Modulation of α-enolase post-translational modifications by dengue virus: Increased secretion of the basic isoforms in infected hepatic cells

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Higa, Luiza M ^a   Curi, Bruno M ^a   Aguiar, Renato S ^a   Cardoso, Cynthia C ^a   De Lorenzi, André G ^b   Sena, Silvia L F ^b   Zingali, Russolina B ^a   Da Poian, Andrea T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b Departamento de Genética Instituto de Biologia Universidade Federal do Rio de Janeiro ^*  (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ENOLASE; CELL PROTEIN; ENOLASE; ISOENZYME;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DENGUE; DENGUE VIRUS; DISEASE SEVERITY; DOSE RESPONSE; ENZYME BLOOD LEVEL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LOCALIZATION; ENZYME RELEASE; GENE EXPRESSION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NONHUMAN; PROTEIN CONTENT; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; TWO DIMENSIONAL ELECTROPHORESIS; VIRUS LOAD; WESTERN BLOTTING; ENZYMOLOGY; LIVER CELL; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); VIROLOGY; VIRUS REPLICATION;

DENGUE VIRUS; HEP G2 CELLS; HEPATOCYTES; HUMANS; ISOENZYMES; PHOSPHOPYRUVATE HYDRATASE; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRUS REPLICATION;

EID: 84940331831     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088314     Document Type: Article

References (73)

1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, et al. (2013). The global distribution and burden of dengue. Nature 496 (7446): 504-507.
2. Guzman A, Istúriz RE. (2010). Update on the global spread of dengue. Int J Antimicrob Agents 36 Suppl 1:S40-42.
3. WHO (2011). Comprehensive guidelines for prevention and control of dengue and dengue haemorrhagic fever. Revised and expanded edition. New Delhi, India: World Health Organization, Regional Office for South-East Asia.
4. WHO (2009) Dengue guidelines for diagnosis, treatment, prevention and control. Third edition. Geneva: World Health Organization.
5. Huang YH, Liu CC, Wang ST, Lei HY, Liu HL, et al. (2001). Activation of coagulation and fibrinolysis during dengue virus infection. J Med Virol 63(3):247-251.
6. Carlos CC, Oishi K, Cinco MT, Mapua CA, Inoue S, et al. (2005). Comparison of clinical features and hematologic abnormalities between dengue fever and dengue hemorrhagic fever among children in the Philippines. Am J Trop Med Hyg73(2):435-40. (Pubitemid 41278725)
7. Sosothikul D, Seksarn P, Pongsewalak S, Thisyakorn U, Lusher J. (2007). Activation of endothelial cells, coagulation and fibrinolysis in children with Dengue virus infection. Thromb Haemost 97(4):627-634. (Pubitemid 46592941)
8. Orsi FA, Angerami RN, Mazetto BM, Quaino SK, Santiago-Bassora F, et al. (2013). Reduced thrombin formation and excessive fibrinolysis are associated with bleeding complications in patients with dengue fever: a case-control study comparing dengue fever patients with and without bleeding manifestations. BMC Infect Dis 13(1):350.
9. Krishnamurti C, Kalayanarooj S, Cutting MA, Peat RA, Rothwell SW, et al. (2001). Mechanisms of hemorrhage in dengue without circulatory collapse. Am J Trop Med Hyg 65(6):840-847. (Pubitemid 34049482)
10. Srichaikul T, Nimmanitaya S, Artchararit N, Siriasawakul T, Sungpeuk P. (1977). Fibrinogen metabolism and disseminated intravascular coagulation in dengue hemorrhagic fever. Am J Trop Med Hyg 26(3):525-32. (Pubitemid 8136750)
11. Funahara Y, Sumarmo, Shirahata A, Setiabudy-Dharma R. (1987). DHF characterized by acute type DIC with increased vascular permeability. Southeast Asian J Trop Med Public Health 18(3):346-350.
12. Isarangkura PB, Pongpanich B, Pintadit P, Phanichyakarn P, Valyasevi A. (1987). Hemostatic derangement in dengue haemorrhagic fever. Southeast Asian J Trop Med Public Health 18(3):331-9.
13. van Gorp EC, Minnema MC, Suharti C, Mairuhu AT, Brandjes DP, et al. (2001). Activation of coagulation factor XI, without detectable contact activation in dengue haemorrhagic fever. Br J Haematol 113(1):94-99.
