Bioluminescence imaging: Basics and practical limitations

Methods in Molecular Biology

Volumn 1098, Issue , 2014, Pages 1-18

  Badr, Christian E ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bioluminescence; Imaging; Luciferase; Lux; Photoprotein

Indexed keywords

AEQUORIN; PHOTOPROTEIN;

ARTICLE; BIOLUMINESCENCE; CALCIUM CELL LEVEL; COPEPOD; CYTOTOXICITY; DECARBOXYLATION; GAUSSIA PRINCEPS; MEDICAL RESEARCH; MOLECULAR IMAGING; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; RENILLA RENIFORMIS;

ANIMALS; HUMANS; LUMINESCENT AGENTS; LUMINESCENT MEASUREMENTS; MOLECULAR IMAGING;

EID: 84934444664     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-62703-718-1_1     Document Type: Article

References (83)

1. Massoud TF, Gambhir SS (2003) Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev 17(5):545-580
2. Weissleder R, Pittet MJ (2008) Imaging in the era of molecular oncology. Nature 452(7187): 580-589
3. Contag CH, Bachmann MH (2002) Advances in in vivo bioluminescence imaging of gene expression. Annu Rev Biomed Eng 4: 235-260
4. O'Brien MA, Daily WJ, Hesselberth PE, Moravec RA, Scurria MA, Klaubert DH, Bulleit RF, Wood KV (2005) Homogeneous, bioluminescent protease assays: caspase-3 as a model. J Biomol Screen 10(2):137-148
5. Ketteler R, Sun Z, Kovacs KF, He WW, Seed B (2008) A pathway sensor for genome-wide screens of intracellular proteolytic cleavage. Genome Biol 9(4):R64
6. Mizushima N, Kuma A (2008) Autophagosomes in GFP-LC3 transgenic mice. Methods Mol Biol 445:119-124
7. Azadniv M, Dugger K, Bowers WJ, Weaver C, Crispe IN (2007) Imaging CD8+ T cell dynamics in vivo using a transgenic luciferase reporter. Int Immunol 19(10):1165-1173. doi: dxm086 [pii] 10.1093/intimm/dxm086
8. Baumjohann D, Lutz MB (2006) Non-invasive imaging of dendritic cell migration in vivo. Immunobiology 211(6-8):587-597
9. Nishijo K, Hosoyama T, Bjornson CR, Schaffer BS, Prajapati SI, Bahadur AN, Hansen MS, Blandford MC, McCleish AT, Rubin BP, Epstein JA, Rando TA, Capecchi MR, Keller C (2009) Biomarker system for studying muscle, stem cells, and cancer in vivo. FASEB J 23(8):2681-2690. doi: fj.08-128116 [pii] 10.1096/fj.08-128116
10. Shah K, Bureau E, Kim DE, Yang K, Tang Y, Weissleder R, Breakefi eld XO (2005) Glioma therapy and real-time imaging of neural precursor cell migration and tumor regression. Ann Neurol 57(1):34-41. doi: 10.1002/ana.20306
11. Zhao H, Tang C, Cui K, Ang BT, Wong ST (2009) A screening platform for glioma growth and invasion using bioluminescence imaging. Laboratory investigation. J Neurosurg 111(2): 238-246. doi: 10.3171/2008.8.JNS08644 10.3171/2008.8.JNS08644 [pii]
12. Livingston JN (1999) Genetically engineered mice in drug development. J Intern Med 245(6):627-635
13. Iyer M, Sato M, Johnson M, Gambhir SS, Wu L (2005) Applications of molecular imaging in cancer gene therapy. Curr Gene Ther 5(6): 607-618
14. Rome C, Couillaud F, Moonen CT (2007) Gene expression and gene therapy imaging. Eur Radiol 17(2):305-319
15. Shimomura O (1985) Bioluminescence in the sea: photoprotein systems. Symp Soc Exp Biol 39:351-372
16. Johnson FH, Shimomura O (1972) Enzymatic and nonenzymatic bioluminescence. Photophysiology 7:275-334
17. Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purifi cation and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59:223-239
