The Role of Nitric Oxide in Apoptosis and Autophagy. Biochemical and Computational Studies.

Nitric Oxide

Volumn , Issue , 2010, Pages 513-537

  Loughran, P A ^a   Bagci, E Z ^b   Zamora, R ^c   Vodovotz, Y ^a   Billiar, T R ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b BOGAZICI UNIVERSITY   (Turkey)

^c Center for Inflammation and Regenerative Modeling   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882503114     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-373866-0.00015-0     Document Type: Chapter

References (174)

1. Afshar R.K., Patra A.K., Olmstead M.M., Mascharak P.K. Syntheses, structures, and reactivities of {Fe-NO}(6) nitrosyls derived from polypyridine-carboxamide ligands: Photoactive NO-donors and reagents for S-nitrosylation of alkyl thiols. Inorg. Chem. 2004, 43:5736-5743.
2. Albakri Q.A., Stuehr D.J. Intracellular assembly of inducible NO synthase is limited by nitric oxide-mediated changes in heme insertion and availability. J. Biol. Chem. 1996, 271:5414-5421.
3. Albina J.E., Cui S., Mateo R.B., Reichner J.S. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 1993, 150:5080-5085.
4. Aller M.A., Arias J.L., Nava M.P., Arias J. Posttraumatic inflammation is a complex response based on the pathological expression of the nervous, immune, and endocrine functional systems. Exp. Biol. Med. (Maywood) 2004, 229:170-181.
5. An G., Vodovotz Y. Translational systems biology: Introduction of an engineering approach to the pathophysiology of the burn patient. J. Burn Care Res. 2008, 29:277-285.
6. An G., Hunt C.A., Clermont G., Neugebauer E., Vodovotz Y. Challenges and rewards on the road to translational systems biology in acute illness: Four case reports from interdisciplinary teams. J. Crit. Care 2007, 22:169-175.
7. Babior B.M. Phagocytes and oxidative stress. Am. J. Med. 2000, 109:33-44.
8. Baek K.J., Thiel B.A., Lucas S., Stuehr D.J. Macrophage nitric oxide synthase subunits: Purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J. Biol. Chem. 1993, 268:21120-21129.
9. Bagci E.Z., Vodovotz Y., Billiar T.R., Ermentrout G.B., Bahar I. Bistability in apoptosis: Roles of Bax, Bcl-2, and Mitochondrial Permeability Transition Pores. Biophys. J. 2006, 90:1546-1559.
10. Bagci E.Z., Vodovotz Y., Billiar T.R., Ermentrout G.B., Bahar I. Computational insights on the competing effects of nitric oxide in regulating apoptosis. PLoS ONE 2008, 3:e2249.
11. Balague C., Targarona E.M., Pujol M., Filella X., Espert J.J., Trias M. Peritoneal response to a septic challenge. Comparison between open laparotomy, pneumoperitoneum laparoscopy, and wall lift laparoscopy. Surg. Endosc. 1999, 13:792-796.
12. Barlow B., Santulli T.V., Heird W.C., Pitt J., Blanc W.A., Schullinger J.N. An experimental study of acute neonatal enterocolitis-the importance of breast milk. J. Pediatr. Surg. 1974, 9:587-595.
13. Beckman J.S., Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and the ugly. Am. J. Physiol. Cell Physiol. 1996, 40:C1424-C1437.
14. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 1990, 87:1620-1624.
15. Bentele M., Lavrik I., Ulrich M., Stosser S., Heermann D.W., Kalthoff H., Krammer P.H., Eils R. Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J. Cell Biol. 2004, 166:839-851.
16. Bergmann A. Autophagy and cell death: No longer at odds. Cell 2007, 131:1032-1034.
17. Bone R.C. Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS). Ann. Intern. Med. 1996, 125:680-687.
18. Bredt D.S., Snyder S.H. Isolation of nitric oxide synthetase, a calmodulin requiring enzyme. Proc. Natl. Acad. Sci. 1990, 87:682-685.
19. Brenman J.E., Chao D.S., Xia H., Aldape K., Bredt D.S. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995, 82:743-752.
20. Bruick R.K. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. USA 2000, 97:9082-9087.
21. Brune B. The intimate relation between nitric oxide and superoxide in apoptosis and cell survival. Antioxid. Redox Signal 2005, 7:497-507.
22. Buchman T.G., Cobb J.P., Lapedes A.S., Kepler T.B. Complex systems analysis: a tool for shock research. Shock 2001, 16:248-251.
