Hexokinase II binding to mitochondria is necessary for kupffer cell activation and is potentiated by ethanol exposure

Journal of Biological Chemistry

Volumn 289, Issue 38, 2014, Pages 26213-26225

  Shulga, Nataly ^a   Pastorino, John G ^a  

^a UMDNJ School of Osteopathic Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CYCLOPHILIN D; GLUCOSE 6 PHOSPHATE; HEXOKINASE; HEXOKINASE II; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NOD LIKE RECEPTOR FAMILY PYRIN DOMAIN CONTAINING 3; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN P67; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SIRTUIN 3; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ADENYLATE KINASE; CYCLOPHILIN; LIPOPOLYSACCHARIDE; PROTEIN BINDING;

AEROBIC GLYCOLYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME REPRESSION; ETHANOL EXPOSURE; EXPOSURE; GENETIC TRANSFECTION; GLYCOLYSIS; KUPFFER CELL; MACROPHAGE ACTIVATION; MALE; MEMBRANE BINDING; MITOCHONDRIAL BINDING; MITOCHONDRIAL DYNAMICS; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RNA INTERFERENCE; ANIMAL; CELL CULTURE; DRUG EFFECTS; ENZYMOLOGY; IMMUNOLOGY; LIVER MITOCHONDRION; METABOLISM; SPRAGUE DAWLEY RAT; TOXICITY;

ADENYLATE KINASE; ANIMALS; CELLS, CULTURED; CYCLOPHILINS; ETHANOL; HEXOKINASE; INFLAMMASOMES; KUPFFER CELLS; LIPOPOLYSACCHARIDES; MALE; MITOCHONDRIA, LIVER; PROTEIN BINDING; RATS, SPRAGUE-DAWLEY; SIRTUIN 3;

EID: 84907211012     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.580175     Document Type: Article

References (48)

