Graphene and Its Derivatives as Modulators of Macrophage Polarization in Cutaneous Wound Healing
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
2022/06/X/NZ3/00289
National Science Centre
Cooperation Program of Charles University, Prague, Czech Republic in the research area of "Physiology and Pathophysiology
Cooperation Program of Charles University, Prague, Czech Republic in the research area of "Physiology and Pathophysiology
PubMed
41440021
PubMed Central
PMC12731964
DOI
10.3390/cells14242001
PII: cells14242001
Knihovny.cz E-zdroje
- Klíčová slova
- biomaterial, cytocompatibility, cytotoxicity, plasticity, skin,
- MeSH
- grafit * farmakologie chemie MeSH
- hojení ran * účinky léků MeSH
- kůže * patologie účinky léků zranění MeSH
- lidé MeSH
- makrofágy * účinky léků metabolismus MeSH
- polarita buněk * účinky léků MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- grafit * MeSH
Graphene-based materials (GBMs), owing to their excellent biomedical properties, can significantly advance the development of nano-biodressings. Their unique physicochemical features, such as high surface area, tunable functionalization, antimicrobial activity, and ability to interact with immune cells, suggest that GBMs may influence key biological processes involved in tissue repair, particularly the immune response. Building on this growing evidence, the aim of this review is to demonstrate that GBMs can serve as tools for modulating macrophage polarization as a strategy for promoting wound healing. We present the mechanisms by which GBMs penetrate macrophages and discuss the effects of GBMs, either in suspension or as scaffolds/grounds/substrates, on macrophage polarization. Moreover, we propose mechanisms underlying the actions of different forms of GBMs on macrophage polarization. Nevertheless, a multitude of uncertainties and significant challenges remain. Chief among these are the pronounced heterogeneity of GBM subtypes, the necessity for exhaustive characterization and in-depth analysis, the formulation of robust experimental designs, and the careful selection of models capable of accurately delineating macrophage populations and guiding their polarization toward achieving targeted wound healing outcomes. This review attempts to systematize and clarify these issues.
Faculty of Health Studies Technical University of Liberec 460 01 Liberec Czech Republic
Faculty of Physics Warsaw University of Technology 00 662 Warsaw Poland
Zobrazit více v PubMed
Joorabloo A., Liu T. Recent Advances in Nanomedicines for Regulation of Macrophages in Wound Healing. J. Nanobiotechnology. 2022;20:407. doi: 10.1186/s12951-022-01616-1. PubMed DOI PMC
E Boniakowski A., Kimball A.S., Jacobs B.N., Kunkel S.L., A Gallagher K. Macrophage-Mediated Inflammation in Normal and Diabetic Wound Healing. J. Immunol. 2017;199:17–24. doi: 10.4049/jimmunol.1700223. PubMed DOI
Kuninaka Y., Ishida Y., Ishigami A., Nosaka M., Matsuki J., Yasuda H., Kofuna A., Kimura A., Furukawa F., Kondo T. Macrophage Polarity and Wound Age Determination. Sci. Rep. 2022;12:20327. doi: 10.1038/s41598-022-24577-9. PubMed DOI PMC
Novoselov K.S., Fal′Ko V.I., Colombo L., Gellert P.R., Schwab M.G., Kim K. A Roadmap for Graphene. Nature. 2012;490:192–200. doi: 10.1038/nature11458. PubMed DOI
Kalbacova M., Broz A., Kong J., Kalbac M. Graphene Substrates Promote Adherence of Human Osteoblasts and Mesenchymal Stromal Cells. Carbon. 2010;48:4323–4329. doi: 10.1016/j.carbon.2010.07.045. DOI
Lasocka I., Jastrzębska E., Zuchowska A., Skibniewska E., Skibniewski M., Szulc-Dąbrowska L., Pasternak I., Sitek J., Kalbacova M.H. Graphene 2d Platform Is Safe and Cytocompatibile for Hacat Cells Growing under Static and Dynamic Conditions. Nanotoxicology. 2022;16:610–628. doi: 10.1080/17435390.2022.2127128. PubMed DOI
Banerjee T., Biswas D., Pal D.S., Miao Y., Iglesias P.A., Devreotes P.N. Spatiotemporal Dynamics of Membrane Surface Charge Regulates Cell Polarity and Migration. Nat. Cell Biol. 2022;24:1499–1515. doi: 10.1038/s41556-022-00997-7. PubMed DOI PMC
