New insights into the pathways initiating and driving pancreatitis

Current Opinion in Gastroenterology

Volumn 32, Issue 5, 2016, Pages 429-435

  Gukovskaya, Anna S ^a   Pandol, Stephen J ^b   Gukovsky, Ilya ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

acute pancreatitis; autophagy; calcium; chronic pancreatitis; lysosomes; mitochondrial permeability transition pore

Indexed keywords

CALCIUM; SIMVASTATIN; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE;

ACINAR CELL; AUTOPHAGY; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL ORGANELLE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; EXPERIMENTAL PANCREATITIS; HUMAN; LYSOSOME; NONHUMAN; PANCREATITIS; REVIEW;

EID: 84978647655     PISSN: 02671379     EISSN: 15317056     Source Type: Journal    
DOI: 10.1097/MOG.0000000000000301     Document Type: Review

References (63)

1. Peery AF, Dellon ES, Lund J, et al. Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 2012; 143: 1179-1187
2. Pandol SJ, Saluja AK, Imrie CW, Banks PA. Acute pancreatitis: bench to the bedside. Gastroenterology 2007; 132: 1127-1151; Erratum: 133: 1056
3. Mareninova OA, Hermann K, French SW, et al. Impaired autophagic flux mediates acinar cell vacuole formation and trypsinogen activation in rodent models of acute pancreatitis. J Clin Invest 2009; 119: 3340-3355
4. Gukovskaya AS, Gukovsky I. Autophagy and pancreatitis. Am J Physiol Gastrointest Liver Physiol 2012; 303: G993-G1003
5. Mareninova OA, Sendler M, Malla SR, et al. Lysosome associated membrane proteins maintain pancreatic acinar cell homeostasis: sLAMP-2 deficient mice develop pancreatitis. Cell Mol Gastroenterol Hepatol 2015; 1:678?694.
6. Diakopoulos KN, Lesina M, Wormann S, et al. Impaired autophagy induces chronic atrophic pancreatitis in mice via sex- and nutrition-dependent processes. Gastroenterology 2015; 148: 626-638
7. Antonucci L, Fagman JB, Kim JY, et al. Basal autophagy maintains pancreatic acinar cell homeostasis and protein synthesis and prevents ER stress. Proc Natl Acad Sci U S A 2015; 112: E6166-E6174
8. Gukovsky I, Gukovskaya AS. Impaired autophagy triggers chronic pancreatitis: lessons from pancreas-specific Atg5 knockout mice. Gastroenterology 2015; 148: 501-505
9. Li N, WuX, Holzer RG, et al. Loss of acinar cell IKKalpha triggers spontaneous pancreatitis in mice. J Clin Invest 2013; 123: 2231-2243
10. Gukovsky I, Li N, Todoric J, et al. Inflammation, autophagy, and obesity: common features in the pathogenesis of pancreatitis and pancreatic cancer. Gastroenterology 2013; 144: 1199-1209
11. Messenger SW, Thomas DD, Cooley MM, et al. Early to late endosome trafficking controls secretion and zymogen activation in rodent and human pancreatic acinar cells. Cell Mol Gastroenterol Hepatol 2015; 1: 695-709
12. Hou Y, Ernst SA, Stuenkel EL, et al. Rab27A is present in mouse pancreatic acinar cells and is required for digestive enzyme secretion. PloS One 2015; 10: e0125596
13. Messenger SW, Falkowski MA, Thomas DD, et al. Vesicle associated membrane protein 8 (VAMP8)-mediated zymogen granule exocytosis is dependent on endosomal trafficking via the constitutive-like secretory pathway. J Biol Chem 2014; 289: 28040-28053
14. Saluja A, Hashimoto S, Saluja M, et al. Subcellular redistribution of lysosomal enzymes during caerulein-induced pancreatitis. Am J Physiol 1987; 253: G508-G516
15. Sherwood MW, Prior IA, Voronina SG, et al. Activation of trypsinogen in large endocytic vacuoles of pancreatic acinar cells. Proc Natl Acad Sci U S A 2007; 104: 5674-5679
16. Bernardi P, Rasola A, Forte M, Lippe G. The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology. Physiol Rev 2015; 95: 1111-1155
17. Mukherjee R, Mareninova OA, Odinokova IV, et al. Mechanism of mitochondrial permeability transition pore induction and damage in the pancreas: inhibition prevents acute pancreatitis by protecting production of ATP. Gut 2015; Jun 12. pii: gutjnl-2014-308553. doi: 10.1136/gutjnl-2014-308553
