Identification of the CXCL12–CXCR4/CXCR7 axis as a potential therapeutic target for immunomodulating macrophage polarization and foreign body response to implanted biomaterials

HoHubbell, 2013, Translating materials design to the clinic, Nat. Mater., 12, 963, 10.1038/nmat3788 Anderson, 2008, Foreign body reaction to biomaterials, Semin. Immunol., 20, 86, 10.1016/j.smim.2007.11.004 Lin, 2014, Chronic inflammation in biomaterial-induced periprosthetic osteolysis: NF-κB as a therapeutic target, Acta Biomater., 10, 1, 10.1016/j.actbio.2013.09.034 Malik, 2011, Inflammasome components Asc and caspase-1 mediate biomaterial-induced inflammation and foreign body response, Proc. Natl. Acad. Sci. U. S. A., 13, 20095, 10.1073/pnas.1105152108 Zhang, 2013, Zwitterionic hydrogels implanted in mice resist the foreign-body reaction, Nat. Biotechnol., 31, 553, 10.1038/nbt.2580 Miller, 1989, In vitro stimulation of fibroblast activity by factors generated from human monocytes activated by biomedical polymers, J. Biomed. Mater. Res., 23, 911, 10.1002/jbm.820230808 Tian, 2009, Thrombospondin 2-null mice display an altered brain foreign body response to polyvinyl alcohol sponge implants, Biomed. Mater., 4, 10.1088/1748-6041/4/1/015010 Wynn, 2008, Cellular and molecular mechanisms of fibrosis, J. Pathol., 214, 199, 10.1002/path.2277 Wynn, 2012, Mechanisms of fibrosis: therapeutic translation for fibrotic disease, Nat. Med., 18, 1028, 10.1038/nm.2807 Langer, 2009, Perspectives and challenges in tissue engineering and regenerative medicine, Adv. Mater., 21, 3235, 10.1002/adma.200902589 Grainger, 2013, All charged up about implanted biomaterials, Nat. Biotechnol., 31, 507, 10.1038/nbt.2600 Jones, 2007, Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells, J. Biomed. Mater. Res. A, 83, 585, 10.1002/jbm.a.31221 Ma, 2014, Improved implant osseointegration of a nanostructured titanium surface via mediation of macrophage polarization, Biomaterials, 35, 9853, 10.1016/j.biomaterials.2014.08.025 Wynn, 2013, Macrophage biology in development, homeostasis and disease, Nature, 496, 445, 10.1038/nature12034 Spiller, 2017, Macrophage-based therapeutic strategies in regenerative medicine, Adv. Drug Deliv. Rev., 1, 74, 10.1016/j.addr.2017.05.010 Glaros, 2009, Macrophages and fibroblasts during inflammation, tissue damage and organ injury, Front. Biosci., 14, 3988, 10.2741/3506 Harding, 2014, Combating medical device fouling, Trends Biotechnol., 32, 140, 10.1016/j.tibtech.2013.12.004 Vegas, 2016, Combinatorial hydrogel library enables identification of materials that mitigate the foreign body response in primates, Nat. Biotechnol., 34, 345, 10.1038/nbt.3462 Paul, 2008, Topographical control of human macrophages by a regularly microstructured polyvinylidene fluoride surface, Biomaterials, 29, 4056, 10.1016/j.biomaterials.2008.07.010 Luu, 2015, Micro- and nanopatterned topographical cues for regulating macrophage cell shape and phenotype, ACS Appl. Mater. Interfaces, 7, 28665, 10.1021/acsami.5b10589 Spiller, 2015, Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds, Biomaterials, 37, 194, 10.1016/j.biomaterials.2014.10.017 Hachim, 2017, Shifts in macrophage phenotype at the biomaterial interface via IL-4 eluting coatings are associated with improved implant integration, Biomaterials, 112, 95, 10.1016/j.biomaterials.2016.10.019 Smith, 2017, Harnessing macrophage plasticity for tissue regeneration, Adv. Drug Deliv. Rev., 15, 193, 