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Cited by 97Bone Tissue Engineering MaterialsWound Healing and TreatmentsTissue Engineering and Regenerative Medicine

Promoting musculoskeletal system soft tissue regeneration by biomaterial-mediated modulation of macrophage polarization

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Ye, Jinchun, Xie, Chang, Wang, Canlong, Huang, Jiayun, Yin, Zi, Heng, Boon Chin, Chen, Xiao, Shen, Weiliang·2021·Bioactive Materials
DOI 10.1016/j.bioactmat.2021.04.017PMC PMC8091177
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Abstract

Musculoskeletal disorders are common in clinical practice. Repairing critical-sized defects in musculoskeletal systems remains a challenge for researchers and surgeons, requiring the application of tissue engineering biomaterials. Successful application depends on the response of the host tissue to the biomaterial and specific healing process of each anatomical structure. The commonly-held view is that biomaterials should be biocompatible to minimize local host immune response. However, a growing number of studies have shown that active modulation of the immune cells, particularly macrophages, via biomaterials is an effective way to control immune response and promote tissue regeneration as well as biomaterial integration. Therefore, we critically review the role of macrophages in the repair of injured musculoskeletal system soft tissues, which have relatively poor regenerative capacities, as well as discuss further enhancement of target tissue regeneration via modulation of macrophage polarization by biomaterial-mediated immunomodulation (biomaterial properties and delivery systems). This active regulation approach rather than passive-evade strategy maximizes the potential of biomaterials to promote musculoskeletal system soft tissue regeneration and provides alternative therapeutic options for repairing critical-sized defects.

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  • For the proper interaction between the scaffold and the immune system, pro-regenerative mechanisms must be in the majority.

    “For the proper interaction between the scaffold and the immune system, pro-regenerative mechanisms must be in the majority [208].”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [208]

    The Introduction and “Biomaterial-mediated modulation of macrophage polarization” section say that directing the immune response toward regeneration can improve scaffold outcomes, while adverse responses can impair them. The paper does not say pro-regenerative mechanisms must be in the majority; its muscle-regeneration section instead emphasizes appropriately timed sequential activation of M1 and M2 macrophages. Page numbers are unavailable in our copy. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • This phenomenon is dependent on the local tissue biochemical environment, which is formed by many cells, including T cells, and determines the range of fibrosis.

    “This phenomenon is dependent on the local tissue biochemical environment, which is formed by many cells, including T cells, and determines the range of fibrosis.”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [208]

    The Introduction says macrophage functions change with the microenvironment, and the tendon/ligament regeneration section links macrophage polarization to pathological fibrosis. The Future perspective also acknowledges roles for T cells and other immune cells, but says those roles are not well understood. Our copy does not establish that a biochemical environment formed by those cells determines the extent of fibrosis (page numbers unavailable). (LLM, conf=0.78)

    Experimental — accuracy not yet measured

  • However, this effect is undesirable for the regeneration of soft tissue.

    “However, this effect is undesirable for the regeneration of soft tissue [208].”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [208]

    The Introduction (page unavailable) says excessive inflammation and other adverse immune responses hinder musculoskeletal tissue regeneration. But the citing sentence does not identify what “this effect” refers to, so our copy cannot establish whether the source supports that specific effect being undesirable. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

  • According to the signal that macrophages receive, they are capable of polarization, or so-called phenotype adaptation.

    “According to the signal that macrophages receive, they are capable of polarization, or so-called phenotype adaptation [208].”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [208]

  • Foreign body giant cells play a crucial role in phenotype adaptation.

    “Foreign body giant cells play a crucial role in phenotype adaptation.”

    From Resorbable Biomaterials Used for 3D Scaffolds in Tissue Engineering: A Review (2023) · cites this paper as [208]

    The Introduction says unresolved inflammation can cause macrophages to fuse into giant cells, while the section on macrophage polarization describes macrophages changing phenotype. Neither passage says foreign body giant cells play a crucial role in phenotype adaptation. A search for giant cells, fusion, and phenotype polarization found no passage establishing that role; page numbers were not available in our copy. (LLM, conf=0.74)

