., and Wuhrer, M. (2010) 2-picoline-borane: A non-toxic reducing agent for oligosaccharide labeling by reductive amination. Proteomics. 10, 2330-2336
34. Selman, M. H., Hemayatkar, M., Deelder, A. M., and Wuhrer, M. (2011) Cotton HILIC SPE microtips for microscale purification and enrichment of glycans and glycopeptides. Anal. Chem. 83, 2492-2499
35. Eriksson, L., Johansson, E., Kettaneh-Wold, N., Trygg, J., Wikstrom, C., and Wold, S. (2006) Multi- and Megavariate Data Analysis: Part I. Basic Principles and Applications, 2nd Ed., Umetrics Academy, Umea, Sweden.
36. Swets, J. A. (1988) Measuring the accuracy of diagnostic systems. Science 240, 1285-1293
37. A, and sialyl Tn antigens in colorectal cancer patients: Multivariate analysis of predictive factors for serum antigen levels. J. Gastroenterol. 36, 166-172
38. A as a new prognostic factor for patients with advanced colorectal-carcinoma. Cancer 75, 2051-2056
39. Yoshimura, M., Nishikawa, A., Ihara, Y., Taniguchi, S., and Taniguchi, N. (1995) Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase-III gene transfection. Proc. Natl. Acad. Sci. U.S.A. 92, 8754-8758
40. Schachter, H. (1986) Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem. Cell Biol. 64, 163-181
41. Yoshimura, M., Ihara, Y., Ohnishi, A., Ijuhin, N., Nishiura, T., Kanakura, Y., Matsuzawa, Y., and Taniguchi, N. (1996) Bisecting N-acetylglucosamine on K562 cells suppresses natural killer cytotoxicity and promotes spleen colonization. Cancer Res. 56, 412-418
42. Song, Y., Aglipay, J. A., Bernstein, J. D., Goswami, S., and Stanley, P. (2010) The bisecting GlcNAc on N-glycans inhibits growth factor signaling and retards mammary tumor progression. Cancer Res. 70, 3361-3371
43. Shimono, R., Mori, M., Akazawa, K., Adachi, Y., and Sgimachi, K. (1994) Immunohistochemical expression of carbohydrate antigen 19-9 in colo-rectal- carcinoma. Am. J. Gastroenterol. 89, 101-105
44. Ugorski, M., and Laskowska, A. (2002) Sialyl LewisA: A tumor-associated carbohydrate antigen involved in adhesion and metastatic potential of cancer cells. Acta Biochim. Pol. 49, 303-311
45. Yamori, T., Kimura, H., Stewart, K., Ota, D. M., Cleary, K. R., and Irimura, T. (1987) Differential production of high molecular weight sulfated glycoproteins in normal colonic mucosa, primary colon carcinoma, and metastases. Cancer Res. 47, 2741-2747
46. Yamori, T., Ota, D. M., Cleary, K. R., Hoff, S., Hager, L. G., and Irimura, T. (1989) Monoclonal antibody against human colonic sulfomucin: Immunochemical detection of its binding sites in colonic mucosa, colorectal primary carcinoma, and metastases. Cancer Res. 49, 887-894
47. Capon, C., Wieruszeski, J. M., Lemoine, J., Byrd, J. C., Leffler, H., and Kim, Y. S. (1997) Sulfated Lewis X determinants as a major structural motif in glycans from LS174T-HM7 human colon carcinoma mucin. J. Biol. Chem. 272, 31957-31968
48. Chandrasekaran, E. V., Xue, J., Piskorz, C., Locke, R. D., Tóth, K., Slocum, H. K., and Matta, K. L. (2007) Potential tumor markers for human gastric cancer: An elevation of glycan:sulfotransferases and a concomitant loss of α1,2-fucosyltransferase activities. J. Cancer Res. Clin. Oncol. 133, 599-611
49. Brockhausen, I., and Kuhns, W. (1997) Role and metabolism of glycoconjugate sulfation. Trends Glycosci. Glycotechnol. 9, 379-398
50. Horlacher, T., Oberli, M. A., Werz, D. B., Kröck, L., Bufali, S., Mishra, R., Sobek, J., Simons, K., Hirashima, M., Niki, T., and Seeberger, P. H. (2010) Determination of carbohydrate-binding preferences of human galectins with carbohydrate microarrays. Chembiochem. 11, 1563-1573
51. Hittelet, A., Legendre, H., Nagy, N., Bronckart, Y., Pector, J. C., Salmon, I., Yeaton, P., Gabius, H. J., Kiss, R., and Camby, I. (2003) Upregulation of galectins-1 and-3 in human colon cancer and their role in regulating cell migration. Int. J. Cancer 103, 370-379
52. Hashii, N., Kawasaki, N., Itoh, S., Nakajima, Y., Kawanishi, T., and Yamaguchi, T. (2009) Alteration of N-glycosylation in the kidney in a mouse model of systemic lupus erythematosus: Relative quantification of Nglycans using an isotope-tagging method. Immunology 126, 336-345
53. Joosten, C. E., Cohen, L. S., Ritter, G., Batt, C. A., and Shuler, M. L. (2004) Glycosylation profiles of the human colorectal cancer A33 antigen naturally expressed in the human colorectal cancer cell line SW1222 and expressed as recombinant protein in different insect cell lines. Biotechnol. Prog. 20, 1273-1279
