Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens ε-toxin

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Ivie, Susan E ^a   Fennessey, Christine M ^a   Sheng, Jinsong ^a   Rubin, Donald H ^a,b   McClain, Mark S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM PERFRINGENS EPSILON TOXIN; CLOSTRIDIUM TOXIN; KIDNEY INJURY MOLECULE 1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; BACTERIAL TOXIN; CLOSTRIDIUM PERFRINGENS EPSILON-TOXIN; MEMBRANE PROTEIN; SMALL INTERFERING RNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; CYTOTOXICITY; DNA MICROARRAY; DOG; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE TRAP INSERTIONAL MUTAGENESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN FUNCTION; RNA INTERFERENCE; TOXIN ANALYSIS; ALTERNATIVE RNA SPLICING; ANIMAL; CELL DEATH; CELL LINE; CHEMISTRY; DRUG EFFECT; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; MAMMAL; METABOLISM; METHODOLOGY; SEQUENCE ALIGNMENT;

CLOSTRIDIUM PERFRINGENS; HEPATITIS A VIRUS; MAMMALIA;

ALTERNATIVE SPLICING; ANIMALS; BACTERIAL TOXINS; CELL DEATH; CELL LINE; DOGS; GENE KNOCKDOWN TECHNIQUES; GENES; HUMANS; MAMMALS; MEMBRANE PROTEINS; MUTAGENESIS, INSERTIONAL; PROTEIN BINDING; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT; TRANSFECTION;

EID: 79952589531     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017787     Document Type: Article

References (78)

1. Smith LDS, Williams BL, (1984) The Pathogenic Anaerobic Bacteria Springfield, Illinois Charles C. Thomas.
2. Goldstein J, Morris WE, Loidl CF, Tironi-Farinatti C, McClane BA, et al. (2009) Clostridium perfringens epsilon toxin increases the small intestinal permeability in mice and rats. PLoS One 4: e7065.
3. Adamson RH, Ly JC, Fernandez-Miyakawa M, Ochi S, Sakurai J, et al. (2005) Clostridium perfringens epsilon-toxin increases permeability of single perfused microvessels of rat mesentery. Infect Immun 73: 4879-4887.
4. Soler-Jover A, Dorca J, Popoff MR, Gibert M, Saura J, et al. (2007) Distribution of Clostridium perfringens epsilon toxin in the brains of acutely intoxicated mice and its effect upon glial cells. Toxicon 50: 530-540.
5. Ghabriel MN, Zhu C, Reilly PL, Blumbergs PC, Manavis J, et al. (2000) Toxin-induced vasogenic cerebral oedema in a rat model. Acta Neurochir Suppl 76: 231-236.
6. Worthington RW, Mulders MS, (1975) Effect of Clostridium perfringens epsilon toxin on the blood brain barrier of mice. Onderstepoort J Vet Res 42: 25-27.
7. Nagahama M, Sakurai J, (1991) Distribution of labeled Clostridium perfringens epsilon toxin in mice. Toxicon 29: 211-217.
8. Soler-Jover A, Blasi J, de Aranda IG, Navarro P, Gibert M, et al. (2004) Effect of Epsilon Toxin-GFP on MDCK Cells and Renal Tubules In Vivo. J Histochem Cytochem 52: 931-942.
9. Fernandez-Miyakawa ME, Sayeed S, Fisher DJ, Poon R, Adams V, et al. (2007) Development and application of a mouse oral challenge model for studying Clostridium perfringens type D infection. Infect Immun.
10. Uzal FA, Kelly WR, Morris WE, Assis RA, (2002) Effects of intravenous injection of Clostridium perfringens type D epsilon toxin in calves. J Comp Pathol 126: 71-75.
11. Uzal FA, Kelly WR, Morris WE, Bermudez J, Baison M, (2004) The pathology of peracute experimental Clostridium perfringens type D enterotoxemia in sheep. J Vet Diagn Invest 16: 403-411.
12. Nagahama M, Kobayashi K, Ochi S, Sakurai J, (1991) Enzyme-linked immunosorbent assay for rapid detection of toxins from Clostridium perfringens. FEMS Microbiol Lett 68: 41-44.
13. Sidorenko GI, (1967) Data on the distribution of Clostridium perfringens in the environment of man. Communication 1. J Hyg Epidemiol Microbiol Immunol 11: 171-177.
