Tightening the retinal glia limitans attenuates neuroinflammation after optic nerve injury.
glia limitans
matrix metalloproteinase-3
neurodegeneration
neuroinflammation
optic nerve crush
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
20
01
2020
revised:
20
05
2020
accepted:
04
06
2020
pubmed:
10
7
2020
medline:
15
12
2021
entrez:
10
7
2020
Statut:
ppublish
Résumé
Increasing evidence suggests that functional impairments at the level of the neurovascular unit (NVU) underlie many neurodegenerative and neuroinflammatory diseases. While being part of the NVU, astrocytes have been largely overlooked in this context and only recently, tightening of the glia limitans has been put forward as an important neuroprotective response to limit these injurious processes. In this study, using the retina as a central nervous system (CNS) model organ, we investigated the structure and function of the glia limitans, and reveal that the blood-retina barrier and glia limitans function as a coordinated double barrier to limit infiltration of leukocytes and immune molecules. We provide in vitro and in vivo evidence for a protective response at the NVU upon CNS injury, which evokes inflammation-induced glia limitans tightening. Matrix metalloproteinase-3 (MMP-3) was found to be a crucial regulator of this process, thereby revealing its beneficial and immunomodulatory role in the CNS. in vivo experiments in which MMP-3 activity was deleted via genetic and pharmacological approaches, combined with a comprehensive study of tight junction molecules, glial end feet markers, myeloid cell infiltration, cytokine expression and neurodegeneration, show that MMP-3 attenuates neuroinflammation and neurodegeneration by tightening the glia limitans, thereby pointing to a prominent role of MMP-3 in preserving the integrity of the NVU upon injury. Finally, we gathered promising evidence to suggest that IL1b, which is also regulated by MMP-3, is at least one of the molecular messengers that induces glia limitans tightening in the injured CNS.
Substances chimiques
Matrix Metalloproteinase 3
EC 3.4.24.17
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2643-2660Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Abbott, N. J., Ronnback, L., & Hansson, E. (2006). Astrocyte-endothelial interactions at the blood-brain barrier. Nature Reviews. Neuroscience, 7(1), 41-53. https://doi.org/10.1038/nrn1824
Agudo, M., Perez-Marin, M. C., Lonngren, U., Sobrado, P., Conesa, A., Canovas, I., … Vidal-Sanz, M. (2008). Time course profiling of the retinal transcriptome after optic nerve transection and optic nerve crush. Molecular Vision, 14, 1050-1063.
Bauer, H., Stelzhammer, W., Fuchs, R., Weiger, T. M., Danninger, C., Probst, G., & Krizbai, I. A. (1999). Astrocytes and neurons express the tight junction-specific protein occludin in vitro. Experimental Cell Research, 250(2), 434-438. https://doi.org/10.1006/excr.1999.4558
Bollaerts, I., Van Houcke, J., Andries, L., De Groef, L., & Moons, L. (2017). Neuroinflammation as fuel for axonal regeneration in the injured vertebrate central nervous system. Mediators of Inflammation, 2017, 9478542-9478514. https://doi.org/10.1155/2017/9478542
Brkic, M., Balusu, S., Libert, C., & Vandenbroucke, R. E. (2015). Friends or foes: Matrix metalloproteinases and their multifaceted roles in neurodegenerative diseases. Mediators of Inflammation, 2015, 620581-620527. https://doi.org/10.1155/2015/620581
Brkic, M., Balusu, S., Van Wonterghem, E., Gorle, N., Benilova, I., Kremer, A., … Vandenbroucke, R. E. (2015). Amyloid beta oligomers disrupt blood-CSF barrier integrity by activating matrix metalloproteinases. The Journal of Neuroscience, 35(37), 12766-12778. https://doi.org/10.1523/JNEUROSCI.0006-15.2015
Chung, Y. C., Kim, Y. S., Bok, E., Yune, T. Y., Maeng, S., & Jin, B. K. (2013). MMP-3 contributes to nigrostriatal dopaminergic neuronal loss, BBB damage, and neuroinflammation in an MPTP mouse model of Parkinson's disease. Mediators of Inflammation, 2013, 370526-370511. https://doi.org/10.1155/2013/370526
De Groef, L., Andries, L., Lemmens, K., Van Hove, I., & Moons, L. (2015). Matrix metalloproteinases in the mouse retina: A comparative study of expression patterns and MMP antibodies. BMC Ophthalmology, 15, 187. https://doi.org/10.1186/s12886-015-0176-y
De Groef, L., Dekeyster, E., Geeraerts, E., Lefevere, E., Stalmans, I., Salinas-Navarro, M., & Moons, L. (2016). Differential visual system organization and susceptibility to experimental models of optic neuropathies in three commonly used mouse strains. Experimental Eye Research, 145, 235-247. https://doi.org/10.1016/j.exer.2016.01.006
De Groef, L., Gaublomme, D., Janssens, E., Dekeyster, E., & Moons, L. (2012). Expression of MMP-2, -3, -9, and -14 in the healthy and diseased mouse retina. Paper presented at the 2012 ARVO Annual Meeting; 6-10 May 2012; Fort Lauderdale, FL.
