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Title: Developing Enzyme Immobilization with Fibrous Membranes: Longevity and Characterization Considerations

Abstract

Fibrous membranes offer broad opportunities to deploy immobilized enzymes in new reactor and application designs, including multiphase continuous flow-through reactions. Enzyme immobilization is a technology strategy that simplifies the separation of otherwise soluble catalytic proteins from liquid reaction media and imparts stabilization and performance enhancement. Flexible immobilization matrices made from fibers have versatile physical attributes, such as high surface area, light weight, and controllable porosity, which give them membrane-like characteristics, while simultaneously providing good mechanical properties for creating functional filters, sensors, scaffolds, and other interface-active biocatalytic materials. This review examines immobilization strategies for enzymes on fibrous membrane-like polymeric supports involving all three fundamental mechanisms of post-immobilization, incorporation, and coating. Post-immobilization offers an infinite selection of matrix materials, but may encounter loading and durability issues, while incorporation offers longevity but has more limited material options and may present mass transfer obstacles. Coating techniques on fibrous materials at different geometric scales are a growing trend in making membranes that integrate biocatalytic functionality with versatile physical supports. Biocatalytic performance parameters and characterization techniques for immobilized enzymes are described, including several emerging techniques of special relevance for fibrous immobilized enzymes. Diverse application examples from the literature, focusing on fibrous matrices, are summarized, and biocatalystmore » longevity is emphasized as a critical performance parameter that needs increased attention to advance concepts from lab scale to broader utilization. This consolidation of fabrication, performance measurement, and characterization techniques, with guiding examples highlighted, is intended to inspire future innovations in enzyme immobilization with fibrous membranes and expand their uses in novel reactors and processes.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]
+ Show Author Affiliations
  1. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences (CNMS); North Carolina State University, Raleigh, NC (United States)
  2. North Carolina State University, Raleigh, NC (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1987792
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Membranes
Additional Journal Information:
Journal Volume: 13; Journal Issue: 5; Journal ID: ISSN 2077-0375
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; enzyme; immobilization; biocatalyst; longevity; performance

Citation Formats

Yuan, Yue, Shen, Jialong, and Salmon, Sonja. Developing Enzyme Immobilization with Fibrous Membranes: Longevity and Characterization Considerations. United States: N. p., 2023. Web. doi:10.3390/membranes13050532.
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Yuan, Yue, Shen, Jialong, & Salmon, Sonja. Developing Enzyme Immobilization with Fibrous Membranes: Longevity and Characterization Considerations. United States. https://doi.org/10.3390/membranes13050532
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Yuan, Yue, Shen, Jialong, and Salmon, Sonja. Sat . "Developing Enzyme Immobilization with Fibrous Membranes: Longevity and Characterization Considerations". United States. https://doi.org/10.3390/membranes13050532. https://www.osti.gov/servlets/purl/1987792.
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@article{osti_1987792,
title = {Developing Enzyme Immobilization with Fibrous Membranes: Longevity and Characterization Considerations},
author = {Yuan, Yue and Shen, Jialong and Salmon, Sonja},
abstractNote = {Fibrous membranes offer broad opportunities to deploy immobilized enzymes in new reactor and application designs, including multiphase continuous flow-through reactions. Enzyme immobilization is a technology strategy that simplifies the separation of otherwise soluble catalytic proteins from liquid reaction media and imparts stabilization and performance enhancement. Flexible immobilization matrices made from fibers have versatile physical attributes, such as high surface area, light weight, and controllable porosity, which give them membrane-like characteristics, while simultaneously providing good mechanical properties for creating functional filters, sensors, scaffolds, and other interface-active biocatalytic materials. This review examines immobilization strategies for enzymes on fibrous membrane-like polymeric supports involving all three fundamental mechanisms of post-immobilization, incorporation, and coating. Post-immobilization offers an infinite selection of matrix materials, but may encounter loading and durability issues, while incorporation offers longevity but has more limited material options and may present mass transfer obstacles. Coating techniques on fibrous materials at different geometric scales are a growing trend in making membranes that integrate biocatalytic functionality with versatile physical supports. Biocatalytic performance parameters and characterization techniques for immobilized enzymes are described, including several emerging techniques of special relevance for fibrous immobilized enzymes. Diverse application examples from the literature, focusing on fibrous matrices, are summarized, and biocatalyst longevity is emphasized as a critical performance parameter that needs increased attention to advance concepts from lab scale to broader utilization. This consolidation of fabrication, performance measurement, and characterization techniques, with guiding examples highlighted, is intended to inspire future innovations in enzyme immobilization with fibrous membranes and expand their uses in novel reactors and processes.},
doi = {10.3390/membranes13050532},
journal = {Membranes},
number = 5,
volume = 13,
place = {United States},
year = {Sat May 20 00:00:00 EDT 2023},
month = {Sat May 20 00:00:00 EDT 2023}
}
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journal, September 2017

