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Comparative expression analysis of let-7 microRNAs during ovary development in Megalobrama amblycephala

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Abstract

As a critical regulator of gene expression, let-7 family miRNAs have been reported to be involved in multiple physiological processes. In this study, in order to elucidate the putative regulatory effect of let-7 miRNAs during fish gonadal development and to identify which member is crucial for this regulation, the expression of ten members including let-7a/b/c/d/e/f/g/h/i/j were quantified in ovary, pituitary, and brain tissues during the different ovarian developmental stages of blunt snout bream Megalobrama amblycephala. According to the data from analysis of expression patterns, let-7a showed the highest expression value in almost all the tested ovaries, pituitaries, and brains, with let-7b and let-7d moderately expressed, following by other let-7 miRNAs. In terms of the differential expression levels of ten let-7 miRNAs at each developmental stage, the results showed that let-7a/b/d/f/h expression gradually increased during the ovary development from stage I to V and dropped significantly at the phase VI in ovary tissues. However, the expression of let-7a/b/e/f in pituitary increased during the ovary development from stage I to IV and declined at stage V. Among all the let-7 miRNAs, let-7a/b/d had the highest expression and their expression patterns were consistent with the gonad development of M. amblycephala. Furthermore, the mostly predicted target genes of let-7 miRNAs are significantly enriched in signaling pathways closely related to gonadal development through KEGG enrichment analysis. These results indicate that let-7 miRNA members, especially let-7a/b/d, may play important roles in the regulation of ovary development in M. amblycephala through negatively regulating expression of their target genes.

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References

  • Ahn HW, Morin RD, Zhao H, Harris RA, Coarfa C, Chen ZJ, Milosavljevic A, Marra MA, Rajkovic A (2010) MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing. Mol Hum Reprod 16:463–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alajez NM, Shi W, Wong D, Lenarduzzi M, Waldron J, Weinreb I (2012) Lin28b promotes head and neck cancer progression via modulation of the insulin-like growth factor survival pathway. Oncotarget 3:1641–1652

    Article  PubMed  PubMed Central  Google Scholar 

  • Alvarezgarcia I, Miska EA (2005) MicroRNA functions in animal development and human disease. Development 132:4653–4662

    Article  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Baumgarten SC, Armouti M, Ko C, Stocco C (2017) IGF1R expression in ovarian granulosa cells is essential for steroidogenesis, follicle survival, and fertility in female mice. Endocrinology 158(7):2309–2318

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao R, Wu WJ, Zhou XL, Xiao P, Wang Y, Liu HL (2015) Expression and preliminary functional profiling of the let-7 family during porcine ovary follicle atresia. Mol Cell 38:304–311

    Article  CAS  Google Scholar 

  • Dweep H, Gretz N, Sticht C (2014) miRWalk database for miRNA-target interactions. Methods Mol Biol 1182:289–305

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Gao L, Shi Z, You F, Zhang J, Li W (2018) Characterization and expression of lin-28a involved in lin28/let-7 signal pathway during early development of P. olivaceus. Fish Physiol Biochem 44:451–463

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Shi Z, Wu M, Zhang J, Liang J, Chen X (2011) Identification and differential expression of microRNAs during metamorphosis of the Japanese flounder (Paralichthys olivaceus). PLoS One 6:e22957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilchrist GC, Allison T, Thomas N, Daniele M, Jonathan LM (2016) MicroRNA expression during bovine oocyte maturation and fertilization. Int J Mol Sci 17:396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain MM, Ghanem N, Hoelker M (2009) Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genomics 10:443–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CX, Chen N, Wu XJ, He Y, Huang CH, Liu H (2017) Zebrafish let-7b acts downstream of hypoxia-inducible factor-1α to assist in hypoxia-mediated cell proliferation and cell cycle regulation. Life Sci 171:21–29

    Article  CAS  PubMed  Google Scholar 

  • Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A (2007) A mammalian microRNA expression atlas based on small rna library sequencing. Cell 129:1401–1414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Liu Y, Wang T, Guan J, Luo Z, Chen H (2011) Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing. Int J Biol Sci 7:1045–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao K, Chai ZX, Zhang SY, Zhong JC (2016) Differential expression and function prediction of mir-383 in yak and cattle-yak testis. China Anim Husb Vet Med 43(2):319–325

  • Lin S, Li H, Mu H, Wen L, Ying L, Jia X (2012) Let-7b regulates the expression of the growth hormone receptor gene in deletion-type dwarf chickens. BMC Genomics 13:1–10

    Article  CAS  Google Scholar 

  • Liu J, Luo M, Sheng Y, Hong Q, Cheng H, Zhou R (2015) Dynamic evolution and biogenesis of small RNAs during sex reversal. Sci Rep-UK 5:9999

    Article  CAS  Google Scholar 

  • Luo MM, Hao LL, Hu F, Dong YN, Gou LX, Zhang WD (2015) MicroRNA profiles and potential regulatory pattern during the early stage of spermatogenesis in mice. Sci China Life Sci 58:442–450

    Article  CAS  PubMed  Google Scholar 

  • Mcbride D, Carré W, Sontakke SD, Hogg CO, Law A, Donadeu FX (2012) Identification of miRNAs associated with the follicular-luteal transition in the ruminant ovary. Reproduction 144:221

    Article  CAS  PubMed  Google Scholar 

  • Mei J, Yan W, Fang J, Yuan G, Chen N, He Y (2014) Identification of a gonad-expression differential gene insulin-like growth factor-1 receptor (Igf1r) in the swamp eel (Monopterus albus). Fish Physiol Biochem 40(4):1181–1190

    CAS  PubMed  Google Scholar 

  • Miles JR, Mcdaneld TG, Wiedmann RT, Cushman RA, Echternkamp SE, Vallet JL (2012) MicroRNA expression profile in bovine cumulus-oocyte complexes: possible role of let-7 and mir-106a in the development of bovine oocytes. Anim Reprod Sci 130:16–26

    Article  CAS  PubMed  Google Scholar 

  • Pépin D, Vanderhyden BC, Picketts DJ, Murphy BD (2007) ISWI chromatin remodeling in ovarian somatic and germ cells: revenge of the NURFs. Trends Endocrinol Metab 18:215–224

    Article  CAS  PubMed  Google Scholar 

  • Rehnitz J, Alcoba DD, Brum IS, Hinderhofer K, Youness B, Strowitzki T, Vogt PH (2017) FMR1 and AKT/mTOR signalling pathways: potential functional interactions controlling folliculogenesis in human granulosa cells. Reprod BioMed Online 35(5):485–493

    Article  CAS  PubMed  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906

    Article  CAS  PubMed  Google Scholar 

  • Ro S, Song R, Park C (2007) Cloning and expression profiling of small RNAs expressed in the mouse ovary. RNA 13:2366–2380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen G, Wu R, Liu B, Dong W, Tu Z, Yang J, Xu Z, Pan T (2014) Upstream and downstream mechanisms for the promoting effects of IGF-1 on differentiation of spermatogonia to primary spermatocytes. Life Sci 101:49–55

    Article  CAS  PubMed  Google Scholar 

  • Sirotkin A, Ovcharenko DR, Laukova M, Mlyncek M (2009) Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. Cell Physiol 219:415–420

    Article  CAS  Google Scholar 

  • Tao W, Sun L, Shi H (2016) Integrated analysis of miRNA and mRNA expression profiles in tilapia gonads at an early stage of sex differentiation. BMC Genomics 17:328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toledano H, D'Alterio C, Czech B, Levine E, Jones DL (2012) The let-7-imp axis regulates ageing of the drosophila testis stem-cell niche. Nature 485:605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong C, Tian F, Zhang C, Zhao K (2017) The microRNA repertoire of Tibetan naked carp Gymnocypris przewalskii: a case study in schizothoracinae fish on the Tibetan plateau. PLoS One 12:e0174534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen J, Gao Z, Luo W, Tong J, Wang W (2013) Observation of gonad at different development stages and expression analysis of kiss2/kiss2r genes in Megalobrama amblycephala. S China Fish Sci 9:44–50

