Jag1b is essential for patterning inner ear sensory cristae by regulating anterior morphogenetic tissue separation and preventing posterior cell death

Ma, Weirui; Zhang, Jian

doi:10.1242/dev.113662

Cited by 12 publications

(11 citation statements)

References 70 publications

(81 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In fact, our tracing experiments suggest that some of the early-Notch active cells can switch off Notch activity and develop into non-sensory cells into a wide range of locations. Furthermore, a study in the zebrafish otic vesicle showed that Jag1 is transiently expressed in cells that end up separating the anterior crista from the macula ( Ma and Zhang, 2015 ). We found that Lmx1a is one of the factors required for the attenuation of lateral induction: the absence of Lmx1a results in expanded Jag1+ territories in the Bsd mouse vestibular system, whilst the overexpression of cLmx1b in the chick inner ear reduces Jag1 expression and results in misplaced sensory patch borders.…”

Section: Discussionmentioning

confidence: 99%

Shaping of inner ear sensory organs through antagonistic interactions between Notch signalling and Lmx1a

Mann

Gálvez

Pedreno

et al. 2017

eLife

View full text Add to dashboard Cite

The mechanisms of formation of the distinct sensory organs of the inner ear and the non-sensory domains that separate them are still unclear. Here, we show that several sensory patches arise by progressive segregation from a common prosensory domain in the embryonic chicken and mouse otocyst. This process is regulated by mutually antagonistic signals: Notch signalling and Lmx1a. Notch-mediated lateral induction promotes prosensory fate. Some of the early Notch-active cells, however, are normally diverted from this fate and increasing lateral induction produces misshapen or fused sensory organs in the chick. Conversely Lmx1a (or cLmx1b in the chick) allows sensory organ segregation by antagonizing lateral induction and promoting commitment to the non-sensory fate. Our findings highlight the dynamic nature of sensory patch formation and the labile character of the sensory-competent progenitors, which could have facilitated the emergence of new inner ear organs and their functional diversification in the course of evolution.

show abstract

Section: Discussionmentioning

confidence: 99%

Shaping of inner ear sensory organs through antagonistic interactions between Notch signalling and Lmx1a

Mann

Gálvez

Pedreno

et al. 2017

eLife

View full text Add to dashboard Cite

show abstract

“…Jag1b is also expressed in the developing lateral line system in zebrafish ( Gwak et al, 2010 ), but its role there is unknown. In the zebrafish otic vesicle, jag1b is expressed in prosensory domains and maintained in sensory patches: it is required both for posterior crista survival (likely acting via Fgf10), and to prevent the spread of a region of Fgf-induced non-sensory cells that segregates the anterior and lateral cristae within the anterior prosensory domain ( Ma and Zhang, 2015 ). In the mouse and chicken inner ear, Jag1-Notch signaling in Sox2-positive prosensory domains blocks cell differentiation, maintaining Sox2 expression and thus the competence of the prosensory domains to form both hair cells and supporting cells ( Kiernan et al, 2006 , Neves et al, 2011 , Dvorakova et al, 2016 ), while lateral inhibition via Delta-Notch signaling, downstream of Atoh1 expression, determines which cells adopt a hair cell versus supporting cell fate ( Neves et al, 2011 ).…”

Section: Discussionmentioning

confidence: 99%

Notch and Fgf signaling during electrosensory versus mechanosensory lateral line organ development in a non-teleost ray-finned fish

Modrell

Tidswell

Baker

2017

Developmental Biology

View full text Add to dashboard Cite

The lateral line system is a useful model for studying the embryonic and evolutionary diversification of different organs and cell types. In jawed vertebrates, this ancestrally comprises lines of mechanosensory neuromasts over the head and trunk, flanked on the head by fields of electrosensory ampullary organs, all innervated by lateral line neurons in cranial lateral line ganglia. Both types of sense organs, and their afferent neurons, develop from cranial lateral line placodes. Current research primarily focuses on the posterior lateral line primordium in zebrafish, which migrates as a cell collective along the trunk; epithelial rosettes form in the trailing zone and are deposited as a line of neuromasts, within which hair cells and supporting cells differentiate. However, in at least some other teleosts (e.g. catfishes) and all non-teleosts, lines of cranial neuromasts are formed by placodes that elongate to form a sensory ridge, which subsequently fragments, with neuromasts differentiating in a line along the crest of the ridge. Furthermore, in many non-teleost species, electrosensory ampullary organs develop from the flanks of the sensory ridge. It is unknown to what extent the molecular mechanisms underlying neuromast formation from the zebrafish migrating posterior lateral line primordium are conserved with the as-yet unexplored molecular mechanisms underlying neuromast and ampullary organ formation from elongating lateral line placodes. Here, we report experiments in an electroreceptive non-teleost ray-finned fish, the Mississippi paddlefish Polyodon spathula, that suggest a conserved role for Notch signaling in regulating lateral line organ receptor cell number, but potentially divergent roles for the fibroblast growth factor signaling pathway, both between neuromasts and ampullary organs, and between paddlefish and zebrafish.

show abstract

“…Indeed, studies on three mouse mutants – Slalom 33 , Headturner 48 , and Ozzy 34 – have described specific point mutations in Jag1 resulting in malformations of the semicircular canals, and we and others observe frequent losses and anomalies of the superior and posterior semicircular canals in AGS patients 14, 15, 37 . Further, the role of Jagged-Notch signaling in the development of the vestibular system also appears to be conserved in zebrafish, as jag1b mutants were independently isolated based on semicircular canal defects 49, 50 . However, we found that NCC-specific loss of Jag1 in mice causes hearing loss without affecting canal morphology, consistent with defects in the stapes and/or other middle and inner ear structures being responsible for hearing defects in these mice.…”

Section: Discussionmentioning

confidence: 99%

Requirement for Jagged1-Notch2 signaling in patterning the bones of the mouse and human middle ear

Teng

Yen

Barske

et al. 2017

Sci Rep

View full text Add to dashboard Cite

Whereas Jagged1-Notch2 signaling is known to pattern the sensorineural components of the inner ear, its role in middle ear development has been less clear. We previously reported a role for Jagged-Notch signaling in shaping skeletal elements derived from the first two pharyngeal arches of zebrafish. Here we show a conserved requirement for Jagged1-Notch2 signaling in patterning the stapes and incus middle ear bones derived from the equivalent pharyngeal arches of mammals. Mice lacking Jagged1 or Notch2 in neural crest-derived cells (NCCs) of the pharyngeal arches display a malformed stapes. Heterozygous Jagged1 knockout mice, a model for Alagille Syndrome (AGS), also display stapes and incus defects. We find that Jagged1-Notch2 signaling functions early to pattern the stapes cartilage template, with stapes malformations correlating with hearing loss across all frequencies. We observe similar stapes defects and hearing loss in one patient with heterozygous JAGGED1 loss, and a diversity of conductive and sensorineural hearing loss in nearly half of AGS patients, many of which carry JAGGED1 mutations. Our findings reveal deep conservation of Jagged1-Notch2 signaling in patterning the pharyngeal arches from fish to mouse to man, despite the very different functions of their skeletal derivatives in jaw support and sound transduction.

show abstract

Jag1b is essential for patterning inner ear sensory cristae by regulating anterior morphogenetic tissue separation and preventing posterior cell death

Cited by 12 publications

References 70 publications

Shaping of inner ear sensory organs through antagonistic interactions between Notch signalling and Lmx1a

Shaping of inner ear sensory organs through antagonistic interactions between Notch signalling and Lmx1a

Notch and Fgf signaling during electrosensory versus mechanosensory lateral line organ development in a non-teleost ray-finned fish

Requirement for Jagged1-Notch2 signaling in patterning the bones of the mouse and human middle ear

Contact Info

Product

Resources

About