Mice lacking the transcription factor Mist1 exhibit an altered stress response and increased sensitivity to caerulein-induced pancreatitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 4, 2007, Pages

  Kowalik, Agnes S ^a   Johnson, Charis L ^a,b   Chadi, Sami A ^a,b   Weston, Jacqueline Y ^a,b   Fazio, Elena N ^a,b   Pin, Christopher L ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Activating transcription factor 3; Apoptosis; Endoplasmic reticulum stress response; Growth arrest and DNA damage inducible 34

Indexed keywords

AMYLASE; CERULETIDE; PROTEIN MIST 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR IIIA; UNCLASSIFIED DRUG;

ACINAR CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; FUNCTIONAL ASSESSMENT; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GROWTH DISORDER; MALE; MOUSE; NONHUMAN; PANCREATITIS; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; TISSUE INJURY; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 3; ACUTE DISEASE; AMYLASES; ANIMALS; ANTIGENS, DIFFERENTIATION; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAERULEIN; CELL CYCLE PROTEINS; CELLS, CULTURED; CHOLECYSTOKININ; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM; EUKARYOTIC INITIATION FACTOR-2; GENE EXPRESSION; IMMEDIATE-EARLY PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PANCREAS, EXOCRINE; PANCREATITIS; REGENERATION; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; STRESS; TIME FACTORS;

EID: 34147119001     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00512.2006     Document Type: Article

References (56)

