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Stem Cells International
Volume 2017 (2017), Article ID 6843727, 10 pages
https://doi.org/10.1155/2017/6843727
Review Article

Infrapatellar Fat Pad Stem Cells: From Developmental Biology to Cell Therapy

1Tissue Engineering Research Group, Department of Anatomy, Royal College of Surgeons in Ireland, Dublin, Ireland
2CNC, Center for Neuroscience and Cell Biology, University of Coimbra, 3004-517 Coimbra, Portugal
3Trinity Centre for Bioengineering, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin, Ireland
4Department of Mechanical and Manufacturing Engineering School of Engineering, Trinity College Dublin, Dublin, Ireland
5Advanced Materials and Bioengineering Research Centre (AMBER), Trinity College Dublin & Royal College of Surgeons in Ireland, Dublin, Ireland

Correspondence should be addressed to Ronaldo J. F. C. do Amaral

Received 26 May 2017; Accepted 3 August 2017; Published 6 September 2017

Academic Editor: Celeste Scotti

Copyright © 2017 Ronaldo J. F. C. do Amaral et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. A. Ahmed and M. T. Hincke, “Strategies for articular cartilage lesion repair and functional restoration,” Tissue Engineering Part B, Reviews, vol. 16, no. 3, pp. 305–329, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. E. B. Hunziker, K. Lippuner, M. J. Keel, and N. Shintani, “An educational review of cartilage repair: precepts & practice--myths & misconceptions--progress & prospects,” Osteoarthritis and Cartilage, vol. 23, no. 3, pp. 334–350, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. G. J. van Osch, M. Brittberg, J. E. Dennis et al., “Cartilage repair: past and future--lessons for regenerative medicine,” Journal of Cellular and Molecular Medicine, vol. 13, no. 5, pp. 792–810, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Wang, Z. Yuan, N. Ma et al., “Advances and prospects in stem cells for cartilage regeneration,” Stem Cells International, vol. 2017, Article ID 4130607, 16 pages, 2017. View at Publisher · View at Google Scholar
  5. M. Brittberg, “Autologous chondrocyte implantation--technique and long-term follow-up,” Injury, vol. 39, Supplement 1, pp. S40–S49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Brittberg, A. Lindahl, A. Nilsson, C. Ohlsson, O. Isaksson, and L. Peterson, “Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation,” The New England Journal of Medicine, vol. 331, no. 14, pp. 889–895, 1994. View at Publisher · View at Google Scholar · View at Scopus
  7. L. A. Vonk, T. S. de Windt, I. C. Slaper-Cortenbach, and D. B. Saris, “Autologous, allogeneic, induced pluripotent stem cell or a combination stem cell therapy? Where are we headed in cartilage repair and why: a concise review,” Stem Cell Research & Therapy, vol. 6, p. 94, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. R. F. LaPrade, J. L. Dragoo, J. L. Koh, I. R. Murray, A. G. Geeslin, and C. R. Chu, “AAOS research symposium updates and consensus: biologic treatment of orthopaedic injuries,” The Journal of the American Academy of Orthopaedic Surgeons, vol. 24, no. 7, pp. e62–e78, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Barbero, S. Grogan, D. Schäfer, M. Heberer, P. Mainil-Varlet, and I. Martin, “Age related changes in human articular chondrocyte yield, proliferation and post-expansion chondrogenic capacity,” Osteoarthritis and Cartilage, vol. 12, no. 6, pp. 476–484, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Barbero, S. Ploegert, M. Heberer, and I. Martin, “Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes,” Arthritis and Rheumatism, vol. 48, no. 5, pp. 1315–1325, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Diaz-Romero, D. Nesic, S. P. Grogan, P. Heini, and P. Mainil-Varlet, “Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells,” Journal of Cellular Physiology, vol. 214, no. 1, pp. 