Plakoglobin has both structural and signalling roles in zebrafish development

Developmental Biology

Volumn 327, Issue 1, 2009, Pages 83-96

  Martin, Eva D ^a   Moriarty, Miriam A ^a   Byrnes, Lucy ^a   Grealy, Maura ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Adherens junctions; ARVC; Desmosomes; Heart development; Morpholino; Plakoglobin; Wnt beta catenin signalling; Zebrafish

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; DICKKOPF 1 PROTEIN; MESSENGER RNA; NOTCH1 RECEPTOR; PLAKOGLOBIN; PLAKOGLOBIN 1A; PLAKOGLOBIN 1B; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG; UVOMORULIN; WNT PROTEIN;

ANGIOGENESIS; ARTICLE; CELL JUNCTION; CLMC GENE; CONTROLLED STUDY; DESMOSOME; ENDOTHELIUM CELL; FERTILIZATION; GENE; GENE EXPRESSION; HEART BEAT; HEART DEVELOPMENT; HEART DISEASE; HEART EDEMA; HEART SIZE; HEART VALVE; HEMATOPOIESIS; IN SITU HYBRIDIZATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REAL TIME POLYMERASE CHAIN REACTION; VMHC GENE; ZEBRA FISH;

DANIO RERIO;

EID: 59649083176     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.11.036     Document Type: Article

References (70)

