ACS Publications. Most Trusted. Most Cited. Most Read
BDNF Induces Widespread Changes in Synaptic Protein Content and Up-Regulates Components of the Translation Machinery:  An Analysis Using High-Throughput Proteomics

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Proteome Res. 2007, 6, 3, 1059-1071
    Article

    BDNF Induces Widespread Changes in Synaptic Protein Content and Up-Regulates Components of the Translation Machinery:  An Analysis Using High-Throughput Proteomics
    Click to copy article linkArticle link copied!

    View Author Information
    Departments of Cell Biology and Neurobiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037
    Other Access OptionsSupporting Information (1)

    Journal of Proteome Research

    Cite this: J. Proteome Res. 2007, 6, 3, 1059–1071
    Click to copy citationCitation copied!
    https://doi.org/10.1021/pr060358f
    Published January 17, 2007
    Copyright © 2007 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    The brain-derived neurotrophic factor (BDNF) plays an important role in neuronal development, and in the formation and plasticity of synaptic connections. These effects of BDNF are at least partially due to the ability of the neurotrophin to increase protein synthesis both globally and locally. However, only a few proteins have been shown to be up-regulated at the synapse by BDNF. Using multidimensional protein identification technology (MudPIT) and relative quantification by spectra counting, we found that several hundred proteins are up-regulated in a synaptoneurosome preparation derived from cultured cortical neurons that were treated with BDNF. These proteins fall into diverse functional categories, including those involved in synaptic vesicle formation and movement, maintenance or remodeling of synaptic structure, mRNA processing, transcription, and translation. A number of translation factors, ribosomal proteins, and tRNA synthetases were rapidly up-regulated by BDNF. This up-regulation of translation components was sensitive to protein synthesis inhibitors and dependent on the activation of the mammalian target of rapamycin (mTOR), a regulator of cap-dependent mRNA translation. The presence of a subset of these proteins and their mRNAs in neuronal processes was corroborated by immunocytochemistry and in situ hybridization, and their up-regulation was confirmed by Western blotting. The data demonstrate that BDNF increases the synthesis of a wide variety of synaptic proteins and suggest that the neurotrophin may enhance the translational capacity of synapses.

    Keywords: BDNF • translation • synapse • MudPIT • spectra count • protein quantification • synaptoneurosomes • ribosomal proteins

    Copyright © 2007 American Chemical Society

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    †

     Department of Cell Biology, The Scripps Research Institute.

    ‡

     Department of Neurobiology, The Scripps Research Institute.

    *

     To whom correspondence should be addressed. E-mails:  John R. Yates III, [email protected]; Peter Vanderklish, [email protected].

    Supporting Information Available

    Click to copy section linkSection link copied!

    Proteins found to be up- or down-regulated in SNS by BDNF were listed in Table S1. The pathways or groups of proteins up-regulated with a confidence level of over 95% are listed in Table S2. This material is available free of charge via the Internet at http://pubs.acs.org.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 94 publications.

