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Mast cells mediate acute inflammatory responses to implanted biomaterials
Open accessAbstract
Implanted biomaterials trigger acute and chronic inflammatory responses. The mechanisms involved in such acute inflammatory responses can be arbitrarily divided into phagocyte transmigration, chemotaxis, and adhesion to implant surfaces. We earlier observed that two chemokines-macrophage inflammatory protein 1alpha/monocyte chemoattractant protein 1-and the phagocyte integrin Mac-1 (CD11b/CD18)/surface fibrinogen interaction are, respectively, required for phagocyte chemotaxis and adherence to biomaterial surfaces. However, it is still not clear how the initial transmigration of phagocytes through the endothelial barrier into the area of the implant is triggered. Because implanted biomaterials elicit histaminic responses in the surrounding tissue, and histamine release is known to promote rapid diapedesis of inflammatory cells, we evaluated the possible role of histamine and mast cells in the recruitment of phagocytes to biomaterial implants. Using i.p. and s. c. implantation of polyethylene terephthalate disks in mice we find: (i) Extensive degranulation of mast cells, accompanied by histamine release, occurs adjacent to short-term i.p. implants. (ii) Simultaneous administration of H1 and H2 histamine receptor antagonists (pyrilamine and famotidine, respectively) greatly diminishes recruitment and adhesion of both neutrophils (<20% of control) and monocytes/macrophages (<30% of control) to implants. (iii) Congenitally mast cell-deficient mice also exhibit markedly reduced accumulation of phagocytes on both i.p. and s.c implants. (iv) Finally, mast cell reconstitution of mast cell-deficient mice restores "normal" inflammatory responses to biomaterial implants. We conclude that mast cells and their granular products, especially histamine, are important in recruitment of inflammatory cells to biomaterial implants. Improved knowledge of such responses may permit purposeful modulation of both acute and chronic inflammation affecting implanted biomaterials.
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“The recruitment is mediated by mast cells, which secrete granular products that attract and promote the adhesion of monocytes and macrophages to the implant.[ 34 ]”
From Unraveling and Harnessing the Immune Response at the Cell–Biomaterial Interface for Tissue Engineering Purposes (2024) · cites this paper as [34]
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“Mast cell degranulation with histamine release and fibrinogen adsorption is known to mediate acute inflammatory responses to implanted biomaterials.[6, 7]”
From Foreign body reaction to biomaterials (2008) · cites this paper as [7]
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“In addition, mast cell degranulation and release of histamine has been shown to play an integral role in recruiting phagocytes, including macrophages, to the site of the implanted biomaterial.[7]”
From Foreign body reaction to biomaterials (2008) · cites this paper as [7]
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The Effects of Cimetidine, Ranitidine, and Famotidine on Human Neutrophil Functions
Mikawa, K., Akamatsu, H., Nishina, K., Shiga, M., Nobuhiro Maekawa, A., Obara, H., & Niwa, Y. (1999) · Anesthesia & Analgesia · doi:10.1097/00000539-199907000-00040 · Cited by 49
“Conflicting in vitro data on the effects of the H2-receptor antagonists on neutrophil chemotaxis have been also reported (12,14, 25 ).”
BackgroundCritical role of tissue mast cells in controlling long-term glucose sensor function in vivo
Klueh, U., Kaur, M., Qiao, Y., & Kreutzer, D. L. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.02.023 · Cited by 48
“In fact, we were able to find only one study on murine mast cells and biomaterials in vivo in the entire literature [7].”
BackgroundAttenuation of acid induced oesophagitis in VR-1 deficient mice
Fujino, K., de la Fuente, S. G., Takami, Y., Takahashi, T., & Mantyh, C. R. (2005) · Gut · doi:10.1136/gut.2005.066795 · Cited by 47
Avula, M., Rao, A. N., McGill, L. D., Grainger, D. W., & Solzbacher, F. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.08.090 · Cited by 48
“MC degranulation of histamine and other pro-inflammatory mediators including heparin, cytokines (TNF-alpha), chemokines, and many proteases together with fibrinogen adsorption are recognized as powerful inducers of acute inflammatory responses to implanted biomaterials [21,22].”
BackgroundInfluence of scaffold design on host immune and stem cell responses
Nair, A., & Tang, L. (2017) · Seminars in Immunology · doi:10.1016/j.smim.2017.03.001 · Cited by 46
“In fact, this histamine mediated inflammatory cell recruitment that is enabled by adsorbed fibrinogen can be minimized by administration of H1 and H2 histamine receptor antagonists [10,11].”
