Radiosensitization of normoxic and hypoxic H1339 lung tumor cells by heat shock protein 90 inhibition is independent of hypoxia inducible factor-1α

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Schilling, Daniela ^a,b   Bayer, Christine ^a   Li, Wei ^c   Molls, Michael ^a   Vaupel, Peter ^a   Multhoff, Gabriele ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (2,4 DIHYDROXY 5 ISOPROPYLPHENYL) 4 (4 MORPHOLINOMETHYLPHENYL) 3 ISOXAZOLECARBOXYLIC ACID ETHYLAMIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TANESPIMYCIN; HEAT SHOCK PROTEIN 90; RADIOSENSITIZING AGENT;

ARTICLE; CANCER CELL CULTURE; CELL HYPOXIA; CELL STRAIN EPLC 272H; CELL STRAIN H1339; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; IRRADIATION; LUNG CARCINOMA; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; RADIOSENSITIVITY; RADIOSENSITIZATION; SIGNAL TRANSDUCTION; UPREGULATION; ANOXIA; DRUG ANTAGONISM; LUNG TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; RADIATION DOSE; TUMOR CELL LINE;

ANOXIA; CELL LINE, TUMOR; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG NEOPLASMS; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS;

EID: 84863062001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031110     Document Type: Article

References (49)

