Deficiency of Niemann-Pick C1 protein protects against diet-induced gallstone formation in mice

Liver International

Volumn 30, Issue 6, 2010, Pages 887-897

  Morales, María Gabriela ^a   Amigo, Ludwig ^a   Balboa, Elisa ^a   Acuña, Mariana ^a   Castro, Juan ^a   Molina, Héctor ^a   Miquel, Juan Francisco ^a   Nervi, Flavio ^a   Rigotti, Attilio ^a   Zanlungo, Silvana ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Biliary lipid secretion; Cholesterol; Lithogenesis; Liver; Niemann Pick type C disease

Indexed keywords

CHOLESTEROL; MEMBRANE PROTEIN; PROTEIN NPC1; UNCLASSIFIED DRUG; ABC TRANSPORTER; CHOLESTEROL 7ALPHA MONOOXYGENASE; CHOLESTEROL INTAKE; CHOLIC ACID; CYP7A1 PROTEIN, MOUSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; NPC1 PROTEIN, MOUSE; NPC2 PROTEIN, MOUSE; PROTEIN; SREBF2 PROTEIN, MOUSE; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; VESICULAR TRANSPORT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE SECRETION; CHOLESTEROL LIVER LEVEL; CONTROLLED STUDY; ENDOCYTOSIS; GALLSTONE FORMATION; GENE EXPRESSION REGULATION; LIPID BILE LEVEL; LIPID DIET; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BAGG ALBINO MOUSE; BILE; CHEMICALLY INDUCED; CHOLESTEROL INTAKE; DISEASE MODEL; GALLSTONES; GENETICS; KNOCKOUT MOUSE; LIVER; MALE; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE; BIOLOGICAL TRANSPORT; CHOLESTEROL 7-ALPHA-HYDROXYLASE; CHOLESTEROL, DIETARY; CHOLIC ACID; DISEASE MODELS, ANIMAL; GALLSTONES; GENE EXPRESSION REGULATION; HYDROXYMETHYLGLUTARYL COA REDUCTASES; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PROTEINS; RECEPTORS, LDL; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; VESICULAR TRANSPORT PROTEINS;

EID: 77954361464     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2010.02230.x     Document Type: Article

References (55)

