Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T22:05:47.245Z Has data issue: false hasContentIssue false

Expression and Deposition of Fibrous Extracellular Matrix Proteins in Cardiac Valves during Chick Development

Published online by Cambridge University Press:  23 December 2010

Hong Tan
Affiliation:
Department of Cell Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, SC 29209, USA
Lorain Junor
Affiliation:
Department of Cell Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, SC 29209, USA
Robert L. Price
Affiliation:
Department of Cell Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, SC 29209, USA
Russell A. Norris
Affiliation:
Department of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA
Jay D. Potts
Affiliation:
Department of Cell Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, SC 29209, USA
Richard L. Goodwin*
Affiliation:
Department of Cell Biology and Anatomy, School of Medicine, University of South Carolina, Columbia, SC 29209, USA
*
Corresponding author. E-mail: Richard.Goodwin@uscmed.sc.edu
Get access

Abstract

Extracellular matrix (ECM) plays essential signaling and structural roles required for the proper function of cardiac valves. Cardiac valves initially form as jelly-like cushions, which must adapt to withstand the increased circulation hemodynamics associated with fetal development and birth. This increased biomechanical stability of the developing valves is largely imparted by ECM proteins, which form a highly organized fibrous meshwork. Since heart valve defects contribute to most congenital heart diseases, understanding valve development will provide insight into the pathogenesis of various congenital valve anomalies. Thus, the goal of this study is to describe the spatiotemporal deposition of fibrous ECM proteins during cardiac valve development. Chick embryonic and fetal atrioventricular and semilunar valves were examined by light, confocal, and transmission electron microscopy (TEM). Our data demonstrate that fibrous ECM proteins are deposited when the leaflets are adopting an elongated and compacted phenotype. A general pattern of increased fibrotic ECM deposition was detected in valve tissues. Also, each ECM protein examined displayed a unique pattern of organization, suggesting that regulation of fibrous protein deposition is complex and likely involves both genetic and mechanical factors. In addition, the TEM study revealed the presence of membrane protrusions from valvular endocardium, indicating a potential mechanism for mechanical force transduction.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aikawa, E., Whittaker, P., Farber, M., Mendelson, K., Padera, R.F., Aikawa, M. & Schoen, F.J. (2006). Human semilunar cardiac valve remodeling by activated cells from fetus to adult: Implications for postnatal adaptation, pathology, and tissue engineering. Circulation 113(10), 13441352.CrossRefGoogle ScholarPubMed
Akishima, S., Sakurai, J. & Jikuya, T. (2004). Stickler syndrome with rapidly progressive mitral valve regurgitation: Report of a case. Kyobu Geka 57(7), 569572.Google ScholarPubMed
Anum, E.A., Hill, L.D., Pandya, A. & Strauss, J.F. 3rd (2009). Connective tissue and related disorders and preterm birth: Clues to genes contributing to prematurity. Placenta 30(3), 207215.CrossRefGoogle ScholarPubMed
Armstrong, E.J. & Bischoff, J. (2004). Heart valve development: Endothelial cell signaling and differentiation. Circ Res 95(5), 459470.CrossRefGoogle ScholarPubMed
Brown, J.C. & Timpl, R. (1995). The collagen superfamily. Int Arch Allergy Immunol 107(4), 484490.CrossRefGoogle ScholarPubMed
Burch, G.H., Gong, Y., Liu, W., Dettman, R.W., Curry, C.J., Smith, L., Miller, W.L. & Bristow, J. (1997). Tenascin-X deficiency is associated with Ehlers-Danlos syndrome. Nat Genet 17(1), 104108.CrossRefGoogle ScholarPubMed
