Recurrent mutations of NOTCH genes in follicular lymphoma identify a distinctive subset of tumours

Journal of Pathology

Volumn 234, Issue 3, 2014, Pages 423-430

  Karube, Kennosuke ^a   Martínez, Daniel ^a   Royo, Cristina ^a   Navarro, Alba ^a   Pinyol, Magda ^a   Cazorla, Maite ^a   Castillo, Paola ^a   Valera, Alexandra ^a   Carrió, Anna ^a   Costa, Dolors ^a   Colomer, Dolors ^a   Rosenwald, Andreas ^b   Ott, German ^c   Esteban, Daniel ^a   Giné, Eva ^a   López Guillermo, Armando ^a   Campo, Elias ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c DR MARGARETE FISCHER BOSCH INSTITUTE OF CLINICAL PHARMACOLOGY   (Germany)

Author keywords

Follicular lymphoma; Mutation; NOTCH1; NOTCH2; Spleen; Transformation

Indexed keywords

NOTCH RECEPTOR; NOTCH2 RECEPTOR; NOTCH1 PROTEIN, HUMAN; NOTCH1 RECEPTOR; NOTCH2 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CARCINOGENESIS; CHROMOSOME TRANSLOCATION; FEMALE; FOLLICULAR LYMPHOMA; GAIN OF FUNCTION MUTATION; GENE FREQUENCY; GENE MUTATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LARGE CELL LYMPHOMA; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPLEEN; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; MIDDLE AGED; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADULT; AGED; DNA MUTATIONAL ANALYSIS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LYMPHOMA, FOLLICULAR; LYMPHOMA, LARGE B-CELL, DIFFUSE; MIDDLE AGED; MUTATION; RECEPTOR, NOTCH1; RECEPTOR, NOTCH2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84925547095     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4428     Document Type: Article

References (43)

1. Swerdlow S, Campo E, Harris N, et al. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues, 4th edn. IARC Press: Lyon, 2009.
2. Lossos IS, Gascoyne RD. Transformation of follicular lymphoma. Best Pract Res Clin Haematol 2011; 24: 147–163.
3. Davies AJ, Rosenwald A, Wright G, et al. Transformation of follicular lymphoma to diffuse large B-cell lymphoma proceeds by distinct oncogenic mechanisms. Br J Haematol 2007; 136: 286–293.
4. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137: 216–233.
5. Fabbri G, Rasi S, Rossi D, et al. Analysis of the chronic lymphocytic leukemia coding genome: role of NOTCH1 mutational activation. J Exp Med 2011; 208: 1389–1401.
6. Puente XS, Pinyol M, Quesada V, et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature 2011; 475: 101–105.
7. Kridel R, Meissner B, Rogic S, et al. Whole transcriptome sequencing reveals recurrent NOTCH1 mutations in mantle cell lymphoma. Blood 2012; 119: 1963–1971.
8. Bea S, Valdes-Mas R, Navarro A, et al. Landscape of somatic mutations and clonal evolution in mantle cell lymphoma. Proc Natl Acad Sci USA 2013; 110: 18250–18255.
9. Kiel MJ, Velusamy T, Betz BL, et al. Whole-genome sequencing identifies recurrent somatic NOTCH2 mutations in splenic marginal zone lymphoma. J ExpMed 2012; 209: 1553–1565.
10. Rossi D, Trifonov V, Fangazio M, et al. The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development. J Exp Med 2012; 209: 1537–1551.
11. Weng AP, Ferrando AA, Lee W, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004; 306: 269–271.
12. Malecki MJ, Sanchez-Irizarry C, Mitchell JL, et al. Leukemia-associated mutations within the NOTCH1 heterodimerization domain fall into at least two distinct mechanistic classes. Mol Cell Biol 2006; 26: 4642–4651.
13. Fryer CJ, White JB, Jones KA. Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol Cell 2004; 16: 509–520.
14. Valera A, Lopez-Guillermo A, Cardesa-Salzmann T, et al. MYC protein expression and genetic alterations have prognostic impact in patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Haematologica 2013; 98: 1554–1562.
15. Agostinelli C, Paterson JC, Gupta R, et al. Detection of LIM domain only 2 (LMO2) in normal human tissues and haematopoietic and non-haematopoietic tumours using a newly developed rabbit monoclonal antibody. Histopathology 2012; 61: 33–46.
16. Kuchinka BD, Kalousek DK, Lomax BL, et al. Interphase cytogenetic analysis of single cell suspensions prepared from previously formalin-fixed and paraffin-embedded tissues. Mod Pathol 1995; 8: 183–186.
17. van Dongen JJ, Langerak AW, Bruggemann M, et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98–3936. Leukemia 2003; 17: 2257–2317.
18. Lopez C, Delgado J, Costa D, et al. Different distribution of NOTCH1 mutations in chronic lymphocytic leukemia with isolated trisomy 12 or associated with other chromosomal alterations. Genes Chromosomes Cancer 2012; 51: 881–889.
19. Lee SY, Kumano K, Nakazaki K, et al. Gain-of-function mutations and copy number increases of Notch2 in diffuse large B-cell lymphoma. Cancer Sci 2009; 100: 920–926.
20. Villamor N, Conde L, Martinez-Trillos A, et al. NOTCH1 mutations identify a genetic subgroup of chronic lymphocytic leukemia patients with high risk of transformation and poor outcome. Leukemia 2013; 27: 1100–1106.
21. Sander CA, Yano T, Clark HM, et al. p53 mutation is associated with progression in follicular lymphomas. Blood 1993; 82: 1994–2004.
22. Takimoto Y, Takafuta T, Imanaka F, et al. Histological progression of follicular lymphoma associated with p53 mutation and rearrangement of the C-MYC gene. Hiroshima J Med Sci 1996; 45: 69–73.
23. Balatti V, Bottoni A, Palamarchuk A, et al. NOTCH1 mutations in CLL associated with trisomy 12. Blood 2012; 119: 329–331.
24. Strefford JC, Sutton LA, Baliakas P, et al. Distinct patterns of novel gene mutations in poor-prognostic stereotyped subsets of chronic lymphocytic leukemia: the case of SF3B1 and subset #2. Leukemia 2013; 27: 2196–2199.
25. Fabbri G, Khiabanian H, Holmes AB, et al. Genetic lesions associated with chronic lymphocytic leukemia transformation to Richter syndrome. J ExpMed 2013; 210: 2273–2288.
26. Guo Y, Karube K, Kawano R, et al. Low-grade follicular lymphoma with t(14;18) presents a homogeneous disease entity otherwise the rest comprises minor groups of heterogeneous disease entities with Bcl2 amplification, Bcl6 translocation or other gene aberrances. Leukemia 2005; 19: 1058–1063.
27. Tagawa H, Karube K, Guo Y, et al. Trisomy 3 is a specific genomic aberration of t(14;18) negative follicular lymphoma. Leukemia 2007; 21: 2549–2551.
28. Karube K, Ying G, Tagawa H, et al. BCL6 gene amplification/3q27 gain is associated with unique clinicopathological characteristics among follicular lymphoma without BCL2 gene translocation. Mod Pathol 2008; 21: 973–978.
29. Leich E, Salaverria I, Bea S, et al. Follicular lymphomas with and without translocation t(14;18) differ in gene expression profiles and genetic alterations. Blood 2009; 114: 826–834.
30. Katzenberger T, Kalla J, Leich E, et al. A distinctive subtype of t(14;18)-negative nodal follicular non-Hodgkin lymphoma characterized by a predominantly diffuse growth pattern and deletions in the chromosomal region 1p36. Blood 2009; 113: 1053–1061.
31. Mollejo M, Rodriguez-Pinilla MS, Montes-Moreno S, et al. Splenic follicular lymphoma: clinicopathologic characteristics of a series of 32 cases. Am J Surg Pathol 2009; 33: 730–738.
32. Pillai S, Cariappa A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat Rev Immunol 2009; 9: 767–777.
33. Simonetti G, Carette A, Silva K, et al. IRF4 controls the positioning of mature B cells in the lymphoid microenvironments by regulating NOTCH2 expression and activity. J ExpMed 2013; 210: 2887–2902.
34. Witt CM, Won WJ, Hurez V, et al. Notch2 haploinsufficiency results in diminished B1 B cells and a severe reduction in marginal zone B cells. J Immunol 2003; 171: 2783–2788.
35. Santos MA, Sarmento LM, Rebelo M, et al. Notch1 engagement by δ-like-1 promotes differentiation of B lymphocytes to antibodysecreting cells. Proc Natl Acad Sci USA 2007; 104: 15454–15459.
36. Yano T, Jaffe ES, Longo DL, et al. MYC rearrangements in histologically progressed follicular lymphomas. Blood 1992; 80: 758–767.
37. Elenitoba-Johnson KS, Gascoyne RD, Lim MS, et al. Homozygous deletions at chromosome 9p21 involving p16 and p15 are associated with histologic progression in follicle center lymphoma. Blood 1998; 91: 4677–4685.
38. Davies AJ, Lee AM, Taylor C, et al. A limited role for TP53 mutation in the transformation of follicular lymphoma to diffuse large B-cell lymphoma. Leukemia 2005; 19: 1459–1465.
39. Pasqualucci L, Khiabanian H, Fangazio M, et al. Genetics of follicular lymphoma transformation. Cell Rep 2014; 6: 130–140.
40. Okosun J, Bodor C, Wang J, et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet 2014; 46: 176–181.
41. Real PJ, Tosello V, Palomero T, et al. γ-Secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia. Nat Med 2009; 15: 50–58.
42. Tosello V, Ferrando AA. The NOTCH signaling pathway: role in the pathogenesis of T-cell acute lymphoblastic leukemia and implication for therapy. Therap Adv Hematol 2013; 4: 199–210.
43. Wu Y, Cain-Hom C, Choy L, et al. Therapeutic antibody targeting of individual Notch receptors. Nature 2010; 464: 1052–1057.