Roles of BMP6/7 in Actin Dynamics in Amyloid β-Induced Neurotoxicity

Abstract

Actin dynamics plays an important role in many physiological functions such as long-term potentiation, neurotransmission, regulatory proteins translocation, ATP cycle, etc. When amyloid β (Aβ)-induced neurotoxicity occurs, the imbalance of actin dynamics leads to dystrophy of dendrites, which is characteristic pathology in Alzheimer’s disease (AD). Transient and persistent Aβ neurotoxicity provokes distinct manifestations of actin dynamics and causes opposing effects in AD. It has been shown that bone morphogenetic protein 6/7 (BMP6/7) protects neuronal morphology against Aβ-induced neurotoxicity, and can directly bind to LIM kinase1 (LIMK1), being one part of the upstream regulatory pathway of actin dynamics. This review aims to discuss a potential mechanism of BMPs underlying maintainance of cytoskeletal stabilization in neurite.

Share and Cite:

Sun, L. , Zhang, Y. & Xiao, S. (2014). Roles of BMP6/7 in Actin Dynamics in Amyloid β-Induced Neurotoxicity. Psychology, 5, 707-717. doi: 10.4236/psych.2014.57082.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Aleksic, M., Walcher, D., Giehl, K., Bach, H., Grub, M., Durst, R., Hombach, V., & Marx, N. (2009). Signalling Processes Involved in C-Peptide-Induced Chemotaxis of CD4-Positive Lymphocytes. Cellular and Molecular Life Sciences, 66, 1974-1984.
http://dx.doi.org/10.1007/s00018-009-9057-y
[2] Ando, K., Fukuhara, S., Moriya, T., Obara, Y., Nakahata, N., & Mochizuki, N. (2013). Rap1 Potentiates Endothelial Cell Junctions by Spatially Controlling Myosin II Activity and Actin Organization. The Journal of Cell Biology, 202, 901-616.
http://dx.doi.org/10.1083/jcb.201301115
[3] Baker, J. L., & Voth, G. A. (2013). Effects of ATP and Actin-Filament Binding on the Dynamics of the Myosin II S1 Domain. Biophysical Journal, 105, 1624-1634.
http://dx.doi.org/10.1016/j.bpj.2013.08.023
[4] Barbara, J. G., Auclair, N., Roisin, M. P., Otani, S., Valjent, E., Caboche, J., Soubrie, P., & Crepel, F. (2003). Direct and Indirect Interactions between Cannabinoid CB1 Receptor and Group II Metabotropic Glutamate Receptor Signalling in Layer V Pyramidal Neurons from the Rat Prefrontal Cortex. European Journal of Neuroscience, 17, 981-990.
http://dx.doi.org/10.1046/j.1460-9568.2003.02533.x
[5] Becker, E. W. (2006). The Roles of ATP in the Dynamics of the Actin Filaments of the Cytoskeleton. The Journal of Biological Chemistry, 387, 401-406.
[6] Bennett, M. R., Farnell, L., & Gibson, W. G. (2011). A Model of NMDA Receptor Control of F-Actin Treadmilling in Synaptic Spines and Their Growth. Bulletin of Mathematical Biology, 73, 2109-2131.
http://dx.doi.org/10.1007/s11538-010-9614-4
[7] Bernstein, B. W., Chen, H., Boyle, J. A., & Bamburg, J. R. (2006). Formation of Actin-ADF/Cofilin Rods Transiently Retards Decline of Mitochondrial Potential and ATP in Stressed Neurons. Cell Physiology—American Journal of Physiology, 291, C828-C839.
http://dx.doi.org/10.1152/ajpcell.00066.2006
[8] Breen, M. J., Moran, D. M., Liu, W., Huang, X., Vary, C. P., & Bergan, R. C. (2013). Endoglin-Mediated Suppression of Prostate Cancer Invasion Is Regulated by Activin and Bone morphogenetic Protein Type II Receptors. PLoS One, 8, e72407.
http://dx.doi.org/10.1371/journal.pone.0072407
[9] Enzmann, G. U., Benton, R. L., Woock, J. P., Howard, R. M., Tsoulfas, P., & Whittemore, S. R. (2005). Consequences of Noggin Expression by Neural Stem, Glia, and Neuronal Precursor Cells Engrafted into the Injured Spinal Cord. Experimental Neurology, 195, 293-304.
http://dx.doi.org/10.1016/j.expneurol.2005.04.021
[10] Chen, L. Y., Rex, C. S., Casale, M. S., Gall, C. M., & Lynch, G. (2007). Changes in Synaptic Morphology Accompany Actin Signaling during LTP. Journal of Neuroscience, 27, 5363-5372.
http://dx.doi.org/10.1523/JNEUROSCI.0164-07.2007
[11] Chotibut, T., Davis, R. W., Arnold, J. C., Frenchek, Z., Gurwara, S., Bondada, V., Geddes, J. W., & Salvatore, M. F. (2013). Ceftriaxone Increases Glutamate Uptake and Reduces Striatal Tyrosine Hydroxylase Loss in 6-OHDA Parkinson’s Model. Molecular Neurobiology, 12. [Epub ahead of print].
[12] Davis, R. C., Maloney, M. T., Minamide, L. S., Flynn, K. C., Stonebraker, M. A., & Bamburg, J. R. (2009). Mapping Cofilin-Actin Rods in Stressed Hippocampal Slices and the Role of cdc42 in Amyloid-Beta-Induced Rods. Journal of Alzheimers Disease, 18, 35-50.
[13] Davis, R. C., Marsden, I. T., Maloney, M. T., Minamide, L. S., Podlisny, M., Selkoe, D. J., & Bamburg, J. R. (2011). Amyloid Beta Dimers/Trimers Potently Induce Cofilin-Actin Rods That Are Inhibited by Maintaining Cofilin-Phosphorylation. Molecular Neurodegeneration, 6, 10.
http://dx.doi.org/10.1186/1750-1326-6-10
[14] Di Liddo, R., Grandi, C., Venturini, M., Dalzoppo, D., Negro, A., Conconi, M. T., & Parnigotto, P. P. (2010). Recombinant Human TAT-OP1 to Enhance NGF Neurogenic Potential: Preliminary Studies on PC12 Cells. Protein Engineering Design and Selection, 23, 889-897.
http://dx.doi.org/10.1093/protein/gzq067
[15] Doherty, G. J., & McMahon, H. T. (2008). Mediation, Modulation and Consequences of Membrane-Cytoskeleton Interactions. Annual Review of Biophysics, 37, 65-95.
http://dx.doi.org/10.1146/annurev.biophys.37.032807.125912
[16] Doi, Y., Miyazaki, M., Yoshiiwa, T., Hara, K., Kataoka, M., & Tsumura, H. (2011). Manipulation of the Anabolic and Catabolic Responses with BMP-2 and Zoledronic Acid in a Rat Femoral Fracture Model. Bone, 49, 777-782.
http://dx.doi.org/10.1016/j.bone.2011.07.005
[17] Eaton, B. A. & Davis, G. W. (2005). Lim Kinase1 Controls Synaptic Stability Downstream of the Type II BMP Receptor. Neuron, 47, 695-708.
http://dx.doi.org/10.1016/j.neuron.2005.08.010
[18] Evans, J. H., & Falke, J. J. (2007). Ca2+ Influx Is an Essential Component of the Positive-Feedback Loop That Maintains Leading-Edge Structure and Activity in Macrophages. Proceedings of the National Academy of Sciences of the United States of America, 104, 16176-16181.
