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The Mantle Exosome and MicroRNAs of Hyriopsis cumingii Involved in Nacre Color Formation

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Abstract

The nacre color of shells has an effect on the pearl color in Hyriopsis cumingii and is an important indicator for its value. The nacre is part of the shell, and some studies have shown that exosomes of the mantle are involved in the formation of shells. Most of the RNA contained in exosomes are microRNAs (miRNAs); however, little information is available on the roles of exosomes and miRNAs on the formation of nacre color in mussels. In this study, exosomes of mantles were extracted from white and purple mussels. High-throughput Illumina sequencing was performed on the white and purple mussel mantle exosomes, and 7,665,167 and 10,994,115 reads were harvested. Using the standard of |log2(Fold change)| ≥ 2, and a p value ≤ 0.05, a total of 54 differentially expressed miRNAs were identified. The miRNAs that regulated the target genes (hcApo, HcTyr, HcTyp-1, HcMitf, HcSRCR1, and HcSRCR2) involved in shell color formation were predicted. Moreover, miR-15b negatively regulated hcApo, which plays important roles in the absorption and transport of β-carotene in H. cumingii. These results improve our understanding of the molecular mechanisms of nacre color formation in H. cumingii.

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References

  • Alipoor SD, Mortaz E, Garssen J, Movassaghi M, Mirsaeidi M, Adcock IM (2016) Exosomes and exosomal miRNA in respiratory diseases. Mediat Inflamm 2016:5628404

    Article  CAS  Google Scholar 

  • Bai Z, Lin J, Ma K, Wang G, Niu D, Li J (2014) Identification of housekeeping genes suitable for gene expression analysis in the pearl mussel, Hyriopsis cumingii, during biomineralization. Mol Genet Genomics 289:717–725

    Article  CAS  PubMed  Google Scholar 

  • Barry PH, Diamond JM (1971) A theory of ion permeation through membranes with fixed neutral sites. J Membr Biol 4:295–330

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Boyiadzis M, Whiteside TL (2015) Information transfer by exosomes: a new frontier in hematologic malignancies. Blood Rev 29:281–290

    Article  CAS  PubMed  Google Scholar 

  • Capello M, Vykoukal JV, Katayama H, Bantis LE, Wang H, Kundnani DL, Aguilar-Bonavides C, Aguilar M, Tripathi SC, Dhillon DS, Momin AA, Peters H, Katz MH, Alvarez H, Bernard V, Ferri-Borgogno S, Brand R, Adler DG, Firpo MA, Mulvihill SJ, Molldrem JJ, Feng Z, Taguchi A, Maitra A, Hanash SM (2019) Exosomes harbor B cell targets in pancreatic adenocarcinoma and exert decoy function against complement-mediated cytotoxicity. Nat Commun 10:254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Liu X, Bai Z, Zhao L, Li J (2016) HcTyr and HcTyp-1 of Hyriopsis cumingii , novel tyrosinase and tyrosinase-related protein genes involved in nacre color formation. Comp Biochem Physiol B Biochem Mol Biol 204:1

    Article  CAS  PubMed  Google Scholar 

  • Clotilde T, Laurence Z, Sebastian A (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2:569–579

    Article  CAS  Google Scholar 

  • Colombo M, Raposo G, Théry C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Ann Rev Cell Dev Biol 30:255–289

    Article  CAS  Google Scholar 

  • Dong C, Wang H, Xue L, Dong Y, Yang L, Fan R, Yu X, Tian X, Ma S, Smith GW (2012) Coat color determination by miR-137 mediated down-regulation of microphthalmia-associated transcription factor in a mouse model. RNA 18:1679–1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5:R1

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Yang YB, Gao XC, Ren HT, Xiong JL, Sun XH (2017) Genome-wide identification and characterization of microRNAs and target prediction by computational approaches in common carp. Gene Rep 8:30–36

    Article  Google Scholar 

  • Hurwitz SN, Sun L, Cole KY, Ford CR 3rd, Olcese JM, Meckes DG Jr (2018) An optimized method for enrichment of whole brain-derived extracellular vesicles reveals insight into neurodegenerative processes in a mouse model of Alzheimer’s disease. J Neurosci Methods 307:210–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jan K, Marc R (2006) RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 34:451–454

    Article  CAS  Google Scholar 

  • Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262:9412–9420

    CAS  PubMed  Google Scholar 

  • Karnaukhov VN (1990) Carotenoids: recent progress, problems and prospects. Comp Biochem Physiol B Comp Biochem 95:1–20

