An Invertebrate Warburg Effect: A Shrimp Virus Achieves Successful Replication by Altering the Host Metabolome via the PI3K-Akt-mTOR Pathway

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Su, Mei An ^a   Huang, Yun Tzu ^a   Chen, I Tung ^b   Lee, Der Yen ^b   Hsieh, Yun Chieh ^a   Li, Chun Yuan ^a   Ng, Tze Hann ^a   Liang, Suh Yuen ^c   Lin, Shu Yu ^c   Huang, Shiao Wei ^b   Chiang, Yi An ^a   Yu, Hon Tsen ^b   Khoo, Kay Hooi ^b,c   Chang, Geen Dong ^b   Lo, Chu Fang ^a,b   Wang, Han Ching ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 8 [4 (1 AMINOCYCLOBUTYL) PHENYL] 9 PHENYL 1, 2, 4 TRIAZOLO [3, 4 F] [1, 6] NAPHTHYRIDIN 3 (2H) ONE; BUPARLISIB; DIHYDROXYACETONE PHOSPHATE; DOUBLE STRANDED RNA; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE; INITIATION FACTOR 4E BINDING PROTEIN 1; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOENOLPYRUVATE; PROTEIN KINASE B; PYRUVIC ACID; RAPAMYCIN; RHEB PROTEIN; TORIN 1; UNCLASSIFIED DRUG; 1-(4-(4-PROPIONYLPIPERAZIN-1-YL)-3-(TRIFLUOROMETHYL)PHENYL)-9-(QUINOLIN-3-YL)BENZO(H)(1,6)NAPHTHYRIDIN-2(1H)-ONE; AMINO ACID; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MULTIPROTEIN COMPLEX; NAPHTHYRIDINE DERIVATIVE; PROTEOME; TARGET OF RAPAMYCIN KINASE; TOR COMPLEX 2;

AMINO ACID SYNTHESIS; AMINOLYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CITRIC ACID CYCLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; GENE EXPRESSION; GENE SILENCING; GLYCOLYSIS; HOST; LIQUID CHROMATOGRAPHY; METABOLOME; NONHUMAN; NUCLEOTIDE METABOLISM; PENTOSE PHOSPHATE CYCLE; PROTEIN PHOSPHORYLATION; PROTEOMICS; RNA INTERFERENCE; SHRIMP; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION; WARBURG EFFECT; WESTERN BLOTTING; WHITE SPOT SYNDROME VIRUS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; ENERGY METABOLISM; GENETICS; METABOLISM; PENAEIDAE; VIROLOGY;

AMINO ACIDS; ANIMALS; CITRIC ACID CYCLE; ENERGY METABOLISM; GLYCOLYSIS; METABOLOME; MONOMERIC GTP-BINDING PROTEINS; MULTIPROTEIN COMPLEXES; NAPHTHYRIDINES; PENAEIDAE; PENTOSE PHOSPHATE PATHWAY; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEOME; PROTO-ONCOGENE PROTEINS C-AKT; TOR SERINE-THREONINE KINASES; VIRUS REPLICATION; WHITE SPOT SYNDROME VIRUS 1;

EID: 84903479945     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004196     Document Type: Article

References (45)

