Skip to main content

Advertisement

Log in

Comparative studies on the proteomic expression patterns in the third- and fifth-stage larvae of Angiostrongylus cantonensis

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Angiostrongylus cantonensis is an important zoonotic parasite causing eosinophilic meningitis and eosinophilic meningoencephalitis in humans. In this study, the protein expression profiles of the infective third- and pathogenic fifth-stage larvae (L3 and L5) of this parasite were compared by proteomic techniques. Isolated protein samples were separated by two-dimensional gel electrophoresis (2-DE), stained with silver nitrate, and analyzed by matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry (MALDI-TOF MS). Proteins from L5 were mainly at pH 5–7 and with molecular weight (MW) 40–100 kDa, whereas those from L3 were at pH 5–6 and with 5–35 kDa. Of 100 protein spots identified, 33 were from L3 whereas 67 from L5 and 63 had known identities, whereas 37 were hypothetical proteins. There were 15 spots of stress proteins, and HSP60 was the most frequently found heat stress proteins in L5. More binding and protein transport-related proteins were found in L5 including peptidylprolyl isomerase (cyclophilin)-like 2, serum albumin, preproalbumin precursor, and dilute class unconventional myosin. L3 had a higher expression of cytoskeleton and membrane proteins than L5. In addition, four protein spots were identified in the sera of the rat host by Western blot analysis. The present proteomic study revealed different protein expression profiles in L3 and L5 of A. cantonensis. These changes may reflect the development of L3 from the poikilothermic snails to L5 in the homoeothemic rats. This information may be useful for the finding of stage-specific proteins and biomarker for diagnosis of angiostrongyliasis.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Alicata JE (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Adv Parasitol 3:223–248

    Article  PubMed  CAS  Google Scholar 

  • Alicata JE (1988) Angiostrongylus cantonensis (eosinophilic meningitis): historical events in its recognition as a new parasitic disease of man. J Wash Acad Sci 78:38–46

    Google Scholar 

  • Asahi H, Izumiyama S, Tolba ME, Kwansa-Bentum B (2011) Plasmodium falciparum: differing effects of non-esterified fatty acids and phospholipids on intraerythrocytic growth in serum-free medium. Exp Parasitol 127:708–713

    Article  PubMed  CAS  Google Scholar 

  • Banora MY, Rodiuc N, Baldacci-Cresp F, Smertenko A, Bleve-Zacheo T, Mellilo MT, Karimi M, Hilson P, Evrard JL, Favery B, Engler G, Abad P, de Almeida Engler J (2011) Feeding cells induced by phytoparasitic nematodes require γ-tubulin ring complex for microtubule reorganization. PLoS Pathog 7:e1002343

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, Nutman TB (2009) Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl Trop Dis 3:e410

    Article  PubMed  PubMed Central  Google Scholar 

  • Bente M, Harder S, Wiesgigl M, Heukeshoven J, Gelhaus C, Krause E, Clos J, Bruchhaus I (2003) Developmentally induced changes of the proteome in the protozoan parasite Leishmania donovani. Proteomics 3:1811–1829

    Article  PubMed  CAS  Google Scholar 

  • Chang SH, Tang P, Wang LC (2011) A transcriptomic study on the pepsin-activated infective larvae of Angiostrongylus cantonensis. Mol Biochem Parasitol 179:47–50

    Article  PubMed  CAS  Google Scholar 

  • Chang SH, Tang P, Yen CM, Chow KP, Wang LC (2014) A transcriptomic analysis on gene expressions in the infective third and pathogenic fifth larval stages of Angiostrongylus cantonensis. Parasitol Int 63:42–48

    Article  PubMed  CAS  Google Scholar 

  • Fang W, Xu S, Wang Y, Ni F, Zhang S, Liu J, Chen X, Luo D (2010) ES proteins analysis of Angiostrongylus cantonensis: products of the potential parasitism genes? Parasitol Res 106:1027–1032

    Article  PubMed  Google Scholar 

  • Huang HC, Yao LL, Song ZM, Li XP, Hua QQ, Li Q, Pan CW, Xia CM (2013) Development-specific differences in the proteomics of Angiostrongylus cantonensis. PLoS ONE 8:e76982

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang KY, Chien KY, Lin YC, Hsu WM, Fong IK, Huang PJ, Yueh YM, Gan RR, Tang P (2009) A proteome reference map of Trichomonas vaginalis. Parasitol Res 104:927–933

    Article  PubMed  Google Scholar 

  • Lal K, Bromley E, Oakes R, Prieto JH, Sanderson SJ, Kurian D, Hunt L, Yates JR 3rd, Wastling JM, Sinden RE, Tomley FM (2009) Proteomic comparison of four Eimeria tenella life-cycle stages: unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite. Proteomics 9:4566–4576

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Leon-Felix J, Ortega-Lopez J, Orozco-Solis R, Arroyo R (2004) Two novel asparaginyl endopeptidase-like cysteine proteinases from the protist Trichomonas vaginalis: their evolutionary relationship within the clan CD cysteine proteinases. Gene 335:25–35

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Lu J, Hu W, Wang SY, Cui SJ, Chi M, Yan Q, Wang XR, Song HD, Xu XN, Wang JJ, Zhang XL, Zhang X, Wang ZQ, Xue CL, Brindley PJ, McManus DP, Yang PY, Feng Z, Chen Z, Han ZG (2006) New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2:e29

