Experientia

, Volume 46, Issue 6, pp 599–611 | Cite as

Intracellular sterol trafficking

  • M. P. Reinhart
Article

Summary

Sterols are acquired by cells either biosynthetically by the interaction of cytoplasmic and endoplasmic reticulum elements, or by endocytosis. The subcellular distribution of sterols, however, argues that sterols are trafficked quickly from sites of acquisition to target membranes, particularly the plasma membrane. The mechanisms mediating this movement might include aqueous diffusion, vesicles of either a unique pathway or of the protein secretory pathway, or carrier proteins. These mechanisms are discussed and the limited data concerning each are presented. Finally, a theory is proposed which describes how sterols and other membrane reinforcing molecules might have driven the evolution of intracellular membranes, thus establishing the dynamic membrane system of modern eukaryotes.

Key words

Sterol synthesis cholesterol plasma membrane endoplasmic reticulum sterol carrier proteins bacteriohopanes 

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Literatur

  1. 1.
    Amar-Costesec, A., Wibo, M., Thines-Sempoux, D., Beaufay, H., and Berthet, J., Analytical study of microsomes and isolated subcellular membranes from rat liver IV. Biochemical, physical, and morphological modifications of microsomal components induced by digitonin, EDTA, and pyrophosphate. J. Cell Biol.62 (1974) 717–745.Google Scholar
  2. 2.
    Appelkvist, E. L., In vitro labeling of peroxisomal cholesterol with radioactive precursors. Biosci. Rep.7 (1987) 853–858.Google Scholar
  3. 3.
    Basu, J., Kundu, M., Bhattacharya, U., Mazumder, C., and Chakrabarti, P., Purification and characterisation of a nonspecific lipid transfer protein from goat liver. Biochim. biophys. Acta959 (1988) 134–142.Google Scholar
  4. 4.
    Behnke, A., Tranum-Jensen, J., and Van Deurs, B., Filipin as a cholesterol probe. II. Filipin-cholesterol interaction in red blood cell membranes. Eur. J. Cell Biol.35 (1984) 200–215.Google Scholar
  5. 5.
    Billheimer, J. T., and Gaylor, J. L., Cytosolic modulators of activities of microsomal enzymes of cholesterol biosynthesis. J. biol. Chem.255 (1980) 8128–8135.Google Scholar
  6. 6.
    Billheimer, J. T., Landrey, J. R., and Conner, R. L., The presence of Acyl-CoA:cholesterol acyltransferase inTetrahymena pyriformis W. Comp. Biochem. Physiol.92B (1989) 675–680.Google Scholar
  7. 7.
    Billheimer, J. T., Strehl, L. L., Davis, G. L., Strauss, J. F. III, and Davis, L. G., Characterization of a cDNA clone encoding rat sterol carrier protein 2. DNA, in press.Google Scholar
  8. 8.
    Bisseret, P., Wolff, G., Albrecht, A. M., Tanaka, T., Nakatani, Y., and Ourrison, G., A direct study of the cohesion of lecithin bilayers: the effect of hopanoids and α,w-dihydroxycarotenoids. Biochem. biophys. Res. Commun.110 (1983) 320–324.Google Scholar
  9. 9.
    Blanchette-Mackie, E. J., Dwyer, N. K., Amende, L. M., Kruth, M. S., Butter, J. D., Sokol, J., Comly, M. E., Vanier, M. T., August, J. T., Brady, R. O., and Pentchev, P. G., Type-C Niemann-Pick disease: low density lipoprotein uptake is associated with premature cholesterol accumulation in the Golgi complex and excessive cholesterol storage in lysosomes. Proc. natl Acad. Sci. USA85 (1988) 8022–8026.Google Scholar
  10. 10.
    Bloj, B., and Zilversmit, D. B., Rat liver proteins capable of transferring phosphatidylethanolamine. Purification and transfer activity for other phospholipids and cholesterol. J. biol. Chem.252 (1977) 1613–1619.Google Scholar
  11. 11.
    Bloj, B., and Zilversmit, D. B., Complete exchangeability of cholesterol in phosphatidylcholine/cholesterol vesicles of different degrees of unsaturation. Biochemistry16 (1977) 3943–3948.Google Scholar
  12. 12.
