Short Term Hypoxia Synergizes with Interleukin 15 Priming in Driving Glycolytic Gene Transcription and Supports Human Natural Killer Cell Activities

Journal of Biological Chemistry

Volumn 291, Issue 25, 2016, Pages 12960-12977

  Squez, Sonia Y Velá ^a   Killian, Doreen ^a   Schulte, Jutta ^a   Sticht, Carsten ^b   Thiel, Manfred ^a   Lindner, Holger A ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CYTOLOGY; DISEASES; GENE EXPRESSION; GENES; PATHOLOGY; TRANSCRIPTION;

EXTRACELLULAR MATRICES; GENE EXPRESSION PROFILING; HYPOXIA-INDUCIBLE FACTORS; IMMUNOREGULATORY CYTOKINES; LOW OXYGEN CONDITIONS; MIGRATION INHIBITORY FACTORS; NATURAL KILLER CELLS; SHORT-TERM CULTURES;

CELLS;

CARBON TETRACHLORIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 15; LACTATE DEHYDROGENASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 4; RANTES; ADENOSINE TRIPHOSPHATE; CHEMOKINE; HYPOXIA INDUCIBLE FACTOR 1; IL15 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER IMMUNOTHERAPY; CELL ACTIVITY; CELL FUNCTION; CELL HYPOXIA; CELL KILLING; CELL MIGRATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENERGY YIELD; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLYCOLYSIS; HUMAN; HUMAN CELL; MACROPHAGE; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ADOPTIVE TRANSFER; CELL MOTION; CELL SURVIVAL; GENETICS; K-562 CELL LINE; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS); TRANSCRIPTION INITIATION;

ADENOSINE TRIPHOSPHATE; ADOPTIVE TRANSFER; APOPTOSIS; CELL HYPOXIA; CELL MOVEMENT; CELL SURVIVAL; CHEMOKINES; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; INTERLEUKIN-15; K562 CELLS; KILLER CELLS, NATURAL; L-LACTATE DEHYDROGENASE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84975065591     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.721753     Document Type: Article

References (72)

