Control of carotenoid biosynthesis through a heme-based cis-trans isomerase

Nature Chemical Biology

Volumn 11, Issue 8, 2015, Pages 598-605

  Beltrán, Jesús ^a,b   Kloss, Brian ^c   Hosler, Jonathan P ^d   Geng, Jiafeng ^e,g   Liu, Aimin ^e   Modi, Anuja ^f   Dawson, John H ^f   Sono, Masanori ^f   Shumskaya, Maria ^a   Ampomah Dwamena, Charles ^a,h   Love, James D ^c,i   Wurtzel, Eleanore T ^a,b  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^e GEORGIA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF SOUTH CAROLINA   (United States)

^g GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^h THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

ⁱ ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CAROTENOID; CIS TRANS ISOMERASE; HEME B COFACTOR; HEME DERIVATIVE; LIGAND; UNCLASSIFIED DRUG; 15-CIS-ZETA-CAROTENE ISOMERASE, ARABIDOPSIS; ARABIDOPSIS PROTEIN; HEME; IRON; ISOENZYME; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; VEGETABLE PROTEIN; ZETA CAROTENE;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ISOLATION; ENZYME LOCALIZATION; ENZYME STRUCTURE; HYDROPHOBICITY; ISOMERIZATION; MEMBRANE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ARABIDOPSIS; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; CHLOROPLAST; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; ISOMERISM; MAIZE; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; CIS-TRANS-ISOMERASES; ESCHERICHIA COLI; GENE EXPRESSION; HEME; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IRON; ISOENZYMES; ISOMERISM; MEMBRANE PROTEINS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PLANT PROTEINS; RECOMBINANT PROTEINS; ZEA MAYS; ZETA CAROTENE;

EID: 84937514111     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1840     Document Type: Article

References (57)

