Skip to main content
SpringerLink
Log in

Mesenchymal Stem Cells Therapeutic Applications in Cartilage Regeneration

  • Chapter
  • First Online:
Therapeutic Applications of Mesenchymal Stem Cells in Veterinary Medicine

  • 211 Accesses

Abstract

Among various joint affections, osteoarthritis is one of the most common joint problems reported in animals. Currently, no effective treatment is available that can treat the condition to the fullest. Mesenchymal stem cells (MSCs) offer a potential tool to address the joint affections. These cells can be harvested from numerous body sources, although the cells derived from musculoskeletal sources appear more suitable. MSCs under cartilaginous-type microenvironment exhibit characteristics of the chondrocytes. This proposes the usefulness of the suitable scaffold/matrices, growth factors or the mechanical factors for the effectiveness of these cells. MSCs in vitro chondrogenesis, however, is affected by various factors and can be correlated with the non-uniform response of MSCs under in vivo system. Numerous in vivo chondrogenic studies, limited in one or the other factors, favour MSCs therapeutic applications although without any guaranteed results. A variable response occurs across the veterinary species with the MSCs transplantation under in vivo studies. The current chapter focuses on the chondrogenic potential of MSCs and the factors that affect their in vitro and in vivo chondrogenesis to provide understanding in the current status and future prospects of the therapy.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdalmula A, Dooley LM, Kaufman C, Washington EA, House JV, Blacklaws BA, Ghosh P, Itescu S, Bailey SR, Kimpton WG (2017) Immunoselected STRO-3+ mesenchymal precursor cells reduce inflammation and improve clinical outcomes in a large animal model of monoarthritis. Stem Cell Res Ther 8:22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Adkisson HD, Gillis MP, Davis EC, Maloney W, Hruska KA (2001) In vitro generation of scaffold independent neocartilage. Clin Orthop Relat Res S391:280–294

    Article  Google Scholar 

  • Al Faqeh H, Nor Hamdan BM, Chen HC, Aminuddin BS, Ruszymah BH (2012) The potential of intra-articular injection of chondrogenic-induced bone marrow stem cells to retard the progression of osteoarthritis in a sheep model. Exp Gerontol 47:458–464

    Article  PubMed  Google Scholar 

  • Alicka M, Kornicka-Garbowska K, Kucharczyk K, Kępska M, Rӧcken M, Marycz K (2020) Age-dependent impairment of adipose-derived stem cells isolated from horses. Stem Cell Res Ther 11(1):4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ando W, Heard BJ, Chung M, Nakamura N, Frank CB, Hart DA (2012) Sheep synovial membrane-derived mesenchymal progenitor cells retain the phenotype of the original tissue that was exposed to in-vivo inflammation: evidence for a suppressed chondrogenic differentiation potential of the cells. Inflamm Res 61:599–608

    Article  CAS  PubMed  Google Scholar 

  • Ardanaz N, Vázquez FJ, Romero A, Remacha AR, Barrachina L, Sanz A, Ranera B, Vitoria A, Albareda J, Prades M, Zaragoza P, Martín-Burriel I, Rodellar C (2016) Inflammatory response to the administration of mesenchymal stem cells in an equine experimental model: effect of autologous, and single and repeat doses of pooled allogeneic cells in healthy joints. BMC Vet Res 12

    Google Scholar 

  • Arnhold S, Elashry MI, Klymiuk MC, Geburek F (2019) Investigation of stemness and multipotency of equine adipose-derived mesenchymal stem cells (ASCs) from different fat sources in comparison with lipoma. Stem Cell Res Ther 10(1):309

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arora A, Sriram M, Kothari A, Katti DS (2017) Co-culture of infrapatellar fat pad-derived mesenchymal stromal cells and articular chondrocytes in plasma clot for cartilage tissue engineering. Cytotherapy. 19(7):881–894

    Article  CAS  PubMed  Google Scholar 

  • Athanasiou AK, Agarwal A, Muffoletto A (1995) Biomechanical properties of hip cartilage in experimental animal models. Clin Orthop 316:254–266

    Article  Google Scholar 

  • Bagge J, MacLeod JN, Berg LC (2020) Cellular proliferation of equine bone marrow- and adipose tissue-derived mesenchymal stem cells decline with increasing donor age. Front Vet Sci 7:602403

    Article  PubMed  PubMed Central  Google Scholar 

  • Barbour KE, Helmick CG, Boring M, Zhang X, Lu H, Holt JB (2016) Prevalence of doctor diagnosed arthritis at state and county levels-United States, 2014. MMWR Morb Mortal Wkly Rep 65(19):489–494

    Article  PubMed  Google Scholar 

  • Bçrziòð U, Matise-Van Houtana I, Pçtersone I, Dûrîtis I, Òikuïðins S, Bogdanova-Jâtniece A, Kâlis M, Svirskis Ð, Skrastiòa D, Ezerta A et al (2018) Characterisation and in vivo safety of canine adipose-derived stem cells. Proc Latvian Acad Sci U S A 72(3):160–171

    Google Scholar 

  • Bekkers JE, Tsuchida AI, van Rijen MH, Vonk LA, Dhert WJ, Creemers LB, Saris DB (2013) Single-stage cell-based cartilage regeneration using a combination of chondrons and mesenchymal stromal cells: comparison with microfracture. Am J Sports Med 41(9):2158–2166

    Article  PubMed  Google Scholar 

  • Berglund AK, Schnabel LV (2017) Allogeneic major histocompatibility complex-mismatched equine bone marrow-derived mesenchymal stem cells are targeted for death by cytotoxic anti-major histocompatibility complex antibodies. Equine Vet J 49(4):539–544

    Article  CAS  PubMed  Google Scholar 

  • Bertolo A, Steffen F, Malonzo-Marty C, Stoyanov J (2015) Canine mesenchymal stem cell potential and the importance of dog breed: implication for cell-based therapies. Cell Transplant 24(10):1969–1980

    Article  PubMed  Google Scholar 

  • Bertoni L, Branly T, Jacquet S, Desancé M, Desquilbet L, Rivory P, Hartmann D-J, Denoix J-M, Audigié F, Galéra P, Demoor M (2019) Intra-articular injection of 2 different dosages of autologous and allogeneic bone marrow- and umbilical cord-derived Mesenchymal stem cells triggers a variable inflammatory response of the fetlock joint on 12 sound experimental horses. Stem Cells Int 2019:9431894

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bertoni L, Jacquet-Guibon S, Branly T, Desancé M, Legendre F, Melin M, Rivory P, Hartmann D-J, Schmutz A, Denoix J-M, Demoor M, Audigié F, Galéra P (2021) Evaluation of allogeneic bone-marrow-derived and umbilical cord blood-derived mesenchymal stem cells to prevent the development of osteoarthritis in an equine model. Int J Mol Sci 22:2499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Black LL, Gaynor J, Gahring D, Adams C, Aron D, Harman S, Gingerich DA, Harman R (2007) Effect of adipose-derived mesenchymal stem and regenerative cells on lameness in dogs with chronic osteoarthritis of the coxofemoral joints: a randomized, double-blinded, multicenter, controlled trial. Vet Ther 8:272–284

    PubMed  Google Scholar 

  • Black LL, Gaynor J, Adams C, Dhupa S, Sams AE, Taylor R, Harman S, Gingerich DA, Harman R (2008) Effect of intraarticular injection of autologous adipose-derived mesenchymal stem and regenerative cells on clinical signs of chronic osteoarthritis of the elbow joint in dogs. Vet Ther 9:192–200

    PubMed  Google Scholar 

  • Bordbar S, LotfiBakhshaiesh N, Khanmohammadi M, Sayahpour FA, Alini M, Baghaban Eslaminejad M (2020) Production and evaluation of decellularized extracellular matrix hydrogel for cartilage regeneration derived from knee cartilage. J Biomed Mater Res A 108(4):938–946

    Article  CAS  PubMed  Google Scholar 

  • Bornes TD, Jomha NM, Mulet-Sierra A, Adesida AB (2015) Hypoxic culture of bone marrow-derived mesenchymal stromal stem cells differentially enhances in vitro chondrogenesis within cell-seeded collagen and hyaluronic acid porous scaffolds. Stem Cell Res Ther 6:84

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bornes TD, Jomha NM, Mulet-Sierra A, Adesida AB (2016) Optimal seeding densities for In Vitro Chondrogenesis of two- and three-dimensional-isolated and -expanded bone marrow-derived Mesenchymal stromal stem cells within a porous collagen scaffold. Tissue Eng Part C Methods 22(3):208–220

    Article  CAS  PubMed  Google Scholar 

  • Bornes TD, Adesida AB, Jomha NM (2018) Articular cartilage repair with mesenchymal stem cells after chondrogenic priming: a pilot study. Tissue Eng 24:9–10

    Google Scholar 

  • Bosnakovski D, Mizuno M, Kim G, Ishiguro T, Okumura M, Iwanaga T, Kadosawa T, Fujinaga T (2004) Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells in pellet cultural system. Exp Hematol 32(5):502–509

    Article  CAS  PubMed  Google Scholar 

  • Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T (2006) Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol Bioeng 93(6):1152–1163

    Article  CAS  PubMed  Google Scholar 

  • Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM (2013) Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 15(6):641–648

    Article  PubMed  PubMed Central  Google Scholar 

  • Bozkurt M, Aşık MD, Gürsoy S, Türk M, Karahan S, Gümüşkaya B, Akkaya M, Şimşek ME, Cay N, Doğan M (2019) Autologous stem cell-derived chondrocyte implantation with bio-targeted microspheres for the treatment of osteochondral defects. J Orthop Surg Res 14(1):394

    Article  PubMed  PubMed Central  Google Scholar 

  • Branly T, Bertoni L, Contentin R, Rakic R, Gomez-Leduc T, Desancé M, Hervieu M, Legendre F, Jacquet S, Audigié F, Denoix JM, Demoor M, Galéra P (2017) Characterization and use of equine bone marrow mesenchymal stem cells in equine cartilage engineering. Study of their hyaline cartilage forming potential when cultured under hypoxia within a biomaterial in the presence of BMP-2 and TGF-ß1. Stem Cell Rev Rep 13(5):611–630

