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Journal of Gastrointestinal Cancer

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01.08.2019 | Original Research

DHA Abolishes the Detrimental Effect of Docetaxel on Downregulation of the MICA via Decreasing the Expression Level of MicroRNA-20a in Gastric Cancer

verfasst von: Najibeh Shekari, Mahsa Javadian, Sima Ghaffari, Behzad Baradaran, Masoud Darabi, Tohid Kazemi

Erschienen in: Journal of Gastrointestinal Cancer | Ausgabe 2/2020

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Abstract

Background

MHC class I chain-related protein A (MICA) is a membrane glycoprotein expressed abnormally on some malignant cells including gastric cancer (GC) cell and elicits anti-tumor immune responses. Downregulation of MICA expression could lead to immune-evasion of cancer cells.

Objective(s)

In this study, we aimed to investigate the effect of docosahexaenoic acid (DHA) and docetaxel alone or in combination on the expression level of MICA and its regulating microRNA (miRNA), miR-20a in MKN45 GC cell line.

Method(s)

MKN45 GC cell line was cultured and MTT assay was performed to determine IC50 of docetaxel. Cells were treated by 18.5 μM docetaxel and 100 μM DHA. After that, RNA extraction and cDNA synthesis were done and the expression level of MICA and miR-20a were determined by quantitative real-time PCR for both treated and untreated cell lines.

Results

Our findings showed less downregulation of the expression level of MICA by the combination of docetaxel/DHA (5.34-fold) compared with docetaxel (45.45-fold) and DHA (55.55-fold). Consistently, combination therapy led to the more downregulation of the expression level of the miR-20a (5.20-fold) in comparison to docetaxel (2.38-fold) and DHA (1.60-fold).

Conclusion(s)

As an unwanted effect of docetaxel therapy in GC, downregulation of MICA expression could lead to weak anti-tumor immune responses. By increasing the expression level of MICA, combination therapy of docetaxel with DHA would be useful to overcome this side effect.

Sitarz R, Skierucha M, Mielko J, Offerhaus GJA, Maciejewski R, Polkowski WP. Gastric cancer: epidemiology, prevention, classification, and treatment. Cancer Manag Res. 2018;10:239–48. https://doi.org/10.2147/cmar.s149619.CrossRefPubMedPubMedCentral

Park SC, Chun HJ. Chemotherapy for advanced gastric cancer: review and update of current practices. Gut and liver. 2013;7(4):385–93. https://doi.org/10.5009/gnl.2013.7.4.385.CrossRefPubMedPubMedCentral

Kanaji S, Suzuki S, Matsuda Y, Hasegawa H, Yamamoto M, Yamashita K, et al. Recent updates in perioperative chemotherapy and recurrence pattern of gastric cancer. Ann Gastroenterol Surg. 2018;2(6):400–5. https://doi.org/10.1002/ags3.12199.CrossRefPubMedPubMedCentral

Al-Batran S-E, Homann N, Schmalenberg H, Kopp H-G, Haag GM, Luley KB, et al. Perioperative chemotherapy with docetaxel, oxaliplatin, and fluorouracil/leucovorin (FLOT) versus epirubicin, cisplatin, and fluorouracil or capecitabine (ECF/ECX) for resectable gastric or gastroesophageal junction (GEJ) adenocarcinoma (FLOT4-AIO): a multicenter, randomized phase 3 trial. Proc Am Soc Clin Oncol. 2017;11:57.

Serini S, Calviello G. Long-chain omega-3 fatty acids and cancer: any cause for concern? Curr Opin Clin Nutri Metab Care. 2018;21(2):83–9. https://doi.org/10.1097/mco.0000000000000439.CrossRef

Liang P, Henning SM, Schokrpur S, Wu L, Doan N, Said J, et al. Effect of dietary omega-3 fatty acids on tumor-associated macrophages and prostate cancer progression. Prostate. 2016;76(14):1293–302. https://doi.org/10.1002/pros.23218.CrossRefPubMedPubMedCentral

