Hereditary pancreatitis caused by mutation-induced misfolding of human cationic trypsinogen: A novel disease mechanism

Human Mutation

Volumn 30, Issue 4, 2009, Pages 575-582

  Kereszturi, Éva ^a   Szmola, Richárd ^a   Kukor, Zoltán ^a   Simon, Peter ^b   Weiss, Frank Ulrich ^b   Lerch, Markus M ^b   Sahin Tóth, Miklós ^a,c  

^a BOSTON UNIVERSITY   (United States)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c NONE   (United States)

Author keywords

Chronic pancreatitis; Endoplasmic reticulum stress; ER; Protein misfolding; PRSS1; Trypsinogen mutation; Unfolded protein response

Indexed keywords

HUMAN CATIONIC TRYPSINOGEN; IMMUNOGLOBULIN BINDING FACTOR; TRYPSINOGEN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ARTICLE; CASE REPORT; CHILD; DISULFIDE BOND; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE MUTATION; GENETIC SCREENING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PANCREATITIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD;

EID: 63749109353     PISSN: 10597794     EISSN: None     Source Type: Journal    
DOI: 10.1002/humu.20853     Document Type: Article

References (43)

1. Applebaum-Shapiro SE, Finch R, Pfutzer RH, Hepp LA, Gates L, Amann S, Martin S, Ulrich CD, Whitcomb DC. 2001. Hereditary pancreatitis in North America: the Pittsburgh-Midwest Multi-Center Pancreatic Study Group Study. Pancreatology 1:439-443.
2. Boulling A, Le Marechal C, Trouve P, RagueenesO,ChenJM, Ferec C. 2007. Functional analysis of pancreatitis-associated missense mutations in the pancreatic secretory trypsin inhibitor (SPINK1) gene. Eur J Hum Genet 15:936-942.
3. Grussenmeyer T, Scheidtmann KH, Hutchinson MA, Eckhart W, Walter G. 1985. Complexes of polyoma virus medium T antigen and cellular proteins. Proc Natl Acad Sci USA 82:7952-7954.
4. Harper LV, Hilton AC, Jones AF. 2003. RT-PCR for the pseudogene-free amplification of the glyceraldehyde-3-phosphate dehydrogenase gene (gapd). Mol Cell Probes 17:261-265.
5. Hirota M, Kitagaki M, Itagaki H, Aiba S. 2006. Quantitative measurement of spliced XBP1 mRNA as an indicator of endoplasmic reticulum stress. J Toxicol Sci 31:149-156.
6. Howes N, Lerch MM, Greenhalf W, Stocken DD, Ellis I, Simon P, Truninger K, Ammann R, Cavallini G, Charnley RM, Uomo G, Delhaye M, Spicak J, Drumm B, Jansen J, Mountford R, Whitcomb DC, Neoptolemos JP. 2004. Clinical and genetic characteristics of hereditary pancreatitis in Europe. Clin Gastroenterol Hepatol 2:252-261.
7. Hucl T, Jesnowski R, Pfützer RH, Elsässer HP, Löhr M. 2007. SPINK1 variants in young-onset pancreatic cancer. J Gastroenterol 42:599.
8. Keiles S, Kammesheidt A. 2006. Identification of CFTR, PRSS1, and SPINK1 mutations in 381 patients with pancreatitis. Pancreas 33:221-227.
9. Keim V, Witt H, Bauer N, Bödeker H, Rosendahl J, Teich N, Mössner J. 2003. The course of genetically determined chronic pancreatitis. JOP 4:146-154.
10. Király O, Boulling A, Witt H, Le Maréchal C, Chen JM, Rosendahl J, Battaggia C, Wartmann T, Sahin-Tóth M, Férec C. 2007a. Signal peptide variants that impair secretion of pancreatic secretory trypsin inhibitor (SPINK1) cause autosomal dominant hereditary pancreatitis. Hum Mutat 28:469-476.
11. Király O, Wartmann T, Sahin-Tóth M. 2007b. Missense mutations in pancreatic secretory trypsin inhibitor (SPINK1) cause intracellular retention and degradation. Gut 56:1433-1438.
12. Kubisch CH, Sans MD, Arumugam T, Ernst SA, Williams JA, Logsdon CD. 2006. Early activation of endoplasmic reticulum stress is associated with arginine-induced acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 291:G238-G245.
