Lack of P-glycoprotein expression by low-dose fractionated radiation results from loss of nuclear factor-κB and NF-Y activation in oral carcinoma cells

Molecular Cancer Research

Volumn 6, Issue 1, 2008, Pages 89-98

  Shareef, Mohammed Momin ^a   Brown, Brandee ^b   Shajahan, Shahin ^b   Sathishkumar, Sabapathi ^b   Arnold, Susanne M ^b   Mohiuddin, Mohammed ^c   Ahmed, Mansoor M ^a,c   Spring, Paul M ^d,e,f  

^a WEIS CENTER FOR RESEARCH   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c FOX CHASE CANCER CENTER   (United States)

^d CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^f UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUCIFERASE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; NUCLEAR FACTOR Y; PROTEIN MEF1; PROTEIN P50; PROTEIN P53; PROTEIN SUBUNIT; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NF R1; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; Y BOX BINDING PROTEIN 1;

APOPTOSIS; ARTICLE; CARCINOMA CELL; CONTROLLED STUDY; DNA BINDING; ENZYME ASSAY; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IONIZING RADIATION; MOUTH CARCINOMA; NICK END LABELING; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION DOSE; RADIATION EXPOSURE; RADIOSENSITIVITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SQUAMOUS CELL CARCINOMA;

APOPTOSIS; BASE SEQUENCE; CCAAT-BINDING FACTOR; CELL LINE, TUMOR; DOSE FRACTIONATION; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MOUTH NEOPLASMS; NF-KAPPA B; P-GLYCOPROTEIN; PROMOTER REGIONS (GENETICS); RADIATION TOLERANCE; RADIATION, IONIZING; TRANSCRIPTION FACTORS; TUMOR STEM CELL ASSAY; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 40749145971     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-07-0221     Document Type: Article

References (44)

