Sensing soluble uric acid by Naip1-Nlrp3 platform.


Journal

Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092

Informations de publication

Date de publication:
05 02 2021
Historique:
received: 17 11 2020
accepted: 15 01 2021
revised: 11 01 2021
entrez: 6 2 2021
pubmed: 7 2 2021
medline: 14 9 2021
Statut: epublish

Résumé

Uric acid (UA), a product of purine nucleotide degradation able to initiate an immune response, represents a breakpoint in the evolutionary history of humans, when uricase, the enzyme required for UA cleavage, was lost. Despite being inert in human cells, UA in its soluble form (sUA) can increase the level of interleukin-1β (IL-1β) in murine macrophages. We, therefore, hypothesized that the recognition of sUA is achieved by the Naip1-Nlrp3 inflammasome platform. Through structural modelling predictions and transcriptome and functional analyses, we found that murine Naip1 expression in human macrophages induces IL-1β expression, fatty acid production and an inflammation-related response upon sUA stimulation, a process reversed by the pharmacological and genetic inhibition of Nlrp3. Moreover, molecular interaction experiments showed that Naip1 directly recognizes sUA. Accordingly, Naip may be the sUA receptor lost through the human evolutionary process, and a better understanding of its recognition may lead to novel anti-hyperuricaemia therapies.

Identifiants

pubmed: 33547278
doi: 10.1038/s41419-021-03445-w
pii: 10.1038/s41419-021-03445-w
pmc: PMC7864962
doi:

Substances chimiques

Fatty Acids 0
IL1B protein, human 0
Inflammasomes 0
Interleukin-1beta 0
NAIP protein, human 0
NLR Family, Pyrin Domain-Containing 3 Protein 0
NLRP3 protein, human 0
Naip1 protein, mouse 0
Neuronal Apoptosis-Inhibitory Protein 0
Nlrp3 protein, mouse 0
Uric Acid 268B43MJ25

