Early to Late Endosome Trafficking Controls Secretion and Zymogen Activation in Rodent and Human Pancreatic Acinar Cells

Cellular and Molecular Gastroenterology and Hepatology

Volumn 1, Issue 6, 2015, Pages 695-709

  Messenger, Scott W ^a   Thomas, Diana D H ^a   Cooley, Michelle M ^a   Jones, Elaina K ^a   Falkowski, Michelle A ^a   August, Benjamin K ^a   Fernandez, Luis A ^b   Gorelick, Fred S ^c,d   Groblewski, Guy E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

Endosome; Pancreatitis; PIKfyve; Trypsin

Indexed keywords

BILE ACID; CHOLECYSTOKININ OCTAPEPTIDE; ENZYME PRECURSOR; GUANOSINE DIPHOSPHATE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; RAB PROTEIN; RAB11A PROTEIN; TOXIN; TRYPSINOGEN; UNCLASSIFIED DRUG;

ACINAR CELL; ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; ENDOSOME; EXOCYTOSIS; HUMAN; HUMAN CELL; LYSOSOME; NONHUMAN; PANCREATITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SMOKING;

EID: 84944472902     PISSN: None     EISSN: 2352345X     Source Type: Journal    
DOI: 10.1016/j.jcmgh.2015.08.002     Document Type: Article

References (47)

