The effects and mechanisms of insulin on systemic inflammatory response and immune cells in severe trauma, burn injury, and sepsis

International Immunopharmacology

Volumn 9, Issue 11, 2009, Pages 1251-1259

  Deng, Hu ping ^a   Chai, Jia ke ^a  

^a First Affiliated Hospital of Chinese   (China)

Author keywords

Burn; Hyperglycemia; Insulin; Leukocytes; Sepsis; Systemic inflammatory response syndrome

Indexed keywords

CELL ADHESION MOLECULE; INSULIN; TRANSCRIPTION FACTOR;

APOPTOSIS; BURN; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL PROTECTION; DRUG EFFECT; DRUG MECHANISM; ENDOTHELIUM CELL; HUMAN; HYPERMETABOLISM; IMMUNOCOMPETENCE; IMMUNOCOMPETENT CELL; INJURY; INJURY SEVERITY; INTESTINE; INTESTINE LYMPHATIC TISSUE; MACROPHAGE; MONOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEPSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; T LYMPHOCYTE;

BURNS; HUMANS; HYPERGLYCEMIA; INFLAMMATION; INFLAMMATION MEDIATORS; INSULIN; LYMPHOCYTES; MODELS, IMMUNOLOGICAL; PHAGOCYTES; SEPSIS; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; WOUNDS AND INJURIES;

EID: 70249118870     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2009.07.009     Document Type: Review

References (103)