    Bloj, B., and Zilversmit, D. B., Accelerated transfer of neutral glycosphingolipids and ganglioside G by a purified lipid transfer protein. J. biol. Chem.256 (1981) 5988–5991.Google Scholar
  13. 13.
    Bloom, M., and Mouritsen, O. G., The evolution of membranes. Can. J. Chem.66 (1988) 706–712.Google Scholar
  14. 14.
    Blouin, A., Bolender, R. P., and Weibel, E. R., Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. J. Cell Biol.72 (1977) 441–455.Google Scholar
  15. 15.
    Brasaemle, D. L., Robertson, A. D., and Attie, A. D., Transbilayer movement of cholesterol in the human erythrocyte membrane. J. Lipid. Res.29 (1988) 481–489.Google Scholar
  16. 16.
    Brown, M. S., and Goldstein, J. L., A receptor-mediated pathway for cholesterol homeostasis. Science232 (1986) 34–47.Google Scholar
  17. 17.
    Cavalier-Smith, T., in: Molecular and Cellular Aspects of Macrobial Evolution, pp. 33–84. Society for General Microbiology Ltd., Symposium 32. Eds M. J. Carlile, J. F. Collins and B. E. B. Moseley. Cambridge University Press 1981.Google Scholar
  18. 18.
    Chanderbhan, R., Noland, B. J., Scallen, T. J., and Vahouny, G. V., Sterol carrier protein 2, delivery of cholesterol from adrenal lipid droplets to mitochondria for pregnenolone synthesis. J. biol. Chem.257 (1982) 8928–8934.Google Scholar
  19. 19.
    Chanderbhan, R., Tanaka, T., Strauss, J. F., Irwin, D., Noland, B. J., Scallen, T. J., and Vahouny, G. V., Evidence for sterol carrier protein 2-like activity in hepatic, adrenal and ovarian cytosol. Biochem. biophys. Res. Commun.117 (1983) 702–709.Google Scholar
  20. 20.
    Chanderbhan, R. F., Kharroubi, A. T., Noland, B. J., Scallen, T. J., and Vahouny, G. V., Sterol carrier protein 2; Further evidence for its role in adrenal steroidogenesis. Endocr. Res.12 (1986) 351–370.Google Scholar
  21. 21.
    Chesterton, C. J., Distribution of cholesterol precursors and other lipids among rat liver intracellular structures: evidence for the endoplasmic reticulum as the site of cholesterol and cholesterol ester synthesis. J. biol. Chem.243 (1968) 1147–1151.Google Scholar
  22. 22.
    Chin, D. J., Luskey, K. L., Anderson, R. G. W., Faust, J. R., Goldstein, J. L., and Brown, M. S., Appearance of crystalloid endoplasmic reticulum in compactin-resistant Chinese hamster cells with a 500-fold increase in 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proc. natl Acad. Sci. USA79 (1982) 1185–1189.Google Scholar
  23. 23.
    Colbeau, A., Nachbaur, J., and Vignais, P. M., Enzymic characterization and lipid composition of rat liver subcellular membranes. Biochim. biophys. Acta249 (1971) 462–492.Google Scholar
  24. 24.
    Coleman, R., and Finean, J. B., Preparation and properties of isolated plasma membranes from guinea pig tissues. Biochim. biophys. Acta125 (1966) 197–206.Google Scholar
  25. 25.
    Comte, J., Maisterrena, B., and Gautheron, D. C., Lipid composition and protein profiles of outer and inner membranes from pig heart mitochondria-comparison with microsomes. Biochim. biophys. Acta419 (1976) 271–284.Google Scholar
  26. 26.
    Crain, R. C., and Zilversmit, D. B., Two nonspecific phospholipid exchange proteins from beef liver. 1. Purification and characterization. Biochemistry19 (1980) 1433–1439.Google Scholar
  27. 27.
    De Cock, H., Meeldijk, J., Overduin, P., Verkleij, A. J., and Tommassen, J., Membrane biogenesis inEscherichia coli: effects of a secA mutation. Biochim. biophys. Acta985 (1989) 313–319.Google Scholar
  28. 28.