D'Onofrio, P. M., Shabanzadeh, A. P., Choi, B. K., Bahr, M., & Koeberle, P. D. (2019). MMP inhibition preserves integrin ligation and FAK activation to induce survival and regeneration in RGCs following optic nerve damage. Investigative Ophthalmology and Visual Science, 60(2), 634-649. https://doi.org/10.1167/iovs.18-25257
Frankowski, J. C., DeMars, K. M., Ahmad, A. S., Hawkins, K. E., Yang, C., Leclerc, J. L., … Candelario-Jalil, E. (2015). Detrimental role of the EP1 prostanoid receptor in blood-brain barrier damage following experimental ischemic stroke. Scientific Reports, 5, 17956. https://doi.org/10.1038/srep17956
Gardner, T. W., Lieth, E., Khin, S. A., Barber, A. J., Bonsall, D. J., Lesher, T., … Brennan, W. A., Jr. (1997). Astrocytes increase barrier properties and ZO-1 expression in retinal vascular endothelial cells. Investigative Ophthalmology and Visual Science, 38(11), 2423-2427.
Geeraerts, E., Dekeyster, E., Gaublomme, D., Salinas-Navarro, M., De Groef, L., & Moons, L. (2016). A freely available semi-automated method for quantifying retinal ganglion cells in entire retinal flatmounts. Experimental Eye Research, 147, 105-113. https://doi.org/10.1016/j.exer.2016.04.010
Gesuete, R., Orsini, F., Zanier, E. R., Albani, D., Deli, M. A., Bazzoni, G., & De Simoni, M. G. (2011). Glial cells drive preconditioning-induced blood-brain barrier protection. Stroke, 42(5), 1445-1453. https://doi.org/10.1161/STROKEAHA.110.603266
Gregory, M. S., Hackett, C. G., Abernathy, E. F., Lee, K. S., Saff, R. R., Hohlbaum, A. M., … Ksander, B. R. (2011). Opposing roles for membrane bound and soluble Fas ligand in glaucoma-associated retinal ganglion cell death. PLoS One, 6(3), e17659. https://doi.org/10.1371/journal.pone.0017659
Grossetete, M., Phelps, J., Arko, L., Yonas, H., & Rosenberg, G. A. (2009). Elevation of matrix metalloproteinases 3 and 9 in cerebrospinal fluid and blood in patients with severe traumatic brain injury. Neurosurgery, 65(4), 702-708. https://doi.org/10.1227/01.NEU.0000351768.11363.48
Gurney, K. J., Estrada, E. Y., & Rosenberg, G. A. (2006). Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiology of Disease, 23(1), 87-96. https://doi.org/10.1016/j.nbd.2006.02.006
Hafez, S., Abdelsaid, M., Fagan, S. C., & Ergul, A. (2018). Peroxynitrite-induced tyrosine nitration contributes to matrix metalloprotease-3 activation: Relevance to hyperglycemic ischemic brain injury and tissue plasminogen activator. Neurochemical Research, 43(2), 259-266. https://doi.org/10.1007/s11064-017-2411-9
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., & Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology, 8(2), R19. https://doi.org/10.1186/gb-2007-8-2-r19
Hollanders, K., Hove, I. V., Sergeys, J., Bergen, T. V., Lefevere, E., Kindt, N., … Stalmans, I. (2017). AMA0428, a potent rock inhibitor, attenuates early and late experimental diabetic retinopathy. Current Eye Research, 42(2), 260-272. https://doi.org/10.1080/02713683.2016.1183030
