Mechanoimmunomodulation-based strategy on advancing tissue-engineered nanotopographic structures

Abstract

The application of nanotopographic structures is considered a promising strategy for improving outcomes in tissue engineering. Nanotopographic structures-mediated immune responses have a more profound influence than the direct modulation of functional cell responses. However, the reported immunomodulatory effects of different nanotopographic structures are inconsistent and unpredictable. Therefore, it is necessary to further understand the general or fundamental biological mechanisms underlying nanotopographic structures-mediated immune regulation to fabricate structures with the desired immunomodulatory properties. Compared to the effects on protein absorption and physiochemical signals, the mechanical forces induced by nanotopographic structures play a more pivotal role in determining immune responses. Elucidating the mechanotransduction mechanisms by which mechanical forces from nanotopographic structures are converted into intracellular biochemical signals in immune cells is crucial. This understanding is essential for the precise regulation of immune responses mediated by nanotopographic structures and for guiding the development of nanotopographic structures with advanced immunomodulatory properties. This review elucidates the impact of nanotopographic structures on cellular mechanical forces and the subsequent activation of mechanosensors. The ensuing mechano-regulatory effects on immune responses are reviewed, and mechanoimmunomodulation is proposed as a strategy for designing nanotopographic structures to modulate immunity. This review contributes to revolutionizing the strategy for developing nanotopographic structures and promotes the application of nanotopographic structures with the mechanoimmunomodulatory property in tissue engineering.

Keywords

Nanotopographic structures / mechanical forces / mechanotransduction / immune responses / mechanoimmunomodulation / tissue engineering microstructures

References

[1] Adhikari J,Chanda A.Effects of surface patterning and topography on the cellular functions of tissue engineered scaffolds with special reference to 3D bioprinting.Biomater Sci2023;11:1236-69

[2] Patel KD,Mandakhbayar N.Coating biopolymer nanofibers with carbon nanotubes accelerates tissue healing and bone regeneration through orchestrated cell- and tissue-regulatory responses.Acta Biomater2020;108:97-110

[3] Choudhary S,Webster TJ.Enhanced functions of vascular cells on nanostructured Ti for improved stent applications.Tissue Eng2007;13:1421-30

[4] Lee SJ,Lim GJ,Stitzel J.In vitro evaluation of electrospun nanofiber scaffolds for vascular graft application.J Biomed Mater Res A2007;83:999-1008

[5] Moore EM,Comeau HY.The immune system and its contribution to variability in regenerative medicine.Tissue Eng Part B Rev2021;27:39-47 PMCID:PMC7891216

[6] Ma QL,Liu RR.Improved implant osseointegration of a nanostructured titanium surface via mediation of macrophage polarization.Biomaterials2014;35:9853-67

[7] Morelli I,George DA,Scarponi S.Masquelet technique: myth or reality? A systematic review and meta-analysis.Injury2016;47 Suppl 6:S68-76

[8] Wang W,Long H.Advances in the Masquelet technique: myeloid-derived suppressor cells promote angiogenesis in PMMA-induced membranes.Acta Biomater2020;108:223-36

[9] Pelissier P,Bareille R,Amedee J.Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration.J Orthop Res2004;22:73-9

[10] Chen Z,Crawford R,Wu C.The effect of osteoimmunomodulation on the osteogenic effects of cobalt incorporated β-tricalcium phosphate.Biomaterials2015;61:126-38

[11] Anderson JM,Chang DT.Foreign body reaction to biomaterials.Semin Immunol2008;20:86-100 PMCID:PMC2327202

[12] Doloff JC,Vegas AJ.Colony stimulating factor-1 receptor is a central component of the foreign body response to biomaterial implants in rodents and non-human primates.Nat Mater2017;16:671-80 PMCID:PMC5445003

[13] Wynn TA.Mechanisms of fibrosis: therapeutic translation for fibrotic disease.Nat Med2012;18:1028-40 PMCID:PMC3405917

[14] 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 Technol2008;2:768-77 PMCID:PMC2769792

[15] Guo Y,Ye C.A practical guide to promote informatics-driven efficient biotopographic material development.Bioact Mater2022;8:515-28 PMCID:PMC8433058

[16] Chen Z,Wei F.Nanotopography-based strategy for the precise manipulation of osteoimmunomodulation in bone regeneration.Nanoscale2017;9:18129-52

[17] Feng R,Xu J.Knowledge gaps in immune response and immunotherapy involving nanomaterials: databases and artificial intelligence for material design.Biomaterials2021;266:120469

[18] Luo J,Xiao Y,Dalby MJ.The influence of nanotopography on cell behaviour through interactions with the extracellular matrix - a review.Bioact Mater2022;15:145-59 PMCID:PMC8940943

[19] Mpoyi E, Cantini M, Reynolds PM, Gadegaard N, Dalby MJ, Salmerón-Sánchez M. Protein adsorption as a key mediator in the nanotopographical control of cell behavior.ACS Nano2016;10:6638-47 PMCID:PMC4980054

[20] Dabare PRL,Quek JY,Hayball J.Nano-roughness-mediated macrophage polarization for desired host immune response.Small Sci2023;3:2300080

[21] Wang C,Lu R,Yuan D.Influence of surface nanotopography and wettability on early phases of peri-implant soft tissue healing: an in-vivo study in dogs.BMC Oral Health2023;23:651 PMCID:PMC10492342

[22] Webster TJ,Siegel RW.Mechanisms of enhanced osteoblast adhesion on nanophase alumina involve vitronectin.Tissue Eng2001;7:291-301

[23] Xie X,Angle MR,Verma P.Mechanical model of vertical nanowire cell penetration.Nano Lett2013;13:6002-8

[24] Guo Y,Ye C.Nanotopographic micro-nano forces finely tune the conformation of macrophage mechanosensitive membrane protein integrin β2 to manipulate inflammatory responses.Nano Res2023;5:1-15 PMCID:PMC9986042

[25] Afzal J, Chang H, Goyal R, Levchenko A. Mechanics of microenvironment as instructive cues guiding stem cell behavior.Curr Stem Cell Rep2016;2:62-72

[26] Zhu C,Lou J,Li K.Mechanosensing through immunoreceptors.Nat Immunol2019;20:1269-78

[27] Zhang X,Thauland TJ.Unraveling the mechanobiology of immune cells.Curr Opin Biotechnol2020;66:236-45

[28] Huse M.Mechanical forces in the immune system.Nat Rev Immunol2017;17:679-90 PMCID:PMC6312705

[29] Mierke CT.Viscoelasticity, like forces, plays a role in mechanotransduction.Front Cell Dev Biol2022;10:789841 PMCID:PMC8864183

[30] Kelkar M,Charras G.Mechanics of the cellular actin cortex: from signalling to shape change.Curr Opin Cell Biol2020;66:69-78

[31] Taylor MP,Enquist LW.Subversion of the actin cytoskeleton during viral infection.Nat Rev Microbiol2011;9:427-39 PMCID:PMC3229036

[32] Schaks M,Rottner K.Actin dynamics in cell migration.Essays Biochem2019;63:483-95 PMCID:PMC6823167

[33] Ventre M,Netti PA.Determinants of cell-material crosstalk at the interface: towards engineering of cell instructive materials.J R Soc Interface2012;9:2017-32 PMCID:PMC3405766

[34] Li X,Zhang W.Nanoscale surface topography reduces focal adhesions and cell stiffness by enhancing integrin endocytosis.Nano Lett2021;21:8518-26 PMCID:PMC8516714

[35] Teo BKK,Lim CK.Nanotopography modulates mechanotransduction of stem cells and induces differentiation through focal adhesion kinase.ACS Nano2013;7:4785-98

[36] Bello D, Fouillen A, Badia A, Nanci A. Nanoporosity stimulates cell spreading and focal adhesion formation in cells with mutated paxillin.ACS Appl Mater Interfaces2020;12:14924-32

[37] Dalby MJ,Riehle MO,Affrossman S.Rapid fibroblast adhesion to 27 nm high polymer demixed nano-topography.Biomaterials2004;25:77-83

[38] Oria R,Escribano J.Force loading explains spatial sensing of ligands by cells.Nature2017;552:219-24

[39] Sun Z,Fässler R.Integrin-mediated mechanotransduction.J Cell Biol2016;215:445-56 PMCID:PMC5119943

[40] Cheng Y.Effects of nanopillars and surface coating on dynamic traction force.Microsyst Nanoeng2023;9:6 PMCID:PMC9814462

[41] Hanson L,Lou HY.Vertical nanopillars for in situ probing of nuclear mechanics in adherent cells.Nat Nanotechnol2015;10:554-62 PMCID:PMC5108456

[42] Persson H,Mølhave K.Fibroblasts cultured on nanowires exhibit low motility, impaired cell division, and DNA damage.Small2013;9:4006-16 PMCID:PMC4282547

[43] Saux G, Bar-Hanin N, Edri A, Hadad U, Porgador A, Schvartzman M. Nanoscale mechanosensing of natural killer cells is revealed by antigen-functionalized nanowires.Adv Mater2019;31:e1805954

[44] Lüchtefeld I,Mejía Morales J.Elasticity spectra as a tool to investigate actin cortex mechanics.J Nanobiotechnol2020;18:147 PMCID:PMC7576730

[45] Di X,Peng L.Cellular mechanotransduction in health and diseases: from molecular mechanism to therapeutic targets.Signal Transduct Target Ther2023;8:282 PMCID:PMC10387486

[46] Xia K,Wang W.Roles of mechanosensitive ion channels in immune cells.Heliyon2024;10:e23318 PMCID:PMC10750075

[47] Driscoll TP,Ahn SJ.Integrin-based mechanosensing through conformational deformation.Biophys J2021;120:4349-59 PMCID:PMC8553792

[48] Sinha B,Ruez R.Cells respond to mechanical stress by rapid disassembly of caveolae.Cell2011;144:402-13 PMCID:PMC3042189

[49] Chang YC,Wang CW.Hippo signaling-mediated mechanotransduction in cell movement and cancer metastasis.Front Mol Biosci2019;6:157 PMCID:PMC7025494

[50] Yamauchi T.Hippo pathway in mammalian adaptive immune system.Cells2019;8:398 PMCID:PMC6563119

[51] Jeffreys N,Zhai Y,Mooney DJ.Mechanical forces amplify TCR mechanotransduction in T cell activation and function.Appl Phys Rev2024;11:011304 PMCID:PMC10848667

[52] Upadhyaya A.Mechanosensing in the immune response.Semin Cell Dev Biol2017;71:137-45 PMCID:PMC5747250

[53] Wang Y,Yang Q.Immunoregulatory role of the mechanosensitive ion channel Piezo1 in inflammation and cancer.Molecules2022;28:213 PMCID:PMC9822220

[54] Scheraga RG,Grove LM.The role of TRPV4 in regulating innate immune cell function in lung inflammation.Front Immunol2020;11:1211 PMCID:PMC7333351

[55] Zhang M,Ye X,Pan L.TRP (transient receptor potential) ion channel family: structures, biological functions and therapeutic interventions for diseases.Signal Transduct Target Ther2023;8:261 PMCID:PMC10319900

[56] Santoni G,Morelli MB,Nabissi M.Danger- and pathogen-associated molecular patterns recognition by pattern-recognition receptors and ion channels of the transient receptor potential family triggers the inflammasome activation in immune cells and sensory neurons.J Neuroinflammation2015;12:21 PMCID:PMC4322456

