Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons

Journal of Neuroscience

Volumn 19, Issue 6, 1999, Pages 2069-2080

  Mowla, S Javad ^a   Pareek, Sangeeta ^a   Farhadi, Hooman F ^a   Petrecca, Kevin ^b   Fawcett, James P ^a   Seidah, Nabil G ^c   Morris, Stephen J ^a   Sossin, Wayne S ^a   Murphy, Richard A ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

BDNF; Constitutive secretion; Furin; Neurotrophin; NGF; Precursor; Regulated secretion

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FURIN; NERVE GROWTH FACTOR; NEUROTROPHIN; PROTEIN PRECURSOR;

ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ENZYME INACTIVATION; ENZYME INHIBITION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TARGETING; REGULATORY MECHANISM;

EID: 0033559386     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-06-02069.1999     Document Type: Article

References (55)

1. Acheson A, Barker PA, Alderson RF, Miller FD, Murphy RA (1991) Detection of brain-derived ncurotrophic factor-like activity in fibrohlasts and Schwann cells: inhibition by antibodies to NGF. Neuron 7:265-275.
2. Allison J, Malcolm L, Culvenor J, Batholomeusz RK, Holmberg K, Miller JF (1991) Overexpression of β2-microglobulin in transgenic mouse islet β cells results in defective insulin secretion. Proc Natl Acad Sci USA 88:2070-2074.
3. Altar CA, DiStefano PS (1998) Neurotrophin trafficking by antcrograde transport. Trends Neurosci 21:433-437.
4. Altar CA, Cai N. Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wicgand SJ (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856-860.
5. Anderson ED, Thomas L, Hayflick JS, Thomas G (1993) Inhibition of HIV-1 gp160-dependent membrane fusion by a furin-directed α1-antitrypsin variant. J Biol Chem 268:24887-24891.
6. Banker GA, Cowan WM (1977) Rat hippocampyl neurons in dispersed cell culture. Brain Res 126:397-442.
7. Benjannet S. Savaria D, Laslop A. Munzcr JC, Chretien M, Marcinkiewicz M, Seidah NG (1997) α1-antitrypsin Portland inhibits processing of precursors mediated by pro-protein convertases primarily within the constitutive secretory pathway. J Biol Chem 272:26210-26218.
8. Blochl A, Thocnen 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. Brechler V, Chu WN, Baxter JD, Thibault G, Reudelhubcr TL (1996) A protease processing site is essential for prorenin sorting to the regulated secretory pathway. J Biol Chem 271:20636-20640.
10. Bresnahan PA, Leduc R, Thomas L, Thorner J, Gibson HL, Brake AJ, Barr PJ, Thomas G (19911) Human fur gene encodes a yeast KEX2-like cndoprotcasc that cleaves pro-bela-NGF in vivo. J Cell Biol 111:2851-2859.
11. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemcnted Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
12. Bunge RP (1994) The role of the Schwann cell in trophic support and regeneration. J Neurol [Suppl] 242:S19-S21.
13. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243-293.
14. Canossa M, Greisheck O. Berninger B. Campana G, Kolheck R, Thoenen H (1997) Neurotrophin release by neurotrophins: implications for activity-dependent neuronal plasticity. Proc Natl Acad Sci USA 94:13279-13286.
15. Cartwright M. Mikheev AM, Heinrich G (1994) Expression of neurotrophin genes in human fibroblasts: differential regulation of the brainderived neurotrophic factor gene. Int J Dev Neurosci 12:685-693.
16. Conner JM. Lauterborn JC, Van Q, Gall CM, Varon S (1997) Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17:2295-2313.
17. DeCamilli P. Jahn R (1990) Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52:625-645.
