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Review Article

Magnetic nanoflowers: a hybrid platform for enzyme immobilization

, , , , , , , , & ORCID Icon show all
Received 07 Jul 2022, Accepted 04 Apr 2023, Published online: 16 Jul 2023

References

  • Sheldon RA, Woodley JM. Role of biocatalysis in sustainable chemistry. Chem Rev. 2018;118:801–838. doi: 10.1021/acs.chemrev.7b00203.
  • Gurung N, Ray S, Bose S, et al. A broader view: microbial enzymes and their relevance in industries, medicine, and beyond. Biomed Res Int. 2013;2013:1–18. doi: 10.1155/2013/329121.
  • Beilen J v, Li Z. Enzyme technology: an overview. Curr Opin Biotechnol. 2002;13:338–344. doi: 10.1016/s0958-1669(02)00334-8.
  • Sharma B, Dangi AK, Shukla P. Contemporary enzyme based technologies for bioremediation: a review. J Environ Manage. 2018;210:10–22. doi: 10.1016/j.jenvman.2017.12.075.
  • Chiang S-J. Strain improvement for fermentation and biocatalysis processes by genetic engineering technology. J Ind Microbiol Biotechnol. 2004;31:99–108. doi: 10.1007/s10295-004-0131-z.
  • Chapman R, Stenzel MH. All wrapped up: stabilization of enzymes within single enzyme nanoparticles. J Am Chem Soc. 2019;141:2754–2769. doi: 10.1021/jacs.8b10338.
  • Bommarius AS, Paye MF. Stabilizing biocatalysts. Chem Soc Rev. 2013;42:6534–6565. doi: 10.1039/c3cs60137d.
  • Sheldon RA, van Pelt, S. Enzyme immobilisation in biocatalysis: why, what and how. Chem Soc Rev. 2013;42:6223–6235. doi: 10.1039/c3cs60075k.
  • Karpavičius A, Coene A, Bender P, et al. Advanced analysis of magnetic nanoflower measurements to leverage their use in biomedicine. Nanoscale Adv. 2021;3:1633–1645. doi: 10.1039/d0na00966k.
  • Niraula G, Mathpal MC, Herrera EZ, et al. Magnetic nanoflowers: synthesis, formation mechanism and hyperthermia application. In: Spinel nanoferrites. Cham: Springer; 2021. p. 129–166.
  • Dhiman N, Chaudhary S, Singh A, et al. Sustainable degradation of pharmaceutical waste using different fungal strains: enzyme induction, kinetics and isotherm studies. Environ Technol Innov. 2022;25:102156. doi: 10.1016/j.eti.2021.102156.
  • Xia Y-M, Zhang J-H, Xia M, et al. Peony-like magnetic graphene oxide/Fe3O4/BiOI nanoflower as a novel photocatalyst for enhanced photocatalytic degradation of rhodamine B and methylene blue dyes. J Mater Sci: mater Electron. 2020;31:1996–2009. doi: 10.1007/s10854-019-02719-6.
  • Subramani IG, Perumal V, Gopinath S, et al. Organic-inorganic hybrid nanoflower production and analytical utilization: fundamental to cutting-edge technologies. Crit Rev Anal Chem. 2022;52:1488–1510. doi: 10.1080/10408347.2021.1889962.
  • Nadar SS, Gawas SD, Rathod VK. Self-assembled organic–inorganic hybrid glucoamylase nanoflowers with enhanced activity and stability. Int J Biol Macromol. 2016;92:660–669. doi: 10.1016/j.ijbiomac.2016.06.071.
  • Nadar SS, Vaidya L, Rathod VK. Enzyme embedded metal organic framework (enzyme–MOF): de novo approaches for immobilization. Int J Biol Macromol. 2020;149:861–876. doi: 10.1016/j.ijbiomac.2020.01.240.
  • Ge J, Lei J, Zare RN. Protein–inorganic hybrid nanoflowers. Nat Nanotechnol. 2012;7:428–432. doi: 10.1038/nnano.2012.80.
  • Bilal M, Asgher M, Shah SZH, et al. Engineering enzyme-coupled hybrid nanoflowers: the quest for optimum performance to meet biocatalytic challenges and opportunities. Int J Biol Macromol. 2019;135:677–690. doi: 10.1016/j.ijbiomac.2019.05.206.
