Skip to main content
Log in

Characteristics of glucose oxidase immobilized on carbon-encapsulated iron nanoparticles decorated with polyethyleneimine

  • Original Paper
  • Published:
Polymer Bulletin Aims and scope Submit manuscript

Abstract

This study aimed to conjugate glucose oxidase (GOX) with carbon-encapsulated iron nanoparticles (Fe@C) which were functionalized with carboxylic groups and decorated with branched polyethyleneimine (PEI), in order to yield Fe@C-NH-PEI-GOX and Fe@C-(CH2)2-CONH-PEI-GOX derivatives. The process of electrostatic attachment of the GOX enzyme on the Fe@C-NH-PEI and Fe@C-(CH2)2CONH-PEI constructs was optimized, and the amount of enzyme attached on the constructs was also estimated. The steady-state kinetics of β-D-glucose oxidation by molecular oxygen, a reaction catalyzed by GOX, were compared using a native GOX enzyme obtained from Aspergillus niger and nanoparticles-conjugated GOX. The Fe@C-NH-PEI-GOX and Fe@C-(CH2)2-CONH-PEI-GOX constructs were formed by electrostatic interaction between positively charged Fe@C-NH-PEI and Fe@C-(CH2)2-CONH-PEI and negatively charged GOX in water media at pH 6. The activity of the immobilized enzyme on Fe@C-NH-PEI-GOX and Fe@C-(CH2)2-CONH-PEI-GOX derivatives was preserved, with Km values of 3271 and 1605 µM, respectively. However, the catalytic activity of Fe@C-NH-PEI-GOX and Fe@C-(CH2)2-CONH-PEI-GOX was reduced up to 20- and tenfold in comparison to that of the free GOX enzyme. The results of the study suggest that PEI is a promising cationic polymer with a high loading capacity and that the use of a simple adsorption process for preparing Fe@C-NH-PEI-GOX and Fe@C-(CH2)2-CONH-PEI-GOX conjugates is a highly efficient approach for stable immobilization of GOX enzyme on carbon-encapsulated iron nanoparticles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. The Sci Total Environ 400(1–3):396–414. https://doi.org/10.1016/j.scitotenv.2008.06.042

    Article  CAS  Google Scholar 

  2. Li J, Xin M, Ma Z, Shi Y, Pan L (2021) Nanomaterials and their applications on bio-inspired wearable electronics. Nanotechnology. https://doi.org/10.1088/1361-6528/abe6c7

    Article  Google Scholar 

  3. Hu X, Zhang Y, Ding T, Liu J, Zhao H (2020) Multifunctional gold nanoparticles: a novel nanomaterial for various medical applications and biological activities. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2020.00990

    Article  Google Scholar 

  4. Rajabathar JR, Periyasami G, Alanazi AM, Govindasamy M, Arunachalam P (2020) Review on carbon nanotube varieties for healthcare application: effect of preparation methods and mechanism insight. Processes. https://doi.org/10.3390/pr8121654

    Article  Google Scholar 

  5. Zhang L, Ying Y, Li Y, Fu Y (2020) Integration and synergy in protein-nanomaterial hybrids for biosensing: strategies and in-field detection applications. Biosens Bioelectron. https://doi.org/10.1016/j.bios.2020.112036

    Article  Google Scholar 

  6. Ates B, Ulu A, Koytepe S, Noma SAA, Kolat VS, Izgi T (2018) Magnetic-propelled Fe3O4-chitosan carriers enhance l-asparaginase catalytic activity: a promising strategy for enzyme immobilization. RSC Adv 8(63):36063–36075. https://doi.org/10.1039/c8ra06346j

    Article  CAS  Google Scholar 

  7. Tarhan T, Ulu A, Saricam M, Culha M, Ates B (2020) Maltose functionalized magnetic core/shell Fe3O4@Au nanoparticles for an efficient L-asparaginase immobilization. Int J Biol Macromol 142:443–451. https://doi.org/10.1016/j.ijbiomac.2019.09.116