1. Carey MC, Paigen B. Epidemiology of the American Indians' burden and its likely genetic origins. Hepatology 2002, 36:781-91.
2. Lammert F, Miquel JF. Gallstone disease: from genes to evidence-based therapy. J Hepatol 2008, 48:S124-35.
3. Sandler RS, Everhart JE, Donowitz M. The burden of selected digestive diseases in the United States. Gastroenterology 2002, 122:1500-11.
4. Lazcano-Ponce EC, Miquel JF, Munoz N. Epidemiology and molecular pathology of gallbladder cancer. CA Cancer J Clin 2001, 51:349-64.
5. Zanlungo S, Nervi F. The molecular and metabolic basis of biliary cholesterol secretion and gallstone disease. Front Biosci 2003, 8:s1166-74.
6. Apstein MD, Carey MC. Pathogenesis of cholesterol gallstones: a parsimonious hypothesis. Eur J Clin Invest 1996, 26:343-52.
7. Turley SD, Dietschy JM. The metabolism and excretion of cholesterol by the liver. The liver: Biology and Pathology 1988, 617-41. Arias IM, Jakoby WBPopper HSchachter DShafritz DA. eds, New York, Raven Press
8. Dietschy JM, Turley SD, Spady DK. Role of the liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J Lipid Res 1993, 34:1637-59.
9. Zanlungo S, Rigotti A. Determinants of transhepatic cholesterol traffic and their relevance for gallstone formation. Liver Int 2009, 29:323-30.
10. Bothman KM, Bravo E. The role of lipoprotein cholesterol in biliary steroid secretion. Studies with in vivo experimental models. Prog Lipid Res 1995, 34:71-97.
11. Wang DQ, Carey MC. Susceptibility to murine cholesterol gallstone formation is not affected by partial disruption of the HDL receptor SR-BI. Biochim Biophys Acta 2002, 1583:141-50.
12. Amigo L, Quiñones V, Mardones P. Impaired biliary cholesterol secretion and decreased gallstone formation in apolipoprotein E-deficient mice fed a high-cholesterol diet. Gastroenterology 2000, 118:772-9.
13. Ikonen E. Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 2008, 9:125-38.
14. Liscum L. Niemann-Pick type C mutations cause lipid traffic jam. Traffic 2000, 1:218-25.
15. Amigo L, Mendoza H, Castro J. Relevance of Niemann-Pick type C1 protein expression in controlling plasma cholesterol and biliary lipid secretion in mice. Hepatology 2002, 36:819-28.
16. Loftus SK, Morris JA, Cartsea ED. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 1997, 277:232-5.
17. Nervi F, Marinovic I, Rigotti A, Ulloa N. Regulation of biliary cholesterol secretion. Functional relationship between the canalicular and sinusoidal cholesterol secretory pathways in the rat. J Clin Invest 1988, 82:1818-25.
18. Allain C, Poon L, Chan C, Richmond W, Fu P. Enzymatic determination of total serum cholesterol. Clin Chem 1974, 20:470-5.
19. Baginski ES, Fos PP, Zack B. Microdetermination of inorganic phosphate, phospholipids and total phosphate in biological material. Clin Chem 1967, 13:326-32.
20. Talalay P. Enzymic analysis of steroid hormones. Methods Biochem Anal 1960, 8:119-43.
21. Carey MC. Critical tables for calculating the cholesterol saturation of native bile. J Lipid Res 1978, 19:945-55.
22. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
23. Koopen NR, Walters H, Voshol P. (1999) Decreased Na+ dependent taurocholate uptake and low expression of sinusoidal Na+ taurocholate cotransporting protein (Ntcp) in livers of Mdr2 P-glycoprotein deficient mice. J Hepatol 1999, 30:14-21.
24. Wang DQ, Paigen B, Carey MC. Phenotypic characterization of Lith genes that determine susceptibility to cholesterol cholelithiasis in inbred mice: physical-chemistry of gallbladder bile. J Lipid Res 1997, 38:1395-411.
25. Rege RV, Prystowsky JB. Inflammation and a thickened mucus layer in mice with cholesterol gallstones. J Surg Res 1998, 74:81-5.
26. Xie C, Turley SD, Pentchev PG, Dietschy JM. Cholesterol balance and metabolism in mice with loss of function of Niemann-Pick C protein. Am J Physiol 1999, 276:E336-44.
27. Garver WS, Jelinek D, Oyarzo JN. Characterization of liver disease and lipid metabolism in the Niemann-Pick C1 mouse. J Cell Biochem 2007, 101:498-516.
28. Beltroy EP, Liu B, Dietschy JM, Turley SD. Lysosomal unesterified cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J Lipid Res 2007, 48:869-81.
