Arginine transportation mechanism through cationic amino acid transporter 1: insights from molecular dynamics studies

References

• Adelman, J. L., Sheng, Y., Choe, S., Abramson, J., Wright, E. M., Rosenberg, J. M., & Grabe, M. (2014). Structural determinants of water permeation through the sodium-galactose transporter vSGLT. Biophysical journal, 106(6), 1280–1289. https://doi.org/10.1016/j.bpj.2014.01.006
   PubMed Web of Science ®Google Scholar
• Ardevol, A., & Hummer, G. (2018). Retinal isomerization and water-pore formation in channelrhodopsin-2. Proceedings of the National Academy of Sciences of the United States of America, 115(14), 3557–3562. https://doi.org/10.1073/pnas.170009111
   PubMed Web of Science ®Google Scholar
• Beckstein, O., Biggin, P. C., & Sansom, M. S. (2001). A hydrophobic gating mechanism for nanopores. The Journal of Physical Chemistry B, 105(51), 12902–12905. https://doi.org/10.1021/jp012233y
   Web of Science ®Google Scholar
• Callea, L., Bonati, L., & Motta, S. (2021). Metadynamics-Based Approaches for Modeling the Hypoxia-Inducible Factor 2α Ligand Binding Process. Journal of Chemical Theory and Computation, 17(7), 3841–3851. https://doi.org/10.1021/acs.jctc.1c00114
   PubMed Web of Science ®Google Scholar
• Chen, H., & Kihara, D. (2008). Estimating quality of template‐based protein models by alignment stability. Proteins, 71(3), 1255–1274. https://doi.org/10.1002/prot.21819
   PubMed Web of Science ®Google Scholar
• Closs, E. I., & Gräf, P. (1999). Cationic amino acid transporters (CATs). Targets for the manipulation of NO synthase activity?. In a G. L. Amidon & W. Sadee (Eds.), Membrane Transporters as Drug Targets. (pp. 229–249). Pharmaceutical biotechnology. https://doi.org/10.1007/0-306-46812-3_8
   Google Scholar
• Closs, E. I., Simon, A., Vékony, N., & Rotmann, A. (2004). Plasma membrane transporters for arginine. The Journal of Nutrition, 134(10 Suppl), 2752S–2759S. https://doi.org/10.1093/jn/134.10.2752S
   PubMed Web of Science ®Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science: A Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• Comalada, M., Yeramian, A., Modolell, M., Lloberas, J., & Celada, A. (2012). Arginine and macrophage activation. In G. I. Henderson & P. M. Adams (Eds.), Leucocytes. (pp. 223–235). Humana Press. https://doi.org/10.1007/978-1-61779-527-5_16
   Google Scholar
• De Santo, C., Booth, S., Vardon, A., Cousins, A., Tubb, V., Perry, T., Noyvert, B., Beggs, A., Ng, M., Halsey, C., Kearns, P., Cheng, P., & Mussai, F. (2018). The arginine metabolome in acute lymphoblastic leukemia can be targeted by the pegylated‐recombinant arginase I BCT‐100. International journal of Cancer, 142(7), 1490–1502. https://doi.org/10.1002/ijc.31170
   PubMed Web of Science ®Google Scholar
• Errasti-Murugarren, E., Fort, J., Bartoccioni, P., Díaz, L., Pardon, E., Carpena, X., Espino-Guarch, M., Zorzano, A., Ziegler, C., Steyaert, J., Fernández-Recio, J., Fita, I., & Palacín, M. (2019). L amino acid transporter structure and molecular bases for the asymmetry of substrate interaction. Nature Communications, 10(1), 1–12. https://doi.org/10.1038/s41467-019-09837-z
   PubMedGoogle Scholar
• Falk, K., Sedlmeier, F., Joly, L., Netz, R. R., & Bocquet, L. (2010). Molecular origin of fast water transport in carbon nanotube membranes: Superlubricity versus curvature dependent friction. Nano letters, 10(10), 4067–4073. https://doi.org/10.1021/nl1021046
   PubMed Web of Science ®Google Scholar
• Feun, L. G., Kuo, M. T., & Savaraj, N. (2015). Arginine deprivation in cancer therapy. Current opinion in Clinical Nutrition and Metabolic Care, 18(1), 78–82. https://doi.org/10.1097/MCO.0000000000000122
   PubMed Web of Science ®Google Scholar
