journal article·2016-04

Microstructural heterogeneity directs micromechanics and mechanobiology in native and engineered fibrocartilage

Woojin M. Han, Su-Jin Heo, Tristan P. Driscoll, John F. Delucca, Claire M. McLeod, Lachlan J. Smith, Randall L. Duncan, Robert L. Mauck, Dawn M. Elliott

Nature Materials· Volume 15· Issue 4
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Abstract

Treatment strategies to address pathologies of fibrocartilaginous tissue are in part limited by an incomplete understanding of structure-function relationships in these load-bearing tissues. There is therefore a pressing need to develop micro-engineered tissue platforms that can recreate the highly inhomogeneous tissue microstructures that are known to influence mechanotransductive processes in normal and diseased tissue. Here, we report the quantification of proteoglycan-rich microdomains in developing, ageing and diseased fibrocartilaginous tissues, and the impact of these microdomains on endogenous cell responses to physiologic deformation within a native-tissue context. We also developed a method to generate heterogeneous tissue-engineered constructs (hetTECs) with non-fibrous proteoglycan-rich microdomains engineered into the fibrous structure, and show that these hetTECs match the microstructural, micromechanical and mechanobiological benchmarks of native tissue. Our tissue-engineered platform should facilitate the study of the mechanobiology of developing, homeostatic, degenerating and regenerating fibrous tissues.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Tendon Structure and Treatment · Osteoarthritis Treatment and Mechanisms · Connective tissue disorders research

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (41)