1. Warburg O, (1956) On the origin of cancer cells. Science 123: 309-314.
2. Kim JW, Dang CV, (2006) Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 66: 8927-8930.
3. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
4. Zwerschke W, Mazurek S, Massimi P, Banks L, Eigenbrodt E, et al. (1999) Modulation of type M2 pyruvate kinase activity by the human papillomavirus type 16 E7 oncoprotein. Proc Natl Acad Sci U S A 96: 1291-1296.
5. Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD, (2006) Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog 2: 1165-1175.
6. Munger J, Bennett BD, Parikh A, Feng XJ, McArdle J, et al. (2008) Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat Biotechnol 26: 1179-1186.
7. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, et al. (2010) Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proc Natl Acad Sci U S A 107: 10696-10701.
8. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, et al. (2010) Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 6: e1000719.
9. Chen IT, Aoki T, Huang YT, Hirono I, Chen TC, et al. (2011) White spot syndrome virus induces metabolic changes resembling the warburg effect in shrimp hemocytes in the early stage of infection. J Virol 24: 12919-12928.
10. Chang PS, Lo CF, Wang YC, Kou GH, (1996) Identification of white spot syndrome associated baculovirus (WSBV) target organs in the shrimp Penaeus monodon by in situ hybridization. Dis Aquat Organ 27: 131-139.
11. Robey RB, Hay N, (2009) Is Akt the "Warburg kinase"?-Akt-energy metabolism interactions and oncogenesis. Semin Cancer Biol 19: 25-31.
12. Bhatt AP, Jacobs SR, Freemerman AJ, Makowski L, Rathmell JC, et al. (2012) Dysregulation of fatty acid synthesis and glycolysis in non-Hodgkin lymphoma. Proc Natl Acad Sci U S A 109: 11818-11823.
13. Noch E, Khalili K, (2012) Oncogenic viruses and tumor glucose metabolism: like kids in a candy store. Mol Cancer Ther 11: 14-23.
14. Mannová P, Beretta L, (2005) Activation of the N-Ras-PI3K-Akt-mTOR pathway by hepatitis C virus: control of cell survival and viral replication. J Virol 79: 8742-8749.
15. Guo H, Zhou T, Jiang D, Cuconati A, Xiao GH, et al. (2007) Regulation of hepatitis B virus replication by the phosphatidylinositol 3-kinase-akt signal transduction pathway. J Virol 81: 10072-10080.
16. Martin S, Saha B, Riley JL, (2012) The battle over mTOR: an emerging theatre in host-pathogen immunity. PLoS Pathog 8: e1002894.
17. Peng L, Liang D, Tong W, Li J, Yuan Z, (2013) Hepatitis C virus NS5A activates the mammalian target of rapamycin (mTOR) pathway, contributing to cell survival by disrupting the interaction between FK506-binding protein 38 (FKBP38) and mTOR. J Biol Chem 285: 20870-20881.
18. Hay N, Sonenberg N, (2004) Upstream and downstream of mTOR. Genes & Dev 18: 1926-1945.
19. Düvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, et al. (2010) Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 39: 171-183.
20. Birungi G, Chen SM, Loy BP, Ng ML, Li SF, (2010) Metabolomics approach for investigation of effects of dengue virus infection using the EA.hy926 cell line. J Proteome Res 9: 6523-6534.
21. Ritter JB, Wahl AS, Freund S, Genzel Y, Reichl U, (2010) Metabolic effects of influenza virus infection in cultured animal cells: Intra- and extracellular metabolite profiling. BMC Syst Biol 4: 61.
22. 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.
23. 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.
24. Kunkel M, Reichert TE, Benz P, Lehr HA, Jeong JH, et al. (2003) Overexpression of Glut-1 and increased glucose metabolism in tumors are associated with a poor prognosis in patients with oral squamous cell carcinoma. Cancer 97: 1015-1024.
25. Huang HT, Leu JH, Huang PY, Chen LL, (2012) A putative cell surface receptor for white spot syndrome virus is a member of a transporter superfamily. PLoS One 7: e33216.
