Sperm-borne sncRNAs: potential biomarkers for semen fertility?
Eli Sellem A * , Hélène Jammes B C and Laurent Schibler A
+ Author Affiliations
- Author Affiliations
A R&D Department, ALLICE, 149 rue de Bercy, 75012 Paris, France.
B Université Paris Saclay, UVSQ, INRAE, BREED, 78350 Jouy en Josas, France.
C Ecole Nationale Vétérinaire d’Alfort, BREED, 94700 Maisons–Alfort, France.
* Correspondence to: eli.sellem@allice.fr
Reproduction, Fertility and Development 34(2) 160-173 https://doi.org/10.1071/RD21276
Published online: 15 October 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the IETS. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Semen infertility or sub-fertility, whether in humans or livestock species, remains a major concern for clinicians and technicians involved in reproduction. Indeed, they can cause tragedies in human relationships or have a dramatic overall negative impact on the sustainability of livestock breeding. Understanding and predicting semen fertility issues is therefore crucial and quality control procedures as well as biomarkers have been proposed to ensure sperm fertility. However, their predictive values appeared to be too limited and additional relevant biomarkers are still required to diagnose sub-fertility efficiently. During the last decade, the study of molecular mechanisms involved in spermatogenesis and sperm maturation highlighted the regulatory role of a variety of small non-coding RNAs (sncRNAs) and led to the discovery that sperm sncRNAs comprise both remnants from spermatogenesis and post-testicular sncRNAs acquired through interactions with extracellular vesicles along epididymis. This has led to the hypothesis that sncRNAs may be a source of relevant biomarkers, associated either with sperm functionality or embryo development. This review aims at providing a synthetic overview of the current state of knowledge regarding implication of sncRNA in spermatogenesis defects and their putative roles in sperm maturation and embryo development, as well as exploring their use as fertility biomarkers.
Keywords: epididymosomes, epigenetic, fertility, fertility prediction, non-genetic sperm legacy, semen, sncRNAs, sperm-born sncRNAs.
References
Abu-Halima, M, Hammadeh, M, Schmitt, J, Leidinger, P, Keller, A, Meese, E, and Backes, C (2013). Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertility and Sterility 99, 1249–1255.e16.| Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments.Crossref | GoogleScholarGoogle Scholar | 23312218PubMed |
Abu-Halima, M, Hammadeh, M, Backes, C, Fischer, U, Leidinger, P, Lubbad, AM, Keller, A, and Meese, E (2014). Panel of five microRNAs as potential biomarkers for the diagnosis and assessment of male infertility. Fertility and Sterility 102, 989–997.e1.
| Panel of five microRNAs as potential biomarkers for the diagnosis and assessment of male infertility.Crossref | GoogleScholarGoogle Scholar | 25108464PubMed |
Alvarez-Rodriguez, M, Martinez, C, Wright, D, Barranco, I, Roca, J, and Rodriguez-Martinez, H (2020). The transcriptome of pig spermatozoa, and its role in fertility. International Journal of Molecular Sciences 21, 1571.
| The transcriptome of pig spermatozoa, and its role in fertility.Crossref | GoogleScholarGoogle Scholar |
Alves, MBR, de Arruda, RP, De Bem, THC, Florez-Rodriguez, SA, de Sá Filho, MF, Belleannée, C, Meirelles, FV, da Silveira, JC, Perecin, F, and Celeghini, ECC (2019). Sperm-borne miR-216b modulates cell proliferation during early embryo development via K-RAS. Scientific Reports 9, 1–14.
| Sperm-borne miR-216b modulates cell proliferation during early embryo development via K-RAS.Crossref | GoogleScholarGoogle Scholar |
Alves, MBR, Celeghini, ECC, and Belleannée, C (2020). From sperm motility to sperm-borne microRNA signatures: new approaches to predict male fertility potential. Frontiers in Cell and Developmental Biology 8, 791.
| From sperm motility to sperm-borne microRNA signatures: new approaches to predict male fertility potential.Crossref | GoogleScholarGoogle Scholar | 32974342PubMed |
Amann, RP, and Waberski, D (2014). Computer-assisted sperm analysis (CASA): capabilities and potential developments. Theriogenology 81, 5–17. e1-3.
| Computer-assisted sperm analysis (CASA): capabilities and potential developments.Crossref | GoogleScholarGoogle Scholar | 24274405PubMed |
Andl, T, Murchison, EP, Liu, F, Zhang, Y, Yunta-Gonzalez, M, Tobias, JW, Andl, CD, Seykora, JT, Hannon, GJ, and Millar, SE (2006). The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles. Current Biology 16, 1041–1049.
| The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles.Crossref | GoogleScholarGoogle Scholar | 16682203PubMed |
Aravin, AA, Sachidanandam, R, Bourc’his, D, Schaefer, C, Pezic, D, Toth, KF, Bestor, T, and Hannon, GJ (2008). A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Molecular Cell 31, 785–799.
| A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice.Crossref | GoogleScholarGoogle Scholar | 18922463PubMed |
Belleannee, C, Calvo, E, Caballero, J, and Sullivan, R (2013). Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biology of Reproduction 89, 30.
| Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis.Crossref | GoogleScholarGoogle Scholar | 23803555PubMed |
Bernstein, E, Kim, SY, Carmell, MA, Murchison, EP, Alcorn, H, Li, MZ, Mills, AA, Elledge, SJ, Anderson, KV, and Hannon, GJ (2003). Dicer is essential for mouse development. Nature Genetics 35, 215–217.
| Dicer is essential for mouse development.Crossref | GoogleScholarGoogle Scholar | 14528307PubMed |
Capra, E, Turri, F, Lazzari, B, Cremonesi, P, Gliozzi, TM, Fojadelli, I, Stella, A, and Pizzi, F (2017). Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between High- and Low-motile sperm populations. BMC Genomics 18, 14.
| Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between High- and Low-motile sperm populations.Crossref | GoogleScholarGoogle Scholar | 28052756PubMed |
Chak, L-L, Mohammed, J, Lai, EC, Tucker-Kellogg, G, and Okamura, K (2015). A deeply conserved, noncanonical miRNA hosted by ribosomal DNA. RNA 21, 375–384.
| A deeply conserved, noncanonical miRNA hosted by ribosomal DNA.Crossref | GoogleScholarGoogle Scholar | 25605965PubMed |
Chalmel, F, and Rolland, AD (2015). Linking transcriptomics and proteomics in spermatogenesis. Reproduction 150, R149–R157.
| Linking transcriptomics and proteomics in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 26416010PubMed |
Chen, Q, Yan, M, Cao, Z, Li, X, Zhang, Y, Shi, J, Feng, GH, Peng, H, Zhang, X, Zhang, Y, Qian, J, Duan, E, Zhai, Q, and Zhou, Q (2016). Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351, 397–400.
| Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.Crossref | GoogleScholarGoogle Scholar | 26721680PubMed |
Chen, X, Zheng, Y, Lei, A, Zhang, H, Niu, H, Li, X, Zhang, P, Liao, M, Lv, Y, Zhu, Z, Pan, C, Dong, W, Chen, H, Wu, D, Liu, W, Hamer, G, Zeng, S, and Zeng, W (2020). Early cleavage of preimplantation embryos is regulated by tRNAGln-TTG-derived small RNAs present in mature spermatozoa. Journal of Biological Chemistry 295, 10885–10900.
| Early cleavage of preimplantation embryos is regulated by tRNAGln-TTG-derived small RNAs present in mature spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Chen, X, Sun, Q, Zheng, Y, Liu, Z, Meng, X, Zeng, W, and Lu, H (2021). Human sperm tsRNA as potential biomarker and therapy target for male fertility. Reproduction 161, 111–122.
| Human sperm tsRNA as potential biomarker and therapy target for male fertility.Crossref | GoogleScholarGoogle Scholar | 33434159PubMed |
Cherlin, T, Magee, R, Jing, Y, Pliatsika, V, Loher, P, and Rigoutsos, I (2020). Ribosomal RNA fragmentation into short RNAs (rRFs) is modulated in a sex- and population of origin-specific manner. BMC Biology 18, 38.
| Ribosomal RNA fragmentation into short RNAs (rRFs) is modulated in a sex- and population of origin-specific manner.Crossref | GoogleScholarGoogle Scholar | 32279660PubMed |
Choi, H, Wang, Z, and Dean, J (2021). Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA. PLOS Genetics 17, e1009485.
| Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA.Crossref | GoogleScholarGoogle Scholar | 33831001PubMed |
Chu, C, Yu, L, Wu, B, Ma, L, Gou, LT, He, M, Guo, Y, Li, ZT, Gao, W, Shi, H, Liu, MF, Wang, H, Chen, CD, Drevet, JR, Zhou, Y, and Zhang, Y (2017). A sequence of 28S rRNA-derived small RNAs is enriched in mature sperm and various somatic tissues and possibly associates with inflammation. Journal of Molecular Cell Biology 9, 256–259.
| A sequence of 28S rRNA-derived small RNAs is enriched in mature sperm and various somatic tissues and possibly associates with inflammation.Crossref | GoogleScholarGoogle Scholar | 28486659PubMed |
Chu, C, Zhang, YL, Yu, L, Sharma, S, Fei, ZL, and Drevet, JR (2019). Epididymal small non-coding RNA studies: progress over the past decade. Andrology 7, 681–689.
| Epididymal small non-coding RNA studies: progress over the past decade.Crossref | GoogleScholarGoogle Scholar | 31044548PubMed |
Chuma, S, and Nakano, T (2013). piRNA and spermatogenesis in mice. Philosophical Transactions of the Royal Society B: Biological Sciences 368, 20110338.
| piRNA and spermatogenesis in mice.Crossref | GoogleScholarGoogle Scholar |
Comazzetto, S, Di Giacomo, M, Rasmussen, KD, Much, C, Azzi, C, Perlas, E, Morgan, M, and O’Carroll, D (2014). Oligoasthenoteratozoospermia and infertility in mice deficient for miR-34b/c and miR-449 loci. PLoS Genetics 10, e1004597.
| Oligoasthenoteratozoospermia and infertility in mice deficient for miR-34b/c and miR-449 loci.Crossref | GoogleScholarGoogle Scholar | 25329700PubMed |
Conine, CC, Sun, F, Song, L, Rivera-Perez, JA, and Rando, OJ (2018). Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice. Developmental Cell 46, 470–480.e3.
| Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice.Crossref | GoogleScholarGoogle Scholar | 30057276PubMed |
Corral-Vazquez, C, Salas-Huetos, A, Blanco, J, Vidal, F, Sarrate, Z, and Anton, E (2019). Sperm microRNA pairs: new perspectives in the search for male fertility biomarkers. Fertility and Sterility 112, 831–841.
| Sperm microRNA pairs: new perspectives in the search for male fertility biomarkers.Crossref | GoogleScholarGoogle Scholar | 31587805PubMed |
Curry, E, Safranski, TJ, and Pratt, SL (2011). Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76, 1532–1539.
| Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility.Crossref | GoogleScholarGoogle Scholar | 21872314PubMed |
Czech, B, and Hannon, GJ (2016). One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends in Biochemical Sciences 41, 324–337.
| One loop to rule them all: the ping-pong cycle and piRNA-guided silencing.Crossref | GoogleScholarGoogle Scholar | 26810602PubMed |
Czech, B, Munafò, M, Ciabrelli, F, Eastwood, EL, Fabry, MH, Kneuss, E, and Hannon, GJ (2018). piRNA-guided genome defense: from biogenesis to silencing. Annual Review of Genetics 52, 131–157.
| piRNA-guided genome defense: from biogenesis to silencing.Crossref | GoogleScholarGoogle Scholar | 30476449PubMed |
de Castro Barbosa, T, Ingerslev, LR, Alm, PS, Versteyhe, S, Massart, J, Rasmussen, M, Donkin, I, Sjö gren, R, Mudry, JM, Vetterli, L, Gupta, S, Krook, A, Zierath, JR, and Barrès, R (2016). High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Molecular Metabolism 5, 184–197.
| High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring.Crossref | GoogleScholarGoogle Scholar | 26977389PubMed |
de Mateo, S, and Sassone-Corsi, P (2014). Regulation of spermatogenesis by small non-coding RNAs: role of the germ granule. Seminars in Cell & Developmental Biology 29, 84–92.
| Regulation of spermatogenesis by small non-coding RNAs: role of the germ granule.Crossref | GoogleScholarGoogle Scholar |
Deng, J, Ptashkin, RN, Chen, Y, Cheng, Z, Liu, G, Phan, T, Deng, X, Zhou, J, Lee, I, Lee, YS, and Bao, X (2015). Respiratory Syncytial Virus Utilizes a tRNA Fragment to Suppress Antiviral Responses Through a Novel Targeting Mechanism. Molecular Therapy 23, 1622–1629.
| Respiratory Syncytial Virus Utilizes a tRNA Fragment to Suppress Antiviral Responses Through a Novel Targeting Mechanism.Crossref | GoogleScholarGoogle Scholar | 26156244PubMed |
Donkin, I, and Barrès, R (2018). Sperm epigenetics and influence of environmental factors. Molecular Metabolism 14, 1–11.
