Desalination by biomimetic aquaporin membranes: Review of status and prospects

Desalination

Volumn 308, Issue , 2013, Pages 34-40

  Tang, C Y ^a,b   Zhao, Y ^a,b   Wang, R ^a,b   Helix Nielsen C ^c,d   Fane, A G ^a,b  

^a Singapore Membrane Technology Centre   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c AQUAPORIN A S   (Denmark)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Aquaporin; Biomimetic membranes; Desalination

Indexed keywords

AQUAPORINS; BIOMIMETIC MEMBRANE; BUILDING BLOCKES; FUTURE PROSPECTS; HIGH WATER; MEMBRANE SEPARATION PROCESS; SOLUTE REJECTION; STATUS AND PROSPECT; WATER DESALINATION; WATER REUSE;

BIOMIMETICS; DESALINATION; PROTEINS; WASTEWATER RECLAMATION; WATER CONSERVATION; WATER FILTRATION; WATER SUPPLY;

MEMBRANES;

DESALINATION; MEMBRANE; PERMEABILITY; SEPARATION; PROTEIN;

EID: 84870765872     PISSN: 00119164     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.desal.2012.07.007     Document Type: Review

References (88)

1. Loeb S., Sourirajan S. Sea water demineralization by means of an osmotic membrane. Adv. Chem. Ser. 1962, 38:117. (et seq).
2. Truby R. Chapter 4: seawater desalination by ultralow energy reverse osmosis. J.Wiley 2008, 87-100. N. Li, N (Eds.).
3. Elimelech M., Phillip W.A. The future of seawater desalination: energy, technology, and the environment. Science 2011, 333:712-717.
4. Bowen W.R. Biomimetic separations - learning from the early development of biological membranes. Desalination 2006, 199:225-227.
5. Kumar M., Grzelakowski M., Zilles J., Clark M., Meier W. Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20719-20724.
6. Pendergast M.M., Hoek E.M.V. A review of water treatment membrane nanotechnologies. Energy Environ. Sci. 2011, 4:1946-1971.
7. Gonen T., Walz T. The structure of aquaporins. Q. Rev. Biophys. 2006, 39:361-396.
8. Fu D., Lu M. The structural basis of water permeation and proton exclusion in aquaporins. Mol. Membr. Biol. 2007, 24:366-374.
9. Ishibashi K. Aquaporin subfamily with unusual NPA boxes. Biochim. Biophys. Acta 2006, 1758:989-993.
10. Verkman A.S. More than just water channels: unexpected cellular roles of aquaporins. J. Cell Sci. 2005, 118:3225-3232.
11. Nielsen S., Frokiaer J., Marples D., Kwon T.H., Agre P., Knepper M.A. Aquaporins in the kidney: from molecules to medicine. Physiol. Rev. 2002, 82:205-244.
12. Denker B.M., Smith B.L., Kuhajda F.P., Agre P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 1988, 263:15634-15642.
13. Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 1992, 256:385-387.
14. Zeidel M.L., Ambudkar S.V., Smith B.L., Agre P. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 1992, 31:7436-7440.
15. Agre P., Sasaki S., Chrispeels M.J. Aquaporins: a family of water channel proteins. Am. J. Physiol. 1993, 265:F461.
16. Verbavatz J.M., Brown D., Sabolic I., Valenti G., Ausiello D.A., Van Hoek A.N., Ma T., Verkman A.S. Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study. J. Cell Biol. 1993, 123:605-618.
17. Borgnia M.J., Agre P. Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2888-2893.
18. Calamita G., Bishai W.R., Preston G.M., Guggino W.B., Agre P. Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J. Biol. Chem. 1995, 270:29063-29066.
19. Savage D.F., Egea P.F., Robles-Colmenares Y., O'Connell J.D., Stroud R.M. Architecture and selectivity in aquaporins: 2.5 a X-ray structure of aquaporin Z. PLoS Biol. 2003, 1:E72.
20. Fu D., Libson A., Miercke L.J., Weitzman C., Nollert P., Krucinski J., Stroud R.M. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 2000, 290:481-486.
21. Xin L., Su H., Nielsen C.H., Tang C., Torres J., Mu Y. Water permeation dynamics of AqpZ: a tale of two states. Biochim. Biophys. Acta 2011, 1808:1581-1586.
22. Nemeth-Cahalan K.L., Hall J.E. pH and calcium regulate the water permeability of aquaporin 0. J. Biol. Chem. 2000, 275:6777-6782.
23. 2+ regulation of aquaporin water permeability. J. Gen. Physiol. 2004, 123:573-580.