75–83, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. R. J. do Amaral, S. Pedrosa Cda, M. C. Kochem et al., “Isolation of human nasoseptal chondrogenic cells: a promise for cartilage engineering,” Stem Cell Research, vol. 8, no. 2, pp. 292–299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Togo, A. Utani, M. Naitoh et al., “Identification of cartilage progenitor cells in the adult ear perichondrium: utilization for cartilage reconstruction,” Laboratory Investigation, vol. 86, no. 5, pp. 445–457, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Ito, J. S. Fitzsimmons, A. Sanyal, M. A. Mello, N. Mukherjee, and S. W. O'Driscoll, “Localization of chondrocyte precursors in periosteum,” Osteoarthritis and Cartilage, vol. 9, no. 3, pp. 215–223, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. G. P. Dowthwaite, J. C. Bishop, S. N. Redman et al., “The surface of articular cartilage contains a progenitor cell population,” Journal of Cell Science, vol. 117, Part 6, pp. 889–897, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Fickert, J. Fiedler, and R. E. Brenner, “Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers,” Arthritis Research & Therapy, vol. 6, no. 5, pp. R422–R432, 2004. View at Publisher · View at Google Scholar
  17. S. Hattori, C. Oxford, and A. H. Reddi, “Identification of superficial zone articular chondrocyte stem/progenitor cells,” Biochemical and Biophysical Research Communications, vol. 358, no. 1, pp. 99–103, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. A. M. Craft, J. S. Rockel, Y. Nartiss, R. A. Kandel, B. A. Alman, and G. M. Keller, “Generation of articular chondrocytes from human pluripotent stem cells,” Nature Biotechnology, vol. 33, no. 6, pp. 638–645, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. C. A. Herberts, M. S. Kwa, and H. P. Hermsen, “Risk factors in the development of stem cell therapy,” Journal of Translational Medicine, vol. 9, p. 29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. P. K. Gupta, A. K. Das, A. Chullikana, and A. S. Majumdar, “Mesenchymal stem cells for cartilage repair in osteoarthritis,” Stem Cell Research & Therapy, vol. 3, no. 4, p. 25, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Nelson, J. Fairclough, and C. W. Archer, “Use of stem cells in the biological repair of articular cartilage,” Expert Opinion on Biological Therapy, vol. 10, no. 1, pp. 43–55, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. S. M. Richardson, G. Kalamegam, P. N. Pushparaj et al., “Mesenchymal stem cells in regenerative medicine: focus on articular cartilage and intervertebral disc regeneration,” Methods, vol. 99, pp. 69–80, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Koga, T. Muneta, T. Nagase et al., “Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit,” Cell and Tissue Research, vol. 333, no. 2, pp. 207–215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. E. A. Jones, A. Crawford, A. English et al., “Synovial fluid mesenchymal stem cells in health and early osteoarthritis: detection and functional evaluation at the single-cell level,” Arthritis and Rheumatism, vol. 58, no. 6, pp. 1731–1740, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. D. H. Lee, C. H. Sonn, S. B. Han, Y. Oh, K. M. Lee, and S. H. Lee, “Synovial fluid CD34(−) CD44(+) CD90(+) mesenchymal stem cell levels are associated with the severity of primary knee osteoarthritis,” Osteoarthritis and Cartilage, vol. 20, no. 2, pp. 106–109, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Mak, C. L. Jablonski, C. A. Leonard et al., “Intra-articular injection of synovial mesenchymal stem cells improves cartilage repair in a mouse injury model,” Scientific Reports, vol. 6, p. 23076, 2016. View at Publisher · View at Google Scholar · View at Scopus
