Myristicin Inhibit Invasion and Migration of Melanoma Cells through Suppression of MMP2 and MMP9 Gene Expression
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Keywords:
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Invasion, Melanoma, Migration, MMP2 & MMP9, Myristicin
Abstract
Melanoma is the deadliest type of skin cancer, having a high mortality rate. This cancer has an aggressive nature, is highly invasive, and has the tendency to metastasize. Matrix metalloproteinases (MMPs) are essential in that process, especially MMP2 and MMP9. Their expression is upregulated during metastasis progression. Myristicin is one example of a compound that can be utilized to target MMP 2 and MMP 9 in melanoma. This research concerns the activity of myristicin to inhibit melanoma cell invasion and migration by suppressing MMP2 and MMP9 gene expression. The MTT assay in this study demonstrated that myristicin exhibited strong cytotoxic activity against melanoma cells. This compound works in a dose-dependent manner by inhibiting cell migration and invasion. The invasion test was performed using the transwell assay, whereas the migration test was performed using the wound healing assay. The invasion assay results were consistent with MMP2 and MMP9 gene expression. These two genes were analyzed using the RT-qPCR technique. It has been demonstrated that low gene expression in melanoma cells inhibits cell invasion. In contrast, higher MMP2 and MMP9 gene expression was associated with an increase in the number of invasive cells on average. However, MMP2 and MMP9 in excessive expression and uncontrolled activity impair the ability of melanoma cells to form a monolayer sheet to cover wound gaps. This condition significantly reduced the migration rate and percentage of wound closure.
References
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Goding, C. (2017). Translation Reprogramming Key Determinant Of Melanoma Invasion. Oncology Times, 39(6); 1–8
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Jonkman, J. E. N., J. A. Cathcart, and F. Xu (2014). An Introduction To The Wound Healing Assay Using Live-Cell Microscopy. Cell Adhesion & Migration, 8(5); 440–451
Ju, R. J., S. J. Stehbens, and N. K. Haass (2018). The Role Of Melanoma Cell-Stroma Interaction In Cell Motility, Invasion, And Metastasis. Frontiers In Medicine, 5; 307
Justus, C. R., N. Leffler, M. Ruiz-Echevarria, and L. V. Yang (2014). In Vitro Cell Migration And Invasion Assays. Journal Of Visualized Experiments, 88; e51046
Krejner, A., L. Malgorzata, and G. Tomasz (2016). Matrix Metalloproteinases In The Wound Microenvironment: Therapeutic Perspectives. Chronic Wound Care Management And Research, 3; 29–39
Lee, B. K., J. H. Kim, J. W. Jung, J. W. Choi, E. S. Han, S. H. Lee, K. H. Ko, and J. H. Ryu (2005). Myristicin-Induced Neurotoxicity In Human Neuroblastoma SK-N-SH Cells. Toxicology Letters, 157(1); 49–56
Lee, K., C. M. Lee, I. D. Jung, Y. Jeong, S. Chun, H. Park, I. Choi, S. Ahn, Y. Shin, S. Lee, S. Yeom, J. Kim, and Y. Park (2007). GATA-3 Is A Key Factor For Th1/Th2 Balance Regulation By Myristicin In A Murine Model Of Asthma. Journal Of Life Science, 17(8); 1090–1099
Luo, L., H. Liang, and L. Liu (2022). Myristicin Regulates Proliferation and Apoptosis in Oxidized Low-Density Lipoprotein-Stimulated Human Vascular Smooth Muscle Cells and Human Umbilical Vein Endothelial Cells by Regulating the PI3K/Akt/NF-kB Signalling Pathway. Pharmaceutical Biology, 60(1); 56–64
