Thymoquinone, A Bioactive Component of Black Caraway Seeds, Causes G1 Phase Cell Cycle Arrest and Apoptosis in Triple-Negative Breast Cancer Cells with Mutant p53

REFERENCES

• Amir , E , Freedman , O C , Seruga , B and Evans , D G . 2010 . Assessing women at high risk of breast cancer: a review of risk assessment models . J Natl Cancer Inst , 102 : 680 – 691 .
   PubMed Web of Science ®Google Scholar
• Koboldt , D C , Fulton , R S , McLellan , M D , Schmidt , H Kalicki-Veizer , J . 2012 . Comprehensive molecular portraits of human breast tumours . Nature , 490 : 61 – 70 .
   PubMed Web of Science ®Google Scholar
• Foulkes , W D , Smith , I E and Reis-Filho , J S . 2010 . Triple-negative breast cancer . N Engl J Med , 363 : 1938 – 1948 .
   PubMed Web of Science ®Google Scholar
• Aggarwal , B B and Shishodia , S . 2006 . Molecular targets of dietary agents for prevention and therapy of cancer . Biochem Pharmacol , 71 : 1397 – 1421 .
   PubMed Web of Science ®Google Scholar
• Kado , K , Forsyth , A , Patel , P R and Schwartz , J A . 2012 . Dietary supplements and natural products in breast cancer trials . Front. Biosci. (Elite Ed.) , 1 : 546 – 567 .
   Google Scholar
• Houghton , P J , Zarka , R , de las Heras , B and Hoult , J R . 1995 . Fixed oil of Nigella sativa and derived thymoquinone inhibit eicosanoid generation in leukocytes and membrane lipid peroxidation . Planta Med , 61 : 33 – 36 .
   PubMed Web of Science ®Google Scholar
• Sayed , M D . 1980 . Traditional medicine in health care . J Ethnopharmacol , 2 : 19 – 22 .
   PubMed Web of Science ®Google Scholar
• Banerjee , S , Padhye , S , Azmi , A , Wang , Z and Philip , P A . 2010 . Review on molecular and therapeutic potential of thymoquinone in cancer . Nutr Cancer , 62 : 938 – 946 .
   PubMed Web of Science ®Google Scholar
• Woo , C C , Kumar , A P , Sethi , G and Tan , K HB . 2012 . Thymoquinone: potential cure for inflammatory disorders and cancer . Biochem Pharmacol , 83 : 443 – 451 .
   PubMed Web of Science ®Google Scholar
• El-Najjar , N , Chatila , M , Moukadem , H , Vuorela , H Ocker , M . 2010 . Reactive oxygen species mediate thymoquinone-induced apoptosis and activate ERK and JNK signaling . Apoptosis , 15 : 183 – 195 .
   PubMed Web of Science ®Google Scholar
• Hussain , A R , Ahmed , M , Ahmed , S , Manogaran , P Platanias , L C . 2011 . Thymoquinone suppresses growth and induces apoptosis via generation of reactive oxygen species in primary effusion lymphoma . Free Radic Biol Med , 50 : 978 – 987 .
   PubMed Web of Science ®Google Scholar
• Li , F , Rajendran , P and Sethi , G . 2010 . Thymoquinone inhibits proliferation, induces apoptosis and chemosensitizes human multiple myeloma cells through suppression of signal transducer and activator of transcription 3 activation pathway . Br J Pharmacol , 161 : 541 – 554 .
   PubMed Web of Science ®Google Scholar
• Badr , G , Mohany , M and Abu-Tarboush , F . 2011 . Thymoquinone decreases F-actin polymerization and the proliferation of human multiple myeloma cells by suppressing STAT3 phosphorylation and Bcl2/Bcl-XL expression . Lipids Health Dis , 10 : 236
   PubMed Web of Science ®Google Scholar
• Paramasivam , A , Sambantham , S , Shabnam , J , Raghunandhakumar , S Anandan , R . 2012 . Anti-cancer effects of thymoquinone in mouse neuroblastoma (Neuro-2a) cells through caspase-3 activation with down-regulation of XIAP . Toxicol Lett , 213 : 151 – 159 .
