Nuclear factor of activated T cells is activated in the endothelium of retinal microvessels in diabetic mice

Journal of Diabetes Research

Volumn 2015, Issue , 2015, Pages

  Zetterqvist, Anna V ^a   Blanco, Fabiana ^a,b   Öhman, Jenny ^a   Kotova, Olga ^a   Berglund, Lisa M ^a   De Frutos Garcia, Sergio ^c   Al Naemi, Raed ^a   Wigren, Maria ^a   McGuire, Paul G ^c   Gonzalez Bosc, Laura V ^c   Gomez, Maria F ^a  

^a LUND UNIVERSITY   (Sweden)

^b DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^c UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APYRASE; ECTONUCLEOTIDASE APYRASE; GLUCOSE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; MESSENGER RNA; OSTEOPONTIN; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; A 285222; CALCIUM; ICAM1 PROTEIN, MOUSE; NFATC1 PROTEIN, MOUSE; NFATC2 PROTEIN, MOUSE; NFATC3 PROTEIN, MOUSE; NFATC4 PROTEIN, MOUSE; PYRAZOLE DERIVATIVE;

AKITA MOUSE; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD RETINA BARRIER; BLOOD VESSEL PERMEABILITY; CELL ACTIVATION; CONTROLLED STUDY; DIABETIC RETINOPATHY; DOWN REGULATION; ENDOTHELIUM; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; IMMUNOFLUORESCENCE; IN VIVO STUDY; INTRAPERITONEAL GLUCOSE TOLERANCE TEST; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA BLOOD VESSEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TISSUE HOMOGENATE; TRANSCRIPTION INITIATION; ANIMAL; AORTA; C57BL MOUSE; CHEMISTRY; DIABETES MELLITUS; EXPERIMENTAL DIABETES MELLITUS; INFLAMMATION; METABOLISM; MICROCIRCULATION; MICROVASCULATURE; PATHOLOGY; PERMEABILITY; RETINA VEIN; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

ANIMALS; AORTA; CALCIUM; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROCIRCULATION; MICROVESSELS; NFATC TRANSCRIPTION FACTORS; OSTEOPONTIN; PERMEABILITY; PYRAZOLES; RETINAL VEIN; RETINAL VESSELS; SIGNAL TRANSDUCTION;

EID: 84928243639     PISSN: 23146745     EISSN: 23146753     Source Type: Journal    
DOI: 10.1155/2015/428473     Document Type: Article

References (53)

