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Mycobacterium marinum antagonistically induces an autophagic response while repressing the autophagic flux in a TORC1- and ESX-1-dependent manner

Cardenal-Muñoz, Elena, Arafah, Sonia, López-Jiménez, Ana Teresa, Kicka, Sébastien, Falaise, Alexandra, Bach, Frauke, Schaad, Olivier, King, Jason S., Hagedorn, Monica, Soldati, Thierry·2017·PLOS Pathogens
DOI 10.1371/journal.ppat.1006344PMC PMC5407849
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Fig 1 M. marinum induces an early autophagic response in D. discoideum. A. Two representative maximum projections showing GFP-Atg8-expressing cells infected (bottom) or mock-infected (top) with mCherry-expressing wt M. marinum. Images were recorded live 1.5 h after infection. White arrowheads point to GFP-Atg8 structures. Scale bars, 10 μm; B. The median and interquartile ranges of the number of GFP-Atg8 structures per cell were calculated. For each condition, 300 cells from independent triplicates were counted. Mann-Whitney test (****p ≤ 0.0001); C. Single sections of live GFP-Atg8-expressing amoebae 1.5 h after infection with mCherry-expressing M. marinum wt. White, magenta and yellow arrowheads point to GFP-Atg8 dots, patches and GFP-Atg8-positive (GFP-Atg8+) MCV, respectively. Scale bars, 5 μm; D. At 1.5 hpi, 256 cells (100%) with GFP-Atg8+ M. marinum were classified as in C. Means and standard deviations from three independent infections are represented; E. EM of the different types of autophagosomes in the vicinity of the MCV at 7 hpi. White asterisks label bacteria, white arrowheads point to round phagophores and autophagosomes, magenta arrowheads point to extended autophagosomes, and the yellow arrowhead indicates a double membrane compartment containing mycobacteria. Nuclei <N>. Scale bars, 1 μm; F. Sections (top) and maximum projections (bottom) showing co-localization (white arrowheads) of autophagy markers with bacteria at 1–1.5 hpi. Around 50% and 30% of the Atg8-positive bacteria were also positive for Ub and GFP-p62, respectively. Scale bars, 5 μm; G. qPCR results of relative abundance of atg8a, atg8b, atg1 and p62 mRNAs at 3 hpi. The mRNA level in non-infected cells is indicated as 1. The mRNA level of the housekeeping gene gapdh was used for normalization. Means and standard deviations from three independent experiments performed in triplicates are represented.
Fig 1 M. marinum induces an early autophagic response in D. discoideum. A. Two representative maximum projections showing GFP-Atg8-expressing cells infected (bottom) or mock-infected (top) with mCherry-expressing wt M. marinum. Images were recorded live 1.5 h after infection. White arrowheads point to GFP-Atg8 structures. Scale bars, 10 μm; B. The median and interquartile ranges of the number of GFP-Atg8 structures per cell were calculated. For each condition, 300 cells from independent triplicates were counted. Mann-Whitney test (****p ≤ 0.0001); C. Single sections of live GFP-Atg8-expressing amoebae 1.5 h after infection with mCherry-expressing M. marinum wt. White, magenta and yellow arrowheads point to GFP-Atg8 dots, patches and GFP-Atg8-positive (GFP-Atg8+) MCV, respectively. Scale bars, 5 μm; D. At 1.5 hpi, 256 cells (100%) with GFP-Atg8+ M. marinum were classified as in C. Means and standard deviations from three independent infections are represented; E. EM of the different types of autophagosomes in the vicinity of the MCV at 7 hpi. White asterisks label bacteria, white arrowheads point to round phagophores and autophagosomes, magenta arrowheads point to extended autophagosomes, and the yellow arrowhead indicates a double membrane compartment containing mycobacteria. Nuclei <N>. Scale bars, 1 μm; F. Sections (top) and maximum projections (bottom) showing co-localization (white arrowheads) of autophagy markers with bacteria at 1–1.5 hpi. Around 50% and 30% of the Atg8-positive bacteria were also positive for Ub and GFP-p62, respectively. Scale bars, 5 μm; G. qPCR results of relative abundance of atg8a, atg8b, atg1 and p62 mRNAs at 3 hpi. The mRNA level in non-infected cells is indicated as 1. The mRNA level of the housekeeping gene gapdh was used for normalization. Means and standard deviations from three independent experiments performed in triplicates are represented.CC BY · PubMed Central
