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Intermolecular domain swapping induces intein-mediated protein alternative splicing.

Aranko AS, Oeemig JS, Kajander T, Iwaï H
Nat Chem Biol 9 616-22 (2013)
Cited: 32 times
EuropePMC logo PMID: 23974115

Abstract

Protein sequences are diversified on the DNA level by recombination and mutation and can be further increased on the RNA level by alternative RNA splicing, involving introns that have important roles in many biological processes. The protein version of introns (inteins), which catalyze protein splicing, were first reported in the 1990s. The biological roles of protein splicing still remain elusive because inteins neither provide any clear benefits nor have an essential role in their host organisms. We now report protein alternative splicing, in which new protein sequences can be produced by protein recombination by intermolecular domain swapping of inteins, as elucidated by NMR spectroscopy and crystal structures. We demonstrate that intein-mediated protein alternative splicing could be a new strategy to increase protein diversity (that is, functions) without any modification in genetic backgrounds. We also exploited it as a post-translational protein conformation-driven switch of protein functions (for example, as highly specific protein interference).

Reviews - 4kl5 mentioned but not cited (2)

  1. Chemoenzymatic Semisynthesis of Proteins. Thompson RE, Muir TW. Chem Rev 120 3051-3126 (2020)
  2. The Evolution of Intein-Based Affinity Methods as Reflected in 30 years of Patent History. Prabhala SV, Gierach I, Wood DW. Front Mol Biosci 9 857566 (2022)

Articles - 4kl5 mentioned but not cited (3)

  1. Design of a Split Intein with Exceptional Protein Splicing Activity. Stevens AJ, Brown ZZ, Shah NH, Sekar G, Cowburn D, Muir TW. J Am Chem Soc 138 2162-2165 (2016)
  2. A promiscuous split intein with expanded protein engineering applications. Stevens AJ, Sekar G, Shah NH, Mostafavi AZ, Cowburn D, Muir TW. Proc Natl Acad Sci U S A 114 8538-8543 (2017)
  3. The crystal structure of the naturally split gp41-1 intein guides the engineering of orthogonal split inteins from cis-splicing inteins. Beyer HM, Mikula KM, Li M, Wlodawer A, Iwaï H. FEBS J 287 1886-1898 (2020)


Reviews citing this publication (6)

  1. Nature's recipe for splitting inteins. Aranko AS, Wlodawer A, Iwaï H. Protein Eng Des Sel 27 263-271 (2014)
  2. Structural and dynamical features of inteins and implications on protein splicing. Eryilmaz E, Shah NH, Muir TW, Cowburn D. J Biol Chem 289 14506-14511 (2014)
  3. The other side of the coin: the tumor-suppressive aspect of oncogenes and the oncogenic aspect of tumor-suppressive genes, such as those along the CCND-CDK4/6-RB axis. Lou X, Zhang J, Liu S, Xu N, Liao DJ. Cell Cycle 13 1677-1693 (2014)
  4. Synthetic Proteins and Peptides for the Direct Interrogation of α-Synuclein Posttranslational Modifications. Pratt MR, Abeywardana T, Marotta NP. Biomolecules 5 1210-1227 (2015)
  5. Genomic profiling to improve embryogenesis in the pig. Prather RS, Redel BK, Whitworth KM, Zhao MT. Anim Reprod Sci 149 39-45 (2014)
  6. Dissection of the MKK3 Functions in Human Cancer: A Double-Edged Sword? Piastra V, Pranteda A, Bossi G. Cancers (Basel) 14 483 (2022)

Articles citing this publication (21)

