Structure and dynamics of inactive and active MARK4: conformational switching through the activation process

References

• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. doi: 10.1016/j.softx.2015.06.001
   Google Scholar
• Ahrari, S., Mogharrab, N., & Navapour, L. (2017). Interconversion of inactive to active conformation of MARK2: Insights from molecular modeling and molecular dynamics simulation. Archives of Biochemistry and Biophysics, 630, 66–80. doi: 10.1016/j.abb.2017.07.002
   PubMed Web of Science ®Google Scholar
• Ando, K., Maruko-Otake, A., Ohtake, Y., Hayashishita, M., Sekiya, M., & Iijima, K. M. (2016). Stabilization of microtubule-unbound tau via tau phosphorylation at Ser262/356 by Par-1/MARK contributes to augmentation of AD-related phosphorylation and Aβ42-induced tau toxicity. PLoS Genetics, 12(3), e1005917. doi: 10.1371/journal.pgen.1005917
   PubMed Web of Science ®Google Scholar
• Angrand, P.-O., Segura, I., Völkel, P., Ghidelli, S., Terry, R., Brajenovic, M., … Acker-Palmer, A. (2006). Transgenic mouse proteomics identifies new 14-3-3-associated proteins involved in cytoskeletal rearrangements and cell signaling. Molecular and Cellular Proteomics, 5(12), 2211–2227. doi: 10.1074/mcp.M600147-MCP200
   PubMed Web of Science ®Google Scholar
• Barouch-Bentov, R., Che, J., Lee, C. C., Yang, Y., Herman, A., Jia, Y., … Sauer, K. (2009). A conserved salt bridge in the G loop of multiple protein kinases is important for catalysis and for in vivo Lyn function. Molecular Cell, 33(1), 43–52. doi: 10.1016/j.molcel.2008.12.024
   PubMed Web of Science ®Google Scholar
• Beghini, A., Magnani, I., Roversi, G., Piepoli, T., Terlizzi, S. D., Moroni, R. F., … Larizza, L. (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(17), 2581–2591.
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J., Postma, J. V., van Gunsteren, W. F., DiNola, A., & Haak, J. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. doi: 10.1063/1.448118
   Web of Science ®Google Scholar
• Berteotti, A., Cavalli, A., Branduardi, D., Gervasio, F. L., Recanatini, M., & Parrinello, M. (2009). Protein conformational transitions: The closure mechanism of a kinase explored by atomistic simulations. Journal of the American Chemical Society, 131(1), 244–250. doi: 10.1021/ja806846q
   PubMed Web of Science ®Google Scholar
• Böhm, H., Brinkmann, V., Drab, M., Henske, A., & Kurzchalia, T. V. (1997). Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Current Biology, 7(8), 603–606. doi: 10.1016/S0960-9822(06)00260-0
   PubMed Web of Science ®Google Scholar
• Bossemeyer, D. (1994). The glycine-rich sequence of protein kinases: A multifunctional element. Trends in Biochemical Sciences, 19(5), 201–205. doi: 10.1016/0968-0004(94)90022-1
   PubMed Web of Science ®Google Scholar
• Brajenovic, M., Joberty, G., Küster, B., Bouwmeester, T., & Drewes, G. (2004). Comprehensive proteomic analysis of human Par protein complexes reveals an interconnected protein network. Journal of Biological Chemistry, 279(13), 12804–12811. doi: 10.1074/jbc.M312171200
   PubMed Web of Science ®Google Scholar
• Bright, N., Thornton, C., & Carling, D. (2009). The regulation and function of mammalian AMPK-related kinases. Acta Physiologica (Oxford, England), 196(1), 15–26. doi: 10.1111/j.1748-1716.2009.01971.x
   PubMed Web of Science ®Google Scholar
• Chen, L., Jiao, Z.-H., Zheng, L.-S., Zhang, Y.-Y., Xie, S.-T., Wang, Z.-X., & Wu, J.-W. (2009). Structural insight into the autoinhibition mechanism of AMP-activated protein kinase. Nature, 459(7250), 1146–1149. doi: 10.1038/nature08075
   PubMed Web of Science ®Google Scholar
• Cheung, J., Ginter, C., Cassidy, M., Franklin, M. C., Rudolph, M. J., Robine, N., … Hendrickson, W. A. (2015). Structural insights into mis-regulation of protein kinase A in human tumors. Proceedings of the National Academy of Sciences United States of America, 112(5), 1374–1379. doi: 10.1073/pnas.1424206112
   PubMed Web of Science ®Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science, 2(9), 1511–1519. doi: 10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅ log (N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. doi: 10.1063/1.464397
   Web of Science ®Google Scholar
• Dolan, P. J., & Johnson, G. V. (2010). The role of tau kinases in Alzheimer's disease. Current Opinion in Drug Discovery and Development, 13(5), 595–603.
