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Cited by 224Glaucoma and retinal disordersNeuroinflammation and Neurodegeneration MechanismsRetinal Diseases and Treatments

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IOP induces upregulation of GFAP and MHC-II and microglia reactivity in mice retina contralateral to experimental glaucoma

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Gallego, Beatriz I, Salazar, Juan J, de Hoz, Rosa, Rojas, Blanca, Ramírez, Ana I, Salinas-Navarro, Manuel, Ortín-Martínez, Arturo, Valiente-Soriano, Francisco J, Avilés-Trigueros, Marcelino, Villegas-Perez, Maria P, Vidal-Sanz, Manuel, Triviño, Alberto, Ramírez, Jose M·2012·Journal of Neuroinflammation
DOI 10.1186/1742-2094-9-92PMC PMC3410794
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Abstract

BACKGROUND: Ocular hypertension is a major risk factor for glaucoma, a neurodegenerative disease characterized by an irreversible decrease in ganglion cells and their axons. Macroglial and microglial cells appear to play an important role in the pathogenic mechanisms of the disease. Here, we study the effects of laser-induced ocular hypertension (OHT) in the macroglia, microglia and retinal ganglion cells (RGCs) of eyes with OHT (OHT-eyes) and contralateral eyes two weeks after lasering. METHODS: Two groups of adult Swiss mice were used: age-matched control (naïve, n=9); and lasered (n=9). In the lasered animals, both OHT-eyes and contralateral eyes were analyzed. Retinal whole-mounts were immunostained with antibodies against glial fibrillary acid protein (GFAP), neurofilament of 200 kD (NF-200), ionized calcium binding adaptor molecule (Iba-1) and major histocompatibility complex class II molecule (MHC-II). The GFAP-labeled retinal area (GFAP-RA), the intensity of GFAP immunoreaction (GFAP-IR), and the number of astrocytes and NF-200 + RGCs were quantified. RESULTS: In comparison with naïve: i) astrocytes were more robust in contralateral eyes. In OHT-eyes, the astrocyte population was not homogeneous, given that astrocytes displaying only primary processes coexisted with astrocytes in which primary and secondary processes could be recognized, the former having less intense GFAP-IR (P<0.001); ii) GFAP-RA was increased in contralateral (P<.05) and decreased in OHT-eyes (P <0.001); iii) the mean intensity of GFAP-IR was higher in OHT-eyes (P<0.01), and the percentage of the retinal area occupied by GFAP+ cells with higher intensity levels was increased in contralateral (P=0.05) and in OHT-eyes (P<0.01); iv) both in contralateral and in OHT-eyes, GFAP was upregulated in Müller cells and microglia was activated; v) MHC-II was upregulated on macroglia and microglia. In microglia, it was similarly expressed in contralateral and OHT-eyes. By contrast, in macroglia, MHC-II upregulation was observed mainly in astrocytes in contralateral eyes and in Müller cells in OHT-eyes; vi) NF-200+ RGCs (degenerated cells) appeared in OHT-eyes with a trend for the GFAP-RA to decrease and for the NF-200+RGC number to increase from the center to the periphery (r= -0.45). CONCLUSION: The use of the contralateral eye as an internal control in experimental induction of unilateral IOP should be reconsidered. The gliotic behavior in contralateral eyes could be related to the immune response. The absence of NF-200+RGCs (sign of RGC degeneration) leads us to postulate that the MHC-II upregulation in contralateral eyes could favor neuroprotection.

