Contribution of αβ T cells to macrophage polarization and MSC recruitment and proliferation on titanium implants

Sadtler, 2019, Divergent immune responses to synthetic and biological scaffolds, Biomaterials, 192, 405, 10.1016/j.biomaterials.2018.11.002 Mariani, 2019, Biomaterials: foreign bodies or tuners for the immune response?, Int. J. Mol. Sci., 20, 636, 10.3390/ijms20030636 Wooley, 2002, Inflammatory responses to orthopaedic biomaterials in the murine air pouch, Biomaterials, 23, 517, 10.1016/S0142-9612(01)00134-X Selders, 2017, An overview of the role of neutrophils in innate immunity, inflammation and host-biomaterial integration, 4, 55 Hotchkiss, 2018, Macrophage response to hydrophilic biomaterials regulates MSC recruitment and T-helper cell populations, Biomaterials, 182, 202, 10.1016/j.biomaterials.2018.08.029 Li, 2020, Macrophage polarization plays roles in bone formation instructed by calcium phosphate ceramics, J. Mater. Chem. B, 8, 1863, 10.1039/C9TB02932J 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 Wang, 2018, Neutrophils in tissue injury and repair, Cell Tissue Res., 371, 531, 10.1007/s00441-017-2785-7 Jhunjhunwala, 2018, Neutrophils at the Biological-Material Interface, ACS Biomater. Sci. Eng., 4, 1128, 10.1021/acsbiomaterials.6b00743 Boersema, 2016, The effect of biomaterials used for tissue regeneration purposes on polarization of macrophages, Biores. Open Access, 5, 10.1089/biores.2015.0041 Abaricia, 2021, Surface characteristics on commercial dental implants differentially activate macrophages in vitro and in vivo, Clin. Oral. Implants Res., 32, 487, 10.1111/clr.13717 Abaricia, 2020, Wnt signaling modulates macrophage polarization and is regulated by biomaterial surface properties, Biomaterials, 243, 10.1016/j.biomaterials.2020.119920 Abaricia, 2020, Hydrophilic titanium surfaces reduce neutrophil inflammatory response and NETosis, Biomater. Sci., 8, 2289, 10.1039/C9BM01474H Abaricia, 2021, Control of innate immune response by biomaterial surface topography, energy, and stiffness, Acta Biomater., 133, 58, 10.1016/j.actbio.2021.04.021 Rodriguez, 2008, T cell subset distributions following primary and secondary implantation at subcutaneous biomaterial implant sites, J. Biomed. Mater. Res. A, 85A, 556, 10.1002/jbm.a.31562 Brodbeck, 2005, Lymphocytes and the foreign body response: lymphocyte enhancement of macrophage adhesion and fusion, J. Biomed. Mater. Res. A, 74A, 222, 10.1002/jbm.a.30313 Adusei, 2021, T lymphocytes as critical mediators in tissue regeneration, fibrosis, and the foreign body response, Acta Biomater., 133, 17, 10.1016/j.actbio.2021.04.023 Villalta, 2014, Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy, Sci. Transl. Med., 6, 258ra142, 10.1126/scitranslmed.3009925 Burzyn, 2013, A special population of regulatory T cells potentiates muscle repair, Cell, 155, 1282, 10.1016/j.cell.2013.10.054 Gravano, 2013, Promotion and prevention of autoimmune disease by CD8+ T cells, J. Autoimmun., 45, 68, 10.1016/j.jaut.2013.06.004 Weiner, 2004, Multiple sclerosis is an inflammatory T-cell–mediated autoimmune disease, Arch. Neurol., 61, 1613, 10.1001/archneur.61.10.1613 Ostroumov, 2017, CD4 and CD8 T lymphocyte interplay in controlling tumor growth, Cell. Mol. Life Sci., 75, 689, 10.1007/s00018-017-2686-7 Matkowski, 2009, The prognostic role of tumor-infiltrating CD4 and CD8 T lymphocytes in breast cancer, Anticancer Res., 29, 2445 Naito, 1998, CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer, Cancer Res., 58, 3491 Wherry, 2004, Memory CD8 T-cell differentiation during viral infection, J. Virol., 78, 5535, 10.1128/JVI.78.11.5535-5545.2004 Maloy, 2000, Cd4+ T cell subsets during virus infection: protective capacity depends on effector cytokine secretion and on