Missense mutations and single nucleotide polymorphisms in ABCB11 impair bile salt export pump processing and function or disrupt pre-messenger RNA splicing

Hepatology

Volumn 49, Issue 2, 2009, Pages 553-567

  Byrne, Jane A ^a,f   Strautnieks, Sandra S ^a   Ihrke, Gudrun ^b   Pagani, Franco ^c   Knisely, A S ^d   Linton, Kenneth J ^e,f   Mieli Vergani, Giorgina ^a   Thompson, Richard J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^d KING S COLLEGE HOSPITAL   (United Kingdom)

^e IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER B11; BILE SALT EXPORT PUMP PROTEIN; GLYCEROL; MESSENGER RNA; MESSENGER RNA PRECURSOR; TAUROCHOLIC ACID; UNCLASSIFIED DRUG; ABCB11 PROTEIN, HUMAN; BILE ACID; RNA PRECURSOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHO CELL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXON; GENE FREQUENCY; HUMAN; HUMAN CELL; IN VITRO STUDY; INCUBATION TEMPERATURE; INTRAHEPATIC CHOLESTASIS; LOW TEMPERATURE PROCEDURES; MISSENSE MUTATION; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TRANSPORT; RNA SPLICING; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; CELL LINE; CRICETULUS; DOG; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HAMSTER; INTRON; METABOLISM;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE ACIDS AND SALTS; CELL LINE; CHO CELLS; CHOLESTASIS, INTRAHEPATIC; CRICETINAE; CRICETULUS; DOGS; EXONS; GENE EXPRESSION REGULATION; HUMANS; INTRONS; MUTATION, MISSENSE; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA PRECURSORS; RNA SPLICING; TRANSFECTION;

EID: 61949292897     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.22683     Document Type: Article

References (67)

