Collagen-based biomaterials: recent advances on regulating cell migration and correlated biomedical applications

Abstract

Cell migration is a fundamental biological process that plays a crucial role in both physiological and pathological conditions, and is largely influenced by the complex microenvironment, particularly the extracellular matrix (ECM), a macromolecular network that governs various cellular interactions. Extensive research has established that ECM-cell interactions are critical in multiple biological processes, with some directly regulating cell migration. Among ECM components, collagens stand out as key regulators of cell movement. However, existing reviews have provided only limited perspectives on the role of collagen-based biomaterials in directing migration across different cell populations. This gap in knowledge hinders a comprehensive understanding of collagen’s full potential. Drawing from systematic literature and our ongoing research, this review aims to summarize advancements over the past five years in the application of collagen-based biomaterials for modulating cell migration. The discussion primarily focuses on three pivotal cell types: stem cells, immune cells, and cancer cells. By shedding light on the functions, mechanisms, and therapeutic potential of collagen in cell migration, this review will contribute to the development of innovative collagen-based biomaterials with applications in wound healing and tissue regeneration.

Keywords

Collagen / Cell migration / Stem cells / Immune cells / Cancer cells / Biological Sciences / Biochemistry and Cell Biology

References

[1] SherwoodDR. Basement membrane remodeling guides cell migration and cell morphogenesis during development. Curr Opin Cell Biol, 2021, 72: 19-27.

[2] BaeyensAA, SchwabSR. Finding a way out: S1P signaling and immune cell migration. Annu Rev Immunol, 2020, 38: 759-784.

[3] LiuJ, ZhangX, ChengY, CaoX. Dendritic cell migration in inflammation and immunity. Cell Mol Immunol, 2021, 18112461-2471.

[4] LuoR, DaiJ, ZhangJ, LiZ. Accelerated skin wound healing by electrical stimulation. Adv Healthcare Mater, 2021, 10162100557.

[5] NovikovNM, ZolotaryovaSY, GautreauAM, DenisovEV. Mutational drivers of cancer cell migration and invasion. Br J Cancer, 2021, 1241102-114.

[6] WeissF, LauffenburgerD, FriedlP. Towards targeting of shared mechanisms of cancer metastasis and therapy resistance. Nat Rev Cancer, 2022, 223157-173.

[7] SenGuptaS, ParentCA, BearJE. The principles of directed cell migration. Nat Rev Mol Cell Biol, 2021, 228529-547.

[8] ChangC-Y, PearceG, BetaneliV, KapustsenkaT, HosseiniK, Fischer-FriedrichE, CorbeilD, KarbanováJ, TaubenbergerA, DahnckeB. The F-actin bundler SWAP-70 promotes tumor metastasis. Life Sci Alliance, 2024, 78e202302307.

[9] McGarryDJ, ArmstrongG, CastinoG, MasonS, ClarkW, ShawR, McGarryL, BlythK, OlsonMF. MICAL1 regulates actin cytoskeleton organization, directional cell migration and the growth of human breast cancer cells as orthotopic xenograft tumours. Cancer Lett, 2021, 519: 226-236.

[10] PasaperaAM, HeisslerSM, EtoM, NishimuraY, FischerRS, ThiamHR, WatermanCM. MARK2 regulates directed cell migration through modulation of myosin II contractility and focal adhesion organization. Curr Biol, 2022, 32122704-2718.

[11] YaoJ, LiG, JiaoY, ZhengY, LiuY, WangG, ZhouL, ZhangH, ZhangX, ShuaiJ. Biological gel-based microchamber array for tumor cell proliferation and migration studies in well-controlled biochemical gradients. Lab Chip, 2021, 21153004-3018.

[12] ZhangH, LinF, HuangJ, XiongC. Anisotropic stiffness gradient-regulated mechanical guidance drives directional migration of cancer cells. Acta Biomater, 2020, 106: 181-192.

[13] De BellyH, PaluchEK, ChalutKJ. Interplay between mechanics and signalling in regulating cell fate. Nat Rev Mol Cell Biol, 2022, 237465-480.

[14] AdebowaleK, GongZ, HouJC, WisdomKM, GarbettD, LeeH-P, NamS, MeyerT, OddeDJ, ShenoyVB. Enhanced substrate stress relaxation promotes filopodia-mediated cell migration. Nat Mater, 2021, 2091290-1299.

[15] ChenL, YuQ, JiaY, XuM, WangY, WangJ, WenT, WangL. Micro-and-nanometer topological gradient of block copolymer fibrous scaffolds towards region-specific cell regulation. J Colloid Interface Sci, 2022, 606: 248-260.

[16] ZhangY, WangX, ZhangY, LiuY, WangD, YuX, WangH, BaiZ, JiangY-C, LiX. Endothelial cell migration regulated by surface topography of poly (ε-caprolactone) nanofibers. ACS Biomater Sci Eng, 2021, 7104959-4970.

[17] ZhongJ, YangY, LiaoL, ZhangC. Matrix stiffness-regulated cellular functions under different dimensionalities. Biomater Sci, 2020, 8102734-2755.

[18] YiB, XuQ, LiuW. An overview of substrate stiffness guided cellular response and its applications in tissue regeneration. Bioactive Mater, 2022, 15: 82-102.

[19] ZhaoX, JinL, ShiH, TongW, GorinD, KotelevtsevY, MaoZ. Recent advances of designing dynamic surfaces to regulate cell adhesion. Colloid Interface Sci Commun, 2020, 35: 100249.

[20] KlosA, SedaoX, ItinaTE, Helfenstein-DidierC, DonnetC, PeyrocheS, VicoL, GuignandonA, DumasV. Ultrafast laser processing of nanostructured patterns for the control of cell adhesion and migration on titanium alloy. Nanomaterials, 2020, 105864.