18. Head JF, Inouye S, Teranishi K, Shimomura O (2000) The crystal structure of the photoprotein aequorin at 2.3 A resolution. Nature 405(6784):372-376. doi: 10.1038/35012659
19. Shimomura O, Johnson FH, Morise H (1974) Mechanism of the luminescent intramolecular reaction of aequorin. Biochemistry 13(16): 3278-3286
20. Baubet V, Le Mouellic H, Campbell AK, Lucas-Meunier E, Fossier P, Brulet P (2000) Chimeric green fl uorescent protein-aequorin as bioluminescent Ca2+ reporters at the singlecell level. Proc Natl Acad Sci U S A 97(13): 7260-7265
21. Meighen EA (1994) Genetics of bacterial bioluminescence. Annu Rev Genet 28:117-139. doi: 10.1146/annurev.ge.28.120194.001001
22. Meighen EA (1991) Molecular biology of bacterial bioluminescence. Microbiol Rev 55(1): 123-142
23. Close DM, Patterson SS, Ripp S, Baek SJ, Sanseverino J, Sayler GS (2010) Autonomous bioluminescent expression of the bacterial luciferase gene cassette (lux) in a mammalian cell line. PloS One 5(8):e12441. doi: 10.1371/ journal.pone.0012441
24. Hollis RP, Lagido C, Pettitt J, Porter AJ, Killham K, Paton GI, Glover LA (2001) Toxicity of the bacterial luciferase substrate, n-decyl aldehyde, to Saccharomyces cerevisiae and Caenorhabditis elegans. FEBS Lett 506(2): 140-142
25. de Wet JR, Wood KV, DeLuca M, Helinski DR, Subramani S (1987) Firefl y luciferase gene: structure and expression in mammalian cells. Mol Cell Biol 7(2):725-737
26. Ando YNK, Yamada N, Enomoto T, Irie T, Kubota H, Ohmiya Y, Akiyama H (2008) Firefl y bioluminescence quantum yield and colour change by pH-sensitive green emission. Nat Photonics 2:44-47
27. de Wet JR, Wood KV, Helinski DR, DeLuca M (1985) Cloning of fi refl y luciferase cDNA and the expression of active luciferase in Escherichia coli. Proc Natl Acad Sci U S A 82(23):7870-7873
28. Lembert N, Idahl LA (1995) Regulatory effects of ATP and luciferin on fi refl y luciferase activity. Biochem J 305(Pt 3):929-933
29. Paroo Z, Bollinger RA, Braasch DA, Richer E, Corey DR, Antich PP, Mason RP (2004) Validating bioluminescence imaging as a highthroughput, quantitative modality for assessing tumor burden. Mol Imaging 3(2):117-124
30. Bhaumik S, Gambhir SS (2002) Optical imaging of Renilla luciferase reporter gene expression in living mice. Proc Natl Acad Sci U S A 99(1):377-382
31. Matthews JC, Hori K, Cormier MJ (1977) Purifi cation and properties of Renilla reniformis luciferase. Biochemistry 16(1):85-91
32. Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefi eld XO (2005) Codonoptimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol Ther 11(3):435-443
33. Wurdinger T, Badr C, Pike L, de Kleine R, Weissleder R, Breakefi eld XO, Tannous BA (2008) A secreted luciferase for ex vivo monitoring of in vivo processes. Nat Methods 5(2):171-173. doi: 10.1038/nmeth.1177
34. Markova SV, Golz S, Frank LA, Kalthof B, Vysotski ES (2004) Cloning and expression of cDNA for a luciferase from the marine copepod Metridia longa. A novel secreted bioluminescent reporter enzyme. J Biol Chem 279(5): 3212-3217. doi: 10.1074/jbc.M309639200
35. Thompson EM, Nagata S, Tsuji FI (1989) Cloning and expression of cDNA for the luciferase from the marine ostracod Vargula hilgendorfi i. Proc Natl Acad Sci U S A 86(17): 6567-6571
36. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fl uorescent proteins. Nat Methods 2(12):905-909. doi: 10.1038/ nmeth819
