Disruption of fractalkine signaling leads to microglial activation and neuronal damage in the diabetic retina

ASN Neuro

Volumn 7, Issue 5, 2015, Pages

  Cardona, Sandra M ^a   Mendiola, Andrew S ^a   Yang, Ya Chin ^a   Adkins, Sarina L ^a   Torres, Vanessa ^a   Cardona, Astrid E ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

CX3CR1; Fractalkine; Inflammation; Microglia; Neurodegeneration; Retinal ganglion cell

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CX3CR1 X; CHEMOKINE RECEPTOR CX3CR1 Y; CHEMOKINE RECEPTOR CX3CR1 Z; COMPLEMENTARY DNA; CYTOKINE ANTIBODY; FRACTALKINE; GAMMA INTERFERON; GLUCOSE; GLYCOPROTEIN P 15095; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; NITRITE; RNA; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; CX3CL1 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DAMAGE; CELL SUSPENSION; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLYCEMIC INDEX; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KNOCKOUT MOUSE; MICROGLIA; MONONUCLEAR CELL; MOUSE; NERVE CELL MEMBRANE; NERVE DEGENERATION; NERVE INJURY; NONHUMAN; POLYMERASE CHAIN REACTION; RETINA NERVE CELL; UPREGULATION; ANIMAL; ASTROCYTE; C57BL MOUSE; EXPERIMENTAL DIABETES MELLITUS; GENETICS; IMMUNOMODULATION; MALE; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA;

ANIMALS; ASTROCYTES; CHEMOKINE CX3CL1; DIABETES MELLITUS, EXPERIMENTAL; INTERLEUKIN-1BETA; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NEUROIMMUNOMODULATION; NEURONS; NITRIC OXIDE; NITRITES; RETINA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84946204508     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1177/1759091415608204     Document Type: Article

References (67)

