RNA-seq reveals different mRNA abundance of transporters and their alternative transcript isoforms during liver development

Toxicological Sciences

Volumn 127, Issue 2, 2012, Pages 592-608

  Cui, Julia Yue ^a   Gunewardena, Sumedha S ^b   Yoo, Byunggil ^b   Liu, Jie ^a   Renaud, Helen J ^a   Lu, Hong ^c   Zhong, Xiao bo ^a   Klaassen, Curtis D ^a  

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

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Development; Liver; Mouse; RNA Seq; Systems toxicology; Transporters

Indexed keywords

ABC TRANSPORTER A1; BREAST CANCER RESISTANCE PROTEIN; CARRIER PROTEIN; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; MEMBRANE PROTEIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 6; NTCP PROTEIN; NUCLEOSIDE TRANSPORTER; OCTAMER TRANSCRIPTION FACTOR; OCTAMER TRANSCRIPTION FACTOR 1; OCTAMER TRANSCRIPTION FACTOR 2; OCTAMER TRANSCRIPTION FACTOR 4; OCTN1 PROTEIN; OCTN2 PROTEIN; OCTN3 PROTEIN; ORGANIC CATION TRANSPORTER 1; PEPTIDE TRANSPORTER 1; PEPTIDE TRANSPORTER 2; PROTEIN OCTN3; TRANSCRIPTOME; UNCLASSIFIED DRUG; UNINDEXED DRUG; URATE ANION EXCHANGER 1 PROTEIN; WILSON DISEASE PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ANALYSIS; LIVER DEVELOPMENT; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; PROTEIN EXPRESSION; RNA ISOLATION; RNA SEQUENCE;

MUS;

EID: 84861467587     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs107     Document Type: Article

References (60)