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma GY, Zhang JZ, Yin GR, Zhang JH, Meng XL, Zhao F (2009) Toxoplasma gondii: proteomic analysis of antigenicity of soluble tachyzoite antigen. Exp Parasitol 122:41–46

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Valladares M, Donnan A, Geldhof P, Jackson F, Rojo-Vázquez FA, Skuce P (2012) Pyrosequencing analysis of the beta-tubulin gene in Spanish Teladorsagia circumcincta field isolates. Vet Parasitol 184:371–376

    Article  PubMed  Google Scholar 

  • O’Hagan R, Piasecki BP, Silva M, Phirke P, Nguyen KC, Hall DH, Swoboda P, Barr MM (2011) The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol 21:1685–1694

    Article  PubMed  Google Scholar 

  • Oura CA, McKellar S, Swan DG, Okan E, Shiels BR (2006) Infection of bovine cells by the protozoan parasite Theileria annulata modulates expression of the ISGylation system. Cell Microbiol 8:276–288

    Article  PubMed  CAS  Google Scholar 

  • Pemberton AD, Knight PA, Wright SH, Miller HR (2004) Proteomic analysis of mouse jejunal epithelium and its response to infection with the intestinal nematode, Trichinella spiralis. Proteomics 4:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Roy N, Nageshan RK, Pallavi R, Chakravarthy H, Chandran S, Kumar R, Gupta AK, Singh RK, Yadav SC, Tatu U (2010) Proteomics of Trypanosoma evansi infection in rodents. PLoS ONE 22:e9796

    Article  Google Scholar 

  • Shim YH, Paik YK (2010) Caenorhabditis elegans proteomics comes of age. Proteomics 10:846–857

    Article  PubMed  CAS  Google Scholar 

  • Song Z, Huang H, Tan F, Zhang E, Hu J, Pan C (2012) Differential proteomics analysis of female and male adults of Angiostrongylus cantonensis. Exp Parasitol 131:169–174

    Article  PubMed  CAS  Google Scholar 

  • Sotillo J, Valero ML, Sánchez Del Pino MM, Fried B, Esteban JG, Marcilla A, Toledo R (2010) Excretory/secretory proteome of the adult stage of Echinostoma caproni. Parasitol Res 107:691–697

    Article  PubMed  Google Scholar 

  • Tazir Y, Steisslinger V, Soblik H, Younis AE, Beckmann S, Grevelding CG, Steen H, Brattig NW, Erttmann KD (2009) Molecular and functional characterisation of the heat shock protein 10 of Strongyloides ratti. Mol Biochem Parasitol 168:149–157

    Article  PubMed  CAS  Google Scholar 

  • Walker J, Vasquez JJ, Gomez MA, Drummelsmith J, Burchmore R, Girard I, Ouellette M (2006) Identification of developmentally-regulated proteins in Leishmania panamensis by proteome profiling of promastigotes and axenic amastigotes. Mol Biochem Parasitol 147:64–73

    Article  PubMed  CAS  Google Scholar 

  • Wang LC, Chao D, Chen ER (1989) Acquired immunity in rats against Angiostrongylus cantonensis infection. Int J Parasitol 19:617–620

    Article  PubMed  CAS  Google Scholar 

  • Wang LC, Chao D, Chen ER (1991) Experimental infection routes of Angiostrongylus cantonensis in mice. J Helminthol 65:296–300

    Article  PubMed  CAS  Google Scholar 

  • Wang LC, Jung SM, Chen CC, Wong HF, Wan DP, Wan YL (2006) Pathological changes in the brains of rabbits experimentally infected with Angiostrongylus cantonensis after albendazole treatment: histopathological and magnetic resonance imaging studies. J Antimicrob Chemother 57:294–300

    Article  PubMed  CAS  Google Scholar 

  • Wang QP, Lai DH, Zhu XQ, Chen XG, Lun ZR (2008) Human Angiostrongyliasis. Lancet Infect Dis 8:621–630

    Article  PubMed  Google Scholar 

  • Wang QP, Wu ZD, Wei J, Owen RL, Lun ZR (2012) Human Angiostrongylus cantonensis: an update. Eur J Clin Microbiol Infect Dis 31:389–395

    Article  PubMed  Google Scholar 

  • Wu Y, Craig A (2006) Comparative proteomic analysis of metabolically labelled proteins from Plasmodium falciparum isolates with different adhesion properties. Malar J 5:67–80

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu SS, Ni F, Luo DM (2009) Expressed sequence tags (ESTs) analysis of Angiostrongylus cantonensis. Chin J Parasitol Parasitic Dis 27:248–250

    Google Scholar 

  • Zhou XW, Kafsack BF, Cole RN, Beckett P, Shen RF, Carruthers VB (2005) The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J Biol Chem 280:34233–34244

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grants from the National Science Council, Executive Yuan, ROC (NSC100-2320-B-182-013 and NSC101-2320-B-182-045) and Chang Gung Memorial Hospital Research Grant CMRPD1B0351. We thank Chang Gung Molecular Medicine Research Center for technical supports.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lian-Chen Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 131 kb)

ESM 2

(DOC 90 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, KY., Cheng, CJ., Yen, CM. et al. Comparative studies on the proteomic expression patterns in the third- and fifth-stage larvae of Angiostrongylus cantonensis . Parasitol Res 113, 3591–3600 (2014). https://doi.org/10.1007/s00436-014-4024-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4024-4

Keywords

Navigation