A metabolic shift toward pentose phosphate pathway is necessary for amyloid fibril- and phorbol 12-myristate 13-Acetate-induced neutrophil extracellular trap (NET) formation

Journal of Biological Chemistry

Volumn 290, Issue 36, 2015, Pages 22174-22183

  Azevedo, Estefania P ^a   Rochael, Natalia C ^a   Guimarães Costa, Anderson B ^a   De Souza Vieira, Thiago S ^a   Ganilho, Juliana ^a   Saraiva, Elvira M ^a   Palhano, Fernando L ^a   Foguel, Debora ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

AMYLOID FIBRIL; EXTRACELLULAR; METABOLIC SHIFT; PENTOSE PHOSPHATE PATHWAY;

METABOLISM;

AMYLOID; CYTOPLASM PROTEIN; FRUCTOSE; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; LACTATE DEHYDROGENASE; MYELOPEROXIDASE; PENTOSE PHOSPHATE; PHORBOL 13 ACETATE 12 MYRISTATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; PROTEIN KINASE B;

ARTICLE; CONTROLLED STUDY; EXTRACELLULAR TRAP; GLUCOSE METABOLISM; HUMAN; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MEMBRANE COMPONENT; MITOCHONDRION; MONOCYTE; NEUTROPHIL; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; CONFOCAL MICROSCOPY; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; METABOLISM; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AMYLOID; EXTRACELLULAR TRAPS; FRUCTOSE; GLUCOSE; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NEUTROPHILS; PENTOSE PHOSPHATE PATHWAY; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; TETRADECANOYLPHORBOL ACETATE;

EID: 84941308720     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.640094     Document Type: Article

References (40)

1. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182
2. Guimarães-Costa A. B, Nascimento M. T., Wardini, A. B., Pinto-da-Silva L. H., Saraiva, E. M. (2012) ETosis: a microbicidal mechanism beyond cell death. J. Parasitol. Res. 2012, 929743
3. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., and Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535
4. Branzk, N., and Papayannopoulos, V. (2013) Molecular mechanisms regulating NETosis in infection and disease. Semin. Immunopathol. 35, 513-530
5. Azevedo, E. P., Guimarães-Costa, A. B., Torezani, G. S., Braga, C. A., Palhano, F. L., Kelly, J. W., Saraiva, E. M., and Foguel, D. (2012) Amyloid fibrils trigger the release of neutrophil extracellular traps (NETs), causing fibril fragmentation by NET-Associated elastase. J. Biol. Chem. 287, 37206-37218
6. Knowles, T. P., Vendruscolo, M., and Dobson, C. M. (2014) The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 15, 384-396
7. Papayannopoulos, V., Metzler, K. D., Hakkim, A., and Zychlinsky, A. (2010) Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191, 677-691
8. Metzler, K. D., Fuchs, T. A., Nauseef, W. M., Reumaux, D., Roesler, J., Schulze, I., Wahn, V., Papayannopoulos, V., and Zychlinsky, A. (2011) Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 117, 953-959
9. Patel, S., Kumar, S., Jyoti, A., Srinag, B. S., Keshari, R. S., Saluja, R., Verma, A., Mitra, K., Barthwal, M. K., Krishnamurthy, H., Bajpai, V. K., and Dikshit, M. (2010) Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation. Nitric Oxide 22, 226-234
10. Cheng, M. L., Ho, H. Y., Lin, H. Y., Lai, Y. C., and Chiu, D. T. (2013) Effective NET formation in neutrophils from individuals with G6PD Taiwan-Hakka is associated with enhanced NADP biosynthesis. Free Radic. Res. 47, 699-709
11. Cooper, P. R., Palmer, L. J., and Chapple, I. L. (2013) Neutrophil extracellular traps as a new paradigm in innate immunity: friend or foe? Periodontol. 2000 63, 165-197
12. Kirchner, T., Möller, S., Klinger, M., Solbach, W., Laskay, T., and Behnen, M. (2012) The impact of various reactive oxygen species on the formation of neutrophil extracellular traps. Mediators Inflamm. 2012, 849136
13. Raad, H., Paclet, M. H., Boussetta, T., Kroviarski, Y., Morel, F., Quinn, M. T., Gougerot-Pocidalo, M. A., Dang, P. M., and El-Benna, J. (2009) Regulation of the phagocyte NADPH oxidase activity: phosphorylation of gp91phox/NOX2 by protein kinase C enhances its diaphorase activity and binding to Rac2, p67phox, and p47phox. FASEB J. 23, 1011-1022
14. Lambeth, J. D., and Neish, A. S. (2014) Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu. Rev. Pathol. 9, 119-145
15. Stanton, R. C. (2012) Glucose-6-phosphate dehydrogenase, NADPH, and cell survival. IUBMB Life 64, 362-369
16. Perner, A., Nielsen, S. E., and Rask-Madsen, J. (2003) High glucose impairs superoxide production from isolated blood neutrophils. Intensive Care Med. 29, 642-645
17. Gray, G. R., Stamatoyannopoulos, G., Naiman, S. C., Kliman, M. R., Klebanoff, S. J., Austin, T., Yoshida, A., and Robinson, G. C. (1973) Neutrophil dysfunction, chronic granulomatous disease, and non-spherocytic haemolytic anaemia caused by complete deficiency of G6PD. Lancet 2, 530-534, 10.1016/S0140-6736(73)92350-7
18. Tsai, K. J., Hung, I. J., Chow, C. K., Stern, A., Chao, S. S., and Chiu, D. T. (1998) Impaired production of nitric oxide, superoxide, and hydrogen peroxide in glucose 6-phosphate-dehydrogenase-deficient granulocytes. FEBS Lett. 436, 411-414
19. Guimarães-Costa, A. B., Nascimento, M. T., Froment, G. S., Soares, R. P., Morgado, F. N., Conceição-Silva, F., and Saraiva, E. M. (2009) Leishmania amazonensis promastigotes induce and are killed by neutrophil extracel-lular traps. Proc. Natl. Acad. Sci. U.S.A. 106, 6748-6753
20. Azevedo, E. P., Pereira, H. M., Garratt, R. C., Kelly, J. W., Foguel, D., and Palhano, F. L. (2011) Dissecting the structure, thermodynamic stability, and aggregation properties of the A25T transthyretin (A25T-TTR) variant involved in leptomeningeal amyloidosis: identifying protein partners that co-Aggregate during A25T-TTR fibrillogenesis in cerebrospinal fluid. Biochemistry 50, 11070-11083
21. Worthington, K., and Worthington, V., eds. (1988) Worthington Manual: Enzymes and Related Biochemicals, 1st Ed., pp. 159-161, Worthington Biochemical Corporation, Freehold, NJ
22. van Raam, B. J., Sluiter, W., de Wit, E., Roos, D., Verhoeven, A. J., and Kuijpers, T. W. (2008) Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organisation. PLoS One 3, e2013
23. Maianski, N. A., Geissler, J., Srinivasula, S. M., Alnemri, E. S., Roos, D., and Kuijpers, T. W. (2004) Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ. 11, 143-153
24. Chacko, B. K., Kramer, P. A., Ravi, S., Johnson, M. S., Hardy, R. W., Ballinger, S. W., and Darley-Usmar, V. M. (2013) Methods for defining distinct bioenergetic profiles in platelets, lymphocytes, monocytes, and neutrophils, and the oxidative burst from human blood. Lab. Invest. 93, 690-700
25. Plesner, L., Plesner, I. W., and Esmann, V. (1974) Kinetic mechanism of glycogen synthase D from human polymorphonuclear leukocytes. J. Biol. Chem. 249, 1119-1125
26. Huang, F. L., and Evans, W. H. (1973) Differences in protein and glycoprotein patterns between mature and immature neutrophil leukocytes. Biochim. Biophys. Acta 317, 394-402
27. Litchfield, W. J., and Wells, W. W. (1977) Selectivity of the 2-deoxyglucose transport system in human and guinea pig polymorphonuclear leukocytes. Infect. Immun. 16, 189-197
28. Martin, S. P., McKinney, G. R and Green, R. (1955) The metabolism of human polymorphonuclear leukocytes. Ann. N.Y. Acad. Sci. 59, 996-1002
29. Gyulkhandanyan, A. V., and Pennefather, P. S. (2004) Shift in the localization of sites of hydrogen peroxide production in brain mitochondria by mitochondrial stress. J Neurochem. 90, 405-421
30. Zmijewski, J. W., Lorne, E., Zhao, X., Tsuruta, Y., Sha, Y., Liu, G., Siegal, G. P., and Abraham, E. (2008) Mitochondrial respiratory complex I regulates neutrophil activation and severity of lung injury. Am. J. Respir. Crit. Care Med. 178, 168-179
31. Zmijewski, J. W., Lorne, E., Banerjee, S., and Abraham, E. (2009) Participation of mitochondrial respiratory complex III in neutrophil activation and lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L624-634
32. Toews, M. L., Liang, M., and Perkins, J. P. (1987) Agonists and phorbol esters desensitize -Adrenergic receptors by different mechanisms. Mol. Pharmacol. 32, 737-742
33. Douda, D. N., Yip, L., Khan, M. A., Grasemann, H., and Palaniyar, N. (2014) Akt is essential to induce NADPH-dependent NETosis and to switch the neutrophil death to apoptosis. Blood. 123, 597-600
34. Peyssonaux, C., and Johnson, R. S. (2004) An unexpected role for hypoxic response: oxygenation and inflammation. Cell Cycle 3, 168-171
35. Rada, B., Jendrysik, M. A., Pang, L., Hayes, C. P., Yoo, D. G., Park, J. J., Moskowitz, S. M., Malech, H. L., and Leto, T. L. (2013) Pyocyanin-enhanced neutrophil extracellular trap formation requires the NADPH oxidase. PLoS One 8, e54205
36. Rabinowitz, J. D., and White, E. (2010) Autophagy and metabolism. Science 330, 1344-1348
37. Rodríguez-Espinosa, O., Rojas-Espinosa, O., Moreno-Altamirano, M. M., López-Villegas, E. O., and Sánchez-García, F. J. (2015) Metabolic requirements for neutrophil extracellular traps (nets) formation. Immunology 145, 213-224
38. Gupte, R. S., Ata, H., Rawat, D., Abe, M., Taylor, M. S., Ochi, R., and Gupte, S. A. (2011) Glucose-6-phosphate dehydrogenase is a regulator of vascular smooth muscle contraction. Antioxid. Redox Signal. 14, 543-558
39. Minucci, A., Giardina, B., Zuppi, C., and Capoluongo, E. (2009) Glucose-6-phosphate dehydrogenase laboratory assay: how, when, and why? IUBMB Life 61, 27-34
40. Louveau, A., Smirnov, I., Keyes, T. J., Eccles, J. D., Rouhani, S. J., Peske, J. D., Derecki, N. C., Castle, D., Mandell, J. W., Lee, K. S., Harris, T. H., Kipnis, J. (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337-341