    Experimental — accuracy not yet measured

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  1. [1]Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016 Lancet 390 10100 2017 1211 1259 28919117 PMC5605509
  2. [2]Shibuya N. Jupiter D.C. Bone graft substitute: allograft and xenograft Clin. Podiatr. Med. Surg. 32 1 2015 21 34 25440415
  3. [3]Briggs A.M. Woolf A.D. Dreinhöfer K. Reducing the global burden of musculoskeletal conditions Bull. World Health Organ. 96 5 2018 366 368 29875522 PMC5985424
  4. [7]Liu Q. Chiu A. Wang L.H. Zwitterionically modified alginates mitigate cellular overgrowth for cell encapsulation Nat. Commun. 10 1 2019 5262 31748525 PMC6868136
  5. [8]Julier Z. Park A.J. Briquez P.S. Martino M.M. Promoting tissue regeneration by modulating the immune system Acta Biomater. 53 2017 13 28 28119112
  6. [9]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. 114 2017 184 192 28712923
  7. [10]Mariani E. Lisignoli G. Borzì R.M. Pulsatelli L. Biomaterials: foreign bodies or tuners for the immune response Int. J. Mol. Sci. 20 3 2019 PMC6386828 30717232
  8. [11]Sadtler K. Estrellas K. Allen B.W. Developing a pro-regenerative biomaterial scaffold microenvironment requires T helper 2 cells Science 352 6283 2016 366 370 27081073 PMC4866509
  9. [13]Smith T.D. Nagalla R.R. Chen E.Y. Liu W.F. Harnessing macrophage plasticity for tissue regeneration Adv. Drug Deliv. Rev. 114 2017 193 205 28449872
  10. [14]Vishwakarma A. Bhise N.S. Evangelista M.B. Engineering immunomodulatory biomaterials to tune the inflammatory response Trends Biotechnol. 34 6 2016 470 482 27138899
  11. [15]Bianchi M.E. DAMPs, PAMPs and alarmins: all we need to know about danger J. Leukoc. Biol. 81 1 2007 1 5 17032697
  12. [16]Kono H. Onda A. Yanagida T. Molecular determinants of sterile inflammation Curr. Opin. Immunol. 26 2014 147 156 24556412
  13. [17]Adair-Kirk T.L. Senior R.M. Fragments of extracellular matrix as mediators of inflammation Int. J. Biochem. Cell Biol. 40 6–7 2008 1101 1110 18243041 PMC2478752
  14. [18]Ozinsky A. Underhill D.M. Fontenot J.D. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors Proc. Natl. Acad. Sci. U. S. A. 97 25 2000 13766 13771 11095740 PMC17650
  15. [19]Eming S.A. Wynn T.A. Martin P. Inflammation and metabolism in tissue repair and regeneration Science 356 6342 2017 1026 1030 28596335
  16. [20]Karin M. Clevers H. Reparative inflammation takes charge of tissue regeneration Nature 529 7586 2016 307 315 26791721 PMC5228603
  17. [23]Mosser D.M. Edwards J.P. Exploring the full spectrum of macrophage activation Nat. Rev. Immunol. 8 12 2008 958 969 19029990 PMC2724991
  18. [25]Martinez F.O. Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment F1000Prime Rep. 6 2014 13 24669294 PMC3944738
  19. [26]Ohmori Y. Hamilton T.A. IL-4-induced STAT6 suppresses IFN-gamma-stimulated STAT1-dependent transcription in mouse macrophages J. Immunol. 159 11 1997 5474 5482 9548487
  20. [27]Venkataraman C. Leung S. Salvekar A. Mano H. Schindler U. Repression of IL-4-induced gene expression by IFN-gamma requires Stat1 activation J. Immunol. 162 7 1999 4053 4061 10201928
  21. [28]Stöger J.L. Gijbels M.J. van der Velden S. Distribution of macrophage polarization markers in human atherosclerosis Atherosclerosis 225 2 2012 461 468 23078881
  22. [29]Davis M.J. Tsang T.M. Qiu Y. Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection mBio 4 3 2013 e00264-13 PMC3684832 23781069
  23. [30]Khallou-Laschet J. Varthaman A. Fornasa G. Macrophage plasticity in experimental atherosclerosis PloS One 5 1 2010 e8852 PMC2810335 20111605
  24. [31]Porcheray F. Viaud S. Rimaniol A.C. Macrophage activation switching: an asset for the resolution of inflammation Clin. Exp. Immunol. 142 3 2005 481 489 16297160 PMC1809537
  25. [32]Smith T.D. Tse M.J. Read E.L. Liu W.F. Regulation of macrophage polarization and plasticity by complex activation signals Integr. Biol. (Camb.) 8 9 2016 946 955 27492191 PMC5148158
  26. [33]Lu L.Y. Loi F. Nathan K. Pro-inflammatory M1 macrophages promote Osteogenesis by mesenchymal stem cells via the COX-2-prostaglandin E2 pathway J. Orthop. Res. 35 11 2017 2378 2385 28248001 PMC5581298
  27. [34]Loi F. Córdova L.A. Zhang R. The effects of immunomodulation by macrophage subsets on osteogenesis in vitro Stem Cell Res. Ther. 7 2016 15 26801095 PMC4724110
  28. [35]Spiller K.L. Nassiri S. Witherel C.E. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds Biomaterials 37 2015 194 207 25453950 PMC4312192
