[en] Bioluminescence is the production of visible light by living organisms. It occurs through the oxidation of luciferin substrates catalysed by luciferase enzymes. Auxiliary proteins, such as fluorescent proteins and luciferin-binding proteins, can modify the light emitted wavelength or stabilize reactive luciferin molecules, respectively. Additionally, calcium ions are crucial for the luminescence across various species. Despite the large phylogenetic distribution of bioluminescent organisms, only a few systems have been comprehensively studied. Notably, cnidarian species of the Renilla genus utilize a coelenterazine-dependent luciferase, a calcium-dependent coelenterazine-binding protein and a green fluorescent protein. We investigated the bioluminescence of three sea pen species: Pennatula phosphorea, Anthoptilum murrayi and Funiculina quadrangularis (Pennatuloidea, Anthozoa). Their light-emission spectra reveal peaks at 510, 513 and 485 nm, respectively. A coelenterazine-based reaction was demonstrated in all three species. Using transcriptome analyses, we identified transcripts coding for luciferases, green fluorescent proteins and coelenterazine-binding proteins for P. phosphorea and A. murrayi. Immunodetection confirmed the expression of luciferase in P. phosphorea and F. quadrangularis. We also expressed recombinant luciferase of A. murrayi, confirming its activity. We highlighted the role of calcium ions in bioluminescence, possibly associated with the mechanism of substrate release at the level of coelenterazine-binding proteins. The study proposes a model for anthozoan bioluminescence, offering new avenues for future ecological and functional research on these luminous organisms.
Duchatelet, Laurent ; Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Walloon Brabant, Belgium
Galeazzo, Gabriela A; Departamento de Oceanografia Física, Química e Geológica, Universidade de São Paulo, Sao Paulo, Brazil
Coubris, Constance; Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Walloon Brabant, Belgium
Bridoux, Laure; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Louvain-la-Neuve, Walloon Brabant, Belgium
Rezsohazy, René; Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Louvain-la-Neuve, Walloon Brabant, Belgium
Melo, Marcelo R S; Departamento de Oceanografia Biológica, Universidade de São Paulo, Sao Paulo, Brazil
Marek, Milan; International Clinical Research Center, Masaryk University, Brno, Czech Republic
Amaral, Danilo T; Centre for Natural and Human Sciences, Universidade Federal do ABC, Santo Andre, Brazil
Dupont, Sam; Biological and Environmental Sciences, Goteborgs Universitet, Goteborg, Sweden ; International Atomic Energy Agency Marine Environment Laboratories, Monaco, Monaco
Garbuglio de Oliveira, Anderson; Department of Chemistry and Biochemistry, Yeshiva University, New York, NY, USA
Delroisse, Jérôme ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Biochimie et biologie moléculaire ; Marine Organisms and Biomimetics, Université de Mons, Mons, Belgium
Language :
English
Title :
Insights into the bioluminescence systems of three sea pens (Cnidaria: Anthozoa): from de novo transcriptome analyses to biochemical assays.
H2020 - 730984 - ASSEMBLE Plus - Association of European Marine Biological Laboratories Expanded
Funders :
F.R.S.-FNRS - Belgian National Fund for Scientific Research FAPESP - Fundação de Amparo à Pesquisa do Estado de São Paulo Czech Science Foundation EU - European Union Czech Ministry of Education, Youth, and Sports CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior
Funding text :
This work was supported by an FRS-FNRS grant (T.0169.20) awarded to the Universit\u00E9 de Louvain\u2014UCLouvain Marine Biology Laboratory and the Universit\u00E9 de Mons Biology of Marine Organisms and Biomimetics Laboratory, by the Czech Science Foundation (GA22-09853S) and by the Czech Ministry of Education, Youth and Sports (RECETOX RI LM2023069, e-INFRALM2018140). The research leading to these results also received funding from the European Union\u2019s Horizon 2020 research and innovation programme under grant agreement no. 730984, ASSEMBLE Plus project. This study was financed in part by the Coordena\u00E7\u00E3o de Aperfei\u00E7oamento de Pessoal de N\u00EDvel Superior\u2014Brasil (CAPES)\u2014Finance Code 88887.605088/2021-00, Funda\u00E7\u00E3o de Amparo \u00E0 Pesquisa do Estado de S\u00E3o Paulo (FAPESP 2017/12909-4, 2020/07600-7) and Yeshiva University Start-up Fund. Acknowledgements
Shimomura O, Yampolsky I. 2019 Bioluminescence: chemical principles and methods, 3rd. edn. Singapore: World Scientific Publishing.
