Abstract
The interaction of nanoparticles with the biological system has increased with the increasing popularity of nanomedicines. Red blood cells (RBCs) are very sensitive, and abundant cells in the blood. They are highly prone to oxidative damage due to constant interaction with oxygen itself, foreign particles in the blood, and the lack of repair mechanism. The cell membrane of RBCs undergoes lipid peroxidation, protein oxidation, and heme degradation which results in altered membrane permeability, changes in the morphology, and functioning of RBCs. The nanoparticles induce oxidative stress, hemolysis, morphological changes, membrane deformability, and alterations in hemoglobin structure in RBCs. In this review, the effects of metallic nanoparticles and their modifications on the physiology, and life span of RBCs are discussed. The detailed analysis of the antioxidant enzymes-like activity of metal nanoparticles is expected to highlight the beneficial use of these metal nanoparticles in RBCs against oxidative stress and the development of new biosafe nanodrugs.
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Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ (2010) Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 242(3):263–269. https://doi.org/10.1016/j.taap.2009.10.016
Alizadeh N, Salimi A (2021) Multienzymes activity of metals and metal oxide nanomaterials: applications from biotechnology to medicine and environmental engineering. J Nanobiotechnology 19(1):26–26. https://doi.org/10.1186/s12951-021-00771-1
Baccarin T, Mitjans M, Lemos-Senna E, Vinardell MP (2015) Protection against oxidative damage in human erythrocytes and preliminary photosafety assessment of Punica granatum seed oil nanoemulsions entrapping polyphenol-rich ethyl acetate fraction. Toxicology in Vitro 30 (1, Part B):421–428. doi:https://doi.org/10.1016/j.tiv.2015.09.020
Baldim V, Yadav N, Bia N, Graillot A, Loubat C, Singh S, Karakoti AS, Berret J-F (2020) Polymer-coated cerium oxide nanoparticles as oxidoreductase-like catalysts. ACS Appl Mater Interfaces 12(37):42056–42066. https://doi.org/10.1021/acsami.0c08778
Barbero F, Russo L, Vitali M, Piella J, Salvo I, Borrajo ML, Busquets-Fité M, Grandori R, Bastús NG, Casals E, Puntes V (2017) Formation of the Protein Corona: The Interface between Nanoparticles and the Immune System. Semin Immunol 34:52–60. https://doi.org/10.1016/j.smim.2017.10.001
Barkur S, Lukose J, Chidangil S (2020) Probing Nanoparticle-cell interaction using micro-Raman spectroscopy: silver and gold nanoparticle-induced stress effects on optically trapped live red blood cells. ACS Omega 5(3):1439–1447. https://doi.org/10.1021/acsomega.9b02988
Berrecoso G, Crecente-Campo J, Alonso MJ (2020) Unveiling the pitfalls of the protein corona of polymeric drug nanocarriers. Drug Deliv Transl Res 10(3):730–750. https://doi.org/10.1007/s13346-020-00745-0
Bhagat S, Singh S (2020) Co-delivery of AKT3 siRNA and PTEN plasmid by antioxidant nanoliposomes for enhanced antiproliferation of prostate cancer cells. ACS Appl Bio Mater 3(7):3999–4011. https://doi.org/10.1021/acsabm.9b01016
Chen F, Liu Y, Wong N-K, Xiao J, So K-F (2017) Oxidative stress in stem cell aging. Cell Transplant 26(9):1483–1495. https://doi.org/10.1177/0963689717735407
Deshmukh AR, Aloui H, Kim BS (2021) Novel biogenic gold nanoparticles catalyzing multienzyme cascade reaction: glucose oxidase and peroxidase mimicking activity. Chem Eng J 421:127859. https://doi.org/10.1016/j.cej.2020.127859
Dias A, Werner M, Ward KR, Fleury J-B, Baulin VA (2019) High-throughput 3D visualization of nanoparticles attached to the surface of red blood cells. Nanoscale 11(5):2282–2288. https://doi.org/10.1039/C8NR09960J