BackgroundSelf-citationNguyen, K. T., Shaikh, N., Shukla, K. P., Su, S., Eberhart, R. C., & Tang, L. (2004) · Biomaterials · doi:10.1016/j.biomaterials.2003.12.033 · Cited by 45
Self-citationAccelerated Clearance of Escherichia coli in Experimental Peritonitis of Histamine-Deficient Mice
Hori, Y., Nihei, Y., Kurokawa, Y., Kuramasu, A., Makabe‐Kobayashi, Y., Terui, T., Doi, H., Satomi, S., Sakurai, E., Nagy, A., et al. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.4.1978 · Cited by 45
“model (18) and in the reaction to implanted biomaterials (11).”
BackgroundMethodInfluentialKitano, M., Norlén, P., & Håkanson, R. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(99)00096-8 · Cited by 45
Durand, M., Barbier, L., Mathieu, L., Poyot, T., Demoures, T., Souraud, J.-B., Masquelet, A., & Collombet, J.-M. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020450 · Cited by 44
Goonoo, N., Gimié, F., Aït-Arsa, I., Cordonin, C., Andries, J., Jhurry, D., & Bhaw‐Luximon, A. (2021) · Biomaterials Science · doi:10.1039/d1bm00379h · Cited by 43
Piatnitskaia, S., Альбертовна, Р. Г., Bilyalov, A. R., Chugunov, S. S., Akhatov, I., Павлов, В. Н., & Kzhyshkowska, J. G. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1349461 · Cited by 45
Hoene, A., Prinz, C., Walschus, U., Lucke, S., Patrzyk, M., Wilhelm, L., Neumann, H. G., & Schlosser, M. (2013) · Biomedical Materials · doi:10.1088/1748-6041/8/3/035009 · Cited by 43
“Other inflammatory and immune cells which were found after implantation of biomaterials include mast cells [10] and natural killer cells [11].”
Effects of mast cell modulation on early host response to implanted synthetic meshes
Orenstein, S. B., Saberski, E. R., Klueh, U., Kreutzer, D. L., & Novitsky, Y. W. (2010) · Hernia · doi:10.1007/s10029-010-0680-1 · Cited by 42
“Many of these products are reported to alter the phenotype and promote migration of inXammatory and immunoregulatory cells [ 13 , 14, 26].”
BackgroundResultInfluentialOki, T., Kitaura, J., Eto, K., Yang, L., Maeda‐Yamamoto, M., Inagaki, N., Nagai, H., Yamanishi, Y., Nakajina, H., Kumagai, H., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.1.52 · Cited by 41
“In contrast, mast cells also participate in a wide variety of pathological processes independent of IgE, including innate immune response (1, 2, 6), tissue repair (1, 2, 7), acute inflammatory response to implanted biomaterials (8), atherosclerosis (9), and certain autoimmune disorders (10).”
BackgroundLudwicka, K., Kołodziejczyk, M., Gendaszewska‐Darmach, E., Chrzanowski, M., Jędrzejczak‐Krzepkowska, M., Rytczak, P., & Bielecki, S. (2018) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34191 · Cited by 40
Reifenrath, J., Wellmann, M., Kempfert, M., Angrisani, N., Welke, B., Gniesmer, S., Kampmann, A., Menzel, H., & Willbold, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031046 · Cited by 44
“[50] these findings lead to the conclusion that mast cells mediated particularly the phagocytosis and therewith degradation of the implanted scaffolds rather than an inflammatory response.”
BackgroundResultInnate and adaptive immune responses in tissue engineering
Sefton, M. V., Babensee, J. E., & Woodhouse, K. A. (2008) · Seminars in Immunology · doi:10.1016/j.smim.2007.12.008 · Cited by 40
“Mast cells release histamine in response to implants, encouraging the recruitment of inflammatory cells to the wound site [124].”
BackgroundBiomaterials-Driven Sterile Inflammation
Chen, H., Agrawal, D. K., & Thankam, F. G. (2022) · Tissue Engineering Part B: Reviews · doi:10.1089/ten.teb.2020.0253 · Cited by 41
“93,94 95–97 The critical role of mast cells and mast cell degranulation at the implant surface, and response to DAMP activation and their prohealing/regenerative effects warrant further research.”