18. Dubois CM, Laprise MH, Blanehette F, Gentry LE, Leduc R (1995) Processing of transforming growth factor beta 1 precursor by human furin convertase. J Biol Chem 270:10618-10624.
19. Edwards RH, Selby MJ, Mobley WC, Weinrich SL, Hruby DE, Rutter WJ (1988) Processing and secretion of nerve growth factor: expression in mammalian cells with a vaccinia virus vector. Mol Cell Biol 8:2456-2464.
20. Fawcett JP, Aloyz R, McLean JH, Pareek S, Miller FD, McPherson PS, Murphy RA (1997) Detection of brain-derived neurotrophic factor in a vesicular fraction of brain synaptosomes. J Biol Chem 272:8837-8840.
21. Fawcett JP. Bamji SX, Causing CG, Aloyz R, Ase AR, Reader TA, McLean JH, Miller FD (1998) Functional evidence that BDNF is an anterograde neuronal trophic factor in the CNS. J Neurosci 18:2808-2821.
22. Ghosh A (1996) Cortical development: with an eye on neurotrophins. Curr Biol 6:130-133.
23. Goodman LJ, Valverde J. Lim F, Geschwind MD, Federoff HJ, Geller AI, Hefti F (1996) Regulated release and polarized localization of brain-derived neurotrophie factor in hippocampal neurons. Mol Cell Neurosci 7:222-238.
24. Haubensak W. Narz F. Heumann R, Lessmann V (1998) BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. J Cell Sci 111:1483-1493.
25. Hempstead BL, Rabin SJ, Kaplan L, Reid S, Parada LF, Kaplan DR (1992) Overexpression of the Trk tyrosine kinase rapidly accelerates nerve growth factor-induced differentiation. Neuron 9:883-896.
26. Heymach JJ, Kruttgen A, Suter U, Shooter EM (1996) The regulated secretion and vectorial targeting of neurotrophins in neuroendocrine and epithelial cells. J Biol Chem 271:25430-25437.
27. Hosaka M, Nagahama M, Kim WS, Watanabe T, Hatsuzawa K, Ikemizu J, Murakami K, Nakayama K (1991) Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the constitutive secretory pathway. J Biol Chem 266:12127-12130.
28. Jung LJ, Scheller RH (1991) Peptide processing and targeting in the neuronal secretory pathway. Science 251:1330-1335.
29. Kelly RB, Bucklcy KM, Burgess TL, Carlson SS, Caroni P, Hooper JE, Katzen A, Moore HP, Pfeffer SR, Schroer TA (1983) Membrane traffic in neurons and peptide-sccreling cells. Cold Spring Harbor Symp Quant Biol 2:697-705.
30. Klumperman J, Spijker S, van Minnen J, Sharp-Baker H, Smit AB, Geraerts WP (1996) Cell type-specific sorting of neuropeptides: a mechanism to modulate peptide composition of large dense-core vesicles. J Neurosci 16:7930-7940.
31. Kruttgen A. Moller JC, Heymach JV, Shooter EM (1998) Neurotrophins induce release of neurotrophins by the regulated secretory pathway. Proc Natl Acad Sci USA 95:9614-9619.
32. Loh YP (1993) Mechanisms of intracellular trafficking and processing of proproteins. Boca Raton. FL: CRC.
33. Luzio JP, Brake B, Banting G, Howell KE, Bragetta P, Stanley KK (1990) Identification, sequencing, and expression of an internal membrane protein of the (ram-Golgi network (TGN38). Biochem J 270:97-102.
34. Matlin KS, Simons K (1983) Reduced temperature prevents transfer of a membrane glycoprotcin to the cell surface but does not prevent terminal glycosylation. Cell 34:233-243.
35. Matthews DJ, Goodman LJ, Gorman CM, Wells JA (1994) A survey of furin substrate specificity using substrate phage display. Protein Sci 3:1197-1205.
36. Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Van Q, Priestley JV (1997) Nerve growth factor treatment increases brainderived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 17:8476-8490.
37. Moore HP, Walker MD, Lee F, Kelly RB (1983) Expressing a human proinsulin cDNA in a mouse ACTH-secreting cell. Intraccllular storage, protcolytic processing, and secretion on stimulation. Cell 35:531-538.
