2-Deoxy-d-glucose treatment decreases anti-inflammatory M2 macrophage polarization in mice with tumor and allergic airway inflammation

Frontiers in Immunology

Volumn 8, Issue JUN, 2017, Pages

  Zhao, Qingjie ^a,b   Chu, Zhulang ^a,b   Zhu, Linnan ^a,b   Yang, Tao ^a   Wang, Peng ^a   Liu, Fang ^b   Huang, Ying ^b   Zhang, Fang ^b   Zhang, Xiaodong ^c   Ding, Wenjun ^b   Zhao, Yong ^a,b  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

2 deoxy d glucose; Allergic airway inflammation; Glycolysis; M2 macrophages; Macrophage polarization; Tumor

Indexed keywords

ARGINASE; CD11B ANTIGEN; CHITIN; DEOXYGLUCOSE; GLUCOSE; INTERLEUKIN 4; LACTATE DEHYDROGENASE; LACTIC ACID; LIPOCORTIN 5;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CELL ACTIVITY; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; EOSINOPHIL; FLOW CYTOMETRY; GLUCOSE INTAKE; GLUCOSE METABOLISM; GLYCOLYSIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MOUSE; MRNA EXPRESSION ASSAY; NEOPLASM; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

EID: 85020468886     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00637     Document Type: Article

References (62)

1. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science (2010) 327:656-61. doi:10.1126/science.1178331
2. Gause WC, Wynn TA, Allen JE. Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths. Nat Rev Immunol (2013) 13:607-14. doi:10.1038/nri3476
3. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol (2002) 23:549-55. doi:10.1016/S1471-4906(02)02302-5
4. Gordon S. Alternative activation of macrophages. Nat Rev Immunol (2003) 3:23-35. doi:10.1038/nri978
5. Wynn TA, Vannella KM. Macrophages in tissue repair, regeneration, and fibrosis. Immunity (2016) 44:450-62. doi:10.1016/j.immuni.2016.02.015
6. Rodriguez-Prados JC, Traves PG, Cuenca J, Rico D, Aragones J, Martin-Sanz P, et al. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol (2010) 185:605-14. doi:10.4049/jimmunol.0901698
7. Odegaard JI, Chawla A. Alternative macrophage activation and metabolism. Annu Rev Pathol (2011) 6:275-97. doi:10.1146/annurev-pathol-011110-130138
8. Odegaard JI, Ganeshan K, Chawla A. Adipose tissue macrophages: amicus adipem? Cell Metab (2013) 18:767-8. doi:10.1016/j.cmet.2013.11.011
9. Zhu L, Zhao Q, Yang T, Ding W, Zhao Y. Cellular metabolism and macrophage functional polarization. Int Rev Immunol (2015) 34:82-100. doi:10.3109/08830185.2014.969421
10. Brown J. Effects of 2-deoxyglucose on carbohydrate metabolism: review of the literature and studies in the rat. Metabolism (1962) 11:1098-112
11. Weindruch R, Keenan KP, Carney JM, Fernandes G, Feuers RJ, Floyd RA, et al. Caloric restriction mimetics: metabolic interventions. J Gerontol A Biol Sci Med Sci (2001) 56(Spec No 1):20-33. doi:10.1093/gerona/56.suppl_1.20
12. Maher JC, Krishan A, Lampidis TJ. Greater cell cycle inhibition and cytotoxicity induced by 2-deoxy-d-glucose in tumor cells treated under hypoxic vs aerobic conditions. Cancer Chemother Pharmacol (2004) 53:116-22. doi:10.1007/s00280-003-0724-7
13. Hawley SA, Ross FA, Chevtzoff C, Green KA, Evans A, Fogarty S, et al. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab (2010) 11:554-65. doi:10.1016/j.cmet.2010.04.001
14. Robinson GL, Dinsdale D, Macfarlane M, Cain K. Switching from aerobic glycolysis to oxidative phosphorylation modulates the sensitivity of mantle cell lymphoma cells to TRAIL. Oncogene (2012) 31:4996-5006. doi:10.1038/onc.2012.13
15. Kellett DN. 2-Deoxyglucose and inflammation. J Pharm Pharmacol (1966) 18:199-200. doi:10.1111/j.2042-7158.1966.tb07853.x
16. Yang L, Xie M, Yang M, Yu Y, Zhu S, Hou W, et al. PKM2 regulates the Warburg effect and promotes HMGB1 release in sepsis. Nat Commun (2014) 5:4436. doi:10.1038/ncomms5436
17. Kelly B, O'Neill LA. Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Res (2015) 25:771-84. doi:10.1038/cr.2015.68
18. Tannahill GM, Curtis AM, Adamik J, Palsson-Mcdermott EM, Mcgettrick AF, Goel G, et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature (2013) 496:238-42. doi:10.1038/nature11986
19. Moon JS, Hisata S, Park MA, Denicola GM, Ryter SW, Nakahira K, et al. mTORC1-induced HK1-dependent glycolysis regulates NLRP3 inflammasome activation. Cell Rep (2015) 12:102-15. doi:10.1016/j.celrep.2015.05.046
20. Ma H, Liu G, Ding W, Wu Y, Cai L, Zhao Y. Diabetes-induced alteration of F4/80+ macrophages: a study in mice with streptozotocin-induced diabetes for a long term. J Mol Med (Berl) (2008) 86:391-400. doi:10.1007/s00109-008-0304-8
21. Liu G, Hu X, Sun B, Yang T, Shi J, Zhang L, et al. Phosphatase Wip1 negatively regulates neutrophil development through p38 MAPK-STAT1. Blood (2013) 121:519-29. doi:10.1182/blood-2012-05-432674
22. Zhu L, Yang T, Li L, Sun L, Hou Y, Hu X, et al. TSC1 controls macrophage polarization to prevent inflammatory disease. Nat Commun (2014) 5:4696. doi:10.1038/ncomms5696
23. Anthony RM, Urban JF Jr, Alem F, Hamed HA, Rozo CT, Boucher JL, et al. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med (2006) 12:955-60. doi:10.1038/nm1451
24. Weng M, Huntley D, Huang IF, Foye-Jackson O, Wang L, Sarkissian A, et al. Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J Immunol (2007) 179:4721-31. doi:10.4049/jimmunol.179.7.4721
25. Sun C, Sun L, Ma H, Peng J, Zhen Y, Duan K, et al. The phenotype and functional alterations of macrophages in mice with hyperglycemia for long term. J Cell Physiol (2012) 227:1670-9. doi:10.1002/jcp.22891
26. Zhang L, Zhang H, Li L, Xiao Y, Rao E, Miao Z, et al. TSC1/2 signaling complex is essential for peripheral naive CD8+ T cell survival and homeostasis in mice. PLoS One (2012) 7:e30592. doi:10.1371/journal.pone.0030592
27. Sun B, Hu X, Liu G, Ma B, Xu Y, Yang T, et al. Phosphatase Wip1 negatively regulates neutrophil migration and inflammation. J Immunol (2014) 192:1184-95. doi:10.4049/jimmunol.1300656
28. Wu T, Zhao Y, Wang H, Li Y, Shao L, Wang R, et al. mTOR masters monocytic myeloid-derived suppressor cells in mice with allografts or tumors. Sci Rep (2016) 6:20250. doi:10.1038/srep20250
29. Chen H, Zhang L, Wang P, Su H, Wang W, Chu Z, et al. mTORC2 controls Th9 polarization and allergic airway inflammation. Allergy (2017). doi:10.1111/all.13152
30. Haque R, Umstead TM, Ponnuru P, Guo X, Hawgood S, Phelps DS, et al. Role of surfactant protein-A (SP-A) in lung injury in response to acute ozone exposure of SP-A deficient mice. Toxicol Appl Pharmacol (2007) 220:72-82. doi:10.1016/j.taap.2006.12.017
31. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature (2014) 513:559-63. doi:10.1038/nature13490
32. Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer (2008) 8:705-13. doi:10.1038/nrc2468