Structured fiber supports for gas phase biocatalysis
journal, May 2005

Reusable optical multi-plate sensing system for pesticide detection by using electrospun membranes as smart support for acetylcholinesterase immobilisation
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  • Cacciotti, Ilaria; Pallotto, Francesca; Scognamiglio, Viviana
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Ionic Liquid-Reconstituted Cellulose Composites as Solid Support Matrices for Biocatalyst Immobilization
journal, September 2005

  • Turner, Megan B.; Spear, Scott K.; Holbrey, John D.
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What Macromolecular Crowding Can Do to a Protein
journal, December 2014

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Characterization of Sol−Gel-Encapsulated Proteins Using Small-Angle Neutron Scattering
journal, September 2009

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Directed immobilization of CGTase: The effect of the enzyme orientation on the enzyme activity and its use in packed-bed reactor for continuous production of cyclodextrins
journal, July 2017

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Immobilization of glucose oxidase on nonwoven fabrics with bombyx mori silk fibroin gel
journal, September 1992

  • Asakura, Tetsuo; Kitaguchi, Motohiro; Demura, Makoto
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Immobilization of Candida rugosa lipase on chitosan with activation of the hydroxyl groups
journal, January 2004

Urease immobilization on an ion-exchange textile for urea hydrolysis
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  • Yeon, Kyeong-Ho; Lueptow, Richard M.
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Chitosan coated cotton cloth supported zero-valent nanoparticles: Simple but economically viable, efficient and easily retrievable catalysts
journal, December 2017

Carbonic Anhydrases in Industrial Applications
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The response surface methodology for optimization of tyrosinase immobilization onto electrospun polycaprolactone–chitosan fibers for use in bisphenol A removal
journal, December 2020

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Improving Biocatalytic Activity of Enzyme-Loaded Nanofibers by Dispersing Entangled Nanofiber Structure
journal, February 2007

  • Nair, Sujith; Kim, Jungbae; Crawford, Brad
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Advances in 3D Gel Printing for Enzyme Immobilization
journal, July 2022

In situ layer-by-layer assembled carbonic anhydrase-coated hollow fiber membrane contactor for rapid CO2 absorption
journal, September 2016

Production of l-DOPA from tyrosinase immobilized on nylon 6,6: enzyme stability and scaleup
journal, March 1998

Immobilization of lysozyme-CLEA onto electrospun chitosan nanofiber for effective antibacterial applications
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Immobilization–Stabilization of Proteins on Nanofibrillated Cellulose Derivatives and Their Bioactive Film Formation
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Bioimprinted lipases in PVA nanofibers as efficient immobilized biocatalysts
journal, November 2016

Enzyme immobilization on cellulose matrixes
journal, July 2016

  • Liu, Yue; Chen, Jonathan Y.
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Immobilization of horseradish peroxidase on electrospun magnetic nanofibers for phenol removal
journal, April 2019

Immobilization of Carbonic Anhydrase in Glass Micropipettes and Glass Fiber Filters for Flow-Through Reactor Applications
journal, August 2018

Simultaneous Heat and Mass Transfer and Chemical Reaction
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Development of an enzyme-immobilized support using a polyester woven fabric
journal, July 2016

Mammalian catalase: a venerable enzyme with new mysteries
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Immobilized enzymes: understanding enzyme – surface interactions at the molecular level
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Decolorization and Detoxification of Textile Dyes with a Laccase from Trametes hirsuta
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Defying the activity–stability trade-off in enzymes: taking advantage of entropy to enhance activity and thermostability
journal, March 2016

