Identification and evaluation of bioactive natural products as potential inhibitors of human microtubule affinity-regulating kinase 4 (MARK4)

References

• Annadurai, N. , Agrawal, K. , Dzubak, P. , Hajduch, M. , & Das, V. (2017). Microtubule affinity-regulating kinases are potential druggable targets for Alzheimer’s disease. Cellular and Molecular Life Sciences , 74 , 4159–4169.10.1007/s00018-017-2574-1
   PubMed Web of Science ®Google Scholar
• Arash, E. H. , Shiban, A. , Song, S. , & Attisano, L. (2017). MARK4 inhibits Hippo signaling to promote proliferation and migration of breast cancer cells. EMBO Reports , e201642455.
   Web of Science ®Google Scholar
• Beghini, A. , Magnani, I. , Roversi, G. , Piepoli, T. , Di Terlizzi, S. , Moroni, R. F. , … Finocchiaro, G. (2003). The neural progenitor-restricted isoform of the MARK4 gene in 19q13. 2 is upregulated in human gliomas and overexpressed in a subset of glioblastoma cell lines. Oncogene , 22 , 2581–2591.10.1038/sj.onc.1206336
   PubMed Web of Science ®Google Scholar
• Biovia, D. S. (2015). Discovery studio modeling environment . San Diego, CA : Dassault Systemes.
   Google Scholar
• Daina, A. , Michielin, O. & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. 7 : 42717.
   Google Scholar
• Devika, N. T. , Amresh, P. , Hassan, M. I. , & Ali, B. M. (2014). Molecular modeling and simulation of the human eNOS reductase domain, an enzyme involved in the release of vascular nitric oxide. Journal of Molecular Modeling , 20 , 2470.10.1007/s00894-014-2470-7
   PubMed Web of Science ®Google Scholar
• Gabrovska, P. , Smith, R. , Tiang, T. , Weinstein, S. , Haupt, L. M. , & Griffiths, L. R. (2012). Development of an eight gene expression profile implicating human breast tumours of all grade. Molecular Biology Reports , 39 , 3879–3892.10.1007/s11033-011-1167-6
   PubMed Web of Science ®Google Scholar
• Gramany, V. , Khan, F. I. , Govender, A. , Bisetty, K. , Singh, S. , & Permaul, K. (2016). Cloning, expression, and molecular dynamics simulations of a xylosidase obtained from Thermomyces lanuginosus. Journal of Biomolecular Structure and Dynamics , 34 , 1681–1692.10.1080/07391102.2015.1089186
   PubMed Web of Science ®Google Scholar
• Guex, N. , & Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis , 18 , 2714–2723.10.1002/(ISSN)1522-2683
   PubMed Web of Science ®Google Scholar
• Harvey, A. L. (2008). Natural products in drug discovery. Drug Discovery Today , 13 , 894–901.10.1016/j.drudis.2008.07.004
   PubMed Web of Science ®Google Scholar
• Hoda, N. , Naz, H. , Jameel, E. , Shandilya, A. , Dey, S. , Hassan, M. I. , … Jayaram, B. (2016). Curcumin specifically binds to the human calcium-calmodulin-dependent protein kinase IV: Fluorescence and molecular dynamics simulation studies. Journal of Biomolecular Structure and Dynamics , 34 , 572–584.10.1080/07391102.2015.1046934
   PubMed Web of Science ®Google Scholar
• Hubbard, R. E. , & Kamran Haider, M. (2010). Hydrogen bonds in proteins: Role and strength . eLS . Wiley.
