Mesobiliverdin IXα enhances rat pancreatic islet yield and function

Frontiers in Pharmacology

Volumn 4 APR, Issue , 2013, Pages

  Ito, Taihei ^a   Chen, Dong ^b,c   Chang, Cheng Wei Tom ^b   Kenmochi, Takashi ^a   Saito, Tomonori ^d   Suzuki, Satoshi ^e   Takemoto, Jon Y ^b  

^a FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UTAH STATE UNIVERSITY   (United States)

^c Utah State University   (United States)

^d SAKURA NATIONAL HOSPITAL   (Japan)

^e BUILDING RESEARCH INSTITUTE   (Japan)

Author keywords

Anti inflammatory; Biliverdin; Islet transplantation; Mesobiliverdin; Pancreatic islets

Indexed keywords

ANTIINFLAMMATORY AGENT; BILIVERDIN; BILIVERDIN REDUCTASE; MESOBILIVERDIN IXALPHA; OXIDOREDUCTASE; PHYCOCYANOBILIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYANOBACTERIUM; DIABETES MELLITUS; DOSE RESPONSE; DRUG IDENTIFICATION; DRUG PURITY; DRUG SYNTHESIS; GLUCOSE BLOOD LEVEL; INTRAVENOUS GLUCOSE TOLERANCE TEST; LIVER; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS TRANSPLANTATION; RAT; STREPTOZOCIN DIABETES;

EID: 84881516515     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2013.00050     Document Type: Article

References (49)

