Role of hepatic transporters in prevention of bile acid toxicity after partial hepatectomy in mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 3, 2009, Pages

  Csanaky, Iván L ^a   Aleksunes, Lauren M ^a   Tanaka, Yuji ^a   Klaassen, Curtis D ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

2 3 Partial hepatectomy; Biliary excretion; Liver regeneration; UPLC MS MS

Indexed keywords

BILE ACID; BILIRUBIN; GLYCINE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 3; PHOSPHOLIPID; TAURINE;

ANIMAL EXPERIMENT; ARTICLE; BILE ACID BLOOD LEVEL; BILE SECRETION; BILIRUBIN BLOOD LEVEL; CONTROLLED STUDY; GENE EXPRESSION; HEPATOBILIARY SYSTEM; LIVER TOXICITY; MALE; MICELLIZATION; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SHAM PROCEDURE; UPREGULATION;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; ATP-BINDING CASSETTE TRANSPORTERS; BILE ACIDS AND SALTS; BILIRUBIN; BLOTTING, WESTERN; ENTEROHEPATIC CIRCULATION; GENE EXPRESSION REGULATION; GLYCINE; HEPATECTOMY; IMMUNOHISTOCHEMISTRY; LIVER; LIVER REGENERATION; MALE; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICELLES; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; PHOSPHOLIPIDS; RNA, MESSENGER; SYMPORTERS; TAURINE; TIME FACTORS;

EID: 69649109377     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90728.2008     Document Type: Article

References (88)

1. Akita H, Suzuki H, Ito K, Kinoshita S, Sato N, Takikawa H, Sugiyama Y. Characterization of bile acid transport mediated by multidrug resistance associated protein 2 and bile salt export pump. Biochim Biophys Acta 1511: 7-16, 2001. (Pubitemid 32206667)
2. Aleksunes LM, Scheffer GL, Jakowski AB, Pruimboom-Brees IM, Manautou JE. Coordinated expression of multidrug resistance-associated proteins (Mrps) in mouse liver during toxicant-induced injury. Toxicol Sci 89: 370-379, 2006.
3. Alnouti Y, Csanaky IL, Klaassen CD. Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 873: 209-217, 2008.
4. Andersen B, Zierz S, Jungermann K. Alteration in zonation of succinate dehydrogenase, phosphoenolpyruvate carboxykinase and glucose-6-phosphatase in regenerating rat liver. Histochemistry 80: 97-101, 1984. (Pubitemid 14174031)
5. Balabaud C, Kron KA, Gumucio JJ. The assessment of the bile salt-nondependent fraction of canalicular bile water in the rat. J Lab Clin Med 89: 393-399, 1977. (Pubitemid 8100794)
6. Baumgartner U, Sellinger M, Ruf G, Jehle L, Ihling C, Farthmann EH. Change of zonal bile acid processing after partial hepatectomy in the rat. J Hepatol 22: 474-480, 1995.
7. Belinsky MG, Dawson PA, Shchaveleva I, Bain LJ, Wang R, Ling V, Chen ZS, Grinberg A, Westphal H, Klein-Szanto A, Lerro A, Kruh GD. Analysis of the in vivo functions of Mrp3. Mol Pharmacol 68: 160-168, 2005.
8. Boyer JL, Klatskin G. Canalicular bile flow and bile secretory pressure. Evidence for a non-bile salt dependent fraction in the isolated perfused rat liver. Gastroenterology 59: 853-859, 1970.
9. Boyer JL, Trauner M, Mennone A, Soroka CJ, Cai SY, Moustafa T, Zollner G, Lee JY, Ballatori N. Upregulation of a basolateral FXR-dependent bile acid efflux transporter OSTα-OSTβ in cholestasis in humans and rodents. Am J Physiol Gastrointest Liver Physiol 290: G1124-G1130, 2006. (Pubitemid 43788293)
10. Brand HS, Deutz NE, Meijer AJ, Jorning GG, Chamuleau RA. In vivo amino acid fluxes in regenerating liver after two-thirds hepatectomy in the rat. J Hepatol 23: 333-340, 1995.
