Skip to main content
Top
Published in: Journal of Ovarian Research 1/2019

Open Access 01-12-2019 | Ovarian Cancer | Review

The Jun N-terminal kinases signaling pathway plays a “seesaw” role in ovarian carcinoma: a molecular aspect

Authors: Yingyu Dou, Xiaoyan Jiang, Hui Xie, Junyu He, Songshu Xiao

Published in: Journal of Ovarian Research | Issue 1/2019

Login to get access

Abstract

Ovarian cancer is the most common gynecological malignancy that causes cancer-related deaths in women today; this being the case, developing an understanding of ovarian cancer has become one of the major driving forces behind cancer research overall. Moreover, such research over the last 20 years has shown that the Jun N-terminal kinase (JNK) signaling pathway plays an important role in regulating cell death, survival, growth and proliferation in the mitogen-activated protein kinases (MAPK) signaling pathway, an important pathway in the formation of cancer. Furthermore, the JNK signaling pathway is often regulated by an abnormal activation in human tumors and is frequently reported in the literature for its effect on the progression of ovarian cancer. Although the FDA has approved some JNK inhibitors for melanoma, the agency has not approved JNK inhibitors for ovarian cancer. However, there are some experimental data on inhibitors and activators of the JNK signaling pathway in ovarian cancer, but related clinical trials need to be further improved. Although the Jun N-terminal kinase (JNK) signaling pathway is implicated in the formation of cancer in general, research has also indicated that it has a role in suppressing cancer as well. Here, we summarize this seemingly contradictory role of the JNK signaling pathway in ovarian cancer, that ‘seesaws’ between promoting and suppressing cancer, as well as summarizing the application of several JNK pathway inhibitors in cancer in general, and ovarian cancer in particular.
Literature
2.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.PubMedCrossRef Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.PubMedCrossRef
3.
go back to reference Torre LA, Trabert B, DeSantis CE, Miller KD, Samimi G, Runowicz CD, Gaudet MM, Jemal A, Siegel RL. Ovarian cancer statistics, 2018. CA Cancer J Clin. 2018;68(4):284–96.PubMedPubMedCentralCrossRef Torre LA, Trabert B, DeSantis CE, Miller KD, Samimi G, Runowicz CD, Gaudet MM, Jemal A, Siegel RL. Ovarian cancer statistics, 2018. CA Cancer J Clin. 2018;68(4):284–96.PubMedPubMedCentralCrossRef
4.
go back to reference Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–32.PubMedCrossRef Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–32.PubMedCrossRef
6.
go back to reference Hirst J, Crow J, Godwin A. Ovarian cancer genetics: subtypes and risk factors; 2018. Hirst J, Crow J, Godwin A. Ovarian cancer genetics: subtypes and risk factors; 2018.
7.
go back to reference Oberaigner W, Minicozzi P, Bielska-Lasota M, Allemani C, de Angelis R, Mangone L, Sant M, Eurocare Working G. Survival for ovarian cancer in Europe: the across-country variation did not shrink in the past decade. Acta Oncol. 2012;51(4):441–53.PubMedCrossRef Oberaigner W, Minicozzi P, Bielska-Lasota M, Allemani C, de Angelis R, Mangone L, Sant M, Eurocare Working G. Survival for ovarian cancer in Europe: the across-country variation did not shrink in the past decade. Acta Oncol. 2012;51(4):441–53.PubMedCrossRef
8.
go back to reference Maas HA, Kruitwagen RF, Lemmens VE, Goey SH, Janssen-Heijnen ML. The influence of age and co-morbidity on treatment and prognosis of ovarian cancer: a population-based study. Gynecol Oncol. 2005;97(1):104–9.PubMedCrossRef Maas HA, Kruitwagen RF, Lemmens VE, Goey SH, Janssen-Heijnen ML. The influence of age and co-morbidity on treatment and prognosis of ovarian cancer: a population-based study. Gynecol Oncol. 2005;97(1):104–9.PubMedCrossRef
9.
go back to reference Schuurman MS, Kruitwagen R, Portielje JEA, Roes EM, Lemmens V, van der Aa MA. Treatment and outcome of elderly patients with advanced stage ovarian cancer: a nationwide analysis. Gynecol Oncol. 2018;149(2):270–4.PubMedCrossRef Schuurman MS, Kruitwagen R, Portielje JEA, Roes EM, Lemmens V, van der Aa MA. Treatment and outcome of elderly patients with advanced stage ovarian cancer: a nationwide analysis. Gynecol Oncol. 2018;149(2):270–4.PubMedCrossRef
10.
go back to reference Jorgensen TL, Teiblum S, Paludan M, Poulsen LO, Jorgensen AY, Bruun KH, Hallas J, Herrstedt J. Significance of age and comorbidity on treatment modality, treatment adherence, and prognosis in elderly ovarian cancer patients. Gynecol Oncol. 2012;127(2):367–74.PubMedCrossRef Jorgensen TL, Teiblum S, Paludan M, Poulsen LO, Jorgensen AY, Bruun KH, Hallas J, Herrstedt J. Significance of age and comorbidity on treatment modality, treatment adherence, and prognosis in elderly ovarian cancer patients. Gynecol Oncol. 2012;127(2):367–74.PubMedCrossRef
11.
go back to reference Vitale SG, Capriglione S, Zito G, Lopez S, Gulino FA, Di Guardo F, Vitagliano A, Noventa M, La Rosa VL, Sapia F, et al. Management of endometrial, ovarian and cervical cancer in the elderly: current approach to a challenging condition. Arch Gynecol Obstet. 2019;299(2):299–315.PubMedCrossRef Vitale SG, Capriglione S, Zito G, Lopez S, Gulino FA, Di Guardo F, Vitagliano A, Noventa M, La Rosa VL, Sapia F, et al. Management of endometrial, ovarian and cervical cancer in the elderly: current approach to a challenging condition. Arch Gynecol Obstet. 2019;299(2):299–315.PubMedCrossRef
12.