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Figures

Figure 1 Retinal whole-mount. GFAP-labeled retinal area (GFAP-RA) and NF-200+RGC counting. A: division of the retina in concentric zones for study and areas of retina selected from each zone; B: photomicrograph illustrating the astrocyte-counting methodology, GFAP+ astrocytes (in green) and DAPI, a nuclear marker (in red); C: photomicrograph of one of the areas of the retina selected for GFAP-RA quantification; D: same area shown in C processed with the threshold tool included in the Metamorph Imaging System. In red, GFAP-labeled retina included in the measurements and processing; E: double immunostaining photographs used to correlate the effect of OHT in both GFAP+ astrocytes (in green) and NF-200+RGCs (in red); F: same area shown in E used for manual counting of NF-200+RGCs. Fluorescence microscopy (B,C,D); Confocal microscopy (E,F). GFAP, glial fibrillary acidic protein; NF-200, 200 kD neurofilament; OHT, ocular hypertension; RGCs, retinal ganglion cells.
Figure 1 Retinal whole-mount. GFAP-labeled retinal area (GFAP-RA) and NF-200+RGC counting. A: division of the retina in concentric zones for study and areas of retina selected from each zone; B: photomicrograph illustrating the astrocyte-counting methodology, GFAP+ astrocytes (in green) and DAPI, a nuclear marker (in red); C: photomicrograph of one of the areas of the retina selected for GFAP-RA quantification; D: same area shown in C processed with the threshold tool included in the Metamorph Imaging System. In red, GFAP-labeled retina included in the measurements and processing; E: double immunostaining photographs used to correlate the effect of OHT in both GFAP+ astrocytes (in green) and NF-200+RGCs (in red); F: same area shown in E used for manual counting of NF-200+RGCs. Fluorescence microscopy (B,C,D); Confocal microscopy (E,F). GFAP, glial fibrillary acidic protein; NF-200, 200 kD neurofilament; OHT, ocular hypertension; RGCs, retinal ganglion cells.CC BY · PubMed Central
Figure 2 Intensity of GFAP immunoreaction. Pseudocolor-intensity maps drawn with MATLAB program. All maps had the same preset color scale that assigned a color to each intensity value, identifying different intensity levels of the GFAP-IR (Müller cells plus astrocytes). Cool colors represent lower intensity levels while warm colors represent higher intensity levels. Although no differences in mean intensity of GFAP-IR were found between naïve (A) and contralateral (B) eyes, differences were found when the comparison was made by the percentage of the retinal area occupied by GFAP+ cells with higher intensity levels. C-D microphotographs were taken from the same retina. They illustrate that OHT-eyes had retinal areas with high (C) and low (D) intensity of GFAP-IR, the later having mainly astrocytes in which only primary processes were detected. GFAP-IR, glial fibrillary acidic protein immunoreaction; OHT, ocular hypertension.
Figure 2 Intensity of GFAP immunoreaction. Pseudocolor-intensity maps drawn with MATLAB program. All maps had the same preset color scale that assigned a color to each intensity value, identifying different intensity levels of the GFAP-IR (Müller cells plus astrocytes). Cool colors represent lower intensity levels while warm colors represent higher intensity levels. Although no differences in mean intensity of GFAP-IR were found between naïve (A) and contralateral (B) eyes, differences were found when the comparison was made by the percentage of the retinal area occupied by GFAP+ cells with higher intensity levels. C-D microphotographs were taken from the same retina. They illustrate that OHT-eyes had retinal areas with high (C) and low (D) intensity of GFAP-IR, the later having mainly astrocytes in which only primary processes were detected. GFAP-IR, glial fibrillary acidic protein immunoreaction; OHT, ocular hypertension.CC BY · PubMed Central
Figure 3 GFAP immunostaining of equivalent areas of the retinal whole-mounts. Astrocyte morphology and GFAP-IR of macroglial cells in naïve and in contralateral and OHT-eyes after 15 days of laser-induced OHT. A-C: overview of the retinal astrocytes around the optic disc in naïve (A), contralateral (B), and OHT-eyes (C). D-L: images correspond to zone 1 of study. In naïve eyes (A, D, G, J), astrocytes formed a homogeneous plexus on the nerve-fiber-RGC layer of cells regularly distributed throughout the retina. This plexus was constituted by stellate cells that could easily be distinguished from each other (D, G). Astrocytes had a rounded body from which numerous primary and secondary processes extended (J) and Müller cells (arrowhead) exhibited punctate GFAP+ structures between the astrocytes (D, G). In contralateral eyes (B, E, H, K), astrocytes were more robust (K) than in naïve eyes (J) and formed a honeycomb network (E, H, K). GFAP+ Müller cells were observed in some retinal areas (arrowhead) in (E, H). Astrocyte morphology in OHT-eyes (C, F, I, L) was not uniform, with astrocytes in which primary and secondary processes could be observed (empty arrow) in (I) and astrocytes in which only primary processes could be observed (arrow) in (I and L). GFAP+ Müller cells (C, F, I) were visible throughout the retina (arrowhead) in (I). Confocal microscopy (A-I); Fluorescence microscopy (J-L). GFAP-IR, glial fibrillary acidic protein immunoreaction; OHT, ocular hypertension; RGC, retinal ganglion cells.
