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Original Research

Thapsigargin induces apoptosis in adrenocortical carcinoma by activating endoplasmic reticulum stress and the JNK signaling pathway: an in vitro and in vivo study

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Pages 2787-2798 | Published online: 12 Aug 2019

References

  • Else T, Kim AC, Sabolch A, et al. Adrenocortical carcinoma. Endocr Rev. 2014;35(2):282–326. doi:10.1210/er.2013-102924423978
  • Bilimoria KY, Shen WT, Elaraj D, et al. Adrenocortical carcinoma in the United States: treatment utilization and prognostic factors. Cancer. 2008;113(11):3130–3136. doi:10.1002/cncr.2388618973179
  • Terzolo M, Baudin AE, Ardito A, et al. Mitotane levels predict the outcome of patients with adrenocortical carcinoma treated adjuvantly following radical resection. Eur J Endocrinol. 2013;169(3):263–270. doi:10.1530/EJE-13-024223704714
  • Gratian L, Pura J, Dinan M, et al. Treatment patterns and outcomes for patients with adrenocortical carcinoma associated with hospital case volume in the United States. Ann Surg Oncol. 2014;21(11):3509–3514. doi:10.1245/s10434-014-3931-z25069860
  • Sidhu S, Sywak M, Robinson B, Delbridge L. Adrenocortical cancer: recent clinical and molecular advances. Curr Opin Oncol. 2004;16(1):13–18.14685087
  • Libe R, Borget I, Ronchi CL, et al. Prognostic factors in stage III-IV adrenocortical carcinomas (ACC): an European Network for the Study of Adrenal Tumor (ENSAT) study. Ann Oncol. 2015;26(10):2119–2125. doi:10.1093/annonc/mdv32926392430
  • Berruti A, Baudin E, Gelderblom H, et al. Adrenal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2012;23(Suppl 7):vii131–vii138. doi:10.1093/annonc/mds23122997446
  • Puglisi S, Perotti P, Cosentini D, et al. Decision-making for adrenocortical carcinoma: surgical, systemic, and endocrine management options. Expert Rev Anticancer Ther. 2018;18(11):1125–1133. doi:10.1080/14737140.2018.151032530117750
  • Berruti A, Fassnacht M, Haak H, et al. Prognostic role of overt hypercortisolism in completely operated patients with adrenocortical cancer. Eur Urol. 2014;65(4):832–838. doi:10.1016/j.eururo.2013.11.00624268504
  • Leibovitz A, McCombs WM 3rd, Johnston D, McCoy CE, Stinson JC. New human cancer cell culture lines. I. SW-13, small-cell carcinoma of the adrenal cortex. J Natl Cancer Inst. 1973;51(2):691–697.4765382
  • Rainey WE, Bird IM, Mason JI. The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Mol Cell Endocrinol. 1994;100(1–2):45–50.8056157
  • Andersen TB, Lopez CQ, Manczak T, Martinez K, Simonsen HT. Thapsigargin–from Thapsia L. to mipsagargin. Molecules. 2015;20(4):6113–6127.25856061
  • Xu C, Ma H, Inesi G, Al-Shawi MK, Toyoshima C. Specific structural requirements for the inhibitory effect of thapsigargin on the Ca2+ ATPase SERCA. J Biol Chem. 2004;279(17):17973–17979. doi:10.1074/jbc.M31326320014970206
  • Jakobsen CM, Denmeade SR, Isaacs JT, Gady A, Olsen CE, Christensen SB. Design, synthesis, and pharmacological evaluation of thapsigargin analogues for targeting apoptosis to prostatic cancer cells. J Med Chem. 2001;44(26):4696–4703. doi:10.1021/jm010985a11741487
  • Tao YK, Yu PL, Bai YP, Yan ST, Zhao SP, Zhang GQ. Role of PERK/eIF2alpha/CHOP endoplasmic reticulum stress pathway in oxidized low-density lipoprotein mediated induction of endothelial apoptosis. Biomed Environ Sci. 2016;29(12):868–876. doi:10.3967/bes2016.11628081747
  • Hauck AK, Bernlohr DA. Oxidative stress and lipotoxicity. J Lipid Res. 2016;57(11):1976–1986. doi:10.1194/jlr.R06659727009116
  • Wang X, Eno CO, Altman BJ, et al. ER stress modulates cellular metabolism. Biochem J. 2011;435(1):285–296. doi:10.1042/BJ2010186421241252
  • Hetz C, Martinon F, Rodriguez D, Glimcher LH. The unfolded protein response: integrating stress signals through the stress sensor IRE1alpha. Physiol Rev. 2011;91(4):1219–1243. doi:10.1152/physrev.00001.201122013210
  • Werner N, Nickenig G, Laufs U. Pleiotropic effects of HMG-CoA reductase inhibitors. Basic Res Cardiol. 2002;97(2):105–116.12002257
  • Porter KE, Turner NA. Statins and myocardial remodelling: cell and molecular pathways. Expert Rev Mol Med. 2011;13:e22. doi:10.1017/S146239941100193121718586