1. Akita mouse model of diabetes. Behavioural Brain Research, 226, 601-605.
2. Al-Shabrawey, M., Bartoli, M., El-Remessy, A. B., Ma, G., Matragoon, S., Lemtalsi, T., Caldwell, R. B. (2008). Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Investigative Ophthalmology & Visual Science, 49, 3231-3238.
3. Aloisi, F. (2001). Immune function of microglia. Glia, 36, 165-179.
4. Antonetti, D. A., Klein, R., & Gardner, T. W. (2012). Diabetic retinopathy. New England Journal of Medicine, 366, 1227-1239.
5. Barber, A. J. (2003). A new view of diabetic retinopathy: A neurodegenerative disease of the eye. Progress in Neuro- Psychopharmacology & Biological Psychiatry, 27, 283-290.
6. Akita mouse as a model of early retinal complications in diabetes. Investigative Ophthalmology & Visual Science, 46, 2210-2218.
7. Benveniste, E. N. (1997). Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. Journal of Molecular Medicine, 75, 165-173.
8. Bessis, A., Bechade, C., Bernard, D., & Roumier, A. (2007). Microglial control of neuronal death and synaptic properties. Glia, 55, 233-238.
9. Brion, M., Sanchez-Salorio, M., Corton, M., de la Fuente, M., Pazos, B., Othman, M., Carracedo, A. (2011). Genetic association study of age-related macular degeneration in the Spanish population. Acta Ophthalmologica, 89, e12-e22.
10. Cardona, A. E., Huang, D., Sasse, M. E., & Ransohoff, R. M. (2006a). Isolation of murine microglial cells for RNA analysis or flow cytometry. Nature Protocols, 1, 1947-1951.
11. Cardona, A., Pioro, E. P., Sasse, M. E., Kostenko, V., Cardona, S. M., Dijkstra, I. M., Ransohoff, R. M. (2006b). Control of microglial neurotoxicity by the fractalkine receptor. Nature Neuroscience, 9, 917-924.
12. Cardona, A. E., Sasse, M. E., Mizutani, M., Cardona, S. M., Liu, L., Savarin, C., Ransohoff, R. M. (2008). Scavenging roles of chemokine receptors: Chemokine receptor deficiency is associated with increased levels of ligand in circulation and tissues. Blood, 112, 256-263.
13. Chan, C. C., Tuo, J., Bojanowski, C. M., Csaky, K. G., & Green, W. R. (2005). Detection of CX3CR1 single nucleotide polymorphism and expression on archived eyes with age-related macular degeneration. Journal of Histology & Histopathology, 20, 857-863.
14. Cheung, N., Mitchell, P., & Wong, T. Y. (2010). Diabetic retinopathy. Lancet, 376, 124-136.
15. Cho, S. H., Sun, B., Zhou, Y., Kauppinen, T. M., Halabisky, B., Wes, P., Gan, L. (2011). CX3CR1 protein signaling modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer disease. The Journal of Biological Chemistry, 286, 32713-32722.
16. Cook, D. N., Chen, S. C., Sullivan, L. M., Manfra, D. J., Wiekowski, M. T., Prosser, D. M., Lira, S. A. (2001). Generation and analysis of mice lacking the chemokine fractalkine. Journal of Molecular Cell Biology, 21, 3159-3165.
17. Corbett, J. A., Wang, J. L., Sweetland, M. A., Lancaster, J. R. Jr., & McDaniel, M. L. (1992). Interleukin 1 beta induces the formation of nitric oxide by beta-cells purified from rodent islets of Langerhans. Evidence for the beta-cell as a source and site of action of nitric oxide. Journal of Clinical Investigation, 90, 2384-2391.
18. Craner, M. J., Lo, A. C., Black, J. A., & Waxman, S. G. (2003). Abnormal sodium channel distribution in optic nerve axons in a model of inflammatory demyelination. Brain, 126, 1552-1561.
19. Dagkalis, A., Wallace, C., Hing, B., Liversidge, J., & Crane, I. J. (2009). CX3CR1-deficiency is associated with increased severity of disease in experimental autoimmune uveitis. Immunology, 128, 25-33.
20. Faure, S., Meyer, L., Costagliola, D., Vaneensberghe, C., Genin, E., Autran, B., Combadiere, C. (2000). Rapid progression to AIDS in HIVþ individuals with a structural variant of the chemokine receptor CX3CR1. Science, 287, 2274-2277.
21. Fujita, H., Tanaka, J., Toku, K., Tateishi, N., Suzuki, Y., Matsuda, S., Maeda, N. (1996). Effects of GM-CSF and ordinary supplements on the ramification of microglia in culture: A morphometrical study. Glia, 18, 269-281.
22. Funamoto, M., Fujio, Y., Kunisada, K., Negoro, S., Tone, E., Osugi, T., Yamauchi-Takihara, K. (2000). Signal transducer and activator of transcription 3 is required for glycoprotein 130- mediated induction of vascular endothelial growth factor in cardiac myocytes. The Journal of Biological Chemistry, 275, 10561-10566.
23. Gardner, T. W., Antonetti, D. A., Barber, A. J., LaNoue, K. F., & Levison, S. W. (2002). Diabetic retinopathy: More than meets the eye. Survey of Ophthalmology, 47(Suppl 2): S253-S262.
24. Akita diabetic mice. Investigative Ophthalmology & Visual Science, 49, 2635-2642.
