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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

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Front. Med.    2022, Vol. 16 Issue (2) : 176-184    https://doi.org/10.1007/s11684-021-0885-y
REVIEW
Paternal environmental exposure-induced spermatozoal small noncoding RNA alteration meditates the intergenerational epigenetic inheritance of multiple diseases
Xin Yin, Azhar Anwar, Yanbo Wang, Huanhuan Hu, Gaoli Liang, Chenyu Zhang()
Nanjing Drum Tower Hospital Center of Molecular Diagnostic and Therapy, State Key Laboratory of Pharmaceutical Biotechnology and Department of Physiology, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, NJU Advanced Institute of Life Sciences (NAILS), School of Life Sciences, Nanjing University, Nanjing 210023, China
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Abstract

Studies of human and mammalian have revealed that environmental exposure can affect paternal health conditions as well as those of the offspring. However, studies that explore the mechanisms that meditate this transmission are rare. Recently, small noncoding RNAs (sncRNAs) in sperm have seemed crucial to this transmission due to their alteration in sperm in response to environmental exposure, and the methodology of microinjection of isolated total RNA or sncRNAs or synthetically identified sncRNAs gradually lifted the veil of sncRNA regulation during intergenerational inheritance along the male line. Hence, by reviewing relevant literature, this study intends to answer the following research concepts: (1) paternal environmental factors that can be passed on to offspring and are attributed to spermatozoal sncRNAs, (2) potential role of paternal spermatozoal sncRNAs during the intergenerational inheritance process, and (3) the potential mechanism by which spermatozoal sncRNAs meditate intergenerational inheritance. In summary, increased attention highlights the hidden wonder of spermatozoal sncRNAs during intergenerational inheritance. Therefore, in the future, more studies should focus on the origin of RNA alteration, the target of RNA regulation, and how sncRNA regulation during embryonic development can be sustained even in adult offspring.
Keywords small noncoding RNAs      epigenetic inheritance      paternal intergenerational inherence      extracellular vesicles     
Corresponding Author(s): Chenyu Zhang   
About author:

Mingsheng Sun and Mingxiao Yang contributed equally to this work.
Just Accepted Date: 11 August 2021   Online First Date: 14 September 2021    Issue Date: 26 April 2022
 Cite this article:   
Xin Yin,Azhar Anwar,Yanbo Wang, et al. Paternal environmental exposure-induced spermatozoal small noncoding RNA alteration meditates the intergenerational epigenetic inheritance of multiple diseases[J]. Front. Med., 2022, 16(2): 176-184.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-021-0885-y
https://academic.hep.com.cn/fmd/EN/Y2022/V16/I2/176
Fig.1  Schematic of the potential mechanism of how environmental stress information molecules are transferred into the male reproductive system via extracellular vesicles.
1 Y Zhang, J Shi, M Rassoulzadegan, F Tuorto, Q Chen. Sperm RNA code programmes the metabolic health of offspring. Nat Rev Endocrinol 2019; 15(8): 489–498
