Abstract
Macrophages are the initial biologic responders to biomaterials. These highly plastic immune sentinels control and modulate responses to materials, foreign or natural. The responses may vary from immune stimulatory to immune suppressive. Several parameters have been identified that influence macrophage response to biomaterials, specifically size, geometry, surface topography, hydrophobicity, surface chemistry, material mechanics, and protein adsorption. In this review, the influence of these parameters is supported with examples of both synthetic and naturally derived materials and illustrates that a combination of these parameters ultimately influences macrophage responses to the biomaterial. Having an understanding of these properties may lead to highly efficient design of biomaterials with desirable biologic response properties.
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References
Ademovic Z, Holst B, Kahn RA, Jorring I, Brevig T, Wei J, Hou X, Winter-Jensen B, Kingshott P (2006) The method of surface PEGylation influences leukocyte adhesion and activation. J Mater Sci Mater Med 17(3):203–211. doi:10.1007/s10856-006-7306-2
Akilbekova D, Philiph R, Graham A, Bratlie KM (2015) Macrophage reprogramming: influence of latex beads with various functional groups on macrophage phenotype and phagocytic uptake in vitro. J Biomed Mater Res A 103(1):262–268. doi:10.1002/jbm.a.35169
Anand G, Sharma S, Dutta AK, Kumar SK, Belfort G (2010) Conformational transitions of adsorbed proteins on surfaces of varying polarity. Langmuir 26(13):10803–10811. doi:10.1021/la1006132
Anderson JM, Miller KM (1984) Biomaterial biocompatibility and the macrophage. Biomaterials 5(1):5–10
Anderson JM, Rodriguez A, Chang DT (2008) Foreign body reaction to biomaterials. Semin Immunol 20(2):86–100. doi:10.1016/j.smim.2007.11.004
Anselmo AC, Zhang M, Kumar S, Vogus DR, Menegatti S, Helgeson ME, Mitragotri S (2015) Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. ACS Nano 9(3):3169–3177. doi:10.1021/acsnano.5b00147
Ballotta V, Driessen-Mol A, Bouten CV, Baaijens FP (2014) Strain-dependent modulation of macrophage polarization within scaffolds. Biomaterials 35(18):4919–4928. doi:10.1016/j.biomaterials.2014.03.002
Barbosa JN, Madureira P, Barbosa MA, Aguas AP (2006) The influence of functional groups of self-assembled monolayers on fibrous capsule formation and cell recruitment. J Biomed Mater Res A 76(4):737–743. doi:10.1002/jbm.a.30602
Barker DE, Retsky MI, Schultz S (1978) “Bleeding” of silicone from bag-gel breast implants, and its clinical relation to fibrous capsule reaction. Plast Reconstr Surg 61(6):836–841
Beacham DA, Wise RJ, Turci SM, Handin RI (1992) Selective inactivation of the Arg-Gly-Asp-Ser (RGDS) binding site in von Willebrand factor by site-directed mutagenesis. J Biol Chem 267(5):3409–3415
Bidan CM, Veldsink AC, Meurs H, Gosens R (2015) Airway and extracellular matrix mechanics in COPD. Front Physiol 6:346. doi:10.3389/fphys.2015.00346
Biswas SK, Mantovani A (2010) Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 11(10):889–896. doi:10.1038/ni.1937
Blakney AK, Swartzlander MD, Bryant SJ (2012) 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(6):1375–1386. doi:10.1002/jbm.a.34104
Blanckmeister CA, Sussdorf DH (1985) Macrophage activation by cross-linked dextran. J Leukoc Biol 37(2):209–219
Boyle JJ, Christou I, Iqbal MB, Nguyen AT, Leung VW, Evans PC, Liu Y, Johns M, Kirkham P, Haskard DO (2012) Solid-phase immunoglobulins IgG and IgM activate macrophages with solid-phase IgM acting via a novel scavenger receptor a pathway. Am J Pathol 181(1):347–361. doi:10.1016/j.ajpath.2012.03.040
Brancato SK, Albina JE (2011) Wound macrophages as key regulators of repair: origin, phenotype, and function. Am J Pathol 178(1):19–25. doi:10.1016/j.ajpath.2010.08.003
