Toll-like receptors and diabetes complications: Recent advances

Current Diabetes Reviews

Volumn 8, Issue 6, 2012, Pages 480-488

  Ramirez, Sandra Rosa ^a   Dasu, Mohan Ravi Krishna ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atherosclerosis; Diabetes mellitus; Inflammation; Nephropathy; Neuropathy; Tlr2; Tlr4; Wound healing

Indexed keywords

BETA DEFENSIN 3; INTERLEUKIN 1BETA; LOW DENSITY LIPOPROTEIN; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHATIDYLINOSITOL 3 KINASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ATHEROSCLEROSIS; CYTOKINE RELEASE; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DISEASE SEVERITY; GENETIC PREDISPOSITION; HUMAN; HYPERGLYCEMIA; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; LEG AMPUTATION; NEUROPATHIC PAIN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; WOUND HEALING;

AMPUTATION; ANIMALS; ATHEROSCLEROSIS; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; IMMUNITY, INNATE; INFLAMMATION; MALE; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; UNITED STATES; WOUND HEALING;

EID: 84870215981     PISSN: 15733998     EISSN: 18756417     Source Type: Journal    
DOI: 10.2174/157339912803529887     Document Type: Article

References (99)

1. Center for Disease Control. National diabetes fact sheet: national estimates and general information on diabetes and pre-diabetes in the United States. Atlanta (GA): U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2011.
2. ShlomoMelmed KSP, P. Reed Larsen, and Henry M. Kronenberg. Williams Textbook of Endocrinology. Philadelphia, PA Elsevier; 2011.
3. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res ClinPract. 2010; 87(1): 4-14
4. Tisch R, McDevitt H. Insulin-dependent diabetes mellitus. Cell. 1996; 85(3): 291-7
5. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006; 124(4): 783-801.
6. O'Neill LA. How Toll-like receptors signal: what we know and what we don't know. Curr Opin in Immunol. 2006; 18(1): 3-9.
7. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004; 4(7): 499-511.
8. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol. 2004; 5(10): 987-95.
9. Pasare C, Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med and Biol. 2005; 560: 11-8.
10. Hoebe K, Janssen E, Beutler B. The interface between innate and adaptive immunity. Nat Immunol. 2004; 5(10): 971-4.
11. Tsan MF, Gao B. Endogenous ligands of Toll-like receptors. J Leukoc Biol. 2004; 76(3): 514-9.
12. Arora P, Garcia-Bailo B, Dastani Z, et al. Genetic polymorphisms of innate immunity-related inflammatory pathways and their association with factors related to type 2 diabetes. BMC Med Genet. 2011; 12: 95.
13. El-Omar EM, Ng MT, Hold GL. Polymorphisms in Toll-like receptor genes and risk of cancer. Oncogene. 2008; 27(2): 244-52.
14. Schroder NW, Schumann RR. Single nucleotide polymorphisms of Toll-like receptors and susceptibility to infectious disease. Lancet Infect Dis. 2005; 5(3): 156-64.
15. BoraskaJelavic T, Barisic M, DrmicHofman I, et al. Microsatelite GT polymorphism in the toll-like receptor 2 is associated with colorectal cancer. Clin Genet. 2006; 70(2): 156-60.
16. Eder W, Klimecki W, Yu L, et al. Toll-like receptor 2 as a major gene for asthma in children of European farmers. J Allergy-ClinImmunol. 2004; 113(3): 482-8.
17. Radstake TR, Franke B, Hanssen S, et al. The Toll-like receptor 4 Asp299Gly functional variant is associated with decreased rheumatoid arthritis disease susceptibility but does not influence disease severity and/or outcome. Arthritis and Rheum. 2004; 50(3): 999-1001.
