Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system

Kükenshöner T, Wohlwend D, Niemoeller C, Dondapati P, Speck J, Adeniran AV, Nieth A, Gerhardt S, Einsle O, Müller K, Arndt KM (2014)
Journal of Structural Biology 186(3): 335-348.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ; ; ; ; ; ;
Abstract / Bemerkung
The design and selection of peptides targeting cellular proteins is challenging and often yields candidates with undesired properties. Therefore we deployed a new selection system based on the twin-arginine translocase (TAT) pathway of Escherichia coli, named hitchhiker translocation (HiT) selection. A pool of alpha-helix encoding sequences was designed and selected for interference with the coiled coil domain (CC) of a melanoma-associated basic-helix-loop-helix-leucine-zipper (bHLHLZ) protein, the microphthalmia associated transcription factor (MITF). One predominant sequence (iM10) was enriched during selection and showed remarkable protease resistance, high solubility and thermal stability while maintaining its specificity. Furthermore, it exhibited nanomolar range affinity towards the target peptide. A mutation screen indicated that target-binding helices of increased homodimer stability and improved expression rates were preferred in the selection process. The crystal structure of the iM10/MITF-CC heterodimer (2.1 angstrom) provided important structural insights and validated our design predictions. Importantly, iM10 did not only bind to the MITF coiled coil, but also to the markedly more stable HLHLZ domain of MITF. Characterizing the selected variants of the semi-rational library demonstrated the potential of the innovative bacterial selection approach. (C) 2014 Elsevier Inc. All rights reserved.
Erscheinungsjahr
Zeitschriftentitel
Journal of Structural Biology
Band
186
Zeitschriftennummer
3
Seite
335-348
ISSN
PUB-ID

Zitieren

Kükenshöner T, Wohlwend D, Niemoeller C, et al. Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system. Journal of Structural Biology. 2014;186(3):335-348.
Kükenshöner, T., Wohlwend, D., Niemoeller, C., Dondapati, P., Speck, J., Adeniran, A. V., Nieth, A., et al. (2014). Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system. Journal of Structural Biology, 186(3), 335-348. doi:10.1016/j.jsb.2014.03.002
Kükenshöner, T., Wohlwend, D., Niemoeller, C., Dondapati, P., Speck, J., Adeniran, A. V., Nieth, A., Gerhardt, S., Einsle, O., Müller, K., et al. (2014). Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system. Journal of Structural Biology 186, 335-348.
Kükenshöner, T., et al., 2014. Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system. Journal of Structural Biology, 186(3), p 335-348.
T. Kükenshöner, et al., “Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system”, Journal of Structural Biology, vol. 186, 2014, pp. 335-348.
Kükenshöner, T., Wohlwend, D., Niemoeller, C., Dondapati, P., Speck, J., Adeniran, A.V., Nieth, A., Gerhardt, S., Einsle, O., Müller, K., Arndt, K.M.: Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system. Journal of Structural Biology. 186, 335-348 (2014).
Kükenshöner, Tim, Wohlwend, Daniel, Niemoeller, Christoph, Dondapati, Padmarupa, Speck, Janina, Adeniran, Adebola V., Nieth, Anita, Gerhardt, Stefan, Einsle, Oliver, Müller, Kristian, and Arndt, Katja M. “Improving coiled coil stability while maintaining specificity by a bacterial hitchhiker selection system”. Journal of Structural Biology 186.3 (2014): 335-348.

4 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Designing helical peptide inhibitors of protein-protein interactions.
Rezaei Araghi R, Keating AE., Curr Opin Struct Biol 39(), 2016
PMID: 27123812
Controlling leucine-zipper partner recognition in cells through modification of a-g interactions.
Azuma Y, Kükenshöner T, Ma G, Yasunaga J, Imanishi M, Tanaka G, Nakase I, Maruno T, Kobayashi Y, Arndt KM, Matsuoka M, Futaki S., Chem Commun (Camb) 50(48), 2014
PMID: 24803110

63 References

Daten bereitgestellt von Europe PubMed Central.

Therapeutic peptides.
Albericio F, Kruger HG., Future Med Chem 4(12), 2012
PMID: 22917241
Comparison of in vivo selection and rational design of heterodimeric coiled coils.
Arndt KM, Pelletier JN, Muller KM, Pluckthun A, Alber T., Structure 10(9), 2002
PMID: 12220495
Antibodies from phage antibody libraries.
Bradbury AR, Marks JD., J. Immunol. Methods 290(1-2), 2004
PMID: 15261570