Brevig T, Holst B, Ademovic Z, Rozlosnik N, Rohrmann JH, Larsen NB, Hansen OC, Kingshott P (2005) The recognition of adsorbed and denatured proteins of different topographies by beta2 integrins and effects on leukocyte adhesion and activation. Biomaterials 26(16):3039–3053. doi:10.1016/j.biomaterials.2004.09.006
Brodbeck WG, Shive MS, Colton E, Nakayama Y, Matsuda T, Anderson JM (2001) Influence of biomaterial surface chemistry on the apoptosis of adherent cells. J Biomed Mater Res 55(4):661–668
Brodbeck WG, Nakayama Y, Matsuda T, Colton E, Ziats NP, Anderson JM (2002) Biomaterial surface chemistry dictates adherent monocyte/macrophage cytokine expression in vitro. Cytokine 18(6):311–319
Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF (2009) Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30(8):1482–1491. doi:10.1016/j.biomaterials.2008.11.040
Bryers JD, Giachelli CM, Ratner BD (2012) Engineering biomaterials to integrate and heal: the biocompatibility paradigm shifts. Biotechnol Bioeng 109(8):1898–1911. doi:10.1002/bit.24559
Bygd HC, Forsmark KD, Bratlie KM (2015) Altering in vivo macrophage responses with modified polymer properties. Biomaterials 56:187–197. doi:10.1016/j.biomaterials.2015.03.042
Carreno MP, Gresham HD, Brown EJ (1993) Isolation of leukocyte response integrin: a novel RGD-binding protein involved in regulation of phagocytic function. Clin Immunol Immunopathol 69(1):43–51
Champion JA, Mitragotri S (2006) Role of target geometry in phagocytosis. Proc Natl Acad Sci U S A 103(13):4930–4934. doi:10.1073/pnas.0600997103
Champion JA, Katare YK, Mitragotri S (2007) Particle shape: a new design parameter for micro- and nanoscale drug delivery carriers. J Control Release 121(1–2):3–9. doi:10.1016/j.jconrel.2007.03.022
Chang DT, Jones JA, Meyerson H, Colton E, Kwon IK, Matsuda T, Anderson JM (2008) Lymphocyte/macrophage interactions: biomaterial surface-dependent cytokine, chemokine, and matrix protein production. J Biomed Mater Res A 87(3):676–687. doi:10.1002/jbm.a.31630
Chen S, Jones JA, Xu Y, Low HY, Anderson JM, Leong KW (2010) Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31(13):3479–3491. doi:10.1016/j.biomaterials.2010.01.074
Classen A, Lloberas J, Celada A (2009) Macrophage activation: classical versus alternative. Methods Mol Biol 531:29–43. doi:10.1007/978-1-59745-396-7_3
Cox TR, Erler JT (2011) Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 4(2):165–178. doi:10.1242/dmm.004077
Cross MC, Toomey RG, Gallant ND (2016) Protein-surface interactions on stimuli-responsive polymeric biomaterials. Biomed Mater 11(2):022002. doi:10.1088/1748-6041/11/2/022002
Dale DC, Boxer L, Liles WC (2008) The phagocytes: neutrophils and monocytes. Blood 112(4):935–945. doi:10.1182/blood-2007-12-077917
Denis C, Williams JA, Lu X, Meyer D, Baruch D (1993) Solid-phase von Willebrand factor contains a conformationally active RGD motif that mediates endothelial cell adhesion through the alpha v beta 3 receptor. Blood 82(12):3622–3630
Derlindati E, Dei Cas A, Montanini B, Spigoni V, Curella V, Aldigeri R, Ardigo D, Zavaroni I, Bonadonna RC (2015) Transcriptomic analysis of human polarized macrophages: more than one role of alternative activation? PLoS One 10(3):e0119751. doi:10.1371/journal.pone.0119751
Diekjiirgen D, Astashkina A, Grainger DW, Holt D, Brooks AE (2012) Cultured primary macrophage activation by lipopolysaccharide depends on adsorbed protein composition and substrate surface chemistry. J Biomater Sci Polym Ed 23(9):1231–1254. doi:10.1163/092050611X580382
DiPietro LA (1995) Wound healing: the role of the macrophage and other immune cells. Shock 4(4):233–240
