Cargo-specific recruitment in clathrin- and dynamin-independent endocytosis.

Actins / metabolism Biological Transport Breast Neoplasms / genetics Cell Movement Clathrin / genetics Dynamins / genetics Endocytosis Female Humans Integrin beta1 / genetics Intracellular Signaling Peptides and Proteins / genetics rab GTP-Binding Proteins / genetics

Journal

Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575

Informations de publication

Date de publication:
10 2021
Historique:
received: 28 09 2020
accepted: 01 09 2021
pubmed: 8 10 2021
medline: 23 11 2021
entrez: 7 10 2021
Statut: ppublish

Résumé

Spatially controlled, cargo-specific endocytosis is essential for development, tissue homeostasis and cancer invasion. Unlike cargo-specific clathrin-mediated endocytosis, the clathrin- and dynamin-independent endocytic pathway (CLIC-GEEC, CG pathway) is considered a bulk internalization route for the fluid phase, glycosylated membrane proteins and lipids. While the core molecular players of CG-endocytosis have been recently defined, evidence of cargo-specific adaptors or selective uptake of proteins for the pathway are lacking. Here we identify the actin-binding protein Swiprosin-1 (Swip1, EFHD2) as a cargo-specific adaptor for CG-endocytosis. Swip1 couples active Rab21-associated integrins with key components of the CG-endocytic machinery-Arf1, IRSp53 and actin-and is critical for integrin endocytosis. Through this function, Swip1 supports integrin-dependent cancer-cell migration and invasion, and is a negative prognostic marker in breast cancer. Our results demonstrate a previously unknown cargo selectivity for the CG pathway and a role for specific adaptors in recruitment into this endocytic route.

Identifiants

DOI: 10.1038/s41556-021-00767-x PMID: 34616024
pubmed: 34616024
doi: 10.1038/s41556-021-00767-x
pii: 10.1038/s41556-021-00767-x
doi:

Substances chimiques

Actins 0
Clathrin 0
Integrin beta1 0
Intracellular Signaling Peptides and Proteins 0
WSB1 protein, human 0
RAB21 protein, human EC 3.6.1.-
rab GTP-Binding Proteins EC 3.6.5.2
Dynamins EC 3.6.5.5

