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Cited by 184Wound Healing and TreatmentsTissue Engineering and Regenerative MedicineOrthopaedic implants and arthroplasty

Implant Fibrosis and the Underappreciated Role of Myofibroblasts in the Foreign Body Reaction

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Noskovicova, Nina, Hinz, Boris, Pakshir, Pardis·2021·Cells
DOI 10.3390/cells10071794PMC PMC8304203
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Abstract

Body implants and implantable medical devices have dramatically improved and prolonged the life of countless patients. However, our body repair mechanisms have evolved to isolate, reject, or destroy any object that is recognized as foreign to the organism and inevitably mounts a foreign body reaction (FBR). Depending on its severity and chronicity, the FBR can impair implant performance or create severe clinical complications that will require surgical removal and/or replacement of the faulty device. The number of review articles discussing the FBR seems to be proportional to the number of different implant materials and clinical applications and one wonders, what else is there to tell? We will here take the position of a fibrosis researcher (which, coincidentally, we are) to elaborate similarities and differences between the FBR, normal wound healing, and chronic healing conditions that result in the development of peri-implant fibrosis. After giving credit to macrophages in the inflammatory phase of the FBR, we will mainly focus on the activation of fibroblastic cells into matrix-producing and highly contractile myofibroblasts. While fibrosis has been discussed to be a consequence of the disturbed and chronic inflammatory milieu in the FBR, direct activation of myofibroblasts at the implant surface is less commonly considered. Thus, we will provide a perspective how physical properties of the implant surface control myofibroblast actions and accumulation of stiff scar tissue. Because formation of scar tissue at the surface and around implant materials is a major reason for device failure and extraction surgeries, providing implant surfaces with myofibroblast-suppressing features is a first step to enhance implant acceptance and functional lifetime. Alternative therapeutic targets are elements of the myofibroblast mechanotransduction and contractile machinery and we will end with a brief overview on such targets that are considered for the treatment of other organ fibroses.

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  • Secreted signaling proteins also activate adaptive immune cells presented by B cells, CD4+ T cells, CD8+ T cells, natural killer cells, etc.

    “In addition, secreted signaling proteins also activate adaptive immune cells presented by B cells, CD4+ T cells, CD8+ T cells, natural killer cells, etc.”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [206]

    Section 5 (page unavailable) says macrophages produce pro-inflammatory cytokines and have effects on adaptive immune cells during the foreign body reaction, supporting the broad signaling claim. It does not identify B cells, CD4+ or CD8+ T cells, and NK cells as cells activated by those secreted proteins; section 8 mentions T cells and NK cells only in a separate discussion of cell depletion. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Released pro-inflammatory cytokines, chemokines, and oxide radicals recruit other neutrophils, mast cells, and monocytes/macrophages.

    “Released pro-inflammatory cytokines, chemokines, and oxide radicals recruit other neutrophils, mast cells, and monocytes/macrophages.”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [206]

  • Pattern recognition receptors situated in the innate immune cell membranes recognize the temporary matrix proteins and target the material for phagocytosis.

    “Pattern recognition receptors situated in the innate immune cell membranes recognize the temporary matrix proteins and target the material for phagocytosis [206].”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [206]

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  1. [1]Ratner B.D. Biomaterials: Been There, Done That, and Evolving into the Future Annu. Rev. Biomed. Eng. 2019 21 171 191 10.1146/annurev-bioeng-062117-120940 31167106 · DOI
  2. [3]Anderson J.M. Exploiting the inflammatory response on biomaterials research and development J. Mater. Sci. Mater. Electron. 2015 26 121 10.1007/s10856-015-5423-5 25690617 · DOI
  3. [5]Veiseh O. Vegas A.J. Domesticating the foreign body response: Recent advances and applications Adv. Drug Deliv. Rev. 2019 144 148 161 10.1016/j.addr.2019.08.010 31491445 PMC6774350 · DOI · Paper page
  4. [6]Williams D.F. Biocompatibility Pathways: Biomaterials-Induced Sterile Inflammation, Mechanotransduction, and Principles of Biocompatibility Control ACS Biomater. Sci. Eng. 2017 3 2 35 10.1021/acsbiomaterials.6b00607 33429689 · DOI
  5. [7]Klopfleisch R. Jung F. The pathology of the foreign body reaction against biomaterials J. Biomed. Mater. Res. Part A 2017 105 927 940 10.1002/jbm.a.35958 27813288 · DOI · Paper page
  6. [8]Grainger D.W. All charged up about implanted biomaterials Nat. Biotechnol. 2013 31 507 509 10.1038/nbt.2600 23752436 · DOI
  7. [9]Adusei K.M. Ngo T.B. Sadtler K. T lymphocytes as critical mediators in tissue regeneration, fibrosis, and the foreign body response Acta Biomater. 2021 10.1016/j.actbio.2021.04.023 33905946 · DOI
  8. [10]Greiner A.M. Sales A. Chen H. Biela S.A. Kaufmann D. Kemkemer R. Nano- and microstructured materials for in vitro studies of the physiology of vascular cells Beilstein J. Nanotechnol. 2016 7 1620 1641 10.3762/bjnano.7.155 28144512 PMC5238670 · DOI
  9. [11]Abaricia J.O. Farzad N. Heath T.J. Simmons J. Morandini L. Olivares-Navarrete R. Control of innate immune response by biomaterial surface topography, energy, and stiffness Acta Biomater. 2021 10.1016/j.actbio.2021.04.021 PMC8497396 33882355 · DOI · Paper page
  10. [12]Mariani E. Lisignoli G. Borzì R.M. Pulsatelli L. Biomaterials: Foreign Bodies or Tuners for the Immune Response? Int. J. Mol. Sci. 2019 20 636 10.3390/ijms20030636 30717232 PMC6386828 · DOI · Paper page
  11. [13]Rosner G.A. Fonacier L.S. Hypersensitivity to biomedical implants: Prevention and diagnosis Allergy Asthma Proc. 2017 38 177 183 10.2500/aap.2017.38.4052 28441987 · DOI
  12. [14]Schalock P.C. Thyssen J.P. Patch Testers’ Opinions Regarding Diagnostic Criteria for Metal Hypersensitivity Reactions to Metallic Implants Dermatitis 2013 24 183 185 10.1097/DER.0b013e31829cb113 23857019 · DOI
