Detergent-free isolation and characterization of cholesterol-rich membrane domains from trans-Golgi network vesicles

Journal of Lipid Research

Volumn 52, Issue 3, 2011, Pages 582-589

  Waugh, Mark G ^a   Chu, K M Emily ^a   Clayton, Emma L ^a   Minogue, Shane ^a   Hsuan, J Justin ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Caveolae; Cholesterol cell tissue; Fluorescence microscopy; Golgi apparatus

Indexed keywords

CHOLESTEROL; GANGLIOSIDE GM1; PHOSPHATIDYLINOSITIDE; RAB11 PROTEIN; SYNTAXIN; SYNTAXIN 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL MEMBRANE; CELL ORGANELLE; CELL VACUOLE; CENTRIFUGATION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ENDOPLASMIC RETICULUM; ENDOSOME; HUMAN; HUMAN CELL; LYSOSOME; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; SUCROSE DENSITY GRADIENT CENTRIFUGATION; TRANS GOLGI NETWORK; VELOCITY CENTRIFUGATION;

ANIMALS; CELL FRACTIONATION; CELL LINE; CENTRIFUGATION, DENSITY GRADIENT; CHOLESTEROL; CYTOPLASMIC VESICLES; DETERGENTS; ENDOPLASMIC RETICULUM; ENDOSOMES; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE MICRODOMAINS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); TRANS-GOLGI NETWORK;

EID: 79953208619     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.D012807     Document Type: Article

References (53)

