Modulation of mRNA expression and activities of xenobiotic metabolizing enzymes, CYP1A1, CYP1A2, CYP2E1, GPx and GSTP1 by the Salicornia freitagii extract in HT-29 human colon cancer cells

Authors

  • Ahmet Altay 1. Erzincan Univesity, Faculty of Science, Department of Chemistry, 24100, Erzincan; 2. Middle East Technical University, Department of Biology, 06800, Ankara
  • Deniz İrtem Kartal 1. Yuzuncu Yıl University, Natural and Applied Sciences, 65080, Van; 2. Middle East Technical University, Department of Biology, 06800, Ankara
  • Gökhan Sadi Karamanoglu Mehmetbey University, Department of Biology, 70100, Karaman
  • Tülin Güray Middle East Technical University, Department of Biology, 06800, Ankara
  • Ahmet Emre Yaprak Ankara University, Department of Biology, 06800, Ankara

Keywords:

glassworts, cytotoxicity, drug metabolism, colon cancer, phase I-II enzymes

Abstract

Phase I-II detoxification and antioxidant enzymes are responsible for the detoxification and elimination of activated carcinogens, acting as important biomarkers for chemoprevention. Among them, cytochrome P450s plays a prominent role in the metabolic activation of xenobiotics. The herb Salicornia freitagii (SF) (Amaranthaceae) is known for its anticancer, antioxidant, antidiabetic and antiinflammatory activities. In this study, we determined the bioactive phenolics in the SF methanol extract and investigated its antiproliferative potential in HT-29 human colon cancer cells. We also investigated the modulation of some phase I and II enzyme (CYP 1A1, 1A2, 2E1, GSTP1 and GPx) mRNA expression and enzymatic activities by the SF extract and its major bioactive phenolic compounds. LC/MS-MS analysis showed that the main phenolic compounds of the methanolic SF extract are vanillic acid (48 µg/100g) and p-coumaric acid (10.8 µg/100g). SF extract, vanillic acid and p-coumaric acid exhibited high antiproliferative activities in HT-29 cells, with IC50 values of 81.79µg/mL, 98.8 µM and 221.6 µM, respectively. The mRNA expression levels of CYP1A2 and CYP2E1 were decreased, while those of GSTP1 and GPx in HT-29 cells were increased after application of either the SF extract or vanillic acid. The SF extract by itself also increased the activities of GPx and GSTP1 enzymes 1.68- and 1.49-fold, respectively. Our data indicate that the SF extract and its major bioactive compound, vanillic acid, could exert a modulatory effect on the expression of enzymes that are involved in xenobiotic activation and detoxification pathways in the gastrointestinal tract. For this reason, SF can be considered as a natural source of chemopreventive agents.

https://doi.org/10.2298/ABS160825118A

Received: August 25, 2016; Revised: October 8, 2016; Accepted: October 13, 2016; Published online: November 3, 2016

How to cite: Altay A, İrtem Kartal D, Sadi G, Güray T, Yaprak AE. Modulation of mRNA expression and activities of xenobiotic metabolizing enzymes, CYP1A1, CYP1A2, CYP2E1, GPx and GSTP1 by the Salicornia freitagii extract in HT-29 human colon cancer cells. Arc Biol Sci. 2017;69(3):439-48.

Downloads

Download data is not yet available.

References

Mudie P, Greer S, Brakel J, Dickson J, Schinkel C, Peterson-Welsh R. Forensic palynology and ethnobotany of Salicornia species (Chenopodiaceae) in northwest Canada and Alaska. Can J Bot. 2005;83(1):111-23.

Chevalier A. Les Salicornes et leur emploi dans l’alimentation: Etude historique, botanique, économique. Rev Bot appliqué d’Agriculture Colon. 1922;2(16):697-785.

Geslin M, Verbist J. Flavonoides de Salicornia europaea. J Nat Prod. 1985;48(1):111-3.

Anwar F, Bhanger M, Nasir M, Ismail S. Analytical characterization of Salicornia bigelovii seed oil cultivated in Pakistan. J Agric Food Chem. 2002;50(15):4210-4.

Lu D, Zhang M, Wang S, Cai J, Zhou X, Zhu C. Nutritional characterization and changes in quality of Salicornia bigelovii Torr. during storage. LWT. Food Sci Technol. 2010;43(3):519-24.

Austenfeld F. Nutrient reserves of Salicornia europaea seeds. Physiol Plant. 1986;68(1):446-50.

Guil J, Torija M, Giménez J, Rodríguez I. Identification of fatty acids in edible wild plants by gas chromatography. J Chromatogr A. 1996;719(3):229-35.

Chung YC, Chun HK, Yang JY, Kim JY, Han EH, Kho YH, Joeng HG. Tungtungmadic acid, a novel antioxidant, from Salicornia herbacea. Arch Pharmacal Res. 2005;28(10):1122-6.

Borkowski B, Drost K. Alkaloide aus Salicornia herbacea L. Pharmazie. 1965;20(38):390-3.

Chiji H, Aiba T, M I. Isolation and identification of two 2,3-unsubstituted chromones from glasswort (Salicornia europaea L.). Agric Biol Chem. 1978;4(1):159-65.

