Spatiotemporal proteomic analyses during pancreas cancer progression identifies serine/threonine stress kinase 4 (STK4) as a novel candidate biomarker for early stage disease

Molecular and Cellular Proteomics

Volumn 13, Issue 12, 2014, Pages 3484-3496

  Mirus, Justin E ^a   Zhang, Yuzheng ^a   Hollingsworth, Michael A ^b   Solan, Joell L ^a   Lampe, Paul D ^a   Hingorani, Sunil R ^a,c  

^a USA   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTRANSFERASE; SERINE THREONINE STRESS KINASE 4; UNCLASSIFIED DRUG; ANTIBODY; CERULETIDE; PROTEIN SERINE THREONINE KINASE; PROTEOME; STK4 PROTEIN, MOUSE; TUMOR MARKER; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CHRONIC PANCREATITIS; CONTROLLED STUDY; EXPERIMENTAL MODEL; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; METASTASIS; MOUSE; NONHUMAN; PANCREAS; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREAS CANCER; PHYSICAL DISEASE BY BODY FUNCTION; PRIORITY JOURNAL; PROTEOMICS; SPATIOTEMPORAL ANALYSIS; SPATIOTEMPORAL PROTEOMIC ANALYSIS; UPREGULATION; ANIMAL; CARCINOMA, PANCREATIC DUCTAL; CHEMICALLY INDUCED; CHEMISTRY; DIFFERENTIAL DIAGNOSIS; DISEASE COURSE; DISEASE MODEL; EARLY DIAGNOSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PANCREATIC NEOPLASMS; PANCREATITIS, CHRONIC; PATHOLOGY; PROTEIN MICROARRAY; SIGNAL TRANSDUCTION; TIME;

MUS;

ANIMALS; ANTIBODIES; BIOMARKERS, TUMOR; CARCINOMA, PANCREATIC DUCTAL; CERULETIDE; DIAGNOSIS, DIFFERENTIAL; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EARLY DIAGNOSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MOLECULAR SEQUENCE ANNOTATION; NEOPLASM PROTEINS; PANCREATIC NEOPLASMS; PANCREATITIS, CHRONIC; PROTEIN ARRAY ANALYSIS; PROTEIN-SERINE-THREONINE KINASES; PROTEOME; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84928229458     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.036517     Document Type: Article

References (46)