Dutta D, Sundaram SK, Teeguarden JG, Riley BJ, Fifield LS, Jacobs JM, Addleman SR, Kaysen GA, Moudgil BM, Weber TJ (2007) Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol Sci 100(1):303–315. doi:10.1093/toxsci/kfm217
Dvir T, Timko BP, Kohane DS, Langer R (2011) Nanotechnological strategies for engineering complex tissues. Nat Nanotechnol 6(1):13–22. doi:10.1038/nnano.2010.246
Edwards PC, Fantasia JE (2007) Review of long-term adverse effects associated with the use of chemically-modified animal and nonanimal source hyaluronic acid dermal fillers. Clin Interv Aging 2(4):509–519
Edwards JP, Zhang X, Frauwirth KA, Mosser DM (2006) Biochemical and functional characterization of three activated macrophage populations. J Leukoc Biol 80(6):1298–1307. doi:10.1189/jlb.0406249
Elsabahy M, Wooley KL (2012) Design of polymeric nanoparticles for biomedical delivery applications. Chem Soc Rev 41(7):2545–2561. doi:10.1039/c2cs15327k
Elzoghby AO, Samy WM, Elgindy NA (2012) Albumin-based nanoparticles as potential controlled release drug delivery systems. J Control Release 157(2):168–182. doi:10.1016/j.jconrel.2011.07.031
Fernandez-Acenero MJ, Zamora E, Borbujo J (2003) Granulomatous foreign body reaction against hyaluronic acid: report of a case after lip augmentation. Dermatol Surg 29(12):1225–1226
Ferrante CJ, Leibovich SJ (2012) Regulation of macrophage polarization and wound healing. Adv Wound Care (New Rochelle) 1(1):10–16. doi:10.1089/wound.2011.0307
Franz S, Allenstein F, Kajahn J, Forstreuter I, Hintze V, Moller S, Simon JC (2013) Artificial extracellular matrices composed of collagen I and high-sulfated hyaluronan promote phenotypic and functional modulation of human pro-inflammatory M1 macrophages. Acta Biomater 9(3):5621–5629. doi:10.1016/j.actbio.2012.11.016
Fukano Y, Knowles NG, Usui ML, Underwood RA, Hauch KD, Marshall AJ, Ratner BD, Giachelli C, Carter WG, Fleckman P, Olerud JE (2006) Characterization of an in vitro model for evaluating the interface between skin and percutaneous biomaterials. Wound Repair Regen 14(4):484–491. doi:10.1111/j.1743-6109.2006.00138.x
Garash R, Bajpai A, Marcinkiewicz BM, Spiller KL (2016) Drug delivery strategies to control macrophages for tissue repair and regeneration. Exp Biol Med (Maywood) 241(10):1054–1063. doi:10.1177/1535370216649444
Garg K, Sell SA, Madurantakam P, Bowlin GL (2009) Angiogenic potential of human macrophages on electrospun bioresorbable vascular grafts. Biomed Mater 4(3):031001. doi:10.1088/1748-6041/4/3/031001
Garg K, Pullen NA, Oskeritzian CA, Ryan JJ, Bowlin GL (2013) Macrophage functional polarization (M1/M2) in response to varying fiber and pore dimensions of electrospun scaffolds. Biomaterials 34(18):4439–4451. doi:10.1016/j.biomaterials.2013.02.065
Getts DR, Martin AJ, McCarthy DP, Terry RL, Hunter ZN, Yap WT, Getts MT, Pleiss M, Luo X, King NJ, Shea LD, Miller SD (2012) Microparticles bearing encephalitogenic peptides induce T-cell tolerance and ameliorate experimental autoimmune encephalomyelitis. Nat Biotechnol 30(12):1217–1224. doi:10.1038/nbt.2434
Gordon S (1986) Macrophage activation and differentiation. Ann Inst Pasteur Immunol 137C(2):197–200
Gordon S (2007) The macrophage: past, present and future. Eur J Immunol 37(Suppl 1):S9–17. doi:10.1002/eji.200737638
Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32(5):593–604. doi:10.1016/j.immuni.2010.05.007
Gordon S, Taylor PR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5(12):953–964. doi:10.1038/nri1733
Gratton SE, Ropp PA, Pohlhaus PD, Luft JC, Madden VJ, Napier ME, DeSimone JM (2008) The effect of particle design on cellular internalization pathways. Proc Natl Acad Sci U S A 105(33):11613–11618. doi:10.1073/pnas.0801763105
Gray JJ (2004) The interaction of proteins with solid surfaces. Curr Opin Struct Biol 14(1):110–115. doi:10.1016/j.sbi.2003.12.001