  13. [15]Porter J.A. Von Fraunhofer J.A. Success or failure of dental implants? A literature review with treatment considerations Gen. Dent. 2005 53 423 16366052
  14. [16]Liaw K. Delfini R.H. Abrahams J.J. Dental Implant Complications Semin. Ultrasound CT MR 2015 36 427 433 10.1053/j.sult.2015.09.007 26589696 · DOI
  15. [17]Tolman D.E. Laney W.R. Tolman D.E. Laney W.R. Tissue-integrated prosthesis complications Int. J. Oral Maxillofac. Implant. 1992 7 477 484 10.1097/00008505-199309000-00018 1299643 · DOI
  16. [18]Quirynen M. De Soete M. Van Steenberghe D. Infectious risks for oral implants: A review of the literature Clin. Oral Implant. Res. 2002 13 1 19 10.1034/j.1600-0501.2002.130101.x 12005139 · DOI
  17. [19]Gibon E. Amanatullah D.F. Loi F. Pajarinen J. Nabeshima A. Yao Z. Hamadouche M. Goodman S.B. The biological response to orthopaedic implants for joint replacement: Part I: Metals J. Biomed. Mater. Res. Part B Appl. Biomater. 2017 105 2162 2173 10.1002/jbm.b.33734 PMC5537059 27328111 · DOI
  18. [20]Urban R.M. Jacobs J. Tomlinson M.J. Gavrilovic J. Black J. Peoc’H M. Dissemination of Wear Particles to the Liver, Spleen, and Abdominal Lymph Nodes of Patients with Hip or Knee Replacement J. Bone Jt. Surg. Am. Vol. 2000 82 457 477 10.2106/00004623-200004000-00002 10761937 · DOI
  19. [21]Hauser R.G. Katsiyiannis W.T. Gornick C.C. Almquist A.K. Kallinen L.M. Deaths and cardiovascular injuries due to device-assisted implantable cardioverter-defibrillator and pacemaker lead extraction Europace 2009 12 395 401 10.1093/europace/eup375 19946113 PMC2825385 · DOI · Paper page
  20. [22]Nof E. Epstein L. Complications of cardiac implants: Handling device infections Eur. Hear. J. 2013 34 229 236 10.1093/eurheartj/ehs352 23091204 · DOI
  21. [23]Tarakji K.G. Chan E.J. Cantillon D.J. Doonan A.L. Hu T. Schmitt S. Fraser T.G. Kim A. Gordon S.M. Wilkoff B. Cardiac implantable electronic device infections: Presentation, management, and patient outcomes Hear. Rhythm. 2010 7 1043 1047 10.1016/j.hrthm.2010.05.016 20470904 · DOI
  22. [24]Baman T.S. Gupta S.K. Valle J.A. Yamada E. Risk Factors for Mortality in Patients with Cardiac Device-Related Infection Circ. Arrhythmia Electrophysiol. 2009 2 129 134 10.1161/CIRCEP.108.816868 19808457 · DOI
  23. [25]Keiler J. Schulze M. Sombetzki M. Heller T. Tischer T. Grabow N. Wree A. Bänsch D. Neointimal fibrotic lead encapsulation—Clinical challenges and demands for implantable cardiac electronic devices J. Cardiol. 2017 70 7 17 10.1016/j.jjcc.2017.01.011 28583688 · DOI
  24. [27]Smith M.C. Love C.J. Extraction of Transvenous Pacing and ICD Leads Pacing Clin. Electrophysiol. 2008 31 736 752 10.1111/j.1540-8159.2008.01079.x 18507548 · DOI
  25. [28]Yakish S.J. Narula A. Foley R. Kohut A. Kutalek S. Superior Vena Cava Echocardiography as a Screening Tool to Predict Cardiovascular Implantable Electronic Device Lead Fibrosis J. Cardiovasc. Ultrasound 2015 23 27 31 10.4250/jcu.2015.23.1.27 25883753 PMC4398781 · DOI
  26. [29]Borenstein A. Friedman O. Combined Breast Implant Explantation and Multilevel Mastopexy Technique Plast. Reconstr. Surg. Glob. Open 2019 7 e2429 10.1097/GOX.0000000000002429 31741816 PMC6799404 · DOI
  27. [30]Gabriel A. Maxwell G.P. The Evolution of Breast Implants Clin. Plast. Surg. 2015 42 399 404 10.1016/j.cps.2015.06.015 26408431 · DOI
  28. [32]Deva A.K. Adams W.P. Jr. Vickery K. The Role of Bacterial Biofilms in Device-Associated Infection Plast. Reconstr. Surg. 2013 132 1319 1328 10.1097/PRS.0b013e3182a3c105 23924649 · DOI
  29. [33]Coroneos C.J. Selber J.C. Offodile A.C. 2nd Butler C.E. Clemens M.W. US FDA Breast Implant Postapproval Studies: Long-term Outcomes in 99,993 Patients Ann Surg. 2019 269 30 36 10.1097/SLA.0000000000002990 30222598 · DOI
  30. [34]Headon H. Kasem A. Mokbel K. Capsular Contracture after Breast Augmentation: An Update for Clinical Practice Arch. Plast. Surg. 2015 42 532 543 10.5999/aps.2015.42.5.532 26430623 PMC4579163 · DOI
  31. [35]Steiert A. Sorg H. Boyce M. Capsular contracture by silicone breast implants: Possible causes, biocompatibility, and prophylactic strategies Med. Devices Évid. Res. 2013 6 211 218 10.2147/MDER.S49522 24324348 PMC3855100 · DOI
  32. [36]Collett D.J. Rakhorst H. Lennox P. Magnusson M. Cooter R. Deva A. Current Risk Estimate of Breast Implant–Associated Anaplastic Large Cell Lymphoma in Textured Breast Implants Plast. Reconstr. Surg. 2019 143 30S 40S 10.1097/PRS.0000000000005567 30817554 · DOI
  33. [37]Stack A. Ali N. Khan N. Breast Implant-associated Anaplastic Large Cell Lymphoma: A Review with Emphasis on the Role of Brentuximab Vedotin J. Cell Immunol. 2020 2 80 89 32914146 PMC7480932
  34. [38]Clemens M.W. Medeiros L.J. Butler C.E. Hunt K.K. Fanale M.A. Horwitz S. Weisenburger D.D. Liu J. Morgan E. Kanagal-Shamanna R. Complete Surgical Excision Is Essential for the Management of Patients with Breast Implant–Associated Anaplastic Large-Cell Lymphoma J. Clin. Oncol. 2016 34 160 168 10.1200/JCO.2015.63.3412 26628470 PMC4872006 · DOI
  35. [39]Clemens M.W. Brody G.S. Mahabir R.C. Miranda R.N. How to Diagnose and Treat Breast Implant-Associated Anaplastic Large Cell Lymphoma Plast Reconstr. Surg. 2018 141 586e 599e 10.1097/PRS.0000000000004262 29595739 · DOI
  36. [40]Sue G.R. Long C. Lee G.K. Management of Mastectomy Skin Necrosis in Implant Based Breast Reconstruction Ann. Plast. Surg. 2017 78 S208 S211 10.1097/SAP.0000000000001045 28301366 · DOI
  37. [41]Hultman C.S. Daiza S. Skin-Sparing Mastectomy Flap Complications After Breast Reconstruction: Review of Incidence, Management, and Outcome Ann. Plast. Surg. 2003 50 249 255 10.1097/01.SAP.0000046784.70583.E1 12800900 · DOI
  38. [42]Rivera-Chacon D.M. Alvarado-Velez M. Acevedo-Morantes C. Singh S.P. Gultepe E. Nagesha D. Sridhar S. Ramirez-Vick J. Fibronectin and Vitronectin Promote Human Fetal Osteoblast Cell Attachment and Proliferation on Nanoporous Titanium Surfaces J. Biomed. Nanotechnol. 2013 9 1092 1097 10.1166/jbn.2013.1601 23858975 PMC3718483 · DOI
  39. [43]Zhang L. Cao Z. Bai T. Carr L.R. Ella-Menye J.-R. Irvin C. Ratner B.D. Jiang S. Zwitterionic hydrogels implanted in mice resist the foreign-body reaction Nat. Biotechnol. 2013 31 553 556 10.1038/nbt.2580 23666011 · DOI · Paper page
  40. [44]Gorbet M.B. Sefton M.V. Biomaterial-associated thrombosis: Roles of coagulation factors, complement, platelets and leukocytes Biomaterials 2004 25 5681 5703 10.1016/j.biomaterials.2004.01.023 15147815 · DOI · Paper page