    Article  CAS  Google Scholar 

  8. Giugliano AMM, Michele (2014) Carbon-based smart nanomaterials in biomedicine and neuroengineering. Beilstein J Nanotechnol 5(1):1849-1863. https://doi.org/10.3762/bjnano.5.196

  9. Ulu A, Noma SAA, Koytepe S, Ates B (2018) Magnetic Fe3O4@MCM-41 core-shell nanoparticles functionalized with thiol silane for efficient l-asparaginase immobilization. Artif Cells Nanomed Biotechnol 46:1035–1045. https://doi.org/10.1080/21691401.2018.1478422

    Article  CAS  Google Scholar 

  10. Bamburowicz-Klimkowska M, Poplawska M, Grudzinski IP (2019) Nanocomposites as biomolecules delivery agents in nanomedicine. J Nanobiotechnol. https://doi.org/10.1186/s12951-019-0479-x

    Article  Google Scholar 

  11. Noma SAA, Ulu A, Acet O, Sanz R, Sanz-Perez ES, Odabasi M, Ates B (2020) Comparative study of ASNase immobilization on tannic acid-modified magnetic Fe3O4/SBA-15 nanoparticles to enhance stability and reusability. New J Chem 44(11):4440–4451. https://doi.org/10.1039/d0nj00127a

    Article  CAS  Google Scholar 

  12. Bankar SB, Bule MV, Singhal RS, Ananthanarayan L (2009) Glucose oxidase - an overview. Biotechnol Adv 27(4):489–501. https://doi.org/10.1016/j.biotechadv.2009.04.003

    Article  CAS  Google Scholar 

  13. Leskovac V, Trivic S, Wohlfahrt G, Kandrac J, Pericin D (2005) Glucose oxidase from Aspergillus niger: the mechanism of action with molecular oxygen, quinones, and one-electron acceptors. Int J Biochem Cell Biol 37(4):731–750. https://doi.org/10.1016/j.biocel.2004.10.014

    Article  CAS  Google Scholar 

  14. Ammam M, Fransaer J (2011) Effects of AC-electrolysis on the enzymatic activity of glucose oxidase. Electroanalysis 23(3):755–763. https://doi.org/10.1002/elan.201000598

    Article  CAS  Google Scholar 

  15. Fu LH, Qi C, Lin J, Huang P (2018) Catalytic chemistry of glucose oxidase in cancer diagnosis and treatment. Chem Soc Rev 47(17):6454–6472. https://doi.org/10.1039/c7cs00891k

    Article  CAS  Google Scholar 

  16. Dubey MK, Zehra A, Aamir M, Meena M, Ahirwal L, Singh S, Shukla S, Upadhyay RS, Bueno-Mari R, Bajpai VK (2017) Improvement strategies, cost effective production, and potential applications of fungal glucose oxidase (GOD): current updates. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01032

    Article  Google Scholar 

  17. Wong CM, Wong KH, Chen XD (2008) Glucose oxidase: natural occurrence, function, properties and industrial applications. Appl Microbiol Biotechnol 78(6):927–938. https://doi.org/10.1007/s00253-008-1407-4

    Article  CAS  Google Scholar 

  18. Li XJ, Xie XF, Xing FG, Xu L, Zhang J, Wang ZD (2019) Glucose oxidase as a control agent against the fungal pathogen Botrytis cinerea in postharvest strawberry. Food Control 105:277–284. https://doi.org/10.1016/j.foodcont.2019.05.037

    Article  CAS  Google Scholar 

  19. Maity D, Minitha CR, Kumar RTR (2019) Glucose oxidase immobilized amine terminated multiwall carbon nanotubes/reduced graphene oxide/polyaniline/gold nanoparticles modified screen-printed carbon electrode for highly sensitive amperometric glucose detection. Mater Sci Eng C-Mater Biol Appl. https://doi.org/10.1016/j.msec.2019.110075

    Article  Google Scholar 

  20. Siddique S, Mukhtar H (2019) Probing the performance of glucose oxidase treated graphene-based field effect transistors. J Nanosci Nanotechnol 19(11):7442–7446. https://doi.org/10.1166/jnn.2019.16723

