Pleiotropic function of Dlx5/6 in the development of mammalian vocal and auditory organs
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
41329676
PubMed Central
PMC12671821
DOI
10.1371/journal.pone.0337426
PII: PONE-D-25-24912
Knihovny.cz E-zdroje
- MeSH
- homeodoménové proteiny * genetika metabolismus MeSH
- morfogeneze MeSH
- myši MeSH
- signální transdukce MeSH
- transkripční faktory SOXE metabolismus genetika MeSH
- transkripční faktory * genetika metabolismus MeSH
- ucho * embryologie MeSH
- vokalizace zvířat * fyziologie MeSH
- vývojová regulace genové exprese MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- Dlx5 protein, mouse MeSH Prohlížeč
- Dlx6 protein, mouse MeSH Prohlížeč
- homeodoménové proteiny * MeSH
- transkripční faktory SOXE MeSH
- transkripční faktory * MeSH
Acoustic communication, a cornerstone of social interactions in mammals, relies on both vocal (effector) and auditory (receptor) organs, which display remarkable morphological diversity across species. The molecular mechanisms supporting the coordinated diversification of effector and receptor systems along with the evolution of species-specific acoustic communication are still poorly understood. A plausible hypothesis is that common genetic pathways orchestrate the parallel morphogenesis of vocal and auditory structures. Here, we addressed this question by generating mutant mice with targeted inactivation of Dlx5/6 genes in the Sox10 lineage, which includes neural crest and otic placode derivatives that contribute to the formation of vocal tract and ear components. We show that Dlx5/6 inactivation led to simultaneous patterning defects in the outer, middle and inner ear and of the jaw, pharynx and larynx musculoskeletal systems. We further show that Dlx5/6 modulate the BMP signalling pathway in both pharyngeal arches and otic vesicle, revealing a common Dlx5/6-BMP axis acting concurrently within the Sox10 derivatives. These findings highlight a pleiotropic role of Dlx5/6 in vocal and auditory morphogenesis, thereby suggesting their contribution in the co-adaptation of effector and receptor organs and in the diversification of acoustic communication in mammals.
Central European Institute of Technology Brno University of Technology Brno Czech Republic
Institut de Biologie Paris Seine Sorbonne Université CNRS Inserm UAR 3631 I2PS Paris France
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Chen Z, Wiens JJ. The origins of acoustic communication in vertebrates. Nat Commun. 2020;11(1):369. doi: 10.1038/s41467-020-14356-3 PubMed DOI PMC
Jorgewich-Cohen G, Townsend SW, Padovese LR, Klein N, Praschag P, Ferrara CR, et al. Common evolutionary origin of acoustic communication in choanate vertebrates. Nat Commun. 2022;13(1):6089. doi: 10.1038/s41467-022-33741-8 PubMed DOI PMC
Ladich F, Winkler H. Acoustic communication in terrestrial and aquatic vertebrates. J Exp Biol. 2017;220(Pt 13):2306–17. doi: 10.1242/jeb.132944 PubMed DOI
Taylor AM, Charlton BD, Reby D. Vocal Production by Terrestrial Mammals: Source, Filter, and Function. In: Suthers RA, Fitch WT, Fay RR, Popper AN, editors. Vertebrate Sound Production and Acoustic Communication. Cham: Springer International Publishing; 2016. p. 229–59.
