White spot syndrome virus protein kinase 1 defeats the host cell's iron-withholding defense mechanism by interacting with host ferritin

Journal of Virology

Volumn 89, Issue 2, 2015, Pages 1083-1093

  Lin, Shin Jen ^a,b   Lee, Der Yen ^b   Wang, Hao Ching ^c   Kang, Shih Ting ^a,b   Hwang, Pung Pung ^d   Kou, Guang Hsiung ^a   Huang, Ming Fen ^c   Chang, Geen Dong ^b   Loa, Chu Fang ^b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

APOFERRITIN; FERRITIN; FERROUS ION; PROTEIN KINASE; PROTEIN KINASE 1; UNCLASSIFIED DRUG; VIRUS PROTEIN; IRON; PROTEIN BINDING; VIRAL PROTEIN;

ARTICLE; ASSAY; ATOMIC ABSORPTION SPECTROMETRY; CELL LEVEL; CELLULAR LABILE IRON POOL; CONTROLLED STUDY; HOST CELL IRON WITHOLDING DEFENSE MECHANISM; HOST RESISTANCE; IMMUNOPRECIPITATION; IRON METABOLISM; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PULLDOWN ASSAY; QUARTZ CRYSTAL MICROBALANCE; SF9 CELL LINE; SHRIMP; VIRUS CELL INTERACTION; VIRUS VIRULENCE; WHITE SPOT SYNDROME VIRUS; ANIMAL; CELL LINE; CENTRIFUGATION; DEFENSE MECHANISM; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; TWO HYBRID SYSTEM;

DECAPODA (CRUSTACEA); SHRIMP WHITE SPOT SYNDROME VIRUS;

ANIMALS; CELL LINE; CENTRIFUGATION; DEFENSE MECHANISMS; FERRITINS; HOST-PATHOGEN INTERACTIONS; IRON; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN KINASES; QUARTZ CRYSTAL MICROBALANCE TECHNIQUES; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS; WHITE SPOT SYNDROME VIRUS 1;

EID: 84920771787     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02318-14     Document Type: Article

References (49)

1. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Eaton JW, Vercellotti GM. 1992. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J Biol Chem 267:18148-18153.
2. Epsztejn S, Glickstein H, Picard V, Slotki IN, Breuer W, Beaumont C, Cabantchik ZI. 1999. H-ferritin subunit overexpression in erythroid cells reduces the oxidative stress response and induces multidrug resistance properties. Blood 94:3593-3603.
3. Theil EC. 1987. Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu Rev Biochem 56:289-315. http://dx.doi.org/10.1146/annurev.bi.56.070187.001445.
4. Weinberg ED, Miklossy J. 2008. Iron withholding: a defense against disease. J Alzheimers Dis 13:451-463.
5. Larson JA, Howie HL, So M. 2004. Neisseria meningitidis accelerates ferritin degradation in host epithelial cells to yield an essential iron source. Mol Microbiol 53:807-820. http://dx.doi.org/10.1111/j.1365-2958.2004.04169.x.
6. Segond D, Abi Khalil E, Buisson C, Daou N, Kallassy M, Lereclus D, Arosio P, Bou-Abdallah F, Nielsen Le Roux C. 2014. Iron acquisition in Bacillus cereus: the roles of IlsA and bacillibactin in exogenous ferritin iron mobilization. PLoS Pathog 10:e1003935. http://dx.doi.org/10.1371/journal.ppat.1003935.
7. Weinberg ED. 1999. Iron loading and disease surveillance. Emerg Infect Dis 5:346-352. http://dx.doi.org/10.3201/eid0503.990305.
8. Whitby PW, Vanwagoner TM, Springer JM, Morton DJ, Seale TW, Stull TL. 2006. Burkholderia cenocepacia utilizes ferritin as an iron source. J Med Microbiol 55:661-668. http://dx.doi.org/10.1099/jmm.0.46199-0.
9. Ben-Arieh SV, Zimerman B, Smorodinsky NI, Yaacubovicz M, Schechter C, Bacik I, Gibbs J, Bennink JR, Yewdell JW, Coligan JE, Firat H, Lemonnier F, Ehrlich R. 2001. Human cytomegalovirus protein US2 interferes with the expression of human HFE, a nonclassical class I major histocompatibility complex molecule that regulates iron homeostasis. J Virol 75:10557-10562. http://dx.doi.org/10.1128/JVI.75.21.10557-10562.2001.
10. Vahdati-Ben Arieh S, Laham N, Schechter C, Yewdell JW, Coligan JE, Ehrlich R. 2003. A single viral protein HCMV US2 affects antigen presentation and intracellular iron homeostasis by degradation of classical HLA class I and HFE molecules. Blood 101:2858-2864. http://dx.doi.org/10.1182/blood-2002-07-2158.
11. Tsuji Y, Akebi N, Lam TK, Nakabeppu Y, Torti SV, Torti FM. 1995. FER-1, an enhancer of the ferritin H gene and a target of E1A-mediated transcriptional repression. Mol Cell Biol 15:5152-5164.
12. Bevilacqua MA, Faniello MC, Quaresima B, Tiano MT, Giuliano P, Feliciello A, Avvedimento VE, Cimino F, Costanzo F. 1997. A common mechanism underlying the E1A repression and the cAMP stimulation of the H ferritin transcription. J Biol Chem 272:20736-20741. http://dx.doi.org/10.1074/jbc.272.33.20736.
13. Pan D, He N, Yang Z, Liu H, Xu X. 2005. Differential gene expression profile in hepatopancreas of WSSV-resistant shrimp (Penaeus japonicus) by suppression subtractive hybridization. Dev Comp Immunol 29:103-112. http://dx.doi.org/10.1016/j.dci.2004.07.001.
14. Zhang J, Li F, Wang Z, Zhang X, Zhou Q, Xiang J. 2006. Cloning, expression and identification of ferritin from Chinese shrimp, Fenneropenaeus chinensis. J Biotechnol 125:173-184. http://dx.doi.org/10.1016/j.jbiotec.2006.03.010.
15. Clavero-Salas A, Sotelo-Mundo RR, Gollas-Galván T, Hernández-López J, Peregrino-Uriarte AB, Muhlia-Almazán A, Yepiz-Plascencia G. 2007. Transcriptome analysis of gills from the white shrimp Litopenaeus vannamei infected with white spot syndrome virus. Fish Shellfish Immunol 23:459-472. http://dx.doi.org/10.1016/j.fsi.2007.01.010.
16. Pongsomboon S, Tang S, Boonda S, Aoki T, Hirono I, Yasuike M, Tassanakajon A. 2008. Differentially expressed genes in Penaeus monodon hemocytes following infection with yellow head virus. BMB Rep 41:670-677. http://dx.doi.org/10.5483/BMBRep.2008.41.9.670.
17. Ruan YH, Kuo CM, Lo CF, Lee MH, Lian JL, Hsieh SL. 2010. Ferritin administration effectively enhances immunity, physiological responses, and survival of Pacific white shrimp (Litopenaeus vannamei) challenged with white spot syndrome virus. Fish Shellfish Immunol 28:542-548. http://dx.doi.org/10.1016/j.fsi.2009.12.013.
18. Liu WJ, Yu HT, Peng SE, Chang YS, Pien HW, Lin CJ, Huang CJ, Tsai MF, Huang CJ, Wang CH, Lin JY, Lo CF, Kou GH. 2001. Cloning, characterization, and phylogenetic analysis of a shrimp white spot syndrome virus gene that encodes a protein kinase. Virology 289:362-377. http://dx.doi.org/10.1006/viro.2001.1091.
19. van Hulten MC, Vlak JM. 2001. Identification and phylogeny of a protein kinase gene of white spot syndrome virus. Virus Genes 22:201-207. http://dx.doi.org/10.1023/A:1008127709325.
20. van Hulten MC, Witteveldt J, Peters S, Kloosterboer N, Tarchini R, Fiers M, Sandbrink H, Lankhorst RK, Vlak JM. 2001. The white spot syndrome virus DNA genome sequence. Virology 28:7-22. http://dx.doi.org/10.1006/viro.2001.1002.
21. Kim CS, Kosuke Z, Nam YK, Kim SK, Kim KH. 2007. Protection of shrimp (Penaeus chinensis) against white spot syndrome virus (WSSV) challenge by double-stranded RNA. Fish Shellfish Immunol 23:242-246. http://dx.doi.org/10.1016/j.fsi.2006.10.012.
22. Hsieh SL, Chiu YC, Kuo CM. 2006. Molecular cloning and tissue distribution of ferritin in Pacific white shrimp (Litopenaeus vannamei). Fish Shellfish Immunol 21:279-283. http://dx.doi.org/10.1016/j.fsi.2005.12.003.
23. Sangsuriya P, Huang JY, Chu YF, Phiwsaiya K, Leekitcharoenphon P, Meemetta W, Senapin S, Huang WP, Withyachumnarnkul B, Flegel TW, Lo CF. 2014. Construction and application of a protein interaction map for white spot syndrome virus (WSSV). Mol Cell Proteomics 13:269-282. http://dx.doi.org/10.1074/mcp.M113.029199.
24. Leu JH, Kuo YC, Kou GH, Lo CF. 2008. Molecular cloning and characterization of an inhibitor of apoptosis protein (IAP) from the tiger shrimp, Penaeus monodon. Dev Comp Immunol 32:121-133. http://dx.doi.org/10.1016/j.dci.2007.05.005.
25. Espósito BP, Epsztejn S, Breuer W, Cabantchik ZI. 2002. A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem 304:1-18. http://dx.doi.org/10.1006/abio.2002.5611.
26. Breuer W, Epsztejn S, Millgram P, Cabantchik IZ. 1995. Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am J Physiol 268:1354-1361.
27. 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. http://dx.doi.org/10.1128/JVI.05385-11.
28. Aziz N, Munro HN. 1987. Iron regulates ferritin mRNA translation through a segment of its 5' untranslated region. Proc Natl Acad Sci USA 84:8478-8482. http://dx.doi.org/10.1073/pnas.84.23.8478.
29. Hentze MW, Rouault TA, Caughman SW, Dancis A, Harford JB, Klausner RD. 1987. A cis-acting element is necessary and sufficient for translational regulation of human ferritin expression in response to iron. Proc Natl Acad Sci USA 84:6730-6734. http://dx.doi.org/10.1073/pnas.84.19.6730.
30. Eisenstein RS. 2000. Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 20:627-662. http://dx.doi.org/10.1146/annurev.nutr.20.1.627.
31. Fraga CG. 2005. Relevance, essentiality and toxicity of trace elements in human health. Mol Aspects Med 26:235-244. http://dx.doi.org/10.1016/j.mam.2005.07.013.
32. Hatefi Y. 1985. The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54:1015-1069. http://dx.doi.org/10.1146/annurev.bi.54.070185.005055.
