[{"ddc":["580"],"tmp":{"image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"isi":1,"article_number":"16527","title":"Phytaspase Is capable of detaching the endoplasmic reticulum retrieval signal from tobacco calreticulin-3","external_id":{"pmid":["38003717"],"isi":["001113792600001"]},"year":"2023","doi":"10.3390/ijms242216527","publication_identifier":{"issn":["1422-0067"]},"_id":"14776","pmid":1,"oa_version":"Published Version","quality_controlled":"1","acknowledgement":"We thank C.U.T. Hellen for critically reading the manuscript. The MALDI MS facility and CLSM became available to us in the framework of Moscow State University Development Programs PNG 5.13 and PNR 5.13.\r\nThis work was funded by the Russian Science Foundation, grant numbers 19-14-00010 and 22-14-00071.","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","article_processing_charge":"Yes","volume":24,"oa":1,"date_updated":"2024-01-10T13:41:10Z","abstract":[{"text":"Soluble chaperones residing in the endoplasmic reticulum (ER) play vitally important roles in folding and quality control of newly synthesized proteins that transiently pass through the ER en route to their final destinations. These soluble residents of the ER are themselves endowed with an ER retrieval signal that enables the cell to bring the escaped residents back from the Golgi. Here, by using purified proteins, we showed that Nicotiana tabacum phytaspase, a plant aspartate-specific protease, introduces two breaks at the C-terminus of the N. tabacum ER resident calreticulin-3. These cleavages resulted in removal of either a dipeptide or a hexapeptide from the C-terminus of calreticulin-3 encompassing part or all of the ER retrieval signal. Consistently, expression of the calreticulin-3 derivative mimicking the phytaspase cleavage product in Nicotiana benthamiana cells demonstrated loss of the ER accumulation of the protein. Notably, upon its escape from the ER, calreticulin-3 was further processed by an unknown protease(s) to generate the free N-terminal (N) domain of calreticulin-3, which was ultimately secreted into the apoplast. Our study thus identified a specific proteolytic enzyme capable of precise detachment of the ER retrieval signal from a plant ER resident protein, with implications for the further fate of the escaped resident.","lang":"eng"}],"keyword":["Inorganic Chemistry","Organic Chemistry","Physical and Theoretical Chemistry","Computer Science Applications","Spectroscopy","Molecular Biology","General Medicine","Catalysis"],"author":[{"id":"e3736151-106c-11ec-b916-c2558e2762c6","full_name":"Teplova, Anastasiia","last_name":"Teplova","first_name":"Anastasiia"},{"last_name":"Pigidanov","full_name":"Pigidanov, Artemii A.","first_name":"Artemii A."},{"first_name":"Marina V.","last_name":"Serebryakova","full_name":"Serebryakova, Marina V."},{"first_name":"Sergei A.","full_name":"Golyshev, Sergei A.","last_name":"Golyshev"},{"full_name":"Galiullina, Raisa A.","last_name":"Galiullina","first_name":"Raisa A."},{"first_name":"Nina V.","full_name":"Chichkova, Nina V.","last_name":"Chichkova"},{"full_name":"Vartapetian, Andrey B.","last_name":"Vartapetian","first_name":"Andrey B."}],"citation":{"short":"A. Teplova, A.A. Pigidanov, M.V. Serebryakova, S.A. Golyshev, R.A. Galiullina, N.V. Chichkova, A.B. Vartapetian, International Journal of Molecular Sciences 24 (2023).","ista":"Teplova A, Pigidanov AA, Serebryakova MV, Golyshev SA, Galiullina RA, Chichkova NV, Vartapetian AB. 2023. Phytaspase Is capable of detaching the endoplasmic reticulum retrieval signal from tobacco calreticulin-3. International Journal of Molecular Sciences. 