Renal protective effects of toll-like receptor 4 signaling blockade in type 2 diabetic mice

Endocrinology

Volumn 154, Issue 6, 2013, Pages 2144-2155

  Cha, J J ^a   Hyun, Y Y ^b   Lee, M H ^a   Kim, J E ^a   Nam, D H ^a   Song, H K ^a   Kang, Y S ^a   Lee, J E ^c   Kim, H W ^c   Han, J Y ^d   Cha, Dae Ryong ^a  

^a Korea University   (South Korea)

^b Sungkyunkwan University   (South Korea)

^c Wonkwang University   (South Korea)

^d Inha University Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

3 PHENYL 4,5 DIHYDRO 5 ISOXASOLE ACETIC ACID; ACETIC ACID; ALBUMIN; GLUCOSE; LIPID; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FOOD INTAKE; GLOMERULOSCLEROSIS; GLYCEMIC CONTROL; INSULIN TOLERANCE TEST; LIPID METABOLISM; MACROPHAGE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PODOCYTE; PRIORITY JOURNAL; RENAL PROTECTION;

3T3-L1 CELLS; ACETATES; ADIPOCYTES; ALBUMINURIA; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, TYPE 2; FATTY ACIDS, NONESTERIFIED; GENE EXPRESSION; GLUCOSE; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; KIDNEY; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; OXAZOLES; PODOCYTES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84878446398     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2080     Document Type: Article

References (50)

