Retinopathy in a novel model of metabolic syndrome and type 2 diabetes: New insight on the inflammatory paradigm

FASEB Journal

Volumn 28, Issue 5, 2014, Pages 2038-2046

  Noda, Kousuke ^a,c   Nakao, Shintaro ^a,b,d   Zandi, Souska ^a,b   Sun, Dawei ^a,b,e   Hayes, K C ^f   Hafezi Moghadam, Ali ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e THE SECOND AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

^f BRANDEIS UNIVERSITY   (United States)

Author keywords

Adhesion molecules; Adipokines; Nile grass rat

Indexed keywords

ADIPONECTIN; CHOLESTEROL; CONCANAVALIN A; HEMOGLOBIN A1C; INSULIN; INTERCELLULAR ADHESION MOLECULE 1; LEPTIN; TRIACYLGLYCEROL; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD RETINA BARRIER; BLOOD VESSEL PERMEABILITY; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE COURSE; ENDOTHELIUM CELL; ERYTHROCYTE; INSULIN BLOOD LEVEL; LEUKOCYTE; LEUKOCYTE ADHERENCE; MALE; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA ARTERY; RETINA BLOOD VESSEL; RETINITIS; TRIACYLGLYCEROL BLOOD LEVEL;

ADHESION MOLECULES; ADIPOKINES; NILE GRASS RAT;

ADIPONECTIN; ANIMALS; BLOOD-RETINAL BARRIER; CELL ADHESION; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2; DIABETIC RETINOPATHY; DISEASE MODELS, ANIMAL; FEMALE; HEMOGLOBIN A, GLYCOSYLATED; INFLAMMATION; INSULIN; INTERCELLULAR ADHESION MOLECULE-1; LEPTIN; LEUKOCYTES; LIPIDS; MALE; METABOLIC SYNDROME X; RATS; RETINA; RETINAL VESSELS; STREPTOZOCIN; TRIGLYCERIDES; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84901020487     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-215715     Document Type: Article

References (40)

