Signaling via pattern recognition receptors NOD2 and TLR2 contributes to immunomodulatory control of lethal pneumovirus infection

Antiviral Research

Volumn 132, Issue , 2016, Pages 131-140

  Rice, Tyler A ^a   Brenner, Todd A ^a   Percopo, Caroline M ^a   Ma, Michelle ^a   Keicher, Jesse D ^b   Domachowske, Joseph B ^c   Rosenberg, Helene F ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b GLAXOSMITHKLINE   (United States)

^c SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Cytokines; Inflammation; Pattern recognition receptors; Pneumovirus; Probiotic

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; PROBIOTIC AGENT; TOLL LIKE RECEPTOR 2; AUTACOID; CYTOKINE; LIGAND; PATTERN RECOGNITION RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EX VIVO STUDY; GENE DELETION; HETEROLOGOUS IMMUNITY; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; LACTOBACILLUS PLANTARUM; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PNEUMOVIRUS INFECTION; PRIORITY JOURNAL; SURVIVAL RATE; VIRUS GENE; ANIMAL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; MORTALITY; MURINE PNEUMONIA VIRUS; PATHOLOGY; PNEUMOVIRUS; SIGNAL TRANSDUCTION; VIROLOGY; VIRUS LOAD;

ANIMALS; CYTOKINES; IMMUNOMODULATION; INFLAMMATION MEDIATORS; LACTOBACILLUS PLANTARUM; LIGANDS; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, KNOCKOUT; MURINE PNEUMONIA VIRUS; NOD2 SIGNALING ADAPTOR PROTEIN; PNEUMOVIRUS; PNEUMOVIRUS INFECTIONS; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; VIRAL LOAD;

EID: 84975467474     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2016.06.002     Document Type: Article

References (64)

