Halloysite Clay Nanotubes for Enzyme Immobilization

Tully, Joshua; Yendluri, Raghuvara; Lvov, Yuri

doi:10.1021/acs.biomac.5b01542

Halloysite Clay Nanotubes for Enzyme Immobilization

Journal Article · Wed Dec 23 00:00:00 EST 2015 · Biomacromolecules

DOI:https://doi.org/10.1021/acs.biomac.5b01542· OSTI ID:1673765

Tully, Joshua ^[1]; Yendluri, Raghuvara ^[2]; Lvov, Yuri ^[3]

Louisiana Tech Univ., Ruston, LA (United States); Louisiana State University
Louisiana Tech Univ., Ruston, LA (United States)
Louisiana Tech Univ., Ruston, LA (United States); Ural Federal Univ., Ekaterinburg (Russia)

Halloysite clay is an aluminosilicate nanotube formed by rolling flat sheets of kaolinite clay. They have a 15 nm lumen, 50–70 nm external diameter, length of 0.5–1 μm, and different inside/outside chemistry. Due to these nanoscale properties, they are used for loading, storage, and controlled release of active chemical agents, including anticorrosions, biocides, and drugs. Here, we studied the immobilization in halloysite of laccase, glucose oxidase, and lipase. Overall, negatively charged proteins taken above their isoelectric points were mostly loaded into the positively charged tube’s lumen. Typical tube loading with proteins was 6–7 wt % from which one-third was released in 5–10 h and the other two-thirds remained, providing enhanced biocatalysis in nanoconfined conditions. Immobilized lipase showed enhanced stability at acidic pH, and the optimum pH shifted to more alkaline pH. Immobilized laccase was more stable with respect to time, and immobilized glucose oxidase showed retention of enzymatic activity up to 70 °C, whereas the native sample was inactive.

View Accepted Manuscript (DOE)

Research Organization:: Louisiana State Univ., Baton Rouge, LA (United States)

Sponsoring Organization:: Russian Science Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES); USEPA

Grant/Contract Number:: SC0012432

OSTI ID:: 1673765

Journal Information:: Biomacromolecules, Journal Name: Biomacromolecules Journal Issue: 2 Vol. 17; ISSN 1525-7797

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (30)

