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Research Article

Molecular insights of anticancer potential of usnic acid towards cervical cancer target proteins: An in silico validation for novel anti-cancer compound from lichens

, , , , &
Received 02 Apr 2023, Accepted 20 Aug 2023, Published online: 11 Sep 2023

References

  • Bahnassy, A. A., Zekri, A. R., Saleh, M., Lotayef, M., Moneir, M., & Shawki, O. (2007). The possible role of cell cycle regulators in multistep process of HPV-associated cervical carcinoma. BMC Clinical Pathology, 7(1), 4. https://doi.org/10.1186/1472-6890-7-4
  • Balasubramanian, M., & Nirmala, P. (2014a). Antimycobacterial activity of foliose lichens on plant and animal pathogens. International Journal of Pharmaceutical Sciences and Research, 5(11), 1000–1006. https://doi.org/10.13040/IJPSR.0975-8232.5(11).4825-31
  • Balasubramanian, M., & Nirmala, P. (2014b). Evaluation of antioxidant properties of foliose lichens. Journal of Chemical and Pharmaceuticacl Research, 6(9), 177–184.
  • Berman, H. M., Battistuz, T., Bhat, T. N., Bluhm, W. F., Bourne, P. E., Burkhardt, K., Feng, Z., Gilliland, G. L., Iype, L., Jain, S., Fagan, P., Marvin, J., Padilla, D., Ravichandran, V., Schneider, B., Thanki, N., Weissig, H., Westbrook, J. D., & Zardecki, C. (2002). The protein data bank. Acta Crystallographica. Section D, Biological Crystallography, 58(Pt 6 No 1), 899–907. https://doi.org/10.1107/s0907444902003451
  • Booth, G. M., Malmstrom, R. D., Kipp, E., & Paul, A. (2012). Cytotoxicity of selected medicinal and non medicinal plant extracts to microbial and cervical cancer cells. Journal of Biomedicine & Biotechnology, 2012, 106746. https://doi.org/10.1155/2012/106746
  • Bowers, K. J., Chow, E., Xu, H., Dror, R. O., Eastwood, M. P., Gregersen, B. A., Klepeis, J. L., Kolossvary, I., Moraes, M. A., Sacerdoti, F. D., Salmon, J. K., Shan, Y., & Shaw, D. E. (2006). Scalable algorithms for molecular dynamics simulations on commodity clusters [Paper presentation] [Paper presentation].Proceedings of the 2006 ACM/IEEE Conference on Supercomputing, SC’06, November. https://doi.org/10.1145/1188455.1188544
  • Brahmkhatri, V. P., Prasanna, C., & Atreya, H. S. (2015). Insulin-like growth factor system in cancer: Novel targeted therapies. BioMed Research International, 2015, 538019. https://doi.org/10.1155/2015/538019
  • Brisson, M., & Drolet, M. (2019). Global elimination of cervical cancer as a public health problem. The Lancet Oncology, 20(3), 319–321. https://doi.org/10.1016/S1470-2045(19)30072-5
  • Broksa, B., Sturdíková, M., Prónayová, N., & Liptaj, T. (1996). Usnic acid and its derivatives. Their inhibition of fungal growth and enzyme activity. Die Pharmazie, 51(3), 195–196. PMID: 8900875.
  • Cardarelli, M., Serino, G., Campanella, L., Ercole, P., De Cicco Nardone, F., Alesiani, O., & Rossiello, F. (1997). Antimitotic effects of usnic acid on different biological systems. Cellular and Molecular Life Sciences: CMLS, 53(8), 667–672. https://doi.org/10.1007/s000180050086
  • Cardile, V., Graziano, A. C. E., Avola, R., Piovano, M., & Russo, A. (2017). Potential anticancer activity of lichen secondary metabolite physodic acid. Chemico-Biological Interactions, 263, 36–45. https://doi.org/10.1016/j.cbi.2016.12.007
  • Carmelo, B., Jose, M., Lopez, N., & Miguel, Q. (1792). The emerging role of TGF-β superfamily coreceptors in cancer. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 10, 954–973. https://doi.org/10.1016/j.bbadis.2009.07.003
  • Cervical Cancer Screening Every 5 Years OK. (2018). Cancer Discov, 8(10), 1204. https://doi.org/10.1158/2159-8290.CD-NB2018-118
  • Chandrasekaran, B., Abed, S. N., Al-Attraqchi, O., Kuche, K., & Tekade, R. K. (2018). Computer-aided prediction of pharmacokinetic (ADMET) properties. Dosage form Design Parameters. Academic Press. 731–755. https://doi.org/10.1016/B978-0-12-814421-3.00021-X
  • CSDD. (2014). http://csdd.tufts. edu/news/complete_story/pr_tufts_csdd_2014_cost_study.
