Identification of CUX1 as the recurrent chromosomal band 7q22 target gene in human uterine leiomyoma

Genes Chromosomes and Cancer

Volumn 52, Issue 1, 2013, Pages 11-23

  Schoenmakers, Eric F P M ^a   Bunt, Jens ^a   Hermers, Lianne ^a   Schepens, Marga ^a   Merkx, Gerard ^a   Janssen, Bert ^a   Kersten, Monique ^a   Huys, Erik ^a   Pauwels, Patrick ^b   Debiec Rychter, Maria ^c   Van Kessel, Ad Geurts ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Stichting Laboratoria voor Pathologie en Medische Microbiologie   (Netherlands)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ADULT; ALLELE; ARTICLE; CASE REPORT; CHROMOSOME 14Q; CHROMOSOME 7Q; CHROMOSOME BAND; CHROMOSOME DELETION; CHROMOSOME INVERSION; CUT LIKE HOMEOBOX 1 GENE; CYTOGENETICS; FEMALE; GENE; GENE IDENTIFICATION; GENOME; HUMAN; PRIORITY JOURNAL; UTERUS MYOMA;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHROMOSOMES, HUMAN, PAIR 7; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; LEIOMYOMA; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; REPRESSOR PROTEINS; TUMOR MARKERS, BIOLOGICAL; UTERINE NEOPLASMS;

EID: 84869868424     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22001     Document Type: Article

References (71)

1. Bajekal N, Li TC. 2000. Fibroids, infertility, pregnancy wastage. Hum Reprod Update 6: 614-620.
2. Bodmer D, Schepens M, Eleveld MJ, Schoenmakers EFPM, Geurts van kessel A. 2003. Disruption of a novel gene, DIRC3, and expression of DIRC3-HSPBAP1 fusion transcripts in a case of familial renal cell cancer and t(2;3)(q35;q21). Genes Chrom Cancer 38: 107-116.
3. Boghosian L, Dal Cin O, Sandberg AA. 1988. An interstitial deletion of chromosome 7 may characterize a subgroup of uterine leiomyoma. Cancer Genet Cytogenet 34: 207-208.
4. Bui T-H, Iselius L 1992. t(7;22)9q31;q12) in a uterine leiomyoma. Cancer Genet Cytogenet 59: 219.
5. Cramer SF, Patel A. 1990. The frequency of uterine leiomyomas. Am J Clin Pathol 94: 435-438.
6. Di Lieto A, De Falco M, Pollio F, Mansueto G, Salvatore G, Somma P, Ciociola F. De Rosa G, Sraibano S. 2005. Clinical response, vascular change, and angiogenesis in gonadotropin-releasing hormone analogue-treated women with uterine myomas. J Soc Gynecol Investig 12: 123-128.
7. Fan S-X, Sreekantaiah C, Berger CS, Medchill M, Pedron S, Sandberg AA. 1990. Cytogenetics findings in nine leiomyomas of the uterus. Cancer Genet Cytogenet 47: 179-189.
8. Flake GP, Andersen J, Dixon D. 2003. Etiology and pathogenesis of uterine leiomyomas: A review. Environ Health Perspect 111: 1037-1054.
9. Flierman PA, Oberye JJ, Hulst VP, Blok S. 2005. Rapid reduction of leiomyoma volume during treatment with the GnRH antagonist ganirelix. BJOG 112: 638-642.
10. Geurts van Kessel AH, Tetteroo PA, von dem Borne AE, Hagemeijer A, Bootsma D. 1983. Expression of human myeloid-associated surface antigens in human-mouse myeloid cell hybrids. Proc Natl Acad Sci USA 80: 3748-3752.
11. Goulet B, Baruch A, Moon NS, Poirier M, Sansregret LL, Erickson A, Bogyo M, Nepveu A. 2004. A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor. Mol Cell 14: 207-219.
12. Goulet B, Truscott M, Nepveu A. 2006. A novel proteolytically processed CDP/Cux isoform of 90 kDa is generated by cathepsin L. Biol Chem 387: 1285-1293.
