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Decorin-containing collagen hydrogels as dimensionally stable scaffolds to study the effects of compressive mechanical loading on angiogenesis

Published online by Cambridge University Press:  20 July 2017

Marissa A. Ruehle ,
Laxminarayanan Krishnan ,
Steven A. LaBelle ,
Nick J. Willett ,
Jeffrey A. Weiss  and
Robert E. Guldberg
Marissa A. Ruehle
Affiliation:
Georgia Institute of Technology, Petit Institute for Bioengineering and Biosciences, Atlanta, GA, USA Emory University, Atlanta, GA, USA
Laxminarayanan Krishnan
Affiliation:
Georgia Institute of Technology, Petit Institute for Bioengineering and Biosciences, Atlanta, GA, USA
Steven A. LaBelle
Affiliation:
University of Utah, Salt Lake City, UT, USA
Nick J. Willett
Affiliation:
Georgia Institute of Technology, Petit Institute for Bioengineering and Biosciences, Atlanta, GA, USA Emory University, Atlanta, GA, USA Atlanta Veteran's Affairs Medical Center, Decatur, GA, USA
Jeffrey A. Weiss
Affiliation:
University of Utah, Salt Lake City, UT, USA
Robert E. Guldberg*
Affiliation:
Georgia Institute of Technology, Petit Institute for Bioengineering and Biosciences, Atlanta, GA, USA
*
Address all correspondence to R. E. Guldberg at robert.guldberg@me.gatech.edu
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Abstract

Angiogenesis is a critical component during wound healing, and the process is sensitive to mechanical stimuli. Current in vitro culture environments used to investigate three-dimensional microvascular growth often lack dimensional stability and the ability to withstand compression. We investigated the ability of decorin (DCN), a proteoglycan known to modulate collagen fibrillogenesis, incorporated into a collagen hydrogel to increase construct dimensional stability while maintaining vascular growth. DCN did not affect microvascular growth parameters, while increasing the compressive modulus of collagen gels and significantly reducing the contraction of 3% collagen gels after 16 days in culture.

Type
Biomaterials for 3D Cell Biology Research Letters
Information
MRS Communications , Volume 7 , Issue 3 , September 2017 , pp. 466 - 471
Copyright
Copyright © Materials Research Society 2017 

