The complex nature of fragile site plasticity and its importance in cancer

Current Opinion in Cell Biology

Volumn 40, Issue , 2016, Pages 131-136

  Sarni, Dan ^a   Kerem, Batsheva ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGENESIS; CELL CYCLE S PHASE; CHROMOSOMAL INSTABILITY; CHROMOSOME FRAGILE SITE; CHROMOSOME REPLICATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; ONCOGENE; PLASTICITY; PRIORITY JOURNAL; REVIEW; STRESS; TUMOR GENE; ANIMAL; DNA REPLICATION; GENETICS; GENOMIC INSTABILITY; NEOPLASM; PATHOLOGY;

ANIMALS; CHROMOSOME FRAGILE SITES; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS; NEOPLASMS; ONCOGENES;

EID: 84962385724     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2016.03.017     Document Type: Review

References (60)

1. Glover T.W., Berger C., Coyle J., Echo B. DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 1984, 67:136-142.
2. Murano I., Kuwano A., kajii t. Fibroblast-specific common fragile sitesinduced by aphidicolin. Hum Genet 1989, 83:45-48.
3. Le Tallec B., Millot G.A., Blin M.E., Brison O., Dutrillaux B., Debatisse M. Common fragile site profiling in epithelial and erythroid cells reveals that most recurrent cancer deletions lie in fragile sites hosting large genes. Cell Rep 2013, 4:420-428.
4. Le Tallec B., Dutrillaux B., Lachages A.-M., Millot G.A., Brison O., Debatisse M. Molecular profiling of common fragile sites in human fibroblasts. Nat Struct Mol Biol 2011, 18:1421-1423.
5. Hosseini S.A., Horton S., Saldivar J.C., Miuma S., Stampfer M.R., Heerema N.A., Huebner K. Common chromosome fragile sites in human and murine epithelial cells and FHIT/FRA3B loss-induced global genome instability. Genes Chromosomes Cancer 2013, 52:1017-1029.
6. Durkin S.G., Glover T.W. Chromosome fragile sites. Annu Rev Genet 2007, 41:169-192.
7. Glover T.W., Hoge A.W., Miller D.E., Ascara-Wilke J.E., Adam A.N., Dagenais S.L., Wilke C.M., Dierick H.A., Beer D.G. The murine Fhit gene is highly similar to its human orthologue and maps to a common fragile site region. Cancer Res 1998, 58:3409-3414.
8. Shiraishi T., Druck T., Mimori K., Flomenberg J., Berk L., Alder H., Miller W., Huebner K., Croce C.M. Sequence conservation at human and mouse orthologous common fragile regions, FRA3B/FHIT and Fra14A2/Fhit. Proc Natl Acad Sci U S A 2001, 98:5722-5727.
9. Krummel K.A., Denison S.R., Calhoun E., Phillips L.A., Smith D.I. The common fragile site FRA16D and its associated gene WWOX are highly conserved in the mouse at Fra8E1. Genes Chromosom Cancer 2002, 34:154-167.
10. Rozier L., El-Achkar E., Apiou F., Debatisse M. Characterization of a conserved aphidicolin-sensitive common fragile site at human 4q22 and mouse 6C1: possible association with an inherited disease and cancer. Oncogene 2004, 23:6872-6880.
11. Ruiz-Herrera A., Garcia F., Fronicke L., Ponsa M., Egozcue J., Caldes M.G., Stanyon R. Conservation of aphidicolin-induced fragile sites in Papionini (Primates) species and humans. Chromosom Res 2004, 12:683-690.
12. Lemoine F.J., Degtyareva N.P., Lobachev K., Petes T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 2005, 120:587-598.
13. Admire A., Shanks L., Danzl N., Wang M., Weier U., Stevens W., Hunt E., Weinert T. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev 2006, 20:159-173.
14. Song W., Dominska M., Greenwell P.W., Petes T.D. Genome-wide high-resolution mapping of chromosome fragile sites in Saccharomyces cerevisiae. Proc Natl Acad Sci 2014, 111:E2210-E2218.
15. Gorgoulis V.G., Vassiliou L-VF, Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio R.A., Kastrinakis N.G., Levy B., et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434:907-913.
16. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
17. Tsantoulis P.K., Kotsinas A., Sfikakis P.P., Evangelou K., Sideridou M., Levy B., Mo L., Kittas C., Wu X.-R., Papavassiliou A.G., et al. Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene 2008, 27:3256-3264.
18. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.-V.F.V., Kolettas E., Niforou K., Zoumpourlis V.C., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444:633-637.
19. Di Micco R., Fumagalli M., Cicalese A., Piccinin S., Gasparini P., Luise C., Schurra C., Garre M., Nuciforo P.G., Bensimon A., et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006, 444:638-642.
