Postnatal development of collagen structure in ovine articular cartilage

BMC Developmental Biology

Volumn 10, Issue , 2010, Pages

  Van Turnhout, Mark C ^a   Schipper, Henk ^a   Engel, Bas ^a   Buist, Willem ^a   Kranenbarg, Sander ^a   Van Leeuwen, Johan L ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN;

ANIMAL; ARTICLE; ARTICULAR CARTILAGE; CHEMISTRY; FEMALE; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; POLARIZATION MICROSCOPY; SEXUAL MATURATION; SHEEP;

ANIMALS; CARTILAGE, ARTICULAR; COLLAGEN; FEMALE; MALE; MICROSCOPY, POLARIZATION; SEXUAL MATURATION; SHEEP;

EID: 77953063676     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-10-62     Document Type: Article

References (76)

1. The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. E Hunziker E Kapfinger J Geiss, Osteoarthritis & Cartilage 2007 15 4 403 413 [Corrigendum in Osteoarthritis & Cartilage 15 (2007) 403-413.] 10.1016/j.joca.2006.09.010 17098451
2. Cellular aspects of the development of diarthrodial joints and articular cartilage. CW Archer H Morrison AA Pitsillides, Journal of Anatomy 1994 184 Pt 3 447 456 7928634
3. The development of articular cartilage: evidence for an appositional growth mechanism. A Hayes S MacPherson H Morrison G Dowthwaite C Archer, Anatomy and Embryology 2001 203 6 469 479 10.1007/s004290100178 11453164
4. Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint. P Brama J Tekoppele R Bank D Karssenberg A Barneveld P Van Weeren, Equine Veterinary Journal 2000 32 19 26 10.2746/042516400777612062 10661380
5. Functional adaptation of equine articular cartilage: the formation of regional biochemical characteristics up to age one year. P Brama J TeKoppele R Bank A Barneveld P Van Weeren, Equine Veterinary Journal 2000 32 3 217 221 10.2746/042516400776563626 10836476
6. Functional adaptation of articular cartilage from birth to maturity under the influence of loading: a biomechanical analysis. H Brommer P Brama M Laasanen H Helminen Jurvelin Van Weeren J PRand, Equine Veterinary Journal 2005 37 2 148 154 10.2746/0425164054223769 15779628
7. Regular joint loading in youth assists in the establishment and strengthening of the collagen network of articular cartilage and contributes to the prevention of osteoarthrosis later in life: a hypothesis. HJ Helminen MM Hyttinen MJ Lammi JP Arokoski T Lapveteläinen J Jurvelin I Kiviranta MI Tammi, Journal of Bone and Mineral Metabolism 2000 18 5 245 257 10.1007/PL00010638 10959613
8. Biochemical composition of equine carpal articular cartilage is influenced by short-term exercise in a site-specific manner. R Murray H Birch K Lakhani A Goodship, Osteoarthritis & Cartilage 2001 9 7 625 632 10.1053/joca.2001.0462 11597175
9. Influence of different exercise levels and age on the biochemical characteristics of immature equine articular cartilage. P Brama J TeKoppele R Bank P Van Weeren A Barneveld, Equine Veterinary Journal Supplement 1999 31 55 61 10999661
10. Contact areas and pressure distribution on the proximal articular surface of the proximal phalanx under sagittal plane loading. P Brama D Karssenberg A Barneveld P Van Weeren, Equine Veterinary Journal 2001 33 26 32 10.2746/042516401776767377 11191606
11. Contact pressures in the human hip joint measured in vivo. W Hodge R Fijan K Carlson R Burgess W Harris R Mann, Proceedings of the National Academy of Sciences of the United States of America 1986 83 9 2879 2883 10.1073/pnas.83.9.2879 3458248
12. Contact area and pressure distribution changes of the equine third carpal bone during loading. JL Palmer AL Bertone A Litsky, Equine Veterinary Journal 1994 26 3 197 202 10.1111/j.2042-3306.1994.tb04369.x 8542838
