{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,6,25]],"date-time":"2025-06-25T17:10:08Z","timestamp":1750871408963,"version":"3.41.0"},"reference-count":41,"publisher":"Institute of Biochemistry","issue":"3","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["BIOMED KHIM"],"published-print":{"date-parts":[[2025,6]]},"abstract":"<jats:p>Carriers based on natural biominerals attract much attention in the context of the development of new drug delivery systems. In this study, the effects of native (CC) and hybrid vaterite microparticles with the inclusion of dextran sulfate (CCDS), chondroitin sulfate (CCCS), heparin (CCHE), fucoidan (CCFU), and pectin (CCPE) have been investigated on the viability and functional activity of neutrophils. Among the tested preparations, only CCFU exhibited a slight cytotoxic effect. Native CC stimulated actin cytoskeleton rearrangements and cell production of reactive oxygen species (ROS), which decreased in the presence of diphenyleneiodonium chloride (DPI), an inhibitor of NADPH oxidase assembly. The CC-induced NADPH oxidase activation was reduced in the presence of inhibitors of non-receptor tyrosine kinases of the Src family, phosphatidylinositol 3-kinase (PI3K), and phospholipase C (PLC). Similar to native CC, hybrid vaterite microparticles also initiated ROS production by neutrophils. After addition of CC and hybrid vaterite microparticles (except CCDS), an increase in the number of neutrophils characterized by higher values of the side scattering value was detected thus indicating a change in the morphological characteristics of the cells. Given the ability of hybrid vaterite microparticles with polysaccharides to activate neutrophil NADPH oxidase, they could be promising systems for the delivery of antibacterial and antiviral drugs.<\/jats:p>","DOI":"10.18097\/pbmcr1561","type":"journal-article","created":{"date-parts":[[2025,6,25]],"date-time":"2025-06-25T16:31:29Z","timestamp":1750869089000},"page":"227-238","source":"Crossref","is-referenced-by-count":0,"title":["Comparative analysis of the effect of hybrid vaterite microparticles with various polysaccharides on neutrophils activity"],"prefix":"10.18097","volume":"71","author":[{"given":"D.V.","family":"Grigorieva","sequence":"first","affiliation":[{"name":"Belarusian State University, Minsk, Belarus"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"E.V.","family":"Mikhalchik","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"D.V.","family":"Mosievich","sequence":"additional","affiliation":[{"name":"Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"P.I.","family":"Mishin","sequence":"additional","affiliation":[{"name":"Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"N.G.","family":"Balabushevich","sequence":"additional","affiliation":[{"name":"Lomonosov Moscow State University, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"O.M.","family":"Panasenko","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine, Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"A.V.","family":"Sokolov","sequence":"additional","affiliation":[{"name":"Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine, Moscow, Russia; Smorodintsev Research Institute of Influenza, St. Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"I.V.","family":"Gorudko","sequence":"additional","affiliation":[{"name":"Belarusian State University, Minsk, Belarus"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"7443","published-online":{"date-parts":[[2025]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","unstructured":"Ferreira A.M., Vikulina A.S., Volodkin D. (2020) CaCO3 crystals as versatile carriers for controlled delivery of antimicrobials. J. Control. Release, 328, 470\u2013489.","DOI":"10.1016\/j.jconrel.2020.08.061"},{"key":"ref2","doi-asserted-by":"publisher","unstructured":"Balabushevich N.G., Kovalenko E.A., Mikhalchik E.V., Filatova L.Y., Volodkin D., Vikulina A.S. (2019) Mucin adsorption on vaterite CaCO3 microcrystals for the prediction of mucoadhesive properties. J. Colloid Interface Sci., 545, 330\u2013339.","DOI":"10.1016\/j.jcis.2019.03.042"},{"key":"ref3","doi-asserted-by":"publisher","unstructured":"Balabushevich N.G., Maltseva L.N., Filatova L.Y., Mosievich D.V., Mishin P.I., Bogomiakova M.E., Lebedeva O.S., Murina M.A., Klinov D.V., Obraztsova E.A., Kharaeva Z.F., Firova R.K., Grigorieva D.V., Gorudko I.V., Panasenko O.M., Mikhalchik E.V. (2024) Influence of natural polysaccharides on the morphology and properties of hybrid vaterite microcrystals. Heliyon, 10(13), e33801.","DOI":"10.1016\/j.heliyon.2024.e33801"},{"key":"ref4","doi-asserted-by":"publisher","unstructured":"Grigorieva D.V., Mikhalchik E.V., Balabushevich N.G., Mosievich D.V., Murina M.A., Panasenko O.M., Sokolov A.V., Gorudko I.V. (2024) Effect of biopolymers and functionalized by them vaterite microparticles on platelet aggregation. J. Evol. Biochem. Physiol., 60(3), 1221\u20131233.","DOI":"10.31857\/S0869813924060107"},{"key":"ref5","doi-asserted-by":"publisher","unstructured":"Balabushevich N.G., Kovalenko E.A., Le-Deygen I.M., Filatova L.Y., Volodkin D., Vikulina A.S. (2019) Hybrid CaCO3-mucin crystals: effective approach for loading and controlled release of cationic drugs. Materials Design, 182, 108020.","DOI":"10.1016\/j.matdes.2019.108020"},{"key":"ref6","doi-asserted-by":"publisher","unstructured":"Galyamina M.A., Pobeguts O.V., Firova R.K., Mosievich D.V., Kharaeva Z.F., Panasenko O.M., Balabushevich N.G., Mikhalchik E.V. (2024) Biological activity of hybrid vaterite-pectin microparticles towards bacteria E. coli and human neutrophils. Bull. Exp. Biol. Med., 177(2), 238\u2013242.","DOI":"10.47056\/0365-9615-2024-177-2-209-214"},{"key":"ref7","doi-asserted-by":"publisher","unstructured":"Campbell J., Ferreira A.M., Bowker L., Hunt J., Volodkin D., Vikulina A. (2022) Dextran and its derivatives: biopolymer additives for the modulation of vaterite CaCO3 crystal morphology and adhesion to cells. Adv. Mater. Interfaces, 9(31), 1\u201310.","DOI":"10.1002\/admi.202201196"},{"key":"ref8","doi-asserted-by":"publisher","unstructured":"Gusliakova O., Verkhovskii R., Abalymov A., Lengert E., Kozlova A., Atkin V., Nechaeva O., Morrison A., Tuchin V., Svenskaya Y. (2021) Transdermal platform for the delivery of the antifungal drug naftifine hydrochloride based on porous vaterite particles. Mater. Sci. Eng. C Mater. Biol. Appl., 119, 111428.","DOI":"10.1016\/j.msec.2020.111428"},{"key":"ref9","doi-asserted-by":"publisher","unstructured":"Feoktistova N.A., Balabushevich N.G., Skirtach A.G., Volodkin D., Vikulina A.S. (2020) Inter-protein interactions govern protein loading into porous vaterite CaCO3 crystals. Phys. Chem. Chem. Phys., 22(17), 9713\u20139722.","DOI":"10.1039\/d0cp00404a"},{"key":"ref10","doi-asserted-by":"publisher","unstructured":"Kim A.L., Dubrovskii A.V., Musin E.V., Tikhonenko S.A. (2023) Determination of phenol with peroxidase immobilized on CaCO3. Int. J. Mol. Sci., 24(7), 6766.","DOI":"10.3390\/ijms24076766"},{"key":"ref11","doi-asserted-by":"publisher","unstructured":"Zhao P., Tian