    1. Wenchang Chang, Dawei Huang, Y. Martin Lo, Qinqiao Tee, Poling Kuo, James Swibea Wu, Wenchung Huang, Szuchuan Shen. Protective Effect of Caffeic Acid against Alzheimer’s Disease Pathogenesis via Modulating Cerebral Insulin Signaling, β-Amyloid Accumulation, and Synaptic Plasticity in Hyperinsulinemic Rats. Journal of Agricultural and Food Chemistry 2019, 67 (27) , 7684-7693. https://doi.org/10.1021/acs.jafc.9b02078
    2. Ya-Juan Wang, Dong-Yun Han, Tracy Tabib, John R. Yates, III, and Ting-Wei Mu . Identification of GABAC Receptor Protein Homeostasis Network Components from Three Tandem Mass Spectrometry Proteomics Approaches. Journal of Proteome Research 2013, 12 (12) , 5570-5586. https://doi.org/10.1021/pr400535z
    3. Bruno Manadas, Ana Rita Santos, Krisztina Szabadfi, João R. Gomes, Spiros D. Garbis, Michael Fountoulakis and Carlos B. Duarte . BDNF-Induced Changes in the Expression of the Translation Machinery in Hippocampal Neurons: Protein Levels and Dendritic mRNA. Journal of Proteome Research 2009, 8 (10) , 4536-4552. https://doi.org/10.1021/pr900366x
    4. Waleed ElGrawani, Guanhua Sun, Fabian P. Kliem, Simon Sennhauser, Sara Pierre-Ferrer, Alex Rosi-Andersen, Ida Boccalaro, Philipp Bethge, Won Do Heo, Fritjof Helmchen, Antoine R. Adamantidis, Daniel B. Forger, Maria S. Robles, Steven A. Brown. BDNF-TrkB signaling orchestrates the buildup process of local sleep. Cell Reports 2024, 43 (7) , 114500. https://doi.org/10.1016/j.celrep.2024.114500
    5. Caroline Brandão-Teles, André S. L. M. Antunes, Talita Aparecida de Moraes Vrechi, Daniel Martins-de-Souza. The Roles of hnRNP Family in the Brain and Brain-Related Disorders. Molecular Neurobiology 2024, 61 (6) , 3578-3595. https://doi.org/10.1007/s12035-023-03747-4
    6. Theresa Harvey, Maribel Rios. The Role of BDNF and TrkB in the Central Control of Energy and Glucose Balance: An Update. Biomolecules 2024, 14 (4) , 424. https://doi.org/10.3390/biom14040424
    7. Alan Jung Park. PKA Anchoring and Synaptic Tagging and Capture. 2024, 121-141. https://doi.org/10.1007/978-3-031-54864-2_6
    8. Sofia Elisa Alzuri, Nicolás Matías Rosas, Natasa Hlavacova, Daniela Jezova, Beata Fuchsova. Role of miR ‐124‐3p in regulatory mechanisms of Gpm6a expression in the hippocampus of chronically stressed rats. Journal of Neurochemistry 2023, 165 (4) , 603-621. https://doi.org/10.1111/jnc.15810
    9. Megha Jhanji, Chintada Nageswara Rao, Jacob C. Massey, Marion C. Hope, Xueyan Zhou, C. Dirk Keene, Tao Ma, Michael D. Wyatt, Jason A. Stewart, Mathew Sajish. Cis- and trans-resveratrol have opposite effects on histone serine-ADP-ribosylation and tyrosine induced neurodegeneration. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-30785-8
    10. Rui O. Costa, Luís F. Martins, Emanuel Tahiri, Carlos B. Duarte. Brain‐derived neurotrophic factor ‐induced regulation of RNA metabolism in neuronal development and synaptic plasticity. WIREs RNA 2022, 13 (5) https://doi.org/10.1002/wrna.1713
    11. Elisa Maffioli, Elisa Angiulli, Simona Nonnis, Francesca Grassi Scalvini, Armando Negri, Gabriella Tedeschi, Ivan Arisi, Flavia Frabetti, Salvatore D’Aniello, Enrico Alleva, Carla Cioni, Mattia Toni. Brain Proteome and Behavioural Analysis in Wild Type, BDNF+/− and BDNF−/− Adult Zebrafish (Danio rerio) Exposed to Two Different Temperatures. International Journal of Molecular Sciences 2022, 23 (10) , 5606. https://doi.org/10.3390/ijms23105606
    12. Rasa Saenno, Oabnithi Dornlakorn, Tanaporn Anosri, Soraya Kaewngam, Apiwat Sirichoat, Anusara Aranarochana, Wanassanun Pannangrong, Peter Wigmore, Jariya Umka Welbat. Caffeic Acid Alleviates Memory and Hippocampal Neurogenesis Deficits in Aging Rats Induced by D-Galactose. Nutrients 2022, 14 (10) , 2169. https://doi.org/10.3390/nu14102169
