Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Reilly, Jackson N ^a   McLaughlin, Eileen A ^a,b   Stanger, Simone J ^a   Anderson, Amanda L ^a   Hutcheon, Kate ^a   Church, Kiralee ^a   Mihalas, Bettina P ^a   Tyagi, Sonika ^c   Holt, Janet E ^d   Eamens, Andrew L ^a   Nixon, Brett ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c Australian Genome Research Facility Ltd   (Australia)

^d UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

ANIMAL; BIOLOGY; CLUSTER ANALYSIS; EPIDIDYMIS; GENETICS; MALE; MALE GENITAL SYSTEM; METABOLISM; MOUSE; SOFTWARE; SPERMATOZOON; SPERMATOZOON MATURATION;

ANIMALS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EPIDIDYMIS; GENITALIA, MALE; MALE; MICE; MICRORNAS; SOFTWARE; SPERM MATURATION; SPERMATOZOA;

EID: 84984645299     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep31794     Document Type: Article

References (64)

1. Hermo, L., Pelletier, R. M., Cyr, D. G. and Smith, C. E. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: Background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech 73, 241-278, doi: 10.1002/jemt.20783 (2010).
2. Cornwall, G. A. New insights into epididymal biology and function. Hum Reprod Update 15, 213-227, doi: 10.1093/humupd/dmn055 (2009).
3. Robaire, B., Hinton, B. T. and Orgebin-Crist, M. C. In Knobil and Neills Physiology of Reproduction, 3rd Edition (ed. J. D. Neill) Ch. 22, 1071-1148 (Elsevier, 2006).
4. Dacheux, J. L., Dacheux, F. and Druart, X. Epididymal protein markers and fertility. Anim Reprod Sci, doi: 10.1016/j.anireprosci.2016.02.034 (2016).
5. Sullivan, R. and Saez, F. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction 146, R21-R35, doi: 10.1530/rep-13-0058 (2013).
6. Sullivan, R. Epididymosomes: a heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian J Androl 17, 726-729, doi: 10.4103/1008-682X.155255 (2015).
7. Martin-DeLeon, P. A. Epididymosomes: transfer of fertility-modulating proteins to the sperm surface. Asian J Androl 17, 720-725, doi: 10.4103/1008-682x.155538 (2015).
8. Martin-DeLeon, P. A. Epididymal SPAM1 and its impact on sperm function. Mol Cell Endocrinol 250, 114-121, doi: 10.1016/j. mce.2005.12.033 (2006).
9. Rejraji, H. et al. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod 74, 1104-1113, doi: 10.1095/biolreprod.105.049304 (2006).
10. Girouard, J., Frenette, G. and Sullivan, R. Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int J Androl 34, e475-e486, doi: 10.1111/j.1365-2605.2011.01203.x (2011).
11. Belleannee, C., Calvo, E., Caballero, J. and Sullivan, R. Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol Reprod 89, 30, doi: 10.1095/biolreprod.113.110486 (2013).
12. Sharma, U. et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351, 391-396, doi: 10.1126/science.aad6780 (2016).
13. Smythies, J., Edelstein, L. and Ramachandran, V. Molecular mechanisms for the inheritance of acquired characteristics-exosomes, microRNA shuttling, fear and stress: Lamarck resurrected? Front Genet 5, 133, doi: 10.3389/fgene.2014.00133 (2014).
14. Eaton, S. A. et al. Roll over Weismann: extracellular vesicles in the transgenerational transmission of environmental effects. Epigenomics 7, 1165-1171, doi: 10.2217/epi.15.58 (2015).
15. Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S. and Bale, T. L. 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 (2013).
16. Rodgers, A. B., Morgan, C. P., Leu, N. A. and Bale, T. L. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA 112, 13699-13704, doi: 10.1073/pnas.1508347112 (2015).
17. Fullston, T. et al. 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 27, 4226-4243, doi: 10.1096/fj.12- 224048 (2013).
18. Chen, Q. et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351, 397-400, doi: 10.1126/science.aad7977 (2016).
