229
Views
1
CrossRef citations to date
0
Altmetric
Research Articles

Disordered regions endow structural flexibility to shell proteins and function towards shell–enzyme interactions in 1,2-propanediol utilization microcompartment

, & ORCID Icon
Pages 8891-8901 | Received 12 Jul 2022, Accepted 16 Oct 2022, Published online: 01 Nov 2022

References

  • Babu, M. M. (2016). The contribution of intrinsically disordered regions to protein function, cellular complexity, and human disease. Biochemical Society Transactions, 44(5), 1185–1200. https://doi.org/10.1042/BST20160172
  • Bari, N. K., Hazra, J. P., Kumar, G., Kaur, S., & Sinha, S. (2020). Probe into a multi-protein prokaryotic organelle using thermal scanning assay reveals distinct properties of the core and the shell. Biochimica et Biophysica Acta. General Subjects, 1864(10), 129680. https://doi.org/10.1016/j.bbagen.2020.129680
  • Cheng, S., Liu, Y., Crowley, C. S., Yeates, T. O., & Bobik, T. A. (2008). Bacterial microcompartments: their properties and paradoxes. BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology, 30(11–12), 1084–1095. https://doi.org/10.1002/bies.20830
  • Cheng, S., Sinha, S., Fan, C., Liu, Y., & Bobik, T. A. (2011). Genetic analysis of the protein shell of the microcompartments involved in coenzyme B12-dependent 1, 2-propanediol degradation by Salmonella. Journal of Bacteriology, 193(6), 1385–1392. https://doi.org/10.1128/JB.01473-10
  • Chowdhury, C., Sinha, S., Chun, S., Yeates, T. O., & Bobik, T. A. (2014). Diverse bacterial microcompartment organelles. Microbiology and Molecular Biology Reviews : MMBR, 78(3), 438–468. https://doi.org/10.1128/MMBR.00009-14
  • Corbella, M., Liao, Q., Moreira, C., Parracino, A., Kasson, P. M., & Kamerlin, S. C. L. (2021). The N-terminal helix-turn-helix motif of transcription factors MarA and Rob drives DNA recognition. The Journal of Physical Chemistry. B, 125(25), 6791–6806. https://doi.org/10.1021/acs.jpcb.1c00771
  • Disfani, F. M., Hsu, W.-L., Mizianty, M. J., Oldfield, C. J., Xue, B., Dunker, A. K., Uversky, V. N., & Kurgan, L. (2012). MoRFpred, a computational tool for sequence-based prediction and characterization of short disorder-to-order transitioning binding regions in proteins. Bioinformatics (Oxford, England), 28(12), i75–i83. https://doi.org/10.1093/bioinformatics/bts209
  • Dosztányi, Z., Mészáros, B., & Simon, I. (2009). ANCHOR: Web server for predicting protein binding regions in disordered proteins. Bioinformatics (Oxford, England), 25(20), 2745–2746. https://doi.org/10.1093/bioinformatics/btp518
  • Fan, C., & Bobik, T. A. (2011). The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment. Journal of Bacteriology, 193(20), 5623–5628. https://doi.org/10.1128/JB.05661-11
  • Fan, C., Cheng, S., Liu, Y., Escobar, C. M., Crowley, C. S., Jefferson, R. E., Yeates, T. O., & Bobik, T. A. (2010). Short N-terminal sequences package proteins into bacterial microcompartments. Proceedings of the National Academy of Sciences of the United States of America, 107(16), 7509–7514. https://doi.org/10.1073/pnas.0913199107
  • Fan, C., Cheng, S., Sinha, S., & Bobik, T. A. (2012). Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments. Proceedings of the National Academy of Sciences of the United States of America, 109(37), 14995–15000. https://doi.org/10.1073/pnas.1207516109