Arakawa Y, Chiji H, Izawa M. Structural elucidation of two new chromones isolated from Glasswort (Salicornia europaea L.). Agric Biol Chem. 1983;47(1):2029-33.

Kong CS, Kim YA, Kim MM, Park JS, Kim JA, Kim SK, Lee BJ, Nam TJ, Seo Y. Flavonoid glycosides isolated from Salicornia herbacea inhibit matrix metalloproteinase in HT1080 cells. Toxicol Vitr. 2008;22(7):1742-8.

Kang S, Kim D, Lee BH, Kim MR, Hong J, Chiang M. Antioxidant properties and cytotoxic effects of fractions from glasswort (Salicornia herbacea) seed extracts on human intestinal cells. Food Sci Biotechnol. 2011;20(1):115-22.

Bang MA, Kim HA, Cho YJ. Hypoglycemic and antioxidant effect of dietary hamcho powder in streptozotocin-induced diabetic rats. J Korean Soc Food Sci Nutr. 2002;31:840-6.

Lee YS, Lee SH, Kim BK, Oguchi K, H SK. Inhibitory effects of isorhamnetin-3-O-β-D-glucoside from Salicornia herbacea on rat lens aldose reductase and sorbitol accumulation in streptozotocin-induced diabetic rat tissues. Biol Pharm Bull. 2005;28(5):916-8.

Rhee M, Park H. Salicornia herbacea: botanical, chemical and pharmacological review of halophyte marsh plant. J Med Plants. 2009;3(8):548-55.

Han SK, Kim SM, Pyo BS. Antioxidative effect of glasswort (Salicornia herbacea L.) on the lipid oxidation of pork. Korean J Food Sci Anim Resour. 2003;23(38):46-9.

Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet Oncol. 2014;383(9):1490-502.

Anand P, Kunnumakara AB, Sundaram C, Kuzhuvelil B, Harikumar KB, Tharakan ST, Lai OS, Sung B, Bharat B, Aggarwal BB. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res. 2008;25(9):9661-9.

Lee SB, Cha KH, Selenge D, Solongo A, Nho CW. The Chemopreventive Effect of Taxifolin Is Exerted through ARE-Dependent Gene Regulation. Bioll. Pharm Bull. 2007;30(6):1074-9.

Guengerich FP, Shimada T. Oxidation of toxic and carcinogenicchemicals by human cytochrome P-450 enzymes. Chem Res Toxicol. 1991;4(4):391-407.

Androutsopoulos V, Tsatsakis A, Spandidos D. Cytochrome P450 CYP1A1: wider roles in cancer progression and prevention. BMC Cancer. 2009;9(187).

Hecht S. Tobacco smoke carcinogens and lung cancer. J Nat Cancer Institue. 1999;91(14):1194-210.

Arinc E, Adali O, Gencler-Ozkan A. Induction of N-nitrosodimethylamine metabolism in liver and lung by in vivo pyridine treatments of rabbits. Arch Toxicol. 2000;74(6):329-34.

Arinc E, Arslan S, Bozcaarmutlu A, Adali O. Effects of diabetes on rabbit kidney and lung CYP2E1 and CYP2B4 expression and drug metabolism and potentiation of carcinogenic activity of N-nitrosodimethylamine in kidney and lung. Food Chem Toxicol Toxicol. 2007;45(1):107-18.

Ding X, Kaminsky LS. Human Extrahepatıc Cytochromes P450: Function in Xenobiotic Metabolism and Tissue-Selective Chemical Toxicity in the Respiratory and Gastrointestinal Tracts. Annu Rev Pharmacol Toxicol. 2002;43(1):149-73.

Bousova I, Skalova L. Inhibition and induction of glutathione S-transferases by flavonoids: possible pharmacological and toxicological consequences. Drug Metab Rev. 2012;44(4):267-86.

Ban N. Transfection of glutathione S-transferase (GST)-π antisense complementary DNA increases the sensitivity of a colon cancer cell line to adriamycin, cisplatin, melphalan, and etoposide. Cancer Res. 1996;56(15):3577-82.

Smith M, Evans C, Doane-Setzer P. Denitrosation of 1, 3-bis (2-chloroethyl)-1-nitrosourea by class mu glutathione transferases and its role in cellular resistance in rat brain tumor cells. Cancer Res. 1989;49(10):2621-5.

Ursini F. Diversity of glutathione peroxidases. Methods Enzym. 1995;252(4):38-53.

Imai H, Narashima K, Arai M. Suppression of leukotriene formation in RBL-2H3 cells that overexpressed phospholipid hydroperoxide glutathione peroxidase. J Biol Chem. 1998;273(4):1990-7.

Haan JB, Bladier C, Griffiths P, Kelner M, Ross D, Cheung NS, Bronson RT, Silvestro MJ, Wield S, Zheng SS, Beart PS, Hertzog PJ, Kola I. Mice with a Homozygous Null Mutation for the Most Abundant Glutathione Peroxidase, Gpx1, Show Increased Susceptibility to the Oxidative Stress-inducing Agents Paraquat and Hydrogen Peroxide. J Biol Chem. 1998;273(35):22528-36.

