Transcriptome dynamics in the asexual cycle of the chordate Botryllus schlosseri

Campagna, Davide; Gasparini, Fabio; Franchi, Nicola; Vitulo, Nicola; Ballin, Francesca; Manni, Lucia; Valle, Giorgio; Ballarin, Loriano

doi:10.1186/s12864-016-2598-1

Cited by 30 publications

(30 citation statements)

References 79 publications

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“…Transcriptome analysis of B. schlosseri (Voskoboynik et al. ; Campagna et al., ) identified an EST similar to the predicted histamine H2 receptor like of the acorn worm Saccoglossus kowalevskii (GenBank accession no. XM_006823267.1 ).…”

Section: Resultsmentioning

confidence: 99%

Histamine Stimulates Ciliary Beat Frequency via the H2 Receptor in the ProtochordateBotryllus schlosseri

Cima

Franchi

2016

J Exp Zool Pt B

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Histamine is a biogenic molecule that plays a role in many physiological pathways via binding to a specific receptor. Histaminergic receptors belong to the large family of seven-transmembrane α-helix domain receptors classified in mammals into four distinct classes: H1, H2, H3, and H4. Despite being widely studied in vertebrates, few data are available on the invertebrate receptors, with only predicted H1 and H2 sequences for nonchordate deuterostomes. Here, we report the first characterized transcript sequence for an H2 receptor from the colonial ascidian Botryllus schlosseri, describing the localization of both transcript and protein during blastogenic development through in situ hybridization and immunohistochemistry. Its phylogenetic relationships with deuterostome orthologous proteins are reported, its role in ciliary beat frequency (CBF) in cultured stigma cells of the branchial basket is outlined, and the effects of histamine and its receptor agonists and antagonists are analyzed. In the presence of increasing concentrations of histamine in the medium, CBF increases similarly to the selective H2 receptor agonist dimaprit. In contrast, ranitidine, which is an inhibitor of the H2 receptor, causes a significant inhibition of CBF, similar to that observed after preincubation with the specific anti-BsHRH2 or the anti-human HRH2 antibody. In cells bordering the branchial basket stigmata, both antibodies colocalize in the proximal region of the ciliary plasmalemma, and histamine is present inside vesicles of the apical region, thus supporting the hypothesis of a histamine-binding H2 receptor control of the pharyngeal mucociliary transport similar to that of the upper respiratory tract and middle ear in mammals.

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Section: Resultsmentioning

confidence: 99%

Histamine Stimulates Ciliary Beat Frequency via the H2 Receptor in the ProtochordateBotryllus schlosseri

Cima

Franchi

2016

J Exp Zool Pt B

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“…Our EST collection was aligned on the Botryllus genome already available online (Voskoboynik et al, 2013). With this approach, many coding sequences (CDS) were recognized and recorded in our database (Campagna et al, 2016). Comparison of our CDS collection (Campagna et al, 2016) with the sequences of the vertebrate genes of interest allowed us to identify a series of nucleotide sequences and to design specific primers (Table 1) for PCR amplification.…”

Section: Exposure To Cadmiummentioning

confidence: 99%

“…With this approach, many coding sequences (CDS) were recognized and recorded in our database (Campagna et al, 2016). Comparison of our CDS collection (Campagna et al, 2016) with the sequences of the vertebrate genes of interest allowed us to identify a series of nucleotide sequences and to design specific primers (Table 1) for PCR amplification. We focused our attention on the sequences of the predicted transcripts for GCLM, GS, Cu/Zn-SOD, GPx3, and GPx5, known as BsGCLM, BsGS, BsCu/Zn-SOD, BsGPx3, and BsGPx5, respectively.…”

Section: Exposure To Cadmiummentioning

confidence: 99%

“…Forward and reverse primers for BsGCLM (BsGCLF-RT and BsGCLR-RT), BsGS (BsGSF-RT and BsGSR-RT), BsCu/ Zn-SOD (BsSODF-RT and BsSODR-RT), BsGPx3 (BsGPx3F and BsGPx3R-RT), BsGPx5 (BsGPx5F-RT and BsGPx5R-RT), and Bsb-actin (BsACTF-RT and BsACTR-RT) transcripts--the last one (Bsb-actin) used as a housekeeping gene--were synthesized by Sigma-Aldrich (St. Louis, MO) ( Table 1). The stable expression of Bsb-actin level (Campagna et al, 2016) explains the choice of cytoplasmic actin as reference gene for quantitative PCR experiments. To exclude contamination by genomic DNA, all of the designed primers contained parts of contiguous exons; a qualitative PCR was also carried out before qRT-PCR.…”