37. Branchini BR, Ablamsky DM, Murtiashaw MH, Uzasci L, Fraga H, Southworth TL (2007) Thermostable red and green light- producing fi refl y luciferase mutants for bioluminescent reporter applications. Anal Biochem 361(2): 253-262. doi: 10.1016/j.ab.2006.10.043
38. Loening AM, Wu AM, Gambhir SS (2007) Red-shifted Renilla reniformis luciferase variants for imaging in living subjects. Nat Methods 4(8):641-643
39. Degeling MH, Maguire CA, Bovenberg MS, Tannous BA (2012) Sensitive assay for mycoplasma detection in mammalian cell culture. Anal Chem 84(9):4227-4232. doi: 10.1021/ ac2033112
40. Maguire CA, Deliolanis NC, Pike L, Niers JM, Tjon-Kon-Fat LA, Sena-Esteves M, Tannous BA (2009) Gaussia luciferase variant for highthroughput functional screening applications. Anal Chem 81(16):7102-7106. doi: 10.1021/ ac901234r
41. Maguire CA, Bovenberg MS, Crommentuijn MH, Niers JM, Kerami M, Teng J, Sena- Esteves M, Badr CE, Tannous BA (2013) Triple bioluminescence imaging for in vivo monitoring of cellular processes. Mol Ther Nucleic Acids (in press)
42. Badr CE, Tannous BA (2011) Bioluminescence imaging: progress and applications. Trends Biotechnol 29(12):624-633. doi: 10.1016/j. tibtech.2011.06.010
43. Tannous BA, Teng J (2011) Secreted blood reporters: insights and applications. Biotechnol Adv 29(6):997-1003. doi: 10.1016/j. biotechadv.2011.08.021
44. Chung E, Yamashita H, Au P, Tannous BA, Fukumura D, Jain RK (2009) Secreted Gaussia luciferase as a biomarker for monitoring tumor progression and treatment response of systemic metastases. PloS One 4(12):e8316. doi: 10.1371/journal.pone.0008316
45. Griesenbach U, Vicente CC, Roberts MJ, Meng C, Soussi S, Xenariou S, Tennant P, Baker A, Baker E, Gordon C, Vrettou C, McCormick D, Coles R, Green AM, Lawton AE, Sumner- Jones SG, Cheng SH, Scheule RK, Hyde SC, Gill DR, Collie DD, McLachlan G, Alton EW (2011) Secreted Gaussia luciferase as a sensitive reporter gene for in vivo and ex vivo studies of airway gene transfer. Biomaterials 32(10):2614- 2624. doi: 10.1016/j.biomaterials.2010.12.001
46. Lupold SE, Johnson T, Chowdhury WH, Rodriguez R (2012) A real time Metridia luciferase based non-invasive reporter assay of mammalian cell viability and cytotoxicity via the beta-actin promoter and enhancer. PloS One 7(5):e36535. doi: 10.1371/journal.pone. 0036535
47. Hiramatsu N, Kasai A, Meng Y, Hayakawa K, Yao J, Kitamura M (2005) Alkaline phosphatase vs luciferase as secreted reporter molecules in vivo. Anal Biochem 339(2):249-256. doi: 10.1016/j.ab.2005.01.023
48. Fan F, Wood KV (2007) Bioluminescent assays for high-throughput screening. Assay Drug Dev Technol 5(1):127-136. doi: 10.1089/adt. 2006.053
49. Czupryna J, Tsourkas A (2011) Firefl y luciferase and RLuc8 exhibit differential sensitivity to oxidative stress in apoptotic cells. PloS One 6(5):e20073. doi: 10.1371/journal.pone. 0020073
50. Moriyama EH, Niedre MJ, Jarvi MT, Mocanu JD, Moriyama Y, Subarsky P, Li B, Lilge LD, Wilson BC (2008) The infl uence of hypoxia on bioluminescence in luciferase-transfected gliosarcoma tumor cells in vitro. Photochem Photobiol Sci 7(6):675-680. doi: 10.1039/ b719231b
51. Zhang Y, Bressler JP, Neal J, Lal B, Bhang HE, Laterra J, Pomper MG (2007) ABCG2/BCRP expression modulates D-Luciferin based bioluminescence imaging. Cancer Res 67(19):9389- 9397. doi: 10.1158/0008-5472.CAN-07-0944