Fig 2 Artificial induction of autophagy restricts M. marinum proliferation. A. GFP-Atg8-expressing cells were infected for 5 h with mCherry-expressing M. marinum wt and treated or not with AR-12 at 2.5 μM for 2 additional hours. Representative maximum projections of live imaging are shown. White arrowheads point to GFP-Atg8 recruitment to MCV. Scale bars, 10 μm; B. Quantification of the percentage of infected cells with GFP-Atg8+ bacteria at 7 hpi. Means and standard deviations from six (mock) and three (AR-12) independent replicates are represented and an unpaired t test showed no statistical significance (ns, p > 0.05). 688 and 297 infected cells were counted for the mock and the AR-12 treatments, respectively; C. Classification of types of GFP-recruitment for infected mock (258 cells) and AR-12 (141 cells) treated. Means and standard deviations from six (mock) and three (AR-12) independent replicates are represented. Unpaired t test (**p ≤ 0.01; ***p ≤ 0.001); D. Cells infected with lux-expressing M. marinum wt bacteria were treated or not with AR-12 at 2.5 μM. Intracellular bacteria growth [relative luminescence units (RLU)] is represented as the mean and standard deviation from triplicates. Statistical differences were calculated with a Bonferroni post hoc test after two-way ANOVA (*p ≤ 0.05).
Fig 2 Artificial induction of autophagy restricts M. marinum proliferation. A. GFP-Atg8-expressing cells were infected for 5 h with mCherry-expressing M. marinum wt and treated or not with AR-12 at 2.5 μM for 2 additional hours. Representative maximum projections of live imaging are shown. White arrowheads point to GFP-Atg8 recruitment to MCV. Scale bars, 10 μm; B. Quantification of the percentage of infected cells with GFP-Atg8+ bacteria at 7 hpi. Means and standard deviations from six (mock) and three (AR-12) independent replicates are represented and an unpaired t test showed no statistical significance (ns, p > 0.05). 688 and 297 infected cells were counted for the mock and the AR-12 treatments, respectively; C. Classification of types of GFP-recruitment for infected mock (258 cells) and AR-12 (141 cells) treated. Means and standard deviations from six (mock) and three (AR-12) independent replicates are represented. Unpaired t test (**p ≤ 0.01; ***p ≤ 0.001); D. Cells infected with lux-expressing M. marinum wt bacteria were treated or not with AR-12 at 2.5 μM. Intracellular bacteria growth [relative luminescence units (RLU)] is represented as the mean and standard deviation from triplicates. Statistical differences were calculated with a Bonferroni post hoc test after two-way ANOVA (*p ≤ 0.05).CC BY · PubMed Central
Fig 3 Autophagy is necessary for the maintenance of the MCV. A. The intracellular growth of lux-expressing M. marinum wt was monitored inside wt and atg1- cells. RLUs are represented as the mean and standard deviation from quadruplicates. Statistical differences were calculated with a Bonferroni post hoc test after two-way ANOVA (**p ≤ 0.01; (****p ≤ 0.0001); B. EM of the locations of M. marinum wt inside wt and atg1- cells at 0.25, 1 and 6 hpi. Black and orange asterisks label bacteria inside a compartment or in the cytosol, respectively. Black arrowheads mark the zoomIn. Nuclei <N>. Scale bars, 2 μm; C. D. discoideum wt, atg8- and atg1- cells were infected with mCherry-expressing M. marinum, fixed and stained against Ub (green) and mCherry (red). Representative maximum projections at 0.25 and 6 hpi are shown. White arrowheads label the ubiquitinated bacteria. Scale bars, 10 μm; D. Quantification of the percentage of intracellular bacteria/MCVs (red) positive for Ub (green) in wt, atg8-, atg1- and atg1-Atg1-GFP cells at 0.25 and 6 hpi. Means and standard deviations from 2–3 independent experiments. 128–299 infected cells were counted per time point and cell line. Unpaired t test (*p ≤ 0.05; ***p ≤ 0.001; **** p ≤ 0.0001).
