Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 108617, 13 pages
http://dx.doi.org/10.1155/2015/108617
Research Article

Decreased TNF Levels and Improved Retinal Ganglion Cell Survival in MMP-2 Null Mice Suggest a Role for MMP-2 as TNF Sheddase

1Laboratory of Neural Circuit Development and Regeneration, Animal Physiology and Neurobiology Section, Department of Biology, KU Leuven, Naamsestraat 61, 3000 Leuven, Belgium
2Inflammation Research Center, VIB, FSVM Building, Technologiepark 927, 9052 Ghent, Belgium
3Department of Biomedical Molecular Biology, Ghent University, FSVM Building, Technologiepark 927, 9052 Ghent, Belgium

Received 7 July 2015; Accepted 27 August 2015

Academic Editor: Ulrich Eisel

Copyright © 2015 Lies De Groef et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. P. Miller, J. Holcomb, I. Al-Ramahi et al., “Matrix metalloproteinases are modifiers of huntingtin proteolysis and toxicity in Huntington's disease,” Neuron, vol. 67, no. 2, pp. 199–212, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Rivera, M. Khrestchatisky, L. Kaczmarek, G. A. Rosenberg, and D. M. Jaworski, “Metzincin proteases and their inhibitors: foes or friends in nervous system physiology?” The Journal of Neuroscience, vol. 30, no. 46, pp. 15337–15357, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. G. A. Rosenberg, “Matrix metalloproteinases and their multiple roles in neurodegenerative diseases,” The Lancet Neurology, vol. 8, no. 2, pp. 205–216, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. V. W. Yong, “Metalloproteinases: mediators of pathology and regeneration in the CNS,” Nature Reviews Neuroscience, vol. 6, no. 12, pp. 931–944, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Verslegers, K. Lemmens, I. Van Hove, and L. Moons, “Matrix metalloproteinase-2 and -9 as promising benefactors in development, plasticity and repair of the nervous system,” Progress in Neurobiology, vol. 105, pp. 60–78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. L. De Groef, I. Van Hove, E. Dekeyster, I. Stalmans, and L. Moons, “MMPs in the trabecular meshwork: promising targets for future glaucoma therapies?” Investigative Ophthalmology and Visual Science, vol. 54, no. 12, pp. 7756–7763, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. L. De Groef, I. Van Hove, E. Dekeyster, I. Stalmans, and L. Moons, “MMPs in the neuroretina and optic nerve: modulators of glaucoma pathogenesis and repair?” Investigative Ophthalmology & Visual Science, vol. 55, no. 3, pp. 1953–1964, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. J. M. Sivak and M. E. Fini, “MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology,” Progress in Retinal and Eye Research, vol. 21, no. 1, pp. 1–14, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. M. A. Wride, J. Geatrell, and J. A. Guggenheim, “Proteases in eye development and disease,” Birth Defects Research Part C—Embryo Today, vol. 78, no. 1, pp. 90–105, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. X. Zhang, M. Cheng, and S. K. Chintala, “Kainic acid-mediated upregulation of matrix metalloproteinase-9 promotes retinal degeneration,” Investigative Ophthalmology and Visual Science, vol. 45, no. 7, pp. 2374–2383, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Zhang, M. Cheng, and S. K. Chintala, “Optic nerve ligation leads to astrocyte-associated matrix metalloproteinase-9 induction in the mouse retina,” Neuroscience Letters, vol. 356, no. 2, pp. 140–144, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. S.-I. Manabe, Z. Gu, and S. A. Lipton, “Activation of matrix metalloproteinase-9 via neuronal nitric oxide synthase contributes to NMDA-induced retinal ganglion cell death,” Investigative Ophthalmology and Visual Science, vol. 46, no. 12, pp. 4747–4753, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. A. R. C. Santos, R. G. Corredor, B. A. Obeso et al., “β1 integrin-focal adhesion kinase (FAK) signaling modulates retinal ganglion cell (RGC) survival,” PLoS ONE, vol. 7, no. 10, Article ID e48332, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. S. K. Chintala, X. Zhang, J. S. Austin, and M. E. Fini, “Deficiency in matrix metalloproteinase