Acinar cell membrane disruption is an early event in experimental acute pancreatitis in rats

Pancreas

Volumn 35, Issue 4, 2007, Pages

  Müller, Michael W ^a   McNeil, Paul L ^b   Büchler, Peter ^c   Ceyhan, Güralp O ^c   Wolf Hieber, Elke ^d   Adler, Guido ^d   Beger, Hans G ^d   Büchler, Markus W ^c   Friess, Helmut ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

Acute pancreatitis; Cerulein; Membrane disruption; Rats; Taurocholate

Indexed keywords

ALBUMIN; BOMBESIN; CALCIUM ION; CERULETIDE; IMMUNOGLOBULIN G; PILOCARPINE;

ACINAR CELL; ACUTE PANCREATITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL DISRUPTION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ACUTE DISEASE; ANIMALS; CAERULEIN; CAPILLARY PERMEABILITY; CELL MEMBRANE; CYTOPLASM; DISEASE MODELS, ANIMAL; EDEMA; IMMUNOGLOBULIN G; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; PANCREAS, EXOCRINE; PANCREATITIS; RATS; RATS, SPRAGUE-DAWLEY; SERUM ALBUMIN; TAUROCHOLIC ACID; TIME FACTORS; VACUOLES;

EID: 37349096600     PISSN: 08853177     EISSN: 15364828     Source Type: Journal    
DOI: 10.1097/mpa.0b013e318120024c     Document Type: Article

References (70)

