FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Matrix Biol / Adult equine bone marrow stromal cells produce a cartilage-l...
Matrix biology : journal of the International Society for Matrix Biology2010; 29(5); 427-438; doi: 10.1016/j.matbio.2010.02.003

Adult equine bone marrow stromal cells produce a cartilage-like ECM mechanically superior to animal-matched adult chondrocytes.

Abstract: Our objective was to evaluate the age-dependent mechanical phenotype of bone marrow stromal cell- (BMSC-) and chondrocyte-produced cartilage-like neo-tissue and to elucidate the matrix-associated mechanisms which generate this phenotype. Cells from both immature (2-4 month-old foals) and skeletally-mature (2-5 year-old adults) mixed-breed horses were isolated from animal-matched bone marrow and cartilage tissue, encapsulated in self-assembling-peptide hydrogels, and cultured with and without TGF-beta1 supplementation. BMSCs and chondrocytes from both donor ages were encapsulated with high viability. BMSCs from both ages produced neo-tissue with higher mechanical stiffness than that produced by either young or adult chondrocytes. Young, but not adult, chondrocytes proliferated in response to TGF-beta1 while BMSCs from both age groups proliferated with TGF-beta1. Young chondrocytes stimulated by TGF-beta1 accumulated ECM with 10-fold higher sulfated-glycosaminoglycan content than adult chondrocytes and 2-3-fold higher than BMSCs of either age. The opposite trend was observed for hydroxyproline content, with BMSCs accumulating 2-3-fold more than chondrocytes, independent of age. Size-exclusion chromatography of extracted proteoglycans showed that an aggrecan-like peak was the predominant sulfated proteoglycan for all cell types. Direct measurement of aggrecan core protein length and chondroitin sulfate chain length by single molecule atomic force microscopy imaging revealed that, independent of age, BMSCs produced longer core protein and longer chondroitin sulfate chains, and fewer short core protein molecules than chondrocytes, suggesting that the BMSC-produced aggrecan has a phenotype more characteristic of young tissue than chondrocyte-produced aggrecan. Aggrecan ultrastructure, ECM composition, and cellular proliferation combine to suggest a mechanism by which BMSCs produce a superior cartilage-like neo-tissue than either young or adult chondrocytes.
Copyright (c) 2010 Elsevier B.V. All rights reserved.
Get Full Text
Publication Date: 2010-02-12 PubMed ID: 20153827PubMed Central: PMC2894996DOI: 10.1016/j.matbio.2010.02.003Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

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.

This study evaluates how the mechanical properties of cartilage-like neo-tissue produced by bone marrow stromal cells (BMSCs) and chondrocytes differ according to age. The results indicated that BMSCs from all ages produced neo-tissue with better mechanical strength compared to either young or adult chondrocytes.

Research objectives and methodology

  • The objective of this research was to understand the influence of age on the mechanical phenotype of cartilage-like neo-tissue produced by BMSCs and chondrocytes. Relatedly, the researchers sought to understand the matrix-related mechanisms that create these phenotypes.
  • Cells from young (2-4 month-old foals) and mature (2-5 year-old adults) horses were acquired from animal-matched bone marrow and cartilage tissue. They were placed in self-assembling-peptide hydrogels and cultivated with and without TGF-beta1 supplementation.

Findings

  • There was high viability of encapsulation for BMSCs and chondrocytes from both donor age groups.
  • BMSCs from both young and adult horses produced neo-tissue with better mechanical stiffness than that produced by chondrocytes of either age.
  • The reaction to TGF-beta1 differed by age. Only the young chondrocytes proliferated in response, while BMSCs from both age groups showed proliferation with TGF-beta1.
  • Young chondrocytes stimulated by TGF-beta1 accumulated extracellular matrix (ECM) with a greater sulfated-glycosaminoglycan content than adult chondrocytes and 2-3 times more than BMSCs of both ages.
  • The opposite pattern was evident for the hydroxyproline content, with BMSCs accumulating 2-3 times more than chondrocytes. This occurred regardless of age.