Figure 3 GFAP immunostaining of equivalent areas of the retinal whole-mounts. Astrocyte morphology and GFAP-IR of macroglial cells in naïve and in contralateral and OHT-eyes after 15 days of laser-induced OHT. A-C: overview of the retinal astrocytes around the optic disc in naïve (A), contralateral (B), and OHT-eyes (C). D-L: images correspond to zone 1 of study. In naïve eyes (A, D, G, J), astrocytes formed a homogeneous plexus on the nerve-fiber-RGC layer of cells regularly distributed throughout the retina. This plexus was constituted by stellate cells that could easily be distinguished from each other (D, G). Astrocytes had a rounded body from which numerous primary and secondary processes extended (J) and Müller cells (arrowhead) exhibited punctate GFAP+ structures between the astrocytes (D, G). In contralateral eyes (B, E, H, K), astrocytes were more robust (K) than in naïve eyes (J) and formed a honeycomb network (E, H, K). GFAP+ Müller cells were observed in some retinal areas (arrowhead) in (E, H). Astrocyte morphology in OHT-eyes (C, F, I, L) was not uniform, with astrocytes in which primary and secondary processes could be observed (empty arrow) in (I) and astrocytes in which only primary processes could be observed (arrow) in (I and L). GFAP+ Müller cells (C, F, I) were visible throughout the retina (arrowhead) in (I). Confocal microscopy (A-I); Fluorescence microscopy (J-L). GFAP-IR, glial fibrillary acidic protein immunoreaction; OHT, ocular hypertension; RGC, retinal ganglion cells.CC BY · PubMed Central
Figure 4 GFAP-labeled retinal area (GFAP-RA) after 15 days of laser-induced OHT. Comparison among areas and concentric zones of the retina analyzed in the three study groups. The GFAP-RA of the OHT-eyes underwent a statistically significant reduction in comparison with naïve and contralateral eyes. This finding was observed when the analysis was made both by retinal areas (13 target areas per retina) (A) and by concentric zones of the retina (disc, central, intermediate, and periphery) (B). Each bar represents the mean ± SD of GFAP-RA. ***P < 0.001 versus naïve and contralateral retinas. ANOVA with Bonferroni test. ANOVA, analysis of variance; GFAP, glial fibrillary acidic protein; OHT, ocular hypertension.
