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Oligomers Modulate Interfibril Branching and Mass Transport Properties of Collagen Matrices

Published online by Cambridge University Press:  10 July 2013

Catherine F. Whittington ,
Eric Brandner ,
Ka Yaw Teo ,
Bumsoo Han ,
Eric Nauman  and
Sherry L. Voytik-Harbin
Catherine F. Whittington
Affiliation:
Weldon School of Biomedical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA
Eric Brandner
Affiliation:
Weldon School of Biomedical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA
Ka Yaw Teo
Affiliation:
School of Mechanical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA
Bumsoo Han
Affiliation:
Weldon School of Biomedical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA School of Mechanical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA
Eric Nauman
Affiliation:
Weldon School of Biomedical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA School of Mechanical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA Department of Basic Medical Sciences, School of Veterinary Medicine, Purdue University, West Lafayette, IN 47907, USA
Sherry L. Voytik-Harbin*
Affiliation:
Weldon School of Biomedical Engineering, College of Engineering, Purdue University, West Lafayette, IN 47907, USA Department of Basic Medical Sciences, School of Veterinary Medicine, Purdue University, West Lafayette, IN 47907, USA
*
*Corresponding author. E-mail: harbins@purdue.edu
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Abstract

Mass transport within collagen-based matrices is critical to tissue development, repair, and pathogenesis, as well as the design of next-generation tissue engineering strategies. This work shows how collagen precursors, specified by intermolecular cross-link composition, provide independent control of collagen matrix mechanical and transport properties. Collagen matrices were prepared from tissue-extracted monomers or oligomers. Viscoelastic behavior was measured in oscillatory shear and unconfined compression. Matrix permeability and diffusivity were measured using gravity-driven permeametry and integrated optical imaging, respectively. Both collagen types showed an increase in stiffness and permeability hindrance with increasing collagen concentration (fibril density); however, different physical property–concentration relationships were noted. Diffusivity was not affected by concentration for either collagen type over the range tested. In general, oligomer matrices exhibited a substantial increase in stiffness and only a modest decrease in transport properties when compared with monomer matrices prepared at the same concentration. The observed differences in viscoelastic and transport properties were largely attributed to increased levels of interfibril branching within oligomer matrices. The ability to relate physical properties to relevant microstructure parameters, including fibril density and interfibril branching, is expected to advance the understanding of cell–matrix signaling, as well as facilitate model-based prediction and design of matrix-based therapeutic strategies.

Keywords

collagen matrixoligomermonomermass transportpermeabilitydiffusivity
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 5 , October 2013 , pp. 1323 - 1333
Copyright
Copyright © Microscopy Society of America 2013 

