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Recombinant Ca2+-regulated photoproteins of ctenophores: current knowledge and application prospects

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Abstract

Bright bioluminescence of ctenophores is conditioned by Ca2+-regulated photoproteins. Although they share many properties characteristic of hydromedusan Ca2+-regulated photoproteins responsible for light emission of marine animals belonging to phylum Cnidaria, a substantial distinction still exists. The ctenophore photoproteins appeared to be extremely sensitive to light—they lose the ability for bioluminescence on exposure to light over the entire absorption spectrum. Inactivation is irreversible because keeping the inactivated photoprotein in the dark does not recover its activity. The capability to emit light can be restored only by incubation of inactivated photoprotein with coelenterazine in the dark at alkaline pH in the presence of oxygen. Although these photoproteins were discovered many years ago, only the cloning of cDNAs encoding these unique bioluminescent proteins in the early 2000s has provided a new impetus for their studies. To date, cDNAs encoding Ca2+-regulated photoproteins from four different species of luminous ctenophores have been cloned. The amino acid sequences of ctenophore photoproteins turned out to completely differ from those of hydromedusan photoproteins (identity less than 29%) though also similar to them having three EF-hand Ca2+-binding sites. At the same time, these photoproteins reveal the same two-domain scaffold characteristic of hydromedusan photoproteins. This review is an attempt to systemize and critically evaluate the data scattered through various articles regarding the structural features of recombinant light-sensitive Ca2+-regulated photoproteins of ctenophores and their bioluminescent and physicochemical properties as well as to compare them with those of hydromedusan photoproteins. In addition, we also discuss the prospects of their biotechnology applications.

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References

  • Aghamaali MR, Jafarian V, Sariri R, Molakarimi M, Rasti B, Taghdir M, Sajedi RH, Hosseinkhani S (2011) Cloning, sequencing, expression and structural investigation of mnemiopsin from Mnemiopsis leidyi: an attempt toward understanding Ca2+-regulated photoproteins. Protein J 30:566–574

    Article  CAS  PubMed  Google Scholar 

  • Allen DG, Blinks JR, Prendergast FG (1977) Aequorin luminescence: relation of light emission to calcium concentration—a calcium-independent component. Science 195:996–998

    Article  CAS  PubMed  Google Scholar 

  • Alonso MT, Rodríguez-Prados M, Navas-Navarro P, Rojo-Ruiz J, García-Sancho J (2017) Using aequorin probes to measure Ca2+ in intracellular organelles. Cell Calcium 64:3–11

    Article  CAS  PubMed  Google Scholar 

  • Anctil M, Shimomura O (1984) Mechanism of photoinactivation and re-activation in the bioluminescence system of the ctenophore Mnemiopsis. Biochemistry 221:269–272

    Article  CAS  Google Scholar 

  • Blinks JR, Wier WG, Hess P, Prendergast FG (1982) Measurement of Ca2+ concentrations in living cells. Prog Biophys Mol Biol 40:1–114

    Article  CAS  PubMed  Google Scholar 

  • Bonora M, Giorgi C, Bononi A, Marchi S, Patergnani S, Rimessi A, Rizzuto R, Pinton P (2013) Subcellular calcium measurements in mammalian cells using jellyfish photoprotein aequorin-based probes. Nat Protoc 8:2105–2118

    Article  CAS  PubMed  Google Scholar 

  • Burakova LP, Natashin PV, Markova SV, Eremeeva EV, Malikova NP, Cheng C, Liu ZJ, Vysotski ES (2016a) Mitrocomin from the jellyfish Mitrocoma cellularia with deleted C-terminal tyrosine reveals a higher bioluminescence activity compared to wild type photoprotein. J Photochem Photobiol B 162:286–297

    Article  CAS  PubMed  Google Scholar 

  • Burakova LP, Natashin PV, Malikova NP, Niu F, Pu M, Vysotski ES, Liu ZJ (2016b) All Ca2+-binding loops of light-sensitive ctenophore photoprotein berovin bind magnesium ions: the spatial structure of Mg2+-loaded apo-berovin. J Photochem Photobiol B 154:57–66

    Article  CAS  PubMed  Google Scholar 

  • Burakova LP, Stepanyuk GA, Eremeeva EV, Vysotski ES (2016c) Role of certain amino acid residues of the coelenterazine-binding cavity in bioluminescence of light-sensitive Ca2+-regulated photoprotein berovin. Photochem Photobiol Sci 15:691–704

