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Cell Therapies for Tendon: Treatments and Regenerative Medicine

  • Anthony Grognuz
  • Pierre-Arnaud Aeberhard
  • Murielle Michetti
  • Nathalie Hirt-Burri
  • Corinne Scaletta
  • Anthony de Buys Roessingh
  • Wassim Raffoul
  • Lee Ann Laurent-ApplegateEmail author
Chapter

Abstract

Tissue engineering and cell therapies are becoming realistic approaches for medical therapeutics and musculoskeletal applications have been among the first to benefit on a large scale. In this chapter, cell sources for tissue engineering for tendon pathologies are addressed. Cell therapies will be described for small defect tendon injuries, such as in the hand, which could adapt well to injectable cell administration along with matrix/scaffold solutions for larger defects. For cell sources, tenocytes, tendon sheath fibroblasts, bone marrow- or adipose-derived stem cells, tendon stem/progenitor cells, induced pluripotent stem cells, amniotic cells, placenta cells, and platelet derivatives have been proposed to enhance tendon regeneration. There are associated advantages and disadvantages for these different strategies. Evolving regulatory requirements have been progressive for use of cells in medicinal practice since the 1950s. Cell banking techniques to expand one cell source to very large stocks have already been described with progenitor cell types in the 1950s for vaccine production. Cellular therapies illustrating human progenitor tenocytes, along with their clinical cell banking potential, are presented as an alternative cell source solution. Potentially interesting therapeutic options can be improved with modern innovation for tendon regeneration and repair.

Keywords

Cell therapy Tenocyte Progenitor cells Tissue engineering Tendopathies Tendon healing 

Notes

Acknowledgements

We would like to thank the Foundation S.A.N.T.E. and Foundation Family Sandoz for financing, in part, our Progenitor Transplantation Program. We also would like to thank the Orthopedic Hospital Foundation for the continued support of our laboratory and students.

References

  1. 1.
    Kannus P, Jozsa L. Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg Am. 1991;73(10):1507–25.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Maffulli N, Barrass V, Ewen SW. Light microscopic histology of Achilles tendon ruptures. A comparison with unruptured tendons. Am J Sports Med. 2000;28(6):857–63.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Paavola M, Kannus P, Järvinen M. Epidemiology of tendon problems in sport. In: Maffulli N, Renström P, Leadbetter W, editors. Tendon Injuries. London: Springer; 2005. p. 32–9.CrossRefGoogle Scholar
  4. 4.
    Gaida JE, Alfredson H, Kiss ZS, Bass SL, Cook JL. Asymptomatic Achilles tendon pathology is associated with a central fat distribution in men and a peripheral fat distribution in women: a cross sectional study of 298 individuals. BMC Musculoskelet Disord. 2010;11:41.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Clayton RA, Court-Brown CM. The epidemiology of musculoskeletal tendinous and ligamentous injuries. Injury. 2008;39(12):1338–44.CrossRefGoogle Scholar
  6. 6.
    Egger AC, Berkowitz MJ. Achilles tendon injuries. Curr Rev Musculoskelet Med. 2017;10(1):72–80.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Kaux JF, Forthomme B, Goff CL, Crielaard JM, Croisier JL. Current opinions on tendinopathy. J Sports Sci Med. 2011;10(2):238–53.PubMedPubMedCentralGoogle Scholar
  8. 8.
    de Jong JP, Nguyen JT, Sonnema AJ, Nguyen EC, Amadio PC, Moran SL. The incidence of acute traumatic tendon injuries in the hand and wrist: a 10-year population-based study. Clin Orthop Surg. 2014;6(2):196–202.PubMedCentralCrossRefGoogle Scholar
  9. 9.
    Kannus P. Structure of the tendon connective tissue. Scand J Med Sci Sports. 2000;10(6):312–20.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Sharma P, Maffulli N. Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am. 2005;87(1):187–202.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Jozsa L, Kannus P, Balint JB, Reffy A. Three-dimensional ultrastructure of human tendons. Acta Anat (Basel). 1991;142(4):306–12.CrossRefGoogle Scholar
  12. 12.