1. Bateman AC, Turner SM, Thomas KS, McCrudden PR, Fine DR, Johnson PA, Johnson CD, Iredale JP. Apoptosis and proliferation of acinar and islet cells in chronic pancreatitis: evidence for differential cell loss mediating preservation of islet function. Gut 50: 542-548, 2002.
2. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326-332, 2000.
3. Bhagat L, Singh VP, Song AM, Van Acker GJ, Agrawal S, Steer ML, Saluja AK. Thermal stress-induced HSP70 mediates protection against intrapancreatic trypsinogen activation and acute pancreatitis in rats. Gastroenterology 122: 156-165, 2002.
4. Bhatia M. Apoptosis versus necrosis in acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 286: G189-G196, 2004.
5. 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 246: 476-483, 1998.
6. Blais JD, Filipenko V, Bi M, Harding HP, Ron D, Koumenis C, Wouters BG, Bell JC. Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol Cell Biol 24: 7469-7482, 2004.
7. Cuadrado A, Gonzalez L, Suarez Y, Martinez T, Munoz A. JNK activation is critical for Aplidin-induced apoptosis. Oncogene 23: 4673-4680, 2004.
8. Dabrowski A, Grady T, Logsdon CD, Williams JA. Jun kinases are rapidly activated by cholecystokinin in rat pancreas both in vitro and in vivo. J Biol Chem 271: 5686-5690, 1996.
9. Dassopoulos T, Ehrenpreis ED. Acute pancreatitis in human immunodeficiency virus-infected patients: a review. Am J Med 107: 78-84, 1999.
10. Fazio EN, Everest M, Colman R, Wang R, Pin CL. Altered Glut-2 accumulation and beta-cell function in mice lacking the exocrine-specific transcription factor, Mist1. J Endocrinol 187: 407-418, 2005.
11. Frossard JL, Rubbia-Brandt L, Wallig MA, Benathan M, Ott T, Morel P, Hadengue A, Suter S, Willecke K, Chanson M. Severe acute pancreatitis and reduced acinar cell apoptosis in the exocrine pancreas of mice deficient for the Cx32 gene. Gastroenterology 124: 481-493, 2003.
12. Gomez G, Lee HM, He Q, Englander EW, Uchida T, Greeley GH Jr. Acute pancreatitis signals activation of apoptosis-associated and survival genes in mice. Exp Biol Med (Maywood) 226: 692-700, 2001.
13. Grady T, Mah'Moud M, Otani T, Rhee S, Lerch MM, Gorelick FS. Zymogen proteolysis within the pancreatic acinar cell is associated with cellular injury. Am J Physiol Gastrointest Liver Physiol 275: G1010-G1017, 1998.
14. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5: 897-904, 2000.
15. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274, 1999.
16. Hegyi P, Rakonczay Z Jr, Sari R, Gog C, Lonovics J, Takacs T, Czako L. L-Arginine-induced experimental pancreatitis. World J Gastroenterol 10: 2003-2009, 2004.
17. Hofbauer B, Saluja AK, Lerch MM, Bhagat L, Bhatia M, Lee HS, Frossard JL, Adler G, Steer ML. Intra-acinar cell activation of trypsinogen during caerulein-induced pancreatitis in rats. Am J Physiol Gastrointest Liver Physiol 275: G352-G362, 1998.
18. Holtz WA, O'Malley KL. Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J Biol Chem 278: 19367-19377, 2003.
19. Jensen JN, Cameron E, Garay MV, Starkey TW, Gianani R, Jensen J. Recapitulation of elements of embryonic development in adult mouse pancreatic regeneration. Gastroenterology 128: 728-741, 2005.
20. Ji B, Chen XQ, Misek DE, Kuick R, Hanash S, Ernst S, Najarian R, Logsdon CD. Pancreatic gene expression during the initiation of acute pancreatitis: identification of EGR-1 as a key regulator. Physiol Genomics 14: 59-72, 2003.
21. Jiang HY, Wek RC. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 280: 14189-14202, 2005.
22. Jiang HY, Wek SA, McGrath BC, Lu D, Hai T, Harding HP, Wang X, Ron D, Cavener DR, Wek RC. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol 24: 1365-1377, 2004.
23. Johnson CL, Kowalik AS, Rajakumar N, Pin CL. Mist1 is necessary for the establishment of granule organization in serous exocrine cells of the gastrointestinal tract. Mech Dev 121: 261-272, 2004.
24. 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 Cell Physiol 269: C1295-C1304, 1995.
25. Katayama T, Imaizumi K, Manabe T, Hitomi J, Kudo T, Tohyama M. Induction of neuronal death by ER stress in Alzheimer's disease. J Chem Neuroanat 28: 67-78, 2004.
26. Kruger B, Albrecht E, Lerch MM. The role of intracellular calcium signaling in premature protease activation and the onset of pancreatitis. Am J Pathol 157: 43-50, 2000.
27. Kuang E, Wan Q, Li X, Xu H, Liu Q, Qi Y. ER Ca2+ depletion triggers apoptotic signals for endoplasmic reticulum (ER) overload response induced by overexpressed reticulon 3 (RTN3/HAP). J Cell Physiol 204: 549-559, 2005.
