The role of dietary phytochemicals in the carcinogenesis via the modulation of miRNA expression
Language English Country Germany Media print-electronic
Document type Journal Article, Review
Grant support
VEGA 1/0136/19
Agentúra Ministerstva Školstva, Vedy, Výskumu a Športu SR
VEGA 1/0124/17
Agentúra Ministerstva Školstva, Vedy, Výskumu a Športu SR
Grant 08-08
Russian Science Support Foundation
PubMed
31127362
PubMed Central
PMC11810323
DOI
10.1007/s00432-019-02940-0
PII: 10.1007/s00432-019-02940-0
Knihovny.cz E-resources
- Keywords
- Cancer, Carcinogenesis, Phytochemicals, Plant-derived food, microRNAs,
- MeSH
- Antineoplastic Agents, Phytogenic administration & dosage pharmacology MeSH
- Carcinogenesis drug effects genetics MeSH
- Humans MeSH
- MicroRNAs biosynthesis genetics MeSH
- Neoplasms drug therapy genetics pathology MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Antineoplastic Agents, Phytogenic MeSH
- MicroRNAs MeSH
PURPOSE: Phytochemicals are naturally occurring plant-derived compounds and some of them have the potential to serve as anticancer drugs. Based on recent evidence, aberrantly regulated expression of microRNAs (miRNAs) is closely associated with malignancy. MicroRNAs are characterized as small non-coding RNAs functioning as posttranscriptional regulators of gene expression. Accordingly, miRNAs regulate various target genes, some of which are involved in the process of carcinogenesis. RESULTS: This comprehensive review emphasizes the anticancer potential of phytochemicals, either isolated or in combination, mediated by miRNAs. The ability to modulate the expression of miRNAs demonstrates their importance as regulators of tumorigenesis. Phytochemicals as anticancer agents targeting miRNAs are widely studied in preclinical in vitro and in vivo research. Unfortunately, their anticancer efficacy in targeting miRNAs is less investigated in clinical research. CONCLUSIONS: Significant anticancer properties of phytochemicals as regulators of miRNA expression have been proven, but more studies investigating their clinical relevance are needed.
Department of Immunology School of Medicine Keimyung University Dalseo Gu Daegu Korea
Department of Internal Medicine Brothers of Mercy Hospital Polni 553 3 63900 Brno Czech Republic
Faculty of Health Science and Social Work Trnava University Trnava Slovakia
Faculty of Medicine Central University Hospital of Asturias University of Oviedo Oviedo Spain
Institute for Health and Sport Victoria University Melbourne Australia
See more in PubMed
Abba ML, Patil N, Leupold JH, Moniuszko M, Utikal J, Niklinski J, Allgayer H (2017) MicroRNAs as novel targets and tools in cancer therapy. Cancer Lett 387:84–94 PubMed
Abbasi BA, Iqbal J, Mahmood T, Khalil AT, Ali B, Kanwal S, Sayed Shah A, Ahmad R (2018) Role of dietary phytochemicals in modulation of miRNA expression: natural swords combating breast cancer. Asian Pac J Trop Med 11:501–509
Abotaleb M, Samuel SM, Varghese E, Varghese S, Kubatka P, Liskova A, Büsselberg D (2018) Flavonoids in cancer and apoptosis. Cancers (Basel) 11:28 PubMed PMC
Avci CB, Susluer SY, Caglar HO, Balci T, Aygunes D, Dodurga Y, Gunduz C (2014) Genistein-induced mir-23b expression inhibits the growth of breast cancer cells. Contemp Oncol (Pozn) 19:32–35 PubMed PMC
Bahena-Ocampo I, Espinosa M, Ceballos-Cancino G, Lizarraga F, Campos-Arroyo D, Schwarz A, Maldonado V, Melendez-Zajgla J, Garcia-Lopez P (2016) miR-10b expression in breast cancer stem cells supports self-renewal through negative PTEN regulation and sustained AKT activation. EMBO Rep 17:648–658 PubMed PMC
Bai JW, Wang X, Zhang YF, Yao GD, Liu H (2017) MicroRNA-320 inhibits cell proliferation and invasion in breast cancer cells by targeting SOX4. Oncol Lett 14:7145–7152 PubMed PMC
Bandara KV, Michael MZ, Gleadle JM (2017) MicroRNA biogenesis in hypoxia. Microrna 6:80–96 PubMed
Bespalov VG, Alexandrov VA, Vysochina GI, Kostikova VA, Baranenko DA (2017) The inhibiting activity of meadowsweet extract on neurocarcinogenesis induced transplacentally in rats by ethylnitrosourea. J Neurooncol 131:459–467 PubMed
Bespalov VG, Alexandrov VA, Semenov AL, Vysochina GI, Kostikova VA, Baranenko DA (2018) The inhibitory effect of PubMed
Blahna MT, Hata A (2012) Smad-mediated regulation of microRNA biosynthesis. FEBS Lett 586:1906–1912 PubMed PMC
