Opposing roles for Bmp signalling during the development of electrosensory lateral line organs

. 2025 Jan 02 ; 14 () : . [epub] 20250102

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39745052

Grantová podpora
Research Studentship Anatomical Society
Research Studentship Cambridge Philosophical Society
Grant 20.07(c) Cambridge Isaac Newton Trust
projects CENAKVA (LM2018099) and Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370) Ministry of Education, Youth and Sports of the Czech Republic
project 22-31141J Czech Science Foundation
BB/P001947/1 Biotechnology and Biological Sciences Research Council - United Kingdom
Grant 20.07[c] Cambridge Isaac Newton Trust
projects CENAKVA [LM2018099] and Biodiversity [CZ.02.1.01/0.0/0.0/16_025/0007370] Ministry of Education, Youth and Sports of the Czech Republic

The lateral line system enables fishes and aquatic-stage amphibians to detect local water movement via mechanosensory hair cells in neuromasts, and many species to detect weak electric fields via electroreceptors (modified hair cells) in ampullary organs. Both neuromasts and ampullary organs develop from lateral line placodes, but the molecular mechanisms underpinning ampullary organ formation are understudied relative to neuromasts. This is because the ancestral lineages of zebrafish (teleosts) and Xenopus (frogs) independently lost electroreception. We identified Bmp5 as a promising candidate via differential RNA-seq in an electroreceptive ray-finned fish, the Mississippi paddlefish (Polyodon spathula; Modrell et al., 2017, eLife 6: e24197). In an experimentally tractable relative, the sterlet sturgeon (Acipenser ruthenus), we found that Bmp5 and four other Bmp pathway genes are expressed in the developing lateral line, and that Bmp signalling is active. Furthermore, CRISPR/Cas9-mediated mutagenesis targeting Bmp5 in G0-injected sterlet embryos resulted in fewer ampullary organs. Conversely, when Bmp signalling was inhibited by DMH1 treatment shortly before the formation of ampullary organ primordia, supernumerary ampullary organs developed. These data suggest that Bmp5 promotes ampullary organ development, whereas Bmp signalling via another ligand(s) prevents their overproduction. Taken together, this demonstrates opposing roles for Bmp signalling during ampullary organ formation.

Před aktualizací

doi: 10.1101/2024.03.07.583945 PubMed

Zobrazit více v PubMed

Andermann P, Ungos J, Raible DW. Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Developmental Biology. 2002;251:45–58. doi: 10.1006/dbio.2002.0820. PubMed DOI

Bai H, Jiang L, Wang X, Gao X, Bing J, Xi C, Wang W, Zhang M, Zhang X, Han Z, Xu J, Zeng S. Transcriptomic analysis of mouse cochleae suffering from gentamicin damage reveals the signalling pathways involved in hair cell regeneration. Scientific Reports. 2019;9:10494. doi: 10.1038/s41598-019-47051-5. PubMed DOI PMC

Baker CVH, Modrell MS, Gillis JA. The evolution and development of vertebrate lateral line electroreceptors. The Journal of Experimental Biology. 2013;216:2515–2522. doi: 10.1242/jeb.082362. PubMed DOI PMC

Baker CVH, Modrell MS. Insights into electroreceptor development and evolution from molecular comparisons with hair cells. Integrative and Comparative Biology. 2018;58:329–340. doi: 10.1093/icb/icy037. PubMed DOI PMC

Baker CVH. In: Electroreception: Fundamental Insights from Comparative Approaches. Carlson BA, Sisneros JA, Popper AN, Fay RR, editors. Cham: Springer; 2019. The development and evolution of lateral line electroreceptors: insights from comparative molecular approaches; pp. 25–62. DOI

Bodznick D, Montgomery JC. In: Electroreception. Popper AN, Fay RR, Bullock TH, editors. New York: Springer; 2005. The physiology of low-frequency electrosensory systems; pp. 132–153. DOI

Bullock TH, Bodznick DA, Northcutt RG. The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sense modality. Brain Research Reviews. 1983;6:25–46. doi: 10.1016/0165-0173(83)90003-6. PubMed DOI

Camacho S, Ostos MDV, Llorente JI, Sanz A, García M, Domezain A, Carmona R. Structural characteristics and development of ampullary organs in Acipenser naccarii. The Anatomical Record. 2007;290:1178–1189. doi: 10.1002/ar.20569. PubMed DOI

