Low-density lipoprotein receptor-related protein 1 (LRP1) regulates the stability and function of GluA1 α-amino-3-hydroxy-5-methyl-4-isoxazole propionicacid (AMPA) receptor in neurons

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Gan, Ming ^a   Jiang, Peizhou ^a   McLean, Pamela ^a   Kanekiyo, Takahisa ^a   Bu, Guojun ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b XIAMEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE A1; GLUTAMIC ACID; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; UNCLASSIFIED DRUG; CALCIUM; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; LOW DENSITY LIPOPROTEIN RECEPTOR; LRP1 PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; FILOPODIUM; GENE SILENCING; IN VITRO STUDY; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS REGULATION; SYNAPTIC TRANSMISSION; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; ENZYME STABILITY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; NERVE CELL; NEURITE; PHOSPHORYLATION; PSEUDOPODIUM;

MUS;

ANIMALS; CALCIUM; CELLS, CULTURED; ENZYME STABILITY; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; NEURITES; NEURONS; PHOSPHORYLATION; PSEUDOPODIA; RECEPTORS, AMPA; RECEPTORS, LDL; TUMOR SUPPRESSOR PROTEINS;

EID: 84917735709     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113237     Document Type: Article

References (68)

1. Herz J, Strickland DK (2001) LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108: 779-784.
2. Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 10: 333-344.
3. Mantuano E, Lam MS, Gonias SL (2013) LRP1 assembles unique co-receptor systems to initiate cell signaling in response to tissue-type plasminogen activator and myelin-associated glycoprotein. The Journal of biological chemistry 288: 34009-34018.
4. Li YH, van Kerkhof P, Marzolo MP, Strous GJ, Bu CJ (2001) Identification of a major cyclic AMPdependent protein kinase A phosphorylation site within the cytoplasmic tail of the low-density lipoprotein receptor-related protein: Implication for receptor-mediated endocytosis. Molecular and Cellular Biology 21: 1185-1195.
5. Betts GN, van der Geer P, Komives EA (2008) Structural and functional consequences of tyrosine phosphorylation in the LRP1 cytoplasmic domain. The Journal of biological chemistry 283: 15656-15664.
6. Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J (2003) LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300: 329-332.
7. Liu Q, Zhang J, Zerbinatti C, Zhan Y, Kolber BJ, et al. (2011) Lipoprotein receptor LRP1 regulates leptin signaling and energy homeostasis in the adult central nervous system. PLoS Biol 9: e1000575.
8. May P, Rohlmann A, Bock HH, Zurhove K, Marth JD, et al. (2004) Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice. Mol Cell Biol 24: 8872-8883.
9. Bu G, Maksymovitch EA, Nerbonne JM, Schwartz AL (1994) Expression and function of the low density lipoprotein receptor-related protein (LRP) in mammalian central neurons. J Biol Chem 269: 18521-18528.
10. Liu Q, Trotter J, Zhang J, Peters MM, Cheng H, et al. (2010) Neuronal LRP1 knockout in adult mice leads to impaired brain lipid metabolism and progressive, age-dependent synapse loss and neurodegeneration. J Neurosci 30: 17068-17078.
11. Kanekiyo T, Zhang J, Liu Q, Liu CC, Zhang L, et al. (2011) Heparan sulphate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-beta uptake. J Neurosci 31: 1644-1651.
12. Kanekiyo T, Cirrito JR, Liu CC, Shinohara M, Li J, et al. (2013) Neuronal Clearance of Amyloid-beta by Endocytic Receptor LRP1. J Neurosci 33: 19276-19283.
13. Martin AM, Kuhlmann C, Trossbach S, Jaeger S, Waldron E, et al. (2008) The functional role of the second NPXY motif of the LRP1 beta-chain in tissue-type plasminogen activator-mediated activation of N-methyl-D-aspartate receptors. J Biol Chem 283: 12004-12013.
14. May P, Reddy YK, Herz J (2002) Proteolytic processing of low density lipoprotein receptor-related protein mediates regulated release of its intracellular domain. J Biol Chem 277: 18736-18743.
15. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, et al. (2003) Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 112: 1533-1540.
16. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17: 31-108.
17. Mayer ML, Armstrong N (2004) Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66: 161-181.
18. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405: 955-959.
19. Huganir RL, Nicoll RA (2013) AMPARs and synaptic plasticity: the last 25 years. Neuron 80: 704-717.
20. Chen W, Prithviraj R, Mahnke AH, McGloin KE, Tan JW, et al. (2009) AMPA glutamate receptor subunits 1 and 2 regulate dendrite complexity and spine motility in neurons of the developing neocortex. Neuroscience 159: 172-182.
21. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, et al. (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6: 136-143.
22. Boudreau AC, Wolf ME (2005) Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. The Journal of neuroscience: the official journal of the Society for Neuroscience 25: 9144-9151.
23. Zhang C, Marek GJ (2008) AMPA receptor involvement in 5-hydroxytryptamine2A receptor-mediated pre-frontal cortical excitatory synaptic currents and DOI-induced head shakes. Progress in neuropsychopharmacology & biological psychiatry 32: 62-71.
24. Man HY, Sekine-Aizawa Y, Huganir RL (2007) Regulation of {alpha}-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proceedings of the National Academy of Sciences of the United States of America 104: 3579-3584.
25. Gendron TF, Brunette E, Mealing GA, Nguyen A, Tauskela JS, et al. (2004) Opposing effects of cyclooxygenase-2 selective inhibitors on oxygen-glucose deprivation-induced neurotoxicity. Eur J Pharmacol 493: 45-55.
26. Lin CH, Lee EH (2012) JNK1 inhibits GluR1 expression and GluR1-mediated calcium influx through phosphorylation and stabilization of Hes-1. The Journal of neuroscience: the official journal of the Society for Neuroscience 32: 1826-1846.
27. Coutinho-Budd J, Ghukasyan V, Zylka MJ, Polleux F (2012) The F-BAR domains from srGAP1, srGAP2 and srGAP3 regulate membrane deformation differently. Journal of cell science 125: 3390-3401.
28. Bats C, Groc L, Choquet D (2007) The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53: 719-734.
29. Farfan P, Lee J, Larios J, Sotelo P, Bu G, et al. (2013) A sorting nexin 17-binding domain within the LRP1 cytoplasmic tail mediates receptor recycling through the basolateral sorting endosome. Traffic 14: 823-838.
30. Kawata K, Kubota S, Eguchi T, Aoyama E, Moritani NH, et al. (2012) Role of LRP1 in transport of CCN2 protein in chondrocytes. Journal of cell science 125: 2965-2972.
31. Laatsch A, Panteli M, Sornsakrin M, Hoffzimmer B, Grewal T, et al. (2012) Low density lipoprotein receptor-related protein 1 dependent endosomal trapping and recycling of apolipoprotein E. PloS one 7: e29385.
32. Fu AK, Hung KW, Fu WY, Shen C, Chen Y, et al. (2011) APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nature neuroscience 14: 181-189.
33. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28: 511-525.
34. Wang Q, Charych EI, Pulito VL, Lee JB, Graziane NM, et al. (2011) The psychiatric disease risk factors DISC1 and TNIK interact to regulate synapse composition and function. Molecular psychiatry 16: 1006-1023.
35. Lee HK, Takamiya K, Han JS, Man H, Kim CH, et al. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112: 631-643.
36. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, et al. (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51: 213-225.
37. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, et al. (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. The Journal of neuroscience: the official journal of the Society for Neuroscience 20: 89-102.
38. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR (1997) Regulatory phosphorylation of AMPAtype glutamate receptors by CaM-KII during long-term potentiation. Science 276: 2042-2045.
39. Derkach V, Barria A, Soderling TR (1999) Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proceedings of the National Academy of Sciences of the United States of America 96: 3269-3274.
40. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, Huganir RL (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16: 1179-1188.
41. Metzger F, Wiese S, Sendtner M (1998) Effect of glutamate on dendritic growth in embryonic rat motoneurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 18: 1735-1742.
42. Maier W, Bednorz M, Meister S, Roebroek A, Weggen S, et al. (2013) LRP1 is critical for the surface distribution and internalization of the NR2B NMDA receptor subtype. Mol Neurodegener 8: 25.
43. Nakajima C, Kulik A, Frotscher M, Herz J, Schafer M, et al. (2013) Low density lipoprotein receptorrelated protein 1 (LRP1) modulates N-methyl-D-aspartate (NMDA) receptor-dependent intracellular signaling and NMDA-induced regulation of postsynaptic protein complexes. The Journal of biological chemistry 288: 21909-21923.
44. Joiner ML, Lise MF, Yuen EY, Kam AY, Zhang M, et al. (2010) Assembly of a beta2-adrenergic receptor-GluR1 signalling complex for localized cAMP signalling. The EMBO journal 29: 482-495.
45. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290: 1364-1368.
46. Beique JC, Andrade R (2003) PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. The Journal of physiology 546: 859-867.
47. Stein V, House DR, Bredt DS, Nicoll RA (2003) Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. The Journal of neuroscience: the official journal of the Society for Neuroscience 23: 5503-5506.
48. Ehrlich I, Malinow R (2004) Postsynaptic density 95 controls AMPA receptor incorporation during longterm potentiation and experience-driven synaptic plasticity. The Journal of neuroscience: the official journal of the Society for Neuroscience 24: 916-927.
49. Colledge M, Snyder EM, Crozier RA, Soderling JA, Jin Y, et al. (2003) Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40: 595-607.
50. He K, Song L, Cummings LW, Goldman J, Huganir RL, et al. (2009) Stabilization of Ca2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation. Proceedings of the National Academy of Sciences of the United States of America 106: 20033-20038.
51. 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.
52. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, et al. (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62: 405-496.
53. Wenthold RJ, Petralia RS, Blahos J, II, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 16: 1982-1989.
54. Monyer H, Seeburg PH, Wisden W (1991) Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6: 799-810.
55. Craig AM, Blackstone CD, Huganir RL, Banker G (1993) The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10: 1055-1068.
56. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, et al. (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15: 193-204.
57. Sans N, Vissel B, Petralia RS, Wang YX, Chang K, et al. (2003) Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. The Journal of neuroscience: the official journal of the Society for Neuroscience 23: 9367-9373.
58. Cull-Candy S, Kelly L, Farrant M (2006) Regulation of Ca2+ -permeable AMPA receptors: synaptic plasticity and beyond. Current opinion in neurobiology 16: 288-297.
59. Spitzer NC (2002) Activity-dependent neuronal differentiation prior to synapse formation: the functions of calcium transients. Journal of physiology, Paris 96: 73-80.
60. Redmond L, Ghosh A (2005) Regulation of dendritic development by calcium signaling. Cell calcium 37: 411-416.
61. Prithviraj R, Kelly KM, Espinoza-Lewis R, Hexom T, Clark AB, et al. (2008) Differential regulation of dendrite complexity by AMPA receptor subunits GluR1 and GluR2 in motor neurons. Developmental neurobiology 68: 247-264.
62. Kanekiyo T, Bu G (2014) The low-density lipoprotein receptor-related protein 1 and amyloid-beta clearance in Alzheimer's disease. Front Aging Neurosci 6: 93.
63. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Annals of neurology 27: 457-464.
64. Arendt T (2009) Synaptic degeneration in Alzheimer's disease. Acta neuropathologica 118: 167-179.
65. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298: 789-791.
66. Zhao WQ, Santini F, Breese R, Ross D, Zhang XD, et al. (2010) Inhibition of calcineurin-mediated endocytosis and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors prevents amyloid beta oligomer-induced synaptic disruption. The Journal of biological chemistry 285: 7619-7632.
67. Kang DE, Pietrzik CU, Baum L, Chevallier N, Merriam DE, et al. (2000) Modulation of amyloid betaprotein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway. The Journal of clinical investigation 106: 1159-1166.
68. Valastro B, Ghribi O, Poirier J, Krzywkowski P, Massicotte G (2001) AMPA receptor regulation and LTP in the hippocampus of young and aged apolipoprotein E-deficient mice. Neurobiology of aging 22: 9-15.