Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 432785, 16 pages
http://dx.doi.org/10.1155/2014/432785
Review Article

Collaborative Action of Toll-Like and Nod-Like Receptors as Modulators of the Inflammatory Response to Pathogenic Bacteria

Molecular Immunology and Signal Transduction Laboratory, Centro Multidisciplinario de Estudios en Biotecnología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Michoacana de San Nicolás de Hidalgo, Km. 9.5 s/n Carretera Morelia-Zinapécuaro, La Palma, Tarímbaro, C.P. 58893 Morelia, MICH, Mexico

Received 14 April 2014; Revised 11 June 2014; Accepted 27 June 2014; Published 1 December 2014

Academic Editor: Marisa I. Gómez

Copyright © 2014 Javier Oviedo-Boyso et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Kumar, T. Kawai, and S. Akira, “Pathogen recognition in the innate immune response,” Biochemical Journal, vol. 420, no. 1, pp. 1–16, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. J. S. Ayres and D. S. Schneider, “Tolerance of infections,” Annual Review of Immunology, vol. 30, pp. 271–294, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Kumar, T. Kawai, and S. Akira, “Toll-like receptors and innate immunity,” Biochemical and Biophysical Research Communications, vol. 388, no. 4, pp. 621–625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Kumar, H. Ingle, D. V. R. Prasad, and H. Kumar, “Recognition of bacterial infection by innate immune sensors,” Critical Reviews in Microbiology, vol. 39, no. 3, pp. 229–246, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. O. Takeuchi, T. Kawai, P. F. Mühlradt et al., “Discrimination of bacterial lipoproteins by Toll-like recepttor 6,” International Immunology, vol. 13, no. 7, pp. 933–940, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. U. Zähringer, B. Lindner, S. Inamura, H. Heine, and C. Alexander, “TLR2 - promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity,” Immunobiology, vol. 213, no. 3-4, pp. 205–224, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Krishna, A. Ray, S. K. Dubey et al., “Lipoglycans contribute to innate immune detection of mycobacteria,” PLoS ONE, vol. 6, no. 12, Article ID e28476, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Blanc, R. Castanier, A. K. Mishra et al., “Gram-positive bacterial lipoglycans based on a glycosylated diacylglycerol lipid anchor are microbe-associated molecular patterns recognized by TLR2,” PLoS ONE, vol. 8, no. 11, Article ID e81593, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Akira, S. Uematsu, and O. Takeuchi, “Pathogen recognition and innate immunity,” Cell, vol. 124, no. 4, pp. 783–801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Medzhitov, “TLR-mediated innate immune recognition,” Seminars in Immunology, vol. 19, no. 1, pp. 1–2, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Kawai and S. Akira, “The role of pattern-recognition receptors in innate immunity: update on toll-like receptors,” Nature Immunology, vol. 11, no. 5, pp. 373–384, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. M. A. Anwar, S. Basith, and S. Choi, “Negative regulatory approaches to the attenuation of Toll-like receptor signaling,” Experimental and Molecular Medicine, vol. 45, pp. 1–14, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Langefeld, M. Walid, R. Ghai, and T. Chakraborty, “Toll-like receptors and NOD-like receptors: domain architecture and cellular signalling,” Advances in Experimental Medicine and Biology, vol. 653, pp. 48–57, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Richez, P. Blanco, I. Rifkin, J.-F. Moreau, and T. Schaeverbeke, “Role for toll-like receptors in autoimmune disease: the example of systemic lupus erythematosus,” Joint Bone Spine, vol. 78, no. 2, pp. 124–130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Xi, F. Shao, X. Y. Bai, G. Cai, Y. Lv, and X. Chen, “Changes in the expression of the Toll-like receptor system in the aging rat kidneys,” PLoS One, vol. 9, no. 5, Article ID e96351, 2014. View at Google Scholar
  16. X. He, Z. Jing, and G. Cheng, “MicroRNAs: new regulators of toll-like receptor signalling pathways,” BioMed Research International, vol. 2014, Article ID 945169, 14 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. A. R. Jayakumar, X. Y. Tong, K. M. Curtis, R. Ruiz-Cordero, M. T. Abreu, and M. D. Norenberg, “Increased Toll-like receptor 4 in cerebral endothelial cell contributes to the astrocyte swelling and brain edema in acute hepatic encephalopathy,” Journal of Neurochemistry, vol. 128, no. 6, pp. 890–903, 2014. View at Publisher · View at Google Scholar
  18. A. Klonowska-Szymczyk, A. Wolska, T. Robak, B. Cebula-Obrzut, P. Smolewski, and E. Robak, “Expression of toll-like receptors 3, 7, and 9 in peripheral blood mononuclear cells from patients with systemic lupus erythematosus,” Mediators of Inflammation, vol. 2014, Article ID 381418, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. L. A. J. O'Neill, E. J. Hennessy, A. E. Parker, and L. A. J. O'Neill, “Targeting toll-like receptors: emerging therapeutics?” Nature Reviews Drug Discovery, vol. 9, no. 4, pp. 293–307, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. M. T. Abreu, “Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function,” Nature Reviews Immunology, vol. 10, no. 2, pp. 131–144, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Ioannidis, F. Ye, B. McNally, M. Willette, and E. Flaño, “Toll-like receptor expression and induction of type I and type III interferons in primary airway epithelial cells,” Journal of Virology, vol. 87, no. 6, pp. 3261–3270, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Pasparakis, I. Haase, and F. O. Nestle, “Mechanisms regulating skin immunity and inflammation,” Nature Reviews Immunology, vol. 14, no. 5, pp. 289–301, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. M. J. Mulla, K. Myrtolli, S. Tadesse et al., “Cutting-edge report: TLR10 plays a role in mediating bacterial peptidoglycan-induced trophoblast apoptosis,” The American Journal of Reproductive Immunology, vol. 69, no. 5, pp. 449–453, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Regan, K. Nally, R. Carmody et al., “Identification of TLR10 as a key mediator of the inflammatory response to Listeria monocytogenes in intestinal epithelial cells and macrophages,” The Journal of Immunology, vol. 191, no. 12, pp. 6084–6092, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. S. M. Y. Lee, K.