Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: Relationship to capillary degeneration and permeability

FASEB Journal

Volumn 29, Issue 5, 2015, Pages 2194-2204

  Du, Yunpeng ^a   Cramer, Megan ^a   Lee, Chieh Allen ^a   Tang, Jie ^a   Muthusamy, Arivalagan ^a   Antonetti, David A ^a   Jin, Hui ^a   Palczewski, Krzysztof ^a   Kern, Timothy S ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

Diabetic retinopathy; GPCRs; Inflammation; NADPH oxidase

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 AMINOETHOXYDIPHENYLBORANE; ADRENERGIC RECEPTOR; ALPHA 1A ADRENERGIC RECEPTOR; APOCYNIN; CALCIUM ION; DOXAZOSIN; G PROTEIN COUPLED RECEPTOR; GLUCOSE; INOSITOL TRISPHOSPHATE; LOFEXIDINE; PHOSPHOLIPASE C; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RETINAL SUPEROXIDE GENERATION; SEROTONIN 2 RECEPTOR; SEROTONIN 4 RECEPTOR; SEROTONIN 6 RECEPTOR; SEROTONIN 7 RECEPTOR; SEROTONIN RECEPTOR; SUPEROXIDE; UNCLASSIFIED DRUG; CYCLIC AMP; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CAPILLARY PERMEABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CAPILLARY; RETINA DEGENERATION; VASCULAR LESION; VISION; ANIMAL; C57BL MOUSE; CAPILLARY; CELL CULTURE; COMPLICATION; CYTOLOGY; EXPERIMENTAL DIABETES MELLITUS; GENETICS; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RETINA; RETINAL DEGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MUS;

ANIMALS; CAPILLARIES; CELLS, CULTURED; CYCLIC AMP; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; MALE; MICE; MICE, INBRED C57BL; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ADRENERGIC; RECEPTORS, SEROTONIN; RETINA; RETINAL DEGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPEROXIDES;

EID: 84934946469     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-269431     Document Type: Article

References (61)

