The nitric oxide scavenger cobinamide profoundly improves survival in a Drosophila melanogaster model of bacterial sepsis

FASEB Journal

Volumn 20, Issue 11, 2006, Pages 1865-1873

  Broderick, Kate E ^a   Feala, Jake ^b   McCulloch, Andrew ^b   Paternostro, Giovanni ^c   Sharma, Vijay S ^a   Pilz, Renate B ^a   Boss, Gerry R ^a,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cardiac function; Cobalamin; Septic shock

Indexed keywords

ANTIBIOTIC AGENT; COBINAMIDE; CYANOCOBALAMIN; GENTAMICIN; LIPOPOLYSACCHARIDE; NITRIC OXIDE; COBAMAMIDE; DROSOPHILA PROTEIN; IMMUNE DEFICIENCY PROTEIN, DROSOPHILA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DROSOPHILA MELANOGASTER; DRUG MECHANISM; DRUG POTENTIATION; ESCHERICHIA COLI; HEART FUNCTION; IMMUNE DEFICIENCY; NONHUMAN; PRIORITY JOURNAL; SEPSIS; STAPHYLOCOCCUS AUREUS; SURVIVAL; ANIMAL; BACTEREMIA; DIET SUPPLEMENTATION; DRUG EFFECT; ENTEROBACTER INFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SEPTIC SHOCK; STAPHYLOCOCCUS INFECTION;

ANIMALIA; BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER;

ANIMALS; BACTEREMIA; COBAMIDES; DIETARY SUPPLEMENTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; SHOCK, SEPTIC; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 33748668209     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-5780com     Document Type: Article

References (47)

