Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Newest Articles
    • Current Issue
    • Methods & Resources
    • Archive
    • Subjects
  • Collections
  • Submit
    • Submit a Manuscript
    • Author Guidelines
    • License, Copyright, Fee
    • FAQ
    • Why Submit
  • About
    • About Us
    • Editors & Staff
    • Board Members
    • Licensing and Reuse
    • Reviewer Guidelines
    • Privacy Policy
    • Advertise
    • Contact Us
    • LSA LLC
  • Alerts
  • Other Publications
    • EMBO Press
    • The EMBO Journal
    • EMBO reports
    • EMBO Molecular Medicine
    • Molecular Systems Biology
    • Rockefeller University Press
    • Journal of Cell Biology
    • Journal of Experimental Medicine
    • Journal of General Physiology
    • Cold Spring Harbor Laboratory Press
    • Genes & Development
    • Genome Research

User menu

  • My alerts

Search

  • Advanced search
Life Science Alliance
  • Other Publications
    • EMBO Press
    • The EMBO Journal
    • EMBO reports
    • EMBO Molecular Medicine
    • Molecular Systems Biology
    • Rockefeller University Press
    • Journal of Cell Biology
    • Journal of Experimental Medicine
    • Journal of General Physiology
    • Cold Spring Harbor Laboratory Press
    • Genes & Development
    • Genome Research
  • My alerts
Life Science Alliance

Advanced Search

  • Home
  • Articles
    • Newest Articles
    • Current Issue
    • Methods & Resources
    • Archive
    • Subjects
  • Collections
  • Submit
    • Submit a Manuscript
    • Author Guidelines
    • License, Copyright, Fee
    • FAQ
    • Why Submit
  • About
    • About Us
    • Editors & Staff
    • Board Members
    • Licensing and Reuse
    • Reviewer Guidelines
    • Privacy Policy
    • Advertise
    • Contact Us
    • LSA LLC
  • Alerts
  • Follow lsa Template on Twitter
Research Article
Source Data
Transparent Process
Open Access

Fibril-induced glutamine-/asparagine-rich prions recruit stress granule proteins in mammalian cells

Katrin Riemschoss, Verena Arndt, View ORCID ProfileBenedetta Bolognesi, Philipp von Eisenhart-Rothe, Shu Liu, Oleksandra Buravlova, Yvonne Duernberger, Lydia Paulsen, Annika Hornberger, André Hossinger, View ORCID ProfileNieves Lorenzo-Gotor, Sebastian Hogl, Stephan A Müller, Gian Tartaglia, Stefan F Lichtenthaler, View ORCID ProfileIna M Vorberg  Correspondence email
Katrin Riemschoss
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Verena Arndt
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Benedetta Bolognesi
2Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Barcelona, Spain
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Benedetta Bolognesi
Philipp von Eisenhart-Rothe
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Shu Liu
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Oleksandra Buravlova
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yvonne Duernberger
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lydia Paulsen
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Annika Hornberger
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
André Hossinger
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nieves Lorenzo-Gotor
2Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Barcelona, Spain
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Nieves Lorenzo-Gotor
Sebastian Hogl
3German Center for Neurodegenerative Diseases (DZNE), Munich, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stephan A Müller
3German Center for Neurodegenerative Diseases (DZNE), Munich, Germany
7Neuroproteomics, School of Medicine, Klinikum rechts der Isar, and Institute for Advanced Study, Technical University of Munich, Munich, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gian Tartaglia
2Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Barcelona, Spain
4Universitat Pompeu Fabra, Barcelona, Spain
5Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stefan F Lichtenthaler
3German Center for Neurodegenerative Diseases (DZNE), Munich, Germany
6Munich Cluster for Systems Neurology (SyNergy), Munich, Germany
7Neuroproteomics, School of Medicine, Klinikum rechts der Isar, and Institute for Advanced Study, Technical University of Munich, Munich, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ina M Vorberg
1German Center for Neurodegenerative Diseases Bonn (DZNE e.V.), Bonn, Germany
8Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Ina M Vorberg
  • For correspondence: ina.vorberg@dzne.de
Published 2 July 2019. DOI: 10.26508/lsa.201800280
  • Article
  • Figures & Data
  • Info
  • Metrics
  • Reviewer Comments
  • PDF
Loading

Article Figures & Data

Figures

  • Supplementary Materials
  • Figure 1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 1. Aggregation state of NM-HA in mouse neuroblastoma cell populations.