Xia L., Zhu W., Wang Y., He S., Chai R. Regulation of Neural Stem Cell Proliferation and Differentiation by Graphene-Based Biomaterials. Neural Plast. 2019;2019:3608386. doi: 10.1155/2019/3608386. PubMed DOI PMC
Abbas Q., Shinde P.A., Abdelkareem M.A., Alami A.H., Mirzaeian M., Yadav A., Olabi A.G. Graphene Synthesis Techniques and Environmental Applications. Materials. 2022;15:7804. doi: 10.3390/ma15217804. PubMed DOI PMC
Lasocka I., Jastrzębska E., Szulc-Dąbrowska L., Skibniewski M., Pasternak I., Kalbacova M.H., Skibniewska E.M. The Effects of Graphene and Mesenchymal Stem Cells in Cutaneous Wound Healing and Their Putative Action Mechanism. Int. J. Nanomed. 2019;14:2281–2299. doi: 10.2147/IJN.S190928. PubMed DOI PMC
Zaaba N.I., Foo K.L., Hashim U., Tan S.J., Liu W.W., Voon C.H. Synthesis of Graphene Oxide Using Modified Hummers Method: Solvent Influence. Procedia Eng. 2017;184:469–477. doi: 10.1016/j.proeng.2017.04.118. DOI
Chen J., Li Y., Huang L., Li C., Shi G. High-Yield Preparation of Graphene Oxide from Small Graphite Flakes Via an Improved Hummers Method with a Simple Purification Process. Carbon. 2015;81:826–834. doi: 10.1016/j.carbon.2014.10.033. DOI
Adetayo A., Runsewe D. Synthesis and Fabrication of Graphene and Graphene Oxide: A Review. Open J. Compos. Mater. 2019;09:207–229. doi: 10.4236/ojcm.2019.92012. DOI
Ahmad N., Kausar A., Muhammad B. An Investigation on 4-Aminobenzoic Acid Modified Polyvinyl Chloride/Graphene Oxide and Pvc/Graphene Oxide Based Nanocomposite Membranes. J. Plast. Film Sheeting. 2016;32:419–448. doi: 10.1177/8756087915616434. DOI
Feng J., Ye Y., Xiao M., Wu G., Ke Y. Synthetic Routes of the Reduced Graphene Oxide. Chem. Pap. 2020;74:3767–3783. doi: 10.1007/s11696-020-01196-0. DOI
Stankovich S., Dikin D.A., Piner R.D., Kohlhaas K.A., Kleinhammes A., Jia Y., Wu Y., Nguyen S.T., Ruoff R.S. Synthesis of Graphene-Based Nanosheets Via Chemical Reduction of Exfoliated Graphite Oxide. Carbon. 2007;45:1558–1565. doi: 10.1016/j.carbon.2007.02.034. DOI
Chen W., Yan L., Bangal P.R. Chemical Reduction of Graphene Oxide to Graphene by Sulfur-Containing Compounds. J. Phys. Chem. C. 2010;114:19885–19890. doi: 10.1021/jp107131v. DOI
Choudhary P., Das S.K. Bio-Reduced Graphene Oxide as a Nanoscale Antimicrobial Coating for Medical Devices. ACS Omega. 2019;4:387–397. doi: 10.1021/acsomega.8b02787. DOI
El-Khawaga A.M., Tantawy H., Elsayed M.A., Abd El-Mageed A.I.A. Synthesis and Applicability of Reduced Graphene Oxide/Porphyrin Nanocomposite as Photocatalyst for Waste Water Treatment and Medical Applications. Sci. Rep. 2022;12:17075. doi: 10.1038/s41598-022-21360-8. PubMed DOI PMC
Manikandan V., Lee N.Y. Reduced Graphene Oxide: Biofabrication and Environmental Applications. Chemosphere. 2022;311:136934. doi: 10.1016/j.chemosphere.2022.136934. PubMed DOI
Zambrano-Andazol I., Vázquez N., Chacón M., Sánchez-Avila R.M., Persinal M., Blanco C., González Z., Menéndez R., Sierra M., Fernández-Vega Á., et al. Reduced Graphene Oxide Membranes in Ocular Regenerative Medicine. Mater. Sci. Eng. C. 2020;114:111075. doi: 10.1016/j.msec.2020.111075. PubMed DOI
Suroto B.J., Sembiring H.F., Fathurrahman M.T., Risdiana R., Riveli N., Hidayat S., Syakir N. The Study of Wettability in Reduced Graphene Oxide Film on Copper Substrate Using Electrostatic Spray Deposition Technique. J. Phys. Conf. Ser. 2018;1080:012020. doi: 10.1088/1742-6596/1080/1/012020. DOI
Backes C., Abdelkader A.M., Alonso C., Andrieux-Ledier A., Arenal R., Azpeitia J., Balakrishnan N., Banszerus L., Barjon J., Bartali R., et al. Production and Processing of Graphene and Related Materials. 2D Mater. 2020;7:022001. doi: 10.1088/2053-1583/ab1e0a. DOI
Kumar V., Kumar A., Lee D.-J., Park S.-S. Estimation of Number of Graphene Layers Using Different Methods: A Focused Review. Materials. 2021;14:4590. doi: 10.3390/ma14164590. PubMed DOI PMC
Ferrari A.C., Basko D.M. Raman Spectroscopy as a Versatile Tool for Studying the Properties of Graphene. Nat. Nanotechnol. 2013;8:235–246. doi: 10.1038/nnano.2013.46. PubMed DOI
Wróblewska A., Duzynska A., Judek J., Stobinski L., Zeranska K., Gertych A., Zdrojek M. Statistical Analysis of the Reduction Process of Graphene Oxide Probed by Raman Spectroscopy Mapping. J. Phys. Condens. Matter. 2017;29:475201. doi: 10.1088/1361-648X/aa92fe. PubMed DOI
