Severe acute pancreatitis and reduced acinar cell apoptosis in the exocrine pancreas of mice deficient for the Cx32 gene

Gastroenterology

Volumn 124, Issue 2, 2003, Pages 481-493

  Frossard, Jean Louis ^a   Rubbia Brandt, Laura ^b   Wallig, Matthew A ^c   Benathan, Messod ^d   Ott, Thomas ^e   Morel, Philippe ^a   Hadengue, Antoine ^a   Suter, Susanne ^a   Willecke, Klaus ^e   Chanson, Marc ^a,f  

^a UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^e UNIVERSITY OF BONN   (Germany)

^f HUG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLASE; CASPASE 3; CERULETIDE; GAP JUNCTION PROTEIN; MYELOPEROXIDASE; PROTEIN BAX; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA;

ACINAR CELL; ACUTE PANCREATITIS; AMYLASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVITY; CELL DEATH; CONTROLLED STUDY; CX32 GENE; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; GAP JUNCTION; GENE; HOMEOSTASIS; IMMUNOFLUORESCENCE TEST; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0037309879     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/gast.2003.50052     Document Type: Article

References (58)

1. Whitcomb D, Gorry M, Preston R, Furey W, Sossenheimer M, Ulrich C, Martin S, Gates L, Amman J, Toskes P, Riddle L, McGrath K, Uono G, Post J, Ehrlich G. Hereditary pancreatitis is caused by mutation in the cationic trypsinogen gene. Nat Genet 1996;14:141-145.
2. Norman J. New approaches to acute pancreatitis: role of inflammatory mediators. Digestion 1999;60:57-60.
3. Saluja AK, Steer M. Pathophysiology of pancreatitis. Role of cytokines and other mediators of inflammation. Digestion 1999;60:27-33.
4. Frossard JL, Hadengue A. Emerging concept in acute pancreatitis. Gastroenterol Clin Biol 2001;25:164-176.
5. Gukovskaya AS, Perkins P, Zaninovic V, Sandoval D, Rutherford R, Fitzsimmons T, Pandol SJ, Poucell-Hatton S. Mechanisms of cell death after pancreatic duct obstruction in the opossum and the rat. Gastroenterology 1996;110:875-884.
6. Kaiser AM, Saluja AK, Sengupta A, Saluja M, Steer ML. Relationship between severity, necrosis, and apoptosis in five models of experimental acute pancreatitis. Am J Physiol 1995;269:C1295-C1304.
7. Thatte U, Dahanukar S. Apoptosis: clinical relevance and pharmacological manipulation. Drugs 1997;54:511-532.
8. Saluja AK, Bhagat L, Lee HS, Bhatia M, Frossard JL, Steer ML. Secretagogue-induced digestive enzyme activation and cell injury in rat pancreatic acini. Am J Physiol 1999;276:G835-G842.
9. Raraty M, Ward J, Vaillant C, Neoptolemos J, Sutton R, Petersen O. Calcium-dependent enzyme activation and vacuole formation in the apical granular region of pancreatic acinar cells. Proc Natl Acad Sci U S A 2000;97:13126-13131.
10. Goodenough D, Goliger J, Paul D. Connexins, connexons and intercellular communication. Annu Rev Biochem 1996;65:475-502.
11. Kumar N, Gilula N. The gap junction communication channel. Cell 1996;84:381-388.
12. Spray D. Molecular physiology of gap junction channels. Clin Exp Pharmacol Physiol 1996;23:1038-1040.
13. Simon A, Goodenough D. Diverse functions of verebrate gap junctions. Trends Cell Biol 1998;8:477-483.
14. White TW, Paul DL. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu Rev Physiol 1999;61:283-310.
15. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem 2002;383:725-737.
16. Plum A, Hallas G, Magin T, Dombrowski F, Hagendorff A, Schumacher B, Wolpert C, Kim J, Lamers WH, Evert M, Meda P, Traub O, Willecke K. Unique and shared functions of different connexins in mice. Curr Biol 2000;10:1083-1091.
17. White TW. Unique and redundant connexin contributions to lens development. Science 2002;295:319-320.
18. Chanson M, Fanjul M, Bosco D, Nelles E, Suter S, Willecke K, Meda P. Enhanced secretion of amylase from exocrine pancreas of Connexin32-deficient mice. J Cell Biol 1998;141:1267-1275.