  41. [45]Jenney C.R. Anderson J.M. Adsorbed serum proteins responsible for surface dependent human macrophage behavior J. Biomed. Mater. Res. 1999 49 435 447 10.1002/(SICI)1097-4636(20000315)49:4<435::AID-JBM2>3.0.CO;2-Y 10602077 · DOI
  42. [46]Wells L.A. Guo H. Emili A. Sefton M.V. The profile of adsorbed plasma and serum proteins on methacrylic acid copolymer beads: Effect on complement activation Biomaterials 2017 118 74 83 10.1016/j.biomaterials.2016.11.036 27940384 · DOI
  43. [47]Zdolsek J. Eaton J.W. Tang L. Histamine release and fibrinogen adsorption mediate acute inflammatory responses to biomaterial implants in humans J. Transl. Med. 2007 5 31 10.1186/1479-5876-5-31 17603911 PMC1929055 · DOI · Paper page
  44. [48]Wulff B.C. Wilgus T.A. Mast cell activity in the healing wound: More than meets the eye? Exp. Dermatol. 2013 22 507 510 10.1111/exd.12169 23802591 PMC3723719 · DOI
  45. [49]Komi D.E.A. Khomtchouk K. Maria P.L.S. A Review of the Contribution of Mast Cells in Wound Healing: Involved Molecular and Cellular Mechanisms Clin. Rev. Allergy Immunol. 2020 58 298 312 10.1007/s12016-019-08729-w 30729428 · DOI
  46. [52]Van Dyken S.J. Locksley R.M. Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: Roles in homeostasis and disease Annu. Rev. Immunol. 2013 31 317 343 10.1146/annurev-immunol-032712-095906 23298208 PMC3606684 · DOI
  47. [53]Kenneth Ward W. 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 2 768 777 10.1177/193229680800200504 19885259 PMC2769792 · DOI
  48. [55]Safferling K. Sütterlin T. Westphal K. Ernst C. Breuhahn K. James M. Jäger D. Halama N. Grabe N. Wound healing revised: A novel reepithelialization mechanism revealed by in vitro and in silico models J. Cell Biol. 2013 203 691 709 10.1083/jcb.201212020 24385489 PMC3840932 · DOI
  49. [57]Schuster R. Rockel J.S. Kapoor M. Hinz B. The inflammatory speech of fibroblasts Immunol. Rev. 2021 10.1111/imr.12971 33987902 · DOI
  50. [58]Hinz B. Lagares D. Evasion of apoptosis by myofibroblasts: A hallmark of fibrotic diseases Nat. Rev. Rheumatol. 2020 16 11 31 10.1038/s41584-019-0324-5 31792399 PMC7913072 · DOI
  51. [60]Dorin R.P. Pohl H.G. De Filippo R.E. Yoo J.J. Atala A. Tubularized urethral replacement with unseeded matrices: What is the maximum distance for normal tissue regeneration? World J. Urol. 2008 26 323 326 10.1007/s00345-008-0316-6 18682960 · DOI
  52. [61]Atala A. Engineering organs Curr. Opin. Biotechnol. 2009 20 575 592 10.1016/j.copbio.2009.10.003 19896823 · DOI
  53. [62]Veiseh O. Doloff J. Ma M. Vegas A.F. Tam H.H. Bader A.R. Li J. Langan E. Wyckoff J. Loo W. Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates Nat. Mater. 2015 14 643 651 10.1038/nmat4290 25985456 PMC4477281 · DOI · Paper page
  54. [63]Vroman L. Adams A.L. Fischer G.C. Munoz P.C. Interaction of high molecular weight kininogen, factor XII, and fibrinogen in plasma at interfaces Blood 1980 55 156 159 10.1182/blood.V55.1.156.156 7350935 · DOI · Paper page
  55. [64]Swartzlander M.D. Barnes C.A. Blakney A.K. Kaar J.L. Kyriakides T.R. Bryant S.J. Linking the foreign body response and protein adsorption to PEG-based hydrogels using proteomics Biomaterials 2015 41 26 36 10.1016/j.biomaterials.2014.11.026 25522962 PMC4629245 · DOI · Paper page
  56. [65]Thang L. Thevenot P. Hu W. Surface Chemistry Influences Implant Biocompatibility Curr. Top. Med. Chem. 2008 8 270 280 10.2174/156802608783790901 18393890 PMC3230929 · DOI · Paper page
  57. [66]Zhou G. Loppnow H. Groth T. A macrophage/fibroblast co-culture system using a cell migration chamber to study inflammatory effects of biomaterials Acta Biomater. 2015 26 54 63 10.1016/j.actbio.2015.08.020 26292266 · DOI · Paper page
  58. [67]Sussman E. Halpin M.C. Muster J. Moon R. Ratner B.D. Porous Implants Modulate Healing and Induce Shifts in Local Macrophage Polarization in the Foreign Body Reaction Ann. Biomed. Eng. 2014 42 1508 1516 10.1007/s10439-013-0933-0 24248559 · DOI · Paper page
  59. [69]Noskovicova N. Schuster R. van Putten S. Ezzo M. Koehler A. Boo S. Coelho N.M. Griggs D. Ruminski P. McCulloch C.A. Suppression of the fibrotic encapsulation of silicone implants by inhibiting the mechanical activation of pro-fibrotic TGF-beta Nat. Biomed. Eng. 2021 10.1038/s41551-021-00722-z 34031559 · DOI
  60. [70]Blakney A.K. Swartzlander M.D. 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 2012 100 1375 1386 10.1002/jbm.a.34104 22407522 PMC3339197 · DOI · Paper page
  61. [71]Prasad B.R. Brook M.A. Smith T. Zhao S. Chen Y. Sheardown H. D’Souza R. Rochev Y. Controlling cellular activity by manipulating silicone surface roughness Colloids Surf. B Biointerfaces 2010 78 237 242 10.1016/j.colsurfb.2010.03.006 20363600 · DOI
  62. [72]Ananth H. Kundapur V. Mohammed H.S. Anand M. Amarnath G.S. Mankar S. A Review on Biomaterials in Dental Implantology Int. J. Biomed. Sci. IJBS 2015 11 113 120 26508905 PMC4614011
  63. [73]Ermis M. Antmen E. Hasirci V. Micro and Nanofabrication methods to control cell-substrate interactions and cell behavior: A review from the tissue engineering perspective Bioact. Mater. 2018 3 355 369 10.1016/j.bioactmat.2018.05.005 29988483 PMC6026330 · DOI
  64. [74]Doloff J.C. Veiseh O. de Mezerville R. Sforza M. Perry T.A. Haupt J. Jamiel M. Chambers C. Nash A. Aghlara-Fotovat S. The surface topography of silicone breast implants mediates the foreign body response in mice, rabbits and humans Nat. Biomed. Eng. 2021 10.1038/s41551-021-00739-4 34155355 · DOI
  65. [75]Wilson C.J. Clegg R. Leavesley D. Pearcy M. Mediation of Biomaterial–Cell Interactions by Adsorbed Proteins: A Review Tissue Eng. 2005 11 1 18 10.1089/ten.2005.11.1 15738657 · DOI · Paper page
  66. [76]Liamas E. Kubiak-Ossowska K. Black R.A. Thomas O.R. Zhang Z.J. Mulheran P.A. Adsorption of Fibronectin Fragment on Surfaces Using Fully Atomistic Molecular Dynamics Simulations Int. J. Mol. Sci. 2018 19 3321 10.3390/ijms19113321 PMC6275015 30366398 · DOI
  67. [77]Felgueiras H.P. Evans M.D.M. Migonney V. Contribution of fibronectin and vitronectin to the adhesion and morphology of MC3T3-E1 osteoblastic cells to poly(NaSS) grafted Ti6Al4V Acta Biomater. 2015 28 225 233 10.1016/j.actbio.2015.09.030 26415777 · DOI
  68. [79]Wei J. Igarashi T. Okumori N. Igarashi T. Maetani T. Liu B. Yoshinari M. Influence of surface wettability on competitive protein adsorption and initial attachment of osteoblasts Biomed. Mater. 2009 4 045002 10.1088/1748-6041/4/4/045002 19525576 · DOI
  69. [80]Tan F. Al-Rubeai M. Customizable Implant-specific and Tissue-Specific Extracellular Matrix Protein Coatings Fabricated Using Atmospheric Plasma Front. Bioeng. Biotechnol. 2019 7 247 10.3389/fbioe.2019.00247 31637236 PMC6787931 · DOI