    13. Mohammad Zaki Bin Ibrahim, Amrita Benoy, Sreedharan Sajikumar. Long‐term plasticity in the hippocampus: maintaining within and ‘tagging’ between synapses. The FEBS Journal 2022, 289 (8) , 2176-2201. https://doi.org/10.1111/febs.16065
    14. Michael Feyder, Carina Plewnia, Ori J. Lieberman, Giada Spigolon, Alessandro Piccin, Lidia Urbina, Benjamin Dehay, Qin Li, Per Nilsson, Mikael Altun, Emanuela Santini, David Sulzer, Erwan Bezard, Anders Borgkvist, Gilberto Fisone. Involvement of Autophagy in Levodopa‐Induced Dyskinesia. Movement Disorders 2021, 36 (5) , 1137-1146. https://doi.org/10.1002/mds.28480
    15. Artem P. Gureev, Vasily N. Popov, Anatoly A. Starkov. Crosstalk between the mTOR and Nrf2/ARE signaling pathways as a target in the improvement of long-term potentiation. Experimental Neurology 2020, 328 , 113285. https://doi.org/10.1016/j.expneurol.2020.113285
    16. Hao Wu, Jing Zhou, Tianhui Zhu, Ivan Cohen, Jason Dictenberg. A kinesin adapter directly mediates dendritic mRNA localization during neural development in mice. Journal of Biological Chemistry 2020, 295 (19) , 6605-6628. https://doi.org/10.1074/jbc.RA118.005616
    17. Yuta Ishizuka, Clive R. Bramham. A simple DMSO-based method for cryopreservation of primary hippocampal and cortical neurons. Journal of Neuroscience Methods 2020, 333 , 108578. https://doi.org/10.1016/j.jneumeth.2019.108578
    18. Freddy Jeanneteau, Margarita Arango-Lievano, Moses V. Chao. Neurotrophin and synaptogenesis. 2020, 167-192. https://doi.org/10.1016/B978-0-12-823672-7.00007-7
    19. Araceli Martínez-Moreno, Alejandro Rivera-Olvera, Martha L. Escobar. BDNF induces in vivo long-lasting enhancement of synaptic transmission and structural reorganization at the hippocampal mossy fibers in a transcription and translation-independent manner. Neurobiology of Learning and Memory 2020, 167 , 107125. https://doi.org/10.1016/j.nlm.2019.107125
    20. Natalie M. Clark, Zhouxin Shen, Steven P. Briggs, Justin W. Walley, Dior R. Kelley. Auxin Induces Widespread Proteome Remodeling in Arabidopsis Seedlings. PROTEOMICS 2019, 19 (17) https://doi.org/10.1002/pmic.201900199
    21. Hyungju Park, Bong-Kiun Kaang. Balanced actions of protein synthesis and degradation in memory formation. Learning & Memory 2019, 26 (9) , 299-306. https://doi.org/10.1101/lm.048785.118
    22. Ekaterina Eremenko, Kritika Mittal, Omer Berner, Nikita Kamenetsky, Anna Nemirovsky, Yehezqel Elyahu, Alon Monsonego. BDNF-producing, amyloid β-specific CD4 T cells as targeted drug-delivery vehicles in Alzheimer's disease. EBioMedicine 2019, 43 , 424-434. https://doi.org/10.1016/j.ebiom.2019.04.019
    23. D. Luke Fischer, Caryl E. Sortwell. BDNF provides many routes toward STN DBS‐mediated disease modification. Movement Disorders 2019, 34 (1) , 22-34. https://doi.org/10.1002/mds.27535
    24. Heather L. Bowling, Shruti Nayak, Katrin Deinhardt. Proteomic Approaches to Dissect Neuronal Signalling Pathways. 2019, 469-475. https://doi.org/10.1007/978-3-030-15950-4_27
    25. Dorit Ron, Anthony Berger. Targeting the intracellular signaling “STOP” and “GO” pathways for the treatment of alcohol use disorders. Psychopharmacology 2018, 235 (6) , 1727-1743. https://doi.org/10.1007/s00213-018-4882-z
    26. Di Yun, Yinghan Zhuang, Michael R. Kreutz, Thomas Behnisch. The role of 19S proteasome associated deubiquitinases in activity-dependent hippocampal synaptic plasticity. Neuropharmacology 2018, 133 , 354-365. https://doi.org/10.1016/j.neuropharm.2018.01.043
    27. Han-Hsuan Liu, Daniel B McClatchy, Lucio Schiapparelli, Wanhua Shen, John R Yates, Hollis T Cline. Role of the visual experience-dependent nascent proteome in neuronal plasticity. eLife 2018, 7 https://doi.org/10.7554/eLife.33420
    28. N. C. Tikhonov, G. P. Plotnikov, V. V. Krasnov, E. V. Grigoryev, D. L. Shukevich. Pharmacological neuroprotection for intracerebral hemorrhages in patients with polyvascular disease. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova 2018, 118 (12) , 19. https://doi.org/10.17116/jnevro201811812119
    29. Graciano Leal, Diogo Comprido, Pasqualino de Luca, Eduardo Morais, Luís Rodrigues, Miranda Mele, Ana R. Santos, Rui O. Costa, Maria Joana Pinto, Sudarshan Patil, Birgitte Berentsen, Pedro Afonso, Laura Carreto, Ka Wan Li, Paulo Pinheiro, Ramiro D. Almeida, Manuel A. S. Santos, Clive R. Bramham, Carlos B. Duarte. The RNA-Binding Protein hnRNP K Mediates the Effect of BDNF on Dendritic mRNA Metabolism and Regulates Synaptic NMDA Receptors in Hippocampal Neurons. eneuro 2017, 4 (6) , ENEURO.0268-17.2017. https://doi.org/10.1523/ENEURO.0268-17.2017
    30. Andressa Radiske, Janine I. Rossato, Maria Carolina Gonzalez, Cristiano A. Köhler, Lia R. Bevilaqua, Martín Cammarota. BDNF controls object recognition memory reconsolidation. Neurobiology of Learning and Memory 2017, 142 , 79-84. https://doi.org/10.1016/j.nlm.2017.02.018
    31. Farr Niere, Kimberly F. Raab-Graham. mTORC1 Is a Local, Postsynaptic Voltage Sensor Regulated by Positive and Negative Feedback Pathways. Frontiers in Cellular Neuroscience 2017, 11 https://doi.org/10.3389/fncel.2017.00152
    32. Md. Abdul Hannan, Md. Mohibbullah, Yong-Ki Hong, Il Soo Moon. Proteomic Analysis of the Neurotrophic Effect of Gelidium amansii in Primary Cultured Neurons. Journal of Medicinal Food 2017, 20 (3) , 279-287. https://doi.org/10.1089/jmf.2016.3848
    33. Debabrata Panja, Clive R. Bramham. BDNF Function in Long-Term Synaptic Plasticity in the Dentate Gyrus In Vivo: Methods for Local Drug Delivery and Biochemical Analysis of Translation. 2017, 241-256. https://doi.org/10.1007/7657_2017_7
    34. Paul E. Gold. Protein Synthesis and Memory. 2017, 293-310. https://doi.org/10.1016/B978-0-12-809324-5.21119-X
    35. G. Leal, C.R. Bramham, C.B. Duarte. BDNF and Hippocampal Synaptic Plasticity. 2017, 153-195. https://doi.org/10.1016/bs.vh.2016.10.004
    36. Y.-H. Shih, S.-F. Tsai, S.-H. Huang, Y.-T. Chiang, M.W. Hughes, S.-Y. Wu, C.-W. Lee, T.-T. Yang, Y.-M. Kuo. Hypertension impairs hippocampus-related adult neurogenesis, CA1 neuron dendritic arborization and long-term memory. Neuroscience 2016, 322 , 346-357. https://doi.org/10.1016/j.neuroscience.2016.02.045
    37. Yiwen Wang, Limei Chen, Yu Gao, Yan Zhang, Caifeng Wang, Yijun Zhou, Yi Hu, Rong Shi, Ying Tian. Effects of prenatal exposure to cadmium on neurodevelopment of infants in Shandong, China. Environmental Pollution 2016, 211 , 67-73. https://doi.org/10.1016/j.envpol.2015.12.038
    38. Daniela C. Dieterich, Michael R. Kreutz. Proteomics of the Synapse – A Quantitative Approach to Neuronal Plasticity. Molecular & Cellular Proteomics 2016, 15 (2) , 368-381. https://doi.org/10.1074/mcp.R115.051482
    39. Alexandra M. Amen, Daniel L. Pham, Mollie K. Meffert. Post-transcriptional Regulation by Brain-Derived Neurotrophic Factor in the Nervous System. 2016, 315-337. https://doi.org/10.1007/978-3-319-25124-0_14
    40. Osamu Nakagawasai, Wataru Nemoto, Hiroshi Onogi, Takahiro Moriya, Jia-Rong Lin, Takayo Odaira, Fukie Yaoita, Takumi Ogawa, Kiminori Ohta, Yasuyuki Endo, Koichi Tan-No. BE360, a new selective estrogen receptor modulator, produces antidepressant and antidementia effects through the enhancement of hippocampal cell proliferation in olfactory bulbectomized mice. Behavioural Brain Research 2016, 297 , 315-322. https://doi.org/10.1016/j.bbr.2015.10.033
