Cellular and Molecular Life Sciences

, Volume 67, Issue 3, pp 387–404 | Cite as

Firefly luciferase: an adenylate-forming enzyme for multicatalytic functions

Review

Abstract

Firefly luciferase is a member of the acyl-adenylate/thioester-forming superfamily of enzymes and catalyzes the oxidation of firefly luciferin with molecular oxygen to emit light. Knowledge of the luminescence mechanism catalyzed by firefly luciferase has been gathered, leading to the discovery of a novel catalytic function of luciferase. Recently, we demonstrated that firefly luciferase has a catalytic function of fatty acyl-CoA synthesis from fatty acids in the presence of ATP, Mg2+ and coenzyme A. Based on identification of fatty acyl-CoA genes in firefly, Drosophila, and non-luminous click beetles, we then proposed that the evolutionary origin of firefly luciferase is a fatty acyl-CoA synthetase in insects. Further, we succeeded in converting the fatty acyl-CoA synthetase of non-luminous insects into functional luciferase showing luminescence activity by site-directed mutagenesis.

Keywords

Bioluminescence Luciferin analogue Inhibitors Fatty acyl-CoA synthetase Molecular evolution 

Notes

Acknowledgment

The author is grateful to Dr. A. Nakagawa (Osaka University, Japan) for illustrating the X-ray structure model of firefly luciferase. Also, the author thanks Dr. T. Hosoya (Tokyo Medical and Dental University, Japan) for discussion about luminescence mechanisms.

References

  1. 1.
    Harvey EN (1952) Bioluminescence. Academic, New YorkGoogle Scholar
  2. 2.
    Haneda Y, Johnson FH (eds) (1966) Bioluminescence in progress. Princeton University Press, New JerseyGoogle Scholar
  3. 3.
    Herring PJ (ed) (1978) Bioluminescence in action. Academic, New YorkGoogle Scholar
  4. 4.
    Campbell AK (1988) Chemiluminescence: principle and applications in biology and medicine. VCH, New YorkGoogle Scholar
  5. 5.
    Shimomura O (2006) Bioluminescence: chemical principles and methods. World Scientific, SingaporeGoogle Scholar
  6. 6.
    Shimomura O (1985) Bioluminescence in the sea: photoprotein systems. Soc Exp Biol Symp 39:351–372Google Scholar
  7. 7.
    Hastings JW, Morin JG (1991) Bioluminescence. In: Prosser CL (ed) Neural and integrative animal physiology. Wiley, New York, pp 131–170Google Scholar
  8. 8.
    Meighen EA, Dunlap PV (1993) Physiological, biochemical and genetic control of bacterial bioluminescence. Adv Microbial Physiol 34:1–67Google Scholar
  9. 9.
    Wilson T, Hastings JW (1998) Bioluminescence. Annu Rev Cell Dev Biol 14:197–230PubMedGoogle Scholar
  10. 10.
    Bronstein I, Fortin J, Stanley PE, Stewart GSAB, Kricka LJ (1994) Chemiluminescent and bioluminescent reporter gene assays. Anal Biochem 219:169–181PubMedGoogle Scholar
  11. 11.
    Greer LF III, Szalay AA (2002) Imaging of light emission from the expression of luciferases in living cells and organisms: a review. Luminescence 17:43–73PubMedGoogle Scholar
  12. 12.
    Lloyd JE (1983) Bioluminescence and communication in insects. Annu Rev Entomol 28:131–160Google Scholar
  13. 13.
    Wood KV (1995) The chemical mechanism and evolutionary development of beetle bioluminescence. Photochem Photobiol 62:662–673Google Scholar
  14. 14.
    Viviani VR (2002) The origin, diversity, and structure function relationships of insect luciferases. Cell Mol Life Sci 59:1833–1850PubMedGoogle Scholar
  15. 15.
    Nakamura M, Niwa K, Maki S, Hirano T, Ohmiya Y, Niwa H (2006) Conversion of a new firefly bioluminescence system using l-luciferin as substrate. Tetrahedron Lett 47:1197–1200Google Scholar
  16. 16.
    McElroy WD, DeLuca M, Travis J (1967) Molecular uniformity in biological catalyses. Science 157:150–160PubMedGoogle Scholar
  17. 17.
    Oba Y, Ojika M, Inouye S (2003) Firefly luciferase is a bifunctional enzyme: ATP-dependent monooxygenase and a long chain fatty acyl-CoA synthetase. FEBS Lett 540:251–254PubMedGoogle Scholar
  18. 18.
    Bitler B, McElroy WD (1957) The preparation and properties of crystalline firefly luciferin. Arch Biochem Biophys 72:358–368PubMedGoogle Scholar
  19. 19.
