[{"_id":"10713","type":"journal_article","article_type":"original","tmp":{"short":"CC BY-NC-ND (4.0)","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","image":"/images/cc_by_nc_nd.png"},"status":"public","date_updated":"2023-08-02T14:06:15Z","department":[{"_id":"DaSi"}],"abstract":[{"lang":"eng","text":"Cells migrate through crowded microenvironments within tissues during normal development, immune response, and cancer metastasis. Although migration through pores and tracks in the extracellular matrix (ECM) has been well studied, little is known about cellular traversal into confining cell-dense tissues. We find that embryonic tissue invasion by Drosophila macrophages requires division of an epithelial ectodermal cell at the site of entry. Dividing ectodermal cells disassemble ECM attachment formed by integrin-mediated focal adhesions next to mesodermal cells, allowing macrophages to move their nuclei ahead and invade between two immediately adjacent tissues. Invasion efficiency depends on division frequency, but reduction of adhesion strength allows macrophage entry independently of division. This work demonstrates that tissue dynamics can regulate cellular infiltration."}],"acknowledged_ssus":[{"_id":"Bio"}],"pmid":1,"oa_version":"Preprint","main_file_link":[{"open_access":"1","url":"https://doi.org/10.1101/2021.04.19.438995"}],"month":"04","intvolume":" 376","publication_identifier":{"issn":["0036-8075"]},"publication_status":"published","language":[{"iso":"eng"}],"issue":"6591","volume":376,"project":[{"name":"Modeling epithelial tissue mechanics during cell invasion","grant_number":"M02379","call_identifier":"FWF","_id":"264CBBAC-B435-11E9-9278-68D0E5697425"}],"citation":{"chicago":"Akhmanova, Maria, Shamsi Emtenani, Daniel Krueger, Attila György, Mariana Pereira Guarda, Mikhail Vlasov, Fedor Vlasov, et al. “Cell Division in Tissues Enables Macrophage Infiltration.” Science. American Association for the Advancement of Science, 2022. https://doi.org/10.1126/science.abj0425.","ista":"Akhmanova M, Emtenani S, Krueger D, György A, Pereira Guarda M, Vlasov M, Vlasov F, Akopian A, Ratheesh A, De Renzis S, Siekhaus DE. 2022. Cell division in tissues enables macrophage infiltration. Science. 376(6591), 394–396.","mla":"Akhmanova, Maria, et al. “Cell Division in Tissues Enables Macrophage Infiltration.” Science, vol. 376, no. 6591, American Association for the Advancement of Science, 2022, pp. 394–96, doi:10.1126/science.abj0425.","short":"M. Akhmanova, S. Emtenani, D. Krueger, A. György, M. Pereira Guarda, M. Vlasov, F. Vlasov, A. Akopian, A. Ratheesh, S. De Renzis, D.E. Siekhaus, Science 376 (2022) 394–396.","ieee":"M. Akhmanova et al., “Cell division in tissues enables macrophage infiltration,” Science, vol. 376, no. 6591. American Association for the Advancement of Science, pp. 394–396, 2022.","ama":"Akhmanova M, Emtenani S, Krueger D, et al. Cell division in tissues enables macrophage infiltration. Science. 2022;376(6591):394-396. doi:10.1126/science.abj0425","apa":"Akhmanova, M., Emtenani, S., Krueger, D., György, A., Pereira Guarda, M., Vlasov, M., … Siekhaus, D. E. (2022). Cell division in tissues enables macrophage infiltration. Science. American Association for the Advancement of Science. https://doi.org/10.1126/science.abj0425"},"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","author":[{"full_name":"Akhmanova, Maria","orcid":"0000-0003-1522-3162","last_name":"Akhmanova","first_name":"Maria","id":"3425EC26-F248-11E8-B48F-1D18A9856A87"},{"orcid":"0000-0001-6981-6938","full_name":"Emtenani, Shamsi","last_name":"Emtenani","id":"49D32318-F248-11E8-B48F-1D18A9856A87","first_name":"Shamsi"},{"full_name":"Krueger, Daniel","last_name":"Krueger","first_name":"Daniel"},{"first_name":"Attila","id":"3BCEDBE0-F248-11E8-B48F-1D18A9856A87","full_name":"György, Attila","orcid":"0000-0002-1819-198X","last_name":"György"},{"last_name":"Pereira Guarda","full_name":"Pereira Guarda, Mariana","id":"6de81d9d-e2f2-11eb-945a-af8bc2a60b26","first_name":"Mariana"},{"last_name":"Vlasov","full_name":"Vlasov, Mikhail","first_name":"Mikhail"},{"last_name":"Vlasov","full_name":"Vlasov, Fedor","first_name":"Fedor"},{"first_name":"Andrei","last_name":"Akopian","full_name":"Akopian, Andrei"},{"first_name":"Aparna","id":"2F064CFE-F248-11E8-B48F-1D18A9856A87","last_name":"Ratheesh","full_name":"Ratheesh, Aparna"},{"first_name":"Stefano","last_name":"De Renzis","full_name":"De Renzis, Stefano"},{"last_name":"Siekhaus","orcid":"0000-0001-8323-8353","full_name":"Siekhaus, Daria