-H. Kok, M. Jaume et al., “Toll-like receptor 10 is involved in induction of innate immune responses to influenza virus infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 10, pp. 3793–3798, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. W. A. Andrade, M. D. C. Souza, E. Ramos-Martinez et al., “Combined action of nucleic acid-sensing toll-like receptors and TLR11/TLR12 heterodimers imparts resistance to toxoplasma gondii in mice,” Cell Host and Microbe, vol. 13, no. 1, pp. 42–53, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. J. C. Roach, G. Glusman, L. Rowen et al., “The evolution of vertebrate Toll-like receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 27, pp. 9577–9582, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Cario and D. K. Podolsky, “Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease,” Infection and Immunity, vol. 68, no. 12, pp. 7010–7017, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. A. T. Gewirtz, T. A. Navas, S. Lyons, P. J. Godowski, and J. L. Madara, “Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression,” The Journal of Immunology, vol. 167, no. 4, pp. 1882–1885, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Otte, E. Cario, and D. K. Podolsky, “Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells,” Gastroenterology, vol. 126, no. 4, pp. 1054–1070, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Shang, M. Fukata, N. Thirunarayanan et al., “TLR signaling in small intestinal epithelium promotes B cells recruitment and IgA production in lamina propria,” Gastroenterology, vol. 135, no. 2, pp. 529–538, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. E. C. Lavelle, C. Murphy, L. A. J. O'Neill, and E. M. Creagh, “The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis,” Mucosal Immunology, vol. 3, no. 1, pp. 17–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. Q. Sha, A. Q. Truong-Tran, J. R. Plitt, L. A. Beck, and R. P. Schleimer, “Activation of airway epithelial cells by toll-like receptor agonists,” The American Journal of Respiratory Cell and Molecular Biology, vol. 31, no. 3, pp. 358–364, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. A. K. Mayer, M. Muehmer, J. Mages et al., “Differential recognition of TLR-dependent microbial ligands in human bronchial epithelial cells,” The Journal of Immunology, vol. 178, no. 5, pp. 3134–3142, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. J. L. Koff, M. X. G. Shao, I. F. Ueki, and J. A. Nadel, “Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 294, no. 6, pp. L1068–L1075, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Guillott, S. Medjane, K. Le-Barillec et al., “Response of human pulmonary epithelial cells to lipopolysaccharide involves toll-like receptor 4 (TLR4)-dependent signaling pathways: evidence for an intracellular compartmentalization of TLR4,” Journal of Biological Chemistry, vol. 279, no. 4, pp. 2712–2718, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Schneberger, S. Caldwell, R. Kanthan, and B. Singh, “Expression of Toll-like receptor 9 in mouse and human lungs,” Journal of Anatomy, vol. 222, no. 5, pp. 495–503, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. N. Iram, M. Mildner, M. Prior et al., “Age-related changes in expression and function of toll-like receptors in human skin,” Development, vol. 139, no. 22, pp. 4210–4219, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. B. S. Baker, J. M. Ovigne, A. V. Powles, S. Corcoran, and L. Fry, “Normal keratinocytes express Toll-like receptors (TLRs) 1, 2 and 5: modulation of TLR expression in chronic plaque psoriasis,” British Journal of Dermatology, vol. 148, no. 4, pp. 670–679, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Pivarcsi, L. Bodai, B. Réthi et al., “Expression and function of Toll-like receptors 2 and 4 in human keratinocytes,” International Immunology, vol. 15, no. 6, pp. 721–730, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Köllisch, B. N. Kalali, V. Voelcker et al., “Various members of the Toll-like receptor family contribute to the innate immune response of human epidermal keratinocytes,” Immunology, vol. 114, no. 4, pp. 531–541, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. X. Dai, K. Sayama, K. Yamasaki et al., “SOCS1-negative feedback of STAT1 activation is a key pathway in the dsRNA-induced innate immune response of human keratinocytes,” Journal of Investigative Dermatology, vol. 126, no. 7, pp. 1574–1581, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. B. N. Kalali, G. Köllisch, J. Mages et al., “Double-stranded RNA induces an antiviral defense status in epidermal keratinocytes through TLR3-, PKR-, and MDA5/RIG-I-mediated differential signaling,” The Journal of Immunology, vol. 181, no. 4, pp. 2694–2704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. M. C. Lebre, A. M. G. Van Der Aar, L. Van Baarsen et al., “Human keratinocytes express functional toll-like receptor 3, 4, 5, and 9,” Journal of Investigative Dermatology, vol. 127, no. 2, pp. 331–341, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. L. S. Miller and R. L. Modlin, “Human keratinocyte Toll-like receptors promote distinct immune responses,” Journal of Investigative Dermatology, vol. 127, no. 2, pp. 262–263, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. J. P.-Y. Ting, R. C. Lovering, E. S. Alnemri et al., “The NLR gene family: a standard nomenclature,” Immunity, vol. 28, no. 3, pp. 285–287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Franchi, J. H. Park, M. H. Shaw et al., “Intracellular NOD-like receptors in innate immunity, infection and disease,” Cellular Microbiology, vol. 10, no. 1, pp. 1–8, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. I. C. Allen, M. A. Scull, C. B. Moore et al., “The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA,” Immunity, vol. 30, no. 4, pp. 556–565, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. A. M. Kvarnhammar, L. Tengroth, M. Adner, and L.