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Age-Dependent Expression of Collagen Receptors and Deformation of Type I Collagen Substrates by Rat Cardiac Fibroblasts

Published online by Cambridge University Press:  11 July 2011

Christopher G. Wilson
Affiliation:
University of South Carolina School of Medicine, Department of Cell Biology & Anatomy, 6439 Garners Ferry Road, Columbia, SC 29209, USA
John W. Stone
Affiliation:
University of South Carolina, Department of Chemistry & Biochemistry, 631 Sumter St., Columbia, SC 29208, USA
Vennece Fowlkes
Affiliation:
University of South Carolina School of Medicine, Department of Cell Biology & Anatomy, 6439 Garners Ferry Road, Columbia, SC 29209, USA
Mary O. Morales
Affiliation:
University of South Carolina School of Medicine, Department of Cell Biology & Anatomy, 6439 Garners Ferry Road, Columbia, SC 29209, USA
Catherine J. Murphy
Affiliation:
University of Illinois at Urbana-Champaign, Department of Chemistry, A512 Chemical & Life Sciences Laboratory, 600 South Mathews Ave., Urbana, IL 61801, USA
Sarah C. Baxter
Affiliation:
University of South Carolina, Department of Mechanical Engineering, 300 Main St., Columbia, SC 29208, USA
Edie C. Goldsmith*
Affiliation:
University of South Carolina School of Medicine, Department of Cell Biology & Anatomy, 6439 Garners Ferry Road, Columbia, SC 29209, USA
*
Corresponding author. E-mail: edie.goldsmith@uscmed.sc.edu
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Abstract

Little is known about how age influences the ways in which cardiac fibroblasts interact with the extracellular matrix. We investigated the deformation of collagen substrates by neonatal and adult rat cardiac fibroblasts in monolayer and three-dimensional (3D) cultures, and quantified the expression of three collagen receptors [discoidin domain receptor (DDR)1, DDR2, and β1 integrin] and the contractile protein alpha smooth muscle actin (α-SMA) in these cells. We report that adult fibroblasts contracted 3D collagen substrates significantly less than their neonate counterparts, whereas no differences were observed in monolayer cultures. Adult cells had lower expression of β1 integrin and α-SMA than neonate cultures, and we detected significant correlations between the expression of α-SMA and each of the collagen receptors in neonate cells but not in adult cells. Consistent with recent work demonstrating age-dependent interactions with myocytes, our results indicate that interactions between cardiac fibroblasts and the extracellular matrix change with age.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2011