Fig 3 Autophagy is necessary for the maintenance of the MCV. A. The intracellular growth of lux-expressing M. marinum wt was monitored inside wt and atg1- cells. RLUs are represented as the mean and standard deviation from quadruplicates. Statistical differences were calculated with a Bonferroni post hoc test after two-way ANOVA (**p ≤ 0.01; (****p ≤ 0.0001); B. EM of the locations of M. marinum wt inside wt and atg1- cells at 0.25, 1 and 6 hpi. Black and orange asterisks label bacteria inside a compartment or in the cytosol, respectively. Black arrowheads mark the zoomIn. Nuclei <N>. Scale bars, 2 μm; C. D. discoideum wt, atg8- and atg1- cells were infected with mCherry-expressing M. marinum, fixed and stained against Ub (green) and mCherry (red). Representative maximum projections at 0.25 and 6 hpi are shown. White arrowheads label the ubiquitinated bacteria. Scale bars, 10 μm; D. Quantification of the percentage of intracellular bacteria/MCVs (red) positive for Ub (green) in wt, atg8-, atg1- and atg1-Atg1-GFP cells at 0.25 and 6 hpi. Means and standard deviations from 2–3 independent experiments. 128–299 infected cells were counted per time point and cell line. Unpaired t test (*p ≤ 0.05; ***p ≤ 0.001; **** p ≤ 0.0001).CC BY · PubMed Central
Fig 4 The early autophagic response caused by M. marinum infection is dependent on ESX-1. A. Percentage of cells containing GFP-Atg8+ M. marinum wt and ΔRD1 at 1.5, 7 and 24 hpi. Means and standard deviations from independent triplicates. A mean of 375 and 230 infected cells per time point was counted for M. marinum wt and ΔRD1 infection, respectively; B. Percentage of M. marinum wt and ΔRD1 bacteria positive for GFP-Ub. Mean and standard deviation from independent triplicates; C. GFP-Ub-expressing atg1- cells were infected with Vibrant DyeCycle Ruby-labelled M. marinum wt, ΔRD1 and ΔRD1::2F9. Means and standard deviations from independent duplicates of the percentage of bacteria positive for GFP-Ub at 7 hpi. A mean of 72–98 bacteria per infection was counted. Unpaired t test (**p ≤ 0.01); D. D. discoideum wt and atg1- cells were infected with lux-expressing M. marinum wt and ΔRD1. The intracellular bacteria growth (RLUs) from triplicates was monitored. Statistical differences at the end of the experiment were calculated with a Bonferroni post hoc test after two-way ANOVA (****p ≤ 0.0001); E. qPCR results of relative abundance of atg8a, atg8b, atg1 and p62 mRNAs at 2, 5 and 24 hpi with M. marinum wt (blue outline) and ΔRD1 (red outline). The mRNA level in non-infected cells is indicated as 1 in the figure (dashed line). The mRNA level of the housekeeping gene gapdh was used for normalization. Means and standard deviations from three independent experiments performed in triplicates are represented; F. GFP-Atg8-expressing cells were infected or mock-infected for 1.5 or 7 h with mCherry-expressing M. marinum wt or with DsRed-expressing M. marinum ΔRD1. Maximum projections were used to measure the Integrated Density (IntDen) of the cytosolic GFP-Atg8 fluorescence compared to the extracellular IntDen (background). Median with interquartile ranges of the cytosolic GFP-Atg8 IntDen per cell. Each dot represents one cell. 210–357 cells per condition from three independent experiments were counted. Mann-Whitney test (****p ≤ 0.0001; **p ≤ 0.01; ns, p > 0.05).
