Abstract
Articular cartilage defects are considered to be associated with the development of osteoarthritis. Research on relevant tissue regeneration is important in the treatment of osteoarthritis. The scaffolds applied in cartilage regeneration should have good histocompatibility and mechanical properties, as well as no cytotoxicity, and promote the proliferation and differentiation of seed cells. Different combinations of peptide sequences in polypeptide hydrogels endow them with unique characteristics including excellent biodegradability and accurate simulation of the extracellular matrix of chondrocytes to maintain the stability of the chondrogenic phenotype and facilitate articular hyaline cartilage regeneration. Thus, the application of polypeptide hydrogels for cartilage regeneration has a bright future. In this study, the research progress of polypeptide hydrogels used in cartilage-regeneration engineering is systematically reviewed. The characteristics, limitations, and prospects of these materials are evaluated.
摘要
关节软骨缺损被认为与骨关节炎的发展有关. 相关组织再生的研究在骨关节炎的治疗中具有重要意义. 用于软骨再生的支架应具有良好的组织相容性, 力学性能及无细胞毒性, 并能促进种子细胞的增殖和分化. 多肽水凝胶中多肽序列的不同组合使其具有优异的生物可降解性和准确模拟软骨细胞细胞外基质的独特特性, 以维持软骨表型的稳定性及促进关节透明软骨的再生. 因此, 多肽水凝胶在软骨再生中的应用前景广阔. 本文系统综述了多肽水凝胶在软骨再生工程中的研究进展. 对这些材料的特点、局限性和前景进行了评价.
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References
GLYN-JONES S, PALMER A J R, AGRICOLA R, et al. Osteoarthritis [J]. The Lancet, 2015, 386(9991): 376–387.
JIN X Z, JONES G, CICUTTINI F, et al. Effect of vitamin D supplementation on tibial cartilage volume and knee pain among patients with symptomatic knee osteoarthritis: A randomized clinical trial [J]. JAMA, 2016, 315(10): 1005–1013.
ARMIENTO A R, STODDART M J, ALINI M, et al. Biomaterials for articular cartilage tissue engineering: Learning from biology [J]. Acta Biomaterialia, 2018, 65: 1–20.
LUO Y Y, SINKEVICIUTE D, HE Y, et al. The minor collagens in articular cartilage [J]. Protein & Cell, 2017, 8(8): 560–572.
GUILAK F, NIMS R J, DICKS A, et al. Osteoarthritis as a disease of the cartilage pericellular matrix [J]. Matrix Biology, 2018, 71/72: 40–50.
KÜHN K, D’LIMA D D, HASHIMOTO S, et al. Cell death in cartilage [J]. Osteoarthritis and Cartilage, 2004, 12(1): 1–16.
KWON H, BROWN W E, LEE C A, et al. Surgical and tissue engineering strategies for articular cartilage and meniscus repair [J]. Nature Reviews Rheumatology, 2019, 15(9): 550–570.
CUCCHIARINI M, MADRY H. Biomaterial-guided delivery of gene vectors for targeted articular cartilage repair [J]. Nature Reviews Rheumatology, 2019, 15(1): 18–29.
TEMENOFF J S, MIKOS A G. Review: Tissue engineering for regeneration of articular cartilage [J]. Biomaterials, 2000, 21(5): 431–440.
ORYAN A, SAHVIEH S. Effectiveness of chitosan scaffold in skin, bone and cartilage healing [J]. International Journal of Biological Macromolecules, 2017, 104: 1003–1011.
GUO T, NOSHIN M, BAKER H B, et al. 3D printed biofunctionalized scaffolds for microfracture repair of cartilage defects [J]. Biomaterials, 2018, 185: 219–231.
MAKRIS E A, GOMOLL A H, MALIZOS K N, et al. Repair and tissue engineering techniques for articular cartilage [J]. Nature Reviews Rheumatology, 2015, 11(1): 21–34.
GUO T, FERLIN K M, KAPLAN D S, et al. Engineering niches for cartilage tissue regeneration [M]//Biology and engineering of stem cell niches. Boston: Academic Press, 2017.
NIE X L, CHUAH Y J, ZHU W Z, et al. Decellularized tissue engineered hyaline cartilage graft for articular cartilage repair [J]. Biomaterials, 2020, 235: 119821.
RINGE J, BURMESTER G R, SITTINGER M. Regenerative medicine in rheumatic disease: Progress in tissue engineering [J]. Nature Reviews Rheumatology, 2012, 8(8): 493–498.
HUANG B J, HU J C, ATHANASIOU K A. Cell-based tissue engineering strategies used in the clinical repair of articular cartilage [J]. Biomaterials, 2016, 98: 1–22.
JIANG Y Z, TUAN R S. Origin and function of cartilage stem/progenitor cells in osteoarthritis [J]. Nature Reviews Rheumatology, 2015, 11(4): 206–212.
GRACEFFA V, VINATIER C, GUICHEUX J, et al. Chasing chimeras: The elusive stable chondrogenic phenotype [J]. Biomaterials, 2019, 192: 199–225.
LEE H P, GU L, MOONEY D J, et al. Mechanical confinement regulates cartilage matrix formation by chondrocytes [J]. Nature Materials, 2017, 16(12): 1243–1251.
WANG Y, CHEN Y, XU Y, et al. Effects of the bonding intensity between hyaluronan and gelatin on chondrogenic phenotypic maintenance [J]. Journal of Materials Chemistry B, 2020, 8: 9062–9074.
VÁZQUEZ-GONZÁLEZ M, WILLNER I. Stimuli-responsive biomolecule-based hydrogels and their applications [J]. Angewandte Chemie International Edition, 2020, 59(36): 15342–15377.
GAO J, ZHAN J, YANG Z M. Enzyme-instructed self-assembly (EISA) and hydrogelation of peptides [J]. Advanced Materials, 2020, 32(3): 1805798.
DING X, ZHAO H M, LI Y Z, et al. Synthetic peptide hydrogels as 3D scaffolds for tissue engineering [J]. Advanced Drug Delivery Reviews, 2020, 160: 78–104.
FRENCH K M, SOMASUNTHARAM I, DAVIS M E. Self-assembling peptide-based delivery of therapeutics for myocardial infarction [J]. Advanced Drug Delivery Reviews, 2016, 96: 40–53.
REN K X, HE C L, XIAO C S, et al. Injectable glycopolypeptide hydrogels as biomimetic scaffolds for cartilage tissue engineering [J]. Biomaterials, 2015, 51: 238–249.
FU K, WU H G, SU Z Q. Self-assembling peptide-based hydrogels: Fabrication, properties, and applications [J]. Biotechnology Advances, 2021, 49: 107752.
CALIARI S R, BURDICK J A. A practical guide to hydrogels for cell culture [J]. Nature Methods, 2016, 13(5): 405–414.
CAI L L, LIU S, GUO J W, et al. Polypeptide-based self-healing hydrogels: Design and biomedical applications [J]. Acta Biomaterialia, 2020, 113: 84–100.
SONG Z Y, HAN Z Y, LV S X, et al. Synthetic polypeptides: From polymer design to supramolecular assembly and biomedical application [J]. Chemical Society Reviews, 2017, 46(21): 6570–6599.
LU Z H, LIU S J, LE Y G, et al. An injectable collagen-genipin-carbon dot hydrogel combined with photodynamic therapy to enhance chondrogenesis [J]. Biomaterials, 2019, 218: 119190.
MREDHA M T I, KITAMURA N, NONOYAMA T, et al. Anisotropic tough double network hydrogel from fish collagen and its spontaneous in vivo bonding to bone [J]. Biomaterials, 2017, 132: 85–95.
SHI W L, SUN M Y, HU X Q, et al. Structurally and functionally optimized silk-fibroin—gelatin scaffold using 3D printing to repair cartilage injury in vitro and in vivo [J]. Advanced Materials, 2017, 29(29): 1701089.
AISENBREY E A, BRYANT S J. The role of chondroitin sulfate in regulating hypertrophy during MSC chondrogenesis in a cartilage mimetic hydrogel under dynamic loading [J]. Biomaterials, 2019, 190/191: 51–62.
PARMAR P A, CHOW L W, ST-PIERRE J P, et al. Collagen-mimetic peptide-modifiable hydrogels for articular cartilage regeneration [J]. Biomaterials, 2015, 54: 213–225.