Greisler H (1988) Macrophage-biomaterial interactions with bioresorbable vascular prostheses. ASAIO Trans 34(4):1051–1059
Greisler HP, Dennis JW, Endean ED, Ellinger J, Friesel R, Burgess W (1989) Macrophage/biomaterial interactions: the stimulation of endothelialization. J Vasc Surg 9(4):588–593
Hanson SE, King SN, Kim J, Chen X, Thibeault SL, Hematti P (2011) The effect of mesenchymal stromal cell-hyaluronic acid hydrogel constructs on immunophenotype of macrophages. Tissue Eng Part A 17(19–20):2463–2471. doi:10.1089/ten.TEA.2010.0716
Helton KL, Ratner BD, Wisniewski NA (2011) Biomechanics of the sensor-tissue interface-effects of motion, pressure, and design on sensor performance and foreign body response-part II: examples and application. J Diabetes Sci Technol 5(3):647–656
Higgins DM, Basaraba RJ, Hohnbaum AC, Lee EJ, Grainger DW, Gonzalez-Juarrero M (2009) Localized immunosuppressive environment in the foreign body response to implanted biomaterials. Am J Pathol 175(1):161–170. doi:10.2353/ajpath.2009.080962
Hu WJ, Eaton JW, Ugarova TP, Tang L (2001) Molecular basis of biomaterial-mediated foreign body reactions. Blood 98(4):1231–1238
Hunt JA, Flanagan BF, McLaughlin PJ, Strickland I, Williams DF (1996) Effect of biomaterial surface charge on the inflammatory response: evaluation of cellular infiltration and TNF alpha production. J Biomed Mater Res 31(1):139–144. doi:10.1002/(SICI)1097-4636(199605)31:1<139::AID-JBM15>3.0.CO;2-I
Ihlenfeld JV, Cooper SL (1979) Transient in vivo protein adsorption onto polymeric biomaterials. J Biomed Mater Res 13(4):577–591. doi:10.1002/jbm.820130405
Iribarren P, Correa SG, Sodero N, Riera CM (2002) Activation of macrophages by silicones: phenotype and production of oxidant metabolites. BMC Immunol 3:6
Irwin EF, Saha K, Rosenbluth M, Gamble LJ, Castner DG, Healy KE (2008) Modulus-dependent macrophage adhesion and behavior. J Biomater Sci Polym Ed 19(10):1363–1382. doi:10.1163/156856208786052407
Isenhath SN, Fukano Y, Usui ML, Underwood RA, Irvin CA, Marshall AJ, Hauch KD, Ratner BD, Fleckman P, Olerud JE (2007) A mouse model to evaluate the interface between skin and a percutaneous device. J Biomed Mater Res A 83(4):915–922. doi:10.1002/jbm.a.31391
Jansch M, Jindal AB, Sharmila BM, Samad A, Devarajan PV, Muller RH (2013) Influence of particle shape on plasma protein adsorption and macrophage uptake. Pharmazie 68(1):27–33
Jenney CR, Anderson JM (2000a) Adsorbed IgG: a potent adhesive substrate for human macrophages. J Biomed Mater Res 50(3):281–290
Jenney CR, Anderson JM (2000b) Adsorbed serum proteins responsible for surface dependent human macrophage behavior. J Biomed Mater Res 49(4):435–447
Kajahn J, Franz S, Rueckert E, Forstreuter I, Hintze V, Moeller S, Simon JC (2012) Artificial extracellular matrices composed of collagen I and high sulfated hyaluronan modulate monocyte to macrophage differentiation under conditions of sterile inflammation. Biomatter 2(4):226--236. doi:10.4161/biom.22855
Kamath S, Bhattacharyya D, Padukudru C, Timmons RB, Tang L (2008) Surface chemistry influences implant-mediated host tissue responses. J Biomed Mater Res A 86(3):617–626. doi:10.1002/jbm.a.31649
Kao WJ, Lee D (2001) In vivo modulation of host response and macrophage behavior by polymer networks grafted with fibronectin-derived biomimetic oligopeptides: the role of RGD and PHSRN domains. Biomaterials 22(21):2901–2909
Kastellorizios M, Tipnis N, Burgess DJ (2015) Foreign body reaction to subcutaneous implants. Adv Exp Med Biol 865:93–108. doi:10.1007/978-3-319-18603-0_6
Kim YK, Que R, Wang SW, Liu WF (2014) Modification of biomaterials with a self-protein inhibits the macrophage response. Adv Healthc Mater 3(7):989–994. doi:10.1002/adhm.201300532
Klein AW (2004) Granulomatous foreign body reaction against hyaluronic acid. Dermatol Surg 30(7):1070. doi:10.1111/j.1524-4725.2004.30320_1.x
