Antimetastatic Effects and Mechanisms of Apo-8′-Lycopenal, an Enzymatic Metabolite of Lycopene, Against Human Hepatocarcinoma SK-Hep-1 Cells

REFERENCES

• Fidler , I J . 1978 . Tumor heterogeneity and the biology of cancer invasion and metastasis . Cancer Res , 38 : 2651 – 2660 .
   PubMed Web of Science ®Google Scholar
• Liotta , L A , Rao , C N and Barsky , S H . 1983 . Tumor invasion and the extracellular matrix . Lab Invest , 49 : 636 – 649 .
   PubMed Web of Science ®Google Scholar
• Parmo-Cabanas , M , Molina-Ortiz , I , Matias-Roman , S , Garcia-Bernal , D Carvajal-Vergara , X . 2006 . Role of metalloproteinases MMP-9 and MT1-MMP in CXCL12-promoted myeloma cell invasion across basement membranes . J Pathol , 208 : 108 – 118 .
   PubMed Web of Science ®Google Scholar
• Kleiner , D E and Stetler-Stevenson , W G . 1999 . Matrix metalloproteinases and metastasis . Cancer Chemother Pharmacol , 43 ( Suppl ) : S42 – S51 .
   PubMed Web of Science ®Google Scholar
• Gokaslan , Z L , Chintala , S K , York , J E , Boyapati , V Jasti , S . 1998 . Expression and role of matrix metalloproteinases MMP-2 and MMP-9 in human spinal column tumors . Clin Exp Metastasis , 16 : 721 – 728 .
   PubMed Web of Science ®Google Scholar
• Sakamoto , Y , Mafune , K , Mori , M , Shiraishi , T Imamura , H . 2000 . Overexpression of MMP-9 correlates with growth of small hepatocellular carcinoma . Int J Oncol , 17 : 237 – 243 .
   PubMed Web of Science ®Google Scholar
• Han , X , Zhang , H , Jia , M , Han , G and Jiang , W . 2004 . Expression of TIMP-3 gene by construction of a eukaryotic cell expression vector and its role in reduction of metastasis in a human breast cancer cell line . Cell Mol Immunol , 1 : 308 – 310 .
   PubMed Web of Science ®Google Scholar
• Libra , M , Scalisi , A , Vella , N , Clementi , S Sorio , R . 2009 . Uterine cervical carcinoma: role of matrix metalloproteinases (review) . Int J Oncol , 34 : 897 – 903 .
   PubMed Web of Science ®Google Scholar
• Yam , J W , Tse , E Y and Ng , I O . 2009 . Role and significance of focal adhesion proteins in hepatocellular carcinoma . J Gastroenterol Hepatol , 24 : 520 – 530 .
   PubMed Web of Science ®Google Scholar
• Miyazaki , T , Kato , H , Nakajima , M , Sohda , M Fukai , Y . 2003 . FAK overexpression is correlated with tumour invasiveness and lymph node metastasis in oesophageal squamous cell carcinoma . Br J Cancer , 89 : 140 – 145 .
   PubMed Web of Science ®Google Scholar
• Schlaepfer , D D , Hanks , S K , Hunter , T and van der Geer , P . 1994 . Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase . Nature , 372 : 786 – 791 .
   PubMed Web of Science ®Google Scholar
• Meng , X N , Jin , Y , Yu , Y , Bai , J Liu , G Y . 2009 . Characterisation of fibronectin-mediated FAK signalling pathways in lung cancer cell migration and invasion . Br J Cancer , 101 : 327 – 334 .
   PubMed Web of Science ®Google Scholar
• Mitra , S K , Hanson , D A and Schlaepfer , D D . 2005 . Focal adhesion kinase: in command and control of cell motility . Nat Rev Mol Cell Biol , 6 : 56 – 68 .
   PubMed Web of Science ®Google Scholar
• Hood , J D and Cheresh , D A . 2002 . Role of integrins in cell invasion and migration . Nat Rev Cancer , 2 : 91 – 100 .
   PubMed Web of Science ®Google Scholar
• Nobes , C D and Hall , A . 1995 . Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia . Cell , 81 : 53 – 62 .