23. Catania R.A., Chaudry I.H. Immunological consequences of trauma and shock. Ann. Acad. Med. Singap. 1999, 28:120-132.
24. Chen Y.Q., Gibson S.B. Is mitochondrial generation of reactive oxygen species a trigger for autophagy?. Autophagy 2008, 4:246-248.
25. Chen G., Ray R., Dubik D., Shi L., Cizeau J., Bleackley R.C., Saxena S., Gietz R.D., Greenberg A.H. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J. Exp. Med. 1997, 186:1975-1983.
26. Chen G., Cizeau J., Vande V.C., Park J.H., Bozek G., Bolton J., Shi L., Dubik D., Greenberg A. Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins. J. Biol. Chem. 1999, 274:7-10.
27. Chen Y., McMillan-Ward E., Kong J., Israels S.J., Gibson S.B. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008, 15:171-182.
28. Cho H.J., Xie Q.-W., Calaycay J., Mumford R.A., Siderek K.M., Lee T.D., Nathan C. Calmodulin is a subunit of nitric oxide synthase from macrophages. J. Exp. Med. 1992, 176:599-604.
29. Chow C.C., Clermont G., Kumar R., Lagoa C., Tawadrous Z., Gallo D., Betten B., Bartels J., Constantine G., Fink M.P., Billiar T.R., Vodovotz Y. The acute inflammatory response in diverse shock states. Shock 2005, 24:74-84.
30. Collins J., Vodovotz Y., Billiar T.R. Biology of nitric oxide: measurement, modulation, and models. Surgical Research 2001, 949-969. Academic Press, San Diego. W. Souba, D. Wilmore (Eds.).
31. Collins J.L., Vodovotz Y., Hierholzer C., Villavicencio R.T., Liu S., Alber S., Gallo D., Stolz D.B., Watkins S.C., Godfrey A., Gooding W., Kelly E., Peitzman A.B., Billiar T.R. Characterization of the expression of inducible nitric oxide synthase in rat and human liver during hemorrhagic shock. Shock 2003, 19:117-122.
32. Curran R.D., Billiar T.R., Stuehr D.J., Hoffmann K., Simmons R.L. Hepatocytes produce nitrogen oxides from L-arginine in response to inflammatory products of Kupffer cells. J. Exp. Med. 1989, 170:1769-1774.
33. Czapksi G., Goldstein S. The role of the reactions of NO with superoxide and oxygen in biological systems: a kinetic approach. Free Radic. Biol. Med. 1995, 19:785-794.
34. Dash P.R., Cartwright J.E., Baker P.N., Johnstone A.P., Whitley G.S. Nitric oxide protects human extravillous trophoblast cells from apoptosis by a cyclic GMP-dependent mechanism and independently of caspase 3 nitrosylation. Exp. Cell Res. 2003, 287:314-324.
35. Davis A.S., Vergne I., Master S.S., Kyei G.B., Chua J., Deretic V. Mechanism of inducible nitric oxide synthase exclusion from mycobacterial phagosomes. PLoS. Pathog. 2007, 3:e186.
36. Degterev A., Hitomi J., Germscheid M., Ch'en I.L., Korkina O., Teng X., Abbott D., Cuny G.D., Yuan C., Wagner G., Hedrick S.M., Gerber S.A., Lugovskoy A., Yuan J. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 2008, 4:313-321.
37. Denninger J.W., Marletta M.A. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim. Biophys. Acta 1999, 1411:334-350.
38. Dimmeler S., Rippmann V., Weiland U., Haendeler J., Zeiher A.M. Angiotensin II induces apoptosis of human endothelial cells. Protective effect of nitric oxide. Circ. Res. 1997, 81:970-976.
39. Ding A., Nathan C. Regulation of cell surface receptor expression by LPS. Bacterial Endotoxic Lipopolysaccharides Molecular and Cellular Biology 1992, vol. I:373-386. CRC Press, Boca Raton, FL. D.C. Morrison, J.L. Ryan (Eds.).
40. Eissing T., Conzelmann H., Gilles E.D., Allgower F., Bullinger E., Scheurich P. Bistability analyses of a caspase activation model for receptor-induced apoptosis. J. Biol. Chem. 2004, 279:36892-36897.
41. Espert L., Denizot M., Grimaldi M., Robert-Hebmann V., Gay B., Varbanov M., Codogno P., Biard-Piechaczyk M. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J. Clin. Invest. 2006, 116:2161-2172.
42. de Fátima A., Zambuzzi W.F., Modolo L.V., Tarsitano C.A., Gadelha F.R., Hyslop S., de Carvalho J.E., Salgado I., Ferreira C.V., Pilli R.A. Cytotoxicity of goniothalamin enantiomers in renal cancer cells: involvement of nitric oxide, apoptosis and autophagy. Chem. Biol. Interact. 2008, 176:143-150.
