209
Views
9
CrossRef citations to date
0
Altmetric
Research Article

Calpain mediates caspase-dependent apoptosis initiated by hydrogen peroxide in pancreatic acinar AR42J cells

, , , , &
Pages 432-446 | Received 31 Jul 2012, Accepted 11 Mar 2013, Published online: 08 Apr 2013

References

  • Fulda S, Gorman AM, Hori O, Samali A. Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010;2010:214074.
  • Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 2002;192:1–15.
  • Halliwell B, Gutteridge JM (eds.). Free Radicals in Biology and Medicine. 3rd ed. Oxford: University Press; 1999.
  • Baumgartner HK, Gerasimenko JV, Thorne C, Ferdek P, Pozzan T, Tepikin AV, et al. Calcium elevation in mitochondria is the main Ca2 + requirement for mitochondrial permeability transition pore (mPTP) opening. J Biol Chem 2009;284:20796–20803.
  • Criddle DN, Gerasimenko JV, Baumgartner HK, Jaffar M, Voronina S, Sutton R, et al. Calcium signalling and pancreatic cell death: apoptosis or necrosis? Cell Death Differ 2007;14:1285–1294.
  • Gerasimenko JV, Gerasimenko OV, Palejwala A, Tepikin AV, Petersen OH, Watson AJ. Menadione-induced apoptosis: roles of cytosolic Ca (2+) elevations and the mitochondrial permeability transition pore. J Cell Sci 2002;115:485–497.
  • Sata N, Klonowski-Stumpe H, Han B, Häussinger D, Niederau C. Cytotoxicity of peroxynitrite in rat pancreatic acinar AR4-2J cells. Pancreas 1997;15:278–284.
  • Song JY, Lim JW, Kim H, Morio T, Kim KH. Oxidative stress induces nuclear loss of DNA repair proteins Ku70 and Ku80 and apoptosis in pancreatic acinar AR42J cells. J Biol Chem 2003;278:36676–36687.
  • Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003;4:552–565.
  • Haidara K, Marion M, Gascon-Barré M, Denizeau F, Averill-Bates DA. Implication of caspases and subcellular compartments in tert-butylhydroperoxide induced apoptosis. Toxicol Appl Pharmacol 2008;229:65–76.
  • Johnson DE. Noncaspase proteases in apoptosis. Leukemia 2000;14:1695–1703.
  • Li Y, Li Y, Feng Q, Arnold M, Peng T. Calpain activation contributes to hyperglycaemia-induced apoptosis in cardiomyocytes. Cardiovasc Res 2009;84:100–110.
  • Martinez JA, Zhang Z, Svetlov SI, Hayes RL, Wang KK, Larner SF. Calpain and caspase processing of caspase-12 contribute to the ER stress-induced cell death pathway in differentiated PC12 cells. Apoptosis 2010;15:1480–1493.
  • Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000;150:887–894.
  • Norberg E, Gogvadze V, Vakifahmetoglu H, Orrenius S, Zhivotovsky B. Oxidative modification sensitizes mitochondrial apoptosis-inducing factor to calpain-mediated processing. Free Radic Biol Med 2010;15:791–797.
  • Waterhouse NJ, Finucane DM, Green DR, Elce JS, Kumar S, Alnemri ES, et al. Calpain activation is upstream of caspases in radiation-induced apoptosis. Cell Death Differ 1998;5: 1051–1061.
  • Pallepati P, Averill-Bates DA. Mild thermotolerance induced at 40°C protects HeLa cells against activation of death receptor-mediated apoptosis by hydrogen peroxide. Free Radic Biol Med 2011;50:667–679.
  • Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 2003;83:31–801.
  • Wang KKW. Calpain and caspase: can you tell the difference? Trends Neurosci 2000;23:20–26.
  • Weber H, Hopp HH, Wagner AC, Noack T, Jonas L, Lüthen F, Schuff-Werner P. Expression and regulation of calpain in rat pancreatic acinar cells. Pancreas 2002;24: 63–74.
  • Weber H, Jonas L, Hühns S, Schuff-Werner P. Dysregulation of the calpain-calpastatin system plays a role in the development of cerulein-induced acute pancreatitis in the rat. Am J Physiol Gastrointest Liver Physiol 2004;286:G932–G941.