52. Pichler A, Prior JL, Piwnica-Worms D (2004) Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. Proc Natl Acad Sci U S A 101(6):1702-1707. doi: 10.1073/pnas.0304326101
53. Berger F, Paulmurugan R, Bhaumik S, Gambhir SS (2008) Uptake kinetics and biodistribution of 14C-D-luciferin-a radiolabeled substrate for the fi refl y luciferase catalyzed bioluminescence reaction: impact on bioluminescence based reporter gene imaging. Eur J Nucl Med Mol Imaging 35(12):2275-2285. doi: 10.1007/s00259-008-0870-6
54. Lin MC, Li JJ, Wang EJ, Princler GL, Kauffman FC, Kung HF (1997) Ethanol down-regulates the transcription of microsomal triglyceride transfer protein gene. Faseb J 11(13): 1145-1152
55. Stratowa C, Audette M (1995) Transcriptional regulation of the human intercellular adhesion molecule-1 gene: a short overview. Immunobiology 193(2-4):293-304
56. Ueda T, Akiyama N, Sai H, Oya N, Noda M, Hiraoka M, Kizaka-Kondoh S (2001) c-IAP2 is induced by ionizing radiation through NF-kappaB binding sites. FEBS Lett 491(1-2): 40-44
57. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J (1994) Mechanism of activation of the TGF-beta receptor. Nature 370(6488): 341-347
58. Herbst KJ, Allen MD, Zhang J (2009) The cAMP-dependent protein kinase inhibitor H-89 attenuates the bioluminescence signal produced by Renilla Luciferase. PloS One 4(5):e5642. doi: 10.1371/journal.pone. 0005642
59. Zhou S, Zawel L, Lengauer C, Kinzler KW, Vogelstein B (1998) Characterization of human FAST-1, a TGF beta and activin signal transducer. Mol Cell 2(1):121-127
60. Ciana P, Raviscioni M, Mussi P, Vegeto E, Que I, Parker MG, Lowik C, Maggi A (2003) In vivo imaging of transcriptionally active estrogen receptors. Nat Med 9(1):82-86, 10.1038/ nm809 nm809 [pii]
61. von Bulow GU, Bram RJ (1997) NF-AT activation induced by a CAML-interacting member of the tumor necrosis factor receptor superfamily. Science 278(5335):138-141
62. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857- 868, S0092-8674(00)80595-4 [pii]
63. Durocher D, Charron F, Warren R, Schwartz RJ, Nemer M (1997) The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors. Embo J 16(18):5687-5696
64. Macian F, Garcia-Rodriguez C, Rao A (2000) Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. Embo J 19(17):4783-4795
65. Phippard D, Manning AM (2003) Screening for inhibitors of transcription factors using luciferase reporter gene expression in transfected cells. Methods Mol Biol 225:19-23
66. Tran H, Brunet A, Grenier JM, Datta SR, Fornace AJ Jr, DiStefano PS, Chiang LW, Greenberg ME (2002) DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296(5567):530-534
67. Svensson RU, Barnes JM, Rokhlin OW, Cohen MB, Henry MD (2007) Chemotherapeutic agents up-regulate the cytomegalovirus promoter: implications for bioluminescence imaging of tumor response to therapy. Cancer Res 67(21):10445-10454. doi: 10.1158/0008- 5472.CAN-07-1955
68. Badr CE, Niers JM, Tjon-Kon-Fat LA, Noske DP, Wurdinger T, Tannous BA (2009) Realtime monitoring of nuclear factor kappaB activity in cultured cells and in animal models. Mol Imaging 8(5):278-290
69. Hingorani M, White CL, Zaidi S, Merron A, Peerlinck I, Gore ME, Nutting CM, Pandha HS, Melcher AA, Vile RG, Vassaux G, Harrington KJ (2008) Radiation-mediated up- regulation of gene expression from replication- defective adenoviral vectors: implications for sodium iodide symporter gene therapy. Clin Cancer Res 14(15):4915-4924. doi: 10.1158/1078-0432.CCR-07-4049
