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Immunodominant antigens in Naegleria fowleri excretory–secretory proteins were potential pathogenic factors

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Abstract

Naegleria fowleri, a ubiquitous pathogenic free-living amoeba, is the most virulent species and causes primary amoebic meningoencephalitis in laboratory animals and humans. The parasite secretes various inducing molecules as biological responses, which are thought to be involved in pathophysiological and immunological events during infection. To investigate what molecules of N. fowleri excretory–secretory proteins (ESPs) are related with amoebic pathogenicity, N. fowleri ESPs fractionated by two-dimensional electrophoresis were reacted with N. fowleri infection or immune sera. To identify immunodominant ESPs, six major protein spots were selected and analyzed by N-terminal sequencing. Finally, six proteins, 58, 40, 24, 21, 18, and 16 kDa of molecular weight, were partially cloned and matched with reference proteins as follow: 58 kDa of exendin-3 precursor, 40 kDa of secretory lipase, 24 kDa of cathepsin B-like proteases and cysteine protease, 21 kDa of cathepsin B, 18 kDa of peroxiredoxin, and 16 kDa of thrombin receptor, respectively. These results suggest that N. fowleri ESPs contained important proteins, which may play an important role in the pathogenicity of N. fowleri.

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References

  • Aragon V, Rossier O, Cianciotto NP (2002) Legionella pneumophila genes that encode lipase and phospholipase C activities. Microbiol 148:2223–2231

    CAS  Google Scholar 

  • Brindley PJ, Kalinna BH, Dalton JP, Day SR, Wong JY, Smythe ML, McManus DP (1997) Proteolytic degradation of host hemoglobin by schistosomes. Mol Biochem Parasitol 89:1–9

    Article  CAS  PubMed  Google Scholar 

  • Bush LE, John DT (1988) Intranasal immunization of mice against Naegleria fowleri. J Protozool 35:172–176

    CAS  PubMed  Google Scholar 

  • Caffrey CR, Ruppel A (1997) Affinity isolation and characterization of the cathepsin B-like proteinase Sj31 from Schistosoma japonicum. J Parasitol 21:327–329

    Google Scholar 

  • Christel CM, DeNardo DF (2006) Release of exendin-4 is controlled by mechanical action in Glia Monsters, Heloderma suspectum. Comp Biochem Physiol 143:85–88

    Google Scholar 

  • Chung YB, Kong Y, Yang HJ, Kang SY, Cho SY (1997) Cysteine protease activities during maturation stages of Paragonimus westermani. J Parasitol 83:902–907

    Article  CAS  PubMed  Google Scholar 

  • Cocks TM, Moffatt JD (2000) Protease-activated receptors: sentries for inflammation? Trends Pharmacol Sci 21:103–108

    Article  CAS  PubMed  Google Scholar 

  • Coughlin SR (1999) How the protease thrombin talks to cells. Proc Natl Acad Sci USA 96:11023–11027

    Article  CAS  PubMed  Google Scholar 

  • Culbertson CG (1970) Pathogenic Naegleria and Hartmannella (Acanthamoeba). Ann N Y Acad Sci 74:1018–1022

    Article  Google Scholar 

  • Darcy F, Deslee D, Santoro F, Charif H, Auriault C, Decoster A, Duquesne V, Capron A (1988) Induction of a protective antibody-dependent response against toxoplasmosis by in vitro excreted/secreted antigens from tachyzoites of Toxoplasma gondii. Parasite Immunol 10:553–567

    Article  CAS  PubMed  Google Scholar 

  • Donnelly S, O’Neill SM, Sekiya M, Mulcahy G, Dalton JP (2005) Thioredoxin peroxidase secretd by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 73:166–173

    Article  CAS  PubMed  Google Scholar 

  • Jeong SR, Kang SY, Lee SC, Song KJ, Im KI, Shin HJ (2004) Decreasing effect of an anti­Nfa1 polyclonal antibody on the in vitro cytotoxicity of pathogenic Naegleria fowleri. Korean J Parasitol 42:35–40

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Kim DS, Shin HJ (2008) Contact-independent cell death of human microglial cells due to pathogenic Naegleria fowleri trophozoites. Korean J Parasitol 46:217–221