33. Jordan A, Reichard P. 1998. Ribonucleotide reductases. Annu Rev Biochem 67:71-98. http://dx.doi.org/10.1146/annurev.biochem.67.1.71.
34. Pang H, Bartlam M, Zeng Q, Miyatake H, Hisano T, Miki K, Wong LL, Gao GF, Rao Z. 2004. Crystal structure of human pirin: an iron-binding nuclear protein and transcription cofactor. J Biol Chem 279:1491-1498. http://dx.doi.org/10.1074/jbc.M310022200.
35. Rudolf J, Makrantoni V, Ingledew WJ, Stark MJ, White MF. 2006. The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol Cell 23:801-808. http://dx.doi.org/10.1016/j.molcel.2006.07.019.
36. Klinge S, Hirst J, Maman JD, Krude T, Pellegrini L. 2007. An iron-sulfur domain of the eukaryotic primase is essential for RNA primer synthesis. Nat Struct Mol Biol 14:875-877. http://dx.doi.org/10.1038/nsmb1288.
37. Cooper CE, Lynagh GR, Hoyes KP, Hider RC, Cammack R, Porter JB. 1996. The relationship of intracellular iron chelation to the inhibition and regeneration of human ribonucleotide reductase. J Biol Chem 271:20291-20299. http://dx.doi.org/10.1074/jbc.271.34.20291.
38. Lamarche N, Matton G, Massie B, Fontecave M, Atta M, Dumas F, Gaudreau P, Langelier Y. 1996. Production of the R2 subunit of ribonucleotide reductase from herpes simplex virus with prokaryotic and eukaryotic expression systems: higher activity of R2 produced by eukaryotic cells related to higher iron-binding capacity. Biochem J 320:129-135.
39. Chabes A, Domkin V, Larsson G, Liu A, Graslund A, Wijmenga S, Thelander L. 2000. Yeast ribonucleotide reductase has a heterodimeric iron-radical-containing subunit. Proc Natl Acad Sci USA 97:2474-2479. http://dx.doi.org/10.1073/pnas.97.6.2474.
40. Dai Y, Gold B, Vishwanatha JK, Rhode SL. 1994. Mimosine inhibits viral DNA synthesis through ribonucleotide reductase. Virology 205:210-216. http://dx.doi.org/10.1006/viro.1994.1636.
41. Romeo AM, Christen L, Niles EG, Kosman DJ. 2001. Intracellular chelation of iron by bipyridyl inhibits DNA virus replication: ribonucleotide reductase maturation as a probe of intracellular iron pools. J Biol Chem 276:24301-24308. http://dx.doi.org/10.1074/jbc.M010806200.
42. Laghaei R, Evans DG, Coalson RD. 2013. Metal binding sites of human H-chain ferritin and iron transport mechanism to the ferroxidase sites: a molecular dynamics simulation study. Proteins 81:1042-1050. http://dx.doi.org/10.1002/prot.24251.
43. Durand JP, Goudard F, Pieri J, Escoubas JM, Schreiber N, Cadoret JP. 2004. Crassostrea gigas ferritin: cDNA sequence analysis for two heavy chain type subunits and protein purification. Gene 338:187-195. http://dx.doi.org/10.1016/j.gene.2004.04.027.
44. Dong F, Zhang X, Culver B, Chew HG, Jr, Kelley RO, Ren J. 2005. Dietary iron deficiency induces ventricular dilation, mitochondrial ultrastructural aberrations and cytochrome c release: involvement of nitric oxide synthase and protein tyrosine nitration. Clin Sci (Lond) 109:277-286. http://dx.doi.org/10.1042/CS20040278.
45. Halliwell B, Gutteridge JM. 1990. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186:1-85. http://dx.doi.org/10.1016/0076-6879(90)86093-B.
46. Ihara K, Maeguchi K, Young CT, Theil EC. 1984. Cell-specific properties of red cell and liver ferritin from bullfrog tadpoles probed by phosphorylation in vitro. J Biol Chem 259:278-283.
47. Rama-Kumar T. 1998. Ph.D. thesis. University of Hyderabad, Hyderabad, India.
48. Weaver J, Pollack S. 1989. Low-Mr iron isolated from guinea pig reticulocytes as AMP-Fe and ATP-Fe complexes. Biochem J 261:787-792.
49. Konopka K, Mareschal JC, Crichton RR. 1981. Iron transfer from transferrin to ferritin mediated by polyphosphate compounds. Biochim Biophys Acta 677:417-423. http://dx.doi.org/10.1016/0304-4165(81)90255-5.