  29. [36]Bondeson J. Blom A.B. Wainwright S. Hughes C. Caterson B. van den Berg W.B. The role of synovial macrophages and macrophage-produced mediators in driving inflammatory and destructive responses in osteoarthritis Arthritis Rheum. 62 3 2010 647 657 20187160
  30. [37]Blom A.B. van Lent P.L. Holthuysen A.E. Synovial lining macrophages mediate osteophyte formation during experimental osteoarthritis Osteoarthritis Cartilage 12 8 2004 627 635 15262242
  31. [38]Culemann S. Grüneboom A. Nicolás-Ávila J.Á. Locally renewing resident synovial macrophages provide a protective barrier for the joint Nature 572 7771 2019 670 675 31391580 PMC6805223
  32. [39]Utomo L. Bastiaansen-Jenniskens Y.M. Verhaar J.A. van Osch G.J. Cartilage inflammation and degeneration is enhanced by pro-inflammatory (M1) macrophages in vitro, but not inhibited directly by anti-inflammatory (M2) macrophages Osteoarthritis Cartilage 24 12 2016 2162 2170 27502245
  33. [40]Zhang H. Lin C. Zeng C. Synovial macrophage M1 polarisation exacerbates experimental osteoarthritis partially through R-spondin-2 Ann. Rheum. Dis. 77 10 2018 1524 1534 29991473
  34. [41]Fahy N. de Vries-van Melle M.L. Lehmann J. Human osteoarthritic synovium impacts chondrogenic differentiation of mesenchymal stem cells via macrophage polarisation state Osteoarthritis Cartilage 22 8 2014 1167 1175 24911520
  35. [42]Dai M. Sui B. Xue Y. Liu X. Sun J. Cartilage repair in degenerative osteoarthritis mediated by squid type II collagen via immunomodulating activation of M2 macrophages, inhibiting apoptosis and hypertrophy of chondrocytes Biomaterials 180 2018 91 103 30031224
  36. [43]Kannus P. Structure of the tendon connective tissue Scand. J. Med. Sci. Sports 10 6 2000 312 320 11085557
  37. [44]Nichols A. Best K.T. Loiselle A.E. The cellular basis of fibrotic tendon healing: challenges and opportunities Transl. Res. 209 2019 156 168 30776336 PMC6545261
  38. [45]de la Durantaye M. Piette A.B. van Rooijen N. Frenette J. Macrophage depletion reduces cell proliferation and extracellular matrix accumulation but increases the ultimate tensile strength of injured Achilles tendons J. Orthop. Res. 32 2 2014 279 285 24307236
  39. [46]Chamberlain C.S. Leiferman E.M. Frisch K.E. The influence of macrophage depletion on ligament healing Connect. Tissue Res. 52 3 2011 203 211 21117894 PMC3110150
  40. [47]Sugg K.B. Lubardic J. Gumucio J.P. Mendias C.L. Changes in macrophage phenotype and induction of epithelial-to-mesenchymal transition genes following acute Achilles tenotomy and repair J. Orthop. Res. 32 7 2014 944 951 24700411 PMC4086481
  41. [48]Manning C.N. Havlioglu N. Knutsen E. The early inflammatory response after flexor tendon healing: a gene expression and histological analysis J. Orthop. Res. 32 5 2014 645 652 24464937 PMC4076155
  42. [49]Virchenko O. Skoglund B. Aspenberg P. Parecoxib impairs early tendon repair but improves later remodeling Am. J. Sports Med. 32 7 2004 1743 1747 15494342
  43. [50]Lin D. Alberton P. Caceres M.D. Volkmer E. Schieker M. Docheva D. Tenomodulin is essential for prevention of adipocyte accumulation and fibrovascular scar formation during early tendon healing Cell Death Dis. 8 10 2017 e3116 PMC5682675 29022912
  44. [51]Gibbons M.A. MacKinnon A.C. Ramachandran P. Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis Am. J. Respir. Crit. Care Med. 184 5 2011 569 581 21680953
  45. [52]Ackerman J.E. Geary M.B. Orner C.A. Bawany F. Loiselle A.E. Obesity/Type II diabetes alters macrophage polarization resulting in a fibrotic tendon healing response PloS One 12 7 2017 e0181127 PMC5501654 28686669
  46. [53]Chamberlain C.S. Clements A. Kink J.A. Extracellular vesicle-educated macrophages promote early achilles tendon healing Stem Cell. 37 5 2019 652 662 PMC6850358 30720911
  47. [54]Chargé S.B. Rudnicki M.A. Cellular and molecular regulation of muscle regeneration Physiol. Rev. 84 1 2004 209 238 14715915
  48. [55]Londhe P. Davie J.K. Interferon-γ resets muscle cell fate by stimulating the sequential recruitment of JARID2 and PRC2 to promoters to repress myogenesis Sci. Signal. 6 305 2013 ra107 24327761 PMC4000160
  49. [56]Tidball J.G. Regulation of muscle growth and regeneration by the immune system Nat. Rev. Immunol. 17 3 2017 165 178 28163303 PMC5452982
  50. [58]Palacios D. Mozzetta C. Consalvi S. TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration Cell Stem Cell 7 4 2010 455 469 20887952 PMC2951277