1. Armeanu S., Buhring H.J., Reuss-Borst M., Muller C.A., and Klein G. E-cadherin is functionally involved in the maturation of the erythroid lineage. J. Cell Biol. 131 (1995) 243-249
2. Asimaki A., Syrris P., Wichter T., Matthias P., Saffitz J.E., and McKenna W.J. A novel dominant mutation in plakoglobin causes arrhythmogenic right ventricular cardiomyopathy. Am. J. Hum. Genet. 81 (2007) 964-973
3. Behrens J., von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., and Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382 (1996) 638-642
4. Beis D., Bartman T., Jin S.W., Scott I.C., D'Amico L.A., Ober E.A., Verkade H., Frantsve J., Field H.A., Wehman A., Baier H., Tallafuss A., Bally-Cuif L., Chen J.N., Stainier D.Y., and Jungblut B. Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 132 (2005) 4193-4204
5. Bierkamp C., McLaughlin K.J., Schwarz H., Huber O., and Kemler R. Embryonic heart and skin defects in mice lacking plakoglobin. Dev. Biol. 180 (1996) 780-785
6. Bierkamp C., Schwarz H., Huber O., and Kemler R. Desmosomal localization of beta-catenin in the skin of plakoglobin null-mutant mice. Development 126 (1999) 371-381
7. Cerda J., Reidenbach S., Pratzel S., and Franke W.W. Cadherin-catenin complexes during zebrafish oogenesis: heterotypic junctions between oocytes and follicle cells. Biol. Reprod. 61 (1999) 692-704
8. Chitaev N.A., Leube R.E., Troyanovsky R.B., Eshkind L.G., Franke W.W., and Troyanovsky S.M. The binding of plakoglobin to desmosomal cadherins: patterns of binding sites and topogenic potential. J. Cell Biol. 133 (1996) 359-369
9. Detrich H.W., Kieran M., Chan F., Barone L., Yee K., Rundstadler J., Pratt S., Ransom D., and Zon L. Intraembryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. 92 (1995) 10713-10717
10. Dorsky R.I., Sheldahl L.C., and Moon R.T. A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev. Biol. 241 (2002) 229-237
11. Fekany K., Yamanaka Y., Leung T., Sirotkin H., Topczewski J., Gates M., Hibi M., Renucci A., Stemple D., Radbill A., Schier A., Driever W., Hirano T., Talbot W., and Solnica-Krezel L. The zebrafish bozozok locus encodes Dharma, a homeodomain protein essential for induction of gastrula organizer and dorsoanterior embryonic structures. Development 126 (1999) 1427-1438
12. Franke W.W., Goldschmidt M.D., Zimbelmann R., Mueller H.M., Schiller D.L., and Cowin P. Molecular cloning and amino acid sequence of human plakoglobin, the common junctional plaque protein. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 4027-4031
13. Fukunaga Y., Liu H., Shimizu M., Komiya S., Kawasuji M., and Nagafuchi A. Defining the roles of beta-catenin and plakoglobin in cell-cell adhesion: isolation of beta-catenin/plakoglobin-deficient F9 cells. Cell Struct. Funct. 30 (2005) 25-34
14. Garcia-Gras E., Lombardi R., Giocondo M.J., Willerson J.T., Schneider M.D., Khoury D.S., and Marian A.J. Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardiomyopathy. J. Clin. Invest. 116 (2006) 2012-2021
15. Garrod D., and Chidgey M. Desmosome structure, composition and function. Biochim. Biophys. Acta (BBA) - Biomembranes 1778 (2008) 572-587
16. Gerull B., Heuser A., Wichter T., Paul M., Basson C.T., McDermott D.A., Lerman B.B., Markowitz S.M., Ellinor P.T., MacRae C.A., Peters S., Grossmann K.S., Michely B., Sasse-Klaassen S., Birchmeier W., Dietz R., Breithardt G., Schulze-Bahr E., and Thierfelder L. Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy. Nat. Genet. 36 (2004) 1162-1164
17. Hashimoto H., Itoh M., Yamanaka Y., Yamashita S., Shimizu T., Solnica-Krezel L., Hibi M., and Hirano T. Zebrafish Dkk1 functions in forebrain specification and axial mesendoderm formation. Dev. Biol. 217 (2000) 138-152
18. Hauptmann G. Two-color detection of mRNA transcript localizations in fish and fly embryos using alkaline phosphatase and beta-galactosidase conjugated antibodies. Dev. Genes Evol. 209 (1999) 317-321
19. Heuser A., Plovie E.R., Ellinor P.T., Grossmann K.S., Shin J.T., Wichter T., Basson C.T., Lerman B.B., Sasse-Klaassen S., Thierfelder L., MacRae C.A., and Gerull B. Mutant desmocollin-2 causes arrhythmogenic right ventricular cardiomyopathy. Am. J. Hum. Genet. 79 (2006) 1081-1088
20. Hu P., Berkowitz P., O'Keefe E.J., and Rubenstein D.S. Keratinocyte adherens junctions initiate nuclear signaling by translocation of plakoglobin from the membrane to the nucleus. J. Investig. Dermatol. 121 (2003) 242-251
21. Huelsken J., Vogel R., Brinkmann V., Erdmann B., Birchmeier C., and Birchmeier W. Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148 (2000) 567-578