54. Bosmann, H. B., and Hall, T. C. (1974) Enzyme activity in invasive tumors of human breast and colon. Proc. Natl. Acad. Sci. U.S.A. 71, 1833-1837
55. Gil-Martín, E., Rodríguez-Berrocal, J., Páez de la Cadena, M., and Fernán-dez-Briera, A. (1997) Alterations of glycosidases in human colonic adenocarcinoma. Clin. Biochem. 30, 17-25
56. Plucinsky, M. C., Prorok, J. J., and Alhadeff, J. A. (1986) β-Hexosaminidase from colon and sera of dukes-classified colorectal cancer patients: Activity levels, isozyme patterns, and kinetic properties. J. Natl. Cancer Inst. 77, 57-62
57. Szajda, S. D., Snarska, J., Jankowska, A., Puchalski, Z., and Zwierz, K. (2008) Isoenzymes A and B of N-acetyl-β-D-hexosaminidase in serum and urine of patients with pancreatic cancer. Hepatogastroenterology 55, 695-698
58. Szajda, S. D., Borzym-Kluczyk, M., Snarska, J., Puchalski, Z., and Zwierz, K. (2009) N-Acetyl-β-D-hexosaminidase and its isoenzymes A and B in blood serum and urine, as a potential colon cancer markers. Hepatogastroenterology 56, 1287-1298
59. Hoja-Lukowicz, D., Ciolczyk, D., Bergquist, J., Lityńska, A., and Laidler, P. (2000) High-mannose-type oligosaccharides from human placental arylsulfatase A are core fucosylated as confirmed by MALDI MS. Glycobiology 10, 551-557
60. Schwarz, P. M., and Elbein, A. D. (1985) The effect of glycoprotein-processing inhibitors on fucosylation of glycoproteins. J. Biol. Chem. 260, 14452-14458
61. Voynow, J. A., Kaiser, R. S., Scanlin, T. F., and Glick, M. C. (1991) Purification and characterization of GDP-L-fucose-N-acetyl β-D- glucosaminide α1-6-fucosyltransferase from cultured human skin fibroblasts: Requirement of a specific biantennary oligosaccharide as substrate. J. Biol. Chem. 266, 21572-21577
62. Crispin, M., Aricescu, A. R., Chang, V. T., Jones, E. Y., Stuart, D. I., Dwek, R. A., Davis, S. J., and Harvey, D. J. (2007) Disruption of α-mannosidase processing induces non-canonical hybrid-type glycosylation. FEBS Lett. 581, 1963-1968
63. Rabouille, C., Hui, N., Hunte, F., Kieckbusch, R., Berger, E. G., Warren, G., and Nilsson, T. (1995) Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108, 1617-1627
64. Velasco, A., Hendricks, L., Moremen, K. W., Tulsiani, D. R., Touster, O., and Farquhar, M. G. (1993) Cell type-dependent variations in the subcellular distribution of α-mannosidase I and II. J. Cell Biol. 122, 39-51
65. Magner, J. A., Novak, W., and Papagiannes, E. (1986) Subcellular localization of fucose incorporation into mouse thyrotropin and free α-subunits: Studies employing subcellular fractionation and inhibitors of the intracellular translocation of proteins. Endocrinology 119, 1315-1328
66. Peracaula, R., Barrabés, S., Sarrats, A., Rudd, P. M., and de Llorens, R. (2008) Altered glycosylation in tumours focused to cancer diagnosis. Dis. Markers 25, 207-218
67. Kyselova, Z., Mechref, Y., Al Bataineh, M. M., Dobrolecki, L. E., Hickey, R. J., Vinson, J., Sweeney, C. J., and Novotny, M. V. (2007) Alterations in the serum glycome due to metastatic prostate cancer. J. Proteome Res. 6, 1822-1832
68. Saldova, R., Fan, Y., Fitzpatrick, J. M., Watson, R. W., and Rudd, P. M. (2011) Core fucosylation and α2-3 sialylation in serum N-glycome is significantly increased in prostate cancer comparing to benign prostate hyperplasia. Glycobiology 21, 195-205
69. Ito, Y., Miyauchi, A., Yoshida, H., Uruno, T., Nakano, K., Takamura, Y., Miya, A., Kobayashi, K., Yokozawa, T., Matsuzuka, F., Taniguchi, N., Matsuura, N., Kuma, K., and Miyoshi, E. (2003) Expression of α1,6-fucosyltransferase (FUT8) in papillary carcinoma of the thyroid: Its linkage to biological aggressiveness and anaplastic transformation. Cancer Lett. 200, 167-172
70. Tabarés, G., Radcliffe, C. M., Barrabés, S., Ramírez, M., Aleixandre, R. N., Hoesel, W., Dwek, R. A., Rudd, P. M., Peracaula, R., and de Llorens, R. (2006) Different glycan structures in prostate-specific antigen from prostate cancer sera in relation to seminal plasma PSA. Glycobiology 16, 132-145
71. Wuhrer, M., Koeleman, C. A., Hokke, C. H., and Deelder, A. M. (2006) Mass spectrometry of proton adducts of fucosylated N-glycans: Fucose transfer between antennae gives rise to misleading fragments. Rapid Commun. Mass Spectrom. 20, 1747-1754