PROJECT PERIODIC REPORT
Grant Agreement number: PIIF-GA-2012-329741
Project acronym: 3W-RGB
Project title: Identification of whether, in which aspects and by which function, a RNA binding
protein, KH-type splicing regulatory protein governs development and function of B cell, a type of
white blood cell
Funding Scheme: Marie Curie International Incoming Fellowship
Date of latest version of Annex I against which the assessment will be made: 30/06/2015
■
Periodic report:
1st
Period covered:
from
2nd
□
3rd
01/07/2013
□
4th
□
to 30/06/2015
Name, title and organisation of the scientific representative of the project's coordinator1:
Dr. Elena Vigorito, The Babraham Institute
Tel: +44 1223 496545
Fax: N.A.
E-mail: ev250@medschl.cam.ac.uk
Project website2 address: N.A.
1
Usually the contact person of the coordinator as specified in Art. 8.1. of the Grant Agreement.
The home page of the website should contain the generic European flag and the FP7 logo which are available in electronic format
at the Europa website (logo of the European flag: http://europa.eu/abc/symbols/emblem/index_en.htm logo of the 7th
FP: http://ec.europa.eu/research/fp7/index_en.cfm?pg=logos). The area of activity of the project should also be mentioned.
2
Declaration by the scientific representative of the project coordinator
I, as scientific representative of the coordinator of this project and in line with the obligations
as stated in Article II.2.3 of the Grant Agreement declare that:

The attached periodic report represents an accurate description of the work carried out in
this project for this reporting period;

The project (tick as appropriate) 3:
■
□
has fully achieved its objectives and technical goals for the period;
has achieved most of its objectives and technical goals for the period with
relatively minor deviations.
□ has failed to achieve critical objectives and/or is not at all on schedule.

The public website, if applicable
□ is up to date
□ is not up to date

To my best knowledge, the financial statements which are being submitted as part of this
report are in line with the actual work carried out and are consistent with the report on
the resources used for the project (section 3.4) and if applicable with the certificate on
financial statement.

All beneficiaries, in particular non-profit public bodies, secondary and higher education
establishments, research organisations and SMEs, have declared to have verified their
legal status. Any changes have been reported under section 3.2.3 (Project Management)
in accordance with Article II.3.f of the Grant Agreement.
Name of scientific representative of the Coordinator: .......Elena Vigorito............................
Date: .......28...../ ......08....../ .....2015...
For most of the projects, the signature of this declaration could be done directly via the IT reporting
tool through an adapted IT mechanism and in that case, no signed paper form needs to be sent
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If either of these boxes below is ticked, the report should reflect these and any remedial actions taken.
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3.1
Publishable summary
This section must be of suitable quality to enable direct publication by the Commission and should
preferably not exceed four pages.
The production of high-affinity antibodies by B cells is essential for the clearance of pathogens. Increased
antibody affinity for antigen is achieved by the process of affinity maturation in germinal centres (GCs). This
is an iterative process in which B cells re-cycle between proliferation and the acquisition of mutations and
antigen-based positive selection of the highest-affinity B cell clones. The post-transcriptional regulator
microRNA (miR)-155 is critical for efficient affinity maturation and the maintenance of the GCs.
We first focused on the function of the miR processing protein KSRP in the regulation of B cell function via
its effect on miR-155. However we concluded that KSRP does not play a major role in GC-B cells based on
experiments using KSRP-deficient mice and therefore shifted the miR-155 itself rather than the miR-155
processing protein. The alternative project then was aimed at understanding the cellular and molecular basis
of miR-155 roles in germinal centre (GC) B cells. Here we reformulated our research objectives as follows:
a) Identify the subset of miR-155 expressing GC-B cells; b) Functionally characterise the miR-155+
subset; c) Identify underlying mechanism how miR-155 regulates GC responses.
In order to understand the cellular and molecular mechanism by which miR-155 regulates GC responses, we
utilised a miR-155 reporter mouse strain and showed that miR-155 is co-expressed with the proto-oncogene
c-Myc in positively-selected B cells. Functionally, miR-155 protects c-Myc+ positively-selected B cells from
apoptosis allowing their clonal expansion, which explains why deletion of miR-155 results in impaired
affinity maturation and the premature collapse of GCs. Molecularly, miR-155 directly inhibits the Jumonji
family member Jarid2, which we identify here as a novel component in the GC response, to promote GC-B
cell survival. Our findings also suggest a basis for cooperation between c-Myc and miR-155 during the
normal GC response, which may explain a longstanding enigma of how c-Myc and miR-155 can
collaboratively function as oncogenes.
