Mitochondria produce reactive nitrogen species via an arginine-independent pathway

Free Radical Research

Volumn 40, Issue 4, 2006, Pages 369-378

  Lacza, Zsombor ^a,b,e   Kozlov, Andrey V ^c   Pankotai, Eszter ^b   Csordás, Attila ^b   Wolf, Gerald ^d   Redl, Heinz ^c   Kollai, Márk ^b   Szabó, Csaba ^b   Busija, David W ^a   Horn, Thomas F W ^d  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c LUDWIG BOLTZMANN INSTITUTE FOR EXPERIMENTAL AND CLINICAL TRAUMATOLOGY   (Austria)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e NONE   (Hungary)

Author keywords

DAF 2; DAF FM; Nitric oxide; Nitric oxide synthase; NOS; ONOO

Indexed keywords

4,5 DIAMINOFLUORESCEIN DIACETATE; ARGININE; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; CITRULLINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; PEROXYNITRITE; REACTIVE NITROGEN SPECIES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CATALYSIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME SUBSTRATE; FLOW CYTOMETRY; HEART MITOCHONDRION; HUMAN; HUMAN CELL; LIVER MITOCHONDRION; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION;

ANIMALS; ARGININE; CELLS, CULTURED; ELECTRON TRANSPORT; FLOW CYTOMETRY; HUMANS; MICE; MICROSCOPY, CONFOCAL; MITOCHONDRIA; REACTIVE NITROGEN SPECIES;

ANIMALIA;

EID: 33644783713     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715760500539139     Document Type: Article

References (47)