Bricogne, 2011
Design of peptide inhibitors that bind the bZIP domain of Epstein-Barr virus protein BZLF1.
Chen TS, Reinke AW, Keating AE., J. Mol. Biol. 408(2), 2011
PMID: 21354428
The CCP4 suite: programs for protein crystallography.
Collaborative Computational Project, Number 4., Acta Crystallogr. D Biol. Crystallogr. 50(Pt 5), 1994
PMID: 15299374
Crystal structure of GCN4-pIQI, a trimeric coiled coil with buried polar residues.
Eckert DM, Malashkevich VN, Kim PS., J. Mol. Biol. 284(4), 1998
PMID: 9837709
Coot: model-building tools for molecular graphics.
Emsley P, Cowtan K., Acta Crystallogr. D Biol. Crystallogr. 60(Pt 12 Pt 1), 2004
PMID: 15572765
Scaling and assessment of data quality.
Evans P., Acta Crystallogr. D Biol. Crystallogr. 62(Pt 1), 2005
PMID: 16369096
Induced heterodimerization and purification of two target proteins by a synthetic coiled-coil tag.
Fernandez-Rodriguez J, Marlovits TC., Protein Sci. 21(4), 2012
PMID: 22362668
Structural specificity in coiled-coil interactions.
Grigoryan G, Keating AE., Curr. Opin. Struct. Biol. 18(4), 2008
PMID: 18555680
Design of protein-interaction specificity gives selective bZIP-binding peptides.
Grigoryan G, Reinke AW, Keating AE., Nature 458(7240), 2009
PMID: 19370028
Characteristic features of amino acid residues in coiled-coil protein structures.
Gromiha MM, Parry DA., Biophys. Chem. 111(2), 2004
PMID: 15381307
Selectional and mutational scope of peptides sequestering the Jun-Fos coiled-coil domain.
Hagemann UB, Mason JM, Muller KM, Arndt KM., J. Mol. Biol. 381(1), 2008
PMID: 18586270
A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants.
Harbury PB, Zhang T, Kim PS, Alber T., Science 262(5138), 1993
PMID: 8248779
Targeting the c-Myc coiled coil with interfering peptides.
Jouaux EM, Schmidtkunz K, Muller KM, Arndt KM., J. Pept. Sci. 14(9), 2008
PMID: 18465834
A bacterial two-hybrid selection system for studying protein-DNA and protein-protein interactions.
Joung JK, Ramm EI, Pabo CO., Proc. Natl. Acad. Sci. U.S.A. 97(13), 2000
PMID: 10852947
XDS.
Kabsch W., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 2), 2010
PMID: 20124692
High-precision isothermal titration calorimetry with automated peak-shape analysis.
Keller S, Vargas C, Zhao H, Piszczek G, Brautigam CA, Schuck P., Anal. Chem. 84(11), 2012
PMID: 22530732
Simultaneous suppression of MITF and BRAF V600E enhanced inhibition of melanoma cell proliferation.
Kido K, Sumimoto H, Asada S, Okada SM, Yaguchi T, Kawamura N, Miyagishi M, Saida T, Kawakami Y., Cancer Sci. 100(10), 2009
PMID: 19659611
A general method to design dominant negatives to B-HLHZip proteins that abolish DNA binding.
Krylov D, Kasai K, Echlin DR, Taparowsky EJ, Arnheiter H, Vinson C., Proc. Natl. Acad. Sci. U.S.A. 94(23), 1997
PMID: 9356439
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7.
Langer G, Cohen SX, Lamzin VS, Perrakis A., Nat Protoc 3(7), 2008
PMID: 18600222
PROCHECK: a program to check the stereochemical quality of protein structures.
Laskowski RA, MacArthur MW, Moss DS, Thornton JM., J Appl Crystallogr 26(2), 1993
PMID: c6802
Lineage-specific transcriptional regulation of DICER by MITF in melanocytes.
Levy C, Khaled M, Robinson KC, Veguilla RA, Chen PH, Yokoyama S, Makino E, Lu J, Larue L, Beermann F, Chin L, Bosenberg M, Song JS, Fisher DE., Cell 141(6), 2010
PMID: 20550935
Predicting coiled coils from protein sequences.
Lupas A, Van Dyke M, Stock J., Science 252(5009), 1991
PMID: 2031185
Semirational design of Jun-Fos coiled coils with increased affinity: Universal implications for leucine zipper prediction and design.
Mason JM, Schmitz MA, Muller KM, Arndt KM., Proc. Natl. Acad. Sci. U.S.A. 103(24), 2006
PMID: 16754880
Role of hydrophobic and electrostatic interactions in coiled coil stability and specificity.
Mason JM, Hagemann UB, Arndt KM., Biochemistry 48(43), 2009
PMID: 19743874
Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability.
McGill GG, Horstmann M, Widlund HR, Du J, Motyckova G, Nishimura EK, Lin YL, Ramaswamy S, Avery W, Ding HF, Jordan SA, Jackson IJ, Korsmeyer SJ, Golub TR, Fisher DE., Cell 109(6), 2002
