Preloader

CDH18 is a fetal epicardial biomarker regulating differentiation towards vascular smooth muscle cells

  • 1.

    Bargehr, J. et al. Epicardial cells derived from human embryonic stem cells augment cardiomyocyte-driven heart regeneration. Nat. Biotechnol. 37, 895–906 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 2.

    Pérez-Pomares, J. M. & de la Pompa, J. L. Signaling during epicardium and coronary vessel development. Circ. Res. 109, 1429–1442 (2011).

    PubMed 

    Google Scholar 

  • 3.

    van Wijk, B. & van den Hoff, M. Epicardium and myocardium originate from a common cardiogenic precursor pool. Trends Cardiovasc. Med. 20, 1–7 (2010).

    PubMed 

    Google Scholar 

  • 4.

    Zhou, B. et al. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Investig. 121, 1894–1904 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 5.

    Gittenberger-de Groot, A. C., Vrancken Peeters, M. P., Mentink, M. M., Gourdie, R. G. & Poelmann, R. E. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ. Res. 82, 1043–1052 (1998).

    CAS 
    PubMed 

    Google Scholar 

  • 6.

    von Gise, A. et al. WT1 regulates epicardial epithelial to mesenchymal transition through β-catenin and retinoic acid signaling pathways. Dev. Biol. 356, 421–431 (2011).

    Google Scholar 

  • 7.

    Braitsch, C. M. & Yutzey, K. E. Transcriptional control of cell lineage development in epicardium-derived cells. J. Dev. Biol. 1, 92–111 (2013).

    PubMed 

    Google Scholar 

  • 8.

    Katz, T. C. et al. Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev. Cell 22, 639–650 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 9.

    Zhou, B. et al. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454, 109–113 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Krainock, M. et al. Epicardial epithelial-to-mesenchymal transition in heart development and disease. J. Clin. Med. 5, 27 (2016).

  • 11.

    Smart, N., Dube, K. N. & Riley, P. R. Coronary vessel development and insight towards neovascular therapy. Int. J. Exp. Pathol. 90, 262–283 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    van Wijk, B., Gunst, Q. D., Moorman, A. F. & van den Hoff, M. J. Cardiac regeneration from activated epicardium. PLoS ONE 7, e44692 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 13.

    Rao, K. S. & Spees, J. L. Harnessing epicardial progenitor cells and their derivatives for rescue and repair of cardiac tissue after myocardial infarction. Curr. Mol. Biol. Rep. 3, 149–158 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Cao, Y. & Cao, J. Covering and re-covering the heart: development and regeneration of the epicardium. J. Cardiovasc. Dev. Dis. 6, 3 (2018).

  • 15.

    Ramjee, V. et al. Epicardial YAP/TAZ orchestrate an immunosuppressive response following myocardial infarction. J. Clin. Investig. 127, 899–911 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 16.

    Wei, K. et al. Epicardial FSTL1 reconstitution regenerates the adult mammalian heart. Nature 525, 479–485 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Sun, X. et al. The extracellular matrix protein agrin is essential for epicardial epithelial-to-mesenchymal transition during heart development. Development 148, dev197525 (2021).

  • 18.

    Walma, D. A. C. & Yamada, K. M. The extracellular matrix in development. Development 147, dev175596 (2020).

  • 19.

    Halbleib, J. M. & Nelson, W. J. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20, 3199–3214 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 20.

    Foty, R. A. & Steinberg, M. S. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255–263 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • 21.

    Hogan, C. et al. Rap1 regulates the formation of E-cadherin-based cell–cell contacts. Mol. Cell. Biol. 24, 6690–6700 (2004).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 22.

    Johnson, E., Theisen, C. S., Johnson, K. R. & Wheelock, M. J. R-cadherin influences cell motility via Rho family GTPases. J. Biol. Chem. 279, 31041–31049 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • 23.

    Luo, J., Treubert-Zimmermann, U. & Redies, C. Cadherins guide migrating Purkinje cells to specific parasagittal domains during cerebellar development. Mol. Cell. Neurosci. 25, 138–152 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • 24.

    Maeda, M., Johnson, K. R. & Wheelock, M. J. Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J. Cell Sci. 118, 873–887 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • 25.

    Reintsch, W. E., Habring-Mueller, A., Wang, R. W., Schohl, A. & Fagotto, F. beta-Catenin controls cell sorting at the notochord-somite boundary independently of cadherin-mediated adhesion. J. Cell Biol. 170, 675–686 (2005).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 26.

    Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861–872 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • 27.

    Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 28.