   PubMed Web of Science ®Google Scholar
• Vega , F M and Ridley , A J . 2008 . Rho GTPases in cancer cell biology . FEBS Lett , 582 : 2093 – 2101 .
   PubMed Web of Science ®Google Scholar
• Hwang , E S and Lee , H J . 2006 . Inhibitory effects of lycopene on the adhesion, invasion, and migration of SK-Hep1 human hepatoma cells . Exp Biol Med (Maywood) , 231 : 322 – 327 .
   PubMed Web of Science ®Google Scholar
• Huang , C S , Shih , M K , Chuang , C H and Hu , M L . 2005 . Lycopene inhibits cell migration and invasion and upregulates Nm23-H1 in a highly invasive hepatocarcinoma, SK-Hep-1 cells . J Nutr , 135 : 2119 – 2123 .
   PubMed Web of Science ®Google Scholar
• Huang , C S , Liao , J W and Hu , M L . 2008 . Lycopene inhibits experimental metastasis of human hepatoma SK-Hep-1 cells in athymic nude mice . J Nutr , 138 : 538 – 543 .
   PubMed Web of Science ®Google Scholar
• Huang , C S , Fan , Y E , Lin , C Y and Hu , M L . 2007 . Lycopene inhibits matrix metalloproteinase-9 expression and down-regulates the binding activity of nuclear factor-kappa B and stimulatory protein-1 . J Nutr Biochem , 18 : 449 – 456 .
   PubMed Web of Science ®Google Scholar
• Hantz , H L , Young , L F and Martin , K R . 2005 . Physiologically attainable concentrations of lycopene induce mitochondrial apoptosis in LNCaP human prostate cancer cells . Exp Biol Med (Maywood) , 230 : 171 – 179 .
   PubMed Web of Science ®Google Scholar
• Ben-Dor , A , Steiner , M , Gheber , L , Danilenko , M Dubi , N . 2005 . Carotenoids activate the antioxidant response element transcription system . Mol Cancer Ther , 4 : 177 – 186 .
   PubMed Web of Science ®Google Scholar
• Britton , G . 1995 . Structure and properties of carotenoids in relation to function . FASEB J , 9 : 1551 – 1558 .
   PubMed Web of Science ®Google Scholar
• Lian , F and Wang , X D . 2008 . Enzymatic metabolites of lycopene induce Nrf2-mediated expression of phase II detoxifying/antioxidant enzymes in human bronchial epithelial cells . Int J Cancer , 123 : 1262 – 1268 .
   PubMed Web of Science ®Google Scholar
• Gajic , M , Zaripheh , S , Sun , F and Erdman , J W . 2006 . Apo-8′-lycopenal and apo-12′-lycopenal are metabolic products of lycopene in rat liver . J Nutr , 136 : 1552 – 1557 .
   PubMed Web of Science ®Google Scholar
• Kopec , R E , Riedl , K M , Harrison , E H , Curley , R W Hruszkewycz , D P . 2010 . Identification and quantification of apo-lycopenals in fruits, vegetables, and human plasma . J Agric Food Chem , 58 : 3290 – 3296 .
   PubMed Web of Science ®Google Scholar
• Lian , F , Smith , D E , Ernst , H , Russell , R M and Wang , X D . 2007 . Apo-10′-lycopenoic acid inhibits lung cancer cell growth in vitro, and suppresses lung tumorigenesis in the A/J mouse model in vivo . Carcinogenesis , 28 : 1567 – 1574 .
   PubMed Web of Science ®Google Scholar
• Ford , N A , Elsen , A C , Zuniga , K , Lindshield , B L and Erdman , J W . 2011 . Lycopene and apo-12′-lycopenal reduce cell proliferation and alter cell cycle progression in human prostate cancer cells . Nutr Cancer , 63 : 256 – 263 .
   PubMed Web of Science ®Google Scholar
• Lin , C Y , Huang , C S and Hu , M L . 2007 . The use of fetal bovine serum as delivery vehicle to improve the uptake and stability of lycopene in cell culture studies . Br J Nutr , 98 : 226 – 232 .
