Mesothelin binding to CA125/MUC16 promotes pancreatic cancer cell motility and invasion via MMP-7 activation

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Chen, Shih Hsun ^a,b   Hung, Wei Chien ^a,b   Wang, Pu ^c   Paul, Colin ^a,b   Konstantopoulos, Konstantinos ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NORTHEASTERN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CA 125 ANTIGEN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MATRILYSIN; MEMBRANE PROTEIN; MESOTHELIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MMP7 PROTEIN, HUMAN; MUC16 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ADENOCARCINOMA; ARTICLE; CELL MOTION; CELL PROLIFERATION; CHEMISTRY; ENZYME ACTIVATION; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HUMAN; IMMUNOPRECIPITATION; METABOLISM; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; TUMOR INVASION; WESTERN BLOTTING;

ADENOCARCINOMA; BLOTTING, WESTERN; CA-125 ANTIGEN; CARCINOMA, PANCREATIC DUCTAL; CELL MOVEMENT; CELL PROLIFERATION; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GPI-LINKED PROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MATRIX METALLOPROTEINASE 7; MEMBRANE PROTEINS; NEOPLASM INVASIVENESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 84878623168     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep01870     Document Type: Article

References (50)

1. Chang, K. & Pastan, I. Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci U S A 93, 136-40 (1996). (Pubitemid 26041483)
2. Argani, P. et al. Mesothelin is overexpressed in the vast majority of ductal adenocarcinomas of the pancreas: identification of a new pancreatic cancer marker by serial analysis of gene expression (SAGE). Clin Cancer Res 7, 3862-8 (2001). (Pubitemid 34044602)
3. Hassan, R. et al. Mesothelin is overexpressed in pancreaticobiliary adenocarcinomas but not in normal pancreas and chronic pancreatitis. Am J Clin Pathol 124, 838-45 (2005). (Pubitemid 41740183)
4. Huang, C. Y. et al. Serum mesothelin in epithelial ovarian carcinoma: a new screening marker and prognostic factor. Anticancer Res 26, 4721-8 (2006).
5. Johnston, F. M. et al. Circulating mesothelin protein and cellular antimesothelin immunity in patients with pancreatic cancer. Clin Cancer Res 15, 6511-8 (2009).
6. Li, M. et al. Mesothelin is a malignant factor and therapeutic vaccine target for pancreatic cancer. Mol Cancer Ther 7, 286-96 (2008). (Pubitemid 351302523)
7. Chang, M. C. et al. Mesothelin enhances invasion of ovarian cancer by inducing MMP-7 through MAPK/ERK and JNK pathways. Biochem J442, 293-302(2012).
8. Servais, E. L. et al. Mesothelin overexpression promotes mesothelioma cell invasion and MMP-9 secretion in an orthotopic mouse model and in epithelioid pleural mesothelioma patients. Clin Cancer Res 18, 2478-89 (2012).
9. Wang, K. et al. Inhibition of mesothelin as a novel strategy for targeting cancer cells. PLoS One 7, e33214 (2012).
10. Rump, A. et al. Binding of ovarian cancer antigen CA125/MUC16 to mesothelin mediates cell adhesion. J Biol Chem 279, 9190-8 (2004). (Pubitemid 38295982)
11. Gubbels, J. A. et al. Mesothelin-MUC16 binding is a high affinity, N-glycan dependent interaction that facilitates peritoneal metastasis of ovarian tumors. Mol Cancer 5, 50 (2006).
12. Kaneko, O. et al. A binding domain on mesothelin for CA125/MUC16. J Biol Chem 284, 3739-49 (2009).
13. O'Brien, T. J. et al. The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 22, 348-66 (2001). (Pubitemid 34062947)
14. Kui Wong, N. et al. Characterization of the oligosaccharides associated with the human ovarian tumor marker CA125. J Biol Chem 278, 28619-34 (2003).
15. Streppel, M. M. et al. Mucin 16 (cancer antigen 125) expression in human tissues and cell lines and correlation with clinical outcome in adenocarcinomas of the pancreas, esophagus, stomach, and colon. Hum Pathol 43, 1755-63 (2012).