1. Koenig W. Insulin resistance, heart disease, and inflammation. Identifying the "at-risk" patient: the earlier the better? The role of inflammatory markers. Int J Clin Pract Suppl 132 (2002) 23-30
2. Read J.L., and Cheng E.Y. Intensive insulin therapy for acute hyperglycemia. AACN Adv Crit Care 18 2 (2007) 200-212
3. Chai J.K., Sheng Z.Y., Lu J.Y., Wen Z.G., Yang H.M., Jia X.M., et al. Characteristics of and strategies for patients with severe burn-blast combined injury. Chin Med J (Engl) 120 20 (2007) 1783-1787
4. Groeneveld A.B., Beishuizen A., and Visser F.C. Insulin: a wonder drug in the critically ill?. Crit Care 6 2 (2002) 102-105
5. Van den Berghe G., Wouters P., Weekers F., Verwaest C., Bruyninckx F., Schetz M., et al. Intensive insulin therapy in the critically ill patients. N Engl J Med 345 19 (2001) 1359-1367
6. Van den Berghe G., Wouters P.J., Bouillon R., Weekers F., Verwaest C., Schetz M., et al. Outcome benefit of intensive insulin therapy in the critically ill: insulin dose versus glycemic control. Crit Care Med 31 2 (2003) 359-366
7. Van den Berghe G., Wilmer A., Hermans G., Meersseman W., Wouters P.J., Milants I., et al. Intensive insulin therapy in the medical ICU. N Engl J Med 354 5 (2006) 449-461
8. Ellger B., Westphal M., Stubbe H.D., Van den Heuvel I., Van Aken H., and Van den Berghe G. Glycemic control in sepsis and septic shock: friend or foe?. Anaesthesist 57 1 (2008) 43-48
9. Vlasselaers D., Milants I., Desmet L., Wouters P.J., Vanhorebeek I., van den Heuvel I., et al. Intensive insulin therapy for patients in paediatric intensive care: a prospective, randomised controlled study. Lancet 373 9663 (2009) 547-556
10. Griesdale D.E., de Souza R.J., van Dam R.M., Heyland D.K., Cook D.J., Malhotra A., et al. Intensive insulin therapy and mortality among critically ill patients: a meta-analysis including NICE-SUGAR study data. CMAJ 180 8 (2009) 821-827 discussion 799-800
11. Bilotta F., Caramia R., Paoloni F.P., Delfini R., and Rosa G. Safety and efficacy of intensive insulin therapy in critical neurosurgical patients. Anesthesiology 110 3 (2009) 611-619
12. Shen C.A., Chai J.K., Yao Y.M., Du X.H., and Sheng Z.Y. Effect of insulin intensive treatment on hyperproteolysis of skeletal muscle in scalded rabbit with sepsis. Chin Crit Care Med 18 3 (2006) 139-142
13. Jeschke M.G., Einspanier R., Klein D., and Jauch K.W. Insulin attenuates the systemic inflammatory response to thermal trauma. Mol Med 8 8 (2002) 443-450
14. Van den Berghe G. Insulin therapy for the critically ill patient. Clin Cornerstone 5 2 (2003) 56-63
15. Jeschke M.G., Klein D., and Herndon D.N. Insulin treatment improves the systemic inflammatory reaction to severe trauma. Ann Surg 239 4 (2004) 553-560
16. Jeschke M.G., Klein D., Bolder U., and Einspanier R. Insulin attenuates the systemic inflammatory response in endotoxemic rats. Endocrinology 145 9 (2004) 4084-4093
17. Van den Berghe G.H. Role of intravenous insulin therapy in critically ill patients. Endocrinol Pract 10 Suppl 2 (2004) 17-20
18. Jeschke M.G., Rensing H., Klein D., Schubert T., Mautes A.E., Bolder U., et al. Insulin prevents liver damage and preserves liver function in lipopolysaccharide-induced endotoxemic rats. J Hepatol 42 6 (2005) 870-879
19. Pidcoke H.F., Wade C.E., and Wolf S.E. Insulin and the burned patient. Crit Care Med 35 9 Suppl (2007) S524-S530
20. Sakurai Y., Aarsland A., Herndon D.N., Chinkes D.L., Pierre E., Nguyen T.T., et al. Stimulation of muscle protein synthesis by long-term insulin infusion in severely burned patients. Ann Surg 222 3 (1995) 283-294
21. Coppack S.W., Jensen M.D., and Miles J.M. In vivo regulation of lipolysis in humans. J Lipid Res 35 2 (1994) 177-193
22. Calder P.C., Dimitriadis G., and Newsholme P. Glucose metabolism in lymphoid and inflammatory cells and tissues. Curr Opin Clin Nutr Metab Care 10 4 (2007) 531-540
23. Esper R.J., Vilariño J.O., Machado R.A., and Paragano A. Endothelial dysfunction in normal and abnormal glucose metabolism. Adv Cardiol 45 (2008) 17-43
