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The role of Toll-like receptor signaling in the macrophage response to implanted materials

Published online by Cambridge University Press:  06 December 2019

Laura A. McKiel
Affiliation:
Department of Chemical Engineering, Queen's University, Dupuis Hall, Room 201, 19 Division St, Kingston, Ontario, CanadaK7K 3N6
Kimberly A. Woodhouse
Affiliation:
Department of Chemical Engineering, Queen's University, Dupuis Hall, Room 201, 19 Division St, Kingston, Ontario, CanadaK7K 3N6
Lindsay E. Fitzpatrick*
Affiliation:
Department of Chemical Engineering, Queen's University, Dupuis Hall, Room 201, 19 Division St, Kingston, Ontario, CanadaK7K 3N6
*
Address all correspondence to Lindsay E. Fitzpatrick at lindsay.fitzpatrick@queensu.ca
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Abstract

Inflammation is facilitated largely by macrophages and other white blood cells, which recognize and respond to evolutionarily conserved damage-associated molecular patterns that are released upon tissue injury and cell stress. Damage-associated molecular patterns are known to bind Toll-like receptors (TLRs) and initiate inflammatory responses through MyD88-dependent NF-κB signaling. Biomaterial implantation activates the innate immune system, resulting in a chronic inflammatory response known as a foreign body reaction (FBR). In this review, the authors discuss the current understanding of damage-initiated TLR signaling in the FBR and the significance of this response in the success of implanted devices.

Type
Prospective Articles
Copyright
Copyright © Materials Research Society 2019

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References

1.Anderson, J.M., Rodriguez, A., and Chang, D.T.: Foreign body reaction to biomaterials. Semin. Immunol. 20, 86 (2008).CrossRefGoogle ScholarPubMed
2.Babensee, J.E.: Interaction of dendritic cells with biomaterials. Semin. Immunol. 20, 101 (2008).CrossRefGoogle ScholarPubMed
3.Luttikhuizen, D.T., Van Amerongen, M.J., De Feijter, P.C., Petersen, A.H., Harmsen, M.C., and Van Luyn, M.J.A.: The correlation between difference in foreign body reaction between implant locations and cytokine and MMP expression. Biomaterials 27, 5763 (2006).CrossRefGoogle ScholarPubMed
4.McKiel, L.A. and Fitzpatrick, L.E.: Toll-like receptor 2-dependent NF-κB/AP-1 activation by damage-associated molecular patterns adsorbed on polymeric surfaces. ACS Biomater. Sci. Eng. 4, 3792 (2018).CrossRefGoogle Scholar
5.Blakney, A.K., Swartzlander, M.D., and Bryant, S.J.: The effects of substrate stiffness on the in vitro activation of macrophages and in vivo host response to poly(ethylene glycol)-based hydrogels. J. Biomed. Mater. Res. A 100, 1375 (2012).CrossRefGoogle ScholarPubMed
6.Chen, S., Jones, J.A., Xu, Y., Low, H.-Y., Anderson, J.M., and Leong, K.W.: Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31, 3479 (2010).CrossRefGoogle Scholar
7.Gessner, A., Lieske, A., Paulke, B., and Müller, R.: Influence of surface charge density on protein adsorption on polymeric nanoparticles: analysis by two-dimensional electrophoresis. Eur. J. Pharm. Biopharm. 54, 165 (2002).CrossRefGoogle ScholarPubMed
8.Veiseh, O., Doloff, J.C., Ma, M., Vegas, A.J., Tam, H.H., Bader, A.R., Li, J., Langan, E., Wyckoff, J., Loo, W.S., Jhunjhunwala, S., Chiu, A., Siebert, S., Tang, K., Hollister-Lock, J., Aresta-Dasilva, S., Bochenek, M., Mendoza-Elias, J., Wang, Y., Qi, M., Lavin, D.M., Chen, M., Dholakia, N., Thakrar, R., Lacík, I., Weir, G.C., Oberholzer, J., Greiner, D.L., Langer, R., and Anderson, D.G.: Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates. Nat. Mater. 14, 643 (2015).CrossRefGoogle ScholarPubMed
9.Slack, S.M., Bohnert, J.L., and Horbett, T.A.: The effects of surface chemistry and coagulation factors on fibrinogen adsorption from plasma. Ann. N. Y. Acad. Sci. 516, 223 (1987).CrossRefGoogle ScholarPubMed
10.Norris, D.A., Clark, R.A., Swigart, L.M., Huff, J.C., Weston, W.L., and Howell, S.E.: Fibronectin fragment(s) are chemotactic for human peripheral blood monocytes. J. Immunol. 129, 1612 (1982).Google ScholarPubMed
11.Zhou, J., Tsai, Y.-T., Weng, H., Baker, D.W., and Tang, L.: Real time monitoring of biomaterial-mediated inflammatory responses via macrophage-targeting NIR nanoprobes. Biomaterials 32, 9383 (2011).CrossRefGoogle ScholarPubMed
12.Bonfield, T.L., Colton, E., Marchant, R.E., and Anderson, J.M.: Cytokine and growth factor production by monocytes/macrophages on protein preadsorbed polymers. J. Biomed. Mater. Res. 26, 837 (1992).CrossRefGoogle ScholarPubMed
