Multiple functions of precursor BDNF to CNS neurons: Negative regulation of neurite growth, spine formation and cell survival

Molecular Brain

Volumn 2, Issue 1, 2009, Pages

  Koshimizu, Hisatsugu ^a   Kiyosue, Kazuyuki ^a   Hara, Tomoko ^a,b   Hazama, Shunsuke ^a,c   Suzuki, Shingo ^a,b   Uegaki, Koichi ^a,b   Nagappan, Guhan ^d   Zaitsev, Eugene ^d   Hirokawa, Takatsugu ^a,b   Tatsu, Yoshiro ^a,b   Ogura, Akihiko ^c   Lu, Bai ^d   Kojima, Masami ^a,b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR PRECURSOR; BRAIN-DERIVED NEUROTROPHIC FACTOR PRECURSOR; MUTANT PROTEIN; POTASSIUM; PROTEIN PRECURSOR; RECOMBINANT PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CELL SECRETION; CELL STRUCTURE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENDRITIC SPINE; FOREBRAIN; GENE EXPRESSION; GENETIC VARIABILITY; GRANULE CELL; HIPPOCAMPUS; HUMAN; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; RAT; SINGLE NUCLEOTIDE POLYMORPHISM; WESTERN BLOTTING; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGY; CELL CULTURE; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; GENETICS; INTRACELLULAR SPACE; METABOLISM; NEURITE; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; SECRETION; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODY SPECIFICITY; APOPTOSIS; BIOLOGICAL TRANSPORT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; COMPUTATIONAL BIOLOGY; CULTURE MEDIA; HIPPOCAMPUS; HUMANS; INTRACELLULAR SPACE; MICE; MUTANT PROTEINS; NEURITES; POLYMORPHISM, SINGLE NUCLEOTIDE; POTASSIUM; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; RATS; RECOMBINANT PROTEINS;

EID: 70349241688     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-2-27     Document Type: Article

References (60)

1. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. M Bibel YA Barde, Genes Dev 2000 14 2919 2937 10.1101/gad.841400 11114882
2. Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. NG Seidah M Chretien, Brain Res 1999 848 45 62 10.1016/S0006-8993(99)01909-5 10701998
3. Neurotrophin-regulated signalling pathways. LF Reichardt, Philos Trans R Soc Lond B Biol Sci 2006 361 1545 1564 10.1098/rstb.2006.1894 16939974
4. Regulation of cell survival by secreted proneurotrophins. R Lee P Kermani KK Teng BL Hempstead, Science 2001 294 1945 1948 10.1126/science.1065057 11729324
5. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. MS Beattie AW Harrington R Lee JY Kim SL Boyce FM Longo JC Bresnahan BL Hempstead SO Yoon, Neuron 2002 36 375 386 10.1016/S0896-6273(02) 01005-X 12408842
6. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. AW Harrington B Leiner C Blechschmitt JC Arevalo R Lee K Morl M Meyer BL Hempstead SO Yoon KM Giehl, Proc Natl Acad Sci USA 2004 101 6226 6230 10.1073/pnas.0305755101 15026568
7. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. HK Teng KK Teng R Lee S Wright S Tevar RD Almeida P Kermani R Torkin ZY Chen FS Lee RT Kraemer A Nykjaer BL Hempstead, J Neurosci 2005 25 5455 5463 10.1523/JNEUROSCI.5123-04.2005 15930396
8. Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. M Volosin W Song RD Almeida DR Kaplan BL Hempstead WJ Friedman, J Neurosci 2006 26 7756 7766 10.1523/JNEUROSCI.1560-06.2006 16855103
9. The many faces of p75NTR. BL Hempstead, Curr Opin Neurobiol 2002 12 260 267 10.1016/S0959-4388(02)00321-5 12049931
10. The yin and yang of neurotrophin action. B Lu PT Pang NH Woo, Nat Rev Neurosci 2005 6 603 614 10.1038/nrn1726 16062169
11. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. T Matsumoto S Rauskolb M Polack J Klose R Kolbeck M Korte YA Barde, Nat Neurosci 2008 11 131 133 10.1038/nn2038 18204444
12. Neuronal release of proBDNF. J Yang CJ Siao G Nagappan T Marinic D Jing K McGrath ZY Chen W Mark L Tessarollo FS Lee B Lu BL Hempstad, Nat Neurosci 2009 12 113 115 10.1038/nn.2244 19136973
13. Whither proBDNF? PA Barker, Nat Neurosci 2009 12 105 106 10.1038/nn0209-105 19172162
14. Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. RS Kenchappa N Zampieri MV Chao PA Barker HK Teng BL Hempstead BD Carter, Neuron 2006 50 219 232 10.1016/j.neuron.2006.03.011 16630834
15. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. NH Woo HK Teng CJ Siao C Chiaruttini PT Pang TA Milner BL Hempstead B Lu, Nat Neurosci 2005 8 1069 1077 10.1038/nn1510 16025106
16. Natively disordered proteins: functions and predictions. P Romero Z Obradovic AK Dunker, Appl Bioinformatics 2004 3 105 113 10.2165/00822942- 200403020-00005 15693736
17. Structure of the brain-derived neurotrophic factor/neurotrophin 3 heterodimer. RC Robinson C Radziejewski DI Stuart EY Jones, Biochemistry 1995 34 4139 4146 10.1021/bi00013a001 7703225
18. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. MF Egan M Kojima JH Callicott TE Goldberg BS Kolachana A Bertolino E Zaitsev B Gold D Goldman M Dean B Lu DR Weinberger, Cell 2003 112 257 269 10.1016/S0092-8674(03)00035-7 12553913
19. Sindbis viral-mediated expression of Ca2+-permeable AMPA receptors at hippocampal CA1 synapses and induction of NMDA receptor-independent long-term potentiation. T Okada N Yamada W Kakegawa K Tsuzuki M Kawamura H Nawa M Iino S Ozawa, Eur J Neurosci 2001 13 1635 1643 10.1046/j.0953-816x.2001.01523.x 11328357
20. Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons. SJ Mowla S Pareek HF Farhadi K Petrecca JP Fawcett NG Seidah SJ Morris WS Sossin RA Murphy, J Neurosci 1999 19 2069 2080 10066260
21. Neurotrophin-3 sorts to the constitutive secretory pathway of hippocampal neurons and is diverted to the regulated secretory pathway by coexpression with brain-derived neurotrophic factor. HF Farhadi SJ Mowla K Petrecca SJ Morris NG Seidah RA Murphy, J Neurosci 2000 20 4059 4068 10818141
22. Method for purifying porcine mature interleukin-18 from silkworm haemolymph. H Nagaya Y Muneta C Enomoto S Matsumoto Y Yokomizo Y Mori, Biotechnol Lett 2004 26 869 873 10.1023/B:bile.0000025894.87314.2d 15269532
23. A new derivatizing agent, trimethylammoniopropyl methanethiosulphonate, is efficient for preparation of recombinant brain-derived neurotrophic factor from inclusion bodies. M Inoue J Akimaru T Nishikawa N Seki H Yamada, Biotechnol Appl Biochem 1998 28 Pt 3 207 213 9799718
24. Neurotrophins and their receptors: a convergence point for many signalling pathways. MV Chao, Nat Rev Neurosci 2003 4 299 309 10.1038/nrn1078 12671646
25. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. SR D'Mello C Galli T Ciotti P Calissano, Proc Natl Acad Sci USA 1993 90 10989 10993 10.1073/pnas.90.23.10989 8248201
26. Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. D Lindholm G Dechant CP Heisenberg H Thoenen, Eur J Neurosci 1993 5 1455 1464 10.1111/j.1460-9568.1993.tb00213.x 7904521
27. Brain-derived neurotrophic factor (BDNF) can prevent apoptosis of rat cerebellar granule neurons in culture. T Kubo T Nonomura Y Enokido H Hatanaka, Brain Res Dev Brain Res 1995 85 249 258 10.1016/0165-3806(94)00220-T 7541321
28. Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. RF Alderson AL Alterman YA Barde RM Lindsay, Neuron 1990 5 297 306 10.1016/0896-6273(90)90166-D 2169269
29. Signaling pathways and survival effects of BDNF and NT-3 on cultured cerebellar granule cells. T Nonomura T Kubo T Oka K Shimoke M Yamada Y Enokido H Hatanaka, Brain Res Dev Brain Res 1996 97 42 50 10.1016/S0165-3806(96)00130-7 8946053