    (A) Immunofluorescence staining of mouse N2a neuroblastoma cells stably expressing soluble yeast Sup35 prion domain NM tagged with the HA antibody epitope (NM-HAsol) and N2a subclones 1c, 2e, and 3b persistently producing NM-HA aggregates (NM-HAagg). NM was detected using mAb anti-HA (green), and nuclei were stained with Hoechst (blue). Scale bar: 5 μm. Note that individual cell clones differ in their respective NM-HA expression levels (Krammer et al, 2009). Cell clones had been isolated from a N2a NM-HA bulk population exposed to recombinant NM amyloid fibrils. (B) The presence of SDS-resistant NM-HA in N2a subclones was determined by a filter trap assay. NM was detected using mAb anti-HA. (C) SDD–AGE analysis of lysates from N2a cells expressing NM-HAsol and NM-HAagg. NM-HA was detected using mAb anti-HA. (D) Schematic illustration of NM-HA. A region highly abundant in Q/N at the amino-terminus is shown in blue (residues 1–38). Note that also other regions in N are enriched in Q/N. The octapepetide repeat region is depicted in green, and the carboxyterminal region of N is marked in black. Chymotrypsin preferentially cleaves at the carboxyl side of amide bonds of tyrosine, tryptophan, and phenylalanine (symbolized by arrow heads). Note that the M domain lacks these residues. Three tyrosine residues are present in the HA epitope. Putative fragments that correspond to the length of peptides identified by Western blot are indicated. (E, F) NM-HA aggregates derived from different N2a cell clones exhibit comparable chymotrypsin patterns. Lysates of N2a NM-HAsol and N2a NM-HAagg clones 1c, 2e, and 3b were subjected to increasing amounts of chymotrypsin or left untreated. Proteins were analyzed by SDS–PAGE and Western blot. NM was detected by 4A5 anti-M domain antibody raised against an epitope spanning amino acid residues 229–247 (Krammer et al, 2008b) (E) or mAb anti-HA (F) (both antibody-binding sites indicated in (D)).

  • Figure 2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 2. Interactomes of soluble and aggregated NM-HA are enriched for intrinsically disordered and nucleic acid–binding proteins.

    (A) Analyzed cell lines. Biological triplicates of N2a subclones 1c, 2e, and 3b, N2a NM-HAsol and wild-type N2a cells were subjected to mass spectrometry analysis after SDS–PAGE and in-gel trypsin digestion of immunoprecipitated NM-HA using anti-HA antibodies. (B) Number of proteins found as putative interactors of soluble (NM-HAsol) and aggregated NM-HA (NM-HAagg) from cell clones 1c, 2e, and 3b combined. (C) Putative interactors of NM-HAsol and the NM-HAagg derived subclones 1c, 2e, and 3b individually. (D) Interactomes of soluble and aggregated NM-HA are enriched for intrinsically disordered proteins. Box-plot shows intrinsic protein disorder of interactors calculated using DisProt (Dunker et al, 2002). Intrinsic disorder of interactors was compared with that of a random subset of the mouse proteome. P-values are 1.7 × 10−8 and 3.48 × 10−9, respectively. Statistics were performed using the Kolmogorov–Smirnov test. Shown below is the corresponding area under the ROC curve (AUROC). (E) Interactomes of soluble and aggregated NM-HA are enriched for nucleic binding proteins. Box-plot displays the nucleic acid binding ability of interactors calculated using the scale of nonclassical RBD (Castello et al, 2012) compared with that of a random subset of the mouse proteome. P-values are 3.30 × 10−13 and 3.46 × 10−11, respectively (Kolmogorov–Smirnov test). Shown below is the AUROC. (F) Intrinsic disorder and increased nucleic binding ability are characteristics of SG proteins. Box-plot shows intrinsic protein disorder calculated (upper panel) using DisProt (Dunker et al, 2002) and nucleic acid binding ability (lower panel) calculated using the Castello scale (Castello et al, 2012) for SGs components compared with a random subset of the human proteome. (G) Interactors of NM-HAagg have a higher propensity to assemble into cytoplasmic granules compared with a random subset of the mouse proteome (Bolognesi et al, 2016). Interactors NM-HAsol versus NM-HAagg: P = 0.2973; NM-HAsol versus random proteome: P = 0.2101; NM-HAagg versus random proteome: P = 2.348 × 10−7. Statistics were performed using the Wilcoxon test.

