A defect of the INK4-Cdk4 checkpoint and Myc collaborate in blastoid mantle cell lymphomalike lymphoma formation in mice

American Journal of Pathology

Volumn 180, Issue 4, 2012, Pages 1688-1701

  Vincent Fabert, Christelle ^a   Fiancette, Rémi ^a   Rouaud, Pauline ^a   Baudet, Christel ^b   Truffinet, Véronique ^a   Magnone, Virginie ^c   Guillaudeau, Angélique ^d   Cogné, Michel ^a   Dubus, Pierre ^b   Denizot, Yves ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d DUPUYTREN UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD5 ANTIGEN; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR 2A; IMMUNOGLOBULIN; LEUKOSIALIN; MYC PROTEIN; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CARCINOGENESIS; CELL COUNT; CELL CYCLE CHECKPOINT; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOGLOBULIN PRODUCTION; LYMPHOPOIESIS; MANTLE CELL LYMPHOMA; MITOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC HYPERMUTATION; WESTERN BLOTTING;

ANIMALS; B-LYMPHOCYTES; CELL CYCLE; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENES, MYC; IMMUNOGLOBULINS; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; LYMPHOMA, MANTLE-CELL; LYMPHOPOIESIS; MICE; MICE, TRANSGENIC; NEOPLASM PROTEINS; PROTEIN ISOFORMS; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84859017982     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.01.004     Document Type: Article

References (72)

1. M. Ruas, G. Peters The p16INK4a/CDKN2A tumor suppressor and its relatives Biochim Biophys Acta 1378 1998 F115 F177
2. M. Marzec, M. Kasprzycka, R. Lai, A.B. Gladden, P. Wlodarski, E. Tomczak, P. Nowell, S.E. Deprimo, S. Sadis, S. Eck, S.J. Schuster, J.A. Diehl, M.A. Wasik Mantle cell lymphoma cells express predominantly cyclin D1 isoform and are higly sensitive to selective inhibition of CDK4 kinase activity Blood 108 2006 1744 1750
3. P. Jares, E. Campo Advances in the understanding of mantle cell lymphoma Br J Haematol 142 2008 149 165
4. S.E. Bodrug, B.J. Warner, M.L. Bath, G.J. Lindeman, A.W. Harris, J.M. Adams Cyclin D1 transgene impedes lymphocyte maturation and collaborates in lymphomagenesis with the myc gene EMBO J 13 1994 2124 2130
5. H. Lovec, A. Grzeschiczek, M.B. Kowalski, T. Mry Cyclin D1/bcl-1 cooperates with myc genes in the generation of B-cell lymphoma in transgenic mice EMBO J 13 1994 3487 3495
6. R. Fiancette, R. Amin, V. Truffinet, C. Vincent-Fabert, N. Cogné, M. Cogné, Y. Denizot A myeloma translocation-like model associating CCND1 with the immunoglobulin heavy-chain locus 3′ enhancers does not promote by itself B cell malignancies Leuk Res 34 2010 1043 1051
7. S. Bea, M. Ribas, J.M. Hernandez, F. Bosch, M. Pinyol, L. Hernandez, J.L. Garcia, T. Flores, M. Conzalez, A. Lopez-Guillermo, M.A. Piris, A. Cardesa, E. Montserrat, R. Miro, E. Campo Increased number of chromosomal imbalances and high-level DNA amplifications in mantle cell lymphoma are associated with blastoid variants Blood 93 1999 4365 4374
8. L. Hernandez, S. Hernandez, S. Bea, M. Pinyol, A. Ferrer, F. Bosch, A. Nadal, P.L. Fernandez, A. Palacin, E. Montserrat, E. Campo c-myc mRNA expression and genomic alterations in mantle cell lymphomas and other nodal non-Hodgkin's lymphomas Leukemia 13 1999 2087 2093
9. M. Parrens, M.A. Belaud-Rotureau, O. Fitoussi, N. Carerre, K. Bouabdallah, G. Marit, P. Dubus, A. de Mascarel, J.P. Merlio Blastoid and common variants of mantle cell lymphoma exhibit distinct immunophenotypic and interphase FISH features Histopathology 48 2006 353 362