13.Leibovich, S.J. and Ross, R.: The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am. J. Pathol. 78, 71 (1975).Google ScholarPubMed
14.Doloff, J.C., Veiseh, O., Vegas, A.J., Tam, H.H., Farah, S., Ma, M., Li, J., Bader, A., Chiu, A., Sadraei, A., Aresta-Dasilva, S., Griffin, M., Jhunjhunwala, S., Webber, M., Siebert, S., Tang, K., Chen, M., Langan, E., Dholokia, N., Thakrar, R., Qi, M., Oberholzer, J., Greiner, D.L., Langer, R., and Anderson, D.G.: Colony stimulating factor-1 receptor is a central component of the foreign body response to biomaterial implants in rodents and non-human primates. Nat. Mater. 16, 671 (2017).CrossRefGoogle ScholarPubMed
15.Cannon, G.J. and Swanson, J.A.: The macrophage capacity for phagocytosis. J. Cell Sci. 101, 907 (1992).Google ScholarPubMed
16.Bonfield, T.L., Colton, E., and Anderson, J.M.: Plasma protein adsorbed biomedical polymers: activation of human monocytes and induction of interleukin 1. J. Biomed. Mater. Res. 23, 535 (1989).CrossRefGoogle ScholarPubMed
17.Collier, T.O. and Anderson, J.M.: Protein and surface effects on monocyte and macrophage adhesion, maturation, and survival. J. Biomed. Mater. Res. 60, 487 (2002).CrossRefGoogle ScholarPubMed
18.Zhao, Q., Topham, N., Anderson, J.M., Hiltner, A., Lodoen, G., and Payet, C.R.: Foreign-body giant cells and polyurethane biostability: in vivo correlation of cell adhesion and surface cracking. J. Biomed. Mater. Res. 25, 177 (1991).CrossRefGoogle ScholarPubMed
19.Kreipe, H., Radzun, H.J., Rudolph, P., Barth, J., Hansmann, M.L., Heidorn, K., and Parwaresch, M.R.: Multinucleated giant cells generated in vitro. Terminally differentiated macrophages with down-regulated c-fms expression. Am. J. Pathol. 130, 232 (1988).Google ScholarPubMed
20.MacLauchlan, S., Skokos, E.A., Meznarich, N., Zhu, D.H., Raoof, S., Shipley, J.M., Senior, R.M., Bornstein, P., and Kyriakides, T.R.: Macrophage fusion, giant cell formation, and the foreign body response require matrix metalloproteinase 9. J. Leukoc. Biol. 85, 617 (2009).CrossRefGoogle ScholarPubMed
21.Hauzenberger, J.R., Hipszer, B.R., Loeum, C., McCue, P.A., DeStefano, M., Torjman, M.C., Kaner, M.T., Dinesen, A.R., Chervoneva, I., Pieber, T.R., and Joseph, J.I.: Detailed analysis of insulin absorption variability and the tissue response to continuous subcutaneous insulin infusion catheter implantation in Swine. Diabetes Technol. Ther. 19, 641 (2017).CrossRefGoogle ScholarPubMed
22.Hauzenberger, J.R., Münzker, J., Kotzbeck, P., Asslaber, M., Bubalo, V., Joseph, J.I., and Pieber, T.R.: Systematic in vivo evaluation of the time-dependent inflammatory response to steel and Teflon insulin infusion catheters. Sci. Rep. 8, 1132 (2018).CrossRefGoogle ScholarPubMed
23.Pickup, J.C., Yemane, N., Brackenridge, A., and Pender, S.: Nonmetabolic complications of continuous subcutaneous insulin infusion: a patient survey. Diabetes Technol. Ther. 16, 145 (2014).CrossRefGoogle ScholarPubMed
24.Sutherland, K., Mahoney, J.R. 2nd, Coury, A.J., and Eaton, J.W.: Degradation of biomaterials by phagocyte-derived oxidants. J. Clin. Invest. 92, 2360 (1993).CrossRefGoogle ScholarPubMed
25.Picha, G.J., Goldstein, J.A., and Stohr, E.: Natural-Y Même polyurethane versus smooth silicone: analysis of the soft-tissue interaction from 3 days to 1 year in the rat animal model. Plast. Reconstr. Surg. 85, 903 (1990).CrossRefGoogle ScholarPubMed
26.Wiggins, M.J., Wilkoff, B., Anderson, J.M., and Hiltner, A.: Biodegradation of polyether polyurethane inner insulation in bipolar pacemaker leads. J. Biomed. Mater. Res. 58, 302 (2001).3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
27.Anderson, J.M. and Miller, K.M.: Biomaterial biocompatibility and the macrophage. Biomaterials 5, 21 (1984).CrossRefGoogle ScholarPubMed
28.Amer, L.D., Saleh, L.S., Walker, C., Thomas, S., Janssen, W.J., Alper, S., and Bryant, S.J.: Inflammation via myeloid differentiation primary response gene 88 signaling mediates the fibrotic response to implantable synthetic poly(ethylene glycol) hydrogels. Acta Biomater. 100, 105 (2019).CrossRefGoogle ScholarPubMed
29.Brash, J. and ten Hove, P.: Effect of plasma dilution on adsorption of fibrinogen to solid surfaces. Thromb. Haemost. 51, 326 (1984).Google ScholarPubMed
30.Ellingsen, J.E.: A study on the mechanism of protein adsorption to TiO2. Biomaterials 12, 593 (1991).CrossRefGoogle Scholar
31.Horbett, T.A.: Mass action effects on competitive adsorption of fibrinogen from hemoglobin solutions and from plasma. Thromb. Haemost. 51, 174 (1984).Google ScholarPubMed
32.Horbett, T.A., Weathersby, P.K., and Hoffman, A.S.: The preferential adsorption of hemoglobin to polyethylene. J. Bioeng. 1, 61 (1977).Google ScholarPubMed
