Leukemia Research
Volume 34, Issue 4 , Pages 430-437 , April 2010

CD9 expression can be used to predict childhood TEL/AML1-positive acute lymphoblastic leukemia: Proposal for an accelerated diagnostic flowchart

  • Virginie Gandemer

      Affiliations

    • Centre National de Recherche Scientifique, Unité Mixte de Recherche 6061 Laboratoire de Génétique et Développement, Equipe Régulation Transcriptionnelle et Oncogenèse, Université de Rennes-1, Rennes Cedex, France
    • OncoPediatric Unit, Centre Hospitalier Universitaire, Rennes, France
  • ,
  • Marc Aubry

      Affiliations

    • Biogenouest®, Transcriptomic Platform, Rennes, France
  • ,
  • Mikael Roussel

      Affiliations

    • Laboratory of Hematology, Centre Hospitalier Universitaire, Rennes, France
  • ,
  • Anne-Gaelle Rio

      Affiliations

    • Centre National de Recherche Scientifique, Unité Mixte de Recherche 6061 Laboratoire de Génétique et Développement, Equipe Régulation Transcriptionnelle et Oncogenèse, Université de Rennes-1, Rennes Cedex, France
  • ,
  • Marie de Tayrac

      Affiliations

    • Centre National de Recherche Scientifique, Unité Mixte de Recherche 6061 Laboratoire de Génétique et Développement, Equipe Régulation Transcriptionnelle et Oncogenèse, Université de Rennes-1, Rennes Cedex, France
    • Medical Genomic Unit, Centre Hospitalier Universitaire, Rennes, France
  • ,
  • Audrey Vallee

      Affiliations

    • Centre National de Recherche Scientifique, Unité Mixte de Recherche 6061 Laboratoire de Génétique et Développement, Equipe Régulation Transcriptionnelle et Oncogenèse, Université de Rennes-1, Rennes Cedex, France
  • ,
  • Jean Mosser

      Affiliations

    • Centre National de Recherche Scientifique, Unité Mixte de Recherche 6061 Laboratoire de Génétique et Développement, Equipe Régulation Transcriptionnelle et Oncogenèse, Université de Rennes-1, Rennes Cedex, France
    • Biogenouest®, Transcriptomic Platform, Rennes, France
    • Medical Genomic Unit, Centre Hospitalier Universitaire, Rennes, France
  • ,
  • Béatrice Ly-Sunnaram

      Affiliations

    • Laboratory of Hematology, Centre Hospitalier Universitaire, Rennes, France
  • ,
  • Marie-Dominique Galibert

      Affiliations

    • Centre National de Recherche Scientifique, Unité Mixte de Recherche 6061 Laboratoire de Génétique et Développement, Equipe Régulation Transcriptionnelle et Oncogenèse, Université de Rennes-1, Rennes Cedex, France
    • Medical Genomic Unit, Centre Hospitalier Universitaire, Rennes, France
    • Corresponding Author InformationCorresponding author at: CNRS UMR 6061 Institut de Génétique et Développement de Rennes, Université de Rennes-1, IFR140 GFAS 2 av du Pr Léon Bernard, CS 34317, 35043 Rennes Cedex, France. Tel.: +33 223 234 705; fax: +33 223 234 607.

Received 17 June 2009 ,Revised 23 September 2009 ,Accepted 25 September 2009.

