Feasibility of a self-assembling peptide hydrogel scaffold for meniscal defect: An in vivo study in a rabbit model.


Journal

Journal of orthopaedic research : official publication of the Orthopaedic Research Society
ISSN: 1554-527X
Titre abrégé: J Orthop Res
Pays: United States
ID NLM: 8404726

Informations de publication

Date de publication:
01 2021
Historique:
received: 01 12 2019
revised: 19 06 2020
accepted: 18 08 2020
pubmed: 28 8 2020
medline: 1 5 2021
entrez: 28 8 2020
Statut: ppublish

Résumé

The inner avascular zone of the meniscus has limited healing capacity as the area is poorly vascularized. Although peptide hydrogels have been reported to regenerate bone and cartilage, their effect on meniscus regeneration remains unknown. We tested whether the self-assembling peptide hydrogel scaffold KI24RGDS stays in the meniscal lesion and facilitates meniscal repair and regeneration in an induced rabbit meniscal defect model. Full-thickness (2.0 mm diameter) cylindrical defects were introduced into the inner avascular zones of the anterior portions of the medial menisci of rabbit knees (n = 40). Right knee defects were left empty (control group) while the left knee defects were transplanted with peptide hydrogel (KI24RGDS group). Macroscopic meniscus scores were significantly higher in the KI24RGDS group than in the control group at 2, 4, and 8 weeks after surgery. Histological examinations including quantitative and qualitative scores indicated that compared with the control group, the reparative tissue in the meniscus was significantly enhanced in the KI24RGDS group at 2, 4, 8, and 12 weeks after surgery. Immunohistochemical staining showed that the reparative tissue induced by KI24RGDS at 12 weeks postimplantation was positive for Type I and II collagen. KI24RGDS is highly biocompatible and biodegradable, with strong stiffness, and a three dimensional structure mimicking native extracellular matrix and RGDS sequences that enhance cell adhesion and proliferation. This in vivo study demonstrated that KI24RGDS remained in the meniscal lesion and facilitated the repair and regeneration in a rabbit meniscal defect model.

Identifiants

pubmed: 32852842
doi: 10.1002/jor.24841
doi:

Substances chimiques

Hydrogels 0

Types de publication

Evaluation Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

165-176

Informations de copyright

© 2020 Orthopaedic Research Society. Published by Wiley Periodicals LLC.

