Peroxynitrite donor SIN-1 alters high-affinity choline transporter activity by modifying its intracellular trafficking

Journal of Neuroscience

Volumn 32, Issue 16, 2012, Pages 5573-5585

  Cuddy, Leah K ^a,b   Gordon, Alexis C ^c   Black, Stefanie A G ^d   Jaworski, Ewa ^a,b   Ferguson, Stephen S G ^a,b   Jane Rylett, R ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b WESTERN UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CHOLINE TRANSPORTER; LINSIDOMINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PEROXYNITRITE; PROTEASOME; RAB PROTEIN; RAB5A PROTEIN; RAB7 PROTEIN; RAB9 PROTEIN; UNCLASSIFIED DRUG; CHOLINE; CLATHRIN; DYNAMIN; NEUROTRANSMITTER TRANSPORTER;

ARTICLE; BINDING ASSAY; BIOTINYLATION; CELL MIGRATION; CHOLINE UPTAKE; CHOLINERGIC TRANSMISSION; COATED VESICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOSOME; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; UBIQUITINATION; CELL SURFACE; CHEMICAL STRESS; CHOLINERGIC NERVE; ENDOCYTOSIS; ENZYMATIC DEGRADATION; GENE INACTIVATION; MICROENVIRONMENT; NONHUMAN; OXIDATIVE STRESS;

CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CHOLINE; CLATHRIN; CYSTEINE PROTEINASE INHIBITORS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; ENDOSOMES; HEMICHOLINIUM 3; HUMANS; LEUPEPTINS; LUMINESCENT PROTEINS; LYSOSOMES; MEMBRANE TRANSPORT PROTEINS; MOLSIDOMINE; MUTATION; NEUROBLASTOMA; NITRIC OXIDE; NITRIC OXIDE DONORS; PEROXYNITROUS ACID; PROTEIN TRANSPORT; RAB5 GTP-BINDING PROTEINS; TIME FACTORS; TRANSFECTION; TRITIUM; UBIQUITINATION;

EID: 84859770293     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/jneurosci.5235-11.2012     Document Type: Article

References (47)

