Exploring protein - protein interaction in cell physiology by reviewing the role of dynein-dynactin interaction as a representative example
DOI:
https://doi.org/10.24193/subbbiol.2023.1.06Keywords:
protein-protein interactions, dynein, dynactin, dysregulation, cargo transportAbstract
Protein-protein interactions are essential for the normal function of cells and are involved in various cellular processes. These interactions can occur through a variety of mechanisms, including hydrogen bonding, ionic interactions, and hydrophobic interactions. Changes in protein-protein interactions can alter the normal function of the cell and lead to various diseases. Understanding protein-protein interactions is important for the development of therapeutic approaches targeting these interactions for the treatment of diseases. In this article, I will discuss the role of protein-protein interactions in normal cellular function, the consequences of changes in these interactions, and the importance and significance of understanding these interactions by using the example of dynein-dynactin.
Article history: Received: 27 February 2023; Revised: 23 March 2023; Accepted: 24 May 2023; Available online: 30 June 2023.
References
Alberts, B. (2014). Molecular Biology of the Cell. 6th Ed. Garland Science New York, pp.930-945
Ananthanarayanan, V., Schattat, M., Vogel, S. K., Krull, A., Pavin, N., & Tolić-Nørrelykke, I. M. (2013). Dynein motion switches from diffusive to directed upon cortical anchoring. Cell, 153(7), 1526–1536. https://doi.org/10.1016/j.cell.2013.05.020
Athanasios, A., Charalampos, V., & Vasileios, T. (2017). Protein-protein interaction (PROTEIN-PROTEIN INTERACTIONS) network: recent advances in drug discovery. Current drug metabolism, 18(1), 5-10.
Berggård, T., Linse, S., & James, P. (2007). Methods for the detection and analysis of protein-protein interactions. Proteomics, 7(16), 2833–2842. https://doi.org/10.1002/pmic.200700131
Bhabha, G., Cheng, H.-C., Zhang, N., Moeller, A., Liao, M., Speir, J. A., Cheng, Y., and Vale, R. D. (2014). Allosteric communication in the dynein motor domain. Cell, 159(4):857–868.
Carvalho, P., Gupta, M. L., Jr, Hoyt, M. A., & Pellman, D. (2004). Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Developmental cell, 6(6), 815–829. https://doi.org/10.1016/j.devcel.2004.05.001
Chaaban, S., & Carter, A. P. (2022). Structure of dynein-dynactin on microtubules shows tandem adaptor binding. Nature, 610(7930), 212–216. https://doi.org/10.1038/s41586-022-05186-y
Devine, M. J., Birsa, N., & Kittler, J. T. (2016). Miro sculpts mitochondrial dynamics in neuronal health and disease. Neurobiology of disease, 90, 27-34.
DeWitt, M. A., Cypranowska, C. A., Cleary, F. B., Belyy, V., and Yildiz, A. (2015). The AAA3 domain of cytoplasmic dynein acts as a switch to facilitate microtubule release. Nature Structural & Molecular Biology, 22(1):73–80.
Dixit, R., Barnett, B., Lazarus, J. E., Tokito, M., Goldman, Y. E., & Holzbaur, E. L. (2009). Microtubule plus-end tracking by CLIP-170 requires EB1. Proceedings of the National Academy of Sciences of the United States of America, 106(2), 492–497. https://doi.org/10.1073/pnas.0807614106
Drerup, C. M., Herbert, A. L., Monk, K. R., & Nechiporuk, A. V. (2017). Regulation of mitochondria-dynactin interaction and mitochondrial retrograde transport in axons. eLife, 6, e22234. https://doi.org/10.7554/eLife.22234
Duellberg, C., Trokter, M., Jha, R., Sen, I., Steinmetz, M. O., & Surrey, T. (2014). Reconstitution of a hierarchical +TIP interaction network controlling microtubule end tracking of dynein. Nature cell biology, 16(8), 804–811. https://doi.org/10.1038/ncb2999
Dunker, A. K., Cortese, M. S., Romero, P., Iakoucheva, L. M., & Uversky, V. N. (2005). Flexible nets. The roles of intrinsic disorder in protein interaction networks. The FEBS journal, 272(20), 5129–5148. https://doi.org/10.1111/j.1742-4658.2005.04948.x
Eckley, D. M., Gill, S. R., Melkonian, K. A., Bingham, J. B., Goodson, H. V., Heuser, J. E., & Schroer, T. A. (1999). Analysis of dynactin subcomplexes reveals a novel actin-related protein associated with the arp1 minifilament pointed end. The Journal of cell biology, 147(2), 307–320. https://doi.org/10.1083/jcb.147.2.307
Elshenawy, M. M., Canty, J. T., Oster, L., Ferro, L. S., Zhou, Z., Blanchard, S. C., and Yildiz, A. (2019). Cargo adaptors regulate steProtein-protein interactionsng and force generation of mammalian dynein-dynactin. Nature Chemical Biology, 15(11):1093–1101.