Fig 4 The early autophagic response caused by M. marinum infection is dependent on ESX-1. A. Percentage of cells containing GFP-Atg8+ M. marinum wt and ΔRD1 at 1.5, 7 and 24 hpi. Means and standard deviations from independent triplicates. A mean of 375 and 230 infected cells per time point was counted for M. marinum wt and ΔRD1 infection, respectively; B. Percentage of M. marinum wt and ΔRD1 bacteria positive for GFP-Ub. Mean and standard deviation from independent triplicates; C. GFP-Ub-expressing atg1- cells were infected with Vibrant DyeCycle Ruby-labelled M. marinum wt, ΔRD1 and ΔRD1::2F9. Means and standard deviations from independent duplicates of the percentage of bacteria positive for GFP-Ub at 7 hpi. A mean of 72–98 bacteria per infection was counted. Unpaired t test (**p ≤ 0.01); D. D. discoideum wt and atg1- cells were infected with lux-expressing M. marinum wt and ΔRD1. The intracellular bacteria growth (RLUs) from triplicates was monitored. Statistical differences at the end of the experiment were calculated with a Bonferroni post hoc test after two-way ANOVA (****p ≤ 0.0001); E. qPCR results of relative abundance of atg8a, atg8b, atg1 and p62 mRNAs at 2, 5 and 24 hpi with M. marinum wt (blue outline) and ΔRD1 (red outline). The mRNA level in non-infected cells is indicated as 1 in the figure (dashed line). The mRNA level of the housekeeping gene gapdh was used for normalization. Means and standard deviations from three independent experiments performed in triplicates are represented; F. GFP-Atg8-expressing cells were infected or mock-infected for 1.5 or 7 h with mCherry-expressing M. marinum wt or with DsRed-expressing M. marinum ΔRD1. Maximum projections were used to measure the Integrated Density (IntDen) of the cytosolic GFP-Atg8 fluorescence compared to the extracellular IntDen (background). Median with interquartile ranges of the cytosolic GFP-Atg8 IntDen per cell. Each dot represents one cell. 210–357 cells per condition from three independent experiments were counted. Mann-Whitney test (****p ≤ 0.0001; **p ≤ 0.01; ns, p > 0.05).CC BY · PubMed Central
Fig 5 Expression of ESX-1 is essential to devoid the MCV of proteolytic activity. Cells expressing GFP-Rab11c, GFP-Rab7a or VatB-RFP, or incubated with LysoSensor Green or DQ Green BSA were infected for 1.5 and 7h with M. marinum wt or ΔRD1 labelled with Vibrant DyeCycle Ruby or expressing mCherry, DsRed or GFP. Representative sections of live imaging at 7 hpi are shown in A, C, E, G and I. White arrowheads point to the sites of recruitment/co-localization to the MCV. Scale bars, 10 μm; The percentage of bacteria/MCVs positive for GFP-Rab11c (B), GFP-Rab7a (D), VatB-RFP (F), LysoSensor Green (H) or DQ Green BSA (J) at 1.5 and 7 hpi was quantified. Mean and standard deviation from 2–3 independent experiments. A minimum of 100 infected cells were counted for each cell line. Unpaired t test compared wt and ΔRD1 bacteria (*p ≤ 0.05; **p ≤ 0.01).
Fig 5 Expression of ESX-1 is essential to devoid the MCV of proteolytic activity. Cells expressing GFP-Rab11c, GFP-Rab7a or VatB-RFP, or incubated with LysoSensor Green or DQ Green BSA were infected for 1.5 and 7h with M. marinum wt or ΔRD1 labelled with Vibrant DyeCycle Ruby or expressing mCherry, DsRed or GFP. Representative sections of live imaging at 7 hpi are shown in A, C, E, G and I. White arrowheads point to the sites of recruitment/co-localization to the MCV. Scale bars, 10 μm; The percentage of bacteria/MCVs positive for GFP-Rab11c (B), GFP-Rab7a (D), VatB-RFP (F), LysoSensor Green (H) or DQ Green BSA (J) at 1.5 and 7 hpi was quantified. Mean and standard deviation from 2–3 independent experiments. A minimum of 100 infected cells were counted for each cell line. Unpaired t test compared wt and ΔRD1 bacteria (*p ≤ 0.05; **p ≤ 0.01).CC BY · PubMed Central
Fig 6 The autophagic flux is blocked during wt M. marinum infection. A. GFP-Atg8-expressing cells were infected or mock-infected for 0.5 or 6 h with mCherry-expressing M. marinum wt or with DsRed-expressing M. marinum ΔRD1 and treated or not with a PI cocktail at 2.5× for one additional hour. Representative maximum projections of live imaging at 1.5 hpi are shown. Scale bars, 10 μm; B. Medians with interquartile ranges of the number of GFP-Atg8 structures per cell from the infections carried out in A. Each dot represents one cell. 178–338 cells per condition from three independent experiments were counted. The λ that define the Poisson distribution of each data set and differences between them were calculated as described in Materials and Methods (*p ≤ 0.05; ****p ≤ 0.0001; ns, p > 0.05); C. Mean and standard deviation of the log2 (λPI/λmock) from the three independent replicates represented in B. A log2 (λPI/λmock) of zero implies that there was a total autophagic block. p-values calculated as described in Materials and Methods (****p ≤ 0.0001; ns, p > 0.05). D. Samples from infections (A) were immunoblotted against GFP. Longer exposure of the free GFP bands is shown as "GFP (high)". Ponceau-S staining as loading control. Representative result from four independent experiments E. Means and standard deviations of the ratio GFP/GFP-Atg8 from the immunoblots represented in D. Unpaired t test (*p ≤ 0.05; **p ≤ 0.01; ns, p > 0.05). F. EM of D. discoideum infected with M. marinum wt for 7 h and incubated or not with PI at 2.5× for an additional hour. White and green asterisks label bacteria and autophagosomes, respectively. White arrowheads point to membrane extensions originating at the MCV. The black arrowhead marks the zoomIn. Scale bars, 2 μm.