16. Haridas, D. et al. Pathobiological implications of MUC16 expression in pancreatic cancer. PLoS One 6, e26839 (2011).
17. Markman, M., Federico, M., Liu, P. Y., Hannigan, E. & Alberts, D. Significance of early changes in the serum CA-125 antigen level on overall survival in advanced ovarian cancer. Gynecol Oncol 103, 195-8 (2006). (Pubitemid 44389869)
18. Bast, R. C., Jr. et al. CA 125: the past and the future. Int J Biol Markers 13, 179-87 (1998).
19. Shimizu, A. et al. Coexpression of MUC16 and mesothelin is related to the invasion process in pancreatic ductal adenocarcinoma. Cancer Sci 103, 739-46 (2012).
20. Einama, T. et al. Co-expression of mesothelin and CA125 correlates with unfavorable patient outcome in pancreatic ductal adenocarcinoma. Pancreas 40, 1276-82 (2011).
21. Yamamoto, H. et al. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human pancreatic adenocarcinomas: clinicopathologic and prognostic significance of matrilysin expression. J Clin Oncol 19, 1118-27 (2001). (Pubitemid 32176289)
22. Bloomston, M., Zervos, E. E. & Rosemurgy, A. S., 2nd. Matrix metalloproteinases and their role in pancreatic cancer: a review of preclinical studies and clinical trials. Ann Surg Oncol 9, 668-74 (2002). (Pubitemid 34857984)
23. Gress, T. M. et al. Expression and in-situ localization of genes coding for extracellular matrix proteins and extracellular matrix degrading proteases in pancreatic cancer. Int J Cancer 62, 407-13 (1995).
24. Crawford, H. C., Scoggins, C. R., Washington, M. K., Matrisian, L. M. & Leach, S. D. Matrix metalloproteinase-7 is expressed by pancreatic cancer precursors and regulates acinar-to-ductal metaplasia in exocrine pancreas. J Clin Invest 109, 1437-44 (2002). (Pubitemid 34596169)
25. Fukushima, H. et al. Association of matrilysin mRNA expression with K-ras mutations and progression in pancreatic ductal adenocarcinomas. Carcinogenesis 22, 1049-52 (2001). (Pubitemid 32633603)
26. Jones, L. E., Humphreys, M. J., Campbell, F., Neoptolemos, J. P. & Boyd, M. T. Comprehensive analysis of matrix metalloproteinase and tissue inhibitor expression in pancreatic cancer: increased expression of matrix metalloproteinase-7 predicts poor survival. Clin Cancer Res 10, 2832-45 (2004). (Pubitemid 38509163)
27. Chen, S. H., Dallas, M. R., Balzer, E. M. & Konstantopoulos, K. Mucin 16 is a functional selectin ligand on pancreatic cancer cells. FASEB J 26, 1349-59 (2012).
28. Balzer, E. M. et al. Physical confinement alters tumor cell adhesion and migration phenotypes. FASEB J 26, 4045-56 (2012).
29. Tong, Z. et al. Chemotaxis of cell populations through confined spaces at single-cell resolution. PLoS One 7, e29211 (2012).
30. Veit, C. et al. Activation of phosphatidylinositol 3-kinase and extracellular signalregulated kinase is required for glial cell line-derived neurotrophic factor-induced migration and invasion of pancreatic carcinoma cells. Cancer Res 64, 5291-300 (2004). (Pubitemid 39006549)
31. Singh, A. K. et al. p38beta MAP kinase as a therapeutic target for pancreatic cancer. Chem Biol Drug Des 80, 266-73 (2012).
