The in vitro immunogenic potential of caspase-3 proficient breast cancer cells with basal low immunogenicity is increased by hypofractionated irradiation

Radiation Oncology

Volumn 10, Issue 1, 2015, Pages

  Kötter, Bernhard ^a   Frey, Benjamin ^a   Winderl, Markus ^a   Rubner, Yvonne ^a   Scheithauer, Heike ^b   Sieber, Renate ^a   Fietkau, Rainer ^a   Gaipl, Udo S ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CD86 ANTIGEN; FLUORESCEIN ISOTHIOCYANATE; HEAT SHOCK PROTEIN 70; HIGH MOBILITY GROUP B1 PROTEIN; HORMONE RECEPTOR; LIPOCORTIN 5; PROPIDIUM IODIDE; PROTEIN P53; CASP3 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CELL ACTIVATION; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELL SPECIFICITY; CELL STIMULATION; CLONOGENESIS; CLONOGENIC ASSAY; COLONY FORMATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME DEFICIENCY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HYPERTHERMIC THERAPY; IMMUNOGENICITY; IN VITRO STUDY; IONIZING RADIATION; MCF 7 CELL LINE; MDA MB231 CELL LINE; MONOCYTE DERIVED DENDRITIC CELL; PROTEIN EXPRESSION; PROTEIN SECRETION; RADIATION DOSE FRACTIONATION; RADIATION RESPONSE; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; SUPERNATANT; UPREGULATION; WILD TYPE; BREAST NEOPLASMS; FLOW CYTOMETRY; HYPOFRACTIONATED RADIOTHERAPY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROCEDURES; RADIATION TOLERANCE; THERMOTHERAPY; TUMOR CELL LINE;

BREAST NEOPLASMS; CASPASE 3; CELL DEATH; CELL LINE, TUMOR; DENDRITIC CELLS; DOSE HYPOFRACTIONATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; HYPERTHERMIA, INDUCED; IN VITRO TECHNIQUES; RADIATION TOLERANCE; RADIOTHERAPY;

EID: 84941634416     PISSN: None     EISSN: 1748717X     Source Type: Journal    
DOI: 10.1186/s13014-015-0506-5     Document Type: Article

References (68)

1. Anderson WF, Rosenberg PS, Prat A, Perou CM and Sherman ME. How many etiological subtypes of breast cancer: two, three, four, or more? J Natl Cancer Inst. 2014; 106:1-11
2. Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, Ehrmann J, et al. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer. 2007;7:55.
3. Allred DC. Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr. 2010;2010:134-8.
4. Dieterich M, Stubert J, Reimer T, Erickson N, Berling A. Influence of lifestyle factors on breast cancer risk. Breast Care (Basel). 2014;9:407-14.
5. Abramson VG, Mayer IA. Molecular heterogeneity of triple negative breast cancer. Curr Breast Cancer Rep. 2014;6:154-8.
6. Su S, Tian Y, Li Y, Ding Y, Ji T, Wu M, et al. "Triple-punch" strategy for triple negative breast cancer therapy with minimized drug dosage and improved antitumor efficacy. ACS Nano. 2015;9:1367-78.
7. Moran MS. Radiation therapy in the locoregional treatment of triple-negative breast cancer. Lancet Oncol. 2015;16:e113-22.
8. Sedlmayer F, Sautter-Bihl ML, Budach W, Dunst J, Fastner G, Feyer P, et al. DEGRO practical guidelines: radiotherapy of breast cancer I: radiotherapy following breast conserving therapy for invasive breast cancer. Strahlenther Onkol. 2013;189:825-33.
9. Roth SL, Audretsch W, Bojar H, Lang I, Willers R, Budach W. Retrospective study of neoadjuvant versus adjuvant radiochemotherapy in locally advanced noninflammatory breast cancer: survival advantage in cT2 category by neoadjuvant radiochemotherapy. Strahlenther Onkol. 2010;186:299-306.
10. Haviland JS, Owen JR, Dewar JA, Agrawal RK, Barrett J, Barrett-Lee PJ, et al. The UK Standardisation of Breast Radiotherapy (START) trials of radiotherapy hypofractionation for treatment of early breast cancer: 10-year follow-up results of two randomised controlled trials. Lancet Oncol. 2013;14:1086-94.
11. Coles CE, Brunt AM, Wheatley D, Mukesh MB, Yarnold JR. Breast radiotherapy: less is more? Clin Oncol (R Coll Radiol). 2013;25:127-34.
12. Dellas K, Vonthein R, Zimmer J, Dinges S, Boicev AD, Andreas P, et al. Hypofractionation with simultaneous integrated boost for early breast cancer: results of the German multicenter phase II trial (ARO-2010-01). Strahlenther Onkol. 2014;190:646-53.
13. Souchon R, Dunst J. The challenge of integrating radiotherapy in the multimodal treatment of breast cancer. Breast Care (Basel). 2011;6:345-6.
14. Golden EB, Frances D, Pellicciotta I, Demaria S, Helen Barcellos-Hoff M, Formenti SC. Radiation fosters dose-dependent and chemotherapy-induced immunogenic cell death. Oncoimmunology. 2014;3, e28518.
15. Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys. 2004;58:862-70.
16. Crittenden M, Kohrt H, Levy R, Jones J, Camphausen K, Dicker A, et al. Current clinical trials testing combinations of immunotherapy and radiation. Semin Radiat Oncol. 2015;25:54-64.
17. Frey B, Weiss EM, Rubner Y, Wunderlich R, Ott OJ, Sauer R, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia. 2012;28:528-42.
18. Schildkopf P, Ott OJ, Frey B, Wadepohl M, Sauer R, Fietkau R, et al. Biological rationales and clinical applications of temperature controlled hyperthermia--implications for multimodal cancer treatments. Curr Med Chem. 2010;17:3045-57.
19. Bruggmoser G, Bauchowitz S, Canters R, Crezee H, Ehmann M, Gellermann J, et al. Guideline for the clinical application, documentation and analysis of clinical studies for regional deep hyperthermia: quality management in regional deep hyperthermia. Strahlenther Onkol. 2012;188 Suppl 2:198-211.
20. Feyerabend T, Wiedemann GJ, Jager B, Vesely H, Mahlmann B, Richter E. Local hyperthermia, radiation, and chemotherapy in recurrent breast cancer is feasible and effective except for inflammatory disease. Int J Radiat Oncol Biol Phys. 2001;49:1317-25.
21. Vernon CC, Hand JW, Field SB, Machin D, Whaley JB, van der Zee J, et al. Radiotherapy with or without hyperthermia in the treatment of superficial localized breast cancer: results from five randomized controlled trials. International Collaborative Hyperthermia Group. Int J Radiat Oncol Biol Phys. 1996;35:731-44.
22. Horsman MR, Overgaard J. Hyperthermia: a potent enhancer of radiotherapy. Clin Oncol (R Coll Radiol). 2007;19:418-26.
23. Oldenborg S, Griesdoorn V, Kusumanto Y, van Os R, Oei SB, Venselaar JLM, et al. Re-irradiation plus hyperthermia for 415 patients with recurrent breast cancer in previously irradiated area - the Amsterdam plus Tilburg experience. Eur J Cancer. 2011;47:S340.
24. Varma S, Myerson R, Moros E, Taylor M, Straube W, Zoberi I. Simultaneous radiotherapy and superficial hyperthermia for high-risk breast carcinoma: a randomised comparison of treatment sequelae in heated versus non-heated sectors of the chest wall hyperthermia. Int J Hyperthermia. 2012;28:583-90.
25. Datta NR, Puric E, Heuberger J, Marder D, Lomax N, Timm O, et al. Hyperthermia and reirradiation for locoregional recurrences in preirradiated breast cancers: a single institutional experience. Swiss Med Wkly. 2015;145:w14133.
26. Sersa G, Cufer T, Paulin SM, Cemazar M, Snoj M. Electrochemotherapy of chest wall breast cancer recurrence. Cancer Treat Rev. 2012;38:379-86.
27. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, et al. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ. 2009;16:1093-107.
28. Rubner Y, Muth C, Strnad A, Derer A, Sieber R, Buslei R, et al. Fractionated radiotherapy is the main stimulus for the induction of cell death and of Hsp70 release of p53 mutated glioblastoma cell lines. Radiat Oncol. 2014;9:89.
29. Thoms J, Bristow RG. DNA repair targeting and radiotherapy: a focus on the therapeutic ratio. Semin Radiat Oncol. 2010;20:217-22.
30. Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2015;22:58-73.
31. Scheithauer H, Belka C, Lauber K, Gaipl US. Immunological aspects of radiotherapy. Radiat Oncol. 2014;9:185.
32. Lauber K, Ernst A, Orth M, Herrmann M, Belka C. Dying cell clearance and its impact on the outcome of tumor radiotherapy. Front Oncol. 2012;2:116.
33. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature. 1997;390:350-1.
34. Rodel F, Frey B, Multhoff G, Gaipl U. Contribution of the immune system to bystander and non-targeted effects of ionizing radiation. Cancer Lett. 2015;356:105-13.
35. Gaipl US, Kuenkele S, Voll RE, Beyer TD, Kolowos W, Heyder P, et al. Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ. 2001;8:327-34.
36. Rovere P, Vallinoto C, Bondanza A, Crosti MC, Rescigno M, Ricciardi-Castagnoli P, et al. Bystander apoptosis triggers dendritic cell maturation and antigen-presenting function. J Immunol. 1998;161:4467-71.
37. Aguilera R, Saffie C, Tittarelli A, Gonzalez FE, Ramirez M, Reyes D, et al. Heat-shock induction of tumor-derived danger signals mediates rapid monocyte differentiation into clinically effective dendritic cells. Clin Cancer Res. 2011;17:2474-83.
38. Gaipl US, Multhoff G, Scheithauer H, Lauber K, Hehlgans S, Frey B, et al. Kill and spread the word: stimulation of antitumor immune responses in the context of radiotherapy. Immunotherapy. 2014;6:597-610.
39. Janicke RU, Ng P, Sprengart ML, Porter AG. Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem. 1998;273:15540-5.
40. Brooks SC, Locke ER, Soule HD. Estrogen receptor in a human cell line (MCF-7) from breast carcinoma. J Biol Chem. 1973;248:6251-3.
41. Lacroix M, Leclercq G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat. 2004;83:249-89.
42. Young RK, Cailleau RM, Mackay B, Reeves WJ. Establishment of epithelial cell line MDA-MB-157 from metastatic pleural effusion of human breast carcinoma. In Vitro. 1974;9:239-45.
43. Overgaard J. Simultaneous and sequential hyperthermia and radiation treatment of an experimental tumor and its surrounding normal tissue in vivo. Int J Radiat Oncol Biol Phys. 1980;6:1507-17.
44. Schildkopf P, Frey B, Ott OJ, Rubner Y, Multhoff G, Sauer R, et al. Radiation combined with hyperthermia induces HSP70-dependent maturation of dendritic cells and release of pro-inflammatory cytokines by dendritic cells and macrophages. Radiother Oncol. 2011;101:109-15.
45. Braselmann H. CFAssay: statistical analysis for the colony formation assay. 2014.
46. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 1994;84:1415-20.
47. Riccardi C, Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc. 2006;1:1458-61.
48. Sherman M, Multhoff G. Heat shock proteins in cancer. Ann N Y Acad Sci. 2007;1113:192-201.
49. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994;179:1109-18.
50. Di Leo A, Curigliano G, Dieras V, Malorni L, Sotiriou C, Swanton C, et al. New approaches for improving outcomes in breast cancer in Europe. Breast. 2015.
51. Tryfonidis K, Senkus E, Cardoso MJ, Cardoso F. Management of locally advanced breast cancer-perspectives and future directions. Nat Rev Clin Oncol. 2015;12:147-62.
52. Zhang P, Castedo M, Tao Y, Violot D, Metivier D, Deutsch E, et al. Caspase independence of radio-induced cell death. Oncogene. 2006;25:7758-70.
53. Ma Z, Yao G, Zhou B, Fan Y, Gao S, Feng X. The Chk1 inhibitor AZD7762 sensitises p53 mutant breast cancer cells to radiation in vitro and in vivo. Mol Med Rep. 2012;6:897-903.
54. Hudis CA, Gianni L. Triple-negative breast cancer: an unmet medical need. Oncologist. 2011;16 Suppl 1:1-11.
55. Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget. 2014;5:403-16.
56. Kulzer L, Rubner Y, Deloch L, Allgauer A, Frey B, Fietkau R, et al. Norm- and hypo-fractionated radiotherapy is capable of activating human dendritic cells. J Immunotoxicol. 2014;11:328-36.
57. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS, Formenti SC, et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res. 2009;15:5379-88.
58. Mao Y, Qu Q, Zhang Y, Liu J, Chen X, Shen K. The value of tumor infiltrating lymphocytes (TILs) for predicting response to neoadjuvant chemotherapy in breast cancer: a systematic review and meta-analysis. PLoS One. 2014;9, e115103.
59. Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, et al. Tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy with or without Carboplatin in human epidermal growth factor receptor 2-positive and triple-negative primary breast cancers. J Clin Oncol. 2015;33:983-91.
60. Tesniere A, Panaretakis T, Kepp O, Apetoh L, Ghiringhelli F, Zitvogel L, et al. Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 2008;15:3-12.
61. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol. 2005;115:1260-7.
62. Soudja SM, Henri S, Mello M, Chasson L, Mas A, Wehbe M, et al. Disrupted lymph node and splenic stroma in mice with induced inflammatory melanomas is associated with impaired recruitment of T and dendritic cells. PLoS One. 2011;6, e22639.
63. Jolesch A, Elmer K, Bendz H, Issels RD, Noessner E. Hsp70, a messenger from hyperthermia for the immune system. Eur J Cell Biol. 2012;91:48-52.
64. Elsner L, Muppala V, Gehrmann M, Lozano J, Malzahn D, Bickeboller H, et al. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J Immunol. 2007;179:5523-33.
65. Modjtahedi N, Giordanetto F, Madeo F, Kroemer G. Apoptosis-inducing factor: vital and lethal. Trends Cell Biol. 2006;16:264-72.
66. Hennel R, Brix N, Seidl K, Ernst A, Scheithauer H, Belka C, et al. Release of monocyte migration signals by breast cancer cell lines after ablative and fractionated gamma-irradiation. Radiat Oncol. 2014;9:85.
67. Zhu EF, Gai SA, Opel CF, Kwan BH, Surana R, Mihm MC, et al. Synergistic innate and adaptive immune response to combination immunotherapy with anti-tumor antigen antibodies and extended serum half-life IL-2. Cancer Cell. 2015;27:489-501.
68. Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann B, et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol. 2013;24:2206-23.