Glycogen synthase kinase-3β and p38 phosphorylate cyclin D2 on Thr280 to trigger its ubiquitin/proteasome-dependent degradation in hematopoietic cells

Oncogene

Volumn 26, Issue 46, 2007, Pages 6630-6640

  Kida, A ^a   Kakihana, K ^a   Kotani, S ^a   Kurosu, T ^a   Miura, O ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Cyclin D2; GSK3 ; p38; PI3K; Proteasomal degradation

Indexed keywords

ALANINE; CYCLIN D2; GLYCOGEN SYNTHASE KINASE 3BETA; INTERLEUKIN 3; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASOME; PROTEIN KINASE B; THREONINE; UBIQUITIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEMATOPOIETIC CELL; HEMATOPOIETIC SYSTEM TUMOR; LEUKEMIA CELL; MOUSE; MYELOMA CELL; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; CYCLINS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LEUKEMIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; THREONINE; UBIQUITIN;

EID: 35348826054     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1210490     Document Type: Article

References (42)

1. Agami R, Bernards R. (2000). Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage. Cell 102: 55-66.
2. Ando K, Ajchenbaum-Cymbalista F, Griffin JD. (1993). Regulation of G1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc Natl Acad Sci USA 90: 9571-9575.
3. Benzeno S, Lu F, Guo M, Barbash O, Zhang F, Herman JG et al. (2006). Identification of mutations that disrupt phosphorylation-dependent nuclear export of cyclin D1. Oncogene 25: 6291-6303.
4. Bergsagel PL, Kuehl WM, Zhan F, Sawyer J, Barlogie B, Shaughnessy Jr J. (2005). Cyclin D dysregulation: an early and unifying pathogenic event in multiple myeloma. Blood 106: 296-303.
5. Brazil DP, Yang ZZ, Hemmings BA. (2004). Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 29: 233-242.
6. Carthon BC, Neumann CA, Das M, Pawlyk B, Li T, Geng Y et al. (2005). Genetic replacement of cyclin D1 function in mouse development by cyclin D2. Mol Cell Biol 25: 1081-1088.
7. Casanovas O, Jaumot M, Paules AB, Agell N, Bachs O. (2004). P38SAPK2 phosphorylates cyclin D3 at Thr-283 and targets it for proteasomal degradation. Oncogene 23: 7537-7544.
8. Casanovas O, Miro F, Estanyol JM, Itarte E, Agell N, Bachs O. (2000). Osmotic stress regulates the stability of cyclin D1 in a p38SAPK2-dependent manner. J Biol Chem 275: 35091-35097.
9. Chiles TC. (2004). Regulation and function of cyclin D2 in B lymphocyte subsets. J Immunol 173: 2901-2907.
10. Chin H, Arai A, Wakao H, Kamiyama R, Miyasaka N, Miura O. (1998). Lyn physically associates with the erythropoietin receptor and may play a role in activation of the Stat5 pathway. Blood 91: 3734-3745.
11. Clappier E, CuccuiniW, Cayuela JM, Vecchione D, Baruchel A, Dombret H et al. (2006). Cyclin D2 dysregulation by chromosomal translocations to TCR loci in T-cell acute lymphoblastic leukemias. Leukemia 20: 82-86.
12. Deininger MW, Vieira SA, Parada Y, Banerji L, Lam EW, Peters G et al. (2001). Direct relation between BCR-ABL tyrosine kinase activity and cyclin D2 expression in lymphoblasts. Cancer Res 61: 8005-8013.
13. Delmer A, Ajchenbaum-Cymbalista F, Tang R, Ramond S, Faussat AM, Marie JP et al. (1995). Overexpression of cyclin D2 in chronic B-cell malignancies. Blood 85: 2870-2876.
14. Deshpande A, Sicinski P, Hinds PW. (2005). Cyclins and cdks in development and cancer: a perspective. Oncogene 24: 2909-2915.
15. Diehl JA, Cheng M, Roussel MF, Sherr CJ. (1998). Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12: 3499-3511.
16. Diehl JA, Zindy F, Sherr CJ. (1997). Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 11: 957-972.
17. Ely S, Di Liberto M, Niesvizky R, Baughn LB, Cho HJ, Hatada EN et al. (2005). Mutually exclusive cyclin-dependent kinase 4/cyclin D1 and cyclin-dependent kinase 6/cyclin D2 pairing inactivates retinoblastoma protein and promotes cell cycle dysregulation in multiple myeloma. Cancer Res 65: 11345-11353.
18. Fox BC, Crew TE, Welham MJ. (2005). Phosphoinositide 3-kinases can act independently of p27Kip1 to regulate optimal IL-3-dependent cell cycle progression and proliferation. Cell Signal 17: 473-487.
19. Hu X, Bryington M, Fisher AB, Liang X, Zhang X, Cui D et al. (2002). Ubiquitin/proteasome-dependent degradation of D-type cyclins is linked to tumor necrosis factor-induced cell cycle arrest. J Biol Chem 277: 16528-16537.
20. Huang W, Chang HY, Fei T, Wu H, Chen YG. (2007). GSK3beta mediates suppression of cyclin D2 expression by tumor suppressor PTEN. Oncogene 26: 2471-2482.
21. Ihle JN. (1995). Cytokine receptor signalling. Nature 377: 591-594.
22. Jena N, Deng M, Sicinska E, Sicinski P, Daley GQ. (2002). Critical role for cyclin D2 in BCR/ABL-induced proliferation of hematopoietic cells. Cancer Res 62: 535-541.
23. Jope RS, Johnson GV. (2004). The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29: 95-102.
24. Karrman K, Andersson A, Bjorgvinsdottir H, Strombeck B, Lassen C, Olofsson T et al. (2006). Deregulation of cyclin D2 by juxtaposition with T-cell receptor alpha/delta locus in t(12;14)(p13;q11)-positive childhood T-cell acute lymphoblastic leukemia. Eur J Haematol 77: 27-34.
25. Kato JY, Sherr CJ. (1993). Inhibition of granulocyte differentiation by G1 cyclins D2 and D3 but not D1. Proc Natl Acad Sci USA 90: 11513-11517.
26. Kozar K, Sicinski P. (2005). Cell cycle progression without cyclin D-CDK4 and cyclin D-CDK6 complexes. Cell Cycle 4: 388-391.
27. Kurosu T, Takahashi Y, Fukuda T, Koyama T, Miki T, Miura O. (2005). p38MAP kinase plays a role in G2 checkpoint activation and inhibits apoptosis of human B cell lymphoma cells treated with etoposide. Apoptosis 10: 1111-1120.
28. Kwak YT, Li R, Becerra CR, Tripathy D, Frenkel EP, Verma UN. (2005). IkappaB kinase alpha regulates subcellular distribution and turnover of cyclin D1 by phosphorylation. J Biol Chem 280: 33945-33952.
29. Kyriakis JM, Avruch J. (2001). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81: 807-869.
30. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ et al. (2006). Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell 24: 355-366.
31. Lucet IS, Fantino E, Styles M, Bamert R, Patel O, Broughton SE et al. (2006). The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor. Blood 107: 176-183.
32. Ma Y, Feng Q, Sekula D, Diehl JA, Freemantle SJ, Dmitrovsky E. (2005). Retinoid targeting of different D-type cyclins through distinct chemopreventive mechanisms. Cancer Res 65: 6476-6483.
33. Malumbres M, Barbacid M. (2001). To cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer 1: 222-231.
34. Miura O, Cleveland JL, Ihle JN. (1993). Inactivation of erythropoietin receptor function by point mutations in a region having homology with other cytokine receptors. Mol Cell Biol 13: 1788-1795.
35. Murray AW. (2004). Recycling the cell cycle: cyclins revisited. Cell 116: 221-234.
36. Naderi S, Gutzkow KB, Lahne HU, Lefdal S, Ryves WJ, Harwood AJ et al. (2004). cAMP-induced degradation of cyclin D3 through association with GSK-3beta. J Cell Sci 117: 3769-3783.
37. Okabe H, Lee SH, Phuchareon J, Albertson DG, McCormick F, Tetsu O. (2006). A critical role for FBXW8 and MAPK in cyclin D1 degradation and cancer cell proliferation. PLoS ONE 1: e128.
38. Parada Y, Banerji L, Glassford J, Lea NC, Collado M, Rivas C et al. (2001). BCR-ABL and interleukin 3 promote haematopoietic cell proliferation and survival through modulation of cyclin D2 and p27Kip1 expression. J Biol Chem 276: 23572-23580.
39. Radosevic N, Delmer A, Tang R, Marie JP, Ajchenbaum-Cymbalista F. (2001). Cell cycle regulatory protein expression in fresh acute myeloid leukemia cells and after drug exposure. Leukemia 15: 559-566.
40. Shao J, Sheng H, DuBois RN, Beauchamp RD. (2000). Oncogenic Ras-mediated cell growth arrest and apoptosis are associated with increased ubiquitin-dependent cyclin D1 degradation. J Biol Chem 275: 22916-22924.
41. Sherr CJ, Roberts JM. (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512.
42. Yang K, Guo Y, Stacey WC, Harwalkar J, Fretthold J, Hitomi M et al. (2006). Glycogen synthase kinase 3 has a limited role in cell cycle regulation of cyclin D1 levels. BMC Cell Biol 7: 33.