Jundishapur Journal of Microbiology

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Cytolethal Distending Toxin From Campylobacter jejuni Requires the Cytoskeleton for Toxic Activity

Estela T. Méndez-Olvera 1 , * , Jaime A. Bustos-Martínez 2 , Yolanda López-Vidal 3 , Antonio Verdugo-Rodríguez 4 and Daniel Martínez-Gómez 5
Authors Information
1 Departamento de Producción Agrícola y Animal, and Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana-Xochimilco, México City, México
2 Departamento de Atención a la Salud, Universidad Autónoma Metropolitana-Xochimilco, México City, México
3 Departamento de Microbiología y Parasitología-Facultad de Medicina, Universidad Nacional Autónoma de México, México City, México
4 Departamento de Microbiología e Inmunología-Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, México City, México
5 Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana-Xochimilco, México City, México
Article information
  • Jundishapur Journal of Microbiology: October 01, 2016, 9 (10); e35591
  • Published Online: September 18, 2016
  • Article Type: Research Article
  • Received: December 23, 2015
  • Revised: September 5, 2016
  • Accepted: September 5, 2016
  • DOI: 10.5812/jjm.35591

To Cite: Méndez-Olvera E T, Bustos-Martínez J A, López-Vidal Y, Verdugo-Rodríguez A, Martínez-Gómez D. Cytolethal Distending Toxin From Campylobacter jejuni Requires the Cytoskeleton for Toxic Activity, Jundishapur J Microbiol. 2016 ; 9(10):e35591. doi: 10.5812/jjm.35591.

Copyright © 2016, Ahvaz Jundishapur University of Medical Sciences. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Objectives
3. Methods
4. Results
5. Discussion
  • 1. Young KT, Davis LM, Dirita VJ. Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol. 2007; 5(9): 665-79[DOI][PubMed]
  • 2. Pickett CL, Pesci EC, Cottle DL, Russell G, Erdem AN, Zeytin H. Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infect Immun. 1996; 64(6): 2070-8[PubMed]
  • 3. Lara-Tejero M, Galan JE. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun. 2001; 69(7): 4358-65[DOI][PubMed]
  • 4. Sugai M, Kawamoto T, Peres SY, Ueno Y, Komatsuzawa H, Fujiwara T, et al. The cell cycle-specific growth-inhibitory factor produced by Actinobacillus actinomycetemcomitans is a cytolethal distending toxin. Infect Immun. 1998; 66(10): 5008-19[PubMed]
  • 5. Johnson WM, Lior H. A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microb Pathog. 1988; 4(2): 115-26[PubMed]
  • 6. Peres SY, Marches O, Daigle F, Nougayrede JP, Herault F, Tasca C, et al. A new cytolethal distending toxin (CDT) from Escherichia coli producing CNF2 blocks HeLa cell division in G2/M phase. Mol Microbiol. 1997; 24(5): 1095-107[PubMed]
  • 7. Cope LD, Lumbley S, Latimer JL, Klesney-Tait J, Stevens MK, Johnson LS, et al. A diffusible cytotoxin of Haemophilus ducreyi. Proc Natl Acad Sci U S A. 1997; 94(8): 4056-61[PubMed]
  • 8. Young VB, Knox KA, Schauer DB. Cytolethal distending toxin sequence and activity in the enterohepatic pathogen Helicobacter hepaticus. Infect Immun. 2000; 68(1): 184-91[PubMed]
  • 9. Okuda J, Kurazono H, Takeda Y. Distribution of the cytolethal distending toxin A gene (cdtA) among species of Shigella and Vibrio, and cloning and sequencing of the cdt gene from Shigella dysenteriae. Microb Pathog. 1995; 18(3): 167-72[PubMed]
  • 10. Haghjoo E, Galan JE. Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci U S A. 2004; 101(13): 4614-9[DOI][PubMed]
  • 11. Guerra L, Cortes-Bratti X, Guidi R, Frisan T. The biology of the cytolethal distending toxins. Toxins (Basel). 2011; 3(3): 172-90[DOI][PubMed]
