Ligand-induced homotypic and heterotypic clustering of apolipoprotein E Receptor 2

Journal of Biological Chemistry

Volumn 289, Issue 23, 2014, Pages 15894-15903

  Divekar, Shailaja D ^a   Burrell, Teal C ^a   Lee, Jennifer E ^a   Weeber, Edwin J ^b   Rebeck, G William ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; GLYCOPROTEINS; LIPOPROTEINS; NEURONS;

AMYLOID PRECURSOR PROTEINS; EXTRACELLULAR GLYCOPROTEINS; INTRACELLULAR DOMAIN; MULTIVALENT LIGANDS; NEURONAL MIGRATION; SIGNALING PATHWAYS; TRANS-MEMBRANE PROTEINS; VERY LOW DENSITY LIPOPROTEIN RECEPTORS;

LIGANDS;

AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E RECEPTOR 2; CARRIER PROTEINS AND BINDING PROTEINS; F SPONDIN PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN FC RAP; RECEPTOR; REELIN; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

ARTICLE; CONTROLLED STUDY; LIGAND BINDING; NERVE CELL; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN CLUSTERIING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN (APP); APOLIPOPROTEIN E (APOE); RECEPTOR; SYNAPSE;

ANIMALS; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; LDL-RECEPTOR RELATED PROTEINS; LIGANDS; MICE; NEURONS; PHOSPHORYLATION;

EID: 84902124968     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.537548     Document Type: Article

References (85)

