Crucial role for phylogenetically conserved cytoplasmic loop 3 in ABCC4 protein expression

Journal of Biological Chemistry

Volumn 288, Issue 31, 2013, Pages 22207-22218

  Cheepala, Satish B ^a   Bao, Ju ^a   Nachagari, Deepa ^a   Sun, Daxi ^a   Wang, Yao ^a   Zhong, Tao ^b   Naren, Anjaparavanda P ^c   Zheng, Jie ^a   Schuetz, John D ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; CYTOPLASMIC LOOPS; HELICAL DOMAINS; MEMBRANE LOCALIZATION; PROTEIN EXPRESSIONS;

AMINO ACIDS;

CELL MEMBRANES;

ABC TRANSPORTER; ATP BINDING CASSETTE PROTEIN C4; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; METHIONINE; TRIFLUOROETHANOL; UNCLASSIFIED DRUG;

ABCC4 GENE; ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CIRCULAR DICHROISM; CONTROLLED STUDY; GENE; GENETIC CONSERVATION; MOLECULAR DYNAMICS; MOLECULAR MODEL; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; THERMOSTABILITY;

ABC TRANSPORTER; CYTOPLASMIC LOOP 3; HOMOLOGY MODELING; MOLECULAR MODELING; MRP4; MULTIDRUG TRANSPORTERS; ZEBRAFISH;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CYTOPLASM; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NIH 3T3 CELLS; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH;

EID: 84881225182     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.476218     Document Type: Article

References (44)

