Bioluminescence as a tool in molecular biology
Katarzyna Pajor 1 , Daniel Sypniewski 1 , Ilona Bednarek 1Abstract
Bioluminescence has been studied for many years by scientists. There are numerous mechanisms of that phenomenon; among them bacterial bioluminescence is the most frequently found in nature. This type of bioluminescence is determined by the appearance of lux operon, which encodes all elements necessary to produce light emission and it does not require any additional substrates supply. Another commonly found example of bioluminescence mechanism is performed by Photinus pyralis. Luciferase of P. pyralis named FLuc requires D-luciferin as a substrate. Bioluminescence is also characteristic for many deep-sea organisms. Most of them are based on oxidation reaction of coelenterazine to coelenteramide mediated by RLuc or GLuc luciferases. Due to the variety of bioluminescence mechanisms in nature, it has become possible to apply them in many sensitive methods that can be used in molecular biology and medicine. The most significant application of bioluminescence is BLI (bioluminescence imaging). This method is cheap and nontoxic which allows both in vitro and in vivo imaging. BLI applications include, e.g. protein-protein interactions, stem cells labeling, tracking of viral, bacterial, fungal and parasitical infections, and carcinogenesis analyses. Bioluminescence has also been used in the creation of modified cell systems capable of light emission in response to certain analytes and thus very sensitive biosensors have been generated. Other important areas of bioluminescence application are immunoassays, ATP assays, and BART analysis (bioluminescent assay in Real-Time) – a very sensitive technique which allows scientists to estimate nucleic acids amplification.
References
- 1. Allard S.T.: Systemy genów reporterowych opartych na zjawisku bioluminescencji. Postępy Biochem., 2008; 54: 350-353
Google Scholar - 2. Badr C.E., Tannous B.A.: Bioluminescence imaging: progress and applications. Trends Biotechnol., 2011; 29: 624-633
Google Scholar - 3. Bakayan A., Domingo B., Miyawaki A., Llopis J.: Imaging Ca2+ activity in mammalian cells and zebrafish with a novel-red emitting aequorin variant. Pflügers Arch., 2015; 467: 2031-2042
Google Scholar - 4. Bergner T., Tabib C.R., Winkler A., Stipsits S., Kayer H., Lee J., Malthouse J.P., Mayhew S., Müller F., Gruber K., Macheroux P.: Structural and biochemical properties of LuxF from Photobacterium leiognathi. Biochim. Biophys. Acta, 2015; 1854: 1466-1475
Google Scholar - 5. Biron K.: Fireflies, dead fish and a glowing bunny: a primer on bioluminescence. BioTeach J., 2003; 1: 19-26
Google Scholar - 6. Close D.M., Patterson S.S., Ripp S., Baek S.J., Sanseverino J., Sayler G.S.: Autonomous bioluminescent expression of the bacterial luciferase gene cassette (lux) in a mammalian cell line. PLoS One, 2010; 5: e12441
Google Scholar - 7. Close D.M., Ripp S., Sayler G.S.: Reporter proteins in whole-cell optical bioreporter detection systems, biosensor integrations, and biosensing apllications. Sensors, 2009; 9: 9147-9174
Google Scholar - 8. Close D.M., Xu T., Sayler G.S., Ripp S.: In vivo bioluminescent imaging (BLI): noninvasive visualization and interrogation of biological processes in living animals. Sensors, 2011; 11: 180-206
Google Scholar - 9. Coleman S.M., McGregor A.: A bright future for bioluminescent imaging in viral research. Future Virol., 2015; 10: 169-183
Google Scholar - 10. da Ros M., Iorio A.L., Consolante D., Cardile F., Muratori M., Fantappiè O., Lucchesi M., Guidi M., Pisano C., Sardi I.: Morphine modulates doxorubicin uptake and improves efficacy of chemotherapy in an intracranial xenograft model of human glioblastoma. Am. J. Cancer Res., 2016; 6: 639-648
Google Scholar - 11. de Almeida P.E., van Rappard J.R., Wu J.C.: In vivo bioluminescence for tracking cell fate and function. Am. J. Physiol. Heart Circ. Physiol., 2011; 301: 663-671
