Expression and hepatobiliary transport characteristics of the concentrative and equilibrative nucleoside transporters in sandwich-cultured human hepatocytes

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 3, 2008, Pages

  Govindarajan, Rajgopal ^a   Endres, Christopher J ^a   Whittington, Dale ^a   LeCluyse, Edward ^b   Pastor Anglada, Marçal ^c   Tse, Chung Ming ^d   Unadkat, Jashvant D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b CellzDirect   (United States)

^c UNIVERSITY OF BARCELONA   (Spain)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biliary efflux; Biliary excretion; Hepatic diseases; Human concentrative nucleoside transporters; Human equilibrative nucleoside transporters; Localization; mRNA; Nucleoside drugs; Phosphorylation; Protein expression

Indexed keywords

EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 2; FIALURIDINE; FORMYCIN B; GUANOSINE; MESSENGER RNA; NUCLEOSIDE TRANSPORTER; RIBAVIRIN; THYMIDINE; CARRIER PROTEIN; CIF NUCLEOSIDE TRANSPORTER; DRUG DERIVATIVE; FORMYCIN DERIVATIVE; NUCLEOSIDE; SLC29A1 PROTEIN, HUMAN; SLC29A2 PROTEIN, HUMAN; URACIL ARABINOSIDE;

ADULT; AGED; ARTICLE; BILE; CELL CULTURE; CELL MEMBRANE; CELLULAR DISTRIBUTION; DRUG DISTRIBUTION; DRUG METABOLISM; EFFUSION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; LIVER CELL; MALE; NUCLEOSIDE TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; CULTURE TECHNIQUE; GENETICS; METABOLISM; MIDDLE AGED;

ADULT; AGED; ARABINOFURANOSYLURACIL; BILE; CELL CULTURE TECHNIQUES; CELL MEMBRANE; CELLS, CULTURED; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; EQUILIBRATIVE-NUCLEOSIDE TRANSPORTER 2; FEMALE; FORMYCINS; GUANOSINE; HEPATOCYTES; HUMANS; MALE; MEMBRANE TRANSPORT PROTEINS; MIDDLE AGED; NUCLEOSIDES; RIBAVIRIN; RNA, MESSENGER; THYMIDINE;

EID: 53449102537     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00542.2007     Document Type: Article

References (40)

1. Aymerich I, Pastor-Anglada M, Casado FJ. Long term endocrine regulation of nucleoside transporters in rat intestinal epithelial cells. J Gen Physiol 124: 505-512, 2004.
2. Baldwin SA, Beal PR, Yao SY, King AE, Cass CE, Young JD. The equilibrative nucleoside transporter family, SLC29. Pflügers Arch 447: 735-743, 2004.
3. Baldwin SA, Yao SY, Hyde RJ, Ng AM, Foppolo S, Barnes K, Ritzel MW, Cass CE, Young JD. Functional characterization of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes. J Biol Chem 280: 15880-15887, 2005.
4. Bender V, Buschlen S, Cassio D. Expression and localization of hepatocyte domain-specific plasma membrane proteins in hepatoma x fibroblast hybrids and in hepatoma dedifferentiated variants. J Cell Sci 111: 3437-3450, 1998.
5. Berthiaume F, Moghe PV, Toner M, Yarmush ML. Effect of extracellular matrix topology on cell structure, function, and physiological responsiveness: hepatocytes cultured in a sandwich configuration. FASEB J 10: 1471-1484, 1996.
6. Burke T, Lee S, Ferguson PJ, Hammond JR. Interaction of 2′,2′-difluorodeoxycytidine (gemcitabine) and formycin B with the Na+-dependent and -independent nucleoside transporters of Ehrlich ascites tumor cells. J Pharmacol Exp Ther 286: 1333-1340, 1998.
7. Casado FJ, Lostao MP, Aymerich I, Larrayoz IM, Duflot S, Rodriguez-Mulero S, Pastor-Anglada M. Nucleoside transporters in absorptive epithelia. J Physiol Biochem 58: 207-216, 2002.
8. Casanova JE, Mishumi Y, Ikehara Y, Hubbard AL, Mostov KE. Direct apical sorting of rat liver dipeptidylpeptidase IV expressed in Madin-Darby canine kidney cells. J Biol Chem 266: 24428-24432, 1991.
9. Chandrasena G, Giltay R, Patil SD, Bakken A, Unadkat JD. Functional expression of human intestinal Na+-dependent and Na+-independent nucleoside transporters in Xenopus laevis oocytes. Biochem Pharmacol 53: 1909-1918, 1997.
10. Chang C, Swaan PW, Ngo LY, Lum PY, Patil SD, Unadkat JD. Molecular requirements of the human nucleoside transporters hCNT1, hCNT2, and hENT1. Mol Pharmacol 65: 558-570, 2004.
11. Che M, Nishida T, Gatmaitan Z, Arias IM. A nucleoside transporter is functionally linked to ectonucleotidases in rat liver canalicular membrane. J Biol Chem 267: 9684-9688, 1992.
12. del Santo B, Valdes R, Mata J, Felipe A, Casado FJ, Pastor-Anglada M. Differential expression and regulation of nucleoside transport systems in rat liver parenchymal and hepatoma cells. Hepatology 28: 1504-1511, 1998.
13. del Santo B, Tarafa G, Felipe A, Casado FJ, Pastor-Anglada M. Developmental regulation of the concentrative nucleoside transporters CNT1 and CNT2 in rat liver. J Hepatol 34: 873-880, 2001.
14. Duflot S, Calvo M, Casado FJ, Enrich C, Pastor-Anglada M. Concentrative nucleoside transporter (rCNT1) is targeted to the apical membrane through the hepatic transcytotic pathway. Exp Cell Res 281: 77-85, 2002.
15. Dunn JC, Tompkins RG, Yarmush ML. Hepatocytes in collagen sandwich: evidence for transcriptional and translational regulation. J Cell Biol 116: 1043-1053, 1992.
16. Elaut G, Henkens T, Papeleu P, Snykers S, Vinken M, Vanhaecke T, Rogiers V. Molecular mechanisms underlying the dedifferentiation process of isolated hepatocytes and their cultures. Curr Drug Metab 7: 629-660, 2006.
17. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436: 967-972, 2005.
18. Fernandez-Veledo S, Jover R, Casado FJ, Gomez-Lechon MJ, Pastor-Anglada M. Transcription factors involved in the expression of SLC28 genes in human liver parenchymal cells. Biochem Biophys Res Commun 353: 381-388, 2007.
19. Food and Drug Administration. Report of an FDA Task Force: Hepatic and Pancreatic Toxicity. Washington, DC: Food and Drug Administration, 1993.
20. Ghibellini G, Vasist LS, Leslie EM, Heizer WD, Kowalsky RJ, Calvo BF, Brouwer KL. In vitro-in vivo correlation of hepatobiliary drug clearance in humans. Clin Pharmacol Ther 81: 406-413, 2007.
