539
Views
3
CrossRef citations to date
0
Altmetric
Original Research

Horseradish Peroxidase-Functionalized Gold Nanoconjugates for Breast Cancer Treatment Based on Enzyme Prodrug Therapy

, , ORCID Icon, , , & show all
Pages 409-422 | Published online: 26 Jan 2022

References

  • Globocan. Estimated number of new cases in 2018, worldwide, all cancers, females, all ages. Glob Scan. 2018;849:2018.
  • Globocan. Estimated number of deaths in 2018, worldwide, all cancers, males, all ages. Glob Scan. 2018;947:2018.
  • Cardoso F, Kyriakides S, Ohno S, et al. Early breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2019;30(8):1194–1220. doi:10.1093/annonc/mdz173
  • Partridge AH, Burstein HJ, Winer EP. Side effects of chemotherapy and combined chemohormonal therapy in women with early-stage breast cancer. J Natl Cancer Inst Monogr. 2001;334(30):135–142. doi:10.1093/oxfordjournals.jncimonographs.a003451
  • Maeda H. The tumor blood vessel as an ideal target for macromolecular anticancer agents. J Control Release. 1992;19(1–3):315–324. doi:10.1016/0168-3659(92)90086-7
  • Matsumura Y, Maeda H, New A. Concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 1986;46(8):6387–6392.
  • Sarkar S, Konar S, Prasad PN, et al. Micellear gold nanoparticles as delivery vehicles for dual tyrosine kinase inhibitor ZD6474 for metastatic breast cancer treatment. Langmuir. 2017;33(31):7649–7659. doi:10.1021/acs.langmuir.7b01072
  • Tran P, Lee S-E, Kim D-H, Pyo Y-C, Park J-S. Recent advances of nanotechnology for the delivery of anticancer drugs for breast cancer treatment. J Pharm Investig. 2020;50(3):261–270. doi:10.1007/s40005-019-00459-7
  • Ensor CM, Holtsberg FW, Bomalaski JS, Clark MA. Pegylated arginine deiminase (ADI-SS PEG20,000 mw) inhibits human melanomas and hepatocellular carcinomas in vitro and in vivo. Cancer Res. 2002;62(19):5443–5450.
  • Avramis VI, Sencer S, Periclou AP, et al. A randomized comparison of native Escherichia coli asparaginase and polyethylene glycol conjugated asparaginase for treatment of children with newly diagnosed standard-risk acute lymphoblastic leukemia: a Children’s Cancer Group study. Blood. 2002;99(6):1986–1994. doi:10.1182/blood.v99.6.1986
  • Schellmann N, Deckert PM, Bachran D, Fuchs H, Bachran C. Targeted enzyme prodrug therapies. Mini Rev Med Chem. 2010;10(10):887–904. doi:10.2174/138955710792007196
  • Xu G, Mcleod HL. Strategies for enzyme/prodrug cancer therapy. Clin Cancer Res. 2001;7:3314–3324.
  • Sharma SK, Bagshawe KD, Melton RG, Sherwood RF. Human immune response to monoclonal antibody-enzyme conjugates in ADEPT pilot clinical trial. Cell Biophys. 1992;21(1–3):109–120. doi:10.1007/BF02789482
  • Francis RJ, Sharma SK, Springer C, et al. A Phase I trial of antibody directed enzyme prodrug therapy (ADEPT) in patients with advanced colorectal carcinoma or other CEA producing tumours. Br J Cancer. 2002;87(6):600–607. doi:10.1038/sj.bjc.6600517
  • Mayer A, Francis RJ, Sharma SK, et al. A Phase I study of single administration of antibody-directed enzyme prodrug therapy with the recombinant anti–carcinoembryonic antigen antibody-enzyme fusion protein MFECP1 and a bis-iodo phenol mustard prodrug. Clin Cancer Res. 2006;12(21):6509LP- 6516. doi:10.1158/1078-0432.CCR-06-0769
  • Cloughesy TF, Landolfi J, Hogan DJ, et al. Phase 1 trial of vocimagene amiretrorepvec and 5-fluorocytosine for recurrent high-grade glioma. Sci Transl Med. 2016;8(341):1–23. doi:10.1126/scitranslmed.aad9784