Zeranska-Chudek K., Wróblewska A., Kowalczyk S., Plichta A., Zdrojek M. Graphene Infused Ecological Polymer Composites for Electromagnetic Interference Shielding and Heat Management Applications. Materials. 2021;14:2856. doi: 10.3390/ma14112856. PubMed DOI PMC
Park M., Kim T., Yang C. Thickness Contrast of Few-Layered Graphene in Sem. Surf. Interface Anal. 2012;44:1538–1541. doi: 10.1002/sia.4995. DOI
Chen C., Liu T., Tang Y., Luo G., Liang G., He W. Epigenetic Regulation of Macrophage Polarization in Wound Healing. Burn. Trauma. 2023;11:tkac057. doi: 10.1093/burnst/tkac057. PubMed DOI PMC
Guimarães G.R., Almeida P.P., de Oliveira Santos L.D.O., Rodrigues L.P., de Carvalho J.L., Boroni M. Hallmarks of Aging in Macrophages: Consequences to Skin Inflammaging. Cells. 2021;10:1323. doi: 10.3390/cells10061323. PubMed DOI PMC
Hesketh M., Sahin K.B., West Z.E., Murray R.Z. Macrophage Phenotypes Regulate Scar Formation and Chronic Wound Healing. Int. J. Mol. Sci. 2017;18:1545. doi: 10.3390/ijms18071545. PubMed DOI PMC
Kim S.Y., Nair M.G. Macrophages in Wound Healing: Activation and Plasticity. Immunol. Cell Biol. 2019;97:258–267. doi: 10.1111/imcb.12236. PubMed DOI PMC
Manole E., Niculite C., Lambrescu I.M., Gaina G., Ioghen O., Ceafalan L.C., Hinescu M.E. Macrophages and Stem Cells—Two to Tango for Tissue Repair? Biomolecules. 2021;11:697. doi: 10.3390/biom11050697. PubMed DOI PMC
Chaintreuil P., Kerreneur E., Bourgoin M., Savy C., Favreau C., Robert G., Jacquel A., Auberger P. The Generation, Activation, and Polarization of Monocyte-Derived Macrophages in Human Malignancies. Front. Immunol. 2023;14:1178337. doi: 10.3389/fimmu.2023.1178337. PubMed DOI PMC
Chen S., Saeed A.F., Liu Q., Jiang Q., Xu H., Xiao G.G., Rao L., Duo Y. Macrophages in Immunoregulation and Therapeutics. Signal Transduct. Target. Ther. 2023;8:207. doi: 10.1038/s41392-023-01452-1. PubMed DOI PMC
Krzyszczyk P., Schloss R., Palmer A., Berthiaume F. The Role of Macrophages in Acute and Chronic Wound Healing and Interventions to Promote Pro-Wound Healing Phenotypes. Front. Physiol. 2018;9:419. doi: 10.3389/fphys.2018.00419. PubMed DOI PMC
Saas P., Chagué C., Maraux M., Cherrier T. Toward the Characterization of Human Pro-Resolving Macrophages? Front. Immunol. 2020;11:593300. doi: 10.3389/fimmu.2020.593300. PubMed DOI PMC
DiPietro L.A., Wilgus T.A., Koh T.J. Macrophages in Healing Wounds: Paradoxes and Paradigms. Int. J. Mol. Sci. 2021;22:950. doi: 10.3390/ijms22020950. PubMed DOI PMC
Willenborg S., Injarabian L., Eming S.A. Role of Macrophages in Wound Healing. Cold Spring Harb. Perspect. Biol. 2022;14:a041216. doi: 10.1101/cshperspect.a041216. PubMed DOI PMC
Hassanshahi A., Moradzad M., Ghalamkari S., Fadaei M., Cowin A.J., Hassanshahi M. Macrophage-Mediated Inflammation in Skin Wound Healing. Cells. 2022;11:2953. doi: 10.3390/cells11192953. PubMed DOI PMC
Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., Gordon S., Hamilton J.A., Ivashkiv L.B., Lawrence T., et al. Macrophage Activation and Polarization: Nomenclature and Experimental Guidelines. Immunity. 2014;41:14–20. doi: 10.1016/j.immuni.2014.06.008. PubMed DOI PMC
Stahl A., Hao D., Barrera J., Henn D., Lin S., Moeinzadeh S., Kim S., Maloney W., Gurtner G., Wang A., et al. A Bioactive Compliant Vascular Graft Modulates Macrophage Polarization and Maintains Patency with Robust Vascular Remodeling. Bioact. Mater. 2022;19:167–178. doi: 10.1016/j.bioactmat.2022.04.004. PubMed DOI PMC
Purcu D.U., Korkmaz A., Gunalp S., Helvaci D.G., Erdal Y., Dogan Y., Suner A., Wingender G., Sag D. Effect of Stimulation Time on the Expression of Human Macrophage Polarization Markers. PLoS ONE. 2022;17:e0265196. PubMed PMC
Kerneur C., Cano C.E., Olive D. Major Pathways Involved in Macrophage Polarization in Cancer. Front. Immunol. 2022;13:1026954. doi: 10.3389/fimmu.2022.1026954. PubMed DOI PMC
Luque-Martin R., Mander P.K., Leenen P.J.M., Winther M.P.J. Classic and New Mediators for in vitro Modelling of Human Macrophages. J. Leukoc. Biol. 2020;109:549–560. doi: 10.1002/JLB.1RU0620-018R. PubMed DOI PMC
