Molecular insights into the structural and dynamical changes of calcium channel TRPV6 induced by its interaction with phosphatidylinositol 4,5-bisphosphate

References

• Ahamad, S., Ali, H., Secco, I., Giacca, M., & Gupta, D. (2022). Anti-fungal drug anidulafungin inhibits SARS-CoV-2 spike-induced syncytia formation by targeting ACE2-spike protein interaction. Frontiers in Genetics, 13, 866474.
   PubMed Web of Science ®Google Scholar
• Ahamad, S., Gupta, D., & Kumar, V. (2022). Targeting SARS-CoV-2 nucleocapsid oligomerization: Insights from molecular docking and molecular dynamics simulations. Journal of Biomolecular Structure & Dynamics, 40(6), 2430–2443. https://doi.org/10.1080/07391102.2020.1839563
   PubMed Web of Science ®Google Scholar
• Ahamad, S., Hema, K., & Gupta, D. (2021). Structural stability predictions and molecular dynamics simulations of RBD and HR1 mutations associated with SARS-CoV-2 spike glycoprotein. Journal of Biomolecular Structure and Dynamics, 23, 1–13. https://doi.org/10.1080/07391102.2021.1889671
   Google Scholar
• Ahamad, S., Islam, A., Ahmad, F., Dwivedi, N., & Hassan, M. I. (2019). 2/3D-QSAR, molecular docking and MD simulation studies of FtsZ protein targeting benzimidazoles derivatives. Computational Biology and Chemistry, 78, 398–413.
   PubMed Web of Science ®Google Scholar
• Balsera, M. A., Wriggers, W., Oono, Y., & Schulten, K. (1996). Principal component analysis and long-time protein dynamics. The Journal of Physical Chemistry, 100(7), 2567–2572. https://doi.org/10.1021/jp9536920
   Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. [Database] https://doi.org/10.1063/1.448118
   Web of Science ®Google Scholar
• Bödding, M., & Flockerzi, V. (2004). Ca2+ dependence of the Ca2+-selective TRPV6 channel. The Journal of Biological Chemistry, 279(35), 36546–36552.
   PubMed Web of Science ®Google Scholar
• Cai, R., Liu, X., Zhang, R., Hofmann, L., Zheng, W., Amin, M. R., Wang, L., Hu, Q., Peng, J. B., Michalak, M., Flockerzi, V., Ali, D. W., Chen, X. Z., & Tang, J. (2020). Autoinhibition of TRPV6 Channel and Regulation by PIP2. iScience, 23(9), 101444. https://doi.org/10.1016/j.isci.2020.101444
   PubMed Web of Science ®Google Scholar
• Case, D. A., Ben-Shalom, I. Y., Brozell, S. R., Cerutti, D. S., Cheatham, I., E, T., Cruzeiro, V. W. D., Darden, T. A., Duke, R. E., Ghoreishi, D., Gilson, M. K., Gohlke, H., Goetz, A. W., Greene, D., Harris, R., Homeyer, N., Huang, Y., Izadi, S., Kovalenko, A., … Kollman, P. A. (2018). AMBER 18. University of California.
   Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mess Ewald: An N•log (N) method for Ewald sums in large systems. Journal of Chemical Physics. 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. (1995). A smooth particle mess Ewald method. Journal of Chemical Physics. 103(19), 8577–8593. https://doi.org/10.1063/1.470117
   Web of Science ®Google Scholar
• Fecher-Trost, C., Weissgerber, P., & Wissenbach, U. (2014). TRPV6 channels. Handbook of Experimental Pharmacology, 222, 359–384.
   PubMedGoogle Scholar
• Feig, M., Karanicolas, J., Brooks, I., & L, C. (2004). MMTSB tool set: Enhanced sampling and multiscale modeling methods for applications in structural biology. Journal of Molecular Graphics & Modelling, 22(5), 377–395. https://doi.org/10.1016/j.jmgm.2003.12.005
   PubMed Web of Science ®Google Scholar
• Gohlke, H., Kiel, C., & Case, D. A. (2003). Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes. Journal of Molecular Biology, 330(4), 891–913. https://doi.org/10.1016/S0022-2836(03)00610-7
   PubMed Web of Science ®Google Scholar
• Hartigan, J. A. (1975). Clustering algorithm. John Willey & Sons, Inc.
   Google Scholar
• Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., de Groot, B. L., Grubmüller, H., & MacKerell, A. D. (2017). CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nature Methods, 14(1), 71–73.