  51. [59]Tonkin J. Temmerman L. Sampson R.D. Monocyte/Macrophage-derived IGF-1 orchestrates murine skeletal muscle regeneration and modulates autocrine polarization Mol. Ther. 23 7 2015 1189 1200 25896247 PMC4817788
  52. [61]Tidball J.G. Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo J. Physiol. 578 Pt 1 2007 327 336 17038433 PMC2075127
  53. [63]Novak M.L. Weinheimer-Haus E.M. Koh T.J. Macrophage activation and skeletal muscle healing following traumatic injury J. Pathol. 232 3 2014 344 355 24255005 PMC4019602
  54. [64]Lemos D.R. Babaeijandaghi F. Low M. Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors Nat. Med. 21 7 2015 786 794 26053624
  55. [65]Roach P. Farrar D. Perry C.C. Surface tailoring for controlled protein adsorption: effect of topography at the nanometer scale and chemistry J. Am. Chem. Soc. 128 12 2006 3939 3945 16551101
  56. [66]Roach P. Farrar D. Perry C.C. Interpretation of protein adsorption: surface-induced conformational changes J. Am. Chem. Soc. 127 22 2005 8168 8173 15926845
  57. [67]Wilson C.J. Clegg R.E. Leavesley D.I. Pearcy M.J. Mediation of biomaterial-cell interactions by adsorbed proteins: a review Tissue Eng. 11 1–2 2005 1 18 15738657
  58. [69]Refai A.K. Textor M. Brunette D.M. Waterfield J.D. Effect of titanium surface topography on macrophage activation and secretion of proinflammatory cytokines and chemokines J. Biomed. Mater. Res. 70 2 2004 194 205 15227664
  59. [70]McWhorter F.Y. Wang T. Nguyen P. Chung T. Liu W.F. Modulation of macrophage phenotype by cell shape Proc. Natl. Acad. Sci. U. S. A. 110 43 2013 17253 17258 24101477 PMC3808615
  60. [71]Vassey M.J. Figueredo G.P. Scurr D.J. Immune modulation by design: using topography to control human monocyte attachment and macrophage differentiation Adv. Sci. 7 11 2020 1903392 PMC7284204 32537404
  61. [74]Hotchkiss K.M. Reddy G.B. Hyzy S.L. Schwartz Z. Boyan B.D. Olivares-Navarrete R. Titanium surface characteristics, including topography and wettability, alter macrophage activation Acta Biomater. 31 2016 425 434 26675126 PMC4728000
  62. [75]Lee C.H. Kim Y.J. Jang J.H. Park J.W. Modulating macrophage polarization with divalent cations in nanostructured titanium implant surfaces Nanotechnology 27 8 2016 085101 26807875
  63. [76]Sommerfeld S.D. Cherry C. Schwab R.M. Interleukin-36γ-producing macrophages drive IL-17-mediated fibrosis Sci. Immunol. 4 40 2019 PMC7549193 31604843
  64. [77]Beattie A.J. Gilbert T.W. Guyot J.P. Yates A.J. Badylak S.F. Chemoattraction of progenitor cells by remodeling extracellular matrix scaffolds Tissue Eng. 15 5 2009 1119 1125 PMC2789572 18837648
  65. [78]Mahon O.R. O'Hanlon S. Cunningham C.C. Orthopaedic implant materials drive M1 macrophage polarization in a spleen tyrosine kinase- and mitogen-activated protein kinase-dependent manner Acta Biomater. 65 2018 426 435 29104084
  66. [79]Mahon O.R. Browe D.C. Gonzalez-Fernandez T. Nano-particle mediated M2 macrophage polarization enhances bone formation and MSC osteogenesis in an IL-10 dependent manner Biomaterials 239 2020 119833 32062479
  67. [80]Miao X. Leng X. Zhang Q. The current state of nanoparticle-induced macrophage polarization and reprogramming research Int. J. Mol. Sci. 18 2 2017 PMC5343871 28178185
  68. [81]Yen H.J. Hsu S.H. Tsai C.L. Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes Small 5 13 2009 1553 1561 19326357
  69. [82]Troidl C. Jung G. Troidl K. The temporal and spatial distribution of macrophage subpopulations during arteriogenesis Curr. Vasc. Pharmacol. 11 1 2013 5 12 23391417
  70. [83]Yu T. Wang W. Nassiri S. Temporal and spatial distribution of macrophage phenotype markers in the foreign body response to glutaraldehyde-crosslinked gelatin hydrogels J. Biomater. Sci. Polym. Ed. 27 8 2016 721 742 26902292 PMC4879875
  71. [84]Chen J. Li M. Yang C. Macrophage phenotype switch by sequential action of immunomodulatory cytokines from hydrogel layers on titania nanotubes Colloids Surf. B Biointerfaces 163 2018 336 345 29331905
  72. [85]Li T. Peng M. Yang Z. 3D-printed IFN-γ-loading calcium silicate-β-tricalcium phosphate scaffold sequentially activates M1 and M2 polarization of macrophages to promote vascularization of tissue engineering bone Acta Biomater. 71 2018 96 107 29549051
  73. [86]O' Brien E.M. Risser G.E. Spiller K.L. Sequential drug delivery to modulate macrophage behavior and enhance implant integration Adv. Drug Deliv. Rev. 149–150 2019 85 94 PMC6858522 31103451
  74. [87]Yoon P. Keylock K.T. Hartman M.E. Freund G.G. Woods J.A. Macrophage hypo-responsiveness to interferon-gamma in aged mice is associated with impaired signaling through Jak-STAT Mech. Ageing Dev. 125 2 2004 137 143 15037019