1. Vivier, E., Raulet, D. H., Moretta, A., Caligiuri, M. A., Zitvogel, L., Lanier, L. L., Yokoyama, W. M., and Ugolini, S. (2011) Innate or adaptive immunity? The example of natural killer cells. Science 331, 44-49
2. Smyth, M. J., Cretney, E., Kelly, J. M., Westwood, J. A., Street, S. E., Yagita, H., Takeda, K., van Dommelen, S. L., Degli-Esposti, M. A., and Hayakawa, Y. (2005) Activation of NK cell cytotoxicity. Mol. Immunol. 42, 501-510
3. Bosco, M. C., Puppo, M., Blengio, F., Fraone, T., Cappello, P., Giovarelli, M., and Varesio, L. (2008) Monocytes and dendritic cells in a hypoxic environment: Spotlights on chemotaxis and migration. Immunobiology 213, 733-749
4. Ohta, A., Diwanji, R., Kini, R., Subramanian, M., Ohta, A., and Sitkovsky, M. (2011) In vivo T cell activation in lymphoid tissues is inhibited in the oxygen-poor microenvironment. Front. Immunol. 2, 27
5. Spencer, J. A., Ferraro, F., Roussakis, E., Klein, A., Wu, J., Runnels, J. M., Zaher, W., Mortensen, L. J., Alt, C., Turcotte, R., Yusuf, R., Côté, D., Vinogradov, S. A., Scadden, D. T., and Lin, C. P. (2014) Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 508, 269-273
6. Carreau, A., El Hafny-Rahbi, B., Matejuk, A., Grillon, C., and Kieda, C. (2011) Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J. Cell. Mol. Med. 15, 1239-1253
7. Sitkovsky, M., and Lukashev, D. (2005) Regulation of immune cells by local-tissue oxygen tension: HIF1α and adenosine receptors. Nat. Rev. Immunol. 5, 712-721
8. Eltzschig, H. K., and Carmeliet, P. (2011) Hypoxia and inflammation. N. Engl. J. Med. 364, 656-665
9. Casazza, A., Di Conza, G., Wenes, M., Finisguerra, V., Deschoemaeker, S., and Mazzone, M. (2014) Tumor stroma: a complexity dictated by the hypoxic tumor microenvironment. Oncogene 33, 1743-1754
10. Baginska, J., Viry, E., Paggetti, J., Medves, S., Berchem, G., Moussay, E., and Janji, B. (2013) The critical role of the tumor microenvironment in shaping natural killer cell-mediated anti-tumor immunity. Front. Immunol. 4, 490
11. Balsamo, M., Manzini, C., Pietra, G., Raggi, F., Blengio, F., Mingari, M. C., Varesio, L., Moretta, L., Bosco, M. C., and Vitale, M. (2013) Hypoxia downregulates the expression of activating receptors involved in NK-cellmediated target cell killing without affecting ADCC. Eur. J. Immunol. 43, 2756-2764
12. Fink, T., Ebbesen, P., Koppelhus, U., and Zachar, V. (2003) Natural killer cell-mediated basal and interferon-enhanced cytotoxicity against liver cancer cells is significantly impaired under in vivo oxygen conditions. Scand. J. Immunol. 58, 607-612
13. Sarkar, S., Germeraad, W. T., Rouschop, K. M., Steeghs, E. M., van Gelder, M., Bos, G. M., and Wieten, L. (2013) Hypoxia induced impairment of NK cell cytotoxicity against multiple myeloma can be overcome by IL-2 activation of the NK cells. PLoS ONE 8, e64835
14. Long, E. O., Kim, H. S., Liu, D., Peterson, M. E., and Rajagopalan, S. (2013) Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol. 31, 227-258
15. Mishra, A., Sullivan, L., and Caligiuri, M. A. (2014) Molecular pathways: interleukin-15 signaling in health and in cancer. Clin. Cancer Res. 20, 2044-2050
16. Van den Bergh, J. M., Van Tendeloo, V. F., and Smits, E. L. (2015) Interleukin-15: new kid on the block for antitumor combination therapy. Cytokine Growth Factor Rev. 26, 15-24
17. Donnelly, R. P., Loftus, R. M., Keating, S. E., Liou, K. T., Biron, C. A., Gardiner, C. M., and Finlay, D. K. (2014) mTORC1-dependent metabolic reprogramming is a prerequisite for NK cell effector function. J. Immunol. 193, 4477- 4484
18. Nandagopal, N., Ali, A. K., Komal, A. K., and Lee, S. H. (2014) The critical role of IL-15-PI3K-mTOR pathway in natural killer cell effector functions. Front. Immunol. 5, 187
