Literature DB >> 22942235

Comprehensive functional analysis of chymotrypsin C (CTRC) variants reveals distinct loss-of-function mechanisms associated with pancreatitis risk.

Sebastian Beer1, Jiayi Zhou, András Szabó, Steven Keiles, Giriraj Ratan Chandak, Heiko Witt, Miklós Sahin-Tóth.   

Abstract

OBJECTIVE: The digestive enzyme chymotrypsin C (CTRC) protects against pancreatitis by promoting degradation of trypsinogen, thereby curtailing potentially harmful trypsinogen activation. Loss-of-function variants in CTRC increase the risk for chronic pancreatitis. The aim of the present study was to perform comprehensive functional analysis of all missense CTRC variants identified to date.
DESIGN: We investigated secretion, activity and degradation of 27 published and five novel CTRC mutants. We also assessed the effect of five mutants on endoplasmic reticulum (ER) stress.
RESULTS: None of the mutants exhibited a gain of function, such as increased secretion or activity. By contrast, 11 mutants showed marked loss of function, three mutants had moderate functional defects, whereas 18 mutants were functionally similar to wild-type CTRC. The functional deficiencies observed were diminished secretion, impaired catalytic activity and degradation by trypsin. Mutants with a secretion defect caused ER stress that was proportional to the loss in secretion. ER stress was not associated with loss-of-function phenotypes related to catalytic defect or proteolytic instability.
CONCLUSIONS: Pathogenic CTRC variants cause loss of function by three distinct but mutually non-exclusive mechanisms that affect secretion, activity and proteolytic stability. ER stress may be induced by a subset of CTRC mutants, but does not represent a common pathological mechanism of CTRC variants. This phenotypic dataset should aid in the classification of the clinical relevance of CTRC variants identified in patients with chronic pancreatitis.

Entities:  

Keywords:  Pancreatic Disease; Pancreatic Disorders; Pancreatic Enzymes; Pancreatic Physiology; Pancreatitis

Mesh:

Substances:

Year:  2012        PMID: 22942235      PMCID: PMC3660471          DOI: 10.1136/gutjnl-2012-303090

Source DB:  PubMed          Journal:  Gut        ISSN: 0017-5749            Impact factor:   23.059


  18 in total

1.  Pancreatitis-associated chymotrypsinogen C (CTRC) mutant elicits endoplasmic reticulum stress in pancreatic acinar cells.

Authors:  Richárd Szmola; Miklós Sahin-Tóth
Journal:  Gut       Date:  2009-11-30       Impact factor: 23.059

Review 2.  Genetic aspects of pancreatitis.

Authors:  David C Whitcomb
Journal:  Annu Rev Med       Date:  2010       Impact factor: 13.739

3.  Association of novel chymotrypsin C gene variations and haplotypes in patients with chronic pancreatitis in Chinese in Taiwan.

Authors:  Ming-Chu Chang; Yu-Ting Chang; Shu-Chen Wei; Po-Chin Liang; I-Shiow Jan; Yi-Ning Su; Chun-Hung Kuo; Jau-Min Wong
Journal:  Pancreatology       Date:  2009-04-29       Impact factor: 3.996

4.  Tropical calcific pancreatitis and its association with CTRC and SPINK1 (p.N34S) variants.

Authors:  Monique H M Derikx; Richard Szmola; Rene H M te Morsche; Santhosh Sunderasan; Ashok Chacko; Joost P H Drenth
Journal:  Eur J Gastroenterol Hepatol       Date:  2009-08       Impact factor: 2.566

Review 5.  Chronic pancreatitis: genetics and pathogenesis.

Authors:  Jian-Min Chen; Claude Férec
Journal:  Annu Rev Genomics Hum Genet       Date:  2009       Impact factor: 8.929

6.  Association of rare chymotrypsinogen C (CTRC) gene variations in patients with idiopathic chronic pancreatitis.

Authors:  Emmanuelle Masson; Jian-Min Chen; Virginie Scotet; Cédric Le Maréchal; Claude Férec
Journal:  Hum Genet       Date:  2008-01-03       Impact factor: 4.132

7.  Comprehensive screening of chymotrypsin C (CTRC) gene in tropical calcific pancreatitis identifies novel variants.

Authors:  Sumit Paliwal; Seema Bhaskar; K Radha Mani; D Nageshwar Reddy; G Venkat Rao; Shivaram Prasad Singh; Varghese Thomas; Giriraj Ratan Chandak
Journal:  Gut       Date:  2012-05-12       Impact factor: 23.059

8.  Chymotrypsin C (CTRC) variants that diminish activity or secretion are associated with chronic pancreatitis.

Authors:  Jonas Rosendahl; Heiko Witt; Richárd Szmola; Eesh Bhatia; Béla Ozsvári; Olfert Landt; Hans-Ulrich Schulz; Thomas M Gress; Roland Pfützer; Matthias Löhr; Peter Kovacs; Matthias Blüher; Michael Stumvoll; Gourdas Choudhuri; Péter Hegyi; René H M te Morsche; Joost P H Drenth; Kaspar Truninger; Milan Macek; Gero Puhl; Ulrike Witt; Hartmut Schmidt; Carsten Büning; Johann Ockenga; Andreas Kage; David Alexander Groneberg; Renate Nickel; Thomas Berg; Bertram Wiedenmann; Hans Bödeker; Volker Keim; Joachim Mössner; Niels Teich; Miklós Sahin-Tóth
Journal:  Nat Genet       Date:  2007-12-02       Impact factor: 38.330

