The immunophysiological impact of bacterial CpG DNA on the gut

Clinica Chimica Acta

Volumn 364, Issue 1-2, 2006, Pages 1-11

  Watson, James L ^a   McKay, Derek M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Bacterial DNA; GI tract; Intestine; Probiotics; TRL9

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKINE; GAMMA INTERFERON; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 12; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PROBIOTIC AGENT; PROTEIN TOLL LIKE RECEPTOR 11; PROTEIN TOLL LIKE RECEPTOR 12; PROTEIN TOLL LIKE RECEPTOR 13; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

BACTERIAL GENE; CELL ACTIVATION; COMMENSALISM; CPG ISLAND; DNA METHYLATION; ENTERITIS; ENTEROPATHY; EPITHELIUM CELL; GASTROINTESTINAL TRACT; GENE THERAPY; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IMMUNOSTIMULATION; INTESTINE FLORA; MUCOSAL IMMUNITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; CPG ISLANDS; DNA, BACTERIAL; GASTROINTESTINAL TRACT; HUMANS; OLIGODEOXYRIBONUCLEOTIDES; TOLL-LIKE RECEPTOR 9;

BACTERIA (MICROORGANISMS);

EID: 31044439147     PISSN: 00098981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cca.2005.05.017     Document Type: Review

References (86)

