Loop diuretic and ion-binding residues revealed by scanning mutagenesis of transmembrane helix 3 (TM3) of Na-K-Cl cotransporter (NKCC1)

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17308-17317

  Somasekharan, Suma ^a   Tanis, Jessica ^a,b   Forbush, Biff ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL SALTS; EXTRACELLULAR; FUROSEMIDES; HOMOLOGY MODELS; ION TRANSLOCATION; ION-BINDING; METHANETHIOSULFONATE; ORGANOCATIONS; POLYAMINES; STRUCTURAL HOMOLOGY; SUBSTITUTION EFFECT; TRANSLOCATION PATHWAY; TRANSMEMBRANE HELICES;

AMINO ACIDS; BIOPHYSICS; CHLORINE COMPOUNDS; ENZYME ACTIVITY; MUTAGENESIS;

IONS;

ALANINE; ASPARAGINE; BUMETANIDE; CYSTEINE; FUROSEMIDE; GLYCINE; ISOLEUCINE; LOOP DIURETIC AGENT; METHIONINE; PHENYLALANINE; POLYAMINE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; THIOMESYLIC ACID METHYL ESTER; TRYPTOPHAN; TYROSINE;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; MEMBRANE TRANSPORT; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY;

BINDING SITES; BUMETANIDE; DIURETICS; HEK293 CELLS; HUMANS; ION TRANSPORT; MESYLATES; MUTAGENESIS; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SULFHYDRYL REAGENTS;

EID: 84861210254     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.356014     Document Type: Article

References (39)