  75. [88]Yih T.C. Al-Fandi M. Engineered nanoparticles as precise drug delivery systems J. Cell. Biochem. 97 6 2006 1184 1190 16440317
  76. [89]Zhou F. Mei J. Yang S. Modified ZIF-8 nanoparticles attenuate osteoarthritis by reprogramming the metabolic pathway of synovial macrophages ACS Appl. Mater. Interfaces 12 2 2020 2009 2022 31849213
  77. [90]Shields C.W. 4th Evans M.A. Wang L.L. Cellular backpacks for macrophage immunotherapy Sci. Adv. 6 18 2020 eaaz6579 PMC7190308 32494680
  78. [91]Lee J. Byun H. Madhurakkat Perikamana S.K. Lee S. Shin H. Current advances in immunomodulatory biomaterials for bone regeneration Adv. Healthc Mater. 8 4 2019 e1801106 30328293
  79. [92]Dai M. Liu X. Wang N. Sun J. Squid type II collagen as a novel biomaterial: isolation, characterization, immunogenicity and relieving effect on degenerative osteoarthritis via inhibiting STAT1 signaling in pro-inflammatory macrophages Mater. Sci. Eng. C Mater. Biol. Appl. 89 2018 283 294 29752100
  80. [93]Arlov Ø. Öztürk E. Steinwachs M. Skjåk-Bræk G. Zenobi-Wong M. Biomimetic sulphated alginate hydrogels suppress IL-1β-induced inflammatory responses in human chondrocytes Eur. Cell. Mater. 33 2017 76 89 28170076
  81. [94]Kerschenmeyer A. Arlov Ø. Malheiro V. Anti-oxidant and immune-modulatory properties of sulfated alginate derivatives on human chondrocytes and macrophages Biomater. Sci. 5 9 2017 1756 1765 28643827
  82. [95]Zantop T. Gilbert T.W. Yoder M.C. Badylak S.F. Extracellular matrix scaffolds are repopulated by bone marrow-derived cells in a mouse model of achilles tendon reconstruction J. Orthop. Res. 24 6 2006 1299 1309 16649228
  83. [96]Derwin K.A. Baker A.R. Spragg R.K. Leigh D.R. Iannotti J.P. Commercial extracellular matrix scaffolds for rotator cuff tendon repair. Biomechanical, biochemical, and cellular properties J. Bone Joint Surg. Am. 88 12 2006 2665 2672 17142417
  84. [97]Dearth C.L. Slivka P.F. Stewart S.A. Inhibition of COX1/2 alters the host response and reduces ECM scaffold mediated constructive tissue remodeling in a rodent model of skeletal muscle injury Acta Biomater. 31 2016 50 60 26612417 PMC4728713
  85. [98]Lin R. Deng C. Li X. Copper-incorporated bioactive glass-ceramics inducing anti-inflammatory phenotype and regeneration of cartilage/bone interface Theranostics 9 21 2019 6300 6313 31534552 PMC6735521
  86. [99]Wu C. Zhou Y. Xu M. Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity Biomaterials 34 2 2013 422 433 23083929
  87. [100]Wang C. Chen B. Wang W. Strontium released bi-lineage scaffolds with immunomodulatory properties induce a pro-regenerative environment for osteochondral regeneration Mater. Sci. Eng. C Mater. Biol. Appl. 103 2019 109833 31349499
  88. [101]Hu T. Xu H. Wang C. Qin H. An Z. Magnesium enhances the chondrogenic differentiation of mesenchymal stem cells by inhibiting activated macrophage-induced inflammation Sci. Rep. 8 1 2018 3406 29467509 PMC5821731
  89. [102]Schoenenberger A.D. Foolen J. Moor P. Silvan U. Snedeker J.G. Substrate fiber alignment mediates tendon cell response to inflammatory signaling Acta Biomater. 71 2018 306 317 29530822
  90. [103]Patel K.H. Dunn A.J. Talovic M. Aligned nanofibers of decellularized muscle ECM support myogenic activity in primary satellite cells in vitro Biomed. Mater. 14 3 2019 035010 30812025
  91. [104]Patel K.H. Talovic M. Dunn A.J. Aligned nanofibers of decellularized muscle extracellular matrix for volumetric muscle loss J. Biomed. Mater. Res. B Appl. Biomater. 108 6 2020 2528 2537 10.1002/jbm.b.34584 32052931 · DOI
  92. [105]Schoenenberger A.D. Tempfer H. Lehner C. Macromechanics and polycaprolactone fiber organization drive macrophage polarization and regulate inflammatory activation of tendon in vitro and in vivo Biomaterials 249 2020 120034 32315865
  93. [106]El Khatib M. Mauro A. Di Mattia M. Electrospun PLGA fiber diameter and alignment of tendon biomimetic fleece potentiate tenogenic differentiation and immunomodulatory function of amniotic epithelial stem cells Cells 9 5 2020 PMC7290802 32413998
  94. [107]Ji X. Lei Z. Yuan M. Cartilage repair mediated by thermosensitive photocrosslinkable TGFβ1-loaded GM-HPCH via immunomodulating macrophages, recruiting MSCs and promoting chondrogenesis Theranostics 10 6 2020 2872 2887 32194841 PMC7052899
  95. [108]Raimondo T.M. Mooney D.J. Functional muscle recovery with nanoparticle-directed M2 macrophage polarization in mice Proc. Natl. Acad. Sci. U. S. A. 115 42 2018 10648 10653 30275293 PMC6196479
