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Sci Rep
2016 Oct 13;6:35030. doi: 10.1038/srep35030.
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Cloning and in vitro characterization of a Schistosoma japonicum aquaglyceroporin that functions in osmoregulation.
Huang Y
,
Li W
,
Lu W
,
Xiong C
,
Yang Y
,
Yan H
,
Liu KC
,
Cao P
.
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As one of the three major human pathogens that cause schistosomiasis, Schistosoma japonicum is the only one that is endemic in China. Despite great progress on schistosomiasis control over the past 50 years in China, S. japonicum transmission still occurs in certain endemic regions, which causes significant public health problems and enormous economic losses. During different life stages, parasites are able to survive dramatic osmolality changes between its vector, fresh water, and mammal host. However, the molecular mechanism of parasite osmoregulation remains unknown. To address this challenging question, we report the first cloning of an S. japonicum aquaglyceroporin (SjAQP) from an isolate from Jiangsu province, China. Expressing SjAQP in Xenopus oocytes facilitated the permeation of water, glycerol, and urea. The water permeability of SjAQP was inhibited by 1 mM HgCl2, 3 mM tetraethylammonium, 1 mM ZnCl2, and 1 mM CuSO4. SjAQP was constitutively expressed throughout the S. japonicum life cycle, including in the egg, miracidia, cercaria, and adult stages. The highest expression was detected during the infective cercaria stage. Our results suggest that SjAQP plays a role in osmoregulation throughout the S. japonicum life cycle, especially during cercariae transformation, which enables parasites to survive osmotic challenges.
Figure 1. Deduced primary protein sequence and phylogenetic analysis of SjAQP.(A) Deduced amino acid sequence of SjAQP and alignment with its homolog SmAQP from Schistosoma mansoni. Asterisks indicate fully conserved residues; colons indicate strongly conserved similar residues with scores >0.5 in the Gonnet PAM 250 matrix; and periods indicate weakly similar residues with scores ≤0.5 in the matrix. The two highly conserved loops of the AQP family are underlined. (B) Phylogenetic analysis of SjAQP and characterized homologs from Homo sapiens (HsAQP1), Bos taurus (BtAQP1), Plasmodium berghei (PbAQP), Plasmodium falciparum (PfAQP), Opisthorchis viverrini (OvAQP), Clonorchis sinensis (CsAQP), Toxoplasma gondii (TgAQP), and Trypanosome brucei (TbAQP). Unit, 0.1 amino acid substitutions per site.
Figure 2. Water-permeating activity of SjAQP.(A) SjAQP-expressing oocytes significantly facilitate water movement across cell membranes, and the permeation is significantly inhibited by 1.0 mM HgCl2. Black and white bars represent permeation coefficients of control or SjAQP-expressing oocytes, respectively. (B) Water permeation by SjAQP-expressing oocytes is significantly inhibited by 3.0 mM tetraethylammonium, 1.0 mM CuSO4, and 1.0 mM ZnCl2. The x-axis is the coefficient of osmotic water permeability, Pf, with the unit 10−4 cm/s. Data are represented as means ± SDs. *p ≤ 0.05, **p ≤ 0.01 by a Student’s t-test.
Figure 3. Solute-permeating activities of SjAQP.(A) SjAQP-expressing oocytes significantly facilitate glycerol movement across oocyte membranes compared with control oocytes (B) SjAQP-expressing oocytes significantly facilitate urea movement across cell membranes compared with control oocytes. The x-axis is the coefficient of solute permeability, Ps, with the unit 10−6 cm/s. Data are represented as means ± SDs. **p ≤ 0.01 by a Student’s t-test.
Figure 4. Expression profiles of SjAQP in different stages of the parasite life cycle.Reverse transcription-quantitative polymerase chain reaction revealed the expression of SjAQP in S. japonicum developmental-specific stages – eggs, miracidia, cercariae, and adults. cDNA levels were normalized using the NADH housekeeping gene as an internal control. neg_snail, naive snails as the negative control; i_snail, S. japonicum infected snails.
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