    Article  CAS  PubMed  Google Scholar 

  • Broeckx S, Zimmerman M, Crocetti S, Suls M, Marien T, Ferguson SJ, Chiers K, Duchateau L, Franco-Obregón A, Wuertz K et al (2014) Regenerative therapies for equine degenerative joint disease: a preliminary study. PLoS One 9(1):e85917

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Broeckx SY, Spaas JH, Chiers K, Duchateau L, Van Hecke L, Van Brantegem L, Dumoulin M, Martens AM, Pille F (2018) Equine allogeneic chondrogenic induced mesenchymal stem cells: a GCP target animal safety and biodistribution study. Res Vet Sci 117:246–254

    Article  CAS  PubMed  Google Scholar 

  • Broeckx SY, Seys B, Suls M, Vandenberghe A, Marien T, Adriaensen E, Declercq J, Van Hecke L, Braun G, Hellmann K et al (2019) Equine allogeneic chondrogenic induced mesenchymal stem cells are an effective treatment for degenerative joint disease in horses. Stem Cells Dev 28(6):410–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckwalter JA, Mankin HJ, Grodzinsky AJ (2005) Articular cartilage and osteoarthritis. Instr Course Lect 54:465–480

    PubMed  Google Scholar 

  • Bundgaard L, Stensballe A, Elbæk KJ, Berg LC (2018) Mapping of equine mesenchymal stromal cell surface proteomes for identification of specific markers using proteomics and gene expression analysis: an in vitro cross-sectional study. Stem Cell Res Ther 9:288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bwalya EC, Kim S, Fang J, Wijekoon HMS, Hosoya K, Okumura M (2017) Effects of pentosane polysulfate and polysulfated glycosaminoglycan on chondrogenesis of canine bone marrow-derived mesenchymal stem cells in alginate and micromass culture. J Vet Med Sci 79(7):1182–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabon Q, Febre M, Gomez N, Cachon T, Pillard P, Carozzo C, Saulnier N, Robert C, Livet V, Rakic R, Plantier N, Saas P, Maddens S, Viguier E (2019) Long-term safety and efficacy of single or repeated intra-articular injection of allogeneic neonatal mesenchymal stromal cells for managing pain and lameness in moderate to severe canine osteoarthritis without anti-inflammatory pharmacological support: pilot clinical study. Front Vet Sci 6:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Caminal M, Moll X, Codina D, Rabanal RM, Morist A, Barrachina J, Garcia F, Pla A, Vives J (2014a) Transitory improvement of articular cartilage characteristics after implantation of polylactide: polyglycolic acid (PLGA) scaffolds seeded with autologous mesenchymal stromal cells in a sheep model of critical-sized chondral defect. Biotechnol Lett 36:2143–2153

    Article  CAS  PubMed  Google Scholar 

  • Caminal M, Fonseca C, Peris D, Moll X, Rabanal RM, Barrachina J, Codina D, Garcίa F, Cairó JJ, Gódia F, Pla A, Vives J (2014b) Use of a chronic model of articular cartilage and meniscal injury for the assessment of long-term effects after autologous mesenchymal stromal cell treatment in sheep. N Biotechnol 31(5):492–498

    Article  CAS  PubMed  Google Scholar 

  • Campos LL, Landim-Alvarenga FC, Ikeda TL, Monteiro BA, Maia L, Freitas-Dell’Aqua CP, De Vita B (2017) Isolation, culture, characterization and cryopreservation of stem cells derived from amniotic mesenchymal layer and umbilical cord tissue of bovine fetuses. Pesquisa Veterinária Brasileira 37(3):278–286

    Article  Google Scholar 

  • Cardoso TC, Okamura LH, Baptistella JC, Gameiro R, Ferreira HL, Marinho M, Flores EF (2017) Isolation, characterization and immunomodulatory-associated gene transcription of Wharton’s jelly-derived multipotent mesenchymal stromal cells at different trimesters of cow pregnancy. Cell Tissue Res 367(2):243–256

    Article  CAS  PubMed  Google Scholar 

  • Caron JP, Genovese RL (2003) Principals and practices of joint disease treatment. In: Ross MW, Dyson S (eds) Diagnosis and management of lameness in the horse, 1st edn. Saunders, Philadelphia (PA), pp 746–764

    Chapter  Google Scholar 

  • Carrade DD, Owens SD, Galuppo LD, Vidal MA, Ferraro GL, Librach F, Buerchler S, Friedman MS, Walker NJ, Borjesson DL (2011) Clinicopathologic findings following intra-articular injection of autologous and allogeneic placentally derived equine mesenchymal stem cells in horses. Cytotherapy 13(4):419–430

    Article  CAS  PubMed  Google Scholar 

  • Cestari H, Costa e Souza JP, Hussni CA, Rodrigues CA, Watanabe MJ, Garcia Alves AL (2021) Intra-articular mesenchymal stem cell therapy on a joint capsule rupture in a horse—a case report. Res Soc Dev 10(12):e211101220370

    Article  Google Scholar 

  • Chang L-B, Peng S-Y, Chou C-J, Chen Y-J, Shiu J-S, Tu P-A, Gao S-X, Chen Y-C, Lin T-K, Wu S-C (2018) Therapeutic potential of amniotic fluid stem cells to treat bilateral ovarian dystrophy in dairy cows in a subtropical region. Reprod Domest Anim 53(4):1024–1024

    Google Scholar 

  • Chapman H-S, Gale AL, Dodson ME, Linardi RL, Ortved KF (2020) Autologous platelet lysate does not enhance chondrogenic differentiation of equine bone marrow-derived mesenchymal stromal cells despite increased TGF-β1 concentration. Stem Cells Dev 29(3):144–155

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Zhao C, Zhao Y, Li L, Liu S, Zhu Z, Guan W (2018) The biological characteristics of sheep umbilical cord mesenchymal stem cells. Can J Vet Res 82:216–224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clegg P, Booth R (2000) Drugs used to treat osteoarthritis in the horse. In Practice 22:594–603

    Article  Google Scholar 

  • Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR (2020a) Single and repeated intra-articular injections in the tarsocrural joint with allogeneic and autologous equine bone marrow-derived mesenchymal stem cells are safe, but did not reduce acute inflammation in an experimental interleukin-1β model of synovitis. Equine Vet J 52(4):601–612

    Article  PubMed  PubMed Central  Google Scholar 

  • Colbath AC, Dow SW, Hopkins LS, Phillips JN, Mcilwraith CW, Goodrich LR (2020b) Allogeneic vs. autologous intra-articular mesenchymal stem cell injection within normal horses: clinical and cytological comparisons suggest safety. Equine Vet J 52(1):144–151

    Article  CAS  PubMed  Google Scholar 

  • Contentin R, Demoor M, Concari M, Desancé M, Audigié F, Branly T, Galéra P (2020) Comparison of the chondrogenic potential of mesenchymal stem cells derived from bone marrow and umbilical cord blood intended for cartilage tissue engineering. Stem Cell Rev Rep 16(1):126–143

    Article  CAS  PubMed  Google Scholar 

  • Critchley S, Sheehy EJ, Cunniffe G, Diaz-Payno P, Carroll SF, Jeon O, Alsberg E, Brama PAJ, Kelly DJ (2020) 3D printing of fibre-reinforced cartilaginous templates for the regeneration of osteochondral defects. Acta Biomater 113:130–143

    Article  CAS  PubMed  Google Scholar 

  • Cuervo B, Rubio M, Sopena J, Dominguez JM, Vilar J, Morales M, Cugat R, Carrillo JM (2014) Hip osteoarthritis in dogs: a randomized study using mesenchymal stem cells from adipose tissue and plasma rich in growth factors. Int J Mol Sci 15:13437–13460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Silva CG, Martins CF, Cardoso TC, da Cunha ER, Bessler HC, MacManus CM, Pivato I, Bao SN (2016) Isolation and characterization of Mesenchymal stem cells derived from bovine Wharton’s jelly and their potential use in cloning by nuclear transfer. Cienc Rural, Santa Maria 46(10):1830–1837

    Article  CAS  Google Scholar 

  • Daems R, Van Hecke L, Schwarzkopf I, Depuydt E, Broeckx SY, David M, Beerts C, Vandekerckhove P, Spaas JH (2019) A feasibility study on the use of equine chondrogenic induced mesenchymal stem cells as a treatment for natural occurring osteoarthritis in dogs. Stem Cells Int 2019:4587594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dar ER, Gugjoo MB, Javaid M, Hussain S, Fazili MR, Dhama K, Alqahtani T, Alqahtani AM, Shah RA, Emran TB (2021) Adipose tissue- and bone marrow-derived mesenchymal stem cells from sheep: culture characteristics. Animals 11(8):2153

    Article  PubMed  PubMed Central  Google Scholar 

  • Delco ML, Goodale M, Talts JF, Pownder SL, Koff MF, Miller AD, Nixon B, Bonassar LJ, Lundgren-Åkerlund E, Fortier LA (2020) Integrin α10β1-selected mesenchymal stem cells mitigate the progression of osteoarthritis in an equine talar impact model. Am J Sports Med 48(3):612–623

    Article  PubMed  Google Scholar 

  • Delling U, Brehm W, Metzger M, Ludewig E, Winter K, Jülke H (2015) In vivo tracking and fate of intra-articularly injected superparamagnetic iron oxide particle-labeled multipotent stromal cells in a sheep model of osteoarthritis. Cell Transplant 24:2379–2390

    Article  PubMed  Google Scholar 

  • Deng Y, Huang G, Zou L, Nong T, Yang X, Cui J, Wei Y, Yang S, Shi D (2018) Isolation and characterization of buffalo (Bubalus bubalis) amniotic mesenchymal stem cells derived from amnion from the first trimester pregnancy. J Vet Med Sci 80(4):710–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desando G, Giavaresi G, Cavallo C, Bartolotti I, Sartoni F, Aldini NN, Martini L, Parrilli A, Mariani E, Fini M, Grigolo B (2016) Autologous bone marrow concentrate in a sheep model of osteoarthritis: new perspectives for cartilage and meniscus repair. Tissue Eng 22(6):608–619

