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Original Article

Functional characterization of Clonorchis sinensis choline transporter

Jeong Yeon Won1orcid, Johnsy Mary Louis2, Eui Sun Roh1, Seok Ho Cha1,*orcid, Jin-Hee Han2,*orcid
Parasites, Hosts and Diseases 2023;61(4):428-438.
Published online: November 28, 2023

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*Correspondence: (csh, shcha@inha.ac.kr; hjh, han.han@kangwon.ac.kr)
• Received: August 4, 2023   • Accepted: September 27, 2023

© 2023 The Korean Society for Parasitology and Tropical Medicine

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  • Functional characterization of glucose transporter 4 involved in glucose uptake in Clonorchis sinensis
    Hojong Jun, Ernest Mazigo, Wang-Jong Lee, Yun-Kyu Park, Jin-Hee Han, Seok Ho Cha
    Parasites, Hosts and Diseases.2024; 62(4): 450.     CrossRef

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Functional characterization of Clonorchis sinensis choline transporter
Parasites Hosts Dis. 2023;61(4):428-438.   Published online November 28, 2023
DOI: https://doi.org/10.3347/PHD.23082
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Functional characterization of Clonorchis sinensis choline transporter
Parasites Hosts Dis. 2023;61(4):428-438.   Published online November 28, 2023
DOI: https://doi.org/10.3347/PHD.23082
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Functional characterization of Clonorchis sinensis choline transporter
Image Image Image Image Image
Fig. 1 Schematic representation of the CsChT characteristics. (A) The predicted topology of the full-length CsChT (1–569 aa.) showed 13 transmembrane segments with the short N-terminus (1–3 aa.) facing the extracellular region and the large C-terminus (498–569 aa.) facing the intracellular region. The number of transmembrane domains and amino acid positions are shown in parenthesis with the residue number. (B) CsChT homology-based model on the human sodium/glucose cotransporter 2 (hSGLT2, PDB ID: 7vsi.1.A) structure. The homology base model was constructed from Tyr 3 (N-terminus, blue color) to Arg 502 (C-terminus, red color). The horizontal bars represent the expected lipid bilayer boundaries of the 13 transmembrane domains. (C) Phylogenetic tree of putative choline transporters in flukes (NCBI accession number shown in parenthesis) constructed using MEGA11 by ML method shows the distance of relationship.
Fig. 2 Uptake of various 3H- or 14C-labeled compounds by CsChT-expressing oocytes. The uptake rates of radiolabelled compounds were measured in water-injected oocytes (Control, white histogram) and CsChT-expressing oocytes (black histogram) for 1 h (mean±SE, n=8–10). The concentrations of substrates were as follows; [3H] choline, 10 μM; [3H] arginine, 100 nM; [14C] α-ketoglutarate, 5 μM; [14C] p-aminohippurate, 10 μM; [3H] taurocholate, 200 nM; [3H] estrone sulfate, 50 nM.
Fig. 3 The transport properties of choline via CsChT. (A) The uptake of 10 μM [3H] choline in the CsChT-expressing oocytes or water-injected (control) oocytes was measured at the indicated CsChT expression times. (B) The uptake of 10 μM [3H] choline in control oocytes (open circle) and CsChT-expressing oocytes (closed circle) was measured at 15 min intervals up to 75 min. All results were represented by mean±SE (n=6–8).
Fig. 4 The sodium dependent transport properties of CsChT. (A) Effect of extracellular cation on [3H] choline uptake in CsChT-expressing oocytes. The uptake rate of [3H] choline (10 μM) was measured in the presence or absence of extracellular Na+. Extracellular Na+ was replaced with equimolar concentration of NMDG (N-methyl-d-glucosamine) and lithium (LiCl). The results were represented by mean±SE (n=6–8). (B) CsChT tertiary structure shows a putative Na+ binding pocket. The five Na+ binding amino acid residues are shown by sphere shapes, including Ala 59, Val 62, Ala 338, Ser 341, and Ser 342.
Fig. 5 Trans-stimulatory effect and concentration dependence of CsChT-mediated uptake of [3H] choline. (A) The lack of a trans-stimulatory effect of choline on CsChT mediated efflux of choline was observed. Oocytes expressed with CsChT were incubated with 10 μM [3H] choline for 1 h and transferred to the ND96 solution (control) or ND96 containing 100 μM or 1,000 μM unlabelled choline. The efflux amount of choline during 1 h was shown as the percentage of the preloaded amount. (B) The uptake rates of choline by control (water-injected) or CsChT-expressing oocytes for 1 h were measured at variable concentrations (mean±SE, n=6–8). Inset, Lineweaver-Burk analysis of concentration dependent uptake of [3H] choline. V represents velocity; S represents the concentration of choline.

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Functional characterization of Clonorchis sinensis choline transporter

Amino acid identity percentages among the other related fluke proteins reported in the NCBI database

Cs Fg Fh Of Pw Sb Sh Sj Sm
Cs 71 72 97 76 70 69 72 63
Fg 95 71 71 69 68 70 63
Fh 72 71 69 68 70 63
Of 68 62 61 64 56
Pw 69 69 71 64
Sb 98 88 85
Sh 87 84
Sj 79

Cs, Clnorchis sinensis (GAA57421.1); Fg, Fasciola gigantica (TPP67279.1); Fh, Fasciola hepatica (THD26485.1); Of, Opisthorchis felineus (TGZ71349.1); Pw, Paragonimus westermani (KAF8572153.1); Sb, Schistosoma bovis (RTG 82711.1); Sh, Schistosoma haematobium (XP_035586184.1); Sj, Schistosoma japonicum (TNN15232.1); Sm, Schistosoma mansoni (XP_018652611.1).

Table 1 Amino acid identity percentages among the other related fluke proteins reported in the NCBI database

Cs, Clnorchis sinensis (GAA57421.1); Fg, Fasciola gigantica (TPP67279.1); Fh, Fasciola hepatica (THD26485.1); Of, Opisthorchis felineus (TGZ71349.1); Pw, Paragonimus westermani (KAF8572153.1); Sb, Schistosoma bovis (RTG 82711.1); Sh, Schistosoma haematobium (XP_035586184.1); Sj, Schistosoma japonicum (TNN15232.1); Sm, Schistosoma mansoni (XP_018652611.1).

Table 1

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