32. Cwik, G., Wallner, G., Skoczylas, T., Ciechanski, A. & Zinkiewicz, K. Cancer antigens 19-9 and 125 in the differential diagnosis of pancreatic mass lesions. Arch Surg 141, 968-73; discussion 974 (2006). (Pubitemid 44583251)
33. Sato, N. et al. Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 63, 4158-66 (2003). (Pubitemid 36917941)
34. Hucl, T. et al. High cancer-specific expression of mesothelin (MSLN) is attributable to an upstream enhancer containing a transcription enhancer factor dependent MCAT motif. Cancer Res 67, 9055-65 (2007). (Pubitemid 47535890)
35. Sternlicht, M. D. & Werb, Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17, 463-516 (2001). (Pubitemid 33096184)
36. Friedl, P. & Alexander, S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147, 992-1009 (2011).
37. Remy, L., Trespeuch, C., Bachy, S., Scoazec, J. Y. & Rousselle, P. Matrilysin 1 influences colon carcinoma cell migration by cleavage of the laminin-5 beta3 chain. Cancer Res 66, 11228-37 (2006). (Pubitemid 46009951)
38. Wroblewski, L. E. et al. Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J Cell Sci 116, 3017-26 (2003). (Pubitemid 36926990)
39. Tan, X. et al. Involvement of matrix metalloproteinase-7 in invasion-metastasis through induction of cell dissociation in pancreatic cancer. Int J Oncol 26, 1283-9 (2005).
40. Jones, S. et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321, 1801-6 (2008).
41. Dallas, M. R. et al. Sialofucosylated podocalyxin is a functional E-and L-selectin ligand expressed by metastatic pancreatic cancer cells. Am J Physiol Cell Physiol 303, C616-24 (2012).
42. Thomas, S. N., Zhu, F., Schnaar, R. L., Alves, C. S. & Konstantopoulos, K. Carcinoembryonic antigen and CD44 variant isoforms cooperate to mediate colon carcinoma cell adhesion to E-and L-selectin in shear flow. J Biol Chem 283, 15647-55 (2008).
43. Burdick, M. M. & Konstantopoulos, K. Platelet-induced enhancement of LS174T colon carcinoma and THP-1 monocytoid cell adhesion to vascular endothelium under flow. Am J Physiol Cell Physiol 287, C539-47 (2004).
44. McCarty, O. J., Jadhav, S., Burdick, M. M., Bell, W. R. & Konstantopoulos, K. Fluid shear regulates the kinetics and molecular mechanisms of activation-dependent platelet binding to colon carcinoma cells. Biophys J 83, 836-48 (2002). (Pubitemid 34803620)
45. Wang, P., Zhu, F., Tong, Z. & Konstantopoulos, K. Response of chondrocytes to shear stress: antagonistic effects of the binding partners Toll-like receptor 4 and caveolin-1. Faseb J 25, 3401-15 (2011).
46. Zhu, F., Wang, P., Kontrogianni-Konstantopoulos, A. & Konstantopoulos, K. Prostaglandin (PG)D(2) and 15-deoxy-Delta(12, 14)-PGJ(2), but not PGE(2), mediate shear-induced chondrocyte apoptosis via protein kinase A-dependent regulation of polo-like kinases. Cell Death Differ 17, 1325-34 (2010).
47. Thomas, S. N., Schnaar, R. L. & Konstantopoulos, K. Podocalyxin-like protein is an E-/L-selectin ligand on colon carcinoma cells: comparative biochemical properties of selectin ligands in host and tumor cells. Am J Physiol Cell Physiol 296, C505-13 (2009).
48. Hanley, W. D. et al. Variant isoforms of CD44 are P-and L-selectin ligands on colon carcinoma cells. FASEB J 20, 337-9 (2006). (Pubitemid 46671163)
49. Napier, S. L., Healy, Z. R., Schnaar, R. L. & Konstantopoulos, K. Selectin ligand expression regulates the initial vascular interactions of colon carcinoma cells: the roles of CD44v and alternative sialofucosylated selectin ligands. J Biol Chem 282, 3433-41 (2007). (Pubitemid 47084453)
50. Wang, P., Zhu, F. & Konstantopoulos, K. Interleukin-6 synthesis in human chondrocytes is regulated via the antagonistic actions of prostaglandin (PG)E2 and 15-deoxy-Delta(12, 14)-PGJ2. PLoS One 6, e27630 (2011).