Pharmacological application of carbon monoxide ameliorates islet-directed autoimmunity in mice via anti-inflammatory and anti-apoptotic effects

Diabetologia

Volumn 57, Issue 5, 2014, Pages 980-990

  Nikolic, Ivana ^a   Saksida, Tamara ^a   Mangano, Katia ^b   Vujicic, Milica ^a   Stojanovic, Ivana ^a   Nicoletti, Ferdinando ^b   Stosic Grujicic, Stanislava ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

Beta cell apoptosis; Carbon monoxide releasing molecule A1; Cytokines; Type 1 diabetes

Indexed keywords

CARBON MONOXIDE; CASPASE 3; CYTOKINE; INSULIN; NITRITE; ANTIINFLAMMATORY AGENT; CASP3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL VIABILITY ASSAY; CONTROLLED STUDY; ELISA KIT; EX VIVO STUDY; HISTOLOGY; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; MACROPHAGE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TH2 CELL; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DIABETES MELLITUS, TYPE 1; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FEMALE; HELPER CELL; IMMUNOLOGY; METABOLISM; NONOBESE DIABETIC MOUSE; OXIDATIVE STRESS; PANCREAS ISLET; TUMOR CELL LINE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; APOPTOSIS; AUTOIMMUNITY; CARBON MONOXIDE; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FEMALE; INSULIN; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; OXIDATIVE STRESS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84898600879     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3170-7     Document Type: Article

References (40)

1. Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517-554 (Pubitemid 27238886)
2. Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583-650
3. Motterlini R, Otterbein LE (2010) The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 9:728-743
4. Fagone P, Mangano K, Quattrocchi C et al (2011) Prevention of clinical and histological signs of proteolipid protein (PLP)-induced experimental allergic encephalomyelitis (EAE) in mice by the water-soluble carbon monoxide-releasing molecule (CORM)-A1. Clin Exp Immunol 163:368-374
5. Fagone P, Mangano K, Coco M et al (2012) Therapeutic potential of carbon monoxide in multiple sclerosis. Clin Exp Immunol 167:179-187
6. Foresti R, Bani-Hani MG, Motterlini R (2008) Use of carbon monoxide as a therapeutic agent: promises and challenges. Intensive Care Med 34:649-658
7. Motterlini R, Mann BE, Johnson TR, Clark JE, Foresti R, Green CJ (2003) Bioactivity and pharmacological actions of carbon monoxide-releasing molecules. Curr Pharm Des 9:2525-2539 (Pubitemid 37236371)
8. Motterlini R, Sawle P, Hammad J et al (2005) CORM-A1: a new pharmacologically active carbon monoxide-releasing molecule. FASEB J 19:284-286 (Pubitemid 40189283)
9. Eizirik DL, Colli ML, Ortis F (2009) The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 5:219-226
10. Herold KC, Vignali DA, Cooke A, Bluestone JA (2013) Type 1 diabetes: translating mechanistic observations into effective clinical outcomes. Nat Rev Immunol 13:243-256
11. + regulatory T cells in the control of autoimmunity: in vivo veritas. Curr Opin Immunol 20:655-662
12. Acharya JD, Ghaskadbi SS (2010) Islets and their antioxidant defense. Islets 2:225-235
13. Günther L, Berberat PO, Haga M et al (2002) Carbon monoxide protects pancreatic cells from apoptosis and improves islet function/survival after transplantation. Diabetes 51:994-999 (Pubitemid 34438341)
14. Hu CM, Lin HH, Chiang MT, Chang PF, Chau LY (2007) Systemic expression of heme oxygenase-1 ameliorates type 1 diabetes in NOD mice. Diabetes 56:1240-1247 (Pubitemid 46715603)
15. Huang SH, Chu CH, Yu JC et al (2010) Transgenic expression of haem oxygenase-1 in pancreatic beta cells protects non-obese mice used as a model of diabetes from autoimmune destruction and prolongs graft survival following islet transplantation. Diabetologia 53:2389-2400
16. Althaus M, Fronius M, Buckhackert Y et al (2009) Carbon monoxide rapidly impairs alveolar fluid clearance by inhibiting epithelial sodium channels. Am J Respir Cell Mol Biol 41:639-650
17. Cvetkovic I, Al-Abed Y, Miljkovic D et al (2005) Critical role of macrophage migration inhibitory factor activity in experimental autoimmune diabetes. Endocrinology 146:2942-2951 (Pubitemid 41002801)
18. Stosic-Grujicic S, Maksimovic D, Badovinac V et al (2001) Antidiabetogenic effect of pentoxifylline is associated with systemic and target tissue modulation of cytokines and nitric oxide production. J Autoimmun 16:47-58 (Pubitemid 32174174)
19. Cvjeticanin T, Miljkovic D, Stojanovic I, Dekanski D, Stosic-Grujicic S (2010) Dried leaf extract of Olea europaea ameliorates islet-directed autoimmunity in mice. Br J Nutr 103:1413-1424
20. + regulatory T cells in diabetes modulation in BALB/c mice. Transl Res 161:118-129
21. Stojanovic I, Saksida T, Nikolic I, Nicoletti F, Stosic-Grujicic S (2012) Macrophage migration inhibitory factor deficiency protects pancreatic islets from cytokine-induced apoptosis in vitro. Clin Exp Immunol 169:156-163
22. Monboisse JC, Garnotel R, Randoux A, Dufer J, Borel JP (1991) Adhesion of human neutrophils to and activation by type-I collagen involving a β2 integrin. J Leukoc Biol 50:373-380
23. Saksida T, Stosic-Grujicic S, Timotijevic G, Sandler S, Stojanovic I (2012) Macrophage migration inhibitory factor deficiency protects pancreatic islets from palmitic acid-induced apoptosis. Immunol Cell Biol 90:688-698
24. Miyazaki J, Araki K, Yamato E et al (1990) Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127:126-132 (Pubitemid 20228111)
25. Rydgren T, Sandler S (2002) Efficacy of 1400 W, a novel inhibitor of inducible nitric oxide synthase, in preventing interleukin-1beta-induced suppression of pancreatic islet function in vitro and multiple low-dose streptozotocin-induced diabetes in vivo. Eur J Endocrinol 147:543-551 (Pubitemid 35238150)
26. Lukic ML, Stosic-Grujicic S, Shahin A (1998) Effector mechanisms in low-dose streptozotocin-induced diabetes. Dev Immunol 6:119-128 (Pubitemid 28409872)
27. Mordes JP, Serreze DV, Greiner DL, Rossini AA (2004) Animal models of autoimmune diabetes mellitus. In: LeRoith D, Taylor SI, Olefsky JM (eds) Diabetes mellitus: a fundamental and clinical text. Lippincott Williams and Wilkins, Philadelphia, pp 591-610
28. + regulatory T cells during autoimmune diabetes. J Exp Med 201:1333-1346 (Pubitemid 40629075)
29. + T cell priming regulates the differentiation of Th1 and Th17 cells and their contribution to arthritis. J Immunol 190:5423-5435
30. Chora AA, Fontoura P, Cunha A et al (2007) Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. J Clin Invest 117:438-447 (Pubitemid 46203972)
31. Kürschner C, Ozmen L, Garotta G, Dembic Z (1992) IFN-gamma receptor-Ig fusion proteins. Half-life, immunogenicity, and in vivo activity. J Immunol 149:4096-4100 (Pubitemid 23068898)
32. Kaplan MH, Sun YL, Hoey T, Grusby MJ (1996) Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382:174-177 (Pubitemid 26242885)
33. Chauveau C, Remy S, Royer PJ et al (2005) Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106:1694-1702 (Pubitemid 41208583)
34. Kapturczak MH, Wasserfall C, Brusko T et al (2004) Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 165:1045-1053 (Pubitemid 39129309)
35. + T cells and protect from type 1 diabetes. Eur J Immunol 43:209-218
36. Tang Q, Adams JY, Tooley AJ et al (2006) Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 7:83-92 (Pubitemid 41823872)
37. Bacchetta R, Bigler M, Touraine JL et al (1994) High levels of interleukin 10 production in vivo are associated with tolerance in SCID patients transplanted with HLA mismatched hematopoietic stem cells. J Exp Med 179:493-502 (Pubitemid 24058737)
38. + regulatory T cells. Cell Mol Immunol 9:464-472
39. Bogner C, Leber B, Andrews DW (2010) Apoptosis: embedded in membranes. Curr Opin Cell Biol 22:845-851
40. Li M, Peterson S, Husney D et al (2007) Interdiction of the diabetic state in NOD mice by sustained induction of heme oxygenase: possible role of carbon monoxide and bilirubin. Antioxid Redox Signal 9:855-863 (Pubitemid 46919588)