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

Authors:  Eva Kereszturi; Richárd Szmola; Zoltán Kukor; Peter Simon; Frank Ulrich Weiss; Markus M Lerch; Miklós Sahin-Tóth
Journal:  Hum Mutat       Date:  2009-04       Impact factor: 4.878

10.  Glucocorticoids increase amylase mRNA levels, secretory organelles, and secretion in pancreatic acinar AR42J cells.

Authors:  C D Logsdon; J Moessner; J A Williams; I D Goldfine
Journal:  J Cell Biol       Date:  1985-04       Impact factor: 10.539

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  42 in total

1.  Variants in pancreatic carboxypeptidase genes CPA2 and CPB1 are not associated with chronic pancreatitis.

Authors:  Eriko Nakano; Andrea Geisz; Atsushi Masamune; Tetsuya Niihori; Shin Hamada; Kiyoshi Kume; Yoichi Kakuta; Yoko Aoki; Yoichi Matsubara; Karolin Ebert; Maren Ludwig; Markus Braun; David A Groneberg; Tooru Shimosegawa; Miklós Sahin-Tóth; Heiko Witt
Journal:  Am J Physiol Gastrointest Liver Physiol       Date:  2015-08-27       Impact factor: 4.052

2.  Variants in CPA1 are strongly associated with early onset chronic pancreatitis.

Authors:  Heiko Witt; Sebastian Beer; Jonas Rosendahl; Jian-Min Chen; Giriraj Ratan Chandak; Atsushi Masamune; Melinda Bence; Richárd Szmola; Grzegorz Oracz; Milan Macek; Eesh Bhatia; Sandra Steigenberger; Denise Lasher; Florence Bühler; Catherine Delaporte; Johanna Tebbing; Maren Ludwig; Claudia Pilsak; Karolin Saum; Peter Bugert; Emmanuelle Masson; Sumit Paliwal; Seema Bhaskar; Agnieszka Sobczynska-Tomaszewska; Daniel Bak; Ivan Balascak; Gourdas Choudhuri; D Nageshwar Reddy; G Venkat Rao; Varghese Thomas; Kiyoshi Kume; Eriko Nakano; Yoichi Kakuta; Tooru Shimosegawa; Lukasz Durko; András Szabó; Andrea Schnúr; Péter Hegyi; Zoltán Rakonczay; Roland Pfützer; Alexander Schneider; David Alexander Groneberg; Markus Braun; Hartmut Schmidt; Ulrike Witt; Helmut Friess; Hana Algül; Olfert Landt; Markus Schuelke; Renate Krüger; Bertram Wiedenmann; Frank Schmidt; Klaus-Peter Zimmer; Peter Kovacs; Michael Stumvoll; Matthias Blüher; Thomas Müller; Andreas Janecke; Niels Teich; Robert Grützmann; Hans-Ulrich Schulz; Joachim Mössner; Volker Keim; Matthias Löhr; Claude Férec; Miklós Sahin-Tóth
Journal:  Nat Genet       Date:  2013-08-18       Impact factor: 38.330

3.  Long-range electrostatic complementarity governs substrate recognition by human chymotrypsin C, a key regulator of digestive enzyme activation.

Authors:  Jyotica Batra; András Szabó; Thomas R Caulfield; Alexei S Soares; Miklós Sahin-Tóth; Evette S Radisky
Journal:  J Biol Chem       Date:  2013-02-19       Impact factor: 5.157

Review 4.  Genetic and phenotypic heterogeneity in tropical calcific pancreatitis.

Authors:  Sumit Paliwal; Seema Bhaskar; Giriraj R Chandak
Journal:  World J Gastroenterol       Date:  2014-12-14       Impact factor: 5.742

Review 5.  Insights into the genetic risk factors for the development of pancreatic disease.

Authors:  Zachary Zator; David C Whitcomb
Journal:  Therap Adv Gastroenterol       Date:  2017-01-05       Impact factor: 4.409

Review 6.  Genetic risk factors for pancreatic disorders.

Authors:  David C Whitcomb
Journal:  Gastroenterology       Date:  2013-06       Impact factor: 22.682

7.  Endoplasmic reticulum stress promotes amyloid-beta peptides production in RGC-5 cells.

Authors:  Bingqian Liu; Yingting Zhu; Jiayi Zhou; Yantao Wei; Chongde Long; Mengfei Chen; Yunlan Ling; Jian Ge; Yehong Zhuo
Journal:  Cell Stress Chaperones       Date:  2014-03-19       Impact factor: 3.667

8.  Inactivation of mesotrypsin by chymotrypsin C prevents trypsin inhibitor degradation.

Authors:  Vanda Toldi; András Szabó; Miklós Sahin-Tóth
Journal:  J Biol Chem       Date:  2020-02-03       Impact factor: 5.157

9.  Functional effects of 13 rare PRSS1 variants presumed to cause chronic pancreatitis.

Authors:  Andrea Schnúr; Sebastian Beer; Heiko Witt; Péter Hegyi; Miklós Sahin-Tóth
Journal:  Gut       Date:  2013-03-01       Impact factor: 23.059

10.  A Carboxyl Ester Lipase (CEL) Mutant Causes Chronic Pancreatitis by Forming Intracellular Aggregates That Activate Apoptosis.

Authors:  Xunjun Xiao; Gabrielle Jones; Wednesday A Sevilla; Donna B Stolz; Kelsey E Magee; Margaret Haughney; Amitava Mukherjee; Yan Wang; Mark E Lowe
Journal:  J Biol Chem       Date:  2016-09-20       Impact factor: 5.157

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