Google Scholar - 12. Donat S., Hasenberg M., Schäfer T., Ohlsen K., Gunzer M., Einsele H., Löffler J., Beilhack A., Krappmann S.: Surface display of Gaussia princeps luciferase allows sensitive fungal pathogen detection during cutaneous aspergillosis. Virulence, 2012; 3: 51-61
Google Scholar - 13. Dragulescu-Andrasi A., Chan C.T., De A., Massoud T.F., Gambhir S.S.: Bioluminescence resonance energy transfer (BRET) imaging of protein-protein interactions within deep tissues of living subjects. Proc. Natl. Acad. Sci. USA, 2011; 108: 12060-12065
Google Scholar - 14. Fan F., Wood K.V.: Bioluminescent assays for high-throughput screening. Assay Drug Dev. Technol., 2007; 5: 127-136
Google Scholar - 15. Francis K.P., Joh D., Bellinger-Kawahara C., Hawkinson M.J., Purchio T.F., Contag P.R.: Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect. Immun., 2000; 68: 3594-3600
Google Scholar - 16. Franke-Fayard B., Janse C.J., Cunha-Rodrigues M., Ramesar J., Büscher P., Que I., Löwik C., Voshol P.J., den Boer M.A., van Duinen S.G., Febbraio M., Mota M.M., Waters A.P.: Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc. Natl. Acad. Sci. USA, 2005; 102: 11468-11473
Google Scholar - 17. Funakoshi S., Miki K., Takaki T., Okubo C., Hatani T., Chonabayashi K., Nishikawa M., Takei I., Oishi A., Narita M., Hoshijima M., Kimura T., Yamanaka S., Yoshida Y.: Enhanced engrafment, proliferation, and therapeutic potential in heart using optimized human iPSC-derived cardiomyocytes. Sci. Rep., 2016; 6: 19111
Google Scholar - 18. Gandelman O.A., Church V.L., Moore C.A., Kiddle G., Carne C.A., Parmar S., Jalal H., Tisi L.C., Murray J.A.: Novel bioluminescent quantitative detection of nucleic acid amplification in real-time. PLoS One, 2010; 5: e14155
Google Scholar - 19. Haddock S.H., Moline M.A., Case J.F.: Bioluminescence in the sea. Ann. Rev. Mar. Sci., 2010; 2: 443-493
Google Scholar - 20. Hastings J.W.: Circadian rhythms in Dinoflagellates: what is the purpose of synthesis and destruction of proteins? Microorganisms, 2013; 1: 26-32
Google Scholar - 21. Huang N.F., Okogbaa J., Babakhanyan A., Cooke J.P.: Bioluminescence imaging of stem cell-based therapeutics for vascular regeneration. Theranostics, 2012; 2: 346-354
Google Scholar - 22. Hutchens M., Luker G.D.: Applications of bioluminescence imaging to the study of infectious diseases. Cell. Microbiol., 2007; 9: 2315-2322
Google Scholar - 23. Hwang D.W., Park K.M., Shim H.K., Jin Y., Oh H.J., Oh S.W., Lee S., Youn H., Joung Y.K., Lee H.J., Kim S.U., Park K.D., Lee D.S.: In vivo bioluminescence imaging for viable human neural stem cells incorporated within in situ gelatin hydrogels. EJNMMI Res., 2014; 4: 61
Google Scholar - 24. Kajigaya N., Hirose Y., Koike S., Fujita T., Yokota N., Hata S., Ikenaga M., Kobayashi N., Takahashi T.: Assessment of contamination using an ATP bioluminescence assay on doorknobs in a university-affiliated hospital in Japan. BMC Res Notes., 2015; 8: 352
Google Scholar - 25. Kim J.B., Urban K., Cochran E., Lee S., Ang A., Rice B., Bata A., Campbell K., Coffee R., Gorodinsky A., Lu Z., Zhou H., Kishimoto T.K., Lassota P.: Non-invasive detection of a small number of bioluminescent cancer cells in vivo. PLoS One, 2010; 5: e9364
Google Scholar - 26. Luker K.E., Luker G.D.: Applications of bioluminescence imaging to antiviral research and therapy: multiple luciferase enzymes and quantitation. Antiviral Res., 2008; 78: 179-187
Google Scholar - 27. Luker K.E., Luker G.D.: Bioluminescence imaging of reporter mice for studies of infection and inflammation. Antiviral Res., 2010; 86: 93-100
Google Scholar - 28. McMillin D.W., Delmore J., Weisberg E., Negri J.M., Geer D.C., Klippel S., Mitsiades N., Schlossman R.L., Munshi N.C., Kung A.L., Griffin J.D., Richardson P.G., Anderson K.C., Mitsiades C.S.: Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity. Nat. Med., 2010; 16: 483-489
Google Scholar - 29. Niers J.M., Kerami M., Pike L., Lewandrowski G., Tannous B.A.: Multimodal in vivo imaging and blood monitoring of intrinsic and extrinsic apoptosis. Mol. Ther., 2011; 19: 1090-1096
Google Scholar - 30. Prescher J.A., Contag C.H.: Guided by the light: visualizing biomolecular processes in living animals with bioluminescence. Curr. Opin. Chem. Biol., 2010; 14: 80-89
Google Scholar - 31. Rasooly R., Do P., Hernlem B.: Sensitive, rapid, quantitative and in vitro method for the detection of biologically active staphylococcal enterotoxin type E. Toxins, 2016; 8: E150
Google Scholar - 32. Roda A., Guardigli M.: Analytical chemiluminescence and bioluminescence: latest achievements and new horizons. Anal. Bioanal. Chem., 2012; 402: 69-76
Google Scholar - 33. Roda A., Guardigli M., Michelini E., Mirasoli M.: Bioluminescence in analytical chemistry and in vivo imaging. Trends Analyt. Chem., 2009; 28: 307- 322
Google Scholar - 34. Roda A., Mirasoli M., Michelini E., Di Fusco M., Zangheri M., Cevenini L., Roda B., Simoni P.: Progress in chemical luminescence-based biosensors: a critical review. Biosens. Bioelectron., 2016; 76: 164-179
Google Scholar - 35. Roda A., Pasini P., Mirasoli M., Michelini E., Guardigli M.: Biotechnological applications of bioluminescence and chemiluminescence. Trends Biotechnol., 2004; 22: 295-303
Google Scholar - 36. Rougeaux C., Becher F., Ezan E., Tournier J.N., Goossens P.L.: In vivo dynamics of active edema and lethal factors during anthrax. Sci. Rep., 2016; 6: 23346
Google Scholar - 37. Saeij J.P., Boyle J.P., Grigg M.E., Arrizabalaga G., Boothroyd J.C.: Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect. Immun., 2005; 73: 695-702
Google Scholar - 38. Stevani C.V., Oliveira A.G., Mendes L.F., Ventura F.F., Waldenmaier H.E., Carvalho R.P., Pereira T.A.: Current status of research on fungal bioluminescence: biochemistry and prospects for ecotoxicological application. Photochem. Photobiol., 2013; 89: 1318-1326
Google Scholar - 39. Turner P.C., McLennan A.G., Bates A.D., White M.R.: Organizacja klonowanych genów. W: Biologia Molekularna. Krótkie wykłady. Wydawnictwo Naukowe PWN, Warszawa 2007, 200-203
Google Scholar - 40. Valiadi M., Iglesias-Rodriguez D.: Understanding bioluminescence in Dinoflagellates – how far have we come? Microorganisms, 2013; 1: 3-25
Google Scholar - 41. Vantaggiato C., Dell’Omo G., Ramachandran B., Manni I., Radaelli E., Scanziani E., Piaggio G., Maggi A., Ciana P.: Bioluminescence imaging of estrogen receptor activity during breast cancer progression. Am. J. Nucl. Med. Mol. Imaging, 2016; 6: 32-41
Google Scholar - 42. Welsh D.K., Kay S.A.: Bioluminescence imaging in living organisms. Curr. Opin. Biotechnol., 2005; 16: 73-78
Google Scholar - 43. Wiles S., Clare S., Harker J., Huett A., Young D., Dougan G., Frankel G.: Organ specifity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell. Microbiol., 2004; 6: 963-972
Google Scholar - 44. Wiles S., Dougan G., Frankel G.: Emergence of a ‘hyperinfectious’ bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell. Microbiol., 2005; 7: 1163-1172
Google Scholar - 45. Wong J.M., Pérez-Moreno J.L., Chan T.Y., Frank T.M., Bracken-Grissom H.D.: Phylogenetic and transcriptomic analyses reveal the evolution of bioluminescence and light detection in marine deep-sea shrimps of the family Oplophoridae (Crustacea: Decapoda). Mol. Phylogenet. Evol., 2015; 83: 278-292
Google Scholar - 46. Wu N., Rathnayaka T., Kuroda Y.: Bacterial expression and re-engineering of Gaussia princeps luciferase and its use as a reporter protein. Biochim. Biophys. Acta, 2015; 1854: 1392-1399
Google Scholar - 47. Xia Z., Rao J.: Biosensing and imaging based on bioluminescence resonance energy transfer. Curr. Opin. Biotechnol., 2009; 20: 37-44
Google Scholar