Roles of heme oxygenase-1 in the antiproliferative and antiapoptotic effects of nitric oxide on Jurkat T cells

Molecular Pharmacology

Volumn 66, Issue 1, 2004, Pages 122-128

  Pae, Hyun Ock ^a   Choi, Byung Min ^a   Oh, Gi Su ^a   Lee, Myeong Su ^a   Ryu, Do Gon ^b   Rhew, Hyun Yul ^c   Kim, Yung Myung ^d   Chung, Hun Taeg ^a,b  

^a Wonkwang University School of Medicine   (South Korea)

^b Wonkwang University   (South Korea)

^c Kosin University   (South Korea)

^d Kangwon National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BILIVERDIN; CONCANAVALIN A; DIMER; FAS ANTIBODY; HEME OXYGENASE 1; IRON; NITROPRUSSIDE SODIUM; OLIGONUCLEOTIDE; PHOSPHOROTHIOIC ACID; PROTOPORPHYRIN; RUTHENIUM; TRICARBOXYLIC ACID;

ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL TYPE; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LEUKEMIA CELL LINE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VASCULAR SMOOTH MUSCLE;

ANTIGENS, CD95; APOPTOSIS; CARBON MONOXIDE; CELL DIVISION; FERRIC COMPOUNDS; GENE EXPRESSION; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; JURKAT CELLS; MEMBRANE PROTEINS; NITRIC OXIDE; T-LYMPHOCYTES;

EID: 3042523740     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.66.1.122     Document Type: Article

References (36)

1. Alam A, Cohen LY, Aouad S, and Sekaly PR (1999) Early activation of caspases during T lymphocyte stimulation results in selective substrate cleavage in non-apoptotic cells. J Exp Med 190:1879-1890.
2. Alcaraz MJ, Fernandez P, and Guillen MI (2003) Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr Pharm Des 9:2541-2551.
3. Alcaraz MJ, Habib A, Creminon C, Vicente AM, Lebret M, Levy-Toledano S, and Maclouf J (2001) Heme oxygenase-1 induction by nitric oxide in RAW 264.7 macrophages is upregulated by a cyclo-oxygenase-2 inhibitor. Biochim Biophys Acta 1526:13-16.
4. Alcaraz MJ, Habib A, Lebret M, Creminon C, Levy-Toledano S, and Maclouf J (2000) Enhanced expression of haem oxygenase-1 by nitric oxide and anti-inflammatory drugs in NIH 3T3 fibroblasts. Br J Pharmacol 130:57-64.
5. Beltran B, Quintero M, Garcia-Zaragoza E, O'Connor E, Esplugues JV, and Moncada S (2002) Inhibition of mitochondrial respiration by endogenous nitric oxide: a critical step in Fas signaling. Proc Natl Acad Sci USA 99:8892-8897.
6. Bernassola F, Catani MV, Corazzari M, Rossi A, and Melino G (2001) Inactivation of multiple targets by nitric oxide in CD95-triggered apoptosis. J Cell Biochem 82:123-133.
7. Bingisser RM, Tilbrook PA, Holt PG, and Kees UR (1998) Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol 160:5729-5734.
8. Bredt DS (1999) Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 31:577-596.
9. Bronte V, Serafini P, Mazzoni A, Segal DM, and Zanovello P (2003) L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol 24:302-306.
10. Choi BM, Pae HO, Kim YM, and Chung HT (2003) Nitric oxide-mediated cytoprotection of hepatocytes from glucose deprivation-induced cytotoxicity: involvement of heme oxygenase-1. Hepatology 37:810-823.
11. Choi BM, Pae HO, Jeong YR, Oh GS, Jun CD, Kim BR, Kim YM, and Chung HT (2004) Overexpression of heme oxygenase (HO)-1 renders jurkat T cells resistant to Fas-mediated apoptosis: involvement of iron released by HO-1. Free Radic Biol Med 36:858-871.
12. Durante W (2003) Heme oxygenase-1 in growth control and its clinical application to vascular disease. J Cell Physiol 95:373-382.
13. Hartsfield CL, Alam J, Cook JL, and Choi AM (1997) Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol 273:L980-L988.
14. Hickman-Davis JM, Fang FC, Nathan C, Shepherd VL, Voelker DR, and Wright JR (2001) Lung surfactant and reactive oxygen-nitrogen species: antimicrobial activity and host-pathogen interactions. Am J Physiol 281:L517-L523.
15. Hoffman RA, Mahidhara RS, Wolf-Johnston AS, Lu L, Thomson AW, and Simmons RL (2002) Differential modulation of CD4 and CD8 T-cell proliferation by induction of nitric oxide synthesis in antigen presenting cells. Transplantation 74:836-845.
16. Kawashima A, Oda Y, Yachie A, Koizumi S, and Nakanishi I (2002) Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol 33:125-130.
17. Kennedy NJ, Kataoka T, Tschopp J, and Budd RC (1999) Caspase activation is required for T cell proliferation. J Exp Med 190:1891-1896.
18. Kosonen O, Kankaanranta H, Lahde M, Vuorinen P, Ylitalo P, and Moilanen E (1998) Nitric oxide-releasing oxatriazole derivatives inhibit human lymphocyte proliferation by a cyclic GMP-independent mechanism. J Pharmacol Exp Ther 286:215-220.
19. Kosonen O, Kankaanranta H, Vuorinen P, and Moilanen E (1997) Inhibition of human lymphocyte proliferation by nitric oxide-releasing oxatriazole derivatives. Eur J Pharmacol 337:55-61.
20. Kroncke KD, Fehsel K, Suschek C, and Kolb-Bachofen V (2001) Inducible nitric oxide synthase-derived nitric oxide in gene regulation, cell death and cell survival. Int Immunopharmacol 1:1407-1420.
21. Mahidhara RS, Hoffman RA, Huang S, Wolf-Johnston A, Vodovotz Y, Simmons RL, and Billiar TR (2003) Nitric oxide-mediated inhibition of caspase-dependent T lymphocyte proliferation. J Leukoc Biol 74:403-411.
22. Morse D and Choi AM (2002) Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27:8-16.
23. Otterbein LE, Soares MP, Yamashita K, and Bach FH (2003a) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449-455.
24. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, et al (2003b) Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 9:183-190.
25. Pae HO, Oh GS, Choi BM, Chae SC, and Chung HT (2003) Differential expressions of heme oxygenase-1 gene in CD25- and CD25+ subsets of human CD4+ T cells. Biochem Biophys Res Commun 306:701-705.
26. Pae HO, Kim HG, Paik YS, Paik SG, Kim YM, Oh GS, and Chung HT (2000) Nitric oxide protects murine embryonic liver cells (BNL CL. 2) from cytotoxicity induced by glucose deprivation. Pharmacol Toxicol 86:140-144.
27. Poss KD and Tonegawa S (1997) Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA 94:10919-10924.
28. Sawle P, Foresti R, Green CJ, and Motterlini R (2001) Homocysteine attenuates endothelial haem oxygenase-1 induction by nitric oxide (NO) and hypoxia. FEBS Lett 508:403-406.
29. Simoncic PD, Lee-Loy A, Barber DL, Tremblay ML, and McGlade CJ (2002) The T cell protein tyrosine phosphatase is a negative regulator of janus family kinases 1 and 3. Curr Biol 12:446-453.
30. Song R, Mahidhara RS, Liu F, Ning W, Otterbein LE, and Choi AM (2002) Carbon monoxide inhibits human airway smooth muscle cell proliferation via mitogenactivated protein kinase pathway. Am J Respir 27:603-610.
31. Song R, Mahidhara RS, Zhou Z, Hoffman RA, Seol DW, Flavell RA, Billiar TR, Otterbein LE, and Choi AM (2004) Carbon monoxide inhibits T lymphocyte proliferation via caspase-dependent pathway. J Immunol 172:1220-1226.
32. Umansky V, Ratter F, Lampel S, Bucur M, Schirrmacher V, and Ushmorov A (2001) Inhibition of nitric-oxide-mediated apoptosis in Jurkat leukemia cells despite cytochrome c release. Exp Cell Res 265:274-282.
33. van der Veen RC (2001) Nitric oxide and T helper cell immunity. Int Immunopharmacol 1:1491-1500.
34. Wagener FA, da Silva JL, Farley T, de Witte T, Kappas A, and Abraham NG (1999) Differential effects of heme oxygenase isoforms on heme mediation of endothelial intracellular adhesion molecule 1 expression. J Pharmacol Exp Ther 291:416-423.
35. Wei XQ, Charles IG, Smith A, Ure J, Feng GJ, Huang FP, Xu D, Muller W, Moncada S, and Liew FY (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature (Lond) 375:408-411.
36. Zech B, Kohl R, von Knethen A, and Brune B (2003) Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases. Biochem J 371:1055-1064.