Escherichia coli cytotoxic necrotizing factor 1 (CNF1): Toxin biology, in Vivo applications and therapeutic potential

Toxins

Volumn 2, Issue 2, 2010, Pages 283-296

  Fabbri, Alessia ^a   Travaglione, Sara ^a   Fiorentini, Carla ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

CNF1; Drug delivery agent; Escherichia coli; Memory; Pain; Vaccine adjuvant

Indexed keywords

ACTIN; CHOLERA TOXIN; CYTOTOXIC NECROTIZING FACTOR 1; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; PERTUSSIS TOXIN; PROTEIN KINASE B; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TETANUS TOXOID;

ADJUVANT THERAPY; ANALGESIC ACTIVITY; ANTIBODY RESPONSE; ARTICLE; CELL ACTIVITY; CELL CULTURE; CELL FUNCTION; COGNITION; DRUG BINDING; DRUG EFFECT; DRUG STRUCTURE; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ESCHERICHIA COLI; EUKARYOTIC CELL; HUMAN; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEARNING; MEMORY; NONHUMAN; PAIN; PROTEIN FUNCTION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TETANUS; ANIMAL; METABOLISM;

ANIMALIA; ESCHERICHIA COLI; EUKARYOTA;

ANIMALS; ESCHERICHIA COLI; EUKARYOTIC CELLS; RHO GTP-BINDING PROTEINS;

EID: 79952051173     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins2020282     Document Type: Article

References (67)