Catalanotto C, Cogoni C, Zardo G (2016) MicroRNA in control of gene expression: an overview of nuclear functions. Int J Mol Sci 17:1712 PubMed PMC
Chan SH, Wang LH (2015) Regulation of cancer metastasis by microRNAs. J Biomed Sci 22:9 PubMed PMC
Chen Y, Gao DY, Huang L (2015) In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv Drug Deliv Rev 81:128–141 PubMed PMC
Cheng CW, Wang HW, Chang CW, Chu HW, Chen CY, Yu JC, Chao JI, Liu HF, Ding SL, Shen CY (2012) MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer. Breast Cancer Res Treat 134:1081–1093 PubMed
Chiou YS, Li S, Ho CT, Pan MH (2018) Prevention of breast cancer by natural phytochemicals: focusing on molecular targets and combinational strategy. Mol Nutr Food Res 62:e1800392 PubMed
Chiu HS, Martínez MR, Komissarova EV, Llobet-Navas D, Bansal M, Paull EO, Califano A (2018) The number of titrated microRNA species dictates ceRNA regulation. Nucleic Acids Res 46:4354–4369 PubMed PMC
Choi SK, Kim HS, Jin T, Hwang EH, Jung M, Moon WK (2016) Overexpression of the miR-141/200c cluster promotes the migratory and invasive ability of triple-negative breast cancer cells through the activation of the FAK and PI3 K/AKT signaling pathways by secreting VEGF-A. BMC Cancer 16:570 PubMed PMC
Coker-Gurkan A, Bulut D, Genc R, Arisan ED, Obakan-Yerlikaya P, Palavan-Unsal N (2018) Curcumin prevented human autocrine growth hormone (GH) signaling mediated NF-κB activation and miR-183-96-182 cluster stimulated epithelial mesenchymal transition in T47D breast cancer cells. Mol Biol Rep 46:355–369 PubMed
Cong N, Du P, Zhang A, Shen F, Su J, Pu P, Wang T, Zjang J, Kang C, Zhang Q (2013) Downregulated microRNA-200a promotes EMT and tumor growth through the wnt/β-catenin pathway by targeting the E-cadherin repressors ZEB1/ZEB2 in gastric adenocarcinoma. Oncol Rep 29:1579–1587 PubMed
Dacosta C, Bao Y (2017) The role of MicroRNAs in the chemopreventive activity of sulforaphane from cruciferous vegetables. Nutrients 9:902 PubMed PMC
Dahiya N, Sherman-Baust CA, Wang TL, Davidson B, Shih I, Zhang Y, Wood W, Becker KG, Morin PJ (2008) MicroRNA expression and identification of putative miRNA targets in ovarian cancer. PLoS One 3:e2436 PubMed PMC
Dang K, Myers KA (2015) The role of hypoxia-induced miR-210 in cancer progression. Int J Mol Sci 16:6353–6372 PubMed PMC
de la Parra C, Castillo-Pichardo L, Cruz-Collazo A, Cubano L, Redis R, Calin GA, Dharmawardhane S (2016) Soy isoflavone genistein-mediated downregulation of miR-155 contributes to the anticancer effects of genistein. Nutr Cancer 68:154–164 PubMed PMC
Derosa G, Maffioli P, Sahebkar A (2016) Ellagic acid and its role in chronic diseases. Adv Exp Med Biol 928:473–479 PubMed
Diaz-Gerevini GT, Repossi G, Dain A, Tarres MC, Das UN, Eynard AR (2016) Beneficial action of resveratrol: how and why? Nutrition 32:174–178 PubMed
Dong J, Liu Y, Liao W, Liu R, Shi P, Wang L (2016) miRNA-223 is a potential diagnostic and prognostic marker for osteosarcoma. J Bone Oncol 5:74–79 PubMed PMC
Dou H, Shen R, Tao J, Huang L, Shi H, Chen H, Wang Y, Wang T (2017) Curcumin suppresses the colon cancer proliferation by inhibiting Wnt/β-catenin pathways via miR-130a. Front Pharmacol 8:877 PubMed PMC
Du C, Weng X, Hu W, Lv Z, Xiao H, Ding C, Gyabaah OA, Xie H, Zhou L, Wu J et al (2015) Hypoxia-inducible MiR-182 promotes angiogenesis by targeting RASA1 in hepatocellular carcinoma. J Exp Clin Cancer Res 34:67 PubMed PMC
Duan J, Zhang H, Qu Y, Deng T, Huang D, Liu R, Zhang L, Bai M, Zhou L, Ying G, Ba Y (2016) Onco-miR-130 promotes cell proliferation and migration by targeting TGFβR2 in gastric cancer. Oncotarget 7:44522–44533 PubMed PMC
Fan Y, Ma X, Li H, Gao Y, Huang Q, Zhang Y, Bao X, Du Q, Luo G, Liu K et al (2018) miR-122 promotes metastasis of clear-cell renal cell carcinoma by downregulating Dicer. Int J Cancer 142:547–560 PubMed
Feitelson MA, Arzumanyan A, Kulathinal RJ, Blain SW, Holcombe RF, Mahajna J, Marino M, Martinez-Chantar ML, Nawroth R, Sanchez-Garcia I et al (2015) Sustained proliferation in cancer: mechanisms and novel therapeutic targets. Semin Cancer Biol 35(Suppl):S25–S54 PubMed PMC
Feng YH, Tsao CJ (2016) Emerging role of microRNA-21 in cancer. Biomed Rep 5:395–402 PubMed PMC
Gandhi NS, Tekade RK, Chougule MB (2014) Nanocarrier mediated delivery of siRNA/miRNA in combination with chemotherapeutic agents for cancer therapy: current progress and advances. J Control Release 194:238–256 PubMed PMC
