ChpK and MazF of the toxin-antitoxin modules are involved in the virulence of Leptospira interrogans during infection

Microbes and Infection

Volumn 17, Issue 1, 2015, Pages 34-47

  Komi, Komi Koukoura ^a   Ge, Yu Mei ^a,b   Xin, Xiao Yang ^a,b   Ojcius, David M ^c   Sun, Dexter ^d   Hu, Wei Lin ^a,b   Zhao, Xin ^a,b   Lin, Xu'ai ^a,b   Yan, Jie ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Leptospira interrogans; Toxin antitoxin module; Virulence

Indexed keywords

ANTITOXIN; BACTERIAL PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN CHPK; PROTEIN MAZF; TOXIN; UNCLASSIFIED DRUG; BACTERIAL TOXIN; CHPI PROTEIN, LEPTOSPIRA INTERROGANS; CHPK PROTEIN, BACTERIA; DNA BINDING PROTEIN;

APOPTOSIS; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL VIABILITY; CHPI GENE; CHPK GENE; CONTROLLED STUDY; CYTOPLASM; DNA DEGRADATION; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEPTOSPIRA INTERROGANS; LEPTOSPIROSIS; MACROPHAGE; MAZE GENE; MAZF GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RNA CLEAVAGE; RNA DEGRADATION; CELL LINE; CELL SURVIVAL; CHEMISTRY; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

EUKARYOTA; LEPTOSPIRA; LEPTOSPIRA INTERROGANS; PROKARYOTA;

APOPTOSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL LINE; CELL SURVIVAL; CYTOPLASM; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; HUMANS; LEPTOSPIRA INTERROGANS; MACROPHAGES; TRANSFECTION; VIRULENCE;

EID: 84921059078     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2014.10.010     Document Type: Article

References (65)

