Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2017, Article ID 9029327, 10 pages
https://doi.org/10.1155/2017/9029327
Research Article

HIF1α-Induced Glycolysis Metabolism Is Essential to the Activation of Inflammatory Macrophages

Department of Physiology and Pathophysiology, Key Laboratory of Molecular Cardiovascular Sciences, Ministry of Education, School of Basic Medical Sciences, Peking University, Beijing 100191, China

Correspondence should be addressed to Changtao Jiang; nc.ude.umjb@oatgnahcgnaij

Received 11 May 2017; Accepted 20 August 2017; Published 13 December 2017

Academic Editor: Hua Wang

Copyright © 2017 Ting Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Cursiefen, L. Chen, L. P. Borges et al., “VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment,” The Journal of Clinical Investigation, vol. 113, no. 7, pp. 1040–1050, 2004. View at Publisher · View at Google Scholar
  2. A. Mantovani, S. Sozzani, M. Locati, P. Allavena, and A. Sica, “Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes,” Trends in Immunology, vol. 23, no. 11, pp. 549–555, 2002. View at Google Scholar
  3. K. J. Moore, F. J. Sheedy, and E. A. Fisher, “Macrophages in atherosclerosis: a dynamic balance,” Nature Reviews Immunology, vol. 13, no. 10, pp. 709–721, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. R. W. Kinne, R. Brauer, B. Stuhlmuller, E. Palombo-Kinne, and G. R. Burmester, “Macrophages in rheumatoid arthritis,” Arthritis Research, vol. 2, no. 3, pp. 189–202, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. E. Careau and E. Y. Bissonnette, “Adoptive transfer of alveolar macrophages abrogates bronchial hyperresponsiveness,” American Journal of Respiratory Cell and Molecular Biology, vol. 31, no. 1, pp. 22–27, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. E. M. Palsson-McDermott, A. M. Curtis, G. Goel et al., “Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the Warburg effect in LPS-activated macrophages,” Cell Metabolism, vol. 21, no. 1, pp. 65–80, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Sica and V. Bronte, “Altered macrophage differentiation and immune dysfunction in tumor development,” The Journal of Clinical Investigation, vol. 117, no. 5, pp. 1155–1166, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. A. L. Doedens, C. Stockmann, M. P. Rubinstein et al., “Macrophage expression of hypoxia-inducible factor-1α suppresses T-cell function and promotes tumor progression,” Cancer Research, vol. 70, no. 19, pp. 7465–7475, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. A. L. Pauleau, R. Rutschman, R. Lang, A. Pernis, S. S. Watowich, and P. J. Murray, “Enhancer-mediated control of macrophage-specific arginase I expression,” Journal of Immunology, vol. 172, no. 12, pp. 7565–7573, 2004. View at Google Scholar
  10. Z. Tan, N. Xie, H. Cui et al., “Pyruvate dehydrogenase kinase 1 participates in macrophage polarization via regulating glucose metabolism,” Journal of Immunology, vol. 194, no. 12, pp. 6082–6089, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. R. K. Bruick and S. L. McKnight, “A conserved family of prolyl-4-hydroxylases that modify HIF,” Science, vol. 294, no. 5545, pp. 1337–1340, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Murdoch, A. Giannoudis, and C. E. Lewis, “Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues,” Blood, vol. 104, no. 8, pp. 2224–2234, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. G. M. Tannahill, A. M. Curtis, J. Adamik et al., “Succinate is an inflammatory signal that induces IL-1β through HIF-1α,” Nature, vol. 496, no. 7444, pp. 238–242, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. P. M. Gubser, G. R. Bantug, L. Razik et al., “Rapid effector function of memory CD8+ T cells requires an immediate-early glycolytic switch,” Nature Immunology, vol. 14, no. 10, pp. 1064–1072, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. G. L. Wang, B. H. Jiang, E. A. Rue, and G. L. Semenza, “Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 12, pp. 5510–5514, 1995. View at Google Scholar
  16. T. Cramer, Y. Yamanishi, B. E. Clausen et al., “HIF-1α is essential for myeloid cell-mediated inflammation,” Cell, vol. 112, no. 5, pp. 645–657, 2003. View at Google Scholar
  17. W. G. Kaelin Jr. and P. J. Ratcliffe, “Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway,” Molecular Cell, vol. 30, no. 4, pp. 393–402, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. Q. He, Z. Gao, J. Yin, J. Zhang, Z. Yun, and J. Ye, “Regulation of HIF-1α activity in adipose tissue by obesity-associated factors: adipogenesis, insulin, and hypoxia,” American Journal of Physiology. Endocrinology and Metabolism, vol. 300, no. 5, pp. E877–E885, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Weidemann and R. S. Johnson, “Biology of HIF-1α,” Cell Death and Differentiation, vol. 15, no. 4, pp. 621–627, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Nizet and R. S. Johnson, “Interdependence of hypoxic and innate immune responses,” Nature Reviews Immunology, vol. 9, no. 9, pp. 609–617, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. J. S. Lewis, J. A. Lee, J. C. Underwood, A. L. Harris, and C. E. Lewis, “Macrophage responses to hypoxia: relevance to disease mechanisms,” Journal of Leukocyte Biology, vol. 66, no. 6, pp. 889–900, 1999. View at Google Scholar
