Sterol-binding proteins and endosomal cholesterol transport
Ximing DU, Hongyuan YANG
Sterol-binding proteins and endosomal cholesterol transport
Endosomal compartments sort and deliver exogenous lipoprotein-derived cholesterol to the endoplasmic reticulum for regulating cellular cholesterol homeostasis. A large number of studies have focused on the removal of endosomal cholesterol, since its accumulation leads to devastating human diseases. Recent studies suggest that cytoplasmic sterol-binding proteins may be involved in endosomal cholesterol transport. In particular, endosome/lysosome-localized or-associated cholesterol-binding proteins may serve as key mediators of cholesterol removal in a non-vesicular manner. Further characterization of these cholesterol-binding proteins will shed light on the molecular mechanisms that regulate endosomal cholesterol sorting.
NPC1 / NPC2 / OSBP/ORP / StAR protein / endosomal cholesterol transport
[1] |
Alpy F, Stoeckel M E, Dierich A, Escola J M, Wendling C, Chenard M P, Vanier M T, Gruenberg J, Tomasetto C, Rio M C (2001). The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J Biol Chem, 276(6): 4261-4269
CrossRef
Pubmed
Google scholar
|
[2] |
Beh C T, Cool L, Phillips J, Rine J (2001). Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics, 157(3): 1117-1140
Pubmed
|
[3] |
Bishop N, Woodman P (2000). ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol Biol Cell, 11(1): 227-239
Pubmed
|
[4] |
Brown M S, Goldstein J L (1986). A receptor-mediated pathway for cholesterol homeostasis. Science, 232(4746): 34-47
CrossRef
Pubmed
Google scholar
|
[5] |
Brown M S, Goldstein J L (2009). Cholesterol feedback: from Schoenheimer’s bottle to Scap’s MELADL. J Lipid Res, 50(Suppl): S15-S27
CrossRef
Pubmed
Google scholar
|
[6] |
Carstea E D, Morris J A, Coleman K G, Loftus S K, Zhang D, Cummings C, Gu J, Rosenfeld M A, Pavan W J, Krizman D B, Nagle J, Polymeropoulos M H, Sturley S L, Ioannou Y A, Higgins M E, Comly M, Cooney A, Brown A, Kaneski C R, Blanchette-Mackie E J, Dwyer N K, Neufeld E B, Chang T Y, Liscum L, Strauss J F 3rd, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O’Neill R R, van Diggelen O P, Elleder M, Patterson M C, Brady R O, Vanier M T, Pentchev P G, Tagle D A (1997). Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science, 277(5323): 228-231
CrossRef
Pubmed
Google scholar
|
[7] |
Chang T Y, Chang C C, Ohgami N, Yamauchi Y (2006). Cholesterol sensing, trafficking, and esterification. Annu Rev Cell Dev Biol, 22(1): 129-157
CrossRef
Pubmed
Google scholar
|
[8] |
Charman M, Kennedy B E, Osborne N, Karten B (2010). MLN64 mediates egress of cholesterol from endosomes to mitochondria in the absence of functional Niemann-Pick Type C1 protein. J Lipid Res, 51(5): 1023-1034
CrossRef
Pubmed
Google scholar
|
[9] |
Davies J P, Ioannou Y A (2000). Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J Biol Chem, 275(32): 24367-24374
CrossRef
Pubmed
Google scholar
|
[10] |
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 (2011). A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J Cell Biol, 192(1): 121-135
CrossRef
Pubmed
Google scholar
|
[11] |
Goldstein J L, DeBose-Boyd R A, Brown M S (2006). Protein sensors for membrane sterols. Cell, 124(1): 35-46
CrossRef
Pubmed
Google scholar
|
[12] |
Harrison K D, Miao R Q, Fernandez-Hernándo C, Suárez Y, Dávalos A, Sessa W C (2009). Nogo-B receptor stabilizes Niemann-Pick type C2 protein and regulates intracellular cholesterol trafficking. Cell Metab, 10(3): 208-218
CrossRef
Pubmed
Google scholar
|
[13] |
Holtta-Vuori M, Ikonen E (2006). Endosomal cholesterol traffic: vesicular and non-vesicular mechanisms meet. Biochem Soc Trans, 34(Pt 3): 392-394
CrossRef
Pubmed
Google scholar
|
[14] |