  70. [81]Khandwekar A. Rho C.K. Modulation of cellular responses on engineered polyurethane implants J. Biomed. Mater. Res. Part A 2012 100 2211 2222 10.1002/jbm.a.34146 22492665 · DOI
  71. [82]He Y. Hower J. Chen S. Bernards M.T. Chang Y. Jiang S. Molecular Simulation Studies of Protein Interactions with Zwitterionic Phosphorylcholine Self-Assembled Monolayers in the Presence of Water Langmuir 2008 24 10358 10364 10.1021/la8013046 18690732 · DOI
  72. [83]Damodaran V.B. Murthy N.S. Bio-inspired strategies for designing antifouling biomaterials Biomater. Res. 2016 20 18 10.1186/s40824-016-0064-4 27326371 PMC4913429 · DOI
  73. [84]Sandor M. Singh D. Silverman R.P. Xu H. De Deyne P.G. Comparative Host Response of 2 Human Acellular Dermal Matrices in a Primate Implant Model Eplasty 2014 14 e7 24570768 PMC3914385
  74. [85]Mathieu V. Vayron R. Richard G. Lambert G. Naili S. Meningaud J.-P. Haiat G. Biomechanical determinants of the stability of dental implants: Influence of the bone–implant interface properties J. Biomech. 2014 47 3 13 10.1016/j.jbiomech.2013.09.021 24268798 · DOI
  75. [86]Vagaská B. Bacáková L. Filová E. Balík K. Osteogenic cells on bio-inspired materials for bone tissue engineering Physiol. Res. 2009 59 309 322 19681662
  76. [87]Tang D. Yang L.-Y. Ou K.-L. Oreffo R. Repositioning Titanium: An In Vitro Evaluation of Laser-Generated Microporous, Microrough Titanium Templates as a Potential Bridging Interface for Enhanced Osseointegration and Durability of Implants Front. Bioeng. Biotechnol. 2017 5 77 10.3389/fbioe.2017.00077 29322044 PMC5732141 · DOI
  77. [88]Lim J.Y. Hansen J.C. Siedlecki C.A. Runt J. Donahue H.J. Human foetal osteoblastic cell response to polymer-demixed nanotopographic interfaces J. R. Soc. Interface 2005 2 97 108 10.1098/rsif.2004.0019 16849169 PMC1578253 · DOI
  78. [89]Zhang Y. Chen S.E. Shao J. Beucken J.J.J.P.V.D. Combinatorial Surface Roughness Effects on Osteoclastogenesis and Osteogenesis ACS Appl. Mater. Interfaces 2018 10 36652 36663 10.1021/acsami.8b10992 30270615 PMC6213029 · DOI
  79. [90]Harvey A.G. Hill E. Bayat A. Designing implant surface topography for improved biocompatibility Expert Rev. Med. Devices 2013 10 257 267 10.1586/erd.12.82 23480094 · DOI
  80. [91]Wixtrom R.N. Garadi V. Leopold J. Canady J.W. Device-Specific Findings of Imprinted-Texture Breast Implants: Characteristics, Risks, and Benefits Aesthetic Surg. J. 2019 40 167 173 10.1093/asj/sjz155 31121016 · DOI
  81. [92]Wong C.-H. Samuel M. Tan B.-K. Song C. Capsular Contracture in Subglandular Breast Augmentation with Textured versus Smooth Breast Implants: A Systematic Review Plast. Reconstr. Surg. 2006 118 1224 1236 10.1097/01.prs.0000237013.50283.d2 17016195 · DOI
  82. [93]Liu X. Zhou L. Pan F. Gao Y. Yuan X. Fan D. Comparison of the Postoperative Incidence Rate of Capsular Contracture among Different Breast Implants: A Cumulative Meta-Analysis PLoS ONE 2015 10 e0116071 10.1371/journal.pone.0116071 25680100 PMC4332657 · DOI
  83. [94]Shin B.H. Kim B.H. Kim S. Lee K. Bin Choy Y. Heo C.Y. Silicone breast implant modification review: Overcoming capsular contracture Biomater. Res. 2018 22 37 10.1186/s40824-018-0147-5 30598837 PMC6302391 · DOI
  84. [95]Barnsley G.P. Sigurdson L.J. Barnsley S.E. Textured Surface Breast Implants in the Prevention of Capsular Contracture among Breast Augmentation Patients: A Meta-Analysis of Randomized Controlled Trials Plast. Reconstr. Surg. 2006 117 2182 2190 10.1097/01.prs.0000218184.47372.d5 16772915 · DOI
  85. [96]Stevens W.G. Nahabedian M.Y. Calobrace M.B. Harrington J.L. Capizzi P.J. Cohen R. d’Incelli R.C. Beckstrand M. Risk factor analysis for capsular contracture: A 5-year Sientra study analysis using round, smooth, and textured implants for breast augmentation Plast Reconstr Surg. 2013 132 1115 1123 10.1097/01.prs.0000435317.76381.68 24056498 · DOI
  86. [97]Derby B.M. Codner M.A. Textured silicone breast implant use in primary augmentation: Core data update and review Plast. Reconstr. Surg. 2015 135 113 124 10.1097/PRS.0000000000000832 25539301 · DOI
  87. [98]Barr S. Hill E. Bayat A. Development, fabrication and evaluation of a novel biomimetic human breast tissue derived breast implant surface Acta Biomater. 2017 49 260 271 10.1016/j.actbio.2016.11.052 27919840 · DOI
  88. [99]Loch-Wilkinson A. Beath K.J. Knight R.J.W. Wessels W.L.F. Magnusson M. Papadopoulos T. Connell T. Lofts J. Locke M. Hopper I. Breast Implant-Associated Anaplastic Large Cell Lymphoma in Australia and New Zealand: High-Surface-Area Textured Implants Are Associated with Increased Risk Plast. Reconstr. Surg. 2017 140 645 654 10.1097/PRS.0000000000003654 28481803 · DOI
  89. [100]Tevis S.E. Hunt K.K. Miranda R.N. Lange C. Pinnix C.C. Iyer S. Butler C.E. Clemens M.W. Breast Implant-Associated Anaplastic Large Cell Lymphoma: A Prospective Series of 52 Patients Ann. Surg. 2020 10.1097/SLA.0000000000004035 32568749 · DOI
  90. [101]Sforza M. Zaccheddu R. Alleruzzo A. Seno A. Mileto D. Paganelli A. Sulaiman H. Payne M. Maurovich-Horvat L. Preliminary 3-Year Evaluation of Experience with SilkSurface and VelvetSurface Motiva Silicone Breast Implants: A Single-Center Experience With 5813 Consecutive Breast Augmentation Cases Aesthetic Surg. J. 2018 38 S62 S73 10.1093/asj/sjx150 PMC5952962 29040364 · DOI
  91. [102]Wolf M.T. Dearth C.L. Ranallo C.A. LoPresti S.T. Carey L.E. Daly K.A. Brown B.N. Badylak S.F. Macrophage polarization in response to ECM coated polypropylene mesh Biomaterials 2014 35 6838 6849 10.1016/j.biomaterials.2014.04.115 24856104 PMC4347831 · DOI
  92. [103]Bracaglia L.G. Fisher J.P. Extracellular Matrix-Based Biohybrid Materials for Engineering Compliant, Matrix-Dense Tissues Adv. Heal. Mater. 2015 4 2475 2487 10.1002/adhm.201500236 PMC4715589 26227679 · DOI
  93. [104]Oakes R. Polei M.D. Skousen J.L. Tresco P.A. An astrocyte derived extracellular matrix coating reduces astrogliosis surrounding chronically implanted microelectrode arrays in rat cortex Biomaterials 2018 154 1 11 10.1016/j.biomaterials.2017.10.001 29117574 · DOI
  94. [105]Robotti F. Bottan S. Fraschetti F. Mallone A. Pellegrini G. Lindenblatt N. Starck C. Falk V. Poulikakos D. Ferrari A. A micron-scale surface topography design reducing cell adhesion to implanted materials Sci. Rep. 2018 8 10887 10.1038/s41598-018-29167-2 30022037 PMC6052105 · DOI
  95. [106]Klos A. Sedao X. Itina T.E. Helfenstein-Didier C. Donnet C. Peyroche S. Vico L. Guignandon A. Dumas V. Ultrafast Laser Processing of Nanostructured Patterns for the Control of Cell Adhesion and Migration on Titanium Alloy Nanomaterials 2020 10 864 10.3390/nano10050864 PMC7712038 32365835 · DOI