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1073-1084

Commentaires et corrections

Type : CommentIn
Type : ErratumIn

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Kaksonen, M. & Roux, A. Mechanisms of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 19, 313–326 (2018).
pubmed: 29410531 doi: 10.1038/nrm.2017.132
Mettlen, M., Chen, P.-H., Srinivasan, S., Danuser, G. & Schmid, S. L. Regulation of clathrin-mediated endocytosis. Annu. Rev. Biochem. 87, 871–896 (2018).
pubmed: 29661000 pmcid: 6383209 doi: 10.1146/annurev-biochem-062917-012644
Sanger, A., Hirst, J., Davies, A. K. & Robinson, M. S. Adaptor protein complexes and disease at a glance. J. Cell Sci. 132, jcs222992 (2019).
Mayor, S., Parton, R. G. & Donaldson, J. G. Clathrin-independent pathways of endocytosis. Cold Spring Harb. Perspect. Biol. 6, a016758 (2014).
Maldonado-Báez, L., Williamson, C. & Donaldson, J. G. Clathrin-independent endocytosis: a cargo-centric view. Exp. Cell Res. 319, 2759–2769 (2013).
pubmed: 23954817 pmcid: 4157725 doi: 10.1016/j.yexcr.2013.08.008
Ferreira, A. P. A. & Boucrot, E. Mechanisms of carrier formation during clathrin-independent endocytosis. Trends Cell Biol. 28, 188–200 (2018).
pubmed: 29241687 doi: 10.1016/j.tcb.2017.11.004
Kirkham, M. et al. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465–476 (2005).
pubmed: 15668297 pmcid: 2171740 doi: 10.1083/jcb.200407078
Howes, M. T. et al. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J. Cell Biol. 190, 675–691 (2010).
pubmed: 20713605 pmcid: 2928008 doi: 10.1083/jcb.201002119
Sathe, M. et al. Small GTPases and BAR domain proteins regulate branched actin polymerisation for clathrin and dynamin-independent endocytosis. Nat. Commun. 9, 1835 (2018).
pubmed: 29743604 pmcid: 5943408 doi: 10.1038/s41467-018-03955-w
Thottacherry, J. J., Sathe, M., Prabhakara, C. & Mayor, S. Spoiled for choice: diverse endocytic pathways function at the cell surface. Annu. Rev. Cell Dev. Biol. 35, 55–84 (2019).
pubmed: 31283376 pmcid: 6917507 doi: 10.1146/annurev-cellbio-100617-062710
Pellinen, T. et al. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of β1-integrins. J. Cell Biol. 173, 767–780 (2006).
pubmed: 16754960 pmcid: 2063892 doi: 10.1083/jcb.200509019
Pellinen, T. et al. Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell 15, 371–385 (2008).
pubmed: 18804435 doi: 10.1016/j.devcel.2008.08.001
Högnäs, G. et al. Cytokinesis failure due to derailed integrin traffic induces aneuploidy and oncogenic transformation in vitro and in vivo. Oncogene 31, 3597–3606 (2012).
pubmed: 22120710 doi: 10.1038/onc.2011.527
Alanko, J. et al. Integrin endosomal signalling suppresses anoikis. Nat. Cell Biol. 17, 1412–1421 (2015).
pubmed: 26436690 pmcid: 4890650 doi: 10.1038/ncb3250
Moreno-Layseca, P., Icha, J., Hamidi, H. & Ivaska, J. Integrin trafficking in cells and tissues. Nat. Cell Biol. 21, 122–132 (2019).
pubmed: 30602723 pmcid: 6597357 doi: 10.1038/s41556-018-0223-z
Meyer, K. & Selbach, M. Quantitative affinity purification mass spectrometry: a versatile technology to study protein–protein interactions. Front. Genet. 6, 237 (2015).
pubmed: 26236332 pmcid: 4500955 doi: 10.3389/fgene.2015.00237
Hubner, N. C. et al. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189, 739–754 (2010).
pubmed: 20479470 pmcid: 2872919 doi: 10.1083/jcb.200911091
Jean, S. & Kiger, A. A. RAB21 activity assay using GST-fused APPL1. Bio-protocol 6, e1738 (2016).
pubmed: 28251173 doi: 10.21769/BioProtoc.1738