migratory capability, J. Exp. Med., 191, 2159, 10.1084/jem.191.12.2159 Raphael, 2015, T cell subsets and their signature cytokines in autoimmune and inflammatory diseases, Cytokine, 74, 5, 10.1016/j.cyto.2014.09.011 Mousset, 2019, Comprehensive phenotyping of T cells using flow cytometry, Cytometry A., 95, 647, 10.1002/cyto.a.23724 Capone, 1998, Kinetics of T cell receptor β, γ, and δ rearrangements during adult thymic development: T cell receptor rearrangements are present in CD44+CD25+ Pro-T thymocytes, Proc. Natl. Acad. Sci. U. S. A., 95, 12522, 10.1073/pnas.95.21.12522 Wilson, 1996, T cell receptor delta gene rearrangement and T early alpha (TEA) expression in immature alpha beta lineage thymocytes: implications for alpha beta/gamma delta lineage commitment, Immunity, 4, 37, 10.1016/S1074-7613(00)80296-4 Lan, 2008, The regulatory, inflammatory, and T cell programming roles of interleukin-2 (IL-2), J. Autoimmun., 31, 7, 10.1016/j.jaut.2008.03.002 T.R. Malek, The main function of IL-2 is to promote the development of T regulatory cells, (n.d.). 10.1189/jlb.0603272. Ono, 2017, Osteoimmunology in Bone Fracture Healing, Curr. Osteoporos Rep, 15, 367, 10.1007/s11914-017-0381-0 S. Kalyan CeMCOR, It may seem inflammatory, but some T cells are innately healing to the bone, (2016). 10.1002/jbmr.2875. Sahbani, 2021, Absence of αβ T cells accelerates disuse bone loss in male mice after spinal cord injury, Ann. N. Y. Acad. Sci., 1487, 43, 10.1111/nyas.14518 Sun, 2022, gd T cells activated in different inflammatory environments are functionally distinct, J. Immunol., 208, 1224, 10.4049/jimmunol.2100967 Ribot, 2020, γδ T cells in tissue physiology and surveillance, Nat. Rev. Immunol., 21, 221, 10.1038/s41577-020-00452-4 Luckheeram, 2012, CD4+T cells: differentiation and functions, Clin. Dev. Immunol., 2012, 12, 10.1155/2012/925135 Mittrücker, 2014, Heterogeneity in the differentiation and function of CD8+ T cells, Arch. Immunol. Ther. Exp. (Warsz.), 62, 449, 10.1007/s00005-014-0293-y Wan, 2021, Novel Immune Subsets and Related Cytokines: Emerging Players in the Progression of Liver Fibrosis, Front Med (Lausanne), 8 Rother, 2015, Disturbed T cell signaling and altered Th17 and regulatory T cell subsets in the pathogenesis of systemic lupus erythematosus, Front. Immunol., 6, 610, 10.3389/fimmu.2015.00610 Yudoh, 2000, Reduced expression of the regulatory CD4 T cell subset is related to Th1/Th2 balance and disease severity in rheumatoid arthritis, Arthritis Rheum., 43, 617, 10.1002/1529-0131(200003)43:3<617::AID-ANR19>3.0.CO;2-B Smigielska-Czepiel, 2014, Comprehensive analysis of miRNA expression in T-cell subsets of rheumatoid arthritis patients reveals defined signatures of naive and memory Tregs, Genes Immun., 15, 115, 10.1038/gene.2013.69 Végran, 2015, Th9 cells: a novel CD4 T-cell subset in the immune war against cancer, Cancer Res., 75, 475, 10.1158/0008-5472.CAN-14-2748 Hirahara, 2016, CD4 + T-cell subsets in inflammatory diseases: beyond the Th1/Th2 paradigm, Int. Immunol., 28, 163, 10.1093/intimm/dxw006 Lazarevic, 2013, T-bet: a bridge between innate and adaptive immunity, Nat. Rev. Immunol., 13, 777, 10.1038/nri3536 Szabo, 2000, A novel transcription factor, T-bet, directs Th1 lineage commitment, Cell, 100, 655, 10.1016/S0092-8674(00)80702-3 Song, 2014, Th17 differentiation and their pro-inflammation function, Adv. Exp. Med. Biol., 841, 99, 10.1007/978-94-017-9487-9_5 Hori, 2003, Control of regulatory T cell development by the transcription factor Foxp3, Science, 299, 1057, 10.1126/science.1079490 Scheffold, 2007, Competition for cytokines: Treg cells take all, Nat. Immunol., 8, 1285, 10.1038/ni1207-1285 Lei, 2015, Regulatory T cell-mediated anti-inflammatory effects promote successful tissue repair in both