The roles of serine protease inhibitor Kazal type 1 (SPINK1) in pancreatic diseases

Experimental Animals

Volumn 60, Issue 5, 2011, Pages 433-444

  Ohmuraya, Masaki ^a   Yamamura, Ken ichi ^b  

^a Priority Organization for Innovation and Excellence   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Autophagy; EGFR; Growth factor; SPINK1 Spink3; Trypsin inhibitor

Indexed keywords

CATHEPSIN B; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERINE PROTEASE INHIBITOR KAZAL TYPE 1; SERINE PROTEASE INHIBITOR KAZAL TYPE 3; TRYPSIN; TRYPSIN INHIBITOR; TRYPSINOGEN; UNCLASSIFIED DRUG;

ACUTE PANCREATITIS; AUTOPHAGY; BILE DUCT CARCINOMA; CANCER GROWTH; CANCER INVASION; CANCER RECURRENCE; CANCER SURVIVAL; CELL GROWTH; CHRONIC PANCREATITIS; GENE; GENE MUTATION; GENETIC PREDISPOSITION; HUMAN; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS DISEASE; REVIEW; SPINK1 GENE;

ANIMALS; AUTOPHAGY; CARRIER PROTEINS; EPIDERMAL GROWTH FACTOR; GLYCOPROTEINS; HUMANS; MICE; MUTATION; NEOPLASMS; PANCREATITIS, CHRONIC; PROSTATIC SECRETORY PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STIMULATION, CHEMICAL; TRYPSIN INHIBITOR, KAZAL PANCREATIC;

MUS;

EID: 80155186900     PISSN: 13411357     EISSN: None     Source Type: Journal    
DOI: 10.1538/expanim.60.433     Document Type: Review

References (76)