  27. I. Sekiya, T. Muneta, M. Horie, and H. Koga, “Arthroscopic transplantation of synovial stem cells improves clinical outcomes in knees with cartilage defects,” Clinical Orthopaedics and Related Research, vol. 473, no. 7, pp. 2316–2326, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. H. V. Almeida, G. M. Cunniffe, T. Vinardell, C. T. Buckley, F. J. O'Brien, and D. J. Kelly, “Coupling freshly isolated CD44(+) infrapatellar fat pad-derived stromal cells with a TGF-beta3 eluting cartilage ECM-derived scaffold as a single-stage strategy for promoting chondrogenesis,” Advanced Healthcare Materials, vol. 4, no. 7, pp. 1043–1053, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. H. V. Almeida, R. Eswaramoorthy, G. M. Cunniffe, C. T. Buckley, F. J. O'Brien, and D. J. Kelly, “Fibrin hydrogels functionalized with cartilage extracellular matrix and incorporating freshly isolated stromal cells as an injectable for cartilage regeneration,” Acta Biomaterialia, vol. 36, pp. 55–62, 2016. View at Publisher · View at Google Scholar · View at Scopus
  30. H. V. Almeida, Y. Liu, G. M. Cunniffe et al., “Controlled release of transforming growth factor-beta3 from cartilage-extra-cellular-matrix-derived scaffolds to promote chondrogenesis of human-joint-tissue-derived stem cells,” Acta Biomaterialia, vol. 10, no. 10, pp. 4400–4409, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. H. V. Almeida, K. J. Mulhall, F. J. O'Brien, and D. J. Kelly, “Stem cells display a donor dependent response to escalating levels of growth factor release from extracellular matrix-derived scaffolds,” Journal of Tissue Engineering and Regenerative Medicine, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Liu, C. T. Buckley, H. V. Almeida, K. J. Mulhall, and D. J. Kelly, “Infrapatellar fat pad-derived stem cells maintain their chondrogenic capacity in disease and can be used to engineer cartilaginous grafts of clinically relevant dimensions,” Tissue Engineering Part A, vol. 20, no. 21-22, pp. 3050–3062, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. E. B. de Sousa, P. L. Casado, V. Moura Neto, M. E. Duarte, and D. P. Aguiar, “Synovial fluid and synovial membrane mesenchymal stem cells: latest discoveries and therapeutic perspectives,” Stem Cell Research & Therapy, vol. 5, no. 5, p. 112, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Marlovits, G. Striessnig, C. T. Resinger et al., “Definition of pertinent parameters for the evaluation of articular cartilage repair tissue with high-resolution magnetic resonance imaging,” European Journal of Radiology, vol. 52, no. 3, pp. 310–319, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Lysholm and J. Gillquist, “Evaluation of knee ligament surgery results with special emphasis on use of a scoring scale,” The American Journal of Sports Medicine, vol. 10, no. 3, pp. 150–154, 1982. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. G. Koh and Y. J. Choi, “Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis,” The Knee, vol. 19, no. 6, pp. 902–907, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. G. Koh, S. B. Jo, O. R. Kwon et al., “Mesenchymal stem cell injections improve symptoms of knee osteoarthritis,” Arthroscopy, vol. 29, no. 4, pp. 748–755, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. G. P. Doner and F. R. Noyes, “Arthroscopic resection of fat pad lesions and infrapatellar contractures,” Arthroscopy techniques, vol. 3, no. 3, pp. e413–e416, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Cai, J. Xu, K. Wang et al., “Association between infrapatellar fat pad volume and knee structural changes in patients with knee osteoarthritis,” The Journal of Rheumatology, vol. 42, no. 10, pp. 1878–1884, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Chuckpaiwong, H. C. Charles, V. B. Kraus, F. Guilak, and J. A. Nunley, “Age-associated increases in the size of the infrapatellar fat pad in knee osteoarthritis as measured by 3T MRI,” Journal of Orthopaedic Research, vol. 28, no. 9, pp. 1149–1154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. S. M. Cowan, H. F. Hart, S. J. Warden, and K. M. Crossley, “Infrapatellar fat pad volume is greater in individuals with patellofemoral joint osteoarthritis and associated with pain,” Rheumatology International, vol. 35, no. 8, pp. 1439–1442, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. J. McConnell, “Running injuries: the infrapatellar fat pad and plica injuries,” Physical Medicine and Rehabilitation Clinics of North America, vol. 27, no. 1, pp. 79–89, 2016. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Ogata and H. K. Uhthoff, “The development of synovial plicae in human knee joints: an embryologic study,” Arthroscopy, vol. 6, no. 4, pp. 315–321, 1990. View at Google Scholar
  44. J. Mace, W. Bhatti, and S. Anand, “Infrapatellar fat pad syndrome: a review of anatomy, function, treatment and dynamics,” Acta Orthopaedica Belgica, vol. 82, no. 1, pp. 94–101, 2016. View at Google Scholar
  45. J. Gallagher, P. Tierney, P. Murray, and M. O'Brien, “The infrapatellar fat pad: anatomy and clinical correlations,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 13, no. 4, pp. 268–272, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. M. A. MacCONAILL, “The movements of bones and joints; the synovial fluid and its assistants,” Journal of Bone and Joint Surgery. British Volume (London), vol. 32-B, no. 2, pp. 244–252, 1950. View at Google Scholar
  47. D. Saddik, E. G. McNally, and M. Richardson, “MRI of Hoffa's fat pad,” Skeletal Radiology, vol. 33, no. 8, pp. 433–444, 2004. View at Publisher · View at Google Scholar
  48. F. Eymard and X. Chevalier, “Inflammation of the infrapatellar fat pad,” Joint, Bone, Spine, vol. 83, no. 4, pp. 389–393, 2016. View at Publisher · View at Google Scholar · View at Scopus
  49. D. V. Davies and J. E. White, “The structure and weight of synovial fat pads,” Journal of Anatomy, vol. 95, pp. 30–37, 1961. View at Google Scholar
  50. A. Ioan-Facsinay and M. Kloppenburg, “An emerging player in knee osteoarthritis: the infrapatellar fat pad,” Arthritis Research & Therapy, vol. 15, no. 6, p. 225, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. W. S. Khan, S. R. Tew, A. B. Adesida, and T. E. Hardingham, “Human infrapatellar fat pad-derived stem cells express the pericyte marker 3G5 and show enhanced chondrogenesis after expansion in fibroblast growth factor-2,” Arthritis Research & Therapy, vol. 10, no. 4, article R74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. J. A. Merida-Velasco, I. Sánchez-Montesinos, J. Espín-Ferra, J. F. Rodríguez-Vázquez, J. R. Mérida-Velasco, and J. Jiménez-Collado, “Development of the human knee joint,” The Anatomical Record, vol. 248, no. 2, pp. 269–278, 1997. View at Google Scholar
  53. L. Longobardi, T. Li, L. Tagliafierro et al., “Synovial joints: from development to homeostasis,” Current Osteoporosis Reports, vol. 13, no. 1, pp. 41–51, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. R. S. Decker, E. Koyama, and M. Pacifici, “Genesis and morphogenesis of limb synovial joints and articular,” Matrix Biology, vol. 39, pp. 5–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Koyama, Y. Shibukawa, M. Nagayama et al., “A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis,” Developmental Biology, vol. 316, no. 1, pp. 62–73, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Pacifici, E. Koyama, Y. Shibukawa et al., “Cellular and molecular mechanisms of synovial joint and articular cartilage formation,” Annals of the New York Academy of Sciences, vol. 1068, pp. 74–86, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. A. J. Roelofs, J. Zupan, A. H. K. Riemen et al., “Joint morphogenetic cells in the adult mammalian synovium,” Nature Communications, vol. 8, article 15040, 2017. View at Publisher · View at Google Scholar
