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Chymase‐producing cells of the innate immune system are required for decidual vascular remodeling and fetal growth

Meyer, Nicole, Woidacki, Katja, Knöfler, Martin, Meinhardt, Gudrun, Nowak, Désirée, Velicky, Philipp, Pollheimer, Jürgen, Zenclussen, Ana C.·2017·Scientific Reports
DOI 10.1038/srep45106PMC PMC5361184
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Abstract

Intrauterine growth restriction (IUGR) is caused by insufficient remodeling of spiral arteries (SAs). The mechanism underlying the relevance of natural killer cells (NKs) and mast cells (MCs) for SA remodeling and its effects on pregnancy outcome are not well understood. We show that NK depletion arrested SA remodeling without affecting pregnancy. MC depletion resulted in abnormally remodeled SAs and IUGR. Combined absence of NKs and MCs substantially affected SA remodeling and impaired fetal growth. We found that α-chymase mast cell protease (Mcpt) 5 mediates apoptosis of uterine smooth muscle cells, a key feature of SA remodeling. Additionally, we report a previously unknown source for Mcpt5: uterine (u) NKs. Mice with selective deletion of Mcpt5+cells had un-remodeled SAs and growth-restricted progeny. The human α-chymase CMA1, phylogenetic homolog of Mcpt5, stimulated the ex vivo migration of human trophoblasts, a pre-requisite for SA remodeling. Our results show that chymases secreted by uMCs and uNKs are pivotal to the vascular changes required to support pregnancy. Understanding the mechanisms underlying pregnancy-induced vascular changes is essential for developing therapeutic options against pregnancy complications associated with poor vascular remodeling.