    41. Heather Bowling, Aditi Bhattacharya, Guoan Zhang, Joseph Z. Lebowitz, Danyal Alam, Peter T. Smith, Kent Kirshenbaum, Thomas A. Neubert, Christine Vogel, Moses V. Chao, Eric Klann. BONLAC: A combinatorial proteomic technique to measure stimulus-induced translational profiles in brain slices. Neuropharmacology 2016, 100 , 76-89. https://doi.org/10.1016/j.neuropharm.2015.07.017
    42. N. M. Rzaeva. Hypothalamic regulation of retinal function. Vestnik oftal'mologii 2016, 132 (3) , 32. https://doi.org/10.17116/oftalma2016132332-36
    43. I. M. Kornilovskiy, A. I. Sultanova, A. A. Burtsev. Riboflavin photo­protection with cross-linking effect in photorefractive ablation of the cornea. Vestnik oftal'mologii 2016, 132 (3) , 37. https://doi.org/10.17116/oftalma2016132337-41
    44. Heather Bowling, Aditi Bhattacharya, Eric Klann, MosesV Chao. Deconstructing brain-derived neurotrophic factor actions in adult brain circuits to bridge an existing informational gap in neuro-cell biology. Neural Regeneration Research 2016, 11 (3) , 363. https://doi.org/10.4103/1673-5374.179031
    45. Graciano Leal, Pedro M. Afonso, Ivan L. Salazar, Carlos B. Duarte. Regulation of hippocampal synaptic plasticity by BDNF. Brain Research 2015, 1621 , 82-101. https://doi.org/10.1016/j.brainres.2014.10.019
    46. Ana Rita Santos, Miranda Mele, Sandra H. Vaz, Blanka Kellermayer, Maddalena Grimaldi, Mariana Colino-Oliveira, Diogo M. Rombo, Diogo Comprido, Ana M. Sebastião, Carlos B. Duarte. Differential Role of the Proteasome in the Early and Late Phases of BDNF-Induced Facilitation of LTP. The Journal of Neuroscience 2015, 35 (8) , 3319-3329. https://doi.org/10.1523/JNEUROSCI.4521-14.2015
    47. Maja Genheden, Justin W. Kenney, Harvey E. Johnston, Antigoni Manousopoulou, Spiros D. Garbis, Christopher G. Proud. BDNF Stimulation of Protein Synthesis in Cortical Neurons Requires the MAP Kinase-Interacting Kinase MNK1. The Journal of Neuroscience 2015, 35 (3) , 972-984. https://doi.org/10.1523/JNEUROSCI.2641-14.2015
    48. Alan Jung Park, Ted Abel. PKA Anchoring and Synaptic Tagging and Capture. 2015, 61-78. https://doi.org/10.1007/978-1-4939-1761-7_5
    49. Ru-Jing Ren, Eric B Dammer, Gang Wang, Nicholas T Seyfried, Allan I Levey. Proteomics of protein post-translational modifications implicated in neurodegeneration. Translational Neurodegeneration 2014, 3 (1) https://doi.org/10.1186/2047-9158-3-23
    50. Jeremie Neasta, Segev Barak, Sami Ben Hamida, Dorit Ron. mTOR complex 1: a key player in neuroadaptations induced by drugs of abuse. Journal of Neurochemistry 2014, 130 (2) , 172-184. https://doi.org/10.1111/jnc.12725
    51. Nobuyuki Takei, Hiroyuki Nawa. mTOR signaling and its roles in normal and abnormal brain development. Frontiers in Molecular Neuroscience 2014, 7 https://doi.org/10.3389/fnmol.2014.00028
    52. O. A. Gomazkov. Neurogenesis as an adaptive function of the adult brain. Biology Bulletin Reviews 2014, 4 (2) , 86-100. https://doi.org/10.1134/S2079086414020029
    53. Heather L. Bowling, Katrin Deinhardt. Proteomic Approaches to Dissect Neuronal Signaling Pathways. 2014, 499-508. https://doi.org/10.1007/978-3-319-06068-2_24
    54. Graciano Leal, Diogo Comprido, Carlos B. Duarte. BDNF-induced local protein synthesis and synaptic plasticity. Neuropharmacology 2014, 76 , 639-656. https://doi.org/10.1016/j.neuropharm.2013.04.005
