Parasites, Hosts and Diseases

"Young-An Bae"

Original Articles

Prostaglandin synthase activity of sigma- and mu-class glutathione transferases in a parasitic trematode, Clonorchis sinensis: Jiyoung Kim, Woon-Mok Sohn, Young-An Bae; Parasites Hosts Dis 2024;62(2):205-216.
Published online May 27, 2024; DOI: https://doi.org/10.3347/PHD.24004

Sigma-class glutathione transferase (GST) proteins with dual GST and prostaglandin synthase (PGS) activities play a crucial role in the establishment of Clonorchis sinensis infection. Herein, we analyzed the structural and enzymatic properties of sigma-class GST (CsGST-σ) proteins to obtain insight into their antioxidant and immunomodulatory functions in comparison with mu-class GST (CsGST-μ) proteins. CsGST-σ proteins conserved characteristic structures, which had been described in mammalian hematopoietic prostaglandin D₂ synthases. Recombinant forms of these CsGST-σ and CsGST-μ proteins expressed in Escherichia coli exhibited considerable degrees of GST and PGS activities with substantially different specific activities. All recombinant proteins displayed higher affinities toward prostaglandin H₂ (PGS substrate; average Km of 30.7 and 3.0 μm for prostaglandin D₂ [PGDS] and E₂ synthase [PGES], respectively) than those toward CDNB (GST substrate; average K_m of 1,205.1 μm). Furthermore, the catalytic efficiency (K_cat/K_m) of the PGDS/PGES activity was higher than that of GST activity (average K_cat/K_m of 3.1, 0.7, and 7.0×10^-3 s^-1μm^-1 for PGDS, PGES, and GST, respectively). Our data strongly suggest that the C. sinensis sigma- and mu-class GST proteins are deeply involved in regulating host immune responses by generating PGD₂ and PGE₂ in addition to their roles in general detoxification.

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Genome-wide identification of histone lysine methyltransferases and their implications in the epigenetic regulation of eggshell formation-related genes in a trematode parasite Clonorchis sinensis: Min-Ji Park, Woon-Mok Sohn, Young-An Bae; Parasites Hosts Dis 2024;62(1):98-116.
Published online February 23, 2024; DOI: https://doi.org/10.3347/PHD.23116

Epigenetic writers including DNA and histone lysine methyltransferases (DNMT and HKMT, respectively) play an initiative role in the differentiation and development of eukaryotic organisms through the spatiotemporal regulation of functional gene expressions. However, the epigenetic mechanisms have long been suspected in helminth parasites lacking the major DNA methyltransferases DNMT1 and DNMT3a/3b. Very little information on the evolutionary status of the epigenetic tools and their role in regulating chromosomal genes is currently available in the parasitic trematodes. We previously suggested the probable role of a DNMT2-like protein (CsDNMT2) as a genuine epigenetic writer in a trematode parasite Clonorchis sinensis. Here, we analyzed the phylogeny of HKMT subfamily members in the liver fluke and other platyhelminth species. The platyhelminth genomes examined conserved genes for the most of SET domain-containing HKMT and Disruptor of Telomeric Silencing 1 subfamilies, while some genes were expanded specifically in certain platyhelminth genomes. Related to the high gene dosages for HKMT activities covering differential but somewhat overlapping substrate specificities, variously methylated histones were recognized throughout the tissues/organs of C. sinensis adults. The temporal expressions of genes involved in eggshell formation were gradually decreased to their lowest levels proportionally to aging, whereas those of some epigenetic tool genes were re-boosted in the later adult stages of the parasite. Furthermore, these expression levels were significantly affected by treatment with DNMT and HKMT inhibitors. Our data strongly suggest that methylated histones are potent epigenetic markers that modulate the spatiotemporal expressions of C. sinensis genes, especially those involved in sexual reproduction.

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Isolation and Characterization of Vaccine Candidate Genes Including CSP and MSP1 in Plasmodium yoelii: Seon-Hee Kim, Young-An Bae, Ju-Young Seoh, Hyun-Jong Yang; Korean J Parasitol 2017;55(3):255-265.
Published online June 30, 2017; DOI: https://doi.org/10.3347/kjp.2017.55.3.255