18. Kutner NG, Johansen KL, Zhang R, Huang Y, Amaral S. Perspectives on the New Kidney Disease Education Benefit: Early Awareness, Race and Kidney Transplant Access in a USRDS Study. Am j Transplant. 2012; 4; 1017-23
19. Caramori ML, Kim Y, Huang C, et al. Cellular basis of diabetic nephropathy: 1. Study design and renal structural-functional relationships in patients with long-standing type 1 diabetes. Diabetes. 2002; 51(2): 506-13.
20. Jefferson JA, Shankland SJ, Pichler RH. Proteinuria in diabetic kidney disease: a mechanistic viewpoint. Kidney Int. 2008; 74(1): 22-36.
21. Osterby R, Gundersen HJ. Glomerular size and structure in diabetes mellitus. I. Early abnormalities. Diabetologia. 1975; 11(3): 225-9.
22. Toyoda M, Najafian B, Kim Y, Caramori ML, Mauer M. Podocyte detachment and reduced glomerular capillary endothelial fenestration in human type 1 diabetic nephropathy. Diabetes. 2007; 56(8): 2155-60.
23. Mauer SM. Structural-functional correlations of diabetic nephropathy. Kidney Int. 1994; 45(2): 612-22.
24. Steffes MW, Bilous RW, Sutherland DE, Mauer SM. Cell and matrix components of the glomerular mesangium in type I diabetes. Diabetes. 1992; 41(6): 679-84.
25. Giorgini A, Brown HJ, Sacks SH, Robson MG. Toll-like receptor 4 stimulation triggers crescentic glomerulonephritis by multiple mechanisms including a direct effect on renal cells. Am J Pathol. 2010; 177(2): 644-53.
26. Mezzano S, Aros C, Droguett A, et al. NF-kappaB activation and overexpression of regulated genes in human diabetic nephropathy. Nephrol Dial Transplant. 2004; 19(10): 2505-12.
27. Li F, Yang N, Zhang L, et al. Increased expression of toll-like receptor 2 in rat diabetic nephropathy. Am J Nephrol. 2010; 32(2): 179-86.
28. Brown HJ, Lock HR, Sacks SH, Robson MG. TLR2 stimulation of intrinsic renal cells in the induction of immune-mediated glomerulonephritis. J Immunol. 2006; 177(3): 1925-31.
29. Devaraj S, Tobias P, Kasinath BS, Ramsamooj R, Afify A, Jialal I. Knockout of toll-like receptor-2 attenuates both the proinflammatory state of diabetes and incipient diabetic nephropathy. Arterioscler, Thromb, and Vasc Biol. 2011; 31(8): 1796-804.
30. Lin M, Yiu WH, Wu HJ, et al. Toll-like receptor 4 promotes tubular inflammation in diabetic nephropathy. J Am Soc Nephrol. 2012; 23(1): 86-102.
31. Tang SC, Leung JC, Lai KN. Diabetic tubulopathy: an emerging entity. Cont Nephrol. 2011; 170: 124-34.
32. Rudofsky G, Jr., Reismann P, Witte S, et al. Asp299Gly and Thr399Ile genotypes of the TLR4 gene are associated with a reduced prevalence of diabetic neuropathy in patients with type 2 diabetes. Diabetes Care. 2004; 27(1): 179-83.
33. Nishizawa T, Bornfeldt KE. Diabetic vascular disease and the potential role of macrophage glucose metabolism. Ann Med.2011
34. Titov VN, ShiriaevaIu K. Pathology of the distal and proximal arterial bed. Pathogenesis of diabetic microangiopathy. Klin Lab Diagn. 2011(4): 3-14.
35. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001; 414(6865): 813-20.
36. Giardino I, Edelstein D, Brownlee M. BCL-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells. J Clin Invest. 1996; 97(6): 1422-8.
37. Purushothaman KR, Purushothaman M, Muntner P, et al. Inflammation, neovascularization and intra-plaque hemorrhage are associated with increased reparative collagen content: implication for plaque progression in diabetic atherosclerosis. Vasc Med. 2011; 16(2): 103-8.
38. Devaraj S, Dasu MR, Park SH, Jialal I. Increased levels of ligands of Toll-like receptors 2 and 4 in type 1 diabetes. Diabetologia. 2009; 52(8): 1665-8.
39. Devaraj S, Jialal I, Yun JM, Bremer A. 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. 2011; 60(2): 256-9.
