Biomphalysin, a New β Pore-forming Toxin Involved in Biomphalaria glabrata Immune Defense against Schistosoma mansoni

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Galinier, Richard ^a,b   Portela, Julien ^a,b   Moné, Yves ^a,b,c,d,e   Allienne, Jean François ^a,b   Henri, Hélène ^c,d,e   Delbecq, Stéphane ^f   Mitta, Guillaume ^a,b   Gourbal, Benjamin ^a,b   Duval, David ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE PERPIGNAN   (France)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITÉ LYON 1   (France)

^e LABORATOIRE DE BIOMÉTRIE ET BIOLOGIE EVOLUTIVE   (France)

^f UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMPHALYSIN; GENOMIC DNA; MESSENGER RNA; PORE FORMING CYTOTOXIC PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BIOMPHALARIA GLABRATA; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION; HEMOLYSIS; IMMUNITY; IMMUNOCYTOCHEMISTRY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMIASIS MANSONI; SPOROCYST; WESTERN BLOTTING;

ANIMALS; BIOMPHALARIA; CLONING, MOLECULAR; HELMINTHIASIS, ANIMAL; HOST-PARASITE INTERACTIONS; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN BINDING; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; VIRULENCE FACTORS;

BIOMPHALARIA GLABRATA; EUKARYOTA; GASTROPODA; SCHISTOSOMA MANSONI;

EID: 84875986475     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003216     Document Type: Article

References (86)

