Stock Ticker

NK cell-derived IFNγ mobilizes free fatty acids from adipose tissue to promote early B cell activation during viral infection

  • Vollmer-Conna, U. et al. Production of pro-inflammatory cytokines correlates with the symptoms of acute sickness behaviour in humans. Psychol. Med. 34, 1289–1297 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wensveen, F. M., Sestan, M. & Polic, B. The immunology of sickness metabolism. Cell Mol. Immunol. 21, 1051–1065 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aviello, G., Cristiano, C., Luckman, S. M. & D’Agostino, G. Brain control of appetite during sickness. Br. J. Pharmacol. 178, 2096–2110 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Francesconi, W. et al. The proinflammatory cytokine interleukin 18 regulates feeding by acting on the bed nucleus of the stria terminalis. J. Neurosci. 36, 5170–5180 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Grunfeld, C. et al. Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters. J. Clin. Invest. 97, 2152–2157 (1996).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tizard, I. Sickness behavior, its mechanisms and significance. Anim. Health Res Rev. 9, 87–99 (2008).

    Article 
    PubMed 

    Google Scholar
     

  • Baazim, H. et al. CD8(+) T cells induce cachexia during chronic viral infection. Nat. Immunol. 20, 701–710 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Marchingo, J. M. & Cantrell, D. A. Protein synthesis, degradation, and energy metabolism in T cell immunity. Cell Mol. Immunol. 19, 303–315 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kohlgruber, A. C. et al. γδT cells producing interleukin-17A regulate adipose regulatory T cell homeostasis and thermogenesis. Nat. Immunol. 19, 464–474 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, D. et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332, 243–247 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wensveen, F. M. et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat. Immunol. 16, 376–385 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lolmede, K., Duffaut, C., Zakaroff-Girard, A. & Bouloumie, A. Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metab. 37, 283–290 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lu, J., Zhao, J., Meng, H. & Zhang, X. Adipose tissue-resident immune cells in obesity and type 2 diabetes. Front. Immunol. 10, 1173 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deiuliis, J. et al. Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers. PLoS ONE 6, e16376 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Goldberg, E. L. et al. Ketogenesis activates metabolically protective γδT cells in visceral adipose tissue. Nat. Metab. 2, 50–61 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stoeckle, M., Kaech, C., Trampuz, A. & Zimmerli, W. The role of diabetes mellitus in patients with bloodstream infections. Swiss Med. Wkly 138, 512–519 (2008).

