Different subcellular localization of Saccharomyces cerevisiae HMG-CoA reductase isozymes at elevated levels corresponds to distinct endoplasmic reticulum membrane proliferations

Molecular Biology of the Cell

Volumn 7, Issue 5, 1996, Pages 769-789

  Koning, Ann J ^a   Roberts, Christopher J ^a   Wright, Robin L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CHIMERIC PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; PROTEIN; STEROL;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE; STEROL SYNTHESIS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0029926584     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.5.769     Document Type: Article

References (70)

1. Aitchison, J.D., Blobel, G., and Rout, M.P. (1995). Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport. J. Cell Biol. 131, 1659-1675.
2. Bachem, U., and Mendgen, K. (1995). Endoplasmic reticulum subcompartments in a plant parasitic fungus and in baker's yeast: differential distribution of lumenal proteins. Exp. Mycol. 19, 137-152.
3. Basson, M.E., Moore, R.L., O'Rear, J., and Rine, J. (1987). Identifying mutations in duplicated functions in Saccharomyces cerevisiae: recessive mutations in HMG-CoA reductase genes Genetics 117, 645-655.
4. Basson, M.E., Thorsness, M.K., Finer-Moore, J., Stroud, R., and Rine, J. (1988). Structural and functional conservation between yeast and human 3-hydroxy-3-methylglutaryl coenzyme A reductases, the rate-limiting enzyme of sterol biosynthesis. Mol. Cell. Biol. 9, 3797-3808.
5. Basson, M.L., Thorsness, M.K., and Rine, J. (1986). Saccharomyces cerevisiae contains two functional genes encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase. Proc. Natl. Acad. Sci. USA 83, 5563-5567.
6. Black, V.H. (1972). The development of smooth-surfaced endoplasmic reticulum in adrenal cortical cells of fetal guinea pigs. Am. J. Anat. 156, 318-418.
7. Byers, B., and Goetsch, L. (1991). Preparation of yeast cells for thin-section electron microscopy. Methods Enzymol. 194, 602-608.
8. Casey, W.M., Keesler, G.A., and Parks, L.W. (1992). Regulation of partitioned sterol biosynthesis in Saccharomyces cerevisiae. J. Bacteriol. 174, 7283-7288.
9. Ceriotti, A., and Colman, A. (1988). Binding to membrane proteins within the endoplasmic reticulum cannot explain the retention of the glucose-regulated protein GRP78 in Xenopus oocytes. EMBO J. 7, 622-638.
10. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W., and Prasher, D.C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
11. Chapman, R.E., and Munro, S. (1994). The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANP1, a member of a new family of genes affecting the secretory pathway. EMBO J. 33, 4896-4907.
12. Chin, D.J., Luskey, K.L., Anderson, R.G.W., Faust, J.R., Goldstein, J.L., and Brown, M.S. (1982). Appearance of crystalloid endoplasmic reticulum in compactin-resistant Chinese hamster cells with a 500-fold elevation in 3-hydroxy-3-methylglutaryl coenzyme A reductase. Proc. Natl. Acad. Sci. USA 79, 1185-1189.
13. Deschenes, R.J., and Broach, J.R. (1987). Fatty acylation is important but not essential for Saccharomyces cerevisiae RAS function. Mol. Cell Biol. 7, 2344-2351.
14. Deshaies, R.J., and Schekman, R. (1990). Structural and functional dissection of Sec62p, a membrane-bound component of the yeast endoplasmic reticulum protein import machinery. Mol. Cell Biol. 10, 6024-6035.
15. Esnault, Y., Blondel, M.-O., Deshaies, R.J., Schekman, R., and Kepes, F. (1993). The yeast SSS1 gene is essential for secretory protein translocation and encodes a conserved protein of the endoplasmic reticulum. EMBO J. 12, 4083-4093.
16. Fawcett, D.W. (1981). The Cell, 2nd ed., Philadelphia, PA: W.B. Saunders, 301-368.
17. Feldheim, D., Rothblatt, J., and Schekman, R. (1992). Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol. Cell Biol. 12, 3288-3296
18. Franzini-Armstrong, C., Kenney, L.J., and Varriano-Marston, E. (1987). The structure of calsequestrin in triads of vertebrate skeletal muscle: a deep-etch study. J. Cell Biol. 105, 49-56.
19. Fringes, B., and Gorgas, K. (1993). Crystalloid smooth endoplasmic reticulum in the quail uropygial gland. Ann. Anat. 175, 231-235.
20. Gaigg, B., Simbeni, R., Hrastnik, C., Paitauf, F., and Daum, G. (1995). Characterization of a microsomal subfraction associated with mitochondria of the yeast, Saccharomyces cerevisiae: involvement in synthesis and import of phospholipids into mitochondria. Biochim. Biophys. Acta 1234, 214-220
