SGP-1 increases dendritic and synaptic development dependent on synaptic activity

Neuroscience Research

Volumn 56, Issue 4, 2006, Pages 372-385

  Cove, Joshua ^a   Morales, Carlos R ^b   Baranes, Danny ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

AMPA receptor; Hippocampus; Neurite outgrowth; SGP 1

Indexed keywords

GLUTAMATE RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; PROSAPOSIN; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DENDRITIC CELL; DENSITY; ENDOCYTOSIS; HIPPOCAMPUS; IMMUNOREACTIVITY; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPTOGENESIS;

ANIMALS; AXONS; CELLS, CULTURED; DENDRITES; ENDOCYTOSIS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; HIPPOCAMPUS; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; MICROSCOPY, FLUORESCENCE; MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SAPOSINS; SYNAPSES; TRANSFECTION;

EID: 33750975102     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2006.08.008     Document Type: Article

References (71)

1. Alonso M., Medina J.H., and Pozzo-Miller L. ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn. Mem. 11 2 (2004) 172-178
2. Baranes D., Lederfein D., Huang Y.Y., Chen M., Bailey C.H., and Kandel E.R. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21 4 (1998) 813-825
3. Baranes D., Lopez-Garcia J.C., Chen M., Bailey C.H., and Kandel E.R. Reconstitution of the hippocampal mossy fiber and associational-commissural pathways in a novel dissociated cell culture system. Proc. Natl. Acad. Sci. U.S.A. 93 10 (1996) 4706-4711
4. Blochl A., and Thoenen H. Localization of cellular storage compartments and sites of constitutive and activity-dependent release of nerve growth factor (NGF) in primary cultures of hippocampal neurons. Mol. Cell Neurosci. 7 3 (1996) 173-190
5. Campana W.M., Hiraiwa M., Addison K.C., and Obrien J.S. Induction of MAPK phosphorylation by prosaposin and prosaptide in PC12 cells. Biochem. Biophys. Res. Commun. 229 3 (1996) 706-712
6. Campana W.M., Hiraiwa M., and O'Brien J.S. Prosaptide activates the MAPK pathway by a G-protein-dependent mechanism essential for enhanced sulfatide synthesis by Schwann cells. FASEB J. 12 3 (1998) 307-314
7. Campana W.M., Mohiuddin L., Misasi R., O'Brien J.S., and Calcutt N.A. Prosaposin-derived peptides enhanced sprouting of sensory neurons in vitro and induced sprouting at motor endplates in vivo. J. Peripher. Nerv. Syst. 5 3 (2000) 126-130
8. Carrigan C.N., and Imperiali B. The engineering of membrane-permeable peptides. Anal. Biochem. 341 2 (2005) 290-298
9. Causing C.G., Gloster A., Aloyz R., Bamji S.X., Chang E., Fawcett J., Kuchel G., and Miller F.D. Synaptic innervation density is regulated by neuron-derived BDNF. Neuron 18 2 (1997) 257-267
10. Chen F., Zhi D., and Xia G. Intracellular FITC-derivatization with PEG. Electrophoresis 26 21 (2005) 4204-4205
11. Cheng B., Furukawa K., O'Keefe J.A., Goodman Y., Kihiko M., Fabian T., and Mattson M.P. Basic fibroblast growth factor selectively increases AMPA-receptor subunit GluR1 protein level and differentially modulates Ca2+ responses to AMPA and NMDA in hippocampal neurons. J. Neurochem. 65 6 (1995) 2525-2536
12. Cheng C.M., Mervis R.F., Niu S.L., Salem Jr. N., Witters L.A., Tseng V., Reinhardt R., and Bondy C.A. Insulin-like growth factor 1 is essential for normal dendritic growth. J. Neurosci. Res. 73 1 (2003) 1-9
