Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T02:38:23.888Z Has data issue: false hasContentIssue false
  • English
  • Français

Cross Talk between Cell–Cell and Cell–Matrix Adhesion Signaling Pathways during Heart Organogenesis: Implications for Cardiac Birth Defects

Published online by Cambridge University Press:  12 May 2005

Kersti K. Linask ,
Shyam Manisastry  and
Mingda Han
Kersti K. Linask
Affiliation:
Department of Pediatrics, University of South Florida, College of Medicine, The Children's Research Institute, St. Petersburg, FL 33701, USA
Shyam Manisastry
Affiliation:
Department of Pediatrics, University of South Florida, College of Medicine, The Children's Research Institute, St. Petersburg, FL 33701, USA
Mingda Han
Affiliation:
Department of Pediatrics, University of South Florida, College of Medicine, The Children's Research Institute, St. Petersburg, FL 33701, USA
Get access

Abstract

The anterior–posterior and dorsal–ventral progression of heart organogenesis is well illustrated by the patterning and activity of two members of different families of cell adhesion molecules: the calcium-dependent cadherins, specifically N-cadherin, and the extracellular matrix glycoproteins, fibronectin. N-cadherin by its binding to the intracellular molecule β-catenin and fibronectin by its binding to integrins at focal adhesion sites, are involved in regulation of gene expression by their association with the cytoskeleton and through signal transduction pathways. The ventral precardiac mesoderm cells epithelialize and become stably committed by the activation of these cell–matrix and intracellular signaling transduction pathways. Cross talk between the adhesion signaling pathways initiates the characteristic phenotypic changes associated with cardiomyocyte differentiation: electrical activity and organization of myofibrils. The development of both organ form and function occurs within a short interval thereafter. Mutations in any of the interacting molecules, or environmental insults affecting either of these signaling pathways, can result in embryonic lethality or fetuses born with severe heart defects. As an example, we have defined that exposure of the embryo temporally to lithium during an early sensitive developmental period affects a canonical Wnt pathway leading to β-catenin stabilization. Lithium exposure results in an anterior–posterior progression of severe cardiac defects.

Keywords

heart organogenesisN-cadherinβ-cateninfibronectincross talkcardiomyocytedifferentiationWnt signalinglithium
Type
Research Article
Information
Microscopy and Microanalysis , Volume 11 , Issue 3 , June 2005 , pp. 200 - 208
Copyright
© 2005 Microscopy Society of America

