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Investigation into the cellular origins of posterior regeneration in the annelid Capitella teleta.

ABSTRACT: Many animals can regenerate, although there is great diversity in regenerative capabilities. A major question in regenerative biology is determining the cellular source of newly formed tissue. The polychaete annelid, Capitella teleta, can regenerate posterior segments following transverse amputation. However, the source, behavior and molecular characteristics of the cells that form new tissue during regeneration are largely unknown. Using an indirect cell tracking method involving 5'-ethynyl-2'-deoxyuridine (EdU) incorporation, we show that cell migration occurs during C. teleta posterior regeneration. Expression of the multipotency/germ line marker CapI-vasa led us to hypothesize that stem cells originate from a multipotent progenitor cell (MPC) cluster, migrate through the coelomic cavity, and contribute to regeneration of tissue. We show that the capacity for posterior regeneration and segment formation is greater with than without the MPC cluster. Finally, we propose a working model of posterior regeneration in C. teleta. This work is the first in C. teleta that addresses the potential source of cells contributing to posterior regeneration, and may provide clues as to why some animals are highly successful regenerators.

SUBMITTER: de Jong DM

PROVIDER: S-EPMC5911572 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Investigation into the cellular origins of posterior regeneration in the annelid <i>Capitella teleta</i>.

de Jong Danielle M DM Seaver Elaine C EC

Regeneration (Oxford, England) 20171206 1

Many animals can regenerate, although there is great diversity in regenerative capabilities. A major question in regenerative biology is determining the cellular source of newly formed tissue. The polychaete annelid, <i>Capitella teleta</i>, can regenerate posterior segments following transverse amputation. However, the source, behavior and molecular characteristics of the cells that form new tissue during regeneration are largely unknown. Using an indirect cell tracking method involving 5'-ethy ...[more]

PMID: 29721327

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Project description:Regeneration, the ability to replace lost tissues and body parts following traumatic injury, occurs widely throughout the animal tree of life. Regeneration occurs either by remodeling of pre-existing tissues, through addition of new cells by cell division, or a combination of both. We describe a staging system for posterior regeneration in the annelid, Capitella teleta, and use the C. teleta Hox gene code as markers of regional identity for regenerating tissue along the anterior-posterior axis. Following amputation of different posterior regions of the animal, a blastema forms and by two days, proliferating cells are detected by EdU incorporation, demonstrating that epimorphosis occurs during posterior regeneration of C. teleta. Neurites rapidly extend into the blastema, and gradually become organized into discrete nerves before new ganglia appear approximately seven days after amputation. In situ hybridization shows that seven of the ten Hox genes examined are expressed in the blastema, suggesting roles in patterning the newly forming tissue, although neither spatial nor temporal co-linearity was detected. We hypothesized that following amputation, Hox gene expression in pre-existing segments would be re-organized to scale, and the remaining fragment would express the complete suite of Hox genes. Surprisingly, most Hox genes display stable expression patterns in the ganglia of pre-existing tissue following amputation at multiple axial positions, indicating general stability of segmental identity. However, the three Hox genes, CapI-lox4, CapI-lox2 and CapI-Post2, each shift its anterior expression boundary by one segment, and each shift includes a subset of cells in the ganglia. This expression shift depends upon the axial position of the amputation. In C. teleta, thoracic segments exhibit stable positional identity with limited morphallaxis, in contrast with the extensive body remodeling that occurs during regeneration of some other annelids, planarians and acoel flatworms.

Project description:The Cytochrome P450 super family (CYP) is responsible for a wide range of functions in metazoans, having roles in both exogenous and endogenous substrate metabolism. Annelids are known to metabolize polycyclic aromatic hydrocarbons (PAHs) and produce estrogen. CYPs are postulated to be key enzymes in these processes in annelids. In this study, the CYP complement (CYPome) of the annelid Capitella teleta has been robustly identified and annotated with the genome assembly available. Phylogenetic analyses were performed to understand the evolutionary relationships between CYPs in C. teleta and other species. Predictions of which CYPs are potentially involved in both PAH metabolism and steroidogensis were made based on phylogeny. Annotation of 84 full length and 12 partial CYP sequences predicted a total of 96 functional CYPs in C. teleta. A further 13 CYP fragments were found but these may be pseudogenes. The C. teleta CYPome contained 24 novel CYP families and seven novel CYP subfamilies within existing families. A phylogenetic analysis identified that the C. teleta sequences were found in 9 of the 11 metazoan CYP clans. Two CYPs, CYP3071A1 and CYP3072A1, did not cluster with any metazoan CYP clans. We found xenobiotic response elements (XREs) upstream of C. teleta CYPs related to vertebrate CYP1 (CYP3060A1, CYP3061A1) and from families with reported transcriptional upregulation in response to PAH exposure (CYP4, CYP331). C. teleta had a CYP51A1 with ?65% identity to vertebrate CYP51A1 sequences and has been predicted to have lanosterol 14 ?-demethylase activity. CYP376A1, CYP3068A1, CYP3069A1, and CYP3070A1 were the most appropriate candidates for steroidogenesis genes based on their phylogeny and warrant further analyses, though no specific aromatase (estrogen synthesis) candidates were found. Presence of XREs upstream of C. teleta CYPs may indicate a functional aryl hydrocarbon receptor in C. teleta and candidate CYPs for studies of PAH metabolism.

