Topological and Developmental Gradients of Calbindin Expression in the Chick's Inner Ear

Hiel, Hakim; Navaratnam, Dasakumar; Oberholtzer, J. Carl; Fuchs, Paul

doi:10.1007/s101620010071

Cited by 25 publications

(25 citation statements)

References 56 publications

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“…Actin was detected by our array but found not to be tonotopically expressed (data not shown), a finding that is intuitive given that the total amount of actin per hair cell does not vary tonotopically in chickens (Tilney and Tilney 1988). The calcium binding protein calbindin was previously found to be expressed at higher levels in basal than in apical hair cells (Navaratnam et al 1995;Navaratnam et al 1997;Hiel et al 2002), a finding that was not confirmed by our microarray data. However, this observation is likely the result of the 3′ bias of the Affymetrix chicken array.…”

Section: Discussioncontrasting

confidence: 92%

“…In contrast, previous work showing tonotopicity of calbindin expression used qPCR primers designed to amplify a portion of the transcript that is present in all 25 variants, and these results are therefore much more reliable (Navaratnam et al 1995(Navaratnam et al , 1997Hiel et al 2002). That calbindin was not found by microarray to be tonotopically expressed therefore likely reflects the spatial distribution of an exceedingly rare splice variant.…”

Section: Tablementioning

confidence: 82%

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Gene Expression Gradients along the Tonotopic Axis of the Chicken Auditory Epithelium

Frucht

Uduman

Kleinstein

et al. 2011

JARO

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There are known differences in the properties of hair cells along the tonotopic axis of the avian auditory epithelium, the basilar papilla (BP). To determine the genetic basis of these differences, we compared gene expression between the high-(HF), middle-, and lowfrequency (LF) thirds of 0-day-old chick auditory epithelia. RNA amplified from each sample was hybridized to whole-genome chicken arrays and GeneSpring software was used to identify differentially expressed genes. Two thousand six hundred sixty-three genes were found to be differentially expressed between the HF and LF segments, using a fold-change cutoff of 2 and a p value of 0.05. Many ion channel genes were differentially expressed between the HF and LF regions of the BP, an expression pattern that was previously established for some but not all of these genes. Quantitative PCR was used to verify tonotopic expression of 15 genes, including KCNMA1 (Slo) and its alternatively spliced STREX exon. Gene set enrichment analyses (GSEA) were performed on the microarray data and revealed many microRNA gene sets significantly enriched in the HF relative to the LF end, suggesting a tonotopic activity gradient. GSEA also suggested differential activity of the kinases protein kinase C and protein kinase A at the HF and LF ends, an interesting corollary to the observation that there is tonotopic expression of the STREX exon that confers on Slo sensitivity to the activity of kinases. Taken together, these results suggest mechanisms of induction and maintenance of tonotopicity and enhance our understanding of the complex nature of proximal-distal gene expression gradients in the chicken BP.

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Section: Discussioncontrasting

confidence: 92%

Section: Tablementioning

confidence: 82%

Gene Expression Gradients along the Tonotopic Axis of the Chicken Auditory Epithelium

Frucht

Uduman

Kleinstein

et al. 2011

JARO

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“…It is not surprising therefore that calmodulin (CaM) has been identified in the cochlea of gerbil (Nakazawa, 2001) and guinea pig (Furness et al 2002), and that calbindin-D28-K (CaB) has been found in the primate (Usami et al 1995) and chick (Hiel et al 2002) inner ear, in the dog cochlea (Coppens et al 2000) and in the otoconia of the musk shrew (Karita et al 1999). In the lizard Podarcis sicula , CaB is present on the outer surface, in the central core (Balsamo et al 2000) and in the organic matrix of otoconia (Piscopo et al 2003(Piscopo et al , 2004.…”

Section: Introductionmentioning

confidence: 99%

Morphological and biochemical analyses of otoliths of the ice‐fish Chionodraco hamatus confirm a common origin with red‐blooded species

Motta¹,

Avallone²,

Balassone

et al. 2008

Journal of Anatomy

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The morphology and composition of the three otoliths of the Antarctic ice-fish Chionodraco hamatus were studied by scanning electron microscopy and X-ray diffraction. The composition of the sagitta, lapillus and asteriscus protein matrices was also analysed by sodium dodecyl sulphate-polyacrylamide gel electrophoresis, western blots and confocal laser scanning microscopy to reveal the presence of and to localize the calcium-binding proteins calmodulin, calbindin and S-100. Morphological results indicated that the otoliths in this ice-fish were similar to those of Trematomus bernacchii , a red-blooded Antarctic species [B. Avallone et al. (2003) J. Submicrosc. Cytol. Pathol. 35 , 69-76], but rather different from those of other teleosts. These two Antarctic species possessed a completely vateritic asteriscus, whereas their sagitta and lapillus were made mostly of aragonite. Parallel analysis of protein patterns in C. hamatus and T. bernacchii revealed that the sagitta significantly differed from the lapillus and asteriscus in both species. The sagitta did not contain the S-100 protein and showed calmodulin and calbindin located in discontinuous or incremental zones, respectively. These results demonstrate that the otoliths of C. hamatus and T. bernacchii share more resemblances than differences and support the idea of a common origin of these species.

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“…Calbindin, encoding a calcium binding protein, is expressed strongly in basal hair cells and this expression gradually becomes weaker in hair cells toward the apex of the BP (Fig. 3C) (22). Graded levels of Calbindin expression in hair cells are postulated to be required for calciumdependent, frequency-specific responses along the tonotopic axis of the BP (22).…”

Section: Resultsmentioning

confidence: 99%

Conserved role of Sonic Hedgehog in tonotopic organization of the avian basilar papilla and mammalian cochlea

Son¹,

Hyun

Ankamreddy

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Sound frequency discrimination begins at the organ of Corti in mammals and the basilar papilla in birds. Both of these hearing organs are tonotopically organized such that sensory hair cells at the basal (proximal) end respond to high frequency sound, whereas their counterparts at the apex (distal) respond to low frequencies. Sonic hedgehog (Shh) secreted by the developing notochord and floor plate is required for cochlear formation in both species. In mice, the apical region of the developing cochlea, closer to the ventral midline source of Shh, requires higher levels of Shh signaling than the basal cochlea farther away from the midline. Here, gain-of-function experiments using Shh-soaked beads in ovo or a mouse model expressing constitutively activated Smoothened (transducer of Shh signaling) show up-regulation of apical genes in the basal cochlea, even though these regionally expressed genes are not necessarily conserved between the two species. In chicken, these altered gene expression patterns precede morphological and physiological changes in sensory hair cells that are typically associated with tonotopy such as the total number of stereocilia per hair cell and gene expression of an inward rectifier potassium channel, IRK1, which is a bona fide feature of apical hair cells in the basilar papilla. Furthermore, our results suggest that this conserved role of Shh in establishing cochlear tonotopy is initiated early in development by Shh emanating from the notochord and floor plate.frequency discrimination | regional identity | Inhba | A2m | Efnb2

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Topological and Developmental Gradients of Calbindin Expression in the Chick's Inner Ear

Cited by 25 publications

References 56 publications

Gene Expression Gradients along the Tonotopic Axis of the Chicken Auditory Epithelium

Gene Expression Gradients along the Tonotopic Axis of the Chicken Auditory Epithelium

Morphological and biochemical analyses of otoliths of the ice‐fish Chionodraco hamatus confirm a common origin with red‐blooded species

Conserved role of Sonic Hedgehog in tonotopic organization of the avian basilar papilla and mammalian cochlea

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