13. Kubisch CH, Logsdon CD. 2007. Secretagogues differentially activate endoplasmic reticulum stress responses in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 292:G1804-G1812.
14. Kuwata K, Hirota M, Shimizu H, Nakae M, Nishihara S, Takimoto A, Mitsushima K, Kikuchi N, Endo K, Inoue M, Ogawa M. 2002. Functional analysis of recombinant pancreatic secretory trypsin inhibitor protein with amino-acid substitution. J Gastroenterol 37:928-934.
15. Le Maréchal C, Bretagne JF, Raguéenès O, Quéré I, Chen JM, Férec C. 2001. Identification of a novel pancreatitis-associated missense mutation, R116C, in the human cationic trypsinogen gene (PRSS1). Mol Genet Metab 74:342-344.
16. Le Maréchal C, Masson E, Chen JM, Morel F, Ruszniewski P, Levy P, Férec C. 2006. Hereditary pancreatitis caused by triplication of the trypsinogen locus. Nat Genet 38:1372-1374.
17. Lengyel Z, Pail G, Sahin-Tóth M. 1998. Affinity purification of recombinant trypsinogen using immobilized ecotin. Protein Expr Purif 12:291-294.
18. Marciniak SJ, Ron D. 2006. Endoplasmic reticulum stress signaling in disease. Physiol Rev 86:1133-1149.
19. Masson E, Chen JM, Scotet V, Le Maréchal C, Férec C. 2008a. Association of rare chymotrypsinogen C (CTRC) gene variations in patients with idiopathic chronic pancreatitis. Hum Genet 123:83-91.
20. Masson E, Le Maréchal C, Chandak GR, Lamoril J, Bezieau S, Mahurkar S, Bhaskar S, Reddy DN, Chen JM, Ferec C. 2008b. Trypsinogen copy number mutations in patients with idiopathic chronic pancreatitis. Clin Gastroenterol Hepatol 6:82-88.
21. Nemoda Z, Sahin-Tóth M. 2006. Chymotrypsin C (caldecrin) stimulates autoactivation of human cationic trypsinogen. J Biol Chem 281:11879-11886.
22. Pfützer RH, Barmada MM, Brunskill AP, Finch R, Hart PS, Neoptolemos J, Furey WF, Whitcomb DC. 2000. SPINK1/PSTI polymorphisms act as disease modifiers in familial and idiopathic chronic pancreatitis. Gastroenterology 119:615-623.
23. Pho-Iam T, Thongnoppakhun W, Yenchitsomanus PT, Limwongse C. 2005. A Thai family with hereditary pancreatitis and increased cancer risk due to a mutation in PRSS1 gene. World J Gastroenterol 11:1634-1638.
24. Rebours V, Boutron-Ruault MC, Schnee M, Ferec C, Maire F, Hammel P, Ruszniewski P, Levy P. 2008. Risk of pancreatic adenocarcinoma in patients with hereditary pancreatitis: a national exhaustive series. Am J Gastroenterol 103:111-119.
25. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529.
26. Rosendahl J, Witt H, Szmola R, Bhatia E, Ózsvári B, Landt O, Schulz HU, Gress TM, Pfützer R, Lohr M, Kovács P, Blüher M, Stumvoll M, Choudhuri G, Hegyi P, te Morsche RH, Drenth JP, Truninger K, Macek M, Jr, Puhl G, Witt U, Schmidt H, Büning C, Ockenga J, Kage A, Groneberg DA, Nickel R, Berg T, Wiedenmann B, Bödeker H, Keim V, Mössner J, Teich N, Sahin-Tóth M. 2008. Chymotrypsin C (CTRC) variants that diminish activity or secretion are associated with chronic pancreatitis. Nat Genet 40:78-82.
27. 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.
28. Sahin-Tóth M, Tóth M. 2000. Gain-of-function mutations associated with hereditary pancreatitis enhance autoactivation of human cationic trypsinogen. Biochem Biophys Res Commun 278:286-289.
29. Sahin-Tóth M. 2006. Biochemical models of hereditary pancreatitis. Endocrinol Metab Clin North Am 35:303-312.
