In Vivo Visualization of Cardiomyocyte Apicobasal Polarity Reveals Epithelial to Mesenchymal-like Transition during Cardiac Trabeculation

Cell Reports

Volumn 17, Issue 10, 2016, Pages 2687-2699

  Jiménez Amilburu, Vanesa ^a   Rasouli, S Javad ^a   Staudt, David W ^b   Nakajima, Hiroyuki ^c   Chiba, Ayano ^c   Mochizuki, Naoki ^c   Stainier, Didier Y R ^a,b  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

apical constriction; apicobasal polarity; cardiomyocyte depolarization; EMT; live imaging; trabeculation; zebrafish

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; NEU DIFFERENTIATION FACTOR; NOTCH RECEPTOR; PODOCALYXIN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1A; TRANSCRIPTION FACTOR SNAIL2; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST1A; TRANSCRIPTION FACTOR TWIST1B; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; CARDIAC MUSCLE CELL; CARDIAC TRABECULATION; CELL FATE; CELL MATURATION; CELL MEMBRANE DEPOLARIZATION; CELL POLARITY; CELL SHAPE; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HEART DEVELOPMENT; HEART MUSCLE BLOOD FLOW; HEART MUSCLE CONTRACTILITY; IN VIVO STUDY; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; TRANSGENE; ZEBRA FISH; ANIMAL; GENETICS; HEART CONTRACTION; HUMAN; METABOLISM; MOLECULAR IMAGING; ORGANOGENESIS; PATHOLOGY; TRANSGENIC ANIMAL; ULTRASTRUCTURE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL POLARITY; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MOLECULAR IMAGING; MORPHOGENESIS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NEUREGULIN-1; ORGANOGENESIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSGENES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85003026472     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.11.023     Document Type: Article

References (80)