-O. Cardell, “Innate immune receptors in human airway smooth muscle cells: activation by TLR1/2, TLR3, TLR4, TLR7 and NOD1 agonists,” PLoS ONE, vol. 8, no. 7, Article ID e68701, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Inohara, M. Chamaillard, C. McDonald, and G. Nuñez, “NOD-LRR proteins: role in host-microbial interactions and inflammatory disease,” Annual Review of Biochemistry, vol. 74, pp. 355–383, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. J. H. Fritz, R. L. Ferrero, D. J. Philpott, and S. E. Girardin, “Nod-like proteins in immunity, inflammation and disease,” Nature Immunology, vol. 7, no. 12, pp. 1250–1257, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. E. M. Creagh and L. A. J. O'Neill, “TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity,” Trends in Immunology, vol. 27, no. 8, pp. 352–357, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Uehara, Y. Fujimoto, K. Fukase, and H. Takada, “Various human epithelial cells express functional Toll-like receptors, NOD1 and NOD2 to produce anti-microbial peptides, but not proinflammatory cytokines,” Molecular Immunology, vol. 44, no. 12, pp. 3100–3111, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Le Bourhis, S. Benko, and S. E. Girardin, “Nod1 and Nod2 in innate immunity and human inflammatory disorders,” Biochemical Society Transactions, vol. 35, no. 6, pp. 1479–1484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. D. J. Philpott, S. Yamaoka, A. Israël, and P. J. Sansonetti, “Invasive Shigella flexneri activates NF-κB through a lipopolysaccharide-dependent innate intracellular response and leads to IL-8 expression in epithelial cells,” Journal of Immunology, vol. 165, no. 2, pp. 903–914, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. S. E. Girardin, R. Tournebize, M. Mavris et al., “CARD4/Nod1 mediates NF-κB and JNK activation by invasive Shigella flexneri,” EMBO Reports, vol. 2, no. 8, pp. 736–742, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. J. G. Kim, S. J. Lee, and M. F. Kagnoff, “Nod1 is an essential signal transducer in intestinal epithelial cells infected with bacteria that avoid recognition by Toll-like receptors,” Infection and Immunity, vol. 72, no. 3, pp. 1487–1495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Opitz, S. Förster, A. C. Hocke et al., “Nod1-mediated endothelial cell activation by Chlamydophila pneumoniae,” Circulation Research, vol. 96, no. 3, pp. 319–326, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Welter-Stahl, D. M. Ojcius, J. Viala et al., “Stimulation of the cytosolic receptor for peptidoglycan, Nod1, by infection with Chlamydia trachomatis or Chlamydia muridarum,” Cellular Microbiology, vol. 8, no. 6, pp. 1047–1057, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Kaparakis, L. Turnbull, L. Carneiro et al., “Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells,” Cellular Microbiology, vol. 12, no. 3, pp. 372–385, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. T. A. Kufer, D. J. Banks, and D. J. Philpott, “Innate immune sensing of microbes by Nod proteins,” Annals of the New York Academy of Sciences, vol. 1072, pp. 19–27, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. S. J. Robertson and S. E. Girardin, “Nod-like receptors in intestinal host defense: controlling pathogens, the microbiota, or both?” Current Opinion in Gastroenterology, vol. 29, no. 1, pp. 15–22, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. S. E. Girardin, I. G. Boneca, J. Viala et al., “Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection,” Journal of Biological Chemistry, vol. 278, no. 11, pp. 8869–8872, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. H. N. Qiu, C. K. Wong, I. M. T. Chu, S. Hu, and C. W. K. Lam, “Muramyl dipeptide mediated activation of human bronchial epithelial cells interacting with basophils: a novel mechanism of airway inflammation,” Clinical and Experimental Immunology, vol. 172, no. 1, pp. 81–94, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Leissinger, R. Kulkarni, R. L. Zemans, G. P. Downey, and S. Jeyaseelan, “Investigating the role of NOD-like receptors in bacterial lung infection,” The American Journal of Respiratory Critical Care Medicine, 2014. View at Publisher · View at Google Scholar
  66. H. Slevogt, J. Seybold, K. N. Tiwari et al., “Moraxella catarrhalis is internalized in respiratory epithelial cells by a trigger-like mechanism and initiates a TLR2- and partly NOD1-dependent inflammatory immune response,” Cellular Microbiology, vol. 9, no. 3, pp. 694–707, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Opitz, A. Püschel, W. Beermann et al., “Listeria monocytogenes activated p38 MAPK and induced IL-8 secretion in a nucleotide-binding oligomerization domain 1-dependent manner in endothelial cells,” The Journal of Immunology, vol. 176, no. 1, pp. 484–490, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. J. L. Barton, T. Berg, L. Didon, and M. Nord, “The pattern recognition receptor Nod1 activates CCAAT/enhancer binding protein β signalling in lung epithelial cells,” European Respiratory Journal, vol. 30, no. 2, pp. 214–222, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Månsson Kvarnhammar, L. Tengroth, M. Adner, and L. O. Cardell, “Innate immune receptors in human airway smooth muscle cells: activation by TLR1/2 TLR3, TLR4, TLR7 and NOD agonists,” PLoS ONE, vol. 8, no. 7, Article ID e68701, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. K. Shimada, S. Chen, P. W. Dempsey et al., “The NOD/RIP2 pathway is essential for host defenses against Chlamydophila pneumoniae lung infection,” PLoS Pathogens, vol. 5, no. 4, Article ID e1000379, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. V. Regueiro, D. Moranta, C. G. Frank et al., “Klebsiella pneumoniae subverts the activation of inflammatory responses in a NOD1-dependent manner,” Cellular Microbiology, vol. 13, no. 1, pp. 135–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. W. R. Berrington, R. Iyer, R. D. Wells, K. D. Smith, S. J. Skerrett, and T. R. Hawn, “NOD1 and NOD2 regulation of pulmonary innate immunity to Legionella pneumophila,” European Journal of Immunology, vol. 40, no. 12, pp. 3519–3527, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. L. H. Travassos, L. A. M. Carneiro, S. E. Girardin et al., “Nod1 participates in the innate immune response to Pseudomonas aeruginosa,” The Journal of Biological Chemistry, vol. 280, no. 44, pp. 36714–36718, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. Y.