Microarray Study of Genes Differentially Modulated in Response to Nitric Oxide in Macrophages

  • Nan, Xuehua (Department of Biology, Institute of Bioscience and Biotechnology, Chungnam National University) ;
  • Maeng, Oky (Department of Biology, Institute of Bioscience and Biotechnology, Chungnam National University) ;
  • Shin, Hyo-Jung (Department of Biology, Institute of Bioscience and Biotechnology, Chungnam National University) ;
  • An, Hyun-Jung (Department of Biology, Institute of Bioscience and Biotechnology, Chungnam National University) ;
  • Yeom, Young-Il (Korea Research Institute of Bioscience and Biotechnology) ;
  • Lee, Hay-Young (Department of Biology, Institute of Bioscience and Biotechnology, Chungnam National University) ;
  • Paik, Sang-Gi (Department of Biology, Institute of Bioscience and Biotechnology, Chungnam National University)
  • Published : 2008.03.31

Abstract

Nitric oxide(NO) has been known to play important roles in numerous physiologic processes including neurotransmission, vasorelaxation, and cellular apoptosis. Using a mouse cDNA gene chip, we examined expression patterns and time course of NO-dependent genes in mouse macrophage RAW264.7 cells. Genes shown to be upregulated more than two fold or at least at two serial time points were further selected and validated by RT-PCR. Finally, 81 selected genes were classified by function as signaling, apoptosis, inflammation, transcription, translation, ionic homeostasis and metabolism. Among those, genes related with signaling, apoptosis and inflammation, such as guanylate cyclase 1, soluble, alpha3(Gucy1a3); protein kinase C, alpha($Pkc{\alpha}$); lymphocyte protein tyrosine kinase(Lck); BCL2/adenovirus E1B 19 kDa-interacting protein(Bnip3); apoptotic protease activating factor 1(Apaf1); X-linked inhibitor of apoptosis(Xiap); cyclin G1(Ccng1); chemokine(C-C motif) ligand 4(Ccl4); B cell translocation gene 2, anti-proliferative(Btg2); lysozyme 2(Lyz2); secreted phosphoprotein 1(Spp1); heme oxygenase(decycling) 1(Hmox1); CD14 antigen(Cd14); and granulin(Grn) may play important roles in NO-dependent responses in murine macrophages.

Keywords

References

  1. Albina JE, Cui S, Mateo RB, and Reichner JS (1993) Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol 150: 5080-5085
  2. An HJ, Maeng O, Kang KH, Lee JO, Kim YS, Paik SG, and Lee H (2006) Activation of Ras up-regulates pro-apoptotic BNIP3 in nitric oxide-induced cell death. J Biol Chem 281: 33939-33948 https://doi.org/10.1074/jbc.M605819200
  3. Balligand JL and Cannon PJ (1997) Nitric oxide synthases and cardiac muscle. Autocrine and paracrine influences. Arterioscler Thromb Vasc Biol 17: 1846-1858 https://doi.org/10.1161/01.ATV.17.10.1846
  4. Bogdan C (2001) Nitric oxide and the regulation of gene expression. Trends Cell Biol 11: 66-75 https://doi.org/10.1016/S0962-8924(00)01900-0
  5. Bogdan C, Rollinghoff M, and Diefenbach A (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12: 64-76 https://doi.org/10.1016/S0952-7915(99)00052-7
  6. Brockhaus F and Brüne B (1999) p53 accumulation in apoptotic macrophages is an energy demanding process that precedes cytochrome c release in response to nitric oxide. Oncogene 18: 6403-6410 https://doi.org/10.1038/sj.onc.1203058
  7. Chen X (2002) Cyclin G: a regulator of the p53-Mdm2 network. Dev Cell 2: 518-519 https://doi.org/10.1016/S1534-5807(02)00182-X
  8. Chen YC, Shen SC, Lee WR, Lin HY, Ko CH, and Lee TJ (2002) Nitric oxide and prostaglandin E2 participate in lipopolysaccharide/ interferon-gamma-induced heme oxygenase 1 and prevent RAW264.7 macrophages from UV-irradiationinduced cell death. J Cell Biochem 86: 331-339 https://doi.org/10.1002/jcb.10230
  9. Hemish J, Nakaya N, Mittal V, and Enikolopov G (2003) Nitric oxide activates diverse signaling pathways to regulate gene expression. J Biol Chem 278: 42321-42329 https://doi.org/10.1074/jbc.M308192200
  10. Kim YM, Lee BS, Yi KY, and Paik SG (1997a) Upstream $NF-{\kappa}B$ site is required for the maximal expression of mouse inducible nitric oxide synthase gene in $interferon-{\gamma}$ plus lipopolysaccharide- induced RAW 264.7 macrophages. Biochem Biophys Res Commun 236: 655-660 https://doi.org/10.1006/bbrc.1997.7031
  11. Kim YM, Talanian RV, and Billiar TR (1997b) Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem 272: 31138-31148 https://doi.org/10.1074/jbc.272.49.31138
  12. Kim SY, Kim JH, Lee HS, Noh SM, Song KS, Cho JS, Jeong HY, Kim WH, Yeom YI, Kim NS, Kim S, Yoo HS, and Kim YS (2007) Meta- and gene set analysis of stomach cancer gene expression data. Mol Cells 24: 200-209
  13. Li L, Zhang J, Block ER, and Patel JM (2004) Nitric oxidemodulated marker gene expression of signal transduction pathways in lung endothelial cells. Nitric Oxide 11: 290-297 https://doi.org/10.1016/j.niox.2004.10.007
  14. MacMicking JD, Nathan C, Hom G, Chartrain N, Fletcher DS, Trumbauer M, Stevens K, Xie QW, Sokol K, Hutchinson N, Chen H, and Mudget JS (1995) Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81: 641-650 https://doi.org/10.1016/0092-8674(95)90085-3
  15. MacMicking J, Xie QW, and Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15: 323-350 https://doi.org/10.1146/annurev.immunol.15.1.323
  16. Marshall HE, Merchant K, and Stamler JS (2000) Nitrosation and oxidation in the regulation of gene expression. FASEB J 14: 1889-1900 https://doi.org/10.1096/fj.00.011rev
  17. Messmer UK, Reimer DM, Reed JC, and Brüne B (1996) Nitric oxide induced poly (ADP- ribose) polymerase cleavage in RAW 264.7 macrophage apoptosis is blocked by Bcl-2. FEBS Letters 38: 162-166
  18. Toda N and Okamura T (1996) Neurogenic nitric oxide (NO) in the regulation of cerebroarterial tone. J Chem Neuroanat 10: 259-265 https://doi.org/10.1016/0891-0618(96)00135-4
  19. Turpaev K, Bouton C, Diet A, Glatigny A, and Drapier JC (2005) Analysis of differentially expressed genes in nitric oxideexposed human monocytic cells. Free Radic Biol Med 38: 1392-1400 https://doi.org/10.1016/j.freeradbiomed.2005.02.002
  20. Yook YH, Kang KH, Maeng O, Kim TR, Lee JO, Kang KI, Kim YS, Paik SG, and Lee H (2004) Nitric oxide induces BNIP3 expression that causes cell death in macrophages. Biochem Biophys Res Commun 321: 298-305 https://doi.org/10.1016/j.bbrc.2004.06.144
  21. Zamora R, Vodovotz Y, Aulak KS, Kim PKM, Kane JM III, Alarcon L, Stuehr DJ, and Billiar TR (2002) A DNA microarray study of nitric oxide-induced genes in mouse hepatocytes: implications for hepatic heme oxygenase-1 expression in ischemia/reperfusion. Nitric Oxide 7: 165-186 https://doi.org/10.1016/S1089-8603(02)00104-0
  22. Zhao Y, Brandish PE, Ballou DP, and Marletta MA (1999) A molecular basis for nitric oxide sensing by soluble guanylate cyclase. Proc Natl Acad Sci USA 96: 14753-14758