Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

ATF3 Mediates Anti-Cancer Activity of Trans-10, cis-12-Conjugated Linoleic Acid in Human Colon Cancer Cells

  • Kim, Kui-Jin (Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland) ;
  • Lee, Jihye (Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland) ;
  • Park, Yeonhwa (Department of Food Science, University of Massachusetts) ;
  • Lee, Seong-Ho (Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland)
  • Received : 2014.09.29
  • Accepted : 2014.12.11
  • Published : 2015.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Conjugated linoleic acids (CLA) are a family of isomers of linoleic acid. CLA increases growth arrest and apoptosis of human colorectal cancer cells through an isomer-specific manner. ATF3 belongs to the ATF/CREB family of transcription factors and is associated with apoptosis in colorectal cancer. The present study was performed to investigate the molecular mechanism by which t10, c12-CLA stimulates ATF3 expression and apoptosis in human colorectal cancer cells. t10, c12-CLA increased an apoptosis in human colorectal cancer cells in dose dependent manner. t10, c12-CLA induced ATF3 mRNA and luciferase activity of ATF3 promoter in a dose-dependent manner. The responsible region for ATF3 transcriptional activation by t10, c12-CLA is located between -147 and -1850 of ATF3 promoter. mRNA stability of ATF3 was not affected by t10, c12-CLA treatment. t10, c12-CLA increases $GSK3{\beta}$ expression and suppresses IGF-1-stimulated phosphorylation of Akt. The knockdown of ATF3 suppressed expression of $GSK3{\beta}$ and NAG-1 and PARP cleavage. The results suggest that t10, c12-CLA induces apoptosis through ATF3-mediated pathway in human colorectal cancer cells.

Keywords

References

  1. Agarwal, A., Das, K., Lerner, N., Sathe, S., Cicek, M., Casey, G. and Sizemore, N. (2005) The AKT/I kappa B kinase pathway promotes angiogenic/metastatic gene expression in colorectal cancer by activating nuclear factor-kappa B and beta-catenin. Oncogene 24, 1021-1031. https://doi.org/10.1038/sj.onc.1208296
  2. Ameri, K., Hammond, E. M., Culmsee, C., Raida, M., Katschinski, D. M., Wenger, R. H., Wagner, E., Davis, R. J., Hai, T., Denko, N. and Harris, A. L. (2007) Induction of activating transcription factor 3 by anoxia is independent of p53 and the hypoxic HIF signalling pathway. Oncogene 26, 284-289. https://doi.org/10.1038/sj.onc.1209781
  3. Aziz, M. H., Nihal, M., Fu, V. X., Jarrard, D. F. and Ahmad, N. (2006) Resveratrol-caused apoptosis of human prostate carcinoma LNCaP cells is mediated via modulation of phosphatidylinositol 3'-kinase/ Akt pathway and Bcl-2 family proteins. Mol. Cancer Ther. 5, 1335-1341. https://doi.org/10.1158/1535-7163.MCT-05-0526
  4. Baek, S. J., Kim, K. S., Nixon, J. B., Wilson, L. C. and Eling, T. E. (2001) Cyclooxygenase inhibitors regulate the expression of a TGF-beta superfamily member that has proapoptotic and antitumorigenic activities. Mol. Pharmacol. 59, 901-908.
  5. Baek, S. J., Okazaki, R., Lee, S. H., Martinez, J., Kim, J. S., Yamaguchi, K., Mishina, Y., Martin, D. W., Shoieb, A., McEntee, M. F. and Eling, T. E. (2006) Nonsteroidal anti-inflammatory drug-activated gene-1 over expression in transgenic mice suppresses intestinal neoplasia. Gastroenterology 131, 1553-1560. https://doi.org/10.1053/j.gastro.2006.09.015
  6. Belury, M. A. (2002) Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annu. Rev. Nutr. 22, 505-531. https://doi.org/10.1146/annurev.nutr.22.021302.121842
  7. Bijur, G. N. and Jope, R. S. (2001) Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3 beta. J. Biol. Chem. 276, 37436-37442. https://doi.org/10.1074/jbc.M105725200
  8. Cekanova, M., Lee, S. H., Donnell, R. L., Sukhthankar, M., Eling, T. E., Fischer, S. M. and Baek, S. J. (2009) Nonsteroidal anti-inflammatory drug-activated gene-1 expression inhibits urethane-induced pulmonary tumorigenesis in transgenic mice. Cancer Prev. Res. (Phila) 2, 450-458. https://doi.org/10.1158/1940-6207.CAPR-09-0057
  9. Chen, B. P., Wolfgang, C. D. and Hai, T. (1996) Analysis of ATF3, a transcription factor induced by physiological stresses and modulated by gadd153/Chop10. Mol. Cell. Biol. 16, 1157-1168. https://doi.org/10.1128/MCB.16.3.1157
  10. Chin, S. F., Storkson, J. M., Liu, W., Albright, K. J. and Pariza, M. W. (1994) Conjugated linoleic acid (9,11- and 10,12-octadecadienoic acid) is produced in conventional but not germ-free rats fed linoleic acid. J. Nutr. 124, 694-701.
  11. Cho, H. J., Kwon, G. T. and Park, J. H. (2009) trans-10,cis-12 Conjugated linoleic acid induces depolarization of mitochondrial membranes in HT-29 human colon cancer cells: a possible mechanism for induction of apoptosis. J. Med. Food 12, 952-958. https://doi.org/10.1089/jmf.2009.0056
  12. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. and Hemmings, B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789. https://doi.org/10.1038/378785a0
  13. Dilzer, A. and Park, Y. (2012) Implication of conjugated linoleic acid (CLA) in human health. Crit. Rev. Food Sci. Nutr. 52, 488-513. https://doi.org/10.1080/10408398.2010.501409
  14. Doble, B. W. and Woodgett, J. R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186. https://doi.org/10.1242/jcs.00384
  15. Donovan, E. A. and Kummar, S. (2008) Role of insulin-like growth factor-1R system in colorectal carcinogenesis. Crit. Rev. Oncol. Hematol. 66, 91-98. https://doi.org/10.1016/j.critrevonc.2007.09.003
  16. Forde, J. E. and Dale, T. C. (2007) Glycogen synthase kinase 3: a key regulator of cellular fate. Cell. Mol. Life Sci. 64, 1930-1944. https://doi.org/10.1007/s00018-007-7045-7
  17. Ha, Y. L., Storkson, J. and Pariza, M. W. (1990) Inhibition of benzo(a) pyrene-induced mouse forestomach neoplasia by conjugated dienoic derivatives of linoleic acid. Cancer Res. 50, 1097-1101.
  18. Hai, T. and Curran, T. (1991) Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl. Acad. Sci. U.S.A. 88, 3720-3724. https://doi.org/10.1073/pnas.88.9.3720
  19. Ip, C., Singh, M., Thompson, H. J. and Scimeca, J. A. (1994) Conjugated linoleic acid suppresses mammary carcinogenesis and proliferative activity of the mammary gland in the rat. Cancer Res. 54, 1212-1215.
  20. Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E. and Forman, D. (2011) Global cancer statistics. CA Cancer J. Clin. 61, 69-90. https://doi.org/10.3322/caac.20107
  21. Jeong, J. B., Choi, J., Lou, Z., Jiang, X. and Lee, S. H. (2013) Patchouli alcohol, an essential oil of Pogostemon cablin, exhibits anti-tumorigenic activity in human colorectal cancer cells. Int. Immunopharmacol. 16, 184-190. https://doi.org/10.1016/j.intimp.2013.04.006
  22. Jope, R. S. and Bijur, G. N. (2002) Mood stabilizers, glycogen synthase kinase-3beta and cell survival. Mol. Psychiatry 7 Suppl 1, S35-45. https://doi.org/10.1038/sj.mp.4001017
  23. Kim, E. J., Kang, I. J., Cho, H. J., Kim, W. K., Ha, Y. L. and Park, J. H. (2003) Conjugated linoleic acid downregulates insulin-like growth factor-I receptor levels in HT-29 human colon cancer cells. J. Nutr. 133, 2675-2681.
  24. Kumar, A. P., Garcia, G. E., Ghosh, R., Rajnarayanan, R. V., Alworth, W. L. and Slaga, T. J. (2003) 4-Hydroxy-3-methoxybenzoic acid methyl ester: a curcumin derivative targets Akt/NF kappa B cell survival signaling pathway: potential for prostate cancer management. Neoplasia 5, 255-266. https://doi.org/10.1016/S1476-5586(03)80057-X
  25. Lee, K. W., Lee, H. J., Cho, H. Y. and Kim, Y. J. (2005) Role of the conjugated linoleic acid in the prevention of cancer. Crit. Rev. Food Sci. Nutr. 45, 135-144. https://doi.org/10.1080/10408690490911800
  26. Lee, S. H., Bahn, J. H., Whitlock, N. C., and Baek, S. J. (2010a) Activating transcription factor 2 (ATF2) controls tolfenamic acid-induced ATF3 expression via MAP kinase pathways. Oncogene 29, 5182-5192. https://doi.org/10.1038/onc.2010.251
  27. Lee, S. H., Krisanapun, C., and Baek, S. J. (2010b) NSAID-activated gene-1 as a molecular target for capsaicin-induced apoptosis through a novel molecular mechanism involving GSK3{beta}, C/EBP {beta}, and ATF3. Carcinogenesis 31, 719-728. https://doi.org/10.1093/carcin/bgq016
  28. Lee, S. H., Min, K. W., Zhang, X. and Baek, S. J. (2013) 3,3'-diindolylmethane induces activating transcription factor 3 (ATF3) via ATF4 in human colorectal cancer cells. J. Nutr. Biochem. 24, 664-671. https://doi.org/10.1016/j.jnutbio.2012.03.016
  29. Lee, S. H., Yamaguchi, K., Kim, J. S., Eling, T. E., Safe, S., Park, Y. and Baek, S. J. (2006) Conjugated linoleic acid stimulates an antitumorigenic protein NAG-1 in an isomer specific manner. Carcinogenesis 27, 972-981. https://doi.org/10.1093/carcin/bgi268
  30. Lim, K. H. and Counter, C. M. (2005) Reduction in the requirement of oncogenic Ras signaling to activation of PI3K/AKT pathway during tumor maintenance. Cancer Cell 8, 381-392. https://doi.org/10.1016/j.ccr.2005.10.014
  31. Negrini, S., Gorgoulis, V. G. and Halazonetis, T. D. (2010) Genomic instability--an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 11, 220-228. https://doi.org/10.1038/nrm2858
  32. Roche, H. M., Noone, E., Sewter, C., Mc Bennett, S., Savage, D., Gibney, M. J., O'Rahilly, S. and Vidal-Puig, A. J. (2002) Isomerdependent metabolic effects of conjugated linoleic acid: insights from molecular markers sterol regulatory element-binding protein-1c and LXRalpha. Diabetes 51, 2037-2044. https://doi.org/10.2337/diabetes.51.7.2037
  33. Shukla, Y. and Singh, R. (2011) Resveratrol and cellular mechanisms of cancer prevention. Ann. N. Y. Acad. Sci. 1215, 1-8. https://doi.org/10.1111/j.1749-6632.2010.05870.x
  34. Umesalma, S. and Sudhandiran, G. (2011) Ellagic acid prevents rat colon carcinogenesis induced by 1, 2 dimethyl hydrazine through inhibition of AKT-phosphoinositide-3 kinase pathway. Eur. J. Pharmacol. 660, 249-258. https://doi.org/10.1016/j.ejphar.2011.03.036
  35. Wang, Z. Q., Stingl, L., Morrison, C., Jantsch, M., Los, M., Schulze-Osthoff, K. and Wagner, E. F. (1997) PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. 11, 2347-2358. https://doi.org/10.1101/gad.11.18.2347
  36. West, K. A., Brognard, J., Clark, A. S., Linnoila, I. R., Yang, X., Swain, S. M., Harris, C., Belinsky, S. and Dennis, P. A. (2003) Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J. Clin. Invest. 111, 81-90. https://doi.org/10.1172/JCI200316147
  37. West, K. A., Linnoila, I. R., Belinsky, S. A., Harris, C. C. and Dennis, P. A. (2004) Tobacco carcinogen-induced cellular transformation increases activation of the phosphatidylinositol 3'-kinase/Akt pathway in vitro and in vivo. Cancer Res. 64, 446-451. https://doi.org/10.1158/0008-5472.CAN-03-3241
  38. Yamaguchi, K., Lee, S. H., Eling, T. E. and Baek, S. J. (2004) Identification of nonsteroidal anti-inflammatory drug-activated gene (NAG-1) as a novel downstream target of phosphatidylinositol 3-kinase/ AKT/GSK-3beta pathway. J. Biol. Chem. 279, 49617-49623. https://doi.org/10.1074/jbc.M408796200