1. Bharti A.R., Nally J.E., Ricaldi J.N., Matthias M.A., Diaz M.M., Lovett M.A. Leptospirosis: a zoonotic disease of global importance. Lancet Infect Dis 2003, 3:757-771.
2. Zhang C.L., Wang H., Yan J. Leptospirosis prevalence in Chinese populations in the last two decades. Microbes Infect 2012, 14:317-323.
3. Sakundarno M., Bertolatti D., Maycock B., Spickett J., Dhaliwal S. Risk factors for leptospirosis infection in humans and implications for public health intervention in Indonesia and the Asia-Pacific region. Asia Pac J Public Health 2014, 26:15-32.
4. Smith J.K., Young M.M., Wilson K.L., Craig S.B. Leptospirosis following a major flood in Central Queensland, Australia. Epidemiol Infect 2013, 141:585-590.
5. Miraglia F., Matsuo M., Morais Z.M., Dellagostin O.A., Seixas F.K., Freitas J.C., et al. Molecular characterization, serotyping, and antibiotic susceptibility profile of Leptospira interrogans serovar Copenhageni isolates from Brazil. Diagn Microbiol Infect Dis 2013, 77:195-199.
6. Lo Y.C., Kintziger K.W., Carson H.J., Patrick S.L., Turabelidze G., Stanek D., et al. Severe leptospirosis similar to pandemic (H1N1) 2009, Florida and Missouri, USA. Emerg Infect Dis 2011, 17:1145-1146.
7. Hotez P.J., Gurwith M. Europe's neglected infections of poverty. Int J Infect Dis 2011, 15:e611-619.
8. Forbes A.E., Zochowski W.J., Dubrey S.W., Sivaprakasam V. Leptospirosis and Weil's disease in the UK. QJM 2012, 105:1151-1162.
9. Goris M.G., Boer K.R., Duarte T.A., Kliffen S.J., Hartskeerl R.A. Human leptospirosis trends, the Netherlands, 1925-2008. Emerg Infect Dis 2013, 19:371-378.
10. Plank R., Dean D. Overview of the epidemiology, microbiology, and pathogenesis of Leptospira spp. in humans. Microbes Infect 2000, 2:1265-1276.
11. Adler B., Moctezuma A. Leptospira and leptospirosis. Vet Microbiol 2010, 140:287-296.
12. McBride A.J., Athanazio D.A., Reis M.G., Ko A.I. Leptospirosis. Curr Opin Infect Dis 2005, 18:376-386.
13. De Brito T., Aiello V.D., da Silva L.F., Goncalves da Silva A.M., Ferreira da Silva W.L., Castelli J.B., et al. Human hemorrhagic pulmonary leptospirosis: pathological findings and pathophysiological correlations. PLoS One 2013, 8:e71743-71753.
14. Dassanayake D.L., Wimalaratna H., Nandadewa D., Nugaliyadda A., Ratnatunga C.N., Agampodi S.B. Predictors of the development of myocarditis or acute renal failure in patients with leptospirosis: an observational study. BMC Infect Dis 2012, 12:e4-10.
15. Lee S.H., Kim S., Park S.C., Kim M.J. Cytotoxic activities of Leptospira interrogans hemolysin SphH as a pore-forming protein on mammalian cells. Infect Immun 2002, 70:315-322.
16. Carvalho E., Barbosa A.S., Gómez R.M., Oliveira M.L., Romero E.C., Goncales A.P., et al. Evaluation of the expression and protective potential of leptospiral sphingomyelinases. Curr Microbiol 2010, 60:134-142.
17. Wang H., Wu Y.F., Ojcius D.M., Yang X.F., Zhang C.L., Ding S.B., et al. Leptospiral hemolysins induce proinflammatory cytokines through Toll-like receptor 2- and 4-mediated JNK and NF-κB signaling pathways. PLoS One 2012, 7:e42266-42280.
18. Faine S., Adler B., Bolin C. Leptospira and leptospirosis 1999, MediSci, Melbourne. 2nd ed.
19. de Souza L., Koury M.C. Isolation and biological activities of endotoxin from Leptospira interrogans. Can J Microbiol 1992, 38:284-289.
20. Engelberg-Kulka H., Glaser G. Addiction modules and programmed cell death and antideath in bacterial cultures. Annu Rev Microbiol 1999, 53:43-70.
21. Hayes F. Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 2003, 301:1496-1499.
22. Gerdes K., Christensen K.S., Løbner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 2005, 3:371-382.
23. Christensen S.K., Gerdes K. RelE toxins from bacteria and archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol Microbiol 2003, 48:1389-1400.
24. Zhang Y.L., Zhang J.J., Hoeflich K.P., Ikura M., Qing G.L., Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol Cell 2003, 12:913-923.
25. Zhang Y.L., Zhu L., Zhang J.J., Inouye M. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J Biol Chem 2005, 280:26080-26088.
26. Muñoz-Gómez A.J., Santos-Sierra S., Berzal-Herranz A., Lemonnier M., Díaz-Orejas R. Insights into the specificity of RNA cleavage by the Escherichia coli MazF toxin. FEBS Lett 2004, 567:316-320.
27. Engelberg-Kulka H., Hazan R., Amitai S. mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria. J Cell Sci 2005, 118:4327-4332.
28. Fu Z.B., Niles D.P., Guido M., Ambrose C.L. Characterization of MazFsa, an endoribonuclease from Staphylococcus aureus. J Bacteriol 2007, 189:8871-8879.
29. Agarwal S., Agarwal S., Bhatnagar R. Identification and characterization of a novel toxin-antitoxin module from Bacillus anthracis. FEBS Lett 2007, 581:1727-1734.
30. Ren S.X., Fu G., Jiang X.G., Zeng R., Miao Y.G., Xu H., et al. Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 2003, 422:888-893.
31. Nascimento A.L., Ko A.I., Martins E.A., Monteiro-Vitorello C.B., Ho P.L., Haake D.A., et al. Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J Bacteriol 2004, 186:2164-2172.
32. Picardeau M., Ren S., Girons I.S. Killing effect and antitoxic activity of the Leptospira interrogans toxin-antitoxin system in Escherichia coli. J Bacteriol 2001, 183:6494-6497.
33. Picardeau M., Dantec C.L., Richard G.F., Girons I.S. The spirochetal chpK-chromosomal toxin-antitoxin locus induces growth inhibition of yeast and mycobacteria. FEMS Microbiol Lett 2003, 229:277-281.
34. Navarre W.W., Zychlinsky A. Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell Microbiol 2000, 2:265-273.
35. Jin D.D., Ojcius D.M., Sun D., Dong H.Y., Luo Y.H., Mao Y.F., et al. Leptospira interrogans induces apoptosis in macrophages via caspase-8- and caspase-3-dependent pathways. Infect Immun 2009, 77:799-809.
36. Li S.J., Ojcius D.M., Liao S.M., Li L.W., Xue F., Dong H.Y., et al. Replication or death: distinct fates of pathogenic Leptospira strain Lai within macrophages of human or mouse origin. Innate Immun 2010, 16:80-92.
37. Hu W.L., Ge Y.M., Ojcius D.M., Sun D., Dong H.Y., Yang X.F., et al. p53-signaling controls cell cycle arrest and caspase-independent apoptosis in macrophages infected with pathogenic Leptospira species. Cell Microbiol 2013, 15:1624-1659.
38. Yamamoto T.A.M., Gerdes K., Tunnacliffe A. Bacterial toxin RelE induces apoptosis in human cells. FEBS Lett 2002, 519:191-194.
39. Gerdes K. Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress. J Bacteriol 2000, 182:561-572.
40. Dong H.Y., Hu Y., Xue F., Sun D., Ojcius D.M., Mao Y.F., et al. Characterization of the ompL1 gene of pathogenic Leptospira species in China and cross-immunogenicity of the OmpL1 protein. BMC Microbiol 2008, 8:223-235.
41. Zhang L., Zhang C.L., Ojcius D.M., Zhao J.F., Lin X.A., Mao Y.F., et al. Identification of Mce as a critical outer membrane protein of pathogenic Leptospira species responsible for RGD motif-dependent adherence and host-cell invasion. Mol Microbiol 2012, 83:1006-1023.
42. Carrillo-Casas E.M., Hernández-Castro R., Suárez-Güemes F., de la Peña-Moctezuma A. Selection of the internal control gene for real-time quantitative RT-PCR assays in temperature treated Leptospira. Curr Microbiol 2008, 56:539-546.
43. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36-46.
44. Liao S.M., Sun A.H., Ojcius D.M., Wu S.L., Zhao J.F., Yan J. Inactivation of the fliY gene encoding a flagellar motor switch protein attenuates mobility and virulence of Leptospira interrogans strain Lai. BMC Microbiol 2009, 9:253-263.
45. Bauby H., Saint G.I., Picardeau M. Construction and complementation of the first auxotrophic mutant in the spirochaete Leptospira meyeri. Microbiology 2003, 149:689-693.
46. Schnoor M., Buers I., Sietmann A., Brodde M.F., Hofnagel O., Robenek H., et al. Efficient non-viral transfection of THP-1 cells. J Immunol Methods 2009, 344:109-115.
47. Tominaga H., Ishiyama M., Ohseto F., Sasamoto K., Hamamoto T., Suzuki K., et al. A water-soluble tetrazolium salt useful for colorimetric cell viability assay. Anal Commun 1999, 36:47-50.
48. Xue F., Dong H.Y., Wu J.Y., Wu Z.W., Hu W.L., Sun A.H., et al. Transcriptional responses of Leptospira interrogans to host innate immunity: significant changes in metabolism, oxygen tolerance, and outer membrane. PLoS Negl Trop Dis 2010, 4:e857-874.
49. Daines D.A., Wu M.H., Yuan S.Y. VapC-1 of nontypeable Haemophilus influenzae is a ribonuclease. J Bacteriol 2007, 189:5041-5048.
50. Kamada K., Fumio H., Burley S.K. Crystal structure of the MazE/MazF complex: molecular bases of antidote-toxin recognition. Mol Cell 2003, 11:875-884.
51. Aizenman E., Engelberg-Kulka H., Glaser G. An Escherichia coli chromosomal "addiction module" regulated by ppGpp: a model for programmed cell death. Proc Natl Acad Sci U S A 1996, 93:6059-6063.
52. Dorn G.W. Molecular mechanisms that differentiate apoptosis from programmed necrosis. Toxicol Pathol 2013, 41:227-234.
53. Gitlin L., Karelsky S., Andino R. Short interfering RNA confers intracellular antiviral immunity in human cells. Nature 2002, 418:430-434.
54. Christensen S.K., Pedersen K., Hansen F.G., Gerdes K. Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J Mol Biol 2003, 332:809-819.
55. Guglielmini J., Szpirer C., Milinkovitch M.C. Automated discovery and phylogenetic analysis of new toxin-antitoxin systems. BMC Microbiol 2008, 8:104-120.
56. Kolodkin-Gal I., Hazan R., Gaathon A., Carmeli S., Engelberg-Kulka H. A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli. Science 2007, 318:652-655.
57. Hazan R., Engelberg-Kulka H. Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1. Mol Genet Genomics 2004, 272:227-234.
58. Wang N.R., Hergenrother P.J. A continuous fluorometric assay for the assessment of MazF ribonuclease activity. Anal Biochem 2007, 371:173-183.
59. de la Cueva-Méndez G., Mills A.D., Clay-Farrace L., Díaz-Orejas R., Laskey R.A. Regulatable killing of eukaryotic cells by the prokaryotic proteins Kid and Kis. EMBO J 2003, 22:246-251.
60. Shimazu T., Degenhardt K., Nur-E-Kamal A., Zhang J., Yoshida T., Zhang Y., et al. NBK/BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition. Genes Dev 2007, 21:929-941.
61. Xue F., Yan J., Picardeau M. Evolution and pathogenesis of Leptospira spp.: lessons learned from the genomes. Microbes Infect 2009, 11:328-333.
62. Ko A.I., Goarant C., Picardeau M. Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat Rev Microbiol 2009, 7:736-747.
63. Cinco M., Banfi E., Soranzo M.R. Studies on the interaction between macrophages and leptospires. J Gen Microbiol 1981, 4:409-413.
64. Davis J.M., Haake D.A., Ramakrishnan L. Leptospira interrogans stably infects zebrafish embryos, altering phagocyte behavior and homing to specific tissues. PLoS Negl Trop Dis 2009, 3:e463-469.
65. Ruiz-Echevarria M.J., Gimenez-Gallego G., Sabariegos-Jareno R., Diaz-Orejas R. Kid, a small protein of the parD stability system of plasmid R1, is an inhibitor of DNA replication acting at the initiation of DNA synthesis. J Mol Biol 1995, 247:568-577.