The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Stowe, Heather M ^a   Calcatera, Samantha M ^a   Dimmick, Marcy A ^a   Andrae, John G ^a   Duckett, Susan K ^a   Pratt, Scott L ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 146; MICRORNA 146A; MICRORNA 335; PHOSPHATASE; PHOSPHOTRANSFERASE; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANGUS CATTLE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; ENVIRONMENTAL CHANGE; ENZYME ACTIVITY; FESCUE TOXICOSIS; GENE CLUSTER; GENE DOSAGE; GENE EXPRESSION; GENE MAPPING; GENOME; INTOXICATION; MALE; MEIOSIS; MICROARRAY ANALYSIS; NONHUMAN; OOCYTE; RNA ISOLATION; RNA SEQUENCE; SPERM; SPERMATOGENESIS; TRANSCRIPTION REGULATION; UPREGULATION; WNT SIGNALING PATHWAY; ZYGOTE; ANIMAL; ANIMAL HUSBANDRY; BIOSYNTHESIS; BOVINE; CATTLE DISEASES; DRUG EFFECTS; FESCUE; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; NEOTYPHODIUM; PATHOGENICITY; PATHOLOGY; PROCEDURES; REPRODUCTION; SEQUENCE ANALYSIS; SPERMATOZOON; TOXICITY;

ANIMAL HUSBANDRY; ANIMALS; CATTLE; CATTLE DISEASES; DATABASES, GENETIC; FESTUCA; GENE EXPRESSION REGULATION; MALE; MICRORNAS; NEOTYPHODIUM; REPRODUCTION; SEQUENCE ANALYSIS, RNA; SPERMATOZOA;

EID: 84914689291     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113163     Document Type: Article

References (46)