40. Bernal-Lopez MR, Llorente-Cortes V, Calleja F, Lopez-Carmona D, Mayas MD, Gomez-Huelgas R. Effect of different degrees of impaired glucose metabolism on the expression of inflammatory markers in monocytes of patients with atherosclerosis. Acta Diabetol. 2011.
41. 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 ClinEndocrinolMetab. 2008; 93(2): 578-83.
42. 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(4): 861-8.
43. Li J, Jin C, Cleveland JC et al. Enhanced inflammatory responses to toll-like receptor 2/4 stimulation in type 1 diabetic coronary artery endothelial cells: the effect of insulin. Cardiovasc Diabetol. 2010; 9: 90.
44. Hodgkinson CP, Laxton RC, Patel K, Ye S. Advanced glycation end-product of low density lipoprotein activates the toll-like 4 receptor pathway implications for diabetic atherosclerosis. Arterioscler Thromb Vasc Biol. 2008; 28(12): 2275-81.
45. Mohammad MK, Morran M, Slotterbeck B, et al. Dysregulated Toll-like receptor expression and signaling in bone marrow-derived macrophages at the onset of diabetes in the non-obese diabetic mouse. Int Immunol. 2006; 18(7): 1101-13.
46. Edfeldt K, Swedenborg J, Hansson GK, Yan ZQ. Expression of toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation. Circulation. 2002; 105(10): 1158-61.
47. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest. 2005; 115(11): 3149-56.
48. Xu XH, Shah PK, Faure E, et al. Toll-like receptor-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL. Circ J. 2001; 104(25): 3103-8.
49. Kiechl S, Lorenz E, Reindl M, et al. Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med. 2002; 347(3): 185-92.
50. Kolz M, Baumert J, Muller M, et al. Association between variations in the TLR4 gene and incident type 2 diabetes is modified by the ratio of total cholesterol to HDL-cholesterol. BMC Med Genet. 2008; 9: 9.
51. Gregg EW, Sorlie P, Paulose-Ram R, et al. Prevalence of lower-extremity disease in the US adult population >=40 years of age with and without diabetes: 1999-2000 national health and nutrition examination survey. Diabetes Care. 2004; 27(7): 1591-7.
52. Duchen LW, Anjorin A, Watkins PJ, Mackay JD. Pathology of autonomic neuropathy in diabetes mellitus. Ann Inter Med. 1980; 92(2 Pt 2): 301-3.
53. Yagihashi S. Diabetic neuropathy--treatment strategy based on clinical guideline of the Japan Diabetes Society. Nihon Rinsho. 2010; 68 Suppl 9: 616-21.
54. Schmidt RE, Feng D, Wang Q, et al. Effect of insulin and an erythropoietin-derived peptide (ARA290) on established neuritic dystrophy and neuronopathy in Akita (Ins2 Akita) diabetic mouse sympathetic ganglia. Exp Neurol. 2011; 232(2): 126-35.
55. Shaikh AS, Somani RS. Animal models and biomarkers of neuropathy in diabetic rodents. Indian J Pharmacol. 2010; 42(3): 129-34.
56. Calcutt NA, Cooper ME, Kern TS, Schmidt AM. Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat Rev Drug Discov. 2009; 8(5): 417-29.
57. Shi XQ, Zekki H, Zhang J. The role of TLR2 in nerve injuryinduced neuropathic pain is essentially mediated through macrophages in peripheral inflammatory response. Glia. 2011; 59(2): 231-41.
58. Nowicki M, Kosacka J, Serke H, Bluher M, Spanel-Borowski K. Altered sciatic nerve fiber morphology and endoneuralmicrovessels in mouse models relevant for obesity, peripheral diabetic polyneuropathy, and the metabolic syndrome. J Neurosci Res. 2012; 90(1): 122-31.
59. El-Mesallamy HO, Hamdy NM, Ezzat OA, Reda AM. Levels of soluble advanced glycation end product-receptors and other soluble serum markers as indicators of diabetic neuropathy in the foot. J Invest Med. 2011; 59(8): 1233-8.