Butcher, J.T., McQuinn, T.C., Sedmera, D., Turner, D. & Markwald, R.R. (2007). Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition. Circ Res 100(10), 15031511.Google Scholar
Combs, M.D. & Yutzey, K.E. (2009). Heart valve development: Regulatory networks in development and disease. Circ Res 105(5), 408421.Google Scholar
de Lange, F.J., Moorman, A.F., Anderson, R.H., Männer, J., Soufan, A.T., de Gier-de Vries, C., Schneider, M.D., Webb, S., van den Hoff, M.J. & Christoffels, V.M. (2004). Lineage and morphogenetic analysis of the cardiac valves. Circ Res 95(6), 645654.CrossRefGoogle ScholarPubMed
Delom, F., Burt, E., Hoischen, A., Veltman, J., Groet, J., Cotter, F.E. & Nizetic, D. (2009). Transchromosomic cell model of Down syndrome shows aberrant migration, adhesion and proteome response to extracellular matrix. Proteome Sci 7, 31.CrossRefGoogle ScholarPubMed
Eisenberg, L.M. & Markwald, R.R. (1995). Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res 77(1), 16.CrossRefGoogle ScholarPubMed
Fabbri, E., Forni, G.L., Guerrini, G. & Borgna-Pignatti, C. (2009). Pseudoxanthomaelasticum-like syndrome and thalassemia: An update. Dermatol Online J 15(7), 7.CrossRefGoogle ScholarPubMed
Garg, V., Muth, A.N., Ransom, J.F., Schluterman, M.K., Barnes, R. & King, I.N. (2005). Mutations in NOTCH1 cause aortic valve disease. Nature 437(7056), 270274.CrossRefGoogle ScholarPubMed
Gaussin, V., Muth, A.N., Ransom, J.F., Schluterman, M.K., Barnes, R., King, I.N., Grossfeld, P.D. & Srivastava, D. (2005). Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res 97(3), 219226.CrossRefGoogle ScholarPubMed
Gittenberger-de Groot, A.C., Bartram, U., Oosthoek, P.W., Bartelings, M.M., Hogers, B., Poelmann, R.E., Jongewaard, I.N. & Klewer, S.E. (2003). Collagen type VI expression during cardiac development and in human fetuses with trisomy 21. Anat Rec A Discov Mol Cell Evol Biol 275(2), 11091116.CrossRefGoogle ScholarPubMed
Hinton, R.B., Lincoln, J., Deutsch, G.H., Osinska, H., Manning, P.B., Benson, D.W. & Yutzey, K.E. (2006). Extracellular matrix remodeling and organization in developing and diseased aortic valves. Circ Res 98(11), 14311438.CrossRefGoogle ScholarPubMed
Hove, J.R., Köster, R.W., Forouhar, A.S., Acevedo-Bolton, G., Fraser, S.E. & Gharib, M. (2003). Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421(6919), 172177.CrossRefGoogle ScholarPubMed
Kadler, K.E., Baldock, C., Bella, J. & Boot-Handford, R.P. (2007). Collagens at a glance. J Cell Sci 120(12), 19551958.CrossRefGoogle ScholarPubMed
Kitten, G.T., Kolker, S.J., Krob, S.L. & Klewer, S.E. (1996). Type VI collagen in the cardiac valves and connective tissue septa during heart development. Braz J Med Biol Res 29(9), 11891193.Google ScholarPubMed
Klewer, S.E., Krob, S.L., Kolker, S.J. & Kitten, G.T. (1998). Expression of type VI collagen in the developing mouse heart. Dev Dyn 211(3), 248255.Google Scholar
Kruithof, B.P., Krawitz, S.A. & Gaussin, V. (2007). Atrioventricular valve development during late embryonic and postnatal stages involves condensation and extracellular matrix remodeling. Dev Biol 302(1), 208217.CrossRefGoogle ScholarPubMed
Lincoln, J., Lange, A.W. & Yutzey, K.E. (2006). Hearts and bones: Shared regulatory mechanisms in heart valve, cartilage, tendon, and bone development. Dev Biol 294(2), 292302.CrossRefGoogle ScholarPubMed
Lindeman, J.H., Ashcroft, B.A., Beenakker, J.W., van Es, M., Koekkoek, N.B., Prins, F.A., Tielemans, J.F., Abdul-Hussien, H., Bank, R.A. & Oosterkamp, T.H. (2010). Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome. Proc Natl Acad Sci USA 107(2), 862865.Google Scholar