Haddock S, Moline M, Case J. 2010 Bioluminescence in the sea. Annu. Rev. Mar. Sci 2, 443-493. (doi:10.1146/annurev-marine-120308-081028)
Delroisse J, Duchatelet L, Flammang P, Mallefet J. 2021 Leaving the dark side? Insights into the evolution of luciferases. Front. Mar. Sci. 8, 673620. (doi:10.3389/fmars.2021.673620)
Fleiss A, Sarkisyan KS. 2019 A brief review of bioluminescent systems (2019). Curr. Genet. 65, 877-882. (doi:10.1007/s00294-019-00951-5)
Hastings JW. 1996 Chemistries and colors of bioluminescent reactions: a review. Gene 173, 5-11. (doi:10.1016/0378-1119(95)00676-1)
Wilson T, Hastings J. 2012 Bioluminescence: living lights, lights for living. Cambridge, MA: Harvard University Press.
Kaskova ZM, Tsarkova AS, Yampolsky IV. 2016 1001 lights: luciferins, luciferases, their mechanisms of action and applications in chemical analysis, biology and medicine. Chem. Soc. Rev. 45, 6048-6077. (doi:10.1039/c6cs00296j)
Duchatelet L, Dupont S. 2024 Marine eukaryote bioluminescence: a review of species and their functional biology. Mar. Life Sci. Technol. (doi:10.1007/s42995-024-00250-0)
Cormier MJ. 1960 Studies of the bioluminescence of Renilla reniformis. Biochim. Biophys. Acta 42, 333-343. (doi:10.1016/0006-3002(60)90797-6)
Matthews JC, Hori K, Cormier MJ. 1977 Purification and properties of Renilla reniformis luciferase. Biochemistry 16, 85-91. (doi:10.1021/bi00620a014)
Lorenz WW, McCann RO, Longiaru M, Cormier MJ. 1991 Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc. Natl Acad. Sci. USA 88, 4438-4442. (doi:10.1073/pnas.88.10.4438)
Schenkmayerova A et al,. 2023 Catalytic mechanism for Renilla-type luciferases. Nat. Catal. 6, 23-38. (doi:10.1038/s41929-022-00895-z)
Inoue S, Kakoi H, Murata M, Goto T, Shimomura O. 1977 Complete structure of Renilla luciferin and luciferyl sulfate. Tetrahedron Lett. 18, 2685-2688. (doi:10.1016/s0040-4039(01)83046-x)
Loening AM, Fenn TD, Gambhir SS. 2007 Crystal structures of the luciferase and green fluorescent protein from Renilla reniformis. J. Mol. Biol. 374, 1017-1028. (doi:10.1016/j.jmb.2007.09.078)
Bessho-Uehara M, Francis WR, Haddock SHD. 2020 Biochemical characterization of diverse deep-sea anthozoan bioluminescence systems. Mar. Biol. 167, 114. (doi:10.1007/s00227-020-03706-w)
DeLeo DM, Bessho-Uehara M, Haddock SHD, McFadden CS, Quattrini AM. 2024 Evolution of bioluminescence in anthozoa with emphasis on octocorallia. Proc. R. Soc. B 291, 20232626. (doi:10.1098/rspb.2023.2626)
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. (doi:10.1002/jcp.1040810218)
Delroisse J, Ullrich-Lüter E, Blaue S, Ortega-Martinez O, Eeckhaut I, Flammang P, Mallefet J. 2017 A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence. Open Biol. 7, 160300. (doi:10.1098/rsob.160300)
Tessler M et al,. 2020 A putative chordate luciferase from a cosmopolitan tunicate indicates convergent bioluminescence evolution across phyla. Sci. Rep. 10, 17724. (doi:10.1038/s41598-020-73446-w)
Lau ES et al,. 2024 Functional characterization of luciferase in a brittle star indicates parallel evolution influenced by genomic availability of haloalkane dehalogenase. BioRxiv. (doi:10.1101/2024.10.14.618359)
Anderson J, Charbonneau H, Cormier M. 1974 Mechanism of calcium induction of Renilla bioluminescence. Involvement of a calcium-triggered luciferin binding protein. Biochemistry 13, 1195-1200. (doi:10.1021/bi00703a602)