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Figure 1 Anti-CD122 treatment depleted peripheral and uterine NKs in control Cpa3+/+ and MC-deficient Cpa3Cre/+ mice. The percentage of CD122+CD3−NK1.1+ pNKs in the spleen (A), blood (B) and inguinal LN (C) at gd10 was analyzed by flow cytometry in samples from PBS- or anti-CD122-treated Cpa3+/+ and Cpa3Cre/+ mice. Results are presented as medians; shown are individual values for each mouse. Statistical analysis was performed with the Mann-Whitney U test (*P < 0.05, **P < 0.001). (D) Representative DBA lectin-stained cross sections of implantations from PBS- or anti-CD122-treated Cpa3+/+ and Cpa3Cre/+ mice at gd10 are depicted (upper panels, i–iv, 10×). Magnifications of the upper panels show uNKs, which are DBA lectin-positive, brown-stained cells within the decidua basalis (lower panels, v-viii, scale bars = 100 μm). (E) Representative toluidine blue-stained cross sections of the uterus from non-pregnant Cpa3+/+ (i) and Cpa3Cre/+ (iii) mice (scale bars = 20 μm) with close-ups (ii,iv) that show uMCs (arrows) in Cpa3+/+ mice but not in Cpa3Cre/+ mice. DBA, Dolichos biflorus agglutinin; gd, gestation day; LN, lymph nodes; p, peripheral; u, uterine.
Figure 1 Anti-CD122 treatment depleted peripheral and uterine NKs in control Cpa3+/+ and MC-deficient Cpa3Cre/+ mice. The percentage of CD122+CD3−NK1.1+ pNKs in the spleen (A), blood (B) and inguinal LN (C) at gd10 was analyzed by flow cytometry in samples from PBS- or anti-CD122-treated Cpa3+/+ and Cpa3Cre/+ mice. Results are presented as medians; shown are individual values for each mouse. Statistical analysis was performed with the Mann-Whitney U test (*P < 0.05, **P < 0.001). (D) Representative DBA lectin-stained cross sections of implantations from PBS- or anti-CD122-treated Cpa3+/+ and Cpa3Cre/+ mice at gd10 are depicted (upper panels, i–iv, 10×). Magnifications of the upper panels show uNKs, which are DBA lectin-positive, brown-stained cells within the decidua basalis (lower panels, v-viii, scale bars = 100 μm). (E) Representative toluidine blue-stained cross sections of the uterus from non-pregnant Cpa3+/+ (i) and Cpa3Cre/+ (iii) mice (scale bars = 20 μm) with close-ups (ii,iv) that show uMCs (arrows) in Cpa3+/+ mice but not in Cpa3Cre/+ mice. DBA, Dolichos biflorus agglutinin; gd, gestation day; LN, lymph nodes; p, peripheral; u, uterine.CC BY · PubMed Central
Figure 2 Impaired spiral artery remodeling in uteri of NK-depleted, MC- and NK/MC-deficient mice. SA wall and lumen diameters from 3 to 10 SAs per mouse in the Cpa3+/+ + PBS (n = 9), Cpa3+/+ + anti-CD122 (n = 4), Cpa3Cre/+ + PBS (n = 8) and Cpa3Cre/+ + anti-CD122 (n = 6) groups were measured, and the wall thickness (A) and wall-to-lumen ratios (B) were calculated. Results are presented as means ± SEM. Data was analyzed by using One-way ANOVA followed by Bonferroni post-test (*P < 0.05, **P < 0.01, ***P < 0.001). (C) Representative images of SAs in gd10 implantation samples, H/E-stained (i–iv, scale bars = 50 μm) or immunofluorescent-stained for SM actin (v–viii), SM actin in combination with DAPI (ix–xii, both scale bars = 20 μm) or DAPI (rectangles). gd, gestation day; SA, spiral artery; SM, smooth muscle.
Figure 2 Impaired spiral artery remodeling in uteri of NK-depleted, MC- and NK/MC-deficient mice. SA wall and lumen diameters from 3 to 10 SAs per mouse in the Cpa3+/+ + PBS (n = 9), Cpa3+/+ + anti-CD122 (n = 4), Cpa3Cre/+ + PBS (n = 8) and Cpa3Cre/+ + anti-CD122 (n = 6) groups were measured, and the wall thickness (A) and wall-to-lumen ratios (B) were calculated. Results are presented as means ± SEM. Data was analyzed by using One-way ANOVA followed by Bonferroni post-test (*P < 0.05, **P < 0.01, ***P < 0.001). (C) Representative images of SAs in gd10 implantation samples, H/E-stained (i–iv, scale bars = 50 μm) or immunofluorescent-stained for SM actin (v–viii), SM actin in combination with DAPI (ix–xii, both scale bars = 20 μm) or DAPI (rectangles). gd, gestation day; SA, spiral artery; SM, smooth muscle.CC BY · PubMed Central
Figure 3 Gestational blood pressure and intrauterine growth in NK-depleted and MC- and NK/MC-deficient mice. Systolic (A) and diastolic (B) blood pressure of pregnant Cpa3+/+ mice treated with PBS (n = 9) or anti-CD122 (n = 5) and pregnant Cpa3Cre/+ mice treated with PBS (n = 8) or anti-CD122 (n = 4). Data were recorded every other day from gd0 to gd18. Results are presented as means ± SEM. Fetal weights (C) and the FPI (D) from the progeny of PBS- (n = 64) or anti-CD122-treated (n = 42) Cpa3+/+ females and PBS- (n = 53) or anti-CD122-treated (n = 42) Cpa3Cre/+ females at gd18. (E) Birth weights of the pups from PBS- (n = 49) or anti-CD122-treated (n = 15) Cpa3+/+ females and PBS- (n = 31) or anti-CD122-treated (n = 19) Cpa3Cre/+ females. In (C–E), results are presented as individual values for each fetus or pup and means. Statistical differences were determined using One-way ANOVA followed by Bonferroni post-test (*P < 0.05, **P < 0.01 and ***P < 0.001). (F) Percentage of fetuses (upper panel, from C) or pups (lower panel, from E) from anti-CD122-treated Cpa3+/+ and PBS- or anti-CD122-treated Cpa3Cre/+ females whose weight was below the 5th percentile (red); between the 5th and the 10th percentile (pink); or above the 10th percentile (blue). FPI, feto-placental index; gd, gestation day.
