Unanimous Model for Describing the Fast Bioluminescence Kinetics of Ca2+‐regulated Photoproteins of Different Organisms

Upon binding their metal ion cofactors, Ca2+‐regulated photoproteins display a rapid increase of light signal, which reaches its peak within milliseconds. In the present study, we investigate bioluminescence kinetics of the entire photoprotein family. All five recombinant hydromedusan Ca2+‐regulated photoproteins—aequorin from Aequorea victoria, clytin from Clytia gregaria, mitrocomin from Mitrocoma cellularia and obelins from Obelia longissima and Obelia geniculata—demonstrate the same bioluminescent kinetics pattern. Based on these findings, for the first time we propose a unanimous kinetic model describing the bioluminescence mechanism of Ca2+‐regulated photoproteins.

[1]  Zhi-jie Liu,et al.  Mitrocomin from the jellyfish Mitrocoma cellularia with deleted C-terminal tyrosine reveals a higher bioluminescence activity compared to wild type photoprotein. , 2016, Journal of photochemistry and photobiology. B, Biology.

[2]  E. Vysotski,et al.  Semisynthetic photoprotein reporters for tracking fast Ca^2+ transients , 2015, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[3]  S. Markova,et al.  Characterization of hydromedusan Ca2+-regulated photoproteins as a tool for measurement of Ca2+concentration , 2014, Analytical and Bioanalytical Chemistry.

[4]  A. Campbell,et al.  An endogenous green fluorescent protein–photoprotein pair in Clytia hemisphaerica eggs shows co-targeting to mitochondria and efficient bioluminescence energy transfer , 2014, Open Biology.

[5]  Zhi-jie Liu,et al.  Crystal structures of the F88Y obelin mutant before and after bioluminescence provide molecular insight into spectral tuning among hydromedusan photoproteins , 2014, The FEBS journal.

[6]  Zhi-jie Liu,et al.  Structures of the Ca2+-regulated photoprotein obelin Y138F mutant before and after bioluminescence support the catalytic function of a water molecule in the reaction. , 2014, Acta crystallographica. Section D, Biological crystallography.

[7]  P. Pinton,et al.  Subcellular calcium measurements in mammalian cells using jellyfish photoprotein aequorin-based probes , 2013, Nature Protocols.

[8]  S. Markova,et al.  Role of key residues of obelin in coelenterazine binding and conversion into 2-hydroperoxy adduct. , 2013, Journal of photochemistry and photobiology. B, Biology.

[9]  Takeharu Nagai,et al.  Genetically encoded Ca(2+) indicators: properties and evaluation. , 2013, Biochimica et biophysica acta.

[10]  A. Visser,et al.  Bioluminescent and spectroscopic properties of His—Trp—Tyr triad mutants of obelin and aequorin , 2013, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[11]  Zhi-jie Liu,et al.  Oxygen Activation of Apo‐obelin–Coelenterazine Complex , 2013, Chembiochem : a European journal of chemical biology.

[12]  Nathan Christopher Shaner,et al.  Expression and characterization of the calcium-activated photoprotein from the ctenophore Bathocyroe fosteri: insights into light-sensitive photoproteins. , 2013, Biochemical and biophysical research communications.

[13]  S. Markova,et al.  The light‐sensitive photoprotein berovin from the bioluminescent ctenophore Beroe abyssicola: a novel type of Ca2+‐regulated photoprotein , 2012, The FEBS journal.

[14]  H. Westerblad,et al.  Methods to detect Ca(2+) in living cells. , 2012, Advances in experimental medicine and biology.

[15]  M. Taghdir,et al.  Cloning, Sequencing, Expression and Structural Investigation of Mnemiopsin from Mnemiopsis leidyi: An Attempt Toward Understanding Ca2+-Regulated Photoproteins , 2011, The protein journal.

[16]  M. Taghdir,et al.  A unique EF-hand motif in mnemiopsin photoprotein from Mnemiopsis leidyi: implication for its low calcium sensitivity. , 2011, Biochemical and biophysical research communications.

[17]  W. Chazin Relating form and function of EF-hand calcium binding proteins. , 2011, Accounts of chemical research.

[18]  S. Markova,et al.  Green-fluorescent protein from the bioluminescent jellyfish Clytia gregaria: cDNA cloning, expression, and characterization of novel recombinant protein , 2010, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[19]  M. Whitaker Genetically encoded probes for measurement of intracellular calcium. , 2010, Methods in cell biology.

[20]  A. Visser,et al.  The intrinsic fluorescence of apo‐obelin and apo‐aequorin and use of its quenching to characterize coelenterazine binding , 2009, FEBS letters.

[21]  S. Inouye Cloning, expression, purification and characterization of an isotype of clytin, a calcium-binding photoprotein from the luminous hydromedusa Clytia gregarium. , 2008, Journal of biochemistry.

[22]  Keiji Hirose,et al.  Determination of Binding Constants , 2007 .

[23]  O. Shimomura Bioluminescence: Chemical Principles and Methods , 2006 .

[24]  J. Rossier,et al.  Calcium dependence of aequorin bioluminescence dissected by random mutagenesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Markova,et al.  Calcium-regulated photoproteins of marine coelenterates , 2006, Molecular Biology.