Aggrecan production and potential implications

  • Size-exclusion chromatography of extracted proteoglycans indicated an aggrecan-like peak was the dominant sulfated proteoglycan for all cell types.
  • Direct evaluation of aggrecan core protein length and chondroitin sulfate chain length by single molecule atomic force microscopy imaging showed that, irrespective of age, BMSCs made longer core protein and chondroitin sulfate chains, and fewer short core protein molecules than chondrocytes.
  • This suggests that the BMSC-produced aggrecan has a phenotype more characteristic of young tissue, compared to the aggrecan produced by chondrocytes. The structure of aggrecan, ECM composition, and cellular proliferation imply a mechanism by which BMSCs produce a better cartilage-like neo-tissue than chondrocytes, regardless of their age.

Cite This Article

APA
Kopesky PW, Lee HY, Vanderploeg EJ, Kisiday JD, Frisbie DD, Plaas AH, Ortiz C, Grodzinsky AJ. (2010). Adult equine bone marrow stromal cells produce a cartilage-like ECM mechanically superior to animal-matched adult chondrocytes. Matrix Biol, 29(5), 427-438. https://doi.org/10.1016/j.matbio.2010.02.003

Publication

Matrix biology : journal of the International Society for Matrix Biology
ISSN: 1569-1802
NlmUniqueID: 9432592
Country: Netherlands
Language: English
Volume: 29
Issue: 5
Pages: 427-438

Researcher Affiliations

Kopesky, P W
  • Department of Biological Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
Lee, H-Y
    Vanderploeg, E J
      Kisiday, J D
        Frisbie, D D
          Plaas, A H K
            Ortiz, C
              Grodzinsky, A J

                MeSH Terms

                • Aggrecans / biosynthesis
                • Animals
                • Bone Marrow Cells / cytology
                • Bone Marrow Cells / physiology
                • Cartilage / physiology
                • Cartilage / ultrastructure
                • Cell Survival / physiology
                • Chondrocytes / cytology
                • Chondrocytes / physiology
                • Chromatography, Gel
                • Extracellular Matrix / physiology
                • Extracellular Matrix / ultrastructure
                • Horses / physiology
                • Hydrogels / pharmacology
                • Hydroxyproline / physiology
                • Male
                • Microscopy, Atomic Force
                • Stress, Mechanical
                • Tissue Engineering / methods
                • Transforming Growth Factor beta / pharmacology

                Grant Funding

                • R01 AR033236 / NIAMS NIH HHS
                • R01 AR033236-26 / NIAMS NIH HHS
                • R37 AR033236 / NIAMS NIH HHS
                • R01 EB003805 / NIBIB NIH HHS
                • EB003805 / NIBIB NIH HHS
                • R01 EB003805-05 / NIBIB NIH HHS
                • AR33236 / NIAMS NIH HHS