1. V. Mai, and J.G. Morris Jr. Colonic bacterial flora: changing understandings in the molecular age J Nutr 134 2004 459 464
2. J.L. Sonnenburg, L.T. Angenent, and J.I. Gordon Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 5 2004 569 573
3. D. Palestrant, Z.E. Holzknecht, B.H. Collins, W. Parker, S.E. Miller, and R.R. Bollinger Microbial biofilms in the gut: visualization by electron microscopy and by acridine orange staining Ultrastruct Pathol 28 2004 23 27
4. D.L. Topping, and P.M. Clifton Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides Physiol Rev 81 2001 1031 1064
5. G. Bouma, and W. Strober The immunological and genetic basis of inflammatory bowel disease Nat Rev Immunol 3 2003 521 533
6. J.L. Madara, and J. Stafford Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers J Clin Invest 83 1989 724 727
7. D.M. McKay, and P.K. Singh Superantigen activation of immune cells evokes epithelial (T84) transport and barrier abnormalities via IFN-gamma and TNF alpha: inhibition of increased permeability, but not diminished secretory responses by TGF-beta2 J Immunol 159 1997 2382 2390
8. L. Ferrier, L. Mazelin, and N. Cenac Stress-induced disruption of colonic epithelial barrier: role of interferon-gamma and myosin light chain kinase in mice Gastroenterology 125 2003 795 804
9. C. Nagler-Anderson Man the barrier! Strategic defences in the intestinal mucosa Nat Rev Immunol 1 2001 59 67
10. P.B. Ernst, F. Song, and G.R. Klimpel Regulation of the mucosal immune response Am J Trop Med Hyg 60 1999 2 9
11. A.J. Macpherson, and T. Uhr Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria Science 303 2004 1662 1665
12. P. Sansonetti Phagocytosis of bacterial pathogens: implications in the host response Semin Immunol 13 2001 381 390
13. A. Nazli, P.C. Yang, and J. Jury Epithelia under metabolic stress perceive commensal bacteria as a threat Am J Pathol 164 2004 947 957
14. C. Mottet, H.H. Uhlig, and F. Powrie Cutting edge: cure of colitis by CD4 + CD25 + regulatory T cells J Immunol 170 2003 3939 3943
15. A. Didierlaurent, J.C. Sirard, J.P. Kraehenbuhl, and M.R. Neutra How the gut senses its content Cell Microbiol 4 2002 61 72
16. S. Akira, and K. Takeda Toll-like receptor signalling Nat Rev Immunol 4 2004 499 511
17. A.M. Krieg CpG motifs in bacterial DNA and their immune effects Annu Rev Immunol 20 2002 709 760
18. A.M. Krieg, A.K. Yi, and S. Matson CpG motifs in bacterial DNA trigger direct B-cell activation Nature 374 1995 546 549
19. S. Sivori, M. Falco, and C.M. Della CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells Proc Natl Acad Sci U S A 101 2004 10116 10121
20. J. Vollmer, R. Weeratna, and P. Payette Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities Eur J Immunol 34 2004 251 262
21. A.M. Krieg, T. Wu, and R. Weeratna Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs Proc Natl Acad Sci U S A 95 1998 12631 12636
22. P. Lenert, W. Rasmussen, R.F. Ashman, and Z.K. Ballas Structural characterization of the inhibitory DNA motif for the type A (D)-CpG-induced cytokine secretion and NK-cell lytic activity in mouse spleen cells DNA Cell Biol 22 2003 621 631
23. J. Vollmer, R.D. Weeratna, and M. Jurk Oligodeoxynucleotides lacking CpG dinucleotides mediate Toll-like receptor 9 dependent T helper type 2 biased immune stimulation Immunology 113 2004 212 223
24. H. Hemmi, O. Takeuchi, and T. Kawai A Toll-like receptor recognizes bacterial DNA Nature 408 2000 740 745
25. B. Lemaitre, E. Nicolas, L. Michaut, J.M. Reichhart, and J.A. Hoffmann The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults Cell 86 1996 973 983
26. K. Tabeta, P. Georgel, and E. Janssen Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection Proc Natl Acad Sci U S A 101 2004 3516 3521
27. S. Bauer, C.J. Kirschning, and H. Hacker Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition Proc Natl Acad Sci U S A 98 2001 9237 9242
28. T.H. Chuang, J. Lee, L. Kline, J.C. Mathison, and R.J. Ulevitch Toll-like receptor 9 mediates CpG-DNA signaling J Leukoc Biol 71 2002 538 544
29. F. Takeshita, C.A. Leifer, and I. Gursel Cutting edge: role of Toll-like receptor 9 in CpG DNA-induced activation of human cells J Immunol 167 2001 3555 3558
30. J. Lund, A. Sato, S. Akira, R. Medzhitov, and A. Iwasaki Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells J Exp Med 198 2003 513 520
31. S. Pichyangkul, K. Yongvanitchit, and U. Kum-arb Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway J Immunol 172 2004 4926 4933
32. C. Coban, K.J. Ishii, and T. Kawai Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin J Exp Med 201 2005 19 25