E","id":"3D224B9E-F248-11E8-B48F-1D18A9856A87","first_name":"Daria E"}],"external_id":{"pmid":["35446632"],"isi":["000788553700039"]},"article_processing_charge":"No","title":"Cell division in tissues enables macrophage infiltration","acknowledgement":"We thank J. Friml, C. Guet, T. Hurd, M. Fendrych and members of the laboratory for comments on the manuscript; the Bioimaging Facility of IST Austria for excellent support and T. Lecuit, E. Hafen, R. Levayer and A. Martin for fly strains. This work was supported by a grant from the Austrian Science Fund FWF: Lise Meitner Fellowship M2379-B28 to M.A and D.S., and internal funding from IST Austria to D.S. and EMBL to S.D.R.","quality_controlled":"1","publisher":"American Association for the Advancement of Science","oa":1,"isi":1,"year":"2022","day":"22","publication":"Science","page":"394-396","date_published":"2022-04-22T00:00:00Z","doi":"10.1126/science.abj0425","date_created":"2022-02-01T11:23:18Z"},{"publisher":"Embo Press","quality_controlled":"1","oa":1,"acknowledgement":"We thank the DGRC (NIH grant 2P40OD010949-10A1) for plasmids, the BDSC (NIH grant P40OD018537) and the VDRC for fly stocks, FlyBase for essential genomic information, the BDGP in situ database for data (Tomancak et al, 2007), the IST Austria Bioimaging facility for support, the VBC Core Facilities for RNA sequencing and analysis, and C. Guet, C. Navarro, C. Desplan, T. Lecuit, I. Miguel-Aliaga, and Siekhaus group members for comments on the manuscript. The VBCF Metabolomics Facility is funded by the City of Vienna through the Vienna Business Agency. This work was supported by the Marie Curie CIG 334077/IRTIM (DES), Austrian Science Fund (FWF) Lise Meitner Fellowship M2379-B28 (MA and DES), Austrian Science Fund (FWF) grant ASI_FWF01_P29638S (DES), NIH/NIGMS (R01GM111779-06 (PR), RO1GM135628-01 (PR), European Research Council (ERC) grant no. 677006 “CMIL” (AB), and Natural Sciences and Engineering Research Council of Canada\r\n(RGPIN-2019-06766) (TRH). ","date_published":"2022-03-23T00:00:00Z","doi":"10.15252/embj.2021109049","date_created":"2022-03-24T13:23:09Z","day":"23","publication":"The Embo Journal","isi":1,"has_accepted_license":"1","year":"2022","project":[{"call_identifier":"FP7","_id":"2536F660-B435-11E9-9278-68D0E5697425","name":"Investigating the role of transporters in invasive migration through junctions","grant_number":"334077"},{"name":"Modeling epithelial tissue mechanics during cell invasion","grant_number":"M02379","call_identifier":"FWF","_id":"264CBBAC-B435-11E9-9278-68D0E5697425"},{"name":"Drosophila TNFa´s Funktion in Immunzellen","grant_number":"P29638","call_identifier":"FWF","_id":"253B6E48-B435-11E9-9278-68D0E5697425"}],"article_number":"e109049","title":"Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos axis in Drosophila","author":[{"last_name":"Emtenani","orcid":"0000-0001-6981-6938","full_name":"Emtenani, Shamsi","first_name":"Shamsi","id":"49D32318-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Elliot T","last_name":"Martin","full_name":"Martin, Elliot T"},{"id":"3BCEDBE0-F248-11E8-B48F-1D18A9856A87","first_name":"Attila","last_name":"György","full_name":"György, Attila","orcid":"0000-0002-1819-198X"},{"last_name":"Bicher","full_name":"Bicher, Julia","first_name":"Julia","id":"3CCBB46E-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Genger","full_name":"Genger, Jakob-Wendelin","first_name":"Jakob-Wendelin"},{"full_name":"Köcher, Thomas","last_name":"Köcher","first_name":"Thomas"},{"id":"3425EC26-F248-11E8-B48F-1D18A9856A87","first_name":"Maria","orcid":"0000-0003-1522-3162","full_name":"Akhmanova, Maria","last_name":"Akhmanova"},{"id":"6de81d9d-e2f2-11eb-945a-af8bc2a60b26","first_name":"Mariana","full_name":"Pereira Guarda, Mariana","last_name":"Pereira Guarda"},{"first_name":"Marko","id":"3047D808-F248-11E8-B48F-1D18A9856A87","full_name":"Roblek, Marko","orcid":"0000-0001-9588-1389","last_name":"Roblek"},{"first_name":"Andreas","full_name":"Bergthaler, Andreas","last_name":"Bergthaler"},{"first_name":"Thomas R","last_name":"Hurd","full_name":"Hurd, Thomas R"},{"first_name":"Prashanth","last_name":"Rangan","full_name":"Rangan, Prashanth"},{"id":"3D224B9E-F248-11E8-B48F-1D18A9856A87","first_name":"Daria E","full_name":"Siekhaus, Daria E","orcid":"0000-0001-8323-8353","last_name":"Siekhaus"}],"article_processing_charge":"Yes (via OA deal)","external_id":{"isi":["000771957000001"]},"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","citation":{"ista":"Emtenani S, Martin ET, György A, Bicher J, Genger J-W, Köcher T, Akhmanova M, Pereira Guarda M, Roblek M, Bergthaler A, Hurd TR, Rangan P, Siekhaus DE. 2022. Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos axis in Drosophila. The Embo Journal. 41, e109049.","chicago":"Emtenani, Shamsi, Elliot T Martin, Attila György, Julia Bicher, Jakob-Wendelin Genger, Thomas Köcher, Maria Akhmanova, et al. “Macrophage Mitochondrial Bioenergetics and Tissue Invasion Are Boosted by an Atossa-Porthos Axis in Drosophila.” The Embo Journal. Embo Press, 2022. https://doi.org/10.15252/embj.2021109049.","short":"S. Emtenani, E.T. Martin, A. György, J. Bicher, J.-W. Genger, T. Köcher, M. Akhmanova, M. Pereira Guarda, M. Roblek, A. Bergthaler, T.R. Hurd, P. Rangan, D.E. Siekhaus, The Embo Journal 41 (2022).","ieee":"S. Emtenani et al., “Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos axis in Drosophila,” The Embo Journal, vol. 41. Embo Press, 2022.","ama":"Emtenani S, Martin ET, György A, et al. Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos axis in Drosophila. The Embo Journal. 2022;41. doi:10.15252/embj.2021109049","apa":"Emtenani, S., Martin, E. T., György, A., Bicher, J., Genger, J.-W., Köcher, T., … Siekhaus, D. E. (2022). Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos axis in Drosophila. The Embo Journal. Embo Press. https://doi.org/10.15252/embj.2021109049","mla":"Emtenani, Shamsi, et al. “Macrophage Mitochondrial Bioenergetics and Tissue Invasion Are Boosted by an Atossa-Porthos Axis in Drosophila.” The Embo Journal, vol. 41, e109049, Embo Press, 2022, doi:10.15252/embj.2021109049."},"month":"03","intvolume":" 41","scopus_import":"1","oa_version":"Published Version","acknowledged_ssus":[{"_id":"Bio"}],"abstract":[{"text":"Cellular metabolism must adapt to changing demands to enable homeostasis. During immune responses or cancer metastasis, cells leading migration into challenging environments require an energy boost, but what controls this capacity is unclear. Here, we study a previously uncharacterized nuclear protein, Atossa (encoded by CG9005), which supports macrophage invasion into the germband of Drosophila by controlling cellular metabolism. First, nuclear Atossa increases mRNA levels of Porthos, a DEAD-box protein, and of two metabolic enzymes, lysine-α-ketoglutarate reductase (LKR/SDH) and NADPH glyoxylate reductase (GR/HPR), thus enhancing mitochondrial bioenergetics. Then Porthos supports ribosome assembly and thereby raises the translational efficiency of a subset of mRNAs, including those affecting mitochondrial functions, the electron transport chain, and metabolism. Mitochondrial respiration measurements, metabolomics, and live imaging indicate that Atossa and Porthos power up OxPhos and energy production to promote the forging of a path into tissues by leading macrophages. Since many crucial physiological responses require increases in mitochondrial energy output, this previously undescribed genetic program may modulate a wide range of cellular behaviors.","lang":"eng"}],"volume":41,"ec_funded":1,"file":[{"file_id":"10919","checksum":"dba48580fe0fefaa4c63078d1d2a35df","content_type":"application/pdf","relation":"main_file","access_level":"open_access","file_name":"Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos axis in Drosopila.pdf","date_created":"2022-03-24T13:22:41Z","file_size":4344585,"date_updated":"2022-03-24T13:22:41Z","creator":"siekhaus"}],"language":[{"iso":"eng"}],"publication_identifier":{"eissn":["1460-2075"]},"publication_status":"published","status":"public","type":"journal_article","article_type":"original","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"_id":"10918","department":[{"_id":"DaSi"},{"_id":"LoSw"}],"file_date_updated":"2022-03-24T13:22:41Z","ddc":["570"],"date_updated":"2023-08-03T06:13:14Z"},{"day":"06","publication":"PLoS Biology","has_accepted_license":"1","isi":1,"year":"2022","doi":"10.1371/journal.pbio.3001494","date_published":"2022-01-06T00:00:00Z","date_created":"2022-01-12T10:18:17Z","page":"e3001494","acknowledgement":"We thank the following for their contributions: Plasmids were supplied by the Drosophila Genomics Resource Center (NIH 2P40OD010949-10A1); fly stocks were provided by K. Brueckner, B. Stramer, M. Uhlirova, O. Schuldiner, the Bloomington Drosophila Stock Center (NIH P40OD018537) and the Vienna Drosophila Resource Center, FlyBase for essential genomic information, and the BDGP in situ database for data. For antibodies, we thank the Developmental Studies Hybridoma Bank, which was created by the Eunice Kennedy Shriver National Institute of Child Health and