OPA1 downregulation is involved in sorafenib-induced apoptosis in hepatocellular carcinoma

Laboratory Investigation

Volumn 93, Issue 1, 2013, Pages 8-19

  Zhao, Xiangxuan ^a   Tian, Changhai ^b   Puszyk, William M ^a   Ogunwobi, Olorunseun O ^a   Cao, Mengde ^a   Wang, Ton ^a   Cabrera, Roniel ^a   Nelson, David R ^a   Liu, Chen ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

apoptosis; liver cancer; mitochondria fragmentation; OPA1; sorafenib

Indexed keywords

CYTOCHROME C; K RAS PROTEIN; OPTIC ATROPHY 1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN KINASE B; RAF PROTEIN; SMALL INTERFERING RNA; SORAFENIB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CARCINOMA CELL; CELL FRACTIONATION; CELL VIABILITY; CHEMOSENSITIZATION; CONTROLLED STUDY; CYTOSOLIC FRACTION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LIVER CELL; LIVER CELL CARCINOMA; LIVER MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR XENOGRAFT; WESTERN BLOTTING;

EID: 84871772322     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2012.144     Document Type: Article

References (48)

1. Jemal A, Murray T, Ward E, et al. Cancer Statistics CA Cancer J Clin 2005;55:10-30.
2. Frilling A, Malago M, Testa G, et al. Liver transplantation for metastasized extragastrointestinal stromal tumor: a case report and an overview of literature. Transplant Proc 2010;42:3843-3848.
3. Panka DJ, Wang W, Atkins MB, et al. The Raf inhibitor BAY 43-9006 (Sorafenib) induces caspase-independent apoptosis in melanoma cells. Cancer Res 2006;66:1611-1619. (Pubitemid 43259945)
4. Winkler J, Rech D, Kallert S, et al. Sorafenib induces sustained molecular remission in FLT3-ITD positive AML with relapse after second allogeneic stem cell transplantation without exacerbation of acute GVHD: a case report. Leuk Res 2010;34:e270-e272.
5. Guida T, Anaganti S, Provitera L, et al. Sorafenib inhibits imatinib-resistant KIT and platelet-derived growth factor receptor beta gatekeeper mutants. Clin Cancer Res 2007;13:3363-3369. (Pubitemid 46944924)
6. Keswani RN, Chumsangsri A, Mustafi R, et al. Sorafenib inhibits MAPK-mediated proliferation in a Barrett's esophageal adenocarcinoma cell line. Dis Esophagus 2008;21:514-521.
7. Busse A, Asemissen AM, Nonnenmacher A, et al. Immunomodulatory effects of sorafenib on peripheral immune effector cells in metastatic renal cell carcinoma. Eur J Cancer 2011;47:690-696.
8. Adnane L, Trail PA, Taylor I, et al. Sorafenib (BAY 43-9006, Nexavar), a dual-action inhibitor that targets RAF/MEK/ERK pathway in tumor cells and tyrosine kinases VEGFR/PDGFR in tumor vasculature. Methods Enzymol 2006;407:597-612. (Pubitemid 43815979)
9. Wilhelm SM, Adnane L, Newell P, et al. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol Cancer Ther 2008;7:3129-3140.
10. Ou DL, Shen YC, Yu SL, et al. Induction of DNA damage-inducible gene GADD45beta contributes to sorafenib-induced apoptosis in hepatocellular carcinoma cells. Cancer Res 2010;70:9309-9318.
11. Ou DL, Shen YC, Yu SL, et al. The Bcl-xL inhibitor, ABT-737, efficiently induces apoptosis and suppresses growth of hepatoma cells in combination with sorafenib. Hepatology 2010;52:1310-1321.
12. Shimizu S, Takehara T, Hikita H, et al. The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma. J Hepatol 2010;52:698-704.
13. Villanueva A, Llovet JM. Targeted therapies for hepatocellular carcinoma. Gastroenterology 2011;140:1410-1426.
14. Roberts LR. Sorafenib in liver cancer-just the beginning. N Engl J Med 2008;359:420-422.
15. Kim R, Byrne MT, Tan A, et al. What is the indication for sorafenib in hepatocellular carcinoma? A clinical challenge. Oncology 2011;25:295.
16. Zhu H, Dong H, Eksioglu E, et al. Hepatitis C triggers apoptosis of newly developed hepatoma cell line through anti-viral defense system. Gastroenterology 2007;133:1649-1659. (Pubitemid 350029762)
17. Ozawa K, Kitamura O, Yamaoka Y, et al. Hepatic cellular responses to liver cancer: abnormalities in metabolism of mitochondria isolated from human liver involved with carcinoma. Ann Surg 1974; 179:79-87.
18. Inaba K. Nucleic acids and protein synthesis in cancer cell mitochondria. II. Amino acid incorporation into proteins of rat liver and hepatoma cell mitochondria. Acta Med Okayama 1968;22:101-112.
19. Huang P, Yu T, Yoon Y. Mitochondrial clustering induced by overexpression of the mitochondrial fusion protein Mfn2 causes mitochondrial dysfunction and cell death. Eur J Cell Biol 2007;86:289-302. (Pubitemid 46825259)
20. Zhang E, Zhang C, Su Y, et al. Newly developed strategies for multifunctional mitochondria-targeted agents in cancer therapy. Drug Discov Today 2011;16:140-146.
21. Cheung EC, Joza N, Steenaart NA, et al. Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis. EMBO J 2006;25:4061-4073. (Pubitemid 44338747)