Hollier, P.-L., Guimbal, S., Mora, P., Diop, A., Cornuault, L., Couffinhal, T., … Chapouly, C. (2020). Genetic disruption of the blood brain barrier leads to protective barrier formation at the glia limitans. bioRxiv. https://doi.org/10.1101/2020.03.13.990762
Horng, S., Therattil, A., Moyon, S., Gordon, A., Kim, K., Argaw, A. T., … John, G. R. (2017). Astrocytic tight junctions control inflammatory CNS lesion pathogenesis. The Journal of Clinical Investigation, 127(8), 3136-3151. https://doi.org/10.1172/JCI91301
Hu, T., You, Q., Chen, D., Tong, J., Shang, L., Luo, J., … Huang, J. (2016). Inhibiting matrix metalloproteinase 3 ameliorates neuronal loss in the ganglion cell layer of rats in retinal ischemia/reperfusion. Neurochemical Research, 41(5), 1107-1118. https://doi.org/10.1007/s11064-015-1800-1
Jalal, F. Y., Yang, Y., Thompson, J., Lopez, A. C., & Rosenberg, G. A. (2012). Myelin loss associated with neuroinflammation in hypertensive rats. Stroke, 43(4), 1115-1122. https://doi.org/10.1161/STROKEAHA.111.643080
Kadam, R. S., Williams, J., Tyagi, P., Edelhauser, H. F., & Kompella, U. B. (2013). Suprachoroidal delivery in a rabbit ex vivo eye model: Influence of drug properties, regional differences in delivery, and comparison with intravitreal and intracameral routes. Molecular Vision, 19, 1198-1210.
Kim, E. M., & Hwang, O. (2011). Role of matrix metalloproteinase-3 in neurodegeneration. Journal of Neurochemistry, 116(1), 22-32. https://doi.org/10.1111/j.1471-4159.2010.07082.x
Kim, J. H., Kim, J. H., Yu, Y. S., Kim, D. H., & Kim, K. W. (2009). Recruitment of pericytes and astrocytes is closely related to the formation of tight junction in developing retinal vessels. Journal of Neuroscience Research, 87(3), 653-659. https://doi.org/10.1002/jnr.21884
Lee, J. Y., Choi, H. Y., Ahn, H. J., Ju, B. G., & Yune, T. Y. (2014). Matrix metalloproteinase-3 promotes early blood-spinal cord barrier disruption and hemorrhage and impairs long-term neurological recovery after spinal cord injury. The American Journal of Pathology, 184(11), 2985-3000. https://doi.org/10.1016/j.ajpath.2014.07.016
Mac Nair, C. E., Schlamp, C. L., Montgomery, A. D., Shestopalov, V. I., & Nickells, R. W. (2016). Retinal glial responses to optic nerve crush are attenuated in Bax-deficient mice and modulated by purinergic signaling pathways. Journal of Neuroinflammation, 13(1), 93. https://doi.org/10.1186/s12974-016-0558-y
Manicone, A. M., & McGuire, J. K. (2008). Matrix metalloproteinases as modulators of inflammation. Seminars in Cell and Developmental Biology, 19(1), 34-41. https://doi.org/10.1016/j.semcdb.2007.07.003
McQuibban, G. A., Gong, J. H., Wong, J. P., Wallace, J. L., Clark-Lewis, I., & Overall, C. M. (2002). Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood, 100(4), 1160-1167.