1. American Cancer Society. Cancer Facts & Figures 2013. Atlanta: American Cancer Society; 2013.
2. Burris, H. A., 3rd, Moore, M. J., Andersen, J., Green, M. R., Rothenberg, M. L., Modiano, M. R., Cripps, M. C., Portenoy, R. K., Storniolo, A. M., Tarassoff, P., Nelson, R., Dorr, F. A., Stephens, C. D., and Von Hoff, D. D. (1997) Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. 15, 2403-2413
3. Ferrone, C. R., Pieretti-Vanmarcke, R., Bloom, J. P., Zheng, H., Szymonifka, J., Wargo, J. A., Thayer, S. P., Lauwers, G. Y., Deshpande, V., Mino-Kenudson, M., Fernandez-del Castillo, C., Lillemoe, K. D., and Warshaw, A. L. (2012) Pancreatic ductal adenocarcinoma: long-term survival does not equal cure. Surgery 152, S43-S49
4. Sener, S. F., Fremgen, A., Menck, H. R., and Winchester, D. P. (1999) Pancreatic cancer: a report of treatment and survival trends for 100,313 patients diagnosed from 1985-1995, using the National Cancer Database. J. Am. Coll. Surg. 189, 1-7
5. Kloppel, G., and Adsay, N. V. (2009) Chronic pancreatitis and the differential diagnosis versus pancreatic cancer. Arch. Pathol. Lab. Med. 133, 382-387
6. Decker, G. A., Batheja, M. J., Collins, J. M., Silva, A. C., Mekeel, K. L., Moss, A. A., Nguyen, C. C., Lake, D. F., and Miller, L. J. (2010) Risk factors for pancreatic adenocarcinoma and prospects for screening. Gastroenterol. Hepatol. 6, 246-254
7. Hingorani, S. R., Petricoin, E. F., Maitra, A., Rajapakse, V., King, C., Jacobetz, M. A., Ross, S., Conrads, T. P., Veenstra, T. D., Hitt, B. A., Kawaguchi, Y., Johann, D., Liotta, L. A., Crawford, H. C., Putt, M. E., Jacks, T., Wright, C. V., Hruban, R. H., Lowy, A. M., and Tuveson, D. A. (2003) Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4, 437-450
8. Hingorani, S. R., Wang, L., Multani, A. S., Combs, C., Deramaudt, T. B., Hruban, R. H., Rustgi, A. K., Chang, S., and Tuveson, D. A. (2005) Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7, 469-483
9. Bardeesy, N., Aguirre, A. J., Chu, G. C., Cheng, K. H., Lopez, L. V., Hezel, A. F., Feng, B., Brennan, C., Weissleder, R., Mahmood, U., Hanahan, D., Redston, M. S., Chin, L., and Depinho, R. A. (2006) Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc. Natl. Acad. Sci. U.S.A. 103, 5947-5952
10. Aguirre, A. J., Bardeesy, N., Sinha, M., Lopez, L., Tuveson, D. A., Horner, J., Redston, M. S., and DePinho, R. A. (2003) Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev. 17, 3112-3126
11. Izeradjene, K., Combs, C., Best, M., Gopinathan, A., Wagner, A., Grady, W. M., Deng, C. X., Hruban, R. H., Adsay, N. V., Tuveson, D. A., and Hingorani, S. R. (2007) Kras(G12D) and Smad4/Dpc4 haploinsufficiency cooperate to induce mucinous cystic neoplasms and invasive adenocarcinoma of the pancreas. Cancer Cell 11, 229-243
12. Gold, D. V., Karanjawala, Z., Modrak, D. E., Goldenberg, D. M., and Hruban, R. H. (2007) PAM4-reactive MUC1 is a biomarker for early pancreatic adenocarcinoma. Clin. Cancer Res. 13, 7380-7387
13. Bausch, D., Thomas, S., Mino-Kenudson, M., Fernandez-del, C. C., Bauer, T. W., Williams, M., Warshaw, A. L., Thayer, S. P., and Kelly, K. A. (2011) Plectin-1 as a novel biomarker for pancreatic cancer. Clin. Cancer Res. 17, 302-309
14. Faca, V. M., Song, K. S., Wang, H., Zhang, Q., Krasnoselsky, A. L., Newcomb, L. F., Plentz, R. R., Gurumurthy, S., Redston, M. S., Pitteri, S. J., Pereira-Faca, S. R., Ireton, R. C., Katayama, H., Glukhova, V., Phanstiel, D., Brenner, D. E., Anderson, M. A., Misek, D., Scholler, N., Urban, N. D., Barnett, M. J., Edelstein, C., Goodman, G. E., Thornquist, M. D., McIntosh, M. W., DePinho, R. A., Bardeesy, N., and Hanash, S. M. (2008) A mouse to human search for plasma proteome changes associated with pancreatic tumor development. PLoS Med. 5, e123
15. Rachagani, S., Torres, M. P., Kumar, S., Haridas, D., Baine, M., Macha, M. A., Kaur, S., Ponnusamy, M. P., Dey, P., Seshacharyulu, P., Johansson, S. L., Jain, M., Wagner, K. U., and Batra, S. K. (2012) Mucin (Muc) expression during pancreatic cancer progression in spontaneous mouse model: potential implications for diagnosis and therapy. J. Hematol. Oncol. 5, 68