                References

                This article includes 53 references
                1. Barbero A, Grogan S, Schäfer D, Heberer M, Mainil-Varlet P, Martin I. Age related changes in human articular chondrocyte yield, proliferation and post-expansion chondrogenic capacity.. Osteoarthritis Cartilage 2004 Jun;12(6):476-84.
                  pubmed: 15135144doi: 10.1016/j.joca.2004.02.010google scholar: lookup
                2. Barry F, Boynton RE, Liu B, Murphy JM. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components.. Exp Cell Res 2001 Aug 15;268(2):189-200.
                  pubmed: 11478845doi: 10.1006/excr.2001.5278google scholar: lookup
                3. Bolton MC, Dudhia J, Bayliss MT. Age-related changes in the synthesis of link protein and aggrecan in human articular cartilage: implications for aggregate stability.. Biochem J 1999 Jan 1;337 ( Pt 1)(Pt 1):77-82.
                  pmc: PMC1219938pubmed: 9854027
                4. Buckwalter JA, Rosenberg LC. Electron microscopic studies of cartilage proteoglycans. Direct evidence for the variable length of the chondroitin sulfate-rich region of proteoglycan subunit core protein.. J Biol Chem 1982 Aug 25;257(16):9830-9.
                  pubmed: 6809744
                5. Buckwalter JA, Roughley PJ, Rosenberg LC. Age-related changes in cartilage proteoglycans: quantitative electron microscopic studies.. Microsc Res Tech 1994 Aug 1;28(5):398-408.
                  pubmed: 7919527doi: 10.1002/jemt.1070280506google scholar: lookup
                6. Buschmann MD, Gluzband YA, Grodzinsky AJ, Kimura JH, Hunziker EB. Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix.. J Orthop Res 1992 Nov;10(6):745-58.
                  pubmed: 1403287doi: 10.1002/jor.1100100602google scholar: lookup
                7. Calabro A, Midura R, Wang A, West L, Plaas A, Hascall VC. Fluorophore-assisted carbohydrate electrophoresis (FACE) of glycosaminoglycans.. Osteoarthritis Cartilage 2001;9 Suppl A:S16-22.
                  pubmed: 11680680doi: 10.1053/joca.2001.0439google scholar: lookup
                8. Chen FH, Tuan RS. Mesenchymal stem cells in arthritic diseases.. Arthritis Res Ther 2008;10(5):223.
                  pmc: PMC2592798pubmed: 18947375doi: 10.1186/ar2514google scholar: lookup
                9. Connelly JT, Wilson CG, Levenston ME. Characterization of proteoglycan production and processing by chondrocytes and BMSCs in tissue engineered constructs.. Osteoarthritis Cartilage 2008 Sep;16(9):1092-100.
                  pmc: PMC2605680pubmed: 18294870doi: 10.1016/j.joca.2008.01.004google scholar: lookup
                10. Davis ME, Hsieh PC, Takahashi T, Song Q, Zhang S, Kamm RD, Grodzinsky AJ, Anversa P, Lee RT. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction.. Proc Natl Acad Sci U S A 2006 May 23;103(21):8155-60.
                  pmc: PMC1472445pubmed: 16698918doi: 10.1073/pnas.0602877103google scholar: lookup
                11. Dean D, Han L, Grodzinsky AJ, Ortiz C. Compressive nanomechanics of opposing aggrecan macromolecules.. J Biomech 2006;39(14):2555-65.
                  pubmed: 16289077doi: 10.1016/j.jbiomech.2005.09.007google scholar: lookup
                12. Dudhia J. Aggrecan, aging and assembly in articular cartilage.. Cell Mol Life Sci 2005 Oct;62(19-20):2241-56.
                  pubmed: 16143826doi: 10.1007/s00018-005-5217-xgoogle scholar: lookup
                13. Eisenberg SR, Grodzinsky AJ. Electrokinetic micromodel of extracellular matrix and other polyelectrolyte networks. PhysicoChemical Hydrodynamics 1988;10:517–539.
                14. Elisseeff J, McIntosh W, Anseth K, Riley S, Ragan P, Langer R. Photoencapsulation of chondrocytes in poly(ethylene oxide)-based semi-interpenetrating networks.. J Biomed Mater Res 2000 Aug;51(2):164-71.
