Novel XBP1s-independent function of IRE1 RNase in HIF-1α-mediated glycolysis upregulation in human macrophages upon stimulation with LPS or saturated fatty acid
Colonval, Megan ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie - Immunologie
Wilkin, Chloé ; Université de Liège - ULiège > GIGA ; Université de Liège - ULiège > GIGA > GIGA I3 - Immunometabolism and Nutrition
L'Homme, Laurent ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie - Immunologie
Lassence, Cédric ; Université de Liège - ULiège > Département des sciences de la vie
Campas, Manon ; Université de Liège - ULiège > Département de pharmacie > Chimie pharmaceutique
Peulen, Olivier ; Université de Liège - ULiège > GIGA > GIGA Cancer - Metastases Research Laboratory
De Tullio, Pascal ; Université de Liège - ULiège > Département de pharmacie > Chimie pharmaceutique
Piette, Jacques ; Université de Liège - ULiège > GIGA > GIGA I3 - Virology and Immunology
Legrand, Sylvie ; Université de Liège - ULiège > GIGA > GIGA I3 - Immunometabolism and Nutrition
Language :
English
Title :
Novel XBP1s-independent function of IRE1 RNase in HIF-1α-mediated glycolysis upregulation in human macrophages upon stimulation with LPS or saturated fatty acid
Publication date :
30 August 2023
Journal title :
Frontiers in Immunology
eISSN :
1664-3224
Publisher :
Frontiers Research Foundation, Lausanne, Switzerland
Ward ZJ Bleich SN Cradock AL Barrett JL Giles CM Flax C et al. Projected U.S. state-level prevalence of adult obesity and severe obesity. N Engl J Med (2019) 381:2440–50. doi: 10.1056/nejmc1917339
Larsson SC Burgess S. Causal role of high body mass index in multiple chronic diseases: a systematic review and meta-analysis of Mendelian randomization studies. BMC Med (2021) 19:320. doi: 10.1186/s12916-021-02188-x
Font-Burgada J Sun B and Karin M. Obesity and cancer: the oil that feeds the flame. Cell Metab (2016) 23:48–62. doi: 10.1016/j.cmet.2015.12.015
Esser N Legrand-Poels S Piette J Scheen AJ and Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract (2014) 105:141–50. doi: 10.1016/j.diabres.2014.04.006
So JS. Roles of endoplasmic reticulum stress in immune responses. Mol Cells (2018) 41:705–16. doi: 10.14348/molcells.2018.0241
Kratz M Coats BR Hisert KB Hagman D Mutskov V Peris P et al. Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages. Cell Metab (2014) 20:614–25. doi: 10.1016/j.cmet.2014.08.010
Huang S Rutkowsky JM Snodgrass RG Ono-Moore KD Schneider DA Newman JW et al. Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J Lipid Res (2012) 53:2002–13. doi: 10.1194/jlr.d029546
Nguyen MT Favelyukis S Nguyen AK Reichart D Scott PA Jenn A et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem (2007) 282:35279–92. doi: 10.1074/jbc.m706762200
Shi H Kokoeva MV Inouye K Tzameli I Yin H Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest (2006) 116:3015–25. doi: 10.1172/jci28898
Lancaster GI Langley KG Berglund NA Kammoun HL Reibe S Estevez E et al. Evidence that TLR4 is not a receptor for saturated fatty acids but mediates lipid-induced inflammation by reprogramming macrophage metabolism. Cell Metab (2018) 27:1096–110. doi: 10.1016/j.cmet.2018.03.014
Robblee MM Kim CC Abate JP Valdearcos M Sandlund KLM Shenoy MK et al. Saturated fatty acids engage an IRE1a-dependent pathway to activate the NLRP3 inflammasome in myeloid cells. Cell Rep (2016) 14:2611–23. doi: 10.1016/j.celrep.2016.02.053
GianFrancesco MA Dehairs J L’homme L Herinckx G Esser N Jansen O et al. Saturated fatty acids induce NLRP3 activation in human macrophages through K+ efflux resulting from phospholipid saturation and Na, K-ATPase disruption. Biochim Biophys Acta Mol Cell Biol Lipids (2019) 1864:1017–30. doi: 10.1016/j.bbalip.2019.04.001
Lamkanfi M Dixit VM. Mechanisms and functions of inflammasomes. Cell (2014) 157:1013–22. doi: 10.1016/j.cell.2014.04.007
Vandanmagsar B Youm YH Ravussin A Galgani JE Stadler K Mynatt RL et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med (2011) 17:179–88. doi: 10.1038/nm.2279
Esser N L’homme L De Roover A Kohnen L Scheen AJ Moutschen M et al. Obesity phenotype is related to NLRP3 inflammasome activity and immunological profile of visceral adipose tissue. Diabetologia (2013) 56:2487–97. doi: 10.1007/s00125-013-3023-9
