GCN2-dependent metabolic stress is essential for endotoxemic cytokine induction and pathology

Molecular and Cellular Biology

Volumn 34, Issue 3, 2014, Pages 428-438

  Liu, Haiyun ^a   Huang, Lei ^a   Bradley, Jillian ^a   Liu, Kebin ^a   Bardhan, Kankana ^a   Ron, David ^b   Mellor, Andrew L ^a   Munn, David H ^a   McGaha, Tracy L ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INITIATION FACTOR 2ALPHA; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PROTEIN; PROTEIN GCN2; TOLL LIKE RECEPTOR 4; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTOXEMIA; GENE EXPRESSION; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; METABOLIC STRESS; MORTALITY; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SEPTICEMIA; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; BLOTTING, WESTERN; CELL LINE; CYTOKINES; ENDOTOXEMIA; ENZYME-LINKED IMMUNOSORBENT ASSAY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INFLAMMATION MEDIATORS; INTERLEUKIN-12; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR CHOP; TRYPTOPHAN;

EID: 84892464676     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00946-13     Document Type: Article

References (45)

1. McGaha TL, Chen Y, Ravishankar B, van Rooijen N, Karlsson MC. 2011. Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 117:5403-5412. http://dx.doi.org/10.1182/blood-2010-11-320028.
2. Murray PJ, Wynn TA. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11:723-737. http://dx.doi.org/10.1038/nri3073.
3. Ravishankar B, Liu H, Shinde R, Chandler P, Baban B, Tanaka M, Munn DH, Mellor AL, Karlsson MC, McGaha TL. 2012. Tolerance to apoptotic cells is regulated by indoleamine 2,3-dioxygenase. Proc. Natl. Acad. Sci. U. S. A. 109:3909-3914. http://dx.doi.org/10.1073/pnas.1117736109.
4. Aragonés J, Elorza A, Acosta-Iborra B, Landazuri MO. 2011. Myeloid hypoxia-inducible factors in inflammatory diseases. Crit. Rev. Immunol. 31:1-13. http://dx.doi.org/10.1615/CritRevImmunol.v31.i1.10.
5. McGaha TL, Huang L, Lemos H, Metz R, Mautino M, Prendergast GC, Mellor AL. 2012. Amino acid catabolism: a pivotal regulator of innate and adaptive immunity. Immunol. Rev. 249:135-157. http://dx.doi.org/10.1111/j.1600-065X.2012.01149.x.
6. Munn DH, Mellor AL. 2013. Indoleamine 2,3 dioxygenase and metabolic control of immune responses. Trends Immunol. 34:137-143. http://dx.doi.org/10.1016/j.it.2012.10.001.
7. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, Azuma M, Blazar BR, Mellor AL, Munn DH. 2007. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J. Clin. Invest. 117:2570-2582. http://dx.doi.org/10.1172/JCI31911.
8. Jung ID, Lee MG, Chang JH, Lee JS, Jeong YI, Lee CM, Park WS, Han J, Seo SK, Lee SY, Park YM. 2009. Blockade of indoleamine 2,3-dioxygenase protects mice against lipopolysaccharide-induced endotoxin shock. J. Immunol. 182:3146-3154. http://dx.doi.org/10.4049/jimmunol.0803104.
9. Smith C, Chang MY, Parker KH, Beury DW, DuHadaway JB, Flick HE, Boulden J, Sutanto-Ward E, Soler AP, Laury-Kleintop LD, Mandik-Nayak L, Metz R, Ostrand-Rosenberg S, Prendergast GC, Muller AJ. 2012. IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer Discov. 2:722-735. http://dx.doi.org/10.1158/2159 -8290.CD-12-0014.
10. Huang L, Lemos HP, Li L, Li M, Chandler PR, Baban B, McGaha TL, Ravishankar B, Lee JR, Munn DH, Mellor AL. 2012. Engineering DNA nanoparticles as immunomodulatory reagents that activate regulatory T cells. J. Immunol. 188:4913-4920. http://dx.doi.org/10.4049/jimmunol.1103668.
11. Munn DH, Mellor AL. 2007. Indoleamine 2,3-dioxygenase and tumorinduced tolerance. J. Clin. Invest. 117:1147-1154. http://dx.doi.org/10.1172/JCI31178.