  • Ji N, Weng D, Liu C, et al. Adenovirus-mediated delivery of herpes simplex virus thymidine kinase administration improves outcome of recurrent high-grade glioma. Oncotarget. 2016;7(4):4369–4378. doi:10.18632/oncotarget.6737
  • Niculescu-Duvaz I, Spooner R, Marais R, Springer CJ. Gene-directed enzyme prodrug therapy. Bioconjug Chem. 1998;9(1):4–22. doi:10.1021/bc970116t
  • Huysmans G, Ranquin A, Wyns L, Steyaert J, Van Gelder P. Encapsulation of therapeutic nucleoside hydrolase in functionalised nanocapsules. J Control Release. 2005;102(1):171–179. doi:10.1016/j.jconrel.2004.10.002
  • Chandrawati R, Olesen MTJ, Marini TCC, et al. Enzyme prodrug therapy engineered into electrospun fibers with embedded liposomes for controlled, localized synthesis of therapeutics. Adv Healthc Mater. 2017;6(17):1700385. doi:10.1002/adhm.201700385
  • Satchi-Fainaro R, Hailu H, Davies JW, Summerford C, Duncan R. PDEPT: polymer-directed enzyme prodrug therapy. 2. HPMA Copolymer-β-lactamase and HPMA Copolymer-C-Dox as a model combination. Bioconjug Chem. 2003;14(4):797–804. doi:10.1021/bc020091k
  • Nishimura T, Sasaki Y, Akiyoshi K. Biotransporting self-assembled nanofactories using polymer vesicles with molecular permeability for enzyme prodrug cancer therapy. Adv Mater. 2017;29(36):1702406. doi:10.1002/adma.201702406
  • Gupta N, Gupta C, Sharma S, Rathi B, Sharma RK, Bohidar HB. Magnetic iron oxide nanoparticles encapsulating horseradish peroxidase (HRP): synthesis, characterization and carrier for the generation of free radicals for potential applications in cancer therapy. RSC Adv. 2016;6(112):111099–111108. doi:10.1039/C6RA24586B
  • Zhou J, Hou J, Rao J, Zhou C, Liu Y, Gao W. Magnetically directed enzyme/prodrug prostate cancer therapy based on β-Glucosidase/Amygdalin. Int J Nanomedicine. 2020;15:4639–4657. doi:10.2147/IJN.S242359
  • Llopis-Lorente A, Garciá-Fernández A, Murillo-Cremaes N, et al. Enzyme-powered gated mesoporous silica nanomotors for on-command intracellular payload delivery. ACS Nano. 2019;13(10):12171–12183. doi:10.1021/acsnano.9b06706
  • Llopis-Lorente A, de Luis B, García-Fernández A, et al. Au–Mesoporous silica nanoparticles gated with disulfide-linked oligo(ethylene glycol) chains for tunable cargo delivery mediated by an integrated enzymatic control unit. J Mater Chem B. 2017;5(33):6734–6739. doi:10.1039/C7TB02045G
  • Wang Z, Chen L, Chu Z, Huang C, Huang Y, Jia N. Gemcitabine-loaded gold nanospheres mediated by albumin for enhanced anti-tumor activity combining with CT imaging. Mater Sci Eng C. 2018;89:106–118. doi:10.1016/j.msec.2018.03.025
  • Iranpour P, Ajamian M, Safavi A, Iranpoor N, Abbaspour A, Javanmardi S. Synthesis of highly stable and biocompatible gold nanoparticles for use as a new X-ray contrast agent. J Mater Sci Mater Med. 2018;29(5):48. doi:10.1007/s10856-018-6053-5
  • Ghahremani F, Kefayat A, Shahbazi-Gahrouei D, Motaghi H, Mehrgardi MA, Haghjooy-Javanmard S. AS1411 aptamer-targeted gold nanoclusters effect on the enhancement of radiation therapy efficacy in breast tumor-bearing mice. Nanomedicine. 2018;13(20):2563–2578. doi:10.2217/nnm-2018-0180
  • Bailly AL, Correard F, Popov A, et al. In vivo evaluation of safety, biodistribution and pharmacokinetics of laser-synthesized gold nanoparticles. Sci Rep. 2019;9(1):1–12. doi:10.1038/s41598-019-48748-3
  • Brust M, Walker M, Bethell D, Schiffrin DJ, Whyman R. Synthesis of thiol-derivatised gold nanoparticles in a two-phase Liquid–Liquid system. J Chem Soc Chem Commun. 1994;(7):801–802. doi:10.1039/C39940000801
