Multifaceted functions of NOD-like receptor proteins in myeloid cells at the intersection of innate and adaptive immunity

Microbiology Spectrum

Volumn 4, Issue 4, 2016, Pages

  Kufer, Thomas A ^a   Nigro, Giulia ^b,c   Sansonetti, Philippe J ^b,c,d  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b INSTITUT PASTEUR   (France)

^c INSERM   (France)

^d l'alimentation et l'Environnement   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL; BONE MARROW CELL; DENDRITIC CELL; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; MACROPHAGE; METABOLISM;

ADAPTIVE IMMUNITY; ANIMALS; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; MACROPHAGES; MYELOID CELLS; NLR PROTEINS; RECEPTORS, PATTERN RECOGNITION;

EID: 85011623239     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MCHD-0021-2015     Document Type: Article

References (82)

1. Janeway CA, Jr. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54: 1-13.
2. Wagner H. 2012. Innate immunity's path to the Nobel Prize 2011 and beyond. Eur J Immunol 42:1089-1092.
3. Unterholzner L. 2013. The interferon response to intracellular DNA: why so many receptors? Immunobiology 218:1312-1321.
4. Fritz JH, Ferrero RL, Philpott DJ, Girardin SE. 2006. Nod-like proteins in immunity, inflammation and disease. Nat Immunol 7:1250-1257.
5. Matzinger P. 1994. Tolerance, danger, and the extended family. Annu Rev Immunol 12:991-1045.
6. Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L, Ogura Y, Kawasaki A, Fukase K, Kusumoto S, Valvano MA, Foster SJ, Mak TW, Nuñez G, Inohara N. 2003. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4:702-707.
7. Girardin SE, Boneca IG, Carneiro LAM, Antignac A, JéhannoM, Viala J, Tedin K, TahaMK, Labigne A, Zähringer U, Coyle AJ, DiStefano PS, Bertin J, Sansonetti PJ, PhilpottDJ. 2003.Nod1 detects a uniquemuropeptide from Gram-negative bacterial peptidoglycan. Science 300:1584-1587.
8. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278:8869-8872.
9. Girardin SE, Travassos LH, Hervé M, Blanot D, Boneca IG, Philpott DJ, Sansonetti PJ, Mengin-Lecreulx D. 2003. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 278: 41702-41708.
10. Gomes LC, Dikic I. 2014. Autophagy in antimicrobial immunity. Mol Cell 54:224-233.
11. Cooney R, Baker J, Brain O, Danis B, Pichulik T, Allan P, Ferguson DJ, Campbell BJ, Jewell D, Simmons A. 2010. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat Med 16:90-97.
12. Homer CR, Richmond AL, Rebert NA, Achkar JP, McDonald C. 2010. ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn's disease pathogenesis. Gastroenterology 139:1630-1641.
13. Travassos LH, Carneiro LA, Ramjeet M, Hussey S, Kim YG, Magalhães JG, Yuan L, Soares F, Chea E, Le Bourhis L, Boneca IG, Allaoui A, Jones NL, Nuñez G, Girardin SE, Philpott DJ. 2010. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol 11:55-62.
14. Juárez E, Carranza C, Hernández-Sánchez F, Loyola E, Escobedo D, León-Contreras JC, Hernández-Pando R, Torres M, Sada E. 2014. Nucleotide-oligomerizing domain-1 (NOD1) receptor activation induces pro-inflammatory responses and autophagy in human alveolar macrophages. BMC Pulm Med 14:152. doi:10.1186/1471-2466-14-152.