   PubMedGoogle Scholar
• Drewes, G. (2004). MARKing tau for tangles and toxicity. Trends in Biochemical Sciences, 29(10), 548–555. doi: 10.1016/j.tibs.2004.08.001
   PubMed Web of Science ®Google Scholar
• Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E.-M., & Mandelkow, E. (1997). MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell, 89(2), 297–308. doi: 10.1016/S0092-8674(00)80208-1
   PubMed Web of Science ®Google Scholar
• Durrant, J. D., Votapka, L., Sørensen, J., & Amaro, R. E. (2014). POVME 2.0: An enhanced tool for determining pocket shape and volume characteristics. Journal of Chemical Theory and Computation, 10(11), 5047–5056. doi: 10.1021/ct500381c
   PubMed Web of Science ®Google Scholar
• Echols, N., Milburn, D., & Gerstein, M. (2003). MolMovDB: Analysis and visualization of conformational change and structural flexibility. Nucleic Acids Research, 31(1), 478–482. doi: 10.1093/nar/gkg104
   PubMed Web of Science ®Google Scholar
• Eisenberg, D., Lüthy, R., & Bowie, J. U. (1997). VERIFY3D: Assessment of protein models with three-dimensional profiles. Methods in Enzymology, 277, 396–404.
   PubMed Web of Science ®Google Scholar
• Endicott, J. A., Noble, M. E., & Johnson, L. N. (2012). The structural basis for control of eukaryotic protein kinases. Annual Review of Biochemistry, 81(1), 587–613. doi: 10.1146/annurev-biochem-052410-090317
   PubMedGoogle Scholar
• Espinosa, L., & Navarro, E. (1998). Human serine/threonine protein kinase EMK1: Genomic structure and cDNA cloning of isoforms produced by alternative splicing. Cytogenetic and Genome Research, 81(3-4), 278–282. doi: 10.1159/000015046
   Google Scholar
• Fischer, D., Mukrasch, M. D., Biernat, J., Bibow, S., Blackledge, M., Griesinger, C., … Zweckstetter, M. (2009). Conformational changes specific for pseudophosphorylation at serine 262 selectively impair binding of tau to microtubules. Biochemistry, 48(42), 10047–10055. doi: 10.1021/bi901090m
   PubMed Web of Science ®Google Scholar
• Fiser, A., Do, R. K., & Sali, A. (2000). Modeling of loops in protein structures. Protein Science: A Publication of the Protein Society, 9(9), 1753–1773. doi: 10.1110/ps.9.9.1753
   PubMed Web of Science ®Google Scholar
• Gu, G. J., Lund, H., Wu, D., Blokzijl, A., Classon, C., von Euler, G., … Kamali-Moghaddam, M. (2013). Role of individual MARK isoforms in phosphorylation of tau at Ser262 in Alzheimer’s disease. NeuroMolecular Medicine, 15(3), 458–469. doi: 10.1007/s12017-013-8232-3
   PubMed Web of Science ®Google Scholar
• Hanks, S. K., & Hunter, T. (1995). Protein kinases 6. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. The FASEB Journal, 9(8), 576–596. doi: 10.1096/fasebj.9.8.7768349
   PubMed Web of Science ®Google Scholar
• Hemmer, W., McGlone, M., Tsigelny, I., & Taylor, S. S. (1997). Role of the glycine triad in the ATP-binding site of cAMP-dependent protein kinase. Journal of Biological Chemistry, 272(27), 16946–16954. doi: 10.1074/jbc.272.27.16946
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. doi: 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
   Web of Science ®Google Scholar
• Huang, H., Zhao, R., Dickson, B. M., Skeel, R. D., & Post, C. B. (2012). αC helix as a switch in the conformational transition of Src/CDK-like kinase domains. The Journal of Physical Chemistry B, 116(15), 4465–4475. doi: 10.1021/jp301628r
   PubMed Web of Science ®Google Scholar
• Huang, J., & MacKerell, A. D. (2013). CHARMM36 all‐atom additive protein force field: Validation based on comparison to NMR data. Journal of Computational Chemistry, 34(25), 2135–2145. doi: 10.1002/jcc.23354
   PubMed Web of Science ®Google Scholar
• Hurov, J. B., Watkins, J. L., & Piwnica-Worms, H. (2004). Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Current Biology, 14(8), 736–741. doi: 10.1016/j.cub.2004.04.007
   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(7), 1845–1868. doi: 10.1039/C3MB70591A
   PubMedGoogle Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen‐bonded and geometrical features. Biopolymers, 22(12), 2577–2637. doi: 10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Kaldis, P., Tsakraklides, V., Ross, K. E., Winter, E., & Cheng, A. (2002). Activating phosphorylation of cyclin-dependent kinases in budding yeast. Austin, TX: Landes Bioscience.