  • Figure 3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 3. Gene Ontology enrichment analysis of NM-HA interactomes.

    For all interactomes, the top 20 Gene Ontology biological process annotations were determined and combined in one list. Depicted are the percentages of genes that fall into this category compared with the respective interactome. Benjamini P-value is shown.

  • Figure 4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 4. Comparison of SGs and NM-HA interactomes.

    (A) Number of SG-associated proteins identified in the NM-HA interactomes. Interactomes were compared with a list of SG interactors curated from literature (Table S1) (Jain et al, 2016; Markmiller et al, 2018). Shown is the percentage of NM-HA interacting proteins that have been reported to be SG components. (B) Number of SG components interacting with both NM-HAsol and NM-HAagg. (C) Number of SG components associated with NM-HAagg in individual subclones 1c, 2e, and 3b (Table S1). (D) Enrichment of proteins with PrlDs in NM-HAsol, NM-HAagg, and SG interactomes (Table S1) compared with the human proteome (in fold change).

  • Figure S1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure S1. The N2a NM-HAagg bulk population propagates SDS-resistant NM-HA prions.

    (A) The presence of SDS-resistant NM-HA polymers in the N2a NM-HAagg bulk population was determined by a filter trap assay (top panel). SDS–PAGE and Western blot analysis were performed as loading control (bottom panel). NM-HA was detected using mAb anti-HA, and actin was detected using mAb anti-actin. (B) SDD–AGE analysis of cell lysates from wild-type N2a cells, N2a cells expressing soluble NM-HA, and the NM-HAagg bulk population. NM-HA was detected using mAb anti-HA. (C) Quantitative analysis of cells bearing aggregates in the N2a NM-HAagg bulk population. Transduced cells were plated in 96-well plates, and six wells were analyzed by automated confocal microscopy. Shown is the number of cells with aggregates within the cell population expressing the transgene. Bars represent mean values ± SD.

  • Figure 5.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 5. Shared components of NM-HA prions and SGs.

    (A) Immunofluorescence staining of N2a NM-HAsol and N2a NM-HAagg bulk cells. NM-HA was detected using mAb anti-HA (red) and SG marker TIA-1 was detected using pAb anti-TIA-1 (green). Nuclei were stained with Hoechst (blue). Scale bar: 5 μm. (B) IP of G3BP and TIAR from lysates of wild-type N2a, N2a NM-HAsol, and N2a NM-HAagg bulk cells using mAb anti-G3BP or pAb anti-TIAR, followed by SDS–PAGE and Western blot. Total cell lysate (extract) was loaded as control. G3BP and TIAR were detected using mAb anti-G3BP and pAb anti-TIAR. NM-HA was detected using mAb anti-HA. (C) N2a NM-HAsol and N2a NM-HAagg cells were incubated with 1 μM SYTO RNASelect for 30 min and subsequently fixed with methanol, followed by immunofluorescence staining. NM was detected using mAb anti-HA (red), and RNA was visualized with SYTO RNASelect (green). Nuclei were stained with Hoechst (blue). Scale bar: 5 μm. (D) N2a NM-HAsol cells were treated with 0.5 mM sodium arsenite for 1 h to induce SGs or cells were left untreated. Immunofluorescence staining was performed using mAb anti-HA (red) and pAb anti-TIAR (green). Nuclei were stained with Hoechst (blue). Scale bar: 5 μm. (E) Protein synthesis was analyzed in N2a NM-HAsol and N2a NM-HAagg cells using the SUnSET method (Schmidt et al, 2009). Cells were incubated with puromycin for 30 min. Incorporated puromycin was detected using mAb anti-puromycin (12D10). (F) Quantitative analysis of puromycin incorporation. Bars represent mean values ± SD. Statistical analysis was performed using t test (n = 3). Significant changes are indicated by asterisks (***P ≤ 0.001). (G) Viability of N2a NM-HAsol cells and N2a NM-HAagg cells was determined by XTT tetrazolium salt assay. Bars represent mean values ± SD. Statistical analysis was performed using t test (n = 3). Changes are not significant (ns).

    Source data are available for this figure.

    Source Data for Figure 5[LSA-2018-00280_SdataF5A.tif][LSA-2018-00280_SdataF5B.tif][LSA-2018-00280_SdataF5C.tif][LSA-2018-00280_SdataF5D.tif][LSA-2018-00280_SdataF5E.tif][LSA-2018-00280_SdataF5F.tif][LSA-2018-00280_SdataF5G.tif][LSA-2018-00280_SdataF5H.tif]

  • Figure S2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure S2. TDP-43 and FUS colocalize with NM-HA aggregates.

    (A) IP of TIA-1 from lysates of wild-type N2a, N2a NM-HAsol, and N2a NM-HAagg cells using mAb anti-TIA-1, followed by SDS–PAGE and Western blot. Total cell lysate (extract) was loaded as control. TIA-1 was detected using pAb anti-TIA-1. NM-HA was detected using mAb anti-HA. (B) Immunofluorescence staining of N2a NM-HAsol and N2a NM-HAagg cells. NM was detected using mAb anti-HA (red), and endogenous FUS was detected using pAb anti-FUS (green). Nuclei were stained with Hoechst (blue). Scale bar: 5 μm. (C) Wild-type N2a, N2a NM-HAsol, and N2a NM-HAagg cells were transfected with a plasmid coding for FLAG-FUS. After 48 h, FUS was immunoprecipitated by using mAb anti-FLAG, followed by SDS–PAGE and Western blot. Total cell lysate (extract) was loaded as control. FUS was detected using mAb anti-FLAG, and NM-HA was detected using mAb anti-HA. (D) N2a NM-HAsol and N2a NM-HAagg cells were transfected with a plasmid coding for TDP-43-YFP and subjected to immunofluorescence staining after 48 h. NM was detected using mAb anti-HA (red), and TDP-43 was detected using pAb anti-TDP-43 (green). Nuclei were stained with Hoechst (blue). Scale bar: 5 μm. (E) Wild-type N2a, N2a NM-HAsol, and N2a NM-HAagg cells were transfected with a plasmid coding for TDP-43-YFP. After 48 h, TDP-43 was immunoprecipitated by using mAb anti-TDP-43, followed by SDS–PAGE and Western blot. Total cell lysate (extract) was loaded as control. TDP-43 was detected using mAb anti-TDP-43, and NM was detected using mAb anti-HA.

    Source data are available for this figure.

    Source Data for Figure S2[LSA-2018-00280_SdataFS2A.tif][LSA-2018-00280_SdataFS2B.tif][LSA-2018-00280_SdataFS2C.tif][LSA-2018-00280_SdataFS2D.tif]

  • Figure S3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure S3. Interaction of NM-GFPagg with G3BP and p62.