    Article  CAS  Google Scholar 

  21. Raba J, Mottola HA (1995) Glucose-oxidase as an analytical reagent. Crit Rev Anal Chem 25(1):1–42. https://doi.org/10.1080/10408349508050556

    Article  CAS  Google Scholar 

  22. Bahulekar R, Ayyangar NR, Ponrathnam S (1991) Polyethyleneimine in immobilization of biocataysts. Enzyme Microb Technol 13(11):858–868. https://doi.org/10.1016/0141-0229(91)90101-f

    Article  CAS  Google Scholar 

  23. Altikatoglu M, Basaran Y, Arioz C, Ogan A, Kuzu H (2010) Glucose oxidase-dextran conjugates with enhanced stabilities against temperature and pH. Appl Biochem Biotechnol 160(8):2187–2197. https://doi.org/10.1007/s12010-009-8812-8

    Article  CAS  Google Scholar 

  24. Holland JT, Lau C, Brozik S, Atanassov P, Banta S (2011) Engineering of glucose oxidase for direct electron transfer via site-specific gold nanoparticle conjugation. J Am Chem Soc 133(48):19262–19265. https://doi.org/10.1021/ja2071237

    Article  CAS  Google Scholar 

  25. Zhu Z, Wang M, Gautam A, Nazor J, Momeu C, Prodanovic R, Schwaneberg U (2007) Directed evolution of glucose oxidase from Aspergillus niger for ferrocenemethanol-mediated electron transfer. Biotechnol J 2(2):241–248. https://doi.org/10.1002/biot.200600185

    Article  CAS  Google Scholar 

  26. Bilal M, Ashraf SS, Romanholo Ferreira LF, Cui J, Lou W-Y, Franco M, Iqbal HMN (2020) Nanostructured materials as a host matrix to develop robust peroxidases-based nanobiocatalytic systems. Int J Biol Macromol 162:1906–1923. https://doi.org/10.1016/j.ijbiomac.2020.08.122

    Article  CAS  Google Scholar 

  27. Malar CG, Seenuvasan M, Kumar KS, Kumar A, Parthiban R (2020) Review on surface modification of nanocarriers to overcome diffusion limitations: an enzyme immobilization aspect. Biochem Eng J. https://doi.org/10.1016/j.bej.2020.107574

    Article  Google Scholar 

  28. Bolivar JM, Nidetzky B (2019) The microenvironment in immobilized enzymes: methods of characterization and its role in determining enzyme performance. Molecules. https://doi.org/10.3390/molecules24193460

    Article  Google Scholar 

  29. Reis CLB, de Sousa EYA, Serpa JD, Oliveira RC, dos Santos JCS (2019) Design of immobilized enzyme biocatalysts: drawbacks and opportunities. Quim Nova 42(7):768–783

    CAS  Google Scholar 

  30. Virgen-Ortiz JJ, dos Santos JCS, Berenguer-Murcia A, Barbosa O, Rodrigues RC, Fernandez-Lafuente R (2017) Polyethylenimine: a very useful ionic polymer in the design of immobilized enzyme biocatalysts. J Mater Chem B 5(36):7461–7490. https://doi.org/10.1039/c7tb01639e

    Article  CAS  Google Scholar 

  31. Xiang XR, Huang H, Hu Y (2017) Research progress on enzyme immobilized on nanocomposites. Chin J Inorg Chem 33(1):1–15

    CAS  Google Scholar 

  32. Jager M, Schubert S, Ochrimenko S, Fischer D, Schubert US (2012) Branched and linear poly(ethylene imine)-based conjugates: synthetic modification, characterization, and application. Chem Soc Rev 41(13):4755–4767. https://doi.org/10.1039/c2cs35146c

    Article  CAS  Google Scholar 

  33. Gao SQ, Tian HY, Xing ZK, Zhang DW, Guo Y, Guo ZP, Zhu XJ, Chen XS (2016) A non-viral suicide gene delivery system traversing the blood brain barrier for non-invasive glioma targeting treatment. J Control Release 243:357–369. https://doi.org/10.1016/j.jconrel.2016.10.027