    O’Brien M. Structure and metabolism of tendons. Scand J Med Sci Sports. 1997;7(2):55–61.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Voleti PB, Buckley MR, Soslowsky LJ. Tendon healing: repair and regeneration. Annu Rev Biomed Eng. 2012;14:47–71.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S. Where tendons and ligaments meet bone: attachment sites ('entheses') in relation to exercise and/or mechanical load. J Anat. 2006;208(4):471–90.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Apostolakos J, Durant TJ, Dwyer CR, Russell RP, Weinreb JH, Alaee F, Beitzel K, MB MC, Cote MP, Mazzocca AD. The enthesis: a review of the tendon-to-bone insertion. Muscles Ligaments Tendons J. 2014;4(3):333–42.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Thomopoulos S, Williams GR, Gimbel JA, Favata M, Soslowsky LJ. Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. J Orthop Res. 2003;21(3):413–9.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Mienaltowski MJ, Birk DE. Structure, physiology, and biochemistry of collagens. Adv Exp Med Biol. 2014;802:5–29.CrossRefGoogle Scholar
  18. 18.
    Nourissat G, Berenbaum F, Duprez D. Tendon injury: from biology to tendon repair. Nat Rev Rheumatol. 2015;11(4):223–33.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Elliott DH. Structure and Function of Mammalian Tendon. Biol Rev Camb Philos Soc. 1965;40:392–421.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Wang JH. Mechanobiology of tendon. J Biomech. 2006;39(9):1563–82.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Liu X, Wu H, Byrne M, Krane S, Jaenisch R. Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci U S A. 1997;94(5):1852–6.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    James R, Kesturu G, Balian G, Chhabra AB. Tendon: biology, biomechanics, repair, growth factors, and evolving treatment options. J Hand Surg Am. 2008;33(1):102–12.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Thomopoulos S, Genin GM, Galatz LM. The development and morphogenesis of the tendon-to-bone insertion - what development can teach us about healing. J Musculoskelet Neuronal Interact. 2010;10(1):35–45.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Young BB, Gordon MK, Birk DE. Expression of type XIV collagen in developing chicken tendons: association with assembly and growth of collagen fibrils. Dev Dyn. 2000;217(4):430–9.CrossRefGoogle Scholar
  25. 25.
    Izu Y, Ansorge HL, Zhang G, Soslowsky LJ, Bonaldo P, Chu ML, Birk DE. Dysfunctional tendon collagen fibrillogenesis in collagen VI null mice. Matrix Biol. 2011;30(1):53–61.CrossRefGoogle Scholar
  26. 26.
    Butler DL, Grood ES, Noyes FR, Zernicke RF. Biomechanics of ligaments and tendons. Exerc Sport Sci Rev. 1978;6:125–81.Google Scholar
  27. 27.
    Yoon JH, Halper J. Tendon proteoglycans: biochemistry and function. J Musculoskelet Neuronal Interact. 2005;5(1):22–34.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol. 1997;136(3):729–43.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Ameye L, Young MF. Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology. 2002;12(9):107R–16R.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Svensson L, Aszodi A, Reinholt FP, Fassler R, Heinegard D, Oldberg A. Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J Biol Chem. 1999;274(14):9636–47.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H. Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol. 1998;141(5):1277–86.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Jelinsky SA, Archambault J, Li L, Seeherman H. Tendon-selective genes identified from rat and human musculoskeletal tissues. J Orthop Res. 2010;28(3):289–97.Google Scholar
  33. 33.
    Shukunami C, Takimoto A, Oro M, Hiraki Y. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol. 2006;298(1):234–47.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development. 2007;134(14):2697–708.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Docheva D, Hunziker EB, Fassler R, Brandau O. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol. 2005;25(2):699–705.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Jozsa L, Lehto M, Kvist M, Balint JB, Reffy A. Alterations in dry mass content of collagen fibers in degenerative tendinopathy and tendon-rupture. Matrix. 1989;9(2):140–6.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Aydin A, Topalan M, Mezdegi A, Sezer I, Ozkan T, Erer M, Ozkan S. [Single-stage flexor tendoplasty in the treatment of flexor tendon injuries]. Acta Orthop Traumatol Turc. 2004;38(1):54–9.Google Scholar
  38. 38.
