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BMC musculoskeletal disorders2008; 9; 149; doi: 10.1186/1471-2474-9-149

Differential gene expression associated with postnatal equine articular cartilage maturation.

Abstract: Articular cartilage undergoes an important maturation process from neonate to adult that is reflected by alterations in matrix protein organization and increased heterogeneity of chondrocyte morphology. In the horse, these changes are influenced by exercise during the first five months of postnatal life. Transcriptional profiling was used to evaluate changes in articular chondrocyte gene expression during postnatal growth and development. Methods: Total RNA was isolated from the articular cartilage of neonatal (0-10 days) and adult (4-5 years) horses, subjected to one round of linear RNA amplification, and then applied to a 9,367-element equine-specific cDNA microarray. Comparisons were made with a dye-swap experimental design. Microarray results for selected genes (COL2A1, COMP, P4HA1, TGFB1, TGFBR3, TNC) were validated by quantitative polymerase chain reaction (qPCR). Results: Fifty-six probe sets, which represent 45 gene products, were up-regulated (p < 0.01) in chondrocytes of neonatal articular cartilage relative to chondrocytes of adult articular cartilage. Conversely, 586 probe sets, which represent 499 gene products, were up-regulated (p < 0.01) in chondrocytes of adult articular cartilage relative to chondrocytes of neonatal articular cartilage. Collagens, matrix-modifying enzymes, and provisional matrix non-collagenous proteins were expressed at higher levels in the articular cartilage of newborn foals. Those genes with increased mRNA abundance in adult chondrocytes included leucine-rich small proteoglycans, matrix assembly, and cartilage maintenance proteins. Conclusions: Differential expression of genes encoding matrix proteins and matrix-modifying enzymes between neonates and adults reflect a cellular maturation process in articular chondrocytes. Up-regulated transcripts in neonatal cartilage are consistent with growth and expansion of the articular surface. Expression patterns in mature articular cartilage indicate a transition from growth to homeostasis, and tissue function related to withstanding shear and weight-bearing stresses.
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Publication Date: 2008-11-05 PubMed ID: 18986532PubMed Central: PMC2585085DOI: 10.1186/1471-2474-9-149Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study analyzes the changes in gene expression of articular chondrocyte, a cell found in the cartilage, during the postnatal growth and development in horses. The research indicates a transformation from growth to homeostasis in adult horse’s cartilage cells, reflecting a maturity process.

Methodology

  • The researchers isolated total RNA from the articular cartilage of neonates (0-10 days old) and adult horses (4-5 years old). The process was subjected to a round of linear RNA amplification.
  • The amplified data was applied to a 9,367-element equine-specific cDNA microarray. This is a biochip that permits multiple genetic sequences to be detected at once.
  • The comparisons were made with a dye-swap experimental design, a technique that controls for dye bias in microarray experiments.
  • To validate the microarray results, selected genes like COL2A1, COMP, P4HA1, TGFB1, TGFBR3, TNC were evaluated by a quantitative polymerase chain reaction (qPCR), a common technique used to measure the level of specific genetic sequences.

Results

  • The study observed 56 probe sets (representing 45 gene products) were up-regulated (p < 0.01) in the chondrocytes of neonatal articular cartilage in comparison with adult articular cartilage.
  • Contrarily, 586 probe sets (representing 499 gene products) were up-regulated (p < 0.01) in the chondrocytes of adult articular cartilage.
  • Genes such as collagens, matrix-modifying enzymes, and provisional matrix non-collagenous proteins were expressed at higher levels in the cartilage of newborn foals, suggesting growth and expansion of the articular surface.
  • Genes indicating leucine-rich small proteoglycans, matrix assembly, and cartilage maintenance proteins had increased mRNA abundance in adult chondrocytes.

Conclusions

  • The differential expression of genes encoding matrix proteins and matrix-modifying enzymes between neonates and adults shows a maturation process in the articular chondrocytes.
  • Expression patterns transitioning from growth to homeostasis in mature articular cartilage suggests the tissue’s function related to enduring shear and weight-bearing stresses.

