DHR51, the Drosophila melanogaster homologue of the human photoreceptor cell-specific nuclear receptor, is a thiolate heme-binding protein

Biochemistry

Volumn 47, Issue 50, 2008, Pages 13252-13260

  De Rosny, Eve ^a,b   De Groot, Arjan ^a,c   Jullian Binard, Celine ^a   Borel, Franck ^a   Suarez, Cristian ^a   Le Pape, Laurent ^a   Fontecilla Camps, Juan C ^a   Jouve, Hélène M ^a  

^a CEA GRENOBLE   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c IRFM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION SPECTROSCOPY; BENCHMARKING; CLONING; DISSOCIATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; GAS ABSORPTION; GENETIC ENGINEERING; LIGANDS; PORPHYRINS; TRANSCRIPTION FACTORS; VOLUMETRIC ANALYSIS;

AXIAL LIGANDS; BINDING ABILITIES; BINDING DOMAINS; BINDING PROTEINS; DISSOCIATION CONSTANTS; DROSOPHILA MELANOGASTER; FERRIC IRONS; ISOTHERMAL TITRATION CALORIMETRIES; NUCLEAR RECEPTORS; PHOTORECEPTOR CELLS; THIOLATE; VISIBLE ABSORPTION SPECTROSCOPIES; VISIBLE SPECTRUMS;

HEMOGLOBIN;

BINDING PROTEIN; CARBON MONOXIDE; CELL NUCLEUS RECEPTOR; CYSTEINE; DHR3 PROTEIN; DHR39 PROTEIN; DHR4 PROTEIN; DHR5 PROTEIN; DHR51 PROTEIN; DHR78 PROTEIN; DHR83 PROTEIN; E78 PROTEIN; ESTROGEN RECEPTOR RELATED RECEPTOR; FERRIC ION; FUSHI TARAZU PROTEIN; HEME; HEPATOCYTE NUCLEAR FACTOR 4; HISTIDINE; NITRIC OXIDE; TAILLESS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CLONING; DISSOCIATION CONSTANT; DROSOPHILA MELANOGASTER; GAS; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SCREENING; ULTRAVIOLET SPECTROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEMEPROTEINS; HUMANS; LIGANDS; MOLECULAR SEQUENCE DATA; PDZ DOMAINS; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEIN BINDING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN; SULFHYDRYL COMPOUNDS;

DROSOPHILA MELANOGASTER; ESCHERICHIA COLI;

EID: 57649136746     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801691b     Document Type: Article

References (49)