[21] WuT, XueJ, XiaY. Engraving the surface of electrospun microfibers with nanoscale grooves promotes the outgrowth of neurites and the migration of schwann cells. Angew Chem Int Ed, 2020, 593615626-15632.

[22] TabdanovED, Rodríguez-MercedNJ, Cartagena-RiveraAX, PuramVV, CallawayMK, EnsmingerEA, PomeroyEJ, YamamotoK, LahrWS, WebberBR. Engineering T cells to enhance 3D migration through structurally and mechanically complex tumor microenvironments. Nat Commun, 2021, 1212815.

[23] LiuQ, ZhengS, YeK, HeJ, ShenY, CuiS, HuangJ, GuY, DingJ. Cell migration regulated by RGD nanospacing and enhanced under moderate cell adhesion on biomaterials. Biomaterials, 2020, 263: 120327.

[24] Yan S, Qian Y, Haghayegh M, Xia Y, Yang S, Cao R, Zhu M. Electrospun organic/inorganic hybrid nanofibers for accelerating wound healing: a review. Journal of Materials Chemistry B 2024.

[25] LiuQ, KimYJ, ImGB, ZhuJ, WuY, LiuY, BhangSH. Inorganic nanoparticles applied as functional therapeutics. Adv Func Mater, 2021, 31122008171.

[26] ChenQ, ZhangD, ZhangW, ZhangH, ZouJ, ChenM, LiJ, YuanY, LiuR. Dual mechanism β-amino acid polymers promoting cell adhesion. Nat Commun, 2021, 121562.

[27] ZhangX, van VeenS, HadaviD, ZhaoY, MohrenR, HabibovićP, HoningM, AlbertazziL, van RijtS. DNA nanoparticle based 2D biointerface to study the effect of dynamic RGD presentation on stem cell adhesion and migration. Small, 2024, 20: 2311402.

[28] LiF, LiuY, DongY, ChuY, SongN, YangD. Dynamic assembly of DNA nanostructures in living cells for mitochondrial interference. J Am Chem Soc, 2022, 144104667-4677.

[29] CarrowJK, SinghKA, JaiswalMK, RamirezA, LokhandeG, YehAT, SarkarTR, SinghI, GaharwarAK. Photothermal modulation of human stem cells using light-responsive 2D nanomaterials. Proc Natl Acad Sci, 2020, 1172413329-13338.

[30] WalmaDAC, YamadaKM. The extracellular matrix in development. Development, 2020, 14710dev175596.

[31] HuangJ, ZhangL, WanD, ZhouL, ZhengS, LinS, QiaoY. Extracellular matrix and its therapeutic potential for cancer treatment. Signal Transduct Target Ther, 2021, 61153.

[32] SutherlandTE, DyerDP, AllenJE. The extracellular matrix and the immune system: a mutually dependent relationship. Science, 2023, 3796633eabp8964.

[33] MillerAE, HuP, BarkerTH. Feeling things out: Bidirectional signaling of the cell–ECM interface, implications in the mechanobiology of cell spreading, migration, proliferation, and differentiation. Adv Healthcare Mater, 2020, 981901445.

[34] YamadaKM, DoyleAD, LuJ. Cell-3D matrix interactions: recent advances and opportunities. Trends Cell Biol, 2022, 3210883-895.

[35] KanchanawongP, CalderwoodDA. Organization, dynamics and mechanoregulation of integrin-mediated cell-ECM adhesions. Nat Rev Mol Cell Biol, 2023, 242142-161.

[36] ZhuL, XiaoYX, ZhuHL, ZuoL, SunC, LeiMA, ZhangJT, WeiBM, QiCB, WangHB. Fish-derived collagen: a promising biomaterial for regulating the migration behavior of MCF-7 cells. Adv Eng Mater, 2024, 26102400415.

[37] LiuX, ZhengC, LuoX, WangX, JiangH. Recent advances of collagen-based biomaterials: multi-hierarchical structure, modification and biomedical applications. Mater Sci Eng C, 2019, 99: 1509-1522.

[38] ZhengM, WangX, ChenY, YueO, BaiZ, CuiB, JiangH, LiuX. A review of recent progress on collagen-based biomaterials. Adv Healthcare Mater, 2023, 12162202042.

[39] SubhanF, HussainZ, TauseefI, ShehzadA, WahidF. A review on recent advances and applications of fish collagen. Crit Rev Food Sci Nutr, 2021, 6161027-1037.

[40] TangC, ZhouK, ZhuY, ZhangW, XieY, WangZ, ZhouH, YangT, ZhangQ, XuB. Collagen and its derivatives: From structure and properties to their applications in food industry. Food Hydrocolloids, 2022, 131: 107748.

[41] YuX, ZhangH, MiaoY, XiongS, HuY. Recent strategies of collagen-based biomaterials for cartilage repair: from structure cognition to function endowment. J Leather Sci Eng, 2022, 4111.

[42] JiangC, CentonzeA, SongY, ChrisnandyA, TikaE, RezakhaniS, ZahediZ, BouvencourtG, DuboisC, Van KeymeulenA, et al. . Collagen signaling and matrix stiffness regulate multipotency in glandular epithelial stem cells in mice. Nat Commun, 2024, 15110482.

[43] ElangoJ, HouC, BaoB, WangS, ValMSD, WenhuiW. The molecular interaction of collagen with cell receptors for biological function. Polymers, 2022, 14: 876.

[44] XuC, XiaoX, HuW, ZhuL, KouH, ZhangJ, WeiB, WangH. Ultrahigh pressure field: A friendly pathway for regulating the cellular adhesion and migration capacity of collagen. Int J Biol Macromol, 2024, 257: 127864.

[45] WangY, FanZ, LiQ, LuJ, WangX, ZhangJ, WuZ. Construction of a myocardial patch with mesenchymal stem cells and poly (CL-co-TOSUO)/collagen scaffolds for myocardial infarction repair by coaxial electrospinning. J Mater Chem B, 2023, 11224980-4990.

[46] DeweyMJ, CollinsAJ, TiffanyA, BarnhouseVR, LuC, KolliopoulosV, MutrejaI, HickokNJ, HarleyBA. Evaluation of bacterial attachment on mineralized collagen scaffolds and addition of manuka honey to increase mesenchymal stem cell osteogenesis. Biomaterials, 2023, 294: 122015.

[47] NogueiraLFB, CruzMAE, de MeloMT, ManigliaBC, CaroleoF, PaolesseR, LopesHB, BelotiMM, CiancagliniP, RamosAP. Collagen/κ-carrageenan-based scaffolds as biomimetic constructs for in vitro bone mineralization dtudies. Biomacromol, 2023, 2431258-1266.

[48] ZhangY, LiZ, GuoB, WangQ, ChenL, ZhuL, ZhangT, WangR, LiW, LuoD, et al. . A zinc oxide nanowire-modified mineralized collagen scaffold promotes infectious bone regeneration. Small, 2024, 20192309230.

[49] ShiS, WangL, SongC, YaoL, XiaoJ. Recent progresses of collagen dressings for chronic skin wound healing. Collagen Leather, 2023, 5131.

[50] LiaoW, YangD, XuZ, ZhaoL, MuC, LiD, GeL. Antibacterial collagen-based nanocomposite dressings for promoting infected wound healing. Adv Healthcare Mater, 2023, 12152203054.

[51] PassosJS, LopesLB, PanitchA. Collagen-binding nanoparticles for paclitaxel encapsulation and breast cancer treatment. ACS Biomater Sci Eng, 2023, 9126805-6820.

[52] NagarN, NaiduG, MishraA, PoluriKM. Protein-based nanocarriers and nanotherapeutics for infection and inflammation. J Pharmacol Exp Ther, 2024, 388191-109.

[53] LiM, LiM, LiX, ShaoW, PeiX, DongR, RenH, JiaL, LiS, MaW. Preparation, characterization and ex vivo skin permeability evaluation of type I collagen-loaded liposomes. Int J Nanomed, 2023, 18: 1853-1871.

[54] KimD, LeeS, ShinD, HongS, ParkS, ChoeJ, SeoJ, LeeJB, ChoiI. Photothermally modulated intracellular delivery of therapeutic proteins using gold-collagen hybrid nanoparticles. ACS Mater Lett, 2024, 62409-417.

[55] ZuoX, XiaoY, YangJ, HeY, HeY, LiuK, ChenX, GuoJ. Engineering collagen-based biomaterials for cardiovascular medicine. Collagen and Leather, 2024, 6133.

[56] Costa AlmeidaCEP, ReisL, CarvalhoL, Costa AlmeidaCM. Collagen implant with gentamicin sulphate reduces surgical site infection in vascular surgery: a prospective cohort study. Int J Surg, 2014, 12101100-1104.

[57] ZhuJ, LiZ, ZouY, LuG, RoncaA, D’AmoraU, LiangJ, FanY, ZhangX, SunY. Advanced application of collagen-based biomaterials in tissue repair and restoration. J Leather Sci Eng, 2022, 4130.

[58] LiuC, NguyenRY, PizzurroGA, ZhangX, GongX, MartinezAR, MakM. Self-assembly of mesoscale collagen architectures and applications in 3D cell migration. Acta Biomater, 2023, 155: 167-181.

[59] MeyerN, BaxDV, BeckJ, CameronRE, BestSM. Adjusting the physico-chemical properties of collagen scaffolds to accommodate primary osteoblasts and endothelial cells. Regen Biomater, 2023, 10: rbad015.

[60] YangC, WangX, XieR, ZhangY, XiaT, LuY, YeF, ZhangP, CaoT, XuY. Dynamically reconstructed collagen fibers for transmitting mechanical signals to assist macrophages tracing breast cancer cells. Adv Func Mater, 2023, 3392211807.

[61] WeiZ, LiuJ, JiaY, LeiM, ZhangS, XiP, MaY, ZhangM, MaJ, WangL. Fiber microarchitecture in interpenetrating collagen-alginate hydrogel with tunable mechanical plasticity regulates tumor cell migration. Adv Healthcare Mater, 2023, 12292301586.

[62] NguyenRY, CabralAT, Rossello-MartinezA, ZulliA, GongX, ZhangQ, YanJ, MakM. Tunable mesoscopic collagen island architectures modulate stem cell behavior. Adv Mater, 2023, 35162207882.

[63] CuiY, LeeP, ReardonJJ, WangA, LynchS, OteroJJ, SizemoreG, WinterJO. Evaluating glioblastoma tumour sphere growth and migration in interaction with astrocytes using 3D collagen-hyaluronic acid hydrogels. J Mater Chem B, 2023, 11245442-5459.

[64] SapudomJ, AlatoomA, MohamedWK, Garcia-SabatéA, McBainI, NasserRA, TeoJC. Dendritic cell immune potency on 2D and in 3D collagen matrices. Biomater Sci, 2020, 8185106-5120.

[65] LiuZ, WanX, WangZL, LiL. Electroactive biomaterials and systems for cell fate determination and tissue regeneration: design and applications. Adv Mater, 2021, 33322007429.

[66] CaiB, LinD, LiY, WangL, XieJ, DaiT, LiuF, TangM, TianL, YuanY. N2-polarized neutrophils guide bone mesenchymal stem cell recruitment and initiate bone regeneration: a missing piece of the bone regeneration puzzle. Adv Sci, 2021, 8192100584.

[67] DongR, BaiY, DaiJ, DengM, ZhaoC, TianZ, ZengF, LiangW, LiuL, DongS. Engineered scaffolds based on mesenchymal stem cells/preosteoclasts extracellular matrix promote bone regeneration. J Tissue Eng, 2020, 11: 2041731420926918.

[68] GreenhalghAD, DavidS, BennettFC. Immune cell regulation of glia during CNS injury and disease. Nat Rev Neurosci, 2020, 213139-152.

[69] GaneshK, MassaguéJ. Targeting metastatic cancer. Nat Med, 2021, 27134-44.

[70] GerstbergerS, JiangQ, GaneshK. Metastasis. Cell, 2023, 18681564-1579.

[71] XueJ, WuT, QiuJ, RutledgeS, TanesML, XiaY. Promoting cell migration and neurite extension along uniaxially aligned nanofibers with biomacromolecular particles in a density gradient. Adv Func Mater, 2020, 30402002031.

[72] SchwabA, HélaryC, RichardsRG, AliniM, EglinD, d'EsteM. Tissue mimetic hyaluronan bioink containing collagen fibers with controlled orientation modulating cell migration and alignment. Mater Today Bio, 2020, 7: 100058.

[73] DavaaG, HongJY, LeeJH, KimMS, BuitragoJO, LiYM, LeeHH, HanDW, LeongKW, HyunJK. Delivery of induced neural stem cells through mechano-tuned silk-collagen hydrogels for the recovery of contused spinal cord in rats. Adv Healthcare Mater, 2023, 1272201720.

[74] PopovC, RadicT, HaastersF, PrallWC, AszodiA, GullbergD, SchiekerM, DochevaD. Integrins α2β1 and α11β1 regulate the survival of mesenchymal stem cells on collagen I. Cell Death Dis, 2011, 27e186-e186.

[75] LundAW, StegemannJP, PlopperGE. Mesenchymal stem cells sense three dimensional type I collagen through discoidin domain receptor 1. Open Stem Cell J, 2009, 1: 40-53

[76] LeeJ, KimS-E, MoonD, DohJ. A multilayered blood vessel/tumor tissue chip to investigate T cell infiltration into solid tumor tissues. Lab Chip, 2021, 21112142-2152.

[77] SadjadiZ, ZhaoR, HothM, QuB, RiegerH. Migration of cytotoxic T lymphocytes in 3D collagen matrices. Biophys J, 2020, 119112141-2152.

[78] HachehoucheLN, ChetouiN, AoudjitF. Implication of discoidin domain receptor 1 in T cell migration in three-dimensional collagen. Mol Immunol, 2010, 4791866-1869.

[79] KaltenbachL, MartzloffP, BambachSK, AizaraniN, MihlanM, GavrilovA, GlaserKM, StecherM, ThünauerR, ThiriotA, et al. . Slow integrin-dependent migration organizes networks of tissue-resident mast cells. Nat Immunol, 2023, 246915-924.

[80] BeunkL, WenN, van HelvertS, BekkerB, RanL, KangR, PaulatT, SygaS, DeutschA, FriedlP. Cell jamming in a collagen-based interface assay is tuned by collagen density and proteolysis. J Cell Sci, 2023.

[81] MosierJA, FabianoED, LudolphCM, WhiteAE, Reinhart-KingCA. Confinement primes cells for faster migration by polarizing active mitochondria. Nanoscale Adv, 2024, 61209-220.

[82] BornLJ, ChangKH, ShoureshiP, LayF, BengaliS, HsuATW, AbadchiSN, HarmonJW, JaySM. HOTAIR-loaded mesenchymal stem/stromal cell extracellular vesicles enhance angiogenesis and wound healing. Adv Healthcare Mater, 2022, 1152002070.

[83] ChenS, WangH, SuY, JohnJV, McCarthyA, WongSL, XieJ. Mesenchymal stem cell-laden, personalized 3D scaffolds with controlled structure and fiber alignment promote diabetic wound healing. Acta Biomater, 2020, 108: 153-167.

[84] ShangF, YuY, LiuS, MingL, ZhangY, ZhouZ, ZhaoJ, JinY. Advancing application of mesenchymal stem cell-based bone tissue regeneration. Bioactive Mater, 2021, 63666-683.

[85] FuX, LiuG, HalimA, JuY, LuoQ, SongG. Mesenchymal stem cell migration and tissue repair. Cells, 2019, 88784.

[86] BaiZ, HuK, ShouZ, YuJ, MengH, ZhouH, ChenL, YuT, LuR, LiN. Layer-by-layer assembly of procyanidin and collagen promotes mesenchymal stem cell proliferation and osteogenic differentiation in vitro and in vivo. Regen Biomater, 2023, 10: rbac107.

[87] XiaH, LiX, GaoW, FuX, FangRH, ZhangL, ZhangK. Tissue repair and regeneration with endogenous stem cells. Nat Rev Mater, 2018, 37174-193.

[88] WangT, HuangQ, RaoZ, LiuF, SuX, ZhaiX, MaJ, LiangY, QuanD, LiaoG. Injectable decellularized extracellular matrix hydrogel promotes salivary gland regeneration via endogenous stem cell recruitment and suppression of fibrogenesis. Acta Biomater, 2023, 169: 256-272.