Cite This Article

APA
Mienaltowski MJ, Huang L, Stromberg AJ, MacLeod JN. (2008). Differential gene expression associated with postnatal equine articular cartilage maturation. BMC Musculoskelet Disord, 9, 149. https://doi.org/10.1186/1471-2474-9-149

Publication

BMC musculoskeletal disorders
ISSN: 1471-2474
NlmUniqueID: 100968565
Country: England
Language: English
Volume: 9
Pages: 149

Researcher Affiliations

Mienaltowski, Michael J
  • University of Kentucky, Department of Veterinary Science, M.H. Gluck Equine Research Center, Lexington, KY 40546-0099, USA. M.Mski@uky.edu
Huang, Liping
    Stromberg, Arnold J
      MacLeod, James N

        MeSH Terms

        • Aging / genetics
        • Aging / metabolism
        • Animals
        • Cartilage, Articular / growth & development
        • Cartilage, Articular / metabolism
        • Chondrocytes / metabolism
        • Collagen Type II / genetics
        • Collagen Type II / metabolism
        • Extracellular Matrix Proteins / genetics
        • Extracellular Matrix Proteins / metabolism
        • Gene Expression Profiling
        • Gene Expression Regulation, Developmental / physiology
        • Growth / genetics
        • Growth / physiology
        • Homeostasis / genetics
        • Homeostasis / physiology
        • Horses / genetics
        • Horses / growth & development
        • Horses / metabolism
        • Intercellular Signaling Peptides and Proteins / genetics
        • Intercellular Signaling Peptides and Proteins / metabolism
        • Proteoglycans / genetics
        • Proteoglycans / metabolism
        • RNA, Messenger / metabolism
        • Receptors, Transforming Growth Factor beta / genetics
        • Receptors, Transforming Growth Factor beta / metabolism
        • Tenascin / genetics
        • Tenascin / metabolism
        • Transforming Growth Factor beta1 / genetics
        • Transforming Growth Factor beta1 / metabolism
        • Up-Regulation / physiology
        • Weight-Bearing / physiology