                  pubmed: 10825215doi: 10.1002/(sici)1097-4636(200008)51:2<164::aid-jbm4>3.0.co;2-wgoogle scholar: lookup
                15. Erickson IE, Huang AH, Chung C, Li RT, Burdick JA, Mauck RL. Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels.. Tissue Eng Part A 2009 May;15(5):1041-52.
                  pmc: PMC2810411pubmed: 19119920doi: 10.1089/ten.tea.2008.0099google scholar: lookup
                16. Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures.. Connect Tissue Res 1982;9(4):247-8.
                  pubmed: 6215207doi: 10.3109/03008208209160269google scholar: lookup
                17. Frank EH, Grodzinsky AJ. Cartilage electromechanics--I. Electrokinetic transduction and the effects of electrolyte pH and ionic strength.. J Biomech 1987;20(6):615-27.
                  pubmed: 3611137doi: 10.1016/0021-9290(87)90282-xgoogle scholar: lookup
                18. Hascall VC, Calabro A, Midura RJ, Yanagishita M. Isolation and characterization of proteoglycans.. Methods Enzymol 1994;230:390-417.
                  pubmed: 8139509doi: 10.1016/0076-6879(94)30026-7google scholar: lookup
                19. Hsieh PC, Davis ME, Gannon J, MacGillivray C, Lee RT. Controlled delivery of PDGF-BB for myocardial protection using injectable self-assembling peptide nanofibers.. J Clin Invest 2006 Jan;116(1):237-48.
                  pmc: PMC1312017pubmed: 16357943doi: 10.1172/jci25878google scholar: lookup
                20. Im GI, Jung NH, Tae SK. Chondrogenic differentiation of mesenchymal stem cells isolated from patients in late adulthood: the optimal conditions of growth factors.. Tissue Eng 2006 Mar;12(3):527-36.
                  pubmed: 16579686doi: 10.1089/ten.2006.12.527google scholar: lookup
                21. Izumikawa T, Koike T, Shiozawa S, Sugahara K, Tamura J, Kitagawa H. Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization: chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members.. J Biol Chem 2008 Apr 25;283(17):11396-406.
                  pubmed: 18316376doi: 10.1074/jbc.m707549200google scholar: lookup
                22. Izumikawa T, Uyama T, Okuura Y, Sugahara K, Kitagawa H. Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor.. Biochem J 2007 May 1;403(3):545-52.
                  pmc: PMC1876374pubmed: 17253960doi: 10.1042/bj20061876google scholar: lookup
                23. Jiang Y, Mishima H, Sakai S, Liu YK, Ohyabu Y, Uemura T. Gene expression analysis of major lineage-defining factors in human bone marrow cells: effect of aging, gender, and age-related disorders.. J Orthop Res 2008 Jul;26(7):910-7.
                  pubmed: 18302252doi: 10.1002/jor.20623google scholar: lookup
                24. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells.. Exp Cell Res 1998 Jan 10;238(1):265-72.
                  pubmed: 9457080doi: 10.1006/excr.1997.3858google scholar: lookup
                25. Kim YJ, Sah RL, Doong JY, Grodzinsky AJ. Fluorometric assay of DNA in cartilage explants using Hoechst 33258.. Anal Biochem 1988 Oct;174(1):168-76.
                  pubmed: 2464289doi: 10.1016/0003-2697(88)90532-5google scholar: lookup
                26. Kimura JH, Caputo CB, Hascall VC. The effect of cycloheximide on synthesis of proteoglycans by cultured chondrocytes from the Swarm rat chondrosarcoma.. J Biol Chem 1981 May 10;256(9):4368-76.
                  pubmed: 6783661
                27. Kisiday J, Jin M, Kurz B, Hung H, Semino C, Zhang S, Grodzinsky AJ. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair.. Proc Natl Acad Sci U S A 2002 Jul 23;99(15):9996-10001.
                  pmc: PMC126613pubmed: 12119393doi: 10.1073/pnas.142309999google scholar: lookup
