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Up-regulation of SUMO E3 ligases during lung schistosomula and adult worm stages

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Abstract

Small ubiquitin-like modifier (SUMO) conjugation of proteins occurs through a concert action of enzymes using a similar ubiquitination mechanism. After a C-terminal peptide is cleaved from the SUMO precursor by a protease to reveal a di-glycine motif, SUMO is activated by an E1 enzyme (Aos1/Uba2) and conjugated to target proteins by the sole E2 enzyme (Ubc9) guided to the appropriate substrates by the SUMO E3 ligase. Previous reports from our group showed that Schistosoma mansoni has two paralogs of SUMO: one E2 conjugation Ubc9 and two SUMO-specific proteases (SENPs). The differential gene expression profile observed for SUMO pathway genes throughout the S. mansoni life cycle attests for the distinct patterns of SUMO conjugates observed during parasite development particularly during the cercariae to schistosomula transition. To continue this investigation, we here analysed the repertoire of SUMO E3 ligases and their expression profiles during cercariae/schistosomula transition. In silico analysis through S. mansoni databases showed two conserved SUMO E3 ligases: protein inhibitor of activated STAT (PIAS) and Ran-binding protein 2 (RanBP2). Furthermore, expression levels of the SUMO E3 ligases were measured by qRT-PCR using total RNA from cercariae, adult worms and mechanically transformed schistosomula. Our data showed an up-regulation of expression in lung schistosomula and adult worm stages. In conclusion, the differential expression of SmPIAS and SmRanBP2 during schistosomula development was similar to the expression levels of all genes related to SUMO conjugation, thereby suggesting that the control of protein activity, localisation or stability during cercariae to schistosomula transition is SUMO-dependent.

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Acknowledgments

The authors would like to thank the following transcriptome initiatives: the São Paulo Transcriptome Consortium, the Minas Gerais Genome Network and the Wellcome Trust Genome Initiative (UK). This work was supported by the following Brazilian research agencies: FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais, CBB 0558/09), NuBio UFOP (Núcleo de Bioinformática da Universidade Federal de Ouro Preto) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico).

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Authors and Affiliations

  1. Núcleo de Pesquisas em Ciências Biológicas, Instituto de Ciências Exatas e Biológicas - ICEB2, Universidade Federal de Ouro Preto, Morro do Cruzeiro, Ouro Preto, MG, Brazil

    Roberta V. Pereira, William de Castro-Borges & Renata Guerra-Sá

  2. Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Patos de Minas, MG, Brazil

    Matheus de S. Gomes

  3. Departamento de Parasitologia, Universidade de São Paulo, Butantan, São Paulo, SP, Brazil

    Fernanda Janku Cabral

  4. Centro de Pesquisas René Rachou, Fiocruz, Belo Horizonte, MG, Brazil

    Liana K. Jannotti-Passos

  5. Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, São Paulo, SP, Brazil

    Vanderlei Rodrigues

Authors
  1. Roberta V. Pereira
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  2. Matheus de S. Gomes
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  3. Fernanda Janku Cabral
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  4. Liana K. Jannotti-Passos
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  5. Vanderlei Rodrigues
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  6. William de Castro-Borges
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  7. Renata Guerra-Sá
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Corresponding author

Correspondence to Renata Guerra-Sá.

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Fig. S1

Domain of SmPIAS. PIAS is characterised by an essential RING-like domain with similarities to the RING finger of ubiquitin E3 ligases. (JPEG 55 kb)

High resolution image (TIFF 512 kb)

Fig. S2

Domain of SmRanBP2. RanBP2 is a component of the nuclear pore complex. This protein has domains that can bind to RanGTP and RanGDP, as well as repeats for nuclear transport receptor binding and a cyclophilin homology region but has no obvious similarity to other E3 ligases. (JPEG 108 kb)

High resolution image (TIFF 951 kb)

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Pereira, R.V., de S. Gomes, M., Cabral, F.J. et al. Up-regulation of SUMO E3 ligases during lung schistosomula and adult worm stages. Parasitol Res 113, 2019–2025 (2014). https://doi.org/10.1007/s00436-014-3841-9

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  • DOI: https://doi.org/10.1007/s00436-014-3841-9

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