Inhibition of Interleukin-6-Induced Matrix Metalloproteinase-2 Expression and Invasive Ability of Lemon Peel Polyphenol Extract in Human Primary Colon Cancer Cells
Abstract
:1. Introduction
2. Results
2.1. The LPE Pretreatment Reduces the rIL-6-Induced Migration and Invasiveness of Human Primary T88 and T93 Colon Cancer Cells
2.2. The LPE Pretreatment Reduces the rIL-6-Induced Up-Regulation of MMP-2 Activity and mRNA Expression Levels in T88 and T93 Cells
2.3. The LPE Pretreatment Inhibits the rIL-6-Dependent STAT3 Phosphorylation Levels in T88 and T93 Cells
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Cell Cultures and Treatments
4.3. Wound Assay
4.4. Matrigel Invasion Assay
4.5. RNA Extraction, Reverse Transcription (RT), and Quantitative Real-Time Polymerase Chain Reaction (qPCR)
4.6. Western Blotting Analysis
4.7. Gelatin Zymography
4.8. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Sample Availability
References
- Macrae, F.A. Colorectal Cancer: Epidemiology, Risk Factors, and Protective Factors. Available online: https://www.uptodate.com/contents/colorectal-cancer-epidemiology-risk-factors-and-protective-factors (accessed on 24 May 2021).
- Thanikachalam, K.; Khan, G. Colorectal Cancer and Nutrition. Nutrients 2019, 11, 164. [Google Scholar] [CrossRef] [Green Version]
- De Rosa, M.; Rega, D.; Costabile, V.; Duraturo, F.; Niglio, A.; Izzo, P.; Pace, U.; Delrio, P. The biological complexity of colorectal cancer: Insights into biomarkers for early detection and personalized care. Ther. Adv. Gastroenterol. 2016, 9, 861–886. [Google Scholar] [CrossRef] [Green Version]
- Jabłońska-Trypuć, A.; Matejczyk, M.; Rosochacki, S. Matrix metalloproteinases (MMPs), the main extracellular matrix (ECM) enzymes in collagen degradation, as a target for anticancer drugs. J. Enzyme Inhib. Med. Chem. 2016, 31, 177–183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cui, N.; Hu, M.; Khalil, R.A. Biochemical and Biological Attributes of Matrix Metalloproteinases. Prog. Mol. Biol. Transl. Sci. 2017, 147, 1–73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sier, C.F.; Kubben, F.J.; Ganesh, S.; Heerding, M.M.; Griffioen, G.; Hanemaaijer, R.; van Krieken, J.H.; Lamers, C.B.; Verspaget, H.W. Tissue levels of matrix metalloproteinases MMP-2 and MMP-9 are related to the overall survival of patients with gastric carcinoma. Br. J. Cancer 1996, 74, 413–417. [Google Scholar] [CrossRef] [Green Version]
- Pagliara, V.; Adornetto, A.; Mammì, M.; Masullo, M.; Sarnataro, D.; Pietropaolo, C.; Arcone, R. Protease Nexin-1 affects migration and invasion of C6 glioma cells through regulation of urokinase Plasminogen Activator and Matrix Metalloprotease-9/2. Biochim. Biophys. Acta 2014, 26, 2631–2644. [Google Scholar] [CrossRef]
- Yang, T.; Zhang, J.; Zhou, J.; Zhu, M.; Wang, L.; Yan, L. Resveratrol inhibits Interleukin-6 induced invasion of human gastric cancer cells. Biomed. Pharmacother. 2018, 99, 766–773. [Google Scholar] [CrossRef]
- Shiozaki, A.; Shimizu, H.; Ichikawa, D.; Konishi, H.; Komatsu, S.; Kubota, T.; Fujiwara, H.; Okamoto, K.; Iitaka, D.; Nakashima, S.; et al. Claudin 1 mediates tumor necrosis factor alpha-induced cell migration in human gastric cancer cells. World J. Gastroenterol. 2014, 21, 17863–17876. [Google Scholar] [CrossRef]
