Growth hormone modulation of the rat hepatic bile transporter system in endotoxin-induced cholestasis

Endocrinology

Volumn 144, Issue 9, 2003, Pages 4008-4017

  Mesotten, Dieter ^a,b   Van Den Berghe, Greet ^b   Liddle, Christopher ^c   Coulter, Sally ^c   Mcdougall, Fiona ^a   Baxter, Robert C ^a   Delhanty, Patric J D ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; ENDOTOXIN; GROWTH HORMONE; HUMAN GROWTH HORMONE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MARKER; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; ORGANIC ANION TRANSPORTER; ABC TRANSPORTER; AKR1C2 PROTEIN, HUMAN; BILE ACID BINDING PROTEINS; BIOLOGICAL MARKER; CARRIER PROTEIN; COTRANSPORTER; CYP3A2 PROTEIN, RAT; GLYCOPROTEIN P; HYDROXYSTEROID DEHYDROGENASE; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 3; ORGANIC ANION TRANSPORTER 1; P GLYCOPROTEIN 2; P-GLYCOPROTEIN 2; SLC22A7 PROTEIN, HUMAN; SLC22A7 PROTEIN, RAT; SODIUM; SODIUM BILE ACID COTRANSPORTER; SODIUM-BILE ACID COTRANSPORTER; UNSPECIFIC MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTASIS; CONTROLLED STUDY; DISEASE EXACERBATION; DRUG FATALITY; DRUG INFUSION; DRUG MEGADOSE; ENDOTOXEMIA; HEPATOBILIARY SYSTEM; IMMUNOBLOTTING; INJECTION; LIVER INJURY; MALE; MODULATION; MORTALITY; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; ANIMAL; BILE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION; GENETICS; INTRAHEPATIC CHOLESTASIS; LIVER; LIVER CELL; METABOLISM; SEPSIS; SPRAGUE DAWLEY RAT;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; ATP-BINDING CASSETTE TRANSPORTERS; BILE; BIOLOGICAL MARKERS; CARRIER PROTEINS; CHOLESTASIS, INTRAHEPATIC; GENE EXPRESSION; GROWTH HORMONE; HEPATOCYTES; HYDROXYSTEROID DEHYDROGENASES; LIPOPOLYSACCHARIDES; LIVER; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; ORGANIC ANION TRANSPORT PROTEIN 1; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; P-GLYCOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SEPSIS; SODIUM; SYMPORTERS;

EID: 0042922508     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2003-0139     Document Type: Article

References (83)

1. Pirovino M, Meister F, Rubli E, Karlaganis G 1989 Preserved cytosolic and synthetic liver function in jaundice of severe extrahepatic infection. Gastroenterology 96:1589-1595
2. Van Bossuyt H, De Zanger RB, Wisse E 1988 Cellular and subcellular distribution of injected lipopolysaccharide in rat liver and its inactivation by bile salts. J Hepatol 7:325-337
3. Fox ES, Broitman SA, Thomas P 1990 Bacterial endotoxins and the liver. Lab Invest 63:733-741
4. Hewett JA, Roth RA 1993 Hepatic and extrahepatic pathobiology of bacterial lipopolysaccharides. Pharmacol Rev 45:381-411
5. Gore DC, Honeycutt D, Jahoor F, Wolfe RR, Herndon DN 1991 Effect of exogenous growth hormone on whole-body and isolated-limb protein kinetics in burned patients. Arch Surg 126:38-43
6. Voerman HJ, van Schijndel RJ, Groeneveld AB, de Boer H, Nauta JP, van der Veen EA, Thijs LG 1992 Effects of recombinant human growth hormone in patients with severe sepsis. Ann Surg 216:648-655
7. Carroll PV 1999 Protein metabolism and the use of growth hormone and insulin-like growth factor-I in the critically ill patient. GH IGF Res 9:400-413
8. Wilmore DW 1999 The use of growth hormone in severely ill patients. Adv Surg 33:261-274
