Molecular characterization of Calymmin, a novel notochord sheath‐associated extracellular matrix protein in the zebrafish embryo

Cerdà, Joan; Gründ, Christine; Franke, Werner W.; Brand, Michael

doi:10.1002/dvdy.10101

Cited by 18 publications

(14 citation statements)

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“…2006); these findings, however, have not been related to the morphogenesis of the elastica externa. Furthermore, in zebrafish, the protein calymmin is transiently expressed by the notochord from 13 to 24 h post‐fertilization, and has been detected in an outer compartment of the notochord sheath (Cerdà et al. 2002), a layer with the same morphological features as the elastica externa observed here at an early stage in salmon (see Cerdà et al.…”

Section: Discussionmentioning

confidence: 63%

Stepwise enforcement of the notochord and its intersection with the myoseptum: an evolutionary path leading to development of the vertebra?

et al. 2006

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The notochord constitutes the main axial support during the embryonic and larval stages, and the arrangement of collagen fibrils within the notochord sheath is assumed to play a decisive role in determining its functional properties as a fibre-wound hydrostatic skeleton. We have found that during early ontogeny in Atlantic salmon stepwise changes occur in the configuration of the collagen fibre-winding of the notochord sheath. The sheath consists of a basal lamina, a layer of type II collagen, and an elastica externa that delimits the notochord; and these constituents are secreted in a specific order. Initially, the collagen fibrils are circumferentially arranged perpendicular to the longitudinal axis, and this specific spatial fibril configuration is maintained until hatching when the collagen becomes reorganized into distinct layers or lamellae. Within each lamella, fibrils are parallel to each other, forming helices around the longitudinal axis of the notochord, with a tangent angle of 75-80 ° to the cranio-caudal axis.The helical geometry shifts between adjacent lamellae, forming enantiomorphous left-and right-handed coils, respectively, thus enforcing the sheath. The observed changes in the fibre-winding configuration may reflect adaptation of the notochord to functional demands related to stage in ontogeny. When the vertebral bodies initially form as chordacentra, the collagen lamellae of the sheath in the vertebral region are fixed by the deposition of minerals; in the intervertebral region, however, they represent a pre-adaptation providing torsional stability to the intervertebral joint. Hence, these modifications of the sheath transform the notochord per se into a functional vertebral column. The elastica externa, encasing the notochord, has serrated surfaces, connected inward to the type II collagen of the sheath, and outward to type I collagen of the mesenchymal connective tissue surrounding the notochord. In a similar manner, the collagen matrix of the neural and haemal arch cartilages is tightly anchored to the outward surface of the elastic membrane. Hence, the elastic membrane may serve as an interface between the notochord and the adjacent structures, with an essential function related to transmission of tensile forces from the musculature. The interconnection between the notochord and the myosepta is discussed in relation to function and to evolution of the arches and the vertebra. Contrary to current understanding, this study also shows that notochord vacuolization does not result in an increased elongation of the embryo, which agrees with the circular arrangement of type II collagen that probably only enables a restricted increase in girth upon vacuolization, not aiding elongation. As the vacuolization occurs during the egg stage, this type of collagen disposition, in combination with an elastica externa, also probably facilitates flexibility and curling of the embryo.

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Section: Discussionmentioning

confidence: 63%

Stepwise enforcement of the notochord and its intersection with the myoseptum: an evolutionary path leading to development of the vertebra?

et al. 2006

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“…46 In the notochord, perp expression ceases at 36 hpf, in parallel with many other markers of differentiating notochord cells, such as the secreted protein Calymmin. 47 In the lens, perp starts to be expressed around 24 hpf and vanishes again during the second day of development, very similar to the dynamics of connexin43 and 44, markers for differentiating lens fiber cells. 48 Similarly, in the gastrointestinal tract, 49,50 pronephric ducts, 51 and cartilage, 52,53 perp expression coincides with cell differentiation.…”

Section: Discussionmentioning

confidence: 75%

Perp is required for tissue-specific cell survival during zebrafish development

2004

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The tumor suppressor p53 has two alternative effects, causing either cell cycle arrest or apoptosis. These different effects are supposed to be mediated by the transcriptional activation of different target genes. perp, encoding a transmembrane protein of the Pmp22 family, is a transcriptional p53 target exclusively upregulated in apoptotic cells. However, its role during normal development had remained largely unclear. Here, we report the isolation and characterization of a zebrafish perp homolog. Upon overexpression in early zebrafish embryos, perp induces apoptosis. In addition, it contributes to p53-dependent and UVinduced cell death. However, during normal zebrafish development, perp displays a p53-independent and spatially restricted expression in specific cell types and tissues. Antisensemediated loss of Perp function leads to increased apoptosis in perp-expressing cells of the developing skin and notochord. We conclude that, in contrast to its proapoptotic function in stressed cells, Perp plays an antiapoptotic role during normal zebrafish development to regulate tissue-specific cell survival. Cell Death and Differentiation (2005) Keywords: perp; p53; pmp22; apoptosis; cell survival; zebrafish; development Abbreviations: AO, acridine orange; BrdU, 5 0 Bromo-2 0 -desoxyuridine; DNp63, amino-terminally truncated isoform of p63; EST, expressed sequence tag; EVL, enveloping layer; hpf, hours postfertilization; mdm2, mouse double minute 2; MO, morpholino oligonucleotide; RT-PCR, polymerase chain reaction after reverse transcription of RNA; SDS-PAGE, sodiumdodecylsulfate polyacrylamide gel electrophoresis; TAp73, transactivating N-terminally full-length isoform of p73; TUNEL, terminal deoxynucleotidyl transferase-mediated biotinylated UTP nick end labeling; UV, ultraviolet; 4 mm, four mismatch control

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“…These include shh (Krauss et al 1993), no tail (SchulteMerker et al 1992), semaphorin Z2 (Halloran et al 1998), calreticulin (Rubinstein et al 2000), treb5 (Liang et al 2001), col2a1 (Yan et al 1995), calymmin (Cerda et al 2002), cathepsin l (Mangos et al 2000), hsp47 (Lele and Krone 1997), and brain subtype creatine kinase (Dickmeis et al 2001b). To assess the pattern of expression of the remaining clones, an in situ hybridization screen with the entire initial set of cDNA clones was performed.…”

Section: Groups Of Coexpressed Genes Identified By In Situ Hybridizationmentioning

confidence: 99%

Expression Profiling and Comparative Genomics Identify a Conserved Regulatory Region Controlling Midline Expression in the Zebrafish Embryo

Dickmeis¹,

Plessy²,

Rastegar³

et al. 2004

Genome Res.

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Differential gene transcription is a fundamental regulatory mechanism of biological systems during development, body homeostasis, and disease. Comparative genomics is believed to be a rapid means for the identification of regulatory sequences in genomes. We tested this approach to identify regulatory sequences that control expression in the midline of the zebrafish embryo. We first isolated a set of genes that are coexpressed in the midline of the zebrafish embryo during somitogenesis stages by gene array analysis and subsequent rescreens by in situ hybridization. We subjected 45 of these genes to Compare and DotPlot analysis to detect conserved sequences in noncoding regions of orthologous loci in the zebrafish and Takifugu genomes. The regions of homology that were scored in nonconserved regions were inserted into expression vectors and tested for their regulatory activity by transient transgenesis in the zebrafish embryo. We identified one conserved region from the connective tissue growth factor gene (ctgf), which was able to drive expression in the midline of the embryo. This region shares sequence similarity with other floor plate/notochord-specific regulatory regions. Our results demonstrate that an unbiased comparative approach is a relevant method for the identification of tissue-specific cis-regulatory sequences in the zebrafish embryo.[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank under accession nos. AY428026-AY428035, CD777505-CD777543, and CD777544-CD778191.]Differential gene transcription is essential for many developmental processes and physiological responses. Moreover, evolution of the body plan is thought to have been driven to a large extent by changes in gene expression, and differences in gene expression are believed to determine disease risk (Davidson 2001; Ludwig 2002 and references therein). A detailed knowledge of the cisregulatory architecture of genomes is thus a central prerequisite for a comprehensive understanding of many fundamental biological processes and has also medical implications.Despite enormous progress in our understanding of transcriptional regulation in vertebrates (Davidson 2001), we are not able to unequivocally predict the pattern and responsiveness of expression by mere sequence analysis of a gene. This is largely because of the structure and the scattered location of cisregulatory regions in the huge vertebrate genomes (Davidson 2001). In vertebrates, promoter regions are rarely sufficient to drive faithful gene transcription. Frequently, other regulatory regions contribute to the correct spatial and temporal expression of genes. These regions can be scattered over large distances in noncoding sequences, and they can be located upstream, downstream, and in intronic regions (Davidson 2001). Regulatory regions are usually a composite of multiple transcription-factorbinding sites. The small size and degenerate DNA sequence of these binding sites renders a genome-wide computational analys...

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Molecular characterization of Calymmin, a novel notochord sheath‐associated extracellular matrix protein in the zebrafish embryo

Cited by 18 publications

References 50 publications

Stepwise enforcement of the notochord and its intersection with the myoseptum: an evolutionary path leading to development of the vertebra?

Stepwise enforcement of the notochord and its intersection with the myoseptum: an evolutionary path leading to development of the vertebra?

Perp is required for tissue-specific cell survival during zebrafish development

Expression Profiling and Comparative Genomics Identify a Conserved Regulatory Region Controlling Midline Expression in the Zebrafish Embryo

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