Generic placeholder image

Current Bioinformatics

Editor-in-Chief

ISSN (Print): 1574-8936
ISSN (Online): 2212-392X

Research Article

Transcriptome Analysis Reveals Possible Virulence Factors of Paragonimus proliferus

Author(s): Sheng-Hao Li, Shu-De Li, Kun-Li Wu, Jun-Yi Li, Hong-Juan Li, Wei-Qun Wang, Li-Jun Yang, Jing-Jing Xu, Guo-Ji Chang, Yan-Ling Zhang, Qiu-Hong Shu, Shan-Shan Zhuang, Zhi-Qiang Ma, Shu-Meiqi He, Min Zhu, Wen-Lin Wang* and Hong-Li Huang*

Volume 16, Issue 2, 2021

Published on: 28 July, 2020

Page: [197 - 206] Pages: 10

DOI: 10.2174/1574893615999200728203648

Price: $65

Abstract

Objective: To identify the possible virulence factors (VFs) of P. proliferus.

Methods: By Illumina HiSeq 4000 RNA-Seq platform, transcriptomes of adult P. proliferus worms were sequenced to predict VFs via screening the homologues of traditional VFs of parasites based on the annotations in the functional databases. Homology analysis was also performed to screen homologous genes between P. proliferus and other four Paragonimus species (i.e., P. kellicotti, P. skrjabini, P. miyazakii and P. westermani) whose transcriptomes were downloaded from the National Center for Biotechnology Information (NCBI) database, and then the differential-expressed homologous genes (DEHGs) were screened via comparisons of P. proliferus and P. kellicotti, P. skrjabini, P. miyazakii and P. westermani, respectively. Finally, an overlap of the predicted VFs and DEHGs was performed to identify possible key VFs that do not only belong to the predicted VFs but also DEHGs.

Results: A total of 1,509 genes of P. proliferus homologous to traditional VFs, including surface antigens (SAGs), secreted proteins (SPs), ATP-Binding Cassette (ABC) Transporters, actin-related proteins (ARPs), aminopeptidases (APases), glycoproteins (GPs), cysteine proteases (CPs), and heat shock proteins (HSPs), were identified. Meanwhile, homology analysis identified 6279 DEHGs among the five species, of which there were 48 DEHGs being mutually differentialexpressed among the four pairs of comparisons, such as MRP, Tuba 3, PI3K, WASF2, ADK, Nop56, DNAH1, PFK-2/FBPase2, Ppp1r7, SSP7. Furthermore, the overlap between the predicted VFs and DEHGs showed 97 genes of the predicted VFs that simultaneously belonged to DEHGs. Strikingly, of these 97 genes, only 26, including Chymotrypsin, Leucine APases, Cathepsin L, HSP 70, and so on, were higher expressed in P. proliferus while all the remaining were lower expressed than in the four other species.

Conclusion: This work provides a fundamental context for further studies of the pathogenicity of P. proliferus. Most of the predicted VFs which simultaneously belonged to DEHGs were lower expressed in P. proliferus.

Keywords: Paragonimus proliferus, transcriptome, virulence factor, pathogenicity, glycoproteins, genes.