Wu X., He W., Mu X., Liu Y., Deng J., Liu Y., Nie X. Macrophage Polarization in Diabetic Wound Healing. Burn. Trauma. 2022;10:tkac051. doi: 10.1093/burnst/tkac051. PubMed DOI PMC
Mosser D.M., Edwards J.P. Exploring the Full Spectrum of Macrophage Activation. Nat. Rev. Immunol. 2008;8:958–969. doi: 10.1038/nri2448. PubMed DOI PMC
Jablonski K.A., Amici S.A., Webb L.M., Ruiz-Rosado J.D.D., Popovich P.G., Partida-Sanchez S., Guerau-de-Arellano M. Novel Markers to Delineate Murine M1 and M2 Macrophages. PLoS ONE. 2015;10:e0145342. doi: 10.1371/journal.pone.0145342. PubMed DOI PMC
Aristorena M., Gallardo-Vara E., Vicen M., Casas-Engel M.d.L., Ojeda-Fernandez L., Nieto C., Blanco F.J., Valbuena-Diez A.C., Botella L.M., Nachtigal P., et al. Mmp-12, Secreted by Pro-Inflammatory Macrophages, Targets Endoglin in Human Macrophages and Endothelial Cells. Int. J. Mol. Sci. 2019;20:3107. doi: 10.3390/ijms20123107. PubMed DOI PMC
Yu T., Gan S., Zhu Q., Dai D., Li N., Wang H., Chen X., Hou D., Wang Y., Pan Q., et al. Modulation of M2 Macrophage Polarization by the Crosstalk between Stat6 and Trim24. Nat. Commun. 2019;10:4353. doi: 10.1038/s41467-019-12384-2. PubMed DOI PMC
Peng H., Xian D., Liu J., Pan S., Tang R., Zhong J. Regulating the Polarization of Macrophages: A Promising Approach to Vascular Dermatosis. J. Immunol. Res. 2020;2020:8148272. doi: 10.1155/2020/8148272. PubMed DOI PMC
Liu L., Stokes J.V., Tan W., Pruett S.B. An Optimized Flow Cytometry Panel for Classifying Macrophage Polarization. J. Immunol. Methods. 2022;511:113378. doi: 10.1016/j.jim.2022.113378. PubMed DOI
Strizova Z., Benesova I., Bartolini R., Novysedlak R., Cecrdlova E., Foley L.K., Striz I. M1/M2 Macrophages and Their Overlaps-Myth or Reality? Clin. Sci. 2023;137:1067–1093. doi: 10.1042/CS20220531. PubMed DOI PMC
Zheng H., Cheng X., Jin L., Shan S., Yang J., Zhou J. Recent Advances in Strategies to Target the Behavior of Macrophages in Wound Healing. Biomed. Pharmacother. 2023;165:115199. doi: 10.1016/j.biopha.2023.115199. PubMed DOI
Xue J.-D., Gao J., Tang A.-F., Feng C. Shaping the Immune Landscape: Multidimensional Environmental Stimuli Refine Macrophage Polarization and Foster Revolutionary Approaches in Tissue Regeneration. Heliyon. 2024;10:e37192. doi: 10.1016/j.heliyon.2024.e37192. PubMed DOI PMC
Zomer H.D., Trentin A.G. Skin Wound Healing in Humans and Mice: Challenges in Translational Research. J. Dermatol. Sci. 2018;90:3–12. doi: 10.1016/j.jdermsci.2017.12.009. PubMed DOI
Colletta A.D., Pelin M., Sosa S., Fusco L., Prato M., Tubaro A. Carbon-Based Nanomaterials and Skin: An Overview. Carbon. 2022;196:683–698. doi: 10.1016/j.carbon.2022.05.036. DOI
Gao Y., Wang X., Fan C. Advances in Graphene-Based 2D Materials for Tendon, Nerve, Bone/Cartilage Regeneration and Biomedicine. iScience. 2024;27:110214. doi: 10.1016/j.isci.2024.110214. PubMed DOI PMC
Xue J., Zheng Y., Yang Z., Huang J., Ma W., Huan Z., Zhu Y., Wu C. Graphene Oxide/Chitosan/Calcium Silicate Aerogels for Hemostasis and Infectious Wound Healing. Regen. Med. Dent. 2025;2:8. doi: 10.53941/rmd.2025.100008. DOI
Ruíz I., González L., Quiroz A., Aguayo C., Toledo J., Fernández K. Optimization and Validation of Chitosan-Reduced Graphene Oxide-Pluronic F-127 Hydrogel Synthesis for Potential Wound Dressing. ChemistrySelect. 2025;10:e02598. doi: 10.1002/slct.202502598. DOI
Xie F., Zou L., Xu Z., Ou X., Guo W., Gao Y., Gao G. Alginate Foam Gel Modified by Graphene Oxide for Wound Dressing. Int. J. Biol. Macromol. 2022;223:391–403. doi: 10.1016/j.ijbiomac.2022.11.013. PubMed DOI
Sareło P., Wiśniewska-Wrona M., Sikora M., Mielan B., Gerasymchuk Y., Wędzyńska A., Boiko V., Hreniak D., Szymonowicz M., Sobieszczańska B., et al. Development and Evaluation of Graphene Oxide-Enhanced Chitosan Sponges as a Potential Antimicrobial Wound Dressing for Infected Wound Management. Int. J. Mol. Sci. 2025;26:7403. doi: 10.3390/ijms26157403. PubMed DOI PMC
Liu Y., Wang L., Wen D., Deng Z., Wu Z., Li S., Li Y. Preparation and Characterization of Nano-Silver/Graphene Oxide Antibacterial Skin Dressing. Sci. Rep. 2025;15:12490. doi: 10.1038/s41598-025-93310-z. PubMed DOI PMC
