Human cationic trypsinogen (PRSS1) variants and chronic pancreatitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 306, Issue 6, 2014, Pages

  Németh, Balázs Csaba ^a   Sahin Tóth, Miklós ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; SERINE PROTEINASE 1; TRYPSINOGEN; TRYPSINOGEN ACTIVATION PEPTIDE; UNCLASSIFIED DRUG; PRSS1 PROTEIN, HUMAN; TRYPSIN;

ALLELE; AUTOSOMAL DOMINANT INHERITANCE; CHRONIC PANCREATITIS; COPY NUMBER VARIATION; DNA SEQUENCE; ENDOPLASMIC RETICULUM STRESS; GENE CONVERSION; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HUMAN; NONHUMAN; PANCREATITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SCREENING; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; ANIMAL MODEL; GENETIC POLYMORPHISM; GENETICS; METABOLISM;

ANIMALS; HUMANS; MODELS, ANIMAL; PANCREATITIS, CHRONIC; POLYMORPHISM, GENETIC; TRYPSIN;

EID: 84900302416     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00419.2013     Document Type: Review

References (68)

1. Archer H, Jura N, Keller J, Jacobson M, Bar-Sagi D. A mouse model of hereditary pancreatitis generated by transgenic expression of R122H trypsinogen. Gastroenterology 131: 1844-1855, 2006.
2. Arduino C, Salacone P, Pasini B, Brusco A, Salmin P, Bacillo E, Robecchi A, Cestino L, Cirillo S, Regge D, Cappello N, Gaia E. Association of a new cationic trypsinogen gene mutation (V39A) with chronic pancreatitis in an Italian family. Gut 54: 1663-1664, 2005.
3. Bernardino AL, Guarita DR, Mott CB, Pedroso MR, Machado MC, Laudanna AA, Tani CM, Almeida FL, Zatz M. CFTR, PRSS1 and SPINK1 mutations in the development of pancreatitis in Brazilian patients. JOP 4: 169-177, 2003.
4. Chang YT, Wei SC, Tien YWLPC, Jan IS, Su YN, Wong JM, Chang MC. Association and differential role of PRSS1 and SPINK1 mutation in early-onset and late-onset idiopathic chronic pancreatitis in Chinese subjects. Gut 58: 885, 2009.
5. Chauvin A, Chen JM, Quemener S, Masson E, Kehrer-Sawatzki H, Ohmle B, Cooper DN, Le Maréchal C, Férec C. Elucidation of the complex structure and origin of the human trypsinogen locus triplication. Hum Mol Genet 18: 3605-3614, 2009.
6. Chen JM, Ferec C. Gene conversion-like missense mutations in the human cationic trypsinogen gene and insights into the molecular evolution of the human trypsinogen family. Mol Genet Metab 71: 463-469, 2000.
7. Chen JM, Piepoli Bis A, Le Bodic L, Ruszniewski P, Robaszkiewicz M, Deprez PH, Raguenes O, Quere I, Andriulli A, Ferec C. Mutational screening of the cationic trypsinogen gene in a large cohort of subjects with idiopathic chronic pancreatitis. Clin Genet 59: 189-193, 2001.
8. Chen JM, Kukor Z, Le Maréchal C, Tóth M, Tsakiris L, Raguénès O, Férec C, Sahin-Tóth M. Evolution of trypsinogen activation peptides. Mol Biol Evol 20: 1767-1777, 2003.
9. Chen JM, Le Maréchal C, Lucas D, Raguénès O, Férec C. "Loss of function" mutations in the cationic trypsinogen gene (PRSS1) may act as a protective factor against pancreatitis. Mol Genet Metab 79: 67-70, 2003.
10. Comfort MW, Steinberg AG. Pedigree of a family with hereditary chronic relapsing pancreatitis. Gastroenterology 21: 54-63, 1952.
11. Dawra R, Sah RP, Dudeja V, Rishi L, Talukdar R, Garg P, Saluja AK. Intra-acinar trypsinogen activation mediates early stages of pancreatic injury but not inflammation in mice with acute pancreatitis. Gastroenterology 141: 2210-2217, 2011.
