Structural insights into aquaporin selectivity and regulation

Current Opinion in Structural Biology

Volumn 33, Issue , 2015, Pages 126-134

  Kreida, Stefan ^a   Törnroth Horsefield, Susanna ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; AQY1 PROTEIN, S CEREVISIAE; CALCIUM; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; HUMAN; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; REGULATORY MECHANISM; REVIEW; STRUCTURE ANALYSIS; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN DOMAIN; PROTEIN TRANSPORT; YEAST;

AQUAPORINS; CALCIUM; ION CHANNEL GATING; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS; YEASTS;

EID: 84941131711     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.08.004     Document Type: Review

References (57)

1. King L.S., Kozono D., Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 2004, 5:687-698.
2. 2 in living organisms. Biochim Biophys Acta 2014, 1840:1592-1595.
3. Geyer R.R., Musa-Aziz R., Qin X., Boron W.F. Relative CO(2)/NH(3) selectivities of mammalian aquaporins 0-9. Am J Physiol Cell Physiol 2013, 304:C985-C994.
4. Soria L.R., Fanelli E., Altamura N., Svelto M., Marinelli R.A., Calamita G. Aquaporin-8-facilitated mitochondrial ammonia transport. Biochem Biophys Res Commun 2010, 393:217-221.
5. Mukhopadhyay R., Bhattacharjee H., Rosen B.P. Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta 2014, 1840:1583-1591.
6. Yasui M., Hazama A., Kwon T.H., Nielsen S., Guggino W.B., Agre P. Rapid gating and anion permeability of an intracellular aquaporin. Nature 1999, 402:184-187.
7. Yool A.J., Weinstein A.M. New roles for old holes: ion channel function in aquaporin-1. News Physiol Sci 2002, 17:68-72.
8. Huber V.J., Tsujita M., Nakada T. Aquaporins in drug discovery and pharmacotherapy. Mol Aspects Med 2012, 33:691-703.
9. Verkman A.S., Anderson M.O., Papadopoulos M.C. Aquaporins: important but elusive drug targets. Nat Rev Drug Discov 2014, 13:259-277.
10. Verkman A.S. Aquaporins in clinical medicine. Annu Rev Med 2012, 63:303-316.
11. Tornroth-Horsefield S., Hedfalk K., Fischer G., Lindkvist-Petersson K., Neutze R. Structural insights into eukaryotic aquaporin regulation. FEBS Lett 2010, 584:2580-2588.
12. Ishibashi K. Aquaporin subfamily with unusual NPA boxes. Biochim Biophys Acta 2006, 1758:989-993.
13. Guan X.G., Su W.H., Yi F., Zhang D., Hao F., Zhang H.G., Liu Y.J., Feng X.C., Ma T.H. NPA motifs play a key role in plasma membrane targeting of aquaporin-4. IUBMB Life 2010, 62:222-226.
14. Sui H., Han B.G., Lee J.K., Walian P., Jap B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature 2001, 414:872-878.
15. Kosinska Eriksson U., Fischer G., Friemann R., Enkavi G., Tajkhorshid E., Neutze R. Subangstrom resolution X-ray structure details aquaporin-water interactions. Science 2013, 340:1346-1349.
16. Pomes R., Roux B. Molecular mechanism of H+ conduction in the single-file water chain of the gramicidin channel. Biophys J 2002, 82:2304-2316.
17. Burykin A., Warshel A. What really prevents proton transport through aquaporin? Charge self-energy versus proton wire proposals. Biophys J 2003, 85:3696-3706.
18. Chakrabarti N., Tajkhorshid E., Roux B., Pomes R. Molecular basis of proton blockage in aquaporins. Structure 2004, 12:65-74.
19. de Groot B.L., Frigato T., Helms V., Grubmuller H. The mechanism of proton exclusion in the aquaporin-1 water channel. J Mol Biol 2003, 333:279-293.
20. de Groot B.L., Grubmuller H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 2001, 294:2353-2357.
21. de Groot B.L., Grubmuller H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr Opin Struct Biol 2005, 15:176-183.
22. Ilan B., Tajkhorshid E., Schulten K., Voth G.A. The mechanism of proton exclusion in aquaporin channels. Proteins 2004, 55:223-228.
23. Jensen M.O., Tajkhorshid E., Schulten K. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys J 2003, 85:2884-2899.
24. Tajkhorshid E., Nollert P., Jensen M.O., Miercke L.J., O'Connell J., Stroud R.M., Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 2002, 296:525-530.
25. Wu B., Steinbronn C., Alsterfjord M., Zeuthen T., Beitz E. Concerted action of two cation filters in the aquaporin water channel. EMBO J 2009, 28:2188-2194.
26. Wree D., Wu B., Zeuthen T., Beitz E. Requirement for asparagine in the aquaporin NPA sequence signature motifs for cation exclusion. FEBS J 2011, 278:740-748.
27. Beitz E., Wu B., Holm L.M., Schultz J.E., Zeuthen T. Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci U S A 2006, 103:269-274.
28. Li H., Chen H., Steinbronn C., Wu B., Beitz E., Zeuthen T., Voth G.A. Enhancement of proton conductance by mutations of the selectivity filter of aquaporin-1. J Mol Biol 2011, 407:607-620.
29. Morais-Cabral J.H., Zhou Y., MacKinnon R. Energetic optimization of ion conduction rate by the K+ selectivity filter. Nature 2001, 414:37-42.