Ward WW, Cormier MJ. 1979 An energy transfer protein in coelenterate bioluminescence. Characterization of the Renilla green-fluorescent protein. J. Biol. Chem. 254, 781-788. (doi:10.1016/s0021-9258(17)37873-0)
Kumar S, Harrylock M, Walsh KA, Cormier MJ, Charbonneau H. 1990 Amino acid sequence of the Ca 2+ -triggered luciferin binding protein of Renilla reniformis. FEBS Lett. 268, 287-290. (doi:10.1016/0014-5793(90)81029-n)
Inouye S. 2007 Expression, purification and characterization of calcium-triggered luciferin-binding protein of Renilla reniformis. Protein Expr. Purif. 52, 66-73. (doi:10.1016/j.pep.2006.07.028)
Titushin MS, Markova SV, Frank LA, Malikova NP, Stepanyuk GA, Lee J, Vysotski ES. 2008 Coelenterazine-binding protein of Renilla muelleri: cDNA cloning, overexpression, and characterization as a substrate of luciferase. Photochem. Photobiol. Sci. 7, 189-196. (doi:10.1039/b713109g)
Ogoh K, Kinebuchi T, Murai M, Takahashi T, Ohmiya Y, Suzuki H. 2013 Dual-color-emitting green fluorescent protein from the sea cactus Cavernularia obesa and its use as a pH indicator for fluorescence microscopy. Luminescence 28, 582-591. (doi:10.1002/bio.2497)
Henry JP, Ninio M. 1978 Control of the Ca 2+ -triggered bioluminescence of Veretillum cynomorium lumisomes. Biochim. Biophys. Acta 504, 40-59. (doi:10.1016/0005-2728(78)90005-1)
Charbonneau H, Cormier MJ. 1979 Ca 2+ -induced bioluminescence in Renilla reniformis. Purification and characterization of a calcium-triggered luciferin-binding protein. J. Biol. Chem. 254, 769-780. (doi:10.1016/s0021-9258(17)37872-9)
Stepanyuk GA, Liu ZJ, Vysotski ES, Lee J, Rose JP, Wang BC. 2009 Structure based mechanism of the Ca 2+ -induced release of coelenterazine from the Renilla binding protein. Proteins 74, 583-593. (doi:10.1002/prot.22173)
Nicol JAC. 1955 Observations on luminescence in Renilla (Pennatulacea). J. Exp. Biol. 32, 32. (doi:10.1242/jeb.32.2.299)
Davenport D, Nicol J. 1956 Observations on luminescence in sea pens (Pennatulacea). Proc. R. Soc. B 144, 480-496. (doi:10.1098/rspb.1956.0005)
Wampler JE, Karkhanis YD, Morin JG, Cormier MJ. 1973 Similarities in the bioluminescence from the Pennatulacea. Biochim. Biophys. Acta 314, 104-109. (doi:10.1016/0005-2728(73)90068-6)
Satterlie RA, Anderson PAV, Case JF. 1980 Colonial coordination in anthozoans: Pennatulacea. Mar. Behav. Physiol. 7, 25-46. (doi:10.1080/10236248009386969)
Germain G, Anctil M. 1988 Luminescent activity and ultrastructural characterization of photocytes dissociated from the coelenterate Renilla köllikeri. Tissue Cell 20, 701-720. (doi:10.1016/0040-8166(88)90017-1)
Anctil M, Boulay D, Larivière L. 1982 Monoaminergic mechanisms associated with control of luminescence and contractile activities in the coelenterate, Renilla köllikeri. J. Exp. Zool. 223, 11-24. (doi:10.1002/jez.1402230103)
Duchatelet L, Coubris C, Pels C, Dupont ST, Mallefet J. 2023 Catecholamine involvement in the bioluminescence control of two species of anthozoans. Life 13, 1798. (doi:10.3390/life13091798)
Morin JG. 1976 Probable functions of bioluminescence in the Pennatulacea (Cnidaria, Anthozoa).. In Coelenterate ecology and behavior (. ed. GO Mackie),. pp. 629-638. Boston, MA: Springer. (doi:10.1007/978-1-4757-9724-4_65)
Delroisse J, Mallefet J, Flammang P. 2016 De novo adult transcriptomes of two European brittle stars: spotlight on opsin-based photoreception. PLoS ONE 11, e0152988. (doi:10.1371/journal.pone.0152988)