Y., Lu Y., Zhang J., Tao A., Xiang G., Liu Y. (2022) Biomimetic calcium carbonate nanoparticles delivered IL-12 mRNA for targeted glioblastoma sono-immunotherapy by ultrasound-induced necroptosis. J. Nanobiotechnol., 20(1), 525.","DOI":"10.1186\/s12951-022-01731-z"},{"key":"ref12","doi-asserted-by":"publisher","unstructured":"Ferreira A.M., Vikulina A.S., Bowker L., Hunt J.A., Loughlin M., Puddu V., Volodkin D. (2024) Nanoarchitectonics of bactericidal coatings based on CaCO3-nanosilver hybrids. ACS Appl. Bio Mater., 7(5), 2872\u20132886.","DOI":"10.1021\/acsabm.3c01228"},{"key":"ref13","doi-asserted-by":"publisher","unstructured":"Mikhalchik E.V., Basyreva L.Y., Gusev S.A., Panasenko O.M., Klinov D.V., Barinov N.A., Morozova O.V., Moscalets A.P., Maltseva L.N., Filatova L.Y., Pronkin E.A., Bespyatykh J.A., Balabushevich N.G. (2022) Activation of neutrophils by mucin-vaterite microparticles. Int. J. Mol. Sci., 23(18), 10579.","DOI":"10.3390\/ijms231810579"},{"key":"ref14","doi-asserted-by":"publisher","unstructured":"Mikhalchik E.V., Maltseva L.N., Firova R.K., Murina M.A., Gorudko I.V., Grigorieva D.V., Ivanov V.A., Obraztsova E.A., Klinov D.V., Shmeleva E.V., Gusev S.A., Panasenko O.M., Sokolov A.V., Gorbunov N.P., Filatova L.Y., Balabushevich N.G. (2023) Incorporation of pectin into vaterite microparticles prevented effects of adsorbed mucin on neutrophil activation. Int. J. Mol. Sci., 24(21), 15927.","DOI":"10.3390\/ijms242115927"},{"key":"ref15","doi-asserted-by":"publisher","unstructured":"Grigorieva D.V., Gorudko I.V., Grudinina N.A., Panasenko O.M., Semak I.V., Sokolov A.V., Timoshenko A.V. (2022) Lactoferrin modified by hypohalous acids: partial loss in activation of human neutrophils. Int. J. Biol. Macromol., 195, 30\u201340.","DOI":"10.1016\/j.ijbiomac.2021.11.165"},{"key":"ref16","doi-asserted-by":"publisher","unstructured":"Gorudko I.V., Grigorieva D.V., Shamova E.V., Kostevich V.A., Sokolov A.V., Mikhalchik E.V., Cherenkevich S.N., Arnhold J., Panasenko O.M. (2014) Hypohalous acid-modified human serum albumin induces neutrophil NADPH oxidase activation, degranulation, and shape change. Free Radic. Biol. Med., 68, 326\u2013334.","DOI":"10.1016\/j.freeradbiomed.2013.12.023"},{"key":"ref17","doi-asserted-by":"publisher","unstructured":"Oparka M., Walczak J., Malinska D., van Oppen L.M.P.E., Szczepanowska J., Koopman W.J.H., Wieckowski M.R. (2016) Quantifying ROS levels using CM-H2DCFDA and HyPer. Methods, 109, 3\u201311.","DOI":"10.1016\/j.ymeth.2016.06.008"},{"key":"ref18","doi-asserted-by":"publisher","unstructured":"Grigorieva D.V., Gorudko I.V., Shamova E.V., Terekhova M.S., Maliushkova E.V., Semak I.V., Cherenkevich S.N., Sokolov A.V., Timoshenko A.V. (2019) Effects of recombinant human lactoferrin on calcium signaling and functional responses of human neutrophils. Arch. Biochem. Biophys., 675, 108122.","DOI":"10.1016\/j.abb.2019.108122"},{"key":"ref19","doi-asserted-by":"publisher","unstructured":"Grynkiewicz G., Poenie M., Tsien R.Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem., 260(6), 3440\u20133450.","DOI":"10.1016\/S0021-9258(19)83641-4"},{"key":"ref20","doi-asserted-by":"publisher","unstructured":"Ren\u00f2 F., Carniato F., Rizzi M., Olivero F., Pittarella P., Marchese L. (2013) Flow cytometry evidence of human granulocytes interaction with polyhedral oligomeric silsesquioxanes: effect of nanoparticle charge. Nanotechnology, 24(18), 185101.","DOI":"10.1088\/0957-4484\/24\/18\/185101"},{"key":"ref21","doi-asserted-by":"publisher","unstructured":"Burt H.M., Jackson J.K., Taylor D.R., Crowther R.S. (1997) Activation of human neutrophils by calcium carbonate polymorphs. Dig. Dis. Sci., 42(6), 1283\u20131289.","DOI":"10.1023\/a:1018870511257"},{"key":"ref22","doi-asserted-by":"publisher","unstructured":"Pang L., Hayes C.P., Buac K., Yoo D.G., Rada B. (2013) Pseudogout-associated inflammatory calcium pyrophosphate dihydrate microcrystals induce formation of neutrophil extracellular traps. J. Immunol., 190(12), 6488\u20136500.","DOI":"10.4049\/jimmunol.1203215"},{"key":"ref23","doi-asserted-by":"publisher","unstructured":"Iversen T.-G., Skotland T., Sandvig K. (2011) Endocytosis and intracellular transport of nanoparticles: present knowledge and need for future studies. Nano Today, 6, 176\u2013185.","DOI":"10.1016\/j.nantod.2011.02.003"},{"key":"ref24","doi-asserted-by":"publisher","unstructured":"Schorn C., Janko C., Latzko M., Chaurio R., Schett G., Herrmann M. (2012) Monosodium urate crystals induce extracellular DNA traps in neutrophils, eosinophils, and basophils but not in mononuclear cells. Front. Immunol., 3, 277.","DOI":"10.3389\/fimmu.2012.00277"},{"key":"ref25","doi-asserted-by":"publisher","unstructured":"Parakhonskiy B., Zyuzin M.V, Yashchenok A., Carregal-Romero S., Rejman J., M\u00f6hwald H., Parak W.J., Skirtach A.G. (2015) The influence of the size and aspect ratio of anisotropic, porous CaCO3 particles on their uptake by cells. J. Nanobiotechnol., 13, 53.","DOI":"10.1186\/s12951-015-0111-7"},{"key":"ref26","doi-asserted-by":"publisher","unstructured":"Bittkau K.S., D\u00f6rschmann P., Bl\u00fcmel M., Tasdemir D., Roider J., Klettner A., Alban S. (2019) Comparison of the effects of fucoidans on the cell viability of tumor and non-tumor cell lines. Marine Drugs, 17(8), 441.","DOI":"10.3390\/md17080441"},{"key":"ref27","doi-asserted-by":"publisher","unstructured":"Horie M., Tabei Y., Sugino S., Eguchi K., Chiba R., Tajika M. (2019) Comparison of proinflammatory potential of needleshaped materials: aragonite and potassium titanate whisker. Arch. Toxicol., 93(10), 2797\u20132810.","DOI":"10.1007\/s00204-019-02556-w"},{"key":"ref28","doi-asserted-by":"publisher","unstructured":"Picco A., Kukulski W., Manenschijn H.E., Specht T., Briggs J.A.G., Kaksonen M. (2018) The contributions of the actin machinery to endocytic membrane bending and vesicle formation. Mol. Biol. Cell, 29(11), 1346\u20131358.","DOI":"10.1091\/mbc.E17-11-0688"},{"key":"ref29","doi-asserted-by":"publisher","unstructured":"Jiang M.H., Zhu L., Jiang J.G. (2010) Immunoregulatory actions of polysaccharides from Chinese herbal medicine. Expert Opin. Ther. Targets, 14(12), 1367\u20131402.","DOI":"10.1517\/14728222.2010.531010"},{"key":"ref30","doi-asserted-by":"publisher","unstructured":"Kim Y.S., Ryu J.H., Han S.J., Choi K.H., Nam K.B., Jang I.H., Lemaitre B., Brey P.T., Lee W.J. (2000) Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and beta-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. J. Biol. Chem., 275(42), 32721\u201332727.","DOI":"10.1074\/jbc.M003934200"},{"key":"ref31","doi-asserted-by":"publisher","unstructured":"Zhang W., Oda T., Yu Q., Jin J.O. (2015) Fucoidan from Macrocystis pyrifera has powerful immune-modulatory effects compared to three other fucoidans. Marine Drugs, 13(3), 1084\u20131104.","DOI":"10.3390\/md13031084"},{"key":"ref32","doi-asserted-by":"publisher","unstructured":"Apostolova E., Lukova P., Baldzhieva A., Katsarov P., Nikolova M., Iliev I., Peychev L., Trica B., Oancea F., Delattre C., Kokova V. (2020) Immunomodulatory and anti-inflammatory effects of fucoidan: a review. Polymers (Basel), 12(10), 2338.","DOI":"10.3390\/polym12102338"},{"key":"ref33","doi-asserted-by":"publisher","unstructured":"Nahm C., Koo Y., Yun T., Kim H., Kang B.