16. Srivastava, S., and Srivastava, R. G. (2005) Proteomics in the forefront of cancer biomarker discovery. J. Proteome Res. 4, 1098-1103
17. Schroder, C., Jacob, A., Tonack, S., Radon, T. P., Sill, M., Zucknick, M., Ruffer, S., Costello, E., Neoptolemos, J. P., Crnogorac-Jurcevic, T., Bauer, A., Fellenberg, K., and Hoheisel, J. D. (2010) Dual-color proteomic profiling of complex samples with a microarray of 810 cancer-related antibodies. Mol. Cell. Proteomics 9, 1271-1280
18. Loch, C. M., Ramirez, A. B., Liu, Y., Sather, C. L., Delrow, J. J., Scholler, N., Garvik, B. M., Urban, N. D., McIntosh, M. W., and Lampe, P. D. (2007) Use of high density antibody arrays to validate and discover cancer serum biomarkers. Mol. Oncol. 1, 313-320
19. Anderson, N. L., and Anderson, N. G. (2002) The human plasma proteome: history, character, and diagnostic prospects. Mol. Cell. Proteomics 1, 845-867
20. Mischak, H., Apweiler, R., Banks, R. E., Conaway, M., Coon, J., Dominiczak, A., Ehrich, J. H., Fliser, D., Girolami, M., Hermjakob, H., Hochstrasser, D., Jankowski, J., Julian, B. A., Kolch, W., Massy, Z. A., Neusuess, C., Novak, J., Peter, K., Rossing, K., Schanstra, J., Semmes, O. J., Theodorescu, D., Thongboonkerd, V., Weissinger, E. M., Van Eyk, J. E., and Yamamoto, T. (2007) Clinical proteomics: a need to define the field and to begin to set adequate standards. Proteomics Clin. Appl. 1, 148-156
21. Ramirez, A. B., Loch, C. M., Zhang, Y., Liu, Y., Wang, X., Wayner, E. A., Sargent, J. E., Sibani, S., Hainsworth, E., Mendoza, E. A., Eugene, R., Labaer, J., Urban, N. D., McIntosh, M. W., and Lampe, P. D. (2010) Use of a single-chain antibody library for ovarian cancer biomarker discovery. Mol. Cell. Proteomics 9, 1449-1460
22. Li, C. I., Mirus, J. E., Zhang, Y., Ramirez, A. B., Ladd, J. J., Prentice, R. L., McIntosh, M. W., Hanash, S. M., and Lampe, P. D. (2012) Discovery and preliminary confirmation of novel early detection biomarkers for triplenegative breast cancer using preclinical plasma samples from the Women's Health Initiative observational study. Breast Cancer Res. Treat. 135, 611-618
23. Smyth, G. K., and Speed, T. (2003) Normalization of cDNA microarray data. Methods 31, 265-273
24. Smyth, G. K. (2005) Limma: Linear Models for Microarray Data, Springer, New York
25. Remmers, N., Anderson, J. M., Linde, E. M., DiMaio, D. J., Lazenby, A. J., Wandall, H. H., Mandel, U., Clausen, H., Yu, F., and Hollingsworth, M. A. (2013) Aberrant expression of mucin core proteins and o-linked glycans associated with progression of pancreatic cancer. Clin. Cancer Res. 19, 1981-1993
26. Rho, J. H., and Lampe, P. D. (2013) High-throughput screening for native autoantigen-autoantibody complexes using antibody microarrays. J. Proteome Res. 12, 2311-2320
27. 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., and Pandey, A. (2009) A compendium of potential biomarkers of pancreatic cancer. PLoS Med. 6, e1000046
28. Chen, R., Crispin, D. A., Pan, S., Hawley, S., McIntosh, M. W., May, D., Anton-Culver, H., Ziogas, A., Bronner, M. P., and Brentnall, T. A. (2010) Pilot study of blood biomarker candidates for detection of pancreatic cancer. Pancreas 39, 981-988
29. Strobel, O., Dor, Y., Stirman, A., Trainor, A., Fernandez-del Castillo, C., Warshaw, A. L., and Thayer, S. P. (2007) Beta cell transdifferentiation does not contribute to preneoplastic/metaplastic ductal lesions of the pancreas by genetic lineage tracing in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 4419-4424
30. Locker, G. Y., Hamilton, S., Harris, J., Jessup, J. M., Kemeny, N., Macdonald, J. S., Somerfield, M. R., Hayes, D. F., and Bast, R. C., Jr. (2006) ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J. Clin. Oncol. 24, 5313-5327
31. Tanaka, M., Shibahara, J., Fukushima, N., Shinozaki, A., Umeda, M., Ishikawa, S., Kokudo, N., and Fukayama, M. (2011) Claudin-18 is an early-stage marker of pancreatic carcinogenesis. J. Histochem. Cytochem. 59, 942-952
