Portulano, C., Paroder-Belenitsky, M. & Carrasco, N. The Na+/I− symporter (NIS): mechanism and medical impact. Endocr. Rev. 35, 106–149 (2014).
Ravera, S., Reyna-Neyra, A., Ferrandino, G., Amzel, L. M. & Carrasco, N. The sodium/iodide symporter (NIS): molecular physiology and preclinical and clinical applications. Annu. Rev. Physiol. 79, 261–289 (2017).
Dai, G., Levy, O. & Carrasco, N. Cloning and characterization of the thyroid iodide transporter. Nature 379, 458–460 (1996).
Mullur, R., Liu, Y. Y. & Brent, G. A. Thyroid hormone regulation of metabolism. Physiol. Rev. 94, 355–382 (2014).
Zhang, Z., Liu, F. & Chen, J. Molecular structure of the ATP-bound, phosphorylated human CFTR. Proc. Natl Acad. Sci. USA 115, 12757–12762 (2018).
Reyna-Neyra, A. et al. The iodide transport defect-causing Y348D mutation in the Na(+)/I(-) symporter renders the protein intrinsically inactive and impairs its targeting to the plasma membrane. Thyroid 31, 1272–1281 (2021).
Tazebay, U. H. et al. The mammary gland iodide transporter is expressed during lactation and in breast cancer. Nat. Med. 6, 871–878 (2000).
Spitzweg, C. et al. The sodium iodide symporter (NIS): novel applications for radionuclide imaging and treatment. Endocr. Relat. Cancer 28, T193–T213 (2021).
Kitzberger, C. et al. The sodium iodide symporter (NIS) as theranostic gene: its emerging role in new imaging modalities and non-viral gene therapy. EJNMMI Res. 12, 25 (2022).
Urnauer, S. et al. EGFR-targeted nonviral NIS gene transfer for bioimaging and therapy of disseminated colon cancer metastases. Oncotarget 8, 92195–92208 (2017).
Miller, A. & Russell, S. J. The use of the NIS reporter gene for optimizing oncolytic virotherapy. Expert Opin. Biol. Ther. 16, 15–32 (2016).
Li, W., Nicola, J. P., Amzel, L. M. & Carrasco, N. Asn441 plays a key role in folding and function of the Na+/I− symporter (NIS). FASEB J. 27, 3229–3238 (2013).
Nicola, J. P. et al. Sodium/iodide symporter mutant V270E causes stunted growth but no cognitive deficiency. J. Clin. Endocrinol. Metab. 100, E1353–E1361 (2015).
Paroder-Belenitsky, M. et al. Mechanism of anion selectivity and stoichiometry of the Na+/I- symporter (NIS). Proc. Natl Acad. Sci. USA 108, 17933–17938 (2011).
Levy, O. et al. N-linked glycosylation of the thyroid Na+/I− symporter (NIS). Implications for its secondary structure model. J. Biol. Chem. 273, 22657–22663 (1998).
Levy, O. et al. Characterization of the thyroid Na+/I− symporter with an anti-COOH terminus antibody. Proc. Natl Acad. Sci. USA 94, 5568–5573 (1997).
Paroder, V., Nicola, J. P., Ginter, C. S. & Carrasco, N. The iodide transport defect-causing mutation R124H: a δ-amino group at position 124 is critical for maturation and trafficking of the Na+/I- symporter (NIS). J. Cell Sci. 126, 3305–3313 (2013).
De la Vieja, A., Reed, M. D., Ginter, C. S. & Carrasco, N. Amino acid residues in transmembrane segment IX of the Na+/I− symporter play a role in its Na+ dependence and are critical for transport activity. J. Biol. Chem. 282, 25290–25298 (2007).
Chew, T. A. et al. Structure and mechanism of the cation-chloride cotransporter NKCC1. Nature 572, 488–492 (2019).
Coleman, J. A., Green, E. M. & Gouaux, E. X-ray structures and mechanism of the human serotonin transporter. Nature 532, 334–339 (2016).
Han, L. et al. Structure and mechanism of the SGLT family of glucose transporters. Nature 601, 274–279(2022).
Niu, Y. et al. Structural basis of inhibition of the human SGLT2-MAP17 glucose transporter. Nature 601, 280–284 (2021).
Yamashita, A., Singh, S. K., Kawate, T., Jin, Y. & Gouaux, E. Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437, 215–223 (2005).
Faham, S. et al. The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321, 810–814 (2008).
Wang, J., Liu, Z., Frank, J. & Moore, P. B. Identification of ions in experimental electrostatic potential maps. IUCrJ 5, 375–381 (2018).
Zhekova, H. R. et al. Mapping of ion and substrate binding sites in human sodium iodide symporter (hNIS). J. Chem. Inf. Model. 60, 1652–1665 (2020).
Nicola, J. P., Carrasco, N. & Amzel, L. M. Physiological sodium concentrations enhance the iodide affinity of the Na+/I− symporter. Nat. Commun. 5, 3948 (2014).
Ravera, S., Quick, M., Nicola, J. P., Carrasco, N. & Amzel, L. M. Beyond non-integer Hill coefficients: a novel approach to analyzing binding data, applied to Na+-driven transporters. J. Gen. Physiol. 145, 555–563 (2015).
Dohan, O. et al. The Na+/I symporter (NIS) mediates electroneutral active transport of the environmental pollutant perchlorate. Proc. Natl Acad. Sci. USA 104, 20250–20255 (2007).
Tran, N. et al. Thyroid-stimulating hormone increases active transport of perchlorate into thyroid cells. Am. J. Physiol. Endocrinol. Metab. 294, E802–E806 (2008).
Zuckier, L. S. et al. Kinetics of perrhenate uptake and comparative biodistribution of perrhenate, pertechnetate, and iodide by NaI symporter-expressing tissues in vivo. J. Nucl. Med. 45, 500–507 (2004).
Eskandari, S. et al. Thyroid Na+/I- symporter. Mechanism, stoichiometry, and specificity. J. Biol. Chem. 272, 27230–27238 (1997).
Llorente-Esteban, A. et al. Allosteric regulation of mammalian Na+/I− symporter activity by perchlorate. Nat. Struct. Mol. Biol. 27, 533–539 (2020).
Boutagy, N. E. et al. Noninvasive in vivo quantification of adeno-associated virus serotype 9-mediated expression of the sodium/iodide symporter under hindlimb ischemia and neuraminidase desialylation in skeletal muscle using single-photon emission computed tomography/computed tomography. Circ. Cardiovasc. Imaging 12, e009063 (2019).
Pavelka, A. et al. CAVER: algorithms for analyzing dynamics of tunnels in macromolecules. IEEE/ACM Trans. Comput. Biol. Bioinform. 13, 505–517 (2016).
Ferrandino, G. et al. Na+ coordination at the Na2 site of the Na+/I− symporter. Proc. Natl Acad. Sci. USA 113, E5379–E5388 (2016).
Sun, L. et al. Molecular dynamics simulations of the surface tension and structure of salt solutions and clusters. J. Phys. Chem. 116, 3198–3204 (2012).
Carugo, O. Buried chloride stereochemistry in the Protein Data Bank. BMC Struct. Biol. 14, 19 (2014).
Kang, B., Tang, H., Zhao, Z. & Song, S. Hofmeister series: insights of ion specificity from amphiphilic assembly and interface property. ACS Omega 5, 6229–6239 (2020).
Marcus, Y. A simple empirical model describing the thermodynamics of hydration of ions of widely varying charges, sizes, and shapes. Biophys. Chem. 51, 111–127 (1994).
Yang, D. & Gouaux, E. Illumination of serotonin transporter mechanism and role of the allosteric site. Sci. Adv. 7, eabl3857 (2021).
Coleman, J. A. & Gouaux, E. Structural basis for recognition of diverse antidepressants by the human serotonin transporter. Nat. Struct. Mol. Biol. 25, 170–175 (2018).
Levy, O., Ginter, C. S., De la Vieja, A., Levy, D. & Carrasco, N. Identification of a structural requirement for thyroid Na+/I- symporter (NIS) function from analysis of a mutation that causes human congenital hypothyroidism. FEBS Lett. 429, 36–40 (1998).
Ferrandino, G. et al. Na+ coordination at the Na2 site of the Na+/I- symporter. Proc. Natl Acad. Sci. USA 113, E5379–E5388 (2016).
Ravera, S., Quick, M., Nicola, J. P., Carrasco, N. & Amzel, L. M. Beyond non-integer Hill coefficients: a novel approach to analyzing binding data, applied to Na+-driven transporters. J. Gen. Physiol. 145, 555–563 (2015).
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
Punjani, A., Zhang, H. & Fleet, D. J. Non-uniform refinement: adaptive regularization improves single-particle cryo-EM reconstruction. Nat. Methods 17, 1214–1221 (2020).
Moriya, T. et al. Size matters: optimal mask diameter and box size for single-particle cryogenic electron microscopy. Preprint at bioRxiv https://doi.org/10.1101/2020.08.23.263707 (2020).
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
Górski, K. M. et al. HEALPix: a framework for high-resolution discretization and fast analysis of data distributed on the sphere. Astrophys. J. 622, 759–771 (2005).
Wang, J., Liu, Z., Frank, J. & Moore, P. B. Identification of ions in experimental electrostatic potential maps. IUCrJ 5, 375–381 (2018).
Lee, J. et al. CHARMM-GUI input generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM simulations using the CHARMM36 additive force field. J. Chem. Theory Comput. 12, 405–413 (2016).
Abraham, M. J. et al. GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1, 19–25 (2015).
Huang, J. et al. CHARMM36m: an improved force field for folded and intrinsically disordered proteins. Nat. Methods 14, 71–73 (2017).
Essmann, U. et al. A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577–8593 (1995).
Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).
Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52, 7182–7190 (1981).
Hess, B., Bekker, H., Berendsen, H. J. & Fraaije, J. G. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463–1472 (1997).
Li, P., Song, L. F. & Merz, K. M. Jr. Systematic parameterization of monovalent ions employing the nonbonded model. J. Chem. Theory Comput. 11, 1645–1657 (2015).
More News
Judge dismisses superconductivity physicist’s lawsuit against university
Future of Humanity Institute shuts: what’s next for ‘deep future’ research?
Star Formation Shut Down by Multiphase Gas Outflow in a Galaxy at a Redshift of 2.45 – Nature