                28. Kisiday JD, Kopesky PW, Evans CH, Grodzinsky AJ, McIlwraith CW, Frisbie DD. Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures.. J Orthop Res 2008 Mar;26(3):322-31.
                  pubmed: 17960654doi: 10.1002/jor.20508google scholar: lookup
                29. Kopesky PW, Vanderploeg EJ, Sandy JS, Kurz B, Grodzinsky AJ. Self-assembling peptide hydrogels modulate in vitro chondrogenesis of bovine bone marrow stromal cells.. Tissue Eng Part A 2010 Feb;16(2):465-77.
                  pmc: PMC2862611pubmed: 19705959doi: 10.1089/ten.tea.2009.0158google scholar: lookup
                30. Lee H-Y, Kopesky PW, Plaas AHK, Diaz MA, Sandy JD, Frisbie DD, Kisiday JD, Ortiz C, Grodzinsky AJ. Adult Equine MSCs Synthesize Aggrecan having Nanomechanical Compressibility and Biochemical Composition Characteristic of Young Growth Cartilage. Presented at the 55th Orthopedic Research Society; Las Vegas, NV. February 22-25, 2009.2009.
                31. Lee RC, Frank EH, Grodzinsky AJ, Roylance DK. Oscillatory compressional behavior of articular cartilage and its associated electromechanical properties.. J Biomech Eng 1981 Nov;103(4):280-92.
                  pubmed: 7311495doi: 10.1115/1.3138294google scholar: lookup
                32. Little PJ, Ballinger ML, Burch ML, Osman N. Biosynthesis of natural and hyperelongated chondroitin sulfate glycosaminoglycans: new insights into an elusive process.. Open Biochem J 2008;2:135-42.
                  pmc: PMC2627520pubmed: 19238187doi: 10.2174/1874091x00802010135google scholar: lookup
                33. Mattern KJ, Nakornchai C, Deen WM. Darcy permeability of agarose-glycosaminoglycan gels analyzed using fiber-mixture and donnan models.. Biophys J 2008 Jul;95(2):648-56.
                  pmc: PMC2440444pubmed: 18375508doi: 10.1529/biophysj.107.127316google scholar: lookup
                34. Mauck RL, Soltz MA, Wang CC, Wong DD, Chao PH, Valhmu WB, Hung CT, Ateshian GA. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels.. J Biomech Eng 2000 Jun;122(3):252-60.
                  pubmed: 10923293doi: 10.1115/1.429656google scholar: lookup
                35. Mauck RL, Yuan X, Tuan RS. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture.. Osteoarthritis Cartilage 2006 Feb;14(2):179-89.
                  pubmed: 16257243doi: 10.1016/j.joca.2005.09.002google scholar: lookup
                36. Mitchell D, Hardingham T. The control of chondroitin sulphate biosynthesis and its influence on the structure of cartilage proteoglycans.. Biochem J 1982 Feb 15;202(2):387-95.
                  pmc: PMC1158123pubmed: 6807292doi: 10.1042/bj2020387google scholar: lookup
                37. Mouw JK, Connelly JT, Wilson CG, Michael KE, Levenston ME. Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells.. Stem Cells 2007 Mar;25(3):655-63.
                  pubmed: 17124008doi: 10.1634/stemcells.2006-0435google scholar: lookup
                38. Ng L, Grodzinsky AJ, Patwari P, Sandy J, Plaas A, Ortiz C. Individual cartilage aggrecan macromolecules and their constituent glycosaminoglycans visualized via atomic force microscopy.. J Struct Biol 2003 Sep;143(3):242-57.
                  pubmed: 14572479doi: 10.1016/j.jsb.2003.08.006google scholar: lookup
                39. Nöth U, Steinert AF, Tuan RS. Technology insight: adult mesenchymal stem cells for osteoarthritis therapy.. Nat Clin Pract Rheumatol 2008 Jul;4(7):371-80.
                  pubmed: 18477997doi: 10.1038/ncprheum0816google scholar: lookup
                40. Patwari P, Gao G, Lee JH, Grodzinsky AJ, Sandy JD. Analysis of ADAMTS4 and MT4-MMP indicates that both are involved in aggrecanolysis in interleukin-1-treated bovine cartilage.. Osteoarthritis Cartilage 2005 Apr;13(4):269-77.
