Cell and Tissue Research

, Volume 370, Issue 1, pp 53–70 | Cite as

Meniscus, articular cartilage and nucleus pulposus: a comparative review of cartilage-like tissues in anatomy, development and function

Review

Abstract

The degradation of cartilage in the human body is impacted by aging, disease, genetic predisposition and continued insults resulting from daily activity. The burden of cartilage defects (osteoarthritis, rheumatoid arthritis, intervertebral disc damage, knee replacement surgeries, etc.) is daunting in light of substantial economic and social stresses. This review strives to broaden the scope of regenerative medicine and tissue engineering approaches used for cartilage repair by comparing and contrasting the anatomical and functional nature of the meniscus, articular cartilage (AC) and nucleus pulposus (NP). Many review papers have provided detailed evaluations of these cartilages and cartilage-like tissues individually but none have comprehensively examined the parallels and inconsistencies in signaling, genetic expression and extracellular matrix composition between tissues. For the first time, this review outlines the importance of understanding these three tissues as unique entities, providing a comparative analysis of anatomy, ultrastructure, biochemistry and function for each tissue. This novel approach highlights the similarities and differences between tissues, progressing research toward an understanding of what defines each tissue as distinctive. The goal of this paper is to provide researchers with the fundamental knowledge to correctly engineer the meniscus, AC and NP without inadvertently developing the wrong tissue function or biochemistry.

Keywords

Articular cartilage Meniscus Nucleus pulposus Development Tissue engineering 

Notes

Acknowledgements

We thank Suzanne Danley for editing the manuscript and Quincy Hathaway for valuable comments and revision. This project was partially supported by Research Grants from the Musculoskeletal Transplant Foundation and the National Institutes of Health (R03AR062763-01A1, R01AR067747-01A1) (to M.P.), Natural Science Foundation of Shanghai City, China (15ZR1414000, to P.F.) and Natural Science Foundation of China (81601889, to S.C.).

Compliance with ethical standards

Author disclosure statement

No competing financial interests exist.