Fig 6 The autophagic flux is blocked during wt M. marinum infection. A. GFP-Atg8-expressing cells were infected or mock-infected for 0.5 or 6 h with mCherry-expressing M. marinum wt or with DsRed-expressing M. marinum ΔRD1 and treated or not with a PI cocktail at 2.5× for one additional hour. Representative maximum projections of live imaging at 1.5 hpi are shown. Scale bars, 10 μm; B. Medians with interquartile ranges of the number of GFP-Atg8 structures per cell from the infections carried out in A. Each dot represents one cell. 178–338 cells per condition from three independent experiments were counted. The λ that define the Poisson distribution of each data set and differences between them were calculated as described in Materials and Methods (*p ≤ 0.05; ****p ≤ 0.0001; ns, p > 0.05); C. Mean and standard deviation of the log2 (λPI/λmock) from the three independent replicates represented in B. A log2 (λPI/λmock) of zero implies that there was a total autophagic block. p-values calculated as described in Materials and Methods (****p ≤ 0.0001; ns, p > 0.05). D. Samples from infections (A) were immunoblotted against GFP. Longer exposure of the free GFP bands is shown as "GFP (high)". Ponceau-S staining as loading control. Representative result from four independent experiments E. Means and standard deviations of the ratio GFP/GFP-Atg8 from the immunoblots represented in D. Unpaired t test (*p ≤ 0.05; **p ≤ 0.01; ns, p > 0.05). F. EM of D. discoideum infected with M. marinum wt for 7 h and incubated or not with PI at 2.5× for an additional hour. White and green asterisks label bacteria and autophagosomes, respectively. White arrowheads point to membrane extensions originating at the MCV. The black arrowhead marks the zoomIn. Scale bars, 2 μm.CC BY · PubMed Central
Fig 7 The early autophagic response, but not the flux blockade induced by M. marinum depends on TORC1. A. Scheme of the putative TORC1 and Ragulator complexes in D. discoideum. Only the proteins conserved in the amoeba are represented. Green arrows indicate activation; red lines, inhibition; B and D. D. discoideum was infected or not with mCherry-expressing M. marinum wt or with DsRed-expressing M. marinum ΔRD1 for 1.5 and 7 hpi and immunoblotted against p-Raptor(S863) (B), and p-4E-BP1(T70) (D). Abp1 was used as loading control. Shown are representative results from four independent experiments; C and E. Mean and standard deviation of the ratio p-Raptor(S863)/Abp1 (C) and p-4E-BP1(T70)/Abp1 (E) from the immunoblots represented in B and D. Unpaired t test (*p ≤ 0.05; **p ≤ 0.01); F. Sections of live cells expressing Lamtor1-GFP, GFP-Rheb, GFP-Lst8 or GFP-Raptor and infected with mCherry-expressing M. marinum wt for 1.5 h. White arrowheads point to the recruitment of the GFP-constructs to the MCV. Scale bars, 10 μm; G. Quantification of the percentage of cells carrying mCherry-expressing M. marinum wt or DsRed-expressing M. marinum ΔRD1 positive for Lamtor1-GFP, GFP-Rheb, GFP-Lst8 or GFP-Raptor at 1.5 and 7 hpi. Mean and standard deviation from three to six independent experiments. A minimum of 100 infected cells were counted for each cell line. Unpaired t test compared wt and ΔRD1 bacteria (*p ≤ 0.05; **p ≤ 0.01).
