Lyotropic Liquid Crystalline Cubic Phases as Versatile Host Matrices for Membrane-Bound Enzymes

Journal of Physical Chemistry Letters

Volumn 7, Issue 8, 2016, Pages 1507-1512

  Sun, Wenjie ^a   Vallooran, Jijo J ^a   Fong, Wye Khay ^a,b   Mezzenga, Raffaele ^a  

^a ETH ZURICH   (Switzerland)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; CRYSTALLINE MATERIALS; ENZYMES; FUEL CELLS; REUSABILITY;

FUEL CELL APPLICATION; HORSE-RADISH PEROXIDASE; IMMOBILIZED MEMBRANES; LYOTROPIC LIQUID CRYSTALLINE; MEMBRANE-BOUND ENZYMES; MICHAELIS-MENTEN KINETIC; STRUCTURAL CHARACTERISTICS; THREE-DIMENSIONAL STRUCTURE;

ENZYME ACTIVITY;

ARTIFICIAL MEMBRANE; D-FRUCTOSE 5-DEHYDROGENASE; HORSERADISH PEROXIDASE; IMMOBILIZED ENZYME; OXIDOREDUCTASE;

ARTIFICIAL MEMBRANE; CHEMISTRY; ENZYME STABILITY; KINETICS; LIQUID CRYSTAL; METABOLISM;

CARBOHYDRATE DEHYDROGENASES; ENZYME STABILITY; ENZYMES, IMMOBILIZED; HORSERADISH PEROXIDASE; KINETICS; LIQUID CRYSTALS; MEMBRANES, ARTIFICIAL;

EID: 84966936567     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/acs.jpclett.6b00416     Document Type: Article

References (54)

