Regulation of the high-affinity choline transporter activity and trafficking by its association with cholesterol-rich lipid rafts

Journal of Neurochemistry

Volumn 128, Issue 5, 2014, Pages 725-740

  Cuddy, Leah K ^a   Winick Ng, Warren ^a   Rylett, Rebecca Jane ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

cholesterol; high affinity choline uptake; lipid rafts; trafficking; transport

Indexed keywords

CARRIER PROTEIN; CELL SURFACE PROTEIN; CHOLESTEROL; CHOLESTEROL OXIDASE; CHOLINE TRANSPORTER PROTEIN; FILIPIN; METHYL BETA CYCLODEXTRIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOTINYLATION; CHOLINE UPTAKE; CHOLINERGIC NERVE; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; FEMALE; FOREBRAIN; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID RAFT; MALE; MEMBRANE DAMAGE; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; YOUNG ADULT;

RATTUS;

CHOLESTEROL; HIGH-AFFINITY CHOLINE UPTAKE; LIPID RAFTS; TRAFFICKING; TRANSPORT;

ANIMALS; BETA-CYCLODEXTRINS; BIOTINYLATION; CELL LINE; CENTRIFUGATION, DENSITY GRADIENT; CHOLESTEROL; CHOLESTEROL OXIDASE; CHOLINE; DATA INTERPRETATION, STATISTICAL; DNA, COMPLEMENTARY; FEMALE; FILIPIN; G(M1) GANGLIOSIDE; HEMICHOLINIUM 3; HUMANS; MALE; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; RATS; SYNAPTOSOMES;

EID: 84896731066     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12490     Document Type: Article

References (77)