1. Mukherjee, S., X. Zha, I. Tabas, and F. R. Maxfield. 1998. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75:1915-1925.
2. Mobius, W., E. van Donselaar, Y. Ohno-Iwashita, Y. Shimada, H. F. Heijnen, J. W. Slot, and H. J. Geuze. 2003. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic. 4:222-231.
3. Chang, T. Y., P. C. Reid, S. Sugii, N. Ohgami, J. C. Cruz, and C. C. Chang. 2005. Niemann-Pick type C disease and intracellular cholesterol trafficking. J. Biol. Chem. 280:20917-20920.
4. Vance, J. E. 2006. Lipid imbalance in the neurological disorder, Niemann-Pick C disease. FEBS Lett. 580:5518-5524. (Pubitemid 44479758)
5. Maxfield, F. R., and I. Tabas. 2005. Role of cholesterol and lipid organization in disease. Nature. 438:612-621. (Pubitemid 41740565)
6. Choudhury, A., D. K. Sharma, D. L. Marks, and R. E. Pagano. 2004. Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit rab4 and perturb membrane recycling. Mol. Biol. Cell. 15: 4500-4511.
7. Lebrand, C., M. Corti, H. Goodson, P. Cosson, V. Cavalli, N. Mayran, J. Faure, and J. Gruenberg. 2002. Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J. 21:1289-1300. (Pubitemid 34246508)
8. Choudhury, A., M. Dominguez, V. Puri, D. K. Sharma, K. Narita, C. L. Wheatley, D. L. Marks, and R. E. Pagano. 2002. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest. 109:1541-1550.
9. Linder, M. D., R. L. Uronen, M. Holtta-Vuori, P. van der Sluijs, J. Peranen, and E. Ikonen. 2007. Rab8-dependent recycling promotes endosomal cholesterol removal in normal and sphingolipidosis cells. Mol. Biol. Cell. 18:47-56.
10. Ganley, I. G., and S. R. Pfeffer. 2006. Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells. J. Biol. Chem. 281:17890-17899.
11. Vainio, S., and E. Ikonen. 2003. Macrophage cholesterol transport: a critical player in foam cell formation. Ann. Med. 35: 146-155.
12. Brusselmans, K., L. Timmermans, T. Van de Sande, P. P. Van Veldhoven, G. Guan, I. Shechter, F. Claessens, G. Verhoeven, and J. V. Swinnen. 2007. Squalene synthase, a determinant of raft-associated cholesterol and modulator of cancer cell proliferation. J. Biol. Chem. 282:18777-18785.
13. Pediconi, M. F., C. E. Gallegos, E. B. De Los Santos, and F. J. Barrantes. 2004. Metabolic cholesterol depletion hinders cell-surface trafficking of the nicotinic acetylcholine receptor. Neuroscience. 128:239-249.
14. Sugii, S., S. Lin, N. Ohgami, M. Ohashi, C. C. Chang, and T. Y. Chang. 2006. Roles of endogenously synthesized sterols in the endocytic pathway. J. Biol. Chem. 281:23191-23206.
15. Waugh, M. G., and J. J. Hsuan. 2009. Preparation of membrane rafts. Methods Mol. Biol. 462:403-414.
16. Zheng, Y. Z., K. B. Berg, and L. J. Foster. 2009. Mitochondria do not contain lipid rafts, and lipid rafts do not contain mitochondrial proteins. J. Lipid Res. 50:988-998.
17. Waugh, M. G., S. Minogue, J. S. Anderson, A. Balinger, D. Blumenkrantz, D. P. Calnan, R. Cramer, and J. J. Hsuan. 2003. Localization of a highly active pool of type II phosphatidylinositol 4-kinase in a p97/valosin-containing- protein-rich fraction of the endoplasmic reticulum. Biochem. J. 373:57-63.
18. Song, K. S., S. Li, T. Okamoto, L. A. Quilliam, M. Sargiacomo, and M. P. Lisanti. 1996. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J. Biol. Chem. 271:9690-9697.
19. Waugh, M. G., D. Lawson, and J. J. Hsuan. 1999. Epidermal growth factor receptor activation is localized within low-buoyant density, non-caveolar membrane domains. Biochem. J. 337:591-597.
20. Simons, J. P., R. Al-Shawi, S. Minogue, M. G. Waugh, C. Wiedemann, S. Evangelou, A. Loesch, T. S. Sihra, R. King, T. T. Warner, et al. 2009. Loss of phosphatidylinositol 4-kinase 2alpha activity causes late onset degeneration of spinal cord axons. Proc. Natl. Acad. Sci. USA. 106:11535-11539.
21. Waugh, M. G., S. Minogue, D. Blumenkrantz, J. S. Anderson, and J. J. Hsuan. 2003. Identification and characterization of differentially active pools of type IIalpha phosphatidylinositol 4-kinase activity in unstimulated A431 cells. Biochem. J. 376:497-503.
22. Waugh, M. G., S. Minogue, D. Chotai, F. Berditchevski, and J. J. Hsuan. 2006. Lipid and peptide control of phosphatidylinositol 4-kinase IIalpha activity on Golgi-endosomal rafts. J. Biol. Chem. 281:3757-3763.
23. Ilangumaran, S., S. Arni, Y. Chicheportiche, A. Briol, and D. C. Hoessli. 1996. Evaluation by dot-immunoassay of the differential distribution of cell surface and intracellular proteins in glycosylphosphatidylinositol-rich plasma membrane domains. Anal. Biochem. 235:49-56.
24. Stan, R. V., W. G. Roberts, D. Predescu, K. Ihida, L. Saucan, L. Ghitescu, and G. E. Palade. 1997. Immunoisolation and partial characterization of endothelial plasmalemmal vesicles (caveolae). Mol. Biol. Cell. 8:595-605.
25. Minogue, S., M. G. Waugh, M. A. De Matteis, D. J. Stephens, F. Berditchevski, and J. J. Hsuan. 2006. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J. Cell Sci. 119:571-581.
