Identification of SLiMs: Mapping and characterizing motif-based protein interactions

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(1)Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1981. Identification of SLiMs: Mapping and characterizing motif-based protein interactions MUHAMMAD ALI. ACTA UNIVERSITATIS UPSALIENSIS UPPSALA 2020. ISSN 1651-6214 ISBN 978-91-513-1048-0 urn:nbn:se:uu:diva-423197.

(2) Dissertation presented at Uppsala University to be publicly examined in Room A1:111a, BMC, Husargatan 3, Uppsala, Friday, 11 December 2020 at 09:00 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Professor Shoshana Wodak (VUB Center for Structural Biology-Universiteit Brussel). Abstract Ali, M. 2020. Identification of SLiMs: Mapping and characterizing motif-based protein interactions. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1981. 78 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-1048-0. During the last twenty years it has become evident that about 35-40% of amino acids in the proteome are in regions that have evolved to remain unstructured. These intrinsically disordered regions contain short linear motifs (SLiMs), which serve as docking sites for protein-protein interactions. SLiMs often mediate low-to-medium affinity interactions that are transient in their nature. The characteristics of SLiM-based interactions make them difficult to be captured using conventional approaches like affinity-purification coupled to mass spectrometry or yeast-twohybrid. We therefore used and developed a dedicated method for large-scale screening of SLiMbased interactions termed proteomic peptide phage display (ProP-PD). Using ProP-PD, We identified large sets of ligands, for the binding pocket of shank1 PDZ domain, containing C-terminal or internal binding motifs and established the consensus motifs to be xTxL/F-COOH and xTxFx respectively. We further validated interactions using biophysical affinity determinations and pulldown experiments. Using X-ray crystallization, we uncovered that shank1 PDZ binds to internal xTxFx motifs using a binding mode similar to that for Cterminal peptides. Adding a level of complexity, we explored interactions of the multiple binding pocket containing FERM domains from four closely related proteins: ezrin, radixin, moesin and merlin. We found hundreds of FERM ligands, which contained binding motifs of at least four different classes. By combining docking simulations with experiments, we established ligands binding to different pockets, and uncovered a complex interplay between distinct pockets. We further developed an optimized version of a phage library that displays intrinsically disordered regions of the human proteome. We benchmarked the library using a set of protein domains and reported better recovery of known SLiM-based interactions. Furthermore, we highlighted the functional aspects of identified SLiMs, in the case of nuclear localization signals, found for binding to importin-subunit alpha-3. Finally, we validated predicted binding of SLiMs in the Sars-CoV-2 host receptor ACE2, which illustrates the importance of fundamental knowledge for SLiMs and their binding partners. This work, taken together, contributes with method development for expansion of motifs based interactomes and provide insights into the plastic yet selective nature of peptide binding proteins. Keywords: Phage display, protein-protein interactions, short linear motifs, PDZ, FERM, affinity, x-ray crystallization, molecular docking, NLS Muhammad Ali, Department of Chemistry - BMC, Biochemistry, Box 576, Uppsala University, SE-75123 Uppsala, Sweden. © Muhammad Ali 2020 ISSN 1651-6214 ISBN 978-91-513-1048-0 urn:nbn:se:uu:diva-423197 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-423197).

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(88) Contents. 1. Introduction .......................................................................................... 11 1.1 Short Linear Motifs (SLiMs) and SLiM-mediated interactions ...... 12 1.1.1 IDRs ....................................................................................... 12 1.1.2 SLiMs ..................................................................................... 13 1.2 SLiM-binding modular domains ..................................................... 14 1.2.1 The PDZ domain .................................................................... 14 1.2.2 The FERM domain................................................................. 17 1.2.3 KPNA4 armadillo repeats ...................................................... 19 1.3 Profiling protein-protein interactions .............................................. 21 1.3.1 Mass spectrometry based approaches .................................... 21 1.3.2 Yeast-two-hybrid ................................................................... 22 1.3.3 Peptide arrays ......................................................................... 23 1.3.4 Peptide phage display............................................................. 24 1.3.5 Proteomic peptide-phage display ........................................... 26 1.4 Characterization of SLiM-based PPIs ............................................ 28 1.4.1 Validations in biological context ........................................... 28 1.4.2 Biophysical affinity measurement ......................................... 29 1.4.3 Structural insights .................................................................. 33. 2. Present Investigations .......................................................................... 35 2.1 Plasticity of ligands binding of shank1 PDZ domain (Paper I) ....... 36 2.1.1 Shank1 PDZ recognizes similar C-terminal and internal PDZbms ............................................................................................... 36 2.1.2 Validating and characterizing the interactions with Cterminal and internal PDZbms ............................................................. 37 2.1.3 Structural details of the interaction between the internal PDZbm of ARAP3 and shank1 ........................................................... 40 2.1.4 Concluding remarks on paper I .............................................. 40 2.2 Specificity and modulation of the SLiM-based interactions with multi-binding pockets domain (Paper II).................................................. 42 2.2.1 Identification of SLiM-based interactions for the FERM domains of the ERMs and merlin ........................................................ 43 2.2.2 Validating interactions ........................................................... 44 2.2.3 Dissecting moesin FERM peptides binding through competition experiments ...................................................................... 45 2.2.4 Elucidating the details of the interactions through docking... 48.

(89) 2.2.5 The -FYDF- containing ZNF622 and BTBD7 peptides bind to the F3a site ....................................................................................... 48 2.2.6 KIRREL3 and TBX4 like peptides dock at F3b site.............. 49 2.2.7 Communication between different FERM binding sites........ 50 2.2.8 Concluding remarks on paper II............................................. 51 2.3 Connecting the proteins at the plasma membrane ........................... 53 2.4 PDZbms and putative FERM binding motifs in ACE2 link SARS-CoV-2 host cell receptor to cellular trafficking (Paper III) ........... 55 2.4.1 Validating the ACE2 PDZbm ................................................ 55 2.4.2 Testing the predicted PTB binding NP.F motif ..................... 56 2.5 Into the future of interaction profiling (Paper IV) ........................... 57 2.5.1 HD2 library design, construction and quality ........................ 57 2.5.2 Benchmarking the novel ProP-PD resource........................... 59 2.5.3 Zooming into one case: the interactions of KPNA4 with NLSs …. ............................................................................................... 61 2.5.4 Concluding remarks on paper IV ........................................... 62 3. Concluding remarks and future perspectives ....................................... 64. 4. Populär sammanfattning på svenska .................................................... 66. 5. Acknowledgements .............................................................................. 69. 6. References ............................................................................................ 71.

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