    Article  CAS  PubMed  Google Scholar 

  • Casey JR, Grinstein S, Orlowski J (2010) Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11:50–61

    Article  CAS  PubMed  Google Scholar 

  • Cormier MJ, Hori K, Karkhanis YD, Anderson JM, Wampler JE, Morin JG, Hastings JW (1973) Evidence for similar biochemical requirements for bioluminescence among the coelenterates. J Cell Physiol 81:291–297

    Article  CAS  PubMed  Google Scholar 

  • Deng L, Markova SV, Vysotski ES, Liu ZJ, Lee J, Rose J, Wang BC (2004) Crystal structure of a Ca2+-discharged photoprotein: implications for mechanisms of the calcium trigger and bioluminescence. J Biol Chem 279:33647–33652

    Article  CAS  PubMed  Google Scholar 

  • Deng L, Vysotski ES, Markova SV, Liu ZJ, Lee J, Rose J, Wang BC (2005) All three Ca2+-binding loops of photoproteins bind calcium ions: the crystal structures of calcium-loaded apo-aequorin and apo-obelin. Protein Sci 14:663–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doi I, Kuse M, Nishikawa T, Isobe M (2009) Selective protein modification by the hydroperoxide intermediate in a photoprotein, aequorin. Bioorg Med Chem 17:3399–3404

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Vysotski ES (2017) Bioluminescent and biochemical properties of Cys-free Ca2+-regulated photoproteins obelin and aequorin. J Photochem Photobiol B 174:97–105

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Vysotski ES (2019) Exploring bioluminescence function of the Ca2+-regulated photoproteins with site-directed mutagenesis. Photochem Photobiol 95:8–23

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Markova SV, Westphal AH, Visser AJ, van Berkel WJ, Vysotski ES (2009) The intrinsic fluorescence of apo-obelin and apo-aequorin and use of its quenching to characterize coelenterazine binding. FEBS Lett 583:1939–1944

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Markova SV, van Berkel WJ, Vysotski ES (2013a) Role of key residues of obelin in coelenterazine binding and conversion into 2-hydroperoxy adduct. J Photochem Photobiol B 127:133–139

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Markova SV, Frank LA, Visser AJ, van Berkel WJ, Vysotski ES (2013b) Bioluminescent and spectroscopic properties of His-Trp-Tyr triad mutants of obelin and aequorin. Photochem Photobiol Sci 12:1016–1024

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Natashin PV, Song L, Zhou Y, van Berkel WJ, Liu ZJ, Vysotski ES (2013c) Oxygen activation of apo-obelin-coelenterazine complex. ChemBioChem 14:739–745

    Article  CAS  PubMed  Google Scholar 

  • Eremeeva EV, Bartsev SI, van Berkel WJ, Vysotski ES (2017) Unanimous model for describing the fast bioluminescence kinetics of Ca2+-regulated photoproteins of different organisms. Photochem Photobiol 93:495–502

    Article  CAS  PubMed  Google Scholar 

  • Fagan TF, Ohmiya Y, Blinks JR, Inouye S, Tsuji FI (1993) Cloning, expression and sequence analysis of cDNA for the Ca2+-binding photoprotein, mitrocomin. FEBS Lett 333:301–305

    Article  CAS  PubMed  Google Scholar 

  • Fourrage C, Swann K, Gonzalez Garcia JR, Campbell AK, Houliston E (2014) An endogenous green fluorescent protein-photoprotein pair in Clytia hemisphaerica eggs shows co-targeting to mitochondria and efficient bioluminescence energy transfer. Open Biol 4:130206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank LA, Krasitskaya VV (2014) Application of enzyme bioluminescence for medical diagnostics. Adv Biochem Eng Biotechnol 144:175–197

    CAS  PubMed  Google Scholar 

  • Ghanbarlou MR, Shirdel SA, Jafarian V, Khalifeh K (2018) Molecular mechanisms governing the evolutionary conservation of glycine in the 6th position of loops ΙΙΙ and ΙV in photoprotein mnemiopsin 2. J Photochem Photobiol B 187:18–24

    Article  CAS  Google Scholar 

  • Gifford JL, Walsh MP, Vogel HJ (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix–loop–helix EF-hand motifs. Biochem J 405:199–221

    Article  CAS  PubMed  Google Scholar 

  • Golz S, Markova S, Burakova L, Frank L, Vysotski E (2005a) Isolated berovin photoprotein and use thereof, WO 2005021591-A1 (Patent)

