Hsp90 inhibitor 17-AAG sensitizes Bcl-2 inhibitor (-)-gossypol by suppressing ERK-mediated protective autophagy and Mcl-1 accumulation in hepatocellular carcinoma cells

Experimental Cell Research

Volumn 328, Issue 2, 2014, Pages 379-387

  Wang, Bin ^a   Chen, Linfeng ^b   Ni, Zhenhong ^a   Dai, Xufang ^c   Qin, Liyan ^a   Wu, Yaran ^a   Li, Xinzhe ^a   Xu, Liang ^d   Lian, Jiqin ^a   He, Fengtian ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c CHONGQING NORMAL UNIVERSITY   (China)

^d UNIVERSITY OF KANSAS CANCER CENTER   (United States)

Author keywords

( ) Gossypol; Autophagy; Bcl 2; ERK; Hsp90

Indexed keywords

BECLIN 1; GOSSYPOL; HEAT SHOCK PROTEIN 90; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN MCL 1; TANESPIMYCIN; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; BENZOQUINONE DERIVATIVE; LIGHT CHAIN 3, HUMAN; MACROCYCLIC LACTAM; MCL1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MYELOID LEUKEMIA FACTOR 1; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIZATION; HEPATOCELLULAR CARCINOMA CELL LINE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; HEPG2 CELL LINE; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BENZOQUINONES; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GOSSYPOL; HEP G2 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; LIVER NEOPLASMS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84908173074     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.08.039     Document Type: Article

References (40)