    DeGrella, R. F., and Simoni, R. D., Intracellular transport of cholesterol to the plasma membrane. J. biol. Chem.257 (1982) 14 256–14 262.Google Scholar
  29. 29.
    Demel, R. A., Louwers, H., Jackson, R. L., and Wirtz, K. W. A., Protein-mediated lipid transfer between monolayers and bilayers. Coll. Surf.10 (1984) 301–311.Google Scholar
  30. 30.
    Dempsey, M. E., Hargis, P. S., McGuire, D. M., McMahon, A., Olson, C. D., Salati, L. M., Clarke, S. D., and Towle, H. C., Role of sterol carrier protein in cholesterol metabolism. Chem. Phys. Lipids38 (1985) 223–237.Google Scholar
  31. 31.
    DeSilva, N. S., and Siu, C.-H., Vesicle-mediated transfer of phospholipids to plasma membrane during cell aggregation ofDictyostelium discoideum. J. biol. Chem.256 (1981) 5845–5850.Google Scholar
  32. 32.
    Engleman, D. M., and Steitz, T. A., The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell23 (1981) 411–422.Google Scholar
  33. 33.
    Ferguson, J. B., and Bloch, K., Purification and properties of a soluble protein activator of rat liver squalene epoxidase. J. biol. Chem.252 (1977) 5381–5385.Google Scholar
  34. 34.
    Flesch, G., and Rohmer, M., Growth inhibition of hopane synthesizing bacteria by squalene cyclase inhibitors. Archs Microbiol.147 (1987) 100–104.Google Scholar
  35. 35.
    Fuks-Holmberg, D., and Bloch, K., Intermembrane transfer of squalene promoted by supernatant protein factor. J. Lipid Res.24 (1983) 402–408.Google Scholar
  36. 36.
    Gavey, K. L., and Scallen, T. J., Studies on the conversion of enzymatically generated microsome-bound squalene to sterol. J. biol. Chem.253 (1978) 5476–5483.Google Scholar
  37. 37.
    Gordon, J. I., Alpers, D. H., Ockner, R. K., and Strauss, A. W., The nucleotide sequence of rat liver fatty acid binding protein mRNA. J. biol. Chem.258 (1983) 3356–3363.Google Scholar
  38. 38.
    Gotlib, L. J., and Searls, D. B., Plasma membrane isolation on DEAE-sephadex beads. Biochim. biophys. Acta602 (1980) 207–212.Google Scholar
  39. 39.
    Gottlieb, M. H., The reactivity of human erythrocyte membrane cholesterol with a cholesterol oxidase. Biochim. biophys. Acta466 (1977) 422–428.Google Scholar
  40. 40.
    Green, C., The movement of cholesterol within cells, in: Sterol biosynthesis and Function. Eds K. E. Suckling and B. C. Baldwin. Biochem. Soc. Trans.11 (1983) 637–639.Google Scholar
  41. 41.
    Habig, W. H., Pabst, M. J., Fleischner, G., Gatmaitan, Z., Arias, I. M., and Jakoby, W. B., The identity of glutathione S-transferase B with ligandin, a major binding protein of liver. Proc. natl Acad. Sci. USA71 (1974) 3879–3882.Google Scholar
  42. 42.
    Hashimoto, S., Drevon, C. A., Weinstein, D. B., Bernett, J. S., Dayton, S., and Steinberg, D., Activity of acyl-CoA:cholesterol acyl-transferase and 3-hydroxy-3-methylglutaryl-CoA reductase in sub-fractions of hepatic microsomes enriched with cholesterol. Biochim. biophys. Acta754 (1983) 126–133.Google Scholar
  43. 43.
    Hodges, T. K., Leonard, R. T., Bracker, C. E., and Keenan, T. W., Purification of an ion stimulated adenosine triphosphatase from plant roots: association with plasma membranes. Proc. natl Acad. Sci. USA69 (1972) 3307–3311.Google Scholar
  44. 44.
    Kandutsch, A. A., Chen, H. W., and Shown, E. P., Binding of 25-hydroxycholesterol and cholesterol to different cytosolic proteins. Proc. natl Acad. Sci. USA74 (1977) 2500–2503.Google Scholar
  45. 45.
