Orientating lipase molecules through surface chemical control for enhanced activity: A QCM-D and ToF-SIMS investigation

Colloids and Surfaces B: Biointerfaces

Volumn 142, Issue , 2016, Pages 173-181

  Joyce, Paul ^a   Kempson, Ivan ^a   Prestidge, Clive A ^a  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Lipase; Lipid digestion; Porous silica; QCM D; Surface chemistry; ToF SIMS

Indexed keywords

ADSORPTION; AMINO ACIDS; DRUG PRODUCTS; HYDROPHILICITY; HYDROPHOBICITY; KINETICS; LIPASES; MASS SPECTROMETRY; MOLECULAR ORIENTATION; MULTIVARIANT ANALYSIS; ORGANIC POLYMERS; QUARTZ CRYSTAL MICROBALANCES; RATE CONSTANTS; SECONDARY ION MASS SPECTROMETRY; SURFACE CHEMISTRY;

CANDIDA ANTARTICA LIPASE; LIPID DIGESTIONS; MULTIVARIATE STATISTICS; POROUS SILICA; PSEUDO FIRST ORDER RATE CONSTANTS; QUARTZ CRYSTAL MICROBALANCE WITH DISSIPATION; TIME OF FLIGHT SECONDARY ION MASS SPECTROMETRY; TOF SIMS;

SILICA;

ACID LIPASE; HISTIDINE DERIVATIVE; LIPID; SILICON DIOXIDE; TRIACYLGLYCEROL LIPASE; FUNGAL PROTEIN; HISTIDINE; TRIACYLGLYCEROL;

ADSORPTION KINETICS; ARTICLE; CANDIDA; CANDIDA ANTARTICA; CHEMICAL BINDING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; HYDROPHILICITY; HYDROPHOBICITY; LIPID METABOLISM; NONHUMAN; POROSITY; QUARTZ CRYSTAL MICROBALANCE; RATE CONSTANT; SECONDARY ION MASS SPECTROMETRY; SURFACE PROPERTY; TIME OF FLIGHT MASS SPECTROMETRY; ADSORPTION; CHEMICAL PHENOMENA; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; ENZYMOLOGY; HYDROLYSIS; ISOLATION AND PURIFICATION; KINETICS; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY;

ADSORPTION; CANDIDA; CATALYTIC DOMAIN; DRUG COMPOUNDING; DRUG DELIVERY SYSTEMS; FUNGAL PROTEINS; HISTIDINE; HYDROLYSIS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; LIPASE; POROSITY; QUARTZ CRYSTAL MICROBALANCE TECHNIQUES; SILICON DIOXIDE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SURFACE PROPERTIES; TRIGLYCERIDES;

EID: 85009454621     PISSN: 09277765     EISSN: 18734367     Source Type: Journal    
DOI: 10.1016/j.colsurfb.2016.02.059     Document Type: Article

References (60)