  58. F. M. Gregoire, “Adipocyte differentiation: from fibroblast to endocrine cell,” Experimental Biology and Medicine (Maywood, New Jersey), vol. 226, no. 11, pp. 997–1002, 2001. View at Google Scholar
  59. M. Coelho, T. Oliveira, and R. Fernandes, “Biochemistry of adipose tissue: an endocrine organ,” Archives of Medical Science, vol. 9, no. 2, pp. 191–200, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. C. H. Saely, K. Geiger, and H. Drexel, “Brown versus white adipose tissue: a mini-review,” Gerontology, vol. 58, no. 1, pp. 15–23, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. M. M. Ibrahim, “Subcutaneous and visceral adipose tissue: structural and functional differences,” Obesity Reviews, vol. 11, no. 1, pp. 11–18, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. B. Prunet-Marcassus, B. Cousin, D. Caton, M. André, L. Pénicaud, and L. Casteilla, “From heterogeneity to plasticity in adipose tissues: site-specific differences,” Experimental Cell Research, vol. 312, no. 6, pp. 727–736, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Baglioni, G. Cantini, G. Poli et al., “Functional differences in visceral and subcutaneous fat pads originate from differences in the adipose stem cell,” PLoS One, vol. 7, no. 5, article e36569, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. D. C. Berry, D. Stenesen, D. Zeve, and J. M. Graff, “The developmental origins of adipose tissue,” Development, vol. 140, no. 19, pp. 3939–3949, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Y. Chau, R. Bandiera, A. Serrels et al., “Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source,” Nature Cell Biology, vol. 16, no. 4, pp. 367–375, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. D. C. Wan and M. T. Longaker, “Fat or fiction: origins matter,” Cell Metabolism, vol. 19, no. 6, pp. 900-901, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Distel, T. Cadoudal, S. Durant, A. Poignard, X. Chevalier, and C. Benelli, “The infrapatellar fat pad in knee osteoarthritis: an important source of interleukin-6 and its soluble receptor,” Arthritis and Rheumatism, vol. 60, no. 11, pp. 3374–3377, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. P. A. Zuk, M. Zhu, H. Mizuno et al., “Multilineage cells from human adipose tissue: implications for cell-based therapies,” Tissue Engineering, vol. 7, no. 2, pp. 211–228, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Crisan, M. Corselli, W. C. Chen, and B. Péault, “Perivascular cells for regenerative medicine,” Journal of Cellular and Molecular Medicine, vol. 16, no. 12, pp. 2851–2860, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. L. da Silva Meirelles, P. C. Chagastelles, and N. B. Nardi, “Mesenchymal stem cells reside in virtually all post-natal organs and tissues,” Journal of Cell Science, vol. 119, Part 11, pp. 2204–2213, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. T. M. Liu, M. Martina, D. W. Hutmacher, J. H. Hui, E. H. Lee, and B. Lim, “Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages,” Stem Cells, vol. 25, no. 3, pp. 750–760, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Maumus, J. A. Peyrafitte, R. D'Angelo et al., “Native human adipose stromal cells: localization, morphology and phenotype,” International Journal of Obesity, vol. 35, no. 9, pp. 1141–1153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Zimmerlin, V. S. Donnenberg, J. P. Rubin, and A. D. Donnenberg, “Mesenchymal markers on human adipose stem/progenitor cells,” Cytometry Part A, vol. 83, no. 1, pp. 134–140, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Bourin, B. A. Bunnell, L. Casteilla et al., “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, vol. 15, no. 6, pp. 641–648, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. K. Maekawa, H. Furukawa, Y. Kanazawa, A. Hijioka, K. Suzuki, and S. Fujimoto, “Electron and immunoelectron microscopy on healing process of the rat anterior cruciate ligament after partial transection: the roles of multipotent fibroblasts in the synovial tissue,” Histology and Histopathology, vol. 11, no. 3, pp. 607–619, 1996. View at Google Scholar