29. Ananthanarayanan M, Balasubramanian N, Makishima M, Mangelsdorf DJ, Suchy FJ. Human bile salt export pump promoter is transactivated by the farnesoid X receptor/bile acid receptor. J Biol Chem 2001, 276:28857-65.
30. Parks DJ, Blanchard SG, Bledsoe RK. Bile acids: natural ligands for an orphan nuclear receptor. Science 1999, 284:1365-8.
31. Repa JJ, Berge KE, Pomajzl C. Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. J Biol Chem 2002, 277:18793-800.
32. Graf GA, Yu L, Li WP. ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion. J Biol Chem 2003, 278:48275-82.
33. Wang DQ, Lammert F, Cohen DE, Paigen B, Carey MC. Cholic acid aids absorption, biliary secretion, and phase transitions of cholesterol in murine cholelithogenesis. Am J Physiol 1999, 276:G751-60.
34. Dixit SS, Sleat DE, Stock AM, Lobel P. Do mammalian NPC1 and NPC2 play a role in intestinal cholesterol absorption? Biochem J 2007, 408:1-5.
35. Xie C, Turley SD, Dietschy JM. Centripetal cholesterol flow from the extrahepatic organs through the liver is normal in mice with mutated Niemann-Pick type C protein. J Lipid Res 2000, 41:1278-89.
36. Berge KE, Tian H, Graf GA. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science 2000, 290:1771-5.
37. Yu L, Gupta S, Xu F. Expression of ABCG5 and ABCG8 is required for regulation of biliary cholesterol secretion. J Biol Chem 2005, 280:8742-7.
38. Wang DQ, Tazuma S, Cohen DE, Carey MC. Feeding natural hydrophilic bile acids inhibits intestinal cholesterol absorption: studies in the gallstone-susceptible mouse. Am J Physiol Gastrointest Liver Physiol 2003, 285:G494-502.
39. Remaley AT, Bark S, Walts AD. Comparative genome analysis of potential regulatory elements in the ABCG5-ABCG8 gene cluster. Biochem Biophys Res Commun 2002, 295:276-82.
40. Vainio S, Bykov I, Hermansson M. Defective insulin receptor activation and altered lipid rafts in Niemann-Pick type C disease hepatocytes. Biochem J 2005, 391:465-72.
41. Goldstein JL, DeBose-Boyd RA, Brown MS. Protein sensors for membrane sterols. Cell 2006, 124:35-46.
42. Murphy C, Parini P, Wang J. Cholic acid as key regulator of cholesterol synthesis, intestinal absorption and hepatic storage in mice. Biochim Biophys Acta 2005, 1735:167-75.
43. Blom TS, Linder MD, Snow K. Defective endocytic trafficking of NPC1 and NPC2 underlying infantile Niemann-Pick type C disease. Hum Mol Genet 2003, 12:257-72.
44. Li H, Repa JJ, Valasek MA. Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick type C disease. J Neuropathol Exp Neurol 2005, 64:323-33.
45. Klein A, Amigo L, Retamal MJ. NPC2 is expressed in human and murine liver and secreted into bile: potential implications for body cholesterol homeostasis. Hepatology 2006, 43:126-33.
46. Sleat DE, Wiseman JA, El-Banna M. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci USA 2004, 101:5886-91.
47. Pramfalk C, Angelin B, Eriksson M, Parini P. Cholesterol regulates ACAT2 gene expression and enzyme activity in human hepatoma cells. Biochem Biophys Res Commun 2007, 364:402-9.
48. Liscum L, Faust JR. Low density lipoprotein (LDL)-mediated suppression of cholesterol synthesis and LDL uptake is defective in Niemann-Pick type C fibroblasts. J Biol Chem 1987, 262:17002-8.
49. Lee FY, Lee H, Hubbert ML, Edwards PA, Zhang Y. FXR, a multipurpose nuclear receptor. Trends Biochem Sci 2006, 31:572-80.
50. Wang DQ, Cohen DE, Carey MC. Biliary lipids and cholesterol gallstone disease. J Lipid Res 2009, 50:S406-11.
51. Naken KE, Labori KJ, Rødningen OK. ABCB4 sequence variations in young adults with cholesterol gallstone disease. Liver Int 2009, 29:743-7.
52. Stieger B. Recent insights into the function and regulation of the bile salt export pump (ABCB11). Curr Opin Lipidol 2009, 20:176-81.
53. Paulusma CC, de Waart DR, Kunne C, Mok KS, Elferink RP. Activity of the bile salt export pump (ABCB11) is critically dependent on canalicular membrane cholesterol content. J Biol Chem 2009, 284:9947-54.
54. Amigo L, Mendoza H, Zanlungo S. Enrichment of canalicular membrane with cholesterol and sphingomyelin prevents bile salt-induced hepatic damage. J Lipid Res 1999, 40:533-42.
55. Liu Y, Binz J, Numerick MJ. Hepatoprotection by the farnesoid X receptor agonist GW4064 in rat models of intra- and extrahepatic cholestasis. J Clin Invest 2003, 112:1678-87.