Biopolym. Cell. 2014; 30(2):90-95.
Огляди
Транслокації, обумовлені локусом важкого ланцюга гена імуноглобуліну людини
1, 2, 3Скляр І. В., 2, 3Ярова О. В., 1, 3Ліпінський М., 2, 3Васецький Є. С.
  1. Інститут Густава Русі
    вул. Едуарда Вальян, 114, Вільжюіф, Франція, 94805
  2. Інститут біології гена РАН
    вул. Вавілова 34/5, Москва, Російська Федерація, 119334
  3. LIA 1066 Об'єднана французько-російська лабораторія з дослідження раку
    Вільжюіф, Франція-Москва, Російська Федерація

Abstract

Транслокації за участі локуса важкого ланцюга гена імуноглобулінів відіграють певну роль в онкогенезі багатьох лімфом і лейкемій, серед яких множинна мієлома, лімфома мантійної зони, лімфома Беркітта та дифузна В-клітинна лімфома. На основі аналізу опублікованих даних ми виділили 11 областей, у яких відбу- ваються транслокації, що призводять до вищезгаданих лімфом і лейкемій. Кожна з таких областей (розміром приблизно 1000 пар нуклеотидів) може брати участь у транслокаціях, які спричиняють один або декілька типів раку. Отримані результати можна використовувати при розробці діагностики транслокацій, які ви- кликають рак крові, а також при ідентифікації потенційних транслокаційних партнерів локуса важкого ланцюга гена імуно- глобулінів на різних стадіях диференціювання В-лімфоцитів.
Keywords: транслокації, важкий ланцюг імуноглобуліну людини, онкогенез, лімфома, лейкемія, диференціювання В-клітин

References

[1] Boveri T. Zur Frage der Entstehung maligner Tumoren. Jena: G. Fisher, 1914; 64 p.
[2] Balmain A. Cancer genetics: from Boveri and Mendel to microarrays. Nat Rev Cancer. 2001; 1(1):77–82.
[3] Nambiar M, Raghavan SC. How does DNA break during chromosomal translocations? Nucleic Acids Res. 2011; 39(14): 5813–25.
[4] Negritto MC. Repairing double-strand DNA breaks. Nature Education. 2010; 3(9):26.
[5] Lieber MR. Warner-Lambert/Parke-Davis award lecture. Pathological and physiological double-strand breaks: roles in cancer, aging, and the immune system. Am J Pathol. 1998; 153 (5):1323–32.
[6] Maizels N. Immunoglobulin gene diversification. Annu Rev Genet. 2005; 39:23–46.
[7] Karanjawala ZE, Hinton DR, Oh E, Hsieh CL, Lieber MR. Developmental retinal apoptosis in Ku86–/– mice. DNA Repair (Amst). 2003; 2(12):1429–34.
[8] Korsmeyer SJ. Chromosomal translocations in lymphoid malignancies reveal novel proto-oncogenes. Annu Rev Immunol. 1992; 10:785–807.
[9] Taub R, Kirsch I, Morton C, Lenoir G, Swan D, Tronick S, Aaronson S, Leder P. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc Natl Acad Sci USA. 1982; 79(24):7837–41.
[10] Mitelman F, Johansson B, Mertens F. Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer. Nat. Genet. 2004; 36(4):331–4.
[11] Harewood L, Schutz F, Boyle S, Perry P, Delorenzi M, Bickmore WA, Reymond A. The effect of translocation-induced nuclear reorganization on gene expression. Genome Res. 2010; 20(5):554–64.
[12] Allinne J, Pichugin A, Iarovaia O, Klibi M, Barat A, Zlotek-Zlotkiewicz E, Markozashvili D, Petrova N, Camara-Clayette V, Ioudinkova ES, Wiels J, Razin SV, Ribrag V, Lipinski M, Vassetzky YS. Perinucleolar relocalization and nucleolin as crucial events in the transcriptional activation of key genes in mantle cell lymphoma. Blood. 2014;
[13] Revy P, Muto T, Levy Y, Geissmann F, Plebani A, Sanal O, Catalan N, Forveille M, Dufourcq-Labelouse R, Gennery A, Tezcan I, Ersoy F, Kayserili H, Ugazio AG, Brousse N, Muramatsu M, Notarangelo LD, Kinoshita K, Honjo T, Fischer A, Durandy A. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell. 2000; 102(5):565–75.
[14] Di Noia JM, Neuberger MS. Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem. 2007; 76:1–22.
[15] Reth M, Radbruch A, Alt F, Honjo T, Alt FW, Neuberger M. Molecular biology of B cells. 1st ed. London: Elsevier. 2004; 600 p.
[16] Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000; 102(5):553–63.
[17] Lieber MR. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem. 2010; 79:181–211.
[18] Klein U, Dalla-Favera R. Germinal centres: role in B-cell physiology and malignancy. Nat Rev Immunol. 2008; 8(1):22–33.
[19] Yu K, Chedin F, Hsieh CL, Wilson TE, Lieber MR. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat Immunol. 2003; 4(5):442–51.
[20] Peled JU, Kuang FL, Iglesias-Ussel MD, Roa S, Kalis SL, Goodman MF, Scharff MD. The biochemistry of somatic hypermutation. Annu Rev Immunol. 2008; 26:481–511.
[21] Lefranc M-P. IGH (Immunoglobulin Heavy) (14q32.33). Atlas Genet Cytogenet Oncol Haematol. 2000; 4(3):278–289.
[22] Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y, Difilippantonio S, Bolland DJ, Chen HT, Corcoran AE, Nussenzweig A, Nussenzweig MC. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell. 2008; 135(6):1028–38.
[23] Unniraman S, Schatz DG. AID and Igh switch region-Myc chromosomal translocations. DNA Repair (Amst). 2006; 5(9–10): 1259–64.
[24] Okazaki IM, Kotani A, Honjo T. Role of AID in tumorigenesis. Adv Immunol. 2007; 94:245–73.
[25] Duquette ML, Pham P, Goodman MF, Maizels N. AID binds to transcription-induced structures in c-MYC that map to regions associated with translocation and hypermutation. Oncogene. 2005; 24(38):5791–8.
[26] Meissner B, Bartram T, Eckert C, Trka J, Panzer-Grumayer R, Hermanova I, Ellinghaus E, Franke A, Moricke A, Schrauder A, Teigler-Schlegel A, Dorge P, Von Stackelberg A, Basso G, Bartram CR, Kirschner-Schwabe R, Bornhauser B, Bourquin JP, Cazzaniga G, Hauer J, Attarbaschi A, Izraeli S, Zaliova M, Cario G, Zimmermann M, Avigad S, Sokalska-Duhme M, Metzler M, Schrappe M, Koehler R, Te Kronnie G, Stanulla M. Frequent and sex-biased deletion of SLX4IP by illegitimate V(D)J-mediated recombination in childhood acute lymphoblastic leukemia. Hum Mol Genet. 2014; 23(3):590–601.
[27] Jardin F, Bastard C, Contentin N, Parmentier F, Picquenot JM, Tilly H, Stevenson FK, Sahota SS. Intronic BCL-6 mutations are preferentially targeted to the translocated allele in t(3;14)(q27; q32) non-Hodgkin B-cell lymphoma. Blood. 2003; 102(5): 1872–6.
[28] Greisman HA, Lu Z, Tsai AG, Greiner TC, Yi HS, Lieber MR. IgH partner breakpoint sequences provide evidence that AID initiates t(11;14) and t(8;14) chromosomal breaks in mantle cell and Burkitt lymphomas. Blood. 2012; 120(14):2864–7.
[29] van de Werken HJ, de Vree PJ, Splinter E, Holwerda SJ, Klous P, de Wit E, de Laat W. 4C technology: protocols and data analysis. Methods Enzymol. 2012; 513:89–112.
[30] Akasaka T, Balasas T, Russell LJ, Sugimoto KJ, Majid A, Walewska R, Karran EL, Brown DG, Cain K, Harder L, Gesk S, Martin-Subero JI, Atherton MG, Bruggemann M, Calasanz MJ, Davies T, Haas OA, Hagemeijer A, Kempski H, Lessard M, Lillington DM, Moore S, Nguyen-Khac F, Radford-Weiss I, Schoch C, Struski S, Talley P, Welham MJ, Worley H, Strefford JC, Harrison CJ, Siebert R, Dyer MJ. Five members of the CEBP transcription factor family are targeted by recurrent IGH translocations in B-cell precursor acute lymphoblastic leukemia (BCPALL). Blood. 2007; 109(8):3451–61.
[31] Kawamata N, Nakamura Y, Miki T, Sato E, Isobe Y, Furusawa S, Hirosawa S, Oshimi K. Detection of chimaeric transcripts of the immunoglobulin heavy chain and BCL6 genes by reversetranscriptase polymerase chain reaction in B-cell non-Hodgkin's lymphomas. Br J Haematol. 1998; 100(3):484–9.
[32] Sonoki T, Harder L, Horsman DE, Karran L, Taniguchi I, Willis TG, Gesk S, Steinemann D, Zucca E, Schlegelberger B, Sole F, Mungall AJ, Gascoyne RD, Siebert R, Dyer MJ. Cyclin D3 is a target gene of t(6;14)(p21.1;q32.3) of mature B-cell malignancies. Blood. 2001; 98(9):2837–44.
[33] Chesi M, Bergsagel PL, Brents LA, Smith CM, Gerhard DS, Kuehl WM. Dysregulation of cyclin D1 by translocation into an IgH gamma switch region in two multiple myeloma cell lines. Blood. 1996; 88(2):674–81.
[34] Fenton JA, Pratt G, Rawstron AC, Sibley K, Rothwell D, Yates Z, Dring A, Richards SJ, Ashcroft AJ, Davies FE, Owen RG, Child JA, Morgan GJ. Genomic characterization of the chromosomal breakpoints of t(4;14) of multiple myeloma suggests more than one possible aetiological mechanism. Oncogene. 2003; 22(7): 1103–13.
[35] Kobayashi S, Taki T, Chinen Y, Tsutsumi Y, Ohshiro M, Kobayashi T, Matsumoto Y, Kuroda J, Horiike S, Nishida K, Taniwaki M. Identification of IGHCdelta-BACH2 fusion transcripts resulting from cryptic chromosomal rearrangements of 14q32 with 6q15 in aggressive B-cell lymphoma/leukemia. Genes Chromosomes Cancer. 2011; 50(4):207–16.
[36] Degan M, Doliana R, Gloghini A, Di Francia R, Aldinucci D, Mazzocut-Zecchin L, Colombatti A, Attadia V, Carbone A, Gattei V. A novel bcl-1/JH breakpoint from a patient affected by mantle cell lymphoma extends the major translocation cluster. J Pathol. 2002; 197(2):256–63.
[37] Moulding C, Rapoport A, Goldman P, Battey J, Lenoir GM, Leder P. Structural analysis of both products of a reciprocal translocation between c-myc and immunoglobulin loci in Burkitt lymphoma. Nucleic Acids Res. 1985; 13(6):2141–52
[38] Gutierrez MI, Bhatia K, Barriga F, Diez B, Muriel FS, De Andreas ML, Epelman S, Risueno C, Magrath IT. Molecular epidemiology of Burkitt's lymphoma from South America: differences in breakpoint location and Epstein-Barr virus association from tumors in other world regions. Blood. 1992; 79(12):3261–6.
[39] Siebert R, Matthiesen P, Harder S, Zhang Y, Borowski A, Zuhlke-Jenisch R, Metzke S, Joos S, Weber-Matthiesen K, Grote W, Schlegelberger B. Application of interphase fluorescence in situ Hybridization for the detection of the Burkitt translocation t(8; 14)(q24;q32) in B-cell lymphomas. Blood. 1998; 91(3):984–90.
[40] Busch K, Borkhardt A, Wossmann W, Reiter A, Harbott J. Combined polymerase chain reaction methods to detect c-myc/IgH rearrangement in childhood Burkitt's lymphoma for minimal residual disease analysis. Haematologica. 2004; 89(7):818–25.
[41] Muller JR, Janz S, Potter M. Differences between Burkitt's lymphomas and mouse plasmacytomas in the immunoglobulin heavy chain/c-myc recombinations that occur in their chromosomal translocations. Cancer Res. 1995; 55(21):5012–8.
[42] Neri A, Barriga F, Knowles DM, Magrath IT, Dalla-Favera R. Different regions of the immunoglobulin heavy-chain locus are involved in chromosomal translocations in distinct pathogenetic forms of Burkitt lymphoma. Proc Natl Acad Sci USA. 1988; 85 (8):2748–52.
[43] Busch K, Keller T, Fuchs U, Yeh RF, Harbott J, Klose I, Wiemels J, Novosel A, Reiter A, Borkhardt A. Identification of two distinct MYC breakpoint clusters and their association with various IGH breakpoint regions in the t(8;14) translocations in sporadic Burkitt-lymphoma. Leukemia. 2007; 21(8):1739–51.
[44] Guikema JE, De Boer C, Haralambieva E, Smit LA, Van Noesel CJ, Schuuring E, Kluin PM. IGH switch breakpoints in Burkitt lymphoma: exclusive involvement of noncanonical class switch recombination. Genes Chromosomes Cancer. 2006; 45(9): 808–19.
[45] Wilda M, Busch K, Klose I, Keller T, Woessmann W, Kreuder J, Harbott J, Borkhardt A. Level of MYC overexpression in pediatric Burkitt's lymphoma is strongly dependent on genomic breakpoint location within the MYC locus. Genes Chromosomes Cancer. 2004; 41(2):178–82.
[46] Siebert R, Matthiesen P, Harder S, Zhang Y, Borowski A, Zuhlke-Jenisch R, Plendl H, Metzke S, Joos S, Zucca E, Weber-Matthiesen K, Roggero E, Grote W, Schlegelberger B. Application of interphase cytogenetics for the detection of t(11;14)(q13;q32) in mantle cell lymphomas. Ann Oncol. 1998; 9(5):519–26.
[47] Andersen NS, Donovan JW, Borus JS, Poor CM, Neuberg D, Aster JC, Nadler LM, Freedman AS, Gribben JG. Failure of immunologic purging in mantle cell lymphoma assessed by polymerase chain reaction detection of minimal residual disease. Blood. 1997; 90(10):4212–21.
[48] Ronchetti D, Finelli P, Richelda R, Baldini L, Rocchi M, Viggiano L, Cuneo A, Bogni S, Fabris S, Lombardi L, Maiolo AT, Neri A. Molecular analysis of 11q13 breakpoints in multiple myeloma. Blood. 1999; 93(4):1330–7.
[49] Welzel N, Le T, Marculescu R, Mitterbauer G, Chott A, Pott C, Kneba M, Du MQ, Kusec R, Drach J, Raderer M, Mannhalter C, Lechner K, Nadel B, Jaeger U. Templated nucleotide addition and immunoglobulin JH-gene utilization in t(11;14) junctions: implications for the mechanism of translocation and the origin of mantle cell lymphoma. Cancer Res. 2001; 61(4):1629–36.
[50] Murga Penas EM, Callet-Bauchu E, Ye H, Gazzo S, Berger F, Schilling G, Albert-Konetzny N, Vettorazzi E, Salles G, Wlodarska I, Du MQ, Bokemeyer C, Dierlamm J. The t(14;18)(q32; q21)/IGH-MALT1 translocation in MALT lymphomas contains templated nucleotide insertions and a major breakpoint region similar to follicular and mantle cell lymphoma. Blood. 2010; 115(11):2214–9.
[51] Tsai AG, Lu Z, Lieber MR. The t(14;18)(q32;q21)/IGH-MALT1 translocation in MALT lymphomas is a CpG-type translocation, but the t(11;18)(q21;q21)/API2-MALT1 translocation in MALT lymphomas is not. Blood. 2010; 115(17):3640–1.
[52] Jaeger U, Purtscher B, Karth GD, Knapp S, Mannhalter C, Lechner K. Mechanism of the chromosomal translocation t(14;18) in lymphoma: detection of a 45-Kd breakpoint binding protein. Blood. 1993; 81(7):1833–40.
[53] Butler MP, Iida S, Capello D, Rossi D, Rao PH, Nallasivam P, Louie DC, Chaganti S, Au T, Gascoyne RD, Gaidano G, Chaganti RS, Dalla-Favera R. Alternative translocation breakpoint cluster region 5' to BCL-6 in B-cell non-Hodgkin's lymphoma. Cancer Res. 2002; 62(14):4089–94.
[54] Rimokh R, Berger F, Delsol G, Digonnet I, Rouault JP, Tigaud JD, Gadoux M, Coiffier B, Bryon PA, Magaud JP. Detection of the chromosomal translocation t(11;14) by polymerase chain reaction in mantle cell lymphomas. Blood. 1994; 83(7):1871–5.
[55] Stamatopoulos K, Kosmas C, Belessi C, Kyriazopoulos P, Papadaki T, Anagnostou D, Loukopoulos D. Molecular analysis of bcl-1/IgH junctional sequences in mantle cell lymphoma: potential mechanism of the t(11;14) chromosomal translocation. Br J Haematol. 1999; 105(1):190–7.
[56] Harris RS, Croom-Carter DS, Rickinson AB, Neuberger MS. Epstein-Barr virus and the somatic hypermutation of immunoglobulin genes in Burkitt's lymphoma cells. J Virol. 2001; 75(21): 10488–92.
[57] Gabrea A, Leif Bergsagel P, Michael Kuehl W. Distinguishing primary and secondary translocations in multiple myeloma. DNA Repair (Amst). 2006; 5(9–10):1225–33.
[58] Lenz G, Nagel I, Siebert R, Roschke AV, Sanger W, Wright GW, Dave SS, Tan B, Zhao H, Rosenwald A, Muller-Hermelink HK, Gascoyne RD, Campo E, Jaffe ES, Smeland EB, Fisher RI, Kuehl WM, Chan WC, Staudt LM. Aberrant immunoglobulin class switch recombination and switch translocations in activated B cell-like diffuse large B cell lymphoma. J Exp Med. 2007; 204 (3):633–43.
[59] Khodabakhshi AH, Morin RD, Fejes AP, Mungall AJ, Mungall KL, Bolger-Munro M, Johnson NA, Connors JM, Gascoyne RD, Marra MA, Birol I, Jones SJ. Recurrent targets of aberrant somatic hypermutation in lymphoma. Oncotarget. 2012; 3(11): 1308–19.