1. Blencowe, B. J., Ahmad, S., and Lee, L. J. (2009). Current-generation highthroughput sequencing: Deepening insights into mammalian transcriptomes. Genes Dev. 23, 1379-1386.
2. Bublitz, M., Morth, J. P., and Nissen, P. (2011). P-type ATPases at a glance. J. Cell Sci. 124, 2515-2519.
3. Bull, L. N., van Eijk, M. J., Pawlikowska, L., DeYoung, J. A., Juijn, J. A., Liao, M., Klomp, L. W., Lomri, N., Berger, R., Scharschmidt, B. F., et al. (1998). A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat. Genet. 18, 219-224.
4. Chen, H. L., Liu, Y. J., Feng, C. H., Wu, C. Y., Shyu, M. K., Yuan, R. H., and Chang, M. H. (2005). Developmental expression of canalicular transporter genes in human liver. J. Hepatol. 43, 472-477.
5. Cheng, X., Buckley, D., and Klaassen, C. D. (2007). Regulation of hepatic bile acid transporters Ntcp and Bsep expression. Biochem. Pharmacol. 74, 1665-1676.
6. Cheng, X., and Klaassen, C. D. (2006). Regulation of mRNA expression of xenobiotic transporters by the pregnane x receptor in mouse liver, kidney, and intestine. Drug Metab. Dispos. 34, 1863-1867.
7. Cheng, X., and Klaassen, C. D. (2009). Tissue distribution, ontogeny, and hormonal regulation of xenobiotic transporters in mouse kidneys. Drug Metab. Dispos. 37, 2178-2185.
8. Cheng, X., Maher, J., Chen, C., and Klaassen, C. D. (2005). Tissue distribution and ontogeny of mouse organic anion transporting polypeptides (Oatps). Drug Metab. Dispos. 33, 1062-1073.
9. Choudhuri, S., and Klaassen, C. D. (2006). Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int. J. Toxicol. 25, 231-259.
10. Crom, W. R., Relling, M. V., Christensen, M. L., Rivera, G. K., and Evans, W. E. (1991). Age-related differences in hepatic drug clearance in children: Studies with lorazepam and antipyrine. Clin. Pharmacol. Ther. 50, 132-140.
11. Csanaky, I. L., Lu, H., Zhang, Y., Ogura, K., Choudhuri, S., and Klaassen, C. D. (2011). Organic anion-transporting polypeptide 1b2 (Oatp1b2) is important for the hepatic uptake of unconjugated bile acids: Studies in Oatp1b2-null mice. Hepatology 53, 272-281.
12. Cui, J. Y., Aleksunes, L. M., Tanaka, Y., Fu, Z. D., Guo, Y., Guo, G. L., Lu, H., Zhong, X. B., and Klaassen, C. D. (2012). Bile acids via FXR initiate the expression of major transporters involved in the enterohepatic circulation of bile acids in newborn mice. Am. J. Physiol. Gastrointest. Liver Physiol.
13. Cui, J. Y., Gunewardena, S. S., Rockwell, C. E., and Klaassen, C. D. (2010). ChIPing the cistrome of PXR in mouse liver. Nucleic Acids Res. 38, 7943-7963.
14. Cui, Y. J., Cheng, X., Weaver, Y. M., and Klaassen, C. D. (2009). Tissue distribution, gender-divergent expression, ontogeny, and chemical inductionof multidrug resistance transporter genes (Mdr1a, Mdr1b, Mdr2) in mice. Drug Metab. Dispos. 37, 203-210.
15. Dawson, P. A., Hubbert, M., Haywood, J., Craddock, A. L., Zerangue, N., Christian, W. V., and Ballatori, N. (2005). The heteromeric organic solute transporter alpha-beta, Ostalpha-Ostbeta, is an ileal basolateral bile acid transporter. J. Biol. Chem. 280, 6960-6968.
16. de Vree, J. M., Jacquemin, E., Sturm, E., Cresteil, D., Bosma, P. J., Aten, J., Deleuze, J. F., Desrochers, M., Burdelski, M., Bernard, O., et al. (1998). Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc. Natl. Acad. Sci. U.S.A. 95, 282-287.
17. de Wildt, S. N., Kearns, G. L., Leeder, J. S., and van den Anker, J. N. (1999). Cytochrome P450 3A: Ontogeny and drug disposition. Clin. Pharmacokinet. 37, 485-505.
18. Dean, M., Hamon, Y., and Chimini, G. (2001). The human ATP-binding cassette (ABC) transporter superfamily. J. Lipid Res. 42, 1007-1017.
19. Desuzinges-Mandon, E., Arnaud, O., Martinez, L., Huche, F., Di Pietro, A., and Falson, P. (2010). ABCG2 transports and transfers heme to albumin through its large extracellular loop. J. Biol. Chem. 285, 33123-33133.
20. Evans, W. E., Relling, M. V., de Graaf, S., Rodman, J. H., Pieper, J. A., Christensen, M. L., and Crom, W. R. (1989). Hepatic drug clearance in children: Studies with indocyanine green as a model substrate. J. Pharm. Sci. 78, 452-456.