References

  1. Adams MA, McNally DS, Dolan P (1996) ‘Stress’ distributions inside interbertebral discs. The effects of age and degeneration. J Bone Joint Surg Br 78:965–972PubMedCrossRefGoogle Scholar
  2. Afoke NY, Byers PD, Hutton WC (1987) Contact pressures in the human hip joint. J Bone Joint Surg Br 69:536–541PubMedGoogle Scholar
  3. Agrawal A, Guttapalli A, Narayan S, Narayan S, Albert TJ, Shapiro IM, Risbud MV (2007) Normoxic stabilization of HIF-1alpha drives glycolytic metabolism and regulates aggrecan gene expression in nucleus pulposus cells of the rat intervertebral disk. Am J Physiol Cell Physiol 293:C621–631PubMedCrossRefGoogle Scholar
  4. Aigner T, Gebhard PM, Schmid E, Bau B, Harley V, Poschl E (2003) SOX9 expression does not correlate with type II collagen expression in adult articular chondrocytes. Matrix Biol 22:363–372PubMedCrossRefGoogle Scholar
  5. Alexopoulos LG, Haider MA, Vail TP, Guilak F (2003) Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J Biomech Eng 125:323–333PubMedCrossRefGoogle Scholar
  6. Archer CW, Dowthwaite GP, Francis-West P (2003) Development of synovial joints. Birth Defects Res C 69:144–155CrossRefGoogle Scholar
  7. arcOGEN Consortium; arcOGEN Collaborators, Zeggini E, Panoutsopoulou K, Southam L, Rayner NW, Day-Williams AG, Lopes MC, Boraska V, Esko T, Evangelou E, Hoffman A, Houwing-Duistermaat JJ, Ingvarsson T, Jonsdottir I, Jonnson H, Kerkhof HJ, Kloppenburg M, Bos SD, Mangino M, Metrustry S, Slagboom PE, Thorleifsson G, Raine EV, Ratnayake M, Ricketts M, Beazley C, Blackburn H, Bumpstead S, Elliott KS, Hunt SE, Potter SC, Shin SY, Yadav VK, Zhai G, Sherburn K, Dixon K, Arden E, Aslam N, Battley PK, Carluke I, Doherty S, Gordon A, Joseph J, Keen R, Koller NC, Mitchell S, O’Neill F, Paling E, Reed MR, Rivadeneira F, Swift D, Walker K, Watkins B, Wheeler M, Birrell F, Ioannidis JP, Meulenbelt I, Metspalu A, Rai A, Salter D, Stefansson K, Stykarsdottir U, Uitterlinden AG, van Meurs JB, Chapman K, Deloukas P, Ollier WE, Wallis GA, Arden N, Carr A, Doherty M, McCaskie A, Willkinson JM, Ralston SH, Valdes AM, Spector TD, Loughlin J (2012) Identification of new susceptibility loci for osteoarthritis (arcOGEN): a genome-wide association study. Lancet 380:815–823CrossRefGoogle Scholar
  8. Aspden RM, Yarker YE, Hukins DW (1985) Collagen orientations in the meniscus of the knee joint. J Anat 140:371–380PubMedPubMedCentralGoogle Scholar
  9. Bank RA, Verzijl N, Lafeber FP, Tekoppele JM (2002) Putative role of lysyl hydroxylation and pyridinoline cross-linking during adolescence in the occurrence of osteoarthritis at old age. Osteoarthritis Cartilage 10:127–134PubMedCrossRefGoogle Scholar
  10. Baratz ME, Fu FH, Mengato R (1986) Meniscal tears: the effect of meniscectomy and of repair on intra-articular contact areas and stress in the human knee. Am J Sports Med 14:270–275PubMedCrossRefGoogle Scholar
  11. Bargar WL, Moreland JR, Markolf KL, Shoemaker SC, Amstutz HC, Grant TT (1980) In vivo stability testing of post-meniscectomy knees. Clin Orthop Relat Res 150:247–252Google Scholar
  12. Bastiaansen-Jenniskens YM, Koevoet W, de Bart AC, van der Linden JC, Zuurmond AM, Weinans H, Verhaar JA, van Osch GJ, Degroot J (2008) Contribution of collagen network features to functional properties of engineered cartilage. Osteoarthritis Cartilage 16:359–366PubMedCrossRefGoogle Scholar
  13. Becerra J, Andrades JA, Guerado E, Zamora-Navas P, Lopez-Puertas JM, Reddi AH (2010) Articular cartilage: structure and regeneration. Tissue Eng Part B 16:617–627CrossRefGoogle Scholar
  14. Blanco JF, Graciani IF, Sanchez-Guijo FM, Muntion S, Hernandez-Campo P, Santamaria C, Carrancio S, Barbado MV, Cruz G, Gutierrez-Cosio S, Herrero C, San Miguel JF, Brinon JG, del Canizo MC (2010) Isolation and characterization of mesenchymal stromal cells from human degenerated nucleus pulposus: comparison with bone marrow mesenchymal stromal cells from the same subjects. Spine (Phila Pa 1976) 35:2259–2265CrossRefGoogle Scholar
  15. Bogduk N, Twomey LT (1987) Clinical anatomy of the lumbar spine, 1st edn. Churchill Livingstone, New York, pp 130–138Google Scholar
  16. Brama PA, Tekoppele JM, Bank RA, van Weeren PR, Barneveld A (1999) Influence of different exercise levels and age on the biochemical characteristics of immature equine articular cartilage. Equine Vet J Suppl 31:55–61CrossRefGoogle Scholar
  17. Buckwalter JA (1983) Articular cartilage. Instr Course Lect 32:349–370PubMedGoogle Scholar
  18. Buckwalter JA, Mankin HJ (1998) Articular cartilage: tissue design and chondrocyte-matrix interactions. Instr Course Lect 47:477–486PubMedGoogle Scholar
  19. Cai D, Marty-Roix R, Hsu HP, Spector M (2001) Lapine and canine bone marrow stromal cells contain smooth muscle actin and contract a collagen-glycosaminoglycan matrix. Tissue Eng 7:829–841PubMedCrossRefGoogle Scholar
  20. Chan WC, Au TY, Tam V, Cheah KS, Chan D (2014) Coming together is a beginning: the making of an intervertebral disc. Birth Defects Res C 102:83–100CrossRefGoogle Scholar
  21. Chen J, Jing L, Gilchrist CL, Richardson WJ, Fitch RD, Setton LA (2009) Expression of laminin isoforms, receptors, and binding proteins unique to nucleus pulposus cells of immature intervertebral disc. Connect Tissue Res 50:294–306PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chen S, Fu P, Cong R, Wu H, Pei M (2015) Strategies to minimize hypertrophy in cartilage engineering and regeneration. Genes Dis 2:76–95Google Scholar
  23. Cheung HS (1987) Distribution of type I, II, III and V in the pepsin solubilized collagens in bovine menisci. Connect Tissue Res 16:343–356PubMedCrossRefGoogle Scholar
  24. Choi JB, Youn I, Cao L, Leddy HA, Gilchrist CL, Setton LA, Guilak F (2007) Zonal changes in the three-dimensional morphology of the chondron under compression: the relationship among cellular, pericellular, and extracellular deformation in articular cartilage. J Biomech 40:2596–2603PubMedPubMedCentralCrossRefGoogle Scholar
  25. Choi H, Johnson ZI, Risbud MV (2015) Understanding nucleus pulposus cell phenotype: a prerequisite for stem cell based therapies to treat intervertebral disc degeneration. Curr Stem Cell Res Ther 10:307–316PubMedPubMedCentralCrossRefGoogle Scholar
  26. Clark CR, Ogden JA (1983) Development of the menisci of the human knee joint. Morphological changes and their potential role in childhood meniscal injury. J Bone Joint Surg Am 65:538–547PubMedCrossRefGoogle Scholar
