Attenuated activation of macrophage TLR9 by DNA from virulent mycobacteria

Journal of Innate Immunity

Volumn 1, Issue 1, 2008, Pages 29-45

  Kiemer, Alexandra K ^a,c,e   Senaratne, Ryan H ^f   Hoppstädter, Jessica ^a   Diesel, Britta ^a   Riley, Lee W ^f   Tabeta, Koichi ^d   Bauer, Stefan ^b   Beutler, Bruce ^d   Zuraw, Bruce L ^e,f  

^a SAARLAND UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Host defence; Inflammation, lung; Macrophages; Mycobacteria; Oligonucleotide; Pathogen associated molecular patterns; Pathogenesis; Toll like receptor; Tuberculosis; Virulence factors

Indexed keywords

BACTERIAL DNA; MESSENGER RNA; OLIGONUCLEOTIDE; TOLL LIKE RECEPTOR 9;

ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL ISOLATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA ISOLATION; GENE EXPRESSION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MONOCYTE; MOUSE; MOUSE MUTANT; MYCOBACTERIOSIS; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WILD TYPE;

ANIMALS; CYTOKINES; DNA, BACTERIAL; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES, ALVEOLAR; MICE; MICE, MUTANT STRAINS; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; PHOSPHOROTHIOATE OLIGONUCLEOTIDES; TOLL-LIKE RECEPTOR 9; TUBERCULOSIS, PULMONARY;

EID: 63449093275     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000142731     Document Type: Article

References (53)