- Vainer, N.; Dehlendorff, C.; Johansen, J.S. Systematic literature review of IL-6 as a biomarker or treatment target in patients with gastric, bile duct, pancreatic and colorectal cancer. Oncotarget 2018, 9, 29820–29841. [Google Scholar] [CrossRef] [Green Version]
- Kossakowska, A.E.; Edwards, D.R.; Prusinkiewicz, C.; Zhang, M.C.; Guo, D.; Urbanski, S.J.; Grogan, T.; Marquez, L.A.; Janowska-Wieczorek, A. Interleukin-6 regulation of matrix metalloproteinase (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMP-1) expression in malignant non-Hodgkin’s lymphomas. Blood 1999, 15, 2080–2089. [Google Scholar] [CrossRef]
- Wang, Y.; Li, L.; Guo, X.; Jin, X.; Sun, W.; Zhang, X.; Xu, R.C. Interleukin-6 signaling regulates anchorage-independent growth, proliferation, adhesion and invasion in human ovarian cancer cells. Cytokine 2012, 59, 228–236. [Google Scholar] [CrossRef]
- Wang, X.; Lee, S.O.; Xia, S.; Jiang, Q.; Luo, J.; Li, L.; Yeh, S.; Chang, C. Endothelial cells enhance prostate cancer metastasis via IL-6→androgen receptor→TGF-β→MMP-9 signals. Mol. Cancer Ther. 2013, 12, 1026–1037. [Google Scholar] [CrossRef] [Green Version]
- Castellana, B.; Aasen, T.; Moreno-Bueno, G.; Dunn, S.E.; Ramón y Caja, S. Interplay between YB-1 and IL-6 promotes the metastatic phenotype in breast cancer cells. Oncotarget 2015, 6, 38239–38256. [Google Scholar] [CrossRef]
- Ashizawa, T.; Okada, R.; Suzuki, Y.; Takagi, M.; Yamazaki, T.; Sumi, T.; Aoki, T.; Ohnuma, S.; Aoki, T. Clinical significance of interleukin-6 (IL-6) in the spread of gastric cancer: Role of IL-6 as a prognostic factor. Gastric Cancer 2005, 8, 124–131. [Google Scholar] [CrossRef] [Green Version]
- Taniguchi, K.; Karin, M. IL-6 and related cytokines as the critical lynchpins between inflammation and cancer. Semin. Immunol. 2014, 26, 54–74. [Google Scholar] [CrossRef]
- Turano, M.; Cammarota, F.; Duraturo, F.; Izzo, P.; De Rosa, M. A Potential Role of IL-6/IL-6R in the Development and Management of Colon Cancer. Membranes 2021, 24, 312. [Google Scholar] [CrossRef]
- Pagliara, V.; Parafati, M.; Adornetto, A.; White, M.C.; Masullo, M.; Grimaldi, M.; Arcone, R. Dibutyryl cAMP- or Interleukin-6-induced astrocytic differentiation enhances mannose binding lectin (MBL)-associated serine protease (MASP)-1/3 expression in C6 glioma cells. Arch. Biochem. Biophys. 2018, 653, 39–49. [Google Scholar] [CrossRef]
- Hirano, T.; Ishihara, K.; Hibi, M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 2000, 19, 2548–2556. [Google Scholar] [CrossRef]
- Luo, J.; Yan, R.; He, X.; He, J. Constitutive activation of STAT3 and cyclin D1 overexpression contribute to proliferation, migration and invasion in gastric cancer cells. Am. J. Transl. Res. 2017, 9, 5671–5677. [Google Scholar]
- Johnson, D.E.; O’Keefe, R.A.; Grandis, J.R. Targeting the IL-6/JAK/STAT3 signalling axis in cancer. Nat. Rev. Clin. Oncol. 2018, 15, 234–248. [Google Scholar] [CrossRef]
- Wang, C.; Wu, W.K.; Liu, X.; To, K.F.; Chen, G.G.; Yu, J.; Ng, E.K. Increased serum chemerin level promotes cellular invasiveness in gastric cancer: A clinical and experimental study. Peptides 2014, 51, 131–138. [Google Scholar] [CrossRef]