indirect and direct manners, Front. Pharmacol., 6, 184, 10.3389/fphar.2015.00184 Kaplan, 2013, Professor, D. of Pediatric Pulmonary Basic Research, Th9 cells: differentiation and disease, Immunol. Rev., 252, 104, 10.1111/imr.12028 Deng, 2021, Deleterious role of th9 cells in pulmonary fibrosis, Cells, 10, 3209, 10.3390/cells10113209 Korn, 2009, IL-17 and Th17 Cells, Annu. Rev. Immunol., 27, 485, 10.1146/annurev.immunol.021908.132710 Jia, 2014, The biology and functions of Th22 cells, Adv. Exp. Med. Biol., 841, 209, 10.1007/978-94-017-9487-9_8 Basu, 2012, Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria, Immunity, 37, 1061, 10.1016/j.immuni.2012.08.024 Roman-Blas, 2022, CD8+ T Cells in OA knee joints are differentiated into subsets depending on OA stage and compartment, J. Clinic. Med., 11, 2814, 10.3390/jcm11102814 Hotchkiss, 2017, Dental implant surface chemistry and energy alter macrophage activation in vitro, Clin. Oral. Implants Res., 28, 414, 10.1111/clr.12814 Hotchkiss, 2016, Titanium surface characteristics, including topography and wettability, alter macrophage activation, Acta Biomater., 31, 425, 10.1016/j.actbio.2015.12.003 Avery, 2022, Canonical Wnt signaling enhances pro-inflammatory response to titanium by macrophages, Biomaterials, 289, 10.1016/j.biomaterials.2022.121797 Avery, 2023, Immune cell response to orthopedic and craniofacial biomaterials depends on biomaterial composition, Acta Biomater., 161, 285, 10.1016/j.actbio.2023.03.007 Wolfram, 2012, T regulatory cells and TH17 cells in peri-silicone implant capsular fibrosis, Plast. Reconstr. Surg., 129 Sadtler, 2016, Developing a pro-regenerative biomaterial scaffold microenvironment requires T helper 2 cells, Science, 352, 366, 10.1126/science.aad9272 Blaschke, 2003, Expression of activation-induced, T cell-derived, and chemokine-related cytokine/lymphotactin and its functional role in rheumatoid arthritis, Arthritis Rheum., 48, 1858, 10.1002/art.11171 Mosmann, 1997, Differentiation and functions of T cell subsets, CIBA Found. Symp., 148 Gawronska-Kozak, 2006, Scarless skin repair in immunodeficient mice, Wound Repair Regen., 14, 265, 10.1111/j.1743-6109.2006.00121.x Tumanov, 2009, T cell-derived lymphotoxin regulates liver regeneration, Gastroenterology, 136 Chung, 2020, Interleukin 17 and senescent cells regulate the foreign body response to synthetic material implants in mice and humans, Sci. Transl. Med., 12, 10.1126/scitranslmed.aax3799 Kopf, 1993, Disruption of the murine IL-4 gene blocks Th2 cytokine responses, Nature, 362, 245, 10.1038/362245a0 Brook, 2022, Transplantation Without Overimmunosuppression (TWO) study protocol: a phase 2b randomised controlled single-centre trial of regulatory T cell therapy to facilitate immunosuppression reduction in living donor kidney transplant recipients, BMJ Open, 12, 10.1136/bmjopen-2022-061864 Harden, 2021, Feasibility, long-term safety, and immune monitoring of regulatory T cell therapy in living donor kidney transplant recipients, Am. J. Transplant., 21, 1603, 10.1111/ajt.16395 Sawitzki, 2020, Regulatory cell therapy in kidney transplantation (The ONE Study): a harmonised design and analysis of seven non-randomised, single-arm, phase 1/2A trials, Lancet, 395, 1627, 10.1016/S0140-6736(20)30167-7 Todo, 2016, A pilot study of operational tolerance with a regulatory T-cell-based cell therapy in living donor liver transplantation, Hepatology, 64, 632, 10.1002/hep.28459 Shevach, 2009, Mechanisms of foxp3+ T regulatory cell-mediated suppression, Immunity, 30, 636, 10.1016/j.immuni.2009.04.010 Gravano, 2012, The battle against immunopathology: infectious tolerance mediated by regulatory T cells, Cell. Mol. Life Sci., 69, 1997, 10.1007/s00018-011-0907-z Barthlott, 2005, CD25+ CD4+ T cells