Altered expression of sialylated glycoproteins in ovarian cancer sera using lectin-based ELISA assay and quantitative glycoproteomics analysis

Journal of Proteome Research

Volumn 12, Issue 7, 2013, Pages 3342-3352

  Wu, Jing ^a   Xie, Xiaolei ^b   Nie, Song ^a   Buckanovich, Ronald J ^a   Lubman, David M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Caprion Proteomics US   (United States)

Author keywords

biomarkers; glycoprotein; lectin based ELISA; mass spectrometry; ovarian cancer

Indexed keywords

CA 125 ANTIGEN; CLUSTERIN; COMPLEMENT FACTOR H; HEMOPEXIN; LECTIN; LEUCINE RICH ALPHA2 GLYCOPROTEIN; SIALOGLYCOPROTEIN; UNCLASSIFIED DRUG; VITAMIN D BINDING PROTEIN;

ADULT; AFFINITY CHROMATOGRAPHY; AGED; ARTICLE; CANCER STAGING; CHEMICAL LABELING; CONTROLLED STUDY; DOWN REGULATION; ENRICHMENT CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; OVARY CANCER; OVARY TUMOR; PERFORMANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEOMICS; SIALYLATION;

ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; LECTINS; OVARIAN NEOPLASMS; PROTEOMICS; ROC CURVE; TUMOR MARKERS, BIOLOGICAL;

SAMBUCUS NIGRA;

EID: 84879899584     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400169n     Document Type: Article

References (60)