1. M. Brownlee, "Biochemistry and molecular cell biology of diabetic complications," Nature, vol. 414, no. 6865, pp. 813-820, 2001.
2. J. Nilsson, L. M. Nilsson, Y.-W. Chen, J. D. Molkentin, D. Erlinge, and M. F. Gomez, "High glucose activates nuclear factor of activated T cells in native vascular smooth muscle," Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 4, pp. 794-800, 2006.
3. L. M. Nilsson-Berglund, A. V. Zetterqvist, J. Nilsson-? Ohman et al., "Nuclear factor of activated T cells regulates osteopontin expression in arterial smooth muscle in response to diabetesinduced hyperglycemia," Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 2, pp. 218-224, 2010.
4. H. Kawamura, T. Sugiyama, D. M. Wu et al., "ATP: a vasoactive signal in the pericyte-containing microvasculature of the rat retina," The Journal of Physiology, vol. 551, no. 3, pp. 787-799, 2003.
5. G. Costa, T. Pereira, A. M. Neto,A. J. Crist'ovão, A. F. Ambr'osio, and P. F. Santos, "High glucose changes extracellular adenosine triphosphate levels in rat retinal cultures," Journal of Neuroscience Research, vol. 87, no. 6, pp. 1375-1380, 2009.
6. T. S. Kern, "Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy," Experimental Diabetes Research, vol. 2007,Article ID 95103, 14 pages, 2007.
7. L. M. Nilsson, Z.-W. Sun, J. Nilsson et al., "Novel blocker of NFATactivation inhibits IL-6 production in humanmyometrial arteries and reduces vascular smooth muscle cell proliferation," The American Journal of Physiology-Cell Physiology, vol. 292, no. 3, pp. C1167-C1178, 2007.
8. M. Y. Lee, S. M. Garvey,A. S. Baras et al., "Integrative genomics identifies DSCR1 (RCAN1) as a novel NFAT-dependent mediator of phenotypic modulation in vascular smooth muscle cells," Human Molecular Genetics, vol. 19, no. 3, pp. 468-479, 2009.
9. A. V. Zetterqvist, L. M. Berglund, F. Blanco et al., "Inhibition of nuclear factor of activated T-cells (NFAT) suppresses accelerated atherosclerosis in diabeticmice," PLoS ONE, vol. 8, no. 6, Article ID e65020, 2013.
10. B. A. Hesser, X. H. Liang,G. Camenisch et al., "Down syndrome critical region protein 1 (DSCR1), a novel VEGF target gene that regulates expression of inflammatory markers on activated endothelial cells," Blood, vol. 104, no. 1, pp. 149-158, 2004.
11. A. W. Orr, M. Y. Lee, J. A. Lemmon et al., "Molecular mechanisms of collagen isotype-specific modulation of smooth muscle cell phenotype," Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 2, pp. 225-231, 2008.
12. D. S. McLeod, D. J. Lefer, C. Merges, andG. A. Lutty, "Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid," The American Journal of Pathology, vol. 147, no. 3, pp. 642-653, 1995.
13. J. Cunha-Vaz, J. R. Faria de Abreu, A. J. Campos, and G. M. Figo, "Early breakdown of the blood retinal barrier in diabetes," British Journal of Ophthalmology, vol. 59, no. 11, pp. 649-656, 1975.
14. D. A. Antonetti, A. J. Barber, L. A. Hollinger, E. B. Wolpert, and T. W. Gardner, "Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors," The Journal of Biological Chemistry, vol. 274, no. 33, pp. 23463-23467, 1999.
15. A. Cerani, N. Tetreault, C. Menard et al., "Neuron-derived semaphorin 3A is an early inducer of vascular permeability in diabetic retinopathy via neuropilin-1," Cell Metabolism, vol. 18, no. 4, pp. 505-518, 2013.
16. G. L. Hern'andez, O. V. Volpert, M. A. 'Iñiguez et al., "Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2," Journal of Experimental Medicine, vol. 193, no. 5, pp. 607-620, 2001.
17. C. A. Bretz, S. Savage, M. Capozzi, and J. S. Penn, "The role of the NFAT signaling pathway in retinal neovascularization," Investigative Ophthalmology & Visual Science, vol. 54, no. 10, pp. 7020-7027, 2013.
18. W. Dong, Y. Li, X. Li et al., "P85alpha mediates NFAT3-dependent VEGF induction in the cellular UVB response," Journal of Cell Science, vol. 126, no. 6, pp. 1317-1322, 2013.