Wen H Gris D Lei Y Jha S Zhang L Huang MT et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol (2011) 12:408–15. doi: 10.1038/ni.2022
L’homme L Esser N Riva L Scheen A Paquot N Piette J et al. Unsaturated fatty acids prevent activation of NLRP3 inflammasome in human monocytes/macrophages. J Lipid Res (2013) 54:2998–3008. doi: 10.1194/jlr.m037861
Volmer R van der Ploeg K and Ron D. Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci USA (2013) 110:4628–33. doi: 10.1073/pnas.1217611110
Volmer R Ron D. Lipid-dependent regulation of the unfolded protein response. Curr Opin Cell Biol (2015) 33:67–73. doi: 10.1016/j.ceb.2014.12.002
Ron D Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol (2007) 8:519–29. doi: 10.1038/nrm2199
Hetz C Zhang K Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol Cell Biol (2020) 21:421–38. doi: 10.1038/s41580-020-0250-z
Hollien J Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science (2006) 313:104. doi: 10.1126/science.1129631
Maurel M Chevet E Tavernier J Gerlo S. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci (2014) 39:245–54. doi: 10.1016/j.tibs.2014.02.008
Urano F Wang X BertolottiZhang Y Chung P Harding HP et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kina IRE1. Science (2000) 287:664. doi: 10.1126/science.287.5453.664
Hetz C Papa FR. The unfolded protein response and cell fate control. Mol Cell (2018) 69:169–81. doi: 10.1016/j.molcel.2017.06.017
Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell (2010) 140:900–17. doi: 10.1016/j.cell.2010.02.034
Grootjans J Kaser A Kaufman RJ Blumberg RS. The unfolded protein response in immunity and inflammation. Nat Rev Immunol (2016) 16:469–84. doi: 10.1038/nri.2016.62
Huang S Xing Y Liu Y. Emerging roles for the ER stress sensor IRE1α in metabolic regulation and disease. J Biol Chem (2019) 294:18726–41. doi: 10.1074/jbc.rev119.007036
Qiu Q Zheng Z Chang L Zhao Y Tan C Dandekar A et al. Toll-like receptor-mediated IRE1α activation as a therapeutic target for inflammatory arthritis. EMBO J (2013) 32:2477–90. doi: 10.1038/emboj.2013.183
Martinon F Chen X Lee A-H Glimcher LH. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol (2010) 11(5):411–8. doi: 10.1038/ni.1857
Trapnell C Roberts A Goff L Pertea G Kim D Kelley DR et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc (2012) 7:562–78. doi: 10.1038/nprot.2012.016
O’Neill LAJ Kishton RJ Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol (2016) 16(9):553–65. doi: 10.1038/nri.2016.70
Erridge C. Endogenous ligands of TLR2 and TLR4: agonists or assistants? J Leukoc Biol (2010) 87:989–99. doi: 10.1189/jlb.1209775
Erridge C Samani NJ. Saturated fatty acids do not directly stimulate Toll-like receptor signaling. Arterioscler Thromb Vasc Biol (2009) 29:1944–9. doi: 10.1161/ATVBAHA.109.194050
Pal D Dasgupta S Kundu R Maitra S Das G Mukhopadhyay S et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med (2012) 18:1279–85. doi: 10.1038/nm.2851
Butcher SK O’Carroll CE Wells CA and Carmody RJ. Toll-like receptors Drive specific Patterns of Tolerance and Training on restimulation of Macrophages. Front Immunol (2018) 9:933. doi: 10.3389/fimmu.2018.00933
Vrieling F Kostidi S Spaink HP Haks MC Mayboroda OA Ottenhoff THM et al. Analyzing the impact of Mycobacterium tuberculosis infection on primary human macrophages by combined exploratory and targeted metabolomics. Sci Rep (2020) 10(1):7085. doi: 10.1038/s41598-020-62911-1
Vijayana V Pradhana P Braudb L Fuchsc HR Guelerd F Motterlinib R et al. Human and murine macrophages exhibit differential metabolic responses to lipopolysaccharide-A divergent role for glycolysis. Redox Biol (2019) 22:101147. doi: 10.1016/j.redox.2019.101147
Kahlenberg JM Dubyak GR. Differing caspase-1 activation states in monocyte versus macrophage models of IL-1beta processing and release. J Leukoc Biol (2004) 76:676–684. doi: 10.1189/jlb.0404221
Yu Q Guo M Zeng W Zeng M Zhang X and Zhang Y. Interactions between NLRP3 inflammasome and glycolysis in macrophages: New insights into chronic inflammation pathogenesis. Immun Inflamm Dis (2022) 10:e581. doi: 10.1002/iid3.581
Corcoran SE O’Neill LAJ. HIF1α and metabolic reprogramming in inflammation. J Clin Invest (2016) 126(10):3699–707. doi: 10.1172/JCI84431