    Kishi Y, Matsuura S, Inoue S, Shimomura O, Goto T (1968) Luciferin and luciopterin isolated from the Japanese firefly, Luciola cruciata. Tetrahedron Lett 9:2847–2850Google Scholar
  20. 20.
    White EH, McCapra F, Field GF, McElroy WD (1961) The structure and synthesis of firefly luciferin. J Am Chem Soc 83:2402–2403Google Scholar
  21. 21.
    White EH, McCapra F, Field GF (1963) The structure and synthesis of firefly luciferin. J Am Chem Soc 85:337–343Google Scholar
  22. 22.
    Blank GE, Pletcher J, Sax M (1971) The molecular structure of firefly d-(−)-luciferin: a single crystal analysis. Biochem Biophys Res Commun 42:583–588PubMedGoogle Scholar
  23. 23.
    Branchini BR, Magyar RA, Murtiashaw MH, Porieer NC (2001) The role of active site residue arginine 218 in firefly luciferase. Biochemistry 40:2410–2418PubMedGoogle Scholar
  24. 24.
    Oba Y, Shintani T, Nakamura T, Ojika M, Inouye S (2008) Determination of the luciferin contents in luminous and non-luminous beetles. Biochem Biosci Biotechnol 272:384–1387Google Scholar
  25. 25.
    Seliger HH, McElroy WD, White EH, Field GF (1961) Stereospecificity and firefly bioluminescence, a comparison of natural and synthetic luciferins. Proc Natl Acad Sci USA 47:1129–1961PubMedGoogle Scholar
  26. 26.
    Lembert N (1996) Firefly luciferase can use l-luciferin to produce light. Biochem J 317:273–277PubMedGoogle Scholar
  27. 27.
    Niwa K, Nakamura M, Ohmiya Y (2006) Stereoisomeric bio-inversion key to biosynthesis of firefly d-luciferin. FEBS Lett 580:5283–5287PubMedGoogle Scholar
  28. 28.
    Rhodes WC, McElroy WD (1958) The synthesis and function of luciferyl-adenylate and oxyluciferyl-adenylate. J Biol Chem 233:1528–1537PubMedGoogle Scholar
  29. 29.
    Seliger HH, McElroy WD (1962) Chemiluminescence of firefly luciferin without enzyme. Science 138:683–685PubMedGoogle Scholar
  30. 30.
    Suzuki N, Sato M, Nishikawa K, Goto T (1969) Synthesis and spectral properties of 2-(6′-hydroxybenzothiazol-2′-yl)-4-hydroxytiazole, a possible emitting species in the firefly bioluminescence. Tetrahedron Lett 53:4683–4684Google Scholar
  31. 31.
    Suzuki N, Goto T (1971) Firefly bioluminescence II. Identification of 2-(6′-hydroxybenzothiazol-2′-yl)-4-hydroxythiazole as a product in the bioluminescence of firefly lanterns and a product in the chemiluminescence of firefly luciferin in DMSO. Tetrahedron Lett 22:2021–2024Google Scholar
  32. 32.
    Suzuki N, Goto T (1972) Synthesis of 4-thiazolone derivatives related to firefly luciferin. Agric Biol Chem 36:2213–2221Google Scholar
  33. 33.
    Hopkins TA, Seliger HH, White EH, Cass MW (1969) The chemiluminescence of firefly luciferin. A model for the bioluminescent reaction and identification if the product excited state. J Am Chem Soc 89:7148–7150Google Scholar
  34. 34.
    Esteves da Silva JCG, Magalhaes JMCS, Fontes T (2001) Identification of enzyme produced firefly oxyluciferin by reverse phase HPLC. Tetrahedron Lett 42:8173–8176Google Scholar
  35. 35.
    Ribeiro C, Esteves da Silva JC (2008) Kinetics of inhibition of firefly luciferase by oxyluciferin and dehydroluciferyl-adenylate. Photochem Photobiol 7:1085–1090Google Scholar
  36. 36.
    Branchini BR, Murtiashaw MH, Magyer RA, Anderson SM (2000) The role of lysine 529, a conserved residue of the acyl-adenylate-forming enzyme superfamily, in firefly luciferase. Biochemistry 39:5433–5440PubMedGoogle Scholar
  37. 37.
    Imai K, Goto T (1988) Improved synthesis of firefly d-luciferyl–d-adenylate—A key intermediate of firefly bioluminescence. Agric Biol Chem 52:2803–2809Google Scholar
  38. 38.
    White EH, Steinmetz MG, Miano JD, Wildes PD, Morland R (1980) Chemi- and bioluminescence of firefly luciferin. J Am Chem Soc 102:3199–3208Google Scholar
  39. 39.
    Shimomura O, Goto T, Johnson FH (1977) Source of oxygen in the CO2 produced in the bioluminescent oxidation of firefly luciferin. Proc Natl Acad Sci USA 74:2799–2802PubMedGoogle Scholar
  40. 40.
