Ganglioside regulation of AMPA receptor trafficking

Journal of Neuroscience

Volumn 34, Issue 39, 2014, Pages 13246-13258

  Prendergast, Jillian ^a   Umanah, George K E ^a   Yoo, Seung Wan ^a   Lagerlöf, Olof ^a   Motari, Mary G ^a   Cole, Robert N ^a   Huganir, Richard L ^a   Dawson, Ted M ^a   Dawson, Valina L ^a   Schnaar, Ronald L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA receptor; Ganglioside; GluR2; N ethylmaleimide sensitive factor; Nicalin; Thorase

Indexed keywords

ADENOSINE 5' O (3 THIOTRIPHOSPHATE); AMPA RECEPTOR; GANGLIOSIDE; GANGLIOSIDE GD 1A; GANGLIOSIDE GD 1B; GANGLIOSIDE GM1; GANGLIOSIDE GT1B; GLUTAMATE RECEPTOR 2; NICALIN; PEPTIDES AND PROTEINS; SIALIDASE; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; THORASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; ATAD1 PROTEIN, RAT; GANGLIOSIDE GM2; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; PROTEIN BINDING; TRISIALOGANGLIOSIDE GT1;

AMNESIA; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSAY; COIMMUNOPRECIPITATION; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INTELLECTUAL IMPAIRMENT; LEARNING DISORDER; MALE; MASS SPECTROMETRY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEOMICS; PULL DOWN ASSAY; RAT; REGULATORY MECHANISM; SEIZURE; SYNAPSE; THIN LAYER CHROMATOGRAPHY; ANIMAL; CELL CULTURE; CEREBELLUM; CYTOLOGY; METABOLISM; NERVE CELL; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELLS, CULTURED; CEREBELLUM; G(M2) GANGLIOSIDE; GANGLIOSIDES; NEURONS; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS;

EID: 84907292136     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1149-14.2014     Document Type: Article

References (55)

1. Acquotti D, Sonnino S (2000) Use of nuclear magnetic resonance spectroscopy in evaluation of ganglioside structure, conformation, and dynamics. Methods Enzymol 312:247-272. CrossRef Medline
2. Almedom RB, Liewald JF, Hernando G, Schultheis C, Rayes D, Pan J, Schedletzky T, Hutter H, Bouzat C, Gottschalk A (2009) An ER-resident membrane protein complex regulates nicotinic acetylcholine receptor subunit composition at the synapse. EMBO J 28:2636 -2649. CrossRef Medline
3. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22:461- 469. CrossRef Medline
4. Araki Y, Lin DT, Huganir RL (2010) Plasma membrane insertion of the AMPA receptor GluA2 subunit is regulated by NSF binding and Q/R editing of the ion pore. Proc Natl Acad Sci U S A 107:11080 -11085. CrossRef Medline
5. Boccuto L, Aoki K, Flanagan-Steet H, Chen CF, Fan X, Bartel F, Petukh M, Pittman A, Saul R, Chaubey A, Alexov E, Tiemeyer M, Steet R, Schwartz CE (2014) A mutation in a ganglioside biosynthetic enzyme, ST3GAL5, results in salt and pepper syndrome, a neurocutaneous disorder with altered glycolipid and glycoprotein glycosylation. Hum Mol Genet 23: 418-433. CrossRef Medline
6. Boukhris A, Schule R, Loureiro JL, Lourenço CM, Mundwiller E, Gonzalez MA, Charles P, Gauthier J, Rekik I, Acosta Lebrigio RF, Gaussen M, Speziani F, Ferbert A, Feki I, Caballero-Oteyza A, Dionne-Laporte A, Amri M, Noreau A, Forlani S, Cruz VT, et al. (2013) Alteration of ganglioside biosynthesis responsible for complex hereditary spastic paraplegia. Am J Hum Genet 93:118 -123. CrossRef Medline
7. Candelise L, Ciccone A (2002) Gangliosides for acute ischemic stroke. Stroke 33:2336. CrossRef Medline
8. Chen Y, Stevens B, Chang J, Milbrandt J, Barres BA, Hell JW (2008) NS21: re-defined and modified supplement B27 for neuronal cultures. J Neurosci Methods 171:239 -247. CrossRef Medline
9. Cole AA, Dosemeci A, Reese TS (2010) Co-segregation of AMPA receptors with G(M1) ganglioside in synaptosomal membrane subfractions. Biochem J 427:535-540. CrossRef Medline
10. Costa E, Armstrong DM, Guidotti A, Kharlamov A, Kiedrowski L, Manev H, Polo A, Wroblewski JT (1994) Gangliosides in the protection against glutamate excitotoxicity. Prog Brain Res 101:357-373. CrossRef Medline
11. de Erausquin GA, Manev H, Guidotti A, Costa E, Brooker G (1990) Gangliosides normalize distorted single-cell intracellular free Ca2+dynamics after toxic doses of glutamate in cerebellar granule cells. Proc Natl Acad Sci U S A 87:8017- 8021. CrossRef Medline
12. De Marco ML, Woods RJ (2009) Atomic-resolution conformational analysis of the GM3 ganglioside in a lipid bilayer and its implications for ganglioside-protein recognition at membrane surfaces. Glycobiology 19: 344-355. CrossRef Medline
13. Fragaki K, Ait-El-Mkadem S, Chaussenot A, Gire C, Mengual R, Bonesso L, Bénéteau M, Ricci JE, Desquiret-Dumas V, Procaccio V, Rötig A, Paquis- Flucklinger V (2013) Refractory epilepsy and mitochondrial dysfunction due to GM3 synthase deficiency. Eur J Hum Genet 21:528 -534. CrossRef Medline
14. Haffner C, Frauli M, Topp S, Irmler M, Hofmann K, Regula JT, Bally-Cuif L, Haass C (2004) Nicalin and its binding partner Nomo are novel Nodal signaling antagonists. EMBO J 23:3041-3050. CrossRef Medline
15. Hakomori SI (2002) The glycosynapse. Proc Natl Acad Sci U S A 99:225- 232. CrossRef Medline
16. Hanley JG (2014) Subunit-specific trafficking mechanisms regulating the synaptic expression of Ca-permeable AMPA receptors. Semin Cell Dev Biol 27:14 -22. CrossRef Medline
17. Harlalka G, Lehman A, Chioza B, Baple EL, Maroofian R, Cross H, Sreekantan-Nair A, Priestman DA, Al-Turki S, McEntagart ME, Proukakis C, Royle L, Kozak RP, Bastaki L, Patton M, Wagner K, Coblentz R, Price J, Mezei M, Schlade-Bartusiak K, et al. (2013) Mutations in B4GALNT1 (GM2 synthase) underlie a new disorder of ganglioside biosynthesis. Brain 136:3618 -3624. CrossRef Medline
18. Hayashi T, Thomas GM, Huganir RL (2009) Dual palmitoylation of NR2 subunits regulates NMDA receptor trafficking. Neuron 64:213-226. CrossRef Medline
19. Henley JM, Wilkinson KA (2013) AMPAreceptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging. Dialogues Clin Neurosci 15:11-27. Medline
20. Henley JM, Barker EA, Glebov OO (2011) Routes, destinations and delays: recent advances in AMPA receptor trafficking. Trends Neurosci 34:258- 268. CrossRef Medline
21. Herbrich SM, Cole RN, West KP Jr, Schulze K, Yager JD, Groopman JD, Christian P, Wu L, O'Meally RN, May DH, McIntosh MW, Ruczinski I (2013) Statistical inference from multiple iTRAQ experiments without using common reference standards. J Proteome Res 12:594-604. CrossRef Medline
22. Hou Q, Huang Y, Amato S, Snyder SH, Huganir RL, Man HY (2008) Regulation of AMPA receptor localization in lipid rafts. Mol Cell Neurosci 38:213-223. CrossRef Medline
23. Ikarashi K, Fujiwara H, Yamazaki Y, Goto J, Kaneko K, Kato H, Fujii S, Sasaki H, Fukumoto S, Furukawa K, Waki H, Furukawa K (2011) Impaired hippocampal long-term potentiation and failure of learning in beta1,4- N-acetylgalactosaminyltransferase gene transgenic mice. Glycobiology 21:1373-1381. CrossRef Medline
24. Isaac JT, Ashby MC, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859-871. CrossRef Medline
25. Kawai H, Allende ML, Wada R, Kono M, Sango K, Deng C, Miyakawa T, Crawley JN, Werth N, Bierfreund U, Sandhoff K, Proia RL (2001) Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures. J Biol Chem 276:6885- 6888. CrossRef Medline
26. Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340 -350. CrossRef Medline
27. Liu SJ, Savtchouk I (2012) Ca(2+) permeable AMPA receptors switch allegiances: mechanisms and consequences. J Physiol 590:13-20. CrossRef Medline
28. Lopez PH, Schnaar RL (2009) Gangliosides in cell recognition and membrane protein regulation. Curr Opin Struct Biol 19:549 -557. CrossRef Medline
29. Löscher W, Schmidt D (2012) Perampanel-new promise for refractory epilepsy? Nat Rev Neurol 8:661- 662. CrossRef Medline
30. Makuch L, Volk L, Anggono V, Johnson RC, Yu Y, Duning K, Kremerskothen J, Xia J, Takamiya K, Huganir RL (2011) Regulation of AMPA receptor function by the human memory-associated gene KIBRA. Neuron 71: 1022-1029. CrossRef Medline
31. Mehta NR, Lopez PH, Vyas AA, Schnaar RL (2007) Gangliosides and Nogo receptors independently mediate myelin-associated glycoprotein inhibition of neurite outgrowth in different nerve cells. J Biol Chem 282:27875- 27886. CrossRef Medline
32. Moeller A, Zhao C, Fried MG, Wilson-Kubalek EM, Carragher B, Whiteheart SW (2012) Nucleotide-dependent conformational changes in the N-Ethylmaleimide Sensitive Factor (NSF) and their potential role in SNARE complex disassembly. J Struct Biol 177:335-343. CrossRef Medline
33. Mountney A, Zahner MR, Sturgill ER, Riley CJ, Aston JW, Oudega M, Schramm LP, Hurtado A, Schnaar RL (2013) Sialidase, chondroitinase ABC, and combination therapy after spinal cord contusion injury. J Neurotrauma 30:181-190. CrossRef Medline
34. Moustafa I, Connaris H, Taylor M, Zaitsev V, Wilson JC, Kiefel MJ, von Itzstein M, Taylor G (2004) Sialic acid recognition by Vibrio cholerae neuraminidase. J Biol Chem 279:40819-40826. CrossRef Medline
35. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97. CrossRef Medline
36. Ogura T, Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure- diverse function. Genes Cells 6:575-597. CrossRef Medline
37. Opazo P, Choquet D (2011) A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 46:1- 8. CrossRef Medline
38. Pan B, Fromholt SE, Hess EJ, Crawford TO, Griffin JW, Sheikh KA, Schnaar RL (2005) Myelin-associated glycoprotein and complementary axonal ligands, gangliosides, mediate axon stability in the CNS and PNS: neuropathology and behavioral deficits in single- and double-null mice. Exp Neurol 195:208 -217. CrossRef Medline
39. Rogawski MA (2013) AMPA receptors as a molecular target in epilepsy therapy. Acta Neurol Scand Suppl 197:9 -18. CrossRef Medline
40. Schnaar RL, Fromholt SE, Gong Y, Vyas AA, Laroy W, Wayman DM, Heffer- Lauc M, Ito H, Ishida H, Kiso M, Griffin JW, Shiekh KA (2002) Immunoglobulin G-class mouse monoclonal antibodies to major brain gangliosides. Anal Biochem 302:276 -284. CrossRef Medline
41. Schnaar RL, Gerardy-Schahn R, Hildebrandt H (2014) Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease and regeneration. Physiol Rev 94:461-518. CrossRef Medline
42. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613- 643. CrossRef Medline
43. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858. CrossRef Medline
44. Simpson MA, Cross H, Gurtz K, Priestman DA, Neville DC, Reinkensmeier G, Wang H, Wiznitzer M, Proukakis C, Verganelaki A, Pryde A, Patton MA, Dwek RA, Butters TD, Platt FM, Crosby AH (2004) Infantile onset symptomatic epilepsy syndrome caused by homozygous loss of function mutations in GM3 synthase. Nat Genet 36:1225-1229. CrossRef Medline
45. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462: 745-756. CrossRef Medline
46. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318 -324. CrossRef Medline
47. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21: 393-400. CrossRef Medline
48. Sonnino S, Prinetti A (2013) Membrane domains and the "lipid raft" concept. Curr Med Chem 20:4 -21. Medline
49. Sturgill ER, Aoki K, Lopez PH, Colacurcio D, Vajn K, Lorenzini I, Majiæ S, Yang WH, Heffer M, Tiemeyer M, Marth JD, Schnaar RL (2012) Biosynthesis of the major brain gangliosides GD1a and GT1b. Glycobiology 22:1289 -1301. CrossRef Medline
50. Vyas KA, Patel HV, Vyas AA, Schnaar RL (2001) Segregation of gangliosides GM1 and GD3 on cell membranes, isolated membrane rafts, and defined supported lipid monolayers. Biol Chem 382:241-250. Medline
51. Wilkinson PA, Simpson MA, Bastaki L, Patel H, Reed JA, Kalidas K, Samilchuk E, Khan R, Warner TT, Crosby AH (2005) A new locus for autosomal recessive complicated hereditary spastic paraplegia (SPG26) maps to chromosome 12p11.1-12q14. J Med Genet 42:80-82. CrossRef Medline
52. Wu G, Lu ZH, Wang J, Wang Y, Xie X, Meyenhofer MF, Ledeen RW (2005) Enhanced susceptibility to kainate-induced seizures, neuronal apoptosis, and death in mice lacking gangliotetraose gangliosides: protection with LIGA 20, a membrane-permeant analog of GM1. J Neurosci 25:11014- 11022. CrossRef Medline
53. Zhang G, Lehmann HC, Manoharan S, Hashmi M, Shim S, Ming GL, Schnaar RL, Lopez PH, Bogdanova N, Sheikh KA (2011a) Anti-ganglioside antibody-mediated activation of RhoA induces inhibition of neurite outgrowth. J Neurosci 31:1664 -1675. CrossRef Medline
54. Zhang J, Wang Y, Chi Z, Keuss MJ, Pai YM, Kang HC, Shin JH, Bugayenko A, Wang H, Xiong Y, Pletnikov MV, Mattson MP, Dawson TM, Dawson VL (2011b) The AAA+ ATPase Thorase regulates AMPA receptordependent synaptic plasticity and behavior. Cell 145:284 -299. CrossRef Medline
55. Zhao C, Slevin JT, WhiteheartSW (2007) Cellular functions of NSF: not just SNAPs and SNAREs. FEBS Lett 581:2140 -2149. CrossRef Medline