33.Roach, P., Farrar, D., and Perry, C.C.: Interpretation of protein adsorption: surface-induced conformational changes. J. Am. Chem. Soc. 127, 8168 (2005).CrossRefGoogle ScholarPubMed
34.Undin, T., Lind, S.B., and Dahlin, A.P.: MS for investigation of time-dependent protein adsorption on surfaces in complex biological samples. Future Sci. OA 1, FSO32 (2015).CrossRefGoogle ScholarPubMed
35.Wojciechowski, P., Ten Hove, P., and Brash, J.L.: Phenomenology and mechanism of the transient adsorption of fibrinogen from plasma (Vroman effect). J. Colloid Interface Sci. 111, 455 (1986).CrossRefGoogle Scholar
36.Vyner, M.C. and Amsden, B.G.: Polymer chain flexibility-induced differences in fetuin A adsorption and its implications on cell attachment and proliferation. Acta Biomater. 31, 89 (2016).CrossRefGoogle ScholarPubMed
37.Fitzpatrick, L.E., Chan, J.W.Y., and Sefton, M.V.: On the mechanism of poly(methacrylic acid –co– methyl methacrylate)-induced angiogenesis: gene expression analysis of dTHP-1 cells. Biomaterials 32, 8957 (2011).CrossRefGoogle ScholarPubMed
38.Milleret, V., Buzzi, S., Gehrig, P., Ziogas, A., Grossmann, J., Schilcher, K., Zinkernagel, A.S., Zucker, A., and Ehrbar, M.: Protein adsorption steers blood contact activation on engineered cobalt chromium alloy oxide layers. Acta Biomater. 24, 343 (2015).CrossRefGoogle ScholarPubMed
39.Wells, L.A., Guo, H., Emili, A., and Sefton, M.V.: The profile of adsorbed plasma and serum proteins on methacrylic acid copolymer beads: effect on complement activation. Biomaterials 118, 74 (2017).CrossRefGoogle ScholarPubMed
40.Andrade, J.D. and Hlady, V.: Plasma protein adsorption: the big twelve. Ann. N. Y. Acad. Sci. 516, 158 (1987).CrossRefGoogle ScholarPubMed
41.Martin, D.C., Semple, J.L., and Sefton, M.V.: Poly(methacrylic acid-co-methyl methacrylate) beads promote vascularization and wound repair in diabetic mice. J. Biomed. Mater. Res. A 93A, 484 (2009).Google Scholar
42.Swartzlander, M.D., Barnes, C.A., Blakney, A.K., Kaar, J.L., Kyriakides, T.R., and Bryant, S.J.: Linking the foreign body response and protein adsorption to PEG-based hydrogels using proteomics. Biomaterials 41, 26 (2015).CrossRefGoogle ScholarPubMed
43.Andersson, J., Ekdahl, K.N., Larsson, R., Nilsson, U.R., and Nilsson, B.: C3 adsorbed to a polymer surface can form an initiating alternative pathway convertase. J. Immunol. 168, 5786 (2002).CrossRefGoogle ScholarPubMed
44.Gleissner, C.A., Shaked, I., Little, K.M., and Ley, K.: CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J. Immunol. 184, 4810 (2010).CrossRefGoogle ScholarPubMed
45.Tzeng, D.Y., Deuel, T.F., Huang, J.S., and Baehner, R.L.: Platelet-derived growth factor promotes human peripheral monocyte activation. Blood 66, 179 (1985).CrossRefGoogle ScholarPubMed
46.Broughton, G., Janis, J.E., and Attinger, C.E.: The basic science of wound healing. Plast. Reconstr. Surg. 117, 12S (2006).CrossRefGoogle ScholarPubMed
47.Edwards, J.P., Zhang, X., Frauwirth, K.A., and Mosser, D.M.: Biochemical and functional characterization of three activated macrophage populations. J. Leukoc. Biol. 80, 1298 (2006).CrossRefGoogle ScholarPubMed
48.Mariani, T.J., Sandefur, S., Roby, J.D., and Pierce, R.A.: Collagenase-3 induction in rat lung fibroblasts requires the combined effects of tumor necrosis factor-alpha and 12-lipoxygenase metabolites: a model of macrophage-induced, fibroblast-driven extracellular matrix remodeling during inflammatory lung injury. Mol. Biol. Cell 9, 1411 (1998).CrossRefGoogle Scholar
49.Wiegand, C., Schönfelder, U., Abel, M., Ruth, P., Kaatz, M., and Hipler, U.-C.: Protease and pro-inflammatory cytokine concentrations are elevated in chronic compared to acute wounds and can be modulated by collagen type I in vitro. Arch. Dermatol. Res. 302, 419 (2010).CrossRefGoogle ScholarPubMed
50.Flick, M.J., Du, X., Witte, D.P., Jirousková, M., Soloviev, D.A., Busuttil, S.J., Plow, E.F., and Degen, J.L.: Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J. Clin. Invest. 113, 1596 (2004).CrossRefGoogle ScholarPubMed
51.Kovacsovics-Bankowski, M., Clark, K., Benacerraf, B., and Rock, K.L.: Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc. Natl. Acad. Sci. USA 90, 4942 (1993).CrossRefGoogle Scholar
52.Hallab, N.J., McAllister, K., Brady, M., and Jarman-Smith, M.: Macrophage reactivity to different polymers demonstrates particle size- and material-specific reactivity: PEEK-OPTIMA® particles versus UHMWPE particles in the submicron, micron, and 10 micron size ranges. J. Biomed. Mater. Res. B Appl. Biomater. 100B, 480 (2012).CrossRefGoogle Scholar
