Melatonin down-regulates microRNA-10a and decreases invasion and migration of triple-negative breast cancer cells
Melatonin and microRNA-10a in breast cancer cells
Keywords:
melatonin, microRNAs, epithelial-mesenchymal transition, metastasis, pineal gland, breast neoplasms
Abstract
Breast cancer metastasis is one of the main factors associated with high mortality rates among patients. MicroRNAs (miRNAs) play an important role in gene expression regulation, and are associated with the metastatic process in breast cancer. Melatonin, a hormone secreted mainly in the pineal gland, has several oncostatic effects. The aim of this study was to investigate the action of melatonin in the modulation of miRNA-10a-5p and its association with metastatic mechanisms. We have evaluated the effects of melatonin on cell viability in MDA-MB-468 cell line after 24 hours of treatment. MDA-MB-468 and MDA-MB-231 cells were either transfected with inhibitor of miR-10a, or received a scrambled miRNA sequence as a negative control, then these cells were treated with or without melatonin. Gene expression of miR-10a was verified by real-time PCR. Invasion and migration assay using matrigel inserts were performed. The protein expression was analyzed by western blotting to quantify the epithelial-mesenchymal transition (EMT) markers (E-cadherin, claudin 7, and vimentin) and proliferation marker (PIK3CA). Our results showed that melatonin (1 mM) significantly decreased cell viability, and also affected miR-10a expression, which suppressed cell invasion and migration. Melatonin reduced vimentin and claudin 7 protein expressions, and increased E-cadherin. In contrast, inhibition of miR-10a reduced vimentin and did not modulate claudin 7 and E-cadherin. In conclusion, we demonstrated the effectiveness of melatonin in decreasing miR-10a, affecting invasion and migration, and proteins involved with the EMT process, which supports its potential role in the regulation of metastasis.
References
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41. Hevia D, et al. (2015) Melatonin uptake through glucose transporters: a new target for melatonin inhibition of cancer. J. Pineal Res. 58 (2): 234–250.
42. Sanchez-Barcelo EJ, et al. (2012) Breast cancer therapy based on melatonin. Recent Pat. Endocr. Metab. Immune Drug Discov. 6 (2): 108–116.
43. Mao L, et al. (2014) Molecular deficiency (ies) in MT1 melatonin signaling pathway underlies the melatonin-unresponsive phenotype in MDA-MB-231 human breast cancer cells. J. Pineal Res. 56 (3): 246–253.
44. Jardim-Perassi BV, et al. (2014) Effect of melatonin on tumor growth and angiogenesis in xenograft model of breast cancer. PLoS One 9 (1): 1–11.
45. Ordoñez R, et al. (2015) Ceramide metabolism regulates autophagy and apoptotic cell death induced by melatonin in liver cancer cells. J. Pineal Res. 59 (2): 178–189.
46. Ke K, Lou T (2017) MicroRNA-10a suppresses breast cancer progression via PI3K/Akt/mTOR pathway. Oncol. Lett. 14 (5): 5994–6000.
47. Chang C-H, et al. (2014) The prognostic significance of RUNX2 and miR-10a/10b and their inter-relationship in breast cancer. J. Transl. Med. 12 (1): 257.
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55. Sasayama T, et al. (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int. J. Cancer 125 (6): 1407–1413.
56. Bloomston M, et al. (2007) MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 297 (17): 1901–1908.
57. Tian Y, et al. (2010) MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J. Biol. Chem. 285 (11): 7986–7994.
58. Ma L, et al. (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682–688.
59. Harquail J, et al. (2012) MicroRNAs and breast cancer malignancy: an overview of miRNA-regulated cancer processes leading to metastasis. Cancer Biomark 11 (6): 269–280.
60. Mao L, et al. (2016) Melatonin Represses Metastasis in Her2-Postive Human Breast Cancer Cells by Suppressing RSK2 Expression. Mol. Cancer Res. 14 (11): 1159–1169.
61. Su S-C, et al. (2017) Cancer metastasis: Mechanisms of inhibition by melatonin. J. Pineal Res. 62 (1): e12370.
62. Wu S-M, et al. (2016) Melatonin set out to ER stress signaling thwarts epithelial mesenchymal transition and peritoneal dissemination via calpain-mediated C/EBP β and NF κ B cleavage. J. Pineal Res. 60 (2): 142–154.
