Host sphingomyelin increases West Nile virus infection in vivo

Journal of Lipid Research

Volumn 57, Issue 3, 2016, Pages 422-432

  Martín Acebes, Miguel A ^a,c   Gabandé Rodríguez, Enrique ^b,e   García Cabrero, Ana M ^d,f   Sánchez, Marina P ^d   Ledesma, María Dolores ^b   Sobrino, Francisco ^a   Saiz, Juan Carlos ^c  

^a Department of Virology and Microbiology and Molecular Neurobiology ^*  (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^c INIA   (Spain)

^d INSTITUTO DE INVESTIGACIÓN SANITARIA DEL HOSPITAL CLÍNICO SAN CARLOS IDISSC   (Spain)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^f CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Brain lipids; Flavivirus; Lipids; Niemann Pick disease; Sphingolipids; Storage diseases

Indexed keywords

SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE EXACERBATION; ENDOPLASMIC RETICULUM MEMBRANE; EX VIVO STUDY; FEMALE; HIPPOCAMPAL SLICE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MORTALITY; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; SKIN FIBROBLAST; SPHINGOLIPID METABOLISM; VIRUS REPLICATION; WEST NILE FEVER; ANIMAL; BRAIN; C57BL MOUSE; DEFICIENCY; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE INACTIVATION; GENETICS; HOST PATHOGEN INTERACTION; INTRACELLULAR MEMBRANE; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY; WEST NILE VIRUS;

ANIMALS; BRAIN; ENDOPLASMIC RETICULUM; FEMALE; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; MALE; MICE; MICE, INBRED C57BL; NIEMANN-PICK DISEASES; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELINS; VIRUS REPLICATION; WEST NILE VIRUS;

EID: 84964325536     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M064212     Document Type: Article

References (57)