gelatinase B (MMP-9) protects against retinal ganglion cell death after optic nerve ligation,” Journal of Biological Chemistry, vol. 277, no. 49, pp. 47461–47468, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. X. Zhang and S. K. Chintala, “Influence of interleukin-1 beta induction and mitogen-activated protein kinase phosphorylation on optic nerve ligation-induced matrix metalloproteinase-9 activation in the retina,” Experimental Eye Research, vol. 78, no. 4, pp. 849–860, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. X. Zhang, T. Sakamoto, Y. Hata et al., “Expression of matrix metalloproteinases and their inhibitors in experimental retinal ischemia-reperfusion injury in rats,” Experimental Eye Research, vol. 74, no. 5, pp. 577–584, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. M.-H. Sun, K.-J. Chen, Y.-P. Tsao et al., “Down-regulation of matrix metalloproteinase-9 by pyrrolidine dithiocarbamate prevented retinal ganglion cell death after transection of optic nerve in rats,” Current Eye Research, vol. 36, no. 11, pp. 1053–1063, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Guo, S. E. Moss, R. A. Alexander, R. R. Ali, F. W. Fitzke, and M. F. Cordeiro, “Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix,” Investigative Ophthalmology and Visual Science, vol. 46, no. 1, pp. 175–182, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. W. Halfter, M. Willem, and U. Mayer, “Basement membrane-dependent survival of retinal ganglion cells,” Investigative Ophthalmology and Visual Science, vol. 46, no. 3, pp. 1000–1009, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. O. A. Agapova, P. L. Kaufman, M. J. Lucarelli, B. T. Gabelt, and M. R. Hernandez, “Differential expression of matrix metalloproteinases in monkey eyes with experimental glaucoma or optic nerve transection,” Brain Research, vol. 967, no. 1-2, pp. 132–143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. O. A. Agapova, C. S. Ricard, M. Salvador-Silva, and M. Rosario Hernandez, “Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes,” Glia, vol. 33, no. 3, pp. 205–216, 2001. View at Google Scholar · View at Scopus
  22. K. Endo, T. Nakamachi, T. Seki et al., “Neuroprotective effect of PACAP against NMDA-induced retinal damage in the mouse,” Journal of Molecular Neuroscience, vol. 43, no. 1, pp. 22–29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Ito, M. Shimazawa, Y. Inokuchi et al., “Degenerative alterations in the visual pathway after NMDA-induced retinal damage in mice,” Brain Research, vol. 1212, pp. 89–101, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. F. Lebrun-Julien, L. Duplan, V. Pernet et al., “Excitotoxic death of retinal neurons in vivo occurs via a non-cell-autonomous mechanism,” Journal of Neuroscience, vol. 29, no. 17, pp. 5536–5545, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Nakano, H. O. Ikeda, M. Hangai et al., “Longitudinal and simultaneous imaging of retinal ganglion cells and inner retinal layers in a mouse model of glaucoma induced by N-methyl-D-aspartate,” Investigative Ophthalmology and Visual Science, vol. 52, no. 12, pp. 8754–8762, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Nakazawa, M. Shimura, M. Ryu et al., “ERK1 plays a critical protective role against N-methyl-D-aspartate-induced retinal injury,” Journal of Neuroscience Research, vol. 86, no. 1, pp. 136–144, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Nakazawa, H. Takahashi, K. Nishijima et al., “Pitavastatin prevents NMDA-induced retinal ganglion cell death by suppressing leukocyte recruitment,” Journal of Neurochemistry, vol. 100, no. 4, pp. 1018–1031, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. L. V. Kalia, S. K. Kalia, and M. W. Salter, “NMDA receptors in clinical neurology: excitatory times ahead,” The Lancet Neurology, vol. 7, no. 8, pp. 742–755, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. R. J. Casson, “Possible role of excitotoxicity in the pathogenesis of glaucoma,” Clinical and Experimental Ophthalmology, vol. 34, no. 1, pp. 54–63, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. N. N. Osborne, M. Ugarte, M. Chao et al., “Neuroprotection in relation to retinal ischemia