13. Havel G, Dahlenfors R, Wedell B, Mark J. 1989. Similar chromosomal evolution in a uterine stromomyosarcoma and in one of two leiomyomas from the same patient. APMIS 97: 143-146.
14. Heim S, Nilbert M, Vanni R, Floderus UM, Mandahl N, Liedgren S, Lecca U, Mitelman F. 1988. A specific translocation, t(12;14)(q14-15;q23-24), characterizes a subgroup of uterine leiomyoma. Cancer Genet Cytogenet 32: 13-17.
15. Hulea, L, Nepveu A. 2012. CUX1 transcription factors: From biochemical activities and cell-based assays to mouse models and human diseases. Gene 497: 18-26.
16. Ishwad CS, Ferrell RE, Davare J, Meloni AM, Sandberg AA, Surti U. 1995. Molecular and cytogenetic analysis of chromosome 7 in uterine leiomyomas. Genes Chrom Cancer 14: 51-55.
17. Ishwad CS, Ferell RE, Hanley K, Davare J, Meloni AM, Sandberg AA, Surti U. 1997. Two discrete regions of deletion at 7q in uterine leiomyomas. Genes Chrom Cancer 19: 156-160.
18. Jani Sait SN, Dal Cin P, Ovanessoff S, Sandberg AA. 1989. A Uterine leiomyoma showing both t(12;14) and del(7) abnormalities. Cancer Genet Cytogenet 37: 157-161.
19. Kataoka S, Yamada H, Hoshi N, Kudo M, Hareyama H, Sakuragi N, Fujimoto S. 2003. Cytogenetic analysis of uterine leiomyoma: the size, histopathology and GnRHa-response in relation to chromosome karyotype. Eur J Obstet Gynecol Reprod Biol 110: 58-62.
20. Kazmierczak B, Dal Cin P, Wanschura S, Borrmann L, Fusco A, Van den Berghe H, Bullerdiek J. 1998. HMGIY is the target of 6p21.3 rearrangements in various benign mesenchymal tumors. Genes Chrom Cancer 4: 279-285.
21. Kettel LM, Murphy AA, Morales AJ, Rivier J, Vale W, Yen SS. 1993. Rapid regression of uterine leiomyomas in response to daily administration of gonadotropin-releasing hormone antagonist. Fertil Steril 60: 642-646.
22. Kiechle-Schwarz M, Sreekantaiah C, Berger CS, Pedron S, Medchill MT, Surti U, Sandberg AA. 1991. Nonrandom cytogenetic changes in Leiomyomas of the female genitourinary tract. A report of 35 cases. Cancer Genet Cytogenet 53: 125-136.
23. Klampfl, T, Harutyunyan A, Berg T, Gisslinger B, Schalling M, Bagienski K, Olcaydu D, Passamonti F, Rumi E, Pietra D, Jäger R, Pieri L, Guglielmelli P, Iacobucci I, Martinelli G, Cazzola M, Vannucchi AM, Gisslinger H, Kralovics R. 2011. Genome integrity of myeloproliferative neoplasms in chronic phase and during disease progression. Blood 118: 167-176.
24. Krzywinski M, Bosdet I, Smailus D, Chiu R, Mathewson C, Wye N, Barber S, Brown-John M, Chan S, Chand S, Cloutier A, Girn N, Lee D, Masson A, Mayo M, Olson T, Pandoh P, Prabhu AL, Schoenmakers E, Tsai M, Albertson D, Lam W, Choy CO, Osoegawa K, Zhao S, de Jong PJ, Schein J, Jones S, Marra MA. 2004. A set of BAC clones spanning the human genome. Nucleic Acids Res 32: 3651-3660.
25. Mäkinen N, Mehine M, Tolvanen J, Kaasinen E, Li Y, Lehtonen HJ, Gentile M, Yan J, Enge M, Taipale M, Aavikko M, Katainen R, Virolainen E, Böhling T, Koski TA, Launonen V, Sjöberg J, Taipale J, Vahteristo P, Aaltonen LA. 2011. MED12, the mediator complex subunit 12 gene, is mutated at high frequency in uterine leiomyomas. Science 334: 252-255.
