Transcriptome analysis of bull semen with extreme nonreturn rate: Use of suppression-subtractive hybridization to identify functional markers for fertility

Biology of Reproduction

Volumn 78, Issue 4, 2008, Pages 618-635

  Lalancette, C ^a   Thibault, C ^a   Bachand, I ^a   Caron, N ^b   Bissonnette, N ^a  

^a SHERBROOKE RESEARCH AND DEVELOPMENT CENTRE   (Canada)

^b Semex Alliance Inc   (Canada)

Author keywords

Gamete biology; Sperm; Spermatogenesis

Indexed keywords

MOLECULAR MARKER; RNA 12S; RNA 18S; TRANSCRIPTOME;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BULL (BOVINE); CELL DIFFERENTIATION; COHORT ANALYSIS; CONTROLLED STUDY; EXPRESSED SEQUENCE TAG; FERTILITY; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; MALE; MALE GENITAL SYSTEM; METABOLISM; MICROARRAY ANALYSIS; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SEMEN ANALYSIS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOON; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; UNINDEXED SEQUENCE; VALIDATION PROCESS;

ANIMALS; CATTLE; CATTLE DISEASES; FERTILITY; GENE EXPRESSION PROFILING; GENE LIBRARY; INFERTILITY, MALE; MALE; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEMEN;

BOVINAE;

EID: 41549093779     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.106.059030     Document Type: Article

References (63)