14. Gleeson-White MH, Bullen JJ, (1955) Clostridium welchii epsilon toxin in the intestinal contents of man. Lancet 268: 384-385.
15. Kohn J, Warrack GH, (1955) Recovery of Clostridium welchii type D from man. Lancet 268: 385.
16. Miller C, Florman S, Kim-Schluger L, Lento P, De La Garza J, et al. (2004) Fulminant and fatal gas gangrene of the stomach in a healthy live liver donor. Liver Transpl 10: 1315-1319.
17. Morinaga G, Nakamura T, Yoshizawa J, Nishida S, (1965) Isolation of Clostridium perfringens Type D from a Case of Gas Gangrene. J Bacteriol 90: 826.
18. Buxton D, (1976) Use of horseradish peroxidase to study the antagonism of Clostridium welchii (Cl. perfringens) type D epsilon toxin in mice by the formalinized epsilon prototoxin. J Comp Pathol 86: 67-72.
19. Nagahama M, Sakurai J, (1992) High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain. Infect Immun 60: 1237-1240.
20. Miyata S, Matsushita O, Minami J, Katayama S, Shimamoto S, et al. (2001) Cleavage of a C-terminal peptide is essential for heptamerization of Clostridium perfringens epsilon-toxin in the synaptosomal membrane. J Biol Chem 276: 13778-13783.
21. Nagahama M, Ochi S, Sakurai J, (1998) Assembly of Clostridium perfringens epsilon-toxin on MDCK cell membrane. J Nat Toxins 7: 291-302.
22. Petit L, Gibert M, Gillet D, Laurent-Winter C, Boquet P, et al. (1997) Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex. J Bacteriol 179: 6480-6487.
23. Petit L, Maier E, Gibert M, Popoff MR, Benz R, (2001) Clostridium perfringens epsilon toxin induces a rapid change of cell membrane permeability to ions and forms channels in artificial lipid bilayers. J Biol Chem 276: 15736-15740.
24. Lindsay CD, (1996) Assessment of aspects of the toxicity of Clostridium perfringens epsilon-toxin using the MDCK cell line. Hum Exp Toxicol 15: 904-908.
25. Chassin C, Bens M, de Barry J, Courjaret R, Bossu JL, et al. (2007) Pore-forming epsilon toxin causes membrane permeabilization and rapid ATP depletion-mediated cell death in renal collecting duct cells. Am J Physiol Renal Physiol 293: F9927-9937.
26. Gonzalez MR, Bischofberger M, Pernot L, van der Goot FG, Freche B, (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci 65: 493-507.
27. Bischof LJ, Kao CY, Los FC, Gonzalez MR, Shen Z, et al. (2008) Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS Pathog 4: e1000176.
28. Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG, (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126: 1135-1145.
29. Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, et al. (2004) Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A 101: 10995-11000.
30. Bellier A, Chen CS, Kao CY, Cinar HN, Aroian RV, (2009) Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans. PLoS Pathog 5: e1000689.
31. Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr, (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci U S A 103: 9897-9902.
32. Skals M, Jorgensen NR, Leipziger J, Praetorius HA, (2009) Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc Natl Acad Sci U S A 106: 4030-4035.
33. Soletti RC, Alves T, Vernal J, Terenzi H, Anderluh G, et al. Inhibition of MAPK/ERK, PKC and CaMKII signaling blocks cytolysin-induced human glioma cell death. Anticancer Res 30: 1209-1215.
34. Banks DJ, Bradley KA, (2007) SILENCE: a new forward genetic technology. Nat Methods 4: 51-53.
35. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I, et al. (2009) Haploid genetic screens in human cells identify host factors used by pathogens. Science 326: 1231-1235.
36. Osipovich AB, White-Grindley EK, Hicks GG, Roshon MJ, Shaffer C, et al. (2004) Activation of cryptic 3′ splice sites within introns of cellular genes following gene entrapment. Nucleic Acids Res 32: 2912-2924.
37. Payne DW, Williamson ED, Havard H, Modi N, Brown J, (1994) Evaluation of a new cytotoxicity assay for Clostridium perfringens type D epsilon toxin. FEMS Microbiol Lett 116: 161-167.
