Polymorphonuclear neutrophils promote dyshesion of tumor cells and elastase-mediated degradation of E-cadherin in pancreatic tumors

European Journal of Immunology

Volumn 42, Issue 12, 2012, Pages 3369-3380

  Gaida, Matthias M ^a   Steffen, Thomas Große ^a   Günther, Frank ^b   Tschaharganeh, Darjus F ^a   Felix, Klaus ^a   Bergmann, Frank ^a   Schirmacher, Peter ^a   Hänsch, Gertrud M ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

E cadherin; Invasion; Pancreatic cancer; PMN elastase; Polymorphonuclear neutrophils

Indexed keywords

ELASTASE; SMALL INTERFERING RNA; UVOMORULIN;

ADULT; AGED; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CANCER PATIENT; CANCER PROGNOSIS; CELL ADHESION; CELL FUNCTION; CELL GROWTH; CELL MIGRATION; CLINICAL ASSESSMENT; CONTROLLED STUDY; DISEASE SEVERITY; DYSHESION; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MEDIATOR; MONOLAYER CULTURE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; PANCREAS ADENOCARCINOMA; PANCREAS BIOPSY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; TISSUE SECTION; TUMOR CELL; TUMOR GROWTH;

ADULT; AGED; AGED, 80 AND OVER; CADHERINS; CARCINOMA, PANCREATIC DUCTAL; CELL ADHESION; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEUKOCYTE ELASTASE; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEUTROPHIL INFILTRATION; NEUTROPHILS; PANCREATIC NEOPLASMS; PROTEOLYSIS;

EID: 84871335586     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242628     Document Type: Article

References (42)