1. Spranger J, Kroke A, Möhlig M, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes . 2003;52:812-817. (Pubitemid 36323590)
2. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286:327-334. (Pubitemid 32656163)
3. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11:98-107.
4. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol. 2001;2:675-680. (Pubitemid 32747155)
5. Kawai T, Akira S. TLR signaling. Semin Immunol. 2007;19:24-32. (Pubitemid 46498752)
6. Kawai T, Akira S. Signaling to NF-κB by Toll-like receptors. Trends Mol Med. 2007;13:460-469.
7. Dasu MR, Devaraj S, Zhao L, Hwang DH, Jialal I. High glucose induces toll-like receptor expression in human monocytes: mechanism of activation. Diabetes. 2008;57:3090-3098.
8. Dasu MR, Jialal I. Free fatty acids in the presence of high glucose amplify monocyte inflammation via Toll-like receptors. Am J Physiol Endocrinol Metab. 2011;300:E145-E154.
9. Song MJ, Kim KH, Yoon JM, Kim JB. Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Biochem Biophys Res Commun. 2006;346:739-745.
10. Devaraj S, Dasu MR, Rockwood J, Winter W, Griffen SC, Jialal I. Increased toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: further evidence of a proinflammatory state. J Clin Endocrinol Metab. 2008;93:578-583. (Pubitemid 351240834)
11. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116:3015-3025. (Pubitemid 44684486)
12. Vitseva OI, Tanriverdi K, Tchkonia TT, et al. Inducible Toll-like receptor and NF-κB regulatory pathway expression in human adipose tissue. Obesity (Silver Spring). 2008;16:932-937. (Pubitemid 351620468)
13. Froy O, Hananel A, Chapnik N, Madar Z. Differential effect of insulin treatment on decreased levels of β-defensins and Toll-like receptors in diabetic rats. Mol Immunol. 2007;44:796-802. (Pubitemid 44415013)
14. Tuttle KR. Linking metabolism and immunology: diabetic nephropathy is an inflammatory disease. J AmSoc Nephrol. 2005;16:1537-1538. (Pubitemid 41716459)
15. Ziyadeh FN, Wolf G. Pathogenesis of the podocytopathy and proteinuria in diabetic glomerulopathy. Curr Diabetes Rev. 2008;4:39-45. (Pubitemid 351210971)
16. Navarro-González JF, Mora-Fernández C. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol. 2008;19:433-442. (Pubitemid 351355386)
17. Wu H, Chen G, Wyburn KR, et al. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest . 2007;117:2847-2859. (Pubitemid 47529615)
18. Cunningham PN, Wang Y, Guo R, He G, Quigg RJ. Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol. 2004;172:2629-2635. (Pubitemid 38182415)
19. Goldstein DR, Tesar BM, Akira S, Lakkis FG. Critical role of the Toll-like receptor signal adaptor protein MyD88 in acute allograft rejection. J Clin Invest. 2003;111:1571-1578. (Pubitemid 38063290)
20. Liu B, Yang Y, Dai J, et al. TLR4 up-regulation at protein or gene level is pathogenic for lupus-like autoimmune disease. J Immunol. 2006;177:6880-6888. (Pubitemid 44715053)
21. Brown HJ, Lock HR, Wolfs TG, Buurman WA, Sacks SH, Robson MG. Toll-like receptor 4 ligation on intrinsic renal cells contributes to the induction of antibody-mediated glomerulonephritis via CXCL1 and CXCL2. J Am Soc Nephrol. 2007;18:1732-1739. (Pubitemid 46870310)
22. Papadimitraki ED, Tzardi M, Bertsias G, Sotsiou E, Boumpas DT. Glomerular expression of toll-like receptor-9 in lupus nephritis but not in normal kidneys: implications for the amplification of the inflammatory response. Lupus. 2009;18:831-835.
23. Stosic-Grujicic S, Cvetkovic I, Mangano K, et al. A potent immunomodulatory compound, (S,R)-3-Phenyl-4,5-dihydro-5-isoxazole acetic acid, prevents spontaneous and accelerated forms of autoimmune diabetes in NOD mice and inhibits the immunoinflammatory diabetes induced by multiple low doses of streptozotocin in CBA/H mice. J Pharmacol Exp Ther. 2007;320:1038-1049. (Pubitemid 46294054)
24. Stojanovic I, Cuzzocrea S, Mangano K, et al. In vitro, ex vivo and in vivo immunopharmacological activities of the isoxazoline compound VGX-1027: modulation of cytokine synthesis and prevention of both organ-specific and systemic autoimmune diseases in murine models. Clin Immunol. 2007;123:311-323. (Pubitemid 46824126)
25. Mangano K, Sardesai N, D'Alcamo M, et al. In vitro inhibition of enterobacteria-reactive CD4+ CD25- T cells and suppression of immunoinflammatory colitis in mice by the novel immunomodulatory agent VGX-1027. Eur J Pharmacol . 2008;586:313-321.
26. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37:911-917.
27. Lee MH, Song HK, Ko GJ, et al. Angiotensin receptor blockers improve insulin resistance in type 2 diabetic rats by modulating adipose tissue. Kidney Int. 2008;74:890-900.
28. Han SY, Kang YS, Jee YH, et al. High glucose and angiotensin II increase β1 integrin and integrin-linked kinase synthesis in cultured mouse podocytes. Cell Tissue Res. 2006;323:321-332. (Pubitemid 43100273)
29. Fasshauer M, Klein J, Neumann S, Eszlinger M, Paschke R. Isoproterenol inhibits resistin gene expression through a G(S)-protein-coupled pathway in 3T3-L1 adipocytes. FEBS letters . 2001;500:60-63. (Pubitemid 32575319)
30. Sieber J, Lindenmeyer MT, Kampe K, et al. Regulation of podocyte survival and endoplasmic reticulum stress by fatty acids. Am J Physiol Renal Physiol. 2010;299:F821-F829.
31. Baker RG, Hayden MS, Ghosh S. NF-κB, inflammation, and metabolic disease. Cell Metab. 2011;13:11-22.
32. Dobrovolskaia MA, Medvedev AE, Thomas KE, et al. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-κ B signaling pathway components. J Immunol. 2003;170:508-519. (Pubitemid 36026178)
33. Dasu MR, Jialal I. Free fatty acids in the presence of high glucose amplify monocyte inflammation via Toll-like receptors. Am J Physiol Endocrinol Metab. 2011;300:E145-E154.
34. Muzio M, Bosisio D, Polentarutti N, et al. Differential expression and regulation of Toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol. 2000;164:5998-6004. (Pubitemid 30389848)
35. Kaur H, Chien A, Jialal I. Hyperglycemia induces Toll like receptor 4 expression and activity in mouse mesangial cells: relevance to diabetic nephropathy. Am J Physiol Renal Physiol. 2012;303:F1145-F1150.
36. Dasu MR, Devaraj S, Park S, Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care. 2010;33:861-868.
37. 1 in patients with chronic kidney disease. Nephron Clin Pract. 2011;119:c97-c104.
38. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci USA. 2009;106:14385-14390.
39. Coward RJ, Welsh GI, Yang J. The human glomerular podocyte is a novel target for insulin action. Diabetes . 2005;54:3095-3102. (Pubitemid 43334361)
40. Mayrhofer C, Krieger S, Huttary N, et al. Alterations in fatty acid utilization and an impaired antioxidant defense mechanism are early events in podocyte injury: a proteomic analysis. Am J Pathol. 2009;174:1191-1202.
41. Sieber J, Lindenmeyer MT, Kampe K, et al. Regulation of podocyte survival and endoplasmic reticulum stress by fatty acids. Am J Physiol Renal Physiol. 2010;299:F821-F829.
42. Lennon R, Pons D, Sabin MA, et al. Saturated fatty acids induce insulin resistance in human podocytes: implications for diabetic nephropathy. Nephrol Dial Transplant. 2009;24:3288-3296.
43. Motojima M, Matsusaka T, Kon V, Ichikawa I. Fibrinogen that appears in Bowman's space of proteinuric kidneys in vivo activates podocyte Toll-like receptors 2 and 4 in vitro. Nephron Exp Nephrol. 2010;114:e39-e47.
44. Banas MC, Banas B, Hudkins KL, et al. TLR4 links podocytes with the innate immune system to mediate glomerular injury. J Am Soc Nephrol. 2008;19:704-713.
45. Reiser J, von Gersdorff G, Loos M, et al. Induction of B7-1 in podocytes is associated with nephrotic syndrome. J Clin Invest. 2004;113:1390-1397. (Pubitemid 39071694)
46. Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, et al. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes . 2007;56:1986-1998. (Pubitemid 47195825)
47. Saberi M, Woods NB, de Luca C, et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 2009;10:419-429.
48. Lin M, Yiu WH, Wu HJ, et al. Toll-like receptor 4 promotes tubular inflammation in diabetic nephropathy. J Am Soc Nephrol. 2012;23:86-102.
49. Zuany-Amorim C, Hastewell J, Walker C. Toll-like receptors as potential therapeutic targets for multiple diseases. Nat Rev Drug Discov. 2002;1:797-807. (Pubitemid 37361563)
50. Clanchy FI, Sacre SM. Modulation of toll-like receptor function has therapeutic potential in autoimmune disease. Expert Opin Biol Ther. 2010;10:1703-1716.