171
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Development of 1,3-diynyl derivatives of noscapine as potent tubulin binding anticancer agents for the management of breast cancer

, , , , ORCID Icon & ORCID Icon
Pages 13136-13153 | Received 08 Jul 2021, Accepted 13 Sep 2021, Published online: 29 Sep 2021

References

  • Aneja, R., Vangapandu, S. N., Lopus, M., Chandra, R., Panda, D., & Joshi, H. C. (2006a). Development of a novel nitro-derivative of noscapine for the potential treatment of drug-resistant ovarian cancer and T-cell lymphoma. Molecular Pharmacology, 69(6), 1801–1809. https://doi.org/10.1124/mol.105.021899
  • Aneja, R., Vangapandu, S. N., Lopus, M., Viswesarappa, V. G., Dhiman, N., Verma, A., Chandra, R., Panda, D., & Joshi, H. C. (2006b). Synthesis of microtubule-interfering halogenated noscapine analogs that perturb mitosis in cancer cells followed by cell death. Biochemical Pharmacology, 72(4), 415–426. https://doi.org/10.1016/j.bcp.2006.05.004
  • Becke, A. D. (1993). A new mixing of Hartree–Fock and local density‐functional theories. The Journal of Chemical Physics, 98(2), 1372–1377. https://doi.org/10.1063/1.464304
  • Beigoli, S., Sharifi Rad, A., Askari, A., Assaran Darban, R., & Chamani, J. (2019). Isothermal titration calorimetry and stopped flow circular dichroism investigations of the interaction between lomefloxacin and human serum albumin in the presence of amino acids. Journal of Biomolecular Structure & Dynamics, 37(9), 2265–2282. https://doi.org/10.1080/07391102.2018.1491421
  • Berendsen, H. J., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1–3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
  • Binkley, J. S., Pople, J. A., & Hehre, W. J. (1980). Self-consistent molecular orbital methods. 21. Small split-valence basis sets for first-row elements. Journal of the American Chemical Society, 102(3), 939–947. https://doi.org/10.1021/ja00523a008
  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1006/abio.1976.9999
  • Calabrese, E. J., & Baldwin, L. A. (2002). Defining hormesis. Human & Experimental Toxicology, 21(2), 91–97. https://doi.org/10.1191/0960327102ht217oa
  • Chamani, J., Moosavi-Movahedi, A. A., Saboury, A. A., Gharanfoli, M., & Hakimelahi, G. H. (2003). Calorimetric indication of the molten globule-like state of cytochrome c induced by n-alkyl sulfates at low concentrations. The Journal of Chemical Thermodynamics, 35(2), 199–207. https://doi.org/10.1016/S0021-9614(02)00312-9
  • Chen, J., Lu, L., Feng, Y., Wang, H., Dai, L., Li, Y., & Zhang, P. (2011). PKD2 mediates multi-drug resistance in breast cancer cells through modulation of P-glycoprotein expression. Cancer Letters, 300(1), 48–56. https://doi.org/10.1016/j.canlet.2010.09.005
  • Crown, J., & O’Leary, M. (2000). The taxanes: An update. The Lancet, 355(9210), 1176–1178. https://doi.org/10.1016/S0140-6736(00)02074-2
  • Dahlström, B., Mellstrand, T., Löfdahl, C. G., & Johansson, M. (1982). Pharmacokinetic properties of noscapine. European Journal of Clinical Pharmacology, 22(6), 535–539. https://doi.org/10.1007/BF00609627
  • Erwin, A. L. (2016). Antibacterial drug discovery targeting the lipopolysaccharide biosynthetic enzyme LpxC. Cold Spring Harbor Perspectives in Medicine, 6(7), a025304. https://doi.org/10.1101/cshperspect.a025304