Eskandari N, Nejadi Babadaei MM, Nikpur S, Ghasrahmad G, Attar F, Heshmati M, Akhtari K, Rezayat Sorkhabadi SM, Mousavi SE, Falahati M (2018) Biophysical, docking, and cellular studies on the effects of cerium oxide nanoparticles on blood components: in vitro. Int J Nanomedicine 13:4575–4589. https://doi.org/10.2147/IJN.S172162
Gao L, Zhuang J, Nie L, Zhang J, Zhang Y, Gu N, Wang T, Feng J, Yang D, Perrett S, Yan X (2007) Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nat Nanotechnol 2(9):577–583. https://doi.org/10.1038/nnano.2007.260
Ghaffari S (2008) Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid Redox Signal 10(11):1923–1940. https://doi.org/10.1089/ars.2008.2142
Guo S, Guo L (2019) Unraveling the multi-enzyme-like activities of iron oxide nanozyme via a first-principles microkinetic study. J Phys Chem C 123(50):30318–30334. https://doi.org/10.1021/acs.jpcc.9b07802
Hameed MK, Ahmady IM, Alawadhi H, Workie B, Sahle-Demessie E, Han C, Chehimi MM, Mohamed AA (2018) Gold-carbon nanoparticles mediated delivery of BSA: Remarkable robustness and hemocompatibility. Colloids Surf, A 558:351–358. https://doi.org/10.1016/j.colsurfa.2018.09.004
He Z, Huang X, Wang C, Li X, Liu Y, Zhou Z, Wang S, Zhang F, Wang Z, Jacobson O, Zhu J-J, Yu G, Dai Y, Chen X (2019) A catalase-like metal-organic framework nanohybrid for O2-evolving synergistic chemoradiotherapy. Angew Chem Int Ed 58(26):8752–8756. https://doi.org/10.1002/anie.201902612
Hirst SM, Karakoti A, Singh S, Self W, Tyler R, Seal S, Reilly CM (2013) Bio-distribution and in vivo antioxidant effects of cerium oxide nanoparticles in mice. Environ Toxicol 28(2):107–118. https://doi.org/10.1002/tox.20704
Huang Y, Jiang J, Wang Y, Chen J, Xi J (2021) Nanozymes as Enzyme Inhibitors. Int J Nanomedicine 16:1143–1155. https://doi.org/10.2147/IJN.S294871
Iofrida C, Daniele S, Pietrobono D, Fusi J, Galetta F, Trincavelli ML, Bonuccelli U, Franzoni F, Martini C (2017) Influence of physical exercise on β-amyloid, α-synuclein and tau accumulation: an in vitro model of oxidative stress in human red blood cells. Arch Ital Biol 155(1–2):33–42. https://doi.org/10.12871/000398292017124
Kotsuruba AV, Kopyak BS, Sagach VF, Spivak MY (2016) Nanocerium restores erythrocyte stability to acid hemolysis by inhibition of oxygen and nitrogen reactive species in old rats. Int J Physiol Pathophysiol 7(1):41–49. https://doi.org/10.1615/IntJPhysPathophys.v7.i1.50
Kozelskaya AI, Panin AV, Khlusov IA, Mokrushnikov PV, Zaitsev BN, Kuzmenko DI, Vasyukov GY (2016) Morphological changes of the red blood cells treated with metal oxide nanoparticles. Toxicol in Vitro 37:34–40. https://doi.org/10.1016/j.tiv.2016.08.012
Kuhn V, Diederich L, Keller TCSt, Kramer CM, Lückstädt W, Panknin C, Suvorava T, Isakson BE, Kelm M, Cortese-Krott MM, (2017) Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism. Anemia Antioxid Redox Signal 26(13):718–742. https://doi.org/10.1089/ars.2016.6954
Kumar N, Kant R, Maurya PK, Rizvi SI (2012) Concentration dependent effect of (−)-Epicatechin on Na+/K+-ATPase and Ca2+-ATPase inhibition induced by free radicals in hypertensive patients: comparison with L-ascorbic acid. Phytother Res 26(11):1644–1647. https://doi.org/10.1002/ptr.4624
Kumar S, Jha I, Mogha NK, Venkatesu P (2020) Biocompatibility of surface-modified gold nanoparticles towards red blood cells and haemoglobin. Appl Surf Sci 512:145573. https://doi.org/10.1016/j.apsusc.2020.145573
Lewandowska H, Wójciuk K, Karczmarczyk U (2021) Metal Nanozymes: New Horizons in Cellular Homeostasis Regulation. Applied Sciences 11 (19). doi:https://doi.org/10.3390/app11199019