26. Mao X, Barfoot R, Hamoudi RA, Easton DF, Flanagan AM, Stratton MR. 1999. Allelotype of uterine leiomyomas. Cancer Genet Cytogenet 114: 89-95.
27. Mark J, Havel G, Grepp C, Dahlenfors R, Wedell B. 1988. Cytogenetical observations in human benign uterine leiomyomas. Anticancer Res 8: 621-626.
28. Mark J, Havel G, Grepp C, Dahlenfors R, Wedell B. 1990. Chromosomal patterns in human benign uterine leiomyomas. Cancer Genet Cytogenet 44: 1-13.
29. Markowski DN, Bartnitzke S, Löning T, Drieschner N, Helmke BM, Bullerdiek J. 2012. MED12 mutations in uterine fibroids-their relationship to cytogenetic subgroups. Int J Cancer 131: 1528-1536.
30. Mashal, RD, Fejzo ML, Friedman AJ, Mitchner N, Nowak RA, Rein MS, Morton CC, Sklar J. 1994. Analysis of androgen receptor DNA reveals the independent clonal origins of uterine leiomyomata and the secondary nature of cytogenetic aberrations in the development of leiomyomata. Genes Chrom Cancer 11: 1-6.
31. Meloni AM, Surti U, Contento AM, Davare J, Sandberg AA. 1992. Uterine leiomyomas: Cytogenetic and histologic profile. Obstet Gynecol 80: 209-217.
32. Mitelman F, Johansson B, Mertens F, editors. 2012. Mitelman Database of Chromosome Aberrations in Cancer. Available at: http://cgap.nci.nih.gov/Chromosomes/Mitelman.
33. Moon NS, Premdas P, Truscott M, Leduy L, Bérubé G, Nepveu A. 2001. S phase-specific proteolytic cleavage is required to activate stable DNA binding by the CDP/Cut homeodomain protein. Mol Cell Biol 21: 6332-6345.
34. Moore SD, Herrick SR, Ince TA, Kleinman MS, Dal Cin P, Morton CC, Quade BJ. 2004. Uterine leiomyomata with t(10;17) disrupt the histone acetyltransferase MORF Cancer Res 64: 5570-5577.
35. Murase E, Siegelman ES, Outwater EK, Perez-Jaffe LA, Tureck RW. 1999. Uterine leiomyomas: Histopathologic features, MR imaging findings, differential diagnosis, and treatment. Radiographics 19: 1179-1197.
36. Nepveu A. 2001. Role of the multifunctional CDP/Cut/Cux homeodomain transcription factor in regulating differentiation, cell growth and development. Gene 270: 1-15.
37. Nilbert M, Heim S, Mandahl N, Flodérus U-M, Willén H, Mitelman F. 1989. Different karyotypic abnormalities, t(1;6) and del(7), in two uterine leiomyomas from the same patient. Cancer Genet Cytogenet 42: 51-53.
38. Nilbert M, Heim S, Mandahl N, Flodérus U-M, Willén H, Mitelman F. 1990. Characteristic chromosome abnormalities, including rearrangements of 6p, del(7q), +12, and t(12;14), in 44 uterine leiomyomas. Hum Genet 85: 605-611.
39. Ochman, H., Gerber, A.S., and Hartl, D.L. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621-623.
40. Ozisik YY, Meloni AM, Powell M, Surti U, Sandberg AA. 1993. Deletion 7q22 in uterine leiomyomata. A cytogenetic review. Cancer Genet Cytogenet 67: 59-64.
41. Ozisik YY, Meloni AM, Surti U, Sandberg AA. 1993. Deletion 7q22 in uterine leiomyoma. Cancer Genet Cytogenet 71: 1-6.