53.Brodbeck, W.G., Patel, J., Voskerician, G., Christenson, E., Shive, M.S., Nakayama, Y., Matsuda, T., Ziats, N.P., and Anderson, J.M.: Biomaterial adherent macrophage apoptosis is increased by hydrophilic and anionic substrates in vivo. Proc. Natl. Acad. Sci. USA 99, 10287 (2002).CrossRefGoogle ScholarPubMed
54.Stein, M., Keshav, S., Harris, N., and Gordon, S.: Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176, 287 (1992).CrossRefGoogle ScholarPubMed
55.Anderson, J.M.: Inflammation, wound healing, and the foreign body response. In Biomaterials Science: An Introduction to Materials in Medicine, edited by Ratner, B., Hoffman, A., Schoen, F., and Lemons, J. (Elsevier, New York, 2004), p. 296.Google Scholar
56.Mcnally, A.K., Defife, K.M., and Anderson, J.M.: Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am. J. Pathol. 149, 975 (1996).Google ScholarPubMed
57.McNally, A.K., Jones, J.A., MacEwan, S.R., Colton, E., and Anderson, J.M.: Vitronectin is a critical protein adhesion substrate for IL-4-induced foreign body giant cell formation. J. Biomed. Mater. Res. A 86A, 535 (2008).CrossRefGoogle Scholar
58.McNally, A.K. and Anderson, J.M.: β1 and β2 integrins mediate adhesion during macrophage fusion and multinucleated foreign body giant cell formation. Am. J. Pathol. 160, 621 (2002).CrossRefGoogle ScholarPubMed
59.Brodbeck, W.G., Nakayama, Y., Matsuda, T., Colton, E., Ziats, N.P., and Anderson, J.M.: Biomaterial surface chemistry dictates adherent monocyte/macrophage cytokine expression in vitro. Cytokine 18, 311 (2002).CrossRefGoogle ScholarPubMed
60.Sridharan, R., Cameron, A.R., Kelly, D.J., Kearney, C.J., and O'Brien, F.J.: Biomaterial based modulation of macrophage polarization: a review and suggested design principles. Mater. Today 18, 313 (2015).CrossRefGoogle Scholar
61.Onuki, Y., Bhardwaj, U., Papadimitrakopoulos, F., and Burgess, D.J.: A review of the biocompatibility of implantable devices: current challenges to overcome foreign body response. J. Diabetes Sci. Technol. 2, 1003 (2008).CrossRefGoogle ScholarPubMed
62.Verreck, F.A.W., de Boer, T., Langenberg, D.M.L., Hoeve, M.A., Kramer, M., Vaisberg, E., Kastelein, R., Kolk, A., de Waal-Malefyt, R., and Ottenhoff, T.H.M.: Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc. Natl. Acad. Sci. USA 101, 4560 (2004).CrossRefGoogle ScholarPubMed
63.Bosisio, D., Polentarutti, N., Sironi, M., Bernasconi, S., Miyake, K., Webb, G.R., Martin, M.U., Mantovani, A., and Muzio, M.: Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by interferon-γ: a molecular basis for priming and synergism with bacterial lipopolysaccharide. Blood 99, 3427 (2002).CrossRefGoogle ScholarPubMed
64.Bota, P.C.S., Collie, A.M.B., Puolakkainen, P., Vernon, R.B., Sage, E.H., Ratner, B.D., and Stayton, P.S.: Biomaterial topography alters healing in vivo and monocyte/macrophage activation in vitro. J. Biomed. Mater. Res. A 95, 649 (2010).CrossRefGoogle ScholarPubMed
65.Deonarine, K., Panelli, M.C., Stashower, M.E., Jin, P., Smith, K., Slade, H.B., Norwood, C., Wang, E., Marincola, F.M., and Stroncek, D.F.: Gene expression profiling of cutaneous wound healing. J. Transl. Med. 5, 11 (2007).CrossRefGoogle ScholarPubMed
66.Madden, L.R., Mortisen, D.J., Sussman, E.M., Dupras, S.K., Fugate, J.A., Cuy, J.L., Hauch, K.D., Laflamme, M.A., Murry, C.E., and Ratner, B.D.: Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc. Natl. Acad. Sci. USA 107, 15211 (2010).CrossRefGoogle ScholarPubMed
67.Modolell, M., Corraliza, I.M., Link, F., Soler, G., and Eichmann, K.: Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH 1 and TH 2 cytokines. Eur. J. Immunol. 25, 1101 (1995).CrossRefGoogle Scholar
68.Krysko, D.V., Agostinis, P., Krysko, O., Garg, A.D., Bachert, C., Lambrecht, B.N., and Vandenabeele, P.: Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol. 32, 157 (2011).CrossRefGoogle ScholarPubMed
69.Smiley, S.T., King, J.A., and Hancock, W.W.: Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J. Immunol. 167, 2887 (2001).CrossRefGoogle ScholarPubMed
70.Ohashi, K., Burkart, V., Flohe, S., and Kolb, H.: Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J. Immunol. 164, 558 (2000).CrossRefGoogle ScholarPubMed
71.Stahl, P.D., Alan, R., and Ezekowitzt, B.: The mannose receptor is a pattern recognition receptor involved in host defense. Curr. Opin. Immunol. 10, 50 (1998).CrossRefGoogle ScholarPubMed
72.Peiser, L., Gough, P.J., Kodama, T., and Gordon, S.: Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect. Immun. 68, 1953 (2000).CrossRefGoogle Scholar
73.Józefowski, S., Arredouani, M., Sulahian, T., and Kobzik, L.: Disparate regulation and function of the class A scavenger receptors SR-AI/II and MARCO. J. Immunol. 175, 8032 (2005).CrossRefGoogle Scholar
