Notch1 modulates timing of G1-S progression by inducing SKP2 transcription and p27Kip1 degradation

Journal of Experimental Medicine

Volumn 202, Issue 1, 2005, Pages 157-168

  Sarmento, Leonor M ^a,c   Huang, Hui ^a   Limon, Ana ^a,d   Gordon, William ^a   Fernandes, Jacquenilson ^a   Tavares, Maria J ^b   Miele, Lucio ^e   Cardoso, Angelo A ^b   Classon, Marie ^a   Carlesso, Nadia ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF LISBON   (Portugal)

^d Science Research Laboratory Inc   (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; F BOX PROTEIN; LIGAND; NOTCH1 RECEPTOR; PROTEASOME; PROTEIN SUBUNIT; S PHASE KINASE ASSOCIATED PROTEIN 2; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE SILENCING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION;

3T3 CELLS; ANIMALS; BASE SEQUENCE; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DNA; G1 PHASE; HUMANS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; RECEPTOR, NOTCH1; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; S PHASE; S-PHASE KINASE-ASSOCIATED PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN;

EID: 22344435698     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20050559     Document Type: Article

References (44)

1. Artavanis-Tsakonas, S., M.D. Rand, and R.J. Lake. 1999. Notch signaling: cell fate control and signal integration in development. Science. 284:770-776.
2. De Strooper, B., W. Annaert, P. Cupers, P. Saftig, K. Craessaerts, J.S. Mumm, E.H. Schroeter, V. Schrijvers, M.S. Wolfe, W.J. Ray, et al. 1999. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:518-522.
3. Davis, R.L., and D.L. Turner. 2001. Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene. 20:8342-8357.
4. Rangarajan, A., C. Talora, R. Okuyama, M. Nicolas, C. Mammucari, H. Oh, J.C. Aster, S. Krishna, D. Metzger, P. Chambon, et al. 2001. Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. EMBO J. 20:3427-3436.
5. Stier, S., T. Cheng, D. Dombkowski, N. Carlesso, and D.T. Scadden. 2002. Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood. 99: 2369-2378.
6. Carlesso, N., J.C. Aster, J. Sklar, and D.T. Scadden. 1999. Notch1-induced delay of human hematopoietic progenitor cell differentiation is associated with altered cell cycle kinetics. Blood. 93:838-848.
7. Ronchini, C., and A.J. Capobianco. 2001. Induction of cyclin D1 transcription and CDK2 activity by Notch(ic): implication for cell cycle disruption in transformation by Notch(ic). Mol. Cell. Biol. 21:5925-5934.
8. Pear, W.S., J.C. Aster, M.L. Scott, R.P. Hasserjian, B. Soffer, J. Sklar, and D. Baltimore. 1996. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183:2283-2291.
9. Nicolas, M., A. Wolfer, K. Raj, J.A. Kummer, P. Mill, M. Van Noort, C.C. Hui, H. Clevers, G.P. Dotto, and F. Radtke. 2003. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33:416-421.
10. Sherr, C.J., and J.M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501-1512.
11. Cheng, T., N. Rodrigues, H. Shen, Y. Yang, D. Dombkowski, M. Sykes, and D.T. Scadden. 2000. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science. 287:1804-1808.
12. Cheng, T., N. Rodrigues, D. Dombkowski, S. Stier, and D.T. Scadden. 2000. Stem cell repopulation efficiency but not pool size is governed by p27(kip1). Nat. Med. 6:1235-1240.
13. Fero, M.L., M. Rivkin, M. Tasch, P. Porter, C.E. Carow, E. Firpo, K. Polyak, L.H. Tsai, V. Broudy, R.M. Perlmutter, et al. 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell. 85:733-744.
14. Carrano, A.C., E. Eytan, A. Hershko, and M. Pagano. 1999. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1:193-199.
15. Bornstein, G., J. Bloom, D. Sitry-Shevah, K. Nakayama, M. Pagano, and A. Hershko. 2003. Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J. Biol. Chem. 278:25752-25757.
16. Classon, M., S. Salama, C. Gorka, R. Mulloy, P. Braun, and E. Harlow. 2000. Combinatorial roles for pRB, p107, and p130 in E2F-mediated cell cycle control. Proc. Natl. Acad. Sci. USA. 97:10820-10825.
17. Berezovska, O., C. Jack, P. McLean, J.C. Aster, C. Hicks, W. Xia, M.S. Wolfe, W.T. Kimberly, G. Weinmaster, D.J. Selkoe, and B.T. Hyman. 2000. Aspartate mutations in presenilin and gamma-secretase inhibitors both impair notch1 proteolysis and nuclear translocation with relative preservation of notch1 signaling. J. Neurochem. 75:583-593.
18. Weng, A.P., Y. Nam, M.S. Wolfe, W.S. Pear, J.D. Griffin, S.C. Blacklow, and J.C. Aster. 2003. Growth suppression of pre-T acute lymphoblastic leukemia cells by inhibition of notch signaling. Mol. Cell. Biol. 23:655-664.
19. Pagano, M., S.W. Tam, A.M. Theodoras, P. Beer-Romero, G. Del Sal, V. Chau, P.R. Yew, G.F. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science. 269:682-685.
20. Nakayama, K., H. Nagahama, Y.A. Minamishima, M. Matsumoto, I. Nakamichi, K. Kitagawa, M. Shirane, R. Tsunematsu, T. Tsukiyama, N. Ishida, et al. 2000. Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J. 19:2069-2081.
21. Spruck, C., H. Strohmaier, M. Watson, A.P. Smith, A. Ryan, T.W. Krek, and S.I. Reed. 2001. A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol. Cell. 7:639-650.
22. Tun, T., Y. Hamaguchi, N. Matsunami, T. Furukawa, T. Honjo, and M. Kawaichi. 1994. Recognition sequence of a highly conserved DNA binding protein RBP-J kappa. Nucleic Acids Res. 22:965-971.
23. Aster, J.C., E.S. Robertson, R.P. Hasserjian, J.R. Turner, E. Kieff, and J. Sklar. 1997. Oncogenic forms of NOTCH1 lacking either the primary binding site for RBP-Jkappa or nuclear localization sequences retain the ability to associate with RBP-Jkappa and activate transcription. J. Biol. Chem. 272:11336-11343.
24. Milner, L.A., and A. Bigas. 1999. Notch as a mediator of cell fate determination in hematopoiesis: evidence and speculation. Blood. 93: 2431-2448.
25. Bennaceur-Griscelli, A., C. Tourino, B. Izac, W. Vainchenker, and L. Coulombel. 1999. Murine stromal cells counteract the loss of long-term culture-initiating cell potential induced by cytokines in CD34(+) CD38(low/neg) human bone marrow cells. Blood. 94:529-538.
26. Dow, R., J. Hendley, A. Pirkmaier, E.A. Musgrove, and D. Germain. 2001. Retinoic acid-mediated growth arrest requires ubiquitylation and degradation of the F-box protein Skp2. J. Biol. Chem. 276:45945-45951.
27. Yasutomo, K., C. Doyle, L. Miele, C. Fuchs, and R.N. Germain. 2000. The duration of antigen receptor signalling determines CD4+ versus CD8+ T-cell lineage fate. Nature. 404:506-510.
28. Cheng, P., A. Zlobin, V. Volgina, S. Gottipati, B. Osborne, E.J. Simel, L. Miele, and D.I. Gabrilovich. 2001. Notch-1 regulates NF-kappaB activity in hemopoietic progenitor cells. J. Immunol. 167:4458-4467.
29. Mancini, S.J., N. Mantei, A. Dumortier, U. Suter, H.R. Macdonald, and F. Radtke. 2004. Jagged1 dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood. 105: 2340-2342.
30. Calvi, L.M., G.B. Adams, K.W. Weibrecht, J.M. Weber, D.P. Olson, M.C. Knight, R.P. Martin, E. Schipani, P. Divieti, F.R. Bringhurst, et al. 2003. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 425:841-846.
31. Pardee, A.B. 1989. G1 events and regulation of cell proliferation. Science. 246:603-608.
32. Cereseto, A., and S. Tsai. 2000. Jagged2 induces cell cycling in confluent fibroblasts susceptible to density-dependent inhibition of cell division. J. Cell. Physiol. 185:425-431.
33. Nie, L., M. Xu, A. Vladimirova, and X.H. Sun. 2003. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J. 22:5780-5792.
34. Rao, P., and T. Kadesch. 2003. The intracellular form of notch blocks transforming growth factor beta-mediated growth arrest in Mv1Lu epithelial cells. Mol. Cell. Biol. 23:6694-6701.
35. Bocchetta, M., L. Miele, H.I. Pass, and M. Carbone. 2003. Notch-1 induction, a novel activity of SV40 required for growth of SV40-transformed human mesothelial cells. Oncogene. 22:81-89.
36. Sriuranpong, V., M.W. Borges, R.K. Ravi, D.R. Arnold, B.D. Nelkin, S.B. Baylin, and D.W. Ball. 2001. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res. 61:3200-3205.
37. Varnum-Finney, B., C. Brashem-Stein, and I.D. Bernstein. 2003. Combined effects of Notch signaling and cytokines induce a multiple log increase in precursors with lymphoid and myeloid reconstituting ability. Blood. 101:1784-1789.
38. Ellisen, L.W., J. Bird, D.C. West, A.L. Soreng, T.C. Reynolds, S.D. Smith, and J. Sklar. 1991. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell. 66:649-661.
39. Pagano, M., and R. Benmaamar. 2003. When protein destruction runs amok, malignancy is on the loose. Cancer Cell. 4:251-256.
40. Latres, E., R. Chiarle, B.A. Schulman, N.P. Pavletich, A. Pellicer, G. Inghirami, and M. Pagano. 2001. Role of the F-box protein Skp2 in lymphomagenesis. Proc. Natl. Acad. Sci. USA. 98:2515-2520.
41. Robertson, E.S., S. Grossman, E. Johannsen, C. Miller, J. Lin, B. Tomkinson, and E. Kieff. 1995. Epstein-Barr virus nuclear protein 3C modulates transcription through interaction with the sequence-specific DNA-binding protein J kappa. J. Virol. 69:3108-3116.
42. Jarriault, S., C. Brou, F. Logeat, E.H. Schroeter, R. Kopan, and A. Israel. 1995. Signalling downstream of activated mammalian Notch. Nature. 377:355-358.
43. Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods. 11:205-214.
44. Nikolic, B., J.P. Gardner, D.T. Scadden, J.S. Arn, D.H. Sachs, and M. Sykes. 1999. Normal development in porcine thymus grafts and specific tolerance of human T cells to porcine donor MHC. J. Immunol. 162:3402-3407.