Cyclin C is a haploinsufficient tumour suppressor

Nature Cell Biology

Volumn 16, Issue 11, 2014, Pages 1080-1091

  Li, Na ^a,b   Fassl, Anne ^a,b   Chick, Joel ^b   Inuzuka, Hiroyuki ^b   Li, Xiaoyu ^a,b   Mansour, Marc R ^a,b,c,d   Liu, Lijun ^a,b   Wang, Haizhen ^a,b   King, Bryan ^e   Shaik, Shavali ^b   Gutierrez, Alejandro ^a,b,c   Ordureau, Alban ^b   Otto, Tobias ^a,b   Kreslavsky, Taras ^a,b   Baitsch, Lukas ^a,b   Bury, Leah ^a,b   Meyer, Clifford A ^a,f   Ke, Nan ^a,b   Mulry, Kristin A ^a,b   Kluk, Michael J ^b   Roy, Moni ^b   Kim, Sunkyu ^g   Zhang, Xiaowu ^h   Geng, Yan ^a,b   Zagozdzon, Agnieszka ^a,b   Jenkinson, Sarah ^d   Gale, Rosemary E ^d   Linch, David C ^d   Zhao, Jean J ^a,b   Mullighan, Charles G ⁱ   Harper, J Wade ^b   Aster, Jon C ^b   Aifantis, Iannis ^e   Von Boehmer, Harald ^a,b   Gygi, Steven P ^b   Wei, Wenyi ^b   Look, A Thomas ^a,b,c   Sicinski, Piotr ^a,b   more..

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^h CELL SIGNALING TECHNOLOGY   (United States)

ⁱ ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYCLIN C; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 3; CYCLIN DEPENDENT KINASE 8; NOTCH1 RECEPTOR; ONCOPROTEIN; PROTEIN CDK19; PROTEIN ICN1; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; EMBRYO; GENE DELETION; GENETIC CODE; HAPLOINSUFFICIENCY; HETEROZYGOSITY; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; T CELL LEUKEMIA; TUMOR SUPPRESSOR GENE; ANIMAL; CELL CULTURE; GENETICS; KNOCKOUT MOUSE; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; CYCLIN C; CYCLIN-DEPENDENT KINASE 3; CYCLIN-DEPENDENT KINASE 8; CYCLIN-DEPENDENT KINASES; HUMANS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTOR, NOTCH1;

EID: 84908489045     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3046     Document Type: Article

References (70)