Figure 4 GFAP-labeled retinal area (GFAP-RA) after 15 days of laser-induced OHT. Comparison among areas and concentric zones of the retina analyzed in the three study groups. The GFAP-RA of the OHT-eyes underwent a statistically significant reduction in comparison with naïve and contralateral eyes. This finding was observed when the analysis was made both by retinal areas (13 target areas per retina) (A) and by concentric zones of the retina (disc, central, intermediate, and periphery) (B). Each bar represents the mean ± SD of GFAP-RA. ***P < 0.001 versus naïve and contralateral retinas. ANOVA with Bonferroni test. ANOVA, analysis of variance; GFAP, glial fibrillary acidic protein; OHT, ocular hypertension.CC BY · PubMed Central
Figure 5 Retinal whole-mount. Double immunostaining for NF-200 and GFAP after 15 days of laser-induced OHT. Axon and RGCs (in red). Macroglia (in green). A-C: Images correspond to area 1 of study. D: image corresponds to area 3 of the study. A-B: NF-200 labelling of RGC axons was rectilinear and uniform in naïve (A) and contralateral eyes (B). NF-200+RGC somas were infrequently observed; C-D: beads on a string-like immunostaining (arrowhead) and small varicosities (yellow arrow) in NF-200+ axons in OHT-eyes. Abnormal staining of cell bodies and primary dendrites of RGCs (white arrow) were more frequently found in OHT-eyes (D) than in naïve and contralateral eyes. Confocal microscopy. GFAP, glial fibrillary acidic protein; OHT, ocular hypertension; RGCs, retinal ganglion cells.
Figure 5 Retinal whole-mount. Double immunostaining for NF-200 and GFAP after 15 days of laser-induced OHT. Axon and RGCs (in red). Macroglia (in green). A-C: Images correspond to area 1 of study. D: image corresponds to area 3 of the study. A-B: NF-200 labelling of RGC axons was rectilinear and uniform in naïve (A) and contralateral eyes (B). NF-200+RGC somas were infrequently observed; C-D: beads on a string-like immunostaining (arrowhead) and small varicosities (yellow arrow) in NF-200+ axons in OHT-eyes. Abnormal staining of cell bodies and primary dendrites of RGCs (white arrow) were more frequently found in OHT-eyes (D) than in naïve and contralateral eyes. Confocal microscopy. GFAP, glial fibrillary acidic protein; OHT, ocular hypertension; RGCs, retinal ganglion cells.CC BY · PubMed Central
Figure 6 Correlation of GFAP-labeled retinal area (GFAP-RA) versus NF-200+RGC number in OHT-eyes after 15 days of laser-induced OHT. There was a trend for the GFAP-RA to decrease and for the NF-200+RGC number to increase from the disc to the periphery in OHT-eyes. Data regarding GFAP-RA are the same as in Figure 3. OHT, ocular hypertension; RGCs, retinal ganglion cells.
Figure 6 Correlation of GFAP-labeled retinal area (GFAP-RA) versus NF-200+RGC number in OHT-eyes after 15 days of laser-induced OHT. There was a trend for the GFAP-RA to decrease and for the NF-200+RGC number to increase from the disc to the periphery in OHT-eyes. Data regarding GFAP-RA are the same as in Figure 3. OHT, ocular hypertension; RGCs, retinal ganglion cells.CC BY · PubMed Central
Figure 7 Iba-1+ cells in the retinal whole-mounts after 15 days of laser-induced OHT. The density of Iba-1+ network was increased in contralateral (B) and OHT-eyes (C) with respect to naïve (A). Higher magnification of equivalent fields in the retinas correspond to area 2 (insets). A-C: 5x; Insets: 10x. Fluorescence microscopy. Iba-1, ionized calcium binding adaptor molecule 1; OHT, ocular hypertension.
Figure 7 Iba-1+ cells in the retinal whole-mounts after 15 days of laser-induced OHT. The density of Iba-1+ network was increased in contralateral (B) and OHT-eyes (C) with respect to naïve (A). Higher magnification of equivalent fields in the retinas correspond to area 2 (insets). A-C: 5x; Insets: 10x. Fluorescence microscopy. Iba-1, ionized calcium binding adaptor molecule 1; OHT, ocular hypertension.CC BY · PubMed Central
Figure 8 MHC-II expression of Iba-1+ cells in retinal whole-mounts after 15 days of laser-induced OHT. Double immunofluorescence staining for Iba-1 (in red) and MHC-II (in green). A-C: in naïve retinas, a constitutive weak expression of MHC-II (arrowheads) was observed in some Iba-1+ cells throughout the retina (B). However, some Iba-1+ cells located in the juxtapapillary area and in the far periphery (A, inset) had a strong constitutive expression of MHC-II (B, inset). E-H: in contralateral eyes, Iba-1+ microglial cells of the retina had morphological changes (H) and showed a stronger expression of MHC-II immunoreaction throughout the retina (F,G) in comparison with naïve (B-D). I-L: Iba-1+ cell in OHT-eyes had a similar up-regulation of MHC-II (J-K) as did contralateral eyes (F-G); however, the cell bodies were larger and the processes thicker and more retracted (L) than in the contralateral (H) retinas. Fluorescence microscopy and image acquisition using the ApoTome. Iba-1, ionized calcium binding adaptor molecule 1; MHC, major histocompatibility complex; OHT, ocular hypertension.
Figure 8 MHC-II expression of Iba-1+ cells in retinal whole-mounts after 15 days of laser-induced OHT. Double immunofluorescence staining for Iba-1 (in red) and MHC-II (in green). A-C: in naïve retinas, a constitutive weak expression of MHC-II (arrowheads) was observed in some Iba-1+ cells throughout the retina (B). However, some Iba-1+ cells located in the juxtapapillary area and in the far periphery (A, inset) had a strong constitutive expression of MHC-II (B, inset). E-H: in contralateral eyes, Iba-1+ microglial cells of the retina had morphological changes (H) and showed a stronger expression of MHC-II immunoreaction throughout the retina (F,G) in comparison with naïve (B-D). I-L: Iba-1+ cell in OHT-eyes had a similar up-regulation of MHC-II (J-K) as did contralateral eyes (F-G); however, the cell bodies were larger and the processes thicker and more retracted (L) than in the contralateral (H) retinas. Fluorescence microscopy and image acquisition using the ApoTome. Iba-1, ionized calcium binding adaptor molecule 1; MHC, major histocompatibility complex; OHT, ocular hypertension.CC BY · PubMed Central
Figure 9 Retinal whole-mount. Double immunostaining for GFAP (red) and MHC-II (in green) after 15 days of laser-induced OHT. A-C: naïve eyes; D-F: contralateral eyes; G-I: OHT-eyes. In contralateral eyes MHC-II immunoreaction of astrocytes (arrow) and Müller cells (arrowhead) in (E) was increased with respect to naïve eyes (arrow) in (B). In OHT-eyes, MHC-II immunoreaction of Müller cells (arrowhead) in (H) was notably upregulated in comparison with contralateral (E). Fluorescence microscopy and image acquisition using the ApoTome. GFAP, glial fibrillary acidic protein; MHC, major histocompatibility complex; OHT, ocular hypertension.
Figure 9 Retinal whole-mount. Double immunostaining for GFAP (red) and MHC-II (in green) after 15 days of laser-induced OHT. A-C: naïve eyes; D-F: contralateral eyes; G-I: OHT-eyes. In contralateral eyes MHC-II immunoreaction of astrocytes (arrow) and Müller cells (arrowhead) in (E) was increased with respect to naïve eyes (arrow) in (B). In OHT-eyes, MHC-II immunoreaction of Müller cells (arrowhead) in (H) was notably upregulated in comparison with contralateral (E). Fluorescence microscopy and image acquisition using the ApoTome. GFAP, glial fibrillary acidic protein; MHC, major histocompatibility complex; OHT, ocular hypertension.CC BY · PubMed Central
Figure 10 Retinal whole-mount. Double immunostaining for GFAP (in red) and MHC-II (in green) after 15 days of laser-induced OHT. The pressure exerted by the cover glass on the retinal whole-mount, produced a retinal-like section effect in some retinal borders. A-C: in contralateral eyes (A), the GFAP immunoreaction (IR) of Müller cells was weaker than in OHT-eyes (D). MHC-II expression was greater in astrocytes (arrow) than in Müller cells (arrowhead) in (B); D-F: in OHT-eyes, MHC-II was upregulated in Müller cells (arrowhead) in (E), the intensity of the staining being greater than in contralateral eyes (arrowhead) in (B). GFAP-IR was absent or faint in those Müller cells exhibiting MHC-II immunostaining (D-F). Both in contralateral (B) and OHT-eyes (E), the retinal-like section effect enabled us to determine that MHC-II upregulation in Müller cells was preferentially located in the end-foot of the cells. Fluorescence microscopy and image acquisition using the ApoTome. GFAP, glial fibrillary acidic protein; MHC, major histocompatibility complex; OHT, ocular hypertension.
