Recent knowledge concerning mammalian sperm chromatin organization and its potential weaknesses when facing oxidative challenge

Basic and Clinical Andrology - Tập 24 Số 1 - 2014
Anaīs Noblanc1, Ayhan Kocer1, Joël R. Drevet1
1GReD Laboratory, CNRS UMR 6293 - INSERM U1103, Clermont Université, Aubière, France

Tóm tắt

Từ khóa


Tài liệu tham khảo

Kouzarides T: Chromatin modifications and their functions. Cell. 2007, 128: 693-705. 10.1016/j.cell.2007.02.005.

Munshi A, Shafi G, Aliya N, Jyothy A: Histone modifications dictate specific biological readouts. J Genet Genomics Yi Chuan Xue Bao. 2009, 36: 75-88. 10.1016/S1673-8527(08)60094-6.

Talbert PB, Henikoff S: Histone variants–ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol. 2010, 11: 264-275. 10.1038/nrm2861.

Lewis JD, Abbott DW, Ausió J: A haploid affair: core histone transitions during spermatogenesis. Biochem Cell Biol. 2003, 81: 131-140. 10.1139/o03-045.

Kimmins S, Sassone-Corsi P: Chromatin remodelling and epigenetic features of germ cells. Nature. 2005, 434: 583-589. 10.1038/nature03368.

Kota SK, Feil R: Epigenetic transitions in germ cell development and meiosis. Dev. Cell. 2010, 19: 675-686. 10.1016/j.devcel.2010.10.009.

Remeseiro S, Losada A: Cohesin, a chromatin engagement ring. Curr Opin Cell Biol. 2013, 25: 63-71. 10.1016/j.ceb.2012.10.013.

Mehta GD, Kumar R, Srivastava S, Ghosh SK: Cohesin: functions beyond sister chromatid cohesion. FEBS lett. 2013, 587: 2299-2312. 10.1016/j.febslet.2013.06.035.

Sasaki H, Matsui Y: Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet. 2008, 9: 129-140. 10.1038/ni1560.

Buard J, Barthès P, Grey C, de Massy B: Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J. 2009, 28: 2616-2624. 10.1038/emboj.2009.207.

Wang JC: Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol. 2002, 3: 430-440. 10.1038/nrm831.

Laberge RM, Boissonneault G: On the nature and origin of DNA strand breaks in elongating spermatids. Biol Reprod. 2005, 73 (2): 289-296. 10.1095/biolreprod.104.036939.

Leduc F, Nkoma GB, Boissonneault G: Spermiogenesis and DNA repair: a possible etiology of human infertility and genetic disorders. Syst Biol Reprod Med. 2008, 54 (1): 3-10. 10.1080/19396360701876823.

Grégoire MC, Massonneau J, Simard O, Gouraud A, Brazeau MA, Arguin M, Leduc F, Boissonneault G: Male-driven de novo mutations in haploid germ cells. Mol Hum Reprod. 2013, 19 (8): 495-499. 10.1093/molehr/gat022.

Caron C, Pivot-Pajot C, Van Grunsven LA, Col E, Lestrat C, Rousseaux S, Khochbin S: Cdyl: a new transcriptional co-repressor. EMBO Rep. 2003, 4: 877-882. 10.1038/sj.embor.embor917.

Shang E, Nickerson HD, Wen D, Wang X, Wolgemuth DJ: The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development. 2007, 134: 3507-3515. 10.1242/dev.004481.

Dhar S, Thota A, Rao MRS: Insights into role of bromodomain, testis-specific (Brdt) in acetylated histone H4-dependent chromatin remodeling in mammalian spermiogenesis. J Biol Chem. 2012, 287: 6387-6405. 10.1074/jbc.M111.288167.

Pivot-Pajot C, Caron C, Govin J, Vion A, Rousseaux S, Khochbin S: Acetylation-dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein. Mol Cell Biol. 2003, 23: 5354-5365. 10.1128/MCB.23.15.5354-5365.2003.

Chiva M, Saperas N, Ribes E: Complex chromatin condensation patterns and nuclear protein transitions during spermiogenesis: examples from mollusks. Tissue Cell. 2011, 43: 367-376. 10.1016/j.tice.2011.08.001.

