Abstract
Biomaterials are used in several clinical applications. Yet they often induce a strong immune response that can lead to implant malfunction and replacement. Thus, it is of crucial importance to deeply understand the biological response to biomaterials. Here, we focus on the molecular mechanisms underlying biomaterial–dendritic cell (DC) interactions. Biomaterials regulate DC adhesion via podosomes in a β2 integrin-dependent manner. Moreover, they primarily affect DC phenotype and function by impinging on multiple Toll-like receptor signaling pathways. By putting biomaterial–DC interactions (and their consequences) in the context of the foreign body response (FBR), we propose that DCs, whose function has been altered by biomaterials, could be engaged in multiple juxtacrine and paracrine interactions with other immune cells including macrophages and neutrophils. Through this complex intercellular network, DCs could affect the immune response at the implantation site initiating (or sustaining) the series of events leading to the FBR. The detailed knowledge of biomaterial–DC interactions could be exploited to design more inert biopolymers, thus minimizing the FBR or biomaterials that elicit controlled and specific immune reactions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20(2):86–100.
Kenneth WW. A review of the foreign-body response to subcutaneously-implanted devices: the role of macrophages and cytokines in biofouling and fibrosis. J Diabetes Sci Technol. 2008; 2(5):768–77.
Bonfield TL, Colton E, Marchant RE, Anderson JM. Cytokine and growth factor production by monocytes/macrophages on protein preadsorbed polymers. J Biomed Mater Res. 1992;26(7): 837–50.
Anderson JM, Ziats NP, Azeez A, Brunstedt MR, Stack S, Bonfield TL. Protein adsorption and macrophage activation on polydimethylsiloxane and silicone rubber. J Biomater Sci Polym Ed. 1995;7(2):159–69.
Jones JA, Dadsetan M, Collier TO, Ebert M, Stokes KS, Ward RS, et al. Macrophage behavior on surface-modified polyurethanes. J Biomater Sci Polym Ed. 2004;15(5):567–84.
Yang D, Jones KS. Effect of alginate on innate immune activation of macrophages. J Biomed Mater Res A. 2009;90(2):411–8.
Sethi RK, Neavyn MJ, Rubash HE, Shanbhag AS. Macrophage response to cross-linked and conventional UHMWPE. Biomaterials. 2003;24(15):2561–73.
Refai AK, Textor M, Brunette DM, Waterfield JD. Effect of titanium surface topography on macrophage activation and secretion of proinflammatory cytokines and chemokines. J Biomed Mater Res A. 2004;70(2):194–205.
Li Y, Schutte RJ, Abu-Shakra A, Reichert WM. Protein array method for assessing in vitro biomaterial-induced cytokine expression. Biomaterials. 2005;26(10):1081–5.
Brodbeck WG, Nakayama Y, Matsuda T, Colton E, Ziats NP, Anderson JM. Biomaterial surface chemistry dictates adherent monocyte/macrophage cytokine expression in vitro. Cytokine. 2002;18(6):311–9.
Brodbeck WG, Patel J, Voskerician G, Christenson E, Shive MS, Nakayama Y, et al. Biomaterial adherent macrophage apoptosis is increased by hydrophilic and anionic substrates in vivo. Proc Natl Acad Sci U S A. 2002;99(16):10287–92.
Kaplan SS, Basford RE, Jeong MH, Simmons RL. Mechanisms of biomaterial-induced superoxide release by neutrophils. J Biomed Mater Res. 1994;28(3):377–86.
Kaplan SS, Basford RE, Jeong MH, Simmons RL. Biomaterial-neutrophil interactions: dysregulation of oxidative functions of fresh neutrophils induced by prior neutrophil-biomaterial interaction. J Biomed Mater Res. 1996;30(1):67–75.
Moore MA, Kaplan DS, Picciolo GL, Wallis RR, Kowolik MJ. Effect of cellulose acetate materials on the oxidative burst of human neutrophils. J Biomed Mater Res. 2001;55(3):257–65.
Patel JD, Krupka T, Anderson JM. iNOS-mediated generation of reactive oxygen and nitrogen species by biomaterial-adherent neutrophils. J Biomed Mater Res A. 2007;80(2):381–90.
