Calnexin-Assisted Biogenesis of the Neuronal Glycine Transporter 2 (GlyT2)

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Arribas González, Esther ^a,c   Alonso Torres, Pablo ^a   Aragón, Carmen ^a,b,c   López Corcuera, Beatriz ^a,b,c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXYNOJIRIMYCIN; CALNEXIN; CASTANOSPERMINE; GLYCAN; GLYCINE; GLYCINE TRANSPORTER 2; SMALL INTERFERING RNA; TUNICAMYCIN; GLUCOSIDASE; GLYCINE TRANSPORTER; MANNOSIDASE; PROTEIN BINDING; SLC6A5 PROTEIN, RAT; THAPSIGARGIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HYPEREKPLEXIA; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RAT; WILD TYPE; AMINO ACID SUBSTITUTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; DRUG EFFECTS; GENETICS; GLYCOSYLATION; KINETICS; METABOLISM; MOUSE; PROTEIN DEGRADATION; PROTEIN PROCESSING; UNFOLDED PROTEIN RESPONSE;

AMINO ACID SUBSTITUTION; ANIMALS; CALNEXIN; CERCOPITHECUS AETHIOPS; COS CELLS; GLUCOSIDASES; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; GLYCOSYLATION; KINETICS; MANNOSIDASES; MICE; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RATS; THAPSIGARGIN; TUNICAMYCIN; UNFOLDED PROTEIN RESPONSE;

EID: 84877034319     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063230     Document Type: Article

References (52)

