Molecular Conservation and Novelties in Vertebrate Ear Development

Abstract

Evolution shaped the vertebrate ear into a complicated three-dimensional structure and positioned the sensory epithelia so that they can extract specific aspects of mechanical stimuli to govern vestibular and hearing-related responses of the whole organism. This information is conducted from the ear via specific neuronal connections to distinct areas of the hindbrain for proper processing. During development, the otic placode, a simple sheet of epidermal cells, transforms into a complicated system of ducts and recesses. This placode also generates the mechanoelectrical transducers, the hair cells, and sensory neurons of the vestibular and cochlear (spiral) ganglia of the ear. We argue that ear development can be broken down into dynamic processes that use a number of known and unknown genes to govern the formation of the threedimensional labyrinth in an interactive fashion. Embedded in this process, but in large part independent of it, is an evolutionary conserved process that induces early the development of the neurosensory component of the ear. We present molecular data suggesting that this later process is, in its basic aspects, related to the mechanosensory cell formation across phyla and is extremely conserved at the molecular level. We suggest that sensory neuron development and maintenance are vertebrate or possibly chordate novelties and present the molecular data to support this notion.

Two contrasting roles for Notch activity in chick inner ear development:specification of prosensory patches and lateral inhibition of hair-cell differentiation

“…Indeed, we noted that ectopic patches tended to form more frequently in vestibular than in auditory regions, and most often in the neighbourhood of the normal sensory patches. Many genes encoding transcription factors or signalling molecules, including components of the FGF, BMP, Hedgehog and Wnt pathways, are expressed in various restricted domains of the early otocyst (Barald and Kelley, 2004;Fekete and Wu, 2002;Fritzsch and Beisel, 2003;Whitfield et al, 2002). It is thus likely that the cooperation of several signalling pathways is required for the establishment of prosensory patches.…”

The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration?

“…(32) However, whereas Neurog1 null mice have a severe reduction in hair cells, notably in the saccule and cochlea, (38) there is only a limited shortening of the cochlea in Neurod1 null mice. (66) This suggests that some precursors that express Neurog1 are also forming hair cells and supporting cells of sensory epithelia whereas precursors that express Neurod1 are already committed to the neuronal lineage. Recently, it was shown that some sensory precursors switch their fate in the absence of Neurog1 and differentiate into hair cells.…”

Evolutionary origins of vertebrate placodes: insights from developmental studies and from comparisons with other deuterostomes

“…Both cell types are placodally derived in vertebrates, and may even originate from a common placodal progenitor cell (reviewed in Fekete and Wu, 2002;Fritzsch and Beisel, 2003). Therefore, it has been proposed that both cell types evolved from a single ancestral type of primary mechanosensory cell Fritzsch and Beisel, 2001 and that specification of sensory neurons involved the secondary recruitment of Neurogenin from an original function during the development of chemosensory neurons as demonstrated for the Drosophila Neurogenin homologue tap (Gautier et al,'97;Ledent et al,'98).…”