1. Meier PJ, Stieger B. Bile salt transporters. Annu Rev Physiol 2002;64:635-661.
2. Higgins CF. ABC transporters: From microorganisms to man. Annu Rev Cell Biol 1992;8:67-113.
3. Byrne JA, Strautnieks SS, Mieli-Vergani G, Higgins CF, Linton KJ, Thompson RJ. The human bile salt export pump: Characterization of substrate specificity and identification of inhibitors. Gastroenterology 2002; 123:1649-1658.
4. Noe J, Stieger B, Meier PJ. Functional expression of the canalicular bile salt export pump of human liver. Gastroenterology 2002;123:1659-1666.
5. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, et al. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 1998;273:10046-10050.
6. Noe J, Hagenbuch B, Meier PJ, St-Pierre MV. Characterization of the mouse bile salt export pump overexpressed in the baculovirus system. HEPATOLOGY 2001;33:1223-1231.
7. Strautnieks SS, Bull LN, Knisely AS, Kocoshis SA, Dahl N, Arnell H, et al. A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat Genet 1998;20:233-238.
8. van Mil SW, van der Woerd WL, van der Brugge G, Sturm E, Jansen PL, Bull LN, et al. Benign recurrent intrahepatic cholestasis type 2 is caused by mutations in ABCB11. Gastroenterology 2004;127:379-384.
9. Arrese M, Macias RI, Briz O, Perez MJ, Marin JJ. Molecular pathogenesis of intrahepatic cholestasis of pregnancy. Expert Rev Mol Med 2008;10:e9.
10. Stieger B, Meier Y, Meier PJ. The bile salt export pump. Pflugers Arch 2007;453:611-620.
11. Wang L, Soroka CJ, Boyer JL. The role of bile salt export pump mutations in progressive familial intrahepatic cholestasis type II. J Clin Invest 2002; 110:965-972.
12. Noe J, Kullak-Ublick GA, Jochum W, Stieger B, Kerb R, Haberl M, et al. Impaired expression and function of the bile salt export pump due to three novel ABCB11 mutations in intrahepatic cholestasis. J Hepatol 2005;43: 536-543.
13. Hayashi H, Takada T, Suzuki H, Akita H, Sugiyama Y. Two common PFIC2 mutations are associated with the impaired membrane trafficking of BSEP/ ABCB11. HEPATOLOGY 2005;41:916-924.
14. Kagawa T, Watanabe N, Mochizuki K, Numari A, Ikeno Y, Itoh J, et al. Phenotypic differences in PFIC2 and BRIC2 correlate with protein stability of mutant Bsep and impaired taurocholate secretion in MDCK II cells. Am J Physiol Gastrointest Liver Physiol 2008;294:G58-G67.
15. Lam P, Pearson CL, Soroka CJ, Xu S, Mennone A, Boyer JL. Levels of plasma membrane expression in progressive and benign mutations of the bile salt export pump (Bsep/Abcb11) correlate with severity of cholestatic diseases. Am J Physiol Cell Physiol 2007;293:C1709-C1716.
16. Ars E, Serra E, Garcia J, Kruyer H, Gaona A, Lazaro C, et al. Mutations affecting mRNA splicing are the most common molecular defects in patients with neurofibromatosis type 1. Hum Mol Genet 2000;9:237-247.
17. Cartegni L, Chew SL, Krainer AR. Listening to silence and understanding nonsense: Exonic mutations that affect splicing. Nat Rev Genet 2002;3: 285-298.
18. Wang GS, Cooper TA. Splicing in disease: Disruption of the splicing code and the decoding machinery. Nat Rev Genet 2007;8:749-761.
19. Gorlov IP, Gorlova OY, Frazier ML, Amos CI. Missense mutations in hMLH1 and hMSH2 are associated with exonic splicing enhancers. Am J Hum Genet 2003;73:1157-1161.
20. Caceres JF, Kornblihtt AR. Alternative splicing: Multiple control mechanisms and involvement in human disease. Trends Genet 2002;18:186-193.
21. Liu HX, Cartegni L, Zhang MQ, Krainer AR. A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nat Genet 2001;27:55-58.
22. Niksic M, Romano M, Buratti E, Pagani F, Baralle FE. Functional analysis of cis-acting elements regulating the alternative splicing of human CFTR exon 9. Hum Mol Genet 1999;8:2339-2349.
23. Aridor H. Traffic jams : A compendium of human diseases that affect intracellular transport processes. Traffic 2000;1:836-851.
24. Skach WR. Defects in processing and trafficking of the cystic fibrosis transmembrane conductance regulator. Kidney Int 2000;57:825-831.
25. Pagani F, Buratti E, Stuani C, Romano M, Zuccato E, Niksic M, et al. Splicing factors induce cystic fibrosis transmembrane regulator exon 9 skipping through a nonevolutionary conserved intronic element. J Biol Chem 2000;275:21041-21047.