21. Galteau, M.M., Antoine, B., and Reggio, H. (1985). Epoxide hydrolase is a marker for the smooth endoplasmic reticulum in rat liver. EMBO J. 4, 2793-2800.
22. Gil, G., Faust, J.R., Chin, D.J., Goldstein, J.L., and Brown, M.S. (1985). Membrane-bound domain of HMG-CoA reductase is required for sterol-enhanced degradation of the enzyme. Cell 41, 249-258.
23. Goldstein, J.L , and Brown, M.S. (1990). Regulation of the mevalonate pathway. Nature 343, 425-430.
24. Guarente, L., and Mason, T. (1983). Heme regulates the transcription of the CYC1 gene of S. cerevisiae via an upstream activation site. Cell 32, 1279-1286.
25. Hamburger, D., Egerton, M., and Riezman, H. (1995). Yeast Gaa1p is required for attachment of a completed GPI anchor onto proteins. J. Cell Biol. 129, 629-639.
26. Hampton, R.Y., Koning, A., Wright, R., and Rine, J. (1996). In vivo examination of membrane protein localization and degradation with GFP. Proc. Natl. Acad. Sci. USA 93, 828-833.
27. Hampton, R.Y., and Rine, J. (1994). Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J. Cell Biol. 125, 299-312.
28. High, S., and Stirling, C.J. (1993). Protein translocation across membranes: common themes in divergent organisms. Trends Cell Biol. 3, 335-339.
29. +-ATPase complex. Mol. Biol. Cell 5, 1039-1050.
30. Jingami, H., Brown, M.S., Goldstein, J.L., Anderson, R.G.W., and Luskey, K.L. (1987). Partial deletion of membrane-bound domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase eliminates sterol-enhanced degradation and prevents formation of crystalloid endoplasmic reticulum. J. Cell Biol. 104, 1693-1704.
31. 6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil. Cytoskeleton 25, 111-128.
32. Laz, T.M., Pietras, D.F., and Sherman, F. (1984). Differential regulation of the duplicated iso-cytochrome c genes in yeast. Proc. Natl. Acad. Sci. USA 81, 4475-4479.
33. Li, O., Heath, C.V., Amberg, D.C., Dockendorff, T.C , Copeland, C.S., Snyder, M., and Cole, C.N. (1995). Mutation or deletion of the Saccharomyces cerevisiae RAT3/NUP133 gene causes temperature-dependent nuclear accumulation of poly(A)+ RNA and constitutive clustering of nuclear pore complexes. Mol. Biol. Cell 6, 410-417.
34. Lum, P.Y., and Wright, R. (1995). Degradation of HMG Co-A reductase-induced membranes in the fission yeast, Schizosaccharomyces pombe. J. Cell Biol. 131, 81-94.
35. Maniatis, T., Fritsch, E.F., and Sambrook, J (1982). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
36. Matile, P., Moor, H., and Robinow, C.F. (1969). The Yeasts. In: Yeast Cytology, vol. I, New York: Academic Press, 219-302.
37. Nishikawa, S., Hirata, A., and Nakano, A. (1994). Inhibition of endoplasmic reticulum (ER)-to-Golgi transport induces relocalization of binding protein (BiP) within the ER to form Bip bodies. Mol. Biol. Cell 5, 1129-1143.
38. Palade, G.E. (1975). Intracellular aspects of the process of protein synthesis. Science 189, 347-358.
39. Parlati, F., Dominguez, M., Bergeron, J J., and Thomas, D.Y. (1995). Saccharomyces cerevisiae CNE1 encodes an endoplasmic reticulum (ER) membrane protein with sequence similarity to calnexin and calreticulum and functions as a constituent of the ER quality control apparatus. J. Biol. Chem. 270, 244-253.
40. Parrish, M., Sengstag, C., Rine, J., and Wright, R. (1995) Identification of the sequences in HMG-CoA reductase required for karmellae assembly. Mol. Biol. Cell 6, 1535-1547.
41. Pathak, R.K , Luskey, K.L., and Anderson, R G W. (1986). Biogenesis of the crystalloid endoplasmic reticulum in UT-1 cells: evidence that newly formed endoplasmic reticulum emerges from the nuclear envelope. J. Cell Biol. 102, 2158-2168.
42. Prasher, D.C., Eckenrode, V.K., Ward, W.W., Prendergast, F.G., and Cormier, M.J. (1992). Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111, 229-233.
43. Preuss, D., Mulholland, J., Kaiser, C.A., Orlean, P., Albright, C., Rose, M.D., Robbins, P.W., and Botstein, D. (1991). Structure of the yeast endoplasmic reticulum: localization of ER proteins using immunofluorescence and immunoelectron microscopy. Yeast 7, 891-911.
44. Pringle, J.R., Preston, R.A., Adams, A.E.M., Stearns, T., Drubin, D.G., Haarer, B.K., and Jones, E.W. (1989). Fluorescence microscopy methods for yeast. Methods Cell Biol. 31, 357-435.
45. Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
46. Roitelman, J., and Simoni, R.D. (1992). Distinct sterol and nonsterol signals for the regulated degradation of 3-hydroxy-3-methylglutaryl-CoA reductase. J. Biol. Chem. 267, 25264-25273.
47. Rose, J.K., and Doms, R.W. (1988). Regulation of protein export from the endoplasmic reticulum. Annu. Rev. Cell Biol. 4, 257-288.
48. Rose, M.D., and Broach, J.R. (1991). Cloning genes by complementation in yeast. Methods Enzymol. 194, 195-230.
49. Rose, M.D., Mistra, L.M., and Vogel, J.P. (1989). KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57, 1211-1221.
50. Satoh, T., Ross, C.A., Villa, A., Supattapone, S., Pozzan, T., Snyder, S.H., and Meldolesi, J. (1990). The inositol 1,4,5-trisphosphate receptor in cerebellar Purkinje cells: quantitative immunogold labeling reveals concentration in an endoplasmic reticulum subcompartment. J Cell Biol. 111, 615-624.
51. Schlenstedt, G., Harris, S., Risse, B., Lill, R., and Silver, P.A. (1995). A yeast DnaJ homologue, Scjlp, can function in the endoplasmic reticulum with BiP/Kar2p via a conserved domain that specifies interactions with Hsp70s. J. Cell Biol. 129, 979-988.
52. Sengstag, C., Stirling, C., Schekman, R., and Rine, J. (1990). Genetic and biochemical evaluation of eukaryotic membrane protein topology: the polytopic structure of S. cerevisiae HMG-CoA reductase. Mol. Cell. Biol. 10, 672-680.
53. Sikorski, R.S., and Hieter, P. (1989). A uniform set of multipurpose shuttle vectors and yeast host strains designed for efficient manipulation of DNA in S. cerevisiae. Genetics 122, 19-27.
54. Singer, I.I., Scott, S., Kazizis, D.M., and Huff, J.W. (1988). Lovastatin, an inhibitor of cholesterol synthesis, induces hydroxymethylglutaryl-coenzyme A reductase directly on membranes of expanded smooth endoplasmic reticulum in rat hepatocytes. Proc. Natl. Acad. Sci. USA 85, 5264-5268.
55. Sisson, J.K., and Fahrenbach, W.H. (1967). Fine structure of steroidogenic cells of a primate cutaneous organ. Am. J. Anat. 121, 337-368.
56. Sitia, R., and Meldolesi, J. (1992). Endoplasmic reticulum: a dynamic patchwork of specialized subdomains. Mol. Biol. Cell 3, 1067-1072.
57. Skalnik, D.G., Narita, H., Kent, C., and Simoni, R.D. (1988). The membrane domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase confers endoplasmic reticulum localization and sterol-regulated degradation onto β-galactosidase. J. Biol. Chem. 263, 6836-6841.
58. Smith, S., and Blobel, G. (1993). The first membrane spanning region of the lamin B receptor is sufficient for sorting to the inner nuclear membrane. J. Cell Biol. 120, 631-637.
59. Strambio-de-Castillia, C., Blobel, G., and Rout, M.P. (1995). Isolation and characterization of nuclear envelopes from the yeast Saccharomyces. J. Cell Biol. 131, 19-31.
60. Tachibana, C., and Stevens, T.H. (1992). The yeast EUG1 gene encodes an endoplasmic reticulum protein that is functionally related to protein disulfide isomerase. Mol. Cell. Biol. 12, 4601-4611.
61. 2+-ATPase, and calsequestrin. J. Neurosci 12, 489-505.
62. Terasaki, M., Song, J., Wong, J.R., Weiss, M.J., and Chen, L.B. (1984). Localization of endoplasmic reticulum in living and glutaraldehyde-fixed cells with fluorescent dyes. Cell 38, 101-108.
63. Thorsness, M., Schafer, W., D'Ari, L.A., and Rine, J. (1989). Positive and negative transcriptional control by heme of genes encoding HMG-CoA reductase in Saccharomyces cerevisiae. Mol. Cell. Biol. 9, 5702-5712.
64. Trueblood, C.E., Wright, R.M., and Poyton, R.O. (1988) Differential regulation of the two genes encoding Saccharomyces cerevisiae cytochrome c oxidase subunit V by heme and the HAP2 and REO1 genes. Mol. Cell Biol. 8, 4537-4540.
65. Vertel, B.M., Walters, L.M., and Mills, D. (1992). Subcompartments of the endoplasmic reticulum. Semin. Cell Biol. 3, 325-341.
66. 2+ ATPase and of the ER lumenal protein, Bip. J. Cell Biol. 113, 779-791.
67. Wright, R., Basson, M., D'Ari, L., and Rine, J. (1988) Increased amounts of HMG-CoA reductase induce "karmellae": a proliferation of stacked membrane pairs surrounding the yeast nucleus. J. Cell Biol. 107, 101-114.
68. Wright, R., Keller, G , Gould, S.J., Subramani, S., and Rine, J. (1990). Cell-type control of membrane biogenesis induced by HMG-CoA reductase overproduction. New Biol. 2, 915-921.
69. Wright, R., and Rine, J. (1989). Transmission electron microscopy and immunocytochemical studies of yeast: analysis of HMG-CoA reductase overproduction by electron microscopy. Methods Cell Biol. 31, 473-512.
70. Yang, C.H., Lambie, E.J., Hardin, J., Craft, J., and Snyder, M. (1989). Higher order structure is present in the yeast nucleus: autoantibody probes demonstrate that the nucleolus lies opposite the spindle pole body. Chromosoma 98, 123-128.