    (A) Bulk population of N2a cells stably expressing NM-GFP (N2a NM-GFPsol) and N2a clone stably propagating NM-GFP aggregates (N2a NM-GFPagg) (Hofmann et al, 2013). N2a NM-GFPagg cells were generated by exposing N2a NM-GFPsol cells to recombinant NM fibrils and subsequent limiting dilution cloning. Scale bar: 30 μm. (B) Validation of interaction of aggregated NM-GFP with G3BP and p62. NM-GFP in lysates of N2a NM-GFPsol or N2a NM-GFPagg cells was immunoprecipitated using GFP-trap magnetic beads. Co-immunprecipitated G3BP or p62 was detected by Western blot. Note that GFP was slightly degraded. Additional lanes were excised for presentation purposes (dashed line). (C) Control IP using unspecific IgG or anti-G3BP or anti-p62 IgGs and cell lysates of N2a NM-GFPagg. Additional lanes were excised for presentation purposes (dashed lines). (D) Pull-down of Flag-FUS transiently expressed in N2a NM-GFPsol and N2a NM-GFPagg cells. GFP-trap magnetic agarose beads were used for IP. (E) Colocalization of p62 with NM-GFP in N2a NM-GFPagg cells. N2a NM-GFPsol and N2a NM-GFPagg were stained with Hoechst and anti-p62. Scale bar: 5 μm.

  • Figure S4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure S4. Association of NM-HA and NM-GFP with SGs is transient.

    (A) N2a NM-HAsol cells were either left untreated or exposed to 0.5 mM arsenite for 30 min. Medium was replaced, and cells were incubated for up to 2 h posttreatment (p.t.). Fixed cells were stained using anti-HA and anti-TIAR antibodies. Scale bar: 10 μm. (B) N2a NM-GFPsol cells exposed to 0.5 mM arsenite for 30 min. Upon replacement of medium, cells were allowed to recover and fixed up to 7 h p.t. The panels on the left show representative individual cells. The panel on the right shows an overview of treated cells (scale bars: 10 and 20 μm, respectively). Arrows indicate SGs. (C) Percentage of cells of (B) with TIAR-positive SGs (only red channel). Treatment was performed in triplicates. For each time point, three images per independent experiment were analyzed. At least 400 cells per time point for each experiment were analyzed. (D) Percentage of NM-GFP expressing cells with SGs and colocalization of NM-GFP with SGs. Images of (B) were quantified. At least 300 cells per time point for each experiment were analyzed.

  • Figure 6.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 6. Interactome validation of proteins involved in degradation pathways.

    (A) IP of endogenous p62 from cell lysates of wild-type N2a, N2a NM-HAsol, and N2a NM-HAagg cells using mAb anti-p62, followed by SDS–PAGE and Western blot. Total cell lysate (extract) was loaded as control. p62 was detected using mAb anti-p62, and NM-HA was detected using mAb anti-HA. Pull-downs using unspecific IgG served as controls. (B) Bulk N2a NM-HAagg cells were either not transfected (for p62 detection) or transfected with constructs encoding for VCP-EGFP, Keap1-GFP, or Ubiquilin-2-FLAG and subjected to immunofluorescence staining 48 h posttransfection. NM-HA was stained using mAb anti-HA (red), p62 was detected using mAb anti-p62 (green), and FLAG was stained using mAb anti-FLAG (green). GFP is shown in green. Nuclei were stained with Hoechst (blue). Scale bar: 5 μm.

  • Figure S5.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure S5. N2a NM-HAsol cells were left untreated (top row, for p62 staining) or transfected with constructs coding for VCP-GFP, Keap1-GFP, and Ubiquilin-2-FLAG and subjected to immunofluorescence staining 48 h posttransfection.

    NM-HA was stained using mAb anti-HA (red), p62 was detected using mAb anti-p62 (green), and FLAG was stained using mAb anti-FLAG (green). GFP is shown in green. Nuclei were stained with Hoechst (blue). Scale bar: 5 μm.

