The MicroRNA Signature of Mouse Spermatozoa Is Substantially Modified During Epididymal Maturation

Biology of Reproduction

Volumn 93, Issue 4, 2015, Pages

  Nixon, Brett ^a   Stanger, Simone J ^a   Mihalas, Bettina P ^a   Reilly, Jackson N ^a   Anderson, Amanda L ^a   Tyagi, Sonika ^b   Holt, Janet E ^c   McLaughlin, Eileen A ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

AGO2; DICER1; Epididymis; Fertilization; Male reproductive tract; MicroRNA; miRNA; Next generation sequencing; Sperm; Sperm maturation; Spermatozoa

Indexed keywords

MICRORNA; ARGONAUTE PROTEIN; DEAD BOX PROTEIN; DICER1 PROTEIN, MOUSE; EIF2C2 PROTEIN, MOUSE; RIBONUCLEASE III;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; EPIDIDYMIS; EPIGENETICS; GENETIC TRANSCRIPTION; MALE; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; SPERMATOZOON; SPERMATOZOON MATURATION; TESTIS; ANIMAL; COMPUTER SIMULATION; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SPERMATOGENESIS;

ANIMALS; ARGONAUTE PROTEINS; COMPUTER SIMULATION; DEAD-BOX RNA HELICASES; EPIDIDYMIS; EPITHELIUM; GENE EXPRESSION REGULATION; MALE; MICE; MICRORNAS; RIBONUCLEASE III; SPERM MATURATION; SPERMATOGENESIS; SPERMATOZOA;

EID: 84943299699     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.132209     Document Type: Article

References (70)