1. Pessot CA, Brito M, Figueroa J, Concha II, Yanez A, Burzio LO. Presence of RNA in the sperm nucleus. Biochem Biophys Res Commun 1989; 158:272-278.
2. Dadoune JP, Siffroi JP, Alfonsi MF. Transcription in haploid male germ cells. Int Rev Cytol 2004; 237:1-56.
3. Kleene KC. A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech Dev 2001; 106:3-23.
4. Geremia R, Boitani C, Conti M, Monesi V. RNA synthesis in spermatocytes and spermatids and preservation of meiotic RNA during spermiogenesis in the mouse. Cell Differ 1977; 5:343-355.
5. Lambard S, Galeraud-Denis I, Martin G, Levy R, Chocat A, Carreau S. Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation. Mol Hum Reprod 2004; 10:535-541.
6. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA. Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 2004; 429:154.
7. Ostermeier GC, Goodrich RJ, Moldenhauer JS, Diamond MP, Krawetz SA. A suite of novel human spermatozoal RNAs. J Androl 2005; 26:70-74.
8. Ostermeier GC, Dix DJ, Miller D, Khatri P, Krawetz SA. Spermatozoal RNA profiles of normal fertile men. Lancet 2002; 360:772-777.
9. Wang H, Zhou Z, Xu M, Li J, Xiao J, Xu ZY, Sha J. A spermatogenesis- related gene expression profile in human spermatozoa and its potential clinical applications. J Mol Med 2004; 82:317-324.
10. Miller D, Ostermeier GC, Krawetz SA. The controversy, potential and roles of spermatozoal RNA. Trends Mol Med 2005; 11:156-163.
11. Yatsenko AN, Roy A, Chen R, Ma L, Murthy LJ, Yan W, Lamb DJ, Matzuk MM. Noninvasive genetic diagnosis of male infertility using spermatozoal RNA: KLHL10 mutations in oligozoospermic patients impair homodimerization. Hum Mol Genet 2006; 15:3411-3419.
12. Braundmeier AG, Miller DJ. The search is on: finding accurate molecular markers of male fertility. J Dairy Sci 2001; 84:1915-1925.
13. Januskauska A, Johannisson A, Rodriguez-Martinez H. Assessment of sperm quality through fluorometry and sperm chromatin structure assay in relation to field fertility of frozen-thawed semen from Swedish AI bulls. Theriogenology 2001; 55:947-961.
14. Thundathil J, Gil J, Januskauskas A, Larsson B, Soderquist L, Mapletoft R, Rodriguez-Martinez H. Relationship between the proportion of capacitated spermatozoa present in frozen-thawed bull semen and fertility with artificial insemination. Int J Androl 1999; 22:366-373.
15. Zhang BR, Larsson B, Lundeheim N, Rodriguez-Martinez H. Relationship between embryo development in vitro and 56-day nonreturn rates of cows inseminated with frozen-thawed semen from dairy bulls. Theriogenology 1997; 48:221-231.
16. Rodriguez-Martinez H. Can we increase the estimative value of semen assessment? Reprod Domest Anim 2006; 41(suppl 2):2-10.
17. Koops WJ, Grossman M, Den Daas JH. A model for reproductive efficiency of dairy bulls. J Dairy Sci 1995; 78:921-928.
18. Zhang BR, Larsson B, Lundeheim N, Rodriguez-Martinez H. Sperm characteristics and zona pellucida binding in relation to field fertility of frozen-thawed semen from dairy AI bulls. Int J Androl 1998; 21:207-216.
19. Zhang BR, Larsson B, Lundeheim N, Haard MG, Rodriguez-Martinez H. Prediction of bull fertility by combined in vitro assessments of frozen-thawed semen from young dairy bulls entering an AI-programme. Int J Androl 1999; 22:253-260.
20. Doepel L, Lessard M, Gagnon N, Lobley GE, Bernier JF, Dubreuil P, Lapierre H. Effect of postruminal glutamine supplementation on immune response and milk production in dairy cows. J Dairy Sci 2006; 89:3107-3121.
21. Ostermeier GC, Goodrich RJ, Diamond MP, Dix DJ, Krawetz SA. Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil Steril 2005; 83:1687-1694.
22. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389-3402.
23. Levesque-Sergerie JP, Duquette M, Thibault C, Bissonnette N. Detection limits of several commercial reverse transcriptase enzymes: impact on the low- and high-abundance transcript levels assessed by quantitative RT-PCR. BMC Molecular Biology 2007; 8:93-110.
24. Morrison TB, Weis JJ, Wittwer CT. Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. Biotechniques 1998; 24:954-962.
25. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci U S A 1996; 93:6025-6030.
26. St John JC, Jokhi RP, Barratt CL. The impact of mitochondrial genetics on male infertility. Int J Androl 2005; 28:65-73.
27. Miller D. Ensuring continuity of the paternal genome: potential roles for spermatozoal RNA in mammalian embryogenesis. Soc Reprod Fertil Suppl 2007; 65:373-389.
28. Evans SJ, Datson NA, Kabbaj M, Thompson RC, Vreugdenhil E, De Kloet ER, Watson SJ, Akil H. Evaluation of Affymetrix GeneChip sensitivity in rat hippocampal tissue using SAGE analysis: serial analysis of gene expression. Eur J Neurosci 2002; 16:409-413.
29. Cao W, Epstein C, Liu H, DeLoughery C, Ge N, Lin J, Diao R, Cao H, Long F, Zhang X, Chen Y, Wright PS, et al. Comparing gene discovery from Affymetrix GeneChip microarrays and Clontech PCR-select cDNA subtraction: a case study. BMC Genomics 2004; 5:26-35.
30. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, Griswold MD, Lee JT. Postmeiotic sex chromatin in the male germline of mice. Curr Biol 2006; 16:660-667.
31. Bouma GJ, Affourtit JP, Bult CJ, Eicher EM. Transcriptional profile of mouse pregranulosa and Sertoli cells isolated from early differentiated fetal gonads. Gene Expr Patterns 2007; 7:113-123.