  • Golz S, Markova S, Burakova L, Frank L, Vysotski E (2005b) Isolated photoprotein bolinopsin, and the use thereof, WO/2005/000885 (Patent)

  • Haddock SHD, Case JF (1999) Bioluminescence spectra of shallow and deep-sea gelatinous zooplankton: ctenophores, medusae and siphonophores. Mar Biol 133:571–582

    Article  Google Scholar 

  • Haddock SH, Moline MA, Case JF (2010) Bioluminescence in the sea. Annu Rev Mar Sci 2:443–493

    Article  Google Scholar 

  • Hakiminia F, Khalifeh K, Sajedi RH, Ranjbar B (2016) Determination of structural elements on the folding reaction of mnemiopsin by spectroscopic techniques. Spectrochim Acta A Mol Biomol Spectrosc 158:49–55

    Article  CAS  PubMed  Google Scholar 

  • Hastings JW, Mitchell G, Mattingly PH, Blinks JR, van Leeuwen M (1969) Response of aequorin bioluminescence to rapid changes in calcium concentration. Nature 222:1047–1050

    Article  CAS  PubMed  Google Scholar 

  • Head JF, Inouye S, Teranishi K, Shimomura O (2000) The crystal structure of the photoprotein aequorin at 2.3 Å resolution. Nature 18:372–376

    Article  CAS  Google Scholar 

  • Hirano T, Takahashi Y, Kondo H, Maki S, Kojima S, Ikeda H, Niwa H (2008) The reaction mechanism for the high quantum yield of Cypridina (Vargula) bioluminescence supported by the chemiluminescence of 6-aryl-2-methylimidazo[1,2-a]pyrazin-3(7H)-ones (Cypridina luciferin analogues). Photochem Photobiol Sci 7:197–207

    Article  CAS  PubMed  Google Scholar 

  • Illarionov BA, Markova SV, Bondar VS, Vysotski ES, Gitelson JI (1992) Cloning and expression of cDNA for the Ca2+-activated photoprotein obelin from the hydroid polyp Obelia longissima. Dokl Akad Nauk 326:911–913

    CAS  Google Scholar 

  • Illarionov BA, Bondar VS, Illarionova VA, Vysotski ES (1995) Sequence of the cDNA encoding the Ca2+-activated photoprotein obelin from the hydroid polyp Obelia longissima. Gene 153:273–274

    Article  CAS  PubMed  Google Scholar 

  • Illarionov BA, Frank LA, Illarionova VA, Bondar VS, Vysotski ES, Blinks JR (2000) Recombinant obelin: cloning and expression of cDNA purification, and characterization as a calcium indicator. Methods Enzymol 305:223–249

    Article  CAS  PubMed  Google Scholar 

  • Inouye S (2008) Cloning, expression, purification and characterization of an isotype of clytin, a calcium-binding photoprotein from the luminous hydromedusa Clytia gregarium. J Biochem 143:711–717

    Article  CAS  PubMed  Google Scholar 

  • Inouye S, Tsuji FI (1993) Cloning and sequence analysis of cDNA for the Ca2+-activated photoprotein, clytin. FEBS Lett 315:343–346

    Article  CAS  PubMed  Google Scholar 

  • Inouye S, Noguchi M, Sakaki Y, Takagi Y, Miyata T, Iwanaga S, Miyata T, Tsuji FI (1985) Cloning and sequence analysis of cDNA for the luminescent protein aequorin. Proc Natl Acad Sci U S A 82:3154–3158

  • Inouye S, Zenno S, Sakaki Y, Tsuji FI (1991) High-level expression and purification of apoaequorin. Protein Expr Purif 2:122–126

    Article  CAS  PubMed  Google Scholar 

  • Jafarian V, Sariri R, Hosseinkhani S, Aghamaali M-R, Sajedi RH, Taghdir M, Hassannia S (2011) A unique EF-hand motif in mnemiopsin photoprotein from Mnemiopsis leidyi: implication for its low calcium sensitivity. BBRC 413:164–170

    CAS  PubMed  Google Scholar 

  • Jafarian V, Sajedi RH, Hosseinkhani S, Sariri R, Taghdir M, Khalifeh K, Vafa M, Aghamaali MR (2018) Structural and functional consequences of EF-hand I recovery in mnemiopsin 2. Int J Biol Macromol 118(Pt B):2006–2013

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki H, Nakayama S, Kretsinger RH (1998) Classification and evolution of EF-hand proteins. Biometals 11:277–295