9. Raguso CA, Genton L, Kyle U, Pichard C 2001 Management of catabolism in metabolically stressed patients: a literature survey about growth hormone application. Curr Opin Clin Nutr Metab Care 4:313-320
10. Takala J, Ruokonen E, Webster NR, Nielsen MS, Zandstra DF, Vundelinckx G, Hinds CJ 1999 Increased mortality associated with growth hormone treatment in critically ill adults. N Engl J Med 341:785-792
11. Ruokonen E, Takala J 2002 Dangers of growth hormone therapy in critically ill patients. Curr Opin Clin Nutr Metab Care 5:199-209
12. Liao W, Rudling M, Angelin B 1996 Growth hormone potentiates the in vivo biological activities of endotoxin in the rat. Eur J Clin Invest 26:254-258
13. Müller M, Jansen PL 1997 Molecular aspects of hepatobiliary transport. Am J Physiol 272:G1285-G1303
14. Trauner M, Meier PJ, Boyer JL 1998 Molecular pathogenesis of cholestasis. N Engl J Med 339:1217-1227
15. Kullak-Ublick GA, Beuers U, Paumgartner G 2000 Hepatobiliary transport. J Hepatol 32:3-18
16. Hooiveld GJ, Van Montfoort JE, Meijer DKF, Müller M 2001 Function and regulation of ATP-binding cassette transport proteins involved in hepatobiliary transport. Eur J Pharm Sci 12:525-543
17. Meier PJ, Stieger B 2002 Bile salt transporters. Annu Rev Physiol 64:635-661
18. +/bile acid cotransport system. Proc Natl Acad Sci USA 88:10629-10633
19. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, Hofmann AF, Meier PJ 1998 The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273:10046-10050
20. +-independent organic anion transporter. Proc Natl Acad Sci USA 91:133-137
21. Noé B, Hagenbuch B, Stieger B, Meier PJ 1997 Isolation of a multispecific organic anion and cardiac glycoside transporter from rat brain. Proc Natl Acad Sci USA 94:10346-10350
22. Reichel C, Gao B, Van Montfoort J, Cattori V, Rahner C, Hagenbuch B, Stieger B, Kamisako T, Meier PJ 1999 Localization and function of the organic anion-transporting polypeptide Oatp2 in rat liver. Gastroenterology 117:688-695
23. Cattori V, Hagenbuch B, Hagenbuch N, Stieger B, Ha R, Winterhalter KE, Meier PJ 2000 Identification of organic anion transporting polypeptide 4 (Oatp4) as a major full-length isoform of the liver-specific transporter-1 (rlst-1) in rat liver. FEBS Lett 474:242-245
24. Kakyo M, Unno M, Tokui T, Nakagomi R, Nishio T, Iwasashi H, Nakai D, Seki M, Suzuki M, Naitoh T, Matsuno S, Yawo H, Abe T 1999 Molecular characterization and functional regulation of a novel rat liver-specific organic anion transporter rlst-1. Gastroenterology 117:770-775
25. Cattori V, van Montfoort JE, Stieger B, Landmann L, Meijer DKF, Winterhalter KH, Meier PJ, Hagenbuch B 2001 Localization of organic anion transporting polypeptide 4 (Oatp4) in rat liver and comparison of its substrate specificity with Oatp1, Oatp2 and Oatp3. Pflugers Arch Eur J Physiol 443:188-195
26. Büchler M, König J, Brom M, Kartenbeck J, Spring H, Horie T, Keppler D 1996 cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 271:15091-15098
27. Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, Scheper RJ, Borst P, Oude Elferink RP 1996 Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271:1126-1128