  • Daina, A., Michielin, O., & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Scientific Reports, 7(1), 42713–42717. https://doi.org/10.1038/srep42717
  • Eryilmaz, I. E., Guney, E. G., Egeli, U., Yurdacan, B., Cecener, G., & Tunca, B. (2018). In vitro cytotoxic and antiproliferative effects of usnic acid on hormone-dependent breast and prostate cancer cells. Journal of Biochemical and Molecular Toxicology, 32(10), e22208. https://doi.org/10.1002/jbt.22208
  • Fang, C., Xiuli, L., Xiangyu, Z., Lili, H., Yongfang, H., Caiying, M., Qi, Y., Jianhong, Z., Wenxia, Z,., & Shi, H. (2012). MiR-125b inhibits tumor growth and promotes apoptosis of cervical cancer cells by targeting phosphoinositide 3-kinase catalytic subunit delta. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 30(5), 1310–1318. https://doi.org/10.1159/000343320
  • Geng, X., Zhang, X., Zhou, B., Zhang, C., Tu, J., Chen, X., Wang, J., Gao, H., Qin, G., & Pan, W. (2018). Usnic acid induces cycle arrest, apoptosis, and autophagy in gastric cancer cells in vitro and in vivo. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 24, 556–566. https://doi.org/10.12659/msm.908568
  • Genheden, S., & Ryde, U. (2015). Ulf the MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
  • Harris, N. J. (1961). Honors Thesis, Clark University, Worcester, Massachusetts.
  • Hosseini, A., & Ghorbani, A. (2015). Cancer therapy with phytochemicals: Evidence from clinical studies. Avicenna Journal of Phytomedicine, 5(2), 84–97. PMID: 25949949.
  • Ingolfsdottir, K. (2002). Usnic acid. Phytochemistry, 61(7), 729–736. https://doi.org/10.1016/s0031-9422(02)00383-7
  • Jiangsu New Medical College. (1977). Chinese Materia Medica Dictionary (1st Vol). Shanghai, China. 1256–1258. https://doi.org/10.3390/molecules27217469.
  • Jin, W. S., Se-Hee, K., & Jin, Y. Y. (2021). PTEN downregulation induces apoptosis and cell cycle arrest in uterine cervical cancer cells. Experimental and Therapeutic Medicine, 22, 1100. https://doi.org/10.3892/etm.2021.10534
  • Krishnaveni, B., Balasubramanian, M., & Gopinath, L. R. (2018). Pharmacological evaluation of parmelioid lichen Flavoparmelia Caperata (L) Hale with special reference to analgesic and anti-inflammatory properties. IOSR Journal of Pharmacy, 8(10), 22–29.
  • Kupchan, S. M., & Kopperman, H. L. (1975). l-usnic acid: Tumor inhibitor isolated from lichens. Experientia, 31(6), 625–625. https://doi.org/10.1007/BF01944592
  • Li, S.-W., Wang, C.-Y., Jou, Y.-J., Huang, S.-H., Hsiao, L.-H., Wan, L., Lin, Y.-J., Kung, S.-H., & Lin, C.-W. (2016). SARS coronavirus papain-like protease inhibits the TLR7 signaling pathway through removing Lys63-Linked polyubiquitination of TRAF3 and TRAF6. International Journal of Molecular Sciences, 17(5), 678. https://doi.org/10.3390/ijms17050678
  • Lowy, D. R., & Schiller, J. T. (2006). Prophylactic human papillomavirus vaccines. The Journal of Clinical Investigation, 116(5), 1167–1173. https://doi.org/10.1172/JCI28607
  • Margareth, M., Mary, A. O. N., Karen, E. M., Nereide, S. S. M., Ana Maria, A. C. L., Alastair, M. T., & Virginia, C. L. A. (2005). Usnic acid: A non-genotoxic compound with anti-cancer properties. Anti-Cancer Drugs, 16(8), 805–809. https://doi.org/10.1097/01.cad.0000175588.09070.77
  • Medina-Alarcón, K. P., Voltan, A. R., Fonseca-Santos, B., Moro, I. J., de Oliveira Souza, F., Chorilli, M., Soares, C. P., Dos Santos, A. G., Mendes-Giannini, M. J. S., & Fusco-Almeida, A. M. (2017). Highlights in nanocarriers for the treatment against cervical cancer. Materials Science & Engineering. C, Materials for Biological Applications, 80, 748–759. https://doi.org/10.1016/j.msec.2017.07.021
