The immune response to RNA suppresses nucleic acid synthesis by limiting ribose 5-phosphate.
Antiviral
Immunity
Metabolism
Nucleotide Biosynthesis
PKR (Protein Kinase RNA-Activated)
PPP (Pentose Phosphate Pathway)
RPIA (Ribose 5-Phosphate Isomerase A)
Journal
The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664
Informations de publication
Date de publication:
22 May 2024
22 May 2024
Historique:
received:
06
09
2023
accepted:
19
03
2024
revised:
29
02
2024
medline:
23
5
2024
pubmed:
23
5
2024
entrez:
22
5
2024
Statut:
aheadofprint
Résumé
During infection viruses hijack host cell metabolism to promote their replication. Here, analysis of metabolite alterations in macrophages exposed to poly I:C recognises that the antiviral effector Protein Kinase RNA-activated (PKR) suppresses glucose breakdown within the pentose phosphate pathway (PPP). This pathway runs parallel to central glycolysis and is critical to producing NADPH and pentose precursors for nucleotides. Changes in metabolite levels between wild-type and PKR-ablated macrophages show that PKR controls the generation of ribose 5-phosphate, in a manner distinct from its established function in gene expression but dependent on its kinase activity. PKR phosphorylates and inhibits the Ribose 5-Phosphate Isomerase A (RPIA), thereby preventing interconversion of ribulose- to ribose 5-phosphate. This activity preserves redox control but decreases production of ribose 5-phosphate for nucleotide biosynthesis. Accordingly, the PKR-mediated immune response to RNA suppresses nucleic acid production. In line, pharmacological targeting of the PPP during infection decreases the replication of the Herpes simplex virus. These results identify an immune response-mediated control of host cell metabolism and suggest targeting the RPIA as a potential innovative antiviral treatment.
Identifiants
pubmed: 38778156
doi: 10.1038/s44318-024-00100-w
pii: 10.1038/s44318-024-00100-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NHMRC
ID : 1143839
Organisme : NHMRC
ID : 1043398
Organisme : Perpetual Tructees
ID : CF07/2408
Organisme : Endeavour Fund
ID : UOOX1904
Informations de copyright
© 2024. The Author(s).
Références
Abrantes JL, Alves CM, Costa J, Almeida FC, Sola-Penna M, Fontes CF, Souza TM (2012) Herpes simplex type 1 activates glycolysis through engagement of the enzyme 6-phosphofructo-1-kinase (PFK-1). Biochim Biophys Acta 1822:1198–1206
pubmed: 22542512
doi: 10.1016/j.bbadis.2012.04.011
Aicardi J, Goutieres F (1984) A progressive familial encephalopathy in infancy with calcifications of the basal ganglia and chronic cerebrospinal fluid lymphocytosis. Ann Neurol 15:49–54
pubmed: 6712192
doi: 10.1002/ana.410150109
Bae S, Kim SY, Do MH, Lee CH, Song YJ (2017) 1,2,3,4,6-penta-O-galloyl-ss-D-glucose, a bioactive compound in Elaeocarpus sylvestris extract, inhibits varicella-zoster virus replication. Antiviral Res 144:266–272
pubmed: 28668556
doi: 10.1016/j.antiviral.2017.06.018
Ben-Sahra I, Hoxhaj G, Ricoult SJH, Asara JM, Manning BD (2016) mTORC1 induces purine synthesis through control of the mitochondrial tetrahydrofolate cycle. Science 351:728–733
pubmed: 26912861
pmcid: 4786372
doi: 10.1126/science.aad0489
Berlanga JJ, Herrero S, de Haro C (1998) Characterization of the hemin-sensitive eukaryotic initiation factor 2alpha kinase from mouse nonerythroid cells. J Biol Chem 273:32340–32346
pubmed: 9822714
doi: 10.1074/jbc.273.48.32340
Bogorad AM, Lin KY, Marintchev A (2017) Novel mechanisms of eIF2B action and regulation by eIF2alpha phosphorylation. Nucleic Acids Res 45:11962–11979
pubmed: 29036434
pmcid: 5714165
doi: 10.1093/nar/gkx845
Bojkova D, Costa R, Reus P, Bechtel M, Jaboreck MC, Olmer R, Martin U, Ciesek S, Michaelis M, Cinatl Jr J (2021) Targeting the pentose phosphate pathway for SARS-CoV-2 therapy. Metabolites 11:699