PMID: 12086670
Importance of leucine zipper domain of mi transcription factor (MITF) for differentiation of mast cells demonstrated using mi(ce)/mi(ce) mutant mice of which MITF lacks the zipper domain.
Morii E, Ogihara H, Kim DK, Ito A, Oboki K, Lee YM, Jippo T, Nomura S, Maeyama K, Lamoreux ML, Kitamura Y., Blood 97(7), 2001
PMID: 11264169
Refinement of macromolecular structures by the maximum-likelihood method.
Murshudov GN, Vagin AA, Dodson EJ., Acta Crystallogr. D Biol. Crystallogr. 53(Pt 3), 1997
PMID: 15299926
Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor.
Opdecamp K, Nakayama A, Nguyen MT, Hodgkinson CA, Pavan WJ, Arnheiter H., Development 124(12), 1997
PMID: 9199364
Main roads to melanoma.
Palmieri G, Capone M, Ascierto ML, Gentilcore G, Stroncek DF, Casula M, Sini MC, Palla M, Mozzillo N, Ascierto PA., J Transl Med 7(), 2009
PMID: 19828018
A bacterial-two-hybrid selection system for one-step isolation of intracellularly functional Nanobodies.
Pellis M, Pardon E, Zolghadr K, Rothbauer U, Vincke C, Kinne J, Dierynck I, Hertogs K, Leonhardt H, Messens J, Muyldermans S, Conrath K., Arch. Biochem. Biophys. 526(2), 2012
PMID: 22583807
Restricted leucine zipper dimerization and specificity of DNA recognition of the melanocyte master regulator MITF.
Pogenberg V, Ogmundsdottir MH, Bergsteinsdottir K, Schepsky A, Phung B, Deineko V, Milewski M, Steingrimsson E, Wilmanns M., Genes Dev. 26(23), 2012
PMID: 23207919
A synthetic coiled-coil interactome provides heterospecific modules for molecular engineering.
Reinke AW, Grant RA, Keating AE., J. Am. Chem. Soc. 132(17), 2010
PMID: 20387835
A gene network regulating lysosomal biogenesis and function.
Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, Di Malta C, Donaudy F, Embrione V, Polishchuk RS, Banfi S, Parenti G, Cattaneo E, Ballabio A., Science 325(5939), 2009
PMID: 19556463
Protein binding specificity versus promiscuity.
Schreiber G, Keating AE., Curr. Opin. Struct. Biol. 21(1), 2010
PMID: 21071205
TAT hitchhiker selection expanded to folding helpers, multimeric interactions and combinations with protein fragment complementation
Speck, Protein Eng. Des. Sel. (), 2012
The semidominant Mi(b) mutation identifies a role for the HLH domain in DNA binding in addition to its role in protein dimerization.
Steingrimsson E, Nii A, Fisher DE, Ferre-D'Amare AR, McCormick RJ, Russell LB, Burley SK, Ward JM, Jenkins NA, Copeland NG., EMBO J. 15(22), 1996
PMID: 8947051
Melanocytes and the microphthalmia transcription factor network.
Steingrimsson E, Copeland NG, Jenkins NA., Annu. Rev. Genet. 38(), 2004
PMID: 15568981
Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene.
Tassabehji M, Newton VE, Read AP., Nat. Genet. 8(3), 1994
PMID: 7874167
TFE3, a transcription factor homologous to microphthalmia, is a potential transcriptional activator of tyrosinase and TyrpI genes.
Verastegui C, Bertolotto C, Bille K, Abbe P, Ortonne JP, Ballotti R., Mol. Endocrinol. 14(3), 2000
PMID: 10707962
Automated structure solution with autoSHARP.
Vonrhein C, Blanc E, Roversi P, Bricogne G., Methods Mol. Biol. 364(), 2007
PMID: 17172768
Extended knobs-into-holes packing in classical and complex coiled-coil assemblies.
Walshaw J, Woolfson DN., J. Struct. Biol. 144(3), 2003
PMID: 14643203
Potent D-peptide inhibitors of HIV-1 entry.
Welch BD, VanDemark AP, Heroux A, Hill CP, Kay MS., Proc. Natl. Acad. Sci. U.S.A. 104(43), 2007
PMID: 17942675
Reengineering natural design by rational design and in vivo library selection: the HLH subdomain in bHLHZ proteins is a unique requirement for DNA-binding function.
Xu J, De Jong AT, Chen G, Chow HK, Damaso CO, Schwartz Mittelman A, Shin JA., Protein Eng. Des. Sel. 23(5), 2010
PMID: 20086039
Photocontrol of coiled-coil proteins in living cells.
Zhang F, Timm KA, Arndt KM, Woolley GA., Angew. Chem. Int. Ed. Engl. 49(23), 2010
PMID: 20419720

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 24631970
PubMed | Europe PMC

Suchen in

Google Scholar