Role of membrane Hsp70 in radiation sensitivity of tumor cells

Radiation Oncology

Volumn 10, Issue 1, 2015, Pages

  Murakami, Naoya ^a,b   Kühnel, Annett ^a   Schmid, Thomas E ^a   Ilicic, Katarina ^a   Stangl, Stefan ^a   Braun, Isabella S ^a   Gehrmann, Mathias ^a   Molls, Michael ^a   Itami, Jun ^b   Multhoff, Gabriele ^a,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b NATIONAL CANCER CENTER HOSPITAL   (Japan)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Apoptosis; Heat shock protein 70; Membrane localization; Radiation resistance; X ray irradiation

Indexed keywords

CASPASE 3; CASPASE 7; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; HISTONE H2AX; LIPOCORTIN 5; SMALL INTERFERING RNA; APOPTOSIS REGULATORY PROTEIN; GAMMA-H2AX PROTEIN, MOUSE; H2AFX PROTEIN, HUMAN; HISTONE; MEMBRANE PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIOSENSITIVITY; STABLE EXPRESSION; TUMOR CELL; UPREGULATION; ANIMAL; BIOSYNTHESIS; CHEMISTRY; COLON TUMOR; COMPARATIVE STUDY; CRISPR CAS SYSTEM; DEFICIENCY; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; PATHOLOGY; PHYSIOLOGY; RADIATION RESPONSE; RADIATION TOLERANCE; SPECIES DIFFERENCE; TUMOR CELL LINE; TUMOR STEM CELL ASSAY;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; COLONIC NEOPLASMS; CRISPR-CAS SYSTEMS; CYTOSOL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HISTONES; HSP70 HEAT-SHOCK PROTEINS; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; RADIATION TOLERANCE; SPECIES SPECIFICITY; TUMOR STEM CELL ASSAY;

EID: 84937691999     PISSN: None     EISSN: 1748717X     Source Type: Journal    
DOI: 10.1186/s13014-015-0461-1     Document Type: Article

References (61)