    Bao, X. et al. Long-term self-renewing human epicardial cells generated from pluripotent stem cells under defined xeno-free conditions. Nat. Biomed. Eng. 1, 0003 (2016).

  • 29.

    Bax, N. A. M. et al. In vitro epithelial-to-mesenchymal transformation in human adult epicardial cells is regulated by TGFβ-signaling and WT1. Basic Res. Cardiol. 106, 829–847 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Burridge, P. W., Keller, G., Gold, J. D. & Wu, J. C. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 10, 16–28 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Compton, L. A., Potash, D. A., Mundell, N. A. & Barnett, J. V. Transforming growth factor-β induces loss of epithelial character and smooth muscle cell differentiation in epicardial cells. Dev. Dyn. 235, 82–93 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 32.

    Iyer, D. et al. Robust derivation of epicardium and its differentiated smooth muscle cell progeny from human pluripotent stem cells. Development 142, 1528–1541 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 33.

    Mummery, C. L. et al. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ. Res. 111, 344–358 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Tuyn, J. V. et al. Epicardial cells of human adults can undergo an epithelial-to-mesenchymal transition and obtain characteristics of smooth muscle cells in vitro. STEM CELLS 25, 271–278 (2007).

    PubMed 

    Google Scholar 

  • 35.

    Witty, A. D. et al. Generation of the epicardial lineage from human pluripotent stem cells. Nat. Biotechnol. 32, 1026–1035 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 36.

    Zhao, J. et al. Efficient differentiation of TBX18(+)/WT1(+) epicardial-like cells from human pluripotent stem cells using small molecular compounds. Stem Cells Dev. 26, 528–540 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 37.

    Watt, A. J., Battle, M. A., Li, J. & Duncan, S. A. GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc. Natl Acad. Sci. USA 101, 12573–12578 (2004).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 38.

    Bai, Y. H. et al. A novel tumor-suppressor, CDH18, inhibits glioma cell invasiveness via UQCRC2 and correlates with the prognosis of glioma patients. Cell. Physiol. Biochem. 48, 1755–1770 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 39.

    Klein, M. E. et al. PDLIM7 and CDH18 regulate the turnover of MDM2 during CDK4/6 inhibitor therapy-induced senescence. Oncogene 37, 5066–5078 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    Shibata, T., Shimoyama, Y., Gotoh, M. & Hirohashi, S. Identification of human cadherin-14, a novel neurally specific type II cadherin, by protein interaction cloning. J. Biol. Chem. 272, 5236–5240 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • 41.

    Funakoshi, S. et al. Enhanced engraftment, proliferation, and therapeutic potential in heart using optimized human iPSC-derived cardiomyocytes. Sci. Rep. 6, 19111 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Yang, J. et al. Guidelines and definitions for research on epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 21, 341–352 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 43.

    Moerkamp, A. T. et al. Human fetal and adult epicardial-derived cells: a novel model to study their activation. Stem Cell Res. Ther. 7, 174 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 44.

    Wei, X. et al. Biological characteristics of embryonic epicardial cells in vitro correlate with embryonic day. Acta Biochim. Biophys. Sin. 49, 14–24 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 45.

    Dokic, D. & Dettman, R. W. VCAM-1 inhibits TGFβ stimulated epithelial–mesenchymal transformation by modulating Rho activity and stabilizing intercellular adhesion in epicardial mesothelial cells. Dev. Biol. 299, 489–504 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 46.

    Dronkers, E., Wauters, M. M. M., Goumans, M. J. & Smits, A. M. Epicardial TGFβ and BMP signaling in cardiac regeneration: what lesson can we learn from the developing heart? Biomolecules 10, 404 (2020).

    CAS 
    PubMed Central 

    Google Scholar 

  • 47.

    Goumans, M. -J. & Ten Dijke, P. TGF-β signaling in control of cardiovascular function. Cold Spring Harbor Perspect. Biol. 10, a022210 (2018).

  • 48.

    Hill, C. R. et al. BMP2 signals loss of epithelial character in epicardial cells but requires the Type III TGFβ receptor to promote invasion. Cell. Signal. 24, 1012–1022 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 49.

    Ishii, Y., Garriock, R. J., Navetta, A. M., Coughlin, L. E. & Mikawa, T. BMP signals promote proepicardial protrusion necessary for recruitment of coronary vessel and epicardial progenitors to the heart. Dev. Cell 19, 307–316 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Lu, J. et al. Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev. Biol. 240, 404–418 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • 51.

