Multicarotenoids at Physiological Levels Inhibit Metastasis in Human Hepatocarcinoma SK-Hep-1 Cells

REFERENCES

• El-Serag HB and Mason AC: Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340, 745–750, 1999.
   PubMed Web of Science ®Google Scholar
• Nagao T, Inoue S, Yoshimi F, Sodeyama M, Omori Y, et al.: Postoperative recurrence of hepatocellular carcinoma. Ann Surg 211, 28–33, 1990.
   PubMed Web of Science ®Google Scholar
• Weinstat-Saslow D and Steeg PS: Angiogenesis and colonization in the tumor metastatic process: basic and applied advances. FASEB J 8, 401–407, 1994.
   PubMed Web of Science ®Google Scholar
• Steeg PS: Tumor metastasis: Mechanistic insights and clinical challenges. Nat Med, 12, 895–904, 2006.
   PubMed Web of Science ®Google Scholar
• Olson JA and Krinsky NI: Introduction: The colorful, fascinating world of the carotenoids: Important physiologic modulators. FASEB J 9, 1547–1550, 1995.
   PubMed Web of Science ®Google Scholar
• Nishino H, Murakosh M, Ii T, Takemura M, Kuchide M, et al.: Carotenoids in cancer chemoprevention. Cancer Metastasis Rev 21, 257–264, 2002.
   PubMed Web of Science ®Google Scholar
• Britton G: Structure and properties of carotenoids in relation to function. FASEB J 9, 1551–1558, 1995.
   PubMed Web of Science ®Google Scholar
• Amengual J, Widjaja-Adhi MA, Rodriguez-Santiago S, Hessel S, Golczak M, et al.: Two carotenoid oxygenases contribute to mammalian provitamin A metabolism. J Biol Chem 288, 34081–34096, 2013.
   PubMed Web of Science ®Google Scholar
• Tucker KL, Chen H, Vogel S, Wilson PW, Schaefer EJ, et al.: Carotenoid intakes, assessed by dietary questionnaire, are associated with plasma carotenoid concentrations in an elderly population. J Nutr, 129, 438–445, 1999.
   PubMed Web of Science ®Google Scholar
• Murakoshi M, Nishino H, Satomi Y, Takayasu J, Hasegawa T, et al.: Potent preventive action of alpha-carotene against carcinogenesis: spontaneous liver carcinogenesis and promoting stage of lung and skin carcinogenesis in mice are suppressed more effectively by alpha-carotene than by beta-carotene. Cancer Res, 52, 6583–6587, 1992.
   PubMed Web of Science ®Google Scholar
• Nishino H, Murakoshi M, Tokuda H, and Satomi Y: Cancer prevention by carotenoids. Arch Biochem Biophys 483, 165–168, 2009.
   PubMed Web of Science ®Google Scholar
• Shardell MD, Alley DE, Hicks GE, El-Kamary SS, Miller RR, et al.: Low-serum carotenoid concentrations and carotenoid interactions predict mortality in US adults: the Third National Health and Nutrition Examination Survey. Nutr Res 31, 178–189, 2011.
   PubMed Web of Science ®Google Scholar
• Lin MC, Wang FY, Kuo YH, and Tang FY: Cancer chemopreventive effects of lycopene: Suppression of MMP-7 expression and cell invasion in human colon cancer cells. J Agric Food Chem 59, 11304–11318, 2011.
   PubMed Web of Science ®Google Scholar
• Huang CS, Fan YE, Lin CY, and Hu ML: 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, 2007.
   PubMed Web of Science ®Google Scholar
• Huang CS, Liao JW, and Hu ML: Lycopene inhibits experimental metastasis of human hepatoma SK-Hep-1 cells in athymic nude mice. J Nutr 138, 538–543, 2008.
   PubMed Web of Science ®Google Scholar
• Huang CS, Shih MK, Chuang CH, and Hu ML: Lycopene inhibits cell migration and invasion and upregulates Nm23-H1 in a highly invasive hepatocarcinoma, SK-Hep-1 cells. J Nutr 135, 2119–2123, 2005.
   PubMed Web of Science ®Google Scholar
• Hwang ES and Lee HJ: Inhibitory effects of lycopene on the adhesion, invasion, and migration of SK-Hep1 human hepatoma cells. Exp Biol Med (Maywood) 231, 322–327, 2006.
   PubMed Web of Science ®Google Scholar
• Kozuki Y, Miura Y, and Yagasaki K: Inhibitory effects of carotenoids on the invasion of rat ascites hepatoma cells in culture. Cancer Lett 151, 111–115, 2000.
   PubMed Web of Science ®Google Scholar
• Pradeep CR and Kuttan G: Effect of beta-carotene on the inhibition of lung metastasis in mice. Phytomedicine 10, 159–164, 2003.
   PubMed Web of Science ®Google Scholar
• Chen HY, Yueh TC, Chen YC, Huang CH, Yang CM, et al.: Antimetastatic effects of alpha-carotene and possible mechanisms of action in human hepatocarcinoma SK-Hep-1 cells. J Agric Food Chem 61, 10368–10376, 2013.
   PubMed Web of Science ®Google Scholar
• Lin YJ, Chien YW, Yang SH, and Cheng HH: Fruits and stir-fried vegetables increase plasma carotenoids in young adults. Asia Pac J Clin Nutr 16, 616–623, 2007.
