Sphingosine Kinase 1 Serves as a Pro-Viral Factor by Regulating Viral RNA Synthesis and Nuclear Export of Viral Ribonucleoprotein Complex upon Influenza Virus Infection

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Seo, Young Jin ^a   Pritzl, Curtis J ^a   Vijayan, Madhuvanthi ^a   Bomb, Kavita ^a   McClain, Mariah E ^a   Alexander, Stephen ^a   Hahm, Bumsuk ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHROMOSOME REGION MAINTENANCE 1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE B; RAN BINDING PROTEIN 3; RIBONUCLEOPROTEIN; SPHINGOSINE KINASE 1; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; INFLUENZA; INTRACELLULAR SIGNALING; NONHUMAN; NUCLEAR EXPORT SIGNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; RNA SYNTHESIS; VIRUS PATHOGENESIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; DOGS; ENZYME ACTIVATION; ENZYME INHIBITORS; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; MADIN DARBY CANINE KIDNEY CELLS; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RIBONUCLEOPROTEINS; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84883313477     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075005     Document Type: Article

References (70)

1. Thompson MG, Shay DK, Zhou H, Bridges CB, Cheng PY, et al. (2010) Estimates of deaths associated with seasonal influenza--- United States, 1976-2007. MMWR Morb Mortal Wkly Rep 59: 1057-1062. PubMed: 20798667.
2. WHO (2011) Global monitoring of antiviral resistance in currently circulating human influenza viruses, November 2011. Wkly Epidemiol Rec 86: 497-501. PubMed: 22128380.
3. Hurt AC, Chotpitayasunondh T, Cox NJ, Daniels R, Fry AM, et al. (2012) Antiviral resistance during the 2009 influenza A H1N1 pandemic: public health, laboratory, and clinical perspectives. Lancet Infect Dis 12: 240-248. doi:10.1016/S1473-3099(11)70318-8. PubMed: 22186145.
4. Rappuoli R, Dormitzer PR, (2012) Influenza: options to improve pandemic preparation. Science 336: 1531-1533. doi:10.1126/science.1221466. PubMed: 22723412.
5. Moscona A, (2009) Global transmission of oseltamivir-resistant influenza. N Engl J Med 360: 953-956. doi:10.1056/NEJMp0900648. PubMed: 19258250.
6. Neumann G, Brownlee GG, Fodor E, Kawaoka Y, (2004) Orthomyxovirus replication, transcription, and polyadenylation. Curr Top Microbiol Immunol 283: 121-143. doi:10.1007/978-3-662-06099-5_4. PubMed: 15298169.
7. Medina RA, García-Sastre A, (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9: 590-603. doi:10.1038/nrmicro2613. PubMed: 21747392.
8. Lamb RA, Krug RM, (2001) Fields Virology Knipe DM, Howley PM, eds. Philadelphia: Lippincott; Williams, Williams 1487-1531 p.
9. Arora DJ, Gasse N, (1998) Influenza virus hemagglutinin stimulates the protein kinase C activity of human polymorphonuclear leucocytes. Arch Virol 143: 2029-2037. doi:10.1007/s007050050439. PubMed: 9856090.
10. Root CN, Wills EG, McNair LL, Whittaker GR, (2000) Entry of influenza viruses into cells is inhibited by a highly specific protein kinase C inhibitor. J Gen Virol 81: 2697-2705. PubMed: 11038382.
11. Sieczkarski SB, Brown HA, Whittaker GR, (2003) Role of protein kinase C betaII in influenza virus entry via late endosomes. J Virol 77: 460-469. doi:10.1128/JVI.77.1.460-469.2003. PubMed: 12477851.
12. Ehrhardt C, Marjuki H, Wolff T, Nürnberg B, Planz O, et al. (2006) Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell Microbiol 8: 1336-1348. doi:10.1111/j.1462-5822.2006.00713.x. PubMed: 16882036.
13. Kumar N, Xin ZT, Liang Y, Ly H, (2008) NF-kappaB signaling differentially regulates influenza virus RNA synthesis. J Virol 82: 9880-9889. doi:10.1128/JVI.00909-08. PubMed: 18701591.
14. Pleschka S, Ludwig S, Planz O, Wolff T, (2009) Signaling Pathways Induced by Influenza Viruses. In: Yang D, eds. RNA viruses: host gene responses to infections: World Scientific. pp. pp. 109-129.
15. Watanabe K, Takizawa N, Katoh M, Hoshida K, Kobayashi N, et al. (2001) Inhibition of nuclear export of ribonucleoprotein complexes of influenza virus by leptomycin B. Virus Res 77: 31-42. doi:10.1016/S0168-1702(01)00263-5. PubMed: 11451485.
16. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, et al. (2001) Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 75: 408-419. doi:10.1128/JVI.75.1.408-419.2001. PubMed: 11119609.
17. Watanabe K, Takizawa N, Noda S, Tsukahara F, Maru Y, et al. (2008) Hsc70 regulates the nuclear export but not the import of influenza viral RNP: A possible target for the development of anti-influenza virus drugs. Drugs Discov Ther 2: 77-84.
18. Pleschka S, Wolff T, Ehrhardt C, Hobom G, Planz O, et al. (2001) Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat Cell Biol 3: 301-305. doi:10.1038/35060098. PubMed: 11231581.
19. Ludwig S, Wolff T, Ehrhardt C, Wurzer WJ, Reinhardt J, et al. (2004) MEK inhibition impairs influenza B virus propagation without emergence of resistant variants. FEBS Lett 561: 37-43. doi:10.1016/S0014-5793(04)00108-5. PubMed: 15013748.
20. Shin YK, Liu Q, Tikoo SK, Babiuk LA, Zhou Y, (2007) Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenza A virus propagation. J Gen Virol 88: 942-950. doi:10.1099/vir.0.82483-0. PubMed: 17325368.
21. Pitson SM, (2011) Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem Sci 36: 97-107. doi:10.1016/j.tibs.2010.08.001. PubMed: 20870412.
22. Oskouian B, Saba JD, (2010) Cancer treatment strategies targeting sphingolipid metabolism. Adv Exp Med Biol 688: 185-205. doi:10.1007/978-1-4419-6741-1_13. PubMed: 20919655.
23. Paugh SW, Paugh BS, Rahmani M, Kapitonov D, Almenara JA, et al. (2008) A selective sphingosine kinase 1 inhibitor integrates multiple molecular therapeutic targets in human leukemia. Blood 112: 1382-1391. doi:10.1182/blood-2008-02-138958. PubMed: 18511810.
24. Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, et al. (2010) Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465: 1084-1088. doi:10.1038/nature09128. PubMed: 20577214.
25. Le Stunff H, Milstien S, Spiegel S, (2004) Generation and metabolism of bioactive sphingosine-1-phosphate. J Cell Biochem 92: 882-899. doi:10.1002/jcb.20097. PubMed: 15258913.
26. Gault CR, Obeid LM, (2011) Still benched on its way to the bedside: sphingosine kinase 1 as an emerging target in cancer chemotherapy. Crit Rev Biochem Mol Biol 46: 342-351. doi:10.3109/10409238.2011.597737. PubMed: 21787121.
27. Orr Gandy KA, Obeid LM, (2013) Targeting the sphingosine kinase/sphingosine 1-phosphate pathway in disease: review of sphingosine kinase inhibitors. Biochim Biophys Acta 1831: 157-166. doi:10.1016/j.bbalip.2012.07.002. PubMed: 22801037.
28. Carr JM, Mahalingam S, Bonder CS, Pitson SM, (2012) Sphingosine kinase 1 in viral infections. Rev Med Virol, 23: 73-84. PubMed: 22639116.
29. Min J, Mesika A, Sivaguru M, Van Veldhoven PP, Alexander H, et al. (2007) (Dihydro)ceramide synthase 1 regulated sensitivity to cisplatin is associated with the activation of p38 mitogen-activated protein kinase and is abrogated by sphingosine kinase 1. Mol Cancer Res 5: 801-812. doi:10.1158/1541-7786.MCR-07-0100. PubMed: 17699106.
30. Olivera A, Kohama T, Edsall L, Nava V, Cuvillier O, et al. (1999) Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J Cell Biol 147: 545-558. doi:10.1083/jcb.147.3.545. PubMed: 10545499.
31. Seo YJ, Blake C, Alexander S, Hahm B, (2010) Sphingosine 1-phosphate-metabolizing enzymes control influenza virus propagation and viral cytopathogenicity. J Virol 84: 8124-8131. doi:10.1128/JVI.00510-10. PubMed: 20519401.
32. Seo YJ, Alexander S, Hahm B, (2011) Does cytokine signaling link sphingolipid metabolism to host defense and immunity against virus infections? Cytokine Growth Factor Rev 22: 55-61. doi:10.1016/j.cytogfr.2010.12.001. PubMed: 21251870.
33. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, et al. (1999) Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96: 9345-9350. doi:10.1073/pnas.96.16.9345. PubMed: 10430945.
34. Eierhoff T, Ludwig S, Ehrhardt C, (2009) The influenza A virus matrix protein as a marker to monitor initial virus internalisation. Biol Chem 390: 509-515. PubMed: 19335204.