    Article  CAS  Google Scholar 

  • Lee J, Glushka J, Markova SV, Vysotski ES (2001) Protein conformational changes in obelin shown by 15N-HSQC nuclear magnetic resonance. In: Case JF, Herring PJ, Robison BH, Haddock SHD, Kricka LJ, Stanley PE (eds) Bioluminescence & chemiluminescence 2000. World Scientific Publishing, Singapore, pp 99–102

    Chapter  Google Scholar 

  • Lewis JC, Daunert S (2000) Photoproteins as luminescent labels in binding assays. Fresenius J Anal Chem 366:760–768

    Article  CAS  PubMed  Google Scholar 

  • Liu ZJ, Vysotski ES, Chen CJ, Rose JP, Lee J, Wang BC (2000) Structure of the Ca2+-regulated photoprotein obelin at 1.7 Å resolution determined directly from its sulfur substructure. Protein Sci (11):2085–2093

  • Liu ZJ, Vysotski ES, Deng L, Lee J, Rose J, Wang BC (2003) Atomic resolution structure of obelin: soaking with calcium enhances electron density of the second oxygen atom substituted at the C2-position of coelenterazine. Biochem Biophys Res Commun 311:433–439

    Article  CAS  PubMed  Google Scholar 

  • Liu ZJ, Stepanyuk GA, Vysotski ES, Lee J, Markova SV, Malikova NP, Wang BC (2006) Crystal structure of obelin after Ca2+-triggered bioluminescence suggests neutral coelenteramide as the primary excited state. Proc Natl Acad Sci U S A 103:2570–2575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahdavi A, Sajedi RH, Hosseinkhani S, Taghdir M, Sariri R (2013) Site-directed mutagenesis of photoprotein mnemiopsin: implication of some conserved residues in bioluminescence properties. Photochem Photobiol Sci 12:467–478

    Article  CAS  PubMed  Google Scholar 

  • Mahdavi A, Sajedi RH, Hosseinkhani S, Taghdir M (2015) Hyperactive Arg39Lys mutated mnemiopsin: implication of positively charged residue in chromophore binding cavity. Photochem Photobiol Sci 14:792–800

    Article  CAS  PubMed  Google Scholar 

  • Malikova NP, Burakova LP, Markova SV, Vysotski ES (2014) Characterization of hydromedusan Ca2+-regulated photoproteins as a tool for measurement of Ca2+ concentration. Anal Bioanal Chem 406:5715–5726

    Article  CAS  PubMed  Google Scholar 

  • Markova SV, Vysotski ES (2015) Coelenterazine-dependent luciferases. Biochemistry (Mosc) 80:714–732

    Article  CAS  Google Scholar 

  • Markova SV, Vysotski ES, Lee J (2001) Obelin hyperexpression in E. coli, purification and characterization. In: Case JF, Herring PJ, Robison BH, Haddock SHD, Kricka LJ, Stanley PE (eds) Bioluminescence & chemiluminescence 2000. World Scientific Publishing, Singapore, pp 115–118

    Chapter  Google Scholar 

  • Markova SV, Vysotski ES, Blinks JR, Burakova LP, Wang BC, Lee J (2002) Obelin from the bioluminescent marine hydroid Obelia geniculata: cloning, expression, and comparison of some properties with those of other Ca2+-regulated photoproteins. Biochemistry 19:2227–2236

    Article  CAS  Google Scholar 

  • Markova SV, Burakova LP, Frank LA, Golz S, Korostileva KA, Vysotski ES (2010) Green-fluorescent protein from the bioluminescent jellyfish Clytia gregaria: cDNA cloning, expression, and characterization of novel recombinant protein. Photochem Photobiol Sci 9:757–765

    Article  CAS  PubMed  Google Scholar 

  • Markova SV, Burakova LP, Golz S, Malikova NP, Frank LA, Vysotski ES (2012) The light-sensitive photoprotein berovin from the bioluminescent ctenophore Beroe abyssicola: a novel type of Ca2+-regulated photoprotein. FEBS J 279:856–870

    Article  CAS  PubMed  Google Scholar 

  • Molakarimi M, Mohseni A, Taghdir M, Pashandi Z, Gorman MA, Parker MW, Naderi-Manesh H, Sajedi RH (2017) QM/MM simulations provide insight into the mechanism of bioluminescence triggering in ctenophore photoproteins. PLoS One 12:e0182317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molakarimi M, Gorman MA, Mohseni A, Pashandi Z, Taghdir M, Naderi-Manesh H, Sajedi RH, Parker MW (2019) Reaction mechanism of the bioluminescent protein mnemiopsin1 revealed by X-ray crystallography and QM/MM simulations. J Biol Chem 294:20–27