Santos TC, Marques AP, Silva SS, Oliveira JM, Mano JF, Castro AG, et al. In vitro evaluation of the behaviour of human polymorphonuclear neutrophils in direct contact with chitosan-based membranes. J Biotechnol. 2007;132(2):218–26.
Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med. 1973;137(5):1142–62.
Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245–52.
Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell. 2001;106(3):255–8.
Auffray C, Sieweke MH, Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol. 2009;27:669–92.
Naik SH, Sathe P, Park HY, Metcalf D, Proietto AI, Dakic A, et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol. 2007;8(11):1217–26.
Chorro L, Sarde A, Li M, Woollard KJ, Chambon P, Malissen B, et al. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J Exp Med. 2009;206(13):3089–100.
Merad M, Ginhoux F, Collin M. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol. 2008;8(12):935–47.
Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, et al. Origin of the lamina propria dendritic cell network. Immunity. 2009;31(3):513–25.
Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity. 2003; 19(1):59–70.
Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol. 2000;18:767–811.
Takeuchi O, Akira S. Signaling pathways activated by microorganisms. Curr Opin Cell Biol. 2007;19(2):185–91.
Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol. 2009;21(4):317–37.
Huppa JB, Davis MM. T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol. 2003;3(12):973–83.
Dustin ML. Insights into function of the immunological synapse from studies with supported planar bilayers. Curr Top Microbiol Immunol. 2010;340:1–24.
Sechi AS, Buer J, Wehland J, Probst-Kepper M. Changes in actin dynamics at the T-cell/APC interface: implications for T-cell anergy? Immunol Rev. 2002;189:98–110.
Sechi AS, Wehland J. Interplay between TCR signalling and actin cytoskeleton dynamics. Trends Immunol. 2004;25(5):257–65.
Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3(12):984–93.
de Jong EC, Smits HH, Kapsenberg ML. Dendritic cell-mediated T cell polarization. Springer Semin Immunopathol. 2005;26(3):289–307.
Ghilardi N, Ouyang W. Targeting the development and effector functions of TH17 cells. Semin Immunol. 2007;19(6):383–93.
Stockinger B, Veldhoen M, Martin B. Th17 T cells: linking innate and adaptive immunity. Semin Immunol. 2007;19(6):353–61.
Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol. 2003;21:685–711.
Morelli AE, Thomson AW. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol. 2007;7(8):610–21.
Andrews DM, Andoniou CE, Scalzo AA, van Dommelen SL, Wallace ME, Smyth MJ, et al. Cross-talk between dendritic cells and natural killer cells in viral infection. Mol Immunol. 2005;42(4):547–55.
Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Munz C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med. 2002;195(3):343–51.
Dubois B, Bridon JM, Fayette J, Barthelemy C, Banchereau J, Caux C, et al. Dendritic cells directly modulate B cell growth and differentiation. J Leukoc Biol. 1999;66(2):224–30.
Fayette J, Dubois B, Vandenabeele S, Bridon JM, Vanbervliet B, Durand I, et al. Human dendritic cells skew isotype switching of CD40-activated naive B cells towards IgA1 and IgA2. J Exp Med. 1997;185(11):1909–18.
Elamanchili P, Diwan M, Cao M, Samuel J. Characterization of poly(D, L-lactic-co-glycolic acid) based nanoparticulate system for enhanced delivery of antigens to dendritic cells. Vaccine. 2004;22(19):2406–12.
Elamanchili P, Lutsiak CM, Hamdy S, Diwan M, Samuel J. “Pathogen-mimicking” nanoparticles for vaccine delivery to dendritic cells. J Immunother. 2007;30(4):378–95.
Yoshida M, Babensee JE. Poly(lactic-co-glycolic acid) enhances maturation of human monocyte-derived dendritic cells. J Biomed Mater Res A. 2004;71(1):45–54.
Babensee JE, Paranjpe A. Differential levels of dendritic cell maturation on different biomaterials used in combination products. J Biomed Mater Res A. 2005;74(4):503–10.
Yoshida M, Babensee JE. Differential effects of agarose and poly(lactic-co-glycolic acid) on dendritic cell maturation. J Biomed Mater Res A. 2006;79(2):393–408.
