Riboflavin inhibits IL-6 expression and p38 activation in islet cells

Cell Transplantation

Volumn 17, Issue 5, 2008, Pages 558-566

  Cobianchi, Lorenzo ^a,b   Fornoni, Alessia ^a   Pileggi, Antonello ^a   Molano, R Damaris ^a   Sanabria, Nahir Y ^a   Gonzalez Quintana, Jorge ^a   Bocca, Nicola ^a   Marzorati, Simona ^a   Zahr, Elsie ^a   Hogan, Anthony R ^a   Ricordi, Camillo ^a   Inverardi, Luca ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

Cytoprotection; IL 6 p38; Inflammation; Pancreatic islets; Riboflavin

Indexed keywords

AUTACOID; CASPASE; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; OXYGEN RADICAL; RIBOFLAVIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CELL STRAIN; CELL STRAIN NIT 1; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; IMMUNOASSAY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET CELL; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; GENE EXPRESSION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; METABOLISM; NONOBESE DIABETIC MOUSE; PANCREAS ISLET;

RODENTIA;

ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; ENZYME ACTIVATION; GENE EXPRESSION; INTERLEUKIN-1BETA; INTERLEUKIN-6; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MALE; MICE; MICE, INBRED NOD; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RIBOFLAVIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 51749093352     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368908785096060     Document Type: Article

References (52)

1. Abdelli, S.; Ansite, J.; Roduit, R.; Borsello, T.; Matsumoto, I.; Sawada, T.; Allaman-Pillet, N.; Henry, H.; Beckmann, J. S.; Hering, B. J.; et al. Intracellular stress signaling pathways activated during human islet preparation and following acute cytokine exposure. Diabetes 53(11):2815-2823; 2004.
2. Afzali, B.; Lombardi, G.; Lechler, R. I.; Lord, G. M. The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin. Exp. Immunol. 148(1):32-46; 2007.
3. Aikin, R.; Rosenberg, L.; Paraskevas, S.; Maysinger, D. Inhibition of caspase-mediated PARP-1 cleavage results in increased necrosis in isolated islets of Langerhans. J. Mol. Med. 82(6):389-397; 2004.
4. Alexandraki, K.; Piperi, C.; Kalofoutis, C.; Singh, J.; Alaveras, A.; Kalofoutis, A. Inflammatory process in type 2 diabetes: The role of cytokines. Ann. NY Acad. Sci. 1084:89-117; 2006.
5. 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.
6. Barnett, M. J.; McGhee-Wilson, D.; Shapiro, A. M.; Lakey, J. R. Variation in human islet viability based on different membrane integrity stains. Cell Transplant. 13(5):481-488; 2004.
7. Berney, T.; Molano, R. D.; Cattan, P.; Pileggi, A.; Vizzardelli, C.; Oliver, R.; Ricordi, C.; Inverardi, L. Endotoxin-mediated delayed islet graft function is associated with increased intra-islet cytokine production and islet cell apoptosis. Transplantation 71(1):125-132; 2001.
8. Berney, T.; Molano, R. D.; Pileggi, A.; Cattan, P.; Vizzardelli, C.; Ricordi, C.; Inverardi, L. Absence of CSF-1-dependent macrophages does not improve function of transplanted islets of Langerhans. Cell Transplant. 10(7):633-637; 2001.
9. Cai, F.; Li, C. R.; Wu, J. L.; Chen, J. G.; Liu, C.; Min, Q.; Yu, W.; Ouyang, C. H.; Chen, J. H. Theaflavin ameliorates cerebral ischemia-reperfusion injury in rats through its anti-inflammatory effect and modulation of STAT-1. Mediators Inflamm. 2006(5):30490; 2006.
10. Campbell, I. L.; Hobbs, M. V.; Dockter, J.; Oldstone, M. B.; Allison, J. Islet inflammation and hyperplasia induced by the pancreatic islet-specific overexpression of interleukin-6 in transgenic mice. Am. J. Pathol. 145(1):157-166; 1994.
11. Cardozo, A. K.; Heimberg, H.; Heremans, Y.; Leeman, R.; Kutlu, B.; Kruhoffer, M.; Orntoft, T.; Eizirik, D. L. A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic beta-cells. J. Biol. Chem. 276(52):48879-48886; 2001.
12. Cattan, P.; Berney, T.; Schena, S.; Molano, R. D.; Pileggi, A.; Vizzardelli, C.; Ricordi, C.; Inverardi, L. Early assessment of apoptosis in isolated islets of Langerhans. Transplantation 71(7):857-862; 2001.
13. Depeint, F.; Bruce, W. R.; Shangari, N.; Mehta, R.; O'Brien, P. J. Mitochondrial function and toxicity: Role of the B vitamin family on mitochondrial energy metabolism. Chem. Biol. Interact. 163(1-2):94-112; 2006.
14. de Souza, A. C.; Kodach, L.; Gadelha, F. R.; Bos, C. L.; Cavagis, A. D.; Aoyama, H.; Peppelenbosch, M. P.; Ferreira, C. V. A promising action of riboflavin as a mediator of leukaemia cell death. Apoptosis 11(10):1761-1771; 2006.
15. Emamaullee, J. A.; Shapiro, A. M. Factors influencing the loss of beta-cell mass in islet transplantation. Cell Transplant. 16(1):1-8; 2007.
16. Floersheim, G. L. Allopurinol, indomethacin and riboflavin enhance radiation lethality in mice. Radiat. Res. 139(2):240-247; 1994.
17. Fornoni, A.; Cobianchi, L.; Sanabria, N. Y.; Pileggi, A.; Molano, R. D.; Ichii, H.; Rosero, S.; Inverardi, L.; Ricordi, C.; Pastori, R. L. The 1-isoform but not d-isoforms of a JNK inhibitory peptide protects pancreatic beta-cells. Biochem. Biophys. Res. Commun. 354(1):227-233; 2007.
18. Gopalakrishnan, A.; Xu, C. J.; Nair, S. S.; Chen, C.; Hebbar, V.; Kong, A. N. Modulation of activator protein-1 (AP-1) and MAPK pathway by flavonoids in human prostate cancer PC3 cells. Arch. Pharm. Res. 29(8):633-644; 2006.
19. Heinrich, P. C.; Behrmann, I.; Haan, S.; Hermanns, H. M.; Muller-Newen, G.; Schaper, F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374(Pt. 1):1-20; 2003.
20. Ichii, H.; Inverardi, L.; Pileggi, A.; Molano, R. D.; Cabrera, O.; Caicedo, A.; Messinger, S.; Kuroda, Y.; Berggren, P. O.; Ricordi, C. A novel method for the assessment of cellular composition and Beta-cell viability in human islet preparations. Am. J. Transplant. 5(7):1635-1645; 2005.
21. Iwanaga, K.; Hasegawa, T.; Hultquist, D. E.; Harada, H.; Yoshikawa, Y.; Yanamadala, S.; Liao, H.; Visovatti, S. H.; Pinsky, D. J. Riboflavin-mediated reduction of oxidant injury, rejection, and vasculopathy after cardiac allotransplantation. Transplantation 83(6):747-753; 2007.
22. Johansson, A.; Sandvik, D.; Carlsson, P. O. Inhibition of p38 MAP kinase in the early posttransplantation phase redistributes blood vessels from the surrounding stroma into the transplanted endocrine tissue. Cell Transplant. 15(6):483-488; 2006.
23. Juang, J. H.; Hsu, B. R.; Kuo, C. H.; Uengt, S. W. Beneficial effects of hyperbaric oxygen therapy on islet transplantation. Cell Transplant. 11(2):95-101; 2002.
24. Klein, D.; Ribeiro, M. M.; Mendoza, V.; Jayaraman, S.; Kenyon, N. S.; Pileggi, A.; Molano, R. D.; Inverardi, L.; Ricordi, C.; Pastori, R. L. Delivery of Bcl-XL or its BH4 domain by protein transduction inhibits apoptosis in human islets. Biochem. Biophys. Res. Commun. 323(2):473-478; 2004.
25. Kodama, K.; Suzuki, M.; Toyosawa, T.; Araki, S. Inhibitory mechanisms of highly purified vitamin B2 on the productions of proinflammatory cytokine and NO in endotoxin-induced shock in mice. Life Sci. 78(2):134-139; 2005.
26. Kristiansen, O. P.; Mandrup-Poulsen, T. Interleukin-6 and diabetes: The good, the bad, or the indifferent? Diabetes 54(Suppl. 2):S114-124; 2005.
27. Latif, Z. A.; Noel, J.; Alejandro, R. A simple method of staining fresh and cultured islets. Transplantation 45(4):827-830; 1988.
28. Mack, C. P.; Hultquist, D. E.; Shlafer, M. Myocardial flavin reductase and riboflavin: a potential role in decreasing reoxygenation injury. Biochem. Biophys. Res. Commun. 212(1):35-40; 1995.
29. Matsuda, T.; Omori, K.; Vuong, T.; Pascual, M.; Valiente, L.; Ferreri, K.; Todorov, I.; Kuroda, Y.; Smith, C. V.; Kandeel, F.; et al. 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.
30. Nagata, N.; Gu, Y.; Hori, H.; Balamurugan, A. N.; Touma, M.; Kawakami, Y.; Wang, W.; Baba, T. T.; Satake, A.; Nozawa, M.; Tabata, Y.; Inoue, K. Evaluation of insulin secretion of isolated rat islets cultured in extracellular matrix. Cell Transplant. 10(4-5):447-451; 2001.
31. Omori, K.; Valiente, L.; Orr, C.; Rawson, J.; Ferreri, K.; Todorov, I.; Medicherla, S.; Protter, A. A.; Schreiner, G. F.; Riggs, A. D.; et al. Inhibition of p38 mitogen-activated protein kinase protects human islets from cryoinjury and improves the yield, viability, and quality of frozen-thawed islets. Transplant. Proc. 37(8):3422-3423; 2005.
32. Paraskevas, S.; Aikin, R.; Maysinger, D.; Lakey, J. R.; Cavanagh, T. J.; Agapitos, D.; Wang, R.; Rosenberg, L. Modulation of JNK and p38 stress activated protein kinases in isolated islets of Langerhans: insulin as an autocrine survival signal. Ann. Surg. 233(1):124-133; 2001.
33. Paraskevas, S.; Aikin, R.; Maysinger, D.; Lakey, J. R.; Cavanagh, T. J.; Hering, B.; Wang, R.; Rosenberg, L. Activation and expression of ERK, JNK, and p38 MAP-kinases in isolated islets of Langerhans: Implications for cultured islet survival. FEBS Lett. 455(3):203-208; 1999.
34. Pileggi, A.; Cobianchi, L.; Inverardi, L.; Ricordi, C. Overcoming the challenges now limiting islet transplantation: a sequential, integrated approach. Ann. NY Acad. Sci. 1079:383-398; 2006.
35. Pileggi, A.; Molano, R. D.; Ricordi, C.; Zahr, E.; Collins, J.; Valdes, R.; Inverardi, L. Reversal of diabetes by pancreatic islet transplantation into a subcutaneous, neovascularized device. Transplantation 81(9):1318-1324; 2006.
36. Pilstrom, B.; Bjork, L.; Bohme, J. Demonstration of a TH1 cytokine profile in the late phase of NOD insulitis. Cytokine 7(8):806-814; 1995.
37. Ponte, G. M.; Pileggi, A.; Messinger, S.; Alejandro, A.; Ichii, H.; Baidal, D. A.; Khan, A.; Ricordi, C.; Goss, J. A.; Alejandro, R. Toward maximizing the success rates of human islet isolation: Influence of donor and isolation factors. Cell Transplant. 16(6):595-607; 2007.
38. Richards, S. K.; Parton, L. E.; Leclerc, I.; Rutter, G. A.; Smith, R. M. Over-expression of AMP-activated protein kinase impairs pancreatic {beta}-cell function in vivo. J. Endocrinol. 187(2):225-235; 2005.
39. Rose, N. L.; Palcic, M. M.; Shapiro, A. M.; Lakey, J. R. Endogenous pancreatic enzyme activity levels show no significant effect on human islet isolation yield. Cell Transplant. 13(2):153-160; 2004.
40. 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.
41. Ruiz, P. A.; Braune, A.; Holzlwimmer, G.; Quintanilla-Fend, L.; Haller, D. Quercetin inhibits TNF-induced NF-{kappa}B transcription factor recruitment to proinflammatory gene promoters in murine intestinal epithelial cells. J. Nutr. 137(5):1208-1215; 2007.
42. Salehi, P.; Mirbolooki, M.; Kin, T.; Tsujimura, T.; Shapiro, A. M.; Churchill, T. A.; Lakey, J. R. Ameliorating injury during preservation and isolation of human islets using the two-layer method with perfluorocarbon and UW solution. Cell Transplant. 15(2):187-194; 2006.
43. Seekamp, A.; Hultquist, D. E.; Till, G. O. Protection by vitamin B2 against oxidant-mediated acute lung injury. Inflammation 23(5):449-460; 1999.
44. Shida, Y.; Igawa, T.; Hakariya, T.; Sakai, H.; Kanetake, H. p38MAPK activation is involved in androgen-independent proliferation of human prostate cancer cells by regulating IL-6 secretion. Biochem. Biophys. Res. Commun. 353(3):744-749; 2007.
45. Toyosawa, T.; Suzuki, M.; Kodama, K.; Araki, S. Effects of intravenous infusion of highly purified vitamin B2 on lipopolysaccharide-induced shock and bacterial infection in mice. Eur. J. Pharmacol. 492(2-3):273-280; 2004.
46. Toyosawa, T.; Suzuki, M.; Kodama, K.; Araki, S. Highly purified vitamin B2 presents a promising therapeutic strategy for sepsis and septic shock. Infect. Immun. 72(3):1820-1823; 2004.
47. Verdrengh, M.; Tarkowski, A. Riboflavin in innate and acquired immune responses. Inflamm. Res. 54(9):390-393; 2005.
48. Wadt, K. A.; Larsen, C. M.; Andersen, H. U.; Nielsen, K.; Karlsen, A. E.; Mandrup-Poulsen, T. Ciliary neurotrophic factor potentiates the beta-cell inhibitory effect of IL-1beta in rat pancreatic islets associated with increased nitric oxide synthesis and increased expression of inducible nitric oxide synthase. Diabetes 47(10):1602-1608; 1998.
49. Wang, L.; Tu, Y. C.; Lian, T. W.; Hung, J. T.; Yen, J. H.; Wu, M. J. Distinctive antioxidant and antiinflammatory effects of flavonols. J. Agric. Food Chem. 54(26):9798-9804; 2006.
50. Wollensak, G.; Sporl, E.; Reber, F.; Pillunat, L.; Funk, R. Corneal endothelial cytotoxicity of riboflavin/UVA treatment in vitro. Ophthalmic Res. 35(6):324-328; 2003.
51. Yonekawa, Y.; Matsumoto, S.; Okitsu, T.; Arata, T.; Iwanaga, Y.; Noguchi, H.; Nagata, H.; O'Neil, J. J.; Tanaka, K. Effective islet isolation method with extremely high islet yields from adult pigs. Cell Transplant. 14(10):757-762; 2005.
52. Zampetaki, A.; Zhang, Z.; Hu, Y.; Xu, Q. Biomechanical stress induces IL-6 expression in smooth muscle cells via Ras/Rac1-p38 MAPK-NF-kappaB signaling pathways. Am. J. Physiol. Heart Circ. Physiol. 288(6):H2946-2954; 2005.