  • Fekete, G. L., & Fekete, L. (2019). Cutaneous leukocytoclastic vasculitis associated with erlotinib treatment: A case report and review of the literature. Experimental and Therapeutic Medicine, 17(2), 1128–1131. https://doi.org/10.3892/etm.2018.6988
  • Fisher, B., Other National Surgical Adjuvant Breast, Costantino, J. P., Wickerham, D. L., Redmond, C. K., Kavanah, M., Cronin, W. M., Vogel, V., Robidoux, A., Dimitrov, N., Atkins, J., Daly, M., Wieand, S., Tan-Chiu, E., Ford, L., & Wolmark, N. (1998). Tamoxifen for prevention of breast cancer: Report of the National Surgical Adjuvant Breast and Bowel Project P-1 study. JNCI: Journal of the National Cancer Institute, 90(18), 1371–1388. https://doi.org/10.1093/jnci/90.18.1371
  • Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., & Shenkin, P. S. (2004). Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. Journal of Medicinal Chemistry, 47(7), 1739–1749. https://doi.org/10.1021/jm0306430
  • Gjerdrum, C., Tiron, C., Høiby, T., Stefansson, I., Haugen, H., Sandal, T., Collett, K., Li, S., McCormack, E., Gjertsen, B. T., Micklem, D. R., Akslen, L. A., Glackin, C., & Lorens, J. B. (2010). Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proceedings of the National Academy of Sciences of the United States of America, 107(3), 1124–1129. https://doi.org/10.1073/pnas.0909333107
  • Gordon, M. S., Binkley, J. S., Pople, J. A., Pietro, W. J., & Hehre, W. J. (1982). Self-consistent molecular-orbital methods. 22. Small split-valence basis sets for second-row elements. Journal of the American Chemical Society, 104(10), 2797–2803. https://doi.org/10.1021/ja00374a017
  • Gubaidullin, R. R., Khalitova, R. R., Nedopekina, D. A., & Spivak, A. Y. (2018). Homo‐and cross coupling of C‐2 propargyl substituted triterpenoic acids: Synthesis of novel symmetrical and unsymmetrical triterpene 1, 3‐diynes. ChemistrySelect, 3(47), 13526–13529. https://doi.org/10.1002/slct.201803522
  • Halgren, T. A., Murphy, R. B., Friesner, R. A., Beard, H. S., Frye, L. L., Pollard, W. T., & Banks, J. L. (2004). Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. Journal of Medicinal Chemistry, 47(7), 1750–1759. https://doi.org/10.1021/jm030644s
  • Hamel, E., & Lin, C. M. (1981). Glutamate-induced polymerization of tubulin: Characteristics of the reaction and application to the large-scale purification of tubulin. Archives of Biochemistry and Biophysics, 209(1), 29–40. https://doi.org/10.1016/0003-9861(81)90253-8
  • Jain, N., Yada, D., Shaik, T. B., Vasantha, G., Reddy, P. S., Kalivendi, S. V., & Sreedhar, B. (2011). Synthesis and antitumor evaluation of nitrovinyl biphenyls: Anticancer agents based on allocolchicines. ChemMedChem, 6(5), 859–868. https://doi.org/10.1002/cmdc.201100019
  • Jensen, L. N., Christrup, L. L., Jacobsen, L., Bonde, J., & Bundgaard, H. (1992). Relative bioavailability in man of noscapine administered in lozenges and mixture. Acta Pharmaceutica Nordica, 4(4), 309–312.
  • Jordan, M. A., Toso, R. J., Thrower, D., & Wilson, L. (1993). Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proceedings of the National Academy of Sciences of the United States of America, 90(20), 9552–9556. https://doi.org/10.1073/pnas.90.20.9552
  • Karlsson, M. O., Dahlström, B., Eckernäs, S. A., Johansson, M., & Alm, A. T. (1990). Pharmacokinetics of oral noscapine. European Journal of Clinical Pharmacology, 39(3), 275–279. https://doi.org/10.1007/BF00315110