1. Francis, G. A., Fayard, E., Picard, F., and Auwerx, J. (2003) Nuclear receptors and the control of metabolism. Annu. Rev. Physiol. 65, 261-311.
2. Bain, D. L., Heneghan, A. F., Connaghan-Jones, K. D., and Miura, M. T. (2007) Nuclear receptor structure: implications for function. Annu. Rev. Physiol. 69, 201-220.
3. Renaud, J. P., and Moras, D. (2000) Structural studies on nuclear receptors. Cell. Mol. Life Sci. 57, 1748-1769.
4. King-Jones, K., and Thummel, C. S. (2005) Nuclear receptors-a perspective from Drosophila. Nat. Rev. Genet. 6, 311-323.
5. Clayton, G. M., Peak-Chew, S. Y., Evans, R. M., and Schwabe, J. W. (2001) The structure of the ultraspiracle ligand-binding domain reveals a nuclear receptor locked in an inactive conformation. Proc. Natl. Acad. Sci. U.S.A. 98, 1549-1554.
6. Baker, K. D., Shewchuk, L. M., Kozlova, T., Makishima, M., Hassell, A., Wisely, B., Caravella, J. A., Lambert, M. H., Retaking, J. L., Krause, H., Thummel, C. S., Willson, T. M., and Mangelsdorf, D. J. (2003) The Drosophila orphan nuclear receptor DHR38 mediates an atypical ecdysteroid signaling pathway. Cell 113, 731-742.
7. Billas, I. M., Iwema, T., Garnier, J. M., Mitschler, A., Rochel, N., and Moras, D. (2003) Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature 426, 91-96.
8. Reinking, J., Lam, M. M., Pardee, K., Sampson, H. M., Liu, S., Yang, P., Williams, S., White, W., Lajoie, G., Edwards, A., and Krause, H. M. (2005) The Drosophila nuclear receptor e75 contains heme and is gas responsive. Cell 122, 195-207.
9. de Rosny, E., de Groot, A., Jullian-Binard, C., Gaillard, J., Borel, F., Pebay-Peyroula, E., Fontecilla-Camps, J. C., and Jouve, H. M. (2006) Drosophila nuclear receptor E75 is a thiolate hemoprotein. Biochemistry 45, 9727-9734.
10. White, K. P., Hurban, P., Watanabe, T., and Hogness, D. S. (1997) Coordination of Drosophila metamorphosis by two ecdysone-induced nuclear receptors. Science 276, 114-117.
11. Raghuram, S., Stayrook, K. R., Huang, P., Rogers, P. M., Nosie, A. K., McClure, D. B., Burris, L. L., Khorasanizadeh, S., Burris, T. P., and Rastinejad, F. (2007) Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat Struct Mol Biol 14, 1207-1213.
12. Yin, L., Wu, N., Curtin, J. C., Qatanani, M., Szwergold, N. R., Reid, R. A., Waitt, G. M., Parks, D. J., Pearce, K. H., Wisely, G. B., and Lazar, M. A. (2007) Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 318, 1786-1789.
13. Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F., George, R. A., Lewis, S. E., Richards, S., Ashburner, M., Henderson, S. N., Sutton, G. G., Wortman, J. R., Yandell, M. D., Zhang, Q., Chen, L. X., Brandon, R. C., Rogers, Y. H., Blazej, R. G., Champe, M., Pfeiffer, B. D., Wan, K. H., Doyle, C., Baxter, E. G., Helt, G., Nelson, C. R., Gabor, G. L., Abril, J. F., Agbayani, A., An, H. J., Andrews-Pfannkoch, C., Baldwin, D., Ballew, R. M., Basu, A., Baxendale, J., Bayraktaroglu, L., Beasley, E. M., Beeson, K. Y., Benos, P. V., Berman, B. P., Bhandari, D., Bolshakov, S., Borkova, D., Botchan, M. R., Bouck, J., Brokstein, P., Brottier, P., Burtis, K. C., Busam, D. A., Butler, H., Cadieu, E., Center, A., Chandra, I., Cherry, J. M., Cawley, S., Dahlke, C., Davenport, L. B., Davies, P., de Pablos, B., Deicher, A., Deng, Z., Mays, A. D., Dew, I., Dietz, S. M., Dodson, K., Doup, L. E., Downes, M., Dugan-Rocha, S., Dunkov, B. C., Dunn, P., Durbin, K. J., Evangelista, C. C., Ferraz, C., Ferriera, S., Fleischmann, W., Fosler, C., Gabrielian, A. E., Garg, N. S., Gelbart, W. M., Glasser, K., Glodek, A., Gong, F., Gorrell, J. H., Gu, Z., Guan, P., Harris, M., Harris, N. L., Harvey, D., Heiman, T. J., Hernandez, J. R., Houck, J., Hostin, D., Houston, K. A., Howland, T. J., Wei, M. H., Ibegwam, C., et al. (2000) The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
14. Milam, A. H., Rose, L., Cideciyan, A. V., Barakat, M. R., Tang, W. X., Gupta, N., Aleman, T. S., Wright, A. F., Stone, E. M., Sheffield, V. C., and Jacobson, S. G. (2002) The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration. Proc. Natl. Acad. Sci. U.S.A. 99, 473-8.
15. de Groot, A., de Rosny, E., Juillan-Binard, C., Ferrer, J. L., Laudet, V., Pierce, R. J., Pebay-Peyroula, E., Fontecilla-Camps, J. C., and Borel, F. (2005) Crystal structure of a novel tetrameric complex of agonist-bound ligand-binding domain of Biomphalaria glabrata retinoid X receptor. J. Mol. Biol. 354, 841-853.
16. Beaven, G. H., Chen, S. H., d'Albis, A., and Gratzer, W. B. (1974) A spectroscopic study of the haemin-human-serum-albumin system. Eur. J. Biochem. 41, 539-546.
17. Deniau, C., Gilli, R., Izadi-Pruneyre, N., Letoffe, S., Delepierre, M., Wandersman, C., Briand, C., and Lecroisey, A. (2003) Thermodynamics of heme binding to the HasA(SM) hemophore: effect of mutations at three key residues for heme uptake. Biochemistry 42, 10627-10633.
18. Izadi, N., Henry, Y., Haladjian, J., Goldberg, M. E., Wandersman, C., Delepierre, M., and Lecroisey, A. (1997) Purification and characterization of an extracellular heme-binding protein, HasA, involved in heme iron acquisition. Biochemistry 36, 7050-7057.
19. Gouet, P., Jouve, H. M., and Dideberg, O. (1995) Crystal structure of Proteus mirabilis PR catalase with and without bound NADPH. J. Mol. Biol. 249, 933-954.
20. Cheesman, M. R., Little, P. J., and Berks, B. C. (2001) Novel heme ligation in a c-type cytochrome involved in thiosulfate oxidation: EPR and MCD of SoxAX from Rhodovulum sulfidophilum. Biochemistry 40, 10562-10569.
21. Dawson, J. H., Andersson, L. A., and Sono, M. (1982) Spectroscopic investigations of ferric cytochrome P-450-CAM ligand complexes. Identification of the ligand trans to cysteinate in the native enzyme. J. Biol. Chem. 257, 3606-3617.
22. Dhawan, I. K., Shelver, D., Thorsteinsson, M. V., Roberts, G. P., and Johnson, M. K. (1999) Probing the heme axial ligation in the CO-sensing CooA protein with magnetic circular dichroism spectroscopy. Biochemistry 38, 12805-12813.
23. Sigman, J. A., Pond, A. E., Dawson, J. H., and Lu, Y. (1999) Engineering cytochrome c peroxidase into cytochrome P450: a proximal effect on heme-thiolate ligation. Biochemistry 38, 11122-11129.
24. Konopka, K., and Waskell, L. (1988) Chemical modification of cytochrome b5, cytochrome c and myoglobin with diethylpyrocarbonate. Biochim. Biophys. Acta 954, 189-200.
25. Nakanishi, N., Takeuchi, F., Okamoto, H., Tamura, A., Hori, H., and Tsubaki, M. (2006) Characterization of heme-coordinating histidyl residues of cytochrome b5 based on the reactivity with diethylpyrocarbonate: a mechanism for the opening of axial imidazole rings. J. Biochem. 140, 561-71.
26. Miles, E. W. (1977) Modification of histidyl residues in proteins by diethylpyrocarbonate. Methods Enzymol. 47, 431-442.
27. Marvin, K. A., Kerby, R. L., Youn, H., Roberts, G. P., and Burstyn, J. N. (2008) The transcription regulator RcoM-2 from Burkholderia xenovorans is a cysteine-ligated hemoprotein that undergoes a redox-mediated ligand switch. Biochemistry 47, 9016-9028.
28. Pazicni, S., Lukat-Rodgers, G. S., Oliveriusova, J., Rees, K. A., Parks, R. B., Clark, R. W., Rodgers, K. R., Kraus, J. P., and Burstyn, J. N. (2004) The redox behavior of the heme in cystathionine beta-synthase is sensitive to pH. Biochemistry 43, 14684-14695.
29. Yoshioka, S., Takahashi, S., Hori, H., Ishimori, K., and Morishima, I. (2001) Proximal cysteine residue is essential for the enzymatic activities of cytochrome P450cam. Eur. J. Biochem. 268, 252-259.
30. Aono, S., Ohkubo, K., Matsuo, T., and Nakajima, H. (1998) Redox-controlled ligand exchange of the heme in the CO-sensing transcriptional activator CooA. J. Biol. Chem. 273, 25757-25764.
31. Igarashi, J., Sato, A., Kitagawa, T., Yoshimura, T., Yamauchi, S., Sagami, I., and Shimizu, T. (2004) Activation of heme-regulated eukaryotic initiation factor 2alpha kinase by nitric oxide is induced by the formation of a five-coordinate NO-heme complex: optical absorption, electron spin resonance, and resonance raman spectral studies. J. Biol. Chem. 279, 15752-15762.
32. Uchida, T., Sato, E., Sato, A., Sagami, I., Shimizu, T., and Kitagawa, T. (2005) CO-dependent activity-controlling mechanism of heme-containing CO-sensor protein, neuronal PAS domain protein 2. J. Biol. Chem. 280, 21358-21368.
33. Perera, R., Sono, M., Sigman, J. A., Pfister, T. D., Lu, Y., and Dawson, J. H. (2003) Neutral thiol as a proximal ligand to ferrous heme iron: implications for heme proteins that lose cysteine thiolate ligation on reduction. Proc. Natl. Acad. Sci. U.S.A. 100, 3641-3646.
34. Reynolds, M. F., Parks, R. B., Burstyn, J. N., Shelver, D., Thorsteinsson, M. V., Kerby, R. L., Roberts, G. P., Vogel, K. M., and Spiro, T. G. (2000) Electronic absorption, EPR, and resonance raman spectroscopy of CooA, a CO-sensing transcription activator from R. rubrum, reveals a five-coordinate NO-heme. Biochemistry 39, 388-396.
35. Yonetani, T., Yamamoto, H., Erman, J. E., Leigh, J. S., Jr., and Reed, G. H. (1972) Electromagnetic properties of hemoproteins. V. Optical and electron paramagnetic resonance characteristics of nitric oxide derivatives of metalloporphyrin-apohemoprotein complexes. J. Biol. Chem. 247, 2447-2455.
36. Derbyshire, E. R., Gunn, A., Ibrahim, M., Spiro, T. G., Britt, R. D., and Marietta, M. A. (2008) Characterization of two different five-coordinate soluble guanylate cyclase ferrous-nitrosyl complexes. Biochemistry 47, 3892-3899.
37. Mense, S. M., and Zhang, L. (2006) Heme: a versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res. 16, 681-692.
38. Shelver, D., Kerby, R. L., He, Y., and Roberts, G. P. (1997) CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein. Proc. Natl. Acad. Sci. U.S.A. 94, 11216-11220.
39. Palanker, L., Necakov, A. S., Sampson, H. M., Ni, R., Hu, C., Thummel, C. S., and Krause, H. M. (2006) Dynamic regulation of Drosophila nuclear receptor activity in vivo. Development 133, 3549-3562.
40. Krey, G., Braissant, O., L'Horset, F., Kalkhoven, E., Perroud, M., Parker, M. G., and Wahli, W. (1997) Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol. Endocrinol. 11, 779-791.
41. Janowski, B. A., Grogan, M. J., Jones, S. A., Wisely, G. B., Kliewer, S. A., Corey, E. J., and Mangelsdorf, D. J. (1999) Structural requirements of ligands for the oxysterol liver X receptors LXRalpha and LXRbeta. Proc. Natl. Acad. Sci. U.S.A. 96, 266-271.
42. Igarashi, J., Kitanishi, K., Martinkova, M., Murase, M., Iizuka, A., and Shimizu, T. (2008) The Roles of thiolate-heme proteins, outer than the P450 cytochromes in the regulation of heme-sensor proteins. Acta Chim. Slov. 67-74.
43. Igarashi, J., Murase, M., Iizuka, A., Pichierri, F., Martinkova, M., and Shimizu, T. (2008) Elucidation of the heme binding site of heme-regulated eukaryotic initiation factor 2alpha kinase and the role of the regulatory motif in heme sensing by spectroscopic and catalytic studies of mutant proteins. J. Biol. Chem. 283, 18782-18791.
44. Ogawa, K., Igarashi, K., Nishitani, C., Shibahara, S., and Fujita, H. (2002) Heme-regulated transcription factor Bachl. J. Health Sci. 48, 1-6.
45. Miksanova, M., Igarashi, J., Minami, M., Sagami, I., Yamauchi, S., Kurokawa, H., and Shimizu, T. (2006) Characterization of heme-regulated eIF2alpha kinase: roles of the N-terminal domain in the oligomeric state, heme binding, catalysis, and inhibition. Biochemistry 45, 9894-9905.
46. Mukaiyama, Y., Uchida, T., Sato, E., Sasaki, A., Sato, Y., Igarashi, J., Kurokawa, H., Sagami, I., Kitagawa, T., and Shimizu, T. (2006) Spectroscopic and DNA-binding characterization of the isolated heme-bound basic helix-loop-helix-PAS-A domain of neuronal PAS protein 2 (NPAS2), a transcription activator protein associated with circadian rhythms. FEBS J. 273, 2528-2539.
47. Wightman, B., Ebert, B., Carmean, N., Weber, K., and Clever, S. (2005) The C. elegans nuclear receptor gene fax-1 and homeobox gene unc-42 coordinate interneuron identity by regulating the expression of glutamate receptor subunits and other neuron-specific genes. Dev. Biol. 287, 74-85.
48. Sengupta, A., Hon, T., and Zhang, L. (2005) Heme deficiency suppresses the expression of key neuronal genes and causes neuronal cell death. Brain Res. Mol. Brain Res. 137, 23-30.
49. Brelivet, Y., Kammerer, S., Rochel, N., Poch, O., and Moras, D. (2004) Signature of the oligomeric behaviour of nuclear receptors at the sequence and structural level. EMBO Rep. 5, 423-429.