Chromothripsis: How does such a catastrophic event impact human reproduction?

Human Reproduction

Volumn 29, Issue 3, 2014, Pages 388-393

  Pellestor, Franck ^a,b  

^a HÔPITAL ARNAUD DE VILLENEUVE   (France)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

chromosomal rearrangement; chromothripsis; embryo; fertilization; genomic instability

Indexed keywords

PROTEIN P53;

APOPTOSIS; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CHROMOSOME REARRANGEMENT; CHROMOSOME STRUCTURE; CHROMOTHRIPSIS; DNA DAMAGE; DNA REPAIR; EMBRYO DEVELOPMENT; FERTILIZATION; GENETIC VARIABILITY; GERMLINE MICRONUCLEUS; HUMAN; MICRONUCLEUS; MITOSIS; NEOPLASM; NONHUMAN; PREIMPLANTATION EMBRYO; REPRODUCTION; REVIEW; TELOMERE; ZYGOTE;

CHROMOSOMAL REARRANGEMENT; CHROMOTHRIPSIS; EMBRYO; FERTILIZATION; GENOMIC INSTABILITY;

CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATIONS; CHROMOSOME DISORDERS; DNA REPAIR; DNA REPLICATION; GENOME, HUMAN; HUMANS; REPRODUCTION;

EID: 84894271576     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu003     Document Type: Review

References (51)