12. Férec C, Raguénès O, Salomon R, Roche C, Bernard JP, Guillot M, Quéré I, Faure C, Mercier B, Audrézet MP, Guillausseau PJ, Dupont C, Munnich A, Bignon JD, Le Bodic L. Mutations in the cationic trypsinogen gene and evidence for genetic heterogeneity in hereditary pancreatitis. J Med Genet 36: 228-232, 1999.
13. Gao F, Liu QC, Zhang S, Zhuang ZH, Lin CZ, Lin XH. PRSS1 intron mutations in patients with pancreatic cancer and chronic pancreatitis. Mol Med Rep 5: 449-451, 2012.
14. Gao F, Li YM, Hong GL, Xu ZF, Liu QC, He QL, Lin LQ, Weng SH. PRSS1_p Leu81Met mutation results in autoimmune pancreatitis. World J Gastroenterol 19: 3332-3338, 2013.
15. Geisz A, Hegyi P, Sahin-Tóth M. Robust autoactivation, chymotrypsin C independence and diminished secretion define a subset of hereditary pancreatitis-associated cationic trypsinogen mutants. FEBS J 280: 2888-2899, 2013.
16. Gorry MC, Gabbaizedeh D, Furey W, Gates LK Jr, Preston RA, Aston CE, Zhang Y, Ulrich C, Ehrlich GD, Whitcomb DC. Mutations in the cationic trypsinogen gene are associated with recurrent acute and chronic pancreatitis. Gastroenterology 113: 1063-1068, 1997.
17. Gou S, Yu J, Wang C, Liu T, Cui P, Li X. Three female familial cases of solid pseudopapillary tumors with a protease serine 1 gene mutation. Pancreas 42: 168-173, 2013.
18. Grocock CJ, Rebours V, Delhaye MN, Andrén-Sandberg A, Weiss FU, Mountford R, Harcus MJ, Niemczyck E, Vitone LJ, Dodd S, Jørgensen MT, Ammann RW, Schaffalitzky de Muckadell O, Butler JV, Burgess P, Kerr B, Charnley R, Sutton R, Raraty MG, Devière J, Whitcomb DC, Neoptolemos JP, Lévy P, Lerch MM, Greenhalf W; European Registry of Hereditary Pancreatitis, and Pancreatic Cancer. The variable phenotype of the p. A16V mutation of cationic trypsinogen (PRSS1) in pancreatitis families. Gut 59: 357-363, 2010.
19. Gullo L, Laghi L, Migliori M, Lucrezio L, Bianchi P, Randolph AE, Mantovani V, Bastagli L, Pezzilli R, Malesci A. SPINK1 and PRSS1 mutations in benign pancreatic hyperenzymemia. Pancreas 37: 31-35, 2008.
20. Hamoir C, Pepermans X, Piessevaux H, Jouret-Mourin A, Weynand B, Habyalimana JB, Leal T, Geubel A, Gigot JF, Deprez PH. Clinical and morphological characteristics of sporadic genetically determined pancreatitis as compared to idiopathic pancreatitis: higher risk of pancreatic cancer in CFTR variants. Digestion 87: 229-239, 2013.
21. 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; European Registry of Hereditary Pancreatitis, and Pancreatic Cancer (EUROPAC). Clinical and genetic characteristics of hereditary pancreatitis in Europe. Clin Gastroenterol Hepatol 2: 252-261, 2004.
22. Joergensen MT, Geisz A, Brusgaard K, Schaffalitzky de Muckadell OB, Hegyi P, Gerdes AM, Sahin-Tóth M. Intragenic duplication: a novel mutational mechanism in hereditary pancreatitis. Pancreas 40: 540-546, 2011.
23. Keiles S, Kammesheidt A. Identification of CFTR, PRSS1, and SPINK1 mutations in 381 patients with pancreatitis. Pancreas 33: 221-227, 2006.
24. Kereszturi E, Sahin-Tóth M. Intracellular autoactivation of human cationic trypsinogen mutants causes reduced trypsinogen secretion and acinar cell death. J Biol Chem 284: 33392-33399, 2009.