    McCapra F (1977) Alternative mechanism of dioxetanone decomposition. J Chem Soc Chem Commun (1977) 946–948Google Scholar
  41. 41.
    Koo J-Y, Schmidt SP, Schuster GB (1978) Bioluminescence of the firefly: key steps in the formation of the electronically excited state for model systems. Proc Natl Acad Sci USA 84:131–135Google Scholar
  42. 42.
    Seliger HH, McElroy WD (1960) Spectral emission and quantum yield of firefly bioluminescence. Arch Biochem Biophys 88:136–141PubMedGoogle Scholar
  43. 43.
    White EH, Roswell DF (1991) Analogs and derivatives of firefly oxyluciferin, the light emitter in firefly bioluminescence. Photochem Photobiol 53:131–136PubMedGoogle Scholar
  44. 44.
    Kajiyama N, Nakano E (1991) Isolation and characterization of mutants of firefly luciferase which produced different color of light. Protein Eng 4:691–693PubMedGoogle Scholar
  45. 45.
    Branchini BR, Murtiashaw MH, Magyar RA, Protier NC, Ruggiero MC, Stroh JG (2002) Yellow-green and red firefly bioluminescence from 5,5′-dimethoxyluciferin. J Am Chem Soc 124:2112–2113PubMedGoogle Scholar
  46. 46.
    McCapra F, Gilfoyle DJ, Young DW, Church NJ, Spencer P (1994) The chemical origin of color differences in beetle bioluminescence. In: Campbell AK, Kricka LJ, Stanley PE (eds) Bioluminescence and chemiluminescence. Fundamentals and applied aspects. Wiley, Chichester, UK, pp 387–391Google Scholar
  47. 47.
    McCapra F (1997) Mechanism in chemiluminescence and bioluminescence—unfinished business. In: Hastings JW, Kricka LJ, Stanley PE (eds) Bioluminescence and chemiluminescence molecular reporting with photons. Wiley, Chichester, UK, pp 7–15Google Scholar
  48. 48.
    Branchini RB, Southworth TL, Murtiashaw MH, Magyar RA, Gonzalez SA, Ruggiero MC, Stroh JG (2004) An alternative mechanism of bioluminescence color determination in firefly luciferase. Biochemistry 43:7255–7262PubMedGoogle Scholar
  49. 49.
    Orlova G, Goddard JD, Brovko LY (2003) The theoretical study of the amazing firefly bioluminescence: the formation and structures of the light emitters. J Am Chem Soc 125:6962–6971PubMedGoogle Scholar
  50. 50.
    Yang T, Goddard JD (2007) Prediction of the geometries and florescence emission energies of oxyluciferins. J Phys Chem 111:4489–4497Google Scholar
  51. 51.
    Nakatani N, Hasegawa J, Nakatuji H (2007) Red light in chemiluminescence and yellow-green light in bioluminescence: color-turning mechanism of firefly, Photinus pyralis, studied by the symmetry-adapted cluster-conjugation interaction method. J Am Chem Soc 129:8756–8765PubMedGoogle Scholar
  52. 52.
    Hirano T, Hasumi Y, Ohtsuka K, Maki S, Niwa H, Yamaji M, Hashizume D (2009) Spectroscopic studies of the light-color modulation mechanism of firefly (beetle) bioluminescence. J Am Chem Soc 131:2385–2396PubMedGoogle Scholar
  53. 53.
    DeLuca M, McElroy WD (1978) Purification and properties of firefly luciferase. Methods Enzymol 57:3–15Google Scholar
  54. 54.
    DeLuca M, Wannlund J, McElroy WD (1979) Factors affecting the kinetics of light emission from crude and purified firefly luciferase. Anal Biochem 95:194–198PubMedGoogle Scholar
  55. 55.
    Webster JJ, Chang JC, Manley ER, Spivey HO, Leach FR (1980) Buffer effects on ATP analysis by firefly luciferase. Anal Biochem 106:7–11PubMedGoogle Scholar
  56. 56.
    Simpson WJ, Hammond JRM (1991) The effect of detergents on firefly luciferase reaction. J Biolumi Chemilumi 6:97–106Google Scholar
  57. 57.
    Ford SR, Chenault KH, Bunton LS, Hampton GJ, McCarthy J, Hall MS, Pangburn SJ, Buck LM, Leach FR (1996) Use of firefly luciferase for ATP measurement: other nucleotides enhance turnover. J Biolumi Chemilumi 11:149–167Google Scholar
  58. 58.
    Airth RL, Rhodes WC, McElroy WD (1958) The function of coenzyme A in luminescence. Biochim Biophys Acta 27:519–532PubMedGoogle Scholar
  59. 59.