  • Ryoo HD, Gorenc T, Steller H. Apoptotic cells can induce compensatory cell proliferation through the JNK and the wingless signaling pathways. Dev Cell. 2004;7(4):491–501. doi:10.1016/j.devcel.2004.08.01915469838
  • Bosch M, Serras F, Martin-Blanco E, Baguna J. JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev Biol. 2005;280(1):73–86. doi:10.1016/j.ydbio.2005.01.00215766749
  • McEwen DG, Peifer M. Puckered, a Drosophila MAPK phosphatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development. 2005;132(17):3935–3946. doi:10.1242/dev.0194916079158
  • Tamori Y, Bialucha CU, Tian AG, et al. Involvement of Lgl and Mahjong/VprBP in cell competition. PLoS Biol. 2010;8(7):e1000422. doi:10.1371/journal.pbio.100041820644714
  • Moreno E, Basler K. dMyc transforms cells into super-competitors. Cell. 2004;117(1):117–129. doi:10.1016/s0092-8674(04)00262-415066287
  • Kolahgar G, Suijkerbuijk SJ, Kucinski I, et al. Cell competition modifies adult stem cell and tissue population dynamics in a JAK-STAT-dependent manner. Dev Cell. 2015;34(3):297–309. doi:10.1016/j.devcel.2015.06.01026212135
  • Yuan ML, Li P, Xing ZH, et al. Inhibition of WEE1 suppresses the tumor growth in laryngeal squamous cell carcinoma. Front Pharmacol. 2018;9:1041. doi:10.3389/fphar.2018.0104130323762
  • Toyoshima C, Nomura H, Sugita Y. Crystal structures of Ca2+-ATPase in various physiological states. Ann N Y Acad Sci. 2003;986:1–8. doi:10.1111/j.1749-6632.2003.tb07131.x12763767
  • Winther AM, Liu H, Sonntag Y, et al. Critical roles of hydrophobicity and orientation of side chains for inactivation of sarcoplasmic reticulum Ca2+-ATPase with thapsigargin and thapsigargin analogs. J Biol Chem. 2010;285(37):28883–28892. doi:10.1074/jbc.M110.13624220551329
  • Rajapaksa G, Nikolos F, Bado I, Clarke R, Gustafsson JA, Thomas C. ERbeta decreases breast cancer cell survival by regulating the IRE1/XBP-1 pathway. Oncogene. 2015;34(31):4130–4141. doi:10.1038/onc.2014.34325347741
  • Senft D, Ronai ZA. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem Sci. 2015;40(3):141–148.25656104
  • Romero-Ramirez L, Cao H, Regalado MP, et al. X box-binding protein 1 regulates angiogenesis in human pancreatic adenocarcinomas. Transl Oncol. 2009;2(1):31–38. doi:10.1593/tlo.0821119252749
  • Wang F, Liu DZ, Xu H, et al. Thapsigargin induces apoptosis by impairing cytoskeleton dynamics in human lung adenocarcinoma cells. The Scientific World Journal. 2014;2014:619050.24605059
  • Omura T, Kaneko M, Okuma Y, et al. A ubiquitin ligase HRD1 promotes the degradation of Pael receptor, a substrate of Parkin. J Neurochem. 2006;99(6):1456–1469. doi:10.1111/j.1471-4159.2006.04155.x17059562
  • Gao B, Lee SM, Chen A, et al. Synoviolin promotes IRE1 ubiquitination and degradation in synovial fibroblasts from mice with collagen-induced arthritis. EMBO Rep. 2008;9(5):480–485. doi:10.1038/embor.2008.3718369366
  • Lei X, Zhang S, Barbour SE, et al. Spontaneous development of endoplasmic reticulum stress that can lead to diabetes mellitus is associated with higher calcium-independent phospholipase A2 expression: a role for regulation by SREBP-1. J Biol Chem. 2010;285(9):6693–6705. doi:10.1074/jbc.M109.08429320032468
  • Wang XZ, Lawson B, Brewer JW, et al. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol. 1996;16(8):4273–4280. doi:10.1128/mcb.16.8.42738754828
  • Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287(5453):664–666. doi:10.1126/science.287.5453.66410650002
  • Nakagawa T, Zhu H, Morishima N, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000;403(6765):98–103. doi:10.1038/4751310638761
  • Araki E, Oyadomari S, Mori M. Endoplasmic reticulum stress and diabetes mellitus. Internal Med. 2003;42(1):7–14. doi:10.2169/internalmedicine.42.712583611
  • Nik-Zainal S, Davies H, Staaf J, et al. Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature. 2016;534(7605):47–54. doi:10.1038/nature1767627135926
  • Konishi H, Fujiya M, Tanaka H, et al. Probiotic-derived ferrichrome inhibits colon cancer progression via JNK-mediated apoptosis. Nat Commun. 2016;7:12365. doi:10.1038/ncomms1236527507542
  • Zikaki K, Aggeli IK, Gaitanaki C, Beis I. Curcumin induces the apoptotic intrinsic pathway via upregulation of reactive oxygen species and JNKs in H9c2 cardiac myoblasts. Apoptosis. 2014;19(6):958–974. doi:10.1007/s10495-014-0979-y24668280