63. Angadi P, Kale A (2015) Epithelial-mesenchymal transition - A fundamental mechanism in cancer progression: An overview. Indian J. Heal. Sci. 8 (2): 77.
64. Wang L, et al. (2015) Activation of IL-8 via PI3K/Akt-dependent pathway is involved in leptin-mediated epithelial-mesenchymal transition in human breast cancer cells. Cancer Biol. Ther. 16 (8): 1220–1230.
65. Jääskeläinen A, et al. (2018) High-level cytoplasmic claudin 3 expression is an independent predictor of poor survival in triple-negative breast cancer. BMC Cancer 18 (1): 223.
66. Lu S, et al. (2013) Claudin expression in high-grade invasive ductal carcinoma of the breast: correlation with the molecular subtype. Mod. Pathol. 26 (4): 485–495.
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2. Chaffer CL, Weinberg RA (2011) A perspective on cancer cell metastasis. Science 331 (6024): 1559–1564.
3. Chen W, et al. (2018) Organotropism: new insights into molecular mechanisms of breast cancer metastasis. NPJ Precis Oncol. 2 (1): 4.
4. Burton R, Bell R (2013) The global challenge of reducing breast cancer mortality. Oncologist 18 (11): 1200–1202.
5. Guan X (2015) Cancer metastases: challenges and opportunities. Acta Pharm. Sin. B 5 (5): 402–418.
6. Scully OJ, et al. (2012) Breast cancer metastasis. Cancer Genomics Proteomics 9 (5): 311–320.
7. Wu Y, et al. (2016) Epithelial-Mesenchymal Transition and Breast Cancer. J. Clin. Med. 5 (2): pii: E13. doi:10.3390/jcm5020013.
8. Hugo H, et al. (2007) Epithelial—mesenchymal and mesenchymal—epithelial transitions in carcinoma progression. J. Cell Physiol. 213 (2): 374–383.
9. Korpal M, et al. (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 (22): 14910–14914.
10. Zhang H, et al. (2010) The microRNA network and tumor metastasis. Oncogene 29 (7): 937–948.
11. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2): 281–297.
12. Iorio MV, et al. (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65 (16): 7065–7070.
13. Iorio MV, Croce CM (2012) MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med. 4 (3): 143–159.
14. Hemmatzadeh M, et al. (2016) The role of oncomirs in the pathogenesis and treatment of breast cancer. Biomed. Pharmacother. 78: 129–139.
15. Badr M, et al. (2019) MicroRNA-21 as a predictor and prognostic factor for trastuzumab therapy in human epidermal growth factor receptor 2-positive metastatic breast cancer. J. Cell Biochem. 120 (3): 3459-3466. doi: 10.1002/jcb.27620.
16. Wang W, Luo Y (2015) MicroRNAs in breast cancer: oncogene and tumor suppressors with clinical potential. J. Zhejiang Univ. Sci. B 16 (1): 18–31.
17. Ma L, et al. (2010) Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat. Biotechnol. 28 (4): 341-7 doi:10.1038/nbt.1618.
18. Tehler D, et al. (2011) The miR-10 microRNA precursor family. RNA Biol. 8 (5): 728–734.
19. Wheeler BM, et al. (2009) The deep evolution of metazoan microRNAs. Evol. Dev. 11 (1): 50–68.
20. Talib WH (2018) Melatonin and cancer hallmarks. Molecules 23 (3): 518.
21. González-González A, et al. (2018) Melatonin: a molecule for reducing breast cancer risk. Molecules 23 (2): 336.
22. Borin TF, et al. (2016) Melatonin decreases breast cancer metastasis by modulating Rho-associated kinase protein-1 expression. J. Pineal Res. 60 (1): 3–15.
23. Ortíz-López L, et al. (2009) ROCK-regulated cytoskeletal dynamics participate in the inhibitory effect of melatonin on cancer cell migration. J. Pineal Res. 46 (1): 15–21.
24. Hill SM, Blask DE (1988) Effects of the pineal hormone melatonin on the proliferation and morphological characteristics of human breast cancer cells (MCF-7) in culture. Cancer Res. 48 (21): 6121–6126.
25. Nooshinfar E, et al. (2016) Melatonin promotes ATO-induced apoptosis in MCF-7 cells: Proposing novel therapeutic potential for breast cancer. Biomed. Pharmacother. 83: 456–465.
26. Lee SE, et al. (2011) MicroRNA and gene expression analysis of melatonin-exposed human breast cancer cell lines indicating involvement of the anticancer effect. J. Pineal Res. 51 (3): 345–352.