• Fotiadis, D., Kanai, Y., & Palacín, M. (2013). The SLC3 and SLC7 families of amino acid transporters. Molecular aspects of Medicine, 34(2-3), 139–158. https://doi.org/10.1016/j.mam.2012.10.007
   PubMed Web of Science ®Google Scholar
• Gao, X., Zhou, L., Jiao, X., Lu, F., Yan, C., Zeng, X., Wang, J., & Shi, Y. (2010). Mechanism of substrate recognition and transport by an amino acid antiporter. Nature, 463(7282), 828–832. https://doi.org/10.1038/nature08741
   PubMed Web of Science ®Google Scholar
• Geiger, R., Rieckmann, J. C., Wolf, T., Basso, C., Feng, Y., Fuhrer, T., Kogadeeva, M., Picotti, P., Meissner, F., Mann, M., Zamboni, N., Sallusto, F., & Lanzavecchia, A. (2016). L-arginine modulates T cell metabolism and enhances survival and anti-tumor activity. Cell, 167(3), 829–842.e13. https://doi.org/10.1016/j.cell.2016.09.031
   PubMed Web of Science ®Google Scholar
• Hatzoglou, M., Fernandez, J., Yaman, I., & Closs, E. (2004). Regulation of cationic amino acid transport: The story of the CAT-1 transporter. Annual review of Nutrition, 24, 377–399. https://doi.org/10.1146/annurev.nutr.23.011702.073120
   PubMed Web of Science ®Google Scholar
• Horner, A., & Pohl, P. (2018). Single-file transport of water through membrane channels. Faraday discussions, 209(0), 9–33. https://doi.org/10.1039/C8FD00122G
   PubMedGoogle Scholar
• Huang, Y., Kang, B. N., Tian, J., Liu, Y., Luo, H. R., Hester, L., & Snyder, S. H. (2007). The cationic amino acid transporters CAT1 and CAT3 mediate NMDA receptor activation-dependent changes in elaboration of neuronal processes via the mammalian target of rapamycin mTOR pathway. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 27(3), 449–458. https://doi.org/10.1523/JNEUROSCI.4489-06.2007
   PubMed Web of Science ®Google Scholar
• Hummer, G. (2007). Water, proton, and ion transport: From nanotubes to proteins. Molecular Physics, 105(2-3), 201–207. https://doi.org/10.1080/00268970601140784
   Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Ilgü, H., Jeckelmann, J. M., Colas, C., Ucurum, Z., Schlessinger, A., & Fotiadis, D. (2018). Effects of mutations and ligands on the thermostability of the L-arginine/agmatine antiporter AdiC and deduced insights into ligand-binding of human L-type amino acid transporters. International Journal of Molecular Sciences, 19(3), 918. https://doi.org/10.3390/ijms19030918
   PubMed Web of Science ®Google Scholar
• Ilgü, H., Jeckelmann, J. M., Gapsys, V., Ucurum, Z., de Groot, B. L., & Fotiadis, D. (2016). Insights into the molecular basis for substrate binding and specificity of the wild-type L-arginine/agmatine antiporter AdiC. Proceedings of the National Academy of Sciences of the United States of America, 113(37), 10358–10363. https://doi.org/10.1073/pnas.1605442113
   PubMed Web of Science ®Google Scholar
• Jo, S., Kim, T., Iyer, V. G., & Im, W. (2008). CHARMM‐GUI: A web‐based graphical user interface for CHARMM. Journal of Computational Chemistry, 29(11), 1859–1865. https://doi.org/10.1002/jcc.20945
   PubMed Web of Science ®Google Scholar
• Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583–589. https://doi.org/10.1038/s41586-021-03819-2
   PubMed Web of Science ®Google Scholar
• Jungnickel, K. E., Parker, J. L., & Newstead, S. (2018). Structural basis for amino acid transport by the CAT family of SLC7 transporters. Nature Communications, 9(1), 1–12. https://doi.org/10.1038/s41467-018-03066-6
   PubMedGoogle Scholar
• Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., & Cheatham, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. https://doi.org/10.1021/ar000033j
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A, Open-Source Drug Discovery Consortium., & Lynn, A. (2014). g_mmpbsa A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R., & Thornton, J. M. (1996). AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. Journal of Biomolecular NMR, 8(4), 477–486. https://doi.org/10.1007/BF00228148
