RCNT2 extracellular cysteines, Cys615 and Cys649, are important for maturation and sorting to the plasma membrane

FEBS Letters

Volumn 588, Issue 23, 2014, Pages 4382-4389

  Pinilla Macua, Itziar ^a,b   Claudio Montero, Ana ^a   Pastor Anglada, Marçal ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

CNT2; Cysteine; Plasma membrane; Sorting

Indexed keywords

CONCENTRATIVE NUCLEOSIDE TRANSPORTER 2; CYSTEINE; GLYCOSIDASE; GLYCOSIDASE I; GLYCOSIDASE II; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CIF NUCLEOSIDE TRANSPORTER; REDUCING AGENT; SIGNAL PEPTIDE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ENZYME INHIBITION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PROTEIN TERTIARY STRUCTURE; RAT;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETULUS; CYSTEINE; ENDOPLASMIC RETICULUM; EXTRACELLULAR SPACE; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; REDUCING AGENTS;

EID: 84910625940     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.10.006     Document Type: Article

References (46)

1. M.U. Mondelli The multifaceted functions of ribavirin: antiviral, immunomodulator or both? Hepatology 2014
2. K.M. King, V.L. Damaraju, M.F. Vickers, S.Y. Yao, T. Lang, and T.E. Tackaberry A comparison of the transportability, and its role in cytotoxicity, of clofarabine, cladribine, and fludarabine by recombinant human nucleoside transporters produced in three model expression systems Mol. Pharmacol. 69 2006 346 353
3. M. Rau, F. Stickel, S. Russmann, C. Manser, P. Becker, and M. Weisskopf Impact of genetic SLC28 transporter and ITPA variants on ribavirin serum level, hemoglobin drop and therapeutic response in patients with HCV infection J. Hepatol. 2012
4. A. D'Avolio, A. Ciancio, M. Siccardi, A. Smedile, M. Simiele, and J. Cusato Negative predictive value of IL28B, SLC28A2, and CYP27B1 SNPs and low RBV plasma exposure for therapeutic response to PEG/IFN-RBV treatment Ther. Drug Monit. 34 2012 722 728
5. L. Li, C.M. Tan, S.H. Koo, K.T. Chong, and E.J. Lee Identification and functional analysis of variants in the human concentrative nucleoside transporter 2, hCNT2 (SLC28A2) in Chinese, Malays and Indians Pharmacogenet. Genomics 17 2007 783 786
6. L. Li, S.H. Koo, I.H. Hong, and E.J. Lee Identification of functional promoter haplotypes of human concentrative nucleoside transporter 2, hCNT2 (SLC28A2) Drug Metab. Pharmacokinet. 24 2009 161 166
7. L.M. Mangravite, I. Badagnani, and K.M. Giacomini Nucleoside transporters in the disposition and targeting of nucleoside analogs in the kidney Eur. J. Pharmacol. 479 2003 269 281
8. Y. Lai, A.H. Bakken, and J.D. Unadkat Simultaneous expression of hCNT1-CFP and hENT1-YFP in Madin-Darby canine kidney cells. Localization and vectorial transport studies J. Biol. Chem. 277 2002 37711 37717
9. E. Errasti-Murugarren, M. Pastor-Anglada, and F.J. Casado Role of Cnt3 in the transepithelial flux of nucleosides and nucleoside-derived drugs J. Physiol. 2007
10. S. Duflot, M. Calvo, F.J. Casado, C. Enrich, and M. Pastor-Anglada Concentrative nucleoside transporter (rCNT1) is targeted to the apical membrane through the hepatic transcytotic pathway Exp. Cell Res. 281 2002 77 85
11. R. Govindarajan, C.J. Endres, D. Whittington, E. LeCluyse, M. Pastor-Anglada, and C.M. Tse Expression and hepatobiliary transport characteristics of the concentrative and equilibrative nucleoside transporters in sandwich-cultured human hepatocytes Am. J. Physiol. Gastrointest. Liver Physiol. 295 2008 G570 G580
