MiR-125b induces cellular senescence in malignant melanoma

BMC Dermatology

Volumn 14, Issue , 2014, Pages

  Nyholm, Anne M ^a   Lerche, Catharina M ^a   Manfé, Valentina ^a   Biskup, Edyta ^a   Johansen, Peter ^a   Morling, Niels ^a   Thomsen, Birthe M ^a   Glud, Martin ^a   Gniadecki, Robert ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Hsa miR 125b; In situ hybridization; Mel Juso; Melanoma; Senescence

Indexed keywords

BETA GALACTOSIDASE; CYCLIN D1; KI 67 ANTIGEN; MICRORNA 125B; PROTEIN P21; PROTEIN P27; PROTEIN P53; MICRORNA; MIRN125 MICRORNA, HUMAN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELLULAR SENESCENCE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CUTANEOUS MELANOMA; CYTOPLASM; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; LYMPH NODE METASTASIS; MALE; MELANOMA; MELANOMA CELL LINE; MOUSE; NONHUMAN; PLASMID; PRIMARY TUMOR; SENESCENCE; STAINING; TUMOR CELL; TUMOR GROWTH; WESTERN BLOTTING; ADULT; AGED; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL AGING; CELL PROLIFERATION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LYMPH NODE; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; UPREGULATION; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CELL AGING; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPH NODES; LYMPHATIC METASTASIS; MALE; MELANOMA; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; TRANSFECTION; TUMOR MARKERS, BIOLOGICAL; UP-REGULATION; YOUNG ADULT;

EID: 84899977134     PISSN: None     EISSN: 14715945     Source Type: Journal    
DOI: 10.1186/1471-5945-14-8     Document Type: Article

References (58)

