Inhibition of JNK3 promotes apoptosis induced by BH3 mimetic S1 in chemoresistant human ovarian cancer cells

Anatomical Record

Volumn 298, Issue 2, 2015, Pages 386-395

  Yang, Xiaochun ^a   Xiang, Xiyan ^a   Xia, Meihui ^a   Su, Jing ^a   Wu, Yao ^a   Shen, Luyan ^a   Xu, Ye ^b   Sun, Liankun ^a  

^a JILIN UNIVERSITY   (China)

^b JILIN MEDICAL COLLEGE   (China)

Author keywords

Apoptosis; Autophagy; BH3 mimetic; Endoplasmic reticulum stress; JNK3; Oxidative stress

Indexed keywords

ENZYME INHIBITOR; GIMERACIL PLUS OTERACIL POTASSIUM PLUS TEGAFUR; MITOGEN ACTIVATED PROTEIN KINASE 12; PROTEIN P62; SR 3576; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BID PROTEIN, HUMAN; BIOMIMETIC MATERIAL; DRUG COMBINATION; MITOGEN ACTIVATED PROTEIN KINASE 10; OTERACIL; PROTEIN BCL 2; PROTEIN BID; S 1 (COMBINATION); TEGAFUR;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER RESISTANCE; CONTROLLED STUDY; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; OVARIAN CANCER CELL LINE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG COMBINATION; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; FEMALE; MOLECULAR MIMICRY; OVARIAN NEOPLASMS; PHYSIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BIOMIMETIC MATERIALS; CELL LINE, TUMOR; DRUG COMBINATIONS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 10; MOLECULAR MIMICRY; OVARIAN NEOPLASMS; OXONIC ACID; PROTO-ONCOGENE PROTEINS C-BCL-2; TEGAFUR;

EID: 84920991808     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22991     Document Type: Article

References (43)

1. Appierto V, Tiberio P, Villani MG, Cavadini E, Formelli F. 2009. PLAB induction in fenretinide-induced apoptosis of ovarian cancer cells occurs via a ROS-dependent mechanism involving ER stress and JNK activation. Carcinogenesis 30:824-831.
2. Brotin E, Meryet-Figuiere M, Simonin K, Duval RE, Villedieu M, Leroy-Dudal J, Saison-Behmoaras E, Gauduchon P, Denoyelle C, Poulain L. 2010. Bcl-XL and MCL-1 constitute pertinent targets in ovarian carcinoma and their concomitant inhibition is sufficient to induce apoptosis. Int J Cancer 126:885-895.
3. Choi JA, Lim YJ, Cho SN, Lee JH, Jeong JA, Kim EJ, Park JB, Kim SH, Park HS, Kim HJ, Song CH. 2013. Mycobacterial HBHA induces endoplasmic reticulum stress-mediated apoptosis through the generation of reactive oxygen species and cytosolic Ca(2+) in murine macrophage RAW 264.7 cells. Cell Death Dis 4:e957.
4. Cruickshanks N, Tang Y, Booth L, Hamed H, Grant S, Dent P. 2012. Lapatinib and obatoclax kill breast cancer cells through reactive oxygen species-dependent endoplasmic reticulum stress. Mol Pharmacol 82:1217-1229.
5. Cui J, Wang Q, Wang J, Lv M, Zhu N, Li Y, Feng J, Shen B, Zhang J. 2009. Basal c-Jun NH2-terminal protein kinase activity is essential for survival and proliferation of T-cell acute lymphoblastic leukemia cells. Mol Cancer Ther 8:3214-3222.
6. Dasmahapatra G, Lembersky D, Rahmani M, Kramer L, Friedberg J, Fisher RI, Dent P, Grant S. 2009. Bcl-2 antagonists interact synergistically with bortezomib in DLBCL cells in association with JNK activation and induction of ER stress. Cancer Biol Ther 8:808-819.
7. Goeroegh T, Beress L, Quabius ES, Ambrosch P, Hoffmann M. 2013. Head and neck cancer cells and xenografts are very sensitive to palytoxin: decrease of c-jun n-terminale kinase-3 expression enhances palytoxin toxicity. Mol Cancer 12.
8. Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, Derijard B, Davis RJ. 1996. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15:2760-2770.
9. Han YH, Moon WJ, You BR, Kim SZ, Kim SH, Park WH. 2009. The effect of MAPK inhibitors on arsenic trioxide-treated Calu-6 lung cells in relation to cell death, ROS and GSH levels. Anticancer Res 29:3837-3844.
10. Heasley LE, Han SY. 2006. JNK regulation of oncogenesis. Mol Cells 21:167-173.
11. Herod JJ, Eliopoulos AG, Warwick J, Niedobitek G, Young LS, Kerr DJ. 1996. The prognostic significance of Bcl-2 and p53 expression in ovarian carcinoma. Cancer Res 56:2178-2184.
12. Howard AN, Bridges KA, Meyn RE, Chandra J. 2009. ABT-737, a BH3 mimetic, induces glutathione depletion and oxidative stress. Cancer Chemother Ppharmacol 65:41-54.
13. Hui L, Zatloukal K, Scheuch H, Stepniak E, Wagner EF. 2008. Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J Clin Invest 118:3943-3953.
14. Kamenecka T, Habel J, Duckett D, Chen W, Ling YY, Frackowiak B, Jiang R, Shin Y, Song X, LoGrasso P. 2009. Structure-activity relationships and X-ray structures describing the selectivity of aminopyrazole inhibitors for c-Jun N-terminal kinase 3 (JNK3) over p38. J Biol Chem 284:12853-12861.
15. Kaminska B, Gozdz A, Zawadzka M, Ellert-Miklaszewska A, Lipko M. 2009. MAPK signal transduction underlying brain inflammation and gliosis as therapeutic target. Anat Rec 292:1902-1913.
16. Karaca B, Atmaca H, Bozkurt E, Kisim A, Uzunoglu S, Karabulut B, Sezgin C, Sanli UA, Uslu R. 2013. Combination of AT-101/cisplatin overcomes chemoresistance by inducing apoptosis and modulating epigenetics in human ovarian cancer cells. Mol Biol Rep 40:3925-3933.
17. Kato H, Nakajima S, Saito Y, Takahashi S, Katoh R, Kitamura M. 2012. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. Cell Death Differ 19:310-320.
18. Ke H, Harris R, Coloff JL, Jin JY, Leshin B, Miliani de Marval P, Tao S, Rathmell JC, Hall RP, Zhang JY. 2010. The c-Jun NH2-terminal kinase 2 plays a dominant role in human epidermal neoplasia. Cancer Res 70:3080-3088.
19. Kim AD, Kang KA, Kim HS, Kim DH, Choi YH, Lee SJ, Kim HS, Hyun JW. 2013. A ginseng metabolite, compound K, induces autophagy and apoptosis via generation of reactive oxygen species and activation of JNK in human colon cancer cells. Cell Death Dis 4:e750.
20. Liu N, Xu Y, Sun JT, Su J, Xiang XY, Yi HW, Zhang ZC, Sun LK. 2013a. The BH3 mimetic S1 induces endoplasmic reticulum stress-associated apoptosis in cisplatin-resistant human ovarian cancer cells although it activates autophagy. Oncol Rep 30:2677-2684.