Martins RP, Ostermeier GC, Krawetz SA: Nuclear matrix interactions at the human protamine domain: a working model of potentiation. J Biol Chem. 2004, 279: 51862-51868. 10.1074/jbc.M409415200.

Dadoune JP: Expression of mammalian spermatozoal nucleoproteins. Microsc Res Tech. 2003, 61: 56-75. 10.1002/jemt.10317.

Ullas KS, Rao MR: Phosphorylation of rat spermatidal protein TP2 by sperm-specific protein kinase A and modulation of its tarnsport into the haploid nucleus. J Biol Chem. 2003, 278: 52673-52680. 10.1074/jbc.M308365200.

Pradeepa MM, Manjunatha S, Sathish V, Agrawal S, Rao MR: Involvement of importin-4 in the transport of tarnsition protein 2 into the spermatid nucleus. Mol Cell Biol. 2008, 28 (13): 4331-4341. 10.1128/MCB.00519-07.

Singh J, Rao MR: Interaction of rat testis protein, TP, with nucleic acids in vitro. Fluorescence quenching, UV absorption, and thermal denaturation studies. J Biol Chem. 1987, 262: 734-740.

Singh J, Rao MR: Interaction of rat testis protein, TP, with nucleosome core particle. Biochem Int. 1988, 17: 701-710.

Akama K, Kondo M, Sato H, Nakano M: Transition protein 4 from boar late spermatid nuclei is a topological factor that stimulates DNA-relaxing activity of topoisomerase I. FEBS Lett. 1999, 442: 189-192. 10.1016/S0014-5793(98)01649-4.

Caron N, Veilleux S, Boissonneault G: Stimulation of DNA repair by the spermatidal TP1 protein. Mol Reprod Dev. 2001, 58: 437-443. 10.1002/1098-2795(20010401)58:4<437::AID-MRD12>3.0.CO;2-Q.

Yu YE, Zhang Y, Unni E, Shirley CR, Deng JM, Russell LD, Weil MM, Behringer RR, Meistrich ML: Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice. Proc Natl Acad Sci U S A. 2000, 97: 4683-4688. 10.1073/pnas.97.9.4683.

Baskaran R, Rao MRS: Interaction of spermatid-specific protein TP2 with nucleic acids, in vitro. A comparative study with TP1. J Biol Chem. 1990, 265: 21039-21047.

Lévesque D, Veilleux S, Caron N, Boissonneault G: Architectural DNA-Binding Properties of the Spermatidal Transition Proteins 1 and 2. Biochem Biophys Res Commun. 1998, 252: 602-609. 10.1006/bbrc.1998.9687.

Zhao M, Shirley CR, Yu YE, Mohapatra B, Zhang Y, Unni E, Deng JM, Arango NA, Terry NH, Weil MM, Russell LD, Behringer RR, Meistrich ML: Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Mol Cell Biol. 2001, 21: 7243-7255. 10.1128/MCB.21.21.7243-7255.2001.

Shirley CR, Hayashi S, Mounsey S, Yanagimachi R, Meistrich ML: Abnormalities and reduced reproductive potential of sperm from Tnp1- and Tnp2-null double mutant mice. Biol Reprod. 2004, 1: 1220-1229.

Aoki VW, Carrell DT: Human protamines and the developing spermatid: their structure, function, expression and relationship with male infertility. Asian J Androl. 2003, 5: 315-324.

Hermo L, Pelletier R-M, Cyr DG, Smith CE: Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 2: changes in spermatid organelles associated with development of spermatozoa. Microsc Res Tech. 2010, 73: 279-319.

Martin-Coello J, Gomendio M, Roldan ERS: Protamine 3 shows evidence of weak, positive selection in mouse species (genus Mus)—but it is not a protamine. Biol Reprod. 2011, 84: 320-326. 10.1095/biolreprod.110.086454.

Balhorn R: Mammalian protamines: structure and molecular interactions. Molecular Biology of Chromosome Function. Edited by: Adolph KW. 1989, New York: Springer, 366-395.