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

158

Références

Land, W. G. How evolution tells us to induce allotolerance. Exp. Clin. Transplant. 13, 46–54 (2015).
pubmed: 25894127
Bottomly, K. & Janeway, C. A. Jr. Antigen presentation by B cells. Nature 337, 24 (1989).
pubmed: 2562905 doi: 10.1038/337024a0
Janeway, C. A. Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54, 1–13 (1989).
pubmed: 2700931 doi: 10.1101/SQB.1989.054.01.003
Janeway, C. A. Jr. The priming of helper T cells. Semin. Immunol. 1, 13–20 (1989).
pubmed: 15630955
Burnet, F. M. The immunological significance of the thymus: an extension of the clonal selection theory of immunity. Australas. Ann. Med. 11, 79–91 (1962).
pubmed: 13874950 doi: 10.1111/imj.1962.11.2.79
Matzinger, P. The danger model: a renewed sense of self. Science 296, 301–5 (2002).
pubmed: 11951032 doi: 10.1126/science.1071059
Matzinger, P. An innate sense of danger. Semin. Immunol. 10, 399–415 (1998).
pubmed: 9840976 doi: 10.1006/smim.1998.0143
So, A. & Thorens, B. Uric acid transport and disease. J. Clin. Investig. 120, 1791–9 (2010).
pubmed: 20516647 doi: 10.1172/JCI42344 pmcid: 2877959
Shi, Y., Evans, J. E. & Rock, K. L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425, 516–21 (2003).
pubmed: 14520412 doi: 10.1038/nature01991
Martinon, F., Petrilli, V., Mayor, A., Tardivel, A. & Tschopp, J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237–41 (2006).
pubmed: 16407889 doi: 10.1038/nature04516
Compston, A. & Coles, A. Multiple sclerosis. Lancet 359, 1221–31 (2002).
pubmed: 11955556 doi: 10.1016/S0140-6736(02)08220-X
Di Giovine, F. S., Malawista, S. E., Nuki, G. & Duff, G. W. Interleukin 1 (IL 1) as a mediator of crystal arthritis. Stimulation of T cell and synovial fibroblast mitogenesis by urate crystal-induced IL 1. J. Immunol. 138, 3213–8 (1987).
pubmed: 3033070 doi: 10.4049/jimmunol.138.10.3213
Martinon, F., Burns, K. & Tschopp, J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10, 417–26 (2002).
pubmed: 12191486 doi: 10.1016/S1097-2765(02)00599-3
Jones, J. D., Vance, R. E. & Dangl, J. L. Intracellular innate immune surveillance devices in plants and animals. Science 354, 6316 (2016).
doi: 10.1126/science.aaf6395
Mondragón-Palomino, M., Stam, R., John-Arputharaj, A. & Dresselhaus, T. Diversification of defensins and NLRs in Arabidopsis species by different evolutionary mechanisms. BMC Evol. Biol. 17, 255 (2017).
pubmed: 29246101 pmcid: 5731061 doi: 10.1186/s12862-017-1099-4
Braga, T. T., Forni, M. F., Correa-Costa, M., Ramos, R. N., Barbuto, J. A. & Branco, P. et al. Soluble uric acid activates the NLRP3 inflammasome. Sci. Rep. 7, 39884 (2017).
pubmed: 28084303 pmcid: 5233987 doi: 10.1038/srep39884
Kingsbury, S. R., Conaghan, P. G. & McDermott, M. F. The role of the NLRP3 inflammasome in gout. J. Inflamm. Res. 4, 39–49 (2011).
pubmed: 22096368 pmcid: 3218743
Martillo, M. A., Nazzal, L. & Crittenden, D. B. The crystallization of monosodium urate. Curr. Rheumatol. Rep. 16, 400 (2014).
pubmed: 24357445 pmcid: 3975080 doi: 10.1007/s11926-013-0400-9
Kratzer, J. T., Lanaspa, M. A., Murphy, M. N., Cicerchi, C., Graves, C. L. & Tipton, P. A. et al. Evolutionary history and metabolic insights of ancient mammalian uricases. Proc. Natl Acad. Sci. USA 111, 3763–8 (2014).
pubmed: 24550457 doi: 10.1073/pnas.1320393111 pmcid: 3956161
Kono, H., Chen, C. J., Ontiveros, F. & Rock, K. L. Uric acid promotes an acute inflammatory response to sterile cell death in mice. J. Clin. Investig. 120, 1939–49 (2010).
pubmed: 20501947 doi: 10.1172/JCI40124 pmcid: 2877935
Cicerchi, C., Li, N., Kratzer, J., Garcia, G., Roncal-Jimenez, C. A. & Tanabe, K. et al. Uric acid-dependent inhibition of AMP kinase induces hepatic glucose production in diabetes and starvation: evolutionary implications of the uricase loss in hominids. FASEB J. 28, 3339–50 (2014).
pubmed: 24755741 pmcid: 4101654 doi: 10.1096/fj.13-243634
Hafner, S. & Weitzman, J. Of mice and men-NAIP homologues face Legionella pneumophila. Microbes Infect. / Inst. Pasteur 14, 1119–22 (2012).
doi: 10.1016/j.micinf.2012.07.010
Diez, E., Lee, S. H., Gauthier, S., Yaraghi, Z., Tremblay, M. & Vidal, S. et al. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33, 55–60 (2003).
