Artículos de revistas
Dact Gene Expression Profiles Suggest A Role For This Gene Family In Integrating Wnt And Tgf-β Signaling Pathways During Chicken Limb Development
Registro en:
Developmental Dynamics. , v. 243, n. 3, p. 428 - 439, 2014.
10588388
10.1002/dvdy.23948
2-s2.0-84894267451
Autor
Sensiate L.A.
Sobreira D.R.
Da Veiga F.C.
Peterlini D.J.
Pedrosa A.V.
Rirsch T.
Joazeiro P.P.
Schubert F.R.
Collares-Buzato C.B.
Xavier-Neto J.
Dietrich S.
Alvares L.E.
Institución
Resumen
Background: Dact gene family encodes multifunctional proteins that are important modulators of Wnt and TGF-β signaling pathways. Given that these pathways coordinate multiple steps of limb development, we investigated the expression pattern of the two chicken Dact genes (Dact1 and Dact2) from early limb bud up to stages when several tissues are differentiating. Results: During early limb development (HH24-HH30) Dact1 and Dact2 were mainly expressed in the cartilaginous rudiments of the appendicular skeleton and perichondrium, presenting expression profiles related, but distinct. At later stages of development (HH31-HH35), the main sites of Dact1 and Dact2 expression were the developing synovial joints. In this context, Dact1 expression was shown to co-localize with regions enriched in the nuclear β-catenin protein, such as developing joint capsule and interzone. In contrast, Dact2 expression was restricted to the interzone surrounding the domains of bmpR-1b expression, a TGF-β receptor with crucial roles during digit morphogenesis. Additional sites of Dact expression were the developing tendons and digit blastemas. Conclusions: Our data indicate that Dact genes are good candidates to modulate and, possibly, integrate Wnt and TGF-β signaling during limb development, bringing new and interesting perspectives about the roles of Dact molecules in limb birth defects and human diseases. Developmental Dynamics 243:428-439, 2014. © 2013 Wiley Periodicals, Inc. 243 3 428 439 Akiyama, H., Chaboissier, M.C., Martin, J.F., Schedl, A., de Crombrugghe, B., The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6 (2002) Genes Dev, 16, pp. 2813-2828 Alvares, L.E., Winterbottom, F.L., Jorge, E.C., Rodrigues Sobreira, D., Xavier-Neto, J., Schubert, F.R., Dietrich, S., Chicken dapper genes are versatile markers for mesodermal tissues, embryonic muscle stem cells, neural crest cells, and neurogenic placodes (2009) Dev Dyn, 238, pp. 1166-1178 Bober, E., Brand-Saberi, B., Ebensperger, C., Wilting, J., Balling, R., Paterson, B.M., Arnold, H.H., Christ, B., Initial steps of myogenesis in somites are independent of influence from axial structures (1994) Development, 120, pp. 3073-3082 Brott, B.K., Sokol, S.Y., Frodo proteins: modulators of Wnt signaling in vertebrate development (2005) Differentiation, 73, pp. 323-329 Brott, B.K., Sokol, S.Y., A vertebrate homolog of the cell cycle regulator Dbf4 is an inhibitor of Wnt signaling required for heart development (2005) Dev Cell, 8, pp. 703-715 Cheyette, B.N., Waxman, J.S., Miller, J.R., Takemaru, K., Sheldahl, L.C., Khlebtsova, N., Fox, E.P., Moon, R.T., Dapper, a Dishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation (2002) Dev Cell, 2, pp. 449-461 Chimal-Monroy, J., Rodriguez-Leon, J., Montero, J.A., Ganan, Y., Macias, D., Merino, R., Hurle, J.M., Analysis of the molecular cascade responsible for mesodermal limb chondrogenesis: Sox genes and BMP signaling (2003) Dev Biol, 257, pp. 292-301 DeLise, A.M., Fischer, L., Tuan, R.S., Cellular interactions and signaling in cartilage development (2000) Osteoarthrit Cartil, 8, pp. 309-334 Duprez, D., Bell, E.J., Richardson, M.K., Archer, C.W., Wolpert, L., Brickell, P.M., Francis-West, P.H., Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb (1996) Mech Dev, 57, pp. 145-157 Duprez, D.M., Kostakopoulou, K., Francis-West, P.H., Tickle, C., Brickell, P.M., Activation of Fgf-4 and HoxD gene expression by BMP-2 expressing cells in the developing chick limb (1996) Development, 122, pp. 1821-1828 Fischer, L., Boland, G., Tuan, R.S., Wnt signaling during BMP-2 stimulation of mesenchymal chondrogenesis (2002) J Cell Biochem, 84, pp. 816-831 Fisher, D.A., Kivimae, S., Hoshino, J., Suriben, R., Martin, P.M., Baxter, N., Cheyette, B.N., Three Dact gene family members are expressed during embryonic development and in the adult brains of mice (2006) Dev Dyn, 235, pp. 2620-2630 Francis-West, P.H., Abdelfattah, A., Chen, P., Allen, C., Parish, J., Ladher, R., Allen, S., Archer, C.W., Mechanisms of GDF-5 action during skeletal development (1999) Development, 126, pp. 1305-1315 Ganan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M.A., Hurle, J.M., Role of TGF beta s and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod (1996) Development, 122, pp. 2349-2357 Gao, X., Wen, J., Zhang, L., Li, X., Ning, Y., Meng, A., Chen, Y.G., Dapper1 is a nucleocytoplasmic shuttling protein that negatively modulates Wnt signaling in the nucleus (2008) J Biol Chem, 283, pp. 35679-35688 Gillhouse, M., Wagner Nyholm, M., Hikasa, H., Sokol, S.Y., Grinblat, Y., Two Frodo/Dapper homologs are expressed in the developing brain and mesoderm of zebrafish (2004) Dev Dyn, 230, pp. 403-409 Gloy, J., Hikasa, H., Sokol, S.Y., Frodo interacts with Dishevelled to transduce Wnt signals (2002) Nat Cell Biol, 4, pp. 351-357 Goulding, M., Lumsden, A., Paquette, A.J., Regulation of Pax-3 expression in the dermomyotome and its role in muscle development (1994) Development, 120, pp. 957-971 Hamburger, V., Hamilton, H.L., A series of normal stages in the development of the chick embryo (1992) Dev Dyn, 195, pp. 231-272. , 1951 Hartmann, C., Tabin, C.J., Dual roles of Wnt signaling during chondrogenesis in the chicken limb (2000) Development, 127, pp. 3141-3159 Hartmann, C., Tabin, C.J., Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton (2001) Cell, 104, pp. 341-351 Healy, C., Uwanogho, D., Sharpe, P.T., Expression of the chicken Sox9 gene marks the onset of cartilage differentiation (1996) Ann NY Acad Sci, 785, pp. 261-262 Hikasa, H., Sokol, S.Y., The involvement of Frodo in TCF-dependent signaling and neural tissue development (2004) Development, 131, pp. 4725-4734 Jia, Y., Yang, Y., Brock, M.V., Zhan, Q., Herman, J.G., Guo, M., Epigenetic regulation of DACT2, a key component of the Wnt signaling pathway in human lung cancer (2012) J Pathol. Jiang, X., Tan, J., Li, J., Kivimae, S., Yang, X., Zhuang, L., Lee, P.L., Yu, Q., DACT3 is an epigenetic regulator of Wnt/beta-catenin signaling in colorectal cancer and is a therapeutic target of histone modifications (2008) Cancer Cell, 13, pp. 529-541 Kardon, G., Harfe, B.D., Tabin, C.J., A Tcf4-positive mesodermal population provides a prepattern for vertebrate limb muscle patterning (2003) Dev Cell, 5, pp. 937-944 Kawakami, Y., Capdevila, J., Buscher, D., Itoh, T., Rodriguez Esteban, C., Izpisua Belmonte, J.C., WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo (2001) Cell, 104, pp. 891-900 Kettunen, P., Kivimae, S., Keshari, P., Klein, O.D., Cheyette, B.N., Luukko, K., Dact1-3 mRNAs exhibit distinct expression domains during tooth development (2010) Gene Expr Patterns, 10, pp. 140-143 Kivimae, S., Yang, X.Y., Cheyette, B.N., All Dact (Dapper/Frodo) scaffold proteins dimerize and exhibit conserved interactions with Vangl, Dvl, and serine/threonine kinases (2011) BMC Biochem, 12, p. 33 