Cernuda-Cernuda R, García-Fernández JM. Structural diversity of the ordinary and specialized lateral line organs. Microscopy Research and Technique. 1996;34:302–312. doi: 10.1002/(SICI)1097-0029(19960701)34:4<302::AID-JEMT3>3.0.CO;2-Q. PubMed DOI

Chagnaud BP, Wilkens LA, Hofmann M. In: The Senses: A Comprehensive Reference (Second Edition) Fritzsch B, editor. Elsevier; 2021. The ampullary electrosensory system – a paddlefish case study; pp. 215–227. DOI

Chang W, Lin Z, Kulessa H, Hebert J, Hogan BLM, Wu DK. Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLOS Genetics. 2008;4:e1000050. doi: 10.1371/journal.pgen.1000050. PubMed DOI PMC

Chitnis AB. In: The Senses: A Comprehensive Reference (Second Edition) Fritzsch B, editor. Elsevier; 2021. Development of the zebrafish posterior lateral line system; pp. 66–84. DOI

Conant D, Hsiau T, Rossi N, Oki J, Maures T, Waite K, Yang J, Joshi S, Kelso R, Holden K, Enzmann BL, Stoner R. Inference of CRISPR edits from Sanger trace data. The CRISPR Journal. 2022;5:123–130. doi: 10.1089/crispr.2021.0113. PubMed DOI

Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339:819–823. doi: 10.1126/science.1231143. PubMed DOI PMC

Cooper RL, Thiery AP, Fletcher AG, Delbarre DJ, Rasch LJ, Fraser GJ. An ancient Turing-like patterning mechanism regulates skin denticle development in sharks. Science Advances. 2018;4:eaau5484. doi: 10.1126/sciadv.aau5484. PubMed DOI PMC

Crampton WGR. Electroreception, electrogenesis and electric signal evolution. Journal of Fish Biology. 2019;95:92–134. doi: 10.1111/jfb.13922. PubMed DOI

Cross EE, Thomason RT, Martinez M, Hopkins CR, Hong CC, Bader DM. Application of small organic molecules reveals cooperative TGFβ and BMP regulation of mesothelial cell behaviors. ACS Chemical Biology. 2011;6:952–961. doi: 10.1021/cb200205z. PubMed DOI PMC

Cunningham F, Allen JE, Allen J, Alvarez-Jarreta J, Amode MR, Armean IM, Austine-Orimoloye O, Azov AG, Barnes I, Bennett R, Berry A, Bhai J, Bignell A, Billis K, Boddu S, Brooks L, Charkhchi M, Cummins C, Da Rin Fioretto L, Davidson C, Dodiya K, Donaldson S, El Houdaigui B, El Naboulsi T, Fatima R, Giron CG, Genez T, Martinez JG, Guijarro-Clarke C, Gymer A, Hardy M, Hollis Z, Hourlier T, Hunt T, Juettemann T, Kaikala V, Kay M, Lavidas I, Le T, Lemos D, Marugán JC, Mohanan S, Mushtaq A, Naven M, Ogeh DN, Parker A, Parton A, Perry M, Piližota I, Prosovetskaia I, Sakthivel MP, Salam AIA, Schmitt BM, Schuilenburg H, Sheppard D, Pérez-Silva JG, Stark W, Steed E, Sutinen K, Sukumaran R, Sumathipala D, Suner MM, Szpak M, Thormann A, Tricomi FF, Urbina-Gómez D, Veidenberg A, Walsh TA, Walts B, Willhoft N, Winterbottom A, Wass E, Chakiachvili M, Flint B, Frankish A, Giorgetti S, Haggerty L, Hunt SE, IIsley GR, Loveland JE, Martin FJ, Moore B, Mudge JM, Muffato M, Perry E, Ruffier M, Tate J, Thybert D, Trevanion SJ, Dyer S, Harrison PW, Howe KL, Yates AD, Zerbino DR, Flicek P. Ensembl 2022. Nucleic Acids Research. 2022;50:D988–D995. doi: 10.1093/nar/gkab1049. PubMed DOI PMC

Dettlaff TA, Ginsburg AS, Schmalhausen OI. Sturgeon Fishes: Developmental Biology and Aquaculture. Berlin: Springer-Verlag; 1993. DOI

Du K, Stöck M, Kneitz S, Klopp C, Woltering JM, Adolfi MC, Feron R, Prokopov D, Makunin A, Kichigin I, Schmidt C, Fischer P, Kuhl H, Wuertz S, Gessner J, Kloas W, Cabau C, Iampietro C, Parrinello H, Tomlinson C, Journot L, Postlethwait JH, Braasch I, Trifonov V, Warren WC, Meyer A, Guiguen Y, Schartl M. The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization. Nature Ecology & Evolution. 2020;4:841–852. doi: 10.1038/s41559-020-1166-x. PubMed DOI PMC

