ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Enzyme Immobilization in Polyelectrolyte Brushes: High Loading and Enhanced Activity Compared to Monolayers

  • Gustav Ferrand-Drake del Castillo
    Gustav Ferrand-Drake del Castillo
    Department of Chemistry and Chemical Engineering, Chalmers University of Technology, 41296 Göteborg, Sweden
  • Meike Koenig
    Meike Koenig
    Leibniz Institute of Polymer Research Dresden, Hohe Str. 6, D-01069 Dresden, Germany
    More by Meike Koenig
  • Martin Müller
    Martin Müller
    Leibniz Institute of Polymer Research Dresden, Hohe Str. 6, D-01069 Dresden, Germany
    Technische Universität Dresden, Physical Chemistry of Polymer Materials, Dresden, Germany
  • Klaus-Jochen Eichhorn
    Klaus-Jochen Eichhorn
    Leibniz Institute of Polymer Research Dresden, Hohe Str. 6, D-01069 Dresden, Germany
  • Manfred Stamm
    Manfred Stamm
    Leibniz Institute of Polymer Research Dresden, Hohe Str. 6, D-01069 Dresden, Germany
    Technische Universität Dresden, Physical Chemistry of Polymer Materials, Dresden, Germany
  • Petra Uhlmann
    Petra Uhlmann
    Leibniz Institute of Polymer Research Dresden, Hohe Str. 6, D-01069 Dresden, Germany
    Department of Chemistry, University of Nebraska−Lincoln, Hamilton Hall, 639 North 12th Street, Lincoln, Nebraska 68588, United States
  • , and 
  • Andreas Dahlin*
    Andreas Dahlin
    Department of Chemistry and Chemical Engineering, Chalmers University of Technology, 41296 Göteborg, Sweden
    *E-mail: [email protected]
Cite this: Langmuir 2019, 35, 9, 3479–3489
Publication Date (Web):February 11, 2019
https://doi.org/10.1021/acs.langmuir.9b00056
Copyright © 2019 American Chemical Society

    Article Views

    1616

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (1)»

    Abstract

    Abstract Image

    Catalysis by enzymes on surfaces has many applications. However, strategies for efficient enzyme immobilization with preserved activity are still in need of further development. In this work, we investigate polyelectrolyte brushes prepared by both grafting-to and grafting-from with the aim to achieve high catalytic activity. For comparison, self-assembled monolayers that bind enzymes with the same chemical interactions are included. We use the model enzyme glucose oxidase and two kinds of polymers: anionic poly(acrylic acid) and cationic poly(diethylamino)methyl methacrylate. Surface plasmon resonance and spectroscopic ellipsometry are used for accurate quantification of surface coverage. Besides binding more enzymes, the “3D-like” brush environment enhances the specific activity compared to immobilization on self-assembled monolayers. For grafting-from brushes, multilayers of enzymes were spontaneously and irreversibly immobilized without conjugation chemistry. When the pH was between the pI of the enzyme and the pKa of the polymer, binding was considerable (thousands of ng/cm2 or up to 50% of the polymer mass), even at physiological ionic strength. However, binding was observed also when the brushes were neutrally charged. For acidic brushes (both grafting-to and grafting-from), the activity was higher for covalent immobilization compared to noncovalent. For grafting-from brushes, a fully preserved specific activity compared to enzymes in the liquid bulk was achieved, both with covalent (acidic brush) and noncovalent (basic brush) immobilization. Catalytic activity of hundreds of pmol cm–2 s–1 was easily obtained for polybasic brushes only tens of nanometers in dry thickness. This study provides new insights for designing functional interfaces based on enzymatic catalysis.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.9b00056.

    • GOX quantification in bulk solution, further activity measurements data, IR spectra, XPS spectra, SE measurements, and details on Michaelis–Menten analysis (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 46 publications.