Kulyk, W.M., Upholt, W.B., Kosher, R.A., Fibronectin gene expression during limb cartilage differentiation (1989) Development, 106, pp. 449-455 Ladher, R.K., Church, V.L., Allen, S., Robson, L., Abdelfattah, A., Brown, N.A., Hattersley, G., Francis-West, P.H., Cloning and expression of the Wnt antagonists Sfrp-2 and Frzb during chick development (2000) Dev Biol, 218, pp. 183-198 Lagathu, C., Christodoulides, C., Virtue, S., Cawthorn, W.P., Franzin, C., Kimber, W.A., Nora, E.D., Sethi, J.K., Dact1, a nutritionally regulated preadipocyte gene, controls adipogenesis by coordinating the Wnt/beta-catenin signaling network (2009) Diabetes, 58, pp. 609-619 Lee, W.C., Hough, M.T., Liu, W., Ekiert, R., Lindstrom, N.O., Hohenstein, P., Davies, J.A., Dact2 is expressed in the developing ureteric bud/collecting duct system of the kidney and controls morphogenetic behavior of collecting duct cells (2010) Am J Physiol Renal Physiol, 299, pp. F740-F751 Meng, F., Cheng, X., Yang, L., Hou, N., Yang, X., Meng, A., Accelerated re-epithelialization in Dpr2-deficient mice is associated with enhanced response to TGFbeta signaling (2008) J Cell Sci, 121, pp. 2904-2912 Merino, R., Ganan, Y., Macias, D., Economides, A.N., Sampath, K.T., Hurle, J.M., Morphogenesis of digits in the avian limb is controlled by FGFs, TGFbetas, and noggin through BMP signaling (1998) Dev Biol, 200, pp. 35-45 Merino, R., Macias, D., Ganan, Y., Rodriguez-Leon, J., Economides, A.N., Rodriguez-Esteban, C., Izpisua-Belmonte, J.C., Hurle, J.M., Control of digit formation by activin signalling (1999) Development, 126, pp. 2161-2170 Merino, R., Rodriguez-Leon, J., Macias, D., Ganan, Y., Economides, A.N., Hurle, J.M., The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb (1999) Development, 126, pp. 5515-5522 Millan, F.A., Denhez, F., Kondaiah, P., Akhurst, R.J., Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo (1991) Development, 111, pp. 131-143 Montero, J.A., Lorda-Diez, C.I., Ganan, Y., Macias, D., Hurle, J.M., Activin/TGFbeta and BMP crosstalk determines digit chondrogenesis (2008) Dev Biol, 321, pp. 343-356 Moore, M.A., Gotoh, Y., Rafidi, K., Gerstenfeld, L.C., Characterization of a cDNA for chicken osteopontin: expression during bone development, osteoblast differentiation, and tissue distribution (1991) Biochemistry, 30, pp. 2501-2508 Moorman, A.F., Houweling, A.C., de Boer, P.A., Christoffels, V.M., Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol (2001) J Histochem Cytochem, 49, pp. 1-8 Mootoosamy, R.C., Dietrich, S., Distinct regulatory cascades for head and trunk myogenesis (2002) Development, 129, pp. 573-583 Newman, S.A., Bhat, R., Activator-inhibitor dynamics of vertebrate limb pattern formation (2007) Birth Defects Res C Embryo Today, 81, pp. 305-319 Riddle, R.D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T.M., Tabin, C., Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb (1995) Cell, 83, pp. 631-640 Schweitzer, R., Chyung, J.H., Murtaugh, L.C., Brent, A.E., Rosen, V., Olson, E.N., Lassar, A., Tabin, C.J., Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments (2001) Development, 128, pp. 3855-3866 Schweitzer, R., Zelzer, E., Volk, T., Connecting muscles to tendons: tendons and musculoskeletal development in flies and vertebrates (2010) Development, 137, pp. 2807-2817 Smith, A., Graham, A., Restricting Bmp-4 mediated apoptosis in hindbrain neural crest (2001) Dev Dyn, 220, pp. 276-283 Spater, D., Hill, T.P., O'Sullivan, R.J., Gruber, M., Conner, D.A., Hartmann, C., Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis (2006) Development, 133, pp. 3039-3049 Storm, E.E., Kingsley, D.M., GDF5 coordinates bone and joint formation during digit development (1999) Dev