1. Doenhoff MJ, Kusel JR, Coles GC, Cioli D, (2002) Resistance of Schistosoma mansoni to praziquantel: is there a problem? Trans R Soc Trop Med Hyg 96: 465-469.
2. Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, et al. (2009) Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl Trop Dis 3: e504.
3. Adema CM, Hertel LA, Miller RD, Loker ES, (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci U S A 94: 8691-8696.
4. Loker ES, Adema CM, Zhang SM, Kepler TB, (2004) Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol Rev 198: 10-24.
5. Hanington PC, Forys MA, Dragoo JW, Zhang SM, Adema CM, et al. (2011) Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc Natl Acad Sci U S A 107: 21087-21092.
6. Baeza Garcia A, Pierce RJ, Gourbal B, Werkmeister E, Colinet D, et al. (2010) Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog 6 (9):: e1001115 doi:10.1371/journal.ppat.1001115.
7. Deleury E, Dubreuil G, Elangovan N, Wajnberg E, Reichhart JM, et al. (2012) Specific versus non-specific immune responses in an invertebrate species evidenced by a comparative de novo sequencing study. PLoS One 7: e32512.
8. Guillou F, Mitta G, Galinier R, Coustau C, (2007) Identification and expression of gene transcripts generated during an anti-parasitic response in Biomphalaria glabrata. Dev Comp Immunol 31: 657-671.
9. Ittiprasert W, Miller A, Myers J, Nene V, El-Sayed NM, et al. (2010) Identification of immediate response genes dominantly expressed in juvenile resistant and susceptible Biomphalaria glabrata snails upon exposure to Schistosoma mansoni. Mol Biochem Parasitol 169: 27-39.
10. Raghavan N, Miller AN, Gardner M, FitzGerald PC, Kerlavage AR, et al. (2003) Comparative gene analysis of Biomphalaria glabrata hemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Mol Biochem Parasitol 126: 181-191.
11. Lockyer AE, Spinks JN, Walker AJ, Kane RA, Noble LR, et al. (2007) Biomphalaria glabrata transcriptome: identification of cell-signalling, transcriptional control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Dev Comp Immunol 31: 763-782.
12. Nowak TS, Woodards AC, Jung Y, Adema CM, Loker ES, (2004) Identification of transcripts generated during the response of resistant Biomphalaria glabrata to Schistosoma mansoni infection using suppression subtractive hybridization. J Parasitol 90: 1034-1040.
13. Bouchut A, Coustau C, Gourbal B, Mitta G, (2007) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach. Parasitology 134: 575-588.
14. Bouchut A, Roger E, Coustau C, Gourbal B, Mitta G, (2006) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. Int J Parasitol 36: 175-184.
15. Bouchut A, Sautiere PE, Coustau C, Mitta G, (2006) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: Potential involvement of proteins from hemocytes revealed by a proteomic approach. Acta Tropica 98: 234-246.
16. Lockyer AE, Spinks J, Kane RA, Hoffmann KF, Fitzpatrick JM, et al. (2008) Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni. BMC Genomics 9: 634.
17. Vergote D, Bouchut A, Sautiere PE, Roger E, Galinier R, et al. (2005) Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol 35: 215-224.
18. Roger E, Gourbal B, Grunau C, Pierce RJ, Galinier R, et al. (2008) Expression analysis of highly polymorphic mucin proteins (Sm PoMuc) from the parasite Schistosoma mansoni. Mol Biochem Parasitol 157: 217-227.
19. Roger E, Grunau C, Pierce RJ, Hirai H, Gourbal B, et al. (2008) Controlled Chaos of Polymorphic Mucins in a Metazoan Parasite (Schistosoma mansoni) Interacting with Its Invertebrate Host (Biomphalaria glabrata). PLoS Negl Trop Dis 2: e330.
20. Roger E, Mitta G, Mone Y, Bouchut A, Rognon A, et al. (2008) Molecular determinants of compatibility polymorphism in the Biomphalaria glabrata/Schistosoma mansoni model: New candidates identified by a global comparative proteomics approach. Mol Biochem Parasitol 157: 205-216.
21. Mone Y, Gourbal B, Duval D, Du Pasquier L, Kieffer-Jaquinod S, et al. (2010) A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis 4.
22. Mitta G, Adema CM, Gourbal B, Loker ES, Theron A, (2012) Compatibility polymorphism in snail/schistosome interactions: From field to theory to molecular mechanisms. Developmental & Comparative Immunology 37: 1-8.
23. Hahn UK, Bender RC, Bayne CJ, (2000) Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Dev Comp Immunol 24: 531-541.
24. Hahn UK, Bender RC, Bayne CJ, (2001) Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87: 292-299.
25. Bender RC, Broderick EJ, Goodall CP, Bayne CJ, (2005) Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails. J Parasitol 91: 275-279.
26. Bender RC, Goodall CP, Blouin MS, Bayne CJ, (2007) Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/resistance to Schistosoma mansoni. Dev Comp Immunol 31: 874-878.
27. Goodall CP, Bender RC, Broderick EJ, Bayne CJ, (2004) Constitutive differences in Cu/Zn superoxide dismutase mRNA levels and activity in hemocytes of Biomphalaria glabrata (Mollusca) that are either susceptible or resistant to Schistosoma mansoni (Trematoda). Molecular and Biochemical Parasitology 137: 321-328.
