Avian Facial Morphogenesis Is Regulated by c-Jun N-terminal Kinase/Planar Cell Polarity (JNK/PCP) Wingless-related (WNT) Signaling

Geetha-Loganathan, Poongodi; Nimmagadda, Suresh; Fu, Katherine; Richman, Joy M.

doi:10.1074/jbc.m113.522003

Cited by 28 publications

(53 citation statements)

References 78 publications

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“…S6). This reporter was activated by LiCl as shown previously (Geetha-Loganathan et al, 2014;Hosseini-Farahabadi et al, 2013). Significant activation by Noggin was observed at certain concentrations but not by RA (Fig.…”

Section: Cross Talk Between Noggin Ra and Wnt Pathwaysmentioning

confidence: 57%

Identification and functional analysis of novel facial patterning genes in the duplicated beak chicken embryo

Nimmagadda

Buchtová

et al. 2015

Developmental Biology

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Cranial neural crest cells form the majority of the facial skeleton. However exactly when the pattering information and hence jaw identity is established is not clear. We know that premigratory neural crest cells contain a limited amount of information about the lower jaw but the upper jaw and facial midline are specified later by local tissue interactions. The environmental signals leading to frontonasal identity have been explored by our group in the past. Altering the levels of two signaling pathways (Bone Morphogenetic Protein) and retinoic acid (RA) in the chicken embryo creates a duplicated midline on the side of the upper beak complete with egg tooth in place of maxillary derivatives (Lee et al., 2001). Here we analyze the transcriptome 16 h after bead placement in order to identify potential mediators of the identity change in the maxillary prominence. The gene list included RA, BMP and WNT signaling pathway genes as well as transcription factors expressed in craniofacial development. There was also cross talk between Noggin and RA such that Noggin activated the RA pathway. We also observed expression changes in several poorly characterized genes including the upregulation of Peptidase Inhibitor-15 (PI15). We tested the functional effects of PI15 overexpression with a retroviral misexpression strategy. PI15 virus induced a cleft beak analogous to human cleft lip. We next asked whether PI15 effects were mediated by changes in expression of major clefting genes and genes in the retinoid signaling pathway. Expression of TP63, TBX22, BMP4 and FOXE1, all human clefting genes, were upregulated. In addition, ALDH1A2, ALDH1A3 and RA target, RARβ were increased while the degradation enzyme CYP26A1 was decreased. Together these changes were consistent with activation of the RA pathway. Furthermore, PI15 retrovirus injected into the face was able to replace RA and synergize with Noggin to induce beak transformations. We conclude that the microarrays have generated a rich dataset containing genes with important roles in facial morphogenesis. Moreover, one of these facial genes, PI15 is a putative clefting gene and is in a positive feedback loop with RA.

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Section: Cross Talk Between Noggin Ra and Wnt Pathwaysmentioning

confidence: 57%

Identification and functional analysis of novel facial patterning genes in the duplicated beak chicken embryo

Nimmagadda

Buchtová

et al. 2015

Developmental Biology

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“…This intricate signaling crosstalk coordinates the convergent growth and morphogenesis of the facial prominences that is essential for aligning these structures prior to fusion (e.g. Geetha-Loganathan et al, 2014; Green et al, 2015; Hu et al, 2015; Linde-Medina et al, 2016; Suzuki et al, 2016). Subsequent interactions between the apposed epithelia then consummate lip and palate fusion (reviewed in Kousa and Schutte, 2016).…”

Section: Introductionmentioning

confidence: 99%

Systems biology of facial development: contributions of ectoderm and mesenchyme

Hooper

Feng

et al. 2017

Developmental Biology

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The rapid increase in gene-centric biological knowledge coupled with analytic approaches for genomewide data integration provides an opportunity to develop systems-level understanding of facial development. Experimental analyses have demonstrated the importance of signaling between the surface ectoderm and the underlying mesenchyme in coordinating facial patterning. However, current transcriptome data from the developing vertebrate face is dominated by the mesenchymal component, and the contributions of the ectoderm are not easily identified. We have generated transcriptome datasets from critical periods of mouse face formation that enable gene expression to be analyzed with respect to time, prominence, and tissue layer. Notably, by separating the ectoderm and mesenchyme we considerably improved the sensitivity compared to data obtained from whole prominences, with more genes detected over a wider dynamic range. From these data we generated a detailed description of ectoderm-specific developmental programs, including pan-ectodermal programs, prominence- specific programs and their temporal dynamics. The genes and pathways represented in these programs provide mechanistic insights into several aspects of ectodermal development. We also used these data to identify co-expression modules specific to facial development. We then used 14 co-expression modules enriched for genes involved in orofacial clefts to make specific mechanistic predictions about genes involved in tongue specification, in nasal process patterning and in jaw development. Our multidimensional gene expression dataset is a unique resource for systems analysis of the developing face; our co-expression modules are a resource for predicting functions of poorly annotated genes, or for predicting roles for genes that have yet to be studied in the context of facial development; and our analytic approaches provide a paradigm for analysis of other complex developmental programs.