  96. [107]Padmanabhan J. Kinser E.R. Stalter M.A. Duncan-Lewis C. Balestrini J.L. Sawyer A.J. Schroers J. Kyriakides T.R. Engineering Cellular Response Using Nanopatterned Bulk Metallic Glass ACS Nano 2014 8 4366 4375 10.1021/nn501874q 24724817 PMC4046793 · DOI
  97. [108]Tan J.L. Tien J. Pirone D.M. Gray D.S. Bhadriraju K. Chen C.S. Cells lying on a bed of microneedles: An approach to isolate mechanical force Proc. Natl. Acad. Sci. USA 2003 100 1484 1489 10.1073/pnas.0235407100 12552122 PMC149857 · DOI
  98. [109]Chen L. Wang D. Peng F. Qiu J. Ouyang L. Qiao Y. Liu X. Nanostructural Surfaces with Different Elastic Moduli Regulate the Immune Response by Stretching Macrophages Nano Lett. 2019 19 3480 3489 10.1021/acs.nanolett.9b00237 31091110 · DOI
  99. [110]Achterberg V.F. Buscemi L. Diekmann H. Smith-Clerc J. Schwengler H. Meister J.-J. Wenck H. Gallinat S. Hinz B. The Nano-Scale Mechanical Properties of the Extracellular Matrix Regulate Dermal Fibroblast Function J. Investig. Dermatol. 2014 134 1862 1872 10.1038/jid.2014.90 24670384 · DOI
  100. [111]Christ A.F. Franze K. Gautier H.O.B. Moshayedi P. Fawcett J. Franklin R. Karadottir R.T. Guck J. Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy J. Biomech. 2010 43 2986 2992 10.1016/j.jbiomech.2010.07.002 20656292 · DOI
  101. [112]Butcher D.T. Alliston T. Weaver V.M. A tense situation: Forcing tumour progression Nat. Rev. Cancer 2009 9 108 122 10.1038/nrc2544 19165226 PMC2649117 · DOI
  102. [114]Majkut S.F. Discher D.E. Cardiomyocytes from late embryos and neonates do optimal work and striate best on substrates with tissue-level elasticity: Metrics and mathematics Biomech. Model. Mechanobiol. 2012 11 1219 1225 10.1007/s10237-012-0413-8 22752667 PMC3475743 · DOI
  103. [115]Ho S.P. Marshall S.J. Ryder M.I. Marshall G.W. The tooth attachment mechanism defined by structure, chemical composition and mechanical properties of collagen fibers in the periodontium Biomaterials 2007 28 5238 5245 10.1016/j.biomaterials.2007.08.031 17870156 PMC2423002 · DOI
  104. [116]Janmey P.A. Fletcher D.A. Reinhart-King C.A. Stiffness Sensing by Cells Physiol. Rev. 2020 100 695 724 10.1152/physrev.00013.2019 31751165 PMC7276923 · DOI
  105. [117]Discher D.E. Smith L. Cho S. Colasurdo M. Garcia A.J. Safran S. Matrix Mechanosensing: From Scaling Concepts in Omics Data to Mechanisms in the Nucleus, Regeneration, and Cancer Annu. Rev. Biophys. 2017 46 295 315 10.1146/annurev-biophys-062215-011206 28532215 PMC5444306 · DOI
  106. [118]Franze K. Janmey P.A. Guck J. Mechanics in Neuronal Development and Repair Annu. Rev. Biomed. Eng. 2013 15 227 251 10.1146/annurev-bioeng-071811-150045 23642242 · DOI
  107. [119]Cox T.R. Erler J.T. Remodeling and homeostasis of the extracellular matrix: Implications for fibrotic diseases and cancer Dis. Model. Mech. 2011 4 165 178 10.1242/dmm.004077 21324931 PMC3046088 · DOI · Paper page
  108. [120]Minev I.R. Musienko P. Hirsch A. Barraud Q. Wenger N. Moraud E.M. Gandar J. Capogrosso M. Milekovic T. Asboth L. Electronic dura mater for long-term multimodal neural interfaces Science 2015 347 159 163 10.1126/science.1260318 25574019 · DOI · Paper page
  109. [121]Moshayedi P. Ng G. Kwok J. Yeo G.S.H. Bryant C.E. Fawcett J. Franze K. Guck J. The relationship between glial cell mechanosensitivity and foreign body reactions in the central nervous system Biomaterials 2014 35 3919 3925 10.1016/j.biomaterials.2014.01.038 24529901 · DOI
  110. [122]Sindhu K. Bansode N. Rémy M. Morel C. Bareille R. Hagedorn M. Hinz B. Barthélémy P. Chassande O. Boiziau C. New injectable self-assembled hydrogels that promote angiogenesis through a bioactive degradation product Acta Biomater. 2020 115 197 209 10.1016/j.actbio.2020.08.012 32814142 · DOI
  111. [123]LeComte A. Descamps E. Bergaud C. A review on mechanical considerations for chronically-implanted neural probes J. Neural. Eng. 2018 15 031001 10.1088/1741-2552/aa8b4f 28885187 · DOI · Paper page
  112. [124]Du Z.J. Kolarcik C.L. Kozai T.D. Luebben S.D. Sapp S.A. Zheng X.S. Nabity J.A. Cui X.T. Ultrasoft microwire neural electrodes improve chronic tissue integration Acta Biomater. 2017 53 46 58 10.1016/j.actbio.2017.02.010 28185910 PMC5512864 · DOI
  113. [125]Doloff J. Veiseh O. Vegas A.J. Tam H.H. Farah S. Ma M. Li J. Bader A. Chiu A. Sadraei A. 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. 2017 16 671 680 10.1038/nmat4866 28319612 PMC5445003 · DOI · Paper page
  114. [126]Miron R.J. Bosshardt D.D. Multinucleated Giant Cells: Good Guys or Bad Guys? Tissue Eng. Part B Rev. 2018 24 53 65 10.1089/ten.teb.2017.0242 28825357 · DOI
  115. [127]Dondossola E. Holzapfel B.M. Alexander S. Filippini S. Hutmacher D.W. Friedl P. Examination of the foreign body response to biomaterials by nonlinear intravital microscopy Nat. Biomed. Eng. 2017 1 1 10 10.1038/s41551-016-0007 28979821 PMC5624536 · DOI · Paper page
  116. [128]Spiller K.L. Anfang R.R. Spiller K.J. Ng J. Nakazawa K.R. Daulton J. Vunjak-Novakovic G. The role of macrophage phenotype in vascularization of tissue engineering scaffolds Biomaterials 2014 35 4477 4488 10.1016/j.biomaterials.2014.02.012 24589361 PMC4000280 · DOI · Paper page
  117. [130]Chung L. Maestas D.R. Jr. Housseau F. Elisseeff J.H. Key players in the immune response to biomaterial scaffolds for regenerative medicine Adv. Drug Deliv. Rev. 2017 114 184 192 10.1016/j.addr.2017.07.006 28712923 · DOI
  118. [132]Mooney J.E. Rolfe B. Osborne G. Sester D.P. van Rooijen N. Campbell G.R. Hume D. Campbell J.H. Cellular Plasticity of Inflammatory Myeloid Cells in the Peritoneal Foreign Body Response Am. J. Pathol. 2010 176 369 380 10.2353/ajpath.2010.090545 20008135 PMC2797897 · DOI · Paper page
  119. [133]Smith T.D. Nagalla R.R. Chen E.Y. Liu W.F. Harnessing macrophage plasticity for tissue regeneration Adv. Drug Deliv. Rev. 2017 114 193 205 10.1016/j.addr.2017.04.012 28449872 · DOI
  120. [134]Martin K.E. García A.J. Macrophage phenotypes in tissue repair and the foreign body response: Implications for biomaterial-based regenerative medicine strategies Acta Biomater. 2021 10.1016/j.actbio.2021.03.038 33775905 PMC8464623 · DOI
  121. [135]Graney P. Lurier E.B. Spiller K.L. Biomaterials and Bioactive Factor Delivery Systems for the Control of Macrophage Activation in Regenerative Medicine ACS Biomater. Sci. Eng. 2017 4 1137 1148 10.1021/acsbiomaterials.6b00747 33418652 · DOI
  122. [136]Bonner J.C. Regulation of PDGF and its receptors in fibrotic diseases Cytokine Growth Factor Rev. 2004 15 255 273 10.1016/j.cytogfr.2004.03.006 15207816 · DOI · Paper page