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References

REFERENCES

Arora, P.D. & McCulloch, C.A. (1994). Dependence of collagen remodelling on alpha-smooth muscle actin expression by fibroblasts. J Cell Physiol 159, 161175.CrossRefGoogle ScholarPubMed
Arora, P.D., Narani, N. & McCulloch, C.A. (1999). The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts. Am J Pathol 154, 871882.CrossRefGoogle ScholarPubMed
Banerjee, I., Fuseler, J.W., Price, R.L., Borg, T.K. & Baudino, T.A. (2007). Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 293, H1883H1891.Google Scholar
Baudino, T.A., Carver, W., Giles, W. & Borg, T.K. (2006). Cardiac fibroblasts: Friend or foe? Am J Physiol Heart Circ Physiol 291, H1015H1026.CrossRefGoogle ScholarPubMed
Baxter, S.C., Morales, M.O. & Goldsmith, E.C. (2008). Adaptive changes in cardiac fibroblast morphology and collagen organization as a result of mechanical environment. Cell Biochem Biophys 51, 3344.CrossRefGoogle ScholarPubMed
Burgess, M.L., Carver, W.E., Terracio, L., Wilson, S.P., Wilson, M.A. & Borg, T.K. (1994). Integrin-mediated collagen gel contraction by cardiac fibroblasts. Effects of angiotensin II. Circ Res 74, 291298.Google Scholar
Carver, W., Molano, I., Reaves, T.A., Borg, T.K. & Terracio, L. (1995). Role of the alpha 1 beta 1 integrin complex in collagen gel contraction in vitro by fibroblasts. J Cell Physiol 165, 425437.CrossRefGoogle ScholarPubMed
Chan, M.W., Arora, P.D., Bozavikov, P. & McCulloch, C.A. (2009). FAK, PIP5KIgamma and gelsolin cooperatively mediate force-induced expression of alpha-smooth muscle actin. J Cell Sci 122, 27692781.CrossRefGoogle ScholarPubMed
Cukierman, E., Pankov, R., Stevens, D.R. & Yamada, K.M. (2001). Taking cell-matrix adhesions to the third dimension. Science 294, 17081712.Google Scholar
Engler, A., Bacakova, L., Newman, C., Hategan, A., Griffin, M. & Discher, D. (2004). Substrate compliance versus ligand density in cell on gel responses. Biophys J 86, 617628.CrossRefGoogle ScholarPubMed
Engler, A.J., Carag-Krieger, C., Johnson, C.P., Raab, M., Tang, H.Y., Speicher, D.W., Sanger, J.W., Sanger, J.M. & Discher, D.E. (2008). Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: Scar-like rigidity inhibits beating. J Cell Sci 121, 37943802.CrossRefGoogle Scholar
Engler, A.J., Sen, S., Sweeney, H.L. & Discher, D.E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677689.CrossRefGoogle ScholarPubMed
Fernandez, P. & Bausch, A.R. (2009). The compaction of gels by cells: A case of collective mechanical activity. Integr Biol (Camb) 1, 252259.CrossRefGoogle Scholar
Flamant, M., Placier, S., Rodenas, A., Curat, C.A., Vogel, W.F., Chatziantoniou, C. & Dussaule, J.C. (2006). Discoidin domain receptor 1 null mice are protected against hypertension-induced renal disease. J Am Soc Nephrol 17, 33743381.CrossRefGoogle ScholarPubMed
Goldsmith, E.C., Hoffman, A., Morales, M.O., Potts, J.D., Price, R.L., McFadden, A., Rice, M. & Borg, T.K. (2004). Organization of fibroblasts in the heart. Dev Dyn 230, 787794.Google Scholar
Goldsmith, E.C., Zhang, X., Watson, J., Hastings, J. & Potts, J.D. (2010). The collagen receptor DDR2 is expressed during early cardiac development. Anat Rec (Hoboken) 293(5), 762769.CrossRefGoogle ScholarPubMed
Grove, D., Zak, R., Nair, K.G. & Aschenbrenner, V. (1969). Biochemical correlates of cardiac hypertrophy. IV. Observations on the cellular organization of growth during myocardial hypertrophy in the rat. Circ Res 25, 473485.CrossRefGoogle ScholarPubMed
Hinz, B., Celetta, G., Tomasek, J.J., Gabbiani, G. & Chaponnier, C. (2001). Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12, 27302741.Google Scholar
Hou, G., Vogel, W.F. & Bendeck, M.P. (2002). Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ Res 90, 11471149.Google Scholar