1. Ahn K., and, Sampson N. S., (2003) Cholesterol oxidase senses subtle changes in lipid bilayer structure. Biochemistry 43, 827-836.
2. Allen J. A., Halverson-Tamboli R. A., and, Rasenick M. M., (2007) Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 8, 128-140.
3. Apparsundaram S., Ferguson S. M., and, Blakeley R. D., (2001) Molecular cloning and characterization of a murine hemicholinium-3-sensitive choline transporter. Biochem. Soc. Trans. 29, 711-716.
4. Apparsundaram S., Martinez V., Parikh V., Kozak R., and, Sarter M., (2005) Increased capacity and density of choline transporters situated in synaptic membranes of the right medial prefrontal cortex of attentional task-performing rats. J. Neurosci. 25, 3851-3856.
5. Baier C. J., Fantini J., and, Barrantes F. J., (2011) Disclosure of cholesterol recognition motifs in transmembrane domains of the human acetylcholine receptor. Sci. Rep. 1 (69), 1-7.
6. Barrett P. J., Song Y., Van Horn W. D., Hustedt E. J., Schafer J. M., Hadziselimovic A., Beel A. J., and, Sanders C. R., (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336, 1168-1171.
7. Black S. A., and, Rylett R. J., (2012) Choline transporter CHT regulation and function in cholinergic neurons. Cent. Nerv. Syst. Agents Med. Chem. 12, 114-121.
8. Black S. A. G., Ribeiro F. M., Ferguson S. S. G., and, Rylett R. J., (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.
9. Butchbach M. E., Tian G., Guo H., and, Lin C. L., (2004) Association of excitatory amino acid transporters, especially EAAT2, with cholesterol-rich lipid raft microdomains: importance for excitatory amino acid transporter localization and function. J. Biol. Chem. 279, 34388-34396.
10. Cremona M. L., Matthies H. J., Pau K., et al,. (2011) Flotillin-1 is essential for PKC-triggered endocytosis and membrane microdomain localization of DAT. Nat. Neurosci. 14, 469-477.
11. Cuddy L. K., Gordon A. C., Black S. A., Jaworski E., Ferguson S. S. G., and, Rylett R. J., (2012) Peroxynitrite donor SIN-1 alters high-affinity choline transporter activity by modifying its intracellular trafficking. J. Neurosci. 32, 5573-5584.
12. Dale L. B., Seachrist J L., Babwah A. V., and, Ferguson S. S., (2004) Regulation of angiotensin II type 1A receptor internalization, retention, degradation and recycling by Rab5, Rab7, and Rab11 GTPases. J. Biol. Chem. 279, 13110-13118.
13. Di Guglielmo G. M., Le Roy C., Goodfellow A. F., and, Wrana J. L., (2003) Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat. Cell Biol. 5, 410-421.
14. Fantini J., and, Barrantes F. J., (2013) How cholesterol interacts with membrane proteins: exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front. Physiol. 4, 1-9.
15. Ferguson S. M., and, Blakely R. D., (2004) The choline transporter resurfaces: new roles for synaptic vesicles? Mol. Interv. 4, 22-37.
16. Ferguson S. S. G., Rylett R. J., and, Collier B., (1994) Regulation of rat brain synaptosomal [3H]hemicholinium-3 binding and [3H]choline transport sites following exposure to choline mustard aziridinium ion. J. Neurochem. 63, 1328-1337.
17. Ferguson S. M., Savchenko V., Apparsundaram S., Zwick M., Wright J., Heilman C. J., Yi H., Levey A. I., and, Blakely R. D., (2003) Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J. Neurosci. 23, 9697-9709.
18. Foster J. D., Adkins S. D., Lever J. R., and, Vaughan R. A., (2008) Phorbol ester induced trafficking-independent regulation and enhanced phosphorylation of the dopamine transporter associated with membrane rafts and cholesterol. J. Neurochem. 105, 1683-1699.
19. Gates J. J., Ferguson S. M., Blakely R. D., and, 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. Gimpl G., Burger K., and, Fahrenholz F., (1997) Cholesterol as modulator of receptor function. Biochemistry 36, 10959-10974.
21. Haga T., and, Noda H., (1973) Choline uptake systems of rat brain synaptosomes. Biochim. Biophys. Acta 291, 564-575.
22. Head B. P., Patel H. H., and, Insel P. A,. (2013) Interaction of membrane/lipid rafts with the cytoskeleton: impact on signalling and function. Biochim. Biophys. Acta doi: 10.1016/j.bbamem.2013.07.018. [epub ahead of print].
23. Helms J. B., and, Zurzolo C., (2004) Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 5, 247-254.
24. Hicks D. A., Nalivaeva N. N., and, Turner A. J., (2012) Lipid rafts and Alzheimer's disease: protein-lipid interactions and perturbation of signalling. Front. Physiol. 3, 189.
25. Hooper N. M., (1999) Detergent-insoluble glycosphingolipid/cholesterol- rich membrane domains, lipid rafts and caveolae (review). Mol. Membr. Biol. 16, 145-156.
26. Janes P. W., Ley S. C., Magee A. I., and, Kabouridis P. S., (2000) The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin. Immunol. 12, 23-34.