1. Bellner, L., Wolstein, J., Patil, K. A., Dunn, M. W., and Laniado-Schwartzman, M. (2011). Biliverdin rescues the HO-2 null mouse phenotype of unresolved chronic inflammation following corneal epithelial injury. Invest. Ophthalmol. Vis. Sci. 52, 3246-3253.
2. Beuhler, R. J., Pierce, R. C., Friedman, L., and Siegelman, H. W. (1976). Cleavage of phycocyanobilin from C-phycocyanin. Separation and mass spectral identification of the products. J. Biol. Chem. 251, 2405-2411.
3. Chen, D., Brown, J. D., Kawasaki, Y., Bommer, J., and Takemoto, J. Y. (2012). Scalable production of biliverdin IXalpha by Escherichia coli. BMC Biotechnol. 12:89. doi:10.1186/1472-6750-12-89
4. Ching, C. D., Harland, R. C., Collins, B. H., Kendall, W., Hobbs, H., and Opara, E. C. (2001). A reliable method for isolation of viable porcine islet cells. Arch. Surg. 136, 276-279.
5. Cunningham, O., Dunne, A., Sabido, P., Lightner, D., and Mantle, T. J. (2000). Studies on the specificity of the tetrapyrrole substrate for human biliverdin-IXalpha reductase and biliverdin-IXbeta reductase. Structure-activity relationships define models for both active sites. J. Biol. Chem. 275, 19009-19017.
6. Emamaullee, J. A., and Shapiro, A. M. J. (2006). Interventional strategies to prevent beta-cell apoptosis in islet transplantation. Diabetes 55, 1907-1914.
7. Fiedor, P., Walaszewski, J., Oluwole, S. F., Licinska, I., Mazurek, A. P., Hardy, M. A., et al. (1996). A novel approach to in vivo visualization of human pancreatic islets. Transplant. Proc. 28, 3514.
8. Florczyk, U. M., Jozkowicz, A., and Dulak, J. (2008). Biliverdin reductase: new features of an old enzyme and its potential therapeutic significance. Pharmacol. Rep. 60, 38-48.
9. Fondevila, C., Katori, M., Lassman, C., Carmody, I., Busuttil, R. W., Bach, F. H., et al. (2003). Biliverdin protects rat livers from ischemia/reperfusion injury. Transplant. Proc. 35, 1798-1799.
10. Fu, G., Liu, H., and Doerksen, R. J. (2012). Molecular modeling to provide insight into the substrate binding and catalytic mechanism of human biliverdin-IXalpha reductase. J. Phys. Chem. B 116, 9580-9594.
11. Fujii, M., Inoguchi, T., Sasaki, S., Maeda, Y., Zheng, J., Kobayashi, K., et al. (2010). Bilirubin and biliverdin protect rodents against diabetic nephropathy by downregulating NAD(P)H oxidase. Kidney Int. 78, 905-919.
12. Gibbs, P. E., Tudor, C., and Maines, M. D. (2012). Biliverdin reductase: more than a namesake -the reductase, its peptide fragments, and biliverdin regulate activity of the three classes of protein kinase C. Front. Pharmacol. 3:31. doi:10.3389/fphar.2012.00031
13. Gibbs, P. E. M., and Maines, M. D. (2007). Biliverdin inhibits activation of NF-?B: reversal of inhibition by human biliverdin reductase. Int. J. Cancer 121, 2567-2574.
14. Greenberg, A. J., Bossenmaier, I., and Schwartz, S. (1971). Green jaundice. A study of serum biliverdin, mesobiliverdin and other green pigments. Am. J. Dig. Dis. 16, 873-880.
15. Hansen, W., Christie, M. R., Kahn, R., Norgaard, A., Abel, I., Petersen, A. M., et al. (1989). Supravital dithizone staining in the isolation of human and rat pancreatic islets. Diabetes Res. 10, 53-57.
16. Ikeda, N., Inoguchi, T., Sonoda, N., Fujii, M., Takei, R., Hirata, E., et al. (2011). Biliverdin protects against the deterioration of glucose tolerance in db/db mice. Diabetologia 54, 2183-2191.
17. Ito, T., Itakura, S., Todorov, I., Rawson, J., Asari, S., Shintaku, J., et al. (2010). Mesenchymal stem cell and islet co-transplantation promotes graft revascularization and function. Transplantation 89, 1438-1445.
18. Ito, T., Omori, K., Rawson, J., Todorov, I., Asari, S., Kuroda, A., et al. (2008). Improvement of canine islet yield by donor pancreas infusion with a p38MAPK inhibitor. Transplantation 86, 321-329.
19. Kapitulnik, J., and Maines, M. D. (2012). The role of bile pigments in health and disease: effects on cell signaling, cytotoxicity and cytoprotection. Front. Pharmacol. 3:136. doi:10.3389/fphar.2012.00136
20. Kenmochi, T., Maruyama, M., Saigo, K., Akutsu, N., Iwashita, C., Otsuki, K., et al. (2008). Successful islet transplantation from the pancreata of non-heart-beating donors. Transplant. Proc. 40, 2568-2570.
21. Matsumoto, S., Noguchi, H., Naziruddin, B., Onaca, N., Jackson, A., Nobuyo, H., et al. (2007). Improvement of pancreatic islet cell isolation for transplantation. Proc. (Bayl. Univ. Med. Cent.) 20, 357-362.
22. McDonagh, A. F. (2001). Turning green to gold. Nat. Struct. Biol. 8, 198-200.
23. McDonagh, A. F. (2005). Biliverdin, immune-mediated liver injury, and the gigo effect. Hepatology 41, 680-681.
24. McPhee, F., Caldera, P. S., Bemis, G. W., Mcdonagh, A. F., Kuntz, I. D., and Craik, C. S. (1996). Bile pigments as HIV-1 protease inhibitors and their effects on HIV-1 viral maturation and infectivity in vitro. Biochem. J. 320, 681-686.
25. Najarian, J. S., Sutherland, D. E., Matas, A. J., Steffes, M. W., Simmons, R. L., and Goetz, F. C. (1977). Human islet transplantation: a preliminary report. Transplant. Proc. 9, 233-236.
26. Nakagami, T., Taji, S., Takahashi, M., and Yamanishi, K. (1992). Antiviral activity of a bile pigment, biliverdin, against human herpesvirus 6 (HHV-6) in vitro. Microbiol. Immunol. 36, 381-390.
27. Nakao, A., Murase, N., Ho, C., Toyokawa, H., Billiar, T. R., and Kanno, S. (2005). Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury. Circulation 112, 587-591.
28. Nakao, A., Otterbein, L. E., Overhaus, M., Sarady, J. K., Tsung, A., Kimizuka, K., et al. (2004). Biliverdin protects the functional integrity of a transplanted syngeneic small bowel. Gastroenterology 127, 595-606.
29. Ollinger, R., Bilban, M., Erat, A., Froio, A., Mcdaid, J., Tyagi, S., et al. (2005). Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 112, 1030-1039.
30. Overhaus, M., Moore, B. A., Barbato, J. E., Behrendt, F. F., Doering, J. G., and Bauer, A. J. (2006). Biliverdin protects against polymicrobial sepsis by modulating inflammatory mediators. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G695-703.
31. Pachori, A. S., Smith, A., Mcdonald, P., Zhang, L., Dzau, V. J., and Melo, L. G. (2007). Heme-oxygenase-1-induced protection against hypoxia/reoxygenation is dependent on biliverdin reductase and its interaction with PI3K/Akt pathway. J. Mol. Cell. Cardiol. 43, 580-592.
32. Ribeiro, M. M., Klein, D., Pileggi, A., Molano, R. D., Fraker, C., Ricordi, C., et al. (2003). Heme oxygenase-1 fused to a TAT peptide transduces and protects pancreatic beta-cells. Biochem. Biophys. Res. Commun. 305, 876-881.
33. Ryan, E. A., Paty, B. W., Senior, P. A., and Shapiro, A. M. (2004). Risks and side effects of islet transplantation. Curr. Diab. Rep. 4, 304-309.
34. Sarady-Andrews, J. K., Liu, F., Gallo, D., Nakao, A., Overhaus, M., Ollinger, R., et al. (2005). Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L1131-L1137.
35. Sedlak, T. W., and Snyder, S. H. (2004). Bilirubin benefits: cellular protection by a biliverdin reductase antioxidant cycle. Pediatrics 113, 1776-1782.
36. Shapiro, A. M., Lakey, J. R., Paty, B. W., Senior, P. A., Bigam, D. L., and Ryan, E. A. (2005). Strategic opportunities in clinical islet transplantation. Transplantation 79, 1304-1307.
37. Shapiro, A. M. J., Lakey, J. R. T., Ryan, E. A., Korbutt, G. S., Toth, E., Warnock, G. L., et al. (2000). Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Eng. J. Med. 343, 230-238.
38. Soares, M. P., and Bach, F. H. (2009). Heme oxygenase-1: from biology to therapeutic potential. Trends Mol. Med. 15, 50-58.
39. Stocker, R., Yamamoto, Y., Mcdonagh, A., Glazer, A., and Ames, B. (1987). Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046.
40. Terry, M. J., Maines, M. D., and Lagarias, J. C. (1993). Inactivation of phytochrome-and phycobiliprotein-chromophore precursors by rat liver biliverdin reductase. J. Biol. Chem. 268, 26099-26106.
41. Tiribelli, C., and Ostrow, J. D. (2005). Intestinal flora and bilirubin. J. Hepatol. 42, 170-172.
42. Vitek, L., Majer, F., Muchova, L., Zelenka, J., Jiraskova, A., Branny, P., et al. (2006). Identification of bilirubin reduction products formed by Clostridium perfringens isolated from human neonatal fecal flora. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 833, 149-157.
43. Wang, H., Ferran, C., Attanasio, C., Calise, F., and Otterbein, L. E. (2011). Induction of protective genes leads to islet survival and function. J. Transplant. 2011, 141898.
44. Wegiel, B., Baty, C. J., Gallo, D., Csizmadia, E., Scott, J. R., Akhavan, A., et al. (2009). Cell surface biliverdin reductase mediates biliverdin-induced anti-inflammatory effects via phosphatidylinositol 3-kinase and Akt. J. Biol. Chem. 284, 21369-21378.
45. Wegiel, B., and Otterbein, L. (2012). Go green: the antiinflammatory effects of biliverdin reductase. Front. Pharmacol. 3:47. doi:10.3389/fphar.2012.00047
46. Yamashita, K., Mcdaid, J., Ollinger, R., Tsui, T.-Y., Berberat, P. O., Usheva, A., et al. (2004). Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J. 18, 765-767.
47. Zheng, J., Inoguchi, T., Sasaki, S., Maeda, Y., Mccarty, M., Fujii, M., et al. (2012). Phycocyanin and phycocyanobilin from Spirulina platensis protect against diabetic nephropathy by inhibiting oxidative stress. Am. J. Physiol. Regul. Comp. Physiol 304, R110-R120.
48. Zhou, H., Qian, H., Liu, J., Zhu, D., Ding, W., Pan, P., et al. (2011). Protection against lung graft injury from brain-dead donors with carbon monoxide, biliverdin, or both. J. Heart Lung Transplant. 30, 460-466.
49. Zhu, Z., Wilson, A. T., Luxon, B. A., Brown, K. E., Mathahs, M. M., Bandyopadhyay, S., et al. (2010). Biliverdin inhibits hepatitis C virus nonstructural 3/4A protease activity: mechanism for the antiviral effects of heme oxygenase? Hepatology 52, 1897-1905.