    Article  CAS  Google Scholar 

  • Dos Santos VH, Pfeifer JPH, De Souza JB, De Castro Stievani F, Hussni CA, De Assis Golim M, Deffune E, Garcia Alves AL (2019) Evaluation of alginate hydrogel encapsulated mesenchymal stem cell migration in horses. Res Vet Sci 124:38–45

    Article  CAS  Google Scholar 

  • Dražilov SS, Mrkovački J, Spasovski V, Fazlagić A, Pavlović S, Nikčević G (2018) The use of canine mesenchymal stem cells for the autologous treatment of osteoarthritis. Acta Vet Hung 66(3):376–389

    Article  CAS  Google Scholar 

  • Duarte Campos DF, Drescher W, Rath B, Tingart M, Fischer H (2012) Supporting biomaterials for articular cartilage repair. Cartilage 3(3):205–221

    Article  PubMed  PubMed Central  Google Scholar 

  • Elkhenany H, Amelse L, Caldwell M, Abdelwahed R, Dhar M (2016) Impact of the source and serial passaging of goat mesenchymal stem cells on osteogenic differentiation potential: implications for bone tissue engineering. J Anim Sci Biotechnol 7:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El-Tookhy, Abou Elkheir W, Mokbel A, Osman A (2008) Intra-articular injection of autologous mesenchymal stem cells in experimental chondral defects in dogs. Egypt Rheumatol 30(2):1–10

    Google Scholar 

  • Endo K, Fujita N, Nakagawa T, Nishimura R (2019a) Comparison of the effect of growth factors on chondrogenesis of canine mesenchymal stem cells. J Vet Med Sci 81(8):1211–1218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endo K, Fujita N, Nakagawa T, Nishimura R (2019b) Effect of fibroblast growth factor-2 and serum on canine mesenchymal stem cell chondrogenesis. Tissue Eng Part A 25(11–12):901–910

    Article  CAS  PubMed  Google Scholar 

  • Erickson IE, van Veen SC, Sengupta S, Kestle SR, Mauck RL (2011) Cartilage matrix formation by bovine mesenchymal stem cells in three-dimensional culture is age-dependent. Clin Orthop Relat Res 469:2744–2753

    Article  PubMed  PubMed Central  Google Scholar 

  • Favreau H, Pijnenburg L, Seitlinger J, Fioretti F, Keller L, Scipioni D, Adriaensen H, Kuchler-Bopp S, Ehlinger M, Mainard D, Rosset P, Hua G, Gentile L, Jessel NB (2020) Osteochondral repair combining therapeutics implant with mesenchymal stem cells spheroids. Nanomedicine 29:102253. https://doi.org/10.1016/j.nano.2020.102253

    Article  CAS  PubMed  Google Scholar 

  • Feitosa MLT, Fadel L, Beltrão-Braga PCB, Wenceslau CV, Kerkis I, Kerkis A, Júnior EHB, Martins JFP, Martins DS, Miglino MA, Ambrósio CE (2010) Successful transplant of mesenchymal stem cells in induced osteonecrosis of the sheep femoral head. Preliminary results. Acta Cir Bras 25(5):416–422

    Article  PubMed  Google Scholar 

  • Feng C, Luo X, He N, Xia H, Lv X, Zhang X, Li D, Wang F, He J, Zhang L, Lin X, Lin L, Yin H, He J, Wang J, Cao W, Wang R, Zhou G, Wang W (2018) Efficacy and persistence of allogeneic adipose derived mesenchymal stem cells combined with hyaluronic acid in osteoarthritis after intra-articular injection in a sheep model. Tissue Eng 24(3–4):219–233

    Article  CAS  Google Scholar 

  • Ferris DJ, Frisbie DD, Kisiday JD, McIlwraith CW, Hague BA, Major MD, Schneider RK, Zubrod CJ, Kawcak CE, Goodrich LR (2014) Clinical outcome after intra-articular administration of bone marrow derived mesenchymal stem cells in 33 horses with stifle injury. Vet Surg 43(3):255–265

    Article  PubMed  Google Scholar 

  • Fisher MB, Henning EA, Söegaard N, Bostrom M, Esterhai JL, Mauck RL (2015) Engineering meniscus structure and function via multi-layered mesenchymal stem cell-seeded nanofibrous scaffolds. J Biomech 48(8):1412–1419

    Article  PubMed  PubMed Central  Google Scholar 

  • Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24(4):150–154

    Article  CAS  PubMed  Google Scholar 

  • Frisbie DD, Cross MW, McIlwraith CW (2006) A comparative study of articular cartilage thickness in the stifle of animal species used in human pre-clinical studies compared to articular cartilage thickness in the human. Vet Comp Orthop Traumatol 19(3):142–146

    Article  CAS  PubMed  Google Scholar 

  • Frisbie DD, Kisiday JD, Kawcak CE, Werpy NM, McIlwraith CW (2009) Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthop Res 27:1675–1680

    Article  PubMed  Google Scholar 

  • Fülber J, Maria DA, Correia da Silva LCL, Massoco CO, Agreste F, Baccarin RYA (2016) Comparative study of equine mesenchymal stem cells from healthy and injured synovial tissues: an in vitro assessment. Stem Cell Res Ther 7:35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fülber J, Agreste FR, Seidel SRT, Sotelo EDP, Barbosa ÂP, Michelacci YM, Baccarin RYA (2021) Chondrogenic potential of mesenchymal stem cells from horses using a magnetic 3D cell culture system. World J Stem Cells 13(6):645–658

    Article  PubMed  PubMed Central  Google Scholar 

  • Futrega K, Music E, Robey PG, Gronthos S, Crawford R, Saifzadeh S, Klein TJ, Doran MR (2021) Characterisation of ovine bone marrow-derived stromal cells (oBMSC) and evaluation of chondrogenically induced micro-pellets for cartilage tissue repair in vivo. Stem Cell Res Ther 12(1):26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabner S, Ertl R, Velde K, Renner M, Jenner F, Egerbacher M, Hlavaty J (2018) Cytokine-induced interleukin-1 receptor antagonist protein expression in genetically engineered equine mesenchymal stem cells for osteoarthritis treatment. J Gene Med 20(5):e3021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gale AL, Mammone RM, Dodson ME, Linardi RL, Ortved KF (2019a) The effect of hypoxia on chondrogenesis of equine synovial membrane-derived and bone marrow-derived mesenchymal stem cells. BMC Vet Res 15(1):201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gale AL, Linardi RL, McClung G, Mammone RM, Ortved KF (2019b) Comparison of the chondrogenic differentiation potential of equine synovial membrane-derived and bone marrow-derived mesenchymal stem cells. Front Vet Sci 6:178

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia RS, Melo UP, Ferreira C, Toscano FS, Cruz GM (2009) Estudoclínico e radiográfico da osteoartritetársicajuvenilempotros da raçamangalargamarchador. Ciên Ani Bras 10(1):254–260

    Google Scholar 

  • Garcia D, Longo UG, Vaquero J, Forriol F, Loppini M, Khan WS, Denaro V (2015) Amniotic membrane transplant for articular cartilage repair: an experimental study in sheep. Curr Stem Cell Res Ther 10:77–83

    Article  CAS  PubMed  Google Scholar 

  • Gershwin LJ (2007) Veterinary autoimmunity: autoimmune diseases in domestic animals. Ann NY Acad Sci 1109:109–101

    Article  PubMed  Google Scholar 

  • Giretova M, Medvecky L, Petrovova E, Cizkova D, Danko J, Mudronova D et al (2019) Polyhydroxybutyrate/chitosan 3D scaffolds promote in vitro and in vivo chondrogenesis. Appl Biochem Biotechnol 189(2):556–575

    Article  CAS  PubMed  Google Scholar 

  • Goldman SM, Barabino GA (2016) Hydrodynamic loading in concomitance with exogenous cytokine stimulation modulates differentiation of bovine mesenchymal stem cells towards osteochondral lineages. BMC Biotechnol 16:10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • González-Fernández ML, Pérez-Castrillo S, Sánchez-Lázaro JA, Prieto-Fernández JG, López-González ME, Lobato-Pérez S, Colaço BJ, Olivera ER, Villar-Suárez V (2016) Assessment of regeneration in meniscal lesions by use of mesenchymal stem cells derived from equine bone marrow and adipose tissue. Am J Vet Res 77:779–788

    Article  PubMed  Google Scholar 

  • Goodrich LR, Chen AC, Werpy NM, Williams AA, Kisiday JD, Su AW, Cory E, Morley PS, McIlwraith CW, Sah RL, Chu CR (2016) Addition of mesenchymal stem cells to autologous platelet-enhanced fibrin scaffolds in chondral defects: does it enhance repair? J Bone Joint Surg 98:23–34

    Article  PubMed  PubMed Central  Google Scholar 

  • Guercio A, Di Marco P, Casella S, Cannella V, Russotto L, Purpari G, Di Bella S, Piccione G (2012) Production of canine mesenchymal stem cells from adipose tissue and their application in dogs with chronic osteoarthritis of the humeroradial joints. Cell Biol Int 36:189–194

    Article  CAS  PubMed  Google Scholar 

  • Gugjoo MB, Pal A (2020) Mesenchymal stem cell research in veterinary sciences. Springer Nature, pp 1–337

    Book  Google Scholar 

  • Gugjoo MB, Amarpal, Sharma GT, Kinjavdekar P, Aithal HP, Pawde AM (2016) Cartilage tissue engineering: role of mesenchymal stem cells along with growth factors and scaffolds. Indian J Med Res 144(3):339–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gugjoo MB, Amarpal, Abdelbaset-Ismail A, Aithal HP, Kinjavdekar P, Pawde AM, Kumar GS, Sharma GT (2017) Mesenchymal stem cells with IGF-1 and TGF-β1 in laminin gel for osteochondral defects in rabbits. Biomed Pharmacother 93:1165–1174