10.1016/j.addr.2017.04.012 Suzuki, 2014, Pulmonary macrophage transplantation therapy, Nature, 514, 450, 10.1038/nature13807 Lee, 2016, Macrophage-based cell therapies: the long and winding road, J. Control. Release, 240, 527, 10.1016/j.jconrel.2016.07.018 Rhen, 2005, Antiinflammatory action of glucocorticoids—new mechanisms for old drugs, N. Engl. J. Med., 353, 1711, 10.1056/NEJMra050541 Doloff, 2017, 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, 10.1038/nmat4866 Doitsidou, 2002, Guidance of primordial germ cell migration by the chemokine SDF-1, Cell, 111, 647, 10.1016/S0092-8674(02)01135-2 Burns, 2006, A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development, J. Exp. Med., 203, 2201, 10.1084/jem.20052144 Petruzziello-Pellegrini, 2012, The CXCR4/CXCR7/SDF-1 pathway contributes to the pathogenesis of Shiga toxin-associated hemolytic uremic syndrome in humans and mice, J. Clin. Invest., 122, 759, 10.1172/JCI57313 Melchionna, 2010, Induction of myogenic differentiation by SDF-1 via CXCR4 and CXCR7 receptors, Muscle Nerve, 41, 828, 10.1002/mus.21611 Song, 2014, Regeneration of chronic myocardial infarction by injectable hydrogels containing stem cell homing factor SDF-1 and angiogenic peptide Ac-SDKP, Biomaterials, 35, 2436, 10.1016/j.biomaterials.2013.12.011 Thevenot, 2010, The effect of incorporation of SDF-1a into PLGA scaffolds on stem cell recruitment and the inflammatory response, Biomaterials, 31, 3997, 10.1016/j.biomaterials.2010.01.144 Haider, 2008, IGF-l-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair, Circ. Res., 103, 1300, 10.1161/CIRCRESAHA.108.186742 Sánchez-Martín, 2013, CXCR7 impact on CXCL12 biology and disease, Trends Mol. Med., 19, 12, 10.1016/j.molmed.2012.10.004 Ma, 2013, Induction of C-X-C chemokine receptor type 7 (CXCR7) switches stromal cell-derived Factor-1 (SDF-1) signaling and phagocytic activity in macrophages linked to atherosclerosis, J. Biol. Chem., 288, 15481, 10.1074/jbc.M112.445510 Brenner, 2015, DPP-4 inhibition ameliorates atherosclerosis by priming monocytes into M2 macrophages, Int. J. Cardiol., 15, 163, 10.1016/j.ijcard.2015.07.044 Sánchez-Martín, 2011, The chemokine CXCL12 regulates monocyte-macrophage differentiation and RUNX3 expression, Blood, 117, 88, 10.1182/blood-2009-12-258186 Gibon, 2017, The biological response to orthopedic implants for joint replacement. II: Polyethylene, ceramics, PMMA, and the foreign body reaction, J. Biomed. Mater. Res. B: Appl. Biomater., 6, 1685, 10.1002/jbm.b.33676 Peterson, 1979, Clinical, radiographical, and histological evaluation of porous roote polymethylmethacrylate dental implants, J. Dent. Res., 58, 489, 10.1177/00220345790580010501 Vasconcelos, 2016, Fibrinogen scaffolds with immunomodulatory properties promote in vivo bone regeneration, Biomaterials, 111, 163, 10.1016/j.biomaterials.2016.10.004 Gilmore, 1999, The Rel/NF-kappaB signal transduction pathway: introduction, Oncogene, 18, 6842, 10.1038/sj.onc.1203237 Saleh, 2016, T.M. Grupp. Acrylic bone cement in total joint arthroplasty: a review, J. Orthop. Res., 34, 737, 10.1002/jor.23184 Rao, 2012, Revision joint replacement, wear particles, and macrophage polarization, Acta Biomater., 8, 2815, 10.1016/j.actbio.2012.03.042 He, 2015, Bone cements for percutaneous vertebroplasty and balloon kyphoplasty: current status and future developments, J. Orthop. Transl., 3, 1 Uto-Konomi, 2013, CXCR7 agonists inhibit the function of CXCL12 by