Ghoncheh M, Pournamdar Z, Salehiniya H (2016) Incidence and mortality and epidemiology of breast cancer in the world. Asian Pac J Cancer Prev 17(S3):43–46 PubMed
Golubnitschaja O, Debald M, Yeghiazaryan K, Kuhn W, Pešta M, Costigliola V, Grech G (2016) Breast cancer epidemic in the early twenty-first century: evaluation of risk factors, cumulative questionnaires and recommendations for preventive measures. Tumour Biol 37:12941–12957 PubMed
Gong J, Cui Z, Li L, Ma Q, Wang Q, Gao Y, Sun H (2015) MicroRNA-25 promotes gastric cancer proliferation, invasion, and migration by directly targeting F-box and WD-40 Domain Protein 7, FBXW7. Tumour Biol 36:7831–7840 PubMed
González-Sarrías A, Núñez-Sánchez MÁ, Tomé-Carneiro J, Tomás-Barberán FA, García-Conesa MT, Espín JC (2016) Comprehensive characterization of the effects of ellagic acid and urolithins on colorectal cancer and key-associated molecular hallmarks: microRNA cell specific induction of CDKN1A (p21) as a common mechanism involved. Mol Nutr Food Res 60:701–716 PubMed
Gu JB, Bao XB, Ma Z (2018) Effects of miR-21 on proliferation and apoptosis in human gastric adenocarcinoma cells. Oncol Lett 15:618–622 PubMed PMC
Guan H, Li W, Li Y, Wang J, Li Y, Tang Y, Lu S (2017) MicroRNA-93 promotes proliferation and metastasis of gastric cancer via targeting TIMP2. PLoS One 12:e0189490 PubMed PMC
Gulyaeva LF, Kushlinskiy NE (2016) Regulatory mechanisms of microRNA expression. J Transl Med 14:143 PubMed PMC
Guo R, Wang Y, Shi WY, Liu B, Hou SQ, Liu L (2012) MicroRNA miR-491-5p targeting both TP53 and Bcl-XL induces cell apoptosis in SW1990 pancreatic cancer cells through mitochondria mediated pathway. Molecules 17:14733–14747 PubMed PMC
Guo LH, Li H, Wang F, Yu J, He JS (2013) The tumor suppressor roles of miR-433 and miR-127 in gastric cancer. Int J Mol Sci 14:14171–14184 PubMed PMC
Guo F, Cogdell D, Hu L, Yang D, Sood AK, Xue F, Zhang W (2014) MiR-101 suppresses the epithelial-to-mesenchymal transition by targeting ZEB1 and ZEB2 in ovarian carcinoma. Oncol Rep 31:2021–2028 PubMed PMC
Guo X, Cai Q, Bao P, Wu J, Wen W, Ye F, Zheng W, Zheng Y, Shu XO (2016) Long-term soy consumption and tumor tissue MicroRNA and gene expression in triple-negative breast cancer. Cancer 122:2544–2551 PubMed PMC
Gurtan AM, Sharp PA (2013) The role of miRNAs in regulating gene expression networks. J Mol Biol 425:3582–3600 PubMed PMC
Hamam R, Ali AM, Alsaleh KA, Kassem M, Alfayez M, Aldahmash A, Alajez NM (2016) microRNA expression profiling on individual breast cancer patients identifies novel panel of circulating microRNA for early detection. Sci Rep 6:25997 PubMed PMC
Hargraves KG, He L, Firestone GL (2015) Phytochemical regulation of the tumor suppressive microRNA, miR-34a, by p53-dependent and independent responses in human breast cancer cells. Mol Carcinog 55:486–498 PubMed PMC
Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, van Rooij E, Olson EN (2010) Modulation of K-Ras-dependent lung tumorigenesis by MicroRNA-21. Cancer Cell 18:282–293 PubMed PMC
Herbert KM, Sarkar SK, Mills M, Delgado De la Herran HC, Neuman KC, Steitz JA (2016) A heterotrimer model of the complete microprocessor complex revealed by single-molecule subunit counting. RNA 22:175–183 PubMed PMC
Humphreys KJ, Conlon MA, Young GP, Topping DL, Hu Y, Winter JM, Le Leu RK (2014) Dietary manipulation of oncogenic microRNA expression in human rectal mucosa: a randomized trial. Cancer Prev Res (Phila) 7:786–795 PubMed
Jiang S, Zhang HW, Lu MH, He XH, Li Y, Gu H, Liu MF, Wang ED (2010) MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 70:3119–3127 PubMed
Jiang F, Zhao W, Zhou L, Zhang L, Liu Z, Yu D (2014) miR-222 regulates the cell biological behavior of oral squamous cell carcinoma by targeting PUMA. Oncol Rep 31:1255–1262 PubMed
Kapinova A, Kubatka P, Golubnitschaja O, Kello M, Zubor P, Solar P, Pec M (2018) Dietary phytochemicals in breast cancer research: anticancer effects and potential utility for effective chemoprevention. Environ Health Prev Med 23:36 PubMed PMC
Kartha RV, Subramanian S (2014) Competing endogenous RNAs (ceRNAs): new entrants to the intricacies of gene regulation. Front Genet 5:8 PubMed PMC
Katchy A, Williams C (2014) Profiling of estrogen-regulated microRNAs in breast cancer cells. J Vis Exp JoVE 84:e51285 PubMed PMC