Human Development of the NIH and is maintained at the University of Iowa, as well as J. Zeitlinger for her generous gift of Dfos antibody. We thank the Vienna BioCenter Core Facilities for RNA sequencing and analysis and the Life Scientific Service Units at IST Austria for technical support and assistance with microscopy and FACS analysis. We thank C. P. Heisenberg, P. Martin, M. Sixt, and Siekhaus group members for discussions and T. Hurd, A. Ratheesh, and P. Rangan for comments on the manuscript.","publisher":"Public Library of Science","quality_controlled":"1","oa":1,"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","citation":{"chicago":"Belyaeva, Vera, Stephanie Wachner, Attila György, Shamsi Emtenani, Igor Gridchyn, Maria Akhmanova, M Linder, Marko Roblek, M Sibilia, and Daria E Siekhaus. “Fos Regulates Macrophage Infiltration against Surrounding Tissue Resistance by a Cortical Actin-Based Mechanism in Drosophila.” PLoS Biology. Public Library of Science, 2022. https://doi.org/10.1371/journal.pbio.3001494.","ista":"Belyaeva V, Wachner S, György A, Emtenani S, Gridchyn I, Akhmanova M, Linder M, Roblek M, Sibilia M, Siekhaus DE. 2022. Fos regulates macrophage infiltration against surrounding tissue resistance by a cortical actin-based mechanism in Drosophila. PLoS Biology. 20(1), e3001494.","mla":"Belyaeva, Vera, et al. “Fos Regulates Macrophage Infiltration against Surrounding Tissue Resistance by a Cortical Actin-Based Mechanism in Drosophila.” PLoS Biology, vol. 20, no. 1, Public Library of Science, 2022, p. e3001494, doi:10.1371/journal.pbio.3001494.","ama":"Belyaeva V, Wachner S, György A, et al. Fos regulates macrophage infiltration against surrounding tissue resistance by a cortical actin-based mechanism in Drosophila. PLoS Biology. 2022;20(1):e3001494. doi:10.1371/journal.pbio.3001494","apa":"Belyaeva, V., Wachner, S., György, A., Emtenani, S., Gridchyn, I., Akhmanova, M., … Siekhaus, D. E. (2022). Fos regulates macrophage infiltration against surrounding tissue resistance by a cortical actin-based mechanism in Drosophila. PLoS Biology. Public Library of Science. https://doi.org/10.1371/journal.pbio.3001494","short":"V. Belyaeva, S. Wachner, A. György, S. Emtenani, I. Gridchyn, M. Akhmanova, M. Linder, M. Roblek, M. Sibilia, D.E. Siekhaus, PLoS Biology 20 (2022) e3001494.","ieee":"V. Belyaeva et al., “Fos regulates macrophage infiltration against surrounding tissue resistance by a cortical actin-based mechanism in Drosophila,” PLoS Biology, vol. 20, no. 1. Public Library of Science, p. e3001494, 2022."},"title":"Fos regulates macrophage infiltration against surrounding tissue resistance by a cortical actin-based mechanism in Drosophila","author":[{"first_name":"Vera","id":"47F080FE-F248-11E8-B48F-1D18A9856A87","full_name":"Belyaeva, Vera","last_name":"Belyaeva"},{"id":"2A95E7B0-F248-11E8-B48F-1D18A9856A87","first_name":"Stephanie","full_name":"Wachner, Stephanie","last_name":"Wachner"},{"orcid":"0000-0002-1819-198X","full_name":"György, Attila","last_name":"György","first_name":"Attila","id":"3BCEDBE0-F248-11E8-B48F-1D18A9856A87"},{"id":"49D32318-F248-11E8-B48F-1D18A9856A87","first_name":"Shamsi","full_name":"Emtenani, Shamsi","orcid":"0000-0001-6981-6938","last_name":"Emtenani"},{"first_name":"Igor","id":"4B60654C-F248-11E8-B48F-1D18A9856A87","last_name":"Gridchyn","full_name":"Gridchyn, Igor","orcid":"0000-0002-1807-1929"},{"last_name":"Akhmanova","full_name":"Akhmanova, Maria","orcid":"0000-0003-1522-3162","id":"3425EC26-F248-11E8-B48F-1D18A9856A87","first_name":"Maria"},{"first_name":"M","full_name":"Linder, M","last_name":"Linder"},{"id":"3047D808-F248-11E8-B48F-1D18A9856A87","first_name":"Marko","orcid":"0000-0001-9588-1389","full_name":"Roblek, Marko","last_name":"Roblek"},{"full_name":"Sibilia, M","last_name":"Sibilia","first_name":"M"},{"id":"3D224B9E-F248-11E8-B48F-1D18A9856A87","first_name":"Daria E","full_name":"Siekhaus, Daria E","orcid":"0000-0001-8323-8353","last_name":"Siekhaus"}],"external_id":{"pmid":["34990456"],"isi":["000971223700001"]},"article_processing_charge":"No","project":[{"grant_number":"P29638","name":"Drosophila TNFa´s Funktion in Immunzellen","call_identifier":"FWF","_id":"253B6E48-B435-11E9-9278-68D0E5697425"},{"name":"Tissue barrier penetration is crucial for immunity and metastasis","grant_number":"24800","_id":"26199CA4-B435-11E9-9278-68D0E5697425"},{"grant_number":"334077","name":"Investigating the role of transporters in invasive migration through