Zhu, G. et al. Structure of the APPL1 BAR-PH domain and characterization of its interaction with Rab5. EMBO J. 26, 3484–3493 (2007).
pubmed: 17581628 pmcid: 1933402 doi: 10.1038/sj.emboj.7601771
Del Olmo, T. et al. APEX2-mediated RAB proximity labeling identifies a role for RAB21 in clathrin-independent cargo sorting. EMBO Rep. 20, e47192 (2019).
pubmed: 30610016 pmcid: 6362359
Croucher, D. R. et al. Bimolecular complementation affinity purification (BiCAP) reveals dimer-specific protein interactions for ERBB2 dimers. Sci. Signal. 9, ra69 (2016).
pubmed: 27405979 doi: 10.1126/scisignal.aaf0793
Bhave, M. et al. Functional characterization of 67 endocytic accessory proteins using multiparametric quantitative analysis of CCP dynamics. Proc. Natl Acad. Sci. USA 117, 31591–31602 (2020).
pubmed: 33257546 pmcid: 7749282 doi: 10.1073/pnas.2020346117
Kumari, S. & Mayor, S. ARF1 is directly involved in dynamin-independent endocytosis. Nat. Cell Biol. 10, 30–41 (2008).
pubmed: 18084285 doi: 10.1038/ncb1666
Schnitzbauer, J., Strauss, M. T., Schlichthaerle, T., Schueder, F. & Jungmann, R. Super-resolution microscopy with DNA-PAINT. Nat. Protoc. 12, 1198–1228 (2017).
pubmed: 28518172 doi: 10.1038/nprot.2017.024
Park, E. J., Yuki, Y., Kiyono, H. & Shimaoka, M. Structural basis of blocking integrin activation and deactivation for anti-inflammation. J. Biomed. Sci. 22, 51 (2015).
pubmed: 26152212 pmcid: 4495637 doi: 10.1186/s12929-015-0159-6
Caldieri, G. et al. Reticulon 3-dependent ER–PM contact sites control EGFR nonclathrin endocytosis. Science 356, 617–624 (2017).
pubmed: 28495747 pmcid: 5432029 doi: 10.1126/science.aah6152
McMahon, H. T. & Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517–533 (2011).
pubmed: 21779028 doi: 10.1038/nrm3151
Thottacherry, J. J. et al. Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells. Nat. Commun. 9, 4217 (2018).
pubmed: 30310066 pmcid: 6181995 doi: 10.1038/s41467-018-06738-5
Krugmann, S. et al. Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr. Biol. 11, 1645–1655 (2001).
pubmed: 11696321 doi: 10.1016/S0960-9822(01)00506-1
Vaggi, F. et al. The Eps8/IRSp53/VASP network differentially controls actin capping and bundling in filopodia formation. PLoS Comput. Biol. 7, e1002088 (2011).
pubmed: 21814501 pmcid: 3140970 doi: 10.1371/journal.pcbi.1002088
Disanza, A. et al. CDC42 switches IRSp53 from inhibition of actin growth to elongation by clustering of VASP. EMBO J. 32, 2735–2750 (2013).
pubmed: 24076653 pmcid: 3801440 doi: 10.1038/emboj.2013.208
Lundmark, R. et al. The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr. Biol. 18, 1802–1808 (2008).
pubmed: 19036340 pmcid: 2726289 doi: 10.1016/j.cub.2008.10.044
Hemalatha, A. & Mayor, S. Recent advances in clathrin-independent endocytosis. F1000Research 8, 138 (2019).
Park, K. R. et al. Structural implications of Ca
pubmed: 27974828 pmcid: 5156911 doi: 10.1038/srep39095
Ariotti, N. et al. Modular detection of GFP-labeled proteins for rapid screening by electron microscopy in cells and organisms. Dev. Cell 35, 513–525 (2015).
pubmed: 26585296 doi: 10.1016/j.devcel.2015.10.016
Paul, N. R., Jacquemet, G. & Caswell, P. T. Endocytic trafficking of integrins in cell migration. Curr. Biol. 25, R1092–R1105 (2015).
pubmed: 26583903 doi: 10.1016/j.cub.2015.09.049
Lim, K. B. et al. The Cdc42 effector IRSp53 generates filopodia by coupling membrane protrusion with actin dynamics. J. Biol. Chem. 283, 20454–20472 (2008).
pubmed: 18448434 doi: 10.1074/jbc.M710185200
Miki, H., Yamaguchi, H., Suetsugu, S. & Takenawa, T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732–735 (2000).