  • Weber H, Hühns S, Lüthen F, Jonas L, Schuff-Werner P. Calpain activation contributes to oxidative stress-induced pancreatic acinar cell injury. Biochem Pharmacol 2005;70: 1241–1252.
  • Weber H, Hühns S, Lüthen F, Jonas L. Calpain-mediated breakdown of cytoskeletal proteins contributes to cholecystokinin-induced damage of rat pancreatic acini. Int J Exp Pathol 2009;90:387–399.
  • Choi WS, Lee EH, Chung CW, Jung YK, Jin BK, Kim SU, et al. Cleavage of Bax is mediated by caspase-dependent or - independent calpain activation in dopaminergic neuronal cells: protective role of Bcl-2. J Neurochem 2001;77:1531–1541.
  • Mandic A, Viktorsson K, Strandberg L, Heiden T, Hansson J, Linder S. Calpain-mediated Bid cleavage and calpain- independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Mol Cell Biol 2002;22: 3003–3013.
  • Eum WS, Li MZ, Sin GS, Choi SY, Park JB, Lee JY, et al. Dexamethasone-induced differentiation of pancreatic AR42J cell involves p21 (waf1/cip1) and MAP kinase pathway. Exp Mol Med 2003;35:379–384.
  • Yu JH, Lim JW, Kim KH, Morio T, Kim H. NADPH oxidase and apoptosis in cerulein-stimulated pancreatic acinar AR42J cells. Free Radical Biol Med 2005;39:590–602.
  • Weber H, Hühns S, Jonas L, Sparmann G, Bastian M, Schuff-Werner P. Hydrogen peroxide-induced activation of defense mechanisms against oxidative stress in rat pancreatic acinar AR42J cells. Free Radical Biol Med 2007;42:830–841.
  • Vitale M, Zauli G, Falcieri E. Apoptosis vs. necrosis. In Purdue cytometry CDROM series, vol 4, 1998; http://www.cyto.purdue.edu/cdroms/cyto4/.
  • Baumgartner HK, Gerasimenko JV, Thorne C, Ashurst LH, Barrow SL, Chvanov MA, et al. Caspase-8-mediated apoptosis induced by oxidative stress is independent of the intrinsic pathway and dependent on cathepsins. Am J Physiol Gastrointest Liver Physiol 2007;293:G296–G307.
  • Das A, McDowell M, Pava MJ, Smith JA, Reiter RJ, Woodward JJ, et al. The inhibition of apoptosis by melatonin in VSC4.1 motoneurons exposed to oxidative stress, glutamate excitotoxicity, or TNF-alpha toxicity involves membrane melatonin receptors. J Pineal Res 2010;48:57–169.
  • Morgado S, Granados MP, Bejarano I, Lopez JJ, Salido GM, Gonzalez A, Pariente JA. Role of intracellular calcium on hydrogen-peroxide-induced apoptosis in rat pancreatic acinar AR42J cells. J Appl Biomed 2008;6:211–224.
  • Weber H, Roesner JP, Nebe B, Rychly J, Werner A, Schröder H, et al. Increased cytosolic Ca2 + amplifies oxygen radical-induced alterations of the ultrastructure and the energy metabolism of isolated rat pancreatic acinar cells. Digestion 1998;59:175–185.
  • Bröker LE, Kruyt FA, Giaccone G. Cell death independent of caspases: a review. Clin Cancer Res 2005;11:3155–3162.
  • Edelstein CL, Yaqoob MM, Alkhunaizi AM, Gengaro PE, Nemenoff RA, Wang KK, Schrier RW. Modulation of hypoxia-induced calpain activity in rat renal proximal tubules. Kidney Int 1996;50;1150–1157.
  • Verdaguer E, Alvira D, Jiménez A, Rimbau V, Camins A, Pallàs M. Inhibition of the cdk5/MEF2 pathway is involved in the antiapoptotic properties of calpain inhibitors in cerebellar neurons. Br J Pharmacol 2005;145:1103–1111.
  • Edelstein CL, Wieder ED, Yaqoob MM, Gengaro PE, Burke TJ, Nemenoff RA, Schrier RW. The role of cysteine proteases in hypoxia-induced rat renal proximal tubular injury. Proc Natl Acad Sci U S A 1995;92:7662–7666.