38. Mowla SJ, Fawcett JP, Pareek S, Seidah NG, Sossin WS, Murphy RA (1997) Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons. Soc Neurosci Abstr 23:875.10.
39. Murphy RA, Acheson A, Hodges R, Haskins J, Richards C, Reklow E, Chlumecky V, Barker PA, Alderson RF, Lindsay RM (1993) Immunological relationships of NGF, BDNF, and NT-3: recognition and functional inhibition by antibodies to NGF. J Neurosci 13:2853-2862.
40. Oda K, Ikeda M, Tsuji E, Sohda M, Takami N, Misumi Y. Ikehara Y (1991) Sequence requirements for proteolytic cleavage of precursors with paired basic amino acids. Biophys Biochem Res Commun 179:1181-1186.
41. Ogi K, Kimura C, Onda H, Arimura A, Fujimo M (1990) Molecular cloning and characterization of cDNA for the precursor of rat pituitary adenylate cyclic activating polypeptide (PACAP). Biophys Biochem Res Commun 173:1271-1279.
42. Pareek S, Suter U, Snipes GJ, Welcher AA, Shooter EM, Murphy RA (1993) Detection and processing of peripheral myelin protein PMP22 in cultured Schwann cells. J Biol Chem 268:10372-10379.
43. Rouille Y, Duguay SJ, Lund K, Furuta M, Gong O, Lipkind G, Oliva AJ, Chan SJ, Steiner DF (1995) Proteolytic processing mechanisms in the biosynthesis of neuroendocrine peptides: the subtilisin-like proprotein convertases. Front Neuroendocrinol 16:322-361.
44. Seidah NG, Chretien M, Day R (1994) The family of subtilisin/kexinlike proprotein and prohormone convertases: divergent or shared functions. Biochimie 76:197-209.
45. Seidah NG, Benjannet S, Pareek S, Chretien M, Murphy RA (1996a) Cellular processing of the neurotrophin precursors of NT3 and BDNF by the mammalian proprotein convertases. FEBS Lett 379:247-250.
46. Seidah NG, Benjannet S, Pareek S, Savaria D, Hamelin J, Goulet B, Laliberte J, Lazure C, Chretien M, Murphy RA (1996h) Cellular processing of the nerve growth factor precursor by the mammalian pro-protein convertases. Biochem J 314:951-960.
47. Singh N, Birdi TJ, Antia NH (1997) Nerve growth factor production and expression of p75 by Schwann cells and neurofibroblasts in response to M. leprae infection and macrophage secretory products. Neuropathol Appl Neurobiol 23:59-67.
48. Snider WD, Lichtman JW (1996) Are neurotrophins synaptotrophins? Mol Cell Neurosci 7:433-442.
49. Sossin WS, Fisher JM, Scheller RH (1990) Sorting within the regulated secretory pathway occurs in the fram-Golgi network. J Cell Biol 110:1-12.
50. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270:593-598.
51. Vollenweider F, Benjannet S, Decroly E, Savaria D, Lazur C, Thomas G, Chretien M, Seidah NG (1996) Comparative cellular processing of the human immunodeficiency virus (HIV-1) envelope glycoprotein gp160 by the mammalian subtilisin/kexin-like convertases. Biochem J 314:521-532.
52. von Bartheld CS, Byers MR, Williams R, Bothwell M (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing nervous system. Nature 379:830-833.
53. Watanabe M, Hirano A, Stcnglein S, Nelson J, Thomas G, Wong TC (1995) Engineered serine protease inhibitor prevents furin-catalyzed activation of the fusion glycoprotein and production of infectious measles virus. J Virol 69:3206-3210.
54. Yan Q, Rosenfeld RD, Metheson CR, Hawkins N, Lopez OT, Bennett L, Welcher AA (1997) Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 78:431-448.
55. Yanagita M, Nakayama K, Takeuchi T (1992) Processing of mutated proinsulin with tetrabasic cleavage sites to bioactive insulin in the non-endocrine cell line, COS-7. FEBS Lett 311:55-59.