    Mack, C. P. Signaling mechanisms that regulate smooth muscle cell differentiation. Arterioscler. Thromb. Vasc. Biol. 31, 1495–1505 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Rudat, C., Norden, J., Taketo, M. M. & Kispert, A. Epicardial function of canonical Wnt-, Hedgehog-, Fgfr1/2-, and Pdgfra-signalling. Cardiovasc. Res. 100, 411–421 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 53.

    Smith, C. L., Baek, S. T., Sung, C. Y. & Tallquist, M. D. Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ. Res. 108, e15–e26 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Zhou, B. P. et al. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial–mesenchymal transition. Nat. Cell Biol. 6, 931–940 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • 55.

    Duan, J. et al. Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J. 31, 429–442 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • 56.

    Heuberger, J. & Birchmeier, W. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb. Perspect. Biol. 2, a002915 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 57.

    Nelson, W. J. & Nusse, R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483–1487 (2004).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 58.

    Shimoyama, Y., Takeda, H., Yoshihara, S., Kitajima, M. & Hirohashi, S. Biochemical characterization and functional analysis of two type II classic cadherins, cadherin-6 and -14, and comparison with E-cadherin. J. Biol. Chem. 274, 11987–11994 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • 59.

    Acharya, A. et al. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development 139, 2139–2149 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 60.

    Braitsch, C. M., Combs, M. D., Quaggin, S. E. & Yutzey, K. E. Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epicardium-derived cells into smooth muscle in the developing heart. Dev. Biol. 368, 345–357 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 61.

    Hu, H., Lin, S., Wang, S. & Chen, X. The role of transcription factor 21 in epicardial cell differentiation and the development of coronary heart disease. Front. Cell Dev. Biol. 8, 457 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 62.

    Lupu, I. E., De Val, S. & Smart, N. Coronary vessel formation in development and disease: mechanisms and insights for therapy. Nat. Rev. Cardiol. 17, 790–806 (2020).

    PubMed 

    Google Scholar 

  • 63.

    Tevosian, S. G. et al. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 101, 729–739 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • 64.

    Zhuge, Y. et al. Role of smooth muscle cells in cardiovascular disease. Int. J. Biol. Sci. 16, 2741–2751 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 65.

    Wu, M. et al. Epicardial spindle orientation controls cell entry into the myocardium. Dev. Cell 19, 114–125 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 66.

    Risebro, C. A., Vieira, J. M., Klotz, L. & Riley, P. R. Characterisation of the human embryonic and foetal epicardium during heart development. Development 142, 3630–3636 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Velecela, V. et al. Epicardial cell shape and maturation are regulated by Wt1 via transcriptional control of Bmp4. Development 146, ev178723 (2019).

  • 68.

    Meigs, T. E., Fields, T. A., McKee, D. D. & Casey, P. J. Interaction of Gα12 and Gα13 with the cytoplasmic domain of cadherin provides a mechanism for β-catenin release. PNAS 98, 519–524 (2001).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 69.

    Rudat, C. & Kispert, A. Wt1 and epicardial fate mapping. Circ. Res. 111, 165–169 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • 70.

    Zamora, M., Männer, J. & Ruiz-Lozano, P. Epicardium-derived progenitor cells require β-catenin for coronary artery formation. PNAS 104, 18109–18114 (2007).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 71.

    Azambuja Ana, P. et al. Retinoic aid and VEGF delay smooth muscle relative to endothelial differentiation to coordinate inner and outer coronary vessel wall morphogenesis. Circ. Res. 107, 204–216 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • 72.

    Guadix, J. A. et al. Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 138, 1093–1097 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 73.

    Sridurongrit, S., Larsson, J., Schwartz, R., Ruiz-Lozano, P. & Kaartinen, V. Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev. Biol. 322, 208–218 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 74.

    Sánchez, N. S. & Barnett, J. V. TGFβ and BMP-2 regulate epicardial cell invasion via TGFβR3 activation of the Par6/Smurf1/RhoA pathway. Cell. Signal. 24, 539–548 (2012).

    PubMed 

    Google Scholar 

  • 75.

    Zhao, W. et al. Effect of TGF-β1 on the migration and recruitment of mesenchymal stem cells after vascular balloon injury: involvement of matrix metalloproteinase-14. Sci. Rep. 6, 21176 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 76.

    Tao, J., Barnett, J. V., Watanabe, M. & Ramírez-Bergeron, D. Hypoxia supports epicardial cell differentiation in vascular smooth muscle cells through the activation of the TGFβ pathway. J. Cardiovasc. Dev. Dis. 5, (2018).

  • Source link