13. Development and ageing of the articular cartilage of the rabbit knee joint: distribution of the fibrillar collagens. YS Bland DE Ashhurst, Anatomy and Embryology 1996 194 6 607 619 10.1007/BF00187473 8957536
14. Changes in the content of the fibrillar collagens and the expression of their mRNAs in the menisci of the rabbit knee joint during development and ageing. YS Bland DE Ashhurst, Histochemical Journal 1996 28 4 265 274 10.1007/BF02409014 8762058
15. The development of articular cartilage: I. The spatial and temporal patterns of collagen types. E Morrison M Ferguson M Bayliss C Archer, Journal of Anatomy 1996 189 Pt 1 9 22 8771392
16. Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. AK Williamson AC Chen K Masuda EJM Thonar RL Sah, Journal of Orthopaedic Research 2003 21 5 872 880 10.1016/S0736-0266(03)00030-5 12919876 (Pubitemid 37045566)
17. Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. J Rieppo M Hyttinen E Halmesmaki H Ruotsalainen A Vasara I Kiviranta J Jurvelin H Helminen, Osteoarthritis & Cartilage 2009 17 4 448 455 10.1016/j.joca.2008.09.004 18849174
18. The ultrastructure of mouse articular cartilage: collagen orientation and implications for tissue functionality. A polarised light and scanning electron microscope study and review. L Hughes C Archer Ia Gwynn, European Cells & Materials Journal 2005 9 68 84
19. Age matters: collagen birefringence of superficial articular cartilage is increased in young guinea-pigs but decreased in older animals after identical physiological type of joint loading. M Hyttinen J Arokoski J Parkkinen M Lammi T Lapveteläinen K Mauranen K Kirly M Tammi H Helminen, Osteoarthritis & Cartilage 2001 9 8 694 701 10.1053/joca.2001.0466 11795988
20. The influence of strenuous exercise on collagen characteristics of articular cartilage in Thoroughbreds age 2 years. P Brama J Tekoppele R Bank A Barneveld E Firth P Van Weeren, Equine Veterinary Journal 2000 32 6 551 554 10.2746/042516400777584613 11093631
21. Long-term cyclical in vivo loading increases cartilage proteoglycan content in a spatially specific manner: an infrared microspectroscopic imaging and polarized light microscopy study. E Saadat H Lan S Majumdar DM Rempel KB King, Arthritis Research & Therapy 2006 8 5 147 10.1186/ar2040 16956418
22. Aged bovine chondrocytes display a diminished capacity to produce a collagen-rich, mechanically functional cartilage extracellular matrix. N Tran-Khanh CD Hoemann MD McKee JE Henderson MD Buschmann, Journal of Orthopaedic Research 2005 23 6 1354 1362 10.1016/j.orthres.2005.05.009.1100230617 16048738
23. Modification of the composition of articular cartilage collagen fibrils with increasing age. A Vaughan-Thomas J Dudhia MT Bayliss KE Kadler VC Duance, Connective Tissue Research 2008 49 5 374 382 10.1080/03008200802325417 18991091
24. Structure-function relationships in enzymatically modified articular cartilage. J Rieppo J Töyräs MT Nieminen V Kovanen MM Hyttinen RK Korhonen JS Jurvelin HJ Helminen, Cells Tissues Organs 2003 175 3 121 132 10.1159/000074628 14663155
25. Articular cartilage in the knee joint of the African elephant, Loxodonta africana, Blumenbach 1797. GF Egger K Witter G Weissengruber G Forstenpointner, Journal of Morphology 2008 269 118 127 10.1002/jmor.10600 17972268
26. Study of altered mechanical properties of articular cartilage in relation to the collagen network. J Wu T Kirk, Advanced Materials Research 2008 41-42 9 14 10.4028/www.scientific.net/AMR.41-42.9