21. Fullwood, M. J., Wei, C. L., Liu, E. T., and Ruan, Y. (2009). Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res. 19, 521-532.
22. Gamba, G. (2001). Alternative splicing and diversity of renal transporters. Am. J. Physiol. Renal Physiol. 281, F781-F794.
23. Hagenbuch, B., and Meier, P. J. (2004). Organic anion transporting polypeptides of the OATP/ SLC21 family: Phylogenetic classification as OATP/ SLCO superfamily, new nomenclature and molecular/functional properties. Pflugers Arch. 447, 653-665.
24. Hagenbuch, B., Scharschmidt, B. F., and Meier, P. J. (1996). Effect of antisense oligonucleotides on the expression of hepatocellular bile acid and organic anion uptake systems in Xenopus laevis oocytes. Biochem. J. 316, 901-904.
25. Hediger, M. A., Romero, M. F., Peng, J. B., Rolfs, A., Takanaga, H., and Bruford, E. A. (2004). The ABCs of solute carriers: Physiological, pathological and therapeutic implications of human membrane transport proteins: Introduction. Pflugers Arch. 447, 465-468.
26. Heubi, J. E., Balistreri, W. F., Partin, J. C., Schubert, W. K., and McGraw, C. A. (1979). Refractory infantile diarrhea due to primary bile acid malabsorption. J. Pediatr. 94, 546-551.
27. Hines, R. N. (2006). Developmental and tissue-specific expression of human flavin-containing monooxygenases 1 and 3. Expert Opin. Drug Metab. Toxicol. 2, 41-49.
28. Hines, R. N. (2007). Ontogeny of human hepatic cytochromes P450. J. Biochem. Mol. Toxicol. 21, 169-175.
29. Kearns, G. L., Abdel-Rahman, S. M., Alander, S. W., Blowey, D. L., Leeder, J. S., and Kauffman, R. E. (2003). Developmental pharmacology- Drug disposition, action, and therapy in infants and children. N. Engl. J. Med. 349, 1157-1167.
30. Klaassen, C. D. (1972). Immaturity of the newborn rat's hepatic excretory function for ouabain. J. Pharmacol. Exp. Ther. 183, 520-526.
31. Klaassen, C. D. (1978). Independence of bile acid and ouabain hepatic uptake: Studies in the newborn rat. Proc. Soc. Exp. Biol. Med. 157, 66-69.
32. Klaassen, C. D., and Aleksunes, L. M. (2010). Xenobiotic, bile acid, and cholesterol transporters: Function and regulation. Pharmacol. Rev. 62, 1-96.
33. Klaassen, C. D., and Lu, H. (2008). Xenobiotic transporters: Ascribing function from gene knockout and mutation studies. Toxicol. Sci. 101, 186-196.
34. Klaassen, C. D., and Slitt, A. L. (2005). Regulation of hepatic transporters by xenobiotic receptors. Curr. Drug Metab. 6, 309-328.
35. Knisely, A. S., Strautnieks, S. S., Meier, Y., Stieger, B., Byrne, J. A., Portmann, B. C., Bull, L. N., Pawlikowska, L., Bilezikci, B., Ozcay, F., et al. (2006). Hepatocellular carcinoma in ten children under five years of age with bile salt export pump deficiency. Hepatology 44, 478-486.
36. La Fontaine, S. L., Firth, S. D., Camakaris, J., Englezou, A., Theophilos, M. B., Petris, M. J., Howie, M., Lockhart, P. J., Greenough, M., Brooks, H., et al. (1998). Correction of the copper transport defect of Menkes patient fibroblasts by expression of the Menkes and Wilson ATPases. J. Biol. Chem. 273, 31375-31380.
37. Lee, J. S., Ward, W. O., Knapp, G., Ren, H., Vallanat, B., Abbott, B., Ho, K., Karp, S. J., and Corton, J. C. (2012). Transcriptional ontogeny of the developing liver. BMC Genomics 13, 33.
38. Lee, J. S., Ward, W. O., Liu, J., Ren, H., Vallanat, B., Delker, D., and Corton, J. C. (2011). Hepatic xenobiotic metabolizing enzyme and transporter gene expression through the life stages of the mouse. PLoS One 6, e24381.
39. Li, T., Huang, J., Jiang, Y., Zeng, Y., He, F., Zhang, M. Q., Han, Z., and Zhang, X. (2009). Multi-stage analysis of gene expression and transcription regulation in C57/B6 mouse liver development. Genomics 93, 235-242.
40. Lickteig, A. J., Cheng, X., Augustine, L. M., Klaassen, C. D., and Cherrington, N. J. (2008). Tissue distribution, ontogeny and induction of the transporters Multidrug and toxin extrusion (MATE) 1 and MATE2 mRNA expression levels in mice. Life Sci. 83, 59-64.
41. Lopez, A. J. (1998). Alternative splicing of pre-mRNA: Developmental consequences and mechanisms of regulation. Annu. Rev. Genet. 32, 279-305.
