Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons

Molecular and Cellular Neurosciences

Volumn 7, Issue 3, 1996, Pages 222-238

  Goodman, Laurie J ^a,f   Valverde, Janet ^a   Lim, Filip ^b   Geschwind, Michael D ^d   Federoff, Howard J ^e   Geller, Alfred I ^c   Hefti, Franz ^a  

^a GENENTECH INC   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^f ILLUMINA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC AMP; BETA GALACTOSIDASE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHLORIDE; CHROMOGRANIN A; COMPLEMENTARY DNA; POTASSIUM CHLORIDE; VIRUS VECTOR;

ANIMAL CELL; ARTICLE; CELL LINE; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPOLARIZATION; FETUS; HERPES SIMPLEX VIRUS; HIPPOCAMPUS; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT; SECRETORY GRANULE;

EID: 0029939502     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0017     Document Type: Article

References (86)

1. Balcarova-Stander, J., Pfeiffer, S. E., Fuller, S. D., and Simons, K. (1984). Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J. 3: 2687-2694.
2. Ballirin, M., Ernfors, P., Lindefors, N., and Persson, H. (1991). Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Exp. Neurol. 114: 35-43.
3. Barde, Y.-A., Edgar, D., and Thoenen, H. (1982). Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1: 549-553.
4. Barde, Y. A. (1989). Trophic factors and neuronal survival. Neuron 2: 1525-1534.
5. Bark, I. C., and Wilson, M. C. (1994). Regulated vesicular fusion in neurons: Snapping together the details. Proc. Natl. Acad. Sci. USA 91: 4621-4624.
6. Bean, A. J., Zhang, X., and Hokfelt, T. (1994). Peptide secretion: what do we know. FASEB J. 8: 630-638.
7. Bernhardt, R., and Matus, A. (1984). Light and electron microscopic studies of the distribution of microtubule-associated prein 2 in rat brain: A difference between dendritic and axonal cytoskeletons. J. Camp. Neurol. 226: 203-221.
8. Blochl, A., and Thoenen, H. (1995). Characterization of Nerve Growth Factor (NGF) Release from Hippocampal Neurons: Evidence for a Constitutive and an Unconventional Sodium-dependent Regulated Pathway. Eur. J. Neurosci. 7: 1220-1228.
9. Blobel, G. (1980). Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA 77: 1496-1500.
10. Burgess, T. L., and Kelly, R. B. (1987). Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3: 243-293.
11. Caceres, A., Banker, G., and Steward, O. (1984). MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. Dev. Brain Res. 13: 314-318.
12. Cameron, P. L., Sudhof, T. C., Jahn, R., and De Camilli, P. (1991). Colocalization of Synaptophysin with transferrin receptors: Implications for synaptic vesicle biogenesis. J. Cell Biol. 115: 151-164.
13. Carroll, R. J., Hammer, R. E., Chan, S. J., Swift, H. H., Rubenstein, A. H., and Steiner, D. F. (1988). A mutant human proinsulin is secreted from the islets of langerhans in increased amounts via an unregulated pathway. Proc. Natl. Acad. Sci. USA 85: 8943-8947.
14. Castren, E., Pitkanen, M., Sirvio, J., Parsadanian, A., Lindholm, D., Thoenen, H., and Riekkinen, P. J. (1993). The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4: 895-898.
15. Craig, A. M., and Banker, G. (1994). Neuronal Polarity. Annu. Rev. Neurosci. 17: 267-310.
16. de Hoop, M. J., and Dotti, C. G. (1993). Membrane traffic in polarized neurons in culture. J. Cell Sci. Suppl. 17: 85-92.
17. Dotti, C. G., Banker, G. A., and Binder, L. I. (1987). The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in situ and in cell culture. Neuroscience 23: 121-130.
18. Dotti, C. G., Sullivan, C. A., and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8: 1454-1468.
19. Dotti, C. G., and Simons, K. (1990). Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell 62: 63-72.
20. Dotti, C. G., Parton, R. G., and Simons, K. (1991). Polarized sorting of glypiated proteins in hippocampal neurons. Nature 349: 158-161.