1. Mayerle J, Hlouschek V, Lerch MM. Current management of acute pancreatitis. Nat Clin Pract Gastroenterol Hepatol. 2005;2(10):473-483.
2. Beger HG, Bittner R, Block S, et al. Bacterial contamination of pancreatic necrosis. A prospective clinical study. Gastroenterology. 1986;91(2):433-438.
3. Kauste A, Hockerstedt K, Ahonen J, et al. Peritoneal lavage as a primary treatment in acute fulminant pancreatitis. Surg Gynecol Obstet. 1983;156(4)458-463.
4. Werner J, Feuerbach S, Uhl W, et al. Management of acute pancreatitis: from surgery to interventional intensive care. Gut. 2005;54(3):426-436.
5. Kloppel G, Dreyer T, Willemer S, et al. Human acute pancreatitis: its pathogenesis in the light of immunocytochemical and ultrastructural findings in acinar cells. Virchows Arch A Pathol Anat Histol. 1986;409(6):791-803.
6. Ohlsson K, Eddeland A. Release of proteolytic enzymes in bile-induced pancreatitis in dogs. Gastroenterology. 1975;69(3):668-675.
7. Adler G, Bieger W, Kern HF. Amino acid transport in the rat exocrine pancreas. III. Effect of maximal and supramaximal hormonal stimulation in vivo. Cell Tissue Res. 1978;194(3):447-462.
8. Adler G, Rohr G, Kern HF. Alteration of membrane fusion as a cause of acute pancreatitis in the rat. Dig Dis Sci. 1982;27(11):993-1002.
9. Watanabe O, Baccino FM, Steer ML, et al. Supramaximal caerulein stimulation and ultrastructure of rat pancreatic acinar cell: early morphological changes during development of experimental pancreatitis. Am J Physiol. 1984;246(4 Pt 1):G457-G467.
10. Lerch MM, Saluja AK, Dawra R, et al. Acute necrotizing pancreatitis in the opossum: earliest morphological changes involve acinar cells. Gastroenterology. 1992;103(1):205-213.
11. McNeil PL. Cellular and molecular adaptations to injurious mechanical stress. Trends Cell Biol. 1993;3(9):302-307.
12. McNeil PL, Ito S. Gastrointestinal cell plasma membrane wounding and resealing in vivo. Gastroenterology. 1989;96(5 Pt 1):1238-1248.
13. McNeil PL, Khakee R. Disruptions of muscle fiber plasma membranes. Role in exercise-induced damage. Am J Pathol. 1992;140(5):1097-1109.
14. Bansal D, Miyake K, Vogel SS, et al. Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature. 2003;423(6936):168-172.
15. Baniukiewicz AA, Dlugosz JW, Gabryelewicz A. The lysosomal hydrolases in the rat pancreas after maximal or supramaximal stimulation with cerulein. Int J Pancreatol. 1994;16(1):71-79.
16. Lampel M, Kern HF. Acute interstitial pancreatitis in the rat induced by excessive doses of a pancreatic secretagogue. Virchows Arch A Pathol Anat Histol. 1977;373(2):97-117.
17. Saikatsu S, Ikeno K, Hanada Y, et al. Intravenous injection of caerulein or cholecystokinin increases the parotid-type and pancreatic-type amylase in the serum of rats. Shika Kiso Igakkai Zasshi. 1989;31(5):592-596.
18. Wisner JR Jr, Ozawa S, Renner IG. Pancreatic exocrine function in unconscious rats treated with submaximal, maximal, and supramaximal doses of bombesin tetradecapeptide. Pancreas. 1989;4(1):83-89.
19. Heinkel K. The rat as experimental animal in experimental diagnosis of pancreas. II. Production of acute hemorrhagic pancreatitis by injection of bile acid into ductus pancreaticus. Klin Wochenschr. 1953;31(31-34):815.
20. Cotran KS, Karnovsky MJ. Vascular leakage induced by horseradish peroxidase in the rat. Proc Soc Exp Biol Med. 1967;126(2):557-561.
21. Vegge T, Haye R. Vascular reactions to horseradish peroxidase in the guinea pig. Histochemistry. 1977;53(3):217-222.
22. Geuze HJ, Slot JW, van der Ley PA, et al. Use of colloidal gold particles in double-labeling immunoelectron microscopy of ultrathin frozen tissue sections. J Cell Biol. 1981;89(3):653-665.
23. Clarke MS, Khakee R, McNeil PL. Loss of cytoplasmic basic fibroblast growth factor from physiologically wounded myofibers of normal and dystrophic muscle. J Cell Sci. 1993;106(Pt 1):121-133.
24. Yu QC, McNeil PL. Transient disruptions of aortic endothelial cell plasma membranes. Am J Pathol. 1992;141(6):1349-1360.
25. Fein A, Terasaki M. Rapid increase in plasma membrane chloride permeability during wound resealing in starfish oocytes. J Gen Physiol. 2005;126(2):151-159.
26. McNeil PL, Terasaki M. Coping with the inevitable: how cells repair a torn surface membrane. Nat Cell Biol. 2001;3(5):E124-E129.
27. McNeil PL, Vogel SS, Miyake K, et al. Patching plasma membrane disruptions with cytoplasmic membrane. J Cell Sci. 2000;113(Pt 11):1891-1902.
28. Terasaki M, Miyake K, McNeil PL. Large plasma membrane disruptions are rapidly resealed by Ca2+-dependent vesicle-vesicle fusion events. J Cell Biol. 1997;139(1):63-74.
29. Miyake K, McNeil PL. Mechanical injury and repair of cells. Crit Care Med. 2003;31(8 suppl):S496-S501.
30. McNeil PL, Kirchhausen T. An emergency response team for membrane repair. Nat Rev Mol Cell Biol. 2005;6(6):499-505.
31. McNeil PL, Steinhardt RA. Loss, restoration, and maintenance of plasma membrane integrity. J Cell Biol. 1997;137(1):1-4.
32. Bockman DE, Guo J, Muller MW, et al. Cell wounding in early experimental acute pancreatitis. Lab Invest. 2004;84(3):362-367.
33. Muller MW, Bockman DE, McNeil PL, et al. Membrane injuries of pancreatic acinar cells are the first changes in early stage acute experimental pancreatitis. Langenbecks Arch Chir Suppl Kongressbd. 1998;115(suppl I):421-425.
34. Cotran RS, Karnovsky MJ, Goth A. Resistance of Wistar-Furth rats to the mast cell-damaging effect of horseradish peroxidase. J Histochem Cytochem. 1968;16(5):382-383.
35. Brackett KA, Crocket A, Joffe SN. Ultrastructure of early development of acute pancreatitis in the rat. Dig Dis Sci. 1983;28(1):74-84.