Graphical Abstract
[1]
CHAI JY Paragonimiasis Handb Clin Neurol 2013; 114: 283-96.
[http://dx.doi.org/10.1016/B978-0-444-53490-3.00023-6] [PMID: 23829919]
[2]
Chung HL, Ho LY, Cheng LT, Tsao WC. The discovery in yunnan province of 2 new species of lung flukes--Paragonimus tuanshanensis sp. Nov. And Paragonimus menglaensis sp. Nov. I. Studies on morphology and life history with discussion on possible pathogenicity to man. Chin Med J 1964; 83: 641-59.
[PMID: 14228262]
[3]
Doanh PN, Hien HV, Nonaka N, Horii Y, Nawa Y. Genetically variant populations of Paragonimus proliferus Hsia & Chen, 1964 from central Vietnam. J Helminthol 2013; 87(2): 141-6.
[http://dx.doi.org/10.1017/S0022149X12000090] [PMID: 22354973]
[4]
Yang BB, Zhou BJ, Li RQ, Bai ZW, Wu OB, Gao XF. Preliminary investigation on Paragonimus in Lvchun county of Yunnan province. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2007; 25(6): 518-9.
[PMID: 18441907]
[5]
Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, Le NT. Discovery of Paragonimus proliferus in Northern Vietnam and their molecular phylogenetic status among genus Paragonimus. Parasitol Res 2008; 102(4): 677-83.
[http://dx.doi.org/10.1007/s00436-007-0811-5] [PMID: 18071749]
[6]
Peregrine AS, Nykamp SG, Carey H, Kruth S. Paragonimosis in a cat and the temporal progression of pulmonary radiographic lesions following treatment. J Am Anim Hosp Assoc 2014; 50(5): 356-60.
[http://dx.doi.org/10.5326/JAAHA-MS-6053] [PMID: 25028442]
[7]
Doanh PN, Hien HV, Tu LA, Nonaka N, Nawa YHY. Molecular identification of the trematode Paragonimus in faecal samples from the wild cat Prionailurus bengalensis in the Da Krong Nature Reserve, Vietnam. J Helminthol 2016; 90(6): 658-62.
[PMID: 26388560]
[8]
Madarame H, Suzuki H, Saitoh Y, et al. Ectopic (subcutaneous) Paragonimus miyazakii infection in a dog. Vet Pathol 2009; 46(5): 945-8.
[http://dx.doi.org/10.1354/vp.08-VP-0237-M-CR] [PMID: 19429999]
[9]
Irie T, Yamaguchi Y, Doanh PN, et al. Infection with Paragonimus westermani of boar-hunting dogs in Western Japan maintained via artificial feeding with wild boar meat by hunters. J Vet Med Sci 2017; 79(8): 1419-25.
[http://dx.doi.org/10.1292/jvms.17-0149] [PMID: 28717056]
[10]
Bouzid M, Hunter PR, Chalmers RM, Tyler KM. Cryptosporidium pathogenicity and virulence. Clin Microbiol Rev 2013; 26(1): 115-34.
[http://dx.doi.org/10.1128/CMR.00076-12] [PMID: 23297262]
[11]
Carmona-Antoñanzas G, Carmichael SN, Heumann J, et al. A Survey of the ATP-Binding Cassette (ABC) Gene Superfamily in the Salmon Louse (Lepeophtheirus salmonis). PLoS One 2015; 10(9), e0137394.
[http://dx.doi.org/10.1371/journal.pone.0137394] [PMID: 26418738]
[12]
Obwaller A, Duchêne M, Bruhn H, et al. Recombinant dissection of myosin heavy chain of Toxocara canis shows strong clustering of antigenic regions. Parasitol Res 2001; 87(5): 383-9.
[http://dx.doi.org/10.1007/s004360000352] [PMID: 11403381]
[13]
Verma SK, Arora A, Murthy PK. Recombinant Calponin of human filariid Brugia malayi: Secondary structure and immunoprophylactic potential. Vaccine 2017; 35(38): 5201-8.
[http://dx.doi.org/10.1016/j.vaccine.2017.07.105] [PMID: 28789852]
[14]
Kumar N. Somlata, Mazumder M, Dutta P, Maiti S, Gourinath S. EhCoactosin stabilizes actin filaments in the protist parasite Entamoeba histolytica. PLoS Pathog 2014; 10(9), e1004362.
[http://dx.doi.org/10.1371/journal.ppat.1004362] [PMID: 25210743]
[15]
Huang Y, Li W, Huang L, et al. Identification and characterization of myophilin-like protein: a life stage and tissue-specific antigen of Clonorchis sinensis. Parasitol Res 2012; 111(3): 1143-50.
[http://dx.doi.org/10.1007/s00436-012-2946-2] [PMID: 22752695]