  • Kasibhatla, S., Amarante-Mendes, G. P., Finucane, D., Brunner, T., Bossy-Wetzel, E., & Green, D. R. (2006). Acridine orange/ethidium bromide (AO/EB) staining to detect apoptosis. CSH Protocols, 2006(3), pdb.prot4493. https://doi.org/10.1101/pdb.prot4493
  • Lee, C. J., Liang, X., Wu, Q., Najeeb, J., Zhao, J., Gopalaswamy, R., Titecat, M., Sebbane, F., Lemaitre, N., Toone, E. J., & Zhou, P. (2016). Drug design from the cryptic inhibitor envelope. Nature Communications, 7, 10638. https://doi.org/10.1038/ncomms10638
  • Lee, C., Yang, W., & Parr, R. G. (1988). Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Physical Review B, Condensed Matter, 37(2), 785–789. https://doi.org/10.1103/physrevb.37.785
  • Lehmann, J., Wright, M. H., & Sieber, S. A. (2016). Making a long journey short: Alkyne functionalization of natural product scaffolds. Chemistry (Weinheim an Der Bergstrasse, Germany), 22(14), 4666–4678. https://doi.org/10.1002/chem.201504419
  • Lettre, H. (1954). Synergists and antagonists of mitotic poisons. Annals of the New York Academy of Sciences, 58(7), 1264–1275. https://doi.org/10.1111/j.1749-6632.1954.tb45907.x
  • Liang, X., Gopalaswamy, R., Navas, F., III, Toone, E. J., & Zhou, P. (2016). A scalable synthesis of the difluoromethyl-allo-threonyl hydroxamate-based LpxC inhibitor LPC-058. The Journal of Organic Chemistry, 81(10), 4393–4398. https://doi.org/10.1021/acs.joc.6b00589
  • Ma, K.-Q., Miao, Y.-H., Li, X., Zhou, Y.-Z., Gao, X.-X., Zhang, X., Chao, J.-B., & Qin, X.-M. (2017). Discovery of 1, 3-diyne compounds as novel and potent antidepressant agents: Synthesis, cell-based assay and behavioral studies. RSC Advances, 7(26), 16005–16014. https://doi.org/10.1039/C7RA01268C
  • Mahaddalkar, T., Naik, P. K., Choudhary, S., Manchukonda, N., Kantevari, S., & Lopus, M. (2017). Structural investigations into the binding mode of a novel noscapine analogue, 9-(4-vinylphenyl) noscapine, with tubulin by biochemical analyses and molecular dynamic simulations. Journal of Biomolecular Structure & Dynamics, 35(11), 2475–2484. https://doi.org/10.1080/07391102.2016.1222969
  • Mahmoudian, M., & Rahimi-Moghaddam, P. (2009). The anti-cancer activity of noscapine: A review. Recent Patents on anti-Cancer Drug Discovery, 4(1), 92–97. https://doi.org/10.2174/157489209787002524
  • Manchukonda, N. K., Naik, P. K., Santoshi, S., Lopus, M., Joseph, S., Sridhar, B., & Kantevari, S. (2013). Rational design, synthesis, and biological evaluation of third generation α-noscapine analogues as potent tubulin binding anti-cancer agents. PLoS One, 8(10), e77970. https://doi.org/10.1371/journal.pone.0077970
  • Manchukonda, N. K., Naik, P. K., Sridhar, B., & Kantevari, S. (2014). Synthesis and biological evaluation of novel biaryl type α-noscapine congeners. Bioorganic & Medicinal Chemistry Letters, 24(24), 5752–5757. https://doi.org/10.1016/j.bmcl.2014.10.046
  • Mattson, M. P., & Cheng, A. (2006). Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends in Neurosciences, 29(11), 632–639. https://doi.org/10.1016/j.tins.2006.09.001
  • McKeon, V. A. (1999). The breast cancer prevention trial: Should women at risk take tamoxifen? Journal of Obstetric, Gynecologic, and Neonatal Nursing: JOGNN, 28(6 Suppl 1), 34–38.