pubmed: 12483212 doi: 10.1038/ng1065
Wright, E. K., Goodart, S. A., Growney, J. D., Hadinoto, V., Endrizzi, M. G. & Long, E. M. et al. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13, 27–36 (2003).
pubmed: 12526741 doi: 10.1016/S0960-9822(02)01359-3
Miao, E. A., Mao, D. P., Yudkovsky, N., Bonneau, R., Lorang, C. G. & Warren, S. E. et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl Acad. Sci. USA 107, 3076–80 (2010).
pubmed: 20133635 doi: 10.1073/pnas.0913087107 pmcid: 2840275
Rayamajhi, M., Zak, D. E., Chavarria-Smith, J., Vance, R. E. & Miao, E. A. Cutting edge: mouse NAIP1 detects the type III secretion system needle protein. J. Immunol. 191, 3986–9 (2013).
pubmed: 24043898 doi: 10.4049/jimmunol.1301549
Zhao, Y., Yang, J., Shi, J., Gong, Y. N., Lu, Q. & Xu, H. et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477, 596–600 (2011).
pubmed: 21918512 doi: 10.1038/nature10510
Ren, T., Zamboni, D. S., Roy, C. R., Dietrich, W. F. & Vance, R. E. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2, e18 (2006).
pubmed: 16552444 pmcid: 1401497 doi: 10.1371/journal.ppat.0020018
Katagiri, N., Shobuike, T., Chang, B., Kukita, A. & Miyamoto, H. The human apoptosis inhibitor NAIP induces pyroptosis in macrophages infected with Legionella pneumophila. Microbes Infect. 14, 1123–32 (2012).
pubmed: 22504023 doi: 10.1016/j.micinf.2012.03.006
Zamboni, D. S., Kobayashi, K. S., Kohlsdorf, T., Ogura, Y., Long, E. M. & Vance, R. E. et al. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7, 318–25 (2006).
pubmed: 16444259 doi: 10.1038/ni1305
Hornung, V., Bauernfeind, F., Halle, A., Samstad, E. O., Kono, H. & Rock, K. L. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847–56 (2008).
pubmed: 18604214 pmcid: 2834784 doi: 10.1038/ni.1631
Schmid-Burgk, J. L., Höning, K., Ebert, T. S. & Hornung, V. CRISPaint allows modular base-specific gene tagging using a ligase-4-dependent mechanism. Nat. Commun. 7, 12338 (2016).
pubmed: 27465542 pmcid: 4974478 doi: 10.1038/ncomms12338
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–20 (2014).
pubmed: 24695404 pmcid: 4103590 doi: 10.1093/bioinformatics/btu170
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–60 (2015).
pubmed: 25751142 pmcid: 4655817 doi: 10.1038/nmeth.3317
Pertea, M., Pertea, G. M., Antonescu, C. M., Chang, T. C., Mendell, J. T. & Salzberg, S. L. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–5 (2015).
pubmed: 25690850 pmcid: 4643835 doi: 10.1038/nbt.3122
Frazee, A. C., Pertea, G., Jaffe, A. E., Langmead, B., Salzberg, S. L. & Leek, J. T. Ballgown bridges the gap between transcriptome assembly and expression analysis. Nat. Biotechnol. 33, 243–6 (2015).
pubmed: 25748911 pmcid: 4792117 doi: 10.1038/nbt.3172
Pertea, M., Kim, D., Pertea, G. M., Leek, J. T. & Salzberg, S. L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 11, 1650–67 (2016).
pubmed: 27560171 pmcid: 5032908 doi: 10.1038/nprot.2016.095
Homola, J. Surface plasmon resonance sensors for detection of chemical and biological species. Chem. Rev. 108, 462–93 (2008).
pubmed: 18229953 doi: 10.1021/cr068107d
Souto, D. E., Faria, A. R., de Andrade, H. M. & Kubota, L. T. Using QCM and SPR for the kinetic evaluation of the binding between a new recombinant chimeric protein and specific antibodies of the visceral leishmaniasis. Curr. Protein Pept. Sci. 16, 782–90 (2015).
pubmed: 25961398 doi: 10.2174/1389203716666150505230416
Sali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815 (1993).
pubmed: 8254673 doi: 10.1006/jmbi.1993.1626
Hu, Z., Yan, C., Liu, P., Huang, Z., Ma, R. & Zhang, C. et al. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341, 172–5 (2013).
pubmed: 23765277 doi: 10.1126/science.1236381
Guerois, R., Nielsen, J. E. & Serrano, L. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol. 320, 369–87 (2002).
pubmed: 12079393 doi: 10.1016/S0022-2836(02)00442-4
Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M. & Meng, E. C. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–12 (2004).
pubmed: 15264254 doi: 10.1002/jcc.20084
Jurrus, E., Engel, D., Star, K., Monson, K., Brandi, J. & Felberg, L. E. et al. Improvements to the APBS biomolecular solvation software suite. Protein Sci. 27, 112–28 (2018).