CHEN Z Y, ZHANG Q, LI H M, et al. Elastin-like polypeptide modified silk fibroin porous scaffold promotes osteochondral repair [J]. Bioactive Materials, 2021, 6(3): 589–601.
HONG H, SEO Y B, KIM D Y, et al. Digital light processing 3D printed silk fibroin hydrogel for cartilage tissue engineering [J]. Biomaterials, 2020, 232: 119679.
QI C, LIU J, JIN Y, et al. Photo-crosslinkable, injectable sericin hydrogel as 3D biomimetic extracellular matrix for minimally invasive repairing cartilage [J]. Biomaterials, 2018, 163: 89–104.
LIU H, CHENG Y L, CHEN J J, et al. Component effect of stem cell-loaded thermosensitive polypeptide hydrogels on cartilage repair [J]. Acta Biomaterialia, 2018, 73: 103–111.
LEE S S, CHOI G E, LEE H J, et al. Layered double hydroxide and polypeptide thermogel nanocomposite system for chondrogenic differentiation of stem cells [J]. ACS Applied Materials & Interfaces, 2017, 9(49): 42668–42675.
KIM S H, LEE H R, YU S J, et al. Hydrogel-laden paper scaffold system for origami-based tissue engineering [J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(50): 15426–15431.
LAM J, CLARK E C, FONG E L S, et al. Evaluation of cell-laden polyelectrolyte hydrogels incorporating poly(l-Lysine) for applications in cartilage tissue engineering [J]. Biomaterials, 2016, 83: 332–346.
LIN C, CROWLEY S T, UCHIDA S, et al. Treatment of intervertebral disk disease by the administration of mRNA encoding a cartilage-anabolic transcription factor [J]. Molecular Therapy: Nucleic Acids, 2019, 16: 162–171.
LI R, XU J B, WONG D S H, et al. Self-assembled N-cadherin mimetic peptide hydrogels promote the chondrogenesis of mesenchymal stem cells through inhibition of canonical Wnt/β-catenin signaling [J]. Biomaterials, 2017, 145: 33–43.
KIM S J, KIM J E, KIM S H, et al. Therapeutic effects of neuropeptide substance P coupled with self-assembled peptide nanofibers on the progression of osteoarthritis in a rat model [J]. Biomaterials, 2016, 74: 119–130.
LU J J, SHEN X Z, SUN X, et al. Increased recruitment of endogenous stem cells and chondrogenic differentiation by a composite scaffold containing bone marrow homing peptide for cartilage regeneration [J]. Theranostics, 2018, 8(18): 5039–5058.
ALMEIDA H V, ESWARAMOORTHY R, CUNNIFFE G M, et al. Fibrin hydrogels functionalized with cartilage extracellular matrix and incorporating freshly isolated stromal cells as an injectable for cartilage regeneration [J]. Acta Biomaterialia, 2016, 36: 55–62.
USTUN YAYLACI S, SARDAN EKIZ M, ARSLAN E, et al. Supramolecular GAG-like self-assembled glycopeptide nanofibers induce chondrogenesis and cartilage regeneration [J]. Biomacromolecules, 2016, 17(2): 679–689.
VEGA S L, KWON M Y, SONG K H, et al. Combinatorial hydrogels with biochemical gradients for screening 3D cellular microenvironments [J]. Nature Communications, 2018, 9: 614.
ARMIENTO A R, ALINI M, STODDART M J. Articular fibrocartilage — Why does hyaline cartilage fail to repair? [J]. Advanced Drug Delivery Reviews, 2019, 146: 289–305.
GU L S, SHAN T T, MA Y X, et al. Novel biomedical applications of crosslinked collagen [J]. Trends in Biotechnology, 2019, 37(5): 464–491.
SORUSHANOVA A, DELGADO L M, WU Z N, et al. The collagen suprafamily: From biosynthesis to advanced biomaterial development [J]. Advanced Materials, 2019, 31(1): 1801651.
KLOTZ B J, GAWLITTA D, ROSENBERG A J W P, et al. Gelatin-methacryloyl hydrogels: Towards biofabrication-based tissue repair [J]. Trends in Biotechnology, 2016, 34(5): 394–407.