60. Manolakis AC, Kapsoritakis AN, Tiaka EK, Sidiropoulos A, Gerovassili A, Satra M, et al. TLR4 gene polymorphisms: evidence for protection against type 2 diabetes but not for diabetesassociated ischaemic heart disease. Euro J Endocrinol. 2011; 165(2): 261-7.
61. Mani R, Yarde S, Edmonds M. Prevalence of deep venous incompetence and microvascular abnormalities in patients with diabetes mellitus. Int JLow Extrem Wounds. 2011; 10(2): 75-9.
62. Lazarus GS, Cooper DM, Knighton DR, Percoraro RE, Rodeheaver G, Robson MC. Definitions and guidelines for assessment of wounds and evaluation of healing. Wound Repair Regen. 1994; 2(3): 165-70.
63. Reiber GE, Vileikyte L, Boyko EJ, et al. Causal pathways for incident lower-extremity ulcers in patients with diabetes from two settings. Diabetes care. 1999; 22(1): 157-62.
64. Wang YN, Lee K, Ledoux WR. Histomorphological evaluation of diabetic and non-diabetic plantar soft tissue. Foot Ankle Int. 2011; 32(8): 802-10.
65. Galkowska H, Wojewodzka U, Olszewski WL. Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers. Wound Repair and Regen. 2006; 14(5): 558-65.
66. Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet. 2005; 366(9502): 2058-61.
67. Dasu MR, Thangappan RK, Bourgette A, DiPietro LA, Isseroff R, Jialal I. TLR2 expression and signaling-dependent inflammation impair wound healing in diabetic mice. Lab Invest. 2010; 90(11): 1628-36.
68. Deiters U, Barsig J, Tawil B, Muhlradt PF. The macrophageactivating lipopeptide-2 accelerates wound healing in diabetic mice. Exp Dermatol. 2004; 13(12): 731-9.
69. Lan CC, Wu CS, Huang SM et al. High-Glucose Environment Inhibits p38MAPK Signaling and Reduces Human beta-Defensin-3 Expression [corrected] in Keratinocytes. Mol Med. 2011; 17(7-8): 771-9.
70. Gollapudi P, Yoon JW, Gollapudi S, Pahl MV, Vaziri ND. Leukocyte toll-like receptor expression in end-stage kidney disease. Am JNephrol. 2010; 31(3): 247-54.
71. Batsford S, Duermueller U, Seemayer C, Mueller C, Hopfer H, Mihatsch M. Protein level expression of Toll-like receptors 2, 4 and 9 in renal disease. NephrolDial Transplant. 2011; 26(4): 1413-6.
72. Koc M, Toprak A, Arikan H, et al. Toll-like receptor expression in monocytes in patients with chronic kidney disease and haemodialysis: relation with inflammation. Nephrol Dial Transplant. 2011; 26(3): 955-63.
73. Skuginna V, Lech M, Allam R, et al. Toll-like receptor signaling and SIGIRR in renal fibrosis upon unilateral ureteral obstruction. PloSOne. 2011; 6(4): e19204.
74. Kalakeche R, Hato T, Rhodes G, et al. Endotoxin uptake by S1 proximal tubular segment causes oxidative stress in the downstream S2 segment. J Am Soc Nephrol. 2011; 22(8): 1505-16.
75. Lepenies J, Eardley KS, Kienitz T, et al. Renal TLR4 mRNA expression correlates with inflammatory marker MCP-1 and profibrotic molecule TGF-beta in patients with chronic kidney disease. Nephron Clin Practice. 2011; 119(2): 97-104.
76. Watts BA 3rd, George T, Sherwood ER, Good DW. Basolateral LPS inhibits NHE3 and HCOFormula absorption through TLR4/MyD88-dependent ERK activation in medullary thick ascending limb. Am J Cell Physiol. 2011; 301(6): 1296-306.
77. Yang X, Kume S, Tanaka Y, et al. GW501516, a PPARdelta agonist, ameliorates tubulointerstitial inflammation in proteinuric kidney disease via inhibition of TAK1-NFkappaB pathway in mice. PloS one. 2011; 6(9): e25271.
78. Hasu M, Thabet M, Tam N, Whitman SC. Specific loss of toll-like receptor 2 on bone marrow derived cells decreases atherosclerosis in LDL receptor null mice. Canadian J Physiol Pharmacol. 2011; 89(10): 737-42.
79. Seimon TA, Nadolski MJ, Liao X, et al. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metabol. 2010; 12(5): 467-82.
