Log in

Dynamic transcriptome landscape of Paragonimus proliferus developmental stages in the rat lungs

  • Genetics, Evolution, and Phylogeny - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Paragonimus proliferus, a lung fluke of the genus Paragonimus, was first reported in Yunnan province, China. P. proliferus can infect Sprague-Dawley (SD) rats and cause lung damage, but there is still no direct evidence of human infection. Until now, there has been a lack of studies on P. proliferus parasitism and development in mammalian lung tissue. The aim of this study was to perform transcriptomic profiling of P. proliferus at different developmental stages. SD rats were infected with P. proliferus metacercariae obtained from crabs; worms isolated from the lungs at different time points as well as metacercariae were subjected to whole transcriptome sequencing. Overall, 34,403 transcripts with the total length of 33,223,828 bp, average length of 965 bp, and N50 of 1833 bp were assembled. Comparative analysis indicated that P. proliferus, similar to other Paragonimus spp., expressed genes related to catabolism, whereas P. proliferus-specific transcripts were related to the maintenance of cellular redox homeostasis, sensitivity to bacteria, and immune response. Transcriptional dynamics analysis revealed that genes involved in the regulation of catabolism and apoptosis had stable expression over the P. proliferus life cycle, whereas those involved in development and immune response showed time-dependent changes. High expression of genes associated with immune response corresponded to that of genes regulating the sensitivity to bacteria and immune protection. We constructed a P. proliferus developmental model, including the development of the body, suckers, blood cells, reproductive and tracheal systems, lymph, skin, cartilage, and other tissues and organs, and an immune response model, which mainly involved T cells and macrophages. Our study provides a foundation for further research into the molecular biology and infection mechanism of P. proliferus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

All data and materials mentioned in this article are available. Sequencing reads were submitted to the NCBI Sequence Read Archive (SRA) under accession numbers SRR13587223–SRR13587234.

References

  • Bairoch A, Apeilr R (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res 28:45–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blair D, Nawa Y, Mitreva M, Doanh PN (2016) Gene diversity and genetic variation in lung flukes (genus Paragonimus). Trans R Soc Trop Med Hyg 110:6–12

    Article  CAS  PubMed  Google Scholar 

  • Blair D, Xu ZB, Agatsuma T (1999) Paragonimiasis and the genus Paragonimus. Adv Parasitol 42:113–222

    Article  CAS  PubMed  Google Scholar 

  • Blair D (1993) Molecular variation in fasciolids and Paragonimus. Acta Trop 53:277–289

    Article  CAS  PubMed  Google Scholar 

  • Blair D (2014) Paragonimiasis. Adv Exp Med Biol 766:115–152

    Article  PubMed  Google Scholar 

  • Chung HL, Ho LY, Cheng LT, Tsao WC (1964) The discover in Yunnan Province of 2 new species of lung flukes. Chin Med J 83:641–659

    CAS  PubMed  Google Scholar 

  • Choi DW (1990) Paragonimus and paragonimiasis in Korea. Kisaengchunghak Chapchi 28:79–102

    PubMed  Google Scholar 

  • Doanh PN, Hien HV, Nonaka N, Horii Y, Nawa Y (2013) Genetically variant populations of Paragonimus proliferus Hsia & Chen, 1964 from central Vietnam. J Helminthol 87:141–146

    Article  CAS  PubMed  Google Scholar 

  • Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, Le NT (2008) Discovery of Paragonimus proliferus in Northern Vietnam and their molecular phylogenetic status among genus Paragonimus. Parasitol Res 102:677–683

    Article  PubMed  Google Scholar 

  • Doanh PN, Tu LA, Van Hien H, Van Duc N, Horii Y, Blair D, Nawa Y (2018) First intermediate hosts of Paragonimus spp. in Vietnam and identification of intramolluscan stages of different Paragonimus species. Parasit Vectors 11:328

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang L (2018) Expression and significance of MMP-9 and TIMP-1 in lung fibrosis of rats infected with paragonimusproliferus. China Med Phar 8:51–56

    Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    Article  CAS  PubMed  Google Scholar 

  • Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, Richter J, Rubin GM, Blake JA, Bult C, Dolan M, Drabkin H, Eppig JT, Hill DP, Ringwald M (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  CAS  PubMed  Google Scholar 

  • Keiser J, Utzinger J (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11:1507–1514

    Article  PubMed  PubMed Central  Google Scholar 

  • Koonin EV, Fedorova ND, Jackson JD, Aviva JR, Krylov DM, Makarova KS, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Rogozin IB, Smirnov S, Sorokin AV, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2004) A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 5(2):R7

    Article  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lateef A, Prabhudas SK, Natarajan P (2018) RNA sequencing and de novo assembly of Solanum trilobatum leaf transcriptome to identify putative transcripts for major metabolic pathways. Sci Rep 8:15375

