Role of tissue plasminogen activator receptor LRP in hippocampal long- term potentiation

Journal of Neuroscience

Volumn 20, Issue 2, 2000, Pages 542-549

  Zhuo, Min ^a   Holtzman, David M ^a   Li, Yonghe ^a   Osaka, Hiroshi ^a   DeMaro, Joe ^a   Jacquin, Mark ^a   Bu, Guojun ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Hippocampus; LRP; LTP; PKA; tPA

Indexed keywords

CELL SURFACE RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR; TISSUE PLASMINOGEN ACTIVATOR;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; HIPPOCAMPUS; IMMEDIATE EARLY GENE; LIGAND BINDING; LONG TERM POTENTIATION; MOUSE; MULTIGENE FAMILY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECEPTOR BINDING; SYNAPTIC TRANSMISSION;

EID: 0034651082     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-02-00542.2000     Document Type: Article

References (71)

1. Abel T, Nguyen PV, Barad M, Deuel TAS, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Abraham CR, Selkoe DJ, Potter H (1988) Immunochemical identification of the serine protease inhibitor alpha 1-antichymotrypsin in the brain amyloid deposits of Alzheimer's disease. Cell 52:487-501.
3. Baranes D, Lederfein D, Huang Y-Y, Chen M, Baily CH, Kandel ER (1998) Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21:813-825.
4. Bellosta S, Nathan BP, Orth M, Dong LM, Mahley RW, Pitas RE (1995) Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth. J Biol Chem 270:27063-27071.
5. Blacker D, Wilcox MA, Laird NM, Rodes L, Horvath SM, Go RCP, Perry R, Watson B, Bassett SS, McInnis MG, Albert MS, Hyman BT, Tanzi RE (1998) Alpha-2 macroglobulin is genetically associated with Alzheimer's disease. Nat Genet 19:357-360.
6. Bu G (1998) Receptor-associated protein: a specialized chaperone and antagonist for members of the LDL receptor gene family. Curr Opin Lipidol 9:149-155.
7. Bu G, Schwartz AL (1998) RAP, a novel type of ER chaperone. Trends Cell Biol 8:272-276.
8. Bu G, Morton PA, Schwartz AL (1992a) Identification and partial characterization by chemical cross-linking of a binding protein for tissue-type plasminogen activator (t-PA) on rat hepatoma cells. A plasminogen activator inhibitor type 1-independent t-PA receptor. J Biol Chem 267:15595-15602.
9. 2-macroglobulin receptor is an hepatic receptor for tissue-type plasminogen activator. Proc Natl Acad Sci USA 89:7427-7431.
10. Bu G, Maksymovitch EA, Schwartz AL (1993) Receptor-mediated endocytosis of tissue-type plasminogen activator by low density lipoprotein receptor-related protein on human hepatoma HepG2 cells. J Biol Chem 268:13002-13009.
11. 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.
12. Bu G, Geuze HJ, Strous GJ, Schwartz AL (1995) 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J 14:2269-2280.
13. Carmeliet P, Schoonjans L, Kiccken L, Ream B, Degen J, Bronson R, DeVos R, Van den Oord JJ, Collen D, Mulligan RC (1994) Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368:419-424.
14. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TVP, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
15. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923.
16. Fagan AM, Bu G, Sun Y, Daugherty A, Holtzman DM (1996) Apolipoprotein E-containing high density lipoprotein promotes neurite outgrowth and is a ligand for the low density lipoprotein receptor-related protein. J Biol Chem 271:30121-30125.
17. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
18. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
19. Frey U, Frey S, Schollmeier F, Krug M (1995) Influence of actinomycin D, a RNA-synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol (Lond) 490:703-711.
20. Frey U, Muller M, Kuhl D (1996) A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J Neurosci 16:2057-2063.
21. Fukao H, Matsuo O (1998) Analysis of tissue-type plasminogen activator receptor (t-PAR) in human endothelial cells. Semin Thromb Hemost 24:269-273.
22. Golden JP, Rana JZ, Davis J, Zahm DS, Jacquin MF (1993) Organization of the proximal, orbital segment of the infraorbital nerve at multiple intervals after axotomy at birth: a quantitative electron microscopic study in rat. J Comp Neurol 338:159-174.