1. Moise, A.R., Al-Babili, S. & Wurtzel, E.T. Mechanistic aspects of carotenoid biosynthesis. Chem. Rev. 114, 164-193 (2014).
2. Wurtzel, E.T., Cuttriss, A. & Vallabhaneni, R. Maize provitamin A carotenoids, current resources and future metabolic engineering challenges. Front. Plant Sci. 3, 29 (2012).
3. Chen, Y., Li, F. & Wurtzel, E.T. Isolation and characterization of the Z-ISO gene encoding a missing component of carotenoid biosynthesis in plants. Plant Physiol. 153, 66-79 (2010).
4. Li, F., Murillo, C. & Wurtzel, E.T. Maize Y9 encodes a product essential for 15-cis zetacarotene isomerization. Plant Physiol. 144, 1181-1189 (2007).
5. Janick-Buckner, D., O'Neal, J., Joyce, E. & Buckner, B. Genetic and biochemical analysis of the y9 gene of maize, a carotenoid biosynthetic gene. Maydica 46, 41-46 (2001).
6. Tatusova, T.A. & Madden, T.L. Blast 2 sequences: a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174, 247-250 (1999).
7. Jones, D.T. Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23, 538-544 (2007).
8. Shumskaya, M. & Wurtzel, E.T. The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci. 208, 58-63 (2013).
9. Ginalski, K., Elofsson, A., Fischer, D. & Rychlewski, L. 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics 19, 1015-1018 (2003).
10. Madej, M.G., Nasiri, H.R., Hilgendorff, N.S., Schwalbe, H. & Lancaster, C.R.D. Evidence for transmembrane proton transfer in a dihaem-containing membrane protein complex. EMBO J. 25, 4963-4970 (2006).
11. Vallat, B.K. et al. Building and assessing atomic models of proteins from structural templates: learning and benchmarks. Proteins 76, 930-945 (2009).
12. Thomas, P.E., Ryan, D. & Levin, W. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 75, 168-176 (1976).
13. Nygaard, T.K., Liu, M., McClure, M.J. & Lei, B. Identification and characterization of the heme-binding proteins SeShp and SeHtsA of Streptococcus equi subspecies equi. BMC Microbiol. 6, 82 (2006).
14. Owens, C.P., Du, J., Dawson, J.H. & Goulding, C.W. Characterization of heme ligation properties of Rv0203, a secreted heme binding protein involved in Mycobacterium tuberculosis heme uptake. Biochemistry 51, 1518-1531 (2012).
15. Boffi, A., Chiancone, E., Takahashi, S. & Rousseau, D.L. Stereochemistry of the Fe(II)- and Fe(III)-cyanide complexes of the homodimeric Scapharca inaequivalvis hemoglobin: a resonance Raman and FTIR study. Biochemistry 36, 4505-4509 (1997).
16. Tsai, A.L. et al. Heme coordination of prostaglandin H synthase. J. Biol. Chem. 268, 8554-8563 (1993).
17. Geng, J., Dornevil, K. & Liu, A. Chemical rescue of the distal histidine mutants of tryptophan 2,3-dioxygenase. J. Am. Chem. Soc. 134, 12209-12218 (2012).
18. Zoppellaro, G. et al. Review: studies of ferric heme proteins with highly anisotropic/highly axial low spin (S = 1/2) electron paramagnetic resonance signals with bis-histidine and histidine-methionine axial iron coordination. Biopolymers 91, 1064-1082 (2009).
19. Zhong, F., Lisi, G.P., Collins, D.P., Dawson, J.H. & Pletneva, E.V. Redox-dependent stability, protonation, and reactivity of cysteine-bound heme proteins. Proc. Natl. Acad. Sci. USA 111, E306-E315 (2014).
20. Smith, A.T. et al. Identification of Cys94 as the distal ligand to the Fe(III) heme in the transcriptional regulator RcoM-2 from Burkholderia xenovorans. J. Biol. Inorg. Chem. 17, 1071-1082 (2012).
21. Enemark, J.H. & Feltham, R.D. Principles of structure, bonding, and reactivity for metal nitrosyl complexes. Coord. Chem. Rev. 13, 339-406 (1974).
22. Yonetani, T., Yamamoto, H., Erman, J.E., Leigh, J.S. Jr. & Reed, G.H. 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 (1972).
23. Sun, J., Wilks, A., Ortiz de Montellano, P.R. & Loehr, T.M. Resonance Raman and EPR spectroscopic studies on heme-heme oxygenase complexes. Biochemistry 32, 14151-14157 (1993).
24. Vickery, L., Nozawa, T. & Sauer, K. Magnetic circular dichroism studies of low-spin cytochromes: temperature dependence and effects of axial coordination on the spectra of cytochrome c and cytochrome b5. J. Am. Chem. Soc. 98, 351-357 (1976).
25. Vickery, L., Nozawa, T. & Sauer, K. Magnetic circular dichroism studies of myoglobin complexes: correlations with heme spin state and axial ligation. J. Am. Chem. Soc. 98, 343-350 (1976).
26. Sono, M., Dawson, J.H., Hall, K. & Hager, L.P. Ligand and halide binding properties of chloroperoxidase: peroxidase-type active site heme environment with cytochrome P-450 type endogenous axial ligand and spectroscopic properties. Biochemistry 25, 347-356 (1986).
27. Dawson, J.H., Andersson, L.A. & Sono, M. 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 (1982).
28. Li, T., Bonkovsky, H.L. & Guo, J.T. Structural analysis of heme proteins: implications for design and prediction. BMC Struct. Biol. 11, 13 (2011).
