Contribution of helicobacter hepaticus cytolethal distending toxin subunits to human epithelial cell cycle arrest and apoptotic death in vitro

Helicobacter

Volumn 18, Issue 6, 2013, Pages 433-443

  Liyanage, Namal P M ^a,c   Dassanayake, Rohana P ^a,d   Kuszynski, Charles A ^b   Duhamel, Gerald E ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; CDT; Cell cycle arrest; Helicobacter hepaticus

Indexed keywords

BACTERIAL PROTEIN; CYTOLETHAL DISTENDING TOXIN; PROTEIN CDTA; PROTEIN CDTB; PROTEIN CDTC; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BACTERIAL STRAIN; CELL CYCLE ARREST; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC TRANSFECTION; GENOTOXICITY; HELA CELL; HELICOBACTER HEPATICUS; HUMAN; HUMAN CELL; IN VITRO STUDY; M PHASE CELL CYCLE CHECKPOINT; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SUBUNIT;

HELICOBACTER HEPATICUS; MUS;

APOPTOSIS; CDT; CELL CYCLE ARREST; HELICOBACTER HEPATICUS;

APOPTOSIS; BACTERIAL TOXINS; CELL CYCLE CHECKPOINTS; CELL LINE; EPITHELIAL CELLS; HELICOBACTER HEPATICUS; HELICOBACTER INFECTIONS; HUMANS; MOLECULAR SEQUENCE DATA;

EID: 84886283200     PISSN: 10834389     EISSN: 15235378     Source Type: Journal    
DOI: 10.1111/hel.12084     Document Type: Article

References (67)

