Macrophage contact dependent and independent TLR4 mechanisms induce β-cell dysfunction and apoptosis in a mouse model of type 2 diabetes

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Cucak, Helena ^a   Mayer, Christopher ^a   Tonnesen, Morten ^a   Thomsen, Lise Høj ^a   Grunnet, Lars Groth ^b   Rosendahl, Alexander ^a  

^a HAGEDORN RESEARCH INSTITUTE   (Denmark)

^b Department of Incretin and Islet Biology ^*  (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD68 ANTIGEN; CYTOKINE; INSULIN; MESSENGER RNA; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CONTACT; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; INSULIN RELEASE; MACROPHAGE; MACROPHAGE FUNCTION; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PHENOTYPE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPLEEN CELL;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CYTOKINES; DIABETES MELLITUS, TYPE 2; FEMALE; FLOW CYTOMETRY; IMMUNOASSAY; INSULIN; ISLETS OF LANGERHANS; LUMINESCENT MEASUREMENTS; MACROPHAGES; MALE; MICE; TOLL-LIKE RECEPTOR 4;

EID: 84897133645     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090685     Document Type: Article

References (49)

1. Zimmet P, Alberti KG, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414: 782-787. (Pubitemid 34000780)
2. Chen L, Magliano DJ, Zimmet PZ (2012) The worldwide epidemiology of type 2 diabetes mellitus-present and future perspectives. Nat Rev Endocrinol 8: 228-236.
3. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
4. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115: 1111-1119. (Pubitemid 40629025)
5. Kim JK, Gimeno RE, Higashimori T, Kim H-J, Choi H, et al. (2004) Inactivation of fatty acid transport protein 1 prevents fat-induced insulin resistance in skeletal muscle. J Clin Invest 113: 756-763. (Pubitemid 38544169)
6. Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1: 135-145.
7. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, et al. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116: 3015-3025. (Pubitemid 44684486)
8. Tsukumo DML, Carvalho-Filho MA, Carvalheira JBC, Prada PO, Hirabara SM, et al. (2007) Loss-of-Function Mutation in Toll-Like Receptor 4 Prevents Diet-Induced Obesity and Insulin Resistance. Diabetes 56: 1986-1998. (Pubitemid 47195825)
9. Radin MS, Sinha S, Bhatt BA, Dedousis N, O'Doherty RM (2008) Inhibition or deletion of the lipopolysaccharide receptor Toll-like receptor-4 confers partial protection against lipid-induced insulin resistance in rodent skeletal muscle. Diabetologia 51: 336-346.
10. Garay-Malpartida H, Mourao R, Mantovani M, Santos I, Sogayar M, et al. (2011) Toll-like receptor 4 (TLR4) expression in human and murine pancreatic beta-cells affects cell viability and insulin homeostasis. BMC Immunology 12: 18.
11. Reyna SM, Ghosh S, Tantiwong P, Meka CSR, Eagan P, et al. (2008) Elevated Toll-Like Receptor 4 Expression and Signaling in Muscle From Insulin- Resistant Subjects. Diabetes 57: 2595-2602.
12. Ladefoged M, Buschard K, Hansen AM (2012) Increased expression of toll-like receptor 4 and inflammatory cytokines, interleukin-6 in particular, in islets from a mouse model of obesity and type 2 diabetes. APMIS.
13. Ehses JA, Perren A, Eppler E, Ribaux P, Pospisilik JA, et al. (2007) Increased Number of Islet-Associated Macrophages in Type 2 Diabetes. Diabetes 56: 2356-2370. (Pubitemid 47358243)
14. Coleman DL (1982) Diabetes-obesity syndromes in mice. Diabetes 31: 1-6.
15. Chan TM, Dehaye JP (1981) Hormone Regulation of Glucose Metabolism in the Genetically Obese-Diabetic Mouse (db/db): Glucose Metabolism in the Perfused Hindquarters of Lean and Obese Mice. Diabetes 30: 211-218. (Pubitemid 11026316)
16. Herberg L, Coleman DL (1977) Laboratory animals exhibiting obesity and diabetes syndromes. Metabolism 26: 59-99. (Pubitemid 8027641)
17. Agudo J, Ayuso E, Jimenez V, Casellas A, Mallol C, et al. (2012) Vascular Endothelial Growth Factor-Mediated Islet Hypervascularization and Inflammation Contribute to Progressive Reduction of b-Cell Mass. Diabetes 61: 2851-2861.
18. Cucak H, Grunnet LG, Rosendahl A (2013) Accumulation of M1-like macrophages in type 2 diabetic islets is followed by a systemic shift in macrophage polarization. J Leukoc Biol.
19. Bell E (2009) Innate immunity: Endothelial cells as sentinels. Nat Rev Immunol 9: 532-533.
20. Creely SJ, McTernan PG, Kusminski CM, Fisher fM, Da Silva NF, et al. (2007) Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. American Journal of Physiology - Endocrinology And Metabolism 292: E740-E747. (Pubitemid 46411051)
21. Vives-Pi M, Somoza N, Fernandez-Alvarez J, Vargas F, Caro P, et al. (2003) Evidence of expression of endotoxin receptors CD14, toll-like receptors TLR4 and TLR2 and associated molecule MD-2 and of sensitivity to endotoxin (LPS) in islet beta cells. Clin Exp Immunol 133: 208-218. (Pubitemid 36918595)
22. Eguchi K, Manabe I, Oishi-Tanaka Y, Ohsugi M, Kono N, et al. (2012) Saturated fatty acid and TLR signaling link beta cell dysfunction and islet inflammation. Cell Metab 15: 518-533.
23. Böni-Schnetzler M, Boller S, Debray S, Bouzakri K, Meier DT, et al. (2009) Free Fatty Acids Induce a Proinflammatory Response in Islets via the Abundantly Expressed Interleukin-1 Receptor I. Endocrinology 150: 5218-5229.
24. Donath MY, Böni-Schnetzler M, Ellingsgaard H, Halban PA, Ehses JA (2010) Cytokine production by islets in health and diabetes: cellular origin, regulation and function. Trends in Endocrinology & Metabolism 21: 261-267.
25. Goldberg A, Parolini M, Chin BY, Czismadia E, Otterbein LE, et al. (2007) Toll-like receptor 4 suppression leads to islet allograft survival. The FASEB Journal 21: 2840-2848. (Pubitemid 47372751)
26. Amyot J, Semache M, Ferdaoussi M, Fontés G, Poitout V (2012) Lipopolysaccharides Impair Insulin Gene Expression in Isolated Islets of Langerhans via Toll-Like Receptor-4 and NF-κB Signalling. PLoS ONE 7: e36200.
27. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, et al. (2005) IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11: 191-198. (Pubitemid 40321355)
28. Xu H, Barnes GT, Yang Q, Tan G, Yang D, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830. (Pubitemid 38063705)
29. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808. (Pubitemid 38063703)
30. Nguyen MTA, Favelyukis S, Nguyen A-K, Reichart D, Scott PA, et al. (2007) A Subpopulation of Macrophages Infiltrates Hypertrophic Adipose Tissue and Is Activated by Free Fatty Acids via Toll-like Receptors 2 and 4 and JNKdependent Pathways. Journal of Biological Chemistry 282: 35279-35292. (Pubitemid 350232441)
31. Orr JS, Puglisi MJ, Ellacott KLJ, Lumeng CN, Wasserman DH, et al. (2012) Toll-like Receptor 4 Deficiency Promotes the Alternative Activation of Adipose Tissue Macrophages. Diabetes 61: 2718-2727.