32. Fukuda, A., Wang, S. C., Morris, J. P. t., Folias, A. E., Liou, A., Kim, G. E., Akira, S., Boucher, K. M., Firpo, M. A., Mulvihill, S. J., and Hebrok, M. (2011) Stat3 and MMP7 contribute to pancreatic ductal adenocarcinoma initiation and progression. Cancer Cell 19, 441-455
33. Buchholz, M., Braun, M., Heidenblut, A., Kestler, H. A., Kloppel, G., Schmiegel, W., Hahn, S. A., Luttges, J., and Gress, T. M. (2005) Transcriptome analysis of microdissected pancreatic intraepithelial neoplastic lesions. Oncogene 24, 6626-6636
34. Hustinx, S. R., Cao, D., Maitra, A., Sato, N., Martin, S. T., Sudhir, D., Iacobuzio-Donahue, C., Cameron, J. L., Yeo, C. J., Kern, S. E., Goggins, M., Mollenhauer, J., Pandey, A., and Hruban, R. H. (2004) Differentially expressed genes in pancreatic ductal adenocarcinomas identified through serial analysis of gene expression. Cancer Biol. Ther. 3, 1254-1261
35. Cantile, M., Franco, R., Tschan, A., Baumhoer, D., Zlobec, I., Schiavo, G., Forte, I., Bihl, M., Liguori, G., Botti, G., Tornillo, L., Karamitopoulou-Diamantis, E., Terracciano, L., and Cillo, C. (2009) HOX D13 expression across 79 tumor tissue types. Int. J. Cancer 125, 1532-1541
36. Jhala, N., Jhala, D., Vickers, S. M., Eltoum, I., Batra, S. K., Manne, U., Eloubeidi, M., Jones, J. J., and Grizzle, W. E. (2006) Biomarkers in diagnosis of pancreatic carcinoma in fine-needle aspirates. Am. J. Clin. Pathol. 126, 572-579
37. Ludwig, E., Olson, S. H., Bayuga, S., Simon, J., Schattner, M. A., Gerdes, H., Allen, P. J., Jarnagin, W. R., and Kurtz, R. C. (2011) Feasibility and yield of screening in relatives from familial pancreatic cancer families. Am. J. Gastroenterol. 106, 946-954
38. Canto, M. I., Hruban, R. H., Fishman, E. K., Kamel, I. R., Schulick, R., Zhang, Z., Topazian, M., Takahashi, N., Fletcher, J., Petersen, G., Klein, A. P., Axilbund, J., Griffin, C., Syngal, S., Saltzman, J. R., Mortele, K. J., Lee, J., Tamm, E., Vikram, R., Bhosale, P., Margolis, D., Farrell, J., and Goggins, M. (2012) Frequent detection of pancreatic lesions in asymptomatic high-risk individuals. Gastroenterology 142, 796-804; quiz e714-e795
39. Schneiderhan, W., Diaz, F., Fundel, M., Zhou, S., Siech, M., Hasel, C., Moller, P., Gschwend, J. E., Seufferlein, T., Gress, T., Adler, G., and Bachem, M. G. (2007) Pancreatic stellate cells are an important source of MMP-2 in human pancreatic cancer and accelerate tumor progression in a murine xenograft model and CAM assay. J. Cell Sci. 120, 512-519
40. Mauviel, A., Nallet-Staub, F., and Varelas, X. (2012) Integrating developmental signals: a Hippo in the (path)way. Oncogene 31, 1743-1756
41. Uhlen, M., Oksvold, P., Fagerberg, L., Lundberg, E., Jonasson, K., Forsberg, M., Zwahlen, M., Kampf, C., Wester, K., Hober, S., Wernerus, H., Bjorling, L., and Ponten, F. (2010) Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248-1250
42. http://www.proteinatlas.org/ENSG00000101109/cancer/tissue/pancreatic+cancer
43. Yuan, F., Xie, Q., Wu, J., Bai, Y., Mao, B., Dong, Y., Bi, W., Ji, G., Tao, W., Wang, Y., and Yuan, Z. (2011) MST1 promotes apoptosis through regulating Sirt1-dependent p53 deacetylation. J. Biol. Chem. 286, 6940-6945
44. Diep, C. H., Zucker, K. M., Hostetter, G., Watanabe, A., Hu, C., Munoz, R. M., Von Hoff, D. D., and Han, H. (2012) Down-regulation of Yes Associated Protein 1 expression reduces cell proliferation and clonogenicity of pancreatic cancer cells. PLoS One 7, e32783
45. George, N. M., Day, C. E., Boerner, B. P., Johnson, R. L., and Sarvetnick, N. E. (2012) Hippo signaling regulates pancreas development through inactivation of Yap. Mol. Cell. Biol. 32, 5116-5128
46. Gao, T., Zhou, D., Yang, C., Singh, T., Penzo-Mendez, A., Maddipati, R., Tzatsos, A., Bardeesy, N., Avruch, J., and Stanger, B. Z. (2013) Hippo signaling regulates differentiation and maintenance in the exocrine pancreas. Gastroenterology 144, 1543-1553