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Crystal structure of native and a mutant of Lampyris turkestanicus luciferase implicate in bioluminescence color shift.

Kheirabadi M, Sharafian Z, Naderi-Manesh H, Heineman U, Gohlke U, Hosseinkhani S
Biochim Biophys Acta 1834 2729-35 (2013)
Cited: 16 times
EuropePMC logo PMID: 24103420

Abstract

Firefly bioluminescence reaction in the presence of Mg(2+), ATP and molecular oxygen is carried out by luciferase. The luciferase structure alterations or modifications of assay conditions determine the bioluminescence color of firefly luciferase. Among different beetle luciferases, Phrixothrix hirtus railroad worm emits either yellow or red bioluminescence color. Sequence alignment analysis shows that the red-emitter luciferase from Phrixothrix hirtus has an additional arginine residue at 353 that is absent in other firefly luciferases. It was reported that insertion of Arg in an important flexible loop350-359 showed changes in bioluminescence color from green to red and the optimum temperature activity was also increased. To explain the color tuning mechanism of firefly luciferase, the structure of native and a mutant (E354R/356R/H431Y) of Lampyris turkestanicus luciferase is determined at 2.7Å and 2.2Å resolutions, respectively. The comparison of structure of both types of Lampyris turkestanicus luciferases reveals that the conformation of this flexible loop is significantly changed by addition of two Arg in this region. Moreover, its surface accessibility is affected considerably and some ionic bonds are made by addition of two positive charge residues. Furthermore, we noticed that the hydrogen bonding pattern of His431 with the flexible loop is changed by replacing this residue with Tyr at this position. Juxtaposition of a flexible loop (residues 351-359) in firefly luciferase and corresponding ionic and hydrogen bonds are essential for color emission.

Articles - 4m46 mentioned but not cited (1)

  1. Beetle luciferases with naturally red- and blue-shifted emission. Carrasco-López C, Ferreira JC, Lui NM, Schramm S, Berraud-Pache R, Navizet I, Panjikar S, Naumov P, Rabeh WM. Life Sci Alliance 1 e201800072 (2018)


Reviews citing this publication (3)

  1. Split-luciferase complementary assay: applications, recent developments, and future perspectives. Azad T, Tashakor A, Hosseinkhani S. Anal Bioanal Chem 406 5541-5560 (2014)
  2. Luciferin-Regenerating Enzyme Crystal Structure Is Solved but its Function Is Still Unclear. Hosseinkhani S, Emamgholi Zadeh E, Sahebazzamani F, Ataei F, Hemmati R. Photochem Photobiol 93 429-435 (2017)
  3. The elusive relationship between structure and colour emission in beetle luciferases. Carrasco-López C, Lui NM, Schramm S, Naumov P. Nat Rev Chem 5 4-20 (2021)

Articles citing this publication (12)

  1. A highly efficient, thermostable and cadmium selective firefly luciferase suitable for ratiometric metal and pH biosensing and for sensitive ATP assays. Pelentir GF, Bevilaqua VR, Viviani VR. Photochem Photobiol Sci 18 2061-2070 (2019)
  2. Prediction of bioluminescent proteins by using sequence-derived features and lineage-specific scheme. Zhang J, Chai H, Yang G, Ma Z. BMC Bioinformatics 18 294 (2017)
  3. Phrixotrix luciferase and 6'-aminoluciferins reveal a larger luciferin phenolate binding site and provide novel far-red combinations for bioimaging purposes. Bevilaqua VR, Matsuhashi T, Oliveira G, Oliveira PSL, Hirano T, Viviani VR. Sci Rep 9 8998 (2019)
  4. Histidine substitution in the most flexible fragments of firefly luciferase modifies its thermal stability. Rahban M, Salehi N, Saboury AA, Hosseinkhani S, Karimi-Jafari MH, Firouzi R, Rezaei-Ghaleh N, Moosavi-Movahedi AA. Arch Biochem Biophys 629 8-18 (2017)
  5. The proton and metal binding sites responsible for the pH-dependent green-red bioluminescence color tuning in firefly luciferases. Viviani VR, Gabriel GVM, Bevilaqua VR, Simões AF, Hirano T, Lopes-de-Oliveira PS. Sci Rep 8 17594 (2018)
  6. ΔFlucs: Brighter Photinus pyralis firefly luciferases identified by surveying consecutive single amino acid deletion mutations in a thermostable variant. Halliwell LM, Jathoul AP, Bate JP, Worthy HL, Anderson JC, Jones DD, Murray JAH. Biotechnol Bioeng 115 50-59 (2018)
  7. Bifunctional role of leucine 300 of firefly luciferase in structural rigidity. Yousefi F, Ataei F, Mortazavi M, Hosseinkhani S. Int J Biol Macromol 101 67-74 (2017)
  8. Surface Arginine Saturation Effect on Unfolding Reaction of Firefly Luciferase: A Thermodynamic and Kinetic Perspective. Solgi Z, Khalifeh K, Hosseinkhani S, Ranjbar B. Photochem Photobiol 92 688-693 (2016)
  9. Effect of pH on the secondary structure and thermostability of beetle luciferases: structural origin of pH-insensitivity. Tomazini A, Carvalho M, Murakami MT, Viviani VR. Photochem Photobiol Sci 22 893-904 (2023)
  10. Increase of segmental mobility through insertion of a flexible linker in split point of firefly luciferase. Bahmani P, Hosseinkhani S. Int J Biol Macromol 94 762-770 (2017)
  11. Label-Free and Bioluminescence-Based Nano-Biosensor for ATP Detection. Karimi E, Nikkhah M, Hosseinkhani S. Biosensors (Basel) 12 918 (2022)
  12. The orange light emitting luciferase from the rare Euryopa clarindae adult railroadworm (Coleoptera:Phengodidae): structural/functional and evolutionary relationship with green and red emitting luciferases. Viviani VR, Benites GR, Souza DR, Pelentir GF, Reis RM, Bechara EJH, Tomazini A. Photochem Photobiol Sci (2023)


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