Ke HL, Li WM, Lin HH, Hsu WC, Hsu YL, Chang LL, Huang CN, Li CC, Chang HP, Yeh HC et al (2017) Hypoxia-regulated MicroRNA-210 overexpression is associated with tumor development and progression in upper tract urothelial carcinoma. Int J Med Sci 14:578–584 PubMed PMC
Kim YJ, Chung SO, Kim JK, Park SU (2017) Recent studies on resveratrol and its biological and pharmacological activity. EXCLI J 16:602–608 PubMed PMC
Kim J, Yao F, Xiao Z, Sun Y, Ma L (2018) MicroRNAs and metastasis: small RNAs play big roles. Cancer Metastasis Rev 37:5–15 PubMed PMC
Klinge CM (2015) miRNAs regulated by estrogens, tamoxifen, and endocrine disruptors and their downstream gene targets. Mol Cell Endocrinol 418:273–297 PubMed PMC
Kong D, Heath E, Chen W, Cher M, Powell I, Heilbrun L, Li Y, Ali S, Sethi S, Hassan O et al (2012) Epigenetic silencing of miR-34a in human prostate cancer cells and tumor tissue specimens can be reversed by BR-DIM treatment. Am J Transl Res 4:14–23 PubMed PMC
Kong W, He L, Richards EJ, Challa S, Xu CX, Permuth-Wey J, Lancaster JM, Coppola D, Sellers TA, Djeu JY et al (2014) Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene 33:679–689 PubMed PMC
Koo KH, Kwon H (2018) MicroRNA miR-4779 suppresses tumor growth by inducing apoptosis and cell cycle arrest through direct targeting of PAK2 and CCND3. Cell Death Dis 9:77 PubMed PMC
Korpal M, Lee ES, Hu G, Kang Y (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283:14910–14914 PubMed PMC
Kubatka P, Uramova S, Kello M, Kajo Karol, Kruzliak P, Mojzis J, Vybohova D, Adamkov M, Jasek K, Lasabova Z et al (2017) Antineoplastic effects of clove buds ( PubMed PMC
Kumarswamy R, Mudduluru G, Ceppi P, Muppala S, Kozlowski M, Niklinski J, Papotti M, Allgayer H (2012) MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int J Cancer 130:2044–2053 PubMed
Kurozumi S, Yamaguchi Y, Kurosumi M, Ohira M, Matsumoto H, Horiguchi J (2017) Recent trends in microRNA research into breast cancer with particular focus on the associations between microRNAs and intrinsic subtypes. J Hum Genet 62:15–24 PubMed
Ladomery MR, Maddocks DG, Wilson ID (2011) MicroRNAs: their discovery, biogenesis, function and potential use as biomarkers in non-invasive prenatal diagnostics. Int J Mol Epidemiol Genet 2:253–260 PubMed PMC
Lan H, Chen W, He G, Yang S (2015) miR-140-5p inhibits ovarian cancer growth partially by repression of PDGFRA. Biomed Pharmacother 75:117–122 PubMed
le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A, Anile C, Maira G, Mercatelli N, Ciafrè SA, Farace MG, Agami R (2007) Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 26:3699–3708 PubMed PMC
Lee CM, Lee J, Nam MJ, Park SH (2018) Indole-3-carbinol induces apoptosis in human osteosarcoma MG-63 and U2OS cells. Biomed Res Int 2018:7970618 PubMed PMC
Lewinska A, Adamczyk-Grochala J, Deregowska A, Wnuk M (2017) Sulforaphane-induced cell cycle arrest and senescence are accompanied by DNA hypomethylation and changes in microRNA profile in breast cancer cells. Theranostics 7:3461–3477 PubMed PMC
Li C, Hashimi SM, Good DA, Cao S, Duan W, Plummer PN, Mellick AS, Wei MQ (2012) Apoptosis and microRNA aberrations in cancer. Clin Exp Pharmacol Physiol 39:739–746 PubMed
Li Q, Eades G, Yao Y, Zhang Y, Zhou Q (2014a) Characterization of a stem-like subpopulation in basal-like ductal carcinoma in situ (DCIS) lesions. J Biol Chem 289:1303–1312 PubMed PMC
Li L, Huang K, You Y, Fu X, Hu L, Song L, Meng Y (2014b) Hypoxia-induced miR-210 in epithelial ovarian cancer enhances cancer cell viability via promoting proliferation and inhibiting apoptosis. Int J Oncol 44:2111–2120 PubMed
Li L, Li B, Chen D, Liu L, Huang C, Lu Z, Lun L, Wan X (2015a) miR-139 and miR-200c regulate pancreatic cancer endothelial cell migration and angiogenesis. Oncol Rep 34:51–58 PubMed
Li D, Xia H, Li ZY, Hua L, Li L (2015b) Identification of novel breast cancer subtype-specific biomarkers by integrating genomics analysis of DNA copy number aberrations and miRNA-mRNA dual expression profiling. Biomed Res Int 2015:746970 PubMed PMC
Li Y, Zhang D, Wang X, Yao X, Ye C, Zhang S, Wang H, Chang C, Xia H, Wang YC et al (2015c) Hypoxia-inducible miR-182 enhances HIF1α signaling via targeting PHD2 and FIH1 in prostate cancer. Sci Rep 5:12495 PubMed PMC
Li Y, Chen S, Shan Z, Bi L, Yu S, Li Y, Xu S (2017a) miR-182-5p improves the viability, mitosis, migration, and invasion ability of human gastric cancer cells by down-regulating RAB27A. Biosci Rep 37:BSR20170136 PubMed PMC