11. Chatzipanagiotou S, Nath A, Vogt B, Jungermann K. Alteration in the capacities as well as in the zonal and cellular distributions of pyruvate kinase L and M2 in regenerating rat liver. Biol Chem Hoppe Seyler 366: 271-280, 1985. (Pubitemid 15085886)
12. Cheng HC, Yang CM, Shiao MS. Zonation of cholesterol and glycerolipid synthesis in regenerating rat livers. Hepatology 17: 280-286, 1993.
13. Cheng X, Buckley D, Klaassen CD. Regulation of hepatic bile acid transporters Ntcp and Bsep expression. Biochem Pharmacol 74: 1665-1676, 2007. (Pubitemid 47614969)
14. Cheng X, Klaassen CD. Critical role of PPAR-alpha in perfluorooctanoic acid- and perfluorodecanoic acid-induced downregulation of Oatp uptake transporters in mouse livers. Toxicol Sci 106: 37-45, 2008.
15. Cheng X, Klaassen CD. Regulation of mRNA expression of xenobiotic transporters by the pregnane x receptor in mouse liver, kidney, and intestine. Drug Metab Dispos 34: 1863-1867, 2006.
16. Cheng X, Maher J, Dieter MZ, Klaassen CD. Regulation of mouse organic anion-transporting polypeptides (Oatps) in liver by prototypical microsomal enzyme inducers that activate distinct transcription factor pathways. Drug Metab Dispos 33: 1276-1282, 2005. (Pubitemid 41196968)
17. Dai G, He L, Bu P, Wan YJ. Pregnane X receptor is essential for normal progression of liver regeneration. Hepatology 47: 1277-1287, 2008. (Pubitemid 351547914)
18. Dawson PA, Hubbert M, Haywood J, Craddock AL, Zerangue N, Christian WV, Ballatori N. The heteromeric organic solute transporter alpha-beta, Ostalpha-Ostbeta, is an ileal basolateral bile acid transporter. J Biol Chem 280: 6960-6968, 2005. (Pubitemid 40341252)
19. De Vree JM, Jacquemin E, Sturm E, Cresteil D, Bosma PJ, Aten J, Deleuze JF, Desrochers M, Burdelski M, Bernard O, Oude Elferink RP, Hadchouel M. Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc Natl Acad Sci USA 95: 282-287, 1998. (Pubitemid 28103945)
20. Digernes V, Bronstad G, Sand TE, Christoffersen T. The proliferation response of rat liver parenchymal cells after partial hepatectomy. A methodological study comparing flow cytometry of nuclear DNA content and in vivo and in vitro uptake of thymidine. Cell Tissue Kinet 15: 521-528, 1982. (Pubitemid 12056289)
21. Donovan JM, Timofeyeva N, Carey MC. Influence of total lipid concentration, bile salt:lecithin ratio, and cholesterol content on inter-mixed micellar/vesicular (non-lecithin-associated) bile salt concentrations in model bile. J Lipid Res 32: 1501-1512, 1991.
22. Dransfeld O, Gehrmann T, Kohrer K, Kircheis G, Holneicher C, Haussinger D, Wettstein M. Oligonucleotide microarray analysis of differential transporter regulation in the regenerating rat liver. Liver Int 25: 1243-1258, 2005. (Pubitemid 41782571)
23. Fickert P, Zollner G, Fuchsbichler A, Stumptner C, Pojer C, Zenz R, Lammert F, Stieger B, Meier PJ, Zatloukal K, Denk H, Trauner M. Effects of ursodeoxycholic and cholic acid feeding on hepatocellular transporter expression in mouse liver. Gastroenterology 121: 170-183, 2001.