  • Kohli V, Madden JF, Bentley RC, Clavien PA. Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis. Gastroenterology 1999;116:168–178.
  • Mehdi S. Cell-penetrating inhibitors of calpain. Trends Biochem Sci 1991;16:150–153.
  • Tsubuki S, Saito Y, Tomioka M, Ito H, Kawashima S. Differential inhibition of calpain and proteasome activities by peptidyl aldehydes of di-leucine and tri-leucine. J Biochem 1996;119:572–576.
  • Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006;7:880–885.
  • Lu TH, Su CC, Chen YW, Yang CY, Wu CC, Hung DZ, et al. Arsenic induces pancreatic β-cell apoptosis via the oxidative stress-regulated mitochondria-dependent endoplasmic reticulum stress-triggered signaling pathways. Toxicol Lett 2011;201: 15–26.
  • Tan Y, Dourdin N, Wu C, De Veyra T, Elce JS, Greer PA. Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J Biol Chem 2006;281:16016–16024.
  • Kerbiriou M, Teng L, Benz N, Trouvé P, Férec C. The calpain, caspase 12, caspase 3 cascade leading to apoptosis is altered in F508del-CFTR expressing cells. PLoS One 2009;4:e8436.
  • Hossain MM, Richardson JR. Mechanism of pyrethroid pesticide-induced apoptosis: role of calpain and the ER stress pathway. Toxicol Sci 2011;122:512–525.
  • Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002;277:34287–34294.
  • Cao Y, Adhikari S, Ang AD, Moore PK, Bhatia M. Mechanism of induction of pancreatic acinar cell apoptosis by hydrogen sulfide. Am J Physiol Cell Physiol 2006;291: C503–C510.
  • Beil M, Leser J, Lutz MP, Gukovskaya A, Seufferlein T, Lynch G, et al. Caspase 8-mediated cleavage of plectin precedes F-actin breakdown in acinar cells during pancreatitis. Am J Physiol Gastrointest Liver Physiol 2002;282: G450–G460.
  • Ullman E, Pan JA, Zong WX. Squamous cell carcinoma antigen 1 promotes caspase-8-mediated apoptosis in response to endoplasmic reticulum stress while inhibiting necrosis induced by lysosomal injury. Mol Cell Biol 2011;31: 2902–29019.
  • Scaffidi C, Medema JP, Krammer PH, Peter ME. FLICE is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J Biol Chem 1997;272: 26953–26958.
  • Chae SU, Ha KC, Piao CS, Chae SW, Chae HJ. Estrogen attenuates cardiac ischemia-reperfusion injury via inhibition of calpain-mediated bid cleavage. Arch Pharm Res 2007;30:1225–1235.
  • Das A, Belagodu A, Reiter RJ, Ray SK, Banik NL. Cytoprotective effects of melatonin on C6 astroglial cells exposed to glutamate excitotoxicity and oxidative stress. J Pineal Res 2008;45:117–124.
  • Selimovic D, Ahmad M, El-Khattouti A, Hannig M, Haïkel Y, Hassan M. Apoptosis-related protein-2 triggers melanoma cell death by a mechanism including both endoplasmic reticulum stress and mitochondrial dysregulation. Carcinogenesis 2011;32:1268–1278.
  • Zhang Z, Larner SF, Liu MC, Zheng W, Hayes RL, Wang KK. Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways. Apoptosis 2009;14:1289–1298.
  • Hwang SM, Li J, Koo NY, Choi SY, Lee SJ, Oh SB, et al. Role of purinergic receptor in alpha fodrin degradation in Par C5 cells. J Dent Res 2009;88:927–932.
  • Takeyama N, Miki S, Hirakawa A, Tanaka T. Role of the mitochondrial permeability transition and cytochrome C release in hydrogen peroxide-induced apoptosis. Exp Cell Res 2002;274:16–24.
  • Fu Y, Tang M, Fan Y, Zou H, Sun X, Xu X. Anti-apoptotic effects of melatonin in retinal pigment epithelial cells. Front Biosci 2012;17:1461–1468.
  • Zhang S, Ye J, Dong G. Neuroprotective effect of baicalein on hydrogen peroxide-mediated oxidative stress and mitochondrial dysfunction in PC12 cells. J Mol Neurosci 2010;40: 311–320.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.