33. E.A. Moseman, X. Liang, and A.J. Dawson Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4 + CD25 + regulatory T cells J Immunol 173 2004 4433 4442
34. K. Katakura, J. Lee, D. Rachmilewitz, G. Li, L. Eckmann, and E. Raz Toll-like receptor 9-induced type I IFN protects mice from experimental colitis J Clin Invest 115 2005 695 702
35. P. Ahmad-Nejad, H. Hacker, M. Rutz, S. Bauer, R.M. Vabulas, and H. Wagner Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments Eur J Immunol 32 2002 1958 1968
36. T. Nishiya, and A.L. DeFranco Ligand-regulated chimeric receptor approach reveals distinctive subcellular localization and signaling properties of the Toll-like receptors J Biol Chem 279 2004 19008 19017
37. E. Latz, A. Schoenemeyer, and A. Visintin TLR9 signals after translocating from the ER to CpG DNA in the lysosome Nat Immunol 5 2004 190 198
38. C.A. Leifer, M.N. Kennedy, A. Mazzoni, C. Lee, M.J. Kruhlak, and D.M. Segal TLR9 is localized in the endoplasmic reticulum prior to stimulation J Immunol 173 2004 1179 1183
39. M. Schnare, A.C. Holt, K. Takeda, S. Akira, and R. Medzhitov Recognition of CpG DNA is mediated by signaling pathways dependent on the adaptor protein MyD88 Curr Biol 10 2000 1139 1142
40. M.A. Lomaga, W.C. Yeh, and I. Sarosi TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling Genes Dev 13 1999 1015 1024
41. N. Suzuki, S. Suzuki, and G.S. Duncan Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4 Nature 416 2002 750 756
42. S. Uematsu, S. Sato, and M. Yamamoto Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7-and TLR9-mediated interferon-{alpha} induction J Exp Med 201 2005 915 923
43. J.J. Gao, V. Diesl, and T. Wittmann Regulation of gene expression in mouse macrophages stimulated with bacterial CpG-DNA and lipopolysaccharide J Leukoc Biol 72 2002 1234 1245
44. T. Kawai, S. Sato, and K.J. Ishii Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6 Nat Immunol 5 2004 1061 1068
45. K. Honda, H. Yanai, and T. Mizutani Role of a transductional- transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling Proc Natl Acad Sci U S A 101 2004 15416 15421
46. L.A. O'Neill, K.A. Fitzgerald, and A.G. Bowie The Toll-IL-1 receptor adaptor family grows to five members Trends Immunol 24 2003 286 290
47. E. Bourke, D. Bosisio, J. Golay, N. Polentarutti, and A. Mantovani The Toll-like receptor repertoire of human B lymphocytes: inducible and selective expression of TLR9 and TLR10 in normal and transformed cells Blood 102 2003 956 963
48. M. Akhtar, J.L. Watson, A. Nazli, and D.M. McKay Bacterial DNA evokes epithelial IL-8 production by a MAPK-dependent, NF-kappaB-independent pathway FASEB J 17 2003 1319 1321
49. A. Krug, A. Towarowski, and S. Britsch 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 31 2001 3026 3037
50. J.M. Otte, E. Cario, and D.K. Podolsky Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells Gastroenterology 126 2004 1054 1070
51. C. Rumio, D. Besusso, and M. Palazzo Degranulation of paneth cells via Toll-like receptor 9 Am J Pathol 165 2004 373 381
52. T. Kawahara, Y. Kuwano, and S. Teshima-Kondo Toll-like receptor 4 regulates gastric pit cell responses to Helicobacter pylori infection J Med Invest 48 2001 190 197
53. H. Jijon, J. Backer, and H. Diaz DNA from probiotic bacteria modulates murine and human epithelial and immune function Gastroenterology 126 2004 1358 1373
54. D.J. Philpott, D.M. McKay, P.M. Sherman, and M.H. Perdue Infection of T84 cells with enteropathogenic Escherichia coli alters barrier and transport functions Am J Physiol 270 1996 G634 G645
55. D.J. Philpott, D.M. McKay, W. Mak, M.H. Perdue, and P.M. Sherman Signal transduction pathways involved in enterohemorrhagic Escherichia coli-induced alterations in T84 epithelial permeability Infect Immun 66 1998 1680 1687
56. K. Madsen, A. Cornish, and P. Soper Probiotic bacteria enhance murine and human intestinal epithelial barrier function Gastroenterology 121 2001 580 591
57. C.L. Wells, R.P. Jechorek, S.B. Olmsted, and S.L. Erlandsen Effect of LPS on epithelial integrity and bacterial uptake in the polarized human enterocyte-like cell line Caco-2 Circ Shock 40 1993 276 288
58. M.T. Abreu, P. Vora, E. Faure, L.S. Thomas, E.T. Arnold, and M. Arditi Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide J Immunol 167 2001 1609 1616
59. M.T. Abreu, E.T. Arnold, and L.S. Thomas TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells J Biol Chem 277 2002 20431 20437