1. Kaczmarek, A., Vandenabeele, P., and Krysko, D. V. (2013) Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38, 209-223
2. Latz, E., Xiao, T. S., and Stutz, A. (2013) Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13, 397-411
3. O'Neill, L. A., Golenbock, D., and Bowie, A. G. (2013) The history of Toll-like receptors-redefining innate immunity. Nat. Rev. Immunol. 13, 453-460
4. Petrasek, J., Bala, S., Csak, T., Lippai, D., Kodys, K., Menashy, V., Barrieau, M., Min, S. Y., Kurt-Jones, E. A., and Szabo, G. (2012) IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J. Clin. Investig. 122, 3476-3489
5. Wen, H., Ting, J. P., and O'Neill, L. A. (2012) A role for the NLRP3 inflammasome in metabolic diseases-did Warburg miss inflammation? Nat. Immunol. 13, 352-357
6. Macintyre, A. N., and Rathmell, J. C. (2013) Activated lymphocytes as a metabolic model for carcinogenesis. Cancer Metab. 1, 5
7. Krawczyk, C. M., Holowka, T., Sun, J., Blagih, J., Amiel, E., DeBerardinis, R. J., Cross, J. R., Jung, E., Thompson, C. B., Jones, R. G., and Pearce, E. J. (2010) Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115, 4742-4749
8. Brand, K. (1997) Aerobic glycolysis by proliferating cells: protection against oxidative stress at the expense of energy yield. J. Bioenerg. Biomembr. 29, 355-364
9. Gatenby, R. A., and Gillies, R. J. (2004) Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4, 891-899
10. Dang, C. V. (2012) Cancer cell metabolism: there is no ROS for the weary. Cancer Discov. 2, 304-307
11. Sun, L., Shukair, S., Naik, T. J., Moazed, F., and Ardehali, H. (2008) Glucose phosphorylation and mitochondrial binding are required for the protective effects of hexokinases I and II. Mol. Cell. Biol. 28, 1007-1017
12. Bustamante, E., Morris, H. P., and Pedersen, P. L. (1981) Energy metabolism of tumor cells. Requirement for a form of hexokinase with a propensity for mitochondrial binding. J. Biol. Chem. 256, 8699-8704
13. Arora, K. K., and Pedersen, P. L. (1988) Functional significance of mitochondrial bound hexokinase in tumor cell metabolism. Evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. J. Biol. Chem. 263, 17422-17428
14. Pastorino, J. G., Shulga, N., and Hoek, J. B. (2002) Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J. Biol. Chem. 277, 7610-7618
15. Abu-Hamad, S., Arbel, N., Calo, D., Arzoine, L., Israelson, A., Keinan, N., Ben-Romano, R., Friedman, O., and Shoshan-Barmatz, V. (2009) The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins. J. Cell Sci. 122, 1906-1916
16. Birnbaum, M. J. (2004) On the InterAktion between hexokinase and the mitochondrion. Dev. Cell 7, 781-782
17. Majewski, N., Nogueira, V., Bhaskar, P., Coy, P. E., Skeen, J. E., Gottlob, K., Chandel, N. S., Thompson, C. B., Robey, R. B., and Hay, N. (2004) Hexokinase- mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830
18. Machida, K., Ohta, Y., and Osada, H. (2006) Suppression of apoptosis by cyclophilin D via stabilization of hexokinase II mitochondrial binding in cancer cells. J. Biol. Chem. 281, 14314-14320
19. Shulga, N., Wilson-Smith, R., and Pastorino, J. G. (2010) Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J. Cell Sci. 123, 894-902
20. Thakur, V., Pritchard, M. T., McMullen, M. R., Wang, Q., and Nagy, L. E. (2006) Chronic ethanol feeding increases activation ofNADPHoxidase by lipopolysaccharide in rat Kupffer cells: role of increased reactive oxygen in LPS-stimulated ERK1/2 activation and TNF-α production. J. Leukoc. Biol. 79, 1348-1356
21. Lippai, D., Bala, S., Petrasek, J., Csak, T., Levin, I., Kurt-Jones, E. A., and Szabo, G. (2013) Alcohol-induced IL-1β in the brain is mediated by NLRP3/ASC inflammasome activation that amplifies neuroinflammation. J. Leukoc. Biol. 94, 171-182
22. Shulga, N., and Pastorino, J. G. (2010) Ethanol sensitizes mitochondria to the permeability transition by inhibiting deacetylation of cyclophilin-D mediated by sirtuin-3. J. Cell Sci. 123, 4117-4127
23. Pastorino, J. G., Simbula, G., Yamamoto, K., Glascott, P. A., Jr., Rothman, R. J., and Farber, J. L. (1996) The cytotoxicity of tumor necrosis factor depends on induction of the mitochondrial permeability transition. J. Biol. Chem. 271, 29792-29798
24. Pastorino, J. G., Hoek, J. B., and Shulga, N. (2005) Activation of glycogen synthase kinase β disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res. 65, 10545-10554
25. Shulga, N., Wilson-Smith, R., and Pastorino, J. G. (2009) Hexokinase II detachment from the mitochondria potentiates cisplatin induced cytotoxicity through a caspase-2 dependent mechanism. Cell Cycle 8, 3355-3364
