Enterotoxicity of a nonribosomal peptide causes antibiotic-associated colitis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 36, 2014, Pages 13181-13186

  Schneditz, Georg ^a   Rentner, Jana ^b   Roier, Sandro ^a   Pletz, Jakob ^b   Herzog, Kathrin A T ^c   Bücker, Roland ^d   Troeger, Hanno ^d   Schild, Stefan ^a   Weber, Hansjörg ^b   Breinbauer, Rolf ^b   Gorkiewicz, Gregor ^c   Högenauer, Christoph ^c   Zechner, Ellen L ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Bacteria; Cytotoxin; Enteric microbiota

Indexed keywords

ANTIINFECTIVE AGENT; BENZODIAZEPINE DERIVATIVE; CASPASE 3; CYTOTOXIN; ENTEROTOXIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; PENICILLIN DERIVATIVE; PEPTIDE; PEPTIDE SYNTHASE; TILIVALLINE;

ACTINOBACTERIA; ANIMAL; APOPTOSIS; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; HUMAN; KLEBSIELLA OXYTOCA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; PATHOLOGY; RIBOSOME;

ACTINOBACTERIA; ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; BENZODIAZEPINONES; CASPASE 3; COLITIS; CYTOTOXINS; ENTEROTOXINS; EPITHELIAL CELLS; HUMANS; KLEBSIELLA OXYTOCA; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PENICILLINS; PEPTIDE SYNTHASES; PEPTIDES; RIBOSOMES;

EID: 84906979439     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1403274111     Document Type: Article

References (51)