1. Ambros V. The functions of animal microRNAs. Nature 2004; 431: 350-355.
2. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455:64-71.
3. Bouhallier F, Allioli N, Lavial F, Chalmel F, Perrard MH, Durand P, Samarut J, Pain B, Rouault JP. Role of miR-34c microRNA in the late steps of spermatogenesis. RNA 2010; 16:720-731.
4. He Z, Kokkinaki M, Pant D, Gallicano GI, Dym M. Small RNA molecules in the regulation of spermatogenesis. Reproduction 2009; 137:901-911.
5. Liu D, Li L, Fu H, Li S, Li J. Inactivation of Dicer1 has a severe cumulative impact on the formation of mature germ cells in mouse testes. Biochem Biophys Res Commun 2012; 422:114-120.
6. McIver SC, Roman SD, Nixon B, McLaughlin EA. miRNA and mammalian male germ cells. Hum Reprod Update 2012; 18:44-59.
7. McIver SC, Stanger SJ, Santarelli DM, Roman SD, Nixon B, McLaughlin EA. A unique combination of male germ cell miRNAs coordinates gonocyte differentiation. PLoS One 2012; 7:e35553.
8. Nicholls PK, Harrison CA, Walton KL, McLachlan RI, O'Donnell L, Stanton PG. Hormonal regulation of sertoli cell micro-RNAs at spermiation. Endocrinology 2011; 152:1670-1683.
9. Bjorkgren I, Gylling H, Turunen H, Huhtaniemi I, Strauss L, Poutanen M, Sipila P. Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane. FASEB J 2015; 29:433-442.
10. Bjorkgren I, Saastamoinen L, Krutskikh A, Huhtaniemi I, Poutanen M, Sipila P. Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling. PLoS One 2012; 7:e38457.
11. Bjorkgren I, Sipila P. The role of Dicer1 in the male reproductive tract. Asian J Androl 2015; 17:737-741.
12. Chu C, Zheng G, Hu S, Zhang J, Xie S, Ma W, Ni M, Tang C, Zhou L, Zhou Y, Liu M, Li Y, et al. Epididymal region-specific miRNA expression and DNA methylation and their roles in controlling gene expression in rats. PLoS One 2015; 10:e0124450.
13. Belleannee C, Calvo E, Thimon V, Cyr DG, Legare C, Garneau L, Sullivan R. Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoS One 2012; 7:e34996.
14. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007; 129:1401-1414.
15. Zhang J, Liu Q, Zhang W, Li J, Li Z, Tang Z, Li Y, Han C, Hall SH, Zhang Y. Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides. Acta Biochim Biophys Sin (Shanghai) 2010; 42:145-153.
16. Nixon B, Stanger SJ, Mihalas BP, Reilly J, Anderson AL, Dun MD, Tyagi S, Holt JE, McLaughlin EA. Next generation sequencing analysis reveals segmental patterns of microRNA expression in mouse epididymal epithelial cells. PLoS One 2015; 10:e0135605.
17. Jodar M, Selvaraju S, Sendler E, Diamond MP, Krawetz SA, Reproductive Medicine Network. The presence, role and clinical use of spermatozoal RNAs. Hum Reprod Update 2013; 19:604-624.
18. Lalancette C, Miller D, Li Y, Krawetz SA. Paternal contributions: new functional insights for spermatozoal RNA. J Cell Biochem 2008; 104: 1570-1579.
19. Peng H, Shi J, Zhang Y, Zhang H, Liao S, Li W, Lei L, Han C, Ning L, Cao Y, Zhou Q, Chen Q, et al. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res 2012; 22: 1609-1612.
20. Sendler E, Johnson GD, Mao S, Goodrich RJ, Diamond MP, Hauser R, Krawetz SA. Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res 2013; 41:4104-4117.
21. Krawetz SA, Kruger A, Lalancette C, Tagett R, Anton E, Draghici S, Diamond MP. A survey of small RNAs in human sperm. Hum Reprod 2011; 26:3401-3412.
22. Miller D, Briggs D, Snowden H, Hamlington J, Rollinson S, Lilford R, Krawetz SA. A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis. Gene 1999; 237:385-392.
23. Miller D, Ostermeier GC. Spermatozoal RNA: why is it there and what does it do? Gynecol Obstet Fertil 2006; 34:840-846.
24. Ostermeier GC, Goodrich RJ, Moldenhauer JS, Diamond MP, Krawetz SA. A suite of novel human spermatozoal RNAs. J Androl 2005; 26: 70-74.
25. Dadoune JP. Spermatozoal RNAs: what about their functions? Microsc Res Tech 2009; 72:536-551.
26. Liu WM, Pang RT, Chiu PC, Wong BP, Lao K, Lee KF, Yeung WS. Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc Natl Acad Sci U S A 2012; 109:490-494.
27. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA. Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 2004; 429:154.
28. Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 2013; 33:9003-9012.
29. McCallie B, Schoolcraft WB, Katz-Jaffe MG. Aberration of blastocyst microRNA expression is associated with human infertility. Fertil Steril 2010; 93:2374-2382.
30. Curry E, Safranski TJ, Pratt SL. Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 2011; 76:1532-1539.
31. Abu-Halima M, Hammadeh M, Backes C, Fischer U, Leidinger P, Lubbad AM, Keller A, Meese E. A panel of five microRNAs as potential biomarkers for the diagnosis and assessment of male infertility. Fertil Steril 2014; 102:989-997.
32. Tscherner A, Gilchrist G, Smith N, Blondin P, Gillis D, LaMarre J. MicroRNA-34 family expression in bovine gametes and preimplantation embryos. Reprod Biol Endocrinol 2014; 12:85.
33. Khazaie Y, Nasr Esfahani MH. MicroRNA and male infertility: a potential for diagnosis. Int J Fertil Steril 2014; 8:113-118.
34. Salas-Huetos A, Blanco J, Vidal F, Mercader JM, Garrido N, Anton E. New insights into the expression profile and function of micro-ribonucleic acid in human spermatozoa. Fertil Steril 2014; 102:213-222.e4.
35. Abu-Halima M, Hammadeh M, Schmitt J, Leidinger P, Keller A, Meese E, Backes C. Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil Steril 2013; 99:1249-1255. e16.