Wilkins MR, Seddon N, Safran RJ. Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol. 2013;28(3):156–66. doi: 10.1016/j.tree.2012.10.002 PubMed DOI
Frisdal A, Trainor PA. Development and evolution of the pharyngeal apparatus. Wiley Interdiscip Rev Dev Biol. 2014;3(6):403–18. doi: 10.1002/wdev.147 PubMed DOI PMC
Heude E, Tesarova M, Sefton EM, Jullian E, Adachi N, Grimaldi A, et al. Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues. Elife. 2018;7:e40179. doi: 10.7554/eLife.40179 PubMed DOI PMC
Lungova V, Thibeault SL. Mechanisms of larynx and vocal fold development and pathogenesis. Cell Mol Life Sci. 2020;77(19):3781–95. doi: 10.1007/s00018-020-03506-x PubMed DOI PMC
Shimizu M, Narboux-Nême N, Gitton Y, de Lombares C, Fontaine A, Alfama G, et al. Probing the origin of matching functional jaws: roles of Dlx5/6 in cranial neural crest cells. Sci Rep. 2018;8(1):14975. doi: 10.1038/s41598-018-33207-2 PubMed DOI PMC
Ziermann JM, Diogo R, Noden DM. Neural crest and the patterning of vertebrate craniofacial muscles. Genesis. 2018;56(6–7):e23097. doi: 10.1002/dvg.23097 PubMed DOI
Adachi N, Bilio M, Baldini A, Kelly RG. Cardiopharyngeal mesoderm origins of musculoskeletal and connective tissues in the mammalian pharynx. Development. 2020;147(3):dev185256. doi: 10.1242/dev.185256 PubMed DOI
Tabler JM, Rigney MM, Berman GJ, Gopalakrishnan S, Heude E, Al-Lami HA, et al. Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx. Elife. 2017;6:e19153. doi: 10.7554/eLife.19153 PubMed DOI PMC
Anthwal N, Thompson H. The development of the mammalian outer and middle ear. J Anat. 2016;228(2):217–32. doi: 10.1111/joa.12344 PubMed DOI PMC
Fuchs JC, Tucker AS. Chapter Nine - Development and Integration of the Ear. In: Chai Y, editor. Current Topics in Developmental Biology. 115. Academic Press; 2015. p. 213–32. PubMed
Heude E, Bouhali K, Kurihara Y, Kurihara H, Couly G, Janvier P, et al. Jaw muscularization requires Dlx expression by cranial neural crest cells. Proc Natl Acad Sci U S A. 2010;107(25):11441–6. doi: 10.1073/pnas.1001582107 PubMed DOI PMC
Neidert AH, Virupannavar V, Hooker GW, Langeland JA. Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci U S A. 2001;98(4):1665–70. doi: 10.1073/pnas.98.4.1665 PubMed DOI PMC
Panganiban G, Rubenstein JLR. Developmental functions of the Distal-less/Dlx homeobox genes. Development. 2002;129(19):4371–86. doi: 10.1242/dev.129.19.4371 PubMed DOI
Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, Mantero S, et al. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development. 1999;126(17):3795–809. doi: 10.1242/dev.126.17.3795 PubMed DOI
Depew MJ, Lufkin T, Rubenstein JLR. Specification of jaw subdivisions by Dlx genes. Science. 2002;298(5592):381–5. doi: 10.1126/science.1075703 PubMed DOI
Beverdam A, Merlo GR, Paleari L, Mantero S, Genova F, Barbieri O, et al. Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: mirror of the past? Genesis. 2002;34(4):221–7. doi: 10.1002/gene.10156 PubMed DOI
Narboux-Neme N, Ekker M, Levi G, Heude E. Posterior axis formation requires Dlx5/Dlx6 expression at the neural plate border. PLoS One. 2019;14(3):e0214063. doi: 10.1371/journal.pone.0214063 PubMed DOI PMC
Merlo GR, Paleari L, Mantero S, Zerega B, Adamska M, Rinkwitz S, et al. The Dlx5 homeobox gene is essential for vestibular morphogenesis in the mouse embryo through a BMP4-mediated pathway. Dev Biol. 2002;248(1):157–69. doi: 10.1006/dbio.2002.0713 PubMed DOI
Robledo RF, Lufkin T. Dlx5 and Dlx6 homeobox genes are required for specification of the mammalian vestibular apparatus. Genesis. 2006;44(9):425–37. doi: 10.1002/dvg.20233 PubMed DOI
Stearns FW. One hundred years of pleiotropy: a retrospective. Genetics. 2010;186(3):767–73. doi: 10.1534/genetics.110.122549 PubMed DOI PMC
Wang Z, Liao B-Y, Zhang J. Genomic patterns of pleiotropy and the evolution of complexity. Proc Natl Acad Sci U S A. 2010;107(42):18034–9. doi: 10.1073/pnas.1004666107 PubMed DOI PMC
