Cytolethal Distending Toxins Require Components of the ER-Associated Degradation Pathway for Host Cell Entry

PLoS Pathogens

Volumn 10, Issue 7, 2014, Pages

  Eshraghi, Aria ^a   Dixon, Shandee D ^a   Tamilselvam, Batcha ^b   Kim, Emily Jin Kyung ^a   Gargi, Amandeep ^b   Kulik, Julia C ^a   Damoiseaux, Robert ^a   Blanke, Steven R ^b   Bradley, Kenneth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL TOXIN; CYTOLETHAL DISTENDING TOXIN; DERL2 PROTEIN, HUMAN; IMMUNOSUPPRESSIVE AGENT; MEMBRANE PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; P97 ATPASE; SYVN1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ANIMAL; CELL MEMBRANE; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; GENE EXPRESSION REGULATION; GENETICS; GOLGI COMPLEX; GROWTH, DEVELOPMENT AND AGING; HAEMOPHILUS DUCREYI; HAMSTER; HELA CELL LINE; HUMAN; IMMUNOPRECIPITATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULCUS MOLLE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BACTERIAL TOXINS; BLOTTING, WESTERN; CELL MEMBRANE; CHANCROID; CHO CELLS; CRICETINAE; CRICETULUS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE EXPRESSION REGULATION; GOLGI APPARATUS; HAEMOPHILUS DUCREYI; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; IMMUNOSUPPRESSIVE AGENTS; MEMBRANE PROTEINS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UBIQUITIN-PROTEIN LIGASES;

EID: 84905375032     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004295     Document Type: Article

References (59)