27. Jayanthi L. D., Samuvel D. J., and, Ramamoorthy S., (2004) Regulated internalization and phosphorylation of the native norepinephrine transporter in response to phorbol esters. Evidence for localization in lipid rafts and lipid raft-mediated internalization. J. Biol. Chem. 279, 19315-19326.
28. Jones K. T., Zhen J., and, Reith M. E. A., (2012) Importance of cholesterol in dopamine transporter function. J. Neurochem. 123, 700-715.
29. Kivipelto M., et al,. (2001) Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. BMJ 322, 1447-1451.
30. Kristofiková Z., Kopecký V., Jr, Hofbauerová K., Hovorková P., and, Rípová D., (2008) Complex of amyloid beta peptides with 24-hydroxycholesterol and its effect on hemicholinium-3 sensitive carriers. Neurochem. Res. 33, 412-421.
31. Lajoie P., and, Nabi I. R., (2007) Regulation of raft-dependent endocytosis. J. Cell Mol. Med. 11, 644-653.
32. Lamb M. E., Zhang C., Shea T., Kyle D. J., and, Leeb-Lundberg L. M., (2002) Human B1 and B2 bradykinin receptors and their agonists target caveolae-related lipid rafts to different degrees in HEK293 cells. Biochemistry 41, 14340-14347.
33. Laude A. J., and, Prior I. A., (2004) Plasma membrane microdomains: organization, function and trafficking. Mol. Membr. Biol. 21, 193-205.
34. Ledesma M. D., Abad-Rodriguez J., Galvan C., Biondi E., Navarro P., Delacourte A., Dingwall C., and, Dotti C. G., (2003) Raft disorganization leads to reduced plasmin activity in Alzheimer's disease brains. EMBO J. 4, 1190-1196.
35. Lindwasser O. W., and, Resh M. D., (2001) Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75, 7913-7924.
36. Lingwood D., and, Simons K., (2010) Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
37. Lorenzen A., Samosh J., Vandewark K., Anborgh P. H., Seah C., Magalhaes A. C., Cregan S. P., Ferguson S. S., and, Pasternak S. H., (2010) Rapid and direct transport of cell surface APP to the lysosome defines a novel selective pathway. Mol. Brain 3, 11.
38. Luga V., McLean S., Le Roy C., O'Connor-McCourt M., Wrana J. L., and, Di Guglielmo G. M., (2009) The extracellular domain of the TGFβ type II receptor regulates membrane raft partitioning. Biochem. J. 421, 119-131.
39. Maekawa S., Iino S., and, Miyata S., (2003) Molecular characterization of the detergent-insoluble cholesterol-rich membrane microdomain (raft) of the central nervous system. Biochim. Biophys. Acta 1610, 261-270.
40. Magnani F., Tate C. G., Wynne S., Williams C., and, Haase J., (2004) Partitioning of the serotonin transporter into lipid microdomains modulates transport of serotonin. J. Biol. Chem. 279, 38770-38778.
41. Martin M., Dotti C. G., and, Ledesma M. D., (2010) Brain cholesterol in normal and pathological aging. Biochim. Biophys. Acta 1801, 934-944.
42. McCabe J. B., and, Berthiaume L. G., (1999) Functional roles for fatty acylated amino-terminal domains in subcellular localization. Mol. Biol. Cell 10, 3771-3786.
43. Mcintosh T. J., and, Simon S. A., (2006) Roles of bilayer material properties in function and distribution of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 35, 177-198.
44. Michaely P. A., Mineo C., Ying Y., and, Anderson R. G. W., (1999) Polarized distribution of endogenous Rac1 and RhoA at the cell surface. J. Biol. Chem. 274, 21430-21436.
45. Misawa H., Nakata K., Matsuura J., Nagao M., Okuda T., and, Haga T., (2001) Distribution of the high-affinity choline transporter in the central nervous system of the rat. Neuroscience 105, 87-98.
46. North P., and, Fleischer S., (1983) Alteration of synaptic membrane cholesterol/phospholipid ratio using a lipid transfer protein. J. Biol. Chem. 258, 1242-1253.
47. Okuda T., Haga T., Kanai Y., Endou H., Ishihara T., and, Katsura I., (2000) Identification and characterization of the high-affinity choline transporter. Nat. Neurosci. 3, 120-125.
48. Okuda T., Okamura M., Kaitsuka C., Haga T., and, Gurwitz D,. (2002) Single nucleotide polymorphism of the human high affinity choline transporter alters transport rate. J. Biol. Chem. 277, 45315-45322.
49. Okuda T., Konishi A., Misawa H., and, Haga T., (2011) Substrate-induced internalization of the high-affinity choline transporter. J. Neurosci. 31, 14989-14997.
50. Okuda T., Osawa C., Yamada H., Hayashi K., Nishikawa S., Ushio T., Kubo Y., Satou M., Ogawa H., and, Haga T., (2012) Transmembrane topology and oligomeric structure of the high-affinity choline transporter. J. Biol. Chem. 287, 42826-42834.
51. Pascual J., Fontan A., Zarranz J. J., Berciano J., Florez J., and, Pazos A., (1991) High-affinity choline uptake carrier in Alzheimer's disease: implications for the cholinergic hypothesis of dementia. Brain Res. 552, 179-174.