Project description:BACKGROUND:How nervous systems evolved remains an unresolved question. Previous studies in vertebrates and arthropods revealed that homologous genes regulate important neurogenic processes such as cell proliferation and differentiation. However, the mechanisms through which such homologs regulate neurogenesis across different bilaterian clades are variable, making inferences about nervous system evolution difficult. A better understanding of neurogenesis in the third major bilaterian clade, Spiralia, would greatly contribute to our ability to deduce the ancestral mechanism of neurogenesis. RESULTS:Using whole-mount in situ hybridization, we examined spatiotemporal gene expression for homologs of soxB, musashi, prospero, achaete-scute, neurogenin, and neuroD in embryos and larvae of the spiralian annelid Capitella teleta, which has a central nervous system (CNS) comprising a brain and ventral nerve cord. For all homologs examined, we found expression in the neuroectoderm and/or CNS during neurogenesis. Furthermore, the onset of expression and localization within the developing neural tissue for each of these genes indicates putative roles in separate phases of neurogenesis, e.g., in neural precursor cells (NPCs) versus in cells that have exited the cell cycle. Ct-soxB1, Ct-soxB, and Ct-ngn are the earliest genes expressed in surface cells in the anterior and ventral neuroectoderm, while Ct-ash1 expression initiates slightly later in surface neuroectoderm. Ct-pros is expressed in single cells in neural and non-neural ectoderm, while Ct-msi and Ct-neuroD are localized to differentiating neural cells in the brain and ventral nerve cord. CONCLUSIONS:These results suggest that the genes investigated in this article are involved in a neurogenic gene regulatory network in C. teleta. We propose that Ct-SoxB1, Ct-SoxB, and Ct-Ngn are involved in maintaining NPCs in a proliferative state. Ct-Pros may function in division of NPCs, Ct-Ash1 may promote cell cycle exit and ingression of NPC daughter cells, and Ct-NeuroD and Ct-Msi may control neuronal differentiation. Our results support the idea of a common genetic toolkit driving neural development whose molecular architecture has been rearranged within and across clades during evolution. Future functional studies should help elucidate the role of these homologs during C. teleta neurogenesis and identify which aspects of bilaterian neurogenesis may have been ancestral or were derived within Spiralia.

Project description:BACKGROUND:Reconstructing the evolutionary history of nervous systems requires an understanding of their architecture and development across diverse taxa. The spiralians encompass diverse body plans and organ systems, and within the spiralians, annelids exhibit a variety of morphologies, life histories, feeding modes and associated nervous systems, making them an ideal group for studying evolution of nervous systems. RESULTS:We describe nervous system development in the annelid Capitella teleta (Blake JA, Grassle JP, Eckelbarger KJ. Capitella teleta, a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. Zoosymposia. 2009;2:25-53) using whole-mount in situ hybridization for a synaptotagmin 1 homolog, nuclear stains, and cross-reactive antibodies against acetylated ?-tubulin, 5-HT and FMRFamide. Capitella teleta is member of the Sedentaria (Struck TH, Paul C, Hill N, Hartmann S, Hosel C, Kube M, et al. Phylogenomic analyses unravel annelid evolution. Nature. 2011;471:95-8) and has an indirectly-developing, lecithotrophic larva. The nervous system of C. teleta shares many features with other annelids, including a brain and a ladder-like ventral nerve cord with five connectives, reiterated commissures, and pairs of peripheral nerves. Development of the nervous system begins with the first neurons differentiating in the brain, and follows a temporal order from central to peripheral and from anterior to posterior. Similar to other annelids, neurons with serotonin-like-immunoreactivity (5HT-LIR) and FMRFamide-like-immunoreactivity (FMRF-LIR) are found throughout the brain and ventral nerve cord. A small number of larval-specific neurons and neurites are present, but are visible only after the central nervous system begins to form. These larval neurons are not visible after metamorphosis while the rest of the nervous system is largely unchanged in juveniles. CONCLUSIONS:Most of the nervous system that forms during larvogenesis in C. teleta persists into the juvenile stage. The first neurons differentiate in the brain, which contrasts with the early formation of peripheral, larval-specific neurons found in some spiralian taxa with planktotrophic larvae. Our study provides a clear indication that certain shared features among annelids - e.g., five connectives in the ventral nerve cord - are only visible during larval stages in particular species, emphasizing the need to include developmental data in ancestral character state reconstructions. The data provided in this paper will serve as an important comparative reference for understanding evolution of nervous systems, and as a framework for future molecular studies of development.

Dataset Information

Investigation into the cellular origins of posterior regeneration in the annelid Capitella teleta.

Publications

Investigation into the cellular origins of posterior regeneration in the annelid <i>Capitella teleta</i>.

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