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Research Article
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Fms-like tyrosine kinase 3 is a regulator of the cardiac side population in mice

View ORCID ProfileGiacomo Della Verde, Michika Mochizuki, Vera Lorenz, View ORCID ProfileJulien Roux, Lifen Xu, View ORCID ProfileLeandra Ramin-Wright, Otmar Pfister, View ORCID ProfileGabriela M Kuster  Correspondence email
Giacomo Della Verde
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
Roles: Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, review, and editing
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  • ORCID record for Giacomo Della Verde
Michika Mochizuki
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
Roles: Conceptualization, Formal analysis, Validation, Investigation, Methodology, Writing—review and editing
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Vera Lorenz
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
Roles: Data curation, Formal analysis, Investigation, Visualization, Methodology, Project administration, Writing—review and editing
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Julien Roux
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
2Swiss Institute of Bioinformatics, Basel, Switzerland
Roles: Resources, Data curation, Software, Formal analysis, Validation, Methodology, Writing—review and editing
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  • ORCID record for Julien Roux
Lifen Xu
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
Roles: Data curation, Formal analysis, Investigation, Visualization, Writing—review and editing
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Leandra Ramin-Wright
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
Roles: Investigation, Writing—review and editing
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  • ORCID record for Leandra Ramin-Wright
Otmar Pfister
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
3Department of Cardiology, University Hospital Basel, Basel, Switzerland
Roles: Conceptualization, Supervision, Funding acquisition, Validation, Methodology, Writing—original draft, review, and editing
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Gabriela M Kuster
1Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
3Department of Cardiology, University Hospital Basel, Basel, Switzerland
Roles: Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Visualization, Methodology, Writing—original draft, review, and editing
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  • ORCID record for Gabriela M Kuster
  • For correspondence: Gabriela.Kuster@usb.ch
Published 13 December 2021. DOI: 10.26508/lsa.202101112
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  • Figure 1.
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    Figure 1. Flt3L−/− hearts show a lower abundance and differences in the composition of the cardiac side population.

    (A) Percentages of cardiac side population (CSP) cells in the cardiomyocyte (CMC)- and erythrocyte-depleted cell population. Verapamil is used as negative control. The red rectangle depicts the tip third of the CSP. Wild type (wt) versus flt3L−/−, n = 11; unpaired t test. Representative flow cytometry readouts are shown. (B) Pyronin Y-low cells in the CSP. wt versus flt3L−/−, n = 3; unpaired t test, P = 0.46. Representative flow cytometry readouts are shown. (C) Sca1+/CD31− fraction in the CSP. wt versus flt3L−/−, n = 7; unpaired t test, P = 0.21. Representative flow cytometry readouts are shown. (D) CD34+ fraction in the CSP. wt versus flt3L−/−, n = 9 and 7; unpaired t test. Representative flow cytometry readouts are shown. Data are mean ± SEM. Each n consists of a pool of four mice.

  • Figure S1.
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    Figure S1.

    Gating strategies for cardiac side population (SP) and pyronin Y. (A) Cardiac SP gating from digested heart suspension from four mice. (B) Pyronin Y-low SP-CPC gating from digested heart suspension.

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    Figure 2. Differences in in vitro behavior unveil a shift in the proliferation-differentiation balance of flt3L−/− side population (SP)-CPCs.

    (A) Flt3L quantification in supernatant from cultured wt and flt3L−/− Sca1+/CD31− SP-CPCs after 48 h in EM2 measured by ELISA. N = 5 and 6, unpaired t test. (B) Recombinant Flt3L-inducible signaling in wt SP-CPCs in EM1. N = 4, Kruskal–Wallis test, followed by Dunn’s multiple comparison test. Representative blots are shown. (Ci) Sca1+/CD31− SP-CPC proliferation curve in EM1, wt versus flt3L−/−, n = 3, unpaired t test at final timepoint. (ii) SP-CPC proliferation curve in EM2, wt versus flt3L−/−, n = 5 and 6; unpaired t test at final timepoint, P = 0.59. Starting cell number = 1 × 104. (Di) Calponin protein expression in EM2, wt versus flt3L−/−, n = 5 and 6; unpaired t test. (ii) Calponin protein expression in smooth muscle differentiation medium (SMD) at day 7, wt versus flt3L−/−, n = 5 and 6; unpaired t test, P = 0.24. Representative blots are shown. (Ei) Expression of phosphorylated Akt (p-Akt) in EM1, wt versus flt3L−/−, n = 3; Mann–Whitney U test, P = 0.1. (ii) p-Akt expression in EM2, wt versus flt3L−/−, n = 5 and 6; unpaired t test, P = 0.50. (iii) p-Akt expression in SMD at day 7, wt versus flt3L−/−, n = 5 and 6; unpaired t test, P = 0.08. Representative blots are shown. (F) Calponin protein expression in wt SP-CPCs in SMD at day 7, after treatment with vehicle or 2 μM Akt inhibitor, vehicle versus treated, n = 4; ratio paired t test. Representative blots are shown. All data are mean ± SEM.

  • Figure 3.
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    Figure 3. The lower vasculogenic potential of flt3L−/− side population (SP)-CPCs reflects in a decreased microvascular density and function of flt3L−/− hearts.

    (A) Differences in endothelial marker gene expression in EM1 (black bars) and EGM2 (blue bars) versus wt EM1, n = 3, unpaired t test. (B) Freshly isolated wt and flt3L−/− SP-CPCs were cultured in EGM2 for 3 wk and vWF-positive cells were quantified, n = 6, unpaired t test, P = 0.52. Representative pictures are shown: vWF (red), nuclei (blue). (C) Analysis of capillaries per myocyte in the left ventricular myocardium of wt versus flt3L−/− hearts, n = 9 and 10, unpaired t test. Representative pictures are shown: IB4 (red), WGA (green). (D) Left ventricular ejection fraction (LVEF) in 12-wk-old wt and flt3L−/− mice, n = 16 and 18, Mann–Whitney U test. All data are given as mean ± SEM. (E) Proposed model of Flt3 regulation of SP-CPCs.

Supplementary Materials

  • Figures
  • Table S1 Single gene analysis.

  • Table S2 Gene set enrichment analysis.

  • Table S3 Gene set enrichment analysis.

  • Table S4 Gene set enrichment analysis.

  • Table S5 List of antibodies and markers used for flow cytometry, Western blotting, and immunocyto- and -histochemistry.

  • Table S6 List of compounds and compositions of culture media.

  • Table S7 List of primers.

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Flt3 regulates cardiac progenitors
Giacomo Della Verde, Michika Mochizuki, Vera Lorenz, Julien Roux, Lifen Xu, Leandra Ramin-Wright, Otmar Pfister, Gabriela M Kuster
Life Science Alliance Dec 2021, 5 (3) e202101112; DOI: 10.26508/lsa.202101112

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Flt3 regulates cardiac progenitors
Giacomo Della Verde, Michika Mochizuki, Vera Lorenz, Julien Roux, Lifen Xu, Leandra Ramin-Wright, Otmar Pfister, Gabriela M Kuster
Life Science Alliance Dec 2021, 5 (3) e202101112; DOI: 10.26508/lsa.202101112
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Volume 5, No. 3
March 2022
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