28. Ishikawa T, Müller M, Klünemann C, Schaub T, Keppler D 1990 ATP-dependent primary active transport of cysteinyl leukotrienes across liver canalicular membrane. Role of the ATP-dependent transport system for glutathione S-conjugates. J Biol Chem 265:19279-19286
29. Gottesman MM, Pastan I 1993 Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62:385-427
30. Silverman JA, Thorgeirsson SS 1995 Regulation and function of the multidrug resistance genes in liver. Prog Liver Dis 13:101-123
31. Vos TA, Hooiveld GJ, Koning H, Childs S, Meijer DK, Moshage H, Jansen PL, Müller M 1998 Up-regulation of the multidrug resistance genes, Mrp1 and Mdr1b, and down-regulation of the organic anion transporter, Mrp2, and the bile salt transporter, Spgp, in endotoxemic rat liver. Hepatology 28:1637-1644
32. Vos TA, Ros JE, Havinga R, Moshage H, Kuipers F, Jansen PL, Müller M 1999 Regulation of hepatic transport systems involved in bile secretion during liver regeneration in rats. Hepatology 29:1833-1839
33. 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 1993 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
34. Oude Elferink RP, Tytgat GN, Groen AK 1997 Hepatic canalicular membrane. I. The role of mdr2 P-glycoprotein in hepatobiliary lipid transport. FASEB J 11:19-28
35. Summerfield JA, Billing BH, Shackleton CH 1976 Identification of bile acids in the serum and urine in cholestasis. Evidence for 6α -hydroxylation of bile acids in man. Biochem J 154:507-516
36. Salen G, Batta AK 1999 Bile acid abnormalities in cholestatic liver diseases. Gastroenterol Clin North Am 28:173-193
37. Kinugasa T, Uchida K, Kadowaki M, Takase H, Nomura Y, Saito Y 1981 Effect of bile duct ligation on bile acid metabolism in rats. J Lipid Res 22:201-207
38. Takita M, Ikawa S, Ogura Y 1988 Effect of bile duct ligation on bile acid and cholesterol metabolism in rats. J Biochem 103:778-786
39. Chang TK, Teixeira J, Gil G, Waxman DJ 1993 The lithocholfc acid 6β-hydroxylase cytochrome P-450, CYP 3A10, is an active catalyst of steroid-hormone 6β-hydroxylation. Biochem J 291:429-433
40. Araya Z, Wikvall K 1999 6α-Hydroxylation of taurochenodeoxycholic acid and lithocholic acid by CYP3A4 in human liver microsomes. Biochim Biophys Acta 1438:47-54
41. Liddle C, Goodwin B 2002 Regulation of hepatic drug metabolism: role of the nuclear receptors PXR and CAR. Semin Liver Dis 22:115-122
42. Moore JT, Goodwin B, Willson TM, Kliewer SA 2002 Nuclear receptor regulation of genes involved in bile acid metabolism. Crit Rev Eukaryot Gene Expr 12:119-135
43. Roelfsema Y, Thomas GB, Lin H, Breier BH, Maxwell L, Oliver MH, Heineman E, Clark RG, Gluckman PD 2001 The metabolic effects of endotoxin are differentially affected by the pattern of GH administration in the rat. J Endocrinol 171:173-181
44. Berger SL, Chirgwin JM 1989 Isolation of RNA. Methods Enzymol 180:3-13
45. Delhanty PJ, Scott CD, Babu S, Baxter RC 2001 Acid-labile subunit regulation during the early stages of liver regeneration: implications for glucoregulation. Am J Physiol 280:E287-E295
46. Mashige F, Tanaka N, Maki A, Kamei S, Yamanaka M 1981 Direct spectrophotometry of total bile acids in serum. Clin Chem 27:1352-1356
47. Hurley JC 1995 Endotoxemia: methods of detection and clinical correlates. Clin Microbiol Rev 8:268-292