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References

Axelrod, D., Koppel, D.E., Schlessinger, J., Elson, E. & Webb, W.W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 16, 1055–1069.Google Scholar
Bailey, J.L., Critser, P.J., Whittington, C., Kuske, J.L., Yoder, M.C. & Voytik-Harbin, S.L. (2011). Collagen oligomers modulate physical and biological properties of three-dimensional self-assembled matrices. Biopolymers 95, 77–93.Google Scholar
Beatty, M.W., Ojha, A.K., Cook, J.L., Alberts, L.R., Mahanna, G.K., Iwasaki, L.R. & Nickel, J.C. (2002). Small intestinal submucosa versus salt-extracted polyglycolic acid-poly-l-lactic acid: A comparison of neocartilage formed in two scaffold materials. Tissue Eng 8, 955–968.CrossRefGoogle ScholarPubMed
Brennan, M. & Davison, P.F. (1980). Role of aldehydes in collagen fibrillogenesis in vitro . Biopolymers 19, 1861–1873.Google Scholar
Brightman, A.O., Rajwa, B.P., Sturgis, J.E., McCallister, M.E., Robinson, J.P. & Voytik-Harbin, S.L. (2000). Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro . Biopolymers 54, 222–234.Google Scholar
Carman, P.C. (1937). Fluid flow through granular beds. Trans Inst Chem Eng 15, 150–166.Google Scholar
Critser, P.J., Kreger, S.T., Voytik-Harbin, S.L. & Yoder, M.C. (2010). Collagen matrix physical properties modulate endothelial colony forming cell-derived vessels in vivo . Microvasc Res 80, 23–30.Google Scholar
Deorosan, B. & Nauman, E.A. (2011). The role of glucose, serum, and three-dimensional cell culture on the metabolism of bone marrow-derived mesenchymal stem cells. Stem Cells Int 2011, 429187. Google Scholar
De Rosa, E., Borselli, C. & Netti, P.A. (2006). Transport of large molecules in hyaluronic acid-based membranes and solution. JMembr Sci 273, 84–88.CrossRefGoogle Scholar
Diamond, S.L. (1999). Engineering design of optimal strategies for blood clot dissolution. Annu Rev Biomed Eng 1, 427–462.Google Scholar
Discher, D., Dong, C., Fredberg, J.J., Guilak, F., Ingber, D., Janmey, P., Kamm, R.D., Schmid-Schonbein, G.W. & Weinbaum, S. (2009). Biomechanics: Cell research and applications for the next decade. Ann Biomed Eng 37, 847–859.Google Scholar
Erikson, A., Andersen, H.N., Naess, S.N., Sikorski, P. & Davies Cde, L. (2008). Physical and chemical modifications of collagen gels: Impact on diffusion. Biopolymers 89, 135–143.Google Scholar
Eyre, D.R. & Wu, J.J. (2005). Collagen cross-links. Top Curr Chem 247, 207–229.CrossRefGoogle Scholar
Gentleman, E., Nauman, E.A., Dee, K.C. & Livesay, G.A. (2004). Short collagen fibers provide control of contraction and permeability in fibroblast-seeded collagen gels. Tissue Eng 10, 421–427.Google Scholar
Gjorevski, N. & Nelson, C.M. (2010). The mechanics of development: Models and methods for tissue morphogenesis. Birth Defects Res C Embryo Today 90, 193–202.Google Scholar
Happel, J. & Brenner, H. (1965). Low Reynolds Number Hydrodynamics. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
Johnson, E.M. & Deen, W.M. (1996). Hydraulic permeability of agarose gels. AIChE J 42, 1220–1224.Google Scholar
Kadler, K.E., Holmes, D.F., Trotter, J.A. & Chapman, J.A. (1996). Collagen fibril formation. Biochem J 316, 1–11.Google Scholar
Knott, L., Tarlton, J.F. & Bailey, A.J. (1997). Chemistry of collagen cross-linking: Biochemical changes in collagen during the partial mineralization of turkey leg tendon. Biochem J 322(Pt 2), 535–542.Google Scholar
Kosto, K.B. & Deen, W.M. (2004). Diffusivities of macromolecules in composite hydrogels. AIChE J 50, 2548–2658.Google Scholar
Kreger, S.T., Bell, B.J., Bailey, J., Stites, E., Kuske, J., Waisner, B. & Voytik-Harbin, S.L. (2010). Polymerization and matrix physical properties as important design considerations for soluble collagen formulations. Biopolymers 93, 690–707.Google Scholar
Kreger, S.T. & Voytik-Harbin, S.L. (2009). Hyaluronan concentration within a 3D collagen matrix modulates matrix viscoelasticity, but not fibroblast response. Matrix Biol 28, 336–346.CrossRefGoogle Scholar
Kuznetsova, N. & Leikin, S. (1999). Does the triple helical domain of type I collagen encode molecular recognition and fiber assembly while telopeptides serve as catalytic domains? Effect of proteolytic cleavage on fibrillogenesis and on collagen-collagen interaction in fibers. J Biol Chem 274, 36083–36088.Google Scholar
Leddy, H.A., Awad, H.A. & Guilak, F. (2004). Molecular diffusion in tissue-engineered cartilage constructs: Effects of scaffold material, time, and culture conditions. J Biomed Mater Res B Appl Biomater 70, 397–406.Google Scholar
Leddy, H.A. & Guilak, F. (2003). Site-specific molecular diffusion in articular cartilage measured using fluorescence recovery after photobleaching. Ann Biomed Eng 31, 753–760.Google Scholar
