Physiological and coordinate downregulation of the NPC1 and NPC2 genes are associated with the sequestration of LDL-derived cholesterol within endocytic compartments

Journal of Cellular Biochemistry

Volumn 108, Issue 5, 2009, Pages 1102-1116

  Jelinek, David ^a   Mount Patrick, Sarah ^a   Kitt, Khameeka N ^b   Chan, Teddy ^c   Francis, Gordon A ^c   Garver, William S ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

ACAT accessible pool; Cholesterol; Cholesteryl ester; Early endosomes; Fibroblasts; Late endosomes lysosomes; Low density lipoprotein; Niemann Pick type C; Sterol regulatory pool

Indexed keywords

CHOLESTEROL ACYLTRANSFERASE; CHOLESTEROL ESTER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LIPID TRANSFER PROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MEMBRANE LIPID; MESSENGER RNA; NIEMANN PICK C1 PROTEIN; NIEMANN PICK C2 PROTEIN; PROTEIN; PROTEIN PRECURSOR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; STEROL REGULATORY ELEMENT BINDING PROTEIN CLEAVAGE ACTIVATING PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ARTICLE; CELL LEVEL; CHOLESTEROL ESTERIFICATION; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; ENDOSOME; FEEDBACK SYSTEM; FIBROBLAST; GENE; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMAN; HUMAN CELL; INSULIN INDUCED GENE 1; LYSOSOME; NIEMANN PICK C1 GENE; NIEMANN PICK C2 GENE; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION;

CARRIER PROTEINS; CELL LINE; CHOLESTEROL, LDL; DOWN-REGULATION; ENDOSOMES; FIBROBLASTS; GLYCOPROTEINS; HUMANS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; SIGNAL TRANSDUCTION; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 72449193255     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22339     Document Type: Article

References (49)