32. Ruiz-Pesini E, Lapena AC, Diez-Sanchez C, Perez-Martos A, Montoya J, Alvarez E, Diaz M, Urries A, Montoro L, Lopez-Perez MJ, Enriquez JA. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am J Hum Genet 2000; 67:682-696.
33. St John JC, Bowles EJ, Amaral A. Sperm mitochondria and fertilisation. Soc Reprod Fertil Suppl 2007; 65:399-416.
34. Fernandez-Moreno MA, Bornstein B, Petit N, Garesse R. The pathophysiology of mitochondrial biogenesis: toward four decades of mitochondrial DNA research. Mol Genet Metab 2000; 71:481-495.
35. Baumber J, Ball BA, Gravance CG, Medina V, Davies-Morel MC. The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential, and membrane lipid peroxidation. J Androl 2000; 21:895-902.
36. Evenson DP, Darzynkiewicz Z, Melamed MR. Simultaneous measurement by flow cytometry of sperm cell viability and mitochondrial membrane potential related to cell motility. J Histochem Cytochem 1982; 30:279-280.
37. Garner DL, Thomas CA, Allen CH. Effect of semen dilution on bovine sperm viability as determined by dual-DNA staining and flow cytometry. J Androl 1997; 18:324-331.
38. Hallap T, Nagy S, Jaakma U, Johannisson A, Rodriguez-Martinez H. Mitochondrial activity of frozen-thawed spermatozoa assessed by MitoTracker Deep Red 633. Theriogenology 2005; 63:2311-2322.
39. Frank SA, Hurst LD. Mitochondria and male disease. Nature 1996; 383:224.
40. Clark HF, Gurney AL, Abaya E, Baker K, Baldwin D, Brush J, Chen J, Chow B, Chui C, Crowley C, Currell B, Deuel B, et al. The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment. Genome Res 2003; 13:2265-2270.
41. Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, Fossa SD, Duale N, Brunborg G, Kallioniemi O, Andrews PW, Lothe RA. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res 2005; 65:5588-5598.
42. Soues S, Kann ML, Fouquet JP, Melki R. The cytosolic chaperonin CCT associates to cytoplasmic microtubular structures during mammalian spermiogenesis and to heterochromatin in germline and somatic cells. Exp Cell Res 2003; 288:363-373.
43. Willison KR, Hynes G, Davies P, Goldsborough A, Lewis VA. Expression of three tÙcomplex genes, Tcp-1, D17Leh117c3, and D17Leh66, in purified murine spermatogenic cell populations. Genet Res 1990; 56:193-201.
44. Lalancette C, Faure RL, Leclerc P. Identification of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: a proteomic approach. Proteomics 2006; 6:4523-4540.
45. Meseguer M, de los Santos MJ, Simon C, Pellicer A, Remohi J, Garrido N. Effect of sperm glutathione peroxidases 1 and 4 on embryo asymmetry and blastocyst quality in oocyte donation cycles. Fertil Steril 2006; 86:1376-1385.
46. Ursini F, Maiorino M, Gregolin C. The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim Biophys Acta 1985; 839:62-70.
47. Ghyselinck NB, Dufaure JP. A mouse cDNA sequence for epididymal androgen-regulated proteins related to glutathione peroxidase. Nucleic Acids Res 1990; 18:7144.
48. McCarrey JR, Watson C, Atencio J, Ostermeier GC, Marahrens Y, Jaenisch R, Krawetz SA. X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse. Genesis 2002; 34:257-266.
49. Turner JM, Mahadevaiah SK, Elliott DJ, Garchon HJ, Pehrson JR, Jaenisch R, Burgoyne PS. Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist. J Cell Sci 2002; 115:4097-4105.
50. Huynh KD, Lee JT. Inheritance of a preinactivated paternal X chromosome in early mouse embryos. Nature 2003; 426:857-862.
51. Cosgrove DJ. New genes and new biological roles for expansins. Curr Opin Plant Biol 2000; 3:73-78.
52. Cosgrove DJ. Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Physiol Plant Mol Biol 1999; 50:391-417.
53. Jin Y, Tashpulatov AS, Katholnigg H, Heberle-Bors E, Touraev A. Isolation and characterization of two wheat beta-expansin genes expressed during male gametophyte development. Protoplasma 2006; 228:13-19.
54. Gatti JL, Castella S, Dacheux F, Ecroyd H, Metayer S, Thimon V, Dacheux JL. Posttesticular sperm environment and fertility. Anim Reprod Sci 2004;82-83:321-339.
55. Laux T, Jurgens G. Embryogenesis: a new start in life. Plant Cell 1997; 9:989-1000.
56. Wobus U, Weber H. Seed maturation: genetic programmes and control signals. Curr Opin Plant Biol 1999; 2:33-38.
57. Li Z, Thomas TL. PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 1998; 10:383-398.
58. McCarty DR. Genetic control and integration of maturation and germination pathways in seed development. Annu Rev Plant Physiol Plant Mol Biol 1995; 46:71-93.
59. Hoecker U, Vasil IK, McCarty DR. Integrated control of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize. Genes Dev 1995; 9:2459-2469.
60. Paek NC, Lee BM, Gyu Bai D, Smith JD. Inhibition of germination gene expression by Viviparous-1 and ABA during maize kernel development. Mol Cells 1998; 8:336-342.
61. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 2004; 26:509-515.
62. Dadoune JP, Pawlak A, Alfonsi MF, Siffroi JP. Identification of transcripts by macroarrays, RT-PCR, and in situ hybridization in human ejaculate spermatozoa. Mol Hum Reprod 2005; 11:133-140.
63. Lewis SE. Is sperm evaluation useful in predicting human fertility? Reproduction 2007; 134:31-40.