24. Schetz M., Vanhorebeek I., Wouters P.J., Wilmer A., and Van den Berghe G. Tight blood glucose control is renoprotective in critically ill patients. J Am Soc Nephrol 19 3 (2008) 571-578
25. Ellger B., Debaveye Y., Vanhorebeek I., Langouche L., Giulietti A., Van Etten E., et al. Survival benefits of intensive insulin therapy in critical illness: impact of maintaining normoglycemia versus glycemia-independent actions of insulin. Diabetes 55 4 (2006) 1096-1105
26. Mesotten D., Swinnen J.V., Vanderhoydonc F., Wouters P., and van den Berghe G. Contribution of circulating lipids to the improved outcome of critical illness by glycemic control with intensive insulin therapy. J Clin Endocrimol Metab 89 (2004) 219-226
27. Krogh-Madsen R., Moller K., Dela F., Kronborg G., and Jauffred S. Pedersen B, effect of hyperglycemia and hyperinsulinemia on the response of IL-6, TNF-alpha, and FFAs to low-dose endotoxemia in humans. Anesthesiology 100 (2004) 861-870
28. Brix-Christensen V., Andersen S.K., Andersen R., Mengel A., Dyhr T., Andersen N.T., et al. Acute hyperinsulinemia restrains endotoxin-induced systemic inflammatory response. Anesthesiology 100 (2004) 861-870
29. Finnerty C.C., Herndon D.N., Przkora R., Pereira C.T., Oliveira H.M., Queiroz D.M., et al. Cytokine expression profile over time in severely burned pediatric patients. Shock 26 1 (2006) 13-19
30. Wang Y.C., Gao F., Jia C.Y., Zhang W.F., Tang C.W., and Hu D.H. Regulating effects of different doses of insulin on serum IL-1 13 and IL-10 in early stage in severely scalded rats. J Fourth Mil Med Univ 27 22 (2006) 2043-2046
31. Hansen T.K., Thiel S., Wouters P.J., Christiansen J.S., and Van den Berghe G. Intensive insulin therapy exerts antiinflammatory effects in critically ill patients and counteracts the adverse effect of low mannose-binding lectin levels. J Clin Endocrinol Metab 88 3 (2003) 1082-1088
32. Takebayashi K., Aso Y., and Inukai T. Initiation of insulin therapy reduces serum concentrations of high-sensitivity C-reactive protein in patients with type 2 diabetes. Metabolism 53 6 (2004) 693-699
33. Zhao X.D., Yao Y.M., Ma J.X., Liang H.P., Yan R.M., Zhang L.Y., et al. Effects of intensive insulin therapy on serum immunoglobulin, complement levels and phagocytosis of monocytes in patients with severe trauma. Chin Crit Care Med 19 5 (2007) 279-282
34. Hartell N.A., Archer H.E., and Bailey C.J. Insulin-stimulated endothelial nitric oxide release is calcium independent and mediated via protein kinase B. Biochem Pharmacol 69 5 (2005) 781-790
35. Zhao X.D., Meng H.D., Yao Y.M., Yan R.M., Deng Q., He Z.J., et al. Effect of intensive insulin therapy on serum proinflammatory cytokine levels in patients with severe trauma. Chin Crit Care Med 17 7 (2005) 406-408
36. Wang Y., Xu G.G., Wu J.H., Zhao X., Miao Q., and Chen W. Effect of intensive insulin therapy on serum proinflammatory cytokine levels in patients with systemic inflammatory response syndrome. Clin Educ Gen Pract 5 1 (2007) 36-38
37. Zhao X.D., Liu B., Yao Y.M., Zhang L.Y., and Liang H.P. Effects of intensive insulin therapy at the early stage on IFN-γ and IL-18 in serum for severe trauma patients. Chin J Crit Care Med 27 1 (2007) 1-3
38. Wang Z.K., Xu L.S., Wang S.L., Liu L.Y., Hu X.Y., Zhu Z.Z., et al. Influence of glucose-insulin-potassium on the levels of inflammatory cytokines and prognosis of MODS in the scalded rats. Chin J Burns 21 6 (2005) 422-425
39. Luo Z.Z., Peng S.L., and Lu G.F. Effect of intensive insulin therapy on prognosis and serum inflammatory cytokine levels in patients with sepsis. Med J West China 19 3 (2007) 392-394
40. Klein D., Schubert T., Horch R.E., Jauch K.W., and Jeschke M.G. Insulin treatment improves hepatic morphology and function through modulation of hepatic signals after severe trauma. Ann Surg 240 2 (2004) 340-349
41. Jeschke M.G., Boehning D.F., Finnerty C.C., and Herndon D.N. Effect of insulin on the inflammatory and acute phase response after burn injury. Crit Care Med 35 9 Suppl (2007) S519-S523