    Aurora A, McCarron J, Iannotti JP, Derwin K. Commercially available extracellular matrix materials for rotator cuff repairs: state of the art and future trends. J Shoulder Elbow Surg. 2007;16(5 Suppl):S171–8.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Verdan CE. Primary repair of flexor tendons. J Bone Joint Surg Am. 1960;42:647–57.CrossRefGoogle Scholar
  40. 40.
    Killian ML, Cavinatto L, Galatz LM, Thomopoulos S. The role of mechanobiology in tendon healing. J Shoulder Elbow Surg. 2012;21(2):228–37.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Gimbel JA, Van Kleunen JP, Williams GR, Thomopoulos S, Soslowsky LJ. Long durations of immobilization in the rat result in enhanced mechanical properties of the healing supraspinatus tendon insertion site. J Biomech Eng. 2007;129(3):400–4.CrossRefGoogle Scholar
  42. 42.
    Chen X, Song XH, Yin Z, Zou XH, Wang LL, Hu H, Cao T, Zheng M, Ouyang HW. Stepwise differentiation of human embryonic stem cells promotes tendon regeneration by secreting fetal tendon matrix and differentiation factors. Stem Cells. 2009;27(6):1276–87.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Watts AE, Yeager AE, Kopyov OV, Nixon AJ. Fetal derived embryonic-like stem cells improve healing in a large animal flexor tendonitis model. Stem Cell Res Ther. 2011;2(1):4.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Ferrara JL, Cooke KR, Teshima T. The pathophysiology of acute graft-versus-host disease. Int J Hematol. 2003;78(3):181–7.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Petersdorf EW, Shuler KB, Longton GM, Spies T, Hansen JA. Population study of allelic diversity in the human MHC class I-related MIC-A gene. Immunogenetics. 1999;49(7-8):605–12.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Mack GS. Osiris seals billion-dollar deal with Genzyme for cell therapy. Nat Biotechnol. 2009;27(2):106–7.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Miller School Physician/Scientists Receive $3M Grant to Treat Burn Wounds with Stem Cells. http://med.miami.edu/news/miller-school-physician-scientists-receive-3-million-defense-grant-to-treat. Accessed 9 Mar 2017
  48. 48.
    Ju YJ, Muneta T, Yoshimura H, Koga H, Sekiya I. Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing. Cell Tissue Res. 2008;332(3):469–78.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Lacitignola L, Crovace A, Rossi G, Francioso E. Cell therapy for tendinitis, experimental and clinical report. Vet Res Commun. 2008;32(Suppl 1):S33–8.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Nixon AJ, Dahlgren LA, Haupt JL, Yeager AE, Ward DL. Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis. Am J Vet Res. 2008;69(7):928–37.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Smith RK. Mesenchymal stem cell therapy for equine tendinopathy. Disabil Rehabil. 2008;30(20-22):1752–8.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Longo UG, Lamberti A, Petrillo S, Maffulli N, Denaro V. Scaffolds in tendon tissue engineering. Stem Cells Int. 2012;2012:517165.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Beredjiklian PK, Favata M, Cartmell JS, Flanagan CL, Crombleholme TM, Soslowsky LJ. Regenerative versus reparative healing in tendon: a study of biomechanical and histological properties in fetal sheep. Ann Biomed Eng. 2003;31(10):1143–52.PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Favata M, Beredjiklian PK, Zgonis MH, Beason DP, Crombleholme TM, Jawad AF, Soslowsky LJ. Regenerative properties of fetal sheep tendon are not adversely affected by transplantation into an adult environment. J Orthop Res. 2006;24(11):2124–32.CrossRefGoogle Scholar
  55. 55.
    Young M. Stem cell applications in tendon disorders: a clinical perspective. Stem Cells Int. 2012;2012:637836.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Ellera Gomes JL, da Silva RC, Silla LM, Abreu MR, Pellanda R. Conventional rotator cuff repair complemented by the aid of mononuclear autologous stem cells. Knee Surg Sports Traumatol Arthrosc. 2012;20(2):373–7.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Awad HA, Boivin GP, Dressler MR, Smith FN, Young RG, Butler DL. Repair of patellar tendon injuries using a cell-collagen composite. J Orthop Res. 2003;21(3):420–31.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Bi Y, Ehirchiou D, Kilts TM, Inkson CA, Embree MC, Sonoyama W, Li L, Leet AI, Seo BM, Zhang L, Shi S, Young MF. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med. 2007;13(10):1219–27.CrossRefGoogle Scholar
  59. 59.
