Regulation of NOD-like receptors and inflammasome activation in cerebral endothelial cells

Journal of Neurochemistry

Volumn 135, Issue 3, 2015, Pages 551-564

  Nagyoszi, Péter ^a   Nyúl Tõth, Ádám ^a   Fazakas, Csilla ^a   Wilhelm, Imola ^a   Kozma, Mihály ^a   Molnár, Judit ^a   Haskõ, János ^a   Krizbai, István A ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

blood brain barrier; cerebral endothelial cells; IL 1 ; inflammasome; NOD like receptors

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CRYOPYRIN; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 33; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MURAMYL DIPEPTIDE; NLRA PROTEIN; NLRC4 PROTEIN; NLRC5 PROTEIN; NLRP1 PROTEIN; NLRP10 PROTEIN; NLRP12 PROTEIN; NLRP5 PROTEIN; NLRP9 PROTEIN; NLRX1 PROTEIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NOD1 PROTEIN, HUMAN; NOD2 PROTEIN, HUMAN;

ARTICLE; BLOOD BRAIN BARRIER; CEREBRAL ENDOTHELIAL CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; NERVOUS SYSTEM INFLAMMATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; ANIMAL; BRAIN; CELL CULTURE; METABOLISM; PHYSIOLOGY; RAT;

ANIMALS; BRAIN; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; INFLAMMASOMES; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; RATS;

EID: 84945180299     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13197     Document Type: Article

References (66)

