Anakinra and tocilizumab enhance survival and function of human islets during culture: Implications for clinical islet transplantation

Cell Transplantation

Volumn 23, Issue 10, 2014, Pages 1199-1211

  Sahraoui, Afaf ^a,b   Kloster Jensen, Kristine ^a,b   Ueland, Thor ^b,c   Korsgren, Olle ^d   Foss, Aksel ^a,b   Scholz, Hanne ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

Anakinra; Culture; Islet; Tocilizumab; Transplantation

Indexed keywords

CYTOKINE RECEPTOR ANTAGONIST; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOSYLATED HEMOGLOBIN; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; STAT3 PROTEIN; TOCILIZUMAB; CYTOKINE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MONOCLONAL ANTIBODY;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; DIABETIC PATIENT; DRUG EFFICACY; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; GRAFT SURVIVAL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET CELL FUNCTION; PANCREAS ISLET TRANSPLANTATION; PROTEIN PHOSPHORYLATION; RECEPTOR BLOCKING; TISSUE CULTURE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CYTOLOGY; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; GENETICS; PANCREAS ISLET; PATHOLOGY; PROCEDURES; SCID MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; APOPTOSIS; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MALE; MICE; MICE, SCID;

EID: 84907974022     PISSN: 09636897     EISSN: 15553892     Source Type: Journal    
DOI: 10.3727/096368913X667529     Document Type: Article

References (45)