25. Kereszturi E, Szmola R, Kukor Z, Simon P, Weiss FU, Lerch MM, Sahin-Tóth M. Hereditary pancreatitis caused by mutation-induced misfolding of human cationic trypsinogen: a novel disease mechanism. Hum Mutat 30: 575-582, 2009.
26. LaRusch J, Barmada MM, Solomon S, Whitcomb DC. Whole exome sequencing identifies multiple, complex etiologies in an idiopathic hereditary pancreatitis kindred. JOP 13: 258-262, 2012.
27. Le Bodic L, Bignon JD, Raguénès O, Mercier B, Georgelin T, Schnee M, Soulard F, Gagne K, Bonneville F, Muller JY, Bachner L, Férec C. The hereditary pancreatitis gene maps to long arm of chromosome 7. Hum Mol Genet 5: 549-554, 1996.
28. Le Maréchal C, Chen JM, Quéré I, Raguénès O, Férec C, Auroux J. Discrimination of three mutational events that result in a disruption of the R122 primary autolysis site of the human cationic trypsinogen (PRSS1) by denaturing high performance liquid chromatography. BMC Genet 2: 19, 2001.
29. Le Maréchal C, Masson E, Chen JM, Morel F, Ruszniewski P, Levy P, Férec C. Hereditary pancreatitis caused by triplication of the trypsinogen locus. Nat Genet 38: 1372-1374, 2006.
30. Lee YJ, Kim KM, Choi JH, Lee BH, Kim GH, Yoo HW. High incidence of PRSS1 and SPINK1 mutations in Korean children with acute recurrent and chronic pancreatitis. J Pediatr Gastroenterol Nutr 52: 478-481, 2011.
31. Liu Q, Lin X, Liu J, Liu A, Gao F. The β409 C/T genotype of PRSS1 protects against pancreatic cancer in the Han Chinese population. Dig Dis Sci 57: 573-579, 2012.
32. Masamune A, Nakano E, Kume K, Takikawa T, Kakuta Y, Shimosegawa T. PRSS1 c.623G>C (p. G208A) variant is associated with pancreatitis in Japan. Gut 63, 366, 2014.
33. Masson E, Le Maréchal C, Chandak GR, Lamoril J, Bezieau S, Mahurkar S, Bhaskar S, Reddy DN, Chen JM, Férec C. Trypsinogen copy number mutations in patients with idiopathic chronic pancreatitis. Clin Gastroenterol Hepatol 6: 82-88, 2008.
34. Masson E, Le Maréchal C, Delcenserie R, Chen JM, Férec C. Hereditary pancreatitis caused by a double gain-of-function trypsinogen mutation. Hum Genet 123: 521-529, 2008.
35. Masson E, Hammel P, Garceau C, Bénech C, Quéméner-Redon S, Chen JM, Férec C. Characterization of two deletions of the CTRC locus. Mol Genet Metab 109: 296-300, 2013.
36. Németh BC, Wartmann T, Halangk W, Sahin-Tóth M. Autoactivation of mouse trypsinogens is regulated by chymotrypsin C via cleavage of the autolysis loop. J Biol Chem 288: 24049-24062, 2013.
37. Nemoda Z, Sahin-Tóth M. The tetra-aspartate motif in the activation peptide of human cationic trypsinogen is essential for autoactivation control but not for enteropeptidase recognition. J Biol Chem 280: 29645-29652, 2005.
38. Nemoda Z, Sahin-Tóth M. Chymotrypsin C (caldecrin) stimulates autoactivation of human cationic trypsinogen. J Biol Chem 281: 11879-11886, 2006.
39. Pandya A, Blanton SH, Landa B, Javaheri R, Melvin E, Nance WE, Markello T. Linkage studies in a large kindred with hereditary pancreatitis confirms mapping of the gene to a 16-cM region on 7q. Genomics 38: 227-230, 1996.