1. Saluja A., Hashimoto S., Saluja M., et al. Subcellular redistribution of lysosomal enzymes during caerulein-induced pancreatitis. Am J Physiol 1987, 253:G508-G516.
2. Gukovsky I., Gukovskaya A.S., Blinman T.A., et al. Early NF-kappaB activation is associated with hormone-induced pancreatitis. Am J Physiol 1998, 275:G1402-G1414.
3. Saluja A.K., Lerch M.M., Phillips P.A., et al. Why does pancreatic overstimulation cause pancreatitis?. Annu Rev Physiol 2007, 69:249-269.
4. Di Paolo G., De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006, 443:651-657.
5. Toker A., Cantley L.C. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 1997, 387:673-676.
6. Gukovsky I., Cheng J.H., Nam K.J., et al. Phosphatidylinositide 3-kinase gamma regulates key pathologic responses to cholecystokinin in pancreatic acinar cells. Gastroenterology 2004, 126:554-566.
7. Singh V.P., Saluja A.K., Bhagat L., et al. Phosphatidylinositol 3-kinase-dependent activation of trypsinogen modulates the severity of acute pancreatitis. J Clin Invest 2001, 108:1387-1395.
8. 2+-ATPase. Am J Physiol Gastrointest Liver Physiol 2004, 287:G1200-G1212.
9. Ho C.Y., Alghamdi T.A., Botelho R.J. Phosphatidylinositol-3,5-bisphosphate: no longer the poor PIP2. Traffic 2012, 13:1-8.
10. Zolov S.N., Bridges D., Zhang Y., et al. In vivo, Pikfyve generates PI(3,5)P2, which serves as both a signaling lipid and the major precursor for PI5P. Proc Natl Acad Sci USA 2012, 109:17472-17477.
11. Castle J.D., Castle A.M. Two regulated secretory pathways for newly synthesized parotid salivary proteins are distinguished by doses of secretagogues. J Cell Sci 1996, 109:2591-2599.
12. Messenger S.W., Falkowski M.A., Thomas D.D.H., 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.
13. (2+)-stimulated secretion in permeabilized acinar cells. J Biol Chem 2001, 276:28866-28872.
14. Messenger S.W., Thomas D.D.H., Falkowski M.A., et al. Tumor protein D52 controls trafficking of an apical endolysosomal secretory pathway in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 2013, 305:G439-G452.
15. Mareninova O.A., Hermann K., French S.W., 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.
16. Kawabata S., Miura T., Morita T., et al. Highly sensitive peptide-4-methylcoumaryl-7-amide substrates for blood-clotting proteases and trypsin. Eur J Biochem FEBS 1988, 172:17-25.
17. Mach L., Mort J.S., Glössl J. Maturation of human procathepsin B. Proenzyme activation and proteolytic processing of the precursor to the mature proteinase, in vitro, are primarily unimolecular processes. J Biol Chem 1994, 269:13030-13035.
18. 2+-sensitive CRHSP-28-binding protein in pancreatic acinar cells. J Biol Chem 2002, 277:35496-35502.
19. Kaspar K.M., Thomas D.D.H., Taft W.B., et al. CaM kinase II regulation of CRHSP-28 phosphorylation in cultured mucosal T84 cells. Am J Physiol Gastrointest Liver Physiol 2003, 285:G1300-G1309.
20. Chaudhuri A., Kolodecik T.R., Gorelick F.S. Effects of increased intracellular cAMP on carbachol-stimulated zymogen activation, secretion, and injury in the pancreatic acinar cell. Am J Physiol Gastrointest Liver Physiol 2005, 288:G235-G243.
21. Ricordi C., Lacy P.E., Finke E.H., et al. Automated method for isolation of human pancreatic islets. Diabetes 1988, 37:413-420.
22. Jefferies H.B.J., Cooke F.T., Jat P., et al. A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 2008, 9:164-170.
23. Cai X., Xu Y., Cheung A.K., et al. PIKfyve, a class III PI kinase, is the target of the small molecular IL-12/IL-23 inhibitor apilimod and a player in Toll-like receptor signaling. Chem Biol 2013, 20:912-921.
24. Osborne S.L., Wen P.J., Boucheron C., et al. PIKfyve negatively regulates exocytosis in neurosecretory cells. J Biol Chem 2008, 283:2804-2813.
25. Liu Y., Lai Y.-C., Hill E.V., et al. Phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) is an AMPK target participating in contraction-stimulated glucose uptake in skeletal muscle. Biochem J 2013, 455:195-206.
26. De Lisle R.C., Williams J.A. Zymogen granule acidity is not required for stimulated pancreatic protein secretion. Am J Physiol 1987, 253:G711-719.
27. Sbrissa D., Ikonomov O.C., Deeb R., et al. Phosphatidylinositol 5-phosphate biosynthesis is linked to PIKfyve and is involved in osmotic response pathway in mammalian cells. J Biol Chem 2002, 277:47276-47284.
28. Cabezas A., Pattni K., Stenmark H. Cloning and subcellular localization of a human phosphatidylinositol 3-phosphate 5-kinase, PIKfyve/Fab1. Gene 2006, 371:34-41.
29. Rink J., Ghigo E., Kalaidzidis Y., et al. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
30. Jing J., Prekeris R. Polarized endocytic transport: the roles of Rab11 and Rab11-FIPs in regulating cell polarity. Histol Histopathol 2009, 24:1171-1180.
31. Ceresa B.P., Lotscher M., Schmid S.L. Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q79l)-induced changes in endosome geometry. J Biol Chem 2001, 276:9649-9654.
32. Ren M., Xu G., Zeng J., et al. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 1998, 95:6187-6192.
33. 2+-dependent phosphorylation modulates lysosomal membrane protein trafficking to the plasma membrane. Am J Physiol Cell Physiol 2010, 298:C725-739.
34. Wartmann T., Mayerle J., Kähne T., et al. Cathepsin L inactivates human trypsinogen, whereas cathepsin L-deletion reduces the severity of pancreatitis in mice. Gastroenterology 2010, 138:726-737.
35. Halangk W., Lerch M.M., Brandt-Nedelev B., et al. Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J Clin Invest 2000, 106:773-781.
36. Orlichenko L., Stolz D.B., Noel P., et al. ADP-ribosylation factor 1 protein regulates trypsinogen activation via organellar trafficking of procathepsin B protein and autophagic maturation in acute pancreatitis. J Biol Chem 2012, 287:24284-24293.
37. Arvan P., Castle J.D. Phasic release of newly synthesized secretory proteins in the unstimulated rat exocrine pancreas. J Cell Biol 1987, 104:243-252.
38. Otani T., Chepilko S.M., Grendell J.H., et al. Codistribution of TAP and the granule membrane protein GRAMP-92 in rat caerulein-induced pancreatitis. Am J Physiol 1998, 275:G999-G1009.
39. Hofbauer B., Saluja A.K., Lerch M.M., et al. Intra-acinar cell activation of trypsinogen during caerulein-induced pancreatitis in rats. Am J Physiol 1998, 275:G352-G362.
40. De Lisle R.C. Altered posttranslational processing of glycoproteins in cerulein-induced pancreatitis. Exp Cell Res 2005, 308:101-113.
41. Waterford S.D., Kolodecik T.R., Thrower E.C., et al. Vacuolar ATPase regulates zymogen activation in pancreatic acini. J Biol Chem 2005, 280:5430-5434.
42. Hurtado-Lorenzo A., Skinner M., El Annan J., et al. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 2006, 8:124-136.
43. Ikonomov O.C., Sbrissa D., Foti M., et al. PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol Biol Cell 2003, 14:4581-4591.
44. 1-V(o) sector interactions and activates the V-ATPase. Mol Biol Cell 2014, 25:1251-1262.
45. Braulke T., Bonifacino J.S. Sorting of lysosomal proteins. Biochim Biophys Acta 2009, 1793:605-614.
46. Rojas R., van Vlijmen T., Mardones G.A., et al. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 2008, 183:513-526.
47. Gukovskaya A.S., Gukovsky I. Autophagy and pancreatitis. Am J Physiol Gastrointest Liver Physiol 2012, 303:G993-G1003.