    Article  CAS  Google Scholar 

  34. Demeneix B, Behr JP (2005). Polyethylenimine (PEI). Non-viral vectors for gene therapy, 2nd Edition: Part 1. Huang L, Hung MC and Wagner E. 53:217–230

  35. Zhang YG, Shu HM, Hu J, Zhang M, Wu JW, Liu KH, Zhu Q (2016) Binding affinity, cellular uptake, and subsequent intracellular trafficking of the nano-gene vector P123-PEI-R13. J Nanomater. https://doi.org/10.1155/2016/7064246

    Article  Google Scholar 

  36. Choosakoonkriang S, Lobo BA, Koe GS, Koe JG, Middaugh CR (2003) Biophysical characterization of PEI/DNA complexes. J Pharm Sci 92(8):1710–1722. https://doi.org/10.1002/jps.10437

    Article  CAS  Google Scholar 

  37. Sun CB, Tang T, Uludag H, Cuervo JE (2011) Molecular dynamics simulations of DNA/PEI complexes: effect of pei branching and protonation state. Biophys J 100(11):2754–2763. https://doi.org/10.1016/j.bpj.2011.04.045

    Article  CAS  Google Scholar 

  38. Taranejoo S, Liu J, Verma P, Hourigan K (2015) A review of the developments of characteristics of PEI derivatives for gene delivery applications. J Appl Polym Sci. https://doi.org/10.1002/app.42096

    Article  Google Scholar 

  39. Degors IMS, Wang CF, Rehman ZU, Zuhorn IS (2019) Carriers break barriers in drug delivery: endocytosis and endosomal escape of gene delivery vectors. Acc Chem Res 52(7):1750–1760. https://doi.org/10.1021/acs.accounts.9b00177

    Article  CAS  Google Scholar 

  40. Di Gioia S, Conese M (2009) Polyethylenimine-mediated gene delivery to the lung and therapeutic applications. Drug Des Dev Ther 2:163–188

    Google Scholar 

  41. Merlin JL, N’Doye A, Bouriez T, Dolivet G (2002) Polyethylenimine derivatives as potent nonviral vectors for gene transfer. Drug News Perspect 15(7):445–451. https://doi.org/10.1358/dnp.2002.15.7.840080

    Article  CAS  Google Scholar 

  42. Kasprzak A, Poplawska M, Bystrzejewski M, Labedz O, Grudzinski IP (2015) Conjugation of polyethylenimine and its derivatives to carbon-encapsulated iron nanoparticles. RSC Adv 5(104):85556–85567. https://doi.org/10.1039/c5ra17912b

    Article  CAS  Google Scholar 

  43. Masotti A, Pitta A, Ortaggi G, Corti M, Innocenti C, Lascialfari A, Marinone M, Marzola P, Daducci A, Sbarbati A, Micotti E, Orsini F, Poletti G, Sangregorio C (2009) Synthesis and characterization of polyethylenimine-based iron oxide composites as novel contrast agents for MRI. Magn Reson Mater Phys, Biol Med 22(2):77–87. https://doi.org/10.1007/s10334-008-0147-x

    Article  CAS  Google Scholar 

  44. Guller AE, Nadort A, Generalova AN, Khaydukov EV, Nechaev AV, Kornienko IA, Petersen EV, Liang L, Shekhter AB, Qian Y, Goldys EM, Zvyagin AV (2018) Rational surface design of upconversion nanoparticles with polyethylenimine coating for biomedical applications: Better Safe than brighter? ACS Biomater Sci Eng 4(9):3143–3153. https://doi.org/10.1021/acsbiomaterials.8b00633

    Article  CAS  Google Scholar 

  45. Zhang Y, Tan X, Ren T, Jia C, Yang Z, Sun H (2018) Folate-modified carboxymethyl-chitosan/polyethylenimine/bovine serum albumin based complexes for tumor site-specific drug delivery. Carbohyd Polym 198:76–85. https://doi.org/10.1016/j.carbpol.2018.06.055

