Dataset Information

Melanotransferrin: New Homolog Genes and Their Differential Expression during Intestinal Regeneration in the Sea Cucumber Holothuria glaberrima.

ABSTRACT: Melanotransferrin (MTf) is a protein associated with oncogenetic, developmental, and immune processes which function remains unclear. The MTf gene has been reported in numerous vertebrate and invertebrate species, including echinoderms. We now report the finding of four different MTfs in the transcriptome of the sea cucumber Holothuria glaberrima. Sequence studies and phylogenetic analyses were done to ascertain the similarities among the putative proteins and their relationship with other transferrin family members. The genes were shown to be differentially expressed in various holothurian organs and to respond differently when the animals were challenged with the immune system activator lipopolysaccharide (LPS). Moreover, the four genes were found to be highly overexpressed during the early stages of intestinal regeneration. The finding of four different genes in the holothurian is particularly surprising, because only one MTf gene has been reported in all other animal species sequenced to date. This finding, combined with the increase expression during intestinal regeneration, suggests a new possible function of MTf in organ regenerative processes.

SUBMITTER: Hernandez-Pasos J

PROVIDER: S-EPMC5432042 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Melanotransferrin: New Homolog Genes and Their Differential Expression during Intestinal Regeneration in the Sea Cucumber Holothuria glaberrima.

Hernández-Pasos Josué J Valentín-Tirado Griselle G García-Arrarás José E JE

Journal of experimental zoology. Part B, Molecular and developmental evolution 20170223 3

Melanotransferrin (MTf) is a protein associated with oncogenetic, developmental, and immune processes which function remains unclear. The MTf gene has been reported in numerous vertebrate and invertebrate species, including echinoderms. We now report the finding of four different MTfs in the transcriptome of the sea cucumber Holothuria glaberrima. Sequence studies and phylogenetic analyses were done to ascertain the similarities among the putative proteins and their relationship with other trans ...[more]

PMID: 28229527

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Project description:Almost every organism has the ability of repairing damaged tissues or replacing lost and worn out body parts, nevertheless the degree of the response substantially differs between each species. Adult sea cucumbers from the Holothuria glaberrima species can eviscerate various organs and the intestinal system is the first one to regenerate. This process involves the formation of a blastema-like structure that derives from the torn mesentery edges by the intervention of specific cellular processes (e.g., cell dedifferentiation and division). Still, the genetic networks controlling the regenerative response in this model system are just starting to be unraveled. In this work we examined if and how the retinoic acid (RA) signaling pathway is involved in the regenerative response of this deuterostome. We first identified and characterized the holothurian orthologs for short chain dehydrogenase/reductase 7 (SDR7) and aldehyde dehydrogenase family 8A1 (ALDH8A1), two enzymes respectively associated with retinaldehyde and RA anabolism. We then showed that the SDR7 transcript was differentially expressed during specific stages of intestinal regeneration while ALDH8A1 did not show significant differences in regenerating tissues when compared to those of normal (non-eviscerated) organisms. Finally, we investigated the consequences of modulating RA signaling during intestinal regeneration using pharmacological tools. We showed that application of an inhibitor (citral) of the enzyme synthesizing RA or a retinoic acid receptor (RAR) antagonist (LE135) resulted in organisms with a significantly smaller intestinal rudiment when compared to those treated with DMSO (vehicle). The two inhibitors caused a reduction in cell division and cell dedifferentiation in the new regenerate when compared to organisms treated with DMSO. Results of treatment with tazarotene (an RAR agonist) were not significantly different from the control. Taken together, these results suggest that the RA signaling pathway is regulating the cellular processes that are crucial for intestinal regeneration to occur. Thus, RA might be playing a role in echinoderm regeneration that is similar to what has been described in other animal systems.

Project description:Among deuterostomes, the regenerative potential is maximally expressed in echinoderms, animals that can quickly replace most injured organs. In particular, sea cucumbers are excellent models for studying organ regeneration since they regenerate their digestive tract after evisceration. However, echinoderms have been sidelined in modern regeneration studies partially because of the lack of genome-wide profiling approaches afforded by modern genomic tools.For the last decade, our laboratory has been using the sea cucumber Holothuria glaberrima to dissect the cellular and molecular events that allow for such amazing regenerative processes. We have already established an EST database obtained from cDNA libraries of normal and regenerating intestine at two different regeneration stages. This database now has over 7000 sequences.In the present work we used a custom-made microchip from Agilent with 60-mer probes for these ESTs, to determine the gene expression profile during intestinal regeneration. Here we compared the expression profile of animals at three different intestinal regeneration stages (3-, 7- and 14-days post evisceration) against the profile from normal (uneviscerated) intestines. The number of differentially expressed probes ranged from 70% at p < 0.05 to 39% at p < 0.001. Clustering analyses show specific profiles of expression for early (first week) and late (second week) regeneration stages. We used semiquantitative reverse transcriptase polymerase chain reaction (RT-PCR) to validate the expression profile of fifteen microarray detected differentially expressed genes which resulted in over 86% concordance between both techniques. Most of the differentially expressed ESTs showed no clear similarity to sequences in the databases and might represent novel genes associated with regeneration. However, other ESTs were similar to genes known to be involved in regeneration-related processes, wound healing, cell proliferation, differentiation, morphological plasticity, cell survival, stress response, immune challenge, and neoplastic transformation. Among those that have been validated, cytoskeletal genes, such as actins, and developmental genes, such as Wnt and Hox genes, show interesting expression profiles during regeneration.Our findings set the base for future studies into the molecular basis of intestinal regeneration. Moreover, it advances the use of echinoderms in regenerative biology, animals that because of their amazing properties and their key evolutionary position, might provide important clues to the genetic basis of regenerative processes.

Dataset Information

Melanotransferrin: New Homolog Genes and Their Differential Expression during Intestinal Regeneration in the Sea Cucumber Holothuria glaberrima.

Publications

Melanotransferrin: New Homolog Genes and Their Differential Expression during Intestinal Regeneration in the Sea Cucumber Holothuria glaberrima.

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