    1. Christian W. Pester, Harm-Anton Klok, Edmondo M. Benetti. Opportunities, Challenges, and Pitfalls in Making, Characterizing, and Understanding Polymer Brushes. Macromolecules 2023, 56 (24) , 9915-9938. https://doi.org/10.1021/acs.macromol.3c01292
    2. Gozde Aktas Eken, Yuming Huang, Yixin Guo, Christopher Ober. Visualization of the pH Response through Autofluorescent Poly(styrene-alt-N-maleimide) Polyelectrolyte Brushes. ACS Applied Polymer Materials 2023, 5 (2) , 1613-1623. https://doi.org/10.1021/acsapm.2c02066
    3. Gozde Aktas Eken, Christopher K. Ober. Strong Polyelectrolyte Brushes via Alternating Copolymers of Styrene and Maleimides: Synthesis, Properties, and Stability. Macromolecules 2022, 55 (13) , 5291-5300. https://doi.org/10.1021/acs.macromol.2c00647
    4. Bhabatosh Mandal, Sneha Mondal, Biswajit Hansda, Shailja Mishra, Ankit Ghosh, Tirtha Biswas, Basudev Das, Tanay kumar Mondal, Pallavi Kumari. Multipoint Immobilization at the Inert Center of Urease on Homofunctional Diazo-Activated Silica Gel: A Way of Restoring Room-Temperature Catalytic Sustainability for Perennial Utilization. Langmuir 2022, 38 (22) , 6826-6840. https://doi.org/10.1021/acs.langmuir.2c00022
    5. Ifra, Awaneesh Singh, Sampa Saha. High Adsorption of α-Glucosidase on Polymer Brush-Modified Anisotropic Particles Acquired by Electrospraying—A Combined Experimental and Simulation Study. ACS Applied Bio Materials 2021, 4 (10) , 7431-7444. https://doi.org/10.1021/acsabm.1c00682
    6. John Andersson, Gustav Ferrand-Drake del Castillo, Pierluigi Bilotto, Fredrik Höök, Markus Valtiner, Andreas Dahlin. Control of Polymer Brush Morphology, Rheology, and Protein Repulsion by Hydrogen Bond Complexation. Langmuir 2021, 37 (16) , 4943-4952. https://doi.org/10.1021/acs.langmuir.1c00271
    7. Xuebin Ma, Haiyan Sui, Qun Yu, Jiwei Cui, Jingcheng Hao. Silica Capsules Templated from Metal–Organic Frameworks for Enzyme Immobilization and Catalysis. Langmuir 2021, 37 (10) , 3166-3172. https://doi.org/10.1021/acs.langmuir.1c00065
    8. Lucca Trachsel, Shivaprakash N. Ramakrishna, Matteo Romio, Nicholas D. Spencer, Edmondo M. Benetti. Topology and Molecular Architecture of Polyelectrolytes Determine Their pH-Responsiveness When Assembled on Surfaces. ACS Macro Letters 2021, 10 (1) , 90-97. https://doi.org/10.1021/acsmacrolett.0c00750
    9. Gustav Ferrand-Drake del Castillo, Rebekah L. N. Hailes, Andreas Dahlin. Large Changes in Protonation of Weak Polyelectrolyte Brushes with Salt Concentration—Implications for Protein Immobilization. The Journal of Physical Chemistry Letters 2020, 11 (13) , 5212-5218. https://doi.org/10.1021/acs.jpclett.0c01289
    10. Héctor Sánchez-Morán, Joel L. Kaar, Daniel K. Schwartz. Supra-biological performance of immobilized enzymes enabled by chaperone-like specific non-covalent interactions. Nature Communications 2024, 15 (1) https://doi.org/10.1038/s41467-024-46719-5
    11. Yi Wang, Chong Cheng, Shuang Li, Shudong Sun, Changsheng Zhao. Immobilization of carbonic anhydrase on modified PES membranes for artificial lungs. Journal of Materials Chemistry B 2024, 12 (9) , 2364-2372. https://doi.org/10.1039/D3TB02553E