  96. [109]Estrellas K.M. Chung L. Cheu L.A. Biological scaffold-mediated delivery of myostatin inhibitor promotes a regenerative immune response in an animal model of Duchenne muscular dystrophy J. Biol. Chem. 293 40 2018 15594 15605 30139748 PMC6177591
  97. [110]Jain S. Tran T.H. Amiji M. Macrophage repolarization with targeted alginate nanoparticles containing IL-10 plasmid DNA for the treatment of experimental arthritis Biomaterials 61 2015 162 177 26004232 PMC4464978
  98. [111]Howard K.A. Paludan S.R. Behlke M.A. Besenbacher F. Deleuran B. Kjems J. Chitosan/siRNA nanoparticle-mediated TNF-alpha knockdown in peritoneal macrophages for anti-inflammatory treatment in a murine arthritis model Mol. Ther. 17 1 2009 162 168 18827803 PMC2834976
  99. [112]Kim J. Kim H.Y. Song S.Y. Synergistic oxygen generation and reactive oxygen species scavenging by manganese ferrite/ceria Co-decorated nanoparticles for rheumatoid arthritis treatment ACS Nano 13 3 2019 3206 3217 30830763
  100. [113]Manferdini C. Paolella F. Gabusi E. From osteoarthritic synovium to synovial-derived cells characterization: synovial macrophages are key effector cells Arthritis Res. Ther. 18 2016 83 27044395 PMC4820904
  101. [114]Wu C.L. Harasymowicz N.S. Klimak M.A. Collins K.H. Guilak F. The role of macrophages in osteoarthritis and cartilage repair Osteoarthritis Cartilage 28 5 2020 544 554 31926267 PMC7214213
  102. [115]Dai M. Sui B. Hua Y. A well defect-suitable and high-strength biomimetic squid type II gelatin hydrogel promoted in situ costal cartilage regeneration via dynamic immunomodulation and direct induction manners Biomaterials 240 2020 119841 32088411
  103. [116]Park K.S. Kim B.J. Lih E. Versatile effects of magnesium hydroxide nanoparticles in PLGA scaffold-mediated chondrogenesis Acta Biomater. 73 2018 204 216 29673840
  104. [117]Harrell C.R. Markovic B.S. Fellabaum C. Arsenijevic A. Volarevic V. Mesenchymal stem cell-based therapy of osteoarthritis: current knowledge and future perspectives Biomed. Pharmacother. 109 2019 2318 2326 30551490
  105. [118]Hamilton A.M. Cheung W.Y. Gómez-Aristizábal A. Iron nanoparticle-labeled murine mesenchymal stromal cells in an osteoarthritic model persists and suggests anti-inflammatory mechanism of action PloS One 14 12 2019 e0214107 PMC6890235 31794570
  106. [119]Patel J.M. Saleh K.S. Burdick J.A. Mauck R.L. Bioactive factors for cartilage repair and regeneration: improving delivery, retention, and activity Acta Biomater. 93 2019 222 238 30711660 PMC6616001
  107. [120]van Roon J.A. van Roy J.L. Gmelig-Meyling F.H. Lafeber F.P. Bijlsma J.W. Prevention and reversal of cartilage degradation in rheumatoid arthritis by interleukin-10 and interleukin-4 Arthritis Rheum. 39 5 1996 829 835 8639180
  108. [121]Joosten L.A. Lubberts E. Helsen M.M. Protection against cartilage and bone destruction by systemic interleukin-4 treatment in established murine type II collagen-induced arthritis Arthritis Res. 1 1 1999 81 91 11056663 PMC17779
  109. [122]Blagih J. Jones R.G. Polarizing macrophages through reprogramming of glucose metabolism Cell Metabol. 15 6 2012 793 795 22682218
  110. [123]Fearon U. Canavan M. Biniecka M. Veale D.J. Hypoxia, mitochondrial dysfunction and synovial invasiveness in rheumatoid arthritis Nat. Rev. Rheumatol. 12 7 2016 385 397 27225300
  111. [124]Patel M.P. Patel R.R. Patel J.K. Chitosan mediated targeted drug delivery system: a review J. Pharm. Pharmaceut. Sci. 13 4 2010 536 557 21486530
  112. [125]Chen X. Zhu X. Ma L. A core-shell structure QRu-PLGA-RES-DS NP nanocomposite with photothermal response-induced M2 macrophage polarization for rheumatoid arthritis therapy Nanoscale 11 39 2019 18209 18223 31560010
  113. [126]Ragelle H. Vandermeulen G. Préat V. Chitosan-based siRNA delivery systems J. Contr. Release 172 1 2013 207 218 23965281
  114. [127]Brennan D.A. Conte A.A. Kanski G. Mechanical considerations for electrospun nanofibers in tendon and ligament repair Adv. Healthc Mater. 7 12 2018 e1701277 29603679
  115. [128]Narayanan G. Vernekar V.N. Kuyinu E.L. Laurencin C.T. Poly (lactic acid)-based biomaterials for orthopaedic regenerative engineering Adv. Drug Deliv. Rev. 107 2016 247 276 27125191 PMC5482531
  116. [129]Dziki J.L. Wang D.S. Pineda C. Sicari B.M. Rausch T. Badylak S.F. Solubilized extracellular matrix bioscaffolds derived from diverse source tissues differentially influence macrophage phenotype J. Biomed. Mater. Res. 105 1 2017 138 147 27601305