21. Dotti, C. G., Kartenbeck, J., and Simons, K. (1993). Polarized distribution of the viral glycoproteins of vesicular stomatitis, fowl plague and semliki forest viruses in hippocampal neurons in culture: A light and electron microscopy study. Brain Res. 610: 141-147.
22. Dragunow, M., Beilharz, E., Mason, B., Lawlor, P., Abraham, W., and Gluckman, P. (1993). Brain-derived neurotrophic factor expression after long term potentiation. Neurosci. Lett. 160: 232-236.
23. Dugich-Djordjevic, M. M., Tocco, G., Willoughby, D. A., Najm, I., Pasinetti, G., Thompson, R. F., Boudry, M., Lapchak, P. A., and Hefti, F. (1992). BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron 8: 1127-1138.
24. Dugich-Djordjevic, M. M., Peterson, C., Isono, F., Ohsawa, F., Widmer, H. R., Denton, T. L., Bennett, G. L., and Hefti, F. (1995). Immunohistochemical visualization of Brain-derived neurotrophic factor in the rat brain. Eur. J. Neurosci., in press.
25. Eide, F. F., Lowenstein, D. H., and Reichardt, L. F. (1993). Neurotrophins and their receptors-Current concepts and implications for neurologic disease. Exp. Neurol. 121: 200-214.
26. Ernfors, P., Ibanez, C. F., Ebendal, T., Olson, L., and Persson, H. (1990a). Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: Developmental and topographical expression. Proc. Natl. Acad. Sci. USA 87: 5454-5458.
27. Ernfors, P., Wetmore, C., Olson, L., and Persson, H. (1990b). Identification of cells in the rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5: 511-526.
28. Elferink, L. A., and Scheller, R. H. (1993). Synaptic vesicle proteins and regulated exocytosis. J. Cell Sci. Suppl. 17: 75-79.
29. Faivre-Sairrailh, C., Genneraini, G., Goridis, C., and Rougon, G. (1992). F3/F11 cell surface molecule expression in the developing mouse cerebellum is polarized at synaptic sites and within granule cells. J. Neurosci. 12: 257-267.
30. Feirreira, A., Caceres, A., and Kosik, K. D. (1993). Intraneuronal compartments of the amyloid precursor protein. J. Neurosci. 13: 3112-3123.
31. Friedman, W., Ernfors, P., and Persson, H. (1991a). Transient and persistent expression of NT3/HDNF mRNA in the rat brain during postnatal development. J. Neurosci. 11: 1577-1584.
32. Friedman, W., Olson, L., and Persson, H. (1991b). Cells that express brain-derived neurotrophic factor in the developing postnatal rat brain. Eur. J. Neurosci. 3: 688-697.
33. Garner, C. C., Tucker, R. P., and Matus, A. (1988). Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336: 674-677.
34. Geller, A. I., and Breakefield, X. O. (1988). A defective HSV-1 vector expresses Escherichia Coli beta-galactosidase in cultured peripheral neurons. Science 241: 1667-1669.
35. Geller, A. I., During, M. J., and Neve, R. L. (1991). Molecular analysis of neuronal physiology of gene transfer into neurons with herpes simplex virus vectors. Trends Neurosci. 14: 428-432.
36. Geller, A. I., During, M. J., Haycock, J. W., Freese, A., and Neve, R. (1993). Long-term increases in neurotransmitter release from neuronal cells expressing a constitutive active adenylate cyclase from a Herpes Simplex Virus type 1 vector. Proc. Natl. Acad. Sci. USA 90: 7603-7607.
37. Goodman, L. J., Kain, S. R., and Firestone, G. L. (1993). Trafficking of wild-type and an endoproteolytic-site mutant of the mouse mammary tumor virus glycoprotein. J. Biol. Chem. 268: 2329-2336.
38. German, C. M., Gies, D. R., McCray, G., and Huang, M. (1990). The human cytomegalovirus major immediate early promoter can be trans-activated by adenovirus early proteins. DNA Pro. Eng. Tech. 2: 3-10.
39. Goslin, K., and Banker, G. (1991). Rat hippocampal neurons in low-density culture. In Culturing Nerve Cells (K. Goslin and G. Banker, Eds.), pp. 251-281. MIT Press, Cambridge, MA.
40. Greene, L. A., and Tischler, A. (1976). Establishment of a noadrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73: 2424-2428.