    Article  CAS  Google Scholar 

  46. Zakeri A, Kouhbanani MAJ, Beheshtkhoo N, Beigi V, Mousavi SM, Hashemi SAR, Zade AK, Amani AM, Savardashtaki A, Mirzaei E, Jahandideh S, Movahedpour A (2018) Polyethylenimine-based nanocarriers in co-delivery of drug and gene: a developing horizon. Nano Rev Exp. https://doi.org/10.1080/20022727.2018.1488497

    Article  Google Scholar 

  47. Xue HY, Liu SM, Wong HL (2014) Nanotoxicity: a key obstacle to clinical translation of siRNA-based nanomedicine. Nanomedicine 9(2):295–312. https://doi.org/10.2217/nnm.13.204

    Article  CAS  Google Scholar 

  48. Padilla-Martinez SG, Martinez-Jothar L, Sampedro JG, Tristan F, Perez E (2015) Enhanced thermal stability and pH behavior of glucose oxidase on electrostatic interaction with polyethylenimine. Int J Biol Macromol 75:453–459. https://doi.org/10.1016/j.ijbiomac.2015.02.005

    Article  CAS  Google Scholar 

  49. Adeel M, Bilal M, Rasheed T, Sharma A, Iqbal HMN (2018) Graphene and graphene oxide: functionalization and nano-bio-catalytic system for enzyme immobilization and biotechnological perspective. Int J Biol Macromol 120:1430–1440. https://doi.org/10.1016/j.ijbiomac.2018.09.144

    Article  CAS  Google Scholar 

  50. Krishnan SK, Singh E, Singh P, Meyyappan M, Nalwa HS (2019) A review on graphene-based nanocomposites for electrochemical and fluorescent biosensors. RSC Adv 9(16):8778–8881. https://doi.org/10.1039/c8ra09577a

    Article  CAS  Google Scholar 

  51. Borysiuk J, Grabias A, Szczytko J, Bystrzejewski M, Twardowski A, Lange H (2008) Structure and magnetic properties of carbon encapsulated Fe nanoparticles obtained by arc plasma and combustion synthesis. Carbon 46(13):1693–1701. https://doi.org/10.1016/j.carbon.2008.07.011

    Article  CAS  Google Scholar 

  52. Bystrzejewski M, Huczko A, Lange H (2005) Arc plasma route to carbon-encapsulated magnetic nanoparticles for biomedical applications. Sens Actuators B-Chem 109(1):81–85. https://doi.org/10.1016/j.snb.2005.03.029

    Article  CAS  Google Scholar 

  53. Poplawska M, Bystrzejewski M, Grudzinski IP, Cywinska MA, Ostapko J, Cieszanowski A (2014) Immobilization of gamma globulins and polyclonal antibodies of class IgG onto carbon-encapsulated iron nanoparticles functionalized with various surface linkers. Carbon 74:180–194. https://doi.org/10.1016/j.carbon.2014.03.022

    Article  CAS  Google Scholar 

  54. Kasprzak A, Poplawska M, Bystrzejewski M, Grudzinski IP (2016) Sulfhydrylated graphene-encapsulated iron nanoparticles directly aminated with polyethylenimine: a novel magnetic nanoplatform for bioconjugation of gamma globulins and polyclonal antibodies. J Mater Chem B 4(33):5593–5607. https://doi.org/10.1039/c6tb00838k

    Article  CAS  Google Scholar 

  55. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150(1):76–85. https://doi.org/10.1016/0003-2697(85)90442-7

    Article  CAS  Google Scholar 

  56. Gimeno P, Bousquet C, Lassu N, Maggio A-F, Civade C, Brenier C, Lempereur L (2015) High-performance liquid chromatography method for the determination of hydrogen peroxide present or released in teeth bleaching kits and hair cosmetic products. J Pharm Biomed Anal 107:386–393. https://doi.org/10.1016/j.jpba.2015.01.018

    Article  CAS  Google Scholar 

  57. Petteys BJ, Frank EL (2011) Rapid determination of vitamin B-2 (riboflavin) in plasma by HPLC. Clin Chim Acta 412(1–2):38–43. https://doi.org/10.1016/j.cca.2010.08.037