1. Leopold, P. & O'Farrell, P. H. An evolutionarily conserved cyclin homolog from Drosophila rescues yeast deficient in G1 cyclins. Cell 66, 1207-1216 (1991).
2. Lew, D. J., Dulic, V. & Reed, S. I. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell 66, 1197-1206 (1991).
3. Malumbres, M. & Barbacid, M. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 9, 153-166 (2009).
4. Liu, Z. J. et al. A critical role for cyclin C in promotion of the hematopoietic cell cycle by cooperation with c-Myc. Mol. Cell Biol. 18, 3445-3454 (1998).
5. Makkonen, K. M., Malinen, M., Ropponen, A., Vaisanen, S. & Carlberg, C. Cell cycle regulatory effects of retinoic acid and forskolin are mediated by the cyclin C gene. J. Mol. Biol. 393, 261-271 (2009).
6. Miyata, Y. et al. Cyclin C regulates human hematopoietic stem/progenitor cell quiescence. Stem Cells 28, 308-317 (2010).
7. Ren, S. & Rollins, B. J. Cyclin C/cdk3 promotes Rb-dependent G0 exit. Cell 117, 239-251 (2004).
8. Saxena, U. H. et al. Phosphorylation by cyclin C/cyclin-dependent kinase 2 following mitogenic stimulation of murine fibroblasts inhibits transcriptional activity of LSF during G1 progression. Mol. Cell Biol. 29, 2335-2345 (2009).
9. Hengartner, C. J. et al. Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol. Cell 2, 43-53 (1998).
10. Leclerc, V., Tassan, J. P., O'Farrell, P. H., Nigg, E. A. & Leopold, P. Drosophila Cdk8, a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II. Mol. Biol. Cell 7, 505-513 (1996).
11. Liao, S. M. et al. A kinase-cyclin pair in the RNA polymerase II holoenzyme. Nature 374, 193-196 (1995).
12. Maldonado, E. et al. A human RNA polymerase II complex associated with SRB and DNA-repair proteins. Nature 381, 86-89 (1996).
13. Rickert, P., Seghezzi, W., Shanahan, F., Cho, H. & Lees, E. Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II. Oncogene 12, 2631-2640 (1996).
14. Tassan, J. P., Jaquenoud, M., Leopold, P., Schultz, S. J. & Nigg, E. A. Identification of human cyclin-dependent kinase 8, a putative protein kinase partner for cyclin C. Proc. Natl Acad. Sci. USA 92, 8871-8875 (1995).
15. Akoulitchev, S., Chuikov, S. & Reinberg, D. TFIIH is negatively regulated by cdk8-containing mediator complexes. Nature 407, 102-106 (2000).
16. Elmlund, H. et al. The cyclin-dependent kinase 8 module sterically blocks Mediator interactions with RNA polymerase II. Proc. Natl Acad. Sci. USA 103, 15788-15793 (2006).
17. Knuesel, M. T., Meyer, K. D., Bernecky, C. & Taatjes, D. J. The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function. Genes Dev. 23, 439-451 (2009).
18. Alarcon, C. et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways. Cell 139, 757-769 (2009).
19. Chi, Y. et al. Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15, 1078-1092 (2001).
20. Fryer, C. J., White, J. B. & Jones, K. A. Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol. Cell 16, 509-520 (2004).
21. Nelson, C., Goto, S., Lund, K., Hung, W. & Sadowski, I. Srb10/Cdk8 regulates yeast filamentous growth by phosphorylating the transcription factor Ste12. Nature 421, 187-190 (2003).
22. Donner, A. J., Szostek, S., Hoover, J. M. & Espinosa, J. M. CDK8 is a stimulus-specific positive coregulator of p53 target genes. Mol. Cell 27, 121-133 (2007).
23. Firestein, R. et al. CDK8 is a colorectal cancer oncogene that regulates β-catenin activity. Nature 455, 547-551 (2008).
24. Morris, E. J. et al. E2F1 represses β-catenin transcription and is antagonized by both pRB and CDK8. Nature 455, 552-556 (2008).
25. Donner, A. J., Ebmeier, C. C., Taatjes, D. J. & Espinosa, J. M. CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat. Struct. Mol. Biol. 17, 194-201 (2010).
26. Furumoto, T. et al. A kinase subunit of the human mediator complex, CDK8, positively regulates transcriptional activation. Genes Cells 12, 119-132 (2007).
27. Li, H. et al. Molecular cloning and chromosomal localization of the human cyclin C (CCNC) and cyclin E (CCNE) genes: deletion of the CCNC gene in human tumors. Genomics 32, 253-259 (1996).
28. Ohata, N. et al. Highly frequent allelic loss of chromosome 6q16-23 in osteosarcoma: involvement of cyclin C in osteosarcoma. Int. J. Mol. Med. 18, 1153-1158 (2006).
29. Bondi, J. et al. Expression and gene amplification of primary (A, B1, D1, D3, and E) and secondary (C and H) cyclins in colon adenocarcinomas and correlation with patient outcome. J. Clin. Pathol. 58, 509-514 (2005).
30. Galamb, O. et al. Evaluation of malignant and benign gastric biopsy specimens by mRNA expression profile and multivariate statistical methods. Cytometry B Clin. Cytom. 72, 299-309 (2007).
31. Husdal, A., Bukholm, G. & Bukholm, I. R. The prognostic value and overexpression of cyclin A is correlated with gene amplification of both cyclin A and cyclin E in breast cancer patient. Cell Oncol. 28, 107-116 (2006).
32. Iqbal, J. et al. Clinical implication of genome-wide profiling in diffuse large B-cell lymphoma and other subtypes of B-cell lymphoma. Indian J. Cancer 44, 72-86 (2007).
33. Xu, W. & Ji, J. Y. Dysregulation of CDK8 and Cyclin C in tumorigenesis. J. Genet. Genomics 38, 439-452 (2011).
34. Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99-103 (1999).
35. Ye, X., Zhu, C. & Harper, J. W. A premature-termination mutation in the Mus musculus cyclin-dependent kinase 3 gene. Proc. Natl Acad. Sci. USA 98, 1682-1686 (2001).
36. Kuhn, R., Schwenk, F., Aguet, M. & Rajewsky, K. Inducible gene targeting in mice. Science 269, 1427-1429 (1995).
37. Malumbres, M. Physiological relevance of cell cycle kinases. Physiol. Rev. 91, 973-1007 (2011).
38. Welcker, M. & Clurman, B. E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8, 83-93 (2008).
39. Weng, A. P. et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306, 269-271 (2004).
40. Thompson, B. J. et al. The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia. J. Exp. Med. 204, 1825-1835 (2007).
41. Chiang, M. Y. et al. Leukemia-associated NOTCH1 alleles are weak tumor initiators but accelerate K-ras-initiated leukemia. J. Clin. Invest. 118, 3181-3194 (2008).
42. Boehm, T., Foroni, L., Kaneko, Y., Perutz, M. F. & Rabbitts, T. H. The rhombotin family of cysteine-rich LIM-domain oncogenes: distinct members are involved in T-cell translocations to human chromosomes 11p15 and 11p13. Proc. Natl Acad. Sci. USA 88, 4367-4371 (1991).
43. Larson, R. C. et al. T cell tumours of disparate phenotype in mice transgenic for Rbtn-2. Oncogene 9, 3675-3681 (1994).
44. McGuire, E. A., Rintoul, C. E., Sclar, G. M. & Korsmeyer, S. J. Thymic overexpression of Ttg-1 in transgenic mice results in T-cell acute lymphoblastic leukemia/lymphoma. Mol. Cell Biol. 12, 4186-4196 (1992).
45. Lin, Y. W., Nichols, R. A., Letterio, J. J. & Aplan, P. D. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 107, 2540-2543 (2006).
46. O'Neil, J. et al. Activating Notch1 mutations in mouse models of T-ALL. Blood 107, 781-785 (2006).
47. Hyytinen, E. R. et al. Defining the region(s) of deletion at 6q16-q22 in human prostate cancer. Genes Chromosomes Cancer 34, 306-312 (2002).
48. Orphanos, V. et al. Allelic imbalance of chromosome 6q in ovarian tumours. Br. J. Cancer 71, 666-669 (1995).
49. Utada, Y. et al. Mapping of target regions of allelic loss in primary breast cancers to 1-cM intervals on genomic contigs at 6q21 and 6q25.3. Jpn. J. Cancer Res. 91, 293-300 (2000).
50. Zhang, Y. et al. A 3-cM commonly deleted region in 6q21 in leukemias and lymphomas delineated by fluorescence in situ hybridization. Genes Chromosomes Cancer 27, 52-58 (2000).
51. Mansour, M. R. et al. Prognostic implications of NOTCH1 and FBXW7 mutations in adults with T-cell acute lymphoblastic leukemia treated on the MRC UKALLXII/ECOG E2993 protocol. J. Clin. Oncol. 27, 4352-4356 (2009).
52. Koch, U. & Radtke, F. Notch signaling in solid tumors. Curr. Top Dev. Biol. 92, 411-55 (2010).
53. Jackson, A. et al. Deletion of 6q16-q21 in human lymphoid malignancies: a mapping and deletion analysis. Cancer Res. 60, 2775-2779 (2000).
54. Sinclair, P. B. et al. A fluorescence in situ hybridization map of 6q deletions in acute lymphocytic leukemia: identification and analysis of a candidate tumor suppressor gene. Cancer Res. 64, 4089-4098 (2004).
55. Lobry, C., Oh, P., Mansour, M. R., Look, A. T. & Aifantis, I. Notch signaling: switching an oncogene to a tumor suppressor. Blood 123, 2451-2459 (2014).
56. Agrawal, N. et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 333, 1154-1157 (2011).
57. Nicolas, M. et al. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33, 416-421 (2003).
58. Stransky, N. et al. The mutational landscape of head and neck squamous cell carcinoma. Science 333, 1157-1160 (2011).
59. King, B. et al. The ubiquitin ligase FBXW7 modulates leukemia-initiating cell activity by regulating MYC stability. Cell 153, 1552-1566 (2013).
60. Li, X., Gounari, F., Protopopov, A., Khazaie, K. & von Boehmer, H. Oncogenesis of T-ALL and nonmalignant consequences of overexpressing intracellular NOTCH1. J. Exp. Med. 205, 2851-2861 (2008).
61. Chiang, M. Y. et al. Identification of a conserved negative regulatory sequence that influences the leukemogenic activity of NOTCH1. Mol. Cell Biol. 26, 6261-6271 (2006).
62. βTRCP ubiquitin ligase. Cancer Cell 18, 147-159 (2010).
63. Emmerich, C. H. et al. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl Acad. Sci. USA 110, 15247-15252 (2013).
64. Vrooman, L. M. et al. Postinduction dexamethasone and individualized dosing of Escherichia coli L-asparaginase each improve outcome of children and adolescents with newly diagnosed acute lymphoblastic leukemia: results from a randomized study-Dana-Farber Cancer Institute ALL Consortium Protocol 00-01. J. Clin. Oncol. 31, 1202-1210 (2013).
65. Winter, S. S. et al. Identification of genomic classifiers that distinguish induction failure in T-lineage acute lymphoblastic leukemia: a report from the children's oncology group. Blood 110, 1429-1438 (2007).
66. Gutierrez, A. et al. Inactivation of LEF1 in T-cell acute lymphoblastic leukemia. Blood 115, 2845-2851 (2010).
67. Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012).
68. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
69. Mansour, M. R. et al. Notch-1 mutations are secondary events in some patients with T-cell acute lymphoblastic leukemia. Clin. Cancer Res. 13, 6964-6969 (2007).
70. Mansour, M. R., Linch, D. C., Foroni, L., Goldstone, A. H. & Gale, R. E. High incidence of Notch-1 mutations in adult patients with T-cell acute lymphoblastic leukemia. Leukemia 20, 537-539 (2006).