10. Y. Yatabe, R. Suzuki, K. Tobinai, Y. Matsuno, R. Ichinohasama, M. Okamoto, M. Yamaguchi, J. Tamaru, N. Uike, Y. Hashimoto, Y. Morishima, T. Suchi, M. Seta, S. Nakamura Significance of cyclin D1 overexpression for the diagnosis of mantle cell lymphoma: a clinicopathologic comparison of cyclin D1-positive MCL and cyclin D1-negative MCL-like B-cell lymphoma Blood 95 2000 2253 2261
11. K. Fu, D.D. Weisenburger, T.C. Greiner, S. Dave, G. Wright, A. Rosenwald, M. Chiorazzi, J. Iqbal, S. Gesk, R. Siebert, D. De Jong, E.S. Jaffe, W.H. Wilson, J. Delabie, G. Ott, B.J. Dave, W.G. Sanger, L.M. Smith, L. Rimsza, R.M. Braziel, H.K. Mller-Hermelink, E. Campo, R.D. Gascoyne, L.M. Staudt, W.C. Chan Lymphoma/Leukaemia Molecular Profiling Project: Cyclin D1-negative mantle cell lymphoma: a clinicopathologic study based on gene expression profiling Blood 106 2005 4315 4321
12. I. Salaverria, A. Zettl, S. Bea, V. Moreno, J. Valls, E. Hartmann, G. Ott, G. Wright, A. Lopez-Guillermo, W.C. Chan, D.D. Weisenburger, R.D. Gascoyne, T.M. Grogan, J. Delabie, E.S. Jaffe, E. Montserrat, H.K. Muller-Hermelink, L.M. Staud, A. Rosenwald, E. Campo Specific secondary genetic alterations in mantle cell lymphoma provide prognosis information independent of the gene expression-based proliferation signature J Clin Oncol 5 2007 1216 1222
13. I. Wlodarska, D. Dierickx, V. Vanhentenrijk, K. van Roosbroeck, H. Pospisilova, F. Minnei, G. Verhoef, J. Thomas, P. Vandenberghe, C. De Wolf-Peeters Translocations targeting CCND2 CCND3, and MYCN do occur in t(11;14)-negative mantle cell lymphoma Blood 111 2008 5683 5690
14. M.R. Smith, I. Joshi, F. Jin, T. Al-Saleem Murine model for mantle cell lymphoma Leukemia 20 2006 891 893
15. R.J. Ford, L. Shen, Y.C. Lin-Lee, L.V. Pham, A. Multani, H.J. Zhou, A.T. Tamayo, C. Zhang, L. Hawthorn, J.K. Cowell, J.L. Ambrus Jr Development of a murine model for blastoid variant mantle-cell lymphoma Blood 109 2007 4899 4906
16. T. Wlfel, M. Hauer, J. Schneider, M. Serrano, C. Wlfel, E. Klehmann-Hieb, E. De Plaen, T. Hankeln, K.H. Meyer zum Bschenfelde, D. Beach A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma Science 269 1995 1281 1284
17. R24C mutation facilitates tumorigenesis and escape from cellular senescence Mol Cell Biol 22 2002 644 656
18. R. Sotillo, P. Dubus, J. Martin, E. de la Cueva, S. Ortega, M. Malumbres, M. Barbacid Wide spectrum of tumors in knock-in mice carrying a Cdk4 protein insensitive to INK4 inhibitors EMBO J 23 2001 6637 6647
19. H. Hermeking, C. Rago, M. Schuhmacher, Q. Li, J.F. Barrett, A.J. Obaya, B.C. O'Connell, M.K. Mateyak, W. Tam, F. Kohlhuber, C.V. Dang, J.M. Sedivy, D. Eick, B. Vogelstein, K.W. Kinzler Identification of CDK4 as a target of c-myc Proc Natl Acad Sci U S A 97 2000 2229 2234
20. V. Truffinet, E. Pinaud, N. Cogné, B. Petit, L. Guglielmi, M. Cogné, Y. Denizot The 3′ IgH locus control region is sufficient to deregulate a c-myc transgene and promote mature B cell malignancies with a predominant Burkitt-like phenotype J Immunol 179 2007 6033 6042
21. C. Vincent, V. Truffinet, R. Fiancette, B. Petit, N. Cogné, M. Cogné, Y. Denizot Uncoupling between Ig somatic hypermutation and oncogene mutation in mouse lymphoma Biochim Biophys Acta 1793 2009 418 426
22. C. Vincent-Fabert, R. Fiancette, M. Cogné, E. Pinaud, Y. Denizot The IgH 3′ regulatory region and its implication in lymphomagenesis Eur J Immunol 40 2010 3306 3311
