Early ear neuronal development, but not olfactory or lens development, can proceed without SOX2
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
R01 AG060504
NIA NIH HHS - United States
R01 DC015252
NIDCD NIH HHS - United States
PubMed
31526806
PubMed Central
PMC6938654
DOI
10.1016/j.ydbio.2019.09.003
PII: S0012-1606(19)30336-7
Knihovny.cz E-zdroje
- Klíčová slova
- Eye, Inner ear, Neuronal projections, Olfactory system, Placode development,
- MeSH
- apoptóza MeSH
- myši knockoutované MeSH
- myši MeSH
- neurogeneze * MeSH
- nosní sliznice embryologie metabolismus MeSH
- oční čočka embryologie metabolismus MeSH
- transkripční faktory SOXB1 genetika metabolismus MeSH
- vnitřní ucho cytologie embryologie metabolismus MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- Sox2 protein, mouse MeSH Prohlížeč
- transkripční faktory SOXB1 MeSH
SOX2 is essential for maintaining neurosensory stem cell properties, although its involvement in the early neurosensory development of cranial placodes remains unclear. To address this, we used Foxg1-Cre to conditionally delete Sox2 during eye, ear, and olfactory placode development. Foxg1-Cre mediated early deletion of Sox2 eradicates all olfactory placode development, and disrupts retinal development and invagination of the lens placode. In contrast to the lens and olfactory placodes, the ear placode invaginates and delaminates NEUROD1 positive neurons. Furthermore, we show that SOX2 is not necessary for early ear neurogenesis, since the early inner ear ganglion is formed with near normal central projections to the hindbrain and peripheral projections to the undifferentiated sensory epithelia of E11.5-12.5 ears. However, later stages of ear neurosensory development, in particular, the late forming auditory system, critically depend on the presence of SOX2. Our data establish distinct differences for SOX2 requirements among placodal sensory organs with similarities between olfactory and lens but not ear placode development, consistent with the unique neurosensory development and molecular properties of the ear.
Department of Biology University of Iowa Iowa City IA USA
Zobrazit více v PubMed
Abello G, Khatri S, Radosevic M, Scotting PJ, Giraldez F, Alsina B, 2010. Independent regulation of Sox3 and Lmx1b by FGF and BMP signaling influences the neurogenic and non-neurogenic domains in the chick otic placode. Dev Biol 339, 166–178. PubMed
Ahmed M, Xu J, Xu PX, 2012. EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear. Development 139, 1965–1977. PubMed PMC
Ashery-Padan R, Marquardt T, Zhou X, Gruss P, 2000. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev 14, 2701–2711. PubMed PMC
Barrionuevo F, Naumann A, Bagheri-Fam S, Speth V, Taketo MM, Scherer G, Neubuser A, 2008. Sox9 is required for invagination of the otic placode in mice. Dev Biol 317, 213–224. PubMed
Bhattacharyya S, Bailey AP, Bronner-Fraser M, Streit A, 2004. Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev Biol 271, 403–414. PubMed
Bianchi LM, Conover JC, Fritzsch B, DeChiara T, Lindsay RM, Yancopoulos GD, 1996. Degeneration of vestibular neurons in late embryogenesis of both heterozygous and homozygous BDNF null mutant mice. Development 122, 1965–1973. PubMed
Bouchard M, de Caprona D, Busslinger M, Xu P, Fritzsch B, 2010. Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. BMC developmental biology 10, 89. PubMed PMC
Chumak T, Bohuslavova R, Macova I, Dodd N, Buckiova D, Fritzsch B, Syka J, Pavlinkova G, 2016. Deterioration of the Medial Olivocochlear Efferent System Accelerates Age-Related Hearing Loss in Pax2-Isl1 Transgenic Mice. Mol Neurobiol 53, 2368–2383. PubMed
Couly GF, Le Douarin NM, 1985. Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110, 422–439. PubMed
Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KS, Pevny LH, Kelley MW, 2008. Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proceedings of the National Academy of Sciences 105, 18396–18401. PubMed PMC
Dastidar SG, Landrieu PMZ, D’Mello SR, 2011. FoxG1 promotes the survival of postmitotic neurons. Journal of Neuroscience 31, 402–413. PubMed PMC
Donner AL, Episkopou V, Maas RL, 2007. Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev Biol 303, 784–799. PubMed PMC
Duggan CD, DeMaria S, Baudhuin A, Stafford D, Ngai J, 2008. Foxg1 is required for development of the vertebrate olfactory system. Journal of Neuroscience 28, 5229–5239. PubMed PMC
Duncan JS, Fritzsch B, 2013. Continued expression of GATA3 is necessary for cochlear neurosensory development. PloS one 8, e62046. PubMed PMC
Dvorakova M, Jahan I, Macova I, Chumak T, Bohuslavova R, Syka J, Fritzsch B, Pavlinkova G, 2016. Incomplete and delayed Sox2 deletion defines residual ear neurosensory development and maintenance. Scientific reports 6, 38253. PubMed PMC
Evsen L, Sugahara S, Uchikawa M, Kondoh H, Wu DK, 2013. Progression of neurogenesis in the inner ear requires inhibition of Sox2 transcription by neurogenin1 and neurod1. Journal of Neuroscience 33, 3879–3890. PubMed PMC
Fariñas I, Jones KR, Tessarollo L, Vigers AJ, Huang E, Kirstein M, De Caprona DC, Coppola V, Backus C, Reichardt LF, Fritzsch B, 2001. Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. Journal of Neuroscience 21, 6170–6180. PubMed PMC
Fritzsch B, Beisel K, Jones K, Farinas I, Maklad A, Lee J, Reichardt L, 2002. Development and evolution of inner ear sensory epithelia and their innervation. Journal of neurobiology 53, 143–156. PubMed PMC
Fritzsch B, Duncan JS, Kersigo J, Gray B, Elliott KL, 2016a. Neuroanatomical Tracing Techniques in the Ear: History, State of the Art, and Future Developments, Sokolowski B, Ed: Auditory and Vestibular Research: Methods and Protocols. Springer Science+Business Media; New York, pp. 243–262. PubMed PMC
Fritzsch B, Elliott KL, Pavlinkova G, 2019. Primary sensory map formations reflect unique needs and molecular cues specific to each sensory system. F1000Research 8. PubMed PMC
Fritzsch B, Kersigo J, Yang T, Jahan I, Pan N, 2016b. Neurotrophic factor function during ear development: expression changes define critical phases for neuronal viability, The Primary Auditory Neurons of the Mammalian Cochlea. Springer, pp. 49–84.
Fritzsch B, Pan N, Jahan I, Elliott KL, 2015. Inner ear development: building a spiral ganglion and an organ of Corti out of unspecified ectoderm. Cell and tissue research 361, 7–24. PubMed PMC
Fritzsch B, Sarai P, Barbacid M, Silos-Santiago I, 1997. Mice with a targeted disruption of the neurotrophin receptor trkB lose their gustatory ganglion cells early but do develop taste buds. International Journal of Developmental Neuroscience 15, 563–576. PubMed
Garaffo G, Conte D, Provero P, Tomaiuolo D, Luo Z, Pinciroli P, Peano C, D’Atri I, Gitton Y, Etzion T, 2015. The Dlx5 and Foxg1 transcription factors, linked via miRNA-9 and-200, are required for the development of the olfactory and GnRH system. Molecular and Cellular Neuroscience 68, 103–119. PubMed PMC
Gu R, Brown RM 2nd, Hsu CW, Cai T, Crowder AL, Piazza VG, Vadakkan TJ, Dickinson ME, Groves AK, 2016. Lineage tracing of Sox2-expressing progenitor cells in the mouse inner ear reveals a broad contribution to non-sensory tissues and insights into the origin of the organ of Corti. Dev Biol 414, 72–84. PubMed PMC
Hagey DW, Klum S, Kurtsdotter I, Zaouter C, Topcic D, Andersson O, Bergsland M, Muhr J, 2018. SOX2 regulates common and specific stem cell features in the CNS and endoderm derived organs. PLoS genetics 14, e1007224. PubMed PMC
