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Published in: European Spine Journal 9/2008

01-09-2008 | Original Article

Anulus fibrosus tension inhibits degenerative structural changes in lamellar collagen

Authors: Jeffrey C. Lotz, Tamer Hadi, Clayton Bratton, Karen M. Reiser, Adam H. Hsieh

Published in: European Spine Journal | Issue 9/2008

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Abstract

Mechanical stress is one of the risk factors believed to influence intervertebral disc degeneration. Animal models have shown that certain regimes of compressive loading can induce a cascade of biological effects that ultimately results in cellular and structural changes in the disc. It has been proposed that both cell-mediated breakdown of collagen and the compromised stability of collagen with loss of anular tension could result in degradation of lamellae in the anulus fibrosus (AF). To determine whether this may be important in the AF, we subjected entire rings of de-cellularized AF tissue to MMP-1 digestion with or without tension. Biomechanical testing found trends of decreasing strength and stiffness when tissues were digested without tension compared with those with tension. To determine the physiologic significance of tissue level tension in the AF, we used an established in vivo murine model to apply a disc compression insult known to cause degeneration. Afterward, that motion segment was placed in fixed-angle bending to impose tissue level tension on part of the AF and compression on the contralateral side. We found that the AF on the convex side of bending retained a healthy lamellar appearance, while the AF on the concave side resembled tissues that had undergone degeneration by loading alone. Varying the time of onset and duration of bending revealed that even a brief duration applied immediately after cessation of compression was beneficial to AF structure on the convex side of bending. Our results suggest that both cell-mediated events and cell-independent mechanisms may contribute to the protective effect of tissue level tension in the AF.
Literature
5.
go back to reference Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477:267–283PubMed Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477:267–283PubMed
7.
go back to reference Ching CT, Chow DH, Yao FY, Holmes AD (2003) The effect of cyclic compression on the mechanical properties of the inter-vertebral disc: an in vivo study in a rat tail model. Clin Biomech (Bristol, Avon) 18:182–189. doi:10.1016/S0268-0033(02)00188-2 CrossRef Ching CT, Chow DH, Yao FY, Holmes AD (2003) The effect of cyclic compression on the mechanical properties of the inter-vertebral disc: an in vivo study in a rat tail model. Clin Biomech (Bristol, Avon) 18:182–189. doi:10.​1016/​S0268-0033(02)00188-2 CrossRef
8.
16.
go back to reference 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 25:506–514PubMed 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 25:506–514PubMed
17.
go back to reference Konttinen YT, Kaapa E, Hukkanen M, Gu XH, Takagi M, Santavirta S et al (1999) Cathepsin G in degenerating and healthy discal tissue. Clin Exp Rheumatol 17:197–204PubMed Konttinen YT, Kaapa E, Hukkanen M, Gu XH, Takagi M, Santavirta S et al (1999) Cathepsin G in degenerating and healthy discal tissue. Clin Exp Rheumatol 17:197–204PubMed
21.
go back to reference Lyons G, Eisenstein SM, Sweet MB (1981) Biochemical changes in intervertebral disc degeneration. Biochim Biophys Acta 673:443–453PubMed Lyons G, Eisenstein SM, Sweet MB (1981) Biochemical changes in intervertebral disc degeneration. Biochim Biophys Acta 673:443–453PubMed
26.
go back to reference Meakin JR, Redpath TW, Hukins DW (2001) The effect of partial removal of the nucleus pulposus from the intervertebral disc on the response of the human annulus fibrosus to compression. Clin Biomech (Bristol, Avon) 16:121–128. doi:10.1016/S0268-0033(00)00075-9 CrossRef Meakin JR, Redpath TW, Hukins DW (2001) The effect of partial removal of the nucleus pulposus from the intervertebral disc on the response of the human annulus fibrosus to compression. Clin Biomech (Bristol, Avon) 16:121–128. doi:10.​1016/​S0268-0033(00)00075-9 CrossRef
27.
go back to reference Miles CA, Ghelashvili M (1999) Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibers. Biophys J 76:3243–3252PubMed Miles CA, Ghelashvili M (1999) Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibers. Biophys J 76:3243–3252PubMed