  • Harmon, T. S., Holehouse, A. S., Rosen, M. K., & Pappu, R. V. (2017). Intrinsically disordered linkers determine the interplay between phase separation and gelation in multivalent proteins. eLife, 6, e30294. https://doi.org/10.7554/eLife.30294
  • Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F., & Sutter, M. (2018). Bacterial microcompartments. Nature Reviews. Microbiology, 16(5), 277–290. https://doi.org/10.1038/nrmicro.2018.10
  • Kumar, G., & Sinha, S. (2021). Biophysical approaches to understand and re-purpose bacterial microcompartments. Current Opinion in Microbiology, 63, 43–51. https://doi.org/10.1016/j.mib.2021.05.008
  • Kumar, G., Bari, N. K., Hazra, J. P., & Sinha, S. (2022). A major shell protein of 1, 2‐propanediol utilization microcompartment conserves the activity of its signature enzyme at higher temperatures. ChemBioChem, 23(9), e202100694. https://doi.org/10.1002/cbic.202100694
  • Kurcinski, M., Badaczewska‐Dawid, A., Kolinski, M., Kolinski, A., & Kmiecik, S. (2020). Flexible docking of peptides to proteins using CABS‐dock. Protein Science, 29(1), 211–222. https://doi.org/10.1002/pro.3771
  • Kuriata, A., Gierut, A. M., Oleniecki, T., Ciemny, M. P., Kolinski, A., Kurcinski, M., & Kmiecik, S. (2018). CABS-flex 2.0: A web server for fast simulations of flexibility of protein structures. Nucleic Acids Research, 46(W1), W338–W343. https://doi.org/10.1093/nar/gky356
  • Latonen, L. (2019). Phase-to-phase with nucleoli–stress responses, protein aggregation and novel roles of RNA. Frontiers in Cellular Neuroscience, 13, 151. https://doi.org/10.3389/fncel.2019.00151
  • Lawrence, A. D., Frank, S., Newnham, S., Lee, M. J., Brown, I. R., Xue, W.-F., Rowe, M. L., Mulvihill, D. P., Prentice, M. B., Howard, M. J., & Warren, M. J. (2014). Solution structure of a bacterial microcompartment targeting peptide and its application in the construction of an ethanol bioreactor. ACS Synthetic Biology, 3(7), 454–465. https://doi.org/10.1021/sb4001118
  • Lehman, B. P., Chowdhury, C., & Bobik, T. A. (2017). The N terminus of the PduB protein binds the protein shell of the Pdu microcompartment to its enzymatic core. Journal of Bacteriology, 199(8), e00785–00716. https://doi.org/10.1128/JB.00785-16
  • Luo, Y., Na, Z., & Slavoff, S. A. (2018). P-bodies: Composition, properties, and functions. Biochemistry, 57(17), 2424–2431. https://doi.org/10.1021/acs.biochem.7b01162
  • Mackinder, L. C. M., Meyer, M. T., Mettler-Altmann, T., Chen, V. K., Mitchell, M. C., Caspari, O., Freeman Rosenzweig, E. S., Pallesen, L., Reeves, G., Itakura, A., Roth, R., Sommer, F., Geimer, S., Mühlhaus, T., Schroda, M., Goodenough, U., Stitt, M., Griffiths, H., & Jonikas, M. C. (2016). A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle. Proceedings of the National Academy of Sciences of the United States of America, 113(21), 5958–5963. https://doi.org/10.1073/pnas.1522866113
  • Mészáros, B., Erdos, G., & Dosztányi, Z. (2018). IUPred2A: Context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Research, 46(W1), W329–W337. https://doi.org/10.1093/nar/gky384
  • Nordyke, C. T., Ahmed, Y. M., Puterbaugh, R. Z., Bowman, G. R., & Varga, K. (2020). Intrinsically disordered bacterial polar organizing protein Z, PopZ, interacts with protein binding partners through an N-terminal Molecular Recognition Feature. Journal of Molecular Biology, 432(23), 6092–6107. https://doi.org/10.1016/j.jmb.2020.09.020
  • Oltrogge, L. M., Chaijarasphong, T., Chen, A. W., Bolin, E. R., Marqusee, S., & Savage, D. F. (2020). Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation. Nature Structural & Molecular Biology, 27(3), 281–287. https://doi.org/10.1038/s41594-020-0387-7
  • Protter, D. S., Rao, B. S., Van Treeck, B., Lin, Y., Mizoue, L., Rosen, M. K., & Parker, R. (2018). Intrinsically disordered regions can contribute promiscuous interactions to RNP granule assembly. Cell Reports, 22(6), 1401–1412. https://doi.org/10.1016/j.celrep.2018.01.036
  • Santner, A. A., Croy, C. H., Vasanwala, F. H., Uversky, V. N., Van, Y.-Y. J., & Dunker, A. K. (2012). Sweeping away protein aggregation with entropic bristles: Intrinsically disordered protein fusions enhance soluble expression. Biochemistry, 51(37), 7250–7262. https://doi.org/10.1021/bi300653m
  • Shin, W.-H., Lee, G. R., Heo, L., Lee, H., & Seok, C. (2014). Prediction of protein structure and interaction by GALAXY protein modeling programs. Bio Design, 2(1), 1–11.
  • Tanaka, S., Sawaya, M. R., & Yeates, T. O. (2010). Structure and mechanisms of a protein-based organelle in Escherichia coli. Science (New York, N.Y.), 327(5961), 81–84. https://doi.org/10.1126/science.1179513
  • Uversky, V. N. (2013). The most important thing is the tail: Multitudinous functionalities of intrinsically disordered protein termini. FEBS Letters, 587(13), 1891–1901. https://doi.org/10.1016/j.febslet.2013.04.042
  • van der Lee, R., Buljan, M., Lang, B., Weatheritt, R. J., Daughdrill, G. W., Dunker, A. K., Fuxreiter, M., Gough, J., Gsponer, J., Jones, D. T., Kim, P. M., Kriwacki, R. W., Oldfield, C. J., Pappu, R. V., Tompa, P., Uversky, V. N., Wright, P. E., & Babu, M. M. (2014). Classification of intrinsically disordered regions and proteins. Chemical Reviews, 114(13), 6589–6631. https://doi.org/10.1021/cr400525m
  • Wang, H., Yan, X., Aigner, H., Bracher, A., Nguyen, N. D., Hee, W. Y., Long, B., Price, G. D., Hartl, F., & Hayer-Hartl, M. (2019). Rubisco condensate formation by CcmM in β-carboxysome biogenesis. Nature, 566(7742), 131–135. https://doi.org/10.1038/s41586-019-0880-5
  • Weng, G., Wang, E., Wang, Z., Liu, H., Zhu, F., Li, D., & Hou, T. (2019). HawkDock: a web server to predict and analyze the protein–protein complex based on computational docking and MM/GBSA. Nucleic Acids Research, 47(W1), W322–W330. https://doi.org/10.1093/nar/gkz397
  • Wheatley, N. M., Gidaniyan, S. D., Liu, Y., Cascio, D., & Yeates, T. O. (2013). Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins. Protein Science, 22(5), 660–665. https://doi.org/10.1002/pro.2246
  • Xue, B., Dunbrack, R. L., Williams, R. W., Dunker, A. K., & Uversky, V. N. (2010). PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochimica et Biophysica Acta, 1804(4), 996–1010. https://doi.org/10.1016/j.bbapap.2010.01.011
  • Xue, B., Williams, R. W., Oldfield, C. J., Dunker, A. K., & Uversky, V. N. (2010). Archaic chaos: Intrinsically disordered proteins in Archaea. BMC Systems Biology, 4(S1), 1–21. https://doi.org/10.1186/1752-0509-4-S1-S1
  • Yan, J., & Kurgan, L. (2017). DRNApred, fast sequence-based method that accurately predicts and discriminates DNA-and RNA-binding residues. Nucleic Acids Research, 45(10), e84-e84. https://doi.org/10.1093/nar/gkx059
  • Zang, K., Wang, H., Hartl, F. U., & Hayer-Hartl, M. (2021). Scaffolding protein CcmM directs multiprotein phase separation in β-carboxysome biogenesis. Nature Structural & Molecular Biology, 28(11), 909–922. https://doi.org/10.1038/s41594-021-00676-5

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.