http://dx.doi.org/10.1073/pnas.0707719104
[19] Foletta, V. C., Lim, M. A., Soosairajah, J., Kelly, A. P., Stanley, E. G., Shannon, M., He, W., Das, S., Massague, J., & Bernard, O. (2003). Direct Signaling by the BMP Type II Receptor via the Cytoskeletal Regulator LIMK1. Journal of Cell Biology, 162, 1089-1098.
http://dx.doi.org/10.1083/jcb.200212060
[20] Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., & Inokuchi, K. (2003). Hippocampal LTP Is Accompanied by Enhanced F-Actin Content within the Dendritic Spine That Is Essential for Late LTP Maintenance In Vivo. Neuron, 38, 447-460.
http://dx.doi.org/10.1016/S0896-6273(03)00206-X
[21] Fulga, T. A., Elson-Schwab, I., Khurana, V., Steinhilb, M. L., Spires, T. L., Hyman, B. T., & Feany, M. B. (2007). Abnormal Bundling and Accumulation of F-Actin Mediates Tau-Induced Neuronal Degeneration in Vivo. Nature Cell Biology, 9, 139-148.
http://dx.doi.org/10.1038/ncb1528
[22] Garred, M. M., Wang, M. M., Guo, X., Harrington, C. A., & Lein, P. J. (2011). Transcriptional Responses of Cultured Rat Sympathetic Neurons during BMP-7-Induced Dendritic Growth. PLoS ONE, 6, e21754.
http://dx.doi.org/10.1371/journal.pone.0021754
[23] Guharoy, M., Szabo, B., Martos, S. C., Kosol, S., & Tompa, P. (2013). Intrinsic Structural Disorder in Cytoskeletal Proteins. Cytoskeleton (Hoboken), 70, 550-571.
http://dx.doi.org/10.1002/cm.21118
[24] Hall, A., & Lalli, G. (2010). Rho and Ras GTPases in Axon Growth, Guidance, and Branching. Cold Spring Harbor Perspectives in Biology, 2, a001818.
http://dx.doi.org/10.1101/cshperspect.a001818
[25] Halpain, S., Hipolito, A., & Saffer, L. (1998). Regulation of F-Actin Stability in Dendritic Spines by Glutamate Receptors and Calcineurin. Journal of Neuroscience, 18, 9835-9844.
[26] Heredia, L., Helguera, P., de Olmos, S., Kedikian, G., Solá Vigo, F., LaFerla, F., Staufenbiel, M., De Olmos, J., Busciglio, J., Cáceres, A., & Lorenzo, A. (2006). Phosphorylation of Actin-Depolymerizing Factor/Cofilin by LIM-Kinase Mediates Amyloid Beta-Induced Degeneration: A Potential Mechanism of Neuronal Dystrophy in Alzheimer’s Disease. Journal of Neuroscience, 26, 6533-6542.
http://dx.doi.org/10.1523/JNEUROSCI.5567-05.2006
[27] Hocking, J. C., Hehr, C. L., Bertolesi, G., Funakoshi, H., Nakamura, T., & McFarlane, S. (2009). LIMK1 Acts Downstream of BMP Signaling in Developing Retinal Ganglion Cell Axons but Not Dendrites. Developmental Biology, 330, 273-285.
http://dx.doi.org/10.1016/j.ydbio.2009.03.027
[28] Hoffman, B. D., Grashoff, C., & Schwartz, M. A. (2011). Dynamic Molecular Processes Mediate Cellular Mechanotransduction. Nature, 475, 316-323.
http://dx.doi.org/10.1038/nature10316
[29] Hotulainen, P., & Hoogenraad, C. C. (2010). Actin in Dendritic Spines: Connecting Dynamics to Function. Journal of Cell Biology, 189, 619-629.
http://dx.doi.org/10.1038/nature10316
[30] Iijima-Ando, K., Sekiya, M., Maruko-Otake, A., Ohtake, Y., Suzuki, E., Lu, B., & Iijima, K. M. (2012). Loss of Axonal Mitochondria Promotes Tau-Mediated Neurodegeneration and Alzheimer’s Disease-Related Tau Phosphorylation via PAR-1. PLoS Genetics, 8, e1002918.
http://dx.doi.org/10.1371/journal.pgen.1002918
[31] Ishibashi, F. (2008). High Glucose Increases Phosphocofilin via Phosphorylation of LIM Kinase Due to Rho/Rho Kinase Activation in Cultured Pig Proximal Tubular Epithelial Cells. Diabetes Research and Clinical Practice, 80, 24-33.
http://dx.doi.org/10.1016/j.diabres.2007.11.004
[32] Jang, D. H., Han, J. H., Lee, S. H., Lee, Y. S., Park, H., Lee, S. H., Kim, H., & Kaang, B. K. (2005). Cofilin Expression Induces Cofilin-Actin Rod Formation and Disrupts Synaptic Structure and Function in Aplysia Synapses. Proceedings of the National Academy of Sciences of the United States of America, 102, 16072-16077.
[33] Janmey, P. A., Kas, J., Shah, J. V., Allen, P. G., & Tang, J. X. (1999). Cytoskeletal Networks and Filament Bundles: Regulation by Proteins and Polycations. The Biological Bulletin, 194, 334-335.
http://dx.doi.org/10.2307/1543105
[34] Kneussel, M., & Wagner, W. (2013). Myosin Motors at Neuronal Synapses: Drivers of Membrane Transport and Actin Dynamics. Nature Reviews Neuroscience, 14, 233-247.
http://dx.doi.org/10.1038/nrn3445
[35] Kousaka, K., Kiyonari, H., Oshima, N., Nagafuchi, A., Shima, Y., Chisaka, O., & Uemura, T. (2008). Slingshot-3 Dephosphorylates ADF/Cofilin but Is Dispensable for Mouse Development. Genesis, 46, 246-255.
http://dx.doi.org/10.1002/dvg.20389
[36] Koyama, T., Boston, D., Ikenouchi, H., & Barry, W. H. (1996). Survival of Metabolically Inhibited Ventricular Myocytes Is Enhanced by Inhibition of Rigor and SR Ca2+ Cycling. American Journal of Physiology, 271, H643-650.
[37] Kreis, P., Hendricusdottir, R., Kay, L., Papageorgiou, I. E., van Diepen, M., Mack, T., Ryves, J., Harwood, A., Leslie, N. R., Kann, O., Parsons, M., & Eickholt, B. J. (2013). Phosphorylation of the Actin Binding Protein Drebrin at S647 Is Regulated by Neuronal Activity and PTEN. PLoS ONE, 8, e71957.
http://dx.doi.org/10.1371/journal.pone.0071957
[38] Lin, T., Zeng, L., Liu, Y., DeFea, K., Schwartz, M. A., Chien, S., & Shyy, J. Y. (2003). Rho-ROCK-LIMK-Cofilin Pathway Regulates Shear Stress Activation of Sterol Regulatory Element Binding Proteins. Circulation Research, 92, 1296-1304.
http://dx.doi.org/10.1161/01.RES.0000078780.65824.8B
[39] Lisman, J. (2003). Actin’s Actions in LTP-Induced Synapse Growth. Neuron, 38, 361-362.
http://dx.doi.org/10.1016/S0896-6273(03)00257-5
[40] Liu, Y., Ren, W., Warburton, R., Toksoz, D., & Fanburg, B. L. (2009). Serotonin Induces Rho/ROCK-Dependent Activation of Smads1/5/8 in Pulmonary Artery Smooth Muscle Cells. The FASEB Journal, 23, 2299-2306.
http://dx.doi.org/10.1096/fj.08-127910
[41] Maloney, M. T., Minamide, L. S., Kinley, A. W., Boyle, J. A., & Bamburg, J. R. (2005). Beta-Secretase-Cleaved Amyloid Precursor Protein Accumulates at Actin Inclusions Induced in Neurons by Stress or Amyloid Beta: A Feedforward Mechanism for Alzheimer’s Disease. The Journal of Neuroscience, 25, 11313-11321.
http://dx.doi.org/10.1523/JNEUROSCI.3711-05.2005
[42] Marsick, B. M., & Letourneau, P. C. (2011). Labeling F-Actin Barbed Ends with Rhodamine-Actin in Permeabilized Neuronal Growth Cones. Journal of Visualized Experiments, 17, Article ID 2409.