12. Munn DH, Sharma MD, Baban B, Harding HP, Zhang Y, Ron D, Mellor AL. 2005. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22:633-642. http://dx.doi.org/10.1016/j.immuni.2005.03.013.
13. Desvignes L, Ernst JD. 2009. Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 31:974-985. http://dx.doi.org/10.1016/j.immuni.2009.10.007.
14. Fallarino F, Grohmann U, Vacca C, Orabona C, Spreca A, Fioretti MC, Puccetti P. 2003. T cell apoptosis by kynurenines. Adv. Exp. Med. Biol. 527:183-190. http://dx.doi.org/10.1007/978-1-4615-0135-0_21.
15. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, Vacca C, Orabona C, Bianchi R, Belladonna ML, Volpi C, Santamaria P, Fioretti MC, Puccetti P. 2006. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J. Immunol. 176:6752-6761.
16. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-1108. http://dx.doi.org/10.1016/S1097-2765(00)00108-8.
17. Caristi S, Piraino G, Cucinotta M, Valenti A, Loddo S, Teti D. 2005. Prostaglandin E2 induces interleukin-8 gene transcription by activating C/EBP homologous protein in human T lymphocytes. J. Biol. Chem. 280: 14433-14442. http://dx.doi.org/10.1074/jbc.M410725200.
18. Li Y, Schwabe RF, DeVries-Seimon T, Yao PM, Gerbod-Giannone MC, Tall AR, Davis RJ, Flavell R, Brenner DA, Tabas I. 2005. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-alpha and interleukin-6: model of NF-kappaB- and map kinasedependent inflammation in advanced atherosclerosis. J. Biol. Chem. 280: 21763-21772. http://dx.doi.org/10.1074/jbc.M501759200.
19. Mahadevan NR, Rodvold J, Sepulveda H, Rossi S, Drew AF, Zanetti M. 2011. Transmission of endoplasmic reticulum stress and proinflammation from tumor cells to myeloid cells. Proc. Natl. Acad. Sci. U. S. A. 108:6561-6566. http://dx.doi.org/10.1073/pnas.1008942108.
20. Hawes AS, Rock CS, Keogh CV, Lowry SF, Calvano SE. 1992. In vivo effects of the antiglucocorticoid RU 486 on glucocorticoid and cytokine responses to Escherichia coli endotoxin. Infect. Immun. 60:2641-2647.
21. Faggioni R, Fantuzzi G, Villa P, Buurman W, van Tits LJ, Ghezzi P. 1995. Independent down-regulation of central and peripheral tumor necrosis factor production as a result of lipopolysaccharide tolerance in mice. Infect. Immun. 63:1473-1477.
22. McGaha TL, Phelps RG, Spiera H, Bona C. 2002. Halofuginone, an inhibitor of type-I collagen synthesis and skin sclerosis, blocks transforming-growth-factor-beta-mediated Smad3 activation in fibroblasts. J. Investig. Dermatol. 118:461-470. http://dx.doi.org/10.1046/j.0022-202x.2001.01690.x.
23. Feldman S, Richardson J, Freeman C, Pollock S, Berger J, Kaplan F, Rhoa G. 1974. In vitro assessment of in vivo absorption of drug complexes. J. Pharm. Sci. 63:454-456. http://dx.doi.org/10.1002/jps.2600630334.
24. Palmiter RD. 1974. Magnesium precipitation of ribonucleoprotein complexes. Expedient techniques for the isolation of undergraded polysomes and messenger ribonucleic acid. Biochemistry 13:3606-3615.
25. Oyadomari S, Mori M. 2004. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11:381-389. http://dx.doi.org/10.1038/sj.cdd.4401373.
26. Clavarino G, Claudio N, Dalet A, Terawaki S, Couderc T, Chasson L, Ceppi M, Schmidt EK, Wenger T, Lecuit M, Gatti E, Pierre P. 2012. Protein phosphatase 1 subunit Ppp1r15a/GADD34 regulates cytokine production in polyinosinic:polycytidylic acid-stimulated dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 109:3006-3011. http://dx.doi.org/10.1073/pnas.1104491109.
27. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619-633. http://dx.doi.org/10.1016/S1097-2765(03)00105-9.