40. Pfützer R, Myers E, Applebaum-Shapiro S, Finch R, Ellis I, Neoptolemos J, Kant JA, Whitcomb DC. Novel cationic trypsinogen (PRSS1) N29T and R122C mutations cause autosomal dominant hereditary pancreatitis. Gut 50: 271-272, 2002.
41. Rebours V, Boutron-Ruault MC, Schnee M, Férec C, Le Maréchal C, Hentic O, Maire F, Hammel P, Ruszniewski P, Lévy P. The natural history of hereditary pancreatitis: a national series. Gut 58: 97-103, 2009.
42. Rosendahl J, Landt O, Bernadova J, Kovacs P, Teich N, Bödeker H, Keim V, Ruffert C, Mössner J, Kage A, Stumvoll M, Groneberg D, Krüger R, Luck W, Treiber M, Becker M, Witt H. CFTR, SPINK1, CTRC and PRSS1 variants in chronic pancreatitis: is the role of mutated CFTR overestimated? Gut 62: 582-592, 2013.
43. Rowen L, Koop BF, Hood L. The complete 685-kilobase DNA sequence of the human beta T cell receptor locus. Science 272: 1755-1762, 1996.
44. Sah RP, Dudeja V, Dawra RK, Saluja AK. Caerulein-induced chronic pancreatitis does not require intra-acinar activation of trypsinogen in mice. Gastroenterology 144: 1076-1085, 2013.
45. Scheele G, Bartelt D, Bieger W. Characterization of human exocrine pancreatic proteins by two-dimensional isoelectric focusing/sodium dodecyl sulfate gel electrophoresis. Gastroenterology 80: 461-473, 1981.
46. Schnúr A, Beer S, Witt H, Hegyi P, Sahin-Tóth M. Functional effects of 13 rare PRSS1 variants presumed to cause chronic pancreatitis. Gut 63: 337-343, 2014.
47. Selig L, Sack U, Gaiser S, Klöppel G, Savkovic V, Mössner J, Keim V, Bödeker H. Characterisation of a transgenic mouse expressing R122H human cationic trypsinogen. BMC Gastroenterol 6: 30, 2006.
48. Simon P, Weiss FU, Sahin-Tóth M, Parry M, Nayler O, Lenfers B, Schnekenburger J, Mayerle J, Domschke W, Lerch MM. 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, 2002.
49. Solomon S, Gelrud A, Whitcomb DC. Low penetrance pancreatitis phenotype in a Venezuelan kindred with a PRSS1 R122H mutation. JOP 14: 187-189, 2013.
50. Sultan M, Werlin S, Venkatasubramani N. Genetic prevalence and characteristics in children with recurrent pancreatitis. J Pediatr Gastroenterol Nutr 54: 645-650, 2012.
51. Szabó A, Sahin-Tóth M. Increased activation of hereditary pancreatitisassociated human cationic trypsinogen mutants in presence of chymotrypsin C. J Biol Chem 287: 20701-20710, 2012.
52. Szabó A, Sahin-Tóth M. Determinants of chymotrypsin C cleavage specificity in the calcium-binding loop of human cationic trypsinogen. FEBS J 279, 4283-4292, 2012.
53. Szmola R, Sahin-Tóth M. Chymotrypsin C (caldecrin) promotes degradation of human cationic trypsin: identity with Rinderknecht's enzyme Y. Proc Natl Acad Sci USA 104: 11227-11232, 2007.
54. Szmola R, Sahin-Tóth M. Uncertainties in the classification of human cationic trypsinogen (PRSS1) variants as hereditary pancreatitis-associated mutations. J Med Genet 47: 348-350, 2010.
55. Tautermann G, Ruebsamen H, Beck M, Dertinger S, Drexel H, Lohse P. R116C mutation of cationic trypsinogen in a Turkish family with recurrent pancreatitis illustrates genetic microheterogeneity of hereditary pancreatitis. Digestion 64: 226-232, 2001.
56. Teich N, Mössner J, Keim V. Mutations of the cationic trypsinogen in hereditary pancreatitis. Hum Mutat 12: 39-43, 1998.
