The Attenuation of Early Benzo(a)Pyrene-Induced Carcinogenic Insults by Diallyl Disulfide (DADS) in MCF-10A Cells

REFERENCES

• Block , E . 1985 . The chemistry of garlic and onions . Sci Am , 252 : 94 – 99 .
   Web of Science ®Google Scholar
• Minami , T , Boku , T , Inada , K , Morita , M and Okazaki , Y . 1989 . Odor components of human breath after the ingestion of grated raw garlic . J Food Sci , 54 : 763 – 765 .
   Web of Science ®Google Scholar
• Corzo-Martinez , M , Corzo , N and Villamiel , M . 2007 . Biological properties of onions and garlic . Trends in Food Sci Technol , 18 : 609 – 625 .
   Web of Science ®Google Scholar
• Iciek , M , Kwiecien , I and Wlodek , L . 2009 . Biological properties of garlic and garlic-derived organosulfur compounds . Environ Mol Mutagen , 50 : 247 – 265 .
   PubMed Web of Science ®Google Scholar
• Tansey , M R and Appleton , J A . 1975 . Inhibition of fungal growth by garlic extract . Mycologia , 67 : 409 – 413 .
   PubMed Web of Science ®Google Scholar
• You , W C , Zhang , L , Gail , M H , Ma , J L Chang , Y S . 1998 . Helicobater pylori infection, garlic intake and precancerous lesions in a Chinese population at low risk of gastric cancer . Int J Epidemiol , 27 : 941 – 944 .
   PubMed Web of Science ®Google Scholar
• Weber , N D , Anderson , D O , North , J A , Murray , B K Lawson , L D . 1992 . In vitro virucidal activity of Allium sativum (garlic) extract and compounds . Planta Med , 58 : 417 – 423 .
   PubMed Web of Science ®Google Scholar
• Chung , L Y . 2006 . The antioxidant properties of garlic compound: allyl cysteine, alliin, allicin, and allyl disulfide . J Med Food , 9 : 205 – 213 .
   PubMed Web of Science ®Google Scholar
• Knowles , L M and Milner , J A . 1998 . Depresses p34cdc2 kinase activity and G2/M phase arrest induced by diallyl disulfide in HCT-15 cells . Nutr Cancer , 30 : 169 – 174 .
   PubMed Web of Science ®Google Scholar
• Milner , J A . 2001 . A historic perspective on garlic and cancer . J Nutr , 131 : 1027S – 1031S .
   PubMed Web of Science ®Google Scholar
• Guyonnet , D , Belloir , C , Suschetet , M , Siess , H and Le Bon , A-M . 2001 . Antimutagenic activity of organosulfur compounds from Allium is associated with phase II enzyme induction . Muta Res , 495 : 135 – 145 .
   PubMed Web of Science ®Google Scholar
• Takahashi , S , Hakoi , K , Yada , H , Hirose , M Ito , N . 1992 . Enchancing effects of diallyl sulfide on hepatocarcinogenesis and inhibitory actions of the related diallyl disulfide on colon and renal carcinogenesis in rats . Carcinogenesis , 13 : 1513 – 1518 .
   PubMed Web of Science ®Google Scholar
• Sundaram , S G and Milner , J A . 1996 . Diallyl disulfide suppresses the growth of human colon tumor cell xenografts in athymic nude mice . J Nutr , 126 : 1355 – 1361 .
   PubMed Web of Science ®Google Scholar
• Sundaram , S G and Milner , J A . 1996 . Diallyl disulfide inhibits the proliferation of human tumor cells in culture . Biochim Biophys Acta , 1315 : 15 – 20 .
   PubMed Web of Science ®Google Scholar
• Suzui , N , Sugie , S , Rahman , K M , Ohnishi , M Yoshimi , N . 1997 . Inhibitory effects of diallyl disulfide or aspirin on 2-amino-1-methyl-6-phenylimidazo–[4,5-b]pyridine-induced mammary carcinogenesis in rats . Jpn J Cancer Res , 88 : 705 – 711 .
   PubMedGoogle Scholar
• Dwivedi , C , Rohlfs , S , Jarvis , D and Engineer , F N . 1992 . Chemoprevention of chemically induced skin tumor development by diallyl sulfide and diallyl disulfide . Pharm Res , 9 : 1668 – 1670 .