19. Marçais, A., Cherfils-Vicini, J., Viant, C., Degouve, S., Viel, S., Fenis, A., Rabilloud, J., Mayol, K., Tavares, A., Bienvenu, J., Gangloff, Y. G., Gilson, E., Vivier, E., and Walzer, T. (2014) The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol. 15, 749-757
20. Keppel, M. P., Saucier, N., Mah, A. Y., Vogel, T. P., and Cooper, M. A. (2015) Activation-specific metabolic requirements for NK Cell IFN-γ production. J. Immunol. 194, 1954-1962
21. Knorr, D. A., Bachanova, V., Verneris, M. R., and Miller, J. S. (2014) Clinical utility of natural killer cells in cancer therapy and transplantation. Semin. Immunol. 26, 161-172
22. Yoon, S. R., Kim, T. D., and Choi, I. (2015) Understanding of molecular mechanisms in natural killer cell therapy. Exp. Mol. Med. 47, e141
23. Childs, R. W., and Carlsten, M. (2015) Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: the force awakens. Nat. Rev. Drug Discov. 14, 487-498
24. Domogala, A., Madrigal, J. A., and Saudemont, A. (2015) Natural killer cell immunotherapy: from bench to bedside. Front. Immunol. 6, 264
25. Kim, T. D., Lee, S. U., Yun, S., Sun, H. N., Lee, S. H., Kim, J. W., Kim, H. M., Park, S. K., Lee, C. W., Yoon, S. R., Greenberg, P. D., and Choi, I. (2011) Human microRNA-27a targets Prf1 and GzmB expression to regulate NK-cell cytotoxicity. Blood 118, 5476-5486
26. Dai, M., Wang, P., Boyd, A. D., Kostov, G., Athey, B., Jones, E. G., Bunney, W. E., Myers, R. M., Speed, T. P., Akil, H., Watson, S. J., and Meng, F. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175
27. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., and Mesirov, J. P. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550
28. Edsparr, K., Johansson, B. R., Goldfarb, R. H., Basse, P. H., Nannmark, U., Speetjens, F. M., Kuppen, P. J., Lennernäs, B., and Albertsson, P. (2009) Human NK cell lines migrate differentially in vitro related to matrix interaction and MMP expression. Immunol. Cell Biol. 87, 489-495
29. Bentz, S., Cee, A., Endlicher, E., Wojtal, K. A., Naami, A., Pesch, T., Lang, S., Schubert, P., Fried, M., Weber, A., Coy, J. F., Goelder, S., Knüchel, R., Hausmann, M., and Rogler, G. (2013) Hypoxia induces the expression of transketolase-like 1 in human colorectal cancer. Digestion 88, 182-192
30. Semenza, G. L. (2009) Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology 24, 97-106
31. Yalcin, A., Telang, S., Clem, B., and Chesney, J. (2009) Regulation of glucose metabolism by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatases in cancer. Exp. Mol. Pathol. 86, 174-179
32. Telang, S., Clem, B. F., Klarer, A. C., Clem, A. L., Trent, J. O., Bucala, R., and Chesney, J. (2012) Small molecule inhibition of 6-phosphofructo-2-kinase suppresses T cell activation. J. Transl. Med. 10, 95
33. Kim, J. W., Tchernyshyov, I., Semenza, G. L., and Dang, C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185
34. Papandreou, I., Cairns, R. A., Fontana, L., Lim, A. L., and Denko, N. C. (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 3, 187-197
35. Grimm, M., Schmitt, S., Teriete, P., Biegner, T., Stenzl, A., Hennenlotter, J., Muhs, H. J., Munz, A., Nadtotschi, T., König, K., Sänger, J., Feyen, O., Hofmann, H., Reinert, S., and Coy, J. F. (2013) A biomarker based detection and characterization of carcinomas exploiting two fundamental biophysical mechanisms in mammalian cells. BMC Cancer 13, 569
36. Buck, M. D., O'Sullivan, D., and Pearce, E. L. (2015) T cell metabolism drives immunity. J. Exp. Med. 212, 1345-1360
37. Palazon, A., Goldrath, A. W., Nizet, V., and Johnson, R. S. (2014) HIF transcription factors, inflammation, and immunity. Immunity 41, 518-528
38. Pearce, E. L., and Pearce, E. J. (2013) Metabolic pathways in immune cell activation and quiescence. Immunity 38, 633-643