Liu T, Bai R, Zhou H, Wang R, Liu J, Zhao Y, Chen C (2020a) The effect of size and surface ligands of iron oxide nanoparticles on blood compatibility. RSC Adv 10(13):7559–7569. https://doi.org/10.1039/C9RA10969B
Liu T, Han S, Pang M, Li J, Wang J, Luo X, Wang Y, Liu Z, Yang X, Ye Z (2020b) Cerium oxide nanoparticles protect red blood cells from hyperthermia-induced damages. J Biomater Appl. https://doi.org/10.1177/0885328220979091
Maćczak A, Cyrkler M, Bukowska B, Michałowicz J (2017) Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study). Toxicol in Vitro 41:143–149. https://doi.org/10.1016/j.tiv.2017.02.018
Maurya PK, Prakash S (2013) Decreased activity of Ca++-ATPase and Na+/K+-ATPase during aging in humans. Appl Biochem Biotechnol 170(1):131–137. https://doi.org/10.1007/s12010-013-0172-8
Maurya PK, Kumar P, Siddiqui N, Tripathi P, Rizvi SI (2010) Age-associated changes in erythrocyte glutathione peroxidase activity: correlation with total antioxidant potential. Indian J Biochem Biophys 47(5):319–321
Maurya PK, Kumar P, Nagotu S, Chand S, Chandra P (2016) Multi-target detection of oxidative stress biomarkers in quercetin and myricetin treated human red blood cells. RSC Adv 6(58):53195–53202. https://doi.org/10.1039/C6RA05121A
Mishra RK, Ahmad A, Vyawahare A, Alam P, Khan TH, Khan R (2021) Biological effects of formation of protein corona onto nanoparticles. Int J Biol Macromol 175:1–18. https://doi.org/10.1016/j.ijbiomac.2021.01.152
Mohanty J, Nagababu E, Rifkind J (2014) Red blood cell oxidative stress impairs oxygen delivery and induces red blood cell aging. Frontiers in Physiology 5 (84). https://doi.org/10.3389/fphys.2014.00084
Murugan C, Murugan N, Sundramoorthy AK, Sundaramurthy A (2019) Nanoceria decorated flower-like molybdenum sulphide nanoflakes: an efficient nanozyme for tumour selective ROS generation and photo thermal therapy. Chem Commun 55(55):8017–8020. https://doi.org/10.1039/C9CC03763B
Ng CT, Yong LQ, Hande MP, Ong CN, Yu LE, Bay BH, Baeg GH (2017) Zinc oxide nanoparticles exhibit cytotoxicity and genotoxicity through oxidative stress responses in human lung fibroblasts and Drosophila melanogaster. Int J Nanomedicine 12:1621–1637. https://doi.org/10.2147/IJN.S124403
Pareek V, Bhargava A, Bhanot V, Gupta R, Jain N, Panwar J (2018) Formation and characterization of protein corona around nanoparticles: a review. J Nanosci Nanotechnol 18(10):6653–6670. https://doi.org/10.1166/jnn.2018.15766
Passi M, Kumar V, Packirisamy G (2020) Theranostic nanozyme: Silk fibroin based multifunctional nanocomposites to combat oxidative stress. Mater Sci Eng, C 107:110255. https://doi.org/10.1016/j.msec.2019.110255
Peloi KE, Ratti BA, Nakamura CV, Neal CJ, Sakthivel TS, Singh S, Seal S, de Oliveira Silva Lautenschlager S (2021) Engineered nanoceria modulate neutrophil oxidative response to low doses of UV-B radiation through the inhibition of reactive oxygen species production. Journal of Biomedical Materials Research Part A n/a (n/a). doi:https://doi.org/10.1002/jbm.a.37251
Preedia Babu E, Subastri A, Suyavaran A, Premkumar K, Sujatha V, Aristatile B, Alshammari GM, Dharuman V, Thirunavukkarasu C (2017) Size dependent uptake and hemolytic effect of zinc oxide nanoparticles on erythrocytes and biomedical potential of ZnO-Ferulic acid conjugates. Sci Rep 7(1):4203–4203. https://doi.org/10.1038/s41598-017-04440-y
Rahul P, Srikanth VN, K. SR, Ashutosh K, Sanjay S, (2016) Effect of gold nanoparticle size and surface coating on human red blood cells. Bioinspired, Biomimetic and Nanobiomaterials 5(3):121–131. https://doi.org/10.1680/jbibn.15.00018