Protein adsorption to polymer particles: Role of surface properties Absolom, D. R.; Zingg, W.; Neumann, A. W. Journal of Biomedical Materials Research, Vol. 21, Issue 2 https://doi.org/10.1002/jbm.820210202	journal	February 1987
Halloysite Clay Nanotubes for Resveratrol Delivery to Cancer Cells: Halloysite Clay Nanotubes for Resveratrol Delivery to Cancer Cells Vergaro, Viviana; Lvov, Yuri M.; Leporatti, Stefano Macromolecular Bioscience, Vol. 12, Issue 9 https://doi.org/10.1002/mabi.201200121	journal	August 2012
Newly emerging applications of halloysite nanotubes: a review: Applications of halloysite nanotubes Du, Mingliang; Guo, Baochun; Jia, Demin Polymer International, Vol. 59, Issue 5 https://doi.org/10.1002/pi.2754	journal	January 2010
Halloysite Nanotubes as Biomimetic Nanoreactors Shchukin, Dmitry?G.; Sukhorukov, Gleb?B.; Price, Ronald?R. Small, Vol. 1, Issue 5 https://doi.org/10.1002/smll.200400120	journal	May 2005
A Stable Nonfluorescent Derivative of Resorufin for the Fluorometric Determination of Trace Hydrogen Peroxide: Applications in Detecting the Activity of Phagocyte NADPH Oxidase and Other Oxidases Zhou, Mingjie; Diwu, Zhenjun; Panchuk-Voloshina, Nataliya Analytical Biochemistry, Vol. 253, Issue 2 https://doi.org/10.1006/abio.1997.2391	journal	November 1997
Size and Shape of Protein Molecules at the Nanometer Level Determined by Sedimentation, Gel Filtration, and Electron Microscopy Erickson, Harold P. Biological Procedures Online, Vol. 11, Issue 1 https://doi.org/10.1007/s12575-009-9008-x	journal	May 2009
Comparative protein adsorption in model systems Shirahama, Hiroyuki; Lyklema, Johannes; Norde, Willem Journal of Colloid and Interface Science, Vol. 139, Issue 1 https://doi.org/10.1016/0021-9797(90)90455-W	journal	October 1990
Simplified para-nitrophenyl palmitate assay for lipases and esterases Gupta, Namita; Rathi, Pooja; Gupta, Rani Analytical Biochemistry, Vol. 311, Issue 1 https://doi.org/10.1016/S0003-2697(02)00379-2	journal	December 2002
Use of coated microtubular halloysite for the sustained release of diltiazem hydrochloride and propranolol hydrochloride Levis, S. R.; Deasy, P. B. International Journal of Pharmaceutics, Vol. 253, Issue 1-2 https://doi.org/10.1016/S0378-5173(02)00702-0	journal	March 2003
Interfacial adsorption of lipases on very hydrophobic support (octadecyl–Sepabeads): immobilization, hyperactivation and stabilization of the open form of lipases Palomo, José M.; Muñoz, Gloria; Fernández-Lorente, Gloria Journal of Molecular Catalysis B: Enzymatic, Vol. 19-20 https://doi.org/10.1016/S1381-1177(02)00178-9	journal	December 2002
Immobilization of enzyme biocatalyst on natural halloysite nanotubes Zhai, Rui; Zhang, Bing; Liu, Lin Catalysis Communications, Vol. 12, Issue 4 https://doi.org/10.1016/j.catcom.2010.09.030	journal	December 2010
Biodiesel production from waste oils by using lipase immobilized on hydrotalcite and zeolites Yagiz, Funda; Kazan, Dilek; Akin, A. Nilgun Chemical Engineering Journal, Vol. 134, Issue 1-3 https://doi.org/10.1016/j.cej.2007.03.041	journal	November 2007
Chitosan–halloysite hybrid-nanotubes: Horseradish peroxidase immobilization and applications in phenol removal Zhai, Rui; Zhang, Bing; Wan, Yazhen Chemical Engineering Journal, Vol. 214 https://doi.org/10.1016/j.cej.2012.10.073	journal	January 2013
Clay nanotube encapsulation for functional biocomposites Lvov, Yuri; Aerov, Artem; Fakhrullin, Rawil Advances in Colloid and Interface Science, Vol. 207 https://doi.org/10.1016/j.cis.2013.10.006	journal	May 2014
Zeolite inorganic supports for BSA immobilization: Comparative study of several zeolite crystals and composite membranes Tavolaro, Adalgisa; Tavolaro, Palmira; Drioli, Enrico Colloids and Surfaces B: Biointerfaces, Vol. 55, Issue 1 https://doi.org/10.1016/j.colsurfb.2006.11.010	journal	March 2007
Enhanced pH and thermal stabilities of invertase immobilized on montmorillonite K-10 Sanjay, G.; Sugunan, S. Food Chemistry, Vol. 94, Issue 4 https://doi.org/10.1016/j.foodchem.2004.12.043	journal	March 2006
Sorption and immobilization of cellulase on silicate clay minerals Safari Sinegani, Ali Akbar; Emtiazi, Giti; Shariatmadari, Hossain Journal of Colloid and Interface Science, Vol. 290, Issue 1 https://doi.org/10.1016/j.jcis.2005.04.030	journal	October 2005
Selective fabrication of iron oxide particles in halloysite lumen Zheng, Pengwu; Du, Yuanyuan; Ma, Xiaofei Materials Chemistry and Physics, Vol. 151 https://doi.org/10.1016/j.matchemphys.2014.11.075	journal	February 2015
Functional polymer–clay nanotube composites with sustained release of chemical agents Lvov, Yuri; Abdullayev, Elshad Progress in Polymer Science, Vol. 38, Issue 10-11 https://doi.org/10.1016/j.progpolymsci.2013.05.009	journal	October 2013
Recent advance in research on halloysite nanotubes-polymer nanocomposite Liu, Mingxian; Jia, Zhixin; Jia, Demin Progress in Polymer Science, Vol. 39, Issue 8 https://doi.org/10.1016/j.progpolymsci.2014.04.004	journal	August 2014
Hydrophobically Modified Halloysite Nanotubes as Reverse Micelles for Water-in-Oil Emulsion Cavallaro, Giuseppe; Lazzara, Giuseppe; Milioto, Stefana Langmuir, Vol. 31, Issue 27 https://doi.org/10.1021/acs.langmuir.5b01181	journal	July 2015
Facile Fabrication of Flowerlike Natural Nanotube/Layered Double Hydroxide Composites as Effective Carrier for Lysozyme Immobilization Wang, Yuanming; Liu, Chuochuo; Zhang, Yatao ACS Sustainable Chemistry & Engineering, Vol. 3, Issue 6 https://doi.org/10.1021/acssuschemeng.5b00104	journal	May 2015
Surface Modification of Halloysite Nanotubes with Dopamine for Enzyme Immobilization Chao, Cong; Liu, Jindun; Wang, Jingtao ACS Applied Materials & Interfaces, Vol. 5, Issue 21 https://doi.org/10.1021/am4022973	journal	October 2013
Adsorption of Proteins to Hydrophobic Sites on Mixed Self-Assembled Monolayers ^† Ostuni, Emanuele; Grzybowski, Bartosz A.; Mrksich, Milan Langmuir, Vol. 19, Issue 5 https://doi.org/10.1021/la020649c	journal	March 2003
Protein Adsorption onto Silica Nanoparticles: Conformational Changes Depend on the Particles' Curvature and the Protein Stability Lundqvist, Martin; Sethson, Ingmar; Jonsson, Bengt-Harald Langmuir, Vol. 20, Issue 24 https://doi.org/10.1021/la0484725	journal	November 2004
Cross-Linked Enzyme Aggregates: A Simple and Effective Method for the Immobilization of Penicillin Acylase Cao, Linqiu; van Rantwijk, Fred; Sheldon, Roger A. Organic Letters, Vol. 2, Issue 10 https://doi.org/10.1021/ol005593x	journal	May 2000
Natural Nanotube-Based Biomimetic Porous Microspheres for Significantly Enhanced Biomolecule Immobilization Chao, Cong; Zhang, Bing; Zhai, Rui ACS Sustainable Chemistry & Engineering, Vol. 2, Issue 3 https://doi.org/10.1021/sc400199v	journal	August 2013
A relationship between protein stability and protein function. Shoichet, B. K.; Baase, W. A.; Kuroki, R. Proceedings of the National Academy of Sciences, Vol. 92, Issue 2 https://doi.org/10.1073/pnas.92.2.452	journal	January 1995
UniProt: a hub for protein information Consortium, UniPot Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212 https://doi.org/10.1093/nar/gku989	journal	October 2014
Halloysite clay minerals — a review Joussein, E.; Petit, S.; Churchman, J. Clay Minerals, Vol. 40, Issue 4 https://doi.org/10.1180/0009855054040180	journal	December 2005

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