1. Abbott N. J., (2013) Blood-brain barrier structure and function and the challenges for CNS drug delivery. J. Inherit. Metab. Dis. 36, 437-449.
2. Abulafia D. P., de Rivero Vaccari J. P., Lozano J. D., Lotocki G., Keane R. W., and, Dietrich W. D., (2009) Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J. Cereb. Blood Flow Metab. 29, 534-544.
3. Adamczak S. E., de Rivero Vaccari J. P., Dale G., Brand F. J. 3rd, Nonner D., Bullock M. R., Dahl G. P., Dietrich W. D., and, Keane R. W., (2014) Pyroptotic neuronal cell death mediated by the AIM2 inflammasome. J. Cereb. Blood Flow Metab. 34, 621-629.
4. Agostini L., Martinon F., Burns K., McDermott M. F., Hawkins P. N., and, Tschopp J., (2004) NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 20, 319-325.
5. Anderson P., (2010) Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat. Rev. Immunol. 10, 24-35.
6. Banks W. A., (2014) The blood-brain barrier in neuroimmunology: tales of separation and assimilation. Brain Behav. Immun. 44, 1-8.
7. Bauernfeind F., Ablasser A., Bartok E., Kim S., Schmid-Burgk J., Cavlar T., and, Hornung V., (2011) Inflammasomes: current understanding and open questions. Cell. Mol. Life Sci. 68, 765-783.
8. Benko S., Philpott D. J., and, Girardin S. E., (2008) The microbial and danger signals that activate Nod-like receptors. Cytokine 43, 368-373.
9. Bulau A. M., Nold M. F., Li S., et al,. (2014) Role of caspase-1 in nuclear translocation of IL-37, release of the cytokine, and IL-37 inhibition of innate immune responses. Proc. Natl Acad. Sci. USA 111, 2650-2655.
10. Choubey D., Duan X., Dickerson E., Ponomareva L., Panchanathan R., Shen H., and, Srivastava R., (2010) Interferon-inducible p200-family proteins as novel sensors of cytoplasmic DNA: role in inflammation and autoimmunity. J. Interferon Cytokine Res. 30, 371-380.
11. Coll R. C., Robertson A. A., Chae J. J., et al,. (2015) A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat. Med. 21, 248-255.
12. Cresswell K. S., Clarke C. J., Jackson J. T., Darcy P. K., Trapani J. A., and, Johnstone R. W., (2005) Biochemical and growth regulatory activities of the HIN-200 family member and putative tumor suppressor protein, AIM2. Biochem. Biophys. Res. Commun. 326, 417-424.
13. Denes A., Coutts G., Lenart N., Cruickshank S. M., Pelegrin P., Skinner J., Rothwell N., Allan S. M., and, Brough D., (2015) AIM2 and NLRC4 inflammasomes contribute with ASC to acute brain injury independently of NLRP3. Proc. Natl Acad. Sci. USA 112, 4050-4055.
14. Dinarello C. A., (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550.
15. Fabian G., Szabo C. A., Bozo B., Greenwood J., Adamson P., Deli M. A., Joo F., Krizbai I. A., and, Szucs M., (1998) Expression of G-protein subtypes in cultured cerebral endothelial cells. Neurochem. Int. 33, 179-185.
16. Fabry Z., Fitzsimmons K. M., Herlein J. A., Moninger T. O., Dobbs M. B., and, Hart M. N., (1993) Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J. Neuroimmunol. 47, 23-34.
17. Ferwerda G., Kramer M., de Jong D., et al,. (2008) Engagement of NOD2 has a dual effect on proIL-1beta mRNA transcription and secretion of bioactive IL-1beta. Eur. J. Immunol. 38, 184-191.
18. Ghonime M. G., Shamaa O. R., Das S., Eldomany R. A., Fernandes-Alnemri T., Alnemri E. S., Gavrilin M. A., and, Wewers M. D., (2014) Inflammasome priming by lipopolysaccharide is dependent upon ERK signaling and proteasome function. J. Immunol. 192, 3881-3888.
19. Girardin S. E., Boneca I. G., Viala J., Chamaillard M., Labigne A., Thomas G., Philpott D. J., and, Sansonetti P. J., (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278, 8869-8872.
20. Girvin A. M., Gordon K. B., Welsh C. J., Clipstone N. A., and, Miller S. D., (2002) Differential abilities of central nervous system resident endothelial cells and astrocytes to serve as inducible antigen-presenting cells. Blood 99, 3692-3701.
21. Gutierrez O., Pipaon C., Inohara N., Fontalba A., Ogura Y., Prosper F., Nunez G., and, Fernandez-Luna J. L., (2002) Induction of Nod2 in myelomonocytic and intestinal epithelial cells via nuclear factor-kappa B activation. J. Biol. Chem. 277, 41701-41705.
22. Hakimi M., Peters A., Becker A., Bockler D., and, Dihlmann S., (2014) Inflammation-related induction of absent in melanoma 2 (AIM2) in vascular cells and atherosclerotic lesions suggests a role in vascular pathogenesis. J. Vasc. Surg. 59, 794-803.