1. El-Serag H.B., Rudolph K.L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007, 132:2557-2576.
2. Tanaka S., Arii S. Molecular targeted therapies in hepatocellular carcinoma. Semin. Oncol. 2012, 39:486-492.
3. Yang Y., Zhu J., Gou H., Cao D., Jiang M., Hou M. Clinical significance of Cox-2, Survivin and Bcl-2 expression in hepatocellular carcinoma (HCC). Med. Oncol. 2011, 28:796-803.
4. Chun E., Lee K.Y. Bcl-2 and Bcl-xL are important for the induction of paclitaxel resistance in human hepatocellular carcinoma cells. Biochem. Biophys. Res. Commun. 2004, 315:771-779.
5. Lessene G., Czabotar P.E., Colman P.M. BCL-2 family antagonists for cancer therapy. Nat. Rev. Drug Discov. 2008, 7:989-1000.
6. Xu L., Yang D., Wang S., Tang W., Liu M., Davis M., Chen J., Rae J.M., Lawrence T., Lippman M.E. (-)-Gossypol enhances response to radiation therapy and results in tumor regression of human prostate cancer. Mol. Cancer Ther. 2005, 4:197-205.
7. Wolter K.G., Wang S.J., Henson B.S., Wang S., Griffith K.A., Kumar B., Chen J., Carey T.E., Bradford C.R., D'Silva N.J. (-)-gossypol inhibits growth and promotes apoptosis of human head and neck squamous cell carcinoma in vivo. Neoplasia 2006, 8:163-172.
8. Lian J., Wu X., He F., Karnak D., Tang W., Meng Y., Xiang D., Ji M., Lawrence T.S., Xu L. A natural BH3 mimetic induces autophagy in apoptosis-resistant prostate cancer via modulating Bcl-2-Beclin1 interaction at endoplasmic reticulum. Cell Death Differ. 2011, 18:60-71.
9. Bajwa N., Liao C., Nikolovska-Coleska Z. Inhibitors of the anti-apoptotic Bcl-2 proteins: a patent review. Expert Opin. Ther. Pat. 2012, 22:37-55.
10. Cheng P., Ni Z., Dai X., Wang B., Ding W., Rae Smith A., Xu L., Wu D., He F., Lian J. The novel BH-3 mimetic apogossypolone induces Beclin-1- and ROS-mediated autophagy in human hepatocellular carcinoma [corrected] cells. Cell Death Dis. 2013, 4:e489.
11. Yufu Y., Nishimura J., Nawata H. High constitutive expression of heat shock protein 90 alpha in human acute leukemia cells. Leuk. Res. 1992, 16:597-605.
12. Ferrarini M., Heltai S., Zocchi M.R., Rugarli C. Unusual expression and localization of heat-shock proteins in human tumor cells. Int. J. Cancer 1992, 51:613-619.
13. Xu C., Liu J., Hsu L.C., Luo Y., Xiang R., Chuang T.H. Functional interaction of heat shock protein 90 and Beclin 1 modulates Toll-like receptor-mediated autophagy. FASEB J. 2011, 25:2700-2710.
14. Cohen-Saidon C., Carmi I., Keren A., Razin E. Antiapoptotic function of Bcl-2 in mast cells is dependent on its association with heat shock protein 90beta. Blood 2006, 107:1413-1420.
15. Schulte T.W., Blagosklonny M.V., Romanova L., Mushinski J.F., Monia B.P., Johnston J.F., Nguyen P., Trepel J., Neckers L.M. Destabilization of Raf-1 by geldanamycin leads to disruption of the Raf-1-MEK-mitogen-activated protein kinase signalling pathway. Mol. Cell. Biol. 1996, 16:5839-5845.
16. Seguin-Py S., Lucchi G., Croizier S., Chakrama F.Z., Despouy G., Le Grand J.N., Ducoroy P., Boireau W., Boyer-Guittaut M., Jouvenot M., Fraichard A., Delage-Mourroux R. Identification of HSP90 as a new GABARAPL1 (GEC1)-interacting protein. Biochimie 2012, 94:748-758.
17. Solit D.B., Basso A.D., Olshen A.B., Scher H.I., Rosen N. Inhibition of heat shock protein 90 function down-regulates Akt kinase and sensitizes tumors to Taxol. Cancer Res. 2003, 63:2139-2144.
18. McCollum A.K., Lukasiewicz K.B., Teneyck C.J., Lingle W.L., Toft D.O., Erlichman C. Cisplatin abrogates the geldanamycin-induced heat shock response. Mol. Cancer Ther. 2008, 7:3256-3264.
19. Yin X., Zhang H., Lundgren K., Wilson L., Burrows F., Shores C.G. BIIB021, a novel Hsp90 inhibitor, sensitizes head and neck squamous cell carcinoma to radiotherapy. Int. J. Cancer 2010, 126:1216-1225.
20. Tse A.N., Klimstra D.S., Gonen M., Shah M., Sheikh T., Sikorski R., Carvajal R., Mui J., Tipian C., O'Reilly E., Chung K., Maki R., Lefkowitz R., Brown K., Manova-Todorova K., Wu N., Egorin M.J., Kelsen D., Schwartz G.K. A phase 1 dose-escalation study of irinotecan in combination with 17-allylamino-17-demethoxygeldanamycin in patients with solid tumors. Clin. Cancer Res. 2008, 14:6704-6711.