    Article  PubMed  PubMed Central  Google Scholar 

  • Li B, McNulty WS, Rosa BA, Tyagi R, Zeng QR, Gu KZ, Weil GJ, Mitreva M (2016) Conservation and diversification of the transcriptomes of adult Paragonimus westermani and P. skrjabini. Parasit Vectors 9:497

    Article  PubMed  PubMed Central  Google Scholar 

  • Li SH, Li SD, Li HJ, Li JY, Xu JJ, Chang GJ, Yang LJ, Wang WQ, Zhang YL (2020) Differentially expressed homologous genes reveal interspecies differences of Paragonimus proliferus based on transcriptome analysis. Helminthologia 57:196–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin R, Xueming LL (2001) Experiment infection of rats with encysted metacercariae of Paragonimus heterotremus through hypodermic and muscle inoculation. Guangxi J Prev Med 7:201–203

    Google Scholar 

  • Liu Q, Wei F, Liu W (2008) Paragonimiasis: an important food-borne zoonosis in China. Trends Parasitol 24:318–323

    Article  PubMed  Google Scholar 

  • Liu Y, Bill R, Fiszman M, Rindflesch T, Pedersen T, Melton GB, Pakhomov SV (2012) Using SemRep to label semantic relations extracted from clinical text. AMIA Annu Symp Proc 2012:587–595

    PubMed  PubMed Central  Google Scholar 

  • Oey H, Zakrzewski M, Narain K, Devi KR, Agatsuma T, Nawaratna S, Gobert GN, Jones MK, Ragan MA, McManus DP, Krause L (2019) Whole-genome sequence of the oriental lung fluke Paragonimus westermani. Gigascience 8:giy146

    Article  Google Scholar 

  • Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  Google Scholar 

  • Moon Yong OH, Chu A, Park JH, Lee JY, Roh EY, Chai YJ, Hwang KT (2019) Simultaneous Paragonimus infection involving the breast and lung: a case report. World J Clin Cases 7:4292–4298

    Article  Google Scholar 

  • Pertea G, **aoqiu H, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19(5):651–652

    Article  CAS  PubMed  Google Scholar 

  • Prasad PK, Tandon V, Biswal DK, Goswami LM, Chatterjee A (2009) Phylogenetic reconstruction using secondary structures and sequence motifs of ITS2 rDNA of Paragonimus westermani (Kerbert, 1878) Braun, 1899 (Digenea: Paragonimidae) and related species. BMC Genomics 10(Suppl 3):S25

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosa BA, Choi YJ, McNulty SN, Jung H, Martin J, Agatsuma T, Sugiyama H, Le TH, Doanh PN, Maleewong W, Blair D, Brindley PJ, Fischer PU, Mitreva M (2020) Comparative genomics and transcriptomics of 4 Paragonimus species provide insights into lung fluke parasitism and pathogenesis. Gigascience 9:giaa073

    Article  PubMed  PubMed Central  Google Scholar 

  • Silachamroon U (2020) Paragonimiasis. In: Hunter’s Tropical Medicine and Emerging Infectious Diseases. Elsevier, Amsterdam, pp 928–931

    Chapter  Google Scholar 

  • Yang BB, Zhou BJ, Li RQ, Bai ZW, Wu OB, Gao XF (2007) Preliminary investigation on Paragonimus in Lvchun county of Yunnan province. Chin Magaz 25:518–519

    Google Scholar 

  • Yoonuan T, Nuamtanong S, Dekumyoy P, Phuphisut O, Adisakwattana P (2016) Molecular and immunological characterization of cathepsin L-like cysteine protease of Paragonimus pseudoheterotremus. Parasitol Res 115:4457–4470

    Article  PubMed  Google Scholar 

  • Zhou BJ, Yang BB, Doanh PN, Yang ZQ, **ang Z, Li CY, Shinohara A, Horii Y, Nawa Y (2008) Sequence analyses of ITS2 and CO1 genes of Paragonimus proliferus obtained in Yunnan province, China and their similarities with those of P. hokuoensis. Parasitol Res 102:1379–1383

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the researchers at our laboratories for their dedication and hard work.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Wen-Lin Wang or Ying-Rong Du.

Ethics declarations

Ethics approval

All studies adhered to procedures consistent with the National Research Council Guide for the Care and Use of Laboratory Animals and were approved by the Institutional Animal Care and Use Committee at Kunming Medical University (NO. KMMU2019047).

Additional information

Section Editor: **ng-Quan ZHU

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Table 1

GO enrichment of transcripts corresponding to all clusters. (XLS 45 kb)

Supplementary Table 2

The z-score expression matrix of significantly enriched GO terms. (XLS 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, SH., Yang, YR., Li, JY. et al. Dynamic transcriptome landscape of Paragonimus proliferus developmental stages in the rat lungs. Parasitol Res 120, 1627–1636 (2021). https://doi.org/10.1007/s00436-021-07111-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07111-0

Keywords

Navigation