Cold shock proteins improve E. coli cell-free synthesis in terms of soluble yields of aggregation-prone proteins.
aggregation-prone proteins
cell-free protein synthesis
cold shock proteins
Journal
Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
11
11
2019
revised:
05
03
2020
accepted:
08
03
2020
pubmed:
13
3
2020
medline:
28
8
2021
entrez:
13
3
2020
Statut:
ppublish
Résumé
Protein folding is usually slowed-down at low temperatures, and thus low-temperature expression is an effective strategy to improve the soluble yield of aggregation-prone proteins. In this study, we investigated the effects of a variety of cold shock proteins and domains (Csps) on an Escherichia coli cell extract-based cell-free protein synthesis system (CF). Most of the 12 Csps that were successfully prepared dramatically improved the protein yields, by factors of more than 5 at 16°C and 2 at 23°C, to levels comparable to those obtained at 30°C. Their stimulatory effects were complementary to each other, while CspD and CspH were inhibitory. The Csps' effects correlated well with their Pfam CSD family scores (PF00313.22). All of the investigated Csps, except CspH, similarly possessed RNA binding and chaperon activities and increased the messenger RNA amount irrespective of their effect, suggesting that the proper balance between these activities was required for the enhancement. Unexpectedly, the 5'-untranslated region of cspA was less effective as the leader sequence. Our results demonstrated that the use of the Csps presented in this study will provide a simple and highly effective strategy for the CF, to improve the soluble yields of aggregation-prone proteins.
Substances chimiques
Cold Shock Proteins and Peptides
0
Protein Aggregates
0
Recombinant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1628-1639Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Abrusci, P., Chiarelli, L. R., Galizzi, A., Fermo, E., Bianchi, P., Zanella, A., & Valentini, G. (2007). Erythrocyte adenylate kinase deficiency: Characterization of recombinant mutant forms and relationship with nonspherocytic hemolytic anemia. Experimental Hematology, 35(8), 1182-1189. https://doi.org/10.1016/j.exphem.2007.05.004
Aoki, M., Matsuda, T., Tomo, Y., Miyata, Y., Inoue, M., Kigawa, T., & Yokoyama, S. (2009). Automated system for high-throughput protein production using the dialysis cell-free method. Protein Expression and Purification, 68(2), 128-136. https://doi.org/10.1016/j.pep.2009.07.017
Bae, W., Xia, B., Inouye, M., & Severinov, K. (2000). Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proceedings of the National Academy of Sciences, USA, 97(14), 7784-7789. https://doi.org/10.1073/pnas.97.14.7784
Buntru, M., Vogel, S., Spiegel, H., & Schillberg, S. (2014). Tobacco BY-2 cell-free lysate: An alternative and highly-productive plant-based in vitro translation system. BMC Biotechnology, 14(1), 37. https://doi.org/10.1186/1472-6750-14-37
Dougherty, W. G., Cary, S. M., & Parks, T. D. (1989). Molecular genetic analysis of a plant virus polyprotein cleavage site: A model. Virology, 171(2), 356-364. https://doi.org/10.1016/0042-6822(89)90603-x
Eddy, S. R. (2011). Accelerated profile HMM searches. PLoS Computational Biology, 7(10):e1002195. https://doi.org/10.1371/journal.pcbi.1002195
El-Gebali, S., Mistry, J., Bateman, A., Eddy, S. R., Luciani, A., Potter, S. C., … Finn, R. D. (2019). The Pfam protein families database in 2019. Nucleic Acids Research, 47(D1), D427-D432. https://doi.org/10.1093/nar/gky995
Fang, L., Jiang, W., Bae, W., & Inouye, M. (1997). Promoter-independent cold-shock induction of cspA and its derepression at 37 degrees C by mRNA stabilization. Molecular Microbiology, 23(2), 355-364. https://doi.org/10.1046/j.1365-2958.1997.2351592.x
