Notch signaling induces SKP2 expression and promotes reduction of p27Kip1 in T-cell acute lymphoblastic leukemia cell lines

Experimental Cell Research

Volumn 313, Issue 14, 2007, Pages 3141-3152

  Dohda, Takeaki ^a   Maljukova, Aljona ^b   Liu, Lining ^a   Heyman, Mats ^b   Grandér, Dan ^b   Brodin, David ^a   Sangfelt, Olle ^b   Lendahl, Urban ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

c Myc; Cancer; Cell cycle; CSL; Hes; Hey; Notch; p27; Skp2; T ALL

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; NOTCH1 RECEPTOR; S PHASE KINASE ASSOCIATED PROTEIN 2;

ACUTE LYMPHOBLASTIC LEUKEMIA; ALLELE; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME INDUCTION; GENE ACTIVATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T CELL LEUKEMIA;

EID: 34547484864     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.04.027     Document Type: Article

References (42)

1. Grabher C., von Boehmer H., and Look A.T. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat. Rev., Cancer 6 (2006) 347-359
2. Ellisen L.W., Bird J., West D.C., Soreng A.L., Reynolds T.C., Smith S.D., and Sklar J. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66 (1991) 649-661
3. Weng A.P., Ferrando A.A., Lee W., Morris J.P.t., Silverman L.B., Sanchez-Irizarry C., Blacklow S.C., Look A.T., and Aster J.C. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306 (2004) 269-271
4. Maillard I., Fang T., and Pear W.S. Regulation of lymphoid development, differentiation, and function by the Notch pathway. Annu. Rev. Immunol. 23 (2005) 945-974
5. Kadesch T. Notch signaling: the demise of elegant simplicity. Curr. Opin. Genet. Dev. 14 (2004) 506-512
6. Aster J.C. Deregulated NOTCH signaling in acute T-cell lymphoblastic leukemia/lymphoma: new insights, questions, and opportunities. Int. J. Hematol. 82 (2005) 295-301
7. Chiang M.Y., Xu M.L., Histen G., Shestova O., Roy M., Nam Y., Blacklow S.C., Sacks D.B., Pear W.S., and Aster J.C. Identification of a conserved negative regulatory sequence that influences the leukemogenic activity of NOTCH1. Mol. Cell. Biol. 26 (2006) 6261-6271
8. Lin Y.W., Nichols R.A., Letterio J.J., and Aplan P.D. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 107 (2006) 2540-2543
9. O'Neil J., Calvo J., McKenna K., Krishnamoorthy V., Aster J.C., Bassing C.H., Alt F.W., Kelliher M., and Look A.T. Activating Notch1 mutations in mouse models of T-ALL. Blood 107 (2006) 781-785
10. Girard L., Hanna Z., Beaulieu N., Hoemann C.D., Simard C., Kozak C.A., and Jolicoeur P. Frequent provirus insertional mutagenesis of Notch1 in thymomas of MMTVD/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis. Genes Dev. 10 (1996) 1930-1944
11. Feldman B.J., Hampton T., and Cleary M.L. A carboxy-terminal deletion mutant of Notch1 accelerates lymphoid oncogenesis in E2A-PBX1 transgenic mice. Blood 96 (2000) 1906-1913
12. Dumortier A., Jeannet R., Kirstetter P., Kleinmann E., Sellars M., dos Santos N.R., Thibault C., Barths J., Ghysdael J., Punt J.A., Kastner P., and Chan S. Notch activation is an early and critical event during T-cell leukemogenesis in Ikaros-deficient mice. Mol. Cell. Biol. 26 (2006) 209-220
13. Iso T., Kedes L., and Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J. Cell. Physiol. 194 (2003) 237-255
14. Kageyama R., Ohtsuka T., Hatakeyama J., and Ohsawa R. Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306 (2005) 343-348