                  pmc: PMC2771540pubmed: 15780640doi: 10.1016/j.joca.2004.10.023google scholar: lookup
                41. Patwari P, Kurz B, Sandy JD, Grodzinsky AJ. Mannosamine inhibits aggrecanase-mediated changes in the physical properties and biochemical composition of articular cartilage.. Arch Biochem Biophys 2000 Feb 1;374(1):79-85.
                  pubmed: 10640399doi: 10.1006/abbi.1999.1538google scholar: lookup
                42. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells.. Science 1999 Apr 2;284(5411):143-7.
                  pubmed: 10102814doi: 10.1126/science.284.5411.143google scholar: lookup
                43. Plaas AH, Sandy JD. Age-related decrease in the link-stability of proteoglycan aggregates formed by articular chondrocytes.. Biochem J 1984 May 15;220(1):337-40.
                  pmc: PMC1153629pubmed: 6743270doi: 10.1042/bj2200337google scholar: lookup
                44. Ragan PM, Chin VI, Hung HH, Masuda K, Thonar EJ, Arner EC, Grodzinsky AJ, Sandy JD. Chondrocyte extracellular matrix synthesis and turnover are influenced by static compression in a new alginate disk culture system.. Arch Biochem Biophys 2000 Nov 15;383(2):256-64.
                  pubmed: 11185561doi: 10.1006/abbi.2000.2060google scholar: lookup
                45. Roughley PJ, White RJ. Age-related changes in the structure of the proteoglycan subunits from human articular cartilage.. J Biol Chem 1980 Jan 10;255(1):217-24.
                  pubmed: 7350154
                46. Scharstuhl A, Schewe B, Benz K, Gaissmaier C, Bühring HJ, Stoop R. Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology.. Stem Cells 2007 Dec;25(12):3244-51.
                  pubmed: 17872501doi: 10.1634/stemcells.2007-0300google scholar: lookup
                47. Semino CE, Merok JR, Crane GG, Panagiotakos G, Zhang S. Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds.. Differentiation 2003 Jun;71(4-5):262-70.
                  pubmed: 12823227doi: 10.1046/j.1432-0436.2003.7104503.xgoogle scholar: lookup
                48. Sheiko SS, Möller M. Visualization of macromolecules--a first step to manipulation and controlled response.. Chem Rev 2001 Dec;101(12):4099-124.
                  pubmed: 11740928doi: 10.1021/cr990129vgoogle scholar: lookup
                49. Tran-Khanh N, Hoemann CD, McKee MD, Henderson JE, Buschmann MD. Aged bovine chondrocytes display a diminished capacity to produce a collagen-rich, mechanically functional cartilage extracellular matrix.. J Orthop Res 2005 Nov;23(6):1354-62.
                  pubmed: 16048738doi: 10.1016/j.orthres.2005.05.009.1100230617google scholar: lookup
                50. Victor XV, Nguyen TK, Ethirajan M, Tran VM, Nguyen KV, Kuberan B. Investigating the elusive mechanism of glycosaminoglycan biosynthesis.. J Biol Chem 2009 Sep 18;284(38):25842-53.
                  pmc: PMC2757986pubmed: 19628873doi: 10.1074/jbc.m109.043208google scholar: lookup
                51. Williamson AK, Chen AC, Sah RL. Compressive properties and function-composition relationships of developing bovine articular cartilage.. J Orthop Res 2001 Nov;19(6):1113-21.
                  pubmed: 11781013doi: 10.1016/s0736-0266(01)00052-3google scholar: lookup
                52. Wilson CG, Nishimuta JF, Levenston ME. Chondrocytes and meniscal fibrochondrocytes differentially process aggrecan during de novo extracellular matrix assembly.. Tissue Eng Part A 2009 Jul;15(7):1513-22.
                  pmc: PMC2810410pubmed: 19260779doi: 10.1089/ten.tea.2008.0106google scholar: lookup
                53. WOESSNER JF Jr. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid.. Arch Biochem Biophys 1961 May;93:440-7.
                  pubmed: 13786180doi: 10.1016/0003-9861(61)90291-0google scholar: lookup

