Evidence for carrier-mediated transport of unconjugated bilirubin across plasma membrane vesicles from human placental trophoblast

Placenta

Volumn 23, Issue 7, 2002, Pages 527-535

  Serrano, M A ^a   Bayon J E ^b   Pascolo, L ^c   Tiribelli, C ^c   Ostrow, J D ^d   Gonzalez Gallego, J ^b   Marin, J J G ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF LEÓN   (Spain)

^c UNIVERSITY OF TRIESTE   (Italy)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BILIRUBIN; BROMSULFOPHTHALEIN; CHOLIC ACID; DOXORUBICIN; ESTRADIOL 17 GLUCURONIDE; ESTRONE SULFATE; METHOTREXATE; SODIUM; VANADIC ACID; CARRIER PROTEIN; DRUG DERIVATIVE; ESTRADIOL; ESTRADIOL 17 BETA GLUCURONIDE; ESTRADIOL-17 BETA-GLUCURONIDE; ESTRONE; TRITIUM;

AMINO ACID TRANSPORT; ARTICLE; BILIRUBIN METABOLISM; CELL MEMBRANE POTENTIAL; CELL MEMBRANE TRANSPORT; DIFFUSION; DIFFUSION COEFFICIENT; DRUG INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; MEMBRANE VESICLE; PLACENTA; PLACENTA CIRCULATION; PRIORITY JOURNAL; TROPHOBLAST; CELL MEMBRANE; FEMALE; METABOLISM; OSMOLARITY; PREGNANCY; TEMPERATURE; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATE; BILIRUBIN; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; DIFFUSION; ESTRADIOL; ESTRONE; FEMALE; HUMANS; HYDROLYSIS; MEMBRANE POTENTIALS; OSMOLAR CONCENTRATION; PREGNANCY; SULFOBROMOPHTHALEIN; TEMPERATURE; TRITIUM; TROPHOBLASTS;

EID: 0036688934     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1053/plac.2002.0838     Document Type: Article

References (43)