22. Hurlstone A.F.L., Haramis A.-P.G., Wienholds E., Begthel H., Korving J., Van Eeden F., Cuppen E., Zivkovic D., Plasterk R.H.A., and Clevers H. The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 425 (2003) 633-637
23. Karnovsky A., and Klymkowsky M. Anterior axis duplication in Xenopus induced by the over-expression of the cadherin-binding protein plakoglobin. Proc. Natl. Acad. Sci. 92 (1995) 4522-4526
24. Kirchhof P., Fabritz L., Zwiener M., Witt H., Schafers M., Zellerhoff S., Paul M., Athai T., Hiller K.-H., Baba H.A., Breithardt G., Ruiz P., Wichter T., and Levkau B. Age- and training-dependent development of arrhythmogenic right ventricular cardiomyopathy in heterozygous plakoglobin-deficient mice. Circulation 114 (2006) 1799-1806
25. Koch U., Wilson A., Cobas M., Kemler R., MacDonald H.R., and Radtke F. Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 111 (2008) 160-164
26. Lawson N.D., and Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248 (2002) 307-318
27. Leung T., Bischof J., Soll I., Niessing D., Zhang D., Ma J., Jackle H., and Driever W. Bozozok directly represses bmp2b transcription and mediates the earliest dorsoventral asymmetry of bmp2b expression in zebrafish. Development 130 (2003) 3639-3649
28. Li L., Chapman K., Hu X., Wong A., and Pasdar M. Modulation of the oncogenic potential of beta-catenin by the subcellular distribution of plakoglobin. Mol. Carcinog. 46 (2007) 824-838
29. Lickert H., Kutsch S., Kanzler B., Tamai Y., Taketo M.M., and Kemler R. Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev. Cell 3 (2002) 171-181
30. Link V., Shevchenko A., and Heisenberg C.P. Proteomics of early zebrafish embryos. BMC Dev. Biol. 6 (2006) 1
31. Loureiro J., and Peifer M. Roles of Armadillo, a Drosophila catenin, during central nervous system development. Curr. Biol. 8 (1998) 622-632
32. Lyons I., Parsons L.M., Hartley L., Li R., Andrews J.E., Robb L., and Harvey R.P. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9 (1995) 1654-1666
33. Maeda O., Usami N., Kondo M., Takahashi M., Goto H., Shimokata K., Kusugami K., and Sekido Y. Plakoglobin (gamma-catenin) has TCF/LEF family-dependent transcriptional activity in beta-catenin-deficient cell line. Oncogene 23 (2004) 964-972
34. Martin E.D., and Grealy M. Plakoglobin expression and localization in zebrafish embryo development. Biochem. Soc. Trans. 32 (2004) 797-798
35. McKoy G., Protonotarios N., Crosby A., Tsatsopoulou A., Anastasakis A., Coonar A., Norman M., Baboonian C., Jeffery S., and McKenna W.J. Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet 355 (2000) 2119-2124
36. Miravet S., Piedra J., Miro F., Itarte E., Garcia de Herreros A., and Dunach M. The transcriptional factor Tcf-4 contains different binding sites for beta-catenin and plakoglobin. J. Biol. Chem. 277 (2002) 1884-1891
37. Molenaar M., van de Wetering M., Oosterwegel M., Peterson-Maduro J., Godsave S., Korinek V., Roose J., Destree O., and Clevers H. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86 (1996) 391-399
38. Naito A.T., Shiojima I., Akazawa H., Hidaka K., Morisaki T., Kikuchi A., and Komuro I. Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc. Natl. Acad. Sci. 103 (2006) 19812-19817
39. Nakashima A., Katagiri T., and Tamura M. Cross-talk between Wnt and bone morphogenetic protein 2 (BMP-2) signaling in differentiation pathway of C2C12 myoblasts. J. Biol. Chem. 280 (2005) 37660-37668
40. O'Boyle S., Bree R.T., McLoughlin S., Grealy M., and Byrnes L. Identification of zygotic genes expressed at the midblastula transition in zebrafish. Biochem. Biophys. Res. Commun. 358 (2007) 462-468
41. Ozawa M., Nuruki K., Toyoyama H., and Ohi Y. Cloning of an alternative form of plakoglobin (gamma-catenin) lacking the fourth armadillo repeat. J. Biochem. 118 (1995) 836-840
42. Patterson L.J., Gering M., and Patient R. Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood 105 (2005) 3502-3511
43. Peifer M., and Wieschaus E. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63 (1990) 1167-1176
44. Peifer M., McCrea P.D., Green K.J., Wieschaus E., and Gumbiner B.M. The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J. Cell Biol. 118 (1992) 681-691
45. Peifer M., Berg S., and Reynolds A.B. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76 (1994) 789-791
46. Pieperhoff S., and Franke W.W. The area composita of adhering junctions connecting heart muscle cells of vertebrates - IV: coalescence and amalgamation of desmosomal and adhaerens junction components - late processes in mammalian heart development. Eur. J. Cell Biol. 86 (2007) 377-391
47. Pieperhoff S., and Franke W.W. The area composita of adhering junctions connecting heart muscle cells of vertebrates.: VI. Different precursor structures in non-mammalian species. Eur. J. Cell Biol. 87 (2008) 413-430