junctions","call_identifier":"FP7","_id":"2536F660-B435-11E9-9278-68D0E5697425"}],"file":[{"relation":"main_file","access_level":"open_access","content_type":"application/pdf","success":1,"file_id":"10615","checksum":"f454212a5522a7818ba4b2892315c478","creator":"cchlebak","file_size":5426932,"date_updated":"2022-01-12T13:50:04Z","file_name":"2022_PLOSBio_Belyaeva.pdf","date_created":"2022-01-12T13:50:04Z"}],"language":[{"iso":"eng"}],"publication_identifier":{"eissn":["1545-7885"],"issn":["1544-9173"]},"publication_status":"published","volume":20,"issue":"1","related_material":{"record":[{"relation":"earlier_version","status":"public","id":"8557"},{"relation":"dissertation_contains","id":"11193","status":"public"}],"link":[{"relation":"earlier_version","url":"https://www.biorxiv.org/content/10.1101/2020.09.18.301481"},{"description":"News on the ISTA Website","url":"https://ista.ac.at/en/news/resisting-the-pressure/","relation":"press_release"}]},"ec_funded":1,"pmid":1,"oa_version":"Published Version","abstract":[{"text":"The infiltration of immune cells into tissues underlies the establishment of tissue-resident macrophages and responses to infections and tumors. Yet the mechanisms immune cells utilize to negotiate tissue barriers in living organisms are not well understood, and a role for cortical actin has not been examined. Here, we find that the tissue invasion of Drosophila macrophages, also known as plasmatocytes or hemocytes, utilizes enhanced cortical F-actin levels stimulated by the Drosophila member of the fos proto oncogene transcription factor family (Dfos, Kayak). RNA sequencing analysis and live imaging show that Dfos enhances F-actin levels around the entire macrophage surface by increasing mRNA levels of the membrane spanning molecular scaffold tetraspanin TM4SF, and the actin cross-linking filamin Cheerio, which are themselves required for invasion. Both the filamin and the tetraspanin enhance the cortical activity of Rho1 and the formin Diaphanous and thus the assembly of cortical actin, which is a critical function since expressing a dominant active form of Diaphanous can rescue the Dfos macrophage invasion defect. In vivo imaging shows that Dfos enhances the efficiency of the initial phases of macrophage tissue entry. Genetic evidence argues that this Dfos-induced program in macrophages counteracts the constraint produced by the tension of surrounding tissues and buffers the properties of the macrophage nucleus from affecting tissue entry. We thus identify strengthening the cortical actin cytoskeleton through Dfos as a key process allowing efficient forward movement of an immune cell into surrounding tissues. ","lang":"eng"}],"acknowledged_ssus":[{"_id":"LifeSc"}],"month":"01","intvolume":" 20","scopus_import":"1","ddc":["570"],"date_updated":"2024-03-27T23:30:28Z","file_date_updated":"2022-01-12T13:50:04Z","department":[{"_id":"DaSi"},{"_id":"JoCs"}],"_id":"10614","status":"public","article_type":"original","type":"journal_article","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"}},{"volume":10,"language":[{"iso":"eng"}],"file":[{"checksum":"77e8720a8e0f3091b98159f85be40893","file_id":"7184","content_type":"application/pdf","access_level":"open_access","relation":"main_file","date_created":"2019-12-16T07:37:50Z","file_name":"2019_NatureComm_Retzer.pdf","date_updated":"2020-07-14T12:47:52Z","file_size":5156533,"creator":"dernst"}],"publication_status":"published","publication_identifier":{"eissn":["20411723"]},"intvolume":" 10","month":"12","scopus_import":"1","oa_version":"Published Version","pmid":1,"abstract":[{"text":"Arabidopsis PIN2 protein directs transport of the phytohormone auxin from the root tip into the root elongation zone. Variation in hormone transport, which depends on a delicate interplay between PIN2 sorting to and from polar plasma membrane domains, determines root growth. By employing a constitutively degraded version of PIN2, we identify brassinolides as antagonists of PIN2 endocytosis. This response does not require de novo protein synthesis, but involves early events in canonical brassinolide signaling. Brassinolide-controlled adjustments in PIN2 sorting and intracellular distribution governs formation of a lateral PIN2 gradient in gravistimulated roots, coinciding with adjustments in auxin signaling and directional root growth. Strikingly, simulations indicate that PIN2 gradient formation is no prerequisite for root bending but rather dampens asymmetric auxin flow and signaling. Crosstalk between brassinolide signaling and endocytic PIN2 sorting, thus, appears essential for determining the rate of