   Google Scholar
• Kato, T., Satoh, S., Okabe, H., Kitahara, O., Ono, K., Kihara, C., … Furukawa, Y. (2001). Isolation of a novel human gene, MARKLI, homologous to MARK3 and its involvement in hepatocellular carcinogenesis. Neoplasia, 3(1), 4–9. doi: 10.1038/sj.neo.7900132
   PubMed Web of Science ®Google Scholar
• Knight, J. D., Qian, B., Baker, D., & Kothary, R. (2007). Conservation, variability and the modeling of active protein kinases. PLoS One, 2(10), e982. doi: 10.1371/journal.pone.0000982
   PubMed Web of Science ®Google Scholar
• Kornev, A. P., Haste, N. M., Taylor, S. S., & Ten Eyck, L. F. (2006). Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proceedings of the National Academy of Sciences United States of America, 103(47), 17783–17788. doi: 10.1073/pnas.0607656103
   PubMed Web of Science ®Google Scholar
• Kornev, A. P., Taylor, S. S., & Ten Eyck, L. F. (2008). A helix scaffold for the assembly of active protein kinases. Proceedings of the National Academy of Sciences United States of America, 105(38), 14377–14382. doi: 10.1073/pnas.0807988105
   PubMed Web of Science ®Google Scholar
• Krupa, A., Preethi, G., & Srinivasan, N. (2004). Structural modes of stabilization of permissive phosphorylation sites in protein kinases: Distinct strategies in Ser/Thr and Tyr kinases. Journal of Molecular Biology, 339(5), 1025–1039. doi: 10.1016/j.jmb.2004.04.043
   PubMed Web of Science ®Google Scholar
• Kuzmanic, A., Sutto, L., Saladino, G., Nebreda, A. R., Gervasio, F. L., & Orozco, M. (2017). Changes in the free-energy landscape of p38α MAP kinase through its canonical activation and binding events as studied by enhanced molecular dynamics simulations. eLife, 6, e22175. doi: 10.7554/eLife.22175
   PubMed Web of Science ®Google Scholar
• Li, F., Gangal, M., Juliano, C., Gorfain, E., Taylor, S. S., & Johnson, D. A. (2002). Evidence for an internal entropy contribution to phosphoryl transfer: A study of domain closure, backbone flexibility, and the catalytic cycle of cAMP-dependent protein kinase. Journal of Molecular Biology, 315(3), 459–469. doi: 10.1006/jmbi.2001.5256
   PubMed Web of Science ®Google Scholar
• Lizcano, J. M., Göransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., … Alessi, D. R. (2004). LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1 . The EMBO Journal, 23(4), 833–843. doi: 10.1038/sj.emboj.7600110
   PubMed Web of Science ®Google Scholar
• Lovell, S. C., Davis, I. W., Arendall, W. B., de Bakker, P. I. W., Word, J. M., Prisant, M. G., … Richardson, D. C. (2003). Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins: Structure, Function, and Bioinformatics, 50(3), 437–450. doi: 10.1002/prot.10286
   PubMed Web of Science ®Google Scholar
• Lund, H., Gustafsson, E., Svensson, A., Nilsson, M., Berg, M., Sunnemark, D., & von Euler, G. (2014). MARK4 and MARK3 associate with early tau phosphorylation in Alzheimer’s disease granulovacuolar degeneration bodies. Acta Neuropathologica Communications, 2(1), 22. doi: 10.1186/2051-5960-2-22
   PubMedGoogle Scholar
• Magnani, I., Novielli, C., Fontana, L., Tabano, S., Rovina, D., Moroni, R. F., … Larizza, L. (2011). Differential signature of the centrosomal MARK4 isoforms in glioma. Analytical Cellular Pathology, 34(6), 319–338. doi: 10.1155/2011/206756
   Web of Science ®Google Scholar
• Martínez, A., Castro, A., & Medina, M. (2006). Glycogen synthase kinase 3 (GSK-3) and its inhibitors: Drug discovery and development. Hoboken, NJ: John Wiley and Sons.
   Google Scholar
• Marx, A., Nugoor, C., Müller, J., Panneerselvam, S., Timm, T., Bilang, M., … Mandelkow, E. (2006). Structural variations in the catalytic and ubiquitin-associated domains of microtubule-associated protein/microtubule affinity regulating kinase (MARK) 1 and MARK2. Journal of Biological Chemistry, 281(37), 27586–27599. doi: 10.1074/jbc.M604865200
   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(6), 1637–1648. doi: 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(7), 332–342. doi: 10.1016/j.tibs.2009.03.008
   PubMed Web of Science ®Google Scholar
• Neić, D., Miller, M. C., Quinkert, Z. T., Stein, M., Chait, B. T., & Stebbins, C. E. (2010). Helicobacter pylori CagA inhibits PAR1-MARK family kinases by mimicking host substrates. Nature Structural and Molecular Biology, 17(1), 130–132.