Freischmidt, A., Hiltl, J., Kalbitzer, H. R., & Horn-Katting, G. (2013). Enhanced in vitro translation at reduced temperatures using a cold-shock RNA motif. Biotechnology Letters, 35(3), 389-395. https://doi.org/10.1007/s10529-012-1091-4
Giuliodori, A. M., Brandi, A., Giangrossi, M., Gualerzi, C. O., & Pon, C. L. (2007). Cold-stress-induced de novo expression of infC and role of IF3 in cold-shock translational bias. RNA, 13(8), 1355-1365. https://doi.org/10.1261/rna.455607
Giuliodori, A. M., Brandi, A., Gualerzi, C. O., & Pon, C. L. (2004). Preferential translation of cold-shock mRNAs during cold adaptation. RNA, 10(2), 265-276. https://doi.org/10.1261/rna.5164904
Giuliodori, A. M., Fabbretti, A., & Gualerzi, C. (2019). Cold-responsive regions of paradigm cold-shock and non-cold-shock mRNAs responsible for cold shock translational bias. International Journal of Molecular Sciences, 20(3), 457. https://doi.org/10.3390/ijms20030457
Giuliodori, A. M., Di Pietro, F., Marzi, S., Masquida, B., Wagner, R., Romby, P., … Pon, C. L. (2010). The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. Molecular Cell, 37(1), 21-33. https://doi.org/10.1016/j.molcel.2009.11.033
Gualerzi, C. O., Giuliodori, A. M., & Pon, C. L. (2003). Transcriptional and post-transcriptional control of cold-shock genes. Journal of Molecular Biology, 331(3), 527-539. https://doi.org/10.1016/s0022-2836(03)00732-0
Hankins, J. S., Zappavigna, C., Prud'homme-Genereux, A., & Mackie, G. A. (2007). Role of RNA structure and susceptibility to RNase E in regulation of a cold shock mRNA, cspA mRNA. Journal of Bacteriology, 189(12), 4353-4358. https://doi.org/10.1128/JB.00193-07
Hayashi, K., & Kojima, C. (2008). pCold-GST vector: A novel cold-shock vector containing GST tag for soluble protein production. Protein Expression and Purification, 62(1), 120-127. https://doi.org/10.1016/j.pep.2008.07.007
Hofweber, R., Horn, G., Langmann, T., Balbach, J., Kremer, W., Schmitz, G., & Kalbitzer, H. R. (2005). The influence of cold shock proteins on transcription and translation studied in cell-free model systems. FEBS Journal, 272(18), 4691-4702. https://doi.org/10.1111/j.1742-4658.2005.04885.x
Horn, G., Hofweber, R., Kremer, W., & Kalbitzer, H. R. (2007). Structure and function of bacterial cold shock proteins. Cellular and Molecular Life Sciences, 64(12), 1457-1470. https://doi.org/10.1007/s00018-007-6388-4
Howard, S. P., Estrozi, L. F., Bertrand, Q., Contreras-Martel, C., Strozen, T., Job, V., … Dessen, A. (2019). Structure and assembly of pilotin-dependent and -independent secretins of the type II secretion system. PLOS Pathogens, 15(5):e1007731. https://doi.org/10.1371/journal.ppat.1007731
Inomata, K., Kamoshida, H., Ikari, M., Ito, Y., & Kigawa, T. (2017). Impact of cellular health conditions on the protein folding state in mammalian cells. Chemical Communications, 53(81), 11245-11248. https://doi.org/10.1039/c7cc06004a
Jiang, W., Hou, Y., & Inouye, M. (1997). CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. Journal of Biological Chemistry, 272(1), 196-202. https://doi.org/10.1074/jbc.272.1.196
Jones, P. G., VanBogelen, R. A., & Neidhardt, F. C. (1987). Induction of proteins in response to low temperature in Escherichia coli. Journal of Bacteriology, 169(5), 2092-2095. https://doi.org/10.1128/jb.169.5.2092-2095.1987
Kigawa, T., Inoue, M., Aoki, M., Matsuda, T., Yabuki, T., Seki, E., … Yokoyama, S. (2007). The use of the Escherichia coli cell-free protein synthesis for structural biology and structural proteomics. In A. S. Spirin & J. R. Swartz (Eds.), Cell-free protein synthesis methods and protocols (pp. 99-109). Weinheim: Wiley-VCH.