1. Ahmed HJ, Svensson LA, Cope LD, Latimer JL, Hansen EJ, et al. (2001) Prevalence of cdtABC genes encoding cytolethal distending toxin among Haemophilus ducreyi and Actinobacillus actinomycetemcomitans strains. J Med Microbiol 50: 860-864.
2. McAuley JL, Linden SK, Png CW, King RM, Pennington HL, et al. (2007) MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 117: 2313-2324.
3. Young VB, Knox KA, Pratt JS, Cortez JS, Mansfield LS, et al. (2004) In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun 72: 2521-2527.
4. Fox JG, Rogers AB, Whary MT, Ge Z, Taylor NS, et al. (2004) Gastroenteritis in NF-kappaB-deficient mice is produced with wild-type Camplyobacter jejuni but not with C. jejuni lacking cytolethal distending toxin despite persistent colonization with both strains. Infect Immun 72: 1116-1125.
5. Purdy D, Buswell CM, Hodgson AE, McAlpine K, Henderson I, et al. (2000) Characterisation of cytolethal distending toxin (CDT) mutants of Campylobacter jejuni. J Med Microbiol 49: 473-479.
6. Ge Z, Rogers AB, Feng Y, Lee A, Xu S, et al. (2007) Bacterial cytolethal distending toxin promotes the development of dysplasia in a model of microbially induced hepatocarcinogenesis. Cell Microbiol 9: 2070-2080.
7. Ge Z, Feng Y, Whary MT, Nambiar PR, Xu S, et al. (2005) Cytolethal distending toxin is essential for Helicobacter hepaticus colonization in outbred Swiss Webster mice. Infect Immun 73: 3559-3567.
8. Gargi A, Reno M, Blanke SR, (2012) Bacterial toxin modulation of the eukaryotic cell cycle: are all cytolethal distending toxins created equally? Front Cell Infect Microbiol 2: 124.
9. Shenker BJ, Hoffmaster RH, Zekavat A, Yamaguchi N, Lally ET, et al. (2001) 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 167: 435-441.
10. Pickett CL, Whitehouse CA, (1999) The cytolethal distending toxin family. Trends Microbiol 7: 292-297.
11. Guidi R, Guerra L, Levi L, Stenerlow B, Fox JG, et al. (2013) Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell Microbiol 15: 98-113.
12. Guerra L, Cortes-Bratti X, Guidi R, Frisan T, (2011) The biology of the cytolethal distending toxins. Toxins (Basel) 3: 172-190.
13. Thelestam M, Frisan T, (2004) Cytolethal distending toxins. Rev Physiol Biochem Pharmacol 152: 111-133.
14. Blanke SR, (2006) Portals and Pathways: Principles of Bacterial Toxin Entry into Host Cells. Microbe 1: 26-32.
15. Elwell CA, Dreyfus LA, (2000) DNase I homologous residues in CdtB are critical for cytolethal distending toxin-mediated cell cycle arrest. Mol Microbiol 37: 952-963.
16. Lara-Tejero M, Galan JE, (2000) A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 290: 354-357.
17. McSweeney LA, Dreyfus LA, (2005) Carbohydrate-binding specificity of the Escherichia coli cytolethal distending toxin CdtA-II and CdtC-II subunits. Infect Immun 73: 2051-2060.
18. Cao L, Bandelac G, Volgina A, Korostoff J, DiRienzo JM, (2008) Role of aromatic amino acids in receptor binding activity and subunit assembly of the cytolethal distending toxin of Aggregatibacter actinomycetemcomitans. Infect Immun 76: 2812-2821.
19. Cao L, Volgina A, Huang CM, Korostoff J, DiRienzo JM, (2005) Characterization of point mutations in the cdtA gene of the cytolethal distending toxin of Actinobacillus actinomycetemcomitans. Mol Microbiol 58: 1303-1321.
20. Nesic D, Stebbins CE, (2005) Mechanisms of assembly and cellular interactions for the bacterial genotoxin CDT. PLoS Pathog 1: e28.
21. Gargi A, Tamilselvam B, Powers B, Prouty MG, Lincecum T, et al. (2013) Cellular interactions of the cytolethal distending toxins from escherichia coli and haemophilus ducreyi. J Biol Chem 288 (11):: 7492-505.
22. Guerra L, Teter K, Lilley BN, Stenerlow B, Holmes RK, et al. (2005) Cellular internalization of cytolethal distending toxin: a new end to a known pathway. Cell Microbiol 7: 921-934.
23. Spooner RA, Watson PD, Marsden CJ, Smith DC, Moore KA, et al. (2004) Protein disulphide-isomerase reduces ricin to its A and B chains in the endoplasmic reticulum. Biochem J 383: 285-293.
24. Day PJ, Owens SR, Wesche J, Olsnes S, Roberts LM, et al. (2001) An interaction between ricin and calreticulin that may have implications for toxin trafficking. J Biol Chem 276: 7202-7208.
25. Slominska-Wojewodzka M, Gregers TF, Walchli S, Sandvig K, (2006) EDEM is involved in retrotranslocation of ricin from the endoplasmic reticulum to the cytosol. Mol Biol Cell 17: 1664-1675.
26. Moreau D, Kumar P, Wang SC, Chaumet A, Chew SY, et al. (2011) Genome-wide RNAi screens identify genes required for Ricin and PE intoxications. Dev Cell 21: 231-244.
27. Li S, Spooner RA, Allen SC, Guise CP, Ladds G, et al. (2010) Folding-competent and folding-defective forms of ricin A chain have different fates after retrotranslocation from the endoplasmic reticulum. Mol Biol Cell 21: 2543-2554.