Machana, S., N. Weerapreeyakul, S. Barusrux, A. Nonpunya, B. Sripanidkulchai, and T. Thitimetharoch (2011). Cytotoxic and Apoptotic Effects of Six Herbal Plants Against the Human Hepatocarcinoma (HepG2) Cell Line. Chinese Medicine, 6; 1–8
Martins, C., C. Doran, I. C. Silva, C. Miranda, J. Rueff, and A. S. Rodrigues (2014). Myristicin from Nutmeg Induces Apoptosis via the Mitochondrial Pathway and Down Regulates Genes of the DNA Damage Response Pathways in Human Leukaemia K562 Cells. Chemico-Biological Interactions, 218; 1–9
Maverakis, E., L. Cornelius, G. Bowen, T. Phan, F. Patel, S. Fitzmaurice, Y. He, B. Burrall, C. Duong, A. Kloxin, H. Sultani, R. Wilken, S. Martinez, and F. Patel (2015). Metastatic Melanoma – A Review of Current and Future Treatment Options. Acta Dermato Venereologica, 95(5); 516–524
Mills, L., C. Tellez, S. Huang, C. Baker, M. Mccarty, L. Green, J. M. Gudas, X. Feng, and M. Bar-Eli (2002). Fully Human Antibodies to MCAM/MUC18 Inhibit Tumor Growth and Metastasis of Human Melanoma. Cancer Research, 62(17); 5106–5114
Napoli, S., C. Scuderi, G. Gattuso, V. Di Bella, S. Candido, M. S. Basile, M. Libra, and L. Falzone (2020). Functional Roles of Matrix Metalloproteinases and Their Inhibitors in Melanoma. Cells, 9(5); 1151
Nazar, S. S. and J. P. Ayyappan (2024). Mechanistic Evaluation of Myristicin on Apoptosis and Cell Cycle Regulation in Breast Cancer Cells. Journal of Biochemical and Molecular Toxicology, 38(6); e23740
Rebecca, V. W., R. Somasundaram, and M. Herlyn (2020). Pre-Clinical Modeling of Cutaneous Melanoma. Nature Communications, 11(1); 2858
Sabino, F. and U. auf dem Keller (2015). Matrix Metalloproteinases in Impaired Wound Healing. Metalloproteinases in Medicine, 2; 1–8
Savitri, R. I., H. A. Nuha, and F. Rifki (2023). Antioxidant, Cytotoxic Activity and Protein Target Inhibition of Ethyl Acetate Fraction Melinjo Seed (Gnetum gnemon L.) by In Vitro and In Silico Studies on HeLa Cervical Cancer Cells. HAYATI Journal Bioscience, 30(5); 864–873
Shay, G., C. C. Lynch, and B. Fingleton (2015). Moving Targets: Emerging Roles for MMPs in Cancer Progression and Metastasis. Matrix Biology, 44-46; 200–206
Shi, L., S. Ramsay, R. Ermis, and D. Carson (2012). In Vitro and In Vivo Studies on Matrix Metalloproteinases Interacting with Small Intestine Submucosa Wound Matrix. International Wound Journal, 9(1); 44–53
Shrikhande, S. S., D. S. Jain, R. B. Athawale, A. N. Bajaj, P. Goel, Z. Kamran, Y. Nikam, and R. Gude (2015). Evaluation of Anti-Metastatic Potential of Cisplatin Polymeric Nanocarriers on B16F10 Melanoma Cells. Saudi Pharmaceutical Journal, 23(4); 341–351
Song, J., X. Xu, S. He, N. Wang, Y. Bai, Z. Chen, B. Li, and S. Zhang (2023). Myristicin Suppresses Gastric Cancer Growth via Targeting the EGFR/ERK Signaling Pathway. Current Molecular Pharmacology, 16(7); 712–724
Suarez-Arnedo, A., F. Torres, C. Clavijo, P. Arbeláez, J. C. Cruz, and C. Muñoz-Camargo (2020). An Image J Plugin for the High Throughput Image Analysis of In Vitro Scratch Wound Healing Assays. PLoS One, 15(7); e0232565
Tsung, A. J., O. Kargiotis, C. Chetty, S. S. Lakka, M. Gujrati, D. G. Spomar, D. H. Dinh, and J. S. Rao (2008). Downregulation of Matrix Metalloproteinase-2 (MMP-2) Utilizing Adenovirus-Mediated Transfer of Small Interfering RNA (siRNA) in a Novel Spinal Metastatic Melanoma Model. International Journal of Oncology, 32(3); 557–564
Villareal, M. O., Y. Sato, K. Matsuyama, and H. Isoda (2018). Daphnane Diterpenes Inhibit the Metastatic Potential of B16F10 Murine Melanoma Cells In Vitro and In Vivo. BMC Cancer, 18(1); 1–11
Weerapreeyakul, N., A. Nonpunya, S. Barusrux, T. Thitimetharoch, and B. Sripanidkulchai (2012). Evaluation of the Anticancer Potential of Six Herbs Against a Hepatoma Cell Line. Chinese Medicine (United Kingdom), 7; 15
Zhang, T., K. Dutton-Regester, K. M. Brown, and N. K. Hayward (2016). The Genomic Landscape of Cutaneous Melanoma. Pigment Cell & Melanoma Research, 29(3); 266–283
Zhao, K., L. Wei, H. Hui, Q. Dai, Q. D. You, Q. L. Guo, and N. Lu (2014). Wogonin Suppresses Melanoma Cell B16-F10 Invasion and Migration by Inhibiting Ras-Mediated Pathways. PLoS One, 9(9); e106458
Zhou, L., K. Yang, T. Andl, R. R. Wickett, and Y. Zhang (2015). Perspective of Targeting Cancer-Associated Fibroblasts in Melanoma. Journal of Cancer, 6(8); 717
Bao, H. and Q. Muge (2021). Anticancer Effect Of Myristicin On Hepatic Carcinoma And Related Molecular Mechanism. Pharmaceutical Biology, 59(1); 1126–1132
Bastian, A., L. Nichita, and S. Zurac (2017). Matrix Metalloproteinases In Melanoma With And Without Regression. In The Role Of Matrix Metalloproteinase In Human Body Pathologies. InTech
Braeuer, R. R., I. R. Watson, C. J. Wu, A. K. Mobley, T. Kamiya, E. Shoshan, and M. Bar-Eli (2014). Why Is Melanoma So Metastatic? Pigment Cell & Melanoma Research, 27(1); 19–36
Cabral-Pacheco, G. A., I. Garza-Veloz, C. Castruita-De la Rosa, J. M. Ramirez-Acuña, B. A. Perez-Romero, J. F. Guerrero-Rodriguez, N. Martinez-Avila, and M. L. Martinez-Fierro (2020). The Roles Of Matrix Metalloproteinases And Their Inhibitors In Human Diseases. International Journal Of Molecular Sciences, 21(24); 9739
Chang, K. F., H. C. Lai, S. C. Lee, X. F. Huang, Y. C. Huang, T. E. Chou, C. Y. Hsiao, and N. M. Tsai (2023). The Effects Of Patchouli Alcohol And Combination With Cisplatin On Proliferation, Apoptosis And Migration In B16F10 Melanoma Cells. Journal Of Cellular And Molecular Medicine, 27(10); 1423–1435
Choi, E. O., E. J. Cho, J. W. Jeong, C. Park, S. H. Hong, H. J. Hwang, S. K. Moon, C. G. Son, W. J. Kim, and Y. H. Choi (2017). Baicalein Inhibits The Migration And Invasion Of B16F10 Mouse Melanoma Cells Through Inactivation Of The Pi3K/Akt Signaling Pathway. Biomolecules And Therapeutics, 25(2); 213–221
Chunyan, D., N. He, L. Zhu, L. Fan, F. Yi, T. Wang, and W. Deng (2020). The Mechanism Of Myristicin Inhibiting Proliferation, Migration And Invasion Of Colon Cancer Cell Lines. Modernization Of Traditional Chinese Medicine And Materia Materia-World Science And Technology, 22(4); 907–913
Cui, S., J. Wang, Q. Wu, J. Qian, C. Yang, and P. Bo (2017). Genistein Inhibits The Growth And Regulates The Migration And Invasion Abilities Of Melanoma Cells Via The FAK/Paxillin And MAPK Pathways. Oncotarget, 8(13); 21674–21691
de Franca, M. N. F., R. G. Isidório, J. H. O. Bonifacio, E. W. P. dos Santos, J. F. Santos, F. M. Ottoni, W. de Lucca Junior, R. Scher, R. J. Alves, and C. B. Corrêa (2021). Anti-Proliferative And Pro-Apoptotic Activity Of Glycosidic Derivatives Of Lawsone In Melanoma Cancer Cell. BMC Cancer, 21(1); 662
Egeblad, M. and Z. Werb (2002). New Functions For The Matrix Metalloproteinases In Cancer Progression. Nature Reviews Cancer, 2(3); 161–174
Falzone, L., R. Salemi, S. Travali, A. Scalisi, J. A. McCubrey, S. Candido, and M. Libra (2016). MMP-9 Overexpression Is Associated With Intragenic Hypermethylation Of MMP9 Gene In Melanoma. Aging, 8(5); 933–944
Gam, D. H., J. H. Park, J. H. Kim, D. H. Beak, and J. W. Kim (2021). Effects Of Allium Sativum Stem Extract On Growth And Migration In Melanoma Cells Through Inhibition Of VEGF, MMP-2, And MMP-9 Genes Expression. Molecules, 27(1); 21
Goding, C. (2017). Translation Reprogramming Key Determinant Of Melanoma Invasion. Oncology Times, 39(6); 1–8
He, D., Z. Ma, K. Xue, and H. Li (2022). Juxtamembrane 2 Mimic Peptide Competitively Inhibits Mitochondrial Trafficking And Activates ROS-Mediated Apoptosis Pathway To Exert Anti-Tumor Effects. Cell Death And Disease, 13(3)
Hessler, M., E. Jalilian, Q. Xu, R. N. Reddy, V. Vasquez-Montes, Z. Szekely, and S. Lin (2020). Biological And Biophysical Underpinnings Of Cell-Cell Fusion And Heterokaryon Formation. Journal Of Cellular Physiology, 236(2); 941–956
Ji, B. C., Y. P. Hsiao, C. H. Tsai, S. Chang, S. Hsu, H. Liu, Y. Huang, J. Lien, and J. Chung (2015). Cantharidin Impairs Cell Migration And Invasion Of A375.S2 Human Melanoma Cells By Suppressing MMP-2 And -9 Through PI3K/NF-kB Signaling Pathways. Anticancer Research, 35(2); 729–738
Jonkman, J. E. N., J. A. Cathcart, and F. Xu (2014). An Introduction To The Wound Healing Assay Using Live-Cell Microscopy. Cell Adhesion & Migration, 8(5); 440–451
Ju, R. J., S. J. Stehbens, and N. K. Haass (2018). The Role Of Melanoma Cell-Stroma Interaction In Cell Motility, Invasion, And Metastasis. Frontiers In Medicine, 5; 307
Justus, C. R., N. Leffler, M. Ruiz-Echevarria, and L. V. Yang (2014). In Vitro Cell Migration And Invasion Assays. Journal Of Visualized Experiments, 88; e51046
Krejner, A., L. Malgorzata, and G. Tomasz (2016). Matrix Metalloproteinases In The Wound Microenvironment: Therapeutic Perspectives. Chronic Wound Care Management And Research, 3; 29–39
Lee, B. K., J. H. Kim, J. W. Jung, J. W. Choi, E. S. Han, S. H. Lee, K. H. Ko, and J. H. Ryu (2005). Myristicin-Induced Neurotoxicity In Human Neuroblastoma SK-N-SH Cells. Toxicology Letters, 157(1); 49–56
Lee, K., C. M. Lee, I. D. Jung, Y. Jeong, S. Chun, H. Park, I. Choi, S. Ahn, Y. Shin, S. Lee, S. Yeom, J. Kim, and Y. Park (2007). GATA-3 Is A Key Factor For Th1/Th2 Balance Regulation By Myristicin In A Murine Model Of Asthma. Journal Of Life Science, 17(8); 1090–1099
Luo, L., H. Liang, and L. Liu (2022). Myristicin Regulates Proliferation and Apoptosis in Oxidized Low-Density Lipoprotein-Stimulated Human Vascular Smooth Muscle Cells and Human Umbilical Vein Endothelial Cells by Regulating the PI3K/Akt/NF-kB Signalling Pathway. Pharmaceutical Biology, 60(1); 56–64
Machana, S., N. Weerapreeyakul, S. Barusrux, A. Nonpunya, B. Sripanidkulchai, and T. Thitimetharoch (2011). Cytotoxic and Apoptotic Effects of Six Herbal Plants Against the Human Hepatocarcinoma (HepG2) Cell Line. Chinese Medicine, 6; 1–8
Martins, C., C. Doran, I. C. Silva, C. Miranda, J. Rueff, and A. S. Rodrigues (2014). Myristicin from Nutmeg Induces Apoptosis via the Mitochondrial Pathway and Down Regulates Genes of the DNA Damage Response Pathways in Human Leukaemia K562 Cells. Chemico-Biological Interactions, 218; 1–9
Maverakis, E., L. Cornelius, G. Bowen, T. Phan, F. Patel, S. Fitzmaurice, Y. He, B. Burrall, C. Duong, A. Kloxin, H. Sultani, R. Wilken, S. Martinez, and F. Patel (2015). Metastatic Melanoma – A Review of Current and Future Treatment Options. Acta Dermato Venereologica, 95(5); 516–524
Mills, L., C. Tellez, S. Huang, C. Baker, M. Mccarty, L. Green, J. M. Gudas, X. Feng, and M. Bar-Eli (2002). Fully Human Antibodies to MCAM/MUC18 Inhibit Tumor Growth and Metastasis of Human Melanoma. Cancer Research, 62(17); 5106–5114
Napoli, S., C. Scuderi, G. Gattuso, V. Di Bella, S. Candido, M. S. Basile, M. Libra, and L. Falzone (2020). Functional Roles of Matrix Metalloproteinases and Their Inhibitors in Melanoma. Cells, 9(5); 1151
Nazar, S. S. and J. P. Ayyappan (2024). Mechanistic Evaluation of Myristicin on Apoptosis and Cell Cycle Regulation in Breast Cancer Cells. Journal of Biochemical and Molecular Toxicology, 38(6); e23740
Rebecca, V. W., R. Somasundaram, and M. Herlyn (2020). Pre-Clinical Modeling of Cutaneous Melanoma. Nature Communications, 11(1); 2858
Sabino, F. and U. auf dem Keller (2015). Matrix Metalloproteinases in Impaired Wound Healing. Metalloproteinases in Medicine, 2; 1–8
Savitri, R. I., H. A. Nuha, and F. Rifki (2023). Antioxidant, Cytotoxic Activity and Protein Target Inhibition of Ethyl Acetate Fraction Melinjo Seed (Gnetum gnemon L.) by In Vitro and In Silico Studies on HeLa Cervical Cancer Cells. HAYATI Journal Bioscience, 30(5); 864–873
Shay, G., C. C. Lynch, and B. Fingleton (2015). Moving Targets: Emerging Roles for MMPs in Cancer Progression and Metastasis. Matrix Biology, 44-46; 200–206
Shi, L., S. Ramsay, R. Ermis, and D. Carson (2012). In Vitro and In Vivo Studies on Matrix Metalloproteinases Interacting with Small Intestine Submucosa Wound Matrix. International Wound Journal, 9(1); 44–53
Shrikhande, S. S., D. S. Jain, R. B. Athawale, A. N. Bajaj, P. Goel, Z. Kamran, Y. Nikam, and R. Gude (2015). Evaluation of Anti-Metastatic Potential of Cisplatin Polymeric Nanocarriers on B16F10 Melanoma Cells. Saudi Pharmaceutical Journal, 23(4); 341–351
Song, J., X. Xu, S. He, N. Wang, Y. Bai, Z. Chen, B. Li, and S. Zhang (2023). Myristicin Suppresses Gastric Cancer Growth via Targeting the EGFR/ERK Signaling Pathway. Current Molecular Pharmacology, 16(7); 712–724
Suarez-Arnedo, A., F. Torres, C. Clavijo, P. Arbeláez, J. C. Cruz, and C. Muñoz-Camargo (2020). An Image J Plugin for the High Throughput Image Analysis of In Vitro Scratch Wound Healing Assays. PLoS One, 15(7); e0232565
Tsung, A. J., O. Kargiotis, C. Chetty, S. S. Lakka, M. Gujrati, D. G. Spomar, D. H. Dinh, and J. S. Rao (2008). Downregulation of Matrix Metalloproteinase-2 (MMP-2) Utilizing Adenovirus-Mediated Transfer of Small Interfering RNA (siRNA) in a Novel Spinal Metastatic Melanoma Model. International Journal of Oncology, 32(3); 557–564
Villareal, M. O., Y. Sato, K. Matsuyama, and H. Isoda (2018). Daphnane Diterpenes Inhibit the Metastatic Potential of B16F10 Murine Melanoma Cells In Vitro and In Vivo. BMC Cancer, 18(1); 1–11
Weerapreeyakul, N., A. Nonpunya, S. Barusrux, T. Thitimetharoch, and B. Sripanidkulchai (2012). Evaluation of the Anticancer Potential of Six Herbs Against a Hepatoma Cell Line. Chinese Medicine (United Kingdom), 7; 15
Zhang, T., K. Dutton-Regester, K. M. Brown, and N. K. Hayward (2016). The Genomic Landscape of Cutaneous Melanoma. Pigment Cell & Melanoma Research, 29(3); 266–283
Zhao, K., L. Wei, H. Hui, Q. Dai, Q. D. You, Q. L. Guo, and N. Lu (2014). Wogonin Suppresses Melanoma Cell B16-F10 Invasion and Migration by Inhibiting Ras-Mediated Pathways. PLoS One, 9(9); e106458
Zhou, L., K. Yang, T. Andl, R. R. Wickett, and Y. Zhang (2015). Perspective of Targeting Cancer-Associated Fibroblasts in Melanoma. Journal of Cancer, 6(8); 717
Authors
Krisnayanti, N. P. E., Mariya, S., Indriawati, I., Dayana, H., Zaelani, B. F. D., Tjandrawinata, R. R., & Darusman, H. S. (2024). Myristicin Inhibit Invasion and Migration of Melanoma Cells through Suppression of MMP2 and MMP9 Gene Expression. Science and Technology Indonesia, 9(4), 884–892. https://doi.org/10.26554/sti.2024.9.4.884-892
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