Show source-provided references
1. Andersson, G. B. Epidemiological features of chronic low-back pain. Lancet 354, 581–585 (1999).10.1016/S0140-6736(99)01312-4 ↗
2. Englund, M., Roemer, F. W., Hayashi, D., Crema, M. D. & Guermazi, A. Meniscus pathology, osteoarthritis and the treatment controversy. Nature Rev. Rheumatol. 8, 412–419 (2012).10.1038/nrrheum.2012.69 ↗
3. Nerurkar, N. L. et al. Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nature Mater. 8, 986–992 (2009).10.1038/nmat2558 ↗
4. Fisher, M. B. et al. Engineering meniscus structure and function via multi-layered mesenchymal stem cell-seeded nanofibrous scaffolds. J. Biomech. 48, 1412–1419 (2015).10.1016/j.jbiomech.2015.02.036 ↗
5. Baek, J. et al. Meniscus tissue engineering using a novel combination of electrospun scaffolds and human meniscus cells embedded within an extracellular matrix hydrogel. J. Orthop. Res. 33, 572–583 (2015).10.1002/jor.22802 ↗
6. Puetzer, J. L., Koo, E. & Bonassar, L. J. Induction of fiber alignment and mechanical anisotropy in tissue engineered menisci with mechanical anchoring. J. Biomech. 48, 1436–1443 (2015).10.1016/j.jbiomech.2015.02.033 ↗
7. Baker, B. M. et al. Sacrificial nanofibrous composites provide instruction without impediment and enable functional tissue formation. Proc. Natl Acad. Sci. USA 109, 14176–14181 (2012).10.1073/pnas.1206962109 ↗
8. Han, W. M. et al. Macro- to microscale strain transfer in fibrous tissues is heterogeneous and tissue-specific. Biophys. J. 105, 807–817 (2013).10.1016/j.bpj.2013.06.023 ↗
9. Upton, M. L., Gilchrist, C. L., Guilak, F. & Setton, L. A. Transfer of macroscale tissue strain to microscale cell regions in the deformed meniscus. Biophys. J. 95, 2116–2124 (2008).10.1529/biophysj.107.126938 ↗
10. Lai, J. H. & Levenston, M. E. Meniscus and cartilage exhibit distinct intra-tissue strain distributions under unconfined compression. Osteoarthritis Cartilage 18, 1291–1299 (2010).10.1016/j.joca.2010.05.020 ↗
11. Bruehlmann, S. B., Hulme, P. A. & Duncan, N. A. In situ intercellular mechanics of the bovine outer annulus fibrosus subjected to biaxial strains. J. Biomech. 37, 223–231 (2004).10.1016/S0021-9290(03)00244-6 ↗
12. Elliott, D. M. & Setton, L. A. Anisotropic and inhomogeneous tensile behavior of the human anulus fibrosus: experimental measurement and material model predictions. J. Biomech. Eng. 123, 256–263 (2001).10.1115/1.1374202 ↗
13. O’Connell, G. D., Guerin, H. L. & Elliott, D. M. Theoretical and uniaxial experimental evaluation of human annulus fibrosus degeneration. J. Biomech. Eng. 131, 111007 (2009).10.1115/1.3212104 ↗
14. Abraham, A. C., Edwards, C. R., Odegard, G. M. & Donahue, T. L. H. Regional and fiber orientation dependent shear properties and anisotropy of bovine meniscus. J. Mech. Behav. Biomed. Mater. 4, 2024–2030 (2011).10.1016/j.jmbbm.2011.06.022 ↗
15. Fang, F., Sawhney, A. S. & Lake, S. P. Different regions of bovine deep digital flexor tendon exhibit distinct elastic, but not viscous, mechanical properties under both compression and shear loading. J. Biomech. 47, 2869–2877 (2014).10.1016/j.jbiomech.2014.07.026 ↗
16. Han, W. M. et al. Impact of cellular microenvironment and mechanical perturbation on calcium signalling in meniscus fibrochondrocytes. Eur. Cell Mater. 27, 321–331 (2014).10.22203/eCM.v027a23 ↗
17. Fang, F. & Lake, S. P. Multiscale strain analysis of tendon subjected to shear and compression demonstrates strain attenuation, fiber sliding, and reorganization. J. Orthop. Res. 33, 1704–1712 (2015).10.1002/jor.22955 ↗
18. Malaviya, P. et al. An in vivo model for load-modulated remodeling in the rabbit flexor tendon. J. Orthop. Res. 18, 116–125 (2000).10.1002/jor.1100180117 ↗
19. Attia, M. et al. Alterations of overused supraspinatus tendon: a possible role of glycosaminoglycans and HARP/pleiotrophin in early tendon pathology. J. Orthop. Res. 30, 61–71 (2012).10.1002/jor.21479 ↗
20. Bell, R. et al. Controlled treadmill exercise eliminates chondroid deposits and restores tensile properties in a new murine tendinopathy model. J. Biomech. 46, 498–505 (2013).10.1016/j.jbiomech.2012.10.020 ↗
21. Bell, R. et al. ADAMTS5 is required for biomechanically-stimulated healing of murine tendinopathy. J. Orthop. Res. 31, 1540–1548 (2013).10.1002/jor.22398 ↗