[16]
Zheng J, Cheng Z, Jia H, Zheng Y. Characterization of aspartyl aminopeptidase from Toxoplasma gondii. Sci Rep 2016; 6: 34448.
[http://dx.doi.org/10.1038/srep34448] [PMID: 27678060]
[17]
Deu E, Leyva MJ, Albrow VE, Rice MJ, Ellman JA, Bogyo M. Functional studies of Plasmodium falciparum dipeptidyl aminopeptidase I using small molecule inhibitors and active site probes. Chem Biol 2010; 17(8): 808-19.
[http://dx.doi.org/10.1016/j.chembiol.2010.06.007] [PMID: 20797610]
[18]
Bartossek T, Jones NG, Schäfer C, et al. Structural basis for the shielding function of the dynamic trypanosome variant surface glycoprotein coat. Nat Microbiol 2017; 2(11): 1523-32.
[http://dx.doi.org/10.1038/s41564-017-0013-6] [PMID: 28894098]
[19]
Pinger J, Chowdhury S, Papavasiliou FN. Variant surface glycoprotein density defines an immune evasion threshold for African trypanosomes undergoing antigenic variation. Nat Commun 2017; 8(1): 828.
[http://dx.doi.org/10.1038/s41467-017-00959-w] [PMID: 29018220]
[20]
Yoonuan T, Nuamtanong S, Dekumyoy P, Phuphisut O, Adisakwattana P. Molecular and immunological characterization of cathepsin L-like cysteine protease of Paragonimus pseudoheterotremus. Parasitol Res 2016; 115(12): 4457-70.
[http://dx.doi.org/10.1007/s00436-016-5232-x] [PMID: 27562899]
[21]
Santos F, Nequiz M, Hernández-Cuevas NA, et al. Maintenance of intracellular hypoxia and adequate heat shock response are essential requirements for pathogenicity and virulence of Entamoeba histolytica. Cell Microbiol 2015; 17(7): 1037-51.
[http://dx.doi.org/10.1111/cmi.12419] [PMID: 25611463]
[22]
Yam XY, Niang M, Madnani KG, Preiser PR. Three is a crowd - new insights into rosetting in Plasmodium falciparum. Trends Parasitol 2017; 33(4): 309-20.
[http://dx.doi.org/10.1016/j.pt.2016.12.012] [PMID: 28109696]
[23]
Chung YB, Kita H, Shin MHA. A 27 kDa cysteine protease secreted by newly excysted Paragonimus westermani metacercariae induces superoxide anion production and degranulation of human eosinophils. Korean J Parasitol 2008; 46(2): 95-9.
[http://dx.doi.org/10.3347/kjp.2008.46.2.95] [PMID: 18552546]
[24]
Dubourg A, Xia D, Winpenny JP, et al. Giardia secretome highlights secreted tenascins as a key component of pathogenesis. Gigascience 2018; 7(3): 1-13.
[http://dx.doi.org/10.1093/gigascience/giy003] [PMID: 29385462]
[25]
Watanabe Costa R, da Silveira JF, Bahia D. Interactions between trypanosoma cruzi secreted proteins and host cell signaling pathways. Front Microbiol 2016; 7: 388.
[http://dx.doi.org/10.3389/fmicb.2016.00388] [PMID: 27065960]
[26]
Lund ME, O’Brien BA, Hutchinson AT, et al. Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse. PLoS One 2014; 9(1), e86289.
[http://dx.doi.org/10.1371/journal.pone.0086289] [PMID: 24466007]
[27]
Raj DK, Mu J, Jiang H, et al. Disruption of a Plasmodium falciparum multidrug resistance-associated protein (PfMRP) alters its fitness and transport of antimalarial drugs and glutathione. J Biol Chem 2009; 284(12): 7687-96.
[http://dx.doi.org/10.1074/jbc.M806944200] [PMID: 19117944]
[28]
Haeberlein S, Obieglo K, Ozir-Fazalalikhan A, et al. Schistosome egg antigens, including the glycoprotein IPSE/alpha-1, trigger the development of regulatory B cells. PLoS Pathog 2017; 13(7), e1006539.
[http://dx.doi.org/10.1371/journal.ppat.1006539] [PMID: 28753651]
[29]
Zhao S, Guan G, Liu J, et al. Screening and identification of host proteins interacting with Theileria annulata cysteine proteinase (TaCP) by yeast-two-hybrid system. Parasit Vectors 2017; 10(1): 536.
[http://dx.doi.org/10.1186/s13071-017-2421-0] [PMID: 29084576]
[30]