19. Nelles E, Bützler D, Jung D, Temme A, Gabriel H, Dahl U, Traub O, Stümpel F, Jungermann K, Zielasek J, Toyka K, Dermietzel R, Willecke K. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc Natl Acad Sci U S A 1996;93:9565-9570.
20. Anzini P, Neuberg DH, Schachner M, Nelles E, Willecke K, Zielasek J, Toyka KV, Suter U, Martini R. Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin 32. J Neurosci 1997;17:4545-4551.
21. Sherer SS, Xu YT, Nelles E, Fischbeck K, Willecke K, Bone LJ. Connexin32-null mice develop demyelinating peripheral neuropathy. Glia 1998;24:8-20.
22. Bhatia M, Wallig MA, Hofbauer B, Lee HS, Frossard JL, Steer ML, Saluja AK. Induction of apoptosis in pancreatic acinar cells reduces the severity of acute pancreatitis. Biochem Biophys Res Commun 1998;246:476-483.
23. Frossard JL, Kwak BR, Chanson M, Morel P, Hadengue A, Mach F. CD40L deficient mice are protected against cerulein-induced acute pancreatitis and pancreatitis-associated lung injury. Gastroenterology 2001;121:184-194.
24. Frossard JL, Saluja A, Bhagat L, Lee H, Bhatia M, Hofbauer B, Steer M. The role of intercellular adhesion molecule 1 and neutrophils in acute pancreatitis and pancreatitis-associated lung injury. Gastroenterology 1999;116:694-701.
25. Kawabata S, Miura T, Morita T, Kato H, Fujikawa K, Takada K, Sakakibara S. Highly sensitive peptide-4-methylcoumaryl-7-amide substrates for blood-clotting proteases and trypsin. Eur J Biochem 1988;172:17-25.
26. Hofbauer B, Saluja A, Lerch M, Bhagat L, Bhatia M, Lee H, Frossard JL, Adler G, Steer M. Intra-acinar cell activation of trypsinogen during caerulein-induced pancreatitis in rats. Am J Physiol 1998;275:G352-G362.
27. Stein AF, Dills RL, Klaassen CD. High-performance liquid chromatographic analysis of glutathione and its thiol and disulfide degradation products. J Chromatogr 1986;381:259-270.
28. Wallig M, Kore A, Crawshow J, Jeffery E. Separation of the toxic and glutathione-enhancing effects of the naturally occurring nitrile, cyanohydroxybutene. Fundam Appl Toxicol 1992;19:598- 606.
29. Ito T, Ogoshi K, Nakano I, Ueda F, Sakai H, Kinjo M, Nawata H. Effect of irsogladine on gap junctions in cerulein-induced acute pancreatitis in rats. Pancreas 1997;15:297-303.
30. Saez J, Araya R, Branes M, Concha M, Contreras J, Eugenin E, Martinez A, Palisson F, Sepulveda M. Gap junctions in inflammatory responses: connexins, regulation and possible functional roles. Current Top Membr 2000;49:555-579.
31. Mensink A, de Haan L, Lakemond C, Koeman J. Inhibition of gap junctional intercellular communication between primary human smooth muscle cells by tumor necrosis factor alpha. Carcinogenesis 1995;16:2063-2067.
32. Hu J, Cotgreave I. Differential regulation of gap junctions by proinflammatory mediators in vitro. J Clin Invest 1997;99:2312-2316.
33. Chanson M, Berclaz P, Scerri I, Dudez T, Wernke-Dollries K, Pizurki L, Pavirani A, Fiedler M, Suter S. Regulation of gap junctional communication by a pro-inflammatory cytokine in cystic fibrosis transmembrane conductance regulator-expressing but not cystic fibrosis airway cells. Am J Pathol 2001;158:1775-1784.
34. Gukovskaya AS, Gukovsky I, Zaninovic V, Song M, Sandoval D, Gukovsky S, Pandol SJ. Pancreatic acinar cells produce, release, and respond to tumor necrosis factor-alpha. Role in regulating cell death and pancreatitis. J Clin Invest 1997;100:1853-1862.
35. Zaninovic V, Gukovskaya A, Gukovsky I, Mouria M, Pandol S. Cerulein upregulates ICAM-1 in pancreatic acinar cells which mediates neutrophil adhesion to these cells. Am J Physiol 2000;279:666-676.
36. Iovanna JL. Redifferentiation and apoptosis of pancreatic cells during acute pancreatitis. Int J Pancreatol 1996;20:77-84.
