Gene expression signature of c-MYC-immortalized human fibroblasts reveals loss of growth inhibitory response to TGF

Cell Cycle

Volumn 10, Issue 15, 2011, Pages 2540-2548

  Wang, Myra L ^a,b   Walsh, Ryan ^c   Robinson, Kristin L ^a   Burchard, Julja ^c,d   Bartz, Steven R ^c   Cleary, Michele ^c,e   Galloway, Denise A ^a   Grandori, Carla ^a,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c ROSETTA INPHARMATICS   (United States)

^d Sirna Therapeutics Inc   (United States)

^e MERCK RESEARCH LABORATORIES   (United States)

Author keywords

c MYC; Gene expression signature; Immortalization; p27; TGF

Indexed keywords

INTERLEUKIN 6; MYC PROTEIN; PROTEIN P27; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL IMMORTALIZATION; CONTROLLED STUDY; FIBROBLAST; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; ONCOGENE C MYC; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

EID: 79961109928     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.15.16309     Document Type: Article

References (62)

1. Hayflick L. THE LIMITED IN VITRO LIFETIME OF HUMAN DIPLOID CELL STRAINS. Exp Cell Res 1965; 37:614-36; PMID: 14315085; DOI: 10.1016/0014-4827(65)90211-9.
2. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res 1961; 25:585- 621; DOI: 10.1016/0014-4827(61)90192-6.
3. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100:57-70; PMID: 10647931; DOI: 10.1016/S0092-8674(00)81683-9.
4. Kim WY, Sharpless NE. The regulation of INK4/ARF in cancer and aging. Cell 2006; 127:265-75; PMID: 17055429; DOI: 10.1016/j.cell.2006.10.003.
5. Sharpless NE. INK4a/ARF: a multifunctional tumor suppressor locus. Mutat Res 2005; 576:22-38; PMID: 15878778; DOI: 10.1016/j.mrfmmm.2004.08.021.
6. Sherr CJ. The INK4a/ARF network in tumour suppression. Nat Rev Mol Cell Biol 2001; 2:731-7; PMID: 11584300; DOI: 10.1038/35096061.
7. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 2009; 9:400- 14; PMID: 19440234; DOI: 10.1038/nrc2657.
8. Belletti B, Nicoloso MS, Schiappacassi M, Chimienti E, Berton S, Lovat F, et al. p27(kip1) functional regulation in human cancer: a potential target for therapeutic designs. Curr Med Chem 2005; 12:1589-605; PMID: 16022660; DOI: 10.2174/0929867054367149.
9. 1-phase progression. Genes Dev 1999; 13:1501-12; PMID: 10385618; DOI: 10.1101/ gad.13.12.1501.
10. Günes C, Lichtsteiner S, Vasserot AP, Englert C. Expression of the hTERT gene is regulated at the level of transcriptional initiation and repressed by Mad1. Cancer Res 2000; 60:2116-21; PMID: 10786671.
11. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, et al. Extension of life-span by introduction of telomerase into normal human cells. Science 1998; 279:349-52; PMID: 9454332; DOI: 10.1126/ science.279.5349.349.
12. INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 1998; 396:84-8; PMID: 9817205; DOI: 10.1038/23962.
13. Artandi SE, DePinho RA. Telomeres and telomerase in cancer. Carcinogenesis 2010; 31:9-18; PMID: 19887512; DOI: 10.1093/carcin/bgp268.
14. INK4a. Cell 1997; 88:593-602; PMID: 9054499; DOI: 10.1016/ S0092-8674(00)81902-9.
15. Benanti JA, Galloway DA. Normal human fibroblasts are resistant to RAS-induced senescence. Mol Cell Biol 2004; 24:2842-52; PMID: 15024073; DOI: 10.1128/MCB.24.7.2842-52.2004.
16. INK4a determines sensitivity of human cells to transformation by cooperating cellular oncogenes. Cancer Cell 2003; 4:301-10; PMID: 14585357; DOI: 10.1016/S1535-6108(03)00242-3.
17. Benanti JA, Wang ML, Myers HE, Robinson KL, Grandori C, Galloway DA. Epigenetic downregulation of ARF expression is a selection step in immortalization of human fibroblasts by c-Myc. Mol Cancer Res 2007; 5:1181-9; PMID: 17982115; DOI: 10.1158/1541-7786.MCR-06-0372.
18. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 1999; 13:2658-69; PMID: 10541552; DOI: 10.1101/gad.13.20.2658.
19. Blagosklonny MV. Cell cycle arrest is not senescence. Aging (Albany NY) 2011; 3:94-101; PMID: 21297220.