go back to reference Bailey MH, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl MC, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371–85 e318.PubMedPubMedCentralCrossRef Bailey MH, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl MC, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371–85 e318.PubMedPubMedCentralCrossRef
14.
go back to reference Burotto M, Chiou VL, Lee JM, Kohn EC. The MAPK pathway across different malignancies: a new perspective. Cancer. 2014;120(22):3446–56.PubMedCrossRef Burotto M, Chiou VL, Lee JM, Kohn EC. The MAPK pathway across different malignancies: a new perspective. Cancer. 2014;120(22):3446–56.PubMedCrossRef
15.
go back to reference Johnson GL, Nakamura K. The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim Biophys Acta. 2007;1773(8):1341–8.PubMedPubMedCentralCrossRef Johnson GL, Nakamura K. The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim Biophys Acta. 2007;1773(8):1341–8.PubMedPubMedCentralCrossRef
17.
go back to reference Seino M, Okada M, Shibuya K, Seino S, Suzuki S, Ohta T, Kurachi H, Kitanaka C. Requirement of JNK signaling for self-renewal and tumor-initiating capacity of ovarian cancer stem cells. Anticancer Res. 2014;34(9):4723–31.PubMed Seino M, Okada M, Shibuya K, Seino S, Suzuki S, Ohta T, Kurachi H, Kitanaka C. Requirement of JNK signaling for self-renewal and tumor-initiating capacity of ovarian cancer stem cells. Anticancer Res. 2014;34(9):4723–31.PubMed
18.
go back to reference Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science. 2002;298(5600):1911–2.PubMedCrossRef Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science. 2002;298(5600):1911–2.PubMedCrossRef
19.
20.
go back to reference Wang X, Destrument A, Tournier C. Physiological roles of MKK4 and MKK7: insights from animal models. Biochim Biophys Acta. 2007;1773(8):1349–57.PubMedCrossRef Wang X, Destrument A, Tournier C. Physiological roles of MKK4 and MKK7: insights from animal models. Biochim Biophys Acta. 2007;1773(8):1349–57.PubMedCrossRef
21.
go back to reference Hayakawa R, Hayakawa T, Takeda K, Ichijo H. Therapeutic targets in the ASK1-dependent stress signaling pathways. Proc Jpn Acad Ser B. 2012;88(8):434–53.CrossRef Hayakawa R, Hayakawa T, Takeda K, Ichijo H. Therapeutic targets in the ASK1-dependent stress signaling pathways. Proc Jpn Acad Ser B. 2012;88(8):434–53.CrossRef
22.
go back to reference Ma FY, Tesch GH, Nikolic-Paterson DJ. ASK1/p38 signaling in renal tubular epithelial cells promotes renal fibrosis in the mouse obstructed kidney. Am J Physiol Renal Physiol. 2014;307(11):F1263–73.PubMedCrossRef Ma FY, Tesch GH, Nikolic-Paterson DJ. ASK1/p38 signaling in renal tubular epithelial cells promotes renal fibrosis in the mouse obstructed kidney. Am J Physiol Renal Physiol. 2014;307(11):F1263–73.PubMedCrossRef
23.
go back to reference Maurya SK, Mishra J, Tripathi VK, Sharma R, Siddiqui MH. Cypermethrin induces astrocyte damage: role of aberrant Ca2+, ROS, JNK, P38, matrix metalloproteinase 2 and migration related reelin protein. Pestic Biochem Physiol. 2014;111:51–9.PubMedCrossRef Maurya SK, Mishra J, Tripathi VK, Sharma R, Siddiqui MH. Cypermethrin induces astrocyte damage: role of aberrant Ca2+, ROS, JNK, P38, matrix metalloproteinase 2 and migration related reelin protein. Pestic Biochem Physiol. 2014;111:51–9.PubMedCrossRef
24.
go back to reference Seki E, Brenner DA, Karin M. A liver full of JNK: signaling in regulation of cell function and disease pathogenesis, and clinical approaches. Gastroenterology. 2012;143(2):307–20.PubMedCrossRef Seki E, Brenner DA, Karin M. A liver full of JNK: signaling in regulation of cell function and disease pathogenesis, and clinical approaches. Gastroenterology. 2012;143(2):307–20.PubMedCrossRef
25.
go back to reference Corazza N, Jakob S, Schaer C, Frese S, Keogh A, Stroka D, Kassahn D, Torgler R, Mueller C, Schneider P, et al. TRAIL receptor-mediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality. J Clin Invest. 2006;116(9):2493–9.PubMedPubMedCentralCrossRef Corazza N, Jakob S, Schaer C, Frese S, Keogh A, Stroka D, Kassahn D, Torgler R, Mueller C, Schneider P, et al. TRAIL receptor-mediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality. J Clin Invest. 2006;116(9):2493–9.PubMedPubMedCentralCrossRef
26.
go back to reference Kim HS, Asmis R. Mitogen-activated protein kinase phosphatase 1 (MKP-1) in macrophage biology and cardiovascular disease. A redox-regulated master controller of monocyte function and macrophage phenotype. Free Radic Biol Med. 2017;109:75–83.PubMedPubMedCentralCrossRef Kim HS, Asmis R. Mitogen-activated protein kinase phosphatase 1 (MKP-1) in macrophage biology and cardiovascular disease. A redox-regulated master controller of monocyte function and macrophage phenotype. Free Radic Biol Med. 2017;109:75–83.PubMedPubMedCentralCrossRef
27.