-G. Kim, J.-H. Park, S. Daignault, K. Fukase, and G. Núñez, “Cross-tolerization between Nod1 and Nod2 signaling results in reduced refractoriness to bacterial infection in Nod2-deficient macrophages,” Journal of Immunology, vol. 181, no. 6, pp. 4340–4346, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. B. Opitz, A. Püschel, B. Schmeck et al., “Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae,” Journal of Biological Chemistry, vol. 279, no. 35, pp. 36426–36432, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Theivanthiran, S. Batra, G. Balamayooran et al., “NOD2 signaling contributes to host defense in the lungs against Escherichia coli infection,” Infection and Immunity, vol. 80, no. 7, pp. 2558–2569, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. G. Ferwerda, S. E. Girardin, B.-J. Kullberg et al., “NOD2 and toll-like receptors are nonredundant recognition systems of Mycobacterium tuberculosis,” PLoS Pathogens, vol. 1, no. 3, article e34, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. K. M. Davis, S. Nakamura, and J. N. Weiser, “Nod2 sensing of lysozyme-digested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice,” The Journal of Clinical Investigation, vol. 121, no. 9, pp. 3666–3676, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Kapetanovic, G. Jouvion, C. Fitting et al., “Contribution of NOD2 to lung inflammation during Staphylococcus aureus-induced pneumonia,” Microbes and Infection, vol. 12, no. 10, pp. 759–767, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. C. Chaput, L. E. Sander, N. Suttorp, and B. Opitz, “NOD-like receptors in lung diseases,” Frontiers in Immunology, vol. 4, article 393, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. F. Bauernfeind and V. Hornung, “Of inflammasomes and pathogens—sensing of microbes by the inflammasome,” EMBO Molecular Medicine, vol. 5, no. 6, pp. 814–826, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. J. A. Hirota, S. A. Hirota, S. M. Warner et al., “The airway epithelium nucleotide-binding domain and leucine-rich repeat protein 3 inflammasome is activated by urban particulate matter,” Journal of Allergy and Clinical Immunology, vol. 129, no. 4, pp. 1116.e6–1125.e6, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. E. S. Alnemri, “Sensing cytoplasmic danger signals by the inflammasome,” Journal of Clinical Immunology, vol. 30, no. 4, pp. 512–519, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Kim, F. Bauernfeind, A. Ablasser et al., “Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome,” European Journal of Immunology, vol. 40, no. 6, pp. 1545–1551, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Meixenberger, F. Pache, J. Eitel et al., “Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1β, depending on listeriolysin O and NLRP3,” Journal of Immunology, vol. 184, no. 2, pp. 922–930, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. R. Muñoz-Planillo, L. Franchi, L. S. Miller, and G. Núñez, “A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome,” The Journal of Immunology, vol. 183, no. 6, pp. 3942–3948, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Eitel, K. Meixenberger, C. van Laak et al., “Rac1 regulates the NLRP3 inflammasome which mediates IL-1beta production in Chlamydophila pneumoniae infected human mononuclear cells,” PLoS ONE, vol. 7, no. 1, Article ID e30379, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. F. Carlsson, J. Kim, C. Dumitru et al., “Host-detrimental role of Esx-1-mediated inflammasome activation in Mycobacterial infection,” PLoS Pathogens, vol. 6, no. 5, pp. 1–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. C. L. Case, L. J. Kohler, J. B. Lima et al., “Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 5, pp. 1851–1856, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. I. C. Allen, M. A. Scull, C. B. Moore et al., “The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA,” Immunity, vol. 30, no. 4, pp. 556–565, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Pothlichet, I. Meunier, B. K. Davis et al., “Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells,” PLoS Pathogens, vol. 9, no. 4, Article ID e1003256, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. E. Park, H. S. Na, Y.-R. Song, S. Y. Shin, Y.-M. Kim, and J. Chung, “Activation of NLRP3 and AIM2 inflammasomes by Porphyromonas gingivalis infection,” Infection and Immunity, vol. 82, no. 1, pp. 112–123, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. N. Saïd-Sadier, E. Padilla, G. Langsley, and D. M. Ojcius, “Aspergillus fumigatus stimulates the NLRP3 inflammasome through a pathway requiring ROS production and the syk tyrosine kinase,” PLoS ONE, vol. 5, no. 4, Article ID e10008, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. A. J. McCoy, Y. Koizumi, N. Higa, and T. Suzuki, “Differential regulation of caspase-1 activation via NLRP3/NLRC4 inflammasomes mediated by aerolysin and type III secretion system during Aeromonas veronii infection,” The Journal of Immunology, vol. 185, no. 11, pp. 7077–7084, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. F. Martinon, K. Burns, and J. Tschopp, “The Inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-β,” Molecular Cell, vol. 10, no. 2, pp. 417–426, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. J. A. Kummer, R. Broekhuizen, H. Everett et al., “Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response,” Journal of Histochemistry and Cytochemistry, vol. 55, no. 5, pp. 443–452, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. E. D. Boyden and W. F. Dietrich, “Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin,” Nature Genetics, vol. 38, no. 2, pp. 