  • Li Y, Wu H, Su Z. Enzyme-based hybrid nanoflowers with high performances for biocatalytic, biomedical, and environmental applications. Coord Chem Rev. 2020;416:213342. doi: 10.1016/j.ccr.2020.213342.
  • Zhang M, Zhang Y, Yang C, et al. Enzyme-inorganic hybrid nanoflowers: classification, synthesis, functionalization and potential applications. Chem Eng J. 2021;415:129075. doi: 10.1016/j.cej.2021.129075.
  • Dube S, Rawtani D. Understanding intricacies of bioinspired organic-inorganic hybrid nanoflowers: a quest to achieve enhanced biomolecules immobilization for biocatalytic, biosensing and bioremediation applications. Adv Colloid Interface Sci. 2021;295:102484. doi: 10.1016/j.cis.2021.102484.
  • Tran TD, Kim MI. Organic-inorganic hybrid nanoflowers as potent materials for biosensing and biocatalytic applications. BioChip J. 2018;12:268–279. doi: 10.1007/s13206-018-2409-7.
  • Costa F d, Cipolatti EP, Furigo Junior A, et al. Nanoflowers: a new approach of enzyme immobilization. Chem Rec. 2022;22:e202100293. doi: 10.1002/tcr.202100293.
  • Nadar SS, Rathod VK. Magnetic-metal organic framework (magnetic-MOF): a novel platform for enzyme immobilization and nanozyme applications. Int J Biol Macromol. 2018;120:2293–2302. doi: 10.1016/j.ijbiomac.2018.08.126.
  • Salgaonkar M, Nadar SS, Rathod VK. Combi-metal organic framework (Combi-MOF) of α-amylase and glucoamylase for one pot starch hydrolysis. Int J Biol Macromol. 2018;113:464–475. doi: 10.1016/j.ijbiomac.2018.02.092.
  • Salgaonkar M, Nadar SS, Rathod VK. Biomineralization of orange peel peroxidase within metal organic frameworks (OPP–MOFs) for dye degradation. J. Environ. Chem. Eng. 2019;7:102969. doi: 10.1016/j.jece.2019.102969.
  • Nadar SS, Rathod VK. One pot synthesis of α-amylase metal organic framework (MOF)-sponge via dip-coating technique. Int J Biol Macromol. 2019;138:1035–1043. doi: 10.1016/j.ijbiomac.2019.07.099.
  • Šulek F, Fernández DP, Knez Ž, et al. Immobilization of horseradish peroxidase as cross-linked enzyme aggregates (CLEAs). Process Biochem. 2011;46:765–769. doi: 10.1016/j.procbio.2010.12.001.
  • Liang K, Ricco R, Doherty CM, et al. Biomimetic mineralization of metal-organic frameworks as protective coatings for biomacromolecules. Nat Commun. 2015;6:1–8. doi: 10.1038/ncomms8240.
  • Somturk B, Hancer M, Ocsoy I, et al. Synthesis of copper ion incorporated horseradish peroxidase-based hybrid nanoflowers for enhanced catalytic activity and stability. Dalton Trans. 2015;44:13845–13852. doi: 10.1039/c5dt01250c.
  • Han J, Luo P, Wang L, et al. Construction of magnetic nanoflower biocatalytic system with enhanced enzymatic performance by biomineralization and its application for bisphenol A removal. J Hazard Mater. 2019;380:120901. doi: 10.1016/j.jhazmat.2019.120901.
  • Mafra A, Ulrich CO, Kornecki LG, et al. Combi-CLEAs of glucose oxidase and catalase for conversion of glucose to gluconic acid eliminating the hydrogen peroxide to maintain enzyme activity in a bubble column reactor. Catalysts. 2019;9:657. doi: 10.3390/catal9080657.
  • Gascón V, Carucci C, Jiménez MB, et al. Rapid in situ immobilization of enzymes in metal–organic framework supports under mild conditions. ChemCatChem. 2017;9:1182–1186. doi: 10.1002/cctc.201601342.
  • Guo J, Wang Y, Zhao M. A self-activated nanobiocatalytic cascade system based on an enzyme-inorganic hybrid nanoflower for colorimetric and visual detection of glucose in human serum. Sensors Actuators B Chem. 2019;284:45–54. doi: 10.1016/j.snb.2018.12.102.