1. Beffert, U., Stolt, P. C., and Herz, J. (2004) Functions of lipoprotein receptors in neurons. J. Lipid Res. 45, 403-409
2. Tissir, F., and Goffinet, A. M. (2003) Reelin and brain development. Nat. Rev. Neurosci. 4, 496-505
3. Beffert, U., Weeber, E. J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J. D., Li, W. P., Adelmann, G., Frotscher, M., Hammer, R. E., and Herz, J. (2005) Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor ApoER2. Neuron 47, 567-579
4. Dumanis, S. B., Cha, H. J., Song, J. M., Trotter, J. H., Spitzer, M., Lee, J. Y., Weeber, E. J., Turner, R. S., Pak, D. T., Rebeck, G. W., and Hoe, H. S. (2011) ApoE receptor 2 regulates synapse and dendritic spine formation. PloS ONE 6, e17203
5. Hack, I., Hellwig, S., Junghans, D., Brunne, B., Bock, H. H., Zhao, S., and Frotscher, M. (2007) Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 134, 3883-3891
6. Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M., and D'Arcangelo, G. (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41, 71-84
7. Niu, S., Yabut, O., and D'Arcangelo, G. (2008) The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J. Neurosci. 28, 10339-10348
8. Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., and Herz, J. (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689-701
9. Howell, B. W., Gertler, F. B., and Cooper, J. A. (1997) Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J. 16, 121-132
10. Reddy, S. S., Connor, T. E., Weeber, E. J., and Rebeck, W. (2011) Similarities and differences in structure, expression, and functions of VLDLR and ApoER2. Mol. Neurodegener. 6, 30
11. Hoe, H. S., Wessner, D., Beffert, U., Becker, A. G., Matsuoka, Y., and Rebeck, G. W. (2005) F-spondin interaction with the apolipoprotein E receptor ApoEr2 affects processing of amyloid precursor protein. Mol. Cell. Biol. 25, 9259-9268
12. Blake, S. M., Strasser, V., Andrade, N., Duit, S., Hofbauer, R., Schneider, W. J., and Nimpf, J. (2008) Thrombospondin-1 binds to ApoER2 and VLDL receptor and functions in postnatal neuronal migration. EMBO J. 27, 3069-3080
13. Burstyn-Cohen, T., Tzarfaty, V., Frumkin, A., Feinstein, Y., Stoeckli, E., and Klar, A. (1999) F-Spondin is required for accurate pathfinding of commissural axons at the floor plate. Neuron 23, 233-246
14. Morimura, T., and Ogawa, M. (2009) Relative importance of the tyrosine phosphorylation sites of Disabled-1 to the transmission of Reelin signaling. Brain Res. 1304, 26-37
15. Gotthardt, M., Trommsdorff, M., Nevitt, M. F., Shelton, J., Richardson, J. A., Stockinger, W., Nimpf, J., and Herz, J. (2000) Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem. 275, 25616-25624
16. Stockinger, W., Brandes, C., Fasching, D., Hermann, M., Gotthardt, M., Herz, J., Schneider, W. J., and Nimpf, J. (2000) The Reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2. J. Biol. Chem. 275, 25625-25632
17. Hoe, H. S., Magill, L. A., Guenette, S., Fu, Z., Vicini, S., and Rebeck, G. W. (2006) FE65 interaction with the ApoE receptor ApoEr2. J. Biol. Chem. 281, 24521-24530
18. Hoe, H. S., Pocivavsek, A., Chakraborty, G., Fu, Z., Vicini, S., Ehlers, M. D., and Rebeck, G. W. (2006) Apolipoprotein E receptor 2 interactions with the N-methyl-D-aspartate receptor. J. Biol. Chem. 281, 3425-3431
19. D'Arcangelo, G., Homayouni, R., Keshvara, L., Rice, D. S., Sheldon, M., and Curran, T. (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24, 471-479
20. Royaux, I., Lambert de Rouvroit, C., D'Arcangelo, G., Demirov, D., and Goffinet, A. M. (1997) Genomic organization of the mouse reelin gene. Genomics 46, 240-250
21. Jossin, Y., Ignatova, N., Hiesberger, T., Herz, J., Lambert de Rouvroit, C., and Goffinet, A. M. (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J. Neurosci. 24, 514-521
22. Yasui, N., Nogi, T., and Takagi, J. (2010) Structural basis for specific recognition of Reelin by its receptors. Structure 18, 320-331
23. Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Forster, E., Sweatt, J. D., and Herz, J. (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem. 277, 39944-39952
24. Rogers, J. T., and Weeber, E. J. (2008) Reelin and apoE actions on signal transduction, synaptic function and memory formation. Neuron Glia Biol. 4, 259-270