| Sperm epigenetics and influence of environmental factors.Crossref | GoogleScholarGoogle Scholar | 29525406PubMed |
Emara, MM, Ivanov, P, Hickman, T, Dawra, N, Tisdale, S, Kedersha, N, Hu, GF, and Anderson, P (2010). Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. Journal of Biological Chemistry 285, 10959–10968.
| Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly.Crossref | GoogleScholarGoogle Scholar |
Fagerlind, M, Stålhammar, H, Olsson, B, and Klinga-Levan, K (2015). Expression of miRNAs in bull spermatozoa correlates with fertility rates. Reproduction in Domestic Animals 50, 587–594.
| Expression of miRNAs in bull spermatozoa correlates with fertility rates.Crossref | GoogleScholarGoogle Scholar | 25998690PubMed |
Fei, T, Zhu, S, Xia, K, Zhang, J, Li, Z, Han, JD, and Chen, YG (2010). Smad2 mediates Activin/Nodal signaling in mesendoderm differentiation of mouse embryonic stem cells. Cell Research 20, 1306–1318.
| Smad2 mediates Activin/Nodal signaling in mesendoderm differentiation of mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 21079647PubMed |
Fernandez-Valverde, SL, Taft, RJ, and Mattick, JS (2010). Dynamic isomiR regulation in Drosophila development. RNA 16, 1881–1888.
| Dynamic isomiR regulation in Drosophila development.Crossref | GoogleScholarGoogle Scholar | 20805289PubMed |
Friedman, RC, Farh, KK-H, Burge, CB, and Bartel, DP (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Research 19, 92–105.
| Most mammalian mRNAs are conserved targets of microRNAs.Crossref | GoogleScholarGoogle Scholar | 18955434PubMed |
Galatenko, VV, Galatenko, AV, Samatov, TR, Turchinovich, AA, Shkurnikov, MY, Makarova, JA, and Tonevitsky, AG (2018). Comprehensive network of miRNA-induced intergenic interactions and a biological role of its core in cancer. Scientific Reports 8, 2418.
| Comprehensive network of miRNA-induced intergenic interactions and a biological role of its core in cancer.Crossref | GoogleScholarGoogle Scholar | 29402894PubMed |
Girard, A, Sachidanandam, R, Hannon, GJ, and Carmell, MA (2006). A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199–202.
| A germline-specific class of small RNAs binds mammalian Piwi proteins.Crossref | GoogleScholarGoogle Scholar | 16751776PubMed |
Girouard, J, Frenette, G, and Sullivan, R (2011). Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. International Journal of Andrology 34, e475–e486.
| Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis.Crossref | GoogleScholarGoogle Scholar | 21875428PubMed |
Gòdia, M, Estill, M, Castelló, A, Balasch, S, Rodríguez-Gil, JE, Krawetz, SA, Sánchez, A, and Clop, A (2019). A RNA-Seq analysis to describe the boar sperm transcriptome and its seasonal changes. Frontiers in Genetics 10, 299.
| A RNA-Seq analysis to describe the boar sperm transcriptome and its seasonal changes.Crossref | GoogleScholarGoogle Scholar | 31040860PubMed |
Goh, WSS, Falciatori, I, Tam, OH, Burgess, R, Meikar, O, Kotaja, N, Hammell, M, and Hannon, GJ (2015). piRNA-directed cleavage of meiotic transcripts regulates spermatogenesis. Genes & Development 29, 1032–1044.
| piRNA-directed cleavage of meiotic transcripts regulates spermatogenesis.Crossref | GoogleScholarGoogle Scholar |
Gommans, WM, Mullen, SP, and Maas, S (2009). RNA editing: a driving force for adaptive evolution? BioEssays 31, 1137–1145.
| RNA editing: a driving force for adaptive evolution?Crossref | GoogleScholarGoogle Scholar | 19708020PubMed |
Gott, JM, and Emeson, RB (2000). Functions and mechanisms of RNA editing. Annual Review of Genetics 34, 499–531.
| Functions and mechanisms of RNA editing.Crossref | GoogleScholarGoogle Scholar | 11092837PubMed |
Gou, LT, Dai, P, Yang, JH, Xue, Y, Hu, YP, Zhou, Y, Kang, JY, Wang, X, Li, H, Hua, MM, Zhao, S, Hu, SD, Wu, LG, Shi, HJ, Li, Y, Fu, XD, Qu, LH, Wang, ED, and Liu, MF (2014). Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis. Cell Research 24, 680–700.
| Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 24787618PubMed |
Grandjean, V, Fourre, S, De Abreu, DA, Derieppe, M-A, Remy, JJ, and Rassoulzadegan, M (2016). RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Scientific Reports 5, 18193.
| RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders.Crossref | GoogleScholarGoogle Scholar |
Guan, L, and Grigoriev, A (2020). Age-related argonaute loading of ribosomal RNA fragments. MicroRNA 9, 142–152.
| Age-related argonaute loading of ribosomal RNA fragments.Crossref | GoogleScholarGoogle Scholar | 31538909PubMed |
Guo, L, Chao, S-B, Xiao, L, Wang, Z-B, Meng, T-G, Li, Y-Y, Han, Z-M, Ouyang, Y-C, Hou, Y, Sun, Q-Y, and Ou, X-H (2017). Sperm-carried RNAs play critical roles in mouse embryonic development. Oncotarget 8, 67394–67405.
| Sperm-carried RNAs play critical roles in mouse embryonic development.Crossref | GoogleScholarGoogle Scholar | 28978041PubMed |
Guzzi, N, and Bellodi, C (2020). Novel insights into the emerging roles of tRNA-derived fragments in mammalian development. RNA Biology 17, 1214–1222.
| Novel insights into the emerging roles of tRNA-derived fragments in mammalian development.Crossref | GoogleScholarGoogle Scholar | 32116113PubMed |
Hamada, AJ, Montgomery, B, and Agarwal, A (2012). Male infertility: a critical review of pharmacologic management. Expert Opinion on Pharmacotherapy 13, 2511–2531.
| Male infertility: a critical review of pharmacologic management.Crossref | GoogleScholarGoogle Scholar | 23121497PubMed |
Hammond, SM (2015). An overview of microRNAs. Advanced Drug Delivery Reviews 87, 3–14.
| An overview of microRNAs.Crossref | GoogleScholarGoogle Scholar | 25979468PubMed |
He, Z, Jiang, J, Kokkinaki, M, Tang, L, Zeng, W, Gallicano, I, Dobrinski, I, and Dym, M (2013). MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem Cells 31, 2205–2217.
| MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1.Crossref | GoogleScholarGoogle Scholar | 23836497PubMed |
Hilz, S, Fogarty, EA, Modzelewski, AJ, Cohen, PE, and Grimson, A (2017). Transcriptome profiling of the developing male germ line identifies the miR-29 family as a global regulator during meiosis. RNA Biology 14, 219–235.