1. Antunes, M., Pereira, T., Cordeiro, J.V., Almeida, L., Jacinto, A., Coordinated waves of actomyosin flow and apical cell constriction immediately after wounding. J. Cell Biol. 202 (2013), 365–379.
2. Aranda, V., Haire, T., Nolan, M.E., Calarco, J.P., Rosenberg, A.Z., Fawcett, J.P., Pawson, T., Muthuswamy, S.K., Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat. Cell Biol. 8 (2006), 1235–1245.
3. Baum, B., Settleman, J., Quinlan, M.P., Transitions between epithelial and mesenchymal states in development and disease. Semin. Cell Dev. Biol. 19 (2008), 294–308.
4. Beis, D., Stainier, D.Y.R., In vivo cell biology: following the zebrafish trend. Trends Cell Biol. 16 (2006), 105–112.
5. Betschinger, J., Mechtler, K., Knoblich, J.A., The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422 (2003), 326–330.
6. Bilder, D., Li, M., Perrimon, N., Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289 (2000), 113–116.
7. Chen, H., Shi, S., Acosta, L., Li, W., Lu, J., Bao, S., Chen, Z., Yang, Z., Schneider, M.D., Chien, K.R., et al. BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131 (2004), 2219–2231.
8. Chen, X., Higgins, J., Cheung, S.T., Li, R., Mason, V., Montgomery, K., Fan, S.T., van de Rijn, M., So, S., Novel endothelial cell markers in hepatocellular carcinoma. Mod. Pathol. 17 (2004), 1198–1210.
9. Cherian, A.V., Fukuda, R., Augustine, S.M., Maischein, H.M., Stainier, D.Y., N-cadherin relocalization during cardiac trabeculation. Proc. Natl. Acad. Sci. USA 113 (2016), 7569–7574.
10. Chi, N.C., Shaw, R.M., Jungblut, B., Huisken, J., Ferrer, T., Arnaout, R., Scott, I., Beis, D., Xiao, T., Baier, H., et al. Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biol., 6, 2008, e109.
11. Clark, B.S., Cui, S., Miesfeld, J.B., Klezovitch, O., Vasioukhin, V., Link, B.A., Loss of Llgl1 in retinal neuroepithelia reveals links between apical domain size, Notch activity and neurogenesis. Development 139 (2012), 1599–1610.
12. D'Amato, G., Luxán, G., del Monte-Nieto, G., Martínez-Poveda, B., Torroja, C., Walter, W., Bochter, M.S., Benedito, R., Cole, S., Martinez, F., et al. Sequential Notch activation regulates ventricular chamber development. Nat. Cell Biol. 18 (2016), 7–20.
13. D'Amico, L., Scott, I.C., Jungblut, B., Stainier, D.Y., A mutation in zebrafish hmgcr1b reveals a role for isoprenoids in vertebrate heart-tube formation. Curr. Biol. 17 (2007), 252–259.
14. David, D.J., Tishkina, A., Harris, T.J., The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137 (2010), 1645–1655.
15. Del Monte, G., Grego-Bessa, J., González-Rajal, A., Bolós, V., De La Pompa, J.L., Monitoring Notch1 activity in development: evidence for a feedback regulatory loop. Dev. Dyn. 236 (2007), 2594–2614.
16. Dewey, E.B., Taylor, D.T., Johnston, C.A., Cell fate decision making through oriented cell division. J. Dev. Biol. 3 (2015), 129–157.
17. Franke, J.D., Montague, R.A., Kiehart, D.P., Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr. Biol. 15 (2005), 2208–2221.
18. Gassmann, M., Casagranda, F., Orioli, D., Simon, H., Lai, C., Klein, R., Lemke, G., Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378 (1995), 390–394.
19. Geling, A., Steiner, H., Willem, M., Bally-Cuif, L., Haass, C., A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3 (2002), 688–694.
20. Grego-Bessa, J., Luna-Zurita, L., del Monte, G., Bolós, V., Melgar, P., Arandilla, A., Garratt, A.N., Zang, H., Mukouyama, Y.S., Chen, H., et al. Notch signaling is essential for ventricular chamber development. Dev. Cell 12 (2007), 415–429.
21. Han, P., Bloomekatz, J., Ren, J., Zhang, R., Grinstein, J.D., Zhao, L., Burns, C.G., Burns, C.E., Anderson, R.M., Chi, N.C., Coordinating cardiomyocyte interactions to direct ventricular chamber morphogenesis. Nature 534 (2016), 700–704.
22. Hardin, J., Keller, R., The behaviour and function of bottle cells during gastrulation of Xenopus laevis. Development 103 (1988), 211–230.
23. Hogan, B.L., Kolodziej, P.A., Organogenesis: molecular mechanisms of tubulogenesis. Nat. Rev. Genet. 3 (2002), 513–523.
24. Jenni, R., Rojas, J., Oechslin, E., Isolated noncompaction of the myocardium. N. Engl. J. Med. 340 (1999), 966–967.
25. Jenni, R., Oechslin, E.N., van der Loo, B., Isolated ventricular non-compaction of the myocardium in adults. Heart 93 (2007), 11–15.
26. Kalluri, R., Weinberg, R.A., The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119 (2009), 1420–1428.
27. Kemphues, K.J., Priess, J.R., Morton, D.G., Cheng, N.S., Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52 (1988), 311–320.