    Article  CAS  PubMed  Google Scholar 

  • Natashin PV, Markova SV, Lee J, Vysotski ES, Liu ZJ (2014a) Crystal structures of the F88Y obelin mutant before and after bioluminescence provide molecular insight into spectral tuning among hydromedusan photoproteins. FEBS J 281:1432–1445

    Article  CAS  PubMed  Google Scholar 

  • Natashin PV, Ding W, Eremeeva EV, Markova SV, Lee J, Vysotski ES, Liu ZJ (2014b) Structures of the Ca2+-regulated photoprotein obelin Y138F mutant before and after bioluminescence support the catalytic function of a water molecule in the reaction. Acta Crystallogr D 70:720–732

    Article  CAS  PubMed  Google Scholar 

  • Ohmiya Y, Hirano T (1996) Shining the light: the mechanism of the bioluminescence reaction of calcium-binding photoproteins. Chem Biol 3:337–347

    Article  CAS  PubMed  Google Scholar 

  • Pashandi Z, Molakarimi M, Sajedi RH, Taghdir M, Naderi-Manesh H (2016) Light induced structural changes of the photoprotein mnemiopsin: characterization and contribution in photoinactivation. J Photochem Photobiol B 165:133–140

    Article  CAS  PubMed  Google Scholar 

  • Powers ML, McDermott AG, Shaner N, Haddock SH (2013) Expression and characterization of the calcium-activated photoprotein from the ctenophore Bathocyroe fosteri: insights into light-sensitive photoproteins. Biochem Biophys Res Commun 431:360–366

    Article  CAS  PubMed  Google Scholar 

  • Prasher DC, McCann RO, Cormier MJ (1985) Cloning and expression of the cDNA coding for aequorin, a bioluminescent calcium-binding protein. Biochem Biophys Res Commun 15:1259–1268

    Article  Google Scholar 

  • Prasher DC, McCann RO, Longiaru M, Cormier MJ (1987) Sequence comparisons of complementary DNAs encoding aequorin isotypes. Biochemistry 26:1326–1332

    Article  CAS  PubMed  Google Scholar 

  • Prokop Z, Monincová M, Chaloupková R, Klvana M, Nagata Y, Janssen DB, Damborský J (2003) Catalytic mechanism of the maloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26. J Biol Chem 278:45094–45100

    Article  CAS  PubMed  Google Scholar 

  • Ridgway EB, Ashley CC (1967) Calcium transients in single muscle fibers. Biochem Biophys Res Commun 29:229–234

    Article  CAS  PubMed  Google Scholar 

  • Romani AM (2011) Cellular magnesium homeostasis. Arch Biochem Biophys 512:1–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnitzler CE, Pang K, Powers ML, Reitzel AM, Ryan JF, Simmons D, Tada T, Park M, Gupta J, Brooks SY, Blakesley RW, Yokoyama S, Haddock SH, Martindale MQ, Baxevanis AD (2012) Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol 10:107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimomura O (2006) Bioluminescence: chemical principles and methods. World Scientific, Singapore

    Book  Google Scholar 

  • Shimomura O, Inouye S (1999) The in situ regeneration and extraction of recombinant aequorin from Escherichia coli cells and the purification of extracted aequorin. Protein Expr Purif 16:91–95

    Article  CAS  PubMed  Google Scholar 

  • Shimomura O, Johnson FH (1972) Structure of the light-emitting moiety of aequorin. Biochemistry 11:1602–1608

    Article  CAS  PubMed  Google Scholar 

  • Shimomura O, Musicki B, Kishi Y, Inouye S (1993) Light-emitting properties of recombinant semi-synthetic aequorins and recombinant fluorescein-conjugated aequorin for measuring cellular calcium. Cell Calcium 14:373–378

    Article  CAS  PubMed  Google Scholar 

  • Stepanyuk GA, Golz S, Markova SV, Frank LA, Lee J, Vysotski ES (2005) Interchange of aequorin and obelin bioluminescence color is determined by substitution of one active site residue of each photoprotein. FEBS Lett 579:1008–1014