  • Cheon HJ, Adhikari MD, Chung M, et al. Magnetic nanoparticles-embedded enzyme-inorganic hybrid nanoflowers with enhanced peroxidase-like activity and substrate channeling for glucose biosensing. Adv Healthc Mater. 2019;8:1–8.
  • Rehman S, Bhatti HN, Bilal M, et al. Cross-linked enzyme aggregates (CLEAs) of Pencilluim notatum lipase enzyme with improved activity, stability and reusability characteristics. Int J Biol Macromol. 2016;91:1161–1169. doi: 10.1016/j.ijbiomac.2016.06.081.
  • He H, Han H, Shi H, et al. Construction of thermophilic lipase-embedded metal-organic frameworks via biomimetic mineralization: a biocatalyst for ester hydrolysis and kinetic resolution. ACS Appl Mater Interfaces. 2016;8:24517–24524. doi: 10.1021/acsami.6b05538.
  • Ke C, Fan Y, Chen Y, et al. A new lipase-inorganic hybrid nanoflower with enhanced enzyme activity. RSC Adv. 2016;6:19413–19416. doi: 10.1039/C6RA01564F.
  • Zhong L, Jiao X, Hu H, et al. Activated magnetic lipase-inorganic hybrid nanoflowers: a highly active and recyclable nanobiocatalyst for biodiesel production. Renew Energy. 2021;171:825–832. doi: 10.1016/j.renene.2021.02.155.
  • Kumar VV, Kumar MPP, Thiruvenkadaravi KV, et al. Preparation and characterization of porous cross linked laccase aggregates for the decolorization of triphenyl methane and reactive dyes. Bioresour Technol. 2012;119:28–34. doi: 10.1016/j.biortech.2012.05.078.
  • Samui A, Sahu SK. One-pot synthesis of microporous nanoscale metal organic frameworks conjugated with laccase as a promising biocatalyst. New J Chem. 2018;42:4192–4200. doi: 10.1039/C7NJ03619A.
  • Zhu P, Wang Y, Li G, et al. Preparation and application of a chemically modified laccase and copper phosphate hybrid flower-like biocatalyst. Biochem Eng J. 2019;144:235–243. doi: 10.1016/j.bej.2019.01.020.
  • Fu M, Xing J, Ge Z. Preparation of laccase-loaded magnetic nanoflowers and their recycling for efficient degradation of bisphenol A. Sci Total Environ. 2019;651:2857–2865. doi: 10.1016/j.scitotenv.2018.10.145.
  • Shcharbin D, Halets-Bui I, Abashkin V, et al. Hybrid metal-organic nanoflowers and their application in biotechnology and medicine. Colloids Surf B Biointerfaces. 2019;182:110354. doi: 10.1016/j.colsurfb.2019.110354.
  • Zhu J, Wen M, Wen W, et al. Recent progress in biosensors based on organic-inorganic hybrid nanoflowers. Biosens Bioelectron. 2018;120:175–187. doi: 10.1016/j.bios.2018.08.058.
  • Altinkaynak C, Tavlasoglu S, Ÿzdemir N, et al. A new generation approach in enzyme immobilization: organic-inorganic hybrid nanoflowers with enhanced catalytic activity and stability. Enzyme Microb Technol. 2016;93–94:105–112. doi: 10.1016/j.enzmictec.2016.06.011.
  • Cui J, Jia S. Organic – inorganic hybrid nanoflowers : a novel host platform for immobilizing biomolecules. Coord Chem Rev. 2017;352:249–263. doi: 10.1016/j.ccr.2017.09.008.
  • Lin Z, Xiao Y, Yin Y, et al. facile synthesis of enzyme-inorganic hybrid nanoflowers and its application as a colorimetric platform for visual detection of hydrogen peroxide and phenol. ACS Appl Mater Interfaces. 2014;6:10775–10782. doi: 10.1021/am502757e.
  • Sun J, Ge J, Liu W, et al. Multi-enzyme co-embedded organic-inorganic hybrid nanoflowers: synthesis and application as a colorimetric sensor. Nanoscale. 2014;6:255–262. doi: 10.1039/c3nr04425d.
  • Wang LB, Wang YC, He R, et al. A new nanobiocatalytic system based on allosteric effect with dramatically enhanced enzymatic performance. J Am Chem Soc. 2013;135:1272–1275. doi: 10.1021/ja3120136.
