Sortilin-Related Receptor SORCS3 Is a Postsynaptic Modulator of Synaptic Depression and Fear Extinction

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Breiderhoff, Tilman ^a   Christiansen, Gitte B ^b   Pallesen, Lone T ^b   Vaegter, Christian ^b   Nykjaer, Anders ^b   Holm, Mai Marie ^b   Glerup, Simon ^b   Willnow, Thomas E ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN SORCS3; RECEPTOR PROTEIN; SORTILIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; FEAR; FEMALE; HIPPOCAMPAL CA1 REGION; IN VIVO STUDY; INTRACELLULAR SIGNALING; LEARNING DISORDER; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY DISORDER; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; POSTSYNAPTIC DENSITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SPATIAL LEARNING;

ANIMALS; BEHAVIOR, ANIMAL; CARRIER PROTEINS; CELL LINE; EVOKED POTENTIALS; EXTINCTION, PSYCHOLOGICAL; FEAR; GENE EXPRESSION; HIPPOCAMPUS; HUMANS; LONG-TERM SYNAPTIC DEPRESSION; MALE; MEMORY; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; NUCLEAR PROTEINS; POST-SYNAPTIC DENSITY; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE;

EID: 84884360159     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075006     Document Type: Article

References (46)

1. Petersen CM, Nielsen MS, Nykjaer A, Jacobsen L, Tommerup N, et al. (1997) Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J Biol Chem 272: 3599-3605. doi:10.1074/jbc.272.6.3599. PubMed: 9013611.
2. Jacobsen L, Madsen P, Moestrup SK, Lund AH, Tommerup N, et al. (1996) Molecular characterization of a novel human hybrid-type receptor that binds the alpha2-macroglobulin receptor-associated protein. J Biol Chem 271: 31379-31383. doi:10.1074/jbc.271.49.31379. PubMed: 8940146.
3. Yamazaki H, Bujo H, Kusunoki J, Seimiya K, Kanaki T, et al. (1996) Elements of neural adhesion molecules and a yeast vacuolar protein sorting receptor are present in a novel mammalian low density lipoprotein receptor family member. J Biol Chem 271: 24761-24768. doi:10.1074/jbc.271.40.24761. PubMed: 8798746.
4. Hampe W, Rezgaoui M, Hermans-Borgmeyer I, Schaller HC, (2001) The genes for the human VPS10 domain-containing receptors are large and contain many small exons. Hum Genet 108: 529-536. doi:10.1007/s004390100504. PubMed: 11499680.
5. Marcusson EG, Horazdovsky BF, Cereghino JL, Gharakhanian E, Emr SD, (1994) The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77: 579-586. doi:10.1016/0092-8674(94)90219-4. PubMed: 8187177.
6. Willnow TE, Petersen CM, Nykjaer A, (2008) VPS10P-domain receptors- regulators of neuronal viability and function. Nat Rev Neurosci 9: 899-909. doi:10.1038/nrg2454. PubMed: 19002190.
7. Nykjaer A, Lee R, Teng KK, Jansen P, Madsen P, et al. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427: 843-848. doi:10.1038/nature02319. PubMed: 14985763.
8. Jansen P, Giehl K, Nyengaard JR, Teng K, Lioubinski O, et al. (2007) Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat Neurosci 10: 1449-1457. doi:10.1038/nn2000. PubMed: 17934455.
9. Vaegter CB, Jansen P, Fjorback AW, Glerup S, Skeldal S, et al. (2011) Sortilin associates with Trk receptors to enhance anterograde transport and neurotrophin signaling. Nat Neurosci 14: 54-61. doi:10.1038/nn.2689. PubMed: 21102451.
10. Teng HK, Teng KK, Lee R, Wright S, Tevar S, et al. (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25: 5455-5463. doi:10.1523/JNEUROSCI.5123-04.2005. PubMed: 15930396.
11. Andersen OM, Reiche J, Schmidt V, Gotthardt M, Spoelgen R, et al. (2005) Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc Natl Acad Sci U S A 102: 13461-13466. doi:10.1073/pnas.0503689102. PubMed: 16174740.
