Insulin modulates protease-activated receptor 2 signaling: Implications for the innate immune response

Journal of Immunology

Volumn 184, Issue 5, 2010, Pages 2702-2709

  Hyun, Eric ^a   Ramachandran, Rithwik ^a   Cenac, Nicolas ^b,c   Houle, Steeve ^a   Rousset, Perrine ^b,c   Saxena, Amit ^b,c   Liblau, Roland S ^b,c   Hollenberg, Morley D ^a   Vergnolle, Nathalie ^a,b,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b CHU PURPAN   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; INSULIN; PROTEINASE ACTIVATED RECEPTOR 2; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; ANTIDIABETIC AGENT; BISINDOLYLMALEIMIDE I; CALCIUM; CHROMONE DERIVATIVE; INDOLE DERIVATIVE; MALEIMIDE DERIVATIVE; MORPHOLINE DERIVATIVE; OLIGOPEPTIDE; SERYL LEUCYL ISOLEUCYL GLYCYL ARGINYL LEUCINAMIDE; SERYL-LEUCYL-ISOLEUCYL-GLYCYL--ARGINYL-LEUCINAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CALCIUM SIGNALING; CELL CULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE; LEUKOCYTE MIGRATION; LOW DRUG DOSE; MOUSE; NONHUMAN; PAW EDEMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL GANGLION; VENULE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; FEMALE; HUMAN; IMMUNOLOGY; LEUKOCYTE ROLLING; MALE; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CALCIUM; CELL LINE; CELLS, CULTURED; CHROMONES; DIABETES MELLITUS, TYPE 1; ENDOTHELIAL CELLS; FEMALE; GANGLIA, SPINAL; HUMANS; HYPOGLYCEMIC AGENTS; IMMUNITY, INNATE; INDOLES; INFLAMMATION; INSULIN; LEUKOCYTE ROLLING; MALE; MALEIMIDES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MORPHOLINES; NEURONS; OLIGOPEPTIDES; RECEPTOR, PAR-2; SIGNAL TRANSDUCTION;

EID: 77951894257     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902171     Document Type: Article

References (35)

1. Dandona, P., A. Chaudhuri, H. Ghanim, and P. Mohanty. 2006. Anti-inflammatory effects of insulin and the pro-inflammatory effects of glucose. Semin. Thorac. Cardiovasc. Surg. 18: 293-301.
2. Ghanim, H., P. Mohanty, R. Deopurkar, C. L. Sia, K. Korzeniewski, S. Abuaysheh, A. Chaudhuri, and P. Dandona. 2008. Acute modulation of Toll-like receptors by insulin. Diabetes Care 31: 1827-1831.
3. Vergnolle, N. 2005. Clinical relevance of proteinase activated receptors (PARs) in the gut. Gut 54: 867-874. (Pubitemid 40732107)
4. Vergnolle, N. 2009. Protease-activated receptors as drug targets in inflammation and pain. Pharmacol. Ther. 123: 292-309.
5. Ramachandran, R., and M. D. Hollenberg. 2008. Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br. J. Pharmacol. 153(Suppl 1): S263-S282.
6. Vergnolle, N., M. D. Hollenberg, K. A. Sharkey, and J. L. Wallace. 1999. Characterization of the inflammatory response to proteinase-activated receptor-2 (PAR2)-activating peptides in the rat paw. Br. J. Pharmacol. 127: 1083-1090.
7. Vergnolle, N. 1999. Proteinase-activated receptor-2-activating peptides induce leukocyte rolling, adhesion, and extravasation in vivo. J. Immunol. 163: 5064-5069. (Pubitemid 29501275)
8. Vergnolle, N., N. W. Bunnett, K. A. Sharkey, V. Brussee, S. J. Compton, E. F. Grady, G. Cirino, N. Gerard, A. I. Basbaum, P. Andrade-Gordon, et al. 2001. Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat. Med. 7: 821-826.
9. Steinhoff, M., N. Vergnolle, S. H. Young, M. Tognetto, S. Amadesi, H. S. Ennes, M. Trevisani, M. D. Hollenberg, J. L. Wallace, G. H. Caughey, et al. 2000. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med. 6: 151-158.
10. Hansen, K. K., P. M. Sherman, L. Cellars, P. Andrade-Gordon, Z. Pan, A. Baruch, J. L. Wallace, M. D. Hollenberg, and N. Vergnolle. 2005. A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc. Natl. Acad. Sci. U SA 102: 8363-8368.
11. Hyun, E., P. Andrade-Gordon, M. Steinhoff, and N. Vergnolle. 2008. Protease-activated receptor-2 activation: a major actor in intestinal inflammation. Gut 57: 1222-1229.
12. Cenac, N., C. N. Andrews, M. Holzhausen, K. Chapman, G. Cottrell, P. Andrade-Gordon, M. Steinhoff, G. Barbara, P. Beck, N. W. Bunnett, et al. 2007. Role for protease activity in visceral pain in irritable bowel syndrome. J. Clin. Invest. 117: 636-647.
13. Shpacovitch, V. M., T. Brzoska, J. Buddenkotte, C. Stroh, C. P. Sommerhoff, J. C. Ansel, K. Schulze-Osthoff, N. W. Bunnett, T. A. Luger, and M. Steinhoff. 2002. Agonists of proteinase-activated receptor 2 induce cytokine release and activation of nuclear transcription factor κB in human dermal microvascular endothelial cells. J. Invest. Dermatol. 118: 380-385.
14. + T cells. Eur. J. Immunol. 22: 1013-1022.
15. + T cell-mediated spontaneous diabetes in neonatal mice. J. Immunol. 157: 978-983.
16. Hollenberg, M. D., M. Saifeddine, S. Sandhu, S. Houle, and N. Vergnolle. 2004. Proteinase-activated receptor-4: evaluation of tethered ligand-derived peptides as probes for receptor function and as inflammatory agonists in vivo. Br. J. Pharmacol. 143: 443-454.
17. Baatz, H., M. Steinbauer, A. G. Harris, and F. Krombach. 1995. Kinetics of white blood cell staining by intravascular administration of rhodamine 6G. Int. J. Microcirc. Clin. Exp. 15: 85-91.
18. Augé, C., D. Balz-Hara, M. Steinhoff, N. Vergnolle, and N. Cenac. 2009. Protease-activated receptor-4 (PAR 4): a role as inhibitor of visceral pain and hypersensitivity. Neurogastroenterol. Motil. 21: 1189-e107.
19. Cenac, N., C. Altier, K. Chapman, W. Liedtke, G. Zamponi, and N. Vergnolle. 2008. Transient receptor potential vanilloid-4 has a major role in visceral hypersensitivity symptoms. Gastroenterology 135: 937-946, 946.
20. Kawabata, A., M. Saifeddine, B. Al-Ani, L. Leblond, and M. D. Hollenberg. 1999. Evaluation of proteinase-activated receptor-1 (PAR-1) agonists and antagonists using cultured cell receptor assay: activation of PAR-2 by PAR-1 ligand. J. Pharmacol. Exp. Ther. 288: 358-370.
21. Saxena, A., J. Bauer, T. Scheikl, J. Zappulla, M. Audebert, S. Desbois, A. Waisman, H. Lassmann, R. S. Liblau, and L. T. Mars. 2008. Cutting edge: multiple sclerosis-like lesions induced by effector CD8 T cells recognizing a sequestered antigen on oligodendrocytes. J. Immunol. 181: 1617-1621.
22. Seeliger, S., C. K. Derian, N. Vergnolle, N. W. Bunnett, R. Nawroth, M. Schmelz, P. Y. Von Der Weid, J. Buddenkotte, C. Sunderkötter, D. Metze, et al. 2003. Proinflammatory role of proteinase-activated receptor-2 in humans and mice during cutaneous inflammation in vivo. FASEB J. 17: 1871-1885.
23. Buddenkotte, J., C. Stroh, I. H. Engels, C. Moormann, V. M. Shpacovitch, S. Seeliger, N. Vergnolle, D. Vestweber, T. A. Luger, K. Schulze-Osthoff, and M. Steinhoff. 2005. Agonists of proteinase-activated receptor-2 stimulate upregulation of intercellular cell adhesion molecule-1 in primary human keratinocytes via activation of NF-kappa B. J. Invest. Dermatol. 124: 38-45.
24. Nguyen, C., A. M. Coelho, E. Grady, S. J. Compton, J. L. Wallace, M. D. Hollenberg, N. Cenac, R. Garcia-Villar, L. Bueno, M. Steinhoff, et al. 2003. Colitis induced by proteinase-activated receptor-2 agonists is mediated by a neurogenic mechanism. Can. J. Physiol. Pharmacol. 81: 920-927.
25. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689.
26. Fernández-Real, J. M., and J. C. Pickup. 2008. Innate immunity, insulin resistance and type 2 diabetes. Trends Endocrinol. Metab. 19: 10-16.
27. Ferrell, W. R., J. C. Lockhart, E. B. Kelso, L. Dunning, R. Plevin, S. E. Meek, A. J. Smith, G. D. Hunter, J. S. McLean, F. McGarry, et al. 2003. Essential role for proteinase-activated receptor-2 in arthritis. J. Clin. Invest. 111: 35-41.
28. Vergnolle, N. 2008. Proteinase-activated receptors (PARs) in infection and inflammation in the gut. Int. J. Biochem. Cell Biol. 40: 1219-1227.
29. Hansen, T. K., S. Thiel, P. J. Wouters, J. S. Christiansen, and G. Van den Berghe. 2003. 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: 1082-1088.
30. Pradhan, A. D., B. M. Everett, N. R. Cook, N. Rifai, and P. M. Ridker. 2009. Effects of initiating insulin and metformin on glycemic control and inflammatory biomarkers among patients with type 2 diabetes: the LANCET randomized trial. JAMA 302: 1186-1194.
31. Kono, T., and F. W. Barham. 1973. Effects of insulin on the levels of adenosine 3′:5′-monophosphate and lipolysis in isolated rat epididymal fat cells. J. Biol. Chem. 248: 7417-7426.
32. Kisfalvi, K., O. Rey, S. H. Young, J. Sinnett-Smith, and E. Rozengurt. 2007. Insulin potentiates Ca2+ signaling and phosphatidylinositol 4,5-bisphosphate hydrolysis induced by Gq protein-coupled receptor agonists through an mTOR-dependent pathway. Endocrinology 148: 3246-3257. (Pubitemid 46996971)
33. Kidd, L. B., G. A. Schabbauer, J. P. Luyendyk, T. D. Holscher, R. E. Tilley, M. Tencati, and N. Mackman. 2008. Insulin activation of the phosphatidylinositol 3-kinase/protein kinase B (Akt) pathway reduces lipopolysaccharide-induced inflammation in mice. J. Pharmacol. Exp. Ther. 326: 348-353.
34. 1B-adrenergic receptor phosphorylation through Gbγ and epidermal growth factor receptor transactivation. Mol. Endocrinol. 20: 2773-2783.
35. 1D-adrenoceptor signaling properties: phosphorylation and desensitization. Int. J. Biochem. Cell Biol. 41: 1276-1283.