1. Taqieddin, E.; Amiji, M. Enzyme Immobilization in Novel Alginate-Chitosan Core/Shell Microcapsules Biomaterials 2004, 25, 1937-1945 10.1016/j.biomaterials.2003.08.034
2. Altstein, M.; Segev, G.; Aharonson, N.; Ben-Aziz, O.; Turniansky, A.; Avnir, D. Sol-Gel-Entrapped Cholinesterases: a Microtiter Plate Method for Monitoring Anti-Cholinesterase Compounds J. Agric. Food Chem. 1998, 46, 3318-3324 10.1021/jf9801015
3. Dyal, A.; Loos, K.; Noto, M.; Chang, S. W.; Spagnoli, C.; Shafi, K. V.; Ulman, A.; Cowman, M.; Gross, R. A. Activity of Candida Rugosa Lipase Immobilized on γ-Fe2O3Magnetic Nanoparticles J. Am. Chem. Soc. 2003, 125, 1684-1685 10.1021/ja021223n
4. Wu, J. C.; Hutchings, C. H.; Lindsay, M. J.; Werner, C. J.; Bundy, B. C. Enhanced Enzyme Stability through Site-Directed Covalent Immobilization J. Biotechnol. 2015, 193, 83-90 10.1016/j.jbiotec.2014.10.039
5. Wahba, M. I.; Hassan, M. E. Novel Grafted Agar Disks for the Covalent Immobilization of β-D-Galactosidase Biopolymers 2015, 103, 675-684 10.1002/bip.22693
6. Luckarift, H. R.; Spain, J. C.; Naik, R. R.; Stone, M. O. Enzyme Immobilization in a Biomimetic Silica Support Nat. Biotechnol. 2004, 22, 211-213 10.1038/nbt931
7. Rodrigues, R. C.; Ortiz, C.; Berenguer-Murcia, A.; Torres, R.; Fernández-Lafuente, R. Modifying Enzyme Activity and Selectivity by Immobilization Chem. Soc. Rev. 2013, 42, 6290-6307 10.1039/C2CS35231A
8. Mateo, C.; Palomo, J. M.; Fernandez-Lorente, G.; Guisan, J. M.; Fernandez-Lafuente, R. Improvement of Enzyme Activity, Stability and Selectivity via Immobilization Techniques Enzyme Microb. Technol. 2007, 40, 1451-1463 10.1016/j.enzmictec.2007.01.018
9. Sun, W.; Vallooran, J. J.; Zabara, A.; Mezzenga, R. Controlling Enzymatic Activity and Kinetics in Swollen Mesophases by Physical Nano-Confinement Nanoscale 2014, 6, 6853-5859 10.1039/c4nr01394h
10. Sun, W.; Vallooran, J. J.; Mezzenga, R. Enzyme Kinetics in Liquid Crystalline Mesophases: Size Matter, But Also Topology Langmuir 2015, 31, 4558-4565 10.1021/acs.langmuir.5b00579
11. Rigaud, J.-L.; Lévy, D. Reconstitution of Membrane Proteins into Liposomes Methods Enzymol. 2003, 372, 65-86 10.1016/S0076-6879(03)72004-7
12. Wadsten, P.; Wöhri, A. B.; Snijder, A.; Katona, G.; Gardiner, A. T.; Cogdell, R. J.; Neutze, R.; Engström, S. Lipidic Sponge Phase Crystallization of Membrane Proteins J. Mol. Biol. 2006, 364, 44-53 10.1016/j.jmb.2006.06.043
13. Mi, L. Z.; Grey, M. J.; Nishida, N.; Walz, T.; Lu, C.; Springer, T. A. Functional and Structural Stability of the Epidermal Growth Factor Receptor in Detergent Micelles and Phospholipid Nanodiscs Biochemistry 2008, 47, 10314-10323 10.1021/bi801006s
14. Bayburt, T. H.; Sligar, S. G. Membrane Protein Assembly into Nanodiscs FEBS Lett. 2010, 584, 1721-1727 10.1016/j.febslet.2009.10.024
15. Demurtas, D.; Guichard, P.; Martiel, I.; Mezzenga, R.; Hébert, C.; Sagalowicz, L. Direct Visualization of Dispersed Lipid Bicontinuous Cubic Phases by Cryo-Electron Tomography Nat. Commun. 2015, 6, 8915 10.1038/ncomms9915
16. Fong, W.; Hanley, T.; Boyd, B. Stimuli Responsive Liquid Crystals Provide 'on-demand' Drug Delivery in vitro and in vivo J. Controlled Release 2009, 135, 218-226 10.1016/j.jconrel.2009.01.009
17. Negrini, R.; Mezzenga, R. pH-Responsive Lyotropic Liquid Crystals for Controlled Drug Delivery Langmuir 2011, 27, 5296-5303 10.1021/la200591u
18. 1 Hosted in the Monoolein/Water Liquid Crystalline Phases Langmuir 1997, 13, 5476-5483 10.1021/la9702188
19. Boyd, B. J.; Whittaker, D. V.; Khoo, S.-M.; Davey, G. Lyotropic Liquid Crystalline Phases Formed from a Glycerate Surfactant as Sustained Release Drug Delivery System Int. J. Pharm. 2006, 309, 218-226 10.1016/j.ijpharm.2005.11.033