240–244, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. S. E. Ewald, J. Chavarria-Smith, and J. C. Boothroyd, “NLRP1 is an inflammasome sensor for Toxoplasma gondii,” Infection and Immunity, vol. 82, no. 1, pp. 460–468, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. A. D. Radian, L. de Almeida, A. Dorfleutner, and C. Stehlik, “NLRP7 and related inflammasome activating pattern recognition receptors and their function in host defense and disease,” Microbes and Infection, vol. 15, no. 8-9, pp. 630–639, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Khare, A. Dorfleutner, N. B. Bryan et al., “An NLRP7-containing inflammasome mediates recognition of microbial lipopeptides in human macrophages,” Immunity, vol. 36, no. 3, pp. 464–476, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Cui, Y. Li, L. Zhu et al., “NLRP4 negatively regulates type I interferon signaling by targeting the kinase TBK1 for degradation via the ubiquitin ligase DTX4,” Nature Immunology, vol. 13, no. 4, pp. 387–395, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. L. Fiorentino, C. Stehlik, V. Oliveira, M. E. Ariza, A. Godzik, and J. C. Reed, “A novel PAAD-containing protein that modulates NF-κB induction by cytokines tumor necrosis factor-α and interleukin-1β,” The Journal of Biological Chemistry, vol. 277, no. 38, pp. 35333–35340, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. N. Jounai, K. Kobiyama, M. Shiina, K. Ogata, K. J. Ishii, and F. Takeshita, “NLRP4 negatively regulates autophagic processes through an association with Beclin1,” The Journal of Immunology, vol. 186, no. 3, pp. 1646–1655, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. P. K. Anand, R. K. S. Malireddi, J. R. Lukens et al., “NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens,” Nature, vol. 488, no. 7411, pp. 389–393, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. P. K. Anand and T.-D. Kanneganti, “NLRP6 in infection and inflammation,” Microbes and Infection, vol. 15, no. 10-11, pp. 661–668, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. J. C. Arthur, J. D. Lich, Z. Ye et al., “NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity,” Journal of Immunology, vol. 185, no. 8, pp. 4515–4519, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. C. A. Lord, D. Savitsky, R. Sitcheran et al., “Blimp-1/PRDM1 mediates transcriptional suppression of the NLR gene NLRP12/monarch-1,” The Journal of Immunology, vol. 182, no. 5, pp. 2948–2958, 2009. View at Publisher · View at Google Scholar · View at Scopus
  108. I. C. Allen, E. McElvania-TeKippe, J. E. Wilson et al., “Characterization of NLRP12 during the in vivo host immune response to Klebsiella pneumoniae and mycobacterium tuberculosis,” PLoS ONE, vol. 8, no. 4, Article ID e60842, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. E. A. Miao, C. M. Alpuche-Aranda, M. Dors et al., “Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf,” Nature Immunology, vol. 7, no. 6, pp. 569–575, 2006. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Lamkanfi and V. M. Dixit, “Inflammasomes: guardians of cytosolic sanctity,” Immunological Reviews, vol. 227, no. 1, pp. 95–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. L. Franchi, R. Muñoz-Planillo, and G. Núñez, “Sensing and reacting to microbes through the inflammasomes,” Nature Immunology, vol. 13, no. 4, pp. 325–332, 2012. View at Publisher · View at Google Scholar · View at Scopus
  112. T. Suzuki, L. Franchi, C. Toma et al., “Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages,” PLoS pathogens, vol. 3, no. 8, article e111, 2007. View at Publisher · View at Google Scholar · View at Scopus
  113. E. A. Miao, D. P. Mao, N. Yudkovsky et al., “Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 7, pp. 3076–3080, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. E. A. Miao and S. E. Warren, “Innate immune detection of bacterial virulence factors via the NLRC4 inflammasome,” Journal of Clinical Immunology, vol. 30, no. 4, pp. 502–506, 2010. View at Publisher · View at Google Scholar · View at Scopus
  115. F. A. Carvalho, I. Nalbantoglu, J. D. Aitken et al., “Cytosolic flagellin receptor NLRC4 protects mice against mucosal and systemic challenges,” Mucosal Immunology, vol. 5, no. 3, pp. 288–298, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. K. Schroder and J. Tschopp, “The inflammasomes,” Cell, vol. 140, no. 6, pp. 821–832, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. V. A. K. Rathinam, Z. Jiang, S. N. Waggoner et al., “The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses,” Nature Immunology, vol. 11, no. 5, pp. 395–402, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. R. J. Dotson, S. M. Rabadi, E. L. Westcott et al., “Repression of inflammasome by Francisella tularensis during early stages of infection,” Journal of Biological Chemistry, vol. 288, no. 33, pp. 23844–23857, 2013. View at Publisher · View at Google Scholar · View at Scopus
  119. K. Belhocine and D. M. Monack, “Francisella infection triggers activation of the AIM2 inflammasome in murine dendritic cells,” Cellular Microbiology, vol. 14, no. 1, pp. 71–80, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. K. Tsuchiya, H. Hara, I. Kawamura et al., “Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes,” Journal of Immunology, vol. 185, no. 2, pp. 1186–1195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. S. E. Warren, A. Armstrong, M. K. Hamilton et al., “cutting edge: Cytosolic bacterial DNA activates the inflammasome via Aim2,” Journal of Immunology, vol. 185, no. 2, pp. 118–121, 2010. View at Publisher · View at Google Scholar · View at Scopus
  122. J. Wu, T. Fernandes-Alnemri, and E. S. Alnemri, “Involvement of the AIM2, NLRC4, and NLRP3 inflammasomes in caspase-1 activation by Listeria monocytogenes,” Journal of Clinical Immunology, vol. 30, no. 5, pp. 693–702, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. H. Saiga, S. Kitada, Y. Shimada et al., “Critical role of AIM2 in Mycobacterium tuberculosis infection,” International Immunology, vol. 24, no. 10, pp. 637–644, 2012. View at Publisher · View at Google Scholar · View at Scopus
  124. Y. Yang, X. Zhou, M. Kouadir et al., “The AIM2 inflammasome is involved in macrophage activation during infectionwith virulent Mycobacterium bovis strain,” The Journal of Infectious Diseases, vol. 208, no. 11, pp. 1849–1858, 2013. View at Publisher · View at Google Scholar · View at Scopus
  125. R. Fang, H. Hara, S. Sakai et al., “Type I interferon signaling regulates activation of the absent in melanoma 2 inflammasome during Streptococcus pneumoniae Infection,” Infection and Immunity, vol. 82, no. 6, pp. 2310–2317, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. R. Hanamsagar, A. Aldrich, and T. Kielian, “Critical role for the AIM2 inflammasome during acute CNS bacterial infection,” Journal of Neurochemistry, vol. 129, no. 4, pp. 704–711, 2014. View at Publisher · View at Google Scholar · View at Scopus
  127. M. C. Chambers and D. S. Schneider, “Balancing resistance and infection tolerance through metabolic means,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 35, pp. 13886–13887, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. R. G. Baker, M. S. Hayden, and S. Ghosh, “NF-κB, inflammation, and metabolic disease,” Cell Metabolism, vol. 13, no. 1, pp. 11–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  129. M. S. Hayden, A. P. West, and S. Ghosh, “NF-κB and the immune response,” Oncogene, vol. 25, no. 51, pp. 6758–6780, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. M. S. Hayden and S. Ghosh, “Shared principles in NF- B signaling,” Cell, vol. 132, no. 3, pp. 344–362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. S. Akira and K. Takeda, “Toll-like receptor signalling,” Nature Reviews Immunology, vol. 4, no. 7, pp. 499–511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  132. T. Kawai and S. Akira, “TLR signaling,” Cell Death and Differentiation, vol. 13, no. 5, pp. 816–825, 2006. View at Publisher · View at Google Scholar · View at Scopus
  133. A. Roeder, C. J. Kirschning, R. A. Rupec, M. Schaller, G. Weindl, and H. C. Korting, “Toll-like receptors as key mediators in innate antifungal immunity,” Medical Mycology, vol. 42, no. 6, pp. 485–498, 2004. View at Publisher · View at Google Scholar · View at Scopus
  134. A. A. Koblansky, D. Jankovic, H. Oh et al., “Recognition of profilin by Toll-like receptor 12 is critical for host resistance to Toxoplasma gondii,” Immunity, vol. 38, no. 1, pp. 119–130, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. K. Takeda and S. Akira, “Toll-like receptors in innate immunity,” International Immunology, vol. 17, no. 1, pp. 1–14, 2005. View at Publisher · View at Google Scholar · View at Scopus
  136. C. A. Janeway Jr. and R. Medzhitov, “Innate immune recognition,” Annual Review of Immunology, vol. 20, pp. 197–216, 2002. View at Publisher · View at Google Scholar · View at Scopus
  137. M. S. Hayden and S. Ghosh, “NF-κB, the first quarter-century: remarkable progress and outstanding questions,” Genes and Development, vol. 26, no. 3, pp. 203–234, 2012. View at Publisher · View at Google Scholar · View at Scopus
  138. T. Kawai and S. Akira, “Toll-like receptor downstream signaling,” Arthritis Research and Therapy, vol. 7, no. 1, pp. 12–19, 2005. View at Publisher · View at Google Scholar · View at Scopus
  139. E. Meylan, K. Burns, K. Hofmann et al., “RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation,” Nature Immunology, vol. 5, no. 5, pp. 503–507, 2004. View at Publisher · View at Google Scholar · View at Scopus
  140. G. Oganesyan, S. K. Saha, B. Guo et al., “Critical role of TRAF3 in the toll-like receptor-dependent and -independent antiviral response,” Nature, vol. 439, no. 7073, pp. 208–211, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. T.-L. Chau, R. Gioia, J.-S. Gatot et al., “Are the IKKs and IKK-related kinases TBK1 and IKK-ε similarly activated?” Trends in Biochemical Sciences, vol. 33, no. 4, pp. 171–180, 2008. View at Publisher · View at Google Scholar · View at Scopus
  142. M. A. Ermolaeva, M.-C. Michallet, N. Papadopoulou et al., “Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses,” Nature Immunology, vol. 9, no. 9, pp. 1037–1046, 2008. View at Publisher · View at Google Scholar · View at Scopus
  143. K. Honda, H. Yanai, H. Negishi et al., “IRF-7 is the master regulator of type-I interferon-dependent immune responses,” Nature, vol. 434, no. 7034, pp. 772–777, 2005. View at Publisher · View at Google Scholar · View at Scopus
  144. B. Barnes, B. Lubyova, and P. M. Pitha, “On the role of IRF in host defense,” Journal of Interferon and Cytokine Research, vol. 22, no. 1, pp. 59–71, 2002. View at Publisher · View at Google Scholar · View at Scopus
  145. C. M. Cham, K. Ko, and T. B. Niewold, “Interferon regulatory factor 5 in the pathogenesis of systemic lupus erythematosus,” Clinical and Developmental Immunology, vol. 2012, Article ID 780436, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  146. C. Bourgeois, O. Majer, I. E. Frohner et al., “Conventional dendritic cells mount a type I IFN response against Candida spp. requiring novel phagosomal TLR7-mediated IFN-β signaling,” The Journal of Immunology, vol. 186, no. 5, pp. 3104–3112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  147. C. Biondo, A. Malara, A. Costa et al., “Recognition of fungal RNA by TLR7 has a nonredundant role in host defense against experimental candidiasis,” European Journal of Immunology, vol. 42, no. 10, pp. 2632–2643, 2012. View at Publisher · View at Google Scholar · View at Scopus
  148. S. E. Girardin, I. G. Boneca, J. Viala et al., “Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection,” The Journal of Biological Chemistry, vol. 278, no. 11, pp. 8869–8872, 2003. View at Publisher · View at Google Scholar · View at Scopus
  149. C.-C. Kuo, A. Lee, and L. A. Campbell, “Cleavage of the N-linked oligosaccharide from the surfaces of Chlamydia species affects attachment and infectivity of the organisms in human epithelial and endothelial cells,” Infection and Immunity, vol. 72, no. 11, pp. 6699–6701, 2004. View at Publisher · View at Google Scholar · View at Scopus