1. Brown, GC. (1999) Nitric oxide and mitochondrial respiration Biochim Biophys Acta, 1411, pp. 351 - 369.
2. Almeida, A and Bolanos, JP and Medina, JM. (1999) Nitric oxide mediates brain mitochondrial maturation immediately after birth FEBS Lett, 452, pp. 290 - 294.
3. Boveris, A and Costa, LE and Poderoso, JJ and Carreras, MC and Cadenas, E. (2000) Regulation of mitochondrial respiration by oxygen and nitric oxide Ann NY Acad Sci, 899, pp. 121 - 135.
4. Pearce, LL and Kanai, AJ and Birder, LA and Pitt, BR and Peterson, J. (2002) The catabolic fate of nitric oxide: The nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase J Biol Chem, 277, pp. 13556 - 13562.
5. Brookes, PS. (2004) Mitochondrial nitric oxide synthase Mitochondrion, 3, pp. 187 - 204.
6. Lacza, Z and Pankotai, E and Csordas, A and Gero, D and Kiss, L and Horvath, EM and Kollai, M and Busija, DW and Szabo, C. (2005) Mitochondrial NO and reactive nitrogen species production: Does mtNOS exist? Nitric Oxide.
7. Ghafourifar, P and Cadenas, E. (2005) Mitochondrial nitric oxide synthase Trends Pharmacol Sci, 26, pp. 190 - 195.
8. Haynes, V and Elfering, S and Traaseth, N and Giulivi, C. (2004) Mitochondrial nitric-oxide synthase: Enzyme expression, characterization, and regulation J Bioenerg Biomembr, 36, pp. 341 - 346.
9. Kozlov, AV and Staniek, K and Nohl, H. (1999) Nitrite reductase activity is a novel function of mammalian mitochondria FEBS Lett, 454, pp. 127 - 130.
10. Loesch, A and Belai, A and Burnstock, G. (1994) An ultrastructural study of NADPH-diaphorase and nitric oxide synthase in the perivascular nerves and vascular endothelium of the rat basilar artery J Neurocytol, 23, pp. 49 - 59.
11. Ghafourifar, P and Richter, C. (1997) Nitric oxide synthase activity in mitochondria FEBS Lett, 418, pp. 291 - 296.
12. Lacza, Z and Puskar, M and Figueroa, JP and Zhang, J and Rajapakse, N and Busija, DW. (2001) Mitochondrial nitric oxide synthase is constitutively active and is functionally upregulated in hypoxia Free Radic Biol Med, 31, pp. 1609 - 1615.
13. Bates, TE and Loesch, A and Burnstock, G and Clark, JB. (1996) Mitochondrial nitric oxide synthase: A ubiquitous regulator of oxidative phosphorylation? Biochem Biophys Res Commun, 218, pp. 40 - 44.
14. Bates, TE and Loesch, A and Burnstock, G and Clark, JB. (1995) Immunocytochemical evidence for a mitochondrially located nitric oxide synthase in brain and liver Biochem Biophys Res Commun, 213, pp. 896 - 900.
15. Giulivi, C and Poderoso, JJ and Boveris, A. (1998) Production of nitric oxide by mitochondria J Biol Chem, 273, pp. 11038 - 11043.
16. Lacza, Z and Snipes, JA and Zhang, J and Horvath, EM and Figueroa, JP and Szabo, C and Busija, DW. (2003) Mitochondrial nitric oxide synthase is not eNOS, nNOS or iNOS Free Radic Biol Med, 35, pp. 1217 - 1228.
17. Lacza, Z and Horn, TF and Snipes, JA and Zhang, J and Roychowdhury, S and Horvath, EM and Figueroa, JP and Kollai, M and Szabo, C and Busija, DW. (2004) Lack of mitochondrial nitric oxide production in the mouse brain J Neurochem, 90, pp. 942 - 951.
18. Yvonne Mei Sian, Tay A1 KSL and Sheu, F-S and Jenner, A and Whiteman, M and Wong, KP and Halliwell, B. (2004) Do Mitochondria make Nitric Oxide? No Free Radic Res, 38, pp. 591 - 599.
19. Lopez-Figueroa, MO and Caamano, C and Morano, MI and Ronn, LC and Akil, H and Watson, SJ. (2000) Direct evidence of nitric oxide presence within mitochondria Biochem Biophys Res Commun, 272, pp. 129 - 133.
20. Dedkova, EN and Ji, X and Lipsius, SL and Blatter, LA. (2004) Mitochondrial calcium uptake stimulates nitric oxide production in mitochondria of bovine vascular endothelial cells Am J Physiol Cell Physiol, 286, pp. C406 - C415.
21. Dennis, J and Bennett, JPJ. (2003) Interactions among nitric oxide and Bcl-family proteins after MPP+ exposure of SH-SY5Y neural cells I: MPP+ increases mitochondrial NO and Bax protein J Neurosci Res, 72, pp. 76 - 88.
22. Yamamoto, Y and Henrich, M and Snipes, RL and Kummer, W. (2003) Altered production of nitric oxide and reactive oxygen species in rat nodose ganglion neurons during acute hypoxia Brain Res, 961, pp. 1 - 9.
23. Zanella, B and Calonghi, N and Pagnotta, E and Masotti, L and Guarnieri, C. (2002) Mitochondrial nitric oxide localization in H9c2 cells revealed by confocal microscopy Biochem Biophys Res Commun, 290, pp. 1010 - 1014.
24. Kojima, H and Nakatsubo, N and Kikuchi, K and Kawahara, S and Kirino, Y and Nagoshi, H and Hirata, Y and Nagano, T. (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: Diaminofluoresceins Anal Chem, 70, pp. 2446 - 2453.
25. Qi, K and Qiu, H and Rutherford, J and Zhao, Y and Nance, DM and Orr, FW. (2004) Direct visualization of nitric oxide release by liver cells after the arrest of metastatic tumor cells in the hepatic microvasculature J Surg Res, 119, pp. 29 - 35.
26. Lorenz, P and Roychowdhury, S and Engelmann, M and Wolf, G and Horn, TF. (2003) Oxyresveratrol and resveratrol are potent antioxidants and free radical scavengers: Effect on nitrosative and oxidative stress derived from microglial cells Nitric Oxide, 9, pp. 64 - 76.