   PubMed Web of Science ®Google Scholar
• Mori , H , Sugie , S , Rahman , W and Suzui , N . 1999 . Chemoprevention of 2-amino-1-methyl-6-phenylimidazoo[4,5-b]pyridine-induced mammary carcinogenesis in rats . Cancer Lett , 143 : 195 – 198 .
   PubMed Web of Science ®Google Scholar
• Chun , H S , Kim , H J and Choi , E H . 2001 . Modulation of cytochrome P4501-mediated bioactivation of benzo[a]pyrene by volatile allyl sulfides in human hepatoma cells . Biosci Biotechnol Biochem , 65 : 2205 – 2212 .
   PubMed Web of Science ®Google Scholar
• Lin , J G , Chen , G W , Su , C C , Hung , C F Yang , C C . 2002 . Effects of garlic components diallyl sulfide and diallyl disulfide in arylamine N-acetyltransferase activity and 2-aminofluorene-DNA adducts in human promyelocytic leukemia cells . Am J Chin Med , 30 : 315 – 325 .
   PubMed Web of Science ®Google Scholar
• Hong , Y S , Ham , Y A , Choi , J H and Kim , J . 2000 . Effects of allyl sulfur compounds and garlic extract on the expression of Bcl-2, Bax, and p53 in non small cell lung cancer cell lines . Exp Mol Med , 32 : 27 – 34 .
   Web of Science ®Google Scholar
• Filomeni , G , Aquilano , K , Rotilio , G and Ciriolo , M . 2003 . Reactive oxygen species-dependent c-Jun NH2-terminal kinase/c-Jun signaling cascade mediates neuroblastoma cell death induced by diallyl disulfide . Cancer Res , 63 : 5940 – 5949 .
   PubMed Web of Science ®Google Scholar
• Li , G , Qiao , C H , Lin , R I , Pinto , J T Osbourne , M P . 1995 . Antiproliferative effects of garlic constituents on cultured human breast cancer cells . Oncol Rep , 2 : 787 – 791 .
   PubMed Web of Science ®Google Scholar
• Drusene , N , Pagniez , A , Mayeur , C , Thomas , M Cherbuy , C . 2004 . Diallyl disulfide (DADS) increases Histone acetylation and p21(waf1/cip1) expression in human colon tumor cell lines . Carcinogenesis , 25 : 1227 – 1236 .
   PubMed Web of Science ®Google Scholar
• Robert , V , Mouille , B , Mayeur , C , Michaud , M and Blachier , F . 2001 . Effects of the garlic compound diallyl disulfide on the metabolism, adherence, and cell cycle of HT-29 colon carcinoma cells: evidence of sensitive and resistant sub-populations . Carcinogenesis , 22 : 1155 – 1161 .
   PubMed Web of Science ®Google Scholar
• Caruso , J A , Reiners , J J , Emond , J , Schultz , T Tainsky , M A . 2001 . Genetic alteration of chromosome 8 is a common feature of human mammary epithelial cell lines transformed in vitro with benzo[a]pyrene . Muta Res , 473 : 85 – 99 .
   PubMed Web of Science ®Google Scholar
• Edwards , N T . 1983 . Polycyclic aromatic hydrocarbons (PAHs) in the environment: a review . J Environ Qual , 12 : 427 – 441 .
   Web of Science ®Google Scholar
• Luttrell , W and Thomas , C . 2007 . Toxic tips: Benzo[a]pyrene . Chem Health and Saf , 14 : 21 – 22 .
   Google Scholar
• International Agency for Research on Cancer: Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures . 2010 . IARC Monogr Eval Carcinog Risks Hum , Vol. 92 , 773 Lyon , , France : World Health Organization, IARC Press .
   Google Scholar
• Lightfoot , T J , Coxhead , J M , Cupid , B C , Nicholson , S and Garner , R C . 2000 . Analysis of DNA adducts by accelerator mass spectrometry in human breast tissue after administration of 2-amino-1-methyl-6-phenylimidazoo[4,5-b]pyridine and benzo[a]pyrene . Muta Res , 472 : 119 – 127 .
   PubMed Web of Science ®Google Scholar
• Hanelt , S , Helbig , R , Hartmann , A , Lang , M Seidel , A . 1997. . A comparative investigation of DNA adducts, DNA strand breaks and gene mutations induced by benzo[a]pyrene and (±)-anti-benzo[a]pyrene-7,8-diol 9,10-epoxide in cultured human cells . Muta Res , 390 : 179 – 188 .
