The equilibrative nucleoside transporter (ENT1) can be phosphorylated at multiple sites by PKC and PKA

Molecular Membrane Biology

Volumn 28, Issue 6, 2011, Pages 412-426

  Reyes, German ^a   Nivillac, Nicole M I ^a   Karim, Muhammad Zia ^a,b   Desouza, Leroi ^a   Siu, K W Michael ^a,b   Coe, Imogen R ^a  

^a YORK UNIVERSITY   (Canada)

^b Department of Chemistry ^*  (Canada)

Author keywords

ENT1; Kinase; Phosphorylation; PKA; PKC; Regulation

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; HISTIDINE; PHOSPHOAMINO ACID; PROTEIN KINASE C; SERINE; THREONINE; UBIQUITIN;

ARTICLE; CONTROLLED STUDY; ENZYME ASSAY; MASS SPECTROMETRY; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SEQUENCE ALIGNMENT;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; PHOSPHORYLATION; PROTEIN KINASE C;

MAMMALIA;

EID: 80051999615     PISSN: 09687688     EISSN: 14645203     Source Type: Journal    
DOI: 10.3109/09687688.2011.604861     Document Type: Article

References (40)

1. Butt SJ, Pitman RM. 2005. Indirect phosphorylation-dependent modulation of postsynaptic nicotinic acetylcholine responses by 5-hydroxytryptamine. Eur J Neurosci 21:1181-1188. (Pubitemid 40516616)
2. Cervinski MA, Foster JD, Vaughan RA. 2010. Syntaxin 1A regulates dopamine transporter activity, phosphorylation and surface expression. Neuroscience 170:408-416.
3. Ciarimboli G, Schlatter E. 2005. Regulation of organic cation transport. Pflugers Arch 449:423-441. (Pubitemid 40238877)
4. Coe IR, Yao L, Diamond I, Gordon AS. 1996. The role of protein kinase C in cellular tolerance to ethanol. J Biol Chem 271:29468-29472. (Pubitemid 26382667)
5. Coe I, Zhang Y, McKenzie T, Naydenova Z. 2002. PKC regulation of the human equilibrative nucleoside transporter, hENT1. FEBS Lett 517:201-205. (Pubitemid 34327659)
6. Fernández Calotti P, Galmarini CM, Cañones C, Gamberale R, Saénz D, Avalos JS, Chianelli M, Rosenstein R, Giordano M. 2008. Modulation of the human equilibrative nucleoside transporter1 (hENT1) activity by IL-4 and PMA in B cells from chronic lymphocytic leukemia. Biochem Pharmacol 75:857-865.
7. Foster JD, Pananusorn B, Vaughan RA. 2002. Dopamine transporters are phosphorylated on N-terminal serines in rat stria-tum. J Biol Chem 277:25178-25186. (Pubitemid 34951824)
8. Galmarini CM, Clarke ML, Falette N, Puisieux A, Mackey JR, Dumontet C. 2002. Expression of a non-functional p53 affects the sensitivity of cancer cells to gemcitabine. Int J Cancer 97:439-445. (Pubitemid 34027801)
9. Gorentla BK, Moritz AE, Foster JD, Vaughan RA. 2009. Proline-directed phosphorylation of the dopamine transporter N-terminal domain. Biochemistry 48:1067-1076.
10. Griffiths M, Yao SY, Abidi F, Phillips SE, Cass CE, Young JD, Baldwin SA. 1997. Molecular cloning and characterization of a nitrobenzylthioinosine- insensitive (ei) equilibrative nucleoside transporter from human placenta. Biochem J 15:739-743. (Pubitemid 28005769)
11. Grimard V, Li C, Ramjeesingh M, Bear CE, Goormaghtigh E, Ruysschaert JM. 2004. Phosphorylation-induced conforma-tional changes of cystic fibrosis transmembrane conductance regulator monitored by attenuated total reflection-Fourier transform IR spectroscopy and fluorescence spectroscopy. J Biol Chem 279:5528-5536. (Pubitemid 38220578)
12. Grimsrud PA, Swaney DL, Wenger CD, Beauchene NA, Coon JJ. 2010. Phosphoproteomics for the masses. ACS Chem Biol 5:105-119.
13. Gunawardena J. 2005. Multisite protein phosphorylation makes a good threshold but can be a poor switch. Proc Natl Acad Sci USA 102:14617-14622. (Pubitemid 41457106)
14. Hou J, Xie Z, Xue P, Cui Z, Chen X, Li J, Cai T, Wu P, Yang F. 2010. Enhanced MALDI-TOF MS analysis of phos-phopeptides using an optimized DHAP/DAHC matrix. J Biomed Biotechnol 2010:759690.
15. Jayanthi LD, Samuvel DJ, Blakely RD, Ramamoorthy S. 2005. Evidence for biphasic effects of protein kinase C on serotonin transporter function, endocytosis, and phosphorylation. Mol Pharmacol 67:2077-2087. (Pubitemid 41007790)
16. Jayanthi LD, Annamalai B, Samuvel DJ, Gether U, Ramamoorthy S. 2006. Phosphorylation of the norepinephrine transporter at threonine 258 and serine 259 is linked to protein kinase C-mediated transporter internalization. J Biol Chem 281:23326-23340. (Pubitemid 44274107)
17. Khoshbouei H, Sen N, Guptaroy B, Johnson L, Lund D, Gnegy ME, Galli A, Javitch JA. 2004. N-terminal phosphory-lation of the dopamine transporter is required for amphetamine-induced efflux. PLoS Biol 2:E78.
18. King AE, Ackley MA, Cass CE, Young JD, Baldwin SA. 2006. Nucleoside transporters: From scavengers to novel therapeutic targets. Trends Pharmacol Sci 27:416-425. (Pubitemid 44051567)