1. Amemiya-Kudo M, Shimano H, Hasty AH, Yahagi N, Yoshikawa T, Matsuzaka T, Okazaki H, Tamura Y, Iizuka Y, Ohashi K, Osuga J, Harada K, Gotoda T, Sato R, Kumura S, Ishibashi S, Yamada N. 2002. Transcriptional activities of nuclear SREBP-1a, -1c, and -2 to different target promoters of lipogenic and cholesterogenic genes. J Lipid Res 43:1220-1235. (Pubitemid 34988170)
2. Brasaemle DI, Attie AD. 1990. Rapid intracellular transport of LDL-derived cholesterol to the plasma membrane in cultured fibroblasts. J Lipid Res 31:103-112.
3. Brown MS, Goldstein JL. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science 232:34-47.
4. Brown MS, Goldstein JL. 1997. The SREBP pathway: Regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89:331-340. (Pubitemid 27220877)
5. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Tagle DA, Strauss JF III, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O'Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG, Tagle DA. 1997. Niemann-Pick C1 disease gene: Homology to mediators of cholesterol homeostasis. Science 277:228-231. (Pubitemid 27446076)
6. Cheruku SR, Xu Z, Dutia R, Lobel P, Storch J. 2006. Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J Biol Chem 281:31594-31604. (Pubitemid 46041425)
7. Du X, Pham YH, Brown AJ. 2004. Effects of 25-hydroxycholesterol on cholesterol esterification and sterol regulatory element binding protein processing are dissociable. J Biol Chem 279:47010-47016.
8. Edwards PA, Ericsson J. 1999. Sterols and isoprenoids: Signaling molecules derived from the cholesterol biosynthetic pathway. Annu Rev Biochem 68:157-185. (Pubitemid 29449190)
9. Folch J, Lees M, Stanley GH. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497-509.
10. Friedland N, Liou H-L, Lobel P, Stock AM. 2003. Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. Proc Natl Acad Sci USA 100:2512-2517. (Pubitemid 36297530)
11. Garver WS, Heidenreich RA, Erickson RP, Thomas MA, Wilson JM. 2000. Localization of the murine Niemann-Pick C1 protein to two distinct intracellular compartments. J Lipid Res 41:673-687.
12. Garver WS, Krishnan K, Gallagos JR, Michikawa M, Francis GA, Heidenreich RA. 2002. Niemann-Pick C1 protein regulates cholesterol transport to the trans-Golgi network and plasma membrane caveolae. J Lipid Res 43:579-589.
13. Garver WS, Jelinek D, Francis GA, Murphy BD. 2008. The Niemann-Pick C1 gene is downregulated by feedback inhibition of the SREBP pathway in human fibroblasts. J Lipid Res 49:1090-1102.
14. Gasingirwa MC, Thirion J, Costa C, Flamion B, Lobel P, Jadot M. 2008. A method to assess the lysosomal residence of proteins in cultured cells. Anal Biochem 374:31-40.
15. Gevry N, Schoonjans K, Guay F, Murphy BD. 2008. Cholesterol supply and SREBPs modulate transcription of the Niemann-Pick C1 gene in steroidogenic tissues. J Lipid Res 49:1024-1033.
16. Hornick CA, Hui DY, DeLamatre JG. 1997. A role for retrosomes in intracellular cholesterol transport from endosomes to the plasma membrane. Am J Phys Cell Physiol 273:C1075-C1081. (Pubitemid 27422188)
17. Iddon CR, Wilkinson J, Bennett AJ, Bennett J, Salter AM, Higgins JA. 2001. A role for smooth endoplasmic reticulum membrane cholesterol ester in determining the intracellular location and regulation of sterol regulatory element binding protein-2. Biochem J 358:415-422. (Pubitemid 32826358)
18. Infante RE, Abi-Mosleh L, Radhakrishnan A, Dale JD, Brown MS, Goldstein JL. 2008a. Purified NPC1 Protein. I. Binding of cholesterol and oxysterol to a 1278-amino acid membrane protein. J Biol Chem 283:1052-1063.
19. Infante RE, Radhakrishnan A, Abi-Mosleh L, Kinch LN, Wang ML, Grishin NV, Goldstein JL, Brown MS. 2008b. Purified NPC1 Protein. II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem 283:1064-1075.
20. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, Goldstein JL. 2008c. NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc Natl Acad Sci USA 105:15287-15292.
21. Johnson WJ, Chacko GK, Phillips MC, Rothblat GH. 1990. The efflux of lysosomal cholesterol from cells. J Biol Chem 265:5546-5553.
22. Khelef N, Soe TT, Quehenberger O, Beatini N, Tabas I, Maxfield FR. 2000. Enrichment of acyl coenzyme A:cholesterol acyltransferase near trans-Golgi network and endocytic recycling compartment. Arterioscler Thromb 20:1769-1776. (Pubitemid 30470592)
23. Ko DC, Binkley J, Sidow A, Scott MP. 2003. The integrity of a cholesterol-binding pocket in Niemann-Pick C2 protein is necessary to control lysosome cholesterol levels. Proc Natl Acad Sci USA 100:2518-2525. (Pubitemid 36297531)
24. Kristiana I, Yang H, Brown AJ. 2008. Different kinetics of cholesterol delivery to components of the cholesterol homeostatic machinary: Implications for cholesterol trafficking to the endoplasmic reticulum. Biochim Biophys Acta 1781:724-730.