Klopfleisch R (2016) Macrophage reaction against biomaterials in the mouse model—Phenotypes, functions and markers. Acta Biomater. doi:10.1016/j.actbio.2016.07.003
Koh TJ, DiPietro LA (2011) Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 13:e23. doi:10.1017/S1462399411001943
Larson TA, Joshi PP, Sokolov K (2012) Preventing protein adsorption and macrophage uptake of gold nanoparticles via a hydrophobic shield. ACS Nano 6(10):9182–9190. doi:10.1021/nn3035155
Liao KL, Bai XF, Friedman A (2013) The role of CD200-CD200R in tumor immune evasion. J Theor Biol 328:65–76. doi:10.1016/j.jtbi.2013.03.017
Loke P, Gallagher I, Nair MG, Zang X, Brombacher F, Mohrs M, Allison JP, Allen JE (2007) Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. J Immunol 179(6):3926–3936
Lynn AD, Bryant SJ (2011) Phenotypic changes in bone marrow-derived murine macrophages cultured on PEG-based hydrogels activated or not by lipopolysaccharide. Acta Biomater 7(1):123–132. doi:10.1016/j.actbio.2010.07.033
Lynn AD, Kyriakides TR, Bryant SJ (2010) Characterization of the in vitro macrophage response and in vivo host response to poly(ethylene glycol)-based hydrogels. J Biomed Mater Res A 93(3):941–953. doi:10.1002/jbm.a.32595
Mackaness GB (1977) Cellular immunity and the parasite. Adv Exp Med Biol 93:65–73
Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677–686. doi:10.1016/j.it.2004.09.015
Martinez FO (2011) Regulators of macrophage activation. Eur J Immunol 41(6):1531–1534. doi:10.1002/eji.201141670
Martinez FO, Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6:13. doi:10.12703/P6-13
Martinez FO, Sica A, Mantovani A, Locati M (2008) Macrophage activation and polarization. Front Biosci 13:453–461
Matlaga BF, Yasenchak LP, Salthouse TN (1976) Tissue response to implanted polymers: the significance of sample shape. J Biomed Mater Res 10(3):391–397. doi:10.1002/jbm.820100308
Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12:991–1045. doi:10.1146/annurev.iy.12.040194.005015
McBane JE, Ebadi D, Sharifpoor S, Labow RS, Santerre JP (2011) Differentiation of monocytes on a degradable, polar, hydrophobic, ionic polyurethane: two-dimensional films vs. three-dimensional scaffolds. Acta Biomater 7(1):115–122. doi:10.1016/j.actbio.2010.08.014
Minardi S, Corradetti B, Taraballi F, Byun JH, Cabrera F, Liu X, Ferrari M, Weiner BK, Tasciotti E (2016) IL-4 release from a biomimetic scaffold for the temporally controlled modulation of macrophage response. Ann Biomed Eng 44(6):2008–2019. doi:10.1007/s10439-016-1580-z
Mitragotri S, Lahann J (2009) Physical approaches to biomaterial design. Nat Mater 8(1):15–23. doi:10.1038/nmat2344
Moon JJ, Huang B, Irvine DJ (2012) Engineering nano- and microparticles to tune immunity. Adv Mater 24(28):3724–3746. doi:10.1002/adma.201200446
Mosser DM (2003) The many faces of macrophage activation. J Leukoc Biol 73(2):209–212
Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8(12):958–969. doi:10.1038/nri2448
Murray PJ, Wynn TA (2011) Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11(11):723–737. doi:10.1038/nri3073
Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, Locati M, Mantovani A, Martinez FO, Mege JL, Mosser DM, Natoli G, Saeij JP, Schultze JL, Shirey KA, Sica A, Suttles J, Udalova I, van Ginderachter JA, Vogel SN, Wynn TA (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41(1):14–20. doi:10.1016/j.immuni.2014.06.008
Nathan C (2008) Metchnikoff’s legacy in 2008. Nat Immunol 9(7):695–698. doi:10.1038/ni0708-695
Nathan C, Muller WA (2001) Putting the brakes on innate immunity: a regulatory role for CD200? Nat Immunol 2(1):17–19. doi:10.1038/83124
Nichols SP, Koh A, Storm WL, Shin JH, Schoenfisch MH (2013) Biocompatible materials for continuous glucose monitoring devices. Chem Rev 113(4):2528–2549. doi:10.1021/cr300387j
