Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome

Human Molecular Genetics

Volumn 14, Issue 6, 2005, Pages 813-825

  Mann, Michael B ^a,b   Hodges, Craig A ^a   Barnes, Ellen ^a,b   Vogel, Hannes ^c   Hassold, Terry J ^a   Luo, Guangbin ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECQ HELICASE;

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BONE DEFECT; CANCER SUSCEPTIBILITY; CENTROMERE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CONTROLLED STUDY; DISEASE MODEL; GENE MUTATION; GENETIC ANALYSIS; GENETIC STABILITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; RASH; ROTHMUND THOMSON SYNDROME; SENSITIZATION; SISTER CHROMATID;

ADENOSINE TRIPHOSPHATASES; ANEUPLOIDY; ANIMALS; CHROMATIDS; CHROMOSOMAL INSTABILITY; DISEASE MODELS, ANIMAL; DNA HELICASES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE; MICE, MUTANT STRAINS; MUTATION; NEOPLASMS; RECQ HELICASES; ROTHMUND-THOMSON SYNDROME;

EID: 15544389502     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddi075     Document Type: Article

References (65)

1. Duesberg, P. and Rasnick, D. (2000) Aneuploidy, the somatic mutation that makes cancer a species of its own. Cell Motil. Cytoskeleton, 47, 81-107.
2. Gebhart, E. and Liehr, T. (2000) Patterns of genomic imbalances in human solid tumors (Review). Int. J. Oncol., 16 383-399.
3. Lengauer, C., Kinzler, K.W. and Vogelstein, B. (1998) Genetic instabilities in human cancers. Nature, 396, 643-649.
4. Mertens, F., Johansson, B., Hoglund, M. and Mitelman, F. (1997) Chromosomal imbalance maps of malignant solid tumors: a cytogenetic survey of 3185 neoplasms. Cancer Res., 57, 2765-2780.
5. Nicklas, R.B. (1997) How cells get the right chromosomes. Science, 275, 632-637.
6. Nicklas, R.B. and Koch, C.A. (1969) Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J. Cell Biol., 43, 40-50.
7. Rieder, C.L. and Salmon, E.D. (1998) The vertebrate cell kinetochore and its roles during mitosis. Trends Cell Biol., 8 310-318.
8. Nasmyth, K. (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science, 297, 559-565.
9. Uhlmann, F. (2001) Chromosome cohesion and segregation in mitosis and meiosis. Curr Opin. Cell Biol., 13, 754-761.
10. Cleveland, D.W., Mao, Y. and Sullivan, K.F. (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell, 112, 407-421.
11. Hickson, I.D. (2003) RecQ helicases: caretakers of the genome. Nat. Rev. Cancer, 3, 169-178.
12. Watt, P.M., Louis, E.J., Borts, R.H. and Hickson, I.D. (1995) Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell, 81, 253-260.
13. Watt, P.M., Hickson, I.D., Borts, R.H. and Louis, E.J. (1996) SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics, 144, 935-945.
14. Stewart, E., Chapman, C.R., Al-Khodairy, F., Carr, A.M. and Enoch, T. (1997) rqh1+, A fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J., 16, 2682-2692.
15. Gangloff, S., McDonald, J.P., Bendixen, C., Arthur, L. and Rothstein, R. (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol., 14, 8391-8398.
16. Ahmad, F., Kaplan, C.D. and Stewart, E. (2002) Helicase activity is only partially required for Schizosaccharomyces pombe Rqh1p function. Yeast, 19, 1381-1398.
17. Kitao, S., Ohsugi, I., Ichikawa, K., Goto, M., Furuichi, Y. and Shimamoto, A. (1998) Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics, 54, 443-452.
18. Kitao, S., Lindor, N.M., Shiratori, M., Furuichi, Y. and Shimamoto, A. (1999) Rothmund-Thomson syndrome responsible gene, RECQL4: genomic structure and products. Genomics, 61, 268-276.
19. Ellis, N.A., Groden, J., Ye, T.Z., Straughen, J., Lennon, D.J., Ciocci, S., Proytcheva, M. and German, J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83 655-666.
20. Kitao, S., Shimamoto, A., Goto, M., Miller, R.W., Smithson, W.A., Lindor, N.M. and Furuichi, Y. (1999) Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet., 22 82-84.
21. Yu, C.E., Oshima, J., Fu, Y.H., Wijsman, E.M., Hisama, F., Alisch, R., Matthews, S., Nakura, J., Miki, T., Ouais, S. et al. (1996) Positional cloning of the Werner's syndrome gene. Science, 272, 258-262.
22. Fukuchi, K., Martin, G.M. and Monnat, R.J., Jr (1989) Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl Acad. Sci. USA 86, 5893-5897.