28.
go back to reference Minond D, Lauer-Fields JL, Nagase H, Fields GB (2004) Matrix metalloproteinase triple-helical peptidase activities are differentially regulated by substrate stability. Biochemistry 43:11474–11481. doi:10.1021/bi048938i PubMedCrossRef Minond D, Lauer-Fields JL, Nagase H, Fields GB (2004) Matrix metalloproteinase triple-helical peptidase activities are differentially regulated by substrate stability. Biochemistry 43:11474–11481. doi:10.​1021/​bi048938i PubMedCrossRef
34.
go back to reference Omlor GW, Lorenz H, Engelleiter K, Richter W, Carstens C, Kroeber MW et al (2006) Changes in gene expression and protein distribution at different stages of mechanically induced disc degeneration—an in vivo study on the New Zealand white rabbit. J Orthop Res 24:385–392. doi:10.1002/jor.20055 PubMedCrossRef Omlor GW, Lorenz H, Engelleiter K, Richter W, Carstens C, Kroeber MW et al (2006) Changes in gene expression and protein distribution at different stages of mechanically induced disc degeneration—an in vivo study on the New Zealand white rabbit. J Orthop Res 24:385–392. doi:10.​1002/​jor.​20055 PubMedCrossRef
38.
go back to reference Palmer EI, Lotz JC (2004) The time-dependent role of cytokines in mechanically induced disc degeneration. In: Transactions of the 50th annual meeting of the Orthopaedic Research Society. San Francisco, p 128 Palmer EI, Lotz JC (2004) The time-dependent role of cytokines in mechanically induced disc degeneration. In: Transactions of the 50th annual meeting of the Orthopaedic Research Society. San Francisco, p 128
40.
go back to reference Reiser KM, Rocha-Mendoza I, Wang M, Yankelevich DR, Bratton C, Knoesen A et al (2004) Polarization-modulated second harmonic generation imaging: method for quantitative assessment of disorganization in anulus. Conf Proc IEEE Eng Med Biol Soc 7:4982–4985PubMed Reiser KM, Rocha-Mendoza I, Wang M, Yankelevich DR, Bratton C, Knoesen A et al (2004) Polarization-modulated second harmonic generation imaging: method for quantitative assessment of disorganization in anulus. Conf Proc IEEE Eng Med Biol Soc 7:4982–4985PubMed
41.
go back to reference Reiser KM, Bratton C, Yankelevich DR, Knoesen A, Rocha-Mendoza I, Lotz JC (2007) Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: Comparison with morphometric analysis. J Biomed Opt 12:064019. doi:10.1117/1.2812631 PubMedCrossRef Reiser KM, Bratton C, Yankelevich DR, Knoesen A, Rocha-Mendoza I, Lotz JC (2007) Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: Comparison with morphometric analysis. J Biomed Opt 12:064019. doi:10.​1117/​1.​2812631 PubMedCrossRef
45.
48.
go back to reference Stoller P, Reiser KM, Celliers PM, Rubenchik AM (2002) Polarization-modulated second harmonic generation in collagen. Biophys J 82:3330–3342PubMedCrossRef Stoller P, Reiser KM, Celliers PM, Rubenchik AM (2002) Polarization-modulated second harmonic generation in collagen. Biophys J 82:3330–3342PubMedCrossRef
50.
go back to reference Sztrolovics R, Alini M, Roughley PJ, Mort JS (1997) Aggrecan degradation in human intervertebral disc and articular cartilage. Biochem J 326(Pt 1):235–241PubMed Sztrolovics R, Alini M, Roughley PJ, Mort JS (1997) Aggrecan degradation in human intervertebral disc and articular cartilage. Biochem J 326(Pt 1):235–241PubMed
54.
go back to reference Weiler C, Nerlich AG, Zipperer J, Bachmeier BE, Boos N (2002) 2002 SSE award competition in basic science: expression of major matrix metalloproteinases is associated with intervertebral disc degradation and resorption. Eur Spine J 11:308–320. doi:10.1007/s00586-002-0472-0 PubMedCrossRef Weiler C, Nerlich AG, Zipperer J, Bachmeier BE, Boos N (2002) 2002 SSE award competition in basic science: expression of major matrix metalloproteinases is associated with intervertebral disc degradation and resorption. Eur Spine J 11:308–320. doi:10.​1007/​s00586-002-0472-0 PubMedCrossRef
Metadata
Title
Anulus fibrosus tension inhibits degenerative structural changes in lamellar collagen
Authors
Jeffrey C. Lotz
Tamer Hadi
Clayton Bratton
Karen M. Reiser
Adam H. Hsieh
Publication date
01-09-2008
Publisher
Springer-Verlag
Published in
European Spine Journal / Issue 9/2008
Print ISSN: 0940-6719
Electronic ISSN: 1432-0932
DOI
https://doi.org/10.1007/s00586-008-0721-y

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