                Citations

                This article has been cited 25 times.
                1. Wang C, Kahle ER, Li Q, Han L. Nanomechanics of Aggrecan: A New Perspective on Cartilage Biomechanics, Disease and Regeneration.. Adv Exp Med Biol 2023;1402:69-82.
                  doi: 10.1007/978-3-031-25588-5_5pubmed: 37052847google scholar: lookup
                2. Nia HT, Ortiz C, Grodzinsky A. Aggrecan: Approaches to Study Biophysical and Biomechanical Properties.. Methods Mol Biol 2022;2303:209-226.
                  doi: 10.1007/978-1-0716-1398-6_17pubmed: 34626381google scholar: lookup
                3. Chen X, Hughes R, Mullin N, Hawkins RJ, Holen I, Brown NJ, Hobbs JK. Mechanical Heterogeneity in the Bone Microenvironment as Characterized by Atomic Force Microscopy.. Biophys J 2020 Aug 4;119(3):502-513.
                  doi: 10.1016/j.bpj.2020.06.026pubmed: 32668233google scholar: lookup
                4. Virk MS, Luo W, Sikes KJ, Li J, Plaas A, Cole BJ. Gene expression profiling of progenitor cells isolated from rat rotator cuff musculotendinous junction.. BMC Musculoskelet Disord 2020 Mar 28;21(1):194.
                  doi: 10.1186/s12891-020-03190-9pubmed: 32222148google scholar: lookup
                5. Han B, Nia HT, Wang C, Chandrasekaran P, Li Q, Chery DR, Li H, Grodzinsky AJ, Han L. AFM-Nanomechanical Test: An Interdisciplinary Tool That Links the Understanding of Cartilage and Meniscus Biomechanics, Osteoarthritis Degeneration, and Tissue Engineering.. ACS Biomater Sci Eng 2017 Sep 11;3(9):2033-2049.
                  doi: 10.1021/acsbiomaterials.7b00307pubmed: 31423463google scholar: lookup
                6. Liebesny PH, Mroszczyk K, Zlotnick H, Hung HH, Frank E, Kurz B, Zanotto G, Frisbie D, Grodzinsky AJ. Enzyme Pretreatment plus Locally Delivered HB-IGF-1 Stimulate Integrative Cartilage Repair In Vitro.. Tissue Eng Part A 2019 Sep;25(17-18):1191-1201.
                  doi: 10.1089/ten.TEA.2019.0013pubmed: 31237484google scholar: lookup
                7. Rakic R, Bourdon B, Demoor M, Maddens S, Saulnier N, Galéra P. Differences in the intrinsic chondrogenic potential of equine umbilical cord matrix and cord blood mesenchymal stromal/stem cells for cartilage regeneration.. Sci Rep 2018 Sep 14;8(1):13799.
                  doi: 10.1038/s41598-018-28164-9pubmed: 30217993google scholar: lookup
                8. Desancé M, Contentin R, Bertoni L, Gomez-Leduc T, Branly T, Jacquet S, Betsch JM, Batho A, Legendre F, Audigié F, Galéra P, Demoor M. Chondrogenic Differentiation of Defined Equine Mesenchymal Stem Cells Derived from Umbilical Cord Blood for Use in Cartilage Repair Therapy.. Int J Mol Sci 2018 Feb 10;19(2).
                  doi: 10.3390/ijms19020537pubmed: 29439436google scholar: lookup
                9. Zhang YT, Niu J, Wang Z, Liu S, Wu J, Yu B. Repair of Osteochondral Defects in a Rabbit Model Using Bilayer Poly(Lactide-co-Glycolide) Scaffolds Loaded with Autologous Platelet-Rich Plasma.. Med Sci Monit 2017 Oct 31;23:5189-5201.
                  doi: 10.12659/msm.904082pubmed: 29088126google scholar: lookup
                10. Liebesny PH, Byun S, Hung HH, Pancoast JR, Mroszczyk KA, Young WT, Lee RT, Frisbie DD, Kisiday JD, Grodzinsky AJ. Growth Factor-Mediated Migration of Bone Marrow Progenitor Cells for Accelerated Scaffold Recruitment.. Tissue Eng Part A 2016 Jul;22(13-14):917-27.
                  doi: 10.1089/ten.TEA.2015.0524pubmed: 27268956google scholar: lookup
                11. Peeters M, van Rijn S, Vergroesen PP, Paul CP, Noske DP, Vandertop WP, Wurdinger T, Helder MN. Bioluminescence-mediated longitudinal monitoring of adipose-derived stem cells in a large mammal ex vivo organ culture.. Sci Rep 2015 Sep 9;5:13960.
                  doi: 10.1038/srep13960pubmed: 26350622google scholar: lookup
                12. Lee B, Han L, Frank EH, Grodzinsky AJ, Ortiz C. Dynamic nanomechanics of individual bone marrow stromal cells and cell-matrix composites during chondrogenic differentiation.. J Biomech 2015 Jan 2;48(1):171-5.
                  doi: 10.1016/j.jbiomech.2014.11.005pubmed: 25468666google scholar: lookup
                13. Florine EM, Miller RE, Liebesny PH, Mroszczyk KA, Lee RT, Patwari P, Grodzinsky AJ. Delivering heparin-binding insulin-like growth factor 1 with self-assembling peptide hydrogels.. Tissue Eng Part A 2015 Feb;21(3-4):637-46.
                  doi: 10.1089/ten.TEA.2013.0679pubmed: 25231349google scholar: lookup
                14. Florine EM, Miller RE, Porter RM, Evans CH, Kurz B, Grodzinsky AJ. Effects of Dexamethasone on Mesenchymal Stromal Cell Chondrogenesis and Aggrecanase Activity: Comparison of Agarose and Self-Assembling Peptide Scaffolds.. Cartilage 2013 Jan 1;4(1):63-74.
                  doi: 10.1177/1947603512455196pubmed: 24533173google scholar: lookup
                15. Sun L, Reagan MR, Kaplan DL. Role of Cartilage Forming Cells in Regenerative Medicine for Cartilage Repair.. Orthop Res Rev 2010 Sep 1;2010(2):85-94.
                  doi: 10.2147/ORR.S7194pubmed: 24049462google scholar: lookup
                16. Brown CP. Advancing musculoskeletal research with nanoscience.. Nat Rev Rheumatol 2013 Oct;9(10):614-23.
                  doi: 10.1038/nrrheum.2013.112pubmed: 23881069google scholar: lookup
                17. Kopesky PW, Byun S, Vanderploeg EJ, Kisiday JD, Frisbie DD, Grodzinsky AJ. Sustained delivery of bioactive TGF-β1 from self-assembling peptide hydrogels induces chondrogenesis of encapsulated bone marrow stromal cells.. J Biomed Mater Res A 2014 May;102(5):1275-85.
                  doi: 10.1002/jbm.a.34789pubmed: 23650117google scholar: lookup
                18. Lee HY, Han L, Roughley PJ, Grodzinsky AJ, Ortiz C. Age-related nanostructural and nanomechanical changes of individual human cartilage aggrecan monomers and their glycosaminoglycan side chains.. J Struct Biol 2013 Mar;181(3):264-73.
                  doi: 10.1016/j.jsb.2012.12.008pubmed: 23270863google scholar: lookup
                19. Han L, Grodzinsky AJ, Ortiz C. Nanomechanics of the Cartilage Extracellular Matrix.. Annu Rev Mater Res 2011 Jul 1;41:133-168.
                  doi: 10.1146/annurev-matsci-062910-100431pubmed: 22792042google scholar: lookup
                20. Gadjanski I, Spiller K, Vunjak-Novakovic G. Time-dependent processes in stem cell-based tissue engineering of articular cartilage.. Stem Cell Rev Rep 2012 Sep;8(3):863-81.
                  doi: 10.1007/s12015-011-9328-5pubmed: 22016073google scholar: lookup
                21. Spiller KL, Maher SA, Lowman AM. Hydrogels for the repair of articular cartilage defects.. Tissue Eng Part B Rev 2011 Aug;17(4):281-99.
                  doi: 10.1089/ten.TEB.2011.0077pubmed: 21510824google scholar: lookup
                22. Erickson IE, van Veen SC, Sengupta S, Kestle SR, Mauck RL. Cartilage matrix formation by bovine mesenchymal stem cells in three-dimensional culture is age-dependent.. Clin Orthop Relat Res 2011 Oct;469(10):2744-53.
                  doi: 10.1007/s11999-011-1869-zpubmed: 21424832google scholar: lookup
                23. Raabe O, Reich C, Wenisch S, Hild A, Burg-Roderfeld M, Siebert HC, Arnhold S. Hydrolyzed fish collagen induced chondrogenic differentiation of equine adipose tissue-derived stromal cells.. Histochem Cell Biol 2010 Dec;134(6):545-54.
                  doi: 10.1007/s00418-010-0760-4pubmed: 21076963google scholar: lookup
                24. Lee HY, Kopesky PW, Plaas A, Sandy J, Kisiday J, Frisbie D, Grodzinsky AJ, Ortiz C. Adult bone marrow stromal cell-based tissue-engineered aggrecan exhibits ultrastructure and nanomechanical properties superior to native cartilage.. Osteoarthritis Cartilage 2010 Nov;18(11):1477-86.
                  doi: 10.1016/j.joca.2010.07.015pubmed: 20692354google scholar: lookup
                25. Kopesky PW, Vanderploeg EJ, Kisiday JD, Frisbie DD, Sandy JD, Grodzinsky AJ. Controlled delivery of transforming growth factor β1 by self-assembling peptide hydrogels induces chondrogenesis of bone marrow stromal cells and modulates Smad2/3 signaling.. Tissue Eng Part A 2011 Jan;17(1-2):83-92.
                  doi: 10.1089/ten.TEA.2010.0198pubmed: 20672992google scholar: lookup
                Subscribe to our newsletter
                Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.