Ablation of the Kinase NDR1 Predisposes Mice to the Development of T Cell Lymphoma

Science Signaling

Volumn 3, Issue 126, 2010, Pages

  Cornils, Hauke ^a   Stegert, Mario R ^a   Hergovich, Alexander ^a   Hynx, Debby ^a   Schmitz, Debora ^a   Dirnhofer, Stephan ^b   Hemmings, Brian A ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN STE20 LIKE KINASE 1; NUCLEAR DBF2 RELATED 1 PROTEIN; NUCLEAR DBF2 RELATED 2 PROTEIN; PROTEIN KINASE; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; NDR1 PROTEIN KINASE, MOUSE; NDR2 PROTEIN KINASE, MOUSE; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL TYPE; CONTROLLED STUDY; GENE EXPRESSION; GENOTYPE; MOUSE; NONHUMAN; PERIPHERAL T CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; THYMOCYTE; ANIMAL; DEFICIENCY; HUMAN; KNOCKOUT MOUSE; LYMPHOMA, T-CELL; PHYSIOLOGY;

ANIMALS; APOPTOSIS; HUMANS; LYMPHOMA, T-CELL; MICE; MICE, KNOCKOUT; PROTEIN-SERINE-THREONINE KINASES;

MAMMALIA; MUS;

EID: 77953815913     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000681     Document Type: Article

References (50)