go back to reference Goldman EH, Chen L, Fu H. Activation of apoptosis signal-regulating kinase 1 by reactive oxygen species through dephosphorylation at serine 967 and 14-3-3 dissociation. J Biol Chem. 2004;279(11):10442–9.PubMedCrossRef Goldman EH, Chen L, Fu H. Activation of apoptosis signal-regulating kinase 1 by reactive oxygen species through dephosphorylation at serine 967 and 14-3-3 dissociation. J Biol Chem. 2004;279(11):10442–9.PubMedCrossRef
28.
go back to reference Li L, Feng Z, Porter AG. JNK-dependent phosphorylation of c-Jun on serine 63 mediates nitric oxide-induced apoptosis of neuroblastoma cells. J Biol Chem. 2004;279(6):4058–65.PubMedCrossRef Li L, Feng Z, Porter AG. JNK-dependent phosphorylation of c-Jun on serine 63 mediates nitric oxide-induced apoptosis of neuroblastoma cells. J Biol Chem. 2004;279(6):4058–65.PubMedCrossRef
29.
go back to reference Maeda S, Karin M. Oncogene at last--c-Jun promotes liver cancer in mice. Cancer Cell. 2003;3(2):102–4.PubMedCrossRef Maeda S, Karin M. Oncogene at last--c-Jun promotes liver cancer in mice. Cancer Cell. 2003;3(2):102–4.PubMedCrossRef
31.
go back to reference Leppa S, Saffrich R, Ansorge W, Bohmann D. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 1998;17(15):4404–13.PubMedPubMedCentralCrossRef Leppa S, Saffrich R, Ansorge W, Bohmann D. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 1998;17(15):4404–13.PubMedPubMedCentralCrossRef
32.
go back to reference Win S, Than TA, Zhang J, Oo C, Min RWM, Kaplowitz N. New insights into the role and mechanism of c-Jun-N-terminal kinase signaling in the pathobiology of liver diseases. Hepatology. 2018;67(5):2013–24.PubMedCrossRef Win S, Than TA, Zhang J, Oo C, Min RWM, Kaplowitz N. New insights into the role and mechanism of c-Jun-N-terminal kinase signaling in the pathobiology of liver diseases. Hepatology. 2018;67(5):2013–24.PubMedCrossRef
33.
go back to reference Win S, Than TA, Fernandez-Checa JC, Kaplowitz N. JNK interaction with Sab mediates ER stress induced inhibition of mitochondrial respiration and cell death. Cell Death Dis. 2014;5:e989.PubMedPubMedCentralCrossRef Win S, Than TA, Fernandez-Checa JC, Kaplowitz N. JNK interaction with Sab mediates ER stress induced inhibition of mitochondrial respiration and cell death. Cell Death Dis. 2014;5:e989.PubMedPubMedCentralCrossRef
34.
go back to reference Lee CM, Lo H-W, Shao R-P, Wang S-C, Xia W, Gershenson DM, Hung M-C. Selective activation of ceruloplasmin promoter in ovarian tumors. Cancer Res. 2004;64(5):1788–93.PubMedCrossRef Lee CM, Lo H-W, Shao R-P, Wang S-C, Xia W, Gershenson DM, Hung M-C. Selective activation of ceruloplasmin promoter in ovarian tumors. Cancer Res. 2004;64(5):1788–93.PubMedCrossRef
35.
go back to reference Huang L, Jin Y, Feng S, Zou Y, Xu S, Qiu S, Li L, Zheng J. Role of Wnt/beta-catenin, Wnt/c-Jun N-terminal kinase and Wnt/Ca (2+) pathways in cisplatin-induced chemoresistance in ovarian cancer. Exp Ther Med. 2016;12(6):3851–8.PubMedPubMedCentralCrossRef Huang L, Jin Y, Feng S, Zou Y, Xu S, Qiu S, Li L, Zheng J. Role of Wnt/beta-catenin, Wnt/c-Jun N-terminal kinase and Wnt/Ca (2+) pathways in cisplatin-induced chemoresistance in ovarian cancer. Exp Ther Med. 2016;12(6):3851–8.PubMedPubMedCentralCrossRef
38.
40.
go back to reference Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 2008;30(6):678–88.PubMedPubMedCentralCrossRef Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 2008;30(6):678–88.PubMedPubMedCentralCrossRef
41.
go back to reference Lu Z, Miao Y, Muhammad I, Tian E, Hu W, Wang J, Wang B, Li R, Li J. Colistin-induced autophagy and apoptosis involves the JNK-Bcl2-Bax signaling pathway and JNK-p53-ROS positive feedback loop in PC-12 cells. Chem Biol Interact. 2017;277:62–73.PubMedCrossRef Lu Z, Miao Y, Muhammad I, Tian E, Hu W, Wang J, Wang B, Li R, Li J. Colistin-induced autophagy and apoptosis involves the JNK-Bcl2-Bax signaling pathway and JNK-p53-ROS positive feedback loop in PC-12 cells. Chem Biol Interact. 2017;277:62–73.PubMedCrossRef
42.
go back to reference Bhattacharjee A, Hasanain M, Kathuria M, Singh A, Datta D, Sarkar J, Mitra K. Ormeloxifene-induced unfolded protein response contributes to autophagy-associated apoptosis via disruption of Akt/mTOR and activation of JNK. Sci Rep. 2018;8(1):2303.PubMedPubMedCentralCrossRef Bhattacharjee A, Hasanain M, Kathuria M, Singh A, Datta D, Sarkar J, Mitra K. Ormeloxifene-induced unfolded protein response contributes to autophagy-associated apoptosis via disruption of Akt/mTOR and activation of JNK. Sci Rep. 2018;8(1):2303.PubMedPubMedCentralCrossRef
43.