Mudgett, J. S., Hutchinson, N. I., Chartrain, N. A., Forsyth, A. J., McDonnell, J., Singer, I. I., … Visco, D. M. (1998). Susceptibility of stromelysin 1-deficient mice to collagen-induced arthritis and cartilage destruction. Arthritis and Rheumatism, 41(1), 110-121. https://doi.org/10.1002/1529-0131(199801)41:1<110::AID-ART14>3.0.CO;2-G
Nicchia, G. P., Pisani, F., Simone, L., Cibelli, A., Mola, M. G., Dal Monte, M., … Svelto, M. (2016). Glio-vascular modifications caused by Aquaporin-4 deletion in the mouse retina. Experimental Eye Research, 146, 259-268. https://doi.org/10.1016/j.exer.2016.03.019
Parks, W. C., Wilson, C. L., & Lopez-Boado, Y. S. (2004). Matrix metalloproteinases as modulators of inflammation and innate immunity. Nature Reviews. Immunology, 4(8), 617-629. https://doi.org/10.1038/nri1418
Quintana, F. J. (2017). Astrocytes to the rescue! Glia limitans astrocytic endfeet control CNS inflammation. The Journal of Clinical Investigation, 127(8), 2897-2899. https://doi.org/10.1172/JCI95769
Rama Rao, K. V., & Kielian, T. (2015). Neuron-astrocyte interactions in neurodegenerative diseases: Role of neuroinflammation. Clin Exp Neuroimmunol, 6(3), 245-263. https://doi.org/10.1111/cen3.12237
Rosenberg, G. A. (2009). Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurology, 8(2), 205-216. https://doi.org/10.1016/S1474-4422(09)70016-X
Salmina, A. B. (2009). Neuron-glia interactions as therapeutic targets in neurodegeneration. Journal of Alzheimer's Disease, 16(3), 485-502. https://doi.org/10.3233/JAD-2009-0988
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., … Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676-682. http://www.nature.com/nmeth/journal/v9/n7/abs/nmeth.2019.html#supplementary-information
Schonbeck, U., Mach, F., & Libby, P. (1998). Generation of biologically active IL-1 beta by matrix metalloproteinases: A novel caspase-1-independent pathway of IL-1 beta processing. Journal of Immunology, 161(7), 3340-3346.
Sergeys, J., Etienne, I., Van Hove, I., Lefevere, E., Stalmans, I., Feyen, J. H. M., … Van Bergen, T. (2019). Longitudinal in vivo characterization of the Streptozotocin-induced diabetic mouse model: Focus on early inner retinal responses. Investigative Ophthalmology and Visual Science, 60(2), 807-822. https://doi.org/10.1167/iovs.18-25372
Siqueiros-Marquez, L., Benard, R., Vacca, O., Charles-Messance, H., Bolanos-Jimenez, R., Guilloneau, X., … Giocanti-Auregan, A. (2017). Protection of glial muller cells by dexamethasone in a mouse model of surgically induced blood-retinal barrier breakdown. Investigative Ophthalmology and Visual Science, 58(2), 876-886. https://doi.org/10.1167/iovs.16-20617
Stanimirovic, D. B., & Friedman, A. (2012). Pathophysiology of the neurovascular unit: Disease cause or consequence? Journal of Cerebral Blood Flow and Metabolism, 32(7), 1207-1221. https://doi.org/10.1038/jcbfm.2012.25
Storkebaum, E., Quaegebeur, A., Vikkula, M., & Carmeliet, P. (2011). Cerebrovascular disorders: Molecular insights and therapeutic opportunities. Nature Neuroscience, 14(11), 1390-1397. https://doi.org/10.1038/nn.2947
Thompson, A. M., Thomas, C. N., Begum, G., Ahmed, Z., Logan, A., Blanch, R. J., & Berry, M. (2018). Early biomarkers of retinal injury in rat optic nerve injury and blunt injury model of ocular trauma. Paper presented at the ARVO, Hawai.