1. Botzler C, Ellwart J, Günther W, Eissner G, Multhoff G. Synergistic effects of heat and ET-18-OCH3 on membrane expression of hsp70 and lysis of leukemic K562 cells. Exp Hematol. 1999;27(3):470-8. doi: 10.1016/S0301-472X(98)00055-1 .
2. Sharma S, Singh R, Kaur M, Kaur G. Late-onset dietary restriction compensates for age-related increase in oxidative stress and alterations of HSP70 and synapsin 1 protein levels in male Wistar rats. Biogerontology. 2010;11(2):197-209. doi: 10.1007/s10522-009-9240-4 .
3. Ciocca DR, Arrigo AP, Calderwood SK. Heat shock proteins and heat shock factor-1 in carcinogenesis and tumor development: an update. Arch Toxicol. 2013;87(1):19-48. doi: 10.1007/s00204-012-0918-z .
4. Dakappagari N, Neely L, Tangri S, Lundgren K, Hipolito L, Estrellado A, et al. An investigation into the potential use of serum Hsp70 as a novel tumour biomarker for Hsp90 inhibitors. Biomarkers. 2010;15(1):31-8. doi: 10.3109/13547500903261347 .
5. Multhoff G, Botzler C, Wiesnet M, Müller E, Meier T, Wilmanns W, et al. A stress-inducible 72-kDa heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int J Cancer. 1995;61(2):272-9.
6. Ferrarini M, Heltai S, Zocchi MR, Rugarli C. Unusual expression and localization of heat-shock proteins in human tumor cells. Int J Cancer. 1992;51(4):613-9.
7. Hantschel M, Pfister K, Jordan A, Scholz R, Andreesen R, Schmitz G, et al. Hsp70 plasma membrane expression on primary tumor biopsy material and bone marrow of leukemic patients. Cell Stress Chaperones. 2000;5(5):438-42. PMC312874.
8. Aghdassi A, Phillips P, Dudeja V, Dhaulakhandi D, Sharif R, Dawra R, et al. Heat shock protein 70 increases tumorigenicity and inhibits apoptosis in pancreatic adenocarcinoma. Cancer Res. 2007;67(2):616-25.
9. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G. Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun. 2001;286(3):433-42. doi: 10.1006/bbrc.2001.5427 .
10. Jäättelä M, Wissing D, Kokholm K, Kallunki T, Egeblad M. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 1998;17(21):6124-34. doi: 10.1093/emboj/17.21.6124 .
11. Gao Y, Han C, Huang H, Xin Y, Xu Y, Luo L, et al. Heat shock protein 70 together with its co-chaperone CHIP inhibits TNF-alpha induced apoptosis by promoting proteasomal degradation of apoptosis signal-regulating kinase1. Apoptosis. 2010;15(7):822-33. doi: 10.1007/s10495-010-0495-7 .
12. Yang X, Wang J, Zhou Y, Wang Y, Wang S, Zhang W. Hsp70 promotes chemoresistance by blocking Bax mitochondrial translocation in ovarian cancer cells. Cancer Lett. 2012;321(2):137-43. doi: 10.1016/j.canlet.2012.01.030 .
13. Kirkegaard T, Roth AG, Petersen NH, Mahalka AK, Olsen OD, Moilanen I, et al. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature. 2010;463(7280):549-53. doi: 10.1038/nature08710 .
14. Bayer C, Liebhardt ME, Schmid TE, Trajkovic-Arsic M, Hube K, Specht HM, et al. Validation of heat shock protein 70 as a tumor-specific biomarker for monitoring the outcome of radiation therapy in tumor mouse models. Int J Radiat Oncol Biol Phys. 2014;88(3):694-700. doi: 10.1016/j.ijrobp.2013.11.008 .
15. Gehrmann M, Specht HM, Bayer C, Brandstetter M, Chizzali B, Duma M, et al. Hsp70 - a biomarker for tumor detection and monitoring of outcome of radiation therapy in patients with squamous cell carcinoma of the head and neck. Radiat Oncol. 2014;9:131. doi: 10.1186/1748-717X-9-131 .
16. Stangl S, Varga J, Freysoldt B, Trajkovic-Arsic M, Siveke JT, Greten FR, et al. Selective in vivo imaging of syngeneic, spontaneous, and xenograft tumors using a novel tumor cell-specific Hsp70 peptide-based probe. Cancer Res. 2014;74(23):6903-12. doi: 10.1158/0008-5472.CAN-14-0413 .
17. Gehrmann M, Stangl S, Foulds GA, Oellinger R, Breuninger S, Rad R, et al. Tumor imaging and targeting potential of an Hsp70-derived 14-mer peptide. PLoS One. 2014;9(8):e105344. doi: 10.1371/journal.pone.0105344 .