1. Biddinger, S. B., and Kahn, C. R. (2006) From mice to men: insights into the insulin resistance syndromes. Annu. Rev. Physiol. 68, 123-158
2. Gesta, S., Tseng, Y. H., and Kahn, C. R. (2007) Developmental origin of fat: tracking obesity to its source. Cell 131, 242
3. Reaven, G. (2004) The metabolic syndrome or the insulin resistance syndrome?-different names, different concepts, and different goals. Endocrinol. Metab. Clin. North. Am. 33, 283-303
4. Mizutani, M., Kern, T. S., and Lorenzi, M. (1996) Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J. Clin. Invest. 97, 2883-2890
5. Antonetti, D. A., Barber, A. J., Bronson, S. K., Freeman, W. M., Gardner, T. W., Jefferson, L. S., Kester, M., Kimball, S. R., Krady, J. K., LaNoue, K. F., Norbury, C. C., Quinn, P. G., Sandirasegarane, L., and Simpson, I. A. (2006) Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 55, 2401-2411
6. Coleman, D. L., and Hummel, K. P. (1973) The influence of genetic background on the expression of the obese (Ob) gene in the mouse. Diabetologia 9, 287-293
7. Dulin, W. E., and Wyse, B. M. (1970) Diabetes in the KK mouse. Diabetologia 6, 317-323
8. Coleman, D. L., and Hummel, K. P. (1974) Hyperinsulinemia in pre-weaning diabetes (db) mice. Diabetologia 10(Suppl), 607-610
9. Portha, B., Serradas, P., Bailbe, D., Suzuki, K., Goto, Y., and Giroix, M. H. (1991) Beta-cell insensitivity to glucose in the GK rat, a spontaneous nonobese model for type II diabetes. Diabetes 40, 486-491
10. Ikeda, H., Shino, A., Matsuo, T., Iwatsuka, H., and Suzuoki, Z. (1981) A new genetically obese-hyperglycemic rat (Wistar fatty). Diabetes 30, 1045-1050
11. Kawano, K., Hirashima, T., Mori, S., Saitoh, Y., Kurosumi, M., and Natori, T. (1992) Spontaneous long-term hyperglycemic rat with diabetic complications: Otsuka Long-Evans Tokushima Fatty (OLETF) strain. Diabetes 41, 1422-1428
12. Sasase, T., Ohta, T., Ogawa, N., Miyajima, K., Ito, M., Yamamoto, H., Morinaga, H., and Matsushita, M. (2006) Preventive effects of glycaemic control on ocular complications of spontaneously diabetic Torii rat. Diabetes Obes. Metab. 8, 501-507
13. Robertson, R. P., Gavareski, D. J., Henderson, J. D., Porte, D., Jr., and Bierman, E. L. (1973) Accelerated triglyceride secretion: a metabolic consequence of obesity. J. Clin. Invest. 52, 1620-1626
14. Schroder, S., Palinski, W., and Schmid-Schonbein, G. W. (1991) Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy. Am. J. Pathol. 139, 81-100
15. Miyamoto, K., Hiroshiba, N., Tsujikawa, A., and Ogura, Y. (1998) In vivo demonstration of increased leukocyte entrapment in retinal microcirculation of diabetic rats. Invest. Ophthalmol. Vis. Sci. 39, 2190-2194
16. Barouch, F. C., Miyamoto, K., Allport, J. R., Fujita, K., Bursell, S. E., Aiello, L. P., Luscinskas, F. W., and Adamis, A. P. (2000) Integrin-mediated neutrophil adhesion and retinal leukostasis in diabetes. Invest. Ophthalmol. Vis. Sci. 41, 1153-1158
17. Miyamoto, K., Khosrof, S., Bursell, S. E., Rohan, R., Murata, T., Clermont, A. C., Aiello, L. P., Ogura, Y., and Adamis, A. P. (1999) Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc. Natl. Acad. Sci. U. S. A. 96, 10836-10841
18. McLeod, D. S., Lefer, D. J., Merges, C., and Lutty, G. A. (1995) Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am. J. Pathol. 147, 642-653
19. Hughes, J. M., Brink, A., Witmer, A. N., Hanraads-de Riemer, M., Klaassen, I., and Schlingemann, R. O. (2004) Vascular leucocyte adhesion molecules unaltered in the human retina in diabetes. Br. J. Ophthalmol. 88, 566-572
20. Noda, K., Melhorn, M. I., Zandi, S., Frimmel, S., Tayyari, F., Hisatomi, T., Almulki, L., Pronczuk, A., Hayes, K. C., and Hafezi-Moghadam, A. (2010) An animal model of spontaneous metabolic syndrome: Nile grass rat. FASEB J. 24, 2443-2453
21. Chen, W., Jump, D. B., Grant, M. B., Esselman, W. J., and Busik, J. V. (2003) Dyslipidemia, but not hyperglycemia, induces inflammatory adhesion molecules in human retinal vascular endothelial cells. Invest. Ophthalmol. Vis. Sci. 44, 5016-5022
22. Taylor, P. D., Wickenden, A. D., Mirrlees, D. J., and Poston, L. (1994) Endothelial function in the isolated perfused mesentery and aortae of rats with streptozotocin-induced diabetes: effect of treatment with the aldose reductase inhibitor, ponalrestat. Br. J. Pharmacol. 111, 42-48
23. Miyahara, S., Kiryu, J., Yamashiro, K., Miyamoto, K., Hirose, F., Tamura, H., Katsuta, H., Nishijima, K., Tsujikawa, A., and Honda, Y. (2004) Simvastatin inhibits leukocyte accumulation and vascular permeability in the retinas of rats with streptozotocin-induced diabetes. Am. J. Pathol. 164, 1697-1706
24. Jariyapongskul, A., Patumraj, S., and Niimi, H. (2003) Cerebral endothelial dysfunction in diabetes: intravital microscopic analysis using streptozotocin-induced diabetic rats. Clin. Hemorheol. Microcirc. 29, 331-335
25. Nguyen, T. T., and Wong, T. Y. (2009) Retinal vascular changes and diabetic retinopathy. Curr. Diab. Rep. 9, 277-283
26. Chaabo, F., Pronczuk, A., Maslova, E., and Hayes, K. (2010) Nutritional correlates and dynamics of diabetes in the Nile rat (Arvicanthis niloticus): a novel model for diet-induced type 2 diabetes and the metabolic syndrome. Nutr. Metab. (Lond.) 7, 29
27. Bolsinger, J., Pronczuk, A., and Hayes, K. C. (2013) Dietary carbohydrate dictates development of type 2 diabetes in the Nile rat. J. Nutr. Biochem. 24, 1945-1952
28. Skondra, D., Noda, K., Almulki, L., Tayyari, F., Frimmel, S., Nakazawa, T., Kim, I. K., Zandi, S., Thomas, K. L., Miller, J. W., Gragoudas, E. S., and Hafezi-Moghadam, A. (2008) Characterization of azurocidin as a permeability factor in the retina: involvement in VEGF-induced and early diabetic blood-retinal barrier breakdown. Invest. Ophthalmol. Vis. Sci. 49, 726-731
29. Sasongko, M. B., Wong, T. Y., Nguyen, T. T., Cheung, C. Y., Shaw, J. E., and Wang, J. J. (2011) Retinal vascular tortuosity in persons with diabetes and diabetic retinopathy. Diabetologia 54, 2409-2416
30. Hammes, H. P., Lin, J., Renner, O., Shani, M., Lundqvist, A., Betsholtz, C., Brownlee, M., and Deutsch, U. (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51, 3107-3112
31. Amos, A. F., McCarty, D. J., and Zimmet, P. (1997) The rising global burden of diabetes and its complications: estimates and projections to the year 2010. Diabet. Med. 14(Suppl. 5), S1-S85
32. Adamis, A. P. (2002) Is diabetic retinopathy an inflammatory disease? Br. J. Ophthalmol. 86, 363-365
33. Masuda, M., Murakami, T., Egawa, H., and Murata, K. (1990) Decreased fluidity of polymorphonuclear leukocyte membrane in streptozocin-induced diabetic rats. Diabetes 39, 466-470
34. Garmy-Susini, B., Jin, H., Zhu, Y., Sung, R. J., Hwang, R., and Varner, J. (2005) Integrin alpha4beta1-VCAM-1-mediated adhesion between endothelial and mural cells is required for blood vessel maturation. J. Clin. Invest. 115, 1542-1551
35. Hafezi-Moghadam, A., Noda, K., Almulki, L., Iliaki, E. F., Poulaki, V., Thomas, K. L., Nakazawa, T., Hisatomi, T., Miller, J. W., and Gragoudas, E. S. (2007) VLA-4 blockade suppresses endotoxin-induced uveitis: in vivo evidence for functional integrin up-regulation. FASEB J. 21, 464-474
36. Ishida, S., Usui, T., Yamashiro, K., Kaji, Y., Ahmed, E., Carrasquillo, K. G., Amano, S., Hida, T., Oguchi, Y., and Adamis, A. P. (2003) VEGF164 is proinflammatory in the diabetic retina. Invest. Ophthalmol. Vis. Sci. 44, 2155-2162
37. Serhan, C. N., Chiang, N., and Van Dyke, T. E. (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361
38. Chen, H., Charlat, O., Tartaglia, L. A., Woolf, E. A., Weng, X., Ellis, S. J., Lakey, N. D., Culpepper, J., Moore, K. J., Breitbart, R. E., Duyk, G. M., Tepper, R. I., and Morgenstern, J. P. (1996) Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84, 491-495
39. Faggioni, R., Feingold, K. R., and Grunfeld, C. (2001) Leptin regulation of the immune response and the immunodeficiency of malnutrition. FASEB J. 15, 2565-2571
40. Hammes, H. P., Feng, Y., Pfister, F., and Brownlee, M. (2011) Diabetic retinopathy: targeting vasoregression. Diabetes 60, 9-16