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“…Pharyngeal endoderm, and neural and non‐neural ectoderm function as key epithelial signaling centers by releasing complex combinations of secreted molecules from well‐characterized pathways including Bone Morphogenetic Protein (BMP), Sonic Hedgehog (SHH), Fibroblast Growth Factor (FGF), and Wingless‐Related (WNT) that are indispensable to the proper patterning and differentiation of neural crest mesenchyme (Alvarado‐Mallart, ; Anderson, Lawrence, Stottmann, Bachiller, & Klingensmith, ; Barlow & Francis‐West, ; Benouaiche, Gitton, Vincent, Couly, & Levi, ; Cela et al, ; Crump et al, ; Ekker et al, ; Francis‐West, Ladher, Barlow, & Graveson, ; Gitton et al, ; Graham, ; Marcucio et al, ; Marcucio, Young, Hu, & Hallgrimsson, ; Pera, Stein, & Kessel, ; Piotrowski & Nusslein‐Volhard, ; Sasai & De Robertis, ; Schneider, Hu, Rubenstein, Maden, & Helms, ; Shimamura, Hartigan, Martinez, Puelles, & Rubenstein, ; Veitch et al, ; Wilson & Tucker, ; Withington, Beddington, & Cooke, ; Xu et al, ). Various members and targets of these pathways also become differentially regulated not only as a mechanism to support the outgrowth of the jaw and facial skeletons (Abzhanov & Tabin, ; Ashique, Fu, & Richman, ; Chong et al, ; Cordero, Schneider, & Helms, ; Couly et al, ; Doufexi & Mina, ; Geetha‐Loganathan, Nimmagadda, Fu, & Richman, ; Havens et al, ; Helms & Schneider, ; Hu, Colnot, & Marcucio, ; Hu et al, ; Liu et al, ; MacDonald, Abbott, & Richman, ; Melnick, Witcher, Bringas, Carlsson, & Jaskoll, ; Miller et al, ; Mina, Wang, Ivanisevic, Upholt, & Rodgers, ; Nimmagadda et al, ; Richman, Herbert, Matovinovic, & Walin, ; Rowe, Richman, & Brickell, ; Schneider, Hu, & Helms, ; Schneider et al, ; Szabo‐Rogers, Geetha‐Loganathan, Nimmagadda, Fu, & Richman, ; Wada et al, ; Young, Chong, Hu, Hallgrimsson, & Marcucio, ) but also as a component of regulating species‐specific size and shape (Abramyan, Leung, &...…”

Section: Origin Of Species‐specific Versus Species‐generic Aspects Ofmentioning

confidence: 99%

“…Benouaiche, Gitton, Vincent, Couly, & Levi, 2008;Cela et al, 2016;Crump et al, 2004;Ekker et al, 1995;Francis-West, Ladher, Barlow, & Graveson, 1998;Gitton et al, 2010;Graham, 2003;Marcucio et al, 2005;Marcucio, Young, Hu, & Hallgrimsson, 2011;Pera, Stein, & Kessel, 1999;Piotrowski & Nusslein-Volhard, 2000;Sasai & De Robertis, 1997;Schneider, Hu, Rubenstein, Maden, & Helms, 2001;Shimamura, Hartigan, Martinez, Puelles, & Rubenstein, 1995;Veitch et al, 1999;Wilson & Tucker, 2004;Withington, Beddington, & Cooke, 2001;Xu et al, 2015). Various members and targets of these pathways also become differentially regulated not only as a mechanism to support the outgrowth of the jaw and facial skeletons Ashique, Fu, & Richman, 2002a;Chong et al, 2012;Cordero, Schneider, & Helms, 2002;Couly et al, 2002;Doufexi & Mina, 2008;Geetha-Loganathan, Nimmagadda, Fu, & Richman, 2014;Havens et al, 2008;Hu, Colnot, & Marcucio, 2008;Hu et al, 2003;Liu et al, 2005;MacDonald, Abbott, & Richman, 2004;Melnick, Witcher, Bringas, Carlsson, & Jaskoll, 2005;Miller et al, 2000;Mina, Wang, Ivanisevic, Upholt, & Rodgers, 2002;Nimmagadda et al, 2015;Richman, Herbert, Matovinovic, & Walin, 1997;…”

Section: Origin Of Species-specific Versus Species-generic Aspects mentioning

confidence: 99%

Neural crest and the origin of species‐specific pattern

Schneider

2018

Genesis

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SummaryFor well over half of the 150 years since the discovery of the neural crest, the special ability of these cells to function as a source of species‐specific pattern has been clearly recognized. Initially, this observation arose in association with chimeric transplant experiments among differentially pigmented amphibians, where the neural crest origin for melanocytes had been duly noted. Shortly thereafter, the role of cranial neural crest cells in transmitting species‐specific information on size and shape to the pharyngeal arch skeleton as well as in regulating the timing of its differentiation became readily apparent. Since then, what has emerged is a deeper understanding of how the neural crest accomplishes such a presumably difficult mission, and this includes a more complete picture of the molecular and cellular programs whereby neural crest shapes the face of each species. This review covers studies on a broad range of vertebrates and describes neural‐crest‐mediated mechanisms that endow the craniofacial complex with species‐specific pattern. A major focus is on experiments in quail and duck embryos that reveal a hierarchy of cell‐autonomous and non‐autonomous signaling interactions through which neural crest generates species‐specific pattern in the craniofacial integument, skeleton, and musculature. By controlling size and shape throughout the development of these systems, the neural crest underlies the structural and functional integration of the craniofacial complex during evolution.

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Avian Facial Morphogenesis Is Regulated by c-Jun N-terminal Kinase/Planar Cell Polarity (JNK/PCP) Wingless-related (WNT) Signaling

Cited by 28 publications

References 78 publications

Identification and functional analysis of novel facial patterning genes in the duplicated beak chicken embryo

Identification and functional analysis of novel facial patterning genes in the duplicated beak chicken embryo

Systems biology of facial development: contributions of ectoderm and mesenchyme

Neural crest and the origin of species‐specific pattern

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