74.Wang, H., Wu, L., and Reinhard, B.M.: Scavenger receptor mediated endocytosis of silver nanoparticles into J774A.1 macrophages is heterogeneous. ACS Nano 6, 7122 (2012).CrossRefGoogle ScholarPubMed
75.Sun, D.H., Trindade, M.C., Nakashima, Y., Maloney, W.J., Goodman, S.B., Schurman, D.J., and Smith, R.L.: Human serum opsonization of orthopedic biomaterial particles: protein-binding and monocyte/macrophage activation in vitro. J. Biomed. Mater. Res. A 65, 290 (2003).CrossRefGoogle ScholarPubMed
76.Müller, R.H., Rühl, D., Lück, M., and Paulke, B.-R.: Influence of fluorescent labelling of polystyrene particles on phagocytic uptake, surface hydrophobicity, and plasma protein adsorption. Pharm. Res. 14, 18 (1997).CrossRefGoogle ScholarPubMed
77.Kusner, D.J., Hall, C.F., and Jackson, S.: Fcγ receptor-mediated activation of phospholipase D regulates macrophage phagocytosis of IgG-opsonized particles. J. Immunol. 162, 2266 (1999).Google Scholar
78.Kemp, A. and Turner, M.: The role of opsonins in vacuolar sealing and the ingestion of zymosan by human neutrophils. Immunology 59, 69 (1986).Google ScholarPubMed
79.Wright, S.D. and Meyer, B.C.: Fibronectin receptor of human macrophages recognizes the sequence Arg-Gly-Asp-Ser. J. Exp. Med. 162, 762 (1985).CrossRefGoogle ScholarPubMed
80.Stahl, P.D. and Ezekowitz, R.A.: The mannose receptor is a pattern recognition receptor involved in host defense. Curr. Opin. Immunol. 10, 50 (1998).CrossRefGoogle ScholarPubMed
81.Netea, M.G., Nold-Petry, C.A., Nold, M.F., Joosten, L.A.B., Opitz, B., van der Meer, J.H.M., van de Veerdonk, F.L., Ferwerda, G., Heinhuis, B., Devesa, I., Funk, C.J., Mason, R.J., Kullberg, B.J., Rubartelli, A., van der Meer, J.W.M., and Dinarello, C.A.: Differential requirement for the activation of the inflammasome for processing and release of IL-1β in monocytes and macrophages. Blood 113, 2324 (2009).CrossRefGoogle ScholarPubMed
82.Caicedo, M.S., Desai, R., McAllister, K., Reddy, A., Jacobs, J.J., and Hallab, N.J.: Soluble and particulate Co-Cr-Mo alloy implant metals activate the inflammasome danger signaling pathway in human macrophages: a novel mechanism for implant debris reactivity. J. Orthop. Res. 27, 847 (2009).CrossRefGoogle ScholarPubMed
83.Ferko, M.-A. and Catelas, I.: Effects of metal ions on caspase-1 activation and interleukin-1β release in murine bone marrow-derived macrophages. PLoS One 13, e0199936 (2018).CrossRefGoogle ScholarPubMed
84.Vandanmagsar, B., Youm, Y.-H., Ravussin, A., Galgani, J.E., Stadler, K., Mynatt, R.L., Ravussin, E., Stephens, J.M., and Dixit, V.D.: The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179 (2011).CrossRefGoogle ScholarPubMed
85.Christo, S., Bachhuka, A., Diener, K.R., Vasilev, K., and Hayball, J.D.: The contribution of inflammasome components on macrophage response to surface nanotopography and chemistry. Sci. Rep. 6, 26207 (2016).CrossRefGoogle ScholarPubMed
86.Christo, S.N., Diener, K.R., Manavis, J., Grimbaldeston, M.A., Bachhuka, A., Vasilev, K., and Hayball, J.D.: Inflammasome components ASC and AIM2 modulate the acute phase of biomaterial implant-induced foreign body responses. Sci. Rep. 6, 20635 (2016).CrossRefGoogle ScholarPubMed
87.Solanki, P.R., Kaushik, A., Ansari, A.A., Sumana, G., and Malhotra, B.: Zinc oxide-chitosan nanobiocomposite for urea sensor. Appl. Phys. Lett. 93, 163903 (2008).CrossRefGoogle Scholar
88.Jameela, S.R., Kumary, T.V., Lal, A.V., and Jayakrishnan, A.: Progesterone-loaded chitosan microspheres: a long acting biodegradable controlled delivery system. J. Control Release 52, 17 (1998).CrossRefGoogle ScholarPubMed
89.Wu, W., Shen, J., Banerjee, P., and Zhou, S.: Chitosan-based responsive hybrid nanogels for integration of optical pH-sensing, tumor cell imaging and controlled drug delivery. Biomaterials 31, 8371 (2010).CrossRefGoogle ScholarPubMed
90.Gudmundsdottir, S., Lieder, R., Sigurjonsson, O.E., and Petersen, P.H.: Chitosan leads to downregulation of YKL-40 and inflammasome activation in human macrophages. J. Biomed. Mater. Res. A 103, 2778 (2015).CrossRefGoogle ScholarPubMed
91.Artlett, C.M., Sassi-Gaha, S., Rieger, J.L., Boesteanu, A.C., Feghali-Bostwick, C.A., and Katsikis, P.D.: The inflammasome activating caspase 1 mediates fibrosis and myofibroblast differentiation in systemic sclerosis. Arthritis Rheum. 63, 3563 (2011).CrossRefGoogle ScholarPubMed
92.Krissansen, G., Elliott, M., Lucas, C., Stomski, F., Berndt, M., Cheresh, D., Lopez, A., and Burns, G.: Identification of a novel integrin beta subunit expressed on cultured monocytes (macrophages). Evidence that one alpha subunit can associate with multiple beta subunits. J. Biol. Chem. 265, 823 (1990).Google ScholarPubMed