    55. Pedro Bekinschtein, Martin Cammarota, Jorge H. Medina. BDNF and memory processing. Neuropharmacology 2014, 76 , 677-683. https://doi.org/10.1016/j.neuropharm.2013.04.024
    56. Claudia R. Ruiz, Jay Shi, Mollie K. Meffert. Transcript specificity in BDNF-regulated protein synthesis. Neuropharmacology 2014, 76 , 657-663. https://doi.org/10.1016/j.neuropharm.2013.05.004
    57. O. A. Gomazkov. Signaling molecules as regulators of neurogenesis in the adult brain. Neurochemical Journal 2013, 7 (4) , 241-255. https://doi.org/10.1134/S1819712413040041
    58. Rebecca M Ring, Ciaran M Regan. Captodiamine, a putative antidepressant, enhances hypothalamic BDNF expression in vivo by synergistic 5-HT 2c receptor antagonism and sigma-1 receptor agonism. Journal of Psychopharmacology 2013, 27 (10) , 930-939. https://doi.org/10.1177/0269881113497614
    59. Jordi Blanco, Miquel Mulero, Luis Heredia, Andreu Pujol, José L. Domingo, Domènec J. Sánchez. Perinatal exposure to BDE-99 causes learning disorders and decreases serum thyroid hormone levels and BDNF gene expression in hippocampus in rat offspring. Toxicology 2013, 308 , 122-128. https://doi.org/10.1016/j.tox.2013.03.010
    60. Yeonju Lee, Jieun Kim, Soyong Jang, Seikwan Oh. Administration of Phytoceramide Enhances Memory and Up-regulates the Expression of pCREB and BDNF in Hippocampus of Mice. Biomolecules and Therapeutics 2013, 21 (3) , 229-233. https://doi.org/10.4062/biomolther.2013.002
    61. Derrick Sek Tong Ong, Ya-Juan Wang, Yun Lei Tan, John R. Yates, Ting-Wei Mu, Jeffery W. Kelly. FKBP10 Depletion Enhances Glucocerebrosidase Proteostasis in Gaucher Disease Fibroblasts. Chemistry & Biology 2013, 20 (3) , 403-415. https://doi.org/10.1016/j.chembiol.2012.11.014
    62. Margaret T. Butko, Jeffrey N. Savas, Beth Friedman, Claire Delahunty, Ford Ebner, John R. Yates, Roger Y. Tsien. In vivo quantitative proteomics of somatosensory cortical synapses shows which protein levels are modulated by sensory deprivation. Proceedings of the National Academy of Sciences 2013, 110 (8) https://doi.org/10.1073/pnas.1300424110
    63. Maribel Rios. BDNF and the central control of feeding: accidental bystander or essential player?. Trends in Neurosciences 2013, 36 (2) , 83-90. https://doi.org/10.1016/j.tins.2012.12.009
    64. F. Jeanneteau, M.V. Chao. Neurotrophins and Synaptogenesis. 2013, 639-658. https://doi.org/10.1016/B978-0-12-397266-8.00107-1
    65. O. A. Gomazkov. Neurotrophins: The therapeutic potential and concept of minipeptides. Neurochemical Journal 2012, 6 (3) , 163-172. https://doi.org/10.1134/S1819712412030075
    66. Kristy L. Townsend, Ryo Suzuki, Tian Lian Huang, Enxuan Jing, Tim J. Schulz, Kevin Lee, Cullen M. Taniguchi, Daniel O. Espinoza, Lindsay E. McDougall, Hongbin Zhang, Tong‐Chuan He, Efi Kokkotou, Yu‐Hua Tseng. Bone morphogenetic protein 7 (BMP7) reverses obesity and regulates appetite through a central mTOR pathway. The FASEB Journal 2012, 26 (5) , 2187-2196. https://doi.org/10.1096/fj.11-199067
    67. Tzu-Wei Lin, Shean-Jen Chen, Tung-Yi Huang, Chia-Yuan Chang, Jih-Ing Chuang, Fong-Sen Wu, Yu-Min Kuo, Chauying J. Jen. Different types of exercise induce differential effects on neuronal adaptations and memory performance. Neurobiology of Learning and Memory 2012, 97 (1) , 140-147. https://doi.org/10.1016/j.nlm.2011.10.006
    68. Margaret Labban, Wayne S. Sossin. Translation of 5′ terminal oligopyrimidine tract (5′TOP) mRNAs in Aplysia Californica is regulated by the target of rapamycin (TOR). Biochemical and Biophysical Research Communications 2011, 404 (3) , 816-821. https://doi.org/10.1016/j.bbrc.2010.12.066
    69. Roger L. Redondo, Richard G. M. Morris. Making memories last: the synaptic tagging and capture hypothesis. Nature Reviews Neuroscience 2011, 12 (1) , 17-30. https://doi.org/10.1038/nrn2963