1. Fredriksson, R., Lagerström, M. C., Lundin, L. G., and Schiöth, H. B. (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paral-ogon groups, and fingerprints. Mol. Pharmacol. 63, 1256-1272
2. Marinissen, M. J., and Gutkind, J. S. (2001) G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol. Sci. 22, 368-376
3. Chen, Y., Palczewska, G., Mustafi, D., Golczak, M., Dong, Z., Sawada, O., Maeda, T., Maeda, A., and Palczewski, K. (2013) Systems pharmacology identifies drug targets for Stargardt disease-associated retinal degeneration. J. Clin. Invest. 123, 5119-5134
4. Usui, S., Oveson, B. C., Lee, S. Y., Jo, Y. J., Yoshida, T., Miki, A., Miki, K., Iwase, T., Lu, L., and Campochiaro, P. A. (2009) NADPH oxidase plays a central role in cone cell death in retinitis pigmentosa. J. Neurochem. 110, 1028-1037
5. Chen, Y., Okano, K., Maeda, T., Chauhan, V., Golczak, M., Maeda, A., and Palczewski, K. (2012) Mechanism of all-trans-retinal toxicity with implications for stargardt disease and age-related macular degeneration. J. Biol. Chem. 287, 5059-5069
6. Kowluru, R. A., Tang, J., and Kern, T. S. (2001) Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes 50, 1938-1942
7. Kanwar, M., Chan, P. S., Kern, T. S., and Kowluru, R. A. (2007) Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Invest. Ophthalmol. Vis. Sci. 48, 3805-3811
8. Berkowitz, B. A., Gradianu, M., Bissig, D., Kern, T. S., and Roberts, R. (2009) Retinal ion regulation in a mouse model of diabetic retinopathy: natural history and the effect of Cu/Zn superoxide dismutase overexpression. Invest. Ophthalmol. Vis. Sci. 50, 2351-2358
9. Du, Y., Veenstra, A., Palczewski, K., and Kern, T. S. (2013) Photoreceptor cells are major contributors to diabetes-induced oxidative stress and local inflammation in the retina. Proc. Natl. Acad. Sci. USA 110, 16586-16591
10. Collier, R. J., Wang, Y., Smith, S. S., Martin, E., Ornberg, R., Rhoades, K., and Romano, C. (2011) Complement deposition and microglial activation in the outer retina in light-induced retinopathy: inhibition by a 5-HT1A agonist. Invest. Ophthalmol. Vis. Sci. 52, 8108-8116
11. Collier, R. J., Patel, Y., Martin, E. A., Dembinska, O., Hellberg, M., Krueger, D. S., Kapin, M. A., and Romano, C. (2011) Agonists at the serotonin receptor (5-HT (1A)) protect the retina from severe photo-oxidative stress. Invest. Ophthalmol. Vis. Sci. 52, 2118-2126
12. Shen, J., Ghai, K., Sompol, P., Liu, X., Cao, X., Iuvone, P. M., and Ye, K. (2012) N-acetyl serotonin derivatives as potent neu-roprotectants for retinas. Proc. Natl. Acad. Sci. USA 109, 3540-3545
13. Thampi, P., Rao, H. V., Mitter, S. K., Cai, J., Mao, H., Li, H., Seo, S., Qi, X., Lewin, A. S., Romano, C., and Boulton, M. E. (2012) The 5HT1a receptor agonist 8-Oh DPAT induces protection from lipofuscin accumulation and oxidative stress in the retinal pigment epithelium. PLoS ONE 7, e34468
14. Renganathan, K., Gu, J., Rayborn, M. E., Crabb, J. S., Salomon, R. G., Collier, R. J., Kapin, M. A., Romano, C., Hollyfield, J. G., and Crabb, J. W. (2013) CEP biomarkers as potential tools for monitoring therapeutics. PLoS ONE 8, e76325
15. Al-Ubaidi, M. R., Font, R. L., Quiambao, A. B., Keener, M. J., Liou, G. I., Overbeek, P. A., and Baehr, W. (1992) Bilateral retinal and brain tumors in transgenic mice expressing simian virus 40 large T antigen under control of the human interphotoreceptor retinoid-binding protein promoter. J. Cell Biol. 119, 1681-1687
16. Lee, C. A., Li, G., Patel, M. D., Petrash, J. M., Benetz, B. A., Veenstra, A., Amengual, J., Von Lintig, J., Burant, C., Tang, J., and Kern, T. S. (2013) Diabetes-induced impairment in visual function in mice: contributions of p38 MAPK, RAGE, leukocytes, and aldose reductase. Invest. Ophthalmol. Vis. Sci. 93, 135-143
17. Tang, J., Allen Lee, C., Du, Y., Sun, Y., Pearlman, E., Sheibani, N., and Kern, T. S. (2013) MyD88-dependent pathways in leukocytes affect the retina in diabetes. PLoS ONE 8, e68871
18. Du, Y., Tang, J., Li, G., Berti-Mattera, L., Lee, C. A., Bartkowski, D., Gale, D., Monahan, J., Niesman, M. R., Alton, G., and Kern, T. S. (2010) Effects of p38 MAPK inhibition on early stages of diabetic retinopathy and sensory nerve function. Invest. Ophthalmol. Vis. Sci. 51, 2158-2164
19. Kern, T. S., Du, Y., Miller, C. M., Hatala, D. A., and Levin, L. A. (2010) Overexpression of Bcl-2 in vascular endothelium inhibits the microvascular lesions of diabetic retinopathy. Am. J. Pathol. 176, 2550-2558
20. Gubitosi-Klug, R. A., Talahalli, R., Du, Y., Nadler, J. L., and Kern, T. S. (2008) 5-Lipoxygenase, but not 12/15-lipoxygenase, contributes to degeneration of retinal capillaries in a mouse model of diabetic retinopathy. Diabetes 57, 1387-1393
