Tmem88 plays an essential role in pharyngeal pouch progenitor specification by inhibiting Wnt/β-catenin signaling
Jingwen Liu, Liping Yang, Zidong Lu, Qiang Wang
Tmem88 plays an essential role in pharyngeal pouch progenitor specification by inhibiting Wnt/β-catenin signaling
Pharyngeal pouches, which are endodermal outpockets that segment the pharyngeal arches, play a crucial role in the development of craniofacial skeletons in vertebrate embryos. Our previous study successfully identified pharyngeal pouch progenitors (PPPs) in zebrafish embryos and emphasized the significance of BMP2b signaling in their specification. However, the specific mechanism by which these progenitors originate from endodermal cells remains largely unknown. Here we found that the pharmacological activation of Wnt signaling pathway disrupts the emergence of PPPs and subsequently hinders the formation of pharyngeal pouches. Moreover, we have identified the expression of tmem88a and tmem88b (collectively known as tmem88a/b) in PPPs during the early-somite stages. Furthermore, the deficiency of tmem88a/b leads to an excessive accumulation of β-catenin in both the cytoplasm and nucleus of endodermal cells that are intended to differentiate into PPPs. Importantly, suppressing the hyperactivation of Wnt/β-catenin signaling through pharmacological treatment, the defects in PPP specification in tmem88a/b−/− mutants are successfully rescued. In summary, our findings establish a clear connection between the specification of PPPs and the regulation of Wnt signaling mediated by Tmem88. These results underscore the pivotal role of Tmem88 in the development of pharyngeal pouches.
Tmem88 / Wnt/β-catenin / pharyngeal pouch / progenitor / specification
[1] |
Graham A, Smith A. Patterning the pharyngeal arches. Bioessays 2001;23:54–61.
CrossRef
Google scholar
|
[2] |
Holzschuh J, Wada N, Wada C, et al. Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. Development 2005;132:3731–42.
CrossRef
Google scholar
|
[3] |
Crump JG, Maves L, Lawson ND, et al. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 2004;131:5703–16.
CrossRef
Google scholar
|
[4] |
Mao A, Zhang M, Li L, et al. Pharyngeal pouches provide a niche microenvironment for arch artery progenitor specification. Development 2021;148:dev192658.
CrossRef
Google scholar
|
[5] |
Ning G, Liu X, Dai M, et al. MicroRNA-92a upholds Bmp signaling by targeting noggin3 during pharyngeal cartilage formation. Dev Cell 2013;24:283–95.
CrossRef
Google scholar
|
[6] |
Mao A, Zhang M, Liu J, et al. PDGF signaling from pharyngeal pouches promotes arch artery morphogenesis. J Genet Genomics 2019;46:551–9.
CrossRef
Google scholar
|
[7] |
Miles B, Srinivasan VN. Embryology, Pharyngeal Pouch. Treasure Island, (FL): StatPearls, 2023.
|
[8] |
Frisdal A, Trainor PA. Development and evolution of the pharyngeal apparatus. Wiley Interdiscip Rev Dev Biol 2014;3: 403–18.
CrossRef
Google scholar
|
[9] |
Li LW, Ning GZ, Yang SY, et al. BMP signaling is required for nkx23-positive pharyngeal pouch progenitor specification in zebrafish. PLoS Genet 2019;15:e1007996.
CrossRef
Google scholar
|
[10] |
Lee HJ, Finkelstein D, Li XF, et al. Identification of transmembrane protein 88 (TMEM88) as a dishevelled-binding protein. J Biol Chem 2010;285:41549–56.
CrossRef
Google scholar
|
[11] |
Lee H, Evans T. TMEM88 inhibits Wnt signaling by promoting Wnt signalosome localization to multivesicular bodies. Iscience 2019;19:267–80.
CrossRef
Google scholar
|
[12] |
Palpant NJ, Pabon L, Rabinowitz JS, et al. Transmembrane protein 88: a Wnt regulatory protein that specifies cardiomyocyte development. Development 2013;140:3799–808.
CrossRef
Google scholar
|
[13] |
Zhang M, Liu J, Mao A, et al. Tmem88 confines ectodermal Wnt2bb signaling in pharyngeal arch artery progenitors for balancing cell cycle progression and cell fate decision. Nat Cardiovasc Res 2023;2:234–50.
CrossRef
Google scholar
|
[14] |
Ni TT, Rellinger EJ, Mukherjee A, et al. Discovering small molecules that promote cardiomyocyte generation by modulating Wnt signaling. Chem Biol. 2011;18:1658–68.
CrossRef
Google scholar
|
[15] |
Johansson M, Giger FA, Fielding T, et al. Dkk1 controls cell-cell interaction through regulation of non-nuclear beta-catenin pools. Dev Cell 2019;51:775–786.e3.
CrossRef
Google scholar
|
[16] |
Neelathi UM, Nogare DD, Chitnis AB. Cxcl12a induces snail1b expression to initiate collective migration and sequential Fgf-dependent neuromast formation in the zebrafish posterior lateral line primordium. Development 2018;145:dev162453.
CrossRef
Google scholar
|
[17] |
Meijer L, Skaltsounis AL, Magiatis P, et al. GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 2003;10:1255–66.
CrossRef
Google scholar
|
[18] |
Vandernoot I, Haerlingen B, Gillotay P, et al. Enhanced canonical Wnt signaling during early zebrafish development perturbs the interaction of cardiac mesoderm and pharyngeal endoderm and causes thyroid specification defects. Thyroid 2021;31:420–38.
CrossRef
Google scholar
|
[19] |
Eivers E, Demagny H, De Robertis EM. Integration of BMP and Wnt signaling via vertebrate Smad1/5/8 and Drosophila Mad. Cytokine Growth Factor Rev 2009;20:357–65.
CrossRef
Google scholar
|
[20] |
He XC, Zhang JW, Tong WG, et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 2004;36:1117–21.
CrossRef
Google scholar
|
[21] |
Polevoy H, Gutkovich YE, Michaelov A, et al. New roles for Wnt and BMP signaling in neural anteroposterior patterning. EMBO Rep 2019;20:e45842.
CrossRef
Google scholar
|
[22] |
Choe CP, Collazo A, Trinh LA, et al. Wnt-dependent epithelial transitions drive pharyngeal pouch formation. Dev Cell 2013;24:296–309.
CrossRef
Google scholar
|
[23] |
Gao J, Liao Y, Qiu M, et al. Wnt/beta-catenin signaling in neural stem cell homeostasis and neurological diseases. Neuroscientist 2021;27:58–72.
CrossRef
Google scholar
|
[24] |
Pinto D, Clevers H. Wnt control of stem cells and differentiation in the intestinal epithelium. Exp Cell Res 2005;306:357–63.
CrossRef
Google scholar
|
[25] |
Poulain M, Ober EA. Interplay between Wnt2 and Wnt2bb controls multiple steps of early foregut-derived organ development. Development 2011;138:3557–68.
CrossRef
Google scholar
|
/
〈 | 〉 |