    Article  CAS  PubMed  Google Scholar 

  • Gugjoo MB, Amarpal, Makhdoomi DM, Sharma GT (2019) Equine mesenchymal stem cells: properties, sources, characterization and potential therapeutic applications. J Equine Vet Sci 72:16–27

    Article  PubMed  Google Scholar 

  • Gugjoo MB, Amarpal AAI, Aithal HP, Kinjavdekar P, Saikumar GS, Sharma GT (2020) Allogeneic mesenchymal stem cells and growth factors in gel scaffold repair osteochondral defect in rabbit. Regen Med 14. https://doi.org/10.2217/rme-2018-0138

  • Guo X, Wang C, Zhang Y, Xia R, Hu M, Duan C, Zhao Q, Dong L, Lu J, Qing SY (2004) Repair of large articular cartilage defects with implants of autologous mesenchymal stem cells seeded into beta-tricalcium phosphate in a sheep model. Tissue Eng 10(11–12):1818–1829

    Article  CAS  PubMed  Google Scholar 

  • Gupta RC, Lall R, Srivastava A, Sinha A (2019) Hyaluronic acid: molecular mechanisms and therapeutic trajectory. Front Vet Sci 6:192

    Article  PubMed  PubMed Central  Google Scholar 

  • Hang D, Wang Q, Guo C, Chen Z, Yan Z (2012) Treatment of osteonecrosis of the femoral head with VEGF165 transgenic bone marrow mesenchymal stem cells in mongrel dogs. Cells Tissues Organs 195:495–506

    Article  CAS  PubMed  Google Scholar 

  • Harman R, Carlson K, Gaynor J, Gustafson S, Dhupa S, Clement K, Hoelzler M, McCarthy T, Schwartz P, Adams C (2016) A prospective, randomized, masked, and placebo-controlled efficacy study of intraarticular allogeneic adipose stem cells for the treatment of osteoarthritis in dogs. Front Vet Sci 3:81

    Article  PubMed  PubMed Central  Google Scholar 

  • Hattori T, Muller C, Gebhard S, Bauer E, Pausch F, Schlund B, Bosl MR, Hess A, Surmann-Schmitt C, von der Mark H et al (2010) SOX9 is a major negative regulator of cartilage vascularization, bone marrow formation and endochondral ossification. Development 137(6):901–911

    Article  CAS  PubMed  Google Scholar 

  • Hegewald AA, Ringe J, Bartel J, Krüger I, Notter M, Barnewitz D, Kaps C, Sittinger M (2004) Hyaluronic acid and autologous synovial fluid induce chondrogenic differentiation of equine mesenchymal stem cells: a preliminary study. Tissue Cell 36:431–438

    Article  CAS  PubMed  Google Scholar 

  • Heinola T, Jukola E, Näkki P, Sukura A (2006) Consequences of hazardous dietary calcium deficiency for fattening bulls. Acta Vet Scand 48:25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hendawy H, Uemura A, Ma D, Namiki R, Samir H, Ahmed MF, Elfadadny A, El-Husseiny HM, Chieh-Jen C, Tanaka R (2021) Tissue harvesting site effect on the canine adipose stromal vascular fraction quantity and quality. Animals 11:460

    Article  PubMed  PubMed Central  Google Scholar 

  • Heo S-J, Thorpe SD, Driscoll TP, Duncan RL, Lee DA, Mauck RL (2015) Biophysical regulation of chromatin architecture instills a mechanical memory in Mesenchymal stem cells. Sci Rep 5:16895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hindle P, Baily J, Khan N, Biant LC, Simpson AHR, Péault B (2016) Perivascular mesenchymal stem cells in sheep: characterization and autologous transplantation in a model of articular cartilage repair. Stem Cells Dev 25(21):1659–1669

    Article  CAS  PubMed  Google Scholar 

  • Hotham WE, Thompson C, Szu-Ting L, Henson FMD (2021) The anti-inflammatory effects of equine bone marrow stem cell-derived extracellular vesicles on autologous chondrocytes. Vet Rec Open 8:e22

    Article  PubMed  PubMed Central  Google Scholar 

  • Houard X, Goldring MB, Berenbaum F (2013) Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis. Curr Rheumatol Rep 15:375–385

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huňáková K, Hluchý M, Špakováb T, Matejová J, Mudroňová D, Kuricová M, Rosocha J, Ledecký V (2020) Study of bilateral elbow joint osteoarthritis treatment using conditioned medium from allogeneic adipose tissue-derived MSCs in Labrador retrievers. Res Vet Sci 132:513–520

    Article  PubMed  CAS  Google Scholar 

  • Hunziker EB (1999) Biological repair of articular cartilage. Clin Orthop 367:135–146

    Article  Google Scholar 

  • Hwang NS, Varghese S, Li H, Elisseeff J (2011) Regulation of osteogenic and chondrogenic differentiation of mesenchymal stem cells in PEG-ECM hydrogels. Cell Tissue Res 344:499–509

    Article  CAS  PubMed  Google Scholar 

  • Iacono E, Pascucci L, Bazzucchi C, Cunto M, Ricci F, Rossi B, Merlo B (2018) Could hypoxia influence basic biological properties and ultrastructural features of adult canine mesenchymal stem/stromal cells? Vet Res Commun 42(4):297–308

    Article  PubMed  Google Scholar 

  • Inui T, Haneda S, Sasaki M, Furuoka H, Ito M, Yanagawa M, Hiyama M, Tabata Y, Sasaki N (2019) Enhanced chondrogenic differentiation of equine bone marrow-derived mesenchymal stem cells in zirconia microwell substrata. Res Vet Sci 125:345–350

    Article  CAS  PubMed  Google Scholar 

  • Ito T, Sawada R, Fujiwara Y, Tsuchiya T (2008) FGF-2 increases osteogenic and chondrogenic differentiation potentials of human mesenchymal stem cells by inactivation of TGF-β signaling. Cytotechnology 56:1

    Article  CAS  PubMed  Google Scholar 

  • Juneau C, Paine R, Chicas E, Gardner E, Bailey L, McDermott J (2016) Current concepts in treatment of patellofemoral osteochondritis dissecans. Int J Sports Phys Ther 11(6):903–925

    PubMed  PubMed Central  Google Scholar 

  • Jurgens WJFM, Kroeze RJ, Zandieh-Doulabi B, van Dijk A, Renders GAP, Smit T, van Milligen FJ, Ritt MJ, Helder MN (2013) One-step surgical procedure for the treatment of osteochondral defects with adipose-derived stem cells in a Caprine knee defect: a pilot study. BioRes Open Access 2(4):315–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kafarnik C, McClellan A, Dziasko M, Daniels JT, Guest DJ (2020) Canine corneal stromal cells have multipotent mesenchymal stromal cell properties in vitro. Stem Cells Dev 29(7):429–435

    Article  CAS  Google Scholar 

  • Kaggie JD, Markides H, Graves MJ, MacKay J, Houston G, El Haj A, Gilbert F, Henson F (2020) Ultra short echo time MRI of iron-labelled mesenchymal stem cells in an ovine osteochondral defect model. Sci Rep 10:8451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamm JL, Parlane NA, Riley CB, Gee EK, Dittmer KE, McIlwraith CW (2019) Blood type and breed-associated differences in cell marker expression on equine bone marrow-derived mesenchymal stem cells including major histocompatibility complex class II antigen expression. PLoS One 14(11):e0225161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katja N, Michaela E, Jochen R, Bernd F, Rudi M, Thomas H et al (2007) BMP7 promotes adipogenic but not osteo−/chondrogenic differentiation of adult human bone marrow-derived stem cells in high-density micro-mass culture. J Cell Biochem 102(3):626–637

    Article  CAS  Google Scholar 

  • Kazemi D, Asenjan S, Dehdilani K, Parsa H (2017) Canine articular cartilage regeneration using mesenchymal stem cells seeded on platelet rich fibrin. Bone Joint Res 6:98–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H-R, Lee J, Byeon JS, Gu N-Y, Lee J, Cho I-S, Cha S-H (2017) Extensive characterization of feline intra-abdominal adipose-derived mesenchymal stem cells. J Vet Sci 18(3):299–306

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim KH, Park TS, Cho B-W, Kim TM (2020) Nanoparticles from equine fetal bone marrow-derived cells enhance the survival of injured chondrocytes. Animals 10:1723

    Article  PubMed Central  Google Scholar 

  • Kim YS, Kim YI, Koh YG (2021) Intra-articular injection of human synovium-derived mesenchymal stem cells in beagles with surgery-induced osteoarthritis. Knee 28:159–168

    Article  PubMed  Google Scholar 

  • Knippenberg M, Helder M, Doulabi BZ, Semeins CM, Wuisman PIJM, Klein-Nulend J (2006) Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochem Biophys Res Commun 342:902–908

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Yamaoka K, Sonomoto K, Fukuyo S, Oshita K, Okada Y, Tanaka Y (2013) IL-17 inhibits chondrogenic differentiation of human mesenchymal stem cells. PLoS One 8(11):e79463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Korchunjit W, Laikul A, Taylor J, Watchararat K, Ritruechai P, Supokawej A, Wongtawan T (2019) Characterisation and allogeneic transplantation of equine bone marrow derived multipotent mesenchymal stromal cells collected from cadavers. J Equine Vet Sci 73:15–23

    Article  Google Scholar 

  • Kriston-Pál É, Czibula Á, Gyuris Z, Balka G, Seregi A, Sükösd F, Süth M, Kiss-Tóth E, Haracska L, Uher F, Monostori É (2017) Characterization and therapeutic application of canine adipose mesenchymal stem cells to treat elbow osteoarthritis. Can J Vet Res 81:73–78