Garcia CP, Lamarque AL, Comba A, Berra MA, Silva RA, Labuckas DO, et al. Synergistic anti-tumor effects of melatonin and PUFAs from walnuts in a murine mammary adenocarcinoma model. Nutrition (Burbank, Los Angeles County, Calif). 2015;31(4):570–7. https://doi.org/10.1016/j.nut.2014.06.001.CrossRef

Trombetta A, Maggiora M, Martinasso G, Cotogni P, Canuto RA, Muzio G. Arachidonic and docosahexaenoic acids reduce the growth of A549 human lung-tumor cells increasing lipid peroxidation and PPARs. Chem Biol Interact. 2007;165(3):239–50. https://doi.org/10.1016/j.cbi.2006.12.014.CrossRefPubMed

Chapkin RS, Seo J, McMurray DN, Lupton JR. Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. Chem Phys Lipids. 2008;153(1):14–23. https://doi.org/10.1016/j.chemphyslip.2008.02.011.CrossRefPubMedPubMedCentral

10.

Menendez JA, Ropero S, Mehmi I, Atlas E, Colomer R, Lupu R. Overexpression and hyperactivity of breast cancer-associated fatty acid synthase (oncogenic antigen-519) is insensitive to normal arachidonic fatty acid-induced suppression in lipogenic tissues but it is selectively inhibited by tumoricidal alpha-linolenic and gamma-linolenic fatty acids: a novel mechanism by which dietary fat can alter mammary tumorigenesis. Int J Oncol. 2004;24(6):1369–83.PubMed

11.

Dai J, Shen J, Pan W, Shen S, Das UN. Effects of polyunsaturated fatty acids on the growth of gastric cancer cells in vitro. Lipids Health Dis. 2013;12:71. https://doi.org/10.1186/1476-511x-12-71.CrossRefPubMedPubMedCentral

12.

Chen D, Gyllensten U. MICA polymorphism: biology and importance in cancer. Carcinogenesis. 2014;35(12):2633–42. https://doi.org/10.1093/carcin/bgu215.CrossRefPubMed

13.

Zhang J, Basher F, Wu JD. NKG2D ligands in tumor immunity: two sides of a coin. Front Immunol. 2015;6:97. https://doi.org/10.3389/fimmu.2015.00097.CrossRefPubMedPubMedCentral

14.

Morisaki T, Onishi H, Koya N, Kiyota A, Tanaka H, Umebayashi M, et al. Combinatorial cytotoxicity of gemcitabine and cytokine-activated killer cells in hepatocellular carcinoma via the NKG2D-MICA/B system. Anticancer Res. 2011;31(7):2505–10.PubMed

15.

Kong YW, Ferland-McCollough D, Jackson TJ, Bushell M. microRNAs in cancer management. The Lancet Oncology. 2012;13(6):e249–58. https://doi.org/10.1016/s1470-2045(12)70073-6.CrossRefPubMed

16.

Tsoukas MA, Ko BJ, Witte TR, Dincer F, Hardman WE, Mantzoros CS. Dietary walnut suppression of colorectal cancer in mice: mediation by miRNA patterns and fatty acid incorporation. J Nutr Biochem. 2015;26(7):776–83. https://doi.org/10.1016/j.jnutbio.2015.02.009.CrossRefPubMed

17.

Shekari N, Baradaran B, Shanehbandi D, Kazemi T. Circulating microRNAs: valuable biomarkers for the diagnosis and prognosis of gastric cancer. Curr Med Chem. 2018;25(6):698–714. https://doi.org/10.2174/0929867324666171003123425.CrossRefPubMed

18.

Liu X, Cai H, Sheng W, Huang H, Long Z, Wang Y. microRNAs expression profile related with response to preoperative radiochemotherapy in patients with locally advanced gastric cancer. BMC Cancer. 2018;18(1):1048. https://doi.org/10.1186/s12885-018-4967-4.CrossRefPubMedPubMedCentral

19.

Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, et al. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol. 2008;9(9):1065–73. https://doi.org/10.1038/ni.1642.CrossRefPubMed

20.

Kishikawa T, Otsuka M, Yoshikawa T, Ohno M, Takata A, Shibata C, et al. Regulation of the expression of the liver cancer susceptibility gene MICA by microRNAs. Sci Rep. 2013;3:2739. https://doi.org/10.1038/srep02739.CrossRefPubMedPubMedCentral

21.

Yang H, Lan P, Hou Z, Guan Y, Zhang J, Xu W, et al. Histone deacetylase inhibitor SAHA epigenetically regulates miR-17-92 cluster and MCM7 to upregulate MICA expression in hepatoma. Br J Cancer. 2015;112(1):112–21. https://doi.org/10.1038/bjc.2014.547.CrossRefPubMed

22.

Xie J, Liu M, Li Y, Nie Y, Mi Q, Zhao S. Ovarian tumor-associated microRNA-20a decreases natural killer cell cytotoxicity by downregulating MICA/B expression. Cell Mol Immunol. 2014;11(5):495–502. https://doi.org/10.1038/cmi.2014.30.CrossRefPubMedPubMedCentral

23.

Zhang Q, Wang Q, Sun W, Gao F, Liu L, Cheng L, et al. Change of circulating and tissue-based miR-20a in human cancers and associated prognostic implication: a systematic review and meta-analysis. Biomed Res Int. 2018;2018:6124927–14. https://doi.org/10.1155/2018/6124927.CrossRefPubMedPubMedCentral

24.

Shekari N, Asghari F, Haghnavaz N, Shanehbandi D, Khaze V, Baradaran B, et al. Let-7a could serve as a biomarker for chemo-responsiveness to docetaxel in gastric cancer. Anti Cancer Agents Med Chem. 2019;19(3):304–9. https://doi.org/10.2174/1871520619666181213110258.CrossRef

25.

Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A. Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr. 2004;79(6):935–45. https://doi.org/10.1093/ajcn/79.6.935.CrossRefPubMed

26.

Slagsvold JE, Pettersen CH, Storvold GL, Follestad T, Krokan HE, Schonberg SA. DHA alters expression of target proteins of cancer therapy in chemotherapy resistant SW620 colon cancer cells. Nutr Cancer. 2010;62(5):611–21. https://doi.org/10.1080/01635580903532366.CrossRefPubMed

27.

Serini S, Ottes Vasconcelos R, Fasano E, Calviello G. How plausible is the use of dietary n-3 PUFA in the adjuvant therapy of cancer? Nutr Res Rev. 2016;29(1):102–25. https://doi.org/10.1017/s0954422416000044.CrossRefPubMed

28.

Shaikh IA, Brown I, Schofield AC, Wahle KW, Heys SD. Docosahexaenoic acid enhances the efficacy of docetaxel in prostate cancer cells by modulation of apoptosis: the role of genes associated with the NF-kappaB pathway. Prostate. 2008;68(15):1635–46. https://doi.org/10.1002/pros.20830.CrossRefPubMed

29.

Gao K, Liang Q, Zhao ZH, Li YF, Wang SF. Synergistic anticancer properties of docosahexaenoic acid and 5-fluorouracil through interference with energy metabolism and cell cycle arrest in human gastric cancer cell line AGS cells. World J Gastroenterol. 2016;22(10):2971–80. https://doi.org/10.3748/wjg.v22.i10.2971.CrossRefPubMedPubMedCentral

30.

Shekari N, Javadian M, Ghasemi M, Baradaran B, Darabi M, Kazemi T. Synergistic beneficial effect of docosahexaenoic acid (DHA) and docetaxel on the expression level of matrix metalloproteinase-2 (MMP-2) and MicroRNA-106b in gastric cancer. J Gastrointes Cancer. 2019. https://doi.org/10.1007/s12029-019-00205-0.

31.

D'Eliseo D, Velotti F. Omega-3 fatty acids and cancer cell cytotoxicity: implications for multi-targeted cancer therapy. J Clin Med. 2016;5(2). https://doi.org/10.3390/jcm5020015.

32.

Ghadially H, Brown L, Lloyd C, Lewis L, Lewis A, Dillon J, et al. MHC class I chain-related protein a and B (MICA and MICB) are predominantly expressed intracellularly in tumour and normal tissue. Br J Cancer. 2017;116(9):1208–17. https://doi.org/10.1038/bjc.2017.79.CrossRefPubMedPubMedCentral

33.

Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A. 1996;93(22):12445–50. https://doi.org/10.1073/pnas.93.22.12445.CrossRefPubMedPubMedCentral

34.

Ribeiro CH, Kramm K, Galvez-Jiron F, Pola V, Bustamante M, Contreras HR, et al. Clinical significance of tumor expression of major histocompatibility complex class I-related chains A and B (MICA/B) in gastric cancer patients. Oncol Rep. 2016;35(3):1309–17. https://doi.org/10.3892/or.2015.4510.CrossRefPubMed

35.

Chen Y, Lin WS, Zhu WF, Lin J, Zhou ZF, Huang CZ, et al. Tumor MICA status predicts the efficacy of immunotherapy with cytokine-induced killer cells for patients with gastric cancer. Immunol Res. 2016;64(1):251–9. https://doi.org/10.1007/s12026-015-8743-0.CrossRefPubMed

36.

Okita R, Wolf D, Yasuda K, Maeda A, Yukawa T, Saisho S, et al. Contrasting effects of the cytotoxic anticancer drug gemcitabine and the EGFR tyrosine kinase inhibitor Gefitinib on NK cell-mediated cytotoxicity via regulation of NKG2D ligand in non-small-cell lung cancer cells. PLoS One. 2015;10(10):e0139809. https://doi.org/10.1371/journal.pone.0139809.CrossRefPubMedPubMedCentral

37.

Codo P, Weller M, Meister G, Szabo E, Steinle A, Wolter M, et al. MicroRNA-mediated down-regulation of NKG2D ligands contributes to glioma immune escape. Oncotarget. 2014;5(17):7651–62. https://doi.org/10.18632/oncotarget.2287.CrossRefPubMedPubMedCentral

38.

Wang B, Wang Q, Wang Z, Jiang J, Yu SC, Ping YF, et al. Metastatic consequences of immune escape from NK cell cytotoxicity by human breast cancer stem cells. Cancer Res. 2014;74(20):5746–57. https://doi.org/10.1158/0008-5472.can-13-2563.CrossRefPubMed

39.

Tang S, Fu H, Xu Q, Zhou Y. miR-20a regulates sensitivity of colorectal cancer cells to NK cells by targeting MICA. Biosci Rep. 2019;39(7):BSR20180695. https://doi.org/10.1042/bsr20180695.CrossRefPubMedPubMedCentral

40.

Zhu SY, Wu QY, Zhang CX, Wang Q, Ling J, Huang XT, et al. miR-20a inhibits the killing effect of natural killer cells to cervical cancer cells by downregulating RUNX1. Biochem Biophys Res Commun. 2018;505(1):309–16. https://doi.org/10.1016/j.bbrc.2018.09.102.CrossRefPubMed

41.

Davidson LA, Wang N, Shah MS, Lupton JR, Ivanov I, Chapkin RS. n-3 polyunsaturated fatty acids modulate carcinogen-directed non-coding microRNA signatures in rat colon. Carcinogenesis. 2009;30(12):2077–84. https://doi.org/10.1093/carcin/bgp245.CrossRefPubMedPubMedCentral

42.

Ross SA, Davis CD. MicroRNA, nutrition, and cancer prevention. Adv Nutri (Bethesda, Md). 2011;2(6):472–85. https://doi.org/10.3945/an.111.001206.CrossRef

43.

Li H, Wu Q, Li T, Liu C, Xue L, Ding J, et al. The miR-17-92 cluster as a potential biomarker for the early diagnosis of gastric cancer: evidence and literature review. Oncotarget. 2017;8(28):45060–71. https://doi.org/10.18632/oncotarget.15023.CrossRefPubMedPubMedCentral

44.

Dhar S, Hicks C, Levenson AS. Resveratrol and prostate cancer: promising role for microRNAs. Mol Nutr Food Res. 2011;55(8):1219–29. https://doi.org/10.1002/mnfr.201100141.CrossRefPubMed

45.