  123. [138]McNally A.K. Anderson J.M. Phenotypic expression in human monocyte-derived interleukin-4-induced foreign body giant cells and macrophages in vitro: Dependence on material surface properties J. Biomed. Mater. Res. A 2015 103 1380 1390 10.1002/jbm.a.35280 25045023 PMC4297257 · DOI
  124. [139]Sheikh Z. Brooks P.J. Barzilay O. Fine N. Glogauer M. Macrophages, Foreign Body Giant Cells and Their Response to Implantable Biomaterials Materials 2015 8 5671 5701 10.3390/ma8095269 28793529 PMC5512621 · DOI · Paper page
  125. [140]Milde R. Ritter J. Tennent G.A. Loesch A. Martinez F.O. Gordon S. Pepys M.B. Verschoor A. Helming L. Multinucleated Giant Cells Are Specialized for Complement-Mediated Phagocytosis and Large Target Destruction Cell Rep. 2015 13 1937 1948 10.1016/j.celrep.2015.10.065 26628365 PMC4675895 · DOI
  126. [141]Aiyelabegan H.T. Sadroddiny E. Fundamentals of protein and cell interactions in biomaterials Biomed. Pharmacother. 2017 88 956 970 10.1016/j.biopha.2017.01.136 28178627 · DOI
  127. [142]Altieri D.C. Mannucci P.M. Capitanio A.M. Binding of fibrinogen to human monocytes J. Clin. Investig. 1986 78 968 976 10.1172/JCI112687 3760194 PMC423733 · DOI
  128. [143]Love R.J. Jones K.S. The recognition of biomaterials: Pattern recognition of medical polymers and their adsorbed biomolecules J. Biomed. Mater. Res. Part A 2013 101 2740 2752 10.1002/jbm.a.34577 23613455 · DOI
  129. [144]Lee T.T. Garcia J.R. Paez J.I. Singh A. Phelps E.A. Weis S. Shafiq Z. Shekaran A. Del Campo A. Garcia A. Light-triggered in vivo activation of adhesive peptides regulates cell adhesion, inflammation and vascularization of biomaterials Nat. Mater. 2015 14 352 360 10.1038/nmat4157 25502097 PMC4336636 · DOI
  130. [146]Sridharan R. Cavanagh B. Cameron A.R. Kelly D.J. O’Brien F.J. Material stiffness influences the polarization state, function and migration mode of macrophages Acta Biomater. 2019 89 47 59 10.1016/j.actbio.2019.02.048 30826478 · DOI · Paper page
  131. [148]Arya R.K. Goswami R. Rahaman S.O. Mechanotransduction via a TRPV4-Rac1 signaling axis plays a role in multinucleated giant cell formation J. Biol. Chem. 2021 296 100129 10.1074/jbc.RA120.014597 33262217 PMC7948992 · DOI
  132. [149]Boersema G.S. Grotenhuis N. Bayon Y. Lange J.F. Bastiaansen-Jenniskens Y.M. The Effect of Biomaterials Used for Tissue Regeneration Purposes on Polarization of Macrophages Biores. Open Access 2016 5 6 14 10.1089/biores.2015.0041 26862468 PMC4744891 · DOI
  133. [150]Abaricia J.O. Shah A.H. Chaubal M. Hotchkiss K.M. Olivares-Navarrete R. Wnt signaling modulates macrophage polarization and is regulated by biomaterial surface properties Biomaterials 2020 243 119920 10.1016/j.biomaterials.2020.119920 32179303 PMC7191325 · DOI
  134. [154]McWhorter F. Wang T. Nguyen P. Chung T. Liu W.F. Modulation of macrophage phenotype by cell shape Proc. Natl. Acad. Sci. USA 2013 110 17253 17258 10.1073/pnas.1308887110 24101477 PMC3808615 · DOI · Paper page
  135. [156]Moon H. Cremmel C.V.M. Kulpa A. Jaeger N.A.F. Kappelhoff R. Overall C.M. Waterfield J.D. Brunette D.M. Novel grooved substrata stimulate macrophage fusion, CCL2 and MMP-9 secretion J. Biomed. Mater. Res. Part A 2016 104 2243 2254 10.1002/jbm.a.35757 27102570 · DOI · Paper page
  136. [157]Shayan M. Padmanabhan J. Morris A.H. Cheung B. Smith R. Schroers J. Kyriakides T.R. Nanopatterned bulk metallic glass-based biomaterials modulate macrophage polarization Acta Biomater. 2018 75 427 438 10.1016/j.actbio.2018.05.051 29859902 PMC6119487 · DOI
  137. [158]Mohiuddin M. Pan H.-A. Hung Y.-C. Huang G.S. Control of growth and inflammatory response of macrophages and foam cells with nanotopography Nanoscale Res. Lett. 2012 7 394 10.1186/1556-276X-7-394 22799434 PMC3507756 · DOI
  138. [159]Padmanabhan J. Augelli M.J. Cheung B. Kinser E.R. Cleary B. Kumar P. Wang R. Sawyer A.J. Li R. Schwarz U. Regulation of cell-cell fusion by nanotopography Sci. Rep. 2016 6 33277 10.1038/srep33277 27615159 PMC5018837 · DOI
  139. [160]Previtera M.L. Sengupta A. Substrate Stiffness Regulates Proinflammatory Mediator Production through TLR4 Activity in Macrophages PLoS ONE 2015 10 e0145813 10.1371/journal.pone.0145813 26710072 PMC4692401 · DOI · Paper page
  140. [161]Irwin E.F. Saha K. Rosenbluth M. Gamble L.J. Castner D.G. Healy K.E. Modulus-dependent macrophage adhesion and behavior J. Biomater. Sci. Polym. Ed. 2008 19 1363 1382 10.1163/156856208786052407 18854128 · DOI · Paper page
  141. [162]Adlerz K.M. Aranda-Espinoza H. Hayenga H.N. Substrate elasticity regulates the behavior of human monocyte-derived macrophages Eur. Biophys. J. 2016 45 301 309 10.1007/s00249-015-1096-8 26613613 · DOI · Paper page
  142. [163]Féréol S. Fodil R. Labat B. Galiacy S. Laurent V.M. Louis B. Isabey D. Planus E. Sensitivity of alveolar macrophages to substrate mechanical and adhesive properties Cell Motil. Cytoskelet. 2006 63 321 340 10.1002/cm.20130 16634082 · DOI · Paper page
  143. [165]Patel N.R. Bole M. Chen C. Hardin C.C. Kho A.T. Mih J. Deng L. Butler J. Tschumperlin D. Fredberg J.J. Cell elasticity determines macrophage function PLoS ONE 2012 7 e41024 10.1371/journal.pone.0041024 23028423 PMC3445606 · DOI · Paper page
  144. [166]Fang J.Y. Yang Z. Han B. Switch of macrophage fusion competency by 3D matrices Sci. Rep. 2020 10 10348 10.1038/s41598-020-67056-9 32587271 PMC7316750 · DOI
  145. [167]Akilbekova D. Bratlie K.M. Quantitative Characterization of Collagen in the Fibrotic Capsule Surrounding Implanted Polymeric Microparticles through Second Harmonic Generation Imaging PLoS ONE 2015 10 e0130386 10.1371/journal.pone.0130386 26125551 PMC4488378 · DOI
  146. [168]Campbell J.H. Efendy J.L. Campbell G.R. Novel Vascular Graft Grown Within Recipient’s Own Peritoneal Cavity Circ. Res. 1999 85 1173 1178 10.1161/01.RES.85.12.1173 10590244 · DOI
  147. [169]Duffield J.S. Lupher M.L. Thannickal V.J. Wynn T.A. Host Responses in Tissue Repair and Fibrosis Annu. Rev. Pathol. Mech. Dis. 2013 8 241 276 10.1146/annurev-pathol-020712-163930 PMC3789589 23092186 · DOI
  148. [170]Schuppan D. Ashfaq-Khan M. Yang A.T. Kim Y.O. Liver fibrosis: Direct antifibrotic agents and targeted therapies Matrix Biol. 2018 68-69 435 451 10.1016/j.matbio.2018.04.006 29656147 · DOI
  149. [171]Fell S. Wang Z. Blanchard A. Nanthakumar C. Griffin M. Transglutaminase 2: A novel therapeutic target for idiopathic pulmonary fibrosis using selective small molecule inhibitors Amino Acids 2021 53 205 217 10.1007/s00726-020-02938-w 33474654 PMC7910249 · DOI