1. T. Andabaka, J.W. Nickerson, M.X. Rojas-Reyes, J.D. Rueda, V. Bacic Vrca, and B. Barsic Monoclonal antibody for reducing the risk of respiratory syncytial virus infection in children Cochrane Database Syst. Rev. 30 2013 4:CD006602
2. L. Arruvito, S. Raiden, and J. Geffner Host response to respiratory syncytial virus infection Curr. Opin. Infect. Dis. 28 2015 259 266
3. R.A. Bem, J.B. Domachowske, and H.F. Rosenberg Animal models of human respiratory syncytial virus disease Am. J. Physiol. Lung Cell Mol. Physiol. 30 2011 L148 L156
4. M.O. Blanken, M.M. Rovers, J.M. Molenaar, P.L. Winkler-Seinstra, A. Meijer, J.L. Kimpen, L. Bont Dutch RSV Neonatal Network Respiratory syncytial virus and recurrent wheeze in healthy preterm infants N. Engl. J. Med. 368 2013 1791 1799
5. B. Bondue, O. Vosters, P. de Nadai, S. Glineur, O. De Henau, S. Luangsay, F. Van Gool, D. Communi, P. De Vuyst, D. Desmecht, and M. Parmentier ChemR23 dampens lung inflammation and enhances anti-viral immunity in a mouse model of acute viral pneumonia PLoS Pathog. 7 2011 e1002358
6. C.A. Bonville, V.K. Lau, J.M. DeLeon, J.L. Gao, A.J. Easton, H.F. Rosenberg, and J.B. Domachowske Functional antagonism of chemokine receptor CCR1 reduces mortality in acute pneumovirus infection in vivo J. Virol. 78 2004 7984 7989
7. C.A. Bonville, N.J. Bennett, M. Koehnlein, D.M. Haines, J.A. Ellis, A.M. DelVecchio, H.F. Rosenberg, and J.B. Domachowske Respiratory dysfunction and proinflammatory chemokines in the pneumonia virus of mice (PVM) model of viral bronchiolitis Virology 349 2006 87 95
8. D.M.E. Bowdish, M.S. Loffredo, S. Mukhopadhyay, A. Mantovani, and S. Gordon Macrophage receptors implicated in the "adaptive" form of innate immunity Microb. Infect. 9 2007 1680 1687
9. 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 J. Clin. Investig. 121 2011 3666 3676
10. E. De Clerq Chemotherapy of respiratory syncytial virus infections: the final breakthrough Int. J. Antimicrob. Agents 45 2015 234 237
11. M.G. Dorrington, A.M. Roche, S.E. Chauvin, Z. Tu, K.L. Mossman, J.N. Weiser, and D.M. Bowdish MARCO is required for TLR2- and Nod2-mediated responses to Streptococcus pneumoniae and clearance of pneumococcal colonization in the murine nasopharynx J. Immunol. 190 2013 250 258
12. M.G. Drake, S.E. Evans, B.F. Dickey, A.D. Fryer, and D.B. Jacoby Toll-like receptor 2/6 and Toll-like receptor-9 agonists suppress viral replication but not airway hyperreactivity in guinea pigs Am. J. Respir. Cell Mol. Biol. 48 2013 790 796
13. K.D. Dyer, J.M. Moser, M. Czapiga, S.J. Siegel, C.M. Percopo, and H.F. Rosenberg Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow J. Immunol. 181 2008 4004 4009
14. K.D. Dyer, K.E. Garcia-Crespo, K.E. Killoran, and H.F. Rosenberg Antigen profiles for the quantitative assessment of eosinophils in mouse tissues by flow cytometry J. Immunol. Methods 369 2011 91 97
15. K.D. Dyer, K.E. Garcia-Crespo, S. Glineur, J.B. Domachowske, and H.F. Rosenberg The pneumonia virus of mice (PVM) model of acute respiratory infection Viruses 4 2012 3494 3510
16. S. Esposito, D. Rigante, and N. Principi Do children's upper respiratory tract infections benefit from probiotics? BMC Infect. Dis. 14 2014 194
17. S.J. Gabryszewski, O. Bachar, K.D. Dyer, C.M. Percopo, K.E. Killoran, J.B. Domachowske, and H.F. Rosenberg Lactobacillus-mediated priming of the respiratory mucosa protects against lethal pneumovirus infection J. Immunol. 186 2011 1151 1161
18. K.E. Garcia-Crespo, C.C. Chan, S.J. Gabryszewski, C.M. Percopo, P. Rigaux, K.D. Dyer, J.B. Domachowske, and H.F. Rosenberg Lactobacillus priming of the respiratory tract: heterologous immunity and protection against lethal pneumovirus infection Antivir. Res. 97 2013 270 279
19. M.L. Garly, C.L. Martins, C. Bale, M.A. Balde, K.L. Hedegaard, P. Gustafson, I.M. Lisse, H.C. Whittle, and P. Aaby BCG scar and positive tuberculun reaction associated with reduced child mortality in West Africa. A non-specific beneficial effect of BCG? Vaccine 21 2003 2782 2790
20. R.S. Gomez, I. Guisle-Marsollier, K. Bohmwald, S.M. Bueno, and A.M. Kalergis Respiratory syncytial virus: pathology, therapeutic drugs, and prophylaxis Immunol. Lett. 162 1 pt A 2014 237 247
21. C.B. Hall, W.J. Hall, C.L. Gala, F.B. MaGill, and J.P. Leddy Long-term prospective study in children after respiratory syncytial virus infection J. Pediatr. 105 1984 358 364