   PubMed Web of Science ®Google Scholar
• Rundhaug , J E , Pung , A , Read , C M and Bertram , J S . 1988 . Uptake and metabolism of beta-carotene and retinal by C3H/10T1/2 cells . Carcinogenesis , 9 : 1541 – 1545 .
   PubMed Web of Science ®Google Scholar
• Rodriguez , E B and Rodriguez-Amaya , D B . 2009 . Lycopene epoxides and apo-lycopenals formed by chemical reactions and autoxidation in model systems and processed foods . J Food Sci , 74 : C674 – C682 .
   PubMed Web of Science ®Google Scholar
• Williams , A W , Boileau , T W , Clinton , S K and Erdman , J W . 2000 . beta-Carotene stability and uptake by prostate cancer cells are dependent on delivery vehicle . Nutr Cancer , 36 : 185 – 190 .
   PubMed Web of Science ®Google Scholar
• Repesh , L A . 1989 . A new in vitro assay for quantitating tumor cell invasion . Invasion Metastasis , 9 : 192 – 208 .
   PubMedGoogle Scholar
• Kleiner , D E and Stetler-Stevenson , W G . 1994 . Quantitative zymography: detection of picogram quantities of gelatinases . Anal Biochem , 218 : 325 – 329 .
   PubMed Web of Science ®Google Scholar
• Giovannucci , E . 1999 . Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature . J Natl Cancer Inst , 91 : 317 – 331 .
   PubMed Web of Science ®Google Scholar
• Campbell , J K , Canene-Adams , K , Lindshield , B L , Boileau , T W Clinton , S K . 2004 . Tomato phytochemicals and prostate cancer risk . J Nutr , 134 : 3486S – 3492S .
   PubMed Web of Science ®Google Scholar
• Miller , E C , Giovannucci , E , Erdman , J W , Bahnson , R Schwartz , S J . 2002 . Tomato products, lycopene, and prostate cancer risk . Urol Clin North Am , 29 : 83 – 93 .
   PubMed Web of Science ®Google Scholar
• Baker , A H , George , S J , Zaltsman , A B , Murphy , G and Newby , A C . 1999 . Inhibition of invasion and induction of apoptotic cell death of cancer cell lines by overexpression of TIMP-3 . Br J Cancer , 79 : 1347 – 1355 .
   PubMed Web of Science ®Google Scholar
• Bloomston , M , Shafii , A , Zervos , E E and Rosemurgy , A S . 2002 . TIMP-1 overexpression in pancreatic cancer attenuates tumor growth, decreases implantation and metastasis, and inhibits angiogenesis . J Surg Res , 102 : 39 – 44 .
   PubMed Web of Science ®Google Scholar
• Ikenaka , Y , Yoshiji , H , Kuriyama , S , Yoshii , J Noguchi , R . 2003 . Tissue inhibitor of metalloproteinases-1 (TIMP-1) inhibits tumor growth and angiogenesis in the TIMP-1 transgenic mouse model . Int J Cancer , 105 : 340 – 346 .
   PubMed Web of Science ®Google Scholar
• Keely , P J , Westwick , J K , Whitehead , I P , Der , C J and Parise , L V . 1997 . Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K . Nature , 390 : 632 – 636 .
   PubMed Web of Science ®Google Scholar
• Nikolopoulos , S N , Blaikie , P , Yoshioka , T , Guo , W and Giancotti , F G . 2004 . Integrin beta4 signaling promotes tumor angiogenesis . Cancer Cell , 6 : 471 – 483 .
   PubMed Web of Science ®Google Scholar
• Cheng , S , Alfonso-Jaume , M A , Mertens , P R and Lovett , D H . 2002 . Tumour metastasis suppressor, nm23-beta, inhibits gelatinase A transcription by interference with transactivator Y-box protein-1 (YB-1) . Biochem J , 366 : 807 – 816 .
   PubMed Web of Science ®Google Scholar
• Ohba , K , Miyata , Y , Koga , S , Kanda , S and Kanetake , H . 2005 . Expression of nm23-H1 gene product in sarcomatous cancer cells of renal cell carcinoma: correlation with tumor stage and expression of matrix metalloproteinase-2, matrix metalloproteinase-9, sialyl Lewis X, and c-erbB-2 . Urology , 65 : 1029 – 1034 .
   PubMed Web of Science ®Google Scholar
• Murakami , M , Meneses , P I , Lan , K and Robertson , E S . 2008 . The suppressor of metastasis Nm23-H1 interacts with the Cdc42 Rho family member and the pleckstrin homology domain of oncoprotein Dbl-1 to suppress cell migration . Cancer Biol Ther , 7 : 677 – 688 .
   PubMed Web of Science ®Google Scholar
• Leone , A , Flatow , U , King , C R , Sandeen , M A Margulies , I M . 1991 . Reduced tumor incidence, metastatic potential, and cytokine responsiveness of nm23-transfected melanoma cells . Cell , 65 : 25 – 35 .
   PubMed Web of Science ®Google Scholar
• Leone , A , Flatow , U , VanHoutte , K and Steeg , P S . 1993 . Transfection of human nm23-H1 into the human MDA-MB-435 breast carcinoma cell line: effects on tumor metastatic potential, colonization and enzymatic activity . Oncogene , 8 : 2325 – 2333 .
   PubMed Web of Science ®Google Scholar
• Liu , F , Zhang , Y , Zhang , X Y and Chen , H L . 2002 . Transfection of the nm23-H1 gene into human hepatocarcinoma cell line inhibits the expression of sialyl Lewis X, alpha1,3 fucosyltransferase VII, and metastatic potential . J Cancer Res Clin Oncol , 128 : 189 – 196 .
   PubMed Web of Science ®Google Scholar
• Brader , S and Eccles , S A . 2004 . Phosphoinositide 3-kinase signalling pathways in tumor progression, invasion and angiogenesis . Tumori , 90 : 2 – 8 .
   PubMed Web of Science ®Google Scholar
• Sivaraman , V S , Wang , H , Nuovo , G J and Malbon , C C . 1997 . Hyperexpression of mitogen-activated protein kinase in human breast cancer . J Clin Invest , 99 : 1478 – 1483 .
   PubMed Web of Science ®Google Scholar
• Lakka , S S , Jasti , S L , Kyritsis , A P , Yung , W K Ali-Osman , F . 2000 . Regulation of MMP-9 (type IV collagenase) production and invasiveness in gliomas by the extracellular signal-regulated kinase and jun amino-terminal kinase signaling cascades . Clin Exp Metastasis , 18 : 245 – 252 .
   PubMed Web of Science ®Google Scholar
• Scartozzi , M , Bearzi , I , Berardi , R , Mandolesi , A Pierantoni , C . 2007 . Epidermal growth factor receptor (EGFR) downstream signalling pathway in primary colorectal tumours and related metastatic sites: optimising EGFR-targeted treatment options . Br J Cancer , 97 : 92 – 97 .
   PubMed Web of Science ®Google Scholar
• Lee , K H , Hyun , M S and Kim , J R . 2003 . Growth factor-dependent activation of the MAPK pathway in human pancreatic cancer: MEK/ERK and p38 MAP kinase interaction in uPA synthesis . Clin Exp Metastasis , 20 : 499 – 505 .
   PubMed Web of Science ®Google Scholar
• Stahl , W and Sies , H . 1996 . Lycopene: a biologically important carotenoid for humans? . Arch Biochem Biophys , 336 : 1 – 9 .
   PubMed Web of Science ®Google Scholar
• Edwards , A J , Vinyard , B T , Wiley , E R , Brown , E D Collins , J K . 2003 . Consumption of watermelon juice increases plasma concentrations of lycopene and beta-carotene in humans . J Nutr , 133 : 1043 – 1050 .
   PubMed Web of Science ®Google Scholar
• Zaripheh , S and Erdman , J W . 2005 . The biodistribution of a single oral dose of [14C]-lycopene in rats prefed either a control or lycopene-enriched diet . J Nutr , 135 : 2212 – 2218 .
   PubMed Web of Science ®Google Scholar