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The evolutionary origin of the Runx/CBFbeta transcription factors--studies of the most basal metazoans.

Sullivan JC, Sher D, Eisenstein M, Shigesada K, Reitzel AM, Marlow H, Levanon D, Groner Y, Finnerty JR, Gat U - BMC Evol. Biol. (2008)

Bottom Line: Comparative structural modeling indicates that the Runx-CBFbeta-DNA complex from most cnidarians and sponges is highly similar to that found in humans, with changes in the residues involved in Runx-CBFbeta dimerization in either of the proteins mirrored by compensatory changes in the binding partner.These results reveal that Runx and CBFbeta likely functioned together to regulate transcription in the common ancestor of all metazoans, and the structure of the Runx-CBFbeta-DNA complex has remained extremely conserved since the human-sponge divergence.The expression data suggest a hypothesis that these genes may have played a role in nerve cell differentiation or maintenance in the common ancestor of cnidarians and bilaterians.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Boston University, 5 Cummington St, Boston, MA 02215, USA. jamescsullivan@gmail.com

ABSTRACT

Background: Members of the Runx family of transcriptional regulators, which bind DNA as heterodimers with CBFbeta, are known to play critical roles in embryonic development in many triploblastic animals such as mammals and insects. They are known to regulate basic developmental processes such as cell fate determination and cellular potency in multiple stem-cell types, including the sensory nerve cell progenitors of ganglia in mammals.

Results: In this study, we detect and characterize the hitherto unexplored Runx/CBFbeta genes of cnidarians and sponges, two basal animal lineages that are well known for their extensive regenerative capacity. Comparative structural modeling indicates that the Runx-CBFbeta-DNA complex from most cnidarians and sponges is highly similar to that found in humans, with changes in the residues involved in Runx-CBFbeta dimerization in either of the proteins mirrored by compensatory changes in the binding partner. In situ hybridization studies reveal that Nematostella Runx and CBFbeta are expressed predominantly in small isolated foci at the base of the ectoderm of the tentacles in adult animals, possibly representing neurons or their progenitors.

Conclusion: These results reveal that Runx and CBFbeta likely functioned together to regulate transcription in the common ancestor of all metazoans, and the structure of the Runx-CBFbeta-DNA complex has remained extremely conserved since the human-sponge divergence. The expression data suggest a hypothesis that these genes may have played a role in nerve cell differentiation or maintenance in the common ancestor of cnidarians and bilaterians.

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Expression of Nv-Runx and Nv-CBFβ in the head region of adult Nematostella anemones. A single anemone specimen was cut into four parts, as shown in the diagram: tentacles, head/pharyngeal region (including tentacle bases), body column, and physa. Reverse-transcription (RT) PCR was performed on an equal amount of total RNA extracted from each of the four body regions. An equivalent fraction of the amplification reaction was visualized on an agarose gel. Using this assay, Nv-Runx expression was detected in the tentacles, and to a lesser extent in the head/pharyngeal region, but not in the column or physa. As a positive control, actin was found to be expressed at high levels in all four body regions.
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Figure 6: Expression of Nv-Runx and Nv-CBFβ in the head region of adult Nematostella anemones. A single anemone specimen was cut into four parts, as shown in the diagram: tentacles, head/pharyngeal region (including tentacle bases), body column, and physa. Reverse-transcription (RT) PCR was performed on an equal amount of total RNA extracted from each of the four body regions. An equivalent fraction of the amplification reaction was visualized on an agarose gel. Using this assay, Nv-Runx expression was detected in the tentacles, and to a lesser extent in the head/pharyngeal region, but not in the column or physa. As a positive control, actin was found to be expressed at high levels in all four body regions.

Mentions: To determine if expression of Nv-Runx and Nv-CBFβ is spatially restricted along the primary body axis of the adult polyp we performed reverse-transcription polymerase chain reaction (RT-PCR) on equal amounts of total RNA isolated from four different body regions: (1) tentacles, (2) head region, (3) body column, and (4) physal region. Using two different primer pairs, Runx expression was detected in the tentacles and head/pharyngeal region but not the body column or physa (Figure 6). High levels of CBFβ expression were observed in the tentacles and head/pharyngeal regions; although a lower level of CBFβ expression could also be detected in the body column. No CBFβ expression was observed in the physal region.