Rizvi SI, Maurya PK (2007) Markers of oxidative stress in erythrocytes during aging in humans. Ann N Y Acad Sci 1100(1):373–382. https://doi.org/10.1196/annals.1395.041
Rzigalinski BA, Giovinco HM, Cheatham BJ (2020) Cerium Oxide Nanoparticles Improve Lifespan of Stored Blood. Military Medicine 185 (Supplement_1):103–109. doi:https://doi.org/10.1093/milmed/usz210
Sarnatskaya V, Shlapa Y, Yushko L, Shton I, Solopan S, Ostrovska G, Kalachniuk L, Negelia A, Garmanchuk L, Prokopenko I, Khudenko N, Maslenny V, Bubnovskaya L, Belous A, Nikolaev V (2020) Biological activity of cerium dioxide nanoparticles. J Biomed Mater Res, Part A 108(8):1703–1712. https://doi.org/10.1002/jbm.a.36936
Shah J, Purohit R, Singh R, Karakoti AS, Singh S (2015) ATP-enhanced peroxidase-like activity of gold nanoparticles. J Colloid Interface Sci 456:100–107. https://doi.org/10.1016/j.jcis.2015.06.015
Shah J, Pandya A, Goyal P, Misra SK, Singh S (2020) BSA-decorated magnesium nanoparticles for scavenging hydrogen peroxide from human hepatic cells. ACS Applied Nano Materials 3(4):3355–3370. https://doi.org/10.1021/acsanm.0c00088
Shah F, Yadav N, Singh S (2021) Phosphotungstate-sandwiched between cerium oxide and gold nanoparticles exhibit enhanced catalytic reduction of 4-nitrophenol and peroxidase enzyme-like activity. Colloids Surf, B 198:111478. https://doi.org/10.1016/j.colsurfb.2020.111478
Shah J, Singh S (2018) Unveiling the role of ATP in amplification of intrinsic peroxidase-like activity of gold nanoparticles. 3 Biotech 8 (1):67. https://doi.org/10.1007/s13205-017-1082-1
Shirsekar P, Kanhe N, Mathe V, Lahir YK, Dongre P (2016) Interaction of zinc oxide nanoparticles with human red blood cells. Bionano Frontier 9:99–104
Singh S (2019) Nanomaterials exhibiting enzyme-like properties (nanozymes): current advances and future perspectives. Front Chem 7:46–46. https://doi.org/10.3389/fchem.2019.00046
Singh R, Singh S (2019) Redox-dependent catalase mimetic cerium oxide-based nanozyme protect human hepatic cells from 3-AT induced acatalasemia. Colloids Surf, B 175:625–635. https://doi.org/10.1016/j.colsurfb.2018.12.042
Singh S, Asal R, Bhagat S (2018) Multifunctional antioxidant nanoliposome-mediated delivery of PTEN plasmids restore the expression of tumor suppressor protein and induce apoptosis in prostate cancer cells. J Biomed Mater Res, Part A 106(12):3152–3164. https://doi.org/10.1002/jbm.a.36510
Singh N, NaveenKumar SK, Geethika M, Mugesh G (2021) A cerium vanadate nanozyme with specific superoxide dismutase activity regulates mitochondrial function and ATP synthesis in neuronal cells. Angew Chem Int Ed 60(6):3121–3130. https://doi.org/10.1002/anie.202011711
Subramaniam VD, Murugesan R, Pathak S (2020) Assessment of the cytotoxicity of cerium, tin, aluminum, and zinc oxide nanoparticles on human cells. J Nanopart Res 22(12):373. https://doi.org/10.1007/s11051-020-05102-3
Sudnitsyna J, Skverchinskaya E, Dobrylko I, Nikitina E, Gambaryan S, Mindukshev I (2020) Microvesicle Formation Induced by Oxidative Stress in Human Erythrocytes. Antioxidants 9 (10). doi:https://doi.org/10.3390/antiox9100929
Tian Y, Tian Z, Dong Y, Wang X, Zhan L (2021) Current advances in nanomaterials affecting morphology, structure, and function of erythrocytes. RSC Adv 11(12):6958–6971. https://doi.org/10.1039/D0RA10124A
Tsakanova G, Arakelova E, Ayvazyan V, Ayvazyan A, Tatikyan S, Grigoryan R, Sargsyan N, Arakelyan A (2020) Two-photon imaging of oxidative stress in living erythrocytes as a measure for human aging. Biomed Opt Express 11(7):3444–3454. https://doi.org/10.1364/BOE.393898