42. Pandis N, Heim S, Bardi G, Flodérus UM, Willén H, Mandahl N, Mitelman F. 1990. Parallel karyotypic evolution and tumor progression in uterine leiomyoma. Genes Chrom Cancer 2: 311-317.
43. Pandis N, Heim S, Bardi G, Flodérus U-M, Willén H, Mandahl N, Mitelman F. 1991. Chromosome analysis of 96 uterine leiomyomas. Cancer Genet Cytogenet 55: 11-18.
44. Rein MS, Friedman AJ, Berbieri RL, Pavelka K, Fletcher JA, Morton CC. 1991. Cytogenetic abnormalities in uterine leiomyomata. Obstet Gynecol 77: 923-926.
45. van Rijk A, Sweers M, Huys E, Kersten M, Merkx G, Debiec-Rychter M, Geurts van Kessel A, Schoenmakers EFPM. 2009. Characterization of the recurrent t(1;2)(p36;p24) chromosomal translocation in human uterine leiomyoma. Cancer Genet Cytogenet 193: 54-62.
46. Sandberg AA. 2005. Updates on the cytogenetics and molecular genetics of bone and soft tissue tumors: Leiomyoma. Cancer Genet Cytogenet 158: 1-26.
47. Sansregret L, Nepveu A. 2008. The multiple roles of CUX1: Insights from mouse models and cell-based assays. Gene 412: 84-94.
48. Sansregret L, Gallo D, Santaguida M, Leduy L, Harada R, Nepveu A. 2010. Hyperphosphorylation by cyclin B/CDK1 in mitosis resets CUX1 DNA binding clock at each cell cycle. J Biol Chem 285: 32834-32843.
49. Santaguida M, Ding Q, Bérubé G, Truscott M, Whyte P, Nepveu A. 2001. Phosphorylation of the CCAAT displacement protein (CDP)/Cux transcription factor by cyclin A-Cdk1 modulates its DNA binding activity in G(2). J Biol Chem 276: 45780-45790.
50. Santaguida M, Nepveu A. 2005. Differential regulation of CDP/Cux p110 by cyclin A/Cdk2 and cyclin A/Cdk1. J Biol Chem 280: 32712-32721.
51. Sargent MS, Weremowicz S, Rein MS, Morton CC. 1994. Translocations in 7q22 define a critical region in uterine leiomyomata. Cancer Genet Cytogenet 77: 65-68.
52. Schoenmakers EF, Wanschura S, Mols R, Bullerdiek J, Van den Berghe H, Van de Ven WJ. 1995. Recurrent rearrangements in the high mobility group protein gene, HMGI-C, in benign mesenchymal tumours. Nat Genet 10: 436-444.
53. Schoenmakers EF, Huysmans C, Van de Ven WJ. 1999. Allelic knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas. Cancer Res 59: 19-23.
54. Schoenmakers, EFPM. Functional integration of alternative cytogenetic routes triggering uterine leiomyomatosis. Oral presentation at the 10th European Workshop on Molecular Cytogenetics in Human solid Tumors/COST B19 workgroup 3 Meeting, La Grande Motte, France, June 8-10, 2006.
55. Sell SM, Altungoz O, Prowse AA, Meloni AM, Surti U, Sandberg AA. 1998. Molecular analysis of chromosome 7q21.3 in uterine leiomyoma: Analysis using markers with linkage to insulin resistance. Cancer Genet Cytogenet 100: 165-168.
56. Sell SM, Tullis C, Stracner D, Song CY, Gewin J. 2005. Minimal interval defined on 7q in uterine leiomyoma. Cancer Genet Cytogenet 157: 67-69.
57. Suijkerbuijk RF, Sinke RJ, Weghuis DE, Roque L, Forus A, Stellink F, Siepman A, van de Kaa C, Soares J, Geurts van Kessel AH. 1994. Amplification of chromosome subregion 12p11.2-p12.1 in a metastasis of an I(12p)-negative seminoma: Relationship to progression? Cancer Genet Cytogenet 78: 145-152.