1. Doffinger R, Patel SY, Kumararatne DS: Host genetic factors and mycobacterial infections: lessons from single gene disorders affecting innate and adaptive immunity. Microbes Infect 2006; 8:1141-1150.
2. Beutler B: Inferences, questions and possibilities in Toll-like receptor signalling. Nature 2004; 430:257-263.
3. Shimada S, Yano O, Inoue H, Kuramoto E, Fukuda T, Yamamoto H, Kataoka T, Tokunaga T: Antitumor activity of the DNA fraction from Mycobacterium bovis BCG. II. Effects on various syngeneic mouse tumors. J Natl Cancer Inst 1985; 74: 681-688.
4. Tokunaga T, Yamamoto H, Shimada S, Abe H, Fukuda T, Fujisawa Y, Furutani Y, Yano O, Kataoka T, Sudo T: Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity. J Natl Cancer Inst 1984; 72: 955-962.
5. Bafica A, Scanga CA, Feng CG, Sher A, Leifer C, Cheever A: TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 2005; 202:1715-1724.
6. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, Akira S: A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408: 740-745.
7. Leifer CA, Kennedy MN, Mazzoni A, Lee C, Kruhlak MJ, Segal DM: TLR9 is localized in the endoplasmic reticulum prior to stimulation. J Immunol 2004; 173:1179-1183.
8. Latz E, Schoenemeyer A, Visintin A, Fitzgerald KA, Monks BG, Knetter CF, Lien E, Nilsen NJ, Espevik T, Golenbock DT: TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat Immunol 2004; 5: 190-198.
9. Miettinen M, Sareneva T, Julkunen I, Matikainen S: IFNs activate Toll-like receptor gene expression in viral infections. Genes Immun 2001; 2: 349-355.
10. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, Giese T, Endres S, Hartmann G: Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 2002; 168:4531-4537.
11. Doyle SE, O'Connell RM, Vaidya SA, Liu PT, Cheng G, Miranda GA, Lane TF, Chow EK, Modlin RL, Suzuki S, Suzuki N, Yeh WC: Toll-like receptors induce a phagocytic gene program through p38. J Exp Med 2004; 199: 81-90.
12. Takeshita F, Suzuki K, Sasaki S, Ishii N, Klinman DM, Ishii KJ: Transcriptional regulation of the human TLR9 gene. J Immunol 2004; 173:2552-2561.
13. Remer KA, Brcic M, Sauter KS, Jungi TW: Human monocytoid cells as a model to study Toll-like receptor-mediated activation. J Immunol Methods 2006; 313: 1-10.
14. Hartmann G, Krieg AM: CpG DNA and LPS induce distinct patterns of activation in human monocytes. Gene Ther 1999; 6:893-903.
15. Hornung V, Guenthner-Biller M, Bourquin C, Ablasser A, Schlee M, Uematsu S, Noronha A, Manoharan M, Akira S, de Fou-gerolles A, Endres S, Hartmann G: Sequence-specific potent induction of IFN-α by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med 2005; 11:263-270.
16. Sawamura D, Abe R, Goto M, Akiyama M, Hemmi H, Akira S, Shimizu H: Direct injection of plasmid DNA into the skin induces dermatitis by activation of monocytes through toll-like receptor 9. J Gene Med 2005; 7:664-671.
17. Fenhalls G, Squires GR, Stevens-Muller L, Bezuidenhout J, Amphlett G, Duncan K, Lukey PT: Associations between Toll-like receptors and interleukin-4 in the lungs of patients with tuberculosis. Am J Respir Cell Mol Biol 2003; 29:28-38.
18. Hoene V, Peiser M, Wanner R: Human monocyte-derived dendritic cells express TLR9 and react directly to the CpG-A oligonucleotide D19. J Leukoc Biol 2006; 80:1328-1336.
19. Mao TK, Lian ZX, Selmi C, Ichiki Y, Ashwood P, Ansari AA, Coppel RL, Shimoda S, Ishibashi H, Gershwin ME: Altered monocyte responses to defined TLR ligands in patients with primary biliary cirrhosis. Hepatology 2005; 42:802-808.
20. Roberts TL, Dunn JA, Terry TD, Jennings MP, Hume DA, Sweet MJ, Stacey KJ: Differences in macrophage activation by bacterial DNA and CpG-containing oligonucleotides. J Immunol 2005; 175: 3569-3576.
21. Kiemer AK, Hartung T, Vollmar AM: cGMP-mediated inhibition of TNF-α production by the atrial natriuretic peptide in murine macrophages. J Immunol 2000; 165:175-181.
22. Plesner A: Increasing the yield of human mononuclear cells and low serum conditions for in vitro generation of macrophages with M-CSF. J Immunol Methods 2003; 279:287-295.
23. Kiemer AK, Vollmar AM: Autocrine regulation of inducible nitric-oxide synthase in macrophages by atrial natriuretic peptide. J Biol Chem 1998; 273:13444-13451.
24. Santos AR, de Miranda AB, Lima LM, Suffys N, Degrave WM: Method for high yield preparation in large and small scale of nucleic acids from mycobacteria. J Microbiol Methods 1992; 15: 83-94.
25. Cotten M, Baker A, Saltik M, Wagner E, Buschle M: Lipopolysaccharide is a frequent contaminant of plasmid DNA preparations and can be toxic to primary human cells in the presence of adenovirus. Gene Ther 1994; 1:239-246.
26. Buryanov Y, Shevchuk T: The use of prokary-otic DNA methyltransferases as experimental and analytical tools in modern biology. Anal Biochem 2005; 338: 1-11.
27. Kiemer AK, Weber NC, Vollmar AM: Induction of IkB: atrial natriuretic peptide as a regulator of the NF-kB pathway. Biochem Biophys Res Commun 2002; 295: 1068-1076.