compete with naive CD4+ T cells for IL-2 and exploit it for the induction of IL-10 production, Int. Immunol., 17, 279, 10.1093/intimm/dxh207 Nakamura, 2001, Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta, J. Exp. Med., 194, 629, 10.1084/jem.194.5.629 Collison, 2007, The inhibitory cytokine IL-35 contributes to regulatory T-cell function, Nature, 450, 566, 10.1038/nature06306 Chen, 2020, Progranulin improves acute lung injury through regulating the differentiation of regulatory T cells and interleukin-10 immunomodulation to promote macrophage polarization, Mediators Inflamm., 2020, 10.1155/2020/9704327 Zhu, 2008, CD4 T cells: fates, functions, and faults, Blood, 112, 1557, 10.1182/blood-2008-05-078154 jun Zhu, 2019, Role of dendritic cells in the host response to biomaterials and their signaling pathways, Acta Biomater., 94, 132, 10.1016/j.actbio.2019.05.038 Keselowsky, 2017, Dendritic cells in the host response to implanted materials, Semin. Immunol., 29, 33, 10.1016/j.smim.2017.04.002 Zheng, 2017, Effect of different titanium surfaces on maturation of murine bone marrow-derived dendritic cells, Sci. Rep., 7, 1 Mempel, 2004, T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases, Nature, 427, 154, 10.1038/nature02238 Godoy, 2020, Differences in T regulatory cells between mouse strains frequently used in immunological research: Treg cell quantities and subpopulations in NOD, B6 and BALB/c mice, Immunol. Lett., 223, 17, 10.1016/j.imlet.2020.04.006 Wang, 2019, Effect of adoptive transfer of CD4+CD25+Foxp3+ Treg induced by trichostatin A on the prevention of spontaneous abortion, J. Reprod. Immunol., 131, 30, 10.1016/j.jri.2018.12.002 Zhou, 2018, The immunosuppressive effects of CD4+ CD25+ regulatory T cells on dendritic cells in patients with chronic hepatitis B, J. Viral Hepat., 25, 733, 10.1111/jvh.12863 Saito, 2008, Sepsis is characterized by the increases in percentages of circulating CD4+CD25+ regulatory T cells and plasma levels of soluble CD25, Tohoku J. Exp. Med., 216, 61, 10.1620/tjem.216.61 Sakaguchi, 1995, Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases, J. Immunol., 155, 1151, 10.4049/jimmunol.155.3.1151 Yamazaki, 2003, Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells, J. Exp. Med., 198, 235, 10.1084/jem.20030422 Fontenot, 2005, Regulatory T cell lineage specification by the forkhead transcription factor foxp3, Immunity, 22, 329, 10.1016/j.immuni.2005.01.016 Fontenot, 2003, Foxp3 programs the development and function of CD4+CD25+ regulatory T cells, Nat. Immunol., 4, 986, 10.1038/ni904 Khattri, 2003, An essential role for Scurfin in CD4+CD25+ T regulatory cells, Nat. Immunol., 4, 993, 10.1038/ni909 Szabo, 2003, Molecular mechanisms regulating Th1 immune responses, Annu. Rev. Immunol., 21, 713, 10.1146/annurev.immunol.21.120601.140942 Ruterbusch, 2020, In vivo CD4+ T cell differentiation and function: revisiting the Th1/Th2 paradigm, Annu. Rev. Immunol., 38, 705, 10.1146/annurev-immunol-103019-085803 Zhu, 2020, The correlation between the Th17/Treg cell balance and bone health, Immun. Ageing, 17, 1, 10.1186/s12979-020-00202-z Sato, 2006, Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction, J. Exp. Med., 203, 2673, 10.1084/jem.20061775 Zaiss, 2007, Treg cells suppress osteoclast formation: a new link between the immune system and bone, Arthritis Rheum., 56, 4104, 10.1002/art.23138 Reinke, 2013, Terminally differentiated CD8+ T cells negatively affect bone regeneration in humans, Sci. Transl. Med., 5, 10.1126/scitranslmed.3004754 Zhang, 2010, Circulating mitochondrial DAMPs cause inflammatory responses to injury, Nature, 464, 104, 10.1038/nature08780 Pearl, 2011, Role of the Toll-like receptor pathway in the recognition of orthopedic implant wear-debris particles, Biomaterials, 32, 5535, 10.1016/j.biomaterials.2011.04.046 Midwood, 2010, DAMPening inflammation by modulating TLR signalling, Mediators Inflamm., 2010 Kolar, 2010, The early fracture hematoma and its potential role in fracture healing, Tissue Eng. Part B, 16, 427, 10.1089/ten.teb.2009.0687 Buchwald, 2013, Osteoclast-induced Foxp3+ CD8 T-cells limit bone loss in mice, Bone, 56, 163, 10.1016/j.bone.2013.05.024 Y. Choi, K.M. Woo, S.