18. Jamieson JD, Palade GE. Intracellular transport of secretory proteins in the pancreatic exocrine cell. IV. Metabolic requirements. J Cell Biol 1968; 39: 589-603
19. Huang W, Cash N, Wen L, et al. Effects of the mitochondria-Targeted antioxidant mitoquinone in murine acute pancreatitis. Med Inflamm 2015; 2015: 901780
20. Logsdon CD, Ji B. The role of protein synthesis and digestive enzymes in acinar cell injury. Nat Rev Gastroenterol Hepatol 2013; 10: 362-370
21. Sah RP, Garg SK, Dixit AK, et al. Endoplasmic reticulum stress is chronically activated in chronic pancreatitis. J Biol Chem 2014; 289: 27551-27561
22. Balazs A, Hegyi P, Sahin-Toth M. Pathogenic cellular role of the p.L104P human cationic trypsinogen variant in chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 2016; 310: G477-G486
23. Nemeth BC, Sahin-Toth M. Human cationic trypsinogen (PRSS1) variants and chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 2014; 306: G466-G473
24. Beer S, Zhou J, Szabo A, et al. Comprehensive functional analysis of chymotrypsin C (CTRC) variants reveals distinct loss-of-function mechanisms associated with pancreatitis risk. Gut 2013; 62: 1616-1624
25. Whitcomb DC. Genetic aspects of pancreatitis. Ann Rev Med 2010; 61: 413-424
26. Lugea A, Waldron RT, Pandol SJ. Pancreatic adaptive responses in alcohol abuse: role of the unfolded protein response. Pancreatology 2015; 15: S1-S5
27. Lugea A, Tischler D, Nguyen J, et al. Adaptive unfolded protein response attenuates alcohol-induced pancreatic damage. Gastroenterology 2011; 140: 987-997
28. Pandol SJ, Gorelick FS, Lugea A. Environmental and genetic stressors and the unfolded protein response in exocrine pancreatic function: a hypothesis. Front Physiol 2011; 2: 8
29. LaRusch J, Lozano-Leon A, Stello K, et al. The common chymotrypsinogen C (CTRC) variant G60G (C.180T) increases risk of chronic pancreatitis but not recurrent acute pancreatitis in a North American population. Clin Trans Gastroenterol 2015; 6: e68
30. Petersen OH, Tepikin AV. Polarized calcium signaling in exocrine gland cells. Ann Rev Physiol 2008; 70: 273-299
31. Pandol SJ, Schoeffield MS, Fimmel CJ, Muallem S. The agonist-sensitive calcium pool in the pancreatic acinar cell. Activation of plasma membrane Ca2+ influx mechanism. J Biol Chem 1987; 262: 16963-16968
32. Muallem S, Schoeffield MS, Fimmel CJ, Pandol SJ. Agonist-sensitive calcium pool in the pancreatic acinar cell. I. Permeability properties. Am J Physiol 1988; 255: G221-G228
33. Muallem S, Schoeffield MS, Fimmel CJ, Pandol SJ. Agonist-sensitive calcium pool in the pancreatic acinar cell. II. Characterization of reloading. Am J Physiol 1988; 255: G229-G235
34. Mukherjee R, Criddle DN, Gukovskaya A, et al. Mitochondrial injury in pancreatitis. Cell Calcium 2008; 44: 14-23
35. Criddle DN, Murphy J, Fistetto G, et al. Fatty acid ethyl esters cause pancreatic calcium toxicity via inositol trisphosphate receptors and loss of ATP synthesis. Gastroenterology 2006; 130: 781-793
36. Gerasimenko JV, Gerasimenko OV, Petersen OH. The role of Ca2+ in the pathophysiology of pancreatitis. J Physiol 2014; 592: 269-280
37. Parekh AB, Putney JW Jr. Store-operated calcium channels. Physiol Rev 2005; 85: 757-810
38. Prakriya M, Feske S, Gwack Y, et al. Orai1 is an essential pore subunit of the CRAC channel. Nature 2006; 443: 230-233
39. Son A, Park S, Shin DM, et al. Orai1 and STIM1 in ER/PM junctions: roles in pancreatic cell function and dysfunction. Am J Physiol Cell Physiol 2016; 310: C414-C422
40. Gerasimenko JV, Gryshchenko O, Ferdek PE, et al. Ca2+ release-activated Ca2+ channel blockade as a potential tool in antipancreatitis therapy. Proc Natl Acad Sci U S A 2013; 110: 13186-13191
41. Criddle DN, Gerasimenko JV, Baumgartner HK, et al. Calcium signalling and pancreatic cell death: apoptosis or necrosis?. Cell Death Differ 2007; 14: 1285-1294
42. Kim MS, Hong JH, Li Q, et al. Deletion of TRPC3 in mice reduces storeoperated Ca2+ influx and the severity of acute pancreatitis. Gastroenterology 2009; 137: 1509-1517