1. Araki, K., Araki, M., and Yamamura, K. 2002. Site-directed integration of the cre gene mediated by Cre recombinase using a combination of mutant lox sites. Nucleic Acids Res. 30: e103.
2. Araki, K., Imaizumi, T., Sekimoto, T., Yoshinobu, K., Yoshimuta, J., Akizuki, M., Miura, K., Araki, M., and Yamamura, K. 1999. Exchangeable gene trap using the Cre/mutated lox system. Cell. Mol. Biol. (Noisy-le-grand). 45: 737-750.
3. Bartelt, D.C., Shapanka, R., and Greene, L.J. 1977. The primary structure of the human pancreatic secretory trypsin inhibitor. Amino acid sequence of the reduced S-aminoethylated protein. Arch. Biochem. Biophys. 179: 189-199.
4. Bellu, A.R. and Kiel, J.A. 2003. Selective degradation of peroxisomes in yeasts. Microsc. Res. Tech. 61: 161-170.
5. Chen, J.M. and Ferec, C. 2000. Molecular basis of hereditary pancreatitis. Eur. J. Hum. Genet. 8: 473-479.
6. Chen, J.M., Mercier, B., Audrezet, M.P., and Ferec, C. 2000. Mutational analysis of the human pancreatic secretory trypsin inhibitor (PSTI) gene in hereditary and sporadic chronic pancreatitis. J. Med. Genet. 37: 67-69.
7. Chen, J.M., Mercier, B., Audrezet, M.P., Raguenes, O., Quere, I., and Ferec, C. 2001. Mutations of the pancreatic secretory trypsin inhibitor (PSTI) gene in idiopathic chronic pancreatitis. Gastroenterology 120: 1061-1064.
8. Chen, J.M., Piepoli Bis, A., Le Bodic, L., Ruszniewski, P., Robaszkiewicz, M., Deprez, P.H., Raguenes, O., Quere, I., Andriulli, A., and Ferec, C. 2001. Mutational screening of the cationic trypsinogen gene in a large cohort of subjects with idiopathic chronic pancreatitis. Clin. Genet. 59: 189-193.
9. Chen, J.M., Raguenes, O., Ferec, C., Deprez, P.H., Verellen-Dumoulin, C., and Andriulli, A. 1999. The A16V signal peptide cleavage site mutation in the cationic trypsinogen gene and chronic pancreatitis. Gastroenterology 117: 1508-1509.
10. Cobb, M.H. 1999. MAP kinase pathways. Prog. Biophys. Mol. Biol. 71: 479-500.
11. Ding, Y., Cravero, J.D., Adrian, K., and Grippo, P. Modeling pancreatic cancer in vivo: from xenograft and carcinogen-induced systems to genetically engineered mice. Pancreas 39: 283-292.
12. Ferec, C., Raguenes, O., Salomon, R., Roche, C., Bernard, J.P., Guillot, M., Quere, I., Faure, C., Mercier, B., Audrezet, M.P., Guillausseau, P.J., Dupont, C., Munnich, A., Bignon, J.D., and Le Bodic, L. 1999. Mutations in the cationic trypsinogen gene and evidence for genetic heterogeneity in hereditary pancreatitis. J. Med. Genet. 36: 228-232.
13. Freeman, T.C., Playford, R.J., Quinn, C., Beardshall, K., Poulter, L., Young, J., and Calam, J. 1990. Pancreatic secretory trypsin inhibitor in gastrointestinal mucosa and gastric juice. Gut 31: 1318-1323.
14. Fukuoka, S., Fushiki, T., Kitagawa, Y., Sugimoto, E., and Iwai, K. 1986. Growth stimulating activity on 3T3 fibroblasts of the molecular weight 6,500-peptide purified from rat pancreatic juice. Biochem. Biophys. Res. Commun. 139: 545-550.
15. Fukuoka, S., Fushiki, T., Kitagawa, Y., Sugimoto, E., and Iwai, K. 1987. Competition of a growth stimulating-/cholecystokinin (CCK) releasing-peptide (monitor peptide) with epidermal growth factor for binding to 3T3 fibroblasts. Biochem. Biophys. Res. Commun. 145: 646-650.
16. Gomez-Lira, M., Bonamini, D., Castellani, C., Unis, L., Cavallini, G., Assael, B.M., and Pignatti, P.F. 2003. Mutations in the SPINK1 gene in idiopathic pancreatitis Italian patients. Eur. J. Hum. Genet. 11: 543-546.