and relevance to glaucoma,” Survey of Ophthalmology, vol. 43, no. 6, pp. S102–S128, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Seki and S. A. Lipton, “Targeting excitotoxic/free radical signaling pathways for therapeutic intervention in glaucoma,” Progress in Brain Research, vol. 173, pp. 495–510, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. T. H. Vu, J. M. Shipley, G. Bergers et al., “MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypetrophic chondrocytes,” Cell, vol. 93, no. 3, pp. 411–422, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Itoh, T. Ikeda, H. Gomi, S. Nakao, T. Suzuki, and S. Itohara, “Unaltered secretion of beta-amyloid precursor protein in gelatinase A (Matrix metalloproteinase 2)-deficient mice,” The Journal of Biological Chemistry, vol. 272, no. 36, pp. 22389–22392, 1997. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Rojas, B. I. Gallego, A. I. Ramírez et al., “Microglia in mouse retina contralateral to experimental glaucoma exhibit multiple signs of activation in all retinal layers,” Journal of Neuroinflammation, vol. 11, article 133, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. A. I. Ramírez, J. J. Salazar, R. de Hoz et al., “Quantification of the effect of different levels of IOP in the astroglia of the rat retina ipsilateral and contralateral to experimental glaucoma,” Investigative Ophthalmology and Visual Science, vol. 51, no. 11, pp. 5690–5696, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. B. I. Gallego, J. J. Salazar, R. de Hoz et al., “IOP induces upregulation of GFAP and MHC-II and microglia reactivity in mice retina contralateral to experimental glaucoma,” Journal of Neuroinflammation, vol. 9, no. 92, pp. 1742–2094, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Parrilla-Reverter, M. Agudo, F. Nadal-Nicolás et al., “Time-course of the retinal nerve fibre layer degeneration after complete intra-orbital optic nerve transection or crush: a comparative study,” Vision Research, vol. 49, no. 23, pp. 2808–2825, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. L. De Groef, K. Lemmens, I. Van Hove, and L. Moons, “Matrix metalloproteinases in the mouse retina: a comparative study of expression patterns and anti-MMP antibodies,” BMC Ophthalmology, In press.
  39. C. Galindo-Romero, M. Avilés-Trigueros, M. Jiménez-López et al., “Axotomy-induced retinal ganglion cell death in adult mice: quantitative and topographic time course analyses,” Experimental Eye Research, vol. 92, no. 5, pp. 377–387, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Vidal-Sanz, M. Salinas-Navarro, F. M. Nadal-Nicolás et al., “Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas,” Progress in Retinal and Eye Research, vol. 31, no. 1, pp. 1–27, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Schindelin, I. Arganda-Carreras, E. Frise et al., “Fiji: an open-source platform for biological-image analysis,” Nature Methods, vol. 9, no. 7, pp. 676–682, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Taylor, K. Arner, and F. Ghosh, “First responders: dynamics of pre-gliotic muller cell responses in the isolated adult rat retina,” Current Eye Research, vol. 11, pp. 1–16, 2014. View at Google Scholar
  43. G. Tezel, “TNF-α signaling in glaucomatous neurodegeneration,” in Progress in Brain Research, B. Giacinto and L. C. N. N. O. Carlo Nucci, Eds., pp. 409–421, Elsevier, 2008. View at Google Scholar
  44. M. D. Sternlicht and Z. Werb, “How matrix metalloproteinases regulate cell behavior,” Annual Review of Cell and Developmental Biology, vol. 17, pp. 463–516, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. A. J. Gearing, P. Beckett, M. Christodoulou et al., “Matrix metalloproteinases and processing of pro-TNF-alpha,” Journal of Leukocyte Biology, vol. 57, no. 5, pp. 774–777, 1995. View at Google Scholar
  46. J. Vandooren, N. Geurts, E. Martens, P. E. Van Den Steen, and G. Opdenakker, “Zymography methods for visualizing hydrolytic enzymes,” Nature Methods, vol. 10, no. 3, pp. 211–220, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Reichenbach and A. Bringmann, Müller Cells in the Healthy and Diseased Retina, Springer, New York, NY, USA, 2010.
