Induction of cellular senescence by doxorubicin is associated with upregulated miR-375 and induction of autophagy in K562 cells

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Yang, Ming Yu ^a,b   Lin, Pai Mei ^c   Liu, Yi Chang ^b,d   Hsiao, Hui Hua ^b,d   Yang, Wen Chi ^b   Hsu, Jui Feng ^b   Hsu, Cheng Ming ^a   Lin, Sheng Fung ^b,d  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c I SHOU UNIVERSITY   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; DOXORUBICIN; MICRORNA 375; MICRORNA 375 INHIBITOR; NUCLEIC ACID SYNTHESIS INHIBITOR; PROTEIN P14; PROTEIN P16; PROTEIN P53; UNCLASSIFIED DRUG; MICRORNA; MIRN375 MICRORNA, HUMAN; PROTEIN 14 3 3; TRANSCRIPTION FACTOR SP1; YWHAZ PROTEIN, HUMAN;

14 3 3ZETA GENE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; ATG18 GENE; ATG9B GENE; AUTOPHAGY; CELL CYCLE ARREST; CELL DEATH; CELL PROLIFERATION; CELL STRAIN K 562; CELLULAR SENESCENCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; PRECANCER; PROTEIN EXPRESSION; RNA ANALYSIS; SP1 GENE; UPREGULATION; BIOLOGICAL MODEL; CELL AGING; DRUG EFFECT; GENETICS; PHYSIOLOGY; TUMOR SUPPRESSOR GENE;

14-3-3 PROTEINS; AUTOPHAGY; CELL AGING; DOXORUBICIN; GENES, P16; GENES, P53; HUMANS; K562 CELLS; MICRORNAS; MODELS, BIOLOGICAL; SP1 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84861000650     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037205     Document Type: Article

References (57)