  • Mishra, S. S., Kumar, N., Singh, H. P., Ranjan, S., & Sharma, C. S. (2018). In silico pharmacokinetic, bioactivity and toxicity study of some selected anti-asthmatic agents. International Journal of Pharmaceutical Sciences and Drug Research, 10(4), 278–282. https://doi.org/10.1016/j.msec.2017.07.021
  • Myers, S., & Baker, A. (2001). Drug discovery–an operating model for a new era. Nature Biotechnology, 19(8), 727–730. PMID: 11479559. https://doi.org/10.1038/90765
  • Nichols, G. E., Williams, M. E., Gaffey, M. J., & Stoler, M. H. (1996). Cyclin D1 gene expression in human cervical neoplasia. Modern Pathology, 9, 418–425. https://doi.org/10.12892/ejgo4135.2018PMID: 8729983.
  • Nicolussi, A., D'Inzeo, S., Capalbo, C., Giannini, G., & Coppa, A. (2017). The role of peroxiredoxins in cancer. Molecular and Clinical Oncology, 6(2), 139–153. PMID: 28357082. https://doi.org/10.3892/mco.2017.1129
  • Noor, H., Ikram, A., Rathinavel, T., Kumarasamy, S., Nasir Iqbal, M., & Bashir, Z. (2021). Immunomodulatory and anti-cytokine therapeutic potential of curcumin and its derivatives for treating COVID-19–a computational modeling. Journal of Biomolecular Structure and Dynamics, 1–16 https://doi.org/10.1080/07391102.20211873190.
  • Pablo, M. A., Mónica, M., Nicolas, M., Jinneth, A., Cristian, G. P., Diana, M., Lina, B., Oscar, G., Juan, C. M., July, C., Alfredo, R. R., Sophie, E., Gerald, L., Murray, S. M. G., Alexis, V., & Nicolas, M. (2020). hTERT protein expression in cytoplasm and nucleus and its association with HPV infection in patients with cervical cancer. Cancer Genomics & Proteomics, 17(5), 615–625. https://doi.org/10.21873/cgp.20218
  • Pimple, S. A., & Mishra, G. A. (2019). Global strategies for cervical cancer prevention and screening. Minerva Ginecologica, 71(4), 313–320. https://doi.org/10.23736/S0026-4784.19.04397-1
  • Pricopie, A.-I., Ionuț, I., Marc, G., Arseniu, A.-M., Vlase, L., Grozav, A., Găină, L. I., Vodnar, D. C., Pîrnău, A., Tiperciuc, B., & Oniga, O. (2019). Design and synthesis of novel 1,3-Thiazole and 2-Hydrazinyl-1,3-Thiazole derivatives as anti-candida agents: In vitro antifungal screening, molecular docking study, and spectroscopic investigation of their binding interaction with bovine serum albumin. Molecules (Basel, Switzerland), 24(19), 3435. 10.3390/molecules24193435
  • Rafanelli, S., Bacchilega, R., Stanganelli, I., & Rafanelli, A. (1995). Contact dermatitis from usnic acid in vaginal ovules. Contact Dermatitis, 33(4), 271–272. https://doi.org/10.1111/j.1600-0536.1995.tb00484.x
  • Romagni, J. G., Meazza, G., Nanayakkara, N. P., & Dayan, F. E. (2000). The phytotoxic lichen metabolite, usnic acid, is a potent inhibitor of plant p-hydroxyphenylpyruvate dioxygenase. FEBS Letters, 480(2-3), 301–305. https://doi.org/10.1016/s0014-5793(00)01907-4
  • Salgado, F., Albornoz, L., Cortéz, C., Stashenko, E., Urrea-Vallejo, K., Nagles, E., Galicia-Virviescas, C., Cornejo, A., Ardiles, A., Simirgiotis, M., García-Beltrán, O., & Areche, C. (2017). Secondary metabolite profiling of species of the genus usnea by UHPLC-ESI-OT-MS-MS. Molecules (Basel, Switzerland), 23(1), 54. https://doi.org/10.3390/molecules23010054
  • Saranyadevi, S., Suresh, K., Mathiyazhagan, N., Muthusamy, R., Thirumalaisamy, R., Arunachalam, C., Tahani, A. A., Indira, K., Arivalagan, P., & Kanda, W. (2022). Spectral and structure characterization of Ferula assafoetida fabricated silver nanoparticles and evaluation of its cytotoxic, and photocatalytic competence. Environmental Research, 204, 111987. https://doi.org/10.1016/j.envres.2021.111987