Ikonen E (2008). Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol, 9(2): 125-138
CrossRef
Pubmed
Google scholar
|
[15] |
Im Y J, Raychaudhuri S, Prinz W A, Hurley J H (2005). Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature, 437(7055): 154-158
CrossRef
Pubmed
Google scholar
|
[16] |
Infante R E, Abi-Mosleh L, Radhakrishnan A, Dale J D, Brown M S, Goldstein J L (2008a). Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J Biol Chem, 283(2): 1052-1063
CrossRef
Pubmed
Google scholar
|
[17] |
Infante R E, Radhakrishnan A, Abi-Mosleh L, Kinch L N, Wang M L, Grishin N V, Goldstein J L, Brown M S (2008b). Purified NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem, 283(2): 1064-1075
CrossRef
Pubmed
Google scholar
|
[18] |
Infante R E, Wang M L, Radhakrishnan A, Kwon H J, Brown M S, Goldstein J L (2008c). NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc Natl Acad Sci USA, 105(40): 15287-15292
CrossRef
Pubmed
Google scholar
|
[19] |
Kwon H J, Abi-Mosleh L, Wang M L, Deisenhofer J, Goldstein J L, Brown M S, Infante R E (2009). Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell, 137(7): 1213-1224
CrossRef
Pubmed
Google scholar
|
[20] |
Lavigne P, Najmanivich R, Lehoux J G (2010). Mammalian StAR-related lipid transfer (START) domains with specificity for cholesterol: structural conservation and mechanism of reversible binding. Subcell Biochem, 51: 425-437
CrossRef
Pubmed
Google scholar
|
[21] |
Lehto M, Laitinen S, Chinetti G, Johansson M, Ehnholm C, Staels B, Ikonen E, Olkkonen V M (2001). The OSBP-related protein family in humans. J Lipid Res, 42(8): 1203-1213
Pubmed
|
[22] |
Lev S (2010). Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat Rev Mol Cell Biol, 11(10): 739-750
CrossRef
Pubmed
Google scholar
|
[23] |
Lingwood D, Simons K (2010). Lipid rafts as a membrane-organizing principle. Science, 327(5961): 46-50
CrossRef
Pubmed
Google scholar
|
[24] |
Liu B, Turley S D, Burns D K, Miller A M, Repa J J, Dietschy J M (2009). Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/- mouse. Proc Natl Acad Sci USA, 106(7): 2377-2382
CrossRef
Pubmed
Google scholar
|
[25] |
Loewen C J, Roy A, Levine T P (2003). A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J, 22(9): 2025-2035
CrossRef
Pubmed
Google scholar
|
[26] |
Maxfield F R, van Meer G (2010). Cholesterol, the central lipid of mammalian cells. Curr Opin Cell Biol, 22(4): 422-429
CrossRef
Pubmed
Google scholar
|
[27] |
Mesmin B, Maxfield F R (2009). Intracellular sterol dynamics. Biochim Biophys Acta, 1791(7): 636-645
Pubmed
|
[28] |
Naureckiene S, Sleat D E, Lackland H, Fensom A, Vanier M T, Wattiaux R, Jadot M, Lobel P (2000). Identification of HE1 as the second gene of Niemann-Pick C disease. Science, 290(5500): 2298-2301
CrossRef
Pubmed
Google scholar
|
[29] |
Ngo M H, Colbourne T R, Ridgway N D (2010). Functional implications of sterol transport by the oxysterol-binding protein gene family. Biochem J, 429(1): 13-24
CrossRef
Pubmed
Google scholar
|
[30] |
Ohgami N, Ko D C, Thomas M, Scott M P, Chang C C, Chang T Y (2004). Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain. Proc Natl Acad Sci USA, 101(34): 12473-12478
CrossRef
Pubmed
Google scholar
|
[31] |
Ohsaki Y, Sugimoto Y, Suzuki M, Hosokawa H, Yoshimori T, Davies J P, Ioannou Y A, Vanier M T, Ohno K, Ninomiya H (2006). Cholesterol depletion facilitates ubiquitylation of NPC1 and its association with SKD1/Vps4. J Cell Sci, 119(Pt 13): 2643-2653
CrossRef
Pubmed
Google scholar
|
[32] |
Okamura N, Kiuchi S, Tamba M, Kashima T, Hiramoto S, Baba T, Dacheux F, Dacheux J L, Sugita Y, Jin Y Z (1999). A porcine homolog of the major secretory protein of human epididymis, HE1, specifically binds cholesterol. Biochim Biophys Acta, 1438(3): 377-387
Pubmed
|
[33] |
