Hyodeoxycholic acid improves HDL function and inhibits atherosclerotic lesion formation in LDLR-knockout mice

FASEB Journal

Volumn 27, Issue 9, 2013, Pages 3805-3817

  Shih, Diana M ^a   Shaposhnik, Zory ^a,b   Meng, Yonghong ^a   Rosales, Melenie ^a   Wang, Xuping ^a   Wu, Judy ^a   Ratiner, Boris ^c   Zadini, Filiberto ^c   Zadini, Giorgio ^c   Lusis, Aldons J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Qualcomm Atheros Inc   (United States)

Author keywords

Bile acid; High density lipoprotein; Intestinal cholesterol absorption; Lowdensity lipoprotein; Reverse cholesterol transport

Indexed keywords

GLUCOSE; HIGH DENSITY LIPOPROTEIN; HYODEOXYCHOLIC ACID; INTERMEDIATE DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; VERY LOW DENSITY LIPOPROTEIN;

ABC TRANSPORTER A1 GENE; ABC TRANSPORTER G1 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ROOT; APOLIPOPROTEIN E GENE; ARTICLE; ATHEROSCLEROSIS; BLOOD CHEMISTRY; BODY COMPOSITION; BODY WEIGHT; BRACHIOCEPHALIC TRUNK; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET; DRUG MECHANISM; EX VIVO STUDY; FEMALE; FOOD INTAKE; GENE; GLUCOSE BLOOD LEVEL; LIPID METABOLISM; MACROPHAGE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

BILE ACID; HIGH-DENSITY LIPOPROTEIN; INTESTINAL CHOLESTEROL ABSORPTION; LOW-DENSITY LIPOPROTEIN; REVERSE CHOLESTEROL TRANSPORT;

ANIMALS; ATHEROSCLEROSIS; CHOLESTEROL, HDL; CHOLESTEROL, LDL; CHOLESTEROL, VLDL; DEOXYCHOLIC ACID; FEMALE; INTESTINAL ABSORPTION; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MICE; MICE, KNOCKOUT; RECEPTORS, LDL;

EID: 84883331800     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-223008     Document Type: Article

References (54)

1. Lusis, A. J. (2000) Atherosclerosis. Nature 407, 233-241
2. Grundy, S. M. (1988) HMG-CoA reductase inhibitors for treatment of hypercholesterolemia. N. Engl. J. Med. 319, 24-33
3. Scandinavian Simvastatin Survival Study Group (1994) Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). Lancet 344, 1383-1389
4. Shepherd, J., Cobbe, S. M., Ford, I., Isles, C. G., Lorimer, A. R., MacFarlane, P. W., McKillop, J. H., and Packard, C. J. (1995) Prevention of coronary heart disease with pravastatin in men with hypercholesterolemia. West of Scotland Coronary Prevention Study Group. N. Engl. J. Med. 333, 1301-1307
5. The LIPID Study Group (1998) Prevention of cardiovascular events and death with pravastatin in patients with coronary heart disease and a broad range of initial cholesterol levels. The Long-Term Intervention with Pravastatin in Ischaemic Disease (LIPID) Study Group. N. Engl. J. Med. 339, 1349-1357
6. Downs, J. R., Clearfield, M., Weis, S., Whitney, E., Shapiro, D. R., Beere, P. A., Langendorfer, A., Stein, E. A., Kruyer, W., and Gotto, A. M., Jr. (1998) Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS. Air Force/Texas Coronary Atherosclerosis Prevention Study. JAMA 279, 1615- 1622
7. Baigent, C., Blackwell, L., Emberson, J., Holland, L. E., Reith, C., Bhala, N., Peto, R. E., Barnes, H., Keech, A., Simes, J., and Collins, R. (2010) Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet 376, 1670-1681
8. Davidson, M. H. (2011) Therapies targeting exogenous cholesterol uptake: new insights and controversies. Curr. Atheroscler. Rep. 13, 95-100
9. Couture, P., and Lamarche, B. (2013) Ezetimibe and bile acid sequestrants: impact on lipoprotein metabolism and beyond. Curr. Opin. Lipidol. 24, 227-232
10. Rader, D. J. (2006) Molecular regulation of HDL metabolism and function: implications for novel therapies. J. Clin. Invest. 116, 3090-3100
11. Digby, J. E., Ruparelia, N., and Choudhury, R. P. (2012) Niacin in cardiovascular disease: recent preclinical and clinical developments. Arterioscler. Thromb. Vasc. Biol. 32, 582-588
12. Barter, P., and Rye, K. A. (2011) Cholesteryl ester transfer protein inhibition to reduce cardiovascular risk: where are we now? Trends Pharmacol. Sci. 32, 694-699
13. Watson, C. E., Weissbach, N., Kjems, L., Ayalasomayajula, S., Zhang, Y., Chang, I., Navab, M., Hama, S., Hough, G., Reddy, T., Soffer, D., Rader, D. J., Fogelman, A. M., and Schecter, A. (2011) Treatment of patients with cardiovascular disease with L-4F, an apo-A1 mimetic, did not improve select biomarkers of HDL function. J. Lipid Res. 52, 361-373
14. Eyssen, H. J., De Pauw, G., and Van Eldere, J. (1999) Formation of hyodeoxycholic acid from muricholic acid and hyocholic acid by an unidentified gram-positive rod termed HDCA-1 isolated from rat intestinal microflora. Appl. Environ. Microbiol. 65, 3158-3163
15. Singhal, A. K., Cohen, B. I., Finver-Sadowsky, J., McSherry, C. K., and Mosbach, E. H. (1984) Role of hydrophilic bile acids and of sterols on cholelithiasis in the hamster. J. Lipid Res. 25, 564-570
16. Singhal, A. K., Cohen, B. I., Mosbach, E. H., Une, M., Stenger, R. J., McSherry, C. K., May-Donath, P., and Palaia, T. (1984) Prevention of cholesterol-induced gallstones by hyodeoxycholic acid in the prairie dog. J. Lipid Res. 25, 539-549
17. Sehayek, E., Ono, J. G., Duncan, E. M., Batta, A. K., Salen, G., Shefer, S., Neguyen, L. B., Yang, K., Lipkin, M., and Breslow, J. L. (2001) Hyodeoxycholic acid efficiently suppresses atherosclerosis formation and plasma cholesterol levels in mice. J. Lipid Res. 42, 1250-1256
18. Cohen-Solal, C., Parquet, M., Ferezou, J., Serougne, C., and Lutton, C. (1995) Effects of hyodeoxycholic acid and alphahyocholic acid, two 6 alpha-hydroxylated bile acids, on cholesterol and bile acid metabolism in the hamster. Biochim. Biophys. Acta 1257, 189-197
19. Wang, D. Q., Tazuma, S., Cohen, D. E. and Carey, M. C. (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
20. Sato, H., Macchiarulo, A., Thomas, C., Gioiello, A., Une, M. Hofmann, A. F., Saladin, R., Schoonjans, K., Pellicciari, R., and Auwerx, J. (2008) Novel potent and selective bile acid derivatives as TGR5 agonists: biological screening, structure-activity relationships, and molecular modeling studies. J. Med. Chem. 51, 1831-1841
21. Song, C., Hiipakka, R. A., and Liao, S. (2000) Selective activation of liver X receptor alpha by 6alpha-hydroxy bile acids and analogs. Steroids 65, 423-427
22. Makishima, M., Lu, T. T., Xie, W., Whitfield, G. K., Domoto, H., Evans, R. M., Haussler, M. R., and Mangelsdorf, D. J. (2002) Vitamin D receptor as an intestinal bile acid sensor. Science 296, 1313-1316
23. Taicher, G. Z., Tinsley, F. C., Reiderman, A., and Heiman, M. L. (2003) Quantitative magnetic resonance (QMR) method for bone and whole-body-composition analysis. Anal. Bioanal. Chem. 377, 990-1002
24. Mehrabian, M., Qiao, J. H., Hyman, R., Ruddle, D., Laughton, C., and Lusis, A. J. (1993) Influence of the apoA-II gene locus on HDL levels and fatty streak development in mice. Arterioscler. Thromb. 13, 1-10
25. Hedrick, C. C., Castellani, L. W., Warden, C. H, Puppione, D. L., and Lusis, A. J. (1993) Influence of mouse apolipoprotein A-II on plasma lipoproteins in transgenic mice. J. Biol. Chem. 268, 20676-20682
26. Navab, M., Hama, S. Y., Hough, G. P., Subbanagounder, G., Reddy, S. T., and Fogelman, A. M. (2001) A cell-free assay for detecting HDL that is dysfunctional in preventing the formation of or inactivating oxidized phospholipids. J. Lipid Res. 42, 1308-1317
27. Qiao, J. H., Xie, P. Z., Fishbein, M. C. Kreuzer, J., Drake, T. A., Demer, L. L., and Lusis, A. J. (1994) Pathology of atheromatous lesions in inbred and genetically engineered mice. Genetic determination of arterial calcification. Arterioscler. Thromb. 14, 1480-1497
28. Shih, D. M., Xia, Y. R., Wang, X. P., Miller, E., Castellani, L. W., Subbanagounder, G., Cheroutre, H., Faull, K. F., Berliner, J. A., Witztum, J. L., and Lusis, A. J. (2000) Combined serum paraoxonase knockout/apolipoprotein E knockout mice exhibit increased lipoprotein oxidation and atherosclerosis. J. Biol. Chem. 275, 17527-17535
29. Bennett, B. J., Wang, S. S., Wang, X., Wu, X., and Lusis, A. J. (2009) Genetic regulation of atherosclerotic plaque size and morphology in the innominate artery of hyperlipidemic mice. Arterioscler. Thromb. Vasc. Biol. 29, 348-355
30. Orozco, L. D., Kapturczak, M. H., Barajas, B., Wang, X., Weinstein, M. M., Wong, J., Deshane, J., Bolisetty, S., Shaposhnik, Z., Shih, D. M., Agarwal, A., Lusis, A. J., and Araujo, J. A. (2007) Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ. Res. 100, 1703-1711
31. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
32. Ramachandran, S., Penumetcha, M., Merchant, N. K., Santanam, N., Rong, R., and Parthasarathy, S. (2005) Exercise reduces preexisting atherosclerotic lesions in LDL receptor knock out mice. Atherosclerosis 178, 33-38
33. Tsimikas, S., Shortal, B. P., Witztum, J. L., and Palinski, W. (2000) In vivo uptake of radiolabeled MDA2, an oxidationspecific monoclonal antibody, provides an accurate measure of atherosclerotic lesions rich in oxidized LDL and is highly sensitive to their regression. Arterioscler. Thromb. Vasc. Biol. 20, 689-697
34. Teupser, D., Pavlides, S., Tan, M., Gutierrez-Ramos, J. C., Kolbeck, R., and Breslow, J. L. (2004) Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc. Natl. Acad. Sci. U. S. A. 101, 17795-17800
35. VanderLaan, P. A., Reardon, C. A., and Getz, G. S. (2004) Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler. Thromb. Vasc. Biol. 24, 12-22
36. Teupser, D., Persky, A. D, and Breslow J. L. (2003) Induction of atherosclerosis by low-fat, semisynthetic diets in LDL receptordeficient C57BL/6J and FVB/NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arterioscler. Thromb. Vasc. Biol. 23, 1907-1913
37. Van de Heijning, B. J., Stolk, M. F., van Erpecum, K. J., Renooij, W., Groen, A. K., and vanBerge-Henegouwen, G. P. (1994) Bile salt-induced cholesterol crystal formation from model bile vesicles: a time course study. J. Lipid Res. 35, 1002-1011
38. Bachrach, W. H., and Hofmann, A. F. (1982) Ursodeoxycholic acid in the treatment of cholesterol cholelithiasis. Part I. Dig. Dis. Sci. 27, 737-761
39. Uy, M. C., Talingdan-Te, M. C., Espinosa, W. Z., Daez, M. L., and Ong, J. P. (2008) Ursodeoxycholic acid in the prevention of gallstone formation after bariatric surgery: a meta-analysis. Obes. Surg. 18, 1532-1538
40. Batta, A. K., Salen, G., and Tint, G. S. (2004) Hydrophilic 7 beta-hydroxy bile acids, lovastatin, and cholestyramine are ineffective in the treatment of cerebrotendinous xanthomatosis. Metabolism 53, 556-562
41. Broughton, G., 2nd. (1994) Chenodeoxycholate: the bile acid. The drug. A review. Am. J. Med. Sci. 307, 54-63
42. Koopman, B. J., Wolthers, B. G., van der Molen, J. C., G. T. Nagel, G. T., Waterreus, R. J., and Oosterhuis, H. J. (1984) Capillary gas chromatographic determinations of urinary bile acids and bile alcohols in CTX patients proving the ineffectivity of ursodeoxycholic acid treatment. Clin. Chim. Acta 142, 103- 111
43. Beltroy, E. P., Liu, B., Dietschy, J. M., and Turley, S. D. (2007) Lysosomal unesterified cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J. Lipid Res. 48, 869-881
44. Krauss, R. M., Lindgren, F. T., Williams, P. T., Kelsey, S. F., Brensike, J., Vranizan, K., Detre, K. M., and Levy, R. I. (1987) Intermediate-density lipoproteins and progression of coronary artery disease in hypercholesterolaemic men. Lancet 2, 62-66
45. Plump, A. S., Smith, J. D., Hayek, T., Aalto-Setälä, K., Walsh, A., Verstuyft, J. G., Rubin, E. M., and Breslow, J. L. (1992) Severe hypercholesterolemia and atherosclerosis in apolipoprotein Edeficient mice created by homologous recombination in ES cells. Cell 71, 343-353
46. Khera, A. V., Cuchel, M., de la Llera-Moya, M., Rodrigues, A., Burke, M. F., Jafri, K., French, B. C., Phillips, J. A., Mucksavage, M. L., Wilensky, R. L., Mohler, E. R., Rothblat, G. H., and Rader, D. J. (2011) Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N. Engl. J. Med. 364, 127-135
47. Nagano, Y., Arai, H., and Kita, T. (1991) High density lipoprotein loses its effect to stimulate efflux of cholesterol from foam cells after oxidative modification. Proc. Natl. Acad. Sci. U. S. A. 88, 6457-6461
48. Shao, B., Pennathur, S., Pagani, I., Oda, M. N., Witztum, J. L., Oram, J. F., and Heinecke, J. W. (2010) Modifying apolipoprotein A-I by malondialdehyde, but not by an array of other reactive carbonyls, blocks cholesterol efflux by the ABCA1 pathway. J. Biol. Chem. 285, 18473-18484
49. Zheng, L., Nukuna, B., Brennan, M. L., Sun, M., Goormastic, M., Settle, M., Schmitt, D., Fu, X., Thomson, L., Fox, P. L., Ischiropoulos, H., Smith, J. D., Kinter, M., and Hazen, S. L. (2004) Apolipoprotein A-I is a selective target for myeloperoxidase- catalyzed oxidation and functional impairment in subjects with cardiovascular disease. J. Clin. Invest. 114, 529-541
50. Navab, M., Ananthramaiah, G. M., Reddy, S. T., Van Lenten, B. J., Ansell, B. J., Fonarow, G. C., Vahabzadeh, K., Hama, S., Hough, G., Kamranpour, N., Berliner, J. A., Lusis, A. J., and Fogelman, A. M. (2004) The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J. Lipid Res. 45, 993-1007
51. Calkin, A. C., and Tontonoz, P. (2012) Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat. Rev. Mol. Cell Biol. 13, 213-224
52. Watanabe, M., Houten, S. M., Mataki, C., Christoffolete, M. A., Kim, B. W., Sato, H., Messaddeq, N., Harney, J. W., Ezaki, O., Kodama, T., Schoonjans, K., Bianco, A. C., and Auwerx, J. (2006) Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439, 484-489
53. Thomas, C., Gioiello, A., Noriega, L., Strehle, A., Oury, J., Rizzo, G., Macchiarulo, A., Yamamoto, H., Mataki, C., Pruzanski, M., Pellicciari, R., Auwerx, J., and Schoonjans, K. (2009) TGR5- mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10, 167-177
54. Thomas, C., Pellicciari, R., Pruzanski, M., Auwerx, J., and Schoonjans, K. (2008) Targeting bile-acid signalling for metabolic diseases. Nat. Rev. Drug Discov. 7, 678-693