27. Kashiwagi, S and Kajimura, M and Yoshimura, Y and Suematsu, M. (2002) Nonendothelial source of nitric oxide in arterioles but not in venules: Alternative source revealed in vivo by diaminofluorescein microfluorography Circ Res, 91, pp. e55 - e64.
28. Roychowdhury, S and Luthe, A and Keilhoff, G and Wolf, G and Horn, TF. (2002) Oxidative stress in glial cultures: Detection by DAF-2 fluorescence used as a tool to measure peroxynitrite rather than nitric oxide Glia, 38, pp. 103 - 114.
29. Jourd'heuil, D. (2002) Increased nitric oxide-dependent nitrosylation of 4,5-diaminofluorescein by oxidants: Implications for the measurement of intracellular nitric oxide Free Radic Biol Med, 33, pp. 676 - 684.
30. Lacza, Z and Horvath, EM and Pankotai, E and Csordas, A and Kollai, M and Szabo, C and Busija, DW. (2005) The novel red-fluorescent probe DAR-4M measures reactive nitrogen species rather than NO J Pharmacol Toxicol Methods.
31. Lacza, Z and Snipes, JA and Miller, AW and Szabo, C and Grover, G and Busija, DW. (2003) Heart mitochondria contain functional ATP-dependent K(+) channels J Mol Cell Cardiol, 35, pp. 1339 - 1347.
32. Broillet, M and Randin, O and Chatton, J. (2001) Photoactivation and calcium sensitivity of the fluorescent NO indicator 4,5-diaminofluorescein (DAF-2): Implications for cellular NO imaging FEBS Lett, 491, pp. 227 - 232.
33. Lacza, Z and Snipes, JA and Kis, B and Szabo, C and Grover, G and Busija, DW. (2003) Investigation of the subunit composition and the pharmacology of the mitochondrial ATP-dependent K(+) channel in the brain Brain Res, 994, pp. 27 - 36.
34. Pacher, P and Liaudet, L and Bai, P and Mabley, JG and Kaminski, PM and Virag, L and Deb, A and Szabo, E and Ungvari, Z and Wolin, MS and Groves, JT and Szabo, C. (2003) Potent metalloporphyrin peroxynitrite decomposition catalyst protects against the development of doxorubicin-induced cardiac dysfunction Circulation, 107, pp. 896 - 904.
35. Kozlov, AV and Szalay, L and Umar, F and Kropik, K and Staniek, K and Niedermuller, H and Bahrami, S and Nohl, H. (2005) Skeletal muscles, heart and lung are the main sources of oxygen radicals in old rats Biochim Biophys Acta, 1740, pp. 382 - 389.
36. Elfering, SL and Sarkela, TM and Giulivi, C. (2002) Biochemistry of mitochondrial nitric-oxide synthase J Biol Chem, 277, pp. 38079 - 38086.
37. Boveris, A and Arnaiz, SL and Bustamante, J and Alvarez, S and Valdez, L and Boveris, AD and Navarro, A. (2002) Pharmacological regulation of mitochondrial nitric oxide synthase Methods Enzymol, 359, pp. 328 - 339.
38. Kanai, AJ and Pearce, LL and Clemens, PR and Birder, LA and VanBibber, MM and Choi, SY and de, GWC and Peterson, J. (2001) Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection Proc Natl Acad Sci USA, 98, pp. 14126 - 14131.
39. Manzo-Avalos, S and Perez-Vazquez, V and Ramirez, J and Aguilera-Aguirre, L and Gonzalez-Hernandez, JC and Clemente-Guerrero, M and Villalobos-Molina, R and Saavedra-Molina, A. (2002) Regulation of the rate of synthesis of nitric oxide by Mg(2+) and hypoxia. Studies in rat heart mitochondria Amino Acids, 22, pp. 381 - 389.
40. Gao, S and Chen, J and Brodsky, SV and Huang, H and Adler, S and Lee, JH and Dhadwal, N and Cohen-Gould, L and Gross, SS and Goligorsky, MS. (2004) Docking of endothelial nitric oxide synthase (eNOS) to the mitochondrial outer membrane: A pentabasic amino acid sequence in the autoinhibitory domain of eNOS targets a proteinase K-cleavable peptide on the cytoplasmic face of mitochondria J Biol Chem, 279, pp. 15968 - 15974.
41. Henrich, M and Hoffmann, K and Konig, P and Gruss, M and Fischbach, T and Godecke, A and Hempelmann, G and Kummer, W. (2002) Sensory neurons respond to hypoxia with NO production associated with mitochondria Mol Cell Neurosci, 20, pp. 307 - 322.
42. Kojima, H and Urano, Y and Kikuchi, K and Higuchi, T and Hirata, Y and Nagano, T. (1999) Fluorescent indicators for imaging nitric oxide production Angew Chem Int Ed Engl, 38, pp. 3209 - 3212.
43. Nohl, H and Staniek, K and Sobhian, B and Bahrami, S and Redl, H and Kozlov, AV. (2000) Mitochondria recycle nitrite back to the bioregulator nitric monoxide Acta Biochim Pol, 47, pp. 913 - 921.
44. Artz, JD and Thatcher, GR. (1998) NO release from NO donors and nitrovasodilators: Comparisons between oxyhemoglobin and potentiometric assays Chem Res Toxicol, 11, pp. 1393 - 1397.
45. Steffen, M and Sarkela, TM and Gybina, AA and Steele, TW and Trasseth, NJ and Kuehl, D and Giulivi, C. (2001) Metabolism of S-nitrosoglutathione in intact mitochondria Biochem J, 356, pp. 395 - 402.
46. Chen, Z and Zhang, J and Stamler, JS. (2002) Identification of the enzymatic mechanism of nitroglycerin bioactivation Proc Natl Acad Sci USA, 99, pp. 8306 - 8311.
47. McGuire, JJ and Anderson, DJ and McDonald, BJ and Narayanasami, R and Bennett, BM. (1998) Inhibition of NADPH-cytochrome P450 reductase and glyceryl trinitrate biotransformation by diphenyleneiodonium sulfate Biochem Pharmacol, 56, pp. 881 - 893.