pubmed: 28836357 doi: 10.1002/pro.3280
Dolinsky, T. J., Nielsen, J. E., McCammon, J. A. & Baker, N. A. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665–W667 (2004).
pubmed: 15215472 pmcid: 441519 doi: 10.1093/nar/gkh381
Grosdidier, A., Zoete, V. & Michielin, O. SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res. 39, W270–W277 (2011).
pubmed: 21624888 pmcid: 3125772 doi: 10.1093/nar/gkr366
Patschan, D., Patschan, S., Gobe, G. G., Chintala, S. & Goligorsky, M. S. Uric acid heralds ischemic tissue injury to mobilize endothelial progenitor cells. J. Am. Soc. Nephrol. 18, 1516–24 (2007).
pubmed: 17409313 doi: 10.1681/ASN.2006070759
Coll, R. C., Robertson, A., Butler, M., Cooper, M. & O’Neill, L. A. The cytokine release inhibitory drug CRID3 targets ASC oligomerisation in the NLRP3 and AIM2 inflammasomes. PLoS ONE 6, e29539 (2011).
pubmed: 22216309 pmcid: 3245271 doi: 10.1371/journal.pone.0029539
Lanaspa, M. A., Sanchez-Lozada, L. G., Choi, Y. J., Cicerchi, C., Kanbay, M. & Roncal-Jimenez, C. A. et al. Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J. Biol. Chem. 287, 40732–44 (2012).
pubmed: 23035112 pmcid: 3504786 doi: 10.1074/jbc.M112.399899
Kuznetsov, A. V., Margreiter, R., Amberger, A., Saks, V. & Grimm, M. Changes in mitochondrial redox state, membrane potential and calcium precede mitochondrial dysfunction in doxorubicin-induced cell death. Biochim. Biophys. Acta 1813, 1144–52 (2011).
pubmed: 21406203 doi: 10.1016/j.bbamcr.2011.03.002
Sborov, D. W., Haverkos, B. M. & Harris, P. J. Investigational cancer drugs targeting cell metabolism in clinical development. Expert Opin. Investig. Drugs 24, 79–94 (2015).
pubmed: 25224845 doi: 10.1517/13543784.2015.960077
O’Neill, L. Immunometabolism and the land of milk and honey. Nat. Rev. Immunol. 17, 217 (2017).
pubmed: 28287105 doi: 10.1038/nri.2017.22
Moon, J. S., Lee, S., Park, M. A., Siempos, II., Haslip, M. & Lee, P. J. et al. UCP2-induced fatty acid synthase promotes NLRP3 inflammasome activation during sepsis. J. Clin. Investig. 125, 665–80 (2015).
pubmed: 25574840 doi: 10.1172/JCI78253 pmcid: 4319445
Ralston, J. C., Lyons, C. L., Kennedy, E. B., Kirwan, A. M. & Roche, H. M. Fatty acids and NLRP3 inflammasome-mediated inflammation in metabolic tissues. Annu. Rev. Nutr. 37, 77–102 (2017).
pubmed: 28826373 doi: 10.1146/annurev-nutr-071816-064836
Xing, J. H., Li, R., Gao, Y. Q., Wang, M. Y., Liu, Y. Z. & Hong, J. et al. NLRP3 inflammasome mediate palmitate-induced endothelial dysfunction. Life Sci. 239, 116882 (2019).
pubmed: 31705915 doi: 10.1016/j.lfs.2019.116882
Huynh, K., Pernes, G., Mellett, N. A., Meikle, P. J., Murphy, A. J. & Lancaster, G. I. Lipidomic profiling of murine macrophages treated with fatty acids of varying chain length and saturation status. Metabolites 8, 2 (2018).
doi: 10.3390/metabo8020029
Zhang, L., Chen, S., Ruan, J., Wu, J., Tong, A. B. & Yin, Q. et al. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science 350, 404–9 (2015).
pubmed: 26449474 pmcid: 4640189 doi: 10.1126/science.aac5789
Hauenstein, A. V., Zhang, L. & Wu, H. The hierarchical structural architecture of inflammasomes, supramolecular inflammatory machines. Curr. Opin. Struct. Biol. 31, 75–83 (2015).
pubmed: 25881155 pmcid: 4476925 doi: 10.1016/j.sbi.2015.03.014
Nichols, R. D., von Moltke, J. & Vance, R. E. NAIP/NLRC4 inflammasome activation in MRP8. Nat. Commun. 8, 2209 (2017).
pubmed: 29263322 pmcid: 5738432 doi: 10.1038/s41467-017-02266-w
Dalbeth, N., Choi, H. K., Joosten, L. A. B., Khanna, P. P., Matsuo, H. & Perez-Ruiz, F. et al. Gout. Nat. Rev. Dis. Prim. 5, 69 (2019).
pubmed: 31558729 doi: 10.1038/s41572-019-0115-y
Qu, Y., Misaghi, S., Newton, K., Maltzman, A., Izrael-Tomasevic, A. & Arnott, D. et al. NLRP3 recruitment by NLRC4 during Salmonella infection. J. Exp. Med. 213, 877–85 (2016).
pubmed: 27139490 pmcid: 4886354 doi: 10.1084/jem.20132234
Liston, A. & Masters, S. L. Homeostasis-altering molecular processes as mechanisms of inflammasome activation. Nat. Rev. Immunol. 17, 208–14 (2017).
pubmed: 28163301 doi: 10.1038/nri.2016.151
