Augmented cholesterol absorption and sarcolemmal sterol enrichment slow small intestinal transit in mice, contributing to cholesterol cholelithogenesis

Journal of Physiology

Volumn 590, Issue 8, 2012, Pages 1811-1824

  Xie, Meimin ^a   Kotecha, Vijay R ^a   Andrade, Jon David P ^a   Fox, James G ^b   Carey, Martin C ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 3; CHOLECYSTOKININ; CHOLESTEROL; DEOXYCHOLIC ACID; EZETIMIBE; SITOSTANOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL ABSORPTION; CHOLESTEROL STONE; CONTROLLED STUDY; DIET; FEMALE; HELICOBACTER HEPATICUS; HELICOBACTER INFECTION; IN VIVO STUDY; INTESTINAL DYSMOTILITY; INTESTINE INFECTION; INTESTINE LENGTH; INTESTINE MOTILITY; INTESTINE PARAMETERS; INTESTINE TRANSIT TIME; INTESTINE WEIGHT; LIPID ABSORPTION; LIPID ANALYSIS; LITHOGENIC DIET; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; SARCOLEMMA; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SMALL INTESTINAL HYPOMOTILITY; SMOOTH MUSCLE FIBER;

ANIMALS; AZETIDINES; BILE; BILE ACIDS AND SALTS; BIOLOGICAL TRANSPORT; CHOLECYSTOKININ; CHOLESTEROL; CHOLIC ACID; DIET, HIGH-FAT; FEMALE; GALLBLADDER; GALLSTONES; GASTROINTESTINAL TRANSIT; HELICOBACTER HEPATICUS; HELICOBACTER INFECTIONS; INTESTINAL ABSORPTION; INTESTINE, SMALL; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MYOCYTES, SMOOTH MUSCLE; SARCOLEMMA; STEROLS;

EID: 84859723609     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.224717     Document Type: Article

References (76)

1. Altmann SW, Davis HR Jr, Zhu LJ, Yao X, Hoos LM, Tetzloff G, Iyer SP, Maguire M, Golovko A, Zeng M, Wang L, Murgolo N & Graziano MP (2004). Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science 303, 1201-1204.
2. Azzaroli F, Mazzella G, Mazzeo C, Simoni P, Festi D, Colecchia A, Montagnani M, Martino C, Villanova N, Roda A & Roda E (1999). Sluggish small bowel motility is involved in determining increased biliary deoxycholic acid in cholesterol gallstone patients. Am J Gastroenterol 94, 2453-2459.
3. Bartlett GR (1959). Phosphorus assay in column chromatography. J Biol Chem 234, 466-468.
4. Brown NJ, Read NW, Richardson A, Rumsey RD & Bogentoft C (1990). Characteristics of lipid substances activating the ileal brake in the rat. Gut 31, 1126-1129.
5. Carey MC (1978). Critical tables for calculating the cholesterol saturation of native bile. J Lipid Res 19, 945-955.
6. Carulli N, Loria P, Bertolotti M, de Leon Ponz M, Menozzi D, Medici G & Piccagli I (1984). Effects of acute changes of bile acid pool composition on biliary lipid secretion. J Clin Invest 74, 614-624.
7. Chen Q, Amaral J, Biancani P & Behar J (1999). Excess membrane cholesterol alters human gallbladder muscle contractility and membrane fluidity. Gastroenterology 116, 678-685.
8. Cong P, Pricolo V, Biancani P & Behar J (2010). Effects of cholesterol on CCK-1 receptors and caveolin-3 proteins recycling in human gallbladder muscle. Am J Physiol Gastrointest Liver Physiol 299, G742-G750.
9. Craven BM (1976). Crystal structure of cholesterol monohydrate. Nature 260, 727-729.
10. Cuevas A, Miquel JF, Reyes MS, Zanlungo S & Nervi F (2004). Diet as a risk factor for cholesterol gallstone disease. J Am Coll Nutr 23, 187-196.
11. Dowling RH (2000). Review: pathogenesis of gallstones. Aliment Pharmacol Ther 14, 39-47.
12. Dowling RH, Hussaini SH, Murphy GM, Besser GM & Wass JA (1992). Gallstones during octreotide therapy. Metabolism 41, 22-33.
13. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
14. Duncan IW, Culbreth PH & Burtis CA (1979). Determination of free, total, and esterified cholesterol by high-performance liquid chromatography. J Chromatogr 162, 281-292.
15. Fan Y, Wu SD & Fu BB (2007). Effect of intestinal transit on the formation of cholesterol gallstones in hamsters. Hepatobiliary Pancreat Dis Int 6, 513-515.
16. Folch J, Lees M & Sloane Stanley GH (1957). A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497-509.
17. Fox JG (2002). The non-H pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50, 273-283.
18. Garcia-Calvo M, Lisnock J, Bull HG, Hawes BE, Burnett DA, Braun MP et al (2005). The target of ezetimibe is Niemann-Pick C1-Like 1 (NPC1L1). Proc Natl Acad Sci U S A 102, 8132-8137.
19. Heaton KW (2000). Review article: epidemiology of gall-bladder disease - role of intestinal transit. Aliment Pharmacol Ther 14, 9-13.
20. Heaton KW, Emmett PM, Symes CL & Braddon FE (1993). An explanation for gallstones in normal-weight women: slow intestinal transit. Lancet 341, 8-10.
21. Heuman DM (1989). Quantitative estimation of the hydrophilic-hydrophobic balance of mixed bile salt solutions. J Lipid Res 30, 719-730.
22. Hussaini SH, Pereira SP, Murphy GM & Dowling RH (1995). Deoxycholic acid influences cholesterol solubilization and microcrystal nucleation time in gallbladder bile. Hepatology 22, 1735-1744.
23. Jennings LJ, Xu QW, Firth TA, Nelson MT & Mawe GM (1999). Cholesterol inhibits spontaneous action potentials and calcium currents in guinea pig gallbladder smooth muscle. Am J Physiol Gastrointest Liver Physiol 277, G1017-G1026.
24. Khanuja B, Cheah YC, Hunt M, Nishina PM, Wang DQ, Chen HW, Billheimer JT, Carey MC & Paigen B (1995). Lith1, a major gene affecting cholesterol gallstone formation among inbred strains of mice. Proc Natl Acad Sci U S A 92, 7729-7733.
25. Kidwai AM (1974). Isolation of plasma membrane from smooth, skeletal, and heart muscle. Methods Enzymol 31, 134-144.
26. Krawczyk M, Wang DQ, Portincasa P & Lammert F (2011). Dissecting the genetic heterogeneity of gallbladder stone formation. Semin Liver Dis 31, 157-172.
27. Lacourse KA, Lay JM, Swanberg LJ, Jenkins C & Samuelson LC (1997). Molecular structure of the mouse CCK-A receptor gene. Biochem Biophys Res Commun 236, 630-635.
28. Lammert F, Carey MC & Paigen B (2001). Chromosomal organization of candidate genes involved in cholesterol gallstone formation: a murine gallstone map. Gastroenterology 120, 221-238.
29. Leiss O & von Bergmann K (1985). Comparison of biliary lipid secretion in non-obese cholesterol gallstone patients with normal, young, male volunteers. Klin Wochenschr 63, 1163-1169.