28. Kiehart, D.P., Galbraith, C.G., Edwards, K.A., Rickoll, W.L., Montague, R.A., Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149 (2000), 471–490.
29. Kikuchi, K., Holdway, J.E., Werdich, A.A., Anderson, R.M., Fang, Y., Egnaczyk, G.F., Evans, T., Macrae, C.A., Stainier, D.Y., Poss, K.D., Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464 (2010), 601–605.
30. Lee, K.-F., Simon, H., Chen, H., Bates, B., Hung, M.-C., Hauser, C., Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378 (1995), 394–398.
31. Lee, J.M., Dedhar, S., Kalluri, R., Thompson, E.W., The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172 (2006), 973–981.
32. Lee, J., Fei, P., Sevag Packard, R.R., Kang, H., Xu, H., Baek, K.I., Jen, N., Chen, J., Yen, H., Kuo, C.C., et al. 4-Dimensional light-sheet microscopy to elucidate shear stress modulation of cardiac trabeculation. J. Clin. Invest., 126, 2016, 3158.
33. Lemmers, C., Michel, D., Lane-Guermonprez, L., Delgrossi, M.H., Médina, E., Arsanto, J.P., Le Bivic, A., CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol. Biol. Cell 15 (2004), 1324–1333.
34. Li, J., Miao, L., Shieh, D., Spiotto, E., Li, J., Zhou, B., Paul, A., Schwartz, R.J., Firulli, A.B., Singer, H.A., et al. Single-Cell Lineage Tracing Reveals that Oriented Cell Division Contributes to Trabecular Morphogenesis and Regional Specification. Cell Rep. 15 (2016), 158–170.
35. Lin, Y.-F., Swinburne, I., Yelon, D., Multiple influences of blood flow on cardiomyocyte hypertrophy in the embryonic zebrafish heart. Dev. Biol. 362 (2012), 242–253.
36. Liu, J., Bressan, M., Hassel, D., Huisken, J., Staudt, D., Kikuchi, K., Poss, K.D., Mikawa, T., Stainier, D.Y.R., A dual role for ErbB2 signaling in cardiac trabeculation. Development 137 (2010), 3867–3875.
37. Mably, J.D., Mohideen, M.A., Burns, C.G., Chen, J.N., Fishman, M.C., heart of glass regulates the concentric growth of the heart in zebrafish. Curr. Biol. 13 (2003), 2138–2147.
38. Malone, M.H., Sciaky, N., Stalheim, L., Hahn, K.M., Linney, E., Johnson, G.L., Laser-scanning velocimetry: a confocal microscopy method for quantitative measurement of cardiovascular performance in zebrafish embryos and larvae. BMC Biotechnol., 7, 2007, 40.
39. Martin, A.C., Kaschube, M., Wieschaus, E.F., Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457 (2009), 495–499.
40. Meyer, D., Birchmeier, C., Multiple essential functions of neuregulin in development. Nature 378 (1995), 386–390.
41. Moorman, A.F.M., Christoffels, V.M., Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83 (2003), 1223–1267.
42. Mosimann, C., Kaufman, C.K., Li, P., Pugach, E.K., Tamplin, O.J., Zon, L.I., Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish. Development 138 (2011), 169–177.
43. Nance, J., Priess, J.R., Cell polarity and gastrulation in C. elegans. Development 129 (2002), 387–397.
44. Ninov, N., Borius, M., Stainier, D.Y., Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 139 (2012), 1557–1567.
45. Ninov, N., Hesselson, D., Gut, P., Zhou, A., Fidelin, K., Stainier, D.Y., Metabolic regulation of cellular plasticity in the pancreas. Curr. Biol. 23 (2013), 1242–1250.
46. Passer, D., van de Vrugt, A., Atmanli, A., Domian, I.J., Atypical protein kinase C-dependent Polarized cell division is required for myocardial trabeculation. Cell Rep. 14 (2016), 1662–1672.
47. Pérez-Pomares, J.M., de la Pompa, J.L., Signaling during epicardium and coronary vessel development. Circ. Res. 109 (2011), 1429–1442.
48. Person, A.D., Klewer, S.E., Runyan, R.B., Cell biology of cardiac cushion development. Jeon, D., (eds.) International Review of Cytology, 2005, Academic Press, 287–335.
49. Peshkovsky, C., Totong, R., Yelon, D., Dependence of cardiac trabeculation on neuregulin signaling and blood flow in zebrafish. Dev. Dyn. 240 (2011), 446–456.
50. Plant, P.J., Fawcett, J.P., Lin, D.C., Holdorf, A.D., Binns, K., Kulkarni, S., Pawson, T., A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5 (2003), 301–308.
51. Prehoda, K.E., Polarization of Drosophila neuroblasts during asymmetric division. Cold Spring Harb. Perspect. Biol., 1, 2009, a001388.
52. Reischauer, S., Arnaout, R., Ramadass, R., Stainier, D.Y., Actin binding GFP allows 4D in vivo imaging of myofilament dynamics in the zebrafish heart and the identification of Erbb2 signaling as a remodeling factor of myofibril architecture. Circ. Res. 115 (2014), 845–856.