        Grant Funding

        • P20 RR016481 / NCRR NIH HHS
        • P20 RR16481 / NCRR NIH HHS

        References

        This article includes 61 references
        1. Brama PA, TeKoppele JM, Bank RA, van Weeren PR, Barneveld A. Influence of site and age on biochemical characteristics of the collagen network of equine articular cartilage.. Am J Vet Res 1999 Mar;60(3):341-5.
          pubmed: 10188817
        2. Brama PA, TeKoppele JM, Bank RA, Barneveld A, van Weeren PR. Development of biochemical heterogeneity of articular cartilage: influences of age and exercise.. Equine Vet J 2002 May;34(3):265-9.
          doi: 10.2746/042516402776186146pubmed: 12108744google scholar: lookup
        3. Brommer H, Brama PA, Laasanen MS, Helminen HJ, van Weeren PR, Jurvelin JS. Functional adaptation of articular cartilage from birth to maturity under the influence of loading: a biomechanical analysis.. Equine Vet J 2005 Mar;37(2):148-54.
          doi: 10.2746/0425164054223769pubmed: 15779628google scholar: lookup
        4. Hall BK. Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. San Diego, CA: Elsevier Academic Press; 2005.
        5. Hunziker EB, Kapfinger E, Geiss J. The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development.. Osteoarthritis Cartilage 2007 Apr;15(4):403-13.
          doi: 10.1016/j.joca.2006.09.010pubmed: 17098451google scholar: lookup
        6. Jadin KD, Bae WC, Schumacher BL, Sah RL. Three-dimensional (3-D) imaging of chondrocytes in articular cartilage: growth-associated changes in cell organization.. Biomaterials 2007 Jan;28(2):230-9.
          doi: 10.1016/j.biomaterials.2006.08.053pmc: PMC2464614pubmed: 16999994google scholar: lookup
        7. Brama PA, Tekoppele JM, Bank RA, Barneveld A, van Weeren PR. Functional adaptation of equine articular cartilage: the formation of regional biochemical characteristics up to age one year.. Equine Vet J 2000 May;32(3):217-21.
          doi: 10.2746/042516400776563626pubmed: 10836476google scholar: lookup
        8. Brama PA, Tekoppele JM, Bank RA, Karssenberg D, Barneveld A, van Weeren PR. Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint.. Equine Vet J 2000 Jan;32(1):19-26.
          doi: 10.2746/042516400777612062pubmed: 10661380google scholar: lookup
        9. van den Hoogen BM, van den Lest CH, van Weeren PR, van Golde LM, Barneveld A. Effect of exercise on the proteoglycan metabolism of articular cartilage in growing foals.. Equine Vet J Suppl 1999 Nov;(31):62-6.
          pubmed: 10999662doi: 10.1111/j.2042-3306.1999.tb05315.xgoogle scholar: lookup
        10. Sasano Y, Furusawa M, Ohtani H, Mizoguchi I, Takahashi I, Kagayama M. Chondrocytes synthesize type I collagen and accumulate the protein in the matrix during development of rat tibial articular cartilage.. Anat Embryol (Berl) 1996 Sep;194(3):247-52.
          pubmed: 8849671doi: 10.1007/bf00187135google scholar: lookup
        11. Bland YS, Ashhurst DE. Development and ageing of the articular cartilage of the rabbit knee joint: distribution of the fibrillar collagens.. Anat Embryol (Berl) 1996 Dec;194(6):607-19.
          pubmed: 8957536doi: 10.1007/bf00187473google scholar: lookup
        12. Bank RA, Bayliss MT, Lafeber FP, Maroudas A, Tekoppele JM. Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage. The age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage.. Biochem J 1998 Feb 15;330 ( Pt 1)(Pt 1):345-51.
          pmc: PMC1219146pubmed: 9461529doi: 10.1042/bj3300345google scholar: lookup
        13. Helminen HJ, Hyttinen MM, Lammi MJ, Arokoski JP, Lapveteläinen T, Jurvelin J, Kiviranta I, Tammi MI. 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.. J Bone Miner Metab 2000;18(5):245-57.
          doi: 10.1007/PL00010638pubmed: 10959613google scholar: lookup
        14. MacLeod JN, Burton-Wurster N, Gu DN, Lust G. Fibronectin mRNA splice variant in articular cartilage lacks bases encoding the V, III-15, and I-10 protein segments.. J Biol Chem 1996 Aug 2;271(31):18954-60.