19. M. Jinnin, D. Medici, L. Park et al., "Suppressed NFATdependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma," Nature Medicine, vol. 14, no. 11, pp. 1236-1246, 2008.
20. B. J. Wilkins, Y.-S. Dai, O. F. Bueno et al., "Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy," Circulation Research, vol. 94, no. 1, pp. 110-118, 2004.
21. C. Gustavsson, C.-D. Agardh, A. V. Zetterqvist, J. Nilsson, E. Agardh, and M. F. Gomez, "Vascular cellular adhesion molecule-1 (VCAM-1) expression in mice retinal vessels is affected by both hyperglycemia and hyperlipidemia," PLoS ONE, vol. 5, no. 9,Article ID e12699, 2010.
22. A. Strom, A. Franzen, C. Wangnerud et al., "Altered vascular remodeling in osteopontin-deficient atherosclerotic mice," Journal of Vascular Research, vol. 41, no. 4, pp. 314-322, 2004.
23. A. J. Barber, D. A. Antonetti, T. S. Kern et al., "The Ins2Akita mouse as a model of early retinal complications in diabetes," Investigative Ophthalmology and Visual Science, vol. 46, no. 6, pp. 2210-2218, 2005.
24. M. F. Gomez, L. V. G. Bosc, A. S. Stevenson, M. K. Wilkerson, D. C. Hill-Eubanks, and M. T. Nelson, "Constitutively elevated nuclear export activity opposes Ca2+-dependent NFATc3 nuclear accumulation in vascular smooth muscle: role of JNK2 and Crm-1," Journal of Biological Chemistry, vol. 278, no. 47, pp. 46847-46853, 2003.
25. A. Rinne, K. Banach, and L. A. Blatter, "Regulation of nuclear factor of activated T cells (NFAT) in vascular endothelial cells," Journal of Molecular and Cellular Cardiology, vol. 47, no. 3, pp. 400-410, 2009.
26. E. O. Hern'andez-Ochoa, M. Contreras, Z. Cseresny'es, and M. F. Schneider, "Ca2+ signal summation and NFATc1 nuclear translocation in sympathetic ganglion neurons during repetitive action potentials," Cell Calcium, vol. 41, no. 6, pp. 559-571, 2007.
27. Y. Xu, L. Yang, S. Yu et al., "Spatiotemporal changes in NFATc4 expression of retinal ganglion cells after light-induced damage," Journal of MolecularNeuroscience, vol. 53, no. 1, pp. 69-77, 2014.
28. L. Monnier and C. Colette, "Glycemic variability: shouldwe and can we prevent it" Diabetes Care, vol. 31, no. supplement 2, pp. S150-S154, 2008.
29. E. P. Kwan, L. Xie, L. Sheu et al., "Munc13-1 deficiency reduces insulin secretion and causes abnormal glucose tolerance," Diabetes, vol. 55, no. 5, pp. 1421-1429, 2006.
30. E. L. Fletcher, J. A. Phipps, M. M. Ward, T. Puthussery, and J. L. Wilkinson-Berka, "Neuronal and glial cell abnormality as predictors of progression of diabetic retinopathy," Current Pharmaceutical Design, vol. 13, no. 26, pp. 2699-2712, 2007.
31. J. Cunha-Vaz, "Characterization and relevance of different diabetic retinopathy phenotypes," Developments in Ophthalmology, vol. 39, pp. 13-30, 2007.
32. M. G. Petrovi?c, P. Koro?sec, M. Ko?snik, and M. Hawlina, "Vitreous levels of interleukin-8 in patients with proliferative diabetic retinopathy," The American Journal of Ophthalmology, vol. 143, no. 1, pp. 175-176, 2007.
33. A. M. A. El-Asrar, L. Missotten, and K. Geboes, "Expression of hypoxia-inducible factor-1 and the protein products of its target genes in diabetic fibrovascular epiretinal membranes," British Journal of Ophthalmology, vol. 91, no. 6, pp. 822-826, 2007.
34. Y. Wakabayashi, Y. Usui, Y. Okunuki et al., "Increased levels of monokine induced by interferon-gamma (Mig) in the vitreous of patients with diabetic retinopathy," DiabeticMedicine, vol. 25, no. 7, pp. 875-877, 2008.
35. M. My'sliwiec, K. Zorena, A. Balcerska, J. My'sliwska, P. Lipowski, and K. Raczy'nska, "The activity of N-acetyl-beta-dglucosaminidase and tumor necrosis factor-alpha at early stage of diabetic retinopathy development in type 1 diabetes mellitus children," Clinical Biochemistry, vol. 39,no. 8, pp. 851-856, 2006.
