Dissection of a hypoxia-induced, nitric oxide-mediated signaling cascade

Molecular Biology of the Cell

Volumn 20, Issue 18, 2009, Pages 4083-4090

  Dijkers, Pascale F ^a   O'Farrell, Patrick H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; GREEN FLUORESCENT PROTEIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE; S NITROSOGLUTATHIONE; S NITROSOGLUTATHIONE REDUCTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELISH; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOLOGICAL MODEL; CALCIUM MOBILIZATION; CELL HYPOXIA; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; ENZYME ACTIVITY; INSECT CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM SIGNALING; CELL HYPOXIA; CELL LINE; CYCLIC GMP; DROSOPHILA MELANOGASTER; FREE RADICAL SCAVENGERS; ION CHANNEL GATING; ION CHANNELS; MITOCHONDRIA; MODELS, BIOLOGICAL; NITRIC OXIDE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-REL; S-NITROSOGLUTATHIONE; SIGNAL TRANSDUCTION;

EID: 70350231533     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-05-0362     Document Type: Article

References (50)

1. Armknecht, S., Boutros, M., Kiger, A., Nybakken, K., Mathey-Prevot, B., and Perrimon, N. (2005). High-throughput RNA interference screens in Drosophila tissue culture cells. Methods Enzymol. 392, 55-73.
2. Bryan, N. S., Rassaf, T., Maloney, R. E., Rodriguez, C. M., Saijo, F., Rodriguez, J. R., and Feelisch, M. (2004). Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo. Proc. Natl. Acad. Sci. USA 101, 4308-4313.
3. Castello, P. R., David, P. S., McClure, T., Crook, Z., and Poyton, R. O. (2006). Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 3, 277-287.
4. Clemens, J. C., Worby, C. A., Simonson-Leff, N., Muda, M., Maehama, T., Hemmings, B. A., and Dixon, J. E. (2000). Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. USA 97, 6499-6503.
5. Coburn, C. M., and Bargmann, C. I. (1996). A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695-706. (Pubitemid 26365348)
6. de Vente, J., Steinbusch, H. W., and Schipper, J. (1987). A new approach to immunocytochemistry of 3′,5′-cyclic guanosine monophosphate: preparation, specificity, and initial application of a new antiserum against formaldehyde-fixed 3′,5′-cyclic guanosine monophosphate. Neuroscience 22, 361-373.
7. Dijkers, P. F., and O'Farrell, P. H. (2007). Drosophila calcineurin promotes induction of innate immune responses. Curr. Biol. 17, 2087-2093.
8. Feelisch, M., Fernandez, B. O., Bryan, N. S., Garcia-Saura, M. F., Bauer, S., Whitlock, D. R., Ford, P. C., Janero, D. R., Rodriguez, J., and Ashrafian, H. (2008). Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and -scavenging systems. J. Biol. Chem. 283, 33927-33934.
9. Foe, V. E., and Alberts, B. M. (1985). Reversible chromosome condensation induced in Drosophila embryos by anoxia: visualization of interphase nuclear organization. J. Cell Biol. 100, 1623-1636.
10. Foley, E., and O'Farrell, P. H. (2003). Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev. 17, 115-125. (Pubitemid 36062513)
11. Foley, E., and O'Farrell, P. H. (2004). Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol. 2, E203. (Pubitemid 39245265)
12. Foster, M. W., McMahon, T. J., and Stamler, J. S. (2003). S-nitrosylation in health and disease. Trends Mol. Med. 9, 160-168.
13. Fulop, V., Moir, J. W., Ferguson, S. J., and Hajdu, J. (1995). The anatomy of a bifunctional enzyme: structural basis for reduction of oxygen to water and synthesis of nitric oxide by cytochrome cd1. Cell 81, 369-377.
14. Gray, J., Karow, D., Lu, H., Chang, A., Chang, J., Ellis, R., Marletta, M., and Bargmann, C. (2004). Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317-322.
15. Ignarro, L. J., Edwards, J. C., Gruetter, D. Y., Barry, B. K., and Gruetter, C. A. (1980). Possible involvement of S-nitrosothiols in the activation of guanylate cyclase by nitroso compounds. FEBS Lett. 110, 275-278.
16. Ignarro, L. J., Fukuto, J. M., Griscavage, J. M., Rogers, N. E., and Byrns, R. E. (1993). 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 90, 8103-8107.
17. Isbell, T., et al. (2008). SNO-hemoglobin is not essential for red blood cell- dependent hypoxic vasodilation. Nat. Med. 14, 773-777.
18. Jensen, D. E., Belka, G. K., and Du Bois, G. C. (1998). S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem. J. 331(Pt 2), 659-668.
19. Kim-Shapiro, D. B., Schechter, A. N., and Gladwin, M. (2006). Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler. Thromb. Vasc. Biol. 26, 697-705.
20. Kozlov, A. V., Staniek, K., and Nohl, H. (1999). Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett. 454, 127-130. (Pubitemid 29296938)
21. Krumenacker, J. S., Hanafy, K. A., and Murad, F. (2004). Regulation of nitric oxide and soluble guanylyl cyclase. Brain Res. Bull. 62, 505-515.
22. Lavista-Llanos, S., Centanin, L., Irisarri, M., Russo, D. M., Gleadle, J. M., Bocca, S. N., Muzzopappa, M., Ratcliffe, P. J., and Wappner, P. (2002). Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar. Mol. Cell. Biol. 22, 6842-6853.
23. Lee, S. J., Feldman, R., and O'Farrell, P. H. (2008). An RNA interference screen identifies a novel regulator of target of rapamycin that mediates hypoxia suppression of translation in Drosophila S2 cells. Mol. Biol. Cell 19, 4051-4061.
24. Leone, A. M., Palmer, R. M., Knowles, R. G., Francis, P. L., Ashton, D. S., and Moncada, S. (1991). Constitutive and inducible nitric oxide synthases incorporate molecular oxygen into both nitric oxide and citrulline. J. Biol. Chem. 266, 23790-23795.
25. Lima, B., et al. (2009). Endogenous S-nitrosothiols protect against myocardial injury. Proc. Natl. Acad. Sci. USA 106, 6297-6302.
26. Lipton, A. J., Johnson, M. A., Macdonald, T., Lieberman, M. W., Gozal, D., and Gaston, B. (2001). S-nitrosothiols signal the ventilatory response to hypoxia. Nature 413, 171-174. (Pubitemid 32867878)
27. Lipton, S. A. (2001). Physiology. Nitric oxide and respiration. Nature 413, 118-119, 121
28. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J., and Stamler, J. S. (2001). A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494. (Pubitemid 32240051)
29. Liu, L., et al. (2004). Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116, 617-628. (Pubitemid 38264436)
30. Lundberg, J., Weitzberg, E., and Gladwin, M. (2008). The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discov. 7, 156-167.
31. Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., and Blake, D. R. (1998). Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett. 427, 225-228. (Pubitemid 28225062)
32. Moncada, S., and Higgs, E. A. (2006). The discovery of nitric oxide and its role in vascular biology. Br. J. Pharmacol. 147(Suppl 1), S193-S201.
33. Morton, D. B. (2004). Atypical soluble guanylyl cyclases in Drosophila can function as molecular oxygen sensors. J. Biol. Chem. 279, 50651-50653.
34. Nakahara, K., Tanimoto, T., Hatano, K., Usuda, K., and Shoun, H. (1993). Cytochrome P-450 55A1 (P-450dNIR) acts as nitric oxide reductase employing NADH as the direct electron donor. J. Biol. Chem. 268, 8350-8355.
35. Nohl, H., Staniek, K., Sobhian, B., Bahrami, S., Redl, H., and Kozlov, A. V. (2000). Mitochondria recycle nitrite back to the bioregulator nitric monoxide. Acta Biochim. Pol. 47, 913-921.
36. Okamoto, N., Tsuruta, K., Imai, Y., Tomura, D., and Shoun, H. (1997). Fungal P450nor: expression in Escherichia coli and site-directed mutageneses at the putative distal region. Arch. Biochem. Biophys. 337, 338-344.
37. Palmer, L. A., Doctor, A., Chhabra, P., Sheram, M. L., Laubach, V. E., Karlinsey, M. Z., Forbes, M. S., Macdonald, T., and Gaston, B. (2007). S-nitrosothiols signal hypoxia-mimetic vascular pathology. J. Clin. Invest. 117, 2592-2601.
38. Postovit, L. M., Sullivan, R., Adams, M. A., and Graham, C. H. (2005). Nitric oxide signalling and cellular adaptations to changes in oxygenation. Toxicology 208, 235-248. (Pubitemid 40187334)
39. Rengasamy, A., and Johns, R. A. (1991). Characterization of endothelium-derived relaxing factor/nitric oxide synthase from bovine cerebellum and mechanism of modulation by high and low oxygen tensions. J. Pharmacol. Exp. Ther. 259, 310-316.
40. Sayed, N., Baskaran, P., Ma, X., van den Akker, F., and Beuve, A. (2007). Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Proc. Natl. Acad. Sci. USA 104, 12312-12317.
41. Segal, S. (2005). Regulation of blood flow in the microcirculation. UMIC 12, 33-45.
42. Stamler, J. S., Lamas, S., and Fang, F. C. (2001). Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106, 675-683. (Pubitemid 32900659)
43. Steffen, M., Sarkela, T. M., Gybina, A. A., Steele, T. W., Trasseth, N. J., Kuehl, D., and Giulivi, C. (2001). Metabolism of S-nitrosoglutathione in intact mitochondria. Biochem. J. 356, 395-402.
44. Teodoro, R. O., and O'Farrell, P. H. (2003). Nitric oxide-induced suspended animation promotes survival during hypoxia. EMBO J. 22, 580-587.
45. 2+]i in activation of eNOS in pressurized arterioles by agonists and wall shear stress. Am. J. Physiol. Heart Circ. Physiol. 281, H606-H612.
46. Vermehren, A., Langlais, K. K., and Morton, D. B. (2006). Oxygen-sensitive guanylyl cyclases in insects and their potential roles in oxygen detection and in feeding behaviors. J. Insect. Physiol. 52, 340-348.
47. Walters, C. L., and Taylor, A. M. (1965). The reduction of nitrite by skeletal-muscle mitochondria. Biochim. Biophys. Acta 96, 522-524.
48. Wingrove, J. A., and O'Farrell, P. H. (1999). Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98, 105-114.
49. Zhou, D., Xue, J., Lai, J. C., Schork, N. J., White, K. P., and Haddad, G. G. (2008). Mechanisms underlying hypoxia tolerance in Drosophila melanogaster: hairy as a metabolic switch. PLoS Genet. 4, e1000221.
50. Zweier, J. L., Wang, P., Samouilov, A., and Kuppusamy, P. (1995). Enzyme-independent formation of nitric oxide in biological tissues. Nat. Med. 1, 804-809.