[89] DaiW, LiuQ, LiS, GaoY, FengC, GuoL, XiaoY, LinH, FanY, ZhangX. Functional injectable hydrogel with spatiotemporal sequential release for recruitment of endogenous stem cells and in situ cartilage regeneration. J Mater Chem B, 2023, 11184050-4064.

[90] SunY, KongJ, GeX, MaoM, YuH, WangY. An antisense oligonucleotide-loaded blood-brain barrier penetrable nanoparticle mediating recruitment of endogenous neural stem cells for the treatment of parkinson’s disease. ACS Nano, 2023, 1754414-4432.

[91] WeberEW, MausMV, MackallCL. The emerging landscape of immune cell therapies. Cell, 2020, 181146-62.

[92] ThorssonV, GibbsDL, BrownSD, WolfD, BortoneDS, YangT-HO, Porta-PardoE, GaoGF, PlaisierCL, EddyJA. The immune landscape of cancer. Immunity, 2018, 484812-830.

[93] ZhangY, ZhangZ. The history and advances in cancer immunotherapy: understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell Mol Immunol, 2020, 178807-821.

[94] BhagwatAS, TorresL, ShestovaO, ShestovM, MellorsPW, FisherHR, FarookiSN, FrostBF, LokenMR, GaymonAL, et al. . Cytokine-mediated CAR T therapy resistance in AML. Nat Med, 2024, 30123697-3708.

[95] IrvineDJ, MausMV, MooneyDJ, WongWW. The future of engineered immune cell therapies. Science, 2022, 3786622853-858.

[96] SternerRC, SternerRM. CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J, 2021, 11469.

[97] DingY, WangY, HuQ. Recent advances in overcoming barriers to cell-based delivery systems for cancer immunotherapy. Exploration, 2022, 2: 20210106.

[98] ZhouY, ChenX, CaoJ, GaoH. Overcoming the biological barriers in the tumor microenvironment for improving drug delivery and efficacy. J Mater Chem B, 2020, 8316765-6781.

[99] LiuJ, ZhangJ, GaoY, JiangY, GuanZ, XieY, HuJ, ChenJ. Barrier permeation and improved nanomedicine delivery in tumor microenvironments. Cancer Letters, 2023, 562: 216166.

[100] Nicolas-BoludaA, VaqueroJ, VimeuxL, GuilbertT, BarrinS, Kantari-MimounC, PonzoM, RenaultG, DeptulaP, PogodaK, et al. . Tumor stiffening reversion through collagen crosslinking inhibition improves T cell migration and anti-PD-1 treatment. eLife, 2021, 10: e58688.

[101] XiaoZ, ToddL, HuangL, Noguera-OrtegaE, LuZ, HuangL, KoppM, LiY, PattadaN, ZhongW. Desmoplastic stroma restricts T cell extravasation and mediates immune exclusion and immunosuppression in solid tumors. Nat Commun, 2023, 1415110.

[102] KohC-H, LeeS, KwakM, KimB-S, ChungY. CD8 T-cell subsets: heterogeneity, functions, and therapeutic potential. Exp Mol Med, 2023, 55112287-2299.

[103] GilesJR, GlobigA-M, KaechSM, WherryEJ. CD8+ T cells in the cancer-immunity cycle. Immunity, 2023, 56102231-2253.

[104] ElangoJ, HouC, BaoB, WangS, ValMSD, WenhuiJE. The molecular interaction of collagen with cell receptors for biological function. Polymers, 2022, 145876.

[105] GubatanJ, KeyashianK, RubinSJS, WangJ, BuckmanCA, SinhaS. Anti-integrins for the treatment of inflammatory bowel disease: current evidence and perspectives. Clin Exp Gastroenterol, 2021, 14: 333-342.

[106] MaityD, BeraK, LiY, GeZ, NiQ, KonstantopoulosK, SunSX. Extracellular hydraulic resistance enhances cell migration. Adv Sci, 2022, 9292200927.

[107] BeraK, KiepasA, GodetI, LiY, MehtaP, IfemembiB, PaulCD, SenA, SerraSA, StoletovK. Extracellular fluid viscosity enhances cell migration and cancer dissemination. Nature, 2022, 6117935365-373.

[108] MehtaP, RahmanZ, Ten DijkeP, BoukanyPE. Microfluidics meets 3D cancer cell migration. Trends Cancer, 2022, 88683-697.

[109] Ibáñez GasparV, McMorrowT. The curcuminoid ef24 in combination with trail reduces human renal cancer cell migration by decreasing mmp-2/mmp-9 activity through a reduction in h2o2. Int J Mol Sci, 2023, 2421043.

[110] LiC, ZhengZ, WuX, XieQ, LiuP, HuY, ChenM, LiuL, ZhaoW, ChenL. Stiff matrix induced srGAP2 tension gradients control migration direction in triple-negative breast cancer. Theranostics, 2023, 13159.

[111] BaschieriF, IllandA, BarbazanJ, ZajacO, HenonC, LoewD, DingliF, VignjevicDM, Lévêque-FortS, MontagnacG. Fibroblasts generate topographical cues that steer cancer cell migration. Sci Adv, 2023, 933eade2120.

[112] MaoB-H, ThiKMN, TangM-J, KammRD, TuT-Y. The interface stiffness and topographic feature dictate interfacial invasiveness of cancer spheroids. Biofabrication, 2023, 151015023.

[113] XuK, FeiW, HuoZ, WangS, LiY, YangG, HongY. PDCD10 promotes proliferation, migration, and invasion of osteosarcoma by inhibiting apoptosis and activating EMT pathway. Cancer Med, 2023, 1221673-1684.