Rius J Guma M Schachtrup C Akassoglou K Zinkernagel AS Nizet V et al. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature (2008) 453(7196):807–11. doi: 10.1038/nature06905
Matsunaga N Tsuchimori N Matsumoto T and Ii M. TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol Pharmacol (2011) 79(1):34–41. doi: 10.1124/mol.110.068064
Chen X Iliopoulos D Zhang Q Tang Q Greenblatt MB Hatziapostolou M et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1a pathway. Nature (2014) 508:103–7. doi: 10.1038/nature13119
Lee AH Iwakoshi NN Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol (2003) 23:7448–59. doi: 10.1128/MCB.23.21.7448-7459.2003
Lee AH Heidtman K Hotamisligil GS Glimcher LH. Dual and opposing roles of the unfolded protein response regulated by IRE1alpha and XBP1 in proinsulin processing and insulin secretion. Proc Natl Acad Sci USA (2011) 108:8885–90. doi: 10.1073/pnas.1105564108
Akiyama M Liew CW Lu S Hu J Martinez R Hambro B et al. X-box binding protein 1 is essential for insulin regulation of pancreatic α-cell function. Diabetes (2013) 62:2439–49. doi: 10.2337/db12-1747
Cani PD Amar J Iglesias MA Poggi M Knauf C Bastelica D et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes (2007) 56:1761–72. doi: 10.2337/db06-1491
Lara-Reyna S Scambler T J Holbrook J Wong C Jarosz-Griffiths HH Martinon F et al. Metabolic reprograming of cystic fibrosis macrophages via the IRE1a arm of the unfolded protein response results in exacerbated inflammation. Front Immunol (2019) 10:1789. doi: 10.3389/fimmu.2019.01789
Guimarães ES Gomes MTR Sanches RCO Matteucci KC Marinho FV and Oliveira SC. The endoplasmic reticulum stress sensor IRE1a modulates macrophage metabolic function during Brucella abortus infection. Front Immunol (2023) 13:1063221. doi: 10.3389/fimmu.2022.1063221
Moszynska A Collawn JF Bartoszewski R. IRE1 endoribonuclease activity modulates hypoxic HIF-1 signaling in human endothelial cells. Biomol (2020) 10:895. doi: 10.3390/biom10060895
Walter F O’Brien A Concannon CG Düssmann H Prehn JHM. ER stress signaling has an activating transcription factor 6 (ATF6)-dependent “off-switch”. J Biol Chem (2018) 293(47):18270–84. doi: 10.1074/jbc.ra118.002121
Sun S Shi G Sha H Ji Y Han X Shu X et al. IRE1 is an endogenous substrate of endoplasmic-reticulum-associated degradation. Nat Cell Biol (2015) 17:1546–55. doi: 10.1038/ncb3266
So JS Hur KY Tarrio M Ruda V Frank-Kamenetsky M Fitzgerald K et al. Silencing of lipid metabolism genes through IRE1alpha mediated mRNA decay lowers plasma lipids in mice. Cell Metab (2012) 16:487–99. doi: 10.1016/j.cmet.2012.09.004
Lam M Marsters SA Ashkenazi A Walter P. Misfolded proteins bind and activate death receptor 5 to trigger apoptosis during unresolved endoplasmic reticulum stress. eLife (2020) 9:e52291. doi: 10.7554/elife.52291
Bae D Moore KA Mella JM Hayashi SY Hollien J. Degradation of Blos1 mRNA by IRE1 repositions lysosomes and protects cells from stress. J Cell Biol (2019) 218:1118–27. doi: 10.1083/jcb.201809027
Dufey E Bravo-San Pedro JM Eggers C González-Quiroz M Urra H Sagredo AI et al. Genotoxic stress triggers the activation of IRE1alpha dependent RNA decay to modulate the DNA damage response. Nat Commun (2020) 11:2401. doi: 10.1038/s41467-020-15694-y
Lhomond S Avril T Dejeans N Voutetakis K Doultsinos D McMahon M et al. Dual IRE1 RNase functions dictate glioblastoma development. EMBO Mol Med (2018) 10:e7929. doi: 10.15252/emmm.201707929
Boden G Duan X Homko C Molina EJ Song W Perez O et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes (2008) 57:2438–44. doi: 10.2337/db08-0604
Gregor MF Yang L Fabbrini E Mohammed BS Eagon JC Hotamisligil GS et al. Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes (2009) 58:693–700. doi: 10.2337/db08-1220
Shan B Wang X Wu Y Xu C Xia Z Dai J et al. The metabolic ER stress sensor IRE1alpha suppresses alternative activation of macrophages and impairs energy expenditure in obesity. Nat Immunol (2017) 18:519–29. doi: 10.1038/ni.3709
Boutens L Hooiveld GJ Dhingra S Cramer RA Netea MG Stienstra R. Unique metabolic activation of adipose tissue macrophages in obesity promotes inflammatory responses. Diabetologia (2018) 61:942–53. doi: 10.1007/s00125-017-4526-6
