Knockdown of heme oxygenase-1 promotes apoptosis and autophagy and enhances the cytotoxicity of doxorubicin in breast cancer cells

Oncology Letters

Volumn 10, Issue 5, 2015, Pages 2974-2980

  Zhu, Xiao Feng ^a   Li, Wen ^a   Ma, Jie Yi ^a   Shao, Nan ^a   Zhang, Yun Jian ^a   Liu, Rui Ming ^a   Wu, Wei Bin ^a   Lin, Ying ^a   Wang, Shen Ming ^a  

^a THE FIRST AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; Breast cancer; Chemoresistance; Doxorubicin; Heme oxygenase 1

Indexed keywords

DOXORUBICIN; HEME OXYGENASE 1; PROTEIN BCL 2; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CELL VIABILITY; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; UPREGULATION; WESTERN BLOTTING;

EID: 84942413903     PISSN: 17921074     EISSN: 17921082     Source Type: Journal    
DOI: 10.3892/ol.2015.3735     Document Type: Article

References (37)

1. Libson S and Lippman M: A review of clinical aspects of breast cancer. Int Rev Psychiatry 26: 4-15, 2014.
2. Peto R, Davies C, Godwin J, Gray R, Pan HC, Clarke M, Cutter D, Darby S, McGale P, Taylor C, et al; Early Breast Cancer Trialists’ Collaborative Group (EBCTCG): Comparisons between different polychemotherapy regimens for early breast cancer: Meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet 379: 432-444, 2012.
3. Videira M, Reis RL and Brito MA: Deconstructing breast cancer cell biology and the mechanisms of multidrug resistance. Biochim Biophys Acta 1846: 312-325, 2014.
4. Kontos CK, Christodoulou MI and Scorilas A: Apoptosis-related BCL2-family members: Key players in chemotherapy. Anticancer Agents Med Chem 14: 353-374, 2014.
5. Maines MD: The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37: 517-554, 1997.
6. Tenhunen R, Marver HS and Schmid R: The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61: 748-755, 1968.
7. Alam J, Shibahara S and Smith A: Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J Biol Chem 264: 6371-6375, 1989.
8. Doi K, Akaike T, Fujii S, Tanaka S, Ikebe N, Beppu T, Shibahara S, Ogawa M and Maeda H: Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer 80: 1945-1954, 1999.
9. Maines MD and Abrahamsson PA: Expression of heme oxygenase-1 (HSP32) in human prostate: Normal, hyperplastic, and tumor tissue distribution. Urology 47: 727-733, 1996.
10. Torisu-Itakura H, Furue M, Kuwano M and Ono M: Co-expression of thymidine phosphorylase and heme oxygenase-1 in macrophages in human malignant vertical growth melanomas. Jpn J Cancer Res 91: 906-910, 2000.
11. Hara E, Takahashi K, Tominaga T, Kumabe T, Kayama T, Suzuki H, Fujita H, Yoshimoto T, Shirato K and Shibahara S: Expression of heme oxygenase and inducible nitric oxide synthase mRNA in human brain tumors. Biochem Biophys Res Commun 224: 153-158, 1996.
12. Sunamura M, Duda DG, Ghattas MH, Lozonschi L, Motoi F, Yamauchi J, Matsuno S, Shibahara S and Abraham NG: Heme oxygenase-1 accelerates tumor angiogenesis of human pancreatic cancer. Angiogenesis 6: 15-24, 2003.
13. Cherrington JM, Strawn LM and Shawver LK: New paradigms for the treatment of cancer: The role of anti-angiogenesis agents. Adv Cancer Res 79: 1-38, 2000.
14. Was H, Cichon T, Smolarczyk R, Rudnicka D, Stopa M, Chevalier C, Leger JJ, Lackowska B, Grochot A, Bojkowska K, et al: Overexpression of heme oxygenase-1 in murine melanoma: Increased proliferation and viability of tumor cells, decreased survival of mice. Am J Pathol 169: 2181-2198, 2006.
15. Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Künzli B, Autschbach F, Meuer S, Büchler MW and Friess H: Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res 11: 3790-3798, 2005.
16. Noh SJ, Bae JS, Jamiyandorj U, Park HS, Kwon KS, Jung SH, Youn HJ, Lee H, Park BH, Chung MJ, et al: Expression of nerve growth factor and heme oxygenase-1 predict poor survival of breast carcinoma patients. BMC Cancer 13: 516, 2013.
17. Busserolles J, Megías J, Terencio MC and Alcaraz MJ: Heme oxygenase-1 inhibits apoptosis in Caco-2 cells via activation of Akt pathway. Int J Biochem Cell Biol 38: 1510-1517, 2006.
18. Chen GG, Liu ZM, Vlantis AC, Tse GM, Leung BC and van Hasselt CA: Heme oxygenase-1 protects against apoptosis induced by tumor necrosis factor-alpha and cycloheximide in papillary thyroid carcinoma cells. J Cell Biochem 92: 1246-1256, 2004.
19. Bolisetty S, Traylor AM, Kim J, Joseph R, Ricart K, Landar A and Agarwal A: Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 21: 1702-1712, 2010.
20. Banerjee P, Basu A, Wegiel B, Otterbein LE, Mizumura K, Gasser M, Waaga-Gasser AM, Choi AM and Pal S: Heme oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis-and autophagy-regulating molecules. J Biol Chem 287: 32113-32123, 2012.
21. Eisenberg-Lerner A, Bialik S, Simon HU and Kimchi A: Life and death partners: Apoptosis, autophagy and the cross-talk between them. Cell Death Differ 16: 966-975, 2009.
22. Shen HM and Codogno P: Autophagic cell death: Loch Ness monster or endangered species? Autophagy 7: 457-465, 2011.
23. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
24. Mayerhofer M, Florian S, Krauth MT, Aichberger KJ, Bilban M, Marculescu R, Printz D, Fritsch G, Wagner O, Selzer E, et al: Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res 64: 3148-3154, 2004.
25. Nuhn P, Künzli BM, Hennig R, Mitkus T, Ramanauskas T, Nobiling R, Meuer SC, Friess H and Berberat PO: Heme oxygenase-1 and its metabolites affect pancreatic tumor growth in vivo. Mol Cancer 8: 37, 2009.
26. Al-Owais MM, Scragg JL, Dallas ML, Boycott HE, Warburton P, Chakrabarty A, Boyle JP and Peers C: Carbon monoxide mediates the anti-apoptotic effects of heme oxygenase-1 in medulloblastoma DAOY cells via K+ channel inhibition. J Biol Chem 287: 24754-24764, 2012.
27. Jäger R, Herzer U, Schenkel J and Weiher H: Overexpression of Bcl-2 inhibits alveolar cell apoptosis during involution and accelerates c-myc-induced tumorigenesis of the mammary gland in transgenic mice. Oncogene 15: 1787-1795, 1997.
28. Boise LH, González-García M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nuñez G and Thompson CB: Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74: 597-608, 1993.
29. Samaddar JS, Gaddy VT, Duplantier J, Thandavan SP, Shah M, Smith MJ, Browning D, Rawson J, Smith SB, Barrett JT, et al: A role for macroautophagy in protection against 4-hydroxytamoxifen-induced cell death and the development of antiestrogen resistance. Mol Cancer Ther 7: 2977-2987, 2008.
30. Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Corominas-Faja B, Cuyàs E, López-Bonet E, Martin-Castillo B, Joven J and Menendez JA: The anti-malarial chloroquine overcomes primary resistance and restores sensitivity to trastuzumab in HER2-positive breast cancer. Sci Rep 3: 2469, 2013.
31. Sun WL, Chen J, Wang YP and Zheng H: Autophagy protects breast cancer cells from epirubicin-induced apoptosis and facilitates epirubicin-resistance development. Autophagy 7: 1035-1044, 2011.
32. Veldhoen RA, Banman SL, Hemmerling DR, Odsen R, Simmen T, Simmonds AJ, Underhill DA and Goping IS: The chemotherapeutic agent paclitaxel inhibits autophagy through two distinct mechanisms that regulate apoptosis. Oncogene 32: 736-746, 2013.
33. Denton D, Nicolson S and Kumar S: Cell death by autophagy: Facts and apparent artefacts. Cell Death Differ 19: 87-95, 2012.
34. Scarlatti F, Maffei R, Beau I, Codogno P and Ghidoni R: Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ 15: 1318-1329, 2008.
35. Di X, Shiu RP, Newsham IF and Gewirtz DA: Apoptosis, autophagy, accelerated senescence and reactive oxygen in the response of human breast tumor cells to adriamycin. Biochem Pharmacol 77: 1139-1150, 2009.
36. Box VG: The intercalation of DNA double helices with doxorubicin and nogalamycin. J Mol Graph Model 26: 14-19, 2007.
37. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, Roelandt R, De Rycke R, Verspurten J, Declercq W, et al: Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 1: e18, 2010.