Enteroviruses harness the cellular endocytic machinery to remodel the host cell cholesterol landscape for effective viral replication

Cell Host and Microbe

Volumn 14, Issue 3, 2013, Pages 281-293

  Ilnytska, Olha ^a   Santiana, Marianita ^a,e   Hsu, Nai Yun ^a   Du, Wen Li ^a,e   Chen, Ying Han ^a,e   Viktorova, Ekaterina G ^b   Belov, Georgy ^b   Brinker, Anita ^c   Storch, Judith ^c   Moore, Christopher ^d   Dixon, Joseph L ^c   Altan Bonnet, Nihal ^a,e  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d GLAXOSMITHKLINE   (United States)

^e NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN; CAVEOLIN 1; CAVEOLIN 2; CHOLESTEROL; CHOLESTEROL ESTER; CLATHRIN; VIRUS RNA;

ARTICLE; CELL MEMBRANE; CELL ORGANELLE; ENDOCYTOSIS; ENTEROVIRUS; HOMEOSTASIS; HOST CELL; LIFE CYCLE; NONHUMAN; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL; PROTEIN PROCESSING; RNA SYNTHESIS; VIRUS ENTRY; VIRUS REPLICATION;

ENTEROVIRUS; HARNESS; RNA VIRUSES;

CELL MEMBRANE; CHOLESTEROL; ENDOCYTOSIS; ENDOSOMES; ENTEROVIRUS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; VIRUS REPLICATION;

EID: 84883893843     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.08.002     Document Type: Article

References (65)

1. R. Andino, G.E. Rieckhof, and D. Baltimore A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA Cell 63 1990 369 380
2. E. Area-Gomez, M. Del Carmen Lara Castillo, M.D. Tambini, C. Guardia-Laguarta, A.J. de Groof, M. Madra, J. Ikenouchi, M. Umeda, T.D. Bird, S.L. Sturley, and E.A. Schon Upregulated function of mitochondria-associated ER membranes in Alzheimer disease EMBO J. 31 2012 4106 4123
3. D.J. Barton, and J.B. Flanegan Coupled translation and replication of poliovirus RNA in vitro: synthesis of functional 3D polymerase and infectious virus J. Virol. 67 1993 822 831
4. G.A. Belov, V. Nair, B.T. Hansen, F.H. Hoyt, E.R. Fischer, and E. Ehrenfeld Complex dynamic development of poliovirus membranous replication complexes J. Virol. 86 2012 302 312
5. S. Bopegamage, J. Kovacova, A. Vargova, J. Motusova, A. Petrovicova, M. Benkovicova, P. Gomolcak, J. Bakkers, F. van Kuppeveld, W.J. Melchers, and J.M. Galama Coxsackie B virus infection of mice: inoculation by the oral route protects the pancreas from damage, but not from infection J. Gen. Virol. 86 2005 3271 3280
6. M.S. Bretscher, and S. Munro Cholesterol and the Golgi apparatus Science 261 1993 1280 1281
7. M.S. Brown, and J.L. Goldstein A receptor-mediated pathway for cholesterol homeostasis Science 232 1986 34 47
8. M.S. Brown, and J.L. Goldstein The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor Cell 89 1997 331 340
9. M.S. Brown, and J.L. Goldstein Sterol regulatory element binding proteins (SREBPs): controllers of lipid synthesis and cellular uptake Nutr. Rev. 56 1998 S1 S3 discussion S54-S75
10. E.Y. Bryleva, M.A. Rogers, C.C. Chang, F. Buen, B.T. Harris, E. Rousselet, N.G. Seidah, S. Oddo, F.M. LaFerla, and T.A. Spencer ACAT1 gene ablation increases 24(S)-hydroxycholesterol content in the brain and ameliorates amyloid pathology in mice with AD Proc. Natl. Acad. Sci. USA 107 2010 3081 3086
11. A.E. Campbell, R.M. Loria, G.E. Madge, and A.M. Kaplan Dietary hepatic cholesterol elevation: effects on coxsackievirus B infection and inflammation Infect. Immun. 37 1982 307 317
12. A.M. Cataldo, C.M. Peterhoff, J.C. Troncoso, T. Gomez-Isla, B.T. Hyman, and R.A. Nixon Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations Am. J. Pathol. 157 2000 277 286
13. T.Y. Chang, and C. Chang Ezetimibe blocks internalization of the NPC1L1/cholesterol complex Cell Metab. 7 2008 469 471
14. T.Y. Chang, C.C. Chang, E. Bryleva, M.A. Rogers, and S.R. Murphy Neuronal cholesterol esterification by ACAT1 in Alzheimer's disease IUBMB Life 62 2010 261 267
15. A.W. Cohen, B. Razani, W. Schubert, T.M. Williams, X.B. Wang, P. Iyengar, D.L. Brasaemle, P.E. Scherer, and M.P. Lisanti Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation Diabetes 53 2004 1261 1270
16. C.T. Cornell, and B.L. Semler Subdomain specific functions of the RNA polymerase region of poliovirus 3CD polypeptide Virology 298 2002 200 213
17. C.T. Cornell, W.B. Kiosses, S. Harkins, and J.L. Whitton Inhibition of protein trafficking by coxsackievirus b3: multiple viral proteins target a single organelle J. Virol. 80 2006 6637 6647
18. S.B. Deitz, D.A. Dodd, S. Cooper, P. Parham, and K. Kirkegaard MHC I-dependent antigen presentation is inhibited by poliovirus protein 3A Proc. Natl. Acad. Sci. USA 97 2000 13790 13795
19. J.A. den Boon, and P. Ahlquist Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories Annu. Rev. Microbiol. 64 2010 241 256
20. D. Dutta, and J.G. Donaldson Search for inhibitors of endocytosis: Intended specificity and unintended consequences Cell. Logist. 2 2012 203 208
21. A.R. English, and G.K. Voeltz Endoplasmic reticulum structure and interconnections with other organelles Cold Spring Harb. Perspect. Biol. 5 2013 a013227
22. D. Franco, H.B. Pathak, C.E. Cameron, B. Rombaut, E. Wimmer, and A.V. Paul Stimulation of poliovirus RNA synthesis and virus maturation in a HeLa cell-free in vitro translation-RNA replication system by viral protein 3CDpro Virol. J. 2 2005 86