[43] Marsick, B. M., Miguel-Ruiz, J. E. S., & Letourneau, P. C. (2012). Activation of Ezrin/Radixin/ Moesin Mediates Attractive Growth Cone Guidance through Regulation of Growth Cone Actin and Adhesion Receptors. Journal of Neuroscience, 32, 282-296.
http://dx.doi.org/10.1523/JNEUROSCI.4794-11.2012
[44] Matsuura, I., Endo, M., Hata, K., Kubo, T., Yamaguchi, A., Saeki, N., & Yamashita, T. (2007). BMP Inhibits Neurite Growth by a Mechanism Dependent on LIM-Kinase. Biochemical Biophysical Research Communications, 360, 868-873.
http://dx.doi.org/10.1016/j.bbrc.2007.06.157
[45] Mendoza-Naranjo, A., Gonzalez-Billault, C., & Maccioni, R. B. (2007). Abeta1-42 Stimulates Actin Polymerization in Hippocampal Neurons through Rac1 and Cdc42 Rho GTPases. Journal of Cell Science, 120, 279-288.
http://dx.doi.org/10.1242/jcs.03323
[46] Minamide, L. S., Striegl, A. M., Boyle, J. A., Meberg, P. J., & Bamburg, J. R. (2000). Neurodegenerative Stimuli Induce Persistent ADF/Cofilin-Actin Rods That Disrupt Distal Neurite Function. Nature Cell Biology, 2, 628-636.
http://dx.doi.org/10.1038/35023579
[47] Miyagi, M., Mikawa, S., Hasegawa, T., Kobayashi, S., Matsuyama, Y., & Sato, K. (2011). Bone Morphogenetic Protein Receptor Expressions in the Adult Rat Brain. Neuroscience, 176, 93-109.
http://dx.doi.org/10.1016/j.neuroscience.2010.12.027
[48] Ng, J. (2008). TGFβ Signals Regulate Axonal Development through Distinct Smad-Independent Mechanisms. Development, 135, 4025-4035.
http://dx.doi.org/10.1242/dev.028209
[49] Ng, J., & Luo, L. (2004). Rho GTPases Regulate Axon Growth through Convergent and Divergent Signaling Pathways. Neuron, 44, 779-793.
http://dx.doi.org/10.1016/j.neuron.2004.11.014
[50] Odabas, S., Feichtinger, G. A., Korkusuz, P., Inci, I., Bilgic, E., Yar, A. S., Cavusoglu, T., Menevse, S., Vargel, I., & Piskin, E. (2013). Auricular Cartilage Repair Using Cryogel Scaffolds Loaded with BMP-7-Expressing Primary Chondrocytes. Journal of Tissue Engineering and Regenerative Medicine, 7, 831-840.
[51] Ono, S. (2007). Mechanism of Depolymerization and Severing of Actin Filaments and Its Significance in Cytoskeletal Dynamics. International Review of Cytology, 258, 1-82.
http://dx.doi.org/10.1016/S0074-7696(07)58001-0
[52] Podkowa, M., Christova, T., Zhao, X., Jian, Y., & Attisano, L. (2013). P21-Activated Kinase (PAK) Is Required for Bone Morphogenetic Protein (BMP)-Induced Dendritogenesis in Cortical Neurons. Molecular Cell Neuroscience, 57, 83-92.
