Sperm protamine-status correlates to the fertility of breeding bulls

Biology of Reproduction

Volumn 92, Issue 4, 2015, Pages

  Dogan, Sule ^a   Vargovic, Peter ^b,g   Oliveira, Rodrigo ^c   Belser, Lauren E ^a   Kaya, Abdullah ^d,h   Moura, Arlindo ^c   Sutovsky, Peter ^b,e   Parrish, John ^f   Topper, Einko ^d   Memili, Erdoğan ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^d Alta Genetics Inc   (United States)

^e University of Missouri   (United States)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

^g INSTITUTE OF EXPERIMENTAL ENDOCRINOLOGY   (Slovakia)

^h SELCUK UNIVERSITY   (Turkey)

Author keywords

Male infertility; PRM1; Protamine; Sperm chromatin; Sperm DNA fragmentation

Indexed keywords

PROTAMINE; TOLONIUM CHLORIDE; CHROMATIN; DNA; NUCLEAR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREEDING; BULL (BOVINE); CELLULAR DISTRIBUTION; CHROMATIN; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA FRAGMENTATION; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MALE; MALE FERTILITY; MALE INFERTILITY; NONHUMAN; NUCLEAR SHAPE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPERM; SPERMATOZOON; SPERMATOZOON HEAD; ANIMAL; BOVINE; CELL SEPARATION; CHEMISTRY; FERTILITY; FLOW CYTOMETRY; INFERTILITY, MALE; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; CATTLE; CELL SEPARATION; CHROMATIN; DNA; FERTILITY; FLOW CYTOMETRY; INFERTILITY, MALE; MALE; NUCLEAR PROTEINS; PROTAMINES; SPERMATOZOA;

EID: 84930588268     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.124255     Document Type: Article

References (59)

1. Ward WS. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 2010; 16:30-36.
2. Gill-Sharma MK, Choudhuri J, D'Souza S. Sperm chromatin protamination:an endocrine perspective. Protein Pept Lett 2011; 18:786-801.
3. Talbert PB, Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 2010; 11:264-275.
4. Miller D, Brinkworth M, Iles D. Paternal DNA packaging in spermatozoa:more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 2010; 139:287-301.
5. Balhorn R. The protamine family of sperm nuclear proteins. Genome Biol 2007; 8:227.
6. 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.
7. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC, Beisel C, Schubeler D, Stadler MB, Peters AH. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 2010; 17:679-687.
8. Gill ME, Erkek S, Peters AH. Parental epigenetic control of embryogenesis:a balance between inheritance and reprogramming? Curr Opin Cell Biol 2012; 24:387-396.
9. Sakkas D, Moffatt O, Manicardi GC, Mariethoz E, Tarozzi N, Bizzaro D. Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol Reprod 2002; 66:1061-1067.
10. Sharma RK, Said T, Agarwal A. Sperm DNA damage and its clinical relevance in assessing reproductive outcome. Asian J Androl 2004; 6:139-148.
11. Marushige Y, Marushige K. Dispersion of mammalian sperm chromatin during fertilization: an in vitro study. Biochim Biophys Acta 1978; 519:1-22.
12. Garcia-Macias V, de Paz P, Martinez-Pastor F, Alvarez M, Gomes-Alves S, Bernardo J, Anel E, Anel L. DNA fragmentation assessment by flow cytometry and Sperm-Bos-Halomax (bright-field microscopy and fluorescence microscopy) in bull sperm. Int J Androl 2007; 30:88-98.
13. Karoui S, Diaz C, Gonzalez-Marin C, Amenabar ME, Serrano M, Ugarte E, Gosalvez J, Roy R, Lopez-Fernandez C, Carabano MJ. Is sperm DNA fragmentation a good marker for field AI bull fertility? J Anim Sci 2012; 90:2437-2449.
14. Gosalvez J, Lopez-Fernandez C, Fernandez JL, Gouraud A, Holt WV. Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol Reprod Dev 2011; 78:951-961.
15. Fortes MR, Holroyd RG, Reverter A, Venus BK, Satake N, Boe-Hansen GB. The integrity of sperm chromatin in young tropical composite bulls. Theriogenology 2012; 78:326-333.
16. Lopez-Fernandez C, Johnston SD, Fernandez JL, Wilson RJ, Gosalvez J. Fragmentation dynamics of frozen-thawed ram sperm DNA is modulated by sperm concentration. Theriogenology 2010; 74:1362-1370.
17. Parrilla I, del Olmo D, Sijses L, Martinez-Alborcia MJ, Cuello C, Vazquez JM, Martinez EA, Roca J. Differences in the ability of spermatozoa from individual boar ejaculates to withstand different semen-processing techniques. Anim Reprod Sci 2012; 132:66-73.
18. Fernandez JL, Muriel L, Goyanes V, Segrelles E, Gosalvez J, Enciso M, LaFromboise M, De Jonge C. Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertil Steril 2005; 84:833-842.
19. Evenson DP, Wixon R. Comparison of the Halosperm test kit with the sperm chromatin structure assay (SCSA) infertility test in relation to patient diagnosis and prognosis. Fertil Steril 2005; 84:846-849.
20. Enciso M, Muriel L, Fernandez JL, Goyanes V, Segrelles E, Marcos M, Montejo JM, Ardoy M, Pacheco A, Gosalvez J. Infertile men with varicocele show a high relative proportion of sperm cells with intense nuclear damage level, evidenced by the sperm chromatin dispersion test. J Androl 2006; 27:106-111.
21. D'Occhio MJ, Hengstberger KJ, Johnston SD. Biology of sperm chromatin structure and relationship to male fertility and embryonic survival. Anim Reprod Sci 2007; 101:1-17.
22. Ballachey BE, Hohenboken WD, Evenson DP. Heterogeneity of sperm nuclear chromatin structure and its relationship to bull fertility. Biol Reprod 1987; 36:915-925.
23. Ballachey BE, Evenson DP, Saacke RG. The sperm chromatin structure assay. Relationship with alternate tests of semen quality and heterospermic performance of bulls. J Androl 1988; 9:109-115.
24. Feugang JM, Rodriguez-Osorio N, Kaya A, Wang H, Page G, Ostermeier GC, Topper EK, Memili E. Transcriptome analysis of bull spermatozoa:implications for male fertility. Reprod Biomed Online 2010; 21:312-324.
25. Aoki VW, Liu L, Jones KP, Hatasaka HH, Gibson M, Peterson CM, Carrell DT. Sperm protamine 1/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertil Steril 2006; 86:1408-1415.
26. Oliva R. Protamines and male infertility. Hum Reprod Update 2006; 12:417-435.
27. de Mateo S, Gazquez C, Guimera M, Balasch J, Meistrich ML, Ballesca JL, Oliva R. Protamine 2 precursors (Pre-P2), protamine 1 to protamine 2 ratio (P1/P2), and assisted reproduction outcome. Fertil Steril 2009; 91:715-722.
28. Balhorn R, Reed S, Tanphaichitr N. Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia 1988; 44:52-55.
29. Zini A, Gabriel SM, Zhang X. The histone to protamine ratio in human spermatozoa: comparative study of whole and processed semen. Fertil Steril 2007; 87:217-219.
30. Gardiner-Garden M, Ballesteros M, Gordon M, Tam PP. Histone-and protamine-DNA association: conservation of different patterns within the beta-globin domain in human sperm. Mol Cell Biol 1998; 18:3350-3356.
31. Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, Hecht NB, Eddy EM. Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet 2001; 28:82-86.
32. Blaschek M, Kaya A, Zwald N, Memili E, Kirkpatrick BW. A wholegenome association analysis of noncompensatory fertility in Holstein bulls. J Dairy Sci 2011; 94:4695-4699.
33. Parrish J, Schindler J, Willenburg K, Enwall L, Kaya A. Quantitative sperm shape analysis: What can this tell us about male fertility. In: 24th Meeting of the National Association of Animal Breeders; 3-4 December, 2012; Columbia, Missouri. Pages 74-80.
34. Parrish JOC, Schindler J, Willenburg K, Enwall L, Kaya A. Quantifying sperm nuclear shape with Fourier harmonic analysis and relationship to spermatogenesis and fertility. In: Association for Applied Animal Andrology, 9th Biennial Conference; 8-10 August 2014; Newcastle, Australia. Pages 30-49.
35. Ostermeier GC, Sargeant GA, Yandell BS, Evenson DP, Parrish JJ. Relationship of bull fertility to sperm nuclear shape. J Androl 2001; 22:595-603.
36. Chang YM, Gianola D, Heringstad B, Klemetsdal G. Effects of trait definition on genetic parameter estimates and sire evaluation for clinical mastitis with threshold models. Animal Science 2004; 79:355-363.
37. Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, Memili E. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2008; 2:19.
38. Zwald NR, Weigel KA, Chang YM, Welper RD, Clay JS. Genetic selection for health traits using producer-recorded data. II. Genetic correlations, disease probabilities, and relationships with existing traits. J Dairy Sci 2004; 87:4295-4302.
39. Zwald NR, Weigel KA, Chang YM, Welper RD, Clay JS. Genetic selection for health traits using producer-recorded data. I. Incidence rates, heritability estimates, and sire breeding values. J Dairy Sci 2004; 87:4287-4294.
40. Beletti ME, Mello ML. Comparison between the toluidine blue stain and the Feulgen reaction for evaluation of rabbit sperm chromatin condensation and their relationship with sperm morphology. Theriogenology 2004; 62:398-402.
41. de Yebra L, Oliva R. Rapid analysis of mammalian sperm nuclear proteins. Anal Biochem 1993; 209:201-203.
42. Odhiambo JF, Sutovsky M, DeJarnette JM, Marshall C, Sutovsky P. Adaptation of ubiquitin-PNA based sperm quality assay for semen evaluation by a conventional flow cytometer and a dedicated platform for flow cytometric semen analysis. Theriogenology 2011; 76:1168-1176.
43. Sutovsky P. Visualization of sperm accessory structures in the mammalian spermatids, spermatozoa, and zygotes by immunofluorescence, confocal, and immunoelectron microscopy. Methods Mol Biol 2004; 253:59-77.
44. Enwall L. Investigating nuclear shape, morphology, and molecular changes in semen from scrotal-insulated Holstein bulls using Fourier harmonic analysis, flow cytometry, and in vitro fertility evaluations. Madison, WI: University of Wisconsin-Madison; 2009. Thesis.
45. Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, Memili E. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2008; 2:19.
46. Bellve AR, Chandrika R, Martinova YS, Barth AH. The perinuclear matrix as a structural element of the mouse sperm nucleus. Biol Reprod 1992; 47:451-465.
47. Tovich PR, Sutovsky P, Oko RJ. Novel aspect of perinuclear theca assembly revealed by immunolocalization of non-nuclear somatic histones during bovine spermiogenesis. Biol Reprod 2004; 71:1182-1194.
48. Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U. Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod 1999; 4:31-37.
49. Karoui S, Di{dotless}az C, González-Mari{dotless}n C, Amenabar ME, Serrano M. Is sperm DNA fragmentation a good marker for field AI bull fertility? J Anim Sci 2012; 90:2437-2449.
50. Fortes MR, Satake N, Corbet DH, Corbet NJ, Burns BM, Moore SS, Boe-Hansen GB. Sperm protamine deficiency correlates with sperm DNA damage in Bos indicus bulls. Andrology 2014; 2:370-378.
51. Ostermeier GC, Sargeant GA, Yandell TBS, Parrish JJ. Measurement of bovine sperm nuclear shape using Fourier harmonic amplitudes. J Androl 2001; 22:584-594.
52. Parrish JJ, Enwall L, Kaya A, Pawshe C, Siddiqui MA, Shamusuddin M. Sperm shape research: an update. In: 21st Meeting of the National Association of Animal Breeders; 8 September 2006, Columbia, Missouri. Pages 19-26.
53. Rahman MB, Vandaele L, Rijsselaere T, Maes D, Hoogewijs M, Frijters A, Noordman J, Granados A, Dernelle E, Shamsuddin M, Parrish JJ, Van Soom A. Scrotal insulation and its relationship to abnormal morphology, chromatin protamination and nuclear shape of spermatozoa in Holstein-Friesian and Belgian Blue bulls. Theriogenology 2011; 76:1246-1257.
54. de Yebra L, Ballesca JL, Vanrell JA, Corzett M, Balhorn R, Oliva R. Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels. Fertil Steril 1998; 69:755-759.
55. Mengual L, Ballesca JL, Ascaso C, Oliva R. Marked differences in protamine content and P1/P2 ratios in sperm cells from percoll fractions between patients and controls. J Androl 2003; 24:438-447.
56. Hammadeh ME, Hamad MF, Montenarh M, Fischer-Hammadeh C. Protamine contents and P1/P2 ratio in human spermatozoa from smokers and non-smokers. Hum Reprod 2010; 25:2708-2720.
57. Depa-Martynow M, Kempisty B, Jagodzinski PP, Pawelczyk L, Jedrzejczak P. Impact of protamine transcripts and their proteins on the quality and fertilization ability of sperm and the development of preimplantation embryos. Reprod Biol 2012; 12:57-72.
58. Dobrinski I, Hughes HP, Barth AD. Flow cytometric and microscopic evaluation and effect on fertility of abnormal chromatin condensation in bovine sperm nuclei. J Reprod Fertil 1994; 101:531-538.
59. Yamauchi Y, Shaman JA, Ward WS. Non-genetic contributions of the sperm nucleus to embryonic development. Asian J Androl 2011; 13:31-35.