27. Role of cartilage collagen fibrils networks in knee joint biomechanics under compression. R Shirazi A Shirazi-Adl M Hurtig, Journal of Biomechanics 2008 41 16 3340 3348 10.1016/j.jbiomech.2008.09.033 19022449
28. Cartilage mechanical response under dynamic compression at physiological stress levels following collagenase digestion. S Park SB Nicoll RL Mauck GA Ateshian, Annals of Biomedical Engineering 2008 36 3 425 434 10.1007/s10439-007-9431-6 18193355
29. Importance of collagen orientation and depth-dependent fixed charge densities of cartilage om mechanical behavior of chondrocytes. RK Korhonen P Julkunen W Wilson W Herzog, Journal of Biomedical Engineering 2008 130 2 21003-1 21003-11
30. Collagen network primarily controls Poisson's ratio of bovine articular cartilage in compression. P Kiviranta J Rieppo RK Korhonen P Julkunen J Töyräs JS Jurvelin, Journal of Orthopaedic Research 2006 24 4 690 699 10.1002/jor.20107 16514661
31. Anisotropy of collagen fibre alignment in bovine cartilage: comparison of polarised light microscopy and spatially resolved diffusion-tensor measurements. Sd Visser J Bowden E Wentrup-Byrne L Rintoul T Bostrom J Pope K Momot, Osteoarthritis & Cartilage 2008 16 6 689 697 10.1016/j.joca.2007.09. 015 18023211
32. Strain-dependent modulation of ultrasound speed in articular cartilage under dynamic compression. P Lötjönen P Julkunen J Töyröas MJ Lammi JS Jurvelin HJ Nieminen, Ultrasound in Medicine and Biology 2009
33. Fluid pressure driven fibril reinforcement in creep and relaxation tests of articular cartilage. L Li R Korhonen J Iivarinen J Jurvelin W Herzog, Medical Engineering and Physics 2008 30 2 182 189 10.1016/j.medengphy.2007.03.001 17524700
34. On the anisotropy and inhomogeneity of permeability in articular cartilage. S Federico W Herzog, Biomechanics and Modeling in Mechanobiology 2008 7 5 367 378 10.1007/s10237-007-0091-0 17619089
35. Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Zweiter Teil: Der Aufbau des Gelenkknorpels in seinen Beziehungen zur Funktion. A Benninghoff, Zeitschrift für Zellforschung und Mikroskopische Anatomie 1925 2 783 862 10.1007/BF00583443
36. Quantitative description of collagen structure in the articular cartilage of the young and adult equine distal metacarpus. MC Van Turnhout MB Haazelager MA Gijsen H Schipper S Kranenbarg JL Van Leeuwen, Animal Biology 2008 58 4 353 370 10.1163/157075608X383674
37. Collagen arrangement in cartilages. NZ Zambrano GS Montes KM Shigihara EM Sanchez LC Junqueira, Acta Anatomica 1982 113 26 38 7113642
38. Maturation of collagen fibril network structure in tibial and femoral cartilage of rabbits. P Julkunen J Iivarinen P Brama J Arokoski J Jurvelin H Helminen, Osteoarthritis & Cartilage 2010 18 3 406 415 10.1016/j.joca.2009. 11.007 19941998
39. Biomechanical, biochemical and structural correlations in immature and mature rabbit articular cartilage. P Julkunen T Harjula J Iivarinen J Marjanen K Seppänen T Närhi J Arokoski MJ Lammi P Brama J Jurvelin H Helminen, Osteoarthritis & Cartilage 2009 17 12 1628 1638 10.1016/j.joca.2009.07.002 19615962
40. Fibril reinforced poroelastic model predicts specifically mechanical behavior of normal, proteoglycan depleted and collagen degraded articular cartilage. RK Korhonen MS Laasanen J Töyräs R Lappalainen HJ Helminen JS Jurvelin, Journal of Biomechanics 2003 36 9 1373 1379 10.1016/S0021-9290(03) 00069-1 12893046
41. Depth-dependent compressive equilibrium properties of articular cartilage explained by its composition. W Wilson J Huyghe C Van Donkelaar, Biomechanics and Modeling in Mechanobiology 2007 6 1-2 43 53 10.1007/s10237-006-0044-z 16710737