53. Rothenpieler, U.W., Dressler, G.R., Pax-2 is required for mesenchyme-to-epithelium conversion during kidney development. Development 119 (1993), 711–720.
54. Royer, C., Lu, X., Epithelial cell polarity: a major gatekeeper against cancer?. Cell Death Differ. 18 (2011), 1470–1477.
55. Samsa, L.A., Yang, B., Liu, J., Embryonic cardiac chamber maturation: trabeculation, conduction, and cardiomyocyte proliferation. Am. J. Med. Genet. C. Semin. Med. Genet. 163C (2013), 157–168.
56. Samsa, L.A., Givens, C., Tzima, E., Stainier, D.Y.R., Qian, L., Liu, J., Cardiac contraction activates endocardial Notch signaling to modulate chamber maturation in zebrafish. Development 142 (2015), 4080–4091.
57. Sawyer, J.M., Harrell, J.R., Shemer, G., Sullivan-Brown, J., Roh-Johnson, M., Goldstein, B., Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol. 341 (2010), 5–19.
58. Schaefer, M., Shevchenko, A., Shevchenko, A., Knoblich, J.A., A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 10 (2000), 353–362.
59. Schober, M., Schaefer, M., Knoblich, J.A., Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 402 (1999), 548–551.
60. Sedmera, D., Pexieder, T., Vuillemin, M., Thompson, R.P., Anderson, R.H., Developmental patterning of the myocardium. Anat. Rec. 258 (2000), 319–337.
61. Sehnert, A.J., Huq, A., Weinstein, B.M., Walker, C., Fishman, M., Stainier, D.Y., Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31 (2002), 106–110.
62. 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 (2008), 208–218.
63. Stainier, D.Y., Zebrafish genetics and vertebrate heart formation. Nat. Rev. Genet. 2 (2001), 39–48.
64. Staudt, D., Stainier, D., Uncovering the molecular and cellular mechanisms of heart development using the zebrafish. Annu. Rev. Genet. 46 (2012), 397–418.
65. Staudt, D.W., Liu, J., Thorn, K.S., Stuurman, N., Liebling, M., Stainier, D.Y.R., High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation. Development 141 (2014), 585–593.
66. Suri, C., Jones, P.F., Patan, S., Bartunkova, S., Maisonpierre, P.C., Davis, S., Sato, T.N., Yancopoulos, G.D., Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87 (1996), 1171–1180.
67. Tabuse, Y., Izumi, Y., Piano, F., Kemphues, K.J., Miwa, J., Ohno, S., Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125 (1998), 3607–3614.
68. Tepass, U., Theres, C., Knust, E., crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61 (1990), 787–799.
69. Thiery, J.P., Acloque, H., Huang, R.Y., Nieto, M.A., Epithelial-mesenchymal transitions in development and disease. Cell 139 (2009), 871–890.
70. Toyofuku, T., Zhang, H., Kumanogoh, A., Takegahara, N., Yabuki, M., Harada, K., Hori, M., Kikutani, H., Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat. Cell Biol. 6 (2004), 1204–1211.
71. VanDusen, N.J., Casanovas, J., Vincentz, J.W., Firulli, B.A., Osterwalder, M., Lopez-Rios, J., Zeller, R., Zhou, B., Grego-Bessa, J., De La Pompa, J.L., et al. Hand2 is an essential regulator for two Notch-dependent functions within the embryonic endocardium. Cell Rep. 9 (2014), 2071–2083.
72. von Gise, A., Pu, W.T., Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ. Res. 110 (2012), 1628–1645.
73. Wang, H.U., Chen, Z.-F., Anderson, D.J., Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93 (1998), 741–753.
74. Westcot, S.E., Hatzold, J., Urban, M.D., Richetti, S.K., Skuster, K.J., Harm, R.M., Lopez Cervera, R., Umemoto, N., McNulty, M.S., Clark, K.J., et al. Protein-trap insertional mutagenesis uncovers new Genes involved in zebrafish skin development, including a neuregulin 2a-based ErbB signaling pathway required during median fin fold morphogenesis. PLoS ONE, 10, 2015, e0130688.
75. Wodarz, A., Ramrath, A., Kuchinke, U., Knust, E., Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402 (1999), 544–547.
76. Yoruk, B., Gillers, B.S., Chi, N.C., Scott, I.C., Ccm3 functions in a manner distinct from Ccm1 and Ccm2 in a zebrafish model of CCM vascular disease. Dev. Biol. 362 (2012), 121–131.
77. Yu, F., Morin, X., Cai, Y., Yang, X., Chia, W., Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100 (2000), 399–409.
78. Yu, F., Kuo, C.T., Jan, Y.N., Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 51 (2006), 13–20.
79. Zhang, W., Chen, H., Qu, X., Chang, C.P., Shou, W., Molecular mechanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy (LVNC). Am. J. Med. Genet. C. Semin. Med. Genet. 163C (2013), 144–156.
80. Zhou, B., Pu, W.T., Epicardial epithelial-to-mesenchymal transition in injured heart. J. Cell. Mol. Med. 15 (2011), 2781–2783.