  • Jana NR, Gearheart L, Murphy CJ. Seeding growth for size control of 5-40 nm diameter gold nanoparticles. Langmuir. 2001;17(22):6782–6786. doi:10.1021/la0104323
  • Perrault SD, Chan WCW. Synthesis and surface modification of highly monodispersed, spherical gold nanoparticles of 50-200 nm. J Am Chem Soc. 2009;131(47):17042–17043. doi:10.1021/ja907069u
  • Grzelczak M, Pérez-Juste J, Mulvaney P, Liz-Marzán LM. Shape control in gold nanoparticle synthesis. Chem Soc Rev. 2008;37(9):1783–1791. doi:10.1039/b711490g
  • Pérez-Calabuig AM, Díez P, Martínez-Ruiz P, Martínez-Máñez R, Sánchez A, Villalonga R. An enzyme-controlled Janus nanomachine for on-command dual and sequential release. Chem Commun. 2020;56(47):6440–6443. doi:10.1039/D0CC01234C
  • Akbarzadeh Khiavi M, Safary A, Aghanejad A, et al. Enzyme-conjugated gold nanoparticles for combined enzyme and photothermal therapy of colon cancer cells. Colloids Surfaces a Physicochem Eng Asp. 2019;572:333–344. doi:10.1016/j.colsurfa.2019.04.019
  • Sendra L, Miguel A, Navarro-Plaza MC, et al. Gold nanoparticle-assisted virus formation by means of the delivery of an oncolytic adenovirus genome. Nanomater. 2020;10(6):1183. doi:10.3390/nano10061183
  • Ramchandani D, Lee SK, Yomtoubian S, Han MS, Tung C-H, Mittal V. Nanoparticle delivery of miR-708 mimetic impairs breast cancer metastasis. Mol Cancer Ther. 2019;18(3):579 LP- 591. doi:10.1158/1535-7163.MCT-18-0702
  • Liu Y, Yang M, Zhang J, et al. Human induced pluripotent stem cells for tumor targeted delivery of gold nanorods and enhanced photothermal therapy. ACS Nano. 2016;10(2):2375–2385. doi:10.1021/acsnano.5b07172
  • Cai Z, Chattopadhyay N, Yang K, et al. 111In-labeled trastuzumab-modified gold nanoparticles are cytotoxic in vitro to HER2-positive breast cancer cells and arrest tumor growth in vivo in athymic mice after intratumoral injection. Nucl Med Biol. 2016;43(12):818–826. doi:10.1016/j.nucmedbio.2016.08.009
  • Abdolahinia ED, Nadri S, Rahbarghazi R, Barar J, Aghanejad A, Omidi Y. Enhanced penetration and cytotoxicity of metformin and collagenase conjugated gold nanoparticles in breast cancer spheroids. Life Sci. 2019;231:116545. doi:10.1016/j.lfs.2019.116545
  • Dreaden EC, Mwakwari SC, Sodji QH, Oyelere AK, El-Sayed MA. Tamoxifen−Poly(ethylene glycol)−thiol gold nanoparticle conjugates: enhanced potency and selective delivery for breast cancer treatment. Bioconjug Chem. 2009;20(12):2247–2253. doi:10.1021/bc9002212
  • Hernández Montoto A, Montes R, Samadi A, et al. Gold nanostars coated with mesoporous silica are effective and nontoxic photothermal agents capable of gate keeping and laser-induced drug release. ACS Appl Mater Interfaces. 2018;10(33):27644–27656. doi:10.1021/acsami.8b08395
  • Hernández Montoto A, Llopis-Lorente A, Gorbe M, et al. Janus gold nanostars–mesoporous silica nanoparticles for NIR-light-triggered drug delivery. Chem – a Eur J. 2019;25(36):8471–8478. doi:10.1002/chem.201900750
  • de Luis B, Morellá-Aucejo Á, Llopis-Lorente A, et al. A chemical circular communication network at the nanoscale. Chem Sci. 2021;12(4):1551–1559. doi:10.1039/D0SC04743K
  • de Luis B, Llopis-Lorente A, Rincón P, et al. An interactive model of communication between abiotic nanodevices and microorganisms. Angew Chemie Int Ed. 2019;58(42):14986–14990. doi:10.1002/anie.201908867
  • Llopis-Lorente A, Díez P, Sánchez A, et al. Interactive models of communication at the nanoscale using nanoparticles that talk to one another. Nat Commun. 2017;8:15511. doi:10.1038/ncomms15511
