Increased activation of hereditary pancreatitis-associated human cationic trypsinogen mutants in presence of chymotrypsin C

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20701-20710

  Szabó, András ^a   Sahin Tóth, Miklós ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION PEPTIDE; AUTOACTIVATION; AUTOSOMAL DOMINANTS; HUMAN CATIONIC TRYPSINOGENS; N-TERMINALS; WILD TYPES;

BIOCHEMISTRY; BIOLOGY;

DEGRADATION;

CHYMOTRYPSIN TRYPSIN;

ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CALCIUM BINDING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE MUTATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; PANCREATITIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION;

AMINO ACID SUBSTITUTION; CHYMOTRYPSIN; ENZYME ACTIVATION; GENETIC DISEASES, INBORN; HEK293 CELLS; HUMANS; MUTATION, MISSENSE; PANCREAS; PANCREATITIS; PROTEOLYSIS; TRYPSIN;

EID: 84862017112     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.360065     Document Type: Article

References (33)

1. 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 (Pubitemid 26338792)
2. Teich, N., Rosendahl, J., Tóth, M., Mössner, J., and Sahin-Tóth, M. (2006) Mutations of human cationic trypsinogen (PRSS1) and chronic pancreatitis. Hum. Mutat. 27, 721-730 (Pubitemid 44205064)
3. Howes, N., Lerch, M. M., Greenhalf, W., Stocken, D. D., Ellis, I., Simon, P., Truninger, K., Ammann, R., Cavallini, G., Charnley, R. M., Uomo, G., Delhaye, M., Spicak, J., Drumm, B., Jansen, J., Mountford, R., Whitcomb, D. C., Neoptolemos, J. P., and European Registry of Hereditary Pancreatitis and Pancreatic Cancer (EUROPAC) (2004) Clinical and genetic characteristics of hereditary pancreatitis in Europe. Clin. Gastroenterol. Hepatol. 2, 252-261 (Pubitemid 38293313)
4. Rebours, V., Boutron-Ruault, M. C., Schnee, M., Férec, C., Le Maréchal, C., Hentic, O., Maire, F., Hammel, P., Ruszniewski, P., and Lévy, P. (2009) The natural history of hereditary pancreatitis: a national series. Gut 58, 97-103
5. Szmola, R., and Sahin-Tóth, M. (2010) Uncertainties in the classification of human cationic trypsinogen (PRSS1) variants as hereditary pancreatitis- associated mutations. J. Med. Genet. 47, 348-350
6. Sahin-Tóth, M. (2000) Human cationic trypsinogen. Role of Asn-21 in zymogen activation and implications in hereditary pancreatitis. J. Biol. Chem. 275, 22750-22755
7. Sahin-Tóth, M., and Tóth, M. (2000) Gain-of-function mutations associated with hereditary pancreatitis enhance autoactivation of human cationic trypsinogen. Biochem. Biophys. Res. Commun. 278, 286-289
8. Teich, N., Nemoda, Z., Köhler, H., Heinritz, W., Mössner, J., Keim, V., and Sahin-Tóth, M. (2005) Gene conversion between functional trypsinogen genes PRSS1 and PRSS2 associated with chronic pancreatitis in a 6-yearold girl. Hum. Mutat. 25, 343-347 (Pubitemid 40524661)
9. Teich, N., Ockenga, J., Hoffmeister, A., Manns, M., Mössner, J., and Keim, V. (2000) Chronic pancreatitis associated with an activation peptide mutation that facilitates trypsin activation. Gastroenterology 119, 461-465 (Pubitemid 30621996)
10. Chen, J. M., Kukor, Z., Le Maréchal, C., Tóth, M., Tsakiris, L., Raguénès, O., Férec, C., and Sahin-Tóth, M. (2003) Evolution of trypsinogen activation peptides. Mol. Biol. Evol. 20, 1767-1777 (Pubitemid 37420930)
11. Joergensen, M. T., Geisz, A., Brusgaard, K., Schaffalitzky de Muckadell, O. B., Hegyi, P., Gerdes, A. M., and Sahin-Tóth, M. (2011) Intragenic duplication: a novel mutational mechanism in hereditary pancreatitis. Pancreas 40, 540-546
12. Simon, P., Weiss, F. U., Sahin-Tóth, M., Parry, M., Nayler, O., Lenfers, B., Schnekenburger, J., Mayerle, J., Domschke, W., and Lerch, M. M. (2002) Hereditary pancreatitis caused by a novel PRSS1 mutation (Arg-122 3 Cys) that alters autoactivation and autodegradation of cationic trypsinogen. J. Biol. Chem. 277, 5404-5410 (Pubitemid 34968587)
13. Kereszturi, E., Szmola, R., Kukor, Z., Simon, P., Weiss, F. U., Lerch, M. M., and Sahin-Tóth, M. (2009) Hereditary pancreatitis caused by mutation-induced misfolding of human cationic trypsinogen: a novel disease mechanism. Hum. Mutat. 30, 575-582
14. Nemoda, Z., and Sahin-Tóth, M. (2006) ChymotrypsinC(caldecrin) stimulates autoactivation of human cationic trypsinogen. J. Biol. Chem. 281, 11879-11886 (Pubitemid 43855449)
15. Szmola, R., and Sahin-Tóth, M. (2007) Chymotrypsin C (caldecrin) promotes degradation of human cationic trypsin: identity with Rinderknecht's enzyme Y. Proc. Natl. Acad. Sci. U.S.A. 104, 11227-11232 (Pubitemid 47175123)