25. Kruth HS, Comly ME, Butler JD, Vanier MT, Fink JK, Wenger DA, Patel S, Pentchev PG. 1986. Type C Niemann-Pick disease. Abnormal metabolism of low-density lipoprotein in homozygous and heterozygous fibroblasts. J Biol Chem 261:16769-16774.
26. Lange Y, Ye J, Rigney M, Steck TL. 1999. Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res 40:2264-2270. (Pubitemid 30017528)
27. Lange Y, Ye J, Steck TL. 2004. How cholesterol homeostasis is regulated by plasma membrane cholesterol in excess of phospholipids. Proc Natl Acad Sci USA 101:11664-11667. (Pubitemid 39095353)
28. Liu R, Lu P, Chu JWK, Sharom FJ. 2009. Characterization of fluorescent sterol binding to purified human NPC1. J Biol Chem 284:1840-1852.
29. Mondal M, Mesmin B, Mukherjee S, Maxfield FR. 2009. Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol Biol Cell 20:581-588.
30. Nakamura Y, Takayama N, Minamitani T, Ikuta T, Ariga H, Matsumoto K. 2000. Primary structure, genomic organization and expression of the major secretory protein of murine epididymis, HE1. Gene 251:55-62. (Pubitemid 30339416)
31. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P. 2000. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290:2298-2301. (Pubitemid 32041569)
32. Neufeld EB, Cooney AM, Pitha J, Dawidowicz EA, Dwyer NK, Pentchev PG, Blanchette-Mackie EJ. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J Biol Chem 271:21604-21613. (Pubitemid 26293030)
33. Neufeld EB, Wastney M, Patel S, Suresh S, Conney AM, Dwyer NK, Roff CF, Ohno K, Morris JA, Carstea ED, Incardona JP, Strauss JF III, Vanier MT, Patterson MC, Brady RO, Pentchev PG, Blanchette-Mackie EJ. 1999. The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J Biol Chem 274:9627-9635. (Pubitemid 129517939)
34. Nohturfft A, Yabe D, Goldstein JL, Brown MS, Espenshade PJ. 2000. Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes. Cell 102:315-323.
35. Ohgami N, Ko DC, Thomas M, Scott MP, Chang CCY, Chang TY. 2004. Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain. Proc Natl Acad Sci USA 101:12473-12478. (Pubitemid 39122048)
36. Radhakrishnan A, McConnell HM. 2000. Chemical activity of cholesterol in membranes. Biochemistry 39:8119-8124.
37. Radhakrishnan A, Sun LP, Kwon HJ, Brown MS, Goldstein JL. 2004. Direct binding of cholesterol to the purified membrane region of SCAP: Mechanism for a sterol-sensing domain. Mol Cell 15:259-268. (Pubitemid 38950972)
38. Radhakrishnan A, Ikeda Y, Joo Kwon H, Brown MS, Goldstein JL. 2007. Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: Oxysterols block transport by binding to Insig. Proc Natl Acad Sci USA 104:6511-6518. (Pubitemid 47175533)
39. Sato R, Inoue J, Kawabe Y, Kodama T, Takano T, Maeda M. 1996. Sterol-dependent transcriptional regulation of sterol regulatory element binding protein-2. J Biol Chem 271:26461-26464. (Pubitemid 26359040)
40. Shimomura I, Shimano JD, Horton JD, Goldstein JL, Brown MS. 1997. Differential expression of exons 1a and 1c in mRNAs for sterol regulatory element binding protein-1 in human and mouse organs and cultured cells. J Clin Invest 99:838-845. (Pubitemid 27123619)
41. Sleat DE, Wiseman JA, El-Banna M, Price SM, Verot L, Shen MM, Tint GS, Vanier MT, Walkley SU, Lobel P. 2004. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci USA 101:5886-5891. (Pubitemid 38520498)
42. Sugii S, Reid PC, Ohgami N, Du H, Chang TY. 2003. Distinct endosomal compartments in early trafficking of low-density lipoprotein-derived cholesterol. J Biol Chem 278:27180-27189. (Pubitemid 36876874)
43. Tabas I, Rosoff WJ, Boykow GC. 1988. Acyl coenzyme A:cholesterol acyltransferase in macrophages utilizes a cellular pool of cholesterol oxidase-accessible cholesterol as substrate. J Biol Chem 263:1266-1272. (Pubitemid 18039928)
44. Underwood KW, Jacobs NL, Howley A, 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. (Pubitemid 28103299)
45. Urano Y, Watanabe H, Murphy SR, Shibuya Y, Geng Y, Peden AA, Chang CCY, Chang TY. 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 USA 105:16513-16518.
46. Wojtanik KM, 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. (Pubitemid 36799812)
47. Xu XX, Tabas I. 1991. Lipoproteins activate acyl-coenzyme A:cholesterol acyltransferase in macrophages only after cellular cholesterol pools are expanded to a critical threshold level. J Biol Chem 266:17040-17048. (Pubitemid 21907903)
48. Yabe D, Brown MS, Goldstein JL. 2002. Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element binding proteins. Proc Natl Acad Sci USA 99:12753-12758.
49. Yang T, Espenshade PJ, Wright ME, Yabe D, Gong Y, Aebersold R, Goldstein JL, Brown MS. 2002. Crucial step in cholesterol homeostasis: Sterols promote binding of SCAP to Insig-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110:489-500. (Pubitemid 35232292)