Eph-Pak2a signaling regulates branching of the pharyngeal endoderm by inhibiting late-stage epithelial dynamics

Development (Cambridge)

Volumn 142, Issue 6, 2015, Pages 1089-1094

  Choe, Chong Pyo ^a   Gage Crump, J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Branching morphogenesis; Craniofacial; Eph ephrin; PAK; Pharyngeal pouches; Zebrafish

Indexed keywords

EPHRIN; EPHRIN B2; EPHRIN B2A; EPHRIN B3; EPHRIN B3B; EPHRIN B4A; EPHRIN RECEPTOR; P21 ACTIVATED KINASE 2; P21 ACTIVATED KINASE 2A; UNCLASSIFIED DRUG; UVOMORULIN; WNT4 PROTEIN; EPHRIN RECEPTOR B4; MORPHOLINO OLIGONUCLEOTIDE; PAK2A PROTEIN, ZEBRAFISH; PROTEIN SERINE THREONINE KINASE; ZEBRAFISH PROTEIN;

ANIMAL CELL; ARTICLE; BILAYER MEMBRANE; BRANCHING MORPHOGENESIS; CELL ADHESION; CELL MEMBRANE; CELL MIGRATION; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; ENDODERM; ENZYME ACTIVATION; EPITHELIUM CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEURAL CREST CELL; NONHUMAN; PHARYNGEAL POUCH; PHARYNX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; ZEBRA FISH; ANIMAL; BRANCHIAL ARCH; CONFOCAL MICROSCOPY; EMBRYOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; METABOLISM; MORPHOGENESIS; PHYSIOLOGY;

DANIO RERIO; VERTEBRATA;

ANIMALS; BRANCHIAL REGION; EPITHELIAL CELLS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; MICROSCOPY, CONFOCAL; MORPHOGENESIS; MORPHOLINOS; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, EPHB4; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84930532696     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.115774     Document Type: Article

References (27)

1. Buchner, D. A., Su, F., Yamaoka, J. S., Kamei, M., Shavit, J. A., Barthel, L. K., McGee, B., Amigo, J. D., Kim, S., Hanosh, A.W. et al. (2007). pak2a mutations cause cerebral hemorrhage in redhead zebrafish. Proc. Natl. Acad. Sci. USA 104, 13996-14001.
2. Cavodeassi, F., Ivanovitch, K. and Wilson, S. W. (2013). Eph/Ephrin signalling maintains eye field segregation from adjacent neural plate territories during forebrain morphogenesis. Development 140, 4193-4202.
3. Choe, C. P., Collazo, A., Trinh, L. A., Pan, L., Moens, C. B. and Crump, J. G. (2013). Wnt-dependent epithelial transitions drive pharyngeal pouch formation. Dev. Cell 24, 296-309.
4. Cowan, C. A. and Henkemeyer, M. (2001). The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413, 174-179.
5. Crump, J. G., Maves, L., Lawson, N. D., Weinstein, B. M. and Kimmel, C. B. (2004). An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 131, 5703-5716.
6. Das, A. and Crump, J. G. (2012). Bmps and id2a act upstream of Twist1 to restrict ectomesenchyme potential of the cranial neural crest. PLoS Genet. 8, e1002710.
7. Dravis, C., Yokoyama, N., Chumley, M. J., Cowan, C. A., Silvany, R. E., Shay, J., Baker, L. A. and Henkemeyer, M. (2004). Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev. Biol. 271, 272-290.
8. Graham, A. (2008). Deconstructing the pharyngeal metamere. J. Exp. Zool. B Mol. Dev. Evol. 310, 336-344.
9. Holmberg, J., Clarke, D. L. and Frisen, J. (2000). Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408, 203-206.
10. Kayser, M. S., Nolt, M. J. and Dalva, M. B. (2008). EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59, 56-69.
11. Klein, R. (2012). Eph/ephrin signalling during development. Development 139, 4105-4109.
12. Knaus, U. G., Morris, S., Dong, H. J., Chernoff, J. and Bokoch, G. M. (1995). Regulation of human leukocyte p21-activated kinases through G protein–coupled receptors. Science 269, 221-223.
13. Kullander, K. and Klein, R. (2002). Mechanisms and functions of Eph and ephrin signalling. Nat. Rev. Mol. Cell Biol. 3, 475-486.
14. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C.-B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
15. Manser, E., Leung, T., Salihuddin, H., Zhao, Z.-S. and Lim, L. (1994). A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46.
16. Martin, G. A., Bollag, G., McCormick, F. and Abo, A. (1995). A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J. 14, 1970-1978.
17. Sells, M. A., Knaus, U. G., Bagrodia, S., Ambrose, D. M., Bokoch, G. M. and Chernoff, J. (1997). Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7, 202-210.
18. Smith, A., Robinson, V., Patel, K. and Wilkinson, D. G. (1997). The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells. Curr. Biol. 7, 561-570.
19. Tallafuss, A. and Bally-Cuif, L. (2003). Tracing of her5 progeny in zebrafish transgenics reveals the dynamics of midbrain-hindbrain neurogenesis and maintenance. Development 130, 4307-4323.
20. Tang, Y., Chen, Z., Ambrose, D., Liu, J., Gibbs, J. B., Chernoff, J. and Field, J. (1997). Kinase-deficient Pak1 mutants inhibit Ras transformation of Rat-1 fibroblasts. Mol. Cell. Biol. 17, 4454-4464.
21. Tay, H. G., Ng, Y. W. and Manser, E. (2010). A vertebrate-specific Chp-PAK-PIX pathway maintains E-cadherin at adherens junctions during zebrafish epiboly. PLoS ONE 5, e10125.
22. Villasenor, A., Chong, D. C., Henkemeyer, M. and Cleaver, O. (2010). Epithelial dynamics of pancreatic branching morphogenesis. Development 137, 4295-4305.
23. Wang, Y.-C., Khan, Z., Kaschube, M. and Wieschaus, E. F. (2012). Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature 484, 390-393.
24. Wang, Y.-C., Khan, Z. and Wieschaus, E. F. (2013). Distinct Rap1 activity states control the extent of epithelial invagination via alpha-catenin. Dev. Cell 25, 299-309.
25. Xu, N.-J. and Henkemeyer, M. (2009). Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat. Neurosci. 12, 268-276.
26. Zisch, A. H., Kalo, M. S., Chong, L. D. and Pasquale, E. B. (1998). Complex formation between EphB2 and Src requires phosphorylation of tyrosine 611 in the EphB2 juxtamembrane region. Oncogene 16, 2657-2670.
27. Zuniga, E., Rippen, M., Alexander, C., Schilling, T. F. and Crump, J. G. (2011). Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton. Development 138, 5147-5156.