[114] GaoZ-W, LiuC, YangL, ChenH-C, YangL-F, ZhangH-Z, DongK. CD73 severed as a potential prognostic marker and promote lung cancer cells migration via enhancing EMT progression. Front Genet, 2021, 12: 728200.

[115] LinX, ZhuangS, ChenX, DuJ, ZhongL, DingJ, WangL, YiJ, HuG, TangG. lncRNA ITGB8-AS1 functions as a ceRNA to promote colorectal cancer growth and migration through integrin-mediated focal adhesion signaling. Mol Ther, 2022, 302688-702.

[116] HuangW, YanY, LiuY, LinM, MaJ, ZhangW, DaiJ, LiJ, GuoQ, ChenH. Exosomes with low miR-34c-3p expression promote invasion and migration of non-small cell lung cancer by upregulating integrin α2β1. Signal Transduct Target Ther, 2020, 5139.

[117] SzulczewskiJM, InmanDR, ProestakiM, NotbohmJ, BurkelBM, PonikSM. Directional cues in the tumor microenvironment due to cell contraction against aligned collagen fibers. Acta Biomater, 2021, 129: 96-109.

[118] PapanicolaouM, ParkerAL, YamM, FilipeEC, WuSZ, ChittyJL, WyllieK, TranE, MokE, NadaliniA, et al. . Temporal profiling of the breast tumour microenvironment reveals collagen XII as a driver of metastasis. Nat Commun, 2022, 1314587.

[119] SasakiN, AsanoY, SorayamaY, KamimuraC, KitanoS, IrieS, KatayamaR, ShimodaH, MatsusakiM. Promoting biological similarity by collagen microfibers in 3D colorectal cancer-stromal tissue: replicating mechanical properties and cancer stem cell markers. Acta Biomater, 2024, 1851161-172.

[120] GonçalvesIG, Garcia-AznarJM. Extracellular matrix density regulates the formation of tumour spheroids through cell migration. PLoS Comput Biol, 2021, 172e1008764.

[121] VasudevanJ, LimCT, FernandezJG. Cell migration and breast cancer metastasis in biomimetic extracellular matrices with independently tunable stiffness. Adv Func Mater, 2020, 30492005383.

[122] WangM, YangY, HanL, HanS, LiuN, XuF, LiF. Effect of three-dimensional ECM stiffness on cancer cell migration through regulating cell volume homeostasis. Biochem Biophys Res Commun, 2020, 5283459-465.

[123] FischerRS, SunX, BairdMA, HourwitzMJ, SeoBR, PasaperaAM, MehtaSB, LosertW, FischbachC, FourkasJT. Contractility, focal adhesion orientation, and stress fiber orientation drive cancer cell polarity and migration along wavy ECM substrates. Proc Natl Acad Sci, 2021, 11822e2021135118.

[124] NilandS, RiscanevoAX, EbleJA. Matrix metalloproteinases shape the tumor microenvironment in cancer progression. Int J Mol Sci, 2021, 231146.

[125] WinklerJ, Abisoye-OgunniyanA, MetcalfKJ, WerbZ. Concepts of extracellular matrix remodelling in tumour progression and metastasis. Nat Commun, 2020, 1115120.

[126] ZhuL, XiaoY-X, ZhuH-L, ZuoL, SunC, LeiM-A, ZhangJ-T, WeiB-M, QiC-B, WangH-B. Fish derived collagen: a promising biomaterial for regulating the migration behavior of MCF-7 cells. Adv Eng Mater, 2024, 26: 2400415.

[127] LafitteM, SirventA, RocheS. Collagen kinase receptors as potential therapeutic targets in metastatic colon cancer. Front Oncol, 2020.

[128] GaoH, ChakrabortyG, ZhangZ, AkalayI, GadiyaM, GaoY, SinhaS, HuJ, JiangC, AkramM, et al. . Multi-organ site metastatic reactivation mediated by non-canonical discoidin domain receptor 1 signaling. Cell, 2016, 166147-62.

[129] HansenC, GreengardP, NairnAC, AnderssonT, VogelWF. Phosphorylation of DARPP-32 regulates breast cancer cell migration downstream of the receptor tyrosine kinase DDR1. Exp Cell Res, 2006, 312204011-4018.

[130] JeitanyM, LeroyC, TostiP, LafitteM, Le GuetJ, SimonV, BonenfantD, RobertB, GrilletF, MolleviC. Inhibition of DDR 1-BCR signalling by nilotinib as a new therapeutic strategy for metastatic colorectal cancer. EMBO Mol Med, 2018, 104e7918.

[131] Nguyen-NgocK-V, CheungKJ, BrenotA, ShamirER, GrayRS, HinesWC, YaswenP, WerbZ, EwaldAJ. ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc Natl Acad Sci, 2012, 10939E2595-E2604.

[132] PatwardhanS, MahadikP, ShettyO, SenS. ECM stiffness-tuned exosomes drive breast cancer motility through thrombospondin-1. Biomaterials, 2021, 279: 121185.

[133] YuanZ, LiY, ZhangS, WangX, DouH, YuX, ZhangZ, YangS, XiaoM. Extracellular matrix remodeling in tumor progression and immune escape: from mechanisms to treatments. Mol Cancer, 2023, 22148.

[134] WeiY, WangK, LuoS, LiF, ZuoX, FanC, LiQ. Programmable DNA hydrogels as artificial extracellular matrix. Small, 2022, 18362107640.

[135] ÁlvarezZ, OrtegaJA, SatoK, SasselliIR, Kolberg-EdelbrockAN, QiuR, MarshallKA, NguyenTP, SmithCS, QuinlanKA. Artificial extracellular matrix scaffolds of mobile molecules enhance maturation of human stem cell-derived neurons. Cell Stem Cell, 2023, 302219-238.

