Tumor-derived trypsin enhances proliferation of intrahepatic cholangiocarcinoma cells by activating protease-activated receptor-2

International Journal of Oncology

Volumn 36, Issue 4, 2010, Pages 793-800

  Nakanuma, Shin Ichi ^a   Tajima, Hidehiro ^a   Okamoto, Kouichi ^a   Hayashi, Hironori ^a   Nakagawara, Hisatoshi ^a   Onishi, Ichiro ^a   Takamura, Hiroyuki ^a   Kitagawa, Hirohisa ^a   Fushida, Sachio ^a   Tani, Takashi ^a   Fujimura, Takashi ^a   Kayahara, Masato ^a   Ohta, Tetsuo ^a   Wakayama, Tomohiko ^a   Iseki, Shoichi ^a   Harada, Shin Ichi ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

Gabexate mesilate; Hepatocellular carcinoma; Intrahepatic cholangiocarcinoma; Protease activated receptor 2; Trypsin; Trypsinogen

Indexed keywords

GABEXATE MESILATE; MESSENGER RNA; PROTEINASE ACTIVATED RECEPTOR 2; TRYPSIN; TRYPSINOGEN;

ADULT; AGED; ARTICLE; BILE DUCT CARCINOMA; CANCER CELL CULTURE; CELL ACTIVITY; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; ENZYME ANALYSIS; ENZYME RELEASE; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; MALE; PRIORITY JOURNAL; PROTEIN SECRETION; WESTERN BLOTTING; ZYMOGRAPHY;

ADULT; AGED; AGED, 80 AND OVER; BILE DUCT NEOPLASMS; BILE DUCTS, INTRAHEPATIC; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CHOLANGIOCARCINOMA; CULTURE MEDIA, SERUM-FREE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FIBROBLASTS; GABEXATE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; RECEPTOR, PAR-2; RNA, MESSENGER; SERINE PROTEINASE INHIBITORS; TRYPSIN;

EID: 77749313041     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000555     Document Type: Article

References (45)

1. The Liver Cancer Study Group of Japan: Primary liver cancer in Japan: Clinicopathologic features and results of surgical treatment. Ann Surg 211: 277-287, 1990.
2. Ohtsuka M, Ito H, Kimura F, et al: Results of surgical treatment for intrahepatic cholangiocarcinoma and clinicopathological factors influencing survival. Br J Surg 89: 1525-1531, 2002.
3. Morimoto Y, Tanaka Y, Ito T, et al: Long-term survival and prognostic factors in the surgical treatment for intrahepatic cholangiocarcinoma. J Hepatobiliary Pancreat Surg 10: 432-440, 2003.
4. Khan SA, Thomas HC, Davidson BR and Taylor-Robinson SD: Cholangiocarcinoma. Lancet 366: 1303-1314, 2005.
5. Ikai I, Itai Y, Okita K, et al: Report of the 15th follow-up survey of primary liver cancer. Hepatol Res 28: 21-29, 2004.
6. Colombari R and Tsui WM: Biliary tumors of liver. Semi Liver Dis 15: 402-413, 1995.
7. Nakanuma Y, Sripa B and Vatanasapt V: Pathology and genetics tumours of the digestive system. In: Intrahepatic cholangio-carcinoma. Hamilton SR and Aaltonen LA (eds). WHO Press, Geneva, pp173-180, 2000.
8. Ohta T, Tajima H, Fushida S, et al: Cationic trypsinogen produced by human pancreatic ductal cancer has the characteristics of spontaneous activation and gelatinolytic activity in the presence of proton. Int J Mol Med 1: 689-92, 1998.
9. Koivunen E, Saksela O, Itkonen O, et al: Human colon carcinoma, fibrosarcoma and leukemia cell lines produce tumor-associated trypsinogen. Int J Cancer 47: 592-596, 1991.
10. Koshikawa N, Yasumitsu H, Umeda M and Miyazaki K: Multiple secretion of matrix serine proteinases by human gastric carcinoma cell lines. Cancer Res 52: 5046-5053, 1992.
11. Ohta T, Terada T, Nagakawa H, et al: Pancreatic trypsinogen and cathepsin B in human pancreatic carcinomas and associated metastatic lesions. Br J Cancer 69: 152-156, 1994.
12. Otha T, Terada T, Nagakawa H, et al: Differential expression of pancreatic trypsinogen and cathepsin B in human scirrhous-type and intestinal-type gastric cancer. Oncol Rep 1: 203-208, 1994.
13. Kawano N, Osawa H, Ito T, et al: Expression of gelatinase A, tissue inhibitor of metalloproteinases-2, matrilysin, and trypsin(ogen) in lung neoplasms: an immunohistochemical study. Hum Pathol 28: 613-622, 1997.
14. Koshikawa N, Yasumitsu H, Nagashima Y, Umeda M and Miyazaki K: Identification of one- and two-chain forms of trypsinogen 1 produced by a human gastric adenocarcinoma cell line. Biochem J 303: 187-190, 1994.
15. Figarella C, Miszczuk-Jamska B and Barett AJ: Possible lysosomal activation of pancreatic zymogens. Activation of both human trypsinogens by cathepsin B and spontaneous acid. Activation of human trypsinogen 1. Biol Chem Hoppe Seyler 369 (Suppl): 293-298, 1998.
16. Tajima H, Ohta T, Elnemr A, et al: Enhanced invasiveness of pancreatic adenocarcinoma cells stably transfected with cationic trypsinogen cDNA. Int J Cancer 94: 699-704, 2001.
17. Ohta T, Futagami F, Arakawa H, et al: Inhibitory effect of a serine protease inhibitor, FOY-305, on the invasion and metastasis of human pancreatic cancers. Int J Oncol 11: 813-817, 1997.
18. Nystedt S, Emilsson K, Larsson AK, Strombeck B and Sundelin J: Molecular cloning and functional expression of the gene encoding the human proteinase-activated receptor 2. Eur J Biochem 232: 84-89, 1995.
19. Bohm SK, Kong W, Bromme D, et al: Molecular cloning: expression and potential functions of the human proteinase-activated receptor-2. Biochem J 314: 1009-1016, 1996.
20. Fox MT, Harriott P, Walker B and Stone SR: Identification of potential activators of proteinase-activated receptor-2. FEBS Lett 417: 267-269, 1997.
21. Déry O, Corvera CU, Steinhoff M and Bunnett NW: Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am J Physiol 274: 1429-1452, 1998.
22. Miyata S, Koshikawa N, Yasumitsu H and Miyazaki K: Trypsin stimulates integrin alpha(5)beta(1)-dependent adhesion to fibronectin and proliferation of human gastric carcinoma cells through activation of proteinase-activated receptor-2. J Biol Chem 275: 4592-4598, 2000.
23. Darmoul D, Gratio V, Devaud H and Laburthe M: Protease-activated receptor 2 in colon cancer: trypsin-induced MAPK phosphorylation and cell proliferation are mediated by epidermal growth factor receptor transactivation. J Biol Chem 279: 20927-20934, 2004.
24. Ohta T, Shimizu K, Yi S, et al: Protease-activated receptor-2 expression and the role of trypsin in cell proliferation in human pancreatic cancers. Int J Oncol 23: 61-66, 2003.
25. Matej R, Mandakova P, Netikova I, Pouckova P and Olejar T: Proteinase-activated receptor-2 expression in breast cancer and the role of trypsin on growth and metabolism of breast cancer cell line MDA MB-231. Physiol Res 56: 475-484, 2007.
26. Sánchez-Hernández PE, Ramirez-Dueñas MG, Albarran-Somoza B, et al: Protease-activated receptor-2 (PAR-2) in cervical cancer proliferation. Gynecol Oncol 108: 19-26, 2008.
27. Jikuhara A, Yoshii M, Iwagaki H, Mori S, Nishibori M and Tanaka N: MAP kinase-mediated proliferation of DLD-1 carcinoma by the stimulation of protease-activated receptor 2. Life Sci 73: 2817-2829, 2003.
28. Terada T, Ohta T, Minato H and Nakanuma Y: Expression of pancreatic trypsinogen/trypsin and cathepsin B in human cholangiocarcinomas and hepatocellular carcinomas. Hum Pathol 26: 746-752, 1995.
29. Liver Cancer Study Group of Japan: The General Rules for the Clinical and Pathological Study of Primary Liver Cancer. 4th edition, Kanehara, pp20-21, 2000 (In Japanese).
30. Wakayama T, Sai Y, Ito A, et al: Heterophilic binding of the adhesion molecules poliovirus receptor and immunoglobulin superfamily 4A in the interaction between mouse spermatogenic and Sertoli cells. Biol Reprod 76: 1081-1090, 2007.
31. Chomczynski P and Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol chloroform extraction. Anal Biochem 162: 156-159, 1987.
32. Emi M, Nakamura Y, Ogawa M, et al: Cloning, characterization and nucleotide sequences of two cDNAs encoding human pancreatic trypsinogens. Gene 41: 305-310, 1986.
33. Yasumitu H, Miyazaki K, Umenishi F, et al: Comparison of extracelluar matrix-degrading activities between 64-kDa and 90-kDa gelatinases purified in inhibitor-free forms from human schwanoma cells. J Biochem 111: 74-80, 1992.
34. Tanriverdi-Akhisaroglu S, Menderes A and Oktay G: Matrix metalloproteinase-2 and -9 activities in human keloids, hypertrophic and atrophic scars: a pilot study. Cell Biochem Funct 27: 81-87, 2009.
35. Yoon W, Jung Y, Kim T, et al: Gabexate mesilate inhibits colon cancer growth, invasion, and metastasis by reducing matrix metalloproteinases and angiogenesis. Clin Cancer Res 10: 4517-4526, 2004.
36. Uchima Y, Sawada T and Hirakawa K: Action of antiproteases on pancreatic cancer cells. JOP 8 (Suppl 4): 479-487, 2007.
37. Lempinen M, Isoniemi H, Mäkisalo H, et al: Enhanced detection of cholangiocarcinoma with serum trypsinogen-2 in patients with severe bile duct strictures. J Hepatol 47: 677-683, 2007.
38. Chung LW: The role of stromal-epithelial interaction in normal and malignant growth. Cancer Surv 23: 33-42, 1995.
39. Pupa SM, Menard S, Forti S, et al: New insights into the role of extracellular matrix during tumor onset and progression. J Cell Physiol 190: 259-267, 2002.
40. Ikeda O, Egami H, Ishiko T, et al: Expression of proteinase-activated receptor-2 in human pancreatic cancer: A possible relation to cancer invasion and induction of fibrosis. Int J Oncol 22: 295-300, 2003.
41. D'Andrea MR, Derian CK, Santulli RJ and Andrade-Gordon P: Differential expression of protease-activated receptors-1 and -2 in stromal fibroblasts of normal, benign, and malignant human tissues. Am J Pathol 158: 2031-2041, 2001.
42. Cederqvist K, Haglund C, Heikkila P, et al: High expression of pulmonary proteinase-activated receptor 2 in acute and chronic lung injury in preterm infants. Pediatr Res 57: 831-836, 2005.
43. Grandaliano G, Pontrelli P, Cerullo G, et al: Protease-activated receptor-2 expression in IgA nephropathy: a potential role in the pathogenesis of interstitial fibrosis. J Am Soc Nephrol 14: 2072-2083, 2003.
44. Masamune A, Kikuta K, Satoh M, et al: Protease-activated receptor-2-mediated proliferation and collagen production of rat pancreatic stellate cells. J Pharmacol Exp Ther 312: 651-658, 2005.
45. Borensztajn K, Stiekema J, Nijmeijer S, et al: Factor Xa stimulates proinflammatory and profibrotic responses in fibroblasts via protease-activated receptor-2 activation. Am J Pathol 172: 309-320, 2008.