  27. Clouet J, Grimandi G, Pot-Vaucel M, Masson M, Fellah HB, Guigand L, Cherel Y, Bord E, Rannou F, Weiss P, Guicheux J, Vinatier C (2009) Identification of phenotypic discriminating markers for intervertebral disc cells and articular chondrocytes. Rheumatology (Oxford) 48:1447–1450CrossRefGoogle Scholar
  28. Cloyd JM, Elliott DM (2007) Elastin content correlates with human disc degeneration in the anulus fibrosus and nucleus pulposus. Spine (Phila Pa 1976) 32:1826–1831CrossRefGoogle Scholar
  29. Cornejo MC, Cho SK, Giannarelli C, Iatridis JC, Purmessur D (2015) Soluble factors from the notochordal-rich intervertebral disc inhibit endothelial cell invasion and vessel formation in the presence and absence of pro-inflammatory cytokines. Osteoarthritis Cartilage 23:487–496PubMedCrossRefGoogle Scholar
  30. Crock HV, Goldwasser M, Yoshizawa H (1988) Vascular anatomy related to the intervertebral disc. In: Ghosh P (ed) Biology of the intervertebral disc. CRC, Boca Raton, pp 109–133Google Scholar
  31. Danzig L, Resnick D, Gonsalves M, Akeson WH (1983) Blood supply to the normal and abnormal menisci of the human knee. Clin Orthop Relat Res 172:271–276Google Scholar
  32. Darling EM, Wilusz RE, Bolognesi MP, Zauscher S, Guilak F (2010) Spatial mapping of the biomechanical properties of the pericellular matrix of articular cartilage measured in situ via atomic force microscopy. Biophys J 98:2848–2856PubMedPubMedCentralCrossRefGoogle Scholar
  33. Declercq HA, Forsyth RG, Verbruggen A, Verdonk R, Cornelissen MJ, Verdonk PC (2012) CD34 and SMA expression of superficial zone cells in the normal and pathological human meniscus. J Orthop Res 30:800–808PubMedCrossRefGoogle Scholar
  34. Donohue PJ, Jahnke MR, Blaha JD, Caterson B (1988) Characterization of link protein(s) from human intervertebral disc tissues. Biochem J 251:739–747PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dowthwaite GP, Bishop JC, Redman SN, Khan IM, Rooney P, Evans DJ, Haughton L, Bayram Z, Boyer S, Thomson B, Wolfe MS, Archer CW (2004) The surface of articular cartilage contains a progenitor cell population. J Cell Sci 117:889–897PubMedCrossRefGoogle Scholar
  36. Duance VC, Crean JK, Sims TJ, Avery N, Smith S, Menage J, Eisenstein SM, Roberts S (1998) Changes in collagen cross-linking in degenerative disc disease and scoliosis. Spine (Phila Pa 1976) 23:2545–2551CrossRefGoogle Scholar
  37. Durr J, Lammi P, Goodman SL, Aigner T, von der Mark K (1996) Identification and immunolocalization of laminin in cartilage. Exp Cell Res 222:225–233PubMedCrossRefGoogle Scholar
  38. Erwin WM, Ashman K, O’Donnel P, Inman RD (2006) Nucleus pulposus notochord cells secrete connective tissue growth factor and up-regulate proteoglycan expression by intervertebral disc chondrocytes. Arthritis Rheum 54:3859–3867PubMedCrossRefGoogle Scholar
  39. Erwin WM, Islam D, Inman RD, Fehlings MG, Tsui FW (2011) Notochordal cells protect nucleus pulposus cells from degradation and apoptosis: implications for the mechanisms of intervertebral disc degeneration. Arthritis Res Ther 13:R215PubMedPubMedCentralCrossRefGoogle Scholar
  40. Eyre DR, Muir H (1977) Quantitative analysis of types I and II collagens in human intervertebral discs at various ages. Biochim Biophys Acta 492:29–42PubMedCrossRefGoogle Scholar
  41. Eyre DR, Wu JJ (1983) Collagen of fibrocartilage: a distinctive molecular phenotype in bovine meniscus. FEBS Lett 158:265–270PubMedCrossRefGoogle Scholar
  42. Eyre DR, Brickley-Parsons DM, Glimcher MJ (1978) Predominance of type I collagen at the surface of avian articular cartilage. FEBS Lett 85:259–263PubMedCrossRefGoogle Scholar
  43. Fairbanks TJ (1948) Knee joint changes after meniscectomy. J Bone Joint Surg Br 30:664–670Google Scholar
  44. Fife RS (1985) Identification of link proteins and a 116,000-Dalton matrix protein in canine meniscus. Arch Biochem Biophys 240:682–688PubMedCrossRefGoogle Scholar
  45. Fithian DC, Kelly MA, Mow VC (1990) Material properties and structure-function relationships in the menisci. Clin Orthop Relat Res 252:19–31Google Scholar
  46. Fox AJ, Bedi A, Rodeo SA (2012) The basic science of human knee menisci: structure, composition, and function. Sports Health 4:340–351PubMedPubMedCentralCrossRefGoogle Scholar
  47. Fox AJ, Wanivenhaus F, Burge AJ, Warren RF, Rodeo SA (2015) The human meniscus: a review of anatomy, function, injury, and advances in treatment. Clin Anat 28:269–287PubMedCrossRefGoogle Scholar
  48. Frank RM, Cole BJ (2013) Complex cartilage cases in the athletic patient: advances in malalignment, instability, articular defects, and meniscal insufficiency. Phys Sportsmed 41:41–52PubMedCrossRefGoogle Scholar
  49. Freeman MAR, Meachim G (1979) Ageing and degeneration. In: Freeman MAR (ed) Adult articular cartilage, 2nd edn. Pitman, London, pp 487–543Google Scholar
  50. Fujii M, Furumatsu T, Yokoyama Y, Kanazawa T, Kajiki Y, Abe N, Ozaki T (2013) Chondromodulin-I derived from the inner meniscus prevents endothelial cell proliferation. J Orthop Res 31:538–543PubMedCrossRefGoogle Scholar
  51. Fujita N, Miyamoto T, Imai J, Hosogane N, Suzuki T, Yagi M, Morita K, Ninomiya K, Miyamoto K, Takaishi H, Matsumoto M, Morioka H, Yabe H, Chiba K, Watanabe S, Toyama Y, Suda T (2005) CD24 is expressed specifically in the nucleus pulposus of intervertebral discs. Biochem Biophys Res Commun 338:1890–1896PubMedCrossRefGoogle Scholar
  52. Gao J, Wei X, Messner K (1998) Healing of the anterior attachment of the rabbit meniscus to bone. Clin Orthop Relat Res 348:246–258CrossRefGoogle Scholar
  53. Gardner E, O’Rahilly R (1968) The early development of the knee joint in staged human embryos. J Anat 102:289–299PubMedPubMedCentralGoogle Scholar
  54. Ghadially FN, Thomas I, Yong N, Lalonde JM (1978) Ultrastructure of rabbit semilunar cartilages. J Anat 125:499–517PubMedPubMedCentralGoogle Scholar
  55. Ghosh P, Taylor TK (1987) The knee joint meniscus. A fibrocartilage of some distinction. Clin Orthop Relat Res 224:52–63Google Scholar
  56. Ghosh P, Ingman AM, Taylor TK (1975) Variations in collagen, non-collagenous proteins, and hexosamine in menisci derived from osteoarthritic and rheumatoid arthritic knee joints. J Rheumatol 2:100–107PubMedGoogle Scholar
  57. Goldring SR (2003) Pathogenesis of bone and cartilage destruction in rheumatoid arthritis. Rheumatology (Oxford) 42(Suppl 2ii):11–16Google Scholar
  58. Gorensek M, Jaksimovic C, Kregar-Velikonja N, Gorensek M, Knezevic M, Jeras M, Pavlovcic V, Cor A (2004) pulposus repair with cultured autologous elastic cartilage derived chondrocytes. Cell Mol Biol Lett 9:363–373PubMedGoogle Scholar
