Irradiation induces glioblastoma cell senescence and senescence-associated secretory phenotype

Tumor Biology

Volumn 37, Issue 5, 2016, Pages 5857-5867

  Jeon, Hee Young ^a   Kim, Jun Kyum ^a   Ham, Seok Won ^a   Oh, Se Yeong ^a   Kim, Jaebong ^b   Park, Jae Bong ^b   Lee, Jae Yong ^b   Kim, Sung Chan ^b   Kim, Hyunggee ^a  

^a Korea University   (South Korea)

^b Hallym University College of Medicine   (South Korea)

Author keywords

Glioblastoma multiforme; Radiotherapy; Recurrence; Senescence; Senescence associated secretory phenotype

Indexed keywords

BETA GALACTOSIDASE; CXCL1 CHEMOKINE; CYCLIN DEPENDENT KINASE INHIBITOR 1; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL GROWTH; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GLIOBLASTOMA CELL LINE; GRO1 GENE; HISTOLOGY; HUMAN; HUMAN CELL; IL1ALPHA GENE; IL1BETA GENE; IL6 GENE; IL8 GENE; IN VITRO STUDY; IN VIVO STUDY; IRRADIATION; MCP1 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENESCENCE; TRANSCRIPTION INITIATION; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; CELL AGING; CELL CYCLE; CELL PROLIFERATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; GLIOBLASTOMA; METABOLISM; PATHOLOGY; PHENOTYPE; RADIATION RESPONSE; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL AGING; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; MICE; NF-KAPPA B; PHENOTYPE; TRANSCRIPTIONAL ACTIVATION;

EID: 84947580647     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-4439-2     Document Type: Article

