Motexafin gadolinium and zinc induce oxidative stress responses and apoptosis in B-cell lymphoma lines

Cancer Research

Volumn 65, Issue 24, 2005, Pages 11676-11688

  Lecane, Philip S ^a   Karaman, Mazen W ^b   Sirisawad, Mint ^a   Naumovski, Louie ^a   Miller, Richard A ^a   Hacia, Joseph G ^b   Magda, Darren ^a  

^a PHARMACYCLICS INC   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GADOLINIUM TEXAPHYRIN; HYPOXIA INDUCIBLE FACTOR 1; MANNITOL; METAL RESPONSE ELEMENT BINDING TRANSCRIPTION FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ZINC ACETATE;

APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; HEMATOLOGIC MALIGNANCY; HOMEOSTASIS; HUMAN; HUMAN CELL; LYMPHOMA CELL; MITOSIS INHIBITION; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ZINC METABOLISM;

ANTINEOPLASTIC AGENTS; APOPTOSIS; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LYMPHOMA, B-CELL; METALLOPORPHYRINS; NF-E2-RELATED FACTOR 2; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; RESPONSE ELEMENTS; S PHASE; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED; ZINC;

EID: 29244453628     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-2754     Document Type: Article

References (52)

1. Costello LC. Franklin RB. Novel role of zinc in the regulation of prostate citrate metabolism and its implications in prostate cancer. Prostate 1998;35: 285-96.
2. Dineley KE, Votyakova TV, Reynolds IJ. Zinc inhibition of cellular energy production: implications for mitochondria and neurodegeneration. J Neurochem 2003;8S: 563-70.
3. Sheline CT, Behrens MM, Choi DW. Zinc-induced cortical neuronal death: contribution of energy failure attributable to loss of NAD(+) and inhibition of glycolysis. J Neurosci 2000;20:3139-46.
4. Lenartowicz E, Wudarczyk J. Enzymatic reduction of 5,5′ -dithiobis-(2-nitrobenzoic acid) by lysate of rat liver mitochondria. Int J Biochem Cell Biol 1995;27:831-7.
5. Rigobello MP, Callegaro MT, Harzon E, Renetti M, Rindoli A. Purification of mitochondrial thioredoxin reductase and its involvement in the redox regulation of membrane permeability. Free Radic Hiol Med 1998;24: 370-6.
6. Magda D, Lecane P, Miller RA, et al. Motexafin gadolinium disrupts zinc metabolism in human cancer cell lines. Cancer Res 2005;65:3837-45.
7. Holmgren A. Thioredoxin. Annu Rev Biochem 1985;54: 237-71.
8. Forbes IJ, Zalewski PD, Giannakis C. Role for zinc in a cellular response mediated by protein kinase C in human B lymphocytes. Exp Cell Res 1991;195:224-9.
9. Csermely P, Szamel M, Resch K, Somogyi J. Zinc can increase the activity of protein kinase C and contributes to its binding to plasma membranes in T lymphocytes. J Biol Chem 1988;263:6487-90.
10. Butcher HL, Kennette WA, Collins O, Zalups RK, Koropatnick J. Metallothionein mediates the level and activity of nuclear factor κB in murine fibroblasts. J Pharmacol Exp Ther 2004;310:589-98.
11. Kim CH, Kim JH, Moon SJ, et al. Pyrithione. a zinc ionophore, inhibits NF-κB activation. Biochem Biophys Res Commun 1999;259:505-9.
12. Hainaut P, Mann K. Zinc binding and redox control of p53 structure and function. Antioxid Redox Signal 2001;3:611-23.
13. O'Halloran TV. Transition metals in control of gene expression. Science 1993;261:715-25.
14. Haase H, Maret W. Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling. Exp Cell Res 2003;291:289-98.
15. Fraker PJ, Telford WG. A reappraisal of the role of zinc in life and death decisions of cells. Proc Soc Exp BiolMed 1997;215:229-36.
16. Mehta MP, Rodrigus P, Terhaard CH, et al. Survival and neurologic outcomes in a randomized trial of motexafin gadolinium and whole-brain radiation therapy in brain metastases. J Clin Oncol 2003;21:2529-36.
17. Biaglow JE, Miller RA, Magda D, Lee I, Tuttle S. Inhibition of thioredoxin reductase by motexafin gadolinium: effects on PLDR. Prog Abst Radiat Res Soc 2002;107.
18. Magda D, Gerasimchuk N, Lecane P, Miller RA, Biaglow JE, Sessler JL. Motexafin gadolinium reacts with ascorbate to produce reactive oxygen species. Chem Commun (Camb) 2002;2730-1.
19. Magda D, Lepp C, Gerasimchuk N, et al. Redox cycling by motexafin gadolinium enhances cellular response to ionizing radiation by forming reactive oxygen species. Int J Radiat Oncol Biol Phys 2001;51: 1025-36.
20. Evens AM, Lecane P, Magda D, et al. Motexafin gadolinium generates reactive oxygen species and induces apoptosis in sensitive and highly resistant multiple myeloma cells. Blood 2005;105:1265-73.
21. Eray M, Tuomikoski T, Wu H, et al. Cross-linking of surface IgG induces apoptosis in a bcl-2 expressing human follicular lymphoma line of mature B cell phenotype. Int Immunol 1994;6:1817-27.
