CoChat
Sign Up
Cited by 21Bone Tissue Engineering MaterialsTissue Engineering and Regenerative MedicineWound Healing and Treatments

Adaptive immunity of materials: Implications for tissue healing and regeneration

Open access
Lee, Jung-Hwan, Shin, Seong-Jin, Lee, Jun Hee, Knowles, Jonathan C., Lee, Hae-Hyoung, Kim, Hae-Won·2024·Bioactive Materials
DOI 10.1016/j.bioactmat.2024.07.027PMC PMC11350271
Open this paper in CoChat — free account

Abstract

outcomes. Our discussion will help understand the materials-regulated immunology events more deeply, and offer the design rationale of materials with tunable matrix properties for accelerated tissue repair and regeneration.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.bioactmat.2024.07.027

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • ECM-bioscaffold degradation products function as DAMPs that ligate pattern-recognition and scavenger receptors on dendritic cells and macrophages; in some contexts they also signal via integrins.

    “ECM-bioscaffold degradation products function as damage-associated molecular patterns (DAMPs) that ligate pattern-recognition and scavenger receptors on dendritic cells and macrophages; in some contexts, they also signal via integrins [2,26,28,29].”

    From Immune Response to Extracellular Matrix Bioscaffolds: A Comprehensive Review (2025) · cites this paper as [26]

    In “Degradable biomaterials and the actions of antigen presenting cells” (page unavailable), the review says some degradation products can be DAMPs and discusses their recognition by immune cells, including macrophages and dendritic cells. It treats direct engagement of specific pattern-recognition receptors as an open question; the passages do not establish ligation of scavenger receptors or integrin signaling by ECM-bioscaffold degradation products. Its integrin discussion concerns T-cell interactions with ECM ligands, not those degradation products. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Evidence indicates that degradation products from ECM bioscaffolds condition antigen presentation and favor regulatory T lymphocyte induction and B lymphocyte tolerance, sustaining a pro-resolution set point that supports scaffold integration.

    “Collectively, the evidence indicates that degradation products from ECMbioscaffolds condition antigen presentation and favor regulatory T lymphocyte induction and B lymphocyte tolerance, sustaining a pro-resolution set point that supports scaffold integration [2,26,34].”

    From Immune Response to Extracellular Matrix Bioscaffolds: A Comprehensive Review (2025) · cites this paper as [26]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 149 · Cited by 21

Research works printed but not linked: 133

  1. [1]Van Parijs L. Abbas A.K. Homeostasis and self-tolerance in the immune system: turning lymphocytes off Science 280 5361 1998 243 248 9535647
  2. [2]Amit I. Winter D.R. Jung S. The role of the local environment and epigenetics in shaping macrophage identity and their effect on tissue homeostasis Nat. Immunol. 17 1 2016 18 25 26681458
  3. [5]Chen G.Y. Nunez G. Sterile inflammation: sensing and reacting to damage Nat. Rev. Immunol. 10 12 2010 826 837 21088683 PMC3114424
  4. [6]Sridharan R. Cameron A.R. Kelly D.J. Kearney C.J. O'Brien F.J. Biomaterial based modulation of macrophage polarization: a review and suggested design principles Mater. Today 18 6 2015 313 325
  5. [7]Hoebe K. Janssen E. Beutler B. The interface between innate and adaptive immunity Nat. Immunol. 5 10 2004 971 974 15454919
  6. [8]Sonnenberg G.F. Hepworth M.R. Functional interactions between innate lymphoid cells and adaptive immunity Nat. Rev. Immunol. 19 10 2019 599 613 31350531 PMC6982279
  7. [9]Du H. Bartleson J.M. Butenko S. Alonso V. Liu W.F. Winer D.A. Butte M.J. Tuning immunity through tissue mechanotransduction Nat. Rev. Immunol. 23 3 2023 174 188 35974148 PMC9379893
  8. [10]Lam N. Lee Y. Farber D.L. A guide to adaptive immune memory Nat. Rev. Immunol. 2024 1 20 38831162
  9. [13]Li W. Zhou P. Yan B. Qi M. Chen Y. Shang L. Guan J. Zhang L. Mao Y. Disc regeneration by injectable fucoidan-methacrylated dextran hydrogels through mechanical transduction and macrophage immunomodulation J. Tissue Eng. 14 2023 20417314231180050 PMC10328174 37427012
  10. [14]Xia Y. Yang R. Wang H. Hou Y. Li Y. Zhu J. Xu F. Fu C. Biomaterials delivery strategies to repair spinal cord injury by modulating macrophage phenotypes J. Tissue Eng. 13 2022 20417314221143059 PMC9806413 36600997
  11. [15]J.-E. Park, D.-H. Kim, Advanced immunomodulatory biomaterials for therapeutic applications, Adv. Healthcare Mater. n/a(n/a) 2304496. PMC11834384 38716543
  12. [17]Namangkalakul W. Nagai S. Jin C. Nakahama K.-i. Yoshimoto Y. Ueha S. Akiyoshi K. Matsushima K. Nakashima T. Takechi M. Iseki S. Augmented effect of fibroblast growth factor 18 in bone morphogenetic protein 2-induced calvarial bone healing by activation of CCL2/CCR2 axis on M2 macrophage polarization J. Tissue Eng. 14 2023 20417314231187960 PMC10387695 37529250
  13. [18]Li W. Zhou P. Yan B. Qi M. Chen Y. Shang L. Guan J. Zhang L. Mao Y. Disc regeneration by injectable fucoidan-methacrylated dextran hydrogels through mechanical transduction and macrophage immunomodulation J. Tissue Eng. 14 2023 20417314231180050 PMC10328174 37427012
  14. [19]Zhou S. Xie M. Su J. Cai B. Li J. Zhang K. New insights into balancing wound healing and scarless skin repair J. Tissue Eng. 14 2023 20417314231185848 PMC10388637 37529248
  15. [20]Gould S.J. Foey A.D. Salih V.M. An organotypic oral mucosal infection model to study host-pathogen interactions J. Tissue Eng. 14 2023 20417314231197310 PMC10590543 37873034
  16. [23]Kazzaz N.M. Sule G. Knight J.S. Intercellular interactions as regulators of NETosis Front. Immunol. 7 2016 PMC5107827 27895638
  17. [24]Vanden Berghe T. Linkermann A. Jouan-Lanhouet S. Walczak H. Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways Nat. Rev. Mol. Cell Biol. 15 2 2014 134 146 24452471
  18. [25]Abaricia J.O. Shah A.H. Olivares-Navarrete R. Substrate stiffness induces neutrophil extracellular trap (NET) formation through focal adhesion kinase activation Biomaterials 271 2021 120715 PMC8044006 33677375
  19. [26]Abaricia J.O. Shah A.H. Musselman R.M. Olivares-Navarrete R. Hydrophilic titanium surfaces reduce neutrophil inflammatory response and NETosis Biomater. Sci. 8 8 2020 2289 2299 32163073
  20. [27]Elangovan G. Mello-Neto J.M. Tadakamadla S.K. Reher P. Figueredo C.M.S. A systematic review on neutrophils interactions with titanium and zirconia surfaces: evidence from in vitro studies Clin Exp Dent Res 8 4 2022 950 958 35535662 PMC9382042
  21. [29]Durant F. Whited J.L. Finding solutions for fibrosis: understanding the innate mechanisms used by super-regenerator vertebrates to combat scarring Adv. Sci. 8 15 2021 e2100407 PMC8336523 34032013
  22. [30]Reichardt P. Dornbach B. Rong S. Beissert S. Gueler F. Loser K. Gunzer M. Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse Blood 110 5 2007 1519 1529 17392507
  23. [31]Moore E.M. Maestas D.R. Jr. Cherry C.C. Garcia J.A. Comeau H.Y. Davenport Huyer L. Kelly S.H. Pena A.N. Blosser R.L. Rosson G.D. Elisseeff J.H. Biomaterials direct functional B cell response in a material-specific manner Sci. Adv. 7 49 2021 eabj5830 PMC8635437 34851674
  24. [33]Liu Y. Suarez-Arnedo A. Shetty S. Wu Y. Schneider M. Collier J.H. Segura T. A balance between pro-inflammatory and pro-reparative macrophages is observed in regenerative D-MAPS Adv. Sci. 10 11 2023 e2204882 PMC10104668 36762570
  25. [34]Tu Z.X. Zhong Y.L. Hu H.Z. Shao D. Haag R.N. Schirner M. Lee J. Sullenger B. Leong K.W. Design of therapeutic biomaterials to control inflammation Nat. Rev. Mater. 7 7 2022 557 574 35251702 PMC8884103
  26. [35]Lanzavecchia A. Sallusto F. The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics Curr. Opin. Immunol. 13 3 2001 291 298 11406360
  27. [36]Rodriguez A. Voskerician G. Meyerson H. MacEwan S.R. Anderson J.M. T cell subset distributions following primary and secondary implantation at subcutaneous biomaterial implant sites J. Biomed. Mater. Res. 85 2 2008 556 565 17729264
  28. [37]Hady T.F. Hwang B. Pusic A.D. Waworuntu R.L. Mulligan M. Ratner B. Bryers J.D. Uniform 40-microm-pore diameter precision templated scaffolds promote a pro-healing host response by extracellular vesicle immune communication J Tissue Eng Regen Med 15 1 2021 24 36 33217150 PMC7954460
  29. [38]Lam A.J. MacDonald K.N. Pesenacker A.M. Juvet S.C. Morishita K.A. Bressler B. iGenoMed C. Pan J.G. Sidhu S.S. Rioux J.D. Levings M.K. Innate control of tissue-reparative human regulatory T cells J. Immunol. 202 8 2019 2195 2209 30850479
  30. [39]Panduro M. Benoist C. Mathis D. T(reg) cells limit IFN-gamma production to control macrophage accrual and phenotype during skeletal muscle regeneration Proc. Natl. Acad. Sci. U. S. A. 115 11 2018 E2585 E2593 29476012 PMC5856564
  31. [40]Li Y. Frei A.W. Yang E.Y. Labrada-Miravet I. Sun C. Rong Y. Samojlik M.M. Bayer A.L. Stabler C.L. In vitro platform establishes antigen-specific CD8(+) T cell cytotoxicity to encapsulated cells via indirect antigen recognition Biomaterials 256 2020 120182 PMC7480933 32599358
  32. [41]Boehler R.M. Graham J.G. Shea L.D. Tissue engineering tools for modulation of the immune response Biotechniques 51 4 2011 239 240 242, 244 passim 21988690 PMC3526814
  33. [43]Lee J.-H. El-Fiqi A. Mandakhbayar N. Lee H.-H. Kim H.-W. Drug/ion co-delivery multi-functional nanocarrier to regenerate infected tissue defect Biomaterials 142 2017 62 76 28727999
  34. [44]Mandakhbayar N. Ji Y. El-Fiqi A. Patel K.D. Yoon D.S. Dashnyam K. Bayaraa O. Jin G. Tsogtbaatar K. Kim T.-H. Lee J.-H. Kim H.-W. Double hits with bioactive nanozyme based on cobalt-doped nanoglass for acute and diabetic wound therapies through anti-inflammatory and pro-angiogenic functions Bioact. Mater. 31 2024 298 311 37637079 PMC10458956
  35. [45]C.J. Li, J.-H. Park, G.S. Jin, N. Mandakhbayar, D. Yeo, J.H. Lee, J.-H. Lee, H.S. Kim, H.-W. Kim, Strontium/silicon/calcium-releasing hierarchically structured 3D-printed scaffolds accelerate osteochondral defect repair, Adv. Healthcare Mater. n/a(n/a) 2400154. 38647029
  36. [46]Kitabayashi C. Fukada T. Kanamoto M. Ohashi W. Hojyo S. Atsumi T. Ueda N. Azuma I. Hirota H. Murakami M. Zinc suppresses Th17 development via inhibition of STAT3 activation Int. Immunol. 22 5 2010 375 386 20215335
  37. [47]Rosenkranz E. Maywald M. Hilgers R.-D. Brieger A. Clarner T. Kipp M. Plümäkers B. Meyer S. Schwerdtle T. Rink L. Induction of regulatory T cells in Th1-/Th17-driven experimental autoimmune encephalomyelitis by zinc administration J. Nutr. Biochem. 29 2016 116 123 26895672
  38. [48]Omilusik K. Priatel John J. Chen X. Wang Yiwen T. Xu H. Choi Kyung B. Gopaul R. McIntyre-Smith A. Teh H.-S. Tan R. Bech-Hansen N.T. Waterfield D. Fedida D. Hunt Simon V. Jefferies Wilfred A. The CaV1.4 calcium channel is a critical regulator of T cell receptor signaling and naive T cell homeostasis Immunity 35 3 2011 349 360 21835646
  39. [49]Trebak M. Kinet J.-P. Calcium signalling in T cells Nat. Rev. Immunol. 19 3 2019 154 169 30622345 PMC6788797
  40. [50]Li W.-T. Wang L.-Y. Chang H.-W. Yang W.-C. Lo C. Pang V.F. Chen M.-H. Jeng C.-R. Th2 cytokine bias induced by silver nanoparticles in peripheral blood mononuclear cells of common bottlenose dolphins (Tursiops truncatus) PeerJ 6 2018 e5432 PMC6147119 30245924
  41. [51]Griffin D.R. Archang M.M. Kuan C.H. Weaver W.M. Weinstein J.S. Feng A.C. Ruccia A. Sideris E. Ragkousis V. Koh J. Plikus M.V. Di Carlo D. Segura T. Scumpia P.O. Activating an adaptive immune response from a hydrogel scaffold imparts regenerative wound healing Nat. Mater. 20 4 2021 560 569 33168979 PMC8005402
  42. [52]Akagi T. Higashi M. Kaneko T. Kida T. Akashi M. Hydrolytic and enzymatic degradation of nanoparticles based on amphiphilic poly(γ-glutamic acid)-graft-l-Phenylalanine copolymers Biomacromolecules 7 1 2006 297 303 16398528
  43. [53]Wongpinyochit T. Johnston B.F. Seib F.P. Degradation behavior of silk nanoparticles—enzyme responsiveness ACS Biomater. Sci. Eng. 4 3 2018 942 951 33418776
  44. [54]Fagerholm S.C. Integrins in health and disease N. Engl. J. Med. 387 16 2022 1519 1521 36170474
  45. [55]Faull R.J. Kovach N.L. Harlan J.M. Ginsberg M.H. Stimulation of integrin-mediated adhesion of T lymphocytes and monocytes: two mechanisms with divergent biological consequences J. Exp. Med. 179 4 1994 1307 1316 7511685 PMC2191445
  46. [56]Hogg N. Laschinger M. Giles K. McDowall A. T-cell integrins: more than just sticking points J. Cell Sci. 116 Pt 23 2003 4695 4705 14600256
  47. [57]Sims T.N. Dustin M.L. The immunological synapse: integrins take the stage Immunol. Rev. 186 2002 100 117 12234366
  48. [58]Krivacic K.A. Levine A.D. Extracellular matrix conditions T cells for adhesion to tissue interstitium J. Immunol. 170 10 2003 5034 5044 12734348
  49. [59]Liu X. Qiao Y. Chen J. Ge G. Basement membrane promotes tumor development by attenuating T cell activation J. Mol. Cell Biol. 14 2 2022 PMC9122659 35090030
  50. [60]Robertson C. Sebastian A. Hinckley A. Rios-Arce N.D. Hynes W.F. Edwards S.A. He W. Hum N.R. Wheeler E.K. Loots G.G. Coleman M.A. Moya M.L. Extracellular matrix modulates T cell clearance of malignant cells in vitro Biomaterials 282 2022 121378 35121359
  51. [61]Rabinovich G.A. Ariel A. Hershkoviz R. Hirabayashi J. Kasai K.I. Lider O. Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1 Immunology 97 1 1999 100 106 10447720 PMC2326819
  52. [62]Neto E.H. Coelho A.L. Sampaio A.L. Henriques M. Marcinkiewicz C. De Freitas M.S. Barja-Fidalgo C. Activation of human T lymphocytes via integrin signaling induced by RGD-disintegrins Biochim. Biophys. Acta 1773 2 2007 176 184 17081636
  53. [63]Kuczek D.E. Larsen A.M.H. Thorseth M.L. Carretta M. Kalvisa A. Siersbaek M.S. Simoes A.M.C. Roslind A. Engelholm L.H. Noessner E. Donia M. Svane I.M. Straten P.T. Grontved L. Madsen D.H. Collagen density regulates the activity of tumor-infiltrating T cells J Immunother Cancer 7 1 2019 68 30867051 PMC6417085
  54. [64]Gao H. Tian Q. Zhu L. Feng J. Zhou Y. Yang J. 3D extracellular matrix regulates the activity of T cells and cancer associated fibroblasts in breast cancer Front. Oncol. 11 2021 764204 PMC8699235 34956886
  55. [65]Stephan M.T. Moon J.J. Um S.H. Bershteyn A. Irvine D.J. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles Nat. Med. 16 9 2010 1035 1041 20711198 PMC2935928
  56. [66]Stephan M.T. Stephan S.B. Bak P. Chen J. Irvine D.J. Synapse-directed delivery of immunomodulators using T-cell-conjugated nanoparticles Biomaterials 33 23 2012 5776 5787 22594972 PMC3395588
  57. [67]Hui E.E. Bhatia S.N. Micromechanical control of cell-cell interactions Proc. Natl. Acad. Sci. U. S. A. 104 14 2007 5722 5726 17389399 PMC1851558
  58. [68]Sadoun A. Biarnes-Pelicot M. Ghesquiere-Dierickx L. Wu A. Theodoly O. Limozin L. Hamon Y. Puech P.H. Controlling T cells spreading, mechanics and activation by micropatterning Sci. Rep. 11 1 2021 6783 33762632 PMC7991639
  59. [69]Krummel M.F. Friedman R.S. Jacobelli J. Modes and mechanisms of T cell motility: roles for confinement and Myosin-IIA Curr. Opin. Cell Biol. 30 2014 9 16 24905977 PMC4178009
  60. [70]Govendir M.A. Kempe D. Sianati S. Cremasco J. Mazalo J.K. Colakoglu F. Golo M. Poole K. Biro M. T cell cytoskeletal forces shape synapse topography for targeted lysis via membrane curvature bias of perforin Dev. Cell 57 18 2022 2237 2247 e8 36113483
  61. [71]Doh J. Irvine D.J. Immunological synapse arrays: patterned protein surfaces that modulate immunological synapse structure formation in T cells Proc. Natl. Acad. Sci. U. S. A. 103 15 2006 5700 5705 16585528 PMC1458636
  62. [72]Jung H.R. Song K.H. Chang J.T. Doh J. Geometrically controlled asymmetric division of CD4+ T cells studied by immunological synapse arrays PLoS One 9 3 2014 e91926 PMC3954838 24632942
  63. [73]Shen K. Thomas V.K. Dustin M.L. Kam L.C. Micropatterning of costimulatory ligands enhances CD4+ T cell function Proc. Natl. Acad. Sci. U. S. A. 105 22 2008 7791 7796 18505845 PMC2409411
  64. [74]Lee J.H. Dustin M.L. Kam L.C. A microfluidic platform reveals differential response of regulatory T cells to micropatterned costimulation arrays Integr. Biol. 7 11 2015 1442 1453 PMC4630128 26400012
  65. [75]Steenblock E.R. Fahmy T.M. A comprehensive platform for ex vivo T-cell expansion based on biodegradable polymeric artificial antigen-presenting cells Mol. Ther. 16 4 2008 765 772 18334990
  66. [76]Wauters A.C. Scheerstra J.F. Vermeijlen I.G. Hammink R. Schluck M. Woythe L. Wu H. Albertazzi L. Figdor C.G. Tel J. Abdelmohsen L. van Hest J.C.M. Artificial antigen-presenting cell topology dictates T cell activation ACS Nano 16 9 2022 15072 15085 35969506 PMC9527792
  67. [77]Cheung A.S. Zhang D.K.Y. Koshy S.T. Mooney D.J. Scaffolds that mimic antigen-presenting cells enable ex vivo expansion of primary T cells Nat. Biotechnol. 36 2 2018 160 169 29334370 PMC5801009
  68. [78]Kumar S. Anselmo A.C. Banerjee A. Zakrewsky M. Mitragotri S. Shape and size-dependent immune response to antigen-carrying nanoparticles J. Contr. Release 220 Pt A 2015 141 148 26437263
  69. [79]Chaudhuri P.K. Wang M.S. Black C.T. Huse M. Kam L.C. Modulating T cell activation using depth sensing topographic cues Adv Biosyst 4 9 2020 e2000143 PMC8404344 32744809
  70. [80]Park J.S. Kim J.H. Soh W.C. Kim N.Y. Lee K.S. Kim C.H. Chung I.J. Lee S. Kim H.R. Jun C.D. Trogocytic molting of T cell microvilli upregulates T cell receptor surface expression and promotes clonal expansion Nat. Commun. 14 1 2023 2980 37221214 PMC10205730
  71. [81]Aramesh M. Stoycheva D. Sandu I. Ihle S.J. Zund T. Shiu J.Y. Forro C. Asghari M. Bernero M. Lickert S. Oxenius A. Vogel V. Klotzsch E. Nanoconfinement of microvilli alters gene expression and boosts T cell activation Proc. Natl. Acad. Sci. U. S. A. 118 40 2021 PMC8501847 34599101
  72. [82]Majedi F.S. Hasani-Sadrabadi M.M. Thauland T.J. Li S. Bouchard L.S. Butte M.J. T-cell activation is modulated by the 3D mechanical microenvironment Biomaterials 252 2020 120058 PMC7307918 32413594
  73. [83]Saraswathibhatla A. Indana D. Chaudhuri O. Cell-extracellular matrix mechanotransduction in 3D Nat. Rev. Mol. Cell Biol. 24 7 2023 495 516 36849594 PMC10656994
  74. [84]Perez Del Rio E. Martinez Miguel M. Veciana J. Ratera I. Guasch J. Artificial 3D culture systems for T cell expansion ACS Omega 3 5 2018 5273 5280 30023914 PMC6044561
  75. [85]Hickey J.W. Dong Y. Chung J.W. Salathe S.F. Pruitt H.C. Li X. Chang C. Fraser A.K. Bessell C.A. Ewald A.J. Gerecht S. Mao H.Q. Schneck J.P. Engineering an artificial T-cell stimulating matrix for immunotherapy Adv. Mater. 31 23 2019 e1807359 PMC8601018 30968468
  76. [86]Perez Del Rio E. Santos F. Rodriguez Rodriguez X. Martinez-Miguel M. Roca-Pinilla R. Aris A. Garcia-Fruitos E. Veciana J. Spatz J.P. Ratera I. Guasch J. CCL21-loaded 3D hydrogels for T cell expansion and differentiation Biomaterials 259 2020 120313 32829146
  77. [87]Joseph J.P. Gugulothu S.B. Nandi D. Chatterjee K. Mechanical properties affect primary T cell activation in 3D bioprinted hydrogels ACS Macro Lett. 12 8 2023 1085 1093 37466277
  78. [89]Nikolova M.P. Chavali M.S. Recent advances in biomaterials for 3D scaffolds: a review Bioact. Mater. 4 2019 271 292 31709311 PMC6829098
  79. [91]Lee J.W. Song K.H. Fibrous hydrogels by electrospinning: novel platforms for biomedical applications J. Tissue Eng. 14 2023 20417314231191881 PMC10423451 37581121
  80. [92]Qazi T.H. Wu J. Muir V.G. Weintraub S. Gullbrand S.E. Lee D. Issadore D. Burdick J.A. Anisotropic rod-shaped particles influence injectable granular hydrogel properties and cell invasion Adv. Mater. 34 12 2022 e2109194 PMC8957565 34932833
  81. [93]Sousa J.P.M. Stratakis E. Mano J. Marques P.A.A.P. Anisotropic 3D scaffolds for spinal cord guided repair: current concepts Biomater. Adv. 148 2023 213353 36848743
  82. [94]Chen B. Jia Y. Gao Y. Sanchez L. Anthony S.M. Yu Y. Janus particles as artificial antigen-presenting cells for T cell activation ACS Appl. Mater. Interfaces 6 21 2014 18435 18439 25343426 PMC4404154
  83. [95]Ben-Akiva E. Hickey J.W. Meyer R.A. Isser A. Shannon S.R. Livingston N.K. Rhodes K.R. Kosmides A.K. Warren T.R. Tzeng S.Y. Schneck J.P. Green J.J. Shape matters: biodegradable anisotropic nanoparticle artificial antigen presenting cells for cancer immunotherapy Acta Biomater. 160 2023 187 197 36812956 PMC10335041
  84. [96]Meyer R.A. Sunshine J.C. Perica K. Kosmides A.K. Aje K. Schneck J.P. Green J.J. Biodegradable nanoellipsoidal artificial antigen presenting cells for antigen specific T-cell activation Small 11 13 2015 1519 1525 25641795 PMC4529071
  85. [97]Blumenthal D. Chandra V. Avery L. Burkhardt J.K. Mouse T cell priming is enhanced by maturation-dependent stiffening of the dendritic cell cortex Elife 9 2020 PMC7417170 32720892