Figure 10 Retinal whole-mount. Double immunostaining for GFAP (in red) and MHC-II (in green) after 15 days of laser-induced OHT. The pressure exerted by the cover glass on the retinal whole-mount, produced a retinal-like section effect in some retinal borders. A-C: in contralateral eyes (A), the GFAP immunoreaction (IR) of Müller cells was weaker than in OHT-eyes (D). MHC-II expression was greater in astrocytes (arrow) than in Müller cells (arrowhead) in (B); D-F: in OHT-eyes, MHC-II was upregulated in Müller cells (arrowhead) in (E), the intensity of the staining being greater than in contralateral eyes (arrowhead) in (B). GFAP-IR was absent or faint in those Müller cells exhibiting MHC-II immunostaining (D-F). Both in contralateral (B) and OHT-eyes (E), the retinal-like section effect enabled us to determine that MHC-II upregulation in Müller cells was preferentially located in the end-foot of the cells. Fluorescence microscopy and image acquisition using the ApoTome. GFAP, glial fibrillary acidic protein; MHC, major histocompatibility complex; OHT, ocular hypertension.CC BY · PubMed Central

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Authors
Gallego, B. I., Salazar, J. J., de Hoz, R., Rojas, B., Ramírez, A. I., Salinas-Navarro, M., Ortín-Martínez, A., Valiente-Soriano, F. J., Avilés-Trigueros, M., Villegas-Perez, M. P., Vidal-Sanz, M., Triviño, A., & Ramírez, J. M.
Affiliations
  • Universidad Complutense de Madrid (ES)
  • Universidad de Murcia (ES)
ORCID
Venue
Journal of Neuroinflammation
Publisher
Springer Science and Business Media LLC
Published
2012-05-14
Volume
9
Issue
1
Pages
92-92
ISSN
1742-2094 (ISSN-L)
DOI
10.1186/1742-2094-9-92
PMC
PMC3410794
OpenAlex
W2029522517
Cited by
224
References
88
Citations by year
2026: 5 · 2025: 9 · 2024: 5 · 2023: 17 · 2022: 18 · 2021: 29 · 2020: 22 · 2019: 15 · 2018: 10 · 2017: 21 · 2016: 24 · 2015: 22 · 2014: 15 · 2013: 8 · 2012: 4
FWCI
14.66
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroinflammation (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by)
  • Library Open Repository (Universidad Complutense Madrid) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Fundación Mutua Madrileña (4131173)
  • Universidad Complutense de Madrid (GR35/10A, GR35/10)
  • Ministerio de Ciencia e Innovación
  • Instituto de Salud Carlos III (RD07/0062/0000, RD07/0062)
Topics
  • Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
Keywords
experimental glaucoma, ocular hypertension, laser-induced ocular hypertension, microglial activation, astrocytes, glial fibrillary acidic protein, MHC class II, retinal ganglion cells, Müller cells, neuroinflammation, fellow eye, neurodegeneration, neurofilaments, Iba1, mice, glaucoma risk factors, neuroprotection
MeSH terms
Animals, Histocompatibility Antigens Class II, Astrocytes, Cell Count, Glaucoma, Glial Fibrillary Acidic Protein, Intraocular Pressure, Male, Nerve Tissue Proteins, Ocular Hypertension, Retina, Retinal Ganglion Cells, Up-Regulation, Microglia, Mice

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