1. Lynch JW, (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 84 (4): 1051-1095.
2. Legendre P, (2001) The glycinergic inhibitory synapse. Cell Mol Life Sci 58 (5-6): 760-793.
3. Harvey RJ, Depner UB, Wassle H, Ahmadi S, Heindl C, et al. (2004) GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 304 (5672): 884-887.
4. Aragón C, López-Corcuera B, (2003) Structure, function and regulation of glycine neurotransporters. Eur J Pharmacol 479 (1-3): 249-262.
5. Gomeza J, Hulsmann S, Ohno K, Eulenburg V, Szoke K, et al. (2003) Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron 40 (4): 785-796.
6. Gomeza J, Ohno K, Hulsmann S, Armsen W, Eulenburg V, et al. (2003) Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 40 (4): 797-806.
7. Aragón C, López-Corcuera B, (2005) Glycine transporters: crucial roles of pharmacological interest revealed by gene deletion. Trends Pharmacol Sci 26 (6): 283-286.
8. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM, (1997) Identification and characterization of the vesicular GABA transporter. Nature 389 (6653): 870-876.
9. Rousseau F, Aubrey KR, Supplisson S, (2008) The glycine transporter GlyT2 controls the dynamics of synaptic vesicle refilling in inhibitory spinal cord neurons. J Neurosci 28 (39): 9755-9768.
10. Suhren O, Bruyn G, Tynman J, (1966) Hyperekplexia. A hereditary startle syndrome. J Neurol Sci 3: 577-605.
11. Chung SK, Vanbellinghen JF, Mullins JG, Robinson A, Hantke J, et al. (2010) Pathophysiological mechanisms of dominant and recessive GLRA1 mutations in hyperekplexia. J Neurosci 30 (28): 9612-9620.
12. Harvey RJ, Topf M, Harvey K, Rees MI, (2008) The genetics of hyperekplexia: more than startle! Trends Genet 24. (9): 439-447.
13. Pérez-Siles G, Morreale A, Leo-Macias A, Pita G, Ortiz AR, et al. (2011) Molecular basis of the differential interaction with lithium of glycine transporters GLYT1 and GLYT2. J Neurochem 118 (2): 195-204.
14. Pérez-Siles G, Núñez E, Morreale A, Jiménez E, Leo-Macías A, et al. (2012) An aspartate residue in the external vestibule of GLYT2 (glycine transporter 2) controls cation access and transport coupling. Biochem J 442 (2): 323-334.
15. Yamashita A, Singh SK, Kawate T, Jin Y, Gouaux E, (2005) Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437 (7056): 215-223.
16. Rees MI, Harvey K, Pearce BR, Chung SK, Duguid IC, et al. (2006) Mutations in the gene encoding GlyT2 (SLC6A5) define a presynaptic component of human startle disease. Nat Genet 38 (7): 801-806.
17. Eulenburg V, Becker K, Gomeza J, Schmitt B, Becker CM, et al. (2006) Mutations within the human GLYT2 (SLC6A5) gene associated with hyperekplexia. Biochem Biophys Res Commun 348 (2): 400-405.
18. Giménez C, Pérez-Siles G, Martinez-Villarreal J, Arribas-González E, Jiménez E, et al. (2012) A Novel Dominant Hyperekplexia Mutation Y705C Alters Trafficking and Biochemical Properties of the Presynaptic Glycine Transporter GlyT2. J Biol Chem 287 (34): 28986-29002.
19. Carta E, Chung SK, James VM, Robinson A, Gill JL, et al. (2012) Mutations in the GlyT2 Gene (SLC6A5) Are a Second Major Cause of Startle Disease. J Biol Chem 287 (34): 28975-28985.
20. Núñez E, Pérez-Siles G, Rodenstein L, Alonso-Torres P, Zafra F, et al. (2009) Subcellular localization of the neuronal glycine transporter GLYT2 in brainstem. Traffic 10 (7): 829-843.
21. de Juan-Sanz J, Zafra F, López-Corcuera B, Aragón C, (2011) Endocytosis of the neuronal glycine transporter GLYT2 is clathrin and ubiquitin mediated from different cell surface subdomains. Traffic 12: 1850-1867.
22. Núñez E, Alonso-Torres P, Fornés A, Aragón C, López-Corcuera B, (2008) The neuronal glycine transporter GLYT2 associates with membrane rafts: functional modulation by lipid environment. J Neurochem 105: 2080-2090.
23. Walter P, Johnson AE, (1994) Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu Rev Cell Biol 10: 87-119.
24. Hebert DN, Molinari M, (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev 87 (4): 1377-1408.
25. Parodi AJ, (2000) Protein glucosylation and its role in protein folding. Annu Rev Biochem 69: 69-93.
26. Schrag JD, Bergeron JJ, Li Y, Borisova S, Hahn M, et al. (2001) The Structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell 8 (3): 633-644.
27. Brockmeier A, Williams DB, (2006) Potent lectin-independent chaperone function of calnexin under conditions prevalent within the lumen of the endoplasmic reticulum. Biochemistry 45 (42): 12906-12916.
28. Lederkremer GZ, (2009) Glycoprotein folding, quality control and ER-associated degradation. Curr Opin Struct Biol 19 (5): 515-523.