15. Irving AT, Mimuro H, Kufer TA, Lo C, Wheeler R, Turner LJ, Thomas BJ, Malosse C, Gantier MP, Casillas LN, Votta BJ, Bertin J, Boneca IG, Sasakawa C, Philpott DJ, Ferrero RL, Kaparakis-Liaskos M. 2014. The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signaling. Cell Host Microbe 15:623-635.
16. Nakamura N, Lill JR, Phung Q, Jiang Z, Bakalarski C, de Mazière A, Klumperman J, Schlatter M, Delamarre L, Mellman I. 2014. Endosomes are specialized platforms for bacterial sensing and NOD2 signalling. Nature 509:240-244.
17. Sorbara MT, Ellison LK, Ramjeet M, Travassos LH, Jones NL, Girardin SE, Philpott DJ. 2013. The protein ATG16L1 suppresses inflammatory cytokines induced by the intracellular sensors Nod1 and Nod2 in an autophagy-independent manner. Immunity 39:858-873.
18. Nigro G, Rossi R, Commere P-H, Jay P, Sansonetti PJ. 2014. The cytosolic bacterial peptidoglycan sensor Nod2 affords stem cell protection and links microbes to gut epithelial regeneration. Cell Host Microbe 15:792-798.
19. Lala S, Ogura Y, Osborne C, Hor SY, Bromfield A, Davies S, Ogunbiyi O, Nuñez G, Keshav S. 2003. Crohn's disease and the NOD2 gene: a role for Paneth cells. Gastroenterology 125:47-57.
20. -/- mice. Gut 61:634-635.
21. Bouskra D, Brézillon C, Bérard M, Werts C, Varona R, Boneca IG, Eberl G. 2008. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456:507-510.
22. Barreau F, Meinzer U, Chareyre F, Berrebi D, Niwa-Kawakita M, Dussaillant M, Foligne B, Ollendorff V, Heyman M, Bonacorsi S, Lesuffleur T, Sterkers G, Giovannini M, Hugot JP. 2007. CARD15/NOD2 is required for Peyer's patches homeostasis in mice. PLoS One 2: e523-e523. doi:10.1371/journal.pone.0000523.
23. Alnabhani Z, Hugot JP, Montcuquet N, Le Roux K, Dussaillant M, Roy M, Leclerc M, Cerf-Bensussan N, Lepage P, Barreau F. 2016. Respective roles of hematopoietic and nonhematopoietic Nod2 on the gut microbiota and mucosal homeostasis. Inflamm Bowel Dis 22:763-773.
24. Janssen CE, Rose CD, De Hertogh G, Martin TM, Bader Meunier B, Cimaz R, Harjacek M, Quartier P, Ten Cate R, Thomee C, Desmet VJ, Fischer A, Roskams T, Wouters CH. 2012. Morphologic and immunohistochemical characterization of granulomas in the nucleotide oligomerization domain 2-related disorders Blau syndrome and Crohn disease. J Allergy Clin Immunol 129:1076-1084.
25. Schroder K, Tschopp J. 2010. The inflammasomes. Cell 140:821-832.
26. Elliott EI, Sutterwala FS. 2015. Initiation and perpetuation of NLRP3 inflammasome activation and assembly. Immunol Rev 265:35-52.
27. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, Fernandes-Alnemri T, Wu J, Monks BG, Fitzgerald KA, Hornung V, Latz E. 2009. Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 183:787-791.
28. Kufer TA, Sansonetti PJ. 2007. Sensing of bacteria: NOD a lonely job. Curr Opin Microbiol 10:62-69.
29. Diez E, Lee SH, Gauthier S, Yaraghi Z, Tremblay M, Vidal S, Gros P. 2003. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat Genet 33:55-60.
30. Wright EK, Jr, Goodart SA, Growney JD, Hadinoto V, Endrizzi MG, Long EM, Sadigh K, Abney AL, Bernstein-Hanley I, Dietrich WF. 2003. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr Biol 13:27-36.
31. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozören N, Jagirdar R, Inohara N, Vandenabeele P, Bertin J, Coyle A, Grant EP, Núñez G. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infectedmacrophages. Nat Immunol 7:576-582.
32. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf. Nat Immunol 7:569-575.
33. Vinzing M, Eitel J, Lippmann J, Hocke AC, Zahlten J, Slevogt H, N'guessan PD, Günther S, Schmeck B, Hippenstiel S, Flieger A, Suttorp N, Opitz B. 2008. NAIP and Ipaf control Legionella pneumophila replication in human cells. J Immunol 180:6808-6815.
34. Vance RE. 2015. The NAIP/NLRC4 inflammasomes. Curr Opin Immunol 32:84-89.
35. Sutterwala FS, Haasken S, Cassel SL. 2014. Mechanism of NLRP3 inflammasome activation. Ann N Y Acad Sci 1319:82-95.
36. Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. 2008. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453:1122-1126.
37. Franchi L, Núñez G. 2008. The Nlrp3 inflammasome is critical for aluminium hydroxide-mediated IL-1β secretion but dispensable for adjuvant activity. Eur J Immunol 38:2085-2089.
38. Li H, Willingham SB, Ting JP, Re F. 2008. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J Immunol 181:17-21.
39. Maisonneuve C, Bertholet S, Philpott DJ, De Gregorio E. 2014. Unleashing the potential of NOD-and Toll-like agonists as vaccine adjuvants. Proc Natl Acad Sci U S A 111:12294-12299.
40. Fritz JH, Le Bourhis L, Sellge G, Magalhaes JG, Fsihi H, Kufer TA, Collins C, Viala J, Ferrero RL, Girardin SE, Philpott DJ. 2007. Nod1-mediated innate immune recognition of peptidoglycan contributes to the onset of adaptive immunity. Immunity 26:445-459.
41. Broderick L, De Nardo D, Franklin BS, Hoffman HM, Latz E. 2015. The inflammasomes and autoinflammatory syndromes. Annu Rev Pathol 10:395-424.
42. Jesus AA, Goldbach-Mansky R. 2014. IL-1 blockade in autoinflammatory syndromes. Annu Rev Med 65:223-244.
43. H2 differentiation. Nat Immunol 16:859-870.
44. Arthur JC, Lich JD, Ye Z, Allen IC, Gris D, Wilson JE, Schneider M, Roney KE, O'Connor BP, Moore CB, Morrison A, Sutterwala FS, Bertin J, Koller BH, Liu Z, Ting JP. 2010. Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J Immunol 185:4515-4519.
45. Tuncer S, Fiorillo MT, Sorrentino R. 2014. The multifaceted nature of NLRP12. J Leukoc Biol 96:991-1000.
46. Lukens JR, Gurung P, Shaw PJ, Barr MJ, Zaki MH, Brown SA, Vogel P, Chi H, Kanneganti TD. 2015. The NLRP12 sensor negatively regulates autoinflammatory disease by modulating interleukin-4 production in T cells. Immunity 42:654-664.
47. Gregor MF, Hotamisligil GS. 2011. Inflammatory mechanisms in obesity. Annu Rev Immunol 29:415-445.
48. Schertzer JD, Tamrakar AK, Magalhães JG, Pereira S, Bilan PJ, Fullerton MD, Liu Z, Steinberg GR, Giacca A, Philpott DJ, Klip A. 2011. NOD1 activators link innate immunity to insulin resistance. Diabetes 60:2206-2215.
49. Zhou YJ, Liu C, Li CL, Song YL, Tang YS, Zhou H, Li A, Li Y, Weng Y, Zheng FP. 2015. Increased NOD1, but not NOD2, activity in subcutaneous adipose tissue from patients with metabolic syndrome. Obesity (Silver Spring) 23:1394-1400.