25. Durakoglugil, M. S., Chen, Y., White, C. L., Kavalali, E. T., and Herz, J. (2009) Reelin signaling antagonizes beta-amyloid at the synapse. Proc. Natl. Acad. Sci. U. S. A. 106, 15938-15943
26. Feinstein, Y., Borrell, V., Garcia, C., Burstyn-Cohen, T., Tzarfaty, V., Frumkin, A., Nose, A., Okamoto, H., Higashijima, S., Soriano, E., and Klar, A. (1999) F-spondin and mindin: two structurally and functionally related genes expressed in the hippocampus that promote outgrowth of embryonic hippocampal neurons. Development 126, 3637-3648
27. Feinstein, Y., and Klar, A. (2004) The neuronal class 2 TSR proteins Fspondin and Mindin: a small family with divergent biological activities. Int. J. Biochem. Cell Biol. 36, 975-980
28. Hoe, H. S., Tran, T. S., Matsuoka, Y., Howell, B. W., and Rebeck, G. W. (2006) DAB1 and Reelin effects on amyloid precursor protein and ApoE receptor 2 trafficking and processing. J. Biol. Chem. 281, 35176-35185
29. Ho, A., and Südhof, T. C. (2004) Binding of F-spondin to amyloid-β precursor protein: a candidate amyloid-β precursor protein ligand that modulates amyloid-β precursor protein cleavage. Proc. Natl. Acad. Sci. U. S. A., 101, 2548-2553
30. Hoe, H. S., and Rebeck, G. W. (2008) Regulated proteolysis of APP and ApoE receptors. Mol. Neurobiol. 37, 64-72
31. Hoe, H. S., Fu, Z., Makarova, A., Lee, J. Y., Lu, C., Feng, L., Pajoohesh-Ganji, A., Matsuoka, Y., Hyman, B. T., Ehlers, M. D., Vicini, S., Pak, D. T., and Rebeck, G. W. (2009) The effects of amyloid precursor protein on postsynaptic composition and activity. J. Biol. Chem. 284, 8495-8506
32. Nalivaeva, N. N., and Turner, A. J. (2013) The amyloid precursor protein: a biochemical enigma in brain development, function and disease. FEBS Lett. 587, 2046-2054
33. Ichinose, J., Murata, M., Yanagida, T., and Sako, Y. (2004) EGF signalling amplification induced by dynamic clustering of EGFR. Biochem. Biophys. Res. Commun. 324, 1143-1149
34. Wimmer-Kleikamp, S. H., Janes, P. W., Squire, A., Bastiaens, P. I., and Lackmann, M. (2004) Recruitment of Eph receptors into signaling clusters does not require ephrin contact. J. Cell Biol. 164, 661-666
35. Lindsay, R. M. (1996) Role of neurotrophins and Trk receptors in the development and maintenance of sensory neurons: an overview. Philos. Trans. R Soc. Lond. B Biol. Sci. 351, 365-373
36. Triantafilou, M., Gamper, F. G., Haston, R. M., Mouratis, M. A., Morath, S., Hartung, T., and Triantafilou, K. (2006) Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002-31011
37. Yasui, N., Kitago, Y., Beppu, A., Kohno, T., Morishita, S., Gomi, H., Nagae, M., Hattori, M., and Takagi, J. (2011) Functional importance of covalent homodimer of Reelin protein linked via its central region. J. Biol. Chem. 286, 35247-35256
38. Ballif, B. A., Arnaud, L., Arthur, W. T., Guris, D., Imamoto, A., and Cooper, J. A. (2004) Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelinstimulated neurons. Curr. Biol. 14, 606-610
39. Ballif, B. A., Arnaud, L., and Cooper, J. A. (2003) Tyrosine phosphorylation of Disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Brain Res. Mol. Brain Res. 117, 152-159
40. Arnaud, L., Ballif, B. A., and Cooper, J. A. (2003) Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23, 9293-9302
41. Cheng, Y. C., Chen, T. A., Chen, C. Y., Liang, C. M., and Liang, S. M. (2012) 3 poly-G-tailed ODNs inhibit F-spondin to induce cell death and neurite retraction in rat embryonic neurons. Mol. Neurobiol. 45, 536-549
42. Cheng, Y. C., Liang, C. M., Chen, Y. P., Tsai, I. H., Kuo, C. C., and Liang, S. M. (2009) F-spondin plays a critical role in murine neuroblastoma survival by maintaining IL-6 expression. J. Neurochem. 110, 947-955
43. Strasser, V., Fasching, D., Hauser, C., Mayer, H., Bock, H. H., Hiesberger, T., Herz, J., Weeber, E. J., Sweatt, J. D., Pramatarova, A., Howell, B., Schneider, W. J., and Nimpf, J. (2004) Receptor clustering is involved in Reelin signaling. Mol. Cell. Biol. 24, 1378-1386
44. Tamboli, I. Y., Heo, D., and Rebeck, G. W. (2014) Extracellular proteolysis of apolipoprotein E (apoE) by secreted serine neuronal protease. PLoS ONE 9, e93120