Hosoya M, Fujioka M, Matsuda S, Ohba H, Shibata S, Nakagawa F, Watabe T, Wakabayashi K, Saga Y, Ogawa K, Okano HJ, Okano H, 2011. Expression and function of Sox21 during mouse cochlea development. Neurochem Res 36, 1261–1269. PubMed
Huang EJ, Liu W, Fritzsch B, Bianchi LM, Reichardt LF, Xiang M, 2001. Brn3a is a transcriptional regulator of soma size, target field innervation and axon pathfinding of inner ear sensory neurons. Development 128, 2421–2432. PubMed PMC
Hwang CH, Simeone A, Lai E, Wu DK, 2009. Foxg1 is required for proper separation and formation of sensory cristae during inner ear development. Developmental dynamics: an official publication of the American Association of Anatomists 238, 2725–2734. PubMed
Jahan I, Kersigo J, Pan N, Fritzsch B, 2010. Neurod1 regulates survival and formation of connections in mouse ear and brain. Cell and tissue research 341, 95–110. PubMed PMC
Kageyama R, Shimojo H, Ohtsuka T, 2019. Dynamic control of neural stem cells by bHLH factors. Neuroscience research 138, 12–18. PubMed
Kamachi Y, Uchikawa M, Tanouchi A, Sekido R, Kondoh H, 2001. Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev 15, 1272–1286. PubMed PMC
Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, de Caprona D, Fritzsch B, 2001. Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429, 615–630. PubMed
Kawauchi S, Kim J, Santos R, Wu H-H, Lander AD, Calof AL, 2009. Foxg1 promotes olfactory neurogenesis by antagonizing Gdf11. Development 136, 1453–1464. PubMed PMC
Kempfle JS, Turban JL, Edge AS, 2016. Sox2 in the differentiation of cochlear progenitor cells. Scientific reports 6, 23293. PubMed PMC
Kersigo J, D’Angelo A, Gray BD, Soukup GA, Fritzsch B, 2011. The role of sensory organs and the forebrain for the development of the craniofacial shape as revealed by Foxg1-cre-mediated microRNA loss. Genesis 49, 326–341. PubMed PMC
Kiernan AE, Pelling AL, Leung KK, Tang AS, Bell DM, Tease C, Lovell-Badge R, Steel KP, Cheah KS, 2005. Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434, 1031–1035. PubMed
Kim W-Y, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, Lee JE, 2001. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128, 417–426. PubMed PMC
Kondoh H, Lovell-Badge R, 2015. Sox2: biology and role in development and disease. Academic Press.
Kopecky BJ, Duncan JS, Elliott KL, Fritzsch B, 2012. Three-dimensional reconstructions from optical sections of thick mouse inner ears using confocal microscopy. Journal of microscopy 248, 292–298. PubMed PMC
Kwan KY, Shen J, Corey DP, 2015. C-MYC transcriptionally amplifies SOX2 target genes to regulate self-renewal in multipotent otic progenitor cells. Stem Cell Reports 4, 47–60. PubMed PMC
Liu M, Pereira FA, Price SD, Chu MJ, Shope C, Himes D, Eatock RA, Brownell WE, Lysakowski A, Tsai MJ, 2000. Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev 14, 2839–2854. PubMed PMC
Luo XJ, Deng M, Xie X, Huang L, Wang H, Jiang L, Liang G, Hu F, Tieu R, Chen R, Gan L, 2013. GATA3 controls the specification of prosensory domain and neuronal survival in the mouse cochlea. Hum Mol Genet 22, 3609–3623. PubMed PMC
Ma Q, Anderson DJ, Fritzsch B, 2000. Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. Journal of the Association for Research in Otolaryngology 1, 129–143. PubMed PMC
Ma Q, Chen Z, del Barco Barrantes I, de la Pompa JL, Anderson DJ, 1998. neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20, 469–482. PubMed
Macova I, Pysanenko K, Chumak T, Dvorakova M, Bohuslavova R, Syka J, Fritzsch B, Pavlinkova G, 2019. Neurod1 is essential for the primary tonotopic organization and related auditory information processing in the midbrain. Journal of Neuroscience 6, 984–1004. PubMed PMC