1. Marshall, J. C. (2003) Such stuff as dreams are made on: Mediator-directed therapy in sepsis. Nat. Rev. Drug Discovery 2, 391-405
2. Clancy, R. M., and Abramson, S. B. (1995) Nitric oxide: a novel mediator of inflammation. Proc. Soc. Exp. Biol. Med. 210
3. Poon, B. Y., Raharjo, E., Patel, K. D., Tavener, S., and Kubes, P. (2003) Complexity of inducible nitric oxide synthase - Cellular source determines benefit versus toxicity. Circulation 108, 1107-1112
4. Nathan, C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051-3064
5. Moncada, S., and Higgs, A. (1993) The L-arginine-nitric oxide pathway. New Engl. J. Med. 329, 2002-2012
6. Kim, H. W., and Greenburg, A. G. (2002) Nitric oxide scavenging, alone or with nitric oxide synthesis inhibition, modulates vascular hyporeactivity in rats with intraperitoneal sepsis. Shock 17, 423-426
7. Spain, D. A., Wilson, M. A., Bar-Natan, M. F., and Garrison, R. N. (1994) Nitric oxide synthase inhibition aggravates intestinal microvascular vasoconstriction and hypoperfusion of bacteremia. J. Trauma 36, 720-725
8. Lopez, A., Lorente, J. A., Steingrub, J., Bakker, J., McLuckie, A., Willatts, S., Brockway, M., Anzueto, A., Holzapfel, L., Breen, D., et al. (2004) Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit. Care Med. 32, 21-30
9. Ichinose, F., Hataishi, R., Wu, J. C., Kawai, N., Rodrigues, A. C. T., Mallari, C., Post, J. M., Parkinson, J. F., Picard, M. H., Bloch, K. D., and Zapol, W. M. (2003) A selective inducible NOS dimerization inhibitor prevents systemic, cardiac, and pulmonary hemodynamic dysfunction in endotoxemic mice. Am. J. Physiol. 285, H2524-H2530
10. Price, S., Mitchell, J. A., Anning, P. B., and Evans, T. W. (2003) Type II nitric oxide synthase activity is cardio-protective in experimental sepsis. Eur. J. Pharmacol. 472, 111-118
11. Vincent, J. L., Zhang, H., Szabo, C., and Preiser, J. C. (2000) Effects of nitric oxide in septic shock. Am. J. Respir. Crit. Care Med. 161, 1781-1785
12. Heneka, M. T., Loschmann, P. A., and Osswald, H. (1997) Polymerized hemoglobin restores cardiovascular and kidney function in endotoxin-induced shock in the rat. J. Clin. Invest. 99, 47-54
13. Greenberg, S. S., Xie, J., Zatarain, J. M., Kapusta, D. R., and Miller, M. J. S. (1995) Hydroxocobalamin (Vitamin B12a) prevents and reverses endotoxin-induced hypotension and mortality in rodents: role of nitric oxide. J. Pharmacol. Exp. Ther. 273, 257-265
14. Sharma, V. S., Pilz, R. B., Boss, G. B., and Magde, D. (2003) Reactions of nitric oxide with vitamin B12 and its precursor, cobinamide. Biochemistry 42, 8900-8908
15. Broderick, K. E., Singh, V., Zhuang, S., Kambo, A., Chen, J. C., Sharma, V. S., Pilz, R. B., and Boss, G. R. (2005) Nitric oxide scavenging by the cobalamin precursor cobinamide. J. Biol. Chem. 280, 8678-8685
16. Lemaitre, B., Kromer-Metzger, E., Michaut, L., Nicolas, E., Meister, M., Georgel, P., Reichhart, J. M., and Hoffmann, J. A. (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. U. S. A. 92, 9465-9469
17. Danishpajooh, I. O., Gudi, T., Chen, Y., Kharitonov, V. G., Sharma, V. S., and Boss, G. R. (2001) Nitric oxide inhibits methionine synthase activity in vivo and disrupts carbon flow through the folate pathway. J. Biol. Chem. 276, 27296-27303
18. Paternostro, G., Vignola, C., Bartsch, D. U., Omens, J. H., McCulloch, A. D., and Reed, J. C. (2001) Age-associated cardiac dysfunction in Drosophila melanogaster. Circ. Res. 88, 1053-1058
19. Aboy, M., McNames, J., Thong, T., Tsunami, D., Ellenby, M. S., and Goldstein, B. (2005) An automatic beat detection algorithm for pressure signals. IEEE Trans. Biomed. Eng. 52, 1662-1670
20. Needham, A. J., Kibart, M., Crossley, H., Ingham, P. W., and Foster, S. J. (2004) Drosophila melanogaster as a model host for Staphylococcus aureus infection. Microbiology 150, 2347-2355
21. Lemaitre, B., Reichhart, J. M., and Hoffmann, J. A. (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. U. S. A. 94, 14614-14619
22. Demerec, M. (1950) Biology of Drosophila, John Wiley & Sons, Inc., New York
23. Georgel, P., Naitza, S., Kappler, C., Ferrandon, D., Zachary, D., Swimmer, C., Kopczynski, C., Duyk, G., Reichhart, J. M., and Hoffmann, J. A. (2001) Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev. Cell. 1, 503-514
24. De Gregorio, E., Spellman, P. T., Tzou, P., Rubin, G. M., and Lemaitre, B. (2002) The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 21, 2568-2579
25. McGettigan, J., McLennan, R. K., Broderick, K. E., Kean, L., Allan, A. K., Cabrero, P., Regulski, M. R., Pollock, V. P., Gould, G. W., Davies, S. A., and Dow, J. A. (2005) Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect. Biochem. Mol Biol. 35, 741-754. 7-5
26. Wright, C. E., Rees, D. D., and Moncada, S. (1992) Protective and pathological roles of nitric oxide in endotoxin shock. Cardiovasc. Res. 26, 48-57
27. Bernard, G. R., Vincent, J. L., Laterre, P. F., LaRosa, S. P., Dhainaut, J. F., Lopez-Rodriguez, A., Steingrub, J. S., Garber, G. E., Helterbrand, J. D., Ely, E. W., and Fisher, C. J., Jr. (2001) Efficacy and safety of recombinant human activated protein C for severe sepsis. N. Engl. J. Med. 344, 699-709
28. ω-amino-L-arginine, an inhibitor of nitric oxide synthase, raises vascular resistance but increases mortality rates in awake canines challenged with endotoxin. J. Exp. Med. 176, 1175-1182
29. Kilbourn, R. G., Gross, S. S., Jubran, A., Adams, J., Griffith, O. W., Levi, R., and Lodato, R. F. (1990) NG-methyl-L-arginine inhibits tumor necrosis factor-induced hypotension: implications for the involvement of nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 87, 3629-3632
30. Thiemermann, C., and Vane, J. (1990) Inhibition of nitric oxide synthesis reduces the hypotension induced by bacterial lipopolysaccharides in the rat in vivo. Eur. J. Pharmacol. 182, 591-595
31. Perrin, D. D., and Sayce, I. G. (1967) Computer calculation of equilibrium concentrations in mixtures of metal ions and complexing species. Talanta 14, 833-842
32. Tickoo, S., and Russell, S. (2002) Drosophila melanogaster as a model system for drug discovery and pathway screening. Curr. Opin. Pharmacol. 2, 555-560
33. Agrawal, N., Pallos, J., Slepko, N., Apostol, B. L., Bodai, L., Chang, L. W., Chiang, A. S., Thompson, L. M., and Marsh, J. L. (2005) Identification of combinatorial drug regimens for treatment of Huntington's disease using Drosophila. Proc. Natl. Acad. Sci. U. S. A. 102, 3777-3781
34. Boman, H. G., Nilsson, I., and Rasmuson, B. (1972) Inducible antibacterial defence system in Drosophila. Nature. 237, 232-235
35. Regulski, M., Stasiv, Y., Tully, T., and Enikolopov, G. (2004) Essential function of nitric oxide synthase in Drosophila. Curr. Biol. 14, R881-R882
36. Bier, E., and Bodmer, R. (2004) Drosophila, an emerging model for cardiac disease. Gene 342, 1-11
37. Johnson, E., Sherry, T., Ringo, J., and Dowse, H. (2002) Modulation of the cardiac pacemaker of Drosophila: cellular mechanisms. J. Comp. Physiol. [B] 172, 227-236
38. Gonzalez, B. E., Mercado, C. K., Johnson, L., Brodsky, N. L., and Bhandari, V. (2003) Early markers of late-onset sepsis in premature neonates: clinical, hematological and cytokine profile. J. Perinat. Med. 31, 60-68
39. Kondo, H., Binder, M. J., Kolhouse, J. F., Smythe, W. R., Podell, E. R., and Allen, R. H. (1982) Presence and formation of cobalamin analogues in multivitamin-mineral pills. J. Clin. Invest. 70, 889-898
40. Fedosov, S. N., Berglund, L., Fedosova, N. U., Nexo, E., and Petersen, T. E. (2002) Comparative analysis of cobalamin binding kinetics and ligand protection for intrinsic factor, transcobalamin, and haptocorrin. J. Biol. Chem. 277, 9989-9996
41. Kondo, H., Kolhouse, J. F., and Allen, R. H. (1980) Presence of cobalamin analogues in animal tissues. Proc. Natl. Acad. Sci. U. S. A. 77, 817-821
42. Kolhouse, J. F., Kondo, H., Allen, N. C., Podell, E., and Allen, R. H. (1978) Cobalamin analogues are present in human plasma and can mask cobalamin deficiency because current radioisotope dilution assays are not specific for true cobalamin. N. Engl. J. Med. 299, 785-792
43. Kolhouse, J. F., and Allen, R. H. (1977) Absorption, plasma transport, and cellular retention of cobalamin analogues in the rabbit. Evidence for the existence of multiple mechanisms that prevent the absorption and tissue dissemination of naturally occurring cobalamin analogues. J. Clin. Invest. 60, 1381-1392
44. Kondo, H., Iseki, T., Goto, S., Ohto, M., and Okuda, K. (1992) Effects of cobalamin, cobalamin analogues and cobalamin binding proteins on P388D1 mouse leukemic cells in culture. Int. J. Hematol. 56, 167-177
45. Weinberg, J. B., Shugars, D. C., Sherman, P. A., Sauls, D. L., and Fyfe, J. A. (1998) Cobalamin inhibition of HIV-1 integrase and integration of HIV-1 DNA into cellular DNA. Biochem. Biophys. Res. Commun. 246, 393-397
46. Coates, M. E., Davies, M. K., Dawson, R., Harrison, G. F., Holdsworth, E. S., Kon, S. K., and Porter, J. W. (1956) The activity for chicks of some vitamin B12-like compounds. Biochem. J. 64, 682-686
47. Stabler, S. P., Brass, E. P., Marcell, P. D., and Allen, R. H. (1991) Inhibition of cobalamin-dependent enzymes by cobalamin analogues in rats. J. Clin. Invest. 87, 1422-1430