Figure 3 Gestational blood pressure and intrauterine growth in NK-depleted and MC- and NK/MC-deficient mice. Systolic (A) and diastolic (B) blood pressure of pregnant Cpa3+/+ mice treated with PBS (n = 9) or anti-CD122 (n = 5) and pregnant Cpa3Cre/+ mice treated with PBS (n = 8) or anti-CD122 (n = 4). Data were recorded every other day from gd0 to gd18. Results are presented as means ± SEM. Fetal weights (C) and the FPI (D) from the progeny of PBS- (n = 64) or anti-CD122-treated (n = 42) Cpa3+/+ females and PBS- (n = 53) or anti-CD122-treated (n = 42) Cpa3Cre/+ females at gd18. (E) Birth weights of the pups from PBS- (n = 49) or anti-CD122-treated (n = 15) Cpa3+/+ females and PBS- (n = 31) or anti-CD122-treated (n = 19) Cpa3Cre/+ females. In (C–E), results are presented as individual values for each fetus or pup and means. Statistical differences were determined using One-way ANOVA followed by Bonferroni post-test (*P < 0.05, **P < 0.01 and ***P < 0.001). (F) Percentage of fetuses (upper panel, from C) or pups (lower panel, from E) from anti-CD122-treated Cpa3+/+ and PBS- or anti-CD122-treated Cpa3Cre/+ females whose weight was below the 5th percentile (red); between the 5th and the 10th percentile (pink); or above the 10th percentile (blue). FPI, feto-placental index; gd, gestation day.CC BY · PubMed Central
Figure 4 Mcpt5 expression in uMCs and uNKs as well as uSMC apoptosis induced by MC-derived chymase in vitro. (A) Real-time RT-PCR of decidual Mcpt5 mRNA at gd10. (B) Western blot analysis (i, relative expression; ii, blot) of decidual Mcpt5 protein (27 kDa) at gd10. β-actin (42 kDa) was used as a protein loading control. For (A and B), the horizontal bars represent medians. Statistical differences were analyzed by using Kruskal Wallis followed by Dunns post test (**P < 0.01, ***P < 0.001). (C) Western blot analysis of Mcpt5 protein in MC/9 cells and PCMCs. (D) Immunofluorescence staining of uNKs (green, DBA lectin, i–ii), Mcpt5+ cells (red, DyLight™ 594, iii–iv) and nuclei (blue, DAPI, vii-viii) in implantation sections from Cpa3+/+ and Cpa3Cre/+ mice (scale bars = 20 μm). Overlay (v–viii) reveals Mcpt5 expression in DBA+ uNKs. Rectangles represent DAPI staining. (E) Flow cytometry analysis of the percentage of Annexin V+ cells following 48 h co-culture of uSMCs with MC/9 cells in the presence or absence of chymase inhibitor from Glycine max (Soybean) (STBI). Results from three independent experiments are presented as median + range. Statistical analysis was performed by using Kruskal Wallis followed by Dunns post test (*P < 0.05). gd, gestation day; PCMCs, peritoneal cavity mast cells; uSMCs, uterine smooth muscle cells.
Figure 4 Mcpt5 expression in uMCs and uNKs as well as uSMC apoptosis induced by MC-derived chymase in vitro. (A) Real-time RT-PCR of decidual Mcpt5 mRNA at gd10. (B) Western blot analysis (i, relative expression; ii, blot) of decidual Mcpt5 protein (27 kDa) at gd10. β-actin (42 kDa) was used as a protein loading control. For (A and B), the horizontal bars represent medians. Statistical differences were analyzed by using Kruskal Wallis followed by Dunns post test (**P < 0.01, ***P < 0.001). (C) Western blot analysis of Mcpt5 protein in MC/9 cells and PCMCs. (D) Immunofluorescence staining of uNKs (green, DBA lectin, i–ii), Mcpt5+ cells (red, DyLight™ 594, iii–iv) and nuclei (blue, DAPI, vii-viii) in implantation sections from Cpa3+/+ and Cpa3Cre/+ mice (scale bars = 20 μm). Overlay (v–viii) reveals Mcpt5 expression in DBA+ uNKs. Rectangles represent DAPI staining. (E) Flow cytometry analysis of the percentage of Annexin V+ cells following 48 h co-culture of uSMCs with MC/9 cells in the presence or absence of chymase inhibitor from Glycine max (Soybean) (STBI). Results from three independent experiments are presented as median + range. Statistical analysis was performed by using Kruskal Wallis followed by Dunns post test (*P < 0.05). gd, gestation day; PCMCs, peritoneal cavity mast cells; uSMCs, uterine smooth muscle cells.CC BY · PubMed Central