pubmed: 11130076 doi: 10.1038/35047107
Pipathsouk, A. et al. WAVE complex self-organization templates lamellipodial formation. J. Cell Biol. 220, e202003086 (2021).
pubmed: 34096975 pmcid: 8185649 doi: 10.1083/jcb.202003086
Koronakis, V. et al. WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc. Natl Acad. Sci. USA 108, 14449–14454 (2011).
pubmed: 21844371 pmcid: 3167530 doi: 10.1073/pnas.1107666108
Schlienger, S., Ramirez, R. A. M. & Claing, A. ARF1 regulates adhesion of MDA-MB-231 invasive breast cancer cells through formation of focal adhesions. Cell. Signal. 27, 403–415 (2015).
pubmed: 25530216 doi: 10.1016/j.cellsig.2014.11.032
Norman, J. C. et al. ARF1 mediates paxillin recruitment to focal adhesions and potentiates Rho-stimulated stress fiber formation in intact and permeabilized Swiss 3T3 fibroblasts. J. Cell Biol. 143, 1981–1995 (1998).
pubmed: 9864369 pmcid: 2175234 doi: 10.1083/jcb.143.7.1981
Shafaq-Zadah, M. et al. Persistent cell migration and adhesion rely on retrograde transport of β
pubmed: 26641717 doi: 10.1038/ncb3287
Ezratty, E. J., Bertaux, C., Marcantonio, E. E. & Gundersen, G. G. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J. Cell Biol. 187, 733–747 (2009).
pubmed: 19951918 pmcid: 2806590 doi: 10.1083/jcb.200904054
Sahgal, P. et al. GGA2 and RAB13 promote activity-dependent β1-integrin recycling. J. Cell Sci. 132, jcs233387 (2019).
pubmed: 31076515 doi: 10.1242/jcs.233387
Hornbruch-Freitag, C., Griemert, B., Buttgereit, D. & Renkawitz-Pohl, R. Drosophila Swiprosin-1/EFHD2 accumulates at the prefusion complex stage during Drosophila myoblast fusion. J. Cell Sci. 124, 3266–3278 (2011).
pubmed: 21896648 doi: 10.1242/jcs.083907
Fan, C.-C. et al. EFHD2 promotes epithelial-to-mesenchymal transition and correlates with postsurgical recurrence of stage I lung adenocarcinoma. Sci. Rep. 7, 14617 (2017).
pubmed: 29097801 pmcid: 5668280 doi: 10.1038/s41598-017-15186-y
Zhang, S. et al. Swiprosin-1 deficiency impairs macrophage immune response of septic mice. JCI Insight 3, e95396 (2018).
pmcid: 5821171 doi: 10.1172/jci.insight.95396
Tu, Y. et al. EFhd2/swiprosin-1 regulates LPS-induced macrophage recruitment via enhancing actin polymerization and cell migration. Int. Immunopharmacol. 55, 263–271 (2018).
pubmed: 29288926 doi: 10.1016/j.intimp.2017.12.030
Reimer, D. et al. B cell speed and B-FDC contacts in germinal centers determine plasma cell output via Swiprosin-1/EFhd2. Cell Rep. 32, 108030 (2020).
pubmed: 32783949 doi: 10.1016/j.celrep.2020.108030
Paul, F. E., Hosp, F. & Selbach, M. Analyzing protein–protein interactions by quantitative mass spectrometry. Methods 54, 387–395 (2011).
pubmed: 21382495 doi: 10.1016/j.ymeth.2011.03.001
Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).
pubmed: 19029910 doi: 10.1038/nbt.1511
Borchers, H. W. pracma: Practical Numerical Math Functions (R Foundation for Statistical Computing, 2019).
Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
pubmed: 30395289 doi: 10.1093/nar/gky1106
Ovesný, M., Křížek, P., Borkovec, J., Svindrych, Z. & Hagen, G. M. ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics 30, 2389–2390 (2014).
pubmed: 24771516 pmcid: 4207427 doi: 10.1093/bioinformatics/btu202
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772 doi: 10.1038/nmeth.2019
Martens, K. J. A., Bader, A. N., Baas, S., Rieger, B. & Hohlbein, J. Phasor based single-molecule localization microscopy in 3D (pSMLM-3D): an algorithm for MHz localization rates using standard CPUs. J. Chem. Phys. 148, 123311 (2018).
