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Mast Cells Participate in Corneal Development in Mice

Liu, Jun, Fu, Ting, Song, Fang, Xue, Yunxia, Xia, Chaoyong, Liu, Peng, Wang, Hanqing, Zhong, Jiajun, Li, Quanrong, Chen, Jiansu, Li, Yangqiu, Cai, Dongqing, Li, Zhijie·2015·Scientific Reports
DOI 10.1038/srep17569PMC PMC4667177
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Abstract

The development of the cornea, a highly specialized transparent tissue located at the anterior of the eye, is coordinated by a variety of molecules and cells. Here, we report that mast cells (MCs), recently found to be involved in morphogenesis, played a potentially important role in corneal development in mice. We show that two different waves of MC migration occurred during corneal development. In the first wave, MCs migrated to the corneal stroma and became distributed throughout the cornea. This wave occurred by embryonic day 12.5, with MCs disappearing from the cornea at the time of eyelid opening. In the second wave, MCs migrated to the corneal limbus and became distributed around limbal blood vessels. The number of MCs in this region gradually increased after birth and peaked at the time of eyelid opening in mice, remaining stable after postnatal day 21. We also show that integrin α4β7 and CXCR2 were important for the migration of MC precursors to the corneal limbus and that c-Kit-dependent MCs appeared to be involved in the formation of limbal blood vessels and corneal nerve fibers. These data clearly revealed that MCs participate in the development of the murine cornea.

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Figure 1 Features and dynamic changes of the first wave MCs during embryonic and neonatal period. (A) This panel shows hematoxylin and eosin staining of a paraffin section taken from an E12.5 mouse eye. The eyelid is not closed at this time. Co, cornea; L, lens; R, retina; and Ch, choroid. Scale bar: 100 μm. (B) This panel contains a transmission electron microscopy image of MCs from an E14.5 mouse cornea. The cytoplasmic granules in this cell are small, heterogeneous, and less electron-dense. Scale bar: 0.5 μm. (C) This panel depicts Alcian Blue–Safranin O staining of an E14.5 mouse cornea. Only Alcian Blue-stained cells are detected. Scale bar: 100 μm. (D) This panel shows immunostaining with avidin-FITC (green) and DAPI (blue) of an eyeball section from an E12.5 mouse. Avidin-positive cells are observed among the posterior mesenchymal cells (upper-right image), and appeared to be continuous with the MCs in the presumptive choroid stroma (left image). Scale bars: lower-right image, 100 μm; upper-right and left images, 20 μm. (E) These images depict immunostaining of cornea with complete limbus with CD31 PE (red) and avidin-FITC (green) during different developmental stages from E14.5 to P13. Scale bars: 200 μm. (F) These panels show immunostaining of cornea with complete limbus from AEO mice with CD31 PE and avidin-FITC at the developmental time points indicated. Scale bars: 200 μm. (G) The number of MCs that migrate into the limbus during the embryonic stages are indicated in this graph. Across these developmental stages, limbal MC number remained relatively unchanged (n = 6 corneas per age group). (H) This graph depicts the number of MCs that migrated into the corneas of normal and AEO mice during the developmental stages indicated. The number of corneal MCs in normal mice increased from E14.5 to E20, gradually decreased after birth, and disappeared at P13. The number of corneal MCs in AEO mice disappeared at P1 (n = 6 corneas per age group). **P < 0.01.