  59. Gouttenoire J, Valcourt U, Ronziere MC, Aubert-Foucher E, Mallein-Gerin F, Herbage D (2004) Modulation of collagen synthesis in normal and osteoarthritic cartilage. Biorheology 41:535–542PubMedGoogle Scholar
  60. Greenwald RA, Moy WW, Seibold J (1978) Functional properties of cartilage proteoglycans. Semin Arthritis Rheum 8:53–67PubMedCrossRefGoogle Scholar
  61. Hattori S, Oxford C, Reddi AH (2007) Identification of superficial zone articular chondrocyte stem/progenitor cells. Biochem Biophys Res Commun 358:99–103PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hay ED (2005) The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 233:706–720PubMedCrossRefGoogle Scholar
  63. Hayes AJ, Benjamin M, Ralphs JR (2001) Extracellular matrix in development of the intervertebral disc. Matrix Biol 20:107–121PubMedCrossRefGoogle Scholar
  64. Hayes AJ, Isaacs MD, Hughes C, Caterson B, Ralphs JR (2011) Collagen fibrillogenesis in the development of the annulus fibrosus of the intervertebral disc. Eur Cell Mater 22:226–241PubMedCrossRefGoogle Scholar
  65. He F, Pei M (2012) Rejuvenation of nucleus pulposus cells using extracellular matrix deposited by synovium-derived stem cells. Spine (Phila Pa 1976) 37:459–469CrossRefGoogle Scholar
  66. He F, Chen X, Pei M (2009) Reconstruction of an in vitro tissue-specific microenvironment to rejuvenate synovium-derived stem cells for cartilage tissue engineering. Tissue Eng Part A 15:3809–3821PubMedCrossRefGoogle Scholar
  67. Heinegard D, Oldberg A (1989) Structure and biology of cartilage and bone matrix noncollagenous macromolecules. FASEB J 3:2042–2051PubMedGoogle Scholar
  68. Herwig J, Egner E, Buddecke E (1984) Chemical changes of human knee joint menisci in various stages of degeneration. Ann Rheum Dis 43:635–640PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hiraki Y, Inoue H, Iyama K, Kamizono A, Ochiai M, Shukunami C, Iijima S, Suzuki F, Kondo J (1997) Identification of chondromodulin I as a novel endothelial cell growth inhibitor. Purification and its localization in the avascular zone of epiphyseal cartilage. J Biol Chem 272:32419–32426PubMedCrossRefGoogle Scholar
  70. Hodge WA, Carlson KL, Fijan RS, Burgess RG, Riley PO, Harris WH, Mann RW (1989) Contact pressures from an instrumented hip endoprosthesis. J Bone Joint Surg Am 71:1378–1386PubMedCrossRefGoogle Scholar
  71. Holm S, Maroudas A, Urban JP, Selstam G, Nachemson A (1981) Nutrition of the intervertebral disc: solute transport and metabolism. Connect Tissue Res 8:101–119PubMedCrossRefGoogle Scholar
  72. Höpker WW, Angres G, Klingel K, Komitowski D, Schuchardt E (1986) Changes of the elastin compartment in the human meniscus. Virchows Arch A 408:575–592CrossRefGoogle Scholar
  73. Hunter CJ, Matyas JR, Duncan NA (2003) The notochordal cell in the nucleus pulposus: a review in the context of tissue engineering. Tissue Eng 9:667–677PubMedCrossRefGoogle Scholar
  74. Hunter CJ, Matyas JR, Duncan NA (2004) The functional significance of cell clusters in the notochordal nucleus pulposus: survival and signaling in the canine intervertebral disc. Spine (Phila Pa 1976) 29:1099–1104CrossRefGoogle Scholar
  75. Hunziker EB (2002) Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 10:432–463PubMedCrossRefGoogle Scholar
  76. Hunziker EB (2010) The structure of articular cartilage. In: Archer C, Ralphs J (eds) Regenerative medicine and biomaterials for the repair of connective tissues. Woodhead, Sawston, pp 83–105CrossRefGoogle Scholar
  77. Hunziker EB, Kapfinger E, Geiss J (2007) The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthritis Cartilage 15:403–413PubMedCrossRefGoogle Scholar
  78. Hynes RO, Yamada KM (1982) Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95:369–377PubMedCrossRefGoogle Scholar
  79. Iatridis JC, Nicoll SB, Michalek AJ, Walter BA, Gupta MS (2013) Role of biomechanics in intervertebral disc degeneration and regenerative therapies: what needs repairing in the disc and what are promising biomaterials for its repair? Spine J 13:243–262PubMedPubMedCentralCrossRefGoogle Scholar
  80. Ikeda T, Kamekura S, Mabuchi A, Kou I, Seki S, Takato T, Nakamura K, Kawaguchi H, Ikegawa S, Chung UI (2004) The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum 50:3561–3573PubMedCrossRefGoogle Scholar
  81. Inkinen RI, Lammi MJ, Lehmonen S, Puustjarvi K, Kaapa E, Tammi MI (1998) Relative increase of biglycan and decorin and altered chondroitin sulfate epitopes in the degenerating human intervertebral disc. J Rheumatol 25:506–514PubMedGoogle Scholar
  82. Inoue H (1981) Three-dimensional architecture of lumbar intervertebral discs. Spine (Phila Pa 1976) 6:139–146CrossRefGoogle Scholar
  83. Iwamoto M, Tamamura Y, Koyama E, Komori T, Takeshita N, Williams JA, Nakamura T, Enomoto-Iwamoto M, Pacifici M (2007) Transcription factor ERG and joint and articular cartilage formation during mouse limb and spine skeletogenesis. Dev Biol 305:40–51PubMedPubMedCentralCrossRefGoogle Scholar
  84. Jackson AR (2015) Notochordal nucleus pulposus cells: prospective strategies for intervertebral disc repair and regeneration. Curr Tissue Eng 4:77–85CrossRefGoogle Scholar
  85. Johnson EF, Chetty K, Moore IM, Stewart A, Jones W (1982) The distribution and arrangement of elastic fibres in the intervertebral disc of the adult human. J Anat 135:301–309PubMedPubMedCentralGoogle Scholar
  86. Johnson WE, Evans H, Menage J, Eisenstein SM, El Haj A, Roberts S (2001) Immunohistochemical detection of Schwann cells in innervated and vascularized human intervertebral discs. Spine (Phila Pa 1976) 26:2550–2557CrossRefGoogle Scholar
  87. Johnstone B, Bayliss MT (1995) The large proteoglycans of the human intervertebral disc. Changes in their biosynthesis and structure with age, topography, and pathology. Spine (Phila Pa 1976) 20:674–684CrossRefGoogle Scholar
  88. Jones BA, Pei M (2012) Synovium-derived stem cells: a tissue-specific stem cell for cartilage engineering and regeneration. Tissue Eng Part B 18:301–311CrossRefGoogle Scholar
  89. Jortikka MO, Inkinen RI, Tammi MI, Parkkinen JJ, Haapala J, Kiviranta I, Helminen HJ, Lammi MJ (1997) Immobilisation causes longlasting matrix changes both in the immobilised and contralateral joint cartilage. Ann Rheum Dis 56:255–261PubMedPubMedCentralCrossRefGoogle Scholar
  90. Jurvelin J, Saamanen AM, Arokoski J, Helminen HJ, Kiviranta I, Tammi M (1988) Biomechanical properties of the canine knee articular cartilage as related to matrix proteoglycans and collagen. Eng Med 17:157–162PubMedCrossRefGoogle Scholar