1. Jemal, A.; Thomas, A.; Murray, T.; Thun, M. Cancer statistics, 2002 CA Cancer J. Clin. 2002, 52 (1) 23-47
2. Moore, R. G.; Miller, M. C.; Steinhoff, M. M.; Skates, S. J.; Lu, K. H.; Lambert-Messerlian, G.; Bast, R. C., Jr. Serum HE4 levels are less frequently elevated than CA125 in women with benign gynecologic disorders Am. J. Obstet. Gynecol. 2012, 206 (4) 351 e1-8
3. Zhang, Z.; Bast, R. C., Jr.; Yu, Y.; Li, J.; Sokoll, L. J.; Rai, A. J.; Rosenzweig, J. M.; Cameron, B.; Wang, Y. Y.; Meng, X. Y.; Berchuck, A.; Van Haaften-Day, C.; Hacker, N. F.; de Bruijn, H. W.; van der Zee, A. G.; Jacobs, I. J.; Fung, E. T.; Chan, D. W. Three biomarkers identified from serum proteomic analysis for the detection of early stage ovarian cancer Cancer Res. 2004, 64 (16) 5882-90
4. Hellstrom, I.; Raycraft, J.; Hayden-Ledbetter, M.; Ledbetter, J. A.; Schummer, M.; McIntosh, M.; Drescher, C.; Urban, N.; Hellstrom, K. E. The HE4 (WFDC2) protein is a biomarker for ovarian carcinoma Cancer Res. 2003, 63 (13) 3695-700
5. Gorelik, E.; Landsittel, D. P.; Marrangoni, A. M.; Modugno, F.; Velikokhatnaya, L.; Winans, M. T.; Bigbee, W. L.; Herberman, R. B.; Lokshin, A. E. Multiplexed immunobead-based cytokine profiling for early detection of ovarian cancer Cancer Epidemiol. Biomarkers Prev. 2005, 14 (4) 981-7
6. Visintin, I.; Feng, Z.; Longton, G.; Ward, D. C.; Alvero, A. B.; Lai, Y.; Tenthorey, J.; Leiser, A.; Flores-Saaib, R.; Yu, H.; Azori, M.; Rutherford, T.; Schwartz, P. E.; Mor, G. Diagnostic markers for early detection of ovarian cancer Clin. Cancer Res. 2008, 14 (4) 1065-72
7. Dieplinger, H.; Ankerst, D. P.; Burges, A.; Lenhard, M.; Lingenhel, A.; Fineder, L.; Buchner, H.; Stieber, P. Afamin and apolipoprotein A-IV: novel protein markers for ovarian cancer Cancer Epidemiol. Biomarkers Prev. 2009, 18 (4) 1127-33
8. Edgell, T.; Martin-Roussety, G.; Barker, G.; Autelitano, D. J.; Allen, D.; Grant, P.; Rice, G. E. Phase II biomarker trial of a multimarker diagnostic for ovarian cancer J. Cancer Res. Clin. Oncol. 2010, 136 (7) 1079-88
9. Moore, L. E.; Pfeiffer, R. M.; Zhang, Z.; Lu, K. H.; Fung, E. T.; Bast, R. C., Jr. Proteomic biomarkers in combination with CA 125 for detection of epithelial ovarian cancer using prediagnostic serum samples from the Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial Cancer 2012, 118 (1) 91-100
10. Yip, P.; Chen, T. H.; Seshaiah, P.; Stephen, L. L.; Michael-Ballard, K. L.; Mapes, J. P.; Mansfield, B. C.; Bertenshaw, G. P. Comprehensive serum profiling for the discovery of epithelial ovarian cancer biomarkers PLoS One 2011, 6 (12) e29533
11. Nolen, B. M.; Lokshin, A. E. Biomarker testing for ovarian cancer: clinical utility of multiplex assays Mol. Diagn. Ther. 2013, 17 (3) 139-46
12. Yurkovetsky, Z.; Skates, S.; Lomakin, A.; Nolen, B.; Pulsipher, T.; Modugno, F.; Marks, J.; Godwin, A.; Gorelik, E.; Jacobs, I.; Menon, U.; Lu, K.; Badgwell, D.; Bast, R. C., Jr.; Lokshin, A. E. Development of a multimarker assay for early detection of ovarian cancer J. Clin. Oncol. 2010, 28 (13) 2159-66
13. Kim, Y. W.; Bae, S. M.; Lim, H.; Kim, Y. J.; Ahn, W. S. Development of multiplexed bead-based immunoassays for the detection of early stage ovarian cancer using a combination of serum biomarkers PLoS One 2012, 7 (9) e44960
14. Tcherkassova, J.; Abramovich, C.; Moro, R.; Chen, C.; Schmit, R.; Gerber, A. Combination of CA125 and RECAF biomarkers for early detection of ovarian cancer Tumour Biol. 2011, 32 (4) 831-8