18. Rerole AL, Jego G, Garrido C. Hsp70: anti-apoptotic and tumorigenic protein. Methods Mol Biol (Clifton, NJ). 2011;787:205-30. doi: 10.1007/978-1-61779-295-3_16 .
19. Sayers TJ. Targeting the extrinsic apoptosis signaling pathway for cancer therapy. Cancer Immunol Immunother. 2011;60(8):1173-80. doi: 10.1007/s00262-011-1008-4 .
20. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2(4):277-88.
21. Kulikov AV, Shilov ES, Mufazalov IA, Gogvadze V, Nedospasov SA, Zhivotovsky B. Cytochrome c: the Achilles' heel in apoptosis. Cell Mol Life Sci. 2012;69(11):1787-97. doi: 10.1007/s00018-011-0895-z .
22. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Hoyer-Hansen M, et al. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med. 2004;200(4):425-35.
23. Jäättelä M. Escaping cell death: survival proteins in cancer. Exp Cell Res. 1999;248(1):30-43.
24. Gotoh T, Terada K, Oyadomari S, Mori M. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ. 2004;11(4):390-402. doi: 10.1038/sj.cdd.4401369 .
25. Stankiewicz AR, Lachapelle G, Foo CP, Radicioni SM, Mosser DD. Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J Biol Chem. 2005;280(46):38729-39.
26. Guo F, Sigua C, Bali P, George P, Fiskus W, Scuto A, et al. Mechanistic role of heat shock protein 70 in Bcr-Abl-mediated resistance to apoptosis in human acute leukemia cells. Blood. 2005;105(3):1246-55. doi: 10.1182/blood-2004-05-2041 .
27. Gehrmann M, Marienhagen J, Eichholtz-Wirth H, Fritz E, Ellwart J, Jäättelä M, et al. Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ. 2005;12(1):38-51. doi: 10.1038/sj.cdd.4401510 .
28. Multhoff G, Botzler C, Jennen L, Schmidt J, Ellwart J, Issels R. Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J Immunol. 1997;158(9):4341-50.
29. Zaarur N, Gabai V, Porco J, Calderwood S, Sherman M. Targeting heat shock response to sensitize cancer cells to proteasome and Hsp90 inhibitors. Cancer Res. 2006;66(3):1783-91.
30. Pulaski BA, Terman DS, Khan S, Muller E, Ostrand-Rosenberg S. Cooperativity of Staphylococcal aureus enterotoxin B superantigen, major histocompatibility complex class II, and CD80 for immunotherapy of advanced spontaneous metastases in a clinically relevant postoperative mouse breast cancer model. Cancer Res. 2000;60(10):2710-5.
31. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816-21. doi: 10.1126/science.1225829 .
32. Pouget JP, Mather SJ. General aspects of the cellular response to low- and high-LET radiation. Eur J Nucl Med. 2001;28(4):541-61.
33. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154(6):1380-9. doi: 10.1016/j.cell.2013.08.021 .
34. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(259):680-5. doi: 10.1038/227680a .
35. Schilling D, Gehrmann M, Steinem C, De MA, Pockley AG, Abend M, et al. Binding of heat shock protein 70 to extracellular phosphatidylserine promotes killing of normoxic and hypoxic tumor cells. FASEB J. 2009;23(8):2467-77. doi: 10.1096/fj.08-125229 .
36. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979;76(9):4350-4. doi: 10.1073/pnas.76.9.4350 .
37. Murakami N, Mori T, Yoshimoto S, Ito Y, Kobayashi K, Ken H, et al. Expression of EpCAM and prognosis in early-stage glottic cancer treated by radiotherapy. Laryngoscope. 2014;124(11):E431-6. doi: 10.1002/lary.24839 .
38. Lee JM, Bernstein A. p53 mutations increase resistance to ionizing radiation. Proc Natl Acad Sci U S A. 1993;90(12):5742-6.
39. Wu H, Schiff DS, Lin Y, Neboori HJ, Goyal S, Feng Z, et al. Ionizing radiation sensitizes breast cancer cells to Bcl-2 inhibitor, ABT-737, through regulating Mcl-1. Radiat Res. 2014;182(6):618-25. doi: 10.1667/RR13856.1 .