  91. Kambic HE, Futani H, McDevitt CA (2000) Cell, matrix changes and alpha-smooth muscle actin expression in repair of the canine meniscus. Wound Repair Regen 8:554–561PubMedCrossRefGoogle Scholar
  92. Kempson GE, Muir H, Swanson SA, Freeman MA (1970) Correlations between stiffness and the chemical constituents of cartilage on the human femoral head. Biochim Biophys Acta 215:70–77PubMedCrossRefGoogle Scholar
  93. Kennedy JC, Alexander IJ, Hayes KC (1982) Nerve supply of the human knee and its functional importance. Am J Sports Med 10:329–335PubMedCrossRefGoogle Scholar
  94. Kevorkian L, Young DA, Darrah C, Donell ST, Shepstone L, Porter S, Brockbank SM, Edwards DR, Parker AE, Clark IM (2004) Expression profiling of metalloproteinases and their inhibitors in cartilage. Arthritis Rheum 50:131–141PubMedCrossRefGoogle Scholar
  95. Khan IM, Salter DM, Bayliss MT, Thomson BM, Archer CW (2001) Expression of clusterin in the superficial zone of bovine articular cartilage. Arthritis Rheum 44:1795–1799PubMedCrossRefGoogle Scholar
  96. King D (1936) The function of semilunar cartilages. J Bone Joint Surg Am 18:1069–1076Google Scholar
  97. Kizawa H, Kou I, Iida A, Sudo A, Miyamoto Y, Fukuda A, Mabuchi A, Kotani A, Kawakami A, Yamamoto S, Uchida A, Nakamura K, Notoya K, Nakamura Y, Ikegawa S (2005) An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat Genet 37:138–144PubMedCrossRefGoogle Scholar
  98. Kopher RA, Penchev VR, Islam MS, Hill KL, Khosla S, Kaufman DS (2010) Human embryonic stem cell-derived CD34+ cells function as MSC progenitor cells. Bone 47:718–728PubMedPubMedCentralCrossRefGoogle Scholar
  99. Koyama E, Shibukawa Y, Nagayama M, Sugito H, Young B, Yuasa T, Okabe T, Ochiai T, Kamiya N, Rountree RB, Kingsley DM, Iwamoto M, Enomoto-Iwamoto M, Pacifici M (2008) A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev Biol 316:62–73PubMedPubMedCentralCrossRefGoogle Scholar
  100. Kypriotou M, Fossard-Demoor M, Chadjichristos C, Ghayor C, de Crombrugghe B, Pujol JP, Galera P (2003) SOX9 exerts a bifunctional effect on type II collagen gene (COL2A1) expression in chondrocytes depending on the differentiation state. DNA Cell Biol 22:119–129PubMedCrossRefGoogle Scholar
  101. Lee H-Y, Han L, Roughley PJ, Grodzinsky AJ, Ortiz C (2013) Age-related nanostructural and nanomechanical changes of individual human cartilage aggrecan monomers and their glycosaminoglycan side chairs. J Struct Biol 181:264–273PubMedCrossRefGoogle Scholar
  102. Lefebvre V, de Crombrugghe B (1998) Toward understanding SOX9 function in chondrocyte differentiation. Matrix Biol 16:529–540PubMedCrossRefGoogle Scholar
  103. Lin BY, Richmond JC, Spector M (2002) Contractile actin expression in torn human menisci. Wound Repair Regen 10:259–266PubMedCrossRefGoogle Scholar
  104. Loeser RF, Goldring SR, Scanzello CR, Goldring MB (2012) Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum 64:1697–1707PubMedPubMedCentralCrossRefGoogle Scholar
  105. Lorenzo P, Bayliss MT, Heinegard D (1998) A novel cartilage protein (CILP) present in the mid-zone of human articular cartilage increases with age. J Biol Chem 273:23463–23468PubMedCrossRefGoogle Scholar
  106. Maroudas AI (1976) Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 260:808–809PubMedCrossRefGoogle Scholar
  107. Maroudas A, Venn M (1977) Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling. Ann Rheum Dis 36:399–406PubMedPubMedCentralCrossRefGoogle Scholar
  108. Maroudas A, Stockwell RA, Nachemson A, Urban J (1975) Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. J Anat 120:113–130PubMedPubMedCentralGoogle Scholar
  109. McDevitt CA, Webber RJ (1990) The ultrastructure and biochemistry of meniscal cartilage. Clin Orthop Relat Res 252:8–18Google Scholar
  110. Meirer F, Pemmer B, Pepponi G, Zoeger N, Wobrauschek P, Sprio S, Tampieri A, Goettlicher J, Steininger R, Mangold S, Roschger P, Berzlanovich A, Hofstaetter JG, Streli C (2011) Assessment of chemical species of lead accumulated in tidemarks of human articular cartilage by X-ray absorption near-edge structure analysis. J Synchrotron Radiat 18:238–244PubMedPubMedCentralCrossRefGoogle Scholar
  111. Melrose J, Ghosh P, Taylor TK (2001) A comparative analysis of the differential spatial and temporal distributions of the large (aggrecan, versican) and small (decorin, biglycan, fibromodulin) proteoglycans of the intervertebral disc. J Anat 198:3–15PubMedPubMedCentralCrossRefGoogle Scholar
  112. Melrose J, Smith S, Cake M, Read R, Whitelock J (2005) Comparative spatial and temporal localisation of perlecan, aggrecan and type I, II and IV collagen in the ovine meniscus: an ageing study. Histochem Cell Biol 124:225–235PubMedCrossRefGoogle Scholar
  113. Merida-Velasco JA, Sanchez-Montesinos I, Espin-Ferra J, Merida-Velasco JR, Rodriguez-Vazquez JF, Jimenez-Collado J (1997) Development of the human knee joint ligaments. Anat Rec 248:259–268PubMedCrossRefGoogle Scholar
  114. Mi M, Shi S, Li T, Holz J, Lee YJ, Sheu TJ, Liao Q, Xiao T (2012) TIMP2 deficient mice develop accelerated osteoarthritis via promotion of angiogenesis upon destabilization of the medial meniscus. Biochem Biophys Res Commun 423:366–372PubMedCrossRefGoogle Scholar
  115. Millward-Sadler SJ, Wright MO, Flatman PW, Salter DM (2004) ATP in the mechanotransduction pathway of normal human chondrocytes. Biorheology 41:567–575PubMedGoogle Scholar
  116. Mine T, Kimura M, Sakka A, Kawai S (2000) Innervation of nociceptors in the menisci of the knee joint: an immunohistochemical study. Arch Orthop Trauma Surg 120:201–204PubMedCrossRefGoogle Scholar
  117. Minogue BM, Richardson SM, Zeef LA, Freemont AJ, Hoyland JA (2010a) Characterization of the human nucleus pulposus cell phenotype and evaluation of novel marker gene expression to define adult stem cell differentiation. Arthritis Rheum 62:3695–3705PubMedCrossRefGoogle Scholar
  118. Minogue BM, Richardson SM, Zeef LA, Freemont AJ, Hoyland JA (2010b) Transcriptional profiling of bovine intervertebral disc cells: implications for identification of normal and degenerate human intervertebral disc cell phenotypes. Arthritis Res Ther 12:R22PubMedPubMedCentralCrossRefGoogle Scholar
  119. Mort JS, Caterson B, Poole AR, Roughley PJ (1985) The origin of human cartilage proteoglycan link-protein heterogeneity and fragmentation during aging. Biochem J 232:805–812PubMedPubMedCentralCrossRefGoogle Scholar
  120. Muinos-Lopez E, Rendal-Vazquez ME, Hermida-Gomez T, Fuentes-Boquete I, Diaz-Prado S, Blanco FJ (2012) Cryopreservation effect on proliferative and chondrogenic potential of human chondrocytes isolated from superficial and deep cartilage. Open Orthop J 6:150–159PubMedPubMedCentralCrossRefGoogle Scholar
  121. Musumeci G, Trovato FM, Pichler K, Weinberg AM, Loreto C, Castrogiovanni P (2013) Extra-virgin olive oil diet and mild physical activity prevent cartilage degeneration in an osteoarthritis model: an in vivo and in vitro study on lubricin expression. J Nutr Biochem 24:2064–2075PubMedCrossRefGoogle Scholar
  122. Musumeci G, Castrogiovanni P, Leonardi R, Trovato FM, Szychlinska MA, Di Giunta A, Loreto C, Castorina S (2014) New perspectives for articular cartilage repair treatment through tissue engineering: A contemporary review. World J Orthop 5:80–88PubMedPubMedCentralCrossRefGoogle Scholar
  123. Mwale F, Roughley P, Antoniou J (2004) Distinction between the extracellular matrix of the nucleus pulposus and hyaline cartilage: a requisite for tissue engineering of intervertebral disc. Eur Cell Mater 8:58–63, discussion 63–54PubMedCrossRefGoogle Scholar
  124. Nakamichi Y, Shukunami C, Yamada T, Aihara K, Kawano H, Sato T, Nishizaki Y, Yamamoto Y, Shindo M, Yoshimura K, Nakamura T, Takahashi N, Kawaguchi H, Hiraki Y, Kato S (2003) Chondromodulin I is a bone remodeling factor. Mol Cell Biol 23:636–644PubMedPubMedCentralCrossRefGoogle Scholar
  125. Nakata K, Shino K, Hamada M, Miyama T, Shinjo H, Horibe S, Tada K, Ochi T, Yoshikawa H (2001) Human meniscus cell: characterization of the primary culture and use for tissue engineering. Clin Orthop Relat Res 391(Suppl):S208–218CrossRefGoogle Scholar
  126. Nakaya Y, Sheng G (2008) Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev Growth Differ 50:755–766PubMedCrossRefGoogle Scholar
  127. Nerurkar NL, Elliott DM, Mauck RL (2010) Mechanical design criteria for intervertebral disc tissue engineering. J Biomech 43:1017–1030PubMedPubMedCentralCrossRefGoogle Scholar
  128. Nixon J (1986) Intervetebral disc mechanics: a review. J R Soc Med 79:100–104PubMedPubMedCentralCrossRefGoogle Scholar
  129. Noyes FR, Stabler CL (1989) A system for grading articular cartilage lesions at arthroscopy. Am J Sports Med 17:505–513PubMedCrossRefGoogle Scholar
  130. Ochi K, Daigo Y, Katagiri T, Saito-Hisaminato A, Tsunoda T, Toyama Y, Matsumoto H, Nakamura Y (2003) Expression profiles of two types of human knee-joint cartilage. J Hum Genet 48:177–182PubMedCrossRefGoogle Scholar
  131. O’Connor BL (1984) The mechanoreceptor innervation of the posterior attachments of the lateral meniscus of the dog knee joint. J Anat 138:15–26PubMedPubMedCentralGoogle Scholar
  132. O’Connor BL, McConnaughey JS (1978) The structure and innervation of cat knee menisci, and their relation to a “sensory hypothesis” of meniscal function. Am J Anat 153:431–442PubMedCrossRefGoogle Scholar
  133. Ogawa H, Kozhemyakina E, Hung HH, Grodzinsky AJ, Lassar AB (2014) Mechanical motion promotes expression of Prg4 in articular cartilage via multiple CREB-dependent, fluid flow shear stress-induced signaling pathways. Genes Dev 28:127–139PubMedPubMedCentralCrossRefGoogle Scholar
  134. Oldberg A, Antonsson P, Hedbom E, Heinegard D (1990) Structure and function of extracellular matrix proteoglycans. Biochem Soc Trans 18:789–792PubMedCrossRefGoogle Scholar
  135. Pacifici M, Koyama E, Shibukawa Y, Wu C, Tamamura Y, Enomoto-Iwamoto M, Iwamoto M (2006) Cellular and molecular mechanisms of synovial joint and articular cartilage formation. Ann N Y Acad Sci 1068:74–86PubMedPubMedCentralCrossRefGoogle Scholar
  136. Patra D, Sandell LJ (2012) Antiangiogenic and anticancer molecules in cartilage. Expert Rev Mol Med 14:e10PubMedCrossRefGoogle Scholar
  137. Pattappa G, Li Z, Peroglio M, Wismer N, Alini M, Grad S (2012) Diversity of intervertebral disc cells: phenotype and function. J Anat 221:480–496PubMedPubMedCentralCrossRefGoogle Scholar
  138. Pazin DE, Gamer LW, Capelo LP, Cox KA, Rosen V (2014) Gene signature of the embryonic meniscus. J Orthop Res 32:46–53PubMedCrossRefGoogle Scholar
  139. Peacock A (1951) Observations on the prenatal development of the intervertebral disc in man. J Anat 85:260–274PubMedPubMedCentralGoogle Scholar
  140. Pearce RH, Mathieson JM, Mort JS, Roughley PJ (1989) Effect of age on the abundance and fragmentation of link protein of the human intervertebral disc. J Orthop Res 7:861–867PubMedCrossRefGoogle Scholar
  141. Pearle AD, Warren RF, Rodeo SA (2005) Basic science of articular cartilage and osteoarthritis. Clin Sports Med 24:1–12PubMedCrossRefGoogle Scholar
  142. Pei M, Seidel J, Vunjak-Novakovic G, Freed LE (2002) Growth factors for sequential cellular de- and re-differentiation in tissue engineering. Biochem Biophys Res Commun 294:149–154PubMedCrossRefGoogle Scholar
  143. Pei M, He F, Kish VL (2011a) Expansion on extracellular matrix deposited by human bone marrow stromal cells facilitates stem cell proliferation and tissue-specific lineage potential. Tissue Eng Part A 17:3067–3076PubMedPubMedCentralCrossRefGoogle Scholar
  144. Pei M, Li JT, Shoukry M, Zhang Y (2011b) A review of decellularized stem cell matrix: a novel cell expansion system for cartilage tissue engineering. Eur Cell Mater 22:333–343, discussion 343 PubMedCrossRefGoogle Scholar
  145. Pei M, Shoukry M, Li J, Daffner SD, France JC, Emery SE (2012) Modulation of in vitro microenvironment facilitates synovium-derived stem cell-based nucleus pulposus tissue regeneration. Spine (Phila Pa 1976) 37:1538–1547CrossRefGoogle Scholar
  146. Peters H, Wilm B, Sakai N, Imai K, Maas R, Balling R (1999) Pax1 and Pax9 synergistically regulate vertebral column development. Development 126:5399–5408PubMedGoogle Scholar
  147. Pizzute T, Lynch K, Pei M (2015) Impact of tissue-specific stem cells on lineage-specific differentiation: a focus on the musculoskeletal system. Stem Cell Rev 11:119–132PubMedPubMedCentralCrossRefGoogle Scholar
  148. Poole CA (1997) Articular cartilage chondrons: form, function and failure. J Anat 191:1–13PubMedPubMedCentralCrossRefGoogle Scholar
  149. Poole AR, Kojima T, Yasuda T, Mwale F, Kobayashi M, Laverty S (2001) Composition and structure of articular cartilage: a template for tissue repair. Clin Orthop Relat Res 391(Suppl):S26–33CrossRefGoogle Scholar
  150. Power KA, Grad S, Rutges JP, Creemers LB, van Rijen MH, O’Gaora P, Wall JG, Alini M, Pandit A, Gallagher WM (2011) Identification of cell surface-specific markers to target human nucleus pulposus cells: expression of carbonic anhydrase XII varies with age and degeneration. Arthritis Rheum 63:3876–3886PubMedCrossRefGoogle Scholar
  151. Proffen BL, McElfresh M, Fleming BC, Murray MM (2012) A comparative anatomical study of the human knee and six animal species. Knee 19:493–499PubMedCrossRefGoogle Scholar