Zhang J. Patterns and evolutionary consequences of pleiotropy. Annu Rev Ecol Evol Syst. 2023;54:1–19. doi: 10.1146/annurev-ecolsys-022323-083451 PubMed DOI PMC
Betancur P, Sauka-Spengler T, Bronner M. A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs. Development. 2011;138(17):3689–98. doi: 10.1242/dev.057836 PubMed DOI PMC
Jacques-Fricke BT, Roffers-Agarwal J, Gammill LS. DNA methyltransferase 3b is dispensable for mouse neural crest development. PLoS One. 2012;7(10):e47794. doi: 10.1371/journal.pone.0047794 PubMed DOI PMC
de Lombares C, Heude E, Alfama G, Fontaine A, Hassouna R, Vernochet C, et al. Dlx5 and Dlx6 expression in GABAergic neurons controls behavior, metabolism, healthy aging and lifespan. Aging (Albany NY). 2019;11(17):6638–56. doi: 10.18632/aging.102141 PubMed DOI PMC
Friedrich G, Soriano P. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 1991;5(9):1513–23. doi: 10.1101/gad.5.9.1513 PubMed DOI
Matsumoto K, Mitani TT, Horiguchi SA, Kaneshiro J, Murakami TC, Mano T, et al. Advanced CUBIC tissue clearing for whole-organ cell profiling. Nat Protoc. 2019;14(12):3506–37. doi: 10.1038/s41596-019-0240-9 PubMed DOI
Tesařová M, Heude E, Comai G, Zikmund T, Kaucká M, Adameyko I, et al. An interactive and intuitive visualisation method for X-ray computed tomography data of biological samples in 3D Portable Document Format. Sci Rep. 2019;9(1):14896. doi: 10.1038/s41598-019-51180-2 PubMed DOI PMC
Sugimoto T, Taya Y, Shimazu Y, Soeno Y, Sato K, Aoba T. Three-Dimensional Visualization of Developing Neurovascular Architecture in the Craniofacial Region of Embryonic Mice. Anat Rec (Hoboken). 2015;298(11):1824–35. doi: 10.1002/ar.23179 PubMed DOI
Vermeiren S, Bellefroid EJ, Desiderio S. Vertebrate Sensory Ganglia: Common and Divergent Features of the Transcriptional Programs Generating Their Functional Specialization. Front Cell Dev Biol. 2020;8:587699. doi: 10.3389/fcell.2020.587699 PubMed DOI PMC
Sajan SA, Rubenstein JLR, Warchol ME, Lovett M. Identification of direct downstream targets of Dlx5 during early inner ear development. Hum Mol Genet. 2011;20(7):1262–73. doi: 10.1093/hmg/ddq567 PubMed DOI PMC
Jeong J, Li X, McEvilly RJ, Rosenfeld MG, Lufkin T, Rubenstein JLR. Dlx genes pattern mammalian jaw primordium by regulating both lower jaw-specific and upper jaw-specific genetic programs. Development. 2008;135(17):2905–16. doi: 10.1242/dev.019778 PubMed DOI PMC
Coles E, Christiansen J, Economou A, Bronner-Fraser M, Wilkinson DG. A vertebrate crossveinless 2 homologue modulates BMP activity and neural crest cell migration. Development. 2004;131(21):5309–17. doi: 10.1242/dev.01419 PubMed DOI
Ikeya M, Kawada M, Kiyonari H, Sasai N, Nakao K, Furuta Y, et al. Essential pro-Bmp roles of crossveinless 2 in mouse organogenesis. Development. 2006;133(22):4463–73. doi: 10.1242/dev.02647 PubMed DOI
Moser M, Binder O, Wu Y, Aitsebaomo J, Ren R, Bode C, et al. BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol. 2003;23(16):5664–79. doi: 10.1128/MCB.23.16.5664-5679.2003 PubMed DOI PMC
Charité J, McFadden DG, Merlo G, Levi G, Clouthier DE, Yanagisawa M, et al. Role of Dlx6 in regulation of an endothelin-1-dependent, dHAND branchial arch enhancer. Genes Dev. 2001;15(22):3039–49. doi: 10.1101/gad.931701 PubMed DOI PMC
Levi G, Mantero S, Barbieri O, Cantatore D, Paleari L, Beverdam A, et al. Msx1 and Dlx5 act independently in development of craniofacial skeleton, but converge on the regulation of Bmp signaling in palate formation. Mech Dev. 2006;123(1):3–16. doi: 10.1016/j.mod.2005.10.007 PubMed DOI
Funato N, Kokubo H, Nakamura M, Yanagisawa H, Saga Y. Specification of jaw identity by the Hand2 transcription factor. Sci Rep. 2016;6:28405. doi: 10.1038/srep28405 PubMed DOI PMC
Kuratani S, Satokata I, Blum M, Komatsu Y, Haraguchi R, Nakamura S, et al. Middle ear defects associated with the double knock out mutation of murine goosecoid and Msx1 genes. Cell Mol Biol (Noisy-le-grand). 1999;45(5):589–99. PubMed