Delroisse J, Duchatelet L, Flammang P, Mallefet J. 2018 De novo transcriptome analyses provide insights into opsin-based photoreception in the lanternshark Etmopterus spinax. PLoS ONE 13, e0209767. (doi:10.1371/journal.pone.0209767)
Delroisse J, Duchatelet L, Flammang P, Mallefet J. 2021 Photophore distribution and enzymatic diversity within the photogenic integument of the cookie-cutter shark Isistius brasiliensis (Chondrichthyes: Dalatiidae). Front. Mar. Sci. 8, 627045. (doi:10.3389/fmars.2021.627045)
Cock PJA, Fields CJ, Goto N, Heuer ML, Rice PM. 2010 The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res. 38, 1767-1771. (doi:10.1093/nar/gkp1137)
Grabherr MG et al,. 2011 Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652. (doi:10.1038/nbt.1883)
Pertea G et al,. 2003 TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19, 651-652. (doi:10.1093/bioinformatics/btg034)
Das S, Shyamal S, Durica DS. 2016 Analysis of annotation and differential expression methods used in RNA-seq studies in crustacean systems. Integr. Comp. Biol. 56, 1067-1079. (doi:10.1093/icb/icw117)
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990 Basic local alignment search tool. J. Mol. Biol. 215, 403-410. (doi:10.1016/s0022-2836(05)80360-2)
Buchfink B, Xie C, Huson DH. 2014 Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60. (doi:10.1038/nmeth.3176)
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005 Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676. (doi:10.1093/bioinformatics/bti610)
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. 2005 InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116-W120. (doi:10.1093/nar/gki442)
Haas BJ et al,. 2013 De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512. (doi:10.1038/nprot.2013.084)
Kearse M et al,. 2012 Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649. (doi:10.1093/bioinformatics/bts199)
Woo J, Howell MH, von Arnim AG. 2009 Structure-function studies on the active site of the coelenterazine-dependent luciferase from Renilla. Protein Sci. 17, 725-735. (doi:10.1110/ps.073355508)
Labas YA, Gurskaya NG, Yanushevich YG, Fradkov AF, Lukyanov KA, Lukyanov SA, Matz MV. 2002 Diversity and evolution of the green fluorescent protein family. Proc. Natl Acad. Sci. USA 99, 4256-4261. (doi:10.1073/pnas.062552299)
Alieva NO et al,. 2008 Diversity and evolution of coral fluorescent proteins. PLoS ONE 3, e2680. (doi:10.1371/journal.pone.0002680)
Li G, Zhang QJ, Zhong J, Wang YQ. 2009 Evolutionary and functional diversity of green fluorescent proteins in cephalochordates. Gene 446, 41-49. (doi:10.1016/j.gene.2009.07.003)
Shagin DA et al,. 2004 GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity. Mol. Biol. Evol. 21, 841-850. (doi:10.1093/molbev/msh079)
Schnitzler CE et al,. 2012 Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol. 10, 107. (doi:10.1186/1741-7007-10-107)
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009 trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973. (doi:10.1093/bioinformatics/btp348)
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. 2015 IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274. (doi:10.1093/molbev/msu300)
Posada D, Crandall KA. 1998 MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818. (doi:10.1093/bioinformatics/14.9.817)
Nicol J. 1958 Observations on the luminescence of Pennatula phosphorea, with a note on the luminescence of Virgularia mirabilis. J. Mar. Biol. Assoc. UK 37, 551-563. (doi:10.1017/S0025315400005610)
