Targeting of parvulin interactors by diazirine mediated cross-linking discloses a cellular role of human Par14/17 in actin polymerization

References

Ananthakrishnan, R. and Ehrlicher, A. (2007). The forces behind cell movement. Int. J. Biol. Sci. 3, 303–317.10.7150/ijbs.3.303Search in Google Scholar PubMed PubMed Central

Black, D.J., Tran, Q.-K., Keightley, A., Chinawalkar, A., McMullin, C., and Persechini, A. (2019). Evaluating calmodulin-protein interactions by rapid photoactivated cross-linking in live cells metabolically labeled with photo-methionine. J. Proteome. Res. 18, 3780–3791.10.1021/acs.jproteome.9b00510Search in Google Scholar PubMed

Burgardt, N.I., Schmidt, A., Manns, A., Schutkowski, A., Jahreis, G., Lin, Y.-J., Schulze, B., Masch, A., Lücke, C., and Weiwad, M. (2015). Parvulin 17-catalyzed tubulin polymerization is regulated by calmodulin in a calcium-dependent manner*. J. Biol. Chem. 290, 16708–16722.10.1074/jbc.M114.593228Search in Google Scholar PubMed PubMed Central

Colquhoun, D. (2014). An investigation of the false discovery rate and the misinterpretation of p-values. R. Soc. Open Sci. 1, 140216.10.1098/rsos.140216Search in Google Scholar PubMed PubMed Central

Cox, J. and Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372.10.1038/nbt.1511Search in Google Scholar PubMed

Cox, J., Neuhauser, N., Michalski, A., Scheltema, R.A., Olsen, J.V., and Mann, M. (2011). Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805.10.1021/pr101065jSearch in Google Scholar PubMed

Cox, J., Hein, M.Y., Luber, C.A., Paron, I., Nagaraj, N., and Mann, M. (2014). Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 13, 2513–2526.10.1074/mcp.M113.031591Search in Google Scholar PubMed PubMed Central

Drozdetskiy, A., Cole, C., Procter, J., and Barton, G.J. (2015). JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43, W389–94.10.1093/nar/gkv332Search in Google Scholar PubMed PubMed Central

Fujiyama, S., Yanagida, M., Hayano, T., Miura, Y., Isobe, T., Fujimori, F., Uchida, T., and Takahashi, N. (2002). Isolation and proteomic characterization of human Parvulin-associating preribosomal ribonucleoprotein complexes. J. Biol. Chem. 277, 23773–23780.10.1074/jbc.M201181200Search in Google Scholar PubMed

Fujiyama-Nakamura, S., Yoshikawa, H., Homma, K., Hayano, T., Tsujimura-Takahashi, T., Izumikawa, K., Ishikawa, H., Miyazawa, N., Yanagida, M., Miura, Y., et al. (2009). Parvulin (Par14), a peptidyl-prolyl cis-trans isomerase, is a novel rRNA processing factor that evolved in the metazoan lineage. Mol. Cell. Proteomics 8, 1552–1565.10.1074/mcp.M900147-MCP200Search in Google Scholar PubMed PubMed Central

Häupl, B., Ihling, C.H., and Sinz, A. (2017). Combining affinity enrichment, cross-linking with photo amino acids, and mass spectrometry for probing protein kinase D2 interactions. Proteomics 17, e1600459.10.1002/pmic.201600459Search in Google Scholar PubMed

Iacobucci, C., Götze, M., Piotrowski, C., Arlt, C., Rehkamp, A., Ihling, C., Hage, C., and Sinz, A. (2018). Carboxyl-photo-reactive MS-cleavable cross-linkers. Unveiling a hidden aspect of diazirine-based reagents. Anal. Chem. 90, 4, 2805–2809.10.1021/acs.analchem.7b04915Search in Google Scholar PubMed

Karpen, S.C. (2017). P value problems. Am. J. Pharm. Educ. 81, 6570.10.5688/ajpe6570Search in Google Scholar PubMed PubMed Central