  86. [98]Jin W. Tamzalit F. Chaudhuri P.K. Black C.T. Huse M. Kam L.C. T cell activation and immune synapse organization respond to the microscale mechanics of structured surfaces Proc. Natl. Acad. Sci. U. S. A. 116 40 2019 19835 19840 31527238 PMC6778209
  87. [99]Hyun J. Kim S.J. Cho S.D. Kim H.W. Mechano-modulation of T cells for cancer immunotherapy Biomaterials 297 2023 122101 37023528
  88. [100]Bonnans C. Chou J. Werb Z. Remodelling the extracellular matrix in development and disease Nat. Rev. Mol. Cell Biol. 15 12 2014 786 801 25415508 PMC4316204
  89. [101]Zhu C. Chen W. Lou J. Rittase W. Li K. Mechanosensing through immunoreceptors Nat. Immunol. 20 10 2019 1269 1278 31534240 PMC7592628
  90. [102]Wahl A. Dinet C. Dillard P. Nassereddine A. Puech P.H. Limozin L. Sengupta K. Biphasic mechanosensitivity of T cell receptor-mediated spreading of lymphocytes Proc. Natl. Acad. Sci. U. S. A. 116 13 2019 5908 5913 30850545 PMC6442626
  91. [103]Saitakis M. Dogniaux S. Goudot C. Bufi N. Asnacios S. Maurin M. Randriamampita C. Asnacios A. Hivroz C. Different TCR-induced T lymphocyte responses are potentiated by stiffness with variable sensitivity Elife 6 2017 PMC5464771 28594327
  92. [104]Meng K.P. Majedi F.S. Thauland T.J. Butte M.J. Mechanosensing through YAP controls T cell activation and metabolism J. Exp. Med. 217 8 2020 PMC7398163 32484502
  93. [105]Basu R. Whitlock B.M. Husson J. Le Floc'h A. Jin W. Oyler-Yaniv A. Dotiwala F. Giannone G. Hivroz C. Biais N. Lieberman J. Kam L.C. Huse M. Cytotoxic T cells use mechanical force to potentiate target cell killing Cell 165 1 2016 100 110 26924577 PMC4808403
  94. [106]Liu Y. Zhang T. Zhang H. Li J. Zhou N. Fiskesund R. Chen J. Lv J. Ma J. Zhang H. Tang K. Cheng F. Zhou Y. Zhang X. Wang N. Huang B. Cell softness prevents cytolytic T-cell killing of tumor-repopulating cells Cancer Res. 81 2 2021 476 488 33168645
  95. [107]Spillane K.M. Tolar P. B cell antigen extraction is regulated by physical properties of antigen-presenting cells J. Cell Biol. 216 1 2017 217 230 27923880 PMC5223605
  96. [108]Chaudhuri O. Cooper-White J. Janmey P.A. Mooney D.J. Shenoy V.B. Effects of extracellular matrix viscoelasticity on cellular behaviour Nature 584 7822 2020 535 546 32848221 PMC7676152
  97. [109]Vining K.H. Marneth A.E. Adu-Berchie K. Grolman J.M. Tringides C.M. Liu Y. Wong W.J. Pozdnyakova O. Severgnini M. Stafford A. Duda G.N. Hodi F.S. Mullally A. Wucherpfennig K.W. Mooney D.J. Mechanical checkpoint regulates monocyte differentiation in fibrotic niches Nat. Mater. 21 8 2022 939 950 35817965 PMC10197159
  98. [110]Chaudhuri O. Gu L. Klumpers D. Darnell M. Bencherif S.A. Weaver J.C. Huebsch N. Lee H.P. Lippens E. Duda G.N. Mooney D.J. Hydrogels with tunable stress relaxation regulate stem cell fate and activity Nat. Mater. 15 3 2016 326 334 26618884 PMC4767627
  99. [111]Khetan S. Guvendiren M. Legant W.R. Cohen D.M. Chen C.S. Burdick J.A. Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels Nat. Mater. 12 5 2013 458 465 23524375 PMC3633615
  100. [112]Adu-Berchie K. Liu Y. Zhang D.K.Y. Freedman B.R. Brockman J.M. Vining K.H. Nerger B.A. Garmilla A. Mooney D.J. Generation of functionally distinct T-cell populations by altering the viscoelasticity of their extracellular matrix Nat. Biomed. Eng. 7 11 2023 1374 1391 37365267 PMC10749992
  101. [113]Hope J.M. Dombroski J.A. Pereles R.S. Lopez-Cavestany M. Greenlee J.D. Schwager S.C. Reinhart-King C.A. King M.R. Fluid shear stress enhances T cell activation through Piezo1 BMC Biol. 20 1 2022 61 35260156 PMC8904069
  102. [114]Sadtler K. Estrellas K. Allen B.W. Wolf M.T. Fan H. Tam A.J. Patel C.H. Luber B.S. Wang H. Wagner K.R. Powell J.D. Housseau F. Pardoll D.M. Elisseeff J.H. Developing a pro-regenerative biomaterial scaffold microenvironment requires T helper 2 cells Science 352 6283 2016 366 370 27081073 PMC4866509
  103. [115]Wang X. Chung L. Hooks J. Maestas D.R. Jr. Lebid A. Andorko J.I. Huleihel L. Chin A.F. Wolf M. Remlinger N.T. Stepp M.A. Housseau F. Elisseeff J.H. Type 2 immunity induced by bladder extracellular matrix enhances corneal wound healing Sci. Adv. 7 16 2021 PMC8051883 33863719
  104. [116]Wolf M.T. Ganguly S. Wang T.L. Anderson C.W. Sadtler K. Narain R. Cherry C. Parrillo A.J. Park B.V. Wang G. Pan F. Sukumar S. Pardoll D.M. Elisseeff J.H. A biologic scaffold-associated type 2 immune microenvironment inhibits tumor formation and synergizes with checkpoint immunotherapy Sci. Transl. Med. 11 477 2019 PMC7254933 30700576
  105. [117]Su N. Hao Y. Wang F. Hou W. Chen H. Luo Y. Mesenchymal stromal exosome-functionalized scaffolds induce innate and adaptive immunomodulatory responses toward tissue repair Sci. Adv. 7 20 2021 PMC8115917 33980490
  106. [118]Zhang B. Yeo R.W.Y. Lai R.C. Sim E.W.K. Chin K.C. Lim S.K. Mesenchymal stromal cell exosome-enhanced regulatory T-cell production through an antigen-presenting cell-mediated pathway Cytotherapy 20 5 2018 687 696 29622483
  107. [119]Crain S.K. Robinson S.R. Thane K.E. Davis A.M. Meola D.M. Barton B.A. Yang V.K. Hoffman A.M. Extracellular vesicles from wharton's jelly mesenchymal stem cells suppress CD4 expressing T cells through transforming growth factor beta and adenosine signaling in a canine model Stem Cell. Dev. 28 3 2019 212 226 30412034
  108. [120]Chen W. Huang Y. Han J. Yu L. Li Y. Lu Z. Li H. Liu Z. Shi C. Duan F. Xiao Y. Immunomodulatory effects of mesenchymal stromal cells-derived exosome Immunol. Res. 64 4 2016 831 840 27115513
  109. [121]Lo Sicco C. Reverberi D. Balbi C. Ulivi V. Principi E. Pascucci L. Becherini P. Bosco M.C. Varesio L. Franzin C. Pozzobon M. Cancedda R. Tasso R. Mesenchymal stem cell-derived extracellular vesicles as mediators of anti-inflammatory effects: endorsement of macrophage polarization Stem Cells Transl Med 6 3 2017 1018 1028 28186708 PMC5442783
  110. [122]Majedi F.S. Hasani-Sadrabadi M.M. Thauland T.J. Keswani S.G. Li S. Bouchard L.S. Butte M.J. Systemic enhancement of antitumour immunity by peritumourally implanted immunomodulatory macroporous scaffolds Nat. Biomed. Eng. 7 1 2023 56 71 36550304 PMC9940651
  111. [123]Tay R.E. Richardson E.K. Toh H.C. Revisiting the role of CD4(+) T cells in cancer immunotherapy-new insights into old paradigms Cancer Gene Ther. 28 1–2 2021 5 17 32457487 PMC7886651
  112. [125]Wood K.J. Bushell A. Hester J. Regulatory immune cells in transplantation Nat. Rev. Immunol. 12 6 2012 417 430 22627860
  113. [126]Doloff J.C. Veiseh O. de Mezerville R. Sforza M. Perry T.A. Haupt J. Jamiel M. Chambers C. Nash A. Aghlara-Fotovat S. Stelzel J.L. Bauer S.J. Neshat S.Y. Hancock J. Romero N.A. Hidalgo Y.E. Leiva I.M. Munhoz A.M. Bayat A. Kinney B.M. Hodges H.C. Miranda R.N. Clemens M.W. Langer R. The surface topography of silicone breast implants mediates the foreign body response in mice, rabbits and humans Nat. Biomed. Eng. 5 10 2021 1115 1130 34155355
  114. [127]Hernandez J.L. Park J. Yao S. Blakney A.K. Nguyen H.V. Katz B.H. Jensen J.T. Woodrow K.A. Effect of tissue microenvironment on fibrous capsule formation to biomaterial-coated implants Biomaterials 273 2021 120806 PMC8135119 33905960
  115. [128]Chung L. Maestas D.R. Jr. Lebid A. Mageau A. Rosson G.D. Wu X. Wolf M.T. Tam A.J. Vanderzee I. Wang X. Andorko J.I. Zhang H. Narain R. Sadtler K. Fan H. Cihakova D. Le Saux C.J. Housseau F. Pardoll D.M. Elisseeff J.H. Interleukin 17 and senescent cells regulate the foreign body response to synthetic material implants in mice and humans Sci. Transl. Med. 12 539 2020 PMC7219543 32295900
  116. [130]Tu Z. Zhong Y. Hu H. Shao D. Haag R. Schirner M. Lee J. Sullenger B. Leong K.W. Design of therapeutic biomaterials to control inflammation Nat. Rev. Mater. 7 7 2022 557 574 35251702 PMC8884103
  117. [131]Walker C.J. Crocini C. Ramirez D. Killaars A.R. Grim J.C. Aguado B.A. Clark K. Allen M.A. Dowell R.D. Leinwand L.A. Anseth K.S. Nuclear mechanosensing drives chromatin remodelling in persistently activated fibroblasts Nat. Biomed. Eng. 5 12 2021 1485 1499 33875841 PMC9102466
  118. [132]Guvendiren M. Burdick J.A. Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics Nat. Commun. 3 1 2012 792 22531177
  119. [134]Eisenbarth S.C. Baumjohann D. Craft J. Fazilleau N. Ma C.S. Tangye S.G. Vinuesa C.G. Linterman M.A. CD4(+) T cells that help B cells - a proposal for uniform nomenclature Trends Immunol. 42 8 2021 658 669 34244056 PMC8324560
  120. [135]Nishio N. Ito S. Suzuki H. Isobe K. Antibodies to wounded tissue enhance cutaneous wound healing Immunology 128 3 2009 369 380 20067537 PMC2770685