Li W, Yang W, Liu Y, Chen S, Chin S, Qi X, Zhao Y, Liu H, Wang J, Mei X, Huang P, Xu D (2017b) MicroRNA-378 enhances inhibitory effect of curcumin on glioblastoma. Oncotarget 8:73938–73946 PubMed PMC
Li M, Yang Y, Kuang Y, Gan X, Zeng W, Liu Y, Guan H (2017c) miR-365 induces hepatocellular carcinoma cell apoptosis through targeting Bcl-2. Exp Ther Med 13:2279–2285 PubMed PMC
Li Y, Domina A, Lim G, Chang T, Zhang T (2018a) Evaluation of curcumin, a natural product in turmeric, on Burkitt lymphoma and acute myeloid leukemia cancer stem cell markers. Future Oncol 14:2353–2360 PubMed
Li X, Zhao Z, Li M, Liu M, Bahena A, Zhang Y, Zhang Y, Nambiar C, Liu G (2018b) Sulforaphane promotes apoptosis, and inhibits proliferation and self-renewal of nasopharyngeal cancer cells by targeting STAT signal through miRNA-124-3p. Biomed Pharmacother 103:473–481 PubMed
Lima RT, Busacca S, Almeida GM, Gaudino G, Fennell DA, Vasconcelos MH (2011) MicroRNA regulation of core apoptosis pathways in cancer. Eur J Cancer 47:163–174 PubMed
Lin S, Gregory RI (2015) MicroRNA biogenesis pathways in cancer. Nat Rev Cancer 15:321–333 PubMed PMC
Liu L, Yu X, Guo X, Tian Z, Su M, Long Y, Huang C, Zhou F, Liu M, Wu X et al (2012) miR-143 is downregulated in cervical cancer and promotes apoptosis and inhibits tumor formation by targeting Bcl-2. Mol Med Rep 5:753–760 PubMed
Liu ZL, Wang H, Liu J, Wang ZX (2013) MicroRNA-21 (miR-21) expression promotes growth, metastasis, and chemo- or radioresistance in non-small cell lung cancer cells by targeting PTEN. Mol Cell Biochem 372:35–45 PubMed
Liu Z, Tu K, Liu Q (2014) Effects of microRNA-30a on migration, invasion and prognosis of hepatocellular carcinoma. FEBS Lett 588:3089–3097 PubMed
Liu J, Meng T, Yuan M, Wen L, Cheng B, Liu N, Huang X, Hong Y, Yuan H, Hu F (2016) MicroRNA-200c delivered by solid lipid nanoparticles enhances the effect of paclitaxel on breast cancer stem cell. Int J Nanomed 11:6713–6725 PubMed PMC
Lopez-Camarillo C, Marchat LA, Arechaga-Ocampo E, Perez-Plasencia C, Del Moral-Hernandez O, Castaneda-Ortiz EJ, Rodriguez-Cuevas S (2012) MetastamiRs: non-coding MicroRNAs driving cancer invasion and metastasis. Int J Mol Sci 13:1347–1379 PubMed PMC
Lu Y, Qin T, Li J, Wang L, Zhang Q, Jiang Z, Mao J (2017) MicroRNA-140-5p inhibits invasion and angiogenesis through targeting VEGF-A in breast cancer. Cancer Gene Ther 24:386–392 PubMed PMC
Macfarlane LA, Murphy PR (2010) MicroRNA: biogenesis, function and role in cancer. Curr Genom 11:537–561 PubMed PMC
Martin del Campo SE, Latchana N, Levine KM, Grignol VP, Fairchild ET, Jaime-Ramirez AC, Dao TV, Karpa VI, Carson M, Ganju A et al (2015) MiR-21 enhances melanoma invasiveness via inhibition of tissue inhibitor of metalloproteinases 3 expression: in vivo effects of MiR-21 inhibitor. PLoS One 10:e0115919 PubMed PMC
McGuire A, Brown JA, Kerin MJ (2015) Metastatic breast cancer: the potential of miRNA for diagnosis and treatment monitoring. Cancer Metastasis Rev 34:145–155 PubMed PMC
Mehrgou A, Akouchekian M (2017) Therapeutic impacts of microRNAs in breast cancer by their roles in regulating processes involved in this disease. J Res Med Sci 22:130 PubMed PMC
Morales S, Monzo M, Navarro A (2017) Epigenetic regulation mechanisms of microRNA expression. Biomol Concepts 8:203–212 PubMed
Munagala R, Aqil F, Vadhanam MV, Gupta RC (2013) MicroRNA ‘signature’ during estrogen-mediated mammary carcinogenesis and its reversal by ellagic acid intervention. Cancer Lett 339:175–184 PubMed PMC
Nakanishi K (2016) Anatomy of RISC: how do small RNAs and chaperones activate Argonaute proteins? Wiley Interdiscip Rev RNA 7:637–660 PubMed PMC
O’Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne) 9:402 PubMed PMC
Oliveto S, Mancino M, Manfrini N, Biffo S (2017) Role of microRNAs in translation regulation and cancer. World J Biol Chem 8:45–56 PubMed PMC
Otsuka K, Yamamoto Y, Ochiya T (2018) Regulatory role of resveratrol, a microRNA-controlling compound, in PubMed PMC
Pan Z, Zhang M, Ma T, Xue ZY, Li GF, Hao LY, Cao JL (2016) Hydroxymethylation of microRNA-365-3p regulates nociceptive behaviors via Kcnh2. J Neurosci 36:2769–2781 PubMed PMC
Pan JH, Abernathy B, Kim YJ, Lee JH, Kim JH, Shin EC, Kim JK (2017) Cruciferous vegetables and colorectal cancer prevention through microRNA regulation: a review. Crit Rev Food Sci Nutr 58:2026–2038 PubMed
Pang L, Li B, Zheng B, Niu L, Ge L (2017) miR-138 inhibits gastric cancer growth by suppressing SOX4. Oncol Rep 38:1295–1302 PubMed
