Skeletal development in <i>Xenopus laevis</i> (Anura: Pipidae)

Trueb, Linda; Howard, James L.

doi:10.1002/jmor.1052140102

Cited by 165 publications

(270 citation statements)

References 27 publications

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“…2A). This staining pattern coincides with the future location of the larval suprarostral plate (Trueb and Hanken, 1992;Seufert et al, 1994), and is similar to the anterior anlagen of the suprarostral cartilages described for Rana temporaria (Spemann, 1898). These paired stains are separate from the presumptive cranial trabeculae, which do not express runx2 until stage 35/36.…”

Section: Runx2 Expressionsupporting

confidence: 84%

“…Instead, a single, continuous and median plate of cartilage is first visible in histological sections through the anterior ethmoid region. Several studies have accepted the homology between the paired suprarostrals of most anurans and the median suprarostral plate of pipids (Sokol, 1975(Sokol, , 1977Trueb and Hanken, 1992;Swart and de Sá, 1999;Pugener et al, 2003). Others, however, have denied this homology because the suprarostral plate does not appear to form from paired chondrogenic precursors (de Beer, 1937;Sedra and Michael, 1957;Roček and Vesley, 1989;Roček, 2003).…”

Section: Runx2 In Larval Xenopus 1657mentioning

confidence: 99%

“…The posterior section of the loop corresponds to the future subocular arch of the palatoquadrate. This arch eventually fuses to the ventrolateral process of the neurocranium, which forms the larval ascending and otic processes (Trueb and Hanken, 1992). The medial and ventral portion of the loop is continuous with a faint patch of staining, which corresponds to the future Meckel's and infrarostral cartilages.…”

Section: Runx2 In Larval Xenopus 1657mentioning

confidence: 99%

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Runx2 is essential for larval hyobranchial cartilage formation in Xenopus laevis

Kerney

Gross

Howard

2007

Developmental Dynamics

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The vertebrate transcription factor protein Runx2 is regarded as a "master regulator" of bone formation due to the dramatic loss of the osseous skeleton in the mouse homozygous knockout. However, Runx2 mRNA also is expressed in the pre-hypertrophic cartilaginous skeleton of the mouse and chicken, where its developmental function is largely unknown. Several tiers of Runx2 regulation exist in the mouse, any of which may account for its seeming biological inactivity during early stages of skeletogenesis. Unlike mouse and chicken, zebrafish require Runx2 function in early cartilage differentiation. The present study reveals that the earlier functional role of Runx2 in cartilage differentiation is shared between zebrafish and Xenopus. A combination of morpholino oligonucleotide injections and neural crest transplants indicate that Runx2 is involved in differentiation of the cartilaginous hyobranchial skeleton in the frog, Xenopus laevis. Additionally, in situ hybridizations show runx2 mRNA expression in mesenchymal precursors of the cartilaginous skull, which reveals the earliest pre-patterning of these cartilages described to date. The early distribution of runx2 resolves the homology of the larval suprarostral plate, which is one of the oldest controversies of anuran skull development. Together these data reveal a shift in Runx2 protein function during vertebrate evolution towards its exclusive roles in cartilage hypertrophy and bone differentiation within the amniote lineage. Developmental Dynamics 236:1650 -1662, 2007.

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Section: Runx2 Expressionsupporting

confidence: 84%

Section: Runx2 In Larval Xenopus 1657mentioning

confidence: 99%

Section: Runx2 In Larval Xenopus 1657mentioning

confidence: 99%

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Runx2 is essential for larval hyobranchial cartilage formation in Xenopus laevis

Kerney

Gross

Howard

2007

Developmental Dynamics

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“…In many previous studies on skeletal development, particularly on amphibians (Kemp and Hoyt 1969;Gaudin 1978;Trueb and Hanken 1992), intraspecific variation in developmental timing has been demonstrated relative to a particular developmental stage (Gaudin 1978), but rarely in relative sequence of ossification events. A major exception to this is the work of Garn and colleagues, who documented intraspecific variation in the order of ossification of bones of the appendicular and axial skeleton of humans (Garn and Rohmann 1960;Garn et al 1961aGarn et al ,b, 1966.…”

Section: Discussionmentioning

confidence: 99%

An Experimental Study of Intraspecific Variation, Developmental Timing, and Heterochrony in Fishes