    PubMed  PubMed Central  Google Scholar 

  • Lam J, Lu S, Lee EJ, Trachtenberg JE, Meretoja VV, Dahlin RL, van den Beucken JJJP, Tabata Y, Wong ME, Jansen JA, Mikos AG, Kasper FK (2014) Osteochondral defect repair using bilayered hydrogels encapsulating both chondrogenically and osteogenically pre-differentiated mesenchymal stem cells in a rabbit model. Osteoarthritis Cartilage 22(9):1291–1300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamani TSD, Ranganath L, Nagaraja BN, Satyanarayana ML, Jamuna KV, Kamran A (2019) Incidence of osteoarthritis in dogs—a clinical study of 64 patients. Int J Sci Environ Technol 8(3):559–564

    Google Scholar 

  • Lara E, Velásquez A, Cabezas J, Rivera N, Pacha P, Rodríguez-Alvarez L, Saravia F, Castro FO (2017) Endometritis and in vitro PGE2 challenge modify properties of cattle endometrial mesenchymal stem cells and their transcriptomic profile. Stem Cells Int 2017:4297639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larsson S, Englund M, Struglics A, Lohmander LS (2015) Interleukin-6 and tumor necrosis factor alpha in synovial fluid are associated with progression of radiographic knee osteoarthritis in subjects with previous meniscectomy. Osteoarthritis Cartilage 23:1906–1914

    Article  CAS  PubMed  Google Scholar 

  • Lee WD, Hurtig MB, Pilliar RM, Stanford WL, Kandel RA (2015) Engineering of hyaline cartilage with a calcified zone using bone marrow stromal cells. Osteoarthritis Cartilage 23(8):1307–1315

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Byeon JS, Lee KS, Gu N-Y, Lee GB, Kim H-R, Cho I-S, Cha S-H (2016) Chondrogenic potential and anti-senescence effect of hypoxia on canine adipose mesenchymal stem cells. Vet Res Commun 40(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26(3):146–155

    Article  CAS  PubMed  Google Scholar 

  • Leung VYL, Gao B, Leung KKH, Melhado IG, Wynn SL, Au TYK, Dung NWF, Lau JYB, Mak ACY, Chan D et al (2011) SOX9 governs differentiation stage-specific gene expression in growth plate chondrocytes via direct concomitant transactivation and repression. PLoS Genet 7(11):e1002356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levato R, Webb WR, Otto IA, Mensinga A, Zhang Y, van Rijen M, van Weeren R, Khan IM, Malda J (2017) The bio in the ink: cartilage regeneration with bioprintable hydrogels and articular cartilage-derived progenitor cells. Acta Biomater 61:41–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Duan X, Fan Z, Chen L, Xing F, Xu Z, Chen Q, Xiang Z (2018) Mesenchymal stem cells in combination with hyaluronic acid for articular cartilage defects. Sci Rep 8:9900

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu S, Sun Y, Chen T, Tao H, Hu Y, Chen S, Chen J (2018) Time from injury to surgery affects graft maturation following posterior cruciate ligament reconstruction with remnant preservation: a magnetic resonance imaging-based study. Art Ther 34:2846–2854

    Google Scholar 

  • Lima VP, Tobin GC, de Jesus Pereira MR, Silveira MD, Witz MI, Nardi NB (2019) Chondrogenic effect of liquid and gelled platelet lysate on canine adipose-derived mesenchymal stromal cells. Res Vet Sci 124:393–398

    Article  CAS  PubMed  Google Scholar 

  • Loeser RF (2011) Aging and osteoarthritis. Curr Opin Rheumatol 23:492–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lozito TP, Tuan RS (2011) Mesenchymal stem cells inhibit both endogenous and exogenous MMPs via secreted TIMPs. J Cell Physiol 226:385–396

    Article  CAS  PubMed  Google Scholar 

  • Lv X, He J, Zhang X, Luo X, He N, Sun Z, Xia H, Liu V, Zhang L, Lin X, Lin L, Yin H, Jiang D, Cao W, Wang R, Zhou G, Wang W (2018) Comparative efficacy of autologous stromal vascular fraction and autologous adipose-derived mesenchymal stem cells combined with hyaluronic acid for the treatment of sheep osteoarthritis. Cell Transplant 27(7):1111–1125

    Article  PubMed  PubMed Central  Google Scholar 

  • Magri C, Schramme M, Febre M, Cauvin E, Labadie F, Saulnier N, Francois I, Lechartier A, Aebischer D, Moncelet A-S, Maddens S (2019) Comparison of efficacy and safety of single versus repeated intra-articular injection of allogeneic neonatal mesenchymal stem cells for treatment of osteoarthritis of the metacarpophalangeal/metatarsophalangeal joint in horses: a clinical pilot study. PLoS One 14(8):e0221317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malagola E, Teunissen M, van der Laan LJ, Verstegen MM, Schotanus BA, van Steenbeek FG, Penning LC, van Wolferen ME, Tryfonidou MA, Spee B (2016) Stem characterization and comparison of canine multipotent stromal cells derived from liver and bone marrow. Stem Cells Dev 25(2):139–150

    Article  CAS  PubMed  Google Scholar 

  • Mancini IAD, Schmidt S, Brommer H, Pouran B, Schäfer S, Tessmar J et al (2020) A composite hydrogel-3D printed thermoplast osteochondral anchor as an example for a zonal approach to cartilage repair: in vivo performance in a long-term equine model. Biofabrication 12(3):035028

    Article  CAS  PubMed  Google Scholar 

  • Mancuso P, Raman S, Glynn A, Barry F, Murphy JM (2019) Mesenchymal stem cell therapy for osteoarthritis: the critical role of the cell secretome. Front Bioeng Biotechnol 7:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Maniwa S, Ochi M, Motomura T, Nishikori T, Chen J, Naora H (2001) Effects of hyaluronic acid and basic fibroblast growth factor on motility of chondrocytes and synovial cells in culture. Acta Orthop Scand 72:299–303

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Lorenzo MJ, Royo-Cañas M, Alegre-Aguarón E, Desportes P, Castiella T, García-Alvarez F, Larrad L (2009) Phenotype and chondrogenic differentiation of mesenchymal cells from adipose tissue of different species. J Orthop Res 27(11):1499–1507

    Article  PubMed  Google Scholar 

  • Marx C, Silveira MD, Selbach I, da Silva AS, Gomes de Macedo Braga LM, Camassola M, Nardi NB (2014) Acupoint injection of autologous stromal vascular fraction and allogeneic adipose-derived stem cells to treat hip dysplasia in dogs. Stem Cells Int 2014:391274

    Article  PubMed  PubMed Central  Google Scholar 

  • Mathiessen A, Conaghan PG (2017) Synovitis in osteoarthritis: current understanding with therapeutic implications. Arthritis Res Ther 19:18–27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mauck RL, Yuan X, Tuan RS (2006) Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 14(2):179–189

    Article  CAS  PubMed  Google Scholar 

  • Mazzotti E, Teti G, Falconi M, Chiarini F, Barboni B, Mazzotti A, Muttini A (2019) Age-related alterations affecting the chondrogenic differentiation of synovial fluid mesenchymal stromal cells in an equine model. Cells 8(10):1116

    Article  CAS  PubMed Central  Google Scholar 

  • McCorry MC, Bonassar LJ (2017) Fiber development and matrix production in tissue engineered menisci using bovine mesenchymal stem cells and fibrochondrocytes. Connect Tissue Res 58(3–4):329–341

    Article  CAS  PubMed  Google Scholar 

  • McCorry MC, Puetzer JL, Bonassar LJ (2016) Characterization of mesenchymal stem cells and fibrochondrocytes in three-dimensional co-culture: analysis of cell shape, matrix production, and mechanical performance. Stem Cell Res Ther 12(7):39

    Article  CAS  Google Scholar 

  • McIlwraith CW, Frisbie DD, Rodkey WG et al (2011) Evaluation of intraarticular mesenchymal stem cells to augment healing of microfractured chondral defects. Arthroscopy 27:1552–1561

    Article  PubMed  Google Scholar 

  • Messaoudi O, Henrionnet C, Bourge K, Loeuille D, Gillet P, Pinzano A (2021) Stem cells and extrusion 3D printing for hyaline cartilage engineering. Cells 10:2

    Article  CAS  Google Scholar 

  • Miki S, Takao M, Miyamoto W, Matsushita T, Kawano H (2015) Intra-articular injection of synovium-derived mesenchymal stem cells with hyaluronic acid can repair articular cartilage defects in a canine model. J Stem Cell Res Ther 5:11

    Article  CAS  Google Scholar 

  • Mocchi M, Bari E, Dotti S, Villa R, Berni P, Conti V, Del Bue M, Squassino GP, Segale L, Ramoni R, Torre ML, Perteghella S, Grolli S (2021a) Canine mesenchymal cell lyosecretome production and safety evaluation after allogenic intraarticular injection in osteoarthritic dogs. Animals 11:3271

    Article  PubMed  PubMed Central  Google Scholar 

  • Mocchi M, Grolli S, Dotti S, Di Silvestre D, Villa R, Berni P, Conti V, Passignani G, Brambilla F, Bue MD, Catenacci L, Sorrenti M, Segale L, Bari E, Mauri P, Torre ML, Perteghella S (2021b) Equine mesenchymal stem/stromal cells freeze-dried secretome (lyosecretome) for the treatment of musculoskeletal diseases: production process validation and batch release test for clinical use. Pharmaceuticals (Basel). 14(6):553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mrugala D, Bony C, Neves N, Caillot L, Fabre S, Moukoko D, Jorgensen C, Noël D (2008) Phenotypic and functional characterisation of ovine mesenchymal stem cells: application to a cartilage defect model. Ann Rheum Dis 67:288–295

    Article  CAS  PubMed  Google Scholar 

  • Murphy JM, Fink DJ, Hunziker EB, Barry FP (2003) Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48(12):3464–3474

    Article  PubMed  Google Scholar 

  • Music E, Futrega K, Doran MR (2018) Sheep as a model for evaluating mesenchymal stem/stromal cell (MSC)-based chondral defect repair. Osteoarthritis Cartilage 26:730–740