42. Three-dimensional fibril-reinforced finite element model of articular cartilage. L Li J Cheung W Herzog, Medical and Biological Engineering and Computing 2009 47 6 607 615 10.1007/s11517-009-0469-5 19266224
43. Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm. W Wilson N Driessen C Van Donkelaar K Ito, Osteoarthritis & Cartilage 2006 14 11 1196 1202 10.1016/j.joca.2006.05.006 16797194
44. The depth-dependent anisotropy of articular cartilage by Fourier-transform infrared imaging (FTIRI). Y Xia N Ramakrishnan A Bidthanapally, Osteoarthritis & Cartilage 2007 15 7 780 788 10.1016/j.joca.2007.01.007 17317225 (Pubitemid 46888155)
45. Detecting structural changes in early experimental osteoarthritis of tibial cartilage by microscopic magnetic resonance imaging and polarised light microscopy. H Alhadlaq Y Xia J Moody J Matyas, Annals of the Rheumatic Diseases 2004 63 6 709 717 10.1136/ard.2003.011783 15140779
46. Articular cartilage thickness and glycosaminoglycan distribution in the young canine knee joint after remobilization of the immobilized limb. I Kiviranta M Tammi J Jurvelin J Arokoski A Säämänen H Helminen, Journal of Orthopaedic Research 1994 12 2 161 167 10.1002/jor.1100120203 8164087
47. Articular cartilage thickness and glycosaminoglycan distribution in the canine knee joint after strenuous running exercise. I Kiviranta M Tammi J Jurvelin J Arokoski AM Säämänen HJ Helminen, Clinical Orthopaedics and Related Research 1992 283 302 308 1395265
48. Quantitative study of articular cartilage and subchondral bone remodeling in the knee joint of dogs after strenuous running training. R Oettmeier J Arokoski AJ Roth HJ Helminen M Tammi K Abendroth, Journal of Bone and Mineral Research 1992 7 Suppl 2 419 S424 10.1002/jbmr.5650071410 1485550
49. Joint congruence. A correlation of joint congruence and thickness of articular cartilage in dogs. WH Simon S Friedenberg S Richardson, Journal of Bone and Joint Surgery. American Volume 1973 55 8 1614 1620
50. Bewegungen des Kniegelenks nach einer neuen Methode am lebenden Menschen gemessen. W Braune O Fischer, Abhandlungen der Mathematisch-Physischen Klasse der Königlich-Sächsischen Gesellschaft der Wissenschaften, Leipzig, Hirzel S, 1891 17 75 150
51. Scale effects in animal joints. I. Articular cartilage thickness and compressive stress. W Simon, Arthritis and Rheumatism 1970 13 3 244 256 10.1002/art.1780130305 5423816
52. Puberty in the Sheep. DL Foster LM Jackson, Knobil and Neill's Physiology of Reproduction Elsevier Inc, Neill JD, 3 2006 2 2127 2176 full-text
53. The effect of skeletal maturity on the regenerative function of intrinsic ACL cells. AN Mastrangelo EM Magarian MP Palmer P Vavken MM Murray, Journal of Orthopaedic Research 2010 28 5 644 651 19890988
54. Genotype and age effects on sheep meat production 1. Production and growth. D Hopkins D Stanley L Martin A Gilmour, Australian Journal of Experimental Agriculture 2007 47 10 1119 1127 10.1071/EA06236 (Pubitemid 47429221)
55. Genotype and gender effects on sheep limb bone growth and maturation: selection for loin depth causes bone hypotrophy. M Cake M Boyce G Gardner D Hopkins D Pethick, Australian Journal of Experimental Agriculture 2007 47 10 1128 1136 10.1071/EA07058 (Pubitemid 47429230)
56. MRI assessment of cartilage ultrastructure. W Gründer, NMR in Biomedicine 2006 19 7 855 876 10.1002/nbm.1092 17075962
57. Effect of loading on the organization of the collagen fibril network in juvenile equine articular cartilage. P Brama J Holopainen P Van Weeren E Firth H Helminen M Hyttinen, Journal of Orthopaedic Research 2009 27 9 1226 1234 10.1002/jor.20866 19242977