    12. Xiaoyun Hou, Qinghong Shi. Conjugation of Candida rugosa lipase with hydrophobic polymer improves esterification activity of vitamin E in nonaqueous solvent. Chinese Journal of Chemical Engineering 2023, 62 , 182-191. https://doi.org/10.1016/j.cjche.2023.04.005
    13. Chen Zhuang, Guanglin Zhu, Yingjun Wang, Lin Wang, Xuetao Shi, Chuanbin Mao. A Facile Crystallization Strategy to Turn Calcium Bisphosphonates into Novel Osteogenesis‐Inducing Biomaterials. Advanced Healthcare Materials 2023, 12 (22) https://doi.org/10.1002/adhm.202203004
    14. Thaís Marcelino, Miguel A. Ramos Docampo, Xiaomin Qian, Carina Ade, Edit Brodszkij, Marcel Ceccato, Morten Foss, Mark Dulchavsky, James C. A. Bardwell, Brigitte Städler. Surfaces Coated with Polymer Brushes Work as Carriers for Histidine Ammonia Lyase. Macromolecular Bioscience 2023, 23 (8) https://doi.org/10.1002/mabi.202200528
    15. Qais M. Al-Bataineh, Ahmad A. Ahmad, Ihsan Aljarrah, Ahmad D. Telfah. Optical and electrical properties of poly(4-styrenesulfonic acid)-polyacrylic acid polyelectrolyte brushes incorporating with potassium permanganate. Surfaces and Interfaces 2023, 39 , 102923. https://doi.org/10.1016/j.surfin.2023.102923
    16. Daniela Eixenberger, Aditya Kumar, Saskia Klinger, Nico Scharnagl, Ayad W. H. Dawood, Andreas Liese. Polymer-Grafted 3D-Printed Material for Enzyme Immobilization—Designing a Smart Enzyme Carrier. Catalysts 2023, 13 (7) , 1130. https://doi.org/10.3390/catal13071130
    17. Qais M. Al-Bataineh, Ahmad D. Telfah, Victoria Shpacovitch, Carlos J. Tavares, Roland Hergenröder. Switchable Polyacrylic Acid Polyelectrolyte Brushes for Surface Plasmon Resonance Applications. Sensors 2023, 23 (9) , 4283. https://doi.org/10.3390/s23094283
    18. Andrei Popkov, Ziran Su, Sigyn Björk Sigurdardóttir, Jianquan Luo, Magdalena Malankowska, Manuel Pinelo. Engineering polyelectrolyte multilayer coatings as a strategy to optimize enzyme immobilization on a membrane support. Biochemical Engineering Journal 2023, 193 , 108838. https://doi.org/10.1016/j.bej.2023.108838
    19. Mustafa Oguzhan Caglayan. Ellipsometric biosensors. 2023, 197-237. https://doi.org/10.1016/B978-0-323-88431-0.00016-8
    20. Taira Ishiguro, Akiko Obata, Kenji Nagata, Toshihiro Kasuga, Toshihisa Mizuno. Core–shell fibremats comprising a poly(AM/DAAM)/ADH nanofibre core and nylon6 shell layer are an attractive immobilization platform for constructing immobilised enzymes. RSC Advances 2022, 12 (54) , 34931-34940. https://doi.org/10.1039/D2RA06620C
    21. Dmitry Galyamin, Lena M. Ernst, Aina Fitó-Parera, Guillem Mira-Vidal, Neus G. Bastús, Neus Sabaté, Victor Puntes. Nanoceria dissolution at acidic pH by breaking off the catalytic loop. Nanoscale 2022, 14 (38) , 14223-14230. https://doi.org/10.1039/D2NR03586C
    22. Vladimir I. Muronetz, Denis V. Pozdyshev, Pavel I. Semenyuk. Polyelectrolytes for Enzyme Immobilization and the Regulation of Their Properties. Polymers 2022, 14 (19) , 4204. https://doi.org/10.3390/polym14194204
    23. Jakub Zdarta, Sigyn Björk Sigurdardóttir, Katarzyna Jankowska, Manuel Pinelo. Laccase immobilization in polyelectrolyte multilayer membranes for 17α-ethynylestradiol removal: Biocatalytic approach for pharmaceuticals degradation. Chemosphere 2022, 304 , 135374. https://doi.org/10.1016/j.chemosphere.2022.135374