1. 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;7:1851-75.
2. Guerra L, Cortes-Bratti X, Guidi R, Frisan T. The biology of the cytolethal distending toxins. Toxins (Basel) 2011;3:172-90.
3. Smith JL, Bayles DO. The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol 2006;32:227-48.
4. den Bakker HC, Moreno Switt AI, Govoni G, Cummings CA, Ranieri ML, Degoricija L, et al. Genome sequencing reveals diversification of virulence factor content and possible host adaptation in distinct subpopulations of Salmonella enterica. BMC Genomics 2011;12:425.
5. 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 USA 2004;101:4614-9.
6. Lara-Tejero M, Galan JE. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun 2001;69:4358-65.
7. Boesze-Battaglia K, Besack D, McKay T, Zekavat A, Otis L, Jordan-Sciutto K, Shenker BJ. Cholesterol-rich membrane microdomains mediate cell cycle arrest induced by Actinobacillus actinomycetemcomitans cytolethal-distending toxin. Cell Microbiol 2006;8:823-36.
8. Lara-Tejero M, Galan JE. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 2000;290:354-7.
9. Nesic D, Hsu Y, Stebbins CE. Assembly and function of a bacterial genotoxin. Nature 2004;429:429-33.
10. Yamada T, Komoto J, Saiki K, Konishi K, Takusagawa F. Variation of loop sequence alters stability of cytolethal distending toxin (CDT): crystal structure of CDT from Actinobacillus actinomycetemcomitans. Protein Sci 2006;15:362-72.
11. Hu X, Stebbins CE. Dynamics and assembly of the cytolethal distending toxin. Proteins 2006;65:843-55.
12. 2+-dependent neutral nuclease. FEMS Microbiol Lett 2005;251:219-25.
13. Elwell CA, Dreyfus LA. DNase I homologous residues in CdtB are critical for cytolethal distending toxin-mediated cell cycle arrest. Mol Microbiol 2000;37:952-63.
14. Mao X, DiRienzo JM. Functional studies of the recombinant subunits of a cytolethal distending holotoxin. Cell Microbiol 2002;4:245-55.
15. Li L, Sharipo A, Chaves-Olarte E, Masucci MG, Levitsky V, Thelestam M, Frisan T. The Haemophilus ducreyi cytolethal distending toxin activates sensors of DNA damage and repair complexes in proliferating and non-proliferating cells. Cell Microbiol 2002;4:87-99.
16. Gargi A, Reno M, Blanke SR. Bacterial toxin modulation of the eukaryotic cell cycle: are all cytolethal distending toxins created equally? Front Cell Infect Microbiol 2012;2:124.
17. Pellicano R, Menard A, Rizzetto M, Megraud F. Helicobacter species and liver diseases: association or causation? Lancet Infect Dis 2008;8:254-60.
18. Ward JM, Fox JG, Anver MR, et al. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J Natl Cancer Inst 1994;86:1222-7.
19. Fox JG, Dewhirst FE, Tully JG, Paster BJ, Yan L, Taylor NS, Collins MJ Jr, Gorelick PL, Ward JM. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol 1994;32:1238-45.
20. Solnick JV, Schauer DB. Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clin Microbiol Rev 2001;14:59-97.
21. Nagamine CM, Sohn JJ, Rickman BH, Rogers AB, Fox JG, Schauer DB. Helicobacter hepaticus infection promotes colon tumorigenesis in the BALB/c-Rag2(-/-) Apc(Min/+) mouse. Infect Immun 2008;76:2758-66.
22. Ge Z, Rogers AB, Feng Y, Lee A, Xu S, Taylor NS, Fox JG. Bacterial cytolethal distending toxin promotes the development of dysplasia in a model of microbially induced hepatocarcinogenesis. Cell Microbiol 2007;9:2070-80.
23. Pratt JS, Sachen KL, Wood HD, Eaton KA, Young VB. Modulation of host immune responses by the cytolethal distending toxin of Helicobacter hepaticus. Infect Immun 2006;74:4496-504.
24. Young VB, Knox KA, Pratt JS, Cortez JS, Mansfield LS, Rogers AB, Fox JG, Schauer DB. In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun 2004;72:2521-7.
25. Suerbaum S, Josenhans C, Sterzenbach T, et al. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci USA 2003;100:7901-6.
26. Nougayrede JP, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005;13:103-10.
27. Avenaud P, Castroviejo M, Claret S, Rosenbaum J, Megraud F, Menard A. Expression and activity of the cytolethal distending toxin of Helicobacter hepaticus. Biochem Biophys Res Commun 2004;318:739-45.