pubmed: 29604874 doi: 10.1063/1.5005899
Farage, E. & Caswell, P. T. Quantitative analysis of integrin trafficking. Methods Mol. Biol. 2217, 251–263 (2021).
pubmed: 33215385 doi: 10.1007/978-1-0716-0962-0_14
Arjonen, A., Alanko, J., Veltel, S. & Ivaska, J. Distinct recycling of active and inactive β1 integrins. Traffic 13, 610–625 (2012).
pubmed: 22222055 pmcid: 3531618 doi: 10.1111/j.1600-0854.2012.01327.x
Berginski, M. E. & Gomez, S. M. The Focal Adhesion Analysis Server: a web tool for analyzing focal adhesion dynamics. F1000Research 2, 68 (2013).
pubmed: 24358855 pmcid: 3752736 doi: 10.12688/f1000research.2-68.v1
Krull, A., Buchholz, T.-O. & Jug, F. Noise2Void—learning denoising from single noisy images. IEEE/CVF Conf. Comp. Vision Pattern Recog. (CVPR) 2019, 2124–2132 (2019).
von Chamier, L. et al. Democratising deep learning for microscopy with ZeroCostDL4Mic. Nat. Commun. 12, 2276 (2021).
doi: 10.1038/s41467-021-22518-0
Arganda-Carreras, I. et al. Trainable Weka Segmentation: a machine learning tool for microscopy pixel classification. Bioinformatics 33, 2424–2426 (2017).
pubmed: 28369169 doi: 10.1093/bioinformatics/btx180
Gilles, J.-F., Dos Santos, M., Boudier, T., Bolte, S. & Heck, N. DiAna, an ImageJ tool for object-based 3D co-localization and distance analysis. Methods 115, 55–64 (2017).
pubmed: 27890650 doi: 10.1016/j.ymeth.2016.11.016
Jacquemet, G. Archived source code for cargo-specific recruitment in clathrin and dynamin-independent endocytosis. Zenodo https://doi.org/10.5281/zenodo.4812018 (2021).
Fazeli, E. et al. Automated cell tracking using StarDist and TrackMate. F1000Research 9, 1279 (2020).
pubmed: 33224481 pmcid: 7670479 doi: 10.12688/f1000research.27019.1
Tinevez, J.-Y. et al. TrackMate: an open and extensible platform for single-particle tracking. Methods 115, 80–90 (2017).
pubmed: 27713081 doi: 10.1016/j.ymeth.2016.09.016
Schmidt, U., Weigert, M., Broaddus, C. & Myers, G. in Medical Image Computing and Computer Assisted Intervention—MICCAI 2018 (eds Frangi, A. F. et al.) 265–273 (Springer, 2018); https://doi.org/10.1007/978-3-030-00934-2_30
Al-Akhrass, H., Ivaska, J. & Jacquemet, G. Stardist model and training dataset for automated tracking of MDA-MB-231 and BT20 cells. Zenodo https://doi.org/10.5281/zenodo.4811213 (2021).
Postma, M. & Goedhart, J. PlotsOfData—a web app for visualizing data together with their summaries. PLOS Biol. 17, e3000202 (2019).
pubmed: 30917112 pmcid: 6453475 doi: 10.1371/journal.pbio.3000202
Heuser, V. D. et al. Formin proteins FHOD1 and INF2 in triple-negative breast cancer: association with basal markers and functional activities. Breast Cancer 12, 1178223418792247 (2018).
pubmed: 30158824 pmcid: 6109849
Dunkler, D., Ploner, M., Schemper, M. & Heinze, G. Weighted Cox regression using the R package coxphw. J. Stat. Softw. 84, 1–26 (2018).
doi: 10.18637/jss.v084.i02
Legler, K. et al. Reduced mannosidase MAN1A1 expression leads to aberrant N-glycosylation and impaired survival in breast cancer. Br. J. Cancer 118, 847–856 (2018).
pubmed: 29381688 pmcid: 5877434 doi: 10.1038/bjc.2017.472
Stamm, H. et al. Targeting the TIGIT–PVR immune checkpoint axis as novel therapeutic option in breast cancer. OncoImmunology 8, e1674605 (2019).
pubmed: 31741778 pmcid: 6844319 doi: 10.1080/2162402X.2019.1674605
Milde-Langosch, K. et al. Prognostic relevance of glycosylation-associated genes in breast cancer. Breast Cancer Res. Treat. 145, 295–305 (2014).
pubmed: 24737166 doi: 10.1007/s10549-014-2949-z