24(22), 16527.","mla":"Teplova, Anastasiia, et al. “Phytaspase Is Capable of Detaching the Endoplasmic Reticulum Retrieval Signal from Tobacco Calreticulin-3.” <i>International Journal of Molecular Sciences</i>, vol. 24, no. 22, 16527, MDPI, 2023, doi:<a href=\"https://doi.org/10.3390/ijms242216527\">10.3390/ijms242216527</a>.","ama":"Teplova A, Pigidanov AA, Serebryakova MV, et al. Phytaspase Is capable of detaching the endoplasmic reticulum retrieval signal from tobacco calreticulin-3. <i>International Journal of Molecular Sciences</i>. 2023;24(22). doi:<a href=\"https://doi.org/10.3390/ijms242216527\">10.3390/ijms242216527</a>","chicago":"Teplova, Anastasiia, Artemii A. Pigidanov, Marina V. Serebryakova, Sergei A. Golyshev, Raisa A. Galiullina, Nina V. Chichkova, and Andrey B. Vartapetian. “Phytaspase Is Capable of Detaching the Endoplasmic Reticulum Retrieval Signal from Tobacco Calreticulin-3.” <i>International Journal of Molecular Sciences</i>. MDPI, 2023. <a href=\"https://doi.org/10.3390/ijms242216527\">https://doi.org/10.3390/ijms242216527</a>.","ieee":"A. Teplova <i>et al.</i>, “Phytaspase Is capable of detaching the endoplasmic reticulum retrieval signal from tobacco calreticulin-3,” <i>International Journal of Molecular Sciences</i>, vol. 24, no. 22. MDPI, 2023.","apa":"Teplova, A., Pigidanov, A. A., Serebryakova, M. V., Golyshev, S. A., Galiullina, R. A., Chichkova, N. V., &#38; Vartapetian, A. B. (2023). Phytaspase Is capable of detaching the endoplasmic reticulum retrieval signal from tobacco calreticulin-3. <i>International Journal of Molecular Sciences</i>. MDPI. <a href=\"https://doi.org/10.3390/ijms242216527\">https://doi.org/10.3390/ijms242216527</a>"},"publication_status":"published","date_created":"2024-01-10T09:24:35Z","file":[{"creator":"dernst","file_id":"14791","content_type":"application/pdf","relation":"main_file","success":1,"date_updated":"2024-01-10T13:39:42Z","access_level":"open_access","date_created":"2024-01-10T13:39:42Z","checksum":"4df7d206ba022b7f54eff1f0aec1659a","file_name":"2023_IJMS_Teplova.pdf","file_size":2637784}],"has_accepted_license":"1","department":[{"_id":"JiFr"}],"publisher":"MDPI","language":[{"iso":"eng"}],"month":"11","date_published":"2023-11-01T00:00:00Z","article_type":"original","publication":"International Journal of Molecular Sciences","issue":"22","file_date_updated":"2024-01-10T13:39:42Z","intvolume":"        24","status":"public","day":"01","type":"journal_article"},{"citation":{"mla":"Friml, Jiří, et al. “ABP1–TMK Auxin Perception for Global Phosphorylation and Auxin Canalization.” <i>Nature</i>, vol. 609, no. 7927, Springer Nature, 2022, pp. 575–81, doi:<a href=\"https://doi.org/10.1038/s41586-022-05187-x\">10.1038/s41586-022-05187-x</a>.","ama":"Friml J, Gallei MC, Gelová Z, et al. ABP1–TMK auxin perception for global phosphorylation and auxin canalization. <i>Nature</i>. 2022;609(7927):575-581. doi:<a href=\"https://doi.org/10.1038/s41586-022-05187-x\">10.1038/s41586-022-05187-x</a>","ista":"Friml J, Gallei MC, Gelová Z, Johnson AJ, Mazur E, Monzer A, Rodriguez Solovey L, Roosjen M, Verstraeten I, Živanović BD, Zou M, Fiedler L, Giannini C, Grones P, Hrtyan M, Kaufmann W, Kuhn A, Narasimhan M, Randuch M, Rýdza N, Takahashi K, Tan S, Teplova A, Kinoshita T, Weijers D, Rakusová H. 2022. ABP1–TMK auxin perception for global phosphorylation and auxin canalization. Nature. 609(7927), 575–581.","short":"J. Friml, M.C. Gallei, Z. Gelová, A.J. Johnson, E. Mazur, A. Monzer, L. Rodriguez Solovey, M. Roosjen, I. Verstraeten, B.D. Živanović, M. Zou, L. Fiedler, C. Giannini, P. Grones, M. Hrtyan, W. Kaufmann, A. Kuhn, M. Narasimhan, M. Randuch, N. Rýdza, K. Takahashi, S. Tan, A. Teplova, T. Kinoshita, D. Weijers, H. Rakusová, Nature 609 (2022) 575–581.","ieee":"J. Friml <i>et al.