Lineage-specific function of Engrailed-2 in the progression of chronic myelogenous leukemia to T cell blast crisis

Cell Cycle

Volumn 13, Issue 11, 2014, Pages 1717-1726

  Abollo Jimeńez, Fernando ^a   Campos Sańchez, Elena ^b   Toboso Navasa, Amparo ^b,f   Vicente Duenãs, Carolina ^a   González Herrero, Inés ^a   Alonso Escudero, Esther ^a   Gonzaĺez, Marcos ^c   Segura, Víctor ^d   Blanco, Óscar ^e   Mart́inez Climent, José Ángel ^d   Sańchez García, Isidro ^a   Cobaleda, Ceśar ^b  

^a INSTITUTO DE INVESTIGACIÓN BIOMÉDICA DE SALAMANCA IBSAL   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^d UNIVERSITY OF NAVARRA   (Spain)

^e UNIVERSITY OF SALAMANCA   (Spain)

^f IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Blast crisis; Chronic myelogenous leukemia; DNA methylation; Engrailed 2; T cell development

Indexed keywords

DNA; ENGRAILED 2 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; NERVE PROTEIN; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLAST CELL CRISIS; BONE MARROW TRANSPLANTATION; CELL FATE; CELL LINEAGE; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; HEMATOPOIESIS; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; T LYMPHOCYTE; TRANSGENIC MOUSE; ANIMAL; CELL DIFFERENTIATION; DISEASE COURSE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROARRAY ANALYSIS; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BLAST CRISIS; CELL DIFFERENTIATION; CPG ISLANDS; DISEASE PROGRESSION; DNA METHYLATION; DNA PRIMERS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; NERVE TISSUE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 84901759493     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.28629     Document Type: Article

References (34)

1. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008; 132:631-44; PMID:18295580; http://dx.doi.org/10.1016/j.cell. 2008.01.025
2. Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer 2007; 7:441-53; PMID:17522713; http://dx.doi.org/10.1038/nrc2147
3. Perrotti D, Cesi V, Trotta R, Guerzoni C, Santilli G, Campbell K, Iervolino A, Condorelli F, Gambacorti-Passerini C, Caligiuri MA, et al. BCR-ABL suppresses C/EBPalpha expression through inhibitory action of hnRNP E2. Nat Genet 2002; 30:48-58; PMID:11753385; http://dx.doi.org/10.1038/ng791
4. Mullighan CG, Miller CB, Radtke I, Phillips LA, Dalton J, Ma J, White D, Hughes TP, Le Beau MM, Pui CH, et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 2008; 453:110-4; PMID:18408710; http://dx.doi.org/10.1038/nature06866
5. Allouche M, Bourinbaiar A, Georgoulias V, Consolini R, Salvatore A, Auclair H, Jasmin C. T cell lineage involvement in lymphoid blast crisis of chronic myeloid leukemia. Blood 1985; 66:1155-61; PMID:3876856
6. Dorfman DM, Longtine JA, Fox EA, Weinberg DS, Pinkus GS. T-cell blast crisis in chronic myelogenous leukemia. Immunophenotypic and molecular biologic findings. Am J Clin Pathol 1997; 107:168-76; PMID:9024065
7. Jelinek J, Gharibyan V, Estecio MR, Kondo K, He R, Chung W, Lu Y, Zhang N, Liang S, Kantarjian HM, et al. Aberrant DNA methylation is associated with disease progression, resistance to imatinib and shortened survival in chronic myelogenous leukemia. PLoS One 2011; 6:e22110; PMID:21760961; http://dx.doi.org/10.1371/journal.pone.0022110
8. Cross SH, Charlton JA, Nan X, Bird AP. Purification of CpG islands using a methylated DNA binding column. Nat Genet 1994; 6:236-44; PMID:8012384; http://dx.doi.org/10.1038/ng0394-236
9. Shiraishi M, Chuu YH, Sekiya T. Isolation of DNA fragments associated with methylated CpG islands in human adenocarcinomas of the lung using a methylated DNA binding column and denaturing gradient gel electrophoresis. Proc Natl Acad Sci U S A 1999; 96:2913-8; PMID:10077611; http://dx.doi.org/10.1073/ pnas.96.6.2913
10. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, Wen B, Wu H, Liu Y, Diep D, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet 2011; 43:768-75; PMID:21706001; http://dx.doi.org/10.1038/ng.865
11. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009; 41:178-86; PMID:19151715; http://dx.doi.org/10.1038/ng. 298
12. Condron BG, Patel NH, Zinn K. Engrailed controls glial/neuronal cell fate decisions at the midline of the central nervous system. Neuron 1994; 13:541-54; PMID:7917290; http://dx.doi.org/10.1016/0896-6273(94)90024-8
13. Davis CA, Joyner AL. Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev 1988; 2(12B):1736-44; PMID:2907320; http://dx.doi.org/10. 1101/gad.2.12b.1736
14. Davis CA, Noble-Topham SE, Rossant J, Joyner AL. Expression of the homeo box-containing gene En-2 delineates a specific region of the developing mouse brain. Genes Dev 1988; 2:361-71; PMID:2454212; http://dx.doi.org/10.1101/gad.2. 3.361
15. Marie B, Bacon JP, Blagburn JM. Double-stranded RNA interference shows that Engrailed controls the synaptic specificity of identified sensory neurons. Curr Biol 2000; 10:289-92; PMID:10712910; http://dx.doi.org/10.1016/S0960- 9822(00)00361-4
16. Terskikh AV, Easterday MC, Li L, Hood L, Kornblum HI, Geschwind DH, Weissman IL. From hematopoiesis to neuropoiesis: evidence of overlapping genetic programs. Proc Natl Acad Sci U S A 2001; 98:7934-9; PMID:11438738; http://dx.doi.org/10.1073/pnas.131200898
17. Antequera F, Boyes J, Bird A. High levels of de novo methylation and altered chromatin structure at CpG islands in cell lines. Cell 1990; 62:503-14; PMID:1974172; http://dx.doi.org/10.1016/0092-8674(90)90015-7
18. Condamine T, Le Luduec JB, Chiffoleau E, Bériou G, Louvet C, Heslan M, Tilly G, Cuturi MC. Characterization of Schlafen-3 expression in effector and regulatory T cells. J Leukoc Biol 2010; 87:451-6; PMID:19996332; http://dx.doi.org/10.1189/jlb.0609410
19. Geserick P, Kaiser F, Klemm U, Kaufmann SH, Zerrahn J. Modulation of T cell development and activation by novel members of the Schlafen (slfn) gene family harbouring an RNA helicase-like motif. Int Immunol 2004; 16:1535-48; PMID:15351786; http://dx.doi.org/10.1093/intimm/dxh155
20. Schwarz DA, Katayama CD, Hedrick SM. Schlafen, a new family of growth regulatory genes that affect thymocyte development. Immunity 1998; 9:657-68; PMID:9846487; http://dx.doi.org/10.1016/S1074-7613(00)80663-9
21. Dai Y, Wong B, Yen YM, Oettinger MA, Kwon J, Johnson RC. Determinants of HMGB proteins required to promote RAG1/2-recombination signal sequence complex assembly and catalysis during V(D)J recombination. Mol Cell Biol 2005; 25:4413-25; PMID:15899848; http://dx.doi.org/10.1128/MCB.25.11.4413-4425.2005
22. Pérez-Caro M, Cobaleda C, González-Herrero I, Vicente-Dueñas C, Bermejo-Rodríguez C, Sánchez-Beato M, Orfao A, Pintado B, Flores T, Sánchez-Martín M, et al. Cancer induction by restriction of oncogene expression to the stem cell compartment. EMBO J 2009; 28:8-20; PMID:19037256; http://dx.doi.org/10.1038/emboj.2008.253
23. Joyner AL, Herrup K, Auerbach BA, Davis CA, Rossant J. Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Science 1991; 251:1239-43; PMID:1672471; http://dx.doi.org/10.1126/science. 1672471
24. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW. World Health Organization classification of tumours. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. Lyon, France: International Agency for Research on Cancer, 2008.
25. Sawada Y, Hino R, Hama K, Ohmori S, Fueki H, Yamada S, Fukamachi S, Tajiri M, Kubo R, Yoshioka M, et al. Type of skin eruption is an independent prognostic indicator for adult T-cell leukemia/lymphoma. Blood 2011; 117:3961-7; PMID:21325600; http://dx.doi.org/10.1182/blood-2010-11-316794
26. Costello JF, Frühwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, Wright FA, Feramisco JD, Peltomäki P, Lang JC, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000; 24:132-8; PMID:10655057; http://dx.doi.org/10.1038/72785
27. García-Ramírez I, Ruiz-Roca L, Martín-Lorenzo A, Blanco O, García-Cenador MB, García-Criado FJ, Vicente-Dueñas C, Sánchez-García I. Genetic background affects susceptibility to tumoral stem cell reprogramming. Cell Cycle 2013; 12:2505-9; PMID:23839033; http://dx.doi.org/10.4161/cc.25544
28. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992; 68:869-77; PMID:1547488; http://dx.doi.org/10.1016/0092-8674(92)90030-G
29. Clark SJ, Harrison J, Paul CL, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res 1994; 22:2990-7; PMID:8065911; http://dx.doi.org/10.1093/nar/22.15.2990
30. Romero-Camarero I, Jiang X, Natkunam Y, Lu X, Vicente-Dueñas C, Gonzalez-Herrero I, Flores T, Garcia JL, McNamara G, Kunder C, et al. Germinal centre protein HGAL promotes lymphoid hyperplasia and amyloidosis via BCR-mediated Syk activation. Nat Commun 2013; 4:1338; PMID:23299888; http://dx.doi.org/10.1038/ncomms2334
31. Vicente-Dueñas C, Fontán L, Gonzalez-Herrero I, Romero-Camarero I, Segura V, Aznar MA, Alonso-Escudero E, Campos-Sanchez E, Ruiz-Roca L, Barajas-Diego M, et al. Expression of MALT1 oncogene in hematopoietic stem/progenitor cells recapitulates the pathogenesis of human lymphoma in mice. Proc Natl Acad Sci U S A 2012; 109:10534-9; PMID:22689981; http://dx.doi.org/10.1073/pnas.1204127109
32. Vicente-Dueñas C, Romero-Camarero I, González-Herrero I, Alonso-Escudero E, Abollo-Jiménez F, Jiang X, Gutierrez NC, Orfao A, Marín N, Villar LM, et al. A novel molecular mechanism involved in multiple myeloma development revealed by targeting MafB to haematopoietic progenitors. EMBO J 2012; 31:3704-17; PMID:22903061; http://dx.doi.org/10.1038/ emboj.2012.227
33. Beltran E, Fresquet V, Martinez-Useros J, Richter-Larrea JA, Sagardoy A, Sesma I, Almada LL, Montes-Moreno S, Siebert R, Gesk S, et al. 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 2011; 108:12461-6; PMID:21746927; http://dx.doi.org/10.1073/pnas.1018941108
34. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31:e15; PMID:12582260; http://dx.doi.org/10.1093/nar/gng015