Li S., Wang J., Zhang H., Zhang X. Advances in Graphene Oxide-Based Polymeric Wound Dressings for Wound Healing. Front. Mater. 2025;12:1635502. doi: 10.3389/fmats.2025.1635502. DOI
Anderson C.F., Mosser D.M. A Novel Phenotype for an Activated Macrophage: The Type 2 Activated Macrophage. J. Leukoc. Biol. 2002;72:101–106. doi: 10.1189/jlb.72.1.101. PubMed DOI
Li P., Ma C., Li J., You S., Dang L., Wu J., Hao Z., Li J., Zhi Y., Chen L., et al. Proteomic Characterization of Four Subtypes of M2 Macrophages Derived from Human Thp-1 Cells. J. Zhejiang Univ. B. 2022;23:407–422. doi: 10.1631/jzus.B2100930. PubMed DOI PMC
Liu N., Zhang B., Sun Y., Song W., Guo S. Macrophage Origin, Phenotypic Diversity, and Modulatory Signaling Pathways in the Atherosclerotic Plaque Microenvironment. Vessel Plus. 2021;5:43. doi: 10.20517/2574-1209.2021.25. DOI
Mamilos A., Winter L., Schmitt V.H., Barsch F., Grevenstein D., Wagner W., Babel M., Keller K., Schmitt C., Gürtler F., et al. Macrophages: From Simple Phagocyte to an Integrative Regulatory Cell for Inflammation and Tissue Regeneration—A Review of the Literature. Cells. 2023;12:276. doi: 10.3390/cells12020276. PubMed DOI PMC
Kuntzel T., Bagnard D. Manipulating Macrophage/Microglia Polarization to Treat Glioblastoma or Multiple Sclerosis. Pharmaceutics. 2022;14:344. doi: 10.3390/pharmaceutics14020344. PubMed DOI PMC
Orecchioni M., Ghosheh Y., Pramod A.B., Ley K. Macrophage Polarization: Different Gene Signatures in M1(Lps+) vs. Classically and M2(Lps–) vs. Alternatively Activated Macrophages. Front. Immunol. 2019;10:1084. doi: 10.3389/fimmu.2019.01084. PubMed DOI PMC
Ross E.A., Devitt A., Johnson J.R. Macrophages: The Good, the Bad, and the Gluttony. Front. Immunol. 2021;12:708186. doi: 10.3389/fimmu.2021.708186. PubMed DOI PMC
Schönborn K., Willenborg S., Schulz J.-N., Imhof T., Eming S.A., Quondamatteo F., Brinckmann J., Niehoff A., Paulsson M., Koch M., et al. Role of Collagen Xii in Skin Homeostasis and Repair. Matrix Biol. 2020;94:57–76. doi: 10.1016/j.matbio.2020.08.002. PubMed DOI
Lin H., Buerki-Thurnherr T., Kaur J., Wick P., Pelin M., Tubaro A., Carniel F.C., Tretiach M., Flahaut E., Iglesias D., et al. Environmental and Health Impacts of Graphene and Other Two-Dimensional Materials: A Graphene Flagship Perspective. ACS Nano. 2024;18:6038–6094. doi: 10.1021/acsnano.3c09699. PubMed DOI PMC
Mendoza-Coronel E., Ortega E. Macrophage Polarization Modulates Fcγr- and Cd13-Mediated Phagocytosis and Reactive Oxygen Species Production, Independently of Receptor Membrane Expression. Front. Immunol. 2017;8:303. doi: 10.3389/fimmu.2017.00303. PubMed DOI PMC
Povo-Retana A., Mojena M., Boscá A., Pedrós J., Peraza D.A., Valenzuela C., Laparra J.M., Calle F., Boscá L. Graphene Particles Interfere with Pro-Inflammatory Polarization of Human Macrophages: Functional and Electrophysiological Evidence. Adv. Biol. 2021;5:2100882. doi: 10.1002/adbi.202100882. PubMed DOI
Mendes R.G., Mandarino A., Koch B., Meyer A.K., Bachmatiuk A., Hirsch C., Gemming T., Schmidt O.G., Liu Z., Rümmeli M.H. Size and Time Dependent Internalization of Label-Free Nano-Graphene Oxide in Human Macrophages. Nano Res. 2017;10:1980–1995. doi: 10.1007/s12274-016-1385-2. DOI
Ma J., Liu R., Wang X., Liu Q., Chen Y., Valle R.P., Zuo Y.Y., Xia T., Liu S. Crucial Role of Lateral Size for Graphene Oxide in Activating Macrophages and Stimulating Pro-Inflammatory Responses in Cells and Animals. ACS Nano. 2015;9:10498–10515. doi: 10.1021/acsnano.5b04751. PubMed DOI PMC
Hoyle C., Rivers-Auty J., Lemarchand E., Vranic S., Wang E., Buggio M., Rothwell N.J., Allan S.M., Kostarelos K., Brough D. Small, Thin Graphene Oxide Is Anti-Inflammatory Activating Nuclear Factor Erythroid 2-Related Factor 2 Via Metabolic Reprogramming. ACS Nano. 2018;12:11949–11962. doi: 10.1021/acsnano.8b03642. PubMed DOI
Malanagahalli S., Murera D., Martín C., Lin H., Wadier N., Dumortier H., Vázquez E., Bianco A. Few Layer Graphene Does Not Affect Cellular Homeostasis of Mouse Macrophages. Nanomaterials. 2020;10:228. doi: 10.3390/nano10020228. PubMed DOI PMC