go back to reference Wang Y, Singh R, Xiang Y, Czaja MJ. Macroautophagy and chaperone-mediated autophagy are required for hepatocyte resistance to oxidant stress. Hepatology. 2010;52(1):266–77.PubMedCrossRef Wang Y, Singh R, Xiang Y, Czaja MJ. Macroautophagy and chaperone-mediated autophagy are required for hepatocyte resistance to oxidant stress. Hepatology. 2010;52(1):266–77.PubMedCrossRef
44.
go back to reference Xu L, Zhang X, Li Y, Lu S, Lu S, Li J, Wang Y, Tian X, Wei JJ, Shao C, et al. Neferine induces autophagy of human ovarian cancer cells via p38 MAPK/ JNK activation. Tumour Biol. 2016;37(7):8721–9.PubMedCrossRef Xu L, Zhang X, Li Y, Lu S, Lu S, Li J, Wang Y, Tian X, Wei JJ, Shao C, et al. Neferine induces autophagy of human ovarian cancer cells via p38 MAPK/ JNK activation. Tumour Biol. 2016;37(7):8721–9.PubMedCrossRef
45.
go back to reference Zhang K, Kaufman RJ. Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem. 2004;279(25):25935–8.PubMedCrossRef Zhang K, Kaufman RJ. Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem. 2004;279(25):25935–8.PubMedCrossRef
46.
go back to reference Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis. 2006;11(1):5–13.CrossRefPubMed Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis. 2006;11(1):5–13.CrossRefPubMed
47.
go back to reference Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013;32(7):805–18.CrossRefPubMed Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013;32(7):805–18.CrossRefPubMed
48.
go back to reference Zheng GF, Cai Z, Meng XK, Zhang Y, Zhu W, Pang XY, Dou L. Unfolded protein response mediated JNK/AP-1 signal transduction, a target for ovarian cancer treatment. Int J Clin Exp Pathol. 2015;8(6):6505–11.PubMedPubMedCentral Zheng GF, Cai Z, Meng XK, Zhang Y, Zhu W, Pang XY, Dou L. Unfolded protein response mediated JNK/AP-1 signal transduction, a target for ovarian cancer treatment. Int J Clin Exp Pathol. 2015;8(6):6505–11.PubMedPubMedCentral
49.
go back to reference Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem. 2001;276(17):13935–40.PubMedCrossRef Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem. 2001;276(17):13935–40.PubMedCrossRef
50.
go back to reference Tong Q, Wu L, Gao Q, Ou Z, Zhu D, Zhang Y. PPARbeta/delta agonist provides neuroprotection by suppression of IRE1alpha-caspase-12-mediated endoplasmic reticulum stress pathway in the rotenone rat model of Parkinson’s disease. Mol Neurobiol. 2016;53(6):3822–31.PubMedCrossRef Tong Q, Wu L, Gao Q, Ou Z, Zhu D, Zhang Y. PPARbeta/delta agonist provides neuroprotection by suppression of IRE1alpha-caspase-12-mediated endoplasmic reticulum stress pathway in the rotenone rat model of Parkinson’s disease. Mol Neurobiol. 2016;53(6):3822–31.PubMedCrossRef
51.
go back to reference Ma L, Wei J, Wan J, Wang W, Wang L, Yuan Y, Yang Z, Liu X, Ming L. Low glucose and metformin-induced apoptosis of human ovarian cancer cells is connected to ASK1 via mitochondrial and endoplasmic reticulum stress-associated pathways. J Exp Clin Cancer Res. 2019;38(1):77.PubMedPubMedCentralCrossRef Ma L, Wei J, Wan J, Wang W, Wang L, Yuan Y, Yang Z, Liu X, Ming L. Low glucose and metformin-induced apoptosis of human ovarian cancer cells is connected to ASK1 via mitochondrial and endoplasmic reticulum stress-associated pathways. J Exp Clin Cancer Res. 2019;38(1):77.PubMedPubMedCentralCrossRef
52.
go back to reference Amos LA, Ma FY, Tesch GH, Liles JT, Breckenridge DG, Nikolic-Paterson DJ, Han Y. ASK1 inhibitor treatment suppresses p38/JNK signalling with reduced kidney inflammation and fibrosis in rat crescentic glomerulonephritis. J Cell Mol Med. 2018;22(9):4522–33.PubMedPubMedCentralCrossRef Amos LA, Ma FY, Tesch GH, Liles JT, Breckenridge DG, Nikolic-Paterson DJ, Han Y. ASK1 inhibitor treatment suppresses p38/JNK signalling with reduced kidney inflammation and fibrosis in rat crescentic glomerulonephritis. J Cell Mol Med. 2018;22(9):4522–33.PubMedPubMedCentralCrossRef
54.
go back to reference Kajihara N, Kukidome D, Sada K, Motoshima H, Furukawa N, Matsumura T, Nishikawa T, Araki E. Low glucose induces mitochondrial reactive oxygen species via fatty acid oxidation in bovine aortic endothelial cells. J Diabetes Investig. 2017;8(6):750–61.PubMedPubMedCentralCrossRef Kajihara N, Kukidome D, Sada K, Motoshima H, Furukawa N, Matsumura T, Nishikawa T, Araki E. Low glucose induces mitochondrial reactive oxygen species via fatty acid oxidation in bovine aortic endothelial cells. J Diabetes Investig. 2017;8(6):750–61.PubMedPubMedCentralCrossRef
55.
go back to reference Choudhury S, Bae S, Ke Q, Lee JY, Kim J, Kang PM. Mitochondria to nucleus translocation of AIF in mice lacking Hsp70 during ischemia/reperfusion. Basic Res Cardiol. 2011;106(3):397–407.PubMedPubMedCentralCrossRef Choudhury S, Bae S, Ke Q, Lee JY, Kim J, Kang PM. Mitochondria to nucleus translocation of AIF in mice lacking Hsp70 during ischemia/reperfusion. Basic Res Cardiol. 2011;106(3):397–407.PubMedPubMedCentralCrossRef
56.