30. Simon P, Weiss FU, Sahin-Tóth M, Parry M, Nayler O, Lenfers B, Schnekenburger J, Mayerle J, Domschke W, Lerch MM. 2002a. Hereditary pancreatitis caused by a novel PRSS1 mutation (Arg-122->Cys) that alters autoactivation and autodegradation of cationic trypsinogen. J Biol Chem 277:5404-5410. Simon P, Weiss FU, Zimmer KP, Rand S, Brinkmann B, Domschke W, Lerch MM. 2002b. Spontaneous and sporadic trypsinogen mutations in idiopathic pancreatitis. JAMA 288:2122.
31. Szmola R, Sahin-Tonovel PRSS1 mutation (Arg-122->Cys) that alters autoactivation and autodegradation of cationic trypsinogen. J Biol Chem 277:5404-5410.
32. th M. 2007. Chymotrypsin C (caldecrin) promotes degradation of human cationic trypsin: identity with Rinderknecht's enzyme Y. Proc Natl Acad Sci USA 104:11227-11232.
33. Tautermann G, Ruebsamen H, Beck M, Dertinger S, Drexel H, Lohse P. 2001. R116C mutation of cationic trypsinogen in a Turkish family with recurrent pancreatitis illustrates genetic microheterogeneity of hereditary pancreatitis. Digestion 64:226-232.
34. Teich N, Bauer N, Mössner J, Keim V. 2002. Mutational screening of patients with nonalcoholic chronic pancreatitis: identification of further trypsinogen variants. Am J Gastroenterol 97:341-346.
35. Teich N, Rosendahl J, Tonovel PRSS1 mutation (Arg-122->Cys) that alters autoactivation and autodegradation of cationic trypsinogen. J Biol Chem 277:5404-5410.
36. th M, Mössner J, Sahin-Tonovel PRSS1 mutation (Arg-122->Cys) that alters autoactivation and autodegradation of cationic trypsinogen. J Biol Chem 277:5404-5410.
37. th M. 2006. Mutations of human cationic trypsinogen (PRSS1) and chronic pancreatitis. Hum Mutat 27:721-730.
38. Whitcomb DC, Gorry MC, Preston RA, Furey W, Sossenheimer MJ, Ulrich CD, Martin SP, Gates LK, Jr, Amann ST, Toskes PP, Liddle R, McGrath K, Uomo G, Post JC, Ehrlich GD. 1996. Hereditary pancreatitis is caused by a mutation in the cationic trypsinogen gene. Nat Genet 14:141-145.
39. Witt H, Luck W, Hennies HC, Classen M, Kage A, Lass U, Landt O, 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.
40. Witt H, Sahin-Tonovel PRSS1 mutation (Arg-122->Cys) that alters autoactivation and autodegradation of cationic trypsinogen. J Biol Chem 277:5404-5410.
41. th M, Landt O, Chen JM, Kähne T, Drenth JP, Kukor Z, Szepessy E, Halangk W, Dahm S, Rohde K, Schulz HU, Le Marechal C, Akar N, Ammann RW, Truninger K, Bargetzi M, Bhatia E, Castellani C, Cavestro GM, Cerny M, Destro-Bisol G, Spedini G, Eiberg H, Jansen JB, Koudova M, Rausova E, Macek M, Jr, Malats N, Real FX, Menzel HJ, Moral P, Galavotti R, Pignatti PF, Rickards O, Spicak J, Zarnescu NO, Bock W, Gress TM, Friess H, Ockenga J, Schmidt H, Pfützer R, Lohr M, Simon P, Weiss FU, Lerch MM, Teich N, Keim V, Berg T, Wiedenmann B, Luck W, Groneberg DA, Becker M, Keil T, Kage A, Bernardova J, Braun M, Guldner C, Halangk J, Rosendahl J, Witt U, Treiber M, Nickel R, Ferec C. 2006. A degradation-sensitive anionic trypsinogen (PRSS2) variant protects against chronic pancreatitis. Nat Genet 38:668-673.
42. Witt H, Apte MV, Keim V, Wilson JS. 2007. Chronic pancreatitis: challenges and advances in pathogenesis, genetics, diagnosis, and therapy. Gastroenterology 132:1557-1573.
43. Zenker M, Mayerle J, Lerch MM, Tagariello A, Zerres K, Durie PR, Beier M, Hulskamp G, Guzman C, Rehder H, Beemer FA, Hamel B, Vanlieferinghen P, Gershoni-Baruch R, Vieira MW, Dumic M, Auslender R, Gil-da-Silva-Lopes VL, Steinlicht S, Rauh M, Shalev SA, Thiel C, Ekici AB, Winterpacht A, Kwon YT, Varshavsky A,Reis A. 2005. Deficiency of UBR1, a ubiquitin ligase of the N-end rule pathway, causes pancreatic dysfunction, malformations and mental retardation (Johanson-Blizzard syndrome). Nat Genet 37:1345-1350.