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References

1.Chien, S.: Effects of disturbed flow on endothelial cells. Ann. Biomed. Eng. 36, 554 (2008).Google Scholar
2.Filipowska, J., Tomaszewski, K.A., Niedzwiedzki, L., Walocha, J.A. and Niedzwiedzki, T.: The role of vasculature in bone development, regeneration and proper systemic functioning. Angiogenesis (2017). PMID: 28194536, doi: 10.1007/s10456-017-9541-1.Google Scholar
3.Lafage-Proust, M.H., Roche, B., Langer, M., Cleret, D., Vanden Bossche, A., Olivier, T. and Vico, L.: Assessment of bone vascularization and its role in bone remodeling. BoneKEy Rep. 4, 662 (2015).Google Scholar
4.Boerckel, J.D., Uhrig, B.A., Willett, N.J., Huebsch, N. and Guldberg, R.E.: Mechanical regulation of vascular growth and tissue regeneration in vivo. Proc. Natl. Acad. Sci. U.S.A. 108, E674 (2011).Google Scholar
5.Hoying, J.B., Boswell, C.A. and Williams, S.K.: Angiogenic potential of microvessel fragments established in three-dimensional collagen gels. In vitro Cell. Dev. Biol. Anim. 32, 409 (1996).Google Scholar
6.Krishnan, L., Underwood, C.J., Maas, S., Ellis, B.J., Kode, T.C., Hoying, J.B. and Weiss, J.A.: Effect of mechanical boundary conditions on orientation of angiogenic microvessels. Cardiovasc. Res. 78, 324 (2008).Google Scholar
7.Edgar, L.T., Hoying, J.B., Utzinger, U., Underwood, C.J., Krishnan, L., Baggett, B.K., Maas, S.A., Guilkey, J.E. and Weiss, J.A.: Mechanical interaction of angiogenic microvessels with the extracellular matrix. J. Biomech. Eng. 136, 021001 (2014).Google Scholar
8.Edgar, L.T., Underwood, C.J., Guilkey, J.E., Hoying, J.B. and Weiss, J.A.: Extracellular matrix density regulates the rate of neovessel growth and branching in sprouting angiogenesis. PLoS ONE 9, e85178 (2014).Google Scholar
9.Huang-Lee, L.L., Cheung, D.T. and Nimni, M.E.: Biochemical changes and cytotoxicity associated with the degradation of polymeric glutaraldehyde derived crosslinks. J. Biomed. Mater. Res. 24, 1185 (1990).Google Scholar
10.Vogel, K.G. and Trotter, J.A.: The effect of proteoglycans on the morphology of collagen fibrils formed in vitro. Coll. Relat. Res. 7, 105 (1987).Google Scholar
11.Danielson, K.G., Baribault, H., Holmes, D.F., Graham, H., Kadler, K.E. and Iozzo, R.V.: Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136, 729 (1997).Google Scholar
12.Robinson, P.S., Huang, T.F., Kazam, E., Iozzo, R.V., Birk, D.E. and Soslowsky, L.J.: Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. J. Biomech. Eng. 127, 181 (2005).Google Scholar
13.Pins, G.D., Christiansen, D.L., Patel, R. and Silver, F.H.: Self-assembly of collagen fibers. Influence of fibrillar alignment and decorin on mechanical properties. Biophys. J. 73, 2164 (1997).Google Scholar
14.Reese, S.P., Underwood, C.J. and Weiss, J.A.: Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Biol. 32, 414 (2013).Google Scholar
15.Choi, H.U., Johnson, T.L., Pal, S., Tang, L.H., Rosenberg, L. and Neame, P.J.: Characterization of the dermatan sulfate proteoglycans, DS-PGI and DS-PGII, from bovine articular cartilage and skin isolated by octyl-sepharose chromatography. J. Biol. Chem. 264, 2876 (1989).Google Scholar
16.Krishnan, L., Hoying, J.B., Nguyen, H., Song, H. and Weiss, J.A.: Interaction of angiogenic microvessels with the extracellular matrix. Am. J. Physiol. Heart Circ. Physiol. 293, H3650 (2007).Google Scholar
17.Bouletreau, P.J., Warren, S.M., Spector, J.A., Peled, Z.M., Gerrets, R.P., Greenwald, J.A. and Longaker, M.T.: Hypoxia and VEGF up-regulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plastic Reconstr. Surg. 109, 2384 (2002).Google Scholar
18.Suzuki, Y., Montagne, K., Nishihara, A., Watabe, T. and Miyazono, K.: BMPs promote proliferation and migration of endothelial cells via stimulation of VEGF-A/VEGFR2 and angiopoietin-1/Tie2 signalling. J. Biochem. 143, 199 (2008).Google Scholar
19.Davies Cde, L., Melder, R.J., Munn, L.L., Mouta-Carreira, C., Jain, R.K. and Boucher, Y.: Decorin inhibits endothelial migration and tube-like structure formation: role of thrombospondin-1. Microvasc. Res. 62, 26 (2001).Google Scholar
20.Zhang, Z., Garron, T., Li, X.J., Liu, Y., Zhang, X., Li, Y.Y. and Xu, W.S.: Recombinant human decorin inhibits TGF-b1 induced contraction of collagen lattice by keloid fibroblasts. Wounds 21, 47 (2009).Google Scholar
21.Zhang, Z., Garron, T.M., Li, X.J., Liu, Y., Zhang, X., Li, Y.Y. and Xu, W.S.: Recombinant human decorin inhibits TGF-beta1-induced contraction of collagen lattice by hypertrophic scar fibroblasts. Burns 35, 527 (2009).Google Scholar
22.Paderi, J.E., Sistiabudi, R., Ivanisevic, A. and Panitch, A.: Collagen-binding peptidoglycans: a biomimetic approach to modulate collagen fibrillogenesis for tissue engineering applications. Tissue Eng. A 15, 2991 (2009).Google Scholar
23.Diamant, J., Keller, A., Baer, E., Litt, M. and Arridge, R.G.: Collagen; ultrastructure and its relation to mechanical properties as a function of ageing. Proc. R. Soc. Lond. B Biol. Sci. 180, 293 (1972).Google Scholar
24.Ingber, D.E. and Folkman, J.: Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J. Cell Biol. 109, 317 (1989).Google Scholar
25.Schonherr, E., Sunderkotter, C., Schaefer, L., Thanos, S., Grassel, S., Oldberg, A., Iozzo, R.V., Young, M.F. and Kresse, H.: Decorin deficiency leads to impaired angiogenesis in injured mouse cornea. J. Vasc. Res. 41, 499 (2004).Google Scholar
26.Grant, D.S., Yenisey, C., Rose, R.W., Tootell, M., Santra, M. and Iozzo, R.V.: Decorin suppresses tumor cell-mediated angiogenesis. Oncogene 21, 4765 (2002).Google Scholar
27.Jarvelainen, H.T., Iruela-Arispe, M.L., Kinsella, M.G., Sandell, L.J., Sage, E.H. and Wight, T.N.: Expression of decorin by sprouting bovine aortic endothelial cells exhibiting angiogenesis in vitro. Exp. Cell Res. 203, 395 (1992).Google Scholar
28.Santra, M., Santra, S., Zhang, J. and Chopp, M.: Ectopic decorin expression up-regulates VEGF expression in mouse cerebral endothelial cells via activation of the transcription factors Sp1, HIF1alpha, and Stat3. J. Neurochem. 105, 324 (2008).Google Scholar
29.Hildebrand, A., Romaris, M., Rasmussen, L.M., Heinegard, D., Twardzik, D.R., Border, W.A. and Ruoslahti, E.: Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem. J. 302(Pt 2), 527 (1994).Google Scholar
30.Ferdous, Z., Wei, V.M., Iozzo, R., Hook, M. and Grande-Allen, K.J.: Decorin-transforming growth factor- interaction regulates matrix organization and mechanical characteristics of three-dimensional collagen matrices. J. Biol. Chem. 282, 35887 (2007).Google Scholar