    Roda A, Guardigli M, Michelini E, Mirasoli M (2009) Bioluminescence in analytical chemistry and in vivo imaging. Trends Anal Chem 28:307–322Google Scholar
  60. 60.
    Seliger HH, McElroy WD (1959) Quantum yield in the oxidation of firefly luciferin. Biochem Biophys Res Commun 1:21–24Google Scholar
  61. 61.
    Ando Y, Niwa K, Yamada N, Enomoto T, Irie T, Kubota H, Ohmiya Y, Akiyama H (2008) Firefly bioluminescence quantum yield and color change by pH-sensitive green emission. Nat Photon 2:44–46Google Scholar
  62. 62.
    Fraga H, Esteves da Silva JCG, Fontes R (2006) Identification of luciferyl adenylate and luciferyl coenzyme A synthesized by firefly luciferase. Chem Bio Chem 5:110–115Google Scholar
  63. 63.
    Okada K, Iio H, Kubota I, Goto T (1974) Firefly bioluminescence. III. Conversion of oxyluciferin to luciferin in firefly. Tetrahedron Lett 32:2771–2774Google Scholar
  64. 64.
    Okada K, Iio H, Goto T (1976) Biosynthesis of firefly luciferin. Probable formation of benzothiazole from p-benzoquinone and cysteine. J Chem Soc Chem Comm (1976) 32Google Scholar
  65. 65.
    McCapra F, Razavi Z (1975) A model for firefly luciferin biosynthesis. J Chem Soc Chem Comm (1975) 42–43Google Scholar
  66. 66.
    McCapra F, Razavi Z (1976) Biosynthesis of luciferin in Pyroporus pellucens. J Chem Soc Chem Commun (1976) 153–154Google Scholar
  67. 67.
    Gomi K, Kajiyama N (2001) Oxyluciferin, a luminescence product of firefly luciferase, is enzymatically regenerated into luciferin. J Biol Chem 276:36508–36513PubMedGoogle Scholar
  68. 68.
    Gomi K, Hiorkawa K, Kajiyama N (2002) Molecular cloning and expression of the cDNAs encoding luciferin-regenerating enzyme from Luciola cruciata and Luciola lateralis. Gene 294:157–166PubMedGoogle Scholar
  69. 69.
    Day JC, Tisi L, Bailey MJ (2004) Evolution of beetle bioluminescence: the origin of beetle luciferin. Luminescence 19:8–20PubMedGoogle Scholar
  70. 70.
    Marques SM, Estreves da Silva JCG (2009) Firefly bioluminescence: a mechanistic approach of luciferase catalyzed reactions. IUBMB Life 61:6–17PubMedGoogle Scholar
  71. 71.
    Oba Y, Kato S, Ojika M, Inouye S (2002) Biosynthesis of luciferin in the sea firefly, Cypridina hilgendorfii: l-tryptophan is a component in Cypridina luciferin. Tetrahedron Lett 43:2389–2392Google Scholar
  72. 72.
    Kato S, Oba Y, Ojika M, Inouye S (2004) Identification of the biosynthetic units of Cypridina luciferin in Cypridina (Vargula) hilgendorfii by LC/ESI-TOF-MS. Tetrahedron 60:11427–11434Google Scholar
  73. 73.
    White EH, Wörther H, Field GF, McElroy WD (1965) Analogs of firefly luciferin. J Org Chem 30:2344–2348Google Scholar
  74. 74.
    White EH, Wörther H, Seliger HH, McElroy WD (1966) Amino analogs of firefly luciferin and biological activity thereof. J Am Chem Soc 88:2015–2019Google Scholar
  75. 75.
    White EH, Wörther H (1966) Analogs of firefly luciferin. III. J Org Chem 31:1484–1488PubMedGoogle Scholar
  76. 76.
    White EH, Rapaport E, Hopkins TA, Seliger HH (1969) Chemi- and bioluminescence of firefly luciferin. J Am Chem Soc 91:2178–2180PubMedGoogle Scholar
  77. 77.
    Seto S, Ogura K, Nishiyama Y (1963) A convenient synthetic method of 2-carbamoyl-6-methoxybenzothiazole, one of intermediates for the synthesis of firefly luciferin. Bull Chem Soc Jpn 36:331–333Google Scholar
  78. 78.
    France C, Blanchot B, Champiar D, Couble P, Declercq G, Millet J-L (1990) Synthesis and characterization of a new substrate of Photinus pyralis luciferase: 4-methyl-d-luciferin. J Clin Chem Clin Biochem 28:471–474Google Scholar
  79. 79.
    Woodroofe CC, Shultz JW, Wood MG, Osterman J, Cali JJ, Daily WJ, Meisenheimer PL, Klaubert DH (2008) N-Alkylated 6′-aminoluciferins are bioluminescent substrates for Ultra-Glo and QuantiLum luciferase: new potential scaffolds for bioluminescent assays. Biochemistry 47:10383–10393PubMedGoogle Scholar
  80. 80.
