Male-driven de novo mutations in haploid germ cells

Molecular Human Reproduction

Volumn 19, Issue 8, 2013, Pages 495-499

  Gregoire, Marie Chantal ^a   Massonneau, Julien ^a   Simard, Olivier ^a   Gouraud, Anne ^a   Brazeau, Marc Andre ^a   Arguin, Melina ^a   Leduc, Frederic ^a   Boissonneault, Guylain ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

DNA damage; DNA replication repair; Gene mutations; Polymorphism; Spermiogenesis

Indexed keywords

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC VARIABILITY; GERM CELL; HAPLOIDY; HERITABILITY; HUMAN; MEIOSIS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; SEX LINKAGE; SPERMATID; SPERMATOGENESIS; SPERMATOZOON;

DNA DAMAGE; DNA REPLICATION/REPAIR; GENE MUTATIONS; POLYMORPHISM; SPERMIOGENESIS;

DNA DAMAGE; DNA REPAIR; GENETIC VARIATION; GERM CELLS; HAPLOIDY; HUMANS; MALE; MUTATION; POLYMORPHISM, GENETIC; SPERMATOGENESIS; SPERMATOZOA;

EID: 84880724048     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat022     Document Type: Article

References (46)

1. Arnheim N, Calabrese P. Understanding what determines the frequency and pattern of human germline mutations. Nat Rev Genet 2009; 10:478-488.
2. Awe S, Renkawitz-Pohl R. Histone H4 acetylation is essential to proceed from a histone- to a protamine-based chromatin structure in spermatid nuclei of Drosophila melanogaster. Syst Biol Reprod Med 2010;56:44-61.
3. Barratt CLR, Aitken RJ, Björndahl L, Carrell DT, de Boer P, Kvist U, Lewis SEM, Perreault SD, Perry MJ, Ramos L et al. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications-a position report, 2010, 824-838.
4. Boissonneault G. Chromatin remodeling during spermiogenesis: a possible role for the transition proteins in DNA strand break repair. FEBS Lett 2002;514:111-114.
5. Cabrero J, Palomino-Morales RJ, Camacho JPM. The DNA-repair Ku70 protein is located in the nucleus and tail of elongating spermatids in grasshoppers. Chromosome Res 2007;15:1093-1100.
6. Collins AR. The comet assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 2004;26:249-261.
7. Duret L, Galtier N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 2009; 10:285-311.
8. Ellegren H. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc Biol Sci 2007;274:1-10.
9. Glaser RL, Jabs EW. Dear old dad. Sci Aging Knowledge Environ 2004;2004: re1.
10. Govin J, Lestrat C, Caron C, Pivot-Pajot C, Rousseaux S, Khochbin S. Histone acetylation-mediated chromatin compaction during mouse spermatogenesis. Ernst Schering Res Found Workshop 2006:57:155-172.
11. Govin J, Escoffier E, Rousseaux S, Kuhn L, Ferro M, Thévenon J, Catena R, Davidson I, Garin J, Khochbin S et al. Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. J Cell Biol 2007;176:283-294.
12. Grégoire MC, Leduc F, Boissonneault G. Spermiogenesis in sperm genetic integrity. In: Zini A, Agarwal A (eds). Sperm chromatin: biological and clinical applications in male infertility and assisted reproduction. New York, NY: Springer, 2011, 307-320.
13. Haldane JBS. The mutation rate of the gene for haemophilia, and its segregation ratios in males and females. Ann Eugen 1947;13:262-271.
14. Hill KA, Nishino H, Buettner VL, Halangoda A, Li W, Sommer SS. The Big Blue(R) transgenic mouse mutation detection assay: the mutation pattern of sectored mutant plaques. Mutat Res 1999;425:47-54.
15. Hurst LD, Ellegren H. Sex biases in the mutation rate. Trends Genet 1998; 14:446-452.
16. Iliakis G. Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother Oncol 2009;92:310-315.
17. Inagaki H, Ohye T, Kogo H, Kato T, Bolor H, Taniguchi M, Shaikh TH, Emanuel BS, Kurahashi H. Chromosomal instability mediated by non-B DNA: cruciform conformation and not DNA sequence is responsible for recurrent translocation in humans. Genome Res 2009; 19:191-198.
18. Johnson RE, Washington MT, Prakash S, Prakash L. Fidelity of human DNA polymerase eta. J Biol Chem 2000;275:7447-7450.
19. Johnson GD, Lalancette C, Linnemann AK, Leduc F, Boissonneault G, Krawetz SA. The sperm nucleus: chromatin, RNA, and the nuclear matrix. Reproduction 2011;141:21-36.
20. Kato T, Yamada K, Inagaki H, Kogo H, Ohye T, Emanuel BS, Kurahashi H. Age has no effect on de novo constitutional t(11;22) translocation frequency in sperm. Fertil Steril 2007;88:1446-1448.
21. Kha DT, Wang G, Natrajan N, Harrison L, Vasquez KM. Pathways for double-strand break repair in genetically unstable Z-DNA-forming sequences. J Mol Biol 2010;398:471-480.
22. Kohler SW, Provost GS, Fieck A, Kretz PL, Bullock WO, Sorge JA, Putman DL, Short JM. Spectra of spontaneous and mutagen-induced mutations in the lacI gene in transgenic mice. Proc Natl Acad Sci USA 1991;88:7958-7962.
23. Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, Gudjonsson SA, Sigurdsson A, Jonasdottir A, Jonasdottir A et al. Rate of de novo mutations and the importance of 's age to disease risk. Nature 2012;488:471-475.
24. Laberge RM, Boissonneault G. On the nature and origin of DNA strand breaks in elongating spermatids. Biol Reprod 2005;73:289-296.
25. Leduc F, Maquennehan V, Nkoma GB, Boissonneault G. DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol Reprod 2008;78:324-332.
26. Leduc F, Acteau G, Grégoire MC, Simard O, Leroux J, Carrier-Leclerc A, Arguin M, Boissonneault G. Post-meiotic DNA damage and response in male germ cells. In: Kruman I (ed.). DNA repair. New York: InTech North America, 2011a.
27. Leduc F, Faucher D, Bikond Nkoma G, Grégoire M-C, Arguin M, Wellinger RJ, Boissonneault G. Genome-wide mapping of DNA strand breaks. PLoS ONE 2011b;6:e17353.
28. Lieber MR. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 2010; 79:181-211.
29. Makova KD, Yang S, Chiaromonte F. Insertions and deletions are male biased too: a whole-genome analysis in rodents. Genome Res 2004; 14:567-573.
30. Marchetti F, Wyrobek AJ. DNA repair decline during mouse spermiogenesis results in the accumulation of heritable DNA damage. DNA Repair (Amst) 2008;7:572-581.
31. Marcon L, Boissonneault G. Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod 2004;70:910-918.
32. McPherson SM, Longo FJ. Nicking of rat spermatid and spermatozoa DNA: possible involvement of DNA topoisomerase II. Dev Biol 1993; 158:122-130.
33. Meyer-Ficca ML, Scherthan H, Burkle A, Meyer RG. Poly(ADP- ribosyl)ation during chromatin remodeling steps in rat spermiogenesis. Chromosoma 2005; 114:67-74.
34. Muratori M, Marchiani S, Maggi M, Forti G, Baldi E. Origin and biological significance of DNA fragmentation in human spermatozoa. Front Biosci 2006; 11:1491-1499.
35. Ohye T, Inagaki H, Kogo H, Tsutsumi M, Kato T, Tong M, Macville MVE, Medne L, Zackai EH, Emanuel BS et al. Paternal origin of the de novo constitutional t(11;22)(q23;q11). EurJ Hum Genet 2010;18:783-787.
36. Olsen A-K, Lindeman B, Wiger R, Duale N, Brunborg G How do male germ cells handle DNA damage? Toxicol Appl Pharmacol 2005;207:521-531.
37. Popa A, Samollow P, Gautier C, Mouchiroud D. The sex-specific impact of meiotic recombination on nucleotide composition. Genome Biol Evol 2012;4:412-422.
38. Rathke C, Baarends WM, Jayaramaiah-Raja S, Bartkuhn M, Renkawitz R, Renkawitz-Pohl R. Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila. J Cell Sci 2007;120:1689-1700.
39. Sakkas D, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 2010; 93:1027-1036.
40. Sayres MAW, Makova KD. Genome analyses substantiate male mutation bias in many species. Bioessays 2011;33:938-945.
41. Taylor J, Tyekucheva S, Zody M, Chiaromonte F, Makova KD. Strong and weak male mutation bias at different sites in the primate genomes: insights from the human-chimpanzee comparison. Mol Biol Evol 2006; 23:565-573.
42. Velando A, Torres R, Alonso-Alvarez C. Avoiding bad genes: oxidatively damaged DNA in germ line and mate choice. Bioessays 2008; 30:1212-1219.
43. Vogel F, Motulsky AG. Human genetics: problems and approaches. Berlin, Germany: Springer, 2010.
44. Wang G, Carbajal S, Vijg J, DiGiovanni J, Vasquez KM. DNA structure-induced genomic instability in vivo. J Natl Cancer Inst 2008; 100:1815-1817.
45. Ward WS. Regulating DNA supercoiling: sperm points the way. Biol Reprod 2011;84:841-843.
46. Wojtczak A, Poplońska K, Kwiatkowska M. Phosphorylation of H2AX histone as indirect evidence for double-stranded DNA breaks related to the exchange of nuclear proteins and chromatin remodeling in Chara vulgaris spermiogenesis. Protoplasma 2008;233:263-267.