23. Halle A., Hornung V., Petzold G. C., Stewart C. R., Monks B. G., Reinheckel T., Fitzgerald K. A., Latz E., Moore K. J., and, Golenbock D. T., (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 9, 857-865.
24. Hanamsagar R., Torres V., and, Kielian T., (2011) Inflammasome activation and IL-1beta/IL-18 processing are influenced by distinct pathways in microglia. J. Neurochem. 119, 736-748.
25. van Heel D. A., Ghosh S., Butler M., et al,. (2005) Muramyl dipeptide and toll-like receptor sensitivity in NOD2-associated Crohn's disease. Lancet 365, 1794-1796.
26. Hisamatsu T., Suzuki M., and, Podolsky D. K., (2003) Interferon-gamma augments CARD4/NOD1 gene and protein expression through interferon regulatory factor-1 in intestinal epithelial cells. J. Biol. Chem. 278, 32962-32968.
27. Hsu L. C., Ali S. R., McGillivray S., et al,. (2008) A NOD2-NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc. Natl Acad. Sci. USA 105, 7803-7808.
28. Inohara N., Ogura Y., Fontalba A., et al,. (2003) Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278, 5509-5512.
29. Kamimura D., Stofkova A., Nishikawa N., Atsumi T., Arima Y., and, Murakami M., (2015) Immune cell gateways in the central nervous system regulated by regional neural stimulations. Clin. Exp. Neuroimmunol. 6, 120-128.
30. King A. E., Horne A. W., Hombach-Klonisch S., Mason J. I., and, Critchley H. O., (2009) Differential expression and regulation of nuclear oligomerization domain proteins NOD1 and NOD2 in human endometrium: a potential role in innate immune protection and menstruation. Mol. Hum. Reprod. 15, 311-319.
31. Krizbai I. A., and, Deli M. A., (2003) Signalling pathways regulating the tight junction permeability in the blood-brain barrier. Cell. Mol. Biol. (Noisy-le-grand). 49, 23-31.
32. Liang L., Tan X., Zhou Q., Zhu Y., Tian Y., Yu H., Kijlstra A., and, Yang P., (2013) IL-1beta triggered by peptidoglycan and lipopolysaccharide through TLR2/4 and ROS-NLRP3 inflammasome-dependent pathways is involved in ocular Behcet's disease. Invest. Ophthalmol. Vis. Sci. 54, 402-414.
33. Martinon F., Burns K., and, Tschopp J., (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10, 417-426.
34. Martinon F., Agostini L., Meylan E., and, Tschopp J., (2004) Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14, 1929-1934.
35. Medzhitov R., (2007) Recognition of microorganisms and activation of the immune response. Nature 449, 819-826.
36. Minkiewicz J., de Rivero Vaccari J. P., and, Keane R. W., (2013) Human astrocytes express a novel NLRP2 inflammasome. Glia 61, 1113-1121.
37. Mo J., Boyle J. P., Howard C. B., Monie T. P., Davis B. K., and, Duncan J. A., (2012) Pathogen sensing by nucleotide-binding oligomerization domain-containing protein 2 (NOD2) is mediated by direct binding to muramyl dipeptide and ATP. J. Biol. Chem. 287, 23057-23067.
38. Mohamed I. N., Ishrat T., Fagan S. C., and, El-Remessy A. B., (2015) Role of inflammasome activation in the pathophysiology of vascular diseases of the neurovascular unit. Antioxid. Redox Signal. 22, 1188-1206.
39. Nagyoszi P., Wilhelm I., Farkas A. E., Fazakas C., Dung N. T., Hasko J., and, Krizbai I. A., (2010) Expression and regulation of toll-like receptors in cerebral endothelial cells. Neurochem. Int. 57, 556-564.
40. Niebuhr M., Baumert K., Heratizadeh A., Satzger I., and, Werfel T., (2014) Impaired NLRP3 inflammasome expression and function in atopic dermatitis due to Th2 milieu. Allergy. 69, 1058-1067.
41. O'Connor W., Jr, Harton J. A., Zhu X., Linhoff M. W., and, Ting J. P., (2003) Cutting edge: CIAS1/cryopyrin/PYPAF1/NALP3/CATERPILLER 1.1 is an inducible inflammatory mediator with NF-kappa B suppressive properties. J. Immunol. 171, 6329-6333.
42. Opitz B., Eitel J., Meixenberger K., and, Suttorp N., (2009) Role of Toll-like receptors, NOD-like receptors and RIG-I-like receptors in endothelial cells and systemic infections. Thromb. Haemost. 102, 1103-1109.
43. Palova-Jelinkova L., Danova K., Drasarova H., et al,. (2013) Pepsin digest of wheat gliadin fraction increases production of IL-1beta via TLR4/MyD88/TRIF/MAPK/NF-kappaB signaling pathway and an NLRP3 inflammasome activation. PLoS ONE 8, e62426.
44. Pan Q., Mathison J., Fearns C., et al,. (2007) MDP-induced interleukin-1beta processing requires Nod2 and CIAS1/NALP3. J. Leukoc. Biol. 82, 177-183.