21. Liu Y, Zhang Z, Song T, Liang F, Xie M, Sheng H. 2013b. Resistance to BH3 mimetic S1 in SCLC cells that up-regulate and phosphorylate Bcl-2 through ERK1/2. Br J Pharmacol 169:1612-1623.
22. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K. 2006. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220-9231.
23. Oh SH, Lim SC. 2009. Endoplasmic reticulum stress-mediated autophagy/apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonenamide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells. J Pharmacol Exp Ther 329:112-122.
24. Raciti M, Lotti LV, Valia S, Pulcinelli FM, Di Renzo L. 2012. JNK2 is activated during ER stress and promotes cell survival. Cell Death Dis 3:e429.
25. Sanchez-Lopez E, Zimmerman T, Gomez del Pulgar T, Moyer MP, Lacal Sanjuan JC, Cebrian A. 2013. Choline kinase inhibition induces exacerbated endoplasmic reticulum stress and triggers apoptosis via CHOP in cancer cells. Cell Death Dis 4:e933.
26. Shore GC, Papa FR, Oakes SA. 2011. Signaling cell death from the endoplasmic reticulum stress response. Curr Opin Cell Biol 23:143-149.
27. Siegel R, Naishadham D, Jemal A. 2012. Cancer statistics, 2012. CA Cancer J Clin 62:10-29.
28. Song T, Chang X, Zhang Z, Liu Y, Shen X. 2012a. S1, a novel Pan-BH3 mimetic, induces apoptosis in Mcl-1-overexpressing cells through Bak. J Pharmacol Sci 119:330-340.
29. Song YJ, Zong ZM, Liu HZ, Mukasa R, Pei DS, Mou J, Wen XR, Liu ZA, Wei XY. 2012b. Heme oxygenase-1 regulates the JNK signaling pathway through the MLK3-MKK7-JNK3 signaling module in brain ischemia injury. Brain Res 1429:1-8.
30. Sung B, Ravindran J, Prasad S, Pandey MK, Aggarwal BB. 2010. Gossypol induces death receptor-5 through activation of the ROS-ERK-CHOP pathway and sensitizes colon cancer cells to TRAIL. J Biol Chem 285:35418-35427.
31. Tang K, Lin Y, Li L-M. 2013. The role of phenethyl isothiocyanate on bladder cancer ADM resistance reversal and its molecular mechanism. Anat Rec 296:899-906.
32. Verhaegen M, Bauer JA, Martin de la Vega C, Wang G, Wolter KG, Brenner JC, Nikolovska-Coleska Z, Bengtson A, Nair R, Elder JT, Van Brocklin M, Carey TE, Bradford CR, Wang S, Soengas MS. 2006. A novel BH3 mimetic reveals a mitogen-activated protein kinase-dependent mechanism of melanoma cell death controlled by p53 and reactive oxygen species. Cancer Res 66:11348-11359.
33. Vivas-Mejia P, Benito JM, Fernandez A, Han HD, Mangala L, Rodriguez-Aguayo C, Chavez-Reyes A, Lin YG, Carey MS, Nick AM, Stone RL, Kim HS, Claret FX, Bornmann W, Hennessy BT, Sanguino A, Peng Z, Sood AK, Lopez-Berestein G. 2010. c-Jun-NH2-kinase-1 inhibition leads to antitumor activity in ovarian cancer. Clin Cancer Res 16:184-194.
34. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. 2008. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 30:678-688.
35. Wong M, Tan N, Zha J, Peale FV, Yue P, Fairbrother WJ, Belmont LD. 2012. Navitoclax (ABT-263) reduces Bcl-x(L)-mediated chemoresistance in ovarian cancer models. Mol Cancer Ther 11:1026-1035.
36. Wong YT, Ruan RS, Tay FEH. 2006. Relationship between levels of oxidative DNA damage, lipid peroxidation and mitochondrial membrane potential in young and old F344 rats. Free Radic Res 40:393-402.
37. Xu C, Bailly-Maitre B, Reed JC. 2005. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656-2664.
38. Xu Y, Yu H, Qin H, Kang J, Yu C, Zhong J, Su J, Li H, Sun L. 2012. Inhibition of autophagy enhances cisplatin cytotoxicity through endoplasmic reticulum stress in human cervical cancer cells. Cancer Lett 314:232-243.
39. Yi N, Chen SY, Ma A, Chen PS, Yao B, Liang TM, Liu C. 2012. Tunicamycin inhibits PDGF-BB-induced proliferation and migration of vascular smooth muscle cells through induction of HO-1. Anat Rec 295:1462-1472.
40. Yu C, Huang X, Xu Y, Li H, Su J, Zhong J, Kang J, Liu Y, Sun L. 2013. Lysosome dysfunction enhances oxidative stress-induced apoptosis through ubiquitinated protein accumulation in HeLa cells. Anat Rec 296:31-39.
41. Zhang Z, Song T, Zhang T, Gao J, Wu G, An L, Du G. 2011. A novel BH3 mimetic S1 potently induces Bax/Bak-dependent apoptosis by targeting both Bcl-2 and Mcl-1. Int J Cancer 128:1724-1735.
42. Zhao Z, Wang J, Tang J, Liu X, Zhong Q, Wang F, Hu W, Yuan Z, Nie C, Wei Y. 2012. JNK- and Akt-mediated Puma expression in the apoptosis of cisplatin-resistant ovarian cancer cells. Biochem J 444:291-301.
43. Zhong JT, Xu Y, Yi HW, Su J, Yu HM, Xiang XY, Li XN, Zhang ZC, Sun LK. 2012. The BH3 mimetic S1 induces autophagy through ER stress and disruption of Bcl-2/Beclin 1 interaction in human glioma U251 cells. Cancer Lett 323:180-187.