48. Rush BF, Sori AJ, Murphy TF, Smith S, Flanagan JJ, Machiedo GW 1988 Endotoxemia and bacteremia during hemorrhagic shock. The link between trauma and sepsis? Ann Surg 207:549-554
49. Pape HC, Dwenger A, Regel G, Auf'm'Kolck M, Gollub F, Wisner D, Sturm JA, Tscherne H 1994 Increased gut permeability after multiple trauma. Br J Surg 81:850-852
50. Casey LC, Balk RA, Bone RC 1993 Plasma cytokine and endotoxin levels correlate with survival in patients with the sepsis syndrome. Arm Intern Med 119:771-778
51. Zarkesh-Esfahani SH, Kolstad O, Metcalfe RA, Watson PF, von Laue S, Walters S, Revhaug A, Weetman AP, Ross RJ 2000 High-dose growth hormone does not affect proinflammatory cytokine (tumor necrosis factor-α, interleukin-6, and interferon-γ) release from activated peripheral blood mononuclear cells or after minimal to moderate surgical stress. J Clin Endocrinol Metab 85:3383-3390
52. Lechner AJ, Velasquez A, Knudsen KR, Johanns CA, Tracy TF, Jr, Matuschak GM 1998 Cholestatic liver injury increases circulating TNF-α and IL-6 and mortality after Escherichia coli endotoxemia. Am J Respir Crit Care Med 157:1550-1558
53. Miki C, McMaster P, Mayer AD, Iriyama K, Suzuki H, Buckels JA 2000 Factors predicting perioperative cytokine response in patients undergoing liver transplantation. Crit Care Med 28:351-354
54. Trauner M, Arrese M, Soroka CJ, Ananthanarayanan M, Koeppel TA, Schlosser SF, Suchy FJ, Keppler D, Boyer JL 1997 The rat canalicular conjugate export pump (Mrp2) is down-regulated in intrahepatic and obstructive cholestasis. Gastroenterology 113:255-264
55. Kubitz R, Wettstein M, Warskulat U, Häussinger D 1999 Regulation of the multidrug resistance protein 2 in the rat liver by lipopolysaccharide and dexamethasone. Gastroenterology 116:401-410
56. Green RM, Beier D, Gollan JL 1996 Regulation of hepatocyte bile salt transporters by endotoxin and inflammatory cytokines in rodents. Gastroenterology 111:193-198
57. Moseley RH, Wang W, Takeda H, Lown K, Shick L, Ananthanarayanan M, Suchy FJ 1996 Effect of endotoxin on bile acid transport in rat liver: a potential model for sepsis-associated cholestasis. Am J Physiol 271:G137-G146
58. Trauner M, Arrese M, Lee H, Boyer JL, Karpen SJ 1998 Endotoxin down-regulates rat hepatic ntcp gene expression via decreased activity of critical transcription factors. J Clin Invest 101:2092-2100
59. Schinkel AH, Mayer U, Wagenaar E, Mol CA, van Deemter L, Smit JJ, van der Valk MA, Voordouw AC, Spits H, van Tellingen O, Zijlmans JM, Fibbe WE, Borst P 1997 Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc Natl Acad Sci USA 94:4028-4033
60. Smit JW, Schinkel AH, Weert B, Meijer DK 1998 Hepatobiliary and intestinal clearance of amphiphilic cationic drugs in mice in which both mdr1a and mdr1b genes have been disrupted. Br J Pharmacol 124:416-424
61. +/taurocholate-cotransporting polypeptide gene expression by activating signal transducer and activator of transcription-5 in liver cells. Endocrinology 142:4212-4222
62. +-taurocholate cotransport and its encoding mRNA in primary cultures of rat hepatocytes. Hepatology 18:1162-1166
63. Rippin SJ, Hagenbuch B, Meier PJ, Stieger B 2001 Cholestatic expression pattern of sinusoidal and canalicular organic anion transport systems in primary cultured rat hepatocytes. Hepatology 33:776-782