  1. Inteins: Nature's Gift to Protein Chemists. Shah NH, Muir TW. Chem Sci 5 446-461 (2014)
  2. Transient misfolding dominates multidomain protein folding. Borgia A, Kemplen KR, Borgia MB, Soranno A, Shammas S, Wunderlich B, Nettels D, Best RB, Clarke J, Schuler B. Nat Commun 6 8861 (2015)
  3. Salt-inducible Protein Splicing in cis and trans by Inteins from Extremely Halophilic Archaea as a Novel Protein-Engineering Tool. Ciragan A, Aranko AS, Tascon I, Iwaï H. J Mol Biol 428 4573-4588 (2016)
  4. Structure-based engineering and comparison of novel split inteins for protein ligation. Aranko AS, Oeemig JS, Zhou D, Kajander T, Wlodawer A, Iwaï H. Mol Biosyst 10 1023-1034 (2014)
  5. Protein splicing of a recombinase intein induced by ssDNA and DNA damage. Lennon CW, Stanger M, Belfort M. Genes Dev 30 2663-2668 (2016)
  6. Segmental isotopic labeling of a single-domain globular protein without any refolding step by an asparaginyl endopeptidase. Mikula KM, Tascón I, Tommila JJ, Iwaï H. FEBS Lett 591 1285-1294 (2017)
  7. Optical control of protein-protein interactions via blue light-induced domain swapping. Reis JM, Burns DC, Woolley GA. Biochemistry 53 5008-5016 (2014)
  8. Small Molecule-Induced Domain Swapping as a Mechanism for Controlling Protein Function and Assembly. Karchin JM, Ha JH, Namitz KE, Cosgrove MS, Loh SN. Sci Rep 7 44388 (2017)
  9. Structural Basis for the Persistence of Homing Endonucleases in Transcription Factor IIB Inteins. Iwaï H, Mikula KM, Oeemig JS, Zhou D, Li M, Wlodawer A. J Mol Biol 429 3942-3956 (2017)
  10. An Atypical Mechanism of Split Intein Molecular Recognition and Folding. Stevens AJ, Sekar G, Gramespacher JA, Cowburn D, Muir TW. J Am Chem Soc 140 11791-11799 (2018)
  11. Conserved residues that modulate protein trans-splicing of Npu DnaE split intein. Wu Q, Gao Z, Wei Y, Ma G, Zheng Y, Dong Y, Liu Y. Biochem J 461 247-255 (2014)
  12. Domain swapping oligomerization of thermostable c-type cytochrome in E. coli cells. Hayashi Y, Yamanaka M, Nagao S, Komori H, Higuchi Y, Hirota S. Sci Rep 6 19334 (2016)
  13. Engineering the hCRBPII Domain-Swapped Dimer into a New Class of Protein Switches. Ghanbarpour A, Pinger C, Esmatpour Salmani R, Assar Z, Santos EM, Nosrati M, Pawlowski K, Spence D, Vasileiou C, Jin X, Borhan B, Geiger JH. J Am Chem Soc 141 17125-17132 (2019)
  14. Mini-Intein Structures from Extremophiles Suggest a Strategy for Finding Novel Robust Inteins. Hiltunen MK, Beyer HM, Iwaï H. Microorganisms 9 1226 (2021)
  15. A streamlined method for preparing split intein for NMR study. Lee YZ, Lee YT, Lin YJ, Chen YJ, Sue SC. Protein Expr Purif 99 106-112 (2014)
  16. Allosteric Influence of Extremophile Hairpin Motif Mutations on the Protein Splicing Activity of a Hyperthermophilic Intein. Chiarolanzio KC, Pusztay JM, Chavez A, Zhao J, Xie J, Wang C, Mills KV. Biochemistry 59 2459-2467 (2020)
  17. Structural Basis for the Propagation of Homing Endonuclease-Associated Inteins. Beyer HM, Iwaï H. Front Mol Biosci 9 855511 (2022)
  18. The Convergence of the Hedgehog/Intein Fold in Different Protein Splicing Mechanisms. Beyer HM, Virtanen SI, Aranko AS, Mikula KM, Lountos GT, Wlodawer A, Ollila OHS, Iwaï H. Int J Mol Sci 21 E8367 (2020)
  19. Tying up the Loose Ends: A Mathematically Knotted Protein. Hsu SD, Lee YC, Mikula KM, Backlund SM, Tascón I, Goldman A, Iwaï H. Front Chem 9 663241 (2021)
  20. Cryptococcus neoformans Prp8 Intein: An In Vivo Target-Based Drug Screening System in Saccharomyces cerevisiae to Identify Protein Splicing Inhibitors and Explore Its Dynamics. Fernandes JAL, Zatti MDS, Arantes TD, Souza MFB, Santoni MM, Rossi D, Zanelli CF, Liu XQ, Bagagli E, Theodoro RC. J Fungi (Basel) 8 846 (2022)
  21. An alternative domain-swapped structure of the Pyrococcus horikoshii PolII mini-intein. Williams JE, Jaramillo MV, Li Z, Zhao J, Wang C, Li H, Mills KV. Sci Rep 11 11680 (2021)


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