{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:11:48Z","timestamp":1760148708691,"version":"build-2065373602"},"reference-count":71,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,5,31]],"date-time":"2023-05-31T00:00:00Z","timestamp":1685491200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Sciences Foundation","doi-asserted-by":"publisher","award":["IOS1349668"],"award-info":[{"award-number":["IOS1349668"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Jeffress Memorial (Virginia, USA)","award":["IOS1349668"],"award-info":[{"award-number":["IOS1349668"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JDB"],"abstract":"<jats:p>The mouth is a central feature of our face, without which we could not eat, breathe, or communicate. A critical and early event in mouth formation is the creation of a \u201chole\u201d which connects the digestive system and the external environment. This hole, which has also been called the primary or embryonic mouth in vertebrates, is initially covered by a 1\u20132 cell layer thick structure called the buccopharyngeal membrane. When the buccopharyngeal membrane does not rupture, it impairs early mouth functions and may also lead to further craniofacial malformations. Using a chemical screen in an animal model (Xenopus laevis) and genetic data from humans, we determined that Janus kinase 2 (Jak2) has a role in buccopharyngeal membrane rupture. We have determined that decreased Jak2 function, using antisense morpholinos or a pharmacological antagonist, caused a persistent buccopharyngeal membrane as well as the loss of jaw muscles. Surprisingly, we observed that the jaw muscle compartments were connected to the oral epithelium that is continuous with the buccopharyngeal membrane. Severing such connections resulted in buccopharyngeal membrane buckling and persistence. We also noted puncta accumulation of F-actin, an indicator of tension, in the buccopharyngeal membrane during perforation. Taken together, the data has led us to a hypothesis that muscles are required to exert tension across the buccopharyngeal membrane, and such tension is necessary for its perforation.<\/jats:p>","DOI":"10.3390\/jdb11020024","type":"journal-article","created":{"date-parts":[[2023,6,1]],"date-time":"2023-06-01T02:12:45Z","timestamp":1685585565000},"page":"24","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Jak2 and Jaw Muscles Are Required for Buccopharyngeal Membrane Perforation during Mouth Development"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1427-9140","authenticated-orcid":false,"given":"Amanda J. 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Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/j.1469-7580.2012.01540.x","article-title":"Development and evolution of the vertebrate primary mouth","volume":"222","author":"Soukup","year":"2013","journal-title":"J. Anat."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1002\/bies.10288","article-title":"About face: Signals and genes controlling jaw patterning and identity in vertebrates","volume":"25","author":"Richman","year":"2003","journal-title":"BioEssays News Rev. Mol. Cell. Dev. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2353","DOI":"10.1002\/dvdy.20833","article-title":"Recent advances in craniofacial morphogenesis","volume":"235","author":"Chai","year":"2006","journal-title":"Dev. Dyn."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Francis-West, P.H., Robson, L., and Evans, D.J.R. (2003). Craniofacial Development: The Tissue and Molecular Interactions That Control Development of the Head, Springer.","DOI":"10.1007\/978-3-642-55570-1"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.semcdb.2010.01.008","article-title":"Evolving maps in craniofacial development","volume":"Volume 21","author":"Gitton","year":"2010","journal-title":"Seminars in Cell & Developmental Biology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1242\/dev.01705","article-title":"New insights into craniofacial morphogenesis","volume":"132","author":"Helms","year":"2005","journal-title":"Development"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e275","DOI":"10.1002\/wdev.275","article-title":"Mouth development","volume":"6","author":"Chen","year":"2017","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1016\/j.celrep.2016.06.073","article-title":"Formation of a \u201cPre-mouth Array\u201d from the Extreme Anterior Domain Is Directed by Neural Crest and Wnt\/PCP Signaling","volume":"16","author":"Jacox","year":"2016","journal-title":"Cell Rep."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1016\/j.celrep.2014.06.026","article-title":"The extreme anterior domain is an essential craniofacial organizer acting through Kinin-Kallikrein signaling","volume":"8","author":"Jacox","year":"2014","journal-title":"Cell Rep."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1016\/S0022-3468(85)80021-X","article-title":"The role of amniotic fluid in fetal nutrition","volume":"20","author":"Mulvihill","year":"1985","journal-title":"J. Pediatr. Surg."