1. Jemal, A., Siegel, R., Xu, J. and Ward, E., Cancer statistics, 2010. CA Cancer J. Clin. 2010. 60: 277-300.
2. Warshaw, A. L. and Fernandez-del Castillo, C., Pancreatic carcinoma. N. Engl. J. Med. 1992. 326: 455-465.
3. Kleeff, J., Beckhove, P., Esposito, I., Herzig, S., Huber, P. E., Lohr, J. M. and Friess, H., Pancreatic cancer microenvironment. Int. J. Cancer 2007. 121: 699-705.
4. De Monte, L., Reni, M., Tassi, E., Clavenna, D., Papa, I., Recalde, H., Braga, M.et al., Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J. Exp. Med. 2011. 208: 469-478.
5. Gaida, M. M., Bach, S. T., Gunther, F., Baseras, B., Tschaharganeh, D. F., Welsch, T., Felix, K. et al., Expression of Galectin-3 in pancreatic ductal adenocarcinoma. Pathol. Oncol. Res. 2011. 18: 299-307.
6. Khayyata, S., Basturk, O. and Adsay, N. V., Invasive micropapillary carcinomas of the ampullo-pancreatobiliary region and their association with tumor-infiltrating neutrophils. Mod. Pathol. 2005. 18: 1504-1511.
7. Reid, M. D., Basturk, O., Thirabanjasak, D., Hruban, R. H., Klimstra, D. S., Bagci, P., Altinel, D. et al., Tumor-infiltrating neutrophils in pancreatic neoplasia. Mod. Pathol. 2011. 24: 1612-1619.
8. Welsch, T., Kleeff, J. and Friess, H., Molecular pathogenesis of pancreatic cancer: advances and challenges. Curr. Mol. Med. 2007. 7: 504-521.
9. Greer, J. B. and Whitcomb, D. C., Inflammation and pancreatic cancer: an evidence-based review. Curr. Opin. Pharmacol. 2009. 9: 411-418.
10. di Carlo, E., Iezzi, M., Pannellini, T., Zaccardi, F., Modesti, A., Forni, G. and Musiani, P., Neutrophils in anti-cancer immunological strategies: old players in new games. J. Hematother. Stem. Cell Res. 2001. 10: 739-748.
11. Kindzelskii, A. L. and Petty, H. R., Early membrane rupture events during neutrophil-mediated antibody-dependent tumor cell cytolysis. J. Immunol. 1999. 162: 3188-3192.
12. Aeed, P. A., Nakajima, M. and Welch, D. R., The role of polymorphonuclear leukocytes (PMN) on the growth and metastatic potential of 13762NF mammary adenocarcinoma cells. Int. J. Cancer 1988. 42: 748-759.
13. Welch, D. R., Schissel, D. J., Howrey, R. P. and Aeed, P. A., Tumor-elicited polymorphonuclear cells, in contrast to "normal" circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells. Proc. Natl. Acad. Sci. USA 1989. 86: 5859-5863.
14. Li, Q., Fukuda, K., Lu, Y., Nakamura, Y., Chikama, T., Kumagai, N. and Nishida, T., Enhancement by neutrophils of collagen degradation by corneal fibroblasts. J. Leukoc. Biol. 2003. 74: 412-419.
15. Marzano, A. V., Cugno, M., Trevisan, V., Lazzari, R., Fanoni, D., Berti, E. and Crosti, C., Inflammatory cells, cytokines and matrix metalloproteinases in amicrobial pustulosis of the folds and other neutrophilic dermatoses. Int. J. Immunopathol. Pharmacol. 2011. 24: 451-460.
16. Borregaard, N., Neutrophils, from marrow to microbes. Immunity 2010. 33: 657-670.
17. Ito, T., Ito, M., Shiozawa, J., Naito, S., Kanematsu, T. and Sekine, I., Expression of the MMP-1 in human pancreatic carcinoma: relationship with prognostic factor. Mod. Pathol. 1999. 12: 669-674.
18. Bramhall, S. R., Neoptolemos, J. P., Stamp, G. W. and Lemoine, N. R., Imbalance of expression of matrix metalloproteinases (MMPs) and tissue inhibitors of the matrix metalloproteinases (TIMPs) in human pancreatic carcinoma. J. Pathol. 1997. 182: 347-355.
19. Nagakawa, Y., Aoki, T., Kasuya, K., Tsuchida, A. and Koyanagi, Y., Histologic features of venous invasion, expression of vascular endothelial growth factor and matrix metalloproteinase-2 and matrix metalloproteinase-9, and the relation with liver metastasis in pancreatic cancer. Pancreas 2002. 24: 169-178.
20. Mayerle, J., Schnekenburger, J., Kruger, B., Kellermann, J., Ruthenburger, M., Weiss, F. U., Nalli, A. et al., Extracellular cleavage of E-cadherin by leukocyte elastase during acute experimental pancreatitis in rats. Gastroenterology 2005. 129: 1251-1267.
21. Mantovani, A., Cassatella, M. A., Costantini, C. and Jaillon, S., Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 2011. 11: 519-531.
