The Marburg Virus VP24 Protein Interacts with Keap1 to Activate the Cytoprotective Antioxidant Response Pathway

Cell Reports

Volumn 6, Issue 6, 2014, Pages 1017-1025

  Edwards, Megan R ^a   Johnson, Britney ^b   Mire, Chad E ^c   Xu, Wei ^b   Shabman, Reed S ^a,d   Speller, Lauren N ^b   Leung, Daisy W ^b   Geisbert, Thomas W ^c   Amarasinghe, Gaya K ^b   Basler, Christopher F ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KELCH LIKE ECH ASSOCIATED PROTEIN 1; PROTEIN VP24; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VIRUS PROTEIN; ANTIOXIDANT; KEAP1 PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL PEPTIDE; VP24 PROTEIN, MARBURG VIRUS;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BINDING AFFINITY; CELL PROTECTION; CONTROLLED STUDY; EBOLA VIRUS; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; MARBURG VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STOICHIOMETRY; UBIQUITINATION; VIRUS MORPHOLOGY; ANIMAL; BIOSYNTHESIS; CHEMICAL STRUCTURE; ENZYME SPECIFICITY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; MARBURG HEMORRHAGIC FEVER; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; VIROLOGY; ANTIOXIDANT ACTIVITY; BINDING SITE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; HOST RESISTANCE; HUMAN CELL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRUCTURE ANALYSIS; TRANSCRIPTION INITIATION; UPREGULATION; VIRUS CELL INTERACTION;

LAKE VICTORIA MARBURGVIRUS; ZAIRE EBOLAVIRUS;

ANIMALS; ANTIOXIDANTS; CYTOPROTECTION; GENE EXPRESSION; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MARBURG VIRUS DISEASE; MARBURGVIRUS; MODELS, MOLECULAR; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TRANSFECTION; VIRAL PROTEINS;

EID: 84897039093     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.01.043     Document Type: Article

References (47)