   PubMed Web of Science ®Google Scholar
• Yi , T , Cho , S-G , Yi , Z , Pang , X Rodriguez , M . 2008 . Thymoquinone inhibits tumor angiogenesis and tumor growth through suppressing AKT and extracellular signal-related kinase signaling pathways . Mol Cancer Res , 7 : 1789 – 1796 .
   Google Scholar
• Kolli-Bouhafs , K , Boukhari , A , Abusnina , A , Velot , E Gies , J P . 2012 . Thymoquinone reduces migration and invasion of human glioblastoma cells associated with FAK, MMP-2 and MMP-9 down-regulation . Invest New Drugs , 30 : 2121 – 2131 .
   PubMed Web of Science ®Google Scholar
• Woo , C C , Loo , S Y , Gee , V , Yap , C W Sethi , G . 2011 . Anticancer activity of thymoquinone in breast cancer cells: possible involvement of PPAR-γ pathway . Biochem Pharmacol , 82 : 464 – 475 .
   PubMed Web of Science ®Google Scholar
• Arafa , El-SA , Zhu , Q , Shah , Z , Wani , G Barakat , B M . 2011 . Thymoquinone up-regulates PTEN expression and induces apoptosis in doxorubicin-resistant human breast cancer cells . Mutat Res , 706 : 28 – 35 .
   PubMed Web of Science ®Google Scholar
• Velho-Pereira , R , Kumar , A , Pandey , B N , Jagtap , A G and Mishra , K P . 2011 . Radiosensitization in human breast carcinoma cells by thymoquinone: role of cell cycle and apoptosis . Cell Biol Int , 35 : 1025 – 1029 .
   PubMed Web of Science ®Google Scholar
• Sutton , K M , Doucette , C D and Hoskin , D W . 2012 . NADPH quinone oxidoreductase 1 mediates breast cancer cell resistance to thymoquinone-induced apoptosis . Biochem Biophys Res Commun , 426 : 421 – 426 .
   PubMed Web of Science ®Google Scholar
• Huovinen , M , Loikkanen , J , Myllynen , P and Vähäkangas , K H . 2011 . Characterization of human breast cancer cell lines for the studies on p53 in chemical carcinogenesis . Toxicol In Vitro , 25 : 1007 – 1017 .
   PubMed Web of Science ®Google Scholar
• Jänicke , R U , Sprengart , M L , Wati , M R and Porter , A G . 1998 . Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis . J Biol Chem , 273 : 9357 – 9360 .
   PubMed Web of Science ®Google Scholar
• Fischer , U , Jänicke , R U and Schulze-Osthoff , K . 2003 . Many cuts to ruin: a comprehensive update of caspase substrates . Cell Death Diff , 10 : 76 – 100 .
   PubMed Web of Science ®Google Scholar
• Tounekti , O , Belehradek , J Jr and Mir , L M . 1995 . Relationships between DNA fragmentation, chromatin condensation, and changes in flow cytometry profiles detected during apoptosis . Exp Cell Res , 217 : 506 – 516 .
   PubMed Web of Science ®Google Scholar
• Cohen , GM . 1997 . Caspases the executioners of apoptosis . Biochem J , 326 : 1 – 16 .
   PubMed Web of Science ®Google Scholar
• Mah , L-J , El-Osta , A and Karagiannis , T C . 2010 . γH2AX: a sensitive molecular marker of DNA damage and repair . Leukemia , 24 : 679 – 686 .
   PubMed Web of Science ®Google Scholar
• D’Amours , D , Germain , M , Orth , K , Dixit , V M and Poirer , G G . 1998 . Proteolysis of poly(ADP-ribose) polymerase by caspase-3: kinetics of cleavage of mono(ADP-ribosyl)ated and DNA-bound substrates . Radiat Res , 150 : 3 – 10 .