45. Brandes, C., Kahr, L., Stockinger, W., Hiesberger, T., Schneider, W. J., and Nimpf, J. (2001) Alternative splicing in the ligand binding domain of mouse ApoE receptor-2 produces receptor variants binding Reelin but not α 2-macroglobulin. J. Biol. Chem. 276, 22160-22169
46. May, P., Bock, H. H., Nimpf, J., and Herz, J. (2003) Differential glycosylation regulates processing of lipoprotein receptors by β-secretase. J. Biol. Chem. 278, 37386-37392
47. Chadwick, W., Brenneman, R., Martin, B., and Maudsley, S. (2010) Complex and multidimensional lipid raft alterations in a murine model of Alzheimer's disease. Int. J. Alzheimers Dis. 2010, 604792
48. Levenson, J. M., Qiu, S., and Weeber, E. J. (2008) The role of Reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene. Biochim. Biophys. Acta 1779, 422-431
49. Ruiz, J., Kouiavskaia, D., Migliorini, M., Robinson, S., Saenko, E. L., Gorlatova, N., Li, D., Lawrence, D., Hyman, B. T., Weisgraber, K. H., and Strickland, D. K. (2005) The apoE isoform binding properties of the VLDL receptor reveal marked differences from LRP and the LDL receptor. J. Lipid Res. 46, 1721-1731
50. Hoe, H. S., Lee, K. J., Carney, R. S., Lee, J., Markova, A., Lee, J. Y., Howell, B. W., Hyman, B. T., Pak, D. T., Bu, G., and Rebeck, G. W. (2009) Interac-tion of reelin with amyloid precursor protein promotes neurite outgrowth. J. Neurosci. 29, 7459-7473
51. Rice, H. C., Young-Pearse, T. L., and Selkoe, D. J. (2013) Systematic evaluation of candidate ligands regulating ectodomain shedding of amyloid precursor protein. Biochemistry 52, 3264-3277
52. Duit, S., Mayer, H., Blake, S. M., Schneider, W. J., and Nimpf, J. (2010) Differential functions of ApoER2 and very low density lipoprotein receptor in Reelin signaling depend on differential sorting of the receptors. J. Biol. Chem. 285, 4896-4908
53. Bouché, E., Romero-Ortega, M. I., Henkemeyer, M., Catchpole, T., Leemhuis, J., Frotscher, M., May, P., Herz, J., and Bock, H. H. (2013) Reelin induces EphB activation. Cell Res. 23, 473-490
54. Bock, H. H., and Herz, J. (2003) Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13, 18-26
55. Hoe, H. S., Minami, S. S., Makarova, A., Lee, J., Hyman, B. T., Matsuoka, Y., and Rebeck, G. W. (2008) Fyn modulation of Dab1 effects on amyloid precursor protein and ApoE receptor 2 processing. J. Biol. Chem. 283, 6288-6299
56. Grant, S. G., O'Dell, T. J., Karl, K. A., Stein, P. L., Soriano, P., and Kandel, E. R. (1992) Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258, 1903-1910
57. Tsujio, I., Tanaka, T., Kudo, T., Nishikawa, T., Shinozaki, K., Grundke-Iqbal, I., Iqbal, K., and Takeda, M. (2000) Inactivation of glycogen synthase kinase-3 by protein kinase C δ: implications for regulation of Tau phosphorylation. FEBS Lett. 469, 111-117
58. Tanaka, T., Tsujio, I., Nishikawa, T., Shinosaki, K., Kudo, T., and Takeda, M. (2000) Significance of Tau phosphorylation and protein kinase regulation in the pathogenesis of Alzheimer disease. Alzheimer Dis. Assoc. Disord. 14, S18-24
59. Liu, S. J., Zhang, A. H., Li, H. L., Wang, Q., Deng, H. M., Netzer, W. J., Xu, H., and Wang, J. Z. (2003) Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of Tau and impairment of spatial memory. J. Neurochem. 87, 1333-1344
60. Hiesberger, T., Trommsdorff, M., Howell, B. W., Goffinet, A., Mumby, M. C., Cooper, J. A., and Herz, J. (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates Tau phosphorylation. Neuron 24, 481-489
61. Schamel, W. W., and Alarcón, B. (2013) Organization of the resting TCR in nanoscale oligomers. Immunol. Rev., 251, 13-20
62. Kumar, R., Ferez, M., Swamy, M., Arechaga, I., Rejas, M. T., Valpuesta, J. M., Schamel, W. W., Alarcon, B., and van Santen, H. M. (2011) Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. Immunity 35, 375-387
63. Manz, B. N., and Groves, J. T. (2010) Spatial organization and signal transduction at intercellular junctions. Nat. Rev. Mol. Cell Biol. 11, 342-352
64. Manz, B. N., Jackson, B. L., Petit, R. S., Dustin, M. L., and Groves, J. (2011) T-cell triggering thresholds are modulated by the number of antigen within individual T-cell receptor clusters. Proc. Natl. Acad. Sci. U. S. A. 108, 9089-9094