Intraparticle Kinetics Unveil Crowding and Enzyme Distribution Effects on the Performance of Cofactor-Dependent Heterogeneous Biocatalysts
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Immobilization of catalase on chitosan film
journal, April 2000

Analysis of contact area between water and irregular fibrous surface for prediction of wettability
journal, January 2016

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Nanodevices for the immobilization of therapeutic enzymes
journal, February 2015

Electrochemistry and electrocatalysis with heme proteins in chitosan biopolymer films
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Biocatalytic Janus membranes for CO 2 removal utilizing carbonic anhydrase
journal, January 2015

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Industrial applications of immobilized nano-biocatalysts
journal, October 2021

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Lipase immobilization on glutaraldehyde-activated nanofibrous membranes for improved enzyme stabilities and activities
journal, November 2012

Enzymatic properties of immobilized carbonic anhydrase and the biocatalyst for promoting CO 2 capture in vertical reactor
journal, June 2016

Enzyme immobilization to ultra-fine cellulose fibers via amphiphilic polyethylene glycol spacers
journal, January 2004

  • Wang, Yuhong; Hsieh, You-Lo
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Interior and surface of monomeric proteins
journal, August 1987

Cooperativity of covalent attachment and ion exchange on alcalase immobilization using glutaraldehyde chemistry: Enzyme stabilization and improved proteolytic activity
journal, December 2018

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Modulating the Activity of Protein Conjugated to Gold Nanoparticles by Site-Directed Orientation and Surface Density of Bound Protein
journal, February 2015

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  • ACS Applied Materials & Interfaces, Vol. 7, Issue 6
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Fabrication of cellulase protein fibers through concentric electrospinning
journal, October 2011

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Areas, Volumes, Packing, and Protein Structure
journal, June 1977

Enhanced bio-catalytic performance and dye degradation potential of chitosan-encapsulated horseradish peroxidase in a packed bed reactor system
journal, January 2017

Immobilized enzymes bioreactors utilizing a magnetic field: A review
journal, May 2017

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Cross-linked enzyme aggregates (CLEA®s): stable and recyclable biocatalysts
journal, November 2007

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Soft-Etch Mesoporous Hole-Conducting Block Copolymer Templates
journal, January 2010

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Immobilization of carbonic anhydrase in alginate and its influence on transformation of CO2 to calcite
journal, April 2012

Facile fabrication of lipase to amine functionalized gold nanoparticles to enhance stability and activity
journal, January 2017

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Wood mimetic hydrogel beads for enzyme immobilization
journal, January 2015

Long period fiber grating based sensor for the detection of triacylglycerides
journal, May 2016

Carbonic anhydrase immobilized on hollow fiber membranes using glutaraldehyde activated chitosan for artificial lung applications
journal, July 2013

  • Kimmel, J. D.; Arazawa, D. T.; Ye, S. -H.
  • Journal of Materials Science: Materials in Medicine, Vol. 24, Issue 11
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Hollow Fiber Membrane Contactors for Post-Combustion Carbon Capture: A Review of Modeling Approaches
journal, November 2020

Thiol-based, site-specific and covalent immobilization of biomolecules for single-molecule experiments
journal, May 2010

  • Zimmermann, Julia L.; Nicolaus, Thomas; Neuert, Gregor
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Immobilized glucose isomerase for the continuous conversion of glucose to fructose
journal, May 1975

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Conjugation and Modeled Structure/Function Analysis of Lysozyme on Glycine Esterified Cotton Cellulose-Fibers
journal, June 2000

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Peptide-Induced Affinity Binding of Carbonic Anhydrase to Carbon Nanotubes
journal, January 2015

  • Chen, Xiaoxing; Wang, Yibing; Wang, Ping
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Immobilization of lipase enzyme in polyvinyl alcohol (PVA) nanofibrous membranes
journal, February 2008

Improvement of hydrogen peroxide stability of Pleurotus eryngii versatile ligninolytic peroxidase by rational protein engineering
journal, January 2014

Acidic sweep gas with carbonic anhydrase coated hollow fiber membranes synergistically accelerates CO2 removal from blood
journal, October 2015

Amperometric enzymic determination of triglycerides in serum
journal, October 1982