16. Rosendahl, J., Witt, H., Szmola, R., Bhatia, E., Ózsvári, B., Landt, O., Schulz, H. U., Gress, T. M., Pfützer, R., Löhr, M., Kovacs, P., Blüher, M., Stumvoll, M., Choudhuri, G., Hegyi, P., te Morsche, R. H., Drenth, J. P., Truninger, K., Macek, M., Jr., Puhl, G., Witt, U., Schmidt, H., Büning, C., Ockenga, J., Kage, A., Groneberg, D. A., Nickel, R., Berg, T., Wiedenmann, B., Bödeker, H., Keim, V., Mössner, J., Teich, N., and Sahin-Tóth, M. (2008) Chymotrypsin C (CTRC) variants that diminish activity or secretion are associated with chronic pancreatitis. Nat. Genet. 40, 78-82
17. Masson, E., Chen, J. M., Scotet, V., Le Maréchal, C., and Férec, C. (2008) Association of rare chymotrypsinogen C (CTRC) gene variations in patients with idiopathic chronic pancreatitis. Hum. Genet. 123, 83-91
18. Zhou, J., and Sahin-Tóth, M. (2011) ChymotrypsinCmutations in chronic pancreatitis. J. Gastroenterol. Hepatol. 26, 1238-1246
19. Király, O., Guan, L., Szepessy, E., Tóth, M., Kukor, Z., and Sahin-Tóth, M. (2006) Expression of human cationic trypsinogen with an authentic N terminus using intein-mediated splicing in aminopeptidase P-deficient Escherichia coli. Protein Expr. Purif. 48, 104-111
20. Kukor, Z., Tóth, M., Pál, G., and Sahin-Tóth, M. (2002) Human cationic trypsinogen. Arg-117 is the reactive site of an inhibitory surface loop that controls spontaneous zymogen activation. J. Biol. Chem. 277, 6111-6117 (Pubitemid 34968398)
21. Bence, M., and Sahin-Tóth, M. (2011) Asparagine-linked glycosylation of human chymotrypsin C is required for folding and secretion but not for enzyme activity. FEBS J. 278, 4338-4350
22. Szabó, A., Héja, D., Szakács, D., Zboray, K., Kékesi, K. A., Radisky, E. S., Sahin-Tóth, M., and Pál, G. (2011) High affinity small protein inhibitors of human chymotrypsin C (CTRC) selected by phage display reveal unusual preference for P4′ acidic residues. J. Biol. Chem. 286, 22535-22545
23. Király, O., Guan, L., and Sahin-Tóth, M. (2011) Expression of recombinant proteins with uniform N termini. Methods Mol. Biol. 705, 175-194
24. Lengyel, Z., Pál, G., and Sahin-Tóth, M. (1998) Affinity purification of recombinant trypsinogen using immobilized ecotin. Protein Expr. Purif. 12, 291-294 (Pubitemid 28360456)
25. Ózsvári, B., Hegyi, P., and Sahin-Tóth, M. (2008) The guinea pig pancreas secretes a single trypsinogen isoform, which is defective in autoactivation. Pancreas 37, 182-188
26. Arduino, C., Salacone, P., Pasini, B., Brusco, A., Salmin, P., Bacillo, E., Robecchi, A., Cestino, L., Cirillo, S., Regge, D., Cappello, N., and Gaia, E. (2005) Association of a new cationic trypsinogen gene mutation (V39A) with chronic pancreatitis in an Italian family. Gut 54, 1663-1664 (Pubitemid 41531792)
27. 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 (Pubitemid 29297613)
28. Grocock, C. J., Rebours, V., Delhaye, M. N., Andrén-Sandberg, A., Weiss, F. U., Mountford, R., Harcus, M. J., Niemczyck, E., Vitone, L. J., Dodd, S., Jørgensen, M. T., Ammann, R. W., Schaffalitzky de Muckadell, O., Butler, J. V., Burgess, P., Kerr, B., Charnley, R., Sutton, R., Raraty, M. G., Devière, J., Whitcomb, D. C., Neoptolemos, J. P., Lévy, P., Lerch, M. M., Greenhalf, W., and European Registry of Hereditary Pancreatitis and Pancreatic Cancer. (2010) The variable phenotype of the p.A16V mutation of cationic trypsinogen (PRSS1) in pancreatitis families. Gut 59, 357-363
29. Joergensen, M. T., Brusgaard, K., Crüger, D. G., Gerdes, A. M., and Schaffalitzky de Muckadell, O. B. (2010) Genetic, epidemiological, and clinical aspects of hereditary pancreatitis: a population-based cohort study in Denmark. Am. J. Gastroenterol. 105, 1876-1883
30. Bertin, C., Pelletier, A. L., Vullierme, M. P., Bienvenu, T., Rebours, V., Hentic, O., Maire, F., Hammel, P., Vilgrain, V., Ruszniewski, P., and Lévy, P. (2012) Pancreas divisum is not a cause of pancreatitis by itself but acts as a partner of genetic mutations. Am. J. Gastroenterol. 107, 311-317
31. Harada, H., Takeda, M., Yabe, H., Hanafusa, E., Hayashi, T., Kunichika, K., Kochi, F., Mishima, K., and Kimura, I. (1980) The calcium concentration in human pure pancreatic juice in chronic pancreatitis. Gastroenterol. Jpn. 15, 355-361 (Pubitemid 11238421)
32. Gerolami, A., Marteau, C., Matteo, A., Sahel, J., Portugal, H., Pauli, A. M., Pastor, J., and Sarles, H. (1989) Calcium carbonate saturation in human pancreatic juice: possible role of ductal H+ secretion. Gastroenterology 96, 881-884 (Pubitemid 19057614)
33. Furui, T., Kondoh, S., Harada, T., Takeuchi, K., Shiraishi, K., Kaino, S., Okuda, S., Okita, K., and Nakamura, K. (2000) Calcium concentration and artificial precipitates in human pancreatic juice. Pancreas 21, 257-261