Byeon, H. E., Jeon, J. Y., Kim, H. J., Kim, D. J., Lee, K. W. & Kang, Y. et al. MicroRNA-132 negatively regulates palmitate-induced NLRP3 inflammasome activation through FOXO3 down-regulation in THP-1 cells. Nutrients 9, 12 (2017).
doi: 10.3390/nu9121370
Wang, L., Chen, Y., Li, X., Zhang, Y. & Gulbins, E. Enhancement of endothelial permeability by free fatty acid through lysosomal cathepsin B-mediated Nlrp3 inflammasome activation. Oncotarget 7, 73229–41 (2016).
pubmed: 27689324 pmcid: 5341975 doi: 10.18632/oncotarget.12302
Terlizzi, M., Colarusso, C., Popolo, A., Pinto, A. & Sorrentino, R. IL-1α and IL-1β-producing macrophages populate lung tumor lesions in mice. Oncotarget 7, 58181–92 (2016).
pubmed: 27528423 pmcid: 5295423 doi: 10.18632/oncotarget.11276
Tapia, E., Cristóbal, M., García-Arroyo, F. E., Soto, V., Monroy-Sánchez, F. & Pacheco, U. et al. Synergistic effect of uricase blockade plus physiological amounts of fructose-glucose on glomerular hypertension and oxidative stress in rats. Am. J. Physiol. Ren. Physiol. 304, F727–36 (2013).
doi: 10.1152/ajprenal.00485.2012
Soltani, Z., Rasheed, K., Kapusta, D. R. & Reisin, E. Potential role of uric acid in metabolic syndrome, hypertension, kidney injury, and cardiovascular diseases: is it time for reappraisal? Curr. Hypertens. Rep. 15, 175–81 (2013).
pubmed: 23588856 pmcid: 3736857 doi: 10.1007/s11906-013-0344-5
Kanbay, M., Afsar, B., Siriopol, D., Unal, H. U., Karaman, M. & Saglam, M. et al. Relevance of uric acid and asymmetric dimethylarginine for modeling cardiovascular risk prediction in chronic kidney disease patients. Int. Urol. Nephrol. 48, 1129–36 (2016).
pubmed: 27007614 doi: 10.1007/s11255-016-1271-6
Smith, K. A., Pearson, C. B., Hachey, A. M., Xia, D. L. & Wachtman, L. M. Alternative activation of macrophages in rhesus macaques (Macaca mulatta) with endometriosis. Comp. Med. 62, 303–10 (2012).
pubmed: 23043784 pmcid: 3415373
Friedman, E. M., Reyes, T. M. & Coe, C. L. Context-dependent behavioral effects of interleukin-1 in the rhesus monkey (Macaca mulatta). Psychoneuroendocrinology 21, 455–68 (1996).
pubmed: 8888368 doi: 10.1016/0306-4530(96)00010-8
Burm, S. M., Peferoen, L. A., Zuiderwijk-Sick, E. A., Haanstra, K. G., ‘t Hart, B. A. & van der Valk, P. et al. Expression of IL-1β in rhesus EAE and MS lesions is mainly induced in the CNS itself. J. Neuroinflamm. 13, 138 (2016).
doi: 10.1186/s12974-016-0605-8
So, A. K. & Martinon, F. Inflammation in gout: mechanisms and therapeutic targets. Nat. Rev. Rheumatol. 13, 639–47 (2017).
pubmed: 28959043 doi: 10.1038/nrrheum.2017.155
Alper, A. B., Chen, W., Yau, L., Srinivasan, S. R., Berenson, G. S. & Hamm, L. L. Childhood uric acid predicts adult blood pressure: the Bogalusa Heart Study. Hypertension 45, 34–8 (2005).
pubmed: 15569853 doi: 10.1161/01.HYP.0000150783.79172.bb
Tang, W., Hong, Y., Province, M. A., Rich, S. S., Hopkins, P. N. & Arnett, D. K. et al. Familial clustering for features of the metabolic syndrome: the National Heart, Lung, and Blood Institute (NHLBI) Family Heart Study. Diabetes Care 29, 631–6 (2006).
pubmed: 16505518 doi: 10.2337/diacare.29.03.06.dc05-0679
Perticone, M., Tripepi, G., Maio, R., Cimellaro, A., Addesi, D. & Baggetta, R. et al. Risk reclassification ability of uric acid for cardiovascular outcomes in essential hypertension. Int. J. Cardiol. 243, 473–8 (2017).
pubmed: 28528984 doi: 10.1016/j.ijcard.2017.05.051
Lee, J. E., Kim, Y. G., Choi, Y. H., Huh, W., Kim, D. J. & Oh, H. Y. Serum uric acid is associated with microalbuminuria in prehypertension. Hypertension 47, 962–7 (2006).
pubmed: 16520402 doi: 10.1161/01.HYP.0000210550.97398.c2
Prattichizzo, F., De Nigris, V., Spiga, R., Mancuso, E., La Sala, L. & Antonicelli, R. et al. Inflammageing and metaflammation: the yin and yang of type 2 diabetes. Ageing Res. Rev. 41, 1–17 (2018).
pubmed: 29081381 doi: 10.1016/j.arr.2017.10.003
Hotamisligil, G. S. Inflammation, metaflammation and immunometabolic disorders. Nature 542, 177–85 (2017).
doi: 10.1038/nature21363 pubmed: 28179656
Christ, A., Lauterbach, M. & Latz, E. Western diet and the immune system: an inflammatory connection. Immunity 51, 794–811 (2019).
pubmed: 31747581 doi: 10.1016/j.immuni.2019.09.020