36. K. Zorena, J. My'sliwska, M. My'sliwiec, A. Balcerska, P. Lipowski, and K. Raczy'nska, "Interleukin-12 and tumour necrosis factor-alpha equilibrium is a prerequisite for clinical course free from late complications in children with type 1 diabetes mellitus," Scandinavian Journal of Immunology, vol. 67,no. 2, pp. 204-208, 2008.
37. R. A. Kowluru and S. Odenbach, "Role of interleukin-1 in the pathogenesis of diabetic retinopathy," British Journal of Ophthalmology, vol. 88, no. 10, pp. 1343-1347, 2004.
38. J. A. Vincent and S. Mohr, "Inhibition of caspase-1/interleukin-1beta signaling prevents degeneration of retinal capillaries in diabetes and galactosemia," Diabetes, vol. 56, no. 1, pp. 224-230, 2007.
39. E. Shimizu, H. Funatsu, H. Yamashita, T. Yamashita, and S. Hori, "Plasma level of interleukin-6 is an indicator for predicting diabetic macular edema," Japanese Journal of Ophthalmology, vol. 46, no. 1, pp. 78-83, 2002.
40. H. Funatsu, H. Yamashita, E. Shimizu, R. Kojima, and S. Hori, "Relationship between vascular endothelial growth factor and interleukin-6 in diabetic retinopathy," Retina, vol. 21, no. 5, pp. 469-477, 2001.
41. A. M. Joussen, V. Poulaki, N. Mitsiades et al., "Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression," The FASEB Journal, vol. 16, no. 3, pp. 438-440, 2002.
42. A. K. W. Lai and A. C. Y. Lo, "Animal models of diabetic retinopathy: summary and comparison," Journal of Diabetes Research, vol. 2013, Article ID 106594, 29 pages, 2013.
43. J. Nilsson-? Ohman, G. N. Fredrikson, L. M. Nilsson-Berglund et al., "Tumor necrosis factor-alpha does not mediate diabetesinduced vascular inflammation in mice," Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 10, pp. 1465-1470, 2009.
44. C.-G. Lee, K.-H. Kang, J.-S. So et al., "A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells,"Molecular Immunology, vol. 46, no. 4, pp. 613-621, 2009.
45. T. Smallie, G. Ricchetti, N. J. Horwood, M. Feldmann, A. R. Clark, and L. M. Williams, "IL-10 inhibits transcription elongation of the human TNF gene in primary macrophages," The Journal of ExperimentalMedicine, vol. 207, no. 10, pp. 2081-2088, 2010.
46. S. P. Didion, D. A. Kinzenbaw, L. I. Schrader, Y. Chu, and F. M. Faraci, "Endogenous interleukin-10 inhibits angiotensin IIinduced vascular dysfunction," Hypertension, vol. 54, no. 3, pp. 619-624, 2009.
47. S. Kase, M. Yokoi, W. Saito et al., "Increased osteopontin levels in the vitreous of patients with diabetic retinopathy," Ophthalmic Research, vol. 39, no. 3, pp. 143-147, 2007.
48. Q. Huang and N. Sheibani, "High glucose promotes retinal endothelial cell migration through activation of Src, PI3K/Akt1/ eNOS, and ERKs," The American Journal of Physiology-Cell Physiology, vol. 295, no. 6, pp. C1647-C1657, 2008.
49. H. Huang, J. K. Gandhi, X. Zhong et al., "TNFalpha is required for late BRB breakdown in diabetic retinopathy, and its inhibition prevents leukostasis and protects vessels and neurons from apoptosis," Investigative Ophthalmology and Visual Science, vol. 52, no. 3, pp. 1336-1344, 2011.
50. D. Navaratna, P. G. McGuire, G. Menicucci, and A. Das, "Proteolytic degradation of VE-cadherin alters the blood-retinal barrier in diabetes," Diabetes, vol. 56, no. 9, pp. 2380-2387, 2007.
51. J. M. Trevillyan, X. G. Chiou, Y.-W. Chen et al., "Potent inhibition ofNFAT activation and T cell cytokine production by novel low molecular weight pyrazole compounds," The Journal of Biological Chemistry, vol. 276, no. 51, pp. 48118-48126, 2001.
52. T. B?rsan, C. Dambrin, K. C. Marsh et al., "Preliminary in vivo pharmacokinetic and pharmacodynamic evaluation of a novel calcineurin-independent inhibitor of NFAT," Transplant International, vol. 17, no. 3, pp. 145-150, 2004.
53. R. Sim'o, J. M. Sundstrom, and D. A. Antonetti, "Ocular anti-VEGF therapy for diabetic retinopathy: the role of VEGF in the pathogenesis of diabetic retinopathy," Diabetes Care, vol. 37, no. 4, pp. 893-899, 2014.