  48. F. R. Vázquez-Chona, A. Swan, W. D. Ferrell et al., “Proliferative reactive gliosis is compatible with glial metabolic support and neuronal function,” BMC Neuroscience, vol. 12, no. 1, article 98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Vohra, J. C. Tsai, and M. Kolko, “The role of inflammation in the pathogenesis of glaucoma,” Survey of Ophthalmology, vol. 58, no. 4, pp. 311–320, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. J.-Y. C. Hsu, R. McKeon, S. Goussev et al., “Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury,” The Journal of Neuroscience, vol. 26, no. 39, pp. 9841–9850, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. M. M. Edwards and S. R. Robinson, “TNF alpha affects the expression of GFAP and S100B: implications for Alzheimer's disease,” Journal of Neural Transmission, vol. 113, no. 11, pp. 1709–1715, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Selmaj, B. Shafit-Zagardo, D. A. Aquino et al., “Tumor necrosis factor-induced proliferation of astrocytes from mature brain is associated with down-regulation of glial fibrillary acidic protein mRNA,” Journal of Neurochemistry, vol. 57, no. 3, pp. 823–830, 1991. View at Publisher · View at Google Scholar · View at Scopus
  53. M. J. Mohan, T. Seaton, J. Mitchell et al., “The tumor necrosis factor-alpha converting enzyme (TACE): a unique metalloproteinase with highly defined substrate selectivity,” Biochemistry, vol. 41, no. 30, pp. 9462–9469, 2002. View at Publisher · View at Google Scholar
  54. C. M. Overall and C. P. Blobel, “In search of partners: linking extracellular proteases to substrates,” Nature Reviews Molecular Cell Biology, vol. 8, no. 3, pp. 245–257, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. R. E. Vandenbroucke, E. Dejonckheere, F. Van Hauwermeiren et al., “Matrix metalloproteinase 13 modulates intestinal epithelial barrier integrity in inflammatory diseases by activating TNF,” EMBO Molecular Medicine, vol. 5, no. 7, pp. 932–948, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Fanjul-Fernández, A. R. Folgueras, S. Cabrera, and C. López-Otín, “Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1803, no. 1, pp. 3–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. Y.-P. Han, T.-L. Tuan, H. Wu, M. Hughes, and W. L. Garner, “TNF-alpha stimulates activation of pro-MMP2 in human skin through NF-(kappa)B mediated induction of MT1-MMP,” Journal of Cell Science, vol. 114, part 1, pp. 131–139, 2001. View at Google Scholar · View at Scopus
  58. G. Tezel, L. Y. Li, R. V. Patil, and M. B. Wax, “TNF-α and TNF-α receptor-1 in the retina of normal and glaucomatous eyes,” Investigative Ophthalmology & Visual Science, vol. 42, no. 8, pp. 1787–1794, 2001. View at Google Scholar · View at Scopus
  59. L. Yuan and A. H. Neufeld, “Tumor necrosis factor-α: a potentially neurodestructive cytokine produced by glia in the human glaucomatous optic nerve head,” GLIA, vol. 32, no. 1, pp. 42–50, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. G. Olmos and J. Lladó, “Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity,” Mediators of Inflammation, vol. 2014, Article ID 861231, 12 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Bringmann, A. Grosche, T. Pannicke, and A. Reichenbach, “GABA and glutamate uptake and metabolism in retinal glial (müller) cells,” Frontiers in Endocrinology, vol. 4, article 48, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Tilleux and E. Hermans, “Neuroinflammation and regulation of glial glutamate uptake in neurological disorders,” Journal of Neuroscience Research, vol. 85, no. 10, pp. 2059–2070, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. M. M. Al-Gayyar and N. M. Elsherbiny, “Contribution of TNF-alpha to the development of retinal neurodegenerative disorders,” European Cytokine Network, vol. 24, no. 1, pp. 27–36, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. G. Tezel, X. Yang, J. Yang, and M. B. Wax, “Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice,” Brain Research, vol. 996, no. 2, pp. 202–212, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. M. K. McCoy and M. G. Tansey, “TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease,” Journal of Neuroinflammation, vol. 5, article 45, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Tweedie, K. Sambamurti, and N. H. Greig, “TNF-α inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets,” Current Alzheimer Research, vol. 4, no. 4, pp. 378–385, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. R. E. Vandenbroucke and C. Libert, “Is there new hope for therapeutic matrix metalloproteinase inhibition?” Nature Reviews Drug Discovery, vol. 13, no. 12, pp. 904–927, 2014. View at Publisher · View at Google Scholar · View at Scopus