1. Bacon CW (1995) Toxic endophyte-infected tall fescue and range grasses: historic perspectives. J Anim Sci 73: 861-870.
2. Belesky D, West C (2009) Abiotic Stresses and Endophyte Effects. In: Fribourg H, Hannaway D, West C, editors. Tall Fescue for the Twenty-first Century. Madison, WI: ASA, CSSA, and SSSA. pp. 49-66.
3. Porter JK, Thompson FN (1992) Effects of fescue toxicosis on reproduction in livestock. J Anim Sci 70: 1594-1603.
4. Strickland JR, Looper ML, Matthews JC, Rosenkrans CF, Flythe MD, et al. (2011) Board-invited review: St. Anthony's Fire in livestock: causes, mechanisms, and potential solutions. J Anim Sci 89: 1603-1626. doi: 10.2527/jas.2010-3478.
5. Hoveland CS (1993) Importance and economic significance of the Acremonium endophytes to performance of animals and grass plant. Agric Ecosyst Environ 44: 3-12. doi: 10.1016/0167-8809(93)90036-O.
6. Allen VG, Segarra E (2001) Anti-quality components in forage: Overview, significance, and economic impact. J Range Manag 54: 409-412.
7. Boling JA (1985) Endophytic fungus and tall fescue utilization by ruminants. Prof Anim Sci 1.
8. Schmidt SP, Danilson DA, Holliman JA, Grimes HW, Wegbster WB (1986) Fescue fungus suppresses growth and reproduction in replacement beef heifers. Highlights Agric Res 3315 Alabama Agric Exp Sta, Auburn Univ, Auburn.
9. Beers KW, Piper EL (1987) Effects of grazing endophyte infected fescue on heifers growth, calving rate and calf birth weight of first calf heifers. Arkansas Farm Res 36.
10. Gay N, Boling JA, Dew R, Miksch DE (1988) Effects of endophyte-infected tall fescue on beef cow-calf performance. Appl Agric Res 3.
11. Washburn SP, Green JT Jr (1991) Performance of replacement beef heifers on endophyte-infected fescue pastures. Proc 40th Annu Conf North Carolina Cattlemen's Assoc February 2.
12. Evans KL, Zavos PM, Hemken RW, Jackson JA (1988) Effects of feeding endophyte-infected (Acremonium coeno- phialum) KY-31 fescue hay on the reproductive development of Holstein bulls. Theriogenology 30: 169-179. doi: 10.1016/0093-691X(88)90274-9.
13. Schuenemann GM, Edwards JL, Hopkins FM, Rohrbach NR, Adair HS, et al. (2005) Fertility aspects in yearling beef bulls grazing endophyte-infected tall fescue pastures. Reprod Fertil Dev 17: 479-486.
14. Jones KL, McCleary CR, King SS, Apgar GA, Griswold KE (2004) CASE STUDY: Consumption of Toxic Fescue Impairs Bull Reproductive Parameters. Prof Anim Sci 20: 437-442.
15. Looper ML, Rorie RW, Person CN, Lester TD, Hallford DM, et al. (2009) Influence of toxic endophyte-infected fescue on sperm characteristics and endocrine factors of yearling Brahman-influenced bulls. J Anim Sci 87: 1184-1191. doi: 10.2527/jas.2008-1258.
16. Schuenemann GM, Edwards JL, Davis MD, Blackmon HE, Scenna FN, et al. (2005) Effects of administration of ergotamine tartrate on fertility of yearling beef bulls. Theriogenology 63: 1407-1418. doi: 10.1016/j.theriogenology.2004.07.014.
17. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA (2004) Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429: 154. doi: 10.1038/429154a.
18. Liu W, Pang RTK, Chiu PCN, Wong BPC, Lao K, et al. (2012) Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Pnas 109: 490-494. doi: 10.1073/pnas.1110368109.
19. Sayed D, Abdellatif M (2011) MicroRNAs in development and disease. Physiol Rev 91: 827-887. doi: 10.1152/physrev.00006.2010.
20. Tong M-H, Mitchell DA, McGowan SD, Evanoff R, Griswold MD (2012) Two miRNA clusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of spermatogonial differentiation in mice. Biol Reprod 86: 72. doi: 10.1095/biolreprod.111.096313.
21. He Z, Kokkinaki M, Pant D, Gallicano GI, Dym M (2009) Small RNA molecules in the regulation of spermatogenesis. Reproduction 137: 901-911. doi: 10.1530/REP-08-0494.
22. McIver SC, Roman SD, Nixon B, McLaughlin EA (2011) miRNA and mammalian male germ cells. Hum Reprod Update 18: 44-59. doi: 10.1093/humupd/dmr041.
23. Govindaraju A, Uzun A, Robertson L, Atli MO, Kaya A, et al. (2012) Dynamics of microRNAs in bull spermatozoa. Reprod Biol Endocrinol 10: 82. doi: 10.1186/1477-7827-10-82.
24. Stowe H, Miller M, Burns M, Calcatera S, Andrae J, et al. (2013) Effects of fescue toxicosis on bull growth, semen characteristics, and breeding soundness evaluation. J Anim Sci 91: 3686-3692. doi: 10.2527/jas2012-6078.
25. Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, et al. (2008) Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18: 610-621. doi: 10.1101/gr.7179508.
26. Lee LW, Zhang SZ, Etheridge A, Ma L, Martin D, et al. (2010) Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA 16: 2170-2180. doi: 10.1261/rna.2225110.preferentially.
27. Cloonan N, Wani S, Xu Q, Gu J, Lea K, et al. (2011) MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol 12: R126. doi: 10.1186/gb-2011-12-12-r126.
28. Guo L, Li H, Liang T, Lu J, Yang Q, et al. (2012) Consistent isomiR expression patterns and 39 addition events in miRNA gene clusters and families implicate functional and evolutionary relationships. Mol Biol Rep 39: 6699-6706. doi: 10.1007/s11033-012-1493-3.
29. Abu-Halima M, Hammadeh M, Schmitt J, Leidinger P, Keller A, et al. (2013) Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil Steril 99: 1249-1255.e16. doi: 10.1016/j.fertnstert.2012.11.054.
30. Curry E, Safranski TJ, Pratt SL (2011) Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76: 1532-1539. doi: 10.1016/j.theriogenology.2011.06.025.
31. Huszar JM, Payne CJ (2013) MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice. Biol Reprod 88: 15. doi: 10.1095/biolreprod.112.103747.
32. Tong M-H, Mitchell D, Evanoff R, Griswold MD (2011) Expression of Mirlet7 family microRNAs in response to retinoic acid-induced spermatogonial differentiation in mice. Biol Reprod 85: 189-197. doi: 10.1095/biolreprod.110.089458.
33. Niu Z, Goodyear SM, Rao S, Wu X, Tobias JW, et al. (2011) MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. PNAS 108: 12740-12745. doi: 10.1073/pnas.1109987108/2/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1109987108.
34. Linsley PS, Schelter J, Burchard J, Kibukawa M, Martin MM, et al. (2007) Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 27: 2240-2252. doi: 10.1128/MCB.02005-06.
35. Kocamis H, Hossain M, Cinar MU, Salilew-Wondim D, Mohammadi-Sangcheshmeh A, et al. (2013) Expression of microRNA and microRNA processing machinery genes during early quail (Coturnix japonica) embryo development. Poult Sci 92: 787-797.
36. Liu W-M, Pang RTK, Cheong AWY, Ng EHY, Lao K, et al. (2012) Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice. PLoS One 7: e37039. doi: 10.1371/journal.pone.0037039.
37. Wang J, Cao N, Yuan M, Cui H, Tang Y, et al. (2012) MicroRNA-125b/Lin28 pathway contributes to the mesendodermal fate decision of embryonic stem cells. Stem Cells Dev 21: 1524-1537. doi: 10.1089/scd.2011.0350.
38. Huang K, Fu J, Zhou W, Li W, Dong S, et al. (2014) MicroRNA-125b regulates osteogenic differentiation of mesenchymal stem cells by targeting Cbfb in vitro. Biochimie doi: 10.10. doi: 10.1016.
39. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-7. doi: 10.1093/nar/gkq1027.
40. Cui X-S, Sun S-C, Kang Y-K, Kim N-H (2013) Involvement of microRNA-335-5p in cytoskeleton dynamics in mouse oocytes. Reprod Fertil Dev 25: 691-699. doi: 10.1071/RD12138.
41. Leung AKL, Sharp PA (2010) MicroRNA Functions in Stress Responses. Mol Cell 40: 205-215. doi: 10.1016/j.molcel.2010.09.027.MicroRNA.
42. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, et al. (2009) MicroRNA-125b is a novel negative regulator of p53. Genes Dev 23: 862-876.
43. Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL (2013) Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 33: 9003-9012. doi: 10.1523/JNEUROSCI.0914-13.2013.
44. Grandjean V, Gounon P, Wagner N, Martin L, Wagner KD, et al. (2009) The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136: 3647-3655. doi: 10.1242/dev.041061.
45. Curry E, Ellis SE, Pratt SL (2009) Detection of porcine sperm microRNAs using a heterologous microRNA microarray and reverse transcriptase polymerase chain reaction. Mol Reprod Dev 76: 218-219. doi: 10.1002/mrd.20980.
46. Krawetz SA, Kruger A, Lalancette C, Tagett R, Anton E, et al. (2011) A survey of small RNAs in human sperm. Hum Reprod 26: 3401-3412. doi: 10.1093/humrep/der329.