    Xu W, Wang Y, Liu E, Sun Y, Luo Z, Xu Z, Liu W, Zhong L, Lv Y, Wang A, Tang Z, Li S, Yang L. Human iPSC-derived neural crest stem cells promote tendon repair in a rat patellar tendon window defect model. Tissue Eng Part A. 2013;19(21-22):2439–51.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Baksh N, Hannon CP, Murawski CD, Smyth NA, Kennedy JG. Platelet-rich plasma in tendon models: a systematic review of basic science literature. Art Ther. 2013;29(3):596–607.Google Scholar
  61. 61.
    Paoloni J, De Vos RJ, Hamilton B, Murrell GA, Orchard J. Platelet-rich plasma treatment for ligament and tendon injuries. Clin J Sport Med. 2011;21(1):37–45.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Taylor DW, Petrera M, Hendry M, Theodoropoulos JS. A systematic review of the use of platelet-rich plasma in sports medicine as a new treatment for tendon and ligament injuries. Clin J Sport Med. 2011;21(4):344–52.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Akhundov K, Pietramaggiori G, Waselle L, Darwiche S, Guerid S, Scaletta C, Hirt-Burri N, Applegate LA, Raffoul WV. Development of a cost-effective method for platelet-rich plasma (PRP) preparation for topical wound healing. Ann Burns Fire Disasters. 2012;25(4):207–13.PubMedCentralGoogle Scholar
  64. 64.
    Kadner A, Hoerstrup SP, Tracy J, Breymann C, Maurus CF, Melnitchouk S, Kadner G, Zund G, Turina M. Human umbilical cord cells: a new cell source for cardiovascular tissue engineering. Ann Thorac Surg. 2002;74(4):S1422–8.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Kaviani A, Guleserian K, Perry TE, Jennings RW, Ziegler MM, Fauza DO. Fetal tissue engineering from amniotic fluid. J Am Coll Surg. 2003;196(4):592–7.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Kaviani A, Perry TE, Barnes CM, Oh JT, Ziegler MM, Fishman SJ, Fauza DO. The placenta as a cell source in fetal tissue engineering. J Pediatr Surg. 2002;37(7):995–9.CrossRefGoogle Scholar
  67. 67.
    Applegate LA, Weber D, Simon J-P, Scaletta C, Hirt-Burri N, de Buys RA, Raffoul W, et al. Organ donation and whole-cell bioprocessing in the Swiss fetal progenitor cell transplantation platform. In: Saidi RF, editor. Organ Donation and Organ Donors: Issues, Challenges and Perspectives. Hauppauge NY: Nova Science Publishers, Inc.; 2013. p. 125–48.Google Scholar
  68. 68.
    Rosser AE, Bachoud-Levi AC. Clinical trials of neural transplantation in Huntington's disease. Prog Brain Res. 2012;200:345–71.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Schackel S, Pauly MC, Piroth T, Nikkhah G, Dobrossy MD. Donor age dependent graft development and recovery in a rat model of Huntington's disease: histological and behavioral analysis. Behav Brain Res. 2013;256:56–63.CrossRefGoogle Scholar
  70. 70.