Rigotti A, Cohen D E, Zanlungo S (2010). STARTing to understand MLN64 function in cholesterol transport. J Lipid Res, 51(8): 2015-2017
CrossRef
Pubmed
Google scholar
|
[34] |
Rosenbaum A I, Zhang G, Warren J D, Maxfield F R (2010). Endocytosis of beta-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proc Natl Acad Sci USA, 107(12): 5477-5482
CrossRef
Pubmed
Google scholar
|
[35] |
Schulz T A, Choi M G, Raychaudhuri S, Mears J A, Ghirlando R, Hinshaw J E, Prinz W A (2009). Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J Cell Biol, 187(6): 889-903
CrossRef
Pubmed
Google scholar
|
[36] |
Sleat D E, Wiseman J A, El-Banna M, Price S M, Verot L, Shen M M, Tint G S, Vanier M T, Walkley S U, Lobel P (2004). Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci USA, 101(16): 5886-5891
CrossRef
Pubmed
Google scholar
|
[37] |
Soccio R E, Breslow J L (2003). StAR-related lipid transfer (START) proteins: mediators of intracellular lipid metabolism. J Biol Chem, 278(25): 22183-22186
CrossRef
Pubmed
Google scholar
|
[38] |
Soccio R E, Breslow J L (2004). Intracellular cholesterol transport. Arterioscler Thromb Vasc Biol, 24(7): 1150-1160
CrossRef
Pubmed
Google scholar
|
[39] |
Subramanian K, Balch W E (2008). NPC1/NPC2 function as a tag team duo to mobilize cholesterol. Proc Natl Acad Sci USA, 105(40): 15223-15224
CrossRef
Pubmed
Google scholar
|
[40] |
Suchanek M, Hynynen R, Wohlfahrt G, Lehto M, Johansson M, Saarinen H, Radzikowska A, Thiele C, Olkkonen V M (2007). The mammalian oxysterol-binding protein-related proteins (ORPs) bind 25-hydroxycholesterol in an evolutionarily conserved pocket. Biochem J, 405(3): 473-480
CrossRef
Pubmed
Google scholar
|
[41] |
Taylor F R, Saucier S E, Shown E P, Parish E J, Kandutsch A A (1984). Correlation between oxysterol binding to a cytosolic binding protein and potency in the repression of hydroxymethylglutaryl coenzyme A reductase. J Biol Chem, 259(20): 12382-12387
Pubmed
|
[42] |
Wang M L, Motamed M, Infante R E, Abi-Mosleh L, Kwon H J, Brown M S, Goldstein J L (2010). Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab, 12(2): 166-173
CrossRef
Pubmed
Google scholar
|
[43] |
Wang P, Zhang Y, Li H, Chieu H K, Munn A L, Yang H (2005a). AAA ATPases regulate membrane association of yeast oxysterol binding proteins and sterol metabolism. EMBO J, 24(17): 2989-2999
CrossRef
Pubmed
Google scholar
|
[44] |
Wang P Y, Weng J, Anderson R G (2005b). OSBP is a cholesterol-regulated scaffolding protein in control of ERK1/2 activation. Science, 307(5714): 1472-1476
CrossRef
Pubmed
Google scholar
|
[45] |
Willenborg M, Schmidt C K, Braun P, Landgrebe J, von Figura K, Saftig P, Eskelinen E L (2005). Mannose 6-phosphate receptors, Niemann-Pick C2 protein, and lysosomal cholesterol accumulation. J Lipid Res, 46(12): 2559-2569
CrossRef
Pubmed
Google scholar
|
[46] |
Wyles J P, McMaster C R, Ridgway N D (2002). Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum. J Biol Chem, 277(33): 29908-29918
CrossRef
Pubmed
Google scholar
|
[47] |
Xu S, Benoff B, Liou H L, Lobel P, Stock A M (2007). Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease. J Biol Chem, 282(32): 23525-23531
CrossRef
Pubmed
Google scholar
|
[48] |
Yan D, Mäyränpää M I, Wong J, Perttilä J, Lehto M, Jauhiainen M, Kovanen P T, Ehnholm C, Brown A J, Olkkonen V M (2008). OSBP-related protein 8 (ORP8) suppresses ABCA1 expression and cholesterol efflux from macrophages. J Biol Chem, 283(1): 332-340
CrossRef
Pubmed
Google scholar
|
[49] |
Yan D, Olkkonen V M (2008). Characteristics of oxysterol binding proteins. Int Rev Cytol, 265: 253-285
CrossRef
Pubmed
Google scholar
|
[50] |
Yang H (2006). Nonvesicular sterol transport: two protein families and a sterol sensor? Trends Cell Biol, 16(9): 427-432
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |