Nanomechanical phenotype of chondroadherin-null murine articular cartilage

Matrix Biology

Volumn 38, Issue , 2014, Pages 84-90

  Batista, Michael A ^a   Nia, Hadi T ^a   Önnerfjord, Patrik ^b   Cox, Karen A ^c   Ortiz, Christine ^a   Grodzinsky, Alan J ^a,d   Heinegård, Dick ^b   Han, Lin ^a,e  

^a Massachusetts Institute of Technology   (United States)

^b LUND UNIVERSITY   (Sweden)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d Department of Electrical Engineering and Computer Science   (United States)

^e DREXEL UNIVERSITY   (United States)

Author keywords

Cartilage; Chondroadherin; Collagen; Murine model; Nanoindentation

Indexed keywords

AGGRECAN; CHONDROADHERIN; PROTEOGLYCAN; UNCLASSIFIED DRUG; COLLAGEN; SCLEROPROTEIN;

ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; ATOMIC FORCE MICROSCOPY; BONE DEVELOPMENT; COLLAGEN FIBER; CONTROLLED STUDY; FEMALE; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN FUNCTION; RIGIDITY; SURFACE PROPERTY; TRANSGENIC MOUSE; VISCOELASTICITY; ANIMAL; BIOMECHANICS; DEFICIENCY; ELASTICITY; METABOLISM; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; BIOMECHANICAL PHENOMENA; CARTILAGE, ARTICULAR; COLLAGEN; ELASTICITY; EXTRACELLULAR MATRIX PROTEINS; MICE; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; PHENOTYPE;

EID: 84908463601     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.05.008     Document Type: Article

References (51)