[136] ZhengD-W, HongS, ZhangQ-L, DongX, PanP, SongW-F, SongW, ChengS-X, ZhangX-Z. Controllable gelation of artificial extracellular matrix for altering mass transport and improving cancer therapies. Nat Commun, 2020, 1114907.

[137] BlumJC, SchenckTL, BirtA, GiuntaRE, WiggenhauserPS. Artificial decellularized extracellular matrix improves the regenerative capacity of adipose tissue derived stem cells on 3D printed polycaprolactone scaffolds. J Tissue Eng, 2021, 12: 20417314211022242.

[138] WuH, ZhangR, HuB, HeY, ZhangY, CaiL, WangL, WangG, HouH, QiuX. A porous hydrogel scaffold mimicking the extracellular matrix with swim bladder derived collagen for renal tissue regeneration. Chin Chem Lett, 2021, 32123940-3947.

[139] AmorimS, ReisCA, ReisRL, PiresRA. Extracellular matrix mimics using hyaluronan-based biomaterials. Trends Biotechnol, 2021, 39190-104.

[140] IndrianiS, BenjakulS, KishimuraH, KarnjanapratumS, NalinanonS. Impact of extraction condition on the yield and molecular characteristics of collagen from Asian bullfrog (Rana tigerina) skin. LWT, 2022, 162: 113439.

[141] JafariH, ListaA, SiekapenMM, Ghaffari-BohlouliP, NieL, AlimoradiH, ShavandiA. Fish collagen: extraction, characterization, and applications for biomaterials engineering. Polymers, 2020, 12102230.

[142] RajabimashhadiZ, GalloN, SalvatoreL, LionettoF. Collagen derived from fish industry waste: progresses and challenges. Polymers, 2023, 153544.

[143] FurtadoM, ChenL, ChenZ, ChenA, CuiW. Development of fish collagen in tissue regeneration and drug delivery. Eng Regen, 2022, 33217-231

[144] LeonardAR, CummingMH, AliMA, CabralJD. Fish collagen cross-linking strategies to improve mechanical and bioactive capabilities for tissue engineering and regenerative medicine. Adv Func Mater, 2024, 34452405335.

[145] ChenQ, PeiY, TangK, Albu-KayaMG. Structure, extraction, processing, and applications of collagen as an ideal component for biomaterials-a review. Collagen Leather, 2023, 5120.

[146] ChangP, GuoK, LiS, WangH, TangM. In situ sodium chloride cross-linked fish skin collagen scaffolds for functional hemostasis materials. Small, 2024, 20112208001.

[147] HuangD, LiY, MaZ, LinH, ZhuX, XiaoY, ZhangX. Collagen hydrogel viscoelasticity regulates MSC chondrogenesis in a ROCK-dependent manner. Sci Adv, 2023, 96eade9497.

[148] KongB, SunL, LiuR, ChenY, ShangY, TanH, ZhaoY, SunL. Recombinant human collagen hydrogels with hierarchically ordered microstructures for corneal stroma regeneration. Chem Eng J, 2022, 428: 131012.

[149] LiZ, DuT, RuanC, NiuX. Bioinspired mineralized collagen scaffolds for bone tissue engineering. Bioactive Mater, 2021, 651491-1511.

[150] ZhangY, LiZ, GuoB, WangQ, ChenL, ZhuL, ZhangT, WangR, LiW, LuoD. A zinc axide nanowire-modified mineralized collagen scaffold promotes infectious bone regeneration. Small, 2024, 20192309230.

[151] ShiW, MirzaS, KussM, LiuB, HartinA, WanS, KongY, MohapatraB, KrishnanM, BandH. Embedded bioprinting of breast tumor cells and organoids using low-concentration collagen-based bioinks. Adv Healthcare Mater, 2023, 12262300905.

[152] GaoZ, LiuX, ZhaoH, XiaS, LiuW, BaiH, LvF, ZhengX, HuangY, GuQ. Synthesis of easily-processable collagen bio-inks using ionic liquid for 3D bioprinted liver tissue models with branched vascular networks. Sci China Chem, 2023, 6651489-1499.

[153] XuC, HuW, XiaoX, ZhuL, ZhangJ, WeiB, WangH. Effects of γ-ray irradiation on the molecular structure of collagen in different product forms. New J Chem, 2023, 47104964-4972.

[154] CrockerDB, HeringTM, AkkusO, OestME, RimnacCM. Dose-dependent effects of gamma radiation sterilization on the collagen matrix of human cortical bone allograft and its influence on fatigue crack propagation resistance. Cell Tissue Bank, 2024, 25: 735.

[155] FengY, NiuL, SunC, TuJ, YuL, XiaoJ. Collagen hydrolysates improve the efficiency of sodium alginate-encapsulated tea polyphenols in beads and the storage stability after commercial sterilization. Int J Biol Macromol, 2023, 231: 123314.

[156] KaripidouN, TzavellasA-N, PetrouN, KatrilakaC, TheodorouK, PitouM, TsiridisE, Choli-PapadopoulouT, AggeliA. Comparative studies of sterilization processes for sensitive medical nano-devices. Mater Today Proc, 2023, 93: 1-8.

[157] De WitR, Van DisD, BertrandM, TiemessenD, SiddiqiS, OosterwijkE, VerhagenA. Scaffold-based tissue engineering: supercritical carbon dioxide as an alternative method for decellularization and sterilization of dense materials. Acta Biomater, 2023, 155: 323-332.

[158] Srinivasan P, Hsieh D-J. Supercritical carbon dioxide facilitated collagen scaffold production for tissue engineering. In Collagen Biomaterials, IntechOpen, 2022.