   Google Scholar
• Humphrey, W. , Dalke, A. , & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics , 14 , 33–38.10.1016/0263-7855(96)00018-5
   PubMed Web of Science ®Google Scholar
• Irwin, J. J. , & Shoichet, B. K. (2005). ZINC − A free database of commercially available compounds for virtual screening. Journal of Chemical Information and Modeling , 45 , 177–182.10.1021/ci049714+
   PubMed Web of Science ®Google Scholar
• Jameel, E. , Naz, H. , Khan, P. , Tarique, M. , Kumar, J. , Mumtazuddin, S. , … Hassan, M. I. (2017). Design, synthesis, and biological evaluation of pyrimidine derivatives as potential inhibitors of human calcium/calmodulin-dependent protein kinase IV. Chemical Biology & Drug Design , 89 , 741–754.10.1111/cbdd.2017.89.issue-5
   PubMed Web of Science ®Google Scholar
• Jenardhanan, P. , Mannu, J. , & Mathur, P. P. (2014). The structural analysis of MARK4 and the exploration of specific inhibitors for the MARK family: A computational approach to obstruct the role of MARK4 in prostate cancer progression. Molecular Biosystems , 10 , 1845–1868.10.1039/C3MB70591A
   PubMed Web of Science ®Google Scholar
• Khan, F. I. , Shahbaaz, M. , Bisetty, K. , Waheed, A. , Sly, W. S. , Ahmad, F. , & Hassan, M. I. (2016). Large scale analysis of the mutational landscape in beta-glucuronidase: A major player of mucopolysaccharidosis type VII. Gene , 576 , 36–44.10.1016/j.gene.2015.09.062
   PubMed Web of Science ®Google Scholar
• Khan, F. I. , Wei, D. Q. , Gu, K. R. , Hassan, M. I. , & Tabrez, S. (2016). Current updates on computer aided protein modeling and designing. International Journal of Biological Macromolecules , 85 , 48–62.10.1016/j.ijbiomac.2015.12.072
   PubMed Web of Science ®Google Scholar
• Khan, P. , Rahman, S. , Queen, A. , Manzoor, S. , Naz, F. , Hasan, G. M. , … Hassan, M. I. (2017). Elucidation of dietary polyphenolics as potential inhibitor of microtubule affinity regulating kinase 4: In silico and in vitro studies. Scientific Reports , 7 , 1912.10.1038/s41598-017-09941-4
   PubMed Web of Science ®Google Scholar
• Khan, S. , Khan, F. I. , Mohammad, T. , Khan, P. , Hasan, G. M. , Lobb, K. A. , … Imtaiyaz Hassan, M. (2018). Exploring molecular insights into the interaction mechanism of cholesterol derivatives with the Mce4A: A combined spectroscopic and molecular dynamic simulation studies. International Journal of Biological Macromolecules , 111 , 548–560.10.1016/j.ijbiomac.2017.12.160
   PubMed Web of Science ®Google Scholar
• Kumari, R. , Kumar, R. , & Lynn, A. (2014). g_mmpbsa – A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling , 54 , 1951–1962.10.1021/ci500020 m
   PubMed Web of Science ®Google Scholar
• Kuzmanic, A. , & Zagrovic, B. (2010). Determination of ensemble-average pairwise root mean-square deviation from experimental B-factors. Biophysical Journal , 98 , 861–871.10.1016/j.bpj.2009.11.011
   PubMed Web of Science ®Google Scholar
• Lee, S. , Lee, I. , Kim, H. , Chang, G. , Chung, J. , & No, K. (2003). The PreADME approach: Web-based program for rapid prediction of physico-chemical, drug absorption and drug-like properties. EuroQSAR 2002 Designing Drugs and Crop Protectants: Processes, problems and solutions 2003 : 418–420.
   Google Scholar
• Lipinski, C. A. , Lombardo, F. , Dominy, B. W. , & Feeney, P. J. (2001). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews , 46 , 3–26.10.1016/S0169-409X(00)00129-0
   PubMed Web of Science ®Google Scholar
• Maisuradze, G. G. , Liwo, A. , & Scheraga, H. A. (2009). Principal component analysis for protein folding dynamics. Journal of Molecular Biology , 385 , 312–329.10.1016/j.jmb.2008.10.018
   PubMed Web of Science ®Google Scholar
• Manning, G.D. B. W. , R. Martinez , T. Hunter , S. Sudarsanam (2002). The protein kinase complement of the human genome. Science , 298 , 1912–1934.10.1126/science.1075762
   PubMed Web of Science ®Google Scholar
• Marx, A. , Nugoor, C. , Panneerselvam, S. , & Mandelkow, E. (2010). Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases. The FASEB Journal , 24 , 1637–1648.10.1096/fj.09-148064
   PubMed Web of Science ®Google Scholar
• Matenia, D. , & Mandelkow, E. M. (2009). The tau of MARK: A polarized view of the cytoskeleton. Trends in Biochemical Sciences , 34 , 33–342.
   PubMed Web of Science ®Google Scholar
• Mazola, Y. , Guirola, O. , Palomares, S. , Chinea, G. , Menendez, C. , Hernandez, L. , & Musacchio, A. (2015). A comparative molecular dynamics study of thermophilic and mesophilic beta-fructosidase enzymes. Journal of Molecular Modeling , 21 , 2772.