1. Alkam T, Nitta A, Mizoguchi H, Itoh A, Nabeshima T (2007) A natural scavenger of peroxynitrites, rosmarinic acid, protects against impairment of memory induced by Abeta(25-35). Behav Brain Res 180:139-145.
2. Apparsundaram S, Ferguson SM, George AL Jr, Blakely RD (2000) Molecular cloning of a human, hemicholinium-3-sensitive choline transporter. Biochem Biophys Res Comm 276:862-867.
3. Ashki N, Hayes KC, Bao F (2008) The peroxynitrite donor 3-morpholinosydnonimine induces reversible changes in electrophysiological properties of neurons of the guinea-pig spinal cord. Neuroscience 156:107-117.
4. Beckman JS (1991) The double-edged role of nitric oxide in brain function and superoxide-mediated injury. J Dev Physiol 15:53-59.
5. Beckman JS (1994) Peroxynitrite versus hydroxyl radical: the role of nitric oxide in superoxide-dependent cerebral injury. Ann N Y Acad Sci 738:69-75.
6. Black SA, Ribeiro FM, Ferguson SS, Rylett RJ (2010) Rapid, transient effects of the protein kinase C activator phorbol 12-myristate 13-acetate on activity and trafficking of the rat high-affinity choline transporter. Neuroscience 167:765-773.
7. Bryan-Lluka LJ, Papacostas MH, Paczkowski FA, Wanstall JC (2004) Nitric oxide donors inhibit 5-hydroxytryptamine (5-HT) uptake by the human 5-HT transporter (SERT). Br J Pharmacol 143:63-70.
8. Chavez JA, Roach WG, Keller SR, Lane WS, Lienhard GE (2008) Inhibition of GLUT4 translocation by Tbc1d1, a Rab GTPase-activating protein abundant in skeletal muscle, is partially relieved by AMP-activated protein kinase activation. J Biol Chem 283:9187-9195.
9. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37-44.
10. Dale LB, Seachrist JL, Babwah AV, Ferguson SS (2004) Regulation of angiotensin II type 1A receptor intracellular retention, degradation, and recycling by Rab5, Rab7, and Rab11 GTPases. J Biol Chem 279:13110-13118.
11. Damke H, Binns DD, Ueda H, Schmid SL, Baba T (2001) Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol Biol Cell 12:2578-2589.
12. Dessy C, Kelly RA, Balligand JL, Feron O (2000) Dynamin mediates caveolar sequestration of muscarinic cholinergic receptors and alteration inNO signaling. EMBO J 19:4272-4280.
13. Di Stasi AM, Mallozzi C, Macchia G, Petrucci TC, Minetti M (1999) Peroxynitrite induces tyrosine nitration and modulates tyrosine phosphorylation of synaptic proteins. J Neurochem 73:727-735.
14. Ferguson SM, Blakely RD (2004) The choline transporter resurfaces: new roles for synaptic vesicles? Mol Interv 4:22-37.
15. Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD (2003) Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci 23:9697-9709.
16. Fernandes R, Hosoya K, Pereira P (2011) Reactive oxygen species downregulate glucose transport system in retinal endothelial cells. AmJ Physiol Cell Physiol 300:C927-C936.
17. Fischer Y, Thomas J, Sevilla L, Muñoz P, Becker C, Holman G, Kozka IJ, Palacín M, Testar X, Kammermeier H, Zorzano A (1997) Insulininduced recruitment of glucose transporter 4 (GLUT4) and GLUT1 in isolated rat cardiac myocytes. Evidence of the existence of different intracellular GLUT4 vesicle populations. J Biol Chem 272:7085-7092.
18. Ford MG, Pearse BM, Higgins MK, Vallis Y, Owen DJ, Gibson A, Hopkins CR, Evans PR, McMahon HT (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291:1051-1055.
19. Gates J Jr, Ferguson SM, Blakely RD, Apparsundaram S (2004) Regulation of choline transporter surface expression and phosphorylation by protein kinase C and protein phosphatase 1/2A. J Pharmacol Exp Ther 310:536-545.
20. Giros B, el Mestikawy S, Bertrand L, Caron MG (1991) Cloning and functional characterization of a cocaine-sensitive dopamine transporter. FEBS Lett 295:149-154.
21. Guermonprez L, Ducrocq C, Gaudry-Talarmain YM (2001) Inhibition of acetylcholine synthesis and tyrosine nitration induced by peroxynitrite are differentially prevented by antioxidants. Mol Pharmacol 60:838-846.
22. Haga T, Noda H (1973) Choline uptake systems of rat brain synaptosomes. Biochim Biophys Acta 291:564-575.
23. Horie T, Ono K, Nagao K, Nishi H, Kinoshita M, Kawamura T, Wada H, Shimatsu A, Kita T, Hasegawa K (2008) Oxidative stress induces GLUT4 translocation by activation of PI3-K/Akt and dual AMPK kinase in cardiac myocytes. J Cell Physiol 215:733-742.
24. Kaye DM, Wiviott SD, Kobzik L, Kelly RA, Smith TW (1997) S-Nitrosothiols inhibit neuronal norepinephrine transport. Am J Physiol 272:H875-H883.