   PubMed Web of Science ®Google Scholar
• Li, J., Shaikh, S. A., Enkavi, G., Wen, P. C., Huang, Z., & Tajkhorshid, E. (2013). Transient formation of water-conducting states in membrane transporters. Proceedings of the National Academy of Sciences, 110(19), 7696–7701. https://doi.org/10.1073/pnas.121898611
   PubMed Web of Science ®Google Scholar
• Liu, B., Wu, R., Law, A. W. K., Feng, X. Q., Bai, L., & Zhou, K. (2016). Channel morphology effect on water transport through graphene bilayers. Scientific Report, 6(1), 1–14. https://doi.org/10.1038/srep38583
   PubMed Web of Science ®Google Scholar
• Lu, Y., Wang, W., Wang, J., Yang, C., Mao, H., Fu, X., Wu, Y., Cai, J., Han, J., Xu, Z., Zhuang, Z., Liu, Z., Hu, H., & Chen, B. (2013). Overexpression of arginine transporter CAT-1 is associated with accumulation of L-arginine and cell growth in human colorectal cancer tissue. PloS one, 8(9), e73866. https://doi.org/10.1371/journal.pone.0073866
   PubMed Web of Science ®Google Scholar
• MacAulay, N., Gether, U., Klaeke, D. A., & Zeuthen, T. (2002). Passive water and urea permeability of a human Na+–glutamate cotransporter expressed in Xenopus oocytes. The Journal of Physiology, 542(Pt 3), 817–828. https://doi.org/10.1113/jphysiol.2002.020586
   PubMed Web of Science ®Google Scholar
• Matthews, D. R., & Wallace, T. M. (2005). Sulphonylureas and the rise and fall of beta-cell function. The British Journal of Diabetes & Vascular Disease, 5(4), 192–196. https://doi.org/10.1177/14746514050050040301
   Google Scholar
• Morris, S. M. Jr, (2006). Arginine: Beyond protein. The American Journal of Clinical Nutrition, 83(2), 508S–512S. https://doi.org/10.1093/ajcn/83.2.508S
   PubMed Web of Science ®Google Scholar
• Morris, S. M. Jr, (2016). Arginine metabolism revisited. The Journal of Nutrition, 146(12), 2579S–2586S. https://doi.org/10.3945/jn.115.226621
   PubMed Web of Science ®Google Scholar
• Patil, M. D., Bhaumik, J., Babykutty, S., Banerjee, U. C., & Fukumura, D. (2016). Arginine dependence of tumor cells: Targeting a chink in cancer’s armor. Oncogene, 35(38), 4957–4972. https://doi.org/10.1038/onc.2016.37
   PubMed Web of Science ®Google Scholar
• Petřek, M., Otyepka, M., Banáš, P., Košinová, P., Koča, J., & Damborský, J. (2006). CAVER: A new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics, 7(1), 1–9. https://doi.org/10.1186/1471-2105-7-316
   PubMedGoogle 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. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Phillips, M. M., Sheaff, M. T., & Szlosarek, P. W. (2013). Targeting arginine-dependent cancers with arginine-degrading enzymes: Opportunities and challenges. Cancer research and Treatment, 45(4), 251–262. https://doi.org/10.4143/crt.2013.45.4.251
   PubMed Web of Science ®Google Scholar
• Rajendran, E., Hapuarachchi, S. V., Miller, C. M., Fairweather, S. J., Cai, Y., Smith, N. C., Cockburn, I. A., Bröer, S., Kirk, K., & Van Dooren, G. G. (2017). Cationic amino acid transporters play key roles in the survival and transmission of apicomplexan parasites. Nature Communications, 8(1), 1–13. https://doi.org/10.1038/ncomms14455
   PubMedGoogle Scholar
• Rhoads, J. M., Niu, X., Odle, J., & Graves, L. M. (2006). Role of mTOR signaling in intestinal cell migration. American journal of Physiology. Gastrointestinal and Liver Physiology, 291(3), G510–G517. https://doi.org/10.1152/ajpgi.00189.2005
   PubMed Web of Science ®Google Scholar
• Riess, C., Shokraie, F., Classen, C. F., Kreikemeyer, B., Fiedler, T., Junghanss, C., & Maletzki, C. (2018). Arginine-depleting enzymes–An increasingly recognized treatment strategy for therapy-refractory malignancies. Cellular physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 51(2), 854–870. https://doi.org/10.1159/000495382
   PubMedGoogle Scholar
• Saito, M., Arimura, N., Hayamizu, K., & Okada, T. (2004). Mechanisms of ion and water transport in perfluorosulfonated ionomer membranes for fuel cells. The Journal of Physical Chemistry B, 108(41), 16064–16070. https://doi.org/10.1021/jp0482565
   Web of Science ®Google Scholar
• Scalise, M., Galluccio, M., Console, L., Pochini, L., & Indiveri, C. (2018). The human SLC7A5 (LAT1): The intriguing histidine/large neutral amino acid transporter and its relevance to human health. Frontiers in Chemistry, 6, 243. https://doi.org/10.3389/fchem.2018.00243
   PubMed Web of Science ®Google Scholar
• Schiebel, J., Gaspari, R., Wulsdorf, T., Ngo, K., Sohn, C., Schrader, T. E., Cavalli, A., Ostermann, A., Heine, A., & Klebe, G. (2018). Intriguing role of water in protein-ligand binding studied by neutron crystallography on trypsin complexes. Nature Communications, 9(1), 1–15. https://doi.org/10.1038/s41467-018-05769-2
   PubMedGoogle Scholar
• Schnorr, O., Suschek, C. V., & Kolb-Bachofen, V. (2003). The importance of cationic amino acid transporter expression in human skin. The Journal of Investigative Dermatology, 120(6), 1016–1022. https://doi.org/10.1046/j.1523-1747.2003.12139.x
   PubMed Web of Science ®Google Scholar
• Singh, S. P., & Konwar, B. K. (2012). Molecular docking studies of quercetin and its analogues against human inducible nitric oxide synthase. SpringerPlus, 1(1), 1–10. https://doi.org/10.1186/2193-1801-1-69
   PubMedGoogle Scholar
• Stourac, J., Vavra, O., Kokkonen, P., Filipovic, J., Pinto, G., Brezovsky, J., Damborsky, J., & Bednar, D. (2019). Caver Web 1.0: Identification of tunnels and channels in proteins and analysis of ligand transport. Nucleic acids Research, 47(W1), W414–W422. https://doi.org/10.1093/nar/gkz378
   PubMed Web of Science ®Google Scholar
• Studer, G., Biasini, M., & Schwede, T. (2014). Assessing the local structural quality of Transmembrane protein models using statistical potentials (QMEANBrane). Bioinformatics (Oxford, England), 30(17), i505–i511. https://doi.org/10.1093/bioinformatics/btu457
   PubMed Web of Science ®Google Scholar
• Too, C. K., & Abdelmagid, S. A. (2017). L-arginine uptake and its role in the survival of breast cancer cells. In V. B. Patel, V. R. Preedy, & R. Rajendram (Eds.), L-arginine in clinical nutrition (pp. 253–268). Humana Press. https://doi.org/10.1007/978-3-319-26009-9_20
   Google Scholar
• Trick, J. L., Chelvaniththilan, S., Klesse, G., Aryal, P., Wallace, E. J., Tucker, S. J., & Sansom, M. S. (2016). Functional annotation of ion channel structures by molecular simulation. Structure (London, England: 1993), 24(12), 2207–2216. https://doi.org/10.1016/j.str.2016.10.005
   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(2), 455–461. https://doi.org/10.1002/jcc.21334
   PubMed Web of Science ®Google Scholar
• Tunyasuvunakool, K., Adler, J., Wu, Z., Green, T., Zielinski, M., Žídek, A., Bridgland, A., Cowie, A., Meyer, C., Laydon, A., Velankar, S., Kleywegt, G. J., Bateman, A., Evans, R., Pritzel, A., Figurnov, M., Ronneberger, O., Bates, R., Kohl, S. A. A., … Hassabis, D. (2021). Highly accurate protein structure prediction for the human proteome. Nature, 596(7873), 590–596. https://doi.org/10.1038/s41586-021-03828-1
   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(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Vargiu, A. V., Ramaswamy, V. K., Malvacio, I., Malloci, G., Kleinekathöfer, U., & Ruggerone, P. (2018). Water-mediated interactions enable smooth substrate transport in a bacterial efflux pump. Biochimica et Biophysica Acta. General Subjects, 1862(4), 836–845. https://doi.org/10.1016/j.bbagen.2018.01.010
   PubMed Web of Science ®Google Scholar
• Vavra, O., Filipovic, J., Plhak, J., Bednar, D., Marques, S. M., Brezovsky, J., Stourac, J., Matyska, L., & Damborsky, J. (2019). CaverDock: A molecular docking-based tool to analyse ligand transport through protein tunnels and channels. Bioinformatics (Oxford, England), 35(23), 4986–4993. https://doi.org/10.1093/bioinformatics/btz386
   PubMed Web of Science ®Google Scholar
• Verrey, F., Closs, E. I., Wagner, C. A., Palacin, M., Endou, H., & Kanai, Y. (2004). CATs and HATs: The SLC7 family of amino acid transporters. Pflugers Archiv: European Journal of Physiology, 447(5), 532–542. https://doi.org/10.1007/s00424-003-1086-z
   PubMed Web of Science ®Google Scholar
• Vina-Vilaseca, A., Bender-Sigel, J., Sorkina, T., Closs, E. I., & Sorkin, A. (2011). Protein kinase C-dependent ubiquitination and clathrin-mediated endocytosis of the cationic amino acid transporter CAT-1. The Journal of Biological Chemistry, 286(10), 8697–8706. https://doi.org/10.1074/jbc.M110.186858
   PubMed Web of Science ®Google Scholar
• Wanasen, N., & Soong, L. (2008). L-arginine metabolism and its impact on host immunity against Leishmania infection. Immunologic research, 41(1), 15–25. https://doi.org/10.1007/s12026-007-8012-y
   PubMed Web of Science ®Google Scholar
• Werner, A., Amann, E., Schnitzius, V., Habermeier, A., Luckner‐Minden, C., Leuchtner, N., Rupp, J., Closs, E. I., & Munder, M. (2016). Induced arginine transport via cationic amino acid transporter‐1 is necessary for human T‐cell proliferation. European journal of Immunology, 46(1), 92–103. https://doi.org/10.1002/eji.201546047
   PubMed Web of Science ®Google Scholar
• Werner, A., Pieh, D., Echchannaoui, H., Rupp, J., Rajalingam, K., Theobald, M., Closs, E. I., & Munder, M. (2019). Cationic amino acid transporter-1-mediated arginine uptake is essential for chronic lymphocytic leukemia cell proliferation and viability. Frontiers in Oncology, 9, 1268. https://doi.org/10.3389/fonc.2019.01268
   PubMed Web of Science ®Google Scholar
• Wu, Z., Alibay, I., Newstead, S., & Biggin, P. C. (2019). Proton control of transitions in an amino acid transporter. Biophysical journal, 117(7), 1342–1351. https://doi.org/10.1016/j.bpj.2019.07.056
   PubMed Web of Science ®Google Scholar
• Yang, L. J., Zou, J., Xie, H. Z., Li, L. L., Wei, Y. Q., & Yang, S. Y. (2009). Steered molecular dynamics simulations reveal the likelier dissociation pathway of imatinib from its targeting kinases c-Kit and Abl. PloS one, 4(12), e8470. https://doi.org/10.1371/journal.pone.0008470
   PubMed Web of Science ®Google Scholar
• Zakoji, N., Akanuma, S. I., Tachikawa, M., & Hosoya, K. I. (2015). Involvement of cationic amino acid transporter 1 in L-arginine transport in rat retinal pericytes. Biological & Pharmaceutical Bulletin, 38(2), 257–262. https://doi.org/10.1248/bpb.b14-00637
   PubMed Web of Science ®Google Scholar
• Zeuthen, T., Gorraitz, E., Her, K., Wright, E. M., & Loo, D. D. (2016). Structural and functional significance of water permeation through cotransporters. Proceedings of the National Academy of Sciences of the United States of America, 113(44), E6887–E6894. https://doi.org/10.1073/pnas.1613744113
   PubMed Web of Science ®Google Scholar
• Zhang, W., Yang, T., Zhou, S., Cheng, J., Yuan, S., Lo, G. V., & Dou, Y. (2019). Molecular Dynamics Simulation of Transmembrane Transport of Chloride Ions in Mutants of Channelrhodopsin. Biomolecules, 9(12), 852. https://doi.org/10.3390/biom9120852
   PubMed Web of Science ®Google Scholar
• Zuo, G., Shen, R., Ma, S., & Guo, W. (2010). Transport properties of single-file water molecules inside a carbon nanotube biomimicking water channel. ACS nano, 4(1), 205–210. https://doi.org/10.1021/nn901334w
   PubMed Web of Science ®Google Scholar