| Transcriptome profiling of the developing male germ line identifies the miR-29 family as a global regulator during meiosis.Crossref | GoogleScholarGoogle Scholar | 27981880PubMed |
Hombach, S, and Kretz, M (2016). Non-coding RNAs: classification, biology and functioning. Advances in Experimental Medicine and Biology 937, 3–17.
| Non-coding RNAs: classification, biology and functioning.Crossref | GoogleScholarGoogle Scholar | 27573892PubMed |
Hua, M, Liu, W, Chen, Y, Zhang, F, Xu, B, Liu, S, Chen, G, Shi, H, and Wu, L (2019). Identification of small non-coding RNAs as sperm quality biomarkers for in vitro fertilization. Cell Discovery 5, 20.
| Identification of small non-coding RNAs as sperm quality biomarkers for in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 30992999PubMed |
Huang, Y-L, Huang, G-Y, Lv, J, Pan, L-N, Luo, X, and Shen, J (2017). miR-100 promotes the proliferation of spermatogonial stem cells via regulating Stat3. Molecular Reproduction and Development 84, 693–701.
| miR-100 promotes the proliferation of spermatogonial stem cells via regulating Stat3.Crossref | GoogleScholarGoogle Scholar | 28569396PubMed |
Huszar, JM, and Payne, CJ (2013). MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice. Biology of Reproduction 88, 15.
| MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice.Crossref | GoogleScholarGoogle Scholar | 23221399PubMed |
Hutvágner, G, McLachlan, J, Pasquinelli, AE, Bálint, É, Tuschl, T, and Zamore, PD (2001). A cellular function for the RNA-interference enzyme dicer in the maturation of the let-7 small temporal RNA. Science 293, 834–838.
| A cellular function for the RNA-interference enzyme dicer in the maturation of the let-7 small temporal RNA.Crossref | GoogleScholarGoogle Scholar | 11452083PubMed |
Ivanov, P, Emara, MM, Villen, J, Gygi, SP, and Anderson, P (2011). Angiogenin-induced tRNA fragments inhibit translation initiation. Molecular Cell 43, 613–623.
| Angiogenin-induced tRNA fragments inhibit translation initiation.Crossref | GoogleScholarGoogle Scholar | 21855800PubMed |
Jia, Y, Mu, JC, and Ackerman, SL (2012). Mutation of a U2 snRNA gene causes global disruption of alternative splicing and neurodegeneration. Cell 148, 296–308.
| Mutation of a U2 snRNA gene causes global disruption of alternative splicing and neurodegeneration.Crossref | GoogleScholarGoogle Scholar | 22265417PubMed |
Karijolich, J, and Yu, YT (2010). Spliceosomal snRNA modifications and their function. RNA Biology 7, 192–204.
| Spliceosomal snRNA modifications and their function.Crossref | GoogleScholarGoogle Scholar | 20215871PubMed |
Karna, KK, Shin, YS, Choi, BR, Kim, HK, and Park, JK (2020). The role of endoplasmic reticulum stress response in male reproductive physiology and pathology: a review. The World Journal of Men’s Health 38, 484–494.
| The role of endoplasmic reticulum stress response in male reproductive physiology and pathology: a review.Crossref | GoogleScholarGoogle Scholar | 31385474PubMed |
Katoh, T, Sakaguchi, Y, Miyauchi, K, Suzuki, T, Kashiwabara, S-I, Baba, T, and Suzuki, T (2009). Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes & Development 23, 433–438.
| Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2.Crossref | GoogleScholarGoogle Scholar |
Keam, SP, and Hutvagner, G (2015). tRNA-Derived Fragments (tRFs): emerging new roles for an ancient RNA in the regulation of gene expression. Life 5, 1638–1651.
| tRNA-Derived Fragments (tRFs): emerging new roles for an ancient RNA in the regulation of gene expression.Crossref | GoogleScholarGoogle Scholar | 26703738PubMed |
Keles, E, Malama, E, Bozukova, S, Siuda, M, Wyck, S, Witschi, U, Bauersachs, S, and Bollwein, H (2021). The micro-RNA content of unsorted cryopreserved bovine sperm and its relation to the fertility of sperm after sex-sorting. BMC Genomics 22, 30.
| The micro-RNA content of unsorted cryopreserved bovine sperm and its relation to the fertility of sperm after sex-sorting.Crossref | GoogleScholarGoogle Scholar | 33413071PubMed |
Koenig, P-A, Nicholls, PK, Schmidt, FI, Hagiwara, M, Maruyama, T, Frydman, GH, Watson, N, Page, DC, and Ploegh, HL (2014). The E2 ubiquitin-conjugating enzyme UBE2J1 is required for spermiogenesis in mice. Journal of Biological Chemistry 289, 34490–34502.
| The E2 ubiquitin-conjugating enzyme UBE2J1 is required for spermiogenesis in mice.Crossref | GoogleScholarGoogle Scholar |
Korhonen, HM, Meikar, O, Yadav, RP, Papaioannou, MD, Romero, Y, Da Ros, M, Herrera, PL, Toppari, J, Nef, S, and Kotaja, N (2011). Dicer is required for haploid male germ cell differentiation in mice. PLoS One 6, e24821.
| Dicer is required for haploid male germ cell differentiation in mice.Crossref | GoogleScholarGoogle Scholar | 21949761PubMed |
Kotaja, N, Bhattacharyya, SN, Jaskiewicz, L, Kimmins, S, Parvinen, M, Filipowicz, W, and Sassone-Corsi, P (2006). The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proceedings of the National Academy of Sciences 103, 2647–2652.
| The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components.Crossref | GoogleScholarGoogle Scholar |
Krill, KT, Gurdziel, K, Heaton, JH, Simon, DP, and Hammer, GD (2013). Dicer deficiency reveals microRNAs predicted to control gene expression in the developing adrenal cortex. Molecular Endocrinology 27, 754–768.
| Dicer deficiency reveals microRNAs predicted to control gene expression in the developing adrenal cortex.Crossref | GoogleScholarGoogle Scholar | 23518926PubMed |
Krishna, S, Raghavan, S, DasGupta, R, and Palakodeti, D (2021). tRNA-derived fragments (tRFs): establishing their turf in post-transcriptional gene regulation. Cellular and Molecular Life Sciences 78, 2607–2619.
| tRNA-derived fragments (tRFs): establishing their turf in post-transcriptional gene regulation.Crossref | GoogleScholarGoogle Scholar | 33388834PubMed |
Kumar, P, Kuscu, C, and Dutta, A (2016). Biogenesis and function of transfer RNA-Related Fragments (tRFs). Trends in Biochemical Sciences 41, 679–689.