17. Gouyer, V., Fontaine, D., Dumont, P., de Wever, O., Fontayne-Devaud, H., Leteurtre, E., Truant, S., Delacour, D., Drobecq, H., Kerckaert, J.P., de Launoit, Y., Bracke, M., Gespach, C., Desseyn, J.L., and Huet, G. 2008. Autocrine induction of invasion and metastasis by tumor-associated trypsin inhibitor in human colon cancer cells. Oncogene 27: 4024-4033.
18. Higashiyama, M., Doi, O., Kodama, K., Yokouchi, H., Tateishi, R., Matsuura, N., Murata, A., Tomita, N., Monden, T., and Ogawa, M. 1992. Immunohistochemical analysis of pancreatic secretory trypsin inhibitor expression in pulmonary adenocarcinoma: its possible participation in scar formation of the tumor tissues. Tumour Biol. 13: 299-307.
19. Higashiyama, M., Monden, T., Tomita, N., Murotani, M., Kawasaki, Y., Morimoto, H., Murata, A., Shimano, T., Ogawa, M., and Mori, T. 1990. Expression of pancreatic secretory trypsin inhibitor (PSTI) in colorectal cancer. Br. J. Cancer 62: 954-958.
20. Horii, A., Kobayashi, T., Tomita, N., Yamamoto, T., Fukushige, S., Murotsu, T., Ogawa, M., Mori, T., and Matsubara, K. 1987. Primary structure of human pancreatic secretory trypsin inhibitor (PSTI) gene. Biochem. Biophys. Res. Commun. 149: 635-641.
21. Huhtala, M.L., Pesonen, K., Kalkkinen, N., and Stenman, U.H. 1982. Purification and characterization of a tumor-associated trypsin inhibitor from the urine of a patient with ovarian cancer. J. Biol. Chem. 257: 13713-13716.
22. Hunt, L.T., Barker, W.C., and Dayhoff, M.O. 1974. Epidermal growth factor: internal duplication and probable relationship to pancreatic secretory trypsin inhibitor. Biochem. Biophys. Res. Commun. 60: 1020-1028.
23. Ida, S., Ohmuraya, M., Hirota, M., Ozaki, N., Hiramatsu, S., Uehara, H., Takamori, H., Araki, K., Baba, H., and Yamamura, K. 2010. Chronic pancreatitis in mice by treatment with choline-deficient ethionine-supplemented diet. Exp. Anim. 59: 421-429.
24. Kaneko, K., Nagasaki, Y., Furukawa, T., Mizutamari, H., Sato, A., Masamune, A., Shimosegawa, T., and Horii, A. 2001. Analysis of the human pancreatic secretory trypsin inhibitor (PSTI) gene mutations in Japanese patients with chronic pancreatitis. J. Hum. Genet. 46: 293-297.
25. Kazal, L.A., Spicer, D.S., and Brahinsky, R.A. 1948. Isolation of a crystalline trypsin inhibitor-anticoagulant protein from pancreas. J. Am. Chem. Soc. 70: 304-340.
26. Kim, J. and Klionsky, D.J. 2000. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu. Rev. Biochem. 69: 303-342.
27. Kiraly, O., Wartmann, T., and Sahin-Toth, M. 2007. Missense mutations in pancreatic secretory trypsin inhibitor (SPINK1) cause intracellular retention and degradation. Gut 56: 1433-1438.
28. Kuwata, K., Hirota, M., Nishimori, I., Otsuki, M., and Ogawa, M. 2003. Mutational analysis of the pancreatic secretory trypsin inhibitor gene in familial and juvenile pancreatitis in Japan. J. Gastroenterol. 38: 365-370.
29. Kuwata, K., Hirota, M., Shimizu, H., Nakae, M., Nishihara, S., Takimoto, A., Mitsushima, K., Kikuchi, N., Endo, K., Inoue, M., and Ogawa, M. 2002. Functional analysis of recombinant pancreatic secretory trypsin inhibitor protein with amino-acid substitution. J. Gastroenterol. 37: 928-934.
30. Kuwata, K., Hirota, M., Sugita, H., Kai, M., Hayashi, N., Nakamura, M., Matsuura, T., Adachi, N., Nishimori, I., and Ogawa, M. 2001. Genetic mutations in exons 3 and 4 of the pancreatic secretory trypsin inhibitor in patients with pancreatitis. J. Gastroenterol. 36: 612-618.