50. Denou E, Lolmède K, Garidou L, Pomie C, Chabo C, Lau TC, Fullerton MD, Nigro G, Zakaroff-Girard A, Luche E, Garret C, Serino M, Amar J, Courtney M, Cavallari JF, Henriksbo BD, Barra NG, Foley KP, McPhee JB, Duggan BM, O'Neill HM, Lee AJ, Sansonetti P, Ashkar AA, KhanWI, Surette MG, Bouloumié A, Steinberg GR, Burcelin R, Schertzer JD. 2015. Defective NOD2 peptidoglycan sensing promotes diet-induced inflammation, dysbiosis, and insulin resistance. EMBO Mol Med 7:259-274.
51. Youm YH, Nguyen KY, Grant RW, Goldberg EL, Bodogai M, Kim D, D'Agostino D, Planavsky N, Lupfer C, Kanneganti TD, Kang S, Horvath TL, Fahmy TM, Crawford PA, Biragyn A, Alnemri E, Dixit VD. 2015. The ketone metabolite β-hydroxybutyrate blocks NLRP3 inflammasomemediated inflammatory disease. Nat Med 21:263-269.
52. L'homme L, Esser N, Riva L, Scheen A, Paquot N, Piette J, Legrand-Poels S. 2013. Unsaturated fatty acids prevent activation of NLRP3 inflammasome in human monocytes/macrophages. J Lipid Res 54:2998-3008.
53. Yan Y, Jiang W, Spinetti T, Tardivel A, Castillo R, Bourquin C, Guarda G, Tian Z, Tschopp J, Zhou R. 2013. Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation. Immunity 38:1154-1163.
54. McNelis JC, Olefsky JM. 2014. Macrophages, immunity, and metabolic disease. Immunity 41:36-48.
55. Krishnaswamy JK, Chu T, Eisenbarth SC. 2013. Beyond pattern recognition: NOD-like receptors in dendritic cells. Trends Immunol 34:224-233.
56. H2-driven allergic inflammation. J Allergy Clin Immunol 126:1284-1293.e10. doi:10.1016/j.jaci.2010.09.021.
57. Magalhaes JG, Fritz JH, Le Bourhis L, Sellge G, Travassos LH, Selvanantham T, Girardin SE, Gommerman JL, Philpott DJ. 2008. Nod2-dependent Th2 polarization of antigen-specific immunity. J Immunol 181:7925-7935.
58. Magalhaes JG, Rubino SJ, Travassos LH, Le Bourhis L, Duan W, Sellge G, Geddes K, Reardon C, LechmannM, Carneiro LA, Selvanantham T, Fritz JH, Taylor BC, Artis D, Mak TW, Comeau MR, Croft M, Girardin SE, Philpott DJ, Philpott DJ. 2011. Nucleotide oligomerization domain-containing proteins instruct T cell helper type 2 immunity through stromal activation. Proc Natl Acad Sci U S A 108:14896-14901.
59. Asano J, Tada H, Onai N, Sato T, Horie Y, Fujimoto Y, Fukase K, Suzuki A, Mak TW, Ohteki T. 2010. Nucleotide oligomerization binding domain-like receptor signaling enhances dendritic cell-mediated crosspriming in vivo. J Immunol 184:736-745.
60. Steimle V, Otten LA, Zufferey M, Mach B. 1993. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75:135-146.
61. Devaiah BN, Singer DS. 2013. CIITA and its dual roles in MHC gene transcription. Front Immunol 4:476. doi:10.3389/fimmu.2013.00476.
62. Kobayashi KS, van den Elsen PJ. 2012. NLRC5: a key regulator of MHC class I-dependent immune responses.Nat Rev Immunol 12:813-820.
63. Meissner TB, Li A, Biswas A, Lee KH, Liu YJ, Bayir E, Iliopoulos D, van den Elsen PJ, Kobayashi KS. 2010. NLR family member NLRC5 is a transcriptional regulator of MHC class I genes. Proc Natl Acad Sci U S A 107:13794-13799.
64. Neerincx A, Lautz K, Menning M, Kremmer E, Zigrino P, Hösel M, Büning H, Schwarzenbacher R, Kufer TA. 2010. A role for the human nucleotide-binding domain, leucine-rich repeat-containing family member NLRC5 in antiviral responses. J Biol Chem 285:26223-26232.
65. Neerincx A, Rodriguez GM, Steimle V, Kufer TA. 2012. NLRC5 controls basal MHC class I gene expression in an MHC enhanceosomedependent manner. J Immunol 188:4940-4950.
66. Ludigs K, Seguín-Estévez Q, Lemeille S, Ferrero I, Rota G, Chelbi S, Mattmann C, MacDonald HR, Reith W, Guarda G. 2015. NLRC5 exclusively transactivatesMHC class I and related genes through a distinctive SXY module. PLoS Genet 11:e1005088. doi:10.1371/journal.pgen.1005088.
67. Neerincx A, Jakobshagen K, Utermöhlen O, Büning H, Steimle V, Kufer TA. 2014. The N-terminal domain of NLRC5 confers transcriptional activity for MHC class I and II gene expression. J Immunol 193:3090-3100.
68. Benko S, Magalhaes JG, Philpott DJ, Girardin SE. 2010. NLRC5 limits the activation of inflammatory pathways. J Immunol 185:1681-1691.
69. Cui J, Zhu L, Xia X, Wang HY, Legras X, Hong J, Ji J, Shen P, Zheng S, Chen ZJ, Wang RF. 2010. NLRC5 negatively regulates the NF-?B and type I interferon signaling pathways. Cell 141:483-496.
70. Davis BK, Roberts RA, Huang MT, Willingham SB, Conti BJ, Brickey WJ, Barker BR, Kwan M, Taxman DJ, Accavitti-Loper MA, Duncan JA, Ting JP. 2011. Cutting edge: NLRC5-dependent activation of the inflammasome. J Immunol 186:1333-1337.
71. Kuenzel S, Till A, Winkler M, Häsler R, Lipinski S, Jung S, Grötzinger J, Fickenscher H, Schreiber S, Rosenstiel P. 2010. The nucleotidebinding oligomerization domain-like receptor NLRC5 is involved in IFN-dependent antiviral immune responses. J Immunol 184:1990-2000.
72. Lian L, Ciraci C, Chang G, Hu J, Lamont SJ. 2012. NLRC5 knockdown in chicken macrophages alters response to LPS and poly (I:C) stimulation. BMC Vet Res 8:23. doi:10.1186/1746-6148-8-23.
73. Tong Y, Cui J, Li Q, Zou J, Wang HY, Wang RF. 2012. Enhanced TLR-induced NF-κB signaling and type I interferon responses in NLRC5 deficient mice. Cell Res 22:822-835.
74. Ranjan P, Singh N, Kumar A, Neerincx A, Kremmer E, Cao W, Davis WG, Katz JM, Gangappa S, Lin R, Kufer TA, Sambhara S. 2015. NLRC5 interacts with RIG-I to induce a robust antiviral response against influenza virus infection. Eur J Immunol 45:758-772.
75. Boiko JR, Borghesi L. 2012. Hematopoiesis sculpted by pathogens: Toll-like receptors and inflammatory mediators directly activate stem cells. Cytokine 57:1-8.
76. Trumpp A, Essers M, Wilson A. 2010. Awakening dormant haematopoietic stem cells. Nat Rev Immunol 10:201-209.
77. King KY, Goodell MA. 2011. Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nat Rev Immunol 11:685-692.
78. Nagai Y, Garrett KP, Ohta S, Bahrun U, Kouro T, Akira S, Takatsu K, Kincade PW. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24:801-812.
79. + hematopoietic cells mediates induction of cytokines and cell differentiation. J Leukoc Biol 85:939-946.
80. Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N, Moseman EA, Huff IV, Junt T, Wagers AJ, Mazo IB, von Andrian UH. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:994-1008.
81. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. 2010. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 16:228-231.
82. Burberry A, Zeng MY, Ding L, Wicks I, Inohara N, Morrison SJ, Núñez G. 2014. Infection mobilizes hematopoietic stem cells through cooperative NOD-like receptor and Toll-like receptor signaling. Cell Host Microbe 15:779-791.