Firefly luciferase and rluc8 exhibit differential sensitivity to oxidative stress in apoptotic cells

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Czupryna, Julie ^a   Tsourkas, Andrew ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; FIREFLY LUCIFERASE; HYDROGEN PEROXIDE; LUCIFERIN; MESSENGER RNA; PROTEASOME; REACTIVE OXYGEN METABOLITE; RENILLA LUCIFERIN 2 MONOOXYGENASE; STAUROSPORINE; PHOTOPROTEIN;

APOPTOSIS; ARTICLE; BIOLUMINESCENCE; CELL DEATH; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SPECIFICITY; FEMALE; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PHYSICAL SENSITIVITY; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN VARIANT; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STABLE EXPRESSION; WESTERN BLOTTING; DRUG EFFECT; LUMINESCENCE; METABOLISM; STANDARD; TUMOR CELL LINE;

RENILLA LUCIFERASE;

APOPTOSIS; CELL LINE, TUMOR; HUMANS; HYDROGEN PEROXIDE; LUCIFERASES, FIREFLY; LUMINESCENT MEASUREMENTS; LUMINESCENT PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 79955928897     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020073     Document Type: Article

References (43)

1. Gupta M, Copeland PR, (2007) Functional analysis of the interplay between translation termination, selenocysteine codon context, and selenocysteine insertion sequence-binding protein 2. J Biol Chem 282: 36797-36807.
2. Luo J, Lin AH, Masliah E, Wyss-Coray T, (2006) Bioluminescence imaging of Smad signaling in living mice shows correlation with excitotoxic neurodegeneration. Proc Natl Acad Sci U S A 103: 18326-18331.
3. Sohn JH, Yeh BI, Choi JW, Yoon J, Namkung J, et al. (2010) Repression of human telomerase reverse transcriptase using artificial zinc finger transcription factors. Mol Cancer Res 8: 246-253.
4. Tang Y, Shah K, Messerli SM, Snyder E, Breakefield X, et al. (2003) In vivo tracking of neural progenitor cell migration to glioblastomas. Hum Gene Ther 14: 1247-1254.
5. Jiang Y, Bernard D, Yu Y, Xie Y, Zhang T, et al. (2010) Split Renilla luciferase protein fragment-assisted complementation (SRL-PFAC) to characterize Hsp90-Cdc37 complex and identify critical residues in protein/protein interactions. J Biol Chem 285: 21023-21036.
6. Nunez G, Benedict MA, Hu Y, Inohara N, (1998) Caspases: the proteases of the apoptotic pathway. Oncogene 17: 3237-3245.
7. Sensibar JA, Liu XX, Patai B, Alger B, Lee C, (1990) Characterization of castration-induced cell death in the rat prostate by immunohistochemical localization of cathepsin D. Prostate 16: 263-276.
8. Squier MK, Miller AC, Malkinson AM, Cohen JJ, (1994) Calpain activation in apoptosis. J Cell Physiol 159: 229-237.
9. Delic J, Morange M, Magdelenat H, (1993) Ubiquitin pathway involvement in human lymphocyte gamma-irradiation-induced apoptosis. Mol Cell Biol 13: 4875-4883.
10. Bellosillo B, Villamor N, Lopez-Guillermo A, Marce S, Esteve J, et al. (2001) Complement-mediated cell death induced by rituximab in B-cell lymphoproliferative disorders is mediated in vitro by a caspase-independent mechanism involving the generation of reactive oxygen species. Blood 98: 2771-2777.
11. Law GH, Gandelman OA, Tisi LC, Lowe CR, Murray JA, (2006) Mutagenesis of solvent-exposed amino acids in Photinus pyralis luciferase improves thermostability and pH-tolerance. Biochem J 397: 305-312.
12. Baggett B, Roy R, Momen S, Morgan S, Tisi L, et al. (2004) Thermostability of firefly luciferases affects efficiency of detection by in vivo bioluminescence. Mol Imaging 3: 324-332.
13. Thompson JF, Geoghegan KF, Lloyd DB, Lanzetti AJ, Magyar RA, et al. (1997) Mutation of a protease-sensitive region in firefly luciferase alters light emission properties. J Biol Chem 272: 18766-18771.
14. Loening AM, Fenn TD, Wu AM, Gambhir SS, (2006) Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. Protein Eng Des Sel 19: 391-400.
15. Jarvis WD, Turner AJ, Povirk LF, Traylor RS, Grant S, (1994) Induction of apoptotic DNA fragmentation and cell death in HL-60 human promyelocytic leukemia cells by pharmacological inhibitors of protein kinase C. Cancer Res 54: 1707-1714.
16. Martinet W, de Meyer GR, Herman AG, Kockx MM, (2004) Reactive oxygen species induce RNA damage in human atherosclerosis. Eur J Clin Invest 34: 323-327.
17. Grune T, Reinheckel T, Davies KJ, (1997) Degradation of oxidized proteins in mammalian cells. FASEB J 11: 526-534.
18. Han YH, Kim SH, Kim SZ, Park WH, (2008) Intracellular GSH levels rather than ROS levels are tightly related to AMA-induced HeLa cell death. Chem Biol Interact 171: 67-78.
19. Preston TJ, Muller WJ, Singh G, (2001) Scavenging of extracellular H2O2 by catalase inhibits the proliferation of HER-2/Neu-transformed rat-1 fibroblasts through the induction of a stress response. J Biol Chem 276: 9558-9564.
20. Herve-Grepinet V, Veillard F, Godat E, Heuze-Vourc'h N, Lecaille F, et al. (2008) Extracellular catalase activity protects cysteine cathepsins from inactivation by hydrogen peroxide. FEBS Lett 582: 1307-1312.
21. Wu HM, Chi KH, Lin WW, (2002) Proteasome inhibitors stimulate activator protein-1 pathway via reactive oxygen species production. FEBS Lett 526: 101-105.
22. Gil J, Almeida S, Oliveira CR, Rego AC, (2003) Cytosolic and mitochondrial ROS in staurosporine-induced retinal cell apoptosis. Free Radic Biol Med 35: 1500-1514.
23. Kikuchi S, Shinpo K, Tsuji S, Takeuchi M, Yamagishi S, et al. (2003) Effect of proteasome inhibitor on cultured mesencephalic dopaminergic neurons. Brain Res 964: 228-236.
24. Alexandrova A, Petrov L, Georgieva A, Kirkova M, Kukan M, (2008) Effects of proteasome inhibitor, MG132, on proteasome activity and oxidative status of rat liver. Cell Biochem Funct 26: 392-398.
25. Grune T, Merker K, Sandig G, Davies KJ, (2003) Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem Biophys Res Commun 305: 709-718.
26. Ullrich O, Reinheckel T, Sitte N, Hass R, Grune T, et al. (1999) Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci U S A 96: 6223-6228.
27. Berlett BS, Stadtman ER, (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272: 20313-20316.
28. Kocha T, Yamaguchi M, Ohtaki H, Fukuda T, Aoyagi T, (1997) Hydrogen peroxide-mediated degradation of protein: different oxidation modes of copper- and iron-dependent hydroxyl radicals on the degradation of albumin. Biochim Biophys Acta 1337: 319-326.
29. Branchini BR, Magyar RA, Marcantonio KM, Newberry KJ, Stroh JG, et al. (1997) Identification of a firefly luciferase active site peptide using a benzophenone-based photooxidation reagent. J Biol Chem 272: 19359-19364.
30. Alter SC, DeLuca M, (1986) The sulfhydryls of firefly luciferase are not essential for activity. Biochemistry 25: 1599-1605.
31. Branchini BR, Magyar RA, Murtiashaw MH, Magnasco N, Hinz LK, et al. (1997) Inactivation of firefly luciferase with N-(iodoacetyl)-N'- (5-sulfo-1-naphthyl)ethylenediamine (I-AEDANS). Arch Biochem Biophys 340: 52-58.
32. Conti E, Stachelhaus T, Marahiel MA, Brick P, (1997) Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. EMBO J 16: 4174-4183.
33. Sala-Newby GB, Campbell AK, (1994) Stepwise removal of the C-terminal 12 amino acids of firefly luciferase results in graded loss of activity. Biochim Biophys Acta 1206: 155-160.
34. Sung D, Kang H, (1998) The N-terminal amino acid sequences of the firefly luciferase are important for the stability of the enzyme. Photochem Photobiol 68: 749-753.
35. Martinvalet D, Dykxhoorn DM, Ferrini R, Lieberman J, (2008) Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death. Cell 133: 681-692.
36. Rudolf E, Rudolf K, Cervinka M, (2008) Selenium activates p53 and p38 pathways and induces caspase-independent cell death in cervical cancer cells. Cell Biol Toxicol 24: 123-141.
37. Franke JC, Plotz M, Prokop A, Geilen CC, Schmalz HG, et al. New caspase-independent but ROS-dependent apoptosis pathways are targeted in melanoma cells by an iron-containing cytosine analogue. Biochem Pharmacol 79: 575-586.
38. Pei XY, Dai Y, Grant S, (2004) Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clin Cancer Res 10: 3839-3852.
39. Pozo-Guisado E, Merino JM, Mulero-Navarro S, Lorenzo-Benayas MJ, Centeno F, et al. (2005) Resveratrol-induced apoptosis in MCF-7 human breast cancer cells involves a caspase-independent mechanism with downregulation of Bcl-2 and NF-kappaB. Int J Cancer 115: 74-84.
40. Simizu S, Imoto M, Masuda N, Takada M, Umezawa K, (1996) Involvement of hydrogen peroxide production in erbstatin-induced apoptosis in human small cell lung carcinoma cells. Cancer Res 56: 4978-4982.
41. Ye J, Ding M, Leonard SS, Robinson VA, Millecchia L, et al. (1999) Vanadate induces apoptosis in epidermal JB6 P+ cells via hydrogen peroxide-mediated reactions. Mol Cell Biochem 202: 9-17.
42. Los M, Herr I, Friesen C, Fulda S, Schulze-Osthoff K, et al. (1997) Cross-resistance of CD95- and drug-induced apoptosis as a consequence of deficient activation of caspases (ICE/Ced-3 proteases). Blood 90: 3118-3129.
43. Martinez-Lorenzo MJ, Gamen S, Etxeberria J, Lasierra P, Larrad L, et al. (1998) Resistance to apoptosis correlates with a highly proliferative phenotype and loss of Fas and CPP32 (caspase-3) expression in human leukemia cells. Int J Cancer 75: 473-481.