   PubMed Web of Science ®Google Scholar
• Lin CY, Huang CS, and Hu ML: 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, 2007.
   PubMed Web of Science ®Google Scholar
• Repesh LA: A new in vitro assay for quantitating tumor cell invasion. Invasion Metastasis 9, 192–208, 1989.
   PubMedGoogle Scholar
• Ni J and Hollander D: Applications of the MTT assay to functional studies of mouse intestinal intraepithelial lymphocytes. J Clin Lab Anal 10, 42–52, 1996.
   PubMed Web of Science ®Google Scholar
• Kleiner DE and Stetler-Stevenson WG: Quantitative zymography: Detection of picogram quantities of gelatinases. Anal Biochem 218, 325–329, 1994.
   PubMed Web of Science ®Google Scholar
• Stahl W, Junghans A, de Boer B, Driomina ES, Briviba K, et al.: Carotenoid mixtures protect multilamellar liposomes against oxidative damage: Synergistic effects of lycopene and lutein. FEBS Lett 427, 305–308, 1998.
   PubMed Web of Science ®Google Scholar
• Chuang CH and Hu ML: Synergistic DNA damage and lipid peroxidation in cultured human white blood cells exposed to 4-(methyl-nitrosamino)-1-(3-pyridyl)-1-butanone and ultraviolet A. Environ Mol Mutagen 47, 73–81, 2006.
   PubMed Web of Science ®Google Scholar
• Liu RH: Potential synergy of phytochemicals in cancer prevention: Mechanism of action. J Nutr 134, 3479S–3485S, 2004.
   PubMed Web of Science ®Google Scholar
• Nishino H: Cancer prevention by natural carotenoids. J Cell Biochem Suppl 27, 86–91, 1997.
   PubMedGoogle Scholar
• Nishino H, Tokuda H, Murakoshi M, Satomi Y, Masuda M, et al.: Cancer prevention by natural carotenoids. Biofactors 13, 89–94, 2000.
   PubMed Web of Science ®Google Scholar
• Duffy MJ and McCarthy K: Matrix metalloproteinases in cancer: Prognostic markers and targets for therapy (review). Int J Oncol 12, 1343–1348, 1998.
   PubMed Web of Science ®Google Scholar
• Libra M, Scalisi A, Vella N, Clementi S, Sorio R, et al.: Uterine cervical carcinoma: Role of matrix metalloproteinases (review). Int J Oncol 34, 897–903, 2009.
   PubMed Web of Science ®Google Scholar
• Bloomston M, Shafii A, Zervos EE, and Rosemurgy AS: TIMP-1 overexpression in pancreatic cancer attenuates tumor growth, decreases implantation and metastasis, and inhibits angiogenesis. J Surg Res 102, 39–44, 2002.
   PubMed Web of Science ®Google Scholar
• Ramer R, Eichele K, and Hinz B: Upregulation of tissue inhibitor of matrix metalloproteinases-1 confers the anti-invasive action of cisplatin on human cancer cells. Oncogene 26, 5822–5827, 2007.
   PubMed Web of Science ®Google Scholar
• Karlsson R, Pedersen ED, Wang Z, and Brakebusch C: Rho GTPase function in tumorigenesis. Biochim Biophys Acta 1796, 91–98, 2009.
   PubMed Web of Science ®Google Scholar
• Cardinault N, Abalain JH, Sairafi B, Coudray C, Grolier P, et al.: Lycopene but not lutein nor zeaxanthin decreases in serum and lipoproteins in age-related macular degeneration patients. Clin Chim Acta 357, 34–42, 2005.
   PubMed Web of Science ®Google Scholar
• Martin KR, Wu D, and Meydani M: The effect of carotenoids on the expression of cell surface adhesion molecules and binding of monocytes to human aortic endothelial cells. Atherosclerosis 150, 265–274, 2000.
   PubMed Web of Science ®Google Scholar
• Palozza P, Muzzalupo R, Trombino S, Valdannini A, and Picci N: Solubilization and stabilization of beta-carotene in niosomes: delivery to cultured cells. Chem Phys Lipids 139, 32–42, 2006.
   PubMed Web of Science ®Google Scholar
• Reboul E, Abou L, Mikail C, Ghiringhelli O, Andre M, et al.: Lutein transport by Caco-2 TC-7 cells occurs partly by a facilitated process involving the scavenger receptor class B type I (SR-BI). Biochem J 387, 455–461, 2005.
   PubMed Web of Science ®Google Scholar
• White WS, Peck KM, KM, Bierer TL, Gugger Gugger ET, and Erdman JW, Jr: Interactions of oral beta-carotene and canthaxanthin in ferrets. J Nutr 123, 1405–1413, 1993.
   PubMed Web of Science ®Google Scholar
• Tyssandier V, Cardinault N, Caris-Veyrat C, Amiot MJ, Grolier P, et al.: Vegetable-borne lutein, lycopene, and beta-carotene compete for incorporation into chylomicrons, with no adverse effect on the medium-term (3-wk) plasma status of carotenoids in humans. Am J Clin Nutr 75, 526–534, 2002.
   PubMed Web of Science ®Google Scholar
• Bosetti C, Talamini R, Montella M, Negri E, Conti E, et al.: Retinol, carotenoids and the risk of prostate cancer: a case-control study from Italy. Int J Cancer 112, 689–692, 2004.
   PubMed Web of Science ®Google Scholar