Lehner, F.K. (1979). On the validity of Fick's law for transient diffusion through a porous medium. Chem Eng Sci 34, 821–825.Google Scholar
Levick, J.R. (1987). Flow through interstitium and other fibrous matrices. Q J Exp Physiol 72, 409–437.Google Scholar
Li, G.P., Bronk, J.T., An, K.N. & Kelly, P.J. (1987). Permeability of cortical bone of canine tibiae. Microvasc Res 34, 302–310.Google Scholar
Maroudas, A. (1970). Distribution and diffusion of solutes in articular cartilage. Biophys J 10, 365–379.Google Scholar
Mechanic, G.L., Katz, E.P., Henmi, M., Noyes, C. & Yamauchi, M. (1987). Locus of a histidine-based, stable trifunctional, helix to helix collagen cross-link: Stereospecific collagen structure of type I skin fibrils. Biochemistry 26, 3500–3509.Google Scholar
Netti, P.A., Berk, D.A., Swartz, M.A., Grodzinsky, A.J. & Jain, R.K. (2000). Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60, 2497–2503.Google Scholar
Nicholson, C. & Tao, L. (1993). Hindered diffusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging. Biophys J 65, 2277–2290.Google Scholar
O'Brien, F.J., Harley, B.A., Waller, M.A., Yannas, I.V., Gibson, L.J. & Prendergast, P.J. (2007). The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol Health Care 15, 3–17.CrossRefGoogle ScholarPubMed
Ogston, A.G., Preston, B.N. & Wells, J.D. (1973). On the transport of compact particles through solutions of chain-polymers. Proc R Soc Lond A 333, 297–316.Google Scholar
Pizzo, A.M., Kokini, K., Vaughn, L.C., Waisner, B.Z. & Voytik-Harbin, S.L. (2005). Extracellular matrix (ECM) microstructural composition regulates local cell-ECM biomechanics and fundamental fibroblast behavior: A multidimensional perspective. J Appl Physiol 98, 1909–1921.CrossRefGoogle ScholarPubMed
Proctor, C.S., Schmidt, M.B., Whipple, R.R., Kelly, M.A. & Mow, V.C. (1989). Material properties of the normal medial bovine meniscus. J Orthop Res 7, 771–782.Google Scholar
Ramanujan, S., Pluen, A., McKee, T.D., Brown, E.B., Boucher, Y. & Jain, R.K. (2002). Diffusion and convection in collagen gels: Implications for transport in the tumor interstitium. Biophys J 83, 1650–1660.Google Scholar
Roeder, B.A., Kokini, K., Sturgis, J.E., Robinson, J.P. & Voytik-Harbin, S.L. (2002). Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 124, 214–222.Google Scholar
Roeder, B.A., Kokini, K. & Voytik-Harbin, S.L. (2009). Fibril microstructure affects strain transmission within collagen extracellular matrices. J Biomech Eng 131, 031004. Google Scholar
Sacks, M.S. & Sun, W. (2003). Multiaxial mechanical behavior of biological materials. Annu Rev Biomed Eng 5, 251–284.CrossRefGoogle ScholarPubMed
Sander, E.A. & Barocas, V.H. (2008). Biomimetic collagen tissues: collagenous tissue engineering and other applications. In Collagen: Structure and Mechanics, Fratzl, P. (Ed.). pp. 475–504. New York: Springer Science+Business Media, LLC.Google Scholar
Serpooshan, V., Julien, M., Nguyen, O., Wang, H., Li, A., Muja, N., Henderson, J.E. & Nazhat, S.N. (2010). Reduced hydraulic permeability of three-dimensional collagen scaffolds attenuates gel contraction and promotes the growth and differentiation of mesenchymal stem cells. Acta Biomater 6, 3978–3987.Google Scholar
Silver, F.H. & Landis, W.J. (2008). Viscoelastiticy, energy storage and transmission and dissipation by extracellular matrices in vertebrates. In Collagen Structure and Mechanics, Fratzl, P. (Ed.), pp. 133–154. New York: Springer.Google Scholar
Stewart, J.M., Schultz, D.S., Lee, O.T. & Trinidad, M.L. (2009). Exogenous collagen cross-linking reduces scleral permeability: Modeling the effects of age-related cross-link accumulation. Invest Ophthalmol Vis Sci 50, 352–357.Google Scholar
Susilo, M.E., Roeder, B.A., Voytik-Harbin, S.L., Kokini, K. & Nauman, E.A. (2010). Development of a three-dimensional unit cell to model the micromechanical response of a collagen-based extracellular matrix. Acta Biomater 6, 1471–1486.Google Scholar
Swartz, M.A. & Fleury, M.E. (2007). Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng 9, 229–256.Google Scholar
Travascio, F., Jackson, A.R., Brown, M.D. & Gu, W.Y. (2009). Relationship between solute transport properties and tissue morphology in human annulus fibrosus. J Orthop Res 27, 1625–1630.CrossRefGoogle ScholarPubMed
Voytik-Harbin, S.L., Rajwa, B. & Robinson, J.P. (2001). Three-dimensional imaging of extracellular matrix and extracellular matrix-cell interactions. Methods Cell Biol 63, 583–597.Google Scholar
Yamauchi, M., Chandler, G.S., Tanzawa, H. & Katz, E.P. (1996). Cross-linking and the molecular packing of corneal collagen. Biochem Biophys Res Commun 219, 311–315.CrossRefGoogle ScholarPubMed
Yamauchi, M., London, R.E., Guenat, C., Hashimoto, F. & Mechanic, G.L. (1987). Structure and formation of a stable histidine-based trifunctional cross-link in skin collagen. J Biol Chem 262, 11428–11434.Google Scholar