    CAS 
    PubMed 

    Google Scholar
     

  • Pugliese, G. et al. Obesity and infectious diseases: pathophysiology and epidemiology of a double pandemic condition. Int J. Obes. 46, 449–465 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Wensveen, F. M., Sestan, M., Turk Wensveen, T. & Polic, B. Beauty and the beast in infection: How immune-endocrine interactions regulate systemic metabolism in the context of infection. Eur. J. Immunol. 49, 982–995 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sacher, T. et al. The major virus-producing cell type during murine cytomegalovirus infection, the hepatocyte, is not the source of virus dissemination in the host. Cell Host Microbe 3, 263–272 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Clausen, B. E., Burkhardt, C., Reith, W., Renkawitz, R. & Forster, I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265–277 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kisanuki, Y. Y. et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230–242 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Eguchi, J. et al. Transcriptional control of adipose lipid handling by IRF4. Cell Metab. 13, 249–259 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mogensen, T. H. & Paludan, S. R. Molecular pathways in virus-induced cytokine production. Microbiol Mol. Biol. Rev. 65, 131–150 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sestan, M. et al. An IFNγ-dependent immune-endocrine circuit lowers blood glucose to potentiate the innate antiviral immune response. Nat. Immunol. 25, 981–993 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zebisch, K., Voigt, V., Wabitsch, M. & Brandsch, M. Protocol for effective differentiation of 3T3-L1 cells to adipocytes. Anal. Biochem. 425, 88–90 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lopez-Ortega, O. et al. The immune response in adipocytes and their susceptibility to infection: a possible relationship with infectobesity. Int. J. Mol. Sci. 23, 6154 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ha, C. W. Y. et al. Translocation of viable gut microbiota to mesenteric adipose drives formation of creeping fat in humans. Cell 183, 666–683 e617 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sestan, M. et al. Virus-induced interferon-γ causes insulin resistance in skeletal muscle and derails glycemic control in obesity. Immunity 49, 164–177 e166 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B. & Lanier, L. L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323–1326 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gorjao, R., Cury-Boaventura, M. F., de Lima, T. M. & Curi, R. Regulation of human lymphocyte proliferation by fatty acids. Cell Biochem. Funct. 25, 305–315 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ioan-Facsinay, A. et al. Adipocyte-derived lipids modulate CD4+ T-cell function. Eur. J. Immunol. 43, 1578–1587 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shaikh, S. R. et al. Differential effects of a saturated and a monounsaturated fatty acid on MHC class I antigen presentation. Scand. J. Immunol. 68, 30–42 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ohno, M. et al. The elucidation of plasma lipidome profiles during severe influenza in a mouse model. Sci. Rep. 13, 14210 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Weisel, F. J. et al. Germinal center B cells selectively oxidize fatty acids for energy while conducting minimal glycolysis. Nat. Immunol. 21, 331–342 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu, Q. et al. The role of B cells in the development of CD4 effector T cells during a polarized Th2 immune response. J. Immunol. 179, 3821–3830 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yew Tan, C. et al. Adipose tissue fatty acid chain length and mono-unsaturation increases with obesity and insulin resistance. Sci. Rep. 5, 18366 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barberis, E. et al. Large-scale plasma analysis revealed new mechanisms and molecules associated with the host response to SARS-CoV-2. Int. J. Mol. Sci. 21, 8623 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arguello, R. J. et al. SCENITH: a flow cytometry-based method to functionally profile energy metabolism with single-cell resolution. Cell Metab. 32, 1063–1075 e1067 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gu, H., Zou, Y. R. & Rajewsky, K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 73, 1155–1164 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Flechtner-Mors, M., Jenkinson, C. P., Alt, A., Adler, G. & Ditschuneit, H. H. Effects of acipimox on the lipolysis rate in subcutaneous adipose tissue of obese subjects. Diabetes Metab. Res Rev. 17, 387–390 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vremec, D., Pooley, J., Hochrein, H., Wu, L. & Shortman, K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164, 2978–2986 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • He, C. et al. CD36 and LC3B initiated autophagy in B cells regulates the humoral immune response. Autophagy 17, 3577–3591 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coelho, M., Oliveira, T. & Fernandes, R. Biochemistry of adipose tissue: an endocrine organ. Arch. Med. Sci.: AMS 9, 191–200 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ibrahim, M. M. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes. Rev. 11, 11–18 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Altintas, M. M. et al. Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice. J. Lipid Res. 52, 480–488 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Douglas, A. et al. Rhythmic IL-17 production by γδT cells maintains adipose de novo lipogenesis. Nature 636, 206–214 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • LaMarche, N. M. et al. Distinct iNKT cell populations use IFNγ or ER Stress-Induced IL-10 to control adipose tissue homeostasis. Cell Metab. 32, 243–258 e246 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chavakis, T., Alexaki, V. I. & Ferrante, A. W. Jr. Macrophage function in adipose tissue homeostasis and metabolic inflammation. Nat. Immunol. 24, 757–766 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krapić, M., Kavazović, I. & Wensveen, F. M. Immunological mechanisms of sickness behavior in viral infection. Viruses 13, 2245 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ferrer, M. et al. Cachexia: a systemic consequence of progressive, unresolved disease. Cell 186, 1824–1845 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schieber, A. M. et al. Disease tolerance mediated by microbiome E. coli involves inflammasome and IGF-1 signaling. Science 350, 558–563 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Redford, S. E., Varanasi, S. K., Sanchez, K. K., Thorup, N. R. & Ayres, J. S. CD4+ T cells regulate sickness-induced anorexia and fat wasting during a chronic parasitic infection. Cell Rep. 42, 112814 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tinahones, F. J. et al. Dietary palmitic acid influences LDL-mediated lymphocyte proliferation differently to other mono- and polyunsaturated fatty acids in rats. Diabetes Nutr. Metab. 17, 250–258 (2004).