26. He, Y., and M. E. Linder. 2009. Differential palmitoylation of the endosomal SNAREs syntaxin 7 and syntaxin 8. J. Lipid Res. 50: 398-404.
27. Lombardi, D., T. Soldati, M. A. Riederer, Y. Goda, M. Zerial, and S. R. Pfeffer. 1993. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12:677-682.
28. Luzio, J. P., B. Brake, G. Banting, K. E. Howell, P. Braghetta, and K. K. Stanley. 1990. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem. J. 270:97-102.
29. Ponnambalam, S., M. Girotti, M. L. Yaspo, C. E. Owen, A. C. Perry, T. Suganuma, T. Nilsson, M. Fried, G. Banting, and G. Warren. 1996. Primate homologues of rat TGN38: primary structure, expression and functional implications. J. Cell Sci. 109: 675-685. (Pubitemid 26092688)
30. Tellam, J. T., D. E. James, T. H. Stevens, and R. C. Piper. 1997. Identification of a mammalian Golgi Sec1p-like protein, mVps45. J. Biol. Chem. 272:6187-6193.
31. Tschantz, W. R., L. Zhang, and P. J. Casey. 1999. Cloning, expression, and cellular localization of a human prenylcysteine lyase. J. Biol. Chem. 274:35802-35808.
32. Smart, E. J., Y. S. Ying, C. Mineo, and R. G. Anderson. 1995. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc. Natl. Acad. Sci. USA. 92:10104-10108.
33. Waugh, M. G., D. Lawson, S. K. Tan, and J. J. Hsuan. 1998. Phosphatidylinositol 4-phosphate synthesis in immunoisolated caveolae-like vesicles and low buoyant density non-caveolar membranes. J. Biol. Chem. 273:17115-17121.
34. Fujita, H., P. L. Tuma, C. M. Finnegan, L. Locco, and A. L. Hubbard. 1998. Endogenous syntaxins 2, 3 and 4 exhibit distinct but overlapping patterns of expression at the hepatocyte plasma membrane. Biochem. J. 329:527-538.
35. Ahluwalia, N., J. J. Bergeron, I. Wada, E. Degen, and D. B. Williams. 1992. The p88 molecular chaperone is identical to the endoplasmic reticulum membrane protein, calnexin. J. Biol. Chem. 267: 10914-10918.
36. Ikonen, E., K. Fiedler, R. G. Parton, and K. Simons. 1995. Prohibitin, an antiproliferative protein, is localized to mitochondria. FEBS Lett. 358:273-277.
37. Ullrich, O., S. Reinsch, S. Urbe, M. Zerial, and R. G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913-924.
38. Bock, J. B., J. Klumperman, S. Davanger, and R. H. Scheller. 1997. Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell. 8:1261-1271.
39. Otto, G. P., M. Razi, J. Morvan, F. Stenner, and S. A. Tooze. 2010. A novel syntaxin 6-interacting protein, SHIP164, regulates syntaxin 6-dependent sorting from early endosomes. Traffic. 11:688-705.
40. Subramaniam, V. N., E. Loh, H. Horstmann, A. Habermann, Y. Xu, J. Coe, G. Griffiths, and W. Hong. 2000. Preferential association of syntaxin 8 with the early endosome. J. Cell Sci. 113:997-1008. (Pubitemid 30179479)
41. He, Y., and M. E. Linder. 2009. Differential palmitoylation of the endosomal SNAREs syntaxin 7 and syntaxin 8. J. Lipid Res. 50: 398-404.
42. Chavrier, P., R. G. Parton, H. P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 62:317-329.
43. Emans, N., J. P. Gorvel, C. Walter, V. Gerke, R. Kellner, G. Griffiths, and J. Gruenberg. 1993. Annexin II is a major component of fusogenic endosomal vesicles. J. Cell Biol. 120:1357-1369.
44. Wang, Y. J., J. Wang, H. Q. Sun, M. Martinez, Y. X. Sun, E. Macia, T. Kirchhausen, J. P. Albanesi, M. G. Roth, and H. L. Yin. 2003. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell. 114:299-310.
45. Mu, F. T., J. M. Callaghan, O. Steele-Mortimer, H. Stenmark, R. G. Parton, P. L. Campbell, J. McCluskey, J. P. Yeo, E. P. Tock, and B. H. Toh. 1995. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J. Biol. Chem. 270:13503-13511.
46. Nakamura, N., C. Rabouille, R. Watson, T. Nilsson, N. Hui, P. Slusarewicz, T. E. Kreis, and G. Warren. 1995. Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131:1715-1726. (Pubitemid 26007969)
47. Herscovics, A. 1999. Importance of glycosidases in mammalian glycoprotein biosynthesis. Biochim. Biophys. Acta. 1473:96-107.
48. Velasco, A., L. Hendricks, K. W. Moremen, D. R. Tulsiani, O. Touster, and M. G. Farquhar. 1993. Cell type-dependent variations in the subcellular distribution of alpha-mannosidase I and II. J. Cell Biol. 122:39-51.
49. Taguchi, T., M. Pypaert, and G. Warren. 2003. Biochemical subfractionation of the mammalian Golgi apparatus. Traffic. 4:344-352. (Pubitemid 36582635)
50. Craige, B., G. Salazar, and V. Faundez. 2008. Phosphatidylinositol-4- Kinase Type II Alpha contains an AP-3 sorting motif and a kinase domain that are both required for endosome traffic. Mol. Biol. Cell. 19:1415-1426.
51. Waugh, M. G., S. Minogue, and J. J. Hsuan. 2009. Quantification of multiple phosphatidylinositol 4-kinase isozyme activities in cell extracts. Methods Mol. Biol. 462:279-289.
52. Urbe, S., L. A. Huber, M. Zerial, S. A. Tooze, and R. G. Parton. 1993. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 334:175-182.
53. De Matteis, M. A., and A. Luini. 2008. Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9:273-284.