1. Fabbri, A.; Travaglione, S.; Falzano, L.; Fiorentini, C. Bacterial protein toxins: current and potential clinical use. Curr Med. Chem. 2008, 15, 1116-1125.
2. Hackett, R.; Kam, P.C. Botulinum toxin: pharmacology and clinical developments: a literature review. Med. Chem. 2007, 3, 333-345.
3. Boquet, P. The cytotoxic necrotizing factor 1 (CNF1) from Escherichia coli. Toxicon 2001, 39, 1673-1680.
4. Elliott, S.J.; Srinivas, S.; Albert, M.J.; Alam, K.; Robins-Browne, R.M.; Gunzburg, S.T.; Mee, B.J.; Chang, B.J. Characterization of the roles of hemolysin and other toxins in enteropathy caused by alpha-hemolytic Escherichia coli linked to human diarrhea. Infect. Immun. 1998, 66, 2040-2051.
5. Okeke, I.N.; Fayinka, S.T.; Lamikanra, A. Antibiotic resistance in Escherichia coli from Nigerian students, 1986-1998. Emerg. Infect. Dis. 2000, 6, 393-396.
6. Paciorek, J. Virulence properties of Escherichia coli faecal strains isolated in Poland from healthy children and strains belonging to serogroups O18, O26, O44, O86, O126 and O127 isolated from children with diarrhoea. J. Med. Microbiol., 2002, 51, 548-556.
7. De Rycke, J.; Milon, A.; Oswald, E. Necrotoxic Escherichia coli (NTEC): two emerging categories of human and animal pathogens. Vet. Res. 1999, 30, 221-233.
8. Landraud, L.; Gauthier, M.; Fosse, T.; Boquet, P. Frequency of Escherichia coli strains producing the cytotoxic necrotizing factor (CNF1) in nosocomial urinary tract infections. Lett. Appl. Microbiol. 2000, 30, 213-216.
9. Blanco, J.; Alonso, M.P.; González, E.A.; Blanco, M.; Garabal, J.I. Virulence factors of bacteraemic Escherichia coli with particular reference to production of cytotoxic necrotizing factor (CNF) by P-fimbriate strains. J. Med. Microbiol. 1990, 31, 175-183.
10. Houdouin, V.; Bonacorsi, S.; Brahimi, N.; Clermont, O.; Nassif, X.; Bingen, E. A uropathogenicity island contributes to the pathogenicity of Escherichia coli strains that cause neonatal meningitis. Infect. Immun. 2002, 70, 5865-5869.
11. Lemonnier, M.; Landraud, L.; Lemichez, E. Rho GTPase-activating bacterial toxins: from bacterial virulence regulation to eukaryotic cell biology. FEMS Microbiol. Rev. 2007, 31, 515-534.
12. Caprioli, A.; Falbo, V.; Roda, L.G.; Ruggeri, F.M.; Zona, C. Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect. Immun. 1983, 39, 1300-1306.
13. Caprioli, A.; Donelli, G.; Falbo, V.; Possenti, R.; Roda, L.G.; Roscetti, G.; Ruggeri, F.M. A cell division-active protein from E. coli. Biochem. Biophys. Res. Commun, 1984, 118, 587-593.
14. Buetow, L.; Flatau, G.; Chiu, K.; Boquet, P.; Ghosh P. Structure of the Rho-activating domain of Escherichia coli cytotoxic necrotizing factor 1. Nat. Struct. Biol. 2001, 8, 584-588.
15. Lemichez, E.; Flatau, G.; Bruzzone, M.; Boquet, P.; Gauthier M. Molecular localization of the Escherichia coli cytotoxic necrotizing factor CNF1 cell-binding and catalytic domains. Mol. Microbiol. 1997, 24, 1061-1070.
16. Pei, S.; Doye, A.; Boquet, P. Mutation of specific acidic residues of the CNF1 T domain into lysine alters cell membrane translocation of the toxin. Mol Microbiol. 2001, 41, 1237-1247.
17. Contamin, S.; Galmiche, A.; Doye, A.; Flatau, G.; Benmerah, A.; Boquet, P. The p21 Rhoactivating toxin cytotoxic necrotizing factor 1 is endocytosed by a clathrin-independent mechanism and enters the cytosol by an acidic-dependent membrane translocation step. Mol. Biol. Cell 2000, 11, 1775-1787.
18. Fabbri, A.; Gauthier, M.; Boquet, P. The 5' region of cnf1 harbours a translational regulatory mechanism for CNF1 synthesis and encodes the cell-binding domain of the toxin. Mol. Microbiol. 1999, 33, 108-118.
19. Chung, J.W.; Hong, S.J.; Kim, K.J.; Goti, D.; Stins, M.F.; Shin, S.; Dawson, V.L.; Dawson, T.M.; Kim, K.S. 37-kDa laminin receptor precursor modulates cytotoxic necrotizing factor 1-mediated RhoA activation and bacterial uptake. J. Biol. Chem. 2003, 278, 16857-16862.
20. Kim, K.J.; Chung, J.W.; Kim, K.S. 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J. Biol. Chem. 2005, 280, 1360-1368.
21. Blumenthal, B.; Hoffmann, C.; Aktories, K.; Backert, S.; Schmidt, G. The Cytotoxic Necrotizing Factors from Yersinia pseudotuberculosis and from Escherichia coli Bind to Different Cellular Receptors but Take the Same Route to the Cytosol. Infect. Immun. 2007, 75, 3344-3353.
22. McNichol, B. A.; Rasmussen, S. B.; Carvalho, H. M.; Meysick, K. C.; O'Brien, A. D. Two domains of cytotoxic necrotizing factor type 1 bind the cellular receptor, laminin receptor precursor protein. Infect. Immun. 2007, 75, 5095-5104.