    Branchini BR, Hayward MM, Bamford S, Brennan PM, Lajiness EJ (1989) Naphtyl- and quinolyllucifferin: green and red light emitting firefly luciferin analogues. Photochem Photobiol 49:689–695PubMedGoogle Scholar
  81. 81.
    Miska W, Geiger R (1987) Synthesis and characterization of luciferin derivatives for use in bioluminescence enhanced enzyme immunoassays. J Clin Chem Clin Biochem 25:23–30PubMedGoogle Scholar
  82. 82.
    Geiger R, Miska W (1987) Bioluminescence enhanced enzyme immunoassay. J Clin Chem Clin Biochem 25:31–38PubMedGoogle Scholar
  83. 83.
    Miska W, Geiger R (1989) Luciferin derivatives in bioluminescence-enhanced enzyme immunoassays. J Biolumi Chemilumi 4:119–128Google Scholar
  84. 84.
    Hauber R, Geiger R (1988) A sensitive, bioluminescent-enhanced detection method for DNA-dot-hybridization. Nucl Acids Res 16:1213PubMedGoogle Scholar
  85. 85.
    Huber R, Geiger R (1987) A new, very sensitive, bioluminescence-enhanced detection system for protein blotting. Ultrasensitive detection systems for protein blotting and DNA hybridization, I. J Clin Chem Clin Biochem 25:511–514Google Scholar
  86. 86.
    Amess R, Baggett N, Darby PR, Goode AR, Vickers EE (1990) Synthesis of luciferin glycoside as substrate for novel ultrasensitive enzyme assays. Carbohydrate Res 205:225–233Google Scholar
  87. 87.
    Monsees T, Miska W, Geiger R (1994) Synthesis and characterization of a bioluminogenic substrate for α-chymotrypsin. Anal Biochem 221:329–334PubMedGoogle Scholar
  88. 88.
    Sudhaharan T, Reddy AR (1999) A bifunctional luminogenic substrate for two luminescent enzymes: firefly luciferase and horseradish peroxidase. Anal Biochem 271:159–167PubMedGoogle Scholar
  89. 89.
    Zhou W, Valley MP, Shultz J, Hawkins EM, Bernad L, Good T, Good D, Riss TL, Klaubert DH, Wood KV (2006) New bioluminogenic substrates for monoamine oxidase assays. J Am Chem Soc 128:3122–3123PubMedGoogle Scholar
  90. 90.
    Valley MP, Zhou W, Hawkins EM, Shultz J, Cali JJ, Worzella T, Bernad L, Good T, Good D, Riss TL, Klaubert DH, Wood KV (2006) A bioluminescent assay for monoamine oxidase activity. Anal Biochem 359:236–246Google Scholar
  91. 91.
    Craig FF, Simmonds AC, Watmore D, McCapra F, White MRH (1991) Membrane-permeable luciferin esters for assay of firefly luciferase in live intact cells. Biochem J 276:637–641PubMedGoogle Scholar
  92. 92.
    Yong J, Thompson DB (1993) An easily synthesized, photolyzable luciferase substrate for in vivo luciferase activity measurement. Biotechniques 15:848–850Google Scholar
  93. 93.
    Shinde R, Perkins J, Contag CH (2006) Luciferin derivatives for enhanced in vitro and in vivo bioluminescence assays. Biochemistry 45:11103–11112PubMedGoogle Scholar
  94. 94.
    Jones LR, Goun EA, Shinde R, Rothbard JB, Contag CH, Wender PA (2006) Releasable luciferin-transporter conjugates: tools for the real-time analysis of cellular uptake and release. J Am Chem Soc 128:6526–6527PubMedGoogle Scholar
  95. 95.
    Wender PA, Goun EA, Jones LR, Pillow TH, Rothbard JB, Shinde R, Contag CH (2007) Real-time analysis of uptake and bioactivatable cleavage of luciferin-transporter conjugates in transgenic reporter mice. Proc Natl Acad Sci USA 104:10340–10345PubMedGoogle Scholar
  96. 96.
    Chandran SS, Williams SA, Denmeade SR (2008) Extended-release PEG-luciferin allows for long-term imaging of firefly luciferase activity in vivo. Luminescence 24:35–38Google Scholar
  97. 97.
    Gates BJ, DeLuca M (1975) The production of oxyluciferin during the firefly luciferase light reaction. Arch Biochem Biophys 169:616–621PubMedGoogle Scholar
  98. 98.
    McElroy WD, Hastings JW, Coulombre J, Sonnenfeld V (1953) The mechanism of action of pyrophosphate in firefly luminescence. Arch Biochem Biophys 46:399–416PubMedGoogle Scholar
  99. 99.
    Lee RT, McElroy WD (1971) Isolation and partial characterization of a peptide derived from the luciferin binding site of firefly luciferase. Arch Biochem Biophys 146:551–556PubMedGoogle Scholar
  100. 100.
    Lee RT, Denburg TL, McElroy WD (1970) Substrate-binding properties of firefly luciferase. Arch Biochem Biophys 141:38–52PubMedGoogle Scholar
  101. 101.
    Ueda I (1965) Effects of diethylether and halothane on firefly luciferin bioluminescence. Anesthesiology 26:603606Google Scholar
  102. 102.
    Ueda I, Suzuki A (1998) Is there a specific receptor for anesthetics? Contrary effects of alcohols and fatty acids on phase transition and bioluminescence of firefly luciferase. Biophys J 75:1052–1057PubMedGoogle Scholar
  103. 103.
    Ueda I, Suzuki A (1998) Irreversible phase transition of firefly luciferase: contrasting effects of volatile anesthetics and myristic acid. Biochim Biophys Acta 1380:313–319PubMedGoogle Scholar
  104. 104.
    Rocha S, Campbell KJ, Roche KC, Perkins ND (2003) The p53-inhibitor pifithrin-α inhibits firefly luciferase activity in vivo and in vitro. BMC Mol Biol 4:1–8Google Scholar
  105. 105.
    Niwa K, Ohmiya Y (2004) Inhibitory effect of lipoic acid on firefly luciferase bioluminescence. Biochem Biophys Res Commun 323:625–629PubMedGoogle Scholar
  106. 106.
    Heitman LH, van Veldhoven JP, Zweemer AM, Ye K, Brussee J, IJzerman AP (2008) False positives in a reporter gene assay: Identification and synthesis of substituted N-pyridin-2-ylbenzamides as competitive inhibitors of firefly luciferase. J Med Chem 51:4724–4729PubMedGoogle Scholar
  107. 107.
    Auld DS, Zhang YQ, Southall NT, Rai G, Landsman M, Maclure J, Langevin D, Thomas CJ, Austin CP, Inglese J (2009) A basis for reduced chemical library inhibition of firefly luciferase obtained from directed evolution. J Med Chem 52:1450–1458Google Scholar
  108. 108.
    Auld DS, Southall NT, Jadhav A, Johnson RL, Diller DJ, Simeonov A, Austin CP, Inglese J (2008) Characterization of chemical libraries for luciferase inhibitory activity. J Med Chem 5:2372–2386Google Scholar
  109. 109.
    Auld DS, Thorne N, Nguyen D-T, Inglese J (2008) A specific mechanism for nonspecific activation in reporter-gene assays. ACS Chem Biol 3:463–470PubMedGoogle Scholar
  110. 110.
    Green AA, McElroy WD (1956) Crystalline firefly luciferase. Biochim Biophys Acta 20:170–176PubMedGoogle Scholar
  111. 111.
    Branchini BR, Marschner TM, Montemurro AM (1980) A convenient affinity chromatography-based purification of firefly luciferase. Anal Biochem 104:386–396PubMedGoogle Scholar
  112. 112.
    Rajgopal S, Vijayalakshmi M (1982) Purification of luciferase by affinity elution chromatography on Blue Dextran columns: comparison of Sepharose and silica as support matrices. J Chromatogr 243:164–167Google Scholar
  113. 113.
    Belinga HF, Steghens JP, Collombel C (1995) Firefly luciferase purification using polyethlene glycol and Dyematrex Orange A. J Chromatogr A 695:33–40Google Scholar
  114. 114.
    Kajiyama N, Masuda T, Tatsumi H, Nakano E (1992) Purification and characterization of luciferases from fireflies, Luciola cruciata and Luciola lateralis. Biochim Biophys Acta 1120:228–232PubMedGoogle Scholar
  115. 115.
    Devine JH, Kutuzova GD, Green VA, Ugarova NN, Baldwin TO (1993) Luciferase from the East European firefly Luciola mingrelica: cloning and nucleotide sequence of the cDNA, overexpression in Escherichia coli and purification of the enzyme. Biochim Biophys Acta 1173:121–132PubMedGoogle Scholar
  116. 116.
    Branchini BR, Magyar RA, Murtiashaw MH, Anderson SM, Zimmer M (1998) Site-directed mutagenesis of histidine 245 in firefly luciferase: a proposed model of the active site. Biochemistry 37:15311–15319PubMedGoogle Scholar
  117. 117.
    Inouye S, Sahara Y (2008) Soluble protein expression in E. coli cells using IgG binding domain of protein A as a solubilizing partner in the cold induced system. Biochem Biophys Res Commun 376:448–453PubMedGoogle Scholar
  118. 118.
    de Wet JR, Wood KV, Helinski DR, DeLuca M (1985) Cloning of firefly luciferase cDNA and the expression of active luciferase in Escherichia coli. Proc Natl Acad Sci USA 82:7870–7873PubMedGoogle Scholar
  119. 119.
    de Wet JR, Wood KV, DeLuca M, Helinski DR, Subramani S (1987) Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol 7:725–737PubMedGoogle Scholar
  120. 120.
    Keller GA, Gould S, DeLuca M, Subramani S (1987) Firefly luciferase is targeted to peroxisomes in mammalian cells. Proc Natl Acad Sci USA 84:3264–3268PubMedGoogle Scholar
  121. 121.
    Cho KH, Lee JS, Choi YD, Boo KS (1999) Structural polymorphism of the luciferase gene in the firefly, Luciola lateralis. Insect Mol Biol 8:193–200PubMedGoogle Scholar
  122. 122.
    Schröder J (1989) Protein sequence homology between plant 4-coumarate:CoA ligase and firefly luciferase. Nucl Acids Res 17:460PubMedGoogle Scholar
  123. 123.
    Suzuki H, Kawarabayasi Y, Kondo J, Abe T, Nishikawa K, Kimura S, Hashimoto T, Yamamoto T (1990) Structure and regulation of rat long-chain acyl-CoA synthetase. J Biol Chem 265:8681–8685PubMedGoogle Scholar
  124. 124.
    Toh H (1991) Sequence analysis of firefly luciferase family reveals a conservative sequence motif. Protein Seq Data Anal 4:111–117PubMedGoogle Scholar
  125. 125.
    Ye L, Buck LM, Schaeffer HJ, Leach FR (1997) Cloning and sequencing of a cDNA for firefly luciferase from Photuris pennsylvanica. Biochim Biophys Acta 1339:39–52PubMedGoogle Scholar
  126. 126.
    Choi YS, Bae JS, Lee KS, Kim SR, Kim I, Kim JG, Kim KY, Kim SE, Suzuki H, Lee SM, Sohn HD, Jin BR (2003) Genomic structure of the luciferase gene and phylogenetic analysis in the Hotaria-group fireflies. Comp Biochem Physiol 134B:199–214Google Scholar
  127. 127.
    Conti E, Franks NP, Brick P (1996) Crystal structure of firefly luciferase throws light on superfamily of adenylate-forming enzymes. Structure 4:287–298PubMedGoogle Scholar
  128. 128.
    Franks NP, Jenkins JE, Conti E, Lieb WR, Brick P (1998) Structural basis for the inhibition of firefly luciferase by a general anesthetic. Biophys J 75:2205–2211PubMedGoogle Scholar
  129. 129.
    Branchini BR, Murtiashaw MH, Carmody JN, Mygatt EE, Southworth TL (2005) Synthesis of an N-acyl sulfamate analog of luciferyl-AMP: a stable and potent inhibitor of firefly luciferase. Bioorg Med Chem Lett 15:3860–3864PubMedGoogle Scholar
  130. 130.
    Nakatsu T, Ichiyama S, Hiratake J, Saldanha A, Kobashi N, Sakata K, Kato H (2006) Structural basis for the spectral difference in luciferase bioluminescence. Nature 440:372–376PubMedGoogle Scholar
  131. 131.
    Oba Y, Sato M, Ojika M, Inouye S (2005) Enzymatic and genetic characterization of firefly luciferase and Drosophila CG6178 as a fatty acyl-CoA synthetase. Biosci Biotechnol Biochem 69:819–828PubMedGoogle Scholar
  132. 132.
    Oba Y, Ojika M, Inouye S (2004) Characterization of CG6178 gene product with high sequence similarity to firefly luciferase in Drosophila melanogaster. Gene 329:137–145PubMedGoogle Scholar
  133. 133.
    Oba Y, Tanaka K, Inouye S (2006) Catalytic properties of domain-exchanged chimeric Proteins between firefly luciferase and Drosophila fatty acyl-CoA synthetase CG6178. Biochem Biocsci Biotechnol 70:2739–2744Google Scholar
  134. 134.
    Oba Y, Sato M, Ohta Y, Inouye S (2006) Identification of paralogous genes of firefly luciferase in the Japanese firefly, Luciola cruciata. Gene 368:53–60PubMedGoogle Scholar
  135. 135.
    Oba Y, Sato M, Inouye S (2006) Cloning and characterization of the homologous genes of firefly luciferase in the mealworm beetle, Tenebrio molitor. Insect Mol Biol 15:293–299PubMedGoogle Scholar
  136. 136.
    Oba Y, Iida K, Ojika M, Inouye S (2008) Orthologous gene of beetle luciferase in non-luminous click beetle, Agrypnus binodulus (Elateridae), encodes a fatty acyl-CoA synthetase. Gene 407:169–175PubMedGoogle Scholar
  137. 137.