36. Jeraldo TL, Coutu JA, Verdier PA, et al. Fundamental cellular heterogeneity of the exocrine pancreas. J Histochem Cytochem. 1996;44(3):215-220.
37. Koike H, Steer ML, Meldolesi J. Pancreatic effects of ethionine: blockade of exocytosis and appearance of crinophagy and autophagy precede cellular necrosis. Am J Physiol. 1982;242(4):G297-G307.
38. Saluja A, Saluja M, Villa A, et al. Pancreatic duct obstruction in rabbits causes digestive zymogen and lysosomal enzyme colocalization. J Clin Invest. 1989;84(4):1260-1266.
39. Willemer S, Bialek R, Adler G. Localization of lysosomal and digestive enzymes in cytoplasmic vacuoles in caerulein-pancreatitis. Histochemistry. 1990;94(2):161-170.
40. McEntee G, Leahy A, Cottell D, et al. Three-dimensional morphological study of the pancreatic microvasculature in caerulein-induced experimental pancreatitis. Br J Surg. 1989;76(8):853-855.
41. Gress TM, Arnold R, Adler G. Structural alterations of pancreatic microvasculature in cerulein-induced pancreatitis in the rat. Res Exp Med (Berl). 1990;190(6):401-412.
42. Grady T, Mah'Moud M, Otani T, et al. Zymogen proteolysis within the pancreatic acinar cell is associated with cellular injury. Am J Physiol. 1998;275(5 Pt 1):G1010-G1017.
43. Powers RE, Grady T, Orchard JL, et al. Different effects of hyperstimulation by similar classes of secretagogues on the exocrine pancreas. Pancreas. 1993;8(1):58-63.
44. Nevalainen TJ. Effects of pilocarpine stimulation on rat pancreatic acinar cells. An electron microscopic study with morphometric analysis. Acta Pathol Microbiol Scand Suppl. 1970;210(suppl 210):1.
45. Adler G, Kern HF, Pan GZ, et al. Secretagogue-induced membrane alterations in dispersed acini from rat pancreas. Eur J Cell Biol. 1984;33(2):234-241.
46. Hirano T, Manabe T, Tobe T. Cellular alterations of parotid gland of rats with acute pancreatitis induced by cerulein. Int J Pancreatol. 1991;10(3-4):217-227.
47. Donaldson LA, Williams RW, Schenk WG, Jr. Experimental pancreatitis: effect of plasma and dextran on pancreatic blood flow. Surgery. 1978;84(3):313-321.
48. Kelly DM, McEntee GP, Delaney C, et al. Temporal relationship of acinar and microvascular changes in caerulein-induced pancreatitis. Br J Surg. 1993;80(9):1174-1176.
49. Sanfey H, Cameron JL. Increased capillary permeability: an early lesion in acute pancreatitis. Surgery. 1984;96(3):485-491.
50. Klar E, Messmer K, Warshaw AL, et al. Pancreatic ischaemia in experimental acute pancreatitis: mechanism, significance and therapy. Br J Surg. 1990;77(11):1205-1210.
51. Raraty M, Ward J, Erdemli G, et al. Calcium-dependent enzyme activation and vacuole formation in the apical granular region of pancreatic acinar cells. Proc Natl Acad Sci U S A. 2000;97(24):13126-13131.
52. McNeil PL. Repairing a torn cell surface: make way, lysosomes to the rescue. J Cell Sci. 2002;115(Pt 5):873-879.
53. McNeil PL, Steinhardt RA. Plasma membrane disruption: repair, prevention, adaptation. Annu Rev Cell Dev Biol. 2003;19:697-731.
54. Bakker AC, Webster P, Jacob WA, et al. Homotypic fusion between aggregated lysosomes triggered by elevated "Ca2+"i in fibroblasts. J Cell Sci. 1997;110(Pt 18):2227-2238.
55. Rodriguez A, Webster P, Ortego J, et al. Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J Cell Biol. 1997;137(1):93-104.
56. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 2001;106(2):157-169.
57. Steinhardt RA, Bi G, Alderton JM. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science. 1994;263(5145):390-393.
58. McNeil PL, Baker MM. Cell surface events during resealing visualized by scanning-electron microscopy. Cell Tissue Res. 2001;304(1):141-146.
59. Togo T, Alderton JM, Bi GQ, et al. The mechanism of facilitated cell membrane resealing. J Cell Sci. 1999;112(Pt 5):719-731.
60. Bruzzone R. The molecular basis of enzyme secretion. Gastroenterology. 1990;99(4):1157-1176.
61. Muallem S. Calcium transport pathways of pancreatic acinar cells. Annu Rev Physiol. 1989;51:83-105.
62. Ochs DL, Korenbrot JI, Williams JA. Relation between free cytosolic calcium and amylase release by pancreatic acini. Am J Physiol. 1985;249(3 Pt 1):G389-G398.
63. Frick TW, Spycher MA, Heitz PU, et al. Hypercalcaemia and pancreatic ultrastructure in cats. Eur J Surg. 1992;158(5):289-294.
64. Frick TW, Hailemariam S, Heitz PU, et al. Acute hypercalcemia induces acinar cell necrosis and intraductal protein precipitates in the pancreas of cats and guinea pigs. Gastroenterology. 1990;98(6):1675-1681.
65. Mithofer K, Fernandez-del CC, Frick TW, et al. Acute hypercalcemia causes acute pancreatitis and ectopic trypsinogen activation in the rat. Gastroenterology. 1995;109(1):239-246.
66. Rinderknecht H. Activation of pancreatic zymogens. Normal activation, premature intrapancreatic activation, protective mechanisms against inappropriate activation. Dig Dis Sci. 1986;31(3):314-321.
67. Frick TW, Fernandez-del CC, Bimmler D, et al. Elevated calcium and activation of trypsinogen in rat pancreatic acini. Gut. 1997;41(3):339-343.
68. Willemer S, Bialek R, Arnold R, et al. Cerulein-induced acute pancreatitis in rats: evidence for reduced calcium affinity of secretory granule membranes. Res Exp Med (Berl). 1990;190(6):413-421.
69. Grady T, Liang P, Ernst SA, et al. Chemokine gene expression in rat pancreatic acinar cells is an early event associated with acute pancreatitis. Gastroenterology. 1997;113(6):1966-1975.
70. Kusske AM, Rongione AJ, Reber HA. Cytokines and acute pancreatitis. Gastroenterology. 1996;110(2):639-642.