  152. Pufe T, Petersen WJ, Miosge N, Goldring MB, Mentlein R, Varoga DJ, Tillmann BN (2004) Endostatin/collagen XVIII--an inhibitor of angiogenesis--is expressed in cartilage and fibrocartilage. Matrix Biol 23:267–276PubMedCrossRefGoogle Scholar
  153. Quinn TM, Häuselmann HJ, Shintani N, Hunziker EB (2013) Cell and matrix morphology in articular cartilage from adult human knee and ankle joints suggests depth-associated adaptations to biomechanical and anatomical roles. Osteoarthritis Cartilage 21:1904–1912PubMedCrossRefGoogle Scholar
  154. Raj PP (2008) Intervertebral disc: anatomy-physiology-pathophysiology-treatment. Pain Pract 8:18–44PubMedCrossRefGoogle Scholar
  155. Rajpurohit R, Risbud MV, Ducheyne P, Vresilovic EJ, Shapiro IM (2002) Phenotypic characteristics of the nucleus pulposus: expression of hypoxia inducing factor-1, glucose transporter-1 and MMP-2. Cell Tissue Res 308:401–407PubMedCrossRefGoogle Scholar
  156. Ray A, Singh PN, Sohaskey ML, Harland RM, Bandyopadhyay A (2015) Precise spatial restriction of BMP signaling is essential for articular cartilage differentiation. Development 142:1169–1179PubMedPubMedCentralCrossRefGoogle Scholar
  157. Renström P, Johnson RJ (1990) Anatomy and biomechanics of the menisci. Clin Sports Med 9:523–538PubMedGoogle Scholar
  158. Responte DJ, Lee JK, Hu JC, Athanasiou KA (2012) Biomechanics-driven chondrogenesis: from embryo to adult. FASEB J 26:3614–3624PubMedPubMedCentralCrossRefGoogle Scholar
  159. Richardson SM, Knowles R, Tyler J, Mobasheri A, Hoyland JA (2008) Expression of glucose transporters GLUT-1, GLUT-3, GLUT-9 and HIF-1alpha in normal and degenerate human intervertebral disc. Histochem Cell Biol 129:503–511PubMedCrossRefGoogle Scholar
  160. Risbud MV, Guttapalli A, Stokes DG, Hawkins D, Danielson KG, Schaer TP, Albert TJ, Shapiro IM (2006) Nucleus pulposus cells express HIF-1 alpha under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment. J Cell Biochem 98:152–159PubMedCrossRefGoogle Scholar
  161. Risbud MV, Guttapalli A, Tsai TT, Lee JY, Danielson KG, Vaccaro AR, Albert TJ, Gazit Z, Gazit D, Shapiro IM (2007) Evidence for skeletal progenitor cells in the degenerate human intervertebral disc. Spine (Phila Pa 1976) 32:2537–2544CrossRefGoogle Scholar
  162. Risbud MV, Schoepflin ZR, Mwale F, Kandel RA, Grad S, Iatridis JC, Sakai D, Hoyland JA (2015) Defining the phenotype of young healthy nucleus pulposus cells: recommendations of the Spine Research Interest Group at the 2014 annual ORS meeting. J Orthop Res 33:283–293PubMedPubMedCentralCrossRefGoogle Scholar
  163. Roberts S, Eisenstein SM, Menage J, Evans EH, Ashton IK (1995) Mechanoreceptors in intervertebral discs. Morphology, distribution, and neuropeptides. Spine (Phila Pa 1976) 20:2645–2651CrossRefGoogle Scholar
  164. Rodrigues-Pinto R, Richardson SM, Hoyland JA (2014) An understanding of intervertebral disc development, maturation and cell phenotype provides clues to direct cell-based tissue regeneration therapies for disc degeneration. Eur Spine J 23:1803–1814PubMedCrossRefGoogle Scholar
  165. Rutges J, Creemers LB, Dhert W, Milz S, Sakai D, Mochida J, Alini M, Grad S (2010) Variations in gene and protein expression in human nucleus pulposus in comparison with annulus fibrosus and cartilage cells: potential associations with aging and degeneration. Osteoarthritis Cartilage 18:416–423PubMedCrossRefGoogle Scholar
  166. Sakai D, Nakamura Y, Nakai T, Mishima T, Kato S, Grad S, Alini M, Risbud MV, Chan D, Cheah KS, Yamamura K, Masuda K, Okano H, Ando K, Mochida J (2012) Exhaustion of nucleus pulposus progenitor cells with ageing and degeneration of the intervertebral disc. Nat Commun 3:1264PubMedPubMedCentralCrossRefGoogle Scholar
  167. Sato K, Kikuchi S, Yonezawa T (1999) In vivo intradiscal pressure measurement in healthy individuals and in patients with ongoing back problems. Spine (Phila Pa 1976) 24:2468–2474CrossRefGoogle Scholar
  168. Schmid TM, Linsenmayer TF (1985) Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues. J Cell Biol 100:598–605PubMedCrossRefGoogle Scholar
  169. Schumacher BL, Block JA, Schmid TM, Aydelotte MB, Kuettner KE (1994) A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. Arch Biochem Biophys 311:144–152PubMedCrossRefGoogle Scholar
  170. Shine KM, Simson JA, Spector M (2009) Lubricin distribution in the human intervertebral disc. J Bone Joint Surg Am 91:2205–2212PubMedCrossRefGoogle Scholar
  171. Shoukry M, Li J, Pei M (2013) Reconstruction of an in vitro niche for the transition from intervertebral disc development to nucleus pulposus regeneration. Stem Cells Dev 22:1162–1176PubMedCrossRefGoogle Scholar
  172. Shrive N (1974) The weight-bearing role of the menisci of the knee. J Bone J Joint [Br] 56:381Google Scholar
  173. Shrive NG, O’Connor JJ, Goodfellow JW (1978) Load bearing in the knee joint. Clin Orthop Relat Res 131:279–287Google Scholar
  174. Shwartz Y, Viukov S, Krief S, Zelzer E (2016) Joint development involves a continuous influx of Gdf5-positive cells. Cell Rep 15:2577–2587PubMedPubMedCentralCrossRefGoogle Scholar
  175. Sive JI, Baird P, Jeziorsk M, Watkins A, Hoyland JA, Freemont AJ (2002) Expression of chondrocyte markers by cells of normal and degenerate intervertebral discs. Mol Pathol 55:91–97PubMedPubMedCentralCrossRefGoogle Scholar
  176. Skaggs DL, Warden WH, Mow VC (1994) Radial tie fibers influence the tensile properties of the bovine medial meniscus. J Orthop Res 12:176–185PubMedCrossRefGoogle Scholar
  177. Smith LJ, Nerurkar NL, Choi KS, Harfe BD, Elliott DM (2011) Degeneration and regeneration of the intervertebral disc: lessons from development. Dis Model Mech 4:31–41PubMedCrossRefGoogle Scholar
  178. Spilker RL, Donzelli PS, Mow VC (1992) A transversely isotropic biphasic finite element model of the meniscus. J Biomech 25:1027–1045PubMedCrossRefGoogle Scholar
  179. Stockwell RA (1971) The interrelationship of cell density and cartilage thickness in mammalian articular cartilage. J Anat 109:411–421PubMedPubMedCentralGoogle Scholar
  180. Stosiek P, Kasper M, Karsten U (1988) Expression of cytokeratin and vimentin in nucleus pulposus cells. Differentiation 39:78–81PubMedCrossRefGoogle Scholar
  181. Sun Z, Wan ZY, Guo YS, Wang HQ, Luo ZJ (2013) FasL on human nucleus pulposus cells prevents angiogenesis in the disc by inducing Fas-mediated apoptosis of vascular endothelial cells. Int J Clin Exp Pathol 6:2376–2385PubMedPubMedCentralGoogle Scholar