  • Nagireddy, P. K., Sridhar, B., & Kantevari, S. (2019). Copper‐catalyzed Glaser‐Hey‐type cross coupling of 9‐ethynyl‐α‐noscapine leading to unsymmetrical 1, 3‐diynyl noscapinoids. Asian Journal of Organic Chemistry, 8(8), 1495–1500. https://doi.org/10.1002/ajoc.201900316
  • Naik, P. K., Chatterji, B. P., Vangapandu, S. N., Aneja, R., Chandra, R., Kanteveri, S., & Joshi, H. C. (2011). Rational design, synthesis and biological evaluations of amino-noscapine: A high affinity tubulin-binding noscapinoid. Journal of Computer-Aided Molecular Design, 25(5), 443–454. https://doi.org/10.1007/s10822-011-9430-4
  • Naik, P. K., Lopus, M., Aneja, R., Vangapandu, S. N., & Joshi, H. C. (2012). In silico inspired design and synthesis of a novel tubulin-binding anti-cancer drug: Folate conjugated noscapine (Targetin). Journal of Computer-Aided Molecular Design, 26(2), 233–247. https://doi.org/10.1007/s10822-011-9508-z
  • Nushtaeva, A. A., Karpushina, A. A., Ermakov, M. S., Gulyaeva, L. F., Gerasimov, A. V., Sidorov, S. V., Gayner, T. A., Yunusova, A. Y., Tkachenko, A. V., Richter, V. A., & Koval, O. A. (2019). Establishment of primary human breast cancer cell lines using "pulsed hypoxia" method and development of metastatic tumor model in immunodeficient mice. Cancer Cell International, 19(1), 46. https://doi.org/10.1186/s12935-019-0766-5
  • Oliva, M. A., Prota, A. E., Rodríguez-Salarichs, J., Bennani, Y. L., Jiménez-Barbero, J., Bargsten, K., Canales, Á., Steinmetz, M. O., & Díaz, J. F. (2020). Structural basis of noscapine activation for tubulin binding. Journal of Medicinal Chemistry, 63(15), 8495–8501. https://doi.org/10.1021/acs.jmedchem.0c00855
  • Osborne, C. K. (1998). Tamoxifen in the treatment of breast cancer. The New England Journal of Medicine, 339(22), 1609–1618. https://doi.org/10.1056/NEJM199811263392207
  • Pace, A., Bove, L., Nisticò, C., Ranuzzi, M., Innocenti, P., Pietrangeli, A., Terzoli, E., & Jandolo, B. (1996). Vinorelbine neurotoxicity: Clinical and neurophysiological findings in 23 patients. Journal of Neurology, Neurosurgery, and Psychiatry, 61(4), 409–411. https://doi.org/10.1136/jnnp.61.4.409
  • Panda, D., Chakrabarti, G., Hudson, J., Pigg, K., Miller, H. P., Wilson, L., & Himes, R. H. (2000). Suppression of microtubule dynamic instability and treadmilling by deuterium oxide. Biochemistry, 39(17), 5075–5081. https://doi.org/10.1021/bi992217f
  • Patel, A. K., Meher, R. K., Reddy, P. K., Pedapati, R. K., Pragyandipta, P., Kantevari, S., Naik, M. R., & Naik, P. K. (2021). Rational design, chemical synthesis and cellular evaluation of novel 1,3-diynyl derivatives of noscapine as potent tubulin binding anticancer agents. Journal of Molecular Graphics & Modelling, 106, 107933. https://doi.org/10.1016/j.jmgm.2021.107933
  • Pietro, W. J., Francl, M. M., Hehre, W. J., DeFrees, D. J., Pople, J. A., & Binkley, J. S. (1982). Self-consistent molecular orbital methods. 24. Supplemented small split-valence basis sets for second-row elements. Journal of the American Chemical Society, 104(19), 5039–5048. https://doi.org/10.1021/ja00383a007
  • Polak, E., & Ribiere, G. (1969). Note sur la Convergence de Methodes de Directions Conjuguees. Revue Francaise Inf Rech Oper. Serie Rouge, 16, 35–43.
  • Rahbar Saadat, Y., Saeidi, N., Zununi Vahed, S., Barzegari, A., & Barar, J. (2015). An update to DNA ladder assay for apoptosis detection. BioImpacts: BI, 5(1), 25–28. https://doi.org/10.15171/bi.2015.01
  • Rieger, A. M., Nelson, K. L., Konowalchuk, J. D., & Barreda, D. R. (2011). Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death. Journal of Visualized Experiments, 24(50), 2597. https://doi.org/10.3791/2597
  • Rowinsky, E. K., & Donehower, R. C. (1991). The clinical pharmacology and use of antimicrotubule agents in cancer chemotherapeutics. Pharmacology & Therapeutics, 52(1), 35–84. https://doi.org/10.1016/0163-7258(91)90086-2
  • Santoshi, S., & Naik, P. K. (2014). Molecular insight of isotypes specific β-tubulin interaction of tubulin heterodimer with noscapinoids. Journal of Computer-Aided Molecular Design, 28(7), 751–763. https://doi.org/10.1007/s10822-014-9756-9
  • Santoshi, S., Manchukonda, N. K., Suri, C., Sharma, M., Sridhar, B., Joseph, S., Lopus, M., Kantevari, S., Baitharu, I., & Naik, P. K. (2015). Rational design of biaryl pharmacophore inserted noscapine derivatives as potent tubulin binding anticancer agents. Journal of Computer-Aided Molecular Design, 29(3), 249–270. https://doi.org/10.1007/s10822-014-9820-5
  • Santoshi, S., Naik, P. K., & Joshi, H. C. (2011). Rational design of novel anti-microtubule agent (9-azido-noscapine) from quantitative structure activity relationship (QSAR) evaluation of noscapinoids. Journal of Biomolecular Screening, 16(9), 1047–1058. https://doi.org/10.1177/1087057111418654
  • Sertel, S., Eichhorn, T., Plinkert, P. K., & Efferth, T. (2011). Cytotoxicity of Thymus vulgaris essential oil towards human oral cavity squamous cell carcinoma. Anticancer Research, 31(1), 81–87.