Pasculli B, Barbano R, Parrella P (2018) Epigenetics of breast cancer: biology and clinical implication in the era of precision medicine. Semin Cancer Biol 51:22–35 PubMed
Patafio FM, Brooks SC, Wei X, Peng Y, Biagi J, Booth CM (2016) Research output and the public health burden of cancer: is there any relationship? Curr Oncol 23:75–80 PubMed PMC
Peschansky VJ, Wahlestedt C (2014) Non-coding RNAs as direct and indirect modulators of epigenetic regulation. Epigenetics 9:3–12 PubMed PMC
Qadir MI, Faheem A (2017) miRNA: a diagnostic and therapeutic tool for pancreatic cancer. Crit Rev Eukaryot Gene Expr 27:197–204 PubMed
Qin W, Zhang K, Clarke K, Weiland T, Sauter ER (2014) Methylation and miRNA effects of resveratrol on mammary tumors vs. normal tissue. Nutr Cancer 66:270–277 PubMed
Qu J, Li M, An J, Zhao B, Zhong W, Gu Q, Cao L, Yang H, Hu C (2015) MicroRNA-33b inhibits lung adenocarcinoma cell growth, invasion, and epithelial-mesenchymal transition by suppressing Wnt/β-catenin/ZEB1 signaling. Int J Oncol 47:2141–2152 PubMed
Razumilava N, Bronk SF, Smoot RL, Fingas CD, Werneburg NW, Roberts LR, Mott JL (2012) miR-25 targets TNF-related apoptosis inducing ligand (TRAIL) death receptor-4 and promotes apoptosis resistance in cholangiocarcinoma. Hepatology 55:465–475 PubMed PMC
Remenyi J, Bajan S, Fuller-Pace FV, Arthur JSC, Hutvagner G (2016) The loop structure and the RNA helicase p72/DDX17 influence the processing efficiency of the mice miR-132. Sci Rep 6:22848 PubMed PMC
Rhodes LV, Martin EC, Segar HC, Miller DF, Buechlein A, Rusch DB, Nephew KP, Burow ME, Collins-Burow BM (2015) Dual regulation by microRNA-200b-3p and microRNA-200b-5p in the inhibition of epithelial-to-mesenchymal transition in triple-negative breast cancer. Oncotarget 6:16638–16652 PubMed PMC
Rigalli JP, Tocchetti GN, Arana MR, Villanueva SS, Catania VA, Theile D, Ruiz ML, Weiss J (2016) The phytoestrogen genistein enhances multidrug resistance in breast cancer cell lines by translational regulation of ABC transporters. Cancer Lett 376:165–172 PubMed
Rokavec M, Li H, Jiang L, Hermeking H (2014) The p53/miR-34 axis in development and disease. J Mol Cell Biol 6:214–230 PubMed
Roscigno G, Puoti I, Giordano I, Donnarumma E, Russo V, Affinito A, Adamo A, Quintavalle C, Todaro M, Vivanco MD et al (2017) MiR-24 induces chemotherapy resistance and hypoxic advantage in breast cancer. Oncotarget 8:19507–19521 PubMed PMC
Ross SA, Davis CD (2014) The emerging role of microRNAs and nutrition in modulating health and disease. Annu Rev Nutr 34:305–336 PubMed
Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16:203–222 PubMed
Sayeed A, Bracci M, Lazzarini R, Tomasetti M, Amati M, Lucarini G, Di Primio R, Santarelli L (2017) Use of potential dietary phytochemicals to target miRNA: promising option for breast cancer prevention and treatment? J Funct Foods 28:177–193
Setijono SR, Park M, Kim G, Kim Y, Cho KW, Song SJ (2018) miR-218 and miR-129 regulate breast cancer progression by targeting Lamins. Biochem Biophys Res Commun 496:826–833 PubMed
Shah MY, Ferrajoli A, Sood AK, Lopez-Berestein G, Calin GA (2016) microRNA therapeutics in cancer—an emerging concept. EBioMedicine 12:34–42 PubMed PMC
Shen G, Li X, Jia YF, Piazza GA, Xi Y (2013) Hypoxia-regulated microRNAs in human cancer. Acta Pharmacol Sin 34:336–341 PubMed PMC
Shi W, Bruce J, Lee M, Yue S, Rowe M, Pintilie M, Kogo R, Bissey PA, Fyles A, Yip KW et al (2016) MiR-449a promotes breast cancer progression by targeting CRIP2. Oncotarget 7:18906–18918 PubMed PMC
Slaby O, Sachlova M, Brezkova V, Hezova R, Kovarikova A, Bischofová S, Sevcikova S, Bienertova-Vasku J, Vasku A, Svoboda M et al (2013) Identification of microRNAs regulated by isothiocyanates and association of polymorphisms inside their target sites with risk of sporadic colorectal cancer. Nutr Cancer 65:247–254 PubMed
Song J, Shao Q, Li C, Liu H, Li J, Wang Y, Song W, Li L, Wang G, Shao Z et al (2017) Effects of microRNA-21 on apoptosis by regulating the expression of PTEN in diffuse large B-cell lymphoma. Medicine 96:e7952 PubMed PMC
Spagnuolo C, Russo GL, Orhan IE, Habtemariam S, Daglia M, Sureda A, Nabavi SF, Devi KP, Loizzo MR, Tundis R et al (2015) Genistein and cancer: current status, challenges, and future directions. Adv Nutr 6:408–419 PubMed PMC