  • 12. Lara-Tejero M, Galan JE. Cytolethal distending toxin: limited damage as a strategy to modulate cellular functions. Trends Microbiol. 2002; 10(3): 147-52[PubMed]
  • 13. Hu X, Nesic D, Stebbins CE. Comparative structure-function analysis of cytolethal distending toxins. Proteins. 2006; 62(2): 421-34[DOI][PubMed]
  • 14. Cortes-Bratti X, Chaves-Olarte E, Lagergard T, Thelestam M. Cellular internalization of cytolethal distending toxin from Haemophilus ducreyi. Infect Immun. 2000; 68(12): 6903-11[PubMed]
  • 15. Nesic D, Hsu Y, Stebbins CE. Assembly and function of a bacterial genotoxin. Nature. 2004; 429(6990): 429-33[DOI][PubMed]
  • 16. Lindmark B, Rompikuntal PK, Vaitkevicius K, Song T, Mizunoe Y, Uhlin BE, et al. Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol. 2009; 9: 220[DOI][PubMed]
  • 17. Jinadasa RN, Bloom SE, Weiss RS, Duhamel GE. Cytolethal distending toxin: a conserved bacterial genotoxin that blocks cell cycle progression, leading to apoptosis of a broad range of mammalian cell lineages. Microbiology. 2011; 157: 1851-75[DOI][PubMed]
  • 18. Eshraghi A, Maldonado-Arocho FJ, Gargi A, Cardwell MM, Prouty MG, Blanke SR, et al. Cytolethal distending toxin family members are differentially affected by alterations in host glycans and membrane cholesterol. J Biol Chem. 2010; 285(24): 18199-207[DOI][PubMed]
  • 19. Lin CD, Lai CK, Lin YH, Hsieh JT, Sing YT, Chang YC, et al. Cholesterol depletion reduces entry of Campylobacter jejuni cytolethal distending toxin and attenuates intoxication of host cells. Infect Immun. 2011; 79(9): 3563-75[DOI][PubMed]
  • 20. Guerra L, Teter K, Lilley BN, Stenerlow B, Holmes RK, Ploegh HL, et al. Cellular internalization of cytolethal distending toxin: a new end to a known pathway. Cell Microbiol. 2005; 7(7): 921-34[DOI][PubMed]
  • 21. Lord JM, Smith DC, Roberts LM. Toxin entry: how bacterial proteins get into mammalian cells. Cell Microbiol. 1999; 1(2): 85-91[PubMed]
  • 22. Sandvig K, van Deurs B. Transport of protein toxins into cells: pathways used by ricin, cholera toxin and Shiga toxin. FEBS Lett. 2002; 529(1): 49-53[PubMed]
  • 23. Bischofberger M, van der Goot FG. Exotoxin secretion: getting out to find the way in. Cell Host Microbe. 2008; 3(1): 7-8[DOI][PubMed]
  • 24. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem. 2009; 78: 857-902[DOI][PubMed]
  • 25. Granger E, McNee G, Allan V, Woodman P. The role of the cytoskeleton and molecular motors in endosomal dynamics. Semin Cell Dev Biol. 2014; 31: 20-9[DOI][PubMed]
  • 26. Day CA, Baetz NW, Copeland CA, Kraft LJ, Han B, Tiwari A, et al. Microtubule motors power plasma membrane tubulation in clathrin-independent endocytosis. Traffic. 2015; 16(6): 572-90[DOI][PubMed]
  • 27. Whitehouse CA, Balbo PB, Pesci EC, Cottle DL, Mirabito PM, Pickett CL. Campylobacter jejuni cytolethal distending toxin causes a G2-phase cell cycle block. Infect Immun. 1998; 66(5): 1934-40[PubMed]
  • 28. Brunelle JL, Green R. One-dimensional SDS-polyacrylamide gel electrophoresis (1D SDS-PAGE). Methods Enzymol. 2014; 541: 151-9[DOI][PubMed]
  • 29. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72: 248-54[PubMed]
  • 30. Meresse P, Dechaux E, Monneret C, Bertounesque E. Etoposide: discovery and medicinal chemistry. Curr Med Chem. 2004; 11(18): 2443-66[PubMed]
  • 31. Rello-Varona S, Gamez A, Moreno V, Stockert JC, Cristobal J, Pacheco M, et al. Metaphase arrest and cell death induced by etoposide on HeLa cells. Int J Biochem Cell Biol. 2006; 38(12): 2183-95[DOI][PubMed]
  • 32. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 1992; 119(3): 493-501[PubMed]
  • 33. Matassov D, Kagan T, Leblanc J, Sikorska M, Zakeri Z. Measurement of apoptosis by DNA fragmentation. Methods Mol Biol. 2004; 282: 1-17[DOI][PubMed]