    Lindvall O. Developing dopaminergic cell therapy for Parkinson's disease--give up or move forward? Mov Disord. 2013;28(3):268–73.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Wirth ED 3rd, Reier PJ, Fessler RG, Thompson FJ, Uthman B, Behrman A, Beard J, Vierck CJ, Anderson DK. Feasibility and safety of neural tissue transplantation in patients with syringomyelia. J Neurotrauma. 2001;18(9):911–29.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Akesson E, Piao JH, Samuelsson EB, Holmberg L, Kjaeldgaard A, Falci S, Sundström E, Seiger A. Long-term culture and neuronal survival after intraspinal transplantation of human spinal cord-derived neurospheres. Physiol Behav. 2007;92(1-2):60–6.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Iwai H, Nori S, Nishimura S, Yasuda A, Takano M, Tsuji O, Fujiyoshi K, Toyama Y, Okano H, Nakamura M. Transplantation of neural stem/progenitor cells at different locations in mice with spinal cord injury. Cell Transplant. 2014;23(11):1451–64.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Mothe AJ, Tator CH. Review of transplantation of neural stem/progenitor cells for spinal cord injury. Int J Dev Neurosci. 2013;31(7):701–13.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Touraine JL, Raudrant D, Golfier F, Rebaud A, Sembeil R, Roncarolo MG, Bacchetta R, D'Oiron R, Lambert T, Gebuhrer L. Reappraisal of in utero stem cell transplantation based on long-term results. Fetal Diagn Ther. 2004;19(4):305–12.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Gridelli B, Vizzini G, Pietrosi G, Luca A, Spada M, Gruttadauria S, Cintorino D, Amico G, Chinnici C, Miki T, Schmelzer E, Conaldi PG, Triolo F, Gerlach JC. Efficient human fetal liver cell isolation protocol based on vascular perfusion for liver cell-based therapy and case report on cell transplantation. Liver Transpl. 2012;18(2):226–37.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Zaret KS, Grompe M. Generation and regeneration of cells of the liver and pancreas. Science. 2008;322(5907):1490–4.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Khan AA, Shaik MV, Parveen N, Rajendraprasad A, Aleem MA, Habeeb MA, Srinivas G, Raj TA, Tiwari SK, Kumaresan K, Venkateswarlu J, Pande G, Habibullah CM. Human fetal liver-derived stem cell transplantation as supportive modality in the management of end-stage decompensated liver cirrhosis. Cell Transplant. 2010;19(4):409–18.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Montanucci P, Pennoni I, Pescara T, Basta G, Calafiore R. Treatment of diabetes mellitus with microencapsulated fetal human liver (FH-B-TPN) engineered cells. Biomaterials. 2013;34(16):4002–12.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Hohlfeld J, de Buys RA, Hirt-Burri N, Chaubert P, Gerber S, Scaletta C, Hohlfeld P, Applegate LA. Tissue engineered fetal skin constructs for paediatric burns. Lancet. 2005;366(9488):840–2.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    De Buys Roessingh AS, Hohlfeld J, Scaletta C, Hirt-Burri N, Gerber S, Hohlfeld P, Gebbers JO, Applegate LA. Development, characterization, and use of a fetal skin cell bank for tissue engineering in wound healing. Cell Transplant. 2006;15(8-9):823–34.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Ramelet AA, Hirt-Burri N, Raffoul W, Scaletta C, Pioletti DP, Offord E, Mansourian R, Applegate LA. Chronic wound healing by fetal cell therapy may be explained by differential gene profiling observed in fetal versus old skin cells. Exp Gerontol. 2009;44(3):208–18.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Pioletti DP, Montjovent MO, Zambelli PY, Applegate L. Bone tissue engineering using foetal cell therapy. Swiss Med Wkly. 2006;136(35-36):557–60.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Darwiche S, Scaletta C, Raffoul W, Pioletti DP, Applegate LA. Epiphyseal chondroprogenitors provide a stable cell source for cartilage cell therapy. Cell Med. 2012;4(1):23–32.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Tenorio DM, Scaletta C, Jaccoud S, Hirt-Burri N, Pioletti DP, Jaques B, Applegate LA. Human fetal bone cells in delivery systems for bone engineering. J Tissue Eng Regen Med. 2011;5(10):806–14.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Grognuz A, Scaletta C, Farron A, Pioletti DP, Raffoul W, Applegate LA. Stability enhancement using hyaluronic acid gels for delivery of human fetal progenitor tenocytes. Cell Med. 2016;8(3):87–97.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Grognuz A, Scaletta C, Farron A, Raffoul W, Applegate LA. Human fetal progenitor tenocytes for regenerative medicine. Cell Transplant. 2016;25(3):463–79.CrossRefGoogle Scholar
  88. 88.
    Laurent-Applegate LA. Preparation of parental cell bank from foetal tissue. WO 2013008174 A1. 2013. www.google.com.na/patents/WO2013008174A1?cl=en. Accessed 9 Mar 2017
  89. 89.