31. Le Marechal, C., Masson, E., Chen, J.M., Morel, F., Ruszniewski, P., Levy, P., and Ferec, C. 2006. Hereditary pancreatitis caused by triplication of the trypsinogen locus. Nat. Genet. 38: 1372-1374.
32. Leach, S.D., Modlin, I.M., Scheele, G.A., and Gorelick, F.S. 1991. Intracellular activation of digestive zymogens in rat pancreatic acini. Stimulation by high doses of cholecystokinin. J. Clin. Invest. 87: 362-366.
33. Lemasters, J.J., Qian, T., He, L., Kim, J.S., Elmore, S.P., Cascio, W.E., and Brenner, D.A. 2002. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid. Redox Signal 4: 769-781.
34. Lowenfels, A.B., Maisonneuve, P., Cavallini, G., Ammann, R.W., Lankisch, P.G., Andersen, J.R., Dimagno, E.P., Andren-Sandberg, A., and Domellof, L. 1993. Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N. Engl. J. Med. 328: 1433-1437.
35. Lowenfels, A.B., Maisonneuve, P., DiMagno, E.P., Elitsur, Y., Gates, L.K. Jr., Perrault, J., and Whitcomb, D.C. 1997. Hereditary pancreatitis and the risk of pancreatic cancer. International Hereditary Pancreatitis Study Group. J. Natl. Cancer Inst. 89: 442-446.
36. Malka, D., Hammel, P., Maire, F., Rufat, P., Madeira, I., Pessione, F., Levy, P., and Ruszniewski, P. 2002. Risk of pancreatic adenocarcinoma in chronic pancreatitis. Gut 51: 849-852.
37. Marchbank, T., Chinery, R., Hanby, A.M., Poulsom, R., Elia, G., and Playford, R.J. 1996. Distribution and expression of pancreatic secretory trypsin inhibitor and its possible role in epithelial restitution. Am. J. Pathol. 148: 715-722.
38. Marchbank, T., Freeman, T.C., and Playford, R.J. 1998. Human pancreatic secretory trypsin inhibitor. Distribution, actions and possible role in mucosal integrity and repair. Digestion 59: 167-174.
39. Masson, E., Le Marechal, C., Chandak, G.R., Lamoril, J., Bezieau, S., Mahurkar, S., Bhaskar, S., Reddy, D.N., Chen, J.M., and Ferec, C. 2008. Trypsinogen copy number mutations in patients with idiopathic chronic pancreatitis. Clin. Gastroenterol Hepatol. 6: 82-88.
40. McKeehan, W.L., Sakagami, Y., Hoshi, H., and McKeehan, K.A. 1986. Two apparent human endothelial cell growth factors from human hepatoma cells are tumor-associated proteinase inhibitors. J. Biol. Chem. 261: 5378-5383.
41. Meijer, A.J. 2003. Amino acids as regulators and componentsof nonproteinogenic pathways. J. Nutr. 133: 2057-2062S.
42. Mizushima, N., Levine, B., Cuervo, A.M., and Klionsky, D.J. 2008. Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075.
43. Neufeld, T.P. TOR-dependent control of autophagy: biting the hand that feeds. Curr. Opin. Cell Biol. 22: 157-168.
44. Niinobu, T., Ogawa, M., Murata, A., Nishijima, J., and Mori, T. 1990. Identification and characterization of receptors specific for human pancreatic secretory trypsin inhibitor. J. Exp. Med. 172: 1133-1142.
45. Niinobu, T., Ogawa, M., Shibata, T., Murata, A., Nishibe, S., Mori, T., and Ogata, N. 1986. Specific binding of human pancreatic secretory trypsin inhibitor to various cultured cells. Res. Commun. Chem. Pathol. Pharmacol. 53: 245-248.
46. Ogawa, M., Matsuura, N., Higashiyama, K., and Mori, T. 1987. Expression of pancreatic secretory trypsin inhibitor in various cancer cells. Res. Commun. Chem. Pathol. Pharmacol. 55: 137-140.