26. Byrne JA, Meara NJ, Rayner AC, Thompson RJ, Knisely AS. Lack of hepatocellular CD10 along bile canaliculi is physiologic in early childhood and persistent in Alagille syndrome. Lab Invest 2007;87:1138-1148.
27. Chuang JZ, Sung CH. The cytoplasmic tail of rhodopsin acts as a novel apical sorting signal in polarized MDCK cells. J Cell Biol 1998;142:1245-1256.
28. Chen HL, Chang PS, Hsu HC, Ni YH, Hsu HY, Lee JH, et al. FIC1 and BSEP defects in Taiwanese patients with chronic intrahepatic cholestasis with low gamma-glutamyltranspeptidase levels. J Pediatr 2002;140:119-124.
29. Jansen PL, Strautnieks SS, Jacquemin E, Hadchouel M, Sokal EM, Hooiveld GJ, et al. Hepatocanalicular bile salt export pump deficiency in patients with progressive familial intrahepatic cholestasis. Gastroenterology 1999;117:1370-1379.
30. Knisely AS, Strautnieks SS, Meier Y, Stieger B, Byrne JA, Portmann BC, et al. Hepatocellular carcinoma in ten children under five years of age with bile salt export pump deficiency. HEPATOLOGY 2006;44:478-486.
31. Strautnieks SS, Byrne JA, Pawlikowska L, Cebecauerova D, Rayner A, Dutton L, et al. Severe bile salt export pump deficiency: 82 different ABCB11 mutations in 109 families. Gastroenterology 2008;134:1203-1214.
32. Walkowiak J, Jankowska I, Pawlowska J, Strautnieks S, Bull L, Thompson R, et al. Exocrine pancreatic function in children with progressive familial intrahepatic cholestasis type 2. J Pediatr Gastroenterol Nutr 2006;42:416-418.
33. Nobili V, Di Giandomenico S, Francalanci P, Callea F, Marcellini M, Santorelli FM. A new ABCB11 mutation in two Italian children with familial intrahepatic cholestasis. J Gastroenterol 2006;41:598-603.
34. Alvarez L, Jara P, Sanchez-Sabate E, Hierro L, Larrauri J, Diaz MC, et al. Reduced hepatic expression of farnesoid X receptor in hereditary cholestasis associated to mutation in ATP8B1. Hum Mol Genet 2004;13:2451-2460.
35. Scheimann AO, Strautnieks SS, Knisely AS, Byrne JA, Thompson RJ, Finegold MJ. Mutations in bile salt export pump (ABCB11) in two children with progressive familial intrahepatic cholestasis and cholangiocarcinoma. J Pediatr 2007;150:556-559.
36. Liu C, Aronow BJ, Jegga AG, Wang N, Miethke A, Mourya R, et al. Novel resequencing chip customized to diagnose mutations in patients with inherited syndromes of intrahepatic cholestasis. Gastroenterology 2007;132: 119-126.
37. Kubitz R, Keitel V, Scheuring S, Kohrer K, Haussinger D. Benign recurrent intrahepatic cholestasis associated with mutations of the bile salt export pump. J Clin Gastroenterol 2006;40:171-175.
38. Lam CW, Cheung KM, Tsui MS, Yan MS, Lee CY, Tong SF. A patient with novel ABCB11 gene mutations with phenotypic transition between BRIC2 and PFIC2. J Hepatol 2006;44:240-242.
39. Lang C, Meier Y, Stieger B, Beuers U, Lang T, Kerb R, et al. Mutations and polymorphisms in the bile salt export pump and the multidrug resistance protein 3 associated with drug-induced liver injury. Pharmacogenet Genomics 2007;17:47-60.
40. Keitel V, Vogt C, Haussinger D, Kubitz R. Combined mutations of canalicular transporter proteins cause severe intrahepatic cholestasis of pregnancy. Gastroenterology 2006;131:624-629.
41. Meier Y, Zodan T, Lang C, Zimmermann R, Kullak-Ublick GA, Meier PJ, et al. Increased susceptibility for intrahepatic cholestasis of pregnancy and contraceptive-induced cholestasis in carriers of the 1331T>C polymorphism in the bile salt export pump. World J Gastroenterol 2008;14:38-45.
42. Pauli-Magnus C, Lang T, Meier Y, Zodan-Marin T, Jung D, Breymann C, et al. Sequence analysis of bile salt export pump (ABCB11) and multidrug resistance p-glycoprotein 3 (ABCB4, MDR3) in patients with intrahepatic cholestasis of pregnancy. Pharmacogenetics 2004;14:91-102.
43. Pauli-Magnus C, Kerb R, Fattinger K, Lang T, Anwald B, Kullak-Ublick GA, et al. BSEP and MDR3 haplotype structure in healthy caucasians, primary biliary cirrhosis and primary sclerosing cholangitis. HEPATOLOGY 2004;39:779-791.