20. Amar-Yuli, I.; Libster, D.; Aserin, A.; Garti, N. Solubilization of Food Bioactives within Lyotropic Liquid Crystalline Mesophases Curr. Opin. Colloid Interface Sci. 2009, 14, 21-32 10.1016/j.cocis.2008.02.001
21. Clogston, J.; Caffrey, M. Controlling Release from the Lipidic Cubic Phase. Amino Acids, Peptides, Proteins and Nucleic Acids J. Controlled Release 2005, 107, 97-111 10.1016/j.jconrel.2005.05.015
22. Angelov, B.; Angelova, A.; Filippov, S. K.; Drechsler, M.; Štěpánek, P.; Lesieur, S. Multicompartment Lipid Cubic Nanoparticles with High Protein Upload: Millisecond Dynamics of Formation ACS Nano 2014, 8, 5216-5226 10.1021/nn5012946
23. Angelov, B.; Angelova, A.; Filippov, S. K.; Narayanan, T.; Drechsler, M.; Štěpánek, P.; Couvreur, P.; Lesieur, S. DNA/Fusogenic Lipid Nanocarrier Assembly: Millisecond Structural Dynamics J. Phys. Chem. Lett. 2013, 4, 1959-1964 10.1021/jz400857z
24. Angelova, A.; Angelov, B.; Drechsler, M.; Garamus, V. M.; Lesieur, S. Protein Entrapment in PEGylated Lipid Nanoparticles Int. J. Pharm. 2013, 454, 625-632 10.1016/j.ijpharm.2013.06.006
25. Braun, V. P.; Stupp, I. S. CdS Mineralization of Hexagonal, Lamellar, and Cubic Lyotropic Liquid Crystals Mater. Res. Bull. 1999, 34, 463-469 10.1016/S0025-5408(99)00030-6
26. Wang, D.; Kou, R.; Choi, D.; Yang, Y.; Nie, Y.; Li, J.; Saraf, L. V.; Hu, D.; Zhang, J.; Graff, G. L.; Liu, J.; Pope, M. A.; Aksay, I. A. Ternary Self-assembly of Ordered Metal Oxide-Graphene Nanocomposites for Electrochemical Energy Storage ACS Nano 2010, 4, 1587-1595 10.1021/nn901819n
27. Cherezov, V.; Rosenbaum, D. M.; Hanson, M. A.; Rasmussen, S. G.; Thian, F. S.; Kobilka, T. S.; Choi, H. J.; Kuhn, P.; Weis, W. I.; Kobilka, B. K.; Stevens, R. C. High-Resolution Crystal Structure of an Engineered Human 2-Adrenergic G Protein-Coupled Receptor Science 2007, 318, 1258-1265 10.1126/science.1150577
28. Caffrey, M.; Cherezov, V. Crystallizing Membrane Proteins Using Lipidic Mesophases Nat. Protoc. 2009, 4, 706-731 10.1038/nprot.2009.31
29. Zabara, A.; Mezzenga, R. Plenty of Room to Crystallize: Swollen Lipidic Mesophases for Improved and Controlled In-Meso Protein Crystallization Soft Matter 2012, 8, 6535-6541 10.1039/c2sm25249j
30. Razumas, V.; Kanapieniené, J.; Nylander, T.; Engström, S.; Larsson, K. Electrochemical Biosensors for Glucose, Lactate, Urea and Creatinine Based on Enzymes Entrapped in a Cubic Liquid Crystalline Phase Anal. Chim. Acta 1994, 289, 155-162 10.1016/0003-2670(94)80098-7
31. Nylander, T.; Mattisson, C.; Razumas, V.; Miezis, Y.; Håkansson, B. A Study of Entrapped Enzyme Stability and Substrate Diffusion in a Monoglyceride-Based Cubic Liquid Crystalline Phase Colloids Surf., A 1996, 114, 311-320 10.1016/0927-7757(96)03563-7
32. Nazaruk, E.; Bilewicz, R. Catalytic Activity of Oxidases Hosted in Lipidic Cubic Phases on Electrodes Bioelectrochemistry 2007, 71, 8-14 10.1016/j.bioelechem.2006.12.007
33. Nazaruk, E.; Bilewicz, R.; Lindblom, G.; Lindholm-Sethson, B. Cubic Phases in Biosensing Systems Anal. Bioanal. Chem. 2008, 391, 1569-1578 10.1007/s00216-008-2149-y
34. Li, D.; Caffrey, M. Lipid Cubic Phase as a Membrane Mimetic for Integral Membrane Protein Enzymes Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 8639-8644 10.1073/pnas.1101815108
35. Nazaruk, E.; Landau, E. M.; Bilewicz, R. Membrane Bound Enzyme Hosted in Liquid Crystalline Cubic Phase for Sensing and Fuel Cells Electrochim. Acta 2014, 140, 96-100 10.1016/j.electacta.2014.05.130