Lucitti, J.L., Jones, E.A., Huang, C., Chen, J., Fraser, S.E. & Dickinson, M.E. (2007). Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134(18), 33173326.CrossRefGoogle ScholarPubMed
Martinsen, B.J. (2005). Reference guide to the stages of chick heart embryology. Dev Dyn 233(4), 12171237.Google Scholar
McGrath, J., Somlo, S., Makova, S., Tian, X. & Brueckner, M. (2003). Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114(1), 6173.Google Scholar
Nesta, F., Leyne, M., Yosefy, C., Simpson, C., Dai, D., Marshall, J.E., Hung, J., Slaugenhaupt, S.A. & Levine, R.A. (2005). New locus for autosomal dominant mitral valve prolapse on chromosome 13: Clinical insights from genetic studies. Circulation 112(13), 20222030.CrossRefGoogle ScholarPubMed
Nuytinck, L., Freund, M., Lagae, L., Pierard, G.E., Hermanns-Le, T. & De Paepe, A. (2000). Classical Ehlers-Danlos syndrome caused by a mutation in type I collagen. Am J Hum Genet 66(4), 13981402.CrossRefGoogle ScholarPubMed
Oberhauser, A.F., Marszalek, P.E., Erickson, H.P. & Fernandez, J.M. (1998). The molecular elasticity of the extracellular matrix protein tenascin. Nature 393(6681), 181185.CrossRefGoogle ScholarPubMed
Parry, D.A.D & Craig, A.S. (1984). Growth and development of collagen fibrils in connective tissue. In Ultrastructure of the Connective Tissue Matrix, Tuggeri, A. & Motta, P.M. (Eds.), pp. 3464. The Hague: Martiners Nijhoff.CrossRefGoogle Scholar
Patwari, P. & Lee, R.T. (2008). Mechanical control of tissue morphogenesis. Circ Res 103(3), 234243.CrossRefGoogle ScholarPubMed
Peacock, J.D., Lu, Y., Koch, M., Kadler, K.E. & Lincoln, J. (2008). Temporal and spatial expression of collagens during murine atrioventricular heart valve development and maintenance. Dev Dyn 237(10), 30513058.Google Scholar
Person, A.D., Klewer, S.E. & Runyan, R.B. (2005). Cell biology of cardiac cushion development. Int Rev Cytol 243, 287335.Google Scholar
Rabkin, E., Aikawa, M., Stone, J.R., Fukumoto, Y., Libby, P. & Schoen, F.J. (2001). Activated interstitial myofibroblasts express catabolic enzymes and mediate matrix remodeling in myxomatous heart valves. Circulation 104(21), 25252532.Google Scholar
Sacks, M.S., Schoen, F.J. & Mayer, J.E. (2009). Bioengineering challenges for heart valve tissue engineering. Ann Rev Biomed Eng 11, 289313.CrossRefGoogle ScholarPubMed
Schellings, M.W., Pinto, Y.M. & Heymans, S. (2004). Matricellular proteins in the heart: Possible role during stress and remodeling. Cardiovasc Res 64(1), 2431.Google Scholar
Schmults, C.D., Phelps, R. & Goldberg, D.J. (2004). Nonablative facial remodeling: Erythema reduction and histologic evidence of new collagen formation using a 300-microsecond 1064-nm Nd:YAG laser. Arch Dermatol 140(11), 13731376.CrossRefGoogle ScholarPubMed
Schroeder, J.A., Jackson, L.F., Lee, D.C. & Camenisch, T.D. (2003). Form and function of developing heart valves: Coordination by extracellular matrix and growth factor signaling. J Mol Med 81(7), 392403.Google Scholar
Snarr, B.S., Kern, C.B. & Wessels, A. (2008). Origin and fate of cardiac mesenchyme. Dev Dyn 237, 28042819.CrossRefGoogle ScholarPubMed
Van der Heiden, K., Groenendijk, B.C., Hierck, B.P., Hogers, B., Koerten, H.K., Mommaas, A.M., Gittenberger-de Groot, A.C. & Poelmann, R.E. (2006). Monocilia on chicken embryonic endocardium in low shear stress areas. Dev Dynam 235, 1928.Google Scholar
van der Rest, M. & Garrone, R. (1991). Collagen family of proteins. FASEB J 5(13), 28142823.Google Scholar
Ward, C., Stadt, H., Hutson, M. & Kirby, M.L. (2005). Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev Biol 284(1), 7283.CrossRefGoogle ScholarPubMed
Weis, S.M., Emery, J.L., Becker, K.D., McBride, D.J. Jr., Omens, J.H. & McCulloch, A.D. (2000). Myocardial mechanics and collagen sructure in the osteogenesis imperfecta murine (OIM). Circ Res 87, 663669.CrossRefGoogle Scholar