80. Shimasaki S, Koga T, Shuto T, et al. Endoplasmic reticulum stress increases the expression and function of toll-like receptor-2 in epithelial cells. Biochem Biophys Res Commun. 2010; 402(2): 235-40.
81. Su X, Ao L, Shi Y, Johnson TR, Fullerton DA, Meng X. Oxidized low density lipoprotein induces bone morphogenetic protein-2 in coronary artery endothelial cells via Toll-like receptors 2 and 4. J Biol Chem. 2011; 286(14): 12213-20.
82. Hanna RN, Shaked I, Hubbeling HG, et al. NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ Res. 2012; 110(3): 416-27.
83. Howell KW, Meng X, Fullerton DA, Jin C, Reece TB, Cleveland JC, Jr. Toll-like receptor 4 mediates oxidized LDL-induced macro phage differentiation to foam cells. J Surg Res. 2011; 171(1): e27-31.
84. Kashiwagi M, Imanishi T, Ozaki Yet al. Differential expression of Toll-like receptor 4 and human monocyte subsets in acute myocardial infarction. Atherosclerosis. 2012; 221(1): 249-53.
85. Sikorski K, Chmielewski S, Przybyl L, et al. STAT1-mediated signal integration between IFNgamma and LPS leads to increased EC and SMC activation and monocyte adhesion. Am J Cell Physiol. 2011; 300(6): C1337-44.
86. Boivin A, Pineau I, Barrette B, et al. Toll-like receptor signaling is critical for Wallerian degeneration and functional recovery after peripheral nerve injury. Journal Neurosci. 2007; 27(46): 12565-76.
87. Kim D, Kim MA, Cho IH, et al. A critical role of toll-like receptor 2 in nerve injury-induced spinal cord glial cell activation and pain hypersensitivity. J Biol Chem. 2007; 282(20): 14975-83.
88. Kim D, You B, Lim H, Lee SJ. Toll-like receptor 2 contributes to chemokine gene expression and macrophage infiltration in the dorsal root ganglia after peripheral nerve injury. Mol Pain. 2011; 7: 74.
89. Bettoni I, Comelli F, Rossini C, et al. Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice. Glia. 2008; 56(12): 1312-9.
90. Koks S, Fernandes C, Kurrikoff K, Vasar E, Schalkwyk LC. Gene expression profiling reveals upregulation of Tlr4 receptors in Cckb receptor deficient mice. Behav Brain Res. 2008; 188(1): 62-70.
91. Tanga FY, Nutile-McMenemy N, DeLeo JA. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. ProcNat AcadSci USA. 2005; 102(16): 5856-61.
92. Lee Y, Kim H, Kim S, Kim KH, Chung JH. Activation of toll-like receptors 2, 3 or 5 induces matrix metalloproteinase-1 and -9 expression with the involvement of MAPKs and NF-kappaB in human epidermal keratinocytes. Exp Dermatol. 2010; 19(8): e44-9.
93. Mersmann J, Habeck K, Latsch K, et al. Left ventricular dilation in toll-like receptor 2 deficient mice after myocardial ischemia/ reperfusion through defective scar formation. Basic Res Cardiol. 2011; 106(1): 89-98.
94. Podolsky DK, Gerken G, Eyking A, Cario E. Colitis-associated variant of TLR2 causes impaired mucosal repair because of TFF3 deficiency. Gastroenterology. 2009; 137(1): 209-20.
95. Pukstad BS, Ryan L, Flo TH, et al. Non-healing is associated with persistent stimulation of the innate immune response in chronic venous leg ulcers. J Dermatol Sci. 2010; 59(2): 115-22.
96. Jagavelu K, Routray C, Shergill U, O'Hara SP, Faubion W, Shah VH. Endothelial cell toll-like receptor 4 regulates fibrosisassociated angiogenesis in the liver. Hepatology. 2010; 52(2): 590-601.
97. Jiang D, Liang J, Fan J, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med. 2005; 11(11): 1173-9.
98. Taylor KR, Yamasaki K, Radek KA, et al. Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J Biol Chem. 2007; 282(25): 18265-75.
99. Wang J, Hori K, Ding J, et al. Toll-like receptors expressed by dermal fibroblasts contribute to hypertrophic scarring. J Cell Physiol. 2011; 226(5): 1265-73.