15. Domenga V., Fardoux P., Lacombe P., Monet M., Maciazek J., Krebs L.T., Klonjkowski B., Berrou E., Mericskay M., Li Z., Tournier-Lasserve E., Gridley T., and Joutel A. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 18 (2004) 2730-2735
16. Lefort K., and Dotto G.P. Notch signaling in the integrated control of keratinocyte growth/differentiation and tumor suppression. Semin. Cancer Biol. 14 (2004) 374-386
17. Reschly E.J., Spaulding C., Vilimas T., Graham W.V., Brumbaugh R.L., Aifantis I., Pear W.S., and Kee B.L. Notch1 promotes survival of E2A-deficient T cell lymphomas through pre-T cell receptor-dependent and -independent mechanisms. Blood 107 (2006) 4115-4121
18. Weng A.P., Millholland J.M., Yashiro-Ohtani Y., Arcangeli M.L., Lau A., Wai C., Del Bianco C., Rodriguez C.G., Sai H., Tobias J., Li Y., Wolfe M.S., Shachaf C., Felsher D., Blacklow S.C., Pear W.S., and Aster J.C. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20 (2006) 2096-2109
19. Nakayama K.I., and Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev., Cancer 6 (2006) 369-381
20. Carrano A.C., Eytan E., Hershko A., and Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1 (1999) 193-199
21. Heyman M., Grander D., Brondum-Nielsen K., Cederblad B., Liu Y., Xu B., and Einhorn S. Interferon system defects in malignant T-cells. Leukemia 8 (1994) 425-434
22. Grander D., Heyman M., Brondum-Nielsen K., Liu Y., Lundgren E., Soderhall S., and Einhorn S. Interferon system in primary acute lymphocytic leukemia cells with or without deletions of the alpha-/beta-interferon genes. Blood 79 (1992) 2076-2083
23. Oberg C., Li J., Pauley A., Wolf E., Gurney M., and Lendahl U. The Notch intracellular domain is ubiquitinated and negatively regulated by the mammalian Sel-10 homolog. J. Biol. Chem. 276 (2001) 35847-35853
24. Kato H., Taniguchi Y., Kurooka H., Minoguchi S., Sakai T., Nomura-Okazaki S., Tamura K., and Honjo T. Involvement of RBP-J in biological functions of mouse Notch1 and its derivatives. Development 124 (1997) 4133-4141
25. Hansson E.M., Teixeira A.I., Gustafsson M.V., Dohda T., Chapman G., Meletis K., Muhr J., and Lendahl U. Recording Notch signaling in real time. Dev. Neurosci. 28 (2006) 118-127
26. Gustafsson M.V., Zheng X., Pereira T., Gradin K., Jin S., Lundkvist J., Ruas J.L., Poellinger L., Lendahl U., and Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9 (2005) 617-628
27. Choi J.W., Pampeno C., Vukmanovic S., and Meruelo D. Characterization of the transcriptional expression of Notch-1 signaling pathway members, Deltex and HES-1, in developing mouse thymocytes. Dev. Comp. Immunol. 26 (2002) 575-588
28. Sarmento L.M., Huang H., Limon A., Gordon W., Fernandes J., Tavares M.J., Miele L., Cardoso A.A., Classon M., and Carlesso N. Notch1 modulates timing of G1-S progression by inducing SKP2 transcription and p27 Kip1 degradation. J. Exp. Med. 202 (2005) 157-168
29. Crespo M., Bosch F., Villamor N., Bellosillo B., Colomer D., Rozman M., Marce S., Lopez-Guillermo A., Campo E., and Montserrat E. ZAP-70 expression as a surrogate for immunoglobulin-variable-region mutations in chronic lymphocytic leukemia. N. Engl. J. Med. 348 (2003) 1764-1775
30. Murata K., Hattori M., Hirai N., Shinozuka Y., Hirata H., Kageyama R., Sakai T., and Minato N. Hes1 directly controls cell proliferation through the transcriptional repression of p27Kip1. Mol. Cell. Biol. 25 (2005) 4262-4271
31. Bloom J., and Pagano M. Deregulated degradation of the cdk inhibitor p27 and malignant transformation. Semin. Cancer Biol. 13 (2003) 41-47
32. Yokoi S., Yasui K., Saito-Ohara F., Koshikawa K., Iizasa T., Fujisawa T., Terasaki T., Horii A., Takahashi T., Hirohashi S., and Inazawa J. A novel target gene, SKP2, within the 5p13 amplicon that is frequently detected in small cell lung cancers. Am. J. Pathol. 161 (2002) 207-216
33. Nakayama K., Nagahama H., Minamishima Y.A., Matsumoto M., Nakamichi I., Kitagawa K., Shirane M., Tsunematsu R., Tsukiyama T., Ishida N., Kitagawa M., and Hatakeyama S. Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. Embo J. 19 (2000) 2069-2081
34. Kossatz U., Dietrich N., Zender L., Buer J., Manns M.P., and Malek N.P. Skp2-dependent degradation of p27kip1 is essential for cell cycle progression. Genes Dev. 18 (2004) 2602-2607
35. Nakayama K., Nagahama H., Minamishima Y.A., Miyake S., Ishida N., Hatakeyama S., Kitagawa M., Iemura S., Natsume T., and Nakayama K.I. Skp2-mediated degradation of p27 regulates progression into mitosis. Dev. Cell 6 (2004) 661-672
36. Cheng T., Rodrigues N., Dombkowski D., Stier S., and Scadden D.T. Stem cell repopulation efficiency but not pool size is governed by p27(kip1). Nat. Med. 6 (2000) 1235-1240
37. Latres E., Chiarle R., Schulman B.A., Pavletich N.P., Pellicer A., Inghirami G., and Pagano M. Role of the F-box protein Skp2 in lymphomagenesis. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2515-2520
38. Andreu E.J., Lledo E., Poch E., Ivorra C., Albero M.P., Martinez-Climent J.A., Montiel-Duarte C., Rifon J., Perez-Calvo J., Arbona C., Prosper F., and Perez-Roger I. BCR-ABL induces the expression of Skp2 through the PI3K pathway to promote p27Kip1 degradation and proliferation of chronic myelogenous leukemia cells. Cancer Res. 65 (2005) 3264-3272
39. Yada M., Hatakeyama S., Kamura T., Nishiyama M., Tsunematsu R., Imaki H., Ishida N., Okumura F., Nakayama K., and Nakayama K.I. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. Embo J. 23 (2004) 2116-2125
40. Sjoblom T., Jones S., Wood L.D., Parsons D.W., Lin J., Barber T., Mandelker D., Leary R.J., Ptak J., Silliman N., Szabo S., Buckhaults P., Farrell C., Meeh P., Markowitz S.D., Willis J., Dawson D., Willson J.K., Gazdar A.F., Hartigan J., Wu L., Liu C., Parmigiani G., Park B.H., Bachman K.E., Papadopoulos N., Vogelstein B., Kinzler K.W., and Velculescu V.E. The Consensus Coding Sequences of Human Breast and Colorectal Cancers. Science 314 5797 (2006) 268-274
41. A. Malyukova, T. Dohda, N. von der Lehr, S. Akhondi, M. Corcoran, M. Heyman, C. Spruck, D. Grandér, U. Lendahl, O. Sangfelt, The tumor suppressor gene hCDC4 is frequently mutated in human T-cell acute lymphoblastic leukemia with functional consequences for Notch signaling. Cancer Research (in press).
42. Palomero T., Lim W.K., Odom D.T., Sulis M.L., Real P.J., Margolin A., Barnes K.C., O'Neil J., Neuberg D., Weng A.P., Aster J.C., Sigaux F., Soulier J., Look A.T., Young R.A., Califano A., and Ferrando A.A. NOTCH1 directly regulates c-MYC and activates a feed-forward loop transcriptional network promoting leukemic cell growth. Proc. Natl. Acad. Sci. U.S.A. 103 48 (2006) 18261-18266