Cited by

  1. Anti-proliferative and Pro-apoptotic Effects by Lees Extracts of Ehwa Makgeolli Containing Oriental Herbs vol.26, pp.2, 2016, https://doi.org/10.5352/JLS.2016.26.2.241
  2. Naringenin-Mediated ATF3 Expression Contributes to Apoptosis in Human Colon Cancer vol.24, pp.2, 2016, https://doi.org/10.4062/biomolther.2015.109
  3. Vitex rotundifolia Fruit Extract Induces Apoptosis Through the Downregulation of ATF3-Mediated Bcl-2 Expression in Human Colorectal Cancer Cells vol.45, pp.04, 2017, https://doi.org/10.1142/S0192415X17500483
  4. Scientific Advances of Milk Enrichment with Conjugated Linoleic Acid to Produce Anti-Cancer Milk vol.In Press, pp.In Press, 2017, https://doi.org/10.17795/ijcp-5868
  5. Pterostilbene activates the GRP78–elF2α–ATF3 cascade of ER stress and subsequently induces apoptosis in human colon cancer cells vol.26, 2016, https://doi.org/10.1016/j.jff.2016.08.027
  6. In Vitro Anticancer Activity of Phlorofucofuroeckol A via Upregulation of Activating Transcription Factor 3 against Human Colorectal Cancer Cells vol.14, pp.4, 2016, https://doi.org/10.3390/md14040069
  7. Antitumor Properties of CLA-Enriched Food Products vol.70, pp.4, 2018, https://doi.org/10.1080/01635581.2018.1460684
  8. Dietary fatty acids modulation of human colon cancer cells: mechanisms and future perspectives vol.69, pp.4, 2018, https://doi.org/10.1080/09637486.2017.1382456
  9. Probiotic Conjugated Linoleic Acid Mediated Apoptosis in Breast Cancer Cells by Downregulation of NF-κB vol.17, pp.7, 2015, https://doi.org/10.14456/apjcp.2016.107/apjcp.2016.17.7.3395
  10. 오미자 박 추출물 및 schizandrin에 의한 암세포 항성장 및 세포사멸 활성 vol.28, pp.4, 2018, https://doi.org/10.5352/jls.2018.28.4.415
  11. Anticancer Activity of a Novel High Phenolic Sorghum Bran in Human Colon Cancer Cells vol.2020, pp.None, 2015, https://doi.org/10.1155/2020/2890536
  12. Master Regulator Activating Transcription Factor 3 (ATF3) in Metabolic Homeostasis and Cancer vol.11, pp.None, 2020, https://doi.org/10.3389/fendo.2020.00556
  13. Loss of activating transcription factor 3 prevents KRAS-mediated pancreatic cancer vol.40, pp.17, 2015, https://doi.org/10.1038/s41388-021-01771-z
  14. Extracellular vesicles-derived microRNA-222 promotes immune escape via interacting with ATF3 to regulate AKT1 transcription in colorectal cancer vol.21, pp.1, 2015, https://doi.org/10.1186/s12885-021-08063-5