1. Ameye L., Young M.F. Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 2002, 12:107R-116R.
2. Ameye L.G., Young M.F. Animal models of osteoarthritis: lessons learned while seeking the 'Holy Grail'. Curr. Opin. Rheumatol. 2006, 18:537-547.
3. Ameye L., Aria D., Jepsen K., Oldberg A., Xu T., Young M.F. Abnormal collagen fibrils in tendons of biglycan/fibromodulin-deficient mice lead to gait impairment, ectopic ossification, and osteoarthritis. FASEB J. 2002, 16:673-680.
4. Buschmann M.D., Kim Y.-J., Wong M., Frank E., Hunziker E.B., Grodzinsky A.J. Stimulation of aggrecan synthesis in cartilage explants by cyclic loading is localized to regions of high interstitial fluid flow. Arch. Biochem. Biophys. 1999, 366:1-7.
5. Camper L., Heinegård D., Lundgren-Åkerlund E. Integrin α2β1 is a receptor for the cartilage matrix protein chondroadherin. J. Cell Biol. 1997, 138:1159-1167.
6. Conover W.J., Iman R.L. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 1981, 35:124-129.
7. Corsi A., Xu T., Chen X.-D., Boyde A., Liang J., Mankani M., Sommer B., Iozzo R.V., Eichstetter I., Robey P.G., Bianco P., Young M.F. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J. Bone Miner. Res. 2002, 17:1180-1189.
8. Eyre D.R., Weis M.A., Wu J.-J. Articular cartilage collagen: an irreplaceable framework?. Eur. Cell Mater. 2006, 12:57-63.
9. Geyer G., Linss W. Toluidine blue staining of cartilage proteoglycan subunits. Acta Histochem. 1978, 61:127-134.
10. Glasson S.S., Blanchet T.J., Morris E.A. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage 2007, 15:1061-1069.
11. Grodzinsky A.J., Roth V., Myers E., Grossman W.D., Mow V.C. The significance of electromechanical and osmotic forces in the nonequilibrium swelling behavior of articular cartilage in tension. J. Biomech. Eng. 1981, 103:221-231.
12. Gupta S., Lin J., Ashby P., Pruitt L. A fiber reinforced poroelastic model of nanoindentation of porcine costal cartilage: a combined experimental and finite element approach. J. Mech. Behav. Biomed. Mater. 2009, 2:326-338.
13. 1 binding motif in chondroadherin mediating cell attachment. J. Biol. Chem. 2011, 286:3925-3934.
14. Haglund L., Tillgren V., Önnerfjord P., Heinegård D. The C-terminal peptide of chondroadherin modulates cellular activity by selectively binding to heparan sulfate chains. J. Biol. Chem. 2013, 288:995-1008.
15. Han L., Frank E.H., Greene J.J., Lee H.-Y., Hung H.-H.K., Grodzinsky A.J., Ortiz C. Time-dependent nanomechanics of cartilage. Biophys. J. 2011, 100:1846-1854.
16. Han L., Grodzinsky A.J., Ortiz C. Nanomechanics of the cartilage extracellular matrix. Annu. Rev. Mater. Res. 2011, 41:133-168.
17. Hayes W.C., Bodine A.J. Flow-independent viscoelastic properties of articular cartilage matrix. J. Biomech. 1978, 11:407-419.
18. Hedbom E., Heinegård D. Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J. Biol. Chem. 1993, 268:27307-27312.
19. Heinegård D. Proteoglycans and more-from molecules to biology. Int. J. Exp. Pathol. 2009, 90:575-586.
20. Hessle L., Stordalen G.A., Wenglén C., Petzold C., Tanner K.E., Brorson S.-H., Baekkevold E.S., Önnerfjord P., Reinholt F.P., Heinegård D. The skeletal phenotype of chondroadherin deficient mice. PLoS One 2013, 8:e63080.
21. Hughes L.C., Archer C.W., ap Gwynn I. The ultrastructure of mouse articular cartilage: collagen orientation and implications for tissue functionality. A polarised light and scanning electron microscope study and review. Eur. Cell. Mater. 2005, 9:68-84.
22. Hunziker E.B., 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, 15:403-413.
23. Hutter J.L., Bechhoefer J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 1993, 64:1868-1873.
24. Iozzo R.V., Goldoni S., Berendsen A.D., Young M.F. Small leucine-rich proteoglycans. The Extracellular Matrix: An Overview 2011, 197-231. Springer-Verlag, Berlin. R.F. Mecham (Ed.).
25. Jepsen K.J., Wu F., Peragallo J.H., Paul J., Roberts L., Ezura Y., Oldberg A., Birk D.E., Chakravarti S. A syndrome of joint laxity and impaired tendon integrity in lumican- and fibromodulin-deficient mice. J. Biol. Chem. 2002, 277:35532-35540.
26. June R.K., Ly S., Fyhrie D.P. Cartilage stress-relaxation proceeds slower at higher compressive strains. Arch. Biochem. Biophys. 2009, 483:75-80.
27. Kalamajski S., Oldberg Å. The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol. 2010, 29:248-253.
28. Larsson T., Sommarin Y., Paulsson M., Antonsson P., Hedbom E., Wendel M., Heinegård D. Cartilage matrix proteins. A basic 36-kda protein with a restricted distribution to cartilage and bone. J. Biol. Chem. 1991, 266:20428-20433.