Biol, 209, pp. 11-27 Suriben, R., Kivimae, S., Fisher, D.A., Moon, R.T., Cheyette, B.N., Posterior malformations in Dact1 mutant mice arise through misregulated Vangl2 at the primitive streak (2009) Nat Genet, 41, pp. 977-985 ten Berge, D., Brugmann, S.A., Helms, J.A., Nusse, R., Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development (2008) Development, 135, pp. 3247-3257 Teran, E., Branscomb, A.D., Seeling, J.M., Dpr Acts as a molecular switch, inhibiting Wnt signaling when unphosphorylated, but promoting Wnt signaling when phosphorylated by casein kinase Idelta/epsilon (2009) PLoS One, 4, pp. e5522 Topol, L., Chen, W., Song, H., Day, T.F., Yang, Y., Sox9 inhibits Wnt signaling by promoting beta-catenin phosphorylation in the nucleus (2009) J Biol Chem, 284, pp. 3323-3333 Tylzanowski, P., De Valck, D., Maes, V., Peeters, J., Luyten, F.P., Zfhx1a and Zfhx1b mRNAs have non-overlapping expression domains during chick and mouse midgestation limb development (2003) Gene Expr Patterns, 3, pp. 39-42 Vortkamp, A., Lee, K., Lanske, B., Segre, G.V., Kronenberg, H.M., Tabin, C.J., Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein (1996) Science, 273, pp. 613-622 Waxman, J.S., Hocking, A.M., Stoick, C.L., Moon, R.T., Zebrafish Dapper1 and Dapper2 play distinct roles in Wnt-mediated developmental processes (2004) Development, 131, pp. 5909-5921 Welten, M.C., Verbeek, F.J., Meijer, A.H., Richardson, M.K., Gene expression and digit homology in the chicken embryo wing (2005) Evol Dev, 7, pp. 18-28 Widelitz, R.B., Jiang, T.X., Murray, B.A., Chuong, C.M., Adhesion molecules in skeletogenesis: II. Neural cell adhesion molecules mediate precartilaginous mesenchymal condensations and enhance chondrogenesis (1993) J Cell Physiol, 156, pp. 399-411 Witte, F., Dokas, J., Neuendorf, F., Mundlos, S., Stricker, S., Comprehensive expression analysis of all Wnt genes and their major secreted antagonists during mouse limb development and cartilage differentiation (2009) Gene Expr Patterns, 9, pp. 215-223 Witte, F., Chan, D., Economides, A.N., Mundlos, S., Stricker, S., Receptor tyrosine kinase-like orphan receptor 2 (ROR2) and Indian hedgehog regulate digit outgrowth mediated by the phalanx-forming region (2010), 107, pp. 14211-14216. , Proc Natl Acad Sci USAXi, S., Yang, M., Tao, Y., Xu, H., Shan, J., Inchauste, S., Zhang, M., Schrump, D.S., Cigarette smoke induces C/EBP-beta-mediated activation of miR-31 in normal human respiratory epithelia and lung cancer cells (2010) PLoS One, 5, pp. e13764 Yamaguchi, T.P., Bradley, A., McMahon, A.P., Jones, S., A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo (1999) Development, 126, pp. 1211-1223 Yang, Y., Niswander, L., Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning (1995) Cell, 80, pp. 939-947 Yang, Y., Topol, L., Lee, H., Wu, J., Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation (2003) Development, 130, pp. 1003-1015 Yau, T.O., Chan, C.Y., Chan, K.L., Lee, M.F., Wong, C.M., Fan, S.T., Ng, I.O., HDPR1, a novel inhibitor of the WNT/beta-catenin signaling, is frequently downregulated in hepatocellular carcinoma: involvement of methylation-mediated gene silencing (2005) Oncogene, 24, pp. 1607-1614 Zhang, L., Zhou, H., Su, Y., Sun, Z., Zhang, H., Zhang, Y., Ning, Y., Meng, A., Zebrafish Dpr2 inhibits mesoderm induction by promoting degradation of nodal receptors (2004) Science, 306, pp. 114-117 Zhang, L., Gao, X., Wen, J., Ning, Y., Chen, Y.G., Dapper 1 antagonizes Wnt signaling by promoting dishevelled degradation (2006) J Biol Chem, 281, pp. 8607-8612 Zou, H., Niswander, L., Requirement for BMP signaling in interdigital apoptosis and scale formation (1996) Science, 272, pp. 738-741