Inhibition of HCV Replication by Oxysterol-Binding Protein-Related Protein 4 (ORP4) through Interaction with HCV NS5B and Alteration of Lipid Droplet Formation

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Park, In Woo ^a,b   Ndjomou, Jean ^a,e   Wen, Yahong ^c   Liu, Ziqing ^a   Ridgway, Neale D ^d   Kao, C Cheng ^c   He, Johnny J ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^c INDIANA UNIVERSITY   (United States)

^d DALHOUSIE UNIVERSITY   (Canada)

^e UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FAT DROPLET; LIPID; LUCIFERASE; NONSTRUCTURAL PROTEIN 5B; OXYSTEROL BINDING PROTEIN RELATED PROTEIN 4; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIPID METABOLISM; LIPOGENESIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PATHOGENESIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; REPLICON; REPORTER GENE; VIRUS INHIBITION; VIRUS REPLICATION;

CELL LINE; GENE EXPRESSION; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; INTRACELLULAR SPACE; LIPID METABOLISM; LIPIDS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, STEROID; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84884217641     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075648     Document Type: Article

References (89)

1. Alter HJ, Seeff LB, (2000) Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin Liver Dis 20: 17-35. doi:10.1055/s-2000-9505. PubMed: 10895429.
2. Hoofnagle JH, (2002) Course and outcome of hepatitis C. Hepatology 36: S21-S29. doi:10.1053/jhep.2002.36227. PubMed: 12407573.
3. Miller RH, Purcell RH, (1990) Hepatitis C virus shares amino acid sequence similarity with pestiviruses and flaviviruses as well as members of two plant virus supergroups. Proc Natl Acad Sci U S A 87: 2057-2061. doi:10.1073/pnas.87.6.2057. PubMed: 2156259.
4. Friebe P, Bartenschlager R, (2002) Genetic analysis of sequences in the 3' nontranslated region of hepatitis C virus that are important for RNA replication. J Virol 76: 5326-5338. doi:10.1128/JVI.76.11.5326-5338.2002. PubMed: 11991961.
5. Yi M, Lemon SM, (2003) 3' nontranslated RNA signals required for replication of hepatitis C virus RNA. J Virol 77: 3557-3568. doi:10.1128/JVI.77.6.3557-3568.2003. PubMed: 12610131.
6. Bartenschlager R, Lohmann V, (2000) Replication of hepatitis C virus. J Gen Virol 81: 1631-1648. PubMed: 10859368.
7. Reed KE, Rice CM, (2000) Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr Top Microbiol Immunol 242: 55-84. doi:10.1007/978-3-642-59605-6_4. PubMed: 10592656.
8. Boyer JC, Haenni AL, (1994) Infectious transcripts and cDNA clones of RNA viruses. Virology 198: 415-426. doi:10.1006/viro.1994.1053. PubMed: 8291226.
9. Lee EG, Linial ML, (2000) Yeast three-hybrid screening of rous sarcoma virus mutants with randomly mutagenized minimal packaging signals reveals regions important for gag interactions. J Virol 74: 9167-9174. doi:10.1128/JVI.74.19.9167-9174.2000. PubMed: 10982363.
10. Strauss JH, Strauss EG, (1994) The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58: 491-562. PubMed: 7968923.
11. Wimmer E, Hellen CU, Cao X, (1993) Genetics of poliovirus. Annu Rev Genet 27: 353-436. doi:10.1146/annurev.ge.27.120193.002033. PubMed: 8122908.
12. Kolykhalov AA, Mihalik K, Feinstone SM, Rice CM, (2000) Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3' nontranslated region are essential for virus replication in vivo. J Virol 74: 2046-2051. doi:10.1128/JVI.74.4.2046-2051.2000. PubMed: 10644379.
13. Yanagi M, St Claire M, Emerson SU, Purcell RH, Bukh J, (1999) In vivo analysis of the 3' untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc Natl Acad Sci U S A 96: 2291-2295. doi:10.1073/pnas.96.5.2291. PubMed: 10051634.
14. Quadri R, Rubbia-Brandt L, Abid K, Negro F, (2001) Detection of the negative-strand hepatitis C virus RNA in tissues: implications for pathogenesis. Antiviral Res 52: 161-171. doi:10.1016/S0166-3542(01)00181-4. PubMed: 11672826.
15. Behrens SE, Tomei L, De Francesco R, (1996) Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J 15: 12-22. PubMed: 8598194.
16. Lohmann V, Körner F, Herian U, Bartenschlager R, (1997) Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J Virol 71: 8416-8428. PubMed: 9343198.