   PubMed Web of Science ®Google Scholar
• Hughes, T. E. T., Pumroy, R. A., Yazici, A. T., Kasimova, M. A., Fluck, E. C., Huynh, K. W., Samanta, A., Molugu, S. K., Zhou, Z. H., Carnevale, V., Rohacs, T., & Moiseenkova-Bell, V. Y. (2018). Structural insights on TRPV5 gating by endogenous modulators. Nature Communications, 9(1), 4198.
   PubMedGoogle Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics and Modelling. 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   Web of Science ®Google Scholar
• Jo, S., Lim, J. B., Klauda, J. B., & Im, W. (2009). CHARMM-GUI membrane builder for mixed bilayers and its application to yeast membranes. Biophysical Journal, 97(1), 50–58.
   PubMed Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Klauda, J. B., Venable, R. M., Freites, J. A., O'Connor, J. W., Tobias, D. J., Mondragon-Ramirez, C., Vorobyov, I., MacKerell, A. D., & Pastor, R. W. (2010). Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types. The Journal of Physical Chemistry B, 114(23), 7830–7843. https://doi.org/10.1021/jp101759q
   PubMed Web of Science ®Google Scholar
• Lee, J., Cha, S. K., Sun, T. J., & Huang, C. L. (2005). PIP2 activates TRPV5 and releases its inhibition by intracellular Mg2+. The Journal of General Physiology, 126(5), 439–451.
   PubMed Web of Science ®Google Scholar
• Lee, J., Cheng, X., Swails, J. M., Yeom, M. S., Eastman, P. K., Lemkul, J. A., Wei, S., Buckner, J. J., C, J., Qi, Y., Jo, S., Pande, V. S. C., A, D., Brooks, C. L., MacKerell, A. D., Klauda, J. B., & Im, W. (2016). CHARMM-GUI input generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM simulations using the CHARMM36 additive force field. Journal of Chemical Theory and Computation, 12(1), 405–413. https://doi.org/10.1021/acs.jctc.5b00935
   PubMed Web of Science ®Google Scholar
• Lieben, L., Benn, B. S., Ajibade, D., Stockmans, I., Moermans, K., Hediger, M. A., Peng, J. B., Christakos, S., Bouillon, R., & Carmeliet, G. (2010). Trpv6 mediates intestinal calcium absorption during calcium restriction and contributes to bone homeostasis. Bone, 47(2), 301–308. https://doi.org/10.1016/j.bone.2010.04.595
   PubMed Web of Science ®Google Scholar
• McGoldrick, L. L., Singh, A. K., Saotome, K., Yelshanskaya, M. V., Twomey, E. C., Grassucci, R. A., & Sobolevsky, A. I. (2018). Opening of the human epithelial calcium channel TRPV6. Nature, 553(7687), 233–237. https://doi.org/10.1038/nature25182
   PubMed Web of Science ®Google Scholar
• Nijenhuis, T., Hoenderop, J. G., van der Kemp, A. W., & Bindels, R. J. (2003). Localization and regulation of the epithelial Ca2+ channel TRPV6 in the kidney. Journal of the American Society of Nephrology, 14(11), 2731–2740.
   PubMed Web of Science ®Google Scholar
• Peng, J. B., Chen, X. Z., Berger, U. V., Vassilev, P. M., Tsukaguchi, H., Brown, E. M., & Hediger, M. A. (1999). Molecular cloning and characterization of a channel-like transporter mediating interstinal calcium absorption. Journal of Biological Chemistry. 274(32), 22739–22746. https://doi.org/10.1074/jbc.274.32.22739
   PubMed Web of Science ®Google Scholar
• Peng, J. B., Chen, X. Z., Berger, U. V., Weremowicz, S., Morton, C. C., Vassilev, P. M., Brown, E. M., & Hediger, M. A. (2000). Human calcium transport protein CaT1. Biochemical and Biophysical Research Communications, 278(2), 326–332.
   PubMed Web of Science ®Google Scholar
• Prasad, K., Ahamad, S., Gupta, D., & Kumar, V. (2021). Targeting cathepsins: A potential link between COVID-19 and associated neurological manifestations. Heliyon, 7(10), e08089. https://doi.org/10.1016/j.heliyon.2021.e08089
   PubMed Web of Science ®Google Scholar
• Rohacs, T. (2014). Phosphoinositide regulation of TRP channels. Handbook of Experimental Pharmacology, 233, 1143–1176.
   Google Scholar
• Rohacs, T., & Nilius, B. (2007). Regulation of transient receptor potential (TRP) channels by phosphoinositides. Pflugers Archiv: European Journal of Physiology, 455(1), 157–168.