https://doi.org/10.1038/s41574-019-0226-2 pmid: 31235802
2 OJ Rando. Intergenerational transfer of epigenetic information in sperm. Cold Spring Harb Perspect Med 2016; 6(5): a022988
https://doi.org/10.1101/cshperspect.a022988 pmid: 26801897
3 K Weigmann. Lifestyle in the sperm: there is growing evidence that epigenetic marks can be inherited. But what is the nature of the information they store and over how many generations do they prevail? EMBO Rep 2014; 15(12): 1233–1237
https://doi.org/10.15252/embr.201439759 pmid: 25381662
4 VM Sales, AC Ferguson-Smith, ME Patti. Epigenetic mechanisms of transmission of metabolic disease across generations. Cell Metab 2017; 25(3): 559–571
https://doi.org/10.1016/j.cmet.2017.02.016 pmid: 28273478
5 LK Klastrup, ST Bak, AL Nielsen. The influence of paternal diet on sncRNA-mediated epigenetic inheritance. Mol Genet Genomics 2019; 294(1): 1–11
https://doi.org/10.1007/s00438-018-1492-8 pmid: 30229293
6 AB Rodgers, CP Morgan, NA Leu, TL Bale. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA 2015; 112(44): 13699–13704
https://doi.org/10.1073/pnas.1508347112 pmid: 26483456
7 K Gapp, A Jawaid, P Sarkies, J Bohacek, P Pelczar, J Prados, L Farinelli, E Miska, IM Mansuy. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 2014; 17(5): 667–669
https://doi.org/10.1038/nn.3695 pmid: 24728267
8 Q Chen, M Yan, Z Cao, X Li, Y Zhang, J Shi, GH Feng, H Peng, X Zhang, Y Zhang, J Qian, E Duan, Q Zhai, Q Zhou. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 2016; 351(6271): 397–400
https://doi.org/10.1126/science.aad7977 pmid: 26721680
9 U Sharma, CC Conine, JM Shea, A Boskovic, AG Derr, XY Bing, C Belleannee, A Kucukural, RW Serra, F Sun, L Song, BR Carone, EP Ricci, XZ Li, L Fauquier, MJ Moore, R Sullivan, CC Mello, M Garber, OJ Rando. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 2016; 351(6271): 391–396
https://doi.org/10.1126/science.aad6780 pmid: 26721685
10 V Grandjean, S Fourré, DA De Abreu, MA Derieppe, JJ Remy, M Rassoulzadegan. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci Rep 2016; 5: 18193
https://doi.org/10.1038/srep18193 pmid: 26658372
11 D Vågerö, PR Pinger, V Aronsson, GJ van den Berg. Paternal grandfather’s access to food predicts all-cause and cancer mortality in grandsons. Nat Commun 2018; 9(1): 5124
https://doi.org/10.1038/s41467-018-07617-9 pmid: 30538239
12 LH Lumey, AD Stein, HS Kahn, KM van der Pal-de Bruin, GJ Blauw, PA Zybert, ES Susser. Cohort profile: the Dutch Hunger Winter families study. Int J Epidemiol 2007; 36(6): 1196–1204
https://doi.org/10.1093/ije/dym126 pmid: 17591638
13 LO Bygren, G Kaati, S Edvinsson. Longevity determined by paternal ancestors’ nutrition during their slow growth period. Acta Biotheor 2001; 49(1): 53–59
https://doi.org/10.1023/A:1010241825519 pmid: 11368478
14 ME Pembrey. Male-line transgenerational responses in humans. Hum Fertil (Camb) 2010; 13(4): 268–271
https://doi.org/10.3109/14647273.2010.524721 pmid: 21117937
15 G Kaati, LO Bygren, S Edvinsson. Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur J Hum Genet 2002; 10(11): 682–688
https://doi.org/10.1038/sj.ejhg.5200859 pmid: 12404098
16 ME Pembrey, LO Bygren, G Kaati, S Edvinsson, K Northstone, M Sjöström, JA; LSPAC Study Team Golding. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 2006; 14(2): 159–166
https://doi.org/10.1038/sj.ejhg.5201538 pmid: 16391557
