The effect of divalent cations on neuronal nitric oxide synthase activity

Toxicological Sciences

Volumn 81, Issue 2, 2004, Pages 325-331

  Weaver, John ^a,b,c   Porasuphatana, Supatra ^d   Tsai, Pei ^b,c   Cao, Guan Liang ^b   Budzichowski, Theodore A ^a   Roman, Linda J ^e   Rosen, Gerald M ^b,c,f  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d KHON KAEN UNIVERSITY   (Thailand)

^e UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^f UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Calmodulin; Divalent cations; Metal toxicity; Nitric oxide; NOS I; Superoxide

Indexed keywords

ARGININE; BARIUM ION; CADMIUM; CALCIUM ION; CITRULLINE; DIVALENT CATION; MANGANESE; NEURONAL NITRIC OXIDE SYNTHASE; NICKEL; NITRIC OXIDE; SUPEROXIDE;

AMINO ACID METABOLISM; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION;

ARGININE; BARIUM; CADMIUM; CALMODULIN; CATIONS, DIVALENT; CITRULLINE; CYCLIC N-OXIDES; CYTOCHROMES C; INDICATORS AND REAGENTS; KINETICS; MANGANESE; NICKEL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; REACTIVE OXYGEN SPECIES; SPIN TRAPPING; XANTHINE OXIDASE;

EID: 5744240626     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/kfh211     Document Type: Article

References (47)

1. Abu-Soud, H. M., Yoho, L. L., and Stuehr, D. J. (1994). Calmodulin controls neuronal nitric oxide synthase by a dual mechanism. J. Biol. Chem. 269, 32047-32050.
2. Chetty, C. S., Reddy, G. R., Suresh, A., Dessaih, D., Ali, S. F., and Slikker, K. J. (2001). Effects of manganese on inositol polyphosphate receptors and nitric oxide synthase activity in the rat brain. Int. J. Toxicol. 20, 275-280.
3. + in hypertensive rats. Hypertension 39, 880-885.
4. Clapham, D. (1995). Calcium signaling. Cell 80, 259-268.
5. Denkhaus, E., and Salnikow, K. (2002). Nickel essentiality, toxicology, and carcinogenicity. Crit. Rev. Oncol. Hematol. 42, 35-56.
6. Förstermann, U., Boissel, J.-P., and Kleinhert, H. (1998). Expressional control of the "constitutive" isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 12, 773-790.
7. Goldstein, G. W., and Ar, D. (1983). Lead activates calmodulin sensitive processes. Life Sci. 33, 1001-1006.
8. Gupta, S., Ahmad, N., Hussain, M., and Srivastava, R. (2000). Involvement of nitric oxide in nickel-induced hyperglycemia in rats. Nitric Oxide 4, 129-138.
9. 2+ in calmodulin. Arch. Toxicol. 54, 61-70.
10. 2+/Calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochem. J. 281, 627-630.
11. Huheey, J., Keiter, E., and Keiter, R. (1993). Inorganic Chemistry Principles of Structure and Reactivity (4th edition). HarperCollins College Publishers, New York.
12. Husain, M., Khanna, V. K., Roy, A., Tandon, R., Pradeep, S., and Set, P. K. (2001). Platelet dopamine receptors and oxidative stress parameters as markers of manganese toxicity. Hum. Exp. Toxicol. 20, 631-636.
13. Jacobs, I. A., Taddeo, J., Kelly, K., and Valernziano, C. (2002). Poisoning as a result of barium styphnate explosion. Am. J. Ind. Med. 41, 285-288.
14. Kern, M., Wisniewski, M., Canell, L., and Audesirk, G. (2000). Inorganic lead and calcium interact positively in activation of calmodulin. Neurotoxicology 21, 353-364.
15. Kobayash, K., Tagawa, S., Daff, S., Sami, I., and Shimizu, T. (2001). Rapid calmodulin-dependent interdomain electron transfer in neuronal nitric-oxide synthase measured by pulse radiolysis. J. Biol. Chem. 276, 39864-39871.
16. Kopp, S. J., Perry, H. M., Perry, E. F., and Erlanger, M. (1983). Cardiac physiologic and tissue metabolic changes following chronic low-level cadmium and cadmium plus lead injestion in the rat. Toxicol. Appl. Pharmacol. 69, 149-160.
17. Kuthan, H., and Ullrich, V. (1982). A quantitative test for superoxide radicals produced in biological systems. Biochem. J. 203, 551-558.
18. Lippard, J., and Berg, J. (1994). Principles of Bioinorganic Chemistry. University Science Books, Sausalito, California.
19. Matsuda, H., and Iyanagi, T. (1999). Calmodulin activates intramolecular electron transfer between the two flavins of neuronal nitric oxide synthase flavin domain. Biochim. Biophys. Acta 1473, 345-355.
20. Mayer, B., John, M., Heinzel, B., Werner, E. R., Wachter, H., Schultz, G., and Böhme, E. (1991). Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxido-reductase. FEBS Lett. 288, 187-191.
21. Miller, R. T., Martasek, P., Omura, T., and Masters, B. S. S. (1999). Rapid kinetic studies of electron transfer in the three isoforms of nitric oxide synthase. Biochem. Biophys. Res. Commun. 265, 184-188.
22. Mills, J., and Johnson, D. (1985). Metal ions as allosteric regulators of calmodulin. J. Biol. Chem. 260, 15100-15105.
23. Mittal, C. K., Harell, W. B., and Mehta, C. S. (1995). Interaction of heavy metal toxicants with brain nitric oxide synthase. Mol. Cell. Biochem. 149/150, 263-265.
24. Moncada, S., and Higgs, A. (1993). The L-arginine-nitric oxide pathway. N. Engl. J. Med. 329, 2002-2012.
25. Murphy, M. E., and Noack, E. (1994). Nitric oxide assay using hemoglobin method. Methods Enzymol. 233, 241-250.
26. Nathan, C., and Xie, Q.-W. (1994). Nitric oxide synthases: Roles, tolls and controls. Cell 78, 915-918.
27. Nishimura, J., Narayanasami, R., Miller, R., Roman, L., Panda, S., and Masters, B. (1999). The stimulatory effects of Hofmeister ions on the activities of neuronal nitric-oxide synthase. J. Biol. Chem. 274, 5399-5406.
28. Ozawa, T., Sasaki, K., and Umezawa, Y. (1999). Metal ion selectivity for the formation of calmodulin-metal-target peptide ternary complex studied by surface plasmon resonance spectroscopy. Biochim. Biophys. Acta 1434, 211-220.
29. 2+/calmodulin-dependent enzyme activation. Biochem. Biophys. Res. Commun. 285, 142-146.
30. Perry, J. M., and Marletta, M. A. (1998). Effects of transition metals on nitric oxide synthase catalysis. Proc. Natl. Acad. Sci. U.S.A. 95, 11101-11106.
31. Pou, S., Keaton, L., Surichamorn, W., and Rosen, G. M. (1999). Mechanism of superoxide generation by neuronal nitric oxide synthase. J. Biol. Chem. 274, 9573-9580.
32. Pou, S., Pou, W. S., Bredt, D. S., Snyder, S. H., and Rosen, G. M. (1992). Generation of superoxide by purified brain nitric oxide synthase. J. Biol. Chem. 267, 24173-24176.
33. Roman, L. J., Martasek, P., and Masters, B. S. S. (2002). Intrinsic and extrinsic modulation of nitric oxide synthase activity. Chem. Rev. 102, 1179-1189.
34. Roman, L. J., Martásek, P., Miller, T. R., Harris, D. E., de la Garza, M. A., Shea, T. M., Kim, J. P., and Masters, B. S. S. (2000). The C terminal of constitutive nitric-oxide synthases control electron flow through the flavin and heme domains and affect modulation of calmodulin. J. Biol. Chem. 275, 29225-29232.
35. Roman, L. J., Sheta, E. A., Martasek, P., Gross, S. S., Liu, Q., and Masters, B. S. S. (1995). High-level expression of functional rat neuronal nitric oxide synthase in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 8428-8432.
36. Rosen, G. M., Tsai, P., Weaver, J., Porasuphatana, S., Roman, L. J., Starkov, A. A., Fiskum, G., and Pou, S. (2002). The role of tetrahydrobiopterin in the regulation of neuronal nitric oxide synthase-generated superoxide. J. Biol. Chem. 277, 40275-40280.
37. Roskams, A. J., Bredt, D. S., Dawson, T. M., and Ronnett, G. V. (1994). Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron 19, 893-903.
38. Schrammel, A., Gorren, A., Stuehr, D., Schmidt, K., and Mayer, B. (1998). Isoform-specific effects of salts on nitric oxide activity. Biochim. Biophys. Acta 1387, 257-263.
39. Sheta, E. A., McMillan, K., and Masters, B. S. S. (1994). Evidence for a bidomain structure of constitutive cerebellar nitric oxide synthase. J. Bol. Chem. 269, 15147-15153.
40. Stolze, K., Udilova, N., Rosenau, T., Hofinger, A., and Nohl, H. (2003). Synthesis and characterization of EMPO-derived 5,5-disubstituted 1-pyrroline N-oxides as spin traps forming exceptionally stable superoxide spin adducts. Biol. Chem. 384, 493-500.
41. Thun, M. J., Osorio, A. M., and Schober, S. (1989). Nephropathy in cadmium workers: Assessment of risk from airborne occupational exposure to cadmium. Br. J. Ind. Med. 46, 689-697.
42. Tian, L., and Lawrence, D. A. (1996). Metal-induced modulation of nitric oxide production in vitro by murine macrophages: lead, nickel, and cobalt utilize different mechanisms. Toxicol. Appl. Pharmacol. 141, 540-547.
43. Tsai, P., Ichikawa, K., Mailer, C., Pou, S., Halpern, H. J., Robinson, B. H., Nielsen, R., and Rosen, G. M. (2003). Esters of 5-carboxy-5-methyl-1-pyrroline N-oxide: A family of spin traps for superoxide. J. Org. Chem. 68, 7811-7817.
44. Weaver, J., Porasuphatana, S., Tsai, P., Cao, G.-L., Budzichowski, T. A., Roman, L. J., and Rosen, G. M. (2002). The activation of neuronal nitric-oxide synthase by various divalent cations. J. Pharmacol. Exp. Therap. 302, 781-786.
45. Weaver, J., Tsai, P., Cao, G.-L., Roman, L. J., and Rosen, G. M. (2003). Modified ferricytochrome c can be used to estimate nitric oxide synthase generation of superoxide. Anal Biochem. 320, 141-143.
46. Yamazaki, J., Ohara, F., Harada, Y., and Nagao, T. (1995). Barium and Strontium can substitute for calcium in stimulating nitric oxide production in the endothelium of canine coronary arteries. Jpn. J. Pharmacol. 68, 25-32.
47. Yoneyama, H., Yamamoto, A., and Kosaka, H. (2001). Neuronal nitric oxide synthase generates superoxide form the oxygenase domain. Biochem. J. 360, 247-253.