[26]  Zhi-jie Liu,et al.  Crystal structure of obelin after Ca2+-triggered bioluminescence suggests neutral coelenteramide as the primary excited state. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Kretsinger,et al.  Evolution of EF-hand calcium-modulated proteins. IV. Exon shuffling did not determine the domain compositions of EF-hand Proteins , 1993, Journal of Molecular Evolution.

[28]  J. Rose,et al.  All three Ca2+‐binding loops of photoproteins bind calcium ions: The crystal structures of calcium‐loaded apo‐aequorin and apo‐obelin , 2005, Protein science : a publication of the Protein Society.

[29]  S. Markova,et al.  Interchange of aequorin and obelin bioluminescence color is determined by substitution of one active site residue of each photoprotein , 2005, FEBS letters.

[30]  E. Vysotski,et al.  Ca2+‐Regulated Photoproteins: Structural Insight into the Bioluminescence Mechanism , 2004 .

[31]  J. Rose,et al.  Crystal Structure of a Ca2+-discharged Photoprotein , 2004, Journal of Biological Chemistry.

[32]  E. Vysotski,et al.  Ca2+-regulated photoproteins: structural insight into the bioluminescence mechanism. , 2004, Accounts of chemical research.

[33]  J. Rose,et al.  Atomic resolution structure of obelin: soaking with calcium enhances electron density of the second oxygen atom substituted at the C2-position of coelenterazine. , 2003, Biochemical and biophysical research communications.

[34]  Konstantin A Lukyanov,et al.  A colourless green fluorescent protein homologue from the non-fluorescent hydromedusa Aequorea coerulescens and its fluorescent mutants. , 2003, The Biochemical journal.

[35]  J. Rose,et al.  Violet bioluminescence and fast kinetics from W92F obelin: structure-based proposals for the bioluminescence triggering and the identification of the emitting species. , 2003, Biochemistry.

[36]  Jun Zhang,et al.  Bioluminescence of Aequorea macrodactyla, a Common Jellyfish Species in the East China Sea , 2002, Marine Biotechnology.

[37]  S. Markova,et al.  Obelin from the bioluminescent marine hydroid Obelia geniculata: cloning, expression, and comparison of some properties with those of other Ca2+-regulated photoproteins. , 2002, Biochemistry.

[38]  J. Rose,et al.  Preparation and X-ray crystallographic analysis of recombinant obelin crystals diffracting to beyond 1.1 A. , 2001, Acta crystallographica. Section D, Biological crystallography.

[39]  V. Bondar,et al.  ALL THREE CALCIUM-BINDING SITES PARTICIPATE IN THE REGULATION OF OBELIN LUMINESCENCE , 2001 .

[40]  Osamu Shimomura,et al.  The crystal structure of the photoprotein aequorin at 2.3 Å resolution , 2000, Nature.

[41]  V. Bondar,et al.  Recombinant obelin: cloning and expression of cDNA purification, and characterization as a calcium indicator. , 2000, Methods in enzymology.

[42]  V. Bondar,et al.  Sequence of the cDNA encoding the Ca(2+)-activated photoprotein obelin from the hydroid polyp Obelia longissima. , 1995, Gene.

[43]  S. Inouye,et al.  Cloning, expression and sequence analysis of cDNA for the Ca2+‐binding photoprotein, mitrocomin , 1993, FEBS letters.

[44]  S. Inouye,et al.  Cloning and sequence analysis of cDNA for the Ca2+‐activated photoprotein, clytin , 1993, FEBS letters.

[45]  M. Ohashi,et al.  Two excited states in aequorin bioluminescence induced by tryptophan modification , 1992, FEBS letters.

[46]  Y. Anraku,et al.  Monitoring of intracellular calcium in Saccharomyces cerevisiae with an apoaequorin cDNA expression system. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[47]  M. J. Cormier,et al.  Sequence comparisons of complementary DNAs encoding aequorin isotypes. , 1987, Biochemistry.

[48]  Y Sakaki,et al.  Cloning and sequence analysis of cDNA for the luminescent protein aequorin. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[49]  M. J. Cormier,et al.  Cloning and expression of the cDNA coding for aequorin, a bioluminescent calcium-binding protein. , 1985, Biochemical and biophysical research communications.

[50]  D. Stephenson,et al.  Studies on the luminescent response of the Ca2+-activated photoprotein, obelin. , 1981, Biochimica et biophysica acta.

[51]  O. Shimomura,et al.  Peroxidized coelenterazine, the active group in the photoprotein aequorin. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[52]  C. Ashley,et al.  The effect of physiologically occurring cations upon aequorin light emission. Determination of the binding constants. , 1977, Biochimica et biophysica acta.

[53]  D. Allen,et al.  Aequorin luminescence: relation of light emission to calcium concentration--a calcium-independent component. , 1977, Science.

[54]  O. Shimomura,et al.  Regeneration of the photoprotein aequorin , 1975, Nature.

[55]  J. W. Hastings,et al.  Response of Aequorin Bioluminescence to Rapid Changes in Calcium Concentration , 1969, Nature.

[56]  E. B. Ridgway,et al.  Calcium transients in single muscle fibers. , 1967, Biochemical and biophysical research communications.