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. C. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Saotome, K., Singh, A., Yelshanskaya, M., & Sobolevsky, A. I. (2016). Crystal structure of the epithelial calcium channel TRPV6. Nature, 534(7608), 506–511. https://doi.org/10.1038/nature17975
   PubMed Web of Science ®Google Scholar
• Singh, A. K., McGoldrick, L. L., Twomey, E. C., & Sobolevsky, A. I. (2018). Mechanism of calmodulin inactivation of the calcium-selective TRP channel TRPV6. Science Advances, 4(8), eaau6088. https://doi.org/10.1126/sciadv.aau6088
   PubMed Web of Science ®Google Scholar
• Singh, A. K., Saotome, K., McGoldrick, L. L., & Sobolevsky, A. I. (2018). Structural bases of TRP channel TRPV6 allosteric modulation by 2-APB. Nature Communications, 9(1), 2465.
   PubMedGoogle Scholar
• Singh, A., Saotome, K., & Sobolevsky, A. I. (2017). Swapping of transmembrane domains in the epithelial calcium channel TRPV6. Scientific Reports, 7(1), 10669.
   PubMedGoogle Scholar
• Stewart, J. M. (2020). TRPV6 as a target for cancer therapy. Journal of Cancer, 11(2), 374–387. https://doi.org/10.7150/jca.31640
   PubMed Web of Science ®Google Scholar
• Suzuki, Y., Chitayat, D., Sawada, H., Deardorff, M. A., McLaughlin, H. M., Begtrup, A., Millar, K., Harrington, J., Chong, K., Roifman, M., Grand, K., Tominaga, M., Takada, F., Shuster, S., Obara, M., Mutoh, H., Kushima, R., & Nishimura, G. (2018). TRPV6 variants interfere with maternal-fetal calcium transport through the placenta and cause transient neonatal hyperparathyroidism. American Journal of Human Genetics, 102(6), 1104–1114.
   PubMed Web of Science ®Google Scholar
• Thyagarajan, B., Lukacs, V., & Rohacs, T. (2008). Hydrolysis of phosphatidylinositol 4,5-bisphosphate mediates calcium-induced inactivation of TRPV6 channels. The Journal of Biological Chemistry, 283(22), 14980–14987.
   PubMed Web of Science ®Google Scholar
• Vennekens, R., Hoenderop, J. G., Prenen, J., Stuiver, M., Willems, P. H., Droogmans, G., Nilius, B., & Bindels, R. J. (2000). Permeation and gating properties of the novel epithelial Ca2+ channel. Journal of Biological Chemistry, 275(6), 3963–3969. https://doi.org/10.1074/jbc.275.6.3963
   PubMed Web of Science ®Google Scholar
• Wang, L., Holmes, R. P., & Peng, J. B. (2017). The L530R variation associated with recurrent kidney stones impairs the structure and function of TRPV5. Biochemical and Biophysical Research Communications, 492(3), 362–367. https://doi.org/10.1016/j.bbrc.2017.08.102
   PubMed Web of Science ®Google Scholar
• Wang, L., Holmes, R. P., & Peng, J.-B. (2016). Molecular modeling of the structural and dynamical changes in calcium channel TRPV5 induced by the African-specific A563T variation. Biochemistry, 55(8), 1254–1264. https://doi.org/10.1021/acs.biochem.5b00732
   PubMed Web of Science ®Google Scholar
• Wu, G. J., Zhang, W., Na, T., Jiang, H., Wu, H., & Peng, J. B. (2012). Suppression of intestinal calcium entry channel TRPV6 by OCRL, a lipid phosphatase associated with Lowe syndrome and Dent disease. American Journal of Physiology Cell Physiology, 302, 1479–1491.
   Web of Science ®Google Scholar
• Zakharian, E., Cao, C., & Rohacs, T. (2011). Intracellular ATP supports TRPV6 activity via lipid kinases and the generation of PtdIns(4,5)P2. FASEB Journal, 25(11), 3915–3928. https://doi.org/10.1096/fj.11-184630
   PubMed Web of Science ®Google Scholar
• Zhuang, L., Peng, J. B., Tou, L., Takanaga, H., Adam, R. M., Hediger, M. A., & Freeman, M. R. (2002). Calcium-selective ion channel, CaT1, is apically localized in gastrointestinal tract epithelia and is aberrantly expressed in human malignancies. Laboratory Investigation, 82(12), 1755–1764.
   PubMed Web of Science ®Google Scholar