14. Van Gorp EC, Setiati TE, Mairuhu AT, Suharti C, ten Cate H, et al. (2002). Impaired fibrinolysis in the pathogenesis of dengue hemorrhagic fever. J Med Virol 67(4):549-554. (Pubitemid 34747676)
15. Onlamoon N, Noisakran S, Hsiao HM, Duncan A, Villinger F, et al. (2010). Dengue virus-induced hemorrhage in a nonhuman primate model. Blood 115(9):1823-1834.
16. Assunção-Miranda I, Amaral FA, Bozza FA, Fagundes CT, Sousa LP, et al. (2010). Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection. FASEB J 24(1):218-228.
17. Luplertlop N, Missé D, Bray D, Deleuze V, Gonzalez JP, et al. (2006). Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep 7(11):1176-1181.
18. Higa LM, Caruso MB, Canellas F, Soares MR, Oliveira-Carvalho AL, et al. (2008). Secretome of HepG2 cells infected with dengue virus: implications for pathogenesis. Biochim Biophys Acta 1784(11):1607-1616.
19. Pancholi V. (2001). Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci 58(7):902-920.
20. Díaz-Ramos A, Roig-Borrellas A, García-Melero A, López-Alemany R. (2012). α-Enolase, a multifunctional protein: its role on pathophysiological situations. J Biomed Biotechnol 2012:156795.
21. Feo S, Arcuri D, Piddini E, Passantino R, Giallongo A. (2000). ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: relationship with Myc promoter-binding protein 1 (MBP-1). FEBS Lett 473(1):47-52. (Pubitemid 30235183)
22. Iida H, Yahara I. (1985). Yeast heat-shock protein of Mr 48,000 is an isoprotein of enolase. Nature 315(6021): 688-690. (Pubitemid 15232887)
23. Aaronson RM, Graven KK, Tucci M, McDonald RJ, Farber HW. (1995). Nonneuronal enolase is an endothelial hypoxic stress protein. J Biol Chem 270(46):27752-27757.
24. Miles LA, Dahlberg CM, Plescia J, Felez J, Kato K, et al. (1991) Role of cellsurface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry 30(6):1682-1691.
25. Redlitz A, Fowler BJ, Plow EF, Miles LA. (1995) The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem 227(1-2):407-415.
26. Capello M, Ferri-Borgogno S, Cappello P, Novelli F. (2011) α-Enolase: a promising therapeutic and diagnostic tumor target. FEBS J 278(7):1064-74.
27. Conceição TM, El-Bacha T, Villas-Bôas CS, Coello G, Ramírez J, et al. (2010). Gene expression analysis during dengue virus infection in HepG2 cells reveals virus control of innate immune response. J Infect 60(1):65-75.
28. Zhou W, Capello M, Fredolini C, Piemonti L, Liotta LA, et al. (2010). Mass spectrometry analysis of the post-translational modifications of alpha-enolase from pancreatic ductal adenocarcinoma cells. J Proteome Res 9(6):2929-2936.
29. Seneviratne SL, Malavige GN, de Silva HJ. (2006) Pathogenesis of liver involvement during dengue viral infections. Trans R Soc Trop Med Hyg 100(7):608-14.
30. Rosen L, Drouet MT, Deubel V. (1999). Detection of dengue virus RNA by reverse transcription-polymerase chain reaction in the liver and lymphoid organs but not in the brain in fatal human infection. Am J Trop Med Hyg 61(5):720-724.
31. Balsitis SJ, Coloma J, Castro G, Alava A, Flores D, et al. (2009). Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. Am J Trop Med Hyg 80(3):416-424.
32. Guabiraba R, Besnard AG, Marques RE, Maillet I, Fagundes CT, et al. (2013). IL-22 modulates IL-17A production and controls inflammation and tissue damage in experimental dengue infection. Eur J Immunol 43(6):1529-1544.
33. Lin YL, Liu CC, Lei HY, Yeh TM, Lin YS, et al. (2000). Infection of five human liver cell lines by dengue-2 virus. J Med Virol 60(4):425-431.
34. Thepparit C, Phoolcharoen W, Suksanpaisan L, Smith DR. (2004). Internalization and propagation of the dengue virus in human hepatoma (HepG2) cells 47(2):78-86.