Rahnama S, Saffar B, Kahrani ZF, Nazari M, Emamzadeh R. 2017 Super RLuc8: a novel engineered Renilla luciferase with a red-shifted spectrum and stable light emission. Enzym. Microb. Technol. 96, 60-66. (doi:10.1016/j.enzmictec.2016.09.009)
Khoshnevisan G, Emamzadeh R, Nazari M, Rasa SMM, Sariri R, Hassani L. 2018 Kinetics, structure, and dynamics of Renilla luciferase solvated in binary mixtures of glycerol and water and the mechanism by which glycerol obstructs the enzyme emitter site. Int. J. Biol. Macromol. 117, 617-624. (doi:10.1016/j.ijbiomac.2018.05.160)
Mallefet J, Duchatelet L, Coubris C. 2020 Bioluminescence induction in the ophiuroid Amphiura filiformis (Echinodermata). J. Exp. Biol. 223, jeb218719. (doi:10.1242/jeb.218719)
Mallefet J, Martinez-Soares P, Eléaume M, O'Hara T, Duchatelet L. 2023 New insights on crinoid (Echinodermata; Crinoidea) bioluminescence. Front. Mar. Sci. 10, 1136138. (doi:10.3389/fmars.2023.1136138)
Loening AM. 2006 Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. Protein Eng. Des. Sel. 19, 391-400. (doi:10.1093/protein/gzl023)
Nandi A, Zhang A, Chu ZT, Xie WJ, Xu Z, Dong S, Warshel A. 2024 Exploring the light-emitting agents in Renilla luciferases by an effective QM/MM approach. J. Am. Chem. Soc. 146, 13875-13885. (doi:10.1021/jacs.4c00963)
Tsuji FI, Ohmiya Y, Fagan TF, Toh H, Inouye S. 1995 Molecular evolution of the Ca 2+ -binding photoproteins of the Hydrozoa. Photochem. Photobiol. 62, 657-661. (doi:10.1111/j.1751-1097.1995.tb08713.x)
Powers ML, McDermott AG, Shaner NC, Haddock SHD. 2013 Erratum to 'Expression and characterization of the calcium-activated photoprotein from the ctenophore Bathocyroe fosteri: insights into light-sensitive photoproteins'. Biochem. Biophys. Res. Commun. 435, 751. (doi:10.1016/j.bbrc.2008.07.166)
Burakova LP, Stepanyuk GA, Eremeeva EV, Vysotski ES. 2016 Role of certain amino acid residues of the coelenterazine-binding cavity in bioluminescence of light-sensitive Ca 2+ -regulated photoprotein berovin. Photochem. Photobiol. Sci. 15, 691-704. (doi:10.1039/c6pp00050a)
Burakova LP, Vysotski ES. 2019 Recombinant Ca 2+ -regulated photoproteins of ctenophores: current knowledge and application prospects. Appl. Microbiol. Biotechnol. 103, 5929-5946. (doi:10.1007/s00253-019-09939-0)
Jumper J et al,. 2021 Highly accurate protein structure prediction with AlphaFold. Nature 596, 583-589. (doi:10.1038/s41586-021-03819-2)
Abramson J et al,. 2024 Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature 630, 493-500. (doi:10.1038/s41586-024-07487-w)
Stepanyuk GA, Liu ZJ, Markova SS, Frank LA, Lee J, Vysotski ES, Wang BC. 2008 Crystal structure of coelenterazine-binding protein from Renilla muelleri at 1.7 Å: why it is not a calcium-regulated photoprotein. Photochem. Photobiol. Sci. 7, 442-447. (doi:10.1039/b716535h)
Buskey EJ, Stearns DE. 1991 The effects of starvation on bioluminescence potential and egg release of the copepod Metridia longa. J. Plankton Res. 13, 885-893. (doi:10.1093/plankt/13.4.885)
Thomson CM, Herring PJ, Campbell AK. 1995 Evidence for de novo biosynthesis of coelenterazine in the bioluminescent midwater shrimp, Systellaspis debilis C. J. Mar. Biol. Assoc. UK 75, 165-171. (doi:10.1017/s0025315400015277)
Oba Y, Kato S ichi, Ojika M, Inouye S. 2009 Biosynthesis of coelenterazine in the deep-sea copepod, Metridia pacifica. Biochem. Biophys. Res. Commun. 390, 684-688. (doi:10.1016/j.bbrc.2009.10.028)