36. Hamatani T. Human spermatozoal RNAs. Fertil Steril 2012; 97:275-281.
37. Govindaraju A, Uzun A, Robertson L, Atli MO, Kaya A, Topper E, Crate EA, Padbury J, Perkins A, Memili E. Dynamics of microRNAs in bull spermatozoa. Reprod Biol Endocrinol 2012; 10:82.
38. Nixon B, MacIntyre DA, Mitchell LA, Gibbs GM, O'Bryan M, Aitken RJ. The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biol Reprod 2006; 74:275-287.
39. Dun MD, Anderson AL, Bromfield EG, Asquith KL, Emmett B, McLaughlin EA, Aitken RJ, Nixon B. Investigation of the expression and functional significance of the novel mouse sperm protein, a disintegrin and metalloprotease with thrombospondin type 1 motifs number 10 (ADAMTS10). Int J Androl 2012; 35:572-589.
40. Kruger TF, Ackerman SB, Simmons KF, Swanson RJ, Brugo SS, Acosta AA. A quick, reliable staining technique for human sperm morphology. Arch Androl 1987; 18:275-277.
41. Baleato RM, Aitken RJ, Roman SD. Vitamin A regulation of BMP4 expression in the male germ line. Dev Biol 2005; 286:78-90.
42. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002; 30:207-210.
43. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25:402-408.
44. Ma W, Hu S, Yao G, Xie S, Ni M, Liu Q, Gao X, Zhang J, Huang X, Zhang Y. An androgen receptor-microrna-29a regulatory circuitry in mouse epididymis. J Biol Chem 2013; 288:29369-29381.
45. Ma W, Xie S, Ni M, Huang X, Hu S, Liu Q, Liu A, Zhang J, Zhang Y. MicroRNA-29a inhibited epididymal epithelial cell proliferation by targeting nuclear autoantigenic sperm protein (NASP). J Biol Chem 2012; 287:10189-10199.
46. Li Y, Wang HY, Wan FC, Liu FJ, Liu J, Zhang N, Jin SH, Li JY. Deep sequencing analysis of small non-coding RNAs reveals the diversity of microRNAs and piRNAs in the human epididymis. Gene 2012; 497: 330-335.
47. Cortadellas N, Durfort M. Fate and composition of cytoplasmic droplet of hamster epididymal spermatozoa. J Morphol 1994; 221:199-210.
48. Sullivan R, Saez F, Girouard J, Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis 2005; 35:1-10.
49. Sullivan R, Saez F. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction 2013; 146:R21-R35.
50. Belleannee C, Calvo E, Caballero J, Sullivan R. Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol Reprod 2013; 89:30.
51. Lotvall J, Valadi H. Cell to cell signalling via exosomes through esRNA. Cell Adh Migr 2007; 1:156-158.
52. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigenpresenting cells. Nat Commun 2011; 2:282.
53. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9: 654-659.
54. Sullivan R, Frenette G, Girouard J. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 2007; 9:483-491.
55. Bachiller D, Schellander K, Peli J, Ruther U. Liposome-mediated DNA uptake by sperm cells. Mol Reprod Dev 1991; 30:194-200.
56. Cossetti C, Lugini L, Astrologo L, Saggio I, Fais S, Spadafora C. Soma-togermline transmission of RNA in mice xenografted with human tumour cells: possible transport by exosomes. PLoS One 2014; 9:e101629.
57. Aitken RJ, Nixon B, Lin M, Koppers AJ, Lee YH, Baker MA. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 2007; 9:554-564.
58. Schoysman R, Vanderzwalmen P, Nijs M, Segal L, Segal-Bertin G, Geerts L, van Roosendaal E, Schoysman D. Pregnancy after fertilisation with human testicular spermatozoa. Lancet 1993; 342:1237.
59. Schoysman R, Segal L, Van Der Zwalmen P, Nijs M, Bertin G, Cittadini E, Cimino C, Ruvolo G, Cefalu E, Palermo R. Assisted fertilization with epididymal spermatozoa. Acta Eur Fertil 1993; 24:7-12.
60. Schjenken JE, Robertson SA. Seminal fluid and immune adaptation for pregnancy-comparative biology in mammalian species. Reprod Domest Anim 2014; 49(suppl 3):27-36.
61. Smythies J, Edelstein L, Ramachandran V. Molecular mechanisms for the inheritance of acquired characteristics-exosomes, microRNA shuttling, fear and stress: Lamarck resurrected? Front Genet 2014; 5:133.
62. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, Mansuy IM. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 2014; 17: 667-669.
63. Colas AR, McKeithan WL, Cunningham TJ, Bushway PJ, Garmire LX, Duester G, Subramaniam S, Mercola M. Whole-genome microRNA screening identifies let-7 and mir-18 as regulators of germ layer formation during early embryogenesis. Genes Dev 2012; 26:2567-2579.
64. Torchinsky A, Toder V. To die or not to die: the function of the transcription factor NF-kappaB in embryos exposed to stress. Am J Reprod Immunol 2004; 51:138-143.
65. Schjenken JE, Glynn DJ, Sharkey DJ, Robertson SA. TLR4 signaling is a major mediator of the female tract response to seminal fluid in mice. Biol Reprod 2015; 93:68.
66. Fullston T, Ohlsson Teague EM, Palmer NO, DeBlasio MJ, Mitchell M, Corbett M, Print CG, Owens JA, Lane M. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 2013; 27:4226-4243.
67. Stowe HM, Calcatera SM, Dimmick MA, Andrae JG, Duckett SK, Pratt SL. The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression. PLoS One 2014; 9:e113163.
68. Marczylo EL, Amoako AA, Konje JC, Gant TW, Marczylo TH. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 2012; 7:432-439.
69. Palmer NO, Bakos HW, Fullston T, Lane M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2012; 2:253-263.
70. Belleannee C, Legare C, Calvo E, Thimon V, Sullivan R. microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum Reprod 2013; 28:1455-1467.