28. Schwende H, Fitzke E, Ambs P, Dieter P: Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25- dihydroxyvitamin D3. J Leukoc Biol 1996; 59:555-561.
29. Baltathakis I, Alcantara O, Boldt DH: Expression of different NF-kB pathway genes in dendritic cells (DCs) or macrophages assessed by gene expression profiling. J Cell Biochem 2001; 83: 281-290.
30. Krug A, Towarowski A, Britsch S, Rothenfusser S, Hornung V, Bals R, Giese T, Engelmann H, Endres S, Krieg AM, Hartmann G: Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur J Immunol 2001; 31: 3026-3037.
31. Rutz M, Metzger J, Gellert T, Luppa P, Lip-ford GB, Wagner H, Bauer S: Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur J Immunol 2004; 34: 2541-2550.
32. Sanjuan MA, Rao N, Lai KTA, Gu Y, Sun S, Fuchs A, Fung-Leung WP, Colonna M, Karlsson L: CpG-induced tyrosine phosphorylation occurs via a TLR9-independent mechanism and is required for cytokine secretion. J Cell Biol 2006; 172:1057-1068.
33. Lee J, Chuang TH, Redecke V, She L, Pitha PM, Carson DA, Raz E, Cottam HB: Molecular basis for the immunostimulatory activity of guanine nucleoside analogs: activation of Toll-like receptor 7. Proc Natl Acad Sci USA 2003; 100:6646-6651.
34. Tabeta K, Georgel P, Janssen E, Du X, Hoebe K, Crozat K, Mudd S, Shamel L, Sovath S, Goode J, Alexopoulou L, Flavell RA, Beutler B: Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci USA 2004; 101:3516-3521.
35. Fremond CM, Yeremeev V, Nicolle DM, Jacobs M, Quesniaux VF, Ryffel B: Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J Clin Invest 2004; 114: 1790-1799.
36. Zarember KA, Godowski PJ: Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 2002; 168:554-561.
37. Suzuki K, Suda T, Naito T, Ide K, Chida K, Nakamura H: Impaired Toll-like receptor 9 expression in alveolar macrophages with no sensitivity to CpG DNA. Am J Respir Crit Care Med 2005; 171:707-713.
38. Maris NA, Dessing MC, de Vos AF, Bresser P, van der Zee JS, Jansen HM, Spek CA, van der Poll T: Toll-like receptor mRNA levels in alveolar macrophages after inhalation of endotoxin. Eur Respir J 2006; 28:622-626.
39. Eaton-Bassiri A, Dillon SB, Cunningham M, Rycyzyn MA, Mills J, Sarisky RT, Mbow ML: Toll-like receptor 9 can be expressed at the cell surface of distinct populations of tonsils and human peripheral blood mononuclear cells. Infect Immun 2004; 72: 7202-7211.
40. Kuo CC, Kuo CW, Liang CM, Liang SM: A transcriptomic and proteomic analysis of the effect of CpG-ODN on human THP-1 monocytic leukemia cells. Proteomics 2005; 5: 894-906.
41. Wang JP, Hayashi T, Datta SK, Kornbluth RS, Raz E, Guiney DG: CpG oligonucleotides partially inhibit growth of Mycobacterium tuberculosis, but not Salmonella or Listeria, in human monocyte-derived macrophages. FEMS Immunol Med Microbiol 2005; 45: 303-310.
42. Roberts TL, Sweet MJ, Hume DA, Stacey KJ: Cutting edge: species-specific TLR9-mediated recognition of CpG and non-CpG phosphorothioate-modified oligonucleotides. J Immunol 2005; 174 : 605-608.
43. Wu CC, Lee J, Raz E, Corr M, Carson DA: Necessity of oligonucleotide aggregation for Toll-like receptor 9 activation. J Biol Chem 2004; 279: 33071-33078.
44. Crozat K, Beutler B: TLR7: a new sensor of viral infection. Proc Natl Acad Sci USA 2004; 101: 6835-6836.
45. Reiling N, Holscher C, Fehrenbach A, Kroger S, Kirschning CJ, Goyert S, Ehlers S: Cutting edge: Toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol 2002; 169:3480-3484.
46. Kamath AB, Alt J, Debbabi H, Behar SM: Toll-like receptor 4-defective C3h/HeJ mice are not more susceptible than other C3H substrains to infection with Mycobacterium tuberculosis. Infect Immun 2003; 71: 4112-4118.
47. Sugawara I, Yamada H, Li C, Mizuno S, Takeuchi O, Akira S: Mycobacterial infection in tlr2 and tlr6 knockout mice. Microbiol Immunol 2003; 47: 327-336.
48. Falcone V, Bassey EB, Toniolo A, Conaldi PG, Collins FM: Differential release of tumor necrosis factor-α from murine peritoneal macrophages stimulated with virulent and avirulent species of mycobacteria. FEMS Immunol Med Microbiol 1994; 8:225-232.
49. Lee KW, Jung J, Lee Y, Kim TY, Choi SY, Park J, Kim DS, Kwon HJ: Immunostimulatory oligodeoxynucleotide isolated from genome wide screening of Mycobacterium bovis chromosomal DNA. Mol Immunol 2006; 43: 2107-2118.
50. Baess I, Mansa B: Determination of genome size and base ratio on deoxyribonucleic acid from mycobacteria. Acta Pathol Microbiol Scand 1978; 86B:309-312.
51. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett J, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG: The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 2003; 10 0 : 7877-7882.
52. Srivastava R, Gopinathan KP, Ramakrish-nan T: Deoxyribonucleic acid methylation in mycobacteria. J Bacteriol 1981; 14 8 : 716-719.
53. Hemavathy KC, Nagaraja V: DNA methyla-tion in mycobacteria: absence of methylation at GATC (Dam) and CCA/TGG (Dcm) sequences. FEMS Immunol Med Microbiol 1995; 11:291-296.