25. Griffin, W. S., & Mrak, R. E. (2002). Interleukin-1 in the genesis and progression of and risk for development of neuronal degeneration in Alzheimer's disease. Journal of Leukocyte Biology, 72, 233-238.
26. Grigsby, J. G., Cardona, S. M., Pouw, C. E., Muniz, A., Mendiola, A. S., Tsin, A. T., Cardona, A. E. (2014). The role of microglia in diabetic retinopathy. Journal of Ophthalmology, 2014, 705-783.
27. Akita mice. The Journal of Immunology, 177, 7250-7256.
28. Hailer, N. P., Vogt, C., Korf, H. W., & Dehghani, F. (2005). Interleukin-1beta exacerbates and interleukin-1 receptor antagonist attenuates neuronal injury and microglial activation after excitotoxic damage in organotypic hippocampal slice cultures. European Journal of Neuroscience, 21, 2347-2360.
29. Harrison, J. K., Fong, A. M., Swain, P. A., Chen, S., Yu, Y. R., Salafranca, M. N., Patel, D. D. (2001). Mutational analysis of the fractalkine chemokine domain. Basic amino acid residues differentially contribute to CX3CR1 binding, signaling, and cell adhesion. Journal of Biological Chemistry, 276, 21632-21641.
30. Heidary, M., Rakhshi, N., Pahlevan, K. M., Behmanesh, M., Sanati, M. H., Sanadgol, N., Nikravesh, A. (2014). The analysis of correlation between IL-1B gene expression and genotyping in multiple sclerosis patients. Journal of the Neurological Sciences, 343, 41-45.
31. Hooper-van, V. T., Schrijver, H. M., Zwiers, A., Crusius, J. B., Knol, D. L., Kalkers, N. F., Uitdehaag, B. M. (2003). The interleukin-1 gene family in multiple sclerosis susceptibility and disease course. Multiple Sclerosis Journal, 9, 535-539.
32. Huang, D., Shi, F. D., Jung, S., Pien, G. C., Wang, J., Salazar- Mather, T. P., Ransohoff, R. M. (2006). The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB Journal, 20, 896-905.
33. Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., Littman, D. R. (2000). Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Journal of Molecular Cell Biology, 20, 4106-4114.
34. Akita) diabetic mouse. Investigative Ophthalmology & Visual Science, 54, 854-863.
35. Kowluru, R. A., & Odenbach, S. (2004). Role of interleukin-1beta in the pathogenesis of diabetic retinopathy. British Journal of Ophthalmology, 88, 1343-1347.
36. Lavalette, S., Raoul, W., Houssier, M., Camelo, S., Levy, O., Calippe, B., Sennlaub, F. (2011). Interleukin-1beta inhibition prevents choroidal neovascularization and does not exacerbate photoreceptor degeneration. American Journal of Pathology, 178, 2416-2423.
37. Liang, K. J., Lee, J. E., Wang, Y. D., Ma, W., Fontainhas, A. M., Fariss, R. N., Wong, W. T. (2009). Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Investigative Ophthalmology & Visual Science, 50, 4444-4451.
38. Lima-Junior, D. S., Costa, D. L., Carregaro, V., Cunha, L. D., Silva, A. L., Mineo, T. W., Zamboni, D. S. (2013). Inflammasomederived IL-1beta production induces nitric oxide-mediated resistance to Leishmania. Journal of Natural Medicines, 19, 909-915.
39. Liu, Z., Condello, C., Schain, A., Harb, R., & Grutzendler, J. (2010). CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-beta phagocytosis. Journal of Neuroscience, 30, 17091-17101.
40. McDermott, D. H., Colla, J. S., Kleeberger, C. A., Plankey, M., Rosenberg, P. S., Smith, E. D., Murphy, P. M. (2000). Genetic polymorphism in CX3CR1 and risk of HIV disease. Science, 290, 2031.
41. McDermott, D. H., Fong, A. M., Yang, Q., Sechler, J. M., Cupples, L. A., Merrell, M. N., Murphy, P. M. (2003). Chemokine receptor mutant CX3CR1-M280 has impaired adhesive function and correlates with protection from cardiovascular disease in humans. Journal of Clinical Investigation, 111, 1241-1250.
42. McDermott, D. H., Halcox, J. P., Schenke, W. H., Waclawiw, M. A., Merrell, M. N., Epstein, N., Murphy, P. M. (2001). Association between polymorphism in the chemokine receptor CX3CR1 and coronary vascular endothelial dysfunction and atherosclerosis. Circulation Research, 89, 401-407.
43. Medel-Matus, J. S., Alvarez-Croda, D. M., Martinez-Quiroz, J., Beltran-Parrazal, L., Morgado-Valle, C., & Lopez-Meraz, M. L. (2014). IL-1beta increases necrotic neuronal cell death in the developing rat hippocampus after status epilepticus by activating type I IL-1 receptor (IL-1RI). International Journal of Developmental Neuroscience, 38, 232-240.
44. Moatti, D., Faure, S., Fumeron, F., Amara, M., Seknadji, P., McDermott, D. H., Combadiere, C. (2001). Polymorphism in the fractalkine receptor CX3CR1 as a genetic risk factor for coronary artery disease. Blood, 97, 1925-1928.
45. Murray, K. N., Parry-Jones, A. R., & Allan, S. M. (2015). Interleukin-1 and acute brain injury. Frontiers in Cellular Neuroscience, 9, 18.
