Abstract
The regeneration of the oral siphon (OS) and other distal structures in the ascidian Ciona intestinalis occurs by epimorphosis involving the formation of a blastema of proliferating cells. Despite the longstanding use of Ciona as a model in molecular developmental biology, regeneration in this system has not been previously explored by molecular analysis. Here we have employed microarray analysis and quantitative real time RT-PCR to identify genes with differential expression profiles during OS regeneration. The majority of differentially expressed genes were downregulated during OS regeneration, suggesting roles in normal growth and homeostasis. However, a subset of differentially expressed genes was upregulated in the regenerating OS, suggesting functional roles during regeneration. Among the upregulated genes were key members of the Notch signaling pathway, including those encoding the delta and jagged ligands, two fringe modulators, and to a lesser extent the notch receptor. In situ hybridization showed a complementary pattern of delta1 and notch gene expression in the blastema of the regenerating OS. Chemical inhibition of the Notch signaling pathway reduced the levels of cell proliferation in the branchial sac, a stem cell niche that contributes progenitor cells to the regenerating OS, and in the OS regeneration blastema, where siphon muscle fibers eventually re-differentiate. Chemical inhibition also prevented the replacement of oral siphon pigment organs, sensory receptors rimming the entrance of the OS, and siphon muscle fibers, but had no effects on the formation of the wound epidermis. Since Notch signaling is involved in the maintenance of proliferative activity in both the Ciona and vertebrate regeneration blastema, the results suggest a conserved evolutionary role of this signaling pathway in chordate regeneration. The genes identified in this investigation provide the foundation for future molecular analysis of OS regeneration.
| Original language | English |
|---|---|
| Pages (from-to) | 304-315 |
| Number of pages | 12 |
| Journal | Developmental Biology |
| Volume | 405 |
| Issue number | 2 |
| DOIs | |
| Publication status | Published - Sep 15 2015 |
| Externally published | Yes |
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Keywords
- Blastema
- Cell
- Ciona intestinalis
- Differential gene expression
- Muscle differentiation
- Notch pathway
- Proliferation
- Regeneration
ASJC Scopus subject areas
- Developmental Biology
- Cell Biology
- Molecular Biology
- Medicine(all)
Cite this
Evolution of the chordate regeneration blastema : Differential gene expression and conserved role of notch signaling during siphon regeneration in the ascidian Ciona. / Hamada, Mayuko; Goricki, Spela; Byerly, Mardi S.; Satoh, Noriyuki; Jeffery, William R.
In: Developmental Biology, Vol. 405, No. 2, 15.09.2015, p. 304-315.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Evolution of the chordate regeneration blastema
T2 - Differential gene expression and conserved role of notch signaling during siphon regeneration in the ascidian Ciona
AU - Hamada, Mayuko
AU - Goricki, Spela
AU - Byerly, Mardi S.
AU - Satoh, Noriyuki
AU - Jeffery, William R.
PY - 2015/9/15
Y1 - 2015/9/15
N2 - The regeneration of the oral siphon (OS) and other distal structures in the ascidian Ciona intestinalis occurs by epimorphosis involving the formation of a blastema of proliferating cells. Despite the longstanding use of Ciona as a model in molecular developmental biology, regeneration in this system has not been previously explored by molecular analysis. Here we have employed microarray analysis and quantitative real time RT-PCR to identify genes with differential expression profiles during OS regeneration. The majority of differentially expressed genes were downregulated during OS regeneration, suggesting roles in normal growth and homeostasis. However, a subset of differentially expressed genes was upregulated in the regenerating OS, suggesting functional roles during regeneration. Among the upregulated genes were key members of the Notch signaling pathway, including those encoding the delta and jagged ligands, two fringe modulators, and to a lesser extent the notch receptor. In situ hybridization showed a complementary pattern of delta1 and notch gene expression in the blastema of the regenerating OS. Chemical inhibition of the Notch signaling pathway reduced the levels of cell proliferation in the branchial sac, a stem cell niche that contributes progenitor cells to the regenerating OS, and in the OS regeneration blastema, where siphon muscle fibers eventually re-differentiate. Chemical inhibition also prevented the replacement of oral siphon pigment organs, sensory receptors rimming the entrance of the OS, and siphon muscle fibers, but had no effects on the formation of the wound epidermis. Since Notch signaling is involved in the maintenance of proliferative activity in both the Ciona and vertebrate regeneration blastema, the results suggest a conserved evolutionary role of this signaling pathway in chordate regeneration. The genes identified in this investigation provide the foundation for future molecular analysis of OS regeneration.
AB - The regeneration of the oral siphon (OS) and other distal structures in the ascidian Ciona intestinalis occurs by epimorphosis involving the formation of a blastema of proliferating cells. Despite the longstanding use of Ciona as a model in molecular developmental biology, regeneration in this system has not been previously explored by molecular analysis. Here we have employed microarray analysis and quantitative real time RT-PCR to identify genes with differential expression profiles during OS regeneration. The majority of differentially expressed genes were downregulated during OS regeneration, suggesting roles in normal growth and homeostasis. However, a subset of differentially expressed genes was upregulated in the regenerating OS, suggesting functional roles during regeneration. Among the upregulated genes were key members of the Notch signaling pathway, including those encoding the delta and jagged ligands, two fringe modulators, and to a lesser extent the notch receptor. In situ hybridization showed a complementary pattern of delta1 and notch gene expression in the blastema of the regenerating OS. Chemical inhibition of the Notch signaling pathway reduced the levels of cell proliferation in the branchial sac, a stem cell niche that contributes progenitor cells to the regenerating OS, and in the OS regeneration blastema, where siphon muscle fibers eventually re-differentiate. Chemical inhibition also prevented the replacement of oral siphon pigment organs, sensory receptors rimming the entrance of the OS, and siphon muscle fibers, but had no effects on the formation of the wound epidermis. Since Notch signaling is involved in the maintenance of proliferative activity in both the Ciona and vertebrate regeneration blastema, the results suggest a conserved evolutionary role of this signaling pathway in chordate regeneration. The genes identified in this investigation provide the foundation for future molecular analysis of OS regeneration.
KW - Blastema
KW - Cell
KW - Ciona intestinalis
KW - Differential gene expression
KW - Muscle differentiation
KW - Notch pathway
KW - Proliferation
KW - Regeneration
UR - http://www.scopus.com/inward/record.url?scp=84939270049&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84939270049&partnerID=8YFLogxK
U2 - 10.1016/j.ydbio.2015.07.017
DO - 10.1016/j.ydbio.2015.07.017
M3 - Article
C2 - 26206613
AN - SCOPUS:84939270049
VL - 405
SP - 304
EP - 315
JO - Developmental Biology
JF - Developmental Biology
SN - 0012-1606
IS - 2
ER -