Nicolete R, dos Santos DF, Faccioli LH (2011) The uptake of PLGA micro or nanoparticles by macrophages provokes distinct in vitro inflammatory response. Int Immunopharmacol 11(10):1557–1563. doi:10.1016/j.intimp.2011.05.014
O’Shea JJ, Murray PJ (2008) Cytokine signaling modules in inflammatory responses. Immunity 28(4):477–487. doi:10.1016/j.immuni.2008.03.002
Ogawara K, Furumoto K, Nagayama S, Minato K, Higaki K, Kai T, Kimura T (2004) Pre-coating with serum albumin reduces receptor-mediated hepatic disposition of polystyrene nanosphere: implications for rational design of nanoparticles. J Control Release 100(3):451–455. doi:10.1016/j.jconrel.2004.07.028
Ogle ME, Segar CE, Sridhar S, Botchwey EA (2016) Monocytes and macrophages in tissue repair: implications for immunoregenerative biomaterial design. Exp Biol Med (Maywood) 241(10):1084–1097. doi:10.1177/1535370216650293
Orringer DA, Koo YE, Chen T, Kopelman R, Sagher O, Philbert MA (2009) Small solutions for big problems: the application of nanoparticles to brain tumor diagnosis and therapy. Clin Pharmacol Ther 85(5):531–534. doi:10.1038/clpt.2008.296
Palmer JA, Abberton KM, Mitchell GM, Morrison WA (2014) Macrophage phenotype in response to implanted synthetic scaffolds: an immunohistochemical study in the rat. Cells Tissues Organs 199(2–3):169–183. doi:10.1159/000363693
Parodi A, Quattrocchi N, van de Ven AL, Chiappini C, Evangelopoulos M, Martinez JO, Brown BS, Khaled SZ, Yazdi IK, Enzo MV, Isenhart L, Ferrari M, Tasciotti E (2013) Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat Nanotechnol 8(1):61–68. doi:10.1038/nnano.2012.212
Patel NR, Bole M, Chen C, Hardin CC, Kho AT, Mih J, Deng L, Butler J, Tschumperlin D, Fredberg JJ, Krishnan R, Koziel H (2012) Cell elasticity determines macrophage function. PLoS One 7(9):e41024. doi:10.1371/journal.pone.0041024
Phillips JM, Kao WJ (2005) Macrophage adhesion on gelatin-based interpenetrating networks grafted with PEGylated RGD. Tissue Eng 11(5–6):964–973. doi:10.1089/ten.2005.11.964
Pugin J, Dunn I, Jolliet P, Tassaux D, Magnenat JL, Nicod LP, Chevrolet JC (1998) Activation of human macrophages by mechanical ventilation in vitro. Am J Physiol 275(6 Pt 1):L1040–L1050
Qie Y, Yuan H, von Roemeling CA, Chen Y, Liu X, Shih KD, Knight JA, Tun HW, Wharen RE, Jiang W, Kim BY (2016) Surface modification of nanoparticles enables selective evasion of phagocytic clearance by distinct macrophage phenotypes. Sci Rep 6:26269. doi:10.1038/srep26269
Ratner BD, Bryant SJ (2004) Biomaterials: where we have been and where we are going. Annu Rev Biomed Eng 6:41–75. doi:10.1146/annurev.bioeng.6.040803.140027
Refai AK, Textor M, Brunette DM, Waterfield JD (2004) Effect of titanium surface topography on macrophage activation and secretion of proinflammatory cytokines and chemokines. J Biomed Mater Res A 70(2):194–205. doi:10.1002/jbm.a.30075
Resnick N, Gimbrone MA Jr (1995) Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J 9(10):874–882
Rich A, Harris AK (1981) Anomalous preferences of cultured macrophages for hydrophobic and roughened substrata. J Cell Sci 50:1–7
Richards RG, Moriarty TF, Miclau T, McClellan RT, Grainger DW (2012) Advances in biomaterials and surface technologies. J Orthop Trauma 26(12):703–707. doi:10.1097/BOT.0b013e31826e37a2
Roach P, Farrar D, Perry CC (2005) Interpretation of protein adsorption: surface-induced conformational changes. J Am Chem Soc 127(22):8168–8173. doi:10.1021/ja042898o
Rongioletti F, Cattarini G, Sottofattori E, Rebora A (2003) Granulomatous reaction after intradermal injections of hyaluronic acid gel. Arch Dermatol 139(6):815–816. doi:10.1001/archderm.139.6.815