22. Epstein AL, Levy R, Kim H, Henle W, Henle G, Kaplan HS. Biology of the human malignant lymphomas. IV. Functional characterization of ten diffuse histiocytic lymphoma cell lines. Cancer 1978;42:2379-91.
23. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
24. Gee KR, Zhou ZL, Ton-That D, Sensi SL, Weiss JH. Measuring zinc in living cells. A new generation of sensitive and selective fluorescent probes. Cell Calcium 2002;31:245-51.
25. Gratzner HG, Leif RC. An immunofluorescence method for monitoring DNA synthesis by flow cytometry. Cytometry 1981;1:385-93.
26. Naumovski L, Ramos J, Sirisawad M, et al. Sapphyrins induce apoptosis in hematopoietic tumor-derived cell lines and show in vivo antitumor activity. Mol Cancer Ther 2005;4:968-76.
27. Mizzen CA, Cartel NJ, Yu WH, Fraser PE, McLachlan DR. Sensitive detection of metallothioneins-1, -2 and -3 in tissue homogenates by immunoblotting: a method for enhanced membrane transfer and retention. J Biochem Biophys Methods 1996;32: 77-83.
28. Karaman MW. Houck ML. Chemnick LG. et al. Comparative analysis of gene-expression patterns in human and African great ape cultured fibroblasts. Genome Res 2003;13:1619-30.
29. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001;98:5116-21.
30. Giedroc DP, Chen X Apuy JL. Metal response element (MRE)-binding transcription factor-1 (MTF-1): structure, function, and regulation. Antioxid Redox Signal 2001;3:577-96.
31. Lichtlen P, Wang Y, Belser T. et al. Target gene search for the metal-responsive transcription factor MTF-1. Nucleic Acids Res 2001;29:1514-23.
32. Lichtlen P, Schaffner W. Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. Bioessays 2001;23:1010-7.
33. Andrews GK. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 2001;14:223-37.
34. Choi DW, Koh JY. Zinc and brain injury. Annu Rev Neurosci 1998;21:347-75.
35. 2+-induced ERK activation mediated by reactive oxygen species causes cell death in differentiated PC12 cells. J Neurochem 2001;78:600-10.
36. Malaiyandi LM, Dineley KE, Reynolds IJ. Divergent consequences arise from metallothionein overexpression in astrocytes: zinc buffering and oxidant-induced zinc release. Glia 2004;45:346-53.
37. Maret W, Vallee BL. Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc Natl Acad Sci U S A 1998;95:3478-82.
38. Chesney J, Mitchell R. Benigni F, et al. An inducible gene product for 6-phosphofructo-2-kinase with an AU-rich instability element role in tumor cell glycolysis and the Warburg effect. Proc Natl Acad Sci U S A 1999;96: 3047-52.
39. Shoshani T, Faerman A, Mett I, et al. Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801. involved in apoptosis. Mol Cell Biol 2002;22: 2283-93.
40. Corradetti MN, Inoki K, Guan KL. The stress-inducted proteins RTP801 and RTP801L are negative regulators of the mammalian target of rapamycin pathway. J Biol Chem 2005;280:9769-72.
41. Freeman RS, Hasbani DM, Lipscomb EA, Straub JA, Xie L. SM-20, EGL-9, and the EGLN family of hypoxia-inducible factor prolyl hydroxylases. Mol Cells 2003;16: 1-12.
42. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004;5:343-54.
43. Hirsila M, Koivunen P, Xu L, Seeley T, Kivirikko KI, Myllyharju J. Effect of desferrioxamine and metals on the hydroxylases in the oxygen sensing pathway. FASEB J 2005;19:1308-10.
44. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32.
45. Lee MJ, Kim JY, Suk K, Park JH. Identification of the hypoxia-inducible factor 1 α-responsive HGTD-P gene as a mediator in the mitochondrial apoptotic pathway. Mol Cell Biol 2004;24:3918-27.
46. Erickson AM, Nevarea Z, Gipp JJ, Mulcahy RT. Identification of a variant antioxidant response element in the promoter of the human glutamate-cysteine ligase modifier subunit gene. Revision of the ARE consensus sequence. J Biol Chem 2002;277: 30730-7.
47. Nioi P, McMahon M, Itoh K, Yamamoto M, Hayes JD. Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem J 2003;374:337-48.
48. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, et al. Direct evidence that sulfhydryl groups of Keapl are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci U S A 2002;99:11908-13.
49. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, et al. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keapl sensor modified by inducers. Proc Natl Acad Sci U S A 2004;101:2040-5.
50. Vargas MR, Pehar M, Cassina P, et al. Fibroblast growth factor-1 induces heme oxygenase-1 via nuclear factor erythroid 2-related factor 2 (Nrf2) in spinal cord astrocytes: Consequences for motor neuron survival. J Biol Chem 2005;280:25571-9.
51. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 2003;278:12029-38.
52. Miller RA, Biaglow JE. The thioredoxin reductase/thioredoxin system. Cancer Biol Ther 2005;4:6-13.