Electronic and Spatial Structures of Water-Soluble Dinitrosyl Iron Complexes with Thiol-Containing Ligands Underlying Their Ability to Act as Nitric Oxide and Nitrosonium Ion Donors
The ability of mononuclear dinitrosyl iron commplexes (M-DNICs) with thiolate ligands to act as NO donors and to trigger S-nitrosation of thiols can be explain only in the paradigm of the model of the [Fe+(NO+)2] core ({Fe(NO)2}7 according to the Enemark-Feltham classification). Similarly, the {(RS？)2Fe+(NO+)2}+ structure describing the distribution of unpaired electron density in M-DNIC corresponds to the low-spin ( ) state with a d7 electron configuration of the iron atom and predominant localization of the unpaired electron on MO( ) and the square planar structure of M-DNIC. On the other side, the formation of molecular orbitals of M-DNIC including orbitals of the iron atom, thiolate and nitrosyl ligands results in a transfer of electron density from sulfur atoms to the iron atom and nitrosyl ligands. Under these conditions, the positive charge on the nitrosyl ligands diminishes appreciably, the interaction of the ligands with hydroxyl ions or with thiols slows down and the hydrolysis of nitrosyl ligands and the S-nitrosating effect of the latter are not manifested. Most probably, the S-nitrosating effect of nitrosyl ligands is a result of weak binding of thiolate ligands to the iron atom under conditions favoring destabilization of M-DNIC. By present, endogenous dinitrosyl iron complexes (DNICs) with thiol-containing ligands, that is, DNICs having a Fe(NO)2 core, were detected in a vast majority of animal tissues and cell cultures [1–8]. These DNIC are generated in the presence of nitric oxide (NO) released from endogenous or exogenous sources (L-arginine or nitrite, resp.). In biological systems, DNIC are predominantly represented by protein-bound mononuclear forms with characteristic anisotropic EPR signals at and , commonly termed as “the 2.03 signal” in accordance with the average value of the -factor [9]. The 2.03 signal was recorded at both low and ambient temperatures. One of the first records of the 2.03 signal in yeast cells and animal tissues obtained by three independent groups of investigators in the USSR, Great Britain, and the USA as early as mid-1960s are shown in Figure 1 [10–14]. Figure 1: The first recordings of 2.03 signal: dry yeast cells (A) [ 10]; wet yeast cells and rabbit liver (B, spectra a, and b, c). Three components of hyperfine structure of EPR signal of Mn ions in MgO sample are shown in spectrum c [ 14]; rat liver carcinoma induced by p-dimethylaminoazobenzene (butter yellow) (C, spectrum b; (a) spectrum from normal liver) [ 11]; (D) livers from rats maintaining 7, 14, 21, 35, and 49 days on a diet containing butter
References
[1]
A. F. Vanin and D. Sh. Burbaev, “Proteins, containing iron-sulfur centers,” Zhurnal Mendeleevskogo Khimicheskogo Obshestva SSSR, vol. 21, pp. 672–676, 1976.
[2]
A. F. Vanin, Nitrosyl non-heme iron complexes in animal tissues and microorganisms, Doctoral thesis, Institute of Chemical Physics, Moscow, Russia, 1980.
[3]
Y. Henry, C. Ducrocq, J. C. Drapier, D. Servent, C. Pellat, and A. Guissani, “Nitric oxide, a biological effector. Electron paramagnetic resonance detection of nitrosyl-iron-protein complexes in whole cells,” European Biophysics Journal, vol. 20, no. 1, pp. 1–15, 1991.
[4]
A. F. Vanin and A. L. Kleschyov, “EPR studies and biological implications of nitrosyl non-heme iron complexes,” in Nitric Oxide in Transplant Rejection and Anti-Tumor Defense, S. Lukiewicz and J. L. Zweier, Eds., pp. 49–82, Kluwer Academic Publishers, 1998.
[5]
A. R. Butler and I. L. Megson, “Non-heme iron nitrosyls in biology,” Chemical Reviews, vol. 102, no. 4, pp. 1155–1165, 2002.