Rostam HM, Singh S, Salazar F, Magennis P, Hook A, Singh T, Vrana NE, Alexander MR, Ghaemmaghami AM (2016) The impact of surface chemistry modification on macrophage polarisation. Immunobiology. doi:10.1016/j.imbio.2016.06.010
Saino E, Focarete ML, Gualandi C, Emanuele E, Cornaglia AI, Imbriani M, Visai L (2011) Effect of electrospun fiber diameter and alignment on macrophage activation and secretion of proinflammatory cytokines and chemokines. Biomacromolecules 12(5):1900–1911. doi:10.1021/bm200248h
Salthouse TN (1984) Some aspects of macrophage behavior at the implant interface. J Biomed Mater Res 18(4):395–401. doi:10.1002/jbm.820180407
Sanchez-Moreno P, Buzon P, Boulaiz H, Peula-Garcia JM, Ortega-Vinuesa JL, Luque I, Salvati A, Marchal JA (2015) Balancing the effect of corona on therapeutic efficacy and macrophage uptake of lipid nanocapsules. Biomaterials 61:266–278. doi:10.1016/j.biomaterials.2015.04.049
Sanders JE, Stiles CE, Hayes CL (2000) Tissue response to single-polymer fibers of varying diameters: evaluation of fibrous encapsulation and macrophage density. J Biomed Mater Res 52(1):231–237
Sanders JE, Bale SD, Neumann T (2002) Tissue response to microfibers of different polymers: polyester, polyethylene, polylactic acid, and polyurethane. J Biomed Mater Res 62(2):222–227. doi:10.1002/jbm.10285
Schutte RJ, Parisi-Amon A, Reichert WM (2009) Cytokine profiling using monocytes/macrophages cultured on common biomaterials with a range of surface chemistries. J Biomed Mater Res A 88(1):128–139. doi:10.1002/jbm.a.31863
Seong SY, Matzinger P (2004) Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 4(6):469–478. doi:10.1038/nri1372
Sharma G, Valenta DT, Altman Y, Harvey S, Xie H, Mitragotri S, Smith JW (2010) Polymer particle shape independently influences binding and internalization by macrophages. J Control Release 147(3):408–412. doi:10.1016/j.jconrel.2010.07.116
Shen M, Garcia I, Maier RV, Horbett TA (2004) Effects of adsorbed proteins and surface chemistry on foreign body giant cell formation, tumor necrosis factor alpha release and procoagulant activity of monocytes. J Biomed Mater Res A 70(4):533–541. doi:10.1002/jbm.a.30069
Shyy JY, Lin MC, Han J, Lu Y, Petrime M, Chien S (1995) The cis-acting phorbol ester “12-O-tetradecanoylphorbol 13-acetate”-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc Natl Acad Sci U S A 92(17):8069–8073
Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176(1):287–292
Sunderkotter C, Steinbrink K, Goebeler M, Bhardwaj R, Sorg C (1994) Macrophages and angiogenesis. J Leukoc Biol 55(3):410–422
Sussman EM, Halpin MC, Muster J, Moon RT, Ratner BD (2014) Porous implants modulate healing and induce shifts in local macrophage polarization in the foreign body reaction. Ann Biomed Eng 42(7):1508–1516. doi:10.1007/s10439-013-0933-0
Valentin JE, Stewart-Akers AM, Gilbert TW, Badylak SF (2009) Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng Part A 15(7):1687–1694. doi:10.1089/ten.tea.2008.0419
Vargas-Machuca I, Gonzalez-Guerra E, Angulo J, del Carmen FM, Martin L, Requena L (2006) Facial granulomas secondary to dermalive microimplants: report of a case with histopathologic differential diagnosis among the granulomas secondary to different injectable permanent filler materials. Am J Dermatopathol 28(2):173–177. doi:10.1097/01.dad.0000181108.46909.8e
Vasconcelos DP, Fonseca AC, Costa M, Amaral IF, Barbosa MA, Aguas AP, Barbosa JN (2013) Macrophage polarization following chitosan implantation. Biomaterials 34(38):9952–9959. doi:10.1016/j.biomaterials.2013.09.012
Veiseh O, Doloff JC, Ma M, Vegas AJ, Tam HH, Bader AR, Li J, Langan E, Wyckoff J, Loo WS, Jhunjhunwala S, Chiu A, Siebert S, Tang K, Hollister-Lock J, Aresta-Dasilva S, Bochenek M, Mendoza-Elias J, Wang Y, Qi M, Lavin DM, Chen M, Dholakia N, Thakrar R, Lacik I, Weir GC, Oberholzer J, Greiner DL, Langer R, Anderson DG (2015) Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates. Nat Mater 14(6):643–651. doi:10.1038/nmat4290
Vijaya Bhaskar TB, Ma N, Lendlein A, Roch T (2015) The interaction of human macrophage subsets with silicone as a biomaterial. Clin Hemorheol Microcirc 61(2):119–133. doi:10.3233/CH-151991
Vogler EA (2012) Protein adsorption in three dimensions. Biomaterials 33(5):1201–1237. doi:10.1016/j.biomaterials.2011.10.059
Vroman L (1962) Effect of absorbed proteins on the wettability of hydrophilic and hydrophobic solids. Nature 196:476–477
Vroman L, Lukosevicius A (1964) Ellipsometer recordings of changes in optical thickness of adsorbed films associated with surface activation of blood clotting. Nature 204:701–703
Walkey CD, Olsen JB, Guo H, Emili A, Chan WC (2012) Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc 134(4):2139–2147. doi:10.1021/ja2084338
Wang X, Ding B, Li B (2013) Biomimetic electrospun nanofibrous structures for tissue engineering. Mater Today (Kidlington) 16(6):229–241. doi:10.1016/j.mattod.2013.06.005
Ward WK, Slobodzian EP, Tiekotter KL, Wood MD (2002) The effect of microgeometry, implant thickness and polyurethane chemistry on the foreign body response to subcutaneous implants. Biomaterials 23(21):4185–4192
Wehner S, Buchholz BM, Schuchtrup S, Rocke A, Schaefer N, Lysson M, Hirner A, Kalff JC (2010) Mechanical strain and TLR4 synergistically induce cell-specific inflammatory gene expression in intestinal smooth muscle cells and peritoneal macrophages. Am J Physiol Gastrointest Liver Physiol 299(5):G1187–G1197. doi:10.1152/ajpgi.00452.2009
Werfel J, Krause S, Bischof AG, Mannix RJ, Tobin H, Bar-Yam Y, Bellin RM, Ingber DE (2013) How changes in extracellular matrix mechanics and gene expression variability might combine to drive cancer progression. PLoS One 8(10):e76122. doi:10.1371/journal.pone.0076122
Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ (2005) Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 11(1–2):1–18. doi:10.1089/ten.2005.11.1
Winter GD (1974) Transcutaneous implants: reactions of the skin-implant interface. J Biomed Mater Res 8(3):99–113. doi:10.1002/jbm.820080311
Wojciak-Stothard B, Curtis A, Monaghan W, MacDonald K, Wilkinson C (1996) Guidance and activation of murine macrophages by nanometric scale topography. Exp Cell Res 223(2):426–435. doi:10.1006/excr.1996.0098
Wolfram D, Tzankov A, Piza-Katzer H (2006) Surgery for foreign body reactions due to injectable fillers. Dermatology 213(4):300–304. doi:10.1159/000096193
Xu LC, Siedlecki CA (2007) Effects of surface wettability and contact time on protein adhesion to biomaterial surfaces. Biomaterials 28(22):3273–3283. doi:10.1016/j.biomaterials.2007.03.032
Yan Y, Gause KT, Kamphuis MM, Ang CS, O’Brien-Simpson NM, Lenzo JC, Reynolds EC, Nice EC, Caruso F (2013) Differential roles of the protein corona in the cellular uptake of nanoporous polymer particles by monocyte and macrophage cell lines. ACS Nano 7(12):10960–10970. doi:10.1021/nn404481f
Zaveri TD, Lewis JS, Dolgova NV, Clare-Salzler MJ, Keselowsky BG (2014) Integrin-directed modulation of macrophage responses to biomaterials. Biomaterials 35(11):3504–3515. doi:10.1016/j.biomaterials.2014.01.007
Acknowledgments
Our original research investigating macrophage activation in response to biomaterials has been funded, in part, by the National Institute of Biomedical Imaging and Bioengineering (EB022374).
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Rayahin, J.E., Gemeinhart, R.A. (2017). Activation of Macrophages in Response to Biomaterials. In: Kloc, M. (eds) Macrophages. Results and Problems in Cell Differentiation, vol 62. Springer, Cham. https://doi.org/10.1007/978-3-319-54090-0_13
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