Yoshida M, Mata J, Babensee JE. Effect of poly(lactic-co-glycolic acid) contact on maturation of murine bone marrow-derived dendritic cells. J Biomed Mater Res A. 2007;80(1):7–12.
Lutsiak ME, Robinson DR, Coester C, Kwon GS, Samuel J. Analysis of poly(D, L-lactic-co-glycolic acid) nanosphere uptake by human dendritic cells and macrophages in vitro. Pharm Res. 2002;19(10):1480–7.
Waeckerle-Men Y, Scandella E, Uetz-Von Allmen E, Ludewig B, Gillessen S, Merkle HP, et al. Phenotype and functional analysis of human monocyte-derived dendritic cells loaded with biodegradable poly(lactide-co-glycolide) microspheres for immunotherapy. J Immunol Methods. 2004;287(1–2):109–24.
Newman KD, Elamanchili P, Kwon GS, Samuel J. Uptake of poly(D, L-lactic-co-glycolic acid) microspheres by antigen-presenting cells in vivo. J Biomed Mater Res. 2002;60(3):480–6.
Schanen BC, Karakoti AS, Seal S, Drake 3rd DR, Warren WL, Self WT. Exposure to titanium dioxide nanomaterials provokes inflammation of an in vitro human immune construct. ACS Nano. 2009;3(9):2523–32.
Arcos D, Vallet-Regi M. Sol–gel silica-based biomaterials and bone tissue regeneration. Acta Biomater. 2010;6(8):2874–88.
Beamer CA, Holian A. Silica suppresses Toll-like receptor ligand-induced dendritic cell activation. FASEB J. 2008;22(6):2053–63.
Shokouhi B, Coban C, Hasirci V, Aydin E, Dhanasingh A, Shi N, et al. The role of multiple toll-like receptor signalling cascades on interactions between biomedical polymers and dendritic cells. Biomaterials. 2010;31(22):5759–71.
Shankar SP, Petrie TA, Garcia AJ, Babensee JE. Dendritic cell responses to self-assembled monolayers of defined chemistries. J Biomed Mater Res A. 2010;92(4):1487–99.
Barbosa JN, Madureira P, Barbosa MA, Aguas AP. The influence of functional groups of self-assembled monolayers on fibrous capsule formation and cell recruitment. J Biomed Mater Res A. 2006;76(4):737–43.
Kamath S, Bhattacharyya D, Padukudru C, Timmons RB, Tang L. Surface chemistry influences implant-mediated host tissue responses. J Biomed Mater Res A. 2008;86(3):617–26.
Krause M, Sechi AS, Konradt M, Monner D, Gertler FB, Wehland J. Fyn-binding protein (Fyb)/SLP-76-associated protein (SLAP), Ena/vasodilator-stimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. J Cell Biol. 2000;149(1):181–94.
Coppolino MG, Krause M, Hagendorff P, Monner DA, Trimble W, Grinstein S, et al. Evidence for a molecular complex consisting of Fyb/SLAP, SLP-76, Nck, VASP and WASP that links the actin cytoskeleton to Fcgamma receptor signalling during phagocytosis. J Cell Sci. 2001;114(Pt 23):4307–18.
Ross R, Jonuleit H, Bros M, Ross XL, Yamashiro S, Matsumura F, et al. Expression of the actin-bundling protein fascin in cultured human dendritic cells correlates with dendritic morphology and cell differentiation. J Invest Dermatol. 2000;115(4):658–63.
Shutt DC, Daniels KJ, Carolan EJ, Hill AC, Soll DR. Changes in the motility, morphology, and F-actin architecture of human dendritic cells in an in vitro model of dendritic cell development. Cell Motil Cytoskeleton. 2000;46(3):200–21.
West MA, Wallin RP, Matthews SP, Svensson HG, Zaru R, Ljunggren HG, et al. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science. 2004;305(5687):1153–7.
van Helden SF, Krooshoop DJ, Broers KC, Raymakers RA, Figdor CG, van Leeuwen FN. A critical role for prostaglandin E2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. J Immunol. 2006;177(3):1567–74.
Rogers TH, Babensee JE. The role of integrins in the recognition and response of dendritic cells to biomaterials. Biomaterials. 2011;32(5):1270–9.