  • Zhang B, Chen J, Wang J, et al. Flower-like BSA/Zn3(PO4)2/Fe3O4 magnetic hybrid particles: preparation and application to adsorption of copper ions. J Chem Eng Data. 2018;63:3913–3922. doi: 10.1021/acs.jced.8b00544.
  • Wang X, Shi J, Li Z, et al. Facile one-pot preparation of chitosan/calcium pyrophosphate hybrid microflowers. ACS Appl Mater Interfaces. 2014;6:14522–14532. doi: 10.1021/am503787h.
  • Yin Y, Xiao Y, Lin G, et al. An enzyme-inorganic hybrid nanoflower based immobilized enzyme reactor with enhanced enzymatic activity. J Mater Chem B. 2015;3:2295–2300. doi: 10.1039/c4tb01697a.
  • Vaidya LB, Nadar SS, Rathod VK. Metal-organic frameworks (MOFs) for enzyme immobilization. In: Metal-organic frameworks for biomedical applications. Woodhead Publishing; 2020. p. 491–523.
  • Majewski MB, Howarth AJ, Li P, et al. Enzyme encapsulation in metal–organic frameworks for applications in catalysis. CrystEngComm. 2017;19:4082–4091. doi: 10.1039/C7CE00022G.
  • Hu Y, Dai L, Liu D, et al. Progress & prospect of metal-organic frameworks (MOFs) for enzyme immobilization (enzyme/MOFs). Renew Sustain Energy Rev. 2018;91:793–801. doi: 10.1016/j.rser.2018.04.103.
  • Li P, Modica JA, Howarth AJ, et al. Toward design rules for enzyme immobilization in hierarchical mesoporous metal-organic frameworks. Chem. 2016;1:154–169. doi: 10.1016/j.chempr.2016.05.001.
  • Mehta J, Bhardwaj N, Bhardwaj SK, et al. Recent advances in enzyme immobilization techniques: metal-organic frameworks as novel substrates. Coord Chem Rev. 2016;322:30–40. doi: 10.1016/j.ccr.2016.05.007.
  • Gkaniatsou E, Sicard C, Ricoux R, et al. Metal–organic frameworks: a novel host platform for enzymatic catalysis and detection. Mater Horiz. 2017;4:55–63. doi: 10.1039/C6MH00312E.
  • Bilal M, Zhao Y, Rasheed T, et al. Magnetic nanoparticles as versatile carriers for enzymes immobilization: a review. Int J Biol Macromol. 2018;120:2530–2544. doi: 10.1016/j.ijbiomac.2018.09.025.
  • Bilal M, Mehmood S, Rasheed T, et al. Bio-catalysis and biomedical perspectives of magnetic nanoparticles as versatile carriers. Magnetochemistry. 2019d;5:42. doi: 10.3390/magnetochemistry5030042.
  • Cheng Z, Chu X, Zhong H, et al. Synthesis of Fe3O4 nanoflowers by a simple and novel solvothermal process. Mater Lett. 2012;76:90–92. doi: 10.1016/j.matlet.2012.02.062.
  • Khosravi M, Azizian S. Synthesis of different nanostructured flower-like iron oxides and study of their performance as adsorbent. Adv Powder Technol. 2014;25:1578–1584. doi: 10.1016/j.apt.2014.05.010.
  • Lu C, Wang H, Ma J, et al. Facile synthesis of superparamagnetic magnetite nanoflowers and their applications in cellular imaging. RSC Adv. 2016;6:42649–42655. doi: 10.1039/C6RA06532E.
  • Bilal M, Asgher M, Cheng H, et al. Multi-point enzyme immobilization, surface chemistry, and novel platforms: a paradigm shift in biocatalyst design. Crit Rev Biotechnol. 2019;39:202–219. doi: 10.1080/07388551.2018.1531822.
  • Sun C, Lee JSH, Zhang M. Magnetic nanoparticles in MR imaging and drug delivery. Adv Drug Deliv Rev. 2008;60:1252–1265. doi: 10.1016/j.addr.2008.03.018.
  • Feng N, Zhang H, Li Y, et al. A novel catalytic material for hydrolyzing cow’s milk allergenic proteins: papain-Cu3(PO4)2·3H2O-magnetic nanoflowers. Food Chem. 2020;311:125911. doi: 10.1016/j.foodchem.2019.125911.
