Circulating autoantibodies to phosphorylated α-enolase are a hallmark of pancreatic cancer

Journal of Proteome Research

Volumn 10, Issue 1, 2011, Pages 105-112

  Tomaino, Barbara ^a,b   Cappello, Paola ^a,b   Capello, Michela ^a,b   Fredolini, Claudia ^a,b,h   Sperduti, Isabella ^c   Migliorini, Paola ^d   Salacone, Paola ^e   Novarino, Anna ^a   Giacobino, Alice ^a   Ciuffreda, Libero ^a   Alessio, Massimo ^f   Nisticò, Paola ^c   Scarpa, Aldo ^g   Pederzoli, Paolo ^g   Zhou, Weidong ^h   Petricoin III, Emanuel F ^h   Liotta, Lance A ^h   Giovarelli, Mirella ^a,b   Milella, Michele ^c   Novelli, Francesco ^a,b  

^a MOLINETTE HOSPITAL   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d UNIVERSITY OF PISA   (Italy)

^e Gastroenterology Unit   (Italy)

^f SAN RAFFAELE HOSPITAL   (Italy)

^g UNIVERSITY OF VERONA   (Italy)

^h GEORGE MASON UNIVERSITY   (United States)

Author keywords

Antibodies; Mass spectrometry; Pancreatic ductal adenocarcinoma; Serological proteome analysis; Tumor associated antigen; Two dimensional electrophoresis

Indexed keywords

ALPHA ENOLASE; ALPHA ENOLASE 1; ALPHA ENOLASE 2; ALPHA ENOLASE 3; ALPHA ENOLASE 4; ALPHA ENOLASE 5; ALPHA ENOLASE 6; ANTINEOPLASTIC AGENT; AUTOANTIBODY; CA 19-9 ANTIGEN; ISOENZYME; SERINE; UNCLASSIFIED DRUG;

ADULT; ADVANCED CANCER; AGED; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CANCER CELL CULTURE; CANCER PATIENT; CANCER TISSUE; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; ENZYME ISOLATION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, NEOPLASM; AUTOANTIBODIES; BLOTTING, WESTERN; CARCINOMA, PANCREATIC DUCTAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HUMANS; MALE; MIDDLE AGED; PANCREATIC NEOPLASMS; PHOSPHOPYRUVATE HYDRATASE; PHOSPHORYLATION; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTEIN ISOFORMS; ROC CURVE;

EID: 79951526292     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100213b     Document Type: Article

References (37)