20. Demidenko ZN, Zubova SG, Bukreeva EI, Pospelov VA, Pospelova TV, Blagosklonny MV. Rapamycin decelerates cellular senescence. Cell Cycle 2009; 8:1888-95; PMID: 19471117; DOI: 10.4161/cc.8.12.8606.
21. Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV, Blagosklonny MV. The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging (Albany NY) 2010; 2:344-52; PMID: 20606252.
22. Leontieva OV, Blagosklonny MV. DNA damaging agents and p53 do not cause senescence in quiescent cells, while consecutive re-activation of mTOR is associated with conversion to senescence. Aging (Albany NY) 2010; 2:924-35; PMID: 21212465.
23. Benanti JA, Galloway DA. The normal response to RAS: senescence or transformation? Cell Cycle 2004; 3:715-7; PMID: 15153805; DOI: 10.4161/cc.3.6.948.
24. Massagué J, Blain SW, Lo RS. TGFbeta signaling in growth control, cancer and heritable disorders. Cell 2000; 103:295-309; PMID: 11057902; DOI: 10.1016/S0092-8674(00)00121-5.
25. Massagué J. TGFbeta in Cancer. Cell 2008; 134:215-30; PMID: 18662538; DOI: 10.1016/j. cell.2008.07.001.
26. Pietenpol JA, Holt JT, Stein RW, Moses HL. Transforming growth factor beta1 suppression of c-myc gene transcription: role in inhibition of keratinocyte proliferation. Proc Natl Acad Sci USA 1990; 87:3758-62; PMID: 2187192; DOI: 10.1073/pnas.87.10.3758.
27. Wu S, Hultquist A, Hydbring P, Cetinkaya C, Oberg F, Larsson LG. TGFbeta enforces senescence in Myctransformed hematopoietic tumor cells through induction of Mad1 and repression of Myc activity. Exp Cell Res 2009; 315:3099-111; PMID: 19766114; DOI: 10.1016/j.yexcr.2009.09.009.
28. Shi Y, Massague J. Mechanisms of TGFbeta signaling from cell membrane to the nucleus. Cell 2003; 113:685-700; PMID: 12809600; DOI: 10.1016/S0092-8674(03) 00432-X
29. Zhang YE. Non-Smad pathways in TGFbeta signaling. Cell Res 2009; 19:128-39; PMID: 19114990; DOI: 10.1038/cr.2008.328.
30. Gordon KJ, Blobe GC. Role of transforming growth factor beta superfamily signaling pathways in human disease. Biochim Biophys Acta 2008; 1782:197-228.
31. Ständer M, Naumann U, Wick W, Weller M. Transforming growth factor beta and p-21: multiple molecular targets of decorin-mediated suppression of neoplastic growth. Cell Tissue Res 1999; 296:221-7; PMID: 10382266; DOI: 10.1007/s004410051283.
32. Liu F, Hata A, Baker JC, Doody J, Carcamo J, Harland RM, et al. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 1996; 381:620-3; PMID: 8637600; DOI: 10.1038/381620a0.
33. Sekiya T, Adachi S, Kohu K, Yamada T, Higuchi O, Furukawa Y, et al. Identification of BMP and activin membrane-bound inhibitor (BAMBI), an inhibitor of transforming growth factor beta signaling, as a target of the beta-catenin pathway in colorectal tumor cells. J Biol Chem 2004; 279:6840-6; PMID: 14660579; DOI: 10.1074/jbc.M310876200.
34. Kortlever RM, Nijwening JH, Bernards R. Transforming growth factor beta requires its target plasminogen activator inhibitor-1 for cytostatic activity. J Biol Chem 2008; 283:24308-13; PMID: 18614541; DOI: 10.1074/jbc.M803341200.
35. Irving JA, Pike RN, Lesk AM, Whisstock JC. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res 2000; 10:1845-64; PMID: 11116082; DOI: 10.1101/gr.GR-1478R.
36. INK4B-cdk4 complexes and inhibits cyclin D1-cdk4 association in human mammary epithelial cells. Mol Cell Biol 1997; 17:2458-67; PMID: 9111314.
37. INK4b. Nat Cell Biol 2001; 3:400-8; PMID: 11283614; DOI: 10.1038/35070086.
38. INK4B is a potential effector of TGFbeta-induced cell cycle arrest. Nature 1994; 371:257-61; PMID: 8078588; DOI: 10.1038/371257a0.
39. Kip1. Oncogene 1996; 13:2447-57; PMID: 8957087.
40. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 1995; 92:5545-9; PMID: 7777546; DOI: 10.1073/ pnas.92.12.5545.
41. 1 arrest. J Biol Chem 2002; 277:41686-92; PMID: 12202478; DOI: 10.1074/jbc.M204307200.
42. Lecanda J, Ganapathy V, D'Aquino-Ardalan C, Evans B, Cadacio C, Ayala A, et al. TGFbeta prevents proteasomal degradation of the cyclin-dependent kinase inhibitor p27kip1 for cell cycle arrest. Cell Cycle 2009; 8:742-56; PMID: 19221482; DOI: 10.4161/cc.8.5.7871.