58. Mechanobiology in the development, maintenance, and degeneration of articular cartilage. GS Beaupré SS Stevens DR Carter, Journal of Rehabilitation Research and Development 2000 37 2 145 151 10850820
59. Modelling cartilage mechanobiology. DR Carter M Wong, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 2003 358 1437 1461 1471 10.1098/rstb.2003.1346 (Pubitemid 37171658)
60. Pressure and shear differentially alter human articular chondrocyte metabolism: a review. RL Smith DR Carter DJ Schurman, Clinical Orthopaedics and Related Research 2004 427 Suppl 89 S95 15480081
61. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. A Maroudas, Nature 1976 260 5554 808 809 10.1038/260808a0 1264261
62. The increased swelling and instantaneous deformation of osteoarthritic cartilage is highly correlated with collagen degradation. RA Bank M Soudry A Maroudas J Mizrahi JM TeKoppele, Arthritis and Rheumatism 2000 43 10 2202 2210 10.1002/1529-0131(200010)43:10<2202::AID-ANR7>3.0.CO;2-E 11037879
63. The role of osmotic pressure and tension-compression nonlinearity in the frictional response of articular cartilage. GA Ateshian MA Soltz RL Mauck IM Basalo CT Hung WM Lai, Transport in Porous Media 2003 50 1-2 5 33 10.1023/A:1020618514874 (Pubitemid 36225141)
64. A chondral modeling theory revisited. MW Hamrick, Journal of Theoretical Biology 1999 201 3 201 208 10.1006/jtbi.1999.1025 10600363
65. Chondrogenesis, joint formation, and articular cartilage regeneration. I Onyekwelu MB Goldring C Hidaka, Journal of Cellular Biochemistry 2009 107 3 383 392 10.1002/jcb.22149 19343794
66. Absence of mechanical loading in utero influences bone mass and architecture but not innervation in MyoD-Myf5-deficient mice. C Gomez V David NM Peet L Vico C Chenu L Malaval TM Skerry, Journal of Anatomy 2007 210 3 259 271 10.1111/j.1469-7580.2007.00698.x 17331176
67. Modelling optical behaviour of birefringent biological tissues for evaluation of quantitative polarised light microscopy. MC Van Turnhout S Kranenbarg JL Van Leeuwen, Journal of Biomedical Optics 2009 14 5 054018-1-11 10.1117/1.3241986 19895120
68. New polarized light microscope with precision universal compensator. R Oldenbourg G Mei, Journal of Microscopy 1995 180 Pt 2 140 147 8537959
69. Polarization microscopy with the LC-microscope. R Oldenbourg, Live Cell Imaging: A Laboratory Manual Cold Spring Harbor Laboratory Press, Goldman RD, Spector DL, 2004 205 238
70. Techniques for fast and sensitive measurements of two-dimensional birefringence distributions. M Shribak R Oldenbourg, Applied Optics 2003 42 16 3009 3017 10.1364/AO.42.003009 12790452
71. GJ Upton B Fingleton, Spatial data analysis by example - Volume 2: Categorical and directional data Wiley series in probability and mathematical statistics, John Wiley and Sons 1989
72. Estimation in generalized linear models with random effects. R Schall, Biometrika 1991 78 4 719 727 10.1093/biomet/78.4.719
73. Approximate inference in generalized linear mixed models. N Breslow D Clayton, Journal of the American Statistical Association 1993 88 421 9 25 10.2307/2290687
74. A simple approach for the analysis of generalized linear mixed models. B Engel A Keen, Statistica Neerlandica 1994 48 1 22 10.1111/j.1467-9574.1994. tb01428.x
75. R Payne S Harding D Murray D Soutar D Baird A Glaser I Channing S Welham A Gilmour R Thompson R Webster, The Guide to GenStat Release 12. VSN International, Hemel Hempstead 2009
76. Small sample inference for fixed effects from restricted maximum likelihood. MG Kenward JH Roger, Biometrics 1997 53 3 983 997 10.2307/2533558 9333350