    Article  CAS  Google Scholar 

  58. Cao X, Li Y, Zhang Z, Yu J, Qian J, Liu S (2012) Catalytic activity and stability of glucose oxidase/horseradish peroxidase co-confined in macroporous silica foam. Analyst 137(24):5785–5791. https://doi.org/10.1039/c2an36237f

    Article  CAS  Google Scholar 

  59. Cui JH, Cui HX, Wang Y, Sun CJ, Li K, Ren HY, Du W (2012) Application of PEI-modified magnetic nanoparticles as gene transfer vector for the genetic modification of animals. Adv Mater Sci Eng. https://doi.org/10.1155/2012/764521

    Article  Google Scholar 

  60. Ciaurriz P, Bravo E, Hamad-Schifferli K (2014) Effect of architecture on the activity of glucose oxidase/horseradish peroxidase/carbon nanoparticle conjugates. J Coll Interface Sci 414:73–81. https://doi.org/10.1016/j.jcis.2013.09.039

    Article  CAS  Google Scholar 

  61. Sun J, Wang CH, Wang YZ, Ji SX, Liu WF (2019) Immobilization of carbonic anhydrase on polyethylenimine/dopamine codeposited membranes. J Appl Polym Sci. https://doi.org/10.1002/app.47784

    Article  Google Scholar 

  62. Ozyilmaz G, Tukel SS, Alptekin O (2005) Activity and storage stability of immobilized glucose oxidase onto magnesium silicate. J Mol Catal B-Enzymatic 35(4–6):154–160. https://doi.org/10.1016/j.molcatb.2005.07.001

    Article  CAS  Google Scholar 

  63. Sozugecer S, Bayramgil NP (2013) Activity of glucose oxidase immobilized onto Fe3+ attached hydroxypropyl methylcellulose films. Coll Surf B-Biointerfaces 101:19–25. https://doi.org/10.1016/j.colsurfb.2012.05.029

    Article  CAS  Google Scholar 

  64. Wang H, Suo JQ, Wang CY, Wang RW (2020) Glucose oxidase immobilization with amino dendritic mesoporous silica nanoparticles and its application in glucose detection. Chem J Chin Univ Chin 41(8):1731–1738. https://doi.org/10.7503/cjcu20200146

    Article  CAS  Google Scholar 

  65. Gunzer G, Hennrich N (1984) Purification of alpha-1-proteinase Inhibitor by Triazine dye affinity-chromatography, ion-exchange chromatography and gel-filtration on fractogel TSK. J Chromatogr 296:221–229. https://doi.org/10.1016/s0021-9673(01)96415-5

    Article  CAS  Google Scholar 

  66. Lin P, Zhang YH, Yao GX, Huo HY, Ren H, Wang YX, Wang SZ, Fang BS (2019) Immobilization of formate dehydrogenase on polyethylenimine-grafted graphene oxide with kinetics and stability study. Eng Life Sci. https://doi.org/10.1002/elsc.201900134

    Article  Google Scholar 

  67. Wang Y, Wang Q, Song X, Cai J (2019) Hydrophilic polyethylenimine modified magnetic graphene oxide composite as an efficient support for dextranase immobilization with improved stability and recyclable performance. Biochem Eng J 141:163–172. https://doi.org/10.1016/j.bej.2018.10.015

    Article  CAS  Google Scholar 

  68. Weng Y, Jiang B, Yang K, Sui Z, Zhang L, Zhang Y (2015) Polyethyleneimine-modified graphene oxide nanocomposites for effective protein functionalization. Nanoscale 7(34):14284–14291. https://doi.org/10.1039/c5nr03370e

    Article  CAS  Google Scholar 

  69. Cheng C, Nie SQ, Li S, Peng H, Yang H, Ma L, Sun SD, Zhao CS (2013) Biopolymer functionalized reduced graphene oxide with enhanced biocompatibility via mussel inspired coatings/anchors. J Mater Chem B 1(3):265–275. https://doi.org/10.1039/c2tb00025c

