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Jimmunol.1800002.Full.Pdf Myeloid Slc2a1-Deficient Murine Model Revealed Macrophage Activation and Metabolic Phenotype Are Fueled by GLUT1 This information is current as Alex J. Freemerman, Liyang Zhao, Ajeeth K. Pingili, Bin of September 25, 2021. Teng, Alyssa J. Cozzo, Ashley M. Fuller, Amy R. Johnson, J. Justin Milner, Maili F. Lim, Joseph A. Galanko, Melinda A. Beck, James E. Bear, Jeremy D. Rotty, Lavanya Bezavada, Heather S. Smallwood, Michelle A. Puchowicz, Juan Liu, Jason W. Locasale, Douglas P. Lee, Brian J. Bennett, E. Dale Abel, Jeff C. Rathmell and Liza Makowski Downloaded from J Immunol published online 18 January 2019 http://www.jimmunol.org/content/early/2019/01/17/jimmun ol.1800002 http://www.jimmunol.org/ Supplementary http://www.jimmunol.org/content/suppl/2019/01/17/jimmunol.180000 Material 2.DCSupplemental Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 25, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Author Choice Freely available online through The Journal of Immunology Author Choice option Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published January 18, 2019, doi:10.4049/jimmunol.1800002 The Journal of Immunology Myeloid Slc2a1-Deficient Murine Model Revealed Macrophage Activation and Metabolic Phenotype Are Fueled by GLUT1 Alex J. Freemerman,*,1 Liyang Zhao,*,1 Ajeeth K. Pingili,† Bin Teng,† Alyssa J. Cozzo,* Ashley M. Fuller,‡ Amy R. Johnson,* J. Justin Milner,*,2 Maili F. Lim,* Joseph A. Galanko,x Melinda A. Beck,* James E. Bear,{ Jeremy D. Rotty,{ Lavanya Bezavada,‖ Heather S. Smallwood,‖ Michelle A. Puchowicz,‖ Juan Liu,# Jason W. Locasale,# Douglas P. Lee,** Brian J. Bennett,†† E. Dale Abel,‡‡,xx Jeff C. Rathmell,{{ and Liza Makowski*,† Macrophages (MFs) are heterogeneous and metabolically flexible, with metabolism strongly affecting immune activation. A classic response to proinflammatory activation is increased flux through glycolysis with a downregulation of oxidative metabolism, whereas alternative activation is primarily oxidative, which begs the question of whether targeting glucose metabolism is a viable Downloaded from approach to control MF activation. We created a murine model of myeloid-specific glucose transporter GLUT1 (Slc2a1) deletion. Bone marrow–derived MFs (BMDM) from Slc2a1M2/2 mice failed to uptake glucose and demonstrated reduced glycolysis and pentose phosphate pathway activity. Activated BMDMs displayed elevated metabolism of oleate and glutamine, yet maximal respiratory capacity was blunted in MF lacking GLUT1, demonstrating an incomplete metabolic reprogramming. Slc2a1M2/2 BMDMs displayed a mixed inflammatory phenotype with reductions of the classically activated pro- and anti-inflammatory M2/2 markers, yet less oxidative stress. Slc2a1 BMDMs had reduced proinflammatory metabolites, whereas metabolites indicative http://www.jimmunol.org/ of alternative activation—such as ornithine and polyamines—were greatly elevated in the absence of GLUT1. Adipose tissue MFs of lean Slc2a1M2/2 mice had increased alternative M2-like activation marker mannose receptor CD206, yet lack of GLUT1 was not a critical mediator in the development of obesity-associated metabolic dysregulation. However, Ldlr2/2 mice lacking myeloid GLUT1 developed unstable atherosclerotic lesions. Defective phagocytic capacity in Slc2a1M2/2 BMDMs may have contributed to unstable atheroma formation. Together, our findings suggest that although lack of GLUT1 blunted glycolysis and the pentose phosphate pathway, MF were metabolically flexible enough that inflammatory cytokine release was not dramatically regulated, yet phagocytic defects hindered MF function in chronic diseases. The Journal of Immunology, 2019, 202: 000–000. by guest on September 25, 2021 acrophages (MFs) are a heterogeneous population development, tissue homeostasis, host defense, and tumor growth of cells within the innate immune system that play (1). MFs exhibit a diverse spectrum of metabolic characteristics M critical roles in a myriad of processes, including (2–10). In vitro studies have informed early findings that classically *Department of Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, (R01 DK105550). J.E.B. is supported by the NIH (R01 GM111557). E.D.A. was sup- NC 25799; †Department of Medicine, University of Tennessee Health Science Cen- ported by NIH Grant U01 HL087947. UNC Gillings School of Global Public Health’s ter, Memphis, TN 38163; ‡Department of Medicine, University of North Carolina at B. Erik and Mabel S. Johansson Scholarship supported L.Z. The UNC Flow Cytometry Chapel Hill, Chapel Hill, NC 27599; xDepartment of Pathology and Laboratory Core Facility was supported in part by Grant P30 CA016086 from Cancer Center Core Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599; Support to the UNC Lineberger Comprehensive Cancer Center. The UNC Royster {Department of Cell Biology and Physiology, University of North Carolina at Chapel Society of Fellows Graduate Fellowships were awarded to A.J.C. and A.M.F. Hill, Chapel Hill, NC 27599; ‖Department of Pediatrics, University of Tennessee The sequences presented in this article have been submitted to the National Center Health Science Center, Memphis, TN 38163; #Department of Pharmacology and for Biotechnology Information Gene Expression Omnibus under accession number Cancer Biology, Duke University School of Medicine, Duke University, Durham, GSE123289. NC 27710; **Omic Insight, Inc., Durham, NC 27713; ††U.S. Department of Agriculture Western Human Nutrition Research Center, Davis, CA 95616; Address correspondence and reprint requests to Dr. Liza Makowski, Cancer Research ‡‡Division of Endocrinology and Metabolism, University of Iowa Carver College of Building Room 322, Cancer Research Building, University of Tennessee Health Medicine, Iowa City, IA 52242; xxFraternal Order of Eagles Diabetes Research Cen- Science Center, 19 South Manassas, Memphis, TN 38163. E-mail address: liza. ter, University of Iowa Carver College of Medicine, Iowa City, IA 52242; and [email protected] {{Department of Pathology, Microbiology, and Immunology, Vanderbilt Center for The online version of this article contains supplemental material. Immunobiology, Vanderbilt University, Nashville, TN 37232 Abbreviations used in this article: Arg1, arginase 1; BMDM, bone marrow–derived 1A.J.F. and L.Z. are cofirst authors. MF; BMT, bone marrow transplant; CLS, crown-like structure; 2-DG, 2-deoxyglu- 2Current address: Division of Biological Sciences, University of California, San cose; ECAR, extracellular acidification rate; eWAT, epididymal white adipose tissue; Diego, La Jolla, CA. FC, final concentration; GSH, glutathione; HFD, high-fat diet; iNOS, inducible NO synthase; LDL, low-density lipoprotein; Ldlr2/2, lacking LDL receptor; LFD, low- ORCIDs: 0000-0003-1960-0199 (L.Z.); 0000-0002-0752-2130 (J.J.M.); 0000-0003- fat diet; LysMCre, B6.129P2-Lyz2tCAM(cre)Ifo/J; Lyz2, lysozyme 2; MF, macrophage; 4871-6828 (M.A.B.); 0000-0002-7766-3502 (J.W.L.); 0000-0002-0766- MFI, median fluorescence intensity; MID, mass isotopomer distribution; MOMA2, 3195 (B.J.B.); 0000-0001-5290-0738 (E.D.A.); 0000-0002-5337-8037 (L.M.). MF/monocyte mAb; MRI, magnetic resonance imaging; OCR, oxygen consumption Received for publication January 3, 2018. Accepted for publication December 3, rate; ORO, Oil Red O; PAI-1, plasminogen activator inhibitor-1; PPP, pentose phos- 2018. phate pathway; qPCR, quantitative PCR; ROS, reactive oxygen species; SVF, stromal-vascular fraction; UNC, University of North Carolina. This work was supported by grants from the American Heart Association (13BGIA17070106) and the National Institutes of Health (NIH) (R00 AA017376), a This article is distributed under The American Association of Immunologists, Inc., University of North Carolina (UNC) Nutrition Obesity Research Consortium pilot award Reuse Terms and Conditions for Author Choice articles. from the NIH (P30DK056350), a UNC McAllister Heart Institute award, and University of Tennessee Health Science Center Methodist Mission support funds to L.M. B.J.B. Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 was supported by the NIH (Grant R01HL128572). J.C.R. was supported by the NIH www.jimmunol.org/cgi/doi/10.4049/jimmunol.1800002 2 MACROPHAGE ACTIVATION AND METABOLISM ARE FUELED BY GLUT1 activated (“M1”-like) MFs use primarily glycolysis, which is obese Slc2a1M2/2 adipose tissue, there were no differences in linked to the proinflammatory phenotype characterized by the glucose or insulin tolerance between Slc2a1M2/2 mice and obese production of high levels of proinflammatory cytokines and reactive floxed littermate controls, measures typically associated with MF oxygen and nitrogen metabolites plus microbicidal and phagocytic markers, thus indicating that increased MF infiltration failed to
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