Li Y., Yuan H., Bussche A.v.D., Creighton M., Hurt R.H., Kane A.B., Gao H. Graphene Microsheets Enter Cells through Spontaneous Membrane Penetration at Edge Asperities and Corner Sites. Proc. Natl. Acad. Sci. USA. 2013;110:12295–12300. doi: 10.1073/pnas.1222276110. PubMed DOI PMC
Artiga Á., Lin H., Bianco A. Interaction of Industrial Graphene and Carbon Nanotubes with Human Primary Macrophages: Assessment of Nanotoxicity and Immune Responses. Carbon. 2024;223:119024. doi: 10.1016/j.carbon.2024.119024. DOI
Cicuéndez M., Casarrubios L., Barroca N., Silva D., Feito M.J., Diez-Orejas R., Marques P.A.A.P., Portolés M.T. Benefits in the Macrophage Response Due to Graphene Oxide Reduction by Thermal Treatment. Int. J. Mol. Sci. 2021;22:6701. doi: 10.3390/ijms22136701. PubMed DOI PMC
Qu G., Liu S., Zhang S., Wang L., Wang X., Sun B., Yin N., Gao X., Xia T., Chen J.-J., et al. Graphene Oxide Induces Toll-Like Receptor 4 (Tlr4)-Dependent Necrosis in Macrophages. ACS Nano. 2013;7:5732–5745. doi: 10.1021/nn402330b. PubMed DOI
Lavín-López M.d.P., Torres-Torresano M., García-Cuesta E.M., Soler-Palacios B., Griera M., Martínez-Rovira M., Martínez-Rovira J.A., Rodríguez-Puyol D., de Frutos S. A Graphene-Based Bioactive Product with a Non-Immunological Impact on Mononuclear Cell Populations from Healthy Volunteers. Nanomaterials. 2024;14:1945. doi: 10.3390/nano14231945. PubMed DOI PMC
Lin H., Ji D.K., Lucherelli M.A., Reina G., Ippolito S., Samorì P., Bianco A. Comparative Effects of Graphene and Molybdenum Disulfide on Human Macrophage Toxicity. Small. 2020;16:e2002194. doi: 10.1002/smll.202002194. PubMed DOI
Lebre F., Boland J.B., Gouveia P., Gorman A.L., Lundahl M.L., Lynch R.I., O’Brien F.J., Coleman J., Lavelle E.C. Pristine Graphene Induces Innate Immune Training. Nanoscale. 2020;12:11192–11200. doi: 10.1039/C9NR09661B. PubMed DOI
Korejwo D., Chortarea S., Louka C., Buljan M., Rothen-Rutishauser B., Wick P., Buerki-Thurnherr T. Gene Expression Profiling of Human Macrophages after Graphene Oxide and Graphene Nanoplatelets Treatment Reveals Particle-Specific Regulation of Pathways. NanoImpact. 2023;29:100452. doi: 10.1016/j.impact.2023.100452. PubMed DOI
Zhou H., Zhao K., Li W., Yang N., Liu Y., Chen C., Wei T. The Interactions between Pristine Graphene and Macrophages and the Production of Cytokines/Chemokines Via Tlr- and NF-κB-Related Signaling Pathways. Biomaterials. 2012;33:6933–6942. doi: 10.1016/j.biomaterials.2012.06.064. PubMed DOI
Feito M.J., Diez-Orejas R., Cicuéndez M., Casarrubios L., Rojo J.M., Portolés M.T. Characterization of M1 and M2 Polarization Phenotypes in Peritoneal Macrophages after Treatment with Graphene Oxide Nanosheets. Colloids Surfaces B Biointerfaces. 2019;176:96–105. doi: 10.1016/j.colsurfb.2018.12.063. PubMed DOI
Deng S., Berry V. Wrinkled, Rippled and Crumpled Graphene: An Overview of Formation Mechanism, Electronic Properties, and Applications. Mater. Today. 2016;19:197–212. doi: 10.1016/j.mattod.2015.10.002. DOI
Kalbacova M.H., Verdanova M., Broz A., Vetushka A., Fejfar A., Kalbac M. Modulated Surface of Single-Layer Graphene Controls Cell Behavior. Carbon. 2014;72:207–214. doi: 10.1016/j.carbon.2014.02.004. DOI
Lasocka I., Skibniewska E., Skibniewski M., Szulc-Dąbrowska L., Jastrzębska E., Pasternak I., Jakub S., Hubalek-Kalbacova M. Graphene Monolayer as an Appropriate Substrate for Mesenchymal Stem Cells Support in Regenerative Medicine. Indian J. Exp. Biol. 2023;61:235–243. doi: 10.56042/ijeb.v61i04.174. DOI
Lasocka I., Szulc-Dąbrowska L., Skibniewski M., Skibniewska E., Gregorczyk-Zboroch K., Pasternak I., Kalbacova M.H. Cytocompatibility of Graphene Monolayer and Its Impact on Focal Cell Adhesion, Mitochondrial Morphology and Activity in Balb/3t3 Fibroblasts. Materials. 2021;14:643. doi: 10.3390/ma14030643. PubMed DOI PMC
Lasocka I., Szulc-Dąbrowska L., Skibniewski M., Skibniewska E., Strupinski W., Pasternak I., Kmieć H., Kowalczyk P. Biocompatibility of Pristine Graphene Monolayer: Scaffold for Fibroblasts. Toxicol. Vitr. 2018;48:276–285. doi: 10.1016/j.tiv.2018.01.028. PubMed DOI
Bellet P., Gasparotto M., Pressi S., Fortunato A., Scapin G., Mba M., Menna E., Filippini F. Graphene-Based Scaffolds for Regenerative Medicine. Nanomaterials. 2021;11:404. doi: 10.3390/nano11020404. PubMed DOI PMC