28. Redmann V, Oresic K, Tortorella LL, Cook JP, Lord M, et al. (2011) Dislocation of ricin toxin A chains in human cells utilizes selective cellular factors. J Biol Chem 286: 21231-21238.
29. Simpson JC, Roberts LM, Romisch K, Davey J, Wolf DH, et al. (1999) Ricin A chain utilises the endoplasmic reticulum-associated protein degradation pathway to enter the cytosol of yeast. FEBS Lett 459: 80-84.
30. Bernardi KM, Forster ML, Lencer WI, Tsai B, (2008) Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell 19: 877-884.
31. Dixit G, Mikoryak C, Hayslett T, Bhat A, Draper RK, (2008) Cholera toxin up-regulates endoplasmic reticulum proteins that correlate with sensitivity to the toxin. Exp Biol Med (Maywood) 233: 163-175.
32. Hebert DN, Bernasconi R, Molinari M, (2010) ERAD substrates: which way out? Semin Cell Dev Biol 21: 526-532.
33. Jarosch E, Taxis C, Volkwein C, Bordallo J, Finley D, et al. (2002) Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol 4: 134-139.
34. Rabinovich E, Kerem A, Frohlich KU, Diamant N, Bar-Nun S, (2002) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 22: 626-634.
35. Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA, (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429: 841-847.
36. Teter K, Holmes RK, (2002) Inhibition of endoplasmic reticulum-associated degradation in CHO cells resistant to cholera toxin, Pseudomonas aeruginosa exotoxin A, and ricin. Infect Immun 70: 6172-6179.
37. Guerra L, Nemec KN, Massey S, Tatulian SA, Thelestam M, et al. (2009) A novel mode of translocation for cytolethal distending toxin. Biochim Biophys Acta 1793: 489-495.
38. Damek-Poprawa M, Jang JY, Volgina A, Korostoff J, DiRienzo JM, (2012) Localization of Aggregatibacter actinomycetemcomitans cytolethal distending toxin subunits during intoxication of live cells. Infect Immun 80: 2761-2770.
39. McSweeney LA, Dreyfus LA, (2004) Nuclear localization of the Escherichia coli cytolethal distending toxin CdtB subunit. Cell Microbiol 6: 447-458.
40. Nishikubo S, Ohara M, Ueno Y, Ikura M, Kurihara H, et al. (2003) An N-terminal segment of the active component of the bacterial genotoxin cytolethal distending toxin B (CDTB) directs CDTB into the nucleus. J Biol Chem 278: 50671-50681.
41. 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.
42. Carette JE, Guimaraes CP, Wuethrich I, Blomen VA, Varadarajan M, et al. (2011) Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nat Biotechnol 29: 542-546.
43. Strausberg RL, Feingold EA, Klausner RD, Collins FS, (1999) The mammalian gene collection. Science 286: 455-457.
44. Banks DJ, Bradley KA, (2007) SILENCE: a new forward genetic technology. Nat Methods 4: 51-53.
45. Mali P, Yang L, Esvelt KM, Aach J, Guell M, et al. (2013) RNA-guided human genome engineering via Cas9. Science 339: 823-826.
46. Dang H, Klokk TI, Schaheen B, McLaughlin BM, Thomas AJ, et al. (2011) Derlin-dependent retrograde transport from endosomes to the Golgi apparatus. Traffic 12: 1417-1431.
47. Huang CH, Hsiao HT, Chu YR, Ye Y, Chen X, (2013) Derlin2 facilitates HRD1-mediated retro-translocation of sonic hedgehog at the endoplasmic reticulum. J Biol Chem 288 (35):: 25330-9.
48. Lilley BN, Ploegh HL, (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429: 834-840.
49. Greenblatt EJ, Olzmann JA, Kopito RR, (2011) Derlin-1 is a rhomboid pseudoprotease required for the dislocation of mutant alpha-1 antitrypsin from the endoplasmic reticulum. Nat Struct Mol Biol 18: 1147-1152.
50. Ye Y, Meyer HH, Rapoport TA, (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414: 652-656.
51. DeLaBarre B, Christianson JC, Kopito RR, Brunger AT, (2006) Central pore residues mediate the p97/VCP activity required for ERAD. Mol Cell 22: 451-462.
52. Wang Y, Zhang Y, Ha Y, (2006) Crystal structure of a rhomboid family intramembrane protease. Nature 444: 179-180.
53. Wu Z, Yan N, Feng L, Oberstein A, Yan H, et al. (2006) Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry. Nat Struct Mol Biol 13: 1084-1091.
54. Sandvig K, van Deurs B, (2005) Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther 12: 865-872.
55. Lilley BN, Gilbert JM, Ploegh HL, Benjamin TL, (2006) Murine polyomavirus requires the endoplasmic reticulum protein Derlin-2 to initiate infection. J Virol 80: 8739-8744.
56. Meyer H, Bug M, Bremer S, (2012) Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat Cell Biol 14: 117-123.
57. Eshraghi A, Maldonado-Arocho FJ, Gargi A, Cardwell MM, Prouty MG, et al. (2010) Cytolethal distending toxin family members are differentially affected by alterations in host glycans and membrane cholesterol. J Biol Chem 285: 18199-18207.
58. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA, (2001) Identification of the cellular receptor for anthrax toxin. Nature 414: 225-229.
59. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, et al. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343-345.