93.Guan, J.-L., Trevithick, J.E., and Hynes, R.: Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul. 2, 951 (1991).CrossRefGoogle ScholarPubMed
94.Suehiro, K., Gailit, J., and Plow, E.F.: Fibrinogen is a ligand for integrin α5β1 on endothelial cells. J. Biol. Chem. 272, 5360 (1997).CrossRefGoogle ScholarPubMed
95.Kamata, T., Wright, R., and Takada, Y.: Critical threonine and aspartic acid residues within the I domains of β2 integrins for interactions with intercellular adhesion molecule 1 (ICAM-1) and C3bi. J. Biol. Chem. 270, 12531 (1995).CrossRefGoogle Scholar
96.Xu, S., Wang, J., Wang, J.-H., and Springer, T.A.: Distinct recognition of complement iC3b by integrins αXβ2 and αMβ2. Proc. Natl. Acad. Sci. USA 114, 3403 (2017).CrossRefGoogle ScholarPubMed
97.Akira, S., Takeda, K., and Kaisho, T.: Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675 (2001).CrossRefGoogle ScholarPubMed
98.Triantafilou, M., Gamper, F.G., Haston, R.M., Mouratis, M.A., Morath, S., Hartung, T., and Triantafilou, K.: Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002 (2006).CrossRefGoogle ScholarPubMed
99.Mäkelä, S.M., Strengell, M., Pietilä, T.E., and Julkunen, I.: Multiple signaling pathways contribute to synergistic TLR ligand-dependent cytokine gene expression in human monocyte-derived macrophages and dendritic cells. J. Leukoc. Biol. 85, 664 (2009).CrossRefGoogle ScholarPubMed
100.Verreck, F.A.W., de Boer, T., Langenberg, D.M.L., van der Zanden, L., and Ottenhoff, T.H.M.: Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-γ- and CD40L-mediated costimulation. J. Leukoc. Biol. 79, 285 (2006).CrossRefGoogle ScholarPubMed
101.Tanimura, N., Saitoh, S., Matsumoto, F., Akashi-Takamura, S., and Miyake, K.: Roles for LPS-dependent interaction and relocation of TLR4 and TRAM in TRIF-signaling. Biochem. Biophys. Res. Commun. 368, 94 (2008).CrossRefGoogle ScholarPubMed
102.Kawai, T., Takeuchi, O., Fujita, T., Inoue, J.-i., Mühlradt, P.F., Sato, S., Hoshino, K., and Akira, S.: Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J. Immunol. 167, 5887 (2001).CrossRefGoogle ScholarPubMed
103.Häcker, H., Redecke, V., Blagoev, B., Kratchmarova, I., Hsu, L.-C., Wang, G.G., Kamps, M.P., Raz, E., Wagner, H., Häcker, G., Mann, M., and Karin, M.: Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439, 204 (2006).CrossRefGoogle ScholarPubMed
104.Panda, S., Nilsson, J.A., and Gekara, N.O.: Deubiquitinase MYSM1 regulates innate immunity through inactivation of TRAF3 and TRAF6 complexes. Immunity 43, 647 (2015).CrossRefGoogle ScholarPubMed
105.Macedo, L., Pinhal-Enfield, G., Alshits, V., Elson, G., Cronstein, B.N., and Leibovich, S.J.: Wound healing is impaired in MyD88-deficient mice a role for MyD88 in the regulation of wound healing by adenosine a 2A receptors. Am. J. Pathol. 171, 1774 (2007).CrossRefGoogle Scholar
106.Dasu, M.R., Thangappan, R.K., Bourgette, A., DiPietro, L.A., Isseroff, R., and Jialal, I.: TLR2 expression and signaling-dependent inflammation impair wound healing in diabetic mice. Lab. Invest. 90, 1628 (2010).CrossRefGoogle ScholarPubMed
107.Lin, Q., Fang, D., Fang, J., Ren, X., Yang, X., Wen, F., and Su, S.B.: Impaired wound healing with defective expression of chemokines and recruitment of myeloid cells in TLR3-deficient mice. J. Immunol. 186, 3710 (2011).CrossRefGoogle ScholarPubMed
108.Lin, Q., Wang, L., Lin, Y., Liu, X., Ren, X., Wen, S., Du, X., Lu, T., Su, S.Y., Yang, X., Huang, W., Zhou, S., Wen, F., and Su, S.B.: Toll-like receptor 3 ligand polyinosinic: polycytidylic acid promotes wound healing in human and murine skin. J. Invest. Dermatol. 132, 2085 (2012).CrossRefGoogle ScholarPubMed
109.Chen, L., Guo, S., Ranzer, M.J., and Dipietro, L.A.: Toll-like receptor 4 has an essential role in early skin wound healing. J. Invest. Dermatol. 133, 258 (2013).CrossRefGoogle ScholarPubMed
110.Seki, E., De Minicis, S., Österreicher, C.H., Kluwe, J., Osawa, Y., Brenner, D.A., and Schwabe, R.F.: TLR4 enhances TGF-β signaling and hepatic fibrosis. Nat. Med. 13, 1324 (2007).CrossRefGoogle ScholarPubMed
111.Zhang, X. and Mosser, D.: Macrophage activation by endogenous danger signals. J. Pathol. 214, 161 (2008).CrossRefGoogle ScholarPubMed
112.Scaffidi, P., Misteli, T., and Bianchi, M.E.: Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191 (2002).CrossRefGoogle ScholarPubMed
113.Vabulas, R.M.: HSP70 as endogenous stimulus of the toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277, 15107 (2002).CrossRefGoogle ScholarPubMed