pubmed: 34677415
pmcid: 8540749
doi: 10.3390/metabo11100699
Boyle L, Wamelink MMC, Salomons GS, Roos B, Pop A, Dauber A, Hwa V, Andrew M, Douglas J, Feingold M et al. (2016) Mutations in TKT are the cause of a syndrome including short stature, developmental delay, and congenital heart defects. Am J Hum Genet 98:1235–1242
pubmed: 27259054
pmcid: 4908149
doi: 10.1016/j.ajhg.2016.03.030
Brooks SS, Anderson S, Bhise V, Botti C (2018) Further delineation of ribose-5-phosphate isomerase deficiency: report of a third case. J Child Neurol 33:784–787
pubmed: 30088433
doi: 10.1177/0883073818789316
Burgos E, Salmon L (2004) Synthesis and evaluation of new 4-phospho-d-erythronic acid derivatives as competitive inhibitors of spinach ribose-5-phosphate isomerase. Tetrahedron Lett 45:753–756
doi: 10.1016/j.tetlet.2003.11.038
Capriles PV, Baptista LP, Guedes IA, Guimaraes AC, Custodio FL, Alves-Ferreira M, Dardenne LE (2015) Structural modeling and docking studies of ribose 5-phosphate isomerase from Leishmania major and Homo sapiens: a comparative analysis for Leishmaniasis treatment. J Mol Graph Model 55:134–147
pubmed: 25528729
doi: 10.1016/j.jmgm.2014.11.002
Chakrabarti A, Sadler AJ, Kar N, Young HA, Silverman RH, Williams BRG (2008) Protein kinase R-dependent regulation of interleukin-10 in response to double-stranded RNA. J Biol Chem 283:25132–25139
pubmed: 18625702
pmcid: 2533086
doi: 10.1074/jbc.M804770200
Chen IT, Aoki T, Huang YT, Hirono I, Chen TC, Huang JY, Chang GD, Lo CF, Wang HC (2011) White spot syndrome virus induces metabolic changes resembling the warburg effect in shrimp hemocytes in the early stage of infection. J Virol 85:12919–12928
pubmed: 21976644
pmcid: 3233138
doi: 10.1128/JVI.05385-11
Chen JJ, Throop MS, Gehrke L, Kuo I, Pal JK, Brodsky M, London IM (1991) Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2 alpha (eIF-2 alpha) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2 alpha kinase. Proc Natl Acad Sci USA 88:7729–7733
pubmed: 1679235
pmcid: 52376
doi: 10.1073/pnas.88.17.7729
Cho MH, Wrabl JO, Taylor J, Hilser VJ (2020) Hidden dynamic signatures drive substrate selectivity in the disordered phosphoproteome. Proc Natl Acad Sci USA 117:23606–23616
pubmed: 32900925
pmcid: 7519349
doi: 10.1073/pnas.1921473117
Ciou SC, Chou YT, Liu YL, Nieh YC, Lu JW, Huang SF, Chou YT, Cheng LH, Lo JF, Chen MJ et al. (2015) Ribose-5-phosphate isomerase A regulates hepatocarcinogenesis via PP2A and ERK signaling. Int J Cancer 137:104–115
pubmed: 25429733
doi: 10.1002/ijc.29361
Clark PM, Flores G, Evdokimov NM, McCracken MN, Chai T, Nair-Gill E, O’Mahony F, Beaven SW, Faull KF, Phelps ME et al (2014) Positron emission tomography probe demonstrates a striking concentration of ribose salvage in the liver. Proc Natl Acad Sci USA 111:E2866–2874
pubmed: 24982199
pmcid: 4104878
doi: 10.1073/pnas.1410326111
Cooper VS, Schneider D, Blot M, Lenski RE (2001) Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183:2834–2841
pubmed: 11292803
pmcid: 99500
doi: 10.1128/JB.183.9.2834-2841.2001
Cortese I, Reich DS, Nath A (2021) Progressive multifocal leukoencephalopathy and the spectrum of JC virus-related disease. Nat Rev Neurol 17:37–51
pubmed: 33219338
doi: 10.1038/s41582-020-00427-y
Covarrubias AJ, Aksoylar HI, Yu J, Snyder NW, Worth AJ, Iyer SS, Wang J, Ben-Sahra I, Byles V, Polynne-Stapornkul T et al. (2016) Akt-mTORC1 signaling regulates Acly to integrate metabolic input to control of macrophage activation. Elife 5:e11612
pubmed: 26894960
pmcid: 4769166
doi: 10.7554/eLife.11612
Coy JF, Dressler D, Wilde J, Schubert P (2005) Mutations in the transketolase-like gene TKTL1: clinical implications for neurodegenerative diseases, diabetes and cancer. Clin Lab 51:257–273