Figure 1 Features and dynamic changes of the first wave MCs during embryonic and neonatal period. (A) This panel shows hematoxylin and eosin staining of a paraffin section taken from an E12.5 mouse eye. The eyelid is not closed at this time. Co, cornea; L, lens; R, retina; and Ch, choroid. Scale bar: 100 μm. (B) This panel contains a transmission electron microscopy image of MCs from an E14.5 mouse cornea. The cytoplasmic granules in this cell are small, heterogeneous, and less electron-dense. Scale bar: 0.5 μm. (C) This panel depicts Alcian Blue–Safranin O staining of an E14.5 mouse cornea. Only Alcian Blue-stained cells are detected. Scale bar: 100 μm. (D) This panel shows immunostaining with avidin-FITC (green) and DAPI (blue) of an eyeball section from an E12.5 mouse. Avidin-positive cells are observed among the posterior mesenchymal cells (upper-right image), and appeared to be continuous with the MCs in the presumptive choroid stroma (left image). Scale bars: lower-right image, 100 μm; upper-right and left images, 20 μm. (E) These images depict immunostaining of cornea with complete limbus with CD31 PE (red) and avidin-FITC (green) during different developmental stages from E14.5 to P13. Scale bars: 200 μm. (F) These panels show immunostaining of cornea with complete limbus from AEO mice with CD31 PE and avidin-FITC at the developmental time points indicated. Scale bars: 200 μm. (G) The number of MCs that migrate into the limbus during the embryonic stages are indicated in this graph. Across these developmental stages, limbal MC number remained relatively unchanged (n = 6 corneas per age group). (H) This graph depicts the number of MCs that migrated into the corneas of normal and AEO mice during the developmental stages indicated. The number of corneal MCs in normal mice increased from E14.5 to E20, gradually decreased after birth, and disappeared at P13. The number of corneal MCs in AEO mice disappeared at P1 (n = 6 corneas per age group). **P < 0.01.CC BY · PubMed Central
Figure 2 Dynamic changes in the second wave of MC migration and the effect of blocking antibodies. (A) These panels show the second wave of MC migration. These left images depict avidin-FITC (green) and CD31 PE (red) immunostaining of the corneal limbus from normal mice and from AEO mice at P2, P12, and P21. Scale bars: 200 μm. The graph depicts the dynamic changes of the second-wave MC in the limbus from normal and AEO mice during development (n = 6 corneas per age group). *P < 0.05; **P < 0.01. (B) These panels show the two waves of limbal and corneal MC migration in normal mice and after injection with an anti-integrin-α4β7 antibody (with isotype IgG injection as control). Immunostaining with CD31 PE (red) and avidin-FITC (green) of corneas with complete limbus from normal and anti-α4β7-treated mice are shown in the left two images. Scale bars: 400 μm. The two graphs depict the dynamic changes of the two waves of MCs distributed in the limbus and cornea, respectively, after anti-α4β7 antibody and isotype IgG injection (n = 6 corneas per age group). *P < 0.05; **P < 0.01. (C) The two waves of limbal and corneal MC migration in normal mice and after injection with an anti-CXCR2 antibody (with isotype IgG control) are shown in these panels. The left two images show immunostaining of corneas with complete limbus from normal and anti-CXCR2 treated mice. Scale bars: 400 μm. The graphs depict the dynamic changes of the two waves of MCs distributed in the limbus and cornea, respectively, after anti-CXCR2 antibody and isotype IgG injection (n = 6 corneas per age group). *P < 0.05; **P < 0.01.
Figure 2 Dynamic changes in the second wave of MC migration and the effect of blocking antibodies. (A) These panels show the second wave of MC migration. These left images depict avidin-FITC (green) and CD31 PE (red) immunostaining of the corneal limbus from normal mice and from AEO mice at P2, P12, and P21. Scale bars: 200 μm. The graph depicts the dynamic changes of the second-wave MC in the limbus from normal and AEO mice during development (n = 6 corneas per age group). *P < 0.05; **P < 0.01. (B) These panels show the two waves of limbal and corneal MC migration in normal mice and after injection with an anti-integrin-α4β7 antibody (with isotype IgG injection as control). Immunostaining with CD31 PE (red) and avidin-FITC (green) of corneas with complete limbus from normal and anti-α4β7-treated mice are shown in the left two images. Scale bars: 400 μm. The two graphs depict the dynamic changes of the two waves of MCs distributed in the limbus and cornea, respectively, after anti-α4β7 antibody and isotype IgG injection (n = 6 corneas per age group). *P < 0.05; **P < 0.01. (C) The two waves of limbal and corneal MC migration in normal mice and after injection with an anti-CXCR2 antibody (with isotype IgG control) are shown in these panels. The left two images show immunostaining of corneas with complete limbus from normal and anti-CXCR2 treated mice. Scale bars: 400 μm. The graphs depict the dynamic changes of the two waves of MCs distributed in the limbus and cornea, respectively, after anti-CXCR2 antibody and isotype IgG injection (n = 6 corneas per age group). *P < 0.05; **P < 0.01.CC BY · PubMed Central
Figure 3 Relative gene expression levels of MC migration-related factors in the corneas of embryonic and postnatal mice. The expression of the following factors was assayed by RT-PCR: MAdCAM1, CXCL1, CXCL2, CXCL3, CXCL5, VCAM1, and SCF at the developmental time points shown above. MAdCAM1, CXCL2, CXCL3, and CXCL5 were expressed at low levels or not expressed in the corneal tissue assayed. The expression of VCAM1, CXCL1, and SCF decreased after birth (n = 3 repeat experiments, each experiment: E18.5-P11, 20 corneas). The relative expression of the target genes were compared with GAPDH. *P < 0.05; **P < 0.01.