Debarle M, Martinage A, Sautiere P, Chevaillier P: Persistence of protamine precursors in mature sperm nuclei of the mouse. Mol Reprod Dev. 1995, 40: 84-90. 10.1002/mrd.1080400111.

Yoshii T, Kuji N, Komatsu S, Iwahashi K, Tanaka Y, Yoshida H, Wada A, Yoshimura Y: Fine resolution of human sperm nucleoproteins by two-dimensional electrophoresis. Mol Hum Reprod. 2005, 11: 677-681. 10.1093/molehr/gah217.

Hud NV, Milanovich FP, Balhorn R: Evidence of novel secondary structure in DNA-bound protamine is revealed by Raman spectroscopy. Biochemistry (Mosc.). 1994, 33: 7528-7535. 10.1021/bi00190a005.

Bench GS, Friz AM, Corzett MH, Morse DH, Balhorn R: DNA and total protamine masses in individual sperm from fertile mammalian subjects. Cytometry. 1996, 23: 263-271. 10.1002/(SICI)1097-0320(19960401)23:4<263::AID-CYTO1>3.0.CO;2-I.

Björndahl L, Kvist U: Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Hum Reprod. 2010, 16: 23-29. 10.1093/molehr/gap099.

Allen MJ, Bradbury EM, Balhorn R: AFM analysis of DNA-protamine complexes bound to mica. Nucleic Acids Res. 1997, 25: 2221-2226. 10.1093/nar/25.11.2221.

Brewer LR, Corzett M, Balhorn R: Protamine-induced condensation and decondensation of the same DNA molecule. Science. 1999, 286: 120-123. 10.1126/science.286.5437.120.

Balhorn R: The protamine family of sperm nuclear proteins. Genome Biol. 2007, 8: 227-10.1186/gb-2007-8-9-227.

Ward WS, Coffey DS: Identification of a sperm nuclear annulus: a sperm DNA anchor. Biol Reprod. 1989, 41: 361-370. 10.1095/biolreprod41.2.361.

Barone JG, De Lara J, Cummings KB, Ward WS: DNA organization in human spermatozoa. J Androl. 1994, 15: 139-144.

Sotolongo B, Lino E, Ward WS: Ability of hamster spermatozoa to digest their own DNA. Biol Reprod. 2003, 69: 2029-2035. 10.1095/biolreprod.103.020594.

Ward WS, Coffey DS: DNA Packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod. 1991, 44: 569-574. 10.1095/biolreprod44.4.569.

McCarthy S, Ward WS: Functional aspects of mammalian sperm chromatin. Hum Fertil Camb Engl. 1999, 2: 56-60. 10.1080/1464727992000198321.

Shaman JA, Yamauchi Y, Ward WS: Function of the sperm nuclear matrix. Arch Androl. 2007, 53: 135-140. 10.1080/01485010701329378.

Shaman JA, Yamauchi Y, Ward WS: The sperm nuclear matrix is required for paternal DNA replication. J Cell Biochem. 2007, 102: 680-688. 10.1002/jcb.21321.

Ward WS: Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod. 2010, 16: 30-36. 10.1093/molehr/gap080.

Balhorn R, Gledhill BL, Wyrobek AJ: Mouse sperm chromatin proteins: quantitative isolation and partial characterization. Biochemistry (Mosc.). 1997, 16: 4074-4080.

Tanphaichitr N, Sobhon P, Taluppeth N, Chalermisarachai P: Basic nuclear proteins in testicular cells and ejaculated spermatozoa in man. Exp Cell Res. 1978, 117: 347-356. 10.1016/0014-4827(78)90148-9.

Van der Heijden GW, Ramos L, Baart EB, van den Berg IM, Derijck AA, van der Vlag J, Martini E, de Boer P: Sperm-derived histones contribute to zygotic chromatin in humans. BioMed Cent Dev Biol. 2008, 8: 34-doi:10.1186/1471-213X-8-34

Nakazawa Y, Shimada A, Noguchi J, Domeki I, Kaneko H, Kikuchi K: Replacement of nuclear protein by histone in pig sperm nuclei during in vitro fertilization. Reproduction. 2002, 124: 565-572. 10.1530/rep.0.1240565.

Ajduk A, Yamauchi Y, Ward MA: Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization. Biol Reprod. 2006, 75: 442-451. 10.1095/biolreprod.106.053223.

Jenkins TG, Carrell DT: Dynamic alterations in the paternal epigenetic landscape following fertilization. Front Genet. 2012, 3: 143-

Jenkins TG, Carrell DT: The sperm epigenome and potential implications for the developing embryo. Reproduction. 2012, 143: 727-734. 10.1530/REP-11-0450.

Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE, Saida M, Sreger K, Tedder P, Miller D: Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res. 2009, 19: 1338-1349. 10.1101/gr.094953.109.

Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR: Distinctive chromatin in human sperm packages genes for embryo development. Nature. 2009, 460: 473-478.

Zalensky AO, Siino JS, Gineitis AA, Zalenskaya IA, Tomilin NV, Yau P, Bradbury EM: Human testis/sperm-specific histone H2B (hTSH2B). Molecular cloning and characterization. J Biol Chem. 2002, 277: 43474-43480. 10.1074/jbc.M206065200.

Li Y, Lalancette C, Miller D, Krawetz SA: Characterization of nucleohistone and nucleoprotamine components in the mature human sperm nucleus. Asian J Androl. 2008, 10: 535-541. 10.1111/j.1745-7262.2008.00410.x.

Noblanc A, Damon-Soubeyrand C, Karrich B, Henry-Berger J, Cadet R, Saez F, Guiton R, Janny L, Pons-Rejraji H, Alvarez JG, Drevet JR, Kocer A: DNA oxidative damage in mammalian spermatozoa: where and why is the male nucleus affected?. Free Radic Biol Med. 2013, 65: 719-723.

Zalenskaya IA, Bradbury EM, Zalensky AO: Chromatin structure of telomere domain in human sperm. Biochem Biophys Res Commun. 2000, 279: 213-218. 10.1006/bbrc.2000.3917.

Zalensky AO, Breneman JW, Zalenskaya IA, Brinkley BR, Bradbury EM: Organization of centromeres in the decondensed nuclei of mature human sperm. Chromosoma. 1993, 102: 509-518. 10.1007/BF00368344.

Mudrak O, Tomilin N, Zalensky A: Chromosome architecture in the decondensing human sperm nucleus. J Cell Sci. 2005, 118: 4541-4550. 10.1242/jcs.02581.

Hazzouri M, Rousseaux S, Mongelard F, Usson Y, Pelletier R, Faure AK, Vourc'h C, Sèle B: Genome organization in the human sperm nucleus studied by FISH and confocal microscopy. Mol Reprod Dev. 2000, 55: 307-315. 10.1002/(SICI)1098-2795(200003)55:3<307::AID-MRD9>3.0.CO;2-P.

Zalenskaya IA, Zalensky AO: Non-random positioning of chromosomes in human sperm nuclei. Chromosome Res. 2004, 12: 163-173.

Mudrak OSB, Nazarov I, Jones EL, Zalensky AO: Positioning of chromosomes in human spermatozoa is determined by ordered centromere arrangement. PLoS ONE. 2012, 7: e52944-10.1371/journal.pone.0052944.

Millan NM, Lau P, Hann M, Ioannou D, Hoffman D, Barrionuevo M, Maxson W, Ory S, Tempest HG: Hierarchical radial and polar organisation of chromosomes in human sperm. Chromosome Res. 2012, 20: 875-887. 10.1007/s10577-012-9323-y.

Morris ID, Ilott S, Dixon L, Brison DR: The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. Hum Reprod Oxf Engl. 2002, 17: 990-998. 10.1093/humrep/17.4.990.

Zini A: Are sperm chromatin and DNA defects relevant in the clinic?. Syst Biol Reprod Med. 2011, 57: 78-85. 10.3109/19396368.2010.515704.

Gawecka JE, Marh J, Ortega M, Yamauchi Y, Ward MA, Ward WS: Mouse zygotes respond to severe sperm DNA damage by delaying paternal DNA replication and embryonic development. PLoS ONE. 2013, 8: e56385-10.1371/journal.pone.0056385.

