Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Effects of retinoic acid isomers on apoptosis and enzymatic antioxidant system in human breast cancer cells

  • Published : 2009.06.30
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Abstract

Retinoic acids (RAs) modulate growth, differentiation, and apoptosis in normal, pre-malignant & malignant cells. In the present study, the effects of RA isomers (all-trans RA, 13-cis RA, and 9-cis RA) on the cell signal transduction of human breast cancer cells have been studied. The relationship between RAs and an enzymatic antioxidant system was also determined. Estrogen-receptor (ER) positive MCF-7 and ER-negative MDA-MB-231 human breast cancer cells were treated with different doses of each RA isomers, all-trans RA, 13-cis RA, or 9-cis RA. Treatment of RA isomers inhibited cell viability and induced apoptosis of MCF-7 cells as a result of increased caspase activity in cytoplasm and cytochrome C released from mitochondria. All-trans RA was the most effective RA isomer in both cell growth inhibition and induction of apoptosis in MCF-7 cells. However, no significant effect of RA isomers was observed on the cell growth or apoptosis in ER-negative MDA-MB-231 cells. In addition, activities of antioxidant enzymes such as catalase and glutathione peroxidase were decreased effectively after treatment of RA in MCF-7 cells, whereas SOD activity was rarely affected. Thus, the present data suggest that all-trans RA is the most potential inducer of apoptosis and modulator of antioxidant enzymes among RA isomers in MCF-7 human breast cancer cells.