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

Akitaya, T. & Bronner-Fraser, M. (1992). Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Dev Dyn 194, 12–20.Google Scholar
Altshuler, L.L., Cohen, L., Szuba, M.P., Burt, V.K., Gitlin, M., & Mintz, J. (1996). Pharmacologic management of psychiatric illness during pregnancy: Dilemmas and guidelines. Am J Psychiatry 153, 592–606.Google Scholar
Bronner-Fraser, M. (1986). Guidance of neural crest migration. Latex beads as probes of surface–substratum interactions. Dev Biol (N Y 1985) 3, 301–337.Google Scholar
Bronner-Fraser, M., Artinger, M., Muschler, J., & Horwitz, A.F. (1992). Developmentally regulated expression of alpha 6 integrin in avian embryos. Development 115, 197–211.Google Scholar
Bronner-Fraser, M. & Lallier, T. (1988). A monoclonal antibody against a laminin-heparan sulfate proteoglycan complex perturbs cranial neural crest migration in vivo. J Cell Biol 106, 1321–1329.Google Scholar
Cachaco, A.S., Chuva de Sousa Lopes, S.M., Kuikman, I., Bajanca, F., Abe, K., Baudoin, C., Sonnenberg, A., Mummery, C.L., & Thorsteinsdottir, S. (2003). Knock-in of integrin beta 1D affects primary but not secondary myogenesis in mice. Development 130, 1659–1671.Google Scholar
Cohen, L.S., Friedman, J.M., Jefferson, J.W., Johnson, E.M., & Weiner, M.L. (1994). A reevaluation of risk of in utero exposure to lithium. JAMA 271, 146–150.Google Scholar
DeHaan, R.L. (1964). Cell interactions and oriented movements during development. J Exp Zool 157, 127–138.Google Scholar
de la Cruz, M.V., Sanchez Gomez, C., & Cayre, R. (1991). The developmental components of the ventricles: Their significance in congenital cardiac malformations. Cardiol Young 1, 123–128.Google Scholar
de la Cruz, M.V. & Sanchez-Gomez, C. (1998). Straight tube heart. Primitive cardiac cavities vs. primitive cardiac segments. In Living Morphogenesis of the Heart, de la Cruz, M.V. & Markwald, R.R. (Eds.), pp. 85–98. Boston: Birkhauser.
de la Cruz, M.V., Sanchez-Gomez, C., & Palomina, M.A. (1989). The primitive cardiac regions in the straight tube heart (Stage 9-) and their anatomical expression in the mature heart: An experimental study in the chick embryo. J Anat 165, 121–131.Google Scholar
Edelman, G.M., Cunningham, B.A., & Thiery, J.P. (1990). Introduction. In Morphoregulatory Molecules, Edelman, G.M., Cunningham, B.A. & Thiery, J.P. (Eds.), pp. 1–5. Indianapolis, IN: Neurosciences Institute Publication.
Eisenberg, C.A., Gourdie, R.G., & Eisenberg, L.M. (1997). Wnt-11 is expresed in early avian mesoderm and required for the differentiation of the quail mesoderm cell line QCE-6. Development 124, 525–536.Google Scholar
Ernst, C.L. & Goldberg, J.F. (2002). The reproductive safety profile of mood stabilizers, atypical antipsychotics, and broad-spectrum psychotropics. J Clin Psychiatry 63(Suppl. 4), 42–55.Google Scholar
Fassler, R., Rohwedel, J., Maltsev, V., Bloch, W., Lentini, S., Guan, K., Gillberg, D., Hescheler, J., Addicks, K., & Wobus, A. (1996). Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta1 integrin. J Cell Sci 109, 2989–2999.Google Scholar
George, E.L., Baldwin, H.S., & Hynes, R.O. (1997). Fibronectins are essential for heart and blood vessel morphogenesis but are dispensable for initial specification of precursor cells. Blood 90, 3073–3081.Google Scholar
George, E.L., Georges-Labouesse, E.N., Patel-King, R.S., Rayburn, H., & Hynes, R.O. (1993). Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079–1091.Google Scholar
Gradl, D., Kuhl, M., & Wedlich, D. (1999). The Wnt/Wg signal transducer β-catenin controls fibronectin expression. Mol Cell Biol 19, 5576–5587.Google Scholar
Hamburger, V. & Hamilton, H.L. (1951). A series of normal stages in the development of the chick embryo. J Morphol 88, 49–92.Google Scholar
Hedgepeth, C.M., Conrad, L.J., Zhang, J., Huang, H.C., Lee, V.M.Y., & Klein, P.S. (1997). Activation of the Wnt signaling pathway: A molecular mechanism for lithium action. Dev Biol 185, 82–91.Google Scholar
Hurlstone, A.F., Haramis, A.P., Wienholds, E., Begthel, H., Korving, J., Van Eeden, F., Cuppen, E., Zivkovic, D., Plasterk, R.H., & Clevers, H. (2003). The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 425, 633–637.Google Scholar