Maitra R, Clement CC, Crisi GM, Cobelli N, Santambrogio L. Immunogenecity of modified alkane polymers is mediated through TLR1/2 activation. PLoS One. 2008;3(6):e2438.
Flo TH, Ryan L, Latz E, Takeuchi O, Monks BG, Lien E, et al. Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J Biol Chem. 2002;277(38):35489–95.
Grandjean-Laquerriere A, Tabary O, Jacquot J, Richard D, Frayssinet P, Guenounou M, et al. Involvement of toll-like receptor 4 in the inflammatory reaction induced by hydroxyapatite particles. Biomaterials. 2007;28(3):400–4.
Seong SY, Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol. 2004;4(6):469–78.
Pastor JC, Puente B, Telleria J, Carrasco B, Sanchez H, Nocito M. Antisilicone antibodies in patients with silicone implants for retinal detachment surgery. Ophthalmic Res. 2001;33(2):87–90.
Zippel R, Wilhelm L, Marusch F, Koch A, Urban G, Schlosser M. Antigenicity of polyester (Dacron) vascular prostheses in an animal model. Eur J Vasc Endovasc Surg. 2001;21(3):202–7.
Schlosser M, Wilhelm L, Urban G, Ziegler B, Ziegler M, Zippel R. Immunogenicity of polymeric implants: long-term antibody response against polyester (Dacron) following the implantation of vascular prostheses into LEW.1A rats. J Biomed Mater Res. 2002;61(3):450–7.
Wilhelm L, Zippel R, von Woedtke T, Kenk H, Hoene A, Patrzyk M, et al. Immune response against polyester implants is influenced by the coating substances. J Biomed Mater Res A. 2007;83(1):104–13.
Zhao Q, Topham N, Anderson JM, Hiltner A, Lodoen G, Payet CR. Foreign-body giant cells and polyurethane biostability: in vivo correlation of cell adhesion and surface cracking. J Biomed Mater Res. 1991;25(2):177–83.
McNally AK, Anderson JM. Interleukin-4 induces foreign body giant cells from human monocytes/macrophages. Differential lymphokine regulation of macrophage fusion leads to morphological variants of multinucleated giant cells. Am J Pathol. 1995;147(5):1487–99.
Kao WJ, McNally AK, Hiltner A, Anderson JM. Role for interleukin-4 in foreign-body giant cell formation on a poly(etherurethane urea) in vivo. J Biomed Mater Res. 1995;29(10):1267–75.
DeFife KM, Jenney CR, McNally AK, Colton E, Anderson JM. Interleukin-13 induces human monocyte/macrophage fusion and macrophage mannose receptor expression. J Immunol. 1997;158(7):3385–90.
McNally AK, DeFife KM, Anderson JM. Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am J Pathol. 1996;149(3):975–85.
Cui W, Ke JZ, Zhang Q, Ke HZ, Chalouni C, Vignery A. The intracellular domain of CD44 promotes the fusion of macrophages. Blood. 2006;107(2):796–805.
Han X, Sterling H, Chen Y, Saginario C, Brown EJ, Frazier WA, et al. CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J Biol Chem. 2000;275(48):37984–92.
Yagi M, Miyamoto T, Sawatani Y, Iwamoto K, Hosogane N, Fujita N, et al. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J Exp Med. 2005;202(3) :345–51.
Bobryshev YV, Inder SJ, Cherian SM, Lord RS, Ao PY, Hawthorne WJ, et al. Colonisation of prosthetic grafts by immunocompetent cells in a sheep model. Cardiovasc Surg. 2001;9(2): 166–76.
Wolfram D, Rainer C, Niederegger H, Piza H, Wick G. Cellular and molecular composition of fibrous capsules formed around silicone breast implants with special focus on local immune reactions. J Autoimmun. 2004;23(1):81–91.
Vasilijic S, Savic D, Vasilev S, Vucevic D, Gasic S, Majstorovic I, et al. Dendritic cells acquire tolerogenic properties at the site of sterile granulomatous inflammation. Cell Immunol. 2005;233(2):148–57.
Megiovanni AM, Sanchez F, Robledo-Sarmiento M, Morel C, Gluckman JC, Boudaly S. Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J Leukoc Biol. 2006;79(5): 977–88.
van Gisbergen KP, Sanchez-Hernandez M, Geijtenbeek TB, van Kooyk Y. Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med. 2005;201(8):1281–92.