37. Hahm K, Kim J, You B, Kim Y, Yim H, Ahn B, Kim W. Induction of apoptosis with an extract of Artemisia asiatica attenuates the severity of cerulein-induced pancreatitis in rats. Pancreas 1998;17:153-157.
38. Kimura K, Shimosegawa T, Abe R, Masamune A, Satoh A, Takasu A, Koizumi M, Toyota T. Low doses of lipopolysaccharide upregulate acinar cell apoptosis in cerulein-induced pancreatitis. Pancreas 1998;17:120-126.
39. Trosko J, Goodman J. Intercellular communication may facilitate apoptosis: implications for tumor promotion. Mol Carcinog 1994;11:8-12.
40. Yamasaki H, Nauss C. Role of connexin genes in growth control. Carcinogenesis 1996;17:1199-1213.
41. Lin J, Weigel H, Cotrina M, Liu S, Bueno E, Hansen A, Hansen T, Goldman S, Nedergraad M. Gap junction-mediated propagation and amplification of cell injury. Nat Neurosci 1998;1:494-500.
42. Andrade-Rosenthal A, Rozental R, Hopperstad M, Wu J, Vironis F, Spray D. Gap junctions: the "kiss of death" and the "kiss of life." Brain Res Rev. 2000;32:308-315.
43. Wilson M, Close T, Trosko J. Cell population, dynamic (apoptosis, mitosis and cell-cell communication) during disruption of homeostasis. Exp Cell Res 2000;254:257-268.
44. Temme A, Buchamann A, Gabriel H, Nelles E, Schwarz M, Willecke K. High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32. Curr Biol 1997;7:713-716.
45. Goldberg GS, Lampe PD, Nicholson BJ. Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat Cell Biol 1999;1:457-459.
46. Kavanagh TJ, Raghu G, White CC, Martin GM, Rabinovitch PS, Eaton DL. Enhancement of glutathione content in glutathione synthetase-deficient fibroblasts from a patient with 5-oxoprolinuria via metabolic cooperation with normal fibroblasts. Exp Cell Res 1994;212:69-76.
47. Nakamura TY, Yamamoto I, Kanno Y, Shiba Y, Goshima K. Metabolic coupling of glutathione between mouse and quail cardiac myocytes and its protective role against oxidative stress. Circ Res 1994;74:806-816.
48. Meister A. Glutathione, ascorbate, and cellular protection. Cancer Res 1994;54:1969s-1975s.
49. Luthen RC, Niederau C, Grendell JH. Intrapancreatic zymogen activation and levels of ATP and glutathione during caerulein pancreatitis in rats. Am J Physiol 1995;268:G592-G603.
50. Grady T, Saluja A, Kaiser A, Steer M. Edema and intrapancreatic trypsinogen activation precede glutathione depletion during caerulein pancreatitis. Am J Physiol 1996;271:G20-G26.
51. Neuschwander-Tetri BA, Ferrel LD, Sukhabotte RJ, Grendell JH. Glutathione monoethyl ester ameliorates caerulein-induced pancreatitis in the mouse. J Clin Invest 1992;89:109-116.
52. Demols A, Van Laethem JL, Quertinmont E, Legros F, Louis H, Le Moine O, Deviere J. N-acetylcysteine decreases severity of acute pancreatitis in mice. Pancreas 2000;20:161-169.
53. Slater AFG, Nobel CSI, Orrenius S. The role of intracellular antioxidants in apoptosis. Biochim Biophys Acta 1995;1271:59-62.
54. Petersen OH, Iwatsuki N. Hormonal control of cell to cell coupling in the exocrine pancreas. In: Rosselin G, Fromageot P, Bonfils S, eds. Hormone receptors in digestion and nutrition. 1979, Amsterdam: Elsevier/North Holland Biomedical, 1979:191-202.
55. Meda P, Bruzzone R, Knodel S, Orci L. Blockage of cell-to-cell communication within pancreatic acini is associated with increased basal release of amylase. J Cell Biol 1986;103:475-483.
56. Meda P, Bruzzone R, Chanson M, Bosco D, Orci L. Junctional coupling modulates secretion of exocrine pancreas. Proc Natl Acad Sci U S A 1987;84:4901-4904.
57. Chanson M, Orci L, Meda P. Extent and modulation of junctional communication between pancreatic acinar cells in vivo. Am J Physiol 1991;261:28-36.
58. 2+. J Biol Chem 1999;274:282-287.