  • Li D, He Q, Cui Y, Duan L, Li J. Immobilization of glucose oxidase onto gold nanoparticles with enhanced thermostability. Biochem Biophys Res Commun. 2007;355(2):488–493. doi:10.1016/j.bbrc.2007.01.183
  • Shikha S, Thakur KG, Bhattacharyya MS. Facile fabrication of lipase to amine functionalized gold nanoparticles to enhance stability and activity. RSC Adv. 2017;7(68):42845–42855. doi:10.1039/C7RA06075K
  • Wu C-S, Wu C-T, Yang Y-S, Ko F-H. An enzymatic kinetics investigation into the significantly enhanced activity of functionalized gold nanoparticles. Chem Commun. 2008;(42):5327–5329. doi:10.1039/B810889G
  • Lan D, Li B, Zhang Z. Chemiluminescence flow biosensor for glucose based on gold nanoparticle-enhanced activities of glucose oxidase and horseradish peroxidase. Biosens Bioelectron. 2008;24(4):934–938. doi:10.1016/j.bios.2008.07.064
  • Veitch NC. Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry. 2004;65(3):249–259. doi:10.1016/j.phytochem.2003.10.022
  • Krainer FW, Glieder A. An updated view on horseradish peroxidases: recombinant production and biotechnological applications. Appl Microbiol Biotechnol. 2015;99(4):1611–1625. doi:10.1007/s00253-014-6346-7
  • Bonifert G, Folkes L, Gmeiner C, Dachs G, Spadiut O. Recombinant horseradish peroxidase variants for targeted cancer treatment. Cancer Med. 2016;5(6):1194–1203. doi:10.1002/cam4.668
  • Tupper J, Greco O, Tozer GM, Dachs GU. Analysis of the horseradish peroxidase/indole-3-acetic acid combination in a three dimensional tumor model. Cancer Gene Ther. 2004;11(7):508–513. doi:10.1038/sj.cgt.7700713
  • Dai M, Liu J, Chen DE, et al. Tumor-targeted gene therapy using Adv-AFP-HRPC/IAA prodrug system suppresses growth of hepatoma xenografted in mice. Cancer Gene Ther. 2012;19(2):77–83. doi:10.1038/cgt.2011.65
  • Tupper J, Stratford MR, Hill S, Tozer GM, Dachs GU. In vivo characterization of horseradish peroxidase with indole-3-acetic acid and 5-bromoindole-3-acetic acid for gene therapy of cancer. Cancer Gene Ther. 2010;17(6):420–428. doi:10.1038/cgt.2009.86
  • Bennett MJ, Marchant A, May ST, Swarup R. Going the distance with auxin: unravelling the molecular basis of auxin transport. Philos Trans R Soc B Biol Sci. 1998;353(1374):1511–1515. doi:10.1098/rstb.1998.0306
  • Diengott I-AM, Diengott D. Hypoglycemic action of indole-3-acetic acid by mouth in patients with diabetes mellitus. Proc Soc Exp Biol Med. 1956;93(1):109–110. doi:10.3181/00379727-93-22678
  • Ryšánek K, Vítek V. Increased excretion of 5-hydroxy-indole-acetic acid after the administration of 3-indole-acetic acid (heteroauxine). Experientia. 1959;15(6):217–218. doi:10.1007/BF02158112
  • Kim D-S, Kim S-Y, Jeong Y-M, et al. Indole-3-acetic acid/horseradish peroxidase-induced apoptosis involves cell surface CD95 (Fas/APO-1) expression. Biol & Pharm Bull. 2006;29(8):1625–1629. doi:10.1248/bpb.29.1625
  • Jeong YM, Oh MH, Kim SY, et al. Indole-3-acetic acid/horseradish peroxidase induces apoptosis in TCCSUP human urinary bladder carcinoma cells. Pharmazie. 2010;65(2):122–126. doi:10.1691/ph.2010.9715
  • Turkevich J, Stevenson PC, Hillier J. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss Faraday Soc. 1951;11:55–75. doi:10.1039/DF9511100055
  • Frens G. Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nat Phys Sci. 1973;241(105):20–22. doi:10.1038/physci241020a0
  • Keesey J. Biochemica Information. In: Biochemica Information. Boehringer Mannheim Biochemicals; 1987:58.
  • Pütter J, Becker R. Methods of enzymatic analysis. Bergmeyer H-UI, editor. Methods of Enzymatic Analysis. 3rd ed. Vol. III: Verlag Chemie; 1974:286–293.
  • Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA. Spheroid-based drug screen: considerations and practical approach. Nat Protoc. 2009;4(3):309–324. doi:10.1038/nprot.2008.226
  • Ivascu A, Kubbies M. Rapid generation of single-tumor spheroids for high-throughput cell function and toxicity analysis. J Biomol Screen. 2006;11(8):922–932. doi:10.1177/1087057106292763
  • Kim D-S, Jeon S-E, Jeong Y-M, Kim S-Y, Kwon S-B, Park K-C. Hydrogen peroxide is a mediator of indole-3-acetic acid/horseradish peroxidase-induced apoptosis. FEBS Lett. 2006;580(5):1439–1446. doi:10.1016/j.febslet.2006.01.073
  • Kim DS, Jeon SE, Park KC. Oxidation of indole-3-acetic acid by horseradish peroxidase induces apoptosis in G361 human melanoma cells. Cell Signal. 2004;16(1):81–88. doi:10.1016/S0898-6568(03)00091-3
  • Rodrigues RC, Ortiz C, Berenguer-Murcia Á, Torres R, Fernández-Lafuente R. Modifying enzyme activity and selectivity by immobilization. Chem Soc Rev. 2013;42(15):6290–6307. doi:10.1039/c2cs35231a
  • Kang T, Kim YG, Kim D, Hyeon T. Inorganic nanoparticles with enzyme-mimetic activities for biomedical applications. Coord Chem Rev. 2020;403:213092. doi:10.1016/j.ccr.2019.213092
  • Wang S, Chen W, Liu A-L, Hong L, Deng -H-H, Lin X-H. Comparison of the peroxidase-like activity of unmodified, amino-modified, and citrate-capped gold nanoparticles. Chemphyschem. 2012;13(5):1199–1204. doi:10.1002/cphc.201100906
  • Gao L, Liu M, Ma G, et al. Peptide-conjugated gold nanoprobe: intrinsic nanozyme-linked immunsorbant assay of integrin expression level on cell membrane. ACS Nano. 2015;9(11):10979–10990. doi:10.1021/acsnano.5b04261
  • Lou D, Tian Y, Zhang Y, et al. Peroxidase-like activity of gold nanoparticles and their gold staining enhanced ELISA application. J Nanosci Nanotechnol. 2018;18(2):951–958. doi:10.1166/jnn.2018.13977
  • Reis-Filho JS, Pusztai L. Gene expression profiling in breast cancer: classification, prognostication, and prediction. Lancet. 2011;378(9805):1812–1823. doi:10.1016/S0140-6736(11)61539-0
  • Balfourier A, Luciani N, Wang G, et al. Unexpected intracellular biodegradation and recrystallization of gold nanoparticles. Proc Natl Acad Sci U S A. 2020;117(1):103–113. doi:10.1073/pnas.1911734116
  • Yan X, Blacklock J, Li J, Möhwald H. One-pot synthesis of polypeptide–gold nanoconjugates for in vitro gene transfection. ACS Nano. 2012;6(1):111–117. doi:10.1021/nn202939s
  • Mukherjee S, Dasari M, Priyamvada S, Kotcherlakota R, Bollu VS, Patra CR. A green chemistry approach for the synthesis of gold nanoconjugates that induce the inhibition of cancer cell proliferation through induction of oxidative stress and their in vivo toxicity study. J Mater Chem B. 2015;3(18):3820–3830. doi:10.1039/C5TB00244C
  • Poulsen AK, Scharff-Poulsen AM, Olsen LF. Horseradish peroxidase embedded in polyacrylamide nanoparticles enables optical detection of reactive oxygen species. Anal Biochem. 2007;366(1):29–36. doi:10.1016/j.ab.2007.04.004
  • Sohrabi N, Rasouli N, Torkzadeh M. Enhanced stability and catalytic activity of immobilized α-amylase on modified Fe3O4 nanoparticles. Chem Eng J. 2014;240:426–433. doi:10.1016/j.cej.2013.11.059
  • Lu H, Stenzel MH. Multicellular tumor spheroids (MCTS) as a 3D in vitro evaluation tool of nanoparticles. Small. 2018;14(13):1702858. doi:10.1002/smll.201702858
  • Hung BY, Kuthati Y, Kankala RK, et al. Utilization of enzyme-immobilized mesoporous silica nanocontainers (IBN-4) in prodrug-activated cancer theranostics. Nanomaterials. 2015;5(4):2169–2191. doi:10.3390/nano5042169
  • Chang F-P, Hung Y, Chang J-H, Lin C-H, Mou C-Y. Enzyme encapsulated hollow silica nanospheres for intracellular biocatalysis. ACS Appl Mater Interfaces. 2014;6(9):6883–6890. doi:10.1021/am500701c
  • Chiu Y-R, Ho W-J, Chao J-S, Yuan C-J. Enzyme-encapsulated silica nanoparticle for cancer chemotherapy. J Nanoparticle Res. 2012;14(4):829. doi:10.1007/s11051-012-0829-1
  • Cao X, Chen C, Yu H, Wang P. Horseradish peroxidase-encapsulated chitosan nanoparticles for enzyme-prodrug cancer therapy. Biotechnol Lett. 2015;37(1):81–88. doi:10.1007/s10529-014-1664-5