Sterol-dependent nuclear import of ORP1S promotes LXR regulated trans-activation of apoE

Experimental Cell Research

Volumn 318, Issue 16, 2012, Pages 2128-2142

  Lee, Sungsoo ^a   Wang, Ping Yuan ^a,c   Jeong, Yangsik ^a,b,d   Mangelsdorf, David J ^a,b   Anderson, Richard G W ^a   Michaely, Peter ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

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

^d Yonsei University Wonju   (South Korea)

Author keywords

LXR; NLS; Nuclear import; ORP1; ORP1S; Oxysterol

Indexed keywords

BINDING PROTEIN; LIVER X RECEPTOR; OXYSTEROL BINDING PROTEIN RELATED PROTEIN 1S; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; ENHANCER REGION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RECEPTOR BINDING; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; TRANSACTIVATION;

EID: 84864301367     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.06.012     Document Type: Article

References (62)

1. Vihervaara T., Jansen M., Uronen R.L., Ohsaki Y., Ikonen E., Olkkonen V.M. Cytoplasmic oxysterol-binding proteins: sterol sensors or transporters?. Chem. Phys. Lipids 2011, 164:443-450.
2. Wang C., JeBailey L., Ridgway N.D. Oxysterol-binding-protein (OSBP)-related protein 4 binds 25-hydroxycholesterol and interacts with vimentin intermediate filaments. Biochem. J. 2002, 361:461-472.
3. Suchanek M., Hynynen R., Wohlfahrt G., Lehto M., Johansson M., Saarinen H., Radzikowska A., Thiele C., Olkkonen V. The mammalian oxysterol-binding protein-related proteins (ORPs) bind 25-hydroxycholesterol in an evolutionarily conserved pocket. Biochem. J. 2007, 405:473-480.
4. Yan D., Jauhiainen M., Hildebrand R., Willems van Dijk K., Van Berkel T., Ehnholm C., Van Eck M., Olkkonen V. Expression of human OSBP-related protein 1L in macrophages enhances atherosclerotic lesion development in LDL receptor-deficient mice. Arterioscler Thromb. Vasc. Biol. 2007, 27:1618-1624.
5. Yan D., Mayranpaa M.I., Wong J., Perttila J., Lehto M., Jauhiainen M., Kovanen P.T., Ehnholm C., Brown A.J., Olkkonen V.M. OSBP-related protein 8 (ORP8) suppresses ABCA1 expression and cholesterol efflux from macrophages. J. Biol. Chem. 2008, 283:332-340.
6. Wang P.-Y., Weng J., Lee S., Anderson R.G.W. The N terminus controls sterol binding while the C terminus regulates the scaffolding function of OSB. J. Biol. Chem. 2008, 283:8034-8045.
7. Hynynen R., Suchanek M., Spandl J., Back N., Thiele C., Olkkonen V.M. OSBP-related protein 2 is a sterol receptor on lipid droplets that regulates the metabolism of neutral lipids. J. Lipid Res. 2009, 50:1305-1315.
8. Ngo M., Ridgway N.D. Oxysterol binding protein-related protein 9 (ORP9) is a cholesterol transfer protein that regulates golgi structure and function. Mol. Biol. Cell 2009, 20:1388-1399.
9. Im Y.J., Raychaudhuri S., Prinz W.A., Hurley J.H. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 2005, 437:154-158.
10. Beh C.T., Rine J. A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J. Cell Sci. 2004, 117:2983-2996.
11. Beh C.T., Alfaro G., Duamel G., Sullivan D.P., Kersting M.C., Dighe S., Kozminski K.G., Menon A.K. Yeast oxysterol-binding proteins: sterol transporters or regulators of cell polarization?. Mol. Cell Biochem. 2009, 326:9-13.
12. Raychaudhuri S., Im Y., Hurley J., Prinz W. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J. Cell Biol. 2006, 173:107-119.
13. Sullivan D.P., Ohvo-Rekila H., Baumann N.A., Beh C.T., Menon A.K. Sterol trafficking between the endoplasmic reticulum and plasma membrane in yeast. Biochem. Soc. Trans. 2006, 34:356-358.
14. Du X., Kumar J., Ferguson C., Schulz T.A., Ong Y.S., Hong W., Prinz W.A., Parton R.G., Brown A.J., Yang H. A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J. Cell Biol. 2011, 192:121-135.
15. Jansen M., Ohsaki Y., Rita Rega L., Bittman R., Olkkonen V., Ikonen E. Role of ORPs in sterol transport from plasma membrane to ER and lipid droplets in mammalian cells. Traffic 2010.
16. Ridgway N.D., Dawson P.A., Ho Y.K., Brown M.S., Goldstein J.L. Translocation of oxysterol binding protein to Golgi apparatus triggered by ligand binding. J. Cell Biol. 1992, 116:307-319.