Myers CL, Wertheimer SJ, Schembri-King J, Parks T, Wallace RW. Induction of ICAM-1 by TNF-alpha, IL-1 beta, and LPS in human endothelial cells after downregulation of PKC. Am J Physiol. 1992;263(4 Pt 1):C767–72.
Iwasawa K, Kameyama T, Ishikawa H, Sawa Y. Induction of ICAM-1 and VCAM-1 on the mouse lingual lymphatic endothelium with TNF-alpha. Acta Histochem Cytochem. 2008;41(5):115–20.
Dinarello CA. IL-1: discoveries, controversies and future directions. Eur J Immunol. 2010; 40(3):599–606.
Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol. 2007;8(10):1086–94.
Petersen LK, Xue L, Wannemuehler MJ, Rajan K, Narasimhan B. The simultaneous effect of polymer chemistry and device geometry on the in vitro activation of murine dendritic cells. Biomaterials. 2009;30(28):5131–42.
Chen H, Li P, Yin Y, Cai X, Huang Z, Chen J, et al. The promotion of type 1 T helper cell responses to cationic polymers in vivo via toll-like receptor-4 mediated IL-12 secretion. Biomaterials. 2010;31(32):8172–80.
Acknowledgments
This work was supported by the Interdisciplinary Center for Clinical Research (IZKF) of the Medical Faculty of RWTH Aachen University.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Appendix
Appendix
See Table 7.1.
Glossary
- Adaptive (or acquired) immune response
-
The process by which the immune system responds to an infection or vaccination by producing specific antibodies towards foreign antigens.
- Antigen presentation
-
The process by which dendritic cells (and, to a minor extent, macrophages and B cells) capture antigens and display them on their surface, thus enabling recognition by T cells.
- Apoptosis
-
A type of specialized cell death by which cells kill themselves. It plays an essential role in many processes such as tissue remodeling during embryonic development.
- Biocompatibility
-
The property of a liquid or a solid substance of being nontoxic and non-dangerous to a living cell or a tissue.
- Chemokines
-
Proteins that activate and stimulate the directional migration of immune cells.
- Cytokines
-
Soluble proteins that are secreted by immune cells and that serve to regulate the immune response.
- Cytotoxicity
-
The attribute of a substance of being toxic to living cells.
- Foreign body giant cell
-
A multinucleated cell that is generated by fusion of macrophages in response to the presence of a large foreign body.
- Immunological memory
-
The ability of the immune system to remember a specific antigen and respond rapidly and vigorously to subsequent encounters with the same antigen.
- Immunological tolerance
-
The non-reactivity of the immune system to specific antigens, primarily self-antigens.
- Inflammatory response
-
One of the earliest reactions of the immune system against tissue damage caused by pathogens, trauma, or toxins. It is characterized by pain, localized heat, skin redness, and swelling.
- Interleukins
-
A class of proteins that act to stimulate and regulate the function of several immune cell types.
- Major histocompatibility complex
-
Cell membrane antigens that are the key determinant of tissue type and transplant compatibility.
- Naïve T cells
-
A T cell that has not yet encountered its cognate antigen.
- Pathogen-associated molecular patterns
-
Molecules associated with pathogens that are recognized by TLRs or other pattern recognition receptors.
- Phenotype
-
In a cell, it represents the morphological and biochemical features as determined by its gene expression profile and interactions with the environment.
- Podosome
-
A highly dynamic, actin-rich, ringlike cellular structure frequently formed by dendritic cells and macrophages that is essential for the adhesion and motility of these cells.
- Toll-like receptors
-
A class of surface or endosomal proteins expressed by immune cells that recognize pathogen-associated molecules.
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Sechi, A.S., Shokouhi, B. (2013). Dendritic Cell–Biomaterial Interactions: Implications for the Onset and Development of the Foreign Body Response. In: Moriarty, T., Zaat, S., Busscher, H. (eds) Biomaterials Associated Infection. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-1031-7_7
Download citation
DOI: https://doi.org/10.1007/978-1-4614-1031-7_7
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-1030-0
Online ISBN: 978-1-4614-1031-7
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)