17. Chen YJ, Chen YH, Chow LP, Tsai YH, Chen PH, et al. (2010) Heat shock protein 72 is associated with the hepatitis C virus replicase complex and enhances viral RNA replication. J Biol Chem 285: 28183-28190. doi:10.1074/jbc.M110.118323. PubMed: 20601427.
18. Ito T, Lai MM, (1997) Determination of the secondary structure of and cellular protein binding to the 3'-untranslated region of the hepatitis C virus RNA genome. J Virol 71: 8698-8706. PubMed: 9343228.
19. Spångberg K, Goobar-Larsson L, Wahren-Herlenius M, Schwartz S, (1999) The La protein from human liver cells interacts specifically with the U-rich region in the hepatitis C virus 3' untranslated region. J Hum Virol 2: 296-307. PubMed: 10551736.
20. Spångberg K, Wiklund L, Schwartz S, (2001) Binding of the La autoantigen to the hepatitis C virus 3' untranslated region protects the RNA from rapid degradation in vitro. J Gen Virol 82: 113-120. PubMed: 11125164.
21. Petrik J, Parker H, Alexander GJ, (1999) Human hepatic glyceraldehyde-3-phosphate dehydrogenase binds to the poly(U) tract of the 3' non-coding region of hepatitis C virus genomic RNA. J Gen Virol 80(12):: 3109-3113. PubMed: 10567641.
22. Gontarek RR, Gutshall LL, Herold KM, Tsai J, Sathe GM, et al. (1999) hnRNP C and polypyrimidine tract-binding protein specifically interact with the pyrimidine-rich region within the 3'NTR of the HCV RNA genome. Nucleic Acids Res 27: 1457-1463. doi:10.1093/nar/27.6.1457. PubMed: 10037806.
23. Tsuchihara K, Tanaka T, Hijikata M, Kuge S, Toyoda H, et al. (1997) Specific interaction of polypyrimidine tract-binding protein with the extreme 3'-terminal structure of the hepatitis C virus genome, the 3'X. J Virol 71: 6720-6726. PubMed: 9261396.
24. Wood J, Frederickson RM, Fields S, Patel AH, (2001) Hepatitis C virus 3'X region interacts with human ribosomal proteins. J Virol 75: 1348-1358. doi:10.1128/JVI.75.3.1348-1358.2001. PubMed: 11152508.
25. Ngo MH, Colbourne TR, Ridgway ND, (2010) Functional implications of sterol transport by the oxysterol-binding protein gene family. Biochem J 429: 13-24. doi:10.1042/BJ20100263. PubMed: 20545625.
26. Huang Y, Chen XC, Konduri M, Fomina N, Lu J, et al. (2006) Mechanistic link between the anti-HCV effect of interferon gamma and control of viral replication by a Ras-MAPK signaling cascade. Hepatology 43: 81-90. doi:10.1002/hep.21011. PubMed: 16374867.
27. Kim JH, Paek KY, Choi K, Kim TD, Hahm B, et al. (2003) Heterogeneous nuclear ribonucleoprotein C modulates translation of c-myc mRNA in a cell cycle phase-dependent manner. Mol Cell Biol 23: 708-720. doi:10.1128/MCB.23.2.708-720.2003. PubMed: 12509468.
28. Henao-Mejia J, Liu Y, Park IW, Zhang J, Sanford J, et al. (2009) Suppression of HIV-1 Nef translation by Sam68 mutant-induced stress granules and nef mRNA sequestration. Mol Cell 33: 87-96. doi:10.1016/j.molcel.2008.11.024. PubMed: 19150430.
29. Ranjith-Kumar CT, Wen Y, Baxter N, Bhardwaj K, Cheng Kao C, (2011) A cell-based assay for RNA synthesis by the HCV polymerase reveals new insights on mechanism of polymerase inhibitors and modulation by NS5A. PLOS ONE 6: e22575. doi:10.1371/journal.pone.0022575. PubMed: 21799903.
30. Blight KJ, Kolykhalov AA, Rice CM, (2000) Efficient initiation of HCV RNA replication in cell culture. Science 290: 1972-1974. doi:10.1126/science.290.5498.1972. PubMed: 11110665.
31. Kapadia SB, Chisari FV, (2005) Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc Natl Acad Sci U S A 102: 2561-2566. doi:10.1073/pnas.0409834102. PubMed: 15699349.
32. Sagan SM, Rouleau Y, Leggiadro C, Supekova L, Schultz PG, et al. (2006) The influence of cholesterol and lipid metabolism on host cell structure and hepatitis C virus replication. Biochem Cell Biol 84: 67-79. doi:10.1139/o05-149. PubMed: 16462891.
33. Ye J, Wang C, Sumpter R Jr., Brown MS, Goldstein JL, et al. (2003) Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation. Proc Natl Acad Sci U S A 100: 15865-15870. doi:10.1073/pnas.2237238100. PubMed: 14668447.
34. Lagace TA, Byers DM, Cook HW, Ridgway ND, (1997) Altered regulation of cholesterol and cholesteryl ester synthesis in Chinese-hamster ovary cells overexpressing the oxysterol-binding protein is dependent on the pleckstrin homology domain. Biochem J 326(Pt. 1): 205-213 PubMed: 9337870.
35. Laitinen S, Lehto M, Lehtonen S, Hyvärinen K, Heino S, et al. (2002) ORP2, a homolog of oxysterol binding protein, regulates cellular cholesterol metabolism. J Lipid Res 43: 245-255. PubMed: 11861666.
36. Lehto M, Olkkonen VM, (2003) The OSBP-related proteins: a novel protein family involved in vesicle transport, cellular lipid metabolism, and cell signalling. Biochim Biophys Acta 1631: 1-11. doi:10.1016/S1388-1981(02)00364-5. PubMed: 12573443.
37. Olkkonen VM, (2004) Oxysterol binding protein and its homologues: new regulatory factors involved in lipid metabolism. Curr Opin Lipidol 15: 321-327. doi:10.1097/00041433-200406000-00013. PubMed: 15166789.
38. Wyles JP, Perry RJ, Ridgway ND, (2007) Characterization of the sterol-binding domain of oxysterol-binding protein (OSBP)-related protein 4 reveals a novel role in vimentin organization. Exp Cell Res 313: 1426-1437. doi:10.1016/j.yexcr.2007.01.018. PubMed: 17350617.
39. Wang C, JeBailey L, Ridgway ND, (2002) Oxysterol-binding-protein (OSBP)-related protein 4 binds 25-hydroxycholesterol and interacts with vimentin intermediate filaments. Biochem J 361: 461-472. doi:10.1042/0264-6021:3610461. PubMed: 11802775.
40. Wyles JP, McMaster CR, Ridgway ND, (2002) Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum. J Biol Chem 277: 29908-29918. doi:10.1074/jbc.M201191200. PubMed: 12023275.
41. Gao L, Aizaki H, He JW, Lai MM, (2004) Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft. J Virol 78: 3480-3488. doi:10.1128/JVI.78.7.3480-3488.2004. PubMed: 15016871.
42. Tu H, Gao L, Shi ST, Taylor DR, Yang T, et al. (1999) Hepatitis C virus RNA polymerase and NS5A complex with a SNARE-like protein. Virology 263: 30-41. doi:10.1006/viro.1999.9893. PubMed: 10544080.
43. Hamamoto I, Nishimura Y, Okamoto T, Aizaki H, Liu M, et al. (2005) Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B. J Virol 79: 13473-13482. doi:10.1128/JVI.79.21.13473-13482.2005. PubMed: 16227268.
44. Su AI, Pezacki JP, Wodicka L, Brideau AD, Supekova L, et al. (2002) Genomic analysis of the host response to hepatitis C virus infection. Proc Natl Acad Sci U S A 99: 15669-15674. doi:10.1073/pnas.202608199. PubMed: 12441396.
45. Raychaudhuri S, Prinz WA, (2010) The diverse functions of oxysterol-binding proteins. Annu Rev Cell Dev Biol 26: 157-177. doi:10.1146/annurev.cellbio.042308.113334. PubMed: 19575662.
46. Parrish NM, Kuhajda FP, Heine HS, Bishai WR, Dick JD, (1999) Antimycobacterial activity of cerulenin and its effects on lipid biosynthesis. J Antimicrob Chemother 43: 219-226. doi:10.1093/jac/43.2.219. PubMed: 11252327.
47. Nohturfft A, Yabe D, Goldstein JL, Brown MS, Espenshade PJ, (2000) Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes. Cell 102: 315-323. doi:10.1016/S0092-8674(00)00037-4. PubMed: 10975522.
48. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, et al. (1999) Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10: 961-974. doi:10.1091/mbc.10.4.961. PubMed: 10198050.
49. Yan D, Lehto M, Rasilainen L, Metso J, Ehnholm C, et al. (2007) Oxysterol binding protein induces upregulation of SREBP-1c and enhances hepatic lipogenesis. Arterioscler Thromb Vasc Biol 27: 1108-1114. doi:10.1161/ATVBAHA.106.138545. PubMed: 17303778.
50. Ferré P, Foufelle F, (2010) Hepatic steatosis: a role for de novo lipogenesis and the transcription factor SREBP-1c. Diabetes Obes Metab 12 (Suppl 2):: 83-92. doi:10.1111/j.1463-1326.2010.01275.x. PubMed: 21029304.
51. Tanner NK, Linder P, (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 8: 251-262. doi:10.1016/S1097-2765(01)00329-X. PubMed: 11545728.
52. Mamiya N, Worman HJ, (1999) Hepatitis C virus core protein binds to a DEAD box RNA helicase. J Biol Chem 274: 15751-15756. doi:10.1074/jbc.274.22.15751. PubMed: 10336476.
53. Owsianka AM, Patel AH, (1999) Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257: 330-340. doi:10.1006/viro.1999.9659. PubMed: 10329544.
54. Ariumi Y, Kuroki M, Abe K, Dansako H, Ikeda M, et al. (2007) DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol 81: 13922-13926. doi:10.1128/JVI.01517-07. PubMed: 17855521.
55. Goh PY, Tan YJ, Lim SP, Tan YH, Lim SG, et al. (2004) Cellular RNA helicase p68 relocalization and interaction with the hepatitis C virus (HCV) NS5B protein and the potential role of p68 in HCV RNA replication. J Virol 78: 5288-5298. doi:10.1128/JVI.78.10.5288-5298.2004. PubMed: 15113910.
56. Guinea R, Carrasco L, (1990) Phospholipid biosynthesis and poliovirus genome replication, two coupled phenomena. EMBO J 9: 2011-2016. PubMed: 2161336.
57. Tang H, Grisé H, (2009) Cellular and molecular biology of HCV infection and hepatitis. Clin Sci (Lond) 117: 49-65. doi:10.1042/CS20080631. PubMed: 19515018.
58. Egger D, Wölk B, Gosert R, Bianchi L, Blum HE, et al. (2002) Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76: 5974-5984. doi:10.1128/JVI.76.12.5974-5984.2002. PubMed: 12021330.
59. El-Hage N, Luo G, (2003) Replication of hepatitis C virus RNA occurs in a membrane-bound replication complex containing nonstructural viral proteins and RNA. J Gen Virol 84: 2761-2769. doi:10.1099/vir.0.19305-0. PubMed: 13679611.
60. Hügle T, Fehrmann F, Bieck E, Kohara M, Kräusslich HG, et al. (2001) The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 284: 70-81. doi:10.1006/viro.2001.0873. PubMed: 11352669.
61. Wölk B, Sansonno D, Kräusslich HG, Dammacco F, Rice CM, et al. (2000) Subcellular localization, stability, and trans-cleavage competence of the hepatitis C virus NS3-NS4A complex expressed in tetracycline-regulated cell lines. J Virol 74: 2293-2304. doi:10.1128/JVI.74.5.2293-2304.2000. PubMed: 10666260.
62. Miyanari Y, Hijikata M, Yamaji M, Hosaka M, Takahashi H, et al. (2003) Hepatitis C virus non-structural proteins in the probable membranous compartment function in viral genome replication. J Biol Chem 278: 50301-50308. doi:10.1074/jbc.M305684200. PubMed: 12963739.
63. Gosert R, Egger D, Lohmann V, Bartenschlager R, Blum HE, et al. (2003) Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J Virol 77: 5487-5492. doi:10.1128/JVI.77.9.5487-5492.2003. PubMed: 12692249.
64. Aizaki H, Lee KJ, Sung VM, Ishiko H, Lai MM, (2004) Characterization of the hepatitis C virus RNA replication complex associated with lipid rafts. Virology 324: 450-461. doi:10.1016/j.virol.2004.03.034. PubMed: 15207630.
65. Wyles JP, Ridgway ND, (2004) VAMP-associated protein-A regulates partitioning of oxysterol-binding protein-related protein-9 between the endoplasmic reticulum and Golgi apparatus. Exp Cell Res 297: 533-547. doi:10.1016/j.yexcr.2004.03.052. PubMed: 15212954.
66. Xu Y, Liu Y, Ridgway ND, McMaster CR, (2001) Novel members of the human oxysterol-binding protein family bind phospholipids and regulate vesicle transport. J Biol Chem 276: 18407-18414. doi:10.1074/jbc.M101204200. PubMed: 11279184.
67. Levine TP, Munro S, (2001) Dual Targeting of Osh1p, a Yeast Homologue of Oxysterol-binding Protein, to both the Golgi and the Nucleus-Vacuole Junction. Mol Biol Cell 12: 1633-1644. doi:10.1091/mbc.12.6.1633. PubMed: 11408574.
68. Levine TP, Munro S, (2002) Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and-independent components. Curr Biol 12: 695-704. doi:10.1016/S0959-440X(02)00403-7. PubMed: 12007412.
69. Yang W, Hood BL, Chadwick SL, Liu S, Watkins SC, et al. (2008) Fatty acid synthase is up-regulated during hepatitis C virus infection and regulates hepatitis C virus entry and production. Hepatology 48: 1396-1403. doi:10.1002/hep.22508. PubMed: 18830996.
70. Pietschmann T, Lohmann V, Kaul A, Krieger N, Rinck G, et al. (2002) Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J Virol 76: 4008-4021. doi:10.1128/JVI.76.8.4008-4021.2002. PubMed: 11907240.
71. Clouston AD, Powell EE, (2002) Interaction of non-alcoholic fatty liver disease with other liver diseases. Best Pract Res Clin Gastroenterol 16: 767-781. doi:10.1053/bega.2002.0329. PubMed: 12406444.
72. Shi ST, Lee KJ, Aizaki H, Hwang SB, Lai MM, (2003) Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J Virol 77: 4160-4168. doi:10.1128/JVI.77.7.4160-4168.2003. PubMed: 12634374.
73. Simons K, Ikonen E, (1997) Functional rafts in cell membranes. Nature 387: 569-572. doi:10.1038/42408. PubMed: 9177342.
74. Simons K, Ikonen E, (2000) How cells handle cholesterol. Science 290: 1721-1726. doi:10.1126/science.290.5497.1721. PubMed: 11099405.
75. Martin S, Parton RG, (2006) Lipid droplets: a unified view of a dynamic organelle. Nat Rev Mol Cell Biol 7: 373-378. doi:10.1038/nrg1836. PubMed: 16550215.
76. Barba G, Harper F, Harada T, Kohara M, Goulinet S, et al. (1997) Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A 94: 1200-1205. doi:10.1073/pnas.94.4.1200. PubMed: 9037030.
77. Hope RG, McLauchlan J, (2000) Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J Gen Virol 81: 1913-1925. PubMed: 10900028.
78. Lerat H, Honda M, Beard MR, Loesch K, Sun J, et al. (2002) Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis C virus. Gastroenterology 122: 352-365. doi:10.1053/gast.2002.31001. PubMed: 11832450.
79. Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, et al. (1997) Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J Gen Virol 78(Pt 7): 1527-1531 PubMed: 9225025.
80. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, et al. (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9: 1089-1097. doi:10.1038/ncb1631. PubMed: 17721513.
81. Ogawa K, Hishiki T, Shimizu Y, Funami K, Sugiyama K, et al. (2009) Hepatitis C virus utilizes lipid droplet for production of infectious virus. Proc Jpn Acad Ser B Phys Biol Sci 85. pp.: 217-228. PubMed: 19644222.
82. Goldstein JL, DeBose-Boyd RA, Brown MS, (2006) Protein sensors for membrane sterols. Cell 124: 35-46. doi:10.1016/j.cell.2005.12.022. PubMed: 16413480.
83. Mesmin B, Maxfield FR, (2009) Intracellular sterol dynamics. Biochim Biophys Acta 1791: 636-645. doi:10.1016/j.bbalip.2009.03.002. PubMed: 19286471.
84. Yang H, (2006) Nonvesicular sterol transport: two protein families and a sterol sensor? Trends Cell Biol 16: 427-432. doi:10.1016/j.tcb.2006.07.002. PubMed: 16876994.
85. Prinz WA, (2007) Non-vesicular sterol transport in cells. Prog Lipid Res 46: 297-314. doi:10.1016/j.plipres.2007.06.002. PubMed: 17709145.
86. Raychaudhuri S, Im YJ, Hurley JH, Prinz WA, (2006) Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J Cell Biol 173: 107-119. doi:10.1083/jcb.200510084. PubMed: 16585271.
87. Beller M, Sztalryd C, Southall N, Bell M, Jäckle H, et al. (2008) COPI complex is a regulator of lipid homeostasis. PLOS Biol 6: e292. doi:10.1371/journal.pbio.0060292. PubMed: 19067489.
88. Kuerschner L, Moessinger C, Thiele C, (2008) Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets. Traffic 9: 338-352. doi:10.1111/j.1600-0854.2007.00689.x. PubMed: 18088320.
89. Boström P, Andersson L, Rutberg M, Perman J, Lidberg U, et al. (2007) SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat Cell Biol 9: 1286-1293. doi:10.1038/ncb1648. PubMed: 17922004.