20. Bester A.C., Roniger M., Oren Y.S., Im M.M., Sarni D., Chaoat M., Bensimon A., Zamir G., Shewach D.S., Kerem B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011, 145:435-446.
21. Arlt M.F., Durkin S.G., Ragland R.L., Glover T.W. Common fragile sites as targets for chromosome rearrangements. DNA Repair (Amst) 2006, 5:1126-1135.
22. Thorland E.C., Myers S.L., Gostout B.S., Smith D.I. Common fragile sites are preferential targets for HPV16 integrations in cervical tumors. Oncogene 2003, 22:1225-1237.
23. Thorland E.C., Myers S.L., Persing D.H., Sarkar G., McGovern R.M., Gostout B.S., Smith D.I. Human papillomavirus type 16 integrations in cervical tumors frequently occur in common fragile sites. Cancer Res 2000, 60:5916-5921.
24. Yu T., Ferber M.J., Cheung T.H., Chung T.K.H., Wong Y.F., Smith D.I. The role of viral integration in the development of cervical cancer. Cancer Genet Cytogenet 2005, 158:27-34.
25. Matovina M., Sabol I., Grubisić G., Gasperov N.M., Grce M. Identification of human papillomavirus type 16 integration sites in high-grade precancerous cervical lesions. Gynecol Oncol 2009, 113:120-127.
26. Bignell G.R., Greenman C.D., Davies H., Butler A.P., Edkins S., Andrews J.M., Buck G., Chen L., Beare D., Latimer C., et al. Signatures of mutation and selection in the cancer genome. Nature 2010, 463:893-898.
27. Hellman A., Zlotorynski E., Scherer S.W., Cheung J., Vincent J.B., Smith D.I., Trakhtenbrot L., Kerem B. A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 2002, 1:89-97.
28. Kotzot D., Martinez M.J., Bagci G., Basaran S., Baumer A., Binkert F., Brecevic L., Castellan C., Chrzanowska K., Dutly F., et al. Parental origin and mechanisms of formation of cytogenetically recognisable de novo direct and inverted duplications. J Med Genet 2000, 37:281-286.
29. Miller C.T., Lin L., Casper A.M., Lim J., Thomas D.G., Orringer M.B., Chang A.C., Chambers A.F., Giordano T.J., Glover T.W., et al. Genomic amplification of MET with boundaries within fragile site FRA7G and upregulation of MET pathways in esophageal adenocarcinoma. Oncogene 2006, 25:409-418.
30. Le Beau M.M., Rassool F.V., Neilly M.E., Espinosa R., Glover T.W., Smith D.I., McKeithan T.W. Replication of a common fragile site, FRA3B, occurs late in S phase and is delayed further upon induction: implications for the mechanism of fragile site induction. Hum Mol Genet 1998, 7:755-761.
31. Palakodeti A., Han Y., Jiang Y., Le Beau M.M. The role of late/slow replication of the FRA16D in common fragile site induction. Genes Chromosom Cancer 2004, 39:71-76.
32. Wang L., Darling J., Zhang J.S., Qian C.P., Hartmann L., Conover C., Jenkins R., Smith D.I. Frequent homozygous deletions in the FRA3B region in tumor cell lines still leave the FHIT exons intact. Oncogene 1998, 16:635-642.
33. Teixeira L.K., Wang X., Li Y., Ekholm-Reed S., Wu X., Wang P., Reed S.I. Cycline deregulation promotes loss of specific genomic regions. Curr Biol 2015, 25:1327-1333.
34. Bhat A., Andersen P.L., Qin Z., Xiao W. Rev3, the catalytic subunit of Pol, is required for maintaining fragile site stability in human cells. Nucleic Acids Res 2013, 41:2328-2339.
35. Minocherhomji S., Ying S., Bjerregaard V.A., Bursomanno S., Aleliunaite A., Wu W., Mankouri H.W., Shen H., Liu Y., Hickson I.D. Replication stress activates DNA repair synthesis in mitosis. Nature 2015, 528:286-290.
36. Letessier A., Millot G.A., Koundrioukoff S., Lachages A.M., Vogt N., Hansen R.S., Malfoy B., Brison O., Debatisse M., Lachagès A.-M. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 2011, 470:120-123.
37. Shah S.N., Opresko P.L., Meng X., Lee M.Y.W.T., Eckert K.a. DNA structure and the Werner protein modulate human DNA polymerase delta-dependent replication dynamics within the common fragile site FRA16D. Nucleic Acids Res 2010, 38:1149-1162.
38. Zlotorynski E., Rahat A., Skaug J., Ben-Porat N., Ozeri E., Hershberg R., Levi A., Scherer S.W., Margalit H., Kerem B. Molecular basis for expression of common and rare fragile sites. Mol Cell Biol 2003, 23:7143-7151.
39. Ozeri-Galai E., Lebofsky R., Rahat A., Bester A.C., Bensimon A., Kerem B. Failure of origin activation in response to fork stalling leads to chromosomal instability at fragile sites. Mol Cell 2011, 43:122-131.