          doi: 10.1074/jbc.271.18.10654pubmed: 8702559google scholar: lookup
        15. MacLeod JN, Fubini SL, Gu DN, Tetreault JW, Todhunter RJ. Effect of synovitis and corticosteroids on transcription of cartilage matrix proteins.. Am J Vet Res 1998 Aug;59(8):1021-6.
          pubmed: 9706207
        16. Chomczynski P, Mackey K. Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources.. Biotechniques 1995 Dec;19(6):942-5.
          pubmed: 8747660
        17. MacLeod JN. Equine articular cartilage microarray (abstract). Plant & Animal Genome Conference XIII San Diego, CA, USA; 2005.
        18. Coleman SJ, Gong G, Gaile DP, Chowdhary BP, Bailey E, Liu L, MacLeod JN. Evaluation of Compass as a comparative mapping tool for ESTs using horse radiation hybrid maps.. Anim Genet 2007 Jun;38(3):294-302.
          doi: 10.1111/j.1365-2052.2007.01603.xpubmed: 17539974google scholar: lookup
        19. Band MR, Olmstead C, Everts RE, Liu ZL, Lewin HA. A 3800 gene microarray for cattle functional genomics: comparison of gene expression in spleen, placenta, and brain.. Anim Biotechnol 2002 May;13(1):163-72.
          doi: 10.1081/ABIO-120005779pubmed: 12212940google scholar: lookup
        20. Eberwine J, Yeh H, Miyashiro K, Cao Y, Nair S, Finnell R, Zettel M, Coleman P. Analysis of gene expression in single live neurons.. Proc Natl Acad Sci U S A 1992 Apr 1;89(7):3010-4.
          doi: 10.1073/pnas.89.7.3010pmc: PMC48793pubmed: 1557406google scholar: lookup
        21. Feldman AL, Costouros NG, Wang E, Qian M, Marincola FM, Alexander HR, Libutti SK. Advantages of mRNA amplification for microarray analysis.. Biotechniques 2002 Oct;33(4):906-12, 914.
          pubmed: 12398200doi: 10.2144/02334mt04google scholar: lookup
        22. Rosenzweig BA, Pine PS, Domon OE, Morris SM, Chen JJ, Sistare FD. Dye bias correction in dual-labeled cDNA microarray gene expression measurements.. Environ Health Perspect 2004 Mar;112(4):480-7.
          pmc: PMC1241902pubmed: 15033598doi: 10.1289/ehp.6694google scholar: lookup
        23. Coleman SJ, Clinton R, MacLeod JN. Construction of a master gene list for a 9322 feature equine cDNA microarray (P587). Abstracts of Plant & Animal Genome Conference XV 2007.
        24. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
          pubmed: 2231712doi: 10.1016/s0022-2836(05)80360-2google scholar: lookup
        25. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery.. Genome Biol 2003;4(5):P3.
          doi: 10.1186/gb-2003-4-9-r60pubmed: 12734009google scholar: lookup
        26. Maglott D, Ostell J, Pruitt KD, Tatusova T. Entrez Gene: gene-centered information at NCBI.. Nucleic Acids Res 2005 Jan 1;33(Database issue):D54-8.
          doi: 10.1093/nar/gki031pmc: PMC539985pubmed: 15608257google scholar: lookup
        27. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE.. Genome Biol 2003;4(10):R70.
          doi: 10.1186/gb-2003-4-6-p4pmc: PMC328459pubmed: 14519205google scholar: lookup
        28. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Edgar R. NCBI GEO: mining tens of millions of expression profiles--database and tools update.. Nucleic Acids Res 2007 Jan;35(Database issue):D760-5.
          doi: 10.1093/nar/gkl887pmc: PMC1669752pubmed: 17099226google scholar: lookup
        29. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.. Neurosci Lett 2003 Mar 13;339(1):62-6.
          doi: 10.1016/S0304-3940(02)01423-4pubmed: 12618301google scholar: lookup
        30. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H. Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula.. J Mol Med (Berl) 2006 Nov;84(11):901-10.
          doi: 10.1007/s00109-006-0097-6pubmed: 16972087google scholar: lookup
        31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.. Genome Biol 2002 Jun 18;3(7):RESEARCH0034.
          doi: 10.1186/gb-2002-3-7-research0034pmc: PMC126239pubmed: 12184808google scholar: lookup
