Article

You have full text access to this OnlineOpen article

Enhanced red-emitting railroad worm luciferase for bioassays and bioimaging†

  1. Xueyan Li1,
  2. Yoshihiro Nakajima1,
  3. Kazuki Niwa1,
  4. Vadim R. Viviani2,
  5. Yoshihiro Ohmiya1,*

Article first published online: 28 OCT 2009

DOI: 10.1002/pro.279

Issue

Protein Science

Protein Science

Volume 19, Issue 1, pages 26–33, January 2010

Additional Information

How to Cite

Li, X., Nakajima, Y., Niwa, K., Viviani, V. R. and Ohmiya, Y. (2010), Enhanced red-emitting railroad worm luciferase for bioassays and bioimaging. Protein Science, 19: 26–33. doi: 10.1002/pro.279

Author Information

  1. 1

    Cell Dynamics Research Group, Research Institute for Cell Engineering, National Institute of Advanced Industrial Science and Technology (AIST), Ikeda, Osaka 563-8577, Japan

  2. 2

    Laboratório de Bioquímica e Biotecnologia de Sistemas Bioluminescentes, Universidade Federal de São Carlos, Campus de Sorocaba, Sorocaba, SP, Brazil

*1-8-31 Midorigaoda, Ikeda, Osaka 563-8577, Japan,

  1. †

    The authors declare no conflicts of interest.

Publication History

  1. Issue published online: 6 JAN 2010
  2. Article first published online: 28 OCT 2009
  3. Accepted manuscript online: 28 OCT 2009 12:00AM EST
  4. Manuscript Accepted: 9 OCT 2009
  5. Manuscript Received: 10 JUL 2009

Funded by

  • NEDO grant (Chemical Substance Management Technology Projects of Development of Simple and Highly Functional Hazard Assessment Methods)
  • The Ministry of Economy, Trade and Industry of Japan

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (199K)

References

  • 1
    Brovko LY, Griffiths MW ( 2007) Illuminating cellular physiology: recent developments. Sci Prog 90: 129–160.
  • 2
    Naylor H ( 1999) Reporter gene technology: the future looks bright. Biochem Pharmacol 58: 749–757.
  • 3
    Roda A, Pasini P, Mirasoli M, Michelini E, Guardig M ( 2004) Biotechnological applications of bioluminescence and chemiluminescence. Trends Biotechnol 22: 295–303.
  • 4
    Dothager RS, Flentie K, Moss B, Pan MH, Kesarwala A, Piwnica-Worms D ( 2009) Advances in bioluminescence imaging of live animal models. Curr Opin Biotech 20: 1–9.
  • 5
    Zhao H, Doyle TC, Coquoz O, Kalish F, Rice BW, Contag CH ( 2005) Emission spectra of bioluminescent reporters and interaction with mammalian tissue determine the sensitivity of detection in vivo. J Biomed Opt 10: 41210.
  • 6
    Villalobos V, Naik S, Piwnica-Worms D ( 2007) Current state of imaging protein–protein interactions in vivo with genetically encoded reporters. Annu Rev Biomed Eng 9: 321–349.
  • 7
    Miloud T, Henrich C, Hämmerling GJ ( 2007) Quantitative comparison of click beetle and firefly luciferases for in vivo bioluminescence imaging. J Biomed Opt 12: 054018.
  • 8
    Kitayama Y, Kondo T, Nakahira Y, Nishimura H, Ohmiya Y, Oyama T ( 2004) An in vivo dual-reporter system of Cyanobacteria using two railroad-worm luciferases with different color emissions. Plant Cell Physiol 45: 109–113.
  • 9
    Nakajima Y, Ikeda M, Kimura T, Honma S, Ohmiya Y, Honma K ( 2004) Biodirectional role of orphan nuclear receptor RORα in clock gene transcriptions demonstrated by a novel reporter assay system. FEBS Lett 565: 122–126.
  • 10
    Nakajima Y, Kimura T, Sugata K, Enomoto T, Asakawa A, Kubota H, Ikeda M, Ohmiya Y ( 2005) Multicolor luciferase assay system: one step monitoring of multiple gene expressions with a single substrate. Biotechniques 38: 891–894.
  • 11
    Noguchi T, Ikeda M, Ohmiya Y, Nakajima Y ( 2008) Simultaneous monitoring of independent gene expression patterns in two types of cocultured fibroblasts with different color-emitting luciferases. BMC Biotechnol 8: 40.
  • 12
    Michelini E, Cevenini L, Mezzanotte L, Ablamsky D, Southworth T, Branchini BR, Roda A ( 2008) Spectral-resolved gene technology for multiplexed bioluminescence and high-content screening. Anal Chem 80: 260–267.
  • 13
    Michelini E, Cevenini L, Mezzanotte L, Ablamsky D, Southworth T, Branchini BR, Roda A ( 2008) Combining intracellular and secreted bioluminescent reporter proteins for multicolor cell-based assays. Photochem Photobiol Sci 7: 212–217.
  • 14
    Viviani VR ( 2002) The origin, diversity and structure–function relationships of insect luciferases. Cell Mol Life Sci 59: 1833–1850.
  • 15
    Viviani VR, Bechara EJH, Ohmiya Y ( 1999) Cloning, sequence analysis, and expression of active Phrixothrix railroad-worms luciferases: relationship between bioluminescence spectra and primary structures. Biochemistry 38: 8271–8279.
  • 16
    Conti E, Franks NP, Brick P ( 1996) Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4: 287–298.
  • 17
    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: 372–376.
  • 18
    Branchini BR, Magyar RA, Murtiashaw MH, Anderson SM, Helgerson LC, Zimmer M ( 1999) Site-directed mutagenesis of firefly luciferase active site amino acids: a proposed model for bioluminescence color. Biochemistry 38: 13223–13230.
  • 19
    Branchini BR, Magyar RA, Murtiashaw MH, Portier NC ( 2001) The role of active site residue Arginine 218 in firefly luciferase bioluminescence. Biochemistry 40: 2410–2418.
  • 20
    Branchini BR, Southworth TL, Murtiashaw MH, Boije H, Fleet SE ( 2003) A mutagenesis study of the putative luciferin binding site residues of firefly luciferase. Biochemistry 42: 10429–10436.
  • 21
    Branchini BR, Southworth TL, Khattak NK, Murtiashaw MH, Fleet E ( 2004) Rational and random mutagenesis of firefly luciferase to identify an efficient emitter of red bioluminescence. Proc SPIE 5329: 170–177.
  • 22
    Branchini BR, Southworth TL, Khattak NF, Michelini E, Roda A ( 2005) Red- and green-emitting firefly luciferase mutants for bioluminescent reporter applications. Anal Biochem 345: 140–148.
  • 23
    Branchini BR, Southworth TL, Khattak NF, Michelini E, Roda A ( 2007) Thermostable red and green light-producing firefly luciferase mutants for bioluminescent reporter applications. Anal Biochem 361: 253–262.
  • 24
    Shapiro E, Lu C, Baneyx F ( 2005) A set of multicolored Photinus pyralis luciferase mutants for in vivo bioluminescence applications. Protein Eng Des Select 18: 581–587.
  • 25
    Moradi A, Hosseinkhani S, Naderi-Manesh H, Sadeghizadeh M, Alipour BS ( 2009) Effect of charge distribution in a flexible loop on the bioluminescence color of firefly luciferases. Biochemistry 48: 575–582.
  • 26
    Kajiyama N, Nakano E ( 1991) Isolation and characterization of mutants of firefly luciferase which produce different colors of light. Protein Eng 4: 691–693.
  • 27
    Tafreshi NK, Hosseinkhani S, Sadeghizadeh M, Sadeghi M, Ranjbar B, Naderi-Manesh H ( 2007) The influence of insertion of critical residue (Arg356) in structure and bioluminescence spectra of firefly luciferase. J Biol Chem 282: 8641–8647.
  • 28
    Promega Corporation ( 2003) Chroma-Glo Luciferase Assay System. Technical Manual No. TM062, Promega, WI.
  • 29
    Baggett B, Roy R, Momen S, Morgan S, Tisi L, Morse D, Gillies RJ ( 2004) Thermostability of firefly luciferases affects efficiency of detection by in vivo bioluminescence. Mol Imaging 3: 324–332.
  • 30
    White PJ, Squirrell DJ, Arnaud P, Lowe CR, Murray JAH ( 1996) Improved thermostability of the North American firefly luciferase: saturation mutagenesis at position 354. Biochem J 319: 343–350.
  • 31
    Tisi LC, White PJ, Squirrell DJ, Murphy MJ, Lowe CR, Murray JAH ( 2002) Development of a thermostable firefly luciferase. Analytica Chimica Acta 457: 115–123.
  • 32
    Law GHE, Gandelman OA, Tisi LC, Lowe CR, Murray JAH ( 2006) Mutagenesis of solvent-exposed amino acids in Photinus pyralis luciferase improves thermostability and pH-tolerance. Biochem J 397: 305–312.
  • 33
    Kajiyama N, Nakano E ( 1993) Thermostabilization of firefly luciferase by a single amino acid substitution at position 217. Biochemistry 32: 13795–13799.
  • 34
    Kajiyama N, Nakano E ( 1994) Enhancement of thermostability of firefly luciferase from Luciola lateralis by a single amino acid substitution. Biosci Biotech Biochem 58: 1170–1171.
  • 35
    Kitayama A, Yoshizaki H, Ohmiya Y, Ueda H, Nagamune T ( 2003) Creation of a thermostable firefly luciferase with pH-insensitive luminescent color. Photochem Photobiol 77: 333–338.
  • 36
    Kyte J, Doolittle RF ( 1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132.
  • 37
    Viviani VR, Arnoldi FGC, Venkatesh B, Silva Neto AJ, Ogawa FGT, Oehlmeyer TL, Ohmiya Y ( 2006) Active-site properties of Phrixothrix railroad worm green and red bioluminescence-eliciting luciferases. J Biochem (Japan) 140: 467–474.
  • 38
    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: 15311–15319.
  • 39
    Viviani VR, Oehlmeyer TL, Arnoldi FGC, Brochetto-Braga MR ( 2005) A new firefly luciferase with bimodal spectrum: identification of structural determinants of spectral pH-sensitivity in firefly luciferase. Photochem Photobiol 81: 843–848.
  • 40
    Vieille C, Zeikus G ( 2001) Hyperthermophilic enzymes: sources, uses and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65: 1–43.
  • 41
    Viviani VR, Ohmiya Y ( 2000) Bioluminescence color determinant of Phrixothrix railroad-worm luciferase: chimeric luciferase, site-directed mutagenesis of Arg215 and guanidine effect. Photochem Photobiol 72: 267–271.
  • 42
    Viviani VR, Arnoldi FGC, Ogawa FTG, Brochetto-Braga MR ( 2007) Few substitutions affect the bioluminescence spectra of Phrixothrix railroad worm (Coleoptera: Phengodidae) luciferases: a site-directed mutagenesis survey. Luminescence 22: 362–369.
    Direct Link:
  • 43
    Viviani VR, Uchida A, Suenaga N, Ryufuku M, Ohmiya Y ( 2001) Thr226 is a key residue for bioluminescence spectra determination in beetle luciferase. Biochem Biophys Res Commun 280: 1286–1291.
  • 44
    Viviani VR, Uchida A, Viviani W, Ohmiya Y ( 2002) The influence of Ala243 (Gly247), Arg 215 and Thr226 (Asn230) on the bioluminescence spectra and pH-sensitivity of railroad worm, click beetle and firefly luciferases. Photochem Photobiol 76: 538–544.
  • 45
    Viviani VR, Neto AJS, Arnoldi FGC, Barbosa JARG, Ohmiya Y ( 2008) The influence of the loop between residues 223–235 in beetle luciferase bioluminescence spectra: a solvent gate for the active site of pH-sensitive luciferases. Photochem Photobiol 84: 138–144.
  • 46
    Orlova G, Goddard JD, Brovko LY ( 2003) Theoretical study of the amazing firefly bioluminescence: the formation and structures of the light emitter. J Am Chem Soc 125: 6962–6971.
  • 47
    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: 2385–2396.
  • 48
    Morton RA, Hopkins TA, Seliger HH ( 1969) Spectroscopic properties of firefly luciferin and related compounds: an approach to product emission. Biochemistry 8: 1598–1607.
  • 49
    Wood KV ( 1995) The chemical mechanism and evolutionary development of beetle bioluminescence. Photochem Photobiol 62: 662–673.
    Direct Link:
  • 50
    Ugarova NN, Brovko LY ( 2002) Protein structure and bioluminescence spectra for firefly bioluminescence. Luminescence 17: 321–330.
    Direct Link:
  • 51
    Branchini BR, Ablamsky DM, Rosenman JM, Uzasci L, Southworth TL, Zimmer M ( 2007) Synergistic mutations produce blue-shifted bioluminescence in firefly luciferase. Biochemistry 46: 13847–13855.
  • 52
    Nakajima Y, Yoshida S, Inoue Y, Ono T ( 1996) Occupation of the QB-binding pocket by a photosystem II inhibitor triggers dark cleavage of the D1 protein subjected to brief preillumination. J Biol Chem 271: 17383–17389.
View Full Article (HTML) Get PDF (199K)