28. Kubisch CH, Sans MD, Arumugam T, Ernst SA, Williams JA, Logsdon CD. Early activation of endoplasmic reticulum stress is associated with arginine-induced acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 291: G238-G245, 2006.
29. Leppa S, Bohmann D. Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene 18: 6158-6162, 1999.
30. Lerch MM, Saluja AK, Runzi M, Dawra R, Saluja M, Steer ML. Pancreatic duct obstruction triggers acute necrotizing pancreatitis in the opossum. Gastroenterology 104: 853-861, 1993.
31. Li J, Holbrook NJ. Elevated gadd153/chop expression and enhanced c-Jun N-terminal protein kinase activation sensitizes aged cells to ER stress. Exp Gerontol 39: 735-744, 2004.
32. Li M, Baumeister P, Roy B, Phan T, Foti D, Luo S, Lee AS. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol Cell Biol 20: 5096-5106, 2000.
33. Liang SH, Zhang W, McGrath BC, Zhang P, Cavener DR. PERK (eIF2alpha kinase) is required to activate the stress-activated MAPKs and induce the expression of immediate-early genes upon disruption of ER calcium homoeostasis. Biochem J 393: 201-209, 2006.
34. 2+ signaling and exocytosis in Mist1 null mice. J Biol Chem 280: 12668-12675, 2005.
35. Matsukawa J, Matsuzawa A, Takeda K, Ichijo H. The ASK1-MAP kinase cascades in mammalian stress response. J Biochem (Tokyo) 136: 261-265, 2004.
36. Nakatani Y, Kaneto H, Kawamori D, Yoshiuchi K, Hatazaki M, Matsuoka TA, Ozawa K, Ogawa S, Hori M, Yamasaki Y, Matsuhisa M. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem 280: 847-851, 2005.
37. Niederau C, Luthen R, Klonowski-Stumpe H, Schreiber R, Soika I, Sata N, Bing H, Haussinger D. The role of calcium in pancreatitis. Hepatogastroenterology 46: 2723-2730, 1999.
38. Niederau C, Niederau M, Luthen R, Strohmeyer G, Ferrell LD, Grendell JH. Pancreatic exocrine secretion in acute experimental pancreatitis. Gastroenterology 99: 1120-1127, 1990.
39. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16: 1345-1355, 2002.
40. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153: 1011-1022, 2001.
41. O'Reilly DA, Yang BM, Creighton JE, Demaine AG, Kingsnorth AN. Mutations of the cationic trypsinogen gene in hereditary and non-hereditary pancreatitis. Digestion 64: 54-60, 2001.
42. Pin CL, Bonvissuto AC, Konieczny SF. Mist1 expression is a common link among serous exocrine cells exhibiting regulated exocytosis. Anat Rec 259: 157-167, 2000.
43. Pin CL, Rukstalis JM, Johnson C, Konieczny SF. The bHLH transcription factor Mist1 is required to maintain exocrine pancreas cell organization and acinar cell identity. J Cell Biol 155: 519-530, 2001.
44. Rukstalis JM, Kowalik A, Zhu L, Lidington D, Pin CL, Konieczny SF. Exocrine specific expression of connexin32 is dependent on the basic helix-loop-helix transcription factor Mist1. J Cell Sci 116: 3315-3325, 2003.
45. 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 Gastrointest Liver Physiol 276: G835-G842, 1999.
46. Saluja AK, Donovan EA, Yamanaka K, Yamaguchi Y, Hofbauer B, Steer ML. Cerulein-induced in vitro activation of trypsinogen in rat pancreatic acini is mediated by cathepsin B. Gastroenterology 113: 304-310, 1997.
47. Saluja AK, Saluja M, Printz H, Zavertnik A, Sengupta A, Steer ML. Experimental pancreatitis is mediated by low-affinity cholecystokinin receptors that inhibit digestive enzyme secretion. Proc Natl Acad Sci USA 86: 8968-8971, 1989.
48. Sans MD, DiMagno MJ, D'Alecy LG, Williams JA. Caerulein-induced acute pancreatitis inhibits protein synthesis through effects on eIF2B and eIF4F. Am J Physiol Gastrointest Liver Physiol 285: G517-G528, 2003.
49. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2: 222-228, 2001.
50. 2-Macroglobulin-murinoglobulin-1- deficient mice. A mouse model for acute pancreatitis. Am J Pathol 155: 983-993, 1999.
51. Witt H. Chronic pancreatitis and cystic fibrosis. Gut 52, Suppl 2: ii31-ii41, 2003.
52. Yan W, Frank CL, Korth MJ, Sopher BL, Novoa I, Ron D, Katze MG. Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci USA 99: 15920-15925, 2002.
53. 2+ oscillations in response to cholecystokinin and carbachol but not to JMV-180 in rat pancreatic acinar cells. J Biol Chem 267: 13830-13835, 1992.
54. Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66: S102-S109, 2006.
55. Zhu L, Tran T, Rukstalis JM, Sun P, Damsz B, Konieczny SF. Inhibition of Mist1 homodimer formation induces pancreatic acinar-toductal metaplasia. Mol Cell Biol 24: 2673-2681, 2004.
56. Zimmermann A, Gloor B, Kappeler A, Uhl W, Friess H, Buchler MW. Pancreatic stellate cells contribute to regeneration early after acute necrotising pancreatitis in humans. Gut 51: 574-578, 2002.