Munz M., Giusca C.E., Myers-Ward R.L., Gaskill D.K., Kazakova O. Thickness-Dependent Hydrophobicity of Epitaxial Graphene. ACS Nano. 2015;9:8401–8411. doi: 10.1021/acsnano.5b03220. PubMed DOI
Meli V.S., Veerasubramanian P.K., Atcha H., Reitz Z., Downing T.L., Liu W.F. Biophysical Regulation of Macrophages in Health and Disease. J. Leukoc. Biol. 2019;106:283–299. doi: 10.1002/JLB.MR0318-126R. PubMed DOI PMC
Cao X., Luo B., Mu Y., Wang C., Lu R., Yao Y., Chen S. The Regulatory Effect of TiO2 nanotubes Loaded with Graphene Oxide on Macrophage Polarization in an Inflammatory Environment. BMC Oral Health. 2024;24:824. doi: 10.1186/s12903-024-04608-9. PubMed DOI PMC
Serrano M.C., Feito M.J., González-Mayorga A., Diez-Orejas R., Matesanz M.C., Portolés M.T. Response of Macrophages and Neural Cells in Contact with Reduced Graphene Oxide Microfibers. Biomater. Sci. 2018;6:2987–2997. doi: 10.1039/C8BM00902C. PubMed DOI
Yan Y., Zhang Y., Li K., Li Y., Qian W., Zhang W., Wang Y., Ma W., Li L. Synergistic Effects of Graphene Microgrooves and Electrical Stimulation on M2 Macrophage Polarization. Biochem. Biophys. Res. Commun. 2024;711:149911. doi: 10.1016/j.bbrc.2024.149911. PubMed DOI
Mei F., Guo Y., Wang Y., Zhou Y., Heng B.C., Xie M., Huang X., Zhang S., Ding S., Liu F., et al. Matrix Stiffness Regulates Macrophage Polarisation Via the Piezo1-Yap Signalling Axis. Cell Prolif. 2024;57:e13640. doi: 10.1111/cpr.13640. PubMed DOI PMC
Tu P.C., Pan Y.L., Liang Z.Q., Yang G.L., Wu C.J., Zeng L., Wang L.N., Sun J., Liu M.M., Yuan Y.F., et al. Mechanical Stretch Promotes Macrophage Polarization and Inflammation Via the Rhoa-Rock/Nf-Κb Pathway. Biomed Res. Int. 2022;2022:6871269. doi: 10.1155/2022/6871269. PubMed DOI PMC
Li J., Xie J., Wang Y., Li X., Yang L., Zhao M., Chen C. Development of Biomaterials to Modulate the Function of Macrophages in Wound Healing. Bioengineering. 2024;11:1017. doi: 10.3390/bioengineering11101017. PubMed DOI PMC
Ou X., Guan L., Guo W., Zhang X., Wu S., Guo D., Li R., Zvyagin A.V., Lin Q., Qu W. Graphene Oxide-Based Injectable Conductive Hydrogel Dressing with Immunomodulatory for Chronic Infected Diabetic Wounds. Mater. Des. 2022;224:111284. doi: 10.1016/j.matdes.2022.111284. DOI
Davis M.J., Tsang T.M., Qiu Y., Dayrit J.K., Freij J.B., Huffnagle G.B., Olszewski M.A. Macrophage M1/M2 Polarization Dynamically Adapts to Changes in Cytokine Microenvironments in Cryptococcus Neoformans Infection. mBio. 2013;4:e00264–13. doi: 10.1128/mBio.00264-13. PubMed DOI PMC
Mezouar S., Mege J.-L. New Tools for Studying Macrophage Polarization: Application to Bacterial Infections. In: Prakash H., editor. Macrophages. IntechOpen; Rijeka, Croatia: 2020.
Geng Y., Hardie J., Landis R.F., Mas-Rosario J.A., Chattopadhyay A.N., Keshri P., Sun J., Rizzo E.M., Gopalakrishnan S., Farkas M.E., et al. High-Content and High-Throughput Identification of Macrophage Polarization Phenotypes. Chem. Sci. 2020;11:8231–8239. doi: 10.1039/D0SC02792H. PubMed DOI PMC
Zhao Y., Huang Y., Liu H., Tan K., Wang R., Jia L., Li W. Macrophages with Different Polarization Phenotypes Influence Cementoblast Mineralization through Exosomes. Stem Cells Int. 2022;2022:4185972. doi: 10.1155/2022/4185972. PubMed DOI PMC
Barros M.H.M., Hauck F., Dreyer J.H., Kempkes B., Niedobitek G. Macrophage Polarisation: An Immunohistochemical Approach for Identifying M1 and M2 Macrophages. PLoS ONE. 2013;8:e80908. doi: 10.1371/journal.pone.0080908. PubMed DOI PMC
Wang Z., Gerstein M., Snyder M. Rna-Seq: A Revolutionary Tool for Transcriptomics. Nat. Rev. Genet. 2009;10:57–63. doi: 10.1038/nrg2484. PubMed DOI PMC
Daniel B., Belk J.A., Meier S.L., Chen A.Y., Sandor K., Czimmerer Z., Varga Z., Bene K., Buquicchio F.A., Qi Y., et al. Macrophage Inflammatory and Regenerative Response Periodicity Is Programmed by Cell Cycle and Chromatin State. Mol. Cell. 2022;83:121–138.e7. doi: 10.1016/j.molcel.2022.11.017. PubMed DOI PMC
Haider S., Pal R. Integrated Analysis of Transcriptomic and Proteomic Data. Curr. Genom. 2013;14:91–110. doi: 10.2174/1389202911314020003. PubMed DOI PMC