23. S.G. Rane, P. Dubus, R.V. Mettus, E.J. Galbreath, G. Boden, E.P. Reddy, M. Barbacid Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in β-islet cell hyperplasia Nat Genet 22 1999 44 52
24. C. Vincent-Fabert, V. Truffinet, R. Fiancette, N. Cogné, M. Cogné, Y. Denizot Ig synthesis and class switching do not require the presence of the hs4 enhancer in the 3′ IgH regulatory region J Immunol 182 2009 6926 6932
25. K. Le Brigand, P. Barbry MEDIANTE: a web-based microarray data manager Bioinformatics 23 2007 1304 1306
26. K. Le Brigand, R. Russell, C. Moreilhon, J.M. Rouillard, B. Jost, F. Amiot, V. Magnone, C. Bole-Feysot, P. Rostagno, V. Virolle, V. Defamie, P. Dessen, G. Williams, P. Lyons, G. Rios, B. Mari, E. Gulari, P. Kastner, X. Gidrol, T.C. Freeman, P. Barbry An open-access long oligonucleotide microarray resource for analysis of the human and mouse transcriptomes Nucleic Acids Res 34 2006 e87
27. C. Moreilhon, D. Gras, C. Hologne, O. Bajolet, F. Cottrez, V. Magnone, M. Merten, H. Groux, E. Puchelle, P. Barbry Live Staphylococcus aureus and bacterial soluble factors induce different transcriptional responses in human airway cells Physiol Genomics 20 2005 244 255
28. J. Wu, S.H. Wu, A. Bollig, A. Thakur, D.J. Liao Identification of the cyclin D1b mRNA variant in mouse Mol Biol Rep 36 2009 953 957
29. A. Menssen, H. Hermeking Characterization of the c-myc-regulated transcriptome by SAGE: identification and analysis of c-myc target genes Proc Nat Acad Sci U S A 99 2002 6274 6279
30. A.B. Gladden, R. Woolery, M.A. Wasik, J.A. Diehl Expression of constitutively nuclear cyclin D1 in murine lymphocytes induces B-cell lymphoma Oncogene 16 2006 998 1007
31. R. Fiancette, P. Rouaud, C. Vincent-Fabert, B. Laffleur, V. Magnone, M. Cogné, Y. Denizot A p53 defect sensitizes various stages of B cell development to lymphomagenesis in mice carrying an IgH 3′ regulatory region-driven c-myc transgene J Immunol 187 2011 5772 5782
32. R.J. Molot, T.C. Meeker, C.T. Wittwer, S.L. Perkins, G.H. Segal, A.S. Masih, R.C. Braylan, C.R. Kjeldsberg Antigen expression and polymerase chain reaction amplification of mantle cell lymphomas Blood 6 1994 1626 1631
33. J. Garcia-Conde, F. Cabanillas Mantle cell lymphoma: a lymphoproliferative disorder associated with aberrant function of the cell cycle Leukemia 10 1996 s78 s83
34. M.S. Neuberger, C. Rada Somatic hypermutation: activation-induced deaminase for C/G followed by polymerase η for A/T J Exp Med 204 2007 7 10
35. M.J. Rummel, S. de Vos, D. Hoelzer, H.P. Koeffler, W.K. Hofmann Altered apoptotic pathways in mantle cell lymphoma Leuk Lymphoma 45 2004 49 54
36. L. Mllauer, I. Mosberger, A. Chott Fas ligand expression in nodal non-Hodgkin's lymphoma Mod Pathol 11 1998 369 375
37. H. Yamaguchi, H. Hanawa, N. Uchida, M. Inamai, K. Sawaguchi, Y. Mitamura, T. Shimada, K. Dan, K. Inokuchi Multistep pathogenesis of leukaemia via the MLL-AF4 chimeric gene/Flt3 gene tyrosine kinase domain (TDK) mutation-related enhancement of S100A6 expression Exp Hematol 37 2009 701 714
38. J. Starkova, B. Zamostna, E. Mejstrikova, R. Krejci, H.A. Drabkin, J. Trka Hox gene expression in phenotypic and genotypic subgroups and low HOXA gene expression as an adverse prognostic factor in pediatric ALL Pediatr Blood Cancer 55 2010 1072 1082
39. T.C. Islam, A.C. Asplund, J.M. Lindvall, L. Nygren, J. Liden, E. Kimby, B. Christensson, C.I. Smith, B. Sande High level of cannabinoid receptor 1, absence of regulator of G protein signalling 13 and differential expression of cyclin D1 in mantle cell lymphoma Leukemia 17 2003 1880 1890