  • Winartasaputra, Handani.; Kuan, Shia S.; Guilbault, George G.
  • Analytical Chemistry, Vol. 54, Issue 12
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Orientational order and mechanical properties of poly(amide-block-aramid) alternating block copolymer films and fibers
journal, December 2006

Enzyme immobilization onto renewable polymeric matrixes: Past, present, and future trends
journal, March 2015

  • Bezerra, Camilla Salviano; de Farias Lemos, Celina Maria Gentil; de Sousa, Marylane
  • Journal of Applied Polymer Science, Vol. 132, Issue 26
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Enzyme entrapment, biocatalyst immobilization without covalent attachment
journal, January 2021

  • Imam, Hasan T.; Marr, Patricia C.; Marr, Andrew C.
  • Green Chemistry, Vol. 23, Issue 14
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Immobilization of α-amylase onto poly(glycidyl methacrylate) grafted electrospun fibers by ATRP
journal, May 2015

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Oriented immobilization of proteins on solid supports for use in biosensors and biochips: a review
journal, August 2015

Progress on polymeric hollow fiber membrane preparation technique from the perspective of green and sustainable development
journal, January 2021

Biodegradable microspheres as carriers for native superoxide dismutase and catalase delivery
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  • Giovagnoli, Stefano; Blasi, Paolo; Ricci, Maurizio
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Durable and Versatile Immobilized Carbonic Anhydrase on Textile Structured Packing for CO2 Capture
journal, September 2022

Nanofibrous membranes for single-step immobilization of hyperthermophilic enzymes
journal, December 2014

The Depth of Chemical Time and the Power of Enzymes as Catalysts
journal, December 2001

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  • Accounts of Chemical Research, Vol. 34, Issue 12
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Polyethylenimine: a very useful ionic polymer in the design of immobilized enzyme biocatalysts
journal, January 2017

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Covalent immobilization of cyclodextrin glucanotransferase on kenaf cellulose nanofiber and its application in ultrafiltration membrane system
journal, April 2017

Extreme Stabilization of a Thermolysin-like Protease by an Engineered Disulfide Bond
journal, April 1997

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High Modulus Regenerated Cellulose Fibers Spun from a Low Molecular Weight Microcrystalline Cellulose Solution
journal, August 2016

  • Zhu, Chenchen; Richardson, Robert M.; Potter, Kevin D.
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Static mixing spacers for spiral wound modules
journal, September 2013

Increased thermal and organic solvent tolerance of modified horseradish peroxidase
journal, February 2006

  • Liu, Jian-Zhong; Wang, Teng-Li; Huang, Ming-Tao
  • Protein Engineering, Design and Selection, Vol. 19, Issue 4
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An overview of technologies for immobilization of enzymes and surface analysis techniques for immobilized enzymes
journal, January 2015

  • Mohamad, Nur Royhaila; Marzuki, Nur Haziqah Che; Buang, Nor Aziah
  • Biotechnology & Biotechnological Equipment, Vol. 29, Issue 2
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A General Overview of Support Materials for Enzyme Immobilization: Characteristics, Properties, Practical Utility
journal, February 2018

  • Zdarta, Jakub; Meyer, Anne; Jesionowski, Teofil
  • Catalysts, Vol. 8, Issue 2
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Application of carbon fibers to flexible enzyme electrodes
journal, November 2016

Immobilization of lipase on cotton cloth using the layer-by-layer self-assembly technique
journal, January 2012

  • Karimpil, Joceline J.; Melo, J. S.; D'Souza, S. F.
  • International Journal of Biological Macromolecules, Vol. 50, Issue 1
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Facile Fabrication of Flowerlike Natural Nanotube/Layered Double Hydroxide Composites as Effective Carrier for Lysozyme Immobilization
journal, May 2015

A Review: Potential Usage of Cellulose Nanofibers (CNF) for Enzyme Immobilization via Covalent Interactions
journal, November 2014

  • Sulaiman, Safwan; Mokhtar, Mohd Noriznan; Naim, Mohd Nazli
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Preparation of biocatalytic nanofibres with high activity and stability via enzyme aggregate coating on polymer nanofibres
journal, April 2005