1. Kool, M., de Haas, M., Scheffer, G. L., Scheper, R. J., van Eijk, M. J., Juijn, J. A., Baas, F., and Borst, P. (1997) Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 57, 3537-3547
2. Schuetz, J. D., Connelly, M. C., Sun, D., Paibir, S. G., Flynn, P. M., Srinivas, R. V., Kumar, A., and Fridland, A. (1999) MRP4: A previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat. Med. 5, 1048-1051
3. Barber, R., Ray, K. P., and Butcher, R. W. (1980) Turnover of adenosine 3', 5'-monophosphate in WI-38 cultured fibroblasts. Biochemistry 19, 2560-2567
4. Brunton, L. L., and Buss, J. E. (1980) Export of cyclic AMP by mammalian reticulocytes. J. Cyclic Nucleotide Res. 6, 369-377
5. Cheepala, S., Hulot, J. S., Morgan, J. A., Sassi, Y., Zhang, W., Naren, A. P., and Schuetz, J. D. (2013) Cyclic nucleotide compartmentalization: contributions of phosphodiesterases and ATP-binding cassette transporters. Annu. Rev. Pharmacol. Toxicol. 53, 231-253
6. Kruh, G. D., Belinsky, M. G., Gallo, J. M., and Lee, K. (2007) Physiological and pharmacological functions of Mrp2, Mrp3, and Mrp4 as determined from recent studies on gene-disrupted mice. Cancer Metastasis Rev. 26, 5-14
7. Wielinga, P. R., Reid, G., Challa, E. E., van der Heijden, I., van Deemter, L., de Haas, M., Mol, C., Kuil, A. J., Groeneveld, E., Schuetz, J. D., Brouwer, C., De Abreu, R. A., Wijnholds, J., Beijnen, J. H., and Borst, P. (2002) Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol. Pharmacol. 62, 1321-1331
8. Krishnamurthy, P., Schwab, M., Takenaka, K., Nachagari, D., Morgan, J., Leslie, M., Du, W., Boyd, K., Cheok, M., Nakauchi, H., Marzolini, C., Kim, R. B., Poonkuzhali, B., Schuetz, E., Evans, W., Relling, M., and Schuetz, J. D. (2008) Transporter-mediated protection against thiopurine-induced hematopoietic toxicity. Cancer Res. 68, 4983-4989
9. Ban, H., Andoh, A., Imaeda, H., Kobori, A., Bamba, S., Tsujikawa, T., Sasaki, M., Saito, Y., and Fujiyama, Y. (2010) The multidrug-resistance protein 4 polymorphism is a new factor accounting for thiopurine sensitivity in Japanese patients with inflammatory bowel disease. J. Gastroenterol. 45, 1014-1021
10. Abla, N., Chinn, L. W., Nakamura, T., Liu, L., Huang, C. C., Johns, S. J., Kawamoto, M., Stryke, D., Taylor, T. R., Ferrin, T. E., Giacomini, K. M., and Kroetz, D. L. (2008) The human multidrug resistance protein 4 (MRP4, ABCC4): functional analysis of a highly polymorphic gene. J. Pharmacol. Exp. Ther. 325, 859-868
11. Janke, D., Mehralivand, S., Strand, D., Gödtel-Armbrust, U., Habermeier, A., Gradhand, U., Fischer, C., Toliat, M. R., Fritz, P., Zanger, U. M., Schwab, M., Fromm, M. F., Nürnberg, P., Wojnowski, L., Closs, E. I., and Lang, T. (2008) 6-Mercaptopurine and 9-(2-phosphonyl-methoxyethyl) adenine (PMEA) transport altered by two missense mutations in the drug transporter gene ABCC4. Hum. Mutat. 29, 659-669
12. Borst, P., de Wolf, C., and van de Wetering, K. (2007) Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch. 453, 661-673
13. Deeley, R. G., Westlake, C., and Cole, S. P. (2006) Transmembrane transport of endo-and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 86, 849-899
14. Sauna, Z. E., Nandigama, K., and Ambudkar, S. V. (2004) Multidrug resistance protein 4 (ABCC4)-mediated ATP hydrolysis: effect of transport substrates and characterization of the post-hydrolysis transition state. J. Biol. Chem. 279, 48855-48864
15. He, L., Aleksandrov, L. A., Cui, L., Jensen, T. J., Nesbitt, K. L., and Riordan, J. R. (2010) Restoration of domain folding and interdomain assembly by second-site suppressors of the ΔF508 mutation in CFTR. FASEB J. 24, 3103-3112
16. He, L., Aleksandrov, A. A., Serohijos, A. W., Hegedus, T., Aleksandrov, L. A., Cui, L., Dokholyan, N. V., and Riordan, J. R. (2008) Multiple membrane-cytoplasmic domain contacts in the cystic fibrosis transmembrane conductance regulator (CFTR) mediate regulation of channel gating. J. Biol. Chem. 283, 26383-26390
17. Serohijos, A. W., Hegedus, T., Aleksandrov, A. A., He, L., Cui, L., Dokholyan, N. V., and Riordan, J. R. (2008) Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function. Proc. Natl. Acad. Sci. U.S.A. 105, 3256-3261
18. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
19. Fukuda, Y., Aguilar-Bryan, L., Vaxillaire, M., Dechaume, A., Wang, Y., Dean, M., Moitra, K., Bryan, J., and Schuetz, J. D. (2011) Conserved intramolecular disulfide bond is critical to trafficking and fate of ATP-binding cassette (ABC) transporters ABCB6 and sulfonylurea receptor 1 (SUR1)/ABCC8. J. Biol. Chem. 286, 8481-8492
20. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185
21. Jacobson, M. P., Pincus, D. L., Rapp, C. S., Day, T. J., Honig, B., Shaw, D. E., and Friesner, R. A. (2004)Ahierarchical approach to all-atom protein loop prediction. Proteins 55, 351-367
