Carnosol induces ROS-mediated beclin1-independent autophagy and apoptosis in triple negative breast cancer

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Al Dhaheri, Yusra ^a   Attoub, Samir ^a   Ramadan, Gaber ^a   Arafat, Kholoud ^a   Bajbouj, Khuloud ^a,c   Karuvantevida, Noushad ^a   AbuQamar, Synan ^a   Eid, Ali ^b   Iratni, Rabah ^a  

^a UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

^b Department of Pharmacology and Therapeutics Faculty of Medicine and Health Sciences United Arab Emirates University ^*  (Qatar)

^c UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; CARNOSOL; CYCLIN DEPENDENT KINASE INHIBITOR 1; HISTONE H2AX; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P27; REACTIVE OXYGEN METABOLITE; TIRON; ABIETANE DERIVATIVE; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; MAPK1 PROTEIN, HUMAN; MEMBRANE PROTEIN; SCAVENGER;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CHEMOTHERAPY; CANCER INHIBITION; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; ELECTRON MICROSCOPY; ENZYME PHOSPHORYLATION; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; PROTEIN EXPRESSION; TRIPLE NEGATIVE BREAST CANCER; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

1,2-DIHYDROXYBENZENE-3,5-DISULFONIC ACID DISODIUM SALT; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DITERPENES, ABIETANE; DNA DAMAGE; FEMALE; FREE RADICAL SCAVENGERS; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84907775913     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109630     Document Type: Article

References (43)