28. Mone Y, Ribou AC, Cosseau C, Duval D, Theron A, et al. (2011) An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions. Int J Parasitol 41: 721-730.
29. Mitta G, Galinier R, Tisseyre P, Allienne JF, Girerd-Chambaz Y, et al. (2005) Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Developmental & Comparative Immunology 29: 393-407.
30. Moné Y, Gourbal B, Duval D, Du Pasquier L, Kieffer-Jaquinod S, et al. (2010) A Large Repertoire of Parasite Epitopes Matched by a Large Repertoire of Host Immune Receptors in an Invertebrate Host/Parasite Model. PLoS Negl Trop Dis 4: e813.
31. Bernheimer AW, Avigad LS (1974) Partial Characterization of Aerolysin, a Lytic Exotoxin from Aeromonas hydrophila. pp. 1016-1021.
32. Husslein V, Huhle B, Jarchau T, Lurz R, Goebel W, et al. (1988) Nucleotide sequence and transcriptional analysis of the aerCaerA region of Aeromonas sobria encoding aerolysin and its regulatory region. Molecular Microbiology 2: 507-517.
33. Ballard J, Crabtree J, Roe BA, Tweten RK, (1995) The primary structure of Clostridium septicum alpha-toxin exhibits similarity with that of Aeromonas hydrophila aerolysin. Infect Immun 63: 340-344.
34. Hunter SE, Clarke IN, Kelly DC, Titball RW (1992) Cloning and nucleotide sequencing of the Clostridium perfringens epsilon-toxin gene and its expression in Escherichia coli. pp. 102-110.
35. Priest FG, Ebdrup L, Zahner V, Carter PE, (1997) Distribution and characterization of mosquitocidal toxin genes in some strains of Bacillus sphaericus. Appl Environ Microbiol 63: 1195-1198.
36. Akiba T, Abe Y, Kitada S, Kusaka Y, Ito A, et al. (2009) Crystal Structure of the Parasporin-2 Bacillus thuringiensis Toxin That Recognizes Cancer Cells. Journal of Molecular Biology 386: 121-133.
37. Okumura S, Saitoh H, Ishikawa T, Mizuki E, Inouye K, et al. (2008) Identification and characterization of a novel cytotoxic protein, parasporin-4, produced by Bacillus thuringiensis A1470 strain. Biotechnology Annual Review: Elsevier. pp. 225-252.
38. Opota O, Vallet-Gély I, Vincentelli R, Kellenberger C, Iacovache I, et al. (2011) Monalysin, a novel ß-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality. PLoS Pathog 7: e1002259.
39. Macpherson H, Bergh Ø, Birkbeck TH, (2012) An aerolysin-like enterotoxin from Vibrio splendidus may be involved in intestinal tract damage and mortalities in turbot, Scophthalmus maximus (L.), and cod, Gadus morhua L., larvae. J Fish Dis 35: 153-167.
40. Szczesny P, Iacovache I, Muszewska A, Ginalski K, van der Goot FG, et al. (2011) Extending the Aerolysin Family: From Bacteria to Vertebrates. PLoS ONE 6: e20349.
41. Rossjohn J, Feil SC, McKinstry WJ, Tsernoglou D, Van Der Goot G, et al. (1998) Aerolysine: A Paradigm for Membrane Insertion of Beta-Sheet Protein Toxins? Journal of Structural Biology 121: 92-100.
42. Knapp O, Stiles B, Popoff MR, (2010) The Aerolysin Like Toxin Family of cytolitic, Pore Forming Toxins. The open toxinology Journal 3: 53-68.
43. Jonas D, Schultheis B, Klas C, Krammer PH, Bhakdi S (1993) Cytocidal effects of Escherichia coli hemolysin on human T lymphocytes. pp. 1715-1721.
44. Nelson K, Brodsky R, Buckley J, (1999) Channels formed by subnanomolar concentrations of the toxin aerolysin trigger apoptosis of T lymphomas. Cell Microbiol 1: 69-74.
45. Sher DJ, Fishman Y, Zhang M, Lebendiker M, Gaathon A, et al. (2005) Hydralysins: a new category of beta-pore-forming toxins in cnidaria. Characterization and preliminary structure-function analysis. J Biol Chem 280: 22847-22855.
46. Castro-Faria-Neto HC, Martins MA, Bozza PT, Perez SAC, Correa-Da-Silva ACV, et al. (1991) Pro-inflammatory activity of enterolobin: A haemolytic protein purified from seeds of the Brazilian tree Enterolobium contortisiliquum. Toxicon 29: 1143-1150.
47. Sousa MV, Richardson M, Fontes W, Morhy L, (1994) Homology between the seed cytolysin enterolobin and bacterial aerolysins. J Protein Chem 13: 659-667.
48. Iacovache I, van der Goot FG, Pernot L, (2008) Pore formation: An ancient yet complex form of attack. Biochimica et Biophysica Acta (BBA)- Biomembranes 1778: 1611-1623.
49. Abrami L, Fivaz M, Glauser PE, Parton RG, van der Goot FG, (1998) A pore-forming toxin interact with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J Cell Biol 140: 525-540.
50. Rossjohn J, Buckley JT, Hazes B, Murzin AG, Read RJ, et al. (1997) Aerolysin and pertussis toxin share a common receptor-binding domain. EMBO J 16: 3426-3434.
51. Diep DB, Nelson KL, Lawrence TS, Sellman BR, Tweten RK, et al. (1999) Expression and properties of an aerolysin-Clostridium septicum alpha toxin hybrid protein. Molecular Microbiology 31: 785-794.
52. Melton-Witt JA, Bentsen LM, Tweten RK, (2006) Identification of Functional Domains of Clostridium septicum Alpha Toxinâ€. Biochemistry 45: 14347-14354.
53. Wilmsen H, Leonard K, Ticheaar W, Buckley J, Pattus F, (1992) The aerolysin membrane channel is formed by heptamerization of the monomer. EMBO J 11: 2457-2463.