Keilhauer, E.C., Hein, M.Y., and Mann, M. (2015). Accurate protein complex retrieval by affinity enrichment mass spectrometry (AE-MS) rather than affinity purification mass spectrometry (AP-MS). Mol. Cell. Proteomics 14, 120–135.10.1074/mcp.M114.041012Search in Google Scholar PubMed PubMed Central

Kessler, D., Papatheodorou, P., Stratmann, T., Dian, E.A., Hartmann-Fatu, C., Rassow, J., Bayer, P., and Mueller, J.W. (2007). The DNA binding parvulin Par17 is targeted to the mitochondrial matrix by a recently evolved prepeptide uniquely present in Hominidae. BMC Biol. 5, 37.10.1186/1741-7007-5-37Search in Google Scholar PubMed PubMed Central

Matena, A., Rehic, E., Hönig, D., Kamba, B., and Bayer, P. (2018). Structure and function of the human parvulins Pin1 and Par14/17. Biol. Chem. 399, 101–125.10.1515/hsz-2017-0137Search in Google Scholar PubMed

Mayor, R. and Etienne-Manneville, S. (2016). The front and rear of collective cell migration. Nat. Rev. Mol. Cell Biol. 17, 97 EP.10.1038/nrm.2015.14Search in Google Scholar PubMed

Michalski, A., Damoc, E., Lange, O., Denisov, E., Nolting, D., Müller, M., Viner, R., Schwartz, J., Remes, P., Belford, M., et al. (2012). Ultra high resolution linear ion trap Orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes. Mol. Cell. Proteomics 11, O111.013698.10.1074/mcp.O111.013698Search in Google Scholar PubMed PubMed Central

Mueller, J.W., Kessler, D., Neumann, D., Stratmann, T., Papatheodorou, P., Hartmann-Fatu, C., and Bayer, P. (2006). Characterization of novel elongated Parvulin isoforms that are ubiquitously expressed in human tissues and originate from alternative transcription initiation. BMC Mol. Biol. 7, 9.10.1186/1471-2199-7-9Search in Google Scholar PubMed PubMed Central

Olsen, J.V., de Godoy, L.M.F., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005). Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010–2021.10.1074/mcp.T500030-MCP200Search in Google Scholar PubMed

Piotrowski, C., Ihling, C.H., and Sinz, A. (2015). Extending the cross-linking/mass spectrometry strategy: facile incorporation of photo-activatable amino acids into the model protein calmodulin in Escherichia coli cells. Methods 89, 121–127.10.1016/j.ymeth.2015.02.012Search in Google Scholar

Rappsilber, J., Mann, M., and Ishihama, Y. (2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896–1906.10.1038/nprot.2007.261Search in Google Scholar

Rehkamp, A., Tänzler, D., Iacobucci, C., Golbik, R.P., Ihling, C.H., and Sinz, A. (2018). Molecular details of retinal guanylyl cyclase 1/GCAP-2 interaction. Front. Mol. Neurosci. 11, 330.10.3389/fnmol.2018.00330Search in Google Scholar

Reimer, T. (2003). Cellular localization and function of peptidyl-prolyl cis-trans isomerase hPar14. Dissertation (Halle-Wittenberg).Search in Google Scholar

Reimer, T., Weiwad, M., Schierhorn, A., Ruecknagel, P.-K., Rahfeld, J.-U., Bayer, P., and Fischer, G. (2003). Phosphorylation of the N-terminal domain regulates subcellular localization and DNA binding properties of the peptidyl-prolyl cis/trans isomerase hPar14. J. Mol. Biol. 330, 955–966.10.1016/S0022-2836(03)00713-7Search in Google Scholar

Ruoho, A.E., Kiefer, H., Roeder, P.E., and Singer, S.J. (1973). The mechanism of photoaffinity labeling. Proc. Natl. Acad. Sci. USA 70, 2567–2571.10.1073/pnas.70.9.2567Search in Google Scholar PubMed PubMed Central

Saeed, U., Kim, J., Piracha, Z.Z., Kwon, H., Jung, J., Chwae, Y.-J., Park, S., Shin, H.-J., and Kim, K. (2019). Parvulin 14 and parvulin 17 bind to HBx and cccDNA and upregulate hepatitis B virus replication from cccDNA to virion in an HBx-dependent manner. J. Virol. 93, e01840-18.10.1128/JVI.01840-18Search in Google Scholar PubMed PubMed Central

Saningong, A.D. and Bayer, P. (2015). Human DNA-binding peptidyl-prolyl cis/trans isomerase Par14 is cell cycle dependently expressed and associates with chromatin in vivo. BMC Biochem. 16, 4.10.1186/s12858-015-0033-xSearch in Google Scholar PubMed PubMed Central

Sekerina, E., Rahfeld, J.U., Müller, J., Fanghänel, J., Rascher, C., Fischer, G., and Bayer, P. (2000). NMR solution structure of hPar14 reveals similarity to the peptidyl prolyl cis/trans isomerase domain of the mitotic regulator hPin1 but indicates a different functionality of the protein. J. Mol. Biol. 301, 1003–1017.10.1006/jmbi.2000.4013Search in Google Scholar PubMed

Shellard, A. and Mayor, R. (2019). Supracellular migration – beyond collective cell migration. J. Cell Sci. 132, jcs226142.10.1242/jcs.226142Search in Google Scholar PubMed

Stark, C., Breitkreutz, B.-J., Reguly, T., Boucher, L., Breitkreutz, A., and Tyers, M. (2006). BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535–9.10.1093/nar/gkj109Search in Google Scholar PubMed PubMed Central

Suchanek, M., Radzikowska, A., and Thiele, C. (2005). Photo-leucine and photo-methionine allow identification of protein-protein interactions in living cells. Nat. Methods 2, 261–267.10.1038/nmeth752Search in Google Scholar

Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N.T., Morris, J.H., Bork, P., et al. (2019). STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613.10.1093/nar/gky1131Search in Google Scholar

Takahashi, N., Yanagida, M., Fujiyama, S., Hayano, T., and Isobe, T. (2003). Proteomic snapshot analyses of preribosomal ribonucleoprotein complexes formed at various stages of ribosome biogenesis in yeast and mammalian cells. Mass. Spectrom. Rev. 22, 287–317.10.1002/mas.10057Search in Google Scholar

Thiele, A., Krentzlin, K., Erdmann, F., Rauh, D., Hause, G., Zerweck, J., Kilka, S., Pösel, S., Fischer, G., Schutkowski, M., et al. (2011). Parvulin 17 promotes microtubule assembly by its peptidyl-prolyl cis/trans isomerase activity. J. Mol. Biol. 411, 896–909.10.1016/j.jmb.2011.06.040Search in Google Scholar

Tyanova, S., Temu, T., Sinitcyn, P., Carlson, A., Hein, M.Y., Geiger, T., Mann, M., and Cox, J. (2016). The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740.10.1038/nmeth.3901Search in Google Scholar

Uchida, T., Fujimori, F., Tradler, T., Fischer, G., and Rahfeld, J.U. (1999). Identification and characterization of a 14 kDa human protein as a novel parvulin-like peptidyl prolyl cis/trans isomerase. FEBS Lett. 446, 278–282.10.1016/S0014-5793(99)00239-2Search in Google Scholar

Vicente-Manzanares, M., Webb, D.J., and Horwitz, A.R. (2005). Cell migration at a glance. J. Cell Sci. 118, 4917–4919.10.1242/jcs.02662Search in Google Scholar PubMed

Vizcaíno, J.A., Csordas, A., del-Toro, N., Dianes, J.A., Griss, J., Lavidas, I., Mayer, G., Perez-Riverol, Y., Reisinger, F., Ternent, T., et al. (2016). 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 44, D447–D456.10.1093/nar/gkv1145Search in Google Scholar PubMed PubMed Central

Zhang, J., Nakatsu, Y., Shinjo, T., Guo, Y., Sakoda, H., Yamamotoya, T., Otani, Y., Okubo, H., Kushiyama, A., Fujishiro, M., et al. (2013). Par14 protein associates with insulin receptor substrate 1 (IRS-1), thereby enhancing insulin-induced IRS-1 phosphorylation and metabolic actions. J. Biol. Chem. 288, 20692–20701.10.1074/jbc.M113.485730Search in Google Scholar PubMed PubMed Central