15. Zou, L.; He, X.; Zhang, J. W. The efficacy of YKL-40 and CA125 as biomarkers for epithelial ovarian cancer Braz. J. Med. Biol. Res. 2010, 43 (12) 1232-8
16. Lu, D.; Kuhn, E.; Bristow, R. E.; Giuntoli, R. L., 2nd; Kjaer, S. K.; Shih, Ie, M.; Roden, R. B. Comparison of candidate serologic markers for type I and type II ovarian cancer Gynecol. Oncol. 2011, 122 (3) 560-6
17. Rice, G. E.; Edgell, T. A.; Autelitano, D. J. Evaluation of midkine and anterior gradient 2 in a multimarker panel for the detection of ovarian cancer J. Exp. Clin. Cancer Res. 2010, 29, 62
18. Saldova, R.; Wormald, M. R.; Dwek, R. A.; Rudd, P. M. Glycosylation changes on serum glycoproteins in ovarian cancer may contribute to disease pathogenesis Dis. Markers 2008, 25 (4-5) 219-32
19. Reis, C. A.; Osorio, H.; Silva, L.; Gomes, C.; David, L. Alterations in glycosylation as biomarkers for cancer detection J. Clin. Pathol. 2010, 63 (4) 322-9
20. Turner, G. A.; Goodarzi, M. T.; Thompson, S. Glycosylation of alpha-1-proteinase inhibitor and haptoglobin in ovarian cancer: evidence for two different mechanisms Glycoconj. J. 1995, 12 (3) 211-8
21. Zhang, H.; Li, X. J.; Martin, D. B.; Aebersold, R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry Nat. Biotechnol. 2003, 21 (6) 660-6
22. Saldova, R.; Royle, L.; Radcliffe, C. M.; Abd Hamid, U. M.; Evans, R.; Arnold, J. N.; Banks, R. E.; Hutson, R.; Harvey, D. J.; Antrobus, R.; Petrescu, S. M.; Dwek, R. A.; Rudd, P. M. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG Glycobiology 2007, 17 (12) 1344-56
23. Ye, B.; Skates, S.; Mok, S. C.; Horick, N. K.; Rosenberg, H. F.; Vitonis, A.; Edwards, D.; Sluss, P.; Han, W. K.; Berkowitz, R. S.; Cramer, D. W. Proteomic-based discovery and characterization of glycosylated eosinophil-derived neurotoxin and COOH-terminal osteopontin fragments for ovarian cancer in urine Clin. Cancer Res. 2006, 12 (2) 432-41
24. Wu, J.; Xie, X.; Liu, Y.; He, J.; Benitez, R.; Buckanovich, R. J.; Lubman, D. M. Identification and confirmation of differentially expressed fucosylated glycoproteins in the serum of ovarian cancer patients using a lectin array and LC-MS/MS J. Proteome Res. 2012, 11 (9) 4541-52
25. Wu, J.; An, Y.; Pu, H.; Shan, Y.; Ren, X.; An, M.; Wang, Q.; Wei, S.; Ji, J. Enrichment of serum low-molecular-weight proteins using C18 absorbent under urea/dithiothreitol denatured environment Anal. Biochem. 2010, 398 (1) 34-44
26. Chiu, P. C.; Chung, M. K.; Koistinen, R.; Koistinen, H.; Seppala, M.; Ho, P. C.; Ng, E. H.; Lee, K. F.; Yeung, W. S. Cumulus oophorus-associated glycodelin-C displaces sperm-bound glycodelin-A and -F and stimulates spermatozoa-zona pellucida binding J. Biol. Chem. 2007, 282 (8) 5378-88
27. Wetprasit, N.; Chulavatnatol, M. Determination of sugar specificity of jackfruit lectin by a simple sugar-lectin binding assay using microtiter plate Biochem. Mol. Biol. Int. 1997, 42 (2) 399-408
28. 1-42 stimulated hippocampal astrocytes reveal that CXCL10 is involved in astrocyte migration J. Proteome Res. 2013, 12 (2) 832-43
29. Chen, S.; LaRoche, T.; Hamelinck, D.; Bergsma, D.; Brenner, D.; Simeone, D.; Brand, R. E.; Haab, B. B. Multiplexed analysis of glycan variation on native proteins captured by antibody microarrays Nat. Methods 2007, 4 (5) 437-44
30. Abraham, R.; Moller, D.; Gabel, D.; Senter, P.; Hellstrom, I.; Hellstrom, K. E. The influence of periodate oxidation on monoclonal antibody avidity and immunoreactivity J. Immunol. Methods 1991, 144 (1) 77-86
31. Wang, Y.; Wu, S. L.; Hancock, W. S. Approaches to the study of N-linked glycoproteins in human plasma using lectin affinity chromatography and nano-HPLC coupled to electrospray linear ion trap-Fourier transform mass spectrometry Glycobiology 2006, 16 (6) 514-23
32. Borges, C. R.; Jarvis, J. W.; Oran, P. E.; Nelson, R. W. Population studies of Vitamin D Binding Protein microheterogeneity by mass spectrometry lead to characterization of its genotype-dependent O-glycosylation patterns J. Proteome Res. 2008, 7 (9) 4143-53
33. Viau, M.; Constans, J.; Debray, H.; Montreuil, J. Isolation and characterization of the O-glycan chain of the human vitamin-D binding protein Biochem. Biophys. Res. Commun. 1983, 117 (1) 324-31
34. Kui Wong, N.; Easton, R. L.; Panico, M.; Sutton-Smith, M.; Morrison, J. C.; Lattanzio, F. A.; Morris, H. R.; Clark, G. F.; Dell, A.; Patankar, M. S. Characterization of the oligosaccharides associated with the human ovarian tumor marker CA125 J. Biol. Chem. 2003, 278 (31) 28619-34
35. Schauer, R. Achievements and challenges of sialic acid research Glycoconj. J. 2000, 17 (7-9) 485-99
36. Sawada, T.; Ho, J. J.; Sagabe, T.; Yoon, W. H.; Chung, Y. S.; Sowa, M.; Kim, Y. S. Biphasic effect of cell surface sialic acids on pancreatic cancer cell adhesiveness Biochem. Biophys. Res. Commun. 1993, 195 (2) 1096-103
37. Hakomori, S. Glycosylation defining cancer malignancy: new wine in an old bottle Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (16) 10231-3
38. Zhao, J.; Patwa, T. H.; Qiu, W.; Shedden, K.; Hinderer, R.; Misek, D. E.; Anderson, M. A.; Simeone, D. M.; Lubman, D. M. Glycoprotein microarrays with multi-lectin detection: unique lectin binding patterns as a tool for classifying normal, chronic pancreatitis and pancreatic cancer sera J. Proteome Res. 2007, 6 (5) 1864-74
39. Dall'Olio, F.; Malagolini, N.; di Stefano, G.; Minni, F.; Marrano, D.; Serafini-Cessi, F. Increased CMP-NeuAc:Gal beta 1,4GlcNAc-R alpha 2,6 sialyltransferase activity in human colorectal cancer tissues Int. J. Cancer 1989, 44 (3) 434-9
40. Kaneko, Y.; Yamamoto, H.; Kersey, D. S.; Colley, K. J.; Leestma, J. E.; Moskal, J. R. The expression of Gal beta 1,4GlcNAc alpha 2,6 sialyltransferase and alpha 2,6-linked sialoglycoconjugates in human brain tumors Acta Neuropathol. 1996, 91 (3) 284-92
41. Tian, Y.; Esteva, F. J.; Song, J.; Zhang, H. Altered expression of sialylated glycoproteins in breast cancer using hydrazide chemistry and mass spectrometry Mol. Cell. Proteomics 2012, 11 (6) M111 011403
42. Harduin-Lepers, A.; Krzewinski-Recchi, M. A.; Colomb, F.; Foulquier, F.; Groux-Degroote, S.; Delannoy, P. Sialyltransferases functions in cancers Front. Biosci. (Elite Ed.) 2012, 4, 499-515
43. Wang, P. H.; Lee, W. L.; Juang, C. M.; Yang, Y. H.; Lo, W. H.; Lai, C. R.; Hsieh, S. L.; Yuan, C. C. Altered mRNA expressions of sialyltransferases in ovarian cancers Gynecol. Oncol. 2005, 99 (3) 631-9
44. Takahashi, N.; Takahashi, Y.; Putnam, F. W. Periodicity of leucine and tandem repetition of a 24-amino acid segment in the primary structure of leucine-rich alpha 2-glycoprotein of human serum Proc. Natl. Acad. Sci. U.S.A. 1985, 82 (7) 1906-10
45. Yu, K. H.; Rustgi, A. K.; Blair, I. A. Characterization of proteins in human pancreatic cancer serum using differential gel electrophoresis and tandem mass spectrometry J. Proteome Res. 2005, 4 (5) 1742-51
46. Okano, T.; Kondo, T.; Kakisaka, T.; Fujii, K.; Yamada, M.; Kato, H.; Nishimura, T.; Gemma, A.; Kudoh, S.; Hirohashi, S. Plasma proteomics of lung cancer by a linkage of multi-dimensional liquid chromatography and two-dimensional difference gel electrophoresis Proteomics 2006, 6 (13) 3938-48
47. Kawakami, T.; Hoshida, Y.; Kanai, F.; Tanaka, Y.; Tateishi, K.; Ikenoue, T.; Obi, S.; Sato, S.; Teratani, T.; Shiina, S.; Kawabe, T.; Suzuki, T.; Hatano, N.; Taniguchi, H.; Omata, M. Proteomic analysis of sera from hepatocellular carcinoma patients after radiofrequency ablation treatment Proteomics 2005, 5 (16) 4287-95
48. Andersen, J. D.; Boylan, K. L.; Jemmerson, R.; Geller, M. A.; Misemer, B.; Harrington, K. M.; Weivoda, S.; Witthuhn, B. A.; Argenta, P.; Vogel, R. I.; Skubitz, A. P. Leucine-rich alpha-2-glycoprotein-1 is upregulated in sera and tumors of ovarian cancer patients J. Ovarian Res. 2010, 3, 21
49. Comunale, M. A.; Wang, M.; Rodemich-Betesh, L.; Hafner, J.; Lamontagne, A.; Klein, A.; Marrero, J.; Di Bisceglie, A. M.; Gish, R.; Block, T.; Mehta, A. Novel changes in glycosylation of serum Apo-J in patients with hepatocellular carcinoma Cancer Epidemiol. Biomarkers Prev. 2011, 20 (6) 1222-9
50. Shannan, B.; Seifert, M.; Boothman, D. A.; Tilgen, W.; Reichrath, J. Clusterin and DNA repair: a new function in cancer for a key player in apoptosis and cell cycle control J. Mol. Histol. 2006, 37 (5-7) 183-8
51. Wei, L.; Xue, T.; Wang, J.; Chen, B.; Lei, Y.; Huang, Y.; Wang, H.; Xin, X. Roles of clusterin in progression, chemoresistance and metastasis of human ovarian cancer Int. J. Cancer 2009, 125 (4) 791-806
52. Redondo, M.; Villar, E.; Torres-Munoz, J.; Tellez, T.; Morell, M.; Petito, C. K. Overexpression of clusterin in human breast carcinoma Am. J. Pathol. 2000, 157 (2) 393-9
53. Pucci, S.; Bonanno, E.; Pichiorri, F.; Angeloni, C.; Spagnoli, L. G. Modulation of different clusterin isoforms in human colon tumorigenesis Oncogene 2004, 23 (13) 2298-304
54. Albert, J. M.; Gonzalez, A.; Massion, P. P.; Chen, H.; Olson, S. J.; Shyr, Y.; Diaz, R.; Lambright, E. S.; Sandler, A.; Carbone, D. P.; Putnam, J. B., Jr.; Johnson, D. H.; Lu, B. Cytoplasmic clusterin expression is associated with longer survival in patients with resected non small cell lung cancer Cancer Epidemiol. Biomarkers Prev. 2007, 16 (9) 1845-51
55. July, L. V.; Akbari, M.; Zellweger, T.; Jones, E. C.; Goldenberg, S. L.; Gleave, M. E. Clusterin expression is significantly enhanced in prostate cancer cells following androgen withdrawal therapy Prostate 2002, 50 (3) 179-88
56. Zhang, L. Y.; Ying, W. T.; Mao, Y. S.; He, H. Z.; Liu, Y.; Wang, H. X.; Liu, F.; Wang, K.; Zhang, D. C.; Wang, Y.; Wu, M.; Qian, X. H.; Zhao, X. H. Loss of clusterin both in serum and tissue correlates with the tumorigenesis of esophageal squamous cell carcinoma via proteomics approaches World J. Gastroenterol. 2003, 9 (4) 650-4
57. Koch-Brandt, C.; Morgans, C. Clusterin: a role in cell survival in the face of apoptosis? Prog. Mol. Subcell Biol. 1996, 16, 130-49
58. Scaltriti, M.; Brausi, M.; Amorosi, A.; Caporali, A.; D'Arca, D.; Astancolle, S.; Corti, A.; Bettuzzi, S. Clusterin (SGP-2, ApoJ) expression is downregulated in low- and high-grade human prostate cancer Int. J. Cancer 2004, 108 (1) 23-30
59. Leskov, K. S.; Klokov, D. Y.; Li, J.; Kinsella, T. J.; Boothman, D. A. Synthesis and functional analyses of nuclear clusterin, a cell death protein J. Biol. Chem. 2003, 278 (13) 11590-600
60. Hassan, M. K.; Watari, H.; Han, Y.; Mitamura, T.; Hosaka, M.; Wang, L.; Tanaka, S.; Sakuragi, N. Clusterin is a potential molecular predictor for ovarian cancer patient's survival: targeting clusterin improves response to paclitaxel J. Exp. Clin. Cancer Res. 2011, 30, 113