30. Zhou Y., Morais-Cabral J.H., Kaufman A., MacKinnon R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0A resolution. Nature 2001, 414:43-48.
31. Johansson I., Karlsson M., Shukla V.K., Chrispeels M.J., Larsson C., Kjellbom P. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 1998, 10:451-459.
32. Alleva K., Niemietz C.M., Sutka M., Maurel C., Parisi M., Tyerman S.D., Amodeo G. Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 2006, 57:609-621.
33. Tournaire-Roux C., Sutka M., Javot H., Gout E., Gerbeau P., Luu D.T., Bligny R., Maurel C. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 2003, 425:393-397.
34. Verdoucq L., Grondin A., Maurel C. Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem J 2008, 415:409-416.
35. Gerbeau P., Amodeo G., Henzler T., Santoni V., Ripoche P., Maurel C. The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 2002, 30:71-81.
36. Frick A., Jarva M., Tornroth-Horsefield S. Structural basis for pH gating of plant aquaporins. FEBS Lett 2013, 587:989-993.
37. Frick A., Jarva M., Ekvall M., Uzdavinys P., Nyblom M., Tornroth-Horsefield S. Mercury increases water permeability of a plant aquaporin through a non-cysteine-related mechanism. Biochem J 2013, 454:491-499.
38. Ahmadpour D., Geijer C., Tamas M.J., Lindkvist-Petersson K., Hohmann S. Yeast reveals unexpected roles and regulatory features of aquaporins and aquaglyceroporins. Biochim Biophys Acta 2014, 1840:1482-1491.
39. Nemeth-Cahalan K.L., Clemens D.M., Hall J.E. Regulation of AQP0 water permeability is enhanced by cooperativity. J Gen Physiol 2013, 141:287-295.
40. Frick A., Eriksson U.K., de Mattia F., Oberg F., Hedfalk K., Neutze R., de Grip W.J., Deen P.M., Tornroth-Horsefield S. X-ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking. Proc Natl Acad Sci U S A 2014, 111:6305-6310.
41. Offringa R., Huang F. Phosphorylation-dependent trafficking of plasma membrane proteins in animal and plant cells. J Integr Plant Biol 2013, 55:789-808.
42. Traub L.M. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 2009, 10:583-596.
43. van Balkom B.W., Savelkoul P.J., Markovich D., Hofman E., Nielsen S., van der Sluijs P., Deen P.M. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 2002, 277:41473-41479.
44. Kamsteeg E.J., Hendriks G., Boone M., Konings I.B., Oorschot V., van der Sluijs P., Klumperman J., Deen P.M. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc Natl Acad Sci U S A 2006, 103:18344-18349.
45. Lu H.A., Sun T.X., Matsuzaki T., Yi X.H., Eswara J., Bouley R., McKee M., Brown D. Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking. J Biol Chem 2007, 282:28721-28732.
46. van Balkom B.W., Boone M., Hendriks G., Kamsteeg E.J., Robben J.H., Stronks H.C., van der Voorde A., van Herp F., van der Sluijs P., Deen P.M. LIP5 interacts with aquaporin 2 and facilitates its lysosomal degradation. J Am Soc Nephrol 2009, 20:990-1001.
47. Noda Y., Horikawa S., Furukawa T., Hirai K., Katayama Y., Asai T., Kuwahara M., Katagiri K., Kinashi T., Hattori M., et al. Aquaporin-2 trafficking is regulated by PDZ-domain containing protein SPA-1. FEBS Lett 2004, 568:139-145.
48. Sjohamn J., Hedfalk K. Unraveling aquaporin interaction partners. Biochim Biophys Acta 2014, 1840:1614-1623.
49. Reichow S.L., Gonen T. Noncanonical binding of calmodulin to aquaporin-0: implications for channel regulation. Structure 2008, 16:1389-1398.
50. Gonen T., Sliz P., Kistler J., Cheng Y., Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 2004, 429:193-197.
51. Harries W.E., Akhavan D., Miercke L.J., Khademi S., Stroud R.M. The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci U S A 2004, 101:14045-14050.
52. Horsefield R., Norden K., Fellert M., Backmark A., Tornroth-Horsefield S., Terwisscha van Scheltinga A.C., Kvassman J., Kjellbom P., Johanson U., Neutze R. High-resolution X-ray structure of human aquaporin 5. Proc Natl Acad Sci U S A 2008, 105:13327-13332.
53. Skalicky J.J., Arii J., Wenzel D.M., Stubblefield W.M., Katsuyama A., Uter N.T., Bajorek M., Myszka D.G., Sundquist W.I. Interactions of the human LIP5 regulatory protein with endosomal sorting complexes required for transport. J Biol Chem 2012, 287:43910-43926.
54. 2+-calmodulin. Nat Struct Mol Biol 2013, 20:1085-1092.
55. Tornroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., Neutze R., Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 2006, 439:688-694.
56. Nyblom M., Frick A., Wang Y., Ekvall M., Hallgren K., Hedfalk K., Neutze R., Tajkhorshid E., Tornroth-Horsefield S. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J Mol Biol 2009, 387:653-668.
57. Moeller H.B., Rittig S., Fenton R.A. Nephrogenic diabetes insipidus: essential insights into the molecular background and potential therapies for treatment. Endocr Rev 2013, 34:278-301.