27. Mori F, et al. (2016) Multitargeting activity of miR-24 inhibits long-term melatonin anticancer effects. Oncotarget 7 (15): doi:10.18632/oncotarget.7978.
28. Marques JHM, et al. (2018) Melatonin restrains angiogenic factors in triple-negative breast cancer by targeting miR-152-3p: In vivo and in vitro studies. Life Sci. 208: 131-138. doi:10.1016/J.LFS.2018.07.012.
29. Zhu C, Huang Q, Zhu H (2018) Melatonin Inhibits the Proliferation of Gastric Cancer Cells Through Regulating the miR-16-5p-Smad3 Pathway. DNA Cell Biol. 37 (3): 244–252.
30. Gu J, et al. (2017) Melatonin inhibits proliferation and invasion via repression of miRNA-155 in glioma cells. Biomed. Pharmacother. 93: 969–975.
31. Kim SJ, et al. (2015) Melatonin ameliorates ER stress-mediated hepatic steatosis through miR-23a in the liver. Biochem. Biophys. Res. Commun. 458 (3): 462–469.
32. Sohn EJ, et al. (2015) Upregulation of miRNA3195 and miRNA374b mediates the anti-angiogenic properties of melatonin in hypoxic PC-3 prostate cancer cells. J. Cancer 6 (1): 19–28.
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25 (4): 402-408. doi:10.1006/meth.2001.1262.
34. Reiter R, et al. (2017) Melatonin, a Full service anti-cancer agent: inhibition of initiation, progression and metastasis. Int. J. Mol. Sci. 18 (4): 843.
35. Lissoni P, et al. (1999) Decreased toxicity and increased efficacy of cancer chemotherapy using the pineal hormone melatonin in metastatic solid tumour patients with poor clinical status. Eur. J. Cancer 35 (12): 1688–1692.
36. Hill SM, et al. (2015) Melatonin: An inhibitor of breast cancer. Endocr. Relat. Cancer 22 (3): R183–R204.
37. Jardim-Perassi BV, et al. (2016) Melatonin regulates angiogenic factors under hypoxia in breast cancer cell lines. Anticancer Agents Med. Chem. 16 (3): 347–358.
38. Maschio-Signorini LB, et al. (2016) Melatonin regulates angiogenic and inflammatory proteins in MDA-MB-231 cell line and in co-culture with cancer-associated fibroblasts. Anticancer Agents Med. Chem. 16 (11): 1474–1484.
39. Colombo JF, et al. (2018) Melatonin differentially modulates NF-КB expression in breast and liver cancer cells. Anticancer Agents Med. Chem 18 (12): 1688-1694. doi:10.2174/1871520618666180131112304.
40. Gonçalves NN, et al. (2016) Effect of melatonin in epithelial mesenchymal transition markers and invasive properties of breast cancer stem cells of canine and human cell lines. PLoS One 11 (3): e0150407.
41. Hevia D, et al. (2015) Melatonin uptake through glucose transporters: a new target for melatonin inhibition of cancer. J. Pineal Res. 58 (2): 234–250.
42. Sanchez-Barcelo EJ, et al. (2012) Breast cancer therapy based on melatonin. Recent Pat. Endocr. Metab. Immune Drug Discov. 6 (2): 108–116.
43. Mao L, et al. (2014) Molecular deficiency (ies) in MT1 melatonin signaling pathway underlies the melatonin-unresponsive phenotype in MDA-MB-231 human breast cancer cells. J. Pineal Res. 56 (3): 246–253.
44. Jardim-Perassi BV, et al. (2014) Effect of melatonin on tumor growth and angiogenesis in xenograft model of breast cancer. PLoS One 9 (1): 1–11.
45. Ordoñez R, et al. (2015) Ceramide metabolism regulates autophagy and apoptotic cell death induced by melatonin in liver cancer cells. J. Pineal Res. 59 (2): 178–189.
46. Ke K, Lou T (2017) MicroRNA-10a suppresses breast cancer progression via PI3K/Akt/mTOR pathway. Oncol. Lett. 14 (5): 5994–6000.
47. Chang C-H, et al. (2014) The prognostic significance of RUNX2 and miR-10a/10b and their inter-relationship in breast cancer. J. Transl. Med. 12 (1): 257.