35. Nakhaei P, Mesplede T, Solis M, Sun Q, Zhao T, et al. (2009) The E3 ubiquitin ligase Triad3A negatively regulates the RIG-I/MAVS signaling pathway by targeting TRAF3 for degradation. PLOS Pathog 5: e1000650. PubMed: 19893624.
36. Pitson SM, Moretti PA, Zebol JR, Lynn HE, Xia P, et al. (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J 22: 5491-5500. doi:10.1093/emboj/cdg540. PubMed: 14532121.
37. Edsall LC, Van Brocklyn JR, Cuvillier O, Kleuser B, Spiegel S, (1998) N,N-Dimethylsphingosine is a potent competitive inhibitor of sphingosine kinase but not of protein kinase C: modulation of cellular levels of sphingosine 1-phosphate and ceramide. Biochemistry 37: 12892-12898. doi:10.1021/bi980744d. PubMed: 9737868.
38. Yatomi Y, Ruan F, Megidish T, Toyokuni T, Hakomori S, et al. (1996) N,N-dimethylsphingosine inhibition of sphingosine kinase and sphingosine 1-phosphate activity in human platelets. Biochemistry 35: 626-633. doi:10.1021/bi9515533. PubMed: 8555236.
39. French KJ, Schrecengost RS, Lee BD, Zhuang Y, Smith SN, et al. (2003) Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res 63: 5962-5969. PubMed: 14522923.
40. Bui M, Wills EG, Helenius A, Whittaker GR, (2000) Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J Virol 74: 1781-1786. doi:10.1128/JVI.74.4.1781-1786.2000. PubMed: 10644350.
41. Martin K, Helenius A, (1991) Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67: 117-130. doi:10.1016/0092-8674(91)90576-K. PubMed: 1913813.
42. O'Neill RE, Talon J, Palese P, (1998) The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J 17: 288-296. doi:10.1093/emboj/17.1.288. PubMed: 9427762.
43. Lindsay ME, Holaska JM, Welch K, Paschal BM, Macara IG, (2001) Ran-binding protein 3 is a cofactor for Crm1-mediated nuclear protein export. J Cell Biol 153: 1391-1402. doi:10.1083/jcb.153.7.1391. PubMed: 11425870.
44. Predicala R, Zhou Y, (2013) The Role of Ran-Binding Protein 3 During Influenza A Virus Replication. J Gen Virol Epub ahead of print. PubMed: 23303829.
45. Yoon SO, Shin S, Liu Y, Ballif BA, Woo MS, et al. (2008) Ran-binding protein 3 phosphorylation links the Ras and PI3-kinase pathways to nucleocytoplasmic transport. Mol Cell 29: 362-375. doi:10.1016/j.molcel.2007.12.024. PubMed: 18280241.
46. Reyes-Del Valle J, Chávez-Salinas S, Medina F, Del Angel RM, (2005) Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol 79: 4557-4567. doi:10.1128/JVI.79.8.4557-4567.2005. PubMed: 15795242.
47. Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV, (2007) Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J Virol 81: 374-383. doi:10.1128/JVI.01134-06. PubMed: 17050612.
48. Medigeshi GR, Hirsch AJ, Streblow DN, Nikolich-Zugich J, Nelson JA, (2008) West Nile virus entry requires cholesterol-rich membrane microdomains and is independent of alphavbeta3 integrin. J Virol 82: 5212-5219. doi:10.1128/JVI.00008-08. PubMed: 18385233.
49. Finnegan CM, Rawat SS, Puri A, Wang JM, Ruscetti FW, et al. (2004) Ceramide, a target for antiretroviral therapy. Proc Natl Acad Sci U S A 101: 15452-15457. doi:10.1073/pnas.0402874101. PubMed: 15489273.
50. Voisset C, Lavie M, Helle F, Op De Beeck A, Bilheu A, et al. (2008) Ceramide enrichment of the plasma membrane induces CD81 internalization and inhibits hepatitis C virus entry. Cell Microbiol 10: 606-617. doi:10.1111/j.1462-5822.2007.01070.x. PubMed: 17979982.
51. Snook CF, Jones JA, Hannun YA, (2006) Sphingolipid-binding proteins. Biochim Biophys Acta 1761: 927-946. doi:10.1016/j.bbalip.2006.06.004. PubMed: 16901751.
52. Seo YJ, Hahm B, (2010) Type I interferon modulates the battle of host immune system against viruses. Adv Appl Microbiol 73: 83-101. doi:10.1016/S0065-2164(10)73004-5. PubMed: 20800760.
53. Wang X, Li M, Zheng H, Muster T, Palese P, et al. (2000) Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J Virol 74: 11566-11573. doi:10.1128/JVI.74.24.11566-11573.2000. PubMed: 11090154.