    CAS  Google Scholar 

  • Xiao J, Zhong H, Zhou Y, Yu F, Gao Y, Luo Y (2014) Identification and characterization of microRNAs in ovary and testis of Nile tilapia (Oreochromis niloticus) by using solexa sequencing technology. PLoS One 9:e86821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Z, Chen J, Li X, Ge J, Pan J, Xu X (2013) Identification and characterization of microRNAs in channel catfish (Ictalurus punctatus) by using Solexa sequencing technology. PLoS One 8:e54174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Sun TC, Zhang AL, Jia-Qi LI (2014) Progress on the research of ovarian miRNA. Chin J Anim Vet Sci 45:509–516

  • Yi S, Gao ZX, Zhao H, Zeng C, Luo W, Chen B (2013) Identification and characterization of microRNAs involved in growth of blunt snout bream (Megalobrama amblycephala) by Solexa sequencing. BMC Genomics 14:754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XD, Zhang YH, Ling YH, Liu Y, Cao HG, Yin ZJ (2013) Characterization and differential expression of microRNAs in the ovaries of pregnant and non-pregnant goats (Capra hircus). BMC Genomics 14:157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao B, Zhao H, Yang Z, Zhao YGY, Wang W, Gao Z (2015) Morphological characteristics and gonadal development of Megalobrama amblycephala(♀)×Parabramis pekinesis (♂)hybrids. J Huazhong Agric Univ 34:89–96

    Google Scholar 

  • Zhao BW, Zhou LF, Liu YL, Wan SM, Gao ZX (2017) Evolution of fish let-7 microRNAs and their expression correlated to growth development in blunt snout bream. Int J Mol Sci 18:646

    Article  CAS  PubMed Central  Google Scholar 

  • Zhu YP, Xue W, Wang JT, Wan YM, Wang SL, Xu P (2012) Identification of common carp (Cyprinus carpio) microRNAs and microRNA-related SNPs. BMC Genomics 13:413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was financially supported by the National Natural Science Foundation of China (Grant No. 31872559), National Key Research and Development Program (Grant No. 2018YFD0900205), Modern Agriculture Industry Technology System Construction Projects of China titled as-Staple Freshwater Fishes Industry Technology System (Grant No. CARS-46-08), and Fundamental Research Funds for the Central Universities (Grant No. 2662018PY035).

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Author notes

  1. Tian Lan and Yu-Long Chen contributed equally to this work.

Authors and Affiliations

  1. College of Fisheries, Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, Key Lab of Freshwater Animal Breeding, Ministry of Agriculture, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Tian Lan, Yu-Long Chen, Bo-Wen Zhao & Ze-Xia Gao

  2. Collaborative Innovation Center for Healthy Freshwater Aquaculture of Hubei Province, Hubei Provincial Engineering Laboratory for Pond Aquaculture, Wuhan, 430070, China

    Tian Lan, Yu-Long Chen, Bo-Wen Zhao & Ze-Xia Gao

  3. Department of Zoology, Government College Women University, Faisalabad, 38860, Pakistan

    Yasmeen Gul

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  1. Tian Lan
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  2. Yu-Long Chen
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  3. Yasmeen Gul
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  4. Bo-Wen Zhao
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  5. Ze-Xia Gao
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Correspondence to Ze-Xia Gao.

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All animals and experiments were conducted in accordance with the “Guidelines for Experimental Animals” of the Ministry of Science and Technology (Beijing, China). The study was approved by the Institutional Animal Care and Use Ethics Committee of Huazhong Agricultural University. All efforts were made to minimize suffering. All experimental procedures involving fish were approved by the institution animal care and use committee of the Huazhong Agricultural University.

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Lan, T., Chen, YL., Gul, Y. et al. Comparative expression analysis of let-7 microRNAs during ovary development in Megalobrama amblycephala. Fish Physiol Biochem 45, 1101–1115 (2019). https://doi.org/10.1007/s10695-019-00624-7

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