        32. Myllyharju J, Kivirikko KI. Collagens, modifying enzymes and their mutations in humans, flies and worms.. Trends Genet 2004 Jan;20(1):33-43.
          doi: 10.1016/j.tig.2003.11.004pubmed: 14698617google scholar: lookup
        33. Lucero HA, Kagan HM. Lysyl oxidase: an oxidative enzyme and effector of cell function.. Cell Mol Life Sci 2006 Oct;63(19-20):2304-16.
          doi: 10.1007/s00018-006-6149-9pubmed: 16909208google scholar: lookup
        34. Asanbaeva A, Masuda K, Thonar EJ, Klisch SM, Sah RL. Cartilage growth and remodeling: modulation of balance between proteoglycan and collagen network in vitro with beta-aminopropionitrile.. Osteoarthritis Cartilage 2008 Jan;16(1):1-11.
          doi: 10.1016/j.joca.2007.05.019pubmed: 17631390google scholar: lookup
        35. Chiquet-Ehrismann R, Tucker RP. Connective tissues: signalling by tenascins.. Int J Biochem Cell Biol 2004 Jun;36(6):1085-9.
          doi: 10.1016/j.biocel.2004.01.007pubmed: 15094123google scholar: lookup
        36. Hsia HC, Schwarzbauer JE. Meet the tenascins: multifunctional and mysterious.. J Biol Chem 2005 Jul 22;280(29):26641-4.
          pubmed: 15932878doi: 10.1074/jbc.r500005200google scholar: lookup
        37. Mackie EJ, Tucker RP. The tenascin-C knockout revisited.. J Cell Sci 1999 Nov;112 ( Pt 22):3847-53.
          pubmed: 10547346doi: 10.1242/jcs.112.22.3847google scholar: lookup
        38. Pacifici M, Iwamoto M, Golden EB, Leatherman JL, Lee YS, Chuong CM. Tenascin is associated with articular cartilage development.. Dev Dyn 1993 Oct;198(2):123-34.
          pubmed: 7508293doi: 10.1002/aja.1001980206google scholar: lookup
        39. Pas J, Wyszko E, Rolle K, Rychlewski L, Nowak S, Zukiel R, Barciszewski J. Analysis of structure and function of tenascin-C.. Int J Biochem Cell Biol 2006;38(9):1594-602.
          doi: 10.1016/j.biocel.2006.03.017pubmed: 16698307google scholar: lookup
        40. Metzger M, Bartsch S, Bartsch U, Bock J, Schachner M, Braun K. Regional and cellular distribution of the extracellular matrix protein tenascin-C in the chick forebrain and its role in neonatal learning.. Neuroscience 2006 Sep 15;141(4):1709-19.
          doi: 10.1016/j.neuroscience.2006.05.025pubmed: 16797128google scholar: lookup
        41. Mackie EJ, Ramsey S. Expression of tenascin in joint-associated tissues during development and postnatal growth.. J Anat 1996 Feb;188 ( Pt 1)(Pt 1):157-65.
          pmc: PMC1167643pubmed: 8655402
        42. Carlin B, Jaffe R, Bender B, Chung AE. Entactin, a novel basal lamina-associated sulfated glycoprotein.. J Biol Chem 1981 May 25;256(10):5209-14.
          pubmed: 6262321
        43. Kimura N, Toyoshima T, Kojima T, Shimane M. Entactin-2: a new member of basement membrane protein with high homology to entactin/nidogen.. Exp Cell Res 1998 May 25;241(1):36-45.
          doi: 10.1006/excr.1998.4016pubmed: 9633511google scholar: lookup
        44. Kohfeldt E, Sasaki T, Göhring W, Timpl R. Nidogen-2: a new basement membrane protein with diverse binding properties.. J Mol Biol 1998 Sep 11;282(1):99-109.
          doi: 10.1006/jmbi.1998.2004pubmed: 9733643google scholar: lookup
        45. Ekblom P, Ekblom M, Fecker L, Klein G, Zhang HY, Kadoya Y, Chu ML, Mayer U, Timpl R. Role of mesenchymal nidogen for epithelial morphogenesis in vitro.. Development 1994 Jul;120(7):2003-14.
          pubmed: 7925005doi: 10.1242/dev.120.7.2003google scholar: lookup
        46. Böse K, Nischt R, Page A, Bader BL, Paulsson M, Smyth N. Loss of nidogen-1 and -2 results in syndactyly and changes in limb development.. J Biol Chem 2006 Dec 22;281(51):39620-9.
          doi: 10.1074/jbc.M607886200pubmed: 17023412google scholar: lookup
        47. Nischt R, Schmidt C, Mirancea N, Baranowsky A, Mokkapati S, Smyth N, Woenne EC, Stark HJ, Boukamp P, Breitkreutz D. Lack of nidogen-1 and -2 prevents basement membrane assembly in skin-organotypic coculture.. J Invest Dermatol 2007 Mar;127(3):545-54.
          doi: 10.1038/sj.jid.5700562pubmed: 17008882google scholar: lookup