  22. K. Y. Lee, S. Gesta, J. Boucher, X. L. Wang, and C. R. Kahn, “The differential role of Hif1β/Arnt and the hypoxic response in adipose function, fibrosis, and inflammation,” Cell Metabolism, vol. 14, no. 4, pp. 491–503, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Kelly and L. A. O'Neill, “Metabolic reprogramming in macrophages and dendritic cells in innate immunity,” Cell Research, vol. 25, no. 7, pp. 771–784, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. L. A. O'Neill and E. J. Pearce, “Immunometabolism governs dendritic cell and macrophage function,” The Journal of Experimental Medicine, vol. 213, no. 1, pp. 15–23, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. X. Xue, S. Ramakrishnan, E. Anderson et al., “Endothelial PAS domain protein 1 activates the inflammatory response in the intestinal epithelium to promote colitis in mice,” Gastroenterology, vol. 145, no. 4, pp. 831–841, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Seki, Y. Habu, T. Kawamura et al., “The liver as a crucial organ in the first line of host defense: the roles of Kupffer cells, natural killer (NK) cells and NK1.1 Ag+ T cells in T helper 1 immune responses,” Immunological Reviews, vol. 174, pp. 35–46, 2000. View at Google Scholar
  27. F. Tacke and H. W. Zimmermann, “Macrophage heterogeneity in liver injury and fibrosis,” Journal of Hepatology, vol. 60, no. 5, pp. 1090–1096, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. C. A. Toth and P. Thomas, “Liver endocytosis and Kupffer cells,” Hepatology, vol. 16, no. 1, pp. 255–266, 1992. View at Google Scholar
  29. S. Gordon and F. O. Martinez, “Alternative activation of macrophages: mechanism and functions,” Immunity, vol. 32, no. 5, pp. 593–604, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. W. Zhang, J. M. Petrovic, D. Callaghan et al., “Evidence that hypoxia-inducible factor-1 (HIF-1) mediates transcriptional activation of interleukin-1β (IL-1β) in astrocyte cultures,” Journal of Neuroimmunology, vol. 174, no. 1-2, pp. 63–73, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. W. Ertel, M. H. Morrison, A. Ayala, and I. H. Chaudry, “Hypoxemia in the absence of blood loss or significant hypotension causes inflammatory cytokine release,” The American Journal of Physiology, vol. 269, no. 1, Part 2, pp. R160–R166, 1995. View at Google Scholar
  32. N. Takeda, E. L. O'Dea, A. Doedens et al., “Differential activation and antagonistic function of HIF-α isoforms in macrophages are essential for NO homeostasis,” Genes & Development, vol. 24, no. 5, pp. 491–501, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Nishi, T. Oda, S. Takabuchi et al., “LPS induces hypoxia-inducible factor 1 activation in macrophage-differentiated cells in a reactive oxygen species-dependent manner,” Antioxidants & Redox Signaling, vol. 10, no. 5, pp. 983–995, 2008. View at Google Scholar
  34. A. Tawakol, P. Singh, M. Mojena et al., “HIF-1α and PFKFB3 mediate a tight relationship between proinflammatory activation and anerobic metabolism in atherosclerotic macrophages,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 35, no. 6, pp. 1463–1471, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. J. M. Olefsky and C. K. Glass, “Macrophages, inflammation, and insulin resistance,” Annual Review of Physiology, vol. 72, pp. 219–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. H. J. Wang, Y. J. Hsieh, W. C. Cheng et al., “JMJD5 regulates PKM2 nuclear translocation and reprograms HIF-1α-mediated glucose metabolism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 1, p. 284, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Chawla, K. D. Nguyen, and Y. P. Goh, “Macrophage-mediated inflammation in metabolic disease,” Nature Reviews Immunology, vol. 11, no. 11, pp. 738–749, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Haschemi, P. Kosma, L. Gille et al., “The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism,” Cell Metabolism, vol. 15, no. 6, pp. 813–826, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Liu, Y. Lu, J. Martinez et al., “Proinflammatory signal suppresses proliferation and shifts macrophage metabolism from Myc-dependent to HIF1α-dependent,” Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 6, pp. 1564–1569, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. M. K. Shin, L. F. Drager, Q. Yao et al., “Metabolic consequences of high-fat diet are attenuated by suppression of HIF-1α,” PLoS One, vol. 7, no. 10, article e46562, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Galvan-Pena and L. A. O'Neill, “Metabolic reprograming in macrophage polarization,” Frontiers in Immunology, vol. 5, p. 420, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. J. Freemerman, A. R. Johnson, G. N. Sacks et al., “Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype,” The Journal of Biological Chemistry, vol. 289, no. 11, pp. 7884–7896, 2014. View at Publisher · View at Google Scholar · View at Scopus