1. Ahmed EA, de Boer P, Philippens ME, Kal HB, de Rooij DG. Parp1-XRCC1 and the repair of DNA double strand breaks in mouse round spermatids. Mutat Res 2010;683:84-90.
2. Berg IL, Neuman R, Lam KWG, Sarbajna S, Odenthal-Hess L, May CA, Jeffreys A. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet 2010;42:859-863.
3. Bickmore WA, van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013;152:1270-1284.
4. Chavez SL, Loewke KE, Han J, Moussavi F, Colls P, Munne S, Behr B, Reijo Pera RA. Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage. Nat Commun 2012;3:1251.
5. Chiang C, Jacobsen JC, Ernst C, Hanscom C, Heilbut A, Blumenthal I, Mills RE, Kirby A, Lindgren AM, Rudiger SR et al. Complex reorganization and predominant non-homologous repair following chromosomal breakage in karyotypically balanced germline rearrangements and transgenic integration. Nat Genet 2012;44:390-998.
6. Corbo RM, Gambina G, Scacchi R. How contemporary human reproductive behaviors influence the role of fertility-related genes: the example of the P53 gene. Plos One 2012;7:e35431.
7. Crasta K, Ganem NJ, Dagher R, Lanterman AB, Ivanova EV, Pan Y, Nezi L, Protopopov A, Chowdhury D, Pellman D. DNA breaks and chromosome pulverization from errors in mitosis. Nature 2012; 482:53-58.
8. Delhanty JDA, Pellestor F (eds) Aneuploidy. Cytogenet Genome Res 2011, 133, 85-294.
9. Dion V, Gasser SM. Chromatin movement in the maintenance of genome stability. Cell 2013;152:1355-1364.
10. Escudero T, Estop A, Fisher J, Munné S. Preimplantation genetic diagnosis for complex chromosome rearrangements. Am J Med Genet A 2008; 146:1662-1669.
11. Fragouli E,Wells D, Delhanty JDA.Chromosomeabnormalities in the human oocyte. Cytogenet Genome Res 2011;133:107-118.
12. Fragouli E, Alfarawati S, Spath K, Jaroudi S, Sarada J, Enciso M,Wells D. The origin and impact of embryonic aneuploidy. Hum Genet 2013; 132:1001-1013.
13. Gardner RJM, Sutherland GR, Shaffer LG. Chromosome Abnormalities and Genetic Counseling, 4th edn. New York, USA: Oxford University Press, 2012.
14. Gudjonsson T, Altmeyer M, Savic V, Toledo L, Dinant C, Grofte M, Bartkova J, Poulsen M, Oka Y, Bekker-Jensen S et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chomosomes. Cell 2012;150:697-709.
15. Harrison RH, Kuo HC, Scriven PN, Handyside AH, Ogilvie CM. Lack of cell cycle checkpoints in human cleavage stage embryos revealed by a clonal pattern of chromosomal mosaicism analysed by sequential multicolour FISH. Zygote 2000;8:217-224.
16. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001;2:280-291.
17. HuW, Zheng T,Wang J. Regulation of fertility by the p53 family members. Genes Cancer 2011;2:420-430.
18. Jones MJK, Jallepalli PV. Chromothripsis: chromosomes in crisis. Dev Cell 2012;23:908-917.
19. Kloosterman WP, Cuppen E. Chromothripsis in congenital disorders and cancer: similarities and differences. Curr Opin Cell Biol 2013;25: 341-348.
20. Kloosterman WP, Gurvey V, van Roosmalen M, Duran KJ, de Bruijn E, Bakker SCM, Letteboer T, van Nesselrooij B, Hochstenbach R, Poot M et al. Chromothripsis as a mechanism driving complex de novo structural rearrangements in the germline. Hum Mol Genet 2011;20:1916-1924.
21. Kloosterman WP, Tavakoli-Yaraki M, van Roosmalen M, van Binsbergen E, Renkens I, Duran KJ, Ballarati L, Vergult S, Giardino D, Hansson K et al. Constitutional chromothripsis rearrangements involve clustered double-stranded DNA breaks and nonhomologous repair mechanisms. Cell Rep 2012;1:648-655.
22. Korbel JO, Campbell PJ. Criteria for inference of chromothripsis in cancer genomes. Cell 2013;152:1226-1236.
23. Lebedev I. Mosaic aneuploidy in early fetal losses. Cytogenet Genome Res 2011;133:169-183.
24. Ledbetter DH. Chaos in the embryo. Nat Med 2008;5:490-491.
25. Lim CK, Cho JW, Kim JY, Kang IS, Shim SH, Jun JH. A healthy live birth after successful preimplantation genetic diagnosis for carriers of complex chromosomes rearrangements. Fertil Steril 2008;90:1680-1684.
26. Liu P, Erez A, Sreenath Nagamani SC, Dhar SU, Kolodziejska KE, Dharmadhikari AV, Lance Cooper M,Wiszniewska J, Zhang F,Withers MA et al. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 2011a;146:889-903.
27. Liu P, Lacaria M, Zhang F, Withers M, Hastings PJ, Lupski JR. Frequency of nonallelic homologous recombination is correlated with length of homology: evidence that ectopic synapsis precedes ectopic crossing-over. Am J Hum Genet 2011b;89:580-588.
28. Liu P, Carvalho CMB, Hastings PJ, Lupski JR. Mechanisms for recurrent and complex human genomic rearrangements. Curr Opin Genet Dev 2012; 22:211-220.
29. Loup V, Bernicot I, Janssens P, Hédon B, Hamamah S, Pellestor F, Anahory T. Combined FISH and PRINS sperm analysis of complex chromosomes rearrangement t(1;19;13): an approach facilitating PGD. Mol Hum Reprod 2010;16:111-116.
30. MaherCA,Wilson RK. Chromothripsis and human disease: piecing together the shattering process. Cell 2012;148:29-32.
31. Mantzouratou A, Delhanty JDA. Aneuploidy in the human cleavage stage embryo. Cytogenet Genome Res 2011;133:141-148.
32. Martin RH (ed). Cytogenetics of human germ cells. Cytogenet Genome Res 2005;111:187-402.
33. Mertzanidou A, Wilton L, Cheng J, Spits C, Vanneste E, Moreau Y, Vermeesch JR, Sermon K. Microarray analysis reveals abnormal chromosomal complements in over 70% of 14 normally developing human embryos. Hum Reprod 2013;28:256-264.
34. Odorisio T, Rodriguez TA, Evans EP, Clarke AR, Burgoyne PS. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet 1998;18:257-261.
35. Oliva R. Protamines and male infertility. Hum Reprod Update 2006; 12:417-435.
36. Pellestor F, Anahory T, Hamamah S. The chromosomal analysis of human oocytes. An overview of established procedures. Hum Reprod Update 2005;11:15-32.
37. Pellestor F, Anahory T, Lefort G, Puechberty J, Liehr T, Hédon B, Sarda P. Complex chromosomal rearrangements: origin and meiotic behavior. Hum Reprod Update 2011a;17:476-494.
38. Pellestor F, Puechberty J,WeiseA, LefortG,Anahory T, Liehr T, Sarda P. Meiotic segregation of complex reciprocal translocations: direct analysis of the spermatozoa of a t(5;13;14) carrier. Fertil Steril 2011b; 95:17-22.
39. Rausch T, Jones DTW, Zapatka M, Stütz AM, Zichner T, Weischenfeldt J, Jäger N, Remke M, Shih D, Northcott PA et al. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations. Cell 2012;148:59-71.
40. Sakkas D, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 2010; 93:1027-1036.
41. Scriven PN, Bint SM, Davies AF, Ogilvie CM. Meiotic outcomes of three-way translocations ascertained in cleavage-stage embryos: refinement of reproductive risks and implications for PGD. Eur J Hum Genet. doi:10.1038/ejhg.2013.237.
42. Sorzano COS, Pascual-Montano A, Sanchez de Diego A, Martinez CA, van Wely KHM. Chromothripsis: breakage-fusion-bridge over and over again. Cell Cycle 2013;12:2016-2023.
43. Stephens PJ, Greenman CD, Fu B,Yang F, Bignell GR, Mudie LJ, Pleasance ED, Wai Lau K, Beare D, Stebbings LA et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 2011;144:27-40.
44. Steuerwald N. Meiotic spindle checkpoints for assessment of aneuploid oocytes. Cytogenet Genome Res 2005;111:256-259.
45. Stevens JB, Abdallah BY, Regan SM, Liu G, Bremer SW, Ye CJ, Heng HH. Comparison of mitotic cell death by chromosome fragmentation to premature chromosome condensation. Mol Cytogenet 2010;3:20-30.
46. Suh AK, Yang A, Kettenbach A, Bamberger C, Michaelis AH, Zhu Z, Elvin JA, Bronson RT, Crum CP, McKeon F. p63 protects the female germ line during meiotic arrest. Nature 2006;444:624-628.
47. Tubio JMC, Estivill X. When catastrophe strikes a cell. Nature 2011; 470:476-477.
48. Vanneste E,VoetT, LeCaigecC,Debrock S, SermonK, StaessenC, Liebaers I, Fryns JP, D'HoogheT,Vermeesch JR.Chromosome instability is common in human cleavage-stage embryos. Nat Med 2009;15:577-583.
49. Voet T, Vanneste E, Vermeesch JR. The human cleavage sage embryo is a cradle of chromosomal rearrangements. Cytogenet Genome Res 2011; 133:160-168.
50. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-310.
51. Wyatt AW, Collins CC. In brief: chromothripsis and cancer. J Pathol 2013; 231:1-3.