45. Peterson G. L., (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83, 346-356.
46. Piecyk M., Wax S., Beck A. R., et al,. (2000) TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. EMBO J. 19, 4154-4163.
47. Pontillo A., Girardelli M., Agostinis C., Masat E., Bulla R., and, Crovella S., (2013) Bacterial LPS differently modulates inflammasome gene expression and IL-1beta secretion in trophoblast cells, decidual stromal cells, and decidual endothelial cells. Reprod. Sci. 20, 563-566.
48. Qiao Y., Wang P., Qi J., Zhang L., and, Gao C., (2012) TLR-induced NF-kappaB activation regulates NLRP3 expression in murine macrophages. FEBS Lett. 586, 1022-1026.
49. Reimer T., Shaw M. H., Franchi L., Coban C., Ishii K. J., Akira S., Horii T., Rodriguez A., and, Nunez G., (2010) Experimental cerebral malaria progresses independently of the Nlrp3 inflammasome. Eur. J. Immunol. 40, 764-769.
50. de Rivero Vaccari J. P., Lotocki G., Marcillo A. E., Dietrich W. D., and, Keane R. W., (2008) A molecular platform in neurons regulates inflammation after spinal cord injury. J. Neurosci. 28, 3404-3414.
51. Rosenstiel P., Fantini M., Brautigam K., Kuhbacher T., Waetzig G. H., Seegert D., and, Schreiber S., (2003) TNF-alpha and IFN-gamma regulate the expression of the NOD2 (CARD15) gene in human intestinal epithelial cells. Gastroenterology 124, 1001-1009.
52. Shaw P. J., Lamkanfi M., and, Kanneganti T. D., (2010) NOD-like receptor (NLR) signaling beyond the inflammasome. Eur. J. Immunol. 40, 624-627.
53. Shimogaki S., Ito S., Komatsu S., Koike R., Miyasaka N., Umezawa K., and, Kubota T., (2014) Inhibition of the NF-kappaB pathway as a candidate therapeutic strategy for cryopyrin-associated periodic syndrome. Mod. Rheumatol. 24, 517-524.
54. Simard J. C., Cesaro A., Chapeton-Montes J., Tardif M., Antoine F., Girard D., and, Tessier P. A., (2013) S100A8 and S100A9 induce cytokine expression and regulate the NLRP3 inflammasome via ROS-dependent activation of NF-kappaB(1.). PLoS ONE 8, e72138.
55. Strowig T., Henao-Mejia J., Elinav E., and, Flavell R., (2012) Inflammasomes in health and disease. Nature 481, 278-286.
56. Takeuchi O., and, Akira S., (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820.
57. Tangi T. N., Elmabsout A. A., Bengtsson T., Sirsjo A., and, Fransen K., (2012) Role of NLRP3 and CARD8 in the regulation of TNF-alpha induced IL-1beta release in vascular smooth muscle cells. Int. J. Mol. Med. 30, 697-702.
58. Ting J. P., Lovering R. C., Alnemri E. S., et al,. (2008) The NLR gene family: a standard nomenclature. Immunity 28, 285-287.
59. Verma S., Nakaoke R., Dohgu S., and, Banks W. A., (2006) Release of cytokines by brain endothelial cells: a polarized response to lipopolysaccharide. Brain Behav. Immun. 20, 449-455.
60. Villegas L. R., Kluck D., Field C., Oberley-Deegan R. E., Woods C., Yeager M. E., El Kasmi K. C., Savani R. C., Bowler R. P., and, Nozik-Grayck E., (2013) Superoxide dismutase mimetic, MnTE-2-PyP, attenuates chronic hypoxia-induced pulmonary hypertension, pulmonary vascular remodeling, and activation of the NALP3 inflammasome. Antioxid. Redox Signal. 18, 1753-1764.
61. Weksler B. B., Subileau E. A., Perriere N., et al,. (2005) Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 19, 1872-1874.
62. Wilhelm I., Nagyoszi P., Farkas A. E., et al,. (2008) Hyperosmotic stress induces Axl activation and cleavage in cerebral endothelial cells. J. Neurochem. 107, 116-126.
63. Windheim M., Lang C., Peggie M., Plater L. A., and, Cohen P., (2007) Molecular mechanisms involved in the regulation of cytokine production by muramyl dipeptide. Biochem. J. 404, 179-190.
64. Zhang P., Dixon M., Zucchelli M., Hambiliki F., Levkov L., Hovatta O., and, Kere J., (2008) Expression analysis of the NLRP gene family suggests a role in human preimplantation development. PLoS ONE 3, e2755.
65. Zhang L., Lu R., Zhao G., Pflugfelder S. C., and, Li D. Q., (2011) TLR-mediated induction of pro-allergic cytokine IL-33 in ocular mucosal epithelium. Int. J. Biochem. Cell Biol. 43, 1383-1391.
66. Zhang Y. Y., Chen H., Sun C., Wang H. Z., Liu M. L., Li Y. Y., Nie X. L., Du M. R., Li D. J., and, Zhang J. P., (2014) Expression and functional characterization of NOD2 in decidual stromal cells isolated during the first trimester of pregnancy. PLoS ONE 9, e99612.