Biocatalytic Yarn for Peroxide Decomposition with Controlled Liquid Transport
journal, February 2021

  • Yuan, Yue; Zhang, Yuxuan; Bilheux, Hassina
  • Advanced Materials Interfaces, Vol. 8, Issue 7
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Functional Properties of Antimicrobial Lysozyme-Chitosan Composite Films
journal, October 2004

Ionic Liquid Platform for Spinning Composite Chitin–Poly(lactic acid) Fibers
journal, June 2018

  • Shamshina, Julia L.; Zavgorodnya, Oleksandra; Berton, Paula
  • ACS Sustainable Chemistry & Engineering, Vol. 6, Issue 8
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Immobilization of catalase via adsorption onto l-histidine grafted functional pHEMA based membrane
journal, November 2001

  • Akgöl, Sinan; Kaçar, Yasemin; Özkara, Serpil
  • Journal of Molecular Catalysis B: Enzymatic, Vol. 15, Issue 4-6
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Bromelain immobilization in cellulose triacetate nanofiber membranes from sugarcane bagasse by electrospinning technique
journal, January 2020

Potential applications of enzymes immobilized on/in nano materials: A review
journal, May 2012

Electrospun polyvinyl alcohol/bovine serum albumin biocomposite membranes for horseradish peroxidase immobilization
journal, November 2016

Graphene Oxide as a Matrix for Enzyme Immobilization
journal, March 2010

  • Zhang, Jiali; Zhang, Feng; Yang, Haijun
  • Langmuir, Vol. 26, Issue 9
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Immobilization of Lipases on Magnetic Collagen Fibers and Its Applications for Short-Chain Ester Synthesis
journal, June 2017

Carbonic Anhydrase as a Model for Biophysical and Physical-Organic Studies of Proteins and Protein−Ligand Binding
journal, March 2008

  • Krishnamurthy, Vijay M.; Kaufman, George K.; Urbach, Adam R.
  • Chemical Reviews, Vol. 108, Issue 3
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Enzymes on material surfaces
journal, May 2012

Enzyme immobilization on electrospun polymer nanofibers: An overview
journal, April 2009

Enzyme-Carrying Polymeric Nanofibers Prepared via Electrospinning for Use as Unique Biocatalysts
journal, October 2002

  • Jia, H.; Zhu, G.; Vugrinovich, B.
  • Biotechnology Progress, Vol. 18, Issue 5
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Effects of internal mass transfer and product inhibition on a simulated immobilized enzyme-catalyzed reactor for lactose hydrolysis
journal, April 2005

Interactions of graphene and graphene oxide with proteins and peptides
journal, February 2013

Laccase immobilization on enzymatically functionalized polyamide 6,6 fibres
journal, November 2007

Cross-linked Polymer Nanofibers for Hyperthermophilic Enzyme Immobilization: Approaches to Improve Enzyme Performance
journal, July 2014

  • Tang, Christina; Saquing, Carl D.; Morton, Stephen W.
  • ACS Applied Materials & Interfaces, Vol. 6, Issue 15
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Quantitative analysis of immobilized metalloenzymes by atomic absorption spectroscopy
journal, November 2004

  • Opwis, Klaus; Knittel, Dierk; Schollmeyer, Eckhard
  • Analytical and Bioanalytical Chemistry, Vol. 380, Issue 7-8
  • DOI: 10.1007/s00216-004-2875-8

Stabilization of Enzymes in Silk Films
journal, March 2009

  • Lu, Shenzhou; Wang, Xiaoqin; Lu, Qiang
  • Biomacromolecules, Vol. 10, Issue 5
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Enzyme textile for removal of urea with coupling process: enzymatic reaction and electrodialysis
journal, September 2002

Covalent attachment of lysozyme to cotton/cellulose materials: protein verses solid support activation
journal, June 2011

A New Type of Optical Fiber Glucose Biosensor With Enzyme Immobilized by Electrospinning
journal, July 2021

Immobilization of glucose oxidase into polyaniline nanofiber matrix for biofuel cell applications
journal, May 2011

Antibacterial functionalization of wool fabric via immobilizing lysozymes
journal, December 2008

  • Wang, Qiang; Fan, Xuerong; Hu, Yingjun
  • Bioprocess and Biosystems Engineering, Vol. 32, Issue 5
  • DOI: 10.1007/s00449-008-0286-5