Fliegauf, M., Benzing, T., & Omran, H. (2007). When cilia go bad: cilia defects and ciliopathies. Nature reviews Molecular cell biology, 8(11), 880-893.
Gama, J. B., Pereira, C., Simões, P. A., Celestino, R., Reis, R. M., Barbosa, D. J., Pires, H. R., Carvalho, C., Amorim, J., Carvalho, A. X., Cheerambathur, D. K., and Gassmann, R. (2017). Molecular mechanism of dynein recruitment to kinetochores by the Rod-Zw10-Zwilch complex and Spindly. The Journal of Cell Biology, 216(4):943–960.
Gibbons, I. R., Garbarino, J. E., Tan, C. E., Reck-Peterson, S. L., Vale, R. D., and Carter, A. P. (2005). The affinity of the dynein microtubule-binding domain is modulated by the conformation of its coiled-coil stalk. The Journal of Biological Chemistry, 280(25):23960–23965.
Gunawardena, S., & Goldstein, L. S. (2004). Cargo‐carrying motor vehicles on the neuronal highway: Transport pathways and neurodegenerative disease. Journal of neurobiology, 58(2), 258-271.
Guo, X., Macleod, G. T., Wellington, A., Hu, F., Panchumarthi, S., Schoenfield, M., Marin, L., Charlton, M. P., Atwood, H. L., & Zinsmaier, K. E. (2005). The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron, 47(3), 379–393. https://doi.org/10.1016/j.neuron.2005.06.027
Ha, J., Lo, K. W., Myers, K. R., Carr, T. M., Humsi, M. K., Rasoul, B. A., Segal, R. A., & Pfister, K. K. (2008). A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. The Journal of cell biology, 181(6), 1027–1039. https://doi.org/10.1083/jcb.200803150
Harris, S. L., & Levine, A. J. (2005). The p53 pathway: positive and negative feedback loops. Oncogene, 24(17), 2899-2908.
Hirokawa, N., Noda, Y., & Okada, Y. (1998). Kinesin and dynein superfamily proteins in organelle transport and cell division. Current opinion in cell biology, 10(1), 60-73.
Holzbaur, E. L., & Vallee, R. B. (1994). DYNEINS: molecular structure and cellular function. Annual review of cell biology, 10, 339–372, https://doi.org/10.1146/annurev.cb.10.110194.002011.
Kang, J. S., Tian, J. H., Pan, P. Y., Zald, P., Li, C., Deng, C., & Sheng, Z. H. (2008). Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell, 132(1), 137–148, https://doi.org/10.1016/j.cell.2007.11.024.
King, S. J., & Schroer, T. A. (2000). Dynactin increases the processivity of the cytoplasmic dynein motor. Nature cell biology, 2(1), 20–24, https://doi.org/10.1038/71338.
Lipka, J., Kuijpers, M., Jaworski, J., & Hoogenraad, C. C. (2013). Mutations in cytoplasmic dynein and its regulators cause malformations of cortical development and neurodegenerative diseases. Biochemical Society Transactions, 41(6), 1605-1612.
Liu J. J. (2017). Regulation of dynein-dynactin-driven vesicular transport. Traffic (Copenhagen, Denmark), 18(6), 336–347, https://doi.org/10.1111/tra.12475.
