Withaferin A inhibits pro-inflammatory cytokine-induced damage to islets in culture and following transplantation

Diabetologia

Volumn 56, Issue 4, 2013, Pages 814-824

  Sorelle, J A ^a   Itoh, T ^b   Peng, H ^a   Kanak, M A ^a   Sugimoto, K ^b   Matsumoto, S ^b   Levy, M F ^c   Lawrence, M C ^b   Naziruddin, B ^c  

^a BAYLOR UNIVERSITY   (United States)

^b BAYLOR RESEARCH INSTITUTE   (United States)

^c BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Beta cell; Cytokine; Islet transplantation; NF B

Indexed keywords

CYTOKINE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SYNAPTOTAGMIN I; WITHAFERIN A;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE RELEASE; DIABETES MELLITUS; DRUG EFFECT; GLUCOSE TOLERANCE TEST; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTECTION; TISSUE INJURY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; CELL CULTURE TECHNIQUES; CHROMATIN IMMUNOPRECIPITATION; CYTOKINES; GLUCOSE TOLERANCE TEST; HUMANS; INFLAMMATION; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; NF-KAPPA B; WITHANOLIDES;

EID: 84876500957     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-012-2813-9     Document Type: Article

References (48)

1. Bennet W, Groth CG, Larsson R, Nilsson B, Korsgren O (2000) Isolated human islets trigger an instant blood mediated inflammatory reaction: implications for intraportal islet transplantation as a treatment for patients with type 1 diabetes. Ups J Med Sci 105:125-133
2. Bennet W, Sundberg B, Groth CG et al (1999) Incompatibility between human blood and isolated islets of Langerhans: a finding with implications for clinical intraportal islet transplantation? Diabetes 48:1907-1914
3. Contreras JL, Eckstein C, Smyth CA et al (2004) Activated protein C preserves functional islet mass after intraportal transplantation: a novel link between endothelial cell activation, thrombosis, inflammation, and islet cell death. Diabetes 53:2804-2814
4. Amrani A, Verdaguer J, Thiessen S, Bou S, Santamaria P (2000) IL-1alpha, IL-1beta, and IFN-gamma mark beta cells for Fas dependent destruction by diabetogenic CD4 (+) T lymphocytes. J Clin Invest 105:459-468
5. Amoli MM, Bagher L (2005) Would blockage of cytokines improve the outcome of pancreatic islet transplantation? Med Hypotheses 66:816-819
6. Flodströma M, Welsh N, Eizirik DL (1996) Cytokines activate the nuclear factor κB (NF-κB) and induce nitric oxide production in human pancreatic islets. FEBS Lett 385:4-6
7. Chen C, Moreno R, Samikannu B, Bretzel RG, Schumitz ML, Linn T (2011) Improved intraportal islet transplantation outcome by systemic IKK-beta inhibition: NF-κB activity in pancreatic islets depends on oxygen availability. Am J Transplant 11:1-10
8. Peng H, Olsen GS, Tamura Y et al (2010) Inhibition of inflammatory cytokine-induced response in human islet cells by Withaferin A. Transplant Proc 42:2058-2061
9. Piemonti L, Leone BE, Nano R et al (2002) Human pancreatic islets produce and secrete MCP-1/ CCL2: relevance in human islet transplantation. Diabetes 51:55-65
10. Melzi R, Mercalli A, Sordi V et al (2010) Role of CCL2/ MCP-1 in islet transplantation. Cell Transplant 19:1031-1046
11. Berghe WV, Sabbe L, Kaileh M, Haegeman G, Heyninek K (2012) Molecular insight in the multifunctional activities of Withaferin A. Biochem Pharmacol 84:1282-1291
12. Chopra A, Lavin P, Patwardhan B, Chitre D (2004) A 32-week randomized, placebo-controlled clinical evaluation of RA-11, an Ayurvedic drug, on osteoarthritis of the knees. J Clin Rheumatol 10:236-245
13. Cooley K, Szczurko O, Perri D et al (2009) Naturopathic care for anxiety: a randomized controlled trial ISRCTN78958974. PLoS One 3:e6628
14. Kaileh M, Berghe WV, Heyerick A et al (2007) Withaferin A strongly elicits IκB kinase β Hyperphosphorylation concomitant with potent inhibition of its kinase activity. J Biol Chem 282:4253-4264
15. Grover A, Shandilya A, Punetha A, Bisaria VS, Sundar D (2010) Inhibition of the NEMO/IKK β association complex formation, a novel mechanism associated with the NF-κB activation suppression by Withania somnifera's key metabolite Withaferin A. BMC Genom 11:S25
16. Maitra R, Porter MA, Huang S, Gilmour BP (2009) Inhibition of NF-kappaB by the natural product Withaferin A in cellular models of cystic fibrosis inflammation. J Inflamm (Lond) 13:15
17. Barnes PJ, Karin M (1996) NF-κB: a pivotal role in orchestrating chronic inflammation. N Engl J Med 336:1066-1071
18. Barnes PJ (1997) Molecules in focus nuclear factor-κB. Int J Biochem Cell Biol 29:867-870
19. Matsumoto S, Takita M, Chaussabel D et al (2011) Improving efficacy of clinical islet transplantation with iodixanol based islet purification, thymoglobulin induction and blockage of IL-1-beta and TNF-alpha. Cell Transplant 20:1641-1647
20. Takita M, Matsumoto S, Noguchi H et al (2010) One hundred human pancreatic islet isolations at Baylor Research Institute. Proc (Bayl Univ Med Cent) 23:341-348
21. Ricordi C, Lacy PE, Scharp DW (1989) Automated islet isolation from human pancreas. Diabetes 38(suppl 1):140-142
22. Matsuoka N, Itoh T, Watarai H et al (2010) High-mobility group box 1 is involved in the initial events of early loss of transplanted islets in mice. J Clin Invest 120:735-743
23. Itoh T, Sugimoto K, Shimoda M et al (2011) Establishment of a prolonged pancreas preservation model for islet isolation research in mice. Islets 3:376-380
24. Fornoni A, Pileggi A, Molano RD et al (2008) Inhibition of c-jun N terminal kinase (JNK) improves functional beta cell mass in human islets and leads to AKT and glycogen synthase kinase-3 (GSK-3) phosphorylation. Diabetologia 51:298-308
25. Delaney CA, Pavlovic D, Hoorens A, Pipeleers DG, Eizirik DL (1997) Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells. Endocrinology 138:2610-2614
26. Huang D, Casale GP, Tian J (2007) Quantitative fluorescence imaging analysis for cancer biomarker discovery: application to beta-catenin in archived prostate samples. Canc Epidemiol Biomarkers Prev 16:1371-1381
27. Oyama K, Minami K, Ishizaki K, Fuse M, Miki T, Seino S (2006) Spontaneous recovery from hyperglycemia by regeneration of pancreatic β-cells in Kir6.2G132S transgenic mice. Diabetes 55:1930-1938
28. Hawiger J (2001) Innate immunity and inflammation: a transcriptional paradigm. Immunol Res 23:99-109
29. Hanada T, Yoshimura A (2002) Regulation of cytokine signaling and inflammation. Cytokine Growth Factor Rev 13:413-421
30. Karin M, Delhase M (2000) The I kappa B kinase (IKK) and NF-kappa B: key elements of proinflammatory signaling. Semin Immunol 12:85-98
31. Kanak M, Iwahashi S, Itoh T et al (2012) Suppression of instant blood-mediated inflammatory reaction by NF-κB blockade. 2012 Rachmiel Levine Diabetes & Obesity Symposium. (Abstract)
32. Hoffmann A, Levchenko A, Scott ML, Baltimore D (2002) The IκB-NF-κB signaling module: temporal control and selective gene activation. Science 298:1241-1245
33. Baeuerle PA, Baltimore D (1988) I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 242:540-546
34. Parry GCN, Mackman N (1994) A set of inducible genes expressed by activated human monocytic and endothelial cells contain κB-like sites that specifically bind c-Rel-p65 heterodimers. J Biol Chem 269:20823-20825
35. Baeuerle PA, Henkel T (1994) Function and activation of NF-κB in the immune system. Annu Rev Immunol 12:141-179
36. Piemonti L, Guidotti LG, Battaglia M (2010) Modulation of early inflammatory reactions to promote engraftment and function of transplanted pancreatic islets in autoimmune diabetes. In: Islam, MS (ed.) The islets of Langerhans. Advances in Experimental Medicine and Biology, Springer Netherlands, Heidelberg, Germany, pp 725-747
37. Rink J, Chen X, Xiaomin Z, Kaufman DB (2012) Conditional and specific inhibition of NF-κB in pancreatic β cells prevents cytokine-induced deleterious effects and improves islet survival post transplant. Surgery 151:330-339
38. Heimber H, Heremans Y, Jobin C et al (2001) Inhibition of cytokine-induced NF-κB activation by adenovirus-mediated expression of a NF-κB super-repressor prevents β-cell apoptosis. Diabetes 50:2219-2224
39. McCall MD, Pawlick R, Shapiro AM (2011) Resveratrol fails to improve marginal mass engraftment of transplanted islets of Langerhans in mice. Islets 3:241-245
40. Yu Y, Hamza A, Zhang T et al (2010) Withaferin A targets heat shock protein 90 in pancreatic cancer cells. Biochem Pharmacol 79:542-551
41. Oh JH, Kwon TK (2009) Withaferin A inhibits tumor necrosis factor-α-induced expression of cell adhesion molecules by inactivation of Akt and NF-κB in human pulmonary epithelial cells. Int Immunopharmacol 9:614-619
42. Oh JH, Lett TJ, Park JW, Kwon TK (2008) Withaferin A inhibits iNOS expression and nitric oxide production by Akt inactivation and down-regulating LPS-induced activity of NF-kappaB in RAW 264.7 cells. Eur J Pharmacol 599:11-17
43. Melloul D (2008) Role of NF-kB in beta-cell death. Biochem Soc Trans 36:334-339
44. Ding X, Wang X, Xue W et al (2012) Blockade of the nuclear factor kappa B pathway prolonged islet allograft survival. Artif Organs 36:e21-e27
45. Shih VF, Tsui R, Caldwell A, Hoffman A (2011) A single NFkB system for both canonical and non-canonical signaling. Cell Res 21:86-102
46. Sumoski W, Baquerizo H, Rabinovitch A (1989) Oxygen free radical scavengers protect rat islet cells from damage by cytokines. Diabetologia 32:792-796
47. Hering BJ, Kandaswamy R, Ansite JD et al (2005) Single-donor, marginal-dose islet transplantation in patients with type 1 diabetes. JAMA 293:830-835
48. McCall M, Pawlick R, Kin T, Shapiro AM (2012) Anakinra potentiates the protective effects of etanercept in transplantation of marginal mass human islets in immunodeficient mice. Am J Transplant 12:322-329