FABP4/aP2 Regulates Macrophage Redox Signaling and Inflammasome Activation via Control of UCP2

REFERENCES

• García-Santamarina S, Boronat S, Domènech A, Ayté J, Molina H, Hidalgo E. 2014. Monitoring in vivo reversible cysteine oxidation in proteins using ICAT and mass spectrometry. Nat Protoc 9:1131–1145. https://doi.org/10.1038/nprot.2014.065.
   PubMed Web of Science ®Google Scholar
• Wisse BE. 2004. The inflammatory syndrome: the role of adipose tissue cytokines in metabolic disorders linked to obesity. J Am Soc Nephrol 15:2792–2800. https://doi.org/10.1097/01.ASN.0000141966.69934.21.
   PubMed Web of Science ®Google Scholar
• Xu H, Hertzel AV, Steen KA, Wang Q, Suttles J, Bernlohr DA. 2015. Uncoupling lipid metabolism from inflammation through fatty acid binding protein-dependent expression of UCP2. Mol Cell Biol 35:1055–1065. https://doi.org/10.1128/MCB.01122-14.
   PubMed Web of Science ®Google Scholar
• Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW, III, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD. 2009. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119:573–581. https://doi.org/10.1172/JCI37048.
   PubMed Web of Science ®Google Scholar
• Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, Strahler JR, Andrews PC, Jakob U. 2008. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci U S A 105:8197–8202. https://doi.org/10.1073/pnas.0707723105.
   PubMed Web of Science ®Google Scholar
• Sen CK. 2001. Cellular thiols and redox-regulated signal transduction. Curr Top Cell Reg 36:1–30. https://doi.org/10.1016/S0070-2137(01)80001-7.
   Google Scholar
• Mailloux RJ, Fu A, Robson-Doucette C, Allister EM, Wheeler MB, Screaton R, Harper M-E. 2012. Glutathionylation state of uncoupling protein-2 and the control of glucose-stimulated insulin secretion. J Biol Chem 287:39673–39685. https://doi.org/10.1074/jbc.M112.393538.
   PubMed Web of Science ®Google Scholar
• Schieber M, Chandel NS. 2014. ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462. https://doi.org/10.1016/j.cub.2014.03.034.
   PubMed Web of Science ®Google Scholar
• Wall SB, Oh J-Y, Diers AR, Landar A. 2012. Oxidative modification of proteins: an emerging mechanism of cell signaling. Front Physiol 3:369. https://doi.org/10.3389/fphys.2012.00369.
   PubMed Web of Science ®Google Scholar
• Brand MD. 2010. The sites and topology of mitochondrial superoxide production. Exp Gerontol 45:466–472. https://doi.org/10.1016/j.exger.2010.01.003.
   PubMed Web of Science ®Google Scholar
• Pfefferle A, Mailloux RJ, Adjeitey CN-K, Harper M-E. 2013. Glutathionylation of UCP2 sensitizes drug resistant leukemia cells to chemotherapeutics. Biochim Biophys Acta 1833:80–89. https://doi.org/10.1016/j.bbamcr.2012.10.006.
   PubMedGoogle Scholar
• Dal Vechio FH, Cerqueira F, Augusto O, Lopes R, Demasi M. 2014. Peptides that activate the 20S proteasome by gate opening increased oxidized protein removal and reduced protein aggregation. Free Radic Biol Med 67:304–313. https://doi.org/10.1016/j.freeradbiomed.2013.11.017.
   PubMedGoogle Scholar
• Leadsham JE, Sanders G, Giannaki S, Bastow EL, Hutton R, Naeimi WR, Breitenbach M, Gourlay CW. 2013. Loss of cytochrome c oxidase promotes RAS-dependent ROS production from the ER resident NADPH oxidase, Yno1p, in yeast. Cell Metab 18:279–286. https://doi.org/10.1016/j.cmet.2013.07.005.
   PubMed Web of Science ®Google Scholar
• Stowe DF, Camara AKS. 2009. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 11:1373–1414. https://doi.org/10.1089/ars.2008.2331.
   PubMed Web of Science ®Google Scholar
• Zhao Q, Wang J, Levichkin IV, Stasinopoulos S, Ryan MT, Hoogenraad NJ. 2002. A mitochondrial specific stress response in mammalian cells. EMBO J 21:4411–4419. https://doi.org/10.1093/emboj/cdf445.
   PubMed Web of Science ®Google Scholar
• Bronner DN, Abuaita BH, Chen X, Fitzgerald KA, Nuñez G, He Y, Yin X-M, O'Riordan MXD. 2015. Endoplasmic reticulum stress activates the inflammasome via NLRP3- and caspase-2-driven mitochondrial damage. Immunity 43:451–462. https://doi.org/10.1016/j.immuni.2015.08.008.
   PubMed Web of Science ®Google Scholar
• Pellegrino MW, Nargund AM, Haynes CM. 2013. Signaling the mitochondrial unfolded protein response. Biochim Biophys Acta 1833:410–416. https://doi.org/10.1016/j.bbamcr.2012.02.019.