42. Maher, J. M., Slitt, A. L., Cherrington, N. J., Cheng, X., and Klaassen, C. D. (2005). Tissue distribution and hepatic and renal ontogeny of the multidrug resistance-associated protein (Mrp) family in mice. Drug Metab. Dispos. 33, 947-955.
43. Maran, R. R., Thomas, A., Roth, M., Sheng, Z., Esterly, N., Pinson, D., Gao, X., Zhang, Y., Ganapathy, V., Gonzalez, F. J., et al. (2009). Farnesoid X receptor deficiency in mice leads to increased intestinal epithelial cell proliferation and tumor development. J. Pharmacol. Exp. Ther. 328, 469-477.
44. Meyer Zu Schwabedissen, H. E., Ware, J. A., Tirona, R. G., and Kim, R. B. (2009). Identification, expression, and functional characterization of fulllength and splice variants of murine organic anion transporting polypeptide 1b2. Mol. Pharm. 6, 1790-1797.
45. Mizuno, N., Niwa, T., Yotsumoto, Y., and Sugiyama, Y. (2003). Impact of drug transporter studies on drug discovery and development. Pharmacol. Rev. 55, 425-461.
46. Moroy, T., and Heyd, F. (2007). The impact of alternative splicing in vivo: Mouse models show the way. RNA 13, 1155-1171.
47. Nakanishi, T., Bailey-Dell, K. J., Hassel, B. A., Shiozawa, K., Sullivan, D. M., Turner, J., and Ross, D. D. (2006). Novel 5' untranslated region variants of BCRP mRNA are differentially expressed in drugselected cancer cells and in normal human tissues: Implications for drug resistance, tissue-specific expression, and alternative promoter usage. Cancer Res. 66, 5007-5011.
48. Natarajan, K., Xie, Y., Nakanishi, T., Beck, W. T., Bauer, K. S., and Ross, D. D. (2011). Identification and characterization of the major alternative promoter regulating Bcrp1/Abcg2 expression in the mouse intestine. Biochim. Biophys. Acta 1809, 295-305.
49. Pedersen, P. L. (2007). Transport ATPases into the year 2008: A brief overview related to types, structures, functions and roles in health and disease. J. Bioenerg. Biomembr. 39, 349-355.
50. Repa, J. J., Berge, K. E., Pomajzl, C., Richardson, J. A., Hobbs, H., and Mangelsdorf, D. J. (2002). Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. J. Biol. Chem. 277, 18793-18800.
51. Richard, K., Hume, R., Kaptein, E., Stanley, E. L., Visser, T. J., and Coughtrie, M. W. (2001). Sulfation of thyroid hormone and dopamine during human development: Ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain. J. Clin. Endocrinol. Metab. 86, 2734-2742.
52. Robinson, J. T., Thorvaldsdottir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., and Mesirov, J. P. (2011). Integrative genomics viewer. Nat. Biotechnol. 29, 24-26.
53. Strassburg, C. P., Strassburg, A., Kneip, S., Barut, A., Tukey, R. H., Rodeck, B., and Manns, M. P. (2002). Developmental aspects of human hepatic drug glucuronidation in young children and adults. Gut 50, 259-265.
54. Tanaka, K., Fujimura-Kamada, K., and Yamamoto, T. (2011). Functions of phospholipid flippases. J. Biochem. 149, 131-143.
55. Terada, K., Nakako, T., Yang, X. L., Iida, M., Aiba, N., Minamiya, Y., Nakai, M., Sakaki, T., Miura, N., and Sugiyama, T. (1998). Restoration of holoceruloplasmin synthesis in LEC rat after infusion of recombinant adenovirus bearing WND cDNA. J. Biol. Chem. 273, 1815-1820.
56. Thomas, A. M., Hart, S. N., Kong, B., Fang, J., Zhong, X. B., and Guo, G. L. (2010). Genome-wide tissue-specific farnesoid X receptor binding in mouse liver and intestine. Hepatology 51, 1410-1419.
57. Wakaumi, M., Ishibashi, K., Ando, H., Kasanuki, H., and Tsuruoka, S. (2005). Acute digoxin loading reduces ABCA8A mRNA expression in the mouse liver. Clin. Exp. Pharmacol. Physiol. 32, 1034-1041.
58. Wang, L., Soroka, C. J., and Boyer, J. L. (2002). The role of bile salt export pump mutations in progressive familial intrahepatic cholestasis type II. J. Clin. Investig. 110, 965-972.
59. Wang, R., Lam, P., Liu, L., Forrest, D., Yousef, I. M., Mignault, D., Phillips, M. J., and Ling, V. (2003). Severe cholestasis induced by cholic acid feeding in knockout mice of sister of P-glycoprotein. Hepatology 38, 1489-1499.
60. Zong, Y., Zhou, S., Fatima, S., and Sorrentino, B. P. (2006). Expression of mouse Abcg2 mRNA during hematopoiesis is regulated by alternative use of multiple leader exons and promoters. J. Biol. Chem. 281, 29625-29632.