pubmed: 15991799
Creek DJ, Jankevics A, Burgess KE, Breitling R, Barrett MP (2012) IDEOM: an Excel interface for analysis of LC-MS-based metabolomics data. Bioinformatics 28:1048–1049
pubmed: 22308147
doi: 10.1093/bioinformatics/bts069
Dar AC, Dever TE, Sicheri F (2005) Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 122:887–900
pubmed: 16179258
doi: 10.1016/j.cell.2005.06.044
Dardonville C, Rinaldi E, Barrett MP, Brun R, Gilbert IH, Hanau S (2004) Selective inhibition of Trypanosoma brucei 6-phosphogluconate dehydrogenase by high-energy intermediate and transition-state analogues. J Med Chem 47:3427–3437
pubmed: 15189039
doi: 10.1021/jm031066i
De Nardo D, Kalvakolanu DV, Latz E (2018) Immortalization of murine bone marrow-derived macrophages. Methods Mol Biol 1784:35–49
pubmed: 29761386
doi: 10.1007/978-1-4939-7837-3_4
Delgado T, Sanchez EL, Camarda R, Lagunoff M (2012) Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLoS Pathog 8:e1002866
pubmed: 22916018
pmcid: 3420960
doi: 10.1371/journal.ppat.1002866
De-Souza EA, Camara H, Salgueiro WG, Moro RP, Knittel TL, Tonon G, Pinto S, Pinca APF, Antebi A, Pasquinelli AE et al. (2019) RNA interference may result in unexpected phenotypes in Caenorhabditis elegans. Nucleic Acids Res 47:3957–3969
pubmed: 30838421
pmcid: 6486631
doi: 10.1093/nar/gkz154
Dey M, Cao C, Dar AC, Tamura T, Ozato K, Sicheri F, Dever TE (2005) Mechanistic link between PKR dimerization, autophosphorylation, and eIF2alpha substrate recognition. Cell 122:901–913
pubmed: 16179259
doi: 10.1016/j.cell.2005.06.041
Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, Triantafellow E, Ma Q, Gorski R, Cleaver S et al. (2010) Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 39:171–183
pubmed: 20670887
pmcid: 2946786
doi: 10.1016/j.molcel.2010.06.022
Ecker J, Liebisch G, Englmaier M, Grandl M, Robenek H, Schmitz G (2010) Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocytes. Proc Natl Acad Sci USA 107:7817–7822
pubmed: 20385828
pmcid: 2867858
doi: 10.1073/pnas.0912059107
Elliott G, O’Hare P (1999) Live-cell analysis of a green fluorescent protein-tagged herpes simplex virus infection. J Virol 73:4110–4119
pubmed: 10196307
pmcid: 104190
doi: 10.1128/JVI.73.5.4110-4119.1999
Essenberg MK, Cooper RA (1975) Two ribose-5-phosphate isomerases from Escherichia coli K12: partial characterisation of the enzymes and consideration of their possible physiological roles. Eur J Biochem 55:323–332
pubmed: 1104357
doi: 10.1111/j.1432-1033.1975.tb02166.x
Fagerberg L, Hallstrom BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K et al (2014) Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics 13:397–406
pubmed: 24309898
doi: 10.1074/mcp.M113.035600
Graille M, Meyer P, Leulliot N, Sorel I, Janin J, Van Tilbeurgh H, Quevillon-Cheruel S (2005) Crystal structure of the S. cerevisiae D-ribose-5-phosphate isomerase: comparison with the archaeal and bacterial enzymes. Biochimie 87:763–769
pubmed: 16054529
doi: 10.1016/j.biochi.2005.03.001
Grucela PK, Fuhrer T, Sauer U, Chao Y, Zhang YE (2023) Ribose 5-phosphate: the key metabolite bridging the metabolisms of nucleotides and amino acids during stringent response in Escherichia coli? Microb Cell 10:141–144
pubmed: 37395996
pmcid: 10311079
doi: 10.15698/mic2023.07.799
Guo X, Wu S, Li N, Lin Q, Liu L, Liang H, Niu Y, Huang Z, Fu X (2019) Accelerated metabolite levels of aerobic glycolysis and the pentose phosphate pathway are required for efficient replication of infectious spleen and kidney necrosis virus in Chinese perch brain cells. Biomolecules 9:440
pubmed: 31480692
pmcid: 6770389
doi: 10.3390/biom9090440
Hansen AM, Chaerkady R, Sharma J, Diaz-Mejia JJ, Tyagi N, Renuse S, Jacob HK, Pinto SM, Sahasrabuddhe NA, Kim MS et al. (2013) The Escherichia coli phosphotyrosine proteome relates to core pathways and virulence. PLoS Pathog 9:e1003403