41. Haass, C., Koo, E. H., Teplow, D. B., and Selkoe, D. J. (1994). Polarized secretion of β-amyloid precursor protein and amyloid b-peptide in MDCK cells. Proc. Natl. Acad. Sci. USA 91: 1564-1568.
42. Hefti, F., Denton, T. L., Knusel, B., and Lapchak, P. A. (1993). Neurotrophic factors: What are they and what are they doing? In Neurotrophic Factors (S. E. Loughlin and J. H. Fallon, Eds.) pp. 25-49. Academic Press, San Diego.
43. Hefti, F., Hartikka, J., and Knusel, B. (1989). Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol. Aging 10: 515-533.
44. Hofer, M. M., Pagliusi, S. R., Hohn, A., Leibrock, J., and Barde, Y.-A. (1990). Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 9: 2459-2464.
45. Hohn, A., Leibrock, J., Bailey, K., and Barde, Y.-A. (1990). Identification and characterization of a novel member of the nerve growth factor/ brain-derived neurotrophic factor family. Nature 344: 339-341.
46. Huttner, W. B., Gerdes, H.-H., and Rosa, P. (1991). The Granin (Chromogranin/secretogranin family). Trends Biochem. Sci. 16: 27-30.
47. Ip, N. Y., Li, Y., Yancopoulos, G. D., and Lindsay, R. M. (1993). Cultured hippocampal neurons show responses to BDNF, NT-3 and NT4, but not NGF. J. Neurosci. 13: 3394-3405.
48. Isackson, P. J., Huntsman, M. M., Murray, K. D., and Gall, C. M. (1991). BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: Temporal patterns of induction distinct from NGF. Neuron 6: 937-948.
49. Kang, H., and Schuman, E. M. (1995). Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267: 1658-1662.
50. Kelly, R. (1985). Pathways of protein secretion in eukaryotes. Science 230: 25-32.
51. Kelly, R. (1991). Secretory granule and synaptic vesicle formation. Curr. Opin. Cell Biol. 3: 654-660.
52. Kelly, R. (1993). Storage and release of neurotransmitter. Cell 72: 43-53.
53. Klein, R., Conway, D., Parada, L. F., and Barbacid, M. (1990a). The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61: 647-656.
54. Klein, R., Martin-Zance, D., Barbacid, M., and Parada, L. F. (1990b). Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 109: 845-850.
55. Kobayashi, T., Storrie, B., Simons, K., and Dotti, C. G. (1992). A functional barrier to movement of lipids in polarized neurons. Nature 359: 647-650.
56. Lamballe, F., Klein, R., and Barbacid, M. (1991). TrkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66: 967-979.
57. Lindstedt, A. D., and Kelly, R. B. (1991). Synaptophysin is sorted form endocytic markers in neuroendocrine PC12 cells but not transfected fibroblasts. Neuron 7: 309-317.
58. Maisonpierre, P. C., Belluscio, L., Friedman, B., Alderson, R. F., Wiegand, S. J., Furth, M. E., Lindsay, R. M., and Yancopoulos, B. D. (1990). NT-3, BDNF and NGF in the developing rat nervous system: Parallel as well as reciprocal patterns of expression. Neuron 5: 501-509.
59. McCarthy, A. M., McMahan, L., and Schaffer, P. A. (1989). Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J. Virol. 63: 18-27.
60. Miller, S. G., and Moore, H-P. (1990). Regulated Secretion. Curr. Opin. Cell Biol. 2: 642-647.
61. Moore, H-P., and Kelly, R. B. (1985). Secretory Protein Targeting in a Pituitary Cell line: differential transport of foreign secretory proteins to distinct secretory pathways. J. Cell Biol. 101: 1773-1781.
62. Noel, G., Zollinger, L., Laliberte, F., Rassart, E., Crine, P., and Boileau, G. (1989). Targeting and pressing of pro-opiomelanocortin in neuronal cell line. J. Neurochem. 52: 1050-1057.
63. O'connor, V., Augustine, G. J., and Betz, H. (1994). Synaptic Vesicle Exocytosis: Molecules and models. Cell 76: 785-787.
64. Ohsawa, F., Widmer, H. R., Knusel, B., Denton, T. L., and Hefti, F. (1993). Response of Embryonic rat hippocampal neurons in culture to neurotrophin-3, brain-derived neurotrophic factor and basic fibroblast growth factor. Neuroscience 57: 67-77.
65. Patterson, S. L., Grover, L. M., Schwartzkroin, P. A., and Bothwell, M. (1992). Neurotrophin expression in rat hippocampal slices: A stimulus Paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9: 1081-1088.