    Article  CAS  PubMed  Google Scholar 

  • Nam HY, Karunanithi P, Poh Loo WC, Naveen SV, Chen HC, Hussin P, Chan L, Kamarul T (2013) The effects of staged intra-articular injection of cultured autologous mesenchymal stromal cells on the repair of damaged cartilage: a pilot study in caprine model. Arthr Res Ther 15:R129

    Article  CAS  Google Scholar 

  • Nicpoń J, Marycz K, Grzesiak J (2013) Therapeutic effect of adipose-derived mesenchymal stem cell injection in horses suffering from bone spavin. Pol J Vet Sci 16(4):753–754

    Article  PubMed  Google Scholar 

  • Noel D, Caton D, Roche S, Bony C, Lehmann S, Casteilla L, Jorgensen C, Cousin B (2008) Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp Cell Res 314:1575–1584

    Article  CAS  PubMed  Google Scholar 

  • Ogueta S, Muñoz J, Obregon E, Delgado-Baeza E, García-Ruiz JP (2002) Prolactin is a component of the human synovial liquid and modulates the growth and chondrogenic differentiation of bone marrow-derived mesenchymal stem cells. Mol Cell Endocrinol 190(1-2):51–63

    Article  CAS  PubMed  Google Scholar 

  • Oh J, Son YS, Kim WH, Kwon O-K, Kang B-J (2021) Mesenchymal stem cells genetically engineered to express platelet-derived growth factor and heme oxygenase-1 ameliorate osteoarthritis in a canine model. J Orthop Surg Res 16(1):43

    Article  PubMed  PubMed Central  Google Scholar 

  • Okazaki R, Sakai A, Uezono Y, Ootsuyama A, Kunugita N, Nakamura T, Norimura T (2001) Sequential changes in transforming growth factor (TGF)-beta1 concentration in synovial fluid and mRNA expression of TGF-beta1 receptors in chondrocytes after immobilization of rabbit knees. J Bone Miner Metab 19(4):228–235

    Article  CAS  PubMed  Google Scholar 

  • Olsen A, Johnson V, Webb T, Santangelo KS, Dow S, Duerr FM (2019) Evaluation of intravenously delivered allogeneic mesenchymal stem cells for treatment of elbow osteoarthritis in dogs: a pilot study. Vet Comp Orthop Traumatol 32(3):173–181

    Article  PubMed  Google Scholar 

  • Ongaro A, Pellati A, Setti S, Masieri FF, Aquila G, Fini M, Caruso A, De Mattei M (2012) Electromagnetic fields counteract IL-1b activity during chondrogenesis of bovine mesenchymal stem cells. J Tissue Eng Regen Med 9(12):E229–E238

    Article  PubMed  CAS  Google Scholar 

  • Park Y, Sugimoto M, Watrin A, Chiquet M, Hunziker EB (2005) BMP-2 induces the expression of chondrocyte-specific genes bovine synovium-derived progenitor cells cultured in three-dimensional alginate hydrogel. Osteoarthritis Cartilage 13:527–536

    Article  CAS  PubMed  Google Scholar 

  • Peach RJ, Hollenbaugh D, Stamenkovic I, Aruffo A (1993) Identification of hyaluronic acid binding sites in the extracellular domain of CD44. J Cell Biol 122(1):257–264

    Article  CAS  PubMed  Google Scholar 

  • Pedersen NC, Morgan JP, Vasseur PB (2000) Canine rheumatoid arthritis. In: Ettinger SJ, Feldman EC (eds) Textbook of veterinary internal medicine: diseases of the dog and cat, vol 1, 5th edn. W.B. Saunders Company, Philadelphia, p 1879

    Google Scholar 

  • Pei Y, Fan J-J, Zhang X-Q, Zhang Z-Y, Yu M (2014) Repairing the osteochondral defect in goat with the tissue-engineered osteochondral graft preconstructed in a double-chamber stirring bioreactor. BioMed Res Int 2014:219203

    Article  PubMed  PubMed Central  Google Scholar 

  • Persson Y, Soderquist L, Ekman S (2007) Joint disorder; a contributory cause to reproductive failure in beef bulls? Acta Vet Scand 49:31

    Article  PubMed  PubMed Central  Google Scholar 

  • Pezzanite LM, Fortier LA, Antczak DF, Cassano JM, Brosnahan MM, Miller D, Schnabel LV (2015) Equine allogeneic bone marrow-derived mesenchymal stromal cells elicit antibody responses in vivo. Stem Cell Res Ther 6:54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pigott JH, Ishihara A, Wellman ML, Russell DS, Bertone AL (2013) Inflammatory effects of autologous, genetically modified autologous, allogeneic, and xenogeneic mesenchymal stem cells after intra-articular injection in horses. Vet Comp Orthop Traumatol 26(6):453–460

    Article  CAS  PubMed  Google Scholar 

  • Port J, Jackson DW, Lee TQ, Simon TM (1996) Meniscal repair supplemented with exogenous fibrin clot and autogenous cultured marrow cells in the goat model. Am J Sports Med 24(4):547–555

    Article  CAS  PubMed  Google Scholar 

  • Prins H-J, Fernandes H, Rozemuller H, van Blitterswijk C, de Boer J, Martens ACM (2016) Spatial distribution and survival of human and goat mesenchymal stromal cells on hydroxyapatite and β-tricalcium phosphate. J Tissue Eng Reg Med 10:233–244

    Article  CAS  Google Scholar 

  • Punwar S, Khan WS (2011) Mesenchymal stem cells and articular cartilage repair: clinical studies and future direction. Open Orthop J 5(1):296–301

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiang Y, Yanhong Z, Jiang P, Shibi L, Quanyi G, Xinlong M, Qun X, Baoshan X, Bin Z, Aiyuan W, Li Z, Wengjing X, Chao Z (2014) Xenoimplantation of an extracellular-matrix-derived, biphasic, cell-scaffold construct for repairing a large femoral-head high-load-bearing osteochondral defect in a canine model. Scientific World Journal 2014:127084

    Article  PubMed  PubMed Central  Google Scholar 

  • Rackwitz L, Djouad F, Janjanin S, Nöth U, Tuan RS (2014) Functional cartilage repair capacity of de-differentiated, chondrocyte- and mesenchymal stem cell-laden hydrogels in vitro. Osteoarthritis Cartilage 22(8):1148–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raheja LF, Galuppo LD, Bowers-Lepore J, Dowd JP, Tablin F, Yelowley CE (2011) Treatment of bilateral medial femoral condyle articular cartilage fissures in a horse using bone marrow-derived multipotent mesenchymal stromal cells. J Equine Vet Sci 31:147–154

    Article  Google Scholar 

  • Rakic R, Bourdon B, Demoor M, Maddens S, Saulnier N, Galéra P (2020) Differences in the intrinsic chondrogenic potential of equine umbilical cord matrix and cord blood mesenchymal stromal/stem cells for cartilage regeneration. Sci Rep 10(1):12075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reesink HL, Sutton RM, Shurer CR et al (2017) Galectin-1 and galectin-3 expression in equine mesenchymal stromal cells (MSCs), synovial fibroblasts and chondrocytes, and the effect of inflammation on MSC motility. Stem Cell Res Ther 8:243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reich CM, Raabe O, Wenisch S, Bridger PS, Kramer M, Arnhold S (2012) Isolation, culture and chondrogenic differentiation of canine adipose tissue- and bone marrow-derived mesenchymal stem cells—a comparative study. Vet Res Commun 36(2):139–148

    Article  PubMed  Google Scholar 

  • Rosa VS, Apolonio EVP, Rossi MC, Constantino LV, de Melo TR, Fonseca-Alves CE, Garcia Alves AL (2021) Encapsulated allogeneic synovial membrane mesenchymal stem cells provide better outcomes of chondral lesions in horses. Stem Cell Res Ther. https://doi.org/10.21203/rs.3.rs-587036/v2

  • Rose R (1977) An analysis of conditions causing lameness in the horse. In: 54th Annual meeting of the Australian Veterinary Association, pp 99–102

    Google Scholar 

  • Sabry D, Shamaa A, Amer M, El-Tookhy O, Abdallah A, Abd El Hassib DM, Amer E, Elamir A (2018) The effect of mesenchymal stem cell derived microvesicles in repair of femoral chondral defects in dogs. J Musculoskelet Res 21(2):1850006

    Article  Google Scholar 

  • Sadeesh EM, Shah F, Yadav PS (2016) Differential developmental competence and gene expression patterns in buffalo (Bubalus bubalis) nuclear transfer embryos reconstructed with fetal fibroblasts and amnion mesenchymal stem cells. Cytotechnology 68(5):1827–1848

    Article  CAS  Google Scholar 

  • Sah RL, Ratcliffe A (2010) Translational models for musculoskeletal tissue engineering and regenerative medicine. Tissue Eng Part B Rev 16(1):1–3

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Adams J, Leddy HA, McNulty AL, O’Conor CJ, Guilak F (2014) The mechanobiology of articular cartilage: bearing the burden of osteoarthritis. Curr Rheumatol Rep 16:451–460

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanjurjo-Rodríguez C, Castro-Viñuelas R, Hermida-Gómez T, Fernández-Vázquez T, Fuentes-Boquete IM, de Toro-Santos FJ, Díaz-Prado SM, Blanco-García FJ (2017) Ovine mesenchymal stromal cells: morphologic, phenotypic and functional characterization for osteochondral tissue engineering. PLoS One 12(1):e0171231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santos VH, Pfeifer JPH, de Souza JB, Milani BHG, de Oliveira RA, Assis MG, Deffune E, Moroz A, Garcia Alves AL (2018) Culture of mesenchymal stem cells derived from equine synovial membrane in alginate hydrogel microcapsules. BMC Vet Res 14:114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sasaki A, Mizuno M, Ozeki N, Katano H, Otabe K, Tsuji K, Koga H, Mochizuki M, Sekiya I (2018) Canine mesenchymal stem cells from synovium have a higher chondrogenic potential than those from infrapatellar fat pad, adipose tissue, and bone marrow. PLoS One 13(8):e0202922