Figure 3 Relative gene expression levels of MC migration-related factors in the corneas of embryonic and postnatal mice. The expression of the following factors was assayed by RT-PCR: MAdCAM1, CXCL1, CXCL2, CXCL3, CXCL5, VCAM1, and SCF at the developmental time points shown above. MAdCAM1, CXCL2, CXCL3, and CXCL5 were expressed at low levels or not expressed in the corneal tissue assayed. The expression of VCAM1, CXCL1, and SCF decreased after birth (n = 3 repeat experiments, each experiment: E18.5-P11, 20 corneas). The relative expression of the target genes were compared with GAPDH. *P < 0.05; **P < 0.01.CC BY · PubMed Central
Figure 4 Proliferation of MCs. (A) Co-staining of corneas from E14.5 and P1 mice with anti-mouse Ki67-PE (red), avidin-FITC (green), and DAPI (blue) are depicted in these images. Avidin-positive MCs in the E14.5 mouse cornea were almost all positive for Ki67 (top three images), whereas avidin and Ki67 staining co-localized in just a few MCs in the P1 mouse cornea (bottom three images). Scale bars: 20 μm. (B) The histogram shows the percentages of Ki67-positive corneal MCs. A significantly smaller percentage of Ki67-positive MCs was detected in the P1 mouse cornea compared to the E14.5 mouse cornea (n = 6 corneas per age group). *P < 0.05. (C) Co-staining of the corneal limbi from P30 mice with anti-mouse Ki67-PE (red), avidin-FITC (green), and DAPI (blue) is shown. Some MCs were positive for both avidin and Ki67 (right, top six images), and some were undergoing mitosis (right, bottom image). Scale bars: left image, 100 μm; magnified right images, 20 μm. (D) Cell-cycle analysis of second-wave MCs by flow cytometry is shown. The top image depicts flow cytometry of cells co-stained with avidin-FITC and PI. The gate for the avidin-positive cells was identified based on the negative control group. The bottom histogram shows the percentages of second-wave limbal MCs from P1, P5, P9, and P13 mice in S/G2/M phases of the cell cycle. The percentages decreased after birth, significantly at P9 and P13 relative to P1 (n = 3 repeat experiments, each experiment: P1-13, 24 limbi). *P < 0.05.
Figure 4 Proliferation of MCs. (A) Co-staining of corneas from E14.5 and P1 mice with anti-mouse Ki67-PE (red), avidin-FITC (green), and DAPI (blue) are depicted in these images. Avidin-positive MCs in the E14.5 mouse cornea were almost all positive for Ki67 (top three images), whereas avidin and Ki67 staining co-localized in just a few MCs in the P1 mouse cornea (bottom three images). Scale bars: 20 μm. (B) The histogram shows the percentages of Ki67-positive corneal MCs. A significantly smaller percentage of Ki67-positive MCs was detected in the P1 mouse cornea compared to the E14.5 mouse cornea (n = 6 corneas per age group). *P < 0.05. (C) Co-staining of the corneal limbi from P30 mice with anti-mouse Ki67-PE (red), avidin-FITC (green), and DAPI (blue) is shown. Some MCs were positive for both avidin and Ki67 (right, top six images), and some were undergoing mitosis (right, bottom image). Scale bars: left image, 100 μm; magnified right images, 20 μm. (D) Cell-cycle analysis of second-wave MCs by flow cytometry is shown. The top image depicts flow cytometry of cells co-stained with avidin-FITC and PI. The gate for the avidin-positive cells was identified based on the negative control group. The bottom histogram shows the percentages of second-wave limbal MCs from P1, P5, P9, and P13 mice in S/G2/M phases of the cell cycle. The percentages decreased after birth, significantly at P9 and P13 relative to P1 (n = 3 repeat experiments, each experiment: P1-13, 24 limbi). *P < 0.05.CC BY · PubMed Central
Figure 5 Corneal limbal blood vessel and corneal nerve fiber development in c-KitW-sh/W-sh and WT mice. (A) The left image shows immunostaining of the limbus from a P3 mouse with avidin-FITC (green), the middle image shows staining with VEGF-PE (red), and the right image shows these two images merged, demonstrating MCs co-staining with VEGF. Scale bars: 20 μm. (B) These images depict immunostaining of corneas from P60 WT and c-KitW-sh/W-sh mutant mice with anti-CD31-FITC (green) and avidin-PE (red). The c-Kit-deficient mice (lower panel) had fewer MCs and a reduced distribution of limbal blood vessels compared to the WT mice (upper panel). Scale