The membranous labyrinth during larval development in lamprey (Lampetra planeri, Bloch, 1784)

Avallone, Bice; Fascio, Umberto; Senatore, Angela; Balsamo, Giuseppe; Bianco, Pier Giorgio; Marmo, Francesco

doi:10.1016/j.heares.2004.09.002

Cited by 7 publications

(5 citation statements)

References 11 publications

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“…1). Adult lamprey inner ears have only two semicircular canals, each with a tricuspid crista, and a single ventrally positioned macula communis that covers the floor of two joined, symmetrical, ciliated chambers (de Burlet and Versteegh, 1930;Lowenstein et al, 1968;Thornhill, 1972;Avallone et al, 2005). A similar pattern, with two semicircular canals, is found in the abundant agnathan fossil record, making it likely that this represents the ancestral condition (Mazan et al, 2000).…”

Section: Introductionmentioning

confidence: 93%

The developing lamprey ear closely resembles the zebrafish otic vesicle:otx1expression can account for all major patterning differences

Hammond

Whitfield

2006

Development

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The inner ear of adult agnathan vertebrates is relatively symmetric about the anteroposterior axis, with only two semicircular canals and a single sensory macula. This contrasts with the highly asymmetric gnathostome arrangement of three canals and several separate maculae. Symmetric ears can be obtained experimentally in gnathostomes in several ways, including by manipulation of zebrafish Hedgehog signalling, and it has been suggested that these phenotypes might represent an atavistic condition. We have found, however, that the symmetry of the adult lamprey inner ear is not reflected in its early development; the lamprey otic vesicle is highly asymmetric about the anteroposterior axis, both morphologically and molecularly, and bears a striking resemblance to the zebrafish otic vesicle. The single sensory macula originates as two foci of hair cells, and later shows regions of homology to the zebrafish utricular and saccular maculae. It is likely, therefore, that the last common ancestor of lampreys and gnathostomes already had well-defined otic anteroposterior asymmetries. Both lamprey and zebrafish otic vesicles express a target of Hedgehog signalling, patched, indicating that both are responsive to Hedgehog signalling. One significant distinction between agnathans and gnathostomes, however, is the acquisition of otic Otx1 expression in the gnathostome lineage. We show that Otx1 knockdown in zebrafish, as in Otx1 -/-mice, gives rise to lamprey-like inner ears. The role of Otx1 in the gnathostome ear is therefore highly conserved; otic Otx1 expression is likely to account not only for the gain of a third semicircular canal and crista in gnathostomes, but also for the separation of the zones of the single macula into distinct regions.

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Section: Introductionmentioning

confidence: 93%

The developing lamprey ear closely resembles the zebrafish otic vesicle:otx1expression can account for all major patterning differences

Hammond

Whitfield

2006

Development

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“…2003, 2004). CaM, CaB, S‐100 and parvalbumin are all parts of the uncalcified organic mass that holds otoconia together in the brook lamprey Lampetra planeri (Avallone et al. 2005).…”

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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“…The macula lagena is a variable sensory organ in the gnathostome group (Fritzsch, 1992; Buran et al,2005). It has been indicated that the macula communis in lamprey contains three clearly distinct macular areas, which could correspond to the saccular, utricular, and lagenar maculae (Avallone et al,2005), suggesting an origin of these three maculae from a single elongated epithelium. Furthermore, it has been proposed that the lagenar macula could originate from the saccular macula (Baird,1974) or from the utricular macula (Platt et al,2004).…”

Section: Discussionmentioning

confidence: 99%

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et al. 2009

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The inner ear is a complex three‐dimensional sensorial structure with auditory and vestibular functions. It originates from the otic placode, which invaginates, forming the otic vesicle; the latter gives rise to neurosensory and nonsensory elements of the adult membranous labyrinth. A hypothesis based on descriptive and experimental evidence suggests that the acquisition of discrete sensory patches during evolution of this primordium may be related to subdivision of an early pansensory domain. In order to gain insight into this developmental mechanism, we carried out a detailed analysis of the spatial and temporal expression pattern of the gene Fgf10, by comparing different markers of otic patterning and hair cell differentiation. Fgf10 expression labels a sensory‐competent domain included in a Serrate‐positive territory from which most of the sensory epithelia arise. Our data show that Fgf10 transcripts are present initially in a narrow ventromedial band of the rudimentary otocyst, extending between its rostral and caudal poles. During development, this Fgf10‐expressing area splits repetitively into several separate subareas, creating six of the eight sensory organs present in birds. Only the lateral crista and the macula neglecta were initially Fgf10 negative, although they activated Fgf10 expression after their specification as sensory elements. These results allowed us to determine a timetable of sensory specification in the developing chick inner ear. The comparison of the expression pattern of Fgf10 with those of other markers of sensory differentiation contributes to our understanding of the mechanism by which vertebrate inner ear prosensory domains have arisen during evolution. J. Comp. Neurol. 521:1136–1164, 2013. © 2012 Wiley Periodicals, Inc.

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The membranous labyrinth during larval development in lamprey (Lampetra planeri, Bloch, 1784)

Cited by 7 publications

References 11 publications

The developing lamprey ear closely resembles the zebrafish otic vesicle:otx1expression can account for all major patterning differences

The developing lamprey ear closely resembles the zebrafish otic vesicle:otx1expression can account for all major patterning differences

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

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