21. Kern, T. S., Miller, C. M., Du, Y., Zheng, L., Mohr, S., Ball, S. L., Kim, M., Jamison, J. A., and Bingaman, D. P. (2007) Topical administration of nepafenac inhibits diabetes-induced retinal microvascular disease and underlying abnormalities of retinal metabolism and physiology. Diabetes 56, 373-379
22. Du, Y., Miller, C. M., and Kern, T. S. (2003) Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic. Biol. Med. 35, 1491-1499
23. Best, T. M., Fiebig, R., Corr, D. T., Brickson, S., and Ji, L. (1999) Free radical activity, antioxidant enzyme, and glutathione changes with muscle stretch injury in rabbits. J. Appl. Physiol. 87, 74-82
24. Antonetti, D. A., Barber, A. J., Khin, S., Lieth, E., Tarbell, J. M., and Gardner, T. W.; Penn State Retina Research Group. (1998) Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells. Diabetes 47, 1953-1959
25. Li, G., Tang, J., Du, Y., Lee, C. A., and Kern, T. S. (2011) Beneficial effects of RAGE-Ig fusion protein on early diabetic retinopathy and tactile allodynia. Mol. Vis. 17, 3156-3165
26. Li, G., Veenstra, A. A., Talahalli, R. R., Wang, X., Gubitosi-Klug, R. A., Sheibani, N., and Kern, T. S. (2012) Marrow-derived cells regulate the development of early diabetic retinopathy and tactile allodynia in mice. Diabetes 61, 3294-3303
27. Veenstra, A. A., Tang, J., and Kern, T. S. (2013) Antagonism of CD11b with neutrophil inhibitory factor (NIF) inhibits vascular lesions in diabetic retinopathy. PLoS ONE 8, e78405
28. Al-Shabrawey, M., Rojas, M., Sanders, T., Behzadian, A., El-Remessy, A., Bartoli, M., Parpia, A. K., Liou, G., and Caldwell, R. B. (2008) Role of NADPH oxidase in retinal vascular inflammation. Invest. Ophthalmol. Vis. Sci. 49, 3239-3244
29. Zheng, L., Du, Y., Miller, C., Gubitosi-Klug, R. A., Ball, S., Berkowitz, B. A., and Kern, T. S. (2007) Critical role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes. Diabetologia 50, 1987-1996
30. Elms, S. C., Toque, H. A., Rojas, M., Xu, Z., Caldwell, R. W., and Caldwell, R. B. (2013) The role of arginase I in diabetes-induced retinal vascular dysfunction in mouse and rat models of diabetes. Diabetologia 56, 654-662
31. Tang, J., Du, Y., Petrash, J. M., Sheibani, N., and Kern, T. S. (2013) Deletion of aldose reductase from mice inhibits diabetes-induced retinal capillary degeneration and superoxide generation. PLoS ONE 8, e62081
32. Billington, C. K., and Hall, I. P. (2012) Novel cAMP signalling paradigms: therapeutic implications for airway disease. Br. J. Pharmacol. 166, 401-410
33. Inoue, T., Suzuki, Y., Yoshimaru, T., and Ra, C. (2008) Reactive oxygen species produced up- or downstream of calcium influx regulate proinflammatory mediator release from mast cells: role of NADPH oxidase and mitochondria. Biochim. Biophys. Acta 1783, 789-802
34. Brown, G. C. (2007) Mechanisms of inflammatory neuro-degeneration: iNOS and NADPH oxidase. Biochem. Soc. Trans. 35, 1119-1121
35. Yamamori, T., Inanami, O., Nagahata, H., Cui, Y., and Kuwabara, M. (2000) Roles of p38 MAPK, PKC and PI3-K in the signaling pathways of NADPH oxidase activation and phagocytosis in bovine polymorphonuclear leukocytes. FEBS Lett. 467, 253-258
36. Al-Shabrawey, M., Bartoli, M., El-Remessy, A. B., Ma, G., Matragoon, S., Lemtalsi, T., Caldwell, R. W., and Caldwell, R. B. (2008) Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Invest. Oph-thalmol. Vis. Sci. 49, 3231-3238
37. Wilkinson-Berka, J. L., Deliyanti, D., Rana, I., Miller, A. G., Agrotis, A., Armani, R., Szyndralewiez, C., Wingler, K., Touyz, R. M., Cooper, M. E., Jandeleit-Dahm, K. A., and Schmidt, H. H. (2014) NADPH oxidase, NOX1, mediates vascular injury in ischemic retinopathy. Antioxid. Redox Signal. 20, 2726-2740
38. Gray, S. P., Di Marco, E., Okabe, J., Szyndralewiez, C., Heitz, F., Montezano, A. C., De Haan, J. B., Koulis, C., El-Osta, A., Andrews, K. L., Chin-Dusting, J. P., Touyz, R. M., Wingler, K., Cooper, M. E., Schmidt, H. H., and Jandeleit-Dahm, K. A. (2013) NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 127, 1888-1902
39. Sedeek, M., Nasrallah, R., Touyz, R. M., and Hébert, R. L. (2013) NADPH oxidases, reactive oxygen species, and the kidney: friend and foe. J. Am. Soc. Nephrol. 24, 1512-1518
40. Chan, E. C., Van Wijngaarden, P., Liu, G. S., Jiang, F., Peshavariya, H., and Dusting, G. J. (2013) Involvement of Nox2 NADPH oxidase in retinal neovascularization. Invest. Ophthalmol. Vis. Sci. 54, 7061-7067