39. Ganeshan, K., and Chawla, A. (2014) Metabolic regulation of immune responses. Annu. Rev. Immunol. 32, 609-634
40. Ghesquière, B., Wong, B. W., Kuchnio, A., and Carmeliet, P. (2014) Metabolism of stromal and immune cells in health and disease. Nature 511, 167-176
41. Roiniotis, J., Dinh, H., Masendycz, P., Turner, A., Elsegood, C. L., Scholz, G. M., and Hamilton, J. A. (2009) Hypoxia prolongs monocyte/macrophage survival and enhanced glycolysis is associated with their maturation under aerobic conditions. J. Immunol. 182, 7974-7981
42. Horng, T. (2015) mTOR trains heightened macrophage responses. Trends Immunol. 36, 1-2
43. Pearce, E. J., and Everts, B. (2015) Dendritic cell metabolism. Nat. Rev. Immunol. 15, 18-29
44. Finlay, D. K., Rosenzweig, E., Sinclair, L. V., Feijoo-Carnero, C., Hukelmann, J. L., Rolf, J., Panteleyev, A. A., Okkenhaug, K., and Cantrell, D. A. (2012) PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8 + T cells. J. Exp. Med. 209, 2441-2453
45. Kung, A. L., Zabludoff, S. D., France, D. S., Freedman, S. J., Tanner, E. A., Vieira, A., Cornell-Kennon, S., Lee, J., Wang, B., Wang, J., Memmert, K., Naegeli, H. U., Petersen, F., Eck, M. J., Bair, K. W., et al. (2004) Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway. Cancer Cell. 6, 33-43
46. Maghazachi, A. A. (2010) Role of chemokines in the biology of natural killer cells. Curr. Top. Microbiol. Immunol. 341, 37-58
47. Maurer, M., and von Stebut, E. (2004) Macrophage inflammatory protein-1. Int. J. Biochem. Cell Biol. 36, 1882-1886
48. Grayson, M. H., and Holtzman, M. J. (2006) Chemokine complexity: the case for CCL5. Am. J. Respir. Cell Mol. Biol. 35, 143-146
49. Cowell, R. M., Xu, H., Galasso, J. M., and Silverstein, F. S. (2002) Hypoxicischemic injury induces macrophage inflammatory protein-1α expression in immature rat brain. Stroke 33, 795-801
50. Yoshida, S., Yoshida, A., Ishibashi, T., Elner, S. G., and Elner, V. M. (2003) Role of MCP-1 and MIP-1α in retinal neovascularization during postischemic inflammation in a mouse model of retinal neovascularization. J. Leukocyte Biol. 73, 137-144
51. Gonsalves, C., and Kalra, V. K. (2010) Endothelin-1-induced macrophage inflammatory protein-1β expression in monocytic cells involves hypoxiainducible factor-1α and AP-1 and is negatively regulated by microRNA-195. J. Immunol. 185, 6253- 6264
52. Walmsley, S. R., Print, C., Farahi, N., Peyssonnaux, C., Johnson, R. S., Cramer, T., Sobolewski, A., Condliffe, A. M., Cowburn, A. S., Johnson, N., and Chilvers, E. R. (2005) Hypoxia-induced neutrophil survival is mediated by HIF-1α dependent NF-oκB activity. J. Exp. Med. 201, 105-115
53. Arnaud, C., Beguin, P. C., Lantuejoul, S., Pepin, J. L., Guillermet, C., Pelli, G., Burger, F., Buatois, V., Ribuot, C., Baguet, J. P., Mach, F., Levy, P., and Dematteis, M. (2011) The inflammatory preatherosclerotic remodeling induced by intermittent hypoxia is attenuated by RANTES/CCL5 inhibition. Am. J. Respir. Crit. Care Med. 184, 724-731
54. Yeligar, S. M., Machida, K., Tsukamoto, H., and Kalra, V. K. (2009) Ethanol augments RANTES/CCL5 expression in rat liver sinusoidal endothelial cells and human endothelial cells via activation of NF-ôB, HIF-1ô, and AP-1. J. Immunol. 183, 5964-5976
55. Skurk, T., Mack, I., Kempf, K., Kolb, H., Hauner, H., and Herder, C. (2009) Expression and secretion of RANTES (CCL5) in human adipocytes in response to immunological stimuli and hypoxia. Horm. Metab. Res. 41, 183-189
56. Lin, S., Wan, S., Sun, L., Hu, J., Fang, D., Zhao, R., Yuan, S., and Zhang, L. (2012) Chemokine C-C motif receptor 5 and C-C motif ligand 5 promote cancer cell migration under hypoxia. Cancer Sci. 103, 904-912