46. Ojima, T., Takagi, H., Suzuma, K., Oh, H., Suzuma, I., Ohashi, H., Yoshimura, N. (2006). EphrinA1 inhibits vascular endothelial growth factor-induced intracellular signaling and suppresses retinal neovascularization and blood-retinal barrier breakdown. American Journal of Pathology, 168, 331-339.
47. Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Gross, C. T. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science, 333, 1456-1458.
48. Patel, J. I., Tombran-Tink, J., Hykin, P. G., Gregor, Z. J., & Cree, I. A. (2006). Vitreous and aqueous concentrations of proangiogenic, antiangiogenic factors and other cytokines in diabetic retinopathy patients with macular edema: Implications for structural differences in macular profiles. Experimental Eye Research, 82, 798-806.
49. Peelen, E., Damoiseaux, J., Muris, A. H., Knippenberg, S., Smolders, J., Hupperts, R., Thewissen, M. (2015). Increased inflammasome related gene expression profile in PBMC may facilitate T helper 17 cell induction in multiple sclerosis. Molecular Immunology, 63, 521-529.
50. Pino, P. A., & Cardona, A. E. (2011). Isolation of brain and spinal cord mononuclear cells using percoll gradients. Journal of Visualized Experiments, 48. doi: 10.3791/2348.
51. Ponomarev, E. D., Shriver, L. P., Maresz, K., & Dittel, B. N. (2005). Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. Journal of Neuroscience Research, 81, 374-389.
52. Ransohoff, R. M., & Cardona, A. E. (2010). The myeloid cells of the central nervous system parenchyma. Nature, 468, 253-262.
53. Raoul, W., Feumi, C., Keller, N., Lavalette, S., Houssier, M., Behar-Cohen, F., Sennlaub, F. (2008). Lipid-bloated subretinal microglial cells are at the origin of drusen appearance in CX3CR1-deficient mice. Ophthalmic Research, 40, 115-119.
54. Re, D. B., & Przedborski, S. (2006). Fractalkine: Moving from chemotaxis to neuroprotection. Nature Neuroscience, 9, 859-861.
55. Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., Gemma, C. (2011). CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. Journal of Neuroscience, 31, 16241-16250.
56. Rossi, D. L., Hardiman, G., Copeland, N. G., Gilbert, D. J., Jenkins, N., Zlotnik, A., Bazan, J. F. (1998). Cloning and characterization of a new type of mouse chemokine. Genomics, 47, 163-170.
57. Schaumberg, D. A., Rose, L., DeAngelis, M. M., Semba, R. D., Hageman, G. S., & Chasman, D. I. (2014). Prospective study of common variants in CX3CR1 and risk of macular degeneration: Pooled analysis from 5 long-term studies. JAMA Ophthalmology, 132, 84-95.
58. Scuderi, S., D'amico, A. G., Federico, C., Saccone, S., Magro, G., Bucolo, C., D'Agata, V. (2015). Different retinal expression patterns of IL-1alpha, IL-1beta, and their receptors in a rat model of type 1 STZ-induced diabetes. Journal of Molecular Neuroscience 56, 431-439.
59. Tang, J., & Kern, T. S. (2011). Inflammation in diabetic retinopathy. Progress in Retinal and Eye Research, 30, 343-358.
60. Tarozzo, G., Bortolazzi, S., Crochemore, C., Chen, S. C., Lira, A. S., Abrams, J. S., Beltramo, M. (2003). Fractalkine protein localization and gene expression in mouse brain. Journal of Neuroscience Research, 73, 81-88.
61. Tarozzo, G., Campanella, M., Ghiani, M., Bulfone, A., & Beltramo, M. (2002). Expression of fractalkine and its receptor, CX3CR1, in response to ischaemia-reperfusion brain injury in the rat. European Journal of Neuroscience, 15, 1663-1668.
62. Tuo, J., Smith, B. C., Bojanowski, C. M., Meleth, A. D., Gery, I., Csaky, K. G., Chan, C. C. (2004). The involvement of sequence variation and expression of CX3CR1 in the pathogenesis of age-related macular degeneration. FASEB Journal, 18, 1297-1299.
63. Vallejo, S., Palacios, E., Romacho, T., Villalobos, L., Peiro, C., & Sanchez-Ferrer, C. F. (2014). The interleukin-1 receptor antagonist anakinra improves endothelial dysfunction in streptozotocin- induced diabetic rats. Cardiovascular Diabetology, 13, 158.
64. Walker, D. G., Dalsing-Hernandez, J. E., Campbell, N. A., & Lue, L. F. (2009). Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: A potential mechanism leading to chronic inflammation. Experimental Neurology, 215, 5-19.
65. Wei, L. H., Kuo, M. L., Chen, C. A., Chou, C. H., Lai, K. B., Lee, C. N., Hsieh, C. Y. (2003). Interleukin-6 promotes cervical tumor growth by VEGF-dependent angiogenesis via a STAT3 pathway. Oncogene, 22, 1517-1527.
66. Xu, Q., Briggs, J., Park, S., Niu, G., Kortylewski, M., Zhang, S., Yu, H. (2005). Targeting Stat3 blocks both HIF-1 and VEGF expression induced by multiple oncogenic growth signaling pathways. Oncogene, 24, 5552-5560.
67. Ye, L., Huang, Y., Zhao, L., Li, Y., Sun, L., Zhou, Y., Zheng, J. C. (2013). IL-1beta and TNF-alpha induce neurotoxicity through glutamate production: A potential role for neuronal glutaminase. Journal of Neurochemistry, 125, 897-908.