| Biogenesis and function of transfer RNA-Related Fragments (tRFs).Crossref | GoogleScholarGoogle Scholar | 27263052PubMed |
Kuscu, C, Kumar, P, Kiran, M, Su, Z, Malik, A, and Dutta, A (2018). tRNA fragments (tRFs) guide Ago to regulate gene expression post-transcriptionally in a Dicer-independent manner. RNA 24, 1093–1105.
| tRNA fragments (tRFs) guide Ago to regulate gene expression post-transcriptionally in a Dicer-independent manner.Crossref | GoogleScholarGoogle Scholar | 29844106PubMed |
Lambert, M, Benmoussa, A, and Provost, P (2019). Small non-coding RNAs derived from eukaryotic ribosomal RNA. Non-coding RNA 5, 16.
| Small non-coding RNAs derived from eukaryotic ribosomal RNA.Crossref | GoogleScholarGoogle Scholar |
Le Blevec, E, Muronova, J, Ray, PF, and Arnoult, C (2020). Paternal epigenetics: Mammalian sperm provide much more than DNA at fertilization. Mol Cell Endocrinol 518, 110964.
| Paternal epigenetics: Mammalian sperm provide much more than DNA at fertilization.Crossref | GoogleScholarGoogle Scholar | 32738444PubMed |
Lee, Y, Ahn, C, Han, J, Choi, H, Kim, J, Yim, J, Lee, J, Provost, P, Radmark, O, Kim, S, and Kim, VN (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.
| The nuclear RNase III Drosha initiates microRNA processing.Crossref | GoogleScholarGoogle Scholar | 14508493PubMed |
Lee, D, Park, D, Park, JH, Kim, JH, and Shin, C (2019). Poly(A)-specific ribonuclease sculpts the 3′ ends of microRNAs. RNA 25, 388–405.
| Poly(A)-specific ribonuclease sculpts the 3′ ends of microRNAs.Crossref | GoogleScholarGoogle Scholar | 30591540PubMed |
Li, L, Song, Y, Shi, X, Liu, J, Xiong, S, Chen, W, Fu, Q, Huang, Z, Gu, N, and Zhang, R (2018a). The landscape of miRNA editing in animals and its impact on miRNA biogenesis and targeting. Genome Research 28, 132–143.
| The landscape of miRNA editing in animals and its impact on miRNA biogenesis and targeting.Crossref | GoogleScholarGoogle Scholar | 29233923PubMed |
Li, Y, Li, R-H, Ran, M-X, Zhang, Y, Liang, K, Ren, Y-N, He, W-C, Zhang, M, Zhou, G-B, Qazi, IH, and Zeng, C-J (2018b). High throughput small RNA and transcriptome sequencing reveal capacitation-related microRNAs and mRNA in boar sperm. BMC Genomics 19, 736.
| High throughput small RNA and transcriptome sequencing reveal capacitation-related microRNAs and mRNA in boar sperm.Crossref | GoogleScholarGoogle Scholar | 30305024PubMed |
Liu, W-M, Pang, RTK, Chiu, PCN, Wong, BPC, Lao, K, Lee, K-F, and Yeung, WSB (2012). Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proceedings of the National Academy of Sciences 109, 490–494.
| Sperm-borne microRNA-34c is required for the first cleavage division in mouse.Crossref | GoogleScholarGoogle Scholar |
Locati, MD, Pagano, JFB, Abdullah, F, Ensink, WA, van Olst, M, van Leeuwen, S, Nehrdich, U, Spaink, HP, Rauwerda, H, Jonker, MJ, Dekker, RJ, and Breit, TM (2018). Identifying small RNAs derived from maternal- and somatic-type rRNAs in zebrafish development. Genome 61, 371–378.
| Identifying small RNAs derived from maternal- and somatic-type rRNAs in zebrafish development.Crossref | GoogleScholarGoogle Scholar | 29425468PubMed |
Loher, P, Londin, ER, and Rigoutsos, I (2014). IsomiR expression profiles in human lymphoblastoid cell lines exhibit population and gender dependencies. Oncotarget 5, 8790–8802.
| IsomiR expression profiles in human lymphoblastoid cell lines exhibit population and gender dependencies.Crossref | GoogleScholarGoogle Scholar | 25229428PubMed |
Maute, RL, Schneider, C, Sumazin, P, Holmes, A, Califano, A, Basso, K, and Dalla-Favera, R (2013). tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proceedings of the National Academy of Sciences 110, 1404–1409.
| tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma.Crossref | GoogleScholarGoogle Scholar |
Menezes, ESB, Badial, PR, El Debaky, H, Husna, AU, Ugur, MR, Kaya, A, Topper, E, Bulla, C, Grant, KE, Bolden-Tiller, O, Moura, AA, and Memili, E (2020). Sperm miR-15a and miR-29b are associated with bull fertility. Andrologia 52, e13412.
| Sperm miR-15a and miR-29b are associated with bull fertility.Crossref | GoogleScholarGoogle Scholar | 31671225PubMed |
Momeni, A, Najafipour, R, Hamta, A, Jahani, S, and Moghbelinejad, S (2020). Expression and methylation pattern of hsa-miR-34 family in sperm samples of infertile men. Reproductive Sciences 27, 301–308.
| Expression and methylation pattern of hsa-miR-34 family in sperm samples of infertile men.Crossref | GoogleScholarGoogle Scholar | 32046388PubMed |
Morikawa, Y, and Cserjesi, P (2004). Extra-embryonic vasculature development is regulated by the transcription factor HAND1. Development 131, 2195–2204.
| Extra-embryonic vasculature development is regulated by the transcription factor HAND1.Crossref | GoogleScholarGoogle Scholar | 15073150PubMed |
Muñoz, X, Mata, A, Bassas, L, and Larriba, S (2015). Altered miRNA signature of developing germ-cells in infertile patients relates to the severity of spermatogenic failure and persists in spermatozoa. Scientific Reports 5, 17991–17991.
| Altered miRNA signature of developing germ-cells in infertile patients relates to the severity of spermatogenic failure and persists in spermatozoa.Crossref | GoogleScholarGoogle Scholar | 26648257PubMed |
Nätt, D, Kugelberg, U, Casas, E, Nedstrand, E, Zalavary, S, Henriksson, P, Nijm, C, Jäderquist, J, Sandborg, J, Flinke, E, Ramesh, R, Örkenby, L, Appelkvist, F, Lingg, T, Guzzi, N, Bellodi, C, Löf, M, Vavouri, T, and Öst, A (2019). Human sperm displays rapid responses to diet. PLoS Biology 17, e3000559.
| Human sperm displays rapid responses to diet.Crossref | GoogleScholarGoogle Scholar | 31877125PubMed |
Niu, Z, Goodyear, SM, Rao, S, Wu, X, Tobias, JW, Avarbock, MR, and Brinster, RL (2011). MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences 108, 12740–12745.
| MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells.Crossref | GoogleScholarGoogle Scholar |
Nixon, B, Stanger, SJ, Mihalas, BP, Reilly, JN, Anderson, AL, Tyagi, S, Holt, JE, and McLaughlin, EA (2015). The MicroRNA signature of mouse spermatozoa is substantially modified during epididymal maturation. Biology of Reproduction 93, 91.
| The MicroRNA signature of mouse spermatozoa is substantially modified during epididymal maturation.Crossref | GoogleScholarGoogle Scholar | 26333995PubMed |
Nixon, B, De Iuliis, GN, Dun, MD, Zhou, W, Trigg, NA, and Eamens, AL (2019a). Profiling of epididymal small non-protein-coding RNAs. Andrology 7, 669–680.
| Profiling of epididymal small non-protein-coding RNAs.Crossref | GoogleScholarGoogle Scholar | 31020794PubMed |
Nixon, B, De Iuliis, GN, Hart, HM, Zhou, W, Mathe, A, Bernstein, IR, Anderson, AL, Stanger, SJ, Skerrett-Byrne, DA, Jamaluddin, MFB, Almazi, JG, Bromfield, EG, Larsen, MR, and Dun, MD (2019b). Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation. Molecular & Cellular Proteomics 18, S91–S108.
| Proteomic Profiling of Mouse Epididymosomes Reveals their Contributions to Post-testicular Sperm Maturation.Crossref | GoogleScholarGoogle Scholar |
O’Brien, J, Hayder, H, Zayed, Y, and Peng, C (2018). Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Frontiers in Endocrinology 9, 402.
| Overview of MicroRNA biogenesis, mechanisms of actions, and circulation.Crossref | GoogleScholarGoogle Scholar | 30123182PubMed |
Ostermeier, GC, Miller, D, Huntriss, JD, Diamond, MP, and Krawetz, SA (2004). Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429, 154.
| Reproductive biology: delivering spermatozoan RNA to the oocyte.Crossref | GoogleScholarGoogle Scholar | 15141202PubMed |
Paris, Z, Fleming, IMC, and Alfonzo, JD (2012). Determinants of tRNA editing and modification: avoiding conundrums, affecting function. Seminars in Cell & Developmental Biology 23, 269–274.
| Determinants of tRNA editing and modification: avoiding conundrums, affecting function.Crossref | GoogleScholarGoogle Scholar |
Paul, P, Chakraborty, A, Sarkar, D, Langthasa, M, Rahman, M, Bari, M, Singha, RS, Malakar, AK, and Chakraborty, S (2018). Interplay between miRNAs and human diseases. Journal of Cellular Physiology 233, 2007–2018.
| Interplay between miRNAs and human diseases.Crossref | GoogleScholarGoogle Scholar | 28181241PubMed |
Penzo, M, Galbiati, A, Treré, D, and Montanaro, L (2016). The importance of being (slightly) modified: the role of rRNA editing on gene expression control and its connections with cancer. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer 1866, 330–338.
| The importance of being (slightly) modified: the role of rRNA editing on gene expression control and its connections with cancer.Crossref | GoogleScholarGoogle Scholar |
Perkins SD, Keel BN, Northrop EJ, McDaneld TG, Cushman RA, Harstine BR, DeJarnette JM, Utt MD, Perry GA (2020) Influence of microRNAs from semen on bovine fertility. In ‘Society for the Study of Reproduction Annual Meeting. Abstract Program’. pp. 181–182. (South Dakota State University: Brookings, SD, USA)
Picardi, E, Manzari, C, Mastropasqua, F, Aiello, I, D’Erchia, AM, and Pesole, G (2016). Corrigendum: Profiling RNA editing in human tissues: towards the inosinome Atlas. Scientific Reports 6, 20755.
| Corrigendum: Profiling RNA editing in human tissues: towards the inosinome Atlas.Crossref | GoogleScholarGoogle Scholar | 26854421PubMed |
Pillai, RS, and Chuma, S (2012). piRNAs and their involvement in male germline development in mice. Development, Growth & Differentiation 54, 78–92.
| piRNAs and their involvement in male germline development in mice.Crossref | GoogleScholarGoogle Scholar |
Raina, M, and Ibba, M (2014). tRNAs as regulators of biological processes. Frontiers in Genetics 5, 171.
| tRNAs as regulators of biological processes.Crossref | GoogleScholarGoogle Scholar | 24966867PubMed |
Reilly, JN, McLaughlin, EA, Stanger, SJ, Anderson, AL, Hutcheon, K, Church, K, Mihalas, BP, Tyagi, S, Holt, JE, Eamens, AL, and Nixon, B (2016). Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Scientific Reports 6, 31794.
| Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome.Crossref | GoogleScholarGoogle Scholar | 27549865PubMed |
Rejraji, H, Sion, B, Prensier, G, Carreras, M, Motta, C, Frenoux, J-M, Vericel, E, Grizard, G, Vernet, P, and Drevet, JR (2006). Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biology of Reproduction 74, 1104–1113.
| Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation.Crossref | GoogleScholarGoogle Scholar | 16510839PubMed |
Romero, Y, Meikar, O, Papaioannou, MD, Conne, B, Grey, C, Weier, M, Pralong, F, De Massy, B, Kaessmann, H, Vassalli, J-D, Kotaja, N, and Nef, S (2011). Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS One 6, e25241.
| Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects.Crossref | GoogleScholarGoogle Scholar | 21998645PubMed |
Rowlison, T, Ottinger, MA, and Comizzoli, P (2018). Key factors enhancing sperm fertilizing ability are transferred from the epididymis to the spermatozoa via epididymosomes in the domestic cat model. Journal of Assisted Reproduction and Genetics 35, 221–228.
| Key factors enhancing sperm fertilizing ability are transferred from the epididymis to the spermatozoa via epididymosomes in the domestic cat model.Crossref | GoogleScholarGoogle Scholar | 29134478PubMed |
Russell, SJ, Stalker, L, Gilchrist, G, Backx, A, Molledo, G, Foster, RA, and LaMarre, J (2016). Identification of PIWIL1 isoforms and their expression in bovine testes, oocytes, and early embryos. Biology of Reproduction 94, 75.
| Identification of PIWIL1 isoforms and their expression in bovine testes, oocytes, and early embryos.Crossref | GoogleScholarGoogle Scholar | 26911426PubMed |
Salas-Huetos, A, Blanco, J, Vidal, F, Godo, A, Grossmann, M, Pons, MC, F-Fernández, S, Garrido, N, and Anton, E (2015). Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile. Fertility and Sterility 104, 591–601.
| Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile.Crossref | GoogleScholarGoogle Scholar | 26143365PubMed |
Salas-Huetos, A, Blanco, J, Vidal, F, Grossmann, M, Pons, MC, Garrido, N, and Anton, E (2016). Spermatozoa from normozoospermic fertile and infertile individuals convey a distinct miRNA cargo. Andrology 4, 1028–1036.
| Spermatozoa from normozoospermic fertile and infertile individuals convey a distinct miRNA cargo.Crossref | GoogleScholarGoogle Scholar | 27676136PubMed |
Savva, YA, Rieder, LE, and Reenan, RA (2012). The ADAR protein family. Genome Biology 13, 252.
| The ADAR protein family.Crossref | GoogleScholarGoogle Scholar | 23273215PubMed |
Schorn, AJ, Gutbrod, MJ, LeBlanc, C, and Martienssen, R (2017). LTR-Retrotransposon Control by tRNA-Derived Small RNAs. Cell 170, 61–71.e11.
| LTR-Retrotransposon Control by tRNA-Derived Small RNAs.Crossref | GoogleScholarGoogle Scholar | 28666125PubMed |
Sellem, E, Broekhuijse, MLWJ, Chevrier, L, Camugli, S, Schmitt, E, Schibler, L, and Koenen, EPC (2015). Use of combinations of in vitro quality assessments to predict fertility of bovine semen. Theriogenology 84, 1447–1454.e5.
| Use of combinations of in vitro quality assessments to predict fertility of bovine semen.Crossref | GoogleScholarGoogle Scholar | 26296523PubMed |
Sellem, E, Marthey, S, Rau, A, Jouneau, L, Bonnet, A, Perrier, J-P, Fritz, S, Le Danvic, C, Boussaha, M, Kiefer, H, Jammes, H, and Schibler, L (2020). A comprehensive overview of bull sperm-borne small non-coding RNAs and their diversity across breeds. Epigenetics & Chromatin 13, 19.
| A comprehensive overview of bull sperm-borne small non-coding RNAs and their diversity across breeds.Crossref | GoogleScholarGoogle Scholar |
Sellem, E, Marthey, S, Rau, A, Jouneau, L, Bonnet, A, Le Danvic, C, Guyonnet, B, Kiefer, H, Jammes, H, and Schibler, L (2021). Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm. Epigenetics & Chromatin 14, 24.
| Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm.Crossref | GoogleScholarGoogle Scholar |
Sendler, E, Johnson, GD, Mao, S, Goodrich, RJ, Diamond, MP, Hauser, R, and Krawetz, SA (2013). Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Research 41, 4104–4117.
| Stability, delivery and functions of human sperm RNAs at fertilization.Crossref | GoogleScholarGoogle Scholar | 23471003PubMed |
Sharma, U (2019). Paternal contributions to offspring health: role of sperm small RNAs in intergenerational transmission of epigenetic information. Frontiers in Cell and Developmental Biology 7, 215.
| Paternal contributions to offspring health: role of sperm small RNAs in intergenerational transmission of epigenetic information.Crossref | GoogleScholarGoogle Scholar | 31681757PubMed |
Sharma, U, Conine, CC, Shea, JM, Boskovic, A, Derr, AG, Bing, XY, Belleannee, C, Kucukural, A, Serra, RW, Sun, F, Song, L, Carone, BR, Ricci, EP, Li, XZ, Fauquier, L, Moore, MJ, Sullivan, R, Mello, CC, Garber, M, and Rando, OJ (2016). Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351, 391–396.
| Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 26721685PubMed |
Sharma, U, Sun, F, Conine, CC, Reichholf, B, Kukreja, S, Herzog, VA, Ameres, SL, and Rando, OJ (2018). Small RNAs are trafficked from the epididymis to developing Mammalian sperm. Developmental Cell 46, 481–494.e6.
| Small RNAs are trafficked from the epididymis to developing Mammalian sperm.Crossref | GoogleScholarGoogle Scholar | 30057273PubMed |
Shi, S, Shi, Q, and Sun, Y (2020). The effect of sperm miR-34c on human embryonic development kinetics and clinical outcomes. Life Sciences 256, 117895.
| The effect of sperm miR-34c on human embryonic development kinetics and clinical outcomes.Crossref | GoogleScholarGoogle Scholar | 32502545PubMed |
Sullivan, R, Frenette, G, and Girouard, J (2007). Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian Journal of Andrology 9, 483–491.
| Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit.Crossref | GoogleScholarGoogle Scholar | 17589785PubMed |
Tan, GC, and Dibb, N (2015). IsomiRs have functional importance. The Malaysian Journal of Pathology 37, 73–81.
| 26277662PubMed |
Tan, GC, Chan, E, Molnar, A, Sarkar, R, Alexieva, D, Isa, IM, Robinson, S, Zhang, S, Ellis, P, Langford, CF, Guillot, PV, Chandrashekran, A, Fisk, NM, Castellano, L, Meister, G, Winston, RM, Cui, W, Baulcombe, D, and Dibb, NJ (2014). 5′ isomiR variation is of functional and evolutionary importance. Nucleic Acids Research 42, 9424–9435.
| 5′ isomiR variation is of functional and evolutionary importance.Crossref | GoogleScholarGoogle Scholar | 25056318PubMed |
Telonis, AG, Loher, P, Honda, S, Jing, Y, Palazzo, J, Kirino, Y, and Rigoutsos, I (2015a). Dissecting tRNA-derived fragment complexities using personalized transcriptomes reveals novel fragment classes and unexpected dependencies. Oncotarget 6, 24797–24822.
| Dissecting tRNA-derived fragment complexities using personalized transcriptomes reveals novel fragment classes and unexpected dependencies.Crossref | GoogleScholarGoogle Scholar | 26325506PubMed |
Telonis, AG, Loher, P, Jing, Y, Londin, E, and Rigoutsos, I (2015b). Beyond the one-locus-one-miRNA paradigm: microRNA isoforms enable deeper insights into breast cancer heterogeneity. Nucleic Acids Research 43, 9158–9175.
| Beyond the one-locus-one-miRNA paradigm: microRNA isoforms enable deeper insights into breast cancer heterogeneity.Crossref | GoogleScholarGoogle Scholar | 26400174PubMed |
Telonis, AG, Magee, R, Loher, P, Chervoneva, I, Londin, E, and Rigoutsos, I (2017). Knowledge about the presence or absence of miRNA isoforms (isomiRs) can successfully discriminate amongst 32 TCGA cancer types. Nucleic Acids Research 45, 2973–2985.