1. [1] Moelans, D., Cool, P., Baeyens, J., Vansant, E.F., Using mesoporous silica materials to immobilise biocatalysis-enzymes. Catal. Commun. 6 (2005), 307–311.
2. [2] Chapus, C., Semeriva, M., Bovier-Lapierre, C., Desnuelle, P., Mechanism of pancreatic lipase action. 1. Interfacial activation of pancreatic lipase. Biochemistry 15 (1976), 4980–4987.
3. [3] Martinelle, M., Holmquist, M., Hult, K., On the interfacial activation of Candida antarctica lipase A and B as compared with Humicola lanuginosa lipase. Biochim. Biophys. Acta 1258 (1995), 272–276.
4. [4] Stergiou, P.-Y., Foukis, A., Filippou, M., Koukouritaki, M., Parapouli, M., Theodorou, L.G., Hatziloukas, E., Afendra, A., Pandey, A., Papamichael, E.M., Advances in lipase-catalyzed esterification reactions. Biotechnol. Adv. 31 (2013), 1846–1859.
5. [5] Vorderwülbecke, T., Kieslich, K., Erdmann, H., Comparison of lipases by different assays. Enzyme Microb. Technol. 14 (1992), 631–639.
6. [6] Reis, P., Holmberg, K., Watzke, H., Leser, M.E., Miller, R., Lipases at interfaces: a review. Adv. Colloid Interface Sci. 147–148 (2009), 237–250.
7. [7] Serra, E., Mayoral, Á., Sakamoto, Y., Blanco, R.M., Díaz, I., Stockholms, u., Immobilization of lipase in ordered mesoporous materials: effect of textural and structural parameters. Microporous Mesoporous Mater. 114 (2008), 201–213.
8. [8] Blanco, R.M., Terreros, P., Fernández-Pérez, M., Otero, C., Dı́az-González, G., Functionalization of mesoporous silica for lipase immobilization: characterization of the support and the catalysts. J. Mol. Catal. B: Enzym. 30 (2004), 83–93.
9. [9] Nikolic, M., Srdic, V., Antov, M., Immobilization of lipase into mesoporous silica particles by physical adsorption. Biocatal. Biotransform. 27 (2009), 254–262.
10. [10] Zhou, Z., Inayat, A., Schwieger, W., Hartmann, M., Improved activity and stability of lipase immobilized in cage-like large pore mesoporous organosilicas. Microporous. Mesoporous. Mat. 154 (2012), 133–141.
11. [11] Joyce, P., Tan, A., Whitby, C.P., Prestidge, C.A., The role of porous nanostructure in controlling lipase-mediated digestion of lipid loaded into silica particles. Langmuir 30 (2014), 2779–2788.
12. [12] Tan, A., Colliat-Dangus, P., Whitby, C.P., Prestidge, C.A., Controlling the enzymatic digestion of lipids using hybrid nanostructured materials. ACS Appl. Mater. Interfaces 6 (2014), 15363–15371.
13. [13] Joyce, P., Kempson, I., Prestidge, C.A., QCM-D and ToF-SIMS investigation to deconvolute the relationship between lipid adsorption and orientation on lipase activity. Langmuir 31 (2015), 10198–10207.
14. [14] Kang, Y., He, J., Guo, X.D., Guo, X., Song, Z.H., Influence of pore diameters on the immobilization of lipase in SBA-15. Ind. Eng. Chem. Res. 46 (2007), 4474–4479.
15. [15] Reis, P., Holmberg, K., Debeche, T., Folmer, B., Fauconnot, L., Watzke, H., Lipase-catalyzed reactions at different surfaces. Langmuir 22 (2006), 8169–8177.
16. [16] Palomo, J.M., Muñoz, G., Fernández-Lorente, G., Mateo, C., Fernández-Lafuente, R., Guisán, J.M., Interfacial adsorption of lipases on very hydrophobic support (octadecyl–sepabeads): immobilization, hyperactivation and stabilization of the open form of lipases. J. Mol. Catal. B Enzym. 19 (2002), 279–286.
17. [17] Tan, A., Simovic, S., Davey, A.K., Rades, T., Boyd, B.J., Prestidge, C.A., Silica nanoparticles to control the lipase-mediated digestion of lipid-based oral delivery systems. Mol. Pharm. 7 (2010), 522–532.
18. [18] Serra, E., Díez, E., Díaz, I., Blanco, R.M., A comparative study of periodic mesoporous organosilica and different hydrophobic mesoporous silicas for lipase immobilization. Microporous Mesoporous Mater. 132 (2010), 487–493.
19. [19] Wannerberger, K., Welin-Klintström, S., Arnebrant, T., Activity and adsorption of lipase from Humicola lanuginosa on surfaces with different wettabilities. Langmuir 13 (1997), 784–790.
20. [20] Sonesson, A.W., Callisen, T.H., Brismar, H., Elofsson, U.M., Adsorption and activity of Thermomyces lanuginosus lipase on hydrophobic and hydrophilic surfaces measured with dual polarization interferometry (DPI) and confocal microscopy. Colloids Surf. B 61 (2008), 208–215.
21. [21] Elwing, H., Welin, S., Askendal, A., Nilsson, U., LundstrÖm, I., A wettability gradient method for studies of macromolecular interactions at the liquid/solid interface. J. Colloid Interface Sci. 119 (1987), 203–210.
22. [22] Gölander, C.-G., Pitt, W.G., Characterization of hydrophobicity gradients prepared by means of Radio frequency plasma discharge. Biomaterials 11 (1990), 32–35.
23. [23] Joyce, P., Whitby, C.P., Prestidge, C.A., Bioactive hybrid particles from poly(D,L-lactide-co-glycolide) nanoparticle stabilized lipid droplets. ACS Appl. Mater. Interfaces 7 (2015), 17460–17470.
24. [24] Sonesson, A., Brismar, H., Callisen, T.H., Elofsson, U., Mobility of Thermomyces lanuginosus lipase on a trimyristin substrate surface. Langmuir 23 (2007), 2706–2713.
25. [25] Sonesson, A., Callisen, T.H., Brismar, H., Elofsson, U., Lipase surface diffusion studied by fluorescence recovery after photobleaching. Langmuir 21 (2005), 11949–11956.
26. [26] Sonesson, A., Elofsson, U., Brismar, H., Callisen, T.H., Adsorption and mobility of a lipase at a hydrophobic surface in the presence of surfactants. Langmuir 22 (2006), 5810–5817.
27. [27] Kempson, I., Barnes, T., Prestidge, C., Use of TOF-SIMS to study adsorption and loading behavior of methylene blue and papain in a nano-porous silicon layer. J. Am. Soc. Mass Spectrom. 21 (2010), 254–260.
28. [28] Kempson, I.M., Chang, P., Bremmell, K., Prestidge, C.A., Low temperature thermal dependent Filgrastim adsorption behavior detected with ToF-SIMS. Langmuir, 29, 2013, 15573.
29. [29] Kempson, I.M., Martin, A.L., Denman, J.A., French, P.W., Prestidge, C.A., Barnes, T.J., Detecting the presence of denatured human serum albumin in an adsorbed protein monolayer using TOF-SIMS. Langmuir, 26, 2010, 12075.
30. [30] Tan, A., Martin, A., Nguyen, T.-H., Boyd, B.J., Prestidge, C.A., Hybrid nanomaterials that mimic the food effect: controlling enzymatic digestion for enhanced oral drug absorption. Angew. Chem. Int. Ed. 51 (2012), 5475–5479.
31. [31] Tan, A., Simovic, S., Davey, A.K., Rades, T., Prestidge, C.A., Silica-lipid hybrid (SLH) microcapsules: a novel oral delivery system for poorly soluble drugs. J. Controlled Release 134 (2009), 62–70.
32. [32] Yasmin, R., Tan, A., Bremmell, K.E., Prestidge, C.A., Lyophilized silica lipid hybrid (SLH) carriers for poorly Water‐Soluble drugs: physicochemical and In vitro pharmaceutical investigations. J. Pharm. Sci. 103 (2014), 2950–2959.
33. [33] Bhatt, A., Barnes, T.J., Prestidge, C.A., Silica nanoparticle stabilization of liquid crystalline lipid dispersions: impact on enzymatic digestion and drug solubilization. Curr. Drug Deliv. 12 (2015), 47–55.
34. [34] Laszlo, J.A., Evans, K.O., Influence of cosolvents on the hydrophobic surface immobilization topography of Candida antarctica lipase B. J. Mol. Catal. B Enzym. 58 (2009), 169–174.
35. [35] Rodahl, M., Hook, F., Krozer, A., Brzezinski, P., Kaesmo, B., Quartz crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments. Rev. Sci. Instrum. 66 (1995), 3924–3930.
36. [36] Sauerbrey, G., Verwendung von schwingquarzen zur Wägung dünner schichten und zur mikrowägung. Z. Phys. 155 (1959), 206–222.
37. [37] Smith, E.A., Thomas, W.D., Kiessling, L.L., Corn, R.M., Surface plasmon resonance imaging studies of protein-carbohydrate interactions. J. Amer. Chem. Soc., 125, 2003, 6140.
38. [38] Langmuir, I., An extension of the phase rule for adsorption under equilibrium and non‐equilibrium conditions. J. Chem. Phys., 1, 1933, 3.
39. [39] Tanaka, M., Mochizuki, A., Shiroya, T., Motomura, T., Shimura, K., Onishi, M., Okahata, Y., Study on kinetics of early stage protein adsorption on poly(2-methoxyethylacrylate) (PMEA) surface. Coll. Surf. A 203 (2002), 195–204.