[6]
A. F. Vanin, E. van Faassen, et al., “DNIC: physico-chemical properties and biological activity,” in Radicals for Live: The Various Forms of Nitric Oxide, E. van Faassen, A. F. Vanin, et al., Eds., pp. 19–74, Elsevier, 2007.
[7]
D. R. Richardson and H. C. Lok, “The nitric oxide-iron interplay in mammalian cells: transport and storage of dinitrosyl iron complexes,” Biochimica et Biophysica Acta, vol. 1780, no. 4, pp. 638–651, 2008.
[8]
A. F. Vanin, “Dinitrosyl iron complexes with thiolate ligands: physico-chemistry, biochemistry and physiology,” Nitric Oxide: Biology and Chemistry, vol. 21, no. 1, pp. 1–13, 2009.
[9]
A. F. Vanin, V. A. Serezhenkov, V. D. Mikoyan, and M. V. Genkin, “The 2.03 signal as an indicator of dinitrosyl-iron complexes with thiol-containing ligands,” Nitric Oxide: Biology and Chemistry, vol. 2, no. 4, pp. 224–234, 1998.
[10]
R. M. Nalbandyan, A. F. Vanin, and L. A. Blumenfeld, “EPR signals of a new type in yeast cells,” in Proceedings of the Free Radicals Processes in Biological Systems, p. 18, Moscow, Russia, 1964.
[11]
J. R. Mallard and M. Kent, “Differences observed between electron spin resonance signals from surviving tumour tissues and from their corresponding normal tissues,” Nature, vol. 204, no. 4964, pp. 1192–1964, 1964.
[12]
A. F. Vanin and R. M. Nalbandyan, “Free radicals of a new type in yeast cells,” Biophysics (Rus), vol. 10, pp. 167–168, 1965.
[13]
A. J. Vithayathil, J. L. Ternberg, and B. Commoner, “Changes in electron spin resonance signals of rat liver during chemical carcinogenesis,” Nature, vol. 207, no. 5003, pp. 1246–1249, 1965.
[14]
A. F. Vanin, A. G. Chetverikov, and L. A. Blumenfel'd, “Investigation of non-heme iron complexes in cells and tissues by the EPR method,” Biophysics (Rus), vol. 12, no. 5, pp. 953–964, 1967.
[15]
A. F. Vanin, A. P. Poltorakov, V. D. Mikoyan, L. N. Kubrina, and D. S. Burbaev, “Polynuclear water-soluble dinitrosyl iron complexes with cysteine or glutathione ligands: electron paramagnetic resonance and optical studies,” Nitric Oxide: Biology and Chemistry, vol. 23, no. 2, pp. 136–149, 2010.
[16]
C. C. McDonald, W. D. Phillips, and H. F. Mower, “An electron spin resonance study of some complexes of iron, nitric oxide, and anionic ligands,” Journal of the American Chemical Society, vol. 87, no. 15, pp. 3319–3326, 1965.
[17]
A. F. Vanin, “Identification of divalent iron complexes with cysteine in biological systems EPR method,” Biochemistry (Moscow), vol. 32, pp. 228–232, 1967.
[18]
A. F. Vanin, V. P. Mokh, V. A. Serezhenkov, and E. I. Chazov, “Vasorelaxing activity of stable powder preparations of dinitrosyl iron complexes with cysteine or glutathione ligands,” Nitric Oxide: Biology and Chemistry, vol. 16, no. 3, pp. 322–330, 2007.
[19]
V. L. Lakomkin, A. F. Vanin, A. A. Timoshin, V. I. Kapelko, and E. I. Chazov, “Long-lasting hypotensive action of stable preparations of dinitrosyl-iron complexes with thiol-containing ligands in conscious normotensive and hypertensive rats,” Nitric Oxide: Biology and Chemistry, vol. 16, no. 4, pp. 413–418, 2007.
[20]
P. I. Mordvintcev, V. G. Rudneva, A. F. Vanin, L. L. Shimkevich, and B. I. Khodorov, “The inhibitory effect of low-molecular dinitrosyl iron complexes on platelet aggregation,” Biochemistry (Moscow), vol. 51, pp. 1851–1857, 1986.
[21]
E. V. Shamova, O. D. Bichan, E. S. Drozd, et al., “Regulation of the functional and mechanical properties of platelet and red blood cells by nitric oxide donors,” Biophysics (Rus), vol. 56, pp. 265–271, 2011.
[22]
O. I. Pisarenko, V. S. Shul'zhenko, I. M. Studneva, Yu. A. Pelogeikina, A. A. Timoshin, and A. F. Vanin, “Effects of dinitrosyl iron complex with glutathione and its components on ischemic rat heart during reperfusion,” Biophysics (Rus), vol. 54, no. 6, pp. 709–713, 2009.
[23]
M. I. Remizova, N. I. Kochetygov, K. A. Gerbout, et al., “Effect of dinitrosyl iron complexes with glutathione on hemorrhagic shock followed by saline treatment,” European Journal of Pharmacology, vol. 662, no. 1–3, pp. 40–46, 2011.
[24]
A. B. Shekhter, T. G. Rudenko, V. A. Serezhenkov, and A. F. Vanin, “Dinitrosyl-iron complexes with cysteine or glutathione accelerate skin wound healing in animals,” Biophysics (Rus), vol. 52, no. 3, pp. 539–547, 2007.
[25]
E. I. Veliev, S. V. Kotov, V. K. Shishlo, V. A. Serezhenkov, V. I. Lozinsky, and A. F. Vanin, “Beneficial effect of dinitrosyl iron complexes with thiol ligands on the rat penile cavernous bodies,” Biophysics (Rus), vol. 53, no. 2, pp. 153–157, 2008.
[26]
A. A. Andreyev-Andriyevsky, V. D. Mikoyan, V. A. Serezhenkov, and A. F. Vanin, “Penile erectile activity of dinitrosyl iron complexes with thiol-containing ligands,” Nitric Oxide: Biology and Chemistry, vol. 24, pp. 217–223, 2011.
[27]
A. F. Vanin and E. I. Chazov, “Prospects of designing the medicines with diverse therapeutic activity on the dasis of dinitrosyl iron complexes with thiol-containing ligands,” Biophysics (Rus), vol. 56, no. 2, pp. 304–315, 2011.
[28]
A. Mülsch, P. Mordvintcev, A. F. Vanin, and R. Busse, “The potent vasodilating and guanylyl cyclase activating dinitrosyl-iron(II) complex is stored in a protein-bound form in vascular tissue and is released by thiols,” FEBS Letters, vol. 294, no. 3, pp. 252–256, 1991.
[29]
Y. P. Vedernikov, P. I. Mordvintcev, I. V. Malenkova, and A. F. Vanin, “Similarity between the vasorelaxing activity of dinitrosyl iron cysteine complexes and endothelium-derived relaxing factor,” European Journal of Pharmacology, vol. 211, no. 3, pp. 313–317, 1992.
[30]
F. W. Flitney, I. L. Megson, D. E. Flitney, and A. R. Butler, “Iron-sulphur cluster nitrosyls, a novel class of nitric oxide generator: mechanism of vasodilator action on rat isolated tail artery,” British Journal of Pharmacology, vol. 107, no. 3, pp. 842–848, 1992.
[31]
F. W. Flitney, I. L. Megson, J. L. M. Thomson, G. D. Kennovin, and A. R. Butler, “Vasodilator responses of rat isolated tail artery enhanced by oxygen-dependent, photochemical release of nitric oxide from iron-sulphur-nitrosyls,” British Journal of Pharmacology, vol. 117, no. 7, pp. 1549–1557, 1996.
[32]
N. A. Sanina, L. A. Syrtsova, N. I. Shkondina et al., “Reactions of sulfur-nitrosyl iron complexes of “ ” family with hemoglobin (Hb): kinetics of Hb-NO formation in aqueous solutions,” Nitric Oxide: Biology and Chemistry, vol. 16, no. 2, pp. 181–188, 2007.
[33]
A. F. Vanin, “Iron diethyldithiocarbamate as spin trap for nitric oxide detection,” Methods in Enzymology, vol. 301, pp. 269–279, 1998.
[34]
A. A. Timoshin, S. A. Gubkina, T. R. Orlova, E. K. Ruuge, A. F. Vanin, and E. I. Chazov, “Study of the nitric oxide level in the tissues of rat organs and its changes after a long-term inhalation of the air with increased no content,” Doklady Biochemistry and Biophysics, vol. 425, no. 1, pp. 110–113, 2009.
[35]
A. A. Timoshin, A. F. Vanin, T. R. Orlova et al., “Protein-bound dinitrosyl-iron complexes appearing in blood of rabbit added with a low-molecular dinitrosyl-iron complex: EPR studies,” Nitric Oxide: Biology and Chemistry, vol. 16, no. 2, pp. 286–293, 2007.
[36]
A. F. Vanin, I. V. Malenkova, O. I. Mordvintsev, and A. Mülsch, “Dinitrosyl iron complexes with thiol-containing ligands and their reversible conversion into nitrosothiols,” Biochemistry (Moscow), vol. 58, no. 7, pp. 1094–1103, 1993.
[37]
M. Boese, P. I. Mordvintcev, A. F. Vanin, R. Busse, and A. Mülsch, “S-nitrosation of serum albumin by dinitrosyl-iron complex,” Journal of Biological Chemistry, vol. 270, no. 49, pp. 29244–29249, 1995.
[38]
B. Mayer, A. L. Kleschyov, H. Stessel et al., “Inactivation of soluble guanylate cyclase by stoichiometric S-nitrosation,” Molecular Pharmacology, vol. 75, no. 4, pp. 886–891, 2009.
[39]
A. F. Vanin, I. V. Malenkova, and V. A. Serezhenkov, “Iron catalyzes both decomposition and synthesis of S-nitrosothiols: optical and electron paramagnetic resonance studies,” Nitric Oxide: Biology and Chemistry, vol. 1, no. 3, pp. 191–203, 1997.
[40]
C. A. Bosworth, J. C. Toledo, J. W. Zmijewski, Q. Li, and J. R. Lancaster, “Dinitrosyliron complexes and the mechanism(s) of cellular protein nitrosothiol formation from nitric oxide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 12, pp. 4671–4676, 2009.
[41]
M. W. Foster, L. Liu, M. Zeng, D. T. Hess, and J. S. Stamler, “A genetic analysis of nitrosative stress,” Biochemistry, vol. 48, no. 4, pp. 792–799, 2009.
[42]
K. A. Pearsall and B. T. Bonner, “Aqueous nitrosyl iron(II) chemistry. 2. Kinetics and mechanism of nitric oxide reduction. The dinitrodsyl complex,” Inorganic Chemistry, vol. 21, pp. 1978–1985, 1982.
[43]
A. F. Vanin and I. V. Malenkova, “Iron is a catalyst of cysteine and glutathione S-nitrosation on contact with nitric oxide in aqueous solutions at neutral pH,” Biochemistry (Moscow), vol. 61, no. 3, pp. 505–513, 1996.
[44]
J. H. Enemark and R. D. Feltham, “Principles of structure, bonding, and reactivity for metal nitrosyl complexes,” Coordination Chemistry Reviews, vol. 13, no. 4, pp. 339–406, 1974.
[45]
B. D'Autréaux, O. Horner, J. L. Oddou et al., “Spectroscopic description of the two nitrosyl-iron complexes responsible for fur inhibition by nitric oxide,” Journal of the American Chemical Society, vol. 126, no. 19, pp. 6005–6016, 2004.
[46]
S. Stojanovic, D. Stanic, M. Nicolic, M. Spasic, and V. Niketic, “Iron catalyzed conversion of NO into nitrosonim (NO+) and nitroxyl (NO-) species,” Nitric Oxide: Biology and Chemistry, vol. 11, no. 3, pp. 256–262, 2004.
[47]
M. T. Bonner and G. Stedman, “The chemistry of nitric oxide and redox-related species,” in Methods of Nitric Oxide Research, M. Feelisch and J. S. Stamler, Eds., pp. 3–18, John Wiley & Sons, New York, NY, USA, 1996.
[48]
A. F. Vanin, “On the stability of the dinitrosyl-iron comlex, a candidate for the endothelium-derived relaxing factor,” Biochemistry (Moscow), vol. 60, pp. 225–230, 1995.
[49]
A. F. Vanin, A. A. Papina, V. A. Serezhenkov, and W. H. Koppenol, “The mechanisms of S-nitrosothiol decomposition catalyzed by iron,” Nitric Oxide: Biology and Chemistry, vol. 10, no. 2, pp. 60–73, 2004.
[50]
D. Sh. Burbaev, D. Sh. Vanin, and L. A. Blumenfeld, “Electronic and spatial structures of paramagnetic dinitrosyl complexes with bivalent iron,” Zhurnal Strukturnoi Khimii, vol. 12, pp. 252–256, 1971.
[51]
D. Sh. Burbaev, Study by EPR method of compounds modeling non-heme iron complexes of biological systems, Ph.D. thesis, Moscow State University, Moscow, Russia, 1971.
[52]
N. S. Garifianov and S. A. Luchkina, “EPR of some nitrosyl compounds of iron,” Doklady Akademii Nauk SSSR, vol. 189, pp. 779–782, 1969.
[53]
B. R. McGarvey, “Theory of the spin hamiltonian parameters for low spin cobalt (II) complexes,” Canadian Journal of Chemistry, vol. 53, no. 16, pp. 2498–2511, 1975.
[54]
A. F. Vanin, N. A. Sanina, V. A. Serezhenkov, D. Sh. Burbaev, V. I. Lozinsky, and S. M. Aldoshin, “Dinitrosyl-iron complexes with thiol-containing ligands: spatial and electronic structures,” Nitric Oxide: Biology and Chemistry, vol. 16, no. 1, pp. 82–93, 2007.
[55]
A. F. Vanin, D. Sh. Burbaev, S. S. Mardanyan, R. M. Nalbandyan, A. A. Mutuskin, and K. V. Pshonova, “On the coordination of iron in iron-sulfur proteins with thiol groups,” in Proceedings of the IY International Biophysics Congress Part 2, pp. 678–683, Moscow, Russia, 1973.
[56]
S. C. Jain, K. V. Reddy, and T. R. Reddy, “EPR of low spin Fe+, Co2+, and Ni3+ cyanide complexes in NacL and KCl,” Journal of Chemical Physics, vol. 62, no. 11, pp. 4366–4372, 1975.
[57]
R. S. Drago, Physical Methods in Chemistry, WB Saunders, Philadelphia, Pa, USA, 1977.
[58]
M. Radón, E. Broclawik, and K. Pierloot, “Electronic structure of selected {Fe(NO)}7 complexes in heme and non-heme architectures: a density functional and multireference ab initio study,” Journal of Physical Chemistry B, vol. 114, no. 3, pp. 1518–1528, 2010.
[59]
R. G. Serres, C. A. Grapperhaus, E. Bothe et al., “Structural, spectroscopic, and computational study of an octahedral, non-heme {Fe–NO}6？8 series: [Fe(NO)(cyclam-ac)]2+1+10,” Journal of the American Chemical Society, vol. 126, no. 16, pp. 5138–5153, 2004.
[60]
C. Y. Chiang, M. L. Miller, J. H. Reibenspies, and M. Y. Darensbourg, “Bismercaptoethanediazacyclooctane as a N2S2 chelating agent and Cys-X-Cys mimic for Fe(NO) and Fe(NO)2,” Journal of the American Chemical Society, vol. 126, no. 35, pp. 10867–10874, 2004.
[61]
P. T. Manoharan and H. B. Gray, “Electronic structure of nitroprusside ion,” Journal of the American Chemical Society, vol. 87, no. 15, pp. 3340–3348, 1965.
[62]
J. D. W. van Voorst and P. Hemmerich, “Electron spin resonance of [Fe(CN)5NO]3- and [Fe(CN)5NOH]2-,” The Journal of Chemical Physics, vol. 45, no. 11, pp. 3914–3918, 1966.
[63]
J. Schmidt, H. Kühr, W. L. Dorn, and J. Kopf, “Nitrosyl-tetracyano-ferrat(II),” Inorganic and Nuclear Chemistry Letters, vol. 10, no. 1, pp. 55–61, 1974.
[64]
D. A. C. McNeil, J. B. Raynor, and M. C. R. Symons, “Structure and reactivity of transition-metal complexes with polyatomic ligands. Part I. Electron spin resonance spectra of [Mn(CN)5NO]2- and [Fe(CN)5NO]3-,” Journal of the Chemical Society A, pp. 410–415, 1965.
[65]
B. Goodman, J. Raynor, and M. Simons, “Electron spin resonance of Bis(N,N-direthyldithiocarbamato) nitrosyl iron,” Journal of the Chemical Society A, pp. 2572–2575, 1969.
[66]
T. T. Lu, S. Z. Lai, Y. W. Li, et al., “Discrimination of mononuclear and dinuclear dinitrosyl iron complexes (DNICs) by SK-edge X-ray absorption spectroscopy: insight into the electronic structure and reactivity of DNICs,” Inorganic Chemistry, vol. 50, no. 12, pp. 5396–5406, 2011.
[67]
A. F. Shestakov, Yu. M. Shul'ga, N. S. Emel'yanova, N. A. Sanina, and S. M. Aldoshin, “Molecular and electronic structure and IR spectra of mononuclear dinitrosyl iron complex [Fe(SC2H3N3) (SC2H2N3)(NO)2]: a theoretical study,” Russian Chemical Bulletin, vol. 56, no. 7, pp. 1289–1297, 2007.
[68]
M. C. Tsai, F. T. Tsai, T. T. Lu et al., “Relative binding affinity of thiolate, imidazolate, phenoxide, and nitrite toward the {Fe(NO)2} motif of dinitrosyl iron complexes (DNICS): the characteristic pre-edge energy of {Fe(NO)2}9 DNICS,” Inorganic Chemistry, vol. 48, no. 19, pp. 9579–9591, 2009.
[69]
S. Ye and F. Neese, “The unusual electronic structure of dinitrosyl iron complexes,” Journal of the American Chemical Society, vol. 132, no. 11, pp. 3646–3647, 2010.
[70]
D. L. H. Williams, Nitrosation Reactions and the Chemistry of Nitric Oxide, Elsevier, 2004.
[71]
Y. I. Chen, W. C. Ku, L. T. Feng et al., “Nitric oxide physiological responses and delivery mechanisms probed by water-soluble Roussin's red ester and {Fe(NO)2}10 DNIC,” Journal of the American Chemical Society, vol. 130, no. 33, pp. 10929–10938, 2008.
[72]
A. F. Vanin and D. I. Aliev, “High spin nitrosyl non-heme iron complexes in animal tissues,” Studia Biofizika, vol. 93, pp. 63–68, 1983.
[73]
Yu. V. Yablokov, V. K. Voronkova, and V. P. Mossina, Paramagnetic Resonance Exchange Clusters (Rus), Nauka, Moscow, Russia, 1988.
[74]
W. R. Hagen, “EPR spectroscopy of iron-sulfur proteins,” Advances in Inorganic Chemistry, vol. 38, pp. 165–222, 1992.
[75]
I. J. Hsu, C. H. Hsieh, S. C. Ke et al., “New members of a class of iron-thiolate-nitrosyl compounds: trinuclear iron-thiolate-nitrosyl complexes containing Fe3S6 core,” Journal of the American Chemical Society, vol. 129, no. 5, pp. 1151–1159, 2007.
[76]
C. B. P. Finn, R. Orbach, and W. P. Wolf, “Spin-lattice relaxation in cerium magnesium nitrate at liquid helium temperature: a new process,” Proceedings of the Physical Society A, vol. 77, no. 494, pp. 261–268, 1961.
[77]
R. Orbach, “Spin-lattice relaxation in rare-earth salts,” Proceedings of the Royal Society A, vol. 264, no. 1319, pp. 458–484, 1961.
[78]
A. Abragam and B. Bleaney, Electron Paramagnetic Resonance of Transition Ions, Clarendon Press, Oxford, UK, 1970.
[79]
J. P. Gayda, J. F. Gibson, R. Cammack, D. O. Hall, and R. Mullinger, “Spin lattice relaxation and exchange interaction in a 2 iron, 2 sulphur protein,” Biochimica et Biophysica Acta, vol. 434, no. 1, pp. 154–163, 1976.
[80]
T. N. Chen, F. C. Lo, M. L. Tsai et al., “Dinitrosyl iron complexes [E5Fe(NO)2]- (E？=？S,Se): a precursor of Roussin's black salt [Fe4E3(NO)7]-,” Inorganica Chimica Acta, vol. 359, no. 8, pp. 2525–2533, 2006.
[81]
N. Ya. Giliano, L. V. Konevega, L. A. Noskin, V. A. Serezhenkov, A. P. Poltorakov, and A. F. Vanin, “Dinitrosyl iron complexes with thiol-containing ligands and apoptosis: studies with HeLa cell cultures,” Nitric Oxide: Biology and Chemistry, vol. 24, no. 3, pp. 151–159, 2011.
[82]
J. C. Yalowich, N. V. Gorbunov, A. V. Kozlov, W. Allan, and V. Kagan, “Mechanisms of nitric oxide protection against tert-butyl hydroperoxide-induced cytotoxicity in iNOS-transduced human erythroleucemia cells,” Biochemistry, vol. 38, pp. 10691–10698, 1999.
[83]
Y. M. Kim, H. T. Chung, R. L. Simmons, and T. R. Billiar, “Cellular non-heme iron content is a determinant of nitric oxide-mediated apoptosis, necrosis, and caspase inhibition,” Journal of Biological Chemistry, vol. 275, no. 15, pp. 10954–10961, 2000.
[84]
S. Zhuang and G. Simon, “Peroxynitrite-induced apoptosis involves activation of multiple caspases in HL-60 cells,” American Journal of Physiology, vol. 279, no. 2, pp. C341–C351, 2000.
[85]
A. L. Kleschyov, S. Strand, S. Schmitt et al., “Dinitrosyl-iron triggers apoptosis in Jurkat cells despite overexpression of Bcl-2,” Free Radical Biology and Medicine, vol. 40, no. 8, pp. 1340–1348, 2006.
[86]
A. de Luca, N. Moroni, A. Serafino, et al., “Treatment of doxorubicin resistant MCF7/Dx cells with nitric oxide causes histone glutathionylation and reverseal of drug resistance,” Biochemical Journal, vol. 440, pp. 175–183, 2011.
[87]
Y. Ji, T. P. M. Akerboom, H. Sies, and J. A. Thomas, “S-nitrosylation and S-glutathiolation of protein sulfhydryls by S-nitroso glutathione,” Archives of Biochemistry and Biophysics, vol. 362, no. 1, pp. 67–78, 1999.
[88]
N. Hogg, “Biological chemistry and clinical potential of S-nitrosothiols,” Free Radical Biology and Medicine, vol. 28, no. 10, pp. 1478–1486, 2000.
[89]
S. J. Coles, P. Easton, H. Sharrod et al., “S-nitrosoglutathione inactivation of the mitochondrial and cytosolic BCAT proteins: S-nitrosation and s-thiolation,” Biochemistry, vol. 48, no. 3, pp. 645–656, 2009.
[90]
L. Tao and A. M. English, “Protein S-glutathiolation triggered by decomposed S-nitrosoglutathione,” Biochemistry, vol. 43, no. 13, pp. 4028–4038, 2004.
