Differential gene susceptibility to sperm DNA damage: Analysis of developmental key genes in trout

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  González Rojo, Silvia ^a   Fernández Díez, Cristina ^a   Guerra, Susana M ^a   Robles, Vanesa ^a   Herraez, Maria Paz ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANOSINE; GUANOSINE DERIVATIVE; HISTONE; PROTAMINE; RIBOSOME DNA; UNCLASSIFIED DRUG; CHROMATIN; HYDROGEN PEROXIDE; NUCLEAR PROTEIN; NUCLEOSOME;

ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CRYOPRESERVATION; DNA DAMAGE; DNA SEQUENCE; FEMALE; GENE LOCATION; GENETIC ANALYSIS; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTOXICITY; IMMUNOCYTOCHEMISTRY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROMOTER REGION; RAINBOW TROUT; SENSITIVITY ANALYSIS; SPERM; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CHROMATIN; DRUG EFFECTS; GENETICS; NUCLEOSOME; RADIATION RESPONSE; SALMONINE; SPERMATOZOON; ULTRAVIOLET RADIATION;

MAMMALIA; ONCORHYNCHUS MYKISS; SALMONIDAE;

ANIMALS; CHROMATIN; DNA DAMAGE; DNA, RIBOSOMAL; HISTONES; HYDROGEN PEROXIDE; MALE; NUCLEAR PROTEINS; NUCLEOSOMES; SPERMATOZOA; TROUT; ULTRAVIOLET RAYS;

EID: 84918572100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114161     Document Type: Article

References (48)

1. Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, et al. (1999) Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 14: 1039-1049.
2. Speyer BE, Pizzey AR, Ranieri M, Joshi R, Delhanty JD, et al. (2010) Fall in implantation rates following ICSI with sperm with high DNA fragmentation. Hum Reprod 25: 1609-1618. 10.1093/humrep/deq116; 10.1093/humrep/deq116
3. Miller D, Brinkworth M, Iles D (2010) Paternal DNA packaging in spermatozoa: More than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139: 287-301. 10.1530/REP-09-0281; 10.1530/REP-09-0281
4. Ward WS (2010) Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 16: 30-36. 10.1093/molehr/gap080; 10.1093/molehr/gap080
5. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, et al. (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460: 473-478. 10.1038/nature08162; 10.1038/nature08162
6. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, et al. (2010) Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 17: 679-687. 10.1038/nsmb.1821 [doi].
7. Wu SF, Zhang H, Cairns BR (2011) Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res 21: 578-589. 10.1101/gr.113167.110; 10.1101/gr.113167.110
8. Shiao YH, Leighty RM, Wang C, Ge X, Crawford EB, et al. (2011) Ontogeny-driven rDNA rearrangement, methylation, and transcription, and paternal influence. PLoS One 6: e22266. 10.1371/journal.pone.0022266 [doi].
9. Noblanc A, Damon-Soubeyrand C, Karrich B, Henry-Berger J, Cadet R, et al. (2013) DNA oxidative damage in mammalian spermatozoa: Where and why is the male nucleus affected? Free Radic Biol Med 65: 719-723. 10.1016/j.freeradbiomed.2013.07.044 [doi].
10. Rothfuss O, Gasser T, Patenge N (2010) Analysis of differential DNA damage in the mitochondrial genome employing a semi-long run real-time PCR approach. Nucleic Acids Res 38: e24. 10.1093/nar/gkp1082; 10.1093/nar/gkp1082
11. Valcarce DG, Carton-Garcia F, Riesco MF, Herraez MP, Robles V (2013) Analysis of DNA damage after human sperm cryopreservation in genes crucial for fertilization and early embryo development. Andrology 1: 723-730. 10.1111/j.2047-2927.2013.00116.x; 10.1111/j.2047-2927.2013.00116.x
12. Riesco MF, Robles V (2013) Cryopreservation causes genetic and epigenetic changes in zebrafish genital ridges. PLoS One 8: e67614. 10.1371/journal.pone.0067614
13. Ausio J, Van Veghel ML, Gomez R, Barreda D (1997) The sperm nuclear basic proteins (SNBPs) of the sponge Neofibularia nolitangere: Implications for the molecular evolution of SNBPs. J Mol Evol 45: 91-96.
14. Eirin-Lopez JM, Lewis JD, Howe le A, Ausio J (2006) Common phylogenetic origin of protamine-like (PL) proteins and histone H1: Evidence from bivalve PL genes. Mol Biol Evol 23: 1304-1317. 10.1093/molbev/msk021
15. Frehlick LJ, Eirin-Lopez JM, Prado A, Su HW, Kasinsky HE, et al. (2006) Sperm nuclear basic proteins of two closely related species of scorpaeniform fish (Sebastes maliger, Sebastolobus sp.) with different sexual reproduction and the evolution of fish protamines. J Exp Zool A Comp Exp Biol 305: 277-287. 10.1002/jez.a.239
16. Saperas N, Chiva M, Pfeiffer DC, Kasinsky HE, Ausio J (1997) Sperm nuclear basic proteins (SNBPs) of agnathans and chondrichthyans: Variability and evolution of sperm proteins in fish. J Mol Evol 44: 422-431.
17. Kurtz K, Saperas N, Ausio J, Chiva M (2009) Spermiogenic nuclear protein transitions and chromatin condensation. proposal for an ancestral model of nuclear spermiogenesis. J Exp Zool B Mol Dev Evol 312B: 149-163. 10.1002/jez.b.21271; 10.1002/jez.b.21271
18. Saperas N, Ausio J, Lloris D, Chiva M (1994) On the evolution of protamines in bony fish: Alternatives to the "retroviral horizontal transmission" hypothesis. J Mol Evol 39: 282-295.
19. Cartón-García F, Riesco MF, Cabrita E, Herráez MP, Robles V (2013) Quantification of lesions in nuclear and mitochondrial genes of Sparus aurata cryopreserved sperm. Aquaculture 402-403: 106.
20. Christoffels A, Koh EG, Chia JM, Brenner S, Aparicio S, et al. (2004) Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol Biol Evol 21: 1146-1151. 10.1093/molbev/msh114
21. Furutani-Seiki M, Wittbrodt J (2004) Medaka and zebrafish, an evolutionary twin study. Mech Dev 121: 629-637. 10.1016/j.mod.2004.05.010
22. Allendorf FW, Stahl G, Ryman N (1984) Silencing of duplicate genes: A null allele polymorphism for lactate dehydrogenase in brown trout (Salmo trutta). Mol Biol Evol 1: 238-248.
23. Mungpakdee S, Seo HC, Angotzi AR, Dong X, Akalin A, et al. (2008) Differential evolution of the 13 atlantic salmon hox clusters. Mol Biol Evol 25: 1333-1343. 10.1093/molbev/msn097; 10.1093/molbev/msn097
24. Avramova Z, Uschewa A, Stephanova E, Tsanev R (1983) Trout sperm chromatin. I. biochemical and immunological study of the protein composition. Eur J Cell Biol 31: 137-142.