1. Abdelli, S.; Ansite, J.; Roduit, R.; Borsello, T.; Matsumoto, I.; Sawada, T.; Allaman-Pillet, N.; Henry, H.; Beckmann, J. S.; Hering, B. J.; Bonny, C. Intracellular stress signaling pathways activated during human islet preparation and following acute cytokine exposure. Diabetes 53(11):2815-2823; 2004
2. Ammendrup, A.; Maillard, A.; Nielsen, K.; Aabenhus Andersen, N.; Serup, P.; Dragsbaek Madsen, O.; Mandrup- Poulsen, T.; Bonny, C. The c-Jun amino-terminal kinase pathway is preferentially activated by interleukin-1 and controls apoptosis in differentiating pancreatic beta-cells. Diabetes 49(9):1468–1476; 2000
3. Brandhorst, H.; Asif, S.; Andersson, K.; Theisinger, B.; Andersson, H. H.; Felldin, M.; Foss, A.; Salmela, K.; Tibell, A.; Tufveson, G.; Korsgren, O.; Brandhorst, D. A new oxygen carrier for improved long-term storage of human pancreata before islet isolation. Transplantation 89(2):155–160; 2010
4. Chen, H.; Gu, X.; Liu, Y.; Wang, J.; Wirt, S. E.; Bottino, R.; Schorle, H.; Sage, J.; Kim, S. K. PDGF signalling controls age-dependent proliferation in pancreatic beta-cells. Nature 478:349–355; 2011
5. Choi, S. E.; Choi, K. M.; Yoon, I. H.; Shin, J. Y.; Kim, J. S.; Park, W. Y.; Han, D. J.; Kim, S. C.; Ahn, C.; Kim, J. Y.; Hwang, E. S.; Cha, C. Y.; Szot, G. L.; Yoon, K. H.; Park, C. G. IL-6 protects pancreatic islet beta cells from pro-inflammatory cytokines-induced cell death and functional impairment in vitro and in vivo. Transpl. Immunol. 13(1):43–53; 2004
6. Citro, A.; Cantarelli, E.; Maffi, P.; Nano, R.; Melzi, R.; Mercalli, A.; Dugnani, E.; Sordi, V.; Magistretti, P.; Daffonchio, L.; Ruffini, P. A.; Allegretti, M.; Secchi, A.; Bonifacio, E.; Piemonti, L. CXCR1/2 inhibition enhances pancreatic islet survival after transplantation. J. Clin. Invest. 122(10):3647–3651; 2012
7. Cowley, M. J.; Weinberg, A.; Zammit, N.; Walters, S. N.; Hawthorne, W. J.; Loudovaris, T.; Thomas, H.; Kay, T.; Gunton, J. E.; Alexander, S. I.; Kaplan, W.; Chapman, J.; O’Connell, P. J.; Grey, S. T. Human islets express a marked pro-inflammatory molecular signature prior to transplantation. Cell Transplant. 21(9):2063–2078; 2012
8. Darville, M. I.; Eizirik, D. L. Regulation by cytokines of the inducible nitric oxide synthase promoter in insulin- producing cells. Diabetologia 41(9):1101–1108; 1998
9. Davalli, A. M.; Scaglia, L.; Zangen, D. H.; Hollister, J.; Bonner-Weir, S.; Weir, G. C. Vulnerability of islets in the immediate posttransplantation period. Dynamic changes in structure and function. Diabetes 45(9):1161–1167; 1996
10. Deshmane, S. L.; Kremlev, S.; Amini, S.; Sawaya, B. E. Monocyte chemoattractant protein-1 (MCP-1): An overview. J. Interferon Cytokine Res. 29(6):313–326; 2009
11. Ehses, J. A.; Lacraz, G.; Giroix, M. H.; Schmidlin, F.; Coulaud, J.; Kassis, N.; Irminger, J. C.; Kergoat, M.; Portha, B.; Homo-Delarche, F.; Donath, M. Y. IL-1 antagonism reduces hyperglycemia and tissue inflammation in the type 2 diabetic GK rat. Proc. Natl. Acad. Sci. USA 106(33):13998–14003; 2009
12. Ehses, J. A.; Perren, A.; Eppler, E.; Ribaux, P.; Pospisilik, J. A.; Maor-Cahn, R.; Gueripel, X.; Ellingsgaard, H.; Schneider, M. K.; Biollaz, G.; Fontana, A.; Reinecke, M.; Homo-Delarche, F.; Donath, M. Y. Increased number of islet-associated macrophages in type 2 diabetes. Diabetes 56(9):2356–2370; 2007
13. Ellingsgaard, H.; Hauselmann, I.; Schuler, B.; Habib, A. M.; Baggio, L. L.; Meier, D. T.; Eppler, E.; Bouzakri, K.; Wueest, S.; Muller, Y. D.; Hansen, A. M.; Reinecke, M.; Konrad, D.; Gassmann, M.; Reimann, F.; Halban, P. A.; Gromada, J.; Drucker, D. J.; Gribble, F. M.; Ehses, J. A.; Donath, M. Y. Interleukin-6 enhances insulin secretion by increasing glucagon- like peptide-1 secretion from L cells and alpha cells. Nat. Med. 17(11):1481–1489; 2011
14. Favaro, E.; Granata, R.; Miceli, I.; Baragli, A.; Settanni, F.; Cavallo Perin, P.; Ghigo, E.; Camussi, G.; Zanone, M. M. The ghrelin gene products and exendin-4 promote survival of human pancreatic islet endothelial cells in hyperglycaemic conditions, through phosphoinositide 3-kinase/Akt, extracellular signal-related kinase (ERK)1/2 and cAMP/protein kinase A (PKA) signalling pathways. Diabetologia 55(4): 1058–1070; 2012
15. Fujii, S.; Tokita, K.; Wada, N.; Ito, K.; Yamauchi, C.; Ito, Y.; Ochiai, A. MEK-ERK pathway regulates EZH2 overexpression in association with aggressive breast cancer subtypes. Oncogene 30(39):4118–4128; 2011
16. Goto, M.; Eich, T. M.; Felldin, M.; Foss, A.; Kallen, R.; Salmela, K.; Tibell, A.; Tufveson, G.; Fujimori, K.; Engkvist, M.; Korsgren, O. Refinement of the automated method for human islet isolation and presentation of a closed system for in vitro islet culture. Transplantation 78(9):1367–1375; 2004
17. Gupta, R. K.; Gao, N.; Gorski, R. K.; White, P.; Hardy, O. T.; Rafiq, K.; Brestelli, J. E.; Chen, G.; Stoeckert, Jr., C. J.; Kaestner, K. H. Expansion of adult beta-cell mass in response to increased metabolic demand is dependent on HNF-4alpha. Genes Dev. 21(7):756–769; 2007
18. Herder, C.; Haastert, B.; Muller-Scholze, S.; Koenig, W.; Thorand, B.; Holle, R.; Wichmann, H. E.; Scherbaum, W. A.; Martin, S.; Kolb, H. Association of systemic chemokine concentrations with impaired glucose tolerance and type 2 diabetes: Results from the Cooperative Health Research in the Region of Augsburg Survey S4 (KORA S4). Diabetes 54(Suppl 2):S11–S17; 2005
19. Kopf, M.; Bachmann, M. F.; Marsland, B. J. Averting inflammation by targeting the cytokine environment. Nat. Rev. Drug Discov. 9(9):703–718; 2010
20. Larsen, C. M.; Faulenbach, M.; Vaag, A.; Ehses, J. A.; Donath, M. Y.; Mandrup-Poulsen, T. Sustained effects of interleukin-1 receptor antagonist treatment in type 2 diabetes. Diabetes Care 32(9):1663–1668; 2009
21. Larsen, C. M.; Faulenbach, M.; Vaag, A.; Volund, A.; Ehses, J. A.; Seifert, B.; Mandrup-Poulsen, T.; Donath, M. Y. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N. Engl. J. Med. 356(15):1517–1526; 2007
22. Larsen, C. M.; Wadt, K. A.; Juhl, L. F.; Andersen, H. U.; Karlsen, A. E.; Su, M. S.; Seedorf, K.; Shapiro, L.; Dinarello, C. A.; Mandrup-Poulsen, T. Interleukin-1betainduced rat pancreatic islet nitric oxide synthesis requires both the p38 and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases. J. Biol. Chem. 273(24):15294–15300; 1998
23. Lund, T.; Fosby, B.; Korsgren, O.; Scholz, H.; Foss, A. Glucocorticoids reduce pro-inflammatory cytokines and tissue factor in vitro and improve function of transplanted human islets in vivo. Transpl. Int. 21(7):669–678; 2008
24. Mandrup-Poulsen, T. Beta-cell apoptosis: Stimuli and signaling. Diabetes 50(Suppl. 1):S58–S63; 2001
25. Mandrup-Poulsen, T.; Pickersgill, L.; Donath, M. Y. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat. Rev. Endocrinol. 6(3):158–166; 2010
26. Matsuda, T.; Omori, K.; Vuong, T.; Pascual, M.; Valiente, L.; Ferreri, K.; Todorov, I.; Kuroda, Y.; Smith, C. V.; Kandeel, F.; Mullen, Y. Inhibition of p38 pathway suppresses human islet production of pro-inflammatory cytokines and improves islet graft function. Am. J. Transplant. 5(3):484–493; 2005
27. Matsumoto, S.; Takita, M.; Chaussabel, D.; Noguchi, H.; Shimoda, M.; Sugimoto, K.; Itoh, T.; Chujo, D.; Sorelle, J.; Onaca, N.; Naziruddin, B.; Levy, M. F. Improving efficacy of clinical islet transplantation with iodixanol based islet purification, thymoglobulin induction and blockage of IL-1-beta and TNF-alpha. Cell Transplant. 20(10):1641-1647; 2011
28. McCall, M.; Pawlick, R.; Kin, T.; Shapiro, A. M. Anakinra potentiates the protective effects of etanercept in transplantation of marginal mass human islets in immunodeficient mice. Am. J. Transplant. 12(2):322–329; 2012
29. Minami, M.; Inoue, M.; Wei, S.; Takeda, K.; Matsumoto, M.; Kishimoto, T.; Akira, S. STAT3 activation is a critical step in gp130-mediated terminal differentiation and growth arrest of a myeloid cell line. Proc. Natl. Acad. Sci. USA 93(9):3963–3966; 1996
30. Negi, S.; Jetha, A.; Aikin, R.; Hasilo, C.; Sladek, R.; Paraskevas, S. Analysis of beta-cell gene expression reveals inflammatory signaling and evidence of dedifferentiation following human islet isolation and culture. PLoS One 7(1): e30415; 2012
31. Noguchi, H.; Naziruddin, B.; Jackson, A.; Shimoda, M.; Ikemoto, T.; Fujita, Y.; Chujo, D.; Takita, M.; Peng, H.; Sugimoto, K.; Itoh, T.; Kobayashi, N.; Onaca, N.; Levy, M. F.; Matsumoto, S. Fresh islets are more effective for islet transplantation than cultured islets. Cell Transplant. 21(2–3):517–523; 2012
32. Nogueira, T. C.; Graciano, M. F.; Anhe, G. F.; Curi, R.; Bordin, S.; Carpinelli, A. R. Short-term modulation of extracellular signal-regulated kinase 1/2 and stress-activated protein kinase/c-Jun NH2-terminal kinase in pancreatic islets by glucose and palmitate: Possible involvement of ceramide. Pancreas 38(5):585–592; 2009
33. Ogata, A.; Morishima, A.; Hirano, T.; Hishitani, Y.; Hagihara, K.; Shima, Y.; Narazaki, M.; Tanaka, T. Improvement of HbA1c during treatment with humanised anti-interleukin 6 receptor antibody, tocilizumab. Ann. Rheum. Dis. 70(6):1164–1165; 2011
34. Oh, Y. S.; Lee, Y. J.; Park, E. Y.; Jun, H. S. Interleukin-6 treatment induces beta-cell apoptosis via STAT-3-mediated nitric oxide production. Diabetes Metab. Res. Rev. 27(8): 813–819; 2011
35. Rabinovitch, A.; Suarez-Pinzon, W. L.; Strynadka, K.; Lakey, J. R.; Rajotte, R.V. Human pancreatic islet betacell destruction by cytokines involves oxygen free radicals and aldehyde production. J. Clin. Endocrinol. Metab. 81(9):3197–3202; 1996
36. Rosenberg, L.; Wang, R.; Paraskevas, S.; Maysinger, D. Structural and functional changes resulting from islet isolation lead to islet cell death. Surgery 126(2):393–398; 1999
37. Sakata, N.; Tan, A.; Chan, N.; Obenaus, A.; Mace, J.; Peverini, R.; Sowers, L.; Chinnock, R.; Hathout, E. Efficacy comparison between intraportal and subcapsular islet transplants in a murine diabetic model. Transplant. Proc. 41(1):346–349; 2009
38. Samavedam, U. K.; Kalies, K.; Scheller, J.; Sadeghi, H.; Gupta, Y.; Jonkman, M. F.; Schmidt, E.; Westermann, J.; Zillikens, D.; Rose-John, S.; Ludwig, R. J. Recombinant IL-6 treatment protects mice from organ specific autoimmune disease by IL-6 classical signalling-dependent IL-1ra induction. J. Autoimmun. 40:74–85; 2012
39. Scheller, J.; Chalaris, A.; Schmidt-Arras, D.; Rose-John, S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 1813(5):878–888; 2011
40. Schwarznau, A.; Hanson, M. S.; Sperger, J. M.; Schram, B. R.; Danobeitia, J. S.; Greenwood, K. K.; Vijayan, A.; Fernandez, L. A. IL-1beta receptor blockade protects islets against pro-inflammatory cytokine induced necrosis and apoptosis. J. Cell. Physiol. 220(2):341–347; 2009
41. Skov, S.; Nielsen, M.; Bregenholt, S.; Odum, N.; Claesson, M. H. Activation of Stat-3 is involved in the induction of apoptosis after ligation of major histocompatibility complex class I molecules on human Jurkat T cells. Blood 91(10):3566–3573; 1998
42. Szot, G. L.; Koudria, P.; Bluestone, J. A. Transplantation of pancreatic islets into the kidney capsule of diabetic mice. J. Vis. Exp. 9:e404; 2007
43. Tanaka, T.; Ogata, A.; Narazaki, M. Tocilizumab for the treatment of rheumatoid arthritis. Expert Rev. Clin. Immunol. 6(6):843–854; 2010
44. Wijesekara, N.; Krishnamurthy, M.; Bhattacharjee, A.; Suhail, A.; Sweeney, G.; Wheeler, M. B. Adiponectin-induced ERK and Akt phosphorylation protects against pancreatic beta cell apoptosis and increases insulin gene expression and secretion. J. Biol. Chem. 285(44):33623–33631; 2010
45. Zhang, B.; Lu, Y.; Campbell-Thompson, M.; Spencer, T.; Wasserfall, C.; Atkinson, M.; Song, S. Alpha1-antitrypsin protects beta-cells from apoptosis. Diabetes 56(5):1316-1323; 2007.