   PubMed Web of Science ®Google Scholar
• Promega, Inc: Technical Bulletin . 2005 . CellTiter 96 AQueous One Soultion Cell Proliferation Assay: instructions for Use of Products G3580, G3581, and G3582 2005 , 1 – 2 . Promega , Madison : WI .
   Google Scholar
• Sigma-Aldrich, Inc: Technical Bulletin . 2005 . PeroxiDetect Kit: for the determination of aqueous and lipid hydroperoxides Sigma-Aldrich, St. Louis , MO
   Google Scholar
• Aboyade-Cole , A , Darling-Reed , S , Oriaku , E , McCaskill , M and Thomas , R . 2008 . Diallyl sulfide inhibits PhiP-induced cell death via the inhibition of DNA strand breaks in normal breast epithelial cells . Oncol Rep , 20 : 319 – 323 .
   PubMed Web of Science ®Google Scholar
• Srivastava , S K , Hu , X , Xia , H , Zaren , H A Chatterjee , M L . 1997 . Mechanism of differential efficacy of garlic organosulfides in preventing benzo(a)pyrene-induced cancer in mice . Cancer Lett , 118 : 61 – 67 .
   PubMed Web of Science ®Google Scholar
• Guyonnet , D , Belloir , C , Suschetet , M , Siess , M H and Le Bon , A-M . 2000 . Liver subcellular fraction from rats treated by organosulfur compounds from allium modulate mutagen activation . Muta Res , 466 : 17 – 26 .
   PubMed Web of Science ®Google Scholar
• Belloir , C , Singh , V , Daurat , C , Siess , M H and Le Bon , A M . 2006 . Protective effects of garlic sulfur compounds against DNA damage induced by direct- and indirect-acting genotoxic agents in HepG2 cells . Food Chem Toxicol , 44 : 827 – 834 .
   PubMed Web of Science ®Google Scholar
• Patri , M , Padmini , A and Babu , P P . 2009 . Polycyclic aromatic hydrocarbons in air and their neurotoxic potency in association with oxidative stress: A brief perspective . Annals of Neurosciences , 16 doi: 10.521/ans.0972.7531.2009.160109
   Google Scholar
• Sagredo , C , Ovrebo , S , Haugen , A , Fujii-Kuriyama , Y Baera , R . 2006 . Quantitative anlysis of benzo[a]pyrene biotransformation and adduct formation in Ahr knockout mice . Toxicol Lett , 167 : 173 – 182 .
   PubMed Web of Science ®Google Scholar
• Perlow , R A , Kolbanovskii , A , Hingerty , B E , Geacintov , N E Broyde , S . 2002 . DNA adducts from a tumorigenic metabolite of benzo[a]pyrene block human RNA polymerase II elongation in a sequence- and stereochemistry-dependent manner . J Mol Biol , 321 : 29 – 47 .
   PubMed Web of Science ®Google Scholar
• Kim , H S , Kwack , S J and Lee , B M . 2000 . Lipid peroxidation, antioxidant enzymes and benzo[a]pyrene-quinones in the blood of rats treated with benzo[a]pyrene . Chem Biol Interact , 127 : 139 – 150 .
   PubMed Web of Science ®Google Scholar
• Spink , D C , Wu , S J , Spink , B C , Hussain , M M Vakharia , D D . 2008 . Induction of CYP1A1 and CYP1B1 by benzo(k)fluoranthene and benzo(a)pyrene in T-47D human breast cancer cells: Roles of PAH interactions and PAH metabolites . Toxicol Appl Pharmacol , 226 : 213 – 224 .
   PubMed Web of Science ®Google Scholar
• Stampfer , M R and Bartley , J C . 1988 . “ Human mammary epithelial cells in culture: differentiation and transformation ” . In Breast Cancer: Cellular and Molecular Biology , Edited by: Dickson , R. and Lippman , M. 1 – 24 . Boston : Kluwer Academic Publishers .
   Google Scholar
• Leadon , S A , Stampfer , M R and Bartley , J . 1988 . Production of oxidative DNA damage during the metabolic activiation of benzo[a]pyrene in human mammary epithelial cells correlates with cell killing . Proc Natl Acad Sci U S A, Cell Biol , 85 : 4365 – 4368 .