12. C. Soler, J. Garcia-Manteiga, R. Valdes, J. Xaus, M. Comalada, and F.J. Casado Macrophages require different nucleoside transport systems for proliferation and activation FASEB J. 15 2001 1979 1988
13. C. Soler, R. Valdes, J. Garcia-Manteiga, J. Xaus, M. Comalada, and F.J. Casado Lipopolysaccharide-induced apoptosis of macrophages determines the up-regulation of concentrative nucleoside transporters Cnt1 and Cnt2 through tumor necrosis factor-alpha-dependent and -independent mechanisms J. Biol. Chem. 276 2001 30043 30049
14. R. Valdes, M.A. Ortega, F.J. Casado, A. Felipe, A. Gil, and A. Sanchez-Pozo Nutritional regulation of nucleoside transporter expression in rat small intestine Gastroenterology 119 2000 1623 1630
15. S. Duflot, B. Riera, S. Fernandez-Veledo, V. Casado, R.I. Norman, and F.J. Casado ATP-sensitive K(+) channels regulate the concentrative adenosine transporter CNT2 following activation by A(1) adenosine receptors Mol. Cell. Biol. 24 2004 2710 2719
16. L. Medina-Pulido, M. Molina-Arcas, C. Justicia, E. Soriano, F. Burgaya, and A.M. Planas Hypoxia and P1 receptor activation regulate the high-affinity concentrative adenosine transporter CNT2 in differentiated neuronal PC12 cells Biochem. J. 454 2013 437 445
17. S. Rodriguez-Mulero, E. Errasti-Murugarren, J. Ballarin, A. Felipe, A. Doucet, and F.J. Casado Expression of concentrative nucleoside transporters SLC28 (CNT1, CNT2, and CNT3) along the rat nephron: effect of diabetes Kidney Int. 68 2005 665 672
18. H. Vitzthum, B. Weiss, W. Bachleitner, B.K. Kramer, and A. Kurtz Gene expression of adenosine receptors along the nephron Kidney Int. 65 2004 1180 1190
19. I. Aymerich, F. Foufelle, P. Ferre, F.J. Casado, and M. Pastor-Anglada Extracellular adenosine activates AMP-dependent protein kinase (AMPK) J. Cell Sci. 119 2006 1612 1621
20. I. Huber-Ruano, I. Pinilla-Macua, G. Torres, F.J. Casado, and M. Pastor-Anglada Link between high-affinity adenosine concentrative nucleoside transporter-2 (CNT2) and energy metabolism in intestinal and liver parenchymal cells J. Cell. Physiol. 2010
21. I. Pinilla-Macua, F.J. Casado, and M. Pastor-Anglada Structural determinants for rCNT2 sorting to the plasma membrane of polarized and non-polarized cells Biochem. J. 442 2012 517 525
22. R.S. Hegde, and S.W. Kang The concept of translocational regulation J. Cell Biol. 182 2008 225 232
23. R. Zimmermann, S. Eyrisch, M. Ahmad, and V. Helms Protein translocation across the ER membrane Biochim. Biophys. Acta 1808 2011 912 924
24. L. Ellgaard, and A. Helenius Quality control in the endoplasmic reticulum Nat. Rev. Mol. Cell Biol. 4 2003 181 191
25. L.A. Rutkevich, and D.B. Williams Participation of lectin chaperones and thiol oxidoreductases in protein folding within the endoplasmic reticulum Curr. Opin. Cell Biol. 23 2011 157 166
26. T. Shibatani, L.L. David, A.L. McCormack, K. Frueh, and W.R. Skach Proteomic analysis of mammalian oligosaccharyltransferase reveals multiple subcomplexes that contain Sec61, TRAP, and two potential new subunits Biochemistry 44 2005 5982 5992
27. C. Ruiz-Canada, D.J. Kelleher, and R. Gilmore Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms Cell 136 2009 272 283
28. D.B. Williams Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum J. Cell Sci. 119 2006 615 623