Malaria is an infectious disease affecting humans, which is transmitted by the bite of Anopheles mosquitoes harboring sporozoites of parasitic protozoans belonging to the genus Plasmodium. Despite past achievements to control the protozoan disease, malaria still remains a significant health threat up to now. In this study, we cloned and characterized the full-unit Plasmodium yoelii genes encoding merozoite surface protein 1 (MSP1), circumsporozoite protein (CSP), and Duffy-binding protein (DBP), each of which can be applied for investigations to obtain potent protective vaccines in the rodent malaria model, due to their specific expression patterns during the parasite life cycle. Recombinant fragments corresponding to the middle and C-terminal regions of PyMSP1 and PyCSP, respectively, displayed strong reactivity against P. yoelii-infected mice sera. Specific native antigens invoking strong humoral immune response during the primary and secondary infections of P. yoelii were also abundantly detected in experimental ICR mice. The low or negligible parasitemia observed in the secondary infected mice was likely to result from the neutralizing action of the protective antibodies. Identification of these antigenic proteins might provide the necessary information and means to characterize additional vaccine candidate antigens, selected solely on their ability to produce the protective antibodies.

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Codon Usage Patterns of Tyrosinase Genes in Clonorchis sinensis: Young-An Bae; Korean J Parasitol 2017;55(2):175-183.
Published online April 30, 2017; DOI: https://doi.org/10.3347/kjp.2017.55.2.175

Abstract
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Codon usage bias (CUB) is a unique property of genomes and has contributed to the better understanding of the molecular features and the evolution processes of particular gene. In this study, genetic indices associated with CUB, including relative synonymous codon usage and effective numbers of codons, as well as the nucleotide composition, were investigated in the Clonorchis sinensis tyrosinase genes and their platyhelminth orthologs, which play an important role in the eggshell formation. The relative synonymous codon usage patterns substantially differed among tyrosinase genes examined. In a neutrality analysis, the correlation between GC₁₂ and GC₃ was statistically significant, and the regression line had a relatively gradual slope (0.218). NC-plot, i.e., GC₃ vs effective number of codons (ENC), showed that most of the tyrosinase genes were below the expected curve. The codon adaptation index (CAI) values of the platyhelminth tyrosinases had a narrow distribution between 0.685/0.714 and 0.797/0.837, and were negatively correlated with their ENC. Taken together, these results suggested that CUB in the tyrosinase genes seemed to be basically governed by selection pressures rather than mutational bias, although the latter factor provided an additional force in shaping CUB of the C. sinensis and Opisthorchis viverrini genes. It was also apparent that the equilibrium point between selection pressure and mutational bias is much more inclined to selection pressure in highly expressed C. sinensis genes, than in poorly expressed genes.

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Analysis of codon usage bias in mitochondrial CO gene among platyhelminthes
Gulshana A. Mazumder, Arif Uddin, Supriyo Chakraborty
Molecular and Biochemical Parasitology.2021; 245: 111410. CrossRef

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Experimental Murine Fascioliasis Derives Early Immune Suppression with Increased Levels of TGF-β and IL-4: Joon-Yong Chung, Young-An Bae, Doo-Hee Yun, Hyun-Jong Yang, Yoon Kong; Korean J Parasitol 2012;50(4):301-308.
Published online November 26, 2012; DOI: https://doi.org/10.3347/kjp.2012.50.4.301

Abstract
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In fascioliasis, T-helper 2 (Th2) responses predominate, while little is known regarding early immune phenomenon. We herein analyzed early immunophenotype changes of BALB/c, C57BL/6, and C3H/He mice experimentally infected with 5 Fasciola hepatica metacercariae. A remarkable expansion of CD19⁺ B cells was observed as early as week 1 post-infection while CD4⁺/CD8⁺ T cells were down-regulated. Accumulation of Mac1⁺ cells with time after infection correlated well with splenomegaly of all mice strains tested. The expression of tumor necrosis factor (TNF)-α mRNA in splenocytes significantly decreased while that of IL-4 up-regulated. IL-1β expression was down-modulated in BALB/c and C57BL/6 mice, but not in C3H/He. Serum levels of transforming growth factor (TGF)-β were considerably elevated in all mice during 3 weeks of infection period. These collective results suggest that experimental murine fascioliasis might derive immune suppression with elevated levels of TGF-β and IL-4 during the early stages of infection.