bars: left images, 200 μm; magnified right images, 100 μm. (C) This graph depicts the differences in limbal vessel development in c-KitW-sh/W-sh and WT mice. From P9 to P120, the limbal vascular network area in c-Kit-deficient mice was reduced compared to that in WT mice (n = 6 corneas per age group). *P < 0.05. (D) Immunostaining of a P1 mouse cornea with a complete limbus with tubulin (red, a nerve marker) and avidin-FITC (green) is depicted in these images. As shown, avidin-positive cells are distributed around nerve fibers. Scale bars: left image, 200 μm; right image, 100 μm. (E) These images show immunostaining with avidin-FITC (green) and neurturin-ALEXA FLUOR 350 (blue) of corneas from P3 mice. The merged image shows that some MCs contained neurturin. Scale bars: 20 μm. (F) Tubulin staining of a cornea with a complete limbus from a P3 WT mouse and cKit-deficient mouse is shown (top images: WT, bottom images: c-KitW-sh/W-sh). Nerve fiber density in c-KitW-sh/W-sh mice was reduced compared to WT mice. Scale bars: left images, 200 μm; right images, 100 μm. (G) The graph depicts the differences in nerve fiber density between WT and c-Kit-deficient mouse corneas. The nerve fiber density in c-KitW-sh/W-sh mouse corneas was significantly reduced compared to that in WT mice corneas at the four time points investigated (n = 6 corneas per age group). *P < 0.05, **P < 0.01.
Figure 5 Corneal limbal blood vessel and corneal nerve fiber development in c-KitW-sh/W-sh and WT mice. (A) The left image shows immunostaining of the limbus from a P3 mouse with avidin-FITC (green), the middle image shows staining with VEGF-PE (red), and the right image shows these two images merged, demonstrating MCs co-staining with VEGF. Scale bars: 20 μm. (B) These images depict immunostaining of corneas from P60 WT and c-KitW-sh/W-sh mutant mice with anti-CD31-FITC (green) and avidin-PE (red). The c-Kit-deficient mice (lower panel) had fewer MCs and a reduced distribution of limbal blood vessels compared to the WT mice (upper panel). Scale bars: left images, 200 μm; magnified right images, 100 μm. (C) This graph depicts the differences in limbal vessel development in c-KitW-sh/W-sh and WT mice. From P9 to P120, the limbal vascular network area in c-Kit-deficient mice was reduced compared to that in WT mice (n = 6 corneas per age group). *P < 0.05. (D) Immunostaining of a P1 mouse cornea with a complete limbus with tubulin (red, a nerve marker) and avidin-FITC (green) is depicted in these images. As shown, avidin-positive cells are distributed around nerve fibers. Scale bars: left image, 200 μm; right image, 100 μm. (E) These images show immunostaining with avidin-FITC (green) and neurturin-ALEXA FLUOR 350 (blue) of corneas from P3 mice. The merged image shows that some MCs contained neurturin. Scale bars: 20 μm. (F) Tubulin staining of a cornea with a complete limbus from a P3 WT mouse and cKit-deficient mouse is shown (top images: WT, bottom images: c-KitW-sh/W-sh). Nerve fiber density in c-KitW-sh/W-sh mice was reduced compared to WT mice. Scale bars: left images, 200 μm; right images, 100 μm. (G) The graph depicts the differences in nerve fiber density between WT and c-Kit-deficient mouse corneas. The nerve fiber density in c-KitW-sh/W-sh mouse corneas was significantly reduced compared to that in WT mice corneas at the four time points investigated (n = 6 corneas per age group). *P < 0.05, **P < 0.01.CC BY · PubMed Central

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Metadata

Authors
Liu, J., Fu, T., Song, F., Xue, Y., Xia, C., Liu, P., Wang, H., Zhong, J., Li, Q., Chen, J., Li, Y., Cai, D., & Li, Z.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2015-12-02
Volume
5
Issue
1
ISSN
2045-2322
DOI
10.1038/srep17569
PMC
PMC4667177
Cited by
39
References
1
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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How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Mast Cells Participate in Corneal Development in Mice. https://app.cochat.ai/papers/10.1038/srep17569
The paper
Liu, J., Fu, T., Song, F., Xue, Y., Xia, C., Liu, P., Wang, H., Zhong, J., Li, Q., Chen, J., Li, Y., Cai, D., & Li, Z. (2015). Mast Cells Participate in Corneal Development in Mice. Scientific Reports. https://doi.org/10.1038/srep17569