    Article  CAS  PubMed  Google Scholar 

  • Klinkert MQ, Felleisen R, Link G, Ruppel A, Beck E (1989) Primary structure of Sm31/32 diagnostic proteins of Schistosoma mansoni and their identification as proteases. Mol Biochem Parasitol 33:113–122

    Article  CAS  PubMed  Google Scholar 

  • Kong Y, Chung YB, Cho SY, Kang SY (1994) Cleavage of immunoglobin G by excretory–secretory cathepsin S-like proteases of Spirometra mansoni plerocercoid. Parasitology 109:611–621

    Article  CAS  PubMed  Google Scholar 

  • Laemli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  Google Scholar 

  • Lee EG, Na BK, Bae YA, Je KSH, EY JuJW, Cho SH, Kim TS, Kang SY, Cho SY, Kong Y (2006) Identification of immunodominant excretory–secretory cysteine proteases of adult Paragonimus westermani by proteome analysis. Proteomics 6:1290–1300

    Article  CAS  PubMed  Google Scholar 

  • Lightowlers MW, Rickard MD (1988) Excretory–secretory products of helminth parasites: effects on host immune responses. Parasitology 96:S123–S166

    PubMed  Google Scholar 

  • Ma P, Visvesvara GS, Martinez AJ, Thedore FH, Daggett PM, Sawyer TK (1990) Naegleria and Acanthamoeba infection: review. Rev Infect Dis 12:490–513

    CAS  PubMed  Google Scholar 

  • Naglik J, Albrecht A, Bader O, Hube B (2004) Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 6:915–926

    Article  CAS  PubMed  Google Scholar 

  • Shepherd JC, Aitken A, McManus DP (1991) A protein secreted in vivo by Echinococcus granulosus inhibits elastase activity and neutrophil chemotaxis. Mol Biochem Parasitol 44:81–90

    Article  CAS  PubMed  Google Scholar 

  • Shin HJ, Cho MS, Jung SY, Kim HI, Park S, Kim HJ, Im KI (2001a) Molecular cloning and characterization of a gene encoding a 13.1 kDa antigenic protein of Naegleria fowleri. J Euk Microbiol 48:713–717

    Article  CAS  PubMed  Google Scholar 

  • Shin MH, Kita H, Park HY, Seoh JY (2001b) Cysteine protease secreted by Paragonimus westermani attenuates effector functions of human eosinophils stimulated with immunoglobulin G. Infect Immun 69:1599–1604

    Article  CAS  PubMed  Google Scholar 

  • Skuce PJ, Redmond DL, Liddell S, Stewart EM, Newlands GF, Smith WD, Knox DP (1999) Molecular cloning and characterization of gut-derived cysteine proteinases associated with a host protective extract from Haemonchus contortus. Parasitology 119:405–412

    Article  CAS  PubMed  Google Scholar 

  • Song KJ, Song KH, Kim JH, Sohn HJ, Lee YJ, Park CE, Shin HJ (2008) Heat shock protein 70 of Naegleria fowleri is important factor for proliferation and in vitro cytotoxicity. Parasitol Res 103:313–317

    Article  PubMed  Google Scholar 

  • Weinbauer GF, Aslam H, Krishnamurthy H, Brinkworth MH, Einspanier A, Hodges JK (2001) Quantitative analysis of spermatogenesis and apoptosis in the common marmoset (Callithrix jacchus) reveals high rates of spermatogonial turnover and high spermatogenic efficiency. Biol Reprod 64:120–126

    Article  CAS  PubMed  Google Scholar 

  • Willaert E (1971) Isolation and in vitro culture of the amoeba of the genus Naegleria. Ann Soc Belg Med Trop 51:701–708

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from National Institute of Health, Korea Centers for Disease Control and Prevention (2007), and partially supported by the Korean Research Foundation Grant funded by the Korea Government (MOEHRD, Basic Research Promotion Fund; R03-2004-000-10003-0).

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Correspondence to Kyoung-Ju Song or Ho-Joon Shin.

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Kyoung-Ju Song and Ho-Joon Shin equally contributed to this work.

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Kim, JH., Yang, AH., Sohn, HJ. et al. Immunodominant antigens in Naegleria fowleri excretory–secretory proteins were potential pathogenic factors. Parasitol Res 105, 1675–1681 (2009). https://doi.org/10.1007/s00436-009-1610-y

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  • DOI: https://doi.org/10.1007/s00436-009-1610-y

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