    Article  CAS  Google Scholar 

  70. Sharifi M, Sohrabi MJ, Hosseinali SH, Hasan A, Kani PH, Talaei AJ, Karim AY, Nanakali NMQ, Salihi A, Aziz FM, Yan B, Khan RH, Saboury AA, Falahati M (2020) Enzyme immobilization onto the nanomaterials: application in enzyme stability and prodrug-activated cancer therapy. Int J Biol Macromol 143:665–676. https://doi.org/10.1016/j.ijbiomac.2019.12.064

    Article  CAS  Google Scholar 

  71. Ren H, Zhang Y, Su J, Lin P, Wang B, Fang B, Wang S (2017) Encapsulation of amine dehydrogenase in hybrid titania nanoparticles by polyethylenimine coating and templated biomineralization. J Biotechnol 241:33–41. https://doi.org/10.1016/j.jbiotec.2016.11.006

    Article  CAS  Google Scholar 

  72. Pazur JH, Kleppe K (1964) Oxidation of glucose and related compounds by glucose oxidase from Aspergillus Niger. Biochemistry 3(4):578–580. https://doi.org/10.1021/bi00892a018

    Article  CAS  Google Scholar 

  73. Cheng KW, Zhang Y, Li YJ, Gao ZG, Chen FH, Sun K, An PJ, Sun C, Jiang Y, Sun BW (2019) A novel pH-responsive hollow mesoporous silica nanoparticle (HMSN) system encapsulating doxorubicin (DOX) and glucose oxidase (GOX) for potential cancer treatment. J Mater Chem B 7(20):3291–3302. https://doi.org/10.1039/c8tb03198c

    Article  CAS  Google Scholar 

  74. Jia HF, Zhu GY, Wang P (2003) Catalytic behaviors of enzymes attached to nanoparticles: the effect of particle mobility. Biotechnol Bioeng 84(4):406–414. https://doi.org/10.1002/bit.10781

    Article  CAS  Google Scholar 

  75. Ramakrishna TRB, Nalder TD, Yang WR, Marshall SN, Barrow CJ (2018) Controlling enzyme function through immobilisation on graphene, graphene derivatives and other two dimensional nanomaterials. J Mater Chem B 6(20):3200–3218. https://doi.org/10.1039/c8tb00313k

    Article  CAS  Google Scholar 

  76. Szefler B, Diudea MV, Grudzinski IP (2016) Nature of polyethyleneimine-glucose oxidase interactions. Stud Univ Babes-Bolyai, Chem 61(1):249–260

    CAS  Google Scholar 

  77. D’Auria S, Marín-Navarro J, Roupain N, Talens-Perales D, Polaina J (2015) Identification and structural analysis of amino acid substitutions that increase the stability and activity of Aspergillus niger glucose oxidase. PLoS ONE 10(12):e0144289. https://doi.org/10.1371/journal.pone.0144289

    Article  CAS  Google Scholar 

  78. Kouassi GK, Irudayaraj J, McCarty G (2005) Activity of glucose oxidase functionalized onto magnetic nanoparticles. Biomagn Res Technol 3(1):1. https://doi.org/10.1186/1477-044x-3-1

    Article  Google Scholar 

  79. Gouda MD, Singh SA, Rao AGA, Thakur MS, Karanth NG (2003) Thermal inactivation of glucose oxidase - mechanism and stabilization using additives. J Biol Chem 278(27):24324–24333. https://doi.org/10.1074/jbc.M208711200

    Article  CAS  Google Scholar 

  80. Eremin AN, Metelitsa DI, Shishko ZF, Mikhailova RV, Yasenko MI, Lobanok AG (2001) Thermal stability of glucose oxidase from Penicillium adametzii. Appl Biochem Microbiol 37(6):578–586. https://doi.org/10.1023/a:1012398900194

    Article  CAS  Google Scholar 

  81. Bayramoglu G, Denizli A, Arica MY (2002) Membrane with incorporated hydrophobic ligand for hydrophobic interaction with proteins: application to lipase adsorption. Polym Int 51(10):966–972. https://doi.org/10.1002/pi.899

    Article  CAS  Google Scholar 

  82. Rodrigues RC, Ortiz C, Berenguer-Murcia A, Torres R, Fernandez-Lafuente R (2013) Modifying enzyme activity and selectivity by immobilization. Chem Soc Rev 42(15):6290–6307. https://doi.org/10.1039/c2cs35231a

    Article  CAS  Google Scholar 

  83. Willner I, Baron R, Willner B (2007) Integrated nanoparticle-biomolecule systems for biosensing and bioelectronics. Biosens Bioelectron 22(9–10):1841–1852. https://doi.org/10.1016/j.bios.2006.09.018

    Article  CAS  Google Scholar 

  84. Zhou L, Jiang Y, Gao J, Zhao X, Ma L, Zhou Q (2012) Oriented immobilization of glucose oxidase on graphene oxide. Biochem Eng J 69:28–31. https://doi.org/10.1016/j.bej.2012.07.025

    Article  CAS  Google Scholar 

  85. Zhou L, Jiang Y, Gao J, Zhao X, Ma L (2012) Graphene oxide as a matrix for the immobilization of glucose oxidase. Appl Biochem Biotechnol 168(6):1635–1642. https://doi.org/10.1007/s12010-012-9884-4

    Article  CAS  Google Scholar 

  86. Cooper CL, Dubin PL, Kayitmazer AB, Turksen S (2005) Polyelectrolyte-protein complexes. Curr Opin Coll Interface Sci 10(1–2):52–78. https://doi.org/10.1016/j.cocis.2005.05.007

    Article  CAS  Google Scholar 

  87. Wang Y, Wang Q, Song X, Cai J (2018) Improving the stability and reusability of dextranase by immobilization on polyethylenimine modified magnetic particles. New J Chem 42(11):8391–8399. https://doi.org/10.1039/c8nj00227d

    Article  CAS  Google Scholar 

  88. An JD, Patterson DA, McNeil S, Hossain MM (2014) Immobilization of lipase on woolen fabrics: enhanced effectiveness in stain removal. Biotechnol Prog 30(4):806–817. https://doi.org/10.1002/btpr.1912

    Article  CAS  Google Scholar 

  89. Dreyer DR, Todd AD, Bielawski CW (2014) Harnessing the chemistry of graphene oxide. Chem Soc Rev 43(15):5288–5301. https://doi.org/10.1039/c4cs00060a

    Article  CAS  Google Scholar 

  90. Hill A, Karboune S, Mateo C (2017) Investigating and optimizing the immobilization of levansucrase for increased transfructosylation activity and thermal stability. Process Biochem 61:63–72. https://doi.org/10.1016/j.procbio.2017.06.011

    Article  CAS  Google Scholar 

  91. Torres R, Mateo C, Fuentes M, Palomo JM, Ortiz C, Fernandez-Lafuente R, Guisan JM (2002) Reversible immobilization of invertase on Sepabeads coated with polyethyleneimine: optimization of the biocatalyst’s stability. Biotechnol Prog 18(6):1221–1226. https://doi.org/10.1021/bp020082q

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by GEMNS project funded by the European Union’s Seventh Framework Program under ERA NET EuroNanoMed II European Innovative Research and Technological Development Projects in Nanomedicine (NCBR Funding No. 08/09/10/ EuroNanoMed/2015). A part of this work was also supported by TEPCAN project funded by the Program "Applied research" under the Norwegian Financial Mechanisms 2014 – 2021/POLNOR 2019 (EEA and Norway Grants), Thematic areas: Welfare, health and care (NCBR Funding No. NOR/POLNOR/TEPCAN/0057/2019-00).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Magdalena Bamburowicz-Klimkowska.

Ethics declarations

Conflict of interest

There are no conflicts to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bamburowicz-Klimkowska, M., Kasprzak, A., Bystrzejewski, M. et al. Characteristics of glucose oxidase immobilized on carbon-encapsulated iron nanoparticles decorated with polyethyleneimine. Polym. Bull. 80, 1565–1586 (2023). https://doi.org/10.1007/s00289-022-04125-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00289-022-04125-1

Keywords

Navigation