32. Yang RB, Mark MR, Gray A, Huang A, Xie MH, et al. (1998) Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395: 284-288. (Pubitemid 28447554)
33. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, et al. (1999) Differential Roles of TLR2 and TLR4 in Recognition of Gram-Negative and Gram-Positive Bacterial Cell Wall Components. Immunity 11: 443-451. (Pubitemid 29504199)
34. Weir GC, Bonner-Weir S (2004) Five Stages of Evolving Beta-Cell Dysfunction During Progression to Diabetes. Diabetes 53: S16-S21. (Pubitemid 39564517)
35. Chou DH, Bodycombe NE, Carrinski HA, Lewis TA, Clemons PA, et al. (2010) Small-Molecule Suppressors of Cytokine-Induced beta-Cell Apoptosis. ACS Chem Biol 5: 729-734.
36. Zhou YP, Berggren PO, Grill V (1996) A fatty acid-induced decrease in pyruvate dehydrogenase activity is an important determinant of beta-cell dysfunction in the obese diabetic db/db mouse. Diabetes 45: 580-586.
37. Spranger J, Kroke A, Mohlig M, Hoffmann K, Bergmann MM, et al. (2003) 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 52: 812-817. (Pubitemid 36323590)
38. Chanchamroen S, Kewcharoenwong C, Susaengrat W, Ato M, Lertmemongkolchai G (2009) Human polymorphonuclear neutrophil responses to Burkholderia pseudomallei in healthy and diabetic subjects. Infect Immun 77: 456-463.
39. Park S, Rich J, Hanses F, Lee JC (2009) Defects in innate immunity predispose C57BL/6J-Leprdb/Leprdb mice to infection by Staphylococcus aureus. Infect Immun 77: 1008-1014.
40. Ikejima S, Sasaki S, Sashinami H, Mori F, Ogawa Y, et al. (2005) Impairment of Host Resistance to Listeria monocytogenes Infection in Liver of db/db and ob/ob Mice. Diabetes 54: 182-189. (Pubitemid 40105111)
41. Zykova SN, Jenssen TG, Berdal M, Olsen R, Myklebust R, et al. (2000) Altered cytokine and nitric oxide secretion in vitro by macrophages from diabetic type II-like db/db mice. Diabetes 49: 1451-1458.
42. Donath MY, Ehses JA, Maedler K, Schumann DM, Ellingsgaard H, et al. (2005) Mechanisms of β-Cell Death in Type 2 Diabetes. Diabetes 54: S108-S113. (Pubitemid 43343338)
43. Collier JJ, Burke SJ, Eisenhauer ME, Lu D, Sapp RC, et al. (2011) Pancreatic β-Cell Death in Response to Pro-Inflammatory Cytokines Is Distinct from Genuine Apoptosis. PLoS ONE 6: e22485.
44. Maedler K, Sergeev P, Ris F, Oberholzer J, Joller-Jemelka HI, et al. (2002) Glucose-induced β cell production of IL-1β contributes to glucotoxicity in human pancreatic islets. J Clin Invest 110: 851-860.
45. Mandrup-Poulsen T, Bendtzen K, Nielsen JH, Bendixen G, Nerup J (1985) Cytokines cause functional and structural damage to isolated islets of Langerhans. Allergy 40: 424-429. (Pubitemid 16256630)
46. Cnop M, Welsh N, Jonas J-C, Jörns A, Lenzen S, et al. (2005) Mechanisms of Pancreatic β-Cell Death in Type 1 and Type 2 Diabetes: Many Differences, Few Similarities. Diabetes 54: S97-S107. (Pubitemid 43343337)
47. Flavin MP, Coughlin K, Ho LT (1997) Soluble macrophage factors trigger apoptosis in cultured hippocampal neurons. Neuroscience 80: 437-448. (Pubitemid 27334593)
48. Yang Y, Wang X, Moore DR, Lightfoot SA, Huycke MM (2012) TNF-α Mediates Macrophage-Induced Bystander Effects through Netrin-1. Cancer Research 72: 5219-5229.
49. Boyle JJ, Bowyer DE, Weissberg PL, Bennett MR (2001) Human Blood-Derived Macrophages Induce Apoptosis in Human Plaque-Derived Vascular Smooth Muscle Cells by Fas-Ligand/Fas Interactions. Arteriosclerosis, Thrombosis, and Vascular Biology 21: 1402-1407. (Pubitemid 34219799)