  • Fotiadou R, Patila M, Hammami MA, et al. Development of effective lipase-hybrid nanoflowers enriched with carbon and magnetic nanomaterials for biocatalytic transformations. Nanomaterials. 2019;9:808. doi: 10.3390/nano9060808.
  • Lee I, Cheon HJ, Adhikari MD, et al. Glucose oxidase-copper hybrid nanoflowers embedded with magnetic nanoparticles as an effective antibacterial agent. Int J Biol Macromol. 2020;155:1520–1531. doi: 10.1016/j.ijbiomac.2019.11.129.
  • Ren W, Li Y, Wang J, et al. Synthesis of magnetic nanoflower immobilized lipase and its continuous catalytic application. New J Chem. 2019;43:11082–11090. doi: 10.1039/C8NJ06429F.
  • Costa IO, Rios NS, Lima PJM, et al. Synthesis of organic-inorganic hybrid nanoflowers of lipases from Candida antarctica type B (CALB) and Thermomyces lanuginosus (TLL): improvement of thermal stability and reusability. Enzyme Microb Technol. 2023;163:110167. doi: 10.1016/j.enzmictec.2022.110167.
  • Cao G, Gao J, Zhou L, et al. Fabrication of Ni2+-nitrilotriacetic acid functionalized magnetic mesoporous silica nanoflowers for one pot purification and immobilization of His-tagged Ω-transaminase. Biochem Eng J. 2017;128:116–125. doi: 10.1016/j.bej.2017.09.019.
  • Rigoldi F, Donini S, Redaelli A, et al. Review: engineering of thermostable enzymes for industrial applications. APL Bioeng. 2018;2:011501.
  • Ansorge-Schumacher MB, Thum O. Immobilised lipases in the cosmetics industry. Chem Soc Rev. 2013;42:6475–6490. doi: 10.1039/c3cs35484a.
  • Hasan F, Shah AA, Hameed A. Industrial applications of microbial lipases. Enzyme Microb Technol. 2006;39:235–251. doi: 10.1016/j.enzmictec.2005.10.016.
  • Gao J, Kong W, Zhou L, et al. Monodisperse core-shell magnetic organosilica nanoflowers with radial wrinkle for lipase immobilization. Chem Eng J. 2017;309:70–79. doi: 10.1016/j.cej.2016.10.021.
  • Christy S, Noschese A, Lomeli-Rodriguez M, et al. Recent progress in the synthesis and applications of glycerol carbonate. Curr Opin Green Sustain Chem. 2018;14:99–107. doi: 10.1016/j.cogsc.2018.09.003.
  • Caro PD, Bandres M, Urrutigoïty M, et al. Recent progress in synthesis of glycerol carbonate and evaluation of its plasticizing properties. Front Chem. 2019;7:308. doi: 10.3389/fchem.2019.00308.
  • Sahani S, Upadhyay SN, Sharma YC. Critical review on production of glycerol carbonate from byproduct glycerol through transesterification. Ind Eng Chem Res. 2021;60:67–88. doi: 10.1021/acs.iecr.0c05011.
  • Du Y, Gao J, Kong W, et al. Enzymatic synthesis of glycerol carbonate using a lipase immobilized on magnetic organosilica nanoflowers as a catalyst. ACS Omega. 2018;3:6642–6650. doi: 10.1021/acsomega.8b00746.
  • Mathew GM, Raina D, Narisetty V, et al. Recent advances in biodiesel production: challenges and solutions. Sci Total Environ. 2021;794:148751. doi: 10.1016/j.scitotenv.2021.148751.
  • Pasha MK, Dai L, Liu D, et al. Biodiesel production with enzymatic technology: progress and perspectives. Biofuels, Bioprod Bioref. 2021;15:1526–1548. doi: 10.1002/bbb.2236.
  • Monteiro RRC, Virgen-Ortiz JJ, Berenguer-Murcia A, et al. Biotechnological relevance of the lipase A from Candida Antarctica. Catal Today. 2021;362:141–154. doi: 10.1016/j.cattod.2020.03.026.
  • Nadar SS, Rathod VK. Sonochemical effect on activity and conformation of commercial lipases. Appl Biochem Biotechnol. 2017;181:1435–1453. doi: 10.1007/s12010-016-2294-2.