ALTUNBAS A, POCHAN D J. Peptide-based and polypeptide-based hydrogels for drug delivery and tissue engineering [J]. Topics in Current Chemistry, 2012, 310: 135–167.
DALY A C, CRITCHLEY S E, RENCSOK E M, et al. A comparison of different bioinks for 3D bioprinting of fibrocartilage and hyaline cartilage [J]. Biofabrication, 2016, 8(4): 045002.
HAN L, XU J L, LU X, et al. Biohybrid methacrylated gelatin/polyacrylamide hydrogels for cartilage repair [J]. Journal of Materials Chemistry B, 2017, 5(4): 731–741.
HAN L, WANG M H, LI P F, et al. Mussel-inspired tissue-adhesive hydrogel based on the polydopamine—chondroitin sulfate complex for growth-factor-free cartilage regeneration [J]. ACS Applied Materials & Interfaces, 2018, 10(33): 28015–28026.
GAN D L, XU T, XING W S, et al. Mussel-inspired dopamine oligomer intercalated tough and resilient gelatin methacryloyl (GelMA) hydrogels for cartilage regeneration [J]. Journal of Materials Chemistry B, 2019, 7(10): 1716–1725.
PARMAR P A, ST-PIERRE J P, CHOW L W, et al. Enhanced articular cartilage by human mesenchymal stem cells in enzymatically mediated transiently RGDS-functionalized collagen-mimetic hydrogels [J]. Acta Biomaterialia, 2017, 51: 75–88.
PARMAR P A, SKAALURE S C, CHOW L W, et al. Temporally degradable collagen-mimetic hydrogels tuned to chondrogenesis of human mesenchymal stem cells [J]. Biomaterials, 2016, 99: 56–71.
PENG Y Y, YOSHIZUMI A, DANON S J, et al. A Streptococcus pyogenes derived collagen-like protein as a non-cytotoxic and non-immunogenic cross-linkable biomaterial [J]. Biomaterials, 2010, 31(10): 2755–2761.
GHOLIPOURMALEKABADI M, SAPRU S, SAMADIKUCHAKSARAEI A, et al. Silk fibroin for skin injury repair: Where do things stand? [J]. Advanced Drug Delivery Reviews, 2020, 153: 28–53.
CHENG G, DAVOUDI Z, XING X, et al. Advanced silk fibroin biomaterials for cartilage regeneration [J]. ACS Biomaterials Science & Engineering, 2018, 4(8): 2704–2715.
DU S, ZHANG J, ZHOU W T, et al. Interactions between fibroin and sericin proteins from Antheraea pernyi and Bombyx mori silk fibers [J]. Journal of Colloid and Interface Science, 2016, 478: 316–323.
KIM S H, YEON Y K, LEE J M, et al. Precisely printable and biocompatible silk fibroin bioink for digital light processing 3D printing [J]. Nature Communications, 2018, 9: 1620.
BASU A, KUNDURU K R, KATZHENDLER J, et al. Poly(α-hydroxy acid)s and poly(α-hydroxy acid-co-α-amino acid)s derived from amino acid [J]. Advanced Drug Delivery Reviews, 2016, 107: 82–96.
GELAIN F, SILVA D, CAPRINI A, et al. BMHP1-derived self-assembling peptides: Hierarchically assembled structures with self-healing propensity and potential for tissue engineering applications [J]. ACS Nano, 2011, 5(3): 1845–1859.
ZAMUNER A, CAVO M, SCAGLIONE S, et al. Design of decorated self-assembling peptide hydrogels as architecture for mesenchymal stem cells [J]. Materials, 2016, 9(9): 727.
CAO F Y, YIN W N, FAN J X, et al. A novel function of BMHP1 and cBMHP1 peptides to induce the osteogenic differentiation of mesenchymal stem cells [J]. Biomaterials Science, 2015, 3(2): 345–351.
BOGUNOVIC L, WETTERS N G, JAIN A, et al. In vitro analysis of micronized cartilage stability in the knee: Effect of fibrin level, defect size, and defect location [J]. Arthroscopy: the Journal of Arthroscopic & Related Surgery, 2019, 35(4): 1212–1218.