29. Lee H.-Y., Han L., Roughley P.J., Grodzinsky A.J., Ortiz C. Age-related nanostructural and nanomechanical changes of individual human cartilage aggrecan monomers and their glycosaminoglycan side chains. J. Struct. Biol. 2013, 181:264-273.
30. Li J., Anemaet W.K., Diaz M.A., Buchanan S., Tortorella M., Malfait A.M., Mikecz K., Sandy J.D., Plaas A. Knockout of ADAMTS5 does not eliminate cartilage aggrecanase activity but abrogates joint fibrosis and promotes cartilage aggrecan deposition in murine osteoarthritis models. J. Orthop. Res. 2010, 29:516-522.
31. Lin D.C., Dimitriadis E.K., Horkay F. Robust strategies for automated AFM force curve analysis-I. Non-adhesive indentation of soft, inhomogeneous materials. J. Biomech. Eng. 2007, 129:430-440.
32. Malda J., de Grauw J.C., Benders K.E.M., Kik M.J.L., van de Lest C.H.A., Creemers L.B., Dhert W.J.A., van Weeren P.R. Of mice, men and elephants: the relation between articular cartilage thickness and body mass. PLoS One 2013, 8:e57683.
33. Månsson B., Wenglén C., Mörgelin M., Saxne T., Heinegård D. Association of chondroadherin with collagen type II. J. Biol. Chem. 2001, 276:32883-32888.
34. Maroudas A. Physicochemical properties of articular cartilage. Adult Articular Cartilage 1979, 215-290. Pitman, England. M.A.R. Freeman (Ed.).
35. Maroudas A., Bayliss M.T., Uchitel-Kaushansky N., Schneiderman R., Gilav E. Aggrecan turnover in human articular cartilage: use of aspartic acid racemization as a marker of molecular age. Arch. Biochem. Biophys. 1998, 350:61-71.
36. Miller G.J., Morgan E.F. Use of microindentation to characterize the mechanical properties of articular cartilage: comparison of biphasic material properties across length scales. Osteoarthritis Cartilage 2010, 18:1051-1057.
37. Mow V.C., Kuei S.C., Lai W.M., Armstrong C.G. Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J. Biomech. Eng. 1980, 102:73-84.
38. Neame P.J., Choi H.U., Rosenberg L.C. The primary structure of the core protein of the small, leucine-rich proteoglycan (PG I) from bovine articular cartilage. J. Biol. Chem. 1989, 264:8653-8661.
39. Neame P.J., Sommarin Y., Boynton R.E., Heinegård D. The structure of a 38-kDa leucine-rich protein (chondroadherin) isolated from bovine cartilage. J. Biol. Chem. 1994, 269:1-8.
40. Ng L., Grodzinsky A.J., 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, 143:242-257.
41. Nia H.T., Han L., Li Y., Ortiz C., Grodzinsky A.J. Poroelasticity of cartilage at the nanoscale. Biophys. J. 2011, 101:2304-2313.
42. Nia H.T., Bozchalooi I.S., Li Y., Han L., Hung H.-H., Frank E.H., Youcef-Toumi K., Ortiz C., Grodzinsky A.J. High-bandwidth AFM-based rheology reveals that cartilage is most sensitive to high loading rates at early stages of impairment. Biophys. J. 2013, 104:1529-1537.
43. Ohtani O. Three-dimensional organization of the connective tissue fibers of the human pancreas: a scanning electron microscopic study of NaOH treated-tissues. Arch. Histol. Jpn. 1987, 50:557-566.
44. Schaefer L., Iozzo R.V. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J. Biol. Chem. 2008, 283:21305-21309.
45. Shen Z.X., Gantcheva S., Månsson B., Heinegård D., Sommarin Y. Chondroadherin expression changes in skeletal development. Biochem. J. 1998, 330:549-557.
46. Stockwell R.A. The interrelationship of cell density and cartilage thickness in mammalian articular cartilage. J. Anat. 1971, 109:411-421.
47. Stolz M., Gottardi R., Raiteri R., Miot S., Martin I., Imer R., Staufer U., Raducanu A., Düggelin M., Baschong W., Daniels A.U., Friederich N.F., Aszodi A., Aebi U. Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nat. Nanotechnol. 2009, 4:186-192.
48. Timoshenko S., Goodier J.N. Thermal stress. Theory of Elasticity 1951, 399-437. McGraw-Hill, New York, NY. 2nd ed.
49. Vanden Berg-Foels W.S., Scipioni L., Huynh C., Wen X. Helium ion microscopy for high-resolution visualization of the articular cartilage collagen network. J. Microsc. 2012, 246:168-176.
50. Verzijl N., DeGroot J., Thorpe S.R., Bank R.A., Shaw J.N., Lyons T.J., Bijlsma J.W.J., Lafeber F.P.J.G., Baynes J.W., TeKoppele J.M. Effect of collagen turnover on the accumulation of advanced glycation end products. J. Biol. Chem. 2000, 275:39027-39031.
51. Wiberg C., Heinegård D., Wenglén C., Timpl R., Mörgelin M. Biglycan organizes collagen VI into hexagonal-like networks resembling tissue structures. J. Biol. Chem. 2002, 277:49120-49126.