114.Taylor, K.R., Trowbridge, J.M., Rudisill, J.A., Termeer, C.C., Simon, J.C., and Gallo, R.L.: Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J. Biol. Chem. 279, 17079 (2004).CrossRefGoogle ScholarPubMed
115.Okamura, Y., Watari, M., Jerud, E.S., Young, D.W., Ishizaka, S.T., Rose, J., Chow, J.C., and Strauss, J.F.: The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276, 10229 (2001).CrossRefGoogle ScholarPubMed
116.Krysko, D.V., Kaczmarek, A., Krysko, O., Heyndrickx, L., Woznicki, J., Bogaert, P., Cauwels, A., Takahashi, N., Magez, S., Bachert, C., and Vandenabeele, P.: TLR-2 and TLR-9 are sensors of apoptosis in a mouse model of doxorubicin-induced acute inflammation. Cell Death Differ. 18, 1316 (2011).CrossRefGoogle Scholar
117.Dumitriu, I.E., Baruah, P., Valentinis, B., Voll, R.E., Herrmann, M., Nawroth, P.P., Arnold, B., Bianchi, M.E., Manfredi, A.A., and Rovere-Querini, P.: Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J. Immunol. 174, 7506 (2005).CrossRefGoogle ScholarPubMed
118.Tattoli, I., Carneiro, L.A., Jéhanno, M., Magalhaes, J.G., Shu, Y., Philpott, D.J., Arnoult, D., and Girardin, S.E.: NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-κB and JNK pathways by inducing reactive oxygen species production. EMBO Rep. 9, 293 (2008).CrossRefGoogle ScholarPubMed
119.Yuita, H., Tsuiji, M., Tajika, Y., Matsumoto, Y., Hirano, K., Suzuki, N., and Irimura, T.: Retardation of removal of radiation-induced apoptotic cells in developing neural tubes in macrophage galactose-type C-type lectin-1-deficient mouse embryos. Glycobiology 15, 1368 (2005).CrossRefGoogle ScholarPubMed
120.Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A., and Bianchi, M.E.: Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551 (2003).CrossRefGoogle ScholarPubMed
121.Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J.M., Ombrellino, M., Che, J., Frazier, A., Yang, H., Ivanova, S., Borovikova, L., Manogue, K.R., Faist, E., Abraham, E., Andersson, J., Andersson, U., Molina, P.E., Abumrad, N.N., Sama, A., and Tracey, K.J.: HMG-1 as a late mediator of endotoxin lethality in mice. Science 285, 248 (1999).CrossRefGoogle ScholarPubMed
122.Hirsiger, S., Simmen, H.P., Werner, C.M.L., Wanner, G.A., and Rittirsch, D.: Danger signals activating the immune response after trauma. Mediators Inflamm. 2012, 1 (2012).CrossRefGoogle ScholarPubMed
123.Land, W.G.: The role of damage-associated molecular patterns (DAMPs) in human diseases: Part II: DAMPs as diagnostics, prognostics and therapeutics in clinical medicine. Sultan Qaboos Univ. Med. J. 15, e157 (2015).Google ScholarPubMed
124.Masouris, I., Klein, M., Dyckhoff, S., Angele, B., Pfister, H.W., and Koedel, U.: Inhibition of DAMP signaling as an effective adjunctive treatment strategy in pneumococcal meningitis. J. Neuroinflammation 14, 214 (2017).CrossRefGoogle ScholarPubMed
125.Lundbäck, P., Klevenvall, L., Ottosson, L., Schierbeck, H., Palmblad, K., Andersson, U., and Harris, H.E.: Anti HMGB1 treatment reduces inflammation in models of experimental autoimmunity. Ann. Rheum. Dis. 71, A79.3 (2012).CrossRefGoogle Scholar
126.Kanellakis, P., Agrotis, A., Kyaw, S., Koulis, C., Ahrens, I., Mori, S., Takahashi, H.K., Liu, K., Peter, K., Nishibori, M., and Bobik, A.: High-mobility group box protein 1 neutralization reduces development of diet-induced atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 31, 313 (2011).CrossRefGoogle ScholarPubMed
127.Piccinini, A.M. and Midwood, K.S.: DAMPening inflammation by modulating TLR signalling. Mediators Inflamm. 2010, 1 (2010).CrossRefGoogle ScholarPubMed
128.Daly, K.A., Liu, S., Agrawal, V., Brown, B.N., Johnson, S.A., Medberry, C.J., and Badylak, S.F.: Damage associated molecular patterns within xenogeneic biologic scaffolds and their effects on host remodeling. Biomaterials 33, 91 (2012).CrossRefGoogle ScholarPubMed
129.Rogers, T.H. and Babensee, J.E.: Altered adherent leukocyte profile on biomaterials in Toll-like receptor 4 deficient mice. Biomaterials 31, 594 (2010).CrossRefGoogle ScholarPubMed
130.Shokouhi, B., Coban, C., Hasirci, V., Aydin, E., Dhanasingh, A., Shi, N., Koyama, S., Akira, S., Zenke, M., and Sechi, A.S.: The role of multiple toll-like receptor signalling cascades on interactions between biomedical polymers and dendritic cells. Biomaterials 31, 5759 (2010).CrossRefGoogle ScholarPubMed
131.Uto, T., Akagi, T., Yoshinaga, K., Toyama, M., Akashi, M., and Baba, M.: The induction of innate and adaptive immunity by biodegradable poly(γ-glutamic acid) nanoparticles via a TLR4 and MyD88 signaling pathway. Biomaterials 32, 5206 (2011).CrossRefGoogle Scholar