Kang HW, Wang F, Wei Q, Zhao YF, Liu M, Li X, et al. miR-20a promotes migration and invasion by regulating TNKS2 in human cervical cancer cells. FEBS Lett. 2012;586(6):897–904. https://doi.org/10.1016/j.febslet.2012.02.020.CrossRefPubMed

46.

Huang G, Nishimoto K, Zhou Z, Hughes D, Kleinerman ES. miR-20a encoded by the miR-17-92 cluster increases the metastatic potential of osteosarcoma cells by regulating Fas expression. Cancer Res. 2012;72(4):908–16. https://doi.org/10.1158/0008-5472.can-11-1460.CrossRefPubMed

47.

Li X, Pan JH, Song B, Xiong EQ, Chen ZW, Zhou ZS, et al. Suppression of CX43 expression by miR-20a in the progression of human prostate cancer. Cancer Biol Ther. 2012;13(10):890–8. https://doi.org/10.4161/cbt.20841.CrossRefPubMed

48.

Chang Y, Liu C, Yang J, Liu G, Feng F, Tang J, et al. MiR-20a triggers metastasis of gallbladder carcinoma. J Hepatol. 2013;59(3):518–27. https://doi.org/10.1016/j.jhep.2013.04.034.CrossRefPubMed

49.

O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435(7043):839–43. https://doi.org/10.1038/nature03677.CrossRefPubMed

50.

Pickering MT, Stadler BM, Kowalik TF. miR-17 and miR-20a temper an E2F1-induced G1 checkpoint to regulate cell cycle progression. Oncogene. 2009;28(1):140–5. https://doi.org/10.1038/onc.2008.372.CrossRefPubMed

51.

Fan X, Liu Y, Jiang J, Ma Z, Wu H, Liu T, et al. miR-20a promotes proliferation and invasion by targeting APP in human ovarian cancer cells. Acta Biochim Biophys Sin. 2010;42(5):318–24.CrossRef

52.

Wang M, Gu H, Qian H, Zhu W, Zhao C, Zhang X, et al. miR-17-5p/20a are important markers for gastric cancer and murine double minute 2 participates in their functional regulation. Euro J Cancer (Oxford, England : 1990). 2013;49(8):2010–21. https://doi.org/10.1016/j.ejca.2012.12.017.CrossRef

53.

Li X, Zhang Z, Yu M, Li L, Du G, Xiao W, et al. Involvement of miR-20a in promoting gastric cancer progression by targeting early growth response 2 (EGR2). Int J Mol Sci. 2013;14(8):16226–39. https://doi.org/10.3390/ijms140816226.CrossRefPubMedPubMedCentral

54.

Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, et al. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem. 2007;282(4):2135–43. https://doi.org/10.1074/jbc.M608939200.CrossRefPubMed

Titel: DHA Abolishes the Detrimental Effect of Docetaxel on Downregulation of the MICA via Decreasing the Expression Level of MicroRNA-20a in Gastric Cancer
verfasst von: Najibeh Shekari
Mahsa Javadian
Sima Ghaffari
Behzad Baradaran
Masoud Darabi
Tohid Kazemi
Publikationsdatum: 01.08.2019
Verlag: Springer US
Erschienen in: Journal of Gastrointestinal Cancer / Ausgabe 2/2020
Print ISSN: 1941-6628
Elektronische ISSN: 1941-6636
DOI: https://doi.org/10.1007/s12029-019-00280-3

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Springer Medizin

DHA Abolishes the Detrimental Effect of Docetaxel on Downregulation of the MICA via Decreasing the Expression Level of MicroRNA-20a in Gastric Cancer

Abstract

Background

Objective(s)

Method(s)

Results

Conclusion(s)

Neu im Fachgebiet Onkologie

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Krebspatienten impfen: Was? Wen? Und wann nicht?

Müde im Alter? Auch an die Nebenniere denken

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Springer Medizin

Abstract

Background

Objective(s)

Method(s)

Results

Conclusion(s)

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