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References

  1. Ahlemeyer B, Bauerbach E, Plath M, Steuber M, Heers C, Tegtmeier F & Krieglstein J (2001). Retinoic acid reduces apoptosis and oxidative stress by preservation of SOD protein level. Free Radic Biol Med 30:1067-1077 https://doi.org/10.1016/S0891-5849(01)00495-6
  2. Arruda VR, Salles TS, Costa FF & Saad ST (1996). Glutathione peroxidase, reduced glutathione, superoxide dismutase and catalse in red cells of patients with hairy cell leukemia. Neoplasia 43:99-102
  3. Bai J, Rodriguez AM, Melendez JA & Cederbaum AI (1999). Overexpression of catalase in cytosolic or mitochondrial compartment protects HepG2 cells against oxidative injury. J Biol Chem 274:26217-26224 https://doi.org/10.1074/jbc.274.37.26217
  4. Brodowicz T, Wiltschke C, Kandioler-Eckersberger D, Grunt TW, Rudas M, Schneider SM, Hejna M, Budinsky A & Zielinski CC (1999). Inhibition of proliferation and induction of apoptosis in soft tissue sarcoma cells by interferon-alpha and retinoids. Br J Cancer 80:1350-1358 https://doi.org/10.1038/sj.bjc.6690528
  5. Chambon P (1996). A decade of molecular biology of retinoic acid receptors. FASEB J 10:940-954
  6. Conte da Frota ML Jr, Comes da Silva E, Behr GA, Roberto de Oliveira M, Dal Pizzol F, Klamt F & Moreira JC (2006). All trans retinoic acid induces free radical generation and modulate antioxidant enzyme activities in rat sertoli cells. Mol Cell Biochem 285:173-179 https://doi.org/10.1007/s11010-005-9077-3
  7. Dietze EC, Caldwell LE, Marcom K, Collins SJ, Yee L, Swisshelm K, Hobbs KB, Bean GR & Seewaldt VL (2002). Retinoids and retinoic acid receptors regulate growth arrest and apoptosis in human mammary epithelial cells and modulate expression of CBP/p300. Microsc Res Tech 59:23-40 https://doi.org/10.1002/jemt.10174
  8. Dimberg A & Oberg F (2003). Retinoic acid-induced cell cycle arrest of human myeloid cell lines. Leuk Lymphoma 44:1641-1650 https://doi.org/10.1080/1042819031000083316
  9. Drisko JA, Chapman J & Hunter VJ (2003). The use of antioxidant therapies during chemotherapy. Gynecol Oncol 88:434-439 https://doi.org/10.1016/S0090-8258(02)00067-7
  10. Freemantle SJ, Spinella MJ & Dmitrovsky E (2003). Retinoids in cancer therapy and chemoprevention: promise meets resistance. Oncogene 22:7305-7315 https://doi.org/10.1038/sj.onc.1206936
  11. Gallagher RE (2002). Retinoic acid resistance in acute promyelocytic leukemia. Leukemia 16:1940-1958 https://doi.org/10.1038/sj.leu.2402719
  12. Gronemeyer H & Miturski R (2001). Molecular mechanisms of retinoid action. Cell Mol Biol Lett 6:3-52
  13. Hara M, Suzuki S, Mori J, Yamashita K, Kumagai M, Sakuma T, Kakizawa T, Takeda T, Miyamoto T, Ichikawa K & Hashizume K (2000). Thyroid hormone regulation of apoptosis induced by retinoic acid in promyeloleukemic HL-60 cells: studies with retinoic acid receptor-specific and retinoid x receptor-specific ligands. Thyroid 10:1023-1034 https://doi.org/10.1089/thy.2000.10.1023
  14. Hayashi K, Yokozaki H, Naka K, Yasui W, Lotan R & Tahara E (2001). Overexpression of retinoic acid receptor beta induces growth arrest and apoptosis in oral cancer cell lines. Jpn J Cancer Res 92:42-50 https://doi.org/10.1111/j.1349-7006.2001.tb01046.x
  15. Hengartner MO (2000). The biochemistry of apoptosis (review). Nature 407:770-776 https://doi.org/10.1038/35037710
  16. Kuida K (2000). Caspase-9. Int J Biochem Cell Biol 32:121-124 https://doi.org/10.1016/S1357-2725(99)00024-2
  17. Kuypers FA, Lewis RA, Hua M, Schott MA, Discher D, Ernst JD & Lubin BH (1996). Detection of altered membrane phospholipids asymmetry in subpopulations of juman red blood cells using fluorescently labeled annexin V. Blood 87:1179-1187
  18. Manor D, Shmidt EN, Budhu A, Flesken-Nikitin A, Zgola M, Page R, Nikitin AY & Noy N (2003). Mammary carcinoma suppression by cellular retinoic acid binding protein-II. Cancer Res 63:4426-4433
  19. Marill J, Idres N, Capron CC, Nguyen E & Chabot GG (2003). Retinoic acid metabolism and mechanism of action: a review. Curr Drug Metab 4:1-10 https://doi.org/10.2174/1389200033336900
  20. Melino G, Thiele CJ, Knight RA & Piacentini M (1997). Retinoids and the control of growth/death decisions in human neuroblastoma cell lines. J Neurooncol 31:65-83 https://doi.org/10.1023/A:1005733430435
  21. Nagase M, Alam MM, Tsushima A, Yoshizawa T & Sakato N (2001). Apoptosis induction by T-2 toxin: activation of caspase-9, caspase-3 and DFF-40/CAD through cytosolic release of cytochrome C in HL-60 cells. Biosci Biotechnol Biochem 65:1741-1747 https://doi.org/10.1271/bbb.65.1741