60. C.C. Schuerer-Maly, L. Eckmann, M.F. Kagnoff, M.T. Falco, and F.E. Maly Colonic epithelial cell lines as a source of interleukin-8: stimulation by inflammatory cytokines and bacterial lipopolysaccharide Immunology 81 1994 85 91
61. M.J. Sweet, K.J. Stacey, D.K. Kakuda, D. Markovich, and D.A. Hume IFN-gamma primes macrophage responses to bacterial DNA J Interferon Cytokine Res 18 1998 263 271
62. M. Uchijima, T. Nagata, T. Aoshi, and Y. Koide IFN-gamma overcomes low responsiveness of myeloid dendritic cells to CpG DNA Immunol Cell Biol 83 2005 92 95
63. E. Cario, G. Gerken, and D.K. Podolsky Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C Gastroenterology 127 2004 224 238
64. S. Rakoff-Nahoum, J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis Cell 118 2004 229 241
65. F. Jugde, C. Boissier, and B. Birebent Stimulation of peripheral blood and intestinal mucosa cells by synthetic CpG oligodeoxynucleotides Hum Immunol 65 2004 218 230
66. R.K. Ikeda, M. Miller, and J. Nayar Accumulation of peribronchial mast cells in a mouse model of ovalbumin allergen induced chronic airway inflammation: modulation by immunostimulatory DNA sequences J Immunol 171 2003 4860 4867
67. F.G. Zhu, and J.S. Marshall CpG-containing oligodeoxynucleotides induce TNF-alpha and IL-6 production but not degranulation from murine bone marrow-derived mast cells J Leukoc Biol 69 2001 253 262
68. H. Matsushima, N. Yamada, H. Matsue, and S. Shimada TLR3-, TLR7-, and TLR9-mediated production of proinflammatory cytokines and chemokines from murine connective tissue type skin-derived mast cells but not from bone marrow-derived mast cells J Immunol 173 2004 531 541
69. N.H. Salzman, D. Ghosh, K.M. Huttner, Y. Paterson, and C.L. Bevins Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin Nature 422 2003 522 526
70. I. Hussain, and J.N. Kline DNA, the immune system, and atopic disease J Investig Dermatol Symp Proc 9 2004 23 28
71. D. Rachmilewitz, F. Karmeli, and K. Takabayashi Immunostimulatory DNA ameliorates experimental and spontaneous murine colitis Gastroenterology 122 2002 1428 1441
72. F. Obermeier, N. Dunger, L. Deml, H. Herfarth, J. Scholmerich, and W. Falk CpG motifs of bacterial DNA exacerbate colitis of dextran sulfate sodium-treated mice Eur J Immunol 32 2002 2084 2092
73. F. Obermeier, N. Dunger, and U.G. Strauch Contrasting activity of cytosin-guanosin dinucleotide oligonucleotides in mice with experimental colitis Clin Exp Immunol 134 2003 217 224
74. K. Hatakka, J. Martio, and M. Korpela Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis-a pilot study Scand J Rheumatol 32 2003 211 215
75. B. Sheil, J. McCarthy, and L. O'Mahony Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis Gut 53 2004 694 700
76. R.B. Sartor Probiotic therapy of intestinal inflammation and infections Curr Opin Gastroenterol 21 2005 44 50
77. D. Rachmilewitz, K. Katakura, and F. Karmeli Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis Gastroenterology 126 2004 520 528
78. E.O. Petrof, K. Kojima, and M.J. Ropeleski Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition Gastroenterology 127 2004 1474 1487
79. D.W. Smith, and C. Nagler-Anderson Preventing intolerance: the induction of nonresponsiveness to dietary and microbial antigens in the intestinal mucosa J Immunol 174 2005 3851 3857
80. A.M. Mowat Anatomical basis of tolerance and immunity to intestinal antigens Nat Rev Immunol 3 2003 331 341
81. S.A. Halperin, G. Van Nest, B. Smith, S. Abtahi, H. Whiley, and J.J. Eiden A phase I study of the safety and immunogenicity of recombinant hepatitis B surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide adjuvant Vaccine 21 2003 2461 2467
82. C.L. Cooper, H.L. Davis, and M.L. Morris CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B HBV vaccine in healthy adults: a double-blind phase I/II study J Clin Immunol 24 2004 693 701
83. C.L. Cooper, H.L. Davis, and M.L. Morris Safety and immunogenicity of CPG 7909 injection as an adjuvant to Fluarix influenza vaccine Vaccine 22 2004 3136 3143
84. D. Wang, E.R. Kandimalla, D. Yu, J.X. Tang, and S. Agrawal Oral administration of second-generation immunomodulatory oligonucleotides induces mucosal Th1 immune responses and adjuvant activity Vaccine 23 2005 2614 2622
85. M. Heikenwalder, M. Polymenidou, and T. Junt Lymphoid follicle destruction and immunosuppression after repeated CpG oligodeoxynucleotide administration Nat Med 10 2004 187 192
86. L.H. Travassos, S.E. Girardin, and D.J. Philpott Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition EMBO Rep 5 2004 1000 1006