41. Suzuki, F., Taniguchi, T., Nakamura, S., Akagi, Y., Kubota, C., Satoh, M., and Muramatsu, I. (2002) Distribution of alpha-1 adrenoceptor subtypes in RNA and protein in rabbit eyes. Br. J. Pharmacol. 135, 600-608
42. Zarbin, M. A., Wamsley, J. K., Palacios, J. M., and Kuhar, M. J. (1986) Autoradiographic localization of high affinity GABA, benzodiazepine, dopaminergic, adrenergic and muscarinic cholinergic receptors in the rat, monkey and human retina. Brain Res. 374, 75-92
43. Woldemussie, E., Wijono, M., and Pow, D. (2007) Localization of alpha 2 receptors in ocular tissues. Vis. Neurosci. 24, 745-756
44. Prabu, S. K., Anandatheerthavarada, H. K., Raza, H., Srinivasan, S., Spear, J. F., and Avadhani, N. G. (2006) Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J. Biol. Chem. 281, 2061-2070
45. Jiang, Y., Walker, R. J., Kern, T. S., and Steinle, J. J. (2010) Application of isoproterenol inhibits diabetic-like changes in the rat retina. Exp. Eye Res. 91, 171-179
46. Steinle, J. J., Chin, V. C., Williams, K. P., and Panjala, S. R. (2008) Beta-adrenergic receptor stimulation modulates iNOS protein levels through p38 and ERK1/2 signaling in human retinal en-dothelial cells. Exp. Eye Res. 87, 30-34
47. Walker, R. J., and Steinle, J. J. (2007) Role of beta-adrenergic receptors in inflammatory marker expression in Müller cells. Invest. Ophthalmol. Vis. Sci. 48, 5276-5281
48. Jiang, Y., and Steinle, J. J. (2010) Systemic propranolol reduces b-wave amplitude in the ERG and increases IGF-1 receptor phosphorylation in rat retina. Invest. Ophthalmol. Vis. Sci. 51, 2730-2735
49. Jiang, Y., Zhang, Q., Liu, L., Tang, J., Kern, T. S., and Steinle, J. J. (2013) b2-adrenergic receptor knockout mice exhibit A diabetic retinopathy phenotype. PLoS ONE 8, e70555
50. Kusari, J., Zhou, S. X., Padillo, E., Clarke, K. G., and Gil, D. W. (2010) Inhibition of vitreoretinal VEGF elevation and bloodretinal barrier breakdown in streptozotocin-induced diabetic rats by brimonidine. Invest. Ophthalmol. Vis. Sci. 51, 1044-1051
51. Hadjiconstantinou, M., Qu, Z. X., Moroi-Fetters, S. E., and Neff, N. H. (1988) Apparent loss of Gi protein activity in the diabetic retina. Eur. J. Pharmacol. 149, 193-194
52. Livingstone, C., McLellan, A. R., McGregor, M. A., Wilson, A., Connell, J. M., Small, M., Milligan, G., Paterson, K. R., and Houslay, M. D. (1991) Altered G-protein expression and adeny-late cyclase activity in platelets of non-insulin-dependent diabetic (NIDDM) male subjects. Biochim. Biophys. Acta 1096, 127-133
53. Abbracchio, M. P., Cattabeni, F., Di Giulio, A. M., Finco, C., Paoletti, A. M., Tenconi, B., and Gorio, A. (1991) Early alterations of Gi/Go protein-dependent transductional processes in the retina of diabetic animals. J. Neurosci. Res. 29, 196-200
54. Descorbeth, M., and Anand-Srivastava, M. B. (2010) Role of oxidative stress in high-glucose- and diabetes-induced increased expression of Gq/11a proteins and associated signaling in vascular smooth muscle cells. Free Radic. Biol. Med. 49, 1395-1405
55. Li, Y., Lappas, G., and Anand-Srivastava, M. B. (2007) Role of oxidative stress in angiotensin II-induced enhanced expression of Gi (alpha) proteins and adenylyl cyclase signaling in A10 vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 292, H1922-H1930
56. Li, Y., Descorbeth, M., and Anand-Srivastava, M. B. (2008) Role of oxidative stress in high glucose-induced decreased expression of Gialpha proteins and adenylyl cyclase signaling in vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 294, H2845-H2854
57. Goraya, T. Y., Wilkins, P., Douglas, J. G., Zhou, J., and Berti-Mattera, L. N. (1995) Signal transduction alterations in peripheral nerves from streptozotocin-induced diabetic rats. J. Neurosci. Res. 41, 518-525
58. Kanwar, M., and Kowluru, R. A. (2008) Diabetes regulates small molecular weight G-protein, H-Ras, in the microvasculature of the retina: implication in the development of retinopathy. Microvasc. Res. 76, 189-193
59. Do Carmo Buonfiglio, D., Peliciari-Garcia, R. A., Do Amaral, F. G., Peres, R., Nogueira, T. C., Afeche, S. C., and Cipolla-Neto, J. (2011) Early-stage retinal melatonin synthesis impairment in streptozotocin-induced diabetic wistar rats. Invest. Ophthalmol. Vis. Sci. 52, 7416-7422
60. Chang, J. C., Ciaccio, P., Schroeder, P., Wright, L., Westwood, R., and Berg, A. L. (2014) Pathology and neurotoxicity in dogs after repeat dose exposure to a serotonin 5-HT1B inhibitor. J. Toxicol. Pathol. 27, 31-42
61. Gavras, I., and Gavras, H. (2001) Benefits and side effects of blood pressure lowering treatment: what was wrong with doxazosin in the ALLHAT? Curr. Control. Trials Cardiovasc. Med. 2, 257-259