go back to reference Sharifi S, Barar J, Hejazi MS, Samadi N. Doxorubicin changes Bax /Bcl-xL ratio, caspase-8 and 9 in breast cancer cells. Adv Pharm Bull. 2015;5(3):351–9.PubMedPubMedCentralCrossRef Sharifi S, Barar J, Hejazi MS, Samadi N. Doxorubicin changes Bax /Bcl-xL ratio, caspase-8 and 9 in breast cancer cells. Adv Pharm Bull. 2015;5(3):351–9.PubMedPubMedCentralCrossRef
57.
go back to reference Hata AN, Engelman JA, Faber AC. The BCL2 family: key mediators of the apoptotic response to targeted anticancer therapeutics. Cancer Discov. 2015;5(5):475–87.PubMedPubMedCentralCrossRef Hata AN, Engelman JA, Faber AC. The BCL2 family: key mediators of the apoptotic response to targeted anticancer therapeutics. Cancer Discov. 2015;5(5):475–87.PubMedPubMedCentralCrossRef
58.
go back to reference Shen K, Xie J, Wang H, Zhang H, Yu M, Lu F, Tan H, Xu H. Cambogin induces caspase-independent apoptosis through the ROS/JNK pathway and epigenetic regulation in breast cancer cells. Mol Cancer Ther. 2015;14(7):1738–49.PubMedCrossRef Shen K, Xie J, Wang H, Zhang H, Yu M, Lu F, Tan H, Xu H. Cambogin induces caspase-independent apoptosis through the ROS/JNK pathway and epigenetic regulation in breast cancer cells. Mol Cancer Ther. 2015;14(7):1738–49.PubMedCrossRef
59.
go back to reference Chen YJ, Liu WH, Kao PH, Wang JJ, Chang LS. Involvement of p38 MAPK- and JNK-modulated expression of Bcl-2 and Bax in Naja nigricollis CMS-9-induced apoptosis of human leukemia K562 cells. Toxicon. 2010;55(7):1306–16.PubMedCrossRef Chen YJ, Liu WH, Kao PH, Wang JJ, Chang LS. Involvement of p38 MAPK- and JNK-modulated expression of Bcl-2 and Bax in Naja nigricollis CMS-9-induced apoptosis of human leukemia K562 cells. Toxicon. 2010;55(7):1306–16.PubMedCrossRef
60.
go back to reference Cui ZY, Park SJ, Jo E, Hwang IH, Lee KB, Kim SW, Kim DJ, Joo JC, Hong SH, Lee MG, et al. Cordycepin induces apoptosis of human ovarian cancer cells by inhibiting CCL5-mediated Akt/NF-kappaB signaling pathway. Cell Death Discov. 2018;4:62.PubMedPubMedCentralCrossRef Cui ZY, Park SJ, Jo E, Hwang IH, Lee KB, Kim SW, Kim DJ, Joo JC, Hong SH, Lee MG, et al. Cordycepin induces apoptosis of human ovarian cancer cells by inhibiting CCL5-mediated Akt/NF-kappaB signaling pathway. Cell Death Discov. 2018;4:62.PubMedPubMedCentralCrossRef
61.
go back to reference Chen TC, Yu MC, Chien CC, Wu MS, Lee YC, Chen YC. Nilotinib reduced the viability of human ovarian cancer cells via mitochondria-dependent apoptosis, independent of JNK activation. Toxicol in Vitro. 2016;31:1–11.PubMedCrossRef Chen TC, Yu MC, Chien CC, Wu MS, Lee YC, Chen YC. Nilotinib reduced the viability of human ovarian cancer cells via mitochondria-dependent apoptosis, independent of JNK activation. Toxicol in Vitro. 2016;31:1–11.PubMedCrossRef
62.
go back to reference Vivas-Mejia P, Benito JM, Fernandez A, Han HD, Mangala L, Rodriguez-Aguayo C, Chavez-Reyes A, Lin YG, Carey MS, Nick AM, et al. c-Jun-NH2-kinase-1 inhibition leads to antitumor activity in ovarian cancer. Clin Cancer Res. 2010;16(1):184–94.PubMedCrossRef Vivas-Mejia P, Benito JM, Fernandez A, Han HD, Mangala L, Rodriguez-Aguayo C, Chavez-Reyes A, Lin YG, Carey MS, Nick AM, et al. c-Jun-NH2-kinase-1 inhibition leads to antitumor activity in ovarian cancer. Clin Cancer Res. 2010;16(1):184–94.PubMedCrossRef
63.
go back to reference du Bois A, Kristensen G, Ray-Coquard I, Reuss A, Pignata S, Colombo N, Denison U, Vergote I, del Campo JM, Ottevanger P, et al. Standard first-line chemotherapy with or without nintedanib for advanced ovarian cancer (AGO-OVAR 12): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet Oncol. 2016;17(1):78–89.PubMedCrossRef du Bois A, Kristensen G, Ray-Coquard I, Reuss A, Pignata S, Colombo N, Denison U, Vergote I, del Campo JM, Ottevanger P, et al. Standard first-line chemotherapy with or without nintedanib for advanced ovarian cancer (AGO-OVAR 12): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet Oncol. 2016;17(1):78–89.PubMedCrossRef
64.
go back to reference Barra F, Lagana AS, Ghezzi F, Casarin J, Ferrero S. Nintedanib for advanced epithelial ovarian cancer: a change of perspective? Summary of evidence from a systematic review. Gynecol Obstet Investig. 2019;84(2):107–17.CrossRef Barra F, Lagana AS, Ghezzi F, Casarin J, Ferrero S. Nintedanib for advanced epithelial ovarian cancer: a change of perspective? Summary of evidence from a systematic review. Gynecol Obstet Investig. 2019;84(2):107–17.CrossRef
65.