        48. Erickson AC, Couchman JR. Still more complexity in mammalian basement membranes.. J Histochem Cytochem 2000 Oct;48(10):1291-306.
          pubmed: 10990484doi: 10.1177/002215540004801001google scholar: lookup
        49. Lorenzo P, Bayliss MT, Heinegård D. A novel cartilage protein (CILP) present in the mid-zone of human articular cartilage increases with age.. J Biol Chem 1998 Sep 4;273(36):23463-8.
          doi: 10.1074/jbc.273.36.23463pubmed: 9722583google scholar: lookup
        50. Johnson K, Farley D, Hu SI, Terkeltaub R. One of two chondrocyte-expressed isoforms of cartilage intermediate-layer protein functions as an insulin-like growth factor 1 antagonist.. Arthritis Rheum 2003 May;48(5):1302-14.
          doi: 10.1002/art.10927pubmed: 12746903google scholar: lookup
        51. Salminen H, Perälä M, Lorenzo P, Saxne T, Heinegård D, Säämänen AM, Vuorio E. Up-regulation of cartilage oligomeric matrix protein at the onset of articular cartilage degeneration in a transgenic mouse model of osteoarthritis.. Arthritis Rheum 2000 Aug;43(8):1742-8.
          doi: 10.1002/1529-0131(200008)43:8<1742::AID-ANR10>3.0.CO;2-Upubmed: 10943864google scholar: lookup
        52. Koelling S, Clauditz TS, Kaste M, Miosge N. Cartilage oligomeric matrix protein is involved in human limb development and in the pathogenesis of osteoarthritis.. Arthritis Res Ther 2006;8(3):R56.
          doi: 10.1186/ar1922pmc: PMC1526624pubmed: 16542502google scholar: lookup
        53. Giannoni P, Siegrist M, Hunziker EB, Wong M. The mechanosensitivity of cartilage oligomeric matrix protein (COMP).. Biorheology 2003;40(1-3):101-9.
          pubmed: 12454393
        54. Burton-Wurster N, Borden C, Lust G, Macleod JN. Expression of the (V+C)- fibronectin isoform is tightly linked to the presence of a cartilaginous matrix.. Matrix Biol 1998 Jul;17(3):193-203.
          doi: 10.1016/S0945-053X(98)90058-0pubmed: 9707342google scholar: lookup
        55. Kawakami Y, Rodriguez-León J, Izpisúa Belmonte JC. The role of TGFbetas and Sox9 during limb chondrogenesis.. Curr Opin Cell Biol 2006 Dec;18(6):723-9.
          doi: 10.1016/j.ceb.2006.10.007pubmed: 17049221google scholar: lookup
        56. Davies LC, Blain EJ, Gilbert SJ, Caterson B, Duance VC. The potential of IGF-1 and TGFbeta1 for promoting "adult" articular cartilage repair: an in vitro study.. Tissue Eng Part A 2008 Jul;14(7):1251-61.
          doi: 10.1089/ten.tea.2007.0211pubmed: 18399732google scholar: lookup
        57. Serra R, Johnson M, Filvaroff EH, LaBorde J, Sheehan DM, Derynck R, Moses HL. Expression of a truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis.. J Cell Biol 1997 Oct 20;139(2):541-52.
          doi: 10.1083/jcb.139.2.541pmc: PMC2139797pubmed: 9334355google scholar: lookup
        58. Rountree RB, Schoor M, Chen H, Marks ME, Harley V, Mishina Y, Kingsley DM. BMP receptor signaling is required for postnatal maintenance of articular cartilage.. PLoS Biol 2004 Nov;2(11):e355.
          doi: 10.1371/journal.pbio.0020355pmc: PMC523229pubmed: 15492776google scholar: lookup
        59. Hildebrand A, Romarís M, Rasmussen LM, Heinegård D, Twardzik DR, Border WA, Ruoslahti E. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta.. Biochem J 1994 Sep 1;302 ( Pt 2)(Pt 2):527-34.
          pmc: PMC1137259pubmed: 8093006doi: 10.1042/bj3020527google scholar: lookup
        60. Schneiderman R, Rosenberg N, Hiss J, Lee P, Liu F, Hintz RL, Maroudas A. Concentration and size distribution of insulin-like growth factor-I in human normal and osteoarthritic synovial fluid and cartilage.. Arch Biochem Biophys 1995 Dec 1;324(1):173-88.
          doi: 10.1006/abbi.1995.9913pubmed: 7503553google scholar: lookup
        61. Dik KJ, Enzerink E, van Weeren PR. Radiographic development of osteochondral abnormalities, in the hock and stifle of Dutch Warmblood foals, from age 1 to 11 months.. Equine Vet J Suppl 1999 Nov;(31):9-15.
          pubmed: 10999655doi: 10.1111/j.2042-3306.1999.tb05308.xgoogle scholar: lookup