24. Flock EV, Bollman J, L. Phospholipid synthesis in damaged and regenerating liver. Fed Proc 5: 133-134, 1946.
25. Frijters CM, Ottenhoff R, van Wijland MJ, van Nieuwkerk CM, Groen AK, Oude Elferink RP. Regulation of mdr2 P-glycoprotein expression by bile salts. Biochem J 321: 389-395, 1997. (Pubitemid 27056485)
26. Fukano S, Saitoh Y, Uchida K, Akiyoshi T, Takeda K. Bile acid metabolism in partially hepatectomized rats. Steroids 45: 209-227, 1985. (Pubitemid 16131132)
27. Geier A, Trautwein C. Bile acids are "homeotrophic" sensors of the functional hepatic capacity and regulate adaptive growth during liver regeneration. Hepatology 45: 251-253, 2007. (Pubitemid 46144386)
28. Geier A, Wagner M, Dietrich CG, Trauner M. Principles of hepatic organic anion transporter regulation during cholestasis, inflammation and liver regeneration. Biochim Biophys Acta 1773: 283-308, 2007. (Pubitemid 46275063)
29. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, Hofmann AF, Meier PJ. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273: 10046-10050, 1998. (Pubitemid 28183107)
30. Grattagliano I, Lauterburg BH, Portincasa P, Caruso ML, Vendemiale G, Valentini AM, Palmieri VO, Palasciano G. Mitochondrial glutathione content determines the rate of liver regeneration after partial hepatectomy in eu- and hypothyroid rats. J Hepatol 39: 571-579, 2003. (Pubitemid 37204658)
31. Green RM, Gollan JL, Hagenbuch B, Meier PJ, Beier DR. Regulation of hepatocyte bile salt transporters during hepatic regeneration. Am J Physiol Gastrointest Liver Physiol 273: G621-G627, 1997. (Pubitemid 27418781)
32. Groothuis GM, Hardonk MJ, Keulemans KP, Nieuwenhuis P, Meijer DK. Autoradiographic and kinetic demonstration of acinar heterogeneity of taurocholate transport. Am J Physiol Gastrointest Liver Physiol 243: G455-G462, 1982.
33. Guo GL, Lambert G, Negishi M, Ward JM, Brewer HB Jr, Kliewer SA, Gonzalez FJ, Sinal CJ. Complementary roles of farnesoid X receptor, pregnane X receptor, and constitutive androstane receptor in protection against bile acid toxicity. J Biol Chem 278: 45062-45071, 2003. (Pubitemid 37432638)
34. Gupta S, Stravitz RT, Pandak WM, Muller M, Vlahcevic ZR, Hylemon PB. Regulation of multidrug resistance 2 P-glycoprotein expression by bile salts in rats and in primary cultures of rat hepatocytes. Hepatology 32: 341-347, 2000. (Pubitemid 30614666)
35. Gurantz D, Laker MF, Hofmann AF. Enzymatic measurement of choline-containing phospholipids in bile. J Lipid Res 22: 373-376, 1981. (Pubitemid 11125140)
36. Hagenbuch B, Dawson P. The sodium bile salt cotransport family SLC10. Pflügers Arch 447: 566-570, 2004. (Pubitemid 38241441)
37. Higgins GM, Anderson RM. Experimental pathology of the liver. I. Restoration of the liver of the white rat following partial surgical removal. Arch Pathol 12: 186-202, 1931.
38. Hofmann AF. Bile acids: the good, the bad, and the ugly. News Physiol Sci 14: 24-29, 1999.
39. Homolya L, Varadi A, Sarkadi B. Multidrug resistance-associated proteins: export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 17: 103-114, 2003. (Pubitemid 37267146)
40. Hoshino M, Hirano A, Hayakawa T, Kamiya Y, Ohiwa T, Tanaka A, Kumai T, Katagiri K, Miyaji M, Takeuchi T. Comparative studies on bile flow and biliary lipid excretion after bile-acid loading in normal and partially hepatectomized rats. Biochem J 305: 367-371, 1995.