48. Pilichou K., Nava A., Basso C., Beffagna G., Bauce B., Lorenzon A., Frigo G., Vettori A., Valente M., Towbin J., Thiene G., Danieli G.A., and Rampazzo A. Mutations in Desmoglein-2 gene are associated with arrhythmogenic right ventricular cardiomyopathy. Circulation 113 (2006) 1171-1179
49. Rampazzo A., Nava A., Malacrida S., Beffagna G., Bauce B., Rossi V., Zimbello R., Simionati B., Basso C., Thiene G., Towbin J.A., and Danieli G.A. Mutation in human desmoplakin domain binding to plakoglobin causes a dominant form of arrhythmogenic right ventricular cardiomyopathy. Am. J. Hum. Genet. 71 (2002) 1200-1206
50. Ransom D.G., Haffter P., Odenthal J., Brownlie A., Vogelsang E., Kelsh R.N., Brand M., van Eeden F.J., Furutani-Seiki M., Granato M., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Mullins M.C., and Nusslein-Volhard C. Characterization of zebrafish mutants with defects in embryonic hematopoiesis. Development 123 (1996) 311-319
51. Ross S.E., Hemati N., Longo K.A., Bennett C.N., Lucas P.C., Erickson R.L., and MacDougald O.A. Inhibition of Adipogenesis by Wnt Signaling. Science 289 (2000) 950-953
52. Rubenstein A., Merriam J., and Klymkowsky M.W. Localizing the adhesive and signaling functions of plakoglobin. Dev. Genet. 20 (1997) 91-102
53. Ruiz P., Brinkmann V., Ledermann B., Behrend M., Grund C., Thalhammer C., Vogel F., Birchmeier C., Gunthert U., Franke W., and Birchmeier W. Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J. Cell Biol. 135 (1996) 215-225
54. Scherz P.J., Huisken J., Sahai-Hernandez P., and Stainier D.Y.R. High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development 135 (2008) 1179-1187
55. Shimizu T., Yamanaka Y., Ryu S.-L., Hashimoto H., Yabe T., Hirata T., Bae Y.-k., Hibi M., and Hirano T. Cooperative roles of Bozozok/Dharma and Nodal-related proteins in the formation of the dorsal organizer in zebrafish. Mech. Dev. 91 (2000) 293-303
56. Solnica-Krezel L., and Driever W. The role of the homeodomain protein Bozozok in zebrafish axis formation. Int. J. Dev. Biol. 45 (2001) 299-310
57. Stainier D.Y. Zebrafish genetics and vertebrate heart formation. Nat. Rev., Genet. 2 (2001) 39-48
58. Tay T.L., Lin Q., Seow T.K., Tan K.H., Hew C.L., and Gong Z. Proteomic analysis of protein profiles during early development of the zebrafish, Danio rerio. Proteomics 6 (2006) 3176-3188
59. Timmerman L.A., Grego-Bessa J., Raya A., Bertran E., Perez-Pomares J.M., Diez J., Aranda S., Palomo S., McCormick F., Izpisua-Belmonte J.C., and de la Pompa J.L. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18 (2004) 99-115
60. Troyanovsky R.B., Chitaev N.A., and Troyanovsky S.M. Cadherin binding sites of plakoglobin: localization, specificity and role in targeting to adhering junctions. J. Cell Sci. 109 (1996) 3069-3078
61. Tsatsopoulou A.A., Protonotarios N.I., and McKenna W.J. Arrhythmogenic right ventricular dysplasia, a cell adhesion cardiomyopathy: insights into disease pathogenesis from preliminary genotype-phenotype assessment. Heart 92 (2006) 1720-1723
62. Ueno S., Weidinger G., Osugi T., Kohn A.D., Golob J.L., Pabon L., Reinecke H., Moon R.T., and Murry C.E. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. 104 (2007) 9685-9690
63. van Es J.H., van Gijn M.E., Riccio O., van den Born M., Vooijs M., Begthel H., Cozijnsen M., Robine S., Winton D.J., Radtke F., and Clevers H. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435 (2005) 959-963
64. Wahl J.K., Sacco P.A., McGranahan-Sadler T.M., Sauppe L.M., Wheelock M.J., and Johnson K.R. Plakoglobin domains that define its association with the desmosomal cadherins and the classical cadherins: identification of unique and shared domains. J. Cell Sci. 109 (1996) 1143-1154
65. Walsh E.C., and Stainier D.Y. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293 (2001) 1670-1673
66. Westerfield M. The Zebrafish Book (1995), University of Oregon Press, Eugene
67. Westin J., and Lardelli M. Three Notch genes in zebrafish:implications for vertebrate Notch gene evoloution and function. Dev. Genes Evol. 207 (1997) 51-63
68. Yelon D., Horne S.A., and Stainier D.Y.R. Restricted Expression of Cardiac Myosin Genes Reveals Regulated Aspects of Heart Tube Assembly in Zebrafish. Dev. Biol. 214 (1999) 23-37
69. Zhou J., Qu J., Yi X.P., Graber K., Huber L., Wang X., Gerdes A.M., and Li F. Upregulation of gamma-catenin compensates for the loss of beta-catenin in adult cardiomyocytes. Am. J. Physiol., Heart Circ. Physiol. 292 (2007) H270-276
70. Zhurinsky J., Shtutman M., and Ben-Ze'ev A. Differential mechanisms of LEF/TCF Family-Dependent transcriptional activation by beta-catenin and plakoglobin. Mol. Cell. Biol. 20 (2000) 4238-4252