  • 34. Vindelov LL, Christensen IJ, Jensen G, Nissen NI. Limits of detection of nuclear DNA abnormalities by flow cytometric DNA analysis. Results obtained by a set of methods for sample-storage, staining and internal standardization. Cytometry. 1983; 3(5): 332-9[DOI][PubMed]
  • 35. Pozarowski P, Darzynkiewicz Z. Analysis of cell cycle by flow cytometry. Methods Mol Biol. 2004; 281: 301-11[DOI][PubMed]
  • 36. Oswald E, Nougayrede JP, Taieb F, Sugai M. Bacterial toxins that modulate host cell-cycle progression. Curr Opin Microbiol. 2005; 8(1): 83-91[DOI][PubMed]
  • 37. Lara-Tejero M, Galan JE. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science. 2000; 290(5490): 354-7[PubMed]
  • 38. Alouf JE. Bacterial protein toxins. An overview. Methods Mol Biol. 2000; 145: 1-26[DOI][PubMed]
  • 39. Lock RB, Galperina OV, Feldhoff RC, Rhodes LJ. Concentration-dependent differences in the mechanisms by which caffeine potentiates etoposide cytotoxicity in HeLa cells. Cancer Res. 1994; 54(18): 4933-9[PubMed]
  • 40. De Rycke J, Oswald E. Cytolethal distending toxin (CDT): a bacterial weapon to control host cell proliferation? FEMS Microbiol Lett. 2001; 203(2): 141-8[PubMed]
  • 41. Shenker BJ, Walker LP, Zekavat A, Dlakic M, Boesze-Battaglia K. Blockade of the PI-3K signalling pathway by the Aggregatibacter actinomycetemcomitans cytolethal distending toxin induces macrophages to synthesize and secrete pro-inflammatory cytokines. Cell Microbiol. 2014; 16(9): 1391-404[DOI][PubMed]
  • 42. Bezine E, Vignard J, Mirey G. The cytolethal distending toxin effects on Mammalian cells: a DNA damage perspective. Cells. 2014; 3(2): 592-615[DOI][PubMed]
  • 43. Thelestam M, Frisan T. Cytolethal distending toxins. Rev Physiol Biochem Pharmacol. 2004; 152: 111-33[DOI][PubMed]
  • 44. Nakajima T, Hirayama J, Tazumi A, Hayashi K, Tasaki E, Asakura M, et al. Comparative analysis of Campylobacter lari cytolethal distending toxin (CDT) effect on HeLa cells. J Basic Microbiol. 2012; 52(5): 559-65[DOI][PubMed]
  • 45. Buder-Hoffmann S, Palmer C, Vacek P, Taatjes D, Mossman B. Different accumulation of activated extracellular signal-regulated kinases (ERK 1/2) and role in cell-cycle alterations by epidermal growth factor, hydrogen peroxide, or asbestos in pulmonary epithelial cells. Am J Respir Cell Mol Biol. 2001; 24(4): 405-13[DOI][PubMed]
  • 46. Quest AF, Leyton L, Parraga M. Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease. Biochem Cell Biol. 2004; 82(1): 129-44[DOI][PubMed]
  • 47. Smith JL, Bayles DO. The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol. 2006; 32(4): 227-48[DOI][PubMed]
  • 48. Ho YS, Duh JS, Jeng JH, Wang YJ, Liang YC, Lin CH, et al. Griseofulvin potentiates antitumorigenesis effects of nocodazole through induction of apoptosis and G2/M cell cycle arrest in human colorectal cancer cells. Int J Cancer. 2001; 91(3): 393-401[PubMed]
  • 49. Braet F, De Zanger R, Jans D, Spector I, Wisse E. Microfilament-disrupting agent latrunculin A induces and increased number of fenestrae in rat liver sinusoidal endothelial cells: comparison with cytochalasin B. Hepatology. 1996; 24(3): 627-35[DOI][PubMed]
  • 50. Eash S, Atwood WJ. Involvement of cytoskeletal components in BK virus infectious entry. J Virol. 2005; 79(18): 11734-41[DOI][PubMed]
  • 51. Saslowsky DE, te Welscher YM, Chinnapen DJ, Wagner JS, Wan J, Kern E, et al. Ganglioside GM1-mediated transcytosis of cholera toxin bypasses the retrograde pathway and depends on the structure of the ceramide domain. J Biol Chem. 2013; 288(36): 25804-9[DOI][PubMed]
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