   PubMed Web of Science ®Google Scholar
• Cano M, Wang L, Wan J, Barnett BP, Ebrahimi K, Qian J, Handa JT. 2014. Oxidative stress induces mitochondrial dysfunction and a protective unfolded protein response in RPE cells. Free Radic Biol Med 69:1–14. https://doi.org/10.1016/j.freeradbiomed.2014.01.004.
   PubMed Web of Science ®Google Scholar
• Krauss S, Zhang C-Y, Lowell BB. 2005. The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6:248–261. https://doi.org/10.1038/nrm1592.
   PubMed Web of Science ®Google Scholar
• Vandanmagsar B, Youm Y-H, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. 2011. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17:179–188. https://doi.org/10.1038/nm.2279.
   PubMed Web of Science ®Google Scholar
• Masters SL, O'Neill LAJ. 2011. Disease-associated amyloid and misfolded protein aggregates activate the inflammasome. Trends Mol Med 17:276–282. https://doi.org/10.1016/j.molmed.2011.01.005.
   PubMedGoogle Scholar
• Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, Ramanujan VK, Wolf AJ, Vergnes L, Ojcius DM, Rentsendorj A, Vargas M, Guerrero C, Wang Y, Fitzgerald KA, Underhill DM, Town T, Arditi M. 2012. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 36:401–414. https://doi.org/10.1016/j.immuni.2012.01.009.
   PubMed Web of Science ®Google Scholar
• Gurung P, Lukens JR, Kanneganti T-D. 2015. Mitochondria: diversity in the regulation of the NLRP3 inflammasome. Trends Mol Med 21:193–201. https://doi.org/10.1016/j.molmed.2014.11.008.
   PubMed Web of Science ®Google Scholar
• Hotamisligil GS, Johnson RS, Distel RJ, Ellis R, Papaioannou VE, Spiegelman BM. 1996. Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science 274:1377–1379. https://doi.org/10.1126/science.274.5291.1377.
   PubMed Web of Science ®Google Scholar
• Makowski L, Boord JB, Maeda K, Babaev VR, Uysal KT, Morgan MA, Parker RA, Suttles J, Fazio S, Hotamisligil GS, Linton MF. 2001. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat Med 7:699–705. https://doi.org/10.1038/89076.
   PubMed Web of Science ®Google Scholar
• Hertzel AV, Hellberg K, Reynolds JM, Kruse AC, Juhlmann BE, Smith AJ, Sanders MA, Ohlendorf DH, Suttles J, Bernlohr DA. 2009. Identification and characterization of a small molecule inhibitor of fatty acid binding proteins. J Med Chem 52:6024–6031. https://doi.org/10.1021/jm900720m.
   PubMed Web of Science ®Google Scholar
• Hotamisligil GS, Bernlohr DA. 2015. Metabolic functions of FABPs—mechanisms and therapeutic implications. Nat Rev Endocrinol 11:592–605. https://doi.org/10.1038/nrendo.2015.122.
   PubMed Web of Science ®Google Scholar
• Xu H, Hertzel AV, Steen KA, Bernlohr DA. 2016. Loss of fatty acid binding protein 4/aP2 reduces macrophage inflammation through activation of SIRT3. Mol Endocrinol 30:325–334. https://doi.org/10.1210/me.2015-1301.
   PubMedGoogle Scholar
• Hui X, Li H, Zhou Z, Lam KSL, Xiao Y, Wu D, Ding K, Wang Y, Vanhoutte PM, Xu A. 2010. Adipocyte fatty acid-binding protein modulates inflammatory responses in macrophages through a positive feedback loop involving c-Jun NH2-terminal kinases and activator protein-1. J Biol Chem 285:10273–10280. https://doi.org/10.1074/jbc.M109.097907.
   PubMed Web of Science ®Google Scholar
• Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R, Bouillaud F, Richard D, Collins S, Ricquier D. 2000. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26:435–439. https://doi.org/10.1038/82565.
   PubMed Web of Science ®Google Scholar
• Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. 2012. Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19. https://doi.org/10.1097/WOX.0b013e3182439613.
   PubMedGoogle Scholar
• Kansanen E, Kuosmanen SM, Leinonen H, Levonen A-L. 2013. The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol 1:45–49. https://doi.org/10.1016/j.redox.2012.10.001.
   PubMed Web of Science ®Google Scholar
• Kwak M-K, Wakabayashi N, Greenlaw JL, Yamamoto M, Kensler TW. 2003. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 23:8786–8794. https://doi.org/10.1128/MCB.23.23.8786-8794.2003.
   PubMed Web of Science ®Google Scholar
• Haynes CM, Fiorese CJ, Lin Y-F. 2013. Evaluating and responding to mitochondrial dysfunction: the mitochondrial unfolded-protein response and beyond. Trends Cell Biol 23:311–318. https://doi.org/10.1016/j.tcb.2013.02.002.
   PubMedGoogle Scholar
• Bota DA, Davies KJA. 2002. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4:674–680. https://doi.org/10.1038/ncb836.
   PubMed Web of Science ®Google Scholar
• Kretz-Remy C, Bates EE, Arrigo AP. 1998. Amino acid analogs activate NF-kappaB through redox-dependent IkappaB-alpha degradation by the proteasome without apparent IkappaB-alpha phosphorylation. Consequence on HIV-1 long terminal repeat activation. J Biol Chem 273:3180–3191.
   PubMedGoogle Scholar
• Kretz-Remy C, Mehlen P, Mirault M, Arrigo A. 1996. Inhibition of IκB-α phosphorylation and degradation and subsequent NF-κB activation by glutathione peroxidase overexpression. J Cell Biol 133:1083–1093. https://doi.org/10.1083/jcb.133.5.1083.
   PubMed Web of Science ®Google Scholar
• Alfonso-Loeches S, Ureña-Peralta JR, Morillo-Bargues MJ, Oliver-De La Cruz J, Guerri C. 2014. Role of mitochondria ROS generation in ethanol-induced NLRP3 inflammasome activation and cell death in astroglial cells. Front Cell Neurosci 8:216. https://doi.org/10.3389/fncel.2014.00216.
   PubMed Web of Science ®Google Scholar
• Pickering AM, Davies KJA. 2012. Degradation of damaged proteins: the main function of the 20S proteasome. Prog Mol Biol Transl Sci 109:227–248. https://doi.org/10.1016/B978-0-12-397863-9.00006-7.
   PubMed Web of Science ®Google Scholar
• Pickering AM, Staab TA, Tower J, Sieburth D, Davies KJA. 2013. A conserved role for the 20S proteasome and Nrf2 transcription factor in oxidative stress adaptation in mammals, Caenorhabditis elegans and Drosophila melanogaster. J Exp Biol 216:543–553. https://doi.org/10.1242/jeb.074757.
   PubMed Web of Science ®Google Scholar
• Wang X. 2001. The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933.
   PubMed Web of Science ®Google Scholar
• Green PS, Leeuwenburgh C. 2002. Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim Biophys Acta 1588:94–101. https://doi.org/10.1016/S0925-4439(02)00144-8.
   PubMed Web of Science ®Google Scholar
• Rainbolt TK, Saunders JM, Wiseman RL. 2014. Stress-responsive regulation of mitochondria through the ER unfolded protein response. Trends Endocrinol Metab 25:528–537. https://doi.org/10.1016/j.tem.2014.06.007.
   PubMed Web of Science ®Google Scholar
• Marchi S, Patergnani S, Pinton P. 2014. The endoplasmic reticulum-mitochondria connection: one touch, multiple functions. Biochim Biophys Acta 1837:461–469. https://doi.org/10.1016/j.bbabio.2013.10.015.
   PubMed Web of Science ®Google Scholar
• López-Crisosto C, Bravo-Sagua R. 2015. ER-to-mitochondria miscommunication and metabolic diseases. Biochim Biophys Acta 1852:2096–2105. https://doi.org/10.1016/j.bbadis.2015.07.011.
   PubMedGoogle Scholar
• Takada Y, Mukhopadhyay A, Kundu GC, Mahabeleshwar GH, Singh S, Aggarwal BB. 2003. Hydrogen peroxide activates NF-kappa B through tyrosine phosphorylation of I kappa B alpha and serine phosphorylation of p65: evidence for the involvement of I kappa B alpha kinase and Syk protein-tyrosine kinase. J Biol Chem 278:24233–24241. https://doi.org/10.1074/jbc.M212389200.
   PubMed Web of Science ®Google Scholar
• Guo H, Callaway JB, Ting JP-Y. 2015. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 21:677–687. https://doi.org/10.1038/nm.3893.
   PubMed Web of Science ®Google Scholar
• Sen CK, Packer L, Baeuerle PA. 1999. Antioxidant and redox regulation of genes. Academic Press, San Diego, CA.
   Google Scholar
• Brüne B, Dehne N, Grossmann N, Jung M, Namgaladze D, Schmid T, Knethen von A, Weigert A. 2013. Redox control of inflammation in macrophages. Antioxid Redox Signal 19:595–637. https://doi.org/10.1089/ars.2012.4785.
   PubMed Web of Science ®Google Scholar
• Taylor RC, Acquaah-Mensah G, Singhal M, Malhotra D, Biswal S. 2008. Network inference algorithms elucidate Nrf2 regulation of mouse lung oxidative stress. PLoS Comput Biol 4:e1000166. https://doi.org/10.1371/journal.pcbi.1000166.
   PubMedGoogle Scholar
• Manzanero S, Gelderblom M, Magnus T. 2011. Calorie restriction and stroke. Exp Transl Stroke Med 3:8. https://doi.org/10.1186/2040-7378-3-8.
   PubMedGoogle Scholar
• Baar RA, Dingfelder CS, Smith LA, Bernlohr DA, Wu C, Lange AJ, Parks EJ. 2005. Investigation of in vivo fatty acid metabolism in AFABP/aP2(-/-) mice. Am J Physiol Endocrinol Metab 288:E187–E193.
   PubMed Web of Science ®Google Scholar
• Ying W, Cheruku PS, Bazer FW, Safe SH, Zhou B. 23June2013. Investigation of macrophage polarization using bone marrow derived macrophages. J Vis Exp. https://doi.org/10.3791/50323.
   Google Scholar