1. Delpire, E., and Mount, D. B. (2002) Human and murine phenotypes associated with defects in cation-chloride cotransport. Annu. Rev. Physiol. 64, 803-843 (Pubitemid 34259250)
2. - cotransporter, in epilepsy- associated malformations of cortical development. Neuroscience 145, 185-196
3. Darman, R. B., and Forbush, B. (2002) A regulatory locus of phosphorylation in the N terminus of the Na-K-Cl cotransporter, NKCC1. J. Biol. Chem. 277, 37542-37550
4. Rinehart, J., Maksimova, Y. D., Tanis, J. E., Stone, K. L., Hodson, C. A., Zhang, J., Risinger, M., Pan, W., Wu, D., Colangelo, C. M., Forbush, B., Joiner, C. H., Gulcicek, E. E., Gallagher, P. G., and Lifton, R. P. (2009) Sites of regulated phosphorylation that control K-Cl cotransporter activity. Cell 138, 525-536
5. - cotransporter (NKCC1) is a homodimer. Biochemistry 39, 3718-3724
6. Pedersen, M., Carmosino, M., and Forbush, B. (2008) Intramolecular and intermolecular fluorescence resonance energy transfer in fluorescent protein-tagged Na-K-Cl cotransporter (NKCC1): sensitivity to regulatory conformational change and cell volume. J. Biol. Chem. 283, 2663-2674
7. - cotransporter described for the first time. J. Biol. Chem. 279, 40769-40777
8. Blaesse, P., Guillemin, I., Schindler, J., Schweizer, M., Delpire, E., Khiroug, L., Friauf, E., and Nothwang, H. G. (2006) Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J. Neurosci. 26, 10407-10419 (Pubitemid 44564591)
9. Monette, M. Y., and Forbush, B. (2012) Regulatory activation is accompanied by movement in the C terminus of the Na-K-Cl cotransporter (NKCC1). J. Biol. Chem. 287, 2210-2220
10. Isenring, P., Jacoby, S. C., Chang, J., and Forbush, B. (1998) Mutagenic mapping of the Na-K-Cl cotransporter for domains involved in ion transport and bumetanide binding. J. Gen. Physiol. 112, 549-558 (Pubitemid 28518954)
11. Giménez, I., Isenring, P., and Forbush, B. (2002) Spatially distributed alternative splice variants of the renal Na-K-Cl cotransporter exhibit dramatically different affinities for the transported ions. J. Biol. Chem. 277, 8767-8770 (Pubitemid 34952940)
12. - cotransporter (NKCC1). J. Biol. Chem. 278, 11811-11817
13. Castañeda-Bueno, M., Vázquez, N., Bustos-Jaimes, I., Hernández, D., Rodríguez-Lobato, E., Pacheco-Alvarez, D., Cariño-Cortés, R., Moreno, E., Bobadilla, N. A., and Gamba, G. (2010)Asingle residue in transmembrane domain 11 defines the different affinity for thiazides between the mammalian and flounder NaCl transporters. Am. J. Physiol. Renal Physiol. 299, F1111-1119
14. +-independent amino acid transporter. Science 325, 1010-1014
15. Fang, Y., Jayaram, H., Shane, T., Kolmakova-Partensky, L., Wu, F., Williams, C., Xiong, Y., and Miller, C. (2009) Structure of a prokaryotic virtual proton pump at 3.2 Å resolution. Nature 460, 1040-1043
16. Gao, X., Zhou, L., Jiao, X., Lu, F., Yan, C., Zeng, X., Wang, J., and Shi, Y. (2010) Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 463, 828-832
17. Kowalczyk, L., Ratera, M., Paladino, A., Bartoccioni, P., Errasti-Murugarren, E., Valencia, E., Portella, G., Bial, S., Zorzano, A., Fita, I., Orozco, M., Carpena, X., Vázquez-Ibar, J. L., and Palacín, M. (2011) Molecular basis of substrate-induced permeation by an amino acid antiporter. Proc. Natl. Acad. Sci. U.S.A. 108, 3935-3940
18. --dependent neurotransmitter transporters. Nature 437, 215-223
19. Khafizov, K., Staritzbichler, R., Stamm, M., and Forrest, L. R. (2010) A study of the evolution of inverted-topology repeats from LeuT-fold transporters using AlignMe. Biochemistry 49, 10702-10713
20. Carmosino, M., Giménez, I., Caplan, M., and Forbush, B. (2008) Exon loss accounts for differential sorting of Na-K-Cl cotransporters in polarized epithelial cells. Mol. Biol. Cell 19, 4341-4351
21. Lytle, C., Xu, J. C., Biemesderfer, D., and Forbush, B., 3rd (1995) Distribution and diversity of Na-K-Cl cotransport proteins: a study with monoclonal antibodies. Am. J. Physiol. 269, C1496-1505
22. Monette, M. Y., Rinehart, J., Lifton, R. P., and Forbush, B. (2011) Rare mutations in the human Na-K-Cl cotransporter (NKCC2) associated with lower blood pressure exhibit impaired processing and transport function. Am. J. Physiol. Renal Physiol. 300, F840-847
23. Jacobs, M. T., Zhang, Y. W., Campbell, S. D., and Rudnick, G. (2007) Ibogaine, a noncompetitive inhibitor of serotonin transport, acts by stabilizing the cytoplasm-facing state of the transporter. J. Biol. Chem. 282, 29441-29447 (Pubitemid 350043359)
24. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
25. Melo, F., and Sali, A. (2007) Fold assessment for comparative protein structure modeling. Protein Sci. 16, 2412-2426 (Pubitemid 350036748)
26. Silberberg, S. D., Chang, T. H., and Swartz, K. J. (2005) Secondary structure and gating rearrangements of transmembrane segments in rat P2X4 receptor channels. J. Gen. Physiol. 125, 347-359
27. Giménez, I., and Forbush, B. (2007) The residues determining differences in ion affinities among the alternative splice variants F, A, and B of the mammalian renal Na-K-Cl cotransporter (NKCC2). J. Biol. Chem. 282, 6540-6547 (Pubitemid 47100870)
28. Lytle, C., McManus, T. J., and Haas, M. (1998) A model of Na-K-2Cl cotransport based on ordered ion binding and glide symmetry. Am. J. Physiol. 274, C299-309
29. Forbush, B., 3rd, and Palfrey, H. C. (1983) [3H]Bumetanide binding to membranes isolated from dog kidney outer medulla: relationship to the Na,K,Cl co-transport system. J. Biol. Chem. 258, 11787-11792
30. - co-transporter: evidence for an intracellular anion modifier site. Biochem. J. 309, 637-642
31. Forrest, L. R., and Rudnick, G. (2009) The rocking bundle: a mechanism for ion-coupled solute flux by symmetrical transporters. Physiology 24, 377-386
32. Shimamura, T., Weyand, S., Beckstein, O., Rutherford, N. G., Hadden, J. M., Sharples, D., Sansom, M. S., Iwata, S., Henderson, P. J., and Cameron, A. D. (2010) Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1. Science 328, 470-473
33. +/ sugar symport. Science 321, 810-814
34. Krishnamurthy, H., and Gouaux, E. (2012) X-ray structures of LeuT in substrate-free outward-open and apo inward-open states. Nature 481, 469-474
35. 3H]Bumetanide binding to duck red cells: correlation with inhibition of (Na + K + 2Cl) co-transport. J. Biol. Chem. 261, 8434-8441
36. Singh, S. K., Piscitelli, C. L., Yamashita, A., and Gouaux, E. (2008) A competitive inhibitor traps LeuT in an open-to-out conformation. Science 322, 1655-1661
37. Talvenheimo, J., Nelson, P. J., and Rudnick, G. (1979) Mechanism of imipramine inhibition of platelet 5-hydroxytryptamine transport. J. Biol. Chem. 254, 4631-4635 (Pubitemid 9203493)
38. +/glucose cotransporter (SGLT1) turnover rate using the ion-trap technique. Biophys. J. 100, 52-59
39. Cherubino, F., Bossi, E., Miszner, A., Ghezzi, C., and Peres, A. (2010) Transient currents in the glycine cotransporter GlyT1 reveal different steps in transport mechanism. J. Mol. Neurosci. 41, 243-251