47. Ogawa, M., Tsushima, T., Ohba, Y., Ogawa, N., Tanaka, S., Ishida, M., and Mori, T. 1985. Stimulation of DNA synthesis in human fibroblasts by human pancreatic secretory trypsin inhibitor. Res. Commun. Chem. Pathol. Pharmacol. 50: 155-158.
48. Ohmachi, Y., Murata, A., Matsuura, N., Yasuda, T., Monden, M., Mori, T., Ogawa, M., and Matsubara, K. 1993. Specific expression of the pancreatic-secretory-trypsin-inhibitor (PSTI) gene in hepatocellular carcinoma. Int. J. Cancer. 55: 728-734.
49. Ohmuraya, M., Hirota, M., Araki, K., Baba, H., and Yamamura, K. 2006. Enhanced trypsin activity in pancreatic acinar cells deficient for serine protease inhibitor kazal type 3. Pancreas 33: 104-106.
50. Ohmuraya, M., Hirota, M., Araki, M., Mizushima, N., Matsui, M., Mizumoto, T., Haruna, K., Kume, S., Takeya, M., Ogawa, M., Araki, K., and Yamamura, K. 2005. Autophagic cell death of pancreatic acinar cells in serine protease inhibitor Kazal type 3-deficient mice. Gastroenterology 129: 696-705.
51. Ohmuraya, M., Ozaki, N., Hirota, M., Baba, H., and Yamamura, K. 2009. Serine protease inhibitor Kazal type 1 (SPINK1): beyond the trypsin inhibitor. Curr. Enzym. Inhib. 5: 110-116.
52. Ohmuraya, M. and Yamamura, K. 2008. Autophagy and acute pancreatitis: a novel autophagy theory for trypsinogen activation. Autophagy 4: 1060-1062.
53. Ozaki, N., Ohmuraya, M., Hirota, M., Ida, S., Wang, J., Takamori, H., Higashiyama, S., Baba, H., and Yamamura, K. 2009. Serine protease inhibitor Kazal type 1 promotes proliferation of pancreatic cancer cells through the epidermal growth factor receptor. Mol. Cancer Res. 7: 1572-1581.
54. Paju, A. and Stenman, U.H. 2006. Biochemistry and clinical role of trypsinogens and pancreatic secretory trypsin inhibitor. Crit. Rev. Clin. Lab. Sci. 43: 103-142.
55. Pfutzer, R.H., Barmada, M.M., Brunskill, A.P., Finch, R., Hart, P.S., Neoptolemos, J., Furey, W.F., and Whitcomb, D.C. 2000. SPINK1/PSTI polymorphisms act as disease modifiers in familial and idiopathic chronic pancreatitis. Gastroenterology 119: 615-623.
56. Roberts, P., Moshitch-Moshkovitz, S., Kvam, E., O'Toole, E., Winey, M., and Goldfarb, D.S. 2003. Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol. Biol. Cell. 14: 129-141.
57. Rossi, L., Pfutzer, R.H., Parvin, S., Ali, L., Sattar, S., Kahn, A.K., Gyr, N., and Whitcomb, D.C. 2001. SPINK1/PSTI mutations are associated with tropical pancreatitis in Bangladesh. A preliminary report. Pancreatology 1: 242-245.
58. Scheving, L.A. 1983. Primary amino acid sequence similarity between human epidermal growth factor-urogastrone, human pancreatic secretory trypsin inhibitor, and members of porcine secretin family. Arch. Biochem. Biophys. 226: 411-413.
59. Schneider, A. 2005. Serine protease inhibitor kazal type 1 mutations and pancreatitis. Clin. Lab. Med. 25: 61-78.
60. Seglen, P.O. and Bohley, P. 1992. Autophagy and other vacuolar protein degradation mechanisms. Experientia 48: 158-172.
61. Steer, M.L. and Meldolesi, J. 1987. The cell biology of experimental pancreatitis. N. Engl. J. Med. 316: 144-150.
62. Steer, M.L., Meldolesi, J., and Figarella, C. 1984. Pancreatitis. The role of lysosomes. Dig. Dis. Sci. 29: 934-938.
63. Stenman, U.H., Huhtala, M.L., Koistinen, R., and Seppala, M. 1982. Immunochemical demonstration of an ovarian cancer-associated urinary peptide. Int. J. Cancer 30: 53-57.
64. Stenman, U.H., Koivunen, E., and Itkonen, O. 1991. Biology and function of tumor-associated trypsin inhibitor, TATI. Scand. J. Clin. Lab. Invest. Suppl. 207: 5-9.