19. Lee EW, Lai Y, Zhang H, Unadkat JD. 2006. Identification of the mitochondrial targeting signal of the human equilibrative nucle-oside transporter 1 (hENT1): Implications for interspecies differences in mitochondrial toxicity of fialuridine. J Biol Chem 281:6700-6706.
20. López-Corcuera B, Aragón C, Geerlings A. 2001. Regulation of glycine transporters. Biochem Soc Trans 29:742-745. (Pubitemid 33131773)
21. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, Jensen PR, Mann M. 2007. The serine/threonine/tyrosine phosphopro-teome of the model bacterium Bacillus subtilis. Mol Cell Prote-omics 6:697-707. (Pubitemid 46630102)
22. Mittag T, Kay LE, Forman-Kay JD. 2010. Protein dynamics and conformational disorder in molecular recognition. J Mol Recog-nit 23:105-116.
23. Mohapatra DP, Park KS, Trimmer JS. 2007. Dynamic regulation of the voltage-gated Kv2.1 potassium channel by multisite phos-phorylation. Biochem Soc Trans 35:1064-1068. (Pubitemid 350206430)
24. Nivillac NM, Wasal K, Villani DF, Naydenova Z, Hanna WJ, Coe IR. 2009. Disrupted plasma membrane localization and loss of function reveal regions of human equilibrative nucleoside transporter 1 involved in structural integrity and activity. Bio-chim Biophys Acta 1788:2326-2334.
25. Procino G, Carmosino M, Marin O, Brunati AM, Contri A, Pinna LA, Mannucci R, Nielsen S, Kwon TH, Svelto M, Valenti G. 2003. Ser-256 phosphorylation dynamics of Aqua-porin 2 during maturation from the ER to the vesicular compartment in renal cells. FASEB J 17:1886-1888.
26. Reyes G, Chalsev M, Nivillac NMI, Coe IR. 2011. Analysis of recombinant tagged equilibrative nucleoside transporter 1 (ENT1) expressed in E. coli. Biochem Cell Biol 89:246-255.
27. Robillard KR, Bone DB, Park JS, Hammond JR. 2008. Characterization of mENT1Delta11, a novel alternative splice variant of the mouse equilibrative nucleoside transporter 1. Mol Pharmacol 74:264-273. (Pubitemid 351872177)
28. Salazar C, Höfer T. 2009. Multisite protein phosphorylation-from molecular mechanisms to kinetic models. FEBS J 276:3177-3198.
29. Saxena SK, Kaur S. 2006. Regulation of epithelial ion channels by Rab GTPases. Biochem Biophy Res Commun 351:582-587. (Pubitemid 44708867)
30. Sen RP, Delicado EG, Alvarez A, Brocklebank AM, Wiley JS, Miras-Portugal MT. 1998. Flow cytometric studies of nucleo-side transport regulation in single chromaffin cells. FEBS Lett 422:368-372. (Pubitemid 28075497)
31. SenGupta DJ, Lum PY, Lai Y, Shubochkina E, Bakken AH, Schneider G, Unadkat JD. 2002. A single glycine mutation in the equilibrative nucleoside transporter gene, hENT1, alters nucleoside transport activity and sensitivity to nitrobenzylthioi-nosine. Biochemistry 41:1512-1519. (Pubitemid 34112740)
32. SenGupta DJ, Unadkat JD. 2004. Glycine 154 of the equilibrative nucleoside transporter, hENT1, is important for nucleoside transport and for conferring sensitivity to the inhibitors nitro-benzylthioinosine, dipyridamole, and dilazep. Biochem Pharmacol 67:453-458. (Pubitemid 38232885)
33. Seo J, Lee KJ. 2004. Post-translational modifications and their biological functions: Proteomic analysis and systematic approaches. J Biochem Mol Biol 37:35-44. (Pubitemid 38402572)
34. Stolk M, Cooper E, Vilk G, Litchfield DW, Hammond JR. 2005. Subtype-specific regulation of equilibrative nucleoside transporters by protein kinase CK2. Biochem J 386:281-289. (Pubitemid 40343785)
35. Sundaram M, Yao SY, Ingram JC, Berry ZA, Abidi F, Cass CE, Baldwin SA, Young JD. 2001. Topology of a human equilibrative, nitrobenzylthioinosine (NBMPR)-sensitive nucleoside transporter (hENT1) implicated in the cellular uptake of adenosine and anti-cancer drugs. J Biol Chem 276:45270-45275.
36. Torres GE. 2006. The dopamine transporter proteome. J Neurochem 97:3-10.
37. van Balkom BW, Savelkoul PJ, Markovich D, Hofman E, Nielsen S, van der Sluijs P, Deen PM. 2002. The role of putative phos-phorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277:41473-41479. (Pubitemid 35257449)
38. Wang JQ, Liu X, Zhang G, Parelkar NK, Arora A, Haines M, Fibuch EE, Mao L. 2006. Phosphorylation of glutamate receptors: A potential mechanism for the regulation of receptor function and psychostimulant action. J Neurosci Res 84:1621-1629. (Pubitemid 44892597)
39. Weinman EJ, Steplock D, Zhang Y, Biswas R, Bloch RJ, Shenolikar S. 2010. Cooperativity between the phosphorylation of Thr95 and Ser77 of NHERF-1 in the hormonal regulation of renal phosphate transport. J Biol Chem 285: 25134-25138.
40. Young JD, Yao SY, Sun L, Cass CE, Baldwin SA. 2008. Human equilibrative nucleoside transporter (ENT) family of nucleoside and nucleobase transporter proteins. Xenobiotica 38: 995-1021.