13. Chung H.J., Xia J., Scannevin R.H., Zhang X., and Huganir R.L. Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20 19 (2000) 7258-7267
14. Coffey E.T., Akerman K.E., and Courtney M.J. Brain derived neurotrophic factor induces a rapid upregulation of synaptophysin and tau proteins via the neurotrophin receptor TrkB in rat cerebellar granule cells. Neurosci. Lett. 227 3 (1997) 177-180
15. Cohen T., Ravid L., Altman N., Madar-Shapiro L., Fein A., Weil M., and Horowitz M. Conservation of expression and alternative splicing in the prosaposin gene. Brain Res. Mol. Brain Res. 129 1-2 (2004) 8-19
16. Danzer S.C., Crooks K.R., Lo D.C., and McNamara J.O. Increased expression of brain-derived neurotrophic factor induces formation of basal dendrites and axonal branching in dentate granule cells in hippocampal explant cultures. J. Neurosci. 22 22 (2002) 9754-9763
17. Davies A.M. Paracrine and autocrine actions of neurotrophic factors. Neurochem. Res. 21 7 (1996) 749-753
18. 2+ mobilization through inositol(1,4,5)trisphosphate or ryanodine receptors in cerebellar granule cells in primary culture. Eur. J. Neurosci. 11 9 (1999) 3015-3022
19. DeSouza S., Fu J., States B.A., and Ziff E.B. Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J. Neurosci. 22 9 (2002) 3493-3503
20. Dijkhuizen P.A., and Ghosh A. Regulation of dendritic growth by calcium and neurotrophin signaling. Prog. Brain Res. 147 (2005) 17-27
21. Ehlers M.D. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28 2 (2000) 511-525
22. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., and Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381 6584 (1996) 706-709
23. Fukudome Y., Tabata T., Miyoshi T., Haruki S., Araishi K., Sawada S., and Kano M. Insulin-like growth factor-I as a promoting factor for cerebellar Purkinje cell development. Eur. J. Neurosci. 17 10 (2003) 2006-2016
24. Furuse H., Waki H., Kaneko K., Fujii S., Miura M., Sasaki H., Ito K.I., Kato H., and Ando S. Effect of the mono- and tetra-sialogangliosides, GM1 and GQ1b, on long-term potentiation in the CA1 hippocampal neurons of the guinea pig. Exp. Brain Res. 123 3 (1998) 307-314
25. Goldin M., and Segal M. Protein kinase C and ERK involvement in dendritic spine plasticity in cultured rodent hippocampal neurons. Eur. J. Neurosci. 17 12 (2003) 2529-2539
26. Goldshmit Y., Greenhalgh C.J., and Turnley A.M. Suppressor of cytokine signalling-2 and epidermal growth factor regulate neurite outgrowth of cortical neurons. Eur. J. Neurosci. 20 9 (2004) 2260-2266
27. Gottschalk W.A., Jiang H., Tartaglia N., Feng L., Figurov A., and Lu B. Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. Learn. Mem. 6 3 (1999) 243-256
28. Hanamura K., Harada A., Katoh-Semba R., Murakami F., and Yamamoto N. BDNF and NT-3 promote thalamocortical axon growth with distinct substrate and temporal dependency. Eur. J. Neurosci. 19 6 (2004) 1485-1493
29. Hartmann M., Heumann R., and Lessmann V. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J. 20 21 (2001) 5887-5897
30. Heyder P., Gaipl U.S., Beyer T.D., Voll E.R., Kern P.M., Stach C., Kalden J.R., and Herrmann M. Early detection of apoptosis by staining of acid-treated apoptotic cells with FITC-labeled lectin from Narcissus pseudonarcissus. Cytometry A 55 2 (2003) 86-93
31. Hiraiwa M., Campana W.M., Martin B.M., and Obrien J.S. Prosaposin receptor: evidence for a G-protein-associated receptor. Biochem. Biophys. Res. Commun. 240 2 (1997) 415-418
32. Hiraiwa M., Campana W.M., Mizisin A.P., Mohiuddin L., and O'Brien J.S. Prosaposin: a myelinotrophic protein that promotes expression of myelin constituents and is secreted after nerve injury. Glia 26 4 (1999) 353-360
33. Hiraiwa M., Soeda S., Kishimoto Y., and Obrien J.S. Binding and transport of gangliosides by prosaposin. Proc. Natl. Acad. Sci. U.S.A. 89 23 (1992) 11254-11258
34. Horch H.W. Local effects of BDNF on dendritic growth. Rev. Neurosci. 15 2 (2004) 117-129
35. Houlgatte R., Mallat M., Brachet P., and Prochiantz A. Secretion of nerve growth factor in cultures of glial cells and neurons derived from different regions of the mouse brain. J. Neurosci. Res. 24 2 (1989) 143-152
36. Howe C.L., and Mobley W.C. Long-distance retrograde neurotrophic signaling. Curr. Opin. Neurobiol. 15 1 (2005) 40-48
37. Itami C., Kimura F., Kohno T., Matsuoka M., Ichikawa M., Tsumoto T., and Nakamura S. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc. Natl. Acad. Sci. U.S.A. 100 22 (2003) 13069-13074
38. Jin X., Hu H., Mathers P.H., and Agmon A. Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J. Neurosci. 23 13 (2003) 5662-5673
39. Kohrmann M., Haubensak W., Hemraj I., Kaether C., Lessmann V.J., and Kiebler M.A. Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J. Neurosci. Res. 58 6 (1999) 831-835
40. Kotani Y., Matsuda S., Sakanaka M., Kondoh K., Ueno S., and Sano A. Prosaposin facilitates sciatic nerve regeneration in vivo. J. Neurochem. 66 5 (1996) 2019-2025
41. Kotani Y., Matsuda S., Wen T.C., Sakanaka M., Tanaka J., Maeda N., Kondoh K., Ueno S., and Sano A. A hydrophilic peptide comprising 18 amino acid residues of the prosaposin sequence has neurotrophic activity in vitro and in vivo. J. Neurochem. 66 5 (1996) 2197-2200
42. Labelle C., and Leclerc N. Exogenous BDNF, NT-3 and NT-4 differentially regulate neurite outgrowth in cultured hippocampal neurons. Brain Res. Dev. Brain Res. 123 1 (2000) 1-11
43. Lee H.K., Barbarosie M., Kameyama K., Bear M.F., and Huganir R.L. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405 6789 (2000) 955-959
44. Lee S.H., Liu L., Wang Y.T., and Sheng M. Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36 4 (2002) 661-674
45. Lee T.J., Sartor O., Luftig R.B., and Koochekpour S. Saposin C promotes survival and prevents apoptosis via PI3K/Akt-dependent pathway in prostate cancer cells. Mol. Cancer 3 1 (2004) 31
46. Lefrancois S., May T., Knight C., Bourbeau D., and Morales C.R. The lysosomal transport of prosaposin requires the conditional interaction of its highly conserved d domain with sphingomyelin. J. Biol. Chem. 277 19 (2002) 17188-17199
47. Li A.J., Suzuki S., Suzuki M., Mizukoshi E., and Imamura T. Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons. Eur. J. Neurosci. 16 7 (2002) 1313-1324
48. Liao D., Scannevin R.H., and Huganir R. Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J. Neurosci. 21 16 (2001) 6008-6017
49. Lu B., and Chow A. Neurotrophins and hippocampal synaptic transmission and plasticity. J. Neurosci. Res. 58 1 (1999) 76-87
50. Lu W., Man H., Ju W., Trimble W.S., MacDonald J.F., and Wang Y.T. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29 1 (2001) 243-254
51. Madar-Shapiro L., Pasmanik-Chor M., Vaccaro A.M., Dinur T., Dagan A., Gatt S., and Horowitz M. Importance of splicing for prosaposin sorting. Biochem. J. 337 (1999) 433-443
52. Majima E., Ishida M., Miki S., Shinohara Y., and Terada H. Specific labeling of the bovine heart mitochondrial phosphate carrier with fluorescein 5-isothiocyanate: roles of Lys185 and putative adenine nucleotide recognition site in phosphate transport. J. Biol. Chem. 276 13 (2001) 9792-9799
53. Morales C.R., and Badran H. Prosaposin ablation inactivates the MAPK and Akt signaling pathways and interferes with the development of the prostate gland. Asian J. Androl. 5 1 (2003) 57-63
54. Nakajima K., Honda S., Tohyama Y., Imai Y., Kohsaka S., and Kurihara T. Neurotrophin secretion from cultured microglia. J. Neurosci. Res. 65 4 (2001) 322-331
55. Obrien J.S., Carson G.S., Seo H.C., Hiraiwa M., and Kishimoto Y. Identification of Prosaposin As a Neurotrophic Factor. Proc. Natl. Acad. Sci. U.S.A. 91 20 (1994) 9593-9596
56. Obrien J.S., Carson G.S., Seo H.C., Hiraiwa M., Weiler S., Tomich J.M., Barranger J.A., Kahn M., Azuma N., and Kishimoto Y. Identification of the neurotrophic factor sequence of prosaposin. FASEB J. 9 8 (1995) 681-685
57. Sano A., Matsuda S., Wen T.C., Kotani Y., Kondoh K., Ueno S., Kakimoto Y., Yoshimura H., and Sakanaka M. Protection by prosaposin against ischemia-induced learning-disability and neuronal loss. Biochem. Biophys. Res. Commun. 204 2 (1994) 994-1000
58. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., and Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284 5421 (1999) 1811-1816
59. Stefani A., Pisani A., Mercuri N.B., and Calabresi P. The modulation of calcium currents by the activation of mGluRs. Functional implications. Mol. Neurobiol. 13 1 (1996) 81-95
60. Sun Y., Jin P., Witte D.P., and Grabowski G.A. Isolation and characterization of the human prosaposin promoter. Gene 218 1-2 (1998) 37-47
61. Tartaglia N., Du J., Tyler W.J., Neale E., Pozzo-Miller L., and Lu B. Protein synthesis-dependent and -independent regulation of hippocampal synapses by brain-derived neurotrophic factor. J. Biol. Chem. 276 40 (2001) 37585-37593
62. Tyler W.J., and Pozzo-Miller L.D. BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 21 12 (2001) 4249-4258
63. Van Aelst L., and Cline H.T. Rho GTPases and activity-dependent dendrite development. Curr. Opin. Neurobiol. 14 3 (2004) 297-304
64. Walicke P.A. Basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J. Neurosci. 8 7 (1988) 2618-2627
65. Wiley H.S., and Burke P.M. Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic 2 1 (2001) 12-18
66. Wilkins R.C., Bellier P.V., Kutzner B.C., and McNamee J.P. Increased FITC fluorescence on LPS stimulated neutrophils cultured in whole blood. Cell Biol. Int. 30 4 (2006) 394-399
67. Wirth M.J., Brun A., Grabert J., Patz S., and Wahle P. Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5. Development 130 23 (2003) 5827-5838
68. Yan L.Z., Otero D.A.C., Hiraiwa M., and O'Brien J.S. Prosaptide (TM) D5 reverses hyperalgesia: inhibition of calcium channels through a pertussis toxin-sensitive G-protein mechanism in the rat. Neurosci. Lett. 278 1-2 (2000) 120-122
69. Yoshida K., and Gage F.H. Fibroblast growth factors stimulate nerve growth factor synthesis and secretion by astrocytes. Brain Res. 538 1 (1991) 118-126
70. Zhao Q., and Morales C.R. Identification of a novel sequence involved in lysosomal sorting of the sphingolipid activator protein prosaposin. J. Biol. Chem. 275 32 (2000) 24829-24839
71. Zhu J.J., Qin Y., Zhao M., Van Aelst L., and Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110 4 (2002) 443-455