pubmed: 23785281
pmcid: 3681748
doi: 10.1371/journal.ppat.1003403
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
pubmed: 11106749
doi: 10.1016/S1097-2765(00)00108-8
He B, Gross M, Roizman B (1997) The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 94:843–848
pubmed: 9023344
pmcid: 19601
doi: 10.1073/pnas.94.3.843
Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V, Skrzypek E (2015) PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res 43:D512–520
pubmed: 25514926
doi: 10.1093/nar/gku1267
Hovanessian AG, Riviere Y, Krust B (1983) Assay of interferon-mediated protein kinase activity from plasma and tissue extracts. Anal Biochem 129:349–356
pubmed: 6189422
doi: 10.1016/0003-2697(83)90561-4
Hu CD, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9:789–798
pubmed: 11983170
doi: 10.1016/S1097-2765(02)00496-3
Huck JH, Verhoeven NM, Struys EA, Salomons GS, Jakobs C, van der Knaap MS (2004) Ribose-5-phosphate isomerase deficiency: new inborn error in the pentose phosphate pathway associated with a slowly progressive leukoencephalopathy. Am J Hum Genet 74:745–751
pubmed: 14988808
pmcid: 1181951
doi: 10.1086/383204
Ishikawa K, Matsui I, Payan F, Cambillau C, Ishida H, Kawarabayasi Y, Kikuchi H, Roussel A (2002) A hyperthermostable D-ribose-5-phosphate isomerase from Pyrococcus horikoshii characterization and three-dimensional structure. Structure 10:877–886
pubmed: 12057201
doi: 10.1016/S0969-2126(02)00779-7
Ito D, Kawamura H, Oikawa A, Ihara Y, Shibata T, Nakamura N, Asano T, Kawabata SI, Suzuki T, Masuda S (2020) ppGpp functions as an alarmone in metazoa. Commun Biol 3:671
pubmed: 33188280
pmcid: 7666150
doi: 10.1038/s42003-020-01368-4
Kern ER, Glasgow LA, Klein RJ, Friedman-Kien AE (1982) Failure of 2-deoxy-D-glucose in the treatment of experimental cutaneous and genital infections due to herpes simplex virus. J Infect Dis 146:159–166
pubmed: 6286785
doi: 10.1093/infdis/146.2.159
Kettwig M, Ternka K, Wendland K, Kruger DM, Zampar S, Schob C, Franz J, Aich A, Winkler A, Sakib MS et al. (2021) Interferon-driven brain phenotype in a mouse model of RNaseT2 deficient leukoencephalopathy. Nat Commun 12:6530
pubmed: 34764281
pmcid: 8586222
doi: 10.1038/s41467-021-26880-x
Kilbourne ED (1959) Inhibition of influenza virus multiplication with a glucose antimetabolite (2-deoxy-D-glucose). Nature 183:271–272
pubmed: 13622777
doi: 10.1038/183271b0
Kleinschmidt-DeMasters BK, Tyler KL (2005) Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N Engl J Med 353:369–374
pubmed: 15947079
doi: 10.1056/NEJMoa051782
Knowles FC, Pon MK, Pon NG (1969) Direct spectrophotometric measurement of the ribosephosphate isomerase catalyzed reaction. Anal Biochem 29:40–47
pubmed: 5781913
doi: 10.1016/0003-2697(69)90005-0
Kuehne A, Emmert H, Soehle J, Winnefeld M, Fischer F, Wenck H, Gallinat S, Terstegen L, Lucius R, Hildebrand J et al (2015) Acute activation of oxidative pentose phosphate pathway as first-line response to oxidative stress in human skin cells. Mol Cell 59:359–371
pubmed: 26190262
doi: 10.1016/j.molcel.2015.06.017
Landini MP (1984) Early enhanced glucose uptake in human cytomegalovirus-infected cells. J Gen Virol 65(Pt 7):1229–1232
pubmed: 6086816
doi: 10.1099/0022-1317-65-7-1229
Leduc CA, Crouch EE, Wilson A, Lefkowitch J, Wamelink MM, Jakobs C, Salomons GS, Sun X, Shen Y, Chung WK (2014) Novel association of early onset hepatocellular carcinoma with transaldolase deficiency. JIMD Rep 12:121–127
pubmed: 24097415
doi: 10.1007/8904_2013_254
Lee KY, Moon CH, Choi SH (2018) Type I interferon and proinflammatory cytokine levels in cerebrospinal fluid of newborns with rotavirus-associated leukoencephalopathy. Brain Dev 40:211–217
