Inhibition of protein synthesis by nitric oxide correlates with cytostatic activity: Nitric oxide induces phosphorylation of initiation factor eIF-2α

Molecular Medicine

Volumn 4, Issue 3, 1998, Pages 179-190

  Kim, Young Myeong ^a,b,d   Son, Kyonghee ^c   Hong, Sun Joo ^d   Green, Angela ^a   Chen, Jane Jane ^e   Tzeng, Edith ^a   Hierholzer, Christian ^a   Billiar, Timothy R ^a,f  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

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

^c RUTGERS UNIVERSITY   (United States)

^d Kangwon National University   (South Korea)

^e HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^f PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2; NITRIC OXIDE;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CYTOSTASIS; KNOCKOUT MOUSE; MOUSE; NONHUMAN; OVARY TUMOR; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS;

EID: 0031902602     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.1007/bf03401915     Document Type: Article

References (44)

1. Billiar TR. (1995) Nitric oxide: Novel biology with clinical relevance. Am. Surg. 221: 339-349.
2. Nathan C, Xie QW. (1994) Nitric oxide synthases: Roles, tolls, and controls. Cell 78: 915-918.
3. Nathan C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J. 6: 3051-3064.
4. Farias-Eisner R, Sherman MP, Aeberhard E, Chaudhuri G. (1994) Nitric oxide is an important mediator for tumoricidal activity in vivo. Proc. Natl. Acad. Sci. USA 91: 9407-9411.
5. Son K, Kim YM. (1995) In vivo cisplatin-exposed macrophages increase immunostimulant-induced nitric oxide synthesis for tumor cell killing. Cancer Res. 55: 5524-5527.
6. Kim YM, Hong SJ, Billiar TR, Simmons RL. (1996) Counterprotective effect of erythrocytes in experimental bacterial peritonitis is due to scavenging of nitric oxide and reactive oxygen intermediates. Infect. Immun. 64: 3074-3080.
7. Lepoivre M, Flaman JM, Bobe P, Lemaire G, Henry Y. (1994) Quenching of the tyrosyl free radical of ribonucleotide reductase by nitric oxide. Relationship to cytostasis induced in tumor cells by cytotoxic macrophages. J. Biol. Chem. 269: 21891-21897.
8. Drapier JC, Hibbs JB Jr. (1986) Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. Inhibition involves the iron-sulfur prosthetic group and is reversible. J. Clin. Invest. 78: 790-797.
9. Drapier JC, Hibbs JB Jr. (1988) Differentiation of murine macrophages to express nonspecific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur enzymes in the macrophage effector cells. J. Immunol. 140: 2829-2838.
10. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and super-oxide. Proc. Natl. Acad. Sci. USA 87: 1620-1624.
11. Kim YM, Bergonia HA, Muller C, Pitt BR, Watkins WD, Lancaster JR Jr. (1995) Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem. 270: 5710-5713.
12. Kim YM, de Vera JE, Watkins SC, Billiar TR. (1997) Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 272: 1402-1411.
13. Kim YM, Bergonia HA, Muller C, Pitt BR, Watkins WD, Lancaster JR Jr. (1995) Nitric oxide and intracellular heme. Adv. Pharmacol. 34: 277-291.
14. Curran RD, Billiar TR, Stuehr DJ, Hofmann K, Simmons RL. (1989) Hepatocytes produce nitrogen oxides from L-arginine in response to inflammatory products of Kupffer cells. J. Exp. Med. 170: 1769-1774.
15. Billiar TR, Curran RD, Stuehr DJ, West MA, Bentz BG, Simmons RL. (1989) An L-arginine dependent mechanism mediates Kupffer cell influences on hepatocyte protein synthesis in vitro. J. Exp. Med. 169: 1467-1472.
16. Curran RD, Ferrari FK, Kispert PH, et al. (1991) Nitric oxide and nitric oxide-generating compounds inhibit hepatocyte protein synthesis. FASEB J. 5: 2085-2092.
17. Jenkins DC, Charles IG, Thomsen LL, et al. (1995) Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA 92: 4392-4396.
18. Karupiah G, Xie QW, Buller RM, Nathan C, Duarte C, MacMicking JD. (1993) Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science 261: 1445-1448.
19. Lowenstein CJ, Hill SL, Lafond-Walker A, et al. (1996) Nitric oxide inhibits viral replication in murine myocarditis. J. Clin. Invest. 97: 1837-1843.
20. Corbett JA, Lancaster JR Jr, Sweetland MA, McDaniel ML. (1991) Interleukin-1-beta-induced formation of EPR-detectable iron-nitrosyl complexes in islets of Langerhans. Role of nitric oxide in interleukin-1-beta-induced inhibition of insulin secretion. J. Biol. Chem. 266: 21351-21354.
21. De Benedetti A, Baglioni C. (1983) Phosphorylation of initiation factor eIF-2α, binding of mRNA to 48S complexes, and its reutilization in initiation of protein synthesis. J. Biol. Chem. 258: 14556-14562.
22. Chen JJ, Throop MS, Gehrke L, et al. (1991) Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2 alpha (eIF-2α) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2α kinase. Proc. Natl. Acad. Sci. USA 88: 7729-7733.
23. Crosby JS, Lee K, London IM, Chen JJ. (1994) Erythroid expression of the heme-regulated eIF-2 alpha kinase. Mol. Cell. Biol. 14: 3906-3914.
24. Samuel CE. (1993) The eIF-2α protein kinase, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 268: 7603-7606.
25. Meurs EF, Watanabe Y, Kadereit S, et al. (1992) Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus growth. J. Virol. 66: 5804-5814.
26. Meurs EF, Galabru J, Barber GN, Katze MG, Hovanessian AG. (1993) Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 90: 232-236.
27. Hinnebusch AG. (1994) The eIF-2 alpha kinases: Regulators of protein synthesis in starvation and stress. Semin. Cell Biol. 5: 417-426.
28. Saville B. (1958) A scheme for the colorimetric determination of microgram amounts of thiol. Analyst 83: 670-672.
29. Tzeng E, Kim YM, Pitt BR, Lizonova A, Kovesdi I, Billiar TR. (1997) Adenoviral transfer of the induciblc nitric oxide synthase gene blocks endothelial cell apoplosis. Surgery 122: 255-263.
30. Kwon G, Bohrer A, Han X, et al. (1996) Characterization of the sphingomyelin content of isolated pancreatic islets. Evaluation of the role of sphingomyelin hydrolysis in the action of interleukin-1 to induce islet overproduction of nitric oxide. Biochim. Biophys. Acta 1300: 63-72.
31. Kim YM, Son K. (1996) A nitric oxide production bioassay for interferon-gamma. J. Immunol. Methods 198: 203-209.
32. Chen W, Drillien R, Spehner D, Buller RML. (1992) Restricted replication of Ectromelia virus in cell culture correlates with mutations in virus-encoded host range gene. Virology 187: 433-442.
33. Maurides PA, Akkaraju GR, Jagus R. (1989) Evaluation of protein phosphorylation state by a combination of vertical slab gel isoelectric focusing and immunoblotting. Anal. Biochem. 183: 144-151.
34. Kim YM, Lancaster JR Jr. (1993) Tetrahydrobiopterin-dependent nitrite oxidation to nitrate in isolated rat hepatocyles. FEBS Lett. 332: 255-259.
35. Der SD, Lau AS. (1995) Involvement of the double-stranded-RNA-dependent kinase PKR in interferon expression and interferon-mediated antiviral activity. Proc. Natl. Acad. Sci. USA 92: 8841-8845.
36. Corbett JA, Sweetland MA, Wang JL, Lancaster JR Jr, McDaniel ML. (1993) Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans. Proc. Natl. Acad. Sci. USA 90: 1731-1735.
37. Stadter J, Bergonia HA, Di Silvio M, et al. (1993) Nonheme iron-nitrosyl complex formation in rat hepatocytes: detection by electron paramagnetic resonance spectroscopy. Arch. Biochem. Biophys. 302: 4-11.
38. Yang JM, London IM, Chen JJ. (1992) Effects of hemin and porphyrin compounds on intersubunit disulfide formation in heme-regulated eIF-2 alpha kinase and the regulation of protein synthesis in reticulocyte lysates. J. Biol Chem. 267: 20519-20524.
39. Ramaiah KV, Dhindsa RS, Chen JJ, London IM, Levein D. (1992) Recycling and phosphorylation of eukaryotic initiation factor 2 on 60S subunits of 80S initiation complexes and polysomes. Proc. Natl. Acad. Sci. USA 89: 12063-12067.
40. Sheffler LA, Wink DA, Melillo G, Cox GW. (1995) Exogenous nitric oxide regulates IFN-gamma plus lipopolysaccharide-induced nitric oxide synthase expression in mouse macrophages. J. Immunol. 155: 886-894.
41. Hibbs JB Jr, Taintor RR, Vavrin Z. (1987) Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 235: 473-476.
42. Drapier JC, Hibbs JB Jr. (1988) Differentiation of marine macrophages to express nonspecific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur enzymes in the macrophage effector cells. J. Immunol. 140: 2829-2838.
43. Petryshyn R, Trachsel H, London IM. (1979) Regulation of protein synthesis in reticulocyte lysates: Immune serum inhibits heme-regulated protein kinase activity and differentiates heme-regulated protein kinase from double-stranded RNA-induced protein kinase. Proc. Natl. Sci. USA 76: 1575-1579.
44. Wu S, Kaufman RJ. (1997) A model for the double-stranded RNA (dsRNA)-dependent dimerization and activation of the dsRNA-activated protein kinase PKR. J. Biol. Chem. 272: 1291-1296.