  117. [130]Valentin J.E. Badylak J.S. McCabe G.P. Badylak S.F. Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study J. Bone Joint Surg. Am. 88 12 2006 2673 2686 17142418
  118. [131]Lee N.M. Erisken C. Iskratsch T. Sheetz M. Levine W.N. Lu H.H. Polymer fiber-based models of connective tissue repair and healing Biomaterials 112 2017 303 312 27770633 PMC5121020
  119. [132]Lin J. Zhou W. Han S. Cell-material interactions in tendon tissue engineering Acta Biomater. 70 2018 1 11 29355716
  120. [133]Fotticchia A. Musson D. Lenardi C. Demirci E. Liu Y. Anisotropic cytocompatible electrospun scaffold for tendon tissue engineering elicits limited inflammatory response in vitro J. Biomater. Appl. 33 1 2018 127 139 29987990
  121. [134]Labow R.S. Meek E. Santerre J.P. Model systems to assess the destructive potential of human neutrophils and monocyte-derived macrophages during the acute and chronic phases of inflammation J. Biomed. Mater. Res. 54 2 2001 189 197 11093178
  122. [135]Wissing T.B. Bonito V. van Haaften E.E. Macrophage-driven biomaterial degradation depends on scaffold microarchitecture Front. Bioeng. Biotechnol. 7 2019 87 31080796 PMC6497794
  123. [136]Sicari B.M. Agrawal V. Siu B.F. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement Tissue Eng. 18 19–20 2012 1941 1948 PMC3463275 22906411
  124. [137]Turner N.J. Yates A.J. Jr. Weber D.J. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction Tissue Eng. 16 11 2010 3309 3317 20528669
  125. [138]Wolf M.T. Dearth C.L. Sonnenberg S.B. Loboa E.G. Badylak S.F. Naturally derived and synthetic scaffolds for skeletal muscle reconstruction Adv. Drug Deliv. Rev. 84 2015 208 221 25174309 PMC5942587
  126. [139]Hong Y. Huber A. Takanari K. Mechanical properties and in vivo behavior of a biodegradable synthetic polymer microfiber-extracellular matrix hydrogel biohybrid scaffold Biomaterials 32 13 2011 3387 3394 21303718 PMC3184831
  127. [141]Sicari B.M. Rubin J.P. Dearth C.L. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss Sci. Transl. Med. 6 234 2014 234ra58 PMC5942588 24786326
  128. [142]Aurora A. Roe J.L. Corona B.T. Walters T.J. An acellular biologic scaffold does not regenerate appreciable de novo muscle tissue in rat models of volumetric muscle loss injury Biomaterials 67 2015 393 407 26256250
  129. [143]Garg K. Ward C.L. Rathbone C.R. Corona B.T. Transplantation of devitalized muscle scaffolds is insufficient for appreciable de novo muscle fiber regeneration after volumetric muscle loss injury Cell Tissue Res. 358 3 2014 857 873 25300647
  130. [144]Corona B.T. Wu X. Ward C.L. McDaniel J.S. Rathbone C.R. Walters T.J. The promotion of a functional fibrosis in skeletal muscle with volumetric muscle loss injury following the transplantation of muscle-ECM Biomaterials 34 13 2013 3324 3335 23384793
  131. [145]Badylak S.F. Dziki J.L. Sicari B.M. Ambrosio F. Boninger M.L. Mechanisms by which acellular biologic scaffolds promote functional skeletal muscle restoration Biomaterials 103 2016 128 136 27376561
  132. [146]Garg K. Ward C.L. Corona B.T. Asynchronous inflammation and myogenic cell migration limit muscle tissue regeneration mediated by a cellular scaffolds Inflamm. Cell Signal 1 4 2014 PMC4776328 26949720
  133. [147]Choi J.S. Lee S.J. Christ G.J. Atala A. Yoo J.J. The influence of electrospun aligned poly(epsilon-caprolactone)/collagen nanofiber meshes on the formation of self-aligned skeletal muscle myotubes Biomaterials 29 19 2008 2899 2906 18400295
  134. [148]Aviss K.J. Gough J.E. Downes S. Aligned electrospun polymer fibres for skeletal muscle regeneration Eur. Cell. Mater. 19 2010 193 204 20467965
  135. [149]Neumann T. Hauschka S.D. Sanders J.E. Tissue engineering of skeletal muscle using polymer fiber arrays Tissue Eng. 9 5 2003 995 1003 14633383
  136. [150]Horsley V. Jansen K.M. Mills S.T. Pavlath G.K. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth Cell 113 4 2003 483 494 12757709
  137. [151]Jenkins S.J. Ruckerl D. Cook P.C. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation Science 332 6035 2011 1284 1288 21566158 PMC3128495
  138. [152]Choi W. Lee J. Lee J. Lee S.H. Kim S. Hepatocyte growth factor regulates macrophage transition to the M2 phenotype and promotes murine skeletal muscle regeneration Front. Physiol. 10 2019 914 31404148 PMC6672745
  139. [153]Nie M. Liu J. Yang Q. MicroRNA-155 facilitates skeletal muscle regeneration by balancing pro- and anti-inflammatory macrophages Cell Death Dis. 7 6 2016 e2261 PMC5143393 27277683

Cited by

Sorted by citations

Authors
Ye, J., Xie, C., Wang, C., Huang, J., Yin, Z., Heng, B. C., Chen, X., & Shen, W.
Affiliations
  • Second Affiliated Hospital of Zhejiang University (CN)
  • Zhejiang University (CN)
  • Peking University (CN)
Corresponding author
  • Chen, Xiao
  • Shen, Weiliang
ORCID
Venue
Bioactive Materials
Publisher
Elsevier BV
Published
2021-11
Volume
6
Issue
11
Pages
4096-4109
ISSN
  • 2097-1192 (ISSN-L)
  • 2452-199X
DOI
10.1016/j.bioactmat.2021.04.017
PMC
PMC8091177
OpenAlex
W3157261962
Cited by
97
References
14
Citations by year
2026: 12 · 2025: 21 · 2024: 27 · 2023: 18 · 2022: 13 · 2021: 6
FWCI
1.35
Type
journal article
Language
en
Open access
Licence
Locations
  • Bioactive Materials (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (81572115, 81572157, 81874019)
  • Zhejiang University
  • National Key Research and Development Program of China (2017YFA0104900)
  • Fundamental Research Funds for the Central Universities
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
  • Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
Keywords
macrophage polarization, critical-size bone defect, biomaterial integration, host immune response, tissue engineering biomaterials, wound healing

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