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scanzello CR, Goldring SR (2012) The role of synovitis in osteoarthritis pathogenesis. Bone 51:249–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt S, Abinzano F, Mensinga A, Teßmar J, Groll J, Malda J, Levato R, Blunk T (2020) Differential production of cartilage ECM in 3D agarose constructs by equine articular cartilage progenitor cells and mesenchymal stromal cells. Int J Mol Sci 21(19):7071

    Article  CAS  PubMed Central  Google Scholar 

  • Shah K, Drury T, Roic I, Hansen P, Malin M, Boyd R, Sumer H, Ferguson R (2018) Outcome of allogeneic adult stem cell therapy in dogs suffering from osteoarthritis and other joint defects. Stem Cells Int 2018:7309201

    Article  PubMed  PubMed Central  Google Scholar 

  • Simonaro CM, Sachot S, Ge Y, He X, DeAngelis VA, Eliyahu E, Leong D, Sun HB, Mason JB, Haskins ME, Richardson DW, Schuchman EH (2013) Acid ceramidase maintains the chondrogenic phenotype of expanded primary chondrocytes and improves the chondrogenic differentiation of bone marrow-derived mesenchymal stem cells. PLoS One 8(4):e62715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith GK, Paster ER, Powers MY, Lawler DE, Biery DN, Shofer FS et al (2006) Lifelong diet restriction and radiographic evidence of osteoarthritis of the hip joint in dogs. J Am Vet Med Assoc. 229:690–693

    Article  PubMed  Google Scholar 

  • Somal A, Bhat IA, Baiju I, Pandey S, Panda BSK, Thakur N, Sarkar M, Chandra V, Saikumar G, Sharma GT (2016) A comparative study of growth kinetics, in vitro differentiation potential and molecular characterization of fetal adnexa derived caprine mesenchymal stem cells. PLoS One 11(6):e0156821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Somal A, Bhat IA, Baiju I, Singh AP, Panda BSK, Desingu PA, Pandey S, Bharti MK, Pal A, Saikumar G, Chandra V, Sharma GT (2017) Impact of cryopreservation on caprine fetal adnexa derived stem cells and its evaluation for growth kinetics, phenotypic characterization and wound healing potential in xenogenic rat model. J Cell Physiol 232(8):2186–2200

    Article  CAS  PubMed  Google Scholar 

  • Song F, Tang J, Geng R, Hu H, Zhu C, Cui W, Fan W (2014) Comparison of the efficacy of bone marrow mononuclear cells and bone mesenchymal stem cells in the treatment of osteoarthritis in a sheep model. Int J Clin Exp Pathol 7:1415–1426

    PubMed  PubMed Central  Google Scholar 

  • Spaas JH, Oosterlinck M, Broeckx S, Dumoulin M, Saunders J, Van Soom A, Pille F, Van de Walle GR (2012) Treatment of equine degenerative joint disease with autologous peripheral blood-derived mesenchymal stem cells: a case report. Vlaams Diergeneeskundig Tijdschrift 81

    Google Scholar 

  • Sreekumar TR, Ansari MM, Chandra VG, Sharma T (2014) Isolation and characterization of buffalo Wharton’s jelly derived mesenchymal stem cells. J Stem Cell Res Ther 4:207

    Google Scholar 

  • Stannus O, Jones G, Cicuttini F (2010) Circulating levels of IL-6 and TNF-alpha are associated with knee radiographic osteoarthritis and knee cartilage loss in older adults. Osteoarthtitis Cartilage 18:1441–1447

    Article  CAS  Google Scholar 

  • Sun J, Lyu J, Xing F, Chen R, Duan X, Xiang Z (2020) A biphasic, demineralized, and decellularized allograft bone-hydrogel scaffold with a cell-based BMP-7 delivery system for osteochondral defect regeneration. J Biomed Mater Res 108:1909–1921

    Article  CAS  Google Scholar 

  • Taghavi M, Parham A, Raji A (2020) The combination of TGF-β3 and BMP-6 synergistically promotes the chondrogenic differentiation of equine bone marrow-derived mesenchymal stem cells. Int J Pept Res Ther 26:727–735

    Article  CAS  Google Scholar 

  • Terraciano V, Hwang N, Moroni L, Park HB, Zhang Z, Mizrahi J, Seliktar D, Elisseeff J (2007) Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 25:2730–2738

    Article  CAS  PubMed  Google Scholar 

  • Teunissen M, Verseijden F, Riemers FM, van Osch GJVM, Tryfonidou MA (2020) The lower in vitro chondrogenic potential of canine adipose tissue-derived mesenchymal stromal cells (MSC) compared to bone marrow derived MSC is not improved by BMP-2 or BMP-6. Vet J 105605

    Google Scholar 

  • Tiwary R, Amarpal, Aithal HP, Kinjavdekar P, Pawde AM, Singh R (2014) Effect of IGF-1 and uncultured autologous bone-marrow-derived mononuclear cells on repair of osteochondral defect in rabbits. Cartilage 5:43–54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toh WS, Lim TC, Kurisawa M, Spector M (2012) Modulation of mesenchymal stem cell chondrogenesis in a tunable hyaluronic acid hydrogel microenvironment. Biomaterials 33:3835–3845

    Article  CAS  PubMed  Google Scholar 

  • Toh WS, Foldager CB, Olsen BR, Spector M (2013) Basement membrane molecule expression attendant to chondrogenesis by nucleus pulposus cells and mesenchymal stem cells. J Orthop Res 31:1136–1143

    Article  CAS  PubMed  Google Scholar 

  • Topol L, Chen W, Song H, Day TF, Yang Y (2009) Sox9 inhibits Wnt signaling by promoting beta-catenin phosphorylation in the nucleus. J Biol Chem 284(5):3323–3333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ude CC, Shamsul BS, Ng MH, Chen HC, Ohnmar H, Amaramalar SN, Ruszymah BHI (2018) Long-term evaluation of osteoarthritis sheep knee, treated with TGF-β3 and BMP-6 induced multipotent stem cells. Exp Gerontol 104:43–51

    Article  CAS  PubMed  Google Scholar 

  • Vahedi P, Jarolmasjed S, Shafaei H, Roshangar L, Rad JS, Ahmadian E (2019) In vivo articular cartilage regeneration through infrapatellar adipose tissue derived stem cell in nanofiber polycaprolactone scaffold. Tissue Cell 57:49–56

    Article  CAS  PubMed  Google Scholar 

  • Van Hecke L, Magri C, Duchateau L, Beerts C, Geburek F, Suls M, Da Dalt L, Patruno M, Saunders J, Broeckx S, Depuydt E, Spaas JH (2021) Repeated intra-articular administration of equine allogeneic peripheral blood-derived mesenchymal stem cells does not induce a cellular and humoral immune response in horses. Vet Immunol Immunopathol 239:110306

    Article  PubMed  CAS  Google Scholar 

  • Varghese S, Hwang NS, Canver AC, Theprungsrikul P, Lin DW, Elisseeff J (2008) Chondroitin sulphate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol 27:12–21

    Article  CAS  PubMed  Google Scholar 

  • Vickers SM, Gotterbarm T, Spector M (2010) Cross-linking affects cellular condensation and chondrogenesis in type II collagen-GAG scaffolds seeded with bone marrow-derived mesenchymal stem cells. J Orthop Res 28(9):1184–1192

    Article  CAS  PubMed  Google Scholar 

  • Vilar JM, Morales M, Santana A, Spinella G, Rubio M, Cuervo B, Cugat R, Carrillo JM (2013) Controlled, blinded force platform analysis of the effect of intraarticular injection of autologous adipose-derived mesenchymal stem cells associated to PRGF-Endoret in osteoarthritic dogs. BMC Vet Res 9:131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vilar JM, Batista M, Morales M, Santana A, Cuervo B, Rubio M, Cugat R, Sopena J, Carrillo JM (2014) Assessment of the effect of intraarticular injection of autologous adipose-derived mesenchymal stem cells in osteoarthritic dogs using a double blinded force platform analysis. BMC Vet Res 10:143

    Article  PubMed  PubMed Central  Google Scholar 

  • Vilar JM, Cuervo B, Rubio M, Sopena J, Domínguez JM, Santana A, Carrillo JM (2016) Effect of intraarticular inoculation of mesenchymal stem cells in dogs with hip osteoarthritis by means of objective force platform gait analysis: concordance with numeric subjective scoring scales. BMC Vet Res 12:223

    Article  PubMed  PubMed Central  Google Scholar 

  • Villatoro AJ, Hermida-Prieto M, Fernández V, Fariñas F, Alcoholado C, Rodríguez-García MI, Mariñas-Pardo L, Becerra J (2018) Allogeneic adipose-derived mesenchymal stem cell therapy in dogs with refractory atopic dermatitis: clinical efficacy and safety. Vet Rec 183(21):654

    Article  PubMed  Google Scholar 

  • Vivas D, Caminal M, Oliver-Vila I, Vives J (2018) Derivation of multipotent mesenchymal stromal cells from sheep bone marrow. Curr Protoc Stem Cell Biol 44(2B):9.1–9.22

    Google Scholar 

  • Wang C, Wang Z, Li A, Bai F, Lu J, Xu S, Li D (2010) Repair of segmental bone-defect of goat’s tibia using a dynamic perfusion culture tissue engineering bone. J Biomed Mat Res A 92:1145–1153

    Google Scholar 

  • Wang M, Peng Z, Vasiliev K (2013) Investigation of wear particles generated in human knee joints using atomic force microscopy. Tribol Lett 51:161–170

    Article  CAS  Google Scholar 

  • Wei FY, Lee JK, Wei L, Qu F, Zhang JZ (2017) Correlation of insulin-like growth factor 1 and osteoarthritic cartilage degradation: a spontaneous osteoarthritis in Guinea pig. Eur Rev Med Pharmacol Sci 21(20):4493–4500