Auteurs

Paulina Moreno-Layseca (P)

Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany.
ORCID: 0000-0002-9456-4178

Niklas Z Jäntti (NZ)

Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
ORCID: 0000-0003-1547-0390

Rashmi Godbole (R)

National Centre for Biological Science (TIFR), Bangalore, India.
The University of Trans-Disciplinary Health Sciences and Technology (TDU), Bangalore, India.

Christian Sommer (C)

Max-Delbrück-Centrum für Molekulare Medizin (MDC), Berlin, Germany.

Guillaume Jacquemet (G)

Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Turku, Finland.
ORCID: 0000-0002-9286-920X

Hussein Al-Akhrass (H)

Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
ORCID: 0000-0002-9630-3000

James R W Conway (JRW)

Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
ORCID: 0000-0003-3787-277X

Pauliina Kronqvist (P)

Institute of Biomedicine, Faculty of Medicine, University of Turku, Turku, Finland.

Roosa E Kallionpää (RE)

Auria Biobank, Turku University Hospital and University of Turku, Turku, Finland.
ORCID: 0000-0003-0146-0060

Leticia Oliveira-Ferrer (L)

University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany.

Pasquale Cervero (P)

University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany.
ORCID: 0000-0002-9417-7733

Stefan Linder (S)

University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany.
ORCID: 0000-0001-8226-2802

Martin Aepfelbacher (M)

University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany.

Henrik Zauber (H)

Max-Delbrück-Centrum für Molekulare Medizin (MDC), Berlin, Germany.

James Rae (J)

Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland, Australia.

Robert G Parton (RG)

Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland, Australia.
Centre for Microscopy and Microanalysis, University of Queensland, Brisbane, Queensland, Australia.
ORCID: 0000-0002-7494-5248

Andrea Disanza (A)

IFOM, Fondazione Istituto FIRC di Oncologia Molecolare and University of Milan, Milan, Italy.
ORCID: 0000-0001-5101-2907

Giorgio Scita (G)

IFOM, Fondazione Istituto FIRC di Oncologia Molecolare and University of Milan, Milan, Italy.
ORCID: 0000-0001-7984-1889

Satyajit Mayor (S)

National Centre for Biological Science (TIFR), Bangalore, India.

Matthias Selbach (M)

Max-Delbrück-Centrum für Molekulare Medizin (MDC), Berlin, Germany.
ORCID: 0000-0003-2454-8751

Stefan Veltel (S)

University Medical Center Hamburg-Eppendorf (UKE), Hamburg, Germany. Stefan.Veltel@hs-bremen.de.
Hochschule Bremen, City University of Applied Sciences, Bremen, Germany. Stefan.Veltel@hs-bremen.de.
ORCID: 0000-0002-4925-3776

Johanna Ivaska (J)

Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland. Johanna.Ivaska@utu.fi.
Department of Life Sciences, University of Turku, Turku, Finland. Johanna.Ivaska@utu.fi.
InFLAMES Research Flagship Center, University of Turku, Turku, Finland. Johanna.Ivaska@utu.fi.
ORCID: 0000-0002-6295-6556

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines du cytosquelette › Protéines des microfilaments › Actines › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Métabolisme › Transport biologique › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Maladies de la peau et du tissu conjonctif › Maladies de la peau › Maladies du sein › Tumeurs du sein › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Phénomènes physiologiques › Mouvement cellulaire › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Protéines du transport vésiculaire › Clathrine › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Protéines du transport vésiculaire › Dynamines › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Endocytose › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs immunologiques › Intégrines › Chaines bêta des intégrines › Antigènes CD29 › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Cargo-specific recruitment in clathrin- and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines G › Protéines G monomériques › Protéines G rab › Cargo-specific recruitment in clathrin- and...