  76. M. Q. Wickham, G. R. Erickson, J. M. Gimble, T. P. Vail, and F. Guilak, “Multipotent stromal cells derived from the infrapatellar fat pad of the knee,” Clinical Orthopaedics and Related Research, no. 412, pp. 196–212, 2003. View at Publisher · View at Google Scholar
  77. K. Ye, R. Felimban, K. Traianedes et al., “Chondrogenesis of infrapatellar fat pad derived adipose stem cells in 3D printed chitosan scaffold,” PLoS One, vol. 9, no. 6, article e99410, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Y. Lee, T. Nakagawa, and A. H. Reddi, “Induction of chondrogenesis and expression of superficial zone protein (SZP)/lubricin by mesenchymal progenitors in the infrapatellar fat pad of the knee joint treated with TGF-beta1 and BMP-7,” Biochemical and Biophysical Research Communications, vol. 376, no. 1, pp. 148–153, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. W. J. Jurgens, A. van Dijk, B. Z. Doulabi et al., “Freshly isolated stromal cells from the infrapatellar fat pad are suitable for a one-step surgical procedure to regenerate cartilage tissue,” Cytotherapy, vol. 11, no. 8, pp. 1052–1064, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. C. T. Buckley, T. Vinardell, S. D. Thorpe et al., “Functional properties of cartilaginous tissues engineered from infrapatellar fat pad-derived mesenchymal stem cells,” Journal of Biomechanics, vol. 43, no. 5, pp. 920–926, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. J. L. Dragoo, B. Samimi, M. Zhu et al., “Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads,” Journal of Bone and Joint Surgery British Volume (London), vol. 85, no. 5, pp. 740–747, 2003. View at Google Scholar
  82. P. Hindle, N. Khan, L. Biant, and B. Péault, “The infrapatellar fat pad as a source of perivascular stem cells with increased chondrogenic potential for regenerative medicine,” Stem Cells Translational Medicine, vol. 6, no. 1, pp. 77–87, 2017. View at Publisher · View at Google Scholar
  83. A. English, E. A. Jones, D. Corscadden et al., “A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteoarthritis,” Rheumatology (Oxford), vol. 46, no. 11, pp. 1676–1683, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. P. Tangchitphisut, N. Srikaew, S. Numhom et al., “Infrapatellar fat pad: an alternative source of adipose-derived mesenchymal stem cells,” Arthritis, vol. 2016, Article ID 4019873, 10 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Vinardell, E. J. Sheehy, C. T. Buckley, and D. J. Kelly, “A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources,” Tissue Engineering Part A, vol. 18, no. 11-12, pp. 1161–1170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Sakaguchi, I. Sekiya, K. Yagishita, and T. Muneta, “Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source,” Arthritis and Rheumatism, vol. 52, no. 8, pp. 2521–2529, 2005. View at Publisher · View at Google Scholar · View at Scopus
  87. S. F. Carroll, C. T. Buckley, and D. J. Kelly, “Cyclic hydrostatic pressure promotes a stable cartilage phenotype and enhances the functional development of cartilaginous grafts engineered using multipotent stromal cells isolated from bone marrow and infrapatellar fat pad,” Journal of Biomechanics, vol. 47, no. 9, pp. 2115–2121, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. L. Luo, A. R. O'Reilly, S. D. Thorpe, C. T. Buckley, and D. J. Kelly, “Engineering zonal cartilaginous tissue by modulating oxygen levels and mechanical cues through the depth of infrapatellar fat pad stem cell laden hydrogels,” Journal of Tissue Engineering and Regenerative Medicine, 2016. View at Publisher · View at Google Scholar · View at Scopus