29. Martinez-Maza R, Poyatos I, López-Corcuera B, Núñez E, Giménez C, et al. (2001) The role of N-glycosylation in transport to the plasma membrane and sorting of the neuronal glycine transporter GLYT2. J Biol Chem 276 (3): 2168-2173.
30. Bartholomaus I, Milan-Lobo L, Nicke A, Dutertre S, Hastrup H, et al. (2008) Glycine transporter dimers: evidence for occurrence in the plasma membrane. J Biol Chem 283 (16): 10978-10991.
31. López-Corcuera B, Núñez E, Martínez-Maza R, Geerlings A, Aragón C, (2001) Substrate-induced conformational changes of extracellular loop 1 in the glycine transporter GLYT2. J Biol Chem 276 (46): 43463-43470.
32. Jiménez E, Zafra F, Pérez-Sen R, Delicado EG, Miras-Portugal MT, et al. (2011) P2Y purinergic regulation of the glycine neurotransmitter transporters. J Biol Chem 286 10712-10724.
33. Zafra F, Gomeza J, Olivares L, Aragón C, Giménez C, (1995) Regional distribution and developmental variation of the glycine transporters GLYT1 and GLYT2 in the rat CNS. Eur J Neurosci 7 (6): 1342-1352.
34. López-Corcuera B, Martínez-Maza R, Núñez E, Roux M, Supplisson S, et al. (1998) Differential properties of two stably expressed brain-specific glycine transporters. J Neurochem 71 (5): 2211-2219.
35. Freeze H, Hak C (2010) Endoglycosidase and Glycoamidase Release of N-Linked Glycans. Current Protocols in Immunology. Wiley Interscience. John Wiley & Sons, Inc.
36. Rutkevich LA, Williams DB, (2011) Participation of lectin chaperones and thiol oxidoreductases in protein folding within the endoplasmic reticulum. Curr Opin Cell Biol 23 (2): 157-166.
37. Deprez P, Gautschi M, Helenius A, (2005) More than one glycan is needed for ER glucosidase II to allow entry of glycoproteins into the calnexin/calreticulin cycle. Mol Cell 19 (2): 183-195.
38. Compain P, Martin OR (2007) Iminosugars: From synthesis to therapeutic applications. John Wiley and Sons Ltd, Chichester, West Sussex, England.
39. Korkhov VM, Milan-Lobo L, Zuber B, Farhan H, Schmid JA, et al. (2008) Peptide-based interactions with calnexin target misassembled membrane proteins into endoplasmic reticulum-derived multilamellar bodies. J Mol Biol 378 (2): 337-352.
40. Kaufman RJ, (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13 (10): 1211-1233.
41. Morello JP, Salahpour A, Petaja-Repo UE, Laperriere A, Lonergan M, et al. (2001) Association of calnexin with wild type and mutant AVPR2 that causes nephrogenic diabetes insipidus. Biochemistry 40 (23): 6766-6775.
42. Esapa CT, McIlhinney RA, Blake DJ, (2005) Fukutin-related protein mutations that cause congenital muscular dystrophy result in ER-retention of the mutant protein in cultured cells. Hum Mol Genet 14 (2): 295-305.
43. Molinari M, Calanca V, Galli C, Lucca P, Paganetti P, (2003) Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299 (5611): 1397-1400.
44. Yan W, Frank CL, Korth MJ, Sopher BL, Novoa I, et al. (2002) Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci U S A 99 (25): 15920-15925.
45. Olivares L, Aragón C, Giménez C, Zafra F, (1994) Carboxyl terminus of the glycine transporter GLYT1 is necessary for correct processing of the protein. J Biol Chem 269 (45): 28400-28404.
46. Denzel A, Molinari M, Trigueros C, Martin JE, Velmurgan S, et al. (2002) Early postnatal death and motor disorders in mice congenitally deficient in calnexin expression. Mol Cell Biol 22 (21): 7398-7404.
47. Tate CG, Whiteley E, Betenbaugh MJ, (1999) Molecular chaperones improve functional expression of the serotonin (5-hydroxytryptamine) transporter in insect cells. Biochem Soc Trans 27 (6): 932-936.
48. Kaushal GP, Pastuszak I, Hatanaka K, Elbein AD, (1990) Purification to homogeneity and properties of glucosidase II from mung bean seedlings and suspension-cultured soybean cells. J Biol Chem 265 (27): 16271-16279.
49. Elbein AD, Tropea JE, Mitchell M, Kaushal GP, (1990) Kifunensine, a potent inhibitor of the glycoprotein processing mannosidase I. J Biol Chem 265. (26): 15599-15605.
50. Hammond C, Braakman I, Helenius A, (1994) Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Natl Acad Sci U S A 91 (3): 913-917.
51. Solda T, Galli C, Kaufman RJ, Molinari M, (2007) Substrate-specific requirements for UGT1-dependent release from calnexin. Mol Cell 27 (2): 238-249.
52. Glozman R, Okiyoneda T, Mulvihill CM, Rini JM, Barriere H, et al. (2009) N-glycans are direct determinants of CFTR folding and stability in secretory and endocytic membrane traffic. J Cell Biol 184 (6): 847-862.