21. Govindarajan R, Bakken AH, Hudkins KL, Lai Y, Casado FJ, Pastor-Anglada M, Tse CM, Hayashi J, Unadkat JD. In situ hybridization and immunolocalization of concentrative and equilibrative nucleoside transporters in the human intestine, liver, kidneys, and placenta. Am J Physiol Regul Integr Comp Physiol 293: R1809-R1822, 2007.
22. Gray JH, Owen RP, Giacomini KM. The concentrative nucleoside transporter family, SLC28. Pflügers Arch 447: 728-734, 2004.
23. Hoffmaster KA, Turncliff RZ, LeCluyse EL, Kim RB, Meier PJ, Brouwer KL. P-glycoprotein expression, localization, and function in sandwich-cultured primary rat and human hepatocytes: relevance to the hepatobiliary disposition of a model opioid peptide. Pharm Res 21: 1294-1302, 2004.
24. Hoofnagle JH, Seeff LB. Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med 355: 2444-2451, 2006.
25. Hu H, Endres CJ, Chang C, Umapathy NS, Lee EW, Fei YJ, Itagaki S, Swaan PW, Ganapathy V, Unadkat JD. Electrophysiological characterization and modeling of the structure activity relationship of the human concentrative nucleoside transporter 3 (hCNT3). Mol Pharmacol 69: 1542-1553, 2006.
26. Jarvis SM, Thorn JA, Glue P. Ribavirin uptake by human erythrocytes and the involvement of nitrobenzylthioinosine-sensitive (es)-nucleoside transporters. Br J Pharmacol 123: 1587-1592, 1998.
27. Kong W, Engel K, Wang J. Mammalian nucleoside transporters. Curr Drug Metab 5: 63-84, 2004.
28. Lai Y, Bakken AH, Unadkat JD. Simultaneous expression of hCNT1-CFP and hENT1-YFP in Madin-Darby canine kidney cells. Localization and vectorial transport studies. J Biol Chem 277: 37711-37717, 2002.
29. Lai Y, Tse CM, Unadkat JD. Mitochondrial expression of the human equilibrative nucleoside transporter 1 (hENT1) results in enhanced mitochondrial toxicity of antiviral drugs. J Biol Chem 279: 4490-4497, 2004.
30. Lertora JJ, Rege AB, Lacour JT, Ferencz N, George WJ, VanDyke RB, Agrawal KC, Hyslop NE Jr. Pharmacokinetics and long-term tolerance to ribavirin in asymptomatic patients infected with human immunodeficiency virus. Clin Pharmacol Ther 50: 442-449, 1991.
31. Liu X, LeCluyse EL, Brouwer KR, Gan LS, Lemasters JJ, Stieger B, Meier PJ, Brouwer KL. Biliary excretion in primary rat hepatocytes cultured in a collagen-sandwich configuration. Am J Physiol Gastrointest Liver Physiol 277: G12-G21, 1999.
32. Liu X, Chism JP, LeCluyse EL, Brouwer KR, Brouwer KL. Correlation of biliary excretion in sandwich-cultured rat hepatocytes and in vivo in rats. Drug Metab Dispos 27: 637-644, 1999.
33. Mangravite LM, Xiao G, Giacomini KM. Localization of human equilibrative nucleoside transporters, hENT1 and hENT2, in renal epithelial cells. Am J Physiol Renal Physiol 284: F902-F910, 2003.
34. McKenzie R, Fried MW, Sallie R, Conjeevaram H, Di Bisceglie AM, Park Y, Savarese B, Kleiner D, Tsokos M, Luciano C, Pruett T, Stokka JL, Straus SE, Hoofnagle JH. Hepatic failure and lactic acidosis due to fialuridine (FIAU), an investigational nucleoside analogue for chronic hepatitis B. N Engl J Med 333: 1099-1105, 1995.
35. +-nucleoside transporters in the human intestine. Am J Physiol Gastrointest Liver Physiol 280: G475-G481, 2001.
36. Paroni R, Del Puppo M, Borghi C, Sirtori CR, Galli Kienle M. Pharmacokinetics of ribavirin and urinary excretion of the major metabolite 1,2,4-triazole-3-carboxamide in normal volunteers. Int J Clin Pharmacol Ther Toxicol 27: 302-307, 1989.
37. Patil SD, Ngo LY, Glue P, Unadkat JD. Intestinal absorption of ribavirin is preferentially mediated by the Na+-nucleoside purine (N1) transporter. Pharm Res 15: 950-952, 1998.
38. Patil SD, Unadkat JD. Sodium-dependent nucleoside transport in the human intestinal brush-border membrane. Am J Physiol Gastrointest Liver Physiol 272: G1314-G1320, 1997.
39. Preston SL, Drusano GL, Glue P, Nash J, Gupta SK, McNamara P. Pharmacokinetics and absolute bioavailability of ribavirin in healthy volunteers as determined by stable-isotope methodology. Antimicrob Agents Chemother 43: 2451-2456, 1999.
40. Zhang P, Tian X, Chandra P, Brouwer KL. Role of glycosylation in trafficking of Mrp2 in sandwich-cultured rat hepatocytes. Mol Pharmacol 67: 1334-1341, 2005.