  89. L. Luo, J. Y. Chu, R. Eswaramoorthy, K. J. Mulhall, and D. J. Kelly, “Engineering tissues that mimic the zonal nature of articular cartilage using decellularized cartilage explants seeded with adult stem cells,” ACS Biomaterials Science & Engineering, 2016. View at Publisher · View at Google Scholar
  90. J. Garcia, C. Mennan, H. S. McCarthy, S. Roberts, J. B. Richardson, and K. T. Wright, “Chondrogenic potency analyses of donor-matched chondrocytes and mesenchymal stem cells derived from bone marrow, infrapatellar fat pad, and subcutaneous fat,” Stem Cells International, vol. 2016, Article ID 6969726, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Garcia, K. Wright, S. Roberts et al., “Characterisation of synovial fluid and infrapatellar fat pad derived mesenchymal stromal cells: the influence of tissue source and inflammatory stimulus,” Scientific Reports, vol. 6, article 24295, 2016. View at Publisher · View at Google Scholar · View at Scopus
  92. J. C. Leijten, N. Georgi, L. Wu, C. A. van Blitterswijk, and M. Karperien, “Cell sources for articular cartilage repair strategies: shifting from monocultures to cocultures,” Tissue Engineering Part B, Reviews, vol. 19, no. 1, pp. 31–40, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Bian, D. Y. Zhai, R. L. Mauck, and J. A. Burdick, “Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage,” Tissue Engineering Part A, vol. 17, no. 7-8, pp. 1137–1145, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. V. V. Meretoja, R. L. Dahlin, F. K. Kasper, and A. G. Mikos, “Enhanced Chondrogenesis in co-cultures with articular chondrocytes and mesenchymal stem cells,” Biomaterials, vol. 33, no. 27, pp. 6362–6369, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. V. V. Meretoja, R. L. Dahlin, S. Wright, F. K. Kasper, and A. G. Mikos, “The effect of hypoxia on the chondrogenic differentiation of co-cultured articular chondrocytes and mesenchymal stem cells in scaffolds,” Biomaterials, vol. 34, no. 17, pp. 4266–4273, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Acharya, A. Adesida, P. Zajac et al., “Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation,” Journal of Cellular Physiology, vol. 227, no. 1, pp. 88–97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. E. J. Kubosch, E. Heidt, A. Bernstein, K. Böttiger, and H. Schmal, “The trans-well coculture of human synovial mesenchymal stem cells with chondrocytes leads to self-organization, chondrogenic differentiation, and secretion of TGFbeta,” Stem Cell Research & Therapy, vol. 7, no. 1, p. 64, 2016. View at Publisher · View at Google Scholar · View at Scopus
  98. F. Hildner, S. Concaro, A. Peterbauer et al., “Human adipose-derived stem cells contribute to chondrogenesis in coculture with human articular chondrocytes,” Tissue Engineering Part A, vol. 15, no. 12, pp. 3961–3969, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Mesallati, E. J. Sheehy, T. Vinardell, C. T. Buckley, and D. J. Kelly, “Tissue engineering scaled-up, anatomically shaped osteochondral constructs for joint resurfacing,” European Cells and Materials, vol. 30, pp. 163–186, 2015. View at Google Scholar
  100. T. Mesallati, C. T. Buckley, and D. J. Kelly, “Engineering cartilaginous grafts using chondrocyte-laden hydrogels supported by a superficial layer of stem cells,” Journal of Tissue Engineering and Regenerative Medicine, vol. 11, no. 5, pp. 1343–1353, 2017. View at Publisher · View at Google Scholar · View at Scopus
  101. F. S. Toghraie, N. Chenari, M. A. Gholipour et al., “Treatment of osteoarthritis with infrapatellar fat pad derived mesenchymal stem cells in rabbit,” The Knee, vol. 18, no. 2, pp. 71–75, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. C. W. Ha and Y. B. Park, “Mesenchymal stem cells versus fat pad-derived cells,” Arthroscopy, vol. 30, no. 4, pp. 419-420, 2014. View at Publisher · View at Google Scholar · View at Scopus