40. Helmrich A., Ballarino M., Tora L. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol Cell 2011, 44:966-977.
41. Jiang Y., Lucas I., Young D.J., Davis E.M., Karrison T., Rest J.S., Le Beau M.M. Common fragile sites are characterized by histone hypoacetylation. Hum Mol Genet 2009, 18:4501-4512.
42. Georgakilas A.G., Tsantoulis P., Kotsinas A., Michalopoulos I., Townsend P., Gorgoulis V.G. Are common fragile sites merely structural domains or highly organized "functional" units susceptible to oncogenic stress?. Cell Mol Life Sci 2014, 71:4519-4544.
43. Ozeri-Galai E., Tur-Sinai M., Bester A.C., Kerem B. Interplay between genetic and epigenetic factors governs common fragile site instability in cancer. Cell Mol Life Sci 2014, 71:4495-4506.
44. McAvoy S., Ganapathiraju S.C., Ducharme-Smith a L., Pritchett J.R., Kosari F., Perez D.S., Zhu Y., James C.D., Smith D.I. Non-random inactivation of large common fragile site genes in different cancers. Cytogenet Genome Res 2007, 118:260-269.
45. Waters C.E., Saldivar J.C., Hosseini S.A., Huebner K. The FHIT gene product: tumor suppressor and genome "caretaker.". Cell Mol Life Sci 2014, 71:4577-4587.
46. Hazan I., Aqeilan R. Current questions and controversies in chromosome fragile site research: does WWOX, the gene product of common fragile site FRA16D, have a passive or active role in cancer?. Cell Death Discov 2015, 1:15040.
47. Zimonjic D.B.B., Druck T., Ohta M., Kastury K., Croce C.M.M., Popescu N.C.C., Huebner K. Positions of chromosome 3p14.2 fragile sites (FRA3B) within the FHIT gene. Cancer Res 1997, 57:1166-1170.
48. Bednarek A.K., Keck-Waggoner C.L., Daniel R.L., Laflin K.J., Bergsagel P.L., Kiguchi K., Brenner A.J., Aldaz C.M. WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. Cancer Res 2001, 61:8068-8073.
49. Gao G., Kasperbauer J.L., Tombers N.M., Wang V., Mayer K., Smith D.I. A selected group of large common fragile site genes have decreased expression in oropharyngeal squamous cell carcinomas. Genes Chromosom Cancer 2014, 53:392-401.
50. Mirkin E.V., Mirkin S.M. Mechanisms of transcription-replication collisions in bacteria. Mol Cell Biol 2005, 25:888-895.
51. Wilson T.E., Arlt M.F., Park S.H., Rajendran S., Paulsen M., Ljungman M., Glover T.W. Large transcription units unify copy number variants and common fragile sites arising under replication stress. Genome Res 2015, 25:189-200.
52. Miron K., Golan-Lev T., Dvir R., Ben-David E., Kerem B. Oncogenes create a unique landscape of fragile sites. Nat Commun 2015, 6:7094.
53. Barlow J.H., Faryabi R.B., Callén E., Wong N., Malhowski A., Chen H.T., Gutierrez-Cruz G., Sun H.-W., McKinnon P., Wright G., et al. Identification of early replicating fragile sites that contribute to genome instability. Cell 2013, 152:620-632.
54. Koundrioukoff S., Carignon S., Técher H., Letessier A., Brison O., Debatisse M. Stepwise activation of the ATR signaling pathway upon increasing replication stress impacts fragile site integrity. PLoS Genet 2013, 9:e1003643.
55. Naim V., Wilhelm T., Debatisse M., Rosselli F. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat Cell Biol 2013, 15:1008-1015.
56. Ying S., Minocherhomji S., Chan K.L., Palmai-Pallag T., Chu W.K., Wass T., Mankouri H.W., Liu Y., Hickson I.D. MUS81 promotes common fragile site expression. Nat Cell Biol 2013, 15:1001-1007.
57. Schwartz M., Zlotorynski E., Goldberg M., Ozeri E., Rahat A., le Sage C., Chen B.P.C., Chen D.J., Agami R., Kerem B. Homologous recombination and nonhomologous end-joining repair pathways regulate fragile site stability. Genes Dev 2005, 19:2715-2726.
58. Bergoglio V., Boyer A.-S., Walsh E., Naim V., Legube G., Lee M.Y.W.T., Rey L., Rosselli F., Cazaux C., Eckert K.A., et al. DNA synthesis by Pol promotes fragile site stability by preventing under-replicated DNA in mitosis. J Cell Biol 2013, 201:395-408.
59. Lukas C., Savic V., Bekker-Jensen S., Doil C., Neumann B., Sølvhøj Pedersen R., Grøfte M., Chan K.L., Hickson I.D., Bartek J., et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 2011, 13:243-253.
60. Hoffman E.A., McCulley A., Haarer B., Arnak R., Feng W. Break-seq reveals hydroxyurea-induced chromosome fragility as a result of unscheduled conflict between DNA replication and transcription. Genome Res 2015, 25:402-412.