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Evaluation of Th1/Th2, regulatory cytokines and transcriptional factor FoxP3 in sheep immunized with a partially protective and non-protective vaccine and challenged with Fasciola hepatica
María Teresa Ruiz-Campillo, Isabel Lourdes Pacheco, Nieves Abril, María José Bautista, Álvaro Martínez-Moreno, Francisco Javier Martínez-Moreno, Leandro Buffoni, José Pérez, Verónica Molina-Hernández, Rafael Zafra
Veterinary Research.2024;[Epub] CrossRef
Fascioliasis: Image Findings, Diagnosis, and Treatment
Jae Seung Lee
Clinical Ultrasound.2024; 9(1): 18. CrossRef
Fasciolosis: pathogenesis, host-parasite interactions, and implication in vaccine development
Luis Miguel Flores-Velázquez, María Teresa Ruiz-Campillo, Guillem Herrera-Torres, Álvaro Martínez-Moreno, Francisco Javier Martínez-Moreno, Rafael Zafra, Leandro Buffoni, Pablo José Rufino-Moya, Verónica Molina-Hernández, José Pérez
Frontiers in Veterinary Science.2023;[Epub] CrossRef
The immunosuppression effects of deforolimus (ridaforolimus, AP23573) on allograft organ transplantation
Lumin Wang, Yanping Li, Dawei Yang, Jiazhao Fu, Bin Zhao, Yaguang Li, Yanrong Ye, Zhongquan Qi
Clinical and Translational Discovery.2023;[Epub] CrossRef
Immunization of Goats with Recombinant Protein 14-3-3 Isoform 2(rHcftt-2) Induced Moderate Protection against Haemonchus contortus Challenge
Yongqian Bu, Caiwen Jia, Xiaowei Tian, Kalibixiati Aimulajiang, Muhammad Ali Memon, Ruofeng Yan, Xiaokai Song, Lixin Xu, Xiangrui Li
Pathogens.2020; 9(1): 46. CrossRef
Characterization of dendritic cells and follicular dendritic cells in the hepatic lymph nodes and liver of sheep experimentally infected with Fasciola hepatica
María Teresa Ruiz-Campillo, Verónica Molina-Hernández, María José Bautista, Isabel L. Pacheco, Rafael Zafra, Leandro Buffoni, Francisco Javier Martínez-Moreno, Alvaro Martínez-Moreno, José Pérez
Veterinary Research.2020;[Epub] CrossRef
Helminth infection-induced carcinogenesis: spectrometric insights from the liver flukes, Opisthorchis and Fasciola
Maria João Gouveia, Maria Y. Pakharukova, Gabriel Rinaldi, Viatcheslav A. Mordvinov, Paul J. Brindley, Fátima Gärtner, Nuno Vale, Martin Michaelis
Experimental Results.2020;[Epub] CrossRef
Fasciola and fasciolosis in ruminants in Europe: Identifying research needs
N. J. Beesley, C. Caminade, J. Charlier, R. J. Flynn, J. E. Hodgkinson, A. Martinez-Moreno, M. Martinez-Valladares, J. Perez, L. Rinaldi, D. J. L. Williams
Transboundary and Emerging Diseases.2018; 65: 199. CrossRef
Fasciola hepatica induces Foxp3 T cell, proinflammatory and regulatory cytokine overexpression in liver from infected sheep during early stages of infection
Isabel L. Pacheco, Nieves Abril, Rafael Zafra, Verónica Molina-Hernández, Noelia Morales-Prieto, María J. Bautista, María T. Ruiz-Campillo, Raúl Pérez-Caballero, Alvaro Martínez-Moreno, José Pérez
Veterinary Research.2018;[Epub] CrossRef
Association of Fasciola hepatica Infection with Liver Fibrosis, Cirrhosis, and Cancer: A Systematic Review
Claudia Machicado, Jorge D. Machicado, Vicente Maco, Angelica Terashima, Luis A. Marcos, Hector H Garcia
PLOS Neglected Tropical Diseases.2016; 10(9): e0004962. CrossRef

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Aspartic proteases of Plasmodium vivax are highly conserved in wild isolates: Byoung-Kuk Na, Eung-Goo Lee, Hyeong-Woo Lee, Shin-Hyeong Cho, Young-An Bae, Yoon Kong, Jong-Koo Lee, Tong-Soo Kim; Korean J Parasitol 2004;42(2):61-66.
Published online June 20, 2004; DOI: https://doi.org/10.3347/kjp.2004.42.2.61

Abstract
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The plasmepsins are the aspartic proteases of malaria parasites. Treatment of aspartic protease inhibitor inhibits hemoglobin hydrolysis and blocks the parasite development in vitro suggesting that these proteases might be exploited their potentials as antimalarial drug targets. In this study, we determined the genetic variations of the aspartic proteases of Plasmodium vivax (PvPMs) of wild isolates. Two plasmepsins (PvPM4 and PvPM5) were cloned and sequenced from 20 P. vivax Korean isolates and two imported isolates. The sequences of the enzymes were highly conserved except a small number of amino acid substitutions did not modify key residues for the function or the structure of the enzymes. The high sequence conservations between the plasmepsins from the isolates support the notion that the enzymes could be reliable targets for new antimalarial chemotherapeutics.