42. Weekers F., Giulietti A.P., Michalaki M., Coopmans W., Van Herck E., Mathieu C., et al. Metabolic, endocrine, and immune effects of stress hyperglycemia in a rabbit model of prolonged critical illness. Endocrinology 144 12 (2003) 5329-5338
43. Langouche L., Vanhorebeek I., Vlasselaers D., Vander Perre S., Wouters P.J., Skogstrand K., et al. Intensive insulin therapy protects the endothelium of critically ill patients. J Clin Invest 115 (2005) 2277-2285
44. Aljada A., Saadeh R., Assian E., Ghanim H., and Dandona P. Insulin inhibits the expression of intercellular adhesion molecule-1 by human aortic endothelial cells through stimulation of nitric oxide. J Clin Endocrinol Metab 85 7 (2000) 2572-2575
45. Dandona P., Aljada A., and Mohanty P. The anti-inflammatory and potential anti-atherogenic effect of insulin: a new paradigm. Diabetologia 45 6 (2002) 924-930
46. Froon A.H.M., Bemetmans M.H.A., and Greve J.W. Increased plasma concentrations of STNFRs in sepsis syndrome correlation with plasma creatinine values. Crit Care Med 22 (1994) 803-809
47. Magnotti L.J., and Deitch E.A. Burns, bacterial translocation, gut barrier function, and failure. J Burn Care Rehabil 26 (2005) 383-391
48. Saadia R., Schein M., MacFarlane C., and Boffard K.D. Gut barrier function and the surgeon. Br J Surg 77 (1990) 487-492
49. Wang X., Wang B., Wu J., and Wang G. Beneficial effects of growth hormone on bacterial translocation during the course of acute necrotizing pancreatitis in rats. Pancreas 23 (2001) 148-156
50. Scopa C.D., Koureleas S., Tsamandas A.C., Spiliopoulou I., Alexandrides T., Filos K.S., et al. Beneficial effects of growth hormone and insulin-like growth factor I on intestinal bacterial translocation, endotoxemia, and apoptosis in experimentally jaundiced rats. J Am Coll Surg 190 (2000) 423-431
51. Ortega M., Gomez-de-Segura I.A., Vazquez I., Lopez J.M., de Guevara C.L., and De-Miguel E. Effects of growth hormone plus a hyperproteic diet on methotrexate-induced injury in rat intestines. Acta Oncol 40 (2001) 615-621
52. Kouris G.J., Liu Q., Rossi H., Djuricin G., Gattuso P., Nathan C., et al. The effect of glucagon-like peptide 2 on intestinal permeability and bacterial translocation in acute necrotizing pancreatitis. Am J Surg 181 (2001) 571-575
53. Huang K.F., Chung D.H., and Herndon D.N. Insulinlike growth factor 1 (IGF-1) reduces gut atrophy and bacterial translocation after severe burn injury. Arch Surg 128 (1993) 47-53
54. Yadavalli G.K., Auletta J.J., Gould M.P., Salata R.A., Lee J.H., and Heinzel F.P. Deactivation of the innate cellular response following endotoxic and surgical injury. Exp Mol Pathol 71 3 (2001) 209-221
55. Iida K.T., Suzuki H., Sone H., Shimano H., Toyoshima H., Yatoh S., et al. Insulin inhibits apoptosis of macrophage cell line, THP-1 cells, via phosphatidylinositol-3-kinase-dependent pathway. Arterioscler Thromb Vasc Biol 22 3 (2002) 380-386
56. Leffler M., Hrach T., Stuerzl M., Horch R.E., Herndon D.N., and Jeschke M.G. Insulin attenuates apoptosis and exerts anti-inflammatory effects in endotoxemic human macrophages. J Surg Res 143 2 (2007) 398-406
57. Hermann C., Assmus B., Urbich C., Zeiher A.M., and Dimmeler S. Insulin-mediated stimulation of protein kinase Akt: a potent survival signaling cascade for endothelial cells. Arterioscler Thromb Vasc Biol 20 2 (2000) 402-409
58. Conejo R., and Lorenzo M. Insulin signaling leading to proliferation, survival, and membrane ruffling in C2C12 myoblasts. J Cell Physiol 187 1 (2001) 96-108
59. Liu J.J., Hu S., Dong N., Sun D., Chai J.K., Zhu J.M., et al. Changes in the percentage of human leukocyte antigen DR in CD(+)(14) monocytes in burned patients. Chin Crit Care Med 15 1 (2003) 23-25
60. Yang H.M., Yu Y., Chai J.K., Hu S., Sheng Z.Y., and Yao Y.M. Low HLA-DR expression on CD14(+) monocytes of burn victims with sepsis, and the effect of carbachol in vitro. Burns 34 8 (2008) 1158-1162
61. Zhao X.D., Meng H.P., Liang H.P., Yao Y.M., Ma J.X., He Z.J., et al. Influence of intensive insulin therapy on rate of CD14 + and expression of CD14 + monocyte human leukocyte antigen DR in severe trauma patients. Chin J Crit Care Med. 26 17 (2006) 481-484