gravity-induced root curvature via attenuation of differential cell elongation.","lang":"eng"}],"department":[{"_id":"DaSi"}],"file_date_updated":"2020-07-14T12:47:52Z","ddc":["570"],"date_updated":"2023-09-06T14:08:21Z","status":"public","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"type":"journal_article","article_type":"original","_id":"7180","date_created":"2019-12-15T23:00:43Z","date_published":"2019-12-01T00:00:00Z","doi":"10.1038/s41467-019-13543-1","publication":"Nature Communications","day":"01","year":"2019","isi":1,"has_accepted_license":"1","oa":1,"quality_controlled":"1","publisher":"Springer Nature","title":"Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter","article_processing_charge":"No","external_id":{"pmid":["31797871"],"isi":["000500508100001"]},"author":[{"first_name":"Katarzyna","last_name":"Retzer","full_name":"Retzer, Katarzyna"},{"first_name":"Maria","id":"3425EC26-F248-11E8-B48F-1D18A9856A87","last_name":"Akhmanova","orcid":"0000-0003-1522-3162","full_name":"Akhmanova, Maria"},{"first_name":"Nataliia","last_name":"Konstantinova","full_name":"Konstantinova, Nataliia"},{"first_name":"Kateřina","last_name":"Malínská","full_name":"Malínská, Kateřina"},{"first_name":"Johannes","last_name":"Leitner","full_name":"Leitner, Johannes"},{"last_name":"Petrášek","full_name":"Petrášek, Jan","first_name":"Jan"},{"last_name":"Luschnig","full_name":"Luschnig, Christian","first_name":"Christian"}],"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","citation":{"mla":"Retzer, Katarzyna, et al. “Brassinosteroid Signaling Delimits Root Gravitropism via Sorting of the Arabidopsis PIN2 Auxin Transporter.” Nature Communications, vol. 10, 5516, Springer Nature, 2019, doi:10.1038/s41467-019-13543-1.","ieee":"K. Retzer et al., “Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter,” Nature Communications, vol. 10. Springer Nature, 2019.","short":"K. Retzer, M. Akhmanova, N. Konstantinova, K. Malínská, J. Leitner, J. Petrášek, C. Luschnig, Nature Communications 10 (2019).","apa":"Retzer, K., Akhmanova, M., Konstantinova, N., Malínská, K., Leitner, J., Petrášek, J., & Luschnig, C. (2019). Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nature Communications. Springer Nature. https://doi.org/10.1038/s41467-019-13543-1","ama":"Retzer K, Akhmanova M, Konstantinova N, et al. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nature Communications. 2019;10. doi:10.1038/s41467-019-13543-1","chicago":"Retzer, Katarzyna, Maria Akhmanova, Nataliia Konstantinova, Kateřina Malínská, Johannes Leitner, Jan Petrášek, and Christian Luschnig. “Brassinosteroid Signaling Delimits Root Gravitropism via Sorting of the Arabidopsis PIN2 Auxin Transporter.” Nature Communications. Springer Nature, 2019. https://doi.org/10.1038/s41467-019-13543-1.","ista":"Retzer K, Akhmanova M, Konstantinova N, Malínská K, Leitner J, Petrášek J, Luschnig C. 2019. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nature Communications. 10, 5516."},"project":[{"name":"Modeling epithelial tissue mechanics during cell invasion","grant_number":"M02379","_id":"264CBBAC-B435-11E9-9278-68D0E5697425","call_identifier":"FWF"}],"article_number":"5516"},{"department":[{"_id":"JiFr"},{"_id":"DaSi"},{"_id":"NanoFab"}],"date_updated":"2023-09-15T12:11:03Z","type":"journal_article","article_type":"original","status":"public","_id":"192","volume":4,"related_material":{"link":[{"url":"https://ist.ac.at/en/news/new-mechanism-for-the-plant-hormone-auxin-discovered/","relation":"press_release","description":"News on IST Homepage"}]},"issue":"7","publication_status":"published","language":[{"iso":"eng"}],"scopus_import":"1","main_file_link":[{"open_access":"1","url":"https://www.ncbi.nlm.nih.gov/pubmed/29942048"}],"month":"06","intvolume":" 4","abstract":[{"text":"The phytohormone auxin is the information carrier in a plethora of developmental and physiological processes in plants(1). It has been firmly established that canonical, nuclear auxin signalling acts through regulation of gene transcription(2). Here, we combined microfluidics, live imaging, genetic engineering and computational modelling to reanalyse the classical case of root growth inhibition(3) by auxin. We show that Arabidopsis roots react to addition and removal of auxin by extremely rapid adaptation of growth rate. This process requires intracellular auxin perception but not transcriptional reprogramming. The formation of the canonical TIR1/AFB-Aux/IAA co-receptor complex is required for the growth regulation, hinting to a novel, non-transcriptional