Details in experimental approach were described in the section 3.2.2.
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3.2 Core of the report for the period: Project objectives, work progress
and achievements, project management
3.2.1 Project objectives for the period
Please provide an overview of the project objectives for the reporting period in question, as
included in Annex I to the Grant Agreement. These objectives are required so that this report is a
stand-alone document.
The aim of this project was to study the function of the microRNA (miR) processing protein KSRP in the
regulation of B cell function via its effect on miR-155. We proposed the following 3 objectives:
a) to address the function of the RNA-binding protein, KSRP, in B cell development;
b) to address the function of KSRP in antigen driven B cell responses;
c) to elucidate the regulatory mechanism of KSRP over microRNA (miR)-155.
Although we established a colony of KSRP deficient mice in the lab, detailed analyses of B cell development
and functions showed that KSRP did not play a major role in B cells. Due to this reason, we decided to
change the direction of the project slightly and focused the microRNA itself rather than the miR-155
processing protein, KSRP. Solid data proving that miR-155 has roles in activated B cells in a B cell intrinsic
manner. The alternative project then was aimed at understanding the cellular and molecular basis of miR155 roles in germinal centre (GC) B cells. Here we reformulated our research objectives as follows:
a) Identify the subset of miR-155 expressing GC-B cells;
b) Functionally characterise the miR-155+ subset;
c) Identify underlying mechanism how miR-155 regulates GC responses.
3.2.2 Work progress and achievements during the period
Please provide a concise overview of the progress of the work in line with the structure of Annex I
to the Grant Agreement.
In order to complete objective a): Identify the subset of miR-155 expressing GC-B cells, a methodology
coupling flow cytometric cell sorting with q-PCR was optimised. In detail, a mouse model system with a
targeted insertion of the Ig heavy chain V-region carrying specificity for Hen Egg Lysozyme (HEL), SWHEL
mouse (J Exp Med, 2003; 197, 845) was used to characterise antigen specific GC-B cells. These mice were
crossed with mir-155-lacZ (-galactosidase)-reporter (mir155-LacZ) mice that allow to detect transcriptional
activity of the miR-155 primary transcripts, mir-155, by measuring lacZ activity. Although lacZ activity is a
good indicator of mir-155 transcription, it may not accurately report mature miR-155 expression. This is due
to the several post-transcriptional steps involved in miR processing.
To identify the subset of GC-B cells that express mature miR-155, I sorted antigen (HEL) specific GC cells
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on the basis of expressing the reporter LacZ in combination with additional surface markers that allows
delineation of GC subsets and then measured miR-155 expression by q-PCR. GC-B cells were divided in
two zones: dark zone (DZ) containing proliferative cells and light zone (LZ) consisting of less proliferative
cells. Each of these zones was further divided on the basis of lacZ-derived fluorescence into lacZ positive
and negative cells. Thus, four subsets, lacZ- DZ, lacZ+ DZ, lacZ- LZ and lacZ+ LZ were dealt in the hereafter
experiments. I discovered that mature miR-155 is only expressed in the subset of lacZ+ LZ cells, but not
that of lacZ+ DZ. Within our knowledge, this is the first report that has defined the subset of GC-B cells
expresses miR-155.
In order to complete objective b): Functionally characterise the miR-155+ subset, HEL-specific GC-B cells
were sorted with the markers described above and their cell cycle status was analysed by staining DNAbinding fluorescent dye, DAPI. Of interest, although it has been known that LZ cells are quiescent apart
from a small subset of c-Myc+ cells (Nat Immunol, 2012: 13, 1083; Nat Immunol, 2012: 13, 1092), lacZ+ LZ
subset contained more cycling cells in the S-phase, compared to lacZ- LZ subset. Furthermore, this lacZ+ LZ
subset expressed the highest level of c-Myc transcript, which indicates that miR-155+ subset co-expresses cMyc. This is important as c-Myc+ cells are considered as positively selected population in the LZ and
proceeding to further proliferation in the DZ (Nat Immunol, 2012: 13, 1083). LacZ+ DZ subset consisted of
most proliferative cells in agreement with literature and thus contained highest proportion for S- and G2Mphases among the four subsets. GC-B cell are required to shuttle between LZ and DZ bidirectionally to
increase their affinity to antigen. Considered percentage of cells in G2M-phase between lacZ+ DZ and lacZ+
LZ, 5.0  0.82 % and 1.5  0.39 % respectively, it appeared that lacZ activity reports the direction of
migration, from LZ to DZ; LacZ+ LZ started cell division, migrated to DZ and proliferate the most by
becoming lacZ+ DZ subset. Thus the lacZ activity in the DZ appears to indicate the cells that have just
migrated from the LZ and lost the expression of miR-155. To characterise further the expression pattern of
miR-155 and c-Myc in LZ B cells, we made use of c-MycGFP reporter mice (Eur J Immunol, 2008: 38,
342). After immunisation with HEL antigen, we sorted 4 populations: c-Myc+ LZ, c-Myc- LZ, c-Myc+ DZ
and c-Myc- DZ B cells from these mice and measured the expression of miR-155 by q-PCR. We confirmed
that c-Myc+ LZ cells expressed higher levels of miR-155 and thus established that c-Myc and miR-155 are
mainly co-expressed in a subset of LZ B cells. We then assessed whether the two molecules are functionally
linked. We split GC-B cells on the basis of c-Myc expression in combination with DZ and LZ delineation.
Apoptosis was measured in miR-155-sufficient and -deficient subsets by AnnexinV staining, in combination
with DAPI. Early apoptotis was determined by detecting AnnexinV+ DAPI- cells. We observed that c-Myc+
cells are more prone to apoptosis in the absence of miR-155 particularly in the LZ whereas c-Myc- miR-155/-
cells were similar to their miR-155+/+ counterparts. To further validate these results, we also measured
apoptosis after delineating DZ and LZ B-cells on the basis of LacZ expression in the presence or absence of
miR-155. Annexin V+ population in lacZ+ LZ subset increased in the absence of miR-155 compared to an
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equivalent cohort of the control, suggesting that miR-155 is important for survival of lacZ+ LZ subset
that contains substantial population of positively selected c-Myc+ cells.
It was previously reported that miR-155 affects optimal GC selection to acquire higher affinity without
failure of somatic hyper mutation machinery (Science, 2007: 316, 604; Immunity, 2007: 27, 847). In
agreement with this, decreased affinity was observed in these HEL-specific GC-B cells. Taken together, our
results suggest that miR-155 expression is required for the survival of c-Myc+ LZ B cells and that failure of
c-Myc+ LZ B cells to receive miR-155-dependent survival signals leads to decreased GC cellularity with
concomitant impaired affinity maturation.
To achieve the final object c): Identify underlying mechanism how miR-155 regulates GC responses, we
utilised the miR-155 target list gained in the previous publication of Dr. Vigorito (Immunity, 2007: 27, 847; J
Exp Med, 2014: 211, 2183). A key miR-155 target candidate in GC responses was selected from genes that
are sufficiently meet two categories; 1) have roles in apoptosis regulations and 2) have specific expression
pattern: in the miR-155-sufficient background, decreased expression in the lacZ+ LZ subset where miR-155
is expressed, but not in the lacZ- LZ whereas no such reduction in the lacZ+ LZ subset in the miR-155deficient backgound. We successfully identified one of such miR-155 targets: Jarid2, a DNA-binding
protein and functionality of the gene in GC responses was confirmed by retroviral gene modification; ectopic
expression of Jarid2 in miR-155+/+ GC-B-cells significantly increased the percentage of LZ B-cells that
undergo apoptosis.
In summary, we uncover a dynamic regulation of miR-155, which is expressed in a small subset of LZ B
cells. The miR-155+ subset is enriched in cycling cells and co-expresses c-Myc, demonstrating that miR-155
expression is linked to positively-selected B cells. Functionally, we observed that expression of miR-155
protects c-Myc+ LZ B cells from apoptosis and thus plays a critical role in the maintenance of the GC
response and in affinity maturation. One of the molecular targets that miR-155 directly inhibits is Jarid2,
whose over-expression promotes apoptosis of LZ B cells. Overall, our results reveal a mechanism of affinity
selection by functionally linking c-Myc and miR-155.