Fan C, Zou S, Wang J, Zhang B, Song J. Neomycin damage and regeneration of hair cells in both mechanoreceptor and electroreceptor lateral line organs of the larval Siberian sturgeon (Acipenser baerii) The Journal of Comparative Neurology. 2016;524:1443–1456. doi: 10.1002/cne.23918. PubMed DOI

Gibbs MA, Northcutt RG. Development of the lateral line system in the shovelnose sturgeon. Brain, Behavior and Evolution. 2004;64:70–84. doi: 10.1159/000079117. PubMed DOI

Gilmour DT, Maischein H-M, Nüsslein-Volhard C. Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron. 2002;34:577–588. doi: 10.1016/s0896-6273(02)00683-9. PubMed DOI

Gilmour D, Knaut H, Maischein H-M, Nüsslein-Volhard C. Towing of sensory axons by their migrating target cells in vivo. Nature Neuroscience. 2004;7:491–492. doi: 10.1038/nn1235. PubMed DOI

Grant KA, Raible DW, Piotrowski T. Regulation of latent sensory hair cell precursors by glia in the zebrafish lateral line. Neuron. 2005;45:69–80. doi: 10.1016/j.neuron.2004.12.020. PubMed DOI

Green JBA, Sharpe J. Positional information and reaction-diffusion: two big ideas in developmental biology combine. Development. 2015;142:1203–1211. doi: 10.1242/dev.114991. PubMed DOI

Guo X, Zhang T, Hu Z, Zhang Y, Shi Z, Wang Q, Cui Y, Wang F, Zhao H, Chen Y. Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development. 2014;141:707–714. doi: 10.1242/dev.099853. PubMed DOI

Hao J, Ho JN, Lewis JA, Karim KA, Daniels RN, Gentry PR, Hopkins CR, Lindsley CW, Hong CC. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chemical Biology. 2010;5:245–253. doi: 10.1021/cb9002865. PubMed DOI PMC

Heller IS, Guenther CA, Meireles AM, Talbot WS, Kingsley DM. Characterization of mouse Bmp5 regulatory injury element in zebrafish wound models. Bone. 2022;155:116263. doi: 10.1016/j.bone.2021.116263. PubMed DOI PMC

Hernández PP, Olivari FA, Sarrazin AF, Sandoval PC, Allende ML. Regeneration in zebrafish lateral line neuromasts: expression of the neural progenitor cell marker sox2 and proliferation-dependent and-independent mechanisms of hair cell renewal. Developmental Neurobiology. 2007;67:637–654. doi: 10.1002/dneu.20386. PubMed DOI

Jiang T-X, Jung H-S, Widelitz RB, Chuong C-M. Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development. 1999;126:4997–5009. doi: 10.1242/dev.126.22.4997. PubMed DOI

Jiang L, Romero-Carvajal A, Haug JS, Seidel CW, Piotrowski T. Gene-expression analysis of hair cell regeneration in the zebrafish lateral line. PNAS. 2014;111:E1383–E92. doi: 10.1073/pnas.1402898111. PubMed DOI PMC

Jørgensen JM. In: Electroreception. Bullock TH, Hopkins CD, Popper AN, Fay RR, editors. New York: Springer; 2005. Morphology of electroreceptive sensory organs; pp. 47–67. DOI

Jørgensen JM. In: Encyclopedia of Fish Physiology: From Genome to Environment. Farrell AP, editor. San Diego: Academic Press; 2011. Morphology of electroreceptive sensory organs; pp. 350–358. DOI

Josberger EE, Hassanzadeh P, Deng Y, Sohn J, Rego MJ, Amemiya CT, Rolandi M. Proton conductivity in ampullae of Lorenzini jelly. Science Advances. 2016;2:e1600112. doi: 10.1126/sciadv.1600112. PubMed DOI PMC

Jung H-S, Francis-West PH, Widelitz RB, Jiang T-X, Ting-Berreth S, Tickle C, Wolpert L, Chuong C-M. Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Developmental Biology. 1998;196:11–23. doi: 10.1006/dbio.1998.8850. PubMed DOI

Kamaid A, Neves J, Giráldez F. Id gene regulation and function in the prosensory domains of the chicken inner ear: a link between Bmp signaling and Atoh1. The Journal of Neuroscience. 2010;30:11426–11434. doi: 10.1523/JNEUROSCI.2570-10.2010. PubMed DOI PMC