    Oba Y (2009) On the origin of beetle luminescence. In: Meyer-Rochow VB (ed) Bioluminescence in focus. Res Signpost, India, pp 277–290Google Scholar
  138. 138.
    Oba Y, Iida K, Inouye S (2009) Functional conversion of fatty acyl-CoA synthetase to firefly luciferase by site-directed mutagenesis: a key substitution responsible for luminescence activity. FEBS Lett 583:2004–2008PubMedGoogle Scholar
  139. 139.
    Masuda T, Tatsumi H, Nakano E (1989) Cloning and sequence analysis of cDNA for luciferase of a Japanese firefly, Luciola cruciata. Gene 77:265–270PubMedGoogle Scholar
  140. 140.
    Tatsumi H, Kajiyama N, Nakano E (1992) Molecular cloning and expression in Escherichia coli of a cDNA clone encoding luciferase of a firefly, Luciola lateralis. Biochim Biophys Acta 1131:161–165PubMedGoogle Scholar
  141. 141.
    Zenno S, Shiraishi S, Inouye S, Saigo K (1993) Photuris firefly luciferase gene. Jpn Pat Appl 5-119050Google Scholar
  142. 142.
    Ohmiya Y, Ohba N, Toh H, Tsuji FI (1995) Cloning, expression and sequence analysis of cDNA for the luciferases from the Japanese fireflies, Pyrocoelia miyako and Hataria parvula. Photochem Photobiol 62:309–313PubMedGoogle Scholar
  143. 143.
    Lee KS, Park HJ, Bae JS, Goo TW, Kim I, Sohn HD, Jin BR (2001) Molecular cloning and expression of a cDNA encoding the luciferase from the firefly, Pyrocoelia rufa. J Biotechnol 92:9–19PubMedGoogle Scholar
  144. 144.
    Choi YS, Lee KS, Bae JS, Lee KM, Kim SR, Kim I, Lee SM, Sohn HD, Jin BR (2002) Molecular cloning and expression of a cDNA encoding the luciferase from the firefly, Hotaria unmunsana. Comp Biochem Physiol B Biochem Mol Biol 132:661–670PubMedGoogle Scholar
  145. 145.
    Sala-Newby GB, Thomson CM, Campbell AK (1996) Sequence and biochemical similarities between the luciferases of the glow-worm Lampyris noctiluca and the firefly Photinus pyralis. Biochem J 313:761–767PubMedGoogle Scholar
  146. 146.
    Alipour BS, Hosseinkhani S, Nikkhah M, Naderi-Manesh H, Chaichi MJ, Osaloo SK (2004) Molecular cloning, sequence analysis, and expression of a cDNA encoding the luciferase from the glow-worm, Lampyris turkestanicus. Biochem Biophys Res Commun 325:215–222PubMedGoogle Scholar
  147. 147.
    Viviani VR, Arnoldi FG, Brochetto-Braga M, Ohmiya Y (2004) Cloning and characterization of the cDNA for the Brazilian Cratomorphus distinctus larval firefly luciferase: similarities with European Lampyris noctiluca and Asiatic Pyrocoelia luciferases. Comp Biochem Physiol B Biochem Mol Biol 139:151–156PubMedGoogle Scholar
  148. 148.
    Emamzadeh AR, Hosseinkhani S, Sadeghizadeh M, Nikkhah M, Chaichi MJ, Mortazavi M (2006) cDNA cloning, expression and homology modeling of a luciferase from the firefly Lampyroidea maculata. J Biochem Mol Biol 39:578–585PubMedGoogle Scholar
  149. 149.
    Wood KV, Lam YA, Seliger HH, McElroy WD (1989) Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors. Science 244:700–702PubMedGoogle Scholar
  150. 150.
    Viviani VR, Silva AC, Perez GL, Santelli RV, Bechara EJ, Reinach FC (1999) Cloning and molecular characterization of the cDNA for the Brazilian larval click-beetle Pyrearinus termitilluminans luciferase. Photochem Photobiol 70:254–260PubMedGoogle Scholar
  151. 151.
    Stolz U, Velez S, Wood KV, Wood M, Feder JL (2003) Darwinian natural selection for orange bioluminescent color in a Jamaican click beetle. Proc Natl Acad Sci USA 100:14955–14959PubMedGoogle Scholar
  152. 152.
    Viviani VR, Bechara EJ, Ohmiya Y (1999) Cloning, sequence analysis, and expression of active Phrixothrix railroad-worms luciferases: relationship between bioluminescence spectra and primary structures. Biochemistry 38:8271–8279PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Yokohama Research Center, Chisso CorporationYokohamaJapan

Personalised recommendations