    Prentice HG, Blacklock HA, Janossy G, Gilmore MJ, Price-Jones L, Tidman N, Trejdosiewicz LK, Skeggs DB, Panjwani D, Ball S, et al. Depletion of T lymphocytes in donor marrow prevents significant graft-versus-host disease in matched allogeneic leukaemic marrow transplant recipients. Lancet. 1984;1(8375):472–6.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Asai S, Otsuru S, Candela ME, Cantley L, Uchibe K, Hofmann TJ, Zhang K, Wapner KL, Soslowsky LJ, Horwitz EM, Enomoto-Iwamoto M. Tendon progenitor cells in injured tendons have strong chondrogenic potential: the CD105-negative subpopulation induces chondrogenic degeneration. Stem Cells. 2014;32(12):3266–77.PubMedCentralCrossRefGoogle Scholar
  91. 91.
    Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31(10):890–6.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Devine SM, Bartholomew AM, Mahmud N, Nelson M, Patil S, Hardy W, Sturgeon C, Hewett T, Chung T, Stock W, Sher D, Weissman S, Ferrer K, Mosca J, Deans R, et al. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol. 2001;29(2):244–55.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, Moseley A, Hoffman R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002;30(1):42–8.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Streit M, Braathen LR. Apligraf - a living human skin equivalent for the treatment of chronic wounds. Int J Artif Organs. 2000;23(12):831–3.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Ober C. HLA and pregnancy: the paradox of the fetal allograft. Am J Hum Genet. 1998;62(1):1–5.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Lomas AJ, Ryan CN, Sorushanova A, Shologu N, Sideri AI, Tsioli V, Fthenakis GC, Tzora A, Skoufos I, Quinlan LR, O'Laighin G, Mullen AM, Kelly JL, Kearns S, Biggs M, Pandit A, Zeugolis DI. The past, present and future in scaffold-based tendon treatments. Adv Drug Deliv Rev. 2015;84:257–77.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Schulze-Tanzil G, Al-Sadi O, Ertel W, Lohan A. Decellularized tendon extracellular matrix-a valuable approach for tendon reconstruction? Cell. 2012;1(4):1010–28.CrossRefGoogle Scholar
  98. 98.
    Ingram JH, Korossis S, Howling G, Fisher J, Ingham E. The use of ultrasonication to aid recellularization of acellular natural tissue scaffolds for use in anterior cruciate ligament reconstruction. Tissue Eng. 2007;13(7):1561–72.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Badylak S, Toombs J, Shelbourne K, Hiles M, Lantz G, Van Sickle D. Small intestinal submucosa as an intra-articular ligamentous graft material: a pilot study in dogs. Vet Comp Orthop Traumatol. 1994;7(3):36–40.CrossRefGoogle Scholar
  100. 100.
    Badylak SF, Tullius R, Kokini K, Shelbourne KD, Klootwyk T, Voytik SL, Kraine MR, Simmons C. The use of xenogeneic small intestinal submucosa as a biomaterial for Achilles tendon repair in a dog model. J Biomed Mater Res. 1995;29(8):977–85.PubMedCrossRefGoogle Scholar
  101. 101.
    Derwin KA, Baker AR, Spragg RK, Leigh DR, Iannotti JP. Commercial extracellular matrix scaffolds for rotator cuff tendon repair. Biomechanical, biochemical, and cellular properties. J Bone Joint Surg Am. 2006;88(12):2665–72.PubMedCrossRefGoogle Scholar
  102. 102.
    Longo UG, Lamberti A, Maffulli N, Denaro V. Tendon augmentation grafts: a systematic review. Br Med Bull. 2010;94:165–88.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Barber FA, Herbert MA, Coons DA. Tendon augmentation grafts: biomechanical failure loads and failure patterns. Art Ther. 2006;22(5):534–8.Google Scholar
  104. 104.
    Valentin JE, Badylak JS, McCabe GP, Badylak SF. Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study. J Bone Joint Surg Am. 2006;88(12):2673–86.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Deeken CR, White AK, Bachman SL, Ramshaw BJ, Cleveland DS, Loy TS, Grant SA. Method of preparing a decellularized porcine tendon using tributyl phosphate. J Biomed Mater Res B Appl Biomater. 2011;96(2):199–206.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Cartmell JS, Dunn MG. Effect of chemical treatments on tendon cellularity and mechanical properties. J Biomed Mater Res. 2000;49(1):134–40.PubMedCrossRefGoogle Scholar
  107. 107.