1. Hayflick L, MOORHEAD PS. The serial cultivation of human diploid cell strains. Exp Cell Res 1961, 25:585-621. 10.1016/0014-4827(61)90192-6, 13905658.
2. Hayflick L. The cell biology of aging. J Invest Dermatol 1979, 73:8-14. 10.1111/1523-1747.ep12532752, 448179.
3. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, Majoor DM, Shay JW, Mooi WJ, Peeper DS. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005, 436:720-724. 10.1038/nature03890, 16079850.
4. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 1990, 345:458-460. 10.1038/345458a0, 2342578.
5. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M, Benguria A, Zaballos A, Flores JM, Barbacid M, Beach D, Serrano M. Tumour biology: senescence in premalignant tumours. Nature 2005, 436:642. 10.1038/436642a, 16079833.
6. Collado M, Serrano M. The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 2006, 6:472-476. 10.1038/nrc1884, 16723993.
7. Collado M, Serrano M. Senescence in tumours: evidence from mice and humans. Nat Rev Cancer 2010, 10:51-57. 10.1038/nrc2772, 3672965, 20029423.
8. Choi J, Shendrik I, Peacocke M, Peehl D, Buttyan R, Ikeguchi EF, Katz AE, Benson MC. Expression of senescence-associated beta-galactosidase in enlarged prostates from men with benign prostatic hyperplasia. Urology 2000, 56:160-166. 10.1016/S0090-4295(00)00538-0, 10869659.
9. Majumder PK, Grisanzio C, O'Connell F, Barry M, Brito JM, Xu Q, Guney I, Berger R, Herman P, Bikoff R, Fedele G, Baek WK, Wang S, Ellwood-Yen K, Wu H, Sawyers CL, Signoretti S, Hahn WC, Loda M, Sellers WR. A prostatic intraepithelial neoplasia-dependent p27 Kip1 checkpoint induces senescence and inhibits cell proliferation and cancer progression. Cancer Cell 2008, 14:146-155. 10.1016/j.ccr.2008.06.002, 2583442, 18691549.
10. Braig M, Lee S, Loddenkemper C, Rudolph C, Peters AH, Schlegelberger B, Stein H, Dorken B, Jenuwein T, Schmitt CA. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 2005, 436:660-665. 10.1038/nature03841, 16079837.
11. Serrano M. Shifting senescence into quiescence by turning up p53. Cell Cycle 2010, 9:4256-4257. 10.4161/cc.9.21.13785, 3578181, 20980826.
12. Gewirtz DA, Holt SE, Elmore LW. Accelerated senescence: an emerging role in tumor cell response to chemotherapy and radiation. Biochem Pharmacol 2008, 76:947-957. 10.1016/j.bcp.2008.06.024, 18657518.
13. Giuliano S, Ohanna M, Ballotti R, Bertolotto C. Advances in melanoma senescence and potential clinical application. Pigment Cell Melanoma Res 2010, 24:295-308.
14. Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012, 13:271-282.
15. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
16. Farh KK, Grimson A, Jan C, Lewis BP, Johnston WK, Lim LP, Burge CB, Bartel DP. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 2005, 310:1817-1821. 10.1126/science.1121158, 16308420.
17. Kato M, Slack FJ. microRNAs: small molecules with big roles - C. elegans to human cancer. Biol Cell 2008, 100:71-81. 10.1042/BC20070078, 18199046.
18. He X, He L, Hannon GJ. The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Res 2007, 67:11099-11101. 10.1158/0008-5472.CAN-07-2672, 18056431.
19. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D. miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Proc Natl Acad Sci U S A 2011, 108:522-527. 10.1073/pnas.1017346108, 3021067, 21187425.
20. Menghini R, Casagrande V, Cardellini M, Martelli E, Terrinoni A, Amati F, Vasa-Nicotera M, Ippoliti A, Novelli G, Melino G, Lauro R, Federici M. MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation 2009, 120:1524-1532. 10.1161/CIRCULATIONAHA.109.864629, 19786632.
21. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010, 11:252-263.
22. Benhamed M, Herbig U, Ye T, Dejean A, Bischof O. Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nat Cell Biol 2012, 14:266-275. 10.1038/ncb2443, 22366686.
23. Noguchi S, Mori T, Otsuka Y, Yamada N, Yasui Y, Iwasaki J, Kumazaki M, Maruo K, Akao Y. Anti-oncogenic microRNA-203 induces senescence by targeting E2F3 in human melanoma cells. J Biol Chem 2012, 287:11769-11777. 10.1074/jbc.M111.325027, 3320925, 22354972.