References 

  1. Goubin A, Auclerc Mf, Auvrignon A, Patte C, Bergeron C, Hemon D, et al. Survival in France after childhood acute leukaemia and non-Hodgkin's lymphoma (1990-2000). Eur J Cancer. 2006;42:534–541
  2. Arico M, Valsecchi Mg, Rizzari C, Barisone E, Biondi A, Casale F, et al. Long-term results of the AIEOP-ALL-95 Trial for Childhood Acute Lymphoblastic Leukemia: insight on the prognostic value of DNA index in the framework of Berlin-Frankfurt-Muenster based chemotherapy. J Clin Oncol. 2008;26:283–289
  3. Gustafsson G, Schmiegelow K, Forestier E, Clausen N, Glomstein A, Jonmundsson G, et al. Improving outcome through two decades in childhood ALL in the Nordic countries: the impact of high-dose methotrexate in the reduction of CNS irradiation. Nordic Society of Pediatric Haematology and Oncology (NOPHO). Leukemia. 2000;14:2267–2275
  4. Pui Ch, Robison Ll, Look At. Acute lymphoblastic leukaemia. Lancet. 2008;371:1030–1043
  5. Schultz Kr, Pullen Dj, Sather Hn, Shuster Jj, Devidas M, Borowitz Mj, et al. Risk- and response-based classification of childhood B-precursor acute lymphoblastic leukemia: a combined analysis of prognostic markers from the Pediatric Oncology Group (POG) and Children's Cancer Group (CCG). Blood. 2007;109:926–935
  6. Vilmer E, Suciu S, Ferster A, Bertrand Y, Cave H, Thyss A, et al. Long-term results of three randomized trials (58831, 58832, 58881) in childhood acute lymphoblastic leukemia: a CLCG-EORTC report. Children Leukemia Cooperative Group. Leukemia. 2000;14:2257–2266
  7. Borkhardt A, Cazzaniga G, Viehmann S, Valsecchi Mg, Ludwig Wd, Burci L, et al. Incidence and clinical relevance of TEL/AML1 fusion genes in children with acute lymphoblastic leukemia enrolled in the German and Italian multicenter therapy trials. Associazione Italiana Ematologia Oncologia Pediatrica and the Berlin-Frankfurt-Munster Study Group. Blood. 1997;90:571–577
  8. Borowitz Mj, Devidas M, Hunger Sp, Bowman Wp, Carroll Aj, Carroll Wl, et al. Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia and its relationship to other prognostic factors: a children's oncology group study. Blood. 2008;111:5477–5485
  9. Loh Ml, Goldwasser Ma, Silverman Lb, Poon Wm, Vattikuti S, Cardoso A, et al. Prospective analysis of TEL/AML1-positive patients treated on Dana-Farber Cancer Institute Consortium Protocol 95-01. Blood. 2006;107:4508–4513
  10. Uckun Fm, Pallisgaard N, Hokland P, Navara C, Narla R, Gaynon Ps , et al. Expression of TEL-AML1 fusion transcripts and response to induction therapy in standard risk acute lymphoblastic leukemia. Leuk Lymphoma. 2001;42:41–56
  11. Pine Sr, Wiemels Jl, Jayabose S, Sandoval C. TEL-AML1 fusion precedes differentiation to pre-B cells in childhood acute lymphoblastic leukemia. Leuk Res. 2003;27:155–164
  12. Sawinska M, Ladon D. Mechanism, detection and clinical significance of the reciprocal translocation t(12;21)(p12;q22) in the children suffering from acute lymphoblastic leukaemia. Leuk Res. 2004;28:35–42
  13. Stams Wa, Beverloo Hb, Den Boer Ml, De Menezes Rx, Stigter Rl, Van Drunen E, et al. Incidence of additional genetic changes in the TEL and AML1 genes in DCOG and COALL-treated t(12;21)-positive pediatric ALL, and their relation with drug sensitivity and clinical outcome. Leukemia. 2006;20:410–416
  14. Zelent A, Greaves M, Enver T. Role of the TEL-AML1 fusion gene in the molecular pathogenesis of childhood acute lymphoblastic leukaemia. Oncogene. 2004;23:4275–4283
  15. Gandemer V, Rio Ag, De Tayrac M, Sibut V, Mottier S, Ly Sunnaram B, et al. Five distinct biological processes and 14 differentially expressed genes characterize TEL/AML1-positive leukemia. BMC Genomics. 2007;8:385
  16. Cook Ga, Wilkinson Da, Crossno Jt, Raghow R, Jennings Lk. The tetraspanin CD9 influences the adhesion, spreading, and pericellular fibronectin matrix assembly of Chinese hamster ovary cells on human plasma fibronectin. Exp Cell Res. 1999;251:356–371
  17. Lagaudriere-Gesbert C, Le Naour F, Lebel-Binay S, Billard M, Lemichez E, Boquet P, et al. Functional analysis of four tetraspans, CD9, CD53, CD81, and CD82, suggests a common role in costimulation, cell adhesion, and migration: only CD9 upregulates HB-EGF activity. Cell Immunol. 1997;182:105–112
  18. Saito Y, Tachibana I, Takeda Y, Yamane H, He P, Suzuki M, et al. Absence of CD9 enhances adhesion-dependent morphologic differentiation, survival, and matrix metalloproteinase-2 production in small cell lung cancer cells. Cancer Res. 2006;66:9557–9565
  19. Wang Jc, Begin Lr, Berube Ng, Chevalier S, Aprikian Ag , Gourdeau H, et al. Down-regulation of CD9 expression during prostate carcinoma progression is associated with CD9 mRNA modifications. Clin Cancer Res. 2007;13:2354–2361
  20. Zvereff V, Wang Jc, Shun K, Lacoste J, Chevrette M. Colocalisation of CD9 and mortalin in CD9-induced mitotic catastrophe in human prostate cancer cells. Br J Cancer. 2007;97:941–948
  21. Canel M, Secades P, Garzon-Arango M, Allonca E, Suarez C, Serrels A, et al. Involvement of focal adhesion kinase in cellular invasion of head and neck squamous cell carcinomas via regulation of MMP-2 expression. Br J Cancer. 2008;98:1274–1284
  22. Crazzolara R, Kreczy A, Mann G, Heitger A, Eibl G, Fink Fm, et al. High expression of the chemokine receptor CXCR4 predicts extramedullary organ infiltration in childhood acute lymphoblastic leukaemia. Br J Haematol. 2001;115:545–553
  23. Furuya M, Kato H, Nishimura N, Ishiwata I, Ikeda H, Ito R, et al. Down-regulation of CD9 in human ovarian carcinoma cell might contribute to peritoneal dissemination: morphologic alteration and reduced expression of beta1 integrin subsets. Cancer Res. 2005;65:2617–2625
  24. Vecchi M, Confalonieri S, Nuciforo P, Vigano Ma, Capra M, Bianchi M, et al. Breast cancer metastases are molecularly distinct from their primary tumors. Oncogene. 2008;27:2148–2158
  25. Wu S, Gessner R, Taube T, Korte A, Von Stackelberg A, Kirchner R, et al. Chemokine IL-8 and chemokine receptor CXCR3 and CXCR4 gene expression in childhood acute lymphoblastic leukemia at first relapse. J Pediatr Hematol Oncol. 2006;28:216–220
  26. Zvieriev V, Wang Jc, Chevrette M. Over-expression of CD9 does not affect in vivo tumorigenic or metastatic properties of human prostate cancer cells. Biochem Biophys Res Commun. 2005;337:498–504
  27. Borowitz Mj , Rubnitz J, Nash M, Pullen Dj, Camitta B. Surface antigen phenotype can predict TEL-AML1 rearrangement in childhood B-precursor ALL: a Pediatric Oncology Group study. Leukemia. 1998;12:1764–1770
  28. Weir Eg, Cowan K, Lebeau P, Borowitz M. A limited antibody panel can distinguish B-precursor acute lymphoblastic leukemia from normal B precursors with four color flow cytometry: implications for residual disease detection. Leukemia. 1999;13:558–567
  29. Barrena S, Almeida J, Yunta M, Lopez A, Fernandez-Mosteirin N, Giralt M, et al. Aberrant expression of tetraspanin molecules in B-cell chronic lymphoproliferative disorders and its correlation with normal B-cell maturation. Leukemia. 2005;19:1376–1383
  30. Yeoh Ej, Ross Me, Shurtleff Sa, Williams Wk, Patel D, Mahfouz R, et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell. 2002;1:133–143
  31. Ross Me, Zhou X, Song G, Shurtleff Sa, Girtman K, Williams Wk, et al. Classification of pediatric acute lymphoblastic leukemia by gene expression profiling. Blood. 2003;102:2951–2959
  32. Lee St, Kim Hj, Kim Sh. Defining an Optimal Number of Immunophenotypic Markers for Lineage Assignment of Acute Leukemias Based on the EGIL Scoring System. Korean J Lab Med. 2006;26:393–399
  33. Bene Mc, Castoldi G, Knapp W, Ludwig Wd, Matutes E, Orfao A, et al. Proposals for the immunological classification of acute leukemias. European Group for the Immunological Characterization of Leukemias (EGIL). Leukemia. 1995;9:1783–1786
  34. Attarbaschi A, Mann G, Konig M, Steiner M, Strehl S, Schreiberhuber A, et al. Mixed lineage leukemia-rearranged childhood pro-B and CD10-negative pre-B acute lymphoblastic leukemia constitute a distinct clinical entity. Clin Cancer Res. 2006;12:2988–2994
  35. Behm Fg, Raimondi Sc, Frestedt Jl, Liu Q, Crist Wm, Downing Jr, et al. Rearrangement of the MLL gene confers a poor prognosis in childhood acute lymphoblastic leukemia, regardless of presenting age. Blood. 1996;87:2870–2877
  36. Von Dongen J, Lhermitte L, Böttcher S, Almeida J, Van Der Velden Vh, Flores-Montero J, Rawstron A, Asnafi V, Lécrevisse Q, Lucio P, Mejstrikova E, Szczepanski T, Kalina T, de Tute R, Brüggemann M, Sedek L, Cullen M, Langerak Aw, Mendoça A, Macintyre E, Martin-Ayuso M, Hrusak O, Vidriales Mb, Orfao A. EuroFlow antibody panels for standardized n-dimensional flow cytometric immunophenotyping of normal, reactive and malignant leucocytes. Leukemia 2010; 24, in press.
  37. Dworzak Mn, Fritsch G, Fleischer C, Printz D, Froschl G, Buchinger P, et al. Multiparameter phenotype mapping of normal and post-chemotherapy B lymphopoiesis in pediatric bone marrow. Leukemia. 1997;11:1266–1273
  38. Lucio P, Parreira A, Van Den Beemd Mw, Van Lochem Eg, Van Wering Er, Baars E, et al. Flow cytometric analysis of normal B cell differentiation: a frame of reference for the detection of minimal residual disease in precursor-B-ALL. Leukemia. 1999;13:419–427
  39. Parkin Jl, Arthur Dc, Abramson Cs, Mckenna Rw, Kersey Jh, Heideman Rl, et al. Acute leukemia associated with the t(4;11) chromosome rearrangement: ultrastructural and immunologic characteristics. Blood. 1982;60:1321–1331
  40. Alessandri Aj, Reid Gs, Bader Sa, Massing Bg, Sorensen Ph, Schultz Kr. ETV6 (TEL)-AML1 pre-B acute lymphoblastic leukaemia cells are associated with a distinct antigen-presenting phenotype. Br J Haematol. 2002;116:266–272
  41. De Zen L, Orfao A, Cazzaniga G, Masiero L, Cocito Mg, Spinelli M, et al. Quantitative multiparametric immunophenotyping in acute lymphoblastic leukemia: correlation with specific genotype. I. ETV6/AML1 ALLs identification. Leukemia. 2000;14:1225–1231
  42. Robinson Hm, Broadfield Zj, Cheung Kl, Harewood L, Harris Rl, Jalali Gr, et al. Amplification of AML1 in acute lymphoblastic leukemia is associated with a poor outcome. Leukemia. 2003;17:2249–2250
  43. Soulier J, Trakhtenbrot L, Najfeld V, Lipton Jm, Mathew S, Avet-Loiseau H, et al. Amplification of band q22 of chromosome 21, including AML1, in older children with acute lymphoblastic leukemia: an emerging molecular cytogenetic subgroup. Leukemia. 2003;17:1679–1682
  44. Kerst G, Kreyenberg H, Roth C, Well C, Dietz K, Coustan-Smith E, et al. Concurrent detection of minimal residual disease (MRD) in childhood acute lymphoblastic leukaemia by flow cytometry and real-time PCR. Br J Haematol. 2005;128:774–782
  45. Panzer-Grumayer Er, Cazzaniga G, Van Der Velden Vh, Del Giudice L, Peham M, Mann G, et al. Immunogenotype changes prevail in relapses of young children with TEL-AML1-positive acute lymphoblastic leukemia and derive mainly from clonal selection. Clin Cancer Res. 2005;11:7720–7727
  46. Zuna J, Ford Am, Peham M, Patel N, Saha V, Eckert C, et al. TEL deletion analysis supports a novel view of relapse in childhood acute lymphoblastic leukemia. Clin Cancer Res. 2004;10:5355–5360
  47. Daser A, Rabbitts Th. Extending the repertoire of the mixed-lineage leukemia gene MLL in leukemogenesis. Genes Dev. 2004;18:965–974
  48. Meyer C, Schneider B, Reichel M, Angermueller S, Strehl S, Schnittger S, et al. Diagnostic tool for the identification of MLL rearrangements including unknown partner genes. Proc Natl Acad Sci USA. 2005;102:449–454
  49. Van Der Velden Vh, Corral L, Valsecchi Mg, Jansen Mw, De Lorenzo P, Cazzaniga G, et al. Prognostic significance of minimal residual disease in infants with acute lymphoblastic leukemia treated within the Interfant-99 protocol. Leukemia. 2009;23:1073–1079

PII: S0145-2126(09)00493-7

doi: 10.1016/j.leukres.2009.09.033

Leukemia Research
Volume 34, Issue 4 , Pages 430-437 , April 2010