Table of Contents Author Guidelines Submit a Manuscript
Erratum

An erratum for this article has been published. To view the erratum, please click here.

Journal of Diabetes Research
Volume 2014, Article ID 790902, 15 pages
http://dx.doi.org/10.1155/2014/790902
Research Article

Hyperglycemia Induces Toll-Like Receptor-2 and -4 Expression and Activity in Human Microvascular Retinal Endothelial Cells: Implications for Diabetic Retinopathy

1Laboratory for Atherosclerosis and Metabolic Research, Division of Endocrinology, Diabetes and Metabolism, Department of Pathology, University of California Davis Medical Center, Research Building 1, Room 3000, 4635 Second Avenue, Sacramento, CA 95817, USA
2Veterans Affairs Medical Center, Mather, CA 95655, USA

Received 31 October 2014; Accepted 10 December 2014; Published 31 December 2014

Academic Editor: Subrata Chakrabarti

Copyright © 2014 Uthra Rajamani and Ishwarlal Jialal. 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. D. A. Antonetti, A. J. Barber, S. K. Bronson et al., “Diabetic retinopathy: seeing beyond glucose-induced microvascular disease,” Diabetes, vol. 55, no. 9, pp. 2401–2411, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Cheung, P. Mitchell, and T. Y. Wong, “Diabetic retinopathy,” The Lancet, vol. 376, no. 9735, pp. 124–136, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. T. Schram, N. Chaturvedi, C. Schalkwijk et al., “Vascular risk factors and markers of endothelial function as determinants of inflammatory markers in type 1 diabetes: the EURODIAB prospective complications study,” Diabetes Care, vol. 26, no. 7, pp. 2165–2173, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. N. Shanmugam, M. A. Reddy, M. Guha, and R. Natarajan, “High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells,” Diabetes, vol. 52, no. 5, pp. 1256–1264, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Devaraj, N. Glaser, S. Griffen, J. Wang-Polagruto, E. Miguelino, and I. Jialal, “Increased monocytic activity and biomarkers of inflammation in patients with type 1 diabetes,” Diabetes, vol. 55, no. 3, pp. 774–779, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Devaraj, M. R. Dasu, and I. Jialal, “Diabetes is a proinflammatory state: a translational perspective,” Expert Review of Endocrinology & Metabolism, vol. 5, no. 1, pp. 19–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. M. V. van Hecke, J. M. Dekker, G. Nijpels et al., “Inflammation and endothelial dysfunction are associated with retinopathy: the Hoorn Study,” Diabetologia, vol. 48, no. 7, pp. 1300–1306, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. B. E. K. Klein, M. D. Knudtson, M. Y. Tsai, and R. Klein, “The relation of markers of inflammation and endothelial dysfunction to the prevalence and progression of diabetic retinopathy: wisconsin epidemiologic study of diabetic retinopathy,” Archives of Ophthalmology, vol. 127, no. 9, pp. 1175–1182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Tang and T. S. Kern, “Inflammation in diabetic retinopathy,” Progress in Retinal and Eye Research, vol. 30, no. 5, pp. 343–358, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Tarr, K. Kaul, M. Chopra, E. M. Kohner, and R. Chibber, “Pathophysiology of diabetic retinopathy,” ISRN Ophthalmology, vol. 2013, Article ID 343560, 13 pages, 2013. View at Publisher · View at Google Scholar
  11. S. Akira and K. Takeda, “Toll-like receptor signalling,” Nature Reviews Immunology, vol. 4, no. 7, pp. 499–511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Beutler, “Inferences, questions and possibilities in Toll-like receptor signalling,” Nature, vol. 430, no. 6996, pp. 257–263, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Devaraj, M. R. Dasu, J. Rockwood, W. Winter, S. C. Griffen, and I. Jialal, “Increased toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: further evidence of a proinflammatory state,” The Journal of Clinical Endocrinology & Metabolism, vol. 93, no. 2, pp. 578–583, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. M. R. Dasu, S. Devaraj, S. Park, and I. Jialal, “Increased Toll-Like Receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects,” Diabetes Care, vol. 33, no. 4, pp. 861–868, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. S. J. Creely, P. G. McTernan, C. M. Kusminski et al., “Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes,” American Journal of Physiology—Endocrinology and Metabolism, vol. 292, no. 3, pp. E740–E747, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. I. Jialal and H. Kaur, “The role of toll-like receptors in diabetes-induced inflammation: implications for vascular complications,” Current Diabetes Reports, vol. 12, no. 2, pp. 172–179, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. K. S. Michelsen, M. H. Wong, P. K. Shah et al., “Lack of toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 29, pp. 10679–10684, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. A. E. Mullick, P. S. Tobias, and L. K. Curtiss, “Modulation of atherosclerosis in mice by Toll-like receptor 2,” The Journal of Clinical Investigation, vol. 115, no. 11, pp. 3149–3156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Devaraj, I. Jialal, J.