57. Teich N, Ockenga J, Hoffmeister A, Manns M, Mössner J, Keim V. Chronic pancreatitis associated with an activation peptide mutation that facilitates trypsin activation. Gastroenterology 119: 461-465, 2000.
58. Teich N, Bauer N, Mössner J, Keim V. Mutational screening of patients with nonalcoholic chronic pancreatitis: identification of further trypsinogen variants. Am J Gastroenterol 97: 341-346, 2002.
59. Teich N, Le Maréchal C, Kukor Z, Caca K, Witzigmann H, Chen JM, Tóth M, Mössner J, Keim V, Férec C, Sahin-Tóth M. Interaction between trypsinogen isoforms in genetically determined pancreatitis: mutation E79K in cationic trypsin (PRSS1) causes increased transactivation of anionic trypsinogen (PRSS2). Hum Mutat 23: 22-31, 2004.
60. Teich N, Nemoda Z, Kohler H, Heinritz W, Mössner J, Keim V, Sahin-Tóth M. Gene conversion between functional trypsinogen genes PRSS1 and PRSS2 associated with chronic pancreatitis in a six-year-old girl. Hum Mutat 25: 343-347, 2005.
61. Teich N, Rosendahl J, Tóth M, Mössner J, Sahin-Tóth M. Mutations of human cationic trypsinogen (PRSS1) and chronic pancreatitis. Hum Mutat 27: 721-730, 2006.
62. Whitcomb DC, Preston RA, Aston CE, Sossenheimer MJ, Barua PS, Zhang Y, Wong-Chong A, White GJ, Wood PG, Gates LK Jr, Ulrich C, Martin SP, Post JC, Ehrlich GD. A gene for hereditary pancreatitis maps to chromosome 7q35. Gastroenterology 110: 1975-1980, 1996.
63. 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. Hereditary pancreatitis is caused by a mutation in the cationic trypsinogen gene. Nat Genet 14: 141-145, 1996.
64. Whitcomb DC, Larusch J, Krasinskas AM, Klei L, Smith JP, Brand RE, Neoptolemos JP, Lerch MM, Tector M, Sandhu BS, Guda NM, Orlichenko L; Alzheimer's Disease Genetics Consortium, Alkaade S, Amann ST, Anderson MA, Baillie J, Banks PA, Conwell D, Coté GA, Cotton PB, Disario J, Farrer LA, Forsmark CE, Johnstone M, Gardner TB, Gelrud A, Greenhalf W, Haines JL, Hartman DJ, Hawes RA, Lawrence C, Lewis M, Mayerle J, Mayeux R, Melhem NM, Money ME, Muniraj T, Papachristou GI, Pericak-Vance MA, Romagnuolo J, Schellenberg GD, Sherman S, Simon P, Singh VP, Slivka A, Stolz D, Sutton R, Weiss FU, Wilcox CM, Zarnescu NO, Wisniewski SR, O'Connell MR, Kienholz ML, Roeder K, Barmada MM, Yadav D, Devlin B. Common genetic variants in the CLDN2 and PRSS1-PRSS2 loci alter risk for alcohol-related and sporadic pancreatitis. Nat Genet 44: 1349-1354, 2012.
65. Witt H, Luck W, Becker M. A signal peptide cleavage site mutation in the cationic trypsinogen gene is strongly associated with chronic pancreatitis. Gastroenterology 117: 7-10, 1999.
66. Yadav D, Lowenfels AB. The epidemiology of pancreatitis and pancreatic cancer. Gastroenterology 144: 1252-1261, 2013.
67. Yilmaz B, Eki{dotless}z F, Karakaş E, Aykut A, Si{dotless}mşek Z, Çoban Ş, Onay H, Özki{dotless}nay F. A rare PRSS1 mutation in a Turkish family with hereditary chronic pancreatitis. Turk J Gastroenterol 23: 826-827, 2012.
68. Zeng K, Liu QC, Lin JH, Lin XH, Zhuang ZH, Gao F, Ou QS. Novel mutations of PRSS1 gene in patients with pancreatic cancer among Han population. Chin Med J (Engl) 124: 2065-2067, 2011.