[159] GrandisRAD, MiottoLN, GenaroLE, Migliatti PolliL, PlepisAMDG, RodriguesFT, MartinsVDCA, Pereira FranchiL, Scarel-CaminagaRM, de OliveiraS, CapoteT. In vitro evaluation of acellular collagen matrices derived from porcine pericardium: influence of the sterilization method on its biological properties. Materials, 2021, 14216255.

[160] ZhangC, QuG, WangQ, ZhaoY, XieY, XuS, LiR, ShenY, GongS, GaoJ. Comparative effects of in-package high pressure steam sterilization and high temperature boiling on the quality changes and shelf life of ready-to-eat sea cucumber. J Food Compos Anal, 2024, 14: 106138.

[161] AdamiakK, SionkowskaA. Current methods of collagen cross-linking. Int J Biol Macromol, 2020, 161: 550-560.

[162] VisserD, RoggK, FuhrmannE, MarziJ, Schenke-LaylandK, HartmannH. Electrospinning of collagen: enzymatic and spectroscopic analyses reveal solvent-independent disruption of the triple-helical structure. J Mater Chem B, 2023, 11102207-2218.

[163] DelgadoLM, PanditA, ZeugolisDI. Influence of sterilisation methods on collagen-based devices stability and properties. Expert Rev Med Devices, 2014, 113305-314.

[164] Dąbrowska-GralakM, SadłoJ, GłuszewskiW, ŁyczkoK, PrzybytniakG, LewandowskaH. The combined effect of humidity and electron beam irradiation on collagen type I—implications for collagen-based devices. Mater Today Commun, 2022, 31: 103255.

[165] Van CauwenberghT, TheysE, StroeykensD, CroonenborghsB, GilletA, DeMentA, Van SchepdaelA, HaghedoorenE. The effect of gamma and ethylene oxide sterilization on a selection of active pharmaceutical ingredients for ophthalmics. J Pharm Sci, 2022, 11172011-2017.

[166] FahimiradS, FahimiradZ, SillanpääM. Efficient removal of water bacteria and viruses using electrospun nanofibers. Sci Total Environ, 2021, 751: 141673.

[167] KaushalS, PinnakaAK, SoniS, SinghalNK. Antibody assisted graphene oxide coated gold nanoparticles for rapid bacterial detection and near infrared light enhanced antibacterial activity. Sens Actuators B Chem, 2021, 329: 129141.

[168] GaoJ, GuoZ, ZhangY, LiuY, XingF, WangJ, LuoX, KongY, ZhangG. Age-related changes in the ratio of Type I/III collagen and fibril diameter in mouse skin. Regen Biomater, 2023, 10: rbac110.

[169] BeckerL, LuC-E, Montes-MojarroIA, LaylandSL, KhalilS, NsairA, DuffyGP, FendF, MarziJ, Schenke-LaylandK. Raman microspectroscopy identifies fibrotic tissues in collagen-related disorders via deconvoluted collagen type I spectra. Acta Biomater, 2023, 162: 278-291.

[170] Masson-MeyersDS, TabatabaeiF, SteinhausL, TothJM, TayebiL. Development of fibroblast/endothelial cell-seeded collagen scaffolds for in vitro prevascularization. J Biomed Mater Res B Appl Biomater, 2023, 1113633-645.

[171] WuSM, ChenF, YangXY, WuTF, SunW, YuL. Probing the interaction between metastatic breast cancer cells and osteoblasts in a thread-based breast-bone co-culture device. Lab Chip, 2023, 23122838-2853.

[172] SolbuAA, CaballeroD, DamigosS, KunduSC, ReisRL, HalaasØ, ChahalAS, StrandBL. Assessing cell migration in hydrogels: an overview of relevant materials and methods. Mater Today Bio, 2023, 18: 100537.

[173] HwangJ, KiickKL, SullivanMO. VEGF-encoding, gene-activated collagen-based matrices promote blood vessel formation and improved wound repair. ACS Appl Mater Interfaces, 2023, 151316434-16447.

[174] GharibshahianM, TorkashvandM, BavisiM, AldaghiN, AlizadehA. Recent advances in artificial intelligent strategies for tissue engineering and regenerative medicine. Skin Res Technol, 2024, 309e70016.

[175] PemmadaR, GowthamNH, XiaY, BasuB, ThomasVSharmaCP, ChandyT, ThomasV. Chapter 3-ML and AI approaches for design of tissue scaffolds. Artificial intelligence in tissue and organ regeneration, 2023CambridgeAcademic Press29-56.

[176] ZhuQ, GaoX, LeveneHB, BrownMD, GuW. Influences of nutrition supply and pathways on the degenerative patterns in human intervertebral disc. Spine, 2016, 417568.

[177] JaberiA, Monemian EsfahaniA, AghabaglouF, ParkJS, NdaoS, TamayolA, YangR. Microfluidic systems with embedded cell culture chambers for high-throughput biological assays. ACS Appl Bio Mater, 2020, 3106661-6671.

[178] YangH, ChenT, HuY, NiuF, ZhengX, SunH, ChengL, SunL. A microfluidic platform integrating dynamic cell culture and dielectrophoretic manipulation for in situ assessment of endothelial cell mechanics. Lab Chip, 2023, 23163581-3592.

Funding

Open Project Funding of Ministry-of-Education Key Laboratory for the Synthesis and Application of Organic Functional Molecules, Hubei University(KLSAOFM2314)

National Natural Science Foundation of China(22178277)

Natural Science Foundation of Hubei Province(2024AFB919)

Application Foundation Frontier Project of Wuhan Science and Technology Bureau(2019020701011478)

RIGHTS & PERMISSIONS

The Author(s)