-H. Ko, Y.J. Lee, S.-J. Park, H.-M. Kim, B.S. Kwon, Osteoclastogenesis is enhanced by activated B cells but suppressed by activated CD8 + T cells, (n.d.). 10.1002/1521-4141. Buchwald, 2013, Osteoclasts and CD8 T cells form a negative feedback loop that contributes to homeostasis of both the skeletal and immune systems, Clin. Dev. Immunol., 2013, 10.1155/2013/429373 Liu, 2011, Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-γ and TNF-α, Nat. Med., 17, 1594, 10.1038/nm.2542 Anderson, 2011, Biocompatibility of implants: Lymphocyte/macrophage interactions, Semin. Immunopathol., 33, 221, 10.1007/s00281-011-0244-1 Rodriguez, 2010, Evaluation of clinical biomaterial surface effects on T lymphocyte activation, J. Biomed. Mater. Res. A, 92A, 214, 10.1002/jbm.a.32362 Zhu, 2020, The role of T cells and macrophages in asthma pathogenesis: a new perspective on mutual crosstalk, Mediators Inflamm., 2020 Atcha, 2021, Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing, Nat. Commun., 12, 10.1038/s41467-021-23482-5 Sridharan, 2019, Material stiffness influences the polarization state, function and migration mode of macrophages, Acta Biomater., 89, 47, 10.1016/j.actbio.2019.02.048 Meli, 2020, YAP-mediated mechanotransduction tunes the macrophage inflammatory response, Sci. Adv., 6, 10.1126/sciadv.abb8471 Guerriero, 2019, Macrophages: their untold story in T cell activation and function, Int. Rev. Cell Mol. Biol., 342, 73, 10.1016/bs.ircmb.2018.07.001 Anderson, 2008, Foreign body reaction to biomaterials, Semin. Immunol., 20, 86, 10.1016/j.smim.2007.11.004 Dorner, 2002, MIP-1α, MIP-1β, RANTES, and ATAC/lymphotactin function together with IFN-γ as type 1 cytokines, Proc. Natl. Acad. Sci. U. S. A., 99, 6181, 10.1073/pnas.092141999 Cocchi, 1995, Identification of RANTES, MIP-1α, and MIP-1β as the major HIV-suppressive factors produced by CD8+ T cells, Science, 270, 1811, 10.1126/science.270.5243.1811 Tiemessen, 2007, CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages, Proc. Natl. Acad. Sci. U. S. A., 104, 19446, 10.1073/pnas.0706832104 Denis, 2004, Ability of T cell subsets and their soluble mediators to modulate the replication of Mycobacterium bovis in bovine macrophages, Cell. Immunol., 232, 1, 10.1016/j.cellimm.2005.01.003 Cassini-Vieira, 2018, Lack of interferon-gamma attenuates foreign body reaction to subcutaneous implants in mice, J. Biomed. Mater. Res. A, 106, 2243, 10.1002/jbm.a.36416 Chen, 2022, Mesenchymal stem cell-immune cell interaction and related modulations for bone tissue engineering, Stem Cells Int., 2022, 10.1155/2022/7153584 Pharoah, 2006, Expression of the inflammatory chemokines CCL5, CCL3 and CXCL10 in juvenile idiopathic arthritis, and demonstration of CCL5 production by an atypical subset of CD8+ T cells, Arthritis Res. Ther., 8, 1, 10.1186/ar1913 Zhou, 2014, Regulatory T cells enhance mesenchymal stem cell survival and proliferation following autologous cotransplantation in ischemic myocardium, J. Thorac. Cardiovasc. Surg., 148, 1131, 10.1016/j.jtcvs.2014.06.029 Croes, 2016, Proinflammatory T cells and IL-17 stimulate osteoblast differentiation, Bone, 84, 262, 10.1016/j.bone.2016.01.010 Rifas, 2003, Inflammatory T cells rapidly induce differentiation of human bone marrow stromal cells into mature osteoblasts, J. Cell. Biochem., 88, 650, 10.1002/jcb.10436