1. Gould , E. A. , and T. Solomon . 2008 . Pathogenic flaviviruses. Lancet . 371 : 500 - 509 .
2. Martín-Acebes , M. A. , and J. C. Saiz . 2012 . West Nile virus: a re-emerging pathogen revisited. World J. Virol. 1 : 51 - 70 .
3. Gillespie , L. K. , A. Hoenen , G. Morgan , and J. M. Mackenzie . 2010 . The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 84 : 10438 - 10447 .
4. Apte-Sengupta , S. , D. Sirohi , and R. J. Kuhn . 2014 . Coupling of replication and assembly in flaviviruses. Curr. Opin. Virol. 9 : 134 - 142 .
5. Martín-Acebes , M. A. , A. B. Blá?zquez , N. Jiménez de Oya , E. Escribano-Romero , and J. C. Saiz . 2011 . West Nile virus replication requires fatty acid synthesis but is independent on phosphatidylinositol-4-phosphate lipids. PLoS One . 6 : e24970 .
6. Welsch , S. , S. Miller , I. Romero-Brey , A. Merz , C. K. Bleck , P. Walther , S. D. Fuller , C. Antony , J. Krijnse-Locker , and R. Bartenschlager . 2009 . Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe . 5 : 365 - 375 .
7. Mackenzie , J. M. , A. A. Khromykh , and R. G. Parton . 2007 . Cholesterol manipulation by West Nile virus perturbs the cellular immune response. Cell Host Microbe . 2 : 229 - 239 .
8. Martín-Acebes , M. A. , T. Merino-Ramos , A. B. Blá?zquez , J. Casas , E. Escribano-Romero , F. Sobrino , and J. C. Saiz . 2014 . The composition of West Nile virus lipid envelope unveils a role of sphingolipid metabolism in flavivirus biogenesis. J. Virol. 88 : 12041 - 12054 .
9. Aktepe , T. E. , H. Pham , and J. M. Mackenzie . 2015 . Differential utilisation of ceramide during replication of the flaviviruses West Nile and dengue virus. Virology . 484 : 241 - 250 .
10. Heaton , N. S. , R. Perera , K. L. Berger , S. Khadka , D. J. Lacount , R. J. Kuhn , and G. Randall . 2010 . Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. Proc. Natl. Acad. Sci. USA . 107 : 17345 - 17350 .
11. Heaton , N. S. , and G. Randall . 2010 . Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe . 8 : 422 - 432 .
12. Perera , R. , C. Riley , G. Isaac , A. S. Hopf-Jannasch , R. J. Moore , K. W. Weitz , L. Pasa-Tolic , T. O. Metz , J. Adamec , and R. J. Kuhn . 2012 . Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLoS Pathog. 8 : e1002584 .
13. Holthuis , J. C. , T. Pomorski , R. J. Raggers , H. Sprong , and G. Van Meer . 2001 . The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81 : 1689 - 1723 .
14. Ceccaldi , P. E. , M. Lucas , and P. Despres . 2004 . New insights on the neuropathology of West Nile virus. FEMS Microbiol. Lett. 233 : 1 - 6 .
15. Gault , C. R. , L. M. Obeid , and Y. A. Hannun . 2010 . An overview of sphingolipid metabolism: from synthesis to breakdown. Adv. Exp. Med. Biol. 688 : 1 - 23 .
16. Lorizate , M. , and H. G. Krausslich . 2011 . Role of lipids in virus replication. Cold Spring Harb. Perspect. Biol. 3 : a004820 .
17. Schneider-Schaulies , J. , and S. Schneider-Schaulies . 2015 . Sphingolipids in viral infection. Biol. Chem. 396 : 585 - 595 .
18. Chukkapalli , V. , N. S. Heaton , and G. Randall . 2012 . Lipids at the interface of virus-host interactions. Curr. Opin. Microbiol. 15 : 512 - 518 .
19. Hirata , Y. , K. Ikeda , M. Sudoh , Y. Tokunaga , A. Suzuki , L. Weng , M. Ohta , Y. Tobita , K. Okano , K. Ozeki , et al . 2012 . Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis. PLoS Pathog. 8 : e1002860 .
20. Brady , R. O. , J. N. Kanfer , M. B. Mock , and D. S. Fredrickson . 1966 . The metabolism of sphingomyelin. II. Evidence of an enzymatic deficiency in Niemann-Pick disease. Proc. Natl. Acad. Sci. USA . 55 : 366 - 369 .
21. Horinouchi , K. , S. Erlich , D. P. Perl , K. Ferlinz , C. L. Bisgaier , K. Sandhoff , R. J. Desnick , C. L. Stewart , and E. H. Schuchman . 1995 . Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10 : 288 - 293 .