24. 2+ and apoplastic water potential. Plant Cell 1996, 8:1181-1191.
25. 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.
26. Zeuthen T., Klaerke D.A. Transport of water and glycerol in aquaporin 3 is gated by H(+). J. Biol. Chem. 1999, 274:21631-21636.
27. 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.
28. Jensen M.O., Mouritsen O.G. Single-channel water permeabilities of Escherichia coli aquaporins AqpZ and GlpF. Biophys. J. 2006, 90:2270-2284.
29. Hille B. Ionic Channels of Excitable Membranes 2001, Sinauer, Sunderland.
30. Gurdon J.B., Lane C.D., Woodland H.R., Marbaix G. Use of frog eggs and oocytes for the study of messenger RNA and its translation in living cells. Nature 1971, 233:177-182.
31. Meinild A.K., Klaerke D.A., Zeuthen T. Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporins 0-5. J. Biol. Chem. 1998, 273:32446-32451.
32. Borgnia M.J., Kozono D., Calamita G., Maloney P.C., Agre P. Functional reconstitution and characterization of AqpZ, the E. coli water channel protein. J. Mol. Biol. 1999, 291:1169-1179.
33. Scheuring S., Ringler P., Borgnia M., Stahlberg H., Müller D.J., Agre P., Engel A. High resolution AFM topographs of the Escherichia coli water channel aquaporin Z. EMBO J. 1999, 18:7.
34. Mathai J.C., Tristram-Nagle S., Nagle J.F., Zeidel M.L. Structural determinants of water permeability through the lipid membrane. J. Gen. Physiol. 2008, 131:8.
35. Hovijitra N.T., Wuu J.J., Peaker B., Swartz J.R. Cell-free synthesis of functional aquaporin Z in synthetic liposomes. Biotechnol. Bioeng. 2009, 104:10.
36. Kaldenhoff R., Bertl A., Otto B., Moshelion M., Uehlein N. Characterization of plant aquaporins. Methods Enzymol. 2007, 428:505-531.
37. Shi L.B., Skach W.R., Ma T., Verkman A.S. Distinct biogenesis mechanisms for the water channels MIWC and CHIP28 at the endoplasmic reticulum. Biochemistry 1995, 34:8250-8256.
38. Altamura N., Calamita G. Systems for production of proteins for biomimetic membrane devices. Biomimetic Membranes for Sensor and Separation Applications 2012, 233-250. Springer, Dordrecht. C. Hélix-Nielsen (Ed.).
39. Lee J.K., Kozono D., Remis J., Kitagawa Y., Agre P., Stroud R.M. Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 A. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18932-18937.
40. Lian J., Ding S., Cai J., Zhang D., Xu Z., Wang X. Improving aquaporin Z expression in Escherichia coli by fusion partners and subsequent condition optimization. Appl. Microbiol. Biotechnol. 2009, 82:463-470.
41. Bienert G.P., Moller A.L., Kristiansen K.A., Schulz A., Moller I.M., Schjoerring J.K., Jahn T.P. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 2007, 282:1183-1192.
42. Fischer G., Kosinska-Eriksson U., Aponte-Santamaria C., Palmgren M., Geijer C., Hedfalk K., Hohmann S., de Groot B.L., Neutze R., Lindkvist-Petersson K. Crystal structure of a yeast aquaporin at 1.15 angstrom reveals a novel gating mechanism. PLoS Biol. 2009, 7:e1000130.
43. Hedfalk K., Pettersson N., Oberg F., Hohmann S., Gordon E. Production, characterization and crystallization of the Plasmodium falciparum aquaporin. Protein Expr. Purif. 2008, 59:69-78.
44. Laize V., Ripoche P., Tacnet F. Purification and functional reconstitution of the human CHIP28 water channel expressed in Saccharomyces cerevisiae. Protein Expr. Purif. 1997, 11:284-288.
45. Pettersson N., Hagstrom J., Bill R.M., Hohmann S. Expression of heterologous aquaporins for functional analysis in Saccharomyces cerevisiae. Curr. Genet. 2006, 50:247-255.
46. Oberg F., Ekvall M., Nyblom M., Backmark A., Neutze R., Hedfalk K. Insight into factors directing high production of eukaryotic membrane proteins; production of 13 human AQPs in Pichia pastoris. Mol. Membr. Biol. 2009, 26:215-227.
47. Azad A.K., Katsuhara M., Sawa Y., Ishikawa T., Shibata H. Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation. Plant Cell Physiol. 2008, 49:1196-1208.