  103. A. J. Hayes, S. MacPherson, H. Morrison, G. Dowthwaite, and C. W. Archer, “The development of articular cartilage: evidence for an appositional growth mechanism,” Anatomy and Embryology (Berl), vol. 203, no. 6, pp. 469–479, 2001. View at Google Scholar
  104. L. Li, P. T. Newton, T. Bouderlique et al., “Superficial cells are self-renewing chondrocyte progenitors, which form the articular cartilage in juvenile mice,” The FASEB Journal, vol. 31, no. 3, pp. 1067–1084, 2017. View at Publisher · View at Google Scholar
  105. S. Alsalameh, R. Amin, T. Gemba, and M. Lotz, “Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage,” Arthritis and Rheumatism, vol. 50, no. 5, pp. 1522–1532, 2004. View at Publisher · View at Google Scholar · View at Scopus
  106. Y. Jiang and R. S. Tuan, “Origin and function of cartilage stem/progenitor cells in osteoarthritis,” Nature Reviews Rheumatology, vol. 11, no. 4, pp. 206–212, 2015. View at Publisher · View at Google Scholar · View at Scopus
  107. C. Zhou, H. Zheng, D. Seol, Y. Yu, and J. A. Martin, “Gene expression profiles reveal that chondrogenic progenitor cells and synovial cells are closely related,” Journal of Orthopaedic Research, vol. 32, no. 8, pp. 981–988, 2014. View at Publisher · View at Google Scholar · View at Scopus
  108. T. Li, L. Longobardi, T. J. Myers et al., “Joint TGF-beta type II receptor-expressing cells: ontogeny and characterization as joint progenitors,” Stem Cells and Development, vol. 22, no. 9, pp. 1342–1359, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. A. Spagnoli, L. O'Rear, R. L. Chandler et al., “TGF-beta signaling is essential for joint morphogenesis,” The Journal of Cell Biology, vol. 177, no. 6, pp. 1105–1117, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. G. Hyde, S. Dover, A. Aszodi, G. A. Wallis, and R. P. Boot-Handford, “Lineage tracing using matrilin-1 gene expression reveals that articular chondrocytes exist as the joint interzone forms,” Developmental Biology, vol. 304, no. 2, pp. 825–833, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. B. O. Zhou, R. Yue, M. M. Murphy, J. G. Peyer, and S. J. Morrison, “Leptin receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow,” Cell Stem Cell, vol. 15, no. 2, pp. 154–168, 2014. View at Publisher · View at Google Scholar · View at Scopus
  112. D. T. Covas, R. A. Panepucci, A. M. Fontes et al., “Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts,” Experimental Hematology, vol. 36, no. 5, pp. 642–654, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. E. Cordeiro-Spinetti, R. S. Taichman, and A. Balduino, “The bone marrow endosteal niche: how far from the surface?” Journal of Cellular Biochemistry, vol. 116, no. 1, pp. 6–11, 2015. View at Publisher · View at Google Scholar
  114. A. Tormin, O. Li, J. C. Brune et al., “CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization,” Blood, vol. 117, no. 19, pp. 5067–5077, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Birbrair, T. Zhang, Z. M. Wang, M. L. Messi, A. Mintz, and O. Delbono, “Pericytes: multitasking cells in the regeneration of injured, diseased, and aged skeletal muscle,” Frontiers in Aging Neuroscience, vol. 6, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Dellavalle, G. Maroli, D. Covarello et al., “Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells,” Nature Communications, vol. 2, p. 499, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. S. Clockaerts, Y. M. Bastiaansen-Jenniskens, J. Runhaar et al., “The infrapatellar fat pad should be considered as an active osteoarthritic joint tissue: a narrative review,” Osteoarthritis and Cartilage, vol. 18, no. 7, pp. 876–882, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. Y. P. Liu, S. Z. Li, F. Yuan et al., “Infrapatellar fat pad may be with tendon repairing ability and closely related with the developing process of patella Baja,” Medical Hypotheses, vol. 77, no. 4, pp. 620–623, 2011. View at Publisher · View at Google Scholar · View at Scopus