29. Wouters, J. et al. Catalytic mechanism of Escherichia coli isopentenyl diphosphate isomerase involves Cys-67, Glu-116, and Tyr-104 as suggested by crystal structures of complexes with transition state analogues and irreversible inhibitors. J. Biol. Chem. 278, 11903-11908 (2003).
30. D'Angelo, P. et al. Unusual heme iron-lipid acyl chain coordination in Escherichia coli flavohemoglobin. Biophys. J. 86, 3882-3892 (2004).
31. Crabtree, R.H. in The Organometallic Chemistry of the Transition Metals 125-158 (John Wiley & Sons, 2005).
32. Pearson, R.G. Hard and soft acids and bases, HSAB, part II: underlying theories. J. Chem. Educ. 45, 643 (1968).
33. Heipieper, H.J., Neumann, G., Kabelitz, N., Kastner, M. & Richnow, H.H. Carbon isotope fractionation during cis-trans isomerization of unsaturated fatty acids in Pseudomonas putida. Appl. Microbiol. Biotechnol. 66, 285-290 (2004).
34. Williams, P.A. et al. Haem-ligand switching during catalysis in crystals of a nitrogen-cycle enzyme. Nature 389, 406-412 (1997).
35. Geng, J., Davis, I., Liu, F. & Liu, A. Bis-Fe(IV): nature's sniper for long-range oxidation. J. Biol. Inorg. Chem. 19, 1057-1067 (2014).
36. Richter, A.S. & Grimm, B. Thiol-based redox control of enzymes involved in the tetrapyrrole biosynthesis pathway. Front. Plant Sci. 4, 371 (2013).
37. Fanciullino, A.L., Bidel, L.P.R. & Urban, L. Carotenoid responses to environmental stimuli: integrating redox and carbon controls into a fruit model. Plant Cell Environ. 37, 273-289 (2014).
38. Davison, P.A. Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418, 203-206 (2002).
39. Johnson, M.P. et al. Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J. Biol. Chem. 282, 22605-22618 (2007).
40. Walter, M.H., Floss, D.S. & Strack, D. Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232, 1-17 (2010).
41. Li, F., Vallabhaneni, R. & Wurtzel, E.T. PSY3, a new member of the phytoene synthase gene family conserved in the Poaceae and regulator of abiotic-stress-induced root carotenogenesis. Plant Physiol. 146, 1333-1345 (2008).
42. Gas, E., Flores-Perez, U., Sauret-Gueto, S. & Rodriguez-Concepcion, M. Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21, 18-23 (2009).
43. Chang, H.-L., Hsu, Y.-T., Kang, C.-Y. & Lee, T.-M. Nitric oxide down-regulation of carotenoid synthesis and PSII activity in relation to very high light-induced singlet oxygen production and oxidative stress in Chlamydomonas reinhardtii. Plant Cell Physiol. 54, 1296-1315 (2013).
44. Khatsenko, O. Interactions between nitric oxide and cytochrome P-450 in the liver. Biochemistry (Mosc) 63, 833-839 (1998).
45. Cooper, C.E. Nitric oxide and iron proteins. Biochim. Biophys. Acta 1411, 290-309 (1999).
46. Munro, A., Girvan, H., McLean, K., Cheesman, M. & Leys, D. in Tetrapyrroles, Birth, Life and Death (eds. Warren, M. & Smith, A.) 160-183 (Landes Bioscience, Austin, Texas, USA, 2009).
47. Doyle, S.A. High-throughput cloning for proteomics research. Methods Mol. Biol. 310, 107-113 (2005).
48. Donnelly, M.I. et al. An expression vector tailored for large-scale, high-throughput purification of recombinant proteins. Protein Expr. Purif. 47, 446-454 (2006).
49. Seiler, C.Y. et al. DNASU plasmid and PSI:Biology-Materials repositories: resources to accelerate biological research. Nucleic Acids Res. 42, D1253-D1260 (2014).
50. Britton, G., Liaaen-Jensen, S. & Pfander, H. in Carotenoids: Spectroscopy Vol.1B (eds. Britton, G., Liaaen-Jensen, S. & Pfander, H.) 13-62 (Birkhäuser, Basel, 1995).
51. Ter Horst, R. & Lolkema, J.S. Rapid screening of membrane topology of secondary transport proteins. Biochim Biophys Acta 1798, 672-680 (2010).
52. Shumskaya, M., Bradbury, L.M.T., Monaco, R.R. & Wurtzel, E.T. Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. Plant Cell 24, 3725-3741 (2012).
53. Quinlan, R.F. et al. Synergistic interactions between carotene ring hydroxylases drive lutein formation in plant carotenoid biosynthesis. Plant Physiol. 160, 204-214 (2012).
54. Varanasi, L. & Hosler, J.P. Subunit III-depleted cytochrome c oxidase provides insight into the process of proton uptake by proteins. Biochim. Biophys. Acta 1817, 545-551 (2012).
55. Berry, E.A. & Trumpower, B.L. Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal. Biochem. 161, 1-15 (1987).
56. Thomas, P.E., Ryan, D. & Levin, W. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 75, 168-176 (1976).
57. Pond, A.E., Roach, M.P., Thomas, M.R., Boxer, S.G. & Dawson, J.H. The H93G myoglobin cavity mutant as a versatile template for modeling heme proteins: ferrous, ferric, and ferryl mixed-ligand complexes with imidazole in the cavity. Inorg. Chem. 39, 6061-6066 (2000).