Ieda, M., Tsuchihashi, T., Ivey, K.N., Ross, R.S., Hong, T.T., Shaw, R.M. & Srivastava, D. (2009). Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 16, 233244.Google Scholar
Jana, N.R., Gearheart, L. & Murphy, C.J. (2001a). Seed-mediated growth approach for shape-controlled synthesis of spheroidal and rod-like gold nanoparticles using a surfactant template. Adv Mater 13, 13891393.3.0.CO;2-F>CrossRefGoogle Scholar
Jana, N.R., Gearheart, L. & Murphy, C.J. (2001b). Wet chemical synthesis of high aspect ratio cylindrical gold nanorods. J Phys Chem B 105, 40654067.Google Scholar
Knezevic, V., Sim, A.J., Borg, T.K. & Holmes, J.W. (2002). Isotonic biaxial loading of fibroblast-populated collagen gels: A versatile, low–cost system for the study of mechanobiology. Biomech Model Mechanobiol 1, 5967.Google Scholar
Lijnen, P., Petrov, V. & Fagard, R. (2003). Transforming growth factor-beta 1-mediated collagen gel contraction by cardiac fibroblasts. J Renin Angiotensin Aldosterone Syst 4, 113118.Google Scholar
Matsuyama, W., Watanabe, M., Shirahama, Y., Oonakahara, K., Higashimoto, I., Yoshimura, T., Osame, M. & Arimura, K. (2005). Activation of discoidin domain receptor 1 on CD14-positive bronchoalveolar lavage fluid cells induces chemokine production in idiopathic pulmonary fibrosis. J Immunol 174, 64906498.CrossRefGoogle ScholarPubMed
Morales, M.O., Price, R.L. & Goldsmith, E.C. (2005). Expression of discoidin domain receptor 2 (DDR2) in the developing heart. Microsc Microanal 11, 260267.Google Scholar
Olaso, E., Ikeda, K., Eng, F.J., Xu, L., Wang, L.H., Lin, H.C. & Friedman, S.L. (2001). DDR2 receptor promotes MMP-2-mediated proliferation and invasion by hepatic stellate cells. J Clin Invest 108, 13691378.CrossRefGoogle ScholarPubMed
Olaso, E., Labrador, J.P., Wang, L., Ikeda, K., Eng, F.J., Klein, R., Lovett, D.H., Lin, H.C. & Friedman, S.L. (2002). Discoidin domain receptor 2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem 277, 36063613.CrossRefGoogle ScholarPubMed
Orendorff, C.J., Baxter, S.C., Goldsmith, E.C. & Murphy, C.J. (2005). Light scattering from gold nanorods: Tracking material deformation. Nanotechnology 16, 16012605.CrossRefGoogle Scholar
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.CrossRefGoogle ScholarPubMed
Sadoshima, J. & Izumo, S. (1993). Molecular characterization of angiotensin II–induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ Res 73, 413423.CrossRefGoogle ScholarPubMed
Stone, J.W., Sisco, P.N., Goldsmith, E.C., Baxter, S.C. & Murphy, C.J. (2007). Using gold nanorods to probe cell-induced collagen deformation. Nano Lett 7, 116119.CrossRefGoogle ScholarPubMed
Villarreal, F.J., Kim, N.N., Ungab, G.D., Printz, M.P. & Dillmann, W.H. (1993). Identification of functional angiotensin II receptors on rat cardiac fibroblasts. Circulation 88, 28492861.Google Scholar
Vogel, W., Brakebusch, C., Fässler, R., Alves, F., Ruggiero, F. & Pawson, T. (2000). Discoidin domain receptor 1 is activated independently of beta(1) integrin. J Biol Chem 275, 57795784.CrossRefGoogle ScholarPubMed
Weber, K.T. & Brilla, C.G. (1993). Structural basis for pathologic left ventricular hypertrophy. Clin Cardiol 16, II10II14.CrossRefGoogle ScholarPubMed
Weber, K.T., Sun, Y., Tyagi, S.C. & Cleutjens, J.P. (1994). Collagen network of the myocardium: Function, structural remodeling and regulatory mechanisms. J Mol Cell Cardiol 26, 279292.CrossRefGoogle ScholarPubMed
Wilson, C.G., Sisco, P.N., Goldsmith, E.C. & Murphy, C.J. (2009). Glycosaminoglycan-functionalized gold nanorods: Interactions with cardiac cells and type I collagen. J Mater Chem 19, 63326340.CrossRefGoogle Scholar
Xu, L., Peng, H., Wu, D., Hu, K., Goldring, M.B., Olsen, B.R. & Li, Y. (2005). Activation of the discoidin domain receptor 2 induces expression of matrix metalloproteinase 13 associated with osteoarthritis in mice. J Biol Chem 280, 548555.CrossRefGoogle ScholarPubMed