58. Takahashi K, Kawamura N, Tsujimura A, Ichimura T, Ito F, Ishiko O, Ogita S. 2001. Association of the shrinkage of uterine leiomyoma treated with GnRH agonist and deletion of long arm of chromosome 7. Int J Oncol 18: 1259-1263.
59. Truscott M, Denault JB, Goulet B, Leduy L, Salvesen GS, Nepveu A. 2007. Carboxylterminal proteolytic processing of CUX1 by a caspase enables transcriptional activation in proliferating cells. J Biol Chem 282: 30216-30226.
60. Turc-Carel C, Dal Cin P, Boghosian L, Terk-Zakarian J, Sandberg AA. 1988. Consistent breakpoints in region 14q22-q24 in uterine leiomyoma. Cancer Genet Cytogenet 32: 25-31.
61. Vadnais C, Davoudi S, Afshin M, Harada R, Dudley R, Clermont PL, Drobetsky E, Nepveu A. 2012. CUX1 transcription factor is required for optimal ATM/ATR-mediated responses to DNA damage. Nucleic Acids Res 40: 4483-4495.
62. Van der Heijden O, Chiu H-C, Park T-C, Takahashi H, LiVolsi VA, Risinger JI, Barrett JC, Berchuck A, Evans AC, Behbekht K, Menzin AW, Liu PC, Benjamin I, Morgan MA, King SA, Rubin SJ, Boyd J. 1998. Allelotype analysis of uterine leiomyoma: localization of a potential tumor suppressor gene to a 4-cM region of chromosome 7q. Molecular Carcinogenesis 23: 243-247.
63. Vanharanta S, Wortham NC, Laiho P, Sjöberg J, Aittomäki K, Arola J, Tomlinson IP, Karhu A, Arango D, Aaltonen LA. 2005. 7q deletion mapping and expression profiling in uterine fibroids. Oncogene 24: 6545-6554.
64. Vanharanta S, Wortham NC, Langford C, El-Bahrawy M, van der Spuy Z, Sjöberg J, Lehtonen R, Karhu A, Tomlinson IP, Aaltonen LA. 2007. Definition of a minimal region of deletion of chromosome 7 in uterine leiomyomas by tiling-path microarray CGH and mutation analysis of known genes in this region. Genes Chromosomes Cancer 46: 451-458.
65. Vanni R, Lecca U, Faa G. 1991. Uterine leiomyoma cytogenetics. II. Report of forty cases. Cancer Genet Cytogenet 53: 247-256.
66. Vanni R, Marras S, Schoenmakers EFPM, Dal Cin P, Kazmierczak B, Senger G, Bullerdiek J, ven de Van WJM, van den Berghe H. 1997. Molecular cytogenetic characterization of del(7q) in two uterine leiomyoma-derived cell lines. Genes Chrom Cancer 18: 155-161.
67. Vanni R, Schoenmakers EFPM, Andria M. 1999. Deletion 7q in uterine leiomyoma: Fluorescence in situ hybridization characterization on primary cytogenetic preparations. Cancer Genet Cytogenet 113: 183-187.
68. Vollenhoven BJ, Lawrence AS, Healy DL. 1997. Uterine Fibroids. Br J Obstet Gynaecol 97: 285-298.
69. Xing YP, Scherer SW, Tsui L-C, Morton CC. 1995. Identification of YACs flanking the 7q breakpoint region in uterine leiomyoma: Report on the second international workshop on human chromosome 7 mapping 1994. Cytogenet Cell Genet 71: 27-28.
70. Xing YP, Powell WL, Morton CC. 1997. The del(7q) subgroup in uterine leiomyomata: Genetic and biologic characteristics. Cancer Genet Cytogenet 98: 69-74.
71. Zeng WR, Scherer SW, Koutsilieris M, Huizenga JJ, Filteau F, Tsui L-C, Nepveu A. 1997. Loss of heterozygosity and reduced expression of the CUTL1 gene in uterine leiomyomas. Oncogene 14: 2355-2365.