12. Rogaeva E, Meng Y, Lee JH, Gu Y, Kawarai T, et al. (2007) The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat Genet 39: 168-177. doi:10.1038/ng1943. PubMed: 17220890.
13. Offe K, Dodson SE, Shoemaker JT, Fritz JJ, Gearing M, et al. (2006) The lipoprotein receptor LR11 regulates amyloid beta production and amyloid precursor protein traffic in endosomal compartments. J Neurosci 26: 1596-1603. doi:10.1523/JNEUROSCI.4946-05.2006. PubMed: 16452683.
14. Lane RF, Raines SM, Steele JW, Ehrlich ME, Lah JA, et al. (2010) Diabetes-associated SorCS1 regulates Alzheimer's amyloid-beta metabolism: evidence for involvement of SorL1 and the retromer complex. J Neurosci 30: 13110-13115. doi:10.1523/JNEUROSCI.3872-10.2010. PubMed: 20881129.
15. Lane RF, Steele JW, Cai D, Ehrlich ME, Attie AD, et al. (2013) Protein Sorting Motifs in the Cytoplasmic Tail of SorCS1 Control Generation of Alzheimer's Amyloid-beta Peptide. J Neurosci 33: 7099-7107. doi:10.1523/JNEUROSCI.5270-12.2013. PubMed: 23595767.
16. Hermey G, Plath N, Hübner CA, Kuhl D, Schaller HC, et al. (2004) The three sorCS genes are differentially expressed and regulated by synaptic activity. J Neurochem 88: 1470-1476. doi:10.1046/j.1471-4159.2004.02286.x. PubMed: 15009648.
17. Schwenk F, Baron U, Rajewsky K, (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081. doi:10.1093/nar/23.24.5080. PubMed: 8559668.
18. Bliss TV, Lomo T, (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232: 331-356. PubMed: 4727084.
19. Collingridge GL, Isaac JT, Wang YT, (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5: 952-962. doi:10.1038/nrn1556. PubMed: 15550950.
20. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, et al. (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287: 2262-2267. doi:10.1126/science.287.5461.2262. PubMed: 10731148.
21. Dudek SM, Bear MF, (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89: 4363-4367. doi:10.1073/pnas.89.10.4363. PubMed: 1350090.
22. Kemp N, McQueen J, Faulkes S, Bashir ZI, (2000) Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur J Neurosci 12: 360-366. doi:10.1046/j.1460-9568.2000.00903.x. PubMed: 10651891.
23. Zucker RS, Regehr WG, (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405. doi:10.1146/annurev.physiol.64.092501.114547. PubMed: 11826273.
24. Dobrunz LE, Stevens CF, (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008. doi:10.1016/S0896-6273(00)80338-4. PubMed: 9208866.
25. Takahashi T, Kajikawa Y, Tsujimoto T, (1998) G-Protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18: 3138-3146. PubMed: 9547222.
26. Collingridge GL, Peineau S, Howland JG, Wang YT, (2010) Long-term depression in the CNS. Nat Rev Neurosci 11: 459-473. doi:10.1038/nrn2867. PubMed: 20559335.
27. Kim MJ, Futai K, Jo J, Hayashi Y, Cho K, et al. (2007) Synaptic accumulation of PSD-95 and synaptic function regulated by phosphorylation of serine-295 of PSD-95. Neuron 56: 488-502. doi:10.1016/j.neuron.2007.09.007. PubMed: 17988632.
28. Volk L, Kim CH, Takamiya K, Yu Y, Huganir RL, (2010) Developmental regulation of protein interacting with C kinase 1 (PICK1) function in hippocampal synaptic plasticity and learning. Proc Natl Acad Sci U S A 107: 21784-21789. doi:10.1073/pnas.1016103107. PubMed: 21106762.
29. Thorsen TS, Madsen KL, Rebola N, Rathje M, Anggono V, et al. (2010) Identification of a small-molecule inhibitor of the PICK1 PDZ domain that inhibits hippocampal LTP and LTD. Proc Natl Acad Sci U S A 107: 413-418. doi:10.1073/pnas.0902225107. PubMed: 20018661.
30. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, et al. (2008) An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron 57: 872-882. doi:10.1016/j.neuron.2008.01.028. PubMed: 18367088.
31. Hanley JG, (2008) PICK1: a multi-talented modulator of AMPA receptor trafficking. Pharmacol Ther 118: 152-160. doi:10.1016/j.pharmthera.2008.02.002. PubMed: 18353440.
32. Xia J, Zhang X, Staudinger J, Huganir RL, (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22: 179-187. doi:10.1016/S0896-6273(00)80689-3. PubMed: 10027300.
33. Citri A, Bhattacharyya S, Ma C, Morishita W, Fang S, et al. (2010) Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression. J Neurosci 30: 16437-16452. doi:10.1523/JNEUROSCI.4478-10.2010. PubMed: 21147983.
34. Schmidt V, Sporbert A, Rohe M, Reimer T, Rehm A, et al. (2007) SorLA/LR11 regulates processing of amyloid precursor protein via interaction with adaptors GGA and PACS-1. J Biol Chem 282: 32956-32964. doi:10.1074/jbc.M705073200. PubMed: 17855360.
35. Fjorback AW, Seaman M, Gustafsen C, Mehmedbasic A, Gokool S, et al. (2012) Retromer Binds the FANSHY Sorting Motif in SorLA to Regulate Amyloid Precursor Protein Sorting and Processing. J Neurosci 32: 1467-1480. doi:10.1523/JNEUROSCI.2272-11.2012. PubMed: 22279231.
36. Myers KM, Davis M, (2007) Mechanisms of fear extinction. Mol Psychiatry 12: 120-150. doi:10.1038/sj.mp.4001939. PubMed: 17160066.
37. Ge Y, Dong Z, Bagot RC, Howland JG, Phillips AG, et al. (2010) Hippocampal long-term depression is required for the consolidation of spatial memory. Proc Natl Acad Sci U S A 107: 16697-16702. doi:10.1073/pnas.1008200107. PubMed: 20823230.
38. Etkin A, Alarcón JM, Weisberg SP, Touzani K, Huang YY, et al. (2006) A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron 50: 127-143. doi:10.1016/j.neuron.2006.03.013. PubMed: 16600861.
39. Brigman JL, Wright T, Talani G, Prasad-Mulcare S, Jinde S, et al. (2010) Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J Neurosci 30: 4590-4600. doi:10.1523/JNEUROSCI.0640-10.2010. PubMed: 20357110.
40. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, et al. (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284: 1805-1811. doi:10.1126/science.284.5421.1805. PubMed: 10364547.
41. Bannerman DM, Niewoehner B, Lyon L, Romberg C, Schmitt WB, et al. (2008) NMDA receptor subunit NR2A is required for rapidly acquired spatial working memory but not incremental spatial reference memory. J Neurosci 28: 3623-3630. doi:10.1523/JNEUROSCI.3639-07.2008. PubMed: 18385321.
42. Ryu J, Futai K, Feliu M, Weinberg R, Sheng M, (2008) Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J Neurosci 28: 8178-8188. doi:10.1523/JNEUROSCI.1944-08.2008. PubMed: 18701680.
43. Lionel AC, Crosbie J, Barbosa N, Goodale T, Thiruvahindrapuram B, et al. (2011) Rare copy number variation discovery and cross-disorder comparisons identify risk genes for ADHD. Sci Transl Med 3: 95ra75. PubMed: 21832240.
44. Bajor LA, Lai Z, Goodrich DE, Miller CJ, Penfold RB, et al. (2013) Posttraumatic stress disorder, depression, and health-related quality of life in patients with bipolar disorder: review and new data from a multi-site community clinic sample. J Affect Disord 145: 232-239. doi:10.1016/j.jad.2012.08.005. PubMed: 23021820.
45. Xia J, Chung HJ, Wihler C, Huganir RL, Linden DJ, (2000) Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 28: 499-510. doi:10.1016/S0896-6273(00)00128-8. PubMed: 11144359.
46. Steinberg JP, Takamiya K, Shen Y, Xia J, Rubio ME, et al. (2006) Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron 49: 845-860. doi:10.1016/j.neuron.2006.02.025. PubMed: 16543133.