   Web of Science ®Google Scholar
• Morris, G. M. , Huey, R. , Lindstrom, W. , Sanner, M. F. , Belew, R. K. , Goodsell, D. S. , & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry , 30 , 2785–2791.10.1002/jcc.v30:16
   PubMed Web of Science ®Google Scholar
• Naiyer, A. , Hassan, M. I. , Islam, A. , Sundd, M. , & Ahmad, F. (2015). Structural characterization of MG and pre-MG states of proteins by MD simulations, NMR, and other techniques. Journal of Biomolecular Structure and Dynamics , 33 , 2267–2284.10.1080/07391102.2014.999354
   PubMed Web of Science ®Google Scholar
• Naz, F. , Anjum, F. , Islam, A. , Ahmad, F. , & Hassan, M. I. (2013). Microtubule affinity-regulating kinase 4: Structure, function, and regulation. Cell Biochemistry and Biophysics , 67 , 485–499.10.1007/s12013-013-9550-7
   PubMed Web of Science ®Google Scholar
• Naz, F. , Islam, A. , Ahmad, F. , & Hassan, M. I. (2015). Atypical PKC phosphorylates microtubule affinity-regulating kinase 4 in vitro. Molecular and Cellular Biochemistry , 410 , 223–228.10.1007/s11010-015-2555-3
   PubMed Web of Science ®Google Scholar
• Naz, F. , Shahbaaz, M. , Bisetty, K. , Islam, A. , Ahmad, F. , & Hassan, M. I. (2015). Designing new kinase inhibitor derivatives as therapeutics against common complex diseases: Structural basis of microtubule affinity-regulating kinase 4 (MARK4) inhibition. OMICS , 19 , 700–711.10.1089/omi.2015.0111
   PubMed Web of Science ®Google Scholar
• Naz, F. , Shahbaaz, M. , Khan, S. , Bisetty, K. , Islam, A. , Ahmad, F. , & Hassan, M. I. (2015). PKR-inhibitor binds efficiently with human microtubule affinity-regulating kinase 4. Journal of Molecular Graphics and Modelling , 62 , 245–252.10.1016/j.jmgm.2015.10.009
   PubMed Web of Science ®Google Scholar
• Naz, H. , Jameel, E. , Hoda, N. , Shandilya, A. , Khan, P. , Islam, A. , … Hassan, M. I. (2016). Structure guided design of potential inhibitors of human calcium-calmodulin dependent protein kinase IV containing pyrimidine scaffold. Bioorganic & Medicinal Chemistry Letters , 26 , 782–788.10.1016/j.bmcl.2015.12.098
   PubMed Web of Science ®Google Scholar
• Naz, H. , Khan, P. , Tarique, M. , Rahman, S. , Meena, A. , Ahamad, S. , … Hassan, M. I. (2016). Binding studies and biological evaluation of beta-carotene as a potential inhibitor of human calcium/calmodulin-dependent protein kinase IV. International Journal of Biological Macromolecules , 96 , 161–170.
   PubMed Web of Science ®Google Scholar
• Naz, F. , Sami, N. , Islam, A. , Ahmad, F. , & Hassan, M. I. (2016). Ubiquitin-associated domain of MARK4 provides stability at physiological pH. International Journal of Biological Macromolecules , 93 , 1147–1154.10.1016/j.ijbiomac.2016.09.087
   PubMed Web of Science ®Google Scholar
• Naz, F. , Khan, F. I. , Mohammad, T. , Khan, P. , Manzoor, S. , Hasan, G. M. , … Hassan, M. I. (2018). Investigation of molecular mechanism of recognition between citral and MARK4: A newer therapeutic approach to attenuate cancer cell progression. International Journal of Biological Macromolecules , 107 , 2580–2589.10.1016/j.ijbiomac.2017.10.143
   PubMed Web of Science ®Google Scholar
• Naz, H. , Tarique, M. , Khan, P. , Luqman, S. , Ahamad, S. , Islam, A. , … Hassan, M. I. (2018). Evidence of vanillin binding to CAMKIV explains the anti-cancer mechanism in human hepatic carcinoma and neuroblastoma cells. Molecular and Cellular Biochemistry , 438 , 35–45.10.1007/s11010-017-3111-0
   PubMed Web of Science ®Google Scholar
• Newman, D. J. , & Cragg, G. M. (2007). Natural products as sources of new drugs over the last 25 years. Journal of Natural Products , 70 , 461–477.10.1021/np068054v
   PubMed Web of Science ®Google Scholar
• Newman, D. J. , & Cragg, G. M. (2016). Natural products as sources of new drugs from 1981 to 2014. Journal of Natural Products , 79 , 629–661.10.1021/acs.jnatprod.5b01055
   PubMed Web of Science ®Google Scholar
• Novielli, C. , Magnani, I. , Tabano, S. , Fontana, L. , Moroni, R. F. , Colombo, E. A. , … Mazzoleni, S. (2010). Dysregulated ratio between MARK4 L and S isoforms during glioma progression. Cancer Genetics and Cytogenetics , 203 , 45.10.1016/j.cancergencyto.2010.07.005
   Google Scholar
• Parveen, I. , Ahmed, N. , Idrees, D. , Khan, P. , & Hassan, M. I. (2017). Synthesis, estrogen receptor binding affinity and molecular docking of pyrimidine-piperazine-chromene and -quinoline conjugates. Bioorganic & Medicinal Chemistry Letters , 27 , 4493–4499.10.1016/j.bmcl.2017.07.077
   PubMed Web of Science ®Google Scholar
• Sack, J. S. , Gao, M. , Kiefer, S. E. , Myers, J. E. , Newitt, J. A. , Wu, S. , & Yan, C. (2016). Crystal structure of microtubule affinity-regulating kinase 4 catalytic domain in complex with a pyrazolopyrimidine inhibitor. Acta Crystallographica Section F: Structural Biology Communications , 72 , 129–134.