64. Cui Y, Konig J, Leier I, Buchholz U, Keppler D 2001 Hepatic uptake of bilirubin and its conjugates by the human organic anion transporter SLC21A6. J Biol Chem 276:9626-9630
65. Zucker SD, Goessling W, Hoppin AG 1999 Unconjugated bilirubin exhibits spontaneous diffusion through model lipid bilayers and native hepatocyte membranes. J Biol Chem 274:10852-10862
66. Roelofsen H, van der Veere CN, Ottenhoff R, Schoemaker B, Jansen PL, Oude Elferink RP 1994 Decreased bilirubin transport in the perfused liver of endotoxemic rats. Gastroenterology 107:1075-1084
67. +-dependent bile-acid transporter. Biochem J 369:23-30
68. Zelcer N, Reid G, Wielinga P, Kuil A, van der Heijden I, Schuetz JD, Borst P 2003 Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem J 371:361-367
69. Ogawa K, Suzuki H, Hirohashi T, Ishikawa T, Meier PJ, Hirose K, Akizawa T, Yoshioka M, Sugiyama Y 2000 Characterization of inducible nature of MRP3 in rat liver. Am J Physiol 278:G438-G446
70. Donner MG, Keppler D 2001 Up-regulation of basolateral multidrug resistance protein 3 (Mrp3) in cholestatic rat liver. Hepatology 34:351-359
71. Soroka CJ, Lee JM, Azzaroli F, Boyer JL 2001 Cellular localization and up-regulation of multidrug resistance-associated protein 3 in hepatocytes and cholangiocytes during obstructive cholestasis in rat liver. Hepatology 33:783-791
72. Trauner M, Boyer JL 2003 Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 83:633-671
73. Jansen PL, Müller M 1999 Early events in sepsis-associated cholestasis. Gastroenterology 116:486-488
74. Hofmann AF 1999 The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med 159:2647-2658
75. Fickert P, Zollner G, Fuchsbichler A, Stumptner C, Pojer C, Zenz R, Lammert F, Stieger B, Meier PJ, Zatloukal K, Denk H, Trauner M 2001 Effects of ursodeoxycholic and cholic acid feeding on hepatocellular transporter expression in mouse liver. Gastroenterology 121:170-183
76. Hori Y, Ohyanagi H 1997 Protective effect of the intravenous administration of ursodeoxycholic acid against endotoxemia in rats with obstructive jaundice. Surg Today 27:140-144
77. Robertson GR, Farrell GC, Liddle C 1998 Sexually dimorphic expression of rat CYP3A9 and CYP3A18 genes is regulated by growth hormone. Biochem Biophys Res Commun 242:57-60
78. Kawai M, Bandiera SM, Chang TK, Bellward GD 2000 Growth hormone regulation and developmental expression of rat hepatic CYP3A18, CYP3A9, and CYP3A2. Biochem Pharmacol 59:1277-1287
79. Roe AL, Warren G, Hou G, Howard G, Shedlofsky SI, Blouin RA 1998 The effect of high dose endotoxin on CYP3A2 expression in the rat. Pharm Res 15:1603-1608
80. Takemura S, Minamiyama Y, Imaoka S, Funae Y, Hirohashi K, Inoue M, Kinoshita H 1999 Hepatic cytochrome P450 is directly inactivated by nitric oxide, not by inflammatory cytokines, in the early phase of endotoxemia. J Hepatol 30:1035-1044
81. Wietholtz H, Marschall HU, Sjovall J, Matern S 1996 Stimulation of bile acid 6α-hydroxylation by rifampin. J Hepatol 24:713-718
82. Mode A, Norstedt G, Simic B, Eneroth P, Gustafsson JA 1981 Continuous infusion of growth hormone feminizes hepatic steroid metabolism in the rat. Endocrinology 108:2103-2108
83. Baxter RC, Zaltsman Z 1984 Induction of hepatic receptors for growth hormone (GH) and prolactin by GH infusion is sex independent. Endocrinology 115:2009-2014