23. Goretzki L, Mueller BM (1998) Low-density-lipoprotein-receptor-related protein (LRP) interacts with a GTP-binding protein. Biochem J 336:381-386.
24. Grimes ML, Zhou J, Beattie EC, Yuen EC, Hall DE, Valletta JS, Topp KS, LaVail JH, Bunnett NW, Mobley WC (1996) Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J Neurosci 16:7950-7964.
25. Hajjar KA, Jacovina AT, Chacko J (1994) An endothelial cell receptor for plasminogen/tissue plasminogen activator. J Biol Chem 269:21191-21197.
26. Hardy MM, Feder J, Wolfe RA, Bu G (1997) Low density lipoprotein receptor-related protein modulates the expression of tissue-type plasminogen activator in human colon fibroblasts. J Biol Chem 272:6812-6817.
27. Hawkins RD, Kandel ER, Siegelbaum SA (1993) Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu Rev Neurosci 16:625-665.
28. Hayden SM, Seeds NW (1996) Modulated expression of plasminogen activator system components in cultured cells from dissociated mouse dorsal root ganglia. J Neurosci 16:2307-2317.
29. Herz J, Hamann U, Rogne S, Myklebost O, Gausepohl H, Stanley KK (1988) Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J 7:4119-4127.
30. Herz J, Clouthier DE, Hammer RE (1992) LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 71:411-421.
31. Herz J, Couthier DE, Hammer RE (1993) Correction: LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 73:428.
32. Hollenbach E, Ackermann S, Hyman BT, Rebeck GW (1998) Confirmation of an association between a polymorphism in exon 3 of the low-density lipoprotein receptor-related protein gene and Alzheimer's disease. Neurology 50:1905-1907.
33. Hollister RD, Kisiel W, Hyman BT (1996) Immunohistochemical localization of tissue factor pathway inhibitor-1 (TFPI-1), a Kunitz protease inhibitor, in Alzheimer's disease. Brain Res 728:13-19.
34. Holtzman DM, Pitas RE, Kilbridge J, Nathan B, Mahley RW, Bu G, Schwartz AL (1995) LRP mediates apolipoprotein E-dependent neurite outgrowth in CNS-derived neuronal cells. Proc Natl Acad Sci USA 92:9480-9484.
35. Holtzman DM, Fagan AM (1998) Potential role of apoE in structural plasticity in the nervous system: implications for disorders of the central nervous system. Trends Cardiovasc Med 8:250-255.
36. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sei USA 96:3228-3233.
37. Huang YY, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learning Memory 1:74-82.
38. Huang YY, Bach ME, Lipp HP, Zhuo M, Wolfer DP, Hawkins RD, Schoonjans L, Kandel ER, Godfraind JM, Mulligan R, Collen D, Carmeliet P (1996) Mice lacking the gene encoding tissue-type plasminogen activator show a selective inference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc Natl Acad Sci USA 93:8699-8704.
39. Kang DE, Saitoh T, Chen X, Xia Y, Masliah E, Hansen LA, Thomas RG, Thal LJ, Katzman R (1997) Genetic association of the low-density lipoprotein receptor-related protein gene (LRP), an apolipoprotein E receptor, with late-onset Alzheimer's disease. Neurology 49:56-61.
40. Kim Y-H, Park J-H, Hong SH, Koh JY (1999) Nonproteolytic neuroprotection by human recombinant tissue plasminogen activator. Science 284:647-650.
41. Knauer MF, Orlando RA, Glabe CG (1996) Cell surface APP751 forms complexes with protease nexin 2 ligands and is internalized via the low density lipoprotein receptor-related protein (LRP). Brain Res 740:6-14.
42. Kounnas MZ, Moir RD, Rebeck GW, Bush AI, Argraves WS, Tanzi RE, Hyman BT, Strickland DK (1995) LDL receptor-related protein, a multifunctional apoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82:331-340.
43. Krieger M, Herz J (1994) Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu Rev Biochem 63:601-637.
44. Lendon CL, Talbot CJ, Craddock NJ, Han SW, Wragg M, Morris JC, Goate AM (1997) Genetic association studies between dementia of the Alzheimer's type and three receptors for apolipoprotein E in a Caucasian population. Neurosci Lett 222:187-190.
45. Liao A, Nitsch RM, Greenberg SM, Finckh U, Blacker D, Albert M, Rebeck GW, Gomezisla T, Clatworthy A, Binetti G, Hock C, Muellerthomsen T, Mann U, Zuchowski K, Beisiegel U, Staehelin H, Growdon JH, Tanzi RE, Hyman BT (1998) Genetic association of an alpha-2-macroglobulin (Va11000I1e) polymorphism and Alzheimer's disease. Hum Mol Genet 7:1953-1956.
46. Lijnen HR, Collen D (1991) Strategies for the improvement of thrombolytic agents. Thromb Haemost 66:88-110.
47. Moser EI, Krobert KA, Moser MB, Morris RG (1998) Impaired spatial learning after saturation of long-term potentiation. Science 281:2038-2042.
48. Nalbantoglu J, Tirado-Santiago G, Lahsaini A, Poirier J, Goncalves O, Verge G, Momoli F, Welner SA, Massicotte G, Julien JP, Shapiro ML (1997) Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387:500-505.
49. Narita M, Bu G, Holtzman DM, Schwartz AL (1997) The low density lipoprotein receptor-related protein (LRP), a multifunctional ApoE receptor, modulates hippocampal neurite development. J Neurochem 68:587-595.
50. Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16:3189-3198.
51. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107.
52. Nicoll RA, Malenka RC (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-118.
53. 2-macroglobulin receptor. Proc Natl Acad Sci USA 89:7422-7426.
54. Orth K, Willnow T, Herz J, Gething MJ, Sambrook J (1994) Low density lipoprotein receptor-related protein is necessary for the internalization of both tissue-type plasminogen activator-inhibitor complexes and free tissue-type plasminogen activator. J Biol Chem 269:21117-21122.
55. Otter M, Barrett-Bergshoeff MM, Rijken DC (1991) Binding of tissue-type plasminogen activator by the mannose receptor. J Biol Chem 266:13931-13935.
56. Pittman RN, Ivins JK, Buettner HM (1989) Neuronal plasminogen activators: cell surface binding sites and involvement in neuronal outgrowth. J Neurosci 9:4269-4286.
57. Qi M, Zhuo M, Skalhegg BS, Brandon EP, Kandel ER, McKnight GS, Idzerda RL (1996) Impaired hippocampal plasticity in mice lacking the Cβ1 catalytic subunit of cAM P-dependent protein kinase. Proc Natl Acad Sci USA 93:1571-1576.
58. Qian Z, Gilbert ME, Colicos MA, Kandel ER, Kuhl D (1993) Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361:453-457.
59. 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Ann Neurol 37:211-217.
60. Schuman EM (1997) Synapse specificity and long-term information storage. Neuron 18:339-342.
61. Seeds NW, Williams BL, Bickford PC (1995) Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270:992-994.
62. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380-1386.
63. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: high avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer's disease. Proc Natl Acad Sci USA 90:1977-1981.
64. Sun YL, Wu S, Bu G, Onifade MK, Patel SN, Ladu MJ, Fagan AM, Holtzman DM (1998) Glial fibrillary acidic protein-apolipoprotein E (apoE) transgenic mice: astrocyte-specific expression and differing biological effects of astrocyte-secreted apoE3 and apoE4 lipoproteins. J Neurosci 18:3261-3272.
65. Trommsdorff M, Borg JP, Margolis B, Herz J (1998) Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J Biol Chem 273:33556-33560.
66. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and apoE receptor 2. Cell 9:689-701.
67. 125I-tissue plasminogen activator binding to cerebellar granule neurons. J Cell Biol 109:265-271.
68. Ware JH, DiBenedetto AJ, Pittman RN (1995) Localization of tissue plasminogen activator mRNA in adult rat brain. Brain Res 37:275-281.
69. Warshawsky I, Bu G, Schwartz AL (1993) Identification of domains on the 39-kDa protein that inhibit the binding of ligands to the low density lipoprotein receptor-related protein. J Biol Chem 268:22046-22054.
70. Welling TH, Huber TS, Messina LM, Stanley JC (1996) Tissue plasminogen activator increases canine endothelial cell proliferation rate through a plasmin-independent, receptor-mediated mechanism. J Surg Res 66:36-42.
71. Willnow TE, Orth K, Herz J (1994) Molecular dissection of ligand binding sites on the low density lipoprotein receptor-related protein. J Biol Chem 269:15827-15832.