26. Boros LG, Lee PW, Brandes JL, Cascante M, Muscarella P, et al. (1998) Nonoxidative pentose phosphate pathways and their direct role in ribose synthesis in tumors: is cancer a disease of cellular glucose metabolism? Med Hypotheses 50: 55-59.
27. Ramos-Montoya A, Lee WN, Bassilian S, Lim S, Trebukhina RV, et al. (2006) Pentose phosphate cycle oxidative and nonoxidative balance: A new vulnerable target for overcoming drug resistance in cancer. Int J Cancer 119: 2733-2741.
28. Nutter LM, Grill SP, Cheng YC, (1985) The sources of thymidine nucleotides for virus DNA synthesis in herpes simplex virus type 2-infected cells. J Biol Chem 260: 13272-13275.
29. Daikoku T, Yamamoto N, Maeno K, Nishiyama Y, (1991) Role of viral ribonucleotide reductase in the increase of dTTP pool size in herpes simplex virus-infected Vero cells. J Gen Virol 72: 1441-1444.
30. Gammon DB, Gowrishankar B, Duraffour S, Andrei G, Upton C, et al. (2010) Vaccinia virus-encoded ribonucleotide reductase subunits are differentially required for replication and pathogenesis. PLoS Pathog 6: e1000984.
31. Leu JH, Yang F, Zhang X, Xu X, Kou GH, et al. (2009) Whispovirus. Curr Top Microbiol Immunol 328: 197-227.
32. Mazurek S, Zwerschke W, Jansen-Dürr P, Eigenbrodt E, (2001) Effects of the human papilloma virus HPV-16 E7 oncoprotein on glycolysis and glutaminolysis: role of pyruvate kinase type M2 and the glycolytic-enzyme complex. Biochem J 2356: 247-256.
33. Ponisovskiy MR, (2010) Cancer metabolism and the Warburg effect as anabolic process outcomes of oncogene operation. Crit Rev Eukaryot Gene Expr 20: 325-339.
34. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, et al. (2007) Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci U S A 104: 19345-19350.
35. King A, Selak MA, Gottlieb E, (2006) Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25: 4675-4682.
36. Spangle JM, Münger K, (2010) The human papillomavirus type 16 E6 oncoprotein activates mTORC1 signaling and increases protein synthesis. J Virol 84: 9398-9407.
37. Yu Y, Alwine JC, (2002) Human cytomegalovirus major immediate-early proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylinositide 3′-OH kinase pathway and cellular kinase Akt. J Virol 76: 3731-3738.
38. Kudchodkar SB, Yu Y, Maguire TG, Alwine JC, (2004) Human cytomegalovirus infection induces rapamycin insensitive phosphorylation of downstream effectors of mTOR kinase. J Virol 78: 11030-11039.
39. Kudchodkar SB, Yu Y, Maguire TG, Alwine JC, (2006) Human cytomegalovirus infection alters the substrate specificities and rapamycin sensitivities of raptor- and rictor-containing complexes. Proc Natl Acad Sci U S A 103: 14182-14187.
40. Kudchodkar SB, Del Prete GQ, Maguire TG, Alwine JC, (2007) AMPK-mediated inhibition of mTOR kinase is circumvented during immediate-early times of human cytomegalovirus infection. J Virol 81: 3649-3651.
41. Buchkovich NJ, Yu Y, Zampieri CA, Alwine JC, (2008) The TORrid affairs of viruses: effects of mammalian DNA viruses on the PI3K-Akt-mTOR signaling pathway. Nat Rev Microbiol 6: 266-275.
42. Söderhäll I, Kim YA, Jiravanichpaisal P, Lee SY, Söderhäll K, (2005) An ancient role for a prokineticin domain in invertebrate hematopoiesis. J Immunol 174: 6153-6160.
43. Wang HC, Wang HC, Kou GH, Lo CF, Huang WP, (2007) Identification of icp11, the most highly expressed gene of shrimp white spot syndrome virus (WSSV). Dis Aquat Organ 74: 179-189.
44. Wang HC, Kondo H, Hirono I, Aoki T, (2010) The Marsupenaeus japonicus voltage-dependent anion channel (MjVDAC) protein is involved in white spot syndrome virus (WSSV) pathogenesis. Fish Shellfish Immunol 29: 94-103.
45. Maira SM, Pecchi S, Huang A, Burger M, Knapp M, et al. (2012) Identification and characterization of NVP-BKM120, an orally available pan-class I PI3-kinase inhibitor. Mol Cancer Ther 11: 317-328.