    PubMed  PubMed Central  Google Scholar 

  • Wei X, Liu B, Liu G, Yang F, Cao F, Dou X, Yu W, Wang B, Zheng G, Cheng L, Ma Z, Zhang Y, Yang J, Wang Z, Li J, Cui D, Wang W, Xie H, Li L, Zhang F, Lineaweaver WC, Zhao D (2019) Mesenchymal stem cell-loaded porous tantalum integrated with biomimetic 3D collagen-based scaffold to repair large osteochondral defects in goats. Stem Cell Res Ther 10(1):72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White JL, Walker NJ, Hu JC, Borjesson DL, Athanasiou KA (2018) A comparison of bone marrow and cord blood mesenchymal stem cells for cartilage self-assembly. Tissue Eng Part A 24(15–16):1262–1272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitehouse M, Howells NR, Parry M, Austin E, Kafienah W, Brady K, Goodship AE, Eldridge JD, Blom AYW, Hollander AP (2017) Repair of torn avascular meniscal cartilage using undifferentiated autologous mesenchymal stem cells: from in vitro optimization to a first-in-human study. Stem Cells Transl Med 6(4):1237–1248

    Article  CAS  PubMed  Google Scholar 

  • Wilke MM, Nydam DV, Nixon AJ (2007) Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model. J Orthop Res 25:913–925

    Article  CAS  PubMed  Google Scholar 

  • Wolfe DF (2018) Abnormalities of the bull–occurrence, diagnosis and treatment of abnormalities of the bull, including structural soundness. Animal 1–10

    Google Scholar 

  • Xue JX, Gong YY, Zhou GD, Wei L, Cao LY, Zhang WJ (2012) Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells induced by acellular cartilage sheets. Biomaterials 33(24):5832–5840

    Article  CAS  PubMed  Google Scholar 

  • Yamada ALM, Carvalho AD, Moroz A, Watanabe MJ, Hussni CA, Rodrigues CA, Garcia Alves AL (2013) Mesenchymal stem cell enhances chondral defects healing in horses. Stem Cell Discov 3(4):218–225

    Article  CAS  Google Scholar 

  • Yamasaki S, Hashimoto Y, Takigami J, Terai S, Mera H, Nakamura H, Wakitani S (2015) Effect of the direct injection of bone marrow mesenchymal stem cells in hyaluronic acid and bone marrow stimulation to treat chondral defects in the canine model. Regen Ther 2:42–48

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamasaki A, Omura T, Murata D, Kobayashi M, Sunaga T, Kusano K, Ueno Y, Kuramoto T, Hobo S, Misumi K (2018) A pilot study of regenerative therapy by implanting synovium-derived mesenchymal stromal cells in equine osteochondral defect models. J Equine Sci 29(4):117–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazoe K, Mishima H, Torigoe K, Iijima H, Watanabe K, Sakai H, Kudo T (2007) Effects of atelocollagen gel containing bone marrow-derived stromal cells on repair of osteochondral defect in a dog. J Vet Med Sci 69(8):835–839

    Article  CAS  PubMed  Google Scholar 

  • Yaneselli KM, Kuhl CP, Terraciano PB, de Oliveira FS, Pizzato SB, Pazza K, Magrisso AB, Torman V, Rial A, Moreno M, Llambí S, Cirne-Lima E, Maisonnave J (2018) Comparison of the characteristics of canine adipose tissue-derived mesenchymal stem cells extracted from different sites and at different passage numbers. J Vet Sci 19(1):13–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Q, Peng J, Lu SB, Guo QY, Zhao B, Zhang L, Wang AY, Xu WJ, Xia Q, Ma XL, Hu YC, Xu BS (2011) Evaluation of an extracellular matrix-derived acellular biphasic scaffold/cell construct in the repair of a large articular high-load-bearing osteochondral defect in a canine model. Chin Med J (Engl) 124:3930–3938

    CAS  Google Scholar 

  • Yang CC, Lin CY, Wang HS, Lyu SR (2013) Matrix metalloproteases and tissue inhibitors of metalloproteinases in medial plica and pannuslike tissue contribute to knee osteoarthritis progression. PLoS One 8(11):e79662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin H, Wang Y, Sun Z, Sun X, Xu Y, Li P, Meng H, Yu X, Xiao B, Fan T, Wang Y, Xu W, Wang A, Guo Q, Peng J, Lu S (2016) Induction of mesenchymal stem cell chondrogenic differentiation and functional cartilage microtissue formation for in vivo cartilage regeneration by cartilage extracellular matrix-derived particles. Acta Biomater 33:96–109

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka M, Shimizu C, Harwood FL, Coutts RD, Amiel D (1997) The effects of hyaluronan during the development of osteoarthritis. Osteoarthritis Cartilage 5:251–260

    Article  CAS  PubMed  Google Scholar 

  • Zayed M, Caniglia C, Misk N, Dhar MS (2017) Donor-matched comparison of chondrogenic potential of equine bone marrow- and synovial fluid-derived mesenchymal stem cells: implications for cartilage tissue regeneration. Front Vet Sci 3:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Zayed M, Newby S, Misk N, Donnell R, Dhar M (2018) Xenogenic implantation of equine synovial fluid-derived mesenchymal stem cells leads to articular cartilage regeneration. Stem Cells Int 1073705

    Google Scholar 

  • Zayed M, Adair S, Dhar M (2021) Effects of normal synovial fluid and interferon gamma on chondrogenic capability and immunomodulatory potential respectively on equine mesenchymal stem cells. Int J Mol Sci 22(12):6391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeiter S, Lezuo P, Ito K (2009) Effect of TGF-β1, BMP-2 and hydraulic pressure on chondrogenic differentiation of bovine bone marrow mesenchymal stromal cells. Biorheology 46:45–55

    Article  CAS  PubMed  Google Scholar 

  • Zhai C, Zhang X, Chen J, He J, Fei H, Liu Y, Luo C, Fan W (2019) The effect of cartilage extracellular matrix particle size on the chondrogenic differentiation of bone marrow mesenchymal stem cells. Regen Med 14(7):663–680

    Article  CAS  PubMed  Google Scholar 

  • Zhang XL, Jiang XQ (2006) Osteoblastic differentiation of goat bone marrow stromal cells after AdBMP-2 mediated transduction in vitro. Shanghai Kou Qiang Yi Xue 15(6):610–613

    PubMed  Google Scholar 

  • Zhang X, Zhai C, Fei H, Liu Y, Wang Z, Luo C, Zhang J, Ding Y, Xu T, Fan W (2018a) Composite silk extracellular-matrix scaffolds for enhanced chondrogenesis of mesenchymal stem cells. Tissue Eng Part C Methods 24(11):645–658

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Liu S, Guo W, Wang M, Hao C, Gao S, Zhang X, Li X, Chen M, Jing X, Wang Z, Peng J, Lu S, Guo Q (2018b) Human umbilical cord Wharton’s jelly mesenchymal stem cells combined with an acellular cartilage extracellular matrix scaffold improve cartilage repair compared with microfracture in a caprine model. Osteoarthritis Cartilage 30077(18):S1063–S4584

    Google Scholar 

  • Zhang Y, Hao C, Guo W, Peng X, Wang M, Yang Z, Li X, Zhang X, Chen M, Sui X, Peng J, Lu S, Liu S, Guo Q, Jiang Q (2020) Co-culture of hWJMSCs and pACs in double biomimetic ACECM oriented scaffold enhances mechanical properties and accelerates articular cartilage regeneration in a caprine model. Stem Cell Res Ther 11(1):180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Zou T, Cui H, Lv Y, Gao D, Ruan C, Zhang X, Zhang Y (2020) Parathyroid hormone (1-34) promotes the effects of 3D printed scaffold-seeded bone marrow mesenchymal stem cells on meniscus regeneration. Stem Cell Res Ther 11:328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou G, Zheng Q, Engin F, Munivez E, Chen Y, Sebald E, Krakow D, Lee B (2006) Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc Natl Acad Sci U S A 103(50):19004–19009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu S, Zhang B, Man C, Ma Y, Hu J (2011) NELL like molecule-1 modified bone marrow mesenchymal stem cells/poly-lactic-co-glycolic acid composite improves repair of large osteochondral defects in mandibular condyle. Osteoarthritis Cartilage 19:743–750

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Wu W, Qu X (2021) Mesenchymal stem cells in osteoarthritis therapy: a review. Am J Transl Res 13(2):448–461

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zorzi AR, Amstalden EMI, Plepis AMG, Martins VCA, Ferretti M, Antonioli E, Duarte ASS, Luzo ACM, Miranda JB (2015) Effect of human adipose tissue mesenchymal stem cells on the regeneration of sheep articular cartilage. Int J Mol Sci 16:26813–26831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zscharnack M, Poesel C, Galle J, Bader A (2009) Low oxygen expansion improves subsequent Chondrogenesis of ovine bone-marrow-derived Mesenchymal stem cells in collagen type I hydrogel. Cells Tissues Organs 190:81–93

    Article  CAS  PubMed  Google Scholar 

  • Zscharnack M, Hepp P, Richter R, Aigner T, Schulz R, Somerson J, Josten C, Bader A, Marquass B (2010) Repair of chronic osteochondral defects using predifferentiated mesenchymal stem cells in an sheep model. Am J Sports Med 38(9):1857–1869

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Veterinary Clinical Complex, Faculty of Veterinary Sciences & Animal Husbandry, Sher-e-Kashmir University of Agricultural Sciences & Technology of Kashmir (SKUAST-K), Srinagar, Jammu and Kashmir, India

    Mudasir Bashir Gugjoo PhD

Authors
  1. Mudasir Bashir Gugjoo PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Gugjoo, M.B. (2022). Mesenchymal Stem Cells Therapeutic Applications in Cartilage Regeneration. In: Therapeutic Applications of Mesenchymal Stem Cells in Veterinary Medicine. Springer, Singapore. https://doi.org/10.1007/978-981-19-3277-9_1

Download citation

Publish with us

Policies and ethics

Search

Navigation