References (41)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;359:492–507.
2. Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96.
3. Grossman SA, Ye X, Piantadosi S, Desideri S, Nabors LB, Rosenfeld M, et al. Survival of patients with newly diagnosed glioblastoma treated with radiation and temozolomide in research studies in the United States. Clin Cancer Res. 2010;16:2443–9.
4. Liang BC, Thornton Jr AF, Sandler HM, Greenberg HS. Malignant astrocytomas: focal tumor recurrence after focal external beam radiation therapy. J Neurosurg. 1991;75:559–63.
5. Sneed PK, Gutin PH, Larson DA, Malec MK, Phillips TL, Prados MD, et al. Patterns of recurrence of glioblastoma multiforme after external irradiation followed by implant boost. Int J Radiat Oncol Biol Phys. 1994;29:719–27.
6. Chang JE, Khuntia D, Robins HI, Mehta MP. Radiotherapy and radiosensitizers in the treatment of glioblastoma multiforme. Clin Adv Hematol Oncol. 2007;894–902:7–15.
7. Tanaka S, Louis DN, Curry WT, Batchelor TT, Dietrich J. Diagnostic and therapeutic avenues for glioblastoma: no longer a dead end? Nat Rev Clin Oncol. 2013;10:14–26.
8. Persano L, Rampazzo E, Basso G, Viola G. Glioblastoma cancer stem cells: role of the microenvironment and therapeutic targeting. Biochem Pharmacol. 2013;85:612–22.
9. Mitchell JB, Choudhuri R, Fabre K, Sowers AL, Citrin D, Zabludoff SD, et al. In vitro and in vivo radiation sensitization of human tumor cells by a novel checkpoint kinase inhibitor, AZD7762. Clin Cancer Res. 2010;16:2076–84.
10. Bernhard EJ, Maity A, Muschel RJ, McKenna WG. Effects of ionizing radiation on cell cycle progression. Radiat Environ Biophys. 1995;34:79–83.
11. Maity A, McKenna WG, Muschel RJ. The molecular basis for cell cycle delays following ionizing radiation: a review. Radiother Oncol. 1994;31:1–13.
12. Campisi J, di Fagagna FA. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007;8:729–40.
13. Roninson IB. Tumor cell senescence in cancer treatment. Cancer Res. 2003;63:2705–15.
14. Bravata V, Minafra L, Russo G, Forte GI, Cammarata FP, Ripamonti M, et al. High-dose ionizing radiation regulates gene expression changes in the MCF7 breast cancer cell line. Anticancer Res. 2015;35:2577–91.
15. Ye C, Zhang X, Wan J, Chang L, Hu W, Bing Z, et al. Radiation-induced cellular senescence results from a slippage of long-term G2 arrested cells into G1 phase. Cell Cycle. 2013;12:1424–32.
16. Hornsby PJ. Senescence as an anticancer mechanism. J Clin Oncol. 2007;25:1852–7.
17. Wu C-H, van Riggelen J, Yetil A, Fan AC, Bachireddy P, Felsher DW. Cellular senescence is an important mechanism of tumor regression upon c-Myc inactivation. Proc Natl Acad Sci U S A. 2007;104:13028–33.
18. Cerella C, Grandjenette C, Dicato M, Diederich M. Roles of apoptosis and cellular senescence in cancer and aging. Curr Drug Targets. 2015.
19. Acosta JC, Banito A, Wuestefeld T, Georgilis A, Janich P, Morton JP, et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat Cell Biol. 2013;15:978–90.
20. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol. 2011;192:547–56.
21. Han NK, Kim BC, Lee HC, Lee YJ, Park MJ, Chi SG, et al. Secretome analysis of ionizing radiation‐induced senescent cancer cells reveals that secreted rkip plays a critical role in neighboring cell migration. Proteomics. 2012;12:2822–32.
22. Acosta JC, O’Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell. 2008;133:1006–18.
23. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 2008;6:2853–68.
24. Liao EC, Hsu YT, Chuah QY, Lee YJ, Hu JY, Huang TC, et al. Radiation induces senescence and a bystander effect through metabolic alterations. Cell Death Dis. 2014;5, e1255.
25. Mosieniak G, Strzeszewska A. The role of cellular senescence in carcinogenesis and antitumor therapy. Postepy Biochem. 2014;60:194–206.
26. Petit V, Massonnet G, Maciorowski Z, Touhami J, Thuleau A, Nemati F, et al. Optimization of tumor xenograft dissociation for the profiling of cell surface markers and nutrient transporters. Lab Investig. 2013;93:611–21.
27. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408:307–10.
28. Pyrko P, Soriano N, Kardosh A, Liu Y-T, Uddin J, Petasis NA, et al. Downregulation of survivin expression and concomitant induction of apoptosis by celecoxib and its non-cyclooxygenase-2-inhibitory analog, dimethyl-celecoxib (DMC), in tumor cells in vitro and in vivo. Mol Cancer. 2006;5:19.
29. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, et al. Control of the senescence-associated secretory phenotype by NF-κB promotes senescence and enhances chemosensitivity. Genes Dev. 2011;25:2125–36.
30. Bartkova J, Hořejší Z, Koed K, Krämer A, Tort F, Zieger K, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature. 2005;434:864–70.
31. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature. 2005;436:720–4.
32. Krtolica A, Parrinello S, Lockett S, Desprez PY, Campisi J. Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc Natl Acad Sci U S A. 2001;98:12072–7.
33. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10:459–66.
34. Yang I, Aghi MK. New advances that enable identification of glioblastoma recurrence. Nat Rev Clin Oncol. 2009;6:648–57.
35. Liu SC, Alomran R, Chernikova SB, Lartey F, Stafford J, Jang T, et al. Blockade of SDF-1 after irradiation inhibits tumor recurrences of autochthonous brain tumors in rats. Neuro Oncol. 2014;16:21–8.
36. Qian B-Z, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222–5.
37. Lu X, Kang Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J Biol Chem. 2009;284:29087–96.
38. Kuo PL, Shen KH, Hung SH, Hsu YL. CXCL1/GROalpha increases cell migration and invasion of prostate cancer by decreasing fibulin-1 expression through NF-kappaB/HDAC1 epigenetic regulation. Carcinogenesis. 2012;33:2477–87.
39. Karin M, Cao Y, Greten FR, Li ZW. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer. 2002;2:301–10.
40. Kim HJ, Hawke N, Baldwin AS. NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ. 2006;13:738–47.
41. Atkinson GP, Nozell SE, Benveniste ET. NF-kappaB and STAT3 signaling in glioma: targets for future therapies. Expert Rev Neurother. 2010;10:575–86.