  • Selvaraj, V., Rathinavel, T., Ammashi, S., & Nasir Iqbal, M. (2023). Polyphenolic phytochemicals exhibit promising SARS-COV-2 papain like protease (PLpro) inhibition validated through a computational approach. Polycyclic Aromatic Compounds, 43(6), 5545–5566. https://doi.org/10.1080/10406638.2022.2103578
  • Shivakumar, D., Williams, J., Wu, Y., Damm, W., Shelley, J., & Sherman, W. (2010). Prediction of absolute solvation free energies using molecular dynamics free energy perturbation and the OPLS force field. Journal of Chemical Theory and Computation, 6(5), 1509–1519. https://doi.org/10.1021/ct900587b
  • Shukla, P., Upreti, D. K., & Tewari, L. M. (2014). Secondary metabolite variability in lichen genus usnea in India: A potential source for bioprospection. G- Journal of Environmental Science and Technology, 2(3), 29–40.
  • Siegel, P. M., & Massague, J. (2003). Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nature Reviews. Cancer, 3(11), 807–821. https://doi.org/10.1038/nrc1208
  • Sindhu, M. S.,Poonkothai, M., &Thirumalaisamy, R. (2022). Phenolic and terpene compounds from Plectranthus amboinicus (Lour.) Spreng. Act as promising hepatic anticancer agents screened through in silico and in vitro approaches. South African Journal of Botany, 149, 145–159. https://doi.org/10.1016/j.sajb.2022.06.001
  • Stanojkovic, T. (2015). Investigations of lichen secondary metabolites with potential anticancer activity. In B. Ranković (Ed). Lichen secondary metabolites: Bioactive properties and pharmaceutical potential (pp. 127–146). Springer International Publishing. https://doi.org/10.1007/978-3-319-13374-4
  • Sun, Y., Wang, H. J., Zhang, W., Wu, Y., Zhang, Z. Q., Feng, L., Wang, L. Q., & Wu, Y. M. (2005). Preliminary study on the inhibition effect of usnic acid on proliferation prostate cancer PC-3M cells. Chinese Journal of Cancer Biotherapy, 12, 289–291. https://doi.org/10.3390/molecules27217469
  • Sweetman, S. C. (2009). Martindale: The complete drug reference; pharmaceutical press (pp. 2409–2410). https://doi.org/10.3163/1536-5050.100.1.018
  • Takai, M., Uehara, Y., & Beisler, J. A. (1979). Usnic acid derivatives as potential antineoplastic agents. Journal of Medicinal Chemistry, 22(11), 1380–1384. https://doi.org/10.1021/jm00197a019
  • Thirumalaisamy, R., Aroulmoji, V., Iqbal, M. N., Deepa, M., Sivasankar, C., Khan, R., & Selvankumar, T. (2021). Molecular insights of the hyaluronic acid-hydroxychloroquine conjugate as a promising drug in targeting SARS-CoV-2 viral proteins. Journal of Molecular Structure, 1238, 130457. https://doi.org/10.1016/j.molstruc.2021.130457
  • Thirumalaisamy, R., Aroulmoji, V., & Nasir Iqbal, M. (2021b). Molecular insights of hyaluronic acid - ethambutol and hyaluronic acid - isoniazid drug conjugates act as promising novel drugs for the treatment of tuberculosis. Journal of Biomolecular Structure & Dynamics, 16, 1–12. https://doi.org/10.1080/07391102.2022.2051748
  • Thirumalaisamy, R., Bhuvaneswari, M., Haritha, S., Jeevarathna, S., Sai Janani, K. S., & Suresh, K. (2022). Curcumin, naringenin and resveratrol from natural plant products hold promising solution for modern world diseases: A recent review. South African Journal of Botany, 151(Part B), 567–580. https://doi.org/10.1016/j.sajb.2022.06.027
  • Thirumalaisamy, R., Sai, J. K., Bhuvaneswari, M., Vinoth, S., & Selvankumar, T. (2021a). Comparative anti–alzheimer’s potential evaluation of curcumin and curcumin analogues obtained from ZINC database: An in-silico validation. Texila International Journal of Public Health, 9(4), 269–283. https://doi.org/10.21522/TIJPH.2013.09.04.Art023
  • Trott, O., & Olson, A. J. (2010). AutoDock vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
  • Vartia, K. O. (1973). The Lichens; Academic Press. : 547–561.