1. Chen AY, Myers JN. Cancer of the oral cavity. Curr Probl Surg 2000;37:633-731.
2. Shah SB, Singer MI, Liberman E, et al. Transmucosal fine-needle aspiration diagnosis of intraoral and intrapharyngeal lesions. Laryngoscope 1999;109:1232-7.
3. Alvi A, Johnson JT. Extracapsular spread in the clinically negative neck (N0): implications and outcome. Otolaryngol Head Neck Surg 1996;114:65-70.
4. Ueda K, Cardarelli C, Gottesman MM, et al. Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci U S A 1987;84:3004-8.
5. Cole SP, Chanda ER, Dicke FP, et al. Non-P-glycoprotein-mediated multidrug resistance in a small cell lung cancer cell line: evidence for decreased susceptibility to drug-induced DNA damage and reduced levels of topoisomerase II. Cancer Res 1991;51:3345-52.
6. Cole SP, Deeley RG. Multidrug resistance associated with overexpression of MRP. Cancer Treat Res 1996;87:39-62.
7. Hirata S, Katoh O, Oguri T, et al. Expression of drug resistance-related genes in head and neck squamous cell carcinomas and normal mucosa. Jpn J Cancer Res 2000;91:84-90.
8. Ng IO, Lam KY, Ng M, et al. Expression of P-glycoprotein, a multidrug-resistance gene product, is induced by radiotherapy in patients with oral squamous cell carcinoma. Cancer 1998;83:851-7.
9. Smyth MJ, Krasovskis E, Sutton VR, et al. The drug efflux protein, P-glycoprotein, additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis. Proc Natl Acad Sci U S A 1998;95:7024-9.
10. Ruth AC, Roninson IB. Effects of the multidrug transporter P-glycoprotein on cellular responses to ionizing radiation. Cancer Res 2000;60:2576-8.
11. Ruefli AA, Smyth MJ, Johnstone RW. HMBA induces activation of a caspase-independent cell death pathway to overcome P-glycoprotein-mediated multidrug resistance. Blood 2000;95:2378-85.
12. Notarbartolo M, Cervello M, Dusonchet L, et al. Resistance to diverse apoptotic triggers in multidrug resistant HL60 cells and its possible relationship to the expression of P-glycoprotein, Fas and of the novel anti-apoptosis factors IAP (inhibitory of apoptosis proteins). Cancer Lett 2002;180:91-101.
13. Joiner MC. Induced radioresistance: an overview and historical perspective. Int J Radiat Biol 1994;65:79-84.
14. Marples B, Greco O, Joiner MC, et al. Molecular approaches to chemoradiotherapy. Eur J Cancer 2002;38:231-9.
15. Dey S, Spring PM, Arnold S, et al. Low-dose fractionated radiation potentiates the effects of paclitaxel in wild-type and mutant p53 head and neck tumor cell lines. Clin Cancer Res 2003;9:1557-65.
16. Spring PM, Arnold SM, Shajahan S, et al. Low dose fractionated radiation potentiates the effects of taxotere in nude mice xenografts of squamous cell carcinoma of head and neck. Cell Cycle 2004;3:479-85.
17. Kuo MT, Liu Z, Wei Y, et al. Induction of human MDR1 gene expression by 2-acetylaminofluorene is mediated by effectors of the phosphoinositide 3-kinase pathway that activate NF-κB signaling. Oncogene 2002;21:1945-54.
18. Ogretmen B, Safa AR. Down-regulation of apoptosis-related bcl-2 but not bcl-xL or bax proteins in multidrug-resistant MCF-7/Adr human breast cancer cells. Int J Cancer 1996;67:608-14.
19. Kato T, Duffey DC, Ondrey FG, et al. Cisplatin and radiation sensitivity in human head and neck squamous carcinomas are independently modulated by glutathione and transcription factor NF-κB. Head Neck 2000;22:748-59.
20. Goldsmith ME, Madden MJ, Morrow CS, et al. A Y-box consensus sequence is required for basal expression of the human multidrug resistance (mdr1) gene. J Biol Chem 1993;268:5856-60.
21. Sundseth R, MacDonald G, Ting J, et al. DNA elements recognizing NF-Y and Sp1 regulate the human multidrug-resistance gene promoter. Mol Pharmacol 1997;51:963-71.
22. Dorn A, Bollekens J, Staub A, et al. A multiplicity of CCAAT box-binding proteins. Cell 1987;50:863-72.
23. Maity SN, Sinha S, Ruteshouser EC, et al. Three different polypeptides are necessary for DNA binding of the mammalian heteromeric CCAAT binding factor. J Biol Chem 1992;267:16574-80.
24. Hu Z, Jin S, Scotto KW. Transcriptional activation of the MDR1 gene by UV irradiation. Role of NF-Y and Sp1. J Biol Chem 2000;275:2979-85.
25. Lee JM, Bernstein A. p53 mutations increase resistance to ionizing radiation. Proc Natl Acad Sci U S A 1993;90:5742-6.
26. Herskowitz I. Functional inactivation of genes by dominant negative mutations. Nature 1987;329:219-22.
27. Canman CE, Lim DS, Cimprich KA, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998;281:1677-9.
28. Short SC, Woodcock M, Marples B, et al. Effects of cell cycle phase on low-dose hyper-radiosensitivity. Int J Radiat Biol 2003;79:99-105.
29. Arnold SM, Regine WF, Ahmed MM, et al. Low-dose fractionated radiation as a chemopotentiator of neoadjuvant paclitaxel and carboplatin for locally advanced squamous cell carcinoma of the head and neck: results of a new treatment paradigm. Int J Radiat Oncol Biol Phys 2004;58:1411-7.
30. Jung M, Notario V, Dritschilo A. Mutations in the p53 gene in radiation-sensitive and -resistant human squamous carcinoma cells. Cancer Res 1992;52:6390-3.
31. Marples B, Wouters BG, Collis SJ, et al. Low-dose hyper-radiosensitivity: a consequence of ineffective cell cycle arrest of radiation-damaged G2-phase cells. Radiat Res 2004;161:247-55.
32. Enns L, Bogen KT, Wizniak J, et al. Low-dose radiation hypersensitivity is associated with p53-dependent apoptosis. Mol Cancer Res 2004;2:557-66.
33. Krueger SA, Joiner MC, Weinfeld M, et al. Role of apoptosis in low-dose hyper-radiosensitivity. Radiat Res 2007;167:260-7.
34. Hill BT, Moran E, Etievant C, et al. Low-dose twice-daily fractionated X-irradiation of ovarian tumor cells in vitro generates drug-resistant cells overexpressing two multidrug resistance-associated proteins, P-glycoprotein and MRP1. Anticancer Drugs 2000;11:193-200.
35. Mantovani R. A survey of 178 NF-Y binding CCAAT boxes. Nucleic Acids Res 1998;26:1135-43.
36. Jin S, Scotto KW. Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol Cell Biol 1998;18:4377-84.
37. Chendil D, Das A, Dey S, et al. Par-4, a pro-apoptotic gene, inhibits radiation-induced NFκB activity and Bcl-2 expression leading to induction of radiosensitivity in human prostate cancer cells PC-3. Cancer Biol Ther 2002;1:152-60.
38. Sanchez AM, Barrett JT, Schoenlein PV. Fractionated ionizing radiation accelerates loss of amplified MDR1 genes harbored by extrachromosomal DNA in tumor cells. Cancer Res 1998;58:3845-54.
39. Nair P, Muthukkumar S, Sells SF, et al. Early growth response-1-dependent apoptosis is mediated by p53. J Biol Chem 1997;272:20131-8.
40. Ahmed MM, Sells SF, Venkatasubbarao K, et al. Ionizing radiation-inducible apoptosis in the absence of p53 linked to transcription factor EGR-1. J Biol Chem 1997;272:33056-61.
41. Chapman NR, Perkins ND. Inhibition of the RelA(p65) NF-κB subunit by Egr-1. J Biol Chem 2000;275:4719-25.
42. Bae HW, Geiser AG, Kim DH, et al. Characterization of the promoter region of the human transforming growth factor-β type II receptor gene. J Biol Chem 1995;270:29460-8.
43. Sells SF, Muthukumar S, Sukhatme VP, et al. The zinc finger transcription factor EGR-1 impedes interleukin-1-inducible tumor growth arrest. Mol Cell Biol 1995;15:682-92.
44. Hamada A, Miyano H, Watanabe H, et al. Interaction of imatinib mesilate with human P-glycoprotein. J Pharmacol Exp Ther 2003;307:824-8.