Current Trends in Improving of Artificial Joints Design and Technologies for Their Arthroplasty
Poliakov, A., Pakhaliuk, V., & Popov, V. L. (2020) · Frontiers in Mechanical Engineering · doi:10.3389/fmech.2020.00004 · Cited by 41
“In addition, mast cell degranulation affects the inflammatory process, which leads to the release of cytokines and histamine, which enhance the immune response (Tang et al., 1998).”
BackgroundLove, R. J., & Jones, K. S. (2013) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.34577 · Cited by 39
Klinkhammer, K., Bockelmann, J., Simitzis, C., Brook, G. A., Grafahrend, D., Gröll, J., Möller, M., Mey, J., & Klee, D. (2010) · Journal of Materials Science Materials in Medicine · doi:10.1007/s10856-010-4112-7 · Cited by 39
“Protein adsorption data suggested that PPol-PEG3 fibers might reduce inflammatory reactions or encapsulation in vivo [8, 9].”
The State of the Art and Prospects for Osteoimmunomodulatory Biomaterials
Negrescu, A. M., & Cîmpean, A. (2021) · Materials · doi:10.3390/ma14061357 · Cited by 42
“Moreover, the adsorbed host fibrinogen, coupled with the histamine release from the mast cells, mediates the acute inflammatory response through the recruitment and adhesion of phagocytes to the implant surface [71,72].”
BackgroundLatest advances: Improving the anti-inflammatory and immunomodulatory properties of PEEK materials
Zhang, Z., Zhang, X., Zheng, Z., Xin, J., Han, S., Qi, J., Zhang, T., Wang, Y., & Zhang, S. (2023) · Materials Today Bio · doi:10.1016/j.mtbio.2023.100748 · Cited by 39
“The release of these cytokines and substances has a significant effect on the subsequent inflammatory response [18,19].”
BackgroundKo, C.-Y., Wu, L., Nair, A., Tsai, Y., Lin, V. K., & Tang, L. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.10.002 · Cited by 37
Self-citationInfluence of polymer molecular weight in osteoinductive composites for bone tissue regeneration
Barbieri, D., Yuan, H., Luo, X., Farè, S., Grijpma, D. W., & de Bruijn, J. D. (2013) · Acta Biomaterialia · doi:10.1016/j.actbio.2013.07.026 · Cited by 37
Macrophage Polarization in Response to Biomaterials for Vascularization
Wang, Y., Fan, Y., & Liu, H. (2021) · Annals of Biomedical Engineering · doi:10.1007/s10439-021-02832-w · Cited by 37
Debprasad, C., Mukherjee, H., Bag, P., Ojha, D., Kumar, K. A., Dutta, S., Kumar, H. P., Chatterjee, T., Sharon, A., & Chakraborti, S. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/254849 · Cited by 37
In vitro and in vivo anti-inflammatory potential of Cryptolepis buchanani
Laupattarakasem, P., Wangsrimongkol, T., Surarit, R., & Hahnvajanawong, C. (2006) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2006.05.029 · Cited by 37
Sabareeswaran, A., Beeran, A. E., Varma, P. R. V. H., Valappil, M. P., & Kumary, T. V. (2016) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2016.02.018 · Cited by 36
Metadata
- Authors
- Tang, L., Jennings, T. A., & Eaton, J. W.
- Affiliations
- Baylor College of Medicine (US)
- ORCID
- Tang, Liping
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1998-07-21
- Volume
- 95
- Issue
- 15
- Pages
- 8841-8846
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC21164
- OpenAlex
- W2037046845
- Cited by
- 272
- References
- 78
- Citations by year
- 2026: 1 · 2025: 8 · 2024: 8 · 2023: 6 · 2022: 4 · 2021: 18 · 2020: 19 · 2019: 8 · 2018: 11 · 2017: 19 · 2016: 16 · 2015: 12 · 2014: 8 · 2013: 14 · 2012: 8
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Surgery › Orthopaedic implants and arthroplasty
- Keywords
- mast cells, histamine, biomaterial implantation, acute inflammation, phagocyte recruitment, neutrophil transmigration, monocyte adhesion, histamine H1 receptor antagonists, H2 receptor antagonists, mast cell-deficient mice, transendothelial migration, macrophage inflammatory protein-1alpha, Mac-1
- MeSH terms
- Animals, Biocompatible Materials, Histamine, Histamine Release, Inflammation, Mast Cells, Phagocytes, Cell Degranulation, Mice
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