1. R. C. Taylor, S. P. Cullen, S. J. Martin, Apoptosis: Controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9, 231-241 (2008).
2. M. Kurokawa, S. Kornbluth, Caspases and kinases in a death grip. Cell 138, 838-854 (2009).
3. M. Radu, J. Chernoff, The DeMSTification of mammalian Ste20 kinases. Curr. Biol. 19, R421-R425 (2009).
4. A. Vichalkovski, E. Gresko, H. Cornils, A. Hergovich, D. Schmitz, B. A. Hemmings, NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr. Biol. 18, 1889-1895 (2008).
5. E. H. Chan, M. Nousiainen, R. B. Chalamalasetty, A. Schäfer, E. A. Nigg, H. H. Sillje, The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24, 2076-2086 (2005).
6. A. Hergovich, M. R. Stegert, D. Schmitz, B. A. Hemmings, NDR kinases regulate essential cell processes from yeast to humans. Nat. Rev. Mol. Cell Biol. 7, 253-264 (2006).
7. D. Pan, Hippo signaling in organ size control. Genes Dev. 21, 886-897 (2007).
8. Q. Zeng, W. Hong, The emerging role of the Hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 13, 188-192 (2008).
9. S. Chiba, M. Ikeda, K. Katsunuma, K. Ohashi, K. Mizuno, MST2- and Furry-mediated activation of NDR1 kinase is critical for precise alignment of mitotic chromosomes. Curr. Biol. 19, 675-681 (2009).
10. A. Hergovich, S. Lamla, E. A. Nigg, B. A. Hemmings, Centrosome-associated NDR kinase regulates centrosome duplication. Mol. Cell 25, 625-634 (2007).
11. M. R. Stegert, R. Tamaskovic, S. J. Bichsel, A. Hergovich, B. A. Hemmings, Regulation of NDR2 protein kinase by multi-site phosphorylation and the S100B calciumbinding protein. J. Biol. Chem. 279, 23806-23812 (2004).
12. W. Geng, B. He, M. Wang, P. N. Adler, The tricornered gene, which is required for the integrity of epidermal cell extensions, encodes the Drosophila nuclear DBF2-related kinase. Genetics 156, 1817-1828 (2000).
13. T. S. Fenske, C. McMahon, D. Edwin, J. C. Jarvis, J. M. Cheverud, M. Minn, V. Mathews, M. A. Bogue, M. A. Province, H. L. McLeod, T. A. Graubert, Identification of candidate alkylator-induced cancer susceptibility genes by whole genome scanning in mice. Cancer Res. 66, 5029-5038 (2006).
14. J. M. Joslin, A. A. Fernald, T. R. Tennant, E. M. Davis, S. C. Kogan, J. Anastasi, J. D. Crispino, M. M. Le Beau, Haploinsufficiency of EGR1, a candidate gene in the del(5q), leads to the development of myeloid disorders. Blood 110, 719-726 (2007).
15. C. Geisen, H. Karsunky, R. Yucel, T. Moroy, Loss of p27Kip1 cooperates with cyclin E in T-cell lymphomagenesis. Oncogene 22, 1724-1729 (2003).
16. Kip1 insufficiency. Cancer Cell 5, 177-189 (2004).
17. C. A. Heckman, H. Duan, P. B. Garcia, L. M. Boxer, Oct transcription factors mediate t(14;18) lymphoma cell survival by directly regulating bcl-2 expression. Oncogene 25, 888-898 (2006).
18. T. Miyazaki, Y. Hirokami, N. Matsuhashi, H. Takatsuka, M. Naito, Increased susceptibility of thymocytes to apoptosis in mice lacking AIM, a novel murine macrophage-derived soluble factor belonging to the scavenger receptor cysteine-rich domain superfamily. J. Exp. Med. 189, 413-422 (1999).
19. S. Nagel, C. Meyer, H. Quentmeier, M. Kaufmann, H. G. Drexler, R. A. MacLeod, MEF2C is activated by multiple mechanisms in a subset of T-acute lymphoblastic leukemia cell lines. Leukemia 22, 600-607 (2008).
20. D. J. Burgess, J. Doles, L. Zender, W. Xue, B. Ma, W. R. McCombie, G. J. Hannon, S. W. Lowe, M. T. Hemann, Topoisomerase levels determine chemotherapy response in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 105, 9053-9058 (2008).
21. M. S. Kulkarni, J. L. Daggett, T. P. Bender, W. M. Kuehl, P. L. Bergsagel, M. E. Williams, Frequent inactivation of the cyclin-dependent kinase inhibitor p18 by homozygous deletion in multiple myeloma cell lines: Ectopic p18 expression inhibits growth and induces apoptosis. Leukemia 16, 127-134 (2002).
22. A. R. Mendelsohn, J. D. Hamer, Z. B. Wang, R. Brent, Cyclin D3 activates Caspase 2, connecting cell proliferation with cell death. Proc. Natl. Acad. Sci. U.S.A. 99, 6871-6876 (2002).
23. K. Tsuchihara, V. Lapin, C. Bakal, H. Okada, L. Brown, M. Hirota-Tsuchihara, K. Zaugg, A. Ho, A. Itie-Youten, M. Harris-Brandts, R. Rottapel, C. D. Richardson, S. Benchimol, T. W. Mak, Ckap2 regulates aneuploidy, cell cycling, and cell death in a p53-dependent manner. Cancer Res. 65, 6685-6691 (2005).
24. B. L. Kee, E and ID proteins branch out. Nat. Rev. Immunol. 9, 175-184 (2009).
25. G. Bain, I. Engel, E. C. Robanus Maandag, H. P. te Riele, J. R. Voland, L. L. Sharp, J. Chun, B. Huey, D. Pinkel, C. Murre, E2A deficiency leads to abnormalities in αβ T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17, 4782-4791 (1997).
26. J. O'Neil, J. Shank, N. Cusson, C. Murre, M. Kelliher, TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Cancer Cell 5, 587-596 (2004).
27. W. Yan, A. Z. Young, V. C. Soares, R. Kelley, R. Benezra, Y. Zhuang, High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell. Biol. 17, 7317-7327 (1997).
28. M. Santarosa, A. Ashworth, Haploinsufficiency for tumour suppressor genes: When you don't need to go all the way. Biochim. Biophys. Acta 1654, 105-122 (2004).
29. A. Raval, S. M. Tanner, J. C. Byrd, E. B. Angerman, J. D. Perko, S. S. Chen, B. Hackanson, M. R. Grever, D. M. Lucas, J. J. Matkovic, T. S. Lin, T. J. Kipps, F. Murray, D. Weisenburger, W. Sanger, J. Lynch, P. Watson, M. Jansen, Y. Yoshinaga, R. Rosenquist, P. J. de Jong, P. Coggill, S. Beck, H. Lynch, A. de la Chapelle, C. Plass, Downregulation of deathassociated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia. Cell 129, 879-890 (2007).
30. L. Valle, T. Serena-Acedo, S. Liyanarachchi, H. Hampel, I. Comeras, Z. Li, Q. Zeng, H. T. Zhang, M. J. Pennison, M. Sadim, B. Pasche, S. M. Tanner, A. de la Chapelle, Germline allele-specific expression of TGFBR1 confers an increased risk of colorectal cancer. Science 321, 1361-1365 (2008).
31. H. Yan, Z. Dobbie, S. B. Gruber, S. Markowitz, K. Romans, F. M. Giardiello, K. W. Kinzler, B. Vogelstein, Small changes in expression affect predisposition to tumorigenesis. Nat. Genet. 30, 25-26 (2002).
32. D. Hanahan, R. A. Weinberg, The hallmarks of cancer. Cell 100, 57-70 (2000).
33. R. Hakem, J. L. de la Pompa, C. Sirard, R. Mo, M. Woo, A. Hakem, A. Wakeham, J. Potter, A. Reitmair, F. Billia, E. Firpo, C. C. Hui, J. Roberts, J. Rossant, T. W. Mak, The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85, 1009-1023 (1996).
34. -/- fibrosarcomas is associated with elevated levels of cyclin kinase inhibitors p21 and p27. Mol. Cell. Biol. 25, 4565-4578 (2005).
35. X. Yang, C. Li, X. Xu, C. Deng, The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc. Natl. Acad. Sci. U.S.A. 95, 3667-3672 (1998).
36. I. Engel, C. Murre, Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proc. Natl. Acad. Sci. U.S.A. 96, 996-1001 (1999).
37. Y. Harima, K. Harima, S. Sawada, Y. Tanaka, S. Arita, T. Ohnishi, Loss of heterozygosity on chromosome 6p21.2 as a potential marker for recurrence after radiotherapy of human cervical cancer. Clin. Cancer Res. 6, 1079-1085 (2000).
38. R. Lukeis, L. Irving, M. Garson, S. Hasthorpe, Cytogenetics of non-small cell lung cancer: Analysis of consistent non-random abnormalities. Genes Chromosomes Cancer 2, 116-124 (1990).
39. R. Morita, J. Ishikawa, M. Tsutsumi, K. Hikiji, Y. Tsukada, S. Kamidono, S. Maeda, Y. Nakamura, Allelotype of renal cell carcinoma. Cancer Res. 51, 820-823 (1991).
40. H. Nagai, T. Kinoshita, H. Suzuki, S. Hatano, T. Murate, H. Saito, Identification and mapping of novel tumor suppressor loci on 6p in diffuse large B-cell non-Hodgkin's lymphoma. Genes Chromosomes Cancer 25, 277-283 (1999).
41. T. Sato, H. Saito, R. Morita, S. Koi, J. H. Lee, Y. Nakamura, Allelotype of human ovarian cancer. Cancer Res. 51, 5118-5122 (1991).
42. B. Vogelstein, E. R. Fearon, S. E. Kern, S. R. Hamilton, A. C. Preisinger, Y. Nakamura, R. White, Allelotype of colorectal carcinomas. Science 244, 207-211 (1989).
43. C. Agostinelli, P. P. Piccaluga, P. Went, M. Rossi, A. Gazzola, S. Righi, T. Sista, C. Campidelli, P. L. Zinzani, B. Falini, S. A. Pileri, Peripheral T cell lymphoma, not otherwise specified: The stuff of genes, dreams and therapies. J. Clin. Pathol. 61, 1160-1167 (2008).
44. 2+-mediated regulation of NDR protein kinase through autophosphorylation and phosphorylation by an upstream kinase. J. Biol. Chem. 278, 6710-6718 (2003).
45. Abbreviations for the amino acids are as follows: D, Asp; E, Glu; H, His; I, Ile; K, Lys; L, Leu; N, Asn; P, Pro; S, Ser; T, Thr; V, Val; and Y, Tyr.
46. A. Bordon, N. Bosco, C. Du Roure, B. Bartholdy, H. Kohler, G. Matthias, A. G. Rolink, P. Matthias, Enforced expression of the transcriptional coactivator OBF1 impairs B cell differentiation at the earliest stage of development. PLoS One 3, e4007 (2008).
47. A. Hergovich, S. J. Bichsel, B. A. Hemmings, Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. Mol. Cell. Biol. 25, 8259-8272 (2005).
48. L. Van Parijs, Y. Refaeli, J. D. Lord, B. H. Nelson, A. K. Abbas, D. Baltimore, Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activationinduced cell death. Immunity 11, 281-288 (1999).
49. M. Senoo, J. P. Manis, F. W. Alt, F. McKeon, p63 and p73 are not required for the development and p53-dependent apoptosis of T cells. Cancer Cell 6, 85-89 (2004).
50. M. van de Wetering, I. Oving, V. Muncan, M. T. Pon Fong, H. Brantjes, D. van Leenen, F. C. Holstege, T. R. Brummelkamp, R. Agami, H. Clevers, Specific inhibition of gene expression using a stably integrated, inducible small-interfering-RNA vector. EMBO Rep. 4, 609-615 (2003).