go back to reference Kamio K, Usuki J, Azuma A, Matsuda K, Ishii T, Inomata M, Hayashi H, Kokuho N, Fujita K, Saito Y, et al. Nintedanib modulates surfactant protein-D expression in A549 human lung epithelial cells via the c-Jun N-terminal kinase-activator protein-1 pathway. Pulm Pharmacol Ther. 2015;32:29–36.PubMedCrossRef Kamio K, Usuki J, Azuma A, Matsuda K, Ishii T, Inomata M, Hayashi H, Kokuho N, Fujita K, Saito Y, et al. Nintedanib modulates surfactant protein-D expression in A549 human lung epithelial cells via the c-Jun N-terminal kinase-activator protein-1 pathway. Pulm Pharmacol Ther. 2015;32:29–36.PubMedCrossRef
66.
go back to reference Liu J, Wang L, Zhang Y, Li S, Sun F, Wang G, Yang T, Wei D, Guo L, Xiao H. Induction of entosis in prostate cancer cells by nintedanib and its therapeutic implications. Oncol Lett. 2019;17(3):3151–62.PubMedPubMedCentral Liu J, Wang L, Zhang Y, Li S, Sun F, Wang G, Yang T, Wei D, Guo L, Xiao H. Induction of entosis in prostate cancer cells by nintedanib and its therapeutic implications. Oncol Lett. 2019;17(3):3151–62.PubMedPubMedCentral
67.
go back to reference Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron. 1999;22(4):667–76.PubMedCrossRef Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron. 1999;22(4):667–76.PubMedCrossRef
68.
70.
go back to reference Bowtell DD, Bohm S, Ahmed AA, Aspuria PJ, Bast RC Jr, Beral V, Berek JS, Birrer MJ, Blagden S, Bookman MA, et al. Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer. Nat Rev Cancer. 2015;15(11):668–79.PubMedPubMedCentralCrossRef Bowtell DD, Bohm S, Ahmed AA, Aspuria PJ, Bast RC Jr, Beral V, Berek JS, Birrer MJ, Blagden S, Bookman MA, et al. Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer. Nat Rev Cancer. 2015;15(11):668–79.PubMedPubMedCentralCrossRef
71.
go back to reference Zhang Y, Cao L, Nguyen D, Lu H. TP53 mutations in epithelial ovarian cancer. Transl Cancer Res. 2016;5(6):650–63.PubMedCrossRef Zhang Y, Cao L, Nguyen D, Lu H. TP53 mutations in epithelial ovarian cancer. Transl Cancer Res. 2016;5(6):650–63.PubMedCrossRef
72.
go back to reference Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, Stewart C, Fereday S, Caldas C, Defazio A, et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol. 2010;221(1):49–56.PubMedPubMedCentralCrossRef Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, Stewart C, Fereday S, Caldas C, Defazio A, et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol. 2010;221(1):49–56.PubMedPubMedCentralCrossRef
73.
go back to reference Ma X, Lu JY, Dong Y, Li D, Malagon JN, Xu T. PP6 disruption synergizes with oncogenic Ras to promote JNK-dependent tumor growth and invasion. Cell Rep. 2017;19(13):2657–64.PubMedPubMedCentralCrossRef Ma X, Lu JY, Dong Y, Li D, Malagon JN, Xu T. PP6 disruption synergizes with oncogenic Ras to promote JNK-dependent tumor growth and invasion. Cell Rep. 2017;19(13):2657–64.PubMedPubMedCentralCrossRef
74.
go back to reference Lim V, Zhu H, Diao S, Hu L, Hu J. PKP3 interactions with MAPK-JNK-ERK1/2-mTOR pathway regulates autophagy and invasion in ovarian cancer. Biochem Biophys Res Commun. 2019;508(2):646–53.PubMedCrossRef Lim V, Zhu H, Diao S, Hu L, Hu J. PKP3 interactions with MAPK-JNK-ERK1/2-mTOR pathway regulates autophagy and invasion in ovarian cancer. Biochem Biophys Res Commun. 2019;508(2):646–53.PubMedCrossRef
75.
go back to reference Echevarria-Vargas IM, Valiyeva F, Vivas-Mejia PE. Upregulation of miR-21 in cisplatin resistant ovarian cancer via JNK-1/c-Jun pathway. PLoS One. 2014;9(5):e97094.PubMedPubMedCentralCrossRef Echevarria-Vargas IM, Valiyeva F, Vivas-Mejia PE. Upregulation of miR-21 in cisplatin resistant ovarian cancer via JNK-1/c-Jun pathway. PLoS One. 2014;9(5):e97094.PubMedPubMedCentralCrossRef
76.
go back to reference Gao N, Liu J, Liu D, Hao Y, Yan L, Ma Y, Zhuang H, Hu Z, Gao J, Yang Z, et al. c-Jun transcriptionally regulates alpha 1, 2-fucosyltransferase 1 (FUT1) in ovarian cancer. Biochimie. 2014;107 Pt B:286–92.PubMedCrossRef Gao N, Liu J, Liu D, Hao Y, Yan L, Ma Y, Zhuang H, Hu Z, Gao J, Yang Z, et al. c-Jun transcriptionally regulates alpha 1, 2-fucosyltransferase 1 (FUT1) in ovarian cancer. Biochimie. 2014;107 Pt B:286–92.PubMedCrossRef
77.
go back to reference Hao Y, Zhu L, Yan L, Liu J, Liu D, Gao N, Tan M, Gao S, Lin B. c-Fos mediates alpha1, 2-fucosyltransferase 1 and Lewis y expression in response to TGF-beta1 in ovarian cancer. Oncol Rep. 2017;38(6):3355–66.PubMedPubMedCentral Hao Y, Zhu L, Yan L, Liu J, Liu D, Gao N, Tan M, Gao S, Lin B. c-Fos mediates alpha1, 2-fucosyltransferase 1 and Lewis y expression in response to TGF-beta1 in ovarian cancer. Oncol Rep. 2017;38(6):3355–66.PubMedPubMedCentral
78.