28. Liyanage NP, Manthey KC, Dassanayake RP, Kuszynski CA, Oakley GG, Duhamel GE. Helicobacter hepaticus cytolethal distending toxin causes cell death in intestinal epithelial cells via mitochondrial apoptotic pathway. Helicobacter 2010;15:98-107.
29. Nyska A, Maronpot RR, Eldridge SR, Haseman JK, Hailey JR. Alteration in cell kinetics in control B6C3F1 mice infected with Helicobacter hepaticus. Toxicol Pathol 1997;25:591-6.
30. Ihrig M, Schrenzel MD, Fox JG. Differential susceptibility to hepatic inflammation and proliferation in AXB recombinant inbred mice chronically infected with Helicobacter hepaticus. Am J Pathol 1999;155:571-82.
31. Hailey JR, Haseman JK, Bucher JR, Radovsky AE, Malarkey DE, Miller RT, Nyska A, Maronpot RR. Impact of Helicobacter hepaticus infection in B6C3F1 mice from twelve National Toxicology Program two-year carcinogenesis studies. Toxicol Pathol 1998;26:602-11.
32. Ge Z, Feng Y, Whary MT, Nambiar PR, Xu S, Ng V, Taylor NS, Fox JG. Cytolethal distending toxin is essential for Helicobacter hepaticus colonization in outbred Swiss Webster mice. Infect Immun 2005;73:3559-67.
33. Chien CC, Taylor NS, Ge Z, Schauer DB, Young VB, Fox JG. Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp. J Med Microbiol 2000;49:525-34.
34. Hansen R, Thomson JM, Fox JG, El-Omar EM, Hold GL. Could Helicobacter organisms cause inflammatory bowel disease? FEMS Immunol Med Microbiol 2011;61:1-14.
35. Dassanayake RP, Zhou Y, Hinkley S, Stryker CJ, Plauche G, Borda JT, Sestak K, Duhamel GE. Characterization of cytolethal distending toxin of Campylobacter species isolated from captive macaque monkeys. J Clin Microbiol 2005;43:641-9.
36. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005;73:1907-16.
37. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995;182:1545-56.
38. Young VB, Knox KA, Schauer DB. Cytolethal distending toxin sequence and activity in the enterohepatic pathogen Helicobacter hepaticus. Infect Immun 2000;68:184-91.
39. Guidi R, Guerra L, Levi L, Stenerlow B, Fox JG, Josenhans C, Masucci MG, Frisan T. Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell Microbiol 2013;15:98-113.
40. Shenker BJ, Hoffmaster RH, Zekavat A, Yamaguchi N, Lally ET, Demuth DR. Induction of apoptosis in human T cells by Actinobacillus actinomycetemcomitans cytolethal distending toxin is a consequence of G2 arrest of the cell cycle. J Immunol 2001;167:435-41.
41. Shenker BJ, Demuth DR, Zekavat A. Exposure of lymphocytes to high doses of Actinobacillus actinomycetemcomitans cytolethal distending toxin induces rapid onset of apoptosis-mediated DNA fragmentation. Infect Immun 2006;74:2080-92.
42. Bielaszewska M, Sinha B, Kuczius T, Karch H. Cytolethal distending toxin from Shiga toxin-producing Escherichia coli O157 causes irreversible G2/M arrest, inhibition of proliferation, and death of human endothelial cells. Infect Immun 2005;73:552-62.
43. Eshraghi A, Maldonado-Arocho FJ, Gargi A, Cardwell MM, Prouty MG, Blanke SR, Bradley KA. Cytolethal distending toxin family members are differentially affected by alterations in host glycans and membrane cholesterol. J Biol Chem 2010;285:18199-207.
44. Shenker BJ, Hoffmaster RH, McKay TL, Demuth DR. Expression of the cytolethal distending toxin (Cdt) operon in Actinobacillus actinomycetemcomitans: evidence that the CdtB protein is responsible for G2 arrest of the cell cycle in human T cells. J Immunol 2000;165:2612-8.
45. Lee RB, Hassane DC, Cottle DL, Pickett CL. Interactions of Campylobacter jejuni cytolethal distending toxin subunits CdtA and CdtC with HeLa cells. Infect Immun 2003;71:4883-90.
46. Elwell C, Chao K, Patel K, Dreyfus L. Escherichia coli CdtB mediates cytolethal distending toxin cell cycle arrest. Infect Immun 2001;69:3418-22.
47. Shounan Y, Feng X, O'Connell PJ. Apoptosis detection by annexin V binding: a novel method for the quantitation of cell-mediated cytotoxicity. J Immunol Methods 1998;217:61-70.
48. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995;184:39-51.
49. Cortes-Bratti X, Chaves-Olarte E, Lagergard T, Thelestam M. The cytolethal distending toxin from the chancroid bacterium Haemophilus ducreyi induces cell-cycle arrest in the G2 phase. J Clin Investig 1999;103:107-15.