Références

Verdonk PC, Forsyth RG, Wang J, et al. Characterisation of human knee meniscus cell phenotype. Osteoarthritis Cartilage. 2005;13:548-560.
Makris EA, Hadidi P, Athanasiou KA. The knee meniscus: structure-function, pathophysiology, current repair techniques, and prospects for regeneration. Biomaterials. 2011;32:7411-7431.
Zaffagnini S, Marcheggiani Muccioli GM, Bulgheroni P, et al. Arthroscopic collagen meniscus implantation for partial lateral meniscal defects: a 2-year minimum follow-up study. Am J Sports Med. 2012;40:2281-2288.
Matsubara H, Okazaki K, Izawa T, et al. New suture method for radial tears of the meniscus: biomechanical analysis of cross-suture and double horizontal suture techniques using cyclic load testing. Am J Sports Med. 2012;40:414-418.
Verdonk P, Beaufils P, Bellemans J, et al. Successful treatment of painful irreparable partial meniscal defects with a polyurethane scaffold: 2-year safety and clinical outcomes. Am J Sports Med. 2012;40:844-853.
Kon E, Filardo G, Zaffagnini S, et al. Biodegradable polyurethane meniscal scaffold for isolated partial lesions or as combined procedure for knees with multiple comorbidities: clinical results at 2 years. Knee Surg Sports Traumatol Arthrosc. 2014;22:128-134.
Rongen JJ, van Tienen TG, van Bochove B, Grijpma DW, Buma P. Biomaterials in search of a meniscus substitute. Biomaterials. 2014;35:3527-3540.
Koutsopoulos S. Self-assembling peptide nanofiber hydrogels in tissue engineering and regenerative medicine: progress, design guidelines, and applications. J Biomed Mater Res A. 2016;104:1002-1016.
Misawa H, Kobayashi N, Soto-Gutierrez A, et al. PuraMatrix facilitates bone regeneration in bone defects of calvaria in mice. Cell Transplant. 2006;15:903-910.
Ando K, Imagama S, Kobayashi K, et al. Feasibility and effects of a self-assembling peptide as a scaffold in bone healing: an in vivo study in rabbit lumbar posterolateral fusion and tibial intramedullary models. J Orthop Res. 2018;36:3285-3293.
Miller RE, Grodzinsky AJ, Vanderploeg EJ, et al. Effect of self-assembling peptide, chondrogenic factors, and bone marrow-derived stromal cells on osteochondral repair. Osteoarthritis Cartilage. 2010;18:1608-1619.
Kisiday J, Jin M, Kurz B, et al. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair. Proc Natl Acad Sci USA. 2002;99:9996-10001.
Holmes TC, de Lacalle S, Su X, Liu G, Rich A, Zhang S. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci USA. 2000;97:6728-6733.
Wan S, Borland S, Richardson SM, Merry CLR, Saiani A, Gough JE. Self-assembling peptide hydrogel for intervertebral disc tissue engineering. Acta Biomater. 2016;46:29-40.
Ye Z, Zhang H, Luo H, et al. Temperature and pH effects on biophysical and morphological properties of self-assembling peptide RADA16-I. J Pept Sci. 2008;14:152-162.
Schneider JP, Pochan DJ, Ozbas B, Rajagopal K, Pakstis L, Kretsinger J. Responsive hydrogels from the intramolecular folding and self-assembly of a designed peptide. J Am Chem Soc. 2002;124:15030-15037.
Miller Y, Ma B, Nussinov R. Polymorphism in self-assembly of peptide-based beta-hairpin contributes to network morphology and hydrogel mechanical rigidity. J Phys Chem B. 2015;119:482-490.
Yan C, Altunbas A, Yucel T, Nagarkar RP, Schneider JP, Pochan DJ. Injectable solid hydrogel: mechanism of shear-thinning and immediate recovery of injectable beta-hairpin peptide hydrogels. Soft Matter. 2010;6:5143-5156.
Hirano Y, Kando Y, Hayashi T, Goto K, Nakajima A. Synthesis and cell attachment activity of bioactive oligopeptides: RGD, RGDS, RGDV, and RGDT. J Biomed Mater Res. 1991;25:1523-1534.
Oda S, Otsuki S, Kurokawa Y, Hoshiyama Y, Nakajima M, Neo M. A new method for meniscus repair using type I collagen scaffold and infrapatellar fat pad. J Biomater Appl. 2015;29:1439-1448.
Toratani T, Nakase J, Numata H, et al. Scaffold-free tissue-engineered allogenic adipose-derived stem cells promote meniscus healing. Arthroscopy. 2017;33:346-354.
Laverty S, Girard CA, Williams JM, Hunziker EB, Pritzker KP. The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in the rabbit. Osteoarthritis Cartilage. 2010;18(suppl 3):S53-S65.
Wachsmuth L, Keiffer R, Juretschke HP, Raiss RX, Kimmig N, Lindhorst E. In vivo contrast-enhanced micro MR-imaging of experimental osteoarthritis in the rabbit knee joint at 7.1T1. Osteoarthritis Cartilage. 2003;11:891-902.
Horie M, Driscoll MD, Sampson HW, et al. Implantation of allogenic synovial stem cells promotes meniscal regeneration in a rabbit meniscal defect model. J Bone Joint Surg Am. 2012;94:701-712.