Aitken RJ, De Iuliis GN: Origins and consequences of DNA damage in male germ cells. Reprod Biomed Online. 2007, 4 (6): 727-33.

Zini A, Boman JM, Belzile E, Ciampi A: Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod. 2008, 23 (12): 2663-2668. 10.1093/humrep/den321.

Studies on Men’s Health and Fertility. Edited by: Agarwal A, Alvarez JG, Aitken JR. 2012, New York, NY 10013, USA: Oxidative Stress Applied Basic Research and Clinical Practice, doi:10.1007/978-1-61779-776-7-5

Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN: Oxidative stress and male reproductive health. Asian J Androl. 2014, 16 (1): 31-38. 10.4103/1008-682X.122203.

Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS: Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod. 1998, 59 (5): 1037-1046. 10.1095/biolreprod59.5.1037.

Kao S-H, Chao H-T, Chen H-W, Hwang TIS, Liao T-L, Wei Y-H: Increase of oxidative stress in human sperm with lower motility. Fertil Steril. 2008, 89: 1183-1190. 10.1016/j.fertnstert.2007.05.029.

Aitken RJ, De Iuliis GN: On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2010, 16 (1): 3-13. 10.1093/molehr/gap059.

Aitken RJ: Free radicals, lipid peroxidation and sperm function. Reprod Fertil Dev. 1995, 7: 659-668. 10.1071/RD9950659.

Agarwal A, Saleh RA, Bedaiwy MA: Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003, 79: 829-843. 10.1016/S0015-0282(02)04948-8.

Aitken RJ, Baker MA, De Iuliis GN, Nixon B: New insights into sperm physiology and pathology. Handb Exp Pharmacol. 2010, 198: 99-115. 10.1007/978-3-642-02062-9_7.

Chabory E, Damon C, Lenoir A, Kauselmann G, Kern H, Zevnik B, Garrel C, Saez F, Cadet R, Henry-Berger J, Schoor M, Gottwald U, Habenicht U, Drevet JR, Vernet P: Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Invest. 2009, 119: 2074-2085.

Meseguer M, Martínez-Conejero JA, O'Connor JE, Pellicer A, Remohí J, Garrido N: The significance of sperm DNA oxidation in embryo development and reproductive outcome in an oocyte donation program: a new model to study a male infertility prognostic factor. Fertil Steril. 2008, 89 (5): 1191-1199. 10.1016/j.fertnstert.2007.05.005.

Gupta S, Agarwal A, Banerjee J, Alvarez JG: The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systemic review. Obstet Gynecol Surv. 2007, 62 (5): 335-347. 10.1097/01.ogx.0000261644.89300.df.

Aitken RJ, Curry BJ: Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal. 2011, 14 (3): 367-381. 10.1089/ars.2010.3186.

Zini A, Sigman M: Are tests of sperm DNA damage clinically useful?. Pros and cons. J Androl. 2009, 30 (3): 219-229. 10.2164/jandrol.108.006908.

Banks S, King SA, Irvine DS, Saunders PTK: Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reprod Camb Engl. 2005, 129: 505-514.

Bennetts LE, De Iuliis GN, Nixon B, Kime M, Zelski K, McVicar CM, Lewis SE, Aitken RJ: Impact of estrogenic compounds on DNA integrity in human spermatozoa: evidence for cross-linking and redox cycling activities. Mutat Res. 2008, 641: 1-11. 10.1016/j.mrfmmm.2008.02.002.

Sakkas D, Alvarez JG: Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010, 93: 1027-1036. 10.1016/j.fertnstert.2009.10.046.

Smith TB, Dun MD, Smith ND, Curry BJ, Connaughton HS, Aitken RJ: The presence of a truncated base excision repair pathway in human spermatozoa that is mediated by OGG1. J Cell Sci. 2013, 126 (6): 1488-1497. 10.1242/jcs.121657.

Noblanc A, Kocer A, Chabory E, Vernet P, Saez F, Cadet R, Conrad M, Drevet JR: Glutathione peroxidases at work on epididymal spermatozoa: an example of the dual effect of reactive oxygen species on mammalian male fertilizing ability. J Androl. 2011, 32: 641-650. 10.2164/jandrol.110.012823.

Drevet JR: Protection of epididymal spermatozoa from oxidative stress. Studies on Men’s Health and Fertility. Edited by: Agarwal A, Alvarez JG, Aitken JR. 2012, New York, NY 10013, USA: Oxidative Stress in Applied Basic Research and Clinical Practice, doi:10.1007/978-1-61779-776-7-5

Vernet P, Aitken RJ, Drevet JR: Antioxidant strategies in the epididymis. Mol Cell Endocrinol. 2004, 216: 31-39. 10.1016/j.mce.2003.10.069.

Chabory E, Damon C, Lenoir A, Henry-Berger J, Vernet P, Cadet R, Saez F, Drevet JR: Mammalian glutathione peroxidases control acquisition and maintenance of spermatozoa integrity. J Anim Sci. 2010, 88: 1321-1331. 10.2527/jas.2009-2583.

Noblanc A, Peltier M, Damon-Soubeyrand C, Kerchkove N, Chabory E, Vernet P, Saez F, Cadet R, Janny L, Pons-Rejraji H, Conrad M, Drevet JR, Kocer A: Epididymis response partly compensates for spermatozoa oxidative defects in snGPx4 and GPx5 double mutant mice. PLoS ONE. 2012, 7 (6): e38565-10.1371/journal.pone.0038565. doi:10.1371/journal.pone.0038565. Epub 2012 Jun 14

Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW: Sequence-specific packaging of DNA in human sperm chromatin. Science. 1987, 236 (4804): 962-964. 10.1126/science.3576213.

Wykes SM, Krawetz SA: The structural organization of sperm chromatin. J Biol Chem. 2003, 278 (32): 29471-29477. 10.1074/jbc.M304545200.

Anachkova B, Djeliova V, Russev G: Nuclear matrix support of DNA replication. J Cell Biochem. 2005, 96: 951-961. 10.1002/jcb.20610.

Wilson RHC, Coverley D: Relationship between DNA replication and the nuclear matrix. Genes Cells. 2013, 18: 17-31. 10.1111/gtc.12010.

Gharagozloo P, Aitken RJ: The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod. 2011, 26 (7): 1628-1640. 10.1093/humrep/der132.

Lewis SE, John Aitken R, Conner SJ, Iuliis GD, Evenson DP, Henkel R, Giwercman A, Gharagozloo P: The impact of sperm DNA damage in assisted conception and beyond: recent advances in diagnosis and treatment. Reprod Biomed Online. 2013, 27 (4): 325-337. 10.1016/j.rbmo.2013.06.014.

The Practice Committee of the American Society for Reproductive Medicine: The clinical utility of sperm DNA integrity testing: a guideline. Fertil Steril. 2008, 90 (5 Suppl): S178-80. doi:10.1016/j.fertnstert.2008.08.054

Barratt CL, Aitken RJ, Björndahl L, Carrell DT, de Boer P, Kvist U, Lewis SE, Perreault SD, Perry MJ, Ramos L, Robaire B, Ward S, Zini A: Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications–a position report. Hum Reprod Oxf Engl. 2010, 25: 824-838. 10.1093/humrep/dep465.

Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, Purvis K, de Angelis P, Claussen OP: Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod. 1999, 14 (4): 1039-1049. 10.1093/humrep/14.4.1039.

Spanò M, Bonde JP, Hjøllund HI, Kolstad HA, Cordelli E, Leter G: Sperm chromatin damage impairs human fertility. The Danish first pregnancy planner study team. Fertil Steril. 2000, 73 (1): 43-50. 10.1016/S0015-0282(99)00462-8.

Cohen-Bacrie P, Belloc S, Menezo YJ, Clement P, Hamidi J, Benkhalifa M: Correlation between DNA damage and sperm parameters: a prospective study of 1,633 patients. Fertil Steril. 2009, 91: 1801-1805. 10.1016/j.fertnstert.2008.01.086.