  • Viswanathan, A. N., Dizon, D. S., Gien, L. T., & Koh, W. J. (2016). Chapter 58-cervical cancer. Clinical radiation oncolog (4th ed., pp. 1173–1202). Elsevier.
  • Weininger, D. (1988). SMILES, a chemical language and information system: 1: Introduction to methodology and encoding rules. Journal of Chemical Information and Computer Sciences, 28(1), 31–36. https://doi.org/10.1021/ci00057a005
  • Wong, K. K. V., Roney, M., Uddin, N., Imran, S., Gazali, A. M., Zamri, N., Rullah, K., & Aluwi, M. F. F. M. (2023). Usnic acid as potential inhibitors of BCL2 and P13K protein through network pharmacology-based analysis, molecular docking and molecular dynamic simulation. Journal of Biomolecular Structure & Dynamics, 1–14. https://doi.org/10.1080/07391102.2023.2178506
  • Wu, R., Duan, L., Cui, F., Cao, J., Xiang, Y., Tang, Y., & Zhou, L. (2015). S100A9 promotes human hepatocellular carcinoma cell growth and invasion through RAGE-mediated ERK1/2 and p38 MAPK pathways. Experimental Cell Research, 334(2), 228–238. https://doi.org/10.1016/j.yexcr.2015.04.008
  • Wu, R., Duan, L., Ye, L., Wang, H., Yang, X., Zhang, Y., Chen, X., Zhang, Y., Weng, Y., Luo, J., Tang, M., Shi, Q., He, T., & Zhou, L. (2013). S100A9 promotes the proliferation and invasion of HepG2 hepatocellular carcinoma cells via the activation of the MAPK signaling pathway. International Journal of Oncology, 42(3), 1001–1010. https://doi.org/10.3892/ijo.2013.1796
  • Yang, Y., Nguyen, T. T., Jeong, M.-H., Crişan, F., Yu, Y. H., Ha, H.-H., Choi, K. H., Jeong, H. G., Jeong, T. C., Lee, K. Y., Kim, K. K., Hur, J.-S., & Kim, H. (2016). Inhibitory activity of (+)-usnic acid against non-small cell lung cancer. PloS One, 11(1), e0146575. https://doi.org/10.1371/journal.pone.0146575
  • Yu, D. Y., Guo, X. L., Gao, H. Y., Cao, H., & Shi, L. Y. (2020). Effects of usnic acid on proliferation and apoptosis of three cancer cell lines. J. Tianjin Norm. Univ, 40, 39–43. https://doi.org/10.3390/molecules27217469
  • Zambare, V. P., & Christopher, L. P. (2012). Biopharmaceutical potential of lichens. Pharmaceutical Biology, 50(6), 778–798. https://doi.org/10.3109/13880209.2011.633089
  • Zhao, Q., He, Y., Wang, X. L., Zhang, Y. X., & Wu, Y. M. (2015). Differentially expressed proteins among normal cervix, cervical intraepithelial neoplasia and cervical squamous cell carcinoma. Clinical & Translational Oncology: Official Publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico, 17(8), 620–631. https://doi.org/10.1007/s12094-015-1287-x
  • Zhu, X., Jin, L., Zou, S., Shen, Q., Jiang, W., Lin, W., & Zhu, X. (2013). Immunohistochemical expression of RAGE and its ligand (S100A9) in cervical lesions. Cell Biochemistry and Biophysics, 66(3), 843–850. https://doi.org/10.1007/s12013-013-9515-x
  • Zwick, E., Bange, J., & Ullrich, A. (2002). Receptor tyrosine kinase as targets for anticancer drugs. Trends in Molecular Medicine, 8(1), 17–23. https://doi.org/10.1016/s1471-4914(01)02217-1

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