Vallabani NVS, Karakoti AS, Singh S (2017) ATP-mediated intrinsic peroxidase-like activity of Fe3O4-based nanozyme: One step detection of blood glucose at physiological pH. Colloids Surf, B 153:52–60. https://doi.org/10.1016/j.colsurfb.2017.02.004
Vallabani NVS, Singh S, Karakoti AS (2019) Investigating the role of ATP towards amplified peroxidase activity of Iron oxide nanoparticles in different biologically relevant buffers. Appl Surf Sci 492:337–348. https://doi.org/10.1016/j.apsusc.2019.06.177
Vallabani NVS, Vinu A, Singh S, Karakoti A (2020) Tuning the ATP-triggered pro-oxidant activity of iron oxide-based nanozyme towards an efficient antibacterial strategy. J Colloid Interface Sci 567:154–164. https://doi.org/10.1016/j.jcis.2020.01.099
Vallabani NVS, Singh S (2018) Recent advances and future prospects of iron oxide nanoparticles in biomedicine and diagnostics. 3 Biotech 8 (6):279. doi:https://doi.org/10.1007/s13205-018-1286-z
Wadhwa R, Aggarwal T, Thapliyal N, Kumar A, Priya, Yadav P, Kumari V, Reddy BSC, Chandra P, Maurya PK (2019) Red blood cells as an efficient in vitro model for evaluating the efficacy of metallic nanoparticles. 3 Biotech 9 (7):279. doi:https://doi.org/10.1007/s13205-019-1807-4
Wang Y, Li H, Guo L, Jiang Q, Liu F (2019) A cobalt-doped iron oxide nanozyme as a highly active peroxidase for renal tumor catalytic therapy. RSC Adv 9(33):18815–18822. https://doi.org/10.1039/C8RA05487H
Wang Q, Zennadi R (2020) Oxidative Stress and Thrombosis during Aging: The Roles of Oxidative Stress in RBCs in Venous Thrombosis. International Journal of Molecular Sciences 21 (12). doi:https://doi.org/10.3390/ijms21124259
Xiang J, Li J, He J, Tang X, Dou C, Cao Z, Yu B, Zhao C, Kang F, Yang L, Dong S, Yang X (2016) Cerium oxide nanoparticle modified scaffold interface enhances vascularization of bone grafts by activating calcium channel of mesenchymal stem cells. ACS Appl Mater Interfaces 8(7):4489–4499. https://doi.org/10.1021/acsami.6b00158
Yadav S, Maurya PK (2021) Biomedical applications of metal oxide nanoparticles in aging and age-associated diseases. 3 Biotech 11 (7):338. doi:https://doi.org/10.1007/s13205-021-02892-8
Yadav N, Singh S (2021a) Polyoxometalate-mediated vacancy-engineered cerium oxide nanoparticles exhibiting controlled biological enzyme-mimicking activities. Inorg Chem 60(10):7475–7489. https://doi.org/10.1021/acs.inorgchem.1c00766
Yadav N, Singh S (2021b) SOD mimetic cerium oxide nanorods protect human hepatocytes from oxidative stress. Emergent Materials. https://doi.org/10.1007/s42247-021-00220-7
Zhang Y, Wang Z, Li X, Wang L, Yin M, Wang L, Chen N, Fan C, Song H (2016) Dietary iron oxide nanoparticles delay aging and ameliorate neurodegeneration in drosophila. Adv Mater 28(7):1387–1393. https://doi.org/10.1002/adma.201503893
Zhu W, Wang L, Li Q, Jiao L, Yu X, Gao X, Qiu H, Zhang Z, Bing W (2021) Will the Bacteria Survive in the CeO2 Nanozyme-H2O2 System? Molecules 26 (12). https://doi.org/10.3390/molecules26123747
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This study was supported by Fellowship from the Council of Scientific and Industrial Research (CSIR), Government of India to Somu Yadav (09/1152(0013)/2019-EMR-I). This agency had no role in the interpretation, or writing the manuscript.
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Yadav, S., Maurya, P.K. Recent advances in the protective role of metallic nanoparticles in red blood cells. 3 Biotech 12, 28 (2022). https://doi.org/10.1007/s13205-021-03087-x
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DOI: https://doi.org/10.1007/s13205-021-03087-x