pubmed: 29150375
doi: 10.1016/j.braindev.2017.10.006
Lehmann HC, Kruger K, Fink GR, Schroeter M (2015) Progressive multifocal leukoencephalopathy after interferon beta-1a monotherapy. J Neurol 262:771–773
pubmed: 25578178
doi: 10.1007/s00415-014-7620-4
Leib DA, Machalek MA, Williams BR, Silverman RH, Virgin HW (2000) Specific phenotypic restoration of an attenuated virus by knockout of a host resistance gene. Proc Natl Acad Sci USA 97:6097–6101
pubmed: 10801979
pmcid: 18564
doi: 10.1073/pnas.100415697
Li Y, Yao CF, Xu FJ, Qu YY, Li JT, Lin Y, Cao ZL, Lin PC, Xu W, Zhao SM et al. (2019) APC/C(CDH1) synchronizes ribose-5-phosphate levels and DNA synthesis to cell cycle progression. Nat Commun 10:2502
pubmed: 31175280
pmcid: 6555833
doi: 10.1038/s41467-019-10375-x
Lin CC, Ding CC, Sun T, Wu J, Chen KY, Zhou P, Chi JT (2021) The regulation of ferroptosis by MESH1 through the activation of the integrative stress response. Cell Death Dis 12:727
pubmed: 34294679
pmcid: 8298397
doi: 10.1038/s41419-021-04018-7
Lin MH, Sugiyama N, Ishihama Y (2015) Systematic profiling of the bacterial phosphoproteome reveals bacterium-specific features of phosphorylation. Sci Signal 8:rs10
pubmed: 26373674
doi: 10.1126/scisignal.aaa3117
Liu B, Fang M, He Z, Cui D, Jia S, Lin X, Xu X, Zhou T, Liu W (2015) Hepatitis B virus stimulates G6PD expression through HBx-mediated Nrf2 activation. Cell Death Dis 6:e1980
pubmed: 26583321
pmcid: 4670929
doi: 10.1038/cddis.2015.322
Liu J, Yu M, Chatnaparat T, Lee JH, Tian Y, Hu B, Zhao Y (2020) Comparative transcriptomic analysis of global gene expression mediated by (p) ppGpp reveals common regulatory networks in Pseudomonas syringae. BMC Genomics 21:296
pubmed: 32272893
pmcid: 7146990
doi: 10.1186/s12864-020-6701-2
Liu MS, Wang D, Morimoto H, Yim HC, Irving AT, Williams BR, Sadler AJ (2014) Molecular dynamics reveal a novel kinase-substrate interface that regulates protein translation. J Mol Cell Biol 6:473–485
pubmed: 25404612
doi: 10.1093/jmcb/mju044
Matsui T, Tanihara K, Date T (2001) Expression of unphosphorylated form of human double-stranded RNA-activated protein kinase in Escherichia coli. Biochem Biophys Res Commun 284:798–807
pubmed: 11396973
doi: 10.1006/bbrc.2001.5039
Mayo CB, Erlandsen H, Mouser DJ, Feinstein AG, Robinson VL, May ER, Cole JL (2019) Structural basis of protein kinase R autophosphorylation. Biochemistry 58:2967–2977
pubmed: 31246429
doi: 10.1021/acs.biochem.9b00161
McCormack SJ, Thomis DC, Samuel CE (1992) Mechanism of interferon action: identification of a RNA binding domain within the N-terminal region of the human RNA-dependent P1/eIF-2 alpha protein kinase. Virology 188:47–56
pubmed: 1373554
doi: 10.1016/0042-6822(92)90733-6
Metz DH, Esteban M (1972) Interferon inhibits viral protein synthesis in L cells infected with vaccinia virus. Nature 238:385–388
pubmed: 4559581
doi: 10.1038/238385a0
Metzler C, Lamprecht P, Hellmich B, Reuter M, Arlt AC, Gross WL (2005) Leucoencephalopathy after treatment of Churg-Strauss syndrome with interferon {alpha}. Ann Rheum Dis 64:1242–1243
pubmed: 16014692
pmcid: 1755617
doi: 10.1136/ard.2004.032664
Miosga T, Zimmermann FK (1996) Cloning and characterization of the first two genes of the non-oxidative part of the Saccharomyces cerevisiae pentose-phosphate pathway. Curr Genet 30:404–409
pubmed: 8929392
doi: 10.1007/s002940050149
Muaddi H, Majumder M, Peidis P, Papadakis AI, Holcik M, Scheuner D, Kaufman RJ, Hatzoglou M, Koromilas AE (2010) Phosphorylation of eIF2alpha at serine 51 is an important determinant of cell survival and adaptation to glucose deficiency. Mol Biol Cell 21:3220–3231
pubmed: 20660158
pmcid: 2938387
doi: 10.1091/mbc.e10-01-0023
Nejepinska J, Malik R, Wagner S, Svoboda P (2014) Reporters transiently transfected into mammalian cells are highly sensitive to translational repression induced by dsRNA expression. PLoS ONE 9:e87517
pubmed: 24475301
pmcid: 3903663
doi: 10.1371/journal.pone.0087517
Newsholme P, Curi R, Gordon S, Newsholme EA (1986) Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem J 239:121–125
pubmed: 3800971
pmcid: 1147248
doi: 10.1042/bj2390121
Park Y, Reyna-Neyra A, Philippe L, Thoreen CC (2017) mTORC1 balances cellular amino acid supply with demand for protein synthesis through post-transcriptional control of ATF4. Cell Rep 19:1083–1090
pubmed: 28494858
pmcid: 5811220
doi: 10.1016/j.celrep.2017.04.042
Perez-Riverol Y, Bai J, Bandla C, Garcia-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M et al. (2022) The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res 50:D543–D552
pubmed: 34723319
doi: 10.1093/nar/gkab1038
Peterson J, Phillips GJ (2008) New pSC101-derivative cloning vectors with elevated copy numbers. Plasmid 59:193–201
pubmed: 18295880
pmcid: 2435062
doi: 10.1016/j.plasmid.2008.01.004
Pluskal T, Castillo S, Villar-Briones A, Oresic M (2010) MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11:395
pubmed: 20650010
pmcid: 2918584
doi: 10.1186/1471-2105-11-395
Poppers J, Mulvey M, Khoo D, Mohr I (2000) Inhibition of PKR activation by the proline-rich RNA binding domain of the herpes simplex virus type 1 Us11 protein. J Virol 74:11215–11221
pubmed: 11070019
pmcid: 113216
doi: 10.1128/JVI.74.23.11215-11221.2000
Ralser M, Wamelink MM, Kowald A, Gerisch B, Heeren G, Struys EA, Klipp E, Jakobs C, Breitenbach M, Lehrach H et al (2007) Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J Biol 6:10
pubmed: 18154684
pmcid: 2373902
doi: 10.1186/jbiol61
Rawlinson SM, Zhao T, Rozario AM, Rootes CL, McMillan PJ, Purcell AW, Woon A, Marsh GA, Lieu KG, Wang LF et al (2018) Viral regulation of host cell biology by hijacking of the nucleolar DNA-damage response. Nat Commun 9:3057
pubmed: 30076298
pmcid: 6076271
doi: 10.1038/s41467-018-05354-7
Rice GI, Forte GM, Szynkiewicz M, Chase DS, Aeby A, Abdel-Hamid MS, Ackroyd S, Allcock R, Bailey KM, Balottin U et al (2013) Assessment of interferon-related biomarkers in Aicardi-Goutieres syndrome associated with mutations in TREX1, RNASEH2A, RNASEH2B, RNASEH2C, SAMHD1, and ADAR: a case-control study. Lancet Neurol 12:1159–1169
pubmed: 24183309
pmcid: 4349523
doi: 10.1016/S1474-4422(13)70258-8
Ritchie DW, Kemp GJ (2000) Protein docking using spherical polar Fourier correlations. Proteins 39:178–194
pubmed: 10737939
doi: 10.1002/(SICI)1097-0134(20000501)39:2<178::AID-PROT8>3.0.CO;2-6
Roberts WK, Hovanessian A, Brown RE, Clemens MJ, Kerr IM (1976) Interferon-mediated protein kinase and low-molecular-weight inhibitor of protein synthesis. Nature 264:477–480
pubmed: 1004583
doi: 10.1038/264477a0
Roos AK, Burgos E, Ericsson DJ, Salmon L, Mowbray SL (2005) Competitive inhibitors of Mycobacterium tuberculosis ribose-5-phosphate isomerase B reveal new information about the reaction mechanism. J Biol Chem 280:6416–6422
pubmed: 15590681
doi: 10.1074/jbc.M412018200
Ross BS, Reddy PG, Zhang HR, Rachakonda S, Sofia MJ (2011) Synthesis of diastereomerically pure nucleotide phosphoramidates. J Org Chem 76:8311–8319
pubmed: 21916475
doi: 10.1021/jo201492m
Roussou I, Thireos G, Hauge BM (1988) Transcriptional-translational regulatory circuit in Saccharomyces cerevisiae which involves the GCN4 transcriptional activator and the GCN2 protein kinase. Mol Cell Biol 8:2132–2139
pubmed: 3290651
pmcid: 363394
Ruda GF, Alibu VP, Mitsos C, Bidet O, Kaiser M, Brun R, Barrett MP, Gilbert IH (2007) Synthesis and biological evaluation of phosphate prodrugs of 4-phospho-D-erythronohydroxamic acid, an inhibitor of 6-phosphogluconate dehydrogenase. ChemMedChem 2:1169–1180
pubmed: 17615587
pmcid: 2248282
doi: 10.1002/cmdc.200700040
Rutner AC (1970) Spinach 5-phosphoribose isomerase. Purification and properties of the enzyme. Biochemistry 9:178–184
pubmed: 4391500
doi: 10.1021/bi00803a023
Saka K, Tadenuma M, Nakade S, Tanaka N, Sugawara H, Nishikawa K, Ichiyoshi N, Kitagawa M, Mori H, Ogasawara N et al (2005) A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Res 12:63–68
pubmed: 16106753
doi: 10.1093/dnares/12.1.63
Selinger M, Tykalova H, Sterba J, Vechtova P, Vavruskova Z, Lieskovska J, Kohl A, Schnettler E, Grubhoffer L (2019) Tick-borne encephalitis virus inhibits rRNA synthesis and host protein production in human cells of neural origin. PLoS Negl Trop Dis 13:e0007745
pubmed: 31560682
pmcid: 6785130
doi: 10.1371/journal.pntd.0007745
Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L, Wek RC (1998) Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18:7499–7509
pubmed: 9819435
pmcid: 109330
doi: 10.1128/MCB.18.12.7499
Shi YX, Huang CJ, Yang ZG (2016) Impact of hepatitis B virus infection on hepatic metabolic signaling pathway. World J Gastroenterol 22:8161–8167
pubmed: 27688657
pmcid: 5037084
doi: 10.3748/wjg.v22.i36.8161
Studer G, Tauriello G, Bienert S, Biasini M, Johner N, Schwede T (2021) ProMod3-A versatile homology modelling toolbox. PLoS Comput Biol 17:e1008667
pubmed: 33507980
pmcid: 7872268
doi: 10.1371/journal.pcbi.1008667
Sun D, Lee G, Lee JH, Kim HY, Rhee HW, Park SY, Kim KJ, Kim Y, Kim BY, Hong JI et al (2010) A metazoan ortholog of SpoT hydrolyzes ppGpp and functions in starvation responses. Nat Struct Mol Biol 17:1188–1194
pubmed: 20818390
doi: 10.1038/nsmb.1906
Thaker SK, Chapa T, Garcia Jr G, Gong D, Schmid EW, Arumugaswami V, Sun R, Christofk HR (2019) Differential metabolic reprogramming by Zika virus promotes cell death in human versus mosquito cells. Cell Metab 29:1206–1216 e1204
pubmed: 30827860
pmcid: 6818653
doi: 10.1016/j.cmet.2019.01.024
Thomis DC, Doohan JP, Samuel CE (1992) Mechanism of interferon action: cDNA structure, expression, and regulation of the interferon-induced, RNA-dependent P1/eIF-2 alpha protein kinase from human cells. Virology 188:33–46
pubmed: 1373553
doi: 10.1016/0042-6822(92)90732-5
Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, Chisholm SW (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci USA 108:E757–764
pubmed: 21844365
pmcid: 3182688
doi: 10.1073/pnas.1102164108
Uppala JK, Ghosh C, Sathe L, Dey M (2018) Phosphorylation of translation initiation factor eIF2alpha at Ser51 depends on site- and context-specific information. FEBS Lett 592:3116–3125
pubmed: 30070006
pmcid: 6167009
doi: 10.1002/1873-3468.13214
van der Knaap MS, Wevers RA, Struys EA, Verhoeven NM, Pouwels PJ, Engelke UF, Feikema W, Valk J, Jakobs C (1999) Leukoencephalopathy associated with a disturbance in the metabolism of polyols. Ann Neurol 46:925–928
pubmed: 10589548
doi: 10.1002/1531-8249(199912)46:6<925::AID-ANA18>3.0.CO;2-J
Vastag L, Koyuncu E, Grady SL, Shenk TE, Rabinowitz JD (2011) Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog 7:e1002124
pubmed: 21779165
pmcid: 3136460
doi: 10.1371/journal.ppat.1002124
Verhoeven NM, Huck JH, Roos B, Struys EA, Salomons GS, Douwes AC, van der Knaap MS, Jakobs C (2001) Transaldolase deficiency: liver cirrhosis associated with a new inborn error in the pentose phosphate pathway. Am J Hum Genet 68:1086–1092
pubmed: 11283793
pmcid: 1226089
doi: 10.1086/320108
Wang A, Huen SC, Luan HH, Yu S, Zhang C, Gallezot JD, Booth CJ, Medzhitov R (2016a) Opposing effects of fasting metabolism on tissue tolerance in bacterial and viral inflammation. Cell 166:1512–1525 e1512
pubmed: 27610573
pmcid: 5555589
doi: 10.1016/j.cell.2016.07.026
Wang CT, Chen YC, Wang YY, Huang MH, Yen TL, Li H, Liang CJ, Sang TK, Ciou SC, Yuh CH et al (2012) Reduced neuronal expression of ribose-5-phosphate isomerase enhances tolerance to oxidative stress, extends lifespan, and attenuates polyglutamine toxicity in Drosophila. Aging Cell 11:93–103
pubmed: 22040003
doi: 10.1111/j.1474-9726.2011.00762.x
Wang JJ, Martin PR, Singleton CK (1997) Aspartate 155 of human transketolase is essential for thiamine diphosphate-magnesium binding, and cofactor binding is required for dimer formation. Biochim Biophys Acta 1341:165–172
pubmed: 9357955
doi: 10.1016/S0167-4838(97)00067-8
Wang RF, Kushner SR (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195–199
pubmed: 2055470
doi: 10.1016/0378-1119(91)90366-J
Wang Y, Wang W, Xu L, Zhou X, Shokrollahi E, Felczak K, van der Laan LJ, Pankiewicz KW, Sprengers D, Raat NJ et al (2016b) Cross talk between nucleotide synthesis pathways with cellular immunity in constraining hepatitis E virus replication. Antimicrob Agents Chemother 60:2834–2848
pubmed: 26926637
pmcid: 4862450
doi: 10.1128/AAC.02700-15
Witek A, Wieczorek M (2009) [Virological and molecular methods in enteroviruses infections in 2004-2008, Poland]. Przegl Epidemiol 63:379–382
Witowski N, Lusczek E, Determan Jr C, Lexcen D, Mulier K, Ostrowski B, Beilman G (2015) A four-compartment metabolomics analysis of the liver, muscle, serum, and urine response to polytrauma with hemorrhagic shock following carbohydrate prefeed. PLoS ONE 10:e0124467
pubmed: 25875111
pmcid: 4396978
doi: 10.1371/journal.pone.0124467
Wood T (1970) Spectrophotometric assay for D-ribose-5-phosphateketol-isomerase and for D-ribulose-5-phosphate 3-epimerase. Anal Biochem 33:297–306
pubmed: 5462169
doi: 10.1016/0003-2697(70)90300-3
Xie Q, Fan F, Wei W, Liu Y, Xu Z, Zhai L, Qi Y, Ye B, Zhang Y, Basu S et al (2017) Multi-omics analyses reveal metabolic alterations regulated by hepatitis B virus core protein in hepatocellular carcinoma cells. Sci Rep 7:41089
pubmed: 28112229
pmcid: 5253728
doi: 10.1038/srep41089
Xu Z, Wang D, Lee X, Williams BR (2004) Biochemical analyses of multiple fractions of PKR purified from Escherichia coli. J Interferon Cytokine Res 24:522–535
pubmed: 15450128
doi: 10.1089/jir.2004.24.522
Xu Z, Williams BR (2000) The B56alpha regulatory subunit of protein phosphatase 2A is a target for regulation by double-stranded RNA-dependent protein kinase PKR. Mol Cell Biol 20:5285–5299
pubmed: 10866685
pmcid: 85978
doi: 10.1128/MCB.20.14.5285-5299.2000
Yang YL, Reis LF, Pavlovic J, Aguzzi A, Schafer R, Kumar A, Williams BR, Aguet M, Weissmann C (1995) Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J 14:6095–6106
pubmed: 8557029
pmcid: 394734
doi: 10.1002/j.1460-2075.1995.tb00300.x
Yau C, Low JZH, Gan ES, Kwek SS, Cui L, Tan HC, Mok DZL, Chan CYY, Sessions OM, Watanabe S et al (2021) Dysregulated metabolism underpins Zika-virus-infection-associated impairment in fetal development. Cell Rep 37:110118
pubmed: 34910902
doi: 10.1016/j.celrep.2021.110118
Yep A, Sorenson RJ, Wilson MR, Showalter HD, Larsen SD, Keller PR, Woodard RW (2011) Enediol mimics as inhibitors of the D-arabinose 5-phosphate isomerase (KdsD) from Francisella tularensis. Bioorg Med Chem Lett 21:2679–2682
pubmed: 21236668
doi: 10.1016/j.bmcl.2010.12.066
Zamanian-Daryoush M, Der SD, Williams BR (1999) Cell cycle regulation of the double stranded RNA activated protein kinase, PKR. Oncogene 18:315–326
pubmed: 9927188
doi: 10.1038/sj.onc.1202293
Zhang R, Andersson CE, Savchenko A, Skarina T, Evdokimova E, Beasley S, Arrowsmith CH, Edwards AM, Joachimiak A, Mowbray SL (2003) Structure of Escherichia coli ribose-5-phosphate isomerase: a ubiquitous enzyme of the pentose phosphate pathway and the Calvin cycle. Structure 11:31–42
pubmed: 12517338
pmcid: 2792023
doi: 10.1016/S0969-2126(02)00933-4