    Article  CAS  PubMed  Google Scholar 

  • Stepanyuk GA, Liu ZJ, Burakova LP, Lee J, Rose J, Vysotski ES, Wang BC (2013) Spatial structure of the novel light-sensitive photoprotein berovin from the ctenophore Beroe abyssicola in the Ca2+-loaded apoprotein conformation state. Biochim Biophys Acta 1834:2139–2146

    Article  CAS  PubMed  Google Scholar 

  • Strynadka NC, James MN (1989) Crystal structures of the helix–loop–helix calcium-binding proteins. Annu Rev Biochem 58:951–998

    Article  CAS  PubMed  Google Scholar 

  • Titushin MS, Feng Y, Stepanyuk GA, Li Y, Markova SV, Golz S, Wang BC, Lee J, Wang J, Vysotski ES, Liu ZJ (2010) NMR-derived topology of a GFP-photoprotein energy transfer complex. J Biol Chem 285:40891–40900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toma S, Chong KT, Nakagawa A, Teranishi K, Inouye S, Shimomura O (2005) The crystal structures of semi-synthetic aequorins. Protein Sci 14:409–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsien RY (1983) Intracellular measurements of ion activities. Annu Rev Biophys Bioeng 12:91–116

    Article  CAS  PubMed  Google Scholar 

  • Vafa M, Khalifeh K, Jafarian V (2018) Negative net charge of EF-hand loop I can affect both calcium sensitivity and substrate binding pattern in mnemiopsin 2. Photochem Photobiol Sci 17:807–814

    Article  CAS  PubMed  Google Scholar 

  • Vysotski ES, Lee J (2004) Ca2+-regulated photoproteins: structural insight into the bioluminescence mechanism. Acc Chem Res 37:405–415

    Article  CAS  PubMed  Google Scholar 

  • Vysotski ES, Lee J (2007) Bioluminescent mechanism of Ca2+-regulated photoproteins from three-dimensional structures. In: Viviani VR, Ohmiya Y (eds) Luciferases and fluorescent proteins: principles and advances in biotechnology and bioimaging. Transworld Research Network, Kerala, pp 19–41

    Google Scholar 

  • Vysotski ES, Liu ZJ, Rose J, Wang BC, Lee J (2001) Preparation and X-ray crystallographic analysis of recombinant obelin crystals diffracting to beyond 1.1 Å. Acta Crystallogr Sect D 57:1919–1921

    Article  CAS  Google Scholar 

  • Vysotski ES, Markova SV, Frank LA (2006) Calcium-regulated photoproteins of marine coelenterates. Molecular Biology 40:404–417

    Article  CAS  Google Scholar 

  • Ward WW, Seliger HH (1974a) Extraction and purification of calcium-activated photoproteins from the ctenophores Mnemiopsis sp. and Beroe ovata. Biochemistry 13:1491–1499

    Article  CAS  PubMed  Google Scholar 

  • Ward WW, Seliger HH (1974b) Properties of mnemiopsin and berovin, calcium-activated photoproteins from the ctenophores Mnemiopsis sp. and Beroe ovata. Biochemistry 13:1500–1509

    Article  CAS  PubMed  Google Scholar 

  • Ward WW, Seliger HH (1976) Action spectrum and quantum yield for the photoinactivation of mnemiopsin, a bioluminescent photoprotein from the ctenophores Mnemiopsis sp. Photochem Photobiol 23:351–363

    Article  CAS  PubMed  Google Scholar 

  • Widder EA (2010) Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328:704–708

    Article  CAS  PubMed  Google Scholar 

  • Wilson T, Hastings JW (2013) Bioluminescence: living lights, lights for living. Harvard University Press, Cambridge

    Google Scholar 

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Funding

This study was funded by the Russian Foundation for Basic Research (No. 17-04-00764) and Russian Foundation for Basic Research (No. 18-44-242001), Government of Krasnoyarsk Territory, Krasnoyarsk Regional Fund of Science, to the research project: Design of universal bioluminescent labels for immuno- and hybridization assays based on luciferases of copepods.

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  1. Photobiology Laboratory, Institute of Biophysics, Russian Academy of Sciences, Siberian Branch, Federal Research Center “Krasnoyarsk Science Center SB RAS”, Krasnoyarsk, 660036, Russia

    Lyudmila P. Burakova & Eugene S. Vysotski

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Correspondence to Eugene S. Vysotski.

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Burakova, L.P., Vysotski, E.S. Recombinant Ca2+-regulated photoproteins of ctenophores: current knowledge and application prospects. Appl Microbiol Biotechnol 103, 5929–5946 (2019). https://doi.org/10.1007/s00253-019-09939-0

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