22. Ledesma , M. D. , A. Prinetti , S. Sonnino , and E. H. Schuchman . 2011 . Brain pathology in Niemann-Pick disease type A: insights from the acid sphingomyelinase knockout mice. J. Neurochem. 116 : 779 - 788 .
23. Galvan , C. , P. G. Camoletto , F. Cristofani , P. P. Van Veldhoven , and M. D. Ledesma . 2008 . Anomalous surface distribution of glycosyl phosphatidyl inositol-anchored proteins in neurons lacking acid sphingomyelinase. Mol. Biol. Cell . 19 : 509 - 522 .
24. Rodriguez-Lafrasse , C. , and M. T. Vanier . 1999 . Sphingosylphosphorylcholine in Niemann-Pick disease brain: accumulation in type A but not in type B. Neurochem. Res. 24 : 199 - 205 .
25. Ng , C. G. , and D. E. Griffin . 2006 . Acid sphingomyelinase deficiency increases susceptibility to fatal alphavirus encephalomyelitis. J. Virol. 80 : 10989 - 10999 .
26. Ng , C. G. , I. Coppens , D. Govindarajan , J. Pisciotta , V. Shulaev , and D. E. Griffin . 2008 . Effect of host cell lipid metabolism on alphavirus replication, virion morphogenesis, and infectivity. Proc. Natl. Acad. Sci. USA . 105 : 16326 - 16331 .
27. Merino-Ramos , T. , A. B. Blazquez , E. Escribano-Romero , R. Canas-Arranz , F. Sobrino , J. C. Saiz , and M. A. Martin-Acebes . 2014 . Protection of a single dose West Nile virus recombinant subviral particle vaccine against lineage 1 or 2 strains and analysis of the cross-reactivity with Usutu virus. PLoS One . 9 : e108056 .
28. Martín-Acebes , M. A. , and J. C. Saiz . 2011 . A West Nile virus mutant with increased resistance to acid-induced inactivation. J. Gen. Virol. 92 : 831 - 840 .
29. Gabandé-Rodríguez , E. , P. Boya , V. Labrador , C. G. Dotti , and M. D. Ledesma . 2014 . High sphingomyelin levels induce lysosomal damage and autophagy dysfunction in Niemann-Pick disease type A. Cell Death Differ. 21 : 864 - 875 .
30. Jurado-Arjona , J. , P. Goni-Oliver , L. Rodriguez-Prada , T. Engel , D. C. Henshall , J. Avila , and F. Hernandez . 2015 . Excitotoxicity induced by kainic acid provokes glycogen synthase kinase-3 truncation in the hippocampus. Brain Res. 1611 : 84 - 92 .
31. Hojjati , M. R. , and X. C. Jiang . 2006 . Rapid, specific, and sensitive measurements of plasma sphingomyelin and phosphatidylcholine. J. Lipid Res. 47 : 673 - 676 .
32. Makino , A. , M. Abe , M. Murate , T. Inaba , N. Yilmaz , F. Hullin-Matsuda , T. Kishimoto , N. L. Schieber , T. Taguchi , H. Arai , et al . 2015 . Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis. FASEB J. 29 : 477 - 493 .
33. Wölk , B. , B. Büchele , D. Moradpour , and C. M. Rice . 2008 . A dynamic view of hepatitis C virus replication complexes. J. Virol. 82 : 10519 - 10531 .
34. Lanciotti , R. S. , A. J. Kerst , R. S. Nasci , M. S. Godsey , C. J. Mitchell , H. M. Savage , N. Komar , N. A. Panella , B. C. Allen , K. E. Volpe , et al . 2000 . Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J. Clin. Microbiol. 38 : 4066 - 4071 .
35. Blá?zquez , A. B. , and J. C. Sá?iz . 2010 . West Nile virus (WNV) transmission routes in the murine model: intrauterine, by breastfeeding and after cannibal ingestion. Virus Res. 151 : 240 - 243 .
36. Scandroglio , F. , J. K. Venkata , N. Loberto , S. Prioni , E. H. Schuchman , V. Chigorno , A. Prinetti , and S. Sonnino . 2008 . Lipid content of brain, brain membrane lipid domains, and neurons from acid sphingomyelinase deficient mice. J. Neurochem. 107 : 329 - 338 .
37. Lanciotti , R. S. , J. T. Roehrig , V. Deubel , J. Smith , M. Parker , K. Steele , B. Crise , K. E. Volpe , M. B. Crabtree , J. H. Scherret , et al . 1999 . Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science . 286 : 2333 - 2337 .
38. Hunsperger , E. A. , and J. T. Roehrig . 2006 . Temporal analyses of the neuropathogenesis of a West Nile virus infection in mice. J. Neurovirol. 12 : 129 - 139 .