22. Chan DC. Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006;125:1241-1252. (Pubitemid 43929096)
23. Westermann B. Mitochondrial dynamics in model organisms: what yeasts, worms and flies have taught us about fusion and fission of mitochondria. Semin Cell Dev Biol 2010;21:542-549.
24. Wenner CE. Targeting mitochondria as a therapeutic target in cancer. J Cell Physiol 2012;227:450-456.
25. Yang F, Brown C, Buettner R, et al. Sorafenib induces growth arrest and apoptosis of human glioblastoma cells through the dephos-phorylation of signal transducers and activators of transcription 3. Mol Cancer Ther 2010;9:953-962.
26. Lei X, Chen Y, Du G. Gossypol induces Bax/Bak-independent activation of apoptosis and cytochrome c release via a conformational change in Bcl-2. FASEB J 2006;20:2147-2149.
27. Tian C, Erdmann N, Zhao J, et al. HIV-infected macrophages mediate neuronal apoptosis through mitochondrial glutaminase. J Neurochem 2008;105:994-1005. (Pubitemid 351562736)
28. Tian C, Murrin LC, Zheng JC. Mitochondrial fragmentation is involved in methamphetamine-induced cell death in rat hippocampal neural progenitor cells. PLoS One 2009;4:e5546.
29. Herrmann M, Lorenz HM, Voll R, et al. A rapid and simple method for the isolation of apoptotic DNA fragments. Nucleic Acids Res 1994; 22:5506-5507.
30. Zheng Y, Yamaguchi H, Tian C, et al. Arsenic trioxide (As(2)O(3)) induces apoptosis through activation of Bax in hematopoietic cells. Oncogene 2005;24:3339-3347. (Pubitemid 40695115)
31. Ramakrishnan V, Timm M, Haug JL, et al. Sorafenib, a dual Raf kinase/vascular endothelial growth factor receptor inhibitor has significant anti-myeloma activity and synergizes with common anti-myeloma drugs. Oncogene 2010;29:1190-1202.
32. Yu C, Friday BB, Lai JP, et al. Cytotoxic synergy between the multi-kinase inhibitor sorafenib and the proteasome inhibitor bortezomib in vitro: induction of apoptosis through Akt and c-Jun NH2-terminal kinase pathways. Mol Cancer Ther 2006;5:2378-2387. (Pubitemid 44530475)
33. Polyakov VY, Soukhomlinova MY, Fais D. Fusion, fragmentation, and fission of mitochondria. Biochemistry (Mosc) 2003;68:838-849.
34. Borentain P, Gregoire E, Hardwigsen J, et al. Liver transplantation in a patient treated by sorafenib for hepatocellular carcinoma. Clin Res Hepatol Gastroenterol 2011;35:234-236.
35. Sacco R, Bargellini I, Gianluigi G, et al. Complete response for advanced liver cancer during sorafenib therapy: case report. BMC Gastroenterol 2011;11:4.
36. Roderburg C, Bubenzer J, Spannbauer M, et al. Long-term survival of a HCC-patient with severe liver dysfunction treated with sorafenib. World J Hepatol 2010;2:239-242.
37. Takezawa K, Okamoto I, Yonesaka K, et al. Sorafenib inhibits non-small cell lung cancer cell growth by targeting B-RAF in KRAS wild-type cells and C-RAF in KRAS mutant cells. Cancer Res 2009;69:6515-6521.
38. Yokoyama H, Lundqvist A, Su S, et al. Toxic effects of sorafenib when given early after allogeneic hematopoietic stem cell transplantation. Blood 2010;116:2858-2859.
39. Gedaly R, Angulo P, Hundley J, et al. PI-103 and sorafenib inhibit hepatocellular carcinoma cell proliferation by blocking Ras/Raf/MAPK and PI3K/AKT/mTOR pathways. Anticancer Res 2010;30:4951-4958.
40. Chai H, Luo AZ, Weerasinghe P, et al. Sorafenib downregulates ERK/Akt and STAT3 survival pathways and induces apoptosis in a human neuroblastoma cell line. Int J Clin Exp Pathol 2010;3:408-415.
41. Chen KF, Yu HC, Liu TH, et al. Synergistic interactions between sorafenib and bortezomib in hepatocellular carcinoma involve PP2A-dependent Akt inactivation. J Hepatol 2010;52:88-95.
42. Rosato RR, Almenara JA, Coe S, et al. The multikinase inhibitor sorafenib potentiates TRAIL lethality in human leukemia cells in association with Mcl-1 and cFLIPL down-regulation. Cancer Res 2007;67:9490-9500. (Pubitemid 47535939)
43. Lierman E, Lahortiga I, Van MH, et al. The ability of sorafenib to inhibit oncogenic PDGFRbeta and FLT3 mutants and overcome resistance to other small molecule inhibitors. Haematologica 2007;92:27-34. (Pubitemid 46232655)
44. Semenzato M, Cogliati S, Scorrano L. Prohibitin(g) cancer: aurilide and killing by OPA1-dependent cristae remodelling. Chem Biol 2011;18:8-9.
45. Kahatri S, Plas DR. Targeting bioenergetics to enhance cancer chemotherapy. Cancer Biol Ther 2009;8:1659-1661.
46. Merkwirth C, Dargazanli S, Tatsuta T, et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 2008;22:476-488. (Pubitemid 351272755)
47. Piao L, Li Y, Kim SJ, et al. Regulation of OPA1-mediated mitochondrial fusion by leucine zipper/EF-hand-containing transmembrane protein-1 plays a role in apoptosis. Cell Signal 2009;21:767-777.
48. Chen L, Gong Q, Stice JP, et al. Mitochondrial OPA1, apoptosis, and heart failure. Cardiovasc Res 2009;84:91-99.