-M. Yun, and A. Bremer, “Demonstration of increased toll-like receptor 2 and toll-like receptor 4 expression in monocytes of type 1 diabetes mellitus patients with microvascular complications,” Metabolism: Clinical and Experimental, vol. 60, no. 2, pp. 256–259, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Devaraj, P. Tobias, B. S. Kasinath, R. Ramsamooj, A. Afify, and I. Jialal, “Knockout of toll-like receptor-2 attenuates both the proinflammatory state of diabetes and incipient diabetic nephropathy,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 8, pp. 1796–1804, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Lin, W. H. Yiu, H. J. Wu et al., “Toll-like receptor 4 promotes tubular inflammation in diabetic nephropathy,” Journal of the American Society of Nephrology, vol. 23, no. 1, pp. 86–102, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. M. R. Dasu, S. Devaraj, L. Zhao, D. H. Hwang, and I. Jialal, “High glucose induces toll-like receptor expression in human monocytes: mechanism of activation,” Diabetes, vol. 57, no. 11, pp. 3090–3098, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Jialal, B. A. Huet, H. Kaur, A. Chien, and S. Devaraj, “Increased toll-like receptor activity in patients with metabolic syndrome,” Diabetes Care, vol. 35, no. 4, pp. 900–904, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. S. K. Venugopal, S. Devaraj, I. Yuhanna, P. Shaul, and I. Jialal, “Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells,” Circulation, vol. 106, no. 12, pp. 1439–1441, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Matsunaga, N. Tsuchimori, T. Matsumoto, and M. Ii, “TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules,” Molecular Pharmacology, vol. 79, no. 1, pp. 34–41, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Takashima, N. Matsunaga, M. Yoshimatsu et al., “Analysis of binding site for the novel small-molecule TLR4 signal transduction inhibitor TAK-242 and its therapeutic effect on mouse sepsis model,” British Journal of Pharmacology, vol. 157, no. 7, pp. 1250–1262, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. L. A. Couture, W. Piao, L. W. Ru, S. N. Vogel, and V. Y. Toshchakov, “Targeting toll-like receptor (TLR) signaling by toll/interleukin-1 receptor (TIR) domain-containing adapter protein/MyD88 adapter-like (TIRAP/Mal)-derived decoy peptides,” Journal of Biological Chemistry, vol. 287, no. 29, pp. 24641–24648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. 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. View at Publisher · View at Google Scholar · View at Scopus
  29. M. K. Mathews, C. Merges, D. S. McLeod, and G. A. Lutty, “Vascular endothelial growth factor and vascular permeability changes in human diabetic retinopathy,” Investigative Ophthalmology and Visual Science, vol. 38, no. 13, pp. 2729–2741, 1997. View at Google Scholar · View at Scopus
  30. T. Hikichi, N. Fujio, J. Akiba, Y. Azuma, M. Takahashi, and A. Yoshida, “Association between the short-term natural history of diabetic macular edema and the vitreomacular relationship in type II diabetes mellitus,” Ophthalmology, vol. 104, no. 3, pp. 473–478, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Canataroglu, I. Varinli, A. A. Ozcan, A. Canataroglu, F. Doran, and S. Varinli, “Interleukin (IL)-6, interleukin (IL)-8 levels and cellular composition of the vitreous humor in proliferative diabetic retinopathy, proliferative vitreoretinopathy, and traumatic proliferative vitreoretinopathy,” Ocular Immunology and Inflammation, vol. 13, no. 5, pp. 375–381, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Schroder, W. Palinski, and G. W. Schmid-Schonbein, “Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy,” American Journal of Pathology, vol. 139, no. 1, pp. 81–100, 1991. View at Google Scholar · View at Scopus