43. Kretzschmar M, Doody J, Timokhina I, Massague J. A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev 1999; 13:804-16; PMID: 10197981; DOI: 10.1101/gad.13.7.804.
44. Letterio J, Rudikoff E, Voong N, Bauer SR. Transforming growth factor-beta1 sensitivity is altered in Abl-Myc- and Raf-Myc-induced mouse pre-Bcell tumors. Stem Cells 2006; 24:2611-7; PMID: 16945999; DOI: 10.1634/stemcells.2005-0623.
45. Bernabeu C, Lopez-Novoa JM, Quintanilla M. The emerging role of TGFbeta superfamily coreceptors in cancer. Biochim Biophys Acta 2009; 1792:954-73.
46. Chen CR, Kang Y, Massague J. Defective repression of c-myc in breast cancer cells: A loss at the core of the transforming growth factor beta growth arrest program. Proc Natl Acad Sci USA 2001; 98:992-9; PMID: 11158583; DOI: 10.1073/pnas.98.3.992.
47. Chen G, Ghosh P, Osawa H, Sasaki CY, Rezanka L, Yang J, et al. Resistance to TGFbeta 1 correlates with aberrant expression of TGFbeta receptor II in human B-cell lymphoma cell lines. Blood 2007; 109:5301-7; PMID: 17339425; DOI: 10.1182/blood-2006-06-032128.
48. Parekh TV, Gama P, Wen X, Demopoulos R, Munger JS, Carcangiu ML, et al. Transforming growth factor beta signaling is disabled early in human endometrial carcinogenesis concomitant with loss of growth inhibition. Cancer Res 2002; 62:2778-90; PMID: 12019154.
49. Diaz-Chavez J, Hernandez-Pando R, Lambert PF, Gariglio P. Downregulation of transforming growth factor-beta type II receptor (TGFbetaRII) protein and mRNA expression in cervical cancer. Mol Cancer 2008; 7:3; PMID: 18184435; DOI: 10.1186/1476-4598-7- 3.
50. Tremain R, Marko M, Kinnimulki V, Ueno H, Bottinger E, Glick A. Defects in TGFbeta signaling overcome senescence of mouse keratinocytes expressing v-Ha-ras. Oncogene 2000; 19:1698-709; PMID: 10763827; DOI: 10.1038/sj.onc. 1203471.
51. Iavarone A, Massague J. Repression of the CDK activator Cdc25A and cell cycle arrest by cytokine TGFbeta in cells lacking the CDK inhibitor p15. Nature 1997; 387:417-22; PMID: 9163429; DOI: 10.1038/387417a0.
52. Spender LC, Inman GJ. TGFbeta induces growth arrest in Burkitt lymphoma cells via transcriptional repression of E2F-1. J Biol Chem 2009; 284:1435-42; PMID: 19022773; DOI: 10.1074/jbc.M808080200.
53. Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 1994; 8:9-22; PMID: 8288131; DOI: 10.1101/gad.8.1.9.
54. Reynisdóttir I, Massague J. The subcellular locations of p15(Ink4b) and p27(Kip1) coordinate their inhibitory interactions with cdk4 and cdk2. Genes Dev 1997; 11:492-503; PMID: 9042862; DOI: 10.1101/gad.11.4.492.
55. Slingerland JM, Hengst L, Pan CH, Alexander D, Stampfer MR, Reed SI. A novel inhibitor of cyclin-Cdk activity detected in transforming growth factor betaarrested epithelial cells. Mol Cell Biol 1994; 14:3683- 94; PMID: 8196612.
56. Warner BJ, Blain SW, Seoane J, Massague J. Myc downregulation by transforming growth factor beta required for activation of the p15(Ink4b) G(1) arrest pathway. Mol Cell Biol 1999; 19:5913-22; PMID: 10454538.
57. Kip1, proliferation and lymphomagenesis. EMBO J 2007; 26:2562-74; PMID: 17464290; DOI: 10.1038/sj.emboj.7601691.
58. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Semin Cancer Biol 2006; 16:253-64; PMID: 16904903; DOI: 10.1016/j.semcancer.2006.07.014.
59. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-76; PMID: 16904174; DOI: 10.1016/j.cell.2006.07.024.
60. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-72; PMID: 18035408; DOI: 10.1016/j.cell.2007.11.019.
61. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-64; PMID: 12925520; DOI: 10.1093/biostatistics/ 4.2.249.
62. Benanti JA, Williams DK, Robinson KL, Ozer HL, Galloway DA. Induction of extracellular matrix-remodeling genes by the senescence-associated protein APA-1. Mol Cell Biol 2002; 22:7385-97; PMID: 12370286; DOI: 10.1128/MCB.22.21. 7385-97.2002.