</i>, “ABP1–TMK auxin perception for global phosphorylation and auxin canalization,” <i>Nature</i>, vol. 609, no. 7927. Springer Nature, pp. 575–581, 2022.","apa":"Friml, J., Gallei, M. C., Gelová, Z., Johnson, A. J., Mazur, E., Monzer, A., … Rakusová, H. (2022). ABP1–TMK auxin perception for global phosphorylation and auxin canalization. <i>Nature</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41586-022-05187-x\">https://doi.org/10.1038/s41586-022-05187-x</a>","chicago":"Friml, Jiří, Michelle C Gallei, Zuzana Gelová, Alexander J Johnson, Ewa Mazur, Aline Monzer, Lesia Rodriguez Solovey, et al. “ABP1–TMK Auxin Perception for Global Phosphorylation and Auxin Canalization.” <i>Nature</i>. Springer Nature, 2022. <a href=\"https://doi.org/10.1038/s41586-022-05187-x\">https://doi.org/10.1038/s41586-022-05187-x</a>."},"publication_status":"published","abstract":[{"lang":"eng","text":"The phytohormone auxin triggers transcriptional reprogramming through a well-characterized perception machinery in the nucleus. By contrast, mechanisms that underlie fast effects of auxin, such as the regulation of ion fluxes, rapid phosphorylation of proteins or auxin feedback on its transport, remain unclear1,2,3. Whether auxin-binding protein 1 (ABP1) is an auxin receptor has been a source of debate for decades1,4. Here we show that a fraction of Arabidopsis thaliana ABP1 is secreted and binds auxin specifically at an acidic pH that is typical of the apoplast. ABP1 and its plasma-membrane-localized partner, transmembrane kinase 1 (TMK1), are required for the auxin-induced ultrafast global phospho-response and for downstream processes that include the activation of H+-ATPase and accelerated cytoplasmic streaming. abp1 and tmk mutants cannot establish auxin-transporting channels and show defective auxin-induced vasculature formation and regeneration. An ABP1(M2X) variant that lacks the capacity to bind auxin is unable to complement these defects in abp1 mutants. These data indicate that ABP1 is the auxin receptor for TMK1-based cell-surface signalling, which mediates the global phospho-response and auxin canalization."}],"author":[{"id":"4159519E-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-8302-7596","last_name":"Friml","full_name":"Friml, Jiří","first_name":"Jiří"},{"id":"35A03822-F248-11E8-B48F-1D18A9856A87","first_name":"Michelle C","last_name":"Gallei","full_name":"Gallei, Michelle C","orcid":"0000-0003-1286-7368"},{"first_name":"Zuzana","last_name":"Gelová","full_name":"Gelová, Zuzana","orcid":"0000-0003-4783-1752","id":"0AE74790-0E0B-11E9-ABC7-1ACFE5697425"},{"id":"46A62C3A-F248-11E8-B48F-1D18A9856A87","first_name":"Alexander J","last_name":"Johnson","full_name":"Johnson, Alexander J","orcid":"0000-0002-2739-8843"},{"first_name":"Ewa","last_name":"Mazur","full_name":"Mazur, Ewa"},{"id":"2DB5D88C-D7B3-11E9-B8FD-7907E6697425","full_name":"Monzer, Aline","last_name":"Monzer","first_name":"Aline"},{"orcid":"0000-0002-7244-7237","last_name":"Rodriguez Solovey","full_name":"Rodriguez Solovey, Lesia","first_name":"Lesia","id":"3922B506-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Roosjen, Mark","last_name":"Roosjen","first_name":"Mark"},{"id":"362BF7FE-F248-11E8-B48F-1D18A9856A87","last_name":"Verstraeten","full_name":"Verstraeten, Inge","orcid":"0000-0001-7241-2328","first_name":"Inge"},{"first_name":"Branka D.","full_name":"Živanović, Branka D.","last_name":"Živanović"},{"first_name":"Minxia","last_name":"Zou","full_name":"Zou, Minxia","id":"5c243f41-03f3-11ec-841c-96faf48a7ef9"},{"last_name":"Fiedler","full_name":"Fiedler, Lukas","first_name":"Lukas","id":"7c417475-8972-11ed-ae7b-8b674ca26986"},{"id":"e3fdddd5-f6e0-11ea-865d-ca99ee6367f4","last_name":"Giannini","full_name":"Giannini, Caterina","first_name":"Caterina"},{"first_name":"Peter","full_name":"Grones, Peter","last_name":"Grones"},{"first_name":"Mónika","last_name":"Hrtyan","full_name":"Hrtyan, Mónika","id":"45A71A74-F248-11E8-B48F-1D18A9856A87"},{"id":"3F99E422-F248-11E8-B48F-1D18A9856A87","first_name":"Walter","orcid":"0000-0001-9735-5315","last_name":"Kaufmann","full_name":"Kaufmann, Walter"},{"first_name":"Andre","last_name":"Kuhn","full_name":"Kuhn, Andre"},{"first_name":"Madhumitha","full_name":"Narasimhan, Madhumitha","last_name":"Narasimhan","orcid":"0000-0002-8600-0671","id":"44BF24D0-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Randuch","full_name":"Randuch, Marek","first_name":"Marek","id":"6ac4636d-15b2-11ec-abd3-fb8df79972ae"},{"full_name":"Rýdza, Nikola","last_name":"Rýdza","first_name":"Nikola"},{"last_name":"Takahashi","full_name":"Takahashi, Koji","first_name":"Koji"},{"orcid":"0000-0002-0471-8285","last_name":"Tan","full_name":"Tan, Shutang","first_name":"Shutang","id":"2DE75584-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Teplova, Anastasiia","last_name":"Teplova","first_name":"Anastasiia","id":"e3736151-106c-11ec-b916-c2558e2762c6"},{"full_name":"Kinoshita, Toshinori","last_name":"Kinoshita","first_name":"Toshinori"},{"first_name":"Dolf","last_name":"Weijers","full_name":"Weijers, Dolf"},{"first_name":"Hana","full_name":"Rakusová, Hana","last_name":"Rakusová"}],"article_processing_charge":"No","volume":609,"date_updated":"2023-11-07T08:16:09Z","oa":1,"publication_identifier":{"issn":["0028-0836"],"eissn":["1476-4687"]},"_id":"12291","pmid":1,"quality_controlled":"1","project":[{"grant_number":"742985","_id":"261099A6-B435-11E9-9278-68D0E5697425","name":"Tracing Evolution of Auxin Transport and Polarity in Plants","call_identifier":"H2020"},{"grant_number":"P29988","call_identifier":"FWF","_id":"262EF96E-B435-11E9-9278-68D0E5697425","name":"RNA-directed DNA methylation in plant development"}],"oa_version":"Submitted Version","acknowledgement":"We acknowledge K. Kubiasová for excellent technical assistance, J. Neuhold, A. Lehner and A. Sedivy for technical assistance with protein production and purification at Vienna Biocenter Core Facilities; Creoptix for performing GCI; and the Bioimaging, Electron Microscopy and Life Science Facilities at ISTA, the Plant Sciences Core Facility of CEITEC Masaryk University, the Core Facility CELLIM (MEYS CR, LM2018129 Czech-BioImaging) and J. Sprakel for their assistance. J.F. is grateful to R. Napier for many insightful suggestions and support. We thank all past and present members of the Friml group for their support and for other contributions to this effort to clarify the controversial role of ABP1 over the past seven years. The project received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 742985 to J.F. and 833867 to D.W.); the Austrian Science Fund (FWF; P29988 to J.F.); the Netherlands Organization for Scientific Research (NWO; VICI grant 865.14.001 to D.W. and VENI grant VI.Veni.212.003 to A.K.); the Ministry of Education, Science and Technological Development of the Republic of Serbia (contract no. 451-03-68/2022-14/200053 to B.D.Ž.); and the MEXT/JSPS KAKENHI to K.T. (20K06685) and T.K. (20H05687 and 20H05910).","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","year":"2022","doi":"10.1038/s41586-022-05187-x","acknowledged_ssus":[{"_id":"Bio"},{"_id":"EM-Fac"},{"_id":"LifeSc"}],"ec_funded":1,"external_id":{"isi":["000851357500002"],"pmid":["36071161"]},"title":"ABP1–TMK auxin perception for global phosphorylation and auxin canalization","isi":1,"ddc":["580"],"day":"15","type":"journal_article","intvolume":"       609","status":"public","publication":"Nature","issue":"7927","file_date_updated":"2023-11-02T17:12:37Z","page":"575-581","month":"09","article_type":"original","date_published":"2022-09-15T00:00:00Z","scopus_import":"1","publisher":"Springer Nature","language":[{"iso":"eng"}],"has_accepted_license":"1","department":[{"_id":"JiFr"},{"_id":"GradSch"},{"_id":"EvBe"},{"_id":"EM-Fac"}],"file":[{"content_type":"application/pdf","relation":"main_file","file_id":"14483","creator":"amally","success":1,"date_updated":"2023-11-02T17:12:37Z","access_level":"open_access","file_name":"Friml Nature 2022_merged.pdf","file_size":79774945,"date_created":"2023-11-02T17:12:37Z","checksum":"a6055c606aefb900bf62ae3e7d15f921"}],"date_created":"2023-01-16T10:04:48Z"}]