  • Vaidya LB, Nadar SS, Rathod VK. Entrapment of surfactant modified lipase within zeolitic imidazolate framework (ZIF)-8. Int J Biol Macromol. 2020;146:678–686. doi: 10.1016/j.ijbiomac.2019.12.164.
  • Wan D, Yan C, Zhang Q. Facile and rapid synthesis of hollow magnetic mesoporous polydopamine nanoflowers with tunable pore structures for lipase immobilization: green production of biodiesel. Ind Eng Chem Res. 2019;58:16358–16369. doi: 10.1021/acs.iecr.9b02788.
  • Hwang ET, Gu MB. Enzyme stabilization by nano/microsized hybrid materials. Eng Life Sci. 2013;13:49–61. doi: 10.1002/elsc.201100225.
  • Bucur B, Munteanu F-D, Marty J-L, et al. Advances in enzyme-based biosensors for pesticide detection. Biosensors. 2018;8:27. doi: 10.3390/bios8020027.
  • Nadar SS, Patil PD, Tiwari MS, et al. Enzyme embedded microfluidic paper-based analytic device (μPAD): a comprehensive review. Crit Rev Biotechnol. 2021;41:1046–1080. doi: 10.1080/07388551.2021.1898327.
  • Hou C, Wang Y, Ding Q, et al. Facile synthesis of enzyme-embedded magnetic metal-organic frameworks as a reusable mimic multi-enzyme system: mimetic peroxidase properties and colorimetric sensor. Nanoscale. 2015;7:18770–18779. doi: 10.1039/c5nr04994f.
  • Alneyadi AH, Rauf MA, Ashraf SS. Oxidoreductases for the remediation of organic pollutants in water–a critical review. Crit Rev Biotechnol. 2018;38:971–988. doi: 10.1080/07388551.2017.1423275.
  • Alshabib M, Onaizi SA. A review on phenolic wastewater remediation using homogeneous and heterogeneous enzymatic processes: current status and potential challenges. Sep Purif Technol. 2019;219:186–207. doi: 10.1016/j.seppur.2019.03.028.
  • Sharma M, Akhter Y, Chatterjee S. A review on remediation of cyanide containing industrial wastes using biological systems with special reference to enzymatic degradation. World J Microbiol Biotechnol. 2019;35:1–14.
  • Abraham A, Chakraborty P. A review on sources and health impacts of bisphenol A. Rev Environ Health. 2020;35:201–210. doi: 10.1515/reveh-2019-0034.
  • Lassouane F, Aït-Amar H, Amrani S, et al. A promising laccase immobilization approach for bisphenol A removal from aqueous solutions. Bioresour Technol. 2019;271:360–367. doi: 10.1016/j.biortech.2018.09.129.
  • Bilal M, Iqbal HMN, Barceló D. Mitigation of bisphenol A using an array of laccase-based robust bio-catalytic cues–a review. Sci Total Environ. 2019;689:160–177. doi: 10.1016/j.scitotenv.2019.06.403.
  • Barylak M, Cendrowski K, Mijowska E. Application of carbonized metal–organic framework as efficient adsorbent of cationic dye. Ind Eng Chem Res. 2018;57:4867–4879. doi: 10.1021/acs.iecr.7b03790.
  • Trukawka M, Cendrowski K, Peruzynska M, et al. Carbonized metal–organic frameworks with trapped cobalt nanoparticles as biocompatible and efficient azo-dye adsorbent. Environ Sci Eur. 2019;31:15. doi: 10.1186/s12302-019-0242-9.
  • Routoula E, Patwardhan SV. Degradation of anthraquinone dyes from effluents: a review focusing on enzymatic dye degradation with industrial potential. Environ Sci Technol. 2020;54:647–664. doi: 10.1021/acs.est.9b03737.
  • Mishra S, Maiti A. Applicability of enzymes produced from different biotic species for biodegradation of textile dyes. Clean Techn Environ Policy. 2019;21:763–781. doi: 10.1007/s10098-019-01681-5.
  • Saravanan A, Kumar PS, Vo DN, et al. A review on catalytic-enzyme degradation of toxic environmental pollutants: microbial enzymes. J Hazard Mater. 2021;419:126451. doi: 10.1016/j.jhazmat.2021.126451.