41. Huang W, Ma K, Zhang J, Qatanani M, Cuvillier J, Liu J, Dong B, Huang X, Moore DD. Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration. Science 312: 233-236, 2006.
42. Jones AL, Hradek GT, Renston RH, Wong KY, Karlaganis G, Paumgartner G. Autoradiographic evidence for hepatic lobular concentration gradient of bile acid derivative. Am J Physiol Gastrointest Liver Physiol 238: G233-G237, 1980.
43. Klaassen CD. Comparison of the effects of two-thirds hepatectomy and bile duct ligation on hepatic excretory function. J Pharmacol Exp Ther 191: 25-31, 1974.
44. Klaassen CD, Lu H. Xenobiotic transporters: ascribing function from gene knockout and mutation studies. Toxicol Sci 101: 186-196, 2008.
45. Komichi D, Tazuma S, Nishioka T, Hyogo H, Une M, Chayama K. Unique inhibition of bile salt-induced apoptosis by lecithins and cytoprotective bile salts in immortalized mouse cholangiocytes. Dig Dis Sci 48: 2315-2322, 2003. (Pubitemid 38021736)
46. Kullak-Ublick GA, Stieger B, Hagenbuch B, Meier PJ. Hepatic transport of bile salts. Semin Liver Dis 20: 273-292, 2000.
47. Kurumiya Y, Nagino M, Nozawa K, Kamiya J, Uesaka K, Sano T, Yoshida S, Nimura Y. Biliary bile acid concentration is a simple and reliable indicator for liver function after hepatobiliary resection for biliary cancer. Surgery 3: 512-520, 2003.
48. Lam P, Wang R, Ling V. Bile acid transport in sister of P-glycoprotein (ABCB11) knockout mice. Biochemistry 44: 12598-12605, 2005. (Pubitemid 41324350)
49. Leazer TM, Klaassen CD. The presence of xenobiotic transporters in rat placenta. Drug Metab Dispos 31: 153-167, 2003.
50. Lefebvre P, Cariou B, Lien F, Kuipers F, Staels B. Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 89: 147-191, 2009.
51. Leong GF, Pessotti RL, Brauer RW. Liver function in regenerating rat liver. CrPO4 colloid uptake and bile flow. Am J Physiol 197: 880-886, 1959.
52. Liu Y, Binz J, Numerick MJ, Dennis S, Luo G, Desai B, MacKenzie KI, Mansfield TA, Kliewer SA, Goodwin B, Jones SA. Hepatoprotection by the farnesoid X receptor agonist GW4064 in rat models of intraand extrahepatic cholestasis. J Clin Invest 112: 1678-1687, 2003. (Pubitemid 38063725)
53. Loeb WF, Quimby FW. The Clinical Chemistry of Laboratory Animals. Oxford, UK: Pergamon, 1989.
54. Maher JM, Slitt AL, Cherrington NJ, Cheng X, Klaassen CD. Tissue distribution and hepatic and renal ontogeny of the multidrug resistance-associated protein (Mrp) family in mice. Drug Metab Dispos 33: 947-955, 2005. (Pubitemid 41002776)
55. Mizuta A, Chijiiwa K, Saiki S, Kuroki S, Nakamura K, Tanaka M. Differences in biliary lipid excretion after major hepatectomy in obstructive jaundiced rats with preoperative internal, external, or no biliary drainage. Eur Surg Res 34: 291-299, 2002.
56. Nakamura K, Ichimiya H, Nakayama F. Alteration of bile acid metabolism in two-thirds hepatectomized rat. J Gastroenterol Hepatol 7: 121-127, 1992.