http://dx.doi.org/10.1016/j.mcn.2013.10.005
[53] Ramabhadran, V., Hatch, A. L., & Higgs, H. N. (2013). Actin Monomers Activate Inverted Formin 2 by Competing with Its Autoinhibitory Interaction. The Journal of Biology Chemistry, 288, 26847-26855.
http://dx.doi.org/10.1074/jbc.M113.472415
[54] Ravera, S., Panfoli, I., Calzia, D., Aluigi, M. G., Bianchini, P., Diaspro, A., Mancardi, G., & Morelli, A. (2009). Evidence for Aerobic ATP Synthesis in Isolated Myelin Vesicles. The International Journal of Biochemistry & Cell Biology, 41, 1581-1591.
http://dx.doi.org/10.1016/j.biocel.2009.01.009
[55] Rex, C. S., Chen, L. Y., Sharma, A., Liu, J., Babayan, A. H., Gall, C. M., & Lynch, G. (2009). Different Rho GTPase-Dependent Signaling Pathways Initiate Sequential Steps in the Consolidation of Long-Term Potentiation. Journal of Cell Biology, 186, 85-97.
http://dx.doi.org/10.1083/jcb.200901084
[56] Reymann, A. C., Suarez, C., Guerin, C., Martiel, J. L., Staiger, C. J., Blanchoin, L., & Boujemaa-Paterski, R. (2011). Turnover of Branched Actin Filament Networks by Stochastic Fragmentation with ADF/Cofilin. Molecular Biology Cell, 22, 2541-2550.
http://dx.doi.org/10.1091/mbc.E11-01-0052
[57] Rustom, A., Saffrich, R., Markovic, I., Walther, P., & Gerdes, H. H. (2004). Nanotubular Highways for Intercellular Organelle Transport. Science, 303, 1007-1010.
http://dx.doi.org/10.1126/science.1093133
[58] Sartori, R., Schirwis, E., Blaauw, B., Bortolanza, S., Zhao, J., Enzo, E., Stantzou, A., Mouisel, E., Toniolo, L., Ferry, A., Stricker, S., Goldberg, A.L., Dupont, S., Piccolo, S., Amthor, H., & Sandri, M. (2013). BMP Signaling Controls Muscle Mass. Nature Genetics, 45, 1309-1318.
http://dx.doi.org/10.1038/ng.2772
[59] Schuh, M. (2011). An Actin-Dependent Mechanism for Long-Range Vesicle Transport. Nature Cell Biology, 13, 1431-1436.
http://dx.doi.org/10.1038/ncb2353
[60] Sepulveda, F. J., Parodi, J., Peoples, R. W., Opazo, C., & Aguayo, L. G. (2010). Synaptotoxicity of Alzheimer Beta Amyloid Can Be Explained by Its Membrane Perforating Property. PLoS ONE, 5, e11820.
http://dx.doi.org/10.1371/journal.pone.0011820
[61] Sinha, B., Koster, D., Ruez, R., Gonnord, P., Bastiani, M., Abankwa, D., Stan, R. V., Butler-Browne, G., Vedie, B., Johannes, L., Morone, N., Parton, R. G., Raposo, G., Sens, P., Lamaze, C., & Nassoy, P. (2011). Cells Respond to Mechanical Stress by Rapid Disassembly of Caveolae. Cell, 144, 402-413.
http://dx.doi.org/10.1016/j.cell.2010.12.031
[62] Song, C., Perides, G., Wang, D., & Liu, Y. F. (2002). Beta-Amyloid Peptide Induces Formation of a Ctin Stress Fibers through p38 Mitogen-Activated Protein Kinase. Journal of Neurochemistry, 83, 828-836.
http://dx.doi.org/10.1046/j.1471-4159.2002.01182.x
[63] Soosairajah, J., Maiti, S., Wiggan, O., Sarmiere, P., Moussi, N., Sarcevic, B., Sampath, R., Bamburg, J. R., & Bernard, O. (2005). Interplay between Components of a Novel LIM Kinase-Slingshot Phosphatase Complex Regulates Cofilin. The EMBO Journal, 24, 473-486.
http://dx.doi.org/10.1038/sj.emboj.7600543
[64] Sun, L., Guo, C., Liu, D., Zhao, Y., Zhang, Y., Song, Z., Han, H., Chen, D., & Zhao, Y. (2011). Protective Effects of Bone Morphogenetic Protein 7 against Amyloid-Beta Induced Neurotoxicity in PC12 Cells. Neuroscience, 184, 151-163.
http://dx.doi.org/10.1016/j.neuroscience.2011.03.059
[65] Suurna, M. V., Ashworth, S. L., Hosford, M., Sandoval, R. M., Wean, S. E., Shah, B. M., Bamburg, J. R., & Molitoris, B. A. (2006). Cofilin Mediates ATP Depletion-Induced Endothelial Cell Actin Alterations. American Journal of Physiology, Renal Physiology, 290, F1398-F1407.
http://dx.doi.org/10.1152/ajprenal.00194.2005
[66] Vlachos, A., Ikenberg, B., Lenz, M., Becker, D., Reifenberg, K., Bas-Orth, C., & Deller, T. (2013). Synaptopodin Regulates Denervation-Induced Homeostatic Synaptic Plasticity. Proceedings of the National Academy of Sciences of the United States of America, 110, 8242-8247.
http://dx.doi.org/10.1073/pnas.1213677110
[67] Wang, Y., Dong, Q., Xu, X. F., Feng, X., Xin, J., Wang, D. D., Yu, H., Tian, T., & Chen, Z. Y. (2013). Phosphorylation of Cofilin Regulates Extinction of Conditioned Aversive Memory via AMPAR Trafficking. Journal of Neuroscience, 33, 6423-6433.
http://dx.doi.org/10.1523/JNEUROSCI.5107-12.2013
[68] Wei, A., Brisby, H., Chung, S. A., & Diwan, A. D. (2008). Bone Morphogenetic Protein-7 Protects Human Intervertebral Disc Cells in Vitro from Apoptosis. The Spine Journal, 8, 466-474.
http://dx.doi.org/10.1016/j.spinee.2007.04.021
[69] Whitehead, G., Jo, J., Hogg, E. L., Piers, T., Kim, D. H., Seaton, G., Seok, H., Bru-Mercier, G., Son, G. H., Regan, P., Hildebrandt, L., Waite, E., Kim, B. C., Kerrigan, T. L., Kim, K., Whitcomb, D. J., Collingridge, G. L., Lightman, S. L., & Cho, K. (2013). Acute Stress Causes Rapid Synaptic Insertion of Ca2+-Permeable AMPA Receptors to Facilitate Long-Term Potentiation in the Hippocampus. Brain, 136, 3753-3765.
http://dx.doi.org/10.1093/brain/awt293
[70] Yabe, T., Samuels, I., & Schwartz, J. P. (2002). Bone Morphogenetic Proteins BMP-6 and BMP-7 Have Differential Effects on Survival and Neurite Outgrowth of Cerebellar Granule Cell Neurons. Journal of Neuroscience Research, 68, 161-168.
http://dx.doi.org/10.1002/jnr.10210
[71] Zhang, X. L., Poschel, B., Faul, C., Upreti, C., Stanton, P. K., & Mundel, P. (2013). Essential Role for Synaptopodin in Dendritic Spine Plasticity of the Developing Hippocampus. Journal of Neuroscience, 33, 12510-12518.
http://dx.doi.org/10.1523/JNEUROSCI.2983-12.2013
[72] Zhao, R., Du, L., Huang, Y., Wu, Y., & Gunst, S. J. (2008). Actin Depolymerization Factor/Cofilin Activation Regulates Actin Polymerization and Tension Development in Canine Tracheal Smooth Muscle. The Journal of Biology Chemistry, 283, 36522-36531.
http://dx.doi.org/10.1074/jbc.M805294200

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.