24. Kozubek J, Ma Z, Fleming E, Duggan T, Wu R, Shin DG, Dadras SS. In-depth characterization of microRNA transcriptome in melanoma. PLoS One 2013, 8:e72699. 10.1371/journal.pone.0072699, 3762816, 24023765.
25. Dar AA, Majid S, De SD, Nosrati M, Bezrookove V, Kashani-Sabet M. miRNA-205 suppresses melanoma cell proliferation and induces senescence via regulation of E2F1 protein. J Biol Chem 2011, 286:16606-16614. 10.1074/jbc.M111.227611, 3089503, 21454583.
26. Glud M, Rossing M, Hother C, Holst L, Hastrup N, Nielsen FC, Gniadecki R, Drzewiecki KT. Downregulation of miR-125b in metastatic cutaneous malignant melanoma. Melanoma Res 2010, 20:479-484. 10.1097/CMR.0b013e32833e32a1, 20827223.
27. Kim KH, Bin BH, Kim J, Son ED, Park PJ, Choi H, Kim BJ, Yu SJ, Kang H, Kang HH, Cho EG, Lee TR. Novel inhibitory function of miR-125b in Melanogenesis. Pigment Cell Melanoma Res 2013, 27:140-144.
28. Kappelmann M, Kuphal S, Meister G, Vardimon L, Bosserhoff AK. MicroRNA miR-125b controls melanoma progression by direct regulation of c-Jun protein expression. Oncogene 2013, 32:2984-2991. 10.1038/onc.2012.307, 22797068.
29. Guan Y, Yao H, Zheng Z, Qiu G, Sun K. MiR-125b targets BCL3 and suppresses ovarian cancer proliferation. Int J Cancer 2010, 128:2274-2283.
30. Huang L, Luo J, Cai Q, Pan Q, Zeng H, Guo Z, Dong W, Huang J, Lin T. MicroRNA-125b suppresses the development of bladder cancer by targeting E2F3. Int J Cancer 2010, 128:1758-1769.
31. Hui AB, Lenarduzzi M, Krushel T, Waldron L, Pintilie M, Shi W, Perez-Ordonez B, Jurisica I, O'Sullivan B, Waldron J, Gullane P, Cummings B, Liu FF. Comprehensive MicroRNA profiling for head and neck squamous cell carcinomas. Clin Cancer Res 2010, 16:1129-1139. 10.1158/1078-0432.CCR-09-2166, 20145181.
32. Baffa R, Fassan M, Volinia S, O'Hara B, Liu CG, Palazzo JP, Gardiman M, Rugge M, Gomella LG, Croce CM, Rosenberg A. MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J Pathol 2009, 219:214-221. 10.1002/path.2586, 19593777.
33. Schaefer A, Jung M, Mollenkopf HJ, Wagner I, Stephan C, Jentzmik F, Miller K, Lein M, Kristiansen G, Jung K. Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int J Cancer 2010, 126:1166-1176.
34. Veerla S, Lindgren D, Kvist A, Frigyesi A, Staaf J, Persson H, Liedberg F, Chebil G, Gudjonsson S, Borg A, Mansson W, Rovira C, Hoglund M. MiRNA expression in urothelial carcinomas: important roles of miR-10a, miR-222, miR-125b, miR-7 and miR-452 for tumor stage and metastasis, and frequent homozygous losses of miR-31. Int J Cancer 2009, 124:2236-2242. 10.1002/ijc.24183, 19127597.
35. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce CM. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A 2004, 101:2999-3004. 10.1073/pnas.0307323101, 365734, 14973191.
36. Glud M, Manfe V, Biskup E, Holst L, Dirksen AM, Hastrup N, Nielsen FC, Drzewiecki KT, Gniadecki R. MicroRNA miR-125b induces senescence in human melanoma cells. Melanoma Res 2011, 21:253-256. 10.1097/CMR.0b013e328345333b, 21460750.
37. UCSC genoma bioinfromatics 2013, http://genome-euro.ucsc.edu/.
38. Voorhoeve PM, Ie SC, Schrier M, Gillis AJ, Stoop H, Nagel R, Liu YP, van DJ, Drost J, Griekspoor A, Zlotorynski E, Yabuta N, De VG, Nojima H, Looijenga LH, Agami R. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 2006, 124:1169-1181. 10.1016/j.cell.2006.02.037, 16564011.
39. Kamstrup MR, Gjerdrum LM, Biskup E, Lauenborg BT, Ralfkiaer E, Woetmann A, Odum N, Gniadecki R. Notch1 as a potential therapeutic target in cutaneous T-cell lymphoma. Blood 2010, 116:2504-2512. 10.1182/blood-2009-12-260216, 20538790.
40. Holst LM, Kaczkowski B, Gniadecki R. Reproducible pattern of microRNA in normal human skin. Exp Dermatol 2010, 19:e201-e205. 10.1111/j.1600-0625.2009.01049.x, 20201961.
41. Holst LM, Kaczkowski B, Glud M, Futoma-Kazmierczak E, Hansen LF, Gniadecki R. The microRNA molecular signature of atypic and common acquired melanocytic nevi: differential expression of miR-125b and let-7c. Exp Dermatol 2011, 20:278-280. 10.1111/j.1600-0625.2010.01163.x, 21166724.
42. Ziegler-Heitbrock HW, Munker R, Johnson J, Petersmann I, Schmoeckel C, Riethmuller G. In vitro differentiation of human melanoma cells analyzed with monoclonal antibodies. Cancer Res 1985, 45:1344-1350.
43. Wach F, Eyrich AM, Wustrow T, Krieg T, Hein R. Comparison of migration and invasiveness of epithelial tumor and melanoma cells in vitro. J Dermatol Sci 1996, 12:118-126. 10.1016/0923-1811(95)00470-X, 8814543.
44. Fidler IJ. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res 1978, 38:2651-2660.
45. Hoek KS, Schlegel NC, Brafford P, Sucker A, Ugurel S, Kumar R, Weber BL, Nathanson KL, Phillips DJ, Herlyn M, Schadendorf D, Dummer R. Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res 2006, 19:290-302. 10.1111/j.1600-0749.2006.00322.x, 16827748.
46. Enomoto Y, Kitaura J, Hatakeyama K, Watanuki J, Akasaka T, Kato N, Shimanuki M, Nishimura K, Takahashi M, Taniwaki M, Haferlach C, Siebert R, Dyer MJ, Asou N, Aburatani H, Nakakuma H, Kitamura T, Sonoki T. Emu/miR-125b transgenic mice develop lethal B-cell malignancies. Leukemia 2011, 25:1849-1856. 10.1038/leu.2011.166, 21738213.
47. Bousquet M, Harris MH, Zhou B, Lodish HF. MicroRNA miR-125b causes leukemia. Proc Natl Acad Sci U S A 2010, 107:21558-21563. 10.1073/pnas.1016611107, 3003065, 21118985.
48. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes Dev 2009, 23:862-876. 10.1101/gad.1767609, 2666337, 19293287.
49. Chaudhuri AA, So AY, Mehta A, Minisandram A, Sinha N, Jonsson VD, Rao DS, O'Connell RM, Baltimore D. Oncomir miR-125b regulates hematopoiesis by targeting the gene Lin28A. Proc Natl Acad Sci U S A 2012, 109:4233-4238. 10.1073/pnas.1200677109, 3306721, 22366319.
50. Yan D, Zhou X, Chen X, Hu DN, Dong XD, Wang J, Lu F, Tu L, Qu J. MicroRNA-34a inhibits uveal melanoma cell proliferation and migration through downregulation of c-Met. Invest Ophthalmol Vis Sci 2009, 50:1559-1565.
51. Jeffries CD, Fried HM, Perkins DO. Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 2011, 17:675-686. 10.1261/rna.2006511, 3062178, 21363885.
52. Ohrt T, Muetze J, Svoboda P, Schwille P. Intracellular localization and routing of miRNA and RNAi pathway components. Curr Top Med Chem 2012, 12:79-88. 10.2174/156802612798919132, 22196276.
53. Liao JY, Ma LM, Guo YH, Zhang YC, Zhou H, Shao P, Chen YQ, Qu LH. Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 3′ trailers. PLoS One 2010, 5:e10563. 10.1371/journal.pone.0010563, 2871053, 20498841.
54. Gu Y, Sun J, Groome LJ, Wang Y. Differential miRNA expression profiles between the first and third trimester human placentas. Am J Physiol Endocrinol Metab 2013, 304:E836-E843. 10.1152/ajpendo.00660.2012, 3625781, 23443922.
55. Vacchi-Suzzi C, Hahne F, Scheubel P, Marcellin M, Dubost V, Westphal M, Boeglen C, Buchmann-Moller S, Cheung MS, Cordier A, De BC, Deurinck M, Frei M, Moulin P, Oakeley E, Grenet O, Grevot A, Stull R, Theil D, Moggs JG, Marrer E, Couttet P. Heart structure-specific transcriptomic atlas reveals conserved microRNA-mRNA interactions. PLoS One 2013, 8:e52442. 10.1371/journal.pone.0052442, 3534709, 23300973.
56. Manfe V, Biskup E, Willumsgaard A, Skov AG, Palmieri D, Gasparini P, Lagana A, Woetmann A, Odum N, Croce CM, Gniadecki R. cMyc/miR-125b-5p signalling determines sensitivity to bortezomib in preclinical model of cutaneous T-cell lymphomas. PLoS One 2013, 8:e59390. 10.1371/journal.pone.0059390, 3602111, 23527180.
57. Xu N, Zhang L, Meisgen F, Harada M, Heilborn J, Homey B, Grander D, Stahle M, Sonkoly E, Pivarcsi A. MicroRNA-125b down-regulates matrix metallopeptidase 13 and inhibits cutaneous squamous cell carcinoma cell proliferation, migration, and invasion. J Biol Chem 2012, 287:29899-29908. 10.1074/jbc.M112.391243, 3436131, 22782903.
58. Arora A, Guduric-Fuchs J, Harwood L, Dellett M, Cogliati T, Simpson DA. Prediction of microRNAs affecting mRNA expression during retinal development. BMC Dev Biol 2010, 10:1. 10.1186/1471-213X-10-1, 2821300, 20053268.