Fig 7 The early autophagic response, but not the flux blockade induced by M. marinum depends on TORC1. A. Scheme of the putative TORC1 and Ragulator complexes in D. discoideum. Only the proteins conserved in the amoeba are represented. Green arrows indicate activation; red lines, inhibition; B and D. D. discoideum was infected or not with mCherry-expressing M. marinum wt or with DsRed-expressing M. marinum ΔRD1 for 1.5 and 7 hpi and immunoblotted against p-Raptor(S863) (B), and p-4E-BP1(T70) (D). Abp1 was used as loading control. Shown are representative results from four independent experiments; C and E. Mean and standard deviation of the ratio p-Raptor(S863)/Abp1 (C) and p-4E-BP1(T70)/Abp1 (E) from the immunoblots represented in B and D. Unpaired t test (*p ≤ 0.05; **p ≤ 0.01); F. Sections of live cells expressing Lamtor1-GFP, GFP-Rheb, GFP-Lst8 or GFP-Raptor and infected with mCherry-expressing M. marinum wt for 1.5 h. White arrowheads point to the recruitment of the GFP-constructs to the MCV. Scale bars, 10 μm; G. Quantification of the percentage of cells carrying mCherry-expressing M. marinum wt or DsRed-expressing M. marinum ΔRD1 positive for Lamtor1-GFP, GFP-Rheb, GFP-Lst8 or GFP-Raptor at 1.5 and 7 hpi. Mean and standard deviation from three to six independent experiments. A minimum of 100 infected cells were counted for each cell line. Unpaired t test compared wt and ΔRD1 bacteria (*p ≤ 0.05; **p ≤ 0.01).CC BY · PubMed Central
Fig 8 Model of the D. discoideum autophagic response during M. marinum infection. Early after engulfment, M. marinum damages the membrane of its MCV in an ESX-1-dependent manner. Membrane perforations might block lysosome fusion and, consequently, autophagic flux. In addition, ESX-1 inhibits TORC1 activity early during infection (1.5 hpi), presumably through a nutrient-sensing pathway as described for other bacteria [75–77]. Downregulation of TORC1, which is always bound to the wt MCV membrane, induces the formation of autophagosomes that somehow repair the membrane damages and provide the MCV with cytoplasmic material. TORC1 re-activation at 7 hpi leads to the decrease in autophagosome formation and recruitment to the MCV, and enhances the blockade of the autophagic flux, which generates proto-lysosomal tubules (ALR). The block in autophagic flux prevents bacteria killing in autolysosomes and degradation of membranes and cytoplasmic material delivered to the MCV via the recruited autophagosomes.
Fig 8 Model of the D. discoideum autophagic response during M. marinum infection. Early after engulfment, M. marinum damages the membrane of its MCV in an ESX-1-dependent manner. Membrane perforations might block lysosome fusion and, consequently, autophagic flux. In addition, ESX-1 inhibits TORC1 activity early during infection (1.5 hpi), presumably through a nutrient-sensing pathway as described for other bacteria [75–77]. Downregulation of TORC1, which is always bound to the wt MCV membrane, induces the formation of autophagosomes that somehow repair the membrane damages and provide the MCV with cytoplasmic material. TORC1 re-activation at 7 hpi leads to the decrease in autophagosome formation and recruitment to the MCV, and enhances the blockade of the autophagic flux, which generates proto-lysosomal tubules (ALR). The block in autophagic flux prevents bacteria killing in autolysosomes and degradation of membranes and cytoplasmic material delivered to the MCV via the recruited autophagosomes.CC BY · PubMed Central

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Metadata

Authors
Cardenal-Muñoz, E., Arafah, S., López-Jiménez, A. T., Kicka, S., Falaise, A., Bach, F., Schaad, O., King, J. S., Hagedorn, M., & Soldati, T.
ORCID
Venue
PLOS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2017-04-17
Volume
13
Issue
4
Pages
e1006344
ISSN
1553-7374
DOI
10.1371/journal.ppat.1006344
PMC
PMC5407849
Cited by
84
References
8
Language
en
Update notices
new_version (2017-04-27)
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030_149390)
  • European Cooperation in Science and Technology (CA15138)

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