  • Sun T, Fu M, Xing J, et al. Magnetic nanoparticles encapsulated laccase nanoflowers: evaluation of enzymatic activity and reusability for degradation of malachite green. Water Sci Technol. 2020;81:29–39. doi: 10.2166/wst.2020.068.
  • Mohammad M, Ahmadpoor F, Shojaosadati SA. Mussel-inspired magnetic nanoflowers as an effective nanozyme and antimicrobial agent for biosensing and catalytic reduction of organic dyes. ACS Omega. 2020;5:18766–18777. doi: 10.1021/acsomega.0c01864.
  • Bilal M, Hussain N, Américo-Pinheiro JHP, et al. Multi-enzyme co-immobilized nano-assemblies: bringing enzymes together for expanding bio-catalysis scope to meet biotechnological challenges. Int J Biol Macromol. 2021;186:735–749. doi: 10.1016/j.ijbiomac.2021.07.064.
  • Gul OT, Ocsoy I. Co-Enzymes based nanoflowers incorporated-magnetic carbon nanotubes: a new generation nanocatalyst for superior removal of cationic and anionic dyes with great repeated use. Environ Technol Innov. 2021;24:101992. doi: 10.1016/j.eti.2021.101992.
  • Taheri-Kafrani A, Kharazmi S, Nasrollahzadeh M, et al. Recent developments in enzyme immobilization technology for high-throughput processing in food industries. Crit Rev Food Sci Nutr. 2021;61:3160–3196. doi: 10.1080/10408398.2020.1793726.
  • Abdelaziz MH, Abdelwahab SF, Wan J, et al. Alternatively activated macrophages; a double-edged sword in allergic asthma. J Transl Med. 2020;18:1–12. doi: 10.1186/s12967-020-02251-w.
  • Dong X, Wang J, Raghavan V. Critical reviews and recent advances of novel non-thermal processing techniques on the modification of food allergens. Crit Rev Food Sci Nutr. 2021;61:196–210. doi: 10.1080/10408398.2020.1722942.
  • Marciniak A, Suwal S, Naderi N, et al. Enhancing enzymatic hydrolysis of food proteins and production of bioactive peptides using high hydrostatic pressure technology. Trends Food Sci Technol. 2018;80:187–198. doi: 10.1016/j.tifs.2018.08.013.
  • Ye M-L, Zhu Y, Lu Y, et al. Magnetic nanomaterials with unique nanozymes-like characteristics for colorimetric sensors: a review. Talanta. 2021;230:122299. doi: 10.1016/j.talanta.2021.122299.
  • Nguyen VD, Styevkó G, Madaras E, et al. Immobilization of β-galactosidase on chitosan-coated magnetic nanoparticles and its application for synthesis of lactulose-based galactooligosaccharides. Process Biochem. 2019;84:30–38. doi: 10.1016/j.procbio.2019.05.021.
  • Badoei-Dalfard A, Monemi F, Hassanshahian M. One-pot synthesis and biochemical characterization of a magnetic collagenase nanoflower and evaluation of its biotechnological applications. Colloids Surf B Biointerfaces. 2022;211:112302. doi: 10.1016/j.colsurfb.2021.112302.
  • Jiang D, Ni D, Rosenkrans ZT, et al. Nanozyme: new horizons for responsive biomedical applications. Chem Soc Rev. 2019;48:3683–3704. doi: 10.1039/c8cs00718g.
  • Wang H, Wan K, Shi X. Recent advances in nanozyme research. Adv Mater. 2019;31:1805368. doi: 10.1002/adma.201805368.
  • Wang Q, Wei H, Zhang Z, et al. Nanozyme: an emerging alternative to natural enzyme for biosensing and immunoassay. TrAC Trends Anal Chem. 2018;105:218–224. doi: 10.1016/j.trac.2018.05.012.
  • Zandieh M, Liu J. Nanozyme catalytic turnover and self-limited reactions. ACS Nano. 2021;15:15645–15655. doi: 10.1021/acsnano.1c07520.
  • Chi M, Zhu Y, Jing L, et al. Fabrication of oxidase-like polyaniline-MnO2 hybrid nanowires and their sensitive colorimetric detection of sulfite and ascorbic acid. Talanta. 2019;191:171–179. doi: 10.1016/j.talanta.2018.08.061.