  150. [172]Hauser S. Wodtke R. Tondera C. Wodtke J. Neffe A.T. Hampe J. Lendlein A. Löser R. Pietzsch J. Characterization of Tissue Transglutaminase as a Potential Biomarker for Tissue Response toward Biomaterials ACS Biomater. Sci. Eng. 2018 5 5979 5989 10.1021/acsbiomaterials.9b01299 33405720 · DOI
  151. [173]Piersma B. Bank R.A. Collagen cross-linking mediated by lysyl hydroxylase 2: An enzymatic battlefield to combat fibrosis Essays Biochem. 2019 63 377 387 10.1042/ebc20180051 31324706 · DOI
  152. [174]Vallet S.D. Ricard-Blum S. Lysyl oxidases: From enzyme activity to extracellular matrix cross-links Essays Biochem. 2019 63 349 364 10.1042/EBC20180050 31488698 · DOI
  153. [175]Chen L. Li S. Li W. LOX/LOXL in pulmonary fibrosis: Potential therapeutic targets J. Drug Target. 2018 27 790 796 10.1080/1061186X.2018.1550649 30457362 · DOI
  154. [176]Tschumperlin D.J. Lagares D. Mechano-therapeutics: Targeting Mechanical Signaling in Fibrosis and Tumor Stroma Pharmacol. Ther. 2020 212 107575 10.1016/j.pharmthera.2020.107575 32437826 PMC7299835 · DOI
  155. [178]Klingberg F. Hinz B. White E.S. The myofibroblast matrix: Implications for tissue repair and fibrosis J. Pathol. 2013 229 298 309 10.1002/path.4104 22996908 PMC4005341 · DOI · Paper page
  156. [179]Neff L.S. Bradshaw A.D. Cross your heart? Collagen cross-links in cardiac health and disease Cell. Signal. 2021 79 109889 10.1016/j.cellsig.2020.109889 33347984 PMC8830414 · DOI
  157. [181]Hinz B. Celetta G. Tomasek J.J. Gabbiani G. Chaponnier C. Alpha-Smooth Muscle Actin Expression Upregulates Fibroblast Contractile Activity Mol. Biol. Cell 2001 12 2730 2741 10.1091/mbc.12.9.2730 11553712 PMC59708 · DOI · Paper page
  158. [182]Hinz B. Dugina V. Ballestrem C. Wehrle-Haller B. Chaponnier C. Alpha-smooth muscle actin Is crucial for focal adhesion maturation in myofibroblasts Mol. Biol. Cell. 2003 14 2508 2519 10.1091/mbc.e02-11-0729 12808047 PMC194898 · DOI · Paper page
  159. [183]Goffin J.M. Pittet P. Csucs G. Lussi J.W. Meister J.-J. Hinz B. Focal adhesion size controls tension-dependent recruitment of α-smooth muscle actin to stress fibers J. Cell Biol. 2006 172 259 268 10.1083/jcb.200506179 16401722 PMC2063555 · DOI
  160. [184]Godbout C. Castella L.F. Smith E.A. Talele N. Chow M.L. Garonna A. Hinz B. The Mechanical Environment Modulates Intracellular Calcium Oscillation Activities of Myofibroblasts PLoS ONE 2013 8 e64560 10.1371/journal.pone.0064560 23691248 PMC3653915 · DOI
  161. [185]Smithmyer M.E. Sawicki L.A. Kloxin A.M. Hydrogel scaffolds as in vitro models to study fibroblast activation in wound healing and disease Biomater. Sci. 2014 2 634 650 10.1039/C3BM60319A 25379176 PMC4217222 · DOI
  162. [186]Majd H. Scherer S.S. Boo S. Ramondetti S. Cambridge E. Raffoul W. Friedrich M. Pittet B. Pioletti D. Hinz B. Novel micropatterns mechanically control fibrotic reactions at the surface of silicone implants Biomaterials 2015 54 136 147 10.1016/j.biomaterials.2015.03.027 25907047 · DOI
  163. [187]Kyle D.J. Oikonomou A. Hill E. Bayat A. Development and functional evaluation of biomimetic silicone surfaces with hierarchical micro/nano-topographical features demonstrates favourable in vitro foreign body response of breast-derived fibroblasts Biomaterials 2015 52 88 102 10.1016/j.biomaterials.2015.02.003 25818416 · DOI
  164. [188]Rockey D.C. Bell P.D. Hill J.A. Fibrosis—A Common Pathway to Organ Injury and Failure N. Engl. J. Med. 2015 372 1138 1149 10.1056/NEJMra1300575 25785971 · DOI · Paper page
  165. [189]Fernández-Colino A. Iop L. Ferreira M.S.V. Mela P. Fibrosis in tissue engineering and regenerative medicine: Treat or trigger? Adv. Drug Deliv. Rev. 2019 146 17 36 10.1016/j.addr.2019.07.007 31295523 · DOI
  166. [190]Henderson N.C. Rieder F. Wynn T.A. Fibrosis: From mechanisms to medicines Nat. Cell Biol. 2020 587 555 566 10.1038/s41586-020-2938-9 PMC8034822 33239795 · DOI · Paper page
  167. [191]Wynn T.A. Ramalingam T.R. Mechanisms of fibrosis: Therapeutic translation for fibrotic disease Nat. Med. 2012 18 1028 1040 10.1038/nm.2807 22772564 PMC3405917 · DOI · Paper page
  168. [192]Love R.J. Jones K.S. Biomaterials, fibrosis, and the use of drug delivery systems in future antifibrotic strategies Crit. Rev. Biomed. Eng. 2009 37 259 281 10.1615/CritRevBiomedEng.v37.i3.20 20402622 · DOI
  169. [193]Gancedo M. Ruiz-Corro L. Salazar-Montes A. Rincón A.R. Armendáriz-Borunda J. Pirfenidone Prevents Capsular Contracture After Mammary Implantation Aesthetic Plast. Surg. 2008 32 32 40 10.1007/s00266-007-9051-4 17968613 · DOI
  170. [194]Henderson N.C. Arnold T.D. Katamura Y. Giacomini M.M. Rodriguez J.D. McCarty J.H. Targeting of alphav integrin identifies a core molecular pathway that regulates fibrosis in several organs Nat. Med. 2013 19 1617 1624 10.1038/nm.3282 24216753 PMC3855865 · DOI · Paper page
  171. [195]Rujitanaroj P.-O. Jao B. Yang R. Wang F. Anderson J.M. Wang J. Chew S.Y. Controlling fibrous capsule formation through long-term down-regulation of collagen type I (COL1A1) expression by nanofiber-mediated siRNA gene silencing Acta Biomater. 2013 9 4513 4524 10.1016/j.actbio.2012.09.029 23036951 PMC3523808 · DOI
  172. [196]Lodyga M. Hinz B. TGF-beta1—A truly transforming growth factor in fibrosis and immunity Semin. Cell Dev. Biol. 2020 101 123 139 10.1016/j.semcdb.2019.12.010 31879265 · DOI
  173. [197]Hinz B. Targeting the myofibroblast to improve wound healing. Volume I: “Therapies and regeneration“ Wound Healing Biomaterials Ågren M.S. Woodhead Publishing Limited Cambridge, UK Springer Science and Business Media Publishing Cambridge, UK 2016 69 100
  174. [198]Distler J.H.W. Gyorfi A.H. Ramanujam M. Whitfield M.L. Konigshoff M. Lafyatis R. Shared and distinct mechanisms of fibrosis Nat. Rev. Rheumatol. 2019 15 705 730 10.1038/s41584-019-0322-7 31712723 · DOI
  175. [200]Saika S. Kawashima Y. Miyamoto T. Okada Y. Ichitanakaa S.- Ohmi S. Minamide A. Yamanaka O. Ohnishi Y. Ooshima A. Immunolocalization of Prolyl 4-Hydroxylase Subunits, α-Smooth Muscle Actin, and Extracellular Matrix Components in Human Lens Capsules with Lens Implants Exp. Eye Res. 1998 66 283 294 10.1006/exer.1997.0434 9533856 · DOI
  176. [201]Zeplin P.H. Larena-Avellaneda A. Schmidt K. Surface Modification of Silicone Breast Implants by Binding the Antifibrotic Drug Halofuginone Reduces Capsular Fibrosis Plast. Reconstr. Surg. 2010 126 266 274 10.1097/PRS.0b013e3181dbc313 20595874 · DOI
  177. [202]Li A.G. Quinn M.J. Siddiqui Y. Wood M.D. Federiuk I.F. Duman H.M. Elevation of transforming growth factor beta (TGFbeta) and its downstream mediators in subcutaneous foreign body capsule tissue J. Biomed. Mater. Res. A 2007 82 498 508 10.1002/jbm.a.31168 17295253 · DOI