- Zhao, G.; Zhu, G.; Huang, Y.; Zheng, W.; Hua, J.; Yang, S.; Zhuang, J.; Ye, J. IL-6 mediates the signal pathway of JAK-STAT3-VEGF-C promoting growth, invasion and lymphangiogenesis in gastric cancer. Oncol. Rep. 2016, 35, 1787–1795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pagliara, V.; Nasso, R.; Di Donato, P.; Finore, I.; Poli, A.; Masullo, M.; Arcone, R. Lemon Peel Polyphenol Extract Reduces Interleukin-6-Induced Cell Migration, Invasiveness, and Matrix Metalloproteinase-9/2 Expression in Human Gastric Adenocarcinoma MKN-28 and AGS Cell Lines. Biomolecules 2019, 9, 833. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nistal, E.; Fernández-Fernández, N.; Vivas, S.; Olcoz, J.L. Factors determining colorectal cancer: The role of the intestinal microbiota. Front. Oncol. 2015, 5, 220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arcone, R.; Palma, M.; Pagliara, V.; Graziani, G.; Masullo, M.; Nardone, G. Green tea polyphenols affect invasiveness of human gastric MKN-28 cells by inhibition of LPS or TNF-α induced Matrix Metalloproteinase-9/2. Biochim. Open 2016, 3, 56–63. [Google Scholar] [CrossRef] [PubMed]
- Fresco, P.; Borges, F.; Diniz, C.; Marques, M.P. New insights on the anticancer properties of dietary polyphenols. Med. Res. Rev. 2006, 26, 747–766. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Donato, P.; Taurisano, V.; Tommonaro, G.; Pasquale, V.; Jiménez, J.M.S.; de Pascual, S.; Poli, T.A.; Nicolaus, B. Biological Properties of Polyphenols Extracts from Agro Industry’s Wastes. Waste Biomass Valorization 2018, 9, 1567–1578. [Google Scholar] [CrossRef]
- Nasso, R.; Pagliara, V.; D’Angelo, S.; Rullo, R.; Masullo, M.; Arcone, R. Annurca Apple Polyphenol Extract Affects Acetyl- Cholinesterase and Mono-Amine Oxidase In Vitro Enzyme Activity. Pharmaceuticals 2021, 14, 62. [Google Scholar] [CrossRef]
- Turano, M.; Costabile, V.; Cerasuolo, A.; Duraturo, F.; Liccardo, R.; Delrio, P.; Pace, U.; Rega, D.; Dodaro, C.A.; Milone, M.; et al. Characterisation of mesenchymal colon tumour-derived cells in tumourspheres as a model for colorectal cancer progression. Int. J. Oncol. 2018, 53, 2379–2396. [Google Scholar] [CrossRef] [Green Version]
- Cammarota, F.; Conte, A.; Aversano, A.; Muto, P.; Ametrano, G.; Riccio, P.; Turano, M.; Valente, V.; Delrio, P.; Izzo, P.; et al. Lithium chloride increases sensitivity to photon irradiation treatment in primary mesenchymal colon cancer cells. Mol. Med. Rep. 2020, 3, 1501–1508. [Google Scholar] [CrossRef] [Green Version]
- Costabile, V.; Duraturo, F.; Delrio, P.; Rega, D.; Pace, U.; Liccardo, R.; Rossi, G.B.; Genesio, R.; Nitsch, L.; Izzo, P.; et al. Lithium chloride induces mesenchymal-to-epithelial reverting transition in primary colon cancer cell cultures. Int. J. Oncol. 2015, 46, 1913–1923. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, M.T.; Lin, B.R.; Chang, C.C.; Chu, C.Y.; Su, H.J.; Chen, S.T.; Jeng, Y.M.; Kuo, M.L. IL-6 induces AGS gastric cancer cell invasion via activation of the c-Src/RhoA/ROCK signaling pathway. Int. J. Cancer 2007, 120, 2600–2608. [Google Scholar] [CrossRef] [PubMed]
- Parsons, S.L.; Watson, S.A.; Collins, H.M.; Griffin, N.R.; Clarke, P.A.; Steele, R.J. Gelatinase (MMP-2 and -9) expression in gastrointestinal malignancy. Br. J. Cancer 1998, 78, 1495–1502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, D.; Li, H.; Zhang, Y.; Yang, H.; Guo, M.; Li, L.; Liu, T. Matrix metalloproteinase 2 promotes cell growth and invasion in colorectal cancer. Acta Biochim. Biophys. Sin. 2011, 43, 840–848. [Google Scholar] [CrossRef] [Green Version]
