Early Steps towards Hearing: Placodes and Sensory Development

Abstract

Sensorineural hearing loss is the most prevalent sensory deficit in humans. Most cases of hearing loss are due to the degeneration of key structures of the sensory pathway in the cochlea, such as the sensory hair cells, the primary auditory neurons, and their synaptic connection to the hair cells. Different cell-based strategies to replace damaged inner ear neurosensory tissue aiming at the restoration of regeneration or functional recovery are currently the subject of intensive research. Most of these cell-based treatment approaches require experimental in vitro models that rely on a fine understanding of the earliest morphogenetic steps that underlie the in vivo development of the inner ear since its initial induction from a common otic–epibranchial territory. This knowledge will be applied to various proposed experimental cell replacement strategies to either address the feasibility or identify novel therapeutic options for sensorineural hearing loss. In this review, we describe how ear and epibranchial placode development can be recapitulated by focusing on the cellular transformations that occur as the inner ear is converted from a thickening of the surface ectoderm next to the hindbrain known as the otic placode to an otocyst embedded in the head mesenchyme. Finally, we will highlight otic and epibranchial placode development and morphogenetic events towards progenitors of the inner ear and their neurosensory cell derivatives.

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

“…We previously showed that various transcription factor genes essential for hair cell development— Six1 , Eya1 , Sox2 , Atoh1 , Pou4f3 (see Sun and Liu, 2023 ; Zine and Fritzsch, 2023 )—are expressed in developing paddlefish ampullary organs, as well as neuromasts ( Modrell et al, 2011a ; Modrell et al, 2011b ; Butts et al, 2014 ; Modrell et al, 2017a ). We confirm here that, in addition to Sox2 ( Figures 1E–H ; Figures 2A, B ), Atoh1 and Pou4f3 are also expressed in both types of lateral line organs in sterlet ( Figures 2C–F ).…”

“…Of the 42 transcription factor genes with validated expression during lateral line organ development in paddlefish and/or sterlet, 29 (69%) were expressed in both ampullary organs and neuromasts ( Table 1 ). These include the key “hair cell” transcription factor genes Six1 , Eya1 , Sox2 , Atoh1 , Pou4f3 and Gfi1 (see Sun and Liu, 2023 ; Zine and Fritzsch, 2023 ). We also identified eight electrosensory-restricted and five mechanosensory-restricted transcription factor genes ( Table 1 ), as discussed further below.…”

“…Developing ampullary organs also express key “hair cell” transcription factor genes (see Sun and Liu, 2023 ; Zine and Fritzsch, 2023 ) including Six1 , Eya1 , Atoh1 and Pou4f3 ( Brn3c ) ( Modrell et al, 2011a ; Butts et al, 2014 ; Modrell et al, 2017a ). Six1 and Eya1 are jointly required to activate Sox2 in otic neurosensory progenitors ( Xu et al, 2021 ) and cooperate with Sox2 to induce Atoh1 expression in cochlear epithelium ( Ahmed et al, 2012 ).…”

Gene networks and the evolution of olfactory organs, eyes, hair cells and motoneurons: a view encompassing lancelets, tunicates and vertebrates

“…The relative lengths of the notochord and neural tube differ; in lancelets the notochord extends beyond the rostral and caudal ends of the neural tube, in tunicates the neural tube extends rostrally beyond the notochord ( Miyamoto and Crowther, 1985 ; Søviknes et al, 2007 ; Søviknes and Glover, 2008 ; Dong et al, 2009 ), and in all vertebrates the notochord ends near the midbrain-hindbrain boundary, so that the entire prosencephalon extends rostrally beyond the notochord ( Welsch et al, 1998 ; Satoh et al, 2014 ; Witten and Hall, 2022 ; Fritzsch et al, 2023 ). In addition, distinct developmental lineages generate neural crest, placodes, eyes, and taste buds in vertebrates, but not in lancelets or tunicates ( Moody and LaMantia, 2015 ; Holland, 2020 ; Elliott et al, 2022 ; Fritzsch and Martin, 2022 ; Adameyko, 2023 ; Zine and Fritzsch, 2023 ).…”

Research progress on the treatment and nursing of sensorineural hearing loss

“…Sensorineural hearing loss (SNHL) is a common otolaryngologic disorder characterized by damage to the auditory nerve resulting in decreased or complete loss of hearing ( Gregory et al, 2023 ; Matsunaga and Nakagawa, 2023 ; Zine and Fritzsch, 2023 ). The incidence of this disease has been increasing in recent years, which may be associated with factors such as fast-paced lifestyles, high-intensity work, and environmental noise pollution in modern society ( Al-Azzawi and Stapleton, 2023 ; Saba et al, 2023 ).…”