132.Babensee, J.E. and Paranjpe, A.: Differential levels of dendritic cell maturation on different biomaterials used in combination products. J. Biomed. Mater. Res. A 74, 503 (2005).CrossRefGoogle ScholarPubMed
133.Vasilijić, S., Savić, D., Vasilev, S., Vucević, D., Gasić, S., Majstorović, I., Janković, S., and Colić, M.: Dendritic cells acquire tolerogenic properties at the site of sterile granulomatous inflammation. Cell. Immunol. 233, 148 (2005).CrossRefGoogle ScholarPubMed
134.Fogg, D.K., Sibon, C., Miled, C., Jung, S., Aucouturier, P., Littman, D.R., Cumano, A., and Geissmann, F.: A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311, 83 (2006).CrossRefGoogle ScholarPubMed
135.Kou, P.M. and Babensee, J.E.: Macrophage and dendritic cell phenotypic diversity in the context of biomaterials. J. Biomed. Mater. Res. A 96, 239 (2010).Google ScholarPubMed
136.Yoshida, M. and Babensee, J.E.: Differential effects of agarose and poly(lactic-co-glycolic acid) on dendritic cell maturation. J. Biomed. Mater. Res. A 79A, 393 (2006).CrossRefGoogle Scholar
137.Yoshida, M., Mata, J., and Babensee, J.E.: Effect of poly(lactic-co-glycolic acid) contact on maturation of murine bone marrow-derived dendritic cells. J. Biomed. Mater. Res. A 80A, 7 (2007).CrossRefGoogle Scholar
138.Teoh, S.: Failure of biomaterials: a review. Int. J. Fatigue 22, 825 (2000).CrossRefGoogle Scholar
139.Wang, Y., Vaddiraju, S., Gu, B., Papadimitrakopoulos, F., and Burgess, D.J.: Foreign body reaction to implantable biosensors: effects of tissue trauma and implant size. J. Diabetes Sci. Technol. 9, 966 (2015).CrossRefGoogle ScholarPubMed
140.Brown, B.N. and Badylak, S.F.: The role of the host immune response in tissue engineering and regenerative medicine. In Principles of Tissue Engineering, edited by Lanza, R., Langer, R., and Vacanti, J. (Academic Press, Cambridge, MA, 2014), p. 497.CrossRefGoogle Scholar
141.Rolfe, B., Mooney, J., Zhang, B., Jahnke, S., Le, S.-J., Chau, Y.-Q., Huang, Q., Wang, H., Campbell, G., and Campbell, J.: The fibrotic response to implanted biomaterials: implications for tissue engineering. In Regenerative Medicine and Tissue Engineering - Cells and Biomaterials, edited by Eberli, D. (Intech Open, London, 2011), p. 551.Google Scholar
142.Sanders, J.E., Cassisi, D.V., Neumann, T., Golledge, S.L., Zachariah, S.G., Ratner, B.D., and Bale, S.D.: Relative influence of polymer fiber diameter and surface charge on fibrous capsule thickness and vessel density for single-fiber implants. J. Biomed. Mater. Res. 65A, 462 (2003).CrossRefGoogle Scholar
143.Percival, V.G., Riddell, J., and Corcoran, T.B.: Single dose dexamethasone for postoperative nausea and vomiting – a matched case-control study of postoperative infection risk. Anaesth. Intensive Care 38, 661 (2010).CrossRefGoogle ScholarPubMed
144.Durmus, M., Karaaslan, E., Ozturk, E., Gulec, M., Iraz, M., Edali, N., and Ersoy, M.O.: The effects of single-dose dexamethasone on wound healing in rats. Anesth. Analg. 97, 1377 (2003).CrossRefGoogle ScholarPubMed
145.Naber, D., Sand, P., and Heigl, B.: Psychopathological and neuropsychological effects of 8-days’ corticosteroid treatment. A prospective study. Psychoneuroendocrinology 21, 25 (1996).CrossRefGoogle ScholarPubMed
146.Patil, S.D., Papadmitrakopoulos, F., and Burgess, D.J.: Concurrent delivery of dexamethasone and VEGF for localized inflammation control and angiogenesis. J. Control. Release 117, 68 (2007).CrossRefGoogle ScholarPubMed
147.Norton, L.W., Koschwanez, H.E., Wisniewski, N.A., Klitzman, B., and Reichert, W.M.: Vascular endothelial growth factor and dexamethasone release from nonfouling sensor coatings affect the foreign body response. J. Biomed. Mater. Res. A 81A, 858 (2007).CrossRefGoogle Scholar
148.Avula, M.N., Rao, A.N., Mcgill, L.D., Grainger, D.W., and Solzbacher, F.: Foreign body response to subcutaneous biomaterial implants in a mast cell-deficient Kit w-Sh murine model. Acta Biomater. 10, 1856 (2014).CrossRefGoogle Scholar
149.Serhan, C.N., Clish, C.B., Brannon, J., Colgan, S.P., Chiang, N., and Gronert, K.: Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J. Exp. Med. 192, 1197 (2000).CrossRefGoogle ScholarPubMed
150.MarketsAndMarkets.com: Biomaterials Market by Application and Geography - Global Forecast 2021 (Northbrook, IL, 2016).Google Scholar
151.Jiang, G. and Zhou, D.D.: Technology advances and challenges in hermetic packaging for implantable medical devices. In Implantable Neural Protheses 2, edited by Zhou, D.D. and Greenbaum, E. (Springer Science + Business Media, New York City, NY, 2010), p. 27.Google Scholar
152.Thwaites, T.: Total recall for medical implants. New Sci. 145, 12 (1995).Google Scholar