26. Cooper, M. R., McCall, C. E., and Dechatelet, L. R. (1971) Stimulation of leukocyte hexose monophosphate shunt activity by ascorbic acid. Infect. Immun. 3, 851-853
27. Dieter, M. P., French, J. E., Boorman, G. A., and Luster, M. I. (1987) Metabolic characterization of mouse bone marrow cells responsive to estrogenic inhibition: hexose monophosphate shunt enzyme activity in enriched populations of mature cells and progenitor cells. J. Leukoc. Biol. 41, 212-219
28. Rist, R. J., and Naftalin, R. J. (1991) Dexamethasone inhibits the hexose monophosphate shunt in activated rat peritoneal macrophages by reducing hexokinase-dependent sugar uptake. Biochem. J. 278, 129-135
29. Tsan, M. F. (1977) Stimulation of the hexose monophosphate shunt independent of hydrogen peroxide and superoxide production in rabbit alveolar macrophages during phagocytosis. Blood 50, 935-945
30. Pearce, E. L., Poffenberger, M. C., Chang, C. H., and Jones, R. G. (2013) Fueling immunity: insights into metabolism and lymphocyte function. Science 342, 1242454
31. Minton, K. (2013) Immunometabolism: what is the point of Warburg? Nat. Rev. Immunol. 13, 472
32. Palsson-McDermott, E. M., and O'Neill, L. A. (2013) The Warburg effect then and now: from cancer to inflammatory diseases. BioEssays 35, 965-973
33. 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
34. Elstrom, R. L., Bauer, D. E., Buzzai, M., Karnauskas, R., Harris, M. H., Plas, D. R., Zhuang, H., Cinalli, R. M., Alavi, A., Rudin, C. M., and Thompson, C. B. (2004) Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 64, 3892-3899
35. Shaw, R. J. (2006) Glucose metabolism and cancer. Curr. Opin. Cell Biol. 18, 598-608
36. Glette, J., and Bassøe, H. H. (1982) Stimulation of the hexose monophosphate shunt activity in human polymorphonuclear leukocytes. Adv. Exp. Med. Biol. 141, 393-400
37. Sagone, A. L., Jr., LoBuglio, A. F., and Balcerzak, S. P. (1974) Alterations in hexose monophosphate shunt during lymphoblastic transformation. Cell. Immunol. 14, 443-452
38. Reed, P. W. (1969) Glutathione and the hexose monophosphate shunt in phagocytizing and hydrogen peroxide-treated rat leukocytes. J. Biol. Chem. 244, 2459-2464
39. Samuvel, D. J., Sundararaj, K. P., Nareika, A., Lopes-Virella, M. F., and Huang, Y. (2009) Lactate boosts TLR4 signaling and NF-κB pathwaymediated gene transcription in macrophages via monocarboxylate transporters and MD-2 up-regulation. J. Immunol. 182, 2476-2484
40. Rajamäki, K., Nordström, T., Nurmi, K., Åkerman, K. E., Kovanen, P. T., Öörni, K., and Eklund, K. K. (2013) Extracellular acidosis is a novel danger signal alerting innate immunity via the NLRP3 inflammasome. J. Biol. Chem. 288, 13410-13419
41. McClain, C. J., Barve, S., Deaciuc, I., Kugelmas, M., and Hill, D. (1999) Cytokines in alcoholic liver disease. Semin. Liver Dis. 19, 205-219
42. Nagy, L. E. (2003) Recent insights into the role of the innate immune system in the development of alcoholic liver disease. Exp. Biol. Med. 228, 882-890
43. McVicker, B. L., Tuma, D. J., Kharbanda, K. K., Kubik, J. L., and Casey, C. A. (2007) Effect of chronic ethanol administration on the in vitro production of proinflammatory cytokines by rat Kupffer cells in the presence of apoptotic cells. Alcohol. Clin. Exp. Res. 31, 122-129
44. Pastorino J. G., Marcineviciute, A., Cahill, A., and Hoek, J. B. (1999) Potentiation by chronic ethanol treatment of the mitochondrial permeability transition. Biochem. Biophys. Res. Commun. 265, 405-409
45. King, A. L., Swain, T. M., Mao, Z., Udoh, U. S., Oliva, C. R., Betancourt, A. M., Griguer, C. E., Crowe, D. R., Lesort, M., and Bailey, S. M. (2014) Involvement of the mitochondrial permeability transition pore in chronic ethanol-mediated liver injury in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 306, G265-G277
46. Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., Brunskill, E. W., Sayen, M. R., Gottlieb, R. A., Dorn, G. W., Robbins, J., and Molkentin, J. D. (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662
47. Du, H., Guo, L., Fang, F., Chen, D., Sosunov, A. A., McKhann, G. M., Yan, Y., Wang, C., Zhang, H., Molkentin, J. D., Gunn-Moore, F. J., Vonsattel, J. P., Arancio, O., Chen, J. X., and Yan, S. D. (2008) Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat. Med. 14, 1097-1105
48. Giorgio, V., Soriano, M. E., Basso, E., Bisetto, E., Lippe, G., Forte, M. A., and Bernardi, P. (2010) Cyclophilin D in mitochondrial pathophysiology. Biochim. Biophys. Acta 1797, 1113-1118