3.2.3 Project management during the period
Please use this section to summarise management of the consortium activities during the period.
Management tasks are indicated in Articles II.2.3 and Article II.16.5 of the Grant Agreement.
Project planning and management have been carried out with regular meetings (once a week) between Dr.
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Nakagawa and Dr. Vigorito. Any raised problem in the project has been discussed in these meetings and has
been successfully solved so far. In addition, there are opportunities for discussions with Dr. Turner and
departmental colleagues regarding progress of this and others’ projects during regular lab meetings; Lab
meeting, every Tuesday at the Babraham Institute, Departmental meeting, every Monday at the Babraham
Institute. The timely change on the original project objectives had a strong impact on the advancement of the
work, which worked out excellently without any delay on the schedule. All resources and techniques needed
to perform the project are maintained in the good standard. Thus, Dr. Nakagawa’s progress of both the
project and training has been fruitful from a management point of view. Although objectives have been
changed from the originally planned ones, the planned milestones have not been impacted.
Dr. Nakagawa has been able to expand scientific network in the field successfully via attending seminars that
were organised by internal and external immunological societies, and thus started new collaborative research
with Prof. Michael Meyer-Hermann (Helmholtz centre for infection research, Germany) and Dr. Michelle
Linterman (The Babraham Institute). Hence this project has aided Dr. Nakagawa to have established a longterm research position in Europe and to provide the opportunity to study in depth how miR-155 functions in
GCs.
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3.3
Deliverables and milestones tables
Deliverables
The deliverables due in this reporting period, as indicated in Annex I to the Grant Agreement have to be uploaded by the responsible participants
(as indicated in Annex I), and then approved and submitted by the Coordinator. Deliverables are of a nature other than periodic or final reports
(ex: "prototypes", "demonstrators" or "others"). The periodic reports and the final report have NOT to be considered as deliverables. If the
deliverables are not well explained in the periodic and/or final reports, then, a short descriptive report should be submitted, so that the
Commission has a record of their existence.
If a deliverable has been cancelled or regrouped with another one, please indicate this in the column "Comments".
If a new deliverable is proposed, please indicate this in the column "Comments".
The number of persons/month for each deliverable has been defined in Annex I of the Grant Agreement and cannot be changed. In SESAM, this
number is automatically transferred from NEF and is not editable. If there is a deviation from the Annex I, then this should be clearly explained
in the comments column.
This table is cumulative, that is, it should always show all deliverables from the beginning of the project.
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TABLE 1. DELIVERABLES
Del.
no.
Deliverable name
Version
WP no.
Lead
beneficiary
Nature
Dissemination
level4
Delivery date
from Annex I
(proj month)
Actual /
Forecast
delivery
date
Dd/mm/
yyyy
4
Status
Comments
No
submitted/
Submitted
PU = Public
PP = Restricted to other programme participants (including the Commission Services).
RE = Restricted to a group specified by the consortium (including the Commission Services).
CO = Confidential, only for members of the consortium (including the Commission Services).
Make sure that you are using the correct following label when your project has classified deliverables.
EU restricted = Classified with the mention of the classification level restricted "EU Restricted"
EU confidential = Classified with the mention of the classification level confidential " EU Confidential "
EU secret = Classified with the mention of the classification level secret "EU Secret "
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Milestones
Please complete this table if milestones are specified in Annex I to the Grant Agreement.
Milestones will be assessed against the specific criteria and performance indicators as defined in
Annex I.
This table is cumulative, which means that it should always show all milestones from the beginning
of the project.
TABLE 2. MILESTONES
Milestone
no.
Milestone
name
Work
package
no
Lead
beneficiary
Delivery
date from
Annex I
dd/mm/yyyy
Achieved
Yes/No
Actual /
Forecast
achievement
date
dd/mm/yyyy
Comments
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3.4 Explanation of the use of the resources and financial statements
The financial statements have to be provided within the Forms C for each beneficiary (if Special Clause 10 applies to your Grant Agreement, a
separate financial statement is provided for each third party as well) together with a summary financial report which consolidates the claimed
Community contribution of all the beneficiaries in an aggregate form, based on the information provided in Form C (Annex VI of the Grant
Agreement) by each beneficiary.
The "Explanation of use of resources" requested in the Grant Agreement for personnel costs, subcontracting, any major costs (ex: purchase of
important equipment, travel costs, large consumable items) and indirect costs, have now to be done within the Forms (user guides are accessible
within the Participant Portal)5.
When applicable, certificates on financial statements shall be submitted by the concerned beneficiaries according to Article II.4.4 of the Grant
Agreement.
Besides the electronic submission, Forms C as well as certificates (if applicable), have to be signed and sent in parallel by post.
5
In the past, the explanation of use of resources requested in the Grant Agreement was done within a table in this section. The merge of this table within the Forms C was a
measure of simplification aimed at avoiding duplication and/or potential discrepancies between the data provided in the table 'Explanation of use of resources' and the data
provided in the Forms C.
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The following table is required only for the funding schemes for Research for the benefit of SMEs
THE TRANSACTION
Please provide a list of the actual cost incurred by the RTD performers during the performance of the work subcontracted to them. These costs
refer only to the agreed 'Transaction'.
Name of RTD
Performer
Number of
person months
Personnel
Costs (€)
Durable
equipment
Consumables
Computing
Overhead
Costs (€)
Other
Costs (€)
Total by
RTD
performer
TOTAL
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IMPORTANT:
Form C varies with the funding scheme used. Please make sure that you use the correct form
corresponding to your project (Templates for Forms C are provided in Annex VI to the Grant
Agreement). An example for collaborative projects is enclosed hereafter.
A Web-based online tool for completing and submitting forms C is accessible via the Participant
Portal: http://ec.europa.eu/research/participants/portal, (except for projects managed by DG MOVE
and ENER).
If some beneficiaries in security research have two different rates of funding (part of the funding
may reach 75% 6 ) then two separate financial statements should be filled by the concerned
beneficiaries and two lines should be entered for these beneficiaries in the summary financial
report.
6
Article 33.1 of the EC FP7 rules for participation - REGULATION (EC) No 1906/2006.
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FP7 - Grant Agreement - Annex VI - Collaborative Project
Form C - Financial Statement (to be filled in by each beneficiary )
Project nr
nnnnnn
Project Acronym
xxxxxxxxxxxxxxxxxxxxx
Period from
To
dd/mm/aa
dd/mm/aa
Funding scheme
Collaborative Project
Is this an adjustment to a previous statement ?
Legal Name
Organisation short Name
Funding % for RTD activities (A)
Yes/No
Participant Identity Code
Beneficiary nr
nn
nn
If flat rate for indirect costs, specify %
%
1- Declaration of eligible costs/lump sum/flate-rate/scale of unit (in €)
RTD
(A)
Type of Activity
Demonstration
Management
(B)
(C)
Other
(D)
TOTAL
(A+B+C+D)
Personnel costs
Subcontracting
Other direct costs
Indirect costs
Lump sums/flat-rate/scale of
unit declared
Total
Maximum EC contribution
Requested EC contribution
2- Declaration of receipts
Did you receive any financial transfers or contributions in kind, free of charge from third parties or did the project
generate any income which could be considered a receipt according to Art.II.17 of the grant agreement ?
If yes, please mention the amount (in €)
Yes/No
3- Declaration of interest yielded by the pre-financing (to be completed only by the coordinator )
Did the pre-financing you received generate any interest according to Art. II.19 ?
If yes, please mention the amount (in €)
Yes/No
4. Certificate on the methodology
Do you declare average personnel costs according to Art. II.14.1 ?
Yes/No
Is there a certificate on the methodology provided by an independent auditor and accepted by the Commission according
to Art. II.4.4 ?
Cost of the certificate (in €), if charged
Name of the auditor
under this project
5- Certificate on the financial statements
Is there a certificate on the financial statements provided by an independent auditor attached to this financial statement
according to Art.II.4.4 ?
Name of the auditor
Yes/No
Yes/No
Cost of the certificate (in €)
6- Beneficiary’s declaration on its honour
We declare on our honour that:
- the costs declared above are directly related to the resources used to attain the objectives of the project and fall within the definition of eligible
costs specified in Articles II.14 and II.15 of the grant agreement, and, if relevant, Annex III and Article 7 (special clauses) of the grant agreement;
- the receipts declared above are the only financial transfers or contributions in kind, free of charge, from third parties and the only income
generated by the project which could be considered as receipts according to Art. II.17 of the grant agreement;
- the interest declared above is the only interest yielded by the pre-financing which falls within the definition of Art. II.19 of the grant agreement ;
- there is full supporting documentation to justify the information hereby declared. It will be made available at the request of the Commission and in
the event of an audit by the Commission and/or by the Court of Auditors and/or their authorised representatives.