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/j.semcdb.2007.04.002","article-title":"Positioning the extreme anterior in Xenopus: Cement gland, primary mouth and anterior pituitary","volume":"18","author":"Dickinson","year":"2007","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1242\/dev.032912","article-title":"The Wnt antagonists Frzb-1 and Crescent locally regulate basement membrane dissolution in the developing primary mouth","volume":"136","author":"Dickinson","year":"2009","journal-title":"Development"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/bs.ctdb.2021.01.001","article-title":"Modeling endoderm development and disease in Xenopus","volume":"145","author":"Edwards","year":"2021","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1002\/ar.1092100312","article-title":"The ultrastructure of oral (buccopharyngeal) membrane formation and rupture in the anuran embryo","volume":"210","author":"Watanabe","year":"1984","journal-title":"Anat. Rec."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/0012-1606(77)90088-4","article-title":"Ultrastructure of oral (buccopharyngeal) membrane formation and rupture in the hamster embryo","volume":"58","author":"Waterman","year":"1977","journal-title":"Dev. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1002\/ar.1092110412","article-title":"Formation and perforation of closing plates in the chick embryo","volume":"211","author":"Waterman","year":"1985","journal-title":"Anat. Rec."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1002\/ar.1091980407","article-title":"Indirect immunofluorescent staining of fibronectin associated with the floor of the foregut during formation and rupture of the oral membrane in the chick embryo","volume":"198","author":"Waterman","year":"1980","journal-title":"Anat. Rec."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1002\/ar.1091970408","article-title":"The ultrastructure of oral (buccopharyngeal) membrane formation and rupture in the chick embryo","volume":"197","author":"Waterman","year":"1980","journal-title":"Anat. Rec."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1097\/00006534-199610000-00020","article-title":"Persistent buccopharyngeal membrane: A report of two cases","volume":"98","author":"Agarwal","year":"1996","journal-title":"Plast. Reconstr. Surg."},{"key":"ref_22","first-page":"125","article-title":"Persistent buccopharyngeal membrane","volume":"17","author":"Arcand","year":"1988","journal-title":"J. Otolaryngol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1097\/00006534-197412000-00011","article-title":"Persistent buccopharyngeal membrane. Case report","volume":"54","author":"Chandra","year":"1974","journal-title":"Plast. Reconstr. Surg."},{"key":"ref_24","first-page":"260","article-title":"Persistent buccopharyngeal membrane","volume":"17","author":"Cotton","year":"1988","journal-title":"J. Otolaryngol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.ijporl.2013.08.041","article-title":"Novel airway findings in a patient with 1p36 deletion syndrome","volume":"78","author":"Ferril","year":"2014","journal-title":"Int. J. Pediatr. Otorhinolaryngol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1002\/ajmg.1320310203","article-title":"Holzgreve-Wagner-Rehder syndrome: Potter sequence associated with persistent buccopharyngeal membrane. A second observation","volume":"31","author":"Legius","year":"1988","journal-title":"Am. J. Med. Genet."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/0030-4220(90)90319-N","article-title":"Persistent buccopharyngeal membrane with cleft palate. A case report","volume":"69","author":"Pillai","year":"1990","journal-title":"Oral Surg. Oral Med. Oral Pathol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1177\/000348949310200305","article-title":"Congenital oral synechiae","volume":"102","author":"Gartlan","year":"1993","journal-title":"Ann. Otol. Rhinol. Laryngol."},{"key":"ref_29","first-page":"699","article-title":"Choanal atresia","volume":"92","author":"Assanasen","year":"2009","journal-title":"J. Med. Assoc. Thai"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/S0165-5876(01)00620-6","article-title":"Unilateral choanal atresia in identical twins: Case report and literature review","volume":"62","author":"Chia","year":"2002","journal-title":"Int. J. Pediatr. Otorhinolaryngol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3389\/fped.2015.00052","article-title":"Current Updates on Choanal Atresia","volume":"3","author":"Kwong","year":"2015","journal-title":"Front. Pediatr."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1164\/rccm.201108-1455CI","article-title":"Obstructive sleep apnea in infants","volume":"185","author":"Katz","year":"2012","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1097\/PRS.0000000000003928","article-title":"Choanal Atresia and Craniosynostosis: Development and Disease","volume":"141","author":"Lesciotto","year":"2018","journal-title":"Plast. Reconstr. Surg."