25. Li X, De Sarno P, Song L, Beckman JS, Jope RS (1998) Peroxynitrite modulates tyrosine phosphorylation and phosphoinositide signalling in human neuroblastoma SH-SY5Y cells: attenuated effects in human 1321N1 astrocytoma cells. Biochem J 331:599-606.
26. Lorenzen A, Samosh J, Vandewark K, Anborgh PH, Seah C, Magalhaes AC, Cregan SP, Ferguson SS, Pasternak SH (2010) Rapid and direct transport of cell surface APP to the lysosome defines a novel selective pathway. Mol Brain 3:11.
27. Martín de Llano JJ, Fuertes G, Andreu EJ, Puig O, Chaves FJ, Soutar AK, Armengod ME, Knecht E (2006) A single point mutation in the lowdensity lipoprotein receptor switches the degradation of its mature protein from the proteasome to the lysosome. Int J Biochem Cell Biol 38:1340-1351.
28. Oh-Hashi K, Maruyama W, Isobe K (2001) Peroxynitrite induces GADD34, 45, and 153 VIA p38MAPKin human neuroblastoma SH-SY5Y cells. Free Radic Biol Med 30:213-221.
29. Okuda T, Haga T (2000) Functional characterization of the human highaffinity choline transporter. FEBS Lett 484:92-97.
30. Okuda T, Haga T, Kanai Y, Endou H, Ishihara T, Katsura I (2000) Identification and characterization of the high-affinity choline transporter. Nat Neurosci 3:120-125.
31. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424.
32. Park SU, Ferrer JV, Javitch JA, Kuhn DM (2002) Peroxynitrite inactivates the human dopamine transporter by modification of cysteine 342: potential mechanism of neurotoxicity in dopamine neurons. J Neurosci 22:4399-4405.
33. Pinthong M, Black SA, Ribeiro FM, Pholpramool C, Ferguson SS, Rylett RJ (2008) Activity and subcellular trafficking of the sodium-coupled choline transporter CHT is regulated acutely by peroxynitrite. Mol Pharmacol 73:801-812.
34. Ramamoorthy S, Bauman AL, Moore KR, Han H, Yang-Feng T, Chang AS, Ganapathy V, Blakely RD (1993) Antidepressant-and cocaine-sensitive human serotonin transporter: molecular cloning, expression, and chromosomal localization. Proc Natl Acad Sci U S A 90:2542-2546.
35. Ribeiro FM, Alves-Silva J, Volknandt W, Martins-Silva C, Mahmud H, Wilhelm A, Gomez MV, Rylett RJ, Ferguson SS, Prado VF, Prado MA (2003) The hemicholinium-3 sensitive high affinity choline transporter is internalized by clathrin-mediated endocytosis and is present in endosomes and synaptic vesicles. J Neurochem 87:136-146.
36. Ribeiro FM, Black SA, Cregan SP, Prado VF, Prado MA, Rylett RJ, Ferguson SS (2005) Constitutive high-affinity choline transporter endocytosis is determined by a carboxyl-terminal tail dileucine motif. J Neurochem 94:86-96.
37. Ribeiro FM, Black SA, Prado VF, Rylett RJ, Ferguson SS, Prado MA (2006) The "ins" and "outs" of the high-affinity choline transporter CHT1. J Neurochem 97:1-12.
38. Ribeiro FM, Pinthong M, Black SA, Gordon AC, Prado VF, Prado MA, Rylett RJ, Ferguson SS (2007) Regulated recycling and plasma membrane recruitment of the high-affinity choline transporter. Eur J Neurosci 26:3437-3448.
39. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G (1997) Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 17:2653-2657.
40. Vanlandingham PA, Ceresa BP (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284:12110-12124.
41. Wakabayashi K, Nakagawa H, Tamura A, Koshiba S, Hoshijima K, Komada M, Ishikawa T (2007) Intramolecular disulfide bond is a critical check point determining degradative fates of ATP-binding cassette (ABC) transporter ABCG2 protein. J Biol Chem 282:27841-27846.
42. Wang B, Yang L, Wang Z, Zheng H (2007) Amyolid precursor protein mediates presynaptic localization and activity of the high-affinity choline transporter. Proc Natl Acad Sci U S A 104:14140-14145.
43. Wang G, Moniri NH, Ozawa K, Stamler JS, Daaka Y (2006) Nitric oxide regulates endocytosis by S-nitrosylation of dynamin. Proc Natl Acad Sci U S A 103:1295-1300.
44. Wang X, Michaelis EK (2010) Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2:12.
45. Whitehead RE, Ferrer JV, Javitch JA, Justice JB (2001) Reaction of oxidized dopamine with endogenous cysteine residues in the human dopamine transporter. J Neurochem 76:1242-1251.
46. Xu J, Kim GM, Chen S, Yan P, Ahmed SH, Ku G, Beckman JS, Xu XM, Hsu CY (2001) iNOS and nitrotyrosine expression after spinal cord injury. J Neurotrauma 18:523-532.
47. Yamamura HI, Snyder SH (1973) High affinity transport of choline into synaptosomes of rat brain. J Neurochem 21:1355-1374.