    Kandutsch, A. A., Chen, H. W., and Heiniger, H. J., Biological activity of some oxygenated sterols. Science201 (1978) 498–501.Google Scholar
  46. 46.
    Kannenberg, E., Blume, A., McElhany, R. N., and Poralla, K., Monolayer and calorimetric studies of phosphatidylcholines containing branched chain fatty acids and their interactions with cholesterol and with a bacterial hopanoid in model membranes. Biochim. biophys. Acta733 (1983) 111–116.Google Scholar
  47. 47.
    Kaplan, M. R., and Simoni, R. D., Transport of cholesterol from the endoplasmic reticulum to the plasma membrane. J. Cell Biol.101 (1985) 446–453.Google Scholar
  48. 48.
    Keller, G. A., Barton, M. C., Shapiro, D. J., and Singer, S. S., 3-Hydroxy-3-methylglutaryl-coenzyme A reductase is present in peroxisomes in normal rat liver cells. Proc. natl Acad. Sci. USA82 (1985) 770–774.Google Scholar
  49. 49.
    Keller, G. A., Pazirandeh, M., and Krisans, S., 3-Hydroxy-3-methylglutaryl coenzyme A reductase localization in rat liver peroxisomes and microsomes of control and cholestyramine-treated animals; quantitative biochemical and immunoelectron microscopical analyses. J. Cell Biol.103 (1986) 875–886.Google Scholar
  50. 50.
    Keller, G. A., Scallen, T. J., Clarke, D., Maher, P. A., Krisans, S. K., and Singer, S. J., Sub-cellular localization of sterol carrier protein 2 in rat hepatocytes: its primary localization to peroxisomes. J. Cell Biol.105 (1989) 1353–1361.Google Scholar
  51. 51.
    Kleinig, H., Nuclear membranes from mammalian liver II. Lipid composition. J. Cell Biol.46 (1970) 396–402.Google Scholar
  52. 52.
    Krisans, S. K., Thompson, S. L., Pena, L. A., Kok, E., and Javitt, N. B., Bile acid synthesis by rat liver peroxisomes: metabolism of 26-hydroxycholesterol to 3-β-hydroxy-5-cholenoic acid. J. Lipid Res.26 (1985) 1324–1332.Google Scholar
  53. 53.
    Lange, Y., Dolde, J., and Steck, T. L., The rate of transmembrane movement of cholesterol in the human erythrocyte. J. biol. Chem.256 (1981) 5321–5323.Google Scholar
  54. 54.
    Lange, Y., and Matthies, H. J. G., Transfer of cholesterol from its site of synthesis to the plasma membrane. J. biol. Chem.259 (1984) 14 624–14 630.Google Scholar
  55. 55.
    Lange, Y., and Muraski, M. F., Topographic heterogeneity in cholesterol biosynthesis. J. biol. Chem.263 (1988) 9366–9373.Google Scholar
  56. 56.
    Lange, Y., and Ramos, B. V., Analysis of the distribution of cholesterol in the intact cell. J. biol. Chem.258 (1983) 15 130–15 134.Google Scholar
  57. 57.
    Lange, Y., and Steck, T. L., Cholesterol-rich intracellular membranes: a precursor to the plasma membrane. J. biol. Chem.260 (1985) 15 592–15 597.Google Scholar
  58. 58.
    Lange, Y., Swaisgood, M. H., Ramos, B. V., and Steck, T. L., Plasma membranes contain half of the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J. biol. Chem.264 (1989) 3786–3793.Google Scholar
  59. 59.
    Li, A. C., Tanaka, R. D., Callaway, K., Fogelman, A. M., and Edwards, P. A., Localization of 3-hydroxy-3-methylglutaryl CoA reductase and 3-hydroxy-3-methylglutaryl CoA synthetase in the rat liver and intestine is effected by cholestyramine and mevinolin. J. Lipid Res.29 (1988) 781–796.Google Scholar
  60. 60.
    Liscum, L., and Faust, J. R., Low density lipoprotein (LDL)-mediated suppression of cholesterol synthesis and LDL uptake is defective in Nieman-Pick type C fibroblasts. J. biol. Chem.262 (1987) 17 002–17 608.Google Scholar
  61. 61.