   PubMed Web of Science ®Google Scholar
• Sami, N. , Kumar, V. , & Hassan, M. I. (2018). Microtubule affinity regulating kinase-4. In S. Choi (Ed.), Encyclopedia of signaling molecules (pp. 3101–3116). Cham: Springer.10.1007/978-3-319-67199-4
   Google Scholar
• Schrödinger, L. (2016). The PyMOL molecular graphics system , Version 1.8 Schrödinger, LLC.
   Google Scholar
• Schuttelkopf, A. W. , & van Aalten, D. M. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica , 60 , 1355–1363.10.1107/S0907444904011679
   PubMed Web of Science ®Google Scholar
• Sun, C. , Tian, L. , Nie, J. , Zhang, H. , Han, X. , & Shi, Y. (2012). Inactivation of MARK4, an AMP-activated protein kinase (AMPK)-related kinase, leads to insulin hypersensitivity and resistance to diet-induced obesity. Journal of Biological Chemistry , 287 , 38305–38315.10.1074/jbc.M112.388934
   PubMed Web of Science ®Google Scholar
• Sun, W. , Lee, S. , Huang, X. , Liu, S. , Inayathullah, M. , Kim, K.-M. , … Rajadas, J. (2016). Attenuation of synaptic toxicity and MARK4/PAR1-mediated Tau phosphorylation by methylene blue for Alzheimer’s disease treatment. Scientific Reports 6 :34784.
   PubMed Web of Science ®Google Scholar
• Syed, S. B. , Khan, F. I. , Khan, S. H. , Srivastava, S. , Hasan, G. M. , Lobb, K. A. , … Hassan, M. I. (2018). Mechanistic insights into the urea-induced denaturation of kinase domain of human integrin linked kinase. International Journal of Biological Macromolecules , 111 , 208–218.10.1016/j.ijbiomac.2017.12.164
   PubMed Web of Science ®Google Scholar
• Thakur, P. K. , Kumar, J. , Ray, D. , Anjum, F. , & Hassan, M. I. (2013). Search of potential inhibitor against New Delhi metallo-beta-lactamase 1 from a series of antibacterial natural compounds. Journal of Natural Science, Biology and Medicine , 4 , 51–56.
   PubMedGoogle Scholar
• Tiana, G. , Simona, F. , De Mori, G. M. , Broglia, R. A. , & Colombo, G. (2004). Understanding the determinants of stability and folding of small globular proteins from their energetics. Protein Science , 13 , 113–124.10.1110/ps.03223804
   PubMed Web of Science ®Google Scholar
• Timm, T. , Balusamy, K. , Li, X. , Biernat, J. , Mandelkow, E. , & Mandelkow, E.-M. (2008). Glycogen synthase kinase (GSK) 3β directly phosphorylates serine 212 in the regulatory loop and inhibits microtubule affinity-regulating kinase (MARK) 2. Journal of Biological Chemistry , 283 , 18873–18882.10.1074/jbc.M706596200
   PubMed Web of Science ®Google Scholar
• Tochio, N. , Koshiba, S. , Kobayashi, N. , Inoue, M. , Yabuki, T. , Aoki, M. , … Motoda, Y. (2006). Solution structure of the kinase-associated domain 1 of mouse microtubule-associated protein/microtubule affinity-regulating kinase 3. Protein Science , 15 , 2534–2543.10.1110/(ISSN)1469-896X
   PubMed Web of Science ®Google Scholar
• 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 , 455–461.
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D. , Lindahl, E. , Hess, B. , Groenhof, G. , Mark, A. E. , & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry , 26 , 1701–1718.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Veber, D. F. , Johnson, S. R. , Cheng, H.-Y. , Smith, B. R. , Ward, K. W. , & Kopple, K. D. (2002). Molecular properties that influence the oral bioavailability of drug candidates. Journal of Medicinal Chemistry , 45 , 2615–2623.10.1021/jm020017n
   PubMed Web of Science ®Google Scholar
• Zhang, L. , Ai, H. , Chen, W. , Yin, Z. , Hu, H. , Zhu, J. , … Liu, H. (2017). CarcinoPred-EL: Novel models for predicting the carcinogenicity of chemicals using molecular fingerprints and ensemble learning methods. Scientific Reports , 7 , 2118.10.1038/s41598-017-02365-0
   PubMed Web of Science ®Google Scholar