Imanaka-Yoshida, K., Knudsen, K., & Linask, K.K. (1998). Initial myofibrillogenesis in precardiac mesoderm cultures. Cell Motil Cytoskeleton 39, 52–62.Google Scholar
Kamino, K. (1991). Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol Rev 71, 53–91.Google Scholar
Klein, P.S. & Melton, D.A. (1996). A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93, 8455–8459.Google Scholar
Koushik, S.V., Wang, J., Rogers, R., Moskophidis, D., Lambert, N.A., Creazzo, R.L., & Conway, S.J. (2001). Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J 15, 1209–1211.Google Scholar
Krotoski, D. & Bronner-Fraser, M. (1990). Distribution of integrins and their ligands in the trunk of Xenopus laevis during neural crest cell migration. J Exp Zool 253, 139–150.Google Scholar
Krotoski, D.M., Domingo, C., & Bronner-Fraser, M. (1986). Distribution of a putative cell surface receptor for fibronectin and laminin in the avian embryo. J Cell Biol 103, 1061–1071.Google Scholar
Lallier, T. & Bronner-Fraser, M. (1993). Inhibition of neural crest cell attachment by integrin antisense oligonucleotides. Science 259, 692–695.Google Scholar
Lash, J.W., Linask, K.K., & Yamada, K.M. (1987). Synthetic peptides that mimic the adhesive recognition signal of fibronectin: Differential effects on cell–cell and cell–substratum adhesion in embryonic chick cells. Dev Biol 123, 411–420.Google Scholar
Lee, H.Y., Kleber, M., Hari, L., Brault, V., Suter, U., Taketo, M.M., Kemler, R., & Sommer, L. (2004). Instructive role of wnt/{beta}-catenin in sensory fate specification in neural crest stem cells. Science 303, 1020–1023.Google Scholar
Linask, K. (2003). Regulation of heart morphology: Current molecular and cellular perspectives on the coordinated emergence of cardiac form and function. Birth Defects Research (Part C) 69, 14–24.Google Scholar
Linask, K.K. (1992a). N-cadherin localization in early heart development and polar expression of Na, K-ATPase, and integrin during pericardial coelom formation and epithelialization of the differentiating myocardium. Dev Biol 151, 213–224.Google Scholar
Linask, K.K. (1992b). Regulatory role of cell adhesion molecules in early heart development. In Formation and Differentiation of Early Embryonic Mesoderm, Bellairs, R., Sanders, E.J. & Lash, J.W. (Eds.), pp. 301–313. New York: Plenum Publishing Corporation.
Linask, K.K. & Gui, Y.H. (1995). Inhibitory effects of ouabain on early heart development and cardiomyogenesis in the chick embryo. Dev Dyn 203, 93–105.Google Scholar
Linask, K., Gui, Y.H., Rasheed, R., & Kwon, L. (1992). Pattern development during pericardial coelom formation and specification of the cardiomyocyte cell population by N-cadherin and the Drosophila armadillo protein homologue in the early chick embryo. Mol Biol Cell 3(Suppl.), 206A.Google Scholar
Linask, K.K., Han, M.D., Artman, M., & Ludwig, C.A. (2001). Sodium-calcium exchanger (NCX-1) and calcium modulation. NCX protein expression patterns and regulation of early heart development. Dev Dyn 221, 249–264.Google Scholar
Linask, K.K., Knudsen, K.A., & Gui, Y.H. (1997). N-cadherin-catenin interaction: Necessary component of cardiac cell compartmentalization during early vertebrate heart development. Dev Biol 185, 148–164.Google Scholar
Linask, K.K. & Lash, J.W. (1986). Precardiac cell migration: Fibronectin localization at mesoderm–endoderm interface during directional movement. Dev Biol 114, 87–101.Google Scholar
Linask, K.K. & Lash, J.W. (1988a). A role for fibronectin in the migration of avian precardiac cells. I. Dose dependent effects of fibronectin antibody. Dev Biol 129, 315–323.Google Scholar
Linask, K.K. & Lash, J.W. (1988b). A role for fibronectin in the migration of avian precardiac cells. II. Rotation of the heart-forming region during different stages and its effects. Dev Biol 129, 324–329.Google Scholar
Linask, K.K. & Lash, J.W. (1990). Fibronectin and integrin distribution on migrating precardiac mesoderm cells. Ann NY Acad Sci 588, 417–420.Google Scholar
