Skp2 directs Myc-mediated suppression of p27Kip1 yet has modest effects on Myc-driven lymphomagenesis

Molecular Cancer Research

Volumn 8, Issue 3, 2010, Pages 353-362

  Old, Jennifer B ^a,e   Kratzat, Susanne ^b   Hoellein, Alexander ^b   Graf, Steffi ^b   Nilsson, Jonas A ^a,f   Nilsson, Lisa ^a,f   Nakayama, Keiichi I ^c   Peschel, Christian ^b   Cleveland, John L ^a,d   Keller, Ulrich B ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c KYUSHU UNIVERSITY   (Japan)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e ISI Forensics Inc   (United States)

^f UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; S PHASE KINASE ASSOCIATED PROTEIN 2; TRANSCRIPTION FACTOR E2F1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; LYMPHOMA; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL;

ANIMALS; CARRIER PROTEINS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOMA, B-CELL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-MYC; S-PHASE KINASE-ASSOCIATED PROTEINS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

MUS MUSCULUS;

EID: 77949681500     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-09-0232     Document Type: Article

References (65)

1. 1-phase progression. Genes Dev 1999;13:1501-12.
2. Coats S, Flanagan WM, Nourse J, Roberts JM. Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 1996;272:877-80.
3. Kiyokawa H, Kineman RD, Manova-Todorova KO, et al. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 1996;85:721-32.
4. Fero ML, Rivkin M, Tasch M, et al. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 1996;85:733-44.
5. Slingerland J, Pagano M. Regulation of the cdk inhibitor p27 and its deregulation in cancer. J Cell Physiol 2000;183:10-7.
6. Philipp-Staheli J, Payne SR, Kemp CJ. p27(Kip1): regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp Cell Res 2001;264:148-68.
7. Fero ML, Randel E, Gurley KE, Roberts JM, Kemp CJ. The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 1998;396:177-80.
8. Muller D, Bouchard C, Rudolph B, et al. Cdk2-dependent phosphorylation of p27 facilitates its Myc-induced release from cyclin E/cdk2 complexes. Oncogene 1997;15:2561-76.
9. Montagnoli A, Fiore F, Eytan E, et al. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev 1999;13:1181-9.
10. 1 and S phase. Nature 2001;413:323-7.
11. Bartek J, Lukas J. Cell cycle. Order from destruction. Science 2001; 294:66-7.
12. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1999;1:193-9.
13. Ganoth D, Bornstein G, Ko TK, et al. The cell-cycle regulatory protein Cks1 is required for SCF(Skp2)-mediated ubiquitinylation of p27. Nat Cell Biol 2001;3:321-4.
14. Spruck C, Strohmaier H, Watson M, et al. A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol Cell 2001;7:639-50.
15. Kudo Y, Kitajima S, Sato S, Miyauchi M, Ogawa I, Takata T. High expression of S-phase kinase-interacting protein 2, human F-box protein, correlates with poor prognosis in oral squamous cell carcinomas. Cancer Res 2001;61:7044-7.
16. Shim EH, Johnson L, Noh HL, et al. Expression of the F-box protein SKP2 induces hyperplasia, dysplasia, and low-grade carcinoma in the mouse prostate. Cancer Res 2003;63:1583-8.
17. Nakayama K, Nagahama H, Minamishima YA, et al. Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J 2000;19:2069-81.
18. Henriksson M, Luscher B. Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv Cancer Res 1996; 68:109-82.
19. Nilsson JA, Cleveland JL. Myc pathways provoking cell suicide and cancer. Oncogene 2003;22:9007-21.
20. Welcker M, Orian A, Jin J, et al. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci U S A 2004;101:9085-90.
21. Liu J, Levens D. Making myc. Curr Top Microbiol Immunol 2006;302: 1-32.
22. Boxer LM, Dang CV. Translocations involving c-myc and c-myc function. Oncogene 2001;20:5595-610.
23. Cavalieri F, Goldfarb M. Growth factor-deprived BALB/c 3T3 murine fibroblasts can enter the S phase after induction of c-myc gene expression. Mol Cell Biol 1987;7:3554-60.
24. Roussel MF, Cleveland JL, Shurtleff SA, Sherr CJ. Myc rescue of a mutant CSF-1 receptor impaired in mitogenic signalling. Nature 1991;353:361-3.
25. Coppola JA, Cole MD. Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature 1986;320:760-3.
26. Askew DS, Ashmun RA, Simmons BC, Cleveland JL. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 1991;6: 1915-22.
27. Zindy F, Eischen CM, Randle DH, et al. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 1998;12:2424-33.
28. Eischen CM, Woo D, Roussel MF, Cleveland JL. Apoptosis triggered by Myc-induced suppression of Bcl-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol Cell Biol 2001;21:5063-70.
29. 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.
30. Vlach J, Hennecke S, Alevizopoulos K, Conti D, Amati B. Growth arrest by the cyclin-dependent kinase inhibitor p27Kip1 is abrogated by c-Myc. EMBO J 1996;15:6595-604.
31. Keller UB, Old JB, Dorsey FC, et al. Myc targets Cks1 to provoke the suppression of p27(Kip1), proliferation and lymphomagenesis. EMBO J 2007;26:2562-74.
32. Polyak K, Lee MH, Erdjument-Bromage H, et al. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 1994;78:59-66.
33. Yang W, Shen J, Wu M, et al. Repression of transcription of the p27 (Kip1) cyclin-dependent kinase inhibitor gene by c-Myc. Oncogene 2001;20:1688-702.
34. Baudino TA, Maclean KH, Brennan J, et al. Myc-mediated proliferation and lymphomagenesis, but not apoptosis, are compromised by E2f1 loss. Mol Cell 2003;11:905-14.
35. 1/Sregulatory genes. Mol Cell Biol 1995;15:4215-24.
36. Bouchard C, Thieke K, Maier A, et al. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. EMBO J 1999;18:5321-33.
37. Hermeking H, Rago C, Schuhmacher M, et al. Identification of CDK4 as a target of c-MYC. Proc Natl Acad Sci U S A 2000;97: 2229-34.
38. Pagano M, Tam SW, Theodoras AM, et al. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 1995;269:682-5.
39. O'Hagan RC, Ohh M, David G, et al. Myc-enhanced expression of Cul1 promotes ubiquitin-dependent proteolysis and cell cycle progression. Genes Dev 2000;14:2185-91.
40. Martins CP, Berns A. Loss of p27(Kip1) but not p21(Cip1) decreases survival and synergizes with MYC in murine lymphomagenesis. EMBO J 2002;21:3739-48.
41. Adams JM, Harris AW, Pinkert CA, et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 1985;318:533-8.
42. Yamasaki L, Jacks T, Bronson R, Goillot E, Harlow E, Dyson NJ. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 1996; 85:537-48.
43. Yokoi S, Yasui K, Mori M, Iizasa T, Fujisawa T, Inazawa J. Amplification and overexpression of SKP2 are associated with metastasis of non-small-cell lung cancers to lymph nodes. Am J Pathol 2004;165: 175-80.
44. Maclean KH, Keller UB, Rodriguez-Galindo C, Nilsson JA, Cleveland JL. c-Myc augments ã irradiation-induced apoptosis by suppressing Bcl-XL. Mol Cell Biol 2003;23:7256-70.
45. Bello-Fernandez C, Packham G, Cleveland JL. The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc Natl Acad Sci U S A 1993;90:7804-8.
46. Blackwood EM, Eisenman RN. Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science 1991;251:1211-7.
47. Zeller KI, Jegga AG, Aronow BJ, O'Donnell KA, Dang CV. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol 2003;4:R69.
48. Latres E, Chiarle R, Schulman BA, et al. Role of the F-box protein Skp2 in lymphomagenesis. Proc Natl Acad Sci U S A 2001;98: 2515-20.
49. Zhang L, Wang C. F-box protein Skp2: a novel transcriptional target of E2F. Oncogene 2006;25:2615-27.
50. Vigo E, Muller H, Prosperini E, et al. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol Cell Biol 1999;19:6379-95.
51. Kim SY, Herbst A, Tworkowski KA, Salghetti SE, Tansey WP. Skp2 regulates Myc protein stability and activity. Mol Cell 2003; 11:1177-88.
52. von der Lehr N, Johansson S, Wu S, et al. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol Cell 2003;11:1189-200.
53. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B. Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 2001;15:2069-82.
54. Lewis BC, Shim H, Li Q, et al. Identification of putative c-Myc-responsive genes: characterization of rcl, a novel growth-related gene. Mol Cell Biol 1997;17:4967-78.
55. Morris MC, Kaiser P, Rudyak S, Baskerville C, Watson MH, Reed SI. Cks1-dependent proteasome recruitment and activation of CDC20 transcription in budding yeast. Nature 2003;423:1009-13.
56. Yu VP, Baskerville C, Grunenfelder B, Reed SI. A kinase-independent function of Cks1 and Cdk1 in regulation of transcription. Mol Cell 2005;17:145-51.
57. Westbrook L, Manuvakhova M, Kern FG, Estes NR II, Ramanathan HN, Thottassery JV. Cks1 regulates cdk1 expression: a novel role during mitotic entry in breast cancer cells. Cancer Res 2007;67: 11393-401.
58. Zhan F, Colla S, Wu X, et al. CKS1B, overexpressed in aggressive disease, regulates multiple myeloma growth and survival through SKP2- and p27Kip1-dependent and -independent mechanisms. Blood 2007;109:4995-5001.
59. Yang G, Ayala G, De Marzo A, et al. Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. Clin Cancer Res 2002;8:3419-26.
60. Salghetti SE, Kim SY, Tansey WP. Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J 1999;18:717-26.
61. Sidman CL, Denial TM, Marshall JD, Roths JB. Multiple mechanisms of tumorigenesis in Eμ-myc transgenic mice. Cancer Res 1993;53: 1665-9.
62. Yada M, Hatakeyama S, Kamura T, et al. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J 2004;23:2116-25.
63. Adhikary S, Marinoni F, Hock A, et al. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 2005;123:409-21.
64. Reichert M, Saur D, Hamacher R, Schmid RM, Schneider G. Phosphoinositide-3-kinase signaling controls S-phase kinase-associated protein 2 transcription via E2F1 in pancreatic ductal adenocarcinoma cells. Cancer Res 2007;67:4149-56.
65. Wang IC, Chen YJ, Hughes D, et al. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol 2005;25:10875-94.