2000

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Abstract. Heterochrony is widely regarded as an important evolutionary mechanism, one that may underlie most, if not all, morphological evolution, yet relatively few studies have examined variation in the sequence of development. Even fewer studies have been designed so that intraspecific variation in the relative sequence of developmental events can be assessed, although this variation must be the basis for evolutionary change. Intraspecific variation in developmental ossification sequences was documented from the zebrafish (Danio rerio) by Cubbage and Mabee (1996) and from the Siamese fighting fish (Betta splendens) by Mabee and Trendler (1996), but a quantitative analysis of the patterns within this variation was not made. Here, we quantify the effect of rearing temperature on the sequence of ossification and characterize the levels and patterns of intraspecific variation in these fishes. For Danio, there were no temperature effects on the sequence of bone development across the cranium, cranial region development, cartilage versus dermal bones, or lateral line bone versus nonassociated bones. Likewise the level of variation in relative sequence (position) of ossification was low, about two ranks, across temperatures. At higher temperatures, we found higher levels of variation in iterated cranial bones and less in bones forming early in the sequence. No temperature effects on variation were found among regions, between lateral line-associated bones and nonassociated bones, between median and paired bones, or across the entire sequence, indicating concordant variability among the three temperatures. Individual bones with the highest levels of variability were not consistent among temperatures.Baseline patterns of intraspecific variation in Danio were compared to those of Betta. For both species, the level of intraspecific variation in sequence position was low and the variability of cranial bones was concordant. Individual bones with the highest levels of variability were not consistent between species. In both species, variation was widespread (distributed evenly across the sequence). We used comparisons (among regions, between dermal and cartilage bones, between lateral line-associated and other bones, between median and paired bones, between iterated and noniterated bones, between feeding-associated bones and others) to see which subsets were most variable and thus potentially useful in predicting high levels of evolutionary change. The only subset of bones that was significantly more variable than others was cartilage bones. If interspecific patterns are parallel to these intraspecific differences, cartilage bones would be expected to show higher levels of heterochrony. Although concordance across the cranial ossification sequence and among regions in Danio, Betta, and two other teleosts, Oryzias and Barbus, suggests an evolutionarily conserved pattern of ossification, identity in sequence position across taxa was not observed for any bone. Thus, variation existed in sequence position across temperatures a...

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“…1C). During metamorphosis, new cartilages contribute to the adult nasal capsule and sound-conducting plectral apparatus (Trueb and Hanken, 1992;Gross and Hanken, 2008). Metamorphic formation of alary and superior prenasal cartilages in the nasal capsule corresponds with heightened col2a1 mRNA expression (Fig.…”

Section: In Situ Hybridizationsmentioning

confidence: 99%

Regulatory elements of Xenopus col2a1 drive cartilaginous gene expression in transgenic frogs

Kerney¹,

Hall²,

Howard³

2010

Int. J. Dev. Biol.

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This study characterizes regulatory elements of collagen 2α1 (col2a1) in Xenopus that enable transgene expression in cartilage-forming chondrocytes. The reporters described in this study drive strong cartilage-specific gene expression, which will be a valuable tool for further investigations of Xenopus skeletal development. While endogenous col2a1 mRNA is expressed in many embryonic tissues, its expression becomes restricted to tadpole and adult chondrocytes. This chondrocyte-specific expression is recapitulated by col2a1 reporter constructs, which were tested through I-SceI meganuclease-mediated transgenesis. These constructs contain a portion of the Xenopus tropicalis col2a1 intron, which aligns to a cartilage-specific intronic enhancer that has been well characterized in mammals. Two overlapping regions of the first intron that are 1.5-Kb and 665-bp long, both of which contain this enhancer sequence, drove EGFP expression in both larval and adult chondrocytes when connected to an upstream promoter. However, neither a truncated 155-bp region that also contains the enhancer, nor a separate 347-bp intronic region that lacks it, was able to drive cartilaginous transgene expression. The two cartilage-specific transgenes are heritable in F1 progeny, which exhibit none of the background expression observed in the injected founders. This study is the first to use the I-SceI technique to characterize an enhancer element in Xenopus, and the first to generate chondrocyte-specific gene expression in a nonmammalian vertebrate. The creation of novel cartilage-specific gene expression provides a new tool for further studies of anuran skeletal development.

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Skeletal development in Xenopus laevis (Anura: Pipidae)

Cited by 165 publications

References 27 publications

Runx2 is essential for larval hyobranchial cartilage formation in Xenopus laevis

Runx2 is essential for larval hyobranchial cartilage formation in Xenopus laevis

An Experimental Study of Intraspecific Variation, Developmental Timing, and Heterochrony in Fishes

Regulatory elements of Xenopus col2a1 drive cartilaginous gene expression in transgenic frogs

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