Section: Exposure To Cadmiummentioning

confidence: 99%

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Protection from Oxidative Stress in Immunocytes of the Colonial Ascidian Botryllus schlosseri: Transcript Characterization and Expression Studies

Franchi

Ballin

Ballarin

2017

The Biological Bulletin

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Botryllus schlosseri is a cosmopolitan colonial ascidian that undergoes cyclical generation changes, or take-overs, during which adult zooids are resorbed and replaced by their buds. At take-over, adult tissues undergo diffuse apoptosis and effete cells are massively ingested by circulating phagocytes, with a consequent increase in oxygen consumption and in production of reactive oxygen species (ROS). The latter are responsible for the death of phagocytes involved in the clearance of apoptotic cells and corpses by phagocytosis-induced apoptosis. However, the majority of phagocytes and hemocytes do not die, even if they experience oxidative stress. This fact suggests the presence of detoxification mechanisms assuring their protection. To test this assumption, we searched for transcripts of genes involved in detoxification in the transcriptome of B. schlosseri. We identified and characterized transcripts for Cu/Zn superoxide dismutase (SOD), γ-glutamyl-cysteine ligase modulatory subunit (GCLM), glutathione synthase (GS), and two glutathione peroxidases (i.e., GPx3 and GPx5), all involved in protection from ROS. We also carried out a phylogenetic analysis of the putative amino acid sequences, confirming their similarity to their vertebrate counterparts, and studied the location of their mRNAs by in situ hybridization on hemocyte monolayers. We also analyzed gene transcription during the colonial blastogenetic cycle, which is the interval of time between one take-over and the next, by qRT-PCR. In addition, we investigated the effects of cadmium (Cd), an inducer of oxidative stress, on gene transcription. Our results indicated that i) antioxidant gene expression is modulated in the course of the blastogenetic cycle and upon exposure to Cd, and ii) hemocytes synthesize both enzymatic and nonenzymatic antioxidants, in line with the idea that they represent a major detoxification system for ascidians.

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“…The data reported include supporting information to the phylogenetic analyses of Franchi et al [1] . They consist of transcript sequences, sequence alignments and comparisons of four apoptosis-related genes identified in the recently-obtained transcriptome of B. schlosseri [2] . The sequences show high similarity with mammalian transcripts for Bax, AIF1, PARP1 and IAP7 and were named BsBax, BsAIF1, BsPARP1 and BsIAP7, respectively.…”

Section: Datamentioning

confidence: 99%

Data on four apoptosis-related genes in the colonial tunicate Botryllus schlosseri

et al. 2016

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The data described are related to the article entitled “Recurrent phagocytosis-induced apoptosis in the cyclical generation change of the compound ascidian Botryllus schlosseri” (Franchi et al., 2016) [1]. Four apoptosis-related genes, showing high similarity with mammalian Bax (a member of the Bcl-2 protein family), AIF1 (apoptosis-inducing factor-1), PARP1 (poly ADP ribose polymerase-1) and IAP7 (inhibitor of apoptosis-7) were identified from the analysis of the trascriptome of B. schlosseri. They were named BsBax, BsAIF1, BsPARP1 and BsIAP7. Here, their deduced amino acid sequence were compared with known sequences of orthologous genes from other deuterostome species together with a study of their identity/similarity.

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Transcriptome dynamics in the asexual cycle of the chordate Botryllus schlosseri

Cited by 30 publications

References 79 publications

Histamine Stimulates Ciliary Beat Frequency via the H2 Receptor in the ProtochordateBotryllus schlosseri

Histamine Stimulates Ciliary Beat Frequency via the H2 Receptor in the ProtochordateBotryllus schlosseri

Protection from Oxidative Stress in Immunocytes of the Colonial Ascidian Botryllus schlosseri: Transcript Characterization and Expression Studies

Data on four apoptosis-related genes in the colonial tunicate Botryllus schlosseri

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