1. Siegel R, Ma, Zou Z, Jemal A (2014) Cancer statistics, CA Cancer J Clin 64: 9-29.
2. Reis-Filho JS, Tutt AN (2008) Triple negative tumours: a critical review. Histopathology, 52: 108-18.
3. Wang S (2008) The promise of cancer therapeutics targeting the TNF-related apoptosis-inducing ligand and TRAIL receptor pathway. Oncogene 27: 6207-6215.
4. Su M, Mei Y, Sinha S (2013) Role of the Crosstalk between Autophagy and Apoptosis in Cancer, Journal of Oncology 2013: 1-14. http://dx.doi.org/10.1155/2013/102735
5. Martin KR (2006) Targeting apoptosis with dietary bioactive agents. Experimental Biolology and Medicine (Maywood). 231: 117-129.
6. Reed JC (2003) Apoptosis-targeted therapies for cancer. Cancer Cell 3: 17-22.
7. Brown JM, Attardi LD (2005) The role of apoptosis in cancer development and treatment response. Nat Rev Cancer 5: 231-237.
8. Mizushima N, Levine B (2010) Autophagy in mammalian development and differentiation. Nat Cell Biol. 12: 823-30.
9. Abe A, Kokuba H (2013) Harmol induces autophagy and subsequent apoptosis in U251MG human glioma cells through the downregulation of surviving. Oncology Reports 29: 1333-1342.
10. Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Diff 16: 966-75.
11. Rabi T, Bishaye A (2009) Terpenoids and breast cancer chemoprevention. Breast Cancer Research and Treatment. Breast Cancer Res Treat. 115: 223-239.
12. Reuben SC, Gopalan A, Petit DM, Bishayee A (2012) Modulation of angiogenesis by dietary phytoconstituents in the prevention and intervention of breast cancer, Mol. Nutr. Food Res. 56: 14-29.
13. Kaczirek K, Schindl M, Weinhausel A, Scheuba C, Passler C, et al. (2004) Cytotoxic activity of camptothecin and paclitaxel in newly established continuous human medullary thyroiod carcinoma cell lines. J Clin Endocrinol Metabol 89: 2397-240.
14. Johanson JJ, Carnosol (2011) A promising anti-cancer and inflammatory agent. Cancer Letters 305: 1-7.
15. Lopez-Jimenez A, Carcia-Caballero M, Medina MA, Quesada AR (2013) Anti-angiogenic properties of carnosol and carnosic acid, two major dietary compounds from rosmary, Eur J Nutr, 52: 85-95.
16. Johnson JJ, Syed DN, Suth Y, Heren CR, Saleem M, et al. (2011) Disruption of androgen and estrogen receptor activity in prostate cancer by a novel dietary diterpene carnosol: implications for chemoprevention, Cancer Prev. Prev. Res. (Phila) 3: 1112-1123.
17. Johnson JJ, Syed DN, Suth Y, Adhami VM, Mukhtar H (2008) Carnosol, a dietary diterpene displays growth inhibitory effects in human prostate cancer PC3 cells leading to G2-phase cell cycle arrest and targets the 5'-AMP-activated protein kinase (AMPK) pathway. Pharm Res. 25: 2125-2134.
18. Park KW, Kundu J, Chae I-G, Kim DH, Yu MH, et al. (2014) Carnosol induces apoptosis through generation of ROS and inactivation of STAT3 signaling in human colon cancer HCT116 cells. International Journal of Oncology 44: 1309-1315.
19. Dorrie J, Sapala K, Zunino SJ (2001) Carnosol-induced apoptosis and downregulation of Bcl-2 in B-lineage leukemia cells, Cancer Letters 170: 33-39.
20. Al Dhaheri Y, Eid A, AbuQamar S, Attoub S, Khasawneh M, et al. (2013) Mitotic arrest and apoptosis in breast cancer cells induced by Origanum majorana extract: upregulation of TNF-α and downregulation of survivin and mutant p53. PLoS One.8(2): e56649. doi: 10.1371/journal.pone.0056649.
21. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, et al. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-60.
22. Wong CH, Iskandar KB, Yadav SK, Hirpara JL, Loh T, et al. (2010) Simultaneous Induction of Non-Canonical Autophagy and Apoptosis in Cancer Cells by ROS-Dependent ERK and JNK Activation. PLoS ONE 5(4): e9996. doi:10.1371/journal.pone.0009996.
23. Yokoyama T, Miyazawa K, Naito M, Toyotake J, Tauchi T, et al. (2008) Vitamin K2 induces autophagy and apoptosis simultaneously in leukemia cells. Autophagy 4: 629-40.
24. Hsu KF, Wu CL, Huang SC, Wu CM, Hsiao JR, et al. (2009) Cathepsin L mediates resveratrol-induced autophagy and apoptotic cell death in cervical cancer cells. Autophagy 5: 451-60.
25. Karna P, Zughaier S, Pannu V, Simmons R, Narayan S, et al. (2010) Induction of Reactive Oxygen Species-mediated Autophagy by a Novel Microtubule-modulating Agent. J. Biol. Chem. 285: 18737-18748.
26. Shrivastava A, Kuzontkoski PM, Groopman JE, Prasad A (2011) Cannabidiol induces programmed cell death in breast cancer cells by coordinating the crosstalk between apoptosis and autophagy. Mol Cancer Ther. 10: 1161-72.
27. Kaina B (2003) DNA damage-triggered apoptosis: critical role of DNA repair, double-strand breaks, cell proliferation and signaling. Biochem Pharmacol. 66: 1547-54. Review.
28. Matsui Y, Kyoi S, Takagi H, Hsu CP, Hariharan N, et al. (2008) Molecular mechanisms and physiological significance of autophagy during myocardial ischemia and reperfusion. Autophagy 4: 409-415.
29. Zhang L, Hao C, Dong G, Tong Z (2012) Analysis of Clinical Features and Outcome of 356 Triple-Negative Breast Cancer Patients in China. Breast Care (Basel) 7: 13-17.
30. Gluz O, Liedtke C, Gottschalk N, Pusztai L, Nitz U, et al. (2009) Triple-negative breastcancer: Current status and future directions. Ann Oncol 20: 1913-1927.
31. Al Dhaheri Y, Attoub S, Arafat K, AbuQamar S, Eid A, et al. (2013) Salinomycin induces apoptosis and senescence in breast cancer: Upregulation of p21, downregulation of survivin and histone H3 and H4 hyperacetylation. Biochimica et Biophysica Acta 1830: 3121-3135.
32. Knodo Y, Kondo S (2006) Autophagy and cancer therapy. Autophagy 2: 85-90.
33. Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R (2008) Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ. 158: 1318-29.
34. Shrivastava A, Kuzontkoski PM, Groopman JE, Prasad A (2011) Cannabidiol induces programmed cell death in breast cancer cells by coordinating the crosstalk between apoptosis and autophagy. Mol Cancer Ther. 10: 1161-72.
35. Karna P, Zughaier S, Pannu V, Simmons R, Narayan S, et al. (2010) Induction of reactive oxygen species-mediated autophagy by a novel microtubule-modulating agent. J Biol Chem. 285: 18737-48.
36. Li X, Li X, Wang J, Ye Z, Li JC (2012) Oridonin up-regulates expression of P21 and induces autophagy and apoptosis in human prostate cancer cells. Int J Biol Sci. 8: 901-12.
37. Yue Z, Yang C, Levine AJ, Heintz N (2003) Beclin1, an autophagic gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 100: 15077-15082.
38. Ling LU, Tan KB, Lin H, Chiu GN (2011) The role of reactive oxygen species and autophagy in safingol-induced cell death. Cell Death Dis. 2: e129. doi: 10.1038/cddis.2011.12.
39. Dewaele M, Maes H, Agostinis P (2010) ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Autophagy. 67: 838-54
40. Rikiishi H (2012) Novel insights into the interplay between apoptosis and autophagy. International Journal of Cell Biology, 2012: 1-14. http://dx.doi.org/10.1155/2012/317645].
41. Robert G, Ben Sahra I, Puissant A, Colosetti P, Belhacene N, et al. (2009) Acadesine Kills Chronic Myelogenous Leukemia (CML) Cells through PKC-Dependent Induction of Autophagic Cell Death. PLoS ONE 4(11): e7889. doi:10.1371/journal.pone.0007889.
42. Puissant A, Robert G, Fenouille N, Luciano F, Cassuto JP, et al. (2010) Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Cancer Res. 70(3): 1042-52. doi: 10.1158/0008-5472.CAN-09-3537. Epub 2010 Jan 26.
43. Puissant A, Nina Fenouille N, and Auberger P (2012) When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res. 2(4): 397-413. Published online Jun 28, 2012.