1. Amit Y & Brenner T (1993) Age-dependent sensitivity of cultured rat glial cells to bilirubin toxicity. Exp Neurol, 121, 248-255.
2. Bashore RA, Smith F & Schenker S (1969) Placental transfer and disposition of bilirubin in the pregnant monkey. Am J Obstet Gynecol, 103, 950-958.
3. Bernstein RB, Novy MJ, Piasecki GJ, Lester R & Jackson BT (1969) Bilirubin metabolism in the fetus. J Clin Invest, 48, 1678-1688.
4. Bervoets K, Schlenzig JS & Bohles H (1994) Bilirubin in the early neonatal period. Is there a positive aspect of hyperbilirubinemia?-A medical hypothesis. Fortschr Med, 112, 192-194.
5. Booth AG, Olaniyan RO & Vanderpuye OA (1980) An improved method for the preparation of human placental syncytiotrophoblast microvilli. Placenta, 1, 327-336.
6. Bravo P, El-Mir MY, Serrano MA, Boyd CAR & Marin JJG (1993) Interaction between cholephilic anions and bile acid transport across basal membrane of human trophoblast. Am J Physiol, 265, G242-G250.
7. Bravo P, Marin JJG, Beveridge MJ & Novak DA (1995) Reconstitution and characterization of ATP-dependent bile acid transport in human and rat placenta. Biochem J, 311, 479-485.
8. Cui Y, Koning J, Leier I, Buchholz U & Keppler D (2001) Hepatic uptake of bilirrubin and its conjugates by the human organic anion-transporting polypeptide SLC21A6. J Biol Chem, 276, 9626-9630.
9. Dumaswala R, Setchell KDR, Moyer MS & Suchy FJ (1993) An anion exchanger mediates bile acid transport across the placental microvillous membrane. Am J Physiol, 264, G1016-G1023.
10. El-Mir MY, Eleno N, Serrano MA, Bravo P & Marin JJG (1991) Bicarbonate-induced activation of taurocholate transport across the basal plasma membrane of human term trophoblast. Am J Physiol, 260, G887-G894.
11. Gourley GR (1997) Bilirubin metabolism and kernicterus. Adv Pediatr, 44, 173-229.
12. Hahm JS, Ostrow JD, Mukerjee P & Celic L (1992) Ionization and self-association of unconjugated bilirubin, determined by rapid solvent partition from chloroform, with further studies of bilirubin solubility. J Lipid Res, 33, 1123-1137.
13. Iioka H, Moriyama I, Hino K & Ichijo MA (1986) A study on human placental bile acid transport system of taurocholate across microvillous membrane. Acta Obst Gynaec Jpn, 38, 837-844.
14. Jedlitschky G, Leier I, Buchholz U, Hummel-Eisenbeiss J, Burchell B & Keppler D (1997) ATP-dependent transport of bilirubin glucuronides by the multidrug resistance protein MRP1 and its hepatocyte canalicular isoform MRP2. Biochem J, 327, 305-310.
15. Kamisaka K, Listowsky I, Betheil JJ & Arias IM (1974) Competitive binding of bilirubin, sulfobromophthalein, indocyanine green and other organic anions to human and bovine serum albumin. Biochim Biophys Acta, 365, 169-180.
16. Kawade N & Onishi S (1981) The prenatal and postnatal development of UDPglucuronosyltransferase activity towards bilirubin and the effect of premature birth on this activity in the human liver. Biochem J, 196, 257-260.
17. Kelley LK, Smith CH & King BF (1983) Isolation and partial characterization of the basal cell membrane of human placental trophoblast. Biochim Biophys Acta, 734, 91-98.
18. Kipp H & Arias IM (2002) Trafficking of canalicular ABC transporters in hepatocytes. Annu Rev Physiol, 64, 595-608.
19. Lester R, Behrman RE & Lucey JF (1963) Transfer of bilirubin-C across monkey placenta. Pediatrics, 32, 416-419.
20. Marin JJG, Bravo P, El-Mir MY & Serrano MA (1995) ATP-dependent bile acid transport across the microvillous membrane of human term trophoblast. Am J Physiol, 268, G685-G694.
21. Marin JJG, Serrano MA, El-Mir MY, Eleno N & Boyd CAR (1990) Bile acid transport by basal membrane vesicles of human term placental trophoblast. Gastroenterology, 99, 1431-1438.
22. Markwell MAK, Haas SM, Bieber LL & Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem, 87, 206-210.
23. 3H]-bilirubin in freshly isolated rat hepatocytes: role of free bilirubin concentration. FEBS Lett, 463, 143-145.
24. Meier PJ & Stieger B (2002) Bile Salt Transporters. Annu Rev Physiol, 64, 635-661.
25. Monte MJ, Rodriguez-Bravo T, Macias RIR, Bravo P, El-Mir MY, Serrano MA, Lopez-Salva A & Marin JJG (1995) Relationship between bile acid transplacental gradients and transport across the fetal-facing plasma membrane of the human trophoblast. Pediatric Res, 38, 156-163.
26. Notter MF & Kendig JW (1986) Differential sensitivity of neural cells to bilirubin toxicity. Exp Neurol, 94, 670-682.
27. Ostrow JD, Mukerjee P & Tiribelli C (1994) Structure and binding of unconjugated bilirubin: Relevance for physiological and pathophysiological function. J Lipid Res, 35, 1715-1737.
28. Pascolo L, Bayon JE, Cupelli F, Ostrow JD & Tiribelli C (1998) ATP-dependent transport of unconjugated bilirubin by rat liver canalicular plasma membrane vesicles. Biochem J, 331, 99-103.
29. Pascolo L, Bayon JE, Serrano MA, Tiribelli C, Ostrow JD, González-Gallego J & Marin JJG (1998) Carrier-mediated passage of unconjugated bilirubin across human placenta. Hepatology (Abstract), 28, 605A.
30. 3H]-bilirubin and its uptake by rat liver basolateral plasma membrane vesicles. Biochem J, 316, 999-1004.
31. Pascolo L, Fernetti C, Garcia-Mediavilla MV, Ostrow JD & Tiribelli C (2001) Mechanisms for the transport of unconjugated bilirubin in human trophoblastic BeWo cells. FEBS Lett, 495, 94-99.
32. Petrovic S, Pascolo L, Gallo R, Cupelli F, Ostrow JD, Gofifeau A, Tiribelli C & Bruschi CV (2000) The products of YCF1 and YLL015w (BPT1) cooperate for the ATP-dependent vacuolar transport of unconjugated bilirubin in Saccharomyces cerevisiae. Yeast, 16, 561-571.
33. Schenker S, Dawber NH & Schmid R (1964) Bilirubin metabolism in the fetus. J Clin Invest, 43, 32-39.
34. Seidman DS, Ergaz Z, Paz I, Laor A, Revel-Vilk S, Stevenson DK & Gale R (1999) Predicting the risk of jaundice in full-term healthy newborns: a prospective population-based study. J Perinatol, 19, 564-567.
35. Sikic BI, Fisher GA, Lum BL, Halsey J, Beketicoreskovic L & Chen G (1997) Modulation and prevention of multidrug resistance by inhibitors of P-glycoprotein. Cancer Chemoth Pharmacol, 40, S13-S19.
36. St-Pierre MV, Serrano MA, Macias RIR, Dubs U, Hoechli M, Lauper U, Meier-Abt PJ & Marin JJG (2000) Expression of multidrug resistance associated proteins in human term placenta. Am J Physiol, 279, R1495-R1503.
37. Suchy FJ, Bucuvalas JC & Novak DA (1987) Determinants of bile formation during development: Ontogeny of hepatic bile acid metabolism and transport. Semin Liver Dis, 7, 77-84.
38. Terrenato L, Bertilaccio C, Spinelli P & Colombo B (1981) The switch from haemoglobin F to A: the time course of qualitative and quantitative variations of haemoglobins after birth. Br J Haematol, 47, 31-41.
39. Wang P, Chowdhury JR, Kim R & Wolkoff AW (2001) Expression of the human organic anion transporting protein OATP2 (OATP-C) is not sufficient to produce bilirubin transport. Hepatology (Abstract), 34, 265A.
40. Webster C, Tiribelli C & Ostrow JD (2001) An improved method for isolation of unconjugated bilirubin from rat and dog bile. J Lab Clin Med, 137, 370-373.
41. Weisiger RA, Ostrow JD, Koehler RK, Webster CC, Mukerjee P, Pascolo L & Tiribelli C (2001) Affinity of human serum albumin for bilirubin varies with albumin concentration and buffer composition: results of a novel ultrafiltration method. J Biol Chem, 276, 29953-29960.
42. Zeng H, Liu G, Rea PA & Kruh GD (2000) Transport of amphipathic anions by human Multidrug Resistance Protein 3. Cancer Res, 60, 4779-4784.
43. Zucker SD & Goessling W (2000) Mechanism of hepatocellular uptake of albumin-bound bilirubin. Biochim Biophys Acta, 1464, 7-17.