branch of this signalling pathway. Our results challenge the current understanding of root growth regulation by auxin and suggest another, presumably non-transcriptional, signalling output of the canonical auxin pathway.","lang":"eng"}],"oa_version":"Submitted Version","pmid":1,"author":[{"id":"43905548-F248-11E8-B48F-1D18A9856A87","first_name":"Matyas","full_name":"Fendrych, Matyas","orcid":"0000-0002-9767-8699","last_name":"Fendrych"},{"orcid":"0000-0003-1522-3162","full_name":"Akhmanova, Maria","last_name":"Akhmanova","first_name":"Maria","id":"3425EC26-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Merrin","orcid":"0000-0001-5145-4609","full_name":"Merrin, Jack","first_name":"Jack","id":"4515C308-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Matous","last_name":"Glanc","full_name":"Glanc, Matous"},{"full_name":"Hagihara, Shinya","last_name":"Hagihara","first_name":"Shinya"},{"first_name":"Koji","full_name":"Takahashi, Koji","last_name":"Takahashi"},{"last_name":"Uchida","full_name":"Uchida, Naoyuki","first_name":"Naoyuki"},{"first_name":"Keiko U","last_name":"Torii","full_name":"Torii, Keiko U"},{"first_name":"Jirí","id":"4159519E-F248-11E8-B48F-1D18A9856A87","last_name":"Friml","full_name":"Friml, Jirí","orcid":"0000-0002-8302-7596"}],"publist_id":"7728","external_id":{"isi":["000443221200017"],"pmid":["29942048"]},"article_processing_charge":"No","title":"Rapid and reversible root growth inhibition by TIR1 auxin signalling","citation":{"ista":"Fendrych M, Akhmanova M, Merrin J, Glanc M, Hagihara S, Takahashi K, Uchida N, Torii KU, Friml J. 2018. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nature Plants. 4(7), 453–459.","chicago":"Fendrych, Matyas, Maria Akhmanova, Jack Merrin, Matous Glanc, Shinya Hagihara, Koji Takahashi, Naoyuki Uchida, Keiko U Torii, and Jiří Friml. “Rapid and Reversible Root Growth Inhibition by TIR1 Auxin Signalling.” Nature Plants. Springer Nature, 2018. https://doi.org/10.1038/s41477-018-0190-1.","short":"M. Fendrych, M. Akhmanova, J. Merrin, M. Glanc, S. Hagihara, K. Takahashi, N. Uchida, K.U. Torii, J. Friml, Nature Plants 4 (2018) 453–459.","ieee":"M. Fendrych et al., “Rapid and reversible root growth inhibition by TIR1 auxin signalling,” Nature Plants, vol. 4, no. 7. Springer Nature, pp. 453–459, 2018.","apa":"Fendrych, M., Akhmanova, M., Merrin, J., Glanc, M., Hagihara, S., Takahashi, K., … Friml, J. (2018). Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nature Plants. Springer Nature. https://doi.org/10.1038/s41477-018-0190-1","ama":"Fendrych M, Akhmanova M, Merrin J, et al. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nature Plants. 2018;4(7):453-459. doi:10.1038/s41477-018-0190-1","mla":"Fendrych, Matyas, et al. “Rapid and Reversible Root Growth Inhibition by TIR1 Auxin Signalling.” Nature Plants, vol. 4, no. 7, Springer Nature, 2018, pp. 453–59, doi:10.1038/s41477-018-0190-1."},"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","page":"453 - 459","date_published":"2018-06-25T00:00:00Z","doi":"10.1038/s41477-018-0190-1","date_created":"2018-12-11T11:45:07Z","isi":1,"year":"2018","day":"25","publication":"Nature Plants","publisher":"Springer Nature","quality_controlled":"1","oa":1},{"article_type":"original","type":"journal_article","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"status":"public","_id":"14","department":[{"_id":"DaSi"},{"_id":"JiFr"}],"file_date_updated":"2020-07-14T12:44:50Z","date_updated":"2023-09-18T08:09:32Z","ddc":["580"],"scopus_import":"1","month":"11","intvolume":" 19","abstract":[{"text":"The intercellular transport of auxin is driven by PIN-formed (PIN) auxin efflux carriers. PINs are localized at the plasma membrane (PM) and on constitutively recycling endomembrane vesicles. Therefore, PINs can mediate auxin transport either by direct translocation across the PM or by pumping auxin into secretory vesicles (SVs), leading to its secretory release upon fusion with the PM. Which of these two mechanisms dominates is a matter of debate. Here, we addressed the issue with a mathematical modeling approach. We demonstrate that the efficiency of secretory transport depends on SV size, half-life of PINs on the PM, pH, exocytosis frequency and PIN density. 