Leitch DB, Julius D. In: Electroreception: Fundamental Insights from Comparative Approaches. Carlson BA, Sisneros JA, Popper AN, Fay RR, editors. Cham: Springer; 2019. Electrosensory transduction: comparisons across structure, afferent response properties, and cellular physiology; pp. 63–90. DOI

Lewis RM, Keller JJ, Wan L, Stone JS. Bone morphogenetic protein 4 antagonizes hair cell regeneration in the avian auditory epithelium. Hearing Research. 2018;364:1–11. doi: 10.1016/j.heares.2018.04.008. PubMed DOI PMC

Li H, Corrales CE, Wang Z, Zhao Y, Wang Y, Liu H, Heller S. BMP4 signaling is involved in the generation of inner ear sensory epithelia. BMC Developmental Biology. 2005;5:16. doi: 10.1186/1471-213X-5-16. PubMed DOI PMC

López-Schier H, Hudspeth AJ. Supernumerary neuromasts in the posterior lateral line of zebrafish lacking peripheral glia. PNAS. 2005;102:1496–1501. doi: 10.1073/pnas.0409361102. PubMed DOI PMC

Ludwig A, Belfiore NM, Pitra C, Svirsky V, Jenneckens I. Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus) Genetics. 2001;158:1203–1215. doi: 10.1093/genetics/158.3.1203. PubMed DOI PMC

Lush ME, Piotrowski T. Sensory hair cell regeneration in the zebrafish lateral line. Developmental Dynamics. 2014;243:1187–1202. doi: 10.1002/dvdy.24167. PubMed DOI PMC

Lush ME, Diaz DC, Koenecke N, Baek S, Boldt H, St Peter MK, Gaitan-Escudero T, Romero-Carvajal A, Busch-Nentwich EM, Perera AG, Hall KE, Peak A, Haug JS, Piotrowski T. scRNA-Seq reveals distinct stem cell populations that drive hair cell regeneration after loss of Fgf and Notch signaling. eLife. 2019;8:e44431. doi: 10.7554/eLife.44431. PubMed DOI PMC

McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Research. 2004;32:W20–W5. doi: 10.1093/nar/gkh435. PubMed DOI PMC

McGraw HF, Drerup CM, Nicolson T, Nechiporuk AV. In: Auditory Development and Plasticity. Cramer KS, Coffin AB, Fay RR, Popper AN, editors. Springer; 2017. The molecular and cellular mechanisms of zebrafish lateral line development; pp. 49–73. DOI

Metcalfe WK. Sensory neuron growth cones comigrate with posterior lateral line primordial cells in zebrafish. The Journal of Comparative Neurology. 1985;238:218–224. doi: 10.1002/cne.902380208. PubMed DOI

Metscher BD, Müller GB. MicroCT for molecular imaging: quantitative visualization of complete three-dimensional distributions of gene products in embryonic limbs. Developmental Dynamics. 2011;240:2301–2308. doi: 10.1002/dvdy.22733. PubMed DOI

Michon F, Forest L, Collomb E, Demongeot J, Dhouailly D. BMP2 and BMP7 play antagonistic roles in feather induction. Development. 2008;135:2797–2805. doi: 10.1242/dev.018341. PubMed DOI PMC

Minařík M, Modrell MS, Gillis JA, Campbell AS, Fuller I, Lyne R, Micklem G, Gela D, Pšenička M, Baker CVH. Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs. Frontiers in Cell and Developmental Biology. 2024a;12:e1327924. doi: 10.3389/fcell.2024.1327924. PubMed DOI PMC

Minařík M, Campbell AS, Franěk R, Vazačová M, Havelka M, Gela D, Pšenička M, Baker CVH. Atoh1 Is required for the formation of lateral line electroreceptors and hair cells, whereas Foxg1 represses an electrosensory fate. bioRxiv. 2024b doi: 10.1101/2023.04.15.537030. DOI

Modrell MS, Bemis WE, Northcutt RG, Davis MC, Baker CVH. Electrosensory ampullary organs are derived from lateral line placodes in bony fishes. Nature Communications. 2011a;2:496. doi: 10.1038/ncomms1502. PubMed DOI PMC

Modrell MS, Buckley D, Baker CVH. Molecular analysis of neurogenic placode development in a basal ray-finned fish. Genesis. 2011b;49:278–294. doi: 10.1002/dvg.20707. PubMed DOI PMC