23. Knust, Z.; Blumenthal, B.; Aktories, K.; Schmidt, G. Cleavage of Escherichia coli cytotoxic necrotizing factor 1 is required for full biologic activity. Infect. Immun. 2009, 77, 1835-1841.
24. Lemichez, E.; Flatau, G.; Bruzzone, M.; Boquet, P.; Gauthier, M. Molecular localization of the Escherichia coli cytotoxic necrotizing factor CNF1 cell-binding and catalytic domains. Mol. Microbiol. 1997, 24, 1061-1070.
25. Schmidt, G.; Selzer, J.; Lerm, M.; Aktories, K. The Rho-deamidating cytotoxic necrotizing factor 1 from Escherichia coli possesses transglutaminase activity. Cysteine 866 and histidine 881 are essential for enzyme activity. J. Biol. Chem. 1998, 273, 13669-13674.
26. DerMardirossian, C.; Bokoch, G.M. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell. Biol. 2005, 15, 356-363.
27. Burridge, K.; Wennerberg, K. Rho and Rac take center stage. Cell 2004, 116, 167-179.
28. Schmidt, A.; Hall, A. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 2002, 16, 1587-1609.
29. Moon, S.; Zheng, Y. Rho GTPase-activating proteins in cell regulation. Trends Cell. Biol. 2003, 13, 13-22.
30. Flatau, G.; Lemichez, E.; Gauthier, M.; Chardin, P.; Paris, S.; Fiorentini, C.; Boquet, P. Toxininduced activation of the G protein p21 Rho by deamidation of glutamine. J. Biol. Chem. 1997, 272, 19532-1953.
31. Schmidt, G.; Sher, P.; Wilm, M.; Selzer, J.; Mann, M.; Aktories, K. Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 1997, 387, 725-729.
32. Lerm, M.; Selzer, J.; Hoffmeyer, A.; Rapp, U.R.; Aktories, K.; Schmidt, G. Deamidation of Cdc42 and Rac by Escherichia coli cytotoxic necrotizing factor 1: activation of the C-Jun Nterminal kinase in HeLa cells. Infect. Immun. 1999, 67, 496-503.
33. Rittinger, K.; Walker, P.A.; Eccleston, J.F.; Nurmahomed, K.; Owen, D.; Laue, E.; Gamblin, S.J.; Smerdon, S.J. Crystal structure of a small G protein in complex with the GTPase-activating protein rhoGAP. Nature 1997, 388, 693-697.
34. Doye, A.; Mettouchi, A.; Bossis, G.; Clément, R.; Buisson-Touati, C.; Flatau, G.; Gagnoux, L.; Piechaczyk, M.; Boquet, P.; Lemichez, E. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 2002, 111, 553-564.
35. Fu, Y.; Galán, J.E. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999, 401, 293-297.
36. Schlumberger, M.C.; Hardt, W.D. Triggered phagocytosis by Salmonella: bacterial molecular mimicry of RhoGTPase activation/deactivation. Curr. Top. Microbiol. Immunol, 2005, 291, 29-42.
37. Jaffe, A.B.; Hall, A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21, 247-269.
38. Fiorentini, C.; Arancia, G.; Caprioli, A.; Falbo, V.; Ruggeri, F.M.; Donelli, G. Cytoskeletal changes induced in HEp-2 cells by the cytotoxic necrotizing factor of Escherichia coli. Toxicon 1988, 26, 1047-1056.
39. Fiorentini, C.; Fabbri, A.; Flatau, G.; Donelli, G.; Matarrese, P.; Lemichez, E.; Falzano, L.; Boquet, P. Escherichia coli cytotoxic necrotizing factor 1 (CNF1), a toxin that activates the Rho GTPase. J. Biol. Chem. 1997, 272, 19532-19537.
40. Falzano, L.; Fiorentini, C.; Donelli, G.; Michel, E.; Kocks, C.; Cossart, P.; Cabanié, L.; Oswald, E.; Boquet, P. Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type 1. Mol. Microbiol. 1993, 9, 1247-1254.
41. Fiorentini, C.; Falzano, L.; Fabbri, A.; Stringaro, A.; Logozzi, M.; Travaglione, S.; Contamin, S.; Arancia, G.; Malorni, W.; Fais, S. Activation of rho GTPases by cytotoxic necrotizing factor 1 induces macropinocytosis and scavenging activity in epithelial cells. Mol. Biol. Cell. 2001, 12, 2061-2273.
42. Hall, A. Rho GTPases and the actin cytoskeleton. Science 1998, 279, 509-514.
43. Lacerda, H.M.; Pullinger, G.D.; Lax, A.J.; Rozengurt, E. Cytotoxic necrotizing factor 1 from Escherichia coli and dermonecrotic toxin from Bordetella bronchiseptica induce p21(rho)-dependent tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 cells. J. Biol. Chem. 1997, 272, 9587-9596.
44. Boyer, L.; Travaglione, S.; Falzano, L.; Gauthier, N.C.; Popoff, M.R.; Lemichez, E.; Fiorentini, C.; Fabbri, A. Rac GTPase instructs Nuclear Factor-kB activating by conveying the SCF complex and IkB-alpha to the ruffling membranes. Mol. Biol. Cell. 2004, 15, 1124-1133.
45. Falzano, L.; Filippini, P.; Travaglione, S.; Miraglia, A.G.; Fabbri, A.; Fiorentini, C. Escherichia coli cytotoxic necrotizing factor 1 blocks cell cycle G2/M transition in uroepithelial cells. Infect. Immun. 2006, 74, 3765-3772.
46. Travaglione, S.; Messina, G.; Fabbri, A.; Falzano, L.; Giammarioli, A.M.; Grossi, M.; Rufini, S.; Fiorentini, C. Cytotoxic necrotizing factor 1 hinders skeletal muscle differentiation in vitro by perturbing the activation/deactivation balance of Rho GTPases. Cell Death Differ. 2005, 12, 78-86.