48. Azad A.K., Sawa Y., Ishikawa T., Shibata H. Heterologous expression of tulip petal plasma membrane aquaporins in Pichia pastoris for water channel analysis. Appl. Environ. Microbiol. 2009, 75:2792-2797.
49. Daniels M.J., Wood M.R., Yeager M. In vivo functional assay of a recombinant aquaporin in Pichia pastoris. Appl. Environ. Microbiol. 2006, 72:1507-1514.
50. Karlsson M., Fotiadis D., Sjovall S., Johansson I., Hedfalk K., Engel A., Kjellbom P. Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett. 2003, 537:68-72.
51. Kukulski W., Schenk A.D., Johanson U., Braun T., de Groot B.L., Fotiadis D., Kjellbom P., Engel A. The 5A structure of heterologously expressed plant aquaporin SoPIP2;1. J. Mol. Biol. 2005, 350:611-616.
52. 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.
53. 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.
54. Yang B., van Hoek A.N., Verkman A.S. Very high single channel water permeability of aquaporin-4 in baculovirus-infected insect cells and liposomes reconstituted with purified aquaporin-4. Biochemistry 1997, 36:7625-7632.
55. Swamy-Mruthinti S., Schey K.L. Mass spectroscopic identification of in vitro glycated sites of MIP. Curr. Eye Res. 1997, 16:936-941.
56. Werten P.J., Hasler L., Koenderink J.B., Klaassen C.H., de Grip W.J., Engel A., Deen P.M. Large-scale purification of functional recombinant human aquaporin-2. FEBS Lett. 2001, 504:200-205.
57. Drake K.D., Schuette D., Chepelinsky A.B., Crabbe M.J. Heterologous expression and topography of the main intrinsic protein (MIP) from rat lens. FEBS Lett. 2002, 512:191-198.
58. Drake K.D., Schuette D., Chepelinsky A.B., Jacob T.J., Crabbe M.J. pH-Dependent channel activity of heterologously-expressed main intrinsic protein (MIP) from rat lens. FEBS Lett. 2002, 512:199-204.
59. 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. 2006, 355:628-639.
60. Yakata K., Hiroaki Y., Ishibashi K., Sohara E., Sasaki S., Mitsuoka K., Fujiyoshi Y. Aquaporin-11 containing a divergent NPA motif has normal water channel activity. Biochim. Biophys. Acta 2007, 1768:688-693.
61. Hayakawa S., Mori M., Okuta A., Kamegawa A., Fujiyoshi Y., Yoshiyama Y., Mitsuoka K., Ishibashi K., Sasaki S., Hattori T., Kuwabara S. Neuromyelitis optica and anti-aquaporin-4 antibodies measured by an enzyme-linked immunosorbent assay. J. Neuroimmunol. 2008, 196:181-187.
62. LaVallie E.R., Lu Z., Diblasio-Smith E.A., Collins-Racie L.A., McCoy J.M. Thioredoxin as a fusion partner for production of soluble recombinant proteins in Escherichia coli. Methods Enzymol. 2000, 326:322-340.
63. Lu Y., Turnbull I.R., Bragin A., Carveth K., Verkman A.S., Skach W.R. Reorientation of aquaporin-1 topology during maturation in the endoplasmic reticulum. Mol. Biol. Cell 2000, 11:2973-2985.
64. Paul D.L., Goodenough D.A. In vitro synthesis and membrane insertion of bovine MP26, an integral protein from lens fiber plasma membrane. J. Cell Biol. 1983, 96:633-638.
65. Xu Z., Lian J., Cai J. Efficient expression of aquaporin Z in Escherichia coli cell-free system using different fusion vectors. Protein Pept. Lett. 2010, 17:181-185.
66. Schwarz D., Junge F., Durst F., Frolich N., Schneider B., Reckel S., Sobhanifar S., Dotsch V., Bernhard F. Preparative scale expression of membrane proteins in Escherichia coli-based continuous exchange cell-free systems. Nat. Protoc. 2007, 2:2945-2957.
67. Hovijitra N.T., Wuu J.J., Peaker B., Swartz J.R. Cell-free synthesis of functional aquaporin Z in synthetic liposomes. Biotechnol. Bioeng. 2009, 104:40-49.
68. Zawada J.F., Yin G., Steiner A.R., Yang J., Naresh A., Roy S.M., Gold D.S., Heinsohn H.G., Murray C.J. Microscale to manufacturing scale-up of cell-free cytokine production-a new approach for shortening protein production development timelines. Biotechnol. Bioeng. 2011, 108:1570-1578.
69. Hansen J.S., Vararattanavech A., Plasencia I., Greisen P.J., Bomholt J., Torres J., Emneus J., Helix-Nielsen C. Interaction between sodium dodecyl sulfate and membrane reconstituted aquaporins: a comparative study of spinach SoPIP2;1 and E. coli AqpZ. Biochim. Biophys. Acta 2011, 1808:2600-2607.
70. Plasencia I., Survery S., Ibragimova S., Hansen J.S., Kjellbom P., Helix-Nielsen C., Johanson U., Mouritsen O.G. Structure and stability of the spinach aquaporin SoPIP2;1 in detergent micelles and lipid membranes. PLoS One 2011, 6:e14674.
71. Andersen O.S., Nielsen C., Maer A.M., Lundbæk J.A., Goulian M., Koeppe R.E. Gramicidin channels as molecular force transducers in lipid bilayers. Biol. Skr. Dan. Vid. Selsk. 1998, 49:75-82.
72. Nielsen C., Goulian M., Andersen O.S. Energetics of inclusion-induced bilayer deformations. Biophys. J. 1998, 74:1966-1983.
73. Pszon-Bartosz K., Hansen J.S., Stibius K.B., Groth J.S., Emneus J., Geschke O., Helix-Nielsen C. Assessing the efficacy of vesicle fusion with planar membrane arrays using a mitochondrial porin as reporter. Biochem. Biophys. Res. Commun. 2011, 406:96-100.
74. Tang C.Y., Kwon Y.-N., Leckie J.O. Effect of membrane chemistry and coating layer on physiochemical properties of thin film composite polyamide RO and NF membranes II. Membrane physiochemical properties and their dependence on polyamide and coating layers. Desalination 2009, 242:168-182.
75. Nielsen C.H. Biomimetic membranes for sensor and separation applications. Anal. Bioanal. Chem. 2009, 395:697-718.
76. Hansen J.S., Perry M.E., Vogel J., Vissing T., Geschke O., Emneus J., Nielsen C.H. Development of an automation technique for the establishment of functional lipid bilayer arrays. J. Micromech. Microeng. 2009, 19:025014.
77. Vogel J., Perry M.E., Hansen J.S., Bollinger P.-Y., Nielsen C.H., Geschke O. Support structure for biomimetic applications. J. Micromech. Microeng. 2009, 19:025026.
78. Hansen J.S., Perry M., Vogel J., Groth J., Vissing T., Larsen M., Geschke O., Emneus J., Bohr H., Nielsen C.H. Large scale biomimetic membrane arrays. Anal. Bioanal. Chem. 2009, 395:719-727.
79. Gonzalez-Perez A., Stibius K.B., Vissing T., Nielsen C.H., Mouritsen O.G. Biomimetic triblock copolymer membrane arrays: a stable template for functional membrane proteins. Langmuir 2009, 25:10447-10450.
80. Rein C., Pszon-Bartosz K., Stibius K.B., Bjornholm T., Helix-Nielsen C. Free-standing biomimetic polymer membrane imaged with atomic force microscopy. Langmuir 2011, 27:499-503.
81. Roerdink Lander M., Ibragimova S., Rein C., Vogel J., Stibius K., Geschke O., Perry M., Helix-Nielsen C. Biomimetic membrane arrays on cast hydrogel supports. Langmuir 2011, 27:7002-7007.
82. Ibragimova S., Stibius K.B., Szewczykowski P., Perry M., Bohr H., Nielsen C.H. Hydrogels for in situ encapsulation of biomimetic membrane arrays. Polym. Adv. Technol. 2011, 23:182-189.
83. Kaufman Y., Berman A., Freger V. Supported lipid bilayer membranes for water purification by reverse osmosis. Langmuir 2010, 26:7388-7395.
84. Zhong P.S., Chung T.-S., Jeyaseelan K., Armugam A. Aquaporin-embedded biomimetic membranes for nanofiltration. J. Membr. Sci. 2012, 407-408:27-33.
85. Sun G., Zhou H., Li Y., Jeyaseelan K., Armugam A., Chung T.-S. A novel method of AquaporinZ incorporation via binary-lipid Langmuir monolayers. Colloids Surf. B Biointerfaces 2012, 89:283-288.
86. Wang H., Chung T.S., Tong Y.W., Jeyaseelan K., Armugam A., Chen Z., Hong M., Meier W. Highly permeable and selective pore-spanning biomimetic membrane embedded with aquaporin z. Small 2012, 8:1185-1190.
87. Li X., Wang R., Tang C.Y., Vararattanavech A., Zhao Y., Torres J., Fane A.G. Preparation of supported lipid membranes for aquaporin Z incorporation. Colloids Surf. B Biointerfaces 2012, 94:333-340.
88. Y. Zhao, C. Qiu, X. Li, A. Vararattanavech, W. Shen, J. Torres, C. Hélix-Nielsen, R. Wang, X. Hu, A.G. Fane, C.Y. Tang, Synthesis of Robust and High-performance Aquaporin-based Biomimetic Membranes by Interfacial Polymerization - Membrane Preparation and RO Performance Characterization, J. Membr. Sci. (under review).