  • Guan BY, Lu Y, Wang Y, et al. Porous iron–cobalt alloy/nitrogen‐doped carbon cages synthesized via pyrolysis of complex metal–organic framework hybrids for oxygen reduction. Adv Funct Mater. 2018;28:1706738. doi: 10.1002/adfm.201706738.
  • Wang S, Deng W, Yang L, et al. Copper-based metal–organic framework nanoparticles with peroxidase-like activity for sensitive colorimetric detection of Staphylococcus aureus. ACS Appl Mater Interfaces. 2017;9:24440–24445. doi: 10.1021/acsami.7b07307.
  • Li T, Wu Q, Wang W, et al. MOF-derived nano-popcorns synthesized by sonochemistry as efficient sensitizers for tumor microwave thermal therapy. Biomaterials. 2020;234:119773. doi: 10.1016/j.biomaterials.2020.119773.
  • Singh S. Nanomaterials exhibiting enzyme-like properties (nanozymes): current advances and future perspectives. Front Chem. 2019;7:46. doi: 10.3389/fchem.2019.00046.
  • He Z, Huang X, Wang C, et al. A catalase‐like metal‐organic framework nanohybrid for O2‐evolving synergistic chemoradiotherapy. Angew Chem. 2019;131:8844–8848. doi: 10.1002/ange.201902612.
  • Centeno MA, Ramírez Reina T, Ivanova S, et al. Au/CeO2 catalysts: structure and CO oxidation activity. Catalysts. 2016;6:158. doi: 10.3390/catal6100158.
  • Lei L, Zhang X, Su Y, et al. Metal–organic framework (MOF)-assisted construction of core–shell nanoflower-like CuO/CF@ NiCoMn–OH for high-performance supercapacitor. Energy Fuels. 2021;35:8387–8395. doi: 10.1021/acs.energyfuels.1c00540.
  • Le PG, Kim MI. Research progress and prospects of nanozyme-based glucose biofuel cells. Nanomaterials. 2021;11:2116. doi: 10.3390/nano11082116.
  • Golchin J, Golchin K, Alidadian N, et al. Nanozyme applications in biology and medicine: an overview. Artif Cells Nanomed Biotechnol. 2017;45:1–8. doi: 10.1080/21691401.2017.1313268.
  • Sun H, Zhou Y, Ren J, et al. Carbon nanozymes: enzymatic properties, catalytic mechanism, and applications. Angew Chem Int Ed Engl. 2018;57:9224–9237. doi: 10.1002/anie.201712469.
  • Chen X, Xianfeng W, Gaihua C, et al. Colorimetric and fluorescent dual-identification of glutathione based on its inhibition on the 3D ball-flower shaped Cu-hemin-MOF’s peroxidase-like activity. Microchim Acta. 2020;187:1–10. doi: 10.1007/s00604-020-04565-4.
  • Liu X, Yan L, Ren H, et al. Facile synthesis of magnetic hierarchical flower-like Co3O4 spheres: mechanism, excellent tetra-enzyme mimics and their colorimetric biosensing applications. Biosens Bioelectron. 2020;165:112342. doi: 10.1016/j.bios.2020.112342.
  • Attar F, Shahpar MG, Rasti B, et al. Nanozymes with intrinsic peroxidase-like activities. J Mol Liq. 2019;278:130–144. doi: 10.1016/j.molliq.2018.12.011.
  • Lu J, Hu Y, Wang P, et al. Electrochemical biosensor based on gold nanoflowers-encapsulated magnetic metal-organic framework nanozymes for drug evaluation with in-situ monitoring of H2O2 released from H9C2 cardiac cells. Sensors Actuators B Chem. 2020;311:127909. doi: 10.1016/j.snb.2020.127909.
  • Li X, Wang L, Du D, et al. Emerging applications of nanozymes in environmental analysis: opportunities and trends. TrAC Trends Anal Chem. 2019;120:115653. doi: 10.1016/j.trac.2019.115653.
  • Meng Y, Li W, Pan X, et al. Applications of nanozymes in the environment. Environ Sci. 2020;7:1305–1318. doi: 10.1039/C9EN01089K.
  • Xiong Y, Chen S, Ye F, et al. Preparation of magnetic core–shell nanoflower Fe 3 O 4@ MnO 2 as reusable oxidase mimetics for colorimetric detection of phenol. Anal Methods. 2015;7:1300–1306. doi: 10.1039/C4AY02687J.

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