Srivastava SK, Arora S, Averett C, Singh S, Singh AP (2015) Modulation of microRNAs by phytochemicals in cancer: underlying mechanisms and translational significance. Biomed Res Int 2015:848710 PubMed PMC
Takahashi RU, Miyazaki H, Ochiya T (2015) The roles of MicroRNAs in breast cancer. Cancers (Basel) 7:598–616 PubMed PMC
Tan W, Liu B, Qu S, Liang G, Luo W, Gong C (2017) MicroRNAs and cancer: key paradigms in molecular therapy. Oncol Lett 15:2735–2742 PubMed PMC
Tao Z, Shi A, Lu C, Song T, Zhang Z, Zhao J (2015) Breast cancer: epidemiology and etiology. Cell Biochem Biophys 72:333–338 PubMed
Tarallo S, Pardini B, Mancuso G, Rosa F, Di Gaetano C, Rosina F, Vineis P, Naccarati A (2014) MicroRNA expression in relation to different dietary habits: a comparison in stool and plasma samples. Mutagenesis 29:385–391 PubMed
Treiber T, Treiber N, Meister G (2018) Regulation of microRNA biogenesis and its crosstalk with other cellular pathways. Nat Rev Mol Cell Biol 20:5–20 PubMed
Tsai HP, Huang SF, Li CF, Chien HT, Chen SC (2018) Differential microRNA expression in breast cancer with different onset age. PLoS One 13:e0191195 PubMed PMC
Uramova S, Kubatka P, Dankova Z, Kapinova A, Zolakova B, Samec M, Zubor P, Zulli A, Valentova V, Kwon TK et al (2018) Plant natural modulators in breast cancer prevention: status quo and future perspectives reinforced by predictive, preventive, and personalized medical approach. EPMA J 9:403–419 PubMed PMC
Ustianenko D, Chiu HS, Treiber T, Weyn-Vanhentenryck SM, Treiber N, Meister G, Zhang C (2018) LIN28 selectively modulates a subclass of Let-7 MicroRNAs. Mol Cell 71:271–283.e5 PubMed PMC
van Schooneveld E, Wildiers H, Vergote I, Vermeulen PB, Dirix LY, Van Laere SJ (2015) Dysregulation of microRNAs in breast cancer and their potential role as prognostic and predictive biomarkers in patient management. Breast Cancer Res 17:21 PubMed PMC
Varghese E, Samuel SM, Abotaleb M, Cheema S, Mamtani R, Büsselberg D (2018) The “Yin and Yang” of natural compounds in anticancer therapy of triple-negative breast cancers. Cancers (Basel) 10:346 PubMed PMC
Varinska L, Gal P, Mojzisova G, Mirossay L, Mojzis J (2015) Soy and breast cancer: focus on angiogenesis. Int J Mol Sci 16:11728–11749 PubMed PMC
Venkatadri R, Muni T, Iyer AK, Yakisich JS, Azad N (2016) Role of apoptosis-related miRNAs in resveratrol-induced breast cancer cell death. Cell Death Dis 7:e2104 PubMed PMC
Wang W, Ren F, Wu Q, Jiang D, Li H, Shi H (2014a) MicroRNA-497 suppresses angiogenesis by targeting vascular endothelial growth factor A through the PI3 K/AKT and MAPK/ERK pathways in ovarian cancer. Oncol Rep 32:2127–2133 PubMed
Wang X, He H, Lu Y, Ren W, Teng KY, Chiang CL, Yang Z, Yu B, Hsu S, Jacob ST et al (2014b) Indole-3-carbinol inhibits tumorigenicity of hepatocellular carcinoma cells via suppression of microRNA-21 and upregulation of phosphatase and tensin homolog. Biochim Biophys Acta 1853:244–253 PubMed PMC
Wang CZ, Yuan P, Li Y (2015) MiR-126 regulated breast cancer cell invasion by targeting ADAM9. Int J Clin Exp Pathol 8:6547–6553 PubMed PMC
Wang Y, Zeng J, Pan J, Geng X, Liu Y, Wu J, Song P, Wang Y, Jia J, Wang L (2016) MicroRNA-200c is involved in proliferation of gastric cancer by directly repressing p27Kip1. Biochem Biophys Rep 8:227–233 PubMed PMC
Wang DX, Zou YJ, Zhuang XB, Chen SX, Lin Y, Li WL, Lin JJ, Lin ZQ (2017) Sulforaphane suppresses EMT and metastasis in human lung cancer through miR-616-5p-mediated GSK3β/β-catenin signaling pathways. Acta Pharmacol Sin 38:241–251 PubMed PMC
Wang D, Tang L, Wu H, Wang K, Gu D (2018a) MiR-127-3p inhibits cell growth and invasiveness by targeting ITGA6 in human osteosarcoma. IUBMB Life 70:411–419 PubMed
Wang K, Tan SL, Lu Q, Xu R, Cao J, Wu SQ, Wang YH, Zhao XK, Zhong ZH (2018b) Curcumin suppresses microRNA-7641-mediated regulation of p16 expression in bladder cancer. Am J Chin Med 46:1357–1368 PubMed
Wang Y, Wang L, Chen C, Chu X (2018c) New insights into the regulatory role of microRNA in tumor angiogenesis and clinical implications. Mol Cancer 17:22 PubMed PMC
Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, Leedman PJ (2009) Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 284:5731–5741 PubMed
Wei D, Yang L, Lv B, Chen L (2017) Genistein suppresses retinoblastoma cell viability and growth and induces apoptosis by upregulating miR-145 and inhibiting its target ABCE1. Mol Vis 23:385–394 PubMed PMC