43. Wen L, Voronina S, Javed MA, et al. Inhibitors of ORAI1 prevent cytosolic calcium-associated injury of human pancreatic acinar cells and acute pancreatitis in 3 mouse models. Gastroenterology 2015; 149: 481-492
44. Huang W, Cane MC, Mukherjee R, et al. Caffeine protects against experimental acute pancreatitis by inhibition of inositol 1, 4, 5-Trisphosphate receptor-mediated Ca2+ release. Gut 2015. [Epub ahead of print]
45. Gerasimenko JV, Lur G, Sherwood MW, et al. Pancreatic protease activation by alcohol metabolite depends on Ca2+ release via acid store IP3 receptors. Proc Natl Acad Sci U S A 2009; 106: 10758-10763
46. Maleth J, Balazs A, Pallagi P, et al. Alcohol disrupts levels and function of the cystic fibrosis transmembrane conductance regulator to promote development of pancreatitis. Gastroenterology 2015; 148: 427-439
47. Hegyi P, Pandol S, Venglovecz V, Rakonczay Z Jr. The acinar-ductal tango in the pathogenesis of acute pancreatitis. Gut 2011; 60: 544-552
48. Jin S, Orabi AI, Le T, et al. Exposure to radiocontrast agents induces pancreatic inflammation by activation of nuclear factor-kappaB, calcium signaling, and calcineurin. Gastroenterology 2015; 149: 753-764
49. Voronina S, Collier D, Chvanov M, et al. The role of Ca2+ influx in endocytic vacuole formation in pancreatic acinar cells. Biochem J 2015; 465: 405-412
50. Song L, Wormann S, Ai J, et al. BCL3 reduces the sterile inflammatory response in pancreatic and biliary tissues. Gastroenterology 2016; 150: 499-512
51. Sendler M, Beyer G, Mahajan UM, et al. Complement Component 5 mediates development of fibrosis, via activation of stellate cells, in 2 mouse models of chronic pancreatitis. Gastroenterology 2015; 149: 765-776
52. Habtezion A. Inflammation in acute and chronic pancreatitis. Curr Opin Gastroenterol 2015; 31: 395-399
53. Huang W, Szatmary P, Wan M, et al. Translational insights into peroxisome proliferator-activated receptors in experimental acute pancreatitis. Pancreas 2016; 45: 167-178
54. Merza M, Hartman H, Rahman M, et al. Neutrophil extracellular traps induce trypsin activation, inflammation, and tissue damage in mice with severe acute pancreatitis. Gastroenterology 2015; 149: 1920-1931
55. Korhonen JT, Dudeja V, Dawra R, et al. Neutrophil extracellular traps provide a grip on the enigmatic pathogenesis of acute pancreatitis. Gastroenterology 2015; 149: 1682-1685
56. Leppkes M, Maueroder C, Hirth S, et al. Externalized decondensed neutrophil chromatin occludes pancreatic ducts and drives pancreatitis. Nat Commun 2016; 7: 10973
57. Sorensen OE, Borregaard N. Neutrophil extracellular traps: the dark side of neutrophils. J Clin Invest 2016; 126: 1612-1620
58. Gukovskaya AS, Vaquero E, Zaninovic V, et al. Neutrophils and NADPH oxidase mediate intrapancreatic trypsin activation in murine experimental acute pancreatitis. Gastroenterology 2002; 122: 974-984
59. Nawaz H, Koutroumpakis E, Easler J, et al. Elevated serum triglycerides are independently associated with persistent organ failure in acute pancreatitis. Am J Gastroenterol 2015; 110: 1497-1503
60. Patel K, Trivedi RN, Durgampudi C, et al. Lipolysis of visceral adipocyte triglyceride by pancreatic lipases converts mild acute pancreatitis to severe pancreatitis independent of necrosis and inflammation. Am J Pathol 2015; 185: 808-819
61. Noel P, Patel K, Durgampudi C, et al. Peripancreatic fat necrosis worsens acute pancreatitis independent of pancreatic necrosis via unsaturated fatty acids increased in human pancreatic necrosis collections. Gut 2016; 65: 100-111
62. Patel K, Durgampudi C, Noel P, et al. Fatty acid ethyl esters are less toxic than their parent fatty acids generated during acute pancreatitis. AmJ Pathol 2016; 186: 874-884
63. Wu BU, Pandol SJ, Liu IL. Simvastatin is associated with reduced risk of acute pancreatitis: findings from a regional integrated healthcare system. Gut 2015; 64: 133-138