65. Teich, N., Ockenga, J., Hoffmeister, A., Manns, M., Mossner, J., and Keim, V. 2000. Chronic pancreatitis associated with an activation peptide mutation that facilitates trypsin activation. Gastroenterology 119: 461-465.
66. Threadgold, J., Greenhalf, W., Ellis, I., Howes, N., Lerch, M.M., Simon, P., Jansen, J., Charnley, R., Laugier, R., Frulloni, L., Olah, A., Delhaye, M., Ihse, I., Schaffalitzky de Muckadell, O.B., Andren-Sandberg, A., Imrie, C.W., Martinek, J., Gress, T.M., Mountford, R., Whitcomb, D., and Neoptolemos, J.P. 2002. The N34S mutation of SPINK1 (PSTI) is associated with a familial pattern of idiopathic chronic pancreatitis but does not cause the disease. Gut 50: 675-681.
67. Tomita, N., Doi, S., Higashiyama, M., Morimoto, H., Murotani, M., Kawasaki, Y., Monden, T., Shimano, T., Horii, A., Yokouchi, H., and et al. 1990. Expression of pancreatic secretory trypsin inhibitor gene in human colorectal tumor. Cancer 66: 2144-2149.
68. Tomita, N., Horii, A., Yamamoto, T., Ogawa, M., Mori, T., and Matsubara, K. 1987. Expression of pancreatic secretory trypsin inhibitor gene in neoplastic tissues. FEBS Lett. 225: 113-119.
69. Tomlins, S.A., Rhodes, D.R., Yu, J., Varambally, S., Mehra, R., Perner, S., Demichelis, F., Helgeson, B.E., Laxman, B., Morris, D.S., Cao, Q., Cao, X., Andren, O., Fall, K., Johnson, L., Wei, J.T., Shah, R.B., Al-Ahmadie, H., Eastham, J.A., Eggener, S.E., Fine, S.W., Hotakainen, K., Stenman, U.H., Tsodikov, A., Gerald, W.L., Lilja, H., Reuter, V.E., Kantoff, P.W., Scardino, P.T., Rubin, M.A., Bjartell, A.S., and Chinnaiyan, A.M. 2008. The role of SPINK1 in ETS rearrangement-negative prostate cancers. Cancer Cell 13: 519-528.
70. Tonouchi, A., Ohtsuka, M., Ito, H., Kimura, F., Shimizu, H., Kato, M., Nimura, Y., Iwase, K., Hiwasa, T., Seki, N., Takiguchi, M., and Miyazaki, M. 2006. Relationship between pancreatic secretory trypsin inhibitor and early recurrence of intrahepatic cholangiocarcinoma following surgical resection. Am. J. Gastroenterol. 101: 1601-1610.
71. van Acker, G.J., Perides, G., and Steer, M.L. 2006. Co-localization hypothesis: a mechanism for the intrapancreatic activation of digestive enzymes during the early phases of acute pancreatitis. World J. Gastroenterol. 12: 1985-1990.
72. Whitcomb, D.C. 2010. Genetic aspects of pancreatitis. Annu. Rev. Med. 61: 413-424.
73. Whitcomb, D.C., Gorry, M.C., Preston, R.A., Furey, W., Sossenheimer, M.J., Ulrich, C.D., Martin, S.P., Gates, L.K. Jr., Amann, S.T., Toskes, P.P., Liddle, R., McGrath, K., Uomo, G., Post, J.C., and Ehrlich, G.D. 1996. Hereditary pancreatitis is caused by a mutation in the cationic trypsinogen gene. Nat. Genet. 14: 141-145.
74. Witt, H., Luck, W., and Becker, M. 1999. A signal peptide cleavage site mutation in the cationic trypsinogen gene is strongly associated with chronic pancreatitis. Gastroenterology 117: 7-10.
75. Witt, H., Luck, W., Hennies, H.C., Classen, M., Kage, A., Lass, U., Landt, O., and Becker, M. 2000. Mutations in the gene encoding the serine protease inhibitor, Kazal type 1 are associated with chronic pancreatitis. Nat. Genet. 25: 213-216.
76. Yamamoto, T., Nakamura, Y., Nishide, J., Emi, M., Ogawa, M., Mori, T., and Matsubara, K. 1985. Molecular cloning and nucleotide sequence of human pancreatic secretory trypsin inhibitor (PSTI) cDNA. Biochem. Biophys. Res. Commun. 132: 605-612.