35. Petrak J, Ivanek R, Toman O, Cmejla R, Cmejlova J, et al. (2008). Déjà vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 8(9):1744-1749 (Pubitemid 351678270)
36. Altenberg B, Greulich KO. (2004). Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics 84(6):1014-1020. (Pubitemid 39469126)
37. Takashima M, Kuramitsu Y, Yokoyama Y, Iizuka N, Fujimoto M, et al. (2005). Overexpression of alpha enolase in hepatitis C virus-related hepatocellular carcinoma: association with tumor progression as determined by proteomic analysis. Proteomics 5(6):1686-1692. (Pubitemid 40593274)
38. Tsai ST, Chien IH, Shen WH, Kuo YZ, Jin YT, et al. (2010). ENO1, a potential prognostic head and neck cancer marker, promotes transformation partly via chemokine CCL20 induction. Eur J Cancer 46(9):1712-23
39. Butterfield DA, Lange ML. (2009). Multifunctional roles of enolase in Alzheimer's disease brain: beyond altered glucose metabolism. J Neurochem 111(4):915-33.
40. Tchankouo-Nguetcheu S, Khun H, Pincet L, Roux P, Bahut M. (2010). Differential protein modulation in midguts of Aedes aegypti infected with chikungunya and dengue 2 viruses. PLoS One 5(10): e13149.
41. Patramool S, Surasombatpattana P, Luplertlop N, Sévéno M, Choumet V, et al. (2011). Proteomic analysis of an Aedes albopictus cell line infected with Dengue serotypes 1 and 3 viruses. Parasit Vectors 18; 4:138.
42. Colpitts TM, Cox J, Vanlandingham DL, Feitosa FM, Cheng G, et al. (2011). Alterations in the Aedes aegypti transcriptome during infection with West Nile, dengue and yellow fever viruses. PLoS Pathog 7(9):e1002189.
43. Le Breton M, Meyniel-Schicklin L, Deloire A, Coutard B, Canard B, et al. (2011). Flavivirus NS3 and NS5 proteins interaction network: a high-throughput yeast two-hybrid screen. BMC Microbiol 11:234.
44. Perconti G, Ferro A, Amato F, Rubino P, Randazzo D, et al. (2007). The kelch protein NS1-BP interacts with alpha-enolase/MBP-1 and is involved in c-Myc gene transcriptional control. Biochim Biophys Acta 1773(12):1774-1785. (Pubitemid 350191977)
45. Miura N, Kirino A, Endo S, Morisaka H, Kuroda K, et al. (2012). Tracing putative trafficking of the glycolytic enzyme enolase via SNARE-driven unconventional secretion. Eukaryot Cell.11(8):1075-1082.
46. Olver C, Vidal M. (2007). Proteomic analysis of secreted exosomes. Subcell Biochem 43:99-131.
47. Wygrecka M, Marsh LM, Morty RE, Henneke I, Guenther A, et al. (2009). Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung. Blood 113(22): 5588-5598.
48. Ciborowski P, Kadiu I, Rozek W, Smith L, Bernhardt K, et al. (2007). Investigating the human immunodeficiency virus type 1-infected monocyte-derived macrophage secretome. Virology 363(1):198-209. (Pubitemid 46678164)
49. Cappello P, Tomaino B, Chiarle R, Ceruti P, Novarino A, et al. (2009) An integrated humoral and cellular response is elicited in pancreatic cancer by alpha-enolase, a novel pancreatic ductal adenocarcinoma-associated antigen. Int J Cancer 1;125(3):639-48.
50. Moscato S, Pratesi F, Sabbatini A, Chimenti D, Scavuzzo M, et al. Surface expression of a glycolytic enzyme, alpha-enolase, recognized by autoantibodies in connective tissue disorders. Eur J Immunol 2000 Dec;30(12):3575-84. (Pubitemid 32005230)
51. Gitlits VM, Toh BH, Sentry JW. (2001). Disease association, origin, and clinical relevance of autoantibodies to the glycolytic enzyme enolase. J Investig Med 49(2):138-145. (Pubitemid 32187087)
52. Terrier B, Degand N, Guilpain P, Servettaz A, Guillevin L, et al. (2007). Alpha-enolase: a target of antibodies in infectious and autoimmune diseases. Autoimmun Rev 6(3):176-182. (Pubitemid 46201958)
53. Pontillo A, Di Toro N, Edomi P, Shadlow A, Ammadeo A, et al. (2011). Anti-α-enolase Antibodies in Serum from Pediatric Patients Affected by Inflammatory Diseases: Diagnostic and Pathogenetic Insights. Int J Rheumatol 2011: 870214.