28. Kilberg MS, Shan J, Su N. 2009. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol. Metab. 20:436- 443. http://dx.doi.org/10.1016/j.tem.2009.05.008.
29. Zhang Y, Broser M, Rom WN. 1994. Activation of the interleukin 6 gene by Mycobacterium tuberculosis or lipopolysaccharide is mediated by nuclear factors NF-IL6 and NF-kappa B. Proc. Natl. Acad. Sci. U. S. A. 91: 2225-2229. http://dx.doi.org/10.1073/pnas.91.6.2225.
30. Neumann M, Wohlleben G, Chuvpilo S, Kistler B, Wirth T, Serfling E, Schimpl A. 1996. CD40, but not lipopolysaccharide and anti-IgM stimulation of primary B lymphocytes, leads to a persistent nuclear accumulation of RelB. J. Immunol. 157:4862-4869.
31. Ohmori Y, Tebo J, Nedospasov S, Hamilton TA. 1994. Kappa B binding activity in a murine macrophage-like cell line. Sequence-specific differences in kappa B binding and transcriptional activation functions. J. Biol. Chem. 269:17684-17690.
32. Xie QW, Kashiwabara Y, Nathan C. 1994. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269: 4705-4708.
33. Endo M, Mori M, Akira S, Gotoh T. 2006. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J. Immunol. 176:6245-6253.
34. Gao H, Schwartz RC. 2009. C/EBPzeta (CHOP/Gadd153) is a negative regulator of LPS-induced IL-6 expression in B cells. Mol. Immunol. 47: 390-397. http://dx.doi.org/10.1016/j.molimm.2009.09.002.
35. Hattori T, Ohoka N, Hayashi H, Onozaki K. 2003. C/EBP homologous protein (CHOP) up-regulates IL-6 transcription by trapping negative regulating NF-IL6 isoform. FEBS Lett. 541:33-39. http://dx.doi.org/10.1016/S0014-5793(03)00283-7.
36. Natsuka S, Akira S, Nishio Y, Hashimoto S, Sugita T, Isshiki H, Kishimoto T. 1992. Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79:460-466.
37. Sharma MD, Hou DY, Liu Y, Koni PA, Metz R, Chandler P, Mellor AL, He Y, Munn DH. 2009. Indoleamine 2,3-dioxygenase controls conversion of Foxp3_Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 113:6102-6111. http://dx.doi.org/10.1182/blood-2008-12-195354.
38. Chiribau CB, Gaccioli F, Huang CC, Yuan CL, Hatzoglou M. 2010. Molecular symbiosis ofCHOPand C/EBP beta isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis. Mol. Cell. Biol. 30: 3722-3731. http://dx.doi.org/10.1128/MCB.01507-09.
39. Yim HS, Choi KM, Kim B, Jung ID, Park YM, Kang YK, Lee MG. 2013. Effect of 1-methyl-D-tryptophan and the adoptive transfer of dendritic cells on polymicrobial sepsis induced by cecal content injection. Microbiol. Immunol. 57:633-639. http://dx.doi.org/10.1111/1348-0421.12081.
40. Reilly JG, McTavish SF, Young AH. 1997. Rapid depletion of plasma tryptophan: a review of studies and experimental methodology. J. Psychopharmacol. 11:381-392. http://dx.doi.org/10.1177/026988119701100416.
41. Richard DM, Dawes MA, Mathias CW, Acheson A, Hill-Kapturczak N, Dougherty DM. 2009. L-tryptophan: basic metabolic functions, behavioral research and therapeutic indications. Int. J. Tryptophan Res. 2:45-60.
42. Wek SA, Zhu S, Wek RC. 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2 alpha protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15:4497-4506.
43. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34:7-11. http://dx.doi.org/10.1042/BST0340007.
44. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, Wek RC. 2003. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol. Cell. Biol. 23:5651-5663. http://dx.doi.org/10.1128/MCB.23.16.5651-5663.2003.
45. Jiang HY, Wek RC. 2005. GCN2 phosphorylation of eIF2alpha activates NF-kappaB in response to UV irradiation. Biochem. J. 385:371-380. http://dx.doi.org/10.1042/BJ20041164.