57. Nakatsukasa H, Silverman JA, Gant TW, Evarts RP, Thorgeirsson SS. Expression of multidrug resistance genes in rat liver during regeneration and after carbon tetrachloride intoxication. Hepatology 18: 1202-1207, 1993. (Pubitemid 23320453)
58. Noshiro M, Nishimoto M, Okuda K. Rat liver cholesterol 7 alphahydroxylase. Pretranslational regulation for circadian rhythm. J Biol Chem 265: 10036-10041, 1990. (Pubitemid 20194360)
59. O'Connor CJ, Wallace RG, Iwamoto K, Taguchi T, Sunamoto J. Bile salt damage of egg phosphatidylcholine liposomes. Biochim Biophys Acta 817: 95-102, 1985. (Pubitemid 15011683)
60. Oppenheimer MJ, Flock EV. Alkaline phosphatase levels in plasma and liver following partial hepatectomy. Am J Physiol 429-448, 1947.
61. Pircher PC, Kitto JL, Petrowski ML, Tangirala RK, Bischoff ED, Schulman IG, Westin SK. Farnesoid X receptor regulates bile acid-amino acid conjugation. J Biol Chem 278: 27703-27711, 2003.
62. Rao A, Haywood J, Craddock AL, Belinsky MG, Kruh GD, Dawson PA. The organic solute transporter alpha-beta, Ostalpha-Ostbeta, is essential for intestinal bile acid transport and homeostasis. Proc Natl Acad Sci USA 105: 3891-3896, 2008. (Pubitemid 351723495)
63. Rausch-Derra LC, Hartley DP, Meier PJ, Klaassen CD. Differential effects of microsomal enzyme-inducing chemicals on the hepatic expression of rat organic anion transporters, OATP1 and OATP2. Hepatology 33: 1469-1478, 2001.
64. Rolo AP, Palmeira CM, Holy JM, Wallace KB. Role of mitochondrial dysfunction in combined bile acid-induced cytotoxicity: the switch between apoptosis and necrosis. Toxicol Sci 79: 196-204, 2004.
65. Rost D, Herrmann T, Sauer P, Schmidts HL, Stieger B, Meier PJ, Stremmel W, Stiehl A. Regulation of rat organic anion transporters in bile salt-induced cholestatic hepatitis: effect of ursodeoxycholate. Hepatology 38: 187-195, 2003. (Pubitemid 36775810)
66. Schubert R, Schmidt KH. Structural changes in vesicle membranes and mixed micelles of various lipid compositions after binding of different bile salts. Biochemistry 27: 8787-8794, 1988. (Pubitemid 19008195)
67. Slitt AL, Allen K, Morrone J, Aleksunes LM, Chen C, Maher JM, Manautou JE, Cherrington NJ, Klaassen CD. Regulation of transporter expression in mouse liver, kidney, and intestine during extrahepatic cholestasis. Biochim Biophys Acta 1768: 637-647, 2007. (Pubitemid 46275582)
68. Smit JJ, Schinkel AH, Oude Elferink RP, Groen AK, Wagenaar E, van Deemter L, Mol CA, Ottenhoff R, van der Lugt NM, van Roon MA, van der Valk MA, Offerhaus GJA, Berns AJM, Borst P. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell 75: 451-462, 1993. (Pubitemid 23335071)
69. Sperber I. Secretion of organic anions in the formation of urine and bile. Pharmacol Rev 11: 109-134, 1959.
70. Stacey NH, Klaassen CD. Uptake of galactose, ouabain and taurocholate into centrilobular and periportal enriched hepatocyte subpopulations. J Pharmacol Exp Ther 216: 634-639, 1981.
71. Staudinger J, Liu Y, Madan A, Habeebu S, Klaassen CD. Coordinate regulation of xenobiotic and bile acid homeostasis by pregnane X receptor. Drug Metab Dispos 29: 1467-1472, 2001. (Pubitemid 33000694)
72. Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klaassen CD, Brown KK, Reinhard J, Willson 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. (Pubitemid 32220852)
73. Stieger B, Meier Y, Meier PJ. The bile salt export pump. Pflügers Arch 453: 611-620, 2007.
74. Teeter LD, Estes M, Chan JY, Atassi H, Sell S, Becker FF, Kuo MT. Activation of distinct multidrug-resistance (P-glycoprotein) genes during rat liver regeneration and hepatocarcinogenesis. Mol Carcinog 8: 67-73, 1993. (Pubitemid 23296311)
75. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27: 502-522, 1969.