57. Allavena, P., Giardina, G., Bianchi, G., and Mantovani, A. (1997) IL-15 is chemotactic for natural killer cells and stimulates their adhesion to vascular endothelium. J. Leukocyte Biol. 61, 729-735
58. Taub, D. D., Sayers, T. J., Carter, C. R., and Ortaldo, J. R. (1995) ô and ô chemokines induce NK cell migration and enhance NK-mediated cytolysis. J. Immunol. 155, 3877-3888
59. Edsparr, K., Basse, P. H., Goldfarb, R. H., and Albertsson, P. (2011) Matrix metalloproteinases in cytotoxic lymphocytes impact on tumour infiltration and immunomodulation. Cancer Microenviron. 4, 351-360
60. Prakash, M. D., Munoz, M. A., Jain, R., Tong, P. L., Koskinen, A., Regner, M., Kleifeld, O., Ho, B., Olson, M., Turner, S. J., Mrass, P., Weninger, W., and Bird, P. I. (2014) Granzyme B promotes cytotoxic lymphocyte transmigration via basement membrane remodeling. Immunity 41, 960-972
61. Grieb, G., Merk, M., Bernhagen, J., and Bucala, R. (2010) Macrophage migration inhibitory factor (MIF): a promising biomarker. Drug News Per-spect. 23, 257-264
62. Simons, D., Grieb, G., Hristov, M., Pallua, N., Weber, C., Bernhagen, J., and Steffens, G. (2011) Hypoxia-induced endothelial secretion of macrophage migration inhibitory factor and role in endothelial progenitor cell recruitment. J. Cell. Mol. Med. 15, 668-678
63. Hira, E., Ono, T., Dhar, D. K., El-Assal, O. N., Hishikawa, Y., Yamanoi, A., and Nagasue, N. (2005) Overexpression of macrophage migration inhibitory factor induces angiogenesis and deteriorates prognosis after radical resection for hepatocellular carcinoma. Cancer 103, 588-598
64. Bacher, M., Schrader, J., Thompson, N., Kuschela, K., Gemsa, D., Waeber, G., and Schlegel, J. (2003) Up-regulation of macrophage migration inhibitory factor gene and protein expression in glial tumor cells during hypoxic and hypoglycemic stress indicates a critical role for angiogenesis in glioblastoma multiforme. Am. J. Pathol. 162, 11-17
65. Krockenberger, M., Dombrowski, Y., Weidler, C., Ossadnik, M., Hönig, A., Häusler, S., Voigt, H., Becker, J. C., Leng, L., Steinle, A., Weller, M., Bucala, R., Dietl, J., and Wischhusen, J. (2008) Macrophage migration inhibitory factor contributes to the immune escape of ovarian cancer by down-regulating NKG2D. J. Immunol. 180, 7338-7348
66. Berthou, C., Bourge, J. F., Zhang, Y., Soulié, A., Geromin, D., Denizot, Y., Sigaux, F., and Sasportes, M. (2000) Interferon-ô-induced membrane PAF-receptor expression confers tumor cell susceptibility to NK perforindependent lysis. Blood 95, 2329-2336
67. Kurschus, F. C., Bruno, R., Fellows, E., Falk, C. S., and Jenne, D. E. (2005) Membrane receptors are not required to deliver granzyme B during killer cell attack. Blood 105, 2049-2058
68. Martinvalet, D., Zhu, P., and Lieberman, J. (2005) Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis. Immunity 22, 355-370
69. Peter, C., Wesselborg, S., Herrmann, M., and Lauber, K. (2010) Dangerous attraction: phagocyte recruitment and danger signals of apoptotic and necrotic cells. Apoptosis 15, 1007-1028
70. Kepp, O., Galluzzi, L., Martins, I., Schlemmer, F., Adjemian, S., Michaud, M., Sukkurwala, A. Q., Menger, L., Zitvogel, L., and Kroemer, G. (2011) Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metastasis Rev. 30, 61-69
71. Bezu, L., Gomes-de-Silva, L. C., Dewitte, H., Breckpot, K., Fucikova, J., Spisek, R., Galluzzi, L., Kepp, O., and Kroemer, G. (2015) Combinatorial strategies for the induction of immunogenic cell death. Front. Immunol. 6, 187
72. Hatfield, S. M., Kjaergaard, J., Lukashev, D., Schreiber, T. H., Belikoff, B., Abbott, R., Sethumadhavan, S., Philbrook, P., Ko, K., Cannici, R., Thayer, M., Rodig, S., Kutok, J. L., Jackson, E. K., Karger, B., et al. (2015) Immunological mechanisms of the antitumor effects of supplemental oxygenation. Sci. Transl. Med. 7, 277ra30