Niemann-Pick type C disease proteins: Orphan transporters or membrane rheostats?

Future Lipidology

Volumn 2, Issue 3, 2007, Pages 357-367

  Munkacsi, Andrew B ^a   Porto, Anthony F ^a   Sturley, Stephen L ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

Cholesterol; Gangliosides; Lysosome; Niemann Pick; Niemann Pick type C1; Niemann Pick type C2; Resistance nodulation division transporter; Rheostat

Indexed keywords

ALLOPREGNENOLONE; ALPHA TOCOPHEROL; CARRIER PROTEIN; CHAPERONE; CHOLESTEROL DERIVATIVE; HYPOCHOLESTEROLEMIC AGENT; MIGLUSTAT; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; NIEMANN PICK C PROTEIN 1; NIEMANN PICK C PROTEIN 2; PROTEIN; REGULATOR PROTEIN; TAMOXIFEN; UBIDECARENONE; UNCLASSIFIED DRUG;

CEREBELLUM DISEASE; DEATH; DRUG POTENTIATION; HUMAN; LIPIDOSIS; NIEMANN PICK DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

EID: 34250317789     PISSN: 17460875     EISSN: None     Source Type: Journal    
DOI: 10.2217/17460875.2.3.357     Document Type: Review

References (56)

1. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R: Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87-123 (2004).
2. Higaki K, Almanzar-Paramio D, Sturley SL: Metazoan and microbial models of Niemann-Pick type C disease. Biochim. Biophys. Acta 1685, 38-47 (2004).
3. Sturley SL, Patterson MC, Balch W, Liscum L: The pathophysiology and mechanisms of NP-C disease. Biochim. Biophys. Acta 1685, 83-87 (2004).
4. Liscum L, Sturley SL: Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim. Biophys. Acta 1685, 22-27 (2004).
5. Koudinov AR, Koudinova NV: Cholesterol homeostasis failure as a unifying cause of synaptic degeneration. J. Neurol. Sci. 229-230, 233-240 (2005).
6. Valenza M, Cattaneo, E: Cholesterol dysfunction in neurodegenerative diseases: is Huntington's disease in the list? Prog. Neurobiol. 80, 165-176 (2006).
7. Pentchev PG: Niemann-Pick C research from mouse to gene. Biochim. Biophys. Acta 1685, 3-7 (2004).
8. Neufeld EB, Wastney M. Patel S et al.: The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J. Biol. Cbem. 274, 9627-9635 (1999).
9. Sun X, Marks DL, Park WD et al.: Niemann-Pick C variant detection by altered sphingolipid trafficking and correlation with mutations within a specific domain of NPC1. Am. J. Hum. Genet. 68, 1361-1372 (2001).
10. Carstea ED, Morris JA, Coleman KG et al.: Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277, 228-231 (1997).
11. Millard EE, Gale SE, Dudley N, Zhang J. Schaffer JE, Ory DS: The sterol-sensing domain of the Niemann-Pick C1 (NPC1) protein regulates trafficking of low density lipoprotein cholesterol. J. Biol. Chem. 280. 28581-28590 (2005).
12. Malathi K, Higaki K, Tinkelenberg AH et al.: Mutagenesis of the putative sterol-sensing domain of yeast Niemann Pick C-related protein reveals a primordial role in subcellular sphingolipid distribution. J. Cell Biol. 164, 547-556 (2004).
13. Millat G, Marcais C, Tomasetto C et al.: Niemann-Pick C1 disease: correlations between NPC1 mutations, levels of NPC1 protein. and phenotypes emphasize the functional significance of the putative sterol-sensing domain and of the cysteine-rich luminal loop. Am. J. Hum. Genet. 68, 1373-1385 (2001).
14. Greer WL, Dobson MJ, Girouard GS, Byers DM, Riddell DC, Neumann PE: Mutations in NPC1 highlight a conserved NPC1-specific cysteine-rich domain. Am. J. Hum. Genet. 65, 1252-1260 (1999).
15. Park WD, O'Brien JF, Lundquist PA et al.: Identification of 58 novel mutations in Niemann-Pick disease type C: correlation with biochemical phenotype and importance of PTC1-like domains in NPC1. Hum. Mutat. 22, 313-325 (2003).
16. Naureckiene S, Sleat DE, Lackland H et al.: Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290, 2298-2301 (2000).
17. Friedland N, Liou HL, Lobel P, Stock AM: Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. Proc. Natl Acad. Sci. USA 100, 2512-2517 (2003).
18. Cheruku SR, Xu Z, Dutia R, Lobel P, Storch J: 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 (2006).
19. Liou HL, Dixit SS, Xu S, Tint GS, Stock AM, Lobel P: NPC2, the protein deficient in Niemann-Pick C2 disease, consists of multiple glycoforms that bind a variety of sterols. J. Biol. Chem. 281. 36710-36723 (2006).
20. Schrantz N, Sagiv Y, Liu Y, Savage PB, Bendelac A, Teyton L: The Niemann-Pick type C2 protein loads isoglobotrihexosylceramide onto CD1d molecules and contributes to the thymic selection of NKT cells. J. Exp. Med. 204, 841-852 (2007).
21. Sleat DE, Wiseman JA, El-Banna M et al.: Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc. Natl Acad. Sci. USA 101, 5886-5891 (2004).
22. Davies JP, Chen FW, Ioannou YA: Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science 290. 2295-2298 (2000).
23. Scott C, Ioannou YA: The NPC1 protein: structure implies function. Biochim. Biophys. Acta 1685, 8-13 (2004).
24. Passeggio J, Liscum L: Flux of fatty acids through NPC1 lysosomes. J. Biol. Chem. 280, 10333-10339 (2005).
25. Chen FW, Gordon RE, Ioannou YA: NPC1 late endosomes contain elevated levels of non-esterified ('free') fatty acids and an abnormally glycosylated form of the NPC2 protein. Biochem. J. 390, 549-561 (2005).
26. Millat G, Chikh K, Naureckiene S et al.: Niemann-Pick disease type C: spectrum of HE1 mutations and genotype/phenotype correlations in the NPC2 group. Am. J. Hum. Genet. 69, 1013-1021 (2001).
27. Garcia-Calvo M, Lisnock J, Bull HG et al.: The target of ezetimibe is Niemann-Pick C1 -Like 1 (NPC1L1). Proc. Natl. Acad. Sci. USA 102, 8132-8137 (2005).
28. Walkley SU, Suzuki K: Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim. Biophys. Acta 1685, 48-62 (2004).
29. Berger AC, Vanderford TH. Gernert KM, Nichols JW, Faundez V, Corbett AH: Saccharomyces cerevisiae Npc2p is a functionally conserved homologue of the human Niemann-Pick disease type C 2 protein, hNPC2. Eukaryot. Cell 4, 1851-1862 (2005).
30. Sym M, Basson M, Johnson C: A model for Niemann-Pick type C disease in the nematode Caenorhabditis elegans. Curr. Biol. 10, 527-530 (2000).
31. Huang X, Suyama K, Buchanan J, Zhu AJ, Scott MP: A Drosophila model of the Niemann-Pick type C lysosome storage disease: dnpc 1 a is required for molting and sterol homeostasis. Development 132, 5115-5124 (2005).
32. Fluegel ML, Parker TJ, Pallanck LJ: Mutations of a Drosophila NPC1 gene confer sterol and ecdysone metabolic defects. Genetics 172, 185-196 (2006).
33. Altmann SW, Davis HR Jr, Zhu LJ et al.: Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science 303, 1201-1204 (2004).
34. Voght SP, Fluegel ML, Andrews LA, Pallanck LJ: Drosophila NPC1b promotes an early step in sterol absorption from the midgut epithelium. Cell Metab. 5, 195-205 (2007).
35. Zhang S, Ren J, Li H et al.: Ncr1p, the yeast ortholog of mammalian Niemann Pick C1 protein, is dispensable for endocytic transport. Traffic 5, 1017-1030 (2004).