The evolutionary origin of the Runx/CBFbeta transcription factors--studies of the most basal metazoans.

Sullivan JC, Sher D, Eisenstein M, Shigesada K, Reitzel AM, Marlow H, Levanon D, Groner Y, Finnerty JR, Gat U - BMC Evol. Biol. (2008)

Expression of Nv-Runx and Nv-CBFβ in the head region of adult Nematostella anemones. A single anemone specimen was cut into four parts, as shown in the diagram: tentacles, head/pharyngeal region (including tentacle bases), body column, and physa. Reverse-transcription (RT) PCR was performed on an equal amount of total RNA extracted from each of the four body regions. An equivalent fraction of the amplification reaction was visualized on an agarose gel. Using this assay, Nv-Runx expression was detected in the tentacles, and to a lesser extent in the head/pharyngeal region, but not in the column or physa. As a positive control, actin was found to be expressed at high levels in all four body regions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2527000&req=5

Figure 6: Expression of Nv-Runx and Nv-CBFβ in the head region of adult Nematostella anemones. A single anemone specimen was cut into four parts, as shown in the diagram: tentacles, head/pharyngeal region (including tentacle bases), body column, and physa. Reverse-transcription (RT) PCR was performed on an equal amount of total RNA extracted from each of the four body regions. An equivalent fraction of the amplification reaction was visualized on an agarose gel. Using this assay, Nv-Runx expression was detected in the tentacles, and to a lesser extent in the head/pharyngeal region, but not in the column or physa. As a positive control, actin was found to be expressed at high levels in all four body regions.
Mentions: To determine if expression of Nv-Runx and Nv-CBFβ is spatially restricted along the primary body axis of the adult polyp we performed reverse-transcription polymerase chain reaction (RT-PCR) on equal amounts of total RNA isolated from four different body regions: (1) tentacles, (2) head region, (3) body column, and (4) physal region. Using two different primer pairs, Runx expression was detected in the tentacles and head/pharyngeal region but not the body column or physa (Figure 6). High levels of CBFβ expression were observed in the tentacles and head/pharyngeal regions; although a lower level of CBFβ expression could also be detected in the body column. No CBFβ expression was observed in the physal region.

Bottom Line: Comparative structural modeling indicates that the Runx-CBFbeta-DNA complex from most cnidarians and sponges is highly similar to that found in humans, with changes in the residues involved in Runx-CBFbeta dimerization in either of the proteins mirrored by compensatory changes in the binding partner.These results reveal that Runx and CBFbeta likely functioned together to regulate transcription in the common ancestor of all metazoans, and the structure of the Runx-CBFbeta-DNA complex has remained extremely conserved since the human-sponge divergence.The expression data suggest a hypothesis that these genes may have played a role in nerve cell differentiation or maintenance in the common ancestor of cnidarians and bilaterians.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Boston University, 5 Cummington St, Boston, MA 02215, USA. jamescsullivan@gmail.com

ABSTRACT

Background: Members of the Runx family of transcriptional regulators, which bind DNA as heterodimers with CBFbeta, are known to play critical roles in embryonic development in many triploblastic animals such as mammals and insects. They are known to regulate basic developmental processes such as cell fate determination and cellular potency in multiple stem-cell types, including the sensory nerve cell progenitors of ganglia in mammals.

Results: In this study, we detect and characterize the hitherto unexplored Runx/CBFbeta genes of cnidarians and sponges, two basal animal lineages that are well known for their extensive regenerative capacity. Comparative structural modeling indicates that the Runx-CBFbeta-DNA complex from most cnidarians and sponges is highly similar to that found in humans, with changes in the residues involved in Runx-CBFbeta dimerization in either of the proteins mirrored by compensatory changes in the binding partner. In situ hybridization studies reveal that Nematostella Runx and CBFbeta are expressed predominantly in small isolated foci at the base of the ectoderm of the tentacles in adult animals, possibly representing neurons or their progenitors.

Conclusion: These results reveal that Runx and CBFbeta likely functioned together to regulate transcription in the common ancestor of all metazoans, and the structure of the Runx-CBFbeta-DNA complex has remained extremely conserved since the human-sponge divergence. The expression data suggest a hypothesis that these genes may have played a role in nerve cell differentiation or maintenance in the common ancestor of cnidarians and bilaterians.

Show MeSH
Related in: MedlinePlus