Lloyd, T. E., Machamer, J., O’Hara, K., Kim, J. H., Collins, S. E., Wong, M. Y., Sahin, B., Imlach, W., Yang, Y., Levitan, E. S., McCabe, B. D., & Kolodkin, A. L. (2012). The p150(Glued) CAP-Gly domain regulates initiation of retrograde transport at synaptic termini. Neuron, 74(2), 344–360, https://doi.org/10.1016/j.neuron.2012.02.026.
Mallik, R., Carter, B. C., Lex, S. A., King, S. J., & Gross, S. P. (2004). Cytoplasmic dynein functions as a gear in response to load. Nature, 427(6975), 649–652. https://doi.org/10.1038/nature02293
McKenney, R. J., Huynh, W., Tanenbaum, M. E., Bhabha, G., and Vale, R. D. (2014). Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science, 345(6194):337–341.
Misko, A., Jiang, S., Wegorzewska, I., Milbrandt, J., & Baloh, R. H. (2010). Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. The Journal of neuroscience: the official journal of the Society for Neuroscience, 30(12), 4232–4240, https://doi.org/10.1523/JNEUROSCI.6248-09.2010.
Nooren, I. M., & Thornton, J. M. (2003). Diversity of protein-protein interactions. The EMBO journal, 22(14), 3486–3492, https://doi.org/10.1093/emboj/cdg359.
Ofran, Y., & Rost, B. (2003). Analysing six types of protein-protein interfaces. Journal of molecular biology, 325(2), 377–387, https://doi.org/10.1016/s0022-2836(02)01223-8.
Pilling, A. D., Horiuchi, D., Lively, C. M., & Saxton, W. M. (2006). Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Molecular biology of the cell, 17(4), 2057–2068, https://doi.org/10.1091/mbc.e05-06-0526.
Rai, A. K., Rai, A., Ramaiya, A. J., Jha, R., & Mallik, R. (2013). Molecular adaptations allow dynein to generate large collective forces inside cells. Cell, 152(1-2), 172–182. https://doi.org/10.1016/j.cell.2012.11.044.
Rao, V. S., Srinivas, K., Sujini, G. N., & Kumar, G. N. (2014). Protein-protein interaction detection: methods and analysis. International journal of proteomics, 2014, 147648. https://doi.org/10.1155/2014/147648.
Reck-Peterson, S. L., Redwine, W. B., Vale, R. D., and Carter, A. P. (2018). The cytoplasmic dynein transport machinery and its many cargoes. Nature Reviews. Molecular Cell Biology, 19(6):382–398.
Roberts, A. J., Numata, N., Walker, M. L., Kato, Y. S., Malkova, B., Kon, T., Ohkura, R., Arisaka, F., Knight, P. J., Sutoh, K., and Burgess, S. A. (2009). AAA+ Ring and linker swing mechanism in the dynein motor. Cell, 136(3):485–495.
Rompolas, P., Patel-King, R. S., & King, S. M. (2012). Association of Lis1 with outer arm dynein is modulated in response to alterations in flagellar motility. Molecular biology of the cell, 23(18), 3554-3565.
Ross, J. L., Wallace, K., Shuman, H., Goldman, Y. E., & Holzbaur, E. L. (2006). Processive bidirectional motion of dynein–dynactin complexes in vitro. Nature cell biology, 8(6), 562-570.
Saotome, M., Safiulina, D., Szabadkai, G., Das, S., Fransson, A., Aspenstrom, P., Rizzuto, R., & Hajnóczky, G. (2008). Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proceedings of the National Academy of Sciences of the United States of America, 105(52), 20728–20733, https://doi.org/10.1073/pnas.0808953105.
Sarmady, M., Dampier, W., & Tozeren, A. (2011). HIV protein sequence hotspots for crosstalk with host hub proteins. PloS one, 6(8), e23293, https://doi.org/10.1371/journal.pone.0023293.
Scheibye-Knudsen, M., Fang, E. F., Croteau, D. L., Wilson, D. M., 3rd, & Bohr, V. A. (2015). Protecting the mitochondrial powerhouse. Trends in cell biology, 25(3), 158–170. https://doi.org/10.1016/j.tcb.2014.11.002
Schmidt, H. and Carter, A. P. (2016). Review: Structure and mechanism of the dynein motor ATPase. Biopolymers, 105(8):557–567.