He L., Jhong J.-H., Chen Q., Huang K.-Y., Strittmatter K., Kreuzer J., DeRan M., Wu X., Lee T.-Y., Slavov N., et al. Global Characterization of Macrophage Polarization Mechanisms and Identification of M2-Type Polarization Inhibitors. Cell Rep. 2021;37:109955. doi: 10.1016/j.celrep.2021.109955. PubMed DOI PMC
Oishi S., Takano R., Tamura S., Tani S., Iwaizumi M., Hamaya Y., Takagaki K., Nagata T., Seto S., Horii T., et al. M2 Polarization of Murine Peritoneal Macrophages Induces Regulatory Cytokine Production and Suppresses T-Cell Proliferation. Immunology. 2016;149:320–328. doi: 10.1111/imm.12647. PubMed DOI PMC
Zogbi C., Oliveira N.C., Levy D., Bydlowski S.P., Bassaneze V., Neri E.A., Krieger J.E. Beneficial Effects of Il-4 and Il-6 on Rat Neonatal Target Cardiac Cells. Sci. Rep. 2020;10:12350. doi: 10.1038/s41598-020-69413-0. PubMed DOI PMC
Herb M., Schatz V., Hadrian K., Hos D., Holoborodko B., Jantsch J., Brigo N. Macrophage Variants in Laboratory Research: Most Are Well Done, But Some are RAW. Front. Cell. Infect. Microbiol. 2024;14:1457323. doi: 10.3389/fcimb.2024.1457323. PubMed DOI PMC
Toda G., Yamauchi T., Kadowaki T., Ueki K. Preparation and Culture of Bone Marrow-Derived Macrophages from Mice for Functional Analysis. STAR Protoc. 2021;2:100246. doi: 10.1016/j.xpro.2020.100246. PubMed DOI PMC
Patel A.A., Ginhoux F., Yona S. Monocytes, Macrophages, Dendritic Cells and Neutrophils: An Update on Lifespan Kinetics in Health and Disease. Immunology. 2021;163:250–261. doi: 10.1111/imm.13320. PubMed DOI PMC
Sim S.L., Kumari S., Kaur S., Khosrotehrani K. Macrophages in Skin Wounds: Functions and Therapeutic Potential. Biomolecules. 2022;12:1659. doi: 10.3390/biom12111659. PubMed DOI PMC
Souci L., Denesvre C. 3D Skin Models in Domestic Animals. Veter. Res. 2021;52:21. doi: 10.1186/s13567-020-00888-5. PubMed DOI PMC
Zhou L., Jiang A., Veenstra J., Ozog D.M., Mi Q.-S. The Roles of Skin Langerhans Cells in Immune Tolerance and Cancer Immunity. Vaccines. 2022;10:1380. doi: 10.3390/vaccines10091380. PubMed DOI PMC
Lee S.H., Sacks D.L. Resilience of Dermis Resident Macrophages to Inflammatory Challenges. Exp. Mol. Med. 2024;56:2105–2112. doi: 10.1038/s12276-024-01313-z. PubMed DOI PMC
Mass E., Nimmerjahn F., Kierdorf K., Schlitzer A. Tissue-Specific Macrophages: How They Develop and Choreograph Tissue Biology. Nat. Rev. Immunol. 2023;23:563–579. doi: 10.1038/s41577-023-00848-y. PubMed DOI PMC
Neagu M., Constantin C., Jugulete G., Cauni V., Dubrac S., Szöllősi A.G., Zurac S. Langerhans Cells—Revising Their Role in Skin Pathologies. J. Pers. Med. 2022;12:2072. doi: 10.3390/jpm12122072. PubMed DOI PMC
Yan B., Liu N., Li J., Li J., Zhu W., Kuang Y., Chen X., Peng C. The Role of Langerhans Cells in Epidermal Homeostasis and Pathogenesis of Psoriasis. J. Cell. Mol. Med. 2020;24:11646–11655. doi: 10.1111/jcmm.15834. PubMed DOI PMC
Monnier M., Paolini L., Vinatier E., Mantovani A., Delneste Y., Jeannin P. Antitumor Strategies Targeting Macrophages: The Importance of Considering the Differences in Differentiation/Polarization Processes between Human and Mouse Macrophages. J. Immunother. Cancer. 2022;10:e005560. doi: 10.1136/jitc-2022-005560. PubMed DOI PMC
Poltavets A.S., Vishnyakova P.A., Elchaninov A.V., Sukhikh G.T., Fatkhudinov T.K. Macrophage Modification Strategies for Efficient Cell Therapy. Cells. 2020;9:1535. doi: 10.3390/cells9061535. PubMed DOI PMC
Zschaler J., Schlorke D., Arnhold J. Differences in Innate Immune Response between Man and Mouse. Crit. Rev. Immunol. 2014;34:433–454. doi: 10.1615/CritRevImmunol.2014011600. PubMed DOI
Shi Y., Zhu N., Qiu Y., Tan J., Wang F., Qin L., Dai A. Resistin-Like Molecules: A Marker, Mediator and Therapeutic Target for Multiple Diseases. Cell Commun. Signal. 2023;21:1–22. doi: 10.1186/s12964-022-01032-w. PubMed DOI PMC
Bailey J.D., Diotallevi M., Nicol T., McNeill E., Shaw A., Chuaiphichai S., Hale A., Starr A., Nandi M., Stylianou E., et al. Nitric Oxide Modulates Metabolic Remodeling in Inflammatory Macrophages through Tca Cycle Regulation and Itaconate Accumulation. Cell Rep. 2019;28:218–230.e7. doi: 10.1016/j.celrep.2019.06.018. PubMed DOI PMC