    Loud, A. V., and Bucher, N. L. R., The turnover of squalene in relation to the biosynthesis of cholesterol. J. biol. Chem.233 (1958) 37–41.Google Scholar
  62. 62.
    Luskey, K. L., Faust, J. R., Chin, D. J., Brown, M. S., and Goldstein, J. L., Amplification of the gene for 3-hydroxy-3-methylglutaryl coenzyme A reductase, but not for the 53 kDa protein, in UT-1 cells. J. biol. Chem.258 (1983) 8462–8469.Google Scholar
  63. 63.
    Margulis, L., Origin of Eukaryotic Cells. Yale University Press, New Haven 1975.Google Scholar
  64. 64.
    McGookey, D. J., and Anderson, R. G. W., Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells. J. Cell Biol.97 (1983) 1156–1168.Google Scholar
  65. 65.
    McLean, L. R., and Phillips, M. C., Mechanism of cholesterol and phosphatidylcholine exchange on transfer between unilamellar vesicles. Am. chem. Soc.20 (1981) 2893–2900.Google Scholar
  66. 66.
    Mitropoulos, K. A., Venkatesan, S., Balasubramaniam, S., and Peters, T. J., The submicrosomal localization of 3-hydroxy-3-methylglutaryl coenzyme-A reductase, cholesterol 7a-hydroxylase and cholesterol in rat liver. Eur. J. Biochem.82 (1978) 419–429.Google Scholar
  67. 67.
    Morris, H. R., Larsen, B. S., and Billheimer, J. T., A mass spectrometric study of the structure of sterol carrier protein SCP2 from rat liver. Biochem. biophys. Res. Commun.154 (1988) 476–482.Google Scholar
  68. 68.
    Nesmeyanova, M. A., On the possible participation of acid phospholipids in the translocation of secreted proteins through the bacterial cytoplasmic membrane. FEBS Lett.142 (1982) 189–193.Google Scholar
  69. 69.
    Noland, B. J., Arebalo, R. E., Hansbury, E., and Scallen, T. J., Purification and properties of sterol carrier protein 2. J. biol. Chem.255 (1980) 4282–4289.Google Scholar
  70. 70.
    O'Malley, B. W., and Schrader, W. T., The receptors of steroid hormones. Sci. Am.234 (1976) 32–43.Google Scholar
  71. 71.
    Ono, T., and Bloch, K., Solubilization and partial characterization of rat liver squalene epoxidase. J. biol. Chem.250 (1975) 1571–1579.Google Scholar
  72. 72.
    Oparin, A. I., The Origin of Life (3rd English edition translated by S. Margulis). Macmillan, 1938.Google Scholar
  73. 73.
    orci, L., Brown, M. S., Goldstein, J. L., Garcia-Segura, L. M., and Anderson, R. G. W., Increase in membrane cholesterol: a possible trigger for degradation of HMG-CoA reductase and crystalloid endoplasmic reticulum in UT-1 cells. Cell36 (1984) 835–845.Google Scholar
  74. 74.
    Osborne, T. F., Goldstein, J. L., and Brown, M. S., 5′ End of HMG-CoA reductase gene contains sequences responsible for cholesterol-mediated inhibition of transcription. Cell42 (1985) 203–212.Google Scholar
  75. 75.
    Ourisson, G., Bigger and better hopanoids. Nature326 (1987) 126–127.Google Scholar
  76. 76.
    Ourisson, G., Rohmer, M., and Poralla, K., Prokaryotic hopanoids and other polyterpenoid sterol surrogates. A. Rev. Microbiol.41 (1987) 301–333.Google Scholar
  77. 77.
    Pastusyzn, A., Noland, B. J., Bazan, J. F., and Fletterick, R. J., Primary sequence and structural analysis of sterol carrier protein 2 from rat liver: homology with immunoglobulins. J. biol. Chem.262 (1987) 13 219–13 227.Google Scholar
  78. 78.
    Pathak, R. K., Luskey, K. L., and Anderson, R. G. W., 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 (1986) 2158–2168.Google Scholar
  79. 79.
