The oxidoreductase, biliverdin reductase, is induced in human renal carcinoma - pH and cofactor-specific increase in activity

Journal of Urology

Volumn 162, Issue 4, 1999, Pages 1467-1472

  Maines, Mahin D ^a,b   Mayer, Robert D ^a   Erturk, Erdal ^a   Huang, Tian J ^a   Disantagnese, Anthony ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Bilirubin; Biliverdin reductase; Heme degradation productions; Kidney cancer

Indexed keywords

BILIVERDIN; OXIDOREDUCTASE;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; HUMAN; HUMAN TISSUE; IMMUNOREGULATION; KIDNEY CARCINOMA; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0032856531     PISSN: 00225347     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-5347(05)68342-5     Document Type: Article

References (45)

1. Kutty, R. K. and Maines, M. D.: Purification and characterization of biliverdin reductase from the rat liver. J. Biol. Chem., 256: 3956, 1981.
2. Huang, T. J., Trakshel, G. M. and Maines, M. D.: Detection often variants of biliverdin reductase in rat liver by two-dimensional gel electrophoresis. J. Biol. Chem., 264: 7844, 1989.
3. Maines, M. D.: Heme Oxygenase: Clinical Applications and Functions. CRC Press Inc.: Boca Raton, FL, 1992.
4. Fakhrai, H. and Maines, M. D.: Expression and characterization of a cDNA for rat kidney biliverdin reductase: evidence suggesting the liver and kidney enzymes are the same transcript product. J. Biol. Chem., 267: 4023, 1992.
5. Maines, M. D., Polevoda, B. V., Huang, T. J. and McCoubrey, W. K. Jr.: Human biliverdin IXα reductase is a zinc-metalloprotein; characterization of purified and Escherichia coli expressed enzymes. Eur. J. Biochem., 235: 372, 1996.
6. Nakagami, T., Taji, S., Takahashi, M. and Yamanishi, K.: Antiviral activity of a bile pigment, biliverdin, against human herpes virus 6 (HH6) in vitro. Microbial Immunol., 36: 381, 1992.
7. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N. and Ames, B. N.: Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043, 1987.
8. Stocker, R. and Ames, B. N.: Potential role of conjugated bilirubin and copper in the metabolism of lipid peroxides in bile. Proc. Nat. Acad. Sci. USA, 84: 8130, 1987.
9. Haga, Y., Tempero, M. A., Kay, D. and Zetterman, R. K.: Intracellular accumulation of unconjugated bilirubin inhibits phytohemagglutinin-induced proliferation and interleukin-2 production of human lymphocytes. Digestive Dis. Sci., 41: 1468, 1996.
10. Haga, Y., Tempero, M. A. and Zetterman, R. K.: Unconjugated bilirubin inhibits in vitro major histocompatibility complex-unrestricted cytotoxicity in human lymphocytes. Biochim. Biophys. Acta, 1316: 29, 1996.
11. Troy, A. J., Summers, K. L., Davidson, P. J., Atkinson, C. H. and Hart, D. N.: Minimal recruitment and activation of dendritic cells within renal cell carcinoma. Clin. Cancer Res., 4: 585, 1998.
12. Kolenko, V., Wang, Q., Riedy, M. C., O'Shea, J., Ritz, J., Cathcart, M. K., Rayman, P, Tubbs, R., Edinger, M., Novick, A., Bukowski, R. and Finke, J.: Tumor-induced suppression of T lymphocyte proliferation coincides with inhibition of Jak3 expression and IL-2 receptor signaling: role of soluble products from human renal cell carcinomas. J. Immunol., 159: 3057, 1997.
13. Sano, K., Nakamura, H. and Matsuo, T.: Mode of inhibitory action of bilirubin on protein kinase C. Pediatr. Res., 19: 587, 1985.
14. Kwak, J. Y., Takeshiege, K., Cheung, B. S. and Minakami, S.: Bilirubin inhibits the activation of superoxide-producing NADPH oxidase in a neutrophil ce411-free system. Biochim. Biophys. Acta, 1076: 369, 1991.
15. Hansen, T. W., Mathiesen, S. B. and Walaas, S. I.: Bilirubin has widespread inhibitory effects on protein phosphorylation. Ped. Res., 39: 1072, 1996.
16. Nishizuka, Y.: The molecular heterogeneity of protein kinase c and its implications for cellular regulation. Nature, 334: 661, 1988.
17. Keryer, G., Celati, C. and Klotz, C.: In isolated human centrosomes, the associated kinases phosphorylate a specific subset of centrosomal proteins. Biol. Cell, 84: 155, 1995.
18. Moore, D. J., Chueh, P. J. and Morre, D. M.: Capsaicin inhibits preferentially the NADH oxidase and growth of transformed cells in culture. Proc. Natl. Acad. Sci. USA, 92: 1831, 1995.
19. Wolvetang, E. J., Larm, J. A., Moutsoulas, P. and Lawen, A.: Apoptosis induced by inhibitors of the plasma membrane NADH-oxidase involves Bcl-2 and calcineurin. Cell Growth Diff., 7: 1315, 1996.
20. Hopkins, P. N., Wu, L. L., Hunt, S. C., James, B. C., Vincen, G. M. and Williams, R. R.: Higher serum bilirubin as associated with decreased risk for early familial coronary artery disease. Arterioscler. Thromb. Vasc. Biol., 16: 250, 1996.
21. Huang, T. J., Trakshel, G. M. and Maines, M. D.: Microheterogeneity of biliverdin reductase in rat liver and spleen.: selective suppression of enzyme variants in liver by bromobenzene. Arch. Biochem. Biophys., 274: 617, 1989.
22. Huang, T. J. and Maines, M. D.: Bromobenzene-mediated alteration in activity and electrophoretic pattern of biliverdin reductase variants in rat kidney. Mol. Pharmacol., 37: 25, 1990.
23. Ewing, J. F., Weber, C. M. and Maines, M. D.: Biliverdin reductase is heat resistant and co-expressed with constitutive and heat shock form of heme oxygenase. J. Neurochem., 61: 1015, 1993.
24. Kingston, R. E.: Preparation of poly(A)+ RNA. In: Current Protocols in Molecular Biology. Edited by Ausubel, F. M., Brent, R., Moore, D. D., Smith, J. A. and Seidman, J. G. Wiley and Sons: New York, p. 451, 1987.
25. Maines, M. D. and Abrahamsson, P. A.: Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic and tumor tissue distribution, Urology, 47: 727, 1996.
26. Minty, A. J., Caravatti, M., Robert, B., Cohen, A., Daubar, P., Weydert, A., Gros, F. and Buckingham, M. E.: Mouse actin messenger RNAs. J. Biol. Chem., 256: ,1008, 1981.
27. Sambrook, J., Fritsch, E. F. and Maniatis, T.: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory: Cold Spring Harbor, NY, 1982.
28. Maines, M. D. and Trakshel, G. M.: Purification and characterization of human biliverdin reductase. Arch. Biochem. Biophys., 300: 320, 1993.
29. Laemmli, U. K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680, 1970.
30. Towbin, H., Staehelin, T. and Gordon, J.: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Nat. Acad. Sci. USA., 76: 4350, 1979.
31. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J.: Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193: 265, 1951.
32. Ewing, J. F. and Maines, M. D.: Immunohistochemical localization of biliverdin reductase in rat brain: age related expression of protein and transcript. Brain Res., 672: 29, 1995.
33. Davis, N. S., DiSant'Agnese, P. A., Ewing, J. F. and Mooney, R. A.: The neuroendocrine prostate: characterization and quantitationof calcitonin in the human gland. J. Urol., 142: 884-888, 1989.
34. Marks, G. S., Brien, J. F., Nakatsu, K. and McLaughlin, B. E.: Does carbon monoxide have a physiological function? Trends Pharmacol. Sci., 12: 185, 1991.
35. Willis, D., Moore, A. R., Frederick, R. and Willoughby, D. A.: Heme oxygenase: a novel target for the modulation of the imflammatory response. Nature Med., 2: 87, 1996.
36. Maines, M. D.: The heme oxygenase system: a regulator of second messenger gases. Ann. Rev. Pharmacol. Toxicol., 37: 517, 1997.
37. Woo, J., Iyer, S., Conrejo, M-C., Mori, N., Gao, L., Maines, M. D. and Buelow, R.: Stress protein induced immunosuppression: inhibition of cellular immune effector functions following overexpression of heme oxygenase-1 (hsp 32). Transplant Immunol., 6: 84-93, 1998.
38. Goodman, A. I., Choudhury, M., deSilva, J. L., Schwartzman, M. L. and Abraham, N. G.: Overexpression of the heme oxygenase gene in renal cell carcinoma. Proc. Soc. Exp. Biol. Med., 214: 54, 1997.
39. Linn, S.: DNA damage by iron and hydrogen peroxide in vitro and in vivo. Drug Metab. Dis., 30: 313, 1988.
40. Althaus, R. and Richter, C.: ADP-ribosylation of proteins. Enzymology and biological significance. Mol. Biol. Biochem. Biophys., 37: 1, 1987.
41. Lautier, D., Lagueux, J., Thibodeau, J., Menard, L. and Pairier, G. G.: Molecular and biochemical features of poly(ADP-ribose) metabolism. Mol. Cell. Biochem., 122: 171, 1993.
42. deMurcia, G.: A structure and function of poly(ADP-ribose) polymerase. Mol. Cell. Biochem., 138: 15, 1994.
43. Berger, N. A.: Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res., 101: 4, 1985.
44. Eliasson, M. J. L., Sampei, K., Mandir, A. S., Hurn, P. D., Traystman, R. J., Bao, J., Pieper, A., Wang, Z-Q., Dawson, T. M., Snyder, S. H. and Dawson, V. L.: Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med., 3: 1089, 1997.
45. Endres, M., Wang, Z-Q., Namura, S., Waeber, C. and Moskowitz, M. A.: Ischemic brain injury is mediated by the activation of poly(ADP-ribose) polymerase. J. Cereb. Blood Flow Metab., 17: 1143, 1997.