22. Scott, A. et al. Increased versican content is associated with tendinosis pathology in the patellar tendon of athletes with jumper’s knee. Scand. J. Med. Sci. Sports 18, 427–435 (2008).10.1111/j.1600-0838.2007.00735.x ↗
23. Wang, V. M. et al. Murine tendon function is adversely affected by aggrecan accumulation due to the knockout of ADAMTS5. J. Orthop. Res. 30, 620–626 (2012).10.1002/jor.21558 ↗
24. Szczesny, S. E. & Elliott, D. M. Interfibrillar shear stress is the loading mechanism of collagen fibrils in tendon. Acta Biomater. 10, 2582–2590 (2014).10.1016/j.actbio.2014.01.032 ↗
25. Chahine, N. O., Wang, C. C.-B., Hung, C. T. & Ateshian, G. A. Anisotropic strain-dependent material properties of bovine articular cartilage in the transitional range from tension to compression. J. Biomech. 37, 1251–1261 (2004).10.1016/j.jbiomech.2003.12.008 ↗
26. Ateshian, G. A., Rajan, V., Chahine, N. O., Canal, C. E. & Hung, C. T. Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. J. Biomech. Eng. 131, 061003 (2009).10.1115/1.3118773 ↗
27. Canal Guterl, C., Hung, C. T. & Ateshian, G. A. Electrostatic and non-electrostatic contributions of proteoglycans to the compressive equilibrium modulus of bovine articular cartilage. J. Biomech. 43, 1343–1350 (2010).10.1016/j.jbiomech.2010.01.021 ↗
28. Baker, B. M., Nerurkar, N. L., Burdick, J. A., Elliott, D. M. & Mauck, R. L. Fabrication and modeling of dynamic multipolymer nanofibrous scaffolds. J. Biomech. Eng. 131, 101012 (2009).10.1115/1.3192140 ↗
29. Raj, A. & Tyagi, S. Detection of individual endogenous RNA transcripts in situ using multiple singly labeled probes. Methods Enzymol. 472, 365–386 (2010).10.1016/S0076-6879(10)72004-8 ↗
30. Raj, A., van den Bogaard, P., Rifkin, S. A., van Oudenaarden, A. & Tyagi, S. Imaging individual mRNA molecules using multiple singly labeled probes. Nature Methods 5, 877–879 (2008).10.1038/nmeth.1253 ↗
31. Plaas, A. et al. Biochemical identification and immunolocalizaton of aggrecan, ADAMTS5 and inter-alpha-trypsin-inhibitor in equine degenerative suspensory ligament desmitis. J. Orthop. Res. 29, 900–906 (2011).10.1002/jor.21332 ↗
32. Asai, S. et al. Tendon progenitor cells in injured tendons have strong chondrogenic potential: the CD105-negative subpopulation induces chondrogenic degeneration. Stem Cells Dayt. Ohio 32, 3266–3277 (2014).10.1002/stem.1847 ↗
33. Heo, S.-J. et al. Fiber stretch and reorientation modulates mesenchymal stem cell morphology and fibrous gene expression on oriented nanofibrous microenvironments. Ann. Biomed. Eng. 39, 2780–2790 (2011).10.1007/s10439-011-0365-7 ↗
34. Mauck, R. L., Yuan, X. & Tuan, R. S. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 14, 179–189 (2006).10.1016/j.joca.2005.09.002 ↗
35. Mauck, R. L., Martinez-Diaz, G. J., Yuan, X. & Tuan, R. S. Regional multilineage differentiation potential of meniscal fibrochondrocytes: implications for meniscus repair. Anat. Rec. 290, 48–58 (2007).10.1002/ar.20419 ↗
36. Qu, F. et al. Repair of dense connective tissues via biomaterial-mediated matrix reprogramming of the wound interface. Biomaterials 39, 85–94 (2015).10.1016/j.biomaterials.2014.10.067 ↗
37. Kim, D. H., Martin, J. T., Elliott, D. M., Smith, L. J. & Mauck, R. L. Phenotypic stability, matrix elaboration and functional maturation of nucleus pulposus cells encapsulated in photocrosslinkable hyaluronic acid hydrogels. Acta Biomater. 12, 21–29 (2015).10.1016/j.actbio.2014.10.030 ↗
38. Peltz, C. D., Perry, S. M., Getz, C. L. & Soslowsky, L. J. Mechanical properties of the long-head of the biceps tendon are altered in the presence of rotator cuff tears in a rat model. J. Orthop. Res. 27, 416–420 (2009).10.1002/jor.20770 ↗
39. Driscoll, T. P., Cosgrove, B. D., Heo, S.-J., Shurden, Z. E. & Mauck, R. L. Cytoskeletal to nuclear strain transfer regulates YAP signaling in mesenchymal stem cells. Biophys. J. 108, 2783–2793 (2015).10.1016/j.bpj.2015.05.010 ↗
40. Maas, S. A., Ellis, B. J., Ateshian, G. A. & Weiss, J. A. FEBio: finite elements for biomechanics. J. Biomech. Eng. 134, 011005 (2012).10.1115/1.4005694 ↗
41. Jacobs, N. T., Cortes, D. H., Vresilovic, E. J. & Elliott, D. M. Biaxial tension of fibrous tissue: using finite element methods to address experimental challenges arising from boundary conditions and anisotropy. J. Biomech. Eng. 135, 021004 (2013).10.1115/1.4023503 ↗