go back to reference Dong C, Ye DX, Zhang WB, Pan HY, Zhang ZY, Zhang L. Overexpression of c-fos promotes cell invasion and migration via CD44 pathway in oral squamous cell carcinoma. J Oral Pathol Med. 2015;44(5):353–60.PubMedCrossRef Dong C, Ye DX, Zhang WB, Pan HY, Zhang ZY, Zhang L. Overexpression of c-fos promotes cell invasion and migration via CD44 pathway in oral squamous cell carcinoma. J Oral Pathol Med. 2015;44(5):353–60.PubMedCrossRef
79.
go back to reference Mikula-Pietrasik J, Sosinska P, Naumowicz E, Maksin K, Piotrowska H, Wozniak A, Szpurek D, Ksiazek K. Senescent peritoneal mesothelium induces a pro-angiogenic phenotype in ovarian cancer cells in vitro and in a mouse xenograft model in vivo. Clin Exp Metastasis. 2016;33(1):15–27.PubMedCrossRef Mikula-Pietrasik J, Sosinska P, Naumowicz E, Maksin K, Piotrowska H, Wozniak A, Szpurek D, Ksiazek K. Senescent peritoneal mesothelium induces a pro-angiogenic phenotype in ovarian cancer cells in vitro and in a mouse xenograft model in vivo. Clin Exp Metastasis. 2016;33(1):15–27.PubMedCrossRef
81.
go back to reference Papa S, Zazzeroni F, Pham CG, Bubici C, Franzoso G. Linking JNK signaling to NF-kappaB: a key to survival. J Cell Sci. 2004;117(Pt 22):5197–208.PubMedCrossRef Papa S, Zazzeroni F, Pham CG, Bubici C, Franzoso G. Linking JNK signaling to NF-kappaB: a key to survival. J Cell Sci. 2004;117(Pt 22):5197–208.PubMedCrossRef
82.
go back to reference Deng X, Xiao L, Lang W, Gao F, Ruvolo P, May WS Jr. Novel role for JNK as a stress-activated Bcl2 kinase. J Biol Chem. 2001;276(26):23681–8.PubMedCrossRef Deng X, Xiao L, Lang W, Gao F, Ruvolo P, May WS Jr. Novel role for JNK as a stress-activated Bcl2 kinase. J Biol Chem. 2001;276(26):23681–8.PubMedCrossRef
83.
go back to reference Yuan D, Huang S, Berger E, Liu L, Gross N, Heinzmann F, Ringelhan M, Connor TO, Stadler M, Meister M, et al. Kupffer cell-derived Tnf triggers cholangiocellular tumorigenesis through JNK due to chronic mitochondrial dysfunction and ROS. Cancer Cell. 2017;31(6):771–89 e776.PubMedCrossRefPubMedCentral Yuan D, Huang S, Berger E, Liu L, Gross N, Heinzmann F, Ringelhan M, Connor TO, Stadler M, Meister M, et al. Kupffer cell-derived Tnf triggers cholangiocellular tumorigenesis through JNK due to chronic mitochondrial dysfunction and ROS. Cancer Cell. 2017;31(6):771–89 e776.PubMedCrossRefPubMedCentral
85.
go back to reference Ham Y-M, Chun K-H, Choi J-S, Kim D-H, Lee S-K. SEK1-dependent JNK1 activation prolongs cell survival during G-Rh2-induced apoptosis. Biochem Biophys Res Commun. 2003;304(2):358–64.PubMedCrossRef Ham Y-M, Chun K-H, Choi J-S, Kim D-H, Lee S-K. SEK1-dependent JNK1 activation prolongs cell survival during G-Rh2-induced apoptosis. Biochem Biophys Res Commun. 2003;304(2):358–64.PubMedCrossRef
86.
go back to reference Laganà AS, Colonese F, Colonese E, Sofo V, Salmeri FM, Granese R, Chiofalo B, Ciancimino L, Triolo O. Cytogenetic analysis of epithelial ovarian cancer’s stem cells: an overview on new diagnostic and therapeutic perspectives. Eur J Gynaecol Oncol. 2015;36(5):495–505.PubMed Laganà AS, Colonese F, Colonese E, Sofo V, Salmeri FM, Granese R, Chiofalo B, Ciancimino L, Triolo O. Cytogenetic analysis of epithelial ovarian cancer’s stem cells: an overview on new diagnostic and therapeutic perspectives. Eur J Gynaecol Oncol. 2015;36(5):495–505.PubMed
87.
go back to reference Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science. 2011;331(6024):1565–70.PubMedCrossRef Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science. 2011;331(6024):1565–70.PubMedCrossRef
88.
go back to reference Lagana AS, Sofo V, Vitale SG, Triolo O. Epithelial ovarian cancer inherent resistance: may the pleiotropic interaction between reduced immunosurveillance and drug-resistant cells play a key role? Gynecol Oncol Rep. 2016;18:57–8.PubMedPubMedCentralCrossRef Lagana AS, Sofo V, Vitale SG, Triolo O. Epithelial ovarian cancer inherent resistance: may the pleiotropic interaction between reduced immunosurveillance and drug-resistant cells play a key role? Gynecol Oncol Rep. 2016;18:57–8.PubMedPubMedCentralCrossRef
90.
go back to reference Sui X, Kong N, Wang X, Fang Y, Hu X, Xu Y, Chen W, Wang K, Li D, Jin W, et al. JNK confers 5-fluorouracil resistance in p53-deficient and mutant p53-expressing colon cancer cells by inducing survival autophagy. Sci Rep. 2014;4:4694.PubMedPubMedCentralCrossRef Sui X, Kong N, Wang X, Fang Y, Hu X, Xu Y, Chen W, Wang K, Li D, Jin W, et al. JNK confers 5-fluorouracil resistance in p53-deficient and mutant p53-expressing colon cancer cells by inducing survival autophagy. Sci Rep. 2014;4:4694.PubMedPubMedCentralCrossRef
92.