    Pentchev, R. G., Comly, M. E., Kruth, M. S., Tokoro, T., Butler, J., Sokol, J., Filling-Katz, M., Quirk, J. M., Marshall, D. C., Patel, S., Vanier, M. T., and Brady, R. O., Group C Niemann-Pick disease: faulty regulation of low-density lipoprotein uptake and cholesterol storage in cultured fibroblasts. FASEB J.1 (1987) 40–45.Google Scholar
  80. 80.
    Pfleger, R. C., Anderson, N. G., and Snyder, F., Lipid class and fatty acid composition of rat liver plasma membranes isolated by zonal centrifugation. Biochemistry7 (1968) 2826–2833.Google Scholar
  81. 81.
    Phillips, M. C., Johnson, W. J., and Rothblat, G. H., Mechanisms and consequences of cellular cholesterol exchange and transfer. Biochim. biophys. Acta906 (1987) 223–276.Google Scholar
  82. 82.
    Prince, R. C., Hopanoids: the world's most abundant molecules? TIBS12 (1987) 455–456.Google Scholar
  83. 83.
    Randall, L. L., Hardy, S. J. S., and Thom, J. R., Export of protein: A biochemical view. A. Rev. Microbiol.41 (1987) 507–541.Google Scholar
  84. 84.
    Reinhart, M. P., Billheimer, J. T., Faust, J. R., and Gaylor, J. L., Subcellular localization of the enzymes of cholesterol biosynthesis and metabolism in rat liver. J. biol. Chem.262 (1987) 9649–9655.Google Scholar
  85. 85.
    Reinhart, M. P., Billheimer, J. T., and Usher, D., Cytolipophorins: lipoprotein-like particles in the cytoplasm of phylogenetically diverse eukaryotes. J. Cell Biol.107 (1988) 654a, abstr. no. 3715.Google Scholar
  86. 86.
    Ritter, M. C., and Dempsey, M. E., Specificity and role in cholesterol biosynthesis of a squalene and sterol carrier protein. J. biol. Chem.246 (1971) 1536–1547.Google Scholar
  87. 87.
    Rohmer, M., Bouvier-Nave, P., and Ourisson, G., Distribution of hopanoid triterpenes in prokaryotes. J. gen. Microbiol.130 (1984) 1137–1150.Google Scholar
  88. 88.
    Saat, Y. A., and Bloch, K. E., Effect of a supernatant protein on microsomal squalene epoxidase and 2,3-oxidosqualene-lanosterol cyclase. J. biol. Chem.251 (1976) 5155–5160.Google Scholar
  89. 89.
    Scallen, T. J., Noland, B. J., Gavey, K. L., Bass, N. M., Ockner, R. K., Chanderbhan, R., and Vahouny, G. V., Sterol carrier protein 2 and fatty acid-binding protein. J. biol. Chem.260 (1985) 4733–4739.Google Scholar
  90. 90.
    Scallen, T. J., Pastuszyn, A., Noland, B. J., Chanderbhan, R., Kharroubi, A., and Vahouny, G. V., Sterol carrier and lipid transfer proteins. Chem. Phys. Lipids38 (1985) 239–261.Google Scholar
  91. 91.
    Scallen, T. J., Seetharam, B., Srikantaiah, M. V., Hansbury, E., and Lewis, M. K., Sterol carrier protein hypothesis: requirement for three substrate-specific soluble proteins in liver cholesterol biosynthesis. Life Sci.16 (1975) 853–874.Google Scholar
  92. 92.
    Scallen, T. J., Srikantaiah, M. V., Seetharam, B., Hansbury, E., and Gavey, K. L., Sterol carrier protein hypothesis. Fedn Proc.33 (1974) 1733–1746.Google Scholar
  93. 93.
    Scallen, T. J., Schuster, M. W., Dhar, A. K., and Skirdlant, H. B., Enzymic synthesis of cholesterol: use of a liver acetone powder. Lipids6 (1971) 162–164.Google Scholar
  94. 94.
    Schroeder, F., Perlmutter, J. F., Glaser, M., and Vagelos, P. R., Isolation and characterization of subcellular membranes with altered phospholipid composition from cultured fibroblasts. J. biol. Chem.251 (1976) 5015–5026.Google Scholar
  95. 95.