PENG Z, SUN H, BUNPETCH V, et al. The regulation of cartilage extracellular matrix homeostasis in joint cartilage degeneration and regeneration [J]. Biomaterials, 2021, 268: 120555.
KIM J S, KIM T H, KANG D L, et al. Chondrogenic differentiation of human ASCs by stiffness control in 3D fibrin hydrogel [J]. Biochemical and Biophysical Research Communications, 2020, 522(1): 213–219.
DE MELO B A G, JODAT Y A, MEHROTRA S, et al. 3D printed cartilage-like tissue constructs with spatially controlled mechanical properties [J]. Advanced Functional Materials, 2019, 29(51): 1906330.
KARGARPOUR Z, NASIRZADE J, STRAUSS F J, et al. Platelet-rich fibrin suppresses in vitro osteoclastogenesis [J]. Journal of Periodontology, 2020, 91(3): 413–421.
WONG C C, OU K L, LIN Y H, et al. Platelet-rich fibrin facilitates one-stage cartilage repair by promoting chondrocytes viability, migration, and matrix synthesis [J]. International Journal of Molecular Sciences, 2020, 21(2): 577.
MCDERMOTT I D. Patellar chondral defect treatment with a cell-free polyglycolic acid-hyaluronan-based implant and platelet-rich fibrin glue after previously failed microfracture [J]. SAGE Open Medical Case Reports, 2019, 7: 2050313X18823470.
BARBON S, STOCCO E, MACCHI V, et al. Platelet-rich fibrin scaffolds for cartilage and tendon regenerative medicine: From bench to bedside [J]. International Journal of Molecular Sciences, 2019, 20(7): 1701.
TIWARI S, BAHADUR P. Modified hyaluronic acid based materials for biomedical applications [J]. International Journal of Biological Macromolecules, 2019, 121: 556–571.
ACAR H, SRIVASTAVA S, CHUNG E J, et al. Self-assembling peptide-based building blocks in medical applications [J]. Advanced Drug Delivery Reviews, 2017, 110/111: 65–79.
OKESOLA B O, WU Y H, DERKUS B, et al. Supramolecular self-assembly to control structural and biological properties of multicomponent hydrogels [J]. Chemistry of Materials, 2019, 31(19): 7883–7897.
WOLF K J, KUMAR S. Hyaluronic acid: Incorporating the bio into the material [J]. ACS Biomaterials Science & Engineering, 2019, 5(8): 3753–3765.
DOU X Q, FENG C L. Amino acids and peptide-based supramolecular hydrogels for three-dimensional cell culture [J]. Advanced Materials, 2017, 29(16): 1604062.
LI S Y, WANG X, CAO B, et al. Effects of nanoscale spatial arrangement of arginine-glycine-aspartate peptides on dedifferentiation of chondrocytes [J]. Nano Letters, 2015, 15(11): 7755–7765.
QIAO Y S, LIU X Z, ZHOU X C, et al. Gelatin templated polypeptide co-cross-linked hydrogel for bone regeneration [J]. Advanced Healthcare Materials, 2020, 9(1): 1901239.
THAMBI T, LI Y, LEE D S. Injectable hydrogels for sustained release of therapeutic agents [J]. Journal of Controlled Release, 2017, 267: 57–66.
ZHENG H Y, YOSHITOMI T, YOSHIMOTO K. Analysis of chirality effects on stem cell fate using three-dimensional fibrous peptide hydrogels [J]. ACS Applied Bio Materials, 2018, 1(3): 538–543.
UMAN S, DHAND A, BURDICK J A. Recent advances in shear-thinning and self-healing hydrogels for biomedical applications [J]. Journal of Applied Polymer Science, 2020, 137(25): 48668.
YADAV N, CHAUHAN M K, CHAUHAN V S. Short to ultrashort peptide-based hydrogels as a platform for biomedical applications [J]. Biomaterials Science, 2020, 8(1): 84–100.
O’BRIEN S, BRANNIGAN R P, IBANEZ R, et al. Biocompatible polypeptide-based interpenetrating network (IPN) hydrogels with enhanced mechanical properties [J]. Journal of Materials Chemistry B, 2020, 8(34): 7785–7791.
