Transcriptional down-regulation and rRNA cleavage in Dictyostelium discoideum mitochondria during Legionella pneumophila infection

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Zhang, Chenyu ^a   Kuspa, Adam ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC AGENT; HYDROGEN PEROXIDE; MESSENGER RNA; MITOCHONDRIAL RNA; RIBOSOME RNA; BACTERIAL PROTEIN;

ACANTHAMOEBA CASTELLANII; ARTICLE; CELL DEATH; CELL STRAIN U937; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; DISEASE COURSE; DOWN REGULATION; HOST CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LARGE RIBOSOMAL SUBUNIT; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; METABOLISM; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROTEIN SYNTHESIS; RNA CLEAVAGE; SMALL RIBOSOMAL SUBUNIT; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DICTYOSTELIUM; GENETIC TRANSCRIPTION; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ACANTHAMOEBA CASTELLANII; AMOEBA (GENUS); BACTERIA (MICROORGANISMS); DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; LEGIONELLA PNEUMOPHILA;

ACANTHAMOEBA CASTELLANII; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CELL DEATH; DICTYOSTELIUM; DOWN-REGULATION; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONELLOSIS; MITOCHONDRIA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; RIBOSOME SUBUNITS, LARGE; RNA, MESSENGER; RNA, RIBOSOMAL; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC; U937 CELLS;

EID: 66349086845     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005706     Document Type: Article

References (58)

1. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, et al. (1977) Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 297: 1189-1197.
2. McDade JE, Shepard CC, Fraser DW, Tsai TR, Redus MA, et al. (1977) Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297: 1197-1203.
3. Chandler FW, Hicklin MD, Blackmon JA (1977) Demonstration of the agent of Legionnaires' disease in tissue. N Engl J Med 297: 1218-1220.
4. Wadowsky RM, Butler LJ, Cook MK, Verma SM, Paul MA, et al. (1988) Growth-supporting activity for Legionella pneumophila in tap water cultures and implication of hartmannellid amoebae as growth factors. Appl Environ Microbiol 54: 2677-2682.
5. Rowbotham TJ (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33: 1179-1183.
6. Rowbotham TJ (1983) Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J Clin Pathol 36: 978-986.
7. Horwitz MA (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
8. Horwitz MA, Maxfield FR (1984) Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J Cell Biol 99: 1936-1943.
9. Tilney LG, Harb OS, Connelly PS, Robinson CG, Roy CR (2001) How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J Cell Sci 114: 4637-4650.
10. Horwitz MA, Silverstein SC (1983) Intracellular multiplication of Legionnaires' disease bacteria (Legionella pneumophila) in human monocytes is reversibly inhibited by erythromycin and rifampin. J Clin Invest 71: 15-26.
11. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, et al. (2004) Legionella effectors that promote nonlytic release from protozoa. Science 303: 1358-1361.
12. Juhas M, Crook DW, Hood DW (2008) Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 10: 2377-2386.
13. Marra A, Blander SJ, Horwitz MA, Shuman HA (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci U S A 89: 9607-9611.
14. Berger KH, Isberg RR (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7: 7-19.
15. Hilbi H, Segal G, Shuman HA (2001) Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol Microbiol 42: 603-617.
16. Hales LM, Shuman HA (1999) Legionella pneumophila contains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect Immun 67: 3662-3666.
17. Rossier O, Cianciotto NP (2001) Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila. Infect Immun 69: 2092-2098.
18. Kessin RH (2001) Dictyostelium: evolution, cell biology, and the development of multicellularity. Cambridge, UK: Cambridge University Press.
19. Abu Kwaik Y, Gao LY, Stone BJ, Venkataraman C, Harb OS (1998) Invasion of protozoa by Legionella pneumophila and its role in bacterial ecology and pathogenesis. Appl Environ Microbiol 64: 3127-3133.
20. Shuman HA, Purcell M, Segal G, Hales L, Wiater LA (1998) Intracellular multiplication of Legionella pneumophila: human pathogen or accidental tourist? Curr Top Microbiol Immunol 225: 99-112.
21. Solomon JM, Rupper A, Cardelli JA, Isberg RR (2000) Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Inf Immun 68: 2939-2947.
22. Hagele S, Kohler R, Merkert H, Schleicher M, Hacker J, et al. (2000) Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2: 165-171.
23. Ogawa S, Yoshino R, Angata K, Iwamoto M, Pi M, et al. (2000) The mitochondrial DNA of Dictyostelium discoideum: complete sequence, gene content and genome organization. Mol Gen Genet 263: 514-519.
24. Wilczynska Z, Barth C, Fisher PR (1997) Mitochondrial mutations impair signal transduction in Dictyostelium discoideum slugs. Biochem Biophys Res Commun 234: 39-43.
25. Feeley JC, Gorman GW, Weaver RE, Mackel DC, Smith HW (1978) Primary isolation media for Legionnaires disease bacterium. J Clin Microbiol 8: 320-325.
26. Feeley JC, Gibson RJ, Gorman GW, Langford NC, Rasheed JK, et al. (1979) Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J Clin Microbiol 10: 437-441.
27. Sussman M (1987) Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. In: Spudich JA, ed. Methods in Cell Biology. Orlando, FL: Ac. Press. pp 9-29.
28. Moffat JF, Tompkins LS (1992) A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellanii. Infect Immun 60: 296-301.
29. Pearlman E, Jiwa AH, Engleberg NC, Eisenstein BI (1988) Growth of Legionella pneumophila in a human macrophage-like (U937) cell line. Microb Pathog 5: 87-95.
30. Byrne B, Swanson MS (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029-3034.
31. Sussman R, Rayner EP (1971) Physical characterization of deoxyribonucleic acids in Dictyostelium discoideum. Arch Biochem Biophys 144: 127-137.
32. Cannone JJ, Subramanian S, Schnare MN, Collett JR, D'Souza LM, et al. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3: 2.
33. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289: 905-920.
34. Ban N, Nissen P, Hansen J, Capel M, Moore PB, et al. (1999) Placement of protein and RNA structures into a 5 A-resolution map of the 50S ribosomal subunit. Nature 400: 841-847.
35. Sayle RA, Milner-White EJ (1995) RASMOL: biomolecular graphics for all. Trends Biochem Sci 20: 374.
36. Barth C, Greferath U, Kotsifas M, Tanaka Y, Alexander S, et al. (2001) Transcript mapping and processing of mitochondrial RNA in Dictyostelium discoideum. Curr Genet 39: 355-364.
37. Muller A, Hacker J, Brand BC (1996) Evidence for apoptosis of human macrophage-like HL-60 cells by Legionella pneumophila infection. Infect Immun 64: 4900-4906.
38. Gao LY, Abu Kwaik Y (1999) Apoptosis in macrophages and alveolar epithelial cells during early stages of infection by Legionella pneumophila and its role in cytopathogenicity. Infect Immun 67: 862-870.
39. Neumeister B, Faigle M, Lauber K, Northoff H, Wesselborg S (2002) Legionella pneumophila induces apoptosis via the mitochondrial death pathway. Microbiology 148: 3639-3650.
40. Morris EJ, Geller HM (1996) Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. J Cell Biol 134: 757-770.
41. Hande KR (1998) Etoposide: four decades of development of a topoisomerase II inhibitor. Eur J Cancer 34: 1514-1521.
42. Matsumoto H, Sasaki Y (1989) Staurosporine, a protein kinase C inhibitor interferes with proliferation of arterial smooth muscle cells. Biochem Biophys Res Commun 158: 105-109.
43. Chien M, Morozova I, Shi S, Sheng H, Chen J, et al. (2004) The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305: 1966-1968.
44. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, et al. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36: 1165-1173.
45. Rossier O, Starkenburg SR, Cianciotto NP (2004) Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires' disease pneumonia. Infect Immun 72: 310-321.
46. Lammertyn E, Anne J (2004) Protein secretion in Legionella pneumophila and its relation to virulence. FEMS Microbiol Lett 238: 273-279.
47. Sadosky AB, Wiater LA, Shuman HA (1993) Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61: 5361-5373.
48. Berger KH, Merriam JJ, Isberg RR (1994) Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol Microbiol 14: 809-822.
49. Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A 85: 8998-9002.
50. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283: 1476-1481.
51. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, et al. (2003) Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115: 97-108.
52. Scandalios JG, ed (1997) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press. pp 1-890.
53. Nulton-Persson AC, Szweda LI (2001) Modulation of mitochondrial function by hydrogen peroxide. J Biol Chem 276: 23357-23361.
54. Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, et al. (2001) Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 88: 529-535.
55. Farbrother P, Wagner C, Na J, Tunggal B, Morio T, et al. (2006) Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol 8: 438-456.
56. Crawford DR, Lauzon RJ, Wang Y, Mazurkiewicz JE, Schools GP, et al. (1997) 16S mitochondrial ribosomal RNA degradation is associated with apoptosis. Free Radic Biol Med 22: 1295-1300.
57. Zhu QL, Hulen D, Liu TY, Clarke M (1997) The cluA(-) mutant of Dictyostelium identifies a novel class of proteins required for dispersion of mitochondria. Proc Natl Acad Sci USA 94: 7308-7313.
58. Horwitz MA (1983) Symbiotic interactions between Legionella pneumophila and human leukocytes. Int Rev Cytol Suppl 14: 307-328.