25. Herráez MP, Robles V, Cabrita E (2008) Rainbow trout (Oncorhynchus mykiss) sperm cryopreservation. In:, Cabrita E, Robles V, Herraez P,, editors. Methods in Reproductive Aquaculture: Marine and Freshwater Species., : CRC Press. pp. 385.
26. Moussa M, Marinet V, Trimeche A, Tainturier D, Anton M (2002) Low density lipoproteins extracted from hen egg yolk by an easy method: Cryoprotective effect on frozen-thawed bull semen. Theriogenology 57: 1695-1706.
27. Wykes SM, Krawetz SA (2003) The structural organization of sperm chromatin. J Biol Chem 278: 29471-29477. 10.1074/jbc.M304545200
28. Moghadam HK, Ferguson MM, Danzmann RG (2005) Evidence for Hox gene duplication in rainbow trout (Oncorhynchus mykiss): A tetraploid model species. J Mol Evol 61: 804-818. 10.1007/s00239-004-0230-5
29. Sikorsky JA, Primerano DA, Fenger TW, Denvir J (2004) Effect of DNA damage on PCR amplification efficiency with the relative threshold cycle method. Biochem Biophys Res Commun 323: 823-830. 10.1016/j.bbrc.2004.08.168
30. Koubek P, Kralova A, Psenicka M, Peknicova J (2008) The optimization of the protocol for immunofluorescence on fish spermatozoa. Theriogenology 70: 852-858. 10.1016/j.theriogenology.2008.05.050 [doi].
31. Perez-Cerezales S, Martinez-Paramo S, Cabrita E, Martinez-Pastor F, de Paz P, et al. (2009) Evaluation of oxidative DNA damage promoted by storage in sperm from sex-reversed rainbow trout. Theriogenology 71: 605-613. 10.1016/j.theriogenology.2008.09.057; 10.1016/j.theriogenology.2008.09.057
32. Dietrich GJ, Szpyrka A, Wojtczak M, Dobosz S, Goryczko K, et al. (2005) Effects of UV irradiation and hydrogen peroxide on DNA fragmentation, motility and fertilizing ability of rainbow trout (Oncorhynchus mykiss) spermatozoa. Theriogenology 64: 1809-1822. 10.1016/j.theriogenology.2005.04.010
33. Wondrak GT, Jacobson EL, Jacobson MK (2002) Photosensitization of DNA damage by glycated proteins. Photochem Photobiol Sci 1: 355-363.
34. Schuch AP, Menck CF (2010) The genotoxic effects of DNA lesions induced by artificial UV-radiation and sunlight. J Photochem Photobiol B 99: 111-116. 10.1016/j.jphotobiol.2010.03.004; 10.1016/j.jphotobiol.2010.03.004
35. Kawanishi S, Hiraku Y, Oikawa S (2001) Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging. Mutat Res. 488: 65-76. S1383574200000594 [pii]
36. Hiraku Y, Ito K, Hirakawa K, Kawanishi S (2007) Photosensitized DNA damage and its protection via a novel mechanism. Photochem Photobiol. 83: 205-212.2006-03-09-IR-840 [pii]
37. Cabrita E, Robles V, Rebordinos L, Sarasquete C, Herraez MP (2005) Evaluation of DNA damage in rainbow trout (Oncorhynchus mykiss) and gilthead sea bream (Sparus aurata) cryopreserved sperm. Cryobiology 50: 144-153. 10.1016/j.cryobiol.2004.12.003
38. Sies H (2014) Role of metabolic H2O2 generation: Redox signaling and oxidative stress. J Biol Chem 289: 8735-8741. 10.1074/jbc.R113.544635 [doi].
39. Linley E, Denyer SP, McDonnell G, Simons C, Maillard JY (2012) Use of hydrogen peroxide as a biocide: New consideration of its mechanisms of biocidal action. J Antimicrob Chemother 67: 1589-1596. 10.1093/jac/dks129 [doi].
40. Han Y, Chen JZ (2013) Oxidative stress induces mitochondrial DNA damage and cytotoxicity through independent mechanisms in human cancer cells. Biomed Res Int 2013: 825065. 10.1155/2013/825065 [doi].
41. Slupphaug G, Kavli B, Krokan HE (2003) The interacting pathways for prevention and repair of oxidative DNA damage. Mutat Res 531: 231-251.
42. Benhusein GM, Mutch E, Aburawi S, Williams FM (2010) Genotoxic effect induced by hydrogen peroxide in human hepatoma cells using comet assay. Libyan J Med 5: 10.3402/ljm.v5i0.4637. 10.3402/ljm.v5i0.4637 [doi].
43. Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: Lessons from a model bacterium. Nat Rev Microbiol 11: 443-454. 10.1038/nrmicro3032 [doi].
44. Dianov GL, Parsons JL (2007) Co-ordination of DNA single strand break repair. DNA Repair (Amst) 6: 454-460. 10.1016/j.dnarep.2006.10.009
45. Perez-Cerezales S, Martinez-Paramo S, Beirao J, Herraez MP (2010) Evaluation of DNA damage as a quality marker for rainbow trout sperm cryopreservation and use of LDL as cryoprotectant. Theriogenology 74: 282-289. 10.1016/j.theriogenology.2010.02.012; 10.1016/j.theriogenology.2010.02.012
46. Thummel R, Li L, Tanase C, Sarras MP Jr, Godwin AR (2004) Differences in expression pattern and function between zebrafish hoxc13 orthologs: Recruitment of Hoxc13b into an early embryonic role. Dev Biol 274: 318-333. 10.1016/j.ydbio.2004.07.018
47. Durston A, Wacker S, Bardine N, Jansen H (2012) Time space translation: A hox mechanism for vertebrate a-p patterning. Curr Genomics 13: 300-307. 10.2174/138920212800793375; 10.2174/138920212800793375
48. Pascual-Anaya J, D Aniello S, Kuratani S, Garcia-Fernandez J (2013) Evolution of hox gene clusters in deuterostomes. BMC Dev Biol 13: 26. 10.1186/1471-213X-13-26