22. Q. Hao, Z. Lu, B.R. Don, C.Q. Huang, and T. Wu Probiotics for preventing acute upper respiratory tract infections Cochrane Database Syst. Rev. 9 2011 CD006895
23. A. Hevia, S. Delgado, B. Sanchez, and A. Margolles Molecular players involved in the interaction between beneficial bacteria and the immune system Front. Microbiol. 6 2015 1285
24. T. Hussell, and T.J. Bell Alveolar macrophages: plasticity in a tissue-specific context Nat. Rev. Immunol. 14 2014 81 93
25. D.C. Ifrim, J. Quintin, L.A.B. Joosten, C. Jacobs, T. Jansen, L. Jacobs, N.A.R. Gow, D.L. Williams, J.W.M. van der Meer, and M.G. Netea Trained immunity or tolerance: opposing functional programs induced in human monocytes after engagement of various pattern recognition receptors Clin. Vaccine Immunol. 21 2014 534 545
26. T. Izumo, T. Maekawa, M. Ida, A. Noguchi, Y. Kitagawa, H. Shibata, H. Yasui, and Y. Kito Effect of intranasal administration of Lactobacillus pentosus S-PT84 on influenza virus infection in mice Int. Immunopharmacol. 10 2010 1101 1106
27. S. Koizumi, D. Wakita, T. Sato, R. Mitamura, T. Izumo, H. Shibata, Y. Koso, K. Chamoto, Y. Togashi, H. Kitamura, and T. Nishimura Essential role of Toll-like receptors for dendritic cell and NK1.1(+) cell-dependent activation of type 1 immunity by Lactobacillus pentosus strain S-PT84 Immunol. Lett. 120 1-2 2008 14 19
28. M. Leissinger, R. Kulkarni, R.L. Zemans, G.P. Downey, and S. Jeyaseelan Investigating the role of nucleotide binding oligomerization domain like receptors in bacterial lung infection Am. J. Respir. Crit. Care Med. 189 2014 1461 1468
29. O. Levy, and M.G. Netea Innate immune memory: implications for development of pediatric immunomodulatory agents and adjuvanted vaccines Pediatr. Res. 75 2014 184 188
30. Y. Liu, N.Y. Fatheree, N. Mangalat, and J.M. Rhoads Lactobacillus reuteri strains reduce incidence and severity of experimental necrotizing enterocolitis via modulation of TLR4 and NF-kB siganling in the intestine Am. J. Physiol. Gastrointest. Liver Physiol. 302 2012 G608 G617
31. M. Locati, A. Mantovani, and A. Sica Macrophage activation and polarization as an adaptive component of innate immunity Adv. Immunol. 120 2013 163 184
32. E. Macho Fernandez, V. Valenti, C. Rockel, C. Hermann, B. Pot, I.G. Boneca, and C. Grangette Anti-inflammatory capacity of selected latobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide Gut 60 2011 1050 1059
33. H.C. Meissner Viral bronchiolitis in children N. Engl. J. Med. 374 2016 62 72
34. S. Mukherjee, and N.W. Lukacs Innate immune responses to respiratory syncytial virus infection Curr. Top. Microbiol. Immunol. 372 2013 139 154
35. M.A. Muller-Anstett, P. Muller, T. Albrecht, M. Nega, J. Wagener, Q. Gao, S. Kaesler, M. Schaller, T. Biedermann, and F. Gotz Staphylococcal peptidoglycan co-localizes with Nod2 and Tlr2 and activated innate immune response via both receptors in primary murine keratinocytes PloS One 7 2010 313153
36. M.G. Netea, J. Quintin, and J.W.M. van der Meer Trained immunity: a memory for innate host defense Cell Host Microbe 9 2011 355 361
37. T.A. Oelschlaeger Mechanisms of probiotic actions - a review Int. J. Med. Microbiol. 300 2010 57 62
38. M. Ozen, G.K. Sandal, and E.C. Dinleyici Probiotics for the prevention of pediatric upper respiratory infections: a systematic review Expert Opin. Biol. Ther. 15 2015 9 20
39. M.K. Park, V. Ngo, Y.M. Kwon, Y.T. Lee, S. Yoo, Y.H. Cho, S.M. Hong, S.H. Hwang, E.J. Ko, Y.J. Jung, D.W. Moon, E.J. Jeong, M.C. Kim, Y.N. Lee, J.H. Jang, J.S. Oh, C.H. Kim, and S.H. Kang Lactobacillus plantarum DK119 as a probiotic confers protection against influenza virus by modulating innate immunity PLoS One 9 2013 e75368
40. V. Pavot, N. Rochereau, J. Resseguier, A. Gutjahr, C. Genin, G. Tiraby, E. Perouzel, T. Lioux, F. Vernejoul, B. Verrier, and S. Paul Cutting edge: new chimeric NOD2/TLR2 adjuvant drastically increases vaccine immunogenicity J. Immunol. 193 2014 5781 5785
41. C.M. Percopo, E.J. Dubovi, R.W. Renshaw, K.D. Dyer, J.B. Domachowske, and H.F. Rosenberg Canine pneumovirus replicates in mouse lung tissue and elicits inflammatory pathology Virology 416 2011 26 31
42. C.M. Percopo, K.D. Dyer, K.E. Garcia-Crespo, S.J. Gabryszewski, A.L. Shaffer 3rd, J.B. Domachowske, and H.F. Rosenberg B cells are not essential for Lactobacillus-mediated protection against lethal pneumovirus infection J. Immunol. 192 2014 5265 5272