Figure 5 Impaired uterine spiral artery remodeling and fetal growth restriction in Mcpt5-deficient pregnant mice. SA wall and lumen diameters from 3 to 10 SAs in Mcpt5-Cre− R-DTA+ control mice (n = 6) or Mcpt5-Cre+ R-DTA+ mice (n = 7) were measured. Based on the mean value obtained for each mouse, the means for the group were calculated and expressed as wall thickness (A) and the wall-to-lumen ratio (B). Statistical differences were analyzed with the Mann-Whitney test (**P < 0.01). (C) Representative images of H/E-stained uterine sections from control (i) and Mcpt5-Cre+ R-DTA+ Mcpt5-deficient mice (ii, scale bars = 50 μm). (D) Birth weights of pups born to pregnant female controls (n = 66) or Mcpt5-Cre+ R-DTA+ mice (n = 38). Individual mice are depicted, with means. Statistical analysis was performed using the unpaired t test (***P < 0.001). (E) Pup weights from the Mcpt5-Cre− R-DTA+ mice were classified as above the 10th percentile (blue) or growth restricted (red, below the 5th percentile; pink, between the 5th and the 10th percentile). Pups from wild type Mcpt5-Cre+ R-DTA+ females served as the basis for calculating the percentiles. SA, spiral artery.
Figure 5 Impaired uterine spiral artery remodeling and fetal growth restriction in Mcpt5-deficient pregnant mice. SA wall and lumen diameters from 3 to 10 SAs in Mcpt5-Cre− R-DTA+ control mice (n = 6) or Mcpt5-Cre+ R-DTA+ mice (n = 7) were measured. Based on the mean value obtained for each mouse, the means for the group were calculated and expressed as wall thickness (A) and the wall-to-lumen ratio (B). Statistical differences were analyzed with the Mann-Whitney test (**P < 0.01). (C) Representative images of H/E-stained uterine sections from control (i) and Mcpt5-Cre+ R-DTA+ Mcpt5-deficient mice (ii, scale bars = 50 μm). (D) Birth weights of pups born to pregnant female controls (n = 66) or Mcpt5-Cre+ R-DTA+ mice (n = 38). Individual mice are depicted, with means. Statistical analysis was performed using the unpaired t test (***P < 0.001). (E) Pup weights from the Mcpt5-Cre− R-DTA+ mice were classified as above the 10th percentile (blue) or growth restricted (red, below the 5th percentile; pink, between the 5th and the 10th percentile). Pups from wild type Mcpt5-Cre+ R-DTA+ females served as the basis for calculating the percentiles. SA, spiral artery.CC BY · PubMed Central
Figure 6 uMCs localize near invading trophoblasts in human first-trimester decidual tissue and MC-conditioned medium and human CMA1 increase the migration of extravillous trophoblasts in vitro. (A) Images depicting the close localization of uMCs and EVTs in first-trimester decidual tissue obtained from elective, legal pregnancy terminations. uMCs were stained for TPSAB1 (i), c-Kit (ii) or CMA1 (iii), and decidual EVTs were identified as pan KRT- (i) or HLA-G-positive (ii,iii) cells (scale bars = 50 μm). (B) Western blot analysis of CMA1 (27 kDa) in lysates from human HMC-1 MCs. β-actin (42 kDa) was used as a loading control. (C) Representative microscopic images of placental first-trimester villous explants cultured in the presence of control medium (i, CTRL), HMC-1-conditioned medium (ii, HMC-1 SN) or rhu CMA1 (iii) (scale bars = 100 μm). (D) The distance migrated by EVTs shown in C was calculated. Results are presented as means ± SEM. Statistical analysis was performed with two-way ANOVA followed by Sidak’s post-hoc correction (**P < 0.01, ***P < 0.001). EVTs, extravillous trophoblasts; rhu, recombinant human; u, uterine.
Figure 6 uMCs localize near invading trophoblasts in human first-trimester decidual tissue and MC-conditioned medium and human CMA1 increase the migration of extravillous trophoblasts in vitro. (A) Images depicting the close localization of uMCs and EVTs in first-trimester decidual tissue obtained from elective, legal pregnancy terminations. uMCs were stained for TPSAB1 (i), c-Kit (ii) or CMA1 (iii), and decidual EVTs were identified as pan KRT- (i) or HLA-G-positive (ii,iii) cells (scale bars = 50 μm). (B) Western blot analysis of CMA1 (27 kDa) in lysates from human HMC-1 MCs. β-actin (42 kDa) was used as a loading control. (C) Representative microscopic images of placental first-trimester villous explants cultured in the presence of control medium (i, CTRL), HMC-1-conditioned medium (ii, HMC-1 SN) or rhu CMA1 (iii) (scale bars = 100 μm). (D) The distance migrated by EVTs shown in C was calculated. Results are presented as means ± SEM. Statistical analysis was performed with two-way ANOVA followed by Sidak’s post-hoc correction (**P < 0.01, ***P < 0.001). EVTs, extravillous trophoblasts; rhu, recombinant human; u, uterine.CC BY · PubMed Central

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Cited by

Sorted by citations

Metadata

Authors
Meyer, N., Woidacki, K., Knöfler, M., Meinhardt, G., Nowak, D., Velicky, P., Pollheimer, J., & Zenclussen, A. C.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2017-03-22
Volume
7
Issue
1
ISSN
2045-2322
DOI
10.1038/srep45106
PMC
PMC5361184
Cited by
62
References
3
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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