54. MacKenzie CR, Hirama T, Buckley JT, (1999) Analysis of receptor binding by the channel-forming toxin aerolysin using surface plasmon resonance. J Biol Chem 274: 22604-22609.
55. Iacovache I, Paumard P, Scheib H, Lesieur C, Sakai N, et al. (2006) A rivet model for channel formation by aerolysin-like pore-forming toxins. EMBO J 25: 457-466.
56. Howard SP, Buckley JT (1985) Activation of the hole-forming toxin aerolysin by extracellular processing. pp. 336-340.
57. Garland WJ, Buckley JT (1988) The cytolytic toxin aerolysin must aggregate to disrupt erythrocytes, and aggregation is stimulated by human glycophorin. pp. 1249-1253.
58. Song T, Toma C, Nakasone N, Iwanaga M, (2004) Aerolysin is activated by metalloprotease in Aeromonas veronii biovar sobria. J Med Microbiol 53 (6):: 477-482.
59. Bech N, Beltran S, Portela J, Rognon A, Allienne J-Fo, et al. Follow-up of the genetic diversity and snail infectivity of a Schistosoma mansoni strain from field to laboratory. Infection, Genetics and Evolution 10: 1039-1045.
60. Theron A, Pages JR, Rognon A, (1997) Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail as related to host susceptibility and sporocyst regulatory processes. Exp Parasitol 85: 1-9.
61. Yoshino T, Laursen J, (1995) Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic (Bge) cells. J Parasitol 81: 714-722.
62. Hansen E (1976) Application of tissue culture of a pulmonate snail to culture of larval of Schistosoma mansoni. New York: Academic Press: 87-97.
63. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: a laboratory manual. 2 ed. New York: Cold Spring Harbor Laboratory Press.
64. Galinier R, Roger E, Sautiere P, Aumelas A, Banaigs B, et al. (2009) Halocyntin and papillosin, two new antimicrobial peptides isolated from hemocytes of the solitary tunicate, Halocynthia papillosa. Journal of Peptide Science 15: 48-55.
65. Mattos AC, Kusel JR, Pimenta PF, Coelho PM, (2006) Activity of praziquantel on in vitro transformed Schistosoma mansoni sporocysts. Mem Inst Oswaldo Cruz 101 Suppl 1: 283-287.
66. Bagos PG, Liakopoulos TD, Spyropoulos IC, Hamodrakas SJ (2004) PRED-TMBB: a web server for predicting the topology of Î2-barrel outer membrane proteins. pp. W400-W404.
67. Bagos P, Liakopoulos T, Spyropoulos I, Hamodrakas S, (2004) A Hidden Markov Model method, capable of predicting and discriminating beta-barrel outer membrane proteins. BMC Bioinformatics (5): 29.
68. Zhang Y, Skolnick J (2005) TM-align: a protein structure alignment algorithm based on the TM-score. pp. 2302-2309.
69. Zhang Y, (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics (9): 40.
70. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols (5): 725-738.
71. Moran Y, Fredman D, Szczesny P, Grynberg M, Technau U, (2012) Recurrent Horizontal Transfer of Bacterial Toxin Genes to Eukaryotes. Mol Biol Evol.
72. Capella-Gutierrez S, Silla-Martinez J, TG T, (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
73. Abascal F, Zardoya R, Posada D, (2005) ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
74. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
75. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
76. Fivaz M, Abrami L, Tsitrin Y, Goot FVd, (2001) Aerolysin from Aeromonas hydrophila and related toxins. Curr Top Microbiol Immunol 257: 35-52.
77. Cole AR, Gibert M, Popoff M, Moss DS, Titball RW, et al. (2004) Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin. Nat Struct Mol Biol 11: 797-798.
78. Tsitrin Y, Morton CJ, El Bez C, Paumard P, Velluz M-C, et al. (2002) Conversion of a transmembrane to a water-soluble protein complex by a single point mutation. Nat Struct Mol Biol 9: 729-733.
79. Green M, Buckley J, (1990) Site-directed mutagenesis of the hole-forming toxin aerolysin: studies on the roles of histidines in receptor binding and oligomerization of the monomer. Biochemistry 29: 2177-2180.
80. Wilmsen HU, Buckley JT, Pattus F, (1991) Site-directed mutagenesis at histidines of aerolysin from Aeromonas hydrophila: a lipid planar bilayer study. Mol Microbiol 5: 2745-2751.
81. Buckley JT, Wilmsen HU, Lesieur C, Schultze A, Pattus F, et al. (1995) Protonation of His-132 promotes oligomerization of the channel-forming toxin Aerolysin. Biochemistry 34: 16450-16455.
82. van der Goot FGPF, Wong KR, Buckley JT, (1993) Oligomerization of the channel-forming toxin aerolysin precedes insertion into lipid bilayers. Biochemistry 32: 2636-2642.
83. Abrami L, Fivaz M, Decroly E, Seidah NG, Jean Fo, et al. (1998) The Pore-forming Toxin Proaerolysin Is Activated by Furin. 273: 32656-32661.
84. Katayama H, Janowiak BE, Brzozowski M, Juryck J, Falke S, et al. (2008) GroEL as a molecular scaffold for structural analysis of the anthrax toxin pore. Nat Struct Mol Biol 15: 754-760.
85. Kyte J, Doolittle RF, (1982) A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157: 105-132.
86. Tellmann G, Geulen O, (2006) LightCycler 480 Real-Time PCR system: Innovative solutions for relative quantification. Biochemica pp. 16-18.