   PubMed Web of Science ®Google Scholar
• Clark , A S , West , K , Streicher , S and Dennis , P A . 2002 . Constitutive and inducible Akt activity promotes resistance to chemotherapy, transtuzumab, or tamoxifen in breast cancer cells . Mol Cancer Ther , 1 : 707 – 717 .
   PubMed Web of Science ®Google Scholar
• Schubert , K M , Scheid , M P and Duronio , V . 2000 . Ceramide inhibits protein kinase B/Akt by promoting dephosphorylation of serine 473 . J Biol Chem , 275 : 13330 – 13335 .
   PubMed Web of Science ®Google Scholar
• Huang , Y , Park , Y C , Rich , R L , Segal , D Myszka , D G . 2001 . Structural basis of caspase inhibition by XIAP: differential roles of the linker versus the BIR domain . Cell , 104 : 781 – 790 .
   PubMed Web of Science ®Google Scholar
• Al-Amri , A M and Bamosa , A O . 2009 . Phase I safety and clinical activity study of thymoquinone in patients with advanced refractory malignant disease . Shiraz E-Med J , 10 : 107 – 111 .
   Google Scholar
• Polyak , K , Waldman , T , He , T C , Kinzler , K W and Vogelstein , B . 1996 . Genetic determinants of p53-induced apoptosis and growth arrest . Genes Dev , 10 : 1945 – 1952 .
   PubMed Web of Science ®Google Scholar
• Roepke , M , Diestel , A , Bajbouj , K , Walluscheck , D Schonfeld , P . 2007 . Lack of p53 augments thymoquinone-induced apoptosis and caspase activation in human osteosarcoma cells . Cancer Biol Ther , 6 : 160 – 169 .
   PubMed Web of Science ®Google Scholar
• Knappskog , S and Lonning , P E . 2012 . p53 and its molecular basis to chemoresistance in breast cancer . Expert Opin Ther Targets , 16 : S23 – S30 . Suppl. 1
   PubMed Web of Science ®Google Scholar
• Gali-Muhtasib , H , Diab-Assaf , M , Boltze , C , Al-Hmaira , J Hartig , R . 2004 . Thymoquinone extracted from black seed triggers apoptotic cell death in human colorectal cancer cells via a p53-dependent mechanism . Int J Oncol , 25 : 857 – 866 .
   PubMed Web of Science ®Google Scholar
• Yang , X , Wang , W , Qin , J J , Wang , M H Sharma , H . 2012 . JKA97, a novel benzylidene analog of harmine, exerts anti-cancer effects by inducing G1 arrest, apoptosis, and p53-independent up-regulation of p21 . PLoS One 7 , : e34303
   PubMed Web of Science ®Google Scholar
• Twiddy , D , Brown , D G , Adrain , C , Jukes , R Martin , S J . 2004 . Pro-apoptotic proteins released from the mitochondria regulate the protein composition and caspase-processing activity of the native Apaf-1/caspase-9 apoptosome complex . J Biol Chem , 279 : 19665 – 19682 .
   PubMed Web of Science ®Google Scholar
• Stennicke , H R , Jürgensmeier , J M , Shin , H , Deveraux , Q Wolf , B B . 1998 . Pro-caspase-3 is a major physiologic target of caspase-8 . J Biol Chem , 273 : 27084 – 27090 .
   PubMed Web of Science ®Google Scholar
• von Haefen , C , Wieder , T , Essmann , F , Schulze-Osthoff , K Dorken , B . 2003 . Paclitaxel-induced apoptosis in BJAB cells proceeds via a death receptor-independent, caspases-3/-8-driven mitochondrial amplification loop . Oncogene , 22 : 2236 – 2247 .
   PubMed Web of Science ®Google Scholar
• Conus , S , Pop , C , Snipas , S J , Salvesen , G S and Simon , H U . 2012 . Cathepsin D primes caspase-8 activation by multiple intra-chain proteolysis . J Biol Chem , 287 : 21142 – 21151 .