48. CHEN W, et al. (2012) miRNA expression profile in primary gastric cancers and paired lymph node metastases indicates that miR-10a plays a role in metastasis from primary gastric cancer to lymph nodes. Exp. Ther. Med. 3 (2): 351–356.
49. Weiss FU, et al. (2009) Retinoic Acid Receptor Antagonists Inhibit miR-10a Expression and Block Metastatic Behavior of Pancreatic Cancer. Gastroenterology 137 (6): 2136–2145.e7.
50. Khan S, et al. (2015) MicroRNA-10a is reduced in breast cancer and regulated in part through retinoic acid. BMC Cancer 15 (1): 345.
51. Hoppe R, et al. (2013) Increased expression of miR-126 and miR-10a predict prolonged relapse-free time of primary oestrogen receptor-positive breast cancer following tamoxifen treatment. Eur. J. Cancer 49 (17): 3598–3608.
52. Pérez-Rivas LG, et al. (2014) A microRNA Signature Associated with Early Recurrence in Breast Cancer. PLoS One 9 (3): e91884.
53. Pogribny IP, et al. (2010) Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin. Int. J. Cancer 127 (8): 1785–1794.
54. Ørom UA, et al. (2008) MicroRNA-10a binds the 5’UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 30 (4): 460–471.
55. Sasayama T, et al. (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int. J. Cancer 125 (6): 1407–1413.
56. Bloomston M, et al. (2007) MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 297 (17): 1901–1908.
57. Tian Y, et al. (2010) MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J. Biol. Chem. 285 (11): 7986–7994.
58. Ma L, et al. (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682–688.
59. Harquail J, et al. (2012) MicroRNAs and breast cancer malignancy: an overview of miRNA-regulated cancer processes leading to metastasis. Cancer Biomark 11 (6): 269–280.
60. Mao L, et al. (2016) Melatonin Represses Metastasis in Her2-Postive Human Breast Cancer Cells by Suppressing RSK2 Expression. Mol. Cancer Res. 14 (11): 1159–1169.
61. Su S-C, et al. (2017) Cancer metastasis: Mechanisms of inhibition by melatonin. J. Pineal Res. 62 (1): e12370.
62. Wu S-M, et al. (2016) Melatonin set out to ER stress signaling thwarts epithelial mesenchymal transition and peritoneal dissemination via calpain-mediated C/EBP β and NF κ B cleavage. J. Pineal Res. 60 (2): 142–154.
63. Angadi P, Kale A (2015) Epithelial-mesenchymal transition - A fundamental mechanism in cancer progression: An overview. Indian J. Heal. Sci. 8 (2): 77.
64. Wang L, et al. (2015) Activation of IL-8 via PI3K/Akt-dependent pathway is involved in leptin-mediated epithelial-mesenchymal transition in human breast cancer cells. Cancer Biol. Ther. 16 (8): 1220–1230.
65. Jääskeläinen A, et al. (2018) High-level cytoplasmic claudin 3 expression is an independent predictor of poor survival in triple-negative breast cancer. BMC Cancer 18 (1): 223.
66. Lu S, et al. (2013) Claudin expression in high-grade invasive ductal carcinoma of the breast: correlation with the molecular subtype. Mod. Pathol. 26 (4): 485–495.
67. Constantinou C, et al. (2018) Expression and clinical significance of claudin-7, PDL-1, PTEN, c-Kit, c-Met, c-Myc, ALK, CK5/6, CK17, p53, EGFR, Ki67, p63 in triple-negative breast cancer-a single centre prospective observational study. In Vivo 32 (2): 303–311.
68. Renner O, et al. (2008) Activation of phosphatidylinositol 3-kinase by membrane localization of p110alpha predisposes mammary glands to neoplastic transformation. Cancer Res. 68 (23): 9643–9653.
69. Kamal A, et al. (2016) Benzo[b]furan derivatives induces apoptosis by targeting the PI3K/Akt/mTOR signaling pathway in human breast cancer cells. Bioorg. Chem. 66: 124–131.
Published
2019-06-12
How to Cite
[1]
Oliveira, J., Marques, J., Lacerda, J., Ferreira, L., Coelho, M. and Zuccari, D. 2019. Melatonin down-regulates microRNA-10a and decreases invasion and migration of triple-negative breast cancer cells. Melatonin Research. 2, 2 (Jun. 2019), 86-99. DOI:https://doi.org/https://doi.org/10.32794/mr11250023.
Section
Research Articles
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