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2383","DOI":"10.1093\/hmg\/ddab205","article-title":"Synergistic role of retinoic acid signaling and Gata3 during primitive choanae formation","volume":"30","author":"Kurosaka","year":"2021","journal-title":"Hum. Mol. Genet."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1093\/hmg\/ddx031","article-title":"Rdh10 loss-of-function and perturbed retinoid signaling underlies the etiology of choanal atresia","volume":"26","author":"Kurosaka","year":"2017","journal-title":"Hum. Mol. Genet."},{"key":"ref_36","first-page":"e50697","article-title":"Facial transplants in Xenopus laevis embryos","volume":"85","author":"Jacox","year":"2014","journal-title":"J. Vis. Exp."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1002\/dvdy.24470","article-title":"Role of JNK during buccopharyngeal membrane perforation, the last step of embryonic mouth formation","volume":"246","author":"Houssin","year":"2017","journal-title":"Dev. Dyn."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ydbio.2014.09.029","article-title":"Hedgehog activity controls opening of the primary mouth","volume":"396","author":"Tabler","year":"2014","journal-title":"Dev. Biol."},{"key":"ref_39","unstructured":"Sive, H., Grainger, R., and Harland, R. (2000). Early Development of Xenopus laevis: A Laboratory Manual, Cold Spring Harbor Laboratory Press."},{"key":"ref_40","unstructured":"Faber, J. (1967). Normal Table of Xenopus Laevis (Daudin): A Systematic and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis, North-Holland."},{"key":"ref_41","unstructured":"Nieuwkoop, P., and Faber, J. (1994). Normal table of Xenopus Laevis.(1967), Daudin."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1002\/pro.4218","article-title":"PANTHER: Making genome-scale phylogenetics accessible to all","volume":"31","author":"Thomas","year":"2022","journal-title":"Protein Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1016\/j.ajhg.2009.03.010","article-title":"DECIPHER: Database of Chromosomal Imbalance and Phenotype in Humans Using Ensembl Resources","volume":"84","author":"Firth","year":"2009","journal-title":"Am. J. Hum. Genet."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Della Gaspera, B., Armand, A.S., Lecolle, S., Charbonnier, F., and Chanoine, C. (2012). Mef2d acts upstream of muscle identity genes and couples lateral myogenesis to dermomyotome formation in Xenopus laevis. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0052359"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1111\/joa.12467","article-title":"Neurotransmitter signaling pathways required for normal development in Xenopus laevis embryos: A pharmacological survey screen","volume":"229","author":"Sullivan","year":"2016","journal-title":"J. Anat."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"3245","DOI":"10.1113\/JP271930","article-title":"Bioelectric signalling via potassium channels: A mechanism for craniofacial dysmorphogenesis in KCNJ2-associated Andersen-Tawil Syndrome","volume":"594","author":"Adams","year":"2016","journal-title":"J. Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/bs.ctdb.2015.07.022","article-title":"Craniofacial Muscle Development","volume":"115","author":"Michailovici","year":"2015","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1111\/j.1469-7580.2010.01315.x","article-title":"A role for FoxN3 in the development of cranial cartilages and muscles in Xenopus laevis (Amphibia: Anura: Pipidae) with special emphasis on the novel rostral cartilages","volume":"218","author":"Schmidt","year":"2011","journal-title":"J. Anat."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"6128","DOI":"10.1021\/bi026964f","article-title":"Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide","volume":"42","author":"Shaw","year":"2003","journal-title":"Biochemistry"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"R96","DOI":"10.1016\/j.cub.2011.12.010","article-title":"Actin filaments as tension sensors","volume":"22","author":"Galkin","year":"2012","journal-title":"Curr. Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.ccr.2005.08.010","article-title":"Tensional homeostasis and the malignant phenotype","volume":"8","author":"Paszek","year":"2005","journal-title":"Cancer Cell"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.ydbio.2012.07.026","article-title":"Muscle contraction controls skeletal morphogenesis through regulation of chondrocyte convergent extension","volume":"370","author":"Shwartz","year":"2012","journal-title":"Dev. Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e38069","DOI":"10.7554\/eLife.38069","article-title":"Mechanical force regulates tendon extracellular matrix organization and tenocyte morphogenesis through TGFbeta signaling","volume":"7","author":"Subramanian","year":"2018","journal-title":"eLife"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1093\/ejo\/cji074","article-title":"Developmental changes in craniofacial morphology in subjects with Duchenne muscular dystrophy","volume":"28","author":"Matsuyuki","year":"2006","journal-title":"Eur. J. Orthod."