   PubMed Web of Science ®Google Scholar
• Fan , T-J , Han , L-H , Cong , R-S and Liang , J . 2005 . Caspase family proteases and apoptosis . Acta Biochim Biophys Sinica , 37 : 719 – 727 .
   PubMed Web of Science ®Google Scholar
• Germain , M , Affar , E B , D’Amours , D , Dixit , V M Salvesen , G S . 1999 . Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7 . J Biol Chem , 274 : 28379 – 28384 .
   PubMed Web of Science ®Google Scholar
• Shimizu , M , Ishii , H , Ogo , N , Unno , Y Matsuno , K . 2010 . S-trityl-L-cysteine derivative induces caspase-independent cell death in K562 human chronic myeloid leukemia cell line . Cancer Lett , 298 : 99 – 106 .
   PubMed Web of Science ®Google Scholar
• Daugas , E , Susin , Z A , Zamzami , N , Ferri , K F Irinopoulou , T . 2000 . Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis . FASEB J , 14 : 729 – 739 .
   PubMed Web of Science ®Google Scholar
• Bayir , H , Fadeel , B , Palladino , M J , Witasp , E Kurnikov , I V . 2006 . Apoptotic interactions of cytochrome c: redox flirting with anionic phospholipids within and outside of mitochondria . Biochim Biophys Acta , 1757 : 648 – 659 .
   PubMed Web of Science ®Google Scholar
• Johnstone , R W , Ruefli , A A and Lowe , S W . 2002 . Apoptosis: a link between cancer genetics and chemotherapy . Cell , 108 : 153 – 164 .
   PubMed Web of Science ®Google Scholar
• Miller , T W , Rexer , B N , Garrrett , J T and Arteaga , C L . 2011 . Mutations in the phosphatidylinositol 3-kinase pathway: role in tumor progression and therapeutic implications in breast cancer . Breast Cancer Res , 13 : 324
   Web of Science ®Google Scholar
• Vestey , S B , Sen , C , Calder , C J , Perks , C M Pignatelli , M . 2005 . Activated Akt expression in breast cancer: correlation with p53, Hdm2 and patient outcome . Eur J Cancer , 41 : 1017 – 1025 .
   PubMed Web of Science ®Google Scholar
• Tang , G , Minemoto , Y , Dibling , B , Purcell , N H Li , Z . 2001 . Inhibition of JNK activation through NF-κB target genes . Nature , 414 : 313 – 317 .
   PubMed Web of Science ®Google Scholar
• Bhat-Nakshatri , P , Sweeney , C J and Nakshatri , H . 2002 . Identification of signal transduction pathways involved in constitutive NF-κB activation in breast cancer cells . Oncogene , 21 : 2066 – 2078 .
   PubMed Web of Science ®Google Scholar
• Banerjee , S , Kaseb , A O , Wang , Z , Kong , D Mohammad , M . 2009 . Antitumor activity of gemcitabine and oxaliplatin is augmented by thymoquinone in pancreatic cancer . Cancer Res , 69 : 5575 – 5583 .
   PubMed Web of Science ®Google Scholar
• Yang , L , Cao , Z , Yan , H and Wood , W C . 2003 . Coexistence of high levels of apoptotic signaling and inhibitor of apoptosis proteins in human tumor cells: implications for cancer specific therapy . Cancer Res , 63 : 6815 – 6824 .
   PubMed Web of Science ®Google Scholar
• Jin , W , Wu , L , Liang , K , Liu , B Lu , Y . 2003 . Roles of the PI-3K and MEK pathways in Ras-mediated chemoresistance in breast cancer cells . Br J Cancer , 89 : 185 – 191 .
   PubMed Web of Science ®Google Scholar
• Crown , J , O’Shaughnessy , J and Gullo , G . 2012 . Emerging targeted therapies in triple-negative breast cancer . Ann Oncol , 23 : vi56 – vi65 .
   PubMed Web of Science ®Google Scholar