22. Jacobson, M. P., Friesner, R. A., Xiang, Z., and Honig, B. (2002) On the role of crystal packing forces in determining protein sidechain conformations. J. Mol. Biol. 320, 597-608
23. Banasavadi-Siddegowda, Y. K., Mai, J., Fan, Y., Bhattacharya, S., Giovannucci, D. R., Sanchez, E. R., Fischer, G., and Wang, X. (2011) FKBP38 peptidylprolyl isomerase promotes the folding of cystic fibrosis transmembrane conductance regulator in the endoplasmic reticulum. J. Biol. Chem. 286, 43071-43080
24. El Hiani, Y., and Linsdell, P. (2012) Role of the juxtamembrane region of cytoplasmic loop 3 in the gating and conductance of the cystic fibrosis transmembrane conductance regulator chloride channel. Biochemistry 51, 3971-3981
25. Unneberg, P., Merelo, J. J., Chacón, P., and Morán, F. (2001) SOMCD: method for evaluating protein secondary structure from UV circular dichroism spectra. Proteins 42, 460-470
26. Seibert, F. S., Linsdell, P., Loo, T. W., Hanrahan, J. W., Riordan, J. R., and Clarke, D. M. (1996) Cytoplasmic loop three of cystic fibrosis transmembrane conductance regulator contributes to regulation of chloride channel activity. J. Biol. Chem. 271, 27493-27499
27. Seibert, F. S., Linsdell, P., Loo, T. W., Hanrahan, J. W., Clarke, D. M., and Riordan, J. R. (1996) Disease-associated mutations in the fourth cytoplasmic loop of cystic fibrosis transmembrane conductance regulator compromise biosynthetic processing and chloride channel activity. J. Biol. Chem. 271, 15139-15145
28. Rosenberg, M. F., O'Ryan, L. P., Hughes, G., Zhao, Z., Aleksandrov, L. A., Riordan, J. R., and Ford, R. C. (2011) The cystic fibrosis transmembrane conductance regulator (CFTR): three-dimensional structure and localization of a channel gate. J. Biol. Chem. 286, 42647-42654
29. Hayashi, H., and Sugiyama, Y. (2007) 4-Phenylbutyrate enhances the cell surface expression and the transport capacity of wild type and mutated bile salt export pumps. Hepatology 45, 1506-1516
30. Loo, T. W., Bartlett, M. C., Detty, M. R., and Clarke, D. M. (2012) The ATPase activity of the P-glycoprotein drug pump is highly activated when the N-terminal and central regions of the nucleotide-binding domains are linked closely together. J. Biol. Chem. 287, 26806-26816
31. Seeger, M. A., and van Veen, H. W. (2009) Molecular basis of multidrug transport by ABC transporters. Biochim. Biophys. Acta 1794, 725-737
32. Ravna, A. W., and Sager, G. (2008) Molecular model of the outward facing state of the human multidrug resistance protein 4 (MRP4/ABCC4). Bioorg. Med. Chem. Lett. 18, 3481-3483
33. Ravna, A. W., and Sager, G. (2009) Molecular modeling studies of ABC transporters involved in multidrug resistance. Mini. Rev. Med. Chem. 9, 186-193
34. Ravna, A. W., Sylte, I., and Sager, G. (2008) A molecular model of a putative substrate releasing conformation of multidrug resistance protein 5 (MRP5). Eur. J. Med. Chem. 43, 2557-2567
35. Hazai, E., and Bikádi, Z. (2008) Homology modeling of breast cancer resistance protein (ABCG2). J. Struct. Biol. 162, 63-74
36. Kanki, K., Kawamura, T., and Watanabe, Y. (2009) Control of ER stress by a chemical chaperone counteracts apoptotic signals in IFN-γ-treated murine hepatocytes. Apoptosis 14, 309-319
37. Chang, C., and Swaan, P. W. (2006) Computational approaches to modeling drug transporters. Eur. J. Pharm. Sci. 27, 411-424
38. Vardy, E., Arkin, I. T., Gottschalk, K. E., Kaback, H. R., and Schuldiner, S. (2004) Structural conservation in the major facilitator superfamily as revealed by comparative modeling. Protein Sci. 13, 1832-1840
39. Walters, R. F., and DeGrado, W. F. (2006) Helix-packing motifs in membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 103, 13658-13663
40. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415
41. Bartoszewski, R. A., Jablonsky, M., Bartoszewska, S., Stevenson, L., Dai, Q., Kappes, J., Collawn, J. F., and Bebok, Z. (2010) A synonymous single nucleotide polymorphism in ΔF508 CFTR alters the secondary structure of the mRNA and the expression of the mutant protein. J. Biol. Chem. 285, 28741-28748
42. Bertolucci, C. M., Guibao, C. D., and Zheng, J. (2005) Structural features of the focal adhesion kinase-paxillin complex give insight into the dynamics of focal adhesion assembly. Protein Sci. 14, 644-652
43. Jordan, I. K., Kota, K. C., Cui, G., Thompson, C. H., and McCarty, N. A. (2008) Evolutionary and functional divergence between the cystic fibrosis transmembrane conductance regulator and related ATP-binding cassette transporters. Proc. Natl. Acad. Sci. U.S.A. 105, 18865-18870
44. Claustres, M., Laussel, M., Desgeorges, M., Giansily, M., Culard, J. F., Razakatsara, G., and Demaille, J. (1993) Analysis of the 27 exons and flanking regions of the cystic fibrosis gene: 40 different mutations account for 91.2% of the mutant alleles in southern France. Hum. Mol. Genet. 2, 1209-1213