1. Shelton DN, Chang E, Whittier PS, Choi D, Funk WD, (1999) Microarray analysis of replicative senescence. Curr. Biol 9: 939-945.
2. Dimri GP, Lee X, Basile G, Acosta M, Scott G, et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92: 9363-9367.
3. Campisi J, d'Adda di Fagagna F, (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8: 729-740.
4. Gruber HE, Hoelscher GL, Ingram JA, Zinchenko N, Hanley EN Jr, (2010) Senescent vs. non-senescent cells in the human annulus in vivo: cell harvest with laser capture microdissection and gene expression studies with microarray analysis. BMC Biotechnol 10: 5.
5. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW, (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602.
6. Campisi J, (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120: 513-522.
7. Jeyapalan JC, Ferreira M, Sedivy JM, Herbig U, (2007) Accumulation of senescent cells in mitotic tissue of aging primates. Mech Ageing Dev 128: 36-44.
8. Fridman AL, Tainsky MA, (2008) Critical pathways in cellular senescence and immortalization revealed by gene expression profiling. Oncogene 27: 5975-5987.
9. Lin HK, Chen Z, Wang G, Nardella C, Lee SW, et al. (2010) Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence. Nature 464: 374-379.
10. Fabian MR, Sonenberg N, Filipowicz W, (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379.
11. Thomas M, Lieberman J, Lal A, (2010) Desperately seeking microRNA targets. Nat Struct Mol Biol 17: 1169-1174.
12. Ambros V, (2004) The functions of animal microRNAs. Nature 431: 350-355.
13. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT, (2005) cMyc-regulated microRNAs modulate E3F1 expression. Nature 435: 839-843.
14. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, et al. (2005) RAS is regulated by the let-7 microRNA family. Cell 120: 635-647.
15. Ivey KN, Srivastava D, (2010) MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7: 36-41.
16. Calin GA, Pekarsky Y, Croce CM, (2007) The role of microRNA and other non-coding RNA in the pathogenesis of chronic lymphocytic leukemia. Best Pract Res Clin Haematol 20: 425-427.
17. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, et al. (2006) Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9: 189-198.
18. Khoshnaw SM, Green AR, Powe DG, Ellis IO, (2009) MicroRNA involvement in the pathogenesis and management of breast cancer. J Clin Pathol 62: 422-428.
19. Farazi TA, Spitzer JI, Morozov P, Tuschl T, (2011) miRNAs in human cancer. J Pathol 223: 102-115.
20. Grillari J, Grillari-Voglauer R, (2010) Novel modulators of senescence, aging, and longevity: Small non-coding RNAs enter the stage. Exp Gerontol 45: 302-311.
21. Hackl M, Brunner S, Fortschegger K, Schreiner C, Micutkova L, et al. (2010) miR-17, miR-19b, miR-20a, and miR-106a are down-regulated in human aging. Aging Cell 9: 291-296.
22. Lafferty-Whyte K, Cairney CJ, Jamieson NB, Oien KA, Keith WN, (2009) Pathway analysis of senescence-associated miRNA targets reveals common processes to different senescence induction mechanisms. Biochim Biophys Acta 1792: 341-352.
23. He L, He X, Lim LP, de Stanchina E, Xuan Z, et al. (2007) A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134.
24. Maes OC, Sarojini H, Wang E, (2009) Stepwise up-regulation of microRNA expression levels from replicating to reversible and irreversible growth arrest states in WI-38 human fibroblasts. J Cell Physiol 221: 109-119.
25. Sugimoto K, Toyoshima H, Sakai R, Miyagawa K, Hagiwara K, et al. (1992) Frequent mutations in the p53 gene in human myeloid leukemia cell lines. Blood 79: 2378-2383.
26. Ogawa S, Hirano N, Sato N, Takahashi T, Hangaishi A, et al. (1994) Homozygous loss of the cyclin-dependent kinase 4-inhibitor (p16) gene in human leukemias. Blood 84: 2431-2435.
27. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L, (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56: 185-229.
28. Faderl S, Kantarjian H, Talpaz M, (1999) Chronic myelogenous leukemia: update on biology and treatment. Oncology 13: 169-180.
29. Narita M, Nunez S, Heard E, Narita M, Lin AW, et al. (2003) Rb-medicated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113: 703-716.
30. Nielsen GP, Stemmer-Rachamimov AO, Shaw J, Roy JE, Koh J, et al. (1999) Immunohistochemical survey of p16INK4A expression in normal human adult and infant tissues. Lab Invest 79 (9): 1137-1143.
31. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Rl-Regaiey K, et al. (2004) Ink4a/Arf expression is a biomarker of aging. J Clin Invest 114 (9): 1299-1307.
32. Artandi SE, Chang S, Lee SL, Alson S, Gottlieb GJ, et al. (2000) Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406: 641-645.
33. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642.
34. Zhang R, Poustovoitov MB, Ye X, Santos HA, Chen W, et al. (2005) Formation of MacroH2A-containing senescence- associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev Cell 8: 19-30.
35. Narita M, Narita M, Krizhanovsky V, Nunez S, Chicas A, et al. (2006) A novel role for high-mobility group A proteins in cellular senescence and heterochromatin formation. Cell 126: 503-514.
36. Czyz M, Jakubowska J, Sztiller-Sikorska M, (2008) STI571/doxorubicin concentration-dependent switch for diverse caspase actions in CML cell line K562. Biochem Pharm 75: 1761-1773.
37. Szulawska A, Arkusinska J, Czyz M, (2007) Accumulation of gamma-globin mRNA and induction of irreversible erythroid differentiation after treatment of CML cell line K562 with new doxorubicin derivatives. Biochem Pharmacol 73: 175-184.
38. Jackson, JG, Pereira-Smith OM, (2006) Primary and compensatory roles for RB family members at cell cycle gene promoters that are deacetylated and downregulated in doxorubicin-induced senescence of breast cancer cells. Mol Cell Biol 26: 2501-2510.
39. Vaz C, Ahmad HM, Sharma P, Gupta R, Kumar L, et al. (2010) Analysis of microRNA transcriptome by deep sequencing of small RNA libraries of peripheral blood. BMC Genomics 11: 288.
40. Tsukamoto Y, Nakda C, Noguchi T, Tanigawa M, Nguyen LT, et al. (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3ζ. Cancer Res 70: 2339-2349.
41. Wach S, Nolte E, Szczyrba J, Stöhr R, Hartmann A, et al. (2011) MicroRNA profiles of prostate carcinoma detected by multiplatform microRNA screening. Int J Cancer Mar 11. doi 10.1002/ijc.26064. [Epub ahead of print].
42. Lajer CB, Nielsen FC, Friis-Hansen L, Norrild B, Borup R, et al. (2011) Different miRNA signatures of oral and pharyngeal squamous cell carcinomas: a prospective translational study. Br J Cancer 104 (5): 830-840.
43. Hui AB, Lenarduzzi M, Krushel T, Waldron L, Pintilie M, et al. (2010) Comprehensive MicroRNA profiling for head and neck squamous cell carcinomas. Clin Cancer Res 16 (4): 1129-1139.
44. Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, et al. (2008) MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 7 (6): 1955-1963.
45. Liu AM, Poon RTP, Luk JM, (2010) MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. 3 Biochem Biophys Res Commun 394 pp. 623-627.
46. Nohata N, Hanazawa T, Kikkawa N, Mutallip M, Sakurai D, et al. (2011) Tumor suppressive microRNA-375 regulates oncogene AEG-1/MTDH in head and neck squamous cell carcinoma (HNSCC). J Hum Genet 56 (8): 595-601.
47. He XX, Chang Y, Meng FY, Wang MY, Xie QH, et al. (2011) MicroRNA-375 targets AEG-1 in hepatocellular carcinoma and suppresses liver cancer cell growth in vitro and in vivo. Oncogene. doi 10.1038/onc.2011.500. [Epub ahead of print] [Epub ahead of print] PubMed PMID.
48. Kong KL, Kwong DL, Chan TH, Law SY, Chen L, et al. (2012) MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut 61 (1): 33-42.
49. Li X, Lin R, Li J, (2011) Epigenetic silencing of microRNA-375 regulates PDK1 expression in esophageal cancer. Dig Dis Sci 56 (10): 2849-2856.
50. Kinoshita T, Nohata N, Yoshino H, Hanazawa T, (2012) Tumor suppressive microRNA-375 regulates lactate dehydrogenase B in maxillary sinus squamous cell carcinoma. Int J Oncol 40 (1): 185-193.
51. Ding L, Xu Y, Zhang W, Deng Y, Si M, et al. (2010) MiR-375 frequently downregulated in gastric cancer inhibits cell proliferation by targeting JAK2. Cell Res 20 (7): 784-93.
52. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, et al. (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70 (6): 2339-2349.
53. Wang F, Li Y, Zhou J, Xu J, Peng C, et al. (2011) miR-375 is down-regulated in squamous cervical cancer and inhibits cell migration and invasion via targeting transcription factor SP1. Am J Pathol 179 (5): 2580-2588.
54. Young AR, Narita M, Ferreira M, Kirschner K, Sadaie M, et al. (2009) Autophagy mediates the mitotic senescence transition. Genes Dev 23: 798-803.
55. Sekito T, Kawamata T, Ichikawa R, Suzuki K, Ohsumi Y, (2009) Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells 4 (5): 525-538.
56. Nair U, Cao Y, Xie Z, Klionsky DJ, (2010) Roles of the lipid-binding motifs of Atg18 and Atg21 in the cytoplasm to vacuole targeting pathway and autophagy. J Biol Chem 285 (15): 11476-11488.
57. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, et al. (2007) Autophagy suppresses tumor progression by limiting chromosomal instability. Gene Dev 21: 1367-1381.