17. Vihervaara T., Uronen R., Wohlfahrt G., Bjorkhem I., Ikonen E., Olkkonen V. Sterol binding by OSBP-related protein 1L regulates late endosome motility and function. Cell. Mol. Life Sci. 2011, 68:537-551.
18. Johansson M., Bocher V., Lehto M., Chinetti G., Kuismanen E., Ehnholm C., Staels B., Olkkonen V. The two variants of oxysterol binding protein-related protein-1 display different tissue expression patterns, have different intracellular localization, and are functionally distinct. Mol. Biol. Cell 2003, 14:903-915.
19. Laitinen S., Olkkonen V.M., Ehnholm C., Ikonen E. Family of human oxysterol binding protein (OSBP) homologues. A novel member implicated in brain sterol metabolism. J. Lipid Res. 1999, 40:2204-2211.
20. Johansson M., Lehto M., Tanhuanpaa K., Cover T.L., Olkkonen V.M. The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol. Biol. Cell 2005, 16:5480-5492.
21. Johansson M., Rocha N., Zwart W., Jordens I., Janssen L., Kuijl C., Olkkonen V., Neefjes J. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol. 2007, 176:459-471.
22. Xu Y., Liu Y., Ridgway N.D., McMaster C.R. Novel members of the human oxysterol-binding protein family bind phospholipids and regulate vesicle transport. J. Biol. Chem. 2001, 276:18407-18414.
23. Willy P., Umesono K., Ong E., Evans R., Heyman R., Mangelsdorf D. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 1995, 9:1033-1045.
24. Apfel R., Benbrook D., Lernhardt E., Ortiz M.A., Salbert G., Pfahl M. A novel orphan receptor specific for a subset of thyroid hormone-responsive elements and its interaction with the retinoid/thyroid hormone receptor subfamily. Mol. Cell Biol. 1994, 14:7025-7035.
25. Song C., Kokontis J.M., Hiipakka R.A., Liao S. Ubiquitous receptor: a receptor that modulates gene activation by retinoic acid and thyroid hormone receptors. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:10809-10813.
26. Edwards P.A., Kennedy M.A., Mak P.A. LXRs; oxysterol-activated nuclear receptors that regulate genes controlling lipid homeostasis. Vascul. Pharmacol. 2002, 38:249-256.
27. Hong C., Tontonoz P. Coordination of inflammation and metabolism by PPAR and LXR nuclear receptors. Curr. Opin. Genet. Dev. 2008, 18:461-467.
28. Budhu A., Noy N. Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest. Mol. Cell Biol. 2002, 22:2632-2641.
29. Tan N., Shaw N., Vinckenbosch N., Liu P., Yasmin R., Desvergne B., Wahli W., Noy N. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol. Cell Biol. 2002, 22:5114-5127.
30. Paik Y., Chang D., Reardon C., Walker M., Taxman E., Taylor J. Identification and characterization of transcriptional regulatory regions associated with expression of the human apolipoprotein E gene. J. Biol. Chem. 1988, 263:13340-13349.
31. Laffitte B., Repa J., Joseph S., Wilpitz D., Kast H., Mangelsdorf D., Tontonoz P. LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:507-512.
32. Jakobsson T., Venteclef N., Toresson G., Damdimopoulos A., Ehrlund A., Lou X., Sanyal S., Steffensen K., Gustafsson J., Treuter E. GPS2 is required for cholesterol efflux by triggering histone demethylation, LXR recruitment, and coregulator assembly at the ABCG1 locus. Mol. Cell 2009, 34:510-518.
33. Dignam J., Lebovitz R., Roeder R. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
34. Kurokawa R., Soderstrom M., Horlein A., Halachmi S., Brown M., Rosenfeld M.G., Glass C.K. Polarity-specific activities of retinoic acid receptors determined by a co-repressor. Nature 1995, 377:451-454.
35. Zehmer J., Bartz R., Liu P., Anderson R. Identification of a novel N-terminal hydrophobic sequence that targets proteins to lipid droplets. J. Cell Sci. 2008, 121:1852-1860.
36. Dyer B., Ferrer F., Klinedinst D., Rodriguez R. A noncommercial dual luciferase enzyme assay system for reporter gene analysis. Anal. Biochem. 2000, 282:158-161.
37. Janowski B.A., Willy P.J., Devi T.R., Falck J.R., Mangelsdorf D.J. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 1996, 383:728-731.
38. Shih S., Allan C., Grehan S., Tse E., Moran C., Taylor J. Duplicated downstream enhancers control expression of the human apolipoprotein E gene in macrophages and adipose tissue. J. Biol. Chem. 2000, 275:31567-31572.
39. Perry R.J., Ridgway N.D. Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein. Mol. Biol. Cell 2006, 17:2604-2616.
40. Lagace T.A., Byers D.M., Cook H.W., Ridgway N.D. Chinese hamster ovary cells overexpressing the oxysterol binding protein (OSBP) display enhanced synthesis of sphingomyelin in response to 25-hydroxycholesterol. J. Lipid Res. 1999, 40:109-116.
41. Feldherr C.M., Akin D. The location of the transport gate in the nuclear pore complex. J. Cell Sci. 1997, 110:3065-3070.
42. Keminer O., Peters R. Permeability of single nuclear pores. Biophys. J. 1999, 77:217-228.
43. Goldfarb D.S., Gariepy J., Schoolnik G., Kornberg R.D. Synthetic peptides as nuclear localization signals. Nature 1986, 322:641-644.
44. Dingwall C., Robbins J., Dilworth S.M., Roberts B., Richardson W.D. The nucleoplasmin nuclear location sequence is larger and more complex than that of SV-40 large T antigen. J. Cell Biol. 1988, 107:841-849.
45. Rajendra Kumar P., Singhal P.K., Vinod S.S., Mahalingam S. A non-canonical transferable signal mediates nuclear import of simian immunodeficiency virus Vpx protein. J. Mol. Biol. 2003, 331:1141-1156.
46. Sessler R., Noy N. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol. Cell 2005, 18:343-353.
47. Lehto M., Hynynen R., Karjalainen K., Kuismanen E., Hyvarinen K., Olkkonen V.M. Targeting of OSBP-related protein 3 (ORP3) to endoplasmic reticulum and plasma membrane is controlled by multiple determinants. Exp. Cell Res. 2005, 310:445-462.
48. Jaworski C.J., Moreira E., Li A., Lee R., Rodriguez I.R. A family of 12 human genes containing oxysterol-binding domains. Genomics 2001, 78:185-196.
49. Peet D.J., Janowski B.A., Mangelsdorf D.J. The LXRs: a new class of oxysterol receptors. Curr. Opin. Genet. Dev. 1998, 8:571-575.
50. Mukherjee S., Ghosh R.N., Maxfield F.R. Endocytosis. Physiol. Rev. 1997, 77:759-803.
51. Prinz W.A. Non-vesicular sterol transport in cells. Prog. Lipid Res. 2007, 46:297-314.
52. Grehan S., Tse E., Taylor J. Two distal downstream enhancers direct expression of the human apolipoprotein E gene to astrocytes in the brain. J. Neurosci. 2001, 21:812-822.
53. Simonet W., Bucay N., Lauer S., Taylor J. A far-downstream hepatocyte-specific control region directs expression of the linked human apolipoprotein E and C-I genes in transgenic mice. J. Biol. Chem. 1993, 268:8221-8229.
54. Pfrieger F.W. Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes?. Bioessays 2003, 25:72-78.
55. Dietschy J.M., Turley S.D. Thematic review series: brain lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J. Lipid Res. 2004, 45:1375-1397.
56. Abildayeva K., Jansen P.J., Hirsch-Reinshagen V., Bloks V.W., Bakker A.H.F., Ramaekers F.C.S., de Vente J., Groen A.K., Wellington C.L., Kuipers F., Mulder M. 24(S)-hydroxycholesterol participates in a liver X receptor-controlled pathway in astrocytes that regulates apolipoprotein E-mediated cholesterol efflux. J. Biol. Chem. 2006, 281:12799-12808.
57. N. Wang, L. Yvan-Charvet, D. Lutjohann, M. Mulder, T. Vanmierlo, T.-W. Kim, A.R. Tall, ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain, FASEB J. (2007) fj.07-9944com.
58. Bachoo R., Kim R., Ligon K., Maher E., Brennan C., Billings N., Chan S., Li C., Rowitch D., Wong W., DePinho R. Molecular diversity of astrocytes with implications for neurological disorders. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8384-8389.
59. Shafaati M., Olin M., Bavner A., Pettersson H., Rozell B., Meaney S., Parini P., Bjorkhem I. Enhanced production of 24S-hydroxycholesterol is not sufficient to drive liver X receptor target genes in vivo. J. Intern Med. 2011, 270:377-387.
60. Heverin M., Bogdanovic N., Lutjohann D., Bayer T., Pikuleva I., Bretillon L., Diczfalusy U., Winblad B., Bjorkhem I. Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer's disease. J. Lipid Res. 2004, 45:186-193.
61. Fu X., Menke J.G., Chen Y., Zhou G., MacNaul K.L., Wright S.D., Sparrow C.P., Lund E.G. 27-Hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J. Biol. Chem. 2001, 276:38378-38387.
62. Kotti T.J., Ramirez D.M., Pfeiffer B.E., Huber K.M., Russell D.W. Brain cholesterol turnover required for geranylgeraniol production and learning in mice. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3869-3874.