| Knowledge about the presence or absence of miRNA isoforms (isomiRs) can successfully discriminate amongst 32 TCGA cancer types.Crossref | GoogleScholarGoogle Scholar | 28206648PubMed |
Tian, H, Li, Z, Peng, D, Bai, X, and Liang, W (2017). Expression difference of miR-10b and miR-135b between the fertile and infertile semen samples (p). Forensic Science International: Genetics Supplement Series 6, e257–e259.
| Expression difference of miR-10b and miR-135b between the fertile and infertile semen samples (p).Crossref | GoogleScholarGoogle Scholar |
Trigg, NA, Eamens, AL, and Nixon, B (2019). The contribution of epididymosomes to the sperm small RNA profile. Reproduction 157, R209–R223.
| The contribution of epididymosomes to the sperm small RNA profile.Crossref | GoogleScholarGoogle Scholar | 30780129PubMed |
Vashisht, A, and Gahlay, GK (2020). Using miRNAs as diagnostic biomarkers for male infertility: opportunities and challenges. Molecular Human Reproduction 26, 199–214.
| Using miRNAs as diagnostic biomarkers for male infertility: opportunities and challenges.Crossref | GoogleScholarGoogle Scholar | 32084276PubMed |
Vincent P, Underwood SL, Dolbec C, Bouchard N, Kroetsch T, Blondin P (2014) Bovine semen quality control in artificial insemination centers. In ‘Bovine reproduction’. (Ed. RM Hopper) pp. 685–695. (John Wiley & Sons, Inc: Hoboken, NJ, USA)
Vojtech, L, Woo, S, Hughes, S, Levy, C, Ballweber, L, Sauteraud, RP, Strobl, J, Westerberg, K, Gottardo, R, Tewari, M, and Hladik, F (2014). Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Research 42, 7290–7304.
| Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions.Crossref | GoogleScholarGoogle Scholar | 24838567PubMed |
Wei, H, Zhou, B, Zhang, F, Tu, Y, Hu, Y, Zhang, B, and Zhai, Q (2013). Profiling and identification of small rDNA-derived RNAs and their potential biological functions. PLoS One 8, e56842.
| Profiling and identification of small rDNA-derived RNAs and their potential biological functions.Crossref | GoogleScholarGoogle Scholar | 23418607PubMed |
Wei, J-W, Huang, K, Yang, C, and Kang, C-S (2017). Non-coding RNAs as regulators in epigenetics (Review). Oncology Reports 37, 3–9.
| Non-coding RNAs as regulators in epigenetics (Review).Crossref | GoogleScholarGoogle Scholar | 27841002PubMed |
Weick, E-M, and Miska, EA (2014). piRNAs: from biogenesis to function. Development 141, 3458–3471.
| piRNAs: from biogenesis to function.Crossref | GoogleScholarGoogle Scholar | 25183868PubMed |
Wightman, B, Ha, I, and Ruvkun, G (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862.
| Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans.Crossref | GoogleScholarGoogle Scholar | 8252622PubMed |
Xu, H, Wang, X, Wang, Z, Li, J, Xu, Z, Miao, M, Chen, G, Lei, X, Wu, J, Shi, H, Wang, K, Zhang, T, and Sun, X (2020). MicroRNA expression profile analysis in sperm reveals hsa-mir-191 as an auspicious omen of in vitro fertilization. BMC Genomics 21, 165.
| MicroRNA expression profile analysis in sperm reveals hsa-mir-191 as an auspicious omen of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 32066367PubMed |
Yang, Q-E, Racicot, KE, Kaucher, AV, Oatley, MJ, and Oatley, JM (2013). MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells. Development 140, 280–290.
| MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells.Crossref | GoogleScholarGoogle Scholar | 23221369PubMed |
Yang, X-Z, Chen, J-Y, Liu, C-J, Peng, J, Wee, YR, Han, X, Wang, C, Zhong, X, Shen, QS, Liu, H, Cao, H, Chen, X-W, Tan, BC-M, and Li, C-Y (2015). Selectively constrained RNA editing regulation crosstalks with piRNA biogenesis in primates. Molecular Biology and Evolution 32, 3143–3157.
| Selectively constrained RNA editing regulation crosstalks with piRNA biogenesis in primates.Crossref | GoogleScholarGoogle Scholar | 26341297PubMed |
Yu, M, Mu, H, Niu, Z, Chu, Z, Zhu, H, and Hua, J (2014). miR-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2. Journal of Cellular Biochemistry 115, 232–242.
| miR-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2.Crossref | GoogleScholarGoogle Scholar | 24038201PubMed |
Yuan, S, Tang, C, Zhang, Y, Wu, J, Bao, J, Zheng, H, Xu, C, and Yan, W (2015). mir-34b/c and mir-449a/b/c are required for spermatogenesis, but not for the first cleavage division in mice. Biology Open 4, 212–223.
| mir-34b/c and mir-449a/b/c are required for spermatogenesis, but not for the first cleavage division in mice.Crossref | GoogleScholarGoogle Scholar | 25617420PubMed |
Zhang, Y, Shi, J, Rassoulzadegan, M, Tuorto, F, and Chen, Q (2019). Sperm RNA code programmes the metabolic health of offspring. Nature Reviews Endocrinology 15, 489–498.
| Sperm RNA code programmes the metabolic health of offspring.Crossref | GoogleScholarGoogle Scholar | 31235802PubMed |
Zhao, S, Gou, L-T, Zhang, M, Zu, L-D, Hua, M-M, Hua, Y, Shi, H-J, Li, Y, Li, J, Li, D, Wang, E-D, and Liu, M-F (2013). piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis. Developmental Cell 24, 13–25.
| piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 23328397PubMed |
Zheng, Y, Ji, B, Song, R, Wang, S, Li, T, Zhang, X, Chen, K, Li, T, and Li, J (2016). Accurate detection for a wide range of mutation and editing sites of microRNAs from small RNA high-throughput sequencing profiles. Nucleic Acids Research 44, e123.
| Accurate detection for a wide range of mutation and editing sites of microRNAs from small RNA high-throughput sequencing profiles.Crossref | GoogleScholarGoogle Scholar | 27229138PubMed |
Zhou, W, De Iuliis, GN, Dun, MD, and Nixon, B (2018). Characteristics of the epididymal luminal environment responsible for sperm maturation and storage. Frontiers in Endocrinology 9, 59.
| Characteristics of the epididymal luminal environment responsible for sperm maturation and storage.Crossref | GoogleScholarGoogle Scholar | 29541061PubMed |
Zinshteyn, B, and Nishikura, K (2009). Adenosine-to-inosine RNA editing. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 1, 202–209.
| Adenosine-to-inosine RNA editing.Crossref | GoogleScholarGoogle Scholar | 20835992PubMed |