62. Yoshida S. Monocyte HLA-DR expression as predictors of clinical outcome for patients with sepsis. Nippon Rinsho 62 12 (2004) 2281-2284
63. Yang H.M., Yu Y., Chai J.K., Hu S., Lei S.H., Zhang D.Q., et al. Study on the relationship between the human leucocyte antigen-DR expression on CD14+ monocytes and sepsis. Zhonghua Shao Shang Za Zhi 23 4 (2007) 272-275
64. Yu W.K., Li W.Q., Wang X.D., Yan X.W., Qi X.P., Li N., et al. Influence and mechanism of a tight control of blood glucose by intensive insulin therapy on human sepsis. Chin J Surg 43 1 (2005) 29-32
65. Yu W.K., Li W.Q., Li N., and Li J.S. Efects of insulin on monocytic cytokines production and expression of HLA-DR in human sepsis. Chin J Gen Surg 21 3 (2006) 218-220
66. Esmann V. The polymorphonuclear leukocyte in diabetes mellitus. J Clin Chem Clin Biochem 21 9 (1983) 561-567
67. Walrand S., Guillet C., Bo irie Y., and Vasson M.P. In vivo evidences that insulin regulates human polymorphonuclear neutrophil functions. J Leukoc Biol 76 6 (2004) 1104-1110
68. Abbas A.K., Murphy K.M., and Sher A. Functional diversity of helper T lymphocytes. Nature 383 6603 (1996) 787-793
69. Dong N., Yao Y.M., Cao Y.J., He L.X., Yu Y., Chai J.K., et al. The clinical significance of changes in immunological function of T lymphocyte in severe burn patients with sepsis. Chin J Burns 23 2 (2007) 84-87
70. Miller A.C., Rashid R.M., and Elamin E.M. The "T" in trauma: the helper T-cell response and the role of immunomodulation in trauma and burn patients. J Trauma 63 6 (2007) 1407-1417
71. Viardot A., Grey S.T., Mackay F., and Chisholm D. Potential antiinflammatory role of insulin via the preferential polarization of effector T cells toward a T helper 2 phenotype. Endocrinology 148 1 (2007) 346-353
72. Stentz F.B., and Kitabchi A.E. De novo emergence of growth factor receptors in activated human CD4+ and CD8+ T lymphocytes. Metabolism 53 1 (2004) 117-122
73. Koffler M., Raskin P., Womble D., and Helderman J.H. Immunobiological consequence of regulation of insulin receptor on alloactivated lymphocytes in normal and obese subjects. Diabetes 40 3 (1991) 364-370
74. Desbois-Mouthon C., Blivet-Van Eggelpoel M.J., Auclair M., Cherqui G., Capeau J., and Caron M. Insulin differentially regulates SAPKs/JNKs and ERKs in CHO cells overexpressing human insulin receptors. Biochem Biophys Res Commun 243 3 (1998) 765-770
75. Huang H., and Paul W.E. Impaired interleukin 4 signaling in T helper type 1 cells. J Exp Med 187 8 (1998) 1305-1313
76. Dandona P., Aljada A., Mohanty P., Ghanim H., Hamouda W., Assian E., et al. Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect?. J Clin Endocrinol Metab 86 7 (2001) 3257-3265
77. Zhang S.L., Li Q.W., Fan X.H., Li X.Y., Cao B.Z., Xing W.J., et al. Effects of intensive insulin therapy on the activity of nuclear factor kappa B in PBMC of the patients with critical illness complicated by hyperglycemia. Med J Chin PLA 33 2 (2008) 207-209
78. Aljada A., Ghanim H., Mohanty P., Kapur N., and Dandona P. Insulin inhibits the pro-inflammatory transcription factor early growth response gene-1 (Egr)-1 expression in mononuclear cells (MNC) and reduces plasma tissue factor (TF) and plasminogen activator inhibitor-1 (PAI-1) concentrations. J Clin Endocrinol Metab 87 3 (2002) 1419-1422
79. Ditschkowski M., Kreuzfelder E., Majetschak M., et al. Reduced B cell HLA-DR expression and natural killer cell counts in patients prone to sepsis after injury. Eur J Surg 165 (1999) 1129-1133
80. Pratt V.C., Tredget E.E., Clandinin M.T., et al. Alterations in lymphocyte function and relation to phospholipid composition after burn injury in humans. Crit Care Med 30 (2002) 1753-1761
81. Venet F., Chung C.S., Monneret G., Huang X., Horner B., Garber M., et al. Regulatory T cell populations in sepsis and trauma. J Leukoc Biol 83 3 (2008) 523-535
82. Tiittanen M., Huupponen J.T., Knip M., and Vaarala O. Insulin treatment in patients with type 1 diabetes induces upregulation of regulatory T-cell markers in peripheral blood mononuclear cells stimulated with insulin in vitro. Diabetes 55 12 (2006) 3446-3454
83. Kidd L.B., Schabbauer G.A., Luyendyk J.P., Holscher T.D., Tilley R.E., Tencati M., et al. Insulin activation of the phosphatidylinositol 3-kinase/protein kinase B (Akt) pathway reduces lipopolysaccharide-induced inflammation in mice. J Pharmacol Exp Ther 326 1 (2008) 348-353
84. Desbois-Mouthon C., Cadoret A., Blivet-Van Eggelpoel M.J., Bertrand F., Caron M., Atfi A., et al. Insulin-mediated cell proliferation and survival involve inhibition of c-Jun N-terminal kinases through a phosphatidylinositol 3-kinase- and mitogen-activated protein kinase phosphatase-1-dependent pathway. Endocrinology 141 3 (2000) 922-931
85. Chi H., Barry S.P., Roth R.J., Wu J.J., Jones E.A., Bennett A.M., et al. Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc Natl Acad Sci U S A 103 7 (2006) 2274-2279
86. Dugo L., Collin M., Allen D.A., Murch O., Foster S.J., Yaqoob M.M., et al. Insulin reduces the multiple organ injury and dysfunction caused by coadministration of lipopolysaccharide and peptidoglycan independently of blood glucose: role of glycogen synthase kinase-3beta inhibition. Crit Care Med 34 5 (2006) 1489-1496
87. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., and Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378 6559 (1995) 785-789
88. Crowder R.J., and Freeman R.S. Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci 18 8 (1998) 2933-2943
89. Zhou B.P., Liao Y., Xia W., Spohn B., Lee M.H., and Hung M.C. Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells. Nat Cell Biol 3 3 (2001) 245-252
90. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 282 5392 (1998) 1318-1321
91. Downward J. How bad phosphorylation is good for survival. Nat Cell Biol 1 2 (1999) E33-E35
92. Kim A.H., Khursigara G., Sun X., Franke T.F., and Chao M.V. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol Cell Biol 21 3 (2001) 893-901
93. Lawlor M.A., and Alessi D.R. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses?. J Cell Sci. 114 16 (2001) 2903-2910
94. Niehof M., Kubicka S., Zender L., Manns M.P., and Trautwein C. 2001 interleukin-6-induced tethering of STAT3 to the LAP/C/EBP_ promoter suggests a new mechanism of transcriptional regulation by STAT3. J Biol Chem 276 12 (2001) 9016-9027
95. Emanuelli B., Peraldi P., Filloux C., Sawka-Verhelle D., Hilton D., and Van Obberghen E. SOCS-3 is an insulin-induced negative regulator of insulin signalling. J Biol Chem 275 21 (2000) 15,985-15,991
96. Nelson P.J., Kim H.T., Manning W.C., Goralski T.J., and Krensky A.M. Genomic organization and transcriptional regulation of the RANTES chemokine gene. J Immunol 151 5 (1993) 2601-2612
97. Jeschke M.G., Klein D., Thasler W.E., Bolder U., Schlitt H.J., Jauch K.W., et al. Insulin decreases inflammatory signal transcription factor expression in primary human liver cells after LPS challenge. Mol Med 14 1-2 (2008) 11-19
98. Aljada A., Ghanim H., Saadeh R., and Dandona P. Insulin inhibits NFkappaB and MCP-l expression in human aortic endothelial cells. J Clin Endocrinol Metab 86 1 (2001) 450-453
99. Yan Y.H., Jing X.L., Chen Y.M., and Chen Y. Role and significance of nuclear factor-κB activity in systemic inflammatory response syndrome. Chin J Postgrad Med 29 4 (2006) 23-25
100. Hang C.H., Shi J.X., Li J.S., Li W.Q., and Wu W. Expressions of intestinal NF-kappa B, TNF-alpha, and IL-6 following traumatic brain injury in rats. J Surg Res 123 2 (2005) 188-193
101. Martin-Ventura J.L., Blanco-Colio L.M., Gomez-Hernandez A., Muñoz-García B., Vega M., Serrano J., et al. Intensive treatment with atorvastatin reduces inflammation in mononuclear cells and human atherosclerotic lesions in one month. Stroke 36 8 (2005) 1796-1800
102. Zhang F., Li Z.L., Shi Y., Zhao M., Xin X.F., and Qian G.S. Nuclear factor κB in LPS stimulated rat alveolar macrophages promotes TNF-α secretion. Chinese Journal of Pathophysiology 23 7 (2007) 1412-1414
103. Grunberger G., and Levy J. Diacylglycerols modulate phosphorylation of the insulin receptor from human mononuclear cells. Eur J Biochem 187 1 (1990) 191-198