Beneficiary’s Stamp
Name of the Person(s) Authorised to sign this Financial Statement
Date & signature
14
FP7 - Grant Agreement - Annex VI - Collaborative Project
Form C - Financial Statement (to be filled in by Third Party ) Only applicable if special clause nr 10 is used
Project nr
nnnnnn
Project Acronym
xxxxxxxxxxxxxxxxxxxxx
Period from
To
dd/mm/aa
dd/mm/aa
Funding scheme
Collaborative Project
Is this an adjustment to a previous statement ?
3rd party legal Name
3rd party Organisation short Name
Funding % for RTD activities (A)
Yes/No
Working for beneficiary nr
nn
If flat rate for indirect costs, specify %
%
1- Declaration of eligible costs/lump sum/flate-rate/scale of unit (in €)
RTD
(A)
Type of Activity
Demonstration
Management
(B)
(C)
Other
(D)
TOTAL
(A+B+C+D)
Personnel costs
Subcontracting
Other direct costs
Indirect costs
Lump sums/flat-rate/scale of
unit declared
Total
Maximum EC contribution
Requested EC contribution
2- Declaration of receipts
Did you receive any financial transfers or contributions in kind, free of charge from third parties or did the project generate
any income which could be considered a receipt according to Art.II.17 of the grant agreement ?
If yes, please mention the amount (in €)
3- Declaration of interest yielded by the pre-financing (to be completed only by the coordinator )
Did the pre-financing you received generate any interest according to Art. II.19 ?
If yes, please mention the amount (in €)
4. Certificate on the methodology
Do you declare average personnel costs according to Art. II.14.1 ?
Yes/No
Yes/No
Is there a certificate on the methodology provided by an independent auditor and accepted by the Commission according
to Art. II.4.4 ?
Cost of the certificate (in €), if charged
Name of the auditor
under this project
5- Certificate on the financial statements
Is there a certificate on the financial statements provided by an independent auditor attached to this financial statement
according to Art.II.4.4 ?
Name of the auditor
Yes/No
Yes/No
Yes/No
Cost of the certificate (in €)
6- Beneficiary’s declaration on its honour
We declare on our honour that:
- the costs declared above are directly related to the resources used to attain the objectives of the project and fall within the definition of eligible
costs specified in Articles II.14 and II.15 of the grant agreement, and, if relevant, Annex III and Article 7 (special clauses) of the grant agreement;
- the receipts declared above are the only financial transfers or contributions in kind, free of charge, from third parties and the only income
generated by the project which could be considered as receipts according to Art. II.17 of the grant agreement;
- the interest declared above is the only interest yielded by the pre-financing which falls within the definition of Art. II.19 of the grant agreement ;
- there is full supporting documentation to justify the information hereby declared. It will be made available at the request of the Commission and in
the event of an audit by the Commission and/or by the Court of Auditors and/or their authorised representatives.
Beneficiary’s Stamp
Name of the Person(s) Authorised to sign this Financial Statement
Date & signature
15
FP7 - Grant Agreement - Annex VI - Collaborative Project
Summary Financial Report - Collaborative Project- to be filled in by the coordinator
Project acronym
Funding scheme
Beneficiar If 3rd Party, linked
y n°
to beneficiary
xxxxxxxxxxxxxxxxxxxxxxxxx
Project nr
dd/mm/aa
to:
dd/mm/aa
Page
1/1
Receipts
Interest
Type of activity
CP
Adjustment
(Yes/No)
Reporting
period from
nnnnnn
Organisation
Short Name
RTD
Total
(A)
Max EC
Contribution
Demonstration
(B)
Max EC
Total
Contribution
Management
(C)
Max EC
Total
Contribution
Other (D)
Total
Max EC
Contribution
Total
(A)+(B)+(C)+(D)
Total
Max EC
Contribution
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
TOTAL
Requested EC contribution for the reporting period (in €)
16
17