21. Ramalingam S.S., Egorin M.J., Ramanathan R.K., Remick S.C., Sikorski R.P., Lagattuta T.F., Chatta G.S., Friedland D.M., Stoller R.G., Potter D.M., Ivy S.P., Belani C.P. A phase I study of 17-allylamino-17-demethoxygeldanamycin combined with paclitaxel in patients with advanced solid malignancies. Clin. Cancer Res. 2008, 14:3456-3461.
22. Modi S., Stopeck A., Linden H., Solit D., Chandarlapaty S., Rosen N., D'Andrea G., Dickler M., Moynahan M.E., Sugarman S., Ma W., Patil S., Norton L., Hannah A.L., Hudis C. HSP90 inhibition is effective in breast cancer: a phase II trial of tanespimycin (17-AAG) plus trastuzumab in patients with HER2-positive metastatic breast cancer progressing on trastuzumab. Clin. Cancer Res. 2011, 17:5132-5139.
23. Lian J., Ni Z., Dai X., Su C., Smith A.R., Xu L., He F. Sorafenib sensitizes (-)-gossypol-induced growth suppression in androgen-independent prostate cancer cells via Mcl-1 inhibition and Bak activation. Mol. Cancer Ther. 2012, 11:416-426.
24. Wang B., Ni Z., Dai X., Qin L., Li X., Xu L., Lian J., He F. The Bcl-2/xL inhibitor ABT-263 increases the stability of Mcl-1 mRNA and protein in hepatocellular carcinoma cells. Mol. Cancer 2014, 13:98.
25. Maiuri M.C., Criollo A., Tasdemir E., Vicencio J.M., Tajeddine N., Hickman J.A., Geneste O., Kroemer G. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 2007, 3:374-376.
26. Voss V., Senft C., Lang V., Ronellenfitsch M.W., Steinbach J.P., Seifert V., Kogel D. The pan-Bcl-2 inhibitor (-)-gossypol triggers autophagic cell death in malignant glioma. Mol. Cancer Res. 2010, 8:1002-1016.
27. Xu C., Liu J., Hsu L.C., Luo Y., Xiang R., Chuang TH. Functional interaction of heat shock protein 90 and Beclin 1 modulates Toll-like receptor-mediated autophagy. FASEB J. 2011, 25:2700-2710.
28. Soga S., Akinaga S., Shiotsu Y. Hsp90 inhibitors as anti-cancer agents, from basic discoveries to clinical development. Curr. Pharm. Des. 2013, 19:366-376.
29. Xiao D., Choi S., Johnson D.E., Vogel V.G., Johnson C.S., Trump D.L., Lee Y.J., Singh S.V. Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2. Oncogene 2004, 23:5594-5606.
30. Ni Z., Wang B., Dai X., Ding W., Yang T., Li X., Lewin S., Xu L., Lian J., He F. HCC cells with high levels of Bcl-2 are resistant to ABT-737 via activation of the ROS-JNK-autophagy pathway. Free Radic. Biol. Med. 2014, 70:194-203.
31. Yang Z., Klionsky D.J. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 2010, 12:814-822.
32. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol Cell Biol 2007, 8:741-752.
33. Ni Z., Dai X., Wang B., Ding W., Cheng P., Xu L., Lian J., He F. Natural Bcl-2 inhibitor (-)- gossypol induces protective autophagy via reactive oxygen species-high mobility group box 1 pathway in Burkitt lymphoma. Leuk. Lymphoma 2013, 54:2263-2268.
34. Seguin-Py S., Lucchi G., Croizier S., Chakrama F.Z., Despouy G., Le Grand J.N., Ducoroy P., Boireau W., Boyer-Guittaut M., Jouvenot M., Fraichard A., Delage-Mourroux R. Identification of HSP90 as a new GABARAPL1 (GEC1)-interacting protein. Biochimie 2012, 94:748-758.
35. Srivastava R.K., Srivastava A.R., Korsmeyer S.J., Nesterova M., Cho-Chung Y.S., Longo D.L. Involvement of microtubules in the regulation of Bcl2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinase. Mol. Cell. Biol. 1998, 18:3509-3517.
36. Stancato L.F., Silverstein A.M., Owens-Grillo J.K., Chow Y.H., Jove R., Pratt W.B. The hsp90-binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J. Biol. Chem. 1997, 272:4013-4020.
37. Akgul C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell. Mol. Life Sci. 2009, 66:1326-1336.
38. Domina AM VJ G.M., Hann S.R., Craig R.W. MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 2004, 23:5301-5315.
39. Zhang X.Q., Huang X.F., Hu X.B., Zhan Y.H., An Q.X., Yang S.M., Xia A.J., Yi J., Chen R., Mu S.J., Wu D.C. Apogossypolone, a novel inhibitor of antiapoptotic Bcl-2 family proteins, induces autophagy of PC-3 and LNCaP prostate cancer cells in vitro. Asian J. Androl. 2010, 12:697-708.
40. Mei H., Lin Z., Wang Y., Wu G., Song Y. Autophagy inhibition enhances pan-Bcl-2 inhibitor AT-101-induced apoptosis in non-small cell lung cancer. Neoplasma 2014, 16:186-192.