30. Dendritic organization in the neurons of the visual and motor cortices of the cat. DA Sholl, J Anat 1953 87 387 406 13117757
31. Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. M Papa MC Bundman V Greenberger M Segal, J Neurosci 1995 15 1 11 7823120
32. Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Y Ji PT Pang L Feng B Lu, Nat Neurosci 2005 8 164 172 10.1038/nn1381 15665879
33. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. DD Murphy M Segal, J Neurosci 1996 16 4059 4068 8753868
34. Theta stimulation polymerizes actin in dendritic spines of hippocampus. B Lin EA Kramar X Bi FA Brucher CM Gall G Lynch, J Neurosci 2005 25 2062 2069 10.1523/JNEUROSCI.4283-04.2005 15728846
35. p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. S Gehler G Gallo E Veien PC Letourneau, J Neurosci 2004 24 4363 4372 10.1523/JNEUROSCI.0404-04.2004 15128850
36. Beta-amyloid(1-42) induces neuronal death through the p75 neurotrophin receptor. A Sotthibundhu AM Sykes B Fox CK Underwood W Thangnipon EJ Coulson, J Neurosci 2008 28 3941 3946 10.1523/JNEUROSCI.0350-08.2008 18400893
37. Diminished neuronal activity increases neuron-neuron connectivity underlying silent synapse formation and the rapid conversion of silent to functional synapses. K Nakayama K Kiyosue T Taguchi, J Neurosci 2005 25 4040 4051 10.1523/JNEUROSCI.4115-04.2005 15843606
38. Brain-derived neurotrophic factor regulates cholesterol metabolism for synapse development. S Suzuki K Kiyosue S Hazama A Ogura M Kashihara T Hara H Koshimizu M Kojima, J Neurosci 2007 27 6417 6427 10.1523/JNEUROSCI.0690-07.2007 17567802
39. Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. MM Bolton AJ Pittman DC Lo, J Neurosci 2000 20 3221 3232 10777787
40. Activation of pro-BDNF by the pericellular serine protease plasmin. K Gray V Ellis, FEBS Lett 2008 582 907 910 10.1016/j.febslet.2008.02.026 18291105
41. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. K Nakayama, Biochem J 1997 327 Pt 3 625 635 9599222
42. Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. G Nagappan E Zaitsev VV Senatorov Jr J Yang BL Hempstead B Lu, Proc Natl Acad Sci USA 2009 106 1267 1272 10.1073/pnas.0807322106 19147841
43. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. ZY Chen D Jing KG Bath A Ieraci T Khan CJ Siao DG Herrera M Toth C Yang BS McEwen BL Hempstead FS Lee, Science 2006 314 140 143 10.1126/science.1129663 17023662
44. The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. M Zagrebelsky A Holz G Dechant YA Barde T Bonhoeffer M Korte, J Neurosci 2005 25 9989 9999 10.1523/JNEUROSCI.2492- 05.2005 16251447
45. Rap1 is involved in the signal transduction of myelin-associated glycoprotein. J Taniguchi M Fujitani M Endo T Kubo FD Miller DR Kaplan T Yamashita, Cell Death Differ 2008 15 408 419 10.1038/sj.cdd.4402278 18049479
46. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. JJ Zhu Y Qin M Zhao L Van Aelst R Malinow, Cell 2002 110 443 455 10.1016/S0092-8674(02)00897-8 12202034
47. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Q Zhou KJ Homma MM Poo, Neuron 2004 44 749 757 10.1016/j.neuron.2004.11.011 15572107
48. Pro-BDNF-induced synaptic depression and retraction at developing neuromuscular synapses. F Yang HS Je Y Ji G Nagappan B Hempstead B Lu, J Cell Biol 2009 185 727 741 10.1083/jcb.200811147 19451278
49. Development of septal cholinergic neurons in culture: plating density and glial cells modulate effects of NGF on survival, fiber growth, and expression of transmitter-specific enzymes. J Hartikka F Hefti, J Neurosci 1988 8 2967 2985 2842468
50. Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3. B Knusel JW Winslow A Rosenthal LE Burton DP Seid K Nikolics F Hefti, Proc Natl Acad Sci USA 1991 88 961 965 10.1073/pnas.88.3.961 1992488
51. Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. H Khosravani Y Zhang S Tsutsui S Hameed C Altier J Hamid L Chen M Villemaire Z Ali FR Jirik GW Zamponi, J Cell Biol 2008 181 551 565 10.1083/jcb.200711002 18443219
52. BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: roles in synaptic modulation. S Suzuki T Numakawa K Shimazu H Koshimizu T Hara H Hatanaka L Mei B Lu M Kojima, J Cell Biol 2004 167 1205 1215 10.1083/jcb.200404106 15596541
53. Sequence Data Analysis for Long Disordered Regions Prediction in the Calcineurin Family. Romero Obradovic K Dunker, Genome Inform Ser Workshop Genome Inform 1997 8 110 124 11072311
54. Sortilin is essential for proNGF-induced neuronal cell death. A Nykjaer R Lee KK Teng P Jansen P Madsen MS Nielsen C Jacobsen M Kliemannel E Schwarz TE Willnow BL Hempstead CM Petersen, Nature 2004 427 843 848 10.1038/nature02319 14985763
55. Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. H Tago H Kimura T Maeda, J Histochem Cytochem 1986 34 1431 1438 2430009
56. Rapid WAVE dynamics in dendritic spines of cultured hippocampal neurons is mediated by actin polymerization. Y Pilpel M Segal, J Neurochem 2005 95 1401 1410 10.1111/j.1471-4159.2005.03467.x 16190876
57. Single-cell electroporation for gene transfer in vivo. K Haas WC Sin A Javaherian Z Li HT Cline, Neuron 2001 29 583 591 10.1016/S0896-6273(01)00235-5 11301019
58. A simple method for organotypic cultures of nervous tissue. L Stoppini PA Buchs D Muller, J Neurosci Methods 1991 37 173 182 10.1016/0165-0270(91)90128-M 1715499
59. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. SH Shi Y Hayashi RS Petralia SH Zaman RJ Wenthold K Svoboda R Malinow, Science 1999 284 1811 1816 10.1126/science.284.5421.1811 10364548
60. Molecular beacons. W Tan K Wang TJ Drake, Curr Opin Chem Biol 2004 8 547 553 10.1016/j.cbpa.2004.08.010 15450499