go back to reference Seino M, Okada M, Sakaki H, Takeda H, Watarai H, Suzuki S, Seino S, Kuramoto K, Ohta T, Nagase S, et al. Time-staggered inhibition of JNK effectively sensitizes chemoresistant ovarian cancer cells to cisplatin and paclitaxel. Oncol Rep. 2016;35(1):593–601.PubMedCrossRef Seino M, Okada M, Sakaki H, Takeda H, Watarai H, Suzuki S, Seino S, Kuramoto K, Ohta T, Nagase S, et al. Time-staggered inhibition of JNK effectively sensitizes chemoresistant ovarian cancer cells to cisplatin and paclitaxel. Oncol Rep. 2016;35(1):593–601.PubMedCrossRef
93.
go back to reference Van Meter M, Simon M, Tombline G, May A, Morello TD, Hubbard BP, Bredbenner K, Park R, Sinclair DA, Bohr VA, et al. JNK phosphorylates SIRT6 to stimulate DNA double-strand break repair in response to oxidative stress by recruiting PARP1 to DNA breaks. Cell Rep. 2016;16(10):2641–50.PubMedPubMedCentralCrossRef Van Meter M, Simon M, Tombline G, May A, Morello TD, Hubbard BP, Bredbenner K, Park R, Sinclair DA, Bohr VA, et al. JNK phosphorylates SIRT6 to stimulate DNA double-strand break repair in response to oxidative stress by recruiting PARP1 to DNA breaks. Cell Rep. 2016;16(10):2641–50.PubMedPubMedCentralCrossRef
94.
go back to reference Marquez RT, Xu L. Bcl-2: Beclin 1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch. Am J Cancer Res. 2012;2(2):214–21.PubMedPubMedCentral Marquez RT, Xu L. Bcl-2: Beclin 1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch. Am J Cancer Res. 2012;2(2):214–21.PubMedPubMedCentral
96.
go back to reference Yang J, Yao S. JNK-Bcl-2/Bcl-xL-Bax/Bak pathway mediates the crosstalk between matrine-induced autophagy and apoptosis via interplay with beclin 1. Int J Mol Sci. 2015;16(10):25744–58.PubMedPubMedCentralCrossRef Yang J, Yao S. JNK-Bcl-2/Bcl-xL-Bax/Bak pathway mediates the crosstalk between matrine-induced autophagy and apoptosis via interplay with beclin 1. Int J Mol Sci. 2015;16(10):25744–58.PubMedPubMedCentralCrossRef
97.
go back to reference Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, Zeng YX, Shao JY. MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA. 2008;14(11):2348–60.PubMedPubMedCentralCrossRef Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, Zeng YX, Shao JY. MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA. 2008;14(11):2348–60.PubMedPubMedCentralCrossRef
98.
go back to reference Gaur AB, Holbeck SL, Colburn NH, Israel MA. Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro-Oncology. 2011;13(6):580–90.PubMedPubMedCentralCrossRef Gaur AB, Holbeck SL, Colburn NH, Israel MA. Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro-Oncology. 2011;13(6):580–90.PubMedPubMedCentralCrossRef
99.
go back to reference Chen S, Chen X, Shan T, Ma J, Lin W, Li W, Kang Y. MiR-21-mediated metabolic alteration of cancer-associated fibroblasts and its effect on pancreatic cancer cell behavior. Int J Biol Sci. 2018;14(1):100–10.PubMedPubMedCentralCrossRef Chen S, Chen X, Shan T, Ma J, Lin W, Li W, Kang Y. MiR-21-mediated metabolic alteration of cancer-associated fibroblasts and its effect on pancreatic cancer cell behavior. Int J Biol Sci. 2018;14(1):100–10.PubMedPubMedCentralCrossRef
100.
go back to reference Wu J, Sun Y, Zhang PY, Qian M, Zhang H, Chen X, Ma D, Xu Y, Chen X, Tang KF. The Fra-1-miR-134-SDS22 feedback loop amplifies ERK/JNK signaling and reduces chemosensitivity in ovarian cancer cells. Cell Death Dis. 2016;7(9):e2384.PubMedPubMedCentralCrossRef Wu J, Sun Y, Zhang PY, Qian M, Zhang H, Chen X, Ma D, Xu Y, Chen X, Tang KF. The Fra-1-miR-134-SDS22 feedback loop amplifies ERK/JNK signaling and reduces chemosensitivity in ovarian cancer cells. Cell Death Dis. 2016;7(9):e2384.PubMedPubMedCentralCrossRef
101.
go back to reference Jiang Y, Jiang J, Jia H, Qiao Z, Zhang J. Recovery of miR-139-5p in ovarian cancer reverses cisplatin resistance by targeting C-Jun. Cell Physiol Biochem. 2018;51(1):129–41.PubMedCrossRef Jiang Y, Jiang J, Jia H, Qiao Z, Zhang J. Recovery of miR-139-5p in ovarian cancer reverses cisplatin resistance by targeting C-Jun. Cell Physiol Biochem. 2018;51(1):129–41.PubMedCrossRef
Metadata
Title
The Jun N-terminal kinases signaling pathway plays a “seesaw” role in ovarian carcinoma: a molecular aspect
Authors
Yingyu Dou
Xiaoyan Jiang
Hui Xie
Junyu He
Songshu Xiao
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2019
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/s13048-019-0573-6

Other articles of this Issue 1/2019

Journal of Ovarian Research 1/2019 Go to the issue