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The Effect of Aqueous Extract of Cinnamon on the Metabolome ofPlasmodium falciparumUsing1HNMR Spectroscopy
Shirin Parvazi, Sedigheh Sadeghi, Mehri Azadi, Maryam Mohammadi, Mohammad Arjmand, Farideh Vahabi, Somye Sadeghzadeh, Zahra Zamani
Journal of Tropical Medicine.2016; 2016: 1. CrossRef
Use of multiplex real-time PCR for detection of common diarrhea causing protozoan parasites in Egypt
John T. Nazeer, Khalifa El Sayed Khalifa, Heidrun von Thien, Mahmoud Mohamed El-Sibaei, Magda Youssef Abdel-Hamid, Ranya Ayman Samir Tawfik, Egbert Tannich
Parasitology Research.2013; 112(2): 595. CrossRef
Imperfect Duplicate Insertions Type of Mutations in Plasmepsin V Modulates Binding Properties of PEXEL Motifs of Export Proteins in Indian Plasmodium vivax
Manmeet Rawat, Sonam Vijay, Yash Gupta, Pramod Kumar Tiwari, Arun Sharma, Rajvir Dahiya
PLoS ONE.2013; 8(3): e60077. CrossRef
Sequence homology and structural analysis of plasmepsin 4 isolated from Indian Plasmodium vivax isolates
Manmeet Rawat, Sonam Vijay, Yash Gupta, Rajnikant Dixit, P.K. Tiwari, Arun Sharma
Infection, Genetics and Evolution.2011; 11(5): 924. CrossRef
Single nucleotide polymorphisms, putatively neutral DNA markers and population genetic parameters in IndianPlasmodium vivaxisolates
BHAVNA GUPTA, ADITYA P. DASH, NALINI SHRIVASTAVA, APARUP DAS
Parasitology.2010; 137(12): 1721. CrossRef
Characterization of plasmepsin V, a membrane-bound aspartic protease homolog in the endoplasmic reticulum of Plasmodium falciparum
Michael Klemba, Daniel E. Goldberg
Molecular and Biochemical Parasitology.2005; 143(2): 183. CrossRef
Purification and Characterization of a Hemoglobin Degrading Aspartic Protease from the Malarial Parasite Plasmodium vivax
Arun Sharma, Alex Eapen, Sarala K. Subbarao
The Journal of Biochemistry.2005; 138(1): 71. CrossRef

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Divergent long-terminal-repeat retrotransposon families in the genome of Paragonimus westermani: Young-An Bae, Yoon Kong; Korean J Parasitol 2003;41(4):221-231.
Published online December 20, 2003; DOI: https://doi.org/10.3347/kjp.2003.41.4.221

Abstract
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To gain information on retrotransposons in the genome of Paragonimus westermani, PCR was carried out with degenerate primers, specific to protease and reverse transcriptase (rt) genes of long-terminal-repeat (LTR) retrotransposons. The PCR products were cloned and sequenced, after which 12 different retrotransposon-related sequences were isolated from the trematode genome. These showed various degrees of identity to the polyprotein of divergent retrotransposon families. A phylogenetic analysis demonstrated that these sequences could be classified into three different families of LTR retrotransposons, namely, Xena, Bel, and Gypsy families. Of these, two mRNA transcripts were detected by reverse transcriptase-PCR, showing that these two elements preserved their mobile activities. The genomic distributions of these two sequences were found to be highly repetitive. These results suggest that there are diverse retrotransposons including the ancient Xena family in the genome of P. westermani, which may have been involved in the evolution of the host genome.

Citations

Citations to this article as recorded by

Gene diversity and genetic variation in lung flukes (genusParagonimus)
David Blair, Yukifumi Nawa, Makedonka Mitreva, Pham Ngoc Doanh
Transactions of The Royal Society of Tropical Medicine and Hygiene.2016; 110(1): 6. CrossRef
Transfection of Platyhelminthes
Bárbara Moguel, Raúl J. Bobes, Julio C. Carrero, Juan P. Laclette
BioMed Research International.2015; 2015: 1. CrossRef
Transient transgenesis of the tapeworm Taenia crassiceps
Bárbara Moguel, Norma Moreno-Mendoza, Raúl J. Bobes, Julio C. Carrero, Jesús Chimal-Monroy, Martha E. Díaz-Hernández, Luis Herrera-Estrella, Juan P. Laclette
SpringerPlus.2015;[Epub] CrossRef
Review Article: ISTR, a Retrotransposons-Based Marker to Assess Plant Genome Variability with Special Emphasis in the Genera <i>Zea</i> and <i>Agave</i>
Martha Isabel Torres-Morán, Norma Almaraz-Abarca, Martha Escoto-Delgadillo
American Journal of Plant Sciences.2012; 03(12): 1820. CrossRef
PwRn1, a novel Ty3/gypsy-like retrotransposon of Paragonimus westermani: molecular characters and its differentially preserved mobile potential according to host chromosomal polyploidy
Young-An Bae, Jong-Sook Ahn, Seon-Hee Kim, Mun-Gan Rhyu, Yoon Kong, Seung-Yull Cho
BMC Genomics.2008;[Epub] CrossRef
Both sense and antisense strands of the LTR of the Schistosoma mansoni Pao-like retrotransposon Sinbad drive luciferase expression
Claudia S. Copeland, Victoria H. Mann, Paul J. Brindley
Molecular Genetics and Genomics.2007; 277(2): 161. CrossRef