    70. María Moreno-Igoa, Raquel Manzano, Sara Oliván, Ana C Calvo, Janne M Toivonen, Rosario Osta. Effects of gene therapy on muscle 18S rRNA expression in mouse model of ALS. BMC Research Notes 2010, 3 (1) https://doi.org/10.1186/1756-0500-3-275
    71. Philip A Robinson. Understanding the molecular basis of Parkinson’s disease, identification of biomarkers and routes to therapy. Expert Review of Proteomics 2010, 7 (4) , 565-578. https://doi.org/10.1586/epr.10.40
    72. Daniela C Dieterich, Jennifer J L Hodas, Géraldine Gouzer, Ilya Y Shadrin, John T Ngo, Antoine Triller, David A Tirrell, Erin M Schuman. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nature Neuroscience 2010, 13 (7) , 897-905. https://doi.org/10.1038/nn.2580
    73. B.J. Casey, Fatima Soliman, Kevin G. Bath, Charles E. Glatt. Imaging genetics and development: Challenges and promises. Human Brain Mapping 2010, 31 (6) , 838-851. https://doi.org/10.1002/hbm.21047
    74. Se Jin Park, Dong Hyun Park, Dong Hyun Kim, Seungjoo Lee, Byung Hoon Yoon, Won Yong Jung, Kyung Tae Lee, Jae Hoon Cheong, Jong Hoon Ryu. The memory-enhancing effects of Euphoria longan fruit extract in mice. Journal of Ethnopharmacology 2010, 128 (1) , 160-165. https://doi.org/10.1016/j.jep.2010.01.001
    75. Clive R. Bramham, Maria N. Alme, Margarethe Bittins, Sjoukje D. Kuipers, Rajeevkumar R. Nair, Balagopal Pai, Debabrata Panja, Manja Schubert, Jonathan Soule, Adrian Tiron, Karin Wibrand. The Arc of synaptic memory. Experimental Brain Research 2010, 200 (2) , 125-140. https://doi.org/10.1007/s00221-009-1959-2
    76. B.J. Casey, C.E. Glatt, N. Tottenham, F. Soliman, K. Bath, D. Amso, M. Altemus, S. Pattwell, R. Jones, L. Levita, B. McEwen, A.M. Magariños, M. Gunnar, K.M. Thomas, J. Mezey, A.G. Clark, B.L. Hempstead, F.S. Lee. Brain-derived neurotrophic factor as a model system for examining gene by environment interactions across development. Neuroscience 2009, 164 (1) , 108-120. https://doi.org/10.1016/j.neuroscience.2009.03.081
    77. Debabrata Panja, Girstaute Dagyte, Michael Bidinosti, Karin Wibrand, Åse-Marit Kristiansen, Nahum Sonenberg, Clive R. Bramham. Novel Translational Control in Arc-dependent Long Term Potentiation Consolidation in Vivo. Journal of Biological Chemistry 2009, 284 (46) , 31498-31511. https://doi.org/10.1074/jbc.M109.056077
    78. Qi Li, Jaimei Liu, Michael Michaud, Michael L. Schwartz, Joseph A. Madri. Strain Differences in Behavioral and Cellular Responses to Perinatal Hypoxia and Relationships to Neural Stem Cell Survival and Self-Renewal. The American Journal of Pathology 2009, 175 (5) , 2133-2145. https://doi.org/10.2353/ajpath.2009.090354
    79. Beulah Leitch, Olga Shevtsova, John Richard Kerr. Selective reduction in synaptic proteins involved in vesicle docking and signalling at synapses in the ataxic mutant mouse stargazer. Journal of Comparative Neurology 2009, 512 (1) , 52-73. https://doi.org/10.1002/cne.21890
    80. Barry B. Kaplan, Anthony E. Gioio, Mi Hillefors, Armaz Aschrafi. Axonal Protein Synthesis and the Regulation of Local Mitochondrial Function. 2009, 1-25. https://doi.org/10.1007/400_2009_1
    81. Mauro Costa-Mattioli, Wayne S. Sossin, Eric Klann, Nahum Sonenberg. Translational Control of Long-Lasting Synaptic Plasticity and Memory. Neuron 2009, 61 (1) , 10-26. https://doi.org/10.1016/j.neuron.2008.10.055
    82. Pierluigi Mauri, Michaela Scigelova. Multidimensional protein identification technology for clinical proteomic analysis. Clinical Chemistry and Laboratory Medicine 2009, 47 (6) https://doi.org/10.1515/CCLM.2009.165
    83. Ting-Wei Mu, Derrick Sek Tong Ong, Ya-Juan Wang, William E. Balch, John R. Yates, Laura Segatori, Jeffery W. Kelly. Chemical and Biological Approaches Synergize to Ameliorate Protein-Folding Diseases. Cell 2008, 134 (5) , 769-781. https://doi.org/10.1016/j.cell.2008.06.037
    84. Li-Jun Zhou, Yi Zhong, Wen-Jie Ren, Yong-Yong Li, Tong Zhang, Xian-Guo Liu. BDNF induces late-phase LTP of C-fiber evoked field potentials in rat spinal dorsal horn. Experimental Neurology 2008, 212 (2) , 507-514. https://doi.org/10.1016/j.expneurol.2008.04.034
    85. Delphine Gobert, Lisa Topolnik, Mounia Azzi, Linda Huang, Frédérique Badeaux, Luc DesGroseillers, Wayne S. Sossin, Jean‐Claude Lacaille. Forskolin induction of late‐LTP and up‐regulation of 5′ TOP mRNAs translation via mTOR, ERK, and PI3K in hippocampal pyramidal cells. Journal of Neurochemistry 2008, 106 (3) , 1160-1174. https://doi.org/10.1111/j.1471-4159.2008.05470.x
    86. Solenne Chardonnet, Pierre Le Marechal, Hélène Cheval, Jean‐Pierre Le Caer, Paulette Decottignies, Olivier Laprevote, Serge Laroche, Sabrina Davis. Large‐scale study of phosphoproteins involved in long‐term potentiation in the rat dentate gyrus in vivo. European Journal of Neuroscience 2008, 27 (11) , 2985-2998. https://doi.org/10.1111/j.1460-9568.2008.06280.x
    87. Vivian Hook, Shin‐Rong Hwang, Jill Wegrzyn, Steven Bark. Neuropeptides: Chemical Activity Profiling and Proteomic Approaches. 2008, 1-13. https://doi.org/10.1002/9780470048672.wecb381
    88. Pedro Bekinschtein, Martin Cammarota, Ivan Izquierdo, Jorge H. Medina. Reviews: BDNF and Memory Formation and Storage. The Neuroscientist 2008, 14 (2) , 147-156. https://doi.org/10.1177/1073858407305850
    89. Wickliffe C. Abraham, Joanna M. Williams. LTP maintenance and its protein synthesis-dependence. Neurobiology of Learning and Memory 2008, 89 (3) , 260-268. https://doi.org/10.1016/j.nlm.2007.10.001
    90. Vivian Hook, Lydiane Funkelstein, Douglas Lu, Steven Bark, Jill Wegrzyn, Shin-Rong Hwang. Proteases for Processing Proneuropeptides into Peptide Neurotransmitters and Hormones. Annual Review of Pharmacology and Toxicology 2008, 48 (1) , 393-423. https://doi.org/10.1146/annurev.pharmtox.48.113006.094812
    91. Joanna M. Williams, Diane Guévremont, Sara E. Mason-Parker, Carthika Luxmanan, Warren P. Tate, Wickliffe C. Abraham. Differential Trafficking of AMPA and NMDA Receptors during Long-Term Potentiation in Awake Adult Animals. The Journal of Neuroscience 2007, 27 (51) , 14171-14178. https://doi.org/10.1523/JNEUROSCI.2348-07.2007
    92. Ka Wan Li, August B. Smit. Proteomics of brain synapses and molecular dissection of synaptic subdomains. PROTEOMICS – Clinical Applications 2007, 1 (11) , 1476-1484. https://doi.org/10.1002/prca.200700328
    93. Clive R. Bramham, David G. Wells. Dendritic mRNA: transport, translation and function. Nature Reviews Neuroscience 2007, 8 (10) , 776-789. https://doi.org/10.1038/nrn2150
    94. Paul A. Haynes, Thomas H. Roberts. Subcellular shotgun proteomics in plants: Looking beyond the usual suspects. PROTEOMICS 2007, 7 (16) , 2963-2975. https://doi.org/10.1002/pmic.200700216
    Download PDF
    Go to Journal of Proteome Research
    Get e-Alerts
    Get e-Alerts

    Journal of Proteome Research

    Cite this: J. Proteome Res. 2007, 6, 3, 1059–1071
    Click to copy citationCitation copied!
    https://doi.org/10.1021/pr060358f
    Published January 17, 2007
    Copyright © 2007 American Chemical Society
    Request reuse permissions

    Article Views

    1406

    Altmetric

    -

    Citations

    94
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.