Cwiklinski K, Jewhurst H, McVeigh P, et al. Infection by the helminth parasite Fasciola hepatica requires rapid regulation of metabolic, virulence, and invasive factors to adjust to its mammalian host. Mol Cell Proteomics 2018; 17(4): 792-809.
[http://dx.doi.org/10.1074/mcp.RA117.000445] [PMID: 29321187]
[31]
Gould EN, Giannone R, Kania SA, Tolbert MK. Cysteine protease 30 (CP30) contributes to adhesion and cytopathogenicity in feline Tritrichomonas foetus. Vet Parasitol 2017; 244: 114-22.
[http://dx.doi.org/10.1016/j.vetpar.2017.07.034] [PMID: 28917301]
[32]
Morrissette N. Targeting Toxoplasma tubules: tubulin, microtubules, and associated proteins in a human pathogen. Eukaryot Cell 2015; 14(1): 2-12.
[http://dx.doi.org/10.1128/EC.00225-14] [PMID: 25380753]
[33]
Koushik AB, Welter BH, Rock ML, Temesvari LA. A genomewide overexpression screen identifies genes involved in the phosphatidylinositol 3-kinase pathway in the human protozoan parasite Entamoeba histolytica. Eukaryot Cell 2014; 13(3): 401-11.
[http://dx.doi.org/10.1128/EC.00329-13] [PMID: 24442890]
[34]
Igetei JE, Liddell S, El-Faham M, Doenhoff MJ. Purification of a chymotrypsin-like enzyme present on adult Schistosoma mansoni worms from infected mice and its characterization as a host carboxylesterase. Parasitology 2016; 143(5): 646-57.
[http://dx.doi.org/10.1017/S0031182016000184] [PMID: 26924446]
[35]
Balasubramanian N, Hao YJ, Toubarro D, Nascimento G, Simões N. Purification, biochemical and molecular analysis of a chymotrypsin protease with prophenoloxidase suppression activity from the entomopathogenic nematode Steinernema carpocapsae. Int J Parasitol 2009; 39(9): 975-84.
[http://dx.doi.org/10.1016/j.ijpara.2009.01.012] [PMID: 19249304]
[36]
Maggioli G, Rinaldi G, Giaudrone I, et al. Expression, purification and characterization of two leucine aminopeptidases of the blood fluke, Schistosoma mansoni. Mol Biochem Parasitol 2018; 219: 17-23.
[http://dx.doi.org/10.1016/j.molbiopara.2017.11.006] [PMID: 29169803]
[37]
Lee YR, Na BK, Moon EK, et al. Essential Role for an M17 leucine aminopeptidase in encystation of Acanthamoeba castellanii. PLoS One 2015; 10(6), e0129884.
[http://dx.doi.org/10.1371/journal.pone.0129884] [PMID: 26075721]
[38]
Kissoon-Singh V, Mortimer L, Chadee K. Entamoeba histolytica cathepsin-like enzymes: Interactions with the host gut. Adv Exp Med Biol 2011; 712: 62-83.
[http://dx.doi.org/10.1007/978-1-4419-8414-2_5] [PMID: 21660659]
[39]
Barenco PV, Lourenço EV, Cunha-Júnior JP, et al. Toxoplasma gondii 70 kDa heat shock protein: systemic detection is associated with the death of the parasites by the immune response and its increased expression in the brain is associated with parasite replication. PLoS One 2014; 9(5), e96527.
[http://dx.doi.org/10.1371/journal.pone.0096527] [PMID: 24801069]
[40]
Sun H, Zhuo X, Zhao X, et al. The heat shock protein 90 of Toxoplasma gondii is essential for invasion of host cells and tachyzoite growth. Parasite 2017; 24: 22.
[http://dx.doi.org/10.1051/parasite/2017023] [PMID: 28627357]
[41]
Singh M, Sharma S, Bhattacharya A, Tatu U. Heat shock protein 90 regulates encystation in Entamoeba. Front Microbiol 2015; 6: 1125.
[http://dx.doi.org/10.3389/fmicb.2015.01125] [PMID: 26528271]
[42]
Hosseini M, Haji-Fatahaliha M, Miahipour A, Yousefi M. New insights to structure and immunological features of Leishmania lipophosphoglycan3 . Biomed Pharmacother 2017; 95: 1369-74..
[http://dx.doi.org/10.1016/j.biopha.2017.09.061] [PMID: 28946184]
[43]
Perez-Morales D, Espinoza B. The role of small heat shock proteins in parasites. Cell Stress Chaperones 2015; 20(5): 767-80.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy