Hepatic bile acid metabolism in the neonatal hamster: Expansion of the bile acid pool parallels increased Cyp7a1 expression levels

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 1, 2009, Pages

  Burke, Katie T ^a   Horn, Paul S ^b   Tso, Patrick ^a   Heubi, James E ^c   Woollett, Laura A ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Development; FGF15; FGFR4; FXR; Hormones; Neonate; SHP

Indexed keywords

BILE ACID; CELL PROTEIN; CHOLESTEROL 7ALPHA MONOOXYGENASE; CYTOCHROME P450 CYP7B1; CYTOCHROME P450 CYP8B1; CYTOCHROME P450 ISOENZYME; DEXAMETHASONE; FARNESOID X RECEPTOR; MESSENGER RNA; PROTEIN SHP; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE ACID SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; LIVER METABOLISM; METABOLIC REGULATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEROL SYNTHESIS; SYRIAN HAMSTER;

AGE FACTORS; AGING; ANIMALS; ANIMALS, NEWBORN; BILE ACIDS AND SALTS; CHOLESTEROL 7-ALPHA-HYDROXYLASE; CHOLESTEROL, DIETARY; CRICETINAE; DEXAMETHASONE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYDROCORTISONE; ISOENZYMES; LIVER; MESOCRICETUS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; STEROID 12-ALPHA-HYDROXYLASE;

EID: 67650079409     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90515.2008     Document Type: Article

References (78)

1. Agbemafle BM, Oesterreicher TJ, Shaw CA, Henning SJ. Immediate early genes of glucocorticoid action on the developing intestine. Am J Physiol Gastrointest Liver Physiol 288: G897-G906, 2005.
2. Agellon LB, Brover VA, Cheema SK, Gbaguidi GF, Walsh A. Dietary cholesterol fails to stimulate the human cholesterol 7α-hydroxylase gene (CYP7A1) in transgenic mice. J Biol Chem 277: 20131-20134, 2002.
3. Baker DM, Wang SL, Bell DJ, Drevon CA, Davis RA. One or more labile proteins regulate the stability of chimeric mRNAs containing the 3′-untranslated region of cholesterol-7α-hydroxylase mRNA. J Biol Chem 275: 19885-19991, 2000.
4. Balasubramaniyan N, Shahid M, Suchy FJ, Ananthanarayanan M. Multiple mechanisms of ontogenic regulation of nuclear receptors during rat liver development. Am J Physiol Gastrointest Liver Physiol 288: G251-G260, 2005.
5. Bilz S, Samuel V, Morina K, Savage D, Choi CS, Shulman GI. Activation of the farnesoid X receptor improves lipid metabolism in combined hyperlipidemic hamsters. Am J Physiol Endocrinol Metab 290: E716-E722, 2006.
6. Boehm G, Braun W, Moro G, Minoli I. Bile acid concentrations in serum and duodenal aspirates of healthy preterm infants: effects of gestational and postnatal age. Biol Neonate 71: 207-214, 1997.
7. Chiang JY, Kimmel R, Stroup D. Regulation of cholesterol 7α-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRα). Gene 262: 257-265, 2001.
8. Chiang JYL. Regulation of bile acid synthesis: pathways, nuclear receptors, and mechanisms. J Hepatol 40: 539-551, 2004.
9. Crestani M, Stroup D, Chiang JYL. Hormonal regulation of the cholesterol 7α-hydroxylase gene (CYP7). J Lipid Res 26: 2419-2432, 1995.
10. Cuesta de Juan S, Monte MJ, Macias RIR, Waunthier V, Buc Calderon PB, Marin JJG. Ontogenic development-associated changes in the expression of genes involved in rat bile acid homeostasis. J Lipid Res 48: 1362-1370, 2007.
11. Dawson PA, Haywood J, Carddock AL, Wilson M, Tietjent M, Kluckman KD, Maeda N, Parks JS. Targeted deletion of the ileal bile acid transporter eliminates enterohepatic cycling of bile acids in mice. J Biol Chem 278: 33920-33927, 2003.
12. De Fabiani E, Crestani M, Marrapodi M, Pinelli A, Golfieri V, Galli G. Identification and characterization of cis-acting elements conferring insulin responsiveness on hamster cholesteryl 7α-hydroxylase gene promoter. Biochem J 347: 147-154, 2000.
13. del Castillo-Olivares A, Gil G. Role of FXR and FTF in bile acid-mediated suppression of cholesterol 7alpha-hydroxylase transcription. Nucleic Acids Res 28: 3584-3593, 2000.
14. Dietschy JM, Turley SD, Spady DK. Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J Lipid Res 34: 1637-1659, 1993.
15. Duane WC, Javitt NB. 27-hydroxycholesterol: production rates in normal human subjects. J Lipid Res 40: 1194-1199, 1999.
16. Fomon SJ, Ziegler EE, Thomas LN, Jensen RL, Filer LJJ. Excretion of fat by normal full-term infants fed various milks and formulas. Am J Clin Nutr 23: 1299-1313, 1970.
17. Goodwin B, Jones SA, Price RR, Watson MA, McKee DD, Moore LB, Galardi C, Wilson JG, Lewis MC, Roth ME, Maloney PR, Willson TM, Kliewer SA. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol Cell 6: 517-526, 2000.
18. Graham TO, Van Thiel DH, Little JM, Lester R. Synthesis of taurocholate by rat fetal liver in organ culture: effects of cortisol in vitro. Am J Physiol Endocrinol Metab Gastrointest Physiol 237: E177-E184, 1979.
19. Gupta S, Stravitz RT, Dent P, Hylemon PB. Down-regulation of cholesterol 7α-hydroxylase (CYP7A1) gene expression by bile acids in primary rat hepatocytes is mediated by the c-Jun N-terminal kinase pathway. J Biol Chem 276: 15816-15822, 2001.
20. Hagenbuch B, Dawson P. The sodium bile salt cotransport family SLC10. Pflügers Arch 447: 566-570, 2004.
21. Hahn P, Innis SM. Cholesterol oxidation and 7α-hydroxylation during postnatal development of the rat. Biol Neonate 46: 48-52, 1984.
22. Hall E, Hylemon PB, Vlahcevic R, Mallonee DH, Valerie K, Avadhani N, Pandak WM. Overexpression of CYP27 in hepatic and extrahepatic cells: role in the regulation of cholesterol homeostasis. Am J Physiol Gastrointest Liver Physiol 281: G293-G301, 2001.
23. Hardikar W, Ananthanarayanan M, Suchy FJ. Differential ontogenic regulation of basolateral and canalicular bile acid transport proteins in rat liver. J Biol Chem 270: 20841-20846, 1995.
24. Hardy KJ, Hoffman NE, Mihaly G, Sewell RB, Smallwood RA. Bile acid metabolism in fetal sheep; perinatal changes in the bile acid pool. J Physiol 309: 1-11, 1980.
25. Heubi J, Balistreri W, Suchy F. Bile salt metabolism in the first year of life. J Lab Clin Med 100: 127-136, 1982.
26. Heubi J, Fondacaro J. Postnatal development of intestinal bile salt transport in the guinea pig. Am J Physiol Gastrointest Liver Physiol 243: G189-G194, 1982.
27. Horton JD, Cuthbert JA, Spady DK. Regulation of hepatic 7α-hydroxylase expression and response to dietary cholesterol in the rat and hamster. J Biol Chem 270: 5381-5387, 1995.
28. Hylemon PB, Gurley EC, Stravitz RT, Sitz JS, Pandak WM, Chiang JYL, Vlahcevic ZR. Hormonal regulation of cholesterol 7α-hydroxylase mRNA levels and transcriptional activity in primary rat hepatocyte cultures. J Biol Chem 267: 16866-16871, 1992.
29. Iizasa H, Genda N, Kitano T, Tomita M, Nishihara K, Hayashi M, Nakamura K, Kobayashi S, Nakashima E. Altered expression and function of P-glycoprotein in dextran sodium sulfate-induced colitis in mice. J Pharm Sci 92: 569-576, 2003.
30. Inagaki T, Choi M, Moschetta A, Peng L, Cummins CL, McDonald JG, Luo G, Jones SA, Goodwin B, Richardson JA, Gerard RD, Repa JJ, Mangelsdorf DJ, Kliewer SA. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab 2: 217-225, 2005.
31. Janowski BA, Willy PJ, Devi TR, Falch JR, Mangelsdorf DJ. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383: 728-731, 1996.
32. Jelinek DF, Andersson S, Slaughter CA, Russell DW. Cloning and regulation of cholesterol 7α-hydroxylase, the rate-limiting enzyme in bile acid biosynthesis. J Biol Chem 265: 8190-8197, 1990.
33. Kerr TA, Saeki L, Schneider M, Schaefer K, Berdy S, Redder T, Shan B, Russell DW, Schwartz M. Loss of nuclear receptor SHP impairs but does not eliminate negative feedback regulation of bile acid synthesis. Dev Cell 2: 713-720, 2002.
34. Lehmann JM, Kliewer SA, Moore LB, Smith-Oliver TA, Oliver BB, Su JL, Sundseth SS, Winegar DA, Blanchard DE, Spencer TA, Willson TM. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem 272: 3137-3140, 1997.
35. Li T, Chiang JY. Mechanism of rifampicin and pregnane X receptor inhibition of human cholesterol 7α-hydroxylase gene transcription. Am J Physiol Gastrointest Liver Physiol 288: G74-G84, 2005.
36. Li T, Kong X, Wosley E, Ellis E, Strom S, Chiang JYL. Insulin regulation of cholesterol 7α-hydroxylase expression in human hepatocytes. Roles of forkhead box 01 and sterol regulatory element-binding protein 1c. J Biol Chem 281: 28745-28754, 2006.
37. Little J, Lester R. Ontogenesis of intestinal bile salt absorption in the neonatal rat. Am J Physiol Gastrointest Liver Physiol 239: G319-G323, 1980.
38. Lu TT, Makishima M, Repa JJ, Schoonjans K, Kerr TA, Auwerx J, Mangelsdorf DJ. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol Cell 6: 507-515, 2000.
39. Macias RIR, Serrano MA, Monte MJ, Jimenez S, Hernandez B, Marin JJG. Long-term effect of treating pregnant rats with ursodeoxycholic acid on the congenital impairment of bile secretion induced in the pups by maternal cholestasis. J Pharmacol Exp Ther 312: 751-758, 2005.
40. Markwell MA, Haas SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87: 206-210, 1978.
41. Massimi M, Lear SR, Huling SL, Jones AL, Erickson SK. Cholesterol 7 α-hydroxylase (CYP7A): patterns of messenger RNA expression during rat liver development. Hepatology 28: 1064-1072, 1998.
42. Matsuzaki Y, Bouscarel B, Ikegami T, Honda A, Doy M, Ceryak S, Fukushima S, Yoshida S, Shoda J, Tanaka N. Selective inhibition of CYP27A1 and of chenodeoxycholic acid synthesis in cholestatic hamster liver. Biochim Biophys Acta 1588: 139-148, 2002.
43. McConihay JA, Horn PS, Woollett LA. The effect of maternal hypercholesterolemia on fetal sterol metabolism in the Golden Syrian hamster. J Lipid Res 42: 1111-1119, 2001.
44. Morris AI, Little JM, Lester R. Development of the bile acid pool in rats from neonatal life through puberty to maturity. Digestion 28: 216-224, 1984.
45. Oelkers P, Kirby LC, Heubi JE, Dawson PA. Primary bile acid malabsorption caused by mutations in the ileal sodium-dependent bile acid transporter gene (SLC10A2). J Clin Invest 99: 1880-1887, 1997.
46. Pandak WM, Bohdan P, Franklund C, Mallonee DH, Eggersten G, Bjorkhem I, Gil G, Vlahcevic R, Hylemon PB. Expression of sterol 12α- hydroxylase alters bile acid pool composition in primary rat hepatocytes and in vivo. Gastroenterology 120: 1801-1809, 2001.
47. Pandak WM, Li YC, Chiang JY, Studer EJ, Gurley EC, Heuman DM, Vlahcevic ZR, Hylemon PB. Regulation of cholesterol 7 α-hydroxylase mRNA and transcriptional activity by taurocholate and cholesterol in the chronic biliary diverted rat. J Biol Chem 266: 3416-3421, 1991.
48. Pandak WM, Ren S, Marques D, Hall E, Redford K, Mallonee K, Bohdan P, Heuman DM, Gil G, Hylemon PB. Transport of cholesterol into mitochondria is rate-limiting for bile acid synthesis via the alternative pathway in primary rat hepatocytes. J Biol Chem 277: 48158-48164, 2002.
49. Princen HMG, Meijer P, Hofstee B. Dexamethasone regulates bile acid synthesis in monolayer cultures of rat hepatocytes by induction of cholesterol 7α-hydroxylase. Biochem J 262: 341-348, 1989.
50. Ren S, Hylemon PB, Marques D, Gurley EC, Bodham P, Hall E, Redford K, Gil G, Pandak WM. Overexpression of cholesterol transporter StAR increases in vivo rates of bile acid synthesis in the rat and mouse. Hepatology 40: 910-917, 2004.
51. Ren S, Hylemon PB, Marques D, Hall E, Redford K, Gil G, Pandak WM. Effect of increasing the expression of cholesterol transporters (StAR, MLN64, and SCP-2) on bile acid synthesis. J Lipid Res 45: 2123-2131, 2004.
52. Repa JJ, Lund EG, Horton JD, Leitersdorf E, Russell DW, Dietschy JM, Turley SD. Disruption of the sterol 27-hydroxylase gene in mice results in hepatomegaly and hypertriglyceridemia. Reversal by cholic acid feeding. J Biol Chem 275: 39685-39692, 2000.
53. Russell DW. The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72: 137-174, 2003.
54. Russell DW, Setchell KDR. Bile acid biosynthesis. Biochemistry 31: 4737-4749, 1992.
55. Schwarz M, Lund E, Setchell K, Kayden H, Zerwekh J, Bjorkhem I, Herz J, Russell D. Disruption of cholesterol 7 α-hydroxylase gene in mice. II. Bile acid deficiency is overcome by induction of oxysterol 7 α-hydroxylase. J Biol Chem 271: 18024-18031, 1996.
56. Schwarz M, Lund EG, Lathe R, Björkhem I, Russell DW. Identification and characterization of a mouse oxysterol 7 α-hydroxylase cDNA. J Biol Chem 272: 23995-24001, 1997.
57. Schwarz M, Russell DW, Dietschy JM, Turley SD. Alternate pathways of bile acid synthesis in the cholesterol 7α-hydroxylase knockout mouse are not upregulated by either cholesterol or cholestyramine feeding. J Lipid Res 42: 1594-1603, 2001.
58. Schwarz M, Russell DW, Dietschy JM, Turley SD. Marked reduction in bile acid synthesis in cholesterol 7α-hydroxylase-deficient mice does not lead to diminished tissue cholesterol turnover or to hypercholesterolemia. J Lipid Res 39: 1833-1843, 1998.
59. Setchell KDR, Schwarz M, O'Connell N, Lund EG, Davis DL, Lathe R, Thompson HR, Tyson RW, Sokol RJ, Russell DW. Identification of a new inborn error in bile acid synthesis: mutation of the oxysterol 7 α-hydroxylase gene causes severe neonatal liver disease. J Clin Invest 102: 1690-1703, 1998.
60. Shneider BL, Dawson PA, Christie DM, Hardikar W, Wong MH, Suchy FJ. Cloning and molecular characterization of the ontogeny of a rat ileal sodium-dependent bile acid transporter. J Clin Invest 95: 745-754, 1995.
61. Signer E, Murphy G, Edkins S, Anderson C. Role of bile salts in fat malabsorption of premature infants. Arch Dis Child 49: 174-180, 1974.
62. Smith JL, Lear SR, Erickson SK. Developmental expression of elements of hepatic cholesterol metabolism in the rat. J Lipid Res 36: 641-652, 1995.
63. Solomon NS, Gartner H, Oesterreicher TJ, Henning SJ. Development of glucocorticoid-responsiveness in mouse intestine. Pediatr Res 49: 782-788, 2001.
64. Song KH, Ellis E, Strom S, Chiang JYL. Hepatocyte growth factor signaling pathway inhibits cholesterol 7α-hydroxylase and bile acid synthesis in human hepatocytes. Hepatology 46: 1993-2002, 2007.
65. Song KH, Li T, Owsley E, Strom S, Chiang JY. Bile acids activate fibroblast growth factor 19 signaling in human hepatocytes to inhibit cholesterol 7 α-hydroxylase gene expression. Hepatology 49: 297-305, 2009.
66. Standinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klassen CD, Brown KK, Reinhard J, Wilson TM, Koller BH, Kliewer SA. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci USA 98: 3369-3374, 2001.
67. Sutano W, De Kloet ER. Species-specificity of corticosteroid receptors in hamster and rat brains. Endocrinology 121: 1405-1411, 1987.
68. Ueki I, Kimura A, Nishyori A, Chen HL, Takei H, Nittono H, Kurosawa T. Neonatal cholestatic liver disease in an Asian patient with a homozygous mutation in the oxysterol 7α-hydroxylase gene. J Pediatr Gastroenterol Nutr 46: 465-469, 2008.
69. Watkins JB, Ingall D, Szczepanik PA, Klein PD, Lester R. Bile salt metabolism in the newborn. Measurement of pool size and synthesis by stable isotope technique. N Engl J Med 188: 431-434, 1973.
70. Watkins JB, Szczepanik P, Gould JB, Klein P, Lester R. Bile salt metabolism in the human premature infant. Preliminary observations of pool size and synthesis rate following prenatal administration of dexamethasone and phenobarbital. Gastroenterology 69: 706-713, 1975.
71. Woollett LA, Wang Y, Buckley DD, Yao L, Chin S, Granholm N, Jones PJH, Setchell KDR, Tso P, Heubi JE. Micellar solubilisation of cholesterol is essential for absorption in humans. Gut 55: 197-204, 2006.
72. Xie MH, Holcomb I, Deuel B, Dowd P, Huang A, Vagts A, Foster J, Liang J, Brush J, Gu Q, Hillan K, Goddard A, Gureney AL. FGF-19, a novel fibroblast growth factor with unique specificity for FGFR4. Cytokine 11: 729-735, 1999.
73. Xu G, Pan L, Erickson SK, Forman BM, Shneider BL, Ananthanarayanan M, Li X, Shefer S, Balasubramaniyan N, Ma L, Asoka H, Lear SR, Nguyen LB, Dussault I, Suchy FJ, Tint GS, Salen G. Removal of the bile acid pool upregulates cholesterol 7α-hydroxylase by deactivating FXR in rabbits. J Lipid Res 43: 45-50, 2002.
74. Yao L, Dawson PA, Woollett LA. Increases in biliary cholesterol-to-bile acid ratio in pregnant hamsters fed low and high levels of cholesterol. Am J Physiol Gastrointest Liver Physiol 284: G263-G268, 2003.
75. Yao L, Horn PS, Heubi JE, Woollett LA. The liver plays a key role in whole body sterol accretion of the neonatal Golden Syrian hamster. Biochim Biophys Acta 1771: 550-557, 2007.
76. Yao L, Jenkins K, Horn PS, Lichtenberg MH, Woollett LA. Inability to fully suppress sterol synthesis rates with exogenous sterol in embryonic and extraembyronic fetal tissues. Biochim Biophys Acta 1171: 1372-1379, 2007.
77. Yaylaoglu MB, Agbemafle BM, Oesterreicher TJ, Finegold MJ, Thaller C, Henning SJ. Diverse patterns of cell-specific gene expression in response to glucocorticoid in the developing small intestine. Am J Physiol Gastrointest Liver Physiol 291: G1041-G1050, 2006.
78. Yu C, Wang F, Kan M, Jin C, Jones RB, Weinstein M, Deng CX, McKeehan WL. Elevated cholesterol metabolism and bile acid synthesis in mice lacking membrane tyrosine kinase receptor FGFR4. J Biol Chem 275: 15482-15489, 2000.