    CAS 
    PubMed 

    Google Scholar
     

  • Abdelmagid, S. A. et al. Comprehensive profiling of plasma fatty acid concentrations in young healthy Canadian adults. PLoS ONE 10, e0116195 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Korbecki, J. & Bajdak-Rusinek, K. The effect of palmitic acid on inflammatory response in macrophages: an overview of molecular mechanisms. Inflamm. Res. 68, 915–932 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Camell, C. & Smith, C. W. Dietary oleic acid increases m2 macrophages in the mesenteric adipose tissue. PLoS ONE 8, e75147 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lancaster, G. I. et al. Evidence that TLR4 is not a receptor for saturated fatty acids but mediates lipid-induced inflammation by reprogramming macrophage metabolism. Cell Metab. 27, 1096–1110 e1095 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhou, T. et al. Upregulation of SLAMF3 on human T cells is induced by palmitic acid through the STAT5-PI3K/Akt pathway and features the chronic inflammatory profiles of type 2 diabetes. Cell Death Dis. 10, 559 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reilly, N. A. et al. Oleic acid triggers metabolic rewiring of T cells poising them for T helper 9 differentiation. iScience 27, 109496 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Frasca, D., Romero, M., Garcia, D., Diaz, A. & Blomberg, B. B. Obesity accelerates age-associated defects in human B cells through a metabolic reprogramming induced by the fatty acid palmitate. Front. Aging 2, 828697 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Newsholme, P. Cellular and metabolic mechanisms of nutrient actions in immune function. Eur. J. Clin. Nutr. 75, 1328–1331 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brookens, S. K. et al. Plasma cell differentiation, antibody quality, and initial germinal center B cell population depend on glucose influx rate. J. Immunol. 212, 43–56 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Caro-Maldonado, A. et al. Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J. Immunol. 192, 3626–3636 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sharma, R. et al. Distinct metabolic requirements regulate B cell activation and germinal center responses. Nat. Immunol. 24, 1358–1369 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Waters, L. R., Ahsan, F. M., Wolf, D. M., Shirihai, O. & Teitell, M. A. Initial B cell activation induces metabolic reprogramming and mitochondrial remodeling. iScience 5, 99–109 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shao, S., Yang, Q., Pan, R., Yu, X. & Chen, Y. Interaction of severe acute respiratory syndrome coronavirus 2 and diabetes. Front. Endocrinol. 12, 731974 (2021).

    Article 

    Google Scholar
     

  • Kavazović, I. et al. Hyperglycemia and not hyperinsulinemia mediates diabetes-induced memory CD8 T-cell dysfunction. Diabetes 71, 706–721 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Zafirova, B. et al. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity https://doi.org/10.1016/j.immuni.2009.06.017 (2009).

  • Gebhardt, T. et al. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524–530 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kavazović, I. et al. Eomes broadens the scope of CD8 T-cell memory by inhibiting apoptosis in cells of low affinity. PLoS Biol. 18, e3000648 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sarafian, M. H. et al. Objective set of criteria for optimization of sample preparation procedures for ultra-high throughput untargeted blood plasma lipid profiling by ultra performance liquid chromatography-mass spectrometry. Anal. Chem. 86, 5766–5774 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tsugawa, H. et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat. Methods https://doi.org/10.1038/nmeth.3393 (2015).

  • Drotleff, B. & Lämmerhofer, M. Guidelines for selection of internal standard-based normalization strategies in untargeted lipidomic profiling by LC–HR-MS/MS. Anal. Chem. acs.analchem.9b01505 (2019).

  • Drotleff, B. et al. Lipidomic profiling of non-mineralized dental plaque and biofilm by untargeted UHPLC-QTOF-MS/MS and SWATH acquisition. Anal. Bioanal. Chem. https://doi.org/10.1007/s00216-019-02364-2 (2020).

  • Source link

    Get RawNews Daily

    Stay informed with our RawNews daily newsletter email

    Republicans balk at going it alone on Iran war funding

    Taylor Frankie Paul’s Ex Dakota Mortensen Speaks Out, Calls Claims ‘Baseless’

    New Zealand February trade deficit narrows, exports and imports both beat expectations

    Kevin O’Leary forecasts power shift in Strait of Hormuz after Iran conflict