17 TH Chen, YH Chiu, BJ Boucher. Transgenerational effects of betel-quid chewing on the development of the metabolic syndrome in the Keelung Community-based Integrated Screening Program. Am J Clin Nutr 2006; 83(3): 688–692
https://doi.org/10.1093/ajcn.83.3.688 pmid: 16522918
18 K Northstone, J Golding, G Davey Smith, LL Miller, M Pembrey. Prepubertal start of father’s smoking and increased body fat in his sons: further characterisation of paternal transgenerational responses. Eur J Hum Genet 2014; 22(12): 1382–1386
https://doi.org/10.1038/ejhg.2014.31 pmid: 24690679
19 R Yehuda, NP Daskalakis, A Lehrner, F Desarnaud, HN Bader, I Makotkine, JD Flory, LM Bierer, MJ Meaney. Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. Am J Psychiatry 2014; 171(8): 872–880
https://doi.org/10.1176/appi.ajp.2014.13121571 pmid: 24832930
20 EL Marczylo, AA Amoako, JC Konje, TW Gant, TH Marczylo. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 2012; 7(5): 432–439
https://doi.org/10.4161/epi.19794 pmid: 22441141
21 G Delbès, BF Hales, B Robaire. Toxicants and human sperm chromatin integrity. Mol Hum Reprod 2010; 16(1): 14–22
https://doi.org/10.1093/molehr/gap087 pmid: 19812089
22 DM Ruden, MD Garfinkel, VE Sollars, X Lu. Waddington’s widget: Hsp90 and the inheritance of acquired characters. Semin Cell Dev Biol 2003; 14(5): 301–310
https://doi.org/10.1016/j.semcdb.2003.09.024 pmid: 14986860
23 M Ptashne. Epigenetics: core misconcept. Proc Natl Acad Sci USA 2013; 110(18): 7101–7103
https://doi.org/10.1073/pnas.1305399110 pmid: 23584020
24 BJ Boucher, SW Ewen, JM Stowers. Betel nut (Areca catechu) consumption and the induction of glucose intolerance in adult CD1 mice and in their F1 and F2 offspring. Diabetologia 1994; 37(1): 49–55
https://doi.org/10.1007/BF00428777 pmid: 8150230
25 M Rassoulzadegan, V Grandjean, P Gounon, S Vincent, I Gillot, F Cuzin. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 2006; 441(7092): 469–474
https://doi.org/10.1038/nature04674 pmid: 16724059
26 EL Greer, TJ Maures, AG Hauswirth, EM Green, DS Leeman, GS Maro, S Han, MR Banko, O Gozani, A Brunet. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 2010; 466(7304): 383–387
https://doi.org/10.1038/nature09195 pmid: 20555324
27 SL Berger. Transgenerational inheritance of longevity: epigenetic mysteries abound. Cell Metab 2012; 15(1): 6–7
https://doi.org/10.1016/j.cmet.2011.12.012 pmid: 22225870
28 BG Dias, KJ Ressler. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 2014; 17(1): 89–96
https://doi.org/10.1038/nn.3594 pmid: 24292232
29 E Benito, C Kerimoglu, B Ramachandran, T Pena-Centeno, G Jain, RM Stilling, MR Islam, V Capece, Q Zhou, D Edbauer, C Dean, A Fischer. RNA-dependent intergenerational inheritance of enhanced synaptic plasticity after environmental enrichment. Cell Rep 2018; 23(2): 546–554
https://doi.org/10.1016/j.celrep.2018.03.059 pmid: 29642011
30 K Gapp, S Soldado-Magraner, M Alvarez-Sánchez, J Bohacek, G Vernaz, H Shu, TB Franklin, D Wolfer, IM Mansuy. Early life stress in fathers improves behavioural flexibility in their offspring. Nat Commun 2014; 5(1): 5466
https://doi.org/10.1038/ncomms6466 pmid: 25405779
31 L Wu, Y Lu, Y Jiao, B Liu, S Li, Y Li, F Xing, D Chen, X Liu, J Zhao, X Xiong, Y Gu, J Lu, X Chen, X Li. Paternal psychological stress reprograms hepatic gluconeogenesis in offspring. Cell Metab 2016; 23(4): 735–743
https://doi.org/10.1016/j.cmet.2016.01.014 pmid: 26908462
32 A Schuster, MK Skinner, W Yan. Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs. Environ Epigenet 2016; 2(1): dvw001
https://doi.org/10.1093/eep/dvw001 pmid: 27390623
33 GR Rompala, A Mounier, CM Wolfe, Q Lin, I Lefterov, GE Homanics. Heavy chronic intermittent ethanol exposure alters small noncoding RNAs in mouse sperm and epididymosomes. Front Genet 2018; 9: 32
https://doi.org/10.3389/fgene.2018.00032 pmid: 29472946
34 KD Wagner, N Wagner, H Ghanbarian, V Grandjean, P Gounon, F Cuzin, M Rassoulzadegan. RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell 2008; 14(6): 962–969
https://doi.org/10.1016/j.devcel.2008.03.009 pmid: 18539123
35 V Grandjean, P Gounon, N Wagner, L Martin, KD Wagner, F Bernex, F Cuzin, M Rassoulzadegan. The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 2009; 136(21): 3647–3655
https://doi.org/10.1242/dev.041061 pmid: 19820183
36 D Holoch, D Moazed. RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 2015; 16(2): 71–84
https://doi.org/10.1038/nrg3863 pmid: 25554358
37 BR Carone, L Fauquier, N Habib, JM Shea, CE Hart, R Li, C Bock, C Li, H Gu, PD Zamore, A Meissner, Z Weng, HA Hofmann, N Friedman, OJ Rando. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010; 143(7): 1084–1096
https://doi.org/10.1016/j.cell.2010.12.008 pmid: 21183072
38 T Fullston, EM Ohlsson Teague, NO Palmer, MJ DeBlasio, M Mitchell, M Corbett, CG Print, JA Owens, M Lane. 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(10): 4226–4243
https://doi.org/10.1096/fj.12-224048 pmid: 23845863
39 H Peng, J Shi, Y Zhang, H Zhang, S Liao, W Li, L Lei, C Han, L Ning, Y Cao, Q Zhou, Q Chen, E Duan. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res 2012; 22(11): 1609–1612
https://doi.org/10.1038/cr.2012.141 pmid: 23044802
40 JN Reilly, EA McLaughlin, SJ Stanger, AL Anderson, K Hutcheon, K Church, BP Mihalas, S Tyagi, JE Holt, AL Eamens, B Nixon. Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Sci Rep 2016; 6(1): 31794
https://doi.org/10.1038/srep31794 pmid: 27549865
41 K Hutcheon, EA McLaughlin, SJ Stanger, IR Bernstein, MD Dun, AL Eamens, B Nixon. Analysis of the small non-protein-coding RNA profile of mouse spermatozoa reveals specific enrichment of piRNAs within mature spermatozoa. RNA Biol 2017; 14(12): 1776–1790
https://doi.org/10.1080/15476286.2017.1356569 pmid: 28816603
42 R Sullivan. Epididymosomes: role of extracellular microvesicles in sperm maturation. Front Biosci (Schol Ed) 2016; 8(1): 106–114
https://doi.org/10.2741/s450 pmid: 26709900
43 M Hua, W Liu, Y Chen, F Zhang, B Xu, S Liu, G Chen, H Shi, L Wu. Identification of small non-coding RNAs as sperm quality biomarkers for in vitro fertilization. Cell Discov 2019; 5(1): 20
https://doi.org/10.1038/s41421-019-0087-9 pmid: 30992999
44 Y Zhang, X Zhang, J Shi, F Tuorto, X Li, Y Liu, R Liebers, L Zhang, Y Qu, J Qian, M Pahima, Y Liu, M Yan, Z Cao, X Lei, Y Cao, H Peng, S Liu, Y Wang, H Zheng, R Woolsey, D Quilici, Q Zhai, L Li, T Zhou, W Yan, F Lyko, Y Zhang, Q Zhou, E Duan, Q Chen. Dnmt2 mediates intergenerational transmission of paternally acquired metabolic disorders through sperm small non-coding RNAs. Nat Cell Biol 2018; 20(5): 535–540
https://doi.org/10.1038/s41556-018-0087-2 pmid: 29695786
45 D Nätt, U Kugelberg, E Casas, E Nedstrand, S Zalavary, P Henriksson, C Nijm, J Jäderquist, J Sandborg, E Flinke, R Ramesh, L Örkenby, F Appelkvist, T Lingg, N Guzzi, C Bellodi, M Löf, T Vavouri, A Öst. Human sperm displays rapid responses to diet. PLoS Biol 2019; 17(12): e3000559
https://doi.org/10.1371/journal.pbio.3000559 pmid: 31877125
46 J Shi, Y Zhang, D Tan, X Zhang, M Yan, Y Zhang, R Franklin, M Shahbazi, K Mackinlay, S Liu, B Kuhle, ER James, L Zhang, Y Qu, Q Zhai, W Zhao, L Zhao, C Zhou, W Gu, J Murn, J Guo, DT Carrell, Y Wang, X Chen, BR Cairns, XL Yang, P Schimmel, M Zernicka-Goetz, S Cheloufi, Y Zhang, T Zhou, Q Chen. PANDORA-seq expands the repertoire of regulatory small RNAs by overcoming RNA modifications. Nat Cell Biol 2021; 23(4): 424–436
https://doi.org/10.1038/s41556-021-00652-7 pmid: 33820973
47 J Kiani, V Grandjean, R Liebers, F Tuorto, H Ghanbarian, F Lyko, F Cuzin, M Rassoulzadegan. RNA-mediated epigenetic heredity requires the cytosine methyltransferase Dnmt2. PLoS Genet 2013; 9(5): e1003498
https://doi.org/10.1371/journal.pgen.1003498 pmid: 23717211
48 G Sarker, W Sun, D Rosenkranz, P Pelczar, L Opitz, V Efthymiou, C Wolfrum, D Peleg-Raibstein. Maternal overnutrition programs hedonic and metabolic phenotypes across generations through sperm tsRNAs. Proc Natl Acad Sci USA 2019; 116(21): 10547–10556
https://doi.org/10.1073/pnas.1820810116 pmid: 31061112
49 D Peleg-Raibstein, G Sarker, K Litwan, SD Krämer, SM Ametamey, R Schibli, C Wolfrum. Enhanced sensitivity to drugs of abuse and palatable foods following maternal overnutrition. Transl Psychiatry 2016; 6(10): e911
https://doi.org/10.1038/tp.2016.176 pmid: 27701408
50 G Sarker, R Berrens, J von Arx, P Pelczar, W Reik, C Wolfrum, D Peleg-Raibstein. Transgenerational transmission of hedonic behaviors and metabolic phenotypes induced by maternal overnutrition. Transl Psychiatry 2018; 8(1): 195
https://doi.org/10.1038/s41398-018-0243-2 pmid: 30315171
51 EJ Radford, M Ito, H Shi, JA Corish, K Yamazawa, E Isganaitis, S Seisenberger, TA Hore, W Reik, S Erkek, AHFM Peters, ME Patti, AC Ferguson-Smith. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 2014; 345(6198): 1255903
https://doi.org/10.1126/science.1255903 pmid: 25011554
52 JM Shea, RW Serra, BR Carone, HP Shulha, A Kucukural, MJ Ziller, MP Vallaster, H Gu, AR Tapper, PD Gardner, A Meissner, M Garber, OJ Rando. Genetic and epigenetic variation, but not diet, shape the sperm methylome. Dev Cell 2015; 35(6): 750–758
https://doi.org/10.1016/j.devcel.2015.11.024 pmid: 26702833
53 E Sendler, GD Johnson, S Mao, RJ Goodrich, MP Diamond, R Hauser, SA Krawetz. Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res 2013; 41(7): 4104–4117
https://doi.org/10.1093/nar/gkt132 pmid: 23471003
54 M Kawano, H Kawaji, V Grandjean, J Kiani, M Rassoulzadegan. Novel small noncoding RNAs in mouse spermatozoa, zygotes and early embryos. PLoS One 2012; 7(9): e44542
https://doi.org/10.1371/journal.pone.0044542 pmid: 22984523
55 SA Krawetz, A Kruger, C Lalancette, R Tagett, E Anton, S Draghici, MP Diamond. A survey of small RNAs in human sperm. Hum Reprod 2011; 26(12): 3401–3412
https://doi.org/10.1093/humrep/der329 pmid: 21989093
56 DM Dietz, Q Laplant, EL Watts, GE Hodes, SJ Russo, J Feng, RS Oosting, V Vialou, EJ Nestler. Paternal transmission of stress-induced pathologies. Biol Psychiatry 2011; 70(5): 408–414
https://doi.org/10.1016/j.biopsych.2011.05.005 pmid: 21679926
57 AB Rodgers, CP Morgan, SL Bronson, S Revello, TL Bale. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 2013; 33(21): 9003–9012
https://doi.org/10.1523/JNEUROSCI.0914-13.2013 pmid: 23699511
58 J Bohacek, M Farinelli, O Mirante, G Steiner, K Gapp, G Coiret, M Ebeling, G Durán-Pacheco, AL Iniguez, F Manuella, JL Moreau, IM Mansuy. Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress. Mol Psychiatry 2015; 20(5): 621–631
https://doi.org/10.1038/mp.2014.80 pmid: 25092246
59 K Gapp, J Bohacek, J Grossmann, AM Brunner, F Manuella, P Nanni, IM Mansuy. Potential of environmental enrichment to prevent transgenerational effects of paternal trauma. Neuropsychopharmacology 2016; 41(11): 2749–2758
https://doi.org/10.1038/npp.2016.87 pmid: 27277118
60 KR McGreevy, P Tezanos, I Ferreiro-Villar, A Pallé, M Moreno-Serrano, A Esteve-Codina, I Lamas-Toranzo, P Bermejo-Álvarez, J Fernández-Punzano, A Martín-Montalvo, R Montalbán, SR Ferrón, EJ Radford, Á Fontán-Lozano, JL Trejo. Intergenerational transmission of the positive effects of physical exercise on brain and cognition. Proc Natl Acad Sci USA 2019; 116(20): 10103–10112
https://doi.org/10.1073/pnas.1816781116 pmid: 31010925
61 Y Wang, ZP Chen, H Hu, J Lei, Z Zhou, B Yao, L Chen, G Liang, S Zhan, X Zhu, F Jin, R Ma, J Zhang, H Liang, M Xing, XR Chen, CY Zhang, JN Zhu, X Chen. Sperm microRNAs confer depression susceptibility to offspring. Sci Adv 2021; 7(7): eabd7605
https://doi.org/10.1126/sciadv.abd7605 pmid: 33568480
62 K Gapp, G van Steenwyk, PL Germain, W Matsushima, KLM Rudolph, F Manuella, M Roszkowski, G Vernaz, T Ghosh, P Pelczar, IM Mansuy, EA Miska. Alterations in sperm long RNA contribute to the epigenetic inheritance of the effects of postnatal trauma. Mol Psychiatry 2020; 25(9): 2162–2174
https://doi.org/10.1038/s41380-018-0271-6 pmid: 30374190
63 JC Chan, CP Morgan, N Adrian Leu, A Shetty, YM Cisse, BM Nugent, KE Morrison, E Jašarević, W Huang, N Kanyuch, AB Rodgers, NV Bhanu, DS Berger, BA Garcia, S Ament, M Kane, C Neill Epperson, TL Bale. Reproductive tract extracellular vesicles are sufficient to transmit intergenerational stress and program neurodevelopment. Nat Commun 2020; 11(1): 1499
https://doi.org/10.1038/s41467-020-15305-w pmid: 32198406
64 WM Liu, RT Pang, PC Chiu, BP Wong, K Lao, KF Lee, WS Yeung. Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc Natl Acad Sci USA 2012; 109(2): 490–494
https://doi.org/10.1073/pnas.1110368109 pmid: 22203953
65 Y Hong, C Wang, Z Fu, H Liang, S Zhang, M Lu, W Sun, C Ye, CY Zhang, K Zen, L Shi, C Zhang, X Chen. Systematic characterization of seminal plasma piRNAs as molecular biomarkers for male infertility. Sci Rep 2016; 6(1): 24229
https://doi.org/10.1038/srep24229 pmid: 27068805
66 TC Roberts. The microRNA Biology of the mammalian nucleus. Mol Ther Nucleic Acids 2014; 3: e188
https://doi.org/10.1038/mtna.2014.40 pmid: 25137140
67 L Sinkkonen, T Hugenschmidt, P Berninger, D Gaidatzis, F Mohn, CG Artus-Revel, M Zavolan, P Svoboda, W Filipowicz. MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat Struct Mol Biol 2008; 15(3): 259–267
https://doi.org/10.1038/nsmb.1391 pmid: 18311153
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