Weiss CN, Ito K (2017) A macro view of microRNAs: the discovery of MicroRNAs and their role in hematopoiesis and hematologic disease. Int Rev Cell Mol Biol 334:99–175 PubMed PMC
Wilk G, Braun R (2018) regQTLs: single nucleotide polymorphisms that modulate microRNA regulation of gene expression in tumors. PLoS Genet 14:e1007837 PubMed PMC
Winther M, Alsner J, Sørensen BS, Wittrup CF, Tramm T, Baeksgaard L, Hofland K, Holtved E, Nordsmark M (2016) Hypoxia-regulated MicroRNAs in gastroesophageal cancer. Anticancer Res 36:721–730 PubMed
Wu Y, Song Y, Xiong Y, Wang X, Xu K, Han B, Bai Y, Li L, Zhang Y, Zhou L (2017) MicroRNA-21 (Mir-21) promotes cell growth and invasion by repressing tumor suppressor PTEN in colorectal cancer. Cell Physiol Biochem 43:945–958 PubMed
Xu H, Hu Y, Qiu W (2017) Potential mechanisms of microRNA-129-5p in inhibiting cell processes including viability, proliferation, migration and invasiveness of glioblastoma cells U87 through targeting FNDC3B. Biomed Pharmacother 87:405–411 PubMed
Xu X, Gao F, Wang J, Tao L, Ye J, Ding L, Ji W, Chen X (2018) MiR-122-5p inhibits cell migration and invasion in gastric cancer by down-regulating DUSP4. Cancer Biol Ther 19:427–435 PubMed PMC
Xue X, Liu Y, Wang Y, Meng M, Wang K, Zang X, Zhao S, Sun X, Cui L, Pan L et al (2016) MiR-21 and MiR-155 promote non-small cell lung cancer progression by downregulating SOCS1, SOCS6, and PTEN. Oncotarget 7:84508–84519 PubMed PMC
Yamada S, Tsukamoto S, Huang Y, Makio A, Kumazoe M, Yamashita S, Tachibana H (2016) Epigallocatechin-3-O-gallate up-regulates microRNA-let-7b expression by activating 67-kDa laminin receptor signaling in melanoma cells. Sci Rep 6:19225 PubMed PMC
Yang Y, Zhang J, Xia T, Li G, Tian T, Wang M, Wang R, Zhao L, Yang Y, Lan K et al (2016) MicroRNA-210 promotes cancer angiogenesis by targeting fibroblast growth factor receptor-like 1 in hepatocellular carcinoma. Oncol Rep 36:2553–2562 PubMed
Yang X, Shi L, Yi C, Yang Y, Chang L, Song D (2017) MiR-210-3p inhibits the tumor growth and metastasis of bladder cancer via targeting fibroblast growth factor receptor-like 1. Am J Cancer Res 7:1738–1753 PubMed PMC
Yang H, Zhang H, Ge S, Ning T, Bai M, Li J, Li S, Sun W, Deng T, Zhang L et al (2018) Exosome-derived miR-130a activates angiogenesis in gastric cancer by targeting C-MYB in vascular endothelial cells. Mol Ther 26:2466–2475 PubMed PMC
Yuan JM (2013) Cancer prevention by green tea: evidence from epidemiologic studies. Am J Clin Nutr 98(6 Suppl):1676S–1681S PubMed PMC
Zendehdel E, Abdollahi E, Momtazi-Borojeni AA, Korani M, Alavizadeh SH, Sahebkar A (2018) The molecular mechanisms of curcumin’s inhibitory effects on cancer stem cells. J Cell Biochem 120:4739–4747 PubMed
Zhan Y, Liang X, Li L, Wang B, Ding F, Li Y, Wang X, Zhan Q, Liu Z (2016) MicroRNA-548j functions as a metastasis promoter in human breast cancer by targeting Tensin1. Mol Oncol 10:838–849 PubMed PMC
Zhang Y, Callaway EC (2002) High cellular accumulation of sulphoraphane, a dietary anticarcinogen, is followed by rapid transporter-mediated export as a glutathione conjugate. Biochem J364(Pt 1):301–307 PubMed PMC
Zhang YQ, Wang WY, Xue JX, Xu Y, Fan P, Caughey BA, Tan WW, Cao GQ, Jiang LL, Lu Y et al (2016) Expression profile on solid subtype of invasive lung adenocarcinoma reveals a panel of four miRNAs to be associated with poor prognosis in Chinese patients. J Cancer 7:1610–1620 PubMed PMC
Zhou H, Chen JX, Yang CS, Yang MQ, Deng Y, Wang H (2014) Gene regulation mediated by microRNAs in response to green tea polyphenol EGCG in mouse lung cancer. BMC Genom 15(Suppl 11):S3 PubMed PMC
Zhu J, Ye Q, Chang L, Xiong W, He Q, Li W (2015) Upregulation of miR-195 enhances the radiosensitivity of breast cancer cells through the inhibition of BCL-2. Int J Clin Exp Med 8:9142–9148 PubMed PMC
Zubor P, Kubatka P, Dankova Z, Gondova A, Kajo K, Hatok J, Samec M, Jagelkova M, Krivus S, Holubekova V et al (2018) miRNA in a multiomic context for diagnosis, treatment monitoring and personalized management of metastatic breast cancer. Future Oncol 14:1847–1867 PubMed
Salvia officinalis L. exerts oncostatic effects in rodent and in vitro models of breast carcinoma
Anti-breast cancer effects of phytochemicals: primary, secondary, and tertiary care
Metabolic Anti-Cancer Effects of Melatonin: Clinically Relevant Prospects
The role of plant-derived natural substances as immunomodulatory agents in carcinogenesis