65. Mossman, K. D., Campi, G., Groves, J. T., and Dustin, M. L. (2005) Altered TCR signaling from geometrically repatterned immunological synapses. Science 310, 1191-1193
66. Bustos, F. J., Varela-Nallar, L., Campos, M., Henriquez, B., Phillips, M., Opazo, C., Aguayo, L. G., Montecino, M., Constantine-Paton, M., Inestrosa, N. C., and van Zundert, B. (2014) PSD95 suppresses dendritic arbor development in mature hippocampal neurons by occluding the clustering of NR2B-NMDA receptors. PloS ONE 9, e94037
67. Ketchum, C., Miller, H., Song, W., and Upadhyaya, A. (2014) Ligand mobility regulates B cell receptor clustering and signaling activation. Biophys. J. 106, 26-36
68. Hsu, C. J., Hsieh, W. T., Waldman, A., Clarke, F., Huseby, E. S., Burkhardt, J. K., and Baumgart, T. (2012) Ligand mobility modulates immunological synapse formation and T cell activation. PloS ONE 7, e32398
69. Caré, B. R., and Soula, H. A. (2013) Receptor clustering affects signal transduction at the membrane level in the reaction-limited regime. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 87, 012720
70. Kozer, N., Barua, D., Orchard, S., Nice, E. C., Burgess, A. W., Hlavacek, W. S., and Clayton, A. H. (2013) Exploring higher-order EGFR oligomerisation and phosphorylation: a combined experimental and theoretical approach. Mol. Biosyst. 9, 1849-1863
71. Arneja, A., Johnson, H., Gabrovsek, L., Lauffenburger, D. A., and White, F. M. (2014) Qualitatively different T cell phenotypic responses to IL-2 versus IL-15 are unified by identical dependences on receptor signal strength and duration. J. Immunol. 192, 123-135
72. Kozer, N., Barua, D., Henderson, C., Nice, E. C., Burgess, A. W., Hlavacek, W. S., and Clayton, A. H. (2014) Recruitment of the adaptor protein Grb2 to EGFR tetramers. Biochemistry 53, 2594-2604
73. Lohmüller, T., Xu, Q., and Groves, J. T. (2013) Nanoscale obstacle arrays frustrate transport of EphA2-Ephrin-A1 clusters in cancer cell lines. Nano Lett. 13, 3059-3064
74. Head, B. P., Patel, H. H., and Insel, P. A. (2014) Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim Biophys Acta 1838, 532-545
75. Kornau, H. C., Schenker, L. T., Kennedy, M. B., and Seeburg, P. H. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740
76. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378, 85-88
77. Dieckmann, M., Dietrich, M. F., and Herz, J. (2010) Lipoprotein receptors: an evolutionarily ancient multifunctional receptor family. Biol. Chem. 391, 1341-1363
78. Young-Pearse, T. L., Bai, J., Chang, R., Zheng, J. B., LoTurco, J. J., and Selkoe, D. J. (2007) A critical function for β-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J. Neurosci. 27, 14459-14469
79. Rice, H. C., Townsend, M., Bai, J., Suth, S., Cavanaugh, W., Selkoe, D. J., and Young-Pearse, T. L. (2012) Pancortins interact with amyloid precursor protein and modulate cortical cell migration. Development 139, 3986-3996
80. Rogers, J. T., Rusiana, I., Trotter, J., Zhao, L., Donaldson, E., Pak, D. T., Babus, L. W., Peters, M., Banko, J. L., Chavis, P., Rebeck, G. W., Hoe, H. S., and Weeber, E. J. (2011) Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density. Learn. Mem. 18, 558-564
81. Li, X., Kypreos, K., Zanni, E. E., and Zannis, V. (2003) Domains of apoE required for binding to apoE receptor 2 and to phospholipids: implications for the functions of apoE in the brain. Biochemistry 42, 10406-10417
82. He, X., Cooley, K., Chung, C. H., Dashti, N., and Tang, J. (2007) Apolipoprotein receptor 2 and X11 α/β mediate apolipoprotein E-induced endocytosis of amyloid-β precursor protein and β-secretase, leading to amyloid-β production. J. Neurosci. 27, 4052-4060
83. Laffont, I., Takahashi, M., Shibukawa, Y., Honke, K., Shuvaev, V. V., Siest, G., Visvikis, S., and Taniguchi, N. (2002) Apolipoprotein E activates Akt pathway in neuro-2a in an isoform-specific manner. Biochem. Biophys. Res. Commun. 292, 83-87
84. Hoe, H. S., Harris, D. C., and Rebeck, G. W. (2005) Multiple pathways of apolipoprotein E signaling in primary neurons. J. Neurochem. 93, 145-155
85. Hoe, H. S., Pocivavsek, A., Dai, H., Chakraborty, G., Harris, D. C., and Rebeck, G. W. (2006) Effects of apoE on neuronal signaling and APP processing in rodent brain. Brain Res. 1112, 70-79