Modrell MS, Lyne M, Carr AR, Zakon HH, Buckley D, Campbell AS, Davis MC, Micklem G, Baker CV. Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome. eLife. 2017a;6:e24197. doi: 10.7554/eLife.24197. PubMed DOI PMC

Modrell MS, Tidswell ORA, Baker CVH. Notch and Fgf signaling during electrosensory versus mechanosensory lateral line organ development in a non-teleost ray-finned fish. Developmental Biology. 2017b;431:48–58. doi: 10.1016/j.ydbio.2017.08.017. PubMed DOI PMC

Mogdans J. In: The Senses: A Comprehensive Reference (Second Edition) Fritzsch B, editor. Elsevier; 2021. Physiology of the peripheral lateral line system; pp. 143–162. DOI

Montgomery J, Bleckmann H, Coombs S. In: In: The Lateral Line System. Coombs SC, Bleckmann H, Fay RR, Popper AN, editors. New York: Springer; 2014. Sensory ecology and neuroethology of the lateral line; pp. 121–150. DOI

Morsli H, Choo D, Ryan A, Johnson R, Wu DK. Development of the mouse inner ear and origin of its sensory organs. The Journal of Neuroscience. 1998;18:3327–3335. doi: 10.1523/JNEUROSCI.18-09-03327.1998. PubMed DOI PMC

Mou C, Jackson B, Schneider P, Overbeek PA, Headon DJ. Generation of the primary hair follicle pattern. PNAS. 2006;103:9075–9080. doi: 10.1073/pnas.0600825103. PubMed DOI PMC

Mowbray C, Hammerschmidt M, Whitfield TT. Expression of BMP signalling pathway members in the developing zebrafish inner ear and lateral line. Mechanisms of Development. 2001;108:179–184. doi: 10.1016/s0925-4773(01)00479-8. PubMed DOI

Nikaido M, Navajas Acedo J, Hatta K, Piotrowski T. Retinoic acid is required and Fgf, Wnt, and Bmp signaling inhibit posterior lateral line placode induction in zebrafish. Developmental Biology. 2017;431:215–225. doi: 10.1016/j.ydbio.2017.09.017. PubMed DOI

Noramly S, Morgan BA. BMPs mediate lateral inhibition at successive stages in feather tract development. Development. 1998;125:3775–3787. doi: 10.1242/dev.125.19.3775. PubMed DOI

Northcutt RG. Evolution of gnathostome lateral line ontogenies. Brain, Behavior and Evolution. 1997;50:25–37. doi: 10.1159/000113319. PubMed DOI

Northcutt RG. In: Electroreception. Bullock TH, Hopkins CD, Popper AN, Fay RR, editors. New York: Springer; 2005. Ontogeny of electroreceptors and their neural circuitry; pp. 112–131. DOI

Ohyama T, Basch ML, Mishina Y, Lyons KM, Segil N, Groves AK. BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. The Journal of Neuroscience. 2010;30:15044–15051. doi: 10.1523/JNEUROSCI.3547-10.2010. PubMed DOI PMC

Pickett SB, Raible DW. Water waves to sound waves: using zebrafish to explore hair cell biology. Journal of the Association for Research in Otolaryngology. 2019;20:1–19. doi: 10.1007/s10162-018-00711-1. PubMed DOI PMC

Piotrowski T, Baker CVH. The development of lateral line placodes: taking a broader view. Developmental Biology. 2014;389:68–81. doi: 10.1016/j.ydbio.2014.02.016. PubMed DOI

Pujades C, Kamaid A, Alsina B, Giraldez F. BMP-signaling regulates the generation of hair-cells. Developmental Biology. 2006;292:55–67. doi: 10.1016/j.ydbio.2006.01.001. PubMed DOI

Rabinowitz R, Offen D. Single-base resolution: increasing the specificity of the CRISPR-Cas system in gene editing. Molecular Therapy. 2021;29:937–948. doi: 10.1016/j.ymthe.2020.11.009. PubMed DOI PMC

Russell DF, Zhang W, Warnock TC, Neiman LL. Lectin binding and gel secretion within Lorenzinian electroreceptors of Polyodon. PLOS ONE. 2022;17:e0276854. doi: 10.1371/journal.pone.0276854. PubMed DOI PMC

Schmierer B, Hill CS. TGFβ-SMAD signal transduction: molecular specificity and functional flexibility. Nature Reviews Molecular Cell Biology. 2007;8:970–982. doi: 10.1038/nrm2297. PubMed DOI