38. Shimamoto S, Tamai E, Matsushita O, Minami J, Okabe A, et al. (2005) Changes in Ganglioside Content Affect the Binding of Clostridium perfringens Epsilon-Toxin to Detergent-Resistant Membranes of Madin-Darby Canine Kidney Cells. Microbiol Immunol 49: 245-253.
39. Shortt SJ, Titball RW, Lindsay CD, (2000) An assessment of the in vitro toxicology of Clostridium perfringens type D epsilon-toxin in human and animal cells. Hum Exp Toxicol 19: 108-116.
40. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101: 6062-6067.
41. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
42. Kaplan G, Totsuka A, Thompson P, Akatsuka T, Moritsugu Y, et al. (1996) Identification of a surface glycoprotein on African green monkey kidney cells as a receptor for hepatitis A virus. Embo J 15: 4282-4296.
43. Feigelstock D, Thompson P, Mattoo P, Zhang Y, Kaplan GG, (1998) The human homolog of HAVcr-1 codes for a hepatitis A virus cellular receptor. J Virol 72: 6621-6628.
44. de Souza AJ, Oak JS, Jordanhazy R, DeKruyff RH, Fruman DA, et al. (2008) T cell Ig and mucin domain-1-mediated T cell activation requires recruitment and activation of phosphoinositide 3-kinase. J Immunol 180: 6518-6526.
45. de Souza AJ, Oriss TB, O'Malley KJ, Ray A, Kane LP, (2005) T cell Ig and mucin 1 (TIM-1) is expressed on in vivo-activated T cells and provides a costimulatory signal for T cell activation. Proc Natl Acad Sci U S A 102: 17113-17118.
46. Holm L, Sander C, (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138.
47. Santiago C, Ballesteros A, Tami C, Martinez-Munoz L, Kaplan GG, et al. (2007) Structures of T Cell immunoglobulin mucin receptors 1 and 2 reveal mechanisms for regulation of immune responses by the TIM receptor family. Immunity 26: 299-310.
48. Cao E, Zang X, Ramagopal UA, Mukhopadhaya A, Fedorov A, et al. (2007) T cell immunoglobulin mucin-3 crystal structure reveals a galectin-9-independent ligand-binding surface. Immunity 26: 311-321.
49. Ryu SE, Truneh A, Sweet RW, Hendrickson WA, (1994) Structures of an HIV and MHC binding fragment from human CD4 as refined in two crystal lattices. Structure 2: 59-74.
50. Seiradake E, Lortat-Jacob H, Billet O, Kremer EJ, Cusack S, (2006) Structural and mutational analysis of human Ad37 and canine adenovirus 2 fiber heads in complex with the D1 domain of coxsackie and adenovirus receptor. J Biol Chem 281: 33704-33716.
51. Nagahama M, Hara H, Fernandez-Miyakawa M, Itohayashi Y, Sakurai J, (2006) Oligomerization of Clostridium perfringens epsilon-Toxin Is Dependent upon Membrane Fluidity in Liposomes. Biochemistry 45: 296-302.
52. Beal DR, Titball RW, Lindsay CD, (2003) The development of tolerance to Clostridium perfringens type D epsilon-toxin in MDCK and G-402 cells. Hum Exp Toxicol 22: 593-605.
53. Kuehn EW, Hirt MN, John AK, Muehlenhardt P, Boehlke C, et al. (2007) Kidney injury molecule 1 (Kim1) is a novel ciliary molecule and interactor of polycystin 2. Biochem Biophys Res Commun 364: 861-866.
54. Kotsis F, Nitschke R, Boehlke C, Bashkurov M, Walz G, et al. (2007) Ciliary calcium signaling is modulated by kidney injury molecule-1 (Kim1). Pflugers Arch 453: 819-829.
55. Thompson P, Lu J, Kaplan GG, (1998) The Cys-rich region of hepatitis A virus cellular receptor 1 is required for binding of hepatitis A virus and protective monoclonal antibody 190/4. J Virol 72: 3751-3761.
56. Song C, Aiken C, (2007) Analysis of human cell heterokaryons demonstrates that target cell restriction of cyclosporine-resistant human immunodeficiency virus type 1 mutants is genetically dominant. J Virol 81: 11946-11956.