OKESOLA B O, LAU H K, DERKUS B, et al. Covalent co-assembly between resilin-like polypeptide and peptide amphiphile into hydrogels with controlled nanostructure and improved mechanical properties [J]. Biomaterials Science, 2020, 8(3): 846–857.
ANNABI N, RANA D, SANI E S, et al. Engineering a sprayable and elastic hydrogel adhesive with antimicrobial properties for wound healing [J]. Biomaterials, 2017, 139: 229–243.
JIN H L, WAN C, ZOU Z W, et al. Tumor ablation and therapeutic immunity induction by an injectable peptide hydrogel [J]. ACS Nano, 2018, 12(4): 3295–3310.
GRIFFIN D R, ARCHANG M M, KUAN C H, et al. Activating an adaptive immune response from a hydrogel scaffold imparts regenerative wound healing [J]. Nature Materials, 2021, 20(4): 560–569.
FAROKHI M, MOTTAGHITALAB F, FATAHI Y, et al. Overview of silk fibroin use in wound dressings [J]. Trends in Biotechnology, 2018, 36(9): 907–922.
KOIVUSALO L, KAUPPILA M, SAMANTA S, et al. Tissue adhesive hyaluronic acid hydrogels for sutureless stem cell delivery and regeneration of corneal epithelium and stroma [J]. Biomaterials, 2019, 225: 119516.
ZHU D Q, WANG H Y, TRINH P, et al. Elastin-like protein-hyaluronic acid (ELP-HA) hydrogels with decoupled mechanical and biochemical cues for cartilage regeneration [J]. Biomaterials, 2017, 127: 132–140.
ZHANG X Z, CAI D D, ZHOU F F, et al. Targeting downstream subcellular YAP activity as a function of matrix stiffness with Verteporfin-encapsulated chitosan microsphere attenuates osteoarthritis [J]. Biomaterials, 2020, 232: 119724.
DAVIDSON M D, BAN E, SCHOONEN A C M, et al. Mechanochemical adhesion and plasticity in multi-fiber hydrogel networks [J]. Advanced Materials, 2020, 32(8): 1905719.
YANG J R, LI Y Q, LIU Y B, et al. Influence of hydrogel network microstructures on mesenchymal stem cell chondrogenesis in vitro and in vivo [J]. Acta Biomaterialia, 2019, 91: 159–172.
JEYAKUMAR V, NICULESCU-MORZSA E, BAUER C, et al. Redifferentiation of articular chondrocytes by hyperacute serum and platelet rich plasma in collagen type I hydrogels [J]. International Journal of Molecular Sciences, 2019, 20(2): 316.
BRETSCHNEIDER H, STIEHLER M, HARTMANN A, et al. Characterization of primary chondrocytes harvested from hips with femoroacetabular impingement [J]. Osteoarthritis and Cartilage, 2016, 24(9): 1622–1628.
NOVAK T, SEELBINDER B, TWITCHELL C M, et al. Mechanisms and microenvironment investigation of cellularized high density gradient collagen matrices via densification [J]. Advanced Functional Materials, 2016, 26(16): 2617–2628.
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Foundation item: the National Natural Science Foundation of China (Nos. 82071160, 81870806, 81800935 and 81974152), the Special Fund for Scientific and Technological Innovation of Shanghai Jiao Tong University (No. ZH2018ZDB09), the “Double Hundred” Project of Shanghai Jiao Tong University School of Medicine (No. 20191832), the Project of the Innovative Research Team of High-Level Local Universities in Shanghai (No. SSMU-ZDCX20180900), the Advanced Research Program of Shanghai Jiao Tong University Affiliated Sixth People’s Hospital (No. ynlc201810), and the Project of the Science and Technology Commission of Shanghai Municipality (No. 18DZ2260200)
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Hu, Y., Zhu, Z., Teng, L. et al. Applications of Polypeptide Hydrogels in Cartilage-Regeneration Engineering. J. Shanghai Jiaotong Univ. (Sci.) 28, 468–485 (2023). https://doi.org/10.1007/s12204-022-2507-5
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DOI: https://doi.org/10.1007/s12204-022-2507-5
Key words
- polypeptide hydrogel
- poly amino acid
- articular cartilage
- cartilage repair
- cartilage-regeneration engineering