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/(SICI)1097-4687(199801)235:1<1::AID-JMOR1>3.0.CO;2-F","article-title":"The effects of muscular dystrophy on craniofacial growth in mice: A study of heterochrony and ontogenetic allometry","volume":"235","author":"Lightfoot","year":"1998","journal-title":"J. Morphol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1111\/j.1469-7580.2007.00730.x","article-title":"The effects of muscular dystrophy on the craniofacial shape of Mus musculus","volume":"210","author":"Jones","year":"2007","journal-title":"J. Anat."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/s41368-020-00110-4","article-title":"FACEts of mechanical regulation in the morphogenesis of craniofacial structures","volume":"13","author":"Du","year":"2021","journal-title":"Int. J. Oral Sci."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Grimaldi, A., Parada, C., and Chai, Y. (2015). A Comprehensive Study of Soft Palate Development in Mice. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0145018"},{"key":"ref_59","unstructured":"Hill, M.A. (2022, August 05). Embryology Buccopharyngeal Membrane. Available online: https:\/\/embryology.med.unsw.edu.au\/embryology\/index.php\/Buccopharyngeal_membrane."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.ydbio.2015.06.007","article-title":"Budgett\u2019s frog (Lepidobatrachus laevis): A new amphibian embryo for developmental biology","volume":"405","author":"Amin","year":"2015","journal-title":"Dev. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.ceb.2020.05.004","article-title":"Forced to communicate: Integration of mechanical and biochemical signaling in morphogenesis","volume":"66","author":"Kindberg","year":"2020","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"e44706","DOI":"10.7554\/eLife.44706","article-title":"Mechanically activated piezo channels modulate outflow tract valve development through the Yap1 and Klf2-Notch signaling axis","volume":"8","author":"Duchemin","year":"2019","journal-title":"eLife"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"947430","DOI":"10.3389\/fcell.2022.947430","article-title":"ECM-transmitted shear stress induces apoptotic cell extrusion in early breast gland development","volume":"10","author":"Friedland","year":"2022","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"110917","DOI":"10.1016\/j.jbiomech.2021.110917","article-title":"Mechanism of cell death of endothelial cells regulated by mechanical forces","volume":"131","author":"Zeng","year":"2022","journal-title":"J. Biomech."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.mod.2016.10.001","article-title":"Apoptotic forces in tissue morphogenesis","volume":"144","author":"Ambrosini","year":"2017","journal-title":"Mech. Dev."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1089\/dna.2019.5087","article-title":"Regulation of Hippo Signaling by Mechanical Signals and the Cytoskeleton","volume":"39","author":"Zhang","year":"2020","journal-title":"DNA Cell Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1038\/s41390-021-01843-6","article-title":"Mechanical strain triggers endothelial-to-mesenchymal transition of the endocardium in the immature heart","volume":"92","author":"Vorisek","year":"2022","journal-title":"Pediatr. Res."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"717404","DOI":"10.3389\/fcell.2021.717404","article-title":"Programmed Cell Death Not as Sledgehammer but as Chisel: Apoptosis in Normal and Abnormal Craniofacial Patterning and Development","volume":"9","author":"Compagnucci","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"287","DOI":"10.3389\/fonc.2018.00287","article-title":"\u201cDo We Know Jack\u201d About JAK? A Closer Look at JAK\/STAT Signaling Pathway","volume":"8","author":"Bousoik","year":"2018","journal-title":"Front. Oncol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Park, S.O., Wamsley, H.L., Bae, K., Hu, Z., Li, X., Choe, S.W., Slayton, W.B., Oh, S.P., Wagner, K.U., and Sayeski, P.P. (2013). Conditional deletion of Jak2 reveals an essential role in hematopoiesis throughout mouse ontogeny: Implications for Jak2 inhibition in humans. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0059675"},{"key":"ref_71","first-page":"e23282","article-title":"JAK-STAT pathway and myogenic differentiation","volume":"2","author":"Jang","year":"2013","journal-title":"Jakstat"}],"container-title":["Journal of Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2221-3759\/11\/2\/24\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:46:22Z","timestamp":1760125582000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2221-3759\/11\/2\/24"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,31]]},"references-count":71,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["jdb11020024"],"URL":"https:\/\/doi.org\/10.3390\/jdb11020024","relation":{},"ISSN":["2221-3759"],"issn-type":[{"type":"electronic","value":"2221-3759"}],"subject":[],"published":{"date-parts":[[2023,5,31]]}}}