   PubMed Web of Science ®Google Scholar
• Noble, M. E., Endicott, J. A., & Johnson, L. N. (2004). Protein kinase inhibitors: Insights into drug design from structure. Science, 303(5665), 1800–1805. doi: 10.1126/science.1095920
   PubMed Web of Science ®Google Scholar
• Nolen, B., Taylor, S., & Ghosh, G. (2004). Regulation of protein kinases: Controlling activity through activation segment conformation. Molecular Cell, 15(5), 661–675. doi: 10.1016/j.molcel.2004.08.024
   PubMed Web of Science ®Google Scholar
• Panneerselvam, S., Marx, A., Mandelkow, E.-M., & Mandelkow, E. (2006). Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure, 14(2), 173–183. doi: 10.1016/j.str.2005.09.022
   PubMed Web of Science ®Google Scholar
• Pardo, O. E., Castellano, L., Munro, C. E., Hu, Y., Mauri, F., Krell, J., … Stebbing, J. (2016). miR-515-5p controls cancer cell migration through MARK4 regulation. EMBO Reports, 17(4), 570–584. doi: 10.15252/embr.201540970
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. doi: 10.1063/1.328693
   Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera—a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. doi: 10.1002/jcc.20084
   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(2), 129–134.
   PubMedGoogle Scholar
• Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234(3), 779–815. doi: 10.1006/jmbi.1993.1626
   PubMed Web of Science ®Google Scholar
• Schlosser, A., Hamann, A., Bossemeyer, D., Schneider, E., & Bakker, E. P. (1993). NAD+ binding to the Escherichia coli K+‐uptake protein TrkA and sequence similarity between TrkA and domains of a family of dehydrogenases suggest a role for NAD + in bacterial transport. Molecular Microbiology, 9(3), 533–543. doi: 10.1111/j.1365-2958.1993.tb01714.x
   PubMed Web of Science ®Google Scholar
• Shan, Y., Arkhipov, A., Kim, E. T., Pan, A. C., & Shaw, D. E. (2013). Transitions to catalytically inactive conformations in EGFR kinase. Proceedings of the National Academy of Sciences of Sciences United States of America, 110(18), 7270–7275. doi: 10.1073/pnas.1220843110
   PubMed Web of Science ®Google Scholar
• Shan, Y., Seeliger, M. A., Eastwood, M. P., Frank, F., Xu, H., Jensen, M. O., … Shaw, D. E. (2009). A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proceedings of the National Academy of Sciences of Sciences United States of America, 106(1), 139–144. doi: 10.1073/pnas.0811223106
   PubMed Web of Science ®Google Scholar
• Shukla, D., Meng, Y., Roux, B., & Pande, V. S. (2014). Activation pathway of Src kinase reveals intermediate states as novel targets for drug design. Nature Communications, 5(1), 3397. doi: 10.1038/ncomms4397
   PubMedGoogle Scholar
• Trinczek, B., Brajenovic, M., Ebneth, A., & Drewes, G. (2004). MARK4 is a novel microtubule-associated proteins/microtubule affinity-regulating kinase that binds to the cellular microtubule network and to centrosomes. Journal of Biological Chemistry, 279(7), 5915–5923. doi: 10.1074/jbc.M304528200
   PubMed Web of Science ®Google Scholar
• Wang, J.-W., Imai, Y., & Lu, B. (2007). Activation of PAR-1 kinase and stimulation of tau phosphorylation by diverse signals require the tumor suppressor protein LKB1. Journal of Neuroscience, 27(3), 574–581. doi: 10.1523/JNEUROSCI.5094-06.2007
   PubMed Web of Science ®Google Scholar
• Wilson, K. P., Fitzgibbon, M. J., Caron, P. R., Griffith, J. P., Chen, W., McCaffrey, P. G., … Su, M. S.-S. (1996). Crystal structure of p38 mitogen-activated protein kinase. Journal of Biological Chemistry, 271(44), 27696–27700. doi: 10.1074/jbc.271.44.27696
   PubMed Web of Science ®Google Scholar
• Zhang, F., Strand, A., Robbins, D., Cobb, M. H., & Goldsmith, E. J. (1994). Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature, 367(6465), 704–711. doi: 10.1038/367704a0
   PubMed Web of Science ®Google Scholar