Whittington Supplementary Material

Supplementary Movie 1. Confocal image stacks for monomer (A, B) and oligomer (C, D) matrices (1.5 mg/mL) collected in combined immunofluorescence and backscattered (reflected) light. Animations show image slice collection (XY plane) at 0.10 um increments through a thickness (A, C) and rotations of reconstructed 3D images (B, D).

Download Whittington Supplementary Material(Video)
Video 1.2 MB

Whittington Supplementary Material

Supplementary Movie 1. Confocal image stacks for monomer (A, B) and oligomer (C, D) matrices (1.5 mg/mL) collected in combined immunofluorescence and backscattered (reflected) light. Animations show image slice collection (XY plane) at 0.10 um increments through a thickness (A, C) and rotations of reconstructed 3D images (B, D).

Download Whittington Supplementary Material(Video)
Video 7.9 MB

Whittington Supplementary Material

Supplementary Movie 1. Confocal image stacks for monomer (A, B) and oligomer (C, D) matrices (1.5 mg/mL) collected in combined immunofluorescence and backscattered (reflected) light. Animations show image slice collection (XY plane) at 0.10 um increments through a thickness (A, C) and rotations of reconstructed 3D images (B, D).

Download Whittington Supplementary Material(Video)
Video 1.4 MB

Whittington Supplementary Material

Supplementary Movie 1. Confocal image stacks for monomer (A, B) and oligomer (C, D) matrices (1.5 mg/mL) collected in combined immunofluorescence and backscattered (reflected) light. Animations show image slice collection (XY plane) at 0.10 um increments through a thickness (A, C) and rotations of reconstructed 3D images (B, D).

Download Whittington Supplementary Material(Video)
Video 7.5 MB