1. Kabakov AE, Kudryavtsev VA, Gabai VL, (2010) Hsp90 inhibitors as promising agents for radiotherapy. J Mol Med 88: 241-7.
2. Vaupel P, Mayer A, (2007) Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26: 225-39.
3. Choi N, Baumann M, Flentje M, Kellokumpu-Lehtinen P, Senan S, et al. (2001) Predictive factors in radiotherapy for non-small cell lung cancer: present status. Lung Cancer 31: 43-56.
4. Semenza GL, (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29: 625-34.
5. Katschinski DM, Le L, Schindler SG, Thomas T, Voss AK, et al. (2004) Interaction of the PAS B domain with HSP90 accelerates hypoxia-inducible factor-1α stabilization. Cell Physiol Biochem 14: 351-60.
6. Trepel J, Mollapour M, Giaccone G, Neckers L, (2010) Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10: 537-49.
7. Eccles SA, Massey A, Raynaud FI, Sharp SY, Box G, et al. (2008) NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res 68: 2850-60.
8. Brough PA, Aherne W, Barril X, Borgognoni J, Boxall K, et al. (2008) 4,5-diarylisoxazole Hsp90 chaperone inhibitors: potential therapeutic agents for the treatment of cancer. J Med Chem 51: 196-218.
9. Camphausen K, Tofilon PJ, (2007) Inhibition of Hsp90: a multitarget approach to radiosensitization. Clin Cancer Res 13: 4326-30.
10. Bisht KS, Bradbury CM, Mattson D, Kaushal A, Sowers A, et al. (2003) Geldanamycin and 17-allylamino-17-demethoxygeldanamycin potentiate the in vitro and in vivo radiation response of cervical tumor cells via the heat shock protein 90-mediated intracellular signaling and cytotoxicity. Cancer Res 63: 8984-95.
11. Aebersold DM, Burri P, Beer KT, Laissue J, Djonov V, et al. (2001) Expression of hypoxia-inducible factor-1α: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res 61: 2911-6.
12. Koukourakis MI, Giatromanolaki A, Sivridis E, Simopoulos C, Turley H, et al. (2002) Hypoxia-inducible factor (HIF1A and HIF2A), angiogenesis, and chemoradiotherapy outcome of squamous cell head-and-neck cancer. Int J Radiat Oncol Biol Phys 53: 1192-202.
13. Schilling D, Bayer C, Emmerich K, Molls M, Vaupel P, Huber RM, et al. Basal HIF-1α expression levels are not predictive for radiosensitivity of human cancer cell lines. Strahlenther Onkol In press 2012.
14. Gardner LB, Li Q, Park MS, Flanagan WM, Semenza GL, et al. (2001) Hypoxia inhibits G1/S transition through regulation of p27 expression. J Biol Chem 276: 7919-26.
15. Banerji U, Walton M, Raynaud F, Grimshaw R, Kelland L, et al. (2005) Pharmacokinetic-pharmacodynamic relationships for the heat shock protein 90 molecular chaperone inhibitor 17-allylamino, 17-demethoxygeldanamycin in human ovarian cancer xenograft models. Clin Cancer Res 11: 7023-32.
16. van de Sluis B, Groot AJ, Vermeulen J, van der WE, van Diest PJ, et al. (2009) COMMD1 promotes pVHL and O2-independent proteolysis of HIF-1α via HSP90/70. PLoS ONE 4: e7332.
17. Liu YV, Baek JH, Zhang H, Diez R, Cole RN, et al. (2007) RACK1 competes with HSP90 for binding to HIF-1α and is required for O2-independent and HSP90 inhibitor-induced degradation of HIF-1α. Mol Cell 25: 207-17.
18. Ehrlich ES, Wang T, Luo K, Xiao Z, Niewiadomska AM, et al. (2009) Regulation of Hsp90 client proteins by a Cullin5-RING E3 ubiquitin ligase. Proc Natl Acad Sci U S A 106: 20330-5.
19. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, et al. (2000) Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60: 7075-83.
20. Carroll VA, Ashcroft M, (2006) Role of hypoxia-inducible factor (HIF)-1α versus HIF-2α in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res 66: 6264-70.
21. Fink T, Kazlauskas A, Poellinger L, Ebbesen P, Zachar V, (2002) Identification of a tightly regulated hypoxia-response element in the promoter of human plasminogen activator inhibitor-1. Blood 99: 2077-83.
22. Artman T, Schilling D, Gnann J, Molls M, Multhoff G, et al. (2010) Irradiation-induced regulation of plasminogen activator inhibitor type-1 and vascular endothelial growth factor in six human squamous cell carcinoma lines of the head and neck. Int J Radiat Oncol Biol Phys 76: 574-82.
23. Said HM, Polat B, Hagemann C, Anacker J, Flentje M, et al. (2009) Absence of GAPDH regulation in tumor-cells of different origin under hypoxic conditions in- vitro. BMC Res Notes 2: 8.
24. Schilling D, Bayer C, Emmerich K, Molls M, Vaupel P, Huber RM, et al. Basal HIF-1α expression levels are not predictive for radiosensitivity of human cancer cell lines. Strahlenther Onkol In press 2011.
25. Vaupel P, (2004) Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol 14: 198-206.
26. Moeller BJ, Dreher MR, Rabbani ZN, Schroeder T, Cao Y, et al. (2005) Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell 8: 99-110.