39. Donadieu , E. , S. Lowenski , J. L. Servely , E. Laloy , T. Lilin , N. Nowotny , J. Richardson , S. Zientara , S. Lecollinet , and M. Coulpier . 2013 . Comparison of the neuropathology induced by two West Nile virus strains. PLoS One . 8 : e84473 .
40. Hoover , L. I. , and B. L. Fredericksen . 2014 . IFN-dependent and -independent reduction in West Nile virus infectivity in human dermal fibroblasts. Viruses . 6 : 1424 - 1441 .
41. Kiyokawa , E. , A. Makino , K. Ishii , N. Otsuka , A. Yamaji-Hasegawa , and T. Kobayashi . 2004 . Recognition of sphingomyelin by lysenin and lysenin-related proteins. Biochemistry . 43 : 9766 - 9773 .
42. Kiyokawa E. , BabaT. , OtsukaN. , MakinoA. , OhnoS. ,T. Kobayashi2005 . Spatial and functional heterogeneity of sphingolipid-rich membrane domainsJ. Biol. Chem.280 : 24072-24084
43. Delgado , A. , J. Casas , A. Llebaria , J. L. Abad , and G. Fabrias . 2006 . Inhibitors of sphingolipid metabolism enzymes. Biochim. Biophys. Acta . 1758 : 1957 - 1977 .
44. Adibhatla , R. M. , J. F. Hatcher , and A. Gusain . 2012 . Tricyclodecan-9-yl-xanthogenate (D609) mechanism of actions: a mini-review of literature. Neurochem. Res. 37 : 671 - 679 .
45. Li , Z. , T. K. Hailemariam , H. Zhou , Y. Li , D. C. Duckworth , D. A. Peake , Y. Zhang , M. S. Kuo , G. Cao , and X. C. Jiang . 2007 . Inhibition of sphingomyelin synthase (SMS) affects intracellular sphingomyelin accumulation and plasma membrane lipid organization. Biochim. Biophys. Acta . 1771 : 1186 - 1194 .
46. Larsen , E. C. , J. F. Hatcher , and R. M. Adibhatla . 2007 . Effect of tricyclodecan-9-yl potassium xanthate (D609) on phospholipid metabolism and cell death during oxygen-glucose deprivation in PC12 cells. Neuroscience . 146 : 946 - 961 .
47. Robert , J. 2004 . MS-209 Schering. Curr. Opin. Investig. Drugs . 5 : 1340 - 1347 .
48. Vá?zquez-Calvo , A. , J. C. Saiz , F. Sobrino , and M. A. Martín-Acebes . 2011 . Inhibition of enveloped virus infection of cultured cells by valproic acid. J. Virol. 85 : 1267 - 1274 .
49. Greseth , M. D. , and P. Traktman . 2014 . De novo fatty acid biosynthesis contributes significantly to establishment of a bioenergetically favorable environment for vaccinia virus infection. PLoS Pathog. 10 : e1004021 .
50. Merino-Ramos , T. , A. Vazquez-Calvo , J. Casas , F. Sobrino , J. C. Saiz , and M. A. Martin-Acebes . 2015 . Modification of the host cell lipid metabolism induced by hypolipidemic drugs targeting the acetyl coenzyme A carboxylase impairs West Nile virus replication. Antimicrob. Agents Chemother. 60 : 307 - 315 .
51. den Boon , J. A. , and P. Ahlquist . 2010 . Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64 : 241 - 256 .
52. Belov , G. A. , and F. J. van Kuppeveld . 2012 . (+)RNA viruses rewire cellular pathways to build replication organelles. Curr. Opin. Virol. 2 : 740 - 747 .
53. Shrestha , B. , D. Gottlieb , and M. S. Diamond . 2003 . Infection and injury of neurons by West Nile encephalitis virus. J. Virol. 77 : 13203 - 13213 .
54. Weng L. , HirataY. , AraiM. , KoharaM. , WakitaT. , WatashiK. , ShimotohnoK. , HeY. , ZhongJ. ,T. Toyoda2010 . Sphingomyelin activates hepatitis C virus RNA polymerase in a genotype-specific mannerJ. Virol.84 : 11761-11770
55. Sakamoto , H. , K. Okamoto , M. Aoki , H. Kato , A. Katsume , A. Ohta , T. Tsukuda , N. Shimma , Y. Aoki , M. Arisawa , et al . 2005 . Host sphingolipid biosynthesis as a target for hepatitis C virus therapy. Nat. Chem. Biol. 1 : 333 - 337 .
56. Katsume , A. , Y. Tokunaga , Y. Hirata , T. Munakata , M. Saito , H. Hayashi , K. Okamoto , Y. Ohmori , I. Kusanagi , S. Fujiwara , et al . 2013 . A serine palmitoyltransferase inhibitor blocks hepatitis C virus replication in human hepatocytes. Gastroenterology . 145 : 865 - 873 .
57. AmemiyaF. MaekawaS. ItakuraY. KanayamaA. MatsuiA. TakanoS. YamaguchiT. ItakuraJ. KitamuraT. InoueT.et al.2008Targeting lipid metabolism in the treatment of hepatitis C virus infectionJ. Infect. Dis.197361-370