    Zhang AY, Bates SJ, Morrow E, Pham H, Pham B, Chang J. Tissue-engineered intrasynovial tendons: optimization of acellularization and seeding. J Rehabil Res Dev. 2009;46(4):489–98.PubMedCrossRefGoogle Scholar
  108. 108.
    Omae H, Zhao C, Sun YL, An KN, Amadio PC. Multilayer tendon slices seeded with bone marrow stromal cells: a novel composite for tendon engineering. J Orthop Res. 2009;27(7):937–42.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Kryger GS, Chong AK, Costa M, Pham H, Bates SJ, Chang J. A comparison of tenocytes and mesenchymal stem cells for use in flexor tendon tissue engineering. J Hand Surg Am. 2007;32(5):597–605.PubMedCrossRefGoogle Scholar
  110. 110.
    Xing S, Liu C, Xu B, Chen J, Yin D, Zhang C. Effects of various decellularization methods on histological and biomechanical properties of rabbit tendons. Exp Ther Med. 2014;8(2):628–34.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Tischer T, Vogt S, Aryee S, Steinhauser E, Adamczyk C, Milz S, Martinek V, Imhoff AB. Tissue engineering of the anterior cruciate ligament: a new method using acellularized tendon allografts and autologous fibroblasts. Arch Orthop Trauma Surg. 2007;127(9):735–41.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Burk J, Erbe I, Berner D, Kacza J, Kasper C, Pfeiffer B, Winter K, Brehm W. Freeze-thaw cycles enhance decellularization of large tendons. Tissue Eng Part C Methods. 2014;20(4):276–84.PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Youngstrom DW, Barrett JG, Jose RR, Kaplan DL. Functional characterization of detergent-decellularized equine tendon extracellular matrix for tissue engineering applications. PLoS One. 2013;8(5):e64151.PubMedCentralCrossRefGoogle Scholar
  114. 114.
    Huang Q, Ingham E, Rooney P, Kearney JN. Production of a sterilised decellularised tendon allograft for clinical use. Cell Tissue Bank. 2013;14(4):645–54.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 115.
    Pridgen BC, Woon CY, Kim M, Thorfinn J, Lindsey D, Pham H, Chang J. Flexor tendon tissue engineering: acellularization of human flexor tendons with preservation of biomechanical properties and biocompatibility. Tissue Eng Part C Methods. 2011;17(8):819–28.PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Raghavan SS, Woon CY, Kraus A, Megerle K, Choi MS, Pridgen BC, Pham H, Chang J. Human flexor tendon tissue engineering: decellularization of human flexor tendons reduces immunogenicity in vivo. Tissue Eng Part A. 2012;18(7-8):796–805.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials. 2011;32(12):3233–43.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomaterials. 2006;27(19):3675–83.PubMedPubMedCentralGoogle Scholar
  119. 119.
    Chen J, Xu J, Wang A, Zheng M. Scaffolds for tendon and ligament repair: review of the efficacy of commercial products. Expert Rev Med Devices. 2009;6(1):61–73.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    Junqueira LCU, Bignolas G, Brentani RR. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J. 1979;11(4):447–55.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Junqueira LCU, Montes GS, Sanchez EM. The influence of tissue section thickness on the study of collagen by the Picrosirius-polarization method. Histochemistry. 1982;74(1):153–6.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Adzick NS, Harrison MR, Glick PL, Beckstead JH, Villa RL, Scheuenstuhl H, Goodson WH 3rd. Comparison of fetal, newborn, and adult wound healing by histologic, enzyme-histochemical, and hydroxyproline determinations. J Pediatr Surg. 1985;20(4):315–9.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Calve S, Dennis RG, Kosnik PE 2nd, Baar K, Grosh K, Arruda EM. Engineering of functional tendon. Tissue Eng. 2004;10(5–6):755–61.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Anthony Grognuz
    • 1
  • Pierre-Arnaud Aeberhard
    • 1
  • Murielle Michetti
    • 1
  • Nathalie Hirt-Burri
    • 1
  • Corinne Scaletta
    • 1
  • Anthony de Buys Roessingh
    • 1
  • Wassim Raffoul
    • 1
  • Lee Ann Laurent-Applegate
    • 1
    Email author
  1. 1.Unit of Regenerative Therapy, Service of Plastic and Reconstructive Surgery, Department of Musculoskeletal MedicineLausanne University HospitalEpalingesSwitzerland

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