22. Cassatella, M. A., Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 1999. 73: 369-509.
23. Owen, C. A., Campbell, M. A., Sannes, P. L., Boukedes, S. S. and Campbell, E. J., Cell surface-bound elastase and cathepsin G on human neutrophils: a novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteinases. J. Cell Biol. 1995. 131: 775-789.
24. Morcos, M., Zimmermann, F., Radsak, M., Worner, I., Kramer, M. D., Roland, J., Hansch, G. M. et al., Autoantibodies to polymorphonuclear neutrophil elastase do not inhibit but enhance elastase activity. Am. J. Kidney Dis. 1998. 31: 978-985.
25. Hirohashi, S. and Kanai, Y., Cell adhesion system and human cancer morphogenesis. Cancer Sci. 2003. 94: 575-581.
26. Cavallaro, U. and Christofori, G., Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat. Rev. Cancer 2004. 4: 118-132.
27. Zemans, R. L., Briones, N., Campbell, M., McClendon, J., Young, S. K., Suzuki, T., Yang, I. V. et al., Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc. Natl. Acad. Sci. USA 2011. 108: 15990-15995.
28. Wada, Y., Yoshida, K., Tsutani, Y., Shigematsu, H., Oeda, M., Sanada, Y., Suzuki, T. et al., Neutrophil elastase induces cell proliferation and migration by the release of TGF-alpha, PDGF and VEGF in esophageal cell lines. Oncol. Rep. 2007. 17: 161-167.
29. Li, Y. J. and Ji, X. R., Relationship between expression of E-cadherin-catenin complex and clinicopathologic characteristics of pancreatic cancer. World J. Gastroenterol. 2003. 9: 368-372.
30. Erkan, M., Reiser-Erkan, C., Michalski, C. W. and Kleeff, J., Tumor microenvironment and progression of pancreatic cancer. Exp. Oncol. 2010. 32: 128-131.
31. Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh, R., Gysemans, C., Beschin, A., De Baetselier, P. et al., Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008. 111: 4233-4244.
32. Zhao, J. J., Pan, K., Wang, W., Chen, J. G., Wu, Y. H., Lv, L., Li, J. J. et al., The prognostic value of tumor-infiltrating neutrophils in gastric adenocarcinoma after resection. PLoS ONE 2012. 7: e33655.
33. Gaida, M. M., Gunther, F., Wagner, C., Friess, H., Giese, N. A., Schmidt, J., Hansch, G. M. et al., Expression of the CXCR6 on polymorphonuclear neutrophils in pancreatic carcinoma and in acute, localized bacterial infections. Clin. Exp. Immunol. 2008. 154: 216-223.
34. Wiedow, O., Muhle, K., Streit, V. and Kameyoshi, Y., Human eosinophils lack human leukocyte elastase. Biochim. Biophys Acta. 1996. 1315: 185-187.
35. Jiang, G., Cao, F., Ren, G., Gao, D., Bhakta, V., Zhang, Y., Cao, H. et al., PRSS3 promotes tumour growth and metastasis of human pancreatic cancer. Gut 2010. 59: 1535-1544.
36. von Burstin, J., Eser, S., Paul, M. C., Seidler, B., Brandl, M., Messer, M., von Werder, A. et al., E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/1ΧAΔH/HDAC2 repressor complex. Gastroenterology 2009. 137: 361-371, 371, e361-e365.
37. Hong, S. M., Li, A., Olino, K., Wolfgang, C. L., Herman, J. M., Schulick, R. D., Iacobuzio-Donahue, C. et al., Loss of E-cadherin expression and outcome among patients with resectable pancreatic adenocarcinomas. Mod. Pathol. 2011. 24: 1237-1247.
38. Bosman, F. T., Carneiro, F., Hruban, R. H. and Theise, N. D. (Eds.), World Health Organisation classification of tumours. Pathology and genetics of tumours of the digestive system. IARC Press, Lyon, 2010.
39. Sobin, L. H., Gospodarowicz, M. G. and Wittekind, C., TNM classification of malignant tumours. John Wiley & Sons, Oxford, 2009.
40. Gaida, M. M., Welsch, T., Herpel, E., Tschaharganeh, D. F., Fischer, L., Schirmacher, P., Hansch, G. M. et al., MHC class II expression in pancreatic tumors: a link to intratumoral inflammation. Virchows Arch. 2012. 460: 47-60.
41. Ceyhan, G. O., Bergmann, F., Kadihasanoglu, M., Erkan, M., Park, W., Hinz, U., Giese, T. et al., The neurotrophic factor artemin influences the extent of neural damage and growth in chronic pancreatitis. Gut 2007. 56: 534-544.
42. Al-Aynati, M. M., Radulovich, N., Riddell, R. H. and Tsao, M. S., Epithelial-cadherin and beta-catenin expression changes in pancreatic intraepithelial neoplasia. Clin. Cancer Res. 2004. 10: 1235-1240.