Auteurs

Tarcio Teodoro Braga (TT)

Department of Basic Pathology, Federal University of Parana, Curitiba, PR, Brazil. tarcio.braga@ufpr.br.
Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil. tarcio.braga@ufpr.br.
Institute of Innate Immunity, University Hospitals Bonn, Bonn, Germany. tarcio.braga@ufpr.br.

Mariana Rodrigues Davanso (MR)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.
Institute of Innate Immunity, University Hospitals Bonn, Bonn, Germany.
Department of Physiology and Biophysics, Institute of Biomedical Sciences I, University of Sao Paulo, São Paulo, SP, Brazil.

Davi Mendes (D)

Department of Microbiology, Institute of Biomedical Sciences II, University of São Paulo, São Paulo, SP, Brazil.

Tiago Antonio de Souza (TA)

Department of Microbiology, Institute of Biomedical Sciences II, University of São Paulo, São Paulo, SP, Brazil.

Anderson Fernandes de Brito (AF)

Department of Life Sciences, Imperial College London, London, SW7 2AZ, UK.

Mario Costa Cruz (MC)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.

Meire Ioshie Hiyane (MI)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.

Dhemerson Souza de Lima (DS)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.

Vinicius Nunes (V)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.

Juliana de Fátima Giarola (J)

Institute of Chemistry, University of Campinas, Campinas, SP, Brazil.

Denio Emanuel Pires Souto (DEP)

Institute of Chemistry, University of Campinas, Campinas, SP, Brazil.
Department of Chemistry, Federal University of Parana, Curitiba, PR, Brazil.

Tomasz Próchnicki (T)

Institute of Innate Immunity, University Hospitals Bonn, Bonn, Germany.

Mario Lauterbach (M)

Institute of Innate Immunity, University Hospitals Bonn, Bonn, Germany.

Stellee Marcela Petris Biscaia (SMP)

Department of Cellular Biology, Federal University of Parana, Curitiba, PR, Brazil.

Rilton Alves de Freitas (RA)

Department of Chemistry, Federal University of Parana, Curitiba, PR, Brazil.

Rui Curi (R)

Department of Physiology and Biophysics, Institute of Biomedical Sciences I, University of Sao Paulo, São Paulo, SP, Brazil.
Interdisciplinary Post-Graduate Program in Health Sciences, Cruzeiro do Sul University, São Paulo, Brazil.

Alessandra Pontillo (A)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.

Eicke Latz (E)

Institute of Innate Immunity, University Hospitals Bonn, Bonn, Germany.
Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA, 01655, USA.
Centre for Molecular Inflammation Research (CEMIR), Norwegian University of Science and Technology, 7491, Trondheim, Norway.

Niels Olsen Saraiva Camara (NOS)

Department of Immunology, Institute of Biomedical Sciences IV, University of São Paulo, São Paulo, SP, Brazil.
Nephrology Division, Federal University of São Paulo, São Paulo, SP, Brazil.
Renal Physiopathology Laboratory, Faculty of Medicine, University of São Paulo, São Paulo, SP, Brazil.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH