Loss of niemann-pick C1 or C2 protein results in similar biochemical changes suggesting that these proteins function in a common lysosomal pathway

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Dixit, Sayali S ^a,b   Jadot, Michel ^c   Sohar, Istvan ^a   Sleat, David E ^a,b   Stock, Ann M ^a,b   Lobel, Peter ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c University of Namur   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHOLESTEROL; LYSOSOME ENZYME; MEMBRANE PROTEIN; NIEMANN PICK C1 PROTEIN; NIEMANN PICK C2 PROTEIN; PEPTIDASE; PROTEINASE; TRIPEPTIDYL PEPTIDASE I; UNCLASSIFIED DRUG; AMINOPEPTIDASE; DIPEPTIDYL PEPTIDASE; NPC1 PROTEIN, MOUSE; NPC2 PROTEIN, MOUSE; PROTEIN; SERINE PROTEINASE; TRIPEPTIDYL-PEPTIDASE 1; VESICULAR TRANSPORT PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN; CARBOHYDRATE METABOLISM; CELL FRACTIONATION; CHOLESTEROL TRANSPORT; COMMON LYSOSOMAL PATHWAY; CONTROLLED STUDY; DENSITY; IN VITRO STUDY; LIPID STORAGE; LIVER; LYSOSOME; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; LIPID METABOLISM; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; TISSUE DISTRIBUTION;

MUS;

AMINOPEPTIDASES; ANIMALS; BRAIN; CHOLESTEROL; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; LIPID METABOLISM; LIVER; LYSOSOMES; MICE; MICE, MUTANT STRAINS; PROTEINS; SERINE PROTEASES; TISSUE DISTRIBUTION; VESICULAR TRANSPORT PROTEINS;

EID: 80052010267     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023677     Document Type: Article

References (47)

1. Rosenbaum AI, Maxfield FR, (2011) Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J Neurochem 116: 789-795.
2. Vanier MT, (2010) Niemann-Pick disease type C. Orphanet J Rare Dis 5: 16.
3. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, et al. (1997) Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277: 228-231.
4. Infante RE, Abi-Mosleh L, Radhakrishnan A, Dale JD, Brown MS, et al. (2008) Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J Biol Chem 283: 1052-1063.
5. Infante RE, Radhakrishnan A, Abi-Mosleh L, Kinch LN, Wang ML, et al. (2008) Purified NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem 283: 1064-1075.
6. Ohgami N, Ko DC, Thomas M, Scott MP, Chang CC, et al. (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.
7. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, et al. (2000) Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290: 2298-2301.
8. Chikh K, Vey S, Simonot C, Vanier MT, Millat G, (2004) Niemann-Pick type C disease: importance of N-glycosylation sites for function and cellular location of the NPC2 protein. Mol Genet Metab 83: 220-230.
9. Baker CS, Magargee SF, Hammerstedt RH, (1993) Cholesterol transfer proteins from ram cauda epidydimal and seminal plasma. Biol Reprod Suppl 48: 86.
10. Liou HL, Dixit SS, Xu S, Tint GS, Stock AM, et al. (2006) 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.
11. Okamura N, Kiuchi S, Tamba M, Kashima T, Hiramoto S, et al. (1999) A porcine homolog of the major secretory protein of human epididymis, HE1, specifically binds cholesterol. Biochim Biophys Acta 1438: 377-387.
12. Xu S, Benoff B, Liou HL, Lobel P, Stock AM, (2007) Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease. J Biol Chem 282: 23525-23531.
13. Sleat DE, Wiseman JA, El-Banna M, Price SM, Verot L, et al. (2004) Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci USA 101: 5886-5891.
14. 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.
15. Xu Z, Farver W, Kodukula S, Storch J, (2008) Regulation of sterol transport between membranes and NPC2. Biochemistry 47: 11134-11143.
16. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, et al. (2008) 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.
17. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, et al. (2009) Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137: 1213-1224.
18. Wang ML, Motamed M, Infante RE, Abi-Mosleh L, Kwon HJ, et al. (2010) Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab 12: 166-173.
19. Abdul-Hammed M, Breiden B, Adebayo MA, Babalola JO, Schwarzmann G, et al. (2010) Role of endosomal membrane lipids and NPC2 in cholesterol transfer and membrane fusion. J Lipid Res 51: 1747-1760.
20. Gallala HD, Breiden B, Sandhoff K, (2011) Regulation of the NPC2 protein-mediated cholesterol trafficking by membrane lipids. J Neurochem 116: 702-707.
21. Storch J, Xu Z, (2009) Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochim Biophys Acta 1791: 671-678.
22. Vance JE, (2010) Transfer of cholesterol by the NPC team. Cell Metab 12: 105-106.
23. Scott C, Higgins ME, Davies JP, Ioannou YA, (2004) Targeting of NPC1 to late endosomes involves multiple signals, including one residing within the putative sterol-sensing domain. J Biol Chem 279: 48214-48223.
24. Neufeld EB, Wastney M, Patel S, Suresh S, Cooney AM, et al. (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.
25. Liscum L, Sturley SL, (2004) Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim Biophys Acta 1685: 22-27.
26. Goldman SD, Krise JP, (2010) Niemann-Pick C1 functions independently of Niemann-Pick C2 in the initial stage of retrograde transport of membrane-impermeable lysosomal cargo. J Biol Chem 285: 4983-4994.
27. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, et al. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277: 232-235.
28. Della Valle MC, Sleat DE, Sohar I, Wen T, Pintar JE, et al. (2006) Demonstration of Lysosomal Localization for the Mammalian Ependymin-related Protein Using Classical Approaches Combined with a Novel Density Shift Method. J Biol Chem 281: 35436-35445.
29. Bhuvaneswaran C, Morris MD, (2000) Lysosome lipid storage disorder in NCTR-BALB/c mice: Spleen and lung lysosomes store unesterified cholesterol but differ in their phospholipid composition. Mol Cell Biochem 214: 15-22.
30. Bhuvaneswaran C, Morris MD, Shio H, Fowler S, (1982) Lysosome lipid storage disorder in NCTR-BALB/c mice. III. Isolation and analysis of storage inclusions from liver. Am J Pathol 108: 160-170.
31. de Duve C, Pressman BC, Gianetto R, Wattiaux R, Appelmans F, (1955) Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J 60: 604-617.
32. Amritraj A, Peake K, Kodam A, Salio C, Merighi A, et al. (2009) Increased activity and altered subcellular distribution of lysosomal enzymes determine neuronal vulnerability in Niemann-Pick type C1-deficient mice. Am J Pathol 175: 2540-2556.
33. Draye JP, Courtoy PJ, Quintart J, Baudhuin P, (1987) Relations between plasma membrane and lysosomal membrane. 2. Quantitative evaluation of plasma membrane marker enzymes in the lysosomes. Eur J Biochem 170: 405-411.
34. Braulke T, Bonifacino JS, (2009) Sorting of lysosomal proteins. Biochim Biophys Acta 1793: 605-614.
35. de Duve C, (1971) Tissue fractionation. Past and present. J Cell Biol 50: 20d-55d.
36. Towatari T, Miyamura T, Kondo A, Kato I, Inoue M, et al. (1998) The structures of asparagine-linked oligosaccharides of rat liver cathepsin L reflect the substrate specificity of lysosomal alpha-mannosidase. Eur J Biochem 256: 163-169.
37. Damme M, Morelle W, Schmidt B, Andersson C, Fogh J, et al. (2010) Impaired lysosomal trimming of N-linked oligosaccharides leads to hyperglycosylation of native lysosomal proteins in mice with alpha-mannosidosis. Mol Cell Biol 30: 273-283.
38. Damme M, Stroobants S, Walkley SU, Lullmann-Rauch R, D'Hooge R, et al. (2011) Cerebellar alterations and gait defects as therapeutic outcome measures for enzyme replacement therapy in alpha-mannosidosis. J Neuropathol Exp Neurol 70: 83-94.
39. Chen FW, Gordon RE, Ioannou YA, (2005) 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.
40. Kirchhoff C, Osterhoff C, Young L, (1996) Molecular cloning and characterization of HE1, a major secretory protein of the human epididymis. Biol Reprod 54: 847-856.
41. Larsen LB, Ravn P, Boisen A, Berglund L, Petersen TE, (1997) Primary structure of EPV20, a secretory glycoprotein containing a previously uncharacterized type of domain. Eur J Biochem 243: 437-441.
42. Klein A, Amigo L, Retamal MJ, Morales MG, Miquel JF, et al. (2006) NPC2 is expressed in human and murine liver and secreted into bile: potential implications for body cholesterol homeostasis. Hepatology 43: 126-133.
43. Dixit SS, Sleat DE, Stock AM, Lobel P, (2007) Do mammalian NPC1 and NPC2 play a role in intestinal cholesterol absorption? Biochem J 408: 1-5.
44. Lin L, Sohar I, Lackland H, Lobel P, (2001) The human CLN2 protein/tripeptidyl-peptidase I is a serine protease that autoactivates at acidic pH. J Biol Chem 276: 2249-2255.
45. Pentchev PG, Gal AE, Booth AD, Omodeo-Sale F, Fouks J, et al. (1980) A lysosomal storage disorder in mice characterized by a dual deficiency of sphingomyelinase and glucocerebrosidase. Biochim Biophys Acta 619: 669-679.
46. Beaufay H, Jacques P, Baudhuin P, Sellinger OZ, Berthet J, et al. (1964) Tissue fractionation studies. 18. Resolution of mitochondrial fractions from rat liver into three distinct populations of cytoplasmic particles by means of density equilibration in various gradients. Biochem J 92: 184-205.
47. Sleat DE, Sohar I, Lackland H, Majercak J, Lobel P, (1996) Rat brain contains high levels of mannose-6-phosphorylated glycoproteins including lysosomal enzymes and palmitoyl-protein thioesterase, an enzyme implicated in infantile neuronal lipofuscinosis. J Biol Chem 271: 19191-19198.