   PubMed Web of Science ®Google Scholar
• Keshava , C , Whipkey , D and Weston , A . 2005 . Transcriptional signatures of environmentally relevant exposures in normal human mammary epithelial cells: benzo[a]pyrene . Cancer Lett , 221 : 201 – 211 .
   PubMed Web of Science ®Google Scholar
• Sigounas , G , Hairr , J W , Cooke , C D , Owen , J R Asch , A S . 2010 . Role of benzoo[a]pyrene in generation of clustered DNA damage in human breast tissue . Free Radic Biol Med , 49 : 77 – 87 .
   PubMed Web of Science ®Google Scholar
• Tampio , M , Markkanen , P , Puttonen , K A , Hagelberg , E Heikkinen , H . 2009 . Induction of PUMA-α and down-regulation of PUMA-β expression is associated with benzo(a)pyrene-induced apoptosis in MCF-7 cells . Toxicol Lett , 188 : 214 – 222 .
   PubMed Web of Science ®Google Scholar
• Sadikovic , B and Rodenhiser , D I . 2006 . Benzopyrene exposure disrupts DNA methylation and growth dynamics in breast cancer cells . Toxicol Appl Pharmacol , 216 : 458 – 468 .
   PubMed Web of Science ®Google Scholar
• Siriwardhana , N and Wang , H-C R . 2008 . Precancerous carcinogenesis of human breast epithelial cells by chronic exposure to benzo[a]pyrene . Mol Carcinog , 47 : 338 – 348 .
   PubMed Web of Science ®Google Scholar
• Tannheimer , S L , Lauer , F T , Lane , J and Burchiel , S W . 1999 . Factors influencing elevation of intracellular Ca2+ in the MCF-10A human mammary epithelial cell line by carcinogenic polycyclic aromatic hydrocarbons . Mol Carcinog , 25 : 48 – 54 .
   PubMed Web of Science ®Google Scholar
• Sheen , L-Y , Wu , C-C , Li , C-K and Tsai , S-J . 2001 . Effect of diallyl sulfide and diallyl disulfide, the active principles of garlic, on the aflatoxin B1-induced DNA damage in primary rat hepatocytes . Toxicol Lett , 122 : 45 – 52 .
   PubMed Web of Science ®Google Scholar
• Kim , J-G , Koh , S-H , Lee , Y J , Lee , K-Y Kim , Y . 2005 . Differential effects of diallyl disulfide on neuronal cells depend on its concentration . Toxicology , 211 : 86 – 96 .
   PubMed Web of Science ®Google Scholar
• Hartwell , L H and Weinert , T A . 1989 . Checkpoints: controls that ensure the order of cell cycle events . Science , 246 : 629 – 634 .
   PubMed Web of Science ®Google Scholar
• Vanparys , C , Maras , M , Lenjou , M , Robbens , J Van Bockstaele , D . 2006 . Flow cytometric cell cycle analysis allows for rapid screening of estrogenicity in MCF-7 breast cancer cells . Toxicol In Vitro , 20 : 1238 – 1248 .
   PubMed Web of Science ®Google Scholar
• Bi , X , Slater , D M , Ohmori , H and Vaziri , C . 2005 . DNA polymerase K is specifically required for the recovery from benzo[a]pyrene-dihydrodiol epoxide (BPDE)-induced S-phase checkpoint . J Biol Chem , 280 : 22343 – 22355 .
   PubMed Web of Science ®Google Scholar
• Xiao , D , Pinto , J T , Gundersen , G G and Weinstein , I B . 2005 . Effects of a series of organosulfur compounds on mitotic arrest and induction of apoptosis in colon cancer cells . Mol Cancer Ther , 4 : 1388 – 1398 .
   PubMed Web of Science ®Google Scholar
• Yuan , J P , Wang , G H , Ling , H , Su , Q Yang , Y H . 2004 . Diallyl disulfide-induced G2/M arrest of human gastric cancer MGC803 cells involves activation of p38 MAP kinase-pathways . World J Gastroenterol , 10 : 2731 – 2734 .
   PubMed Web of Science ®Google Scholar
• Gunadharini , D N , Arunkumar , A , Krishnamoorthy , G , Muthuvel , R Vijaybabu . 2006 . Antiproliferative effect of diallyl disulfide (DADS) on prostate cancer cell line LNCaP . Cell Biochem Funct , 24 : 407 – 412 .