Linask, K.K. & Lash, J.W. (1993). Early heart development: Dynamics of endocardial cell sorting suggests a common origin with cardiomyocytes. Dev Dyn 195, 62–69.Google Scholar
Linask, K.K., Ludwig, C., Han, M.D., Liu, X., Radice, G.L., & Knudsen, K.A. (1998). N-cadherin/catenin-mediated morphoregulation of somite formation. Dev Biol 202, 85–102.Google Scholar
Lough, J. & Sugi, Y. (2000). Endoderm and heart development. Dev Dyn 217, 327–342.Google Scholar
Luo, Y. & Radice, G.L. (2003). Cadherin-mediated adhesion is essential for myofibril continuity across the plasma membrane but not for assembly of the contractile apparatus. J Cell Sci 116, 1471–1479.Google Scholar
Markwald, R.R., Nakaoka, T., & Mjaatvedt, C.H. (2000). Overview: Formation of the primary heart tube. In Etiology and Morphogenesis of Congenital Heart Disease: Twenty Years of Progress in Genetics and Developmental Biology, Clark, E.B., Nakazawa, M. & Takao, A. (Eds.), pp. 103–114B. Armonk, NY: Futura Publishing Co., Inc.
Markwald, R.R., Trusk, T., & Moreno-Rodriguez, R. (1998). Formation and septation of the tubular heart: Integrating the dynamics of morphology with emerging molecular concepts. In Living Morphogenesis of the Heart, de la Cruz, M.V. & Markwald, R.R. (Eds.), pp. 43–84. Boston: Birkhauser.
Marlow, F., Topczewski, J., Sepich, D., & Solnica-Krezel, L. (2002). Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr Biol 12, 876–884.Google Scholar
Marvin, M.J., Di Rocco, G., Gardiner, A., Bush, S.M., & Lassar, A.B. (2001). Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes & Dev 15, 316–327.Google Scholar
Moncrieff, J. (1997). Lithium: Evidence reconsidered. Br J Psych 171, 113–119.Google Scholar
Pandur, P., Lasche, M., Eisenberg, L., & Kuhl, M. (2002). Wnt-11 activation of a non-canonical Wnt signaling pathway is required for cardiogenesis. Nature 418, 636–641.Google Scholar
Peifer, M. (1995). Cell adhesion and signal transduction: The Armadillo connection. Trends Cell Biol 5, 224–229.Google Scholar
Radice, G.L., Rayburn, H., Matsunami, H., Knudsen, K.A., Takeichi, M., & Hynes, R.O. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181, 64–78.Google Scholar
Rodriguez-Boulan, E. & Nelson, W.J. (1989). Morphogenesis of the polarized epithelial cell phenotype. Science 245, 718–724.Google Scholar
Schneider, V.A. & Mercola, M. (2001). Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes & Dev 15, 304–315.Google Scholar
Stambolic, V., Ruel, L., & Woodgett, J.R. (1996). Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 6, 1664–1668.Google Scholar
Sugi, Y. & Markwald, R.R. (1996). Formation and early morphogenesis of endocardial endothelial precursor cells and the role of endoderm. Dev Biol 175, 66–83.Google Scholar
Suksaweang, S., Lin, C.M., Jiang, T.X., Hughes, M.W., Widelitz, R.B., & Chuong, C.M. (2004). Morphogenesis of chicken liver: Identification of localized growth zones and the role of beta-catenin/Wnt in size regulation. Dev Biol 266, 109–122.Google Scholar
Suzuki, H.R., Solursh, M., & Baldwin, H.S. (1995). Relationship between fibronectin expression during gastrulation and heart formation in the rat embryo. Dev Dyn 204, 259–277.Google Scholar
Takeichi, M. (1988). The cadherins: Cell–cell adhesion molecules controlling animal morphogenesis. Development 102, 639–655.Google Scholar
Trinh, L.A. & Stainier, D.Y. (2003). Epithelial organization and migration of the myocardial precursors require cell–substratum interaction in zebrafish. Mol Biol Cell 14, 140a.Google Scholar
Trinkaus, J. (1984). Cells into Organs. Englewood Cliffs, NJ: Prentice-Hall, Inc.
Wakimoto, K., Kobayashi, K., Kuro-o, M., Yao, A., Iwamoto, K., Yanaka, N., Kita, S., Nishida, A., Azuma, S., Toyoda, Y., Omori, K., Imahie, H., Oka, T., Kudoh, S., Kohmoto, O., Yazaki, Y., Shigekawa, M., Imai, Y., Nabeshima, Y.-I., & Komuro, I. (2000). Targeted disruption of Na+/Ca++ exchanger gene leads to cardiomyocyte apoptosis and defects in heartbeat. J Biol Chem 275, 36991–36998.Google Scholar
Wheelock, M.J. & Johnson, K.R. (2003). Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15, 509–514.Google Scholar
Yu, X. & Malenka, R.C. (2003). Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6, 1169–1177.Google Scholar