down-regulation of CXCR4, Biochem. Biophys. Res. Commun., 431, 772, 10.1016/j.bbrc.2013.01.032 Oishi, 2015, Development of novel CXC chemokine receptor 7 (CXCR7) ligands: selectivity switch from CXCR4 antagonists with a cyclic pentapeptide scaffold, J. Med. Chem., 58, 5218, 10.1021/acs.jmedchem.5b00216 Karin, 2010, The multiple faces of CXCL12 (SDF-1a) in the regulation of immunity during health and disease, J. Leukoc. Biol., 88, 463, 10.1189/jlb.0909602 Zohar, 2008, CXCL12 (SDF-1a) suppresses ongoing experimental autoimmune encephalomyelitis by selecting antigenspecific regulatory T cells, J. Exp. Med., 205, 2643, 10.1084/jem.20080730 Wei, 2012, Upregulation of SDF-1 is associated with atherosclerosis lesions induced by LDL concentration polarization, Ann. Biomed. Eng., 40, 1018, 10.1007/s10439-011-0486-z Zernecke, 2008, Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis, Circ. Res., 102, 209, 10.1161/CIRCRESAHA.107.160697 Levoye, 2009, CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling, Blood, 113, 6085, 10.1182/blood-2008-12-196618 Song, 2019, CXCR7/CXCR4 heterodimer-induced histone demethylation: a new mechanism of colorectal tumorigenesis, Oncogene, 38, 1560, 10.1038/s41388-018-0519-2 Lawrence, 2011, Transcriptional regulation of macrophage polarization: enabling diversity with identity, Nat. Rev. Immunol., 11, 750, 10.1038/nri3088 Darnell, 1994, Jak–STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins, Science, 264, 1415, 10.1126/science.8197455 Takeda, 1996, Essential role of Stat6 in IL-4 signalling, Nature, 380, 627, 10.1038/380627a0 Mantovani, 2004, The chemokine system in diverse forms of macrophage activation and polarization, Trends Immunol., 25, 677, 10.1016/j.it.2004.09.015 O’Neill, 2006, Targeting signal transduction as a strategy to treat inflammatory diseases, Nat. Rev. Drug Discov., 5, 549, 10.1038/nrd2070 Furlong, 2017, Evolutionary and comparative genomics to drive rational drug design, with particular focus on neuropeptide seven-transmembrane receptors, Biomol. Ther. (Seoul), 25, 57, 10.4062/biomolther.2016.199 Furlong, 2014, Biased ligand modulation of seven transmembrane receptors (7TMRs): functional implications for drug discovery, Biomol. Ther. (Seoul), 57, 6887 Ahmad, 2015, Hunting for the function of orphan GPCRs - beyond the search for the endogenous ligand, Br. J. Pharmacol., 172, 3212, 10.1111/bph.12942 Rask-Andersen, 2011, Trends in the exploitation of novel drug targets, Nat. Rev. Drug Discov., 10, 579, 10.1038/nrd3478 Dondossola, 2016, Examination ofthe foreign body response to biomaterials by nonlinear intravital microscopy, Nat. Biomed. Eng., 1, 10.1038/s41551-016-0007 Ma, 2014, Atorvastatin inhibits CXCR7 induction to reduce macrophage migration, Biochem. Pharmacol., 89, 99, 10.1016/j.bcp.2014.02.014 Almuti, 2006, Effects of statins beyond lipid lowering: potential for clinical benefits, Int. J. Cardiol., 109, 7, 10.1016/j.ijcard.2005.05.056 Greenwood, 2006, Statin therapy and autoimmune disease: from protein prenylation to immunomodulation, Natl. Rev., 6, 358 Zhao, 2015, Simvastatin reduces burn injury-induced splenic apoptosis via down-regulation of the TNF-α/ NF-κB pathway, Ann. Surg., 261, 1006, 10.1097/SLA.0000000000000764 Dichtl, 2003, HMG-CoA reductase inhibitors regulate inflammatory transcription factors in human endothelial and vascular smooth muscle cells, Arterioscler. Thromb. Vasc. Biol., 23, 58, 10.1161/01.ATV.0000043456.48735.20