    Sinensky, M., and Strobel, G., Chemical composition of cellular fractions enriched in plasma membranes from sugar cane. Plant Sci. Lett.6 (1976) 209–214.Google Scholar
  96. 96.
    Singer, I. I., Scott, S., Kazazis, D. M., and Huff, J. W., Lovastatin, an inhibitor of cholesterol synthesis, induces hydroxymethylglutarylcoenzyme A reductase directly on membranes of expanded smooth endoplasmic reticulum in rat hepatocytes. Proc. natl Acad. Sci. USA85 (1988) 5264–5268.Google Scholar
  97. 97.
    Singer, S. J., Maher, P. A., and Yaffe, M. P., On the translocation of proteins across membranes. Proc. natl Acad. Sci. USA84 (1987) 1015–1019.Google Scholar
  98. 98.
    Srikantaiah, M. V., Hansbury, E., Loughran, E. D., and Scallen, T. J., Purification and properties of sterol carrier protein 1. J. biol. Chem.251 (1976) 5496–5504.Google Scholar
  99. 99.
    Sziegoleit, A., Purification and characterization of a cholesterol-binding protein from human pancreas. Biochem. J.207 (1982) 573–582.Google Scholar
  100. 100.
    Sziegoleit, A., A novel proteinase from human pancreas. Biochem. J.219 (1984) 735–742.Google Scholar
  101. 101.
    Tai, M.-H., and Bloch, K., Squalene epoxidase of rat liver. J. biol. Chem.247 (1972) 3767–3773.Google Scholar
  102. 102.
    Tanaka, T., Billheimer, J. T., and Strauss, J. F., Luteinized rat ovaries contain a sterol carrier protein. Endocrinology114 (1984) 533–540.Google Scholar
  103. 103.
    Taylor, F. R., Saucier, S. E., Shown, E. P., Parish, E. J., and Kandutsch, A. A., Correlation between oxysterol binding to a cytosolic binding protein and potency in the repression of hydroxymethylglutaryl coenzyme A reductase. J. biol. Chem.259 (1984) 12 382–12 387.Google Scholar
  104. 104.
    Taylor, F. R., Kandutsch, A. A., Gayen, A. K., Nelson, J. A., Nelson, S. S., Shirwa, S., and Spencer, T. A., 24,25-Epoxysterol metabolism in cultured mammalian cells and repression of 3-hydroxy-3-methylglutaryl-CoA reductase. J. biol. Chem.261 (1986) 15 039–15 044.Google Scholar
  105. 105.
    Taylor, F. R., and Kandutsch, A. A., in: The Oxysterol Receptor in Sterol/Steroid Hormone Mechanism of Action, pp. 395–407. Eds R. Kumar, and T. Spelsberg. Martinus Nijhoff, Boston 1987.Google Scholar
  106. 106.
    Tchen, T. T., and Bloch, K., On the conversion of squalene to lanosterol in vitro. J. biol. Chem.226 (1957) 921–930.Google Scholar
  107. 107.
    Teerlink, T., Van Der Krift, T. P., Van Heusden, G. P., and Wirtz, K. W. A., Determination of nonspecific lipid transfer protein in rat tissues and Morris hepatomas by enzyme immunoassay. Biochim. biophys. Acta793 (1984) 251–259.Google Scholar
  108. 108.
    Thines-Sempoux, D., Amar-Costesec, A., Beaufay, H., and Berthet, J., The association of cholesterol, 5′-nucleotidase and alkaline phosphodiesterase I with a dinstinct group of microsomal particles. J. Cell Biol.43 (1969) 189–192.Google Scholar
  109. 109.
    Thompson, S. L., Burrows, R., Laub, R. J., and Krisans, S. K., Cholesterol synthesis in rat liver peroxisomes. Conversion of mevalonic acid to cholesterol. J. biol. Chem.262 (1987) 17 420–17 425.Google Scholar
  110. 110.
    Trzaskos, J. M., and Gaylor, J. L., Cytosolic modulators of activities of microsomal enzymes of cholesterol biosynthesis. Purification and characterization of a non-specific lipid-transfer protein. Biochim. biophys. Acta751 (1983) 52–65.Google Scholar
  111. 111.
    Trzeciak, W. H., Simpson, E. R., Scallen, T. J., Vahouny, G. V., and Waterman, M. R., Studies on the synthesis of sterol carrier protein 2 in rat adrenocortical cells in monolayer culture. J. biol. Chem.262 (1987) 3713–3717.Google Scholar
  112. 112.
    Tsuneoka, M., Yamamoto, A., Fujiki, Y., and Tashiro, Y., Nonspecific lipid transfer protein (sterol carrier protein 2) is located in rat liver peroxisomes. J. Biochem.104 (1988) 560–564.Google Scholar
  113. 113.
    Ulsamer, A. G., Wright, P. L., Wetzel, M. G., and Korn, E. D., Plasma and phagosome membranes ofAcanthamoeba castellanii. J. Cell Biol.51 (1971) 193–215.Google Scholar
  114. 114.
    Vahouny, G. V., Chanderbhan, R., Noland, B. J., Irwin, D., Dennis, P., Lambeth, J. D., and Scallen, T. J., Sterol carrier protein 2. J. biol. Chem.258 (1983) 11 731–11 737.Google Scholar
  115. 115.
    Van Amerongen, A., Teerlink, T., Van Heusden, G. P. H., and Wirtz, K. W. A., The non-specific lipid transfer protein (sterol carrier protein 2) from rat and bovine liver. Chem. Phys. Lipids38 (1985) 195–204.Google Scholar
  116. 116.
    Van Amerongen, A., Helms, J. B., van der Krift, T. P., Schutgens, R. B. H., and Wirtz, K. W. A., Purification of nonspecific lipid transfer protein (sterol carrier protein 2) from human liver and its deficiency in livers from patients with cerebro-hepato-renal (Zellweger) syndrome. Biochim. biophys. Acta919 (1987) 149–155.Google Scholar
  117. 117.
    Van Deenen, L. L. M., and DeGier, J., Lipids of the red cell membrane, in: The Red Blood Cell, 2nd edn, pp. 147–211. Ed. D. M. Surgenor. Academic Press, New York 1974.Google Scholar
  118. 118.
    Van der Krift, T. P., Leunissen, J., Teerlink, T., Van Heusden, G. P. H., Verkleij, A. J., and Wirtz, K. W. A., Ultrastructural localization of a peroxisomal protein in rat liver using the specific antibody against the non-specific lipid transfer protein (sterol carrier protein 2). Biochim. biophys. Acta812 (1985) 387–392.Google Scholar
  119. 119.
    Van Meer, G., Plasma membrane cholesterol pools. TIBS12 (1987) 375–376.Google Scholar
  120. 120.
    Verner, K., and Schatz, G., Protein translocation across membranes. Science241 (1988) 1307–1313.Google Scholar
  121. 121.
    Von Heijne, G., and Blomberg, C., Trans-membrane translocation of proteins. The direct transfer model. Eur. J. Biochem.97 (1979) 175–181.Google Scholar
  122. 122.
    Wattenberg, B. W., and Silbert, D. F., Sterol partitioning among intracellular membranes-testing a model for cellular sterol distribution. J. biol. Chem.258 (1983) 2284–2289.Google Scholar
  123. 123.
    Westerman, J., and Wirtz, K. W. A., The primary structure of the nonspecific lipid transfer protein. Biochem. biophys. Res. Commun.127 (1985) 333–338.Google Scholar
  124. 124.
    Wickner, W. T., and Lodish, H. F., Multiple mechanisms of protein insertion into and across membranes. Science230 (1985) 400–407.Google Scholar
  125. 125.
    Wieland, F. T., Gleason, M. L., Serafini, T. A., and Rothman, J. E., The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell.50 (1987) 289–300.Google Scholar
  126. 126.
    Yeagle, P. L., Cholesterol and the cell membrane. Biochim. biophys. Acta822 (1985) 267–287.Google Scholar

Copyright information

© Birkhäuser Verlag 1990

Authors and Affiliations

  • M. P. Reinhart
    • 1
  1. 1.Biochemistry and Chemistry of LipidsUSDA-ARS-ERRCPhiladelphiaUSA

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