50. Krishnan N, Doster AR, Duhamel GE, Becker DF. Characterization of a Helicobacter hepaticus putA mutant strain in host colonization and oxidative stress. Infect Immun 2008;76:3037-44.
51. Shenker BJ, Besack D, McKay T, Pankoski L, Zekavat A, Demuth DR. Actinobacillus actinomycetemcomitans cytolethal distending toxin (Cdt): evidence that the holotoxin is composed of three subunits: CdtA, CdtB, and CdtC. J Immunol 2004;172:410-7.
52. Shenker BJ, Besack D, McKay T, Pankoski L, Zekavat A, Demuth DR. Induction of cell cycle arrest in lymphocytes by Actinobacillus actinomycetemcomitans cytolethal distending toxin requires three subunits for maximum activity. J Immunol 2005;174:2228-34.
53. Frisk A, Lebens M, Johansson C, Ahmed H, Svensson L, Ahlman K, Lagergård T. The role of different protein components from the Haemophilus ducreyi cytolethal distending toxin in the generation of cell toxicity. Microb Pathog 2001;30:313-24.
54. Wising C, Svensson LA, Ahmed HJ, Sundaeus V, Ahlman K, Jonsson IM, Mölne L, Lagergård T. Toxicity and immunogenicity of purified Haemophilus ducreyi cytolethal distending toxin in a rabbit model. Microb Pathog 2002;33:49-62.
55. McSweeney LA, Dreyfus LA. Nuclear localization of the Escherichia coli cytolethal distending toxin CdtB subunit. Cell Microbiol 2004;6:447-58.
56. Akifusa S, Poole S, Lewthwaite J, Henderson B, Nair SP. Recombinant Actinobacillus actinomycetemcomitans cytolethal distending toxin proteins are required to interact to inhibit human cell cycle progression and to stimulate human leukocyte cytokine synthesis. Infect Immun 2001;69:5925-30.
57. Lewis DA, Stevens MK, Latimer JL, Ward CK, Deng K, Blick R, Lumbley SR, Ison CA, Hansen EJ. Characterization of Haemophilus ducreyi cdtA, cdtB, and cdtC mutants in in vitro and in vivo systems. Infect Immun 2001;69:5626-34.
58. Gelfanova V, Hansen EJ, Spinola SM. Cytolethal distending toxin of Haemophilus ducreyi induces apoptotic death of Jurkat T cells. Infect Immun 1999;67:6394-402.
59. Xu T, Lundqvist A, Ahmed HJ, Eriksson K, Yang Y, Lagergard T. Interactions of Haemophilus ducreyi and purified cytolethal distending toxin with human monocyte-derived dendritic cells, macrophages and CD4+ T cells. Microbes Infect 2004;6:1171-81.
60. Wising C, Azem J, Zetterberg M, Svensson LA, Ahlman K, Lagergard T. Induction of apoptosis/necrosis in various human cell lineages by Haemophilus ducreyi cytolethal distending toxin. Toxicon: Official Journal of the International Society on Toxinology 2005;45:767-76.
61. Yamamoto K, Tominaga K, Sukedai M, Okinaga T, Iwanaga K, Nishihara T, Fukuda J. Delivery of cytolethal distending toxin B induces cell cycle arrest and apoptosis in gingival squamous cell carcinoma in vitro. Eur J Oral Sci 2004;112:445-51.
62. Nalbant A, Chen C, Wang Y, Zadeh HH. Induction of T-cell apoptosis by Actinobacillus actinomycetemcomitans mutants with deletion of ltxA and cdtABC genes: possible activity of GroEL-like molecule. Oral Microbiol Immunol 2003;18:339-49.
63. Ohara M, Hayashi T, Kusunoki Y, Miyauchi M, Takata T, Sugai M. Caspase-2 and caspase-7 are involved in cytolethal distending toxin-induced apoptosis in Jurkat and MOLT-4 T-cell lines. Infect Immun 2004;72:871-9.
64. Ohara M, Hayashi T, Kusunoki Y, Nakachi K, Fujiwara T, Komatsuzawa H, Sugai M. Cytolethal distending toxin induces caspase-dependent and -independent cell death in MOLT-4 cells. Infect Immun 2008;76:4783-91.
65. Rabin SD, Flitton JG, Demuth DR. Aggregatibacter actinomycetemcomitans cytolethal distending toxin induces apoptosis in nonproliferating macrophages by a phosphatase-independent mechanism. Infect Immun 2009;77:3161-9.
66. Hickey TE, Majam G, Guerry P. Intracellular survival of Campylobacter jejuni in human monocytic cells and induction of apoptotic death by cytholethal distending toxin. Infect Immun 2005;73:5194-7.
67. Gargi A, Tamilselvam B, Powers B, Prouty MG, Lincecum T, Eshraghi A, Maldonado-Arocho FJ, Wilson BA, Bradley KA, Blanke SR. Cellular interactions of the cytolethal distending toxins from Escherichia coli and Haemophilus ducreyi. J Biol Chem 2013;288:7492-7505.