19. Marczylo, E. L., Amoako, A. A., Konje, J. C., Gant, T. W. and Marczylo, T. H. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7, 432-439, doi: 10.4161/epi.19794 (2012).
20. Bale, T. L. Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci 16, 332-344, doi: 10.1038/nrn3818 (2015).
21. Hermo, L., Pelletier, R. M., Cyr, D. G. and Smith, C. E. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech 73, 241-278, doi: 10.1002/jemt.20783 (2010).
22. Nixon, B. et al. The microRNA signature of mouse spermatozoa is substantially modified during epididymal maturation. Biol Reprod, doi: 10.1095/biolreprod.115.132209 (2015).
23. Colombo, M., Raposo, G. and Thery, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 30, 255-289, doi: 10.1146/annurev-cellbio-101512-122326 (2014).
24. Raposo, G. and Stoorvogel, W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200, 373-383, doi: 10.1083/jcb.201211138 (2013).
25. Fischer, K. A. et al. 15-Lipoxygenase is a component of the mammalian sperm cytoplasmic droplet. Reproduction 130, 213-222, doi: 10.1530/rep.1.00646 (2005).
26. Nixon, B. et al. Next generation sequencing analysis reveals segmental patterns of microRNA expression in mouse epididymal epithelial cells. PLoS One 10, e0135605, doi: 10.1371/journal.pone.0135605 (2015)
27. Frenette, G., Lessard, C. and Sullivan, R. Selected proteins of "prostasome-like particles" from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 67, 308-313, 10.1095/biolreprod67.1.308 (2002).
28. Bjorkgren, I. et al. Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling. PLoS One 7, e38457, doi: 10.1371/journal.pone.0038457 (2012).
29. Bjorkgren, I. et al. Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane. FASEB J 29, 433-442, doi: 10.1096/fj.14-259382 (2015).
30. Belleannee, C. et al. Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoS One 7, e34996, doi: 10.1371/journal.pone.0034996 (2012).
31. Frenette, G., Girouard, J. and Sullivan, R. Comparison between epididymosomes collected in the intraluminal compartment of the bovine caput and cauda epididymidis. Biol Reprod 75, 885-890, doi: 10.1095/biolreprod.106.054692 (2006).
32. Frenette, G. et al. Characterization of two distinct populations of epididymosomes collected in the intraluminal compartment of the bovine cauda epididymis. Biol Reprod 83, 473-480, doi: 10.1095/biolreprod.109.082438 (2010).
33. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654-659, doi: 10.1038/ncb1596 (2007).
34. Thery, C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 3, 15, doi: 10.3410/B3-15 (2011).
35. Lee, Y., El Andaloussi, S. and Wood, M. J. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21, R125-R134, doi: 10.1093/hmg/dds317 (2012).
36. Li, C. C. et al. Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol 10, 1333-1344, doi: 10.4161/rna.25281 (2013).
37. Villarroya-Beltri, C. et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4, 2980, doi: 10.1038/ncomms3980 (2013).
38. Guduric-Fuchs, J. et al. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics 13, 357, doi: 10.1186/1471-2164-13-357 (2012).
39. Aitken, R. J. et al. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 9, 554-564, doi: 10.1111/j.1745-7262.2007.00280.x (2007).
40. Yuan, S. et al. Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development 143, 635-647, doi: 10.1242/dev.131755 (2016).
41. Al-Dossary, A. A., Bathala, P., Caplan, J. L. and Martin-DeLeon, P. A. Oviductosome-Sperm Membrane interaction in cargo delivery: Detection of fusion and underlying molecular players using three-dimensional super-resolution structured illumination microscopy (SR-SIM). J Biol Chem 290, 17710-17723, doi: 10.1074/jbc.M114.633156 (2015).
42. Machtinger, R., Laurent, L. C. and Baccarelli, A. A. Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum Reprod Update 22, 182-193, doi: 10.1093/humupd/dmv055 (2016).
43. DAmours, O. et al. Epididymosomes transfer epididymal sperm binding protein 1 (ELSPBP1) to dead spermatozoa during epididymal transit in bovine. Biol Reprod 87, 94, doi: 10.1095/biolreprod.112.100990 (2012).
44. Lane, M., Robker, R. L. and Robertson, S. A. Parenting from before conception. Science 345, 756-760, doi: 10.1126/science.1254400 (2014).
45. Belleannee, C., Legare, C., Calvo, E., Thimon, V. and Sullivan, R. microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum Reprod 28, 1455-1467, doi: 10.1093/humrep/det088 (2013).
46. Palmer, N. O., Bakos, H. W., Fullston, T. and Lane, M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2, 253-263, doi: 10.4161/spmg.21362 (2012).
47. Cossetti, C. et al. Soma-to-germline transmission of RNA in mice xenografted with human tumour cells: possible transport by exosomes. PLoS One 9, e101629, doi: 10.1371/journal.pone.0101629 (2014).
48. Thery, C., Zitvogel, L. and Amigorena, S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2, 569-579, doi: 10.1038/nri855 (2002).
49. Johnston, D. S. et al. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod 73, 404-413, doi: 10.1095/biolreprod.105.039719 (2005).
50. Sharkey, D. J., Schjenken, J. E., Mottershead, D. G. and Robertson, S. A. Seminal fluid factors regulate activin A and follistatin synthesis in female cervical epithelial cells. Mol Cell Endocrinol 417, 178-190, doi: 10.1016/j.mce.2015.09.022 (2015).
51. Schjenken, J. E. and Robertson, S. A. Seminal Fluid Signalling in the Female Reproductive Tract: Implications for Reproductive Success and Offspring Health. Adv Exp Med Biol 868, 127-158, doi: 10.1007/978-3-319-18881-2-6 (2015).
52. Biggers, J. D., Whitten, W. K. and Whittingham, D. G. In Methods in Mammalian Embryology (ed. J. C. Daniel) 86-116 (Freeman Press, 1971).
53. Anderson, A. L. et al. Assessment of microRNA expression in mouse epididymal epithelial cells and spermatozoa by next generation sequencing. Genom Data 6, 208-211, doi: 10.1016/j.gdata.2015.09.012 (2015).
54. Thery, C., Amigorena, S., Raposo, G. and Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3, Unit 3 22, doi: 10.1002/0471143030.cb0322s30 (2006).
55. Tauro, B. J. et al. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods 56, 293-304, doi: 10.1016/j.ymeth.2012.01.002 (2012).
56. Hermo, L., Dworkin, J. and Oko, R. Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat 183, 107-124, doi: 10.1002/aja.1001830202 (1988).
57. Reid, A. T. et al. Glycogen synthase kinase 3 regulates acrosomal exocytosis in mouse spermatozoa via dynamin phosphorylation. FASEB J 29, 2872-2882, doi: 10.1096/fj.14-265553 (2015).
58. Principe, S. et al. In-depth proteomic analyses of exosomes isolated from expressed prostatic secretions in urine. Proteomics 13, 1667-1671, doi: 10.1002/pmic.201200561 (2013).
59. Ng, Y. H. et al. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One 8, e58502, doi: 10.1371/journal.pone.0058502 (2013).
60. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10-12, doi: 10.14806/ej.17.1.200 (2011).
61. Friedlander, M. R. et al. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26, 407-415, doi: 10.1038/nbt1394 (2008).
62. McCarthy, D. J., Chen, Y. and Smyth, G. K. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40, 4288-4297, doi: 10.1093/nar/gks042 (2012).
63. Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43, e47, doi: 10.1093/nar/gkv007 (2015).
64. Schmittgen, T. D. and Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3, 1101-1108, doi: 10.1038/nprot.2008.73 (2008).