30. Leontiadis GI, Minopoulos GI, Maltezos E, Kotsiou S, Manolas KI, Simopoulos K & Hatseras D (2004). Effects of Helicobacter pylori infection on gastric emptying rate in patients with non-ulcer dyspepsia. World J Gastroenterol 10, 1750-1754.
31. Lyons MA & Wittenburg H (2006). Cholesterol gallstone susceptibility loci: a mouse map, candidate gene evaluation, and guide to human LITH genes. Gastroenterology 131, 1943-1970.
32. Marcus SN & Heaton KW (1986). Intestinal transit, deoxycholic acid and the cholesterol saturation of bile - three inter-related factors. Gut 27, 550-558.
33. Maurer KJ, Carey MC & Fox JG (2009). Roles of infection, inflammation, and the immune system in cholesterol gallstone formation. Gastroenterology 136, 425-440.
34. Maurer KJ, Ihrig MM, Rogers AB, Ng V, Bouchard G, Leonard MR, Carey MC & Fox JG (2005). Identification of cholelithogenic enterohepatic Helicobacter species and their role in murine cholesterol gallstone formation. Gastroenterology 128, 1023-1033.
35. Maurer KJ, Rao VP, Ge Z, Rogers AB, Oura TJ, Carey MC & Fox JG (2007). T-cell function is critical for murine cholesterol gallstone formation. Gastroenterology 133, 1304-1315.
36. Maurer KJ, Rogers AB, Ge Z, Wiese AJ, Carey MC & Fox JG (2006). Helicobacter pylori and cholesterol gallstone formation in C57L/J mice: a prospective study. Am J Physiol Gastrointest Liver Physiol 290, G175-G182.
37. Méndez-Sánchez N, Zamora-Valdés D, Chávez-Tapia NC & Uribe M (2007). Role of diet in cholesterol gallstone formation. Clin Chim Acta 376, 1-8.
38. Miller MS, Galligan JJ & Burks TF (1981). Accurate measurement of intestinal transit in the rat. J Pharmacol Methods 6, 211-217.
39. Minocha A, Mokshagundam S, Gallo SH & Rahal PS (1994). Alterations in upper gastrointestinal motility in Helicobacter pylori-positive nonulcer dyspepsia. Am J Gastroenterol 89, 1797-1800.
40. Paigen B & Carey MC (2002). Gallstones. In The Genetic Basis of Common Diseases, 2nd edn, ed. King R, Rotter J & Motulsky A, pp. 298-335. Oxford University Press, New York .
41. Patel KM, Shah DH, Patel JB, Patel JS, Garg CS & Sen DJ (2011). Chemistry of four membered heterocyclic ezetimibe as lipid lowering agent. Int J Drug Dev Res 3, 104-110.
42. Pieramico O, Ditschuneit H & Malfertheiner P (1993). Gastrointestinal motility in patients with non-ulcer dyspepsia: a role for Helicobacter pylori infection? Am J Gastroenterol 88, 364-368.
43. Pomare EW, Heaton KW, Low-Beer TS & Espiner HJ (1976). The effect of wheat bran upon bile salt metabolism and upon the lipid composition of bile in gallstone patients. Am J Dig Dis 21, 521-526.
44. de Leon Ponz M, Iori R, Barbolini G, Pompei G, Zaniol P & Carulli N (1982). Influence of small-bowel transit time on dietary cholesterol absorption in human beings. N Engl J Med 307, 102-103.
45. Price WE, Shehadeh Z, Thompson GH, Underwood LD & Jacobson ED (1969). Effects of acetylcholine on intestinal blood flow and motility. Am J Physiol 216, 343-347.
46. Reuben A, Maton PN, Murphy GM & Dowling RH (1985). Bile lipid secretion in obese and non-obese individuals with and without gallstones. Clin Sci (Lond) 69, 71-79.
47. Rybal'chenko VK, Pogrebnoi PV, Gruzina TG & Karamushka VI (1984). Extraction of plasma membranes from smooth muscle cells of the rabbit small intestine (in Russian). Biull Eksp Biol Med 97, 106-108.
48. Sambrook J, Fritsch E & Maniatis T (1989). In Molecular Cloning: A Laboratory Manual, 2nd edn, Appendix B12. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York .
49. Shaffer EA & Small DM (1977). Biliary lipid secretion in cholesterol gallstone disease. The effect of cholecystectomy and obesity. J Clin Invest 59, 828-840.
50. Shieh HS, Hoard LG & Nordman CE (1977). Crystal structure of anhydrous cholesterol. Nature 267, 287-289.
51. Shoda J, He BF, Tanaka N, Matsuzaki Y, Osuga T, Yamamori S, Miyazaki H & Sjövall J (1995). Increase of deoxycholate in supersaturated bile of patients with cholesterol gallstone disease and its correlation with de novo syntheses of cholesterol and bile acids in liver, gallbladder emptying, and small intestinal transit. Hepatology 21, 1291-1302.
52. Stolk MF, van de Heijning BJ, van Erpecum KJ, van den Broek AM, Renooij W & van Berge-Henegouwen GP (1994). The effect of bile acid hydrophobicity on nucleation of several types of cholesterol crystals from model bile vesicles. J Hepatol 20, 802-810.
53. Thomas LA, Veysey MJ, Murphy GM, Russell-Jones D, French GL, Wass JA & Dowling RH (2005). Octreotide induced prolongation of colonic transit increases faecal anaerobic bacteria, bile acid metabolising enzymes, and serum deoxycholic acid in patients with acromegaly. Gut 54, 630-635.
54. Thornton JR, Emmett PM & Heaton KW (1983). Diet and gall stones: effects of refined and unrefined carbohydrate diets on bile cholesterol saturation and bile acid metabolism. Gut 24, 2-6.
55. Traber MG & Ostwald R (1978). Cholesterol absorption and steroid excretion in cholesterol-fed guinea pigs. J Lipid Res 19, 448-456.
56. Turley SD & Dietschy JM (1978). Re-evaluation of the 3 alpha-hydroxysteroid dehydrogenase assay for total bile acids in bile. J Lipid Res 19, 924-928.
57. van Erpecum KJ & Carey MC (1997). Influence of bile salts on molecular interactions between sphingomyelin and cholesterol: relevance to bile formation and stability. Biochim Biophys Acta 1345, 269-282.
58. van Erpecum KJ & van Berge-Henegouwen GP (1999). Gallstones: an intestinal disease? Gut 44, 435-438.
59. Vercaemst R, Union A, Rosseneu M, De Craene I, De Backer G & Kornitzer M (1989). Quantitation of plasma free cholesterol and cholesteryl esters by high performance liquid chromatography. Study of a normal population. Atherosclerosis 78, 245-250.
60. Veysey MJ, Malcolm P, Mallet AI, Jenkins PJ, Besser GM, Murphy GM & Dowling RH (2001). Effects of cisapride on gall bladder emptying, intestinal transit, and serum deoxycholate: a prospective, randomised, double blind, placebo controlled trial. Gut 49, 828-834.
61. Wang DQ, Cohen DE & Carey MC (2009). Biliary lipids and cholesterol gallstone disease. J Lipid Res 50, Suppl, S406-S411.
62. Wang DQ, Lammert F, Cohen DE, Paigen B & Carey MC (1999a). Cholic acid aids absorption, biliary secretion, and phase transitions of cholesterol in murine cholelithogenesis. Am J Physiol Gastrointest Liver Physiol 276, G751-G760.
63. Wang DQ, Lammert F, Paigen B & Carey MC (1999b). Phenotypic characterization of Lith genes that determine susceptibility to cholesterol cholelithiasis in inbred mice: pathophysiology of biliary lipid secretion. J Lipid Res 40, 2066-2079.
64. Wang DQ, Paigen B & Carey MC (1997). Phenotypic characterization of Lith genes that determine susceptibility to cholesterol cholelithiasis in inbred mice: physical-chemistry of gallbladder bile. J Lipid Res 38, 1395-1411.
65. Wang DQ, Paigen B & Carey MC (2001). Genetic factors at the enterocyte level account for variations in intestinal cholesterol absorption efficiency among inbred strains of mice. J Lipid Res 42, 1820-1830.
66. Wang DQ, Schmitz F, Kopin AS & Carey MC (2004). Targeted disruption of the murine cholecystokinin-1 receptor promotes intestinal cholesterol absorption and susceptibility to cholesterol cholelithiasis. J Clin Invest 114, 521-528.
67. Wang DQ, Tazuma S, Cohen DE & Carey MC (2003). Feeding natural hydrophilic bile acids inhibits intestinal cholesterol absorption: studies in the gallstone-susceptible mouse. Am J Physiol Gastrointest Liver Physiol 285, G494-G502.
68. Wang HH, Portincasa P, Méndez-Sánchez N, Uribe M & Wang DQ (2008). Effect of ezetimibe on the prevention and dissolution of cholesterol gallstones. Gastroenterology 134, 2101-2110.
69. Whitehead RH, Demmler K, Rockman SP & Watson NK (1999). Clonogenic growth of epithelial cells from normal colonic mucosa from both mice and humans. Gastroenterology 117, 858-865.
70. Woollett LA, Buckley DD, Yao L, Jones PJ, Granholm NA, Tolley EA, Tso P & Heubi JE (2004). Cholic acid supplementation enhances cholesterol absorption in humans. Gastroenterology 126, 724-731.
71. Xiao ZL, Chen Q, Amaral J, Biancani P, Jensen RT & Behar J (1999). CCK receptor dysfunction in muscle membranes from human gallbladders with cholesterol stones. Am J Physiol Gastrointest Liver Physiol 276, G1401-G1407.
72. Xu QW, Scott RB, Tan DT & Shaffer EA (1996). Slow intestinal transit: a motor disorder contributing to cholesterol gallstone formation in the ground squirrel. Hepatology 23, 1664-1672.
73. Xu QW, Scott RB, Tan DT & Shaffer EA (1998). Effect of the prokinetic agent, erythromycin, in the Richardson ground squirrel model of cholesterol gallstone disease. Hepatology 28, 613-619.
74. Yu P, Chen Q, Biancani P & Behar J (1996). Membrane cholesterol alters gallbladder muscle contractility in prairie dogs. Am J Physiol Gastrointest Liver Physiol 271, G56-G61.
75. Yu P, Chen Q, Xiao Z, Harnett K, Biancani P & Behar J (1998). Signal transduction pathways mediating CCK-induced gallbladder muscle contraction. Am J Physiol Gastrointest Liver Physiol 275, G203-G211.
76. Zúñiga S, Molina H, Azocar L, Amigo L, Nervi F, Pimentel F, Jarufe N, Arrese M, Lammert F & Miquel JF (2008). Ezetimibe prevents cholesterol gallstone formation in mice. Liver Int 28, 935-947.