Stundl J, Soukup V, Franěk R, Pospisilova A, Psutkova V, Pšenička M, Cerny R, Bronner ME, Medeiros DM, Jandzik D. Efficient CRISPR mutagenesis in sturgeon demonstrates its utility in large, slow-maturing vertebrates. Frontiers in Cell and Developmental Biology. 2022;10:e750833. doi: 10.3389/fcell.2022.750833. PubMed DOI PMC

Thisse B, Thisse C. Fast release clones: a high throughput expression analysis. ZFIN Direct Data Submission. 2004. [February 1, 2024]. http://zfin.org

Tong X, Zhu C, Liu L, Huang M, Xu J, Chen X, Zou J. Role of Sostdc1 in skeletal biology and cancer. Frontiers in Physiology. 2022;13:1029646. doi: 10.3389/fphys.2022.1029646. PubMed DOI PMC

Undurraga CA, Gou Y, Sandoval PC, Nuñez VA, Allende ML, Riley BB, Hernández PP, Sarrazin AF. Sox2 and Sox3 are essential for development and regeneration of the zebrafish lateral line. bioRxiv. 2019 doi: 10.1101/856088. DOI

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3-new capabilities and interfaces. Nucleic Acids Research. 2012;40:e115. doi: 10.1093/nar/gks596. PubMed DOI PMC

Uribe-Salazar JM, Kaya G, Sekar A, Weyenberg K, Ingamells C, Dennis MY. Evaluation of CRISPR gene-editing tools in zebrafish. BMC Genomics. 2022;23:12. doi: 10.1186/s12864-021-08238-1. PubMed DOI PMC

Vonica A, Bhat N, Phan K, Guo J, Iancu L, Weber JA, Karger A, Cain JW, Wang ECE, DeStefano GM, O’Donnell-Luria AH, Christiano AM, Riley B, Butler SJ, Luria V. Apcdd1 is a dual BMP/Wnt inhibitor in the developing nervous system and skin. Developmental Biology. 2020;464:71–87. doi: 10.1016/j.ydbio.2020.03.015. PubMed DOI PMC

Wada H, Dambly-Chaudière C, Kawakami K, Ghysen A. Innervation is required for sense organ development in the lateral line system of adult zebrafish. PNAS. 2013;110:5659–5664. doi: 10.1073/pnas.1214004110. PubMed DOI PMC

Wada H, Kawakami K. Size control during organogenesis: Development of the lateral line organs in zebrafish. Development, Growth & Differentiation. 2015;57:169–178. doi: 10.1111/dgd.12196. PubMed DOI

Wang J, Lu C, Zhao Y, Tang Z, Song J, Fan C. Transcriptome profiles of sturgeon lateral line electroreceptor and mechanoreceptor during regeneration. BMC Genomics. 2020;21:875. doi: 10.1186/s12864-020-07293-4. PubMed DOI PMC

Warth P, Hilton EJ, Naumann B, Olsson L, Konstantinidis P. Development of the muscles associated with the mandibular and hyoid arches in the Siberian sturgeon, Acipenser baerii (Acipenseriformes: Acipenseridae) Journal of Morphology. 2018;279:163–175. doi: 10.1002/jmor.20761. PubMed DOI

Winklbauer R. Development of the lateral line system in Xenopus. Progress in Neurobiology. 1989;32:181–206. doi: 10.1016/0301-0082(89)90016-6. PubMed DOI

Wu DK, Oh S-H. Sensory organ generation in the chick inner ear. The Journal of Neuroscience. 1996;16:6454–6462. doi: 10.1523/JNEUROSCI.16-20-06454.1996. PubMed DOI PMC

Yadin D, Knaus P, Mueller TD. Structural insights into BMP receptors: Specificity, activation and inhibition. Cytokine & Growth Factor Reviews. 2016;27:13–34. doi: 10.1016/j.cytogfr.2015.11.005. PubMed DOI

Zhang X, Xia K, Lin L, Zhang F, Yu Y, St Ange K, Han X, Edsinger E, Sohn J, Linhardt RJ. Structural and functional components of the skate sensory organ ampullae of Lorenzini. ACS Chemical Biology. 2018;13:1677–1685. doi: 10.1021/acschembio.8b00335. PubMed DOI

Zimmerman LB, De Jesús-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 1996;86:599–606. doi: 10.1016/s0092-8674(00)80133-6. PubMed DOI

Zobrazit více v PubMed

Dryad
10.5061/dryad.9s4mw6mt5

GEO
GSE92470

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...