  182. Takao T, Iwaki T, Kondo J, Hiraki Y (2000) Immunohistochemistry of chondromodulin-I in the human intervertebral discs with special reference to the degenerative changes. Histochem J 32:545–550PubMedCrossRefGoogle Scholar
  183. Tao Y, Zhou X, Liu D, Li H, Liang C, Li F, Chen Q (2016) Proportion of collagen type II in the extracellular matrix promotes the differentiation of human adipose-derived mesenchymal stem cells into nucleus pulposus cells. Biofactors 42:212–223PubMedGoogle Scholar
  184. Tengblad A, Pearce RH, Grimmer BJ (1984) Demonstration of link protein in proteoglycan aggregates from human intervertebral disc. Biochem J 222:85–92PubMedPubMedCentralCrossRefGoogle Scholar
  185. Tian Y, Yuan W, Fujita N, Wang J, Wang H, Shapiro IM, Risbud MV (2013) Inflammatory cytokines associated with degenerative disc disease control aggrecanase-1 (ADAMTS-4) expression in nucleus pulposus cells through MAPK and NF-kappaB. Am J Pathol 182:2310–2321PubMedPubMedCentralCrossRefGoogle Scholar
  186. Tran CM, Fujita N, Huang BL, Ong JR, Lyons KM, Shapiro IM, Risbud MV (2013) Hypoxia-inducible factor (HIF)-1alpha and CCN2 form a regulatory circuit in hypoxic nucleus pulposus cells: CCN2 suppresses HIF-1alpha level and transcriptional activity. J Biol Chem 288:12654–12666PubMedPubMedCentralCrossRefGoogle Scholar
  187. Treppo S, Koepp H, Quan EC, Cole AA, Kuettner KE, Grodzinsky AJ (2000) Comparison of biomechanical and biochemical properties of cartilage from human knee and ankle pairs. J Orthop Res 18:739–748PubMedCrossRefGoogle Scholar
  188. Upton ML, Chen J, Setton LA (2006) Region-specific constitutive gene expression in the adult porcine meniscus. J Orthop Res 24:1562–1570PubMedCrossRefGoogle Scholar
  189. Urban JP, McMullin JF (1988) Swelling pressures of the lumbar intervertebral discs: influence of age, spinal level, composition, and degeneration. Spine (Phila Pa 1976) 13:179–187CrossRefGoogle Scholar
  190. Urban JP, Roberts S (1995) Development and degeneration of the intervertebral discs. Mol Med Today 1:329–335PubMedCrossRefGoogle Scholar
  191. Urban JP, Maroudas A, Bayliss MT, Dillon J (1979) Swelling pressures of proteoglycans at the concentrations found in cartilaginous tissues. Biorheology 16:447–464PubMedGoogle Scholar
  192. Verdonk PC, Forsyth RG, Wang J, Almqvist KF, Verdonk R, Veys EM, Verbruggen G (2005) Characterisation of human knee meniscus cell phenotype. Osteoarthritis Cartilage 13:548–560PubMedCrossRefGoogle Scholar
  193. Vergroesen P-PA, van der Veen AJ, van Royen BJ, Kingma I, Smit TH (2014) Intradiscal pressure depends on recent loading and correlates with disc height and compressive stiffness. Eur Spine J 23:2359–2368PubMedCrossRefGoogle Scholar
  194. Vonk LA, Kroeze RJ, Doulabi BZ, Hoogendoorn RJ, Huang C, Helder MN, Everts V, Bank RA (2010) Caprine articular, meniscus and intervertebral disc cartilage: an integral analysis of collagen network and chondrocytes. Matrix Biol 29:209–218PubMedCrossRefGoogle Scholar
  195. Walker PS, Erkman MJ (1975) The role of the menisci in force transmission across the knee. Clin Orthop Relat Res 109:184–192CrossRefGoogle Scholar
  196. Wang P, Zhang F, He Q, Wang J, Shiu HT, Shu Y, Tsang WP, Liang S, Zhao K, Wan C (2016) Flavonoid compound icariin activates hypoxia inducible factor-1alpha in chondrocytes and promotes articular cartilage repair. PLoS ONE 11:e0148372PubMedPubMedCentralCrossRefGoogle Scholar
  197. Warren R, Arnoczky SP, Wickiewicz TL (1986) Anatomy of the knee. In: Nicholas JA, Hershman EB (eds) The lower extremity and spine in sports medicine. Mosby: St. Louis, pp 657–694Google Scholar
  198. Waters RL, Lunsford BR, Perry J, Byrd R (1988) Energy-speed relationship of walking: standard tables. J Orthop Res 6:215–222PubMedCrossRefGoogle Scholar
  199. Wilke HJ, Neef P, Caimi M, Hoogland T, Claes LE (1999) New in vivo measurements of pressures in the intervertebral disc in daily life. Spine (Phila Pa 1976) 24:755–762CrossRefGoogle Scholar
  200. Wilke HJ, Neef P, Hinz B, Seidel H, Claes L (2001) Intradiscal pressure together with anthropometric data—a data set for the volidation of models. Clin Biomech (Bristol, Avon) 16(Suppl 1):S111–126CrossRefGoogle Scholar
  201. Williamson AK, Chen AC, Sah RL (2001) Compressive properties and function-composition relationships of developing bovine articular cartilage. J Orthop Res 19:1113–1121PubMedCrossRefGoogle Scholar
  202. Williamson AK, Chen AC, Masuda K, Thonar EJ, Sah RL (2003) Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. J Orthop Res 21:872–880PubMedCrossRefGoogle Scholar
  203. Wong M, Carter DR (2003) Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33:1–13PubMedCrossRefGoogle Scholar
  204. Yasuhara R, Ohta Y, Yuasa T, Kondo N, Hoang T, Addya S, Fortina P, Pacifici M, Iwamoto M, Enomoto-Iwamoto M (2011) Roles of beta-catenin signaling in phenotypic expression and proliferation of articular cartilage superficial zone cells. Lab Invest 91:1739–1752PubMedPubMedCentralCrossRefGoogle Scholar
  205. Yu J, Tirlapur U, Fairbank J, Handford P, Roberts S, Winlove CP, Cui Z, Urban J (2007) Microfibrils, elastin fibres and collagen fibres in the human intervertebral disc and bovine tail disc. J Anat 210:460–471PubMedPubMedCentralCrossRefGoogle Scholar
  206. Yukata K, Matsui Y, Shukunami C, Takimoto A, Goto T, Nishizaki Y, Nakamichi Y, Kubo T, Sano T, Kato S, Hiraki Y, Yasui N (2008) Altered fracture callus formation in chondromodulin-I deficient mice. Bone 43:1047–1056PubMedCrossRefGoogle Scholar
  207. Zhang Y, Pizzute T, Pei M (2014) A review of crosstalk between MAPK and Wnt signals and its impact on cartilage regeneration. Cell Tissue Res 358:633–649PubMedPubMedCentralCrossRefGoogle Scholar
  208. Zhang Y, Chen S, Pei M (2016a) Biomechanical signals guiding stem cell cartilage engineering: from molecular adaption to tissue functionality. Eur Cell Mater 30:59–78CrossRefGoogle Scholar
  209. Zhang X, Prasadam I, Fang W, Crawford R, Xiao Y (2016b) Chondromodulin-1 ameliorates osteoarthritis progression by inhibiting HIF-2alpha activity. Osteoarthritis Cartilage 24:1970–1980PubMedCrossRefGoogle Scholar
  210. Zimny ML, Albright DJ, Dabezies E (1988) Mechanoreceptors in the human medial meniscus. Acta Anat (Basel) 133:35–40CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Stem Cell and Tissue Engineering Laboratory, Department of Orthopaedics and Division of Exercise PhysiologyWest Virginia UniversityMorgantownUSA
  2. 2.Department of Orthopaedics, Changzheng HospitalSecond Military Medical UniversityShanghaiPeople’s Republic of China

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