76. Tsuboi K, Tazuma S, Nishioka T, Chayama K. Partial characterization of cytoprotective mechanisms of lecithin against bile salt-induced bile duct damage. J Gastroenterol 39: 955-960, 2004. (Pubitemid 39490172)
77. Ujhazy P, Ortiz D, Misra S, Li S, Moseley J, Jones H, Arias IM. Familial intrahepatic cholestasis 1: studies of localization and function. Hepatology 34: 768-775, 2001. (Pubitemid 32928002)
78. Van Noorden CJ, Vogels IM, Houtkooper JM. Cytophotometric analysis of alkaline phosphatase and 5′-nucleotidase activity in regenerating rat liver after partial hepatectomy. Cell Biochem Funct 6: 53-60, 1988.
79. Van Noorden CJ, Vogels IM, James J. Adaptive sex-dependent changes in the zonation of carbohydrate and lipid metabolism in rat liver lobules after partial hepatectomy. Hepatology 20: 714-724, 1994. (Pubitemid 24271282)
80. Vos TA, Ros JE, Havinga R, Moshage H, Kuipers F, Jansen PL, Muller M. Regulation of hepatic transport systems involved in bile secretion during liver regeneration in rats. Hepatology 29: 1833-1839, 1999.
81. Wagner M, Fickert P, Zollner G, Fuchsbichler A, Silbert D, Tsybrovskyy O, Zatloukal K, Guo GL, Schuetz JD, Gonzalez FJ, Marschall HU, Denk H, Trauner M. Role of farnesoid X receptor in determining hepatic ABC transporter expression and liver injury in bile duct-ligated mice. Gastroenterology 125: 825-838, 2003. (Pubitemid 37070700)
82. Weglarz TC, Sandgren EP. Timing of hepatocyte entry into DNA synthesis after partial hepatectomy is cell autonomous. Proc Natl Acad Sci USA 97: 12595-12600, 2000.
83. Wolters H, Elzinga BM, Baller JF, Boverhof R, Schwarz M, Stieger B, Verkade HJ, Kuipers F. Effects of bile salt flux variations on the expression of hepatic bile salt transporters in vivo in mice. J Hepatol 37: 556-563, 2002. (Pubitemid 35305533)
84. Xia X, Francis H, Glaser S, Alpini G, LeSage G. Bile acid interactions with cholangiocytes. World J Gastroenterol 12: 3553-3563, 2006.
85. Xie W, Radominska-Pandya A, Shi Y, Simon CM, Nelson MC, Ong ES, Waxman DJ, Evans RM. An essential role for nuclear receptors SXR/PXR in detoxification of cholestatic bile acids. Proc Natl Acad Sci USA 98: 3375-3380, 2001. (Pubitemid 32220853)
86. Zollner G, Fickert P, Silbert D, Fuchsbichler A, Stumptner C, Zatloukal K, Denk H, Trauner M. Induction of short heterodimer partner 1 precedes downregulation of Ntcp in bile duct-ligated mice. Am J Physiol Gastrointest Liver Physiol 282: G184-G191, 2002. (Pubitemid 34650113)
87. Zollner G, Trauner M. Mechanisms of cholestasis. Clin Liver Dis 12: 1-26, vii, 2008.
88. Zollner G, Wagner M, Moustafa T, Fickert P, Silbert D, Gumhold J, Fuchsbichler A, Halilbasic E, Denk H, Marschall HU, Trauner M. Coordinated induction of bile acid detoxification and alternative elimination in mice: role of FXR-regulated organic solute transporter-alpha/beta in the adaptive response to bile acids. Am J Physiol Gastrointest Liver Physiol 290: G923-G932, 2006.