43. C.M. Percopo, K.D. Dyer, K.A. Karpe, J.B. Domachowske, and H.F. Rosenberg Eosinophils and respiratory virus infection: a dual-standard curve qRT-PCR-based method for determining virus recovery from mouse lung tissue Methods Mol. Biol. 1178 2014 257 266
44. C.M. Percopo, T.A. Rice, T.A. Brenner, K.D. Dyer, J.L. Luo, K. Kanakabandi, D.E. Sturdevant, S.F. Porcella, J.B. Domachowske, J.D. Keicher, and H.F. Rosenberg Immunobiotic Lactobacillus administered post-exposure averts the lethal sequelae of respiratory virus infection Antivir. Res. 121 2015 109 119
45. 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
46. H.F. Rosenberg, and J.B. Domachowske Inflammatory responses to respiratory syncytial virus (RSV) infection and the development of immunomodulatory pharmacotherapeutics Curr. Med. Chem. 19 2012 1424 1431
47. J. Royet, D. Gupta, and R. Dziarski Peptidoglycan recognition proteins: modulators of the microbiome and inflammation Nat. Rev. Immunol. 11 2011 837 851
48. S. Scheer, C. Krempl, C. Kallfass, S. Frey, T. Jakob, G. Mouahid, H. Mone, A. Schmitt-Graff, P. Staeheli, and M.C. Lamers S. mansoni bolsters anti-viral immunity in the murine respiratory tract PLoS One 9 2014 e112469
49. M. Shafique, T. Meijerhof, J. Wilschut, and A. de Haan Evaluation of an intranasal virosomal vaccine against respiratory syncytial virus in mice: effect of TLR2 and NOD2 ligands on induction of systemic and mucosal immune responses PLoS One 8 2013 e61287
50. J.S. Siegle, N. Hansbro, C. Dong, P. Angkasekwinai, P.S. Foster, and R.K. Kumar Blocking induction of T helper type 2 responses prevents development of disease in a model of childhood asthma Clin. Exp. Immunol. 165 2011 19 28
51. C.M. Tabarani, C.A. Bonville, M. Suryadevara, P. Branigan, D. Wang, D. Huang, H.F. Rosenberg, and J.B. Domachowske Novel inflammatory markers, clinical risk factors, and virus type associated with severe respiratory syncytial virus infection Pediatr. Infect. Dis. J. 32 2013 e437 e442
52. V. Taverniti, and S. Guglielmetti The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of parabiotic concept) Genes Nutr. 6 2011 261 274
53. Y. Tomasada, E. Chiba, H. Zelaya, T. Takahashi, K. Tsykida, H. Kitazawa, S. Alvarez, and J. Villena Nasally administered Lactobacillus rhamnossus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection BMC Immunol. 14 2013 40
54. M.J. Tuvim, B.E. Gilbert, B.F. Dickey, and S.E. Evans Synergistic TLR2/6 and TLR9 activation protects mice against lethal influenza pneumonia PLoS One 7 2012 e30596
55. J.W.M. van der Meer, L.A.B. Joosten, N. Riksen, and M.G. Netea Trained immunity: a smart way to enhance innate immune defence Mol. Immunol. 68 2015 40 44
56. E.E. Walsh, and A.R. Falsey Respiratory syncytial virus infection in adult populations Infect. Disord. Drug Targets 12 2012 98 102
57. K.B. Walsh, J.R. Teijaro, L.G. Brock, D.M. Fremgen, P.L. Collins, H. Rosen, and M.B. Oldstone Animal model of respiratory syncytial virus: CD8+ T cells cause a cytokine storm that is chemically tractable by sphingosine-1-phoshpate receptor agonist therapy J. Virol. 88 2014 6281 6293
58. T. Watanabe, A. Kitani, P.J. Murray, Y. Wakatsuki, I.J. Fuss, and W. Strober Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis Immunity 25 2006 473 485
59. R.C. Welliver Sr. The immune response to respiratory syncytial virus infection:friend or foe? Clin. Rev. Allergy Immunol. 34 2008 163 173
60. E. Wissinger, J. Goulding, and T. Hussell Immune homeostasis in the respiratory tract and its impact on heterologous infection Semin. Immunol. 21 2009 147 155
61. J.P. Wong, L.P. Nagata, M.E. Christopher, A.M. Salazar, and R.M.K. Dale Prophylaxis of acute respiratory virus infections using nucleic acid based drugs Vaccine 23 2005 2266 2268
62. Q. Wu, M.C. Liu, J. Yang, J.F. Wang, and Y.H. Zhu Lactobacillus rhamnosus GR-1 ameliorates Escherichia coli-induced inflammation and cell damage via attenuation of ASC-independent NLRP3 inflammasome activation Appl. Environ. Microbiol. 82 2015 117 1182
63. Z. Yang, I.J. Fuss, T. Watanabe, N. Asano, M.P. Davey, J.T. Rosenbaum, W. Strober, and A. Kitani NOD2 transgenic mice exhibit enhanced MDP-mediated down-regulation of TLR2 responses and resistance to colitis induction Gastroenterology 133 2007 1510 1521
64. X. Yu, J. Zeng, and J. Xie Navigating through the maze of TLR2-mediated signaling network for better mycobacterium infection control Biochimie 102 2014 1 8