  121. [136]Singh A. Biomaterials innovation for next generation ex vivo immune tissue engineering Biomaterials 130 2017 104 110 28335993
  122. [137]Swartz M.A. Hirosue S. Hubbell J.A. Engineering approaches to immunotherapy Sci. Transl. Med. 4 148 2012 148rv9 22914624
  123. [138]Li A.W. Sobral M.C. Badrinath S. Choi Y. Graveline A. Stafford A.G. Weaver J.C. Dellacherie M.O. Shih T.Y. Ali O.A. Kim J. Wucherpfennig K.W. Mooney D.J. A facile approach to enhance antigen response for personalized cancer vaccination Nat. Mater. 17 6 2018 528 534 29507416 PMC5970019
  124. [141]Lindell D.M. Berlin A.A. Schaller M.A. Lukacs N.W. B cell antigen presentation promotes Th2 responses and immunopathology during chronic allergic lung disease PLoS One 3 9 2008 e3129 PMC2518863 18769622
  125. [142]Linton P.J. Bautista B. Biederman E. Bradley E.S. Harbertson J. Kondrack R.M. Padrick R.C. Bradley L.M. Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo J. Exp. Med. 197 7 2003 875 883 12668647 PMC2193894
  126. [143]Affara N.I. Ruffell B. Medler T.R. Gunderson A.J. Johansson M. Bornstein S. Bergsland E. Steinhoff M. Li Y. Gong Q. Ma Y. Wiesen J.F. Wong M.H. Kulesz-Martin M. Irving B. Coussens L.M. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas Cancer Cell 25 6 2014 809 821 24909985 PMC4063283
  127. [144]Tiemessen M.M. Jagger A.L. Evans H.G. van Herwijnen M.J. John S. Taams L.S. CD4+ CD25+ Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages Proc. Natl. Acad. Sci. USA 104 49 2007 19446 19451 18042719 PMC2148309
  128. [145]Cosgrove B.D. Mui K.L. Driscoll T.P. Caliari S.R. Mehta K.D. Assoian R.K. Burdick J.A. Mauck R.L. N-cadherin adhesive interactions modulate matrix mechanosensing and fate commitment of mesenchymal stem cells Nat. Mater. 15 12 2016 1297 1306 27525568 PMC5121068
  129. [146]Venet F. Pachot A. Debard A.L. Bohe J. Bienvenu J. Lepape A. Powell W.S. Monneret G. Human CD4+CD25+ regulatory T lymphocytes inhibit lipopolysaccharide-induced monocyte survival through a Fas/Fas ligand-dependent mechanism J. Immunol. 177 9 2006 6540 6547 17056586
  130. [147]Mosser D.M. Edwards J.P. Exploring the full spectrum of macrophage activation Nat. Rev. Immunol. 8 12 2008 958 969 19029990 PMC2724991
  131. [148]Kraaij M.D. Savage N.D. van der Kooij S.W. Koekkoek K. Wang J. van den Berg J.M. Ottenhoff T.H. Kuijpers T.W. Holmdahl R. van Kooten C. Gelderman K.A. Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species Proc. Natl. Acad. Sci. U. S. A. 107 41 2010 17686 17691 20861446 PMC2955141
  132. [149]Okeke E.B. Okwor I. Uzonna J.E. Regulatory T cells restrain CD4+ T cells from causing unregulated immune activation and hypersensitivity to lipopolysaccharide challenge J. Immunol. 193 2 2014 655 662 24943218
  133. [150]Miwa H. Antao O.Q. Kelly-Scumpia K.M. Baghdasarian S. Mayer D.P. Shang L. Sanchez G.M. Archang M.M. Scumpia P.O. Weinstein J.S. Di Carlo D. Improved humoral immunity and protection against influenza virus infection with a 3d porous biomaterial vaccine Adv. Sci. 10 31 2023 e2302248 PMC10625058 37750461

Authors
Lee, J.-H., Shin, S.-J., Lee, J. H., Knowles, J. C., Lee, H.-H., & Kim, H.-W.
Affiliations
  • Dankook University (KR)
  • University College London (GB)
Corresponding author
  • Lee, Jung-Hwan
  • Kim, Hae-Won
ORCID
Venue
Bioactive Materials
Publisher
Elsevier BV
Published
2024-11
Volume
41
Pages
499-522
ISSN
  • 2097-1192 (ISSN-L)
  • 2452-199X
DOI
10.1016/j.bioactmat.2024.07.027
PMC
PMC11350271
OpenAlex
W4401454990
Cited by
21
References
149
Citations by year
2026: 9 · 2025: 10 · 2024: 2
FWCI
0.75
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)
  • UCL Discovery (University College London) (submittedVersion, cc-by-nc-nd)
Funders
  • National Research Foundation of Korea (RS-2024-00348908, 2021R1A5A2022318, RS-2023-00220408, RS-2024-00334160, 2019R1A6A1A11034536)
  • UBM
  • Ministry of Science, ICT and Future Planning
  • Ministry of Education
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
Keywords
adaptive immunity, tissue repair, tissue regeneration, tunable biomaterials

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review