  33. A. D. Meleth, E. Agrón, C.-C. Chan et al., “Serum inflammatory markers in diabetic retinopathy,” Investigative Ophthalmology and Visual Science, vol. 46, no. 11, pp. 4295–4301, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. A. M. Joussen, V. Poulaki, M. L. Le et al., “A central role for inflammation in the pathogenesis of diabetic retinopathy,” The FASEB Journal, vol. 18, no. 12, pp. 1450–1452, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Kaur, A. Chien, and I. Jialal, “Hyperglycemia induces toll like receptor 4 expression and activity in mouse mesangial cells: Relevance to diabetic nephropathy,” The American Journal of Physiology—Renal Physiology, vol. 303, no. 8, pp. F1145–F1150, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. J.-X. Chen and A. Stinnett, “Critical role of the NADPH oxidase subunit p47phox on vascular TLR expression and neointimal lesion formation in high-fat diet-induced obesity,” Laboratory Investigation, vol. 88, no. 12, pp. 1316–1328, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. R. A. Kowluru and S. N. Abbas, “Diabetes-induced mitochondrial dysfunction in the retina,” Investigative Ophthalmology and Visual Science, vol. 44, no. 12, pp. 5327–5334, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. R. A. Kowluru, J. Tang, and T. S. Kern, “Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy,” Diabetes, vol. 50, no. 8, pp. 1938–1942, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. T. S. Kern, R. A. Kowluru, and R. L. Engerman, “Abnormalities of retinal metabolism in diabetes or galactosemia: ATPases and glutathione,” Investigative Ophthalmology & Visual Science, vol. 35, no. 7, pp. 2962–2967, 1994. View at Google Scholar · View at Scopus
  40. S. Z. Safi, R. Qvist, G. O. Yan, and I. S. Ismail, “Differential expression and role of hyperglycemia induced oxidative stress in epigenetic regulation of β1, β2 and β3-adrenergic receptors in retinal endothelial cells,” Acta Veterinaria Scandinavica, vol. 7, article 29, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. J. V. Busik, S. Mohr, and M. B. Grant, “Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators,” Diabetes, vol. 57, no. 7, pp. 1952–1965, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Miyamoto, S. Khosrof, S.-E. Bursell et al., “Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10836–10841, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. N. N. Vagaja, N. Binz, S. McLenachan, E. P. Rakoczy, and P. G. McMenamin, “Influence of endotoxin-mediated retinal inflammation on phenotype of diabetic retinopathy in Ins2Akita mice,” British Journal of Ophthalmology, vol. 97, no. 10, pp. 1343–1350, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Devaraj, P. Tobias, and I. Jialal, “Knockout of toll-like receptor-4 attenuates the pro-inflammatory state of diabetes,” Cytokine, vol. 55, no. 3, pp. 441–445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Dvoriantchikova, D. J. Barakat, E. Hernandez, V. I. Shestopalov, and D. Ivanov, “Toll-like receptor 4 contributes to retinal ischemia/reperfusion injury,” Molecular Vision, vol. 16, pp. 1907–1912, 2010. View at Google Scholar · View at Scopus
  46. J. Tang, C. Allen Lee, Y. Du et al., “MyD88-dependent pathways in leukocytes affect the retina in diabetes,” PLoS ONE, vol. 8, no. 7, Article ID e68871, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Ma, H. Wu, C. Y. Zhao, U. Panchapakesan, C. Pollock, and S. J. Chadban, “Requirement for TLR2 in the development of albuminuria, inflammation and fibrosis in experimental diabetic nephropathy,” International Journal of Clinical and Experimental Pathology, vol. 7, no. 2, pp. 481–495, 2014. View at Google Scholar · View at Scopus
  48. A. Taye, A. H. Saad, A. H. Kumar, and H. Morawietz, “Effect of apocynin on NADPH oxidase-mediated oxidative stress-LOX-1-eNOS pathway in human endothelial cells exposed to high glucose,” European Journal of Pharmacology, vol. 627, no. 1–3, pp. 42–48, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. M. R. Dasu, S. Devaraj, and I. Jialal, “High glucose induces IL-1β expression in human monocytes: mechanistic insights,” American Journal of Physiology—Endocrinology and Metabolism, vol. 293, no. 1, pp. E337–E346, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. V. Thallas-Bonke, S. R. Thorpe, M. T. Coughlan et al., “Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-α-dependent pathway,” Diabetes, vol. 57, no. 2, pp. 460–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Morigi, S. Angioletti, B. Imberti et al., “Leukocyte-endothelial interaction is augmented by high glucose concentrations and hyperglycemia in a NF-kB-dependent fashion,” Journal of Clinical Investigation, vol. 101, no. 9, pp. 1905–1915, 1998. View at Publisher · View at Google Scholar · View at Scopus