36. Vallooran, J. J.; Handschin, S.; Pillai, S. M.; Vetter, B. N.; Rusch, S.; Beck, H.-P.; Mezzenga, R. Lipidic Cubic Phases as Versatile Platform for the Rapid Detection of Biomarkers, Viruses, Bacteria and Parasites Adv. Funct. Mater. 2016, 26, 181-190 10.1002/adfm.201503428
37. Barauskas, J.; Landh, T. Phase Behavior of the Phytantriol/Water System Langmuir 2003, 19, 9562-9565 10.1021/la0350812
38. Dong, Y.-D.; Larson, I.; Hanley, T.; Boyd, B. J. Bulk and Dispersed Aqueous Phase Behaviors of Phytantriol: Effect of Vitamin E Acetate and F127 Polymer on Liquid Crystal Nanostructure Langmuir 2006, 22, 9512-9518 10.1021/la061706v
39. Dong, Y.-D.; Dong, W. A.; Larson, I.; Rappolt, M.; Amenitsch, H.; Hanley, T.; Boyd, B. J. Impurities in Commercial Phytantriol Significantly Alter Its Lyotropic Liquid-Crystalline Phase Behavior Langmuir 2008, 24, 6998-7003 10.1021/la8005579
40. Kulkarni, C. V.; Wachter, W.; Iglesias-Salto, G.; Engelskirchen, S.; Ahualli, S. Monoolein: a Magic Lipid? Phys. Chem. Chem. Phys. 2011, 13, 3004-3021 10.1039/C0CP01539C
41. Qiu, H.; Caffrey, M. The Phase Diagram of the Monoolein/Water System: Metastability and Equilibrium Aspects Biomaterials 2000, 21, 223-234 10.1016/S0142-9612(99)00126-X
42. Mezzenga, R.; Meyer, C.; Servais, C.; Romoscanu, A.; Sagalowicz, L.; Hayward, R. Shear Rheology of Lyotropic Liquid Crystals: a Case Study Langmuir 2005, 21, 3322-3333 10.1021/la046964b
43. Yamada, Y.; Aida, K.; Uemura, T. Enzymatic Studies on the Oxidation of Sugar and Sugar Alcohol. I. Purification and Properties of Article-Bound Fructose Dehydrogenase J. Biochem. 1967, 61, 636-646
44. Ameyama, M.; Shinagawa, E.; Matsushita, K.; Adachi, O. D-Fructose Dehydrogenase of Gluconobacter Industrius: Purification, Characterization, and Application to Enzymatic Microdetermination of D-Fructose J. Bacteriol. 1981, 145, 814-23
45. Kato, K.; Walde, P.; Mitsui, H.; Higashi, N. Enzymatic and Stability of D-Fructose Dehydrogenase and Sarcosine Dehydrogenase Immobilized onto Giant Vesicles Biotechnol. Bioeng. 2003, 84, 415-423 10.1002/bit.10784
46. Minteer, S. D.; Liaw, B. Y.; Cooney, M. J. Enzyme-Based Biofuel Cells Curr. Opin. Biotechnol. 2007, 18, 228-234 10.1016/j.copbio.2007.03.007
47. Moehlenbrock, M. J.; Minteer, S. D. Extended Lifetime Biofuel Cells Chem. Soc. Rev. 2008, 37, 1188-1196 10.1039/b708013c
48. Kim, J.; Jia, H.; Wang, P. Challenges in Biocatalysis for Enzyme-Based Biofuel Cells Biotechnol. Adv. 2006, 24, 296-308 10.1016/j.biotechadv.2005.11.006
49. Turner, D. C.; Wang, Z. G.; Gruner, S. M.; Mannock, D. A.; McElhaney, R. N. Structural Study of the Inverted Cubic Phases of Di-Dodecyl Alkyl-Beta-D-Glucopyranosyl-Rac-Glycerol J. Phys. II 1992, 2, 2039-2063 10.1051/jp2:1992250
50. Briggs, J.; Chung, H.; Caffrey, M. The Temperature-Composition Phase Diagram and Mesophase Structure Characterization of the Monoolein/Water System J. Phys. II 1996, 6, 723-751 10.1051/jp2:1996208
51. Cheng, A.; Hummel, B.; Qiu, H.; Caffrey, M. A Simple Mechanical Mixer for Small Viscous Lipid-Containing Samples Chem. Phys. Lipids 1998, 95, 11-21 10.1016/S0009-3084(98)00060-7
52. Amine, A.; Moscone, D.; Bernardo, R. A.; Marconi, E.; Palleschi, G. A New Enzymatic Spectrophotometric Assay for the Determination of Lactulose in Milk Anal. Chim. Acta 2000, 406, 217-224 10.1016/S0003-2670(99)00765-5
53. Angelova, A.; Ollivon, M.; Campitelli, A.; Bourgaux, C. Lipid Cubic Phases as Stable Nanochannel Network Structures for Protein Biochip Development: X-ray Diffraction Study Langmuir 2003, 19, 6928-6935 10.1021/la0345284
54. Nazaruk, E.; Górecka, E.; Bilewicz, R. Enzymes and Mediators Hosted Together in Lipidic Mesophases for the Construction of Biodevices J. Colloid Interface Sci. 2012, 385, 130-136 10.1016/j.jcis.2012.06.087