Cutting Edge: Critical role of glycolysis in human plasmacytoid dendritic cell antiviral responses

Journal of Immunology

Volumn 196, Issue 5, 2016, Pages 2004-2009

  Bajwa, Gagan ^a,b   DeBerardinis, Ralph J ^a   Shao, Baomei ^b   Hall, Brian ^c   Farrar, J David ^a   Gill, Michelle A ^a,b  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c Amnis Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; B7 ANTIGEN; BETA ACTIN; BETA GLUCURONIDASE; CD123 ANTIGEN; CD2 ASSOCIATED PROTEIN; CD86 ANTIGEN; GLUCOSE; HEXOKINASE; HLA DR ANTIGEN; INFLUENZA VACCINE; INTERFERON REGULATORY FACTOR 7; LACTATE DEHYDROGENASE; LACTIC ACID;

ADULT; ARTICLE; CELL MATURATION; CELL METABOLISM; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; GENETIC ANALYSIS; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VIRUS; MALE; NORMAL HUMAN; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY VIRUS; VIRUS IMMUNITY; VOLUNTEER; DENDRITIC CELL; DNA MICROARRAY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; GAS CHROMATOGRAPHY; IMMUNOLOGY; MASS SPECTROMETRY; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

ADULT; CHROMATOGRAPHY, GAS; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; ENZYME-LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; GLYCOLYSIS; HUMANS; INFLUENZA VACCINES; INFLUENZA, HUMAN; INTERFERON-ALPHA; MALE; MASS SPECTROMETRY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84962030790     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501557     Document Type: Article

References (36)