29. J.D. Oliver, H.L. Roderick, D.H. Llewellyn, and S. High ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin Mol. Biol. Cell 10 1999 2573 2582
30. N. Hosokawa, Y. Kamiya, and K. Kato The role of MRH domain-containing lectins in ERAD Glycobiology 20 2010 651 660
31. M. Molinari N-glycan structure dictates extension of protein folding or onset of disposal Nat. Chem. Biol. 3 2007 313 320
32. G.Z. Lederkremer Glycoprotein folding, quality control and ER-associated degradation Curr. Opin. Struct. Biol. 19 2009 515 523
33. L.M. Mangravite, and K.M. Giacomini Sorting of rat SPNT in renal epithelium is independent of N-glycosylation Pharm. Res. 20 2003 319 323
34. B. del Santo, R. Valdes, J. Mata, A. Felipe, F.J. Casado, and M. Pastor-Anglada Differential expression and regulation of nucleoside transport systems in rat liver parenchymal and hepatoma cells Hepatology 28 1998 1504 1511
35. M.D. Slugoski, K.M. Smith, R. Mulinta, A.M. Ng, S.Y. Yao, and E.L. Morrison A conformationally mobile cysteine residue (Cys-561) modulates Na+ and H+ activation of human CNT3 J. Biol. Chem. 283 2008 24922 24934
36. M.D. Slugoski, A.M. Ng, S.Y. Yao, K.M. Smith, C.C. Lin, and J. Zhang A proton-mediated conformational shift identifies a mobile pore-lining cysteine residue (Cys-561) in human concentrative nucleoside transporter 3 J. Biol. Chem. 283 2008 8496 8507
37. L. Qin, S.P. Tam, and R.G. Deeley Effect of multiple cysteine substitutions on the functionality of human multidrug resistance protein 1 expressed in human embryonic kidney 293 cells: identification of residues essential for function Drug Metab. Dispos. 40 2012 1403 1413
38. K. Tanaka, F. Zhou, K. Kuze, and G. You Cysteine residues in the organic anion transporter mOAT1 Biochem. J. 380 2004 283 287
39. T. Keller, B. Egenberger, V. Gorboulev, F. Bernhard, Z. Uzelac, and D. Gorbunov The large extracellular loop of organic cation transporter 1 influences substrate affinity and is pivotal for oligomerization J. Biol. Chem. 286 2011 37874 37886
40. S. Brast, A. Grabner, S. Sucic, H.H. Sitte, E. Hermann, and H. Pavenstadt The cysteines of the extracellular loop are crucial for trafficking of human organic cation transporter 2 to the plasma membrane and are involved in oligomerization FASEB J. 26 2012 976 986
41. E. Hanggi, A.F. Grundschober, S. Leuthold, P.J. Meier, and M.V. St-Pierre Functional analysis of the extracellular cysteine residues in the human organic anion transporting polypeptide, OATP2B1 Mol. Pharmacol. 70 2006 806 817
42. M. Jindrichova, P. Kuzyk, S. Li, S.S. Stojilkovic, and H. Zemkova Conserved ectodomain cysteines are essential for rat P2X7 receptor trafficking Purinergic Signal. 8 2012 317 325
43. Z.L. Johnson, C.G. Cheong, and S.Y. Lee Crystal structure of a concentrative nucleoside transporter from Vibrio cholerae at 2.4 A Nature 483 2012 489 493
44. E. Tokhtaeva, G. Sachs, and O. Vagin Diverse pathways for maturation of the Na, K-ATPase beta1 and beta2 subunits in the endoplasmic reticulum of Madin-Darby canine kidney cells J. Biol. Chem. 285 2010 39289 39302
45. U.G. Danilczyk, and D.B. Williams The lectin chaperone calnexin utilizes polypeptide-based interactions to associate with many of its substrates in vivo J. Biol. Chem. 276 2001 25532 25540
46. N. Dickerhof, T. Kleffmann, R. Jack, and S. McCormick Bacitracin inhibits the reductive activity of protein disulfide isomerase by disulfide bond formation with free cysteines in the substrate-binding domain FEBS J. 2011