27. Dungey FA, Caldecott KW, Chalmers AJ, (2009) Enhanced radiosensitization of human glioma cells by combining inhibition of poly(ADP-ribose) polymerase with inhibition of heat shock protein 90. Mol Cancer Ther 8: 2243-54.
28. Russell JS, Burgan W, Oswald KA, Camphausen K, Tofilon PJ, (2003) Enhanced cell killing induced by the combination of radiation and the heat shock protein 90 inhibitor 17-allylamino-17- demethoxygeldanamycin: a multitarget approach to radiosensitization. Clin Cancer Res 9: 3749-55.
29. Noguchi M, Yu D, Hirayama R, Ninomiya Y, Sekine E, et al. (2006) Inhibition of homologous recombination repair in irradiated tumor cells pretreated with Hsp90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Biochem Biophys Res Commun 351: 658-63.
30. Stingl L, Stuhmer T, Chatterjee M, Jensen MR, Flentje M, et al. (2010) Novel HSP90 inhibitors, NVP-AUY922 and NVP-BEP800, radiosensitise tumour cells through cell-cycle impairment, increased DNA damage and repair protraction. Br J Cancer 102: 1578-91.
31. Ibrahim NO, Hahn T, Franke C, Stiehl DP, Wirthner R, et al. (2005) Induction of the hypoxia-inducible factor system by low levels of heat shock protein 90 inhibitors. Cancer Res 65: 11094-100.
32. Katschinski DM, Le L, Heinrich D, Wagner KF, Hofer T, et al. (2002) Heat induction of the unphosphorylated form of hypoxia-inducible factor-1α is dependent on heat shock protein-90 activity. J Biol Chem 277: 9262-7.
33. Mabjeesh NJ, Post DE, Willard MT, Kaur B, Van Meir EG, et al. (2002) Geldanamycin induces degradation of hypoxia-inducible factor 1α protein via the proteosome pathway in prostate cancer cells. Cancer Res 62: 2478-82.
34. Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, et al. (2002) Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J Biol Chem 277: 29936-44.
35. Gaspar N, Sharp SY, Eccles SA, Gowan S, Popov S, et al. (2010) Mechanistic evaluation of the novel HSP90 inhibitor NVP-AUY922 in adult and pediatric glioblastoma. Mol Cancer Ther 9: 1219-33.
36. Zhou J, Schmid T, Frank R, Brune B, (2004) PI3K/Akt is required for heat shock proteins to protect hypoxia-inducible factor 1α from pVHL-independent degradation. J Biol Chem 279: 13506-13.
37. Fay MJ, Longo KA, Karathanasis GA, Shope DM, Mandernach CJ, et al. (2003) Analysis of CUL-5 expression in breast epithelial cells, breast cancer cell lines, normal tissues and tumor tissues. Mol Cancer 2: 40.
38. van de Sluis B, Mao X, Zhai Y, Groot AJ, Vermeulen JF, et al. (2010) COMMD1 disrupts HIF-1alpha/beta dimerization and inhibits human tumor cell invasion. J Clin Invest 120: 2119-30.
39. Yang J, Zhang L, Erbel PJ, Gardner KH, Ding K, et al. (2005) Functions of the Per/ARNT/Sim domains of the hypoxia-inducible factor. J Biol Chem 280: 36047-54.
40. Kim WY, Oh SH, Woo JK, Hong WK, Lee HY, (2009) Targeting heat shock protein 90 overrides the resistance of lung cancer cells by blocking radiation-induced stabilization of hypoxia-inducible factor-1α. Cancer Res 69: 1624-32.
41. Liu J, Zhang J, Wang X, Li Y, Chen Y, et al. (2010) HIF-1 and NDRG2 contribute to hypoxia-induced radioresistance of cervical cancer Hela cells. Exp Cell Res 316: 1985-93.
42. Kessler J, Hahnel A, Wichmann H, Rot S, Kappler M, et al. (2010) HIF-1α inhibition by siRNA or chetomin in human malignant glioma cells: effects on hypoxic radioresistance and monitoring via CA9 expression. BMC Cancer 10: 605.
43. Akakura N, Kobayashi M, Horiuchi I, Suzuki A, Wang J, et al. (2001) Constitutive expression of hypoxia-inducible factor-1α renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res 61: 6548-54.
44. Sasabe E, Tatemoto Y, Li D, Yamamoto T, Osaki T, (2005) Mechanism of HIF-1α-dependent suppression of hypoxia-induced apoptosis in squamous cell carcinoma cells. Cancer Sci 96: 394-402.
45. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, et al. (1998) Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-90.
46. Greijer AE, van der Wall E, (2004) The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J Clin Pathol 57: 1009-14.
47. Schilling D, Gehrmann M, Steinem C, De MA, Pockley AG, et al. (2009) Binding of heat shock protein 70 to extracellular phosphatidylserine promotes killing of normoxic and hypoxic tumor cells. FASEB J 23: 2467-77.
48. Schilling D, Bayer C, Geurts-Moespot A, Sweep FC, Pruschy M, et al. (2007) Induction of plasminogen activator inhibitor type-1 (PAI-1) by hypoxia and irradiation in human head and neck carcinoma cell lines. BMC Cancer 7: 143.
49. Gehrmann M, Liebisch G, Schmitz G, Anderson R, Steinem C, et al. (2008) Tumor-specific Hsp70 plasma membrane localization is enabled by the glycosphingolipid Gb3. PLoS ONE 3: e1925.