Smirnova, E., Griparic, L., Shurland, D. L., & van der Bliek, A. M. (2001). Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Molecular biology of the cell, 12(8), 2245–2256, https://doi.org/10.1091/mbc.12.8.2245.
Stamenovic, D., Mijailovich, S. M., Tolić-Nørrelykke, I. M., Chen, J., & Wang, N. (2002). Cell prestress. II. Contribution of microtubules. American Journal of Physiology-Cell Physiology, 282(3), C617-C624.
Stowers, R. S., Megeath, L. J., Górska-Andrzejak, J., Meinertzhagen, I. A., & Schwarz, T. L. (2002). Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron, 36(6), 1063–1077, https://doi.org/10.1016/s0896-6273(02)01094-2.
Twelvetrees, A. E., Pernigo, S., Sanger, A., Guedes-Dias, P., Schiavo, G., Steiner, R. A., Dodding, M. P., & Holzbaur, E. L. (2016). The Dynamic Localization of Cytoplasmic Dynein in Neurons Is Driven by Kinesin-1. Neuron, 90(5), 1000–1015, https://doi.org/10.1016/j.neuron.2016.04.046.
Urnavicius, L., Lau, C. K., Elshenawy, M. M., Morales-Rios, E., Motz, C., Yildiz, A., and Carter, A. P. (2018). Cryo-EM shows how dynactin recruits two dyneins for faster movement. Nature, 554(7691):202–206.
Urnavicius, L., Zhang, K., Diamant, A. G., Motz, C., Schlager, M. A., Yu, M., Patel, N. A., Robinson, C. V., and Carter, A. P. (2015). The structure of the dynactin complex and its interaction with dynein. Science, 347(6229):1441–1446.
Vaughan, K. T., & Vallee, R. B. (1995). Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. The Journal of cell biology, 131(6 Pt 1), 1507–1516, https://doi.org/10.1083/jcb.131.6.1507.
von Mering, C., Krause, R., Snel, B., Cornell, M., Oliver, S. G., Fields, S., & Bork, P. (2002). Comparative assessment of large-scale data sets of protein-protein interactions. Nature, 417(6887), 399–403. https://doi.org/10.1038/nature750
Vona, R., Mileo, A. M., & Matarrese, P. (2021). Microtubule-Based Mitochondrial Dynamics as a Valuable Therapeutic Target in Cancer. Cancers, 13(22), 5812.
Wheway, G., Parry, D. A., & Johnson, C. A. (2014). The role of primary cilia in the development and disease of the retina. Organogenesis, 10(1), 69-85.
Yanagida M. (2002). Functional proteomics; current achievements. Journal of chromatography. B, Analytical technologies in the biomedical and life sciences, 771(1-2), 89–106. https://doi.org/10.1016/s1570-0232(02)00074-0
Yano, H., Lee, F. S., Kong, H., Chuang, J., Arevalo, J., Perez, P., Sung, C., & Chao, M. V. (2001). Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. The Journal of neuroscience : the official journal of the Society for Neuroscience, 21(3), RC125, https://doi.org/10.1523/JNEUROSCI.21-03-j0003.2001.
Yeh, T. Y., Quintyne, N. J., Scipioni, B. R., Eckley, D. M., & Schroer, T. A. (2012). Dynactin’s pointed-end complex is a cargo-targeting module. Molecular biology of the cell, 23(19), 3827–3837. https://doi.org/10.1091/mbc.E12-07-0496
Zhang, A. (2009). Protein interaction networks: computational analysis. Cambridge University Press.
Zhang, K., Foster, H. E., Rondelet, A., Lacey, S. E., Bahi-Buisson, N., Bird, A. W., and Carter, A. P. (2017). Cryo-EM Reveals How Human Cytoplasmic Dynein Is Auto-inhibited and Activated. Cell, 169(7):1303–1314.e18
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Studia Universitatis Babeș-Bolyai Biologia
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