70. Harms JS, Oliveira SC, Splitter GA (1999) Regulation of transgene expression in genetic immunization. Braz J Med Biol Res 32(2): 155-162
71. O'Neill K, Lyons SK, Gallagher WM, Curran KM, Byrne AT (2010) Bioluminescent imaging: a critical tool in pre-clinical oncology research. J Pathol 220(3):317-327. doi: 10.1002/path. 2656
72. Edinger M, Cao YA, Hornig YS, Jenkins DE, Verneris MR, Bachmann MH, Negrin RS, Contag CH (2002) Advancing animal models of neoplasia through in vivo bioluminescence imaging. Eur J Cancer 38(16):2128-2136
73. Curtis A, Calabro K, Galarneau JR, Bigio IJ, Krucker T (2011) Temporal variations of skin pigmentation in C57BL/6 mice affect optical bioluminescence quantitation. Mol Imaging Biol 13(6):1114-1123. doi: 10.1007/s11307- 010-0440-8
74. Branchini BR, Southworth TL, Khattak NF, Michelini E, Roda A (2005) Red- and greenemitting fi refl y luciferase mutants for bioluminescent reporter applications. Anal Biochem 345(1):140-148, S0003-2697(05)00532-4 [pii] 10.1016/j.ab.2005.07.015
75. Caysa H, Jacob R, Muther N, Branchini B, Messerle M, Soling A (2009) A redshifted codon-optimized fi refl y luciferase is a sensitive reporter for bioluminescence imaging. Photochem Photobiol Sci 8(1):52-56. doi: 10.1039/b814566k
76. Thorne N, Shen M, Lea WA, Simeonov A, Lovell S, Auld DS, Inglese J (2012) Firefl y luciferase in chemical biology: a compendium of inhibitors, mechanistic evaluation of chemotypes, and suggested use as a reporter. Chem Biol 19(8):1060- 1072. doi: 10.1016/j.chembiol.2012.07.015
77. Auld DS, Thorne N, Nguyen DT, Inglese J (2008) A specifi c mechanism for nonspecifi c activation in reporter-gene assays. ACS Chem Biol 3(8):463-470. doi: 10.1021/cb8000793
78. Pang YP, Park JG, Wang S, Vummenthala A, Mishra RK, McLaughlin JE, Di R, Kahn JN, Tumer NE, Janosi L, Davis J, Millard CB (2011) Small-molecule inhibitor leads of ribosome- inactivating proteins developed using the doorstop approach. PloS One 6(3):e17883. doi: 10.1371/journal.pone.0017883
79. Auld DS, Lovell S, Thorne N, Lea WA, Maloney DJ, Shen M, Rai G, Battaile KP, Thomas CJ, Simeonov A, Hanzlik RP, Inglese J (2010) Molecular basis for the high-affi nity binding and stabilization of fi refl y luciferase by PTC124. Proc Natl Acad Sci U S A 107(11): 4878-4883. doi: 10.1073/pnas.0909141107
80. Auld DS, Thorne N, Maguire WF, Inglese J (2009) Mechanism of PTC124 activity in cellbased luciferase assays of nonsense codon suppression. Proc Natl Acad Sci U S A 106(9):3585-3590. doi: 10.1073/ pnas.0813345106
81. Badr CE, Hewett JW, Breakefi eld XO, Tannous BA (2007) A highly sensitive assay for monitoring the secretory pathway and ER stress. PloS One 2(6):e571. doi: 10.1371/journal. pone.0000571
82. Keyaerts M, Remory I, Caveliers V, Breckpot K, Bos TJ, Poelaert J, Bossuyt A, Lahoutte T (2012) Inhibition of fi refl y luciferase by general anesthetics: effect on in vitro and in vivo bioluminescence imaging. PloS One 7(1):e30061. doi: 10.1371/journal.pone.0030061
83. Feng Y, Mitchison TJ, Bender A, Young DW, Tallarico JA (2009) Multi-parameter phenotypic profi ling: using cellular effects to characterize small-molecule compounds. Nat Rev Drug Discov 8(7):567-578