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Evolutionary course of CsRn1 long-terminal-repeat retrotransposon and its heterogeneous integrations into the genome of the liver fluke, Clonorchis sinensis: Young-An Bae, Yoon Kong; Korean J Parasitol 2003;41(4):209-219.
Published online December 20, 2003; DOI: https://doi.org/10.3347/kjp.2003.41.4.209

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The evolutionary course of the CsRn1 long-terminal-repeat (LTR) retrotransposon was predicted by conducting a phylogenetic analysis with its paralog LTR sequences. Based on the clustering patterns in the phylogenetic tree, multiple CsRn1 copies could be grouped into four subsets, which were shown to have different integration times. Their differential sequence divergences and heterogeneous integration patterns strongly suggested that these subsets appeared sequentially in the genome of C. sinensis. Members of recently expanding subset showed the lowest level of divergence in their LTR and reverse transcriptase gene sequences. They were also shown to be highly polymorphic among individual genomes of the trematode. The CsRn1 element exhibited a preference for repetitive, agenic chromosomal regions in terms of selecting integration targets. Our results suggested that CsRn1 might induce a considerable degree of intergenomic variation and, thereby, have influenced the evolution of the C. sinensis genome.

Citations

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Recurrent emergence of structural variants of LTR retrotransposon CsRn1 evolving novel expression strategy and their selective expansion in a carcinogenic liver fluke, Clonorchis sinensis
Seon-Hee Kim, Yoon Kong, Young-An Bae
Molecular and Biochemical Parasitology.2017; 214: 14. CrossRef
Genomics and transcriptomics of the Chinese liver fluke Clonorchis sinensis (Opisthorchiidae, Trematoda)
G. N. Chelomina
Molecular Biology.2017; 51(2): 184. CrossRef
Egg-specific expression of protein with DNA methyltransferase activity in the biocarcinogenic liver fluke Clonorchis sinensis
SEON-HEE KIM, HYE-JEONG CHO, WOON-MOK SOHN, CHUN-SEOB AHN, YOON KONG, HYUN-JONG YANG, YOUNG-AN BAE
Parasitology.2015; 142(9): 1228. CrossRef
Progress on the transcriptomics of carcinogenic liver flukes of humans—Unique biological and biotechnological prospects
Neil D. Young, Aaron R. Jex, Cinzia Cantacessi, Bronwyn E. Campbell, Thewarach Laha, Woon-Mok Sohn, Banchob Sripa, Alex Loukas, Paul J. Brindley, Robin B. Gasser
Biotechnology Advances.2010; 28(6): 859. CrossRef
The biology and evolution of transposable elements in parasites
M. Carmen Thomas, Francisco Macias, Carlos Alonso, Manuel C. López
Trends in Parasitology.2010; 26(7): 350. CrossRef
Functional Genes and Proteins of Clonorchis sinensis
Tae Im Kim, Byoung-Kuk Na, Sung-Jong Hong
The Korean Journal of Parasitology.2009; 47(Suppl): S59. CrossRef
Molecular genetic profiles among individual Clonorchis sinensis adults collected from cats in two geographic regions of China revealed by RAPD and MGE-PCR methods
De-Hua Lai, Qiao-Ping Wang, Wen Chen, Lian-Shun Cai, Zhong-Dao Wu, Xing-Quan Zhu, Zhao-Rong Lun
Acta Tropica.2008; 107(2): 213. CrossRef
PwRn1, a novel Ty3/gypsy-like retrotransposon of Paragonimus westermani: molecular characters and its differentially preserved mobile potential according to host chromosomal polyploidy
Young-An Bae, Jong-Sook Ahn, Seon-Hee Kim, Mun-Gan Rhyu, Yoon Kong, Seung-Yull Cho
BMC Genomics.2008;[Epub] CrossRef