36. Berger AC, Hanson PK, Wylie Nichols J, Corbett AH: A yeast model system for functional analysis of the Niemann-Pick type C protein 1 homolog, Ncr1p. Traffic 6, 907-917 (2005).
37. Ohgami N, Ko DC, Thomas M, Scott MP, Chang CC, Chang TY: 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 (2004).
38. Ko DC, Binkley J, Sidow A, Scott MP: 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 (2003).
39. Patterson MC, Di Bisceglie AM, Higgins JJ et al.: The effect of cholesterol-lowering agents on hepatic and plasma cholesterol in Niemann-Pick disease type C. Neurology 43, 61-64 (1993).
40. Somers KL, Wenger DA, Royals MA et al.: Complementation studies in human and feline Niemann-Pick type C disease. Mol. Genet. Metab. 66, 117-121 (1999).
41. Hsu YS, Hwu WL. Huang SF et al.: Niemann-Pick disease type C (a cellular cholesterol lipidosis) treated by bone marrow transplantation. Bone Marrow Transplant. 24, 103-107 (1999).
42. Xie C, Burns DK, Turley SD, Dietschy JM: Cholesterol is sequestered in the brains of mice with Niemann-Pick type C disease but turnover is increased. J. Neuropathol. Exp. Neurol. 59, 1106-1117 (2000).
43. Zervas M, Somers KL, Thrall MA. Walkley SU: Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11. 1283-1287 (2001).
44. Lachmann RH, te Vruchte D, Lloyd-Evans E et al.: Treatment with miglustat reverses the lipid-trafficking defect in Niermann-Pick disease type C. Neurobiol. Dis. 16, 654-658 (2004).
45. Henderson LP. Lin L, Prasad A, Paul CA, Chang TY. Maue RA: Embryonic striatal neurons from Niemann-Pick type C mice exhibit defects in cholesterol metabolism and neurotrophin responsiveness. J. Biol. Chem. 275(26), 20179-20187 (2000).
46. Griffin LD, Gong W, Verot L, Mellon SH: Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med. 10, 704-711 (2004).
47. Ory DS: Nuclear receptor signaling in the control of cholesterol homeostasis: have the orphans found a home? Circ. Res. 95, 660-670 (2004).
48. Millat G, Bailo N, Molinero, S, Rodriguez C. Chikh K, Vanier MT: Niemann-Pick C disease: use of denaturing high performance liquid chromatography for the detection of NPC1 and NPC2 genetic variations and impact on management of patients and families. Mol. Cenet. Metab. 86, 220-232 (2005).
49. Imrie J. Dasgupta S, Besley GT et al.: The natural history of Niemann-Pick disease type C in the UK. J. Inherit. Metab. Dis. 30(1), 51-59 (2006).
50. Bauer P, Knoblich R. Bauer C et al.: NPC1: complete genomic sequence, mutation analysis, and characterization of haplotypes. Hum. Mutat. 19, 30-38 (2002).
51. Reddy JV, Ganley IG, Pfeffer SR: Clues to neuro-degeneration in Niemann-Pick type C disease from global gene expression profiling. PLoS ONE 1. E19 (2006).
52. Ganley IG. Pfeffer SR: Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells. J. Biol. Chem. 281, 17890-17899 (2006).
53. Bascunan-Castillo EC, Erickson RP, Howison CM et al.: Tamoxifen and vitamin E treatments delay symptoms in the mouse model of Niemann-Pick C. J. Appl. Genet. 45, 461-467 (2004).
54. Langmade SJ, Gale SE, Frolov A et al.: Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc. Natl Acad. Sci. USA 103, 13807-13812 (2006).
55. Davies JP, Ioannou YA: 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, 24367-24374 (2000).
56. Hogue CW: Cn3D: a new generation of three-dimensional molecular structure viewer. Trends Biochem. Sci. 22, 314-316 (1997).