Mutation of a single amino acid converts the human water channel aquaporin 5 into an anion channel

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 6, 2013, Pages

  Qin, Xue ^a   Boron, Walter F ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anion channel; Aquaporin 5; Gas channels; Gas transport; Water transport

Indexed keywords

AMINO ACID; ANION CHANNEL; AQUAPORIN 5; AQUAPORIN 6; ARGININE; ASPARTIC ACID; CARBON DIOXIDE; CHLOROMERCURIBENZENESULFONIC ACID; CYSTEINE; GLUTAMIC ACID; LEUCINE; NITROGEN DIOXIDE; SERINE; WATER;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANION TRANSPORT; ARTICLE; BIOTINYLATION; BIOTRANSFORMATION; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; ION CONDUCTANCE; MICROELECTRODE; NONHUMAN; OOCYTE; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SURFACE PROPERTY; VIDEORECORDING; VOLTAGE CLAMP; WATER PERMEABILITY; WILD TYPE; XENOPUS;

ANION CHANNEL; AQUAPORIN 5; GAS CHANNELS; GAS TRANSPORT; WATER TRANSPORT;

AMINO ACID SUBSTITUTION; ANIMALS; ANIONS; AQUAPORIN 5; CARBON DIOXIDE; CELL MEMBRANE; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNELS; LEUCINE; OOCYTES; PERMEABILITY; POINT MUTATION; WATER; XENOPUS LAEVIS;

EID: 84884364944     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00129.2013     Document Type: Article

References (57)

1. Agemark M, Kowal J, Kukulski W, Nordén K, Gustavsson N, Johanson U, Engel A, Kjellbom P. Reconstitution of water channel function and 2D-crystallization of human aquaporin 8. Biochim Biophys Acta 1818: 839-850, 2012.
2. Agre P. Aquaporin water channels (Nobel Lecture). Angew Chem Int Ed Engl 43: 4278-4290, 2004.
3. Boron WF. Sharpey-Schafer lecture: gas channels. Exp Physiol 95: 1107-1130, 2010.
4. Cooper GJ, Boron WF. Effect of pCMBS on CO2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant. Am J Physiol Cell Physiol 275: C1481-C1486, 1998.
5. Cooper GJ, Zhou Y, Bouyer P, Grichtchenko II, Boron WF. Transport of volatile solutes through AQP1. J Physiol 542: 17-29, 2002.
6. Endeward V, Cartron JP, Ripoche P, Gros G. RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane. FASEB J 22: 64-73, 2008.
7. Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV, Supuran CT, King LS, Boron WF, Gros G. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J 20: 1974-1981, 2006.
8. Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P, Krucinski J, Stroud RM. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290: 481-486, 2000.
9. Geyer RR, Musa-Aziz R, Enkavi G, Mahinthichaichan P, Tajkhorshid E, Boron WF. Movement of NH3 through the human urea transporter B (UT-B): a new gas channel. Am J Physiol Renal Physiol 304: F1447-F1457, 2013.
10. Geyer RR, Musa-Aziz R, Qin X, Boron WF. Relative CO2/NH3 selectivities of mammalian aquaporins 0-9. Am J Physiol Cell Physiol 304: C985-C994, 2013.
11. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429: 193-197, 2004.
12. Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M. Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45: 521-529, 2004.
13. Harries WEC, Akhavan D, Miercke LJW, Khademi S, Stroud RM. The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci USA 101: 14045-14050, 2004.
14. 2+ activation. J Biol Chem 277: 29224-29230, 2002.
15. Herrera M, Garvin JL. Novel role of AQP-1 in NO-dependent vasorelaxation. Am J Physiol Renal Physiol 292: F1443-F1451, 2007.
16. Herrera M, Hong NJ, Garvin JL. Aquaporin-1 transports NO across cell membranes. Hypertension 48: 157-164, 2006.
17. Hiroaki Y, Tani K, Kamegawa A, Gyobu N, Nishikawa K, Suzuki H, Walz T, Sasaki S, Mitsuoka K, Kimura K, Mizoguchi A, Fujiyoshi Y. Implications of the aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 355: 628-639, 2006.
18. Ho JD, Yeh R, Sandstrom A, Chorny I, Harries WE, Robbins RA, Miercke LJW, Stroud RM. Crystal structure of human aquaporin 4 at 1.8 A and its mechanism of conductance. Proc Natl Acad Sci USA 106: 7437-7442, 2009.
19. Horsefield R, Nordén K, Fellert M, Backmark A, Törnroth-Horsefield S, Terwisscha van Scheltinga AC, Kvassman J, Kjellbom P, Johanson U, Neutze R. High-resolution x-ray structure of human aquaporin 5. Proc Natl Acad Sci USA 105: 13327-13332, 2008.
20. Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M. Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J Biol Chem 277: 39873-39879, 2002.
21. Jiang J, Daniels BV, Fu D. Crystal structure of AqpZ tetramer reveals two distinct Arg-189 conformations associated with water permeation through the narrowest constriction of the water-conducting channel. J Biol Chem 281: 454-460, 2006.
22. Jung JS, Preston GM, Smith BL, Guggino WB, Agre P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem 269: 14648-14654, 1994.
23. Karabasil MR, Hasegawa T, Azlina A, Purwanti N, Yao C, Akamatsu T, Tomioka S, Hosoi K. Effects of naturally occurring G103D point mutation of AQP5 on its water permeability, trafficking and cellular localization in the submandibular gland of rats. Biol Cell 103: 69-86, 2011.
24. King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5: 687-698, 2004.
25. Kustu S, Inwood W. Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels. Transfus Clin Biol 13: 103-110, 2006.
26. Lee JK, Kozono D, Remis J, Kitagawa Y, Agre P, Stroud RM. Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 A. Proc Natl Acad Sci USA 102: 18932-18937, 2005.
27. Lee MD, Bhakta KY, Raina S, Yonescu R, Griffin CA, Copeland NG, Gilbert DJ, Jenkins NA, Preston GM, Agre P. The human Aquaporin-5 gene. Molecular characterization and chromosomal localization. J Biol Chem 271: 8599-8604, 1996.
28. Liu K, Kozono D, Kato Y, Agre P, Hazama A, Yasui M. Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution. Proc Natl Acad Sci USA 102: 2192-2197, 2005.
29. Ma T, Yang B, Umenishi F, Verkman AS. Closely spaced tandem arrangement of AQP2, AQP5, and AQP6 genes in a 27-kilobase segment at chromosome locus 12q13. Genomics 43: 387-389, 1997.
30. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature 407: 599-605, 2000.
31. Murdiastuti K, Purwanti N, Karabasil MR, Li X, Yao C, Akamatsu T, Kanamori N, Hosoi K. A naturally occurring point mutation in the rat aquaporin 5 gene, influencing its protein production by and secretion of water from salivary glands. Am J Physiol Gastrointest Liver Physiol 291: G1081-G1088, 2006.
32. Musa-Aziz R, Boron WF, Parker MD. Using fluorometry and ionsensitive microelectrodes to study the functional expression of heterologously- expressed ion channels and transporters in Xenopus oocytes. Methods 51: 134-145, 2010.
33. Musa-Aziz R, Chen LM, Pelletier MF, Boron WF. Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 106: 5406-5411, 2009.
34. +. J Membr Biol 228: 15-31, 2009.
35. Musa-Aziz R, Pergher P, Boron WF. Evidence from surface-pH transients that DIDS and pCMBS reduce the CO2 permeability of AQP1 expressed in Xenopus oocytes (Abstract). J Am Soc Nephrol 19: 350A, 2008.
36. Nakhoul NL, Davis BA, Romero MF, Boron WF. Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. Am J Physiol Cell Physiol 274: C543-C548, 1998.
37. - cotransporter (SLC4A4) in a case of proximal renal tubular acidosis with hypokalaemic paralysis. J Physiol 590: 2009-2034, 2012.
38. Prasad GV, Coury LA, Finn F, Zeidel ML. Reconstituted aquaporin 1 water channels transport CO2 across membranes. J Biol Chem 273: 33123-33126, 1998.
39. Preston GM, Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci USA 88: 11110-11114, 1991.
40. Preston GM, Carroll TP, Guggino WB, Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256: 385-387, 1992.
41. Preston GM, Jung JS, Guggino WB, Agre P. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem 268: 17-20, 1993.
42. Qin X, Boron WF. Effect of DIDS and pCMBS on the CO2 permeability of human aquaporin-5 (AQP5) (Abstract). FASEB J 24: 610-5, 2010.
43. Ripoche P, Goossens D, Devuyst O, Gane P, Colin Y, Verkman AS, Cartron JP. Role of RhAG and AQP1 in NH3 and CO2 gas transport in red cell ghosts: a stopped-flow analysis. Transfus Clin Biol 13: 117-122, 2006.
44. Savage DF, Egea PF, Robles-Colmenares Y, O'Connell JD 3rd, Stroud RM. Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z. PLoS Biol 1: E72, 2003.
45. Schenk AD, Werten PJ, Scheuring S, de Groot BL, Müller SA, Stahlberg H, Philippsen A, Engel A. The 4.5 Å structure of human AQP2. J Mol Biol 350: 278-289, 2005.
46. Sui H, Han BG, Lee JK, Walian P, Jap BK. Structural basis of water-specific transport through the AQP1 water channel. Nature 414: 872-878, 2001.
47. Tajkhorshid E, Nollert P, Jensen MØ, Miercke LJW, O'Connell J, Stroud RM, Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296: 525-530, 2002.
48. Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 439: 688-694, 2006.
49. Toye AM, Parker MD, Daly CM, Lu J, Virkki LV, Pelletier MF, Boron WF. The human NBCe1-A mutant R881C, associated with proximal renal tubular acidosis, retains function but is mistargeted in polarized renal epithelia. Am J Physiol Cell Physiol 291: C788-C801, 2006.
50. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425: 734-737, 2003.
51. Uehlein N, Otto B, Eilingsfeld A, Itel F, Meier W, Kaldenhoff R. Gas-tight triblock-copolymer membranes are converted to CO2 permeable by insertion of plant aquaporins. Sci Rep 2: 538, 2012.
52. Walz T, Hirai T, Murata K, Heymann JB, Mitsuoka K, Fujiyoshi Y, Smith BL, Agre P, Engel A. The three-dimensional structure of aquaporin-1. Nature 387: 624-627, 1997.
53. Walz T, Smith BL, Zeidel ML, Engel A, Agre P. Biologically active two-dimensional crystals of aquaporin CHIP. J Biol Chem 269: 1583-1586, 1994.
54. Wang Y, Cohen J, Boron WF, Schulten K, Tajkhorshid E. Exploring gas permeability of cellular membranes and membrane channels with molecular dynamics. J Struct Biol 157: 534-544, 2007.
55. Wang Y, Tajkhorshid E. Nitric oxide conduction by the brain aquaporin AQP4. Proteins 78: 661-670, 2010.
56. Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P. Rapid gating and anion permeability of an intracellular aquaporin. Nature 402: 184-187, 1999.
57. Zhang YB, Chen LY. In silico study of Aquaporin V: effects and affinity of the central pore-occluding lipid. Biophys Chem 171: 24-30, 2013.