54. Tomaino B, Cappello P, Capello M, Fredolini C, Sperduti I, et al. (2011). Circulating autoantibodies to phosphorylated á-enolase are a hallmark of pancreatic cancer 10(1):105-12.
55. Kinloch A, Tatzer V, Wait R, Peston D, Lundberg K, et al. (2005).Identification of citrullinated alpha-enolase as a candidate autoantigen in rheumatoid arthritis. Arthritis Res Ther 7(6):R1421-1429.
56. Yang HB, Zheng WJ, Zhang X, Tang FL. (2011) Induction of endothelial cell apoptosis by anti-alpha-enolase antibody. Chin Med Sci J 26(3):152-7.
57. Bae S, Kim H, Lee N, Won C, Kim HR, et al. (2012). α-Enolase expressed on the surfaces of monocytes and macrophages induces robust synovial inflammation in rheumatoid arthritis. J Immunol 189(1):365-72.
58. Kumar Y, Liang C, Bo Z, Rajapakse JC, Ooi EE, et al. (2012). Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLoS Negl Trop Dis 6(11):e1887.
59. Jang B, Jeon YC, Choi JK, Park M, Kim JI, et al. (2012). Peptidylarginine deiminase modulates the physiological roles of enolase via citrullination: links between altered multifunction of enolase and neurodegenerative diseases. Biochem J 445(2):183-92.
60. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, et al. (2007). Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131(6):1190-203. (Pubitemid 350235027)
61. Yu LR, Zhu Z, Chan KC, Issaq HJ, Dimitrov DS, et al. (2007). Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J Proteome Res 6(11):4150-4162. (Pubitemid 350158493)
62. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, et al. (2002). Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem 82(6):1524-32
63. Perluigi M, Poon HF, Maragos W, Pierce WM, Klein JB, et al. (2005). Proteomic analysis of protein expression and oxidative modification in r6/2 transgenic mice: a model of Huntington disease. Mol Cell Proteomics 4(12):1849-61. (Pubitemid 41830180)
64. Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, et al. (2003). Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem 85(6):1394-401. (Pubitemid 36702552)
65. Newman SF, Sultana R, Perluigi M, Coccia R, Cai J, et al. (2007). An increase in S-glutathionylated proteins in the Alzheimer's disease inferior parietal lobule, a proteomics approach. J Neurosci Res 85(7):1506-14. (Pubitemid 46724394)
66. Peng C, Lu Z, Xie Z, Cheng Z, Chen Y, et al. (2011). The first identification of lysine malonylation substrates and its regulatory enzyme. Mol Cell Proteomics 10(12):M111.012658, 1-12.
67. Mann M, Jensen ON. (2003). Proteomic analysis of post-translational modifications. Nat Biotechnol 21(3):255-261. (Pubitemid 36314808)
68. Jin X, Wang LS, Xia L, Zheng Y, Meng C, et al. (2008). Hyper-phosphorylation of alpha-enolase in hypertrophied left ventricle of spontaneously hypertensive rat. Biochem Biophys Res Commun 371(4):804-809.
69. López-Alemany R, Suelves M, Muñoz-Cánoves P. (2003).Plasmin generation dependent on alpha-enolase-type plasminogen receptor is required for myogenesis. Thromb Haemost 90(4):724-733.
70. Díaz-Ramos À, Roig-Borrellas A, García-Melero A, Llorens A, López-Alemany R. (2012). Requirement of plasminogen binding to its cell-surface receptor α-enolase for efficient regeneration of normal and dystrophic skeletal muscle. PLoS One 7(12):e50477.
71. Hsiao KC, Shih NY, Fang HL, Huang TS, Kuo CC, et al. (2013). Surface α-Enolase Promotes Extracellular Matrix Degradation and Tumor Metastasis and Represents a New Therapeutic Target. PLoS One 8(7):e69354.
72. Sha J, Erova TE, Alyea RA, Wang S, Olano JP, et al. (2009) Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. J Bacteriol 191(9):3095-107.
73. Bergmann S, Rohde M, Preissner KT, Hammerschmidt S. (2005). The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration. Thromb Haemost 94(2):304-11. (Pubitemid 41122484)