Usui, Y., Westenskow, P. D., Kurihara, T., Aguilar, E., Sakimoto, S., Paris, L. P., … Friedlander, M. (2015). Neurovascular crosstalk between interneurons and capillaries is required for vision. The Journal of Clinical Investigation, 125(6), 2335-2346. https://doi.org/10.1172/JCI80297
Van Hove, H., Martens, L., Scheyltjens, I., De Vlaminck, K., Pombo Antunes, A. R., De Prijck, S., … Movahedi, K. (2019). A single-cell atlas of mouse brain macrophages reveals unique transcriptional identities shaped by ontogeny and tissue environment. Nature Neuroscience, 22(6), 1021-1035. https://doi.org/10.1038/s41593-019-0393-4
Van Hove, I., Lefevere, E., De Groef, L., Sergeys, J., Salinas-Navarro, M., Libert, C., … Moons, L. (2016). MMP-3 deficiency alleviates endotoxin-induced acute inflammation in the posterior eye segment. International Journal of Molecular Sciences, 17(11), 1825. https://doi.org/10.3390/ijms17111825
Van Hove, I., Lemmens, K., Van de Velde, S., Verslegers, M., & Moons, L. (2012). Matrix metalloproteinase-3 in the central nervous system: A look on the bright side. Journal of Neurochemistry, 2012(2), 1471-4159.
Van Lint, P., & Libert, C. (2007). Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. Journal of Leukocyte Biology, 82(6), 1375-1381. https://doi.org/10.1189/jlb.0607338
Vanden Berghe, T., Hulpiau, P., Martens, L., Vandenbroucke, R. E., Van Wonterghem, E., Perry, S. W., … Vandenabeele, P. (2015). Passenger mutations confound interpretation of all genetically modified congenic mice. Immunity, 43(1), 200-209. https://doi.org/10.1016/j.immuni.2015.06.011
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3(7), RESEARCH0034.
Vecino, E., Rodriguez, F. D., Ruzafa, N., Pereiro, X., & Sharma, S. C. (2016). Glia-neuron interactions in the mammalian retina. Progress in Retinal and Eye Research, 51, 1-40. https://doi.org/10.1016/j.preteyeres.2015.06.003
Verslegers, M., Van Hove, I., Dekeyster, E., Gantois, I., Hu, T.-T., D’Hooge, R., Arckens, L., & Moons, L. (2015). MMP-2 mediates Purkinje cell morphogenesis and spine development in the mouse cerebellum. Brain Structure and Function, 220, (3), 1601-1617. http://dx.doi.org/10.1007/s00429-014-0747-3
Wallach, D., Varfolomeev, E. E., Malinin, N. L., Goltsev, Y. V., Kovalenko, A. V., & Boldin, M. P. (1999). Tumor necrosis factor receptor and Fas signaling mechanisms. Annual Review of Immunology, 17, 331-367. https://doi.org/10.1146/annurev.immunol.17.1.331
Wang, S., Miura, M., Jung, Y. K., Zhu, H., Li, E., & Yuan, J. (1998). Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell, 92(4), 501-509. https://doi.org/10.1016/s0092-8674(00)80943-5
Wetzel, M., Li, L., Harms, K. M., Roitbak, T., Ventura, P. B., Rosenberg, G. A., … Cunningham, L. A. (2008). Tissue inhibitor of metalloproteinases-3 facilitates Fas-mediated neuronal cell death following mild ischemia. Cell Death and Differentiation, 15(1), 143-151. https://doi.org/10.1038/sj.cdd.4402246
Wilcock, D. M., Vitek, M. P., & Colton, C. A. (2009). Vascular amyloid alters astrocytic water and potassium channels in mouse models and humans with Alzheimer's disease. Neuroscience, 159(3), 1055-1069. https://doi.org/10.1016/j.neuroscience.2009.01.023
Yang, Z., Quigley, H. A., Pease, M. E., Yang, Y., Qian, J., Valenta, D., & Zack, D. J. (2007). Changes in gene expression in experimental glaucoma and optic nerve transection: The equilibrium between protective and detrimental mechanisms. Investigative Ophthalmology and Visual Science, 48(12), 5539-5548. https://doi.org/10.1167/iovs.07-0542