Natural Nanotube-Based Biomimetic Porous Microspheres for Significantly Enhanced Biomolecule Immobilization
journal, August 2013

  • Chao, Cong; Zhang, Bing; Zhai, Rui
  • ACS Sustainable Chemistry & Engineering, Vol. 2, Issue 3
  • DOI: 10.1021/sc400199v

Metal-organic framework/enzyme coated optical fibers as waveguide-based biosensors
journal, June 2019

Estimation of the Effectiveness Factor for Immobilized Enzyme Catalysts through a Simple Conversion Assay
journal, November 2019

Improved thermal performance of Thermomyces lanuginosus GH11 xylanase by engineering of an N-terminal disulfide bridge
journal, May 2012

Immobilization of α-amylase in ultrafine polyvinyl alcohol (PVA) fibers via electrospinning and their stability on different substrates
journal, April 2019

  • Porto, Mariana Dias Antunes; dos Santos, Jaqueline Pozzada; Hackbart, Helen
  • International Journal of Biological Macromolecules, Vol. 126
  • DOI: 10.1016/j.ijbiomac.2018.12.263

Biocatalysis: Enzymatic Synthesis for Industrial Applications
journal, August 2020

  • Wu, Shuke; Snajdrova, Radka; Moore, Jeffrey C.
  • Angewandte Chemie International Edition, Vol. 60, Issue 1
  • DOI: 10.1002/anie.202006648

Kinetics of Secondary Structure Recovery during the Refolding of Reduced Hen Egg White Lysozyme
journal, October 1997

  • Roux, Pascale; Delepierre, Muriel; Goldberg, Michel E.
  • Journal of Biological Chemistry, Vol. 272, Issue 40
  • DOI: 10.1074/jbc.272.40.24843

Fabricating polystyrene fiber-dehydrogenase assemble as a functional biocatalyst
journal, January 2015

Agarose and Its Derivatives as Supports for Enzyme Immobilization
journal, November 2016

Carbonic Anhydrase Immobilized on Textile Structured Packing Using Chitosan Entrapment for CO2 Capture
journal, June 2022

Enzymic Thin Film Coatings for Bioactive Materials
journal, June 2008

  • Tong, X.; Trivedi, A.; Jia, H.
  • Biotechnology Progress, Vol. 24, Issue 3
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Preparation of high strength chitosan fibers by using ionic liquid as spinning solution
journal, January 2012

  • Li, Lu; Yuan, Bing; Liu, Shiwei
  • Journal of Materials Chemistry, Vol. 22, Issue 17
  • DOI: 10.1039/c2jm30555k

Protease immobilization on cellulose monoacetate/chitosan-blended nanofibers
journal, July 2017

  • Demirkan, Elif; Avci, Tuba; Aykut, Yakup
  • Journal of Industrial Textiles, Vol. 47, Issue 8
  • DOI: 10.1177/1528083717720205

A Novel Xylan-Polyvinyl Alcohol Hydrogel Bead with Laccase Entrapment for Decolorization of Reactive Black 5
journal, July 2016

Modified PMMA monosize microbeads for glucose oxidase immobilization
journal, January 1997

Immobilised enzymes: science or art?
journal, April 2005

Guidelines and Cost Analysis for Catalyst Production in Biocatalytic Processes
journal, January 2011

  • Tufvesson, Pär; Lima-Ramos, Joana; Nordblad, Mathias
  • Organic Process Research & Development, Vol. 15, Issue 1
  • DOI: 10.1021/op1002165

Immobilised enzymes: carrier-bound or carrier-free?
journal, August 2003

Immobilization of Horseradish Peroxidase on Nonwoven Polyester Fabric Coated with Chitosan
journal, September 2007

  • Mohamed, Saleh A.; Aly, A. S.; Mohamed, Tarek M.
  • Applied Biochemistry and Biotechnology, Vol. 144, Issue 2
  • DOI: 10.1007/s12010-007-8026-x

Enzyme catalysis on solid surfaces
journal, June 2008

Laccase immobilization on bacterial nanocellulose membranes: Antimicrobial, kinetic and stability properties
journal, July 2016

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