Maier EC, Saxena A, Alsina B, Bronner ME, Whitfield TT, 2014. Sensational placodes: Neurogenesis in the otic and olfactory systems. Developmental biology 389, 50–67. PubMed PMC
Mak AC, Szeto IY, Fritzsch B, Cheah KS, 2009. Differential and overlapping expression pattern of SOX2 and SOX9 in inner ear development. Gene Expression Patterns 9, 444–453. PubMed PMC
Maklad A, Kamel S, Wong E, Fritzsch B, 2010. Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice. Cell and tissue research 340, 303–321. PubMed PMC
Martinez-Monedero R, Yi E, Oshima K, Glowatzki E, Edge AS, 2008. Differentiation of inner ear stem cells to functional sensory neurons. Developmental neurobiology 68, 669–684. PubMed
Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, Morris K, Feng F, Jones K, Lee J, Fritzsch B, 2005. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Developmental dynamics: an official publication of the American Association of Anatomists 234, 633–650. PubMed PMC
McLeod MJ, 1980. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22, 299–301. PubMed
Neves J, Kamaid A, Alsina B, Giraldez F, 2007. Differential expression of Sox2 and Sox3 in neuronal and sensory progenitors of the developing inner ear of the chick. J Comp Neurol 503, 487–500. PubMed
Nishimura K, Noda T, Dabdoub A, 2017. Dynamic expression of Sox2, Gata3, and Prox1 during primary auditory neuron development in the mammalian cochlea. PloS one 12, e0170568. PubMed PMC
Panaliappan TK, Wittmann W, Jidigam VK, Mercurio S, Bertolini JA, Sghari S, Bose R, Patthey C, Nicolis SK, Gunhaga L, 2018. Sox2 is required for olfactory pit formation and olfactory neurogenesis through BMP restriction and Hes5 upregulation. Development 145, dev153791. PubMed PMC
Pauley S, Lai E, Fritzsch B, 2006. Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Developmental dynamics: an official publication of the American Association of Anatomists 235, 2470–2482. PubMed PMC
Puligilla C, Dabdoub A, Brenowitz SD, Kelley MW, 2010. Sox2 induces neuronal formation in the developing mammalian cochlea. Journal of Neuroscience 30, 714–722. PubMed PMC
Quinn JC, West JD, Hill RE, 1996. Multiple functions for Pax6 in mouse eye and nasal development. Genes Dev 10, 435–446. PubMed
Reiprich S, Wegner M, 2015. From CNS stem cells to neurons and glia: Sox for everyone. Cell and tissue research 359, 111–124. PubMed
Shen W, Ba R, Su Y, Ni Y, Chen D, Xie W, Pleasure SJ, Zhao C, 2018. Foxg1 Regulates the Postnatal Development of Cortical Interneurons. Cerebral Cortex. PubMed PMC
Simmons D, Duncan J, de Caprona DC, Fritzsch B, 2011. Development of the inner ear efferent system, Auditory and vestibular efferents. Springer, pp. 187–216.
Steevens AR, Glatzer JC, Kellogg CC, Low WC, Santi PA, Kiernan AE, 2019. SOX2 is required for inner ear growth and cochlear nonsensory formation before sensory development. Development 146. PubMed PMC
Steevens AR, Sookiasian DL, Glatzer JC, Kiernan AE, 2017. SOX2 is required for inner ear neurogenesis. Scientific reports 7, 4086. PubMed PMC
Taranova OV, Magness ST, Fagan BM, Wu Y, Surzenko N, Hutton SR, Pevny LH, 2006. SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev 20, 1187–1202. PubMed PMC
Wegner M, 1999. From head to toes: the multiple facets of Sox proteins. Nucleic acids research 27, 1409–1420. PubMed PMC
Wegner M, Stolt CC, 2005. From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci 28, 583–588. PubMed
Wood HB, Episkopou V, 1999. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86, 197–201. PubMed
Harmony in the Molecular Orchestra of Hearing: Developmental Mechanisms from the Ear to the Brain
Development in the Mammalian Auditory System Depends on Transcription Factors
Molecular Aspects of the Development and Function of Auditory Neurons