Freedman JE, Loscalzo J, Benoit SE. Decreased platelet inhibition by nitric oxide in two brothers with a history of arterial thrombosis. J Clin Invest. 1996;97(4):979-87.

Lowry O, Rosebrough NJ, Farr AL, Randall RJ. Protein Measurement with the Folin Phenol Reagent. J Biol Chem. 1951;193(1):265-75.

Habig WH, Pabst MJ, Jakoby WB. Glutathione Stransferase: the first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):7130-39.

Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Lab Clin Med. 1967;70(1):158-69.

Bertin RL, Gonzaga VG, Borges GSC, Azevedo MS, Maltez HF, Heller M. Nutrient composition and, identification/quantification of major phenolic compounds in Sarcocornia ambigua (Amaranthaceae) using HPLC-ESI-MS/MS. Food Res Int. 2014;55(1):404-11.

Choi YM, An S, Lee EM. CYP1A1 is a target of miR-892amediated post-transcriptional repression. Int J Oncol. 2012;41(1):331-36.

Mohri T, Nakajima M, Fukami T. Human CYP2E1 is regulated by miR-378. Biochem Pharmacol. 2010;79(7):1045-52.

McManus ME, Burgess WM, Veronese ME. Metabolism of 2 acetylaminofluorene and benzo (A) pyrene and activation of foodderived heterocyclic amine mutagens by human cytochromes P-450. Cancer Res. 1990;50(11):3367-76.

Miller EC, Miller JA. Mechanisms of chemical carcinogenesis: Nature of proximate carcinogens and interactions with macromolecules. Pharmacol Rev. 1966;18(1):805-38.

Arinç E, Yilmaz D, Bozcaarmutlu A. Mechanism of inhibition of CYP1A1 and glutathione S-transferase activities in fish liver by quercetin, resveratrol, naringenin, hesperidin, and rutin. Nutr Cancer. 2015;67(1):137-44.

Karakurt S, Semiz A, Celik G, Gencler-Ozkan AM, Sen A, Adali O. Epilobium hirsutum alters xenobiotic metabolizing CYP1A1, CYP2E1, NQO1 and GPx activities, mRNA and protein levels in rats. Pharm Biol. 2013;51(5):650-8.

Suganuma M, Okabe S, Kai Y, Sueoka N, Sueoka E, Fujiki H. Synergistic effects of (˗)-epigallocatechin gallate with (˗)-epicatechin, sulindac, or tamoxifen on cancer-preventiveactivity in the human lung cancer cellline PC-9. Cancer Res. 1999;59:(1):44-7.

Kronenberg S, Esser C, Carlberg C. An aryl hydrocarbon receptor conformation acts as the functional core of nuclear dioxin signaling. Nucleic Acids Res. 2000;28(12):2286-91.

Lin J, Lu A. Inhibition and induction of cytochrome P450 and the clinical implications. Clin Pharmacokinet. 1998;35(5):361-90.

Kohn MC, Walker NJ, Kim AH, Portier CJ. Physiological modeling of a proposed mechanism of enzyme induction by TCDD. Toxicology. 2001;162(3): 193-208.

Ciolino H, Daschner P, Yeh G. Dietary flavonols quercetin and kaempferol are ligands of the aryl hydrocarbon receptor that affect CYP1A1 transcription differentially. J Biochem. 1999;340(3):715-22.

Gonzalez FJ. Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat Res. 2005;56(1):101-10.

Karakurt S, Semiz A, Celik G, Gencler-Ozkan A, Sen A, Adali O. Contribution of ellagic acid on the antioxidant potential of medicinal plant Epilobium hirsutum. Nutr Cancer. 2016;68(1):173-83.

Karakurt S, Adali O. Tannic Acid Inhibits Proliferation, Migration, Invasion of Prostate Cancer and Modulates Drug Metabolizing and Antioxidant Enzymes. Anticancer Agents Med Chem. 2016;16(6):781-9.

Na HY, Surh YJ. Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food Chem Toxicol. 2008;46(4):1271-8.

Cheng WH, Ho YS, Valentine BA. Cellular glutathione peroxidase is the mediator of body selenium to protect against paraquat lethality in transgenic mice. J Nutr. 1998;128(7):1070-6.

Battin EE, Brumaghim JL. Antioxidant activity of sulfur and selenium: A review of reactive oxygen species scavenging, glutathione peroxidase, and metal-binding antioxidant mechanisms. Cell Biochem Biophys. 2009;55(1):1-23.

Downloads

Published

2017-08-11

How to Cite

1.
Altay A, İrtem Kartal D, Sadi G, Güray T, Yaprak AE. Modulation of mRNA expression and activities of xenobiotic metabolizing enzymes, CYP1A1, CYP1A2, CYP2E1, GPx and GSTP1 by the Salicornia freitagii extract in HT-29 human colon cancer cells. Arch Biol Sci [Internet]. 2017Aug.11 [cited 2024Mar.28];69(3):439-48. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/934

Issue

Section

Articles

Most read articles by the same author(s)