66. Peterson, C., Neal, J. H., and Cotman, C. W. (1989). Development of N-methyl-D-aspartate excitotoxicity in cultured hippocampal neurons. Dev. Brain Res. 48: 187-195.
67. Pietrini, B., Matteoli, M., Banker, G., and Caplan, M. J. (1992). Immunolocalization of two Na, K-ATPase isoforms in hippocampal neurons in culture. Proc. Natl. Acad. Sci. USA 89: 8414-8418.
68. Phillips, H. S., Hains, J. M., Laramee, G. R., Rosenthal, A., and Winslow, J. W. (1990). Widespread expression of BDNF but not NTS by target areas of basal forebrain cholinergic neurons. Science 250: 290-292.
69. Powell, S. K., and Rodriguez-Boulan, E. (1992). Polarity of Epithelial and Neuronal Cells. Annu. Rev. Cell Biol. 8: 395-427.
70. Rodriguez-Boulan, E., and Zurzolo, C. (1993). Polarity signals in epithelial cells. J. Cell. Sci. Suppl. 17: 9-12.
71. Sanes, J. R., Rubenstein, J. L. R., and Nicolas, J. F. (1986) Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 5: 3133-3142.
72. Shelton, D. L., Sutherland, J., Gripp, J., Camerato, T., Armanini, M. P., Phillips, H. S., Carroll, K., Spencer, S. D., and Levinson, A. D. (1994). Human trks: Molecular cloning, tissue distribution and expression of extracellular domain immunoadhesions. J. Neurol. 15: 477-491.
73. Smith, S. J., and Augustine, G. J. (1988). Calcium ions, active zones and synaptic transmitter release. Trends Neurosci. 11: 458-464.
74. Smith, I. L., Hardwicke, M. A., and Sandri-Goldin, R. M. (1992). Evidence that the herpes simplex virus immediate early protein ICP27 acts post-transcriptionally during infection to regulate gene expression. Virology 186: 74-86.
75. Snider, W. D. (1994). Functions of the neurotrophins during nervous system development: What are the knockouts are teaching us. Cell 77: 627-638.
76. Spaete, R. R., and Frenkel, N. (1982). The herpes simplex virus amplicon: a new eucaryotic defective virus cloning-amplifying vector. Cell 20: 295-304.
77. Spear, P. G., and Roizman, B. (1981). Herpes simplex viruses, In DNA Tumor Viruses. (J. Tooze, Ed.) pp. 615-746. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
78. Stander, J. B., Pfeiffer, S. E., Fuller, S. D., and Simons, K. (1984). Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. Embo J. 3: 2687-2694.
79. Steward, O. (1994). Dendrites as compartments for macromolecular synthesis. Proc. Natl. Acad. Sci. USA 91: 10766-10768.
80. Stoller, T. J., and Shields, D. (1989). The propeptide of presomatiostatin mediates intracellular transport and secretion of alpha-globin from mammalian cells. J. Cell Biol. 108: 1647-1655.
81. Thoenen, H., Bandtlow, C., and Heumann, R. (1987). The physiological function of nerve growth factor in the central nervous system: Comparison with the periphery. Rev. Physiol. Biochem. Pharmacol. 109: 145-178.
82. Timmusk, T., Belluardo, N., Metsis, M., and Persson, H. (1993). Widespread and developmentally regulated expression of neurotrophin-4 mRNA in rat brain and peripheral tissues. Eur. J. Neurosci. 5: 605-613.
83. Walch-Solimena, C., Takei, K., Marek, K. L., Midyett, K., Sudhof, T. C., De Camilli, P., and Jahn, R. (1993). Synaptotagmin: a membrane constituent of neuropeptide-containing large dense-core vesicles. J. Neurosci. 13: 3895-3903.
84. Wetmore, C., Ernfors, P., Persson, H., and Olson, L. (1990). Localization of brain-derived neurotrophic factor mRNA to neurons in the brain by in situ hybridization. Exp. Neurol. 109: 141-152.
85. Whittmore, S. R., and Seiger, A. (1987). The expression, localization and functional significance of beta-nerve growth factor in the central nervous system. Brain Res. Rev. 12: 439-464.
86. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., and Lindholm, D. (1990). Activity Dependent Regulation of BDNF and NGF mRNAs in the Rat Hippocampus is Mediated by non-NMDA Glutamate Receptors. EMBO J. 9: 3545-3550.