  178. [203]Avula M.N. Rao A.N. McGill L.D. Grainger D.W. Solzbacher F. Modulation of the foreign body response to implanted sensor models through device-based delivery of the tyrosine kinase inhibitor, masitinib Biomaterials 2013 34 9737 9746 10.1016/j.biomaterials.2013.08.090 24060424 · DOI
  179. [204]Ward W.K. Li A.G. Siddiqui Y. Federiuk I.F. Wang X.-J. Increased expression of Interleukin-13 and connective tissue growth factor, and their potential roles during foreign body encapsulation of subcutaneous implants J. Biomater. Sci. Polym. Ed. 2008 19 1065 1072 10.1163/156856208784909408 18644231 · DOI
  180. [205]Castro P. Marques S.M. Viana C.T. Campos P.P. Ferreira M.A. Barcelos L.S. Andrade S.P. Deletion of the chemokine receptor CCR2 attenuates foreign body reaction to implants in mice Microvasc. Res. 2014 95 37 45 10.1016/j.mvr.2014.07.002 25020267 · DOI
  181. [207]Liao Y. Ouyang L. Ci L. Chen B. Lv D. Li Q. Sun Y. Fei J. Bao S. Liu X. Pravastatin regulates host foreign-body reaction to polyetheretherketone implants via miR-29ab1-mediated SLIT3 upregulation Biomaterials 2019 203 12 22 10.1016/j.biomaterials.2019.02.027 30851489 · DOI
  182. [208]Klueh U. Dorsky D.I. Kreutzer D.L. Enhancement of implantable glucose sensor function in vivo using gene transfer-induced neovascularization Biomaterials 2005 26 1155 1163 10.1016/j.biomaterials.2004.04.017 15451635 · DOI · Paper page
  183. [209]Tschumperlin D.J. Ligresti G. Hilscher M.B. Shah V.H. Mechanosensing and fibrosis J. Clin. Investig. 2018 128 74 84 10.1172/JCI93561 29293092 PMC5749510 · DOI
  184. [210]Santos A. Lagares D. Matrix Stiffness: The Conductor of Organ Fibrosis Curr. Rheumatol. Rep. 2018 20 2 10.1007/s11926-018-0710-z 29349703 · DOI
  185. [211]Kuehlmann B. Bonham C.A. Zucal I. Prantl L. Gurtner G.C. Mechanotransduction in Wound Healing and Fibrosis J. Clin. Med. 2020 9 1423 10.3390/jcm9051423 32403382 PMC7290354 · DOI
  186. [212]Martinac B. The ion channels to cytoskeleton connection as potential mechanism of mechanosensitivity Biochim. Biophys. Acta (BBA) Biomembr. 2014 1838 682 691 10.1016/j.bbamem.2013.07.015 23886913 · DOI
  187. [213]Jo J. Nansa S.A. Kim D.-H. Molecular Regulators of Cellular Mechanoadaptation at Cell–Material Interfaces Front. Bioeng. Biotechnol. 2020 8 608569 10.3389/fbioe.2020.608569 33364232 PMC7753015 · DOI
  188. [214]Sun Z. Guo S.S. Fässler R. Integrin-mediated mechanotransduction J. Cell Biol. 2016 215 445 456 10.1083/jcb.201609037 27872252 PMC5119943 · DOI
  189. [215]Bachmann M. Kukkurainen S. Hytonen V.P. Wehrle-Haller B. Cell Adhesion by Integrins Physiol. Rev. 2019 99 1655 1699 10.1152/physrev.00036.2018 31313981 · DOI
  190. [216]Jansen K.A. Atherton P. Ballestrem C. Mechanotransduction at the cell-matrix interface Semin. Cell Dev. Biol. 2017 71 75 83 10.1016/j.semcdb.2017.07.027 28754442 · DOI
  191. [217]Revach O.-Y. Grosheva I. Geiger B. Biomechanical regulation of focal adhesion and invadopodia formation J. Cell Sci. 2020 133 10.1242/jcs.244848 33093229 · DOI
  192. [219]Hintermann E. Christen U. The Many Roles of Cell Adhesion Molecules in Hepatic Fibrosis Cells 2019 8 1503 10.3390/cells8121503 PMC6952767 31771248 · DOI
  193. [220]Schnittert J. Bansal R. Storm G. Prakash J. Integrins in wound healing, fibrosis and tumor stroma: High potential targets for therapeutics and drug delivery Adv. Drug Deliv. Rev. 2018 129 37 53 10.1016/j.addr.2018.01.020 29414674 · DOI
  194. [221]Schulz J.N. Plomann M. Sengle G. Gullberg D. Krieg T. Eckes B. New developments on skin fibrosis—Essential signals emanating from the extracellular matrix for the control of myofibroblasts Matrix Biol. 2018 68 522 532 10.1016/j.matbio.2018.01.025 29408278 · DOI
  195. [222]Maldonado H. Hagood J.S. Cooperative signaling between integrins and growth factor receptors in fibrosis J. Mol. Med. 2021 99 213 224 10.1007/s00109-020-02026-2 33392631 · DOI
  196. [223]Martino M. Briquez P.S. Güç E. Tortelli F. Kilarski W.W. Metzger S. Rice J.J. Kuhn G.A. Müller R. Swartz M.A. Growth Factors Engineered for Super-Affinity to the Extracellular Matrix Enhance Tissue Healing Science 2014 343 885 888 10.1126/science.1247663 24558160 · DOI
  197. [224]Wipff P.J. Hinz B. Integrins and the activation of latent transforming growth factor beta1—An intimate relationship Eur. J. Cell Biol. 2008 87 601 615 10.1016/j.ejcb.2008.01.012 18342983 · DOI
  198. [225]Hinz B. It has to be the alphav: Myofibroblast integrins activate latent TGF-beta1 Nat. Med. 2013 19 1567 1568 10.1038/nm.3421 24309651 · DOI
  199. [226]Wilson S.E. TGF beta -1, -2 and -3 in the modulation of fibrosis in the cornea and other organs Exp. Eye Res. 2021 207 108594 10.1016/j.exer.2021.108594 33894227 · DOI
  200. [228]Rifkin D.B. Rifkin W. Zilberberg L. LTBPs in biology and medicine: LTBP diseases Matrix Biol. 2018 71 90 99 10.1016/j.matbio.2017.11.014 29217273 PMC5988920 · DOI

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Sorted by citations

Authors
Noskovicova, N., Hinz, B., & Pakshir, P.
Affiliations
  • Laboratory of Tissue Repair and Regeneration, Faculty of Dentistry, University of Toronto, Toronto, ON M5G 1G6, Canada
  • University of Toronto (CA)
Corresponding author
  • Hinz, Boris
  • Pakshir, Pardis
ORCID
Venue
Cells
Publisher
MDPI AG
Published
2021-07-15
Volume
10
Issue
7
Pages
1794
ISSN
2073-4409 (ISSN-L)
DOI
10.3390/cells10071794
PMC
PMC8304203
OpenAlex
W3178890732
Cited by
184
References
37
Citations by year
2026: 42 · 2025: 49 · 2024: 40 · 2023: 32 · 2022: 19 · 2021: 2
FWCI
2.65
Type
journal article
Language
en
Open access
Licence
Locations
  • Cells (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • TSpace (University of Toronto) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Canadian Institutes of Health Research (375597)
  • Canada Foundation for Innovation (36050, 38861, 36349)
  • Ontario Research Foundation (36050, 38861, 36349)
  • Mathematics of Information Technology and Complex Systems (MITACS) (IT13587)
Topics
  • Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Health Sciences › Medicine › Surgery › Orthopaedic implants and arthroplasty
Keywords
foreign body reaction, myofibroblasts, biomedical implants, wound healing, macrophages, chronic inflammation, implant surface topography, mechanotransduction, scar tissue, device failure
MeSH terms
Fibroblasts, Foreign-Body Reaction, Humans, Macrophages, Prostheses and Implants, Mechanotransduction, Cellular, Myofibroblasts

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