33. Marin-Hernandez A, Gallardo-Perez JC, Ralph SJ, Rodriguez-Enriquez S, Moreno-Sanchez R. HIF-1alpha modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem (2009) 9:1084-101. doi:10.2174/138955709788922610
34. Ellinghaus P, Heisler I, Unterschemmann K, Haerter M, Beck H, Greschat S, et al. BAY 87-2243, a highly potent and selective inhibitor of hypoxia-induced gene activation has antitumor activities by inhibition of mitochondrial complex I. Cancer Med (2013) 2:611-24. doi:10.1002/cam4.112
35. Murray JK, Balan C, Allgeier AM, Kasparian A, Viswanadhan V, Wilde C, et al. Dipeptidyl-quinolone derivatives inhibit hypoxia inducible factor-1alpha prolyl hydroxylases-1,-2, and-3 with altered selectivity. J Comb Chem (2010) 12:676-86. doi:10.1021/cc100073a
36. Tian YM, Yeoh KK, Lee MK, Eriksson T, Kessler BM, Kramer HB, et al. Differential sensitivity of hypoxia inducible factor hydroxylation sites to hypoxia and hydroxylase inhibitors. J Biol Chem (2011) 286:13041-51. doi:10.1074/jbc.M110.211110
37. O'Neill LA, Hardie DG. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature (2013) 493:346-55. doi:10.1038/nature11862
38. DeSalvo J, Kuznetsov JN, Du J, Leclerc GM, Leclerc GJ, Lampidis TJ, et al. Inhibition of Akt potentiates 2-DG-induced apoptosis via downregulation of UPR in acute lymphoblastic leukemia. Mol Cancer Res (2012) 10:969-78. doi:10.1158/1541-7786.MCR-12-0125
39. Meley D, Bauvy C, Houben-Weerts JH, Dubbelhuis PF, Helmond MT, Codogno P, et al. AMP-activated protein kinase and the regulation of autophagic proteolysis. J Biol Chem (2006) 281:34870-9. doi:10.1074/jbc.M605488200
40. Kim YM, Kim MY, Kim HJ, Roh GS, Ko GH, Seo HG, et al. Compound C independent of AMPK inhibits ICAM-1 and VCAM-1 expression in inflammatory stimulants-activated endothelial cells in vitro and in vivo. Atherosclerosis (2011) 219:57-64. doi:10.1016/j.atherosclerosis.2011.06.043
41. Bowman SM, Free SJ. The structure and synthesis of the fungal cell wall. Bioessays (2006) 28:799-808. doi:10.1002/bies.20441
42. Kreider T, Anthony RM, Urban JF Jr, Gause WC. Alternatively activated macrophages in helminth infections. Curr Opin Immunol (2007) 19:448-53. doi:10.1016/j.coi.2007.07.002
43. Reese TA, Liang HE, Tager AM, Luster AD, Van Rooijen N, Voehringer D, et al. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature (2007) 447:92-6. doi:10.1038/nature05746
44. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol (2010) 11:936-44. doi:10.1038/ni.1920
45. Zhan X, Jia L, Niu Y, Qi H, Chen X, Zhang Q, et al. Targeted depletion of tumour-associated macrophages by an alendronate-glucomannan conjugate for cancer immunotherapy. Biomaterials (2014) 35:10046-57. doi:10.1016/j.biomaterials.2014.09.007
46. Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, et al. Oxidative metabolism and PGC-1 beta attenuate macrophage-mediated inflammation. Cell Metab (2006) 4:255-255. doi:10.1016/j.cmet.2006.08.006
47. Huang SC, Everts B, Ivanova Y, O'Sullivan D, Nascimento M, Smith AM, et al. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat Immunol (2014) 15:846-55. doi:10.1038/ni.2956
48. Sokoloff B, Eddy WH, Saelhof CC, Beach J. Glucose antagonists in experimental cancer. AMA Arch Pathol (1955) 59:729-32
49. Nelson T, Kaufman EE, Sokoloff L. 2-Deoxyglucose incorporation into rat brain glycogen during measurement of local cerebral glucose utilization by the 2-deoxyglucose method. J Neurochem (1984) 43:949-56. doi:10.1111/j.1471-4159.1984.tb12829.x
50. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell (2005) 18:283-93. doi:10.1016/j.molcel.2005.03.027
51. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell (2008) 30:214-26. doi:10.1016/j.molcel.2008.03.003
52. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab (2005) 1:361-70. doi:10.1016/j.cmet.2005.05.004
53. Faubert B, Boily G, Izreig S, Griss T, Samborska B, Dong Z, et al. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metab (2013) 17:113-24. doi:10.1016/j.cmet.2012.12.001
54. Dioum EM, Chen R, Alexander MS, Zhang Q, Hogg RT, Gerard RD, et al. Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science (2009) 324:1289-93. doi:10.1126/science.1169956
55. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med (2010) 207:2439-53. doi:10.1084/jem.20100587
56. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med (2011) 208:1367-76. doi:10.1084/jem.20110278
57. Huang CC, Wang SY, Lin LL, Wang PW, Chen TY, Hsu WM, et al. Glycolytic inhibitor 2-deoxyglucose simultaneously targets cancer and endothelial cells to suppress neuroblastoma growth in mice. Dis Model Mech (2015) 8:1247-54. doi:10.1242/dmm.021667
58. Ciavardelli D, Rossi C, Barcaroli D, Volpe S, Consalvo A, Zucchelli M, et al. Breast cancer stem cells rely on fermentative glycolysis and are sensitive to 2-deoxyglucose treatment. Cell Death Dis (2014) 5:e1336. doi:10.1038/cddis.2014.285
59. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol (2004) 25:677-86. doi:10.1016/j.it.2004.09.015
60. Hagemann T, Wilson J, Burke F, Kulbe H, Li NF, Pluddemann A, et al. Ovarian cancer cells polarize macrophages toward a tumor-associated phenotype. J Immunol (2006) 176:5023-32. doi:10.4049/jimmunol.176.8.5023
61. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science (2011) 331:1612-6. doi:10.1126/science.1198443
62. Melgert BN, Ten Hacken NH, Rutgers B, Timens W, Postma DS, Hylkema MN. More alternative activation of macrophages in lungs of asthmatic patients. J Allergy Clin Immunol (2011) 127:831-3. doi:10.1016/j.jaci.2010.10.045