1. Jemal, A.; Siegel, R.; Ward, E.; Hao, Y.; Xu, J.; Murray, T.; Thun, M. J. Cancer statistics, 2008. CA Cancer J. Clin. 2008, 58 (2), 71-96.
2. Omura, N.; Goggins, M. Epigenetics and epigenetic alterations in pancreatic cancer. Int. J. Clin. Exp. Pathol. 2009, 2 (4), 310-26.
3. Goggins, M. Molecular markers of early pancreatic cancer. J. Clin. Oncol. 2005, 23 (20), 4524-31. (Pubitemid 46196582)
4. Michl, P.; Pauls, S.; Gress, T. M. Evidence-based diagnosis and staging of pancreatic cancer. Best Pract. Res. Clin. Gastroenterol. 2006, 20 (2), 227-51.
5. Cappello, P.; Tomaino, B.; Chiarle, R.; Ceruti, P.; Novarino, A.; Castagnoli, C.; Migliorini, P.; Perconti, G.; Giallongo, A.; Milella, M.; Monsurro, V.; Barbi, S.; Scarpa, A.; Nistico, P.; Giovarelli, M.; Novelli, F. An integrated humoral and cellular response is elicited in pancreatic cancer by alpha-enolase, a novel pancreatic ductal adenocarcinoma-associated antigen. Int. J. Cancer 2009, 125 (3), 639-48.
6. Kuramitsu, Y.; Nakamura, K. Proteomic analysis of cancer tissues: shedding light on carcinogenesis and possible biomarkers. Proteomics 2006, 6 (20), 5650-61. (Pubitemid 44683228)
7. Lu, Z.; Hu, L.; Evers, S.; Chen, J.; Shen, Y. Differential expression profiling of human pancreatic adenocarcinoma and healthy pancreatic tissue. Proteomics 2004, 4 (12), 3975-88. (Pubitemid 39657472)
8. Chen, R.; Pan, S.; Brentnall, T. A.; Aebersold, R. Proteomic profiling of pancreatic cancer for biomarker discovery. Mol. Cell. Proteomics 2005, 4 (4), 523-33. (Pubitemid 40590569)
9. Mikuriya, K.; Kuramitsu, Y.; Ryozawa, S.; Fujimoto, M.; Mori, S.; Oka, M.; Hamano, K.; Okita, K.; Sakaida, I.; Nakamura, K. Expression of glycolytic enzymes is increased in pancreatic cancerous tissues as evidenced by proteomic profiling by two-dimensional electrophoresis and liquid chromatography-mass spectrometry/ mass spectrometry. Int. J. Oncol. 2007, 30 (4), 849-55.
10. Tu, S. H.; Chang, C. C.; Chen, C. S.; Tam, K. W.; Wang, Y. J.; Lee, C. H.; Lin, H. W.; Cheng, T. C.; Huang, C. S.; Chu, J. S.; Shih, N. Y.; Chen, L. C.; Leu, S. J.; Ho, Y. S.; Wu, C. H. Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells. Breast Cancer Res. Treat. 2010, 121, 539-53.
11. Sahin, U.; Tureci, O.; Pfreundschuh, M. Serological identification of human tumor antigens. Curr. Opin. Immunol. 1997, 9 (5), 709-16. (Pubitemid 27485301)
12. Harsha, H. C.; Kandasamy, K.; Ranganathan, P.; Rani, S.; Ramabadran, S.; Gollapudi, S.; Balakrishnan, L.; Dwivedi, S. B.; Telikicherla, D.; Selvan, L. D.; Goel, R.; Mathivanan, S.; Marimuthu, A.; Kashyap, M.; Vizza, R. F.; Mayer, R. J.; Decaprio, J. A.; Srivastava, S.; Hanash, S. M.; Hruban, R. H.; Pandey, A. A compendium of potential biomarkers of pancreatic cancer. PLoS Med. 2009, 6 (4), e1000046.
13. Tomaino, B.; Cappello, P.; Capello, M.; Fredolini, C.; Ponzetto, A.; Novarino, A.; Ciuffreda, L.; Bertetto, O.; Angelis, C. D.; Gaia, E.; Salacone, P.; Milella, M.; Nistico, P.; Alessio, M.; Chiarle, R.; Giuffrida, M. G.; Giovarelli, M.; Novelli, F. Autoantibody Signature in Human Ductal Pancreatic Adenocarcinoma. J. Proteome Res. 2007, 6, 4025-31. (Pubitemid 350032566)
14. Moscato, S.; Pratesi, F.; Sabbatini, A.; Chimenti, D.; Scavuzzo, M.; Passatino, R.; Bombardieri, S.; Giallongo, A.; Migliorini, P. Surface expression of a glycolytic enzyme, alpha-enolase, recognized by autoantibodies in connective tissue disorders. Eur. J. Immunol. 2000, 30 (12), 3575-84. (Pubitemid 32005230)
15. Shevchenko, A.; Jensen, O. N.; Podtelejnikov, A. V.; Sagliocco, F.; Wilm, M.; Vorm, O.; Mortensen, P.; Shevchenko, A.; Boucherie, H.; Mann, M. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. U.S.A. 1996, 93 (25), 14440-5. (Pubitemid 26418985)
16. Luchini, A.; Geho, D. H.; Bishop, B.; Tran, D.; Xia, C.; Dufour, R. L.; Jones, C. D.; Espina, V.; Patanarut, A.; Zhou, W.; Ross, M. M.; Tessitore, A.; Petricoin, E. F., 3rd; Liotta, L. A. Smart hydrogel particles: biomarker harvesting: one-step affinity purification, size exclusion, and protection against degradation. Nano Lett. 2008, 8 (1), 350-61. (Pubitemid 351177827)
17. Filsoufi, F.; Rahmanian, P. B.; Castillo, J. G.; Chikwe, J.; Adams, D. H. Logistic risk model predicting postoperative respiratory failure in patients undergoing valve surgery. Eur. J. Cardiothorac. Surg. 2008, 34 (5), 953-9.
18. Lemeshow, S.; Le Gall, J. R. Modeling the severity of illness of ICU patients. A systems update. J. Am. Med. Assoc. 1994, 272 (13), 1049-55. (Pubitemid 24294657)
19. Novelli, F.; Tomaino, B.; Cappello, P. Novel antigens and antibodies associated to pancreatic ductal adenocarcinoma. 2008, WO/2008/037792.
20. Yu, L. R.; Zhu, Z.; Chan, K. C.; Issaq, H. J.; Dimitrov, D. S.; Veenstra, T. D. Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J. Proteome Res. 2007, 6 (11), 4150-62. (Pubitemid 350158493)
21. Rush, J.; Moritz, A.; Lee, K. A.; Guo, A.; Goss, V. L.; Spek, E. J.; Zhang, H.; Zha, X. M.; Polakiewicz, R. D.; Comb, M. J. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23 (1), 94-101. (Pubitemid 41724631)
22. Rikova, K.; Guo, A.; Zeng, Q.; Possemato, A.; Yu, J.; Haack, H.; Nardone, J.; Lee, K.; Reeves, C.; Li, Y.; Hu, Y.; Tan, Z.; Stokes, M.; Sullivan, L.; Mitchell, J.; Wetzel, R.; Macneill, J.; Ren, J. M.; Yuan, J.; Bakalarski, C. E.; Villen, J.; Kornhauser, J. M.; Smith, B.; Li, D.; Zhou, X.; Gygi, S. P.; Gu, T. L.; Polakiewicz, R. D.; Rush, J.; Comb, M. J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131 (6), 1190-203. (Pubitemid 350235027)
23. Molina, H.; Horn, D. M.; Tang, N.; Mathivanan, S.; Pandey, A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (7), 2199-204. (Pubitemid 46391375)
24. Dephoure, N.; Zhou, C.; Villen, J.; Beausoleil, S. A.; Bakalarski, C. E.; Elledge, S. J.; Gygi, S. P. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (31), 10762-7.
25. Cavallo, F.; Calogero, R. A.; Forni, G. Are oncoantigens suitable targets for anti-tumour therapy. Nat. Rev. Cancer 2007, 7 (9), 707-13. (Pubitemid 47327413)
26. Yang, F.; Xiao, Z. Q.; Zhang, X. Z.; Li, C.; Zhang, P. F.; Li, M. Y.; Chen, Y.; Zhu, G. Q.; Sun, Y.; Liu, Y. F.; Chen, Z. C. Identification of tumor antigens in human lung squamous carcinoma by serological proteome analysis. J. Proteome Res. 2007, 6 (2), 751-8. (Pubitemid 46340178)
27. Li, C.; Xiao, Z.; Chen, Z.; Zhang, X.; Li, J.; Wu, X.; Li, X.; Yi, H.; Li, M.; Zhu, G.; Liang, S. Proteome analysis of human lung squamous carcinoma. Proteomics 2006, 6 (2), 547-58. (Pubitemid 43208034)
28. Nakanishi, T.; Takeuchi, T.; Ueda, K.; Murao, H.; Shimizu, A. Detection of eight antibodies in cancer patients' sera against proteins derived from the adenocarcinoma A549 cell line using proteomics-based analysis. J. Chromatogr., B: Analyt. Technol. Biomed. Life Sci. 2006, 838 (1), 15-20. (Pubitemid 43832210)
29. Cui, J. W.; Li, W. H.; Wang, J.; Li, A. L.; Li, H. Y.; Wang, H. X.; He, K.; Li, W.; Kang, L. H.; Yu, M.; Shen, B. F.; Wang, G. J.; Zhang, X. M. Proteomics-based identification of human acute leukemia antigens that induce humoral immune response. Mol. Cell. Proteomics 2005, 4 (11), 1718-24. (Pubitemid 41749265)
30. Almeras, L.; Lefranc, D.; Drobecq, H.; de Seze, J.; Dubucquoi, S.; Vermersch, P.; Prin, L. New antigenic candidates in multiple sclerosis: identification by serological proteome analysis. Proteomics 2004, 4 (7), 2184-94. (Pubitemid 38880382)
31. Riker, A.; Libutti, S. K.; Bartlett, D. L. Advances in the early detection, diagnosis, and staging of pancreatic cancer. Surg. Oncol. 1997, 6 (3), 157-69. (Pubitemid 28119140)
32. Gemmel, C.; Eickhoff, A.; Helmstadter, L.; Riemann, J. F. Pancreatic cancer screening: state of the art. Expert Rev. Gastroentero. Hepatol. 2009, 3 (1), 89-96.
33. Gelibter, A.; Malaguti, P.; Di Cosimo, S.; Bria, E.; Ruggeri, E. M.; Carlini, P.; Carboni, F.; Ettorre, G. M.; Pellicciotta, M.; Giannarelli, D.; Terzoli, E.; Cognetti, F.; Milella, M. Fixed dose-rate gemcitabine infusion as first-line treatment for advanced-stage carcinoma of the pancreas and biliary tree. Cancer 2005, 104 (6), 1237-45. (Pubitemid 41278959)
34. Yokoi, K.; Fidler, I. J. Hypoxia increases resistance of human pancreatic cancer cells to apoptosis induced by gemcitabine. Clin. Cancer Res. 2004, 10 (7), 2299-306. (Pubitemid 38445687)
35. Pancholi, V. Multifunctional alpha-enolase: its role in diseases. Cell. Mol. Life Sci. 2001, 58 (7), 902-20. (Pubitemid 32652817)
36. Laheru, D.; Jaffee, E. M. Immunotherapy for pancreatic cancer - science driving clinical progress. Nat. Rev. Cancer 2005, 5 (6), 459-67. (Pubitemid 40791488)
37. Sobin, L. H. UICC TNM classification of malignant tumors, 6th ed.; John Wiley and Sons: New York, 2002.