57. Nophar Y, Holtmann H, Ber R, Wallach D, (1988) Dominance of resistance to the cytocidal effect of tumor necrosis factor in heterokaryons formed by fusion of resistant and sensitive cells. J Immunol 140: 3456-3460.
58. Munk C, Brandt SM, Lucero G, Landau NR, (2002) A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc Natl Acad Sci U S A 99: 13843-13848.
59. Scobie HM, Rainey GJ, Bradley KA, Young JA, (2003) Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci U S A 100: 5170-5174.
60. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA, (2001) Identification of the cellular receptor for anthrax toxin. Nature 414: 225-229.
61. Abrami L, Kunz B, Deuquet J, Bafico A, Davidson G, et al. (2008) Functional interactions between anthrax toxin receptors and the WNT signalling protein LRP6. Cell Microbiol 10: 2509-2519.
62. Wei W, Lu Q, Chaudry GJ, Leppla SH, Cohen SN, (2006) The LDL receptor-related protein LRP6 mediates internalization and lethality of anthrax toxin. Cell 124: 1141-1154.
63. Graves PE, Siroux V, Guerra S, Klimecki WT, Martinez FD, (2005) Association of atopy and eczema with polymorphisms in T-cell immunoglobulin domain and mucin domain-IL-2-inducible T-cell kinase gene cluster in chromosome 5 q 33. J Allergy Clin Immunol 116: 650-656.
64. Nakajima T, Wooding S, Satta Y, Jinnai N, Goto S, et al. (2005) Evidence for natural selection in the HAVCR1 gene: high degree of amino-acid variability in the mucin domain of human HAVCR1 protein. Genes Immun 6: 398-406.
65. Genovese G, Friedman DJ, Ross MD, Lecordier L, Uzureau P, et al. Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329: 841-845.
66. Pier GB, Grout M, Zaidi T, Meluleni G, Mueschenborn SS, et al. (1998) Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393: 79-82.
67. Schroeder SA, Gaughan DM, Swift M, (1995) Protection against bronchial asthma by CFTR delta F508 mutation: a heterozygote advantage in cystic fibrosis. Nat Med 1: 703-705.
68. Pany S, Krishnasastry MV, (2007) Aromatic residues of Caveolin-1 binding motif of alpha-hemolysin are essential for membrane penetration. Biochem Biophys Res Commun 363: 197-202.
69. Vijayvargia R, Kaur S, Sangha N, Sahasrabuddhe AA, Surolia I, et al. (2004) Assembly of alpha-hemolysin on A431 cells leads to clustering of Caveolin-1. Biochem Biophys Res Commun 324: 1124-1129.
70. Pany S, Vijayvargia R, Krishnasastry MV, (2004) Caveolin-1 binding motif of alpha-hemolysin: its role in stability and pore formation. Biochem Biophys Res Commun 322: 29-36.
71. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
72. Miyata S, Minami J, Tamai E, Matsushita O, Shimamoto S, et al. (2002) Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes. J Biol Chem 277: 39463-39468.
73. Oyston PC, Payne DW, Havard HL, Williamson ED, Titball RW, (1998) Production of a non-toxic site-directed mutant of Clostridium perfringens epsilon-toxin which induces protective immunity in mice. Microbiology 144 (Pt 2): 333-341.
74. Pelish TM, McClain MS, (2009) Dominant-negative inhibitors of the clostridium perfringens {epsilon}-toxin. J Biol Chem.
75. Lewis M, Weaver CD, McClain MS, (2010) Identification of Small Molecule Inhibitors of Clostridium perfringens epsilon-Toxin Cytotoxicity Using a Cell-Based High-Throughput Screen. Toxins (Basel) 2: 1825-1847.
76. McClain MS, Cover TL, (2007) Functional Analysis of Neutralizing Antibodies against Clostridium perfringens Epsilon-Toxin. Infect Immun 75: 1785-1793.
77. Minami J, Katayama S, Matsushita O, Matsushita C, Okabe A, (1997) Lambda-toxin of Clostridium perfringens activates the precursor of epsilon-toxin by releasing its N- and C-terminal peptides. Microbiol Immunol 41: 527-535.
78. Hauer PJ, Clough NE, (1999) Development of monoclonal antibodies suitable for use in antigen quantification potency tests for clostridial veterinary vaccines. Dev Biol Stand 101: 85-94.