Kigawa, T., Yabuki, T., Matsuda, N., Matsuda, T., Nakajima, R., Tanaka, A., & Yokoyama, S. (2004). Preparation of Escherichia coli cell extract for highly productive cell-free protein expression. Journal of Structural and Functional Genomics, 5(1-2), 63-68. https://doi.org/10.1023/B:JSFG.0000029204.57846.7d
Kim, D.-M., Kigawa, T., Choi, C.-Y., & Yokoyama, S. (1996). A highly efficient cell-free protein synthesis system from Escherichia coli. European Journal of Biochemistry, 239(3), 881-886. https://doi.org/10.1111/j.1432-1033.1996.0881u.x
Kim, M. H., & Imai, R. (2015). Determination of RNA chaperone activity using an Escherichia coli mutant. Methods in Molecular Biology, 1259, 117-123. https://doi.org/10.1007/978-1-4939-2214-7_8
Kim, S. H., Heo, M. A., Kim, Y. J., Kim, S. Y., Neelamegam, R., & Lee, S. G. (2008). The effect of the cspA 5'-untranslated region on recombinant protein production at low temperature. Biotechnology and Bioprocess Engineering, 13(3), 366-371. https://doi.org/10.1007/s12257-008-0027-2
Kukimoto-Niino, M., Takagi, T., Akasaka, R., Murayama, K., Uchikubo-Kamo, T., Terada, T., … Yokoyama, S. (2006). Crystal structure of the RUN domain of the RAP2-interacting protein x. Journal of Biological Chemistry, 281(42), 31843-31853. https://doi.org/10.1074/jbc.M604960200
Lindquist, J. A., & Mertens, P. R. (2018). Cold shock proteins: From cellular mechanisms to pathophysiology and disease. Cell Communication and Signaling, 16(1), 63. https://doi.org/10.1186/s12964-018-0274-6
Madin, K., Sawasaki, T., Ogasawara, T., & Endo, Y. (2000). A highly efficient and robust cell-free protein synthesis system prepared from wheat embryos: Plants apparently contain a suicide system directed at ribosomes. Proceedings of the National Academy of Sciences of the United States of America, 97(2), 559-564. https://doi.org/10.1073/pnas.97.2.559
Matsuda, T., Koshiba, S., Tochio, N., Seki, E., Iwasaki, N., Yabuki, T., … Kigawa, T. (2007). Improving cell-free protein synthesis for stable-isotope labeling. Journal of Biomolecular NMR, 37(3), 225-229. https://doi.org/10.1007/s10858-006-9127-5
Michaux, C., Holmqvist, E., Vasicek, E., Sharan, M., Barquist, L., Westermann, A. J., … Vogel, J. (2017). RNA target profiles direct the discovery of virulence functions for the cold-shock proteins CspC and CspE. Proceedings of the National Academy of Sciences, USA, 114(26), 6824-6829. https://doi.org/10.1073/pnas.1620772114
Mikami, S., Masutani, M., Sonenberg, N., Yokoyama, S., & Imataka, H. (2006). An efficient mammalian cell-free translation system supplemented with translation factors. Protein Expression and Purification, 46(2), 348-357. https://doi.org/10.1016/j.pep.2005.09.021
Nameki, N., Tochio, N., Koshiba, S., Inoue, M., Yabuki, T., Aoki, M., … Yokoyama, S. (2005). Solution structure of the PWWP domain of the hepatoma-derived growth factor family. Protein Science, 14(3), 756-764. https://doi.org/10.1110/ps.04975305
Numata, K., Motoda, Y., Watanabe, S., Osanai, T., & Kigawa, T. (2015). Co-expression of two polyhydroxyalkanoate synthase subunits from Synechocystis sp. PCC 6803 by cell-free synthesis and their specific activity for polymerization of 3-hydroxybutyryl-coenzyme A. Biochemistry, 54(6), 1401-1407. https://doi.org/10.1021/bi501560b
Pey, A. L., Mesa-Torres, N., Chiarelli, L. R., & Valentini, G. (2013). Structural and energetic basis of protein kinetic destabilization in human phosphoglycerate kinase 1 deficiency. Biochemistry, 52(7), 1160-1170. https://doi.org/10.1021/bi301565m
Phadtare, S., & Inouye, M. (1999). Sequence-selective interactions with RNA by CspB, CspC and CspE, members of the CspA family of Escherichia coli. Molecular Microbiology, 33(5), 1004-1014. https://doi.org/10.1046/j.1365-2958.1999.01541.x
Phadtare, S., Inouye, M., & Severinov, K. (2002). The nucleic acid melting activity of Escherichia coli CspE is critical for transcription antitermination and cold acclimation of cells. Journal of Biological Chemistry, 277(9), 7239-7245. https://doi.org/10.1074/jbc.M111496200
Phadtare, S., & Severinov, K. (2005). Nucleic acid melting by Escherichia coli CspE. Nucleic Acids Research, 33(17), 5583-5590. https://doi.org/10.1093/nar/gki859
Qing, G., Ma, L. C., Khorchid, A., Swapna, G. V., Mal, T. K., Takayama, M. M., … Inouye, M. (2004). Cold-shock induced high-yield protein production in Escherichia coli. Nature Biotechnology, 22(7), 877-882. https://doi.org/10.1038/nbt984
Rennella, E., Sara, T., Juen, M., Wunderlich, C., Imbert, L., Solyom, Z., … Brutscher, B. (2017). RNA binding and chaperone activity of the E. coli cold-shock protein CspA. Nucleic Acids Research, 45(7), 4255-4268. https://doi.org/10.1093/nar/gkx044
Sachs, R., Max, K. E., Heinemann, U., & Balbach, J. (2012). RNA single strands bind to a conserved surface of the major cold shock protein in crystals and solution. RNA, 18(1), 65-76. https://doi.org/10.1261/rna.02809212
Sasaki, K., & Imai, R. (2011). Pleiotropic roles of cold shock domain proteins in plants. Frontiers in Plant Science, 2, 116. https://doi.org/10.3389/fpls.2011.00116
Seki, E., Matsuda, N., Yokoyama, S., & Kigawa, T. (2008). Cell-free protein synthesis system from Escherichia coli cells cultured at decreased temperatures improves productivity by decreasing DNA template degradation. Analytical Biochemistry, 377(2), 156-161. https://doi.org/10.1016/j.ab.2008.03.001
Shirano, Y., & Shibata, D. (1990). Low-temperature cultivation of Escherichia coli carrying a rice lipoxygenasqe L-2 Cdna produces a soluble and active enzyme at a high-level. FEBS Letters, 271(1-2), 128-130. https://doi.org/10.1016/0014-5793(90)80388-Y
Suzuki, M., Mao, L., & Inouye, M. (2007). Single protein production (SPP) system in Escherichia coli. Nature Protocols, 2(7), 1802-1810. https://doi.org/10.1038/nprot.2007.252
Tarui, H., Imanishi, S., & Hara, T. (2000). A novel cell-free translation/glycosylation system prepared from insect cells. Journal of Bioscience and Bioengineering, 90(5), 508-514. https://doi.org/10.1016/S1389-1723(01)80031-1
Thoring, L., Dondapati, S. K., Stech, M., Wüstenhagen, D. A., & Kubick, S. (2017). High-yield production of “difficult-to-express” proteins in a continuous exchange cell-free system based on CHO cell lysates. Scientific Reports, 7(1):11710. https://doi.org/10.1038/s41598-017-12188-8
Vopel, T., & Makhatadze, G. I. (2012). Enzyme activity in the crowded milieu. PLOS One, 7(6):e39418. https://doi.org/10.1371/journal.pone.0039418
Xia, B., Ke, H., & Inouye, M. (2001). Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Molecular Microbiology, 40(1), 179-188. https://doi.org/10.1046/j.1365-2958.2001.02372.x
Yabuki, T., Motoda, Y., Hanada, K., Nunokawa, E., Saito, M., Seki, E., … Yokoyama, S. (2007). A robust two-step PCR method of template DNA production for high-throughput cell-free protein synthesis. Journal of Structural and Functional Genomics, 8(4), 173-191. https://doi.org/10.1007/s10969-007-9038-z
Yamanaka, K., Mitta, M., & Inouye, M. (1999). Mutation analysis of the 5′ untranslated region of the cold shock cspA mRNA of Escherichia coli. Journal of Bacteriology, 181(20), 6284-6291.
Yamanaka, K., Zheng, W., Crooke, E., Wang, Y. H., & Inouye, M. (2001). CspD, a novel DNA replication inhibitor induced during the stationary phase in Escherichia coli. Molecular Microbiology, 39(6), 1572-1584. https://doi.org/10.1046/j.1365-2958.2001.02345.x
Zhang, Y., Burkhardt, D. H., Rouskin, S., Li, G. W., Weissman, J. S., & Gross, C. A. (2018). A stress response that monitors and regulates mRNA structure is central to cold shock adaptation. Molecular Cell, 70(2), 274-286.e277. https://doi.org/10.1016/j.molcel.2018.02.035
Zubay, G. (1973). In vitro synthesis of protein in microbial systems. Annual Review of Genetics, 7, 267-287. https://doi.org/10.1146/annurev.ge.07.120173.001411