  150. B. Fournier and D. J. Philpott, “Recognition of Staphylococcus aureus by the innate immune system,” Clinical Microbiology Reviews, vol. 18, no. 3, pp. 521–540, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. L. L. Bourhis, S. Benko, and S. E. Girardin, “Nod1 and Nod2 in innate immunity and human inflammatory disorders,” Biochemical Society Transactions, vol. 35, no. 6, pp. 1479–1484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. X. Xie, L. Wang, F. Gong et al., “Intracellular Staphylococcus aureus-induced NF-κB activation and proinflammatory responses of P815 cells are mediated by NOD2,” Journal of Huazhong University of Science and Technology (Medical Sciences), vol. 32, no. 3, pp. 317–323, 2012. View at Publisher · View at Google Scholar · View at Scopus
  153. C. Chaput, L. E. Sander, N. Suttorp, and B. Opitz, “NOD-like receptors in lung diseases,” Frontiers in Immunology, vol. 4, no. 393, pp. 1–12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  154. K. Kersse, M. J. M. Bertrand, M. Lamkanfi, and P. Vandenabeele, “NOD-like receptors and the innate immune system: coping with danger, damage and death,” Cytokine & Growth Factor Reviews, vol. 22, no. 5-6, pp. 257–276, 2011. View at Publisher · View at Google Scholar · View at Scopus
  155. J. H. Fritz, L. Le Bourhis, G. Sellge et al., “Nod1-mediated innate immune recognition of peptidoglycan contributes to the onset of adaptive immunity,” Immunity, vol. 26, no. 4, pp. 445–459, 2007. View at Publisher · View at Google Scholar · View at Scopus
  156. C. C. Allison, T. A. Kufer, E. Kremmer, M. Kaparakis, and R. L. Ferrero, “Helicobacter pylori induces MAPK phosphorylation and AP-1 activation via a NOD1-dependent mechanism,” Journal of Immunology, vol. 183, no. 12, pp. 8099–8109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  157. J. Ferrand and R. L. Ferrero, “Recognition of extracellular bacteria by NLRs and its role in the development of adaptive immunity,” Frontiers in Immunology, vol. 4, no. 344, pp. 1–12, 2013. View at Google Scholar
  158. Q. Pan, V. Kravchenko, A. Katz et al., “NF-κB-inducing kinase regulates selected gene expression in the Nod2 signaling pathway,” Infection and Immunity, vol. 74, no. 4, pp. 2121–2127, 2006. View at Publisher · View at Google Scholar · View at Scopus
  159. J.-H. Park, Y.-G. Kim, C. McDonald et al., “RICK/RIP2 mediates innate immune responses induced through Nod1 and Nod2 but not TLRs,” The Journal of Immunology, vol. 178, no. 4, pp. 2380–2386, 2007. View at Publisher · View at Google Scholar · View at Scopus
  160. J.-H. Park, Y.-G. Kim, M. Shaw et al., “Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells,” The Journal of Immunology, vol. 179, no. 1, pp. 514–521, 2007. View at Publisher · View at Google Scholar · View at Scopus
  161. K. Geddes, S. Rubino, C. Streutker et al., “Nod1 and Nod2 regulation of inflammation in the Salmonella colitis model,” Infection and Immunity, vol. 78, no. 12, pp. 5107–5115, 2010. View at Publisher · View at Google Scholar · View at Scopus
  162. T. Langefeld, W. Mohamed, R. Ghai, and T. Chakraborty, “Toll-like receptors and NOD-likereceptors: domain architecture and cellular signaling,” in Target Pattern Recognition in Innate Immunity, Landes Bioscience and Springer Science, 2009. View at Google Scholar
  163. C. Nembrini, J. Kisielow, A. T. Shamshiev et al., “The kinase-activity of Rip2 determines its stability and consequently Nod1—and Nod2-mediated immune responses,” Journal of Biological Chemistry, vol. 284, no. 29, pp. 19183–19188, 2009. View at Publisher · View at Google Scholar · View at Scopus
  164. H. T. Le and J. A. Harton, “Pyrin- and CARD-only proteins as regulators of NLR functions,” Frontiers in Immunology, vol. 4, article 275, Article ID Article 275, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  165. J. G. Magalhaes, M. T. Sorbara, S. E. Girardin, and D. J. Philpott, “What is new with Nods?” Current Opinion in Immunology, vol. 23, no. 1, pp. 29–34, 2011. View at Publisher · View at Google Scholar · View at Scopus
  166. M. J. M. Bertrand, K. Doiron, K. Labbé, R. G. Korneluk, P. A. Barker, and M. Saleh, “Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immune signaling by the pattern recognition receptors NOD1 and NOD2,” Immunity, vol. 30, no. 6, pp. 789–801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  167. P. Vandenabeele and M. J. M. Bertrand, “The role of the IAP E3 ubiquitin ligases in regulating pattern-recognition receptor signalling,” Nature Reviews Immunology, vol. 12, no. 12, pp. 833–844, 2012. View at Publisher · View at Google Scholar · View at Scopus
  168. D. Zhang, G. Zhang, M. S. Hayden et al., “A Toll-like receptor that prevents infection by uropathogenic bacteria,” Science, vol. 303, no. 5663, pp. 1522–1526, 2004. View at Publisher · View at Google Scholar · View at Scopus
  169. B. Zurek, M. Proell, R. N. Wagner, R. Schwarzenbacher, and T. A. Kufer, “Mutational analysis of human NOD1 and NOD2 NACHT domains reveals different modes of activation,” Innate Immunity, vol. 18, no. 1, pp. 100–111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  170. A. Uehara, S. Yang, Y. Fujimoto et al., “Muramyldipeptide and diaminopimelic acid-containing desmuramylpeptides in combination with chemically synthesized Toll-like receptor agonists synergistically induced production of interleukin-8 in a NOD2- and NOD1-dependent manner, respectively, in human monocytic cells in culture,” Cellular Microbiology, vol. 7, no. 1, pp. 53–61, 2005. View at Publisher · View at Google Scholar · View at Scopus
  171. A. Uehara and H. Takada, “Synergism between TLRs and NOD1/2 in oral epithelial cells,” Journal of Dental Research, vol. 87, no. 7, pp. 682–686, 2008. View at Publisher · View at Google Scholar · View at Scopus
  172. J. H. Fritz, S. E. Girardin, C. Fitting et al., “Synergistic stimulation of human monocytes and dendritic cells by toll-like receptor 4 and NOD1- and NOD2- activating agonists,” European Journal of Immunology, vol. 35, no. 8, pp. 2459–2470, 2005. View at Publisher · View at Google Scholar · View at Scopus
  173. K. S. Kobayashi, M. Chamaillard, Y. Ogura et al., “Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract,” Science, vol. 307, no. 5710, pp. 731–734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  174. H. Tada, S. Aiba, K. I. Shibata, T. Ohteki, and H. Takada, “Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells,” Infection and Immunity, vol. 73, no. 12, pp. 7967–7976, 2005. View at Publisher · View at Google Scholar · View at Scopus
  175. D. A. van Heel, S. Ghosh, M. Butler et al., “Synergistic enhancement of Toll-like receptor responses by NOD1 activation,” European Journal of Immunology, vol. 35, no. 8, pp. 2471–2476, 2005. View at Publisher · View at Google Scholar · View at Scopus
  176. M. G. Netea, G. Ferwerda, D. J. de Jong et al., “Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release,” The Journal of Immunology, vol. 174, no. 10, pp. 6518–6523, 2005. View at Publisher · View at Google Scholar · View at Scopus
  177. B. C. Mercier, E. Ventre, M.-L. Fogeron et al., “NOD1 cooperates with TLR2 to enhance T cell receptor-mediated activation in CD8 T cells,” PLoS ONE, vol. 7, no. 7, Article ID e42170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  178. H. Schwarz, G. Posselt, P. Wurm, M. Ulbing, A. Duschl, and J. Horejs-Hoeck, “TLR8 and NOD signaling synergistically induce the production of IL-1β and IL-23 in monocyte-derived DCs and enhance the expression of the feedback inhibitor SOCS2,” Immunobiology, vol. 218, no. 4, pp. 533–542, 2013. View at Publisher · View at Google Scholar · View at Scopus
  179. G. Ferwerda, B. J. Kullberg, D. J. de Jong et al., “Mycobacterium paratuberculosis is recognized by Toll-like receptors and NOD2,” Journal of Leukocyte Biology, vol. 82, no. 4, pp. 1011–1018, 2007. View at Publisher · View at Google Scholar · View at Scopus
  180. L. O. Moreira, K. C. El Kasmi, A. M. Smith et al., “The TLR2-MyD88-NOD2-RIPK2 signalling axis regulates a balanced pro-inflammatory and IL-10-mediated anti-inflammatory cytokine response to Gram-positive cell walls,” Cellular Microbiology, vol. 10, no. 10, pp. 2067–2077, 2008. View at Publisher · View at Google Scholar · View at Scopus
  181. A. G. Joyee and X. Yang, “Role of toll-like receptors in immune responses to chlamydial infections,” Current Pharmaceutical Design, vol. 14, no. 6, pp. 593–600, 2008. View at Publisher · View at Google Scholar · View at Scopus
  182. W. R. Berrington, K. D. Smith, S. J. Skerrett, and T. R. Hawn, “Nucleotide-binding oligomerization domain containing-like receptor family, caspase recruitment domain (CARD) containing 4 (NLRC4) regulates intrapulmonary replication of aerosolized Legionella pneumophila,” BMC Infectious Diseases, vol. 13, no. 1, article 371, 2013. View at Publisher · View at Google Scholar · View at Scopus
  183. K. A. Archer, F. Ader, K. S. Kobayashi, R. A. Flavell, and C. R. Roy, “Cooperation between multiple microbial pattern recognition systems is important for host protection against the intracellular pathogen Legionella pneumophila,” Infection and Immunity, vol. 78, no. 6, pp. 2477–2487, 2010. View at Publisher · View at Google Scholar · View at Scopus
  184. M. S. Jabir, N. D. Ritchie, D. Li et al., “Caspase-1 cleavage of the TLR adaptor TRIF inhibits autophagy and β-interferon production during Pseudomonas aeruginosa infection,” Cell Host and Microbe, vol. 15, no. 2, pp. 214–227, 2014. View at Publisher · View at Google Scholar · View at Scopus
  185. E. Faure, J.-B. Mear, K. Faure et al., “Pseudomonas aeruginosa type-3 secretion system dampens host defense by exploiting the NLRC4-coupled inflammasome,” American Journal of Respiratory and Critical Care Medicine, vol. 189, no. 7, pp. 799–811, 2014. View at Publisher · View at Google Scholar · View at Scopus
  186. D.-J. Kim, J.-H. Park, L. Franchi, S. Backert, and G. Núñez, “The Cag pathogenicity island and interaction between TLR2/NOD2 and NLRP3 regulate IL-1β production in Helicobacter pylori infected dendritic cells,” European Journal of Immunology, vol. 43, no. 10, pp. 2650–2658, 2013. View at Publisher · View at Google Scholar · View at Scopus
  187. A. I. Tukhvatulin, I. I. Gitlin, D. V. Shcheblyakov et al., “Combined stimulation of toll-like receptor 5 and nod1 strongly potentiates activity of NF-κB, resulting in enhanced innate immune reactions and resistance to Salmonella enterica serovar typhimurium infection,” Infection and Immunity, vol. 81, no. 10, pp. 3855–3864, 2013. View at Publisher · View at Google Scholar · View at Scopus
  188. T. Volz, M. Nega, J. Buschmann et al., “Natural Staphylococcus aureus-derived peptidoglycan fragments activate NOD2 and act as potent costimulators of the innate immune system exclusively in the presence of TLR signals,” FASEB Journal, vol. 24, no. 10, pp. 4089–4102, 2010. View at Publisher · View at Google Scholar · View at Scopus
  189. M. A. Müller-Anstett, P. Müller, T. Albrecht et al., “Staphylococcal peptidoglycan co-localizes with Nod2 and TLR2 and activates innate immune response via both receptors in primary murine keratinocytes,” PLoS ONE, vol. 5, no. 10, Article ID e13153, 2010. View at Publisher · View at Google Scholar · View at Scopus
  190. C. Toma, N. Higa, Y. Koizumi et al., “Pathogenic Vibrio activate NLRP3 inflammasome via cytotoxins and TLR/nucleotide-binding oligomerization domain-mediated NF-κB signaling,” The Journal of Immunology, vol. 184, no. 9, pp. 5287–5297, 2010. View at Publisher · View at Google Scholar · View at Scopus
  191. E. J. Hennessy, A. E. Parker, and L. A. J. O'Neill, “Targeting Toll-like receptors: emerging therapeutics?” Nature Reviews Drug Discovery, vol. 9, no. 4, pp. 293–307, 2010. View at Publisher · View at Google Scholar · View at Scopus
  192. A. Zhou, S. Li, J. Wu, F. A. Khan, and S. Zhang, “Interplay between microRNAs and host pathogen recognition receptors (PRRs) signaling pathways in response to viral infection,” Virus Research, vol. 184, pp. 1–6, 2014. View at Publisher · View at Google Scholar · View at Scopus
  193. F. J. Sheedy and L. A. J. O'Neill, “Adding fuel to fire: MicroRNAs as a new class of mediators of inflammation,” Annals of the Rheumatic Diseases, vol. 67, supplement 3, pp. iii50–iii55, 2008. View at Publisher · View at Google Scholar · View at Scopus