  • Shi, W., & Lei, A. (2014). 1, 3-Diyne chemistry: Synthesis and derivations. Tetrahedron Letters, 55(17), 2763–2772. https://doi.org/10.1016/j.tetlet.2014.03.022
  • Theiss, C., & Meller, K. (2000). Taxol impairs anterograde axonal transport of microinjected horseradish peroxidase in dorsal root ganglia neurons in vitro. Cell and Tissue Research, 299(2), 213–224. https://doi.org/10.1007/s004419900120
  • Topp, K. S., Tanner, K. D., & Levine, J. D. (2000). Damage to the cytoskeleton of large diameter sensory neurons and myelinated axons in vincristine-induced painful peripheral neuropathy in the rat. The Journal of Comparative Neurology, 424(4), 563–576. https://doi.org/10.1002/1096-9861(20000904)424:4<563::AID-CNE1>3.0.CO;2-U
  • Verma, P., Manchukonda, N. K., Kantevari, S., & Lopus, M. (2021). Induction of microtubule hyper stabilization and robust G2/M arrest by N-4-CN in human breast carcinoma MDA-MB-231 cells. Fundamental & Clinical Pharmacology. https://doi.org/10.1111/fcp.12660. Epub ahead of print. PMID: 33576046
  • Verma, P., Nagireddy, P., Prassanawar, S. S., Nirmala, J. G., Gupta, A., Kantevari, S., & Lopus, M. (2020). 9-PAN promotes tubulin- and ROS-mediated cell death in human triple-negative breast cancer cells. The Journal of Pharmacy and Pharmacology, 72(11), 1585–1594. https://doi.org/10.1111/jphp.13349
  • Wang, Y., O'Brate, A., Zhou, W., & Giannakakou, P. (2005). Resistance to microtubule-stabilizing drugs involves two events: Beta-tubulin mutation in one allele followed by loss of the second allele. Cell Cycle (Georgetown, TX), 4(12), 1847–1853. https://doi.org/10.4161/cc.4.12.2264
  • Wang, Y., Schmid-Bindert, G., & Zhou, C. (2012). Erlotinib in the treatment of advanced non-small cell lung cancer: An update for clinicians. Therapeutic Advances in Medical Oncology, 4(1), 19–29. https://doi.org/10.1177/1758834011427927
  • Warolin, C. (1999). Pierre-Jean Robiquet: (Rennes, 14 janvier 1780 - Paris, 29 avril 1840) [Pierre-Jean Robiquet. Revue D'histoire de la Pharmacie, 87(321), 97–110. https://doi.org/10.3406/pharm.1999.4935
  • Ye, K., Ke, Y., Keshava, N., Shanks, J., Kapp, J. A., Tekmal, R. R., Petros, J., & Joshi, H. C. (1998). Opium alkaloid noscapine is an antitumor agent that arrests metaphase and induces apoptosis in dividing cells. Proceedings of the National Academy of Sciences of the United States of America, 95(4), 1601–1606. https://doi.org/10.1073/pnas.95.4.1601
  • Zhou, J., Liu, M., Aneja, R., Chandra, R., Lage, H., & Joshi, H. C. (2006). Reversal of P-glycoprotein-mediated multidrug resistance in cancer cells by the c-Jun NH2-terminal kinase. Cancer Research, 66(1), 445–452. https://doi.org/10.1158/0008-5472.CAN-05-1779

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.