- Farinetti, A.; Zurlo, V.; Manenti, A.; Coppi, F.; Mattioli, A.V. Mediterranean diet and colorectal cancer: A systematic review. Nutrition 2017, 44, 83–88. [Google Scholar] [CrossRef] [PubMed]
- Fung, T.T.; McCullough, M.L.; Newby, P.K.; Manson, J.E.; Meigs, J.B.; Rifai, N.; Willett, W.C.; Hu, F.B. Diet-quality scores and plasma concentrations of markers of inflammation and endothelial dysfunction. Am. J. Clin. Nutr. 2005, 82, 163–173. [Google Scholar] [CrossRef]
- Nichenametla, S.N.; Taruscio, T.G.; Barney, D.L.; Exon, J.H. A review of the effects and mechanisms of polyphenolics in cancer. Crit. Rev. Food Sci. Nutr. 2006, 46, 161–183. [Google Scholar] [CrossRef] [PubMed]
- Rose-John, S. IL-6 Trans-Signaling via the Soluble IL-6 Receptor: Importance for the Pro-Inflammatory Activities of IL-6. Int. J. Biol. Sci. 2012, 8, 1237–1247. [Google Scholar] [CrossRef]
- Arcone, R.; Pucci, P.; Zappacosta, F.; Fontaine, V.; Malorni, A.; Marino, G.; Ciliberto, G. Single-step purification and structural characterization of human interleukin-6 produced in Escherichia coli from a T7 RNA polymerase expression vector. Eur. J. Biochem. 1991, 198, 541–547. [Google Scholar] [CrossRef]
- Singleton, V.L.; Rossi, J.A. Colorimetry of total phenolics with phosphomolybdic phosphotungstic acid reagents. Am. J. Enol. Viticult. 1965, 16, 144–158. [Google Scholar]
- Tam, J.C.; Lau, K.M.; Liu, C.L.; To, M.H.; Kwok, H.F.; Lai, K.K.; Lau, C.P.; Ko, C.H.; Leung, P.C.; Fung, K.P.; et al. The in vivo and in vitro diabetic wound healing effects of a 2-herb formula and its mechanisms of action. J. Ethnopharmacol. 2011, 134, 831–838. [Google Scholar] [CrossRef] [PubMed]
- Bradford, M.M. A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein dye binding. Ann. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680–685. [Google Scholar] [CrossRef] [PubMed]
- Adornetto, A.; Pagliara, V.; Di Renzo, G.; Arcone, R. Polychlorinated biphenyls impair dibutyryl cAMP-induced astrocytic differentiation in rat C6 glial cell line. FEBS Open Bio 2013, 29, 459–466. [Google Scholar] [CrossRef]
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Pagliara, V.; De Rosa, M.; Di Donato, P.; Nasso, R.; D’Errico, A.; Cammarota, F.; Poli, A.; Masullo, M.; Arcone, R. Inhibition of Interleukin-6-Induced Matrix Metalloproteinase-2 Expression and Invasive Ability of Lemon Peel Polyphenol Extract in Human Primary Colon Cancer Cells. Molecules 2021, 26, 7076. https://doi.org/10.3390/molecules26237076
Pagliara V, De Rosa M, Di Donato P, Nasso R, D’Errico A, Cammarota F, Poli A, Masullo M, Arcone R. Inhibition of Interleukin-6-Induced Matrix Metalloproteinase-2 Expression and Invasive Ability of Lemon Peel Polyphenol Extract in Human Primary Colon Cancer Cells. Molecules. 2021; 26(23):7076. https://doi.org/10.3390/molecules26237076
Chicago/Turabian StylePagliara, Valentina, Marina De Rosa, Paola Di Donato, Rosarita Nasso, Antonio D’Errico, Francesca Cammarota, Annarita Poli, Mariorosario Masullo, and Rosaria Arcone. 2021. "Inhibition of Interleukin-6-Induced Matrix Metalloproteinase-2 Expression and Invasive Ability of Lemon Peel Polyphenol Extract in Human Primary Colon Cancer Cells" Molecules 26, no. 23: 7076. https://doi.org/10.3390/molecules26237076