52. Pike L. J., (2006) Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47, 1597-1598.
53. Pinthong M., Black S. A., Ribeiro F. M., Pholpramool C., Ferguson S. S., and, Rylett R. J., (2008) Activity and subcellular trafficking of the sodium-coupled choline transporter CHT is regulated acutely by peroxynitrite. Mol. Pharmacol. 73, 801-812.
54. Poirier J., Delisle M. C., Quirion R., Aubert I., Farlow M., Lahiri D., et al,. (1995) Apolipoprotein E4 allele as a predictor of cholinergic deficits and treatment outcome in Alzheimer disease. Proc. Natl Acad. Sci. USA 92, 12260-12264.
55. Ribeiro F. M., Alves-Silva J., Volknandt W., et al,. (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.
56. Ribeiro F. M., Black S. A., Cregan S. P., Prado V. F., Prado M. A., Rylett R. J., and, Ferguson S. S., (2005) Constitutive high-affinity choline transporter endocytosis is determined by a carboxyl-terminal tail dileucine motif. J. Neurochem. 94, 86-96.
57. Ribeiro F. M., Black S. A., Prado V. F., Rylett R. J., Ferguson S. S., and, Prado M. A., (2006) The "ins" and "outs" of the high-affinity choline transporter CHT1. J. Neurochem. 97, 1-12.
58. Ribeiro F. M., Pinthong M., Black S. A., Gordon A. C., Prado V. F., Prado M. A., Rylett R. J., and, Ferguson S. S., (2007) Regulated recycling and plasma membrane recruitment of the high-affinity choline transporter. Eur. J. Neurosci. 26, 3437-3448.
59. Rodal S. K., Skretting G., Garred Ø., Vilhardt F., van Deurs B., and, Sandvig K., (1999) Extraction of cholesterol with methyl-β- cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10, 961-974.
60. Rylett R. J., (1986) Choline mustard: an irreversible ligand for use in studies of choline transport mechanisms at the cholinergic nerve terminal. Can. J. Physiol. Pharmacol. 64, 334-340.
61. Rylett R. J., and, Walters S. A., (1990) Uptake and metabolism of [3H]choline mustard by cholinergic nerve terminals from rat brain. Neuroscience 36, 483-489.
62. Rylett R. J., Ball M. J., and, Colhoun E. H., (1983) Evidence for high-affinity choline transport in synaptosomes prepared from hippocampus and neocortex of patients with Alzheimer's disease. Brain Res. 289, 169-175.
63. Saltarelli M. D., Lowenstein P. R., and, Coyle J. T., (1987) Rapid in vitro modulation of [3H]hemicholinium-3 binding sites in rat striatal slices. Eur. J. Pharmacol. 135, 35-40.
64. Samuvel D. J., Jayanthi L. D., Bhat N. R., and, Ramamoorthy S., (2005) A role for p38 mitogen-activated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression. J. Neurosci. 25, 29-41.
65. Scanlon S. M., Williams D. C., and, Schloss P., (2001) Membrane cholesterol modulates serotonin transporter activity. Biochemistry 40, 10507-10513.
66. Shouffani A., and, Kanner B. I., (1990) Cholesterol is required for the reconstruction of the sodium- and chloride-coupled, -aminobutyric acid transporter from rat brain. J. Biol. Chem. 265, 6002-6008.
67. Simons K., and, Ikonen E., (1997) Functional rafts in cell membranes. Nature 387, 569-572.
68. Simons K., and, Toomre D., (2000) Lipid rafts, and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
69. Simons M., Keller P., Dichgans J., and, Schulz J. B., (2001) Cholesterol and Alzheimer's disease: is there a link? Neurology 57, 1089-1093.
70. Slotkin T. A., Nemeroff C. B., Bissette G., and, Seidler F. J., (1994) Overexpression of the high affinity choline transporter in cortical regions affected by Alzheimer's disease. Evidence from rapid autopsy studies. J. Clin. Invest. 94, 696-702.
71. Song K. S, Li S., Okamato T., Quilliam L. A., Sargiacomo M., and, Lisanti M. P., (1996) Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J. Biol. Chem. 271, 9690-9697.
72. Subtil A., Gaidarov I., Kobylarz K., Lampson M. A., Keen J. H., and, McGraw T. E., (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl Acad. Sci. USA 96, 6775-6780.
73. Wang B., Yang L., Wang Z., and, Zheng H., (2007) Amyolid precursor protein mediates presynaptic localization and activity of the high-affinity choline transporter. Proc. Natl Acad. Sci. USA 104, 14140-14145.
74. Waser P. G., Oxterwalder M., and, Schonenberger E., (1978) Autoradiography of 14C-choline uptake in endplates and skeletal muscle of mice. Naunyn Schmiedebergs Arch. Pharmacol. 302, 173-179.
75. Waugh M. G., Lawson D., and, Hsuan J. J., (1999) Epidermal growth factor receptor activation is localized within lowbuoyant density, non-caveolar membrane domains. Biochem. J. 337, 591-597.
76. Yamamura H. I., and, Snyder S. H., (1973) High affinity transport of choline into synaptosomes of rat brain. J. Neurochem. 21, 1355-1374.
77. Zidovetzki R., and, Levitan I., (2007) Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, and control strategies. Biochim. Biophys. Acta 1768, 1311-1324.