43. Foresti R., Sarathchandra P., Clark J.E., Green C.J., Motterlini R. Peroxynitrite induces haem oxygenase-1in vascular endothelial cells: a link to apoptosis. Biochem. J 1999, 339(Pt 3):729-736.
44. Forstermann U., Schmidt H.H., Pollock J.S., Sheng H., Mitchell J.A., Warner T.D., Nakane M., Murad F. Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochem. Pharmacol. 1991, 42:1849-1857.
45. Freeman B.D., Natanson C. Anti-inflammatory therapies in sepsis and septic shock. Expert Opin. Investig. Drugs 2000, 9:1651-1663.
46. Fukuo K., Hata S., Suhara T., Nakahashi T., Shinto Y., Tsujimoto Y., Morimoto S., Ogihara T. Nitric oxide induces upregulation of Fas and apoptosis in vascular smooth muscle. Hypertension 1996, 27:823-826.
47. Fussenegger M., Bailey J.E., Varner J. A mathematical model of caspase function in apoptosis. Nature Biotechnol. 2000, 18:768-774.
48. Garban H.J., Bonavida B. Nitric oxide sensitizes ovarian tumor cells to Fas-induced apoptosis. Gynecol. Oncol. 1999, 73:257-264.
49. Garban H.J., Bonavida B. Nitric oxide inhibits the transcription repressor Yin-Yang 1 binding activity at the silencer region of the Fas promoter: a pivotal role for nitric oxide in the up-regulation of Fas gene expression in human tumor cells. JI 2001, 167:75-81.
50. Geller D.A., Lowenstein C.J., Shapiro R.A., Nussler A.K., Di Silvio M., Wang S.C., Nakayama D.K., Simmons R.L., Snyder S.H., Billiar T.R. Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc. Natl. Acad. Sci. USA 1993, 90:3491-3495.
51. Ghosh D.K., Abu-Soud H.M., Stuehr D.J. Reconstitution of the second step in NO synthesis using the isolated oxygenase and reductase domains of macrophage NO synthase. Biochemistry 1995, 34:11316-11320.
52. Glynne P.A., Darling K.E., Picot J., Evans T.J. Epithelial inducible nitric-oxide synthase is an apical EBP50-binding protein that directs vectorial nitric oxide output. J. Biol. Chem. 2002, 277:33132-33138.
53. Gozuacik D., Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23:2891-2906.
54. Grisham M.B., Jourd'Heuil D., Wink D.A. Nitric oxide - I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 1999, 276:G315-G321.
55. Ha K.S., Kim K.M., Kwon Y.G., Bai S.K., Nam W.D., Yoo Y.M., Kim P.K.M., Chung H.T., Billiar T.R., Kim Y.M. Nitric oxide prevents 6-hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/Akt activation. FASEB J 2003, 17:1036-1047.
56. Hack C.E., Zeerleder S. The endothelium in sepsis: source of and a target for inflammation. Crit. Care Med. 2001, 29:S21-S27.
57. Hahn B.H., Singh R.P., La Cava A., Ebling F.M. Tolerogenic treatment of lupus mice with consensus peptide induces Foxp3-expressing, apoptosis-resistant, TGFbeta-secreting CD8+ T cell suppressors. J. Immunol. 2005, 175:7728-7737.
58. Hardaway R.M. Traumatic shock. Mil. Med. 2006, 171:278-279.
59. Hemish J., Nakaya N., Mittal V., Enikolopov G. Nitric oxide activates diverse signaling pathways to regulate gene expression. J. Biol. Chem. 2003, 278:42321-42329.
60. Hibbs J.B., Taintor R.R., Vavrin Z. Macrophage cytotoxicity: Role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 1987, 235:473-476.
61. Hibbs J.B., Vavrin Z., Taintor R.R. L-arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. J. Immunol. 1987, 138:550.
62. Hierholzer C., Harbrecht B., Menezes J.M., Kane J., MacMicking J., Nathan C.F., Peitzman A.B., Billiar T.R., Tweardy D.J. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J. Exp. Med. 1998, 187:917-928.
63. Hon, W.M., Lee, K.H., Khoo, H.E., 2002. Nitric oxide in liver diseases - Friend, foe, or just passerby?
64. Hu T.M., Hayton W.L., Mallery S.R. Kinetic modeling of nitric-oxide-associated reaction network. Pharm. Res, 2006, 23:1702-1711.