Wang RN, Green J, Wang Z, Deng Y, Qiao M, Peabody M, et al. Bone Morphogenetic Protein (BMP) signaling in development and human diseases. Genes Dis. 2014;1(1):87–105. doi: 10.1016/j.gendis.2014.07.005 PubMed DOI PMC
Vincentz JW, Casasnovas JJ, Barnes RM, Que J, Clouthier DE, Wang J, et al. Exclusion of Dlx5/6 expression from the distal-most mandibular arches enables BMP-mediated specification of the distal cap. Proc Natl Acad Sci U S A. 2016;113(27):7563–8. doi: 10.1073/pnas.1603930113 PubMed DOI PMC
Ramachandran J, Zhou W, Bardenhagen AE, Nasr T, Yates ER, Zorn AM, et al. Hedgehog regulation of epithelial cell state and morphogenesis in the larynx. Elife. 2022;11:e77055. doi: 10.7554/eLife.77055 PubMed DOI PMC
Elliott KH, Chen X, Salomone J, Chaturvedi P, Schultz PA, Balchand SK, et al. Gli3 utilizes Hand2 to synergistically regulate tissue-specific transcriptional networks. Elife. 2020;9:e56450. doi: 10.7554/eLife.56450 PubMed DOI PMC
Ellies DL, Stock DW, Hatch G, Giroux G, Weiss KM, Ekker M. Relationship between the genomic organization and the overlapping embryonic expression patterns of the zebrafish dlx genes. Genomics. 1997;45(3):580–90. doi: 10.1006/geno.1997.4978 PubMed DOI
Keer S, Neilson KM, Cousin H, Majumdar HD, Alfandari D, Klein SL, et al. Bop1 is required to establish precursor domains of craniofacial tissues. Genesis. 2024;62(1):e23580. doi: 10.1002/dvg.23580 PubMed DOI PMC
Papalopulu N, Kintner C. Xenopus Distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. Development. 1993;117(3):961–75. doi: 10.1242/dev.117.3.961 PubMed DOI
Sohail A, Bendall AJ. DLX gene expression in the developing chick pharyngeal arches and relationship to endothelin signaling and avian jaw patterning. Dev Dyn. 2024;253(2):255–71. doi: 10.1002/dvdy.653 PubMed DOI
Talbot JC, Johnson SL, Kimmel CB. hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. Development. 2010;137(15):2507–17. doi: 10.1242/dev.049700 PubMed DOI PMC
Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, et al. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science. 2011;334(6055):521–4. doi: 10.1126/science.1211028 PubMed DOI
Le Maître A, Grunstra NDS, Pfaff C, Mitteroecker P. Evolution of the Mammalian Ear: An Evolvability Hypothesis. Evol Biol. 2020;47(3):187–92. doi: 10.1007/s11692-020-09502-0 PubMed DOI PMC
Charlton BD, Owen MA, Swaisgood RR. Coevolution of vocal signal characteristics and hearing sensitivity in forest mammals. Nat Commun. 2019;10(1):2778. doi: 10.1038/s41467-019-10768-y PubMed DOI PMC
Levi G, de Lombares C, Giuliani C, Iannuzzi V, Aouci R, Garagnani P, et al. DLX5/6 GABAergic Expression Affects Social Vocalization: Implications for Human Evolution. Mol Biol Evol. 2021;38(11):4748–64. doi: 10.1093/molbev/msab181 PubMed DOI PMC
Wilkins AS, Wrangham RW, Fitch WT. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197(3):795–808. doi: 10.1534/genetics.114.165423 PubMed DOI PMC
Lesch R, Fitch WT. The domestication of the larynx: The neural crest connection. J Exp Zool B Mol Dev Evol. 2024;342(4):342–9. doi: 10.1002/jez.b.23251 PubMed DOI PMC
Wilkins AS, Wrangham R, Fitch WT. The neural crest/domestication syndrome hypothesis, explained: reply to Johnsson, Henriksen, and Wright. Genetics. 2021;219(1):iyab098. doi: 10.1093/genetics/iyab098 PubMed DOI PMC
Boeckx C, Benítez-Burraco A. The shape of the human language-ready brain. Front Psychol. 2014;5:282. doi: 10.3389/fpsyg.2014.00282 PubMed DOI PMC
Gokhman D, Nissim-Rafinia M, Agranat-Tamir L, Housman G, García-Pérez R, Lizano E, et al. Differential DNA methylation of vocal and facial anatomy genes in modern humans. Nat Commun. 2020;11(1):1189. doi: 10.1038/s41467-020-15020-6 PubMed DOI PMC
Birnbaum RY, Everman DB, Murphy KK, Gurrieri F, Schwartz CE, Ahituv N. Functional characterization of tissue-specific enhancers in the DLX5/6 locus. Hum Mol Genet. 2012;21(22):4930–8. doi: 10.1093/hmg/dds336 PubMed DOI PMC
Robledo RF, Rajan L, Li X, Lufkin T. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev. 2002;16(9):1089–101. doi: 10.1101/gad.988402 PubMed DOI PMC