54. García-Sastre A, (2011) Induction and evasion of type I interferon responses by influenza viruses. Virus Res 162: 12-18. doi:10.1016/j.virusres.2011.10.017. PubMed: 22027189.
55. Wurzer WJ, Ehrhardt C, Pleschka S, Berberich-Siebelt F, Wolff T, et al. (2004) NF-kappaB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J Biol Chem 279: 30931-30937. doi:10.1074/jbc.M403258200. PubMed: 15143063.
56. Nimmerjahn F, Dudziak D, Dirmeier U, Hobom G, Riedel A, et al. (2004) Active NF-kappaB signalling is a prerequisite for influenza virus infection. J Gen Virol 85: 2347-2356. doi:10.1099/vir.0.79958-0. PubMed: 15269376.
57. Hayden MS, Ghosh S, (2012) NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26: 203-234. doi:10.1101/gad.183434.111. PubMed: 22302935.
58. Dai F, Lin X, Chang C, Feng XH, (2009) Nuclear export of Smad2 and Smad3 by RanBP3 facilitates termination of TGF-beta signaling. Dev Cell 16: 345-357. doi:10.1016/j.devcel.2009.01.022. PubMed: 19289081.
59. Hendriksen J, Fagotto F, van der Velde H, van Schie M, Noordermeer J, et al. (2005) RanBP3 enhances nuclear export of active (beta)-catenin independently of CRM1. J Cell Biol 171: 785-797. doi:10.1083/jcb.200502141. PubMed: 16314428.
60. Yamane D, Zahoor MA, Mohamed YM, Azab W, Kato K, et al. (2009) Inhibition of sphingosine kinase by bovine viral diarrhea virus NS3 is crucial for efficient viral replication and cytopathogenesis. J Biol Chem 284: 13648-13659. doi:10.1074/jbc.M807498200. PubMed: 19293152.
61. Wati S, Rawlinson SM, Ivanov RA, Dorstyn L, Beard MR, et al. (2011) Tumour necrosis factor alpha (TNF-alpha) stimulation of cells with established dengue virus type 2 infection induces cell death that is accompanied by a reduced ability of TNF-alpha to activate nuclear factor kappa B and reduced sphingosine kinase-1 activity. J Gen Virol 92: 807-818. doi:10.1099/vir.0.028159-0. PubMed: 21148274.
62. Monick MM, Cameron K, Powers LS, Butler NS, McCoy D, et al. (2004) Sphingosine kinase mediates activation of extracellular signal-related kinase and Akt by respiratory syncytial virus. Am J Respir Cell Mol Biol 30: 844-852. doi:10.1165/rcmb.2003-0424OC. PubMed: 14742298.
63. Machesky NJ, Zhang G, Raghavan B, Zimmerman P, Kelly SL, et al. (2008) Human cytomegalovirus regulates bioactive sphingolipids. J Biol Chem 283: 26148-26160. doi:10.1074/jbc.M710181200. PubMed: 18644793.
64. Strub GM, Maceyka M, Hait NC, Milstien S, Spiegel S, (2010) Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol 688: 141-155. doi:10.1007/978-1-4419-6741-1_10. PubMed: 20919652.
65. Xia P, Wang L, Moretti PA, Albanese N, Chai F, et al. (2002) Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J Biol Chem 277: 7996-8003. doi:10.1074/jbc.M111423200. PubMed: 11777919.
66. Marsolais D, Hahm B, Walsh KB, Edelmann KH, McGavern D, et al. (2009) A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection. Proc Natl Acad Sci U S A 106: 1560-1565. doi:10.1073/pnas.0812689106. PubMed: 19164548.
67. Walsh KB, Teijaro JR, Wilker PR, Jatzek A, Fremgen DM, et al. (2011) Suppression of cytokine storm with a sphingosine analog provides protection against pathogenic influenza virus. Proc Natl Acad Sci U S A 108: 12018-12023. doi:10.1073/pnas.1107024108. PubMed: 21715659.
68. Teijaro JR, Walsh KB, Cahalan S, Fremgen DM, Roberts E, et al. (2011) Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 146: 980-991. doi:10.1016/j.cell.2011.08.015. PubMed: 21925319.
69. Pchejetski D, Nunes J, Coughlan K, Lall H, Pitson SM, et al. (2011) The involvement of sphingosine kinase 1 in LPS-induced Toll-like receptor 4-mediated accumulation of HIF-1alpha protein, activation of ASK1 and production of the pro-inflammatory cytokine IL-6. Immunol Cell Biol 89: 268-274.
70. Snider AJ, Kawamori T, Bradshaw SG, Orr KA, Gilkeson GS, et al. (2009) A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J 23: 143-152. doi:10.1096/fj.08-118109. PubMed: 18815359.