65. Huber A., Saur D., Kurjak M., Schusdziarra V., Allescher H.D. Characterization and splice variants of neuronal nitric oxide synthase in rat small intestine. Am. J. Physiol. 1998, 275:G1146-G1156.
66. Huerta-Yepez S., Vega M., Jazirehi A., Garban H., Hongo F., Cheng G., Bonavida B. Nitric oxide sensitizes prostate carcinoma cell lines to TRAIL-mediated apoptosis via inactivation of NF-kappa B and inhibition of Bcl-xl expression. Oncogene 2004, 23:4993-5003.
67. Huie R.E., Padmaja A.S. The reaction of NO with superoxide. Free Radic. Res. Commun. 1993, 18:195-199.
68. Ibiza S., Perez-Rodriguez A., Ortega A., Martinez-Ruiz A., Barreiro O., Garcia-Dominguez C.A., Victor V.M., Esplugues J.V., Rojas J.M., Sanchez-Madrid F., Serrador J.M. Endothelial nitric oxide synthase regulates N-Ras activation on the Golgi complex of antigen-stimulated T cells. Proc. Natl. Acad. Sci. USA 2008, 105:10507-10512.
69. Ignarro L.J., Fukuto J.M., Griscavage J.M., Rogers N.E., Byrns R.E. Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate: comparison with enzymatically formed nitric oxide from L-arginine. Proc. Natl. Acad. Sci. USA 1993, 90:8103-8107.
70. Jaeschke H., Smith C.W. Mechanisms of neutrophil-induced parenchymal cell injury. J. Leukoc. Biol. 1997, 61:647-653.
71. Jawa R.S., Kulaylat M.N., Baumann H., Dayton M.T. What is new in cytokine research related to trauma/critical care. J. Intensive Care Med. 2006, 21:63-85.
72. Johnson M.L., Billiar T.R. Roles of nitric oxide in surgical infection and sepsis. World J. Surg. 1998, 22:187-196.
73. Ju H., Zou R., Venema V.J., Venema R.C. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol. Chem. 1997, 272:18522-18525.
74. Kholodenko B.N. Cell-signalling dynamics in time and space. Nat. Rev. Mol. Cell Biol. 2006, 7:165-176.
75. Kim Y.-M., Bergonia H.A., Müller C., Pitt B.R., Watkins W.D., Lancaster J.R. Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem. 1995, 270:5710-5713.
76. Kim Y.M., Bergonia H.A., Muller C., Pitt B.R., Watkins W.D., Lancaster J.R. Nitric oxide and intracellular heme. Adv. Pharmacol. 1995, 34:277-291.
77. Kim Y.M., Talanian R.V., Billiar T.R. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 1997, 272:31138-31148.
78. Kim Y.M., Bombeck C.A., Billiar T.R. Nitric oxide as a bifunctional regulator of apoptosis. Circ. Res. 1999, 84:253-256.
79. Kim Y.M., Chung H.T., Simmons R.L., Billiar T.R. Cellular non-heme iron content is a determinant of nitric oxide-mediated apoptosis, necrosis, and caspase inhibition. J. Biol. Chem. 2000, 275:10954-10961.
80. Kim P.K.M., Zamora R., Petrosko P., Billiar T.R. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 2001, 1:1421-1441.
81. Kim P.K.M., Zuckerbraun B.S., Otterbein L.E., Vodovotz Y., Billiar T.R. 'Til death do us part: nitric oxide and mechanisms of hepatotoxicity. Biol. Chem. 2004, 365:11-15.
82. Kim H.S., Loughran P.A., Kim P.K., Billiar T.R., Zuckerbraun B.S. Carbon monoxide protects hepatocytes from TNF-alpha/Actinomycin D by inhibition of the caspase-8-mediated apoptotic pathway. Biochem. Biophys. Res. Commun. 2006, 344:1172-1178.
83. Kim H.S., Loughran P.A., Billiar T.R. Carbon monoxide decreases the level of iNOS protein and active dimer in IL-1 beta-stimulated hepatocytes. Nitric Oxide 2008, 18:256-265.
84. Kim H.S., Loughran P.A., Rao J., Billiar T.R., Zuckerbraun B.S. Carbon monoxide activates NF-kappa B via ROS generation and Akt pathways to protect against cell death of hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295:G146-G152.