1. Amman B.R., Carroll S.A., Reed Z.D., Sealy T.K., Balinandi S., Swanepoel R., Kemp A., Erickson B.R., Comer J.A., Campbell S., et al. Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathog. 2012, 8:e1002877.
2. Baird L., Dinkova-Kostova A.T. The cytoprotective role of the Keap1-Nrf2 pathway. Arch. Toxicol. 2011, 85:241-272.
3. Bamberg S., Kolesnikova L., Möller P., Klenk H.D., Becker S. VP24 of Marburg virus influences formation of infectious particles. J.Virol. 2005, 79:13421-13433.
4. Beniac D.R., Melito P.L., Devarennes S.L., Hiebert S.L., Rabb M.J., Lamboo L.L., Jones S.M., Booth T.F. The organisation of Ebola virus reveals a capacity for extensive, modular polyploidy. PLoS One 2012, 7:e29608.
5. Bharat T.A., Riches J.D., Kolesnikova L., Welsch S., Krähling V., Davey N., Parsy M.L., Becker S., Briggs J.A. Cryo-electron tomography of Marburg virus particles and their morphogenesis within infected cells. PLoS Biol. 2011, 9:e1001196.
6. Bharat T.A., Noda T., Riches J.D., Kraehling V., Kolesnikova L., Becker S., Kawaoka Y., Briggs J.A. Structural dissection of Ebola virus and its assembly determinants using cryo-electron tomography. Proc. Natl. Acad. Sci. USA 2012, 109:4275-4280.
7. Brauburger K., Hume A.J., Mühlberger E., Olejnik J. Forty-five years of Marburg virus research. Viruses 2012, 4:1878-1927.
8. Burdette D., Olivarez M., Waris G. Activation of transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway. J.Gen. Virol. 2010, 91:681-690.
9. Cho H.Y., Imani F., Miller-DeGraff L., Walters D., Melendi G.A., Yamamoto M., Polack F.P., Kleeberger S.R. Antiviral activity of Nrf2 in a murine model of respiratory syncytial virus disease. Am. J. Respir. Crit. Care Med. 2009, 179:138-150.
10. Chorley B.N., Campbell M.R., Wang X., Karaca M., Sambandan D., Bangura F., Xue P., Pi J., Kleeberger S.R., Bell D.A. Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoid X receptor alpha. Nucleic Acids Res. 2012, 40:7416-7429.
11. Copple I.M. The Keap1-Nrf2 cell defense pathway-a promising therapeutic target?. Adv. Pharmacol. 2012, 63:43-79.
12. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc. Natl. Acad. Sci. USA 2002, 99:11908-11913.
13. Fan W., Tang Z., Chen D., Moughon D., Ding X., Chen S., Zhu M., Zhong Q. Keap1 facilitates p62-mediated ubiquitin aggregate clearance via autophagy. Autophagy 2010, 6:614-621.
14. Hill-Batorski L., Halfmann P., Neumann G., Kawaoka Y. The cytoprotective enzyme heme oxygenase-1 suppresses Ebola virus replication. J.Virol. 2013, 87:13795-13802.
15. Hoenen T., Groseth A., Kolesnikova L., Theriault S., Ebihara H., Hartlieb B., Bamberg S., Feldmann H., Ströher U., Becker S. Infection of naive target cells with virus-like particles: implications for the function of ebola virus VP24. J.Virol. 2006, 80:7260-7264.
16. Huang Y., Xu L., Sun Y., Nabel G.J. The assembly of Ebola virus nucleocapsid requires virion-associated proteins 35 and 24 and posttranslational modification of nucleoprotein. Mol. Cell 2002, 10:307-316.
17. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13:76-86.
18. Ivanov A.V., Smirnova O.A., Ivanova O.N., Masalova O.V., Kochetkov S.N., Isaguliants M.G. Hepatitis C virus proteins activate NRF2/ARE pathway by distinct ROS-dependent and independent mechanisms in HUH7 cells. PLoS One 2011, 6:e24957.
19. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
20. Kesic M.J., Simmons S.O., Bauer R., Jaspers I. Nrf2 expression modifies influenza A entry and replication in nasal epithelial cells. Free Radic. Biol. Med. 2011, 51:444-453.
21. Kim J.E., You D.J., Lee C., Ahn C., Seong J.Y., Hwang J.I. Suppression of NF-kappaB signaling by KEAP1 regulation of IKKbeta activity through autophagic degradation and inhibition of phosphorylation. Cell. Signal. 2010, 22:1645-1654.
22. Komatsu M., Kurokawa H., Waguri S., Taguchi K., Kobayashi A., Ichimura Y., Sou Y.S., Ueno I., Sakamoto A., Tong K.I., et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 2010, 12:213-223.
23. Lau A., Wang X.J., Zhao F., Villeneuve N.F., Wu T., Jiang T., Sun Z., White E., Zhang D.D. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 2010, 30:3275-3285.
24. Lee D.F., Kuo H.P., Liu M., Chou C.K., Xia W., Du Y., Shen J., Chen C.T., Huo L., Hsu M.C., et al. KEAP1 E3 ligase-mediated downregulation of NF-kappaB signaling by targeting IKKbeta. Mol. Cell 2009, 36:131-140.