-T., Yang M.-P. (2023) Fucoidan increases porcine neutrophil extracellular trap formation through TNF-\u03b1 from peripheral blood mononuclear cells. J. Vet. Clin., 40(3), 175\u2013181 DOI: 10.17555\/jvc.2023.40.3.175.","DOI":"10.17555\/jvc.2023.40.3.175"},{"key":"ref34","doi-asserted-by":"publisher","unstructured":"Castro R., Zarra I., Lamas J. (2004) Water-soluble seaweed extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture, 229, 67\u201378.","DOI":"10.1016\/S0044-8486(03)00401-0"},{"key":"ref35","doi-asserted-by":"publisher","unstructured":"Li H., Liu Y., Zheng Y., Zhang M., Wang X., Cheng H., Xu J., Chen X., Zhao X., Ding Z. (2023) Enhancement of seaweed polysaccharides (fucoidan and laminarin) on the phagocytosis of macrophages via activation of intelectin in blunt snout bream (Megalobrama amblycephala). Front. Marine Sci., 10, 1124880.","DOI":"10.3389\/fmars.2023.1124880"},{"key":"ref36","doi-asserted-by":"publisher","unstructured":"Gerasimov I.G., Ignatov D.Y. (2005) Blood coagulation initiates respiratory burst in neutrophils. Bull. Exp. Biol. Med., 140(1), 77\u201379.","DOI":"10.1007\/s10517-005-0416-x"},{"key":"ref37","doi-asserted-by":"publisher","unstructured":"Johann S., Zoller C., Haas S., Bl\u00fcmel G., F\u00f6rster R. (1996) Anticoagulant glycosaminoglycans activate respiratory burst in neutrophils and monocytes. Clin. Appl. Thromb. Hemost., 2(2), 116\u2013122.","DOI":"10.1177\/107602969600200206"},{"key":"ref38","doi-asserted-by":"publisher","unstructured":"Li G., Keenan A.C., Young J.C., Hall M.J., Pamuklar Z., Ohman E.M., Steinhubl S.R., Smyth S.S. (2007) Effects of unfractionated heparin and glycoprotein IIb\/IIIa antagonists versus bivalirdin on myeloperoxidase release from neutrophils. Arterioscler. Thromb. Vasc. Biol., 27(8), 1850\u20131856.","DOI":"10.1161\/ATVBAHA.107.144576"},{"key":"ref39","doi-asserted-by":"publisher","unstructured":"Freitas M., Porto G., Lima J.L., Fernandes E. (2008) Isolation and activation of human neutrophils in vitro. The importance of the anticoagulant used during blood collection. Clin. Biochem., 41(7\u20138), 570\u2013575.","DOI":"10.1016\/j.clinbiochem.2007.12.021"},{"key":"ref40","unstructured":"Zaporozhets T.S., Besednova N.N., Liamkin G.P., Loenko Iu.N., Popov A.M. (1991) Immunomoduliruiushchie svoistva pektina iz morskoi travy Zostera"},{"key":"ref41","unstructured":"Zaitseva O.O., Polezhaeva T.V., Khudyakov A.N., Solomina O.N., Laptev D.S., Svedentsov E.P., Utemov S.V., Kostyaev A.A. (2013) Influence of pectins on NADPH oxidase and phagocytic activity of neutrophils during cryopreservation. CryoLetters, 34(5), 544\u2013548."}],"container-title":["Biomeditsinskaya Khimiya"],"original-title":[],"language":"ru","deposited":{"date-parts":[[2025,6,25]],"date-time":"2025-06-25T16:32:00Z","timestamp":1750869120000},"score":1,"resource":{"primary":{"URL":"http:\/\/pbmc.ibmc.msk.ru\/en\/article-en\/PBMC-2025-71-3-227"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025]]},"references-count":41,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025]]},"published-print":{"date-parts":[[2025]]}},"URL":"https:\/\/doi.org\/10.18097\/pbmcr1561","relation":{},"ISSN":["2310-6905","2310-6972"],"issn-type":[{"value":"2310-6905","type":"electronic"},{"value":"2310-6972","type":"print"}],"subject":[],"published":{"date-parts":[[2025]]}}}