        Citations

        This article has been cited 17 times.
        1. Degen RM, Firth A, Sehmbi H, Martindale A, Wanlin S, Chen C, Marsh JD, Willits K, Bryant D. Multimodal analgesia did not improve post-operative pain scores, reduce opioid consumption or reduce length of stay following hip arthroscopy. Knee Surg Sports Traumatol Arthrosc 2023 Sep;31(9):4016-4026.
          doi: 10.1007/s00167-023-07445-5pubmed: 37170015google scholar: lookup
        2. López-Jiménez C, Chiu LLY, Waldman SD, Guilak F, Koch TG. TRPV4 activation enhances compressive properties and glycosaminoglycan deposition of equine neocartilage sheets. Osteoarthr Cartil Open 2022 Jun;4(2):100263.
          doi: 10.1016/j.ocarto.2022.100263pubmed: 36475280google scholar: lookup
        3. Bagge J, Berg LC, Janes J, MacLeod JN. Donor age effects on in vitro chondrogenic and osteogenic differentiation performance of equine bone marrow- and adipose tissue-derived mesenchymal stromal cells. BMC Vet Res 2022 Nov 3;18(1):388.
          doi: 10.1186/s12917-022-03475-2pubmed: 36329434google scholar: lookup
        4. Mok CH, MacLeod JN. Kinetics of Gene Expression Changes in Equine Fetal Interzone and Anlagen Cells Over 14 Days of Induced Chondrogenesis. Front Vet Sci 2021;8:722324.
          doi: 10.3389/fvets.2021.722324pubmed: 34434986google scholar: lookup
        5. Kwon H, Brown WE, O'Leary SA, Hu JC, Athanasiou KA. Rejuvenation of extensively passaged human chondrocytes to engineer functional articular cartilage. Biofabrication 2021 Apr 2;13(3).
          doi: 10.1088/1758-5090/abd9d9pubmed: 33418542google scholar: lookup
        6. Bagge J, MacLeod JN, Berg LC. Cellular Proliferation of Equine Bone Marrow- and Adipose Tissue-Derived Mesenchymal Stem Cells Decline With Increasing Donor Age. Front Vet Sci 2020;7:602403.
          doi: 10.3389/fvets.2020.602403pubmed: 33363241google scholar: lookup
        7. Pechanec MY, Boyd TN, Baar K, Mienaltowski MJ. Adding exogenous biglycan or decorin improves tendon formation for equine peritenon and tendon proper cells in vitro. BMC Musculoskelet Disord 2020 Sep 23;21(1):627.
          doi: 10.1186/s12891-020-03650-2pubmed: 32967653google scholar: lookup
        8. Gruber BL, Mienaltowski MJ, MacLeod JN, Schittny J, Kasper S, Flück M. Tenascin-C expression controls the maturation of articular cartilage in mice. BMC Res Notes 2020 Feb 17;13(1):78.
          doi: 10.1186/s13104-020-4906-8pubmed: 32066496google scholar: lookup
        9. Thampi P, Liu J, Zeng Z, MacLeod JN. Changes in the appendicular skeleton during metamorphosis in the axolotl salamander (Ambystoma mexicanum). J Anat 2018 Oct;233(4):468-477.
          doi: 10.1111/joa.12846pubmed: 29992565google scholar: lookup
        10. Decker RS. Articular cartilage and joint development from embryogenesis to adulthood. Semin Cell Dev Biol 2017 Feb;62:50-56.
          doi: 10.1016/j.semcdb.2016.10.005pubmed: 27771363google scholar: lookup
        11. Decker RS, Koyama E, Pacifici M. Articular Cartilage: Structural and Developmental Intricacies and Questions. Curr Osteoporos Rep 2015 Dec;13(6):407-14.
          doi: 10.1007/s11914-015-0290-zpubmed: 26408155google scholar: lookup
        12. Peffers M, Liu X, Clegg P. Transcriptomic signatures in cartilage ageing. Arthritis Res Ther 2013 Aug 23;15(4):R98.
          doi: 10.1186/ar4278pubmed: 23971731google scholar: lookup
        13. Xue X, Zheng Q, Wu H, Zou L, Li P. Different responses to mechanical injury in neonatal and adult ovine articular cartilage. Biomed Eng Online 2013 Jun 17;12:53.
          doi: 10.1186/1475-925X-12-53pubmed: 23773399google scholar: lookup
        14. Sun M, Chen S, Adams SM, Florer JB, Liu H, Kao WW, Wenstrup RJ, Birk DE. Collagen V is a dominant regulator of collagen fibrillogenesis: dysfunctional regulation of structure and function in a corneal-stroma-specific Col5a1-null mouse model. J Cell Sci 2011 Dec 1;124(Pt 23):4096-105.
          doi: 10.1242/jcs.091363pubmed: 22159420google scholar: lookup
        15. Mienaltowski MJ, Huang L, Frisbie DD, McIlwraith CW, Stromberg AJ, Bathke AC, Macleod JN. Transcriptional profiling differences for articular cartilage and repair tissue in equine joint surface lesions. BMC Med Genomics 2009 Sep 14;2:60.
          doi: 10.1186/1755-8794-2-60pubmed: 19751507google scholar: lookup
        16. Guan L, Feng L, Wang C, Xie Y. FGFRL1: Structure, Molecular Function, and Involvement in Human Disease. Curr Issues Mol Biol 2025 Apr 17;47(4).
          doi: 10.3390/cimb47040286pubmed: 40699684google scholar: lookup
        17. Hammer FA, Hölmich P, Nehlin JO, Vomstein K, Blønd L, Hölmich LR, Barfod KW, Bagge J. Microfragmented abdominal adipose tissue-derived stem cells from knee osteoarthritis patients aged 29-65 years demonstrate in vitro stemness and low levels of cellular senescence. J Exp Orthop 2024 Jul;11(3):e12056.
          doi: 10.1002/jeo2.12056pubmed: 38911188google scholar: lookup
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