3D structured illumination microscopy (SIM) was used to determine PIN density on the PM. Combining this data with published values of the other parameters, we show that the transport activity of PINs in SVs would have to be at least 1000× greater than on the PM in order to produce a comparable macroscopic auxin transport. If both transport mechanisms operated simultaneously and PINs were equally active on SVs and PM, the contribution of secretion to the total auxin flux would be negligible. In conclusion, while secretory vesicle-mediated transport of auxin is an intriguing and theoretically possible model, it is unlikely to be a major mechanism of auxin transport inplanta.","lang":"eng"}],"oa_version":"Published Version","issue":"11","volume":19,"ec_funded":1,"publication_identifier":{"eissn":["1422-0067"]},"publication_status":"published","file":[{"file_name":"2018_IJMS_Hille.pdf","date_created":"2018-12-17T16:04:11Z","file_size":2200593,"date_updated":"2020-07-14T12:44:50Z","creator":"dernst","file_id":"5719","checksum":"e4b59c2599b0ca26ebf5b8434bcde94a","content_type":"application/pdf","relation":"main_file","access_level":"open_access"}],"language":[{"iso":"eng"}],"project":[{"name":"Tracing Evolution of Auxin Transport and Polarity in Plants","grant_number":"742985","call_identifier":"H2020","_id":"261099A6-B435-11E9-9278-68D0E5697425"},{"grant_number":"I03630","name":"Molecular mechanisms of endocytic cargo recognition in plants","_id":"26538374-B435-11E9-9278-68D0E5697425","call_identifier":"FWF"}],"author":[{"first_name":"Sander","last_name":"Hille","full_name":"Hille, Sander"},{"orcid":"0000-0003-1522-3162","full_name":"Akhmanova, Maria","last_name":"Akhmanova","first_name":"Maria","id":"3425EC26-F248-11E8-B48F-1D18A9856A87"},{"orcid":"0000-0003-0619-7783","full_name":"Glanc, Matous","last_name":"Glanc","id":"1AE1EA24-02D0-11E9-9BAA-DAF4881429F2","first_name":"Matous"},{"first_name":"Alexander J","id":"46A62C3A-F248-11E8-B48F-1D18A9856A87","last_name":"Johnson","full_name":"Johnson, Alexander J","orcid":"0000-0002-2739-8843"},{"full_name":"Friml, Jirí","orcid":"0000-0002-8302-7596","last_name":"Friml","id":"4159519E-F248-11E8-B48F-1D18A9856A87","first_name":"Jirí"}],"publist_id":"8042","article_processing_charge":"No","external_id":{"isi":["000451528500282"]},"title":"Relative contribution of PIN-containing secretory vesicles and plasma membrane PINs to the directed auxin transport: Theoretical estimation","citation":{"chicago":"Hille, Sander, Maria Akhmanova, Matous Glanc, Alexander J Johnson, and Jiří Friml. “Relative Contribution of PIN-Containing Secretory Vesicles and Plasma Membrane PINs to the Directed Auxin Transport: Theoretical Estimation.” International Journal of Molecular Sciences. MDPI, 2018. https://doi.org/10.3390/ijms19113566.","ista":"Hille S, Akhmanova M, Glanc M, Johnson AJ, Friml J. 2018. Relative contribution of PIN-containing secretory vesicles and plasma membrane PINs to the directed auxin transport: Theoretical estimation. International Journal of Molecular Sciences. 19(11).","mla":"Hille, Sander, et al. “Relative Contribution of PIN-Containing Secretory Vesicles and Plasma Membrane PINs to the Directed Auxin Transport: Theoretical Estimation.” International Journal of Molecular Sciences, vol. 19, no. 11, MDPI, 2018, doi:10.3390/ijms19113566.","ieee":"S. Hille, M. Akhmanova, M. Glanc, A. J. Johnson, and J. Friml, “Relative contribution of PIN-containing secretory vesicles and plasma membrane PINs to the directed auxin transport: Theoretical estimation,” International Journal of Molecular Sciences, vol. 19, no. 11. MDPI, 2018.","short":"S. Hille, M. Akhmanova, M. Glanc, A.J. Johnson, J. Friml, International Journal of Molecular Sciences 19 (2018).","ama":"Hille S, Akhmanova M, Glanc M, Johnson AJ, Friml J. Relative contribution of PIN-containing secretory vesicles and plasma membrane PINs to the directed auxin transport: Theoretical estimation. International Journal of Molecular Sciences. 2018;19(11). doi:10.3390/ijms19113566","apa":"Hille, S., Akhmanova, M., Glanc, M., Johnson, A. J., & Friml, J. (2018). Relative contribution of PIN-containing secretory vesicles and plasma membrane PINs to the directed auxin transport: Theoretical estimation. International Journal of Molecular Sciences. MDPI. https://doi.org/10.3390/ijms19113566"},"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","publisher":"MDPI","quality_controlled":"1","oa":1,"acknowledgement":"European Research Council (ERC): 742985 to Jiri Friml; M.A. was supported by the Austrian Science Fund (FWF) (M2379-B28); AJ was supported by the Austria Science Fund (FWF): I03630 to Jiri Friml.","doi":"10.3390/ijms19113566","date_published":"2018-11-12T00:00:00Z","date_created":"2018-12-11T11:44:09Z","has_accepted_license":"1","isi":1,"year":"2018","day":"12","publication":"International Journal of Molecular Sciences"}]