  • Figure 7.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 7. Fibril-induced NM prions do not evolve from SGs.

    N2a NM-HAsol cells were incubated with 5 μM recombinant NM fibrils (monomer concentration) for the indicated time points and subsequently analyzed for NM-HA aggregate induction and SGs. As a positive control, cells were incubated with 0.5 mM sodium arsenite for 1 h without addition of fibrils. Immunofluorescence staining was performed using mAb anti-HA (green) and pAb anti-TIAR (red). Nuclei were stained with Hoechst (blue). Scale bar: 10 μm.

Supplementary Materials

  • Figures
  • Table S1 Present in more than two biological replicates with ≥two unique peptides + not present in N2A (≥two UP).

PreviousNext
Back to top
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word on Life Science Alliance.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Fibril-induced glutamine-/asparagine-rich prions recruit stress granule proteins in mammalian cells
(Your Name) has sent you a message from Life Science Alliance
(Your Name) thought you would like to see the Life Science Alliance web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Prions interact with stress granule components
Katrin Riemschoss, Verena Arndt, Benedetta Bolognesi, Philipp von Eisenhart-Rothe, Shu Liu, Oleksandra Buravlova, Yvonne Duernberger, Lydia Paulsen, Annika Hornberger, André Hossinger, Nieves Lorenzo-Gotor, Sebastian Hogl, Stephan A Müller, Gian Tartaglia, Stefan F Lichtenthaler, Ina M Vorberg
Life Science Alliance Jul 2019, 2 (4) e201800280; DOI: 10.26508/lsa.201800280

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Share
Prions interact with stress granule components
Katrin Riemschoss, Verena Arndt, Benedetta Bolognesi, Philipp von Eisenhart-Rothe, Shu Liu, Oleksandra Buravlova, Yvonne Duernberger, Lydia Paulsen, Annika Hornberger, André Hossinger, Nieves Lorenzo-Gotor, Sebastian Hogl, Stephan A Müller, Gian Tartaglia, Stefan F Lichtenthaler, Ina M Vorberg
Life Science Alliance Jul 2019, 2 (4) e201800280; DOI: 10.26508/lsa.201800280
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
Issue Cover

In this Issue

Volume 2, No. 4
August 2019
  • Table of Contents
  • Cover (PDF)
  • About the Cover
  • Masthead (PDF)
Advertisement

Jump to section

  • Article
    • Abstract
    • Introduction
    • Results
    • Discussion
    • Materials and Methods
    • Acknowledgements
    • References
  • Figures & Data
  • Info
  • Metrics
  • Reviewer Comments
  • PDF

Subjects

  • Cell Biology

Related Articles

  • No related articles found.

Cited By...

  • Intercellular Transmission of a Synthetic Bacterial Cytotoxic Prion-Like Protein in Mammalian Cells
  • Intercellular transmission of a bacterial cytotoxic prion-like protein in mammalian cells
  • Google Scholar

More in this TOC Section

  • SorCS1 in amyloid-β synaptic pathology
  • The GET pathway acts in promoting mitophagy
  • Proximity to the SC promotes exchanges
Show more Research Article

Similar Articles

EMBO Press LogoRockefeller University Press LogoCold Spring Harbor Logo

Content

  • Home
  • Newest Articles
  • Current Issue
  • Archive
  • Subject Collections

For Authors

  • Submit a Manuscript
  • Author Guidelines
  • License, copyright, Fee

Other Services

  • Alerts
  • Twitter
  • RSS Feeds

More Information

  • Editors & Staff
  • Reviewer Guidelines
  • Feedback
  • Licensing and Reuse
  • Privacy Policy

ISSN: 2575-1077
© 2023 Life Science Alliance LLC

Life Science Alliance is registered as a trademark in the U.S. Patent and Trade Mark Office and in the European Union Intellectual Property Office.