   PubMed Web of Science ®Google Scholar
• Arunkumar , A , Vijayababu , M R , Srinivasan , N , Aruldhas , M M and Arunakaran , J . 2006 . Garlic compound, diallyl disulfide induces cell cycle arrest in prostate cancer cell line PC-3 . Mol Cell Biochem , 288 : 107 – 113 .
   PubMed Web of Science ®Google Scholar
• Knowles , L M and Milner , J A . 2000 . Diallyl disulfide inhibits p34cdc2 kinase activity through changes in complex formation and phosphorylation . Carcinogenesis , 21 : 1129 – 1134 .
   PubMed Web of Science ®Google Scholar
• Yang , J-S , Chen , G-W , Hsia , T-C , HO , H-C Ho , C-C . 2009 . Diallyl disulfide induces apoptosis in human colon cancer cell line (COLO 205) through induction of reactive oxygen species, endoplasmic reticulum stress, caspases casade and mitochondrial-dependent pathways . Food Chem Toxicol , 47 : 171 – 179 .
   PubMed Web of Science ®Google Scholar
• Wu , C C , Chung , J G , Tsai , S Y , Yang , J H and Sheen , L Y . 2004 . Differential affects of allyl sulfides from garlic essential oil on cell cycle regulation in human liver tumor cells . Food Chem Toxicol , 42 : 1937 – 1947 .
   PubMed Web of Science ®Google Scholar
• Munday , R , Munday , J S and Munday , C M . 2003 . Comparative effects of mono-, di-, tri-, and tetrasulfides derived from plants of the Allium family: Redox cycling in vitro and hemolytic activity and phase 2 enzyme induction in vivo . Free Radical Biol Med , 34 : 1200 – 1211 .
   PubMed Web of Science ®Google Scholar
• Kwon , K B , Yoo , S J , Ryu , D G , Yang , J Y Rho , H W . 2002 . Induction of apoptosis by diallyl disulfide through activation of caspase-3 in human leukemia HL-60 cells . Biochem Pharmacol , 63 : 41 – 47 .
   PubMed Web of Science ®Google Scholar
• Nagaraj , N S , Anilakumar , K R and Singh , O V . 2010 . Diallyl sulfide causes caspase-dependent apoptosis in human cancer cells through a Bax-triggered mitochondrial pathway . J Nutr Biochem , 21 : 405 – 412 .
   PubMed Web of Science ®Google Scholar
• Sallmyr , A , Fan , J and Rassool , F V . 2008 . Genomic instability in myeloid malignancies: Increased reactive oxygen species (ROS), DNA double strand breaks (DSBs), and error-prone repair . Cancer Lett , 270 : 1 – 9 .
   PubMed Web of Science ®Google Scholar
• Blasiak , J , Arabski , M , Krupa , R , Wozniak , K Rykala , J . 2004 . Basal, oxidative, and alkylative DNA damage, DNA repair efficacy and mutagen sensitivity in breast cancer . Muta Res , 554 : 139 – 148 .
   PubMed Web of Science ®Google Scholar
• Smith , T R , Miller , M S , Lohman , K K , Case , L D and Hu , J L . 2003 . DNA damage and breast cancer risk . Carcinogenesis , 24 : 883 – 889 .
   PubMed Web of Science ®Google Scholar
• Wasson , G R , McKelvey-Martin , V J and Downes , C S . 2008 . The use of the comet assay in the study of human nutrition and cancer . Mutagenesis , 23 : 153 – 162 .
   PubMed Web of Science ®Google Scholar
• Garcia , A , Haza , A I , Arranz , N , Delgado , M E Rafter , J . 2008 . Organosulfur compounds alone or in combination with vitamin C protect towards N-nitrosopiperidine and N-nitrosodibutylamine-induced oxidative DNA damage in HepG2 cells . Chem Biol Interact , 173 : 9 – 18 .
   PubMed Web of Science ®Google Scholar
• Arranz , N , Haza , A I , Garcia , A , Moller , L Rafter , J . 2007 . Protective effects of organosulfur compounds towards N-nitrosamine-induced DNA damage in the single-cell gel electrophoresis (SCGE)/HepG2 assay . Food Chem Toxicol , 45 : 1662 – 1669 .
   PubMed Web of Science ®Google Scholar