Box C/D small nucleolar RNA (snoRNA) U60 regulates intracellular cholesterol trafficking

Journal of Biological Chemistry

Volumn 288, Issue 50, 2013, Pages 35703-35713

  Brandis, Katrina A ^a   Gale, Sarah ^a   Jinn, Sarah ^a   Langmade, Stephen J ^a   Dudley Rucker, Nicole ^a   Jiang, Hui ^a   Sidhu, Rohini ^a   Ren, Aileen ^a   Goldberg, Anna ^a   Schaffer, Jean E ^a   Ory, Daniel S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR CHOLESTEROL; CHINESE HAMSTER OVARY CELLS; CHOLESTEROL HOMEOSTASIS; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; ENDOPLASMIC RETICULUM; INSERTIONAL MUTAGENESIS; INTRACELLULAR CHOLESTEROL;

ALKYLATION; CELL CULTURE; CELL MEMBRANES; GENES; PHYSIOLOGY; RNA;

CHOLESTEROL;

CHOLESTEROL; CHOLESTEROL ESTER; SMALL NUCLEOLAR RNA; SMALL NUCLEOLAR RNA U60; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MEMBRANE TRANSPORT; CELL MUTANT; CELL STRAIN; CELL STRAIN A1; CHO CELL; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENOTYPE; HAPLOINSUFFICIENCY; INTERNALIZATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; RNA METHYLATION;

CHOLESTEROL; CHOLESTEROL REGULATION; INTRACELLULAR TRAFFICKING; LIPID TRANSPORT; NONCODING RNA; SMALL NUCLEOLAR RNA (SNORNA);

AMPHOTERICIN B; ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CHO CELLS; CHOLESTEROL; CRICETINAE; CRICETULUS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC LOCI; HAPLOINSUFFICIENCY; HUMANS; INTRACELLULAR SPACE; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHATIDYLCHOLINES; RATS; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA, SMALL NUCLEOLAR;

EID: 84890327720     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.488577     Document Type: Article

References (41)

1. Kennedy, B. E., Charman, M., and Karten, B. (2012) Niemann-Pick Type C2 protein contributes to the transport of endosomal cholesterol to mitochondria without interacting with NPC1. J. Lipid Res. 53, 2632-2642
2. Underwood, K. W., Jacobs, N. L., Howley, A., and Liscum, L. (1998) Evidence for a cholesterol transport pathway from lysosomes to endoplasmic reticulum that is independent of the plasma membrane. J. Biol. Chem. 273, 4266-4274
3. Urano, Y., Watanabe, H., Murphy, S. R., Shibuya, Y., Geng, Y., Peden, A. A., Chang, C. C., and Chang, T. Y. (2008) Transport of LDL-derived cholesterol from the NPC1 compartment to the ER involves the trans-Golgi network and the SNARE protein complex. Proc. Natl. Acad. Sci. U.S.A. 105, 16513-16518
4. Lange, Y., Ye, J., Rigney, M., and Steck, T. L. (1999) Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J. Lipid Res. 40, 2264-2270
5. Chang, T. Y., Chang, C. C., Ohgami, N., and Yamauchi, Y. (2006) Cholesterol sensing, trafficking, and esterification. Annu. Rev. Cell Dev. Biol. 22, 129-157
6. Lange, Y., and Steck, T. L. (2008) Cholesterol homeostasis and the escape tendency (activity) of plasma membrane cholesterol. Prog. Lipid Res. 47, 319-332
7. Munn, N. J., Arnio, E., Liu, D., Zoeller, R. A., and Liscum, L. (2003) Deficiency in ethanolamine plasmalogen leads to altered cholesterol transport. J. Lipid Res. 44, 182-192
8. Yamauchi, Y., Reid, P. C., Sperry, J. B., Furukawa, K., Takeya, M., Chang, C. C., and Chang, T. Y. (2007) Plasma membrane rafts complete cholesterol synthesis by participating in retrograde movement of precursor sterols. J. Biol. Chem. 282, 34994-35004
9. Baumann, N. A., Sullivan, D. P., Ohvo-Rekilä, H., Simonot, C., Pottekat, A., Klaassen, Z., Beh, C. T., and Menon, A. K. (2005) Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration. Biochemistry 44, 5816-5826
10. Jansen, M., Ohsaki, Y., Rita Rega, L., Bittman, R., Olkkonen, V. M., and Ikonen, E. (2011) Role of ORPs in sterol transport from plasma membrane to ER and lipid droplets in mammalian cells. Traffic 12, 218-231
11. Mesmin, B., Pipalia, N. H., Lund, F. W., Ramlall, T. F., Sokolov, A., Eliezer, D., and Maxfield, F. R. (2011) STARD4 abundance regulates sterol transport and sensing. Mol. Biol. Cell 22, 4004-4015
12. Schulz, T. A., Choi, M. G., Raychaudhuri, S., Mears, J. A., Ghirlando, R., Hinshaw, J. E., and Prinz, W. A. (2009) Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J. Cell Biol. 187, 889-903
13. Dahl, N. K., Daunais, M. A., and Liscum, L. (1994) A second complementation class of cholesterol transport mutants with a variant Niemann-Pick type C phenotype. J. Lipid Res. 35, 1839-1849
14. Dahl, N. K., Reed, K. L., Daunais, M. A., Faust, J. R., and Liscum, L. (1992) Isolation and characterization of Chinese hamster ovary cells defective in the intracellular metabolism of low density lipoprotein-derived cholesterol. J. Biol. Chem. 267, 4889-4896
15. Jacobs, N. L., Andemariam, B., Underwood, K. W., Panchalingam, K., Sternberg, D., Kielian, M., and Liscum, L. (1997) Analysis of a Chinese hamster ovary cell mutant with defective mobilization of cholesterol from the plasma membrane to the endoplasmic reticulum. J. Lipid Res. 38, 1973-1987
16. Wojtanik, K. M., and Liscum, L. (2003) The transport of low density lipoprotein- derived cholesterol to the plasma membrane is defective in NPC1 cells. J. Biol. Chem. 278, 14850-14856
17. Gale, S. E., Westover, E. J., Dudley, N., Krishnan, K., Merlin, S., Scherrer, D. E., Han, X., Zhai, X., Brockman, H. L., Brown, R. E., Covey, D. F., Schaffer, J. E., Schlesinger, P., and Ory, D. S. (2009) Side chain oxygenated cholesterol regulates cellular cholesterol homeostasis through direct sterol- membrane interactions. J. Biol. Chem. 284, 1755-1764
18. Olsen, B. N., Schlesinger, P. H., Ory, D. S., and Baker, N. A. (2011) 25-Hydroxycholesterol increases the availability of cholesterol in phospholipid membranes. Biophys. J. 100, 948-956
19. Borradaile, N. M., Han, X., Harp, J. D., Gale, S. E., Ory, D. S., and Schaffer, J. E. (2006) Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 47, 2726-2737
20. Friedrich, G., and Soriano, P. (1991) Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5, 1513-1523
21. Lange, Y., Ory, D. S., Ye, J., Lanier, M. H., Hsu, F. F., and Steck, T. L. (2008) Effectors of rapid homeostatic responses of endoplasmic reticulum cholesterol and 3-hydroxy-3-methylglutaryl-CoA reductase. J. Biol. Chem. 283, 1445-1455
22. Hanson, P. I., Roth, R., Lin, Y., and Heuser, J. E. (2008) Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389-402
23. Sokolov, A., and Radhakrishnan, A. (2010) Accessibility of cholesterol in endoplasmic reticulum membranes and activation of SREBP-2 switch abruptly at a common cholesterol threshold. J. Biol. Chem. 285, 29480-29490
24. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
25. Fan, M., Sidhu, R., Fujiwara, H., Tortelli, B., Zhang, J., Davidson, C., Walkley, S. U., Bagel, J. H., Vite, C., Yanjanin, N. M., Porter, F. D., Schaffer, J. E., and Ory, D. S. (2013) Identification of Niemann-Pick C1 disease biomarkers through sphingolipid profiling. J. Lipid Res. 54, 2800-2814
26. Lewis, S. E., Listenberger, L. L., Ory, D. S., and Schaffer, J. E. (2001) Membrane topology of the murine fatty acid transport protein 1. J. Biol. Chem. 276, 37042-37050
27. Belin, S., Beghin, A., Solano-Gonzàlez, E., Bezin, L., Brunet-Manquat, S., Textoris, J., Prats, A. C., Mertani, H. C., Dumontet, C., and Diaz, J. J. (2009) Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS One 4, e7147
28. Millard, E. E., Srivastava, K., Traub, L. M., Schaffer, J. E., and Ory, D. S. (2000) Niemann-pick type C1 (NPC1) overexpression alters cellular cholesterol homeostasis. J. Biol. Chem. 275, 38445-38451
29. Olsen, B. N., Bielska, A. A., Lee, T., Daily, M. D., Covey, D. F., Schlesinger, P. H., Baker, N. A., and Ory, D. S. (2013) The structural basis of cholesterol accessibility in membranes. Biophys. J. 105, 1838-1847
30. Hirose, T., and Steitz, J. A. (2001) Position within the host intron is critical for efficient processing of box C/D snoRNAs in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 98, 12914-12919
31. Lowe, T. M., and Eddy, S. R. (1999) A computational screen for methylation guide snoRNAs in yeast. Science 283, 1168-1171
32. Lange, Y., Tabei, S. M., Ye, J., and Steck, T. L. (2013) Stability and stoichiometry of bilayer phospholipid-cholesterol complexes: Relationship to cellular sterol distribution and homeostasis. Biochemistry 52, 6950-6959
33. Michel, C. I., Holley, C. L., Scruggs, B. S., Sidhu, R., Brookheart, R. T., Listenberger, L. L., Behlke, M. A., Ory, D. S., and Schaffer, J. E. (2011) Small nucleolar RNAs U32a, U33, and U35a are critical mediators of metabolic stress. Cell Metab. 14, 33-44
34. Brameier, M., Herwig, A., Reinhardt, R., Walter, L., and Gruber, J. (2011) Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res. 39, 675-686
35. Kishore, S., Khanna, A., Zhang, Z., Hui, J., Balwierz, P. J., Stefan, M., Beach, C., Nicholls, R. D., Zavolan, M., and Stamm, S. (2010) The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum. Mol. Genet. 19, 1153-1164
36. Xia, J., Joyce, C. E., Bowcock, A. M., and Zhang, W. (2013) Noncanonical microRNAs and endogenous siRNAs in normal and psoriatic human skin. Hum. Mol. Genet. 22, 737-748
37. Marquart, T. J., Allen, R. M., Ory, D. S., and Baldán, A. (2010) miR-33 links SREBP-2 induction to repression of sterol transporters. Proc. Natl. Acad. Sci. U.S.A. 107, 12228-12232
38. Najafi-Shoushtari, S. H., Kristo, F., Li, Y., Shioda, T., Cohen, D. E., Gerszten, R. E., and Näär, A. M. (2010) MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328, 1566-1569
39. Rayner, K. J., Sheedy, F. J., Esau, C. C., Hussain, F. N., Temel, R. E., Parathath, S., van Gils, J. M., Rayner, A. J., Chang, A. N., Suarez, Y., Fernandez-Hernando, C., Fisher, E. A., and Moore, K. J. (2011) Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J. Clin. Invest. 121, 2921-2931
40. Reed, B. D., Charos, A. E., Szekely, A. M., Weissman, S. M., and Snyder, M. (2008) Genome-wide occupancy of SREBP1 and its partners NFY and SP1 reveals novel functional roles and combinatorial regulation of distinct classes of genes. PLoS Genet. 4, e1000133
41. Norlin, M., and Chiang, J. Y. (2004) Transcriptional regulation of human oxysterol 7α-hydroxylase by sterol response element binding protein. Biochem. Biophys. Res. Commun. 316, 158-164