23. Goto, M., Miller, R.W., Ishikawa, Y. and Sugano, H. (1996) Excess of rare cancers in Werner syndrome (adult progeria). Cancer Epidemiol. Biomarkers Prev., 5, 239-246.
24. German, J. (1993) Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore), 72, 393-406.
25. Vennos, E.M. and James, W.D. (1995) Rothmund-Thomson syndrome. Dermatol. Clin., 13, 143-150.
26. Wang, L.L., Levy, M.L., Lewis, R.A., Chintagumpala, M.M., Lev, D., Rogers, M. and Pion, S.E. (2001) Clinical manifestations in a cohort of 41 Rothmund-Thomson syndrome patients. Am. J. Med. Genet. 102, 11-17.
27. Kerr, B., Ashcroft, G.S., Scott, D., Horan, M.A., Ferguson, M.W. and Donnai, D. (1996) Rothmund-Thomson syndrome: two case reports show heterogeneous cutaneous abnormalities, an association with genetically programmed ageing changes, and increased chromosomal radiosensitivity. J. Med. Genet., 33, 928-934.
28. Wang, L.L., Gannavarapu, A., Kozinetz, C.A., Levy, M.L., Lewis, R.A., Chintagumpala, M.M., Ruiz-Maldanado, R., Contreras-Ruiz, J., Cunniff, C., Erickson, R.P. et al. (2003) Association between osteosarcoma and deleterious mutations in the RECQL4 gene in Rothmund-Thomson syndrome. J. Natl Cancer Inst., 95, 669-674.
29. Lindor, N.M., Furuichi, Y., Kitao, S., Shimamoto, A., Arndt, C. and Jalal, S. (2000) Rothmund-Thomson syndrome due to RECQ4 helicase mutations: report and clinical and molecular comparisons with Bloom syndrome and Werner syndrome. Am. J. Med. Genet., 90, 223-228.
30. Pujol, L.A., Erickson, R.P., Heidenreich, R.A. and Cunniff, C. (2000) Variable presentation of Rothmund-Thomson syndrome. Am. J. Med. Genet., 95, 204-207.
31. Balraj, P., Concannon, P., Jamal, R., Beghini, A., Hoe, T.S., Khoo, A.S. and Volpi, L. (2002) An unusual mutation in RECQ4 gene leading to Rothmund-Thomson syndrome. Mutat. Res., 508, 99-105.
32. Beghini, A., Castorina, P., Roversi, G., Modiano, P. and Larizza, L. (2003) RNA processing defects of the helicase gene RECQL4 in a compound heterozygous Rothmund-Thomson patient. Am. J. Med. Genet., 120A, 395-399.
33. Durand, F., Castorina, P., Morant, C., Delobel, B., Barouk, E. and Modiano, P. (2002) Rothmund-Thomson syndrome, trisomy 8 mosaicism and RECQ4 gene mutation. Ann. Dermatol. Venereol., 129, 892-895.
34. Miozzo, M., Castorina, P., Riva, P., Dalpra, L., Fuhrman Conti, A.M., Volpi, L., Hoe, T.S., Khoo, A., Wiegant, J., Rosenberg, C. et al. (1998) Chromosomal instability in fibroblasts and mesenchymal tumors from 2 sibs with Rothmund-Thomson syndrome. Int. J. Cancer, 77, 504-510.
35. Ohhata, T., Araki, R., Fukumura, R., Kuroiwa, A., Matsuda, Y., Tatsumi, K. and Abe, M. (2000) Cloning, genomic structure and chromosomal localization of the gene encoding mouse DNA helicase RecQ helicase protein-like 4. Gene, 261, 251-258.
36. Moser, A.R., Pitot, H.C. and Dove, W.F. (1990) A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science, 247, 322-324.
37. Luo, G., Santoro, I.M., McDaniel, L.D., Nishijima, I., Mills, M., Youssoufian, H., Vogel, H., Schultz, R.A. and Bradley, A. (2000) Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet., 26, 424-429.
38. Rudolph, K.L., Millard, M., Bosenberg, M.W. and DePinho, R.A. (2001) Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat. Genet., 28, 155-159.
39. Storchova, Z. and Pellman, D. (2004) From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell Biol. 5, 45-54.
40. Fukasawa, K., Choi, T., Kuriyama, R., Rulong, S. and Vande Woude, G.F. (1996) Abnormal centrosome amplification in the absence of p53. Science, 271, 1744-1747.
41. Parry, D.M., Mulvihill, J.J., Tsai, S.E., Kaiser-Kupfer, M.I. and Cowan, J.M. (1986) SC phocomelia syndrome, premature centromere separation, and congenital cranial nerve paralysis in two sisters, one with malignant melanoma. Am. J. Med. Genet., 24, 653-672.
42. Chamla, Y., Roumy, M., Lassegues, M. and Battin, J. (1980) Altered sensitivity to cholchicine and PHA in human cultured cells. Hum. Genet., 53, 249-253.
43. Ichikawa, K., Noda, T. and Furuichi, Y. (2002) Preparation of the gene targeted knockout mice for human premature aging diseases, Werner syndrome, and Rothmund-Thomson syndrome caused by the mutation of DNA helicases. Nippon Yakurigaku Zasshi, 119, 219-226.