40. Zhang P, Leu JI, Murphy ME, George DL, Marmorstein R. Crystal structure of the stress-inducible human heat shock protein 70 substrate-binding domain in complex with peptide substrate. PLoS ONE. 2014;9(7):e103518. doi: 10.1371/journal.pone.0103518 .
41. Daugaard M, Rohde M, Jäättelä M. The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett. 2007;581(19):3702-10. doi: 10.1016/j.febslet.2007.05.039 .
42. Daugaard M, Jäättelä M, Rohde M. Hsp70-2 is required for tumor cell growth and survival. Cell Cycle. 2005;4(7):877-80.
43. Zorzi E, Bonvini P. Inducible hsp70 in the regulation of cancer cell survival: analysis of chaperone induction, expression and activity. Cancer. 2011;3(4):3921-56. doi: 10.3390/cancers3043921 .
44. Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, et al. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol. 2000;2(8):469-75.
45. Pandey P, Saleh A, Nakazawa A, Kumar S, Srinivasula SM, Kumar V, et al. Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J. 2000;19(16):4310-22.
46. Park HS, Cho SG, Kim CK, Hwang HS, Noh KT, Kim MS, et al. Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol Cell Biol. 2002;22(22):7721-30.
47. Petersen NH, Kirkegaard T, Olsen OD, Jäättelä M. Connecting Hsp70, sphingolipid metabolism and lysosomal stability. Cell Cycle. 2010;9(12):2305-9.
48. Hightower LE, Guidon PT. Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proetisn. J Cell Physiol. 1989;138(2):257-66.
49. Nickel W, Seedorf M. Unconventional mechansims of proetein transport to the cell surface of eukaryotic cells. Annu Rev Cell Dev Biol. 2008;24:287-308. doi: 10.1146/annurev.cellbio.24.110707.175320 .
50. Multhoff G. Heat shock protein 70 (Hsp70): membrane location, export and immunological relevance. Methods. 2007;43(3):229-37. doi: 10.1016/j.ymeth.2007.06.006 .
51. Gehrmann M, Liebisch G, Schmitz G, Anderson R, Steinem C, De MA, et al. Tumor-specific Hsp70 plasma membrane localization is enabled by the glycosphingolipid Gb3. PLoS ONE. 2008;3(4):e1925.
52. Komarova EY, Meshalkina DA, Aksenov ND, Pchelin IM, Martynova E, Margulis BA, et al. The discovery of Hsp70 domain with cell-penetrating activity. Cell Stress Chaperones. 2015;20:343-54. doi: 10.1007/s12192-014-0554-z .
53. Shevtsov MA, Komarova EY, Meshalkina DA, Bychkova NV, Aksenov ND, Abkin SV, et al. Exogenously delivered Hsp70 displaces its endogenous analogue and sensitizes cenacer cells to lymphyocytes-mediated cytotoxicity. Oncotarget. 2014;5(10):3101-14.
54. Horvath I, Vigh L. Cell biology: Stability in times of stress. Nature. 2010;463(7280):436-8. doi: 10.1038/463436a .
55. Olive PL, Banath JP, Sinnott LT. Phosphorylated histone H2AX in spheroids, tumors, and tissues of mice exposed to etoposide and 3-amino-1,2,4-benzotriazine-1,3-dioxide. Cancer Res. 2004;64(15):5363-9. doi: 10.1158/0008-5472.CAN-04-0729 .
56. Olive PL, Banath JP. Phosphorylation of histone H2AX as a measure of radiosensitivity. Int J Radiat Oncol Biol Phys. 2004;58(2):331-5.
57. Tait SW, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol. 2010;11(9):621-32. doi: 10.1038/nrm2952 .
58. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ. 2000;7(12):1166-73. doi: 10.1038/sj.cdd.4400783 .
59. Pfister K, Radons J, Busch R, Tidball JG, Pfeifer M, Freitag L, et al. Patient survival by Hsp70 membrane phenotype: association with different routes of metastasis. Cancer. 2007;110(4):926-35. doi: 10.1002/cncr.22864 .
60. Breuninger S, Ertl J, Bayer C, Knape C, Gunther S, Regel I, et al. Quantative analysis of liposomal Hsp70 in the blood of tumor patients using a novel lipHsp70 ELISA. J Clin Cell Immunol. doi:org/ 10.4172/2155-9899.1000264 .
61. Gehrmann M, Cervello M, Montalto G, Capello F, Gulino A, Knape C, et al. Hsp70 serum levels differ significantly in patients with chronic hepatitis, lievr chirrosis and hepatocellular carcinoma. Front Immunol. 2014;5:307. doi: 10.3389/fimmu.2014.00307 . eCollection2014.