1. Thompson, W. W., D. K. Shay, E. Weintraub, L. Brammer, C. B. Bridges, N. J. Cox, and K. Fukuda. 2004. Influenza-associated hospitalizations in the United States. JAMA 292: 1333-1340
2. Swiecki, M., and M. Colonna. 2010. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol. Rev. 234: 142-162
3. Swiecki, M., and M. Colonna. 2010. Accumulation of plasmacytoid DC: roles in disease pathogenesis and targets for immunotherapy. Eur. J. Immunol. 40: 2094-2098
4. Gill, M. A., K. Long, T. Kwon, L. Muniz, A. Mejias, J. Connolly, L. Roy, J. Banchereau, and O. Ramilo. 2008. Differential recruitment of dendritic cells and monocytes to respiratory mucosal sites in children with influenza virus or respiratory syncytial virus infection. J. Infect. Dis. 198: 1667-1676
5. Kaminski, M. M., A. Ohnemus, M. Cornitescu, and P. Staeheli. 2012. Plasmacytoid dendritic cells and Toll-like receptor 7-dependent signalling promote efficient protection of mice against highly virulent influenza A virus. J. Gen. Virol. 93: 555-559
6. Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, and Y. J. Liu. 1999. The nature of the principal type 1 interferonproducing cells in human blood. Science 284: 1835-1837
7. Ivashkiv, L. B., and L. T. Donlin. 2014. Regulation of type I interferon responses. Nat. Rev. Immunol. 14: 36-49
8. Kadowaki, N., and Y. J. Liu. 2002. Natural type I interferon-producing cells as a link between innate and adaptive immunity. Hum. Immunol. 63: 1126-1132
9. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531
10. Di Domizio, J., A. Blum, M. Gallagher-Gambarelli, J. P. Molens, L. Chaperot, and J. Plumas. 2009. TLR7 stimulation in human plasmacytoid dendritic cells leads to the induction of early IFN-inducible genes in the absence of type I IFN. Blood 114: 1794-1802
11. Guiducci, C., C. Ghirelli, M. A. Marloie-Provost, T. Matray, R. L. Coffman, Y. J. Liu, F. J. Barrat, and V. Soumelis. 2008. PI3K is critical for the nuclear translocation of IRF-7 and type I IFN production by human plasmacytoid predendritic cells in response to TLR activation. J. Exp. Med. 205: 315-322
12. Chao, Y., N. Kaliaperumal, A. S. Chretien, S. Tang, B. Lee, M. Poidinger, A. M. Fairhurst, and J. E. Connolly. 2014. Human plasmacytoid dendritic cells regulate IFN-a production through activation-induced splicing of IL-18Ra. J. Leukoc. Biol. 96: 1037-1046
13. Cao, W., D. B. Rosen, T. Ito, L. Bover, M. Bao, G. Watanabe, Z. Yao, L. Zhang, L. L. Lanier, and Y. J. Liu. 2006. Plasmacytoid dendritic cell-specific receptor ILT7-FcεRIγ inhibits Toll-like receptor-induced interferon production. J. Exp. Med. 203: 1399-1405
14. Gill, M. A., G. Bajwa, T. A. George, C. C. Dong, I. I. Dougherty, N. Jiang, V. N. Gan, and R. S. Gruchalla. 2010. Counterregulation between the FceεRI pathway and antiviral responses in human plasmacytoid dendritic cells. J. Immunol. 184: 5999-6006
15. Teach, S. J., M. A. Gill, A. Togias, C. A. Sorkness, S. J. Arbes, Jr., A. Calatroni, J. J. Wildfire, P. J. Gergen, R. T. Cohen, J. A. Pongracic, et al. 2015. Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. J. Allergy Clin. Immunol. 136: 1476-1485
16. Piqueras, B., J. Connolly, H. Freitas, A. K. Palucka, and J. Banchereau. 2006. Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107: 2613-2618
17. Semenza, G. L., P. H. Roth, H. M. Fang, and G. L. Wang. 1994. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269: 23757-23763
18. Cramer, T., Y. Yamanishi, B. E. Clausen, I. Förster, R. Pawlinski, N. Mackman, V. H. Haase, R. Jaenisch, M. Corr, V. Nizet, et al. 2003. HIF-1a is essential for myeloid cell-mediated inflammation. Cell 112: 645-657
19. Werth, N., C. Beerlage, C. Rosenberger, A. S. Yazdi, M. Edelmann, A. Amr, W. Bernhardt, C. von Eiff, K. Becker, A. Schäfer, et al. 2010. Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLoS One 5: e11576
20. Tolnay, A. E., C. R. Baskin, T. M. Tumpey, P. J. Sabourin, C. L. Sabourin, J. P. Long, J. A. Pyles, R. A. Albrecht, A. García-Sastre, M. G. Katze, and H. Bielefeldt-Ohmann. 2010. Extrapulmonary tissue responses in cynomolgus macaques (Macaca fascicularis) infected with highly pathogenic avian influenza A (H5N1) virus. Arch. Virol. 155: 905-914
21. Bunnell, T. M., B. J. Burbach, Y. Shimizu, and J. M. Ervasti. 2011. b-Actin specifically controls cell growth, migration, and the G-actin pool. Mol. Biol. Cell 22: 4047-4058
22. Liu, Y. J. 2001. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106: 259-262
23. Srivatsan, S., M. Swiecki, K. Otero, M. Cella, and A. S. Shaw. 2013. CD2- associated protein regulates plasmacytoid dendritic cell migration, but is dispensable for their development and cytokine production. J. Immunol. 191: 5933-5940
24. Nigro, P., G. Pompilio, and M. C. Capogrossi. 2013. Cyclophilin A: a key player for human disease. Cell Death Dis. 4: e888
25. Cao, W., L. Bover, M. Cho, X. Wen, S. Hanabuchi, M. Bao, D. B. Rosen, Y. H. Wang, J. L. Shaw, Q. Du, et al. 2009. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J. Exp. Med. 206: 1603-1614
26. Burke, J. D., L. C. Platanias, and E. N. Fish. 2014. b Interferon regulation of glucose metabolism is PI3K/Akt dependent and important for antiviral activity against coxsackievirus B3. J. Virol. 88: 3485-3495
27. Kuznik, A., M. Bencina, U. Svajger, M. Jeras, B. Rozman, and R. Jerala. 2011. Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J. Immunol. 186: 4794-4804
28. Krawczyk, C. M., T. Holowka, J. Sun, J. Blagih, E. Amiel, R. J. DeBerardinis, J. R. Cross, E. Jung, C. B. Thompson, R. G. Jones, and E. J. Pearce. 2010. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115: 4742-4749
29. Malinarich, F., K. Duan, R. A. Hamid, A. Bijin, W. X. Lin, M. Poidinger, A. M. Fairhurst, and J. E. Connolly. 2015. High mitochondrial respiration and glycolytic capacity represent a metabolic phenotype of human tolerogenic dendritic cells. J. Immunol. 194: 5174-5186
30. MacIver, N. J., R. D. Michalek, and J. C. Rathmell. 2013. Metabolic regulation of T lymphocytes. Annu. Rev. Immunol. 31: 259-283
31. Pfeiffer, T., S. Schuster, and S. Bonhoeffer. 2001. Cooperation and competition in the evolution of ATP-producing pathways. Science 292: 504-507
32. Everts, B., E. Amiel, S. C. Huang, A. M. Smith, C. H. Chang, W. Y. Lam, V. Redmann, T. C. Freitas, J. Blagih, G. J. van der Windt, et al. 2014. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKe supports the anabolic demands of dendritic cell activation. Nat. Immunol. 15: 323-332
33. Tennant, D. A., R. V. Durán, and E. Gottlieb. 2010. Targeting metabolic transformation for cancer therapy. Nat. Rev. Cancer 10: 267-277
34. Dolganiuc, A., S. Chang, K. Kodys, P. Mandrekar, G. Bakis, M. Cormier, and G. Szabo. 2006. Hepatitis C virus (HCV) core protein-induced, monocytemediated mechanisms of reduced IFN-α and plasmacytoid dendritic cell loss in chronic HCV infection. J. Immunol. 177: 6758-6768
35. Soumelis, V., I. Scott, F. Gheyas, D. Bouhour, G. Cozon, L. Cotte, L. Huang, J. A. Levy, and Y. J. Liu. 2001. Depletion of circulating natural type 1 interferon producing cells in HIV-infected AIDS patients. Blood 98: 906-912
36. Kanzler, H., F. J. Barrat, E. M. Hessel, and R. L. Coffman. 2007. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat. Med. 13: 552-559