Bessho-Uehara M, Huang W, Patry WL, Browne WE, Weng JK, Haddock SHD. 2020 Evidence for de novo biosynthesis of the luminous substrate coelenterazine in ctenophores. iScience 23, 101859. (doi:10.1016/j.isci.2020.101859)
Francis WR, Shaner NC, Christianson LM, Powers ML, Haddock SHD. 2015 Occurrence of isopenicillin-N-synthase homologs in bioluminescent ctenophores and implications for coelenterazine biosynthesis. PLoS ONE 10, e0128742. (doi:10.1371/journal.pone.0128742)
Haddock SH, Rivers TJ, Robison BH. 2001 Can coelenterates make coelenterazine? Dietary requirement for luciferin in cnidarian bioluminescence. Proc. Natl Acad. Sci. USA 98, 11148-11151. (doi:10.1073/pnas.201329798)
Herring PJ. 1991 Observations on bioluminescence in some deep-water anthozoans.. In Coelenterate biology: recent research on Cnidaria and Ctenophora (eds RB Williams, PFS Cornelius, RG Hughes, EA Robson),. pp. 573-579. Dordrecht, The Netherlands: Springer. (doi:10.1007/978-94-011-3240-4_80)
Coubris C, Duchatelet L, Delroisse J, Bayaert WS, Parise L, Eloy MC, Pels C, Mallefet J. 2024 Maintain the light, long-term seasonal monitoring of luminous capabilities in the brittle star Amphiura filiformis. Sci. Rep. 14, 13238. (doi:10.1038/s41598-024-64010-x)
Herring PJ. 1978 Bioluminescence of invertebrates other than insects.. In Bioluminescence in action (ed PJ Herring),. pp. 199-240. London, UK: Academic Press.
Inouye S, Watanabe K, Nakamura H, Shimomura O. 2000 Secretional luciferase of the luminous shrimp Oplophorus gracilirostris: cDNA cloning of a novel imidazopyrazinone luciferase. FEBS Lett. 481, 19-25. (doi:10.1016/s0014-5793(00)01963-3)
Kobilka B. 1992 Adrenergic receptors as models for G protein-coupled receptors. Annu. Rev. Neurosci. 15, 87-114. (doi:10.1146/annurev.ne.15.030192.000511)
Neves SR, Ram PT, Iyengar R. 2002 G protein pathways. Science 296, 1636-1639. (doi:10.1126/science.1071550)
Brown AM, Birnbaumer L. 1988 Direct G protein gating of ion channels. Am. J. Physiol. Heart Circ. Physiol. 254, H401-H410. (doi:10.1152/ajpheart.1988.254.3.h401)
Hille B. 1994 Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci. 17, 531-536. (doi:10.1016/0166-2236(94)90157-0)
Dolphin AC. 2003 G protein modulation of voltage-gated calcium channels. Pharmacol. Rev. 55, 607-627. (doi:10.1124/pr.55.4.3)
Tedford HW, Zamponi GW. 2006 Direct G protein modulation of Cav2 calcium channels. Pharmacol. Rev. 58, 837-862. (doi:10.1124/pr.58.4.11)
Roda A, Pasini P, Mirasoli M, Michelini E, Guardigli M. 2004 Biotechnological applications of bioluminescence and chemiluminescence. Trends Biotechnol. 22, 295-303. (doi:10.1016/j.tibtech.2004.03.011)
Kirkpatrick A, Xu T, Ripp S, Sayler G, Close D. 2019 Biotechnological advances in luciferase enzymes.. In Bioluminescence: analytical applications and basic biology (. ed. S Hirobumi),. pp. 1-23. London, UK: IntechOpen. (doi:10.5772/intechopen.85313)
Welsh DK, Kay SA. 2005 Bioluminescence imaging in living organisms. Curr. Opin. Biotechnol. 16, 73-78. (doi:10.1016/j.copbio.2004.12.006)
Kudryavtsev AN, Krasitskaya VV, Efremov MK, Zangeeva SV, Rogova AV, Tomilin FN, Frank LA. 2023 Ca 2+ -triggered coelenterazine-binding protein Renilla expected and unexpected features. Int. J. Mol. Sci. 24, 2144. (doi:10.3390/ijms24032144)
Duchatelet L, Galeazzo GA, Coubris C, Bridoux L, Rezsohazy R, Melo MRS et al,. 2025 Supplementary material from: Insights into the bioluminescence systems of three sea pens (Cnidaria: Anthozoa): from de novo transcriptome analyses to biochemical assays. Figshare. (doi:10.6084/m9.figshare.c.7735482)