1. Eckburg PB, et al. (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635-1638.
2. Sommer F, Bäckhed F (2013) The gut microbiota - masters of host development and physiology. Nat Rev Microbiol 11(4):227-238.
3. Karlsson FH, et al. (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498(7452):99-103.
4. Yoshimoto S, et al. (2013) Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499(7456):97-101.
5. Olszak T, et al. (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336(6080):489-493.
6. Schnabl B, Brenner DA (2014) Interactions between the intestinal microbiome and liver diseases. Gastroenterology 146(6):1513-1524.
7. Henao-Mejia J, et al. (2012) Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482(7384):179-185.
8. Russell WR, Hoyles L, Flint HJ, Dumas ME (2013) Colonic bacterial metabolites and human health. Curr Opin Microbiol 16(3):246-254.
9. Högenauer C, Hammer HF, Krejs GJ, Reisinger EC (1998) Mechanisms and management of antibiotic-associated diarrhea. Clin Infect Dis 27(4):702-710.
10. Stecher B, Maier L, Hardt WD (2013) 'Blooming' in the gut: How dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11(4):277-284.
11. Ayres JS, Trinidad NJ, Vance RE (2012) Lethal inflammasome activation by a multi-drug-resistant pathobiont upon antibiotic disruption of the microbiota. Nat Med 18(5):799-806.
12. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9(5):313-323.
13. Beaugerie L, et al.; Infectious Colitis Study Group (2003) Klebsiella oxytoca as an agent of antibiotic-associated hemorrhagic colitis. Clin Gastroenterol Hepatol 1(5):370-376.
14. Högenauer C, et al. (2006) Klebsiella oxytoca as a causative organism of antibiotic-associated hemorrhagic colitis. N Engl J Med 355(23):2418-2426.
15. Zollner-Schwetz I, et al. (2008) Role of Klebsiella oxytoca in antibiotic-associated diarrhea. Clin Infect Dis 47(9):e74-e78.
16. Livermore DM (1995) beta-Lactamases in laboratory and clinical resistance. Clin Microbiol Rev 8(4):557-584.
17. Chow J, Tang H, Mazmanian SK (2011) Pathobionts of the gastrointestinal microbiota and inflammatory disease. Curr Opin Immunol 23(4):473-480.
18. Minami J, Okabe A, Shiode J, Hayashi H (1989) Production of a unique cytotoxin by Klebsiella oxytoca. Microb Pathog 7(3):203-211.
19. Joainig MM, et al. (2010) Cytotoxic effects of Klebsiella oxytoca strains isolated from patients with antibiotic-associated hemorrhagic colitis or other diseases caused by infections and from healthy subjects. J Clin Microbiol 48(3):817-824.
20. Higaki M, Chida T, Takano H, Nakaya R (1990) Cytotoxic component(s) of Klebsiella oxytoca on Hep-2 cells. Microbiol Immunol 34(2):147-151.
21. Herzog KA, et al. (2014) Genotypes of Klebsiella oxytoca isolates from patients with nosocomial pneumonia are distinct from those of isolates from patients with anti-biotic-associated hemorrhagic colitis. J Clin Microbiol 52(5):1607-1616.
22. Marahiel MA (2009) Working outside the protein-synthesis rules: Insights into non-ribosomal peptide synthesis. J Pept Sci 15(12):799-807.
23. Fischbach MA, Walsh CT (2006) Assembly-line enzymology for polyketide and non-ribosomal Peptide antibiotics: Logic, machinery, and mechanisms. Chem Rev 106(8):3468-3496.
24. Bachmann BO, Ravel J (2009) Chapter 8. Methods for in silico prediction of microbial polyketide and nonribosomal peptide biosynthetic pathways from DNA sequence data. Methods Enzymol 458:181-217.
25. Stachelhaus T, Mootz HD, Marahiel MA (1999) The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 6(8):493-505.
26. Srinivasan PR, Rothschild J, Sprinson DB (1963) The enzymic conversion of 3-deoxy-D-arabino-heptulosonic acid 7-phosphate to 5-dehydroquinate. J Biol Chem 238:3176-3182.
27. Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473-503.
28. Herrmann KM (1995) The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 107(1):7-12.
29. Buchrieser C, Brosch R, Bach S, Guiyoule A, Carniel E (1998) The high-pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal asn tRNA genes. Mol Microbiol 30(5):965-978.
30. Lin TL, Lee CZ, Hsieh PF, Tsai SF, Wang JT (2008) Characterization of integrative and conjugative element ICEKp1-associated genomic heterogeneity in a Klebsiella pneumoniae strain isolated from a primary liver abscess. J Bacteriol 190(2):515-526.
31. Schubert S, Dufke S, Sorsa J, Heesemann J (2004) A novel integrative and conjugative element (ICE) of Escherichia coli: The putative progenitor of the Yersinia high-pathogenicity island. Mol Microbiol 51(3):837-848.
32. Putze J, et al. (2009) Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect Immun 77(11):4696-4703.
33. Li W, Chou S, Khullar A, Gerratana B (2009) Cloning and characterization of the biosynthetic gene cluster for tomaymycin, an SJG-136 monomeric analog. Appl Environ Microbiol 75(9):2958-2963.
34. Li W, Khullar A, Chou S, Sacramo A, Gerratana B (2009) Biosynthesis of sibiromycin, a potent antitumor antibiotic. Appl Environ Microbiol 75(9):2869-2878.
35. Hu Y, et al. (2007) Benzodiazepine biosynthesis in Streptomyces refuineus. Chem Biol 14(6):691-701.
36. Hurley LH, Lasswell WL, Malhotra RK, Das NV (1979) Pyrrolo[1,4]benzodiazepine antibiotics. Biosynthesis of the antitumor antibiotic sibiromycin by Streptosporangium sibiricum. Biochemistry 18(19):4225-4229.
37. Mohr N, Budzikiewicz H (1982) Tilivalline, a new pyrrolo[2, 1-c][1,4] benzodiazepine metabolite from klebsiella. Tetrahedron 38(1):147-152.
38. Nagasaka T, Koseki Y (1998) Stereoselective synthesis of tilivalline(1). J Org Chem 63(20):6797-6801.
39. Shioiri T, et al. (1995) Structure-cytotoxicity relationship of tilivalline derivatives. Anticancer Drug Des 10(2):167-176.
40. Högenauer C, Hinterleitner T (2008) Klebsiella oxytoca as a cause of antibiotic-associated colitis. Emerging Infections, eds Scheld WMHS, Hughes JM (ASM, Washington, DC), pp 293-311.
41. Nougayrède JP, et al. (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313(5788):848-851.
42. Lai YC, et al. (2014) Genotoxic Klebsiella pneumoniae in Taiwan. PloS ONE 9(5):e96292.
43. Gerratana B (2012) Biosynthesis, synthesis, and biological activities of pyrrolobenzodiazepines. Med Res Rev 32(2):254-293.
44. Rahbaek L, Breinholt J (1999) Circumdatins D, E, and F: Further fungal benzodiazepine analogues from aspergillus ochraceus. J Nat Prod 62(6):904-905.
45. López-Gresa MP, et al. (2005) Circumdatin H, a new inhibitor of mitochondrial NADH oxidase, from Aspergillus ochraceus. J Antibiot (Tokyo) 58(6):416-419.
46. Arthur JC, et al. (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338(6103):120-123.
47. Cuevas-Ramos G, et al. (2010) Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA 107(25):11537-11542.
48. Secher T, Samba-Louaka A, Oswald E, Nougayrède JP (2013) Escherichia coli producing colibactin triggers premature and transmissible senescence in mammalian cells. PloS ONE 8(10):e77157.
49. Hurley LH, Gairola C, Zmijewski M (1977) Pyrrolo(1,4)benzodiazepine antitumor antibiotics. In vitro interaction of anthramycin, sibiromycin and tomaymycin with DNA using specifically radiolabelled molecules. Biochim Biophys Acta 475(3):521-535.
50. Hartley JA (2011) The development of pyrrolobenzodiazepines as antitumour agents. Expert Opin Investig Drugs 20(6):733-744.
51. Hurley LH (1977) Pyrrolo(1,4)benzodiazepine antitumor antibiotics. Comparative aspects of anthramycin, tomaymycin and sibiromycin. J Antibiot (Tokyo) 30(5):349-370.