25. Lee J., Koh K., Kim Y.E., Ahn J.H., Kim S. Upregulation of Nrf2 expression by human cytomegalovirus infection protects host cells from oxidative stress. J.Gen. Virol. 2013, 94:1658-1668.
26. Lo S.C., Hannink M. PGAM5, a Bcl-XL-interacting protein, is a novel substrate for the redox-regulated Keap1-dependent ubiquitin ligase complex. J.Biol. Chem. 2006, 281:37893-37903.
27. Lo S.C., Li X., Henzl M.T., Beamer L.J., Hannink M. Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling. EMBO J. 2006, 25:3605-3617.
28. Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 2013, 53:401-426.
29. Magesh S., Chen Y., Hu L. Small molecule modulators of Keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents. Med. Res. Rev. 2012, 32:687-726.
30. Mateo M., Reid S.P., Leung L.W., Basler C.F., Volchkov V.E. Ebolavirus VP24 binding to karyopherins is required for inhibition of interferon signaling. J.Virol. 2010, 84:1169-1175.
31. Mateo M., Carbonnelle C., Martinez M.J., Reynard O., Page A., Volchkova V.A., Volchkov V.E. Knockdown of Ebola virus VP24 impairs viral nucleocapsid assembly and prevents virus replication. J.Infect. Dis. 2011, 204(Suppl 3):S892-S896.
32. McMahon M., Itoh K., Yamamoto M., Hayes J.D. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J.Biol. Chem. 2003, 278:21592-21600.
33. Niture S.K., Jaiswal A.K. Inhibitor of Nrf2 (INrf2 or Keap1) protein degrades Bcl-xL via phosphoglycerate mutase 5 and controls cellular apoptosis. J.Biol. Chem. 2011, 286:44542-44556.
34. Noda T., Ebihara H., Muramoto Y., Fujii K., Takada A., Sagara H., Kim J.H., Kida H., Feldmann H., Kawaoka Y. Assembly and budding of Ebolavirus. PLoS Pathog. 2006, 2:e99.
35. Padmanabhan B., Nakamura Y., Yokoyama S. Structural analysis of the complex of Keap1 with a prothymosin alpha peptide. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2008, 64:233-238.
36. Pichlmair A., Kandasamy K., Alvisi G., Mulhern O., Sacco R., Habjan M., Binder M., Stefanovic A., Eberle C.A., Goncalves A., et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 2012, 487:486-490.
37. Reid S.P., Leung L.W., Hartman A.L., Martinez O., Shaw M.L., Carbonnelle C., Volchkov V.E., Nichol S.T., Basler C.F. Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J.Virol. 2006, 80:5156-5167.
38. Reid S.P., Valmas C., Martinez O., Sanchez F.M., Basler C.F. Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J.Virol. 2007, 81:13469-13477.
39. Schaedler S., Krause J., Himmelsbach K., Carvajal-Yepes M., Lieder F., Klingel K., Nassal M., Weiss T.S., Werner S., Hildt E. Hepatitis B virus induces expression of antioxidant response element-regulated genes by activation of Nrf2. J.Biol. Chem. 2010, 285:41074-41086.
40. Tong K.I., Katoh Y., Kusunoki H., Itoh K., Tanaka T., Yamamoto M. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol. Cell. Biol. 2006, 26:2887-2900.
41. Tong K.I., Padmanabhan B., Kobayashi A., Shang C., Hirotsu Y., Yokoyama S., Yamamoto M. Different electrostatic potentials define ETGE and DLG motifs as hinge and latch in oxidative stress response. Mol. Cell. Biol. 2007, 27:7511-7521.
42. Towner J.S., Amman B.R., Sealy T.K., Carroll S.A., Comer J.A., Kemp A., Swanepoel R., Paddock C.D., Balinandi S., Khristova M.L., et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 2009, 5:e1000536.
43. Valmas C., Grosch M.N., Schümann M., Olejnik J., Martinez O., Best S.M., Krähling V., Basler C.F., Mühlberger E. Marburg virus evades interferon responses by a mechanism distinct from ebola virus. PLoS Pathog. 2010, 6:e1000721.
44. Watanabe S., Noda T., Halfmann P., Jasenosky L., Kawaoka Y. Ebola virus (EBOV) VP24 inhibits transcription and replication of the EBOV genome. J.Infect. Dis. 2007, 196(Suppl 2):S284-S290.
45. Wenigenrath J., Kolesnikova L., Hoenen T., Mittler E., Becker S. Establishment and application of an infectious virus-like particle system for Marburg virus. J.Gen. Virol. 2010, 91:1325-1334.
46. Zhang D.D., Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 2003, 23:8137-8151.
47. Zhang A.P., Bornholdt Z.A., Liu T., Abelson D.M., Lee D.E., Li S., Woods V.L., Saphire E.O. The ebola virus interferon antagonist VP24 directly binds STAT1 and has a novel, pyramidal fold. PLoS Pathog. 2012, 8:e1002550.