    24. Samiksha Shrivastava, Ifra, Sampa Saha, Awaneesh Singh. Dissipative particle dynamics simulation study on ATRP-brush modification of variably shaped surfaces and biopolymer adsorption. Physical Chemistry Chemical Physics 2022, 24 (30) , 17986-18003. https://doi.org/10.1039/D2CP01749K
    25. Dennis Sebastian Wunschik, André Lorenz, Kim Nadine Ingenbosch, Jochen Stefan Gutmann, Kerstin Hoffmann-Jacobsen. Activation and Stabilization of Lipase B from Candida antarctica by Immobilization on Polymer Brushes with Optimized Surface Structure. Applied Biochemistry and Biotechnology 2022, 194 (8) , 3384-3399. https://doi.org/10.1007/s12010-022-03913-9
    26. Soo Hyun Lee, Won-Chul Lee, Eun Hye Koh, Iris Baffour Ansah, Jun-Yeong Yang, ChaeWon Mun, Seunghun Lee, Dong-Ho Kim, Ho Sang Jung, Sung-Gyu Park. Organometallic hotspot engineering for ultrasensitive EC-SERS detection of pathogenic bacteria-derived DNAs. Biosensors and Bioelectronics 2022, 210 , 114325. https://doi.org/10.1016/j.bios.2022.114325
    27. Guangzhi Zhou, Ming Li. Near‐Infrared‐II Plasmonic Trienzyme‐Integrated Metal–Organic Frameworks with High‐Efficiency Enzyme Cascades for Synergistic Trimodal Oncotherapy. Advanced Materials 2022, 34 (24) https://doi.org/10.1002/adma.202200871
    28. Gustav Ferrand‐Drake del Castillo, Maria Kyriakidou, Zeynep Adali, Kunli Xiong, Rebekah L. N. Hailes, Andreas Dahlin. Electrically Switchable Polymer Brushes for Protein Capture and Release in Biological Environments**. Angewandte Chemie 2022, 134 (22) https://doi.org/10.1002/ange.202115745
    29. Gustav Ferrand‐Drake del Castillo, Maria Kyriakidou, Zeynep Adali, Kunli Xiong, Rebekah L. N. Hailes, Andreas Dahlin. Electrically Switchable Polymer Brushes for Protein Capture and Release in Biological Environments**. Angewandte Chemie International Edition 2022, 61 (22) https://doi.org/10.1002/anie.202115745
    30. Kazuhiko Ishihara, Kyoko Fukazawa. Cell-membrane-inspired polymers for constructing biointerfaces with efficient molecular recognition. Journal of Materials Chemistry B 2022, 10 (18) , 3397-3419. https://doi.org/10.1039/D2TB00242F
    31. Noelia M. Sanchez-Ballester, Flavien Sciortino, Sajjad Husain Mir, Gaulthier Rydzek. Weak Polyelectrolytes as Nanoarchitectonic Design Tools for Functional Materials: A Review of Recent Achievements. Molecules 2022, 27 (10) , 3263. https://doi.org/10.3390/molecules27103263
    32. Dionysios D. Neofytos, Aristeidis Papagiannopoulos, Evangelia D. Chrysina, Stergios Pispas. Formation and physicochemical properties of glycogen phosphorylase in complex with a cationic polyelectrolyte. International Journal of Biological Macromolecules 2022, 206 , 371-380. https://doi.org/10.1016/j.ijbiomac.2022.02.136
    33. John Andersson, Justas Svirelis, Gustav Ferrand-Drake del Castillo, Takumi Sannomiya, Andreas Dahlin. Surface plasmon resonance sensing with thin films of palladium and platinum – quantitative and real-time analysis. Physical Chemistry Chemical Physics 2022, 24 (7) , 4588-4594. https://doi.org/10.1039/D1CP05381G
    34. Andreas Dahlin. Biochemical Sensing with Nanoplasmonic Architectures: We Know How but Do We Know Why?. Annual Review of Analytical Chemistry 2021, 14 (1) , 281-297. https://doi.org/10.1146/annurev-anchem-091420-090751
    35. Evren Sel, Ahmet Ulu, Burhan Ateş, Süleyman Köytepe. Comparative study of catalase immobilization via adsorption on P(MMA-co-PEG500MA) structures as an effective polymer support. Polymer Bulletin 2021, 78 (5) , 2663-2684. https://doi.org/10.1007/s00289-020-03233-0
    36. Zülfikar Temoçin. Designing of a stable and selective glucose biosensor by glucose oxidase immobilization on glassy carbon electrode sensitive to H2O2 via nanofiber interface. Journal of Applied Electrochemistry 2021, 51 (2) , 283-293. https://doi.org/10.1007/s10800-020-01502-4
    37. Shuo Zeng, Jinwei Shi, Anchao Feng, Zhao Wang. Modification of Electrospun Regenerate Cellulose Nanofiber Membrane via Atom Transfer Radical Polymerization (ATRP) Approach as Advanced Carrier for Laccase Immobilization. Polymers 2021, 13 (2) , 182. https://doi.org/10.3390/polym13020182
    38. Adél Szerlauth, Szabolcs Muráth, Istvan Szilagyi. Layered double hydroxide-based antioxidant dispersions with high colloidal and functional stability. Soft Matter 2020, 16 (46) , 10518-10527. https://doi.org/10.1039/D0SM01531H
    39. Tai-Lam Nghiem, Deniz Coban, Stefanie Tjaberings, André H. Gröschel. Recent Advances in the Synthesis and Application of Polymer Compartments for Catalysis. Polymers 2020, 12 (10) , 2190. https://doi.org/10.3390/polym12102190
    40. G. Ferrand-Drake del Castillo, R. L. N. Hailes, Z. Adali-Kaya, T. Robson, Andreas Dahlin. Generic high-capacity protein capture and release by pH control. Chemical Communications 2020, 56 (44) , 5889-5892. https://doi.org/10.1039/D0CC01250E
    41. Stephanie Klinghammer, Sebastian Rauch, Sebastian Pregl, Petra Uhlmann, Larysa Baraban, Gianaurelio Cuniberti. Surface Modification of Silicon Nanowire Based Field Effect Transistors with Stimuli Responsive Polymer Brushes for Biosensing Applications. Micromachines 2020, 11 (3) , 274. https://doi.org/10.3390/mi11030274
    42. Artem Levin, Andreas Hartl, Oliver Reiser, Claus Czeslik. High-pressure study of magnetic nanoparticles with a polyelectrolyte brush as carrier particles for enzymes. Colloids and Surfaces B: Biointerfaces 2019, 182 , 110344. https://doi.org/10.1016/j.colsurfb.2019.110344
    43. Artem Levin, Süleyman Cinar, Michael Paulus, Julia Nase, Roland Winter, Claus Czeslik. Analyzing protein-ligand and protein-interface interactions using high pressure. Biophysical Chemistry 2019, 252 , 106194. https://doi.org/10.1016/j.bpc.2019.106194
    44. Ya Zhao, Li Liu, Hanying Zhao. Surface Reconstruction by a Coassembly Approach. Angewandte Chemie 2019, 131 (31) , 10687-10691. https://doi.org/10.1002/ange.201903798
    45. Ya Zhao, Li Liu, Hanying Zhao. Surface Reconstruction by a Coassembly Approach. Angewandte Chemie International Edition 2019, 58 (31) , 10577-10581. https://doi.org/10.1002/anie.201903798
    46. Meike Koenig, Ulla König, Klaus-Jochen Eichhorn, Martin Müller, Manfred Stamm, Petra Uhlmann. In-situ-Investigation of Enzyme Immobilization on Polymer Brushes. Frontiers in Chemistry 2019, 7 https://doi.org/10.3389/fchem.2019.00101

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect