Structure of the Mg-chelatase cofactor GUN4 reveals a novel hand-shaped fold for porphyrin binding

PLoS Biology

Volumn 3, Issue 5, 2005, Pages 0777-0789

  Verdecia, Mark A ^a,d   Larkin, Robert M ^b,e   Ferrer, Jean Luc ^c   Riek, Roland ^a   Chory, Joanne ^a   Noel, Joseph P ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d Stony Brook University   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; GUN4 PROTEIN; MAGNESIUM CHELATASE; PORPHYRIN; PROTEIN; PROTOPORPHYRIN; TETRAPYRROLE DERIVATIVE; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CHLOROPHYLL; GUN4 PROTEIN, ARABIDOPSIS; LYASE; RECOMBINANT PROTEIN; SIGNAL PEPTIDE;

ARTICLE; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SYNECHOCYSTIS; ARABIDOPSIS; BINDING SITE; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR CLONING; PROTEIN FOLDING; RESTRICTION MAPPING;

ARABIDOPSIS THALIANA; SYNECHOCYSTIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CHLOROPHYLL; CLONING, MOLECULAR; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYASES; PORPHYRINS; PROTEIN FOLDING; RECOMBINANT PROTEINS; RESTRICTION MAPPING;

EID: 21844476152     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0030151     Document Type: Article

References (58)

1. Butow RA, Avadhani NG (2004) Mitochondrial signaling: The retrograde response. Mol Cell 14: 1-15.
2. Zhang K, Kaufman RJ (2004) Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem 279: 25935-25938.
3. Rodermel S (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci 6: 471-478.
4. Richly E, Dietzmann A, Biehl A, Kurth J, Laloi C (2003) Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep 4: 491-498.
5. Rodermel S, Park S (2003) Pathways of intracellular communication: Tetrapyrroles and plastid-to-nucleus signaling. Bioessays 25: 631-636.
6. Strand Å , Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421: 79-83.
7. Johanningmeier U, Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. Possible involvement of chlorophyll synthesis precursors. J Biol Chem 259: 13541-13549.
8. Oster U, Brunner H, Rüdiger W (1996) The greening process in cress seedlings. V. Possible interference of chlorophyll precursors, accumulated after thujaplicin treatment, with light-regulated expression of Lhc genes. Photochem Photobiol 36: 255-261.
9. Kropat J, Oster U, Rüdiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heatshock genes. Proc Natl Acad Sci U S A 94: 14168-14172.
10. Kropat J, Oster U, Rüdiger W, Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24: 523-531.
11. La Rocca N, Rascio N, Oster U, Rüdiger W (2001) Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta 213: 101-108.
12. Chen JJ, London IM (1995) Regulation of protein synthesis by heme regulated eIF-2 alpha kinase. Trends Biochem Sci 20: 105-108.
13. Zhang L, Hach A (1999) Molecular mechanism of heme signaling in yeast: The transcriptional activator Hap1 serves as the key mediator. Cell Mol Life Sci 56: 415-426.
14. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C (2001) Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J 20: 2835-2843.
15. Qi Z, O'Brian M (2002) Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis. Mol Cell 9: 155-162.
16. Cornah JE, Roper JM, Pal Singh D, Smith AG (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.). Biochem J 362: 423-432.
17. Thomas J, Weinstein JD (1990) Measurement of heme efflux and heme content in isolated developing cotyledons. Plant Physiol 94: 1414-1423.
18. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci U S A 98: 20532058.
19. Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787-799.
20. Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902-906.
21. Willows RD (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep 20: 327-341.
22. Whyte BJ, Castelfranco PA (1993) Breakdown of thylakoid pigments by soluble proteins of developing chloroplasts. Biochem J 290: 361-367.
23. Wilde A, Mikolajczyk S, Alawady A, Lokstein H, Grimm B (2004) The GUN4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571:119-123.
24. D'Andrea LD, Regan L (2003) TPR proteins: The versatile helix. Trends Biochem Sci 12: 655-662.
25. Yaffe MB, Elia AE (2001) Phosphoserine/threonine-binding domains. Curr Opin Cell Biol 2: 131-138.
26. Schleiff E, Soll J (2000) Travelling of proteins through membranes: Translocation into chloroplasts. Planta 211: 449-456.
27. Holm L, Sander C (1998) Touring protein fold space with Dali/FSSP. Nucl Acids Res 26: 316-319.
28. Keller R, Groudinsky O, Wuthrich K (1976) Contact-shifter resonances in the 1H NMR spectra of cytochrome b5. Resonance identification and spin density distribution in the heme group. Biochim Biophy Acta 427: 497-511.
29. Karger GA, Reid JD, Hunter CN (2001) Characterization of the binding deuteroporphyrin IX to the magnesium chelatase H subunit and spectroscopic properties of the complex. Biochemistry 40: 9291-9299.
30. Lecerof D, Fodje M, Hansson A, Hansson M, Al-Karadaghi S. (2000) Structural and mechanistic basis of porphyrin metallation by ferrochelatase. J Mol Biol 297: 221-232.
31. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, et al. (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109-136
32. Willows RD, Lake V, Roberts TH, Beale SI (2003) Inactivation of Mg chelatase during transition from anaerobic to aerobic growth in Rhodobacter capsulatus. J Bacteriol 185: 3249-3258.
33. Sigfridsson J, Ryde U (2003) The importance of porphyrin distortions for the ferrochelatase reaction. Biol Inorg Chem 8: 273-282.
34. Hirsch JD, Beyer CF, Malkowitz L, Loullis CC, Blume AJ (1988) Characterization of ligand binding to mitochondrial benzodiazepine receptors. Mol Pharmacol 34: 164-172.
35. Kessel D (1988) Interactions between porphyrins and mitochondrial benzodiazepine receptors. Cancer Lett 39: 193-198.
36. Verma A, Snyder S (1988) Characterization of porphyrin interactions with peripheral type benzodiazepine receptors. Mol Pharmacol 34: 800-805.
37. Yeliseev AA, Kaplan S (1999) A novel mechanism for the regulation of photosynthesis gene expression by the TspO outer membrane protein Rhodobacter sphaeroides 2.4.1. J. Biol Chem 274: 21234-21243.
38. Papadopoulos V, Mukhin AG, Costa E, Krueger KE (1990) The peripheral-type benzodiazepine receptor is functionally linked to Leydig cell steroidogenesis. J Biol Chem 265: 3772-3779.
39. Anholt RR, De Souza EB, Oster-Granite ML, Snyder SH (1985) Peripheraltype benzodiazepine receptors: Autoradiographic localization in wholebody sections of neonatal rats. J Pharmacol Exp Ther 233: 517-526.
40. Anholt RR, Aebi U, Pedersen PL, Snyder SH (1986) Solubilization and reassembly of the mitochondrial benzodiazepine receptor. Biochemistry 22: 2120-2212.
41. Wendler G, Lindemann P, Lacapere JJ, Papadopoulos V (2003) Protoporphyrin IX binding and transport by recombinant mouse PBR. Biochem Biophys Res Commun 311: 847-852.
42. Zeng X, Kaplan S (2001) TspO as a modulator of the repressor/ antirepressor (PpsR/AppA) regulatory system in Rhodobacter sphaeroides 2.4.1. J Bacteriol 183: 6355-6364.
43. Yeliseev AA, Kaplan S (2000) TspO of rhodobacter sphaeroides. A structural and functional model for the mammalian peripheral benzodiazepine receptor. J Biol Chem 275: 5657-5667.
44. Jez, JM, Ferrer JL, Bowman ME, Dixon RA, Noel JP (2000) Dissection of malonyl-coenzyme A decarboxylation from polyketide formation in the reaction mechanism of a plant polyketide synthase. Biochemistry 5: 890-902.
45. Perrin MH, DiGuccio MR, Koerber SC, Rivier JE, Kunitake KS, et al. (2003) A soluble form of the first extracellular domain of mouse type 2beta corticotropin-releasing factor receptor reveals differential ligand specificity. J Biol Chem 278: 15595-15600.
46. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromol Crystallogr, Pt A. 276: 307-326.
47. Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55: 849-861.
48. Terwilliger TC (2000) Maximum likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972.
49. Terwilliger TC (2002) Automated main-chain model-building by template-matching and iterative fragment extension. Acta Crystallogr D Biol Crystallogr 59: 34-44.
50. Jones AT, Zou J-Y, Cowan S, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119.
51. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
52. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
53. Cavanagh J, Fairbrother WJ, Palme AG, Skelton NJ (1996) Protein NMR spectroscopy, principles and practice. Academic: New York. 587 p.
54. Jones G, Willet P, Glen RC, Leach AR, Taylor R (1997) Development and validation of a genetic algorithm for flexible docking. J Mol Biol 267: 727-748.
55. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF chimera - A visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
56. Jensen PE, Gibson LCD, Hunter CN (1998) Determinants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC6803. Biochem J 334:335-344.
57. Kraulis PJ (1991) MOLSCRIPT. A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946-950.
58. Nicholls A, Sharp KA, Honig B (1991) Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296.