44. Hoki, Y., Araki, R., Fujimori, A., Ohhata, T., Koseki, H., Fukumura, R., Nakamura, M., Takahashi, H., Noda, Y., Kito, S. et al. (2003) Growth retardation and skin abnormalities of the Recql4-deficient mouse. Hum. Mol. Genet., 12, 2293-2299.
45. Siitonen, H.A., Kopra, O., Kaariainen, H., Haravuori, H., Winter, R.M., Saamanen, A.M., Peltonen, L. and Kestila, M. (2003) Molecular defect of the Rapadilino syndrome expands the phenotype spectrum of Recql diseases. Hum. Mol. Genet., 21, 2837-2844.
46. Nomura, M., Suzuki, M., Suzuki, Y., Ikeda, H., Tamura, J., Koike, M., Jie, T. and Itoh, G. (1996) Cyclophosphamide-induced apoptosis induces phocomelia in the mouse. Arch. Toxicol., 70, 672-677.
47. Liang, L., Shao, C., Deng, L., Mendonca, M.S., Stambrook, P.J. and Tischfield, J.A. (2002) Radiation-induced genetic instability in vivo depends on p53 status. Mutat. Res., 502, 69-80.
48. Hiddemann, W., Roessner, A., Wormann, B., Mellin, W., Klockenkemper, B., Bosing, T., Buchner, T. and Grundmann, E. (1987) Tumor heterogeneity in osteosarcoma as identified by flow cytometry. Cancer 59, 324-328.
49. Bauer, H.C., Kreicbergs, A., Silfversward, C. and Tribukait, B. (1988) DNA analysis in the differential diagnosis of osteosarcoma. Cancer, 61, 2532-2540.
50. Hollander, M.C., Sheikh, M.S., Bulavin, D.V., Lundgren, K., Augeri-Henmueller, L., Shehee, R., Molinaro, T.A., Kim, K.E., Tolosa, E., Ashwell, J.D. et al. (1999) Genomic instability in Gadd45a-deficient mice. Nat. Genet., 23, 176-184.
51. Celeste, A., Difilippantonio, S., Difilippantonio, M.J., Fernandez-Capetillo, O., Pilch, D.R., Sedelnikova, O.A., Eckhaus, M., Ried, T., Bonner, W.M. and Nussenzweig, A. (2003) H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell, 114 371-383.
52. Lengauer, C., Kinzler, K.W. and Vogelstein, B. (1997) Genetic instability in colorectal cancers. Nature, 386, 623-627.
53. Plaja, A., Mediano, C., Cano, L., Vendrell, T., Sarret, E., Farran, I. and Sanchez, M.A. (2003) Prenatal diagnosis of a rare chromosomal instability syndrome: variegated aneuploidy related to premature centromere division (PCD). Am. J. Med. Genet., 117A 85-86.
54. Kajii, T., Kawai, T., Takumi, T., Misu, H., Mabuchi, O., Takahashi, Y., Tachino, M., Nihei, F. and Ikeuchi, T. (1998) Mosaic variegated aneuploidy with multiple congenital abnormalities: homozygosity for total premature chromatid separation trait. Am. J. Med. Genet., 78, 245-249.
55. Wu, L. and Hickson, I.D. (2002) RecQ helicases and cellular responses to DNA damage. Mutat. Res., 509, 35-47.
56. Warren, C.D., Eckley, D.M., Lee, M.S., Hanna, J.S., Hughes, A., Peyser, B., Jie, C., Irizarry, R. and Spencer, F.A. (2004) S-phase checkpoint genes safeguard high-fidelity sister chromatid cohesion. Mol. Biol. Cell., 15, 1724-1735.
57. Kawabe, T., Tsuyama, N., Kitao, S., Nishikawa, K., Shimamoto, A., Shiratori, M., Matsumoto, T., Anno, K., Sato, T., Mitsui, Y. et al. (2000) Differential regulation of human RecQ family helicases in cell transformation and cell cycle. Oncogene, 19, 4764-4772.
58. Uhlmann, F. and Nasmyth, K. (1998) Cohesion between sister chromatids must be established during DNA replication. Curr. Biol., 8, 1095-1101.
59. Yin, J., Tae Kwon, Y., Varshavsky, A. and Wang, W. (2004) RECQL4, mutated in the Rothmund-Thomson and RAPADILINO syndromes, interacts with ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Hum. Mol. Genet., 13, 2421-2430.
60. Bachmair, A., Finley, D. and Varshavsky, A. (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science, 234, 179-186.
61. Rao, H., Uhlmann, F., Nasmyth, K. and Varshavsky, A. (2001) Degradation of a cohesin subunit by the N-end rule pathway is essential for chromosome stability. Nature, 410, 955-959.
62. Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. and Matzuk, M.M. (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 383, 531-535.
63. Ramirez-Solis, R., Davis, A.C. and Bradley, A. (1993) Gene targeting in embryonic stem cells. Methods Enzymol., 225, 855-878.
64. Hogan, B., Beddington, R., Costantini, F. and Lacey, E. (1994) Manipulating the Mouse Embryo: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
65. Van Stedum, S. and King, W. (2002) Basic FISH techniques and troubleshooting. Methods Mol. Biol., 204, 51-63.