Zhang S, Matsushita T, Kuroda R, et al. Local administration of simvastatin stimulates healing of an avascular meniscus in a rabbit model of a meniscal defect. Am J Sports Med. 2016;44:1735-1743.
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671-675.
Ishida K, Kuroda R, Miwa M, et al. The regenerative effects of platelet-rich plasma on meniscal cells in vitro and its in vivo application with biodegradable gelatin hydrogel. Tissue Eng. 2007;13:1103-1112.
Krenn V, Morawietz L, Haupl T, Neidel J, Petersen I, Konig A. Grading of chronic synovitis--a histopathological grading system for molecular and diagnostic pathology. Pathol Res Pract. 2002;198:317-325.
Longo UG, Loppini M, Romeo G, Maffulli N, Denaro V. Histological scoring systems for tissue-engineered, ex vivo and degenerative meniscus. Knee Surg Sports Traumatol Arthrosc. 2013;21:1569-1576.
Tissakht M, Ahmed AM. Tensile stress-strain characteristics of the human meniscal material. J Biomech. 1995;28:411-422.
Rey-Rico A, Cucchiarini M, Madry H. Hydrogels for precision meniscus tissue engineering: a comprehensive review. Connect Tissue Res. 2017;58:317-328.
Hou S, Wang X, Park S, Jin X, Ma PX. Rapid Self-integrating, injectable hydrogel for tissue complex regeneration. Adv Healthc Mater. 2015;4(1491-1495):1423-1425.
Niu W, Guo W, Han S, Zhu Y, Liu S, Guo Q. Cell-based strategies for meniscus tissue engineering. Stem Cells Int. 2016;2016:4717184.
Guo W, Xu W, Wang Z, et al. Cell-free strategies for repair and regeneration of meniscus injuries through the recruitment of endogenous stem/progenitor cells. Stem Cells Int. 2018;2018:5310471.
Spees JL, Lee RH, Gregory CA. Mechanisms of mesenchymal stem/stromal cell function. Stem Cell Res Ther. 2016;7:125.
Kondo S, Muneta T, Nakagawa Y, et al. Transplantation of autologous synovial mesenchymal stem cells promotes meniscus regeneration in aged primates. J Orthop Res. 2017;35:1274-1282.
Rodkey WG, DeHaven KE, Montgomery WH, et al. Comparison of the collagen meniscus implant with partial meniscectomy. A prospective randomized trial. J Bone Joint Surg Am. 2008;90:1413-1426.
Pugliese R, Gelain F. Peptidic biomaterials: From self-assembling to regenerative medicine. Trends Biotechnol. 2017;35:145-158.
Zhu J, Marchant RE. Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devices. 2011;8:607-626.
Ballyns JJ, Wright TM, Bonassar LJ. Effect of media mixing on ECM assembly and mechanical properties of anatomically-shaped tissue engineered meniscus. Biomaterials. 2010;31:6756-6763.
Shin H, Jo S, Mikos AG. Biomimetic materials for tissue engineering. Biomaterials. 2003;24:4353-4364.
Lu J, Wang X. Biomimetic self-assembling peptide hydrogels for tissue engineering applications. Adv Exp Med Biol. 2018;1064:297-312.
Hersel U, Dahmen C, Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials. 2003;24:4385-4415.
Comisar WA, Hsiong SX, Kong HJ, Mooney DJ, Linderman JJ. Multi-scale modeling to predict ligand presentation within RGD nanopatterned hydrogels. Biomaterials. 2006;27:2322-2329.
Deponti D, Di Giancamillo A, Scotti C, Peretti GM, Martin I. Animal models for meniscus repair and regeneration. J Tissue Eng Regen Med. 2015;9:512-527.

Auteurs

Nobuhiro Okuno (N)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Shuhei Otsuki (S)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Jo Aoyama (J)

Department of Chemistry and Materials Engineering, Faculty of Chemistry, Materials, and Bioengineering, Kansai University, Osaka, Japan.

Kosuke Nakagawa (K)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Tomohiko Murakami (T)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Kuniaki Ikeda (K)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Yoshinobu Hirose (Y)

Department of Pathology, Osaka Medical College, Osaka, Japan.

Hitoshi Wakama (H)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Tomohiro Okayoshi (T)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Yoshinori Okamoto (Y)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Yoshiaki Hirano (Y)

Department of Chemistry and Materials Engineering, Faculty of Chemistry, Materials, and Bioengineering, Kansai University, Osaka, Japan.

Masashi Neo (M)

Department of Orthopedic Surgery, Osaka Medical College, Osaka, Japan.

Articles similaires

Humans Students, Medical Robotic Surgical Procedures Feasibility Studies Female
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH