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Frequent Dysregulation of the c-maf Proto-Oncogene at 16q23 by Translocation to an Ig Locus in Multiple Myeloma

Marta Chesi, P. Leif Bergsagel, Oluwatoyin O. Shonukan, Maria Luisa Martelli, Leslie A. Brents, Theresa Chen, Evelin Schröck, Thomas Ried, and W. Michael Kuehl

From the Genetics Department, Medicine Branch, National Cancer Institute, Bethesda, MD; the Department of Medicine, Division of Hematology and Oncology, Cornell University Medical College, New York, NY; and the Genome Technology Branch, National Institutes of Health-National Center for Human Genome Research, Bethesda, MD.

Dysregulation of oncogenes by translocation to an IgH (14q32) or IgL (kappa , 2p11 or lambda , 22q11) locus is a frequent event in the pathogenesis of B-cell tumors. Translocations involving an IgH locus and a diverse but nonrandom array of chromosomal loci occur in most multiple myeloma (MM) tumors even though the translocations often are not detected by conventional cytogenetic analysis. In a continuing analysis of translocations in 21 MM lines, we show that the novel, karyotypically silent t(14;16)(q32.3;q23) translocation is present in 5 MM lines, with cloned breakpoints from 4 lines dispersed over an approximately 500-kb region centromeric to the c-maf proto-oncogene at 16q23. Another line has a t(16;22)(q23;q11), with the breakpoint telomeric to c-maf, so that the translocation breakpoints in these 6 lines bracket c-maf. Only these 6 lines overexpress c-maf mRNA. As predicted for dysregulation of c-maf by translocation, there is selective expression of one c-maf allele in 2 informative lines with translocations. This is the first human tumor in which the basic zipper c-maf transcription factor is shown to function as an oncogene.

Blood, Vol. 91 No. 12 (June 15), 1998: pp. 4457-4463
© 1998 by The American Society of Hematology.


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K. Ried, M. Finnis, L. Hobson, M. Mangelsdorf, S. Dayan, J. K. Nancarrow, E. Woollatt, G. Kremmidiotis, A. Gardner, D. Venter, et al.
Common chromosomal fragile site FRA16D sequence: identification of the FOR gene spanning FRA16D and homozygous deletions and translocation breakpoints in cancer cells
Hum. Mol. Genet., July 1, 2000; 9(11): 1651 - 1663.
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Am. J. Pathol.Home page
G. Pruneri, S. Fabris, L. Baldini, N. Carboni, S. Zagano, M. A. Colombi, G. Ciceri, L. Lombardi, M. Rocchi, R. Buffa, et al.
Immunohistochemical Analysis of Cyclin D1 Shows Deregulated Expression in Multiple Myeloma with the t(11;14)
Am. J. Pathol., May 1, 2000; 156(5): 1505 - 1513.
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BloodHome page
J. W. G. Janssen, J.-W. Vaandrager, T. Heuser, A. Jauch, P. M. Kluin, E. Geelen, P. L. Bergsagel, W. M. Kuehl, H. G. Drexler, T. Otsuki, et al.
Concurrent activation of a novel putative transforming gene, myeov, and cyclin D1 in a subset of multiple myeloma cell lines with t(11;14)(q13;q32)
Blood, April 15, 2000; 95(8): 2691 - 2698.
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Cancer Res.Home page
A. K. Bednarek, K. J. Laflin, R. L. Daniel, Q. Liao, K. A. Hawkins, and C. M. Aldaz
WWOX, a Novel WW Domain-containing Protein Mapping to Human Chromosome 16q23.3-24.1, a Region Frequently Affected in Breast Cancer
Cancer Res., April 1, 2000; 60(8): 2140 - 2145.
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Cancer Res.Home page
M. Mangelsdorf, K. Ried, E. Woollatt, S. Dayan, H. Eyre, M. Finnis, L. Hobson, J. Nancarrow, D. Venter, E. Baker, et al.
Chromosomal Fragile Site FRA16D and DNA Instability in Cancer
Cancer Res., March 1, 2000; 60(6): 1683 - 1689.
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Cancer Res.Home page
A. J. W. Paige, K. J. Taylor, A. Stewart, J. G. Sgouros, H. Gabra, G. C. Sellar, J. F. Smyth, D. J. Porteous, and J. E. V. Watson
A 700-kb Physical Map of a Region of 16q23.2 Homozygously Deleted in Multiple Cancers and Spanning the Common Fragile Site FRA16D
Cancer Res., March 1, 2000; 60(6): 1690 - 1697.
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BloodHome page
E. E. Plowright, Z. Li, P. L. Bergsagel, M. Chesi, D. L. Barber, D. R. Branch, R. G. Hawley, and A. K. Stewart
Ectopic expression of fibroblast growth factor receptor 3 promotes myeloma cell proliferation and prevents apoptosis
Blood, February 1, 2000; 95(3): 992 - 998.
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Proc. Natl. Acad. Sci. USAHome page
Y. Shou, M. L. Martelli, A. Gabrea, Y. Qi, L. A. Brents, A. Roschke, G. Dewald, I. R. Kirsch, P. L. Bergsagel, and W. M. Kuehl
Diverse karyotypic abnormalities of the c-myc locus associated with c-myc dysregulation and tumor progression in multiple myeloma
PNAS, January 4, 2000; 97(1): 228 - 233.
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J. Virol.Home page
M. Li, X. Huang, Z. Zhu, and E. Gorelik
Sequence and Insertion Sites of Murine Melanoma-Associated Retrovirus
J. Virol., November 1, 1999; 73(11): 9178 - 9186.
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BloodHome page
P. Finelli, S. Fabris, S. Zagano, L. Baldini, D. Intini, L. Nobili, L. Lombardi, A. T. Maiolo, and A. Neri
Detection of t(4;14)(p16.3;q32) Chromosomal Translocation in Multiple Myeloma by Double-Color Fluorescent In Situ Hybridization
Blood, July 15, 1999; 94(2): 724 - 732.
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BloodHome page
M. Chesi, E. Nardini, R. S.C. Lim, K. D. Smith, W. M. Kuehl, and P. L. Bergsagel
The t(4;14) Translocation in Myeloma Dysregulates Both FGFR3 and a Novel Gene, MMSET, Resulting in IgH/MMSET Hybrid Transcripts
Blood, November 1, 1998; 92(9): 3025 - 3034.
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J. Biol. Chem.Home page
T. K. Hale, C. Myers, R. Maitra, T. Kolzau, M. Nishizawa, and A. W. Braithwaite
Maf Transcriptionally Activates the Mouse p53 Promoter and Causes a p53-dependent Cell Death
J. Biol. Chem., June 9, 2000; 275(24): 17991 - 17999.
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J. Biol. Chem.Home page
K. Kataoka, K. Yoshitomo-Nakagawa, S. Shioda, and M. Nishizawa
A Set of Hox Proteins Interact with the Maf Oncoprotein to Inhibit Its DNA Binding, Transactivation, and Transforming Activities
J. Biol. Chem., January 5, 2001; 276(1): 819 - 826.
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J. Biol. Chem.Home page
K. Kataoka, S. Shioda, K. Yoshitomo-Nakagawa, H. Handa, and M. Nishizawa
Maf and Jun Nuclear Oncoproteins Share Downstream Target Genes for Inducing Cell Transformation
J. Biol. Chem., September 21, 2001; 276(39): 36849 - 36856.
[Abstract] [Full Text] [PDF]



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