Recombinant Ca2+-regulated photoproteins of ctenophores: current knowledge and application prospects
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.
KeywordsBioluminescence Coelenterazine Photoinactivation Intracellular calcium
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.
Compliance with ethical standards
This article does not contain any studies with human participants performed by any of the authors.
Conflict of interest
The authors declare that they have no competing interests.
- 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 30:566–574CrossRefGoogle 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 162:286–297CrossRefGoogle Scholar
- Frank LA, Krasitskaya VV (2014) Application of enzyme bioluminescence for medical diagnostics. Adv Biochem Eng Biotechnol 144:175–197Google Scholar
- Golz S, Markova S, Burakova L, Frank L, Vysotski E (2005a) Isolated berovin photoprotein and use thereof, WO 2005021591-A1 (Patent)Google Scholar
- Golz S, Markova S, Burakova L, Frank L, Vysotski E (2005b) Isolated photoprotein bolinopsin, and the use thereof, WO/2005/000885 (Patent)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 7:197–207CrossRefGoogle 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 326:911–913Google 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 82:3154–3158Google 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 413:164–170Google 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 99–102CrossRefGoogle 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):2085–2093Google 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 115–118CrossRefGoogle 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 10:107CrossRefGoogle 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 19–41Google Scholar
- Wilson T, Hastings JW (2013) Bioluminescence: living lights, lights for living. Harvard University Press, CambridgeGoogle Scholar