[57] Michalick L.TRPV4-a missing link between mechanosensation and immunity.Front Immunol2020;11:413 PMCID:PMC7076180

[58] Hellmich UA.Structural biology of TRP channels.Handb Exp Pharmacol2014;223:963-90 PMCID:PMC5075240

[59] Méndez-Reséndiz KA,González-Ramírez R,Rosenbaum T.Steroids and TRP channels: a close relationship.Int J Mol Sci2020;21:3819 PMCID:PMC7325571

[60] Voets T,Owsianik G.Sensing with TRP channels.Nat Chem Biol2005;1:85-92

[61] Loukin S,Su Z,Kung C.Wild-type and brachyolmia-causing mutant TRPV4 channels respond directly to stretch force.J Biol Chem2010;285:27176-81 PMCID:PMC2930716

[62] Soya M,Sobhan U.Plasma membrane stretch activates transient receptor potential vanilloid and ankyrin channels in Merkel cells from hamster buccal mucosa.Cell Calcium2014;55:208-18

[63] Du H,Butenko S.Tuning immunity through tissue mechanotransduction.Nat Rev Immunol2023;23:174-88 PMCID:PMC9379893

[64] Dutta B,Rahaman SO.TRPV4 plays a role in matrix stiffness-induced macrophage polarization.Front Immunol2020;11:570195 PMCID:PMC7767862

[65] Pairet N,Fois G.TRPV4 inhibition attenuates stretch-induced inflammatory cellular responses and lung barrier dysfunction during mechanical ventilation.PLoS One2018;13:e0196055 PMCID:PMC5903668

[66] Goswami R,Sharma S.TRPV4 calcium-permeable channel is a novel regulator of oxidized LDL-induced macrophage foam cell formation.Free Radic Biol Med2017;110:142-50

[67] Li M,Zheng YF.Transient receptor potential vanilloid 4 is a critical mediator in LPS mediated inflammation by mediating calcineurin/NFATc3 signaling.Biochem Biophys Res Commun2019;513:1005-12

[68] Rayees S,Tauseef M.PAR2-mediated cAMP generation suppresses TRPV4-dependent Ca²⁺ signaling in alveolar macrophages to resolve TLR4-induced inflammation.Cell Rep2019;27:793-805.e4 PMCID:PMC6485424

[69] Atobe M.Activation of transient receptor potential vanilloid (TRPV) 4 as a therapeutic strategy in osteoarthritis.Curr Top Med Chem2019;19:2254-67

[70] Atobe M,Muramatsu S.Discovery of novel transient receptor potential vanilloid 4 (TRPV4) agonists as regulators of chondrogenic differentiation: identification of quinazolin-4(3H)-ones and in vivo studies on a surgically induced rat model of osteoarthritis.J Med Chem2019;62:1468-83

[71] Xu S,Yin M.A novel TRPV4-specific agonist inhibits monocyte adhesion and atherosclerosis.Oncotarget2016;7:37622-35 PMCID:PMC5122337

[72] Thoppil RJ,Cappelli HC.TRPV4 channel activation selectively inhibits tumor endothelial cell proliferation.Sci Rep2015;5:14257 PMCID:PMC4585691

[73] Qin L,Chen S.Roles of mechanosensitive channel Piezo1/2 proteins in skeleton and other tissues.Bone Res2021;9:44 PMCID:PMC8526690

[74] Jankovsky N,Demagny J.Recent advances in the pathophysiology of PIEZO1-related hereditary xerocytosis.Am J Hematol2021;96:1017-26

[75] Fang XZ,Xu JQ.Structure, kinetic properties and biological function of mechanosensitive Piezo channels.Cell Biosci2021;11:13 PMCID:PMC7796548

[76] Liang X.Structural biology: piezo senses tension through curvature.Curr Biol2018;28:R357-9 PMCID:PMC6452451

[77] Geng J,Zhang J.TLR4 signalling via Piezo1 engages and enhances the macrophage mediated host response during bacterial infection.Nat Commun2021;12:3519 PMCID:PMC8192512

[78] Atcha H,Holt JR.Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing.Nat Commun2021;12:3256 PMCID:PMC8167181

[79] Wu J,Liao Z.Self-amplifying loop of NF-κB and periostin initiated by PIEZO1 accelerates mechano-induced senescence of nucleus pulposus cells and intervertebral disc degeneration.Mol Ther2022;30:3241-56 PMCID:PMC9552911

[80] Solis AG,Steach HR.Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity.Nature2019;573:69-74 PMCID:PMC6939392

[81] Baratchi S,Wallert M.Transcatheter aortic valve implantation represents an anti-inflammatory therapy via reduction of shear stress-induced, Piezo-1-mediated monocyte activation.Circulation2020;142:1092-105

[82] Aykut B,Kim JI.Targeting Piezo1 unleashes innate immunity against cancer and infectious disease.Sci Immunol2020;5:eabb5168

[83] Wang J,Wan Z.Profiling the origin, dynamics, and function of traction force in B cell activation.Sci Signal2018;11:eaai9192

[84] Wan Z,Chen H.The activation of IgM- or isotype-switched IgG- and IgE-BCR exhibits distinct mechanical force sensitivity and threshold.Elife2015;4:e06925 PMCID:PMC4555871

[85] Kwak K,George R.B cell responses to membrane-presented antigens require the function of the mechanosensitive cation channel Piezo1.Sci Signal2023;16:eabq5096 PMCID:PMC10691204

[86] Jairaman A,Dynes JL.Piezo1 channels restrain regulatory T cells but are dispensable for effector CD4⁺ T cell responses.Sci Adv2021;7:eabg5859 PMCID:PMC8262815

[87] Abiff M,Bonner M.Piezo1 facilitates optimal T cell activation during tumor challenge.Oncoimmunology2023;12:2281179 PMCID:PMC10732680

[88] Liu CSC,Paul B.Cutting edge: Piezo1 mechanosensors optimize human T cell activation.J Immunol2018;200:1255-60

[89] Hope JM,Pereles RS.Fluid shear stress enhances T cell activation through Piezo1.BMC Biol2022;20:61 PMCID:PMC8904069

[90] Campbell ID.Integrin structure, activation, and interactions.Cold Spring Harb Perspect Biol2011;3:a004994 PMCID:PMC3039929

[91] Cormier A,Ito S.Cryo-EM structure of the αvβ8 integrin reveals a mechanism for stabilizing integrin extension.Nat Struct Mol Biol2018;25:698-704 PMCID:PMC6214843

[92] Bouaouina M,Calderwood DA.Talin and signaling through integrins.Methods Mol Biol2012;757:325-47 PMCID:PMC5642996

[93] Park EJ,Kiyono H.Structural basis of blocking integrin activation and deactivation for anti-inflammation.J Biomed Sci2015;22:51 PMCID:PMC4495637

[94] Friedland JC,Boettiger D.Mechanically activated integrin switch controls alpha5beta1 function.Science2009;323:642-4

[95] Gingras AR.Signal transduction: physical deformation of the membrane activates integrins.Curr Biol2020;30:R397-400

[96] Kechagia JZ,Roca-Cusachs P.Integrins as biomechanical sensors of the microenvironment.Nat Rev Mol Cell Biol2019;20:457-73

[97] Dembo M,Saxman K.The reaction-limited kinetics of membrane-to-surface adhesion and detachment.Proc R Soc Lond B Biol Sci1988;234:55-83

[98] Kong F,Mould AP,Zhu C.Demonstration of catch bonds between an integrin and its ligand.J Cell Biol2009;185:1275-84 PMCID:PMC2712956

[99] Case LB.Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch.Nat Cell Biol2015;17:955-63 PMCID:PMC6300998

[100] Ma H,Zhao X.Periostin promotes colorectal tumorigenesis through integrin-FAK-Src pathway-mediated YAP/TAZ activation.Cell Rep2020;30:793-806.e6

[101] Dai J,Chen Y.Matrix stiffness regulates epithelial-mesenchymal transition via cytoskeletal remodeling and MRTF-A translocation in osteosarcoma cells.J Mech Behav Biomed Mater2019;90:226-38

[102] Dwyer SF,Gelman IH.Identification of novel focal adhesion kinase substrates: role for FAK in NFκB signaling.Int J Biol Sci2015;11:404-10 PMCID:PMC4366639

[103] Jain N.Spatial confinement downsizes the inflammatory response of macrophages.Nat Mater2018;17:1134-44 PMCID:PMC6615903

[104] Fu Y,Chen T.Nanotube patterning reduces macrophage inflammatory response via nuclear mechanotransduction.J Nanobiotechnol2023;21:229 PMCID:PMC10354937

[105] Mia MM,Abdul Ghani SAB.YAP/TAZ deficiency reprograms macrophage phenotype and improves infarct healing and cardiac function after myocardial infarction.PLoS Biol2020;18:e3000941 PMCID:PMC7735680

[106] Batista FD,Barral P.The role of integrins and coreceptors in refining thresholds for B-cell responses.Immunol Rev2007;218:197-213

[107] Wang JC,Wu X.A B-cell actomyosin arc network couples integrin co-stimulation to mechanical force-dependent immune synapse formation.Elife2022;11:e72805 PMCID:PMC9142150

[108] Wang X,Bannard O.Integrin-mediated interactions between B cells and follicular dendritic cells influence germinal center B cell fitness.J Immunol2014;192:4601-9 PMCID:PMC4056595

[109] Andreani V,Fässler R.Integrin β1 regulates marginal zone B cell differentiation and PI3K signaling.J Exp Med2023;220:e20220342 PMCID:PMC9814157

[110] Hogg N,Giles K.T-cell integrins: more than just sticking points.J Cell Sci2003;116:4695-705

[111] Monks CR,Kupfer H,Kupfer A.Three-dimensional segregation of supramolecular activation clusters in T cells.Nature1998;395:82-6

[112] Jankowska KI,Roy NH.Integrins modulate T cell receptor signaling by constraining actin flow at the immunological synapse.Front Immunol2018;9:25

[113] Dimitrov S,Besedovsky L.Activated integrins identify functional antigen-specific CD8⁺ T cells within minutes after antigen stimulation.Proc Natl Acad Sci USA2018;115:E5536-45 PMCID:PMC6004473

[114] Tabdanov E,Kumari S.Micropatterning of TCR and LFA-1 ligands reveals complementary effects on cytoskeleton mechanics in T cells.Integr Biol2015;7:1272-84 PMCID:PMC4593733

[115] Wang MS,Sanchez EE.Mechanically active integrins target lytic secretion at the immune synapse to facilitate cellular cytotoxicity.Nat Commun2022;13:3222 PMCID:PMC9184626

[116] Harris J,Hope JC,Howard CJ.Caveolae and caveolin in immune cells: distribution and functions.Trends Immunol2002;23:158-64

[117] Smart EJ,McNiven MA.Caveolins, liquid-ordered domains, and signal transduction.Mol Cell Biol1999;19:7289-304 PMCID:PMC84723

[118] Parton RG.Caveolae as plasma membrane sensors, protectors and organizers.Nat Rev Mol Cell Biol2013;14:98-112

[119] Nassoy P.Stressing caveolae new role in cell mechanics.Trends Cell Biol2012;22:381-9

[120] Pozo MA, Lolo FN, Echarri A. Caveolae: mechanosensing and mechanotransduction devices linking membrane trafficking to mechanoadaptation.Curr Opin Cell Biol2021;68:113-23

[121] Wang XM,Nakahira K,Choi AMK.The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1.J Immunol2009;182:3809-18

[122] Bucci M,Rudic RD.In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation.Nat Med2000;6:1362-7

[123] Liou JY,Gilroy DW,Wu KK.Colocalization and interaction of cyclooxygenase-2 with caveolin-1 in human fibroblasts.J Biol Chem2001;276:34975-82

[124] Shihata WA,Andrews KL.Caveolae: a role in endothelial inflammation and mechanotransduction?.Front Physiol2016;7:628 PMCID:PMC5168557

[125] Qin L,Ao BX.Caveolae and Caveolin-1 integrate reverse cholesterol transport and inflammation in atherosclerosis.Int J Mol Sci2016;17:429 PMCID:PMC4813279

[126] Wang XM,Song R.Caveolin-1 confers antiinflammatory effects in murine macrophages via the MKK3/p38 MAPK pathway.Am J Respir Cell Mol Biol2006;34:434-42 PMCID:PMC2644205

[127] Medina FA,Sotgia F,Lisanti MP.A novel role for caveolin-1 in B lymphocyte function and the development of thymus-independent immune responses.Cell Cycle2006;5:1865-71

[128] Minguet S,Schaffer AM.Caveolin-1-dependent nanoscale organization of the BCR regulates B cell tolerance.Nat Immunol2017;18:1150-9 PMCID:PMC5608079

[129] Aramesh M,Essand M.Enhanced cellular uptake through nanotopography-induced macropinocytosis.Adv Funct Mater2024;34:2400487

[130] Hyun J,Cho SD.Mechano-modulation of T cells for cancer immunotherapy.Biomaterials2023;297:122101

[131] Swaminathan V.Decoding mechanical cues by molecular mechanotransduction.Curr Opin Cell Biol2021;72:72-80

[132] Goriainov V,Sjostrom T,Su B.Harnessing nanotopography to enhance osseointegration of clinical orthopedic titanium implants-an in vitro and in vivo analysis.Front Bioeng Biotechnol2018;6:44 PMCID:PMC5905351

[133] Luo J,Gao X.TiO₂ nanotopography-driven osteoblast adhesion through coulomb’s force evolution.ACS Appl Mater Interfaces2022;14:34400-14 PMCID:PMC9354007

[134] Alves-Rezende MCR,De Oliveira Limírio JPJ,Limírio PHJO.The role of TiO₂ nanotube surface on osseointegration of titanium implants: biomechanical and histological study in rats.Microsc Res Technol2020;83:817-23

[135] Long EG,Gallagher MB,Brown JL.Human mesenchymal stem cell morphology, migration, and differentiation on micro and nano-textured titanium.Bioact Mater2019;4:249-55 PMCID:PMC6812408

[136] Vasita R.Nanofibers and their applications in tissue engineering.Int J Nanomed2006;1:15-30 PMCID:PMC2426767

[137] Schieber R,Hans M.Direct laser interference patterning of CoCr alloy surfaces to control endothelial cell and platelet response for cardiovascular applications.Adv Healthc Mater2017;6:1700327

[138] Gonciar D,Agoston-Coldea L.Nanoparticles targeting the molecular pathways of heart remodeling and regeneration.Pharmaceutics2022;14:711 PMCID:PMC9028351

[139] Mukhopadhyay M.Immunomechanics.Nat Methods2023;20:35

[140] Cheng B,Huang G.Cellular mechanosensing of the biophysical microenvironment: a review of mathematical models of biophysical regulation of cell responses.Phys Life Rev2017;22-3:88-119 PMCID:PMC5712490

[141] Han S,Park S.Nano-biomaterials and advanced fabrication techniques for engineering skeletal muscle tissue constructs in regenerative medicine.Nano Converg2023;10:48 PMCID:PMC10590364

[142] Dong Z,Zhang H.3D printing of inherently nanoporous polymers via polymerization-induced phase separation.Nat Commun2021;12:247 PMCID:PMC7801408