» Articles » PMID: 33913473

Apoptosis is a Generator of Wnt-dependent Regeneration and Homeostatic Cell Renewal in the Ascidian Ciona

Overview
Journal Biol Open
Specialty Biology
Date 2021 Apr 29
PMID 33913473
Citations 8
Authors
Affiliations
Soon will be listed here.
Abstract

In the ascidian Ciona intestinalis, basal body parts regenerate distal structures but distal body parts do not replace basal structures. Regeneration involves the activity of adult stem cells in the branchial sac, which proliferate and produce migratory progenitor cells for tissue and organ replacement. Branchial sac-derived stem cells also replenish recycling cells lining the pharyngeal fissures during homeostatic growth. Apoptosis at injury sites occurs early during regeneration and continuously in the pharyngeal fissures during homeostatic growth. Caspase 1 inhibitor, caspase 3 inhibitor, or pan-caspase inhibitor Z-VAD-FMK treatment blocked apoptosis, prevented regeneration, and suppressed branchial sac growth and function. A pharmacological screen and siRNA-mediated gene knockdown indicated that regeneration requires canonical Wnt signaling. Wnt3a protein rescued both caspase-blocked regeneration and branchial sac growth. Inhibition of apoptosis did not affect branchial sac stem cell proliferation but prevented the survival of progenitor cells. After bisection across the mid-body, apoptosis occurred only in the regenerating basal fragments, although both fragments contained a part of the branchial sac, suggesting that apoptosis is unilateral at the wound site and the presence of branchial sac stem cells is insufficient for regeneration. The results suggest that apoptosis-dependent Wnt signaling mediates regeneration and homeostatic growth in Ciona.

Citing Articles

PI3K-AKT-mediated phosphorylation of Thr260 in CgCaspase-3/6/7 regulates heat-induced activation in oysters.

Wang C, Du M, Jiang Z, Cong R, Wang W, Zhang T Commun Biol. 2024; 7(1):1459.

PMID: 39511363 PMC: 11543851. DOI: 10.1038/s42003-024-07184-4.


Evolution of Apoptotic Signaling Pathways Within Lophotrochozoans.

Horkan H, Popgeorgiev N, Vervoort M, Gazave E, Krasovec G Genome Biol Evol. 2024; 16(10).

PMID: 39318156 PMC: 11463336. DOI: 10.1093/gbe/evae204.


Intrinsic apoptosis is evolutionarily divergent among metazoans.

Krasovec G, Horkan H, Queinnec E, Chambon J Evol Lett. 2024; 8(2):267-282.

PMID: 38525035 PMC: 10959488. DOI: 10.1093/evlett/qrad057.


The ctenophore Mnemiopsis leidyi deploys a rapid injury response dating back to the last common animal ancestor.

Mitchell D, Edgar A, Mateu J, Ryan J, Martindale M Commun Biol. 2024; 7(1):203.

PMID: 38374160 PMC: 10876535. DOI: 10.1038/s42003-024-05901-7.


Differentially expressed chaperone genes reveal a stress response required for unidirectional regeneration in the basal chordate Ciona.

Jeffery W, Li B, Ng M, Li L, Goricki S, Ma L BMC Biol. 2023; 21(1):148.

PMID: 37365564 PMC: 10294541. DOI: 10.1186/s12915-023-01633-y.


References
1.
Kassmer S, Nourizadeh S, De Tomaso A . Cellular and molecular mechanisms of regeneration in colonial and solitary Ascidians. Dev Biol. 2018; 448(2):271-278. DOI: 10.1016/j.ydbio.2018.11.021. View

2.
Freeman G . THE ROLE OF BLOOD CELLS IN THE PROCESS OF ASEXUAL REPORODUCTION IN THE TUNICATE PEROPHORA VIRIDIS. J Exp Zool. 1964; 156:157-83. DOI: 10.1002/jez.1401560204. View

3.
Whyte J, Smith A, Helms J . Wnt signaling and injury repair. Cold Spring Harb Perspect Biol. 2012; 4(8):a008078. PMC: 3405869. DOI: 10.1101/cshperspect.a008078. View

4.
Bergmann A, Steller H . Apoptosis, stem cells, and tissue regeneration. Sci Signal. 2010; 3(145):re8. PMC: 2991142. DOI: 10.1126/scisignal.3145re8. View

5.
Hwang J, Kobayashi C, Agata K, Ikeo K, Gojobori T . Detection of apoptosis during planarian regeneration by the expression of apoptosis-related genes and TUNEL assay. Gene. 2004; 333:15-25. DOI: 10.1016/j.gene.2004.02.034. View