40. E.G. Rizzatti, R.P. Falcao, R.A. Panepucci, R. Proto-Siqueira, W.T. Anselmo-Lima, O.K. Okamoto, M.A. Zago Gene expression profiling of mantle cell lymphoma cells reveals aberrant expression of genes from the PI3K-AKT. WNT and TGFβ signalling pathways Br J Haematol 130 2005 516 526
41. S. Ek, C.M. Hgerkorp, M. Dictor, M. Ehinger, C.A.K. Borrebaeck Mantle cell lymphoma express a distinct gene signature affecting lymphocyte trafficking and growth regulation as compared with subpopulations of normal human B cells Cancer Res 62 2002 4398 4405
42. M. Schraders, P. Jares, S. Bea, E.F.P.M. Schoenmakers, H.J.M. van Krieken, E. Campo, P.J.T.A. Groenen Integrated genomic and expression profiling in mantle cell lymphoma: identification of gene-dosage regulated candidate genes Br J Haematol 143 2008 210 221
43. J.K. Kim, J.A. Diehl Nuclear cyclin D1: an oncogenic driver in human cancer J Cell Physiol 220 2009 292 296
44. E. Beltran, V. Fresquet, J. Martinez-Useros, J.A. Richter-Larrea, A. Sagardoy, I. Sesma, L.L. Almada, S. Montes-Moreno, R. Siebert, S. Gesk, M.J. Calasanz, R. Malumbres, M. Rieger, F. Prosper, I.S. Lossos, M.A. Piris, M.E. Fernadez-Zapico, J.A. Martinez-Climent A cyclin-D1 interaction with BAX underlies its oncogenic role and potential as a therapeutic target in mantle cell lymphoma Proc Natl Acad Sci U S A 108 2011 12461 12466
45. G. Tchakarska, M. Roussel, X. Troussard, B. Sola Cyclin D1 inhibits mitochondrial activity in B cells Cancer Res 71 2011 1690 1699
46. F. Jardin, J.M. Picquenot, F. Parmentier, P. Ruminy, M. Cornic, D. Penther, P. Bertrand, H. Lanic, O. Cassuto, C. Humbrecht, E. Lemasle, A. Wautier, C. Bastard, H. Tilly Detection of gene copy number aberrations in mantled cell lymphoma by a single quantitative multiplex PCR assay: clinicopathological relevance and prognosis value Br J Haematol 146 2009 607 618
47. C. Lévêque, V. Marsaud, J.M. Renoir, B. Sola Alternative cyclin D1 forms a and b have different biological functions in the cell cycle of B lymphocytes Exp Cell Res 313 2007 2719 2729
48. J. Martin, S.L. Hunt, P. Dubus, R. Sotillo, F. Néhmé- Pélluard, M.A. Magnuson, A.F. Parlow, M. Malumbres, S. Ortega, M. Barbacid Genetic rescue of Cdk4 null mice restores pancreatic beta-cell proliferation but not homeostatic cell number Oncogene 22 2003 5261 5269
49. D. Santamaria, C. Barrire, A. Cerqueira, S. Hunt, C. Tardy, K. Newton, J.F. Caceres, P. Dubus, M. Malumbres, M. Barbacid Cdk1 is sufficient to drive the mammalian cell cycle Nature 448 2007 811 815
50. N. Mori, R. Yang, N. Kawamata, C.W. Miller, H. Mizoguchi, H.P. Koeffler Absence of R24C mutation of the CDK4 gene in leukemias and solid tumors Int J Hematol 77 2003 259 262
51. T. Tsutsui, B. Hesabi, D.S. Moons, P.P. Pandolfi, K.S. Hansel, A. Koff, H. Kiyokawa Targeted disruption of CDK4 delays cell cycle entry with enhanced p27(Kip1) activity Mol Cell Biol 19 1999 7011 7019
52. E.F. Wagner, M. Hleb, N. Hanna, S. Sharma A pivotal role of cyclin D3 and cyclin-dependent kinase inhibitor p27 in the regulation of IL-2-.IL-4-, or IL-10-mediated human B cell proliferation J Immunol 161 1998 1123 1131
53. kip1 cyclin-dependent kinase inhibitors is regulated differently during human B cell differentiation J Immunol 165 2000 4346 4352
54. N. Solvason, W.W. Wu, N. Kabra, W. Wu, E. Lees, M.C. Howard Induction of cell cycle regulatory proteins in anti-immunoglobulin-stimulated mature B lymphoytes J Exp Med 184 1996 407 417
55. D. Tormo, A. Ferrer, E. Gaffal, J. Wenzel, J. Basner-Tschakarjan E Steitz, L.C. Heukamp, I. Gtgemann, R. Buettner, M. Malumbres, M. Barbacid, G. Merlino, T. Tting Rapid growth of invasive metastatic melanoma in carcinogen-treated hepatocyte growth factor/scatter factor-transgenic mice carrying an oncogenic CDK4 mutation Am J Pathol 169 2006 665 672
56. S. Pelengaris, M. Khan, G. Evan c-MYC: more than just a matter of life and death Nat Rev Cancer 2 2002 764 776
57. INK4A uncouples growth from cell cycle progression in leukaemia cells with deregulated cyclin E and c-myc expression Leukemia 19 2005 1051 1057
58. P.L. Miliani de Marval, E. Marcias, R. Rounbehler, P. Sicinski, H. Kiyokawa, D.G. Johnson, C.J. Conti, M.L. Rodriguez-Puebla Lack of cyclin-dependent kinase 4 inhibits c-myc tumorigenic activities in epithelial tissues Mol Cell Biol 24 2004 7538 7547
59. kip1 protein by cyclin D1 in typical and blastic variants of mantle cell lymphoma (MCL): implication for pathogenesis Blood 101 2003 3181 3187
60. Warf1 genes are associated with aggressive variants of mantle cell lymphomas Blood 89 1997 272 280
61. L. Quintanilla-Martinez, J. Slotta-Huspenina, I. Koch, M. Klier, E.D. Hsi, L. de Leval, W. Klapper, S. Gesk, R. Siebert, F. Fend Differential diagnosis of cyclin D2+ mantle cell lymphoma based on fluorescence in situ hybridization and quantitative real-time-PCR Haematologica 94 2009 1595 1598
62. A. Matolcsy, A. Chadburn, D.M. Knowles De novo CD5-positive and Richter's syndrome-associated diffuse large B cell lymphomas are genotypically distinct Am J Pathol 147 1995 207 216
63. + diffuse large B-cell lymphomas express VH genes with somatic mutation Blood 91 1998 1145 1151
64. INK4A as upstream regulators of Myc Oncogene 15 1997 179 192
65. J. Wang, L.M. Boxer Regulatory elements in the immunoglobulin heavy chain gene 3′-enhancers induce c-myc deregulation and lymphomagenesis in murine B cells J Biol Chem 280 2005 12766 12773
66. Y. Refaeli, R.M. Young, B.C. Turner, J. Duda, K.A. Field, J.M. Bishop The B cell antigen receptor and overexpression of MYC can cooperate in the genesis of B cell lymphomas PLOS Biol 6 2008 e152
67. A. Gladkikh, D. Potashnikova, E. Korneva, O. Khudoleeva, I. Vorobjev Cyclin D1 expression in B-cell lymphomas Exp Hematol 38 2010 1047 1057
68. V. Bryja, J. Pachernik, J. Vondracek, K. Soucek, L. Cajanek, V. Horvath, Z. Holubcova, P. Dvorak, A. Hampl Lineage specific composition of D-CDK4/CDK6-p27 complexes reveals distinct functions of CDK4. CDK6 and individual D-type cyclins in differentiating cells of embryonic origin Cell Prolif 41 2008 875 893
69. S. Paternot, J.E. Dumont, P.P. Roger Differential utilization of cyclin D1 and cyclin D3 in the distinct mitogenic stimulations by growth factors and TSH of human thymocytes in primary culture Mol Endocrinol 20 2006 3279 3292
70. J. Bartkova, J. Lukas, M. Strauss, J. Bartek Cyclin D3: requirement for G1/S transition and high abundance in quiescent tissues suggest a dual role in proliferation and differentiation Oncogene 17 1998 1027 1037
71. L. Guglielmi, M. Le Bert, V. Truffinet, M. Cogné, Y. Denizot Insulators to improve expression of a 3′IgH LCR-driven reporter gene in transgenic mouse models Biochem Biophys Res Commun 307 2003 466 471
72. E. Pinaud, M. Marquet, R. Fiancette, S. Péron, C. Vincent-Fabert, Y. Denizot, M. Cogné The IgH locus 3′ regulatory region: pulling the strings from behind Adv Immunol 110 2011 27 70