40. [40] Hayashi, T., Tanaka, Y., Koide, Y., Tanaka, M., Hara, M., Mechanism underlying bioinertness of self-assembled monolayers of oligo(ethyleneglycol)-terminated alkanethiols on gold: protein adsorption, platelet adhesion, and surface forces. Phys. Chem. Chem. Phys. 14 (2012), 10196–10206.
41. [41] Hirata, T., Matsuno, H., Tanaka, M., Tanaka, K., Surface segregation of poly(2-methoxyethyl acrylate) in a mixture with poly(methyl methacrylate). Phys. Chem. Chem. Phys. 13 (2011), 4928–4934.
42. [42] Morita, S., Tanaka, M., Effect of sodium chloride on hydration structures of PMEA and P(MPC-r-BMA). Langmuir, 30, 2014, 10698.
43. [43] Roach, P., Farrar, D., Perry, C.C., Interpretation of protein adsorption: surface-induced conformational changes. J. Amer. Chem. Soc. 127 (2005), 8168–8173.
44. [44] Helm, C.A., Israelachvili, J.N., McGuiggan, P.M., Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers. Science, 246, 1989, 919 (New York, N.Y.).
45. [45] Kapsabelis, S., Prestidge, C.A., Adsorption of ethyl(hydroxyethyl) cellulose onto silica particles: the role of surface chemistry and temperature. J. Colloid Interface Sci. 228 (2000), 297–305.
46. [46] Ericsson, D.J., Kasrayan, A., Johansson, P., Bergfors, T., Sandström, A.G., Bäckvall, J.-E., Mowbray, S.L., X-ray structure of Candida antarctica lipase a shows a novel lid structure and a likely mode of interfacial activation. J. Mol. Biol. 376 (2008), 109–119.
47. [47] Ghabbour, E.A., Davies, G., Environmental insights from Langmuir adsorption site capacities. Coll. Surf. A 381 (2011), 37–40.
48. [48] Reis, P., Holmberg, K., Miller, R., Leser, M.E., Raab, T., Watzke, H.J., Lipase reaction at interfaces as self-limiting processes, 12, 2009, 8.
49. [49] Israelachvili, J.N., Pashley, R.M., Measurement of the hydrophobic interaction between two hydrophobic surfaces in aqueous electrolyte solutions. J. Colloid Interface Sci. 98 (1984), 500–514.
50. [50] Awsiuk, K., Budkowski, A., Psarouli, A., Petrou, P., Bernasik, A., Kakabakos, S., Rysz, J., Raptis, I., Protein adsorption and covalent bonding to silicon nitride surfaces modified with organo-silanes: comparison using AFM, angle-resolved XPS and multivariate ToF-SIMS analysis. Colloids Surf. B 110 (2013), 217–224.
51. [51] Hook, A.L., Williams, P.M., Alexander, M.R., Scurr, D.J., Multivariate ToF-SIMS image analysis of polymer microarrays and protein adsorption. Biointerphases, 10, 2015, 019005.
52. [52] Killian, M.S., Krebs, H.M., Schmuki, P., Protein denaturation detected by time-of-flight secondary ion mass spectrometry. Langmuir, 27, 2011, 7510.
53. [53] E.I. AG, Aerosil, 2013.
54. [54] Verger, R., ‘Interfacial activation’ of lipases: facts and artifacts. Trends Biotechnol. 15 (1997), 32–38.
55. [55] Armand, M., Borel, P., Ythier, P., Dutot, G., Melin, C., Senft, M., Effects of droplet size, triacylglycerol composition, and calcium on the hydrolysis of complex emulsions by pancreatic lipase: an in vitro study. J. Nutr. Biochem. 3 (1992), 333–341.
56. [56] Malacata, F.X., Hill, C.G., Amundson, C.H., Use of a lipase immobilized in a membrane reactor to hydrolyze the glycerides of butteroil. Biotechnol. Bioeng. 38 (1991), 853–868.
57. [57] Wannerberger, K., Arnebrant, T., Adsorption of lipase to silica and methylated silica surfaces. J. Colloid Interface Sci. 177 (1996), 316–324.
58. [58] Simovic, S., Heard, P., Prestidge, C.A., Hybrid lipid-silica microcapsules engineered by phase coacervation of Pickering emulsions to enhance lipid hydrolysis. Phys. Chem. Chem. Phys. 12 (2010), 7162–7170.
59. [59] Simovic, S., Heard, P., Hui, H., Song, Y., Peddie, F., Davey, A.K., Lewis, A., Rades, T., Prestidge, C.A., Dry hybrid lipid-silica microcapsules engineered from submicron lipid droplets and nanoparticles as a novel delivery system for poorly soluble drugs. Mol. Pharm. 6 (2009), 861–872.
60. [60] Tan, A., Eskandar, N.G., Rao, S., Prestidge, C.A., First in man bioavailability and tolerability studies of a silica-lipid hybrid (Lipoceramic) formulation: a Phase I study with ibuprofen. Drug Deli. Transl. Res., 4, 2014, 212.