85. Kitano H. Systems biology: A brief overview. Science 2002, 295:1662-1664.
86. Kitano H. Computational cellular dynamics: a network-physics integral. Nat. Rev. Mol. Cell Biol. 2006, 7:163.
87. Kobayashi Y., Kume A., Li M., Doyu M., Hata M., Ohtsuka K., Sobue G. Chaperones Hsp70 and Hsp40 suppress aggregate formation and apoptosis in cultured neuronal cells expressing truncated androgen receptor protein with expanded polyglutamine tract. J. Biol. Chem. 2000, 275:8772-8778.
88. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 2008, 9:1004-1010.
89. Kuncewicz T., Balakrishnan P., Snuggs M.B., Kone B.C. Specific association of nitric oxide synthase-2 with Rac isoforms in activated murine macrophages. Am. J. Physiol. Renal Physiol. 2001, 281:F326-F336.
90. Lagoa C.E., Bartels J., Baratt A., Tseng G., Clermont G., Fink M.P., Billiar T.R., Vodovotz Y. The role of initial trauma in the host's response to injury and hemorrhage: Insights from a comparison of mathematical simulations and hepatic transcriptomic analysis. Shock 2006, 26:592-600.
91. Lancaster J. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc. Natl. Acad. Sci. USA 1994, 91:8137-8141.
92. Landry D.W., Oliver J.A. The pathogenesis of vasodilatory shock. N. Engl. J. Med. 2001, 345:588-595.
93. Langer D.A., Das A., Semela D., Kang-Decker N., Hendrickson H., Bronk S.F., Katusic Z.S., Gores G.J., Shah V.H. Nitric oxide promotes caspase-independent hepatic stellate cell apoptosis through the generation of reactive oxygen species. Hepatology 2008, 47:1983-1993.
94. Lee V.G., Johnson M.L., Baust J., Laubach V.E., Watkins S.C., Billiar T.R. The roles of iNOS in liver ischemia-reperfusion injury. Shock 2001, 16:355-360.
95. Legewie S., Bluthgen N., Herzel H. Mathematical modeling identifies inhibitors of apoptosis as mediators of positive feedback and bistability. PLoS Comput. Biol. 2006, 2:1061-1073.
96. Levine B., Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell. 2004, 6:463-477.
97. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
98. Li C.Q., Wogan G.N. Nitric oxide as a modulator of apoptosis. Cancer Lett. 2005, 226:1-15.
99. Li J.R., Billiar T.R., Talanian R.V., Kim Y.M. Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem. Biophys. Res. Commun. 1997, 240:419-424.
100. Loughran P.A., Stolz D.B., Vodovotz Y., Watkins S.C., Simmons R.L., Billiar T.R. Monomeric inducible nitric oxide synthase localizes to peroxisomes in hepatocytes. Proc. Natl Acad. Sci. USA 2005, 102:13837-13842.
101. Lundberg J.O., Weitzberg E., Gladwin M.T. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discov. 2008, 7:156-167.
102. Mahidhara R., Billiar T.R. Apoptosis in sepsis. Crit. Care Med. 2000, 28:N105-N113.
103. Matzinger P. The danger model: a renewed sense of self. Science 2002, 296:301-305.
104. Mayers I., Johnson D. The nonspecific inflammatory response to injury. Can. J. Anaesth. 1998, 45:871-879.
105. McMillan K., Masters B.S. Prokaryotic expression of the heme- and flavin-binding domains of rat neuronal nitric oxide synthase as distinct polypeptides: identification of the heme-binding proximal thiolate ligand as cysteine-415. Biochemistry 1995, 34:3686-3693.
106. McMillan K., Bredt D.S., Hirsch D.J., Snyder S.H., Clark J.E., Masters B.S. Cloned, expressed rat cerebellar nitric oxide synthase contains stoichiometric amounts of heme, which binds carbon monoxide. Proc. Natl. Acad. Sci. USA 1992, 89:11141-11145.
107. Messmer U.K., Brune B. Nitric oxide-induced apoptosis: p53-dependent and p53-independent signalling pathways. Biochem. J. 1996, 319(Pt 1):299-305.
108. Messmer U.K., Ankarcrona M., Nicotera P., Brune B. p53 expression in nitric oxide-induced apoptosis. FEBS Lett. 1994, 355:23-26.
109. Migita K., Yamasaki S., Kita M., Ida H., Shibatomi K., Kawakami A., Aoyagi T., Eguchi K. Nitric oxide protects cultured rheumatoid synovial cells from Fas-induced apoptosis by inhibiting caspase-3. Immunology 2001, 103:362-367.
110. Mollen K.P., Anand R.J., Tsung A., Prince J.M., Levy R.M., Billiar T.R. Emerging paradigm: toll-like receptor 4-sentinel for the detection of tissue damage. Shock 2006, 26:430-437.
111. Motterlini R., Green C.J., Foresti R. Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid. Redox Signal 2002, 4:615-624.
112. Nathan C., Xie Q.-W. Nitric oxide synthases: Roles, tolls, and controls. Cell 1994, 78:915-918.
113. Naughton P., Foresti R., Bains S.K., Hoque M., Green C.J., Motterlini R. Induction of heme oxygenase 1 by nitrosative stress. A role for nitroxyl anion. J. Biol. Chem. 2002, 277:40666-40674.
114. Neugebauer E.A., Willy C., Sauerland S. Complexity and non-linearity in shock research: reductionism or synthesis?. Shock 2001, 16:252-258.
115. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A., et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376:37-43.
116. Nussler A.K., Di Silvio M., Billiar T.R., Hoffman R.A., Geller D.A., Selby R., Madariage J., Simmons R.L. Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J. Exp. Med. 1992, 176:261.
117. Olson S.Y., Garban H.J. Regulation of apoptosis-related genes by nitric oxide in cancer. Nitric Oxide 2008, 19:170-176.
118. Ou J., Carlos T.M., Watkins S.C., Saavedra J.E., Keefer L.K., Kim Y.M., Harbrecht B.G., Billiar T.R. Differential effects of nonselective nitric oxide synthase (NOS) and selective inducible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression, and neutrophil accumulation during endotoxemia. Nitric Oxide 1997, 1:404-416.
119. Papapetropoulos A., Desai K.M., Rudic R.D., Mayer B., Zhang R., Ruiz-Torres M.P., Garcia-Cardena G., Madri J.A., Sessa W.C. Nitric oxide synthase inhibitors attenuate transforming-growth-factor- beta 1-stimulated capillary organization in vitro. Am. J. Pathol. 1997, 150:1835-1844.
120. Papapetropoulos A., Rudic R.D., Sessa W.C. Molecular control of nitric oxide synthases in the cardiovascular system. Cardiovasc. Res. 1999, 43:509-520.
121. Pattingre S., Tassa A., Qu X.P., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
122. Peitzman A.B., Billiar T.R., Harbrecht B.G., Kelly E., Udekwu A.O., Simmons R.L. Hemorrhagic shock. Curr. Probl. Surg. 1995, 32:925-1002.
123. Peng H.B., Libby P., Liao J.K. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J. Biol. Chem. 1995, 270:14214-14219.
124. Pilz R.B., Casteel D.E. Regulation of gene expression by cyclic GMP. Circ. Res. 2003, 93:1034-1046.
125. Potoka D.A., Nadler E.P., Upperman J.S., Ford H.R. Role of nitric oxide and peroxynitrite in gut barrier failure. World J. Surg. 2002, 26:806-811.
126. Prince J.M., Levy R.M., Bartels J., Baratt A., Kane J.M., Lagoa C., Rubin J., Day J., Wei J., Fink M.P., Goyert S.M., Clermont G., Billiar T.R., Vodovotz Y. In silico and in vivo approach to elucidate the inflammatory complexity of CD14-deficient mice. Mol. Med. 2006, 12:88-96.
127. Pryor W.A., Squadrito G.L. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 1995, 268:699-722.
128. Rabkin S.W. Nitric oxide-induced cell death in the heart: the role of autophagy. Autophagy 2007, 3:347-349.
129. Rabkin S.W., Klassen S.S. Nitric oxide differentially regulates the gene expression of caspase genes but not some autophagic genes. Nitric Oxide 2007, 16:339-347.
130. Ratovitski E.A., Bao C., Quick R.A., McMillan A., Kozlovsky C., Lowenstein C.J. An inducible nitric-oxide synthase (NOS)-associated protein inhibits NOS dimerization and activity. J. Biol. Chem. 1999, 274:30250-30257.
131. Remick D.G., Villarete L. Regulation of cytokine gene expression by reactive oxygen and reactive nitrogen intermediates. J. Leukoc. Biol. 1996, 59:471-475.
132. Rose S., Marzi I. Mediators in polytrauma-pathophysiological significance and clinical relevance. Langenbecks Arch. Surg. 1998, 383:199-208.
133. Salvucci O., Carsana M., Bersani I., Tragni G., Anichini A. Antiapoptotic role of endogenous nitric oxide in human melanoma cells. Cancer Res. 2001, 61:318-326.
134. Sengupta R., Ryter S.W., Zuckerbraun B.S., Tzeng E., Billiar T.R., Stoyanovsky D.A. Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry 2007, 46:8472-8483.
135. Siehs C., Oberbauer R., Mayer G., Lukas A., Mayer B. Discrete simulation of regulatory homo- and heterodimerization in the apoptosis effector phase. Bioinformatics 2002, 18:67-76.
136. Spencer J.P.E., Wong J., Jenner A., Aruoma O.I., Cross C.E., Halliwell B. Base modification and strand breakage in isolated calf thymus DNA and in DNA from human skin epidermal keratinocytes exposed to peroxynitrite or 3-morpholinosydnonimine. Chem. Res. Toxicol. 1996, 9:1152-1158.
137. Stassi G., De M.R., Trucco G., Rudert W., Testi R., Galluzzo A., Giordano C., Trucco M. Nitric oxide primes pancreatic beta cells for Fas-mediated destruction in insulin-dependent diabetes mellitus. J. Exp. Med. 1997, 186:1193-1200.
138. Stolz D.B., Zamora R., Vodovotz Y., Loughran P.A., Billiar T.R., Kim Y.M., Simmons R.L., Watkins S.C. Peroxisomal localization of inducible nitric oxide synthase in hepatocytes. Hepatology 2002, 36:81-93.
139. Stone J.R., Marletta M.A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 1994, 33:5636-5640.
140. Stucki J.W., Simon H.U. Mathematical modeling of caspase-3 activation and degradation. J. Theor. Biol. 2005, 234:123-131.
141. Stuehr D.J., Ikeda-Saito M. Spectral characterization of brain and macrophage nitric oxide synthases. J. Biol. Chem. 1992, 267:20547-20550.
142. Taylor B.S., Alarcon L.H., Billiar T.R. Inducible nitric oxide synthase in the liver: regulation and function. Biochemistry Mosc. 1998, 63:766-781.
143. Thomas D.D., Miranda K.M., Colton C.A., Citrin D., Espey M.G., Wink D.A. Heme proteins and nitric oxide (NO): the neglected, eloquent chemistry in NO redox signaling and regulation. Antioxid. Redox Signal 2003, 5:307-317.
144. Torres A., Bentley T., Bartels J., Sarkar J., Barclay D., Namas R., Constantine G., Zamora R., Puyana J.C., Vodovotz Y. Mathematical modeling of post-hemorrhage inflammation in mice: studies using a novel, computer-controlled, closed-loop hemorrhage apparatus. Shock 2009, 32:172-178.
145. Tzeng E., Billiar T.R., Robbins P.D., Loftus M., Stuehr D.J. Expression of human inducible nitric oxide synthase in a tetrahydrobiopterin (H4B)-deficient cell line: H4B promotes assembly of enzyme subunits into an active dimer. Proc. Natl. Acad. Sci. USA 1995, 92:11771-11775.
146. Upperman J.S., Potoka D., Grishin A., Hackam D., Zamora R., Ford H.R. Mechanisms of nitric oxide-mediated intestinal barrier failure in necrotizing enterocolitis. Semin. Pediatr. Surg. 2005, 14:159-166.
147. Vande V.C., Cizeau J., Dubik D., Alimonti J., Brown T., Israels S., Hakem R., Greenberg A.H. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell Biol. 2000, 20:5454-5468.
148. Vodovotz Y., Russell D., Xie Q.-W., Bogdan C., Nathan C. Vesicle association of nitric oxide synthase from primary mouse macrophages. J. Immunol. 1995, 154:2914-2925.
149. Vodovotz Y., Letterio J.J., Geiser A.G., Chesler L., Roberts A.B., Sparrow J. Control of nitric oxide production by endogenous transforming growth factorβ1 and systemic nitric oxide in retinal pigment epithelial cells and peritoneal macrophages. J. Leukoc. Biol. 1996, 60:261-270.
150. Vodovotz Y., Kim P.K.M., Bagci Z., Ermentrout G.B., Chow C.C., Bahar I., Billiar T.R. Inflammatory modulation of hepatocyte apoptosis by nitric oxide: In vivo, in vitro and in silico studies. Curr. Mol. Med. 2004, 4:753-762.
151. Vodovotz Y., Csete M., Bartels J., Chang S., An G. Translational systems biology of inflammation. PLoS. Comput. Biol. 2008, 4:1-6.
152. Vodovotz Y., Constantine G., Rubin J., Csete M., Voit E.O., An G. Mechanistic simulations of inflammation: Current state and future prospects. Math. Biosci. 2009, 217:1-10.
153. Volk H.D., Reinke P., Docke W.D. Clinical aspects: from systemic inflammation to 'immunoparalysis'. Chem. Immunol. 2000, 74:162-177.
154. Wang, Y., Vodovotz, Y., Kim, P.K.M., Zamora, R., Billiar, T.R., 2001. Mechanisms of hepatoprotection by nitric oxide. Ann. NY Acad. Sci.
155. Wang Y., Vodovotz Y., Kim P.K.M., Zamora R., Billiar T.R. Mechanisms of hepatoprotection by nitric oxide. Ann. NY Acad. Sci. 2002, 962:415-422.
156. Watanabe Y., Nishio M., Hamaji S., Hayashi Y., Hu Y., Hidaka H. Neuronal nitric oxide synthase-membrane phospholipid interactions. Arch. Biochem. Biophys. 1998, 358:68-73.
157. Webster K.A., Graham R.M., Bishopric N.H. BNip3 and signal-specific programmed death in the heart. J. Mol. Cell Cardiol. 2005, 38:35-45.
158. Wei M.C., Zong W.X., Cheng E.H.Y., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacCregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
159. Weller R., Schwentker A., Billiar T.R., Vodovotz Y. Autologous nitric oxide protects mouse and human keratinocytes from ultraviolet B radiation-induced apoptosis. Am. J. Physiol. 2003, 284:C1140-C1148.
160. Wink D.A., Mitchell J.B. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 1998, 25:434-456.
161. Wink D.A., Nims R.W., Darbyshire J.F., Christodoulou D., Hanbauer I., Cox G.W., Laval F., Laval J., Cook J.A., Krishna M.C., Degraff W.G., Mitchell J.B. Reaction kinetics for nitrosation of cysteine and glutathione in aerobic nitric oxide solutions at neutral pH. Insights into the fate and physiological effects of intermediates generated in the NO/O2 reaction. Chem. Res. Toxicol. 1994, 7:519-525.
162. Wink D.A., Feelisch M., Vodovotz Y., Fukuto J., Grisham M.B. The chemical biology of nitric oxide. Reactive Oxygen Species in Biological Systems: An Interdisciplinary Approach 1999, 245-291. Kluwer Academic/Plenum Publishing, New York. D.L. Gilbert, C.A. Colton (Eds.).
163. Wyllie A.H., Kerr J.F., Currie A.R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 1980, 68:251-306.
164. Xie Q.-W., Nathan C. The high-output nitric oxide pathway: role and regulation. J. Leukoc. Biol. 1994, 56:576-582.
165. Yang J., Wu L.J., Tashino S., Onodera S., Ikejima T. Reactive oxygen species and nitric oxide regulate mitochondria-dependent apoptosis and autophagy in evodiamine-treated human cervix carcinoma HeLa cells. Free Radic. Res. 2008, 42:492-504.
166. Yee E.L., Pitt B.R., Billiar T.R., Kim Y.M. Effect of nitric oxide on heme metabolism in pulmonary artery endothelial cells. Am. J. Physiol. 1996, 271:L512-L518.
167. Yuan J., Horvitz H.R. A first insight into the molecular mechanisms of apoptosis. Cell 2004, 116(2 Suppl):S53-S56. 1 p following S59.
168. Zamora R., Vodovotz Y., Billiar T.R. Inducible nitric oxide synthase and inflammatory diseases. Mol. Med. 2000, 6:347-373.
169. Zamora R., Alarcon L., Vodovotz Y., Betten B., Kim P.K., Gibson K.F., Billiar T.R. Nitric oxide suppresses the expression of Bcl-2 binding protein BNIP3in hepatocytes. J. Biol. Chem. 2001, 276:46887-46895.
170. Zamora R., Bryan N.S., Boyle P., Wong C., Milsom A.B., Jaffe R., Feelisch M., Ford H.R. Nitrosative stress in an animal model of necrotizing enterocolitis. Free Radic. Biol. Med. 2005, 39:1428-1437.
171. Zamora R., Vodovotz Y., Betten B., Wong C., Zuckerbraun B., Gibson K.F., Ford H.R. Intestinal and hepatic expression of BNIP3in necrotizing enterocolitis: regulation by nitric oxide and peroxynitrite. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G822-G830.
172. Zhang W., Kuncewicz T., Yu Z.Y., Zou L., Xu X., Kone B.C. Protein-protein interactions involving inducible nitric oxide synthase. Acta Physiol. Scand. 2003, 179:137-142.
173. Zong W.X., Lindsten T., Ross A.J., MacGregor G.R., Thompson C.B. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 2001, 15:1481-1486.
174. Zuckerbraun B.S., Billiar T.R., Otterbein S.L., Kim P.K.M., Liu F., Choi A.M.K., Bach F.H., Otterbein L.E. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J. Exp. Med. 2003, 198:1707-1716.