47. Falzano, L.; Quaranta, M.G.; Travaglione, S.; Filippini, P.; Fabbri, A.; Viora, M.; Donelli, G.; Fiorentini, C. Cytotoxic necrotizing factor 1 enhances reactive oxygen species-dependent transcription and secretion of proinflammatory cytokines in human uroepithelial cells. Infect Immun. 2003, 71, 4178-4181.
48. Fiorentini, C.; Matarrese, P.; Straface, E.; Falzano, L.; Donelli, G.; Boquet, P.; Malorni, W. Rhodependent cell spreading activated by E. coli cytotoxic necrotizing factor 1 hinders apoptosis in epithelial cells. Cell Death Differ. 1998, 5, 720-728.
49. Fiorentini, C.; Matarrese, P.; Straface, E.; Falzano, L.; Fabbri, A.; Donelli, G.; Cossarizza, A.; Boquet, P.; Malorni, W. Toxin-induced activation of Rho GTP-binding protein increases Bcl-2 expression and influences mitochondrial homeostasis. Exp. Cell. Res. 1998, 242, 341-350.
50. Giamboi Miraglia, A.; Travaglione, S.; Meschini, S.; Falzano, L.; Matarrese, P.; Quaranta, M.G.; Viora, M.; Fiorentini, C.; Fabbri, A. Cytotoxic necrotizing factor 1 prevents apoptosis via the Akt/IkappaB kinase pathway: role of nuclear factor-kappaB and Bcl-2. Mol. Biol. Cell 2007, 18, 2735-2744.
51. Munro, P.; Flatau, G.; Doye, A.; Boyer, L.; Oregioni, O.; Mege, J.L.; Landraud, L.; Lemichez, E. Activation and proteasomal degradation of rho GTPases by cytotoxic necrotizing factor-1 elicit a controlled inflammatory response. J. Biol. Chem. 2004, 279, 35849-35857.
52. Thomas, W.; Ascott, Z.K.; Harmey, D.; Slice, L.W.; Rozengurt, E.; Lax, A.J. Cytotoxic necrotizing factor from Escherichia coli induces RhoA-dependent expression of the cyclooxygenase-2 Gene. Infect. Immun. 2001, 69, 6839-6845.
53. Falzano, L.; Rivabene, R.; Santini, M.T.; Fabbri, A.; Fiorentini, C. An Escherichia coli cytotoxin increases superoxide anion generation via rac in epithelial cells. Biochem. Biophys. Res. Commun. 2001, 283, 1026-1030.
54. Zito, K.; Knott, G.; Shepherd, G.M.; Shenolikar, S.; Svoboda, K. Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 2004, 44, 321-334.
55. Fukazawa, Y.; Saitoh, Y.; Ozawa, F.; Ohta, Y.; Mizuno, K.; Inokuchi, K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 2003, 38, 447-446.
56. Diana, G.; Valentini, G.; Travaglione, S.; Falzano, L.; Pieri, M.; Zona, C.; Meschini, S.; Fabbri, A.; Fiorentini, C. Enhancement of learning and memory after activation of cerebral Rho GTPases. Proc. Natl. Acad. Sci. USA 2007, 104, 636-641.
57. Kamiya, N.; Asano, I.; Yoshino, J.; Sasaki, K.; Honma, Y.; Kawase, H.; Yokochi, T.; Shiraki, K.; Tsuji, T. Long-term persistence of cellular immunity to Oka vaccine virus induced by pernasal coadministration with Escherichia coli enterotoxin in mice. Vaccine 2001, 19, 3131-3136.
58. Vajdy, M.; Lycke, N. Presence of antigen-specific long-term memory cells in systemic lymphoid tissues as well as locally in the gut lamina propria following oral immunization with cholera toxin adjuvant. Adv. Exp. Med. Biol. 1995, 371B, 1495-1500.
59. Chiarella, P.; Massi, E.; De Robertis, M.; Signori, E.; Fazio, V.M. Adjuvants in vaccines and for immunisation: current trends. Expert. Opin. Biol. Ther. 2007, 7, 1551-1562.
60. Munro, P.; Flatau, G.; Anjuère, F.; Hofman, V.; Czerkinsky, C.; Lemichez, E. The Rho GTPase activators CNF1 and DNT bacterial toxins have mucosal adjuvant properties. Vaccine 2005, 23, 2551-2556.
61. Munro, P.; Flatau, G.; Lemichez, E. Intranasal immunization with tetanus toxoid and CNF1 as a new mucosal adjuvant protects BALB/c mice against lethal challenge. Vaccine 2007, 25, 8702-8706.
62. Bhave, G.; Gereau, R.W. Growing pains: the cytoskeleton as a critical regulator of pain plasticity. Neuron 2003, 39, 577-579.
63. Dina, O.A.; McCarter, G.C.; de Coupade, C.; Levine, J.D. Role of the sensory neuron cytoskeleton in second messenger signaling for inflammatory pain. Neuron 2003, 39, 613-624.
64. Goswami, C.; Dreger, M.; Otto, H.; Schwappach, B.; Hucho, F. Rapid disassembly of dynamic microtubules upon activation of the capsaicin receptor TRPV1. J. Neurochem. 2006, 96, 254-266.
65. Porro, C.A.; Cavazzuti, M. Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog. Neurobiol. 1993, 41, 565-607.
66. Pavone, F.; Luvisetto, S.; Marinelli, S.; Straface, E.; Fabbri, A.; Falzano, L.; Fiorentini, C.; Malorni, W. The Rac GTPase-activating bacterial protein toxin CNF1 induces analgesia upregulating mu-opioid receptors. Pain 2009, 145, 219-229.
67. Mason, P. Deconstructing endogenous pain modulations. J. Neurophysiol. 2005, 94, 1659-1663.