23. Y. Fu, A. Hoang, G. Escher, R.G. Parton, Z. Krozowski, and D. Sviridov Expression of caveolin-1 enhances cholesterol efflux in hepatic cells J. Biol. Chem. 279 2004 14140 14146
24. A.L. Greninger, G.M. Knudsen, M. Betegon, A.L. Burlingame, and J.L. Derisi The 3A protein from multiple picornaviruses utilizes the golgi adaptor protein ACBD3 to recruit PI4KIIIβ J. Virol. 86 2012 3605 3616
25. M.G. Gustafsson, L. Shao, P.M. Carlton, C.J. Wang, I.N. Golubovskaya, W.Z. Cande, D.A. Agard, and J.W. Sedat Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination Biophys. J. 94 2008 4957 4970
26. M. Hölttä-Vuori, R.L. Uronen, J. Repakova, E. Salonen, I. Vattulainen, P. Panula, Z. Li, R. Bittman, and E. Ikonen BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms Traffic 9 2008 1839 1849
27. M.T. Howes, S. Mayor, and R.G. Parton Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis Curr. Opin. Cell Biol. 22 2010 519 527
28. K. Hsieh, Y.K. Lee, C. Londos, B.M. Raaka, K.T. Dalen, and A.R. Kimmel Perilipin family members preferentially sequester to either triacylglycerol- specific or cholesteryl-ester-specific intracellular lipid storage droplets J. Cell Sci. 125 2012 4067 4076
29. T.H. Hsu, and K.R. Spindler Identifying host factors that regulate viral infection PLoS Pathog. 8 2012 e1002772 10.1371/journal.ppat.1002772
30. N.Y. Hsu, O. Ilnytska, G. Belov, M. Santiana, Y.H. Chen, P.M. Takvorian, C. Pau, H. van der Schaar, N. Kaushik-Basu, and T. Balla Viral reorganization of the secretory pathway generates distinct organelles for RNA replication Cell 141 2010 799 811
31. E. Ikonen Cellular cholesterol trafficking and compartmentalization Nat. Rev. Mol. Cell Biol. 9 2008 125 138
32. A. Iwasaki, R. Welker, S. Mueller, M. Linehan, A. Nomoto, and E. Wimmer Immunofluorescence analysis of poliovirus receptor expression in Peyer's patches of humans, primates, and CD155 transgenic mice: implications for poliovirus infection J. Infect. Dis. 186 2002 585 592
33. M. Jansen, Y. Ohsaki, L. Rita Rega, R. Bittman, V.M. Olkkonen, and E. Ikonen Role of ORPs in sterol transport from plasma membrane to ER and lipid droplets in mammalian cells Traffic 12 2011 218 231
34. L. Jia, J.L. Betters, and L. Yu Niemann-pick C1-like 1 (NPC1L1) protein in intestinal and hepatic cholesterol transport Annu. Rev. Physiol. 73 2011 239 259
35. J.M. Karasinska, and M.R. Hayden Cholesterol metabolism in Huntington disease Nat. Rev. Neurol. 7 2011 561 572
36. Z.A. Knight, B. Gonzalez, M.E. Feldman, E.R. Zunder, D.D. Goldenberg, O. Williams, R. Loewith, D. Stokoe, A. Balla, and B. Toth A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling Cell 125 2006 733 747
37. J.J. Krukemyer, and R.L. Talbert Lovastatin: a new cholesterol-lowering agent Pharmacotherapy 7 1987 198 210
38. Y. Lange, F. Strebel, and T.L. Steck Role of the plasma membrane in cholesterol esterification in rat hepatoma cells J. Biol. Chem. 268 1993 13838 13843
39. Y. Lange, J. Ye, M. Rigney, and T.L. Steck Dynamics of lysosomal cholesterol in Niemann-Pick type C and normal human fibroblasts J. Lipid Res. 43 2002 198 204
40. X. Li, and M. DiFiglia The recycling endosome and its role in neurological disorders Prog. Neurobiol. 97 2012 127 141
41. J. Lippincott-Schwartz, and R.D. Phair Lipids and cholesterol as regulators of traffic in the endomembrane system Annu. Rev. Biophys. 39 2010 559 578
42. E. Macia, M. Ehrlich, R. Massol, E. Boucrot, C. Brunner, and T. Kirchhausen Dynasore, a cell-permeable inhibitor of dynamin Dev. Cell 10 2006 839 850
43. J.M. Mackenzie, A.A. Khromykh, and R.G. Parton Cholesterol manipulation by West Nile virus perturbs the cellular immune response Cell Host Microbe 2 2007 229 239
44. M. Martinez-Vicente, Z. Talloczy, E. Wong, G. Tang, H. Koga, S. Kaushik, R. de Vries, E. Arias, S. Harris, D. Sulzer, and A.M. Cuervo Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease Nat. Neurosci. 13 2010 567 576
45. F.R. Maxfield, and D. Wüstner Intracellular cholesterol transport J. Clin. Invest. 110 2002 891 898
46. M.A. McCloskey, and M.M. Poo Rates of membrane-associated reactions: reduction of dimensionality revisited J. Cell Biol. 102 1986 88 96
47. J. Mercer, M. Schelhaas, and A. Helenius Virus entry by endocytosis Annu. Rev. Biochem. 79 2010 803 833
48. S. Miller, and J. Krijnse-Locker Modification of intracellular membrane structures for virus replication Nat. Rev. Microbiol. 6 2008 363 374
49. A. Molla, K.S. Harris, A.V. Paul, S.H. Shin, J. Mugavero, and E. Wimmer Stimulation of poliovirus proteinase 3Cpro-related proteolysis by the genome-linked protein VPg and its precursor 3AB J. Biol. Chem. 269 1994 27015 27020
50. B.J. Nichols, A.K. Kenworthy, R.S. Polishchuk, R. Lodge, T.H. Roberts, K. Hirschberg, R.D. Phair, and J. Lippincott-Schwartz Rapid cycling of lipid raft markers between the cell surface and Golgi complex J. Cell Biol. 153 2001 529 541
51. R.G. Parton, and M.A. del Pozo Caveolae as plasma membrane sensors, protectors and organizers Nat. Rev. Mol. Cell Biol. 14 2013 98 112
52. A.V. Paul, C.F. Yang, S.K. Jang, R.J. Kuhn, H. Tada, M. Nicklin, H.G. Kräusslich, C.K. Lee, and E. Wimmer Molecular events leading to poliovirus genome replication Cold Spring Harb. Symp. Quant. Biol. 52 1987 343 352
53. W.A. Prinz A bridge to understanding lipid droplet growth Dev. Cell 24 2013 335 336
54. A.I. Rosenbaum, and F.R. Maxfield Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches J. Neurochem. 116 2011 789 795
55. R.K. Rowe, J.W. Suszko, and A. Pekosz Roles for the recycling endosome, Rab8, and Rab11 in hantavirus release from epithelial cells Virology 382 2008 239 249
56. J. Sasaki, K. Ishikawa, M. Arita, and K. Taniguchi ACBD3-mediated recruitment of PI4KB to picornavirus RNA replication sites EMBO J. 31 2012 754 766
57. K. Simons, and J.L. Sampaio Membrane organization and lipid rafts Cold Spring Harb. Perspect. Biol. 3 2011 a004697
58. S. Treusch, S. Hamamichi, J.L. Goodman, K.E. Matlack, C.Y. Chung, V. Baru, J.M. Shulman, A. Parrado, B.J. Bevis, and J.S. Valastyan Functional links between Aβ toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast Science 334 2011 1241 1245
59. E. Trushina, R.D. Singh, R.B. Dyer, S. Cao, V.H. Shah, R.G. Parton, R.E. Pagano, and C.T. McMurray Mutant huntingtin inhibits clathrin-independent endocytosis and causes accumulation of cholesterol in vitro and in vivo Hum. Mol. Genet. 15 2006 3578 3591
60. E.M. van Dam, and W. Stoorvogel Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles Mol. Biol. Cell 13 2002 169 182
61. J. Velier, M. Kim, C. Schwarz, T.W. Kim, E. Sapp, K. Chase, N. Aronin, and M. DiFiglia Wild-type and mutant huntingtins function in vesicle trafficking in the secretory and endocytic pathways Exp. Neurol. 152 1998 34 40
62. L.J. Wang, and B.L. Song Niemann-Pick C1-Like 1 and cholesterol uptake Biochim. Biophys. Acta 1821 2012 964 972
63. D.E. Warnock, C. Roberts, M.S. Lutz, W.A. Blackburn, W.W. Young Jr., and J.U. Baenziger Determination of plasma membrane lipid mass and composition in cultured Chinese hamster ovary cells using high gradient magnetic affinity chromatography J. Biol. Chem. 268 1993 10145 10153
64. E. Wessels, D. Duijsings, T.K. Niu, S. Neumann, V.M. Oorschot, F. de Lange, K.H. Lanke, J. Klumperman, A. Henke, and C.L. Jackson A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1 Dev. Cell 11 2006 191 201
65. V. Zhendre, A. Grélard, M. Garnier-Lhomme, S. Buchoux, B. Larijani, and E.J. Dufourc Key role of polyphosphoinositides in dynamics of fusogenic nuclear membrane vesicles PLoS ONE 6 2011 e23859 10.1371/journal.pone. 0023859