44. Meier Y, Pauli-Magnus C, Zanger UM, Klein K, Schaeffeler E, Nussler AK, et al. Interindividual variability of canalicular ATP-binding-cassette (ABC)-transporter expression in human liver. HEPATOLOGY 2006;44:62-74.
45. Lang T, Haberl M, Jung D, Drescher A, Schlagenhaufer R, Keil A, et al. Genetic variability, haplotype structures, and ethnic diversity of hepatic transporters MDR3 (ABCB4) and bile salt export pump (ABCB11). Drug Metab Dispos 2006;34:1582-1599.
46. Plass JR, Mol O, Heegsma J, Geuken M, Faber KN, Jansen PL, et al. Farnesoid X receptor and bile salts are involved in transcriptional regulation of the gene encoding the human bile salt export pump. HEPATOLOGY 2002;35:589-596.
47. Fairbrother WG, Yeh RF, Sharp PA, Burge CB. Predictive identification of exonic splicing enhancers in human genes. Science 2002;297:1007-1013.
48. Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR. ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res 2003;31: 3568-3571.
49. Smith PJ, Zhang C, Wang J, Chew SL, Zhang MQ, Krainer AR. An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers. Hum Mol Genet 2006;15:2490-2508.
50. Reese MG. Splice site prediction by neural network. Available at: Http:// fruitfly.org/seq⊤ols/splice.html.
51. Reese MG, Eeckman FH, Kulp D, Haussler D. Improved splice site detection in Genie. J Comput Biol 1997;4:311-323.
52. Burge CB. FAS-ESS web server. Available at: Http://genes.mit.edu/fas-ess.
53. Wang Z, Rolish ME, Yeo G, Tung V, Mawson M, Burge CB. Systematic identification and analysis of exonic splicing silencers. Cell 2004;119:831-845.
54. Brown CR, Hong-Brown LQ, Welch WJ. Correcting temperature-sensitive protein folding defects. J Clin Invest 1997;99:1432-1444.
55. Maitra R, Shaw CM, Stanton BA, Hamilton JW. Increased functional cell surface expression of CFTR and Delta F508-CFTR by the anthracycline doxorubicin. Am J Physiol Cell Physiol 2001;280:C1031-1037.
56. Sato S, Ward CL, Krouse ME, Wine JJ, Kopito RR. Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J Biol Chem 1996;271:635-638.
57. Chen F, Ananthanarayanan M, Emre S, Neimark E, Bull LN, Knisely AS, et al. Progressive familial intrahepatic cholestasis, type 1, is associated with decreased farnesoid X receptor activity. Gastroenterology 2004;126:756-764.
58. Goto K, Sugiyama K, Sugiura T, Ando T, Mizutani F, Terabe K, et al. Bile salt export pump gene mutations in two Japanese patients with progressive familial intrahepatic cholestasis. J Pediatr Gastroenterol Nutr 2003;36: 647-650.
59. Jung C, Driancourt C, Baussan C, Zater M, Hadchouel M, Meunier-Rotival M, et al. Prenatal molecular diagnosis of inherited cholestatic diseases. J Pediatr Gastroenterol Nutr 2007;44:453-458.
60. Plass JR, Mol O, Heegsma J, Geuken M, de Bruin J, Elling G, et al. A progressive familial intrahepatic cholestasis type 2 mutation causes an unstable, temperature-sensitive bile salt export pump. J Hepatol 2004; 40:24-30.
61. Byrne JA, Strautnieks SS, Ihrke G, Knisely AS, Jankowska I, Pawlowska J, et al. Investigation of mRNA splicing associated with the common BSEP mutations: An important disease mechanism for D482G. HEPATOLOGY 2005;42:518A-519A.
62. Nielsen KB, Sorensen S, Cartegni L, Corydon TJ, Doktor TK, Schroeder LD, et al. Seemingly neutral polymorphic variants may confer immunity to splicing-inactivating mutations: A synonymous SNP in exon 5 of MCAD protects from deleterious mutations in a flanking exonic splicing enhancer. Am J Hum Genet 2007;80:416-432.
63. Keene JD. RNA regulons: Coordination of post-transcriptional events. Nat Rev Genet 2007;8:533-543.
64. Frelet A, Klein M. Insight in eukaryotic ABC transporter function by mutation analysis. FEBS Lett 2006;580:1064-1084.
65. Creighton T. Proteins. New York: W.H. Freeman and Company, 1993.
66. Hayashi H, Sugiyama Y. 4-Phenylbutyrate enhances the cell surface expression and the transport capacity of wild-type and mutated bile salt export pumps. HEPATOLOGY 2007;45:1506-1516.
67. De Vree JM, Ottenhoff R, Bosma PJ, Smith AJ, Aten J, Oude Elferink RP. Correction of liver disease by hepatocyte transplantation in a mouse model of progressive familial intrahepatic cholestasis. Gastroenterology 2000; 119:1720-1730.