  22. Nagpal S & Chandraratna RA (2000). Recent developments in receptor-selective retinoids. Curr Pharm Des 6:919-931 https://doi.org/10.2174/1381612003400146
  23. Napoli JL (1996). Retinoic acid biosynthesis and metabolism. FASEB J 10:993-1001
  24. Nelson AM, Gilliland KL, Cong Z & Thiboutot DM (2006). 13-cis retinoic acid induces apoptosis and cell cycle arrest in human SEB-1 sebocytes. J Invest Dermatol 126:2178-2189 https://doi.org/10.1038/sj.jid.5700289
  25. Nordberg J & Arner ES (2001). Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287-1312 https://doi.org/10.1016/S0891-5849(01)00724-9
  26. Ott DB & Lachance PA (1979). Retinoic acid-a review. Am J Clin Nutr 32:2522-2531
  27. Ott M, Gogvadze V, Orrenius S & Zhivotovsky B (2007). Mitochondria, oxidative stress and cell death. Apoptosis 12:913-922 https://doi.org/10.1007/s10495-007-0756-2
  28. Paik J, Blaner WS, Sommer KM, Moe R & Swisshlem K (2003). Retinoids, retinoic acid receptors, and breast cancer. Cancer Invest 21:304-312 https://doi.org/10.1081/CNV-120016425
  29. Pepper C, Ali K, Thomas A, Hoy T, Fegan C, Chowdary P, Kell J & Bentley P (2002). Retinoid-induced apoptosis in B-cell chronic lymphocytic leukaemia cells is mediated through caspase-3 activation and is independent of p53, the retinoic acid receptor, and differentiation. Eur J Haematol 69:227-235 https://doi.org/10.1034/j.1600-0609.2002.02799.x
  30. Pettersson F, Dalgleish AG, Bissonnette RP & Colston KW (2002). Retinoids cause apoptosis in pancreatic cancer cells via activation of RAR-gamma and altered expression of Bcl-2/Bax. Br J Cancer 87:555-561 https://doi.org/10.1038/sj.bjc.6600496
  31. Pigault C, Follenius-Wund A, Schmutz M, Freyssinet JM & Brisson A (1994). Formation of two-dimensional arrays of annexin V on phosphatidylserine-containing liposomes. J Mol Biol 236:199-208 https://doi.org/10.1006/jmbi.1994.1129
  32. Prakash P, Russell RM & Krinsky NI (2001). In vitro inhibition of proliferation of estrogen-dependent and estrogen independent human breast cancer cells treated with carotenoids or retinoids. J Nutr 131:1574-1580
  33. Ralhan R & Kaur J (2003). Retinoids as chemopreventive agents. J Biol Regul Homeost Agents 17:66-91
  34. Raloff J (2000). Antioxidants may help cancers thrive. Science News 157:5
  35. Rishi AK, Zhang L, Boyanapalli M, Wali A, Mohammad RM, Yu Y, Fontana JA, Hatfield JS, Dawson MI, Majumdar AP & Reichert U (2003). Identification and characterization of a cell cycle and apoptosis regulatory protein-1 as a novel mediator of apoptosis signaling by retinoid CD437. J Biol Chem 278:33422-33435 https://doi.org/10.1074/jbc.M303173200
  36. Sato Y, Meller R, Yang T, Taki W & Simon RP (2008). Stereoselective neuroprotection against stroke with vitamin A derivatives. Brain Res 1241:188-192 https://doi.org/10.1016/j.brainres.2008.09.020
  37. Seewaldt VL, Johnson BS, Parker MB, Collins SJ & Swisshelm K (1995). Expression of retinoic acid receptor beta mediates retinoic acid-induced growth arrest and apoptosis in breast cancer cells. Cell Growth Differ 6:1077-1088
  38. Smith MA, Parkinson DR, Cheson BD & Friedman MA (1992). Retinoids in cancer therapy. J Clin Oncol 10:839-864
  39. Soprano DR, Qin P & Soprano KJ (2004). Retinoic acid receptors and cancers. Annu Rev Nutr 24:201-221 https://doi.org/10.1146/annurev.nutr.24.012003.132407
  40. Stennicke HR & Salvesen GS (2000). Caspase assays. Methods Enzymol 322:91-100 https://doi.org/10.1016/S0076-6879(00)22010-7
  41. Sutherland MW & Learmonth BA (1997). The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismutase. Free Radic Res 27:283-289 https://doi.org/10.3109/10715769709065766
  42. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M & Yodoi J (2002). Redox control of cell death. Antioxi Redox Signal 4:405-414 https://doi.org/10.1089/15230860260196209
  43. Villa P, Kaufmann SH & Earnshaw WC (1997). Caspase and caspase inhibitors. Trends Biochem Sci 22:388-393 https://doi.org/10.1016/S0968-0004(97)01107-9
  44. Windhorst DB & Nigra T (1982). General clinical toxicology of oral retinoids. J Am Acad Dermatol 6:675-682 https://doi.org/10.1016/S0190-9622(82)70056-8
  45. Xu Q, Konta T & Kitamura M (2002). Retinoic acid regulation of mesangial cell apoptosis. Exp Nephrol 10:171-175 https://doi.org/10.1159/000058343
  46. Xu XC, Liu X, Tahara E, Lippman SM & Lotan R (1999). Expression and up-regulation of retinoic acid receptor-beta is associated with retinoid sensitivity and colony formation in esophageal cancer cell lines. Cancer Res 59:2477-2483

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