    Article  CAS  Google Scholar 

  • Keller S, Sanderson MP, Stoeck A, Altevogt P (2006) Exosomes: from biogenesis and secretion to biological function. Immunol Lett 107:102–108

    Article  CAS  PubMed  Google Scholar 

  • Kennell JA, Cadigan KM, Shakhmantsir I, Waldron EJ (2012) The microRNA miR-8 is a positive regulator of pigmentation and eclosion in Drosophila. Dev Dyn 241:161–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koul A, Yogindran S, Sharma D, Kaul S, Rajam MV, Dhar MK (2016) Carotenoid profiling, in silico analysis and transcript profiling of miRNAs targeting carotenoid biosynthetic pathway genes in different developmental tissues of tomato. Plant Physiol Biochem 108:412–421

    Article  CAS  PubMed  Google Scholar 

  • Li X (2014) Expression of carotenoids accumulation related genes and effect on the color of shell nacre in Hyriopsis cumingii. Doctoral Thesis, Shanghai Ocean University

  • Li N, Hu J, Wang S, Cheng J, Hu X, Lu Z, Lin Z, Zhu W, Bao Z (2010) Isolation and identification of the main carotenoid pigment from the rare orange muscle of the Yesso scallop. Food Chem 118:616–619

    Article  CAS  Google Scholar 

  • Li X, Bai Z, Luo H, Liu Y, Wang G, Li J (2014) Cloning, differential tissue expression of a novel hcApo gene, and its correlation with total carotenoid content in purple and white inner-shell color pearl mussel Hyriopsis cumingii. Gene 538:258–265

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Bai Z, Han X, Li J (2017) Freshwater nucleated pearl quality is influenced by host mussel growth traits in Hyriopsis cumingii. Aquac Res 48:4656–4665

    Article  CAS  Google Scholar 

  • Liu Y, Xue L, Gao H, Chang L, Yu X, Zhu Z, He X, Geng J, Dong Y, Li H, Zhang L, Wang H (2019) Exosomal miRNA derived from keratinocytes regulates pigmentation in melanocytes. J Dermatol Sci 93:159–167

    Article  CAS  PubMed  Google Scholar 

  • Lötvall J, Hill AF, Hochberg F, Buzás EI, Vizio DD, Gardiner C, Yong SG, Kurochkin IV, Mathivanan S, Quesenberry P (2014) Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles 3:26913

    Article  PubMed  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J 17:10

    Article  Google Scholar 

  • Miyoshi T, Matsuda Y, Komatsu H (1987) Fluorescence from pearls to distinguish mother oysters used in pearl culture. Jpn J Appl Phys 26:578–581

  • Mount AS, Wheeler AP, Paradkar RP, Snider D (2004) Hemocyte-mediated shell mineralization in the eastern oyster. Science 304:297–300

    Article  CAS  PubMed  Google Scholar 

  • Mount AS, Gohad NV, Hansen DC, Mueller K, Johnstone MB (2010) Deposition of nanocrystalline calcite on surfaces by a tissue and cellular biomineralization. US patent 2010/0150982 A1

  • Neff JM (1972) Ultrastructural studies of periostracum formation in the hard shelled clam Mercenaria mercenaria (L). Tissue Cell 4:311–326

    Article  CAS  PubMed  Google Scholar 

  • Poggio M, Hu T, Pai C-C, Chu B, Belair CD, Chang A, Montabana E, Lang UE, Fu Q, Fong L, Blelloch R (2019) Suppression of exosomal PD-L1 induces systemic anti-tumor immunity and memory. Cell 177:414–427

  • Qiao Y, Zhang J, Zhang J, Wang Z, Ran A, Guo H, Wang D, Zhang J (2017) Integrated RNA-seq and sRNA-seq analysis reveals miRNA effects on secondary metabolism in Solanum tuberosum L. Mol Genet Genomics 292:37–52

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Huang D, Sun C, Li J, Bai Z (2018) Cloning of a microphthalmia-associated transcription factor gene and its functional analysis in nacre formation and melanin synthesis in Hyriopsis cumingii. Aquac Fish 3:217–224

    Article  Google Scholar 

  • Shi L, Liu X, Mao J, Han X (2014) Study of coloration mechanism of cultured freshwater pearls from mollusk Hyriopsis cumingii. J Appl Spectrosc 81:97–101

    Article  CAS  Google Scholar 

  • Suresh M, Fahner CJ, Reid GE, Simpson RJ (2012) ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 40:D1241

    Article  CAS  Google Scholar 

  • Tan F, Yin J (2005) Application of RNAi to cancer research and therapy. Front Biosci 10:1946–1960

    Article  CAS  PubMed  Google Scholar 

  • Tian X, Pang X, Wang L, Li M, Dong C, Ma X, Wang L, Song D, Feng J, Xu P, Li X (2018) Dynamic regulation of mRNA and miRNA associated with the developmental stages of skin pigmentation in Japanese ornamental carp. Gene 666:32–43

    Article  CAS  PubMed  Google Scholar 

  • Van Bennekum A, Werder M, Thuahnai ST, Chang-Hoon H, Phu D, Williams DL, Wettstein P, Schulthess G, Phillips MC, Hauser H (2005) Class B scavenger receptor-mediated intestinal absorption of dietary β-carotene and cholesterol. Biochemistry 44:4517–4525

    Article  CAS  PubMed  Google Scholar 

  • Vaz C, Ahmad HM, Sharma P, Gupta R, Kumar L, Kulshreshtha R, Bhattacharya A (2010) Analysis of microRNA transcriptome by deep sequencing of small RNA libraries of peripheral blood. BMC Genomics 11:288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vella LJ, Scicluna BJ, Cheng L, Bawden EG, Masters CL, Ang CS, Willamson N, McLean C, Barnham KJ, Hill AF (2017) A rigorous method to enrich for exosomes from brain tissue. J Extracell Vesicles 6:1348885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Victor A (2004) The functions of animal microRNAs. Nature 431:350–355

    Article  CAS  Google Scholar 

  • Wang GL, Yuan YM, Jia-Le LI (2007) SSR analysis of genetic diversity and phylogenetic relationships among different populations of Hyriopsis cumingii from the five lakes of China. J Fish China 12:12–18

    Google Scholar 

  • Wang L, Zhu W, Dong Z, Song F, Dong J, Fu J (2018) Comparative microRNA-seq analysis depicts candidate miRNAs involved in skin color differentiation in red tilapia. Int J Mol Sci 19

  • Xue M, Chen W, Xiang A, Wang R, Chen H, Pan J, Pang H, An H, Wang X, Hou H (2017) Hypoxic exosomes facilitate bladder tumor growth and development through transferring long non-coding RNA-UCA1. Mol Cancer 16:143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi L, Samir EA, Wood MJA (2012) Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21:125–134

    Article  CAS  Google Scholar 

  • Yin JQ, Wan Y (2002) RNA-mediated gene regulation system: now and the future (review). Int J Mol Med 10:355–365

    CAS  PubMed  Google Scholar 

  • Yonekura L, Nagao A (2007) Intestinal absorption of dietary carotenoids. Mol Nutr Food Res 51:107–115

    Article  CAS  PubMed  Google Scholar 

  • Ytrestøyl T, Coral-Hinostroza G, Hatlen B, Robb DHF, Bjerkeng B (2004) Carotenoid and lipid content in muscle of Atlantic salmon, Salmo salar, transferred to seawater as 0+ or 1+ smolts ☆. Comp Biochem Physiol B Biochem Mol Biol 138:29–40

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Xiaodong F, Ximing G, Li L, Ruibang L, Fei X, Pengcheng Y, Linlin Z, Xiaotong W, Haigang Q (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li S, Li L, Li M, Guo C, Yao J, Mi S (2015) Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 13:17–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng H, Liu H, Zhang T, Wang S, Sun Z, Liu W, Li Y (2010) Total carotenoid differences in scallop tissues of Chlamys nobilis (Bivalve: Pectinidae) with regard to gender and shell colour. Food Chem 122:1164–1167

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Cloud-Seq Biotech Ltd. Co. (Shanghai, China) for microRNA sequencing services and subsequent bioinformatics analyses.

Funding

This study was financially supported by the National Natural Science Foundation of China (31672654), National Key R&D Program of China (2018YFD0901406), and the Modern Agro-industry Technology Research System (CARS-49).

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Authors and Affiliations

  1. Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, Shanghai, 201306, China

    Xiajun Chen, Zhiyi Bai & Jiale Li

  2. National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, 201306, China

    Xiajun Chen, Zhiyi Bai & Jiale Li

  3. Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai, 201306, China

    Xiajun Chen & Zhiyi Bai

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  1. Xiajun Chen
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Correspondence to Jiale Li.

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Mussels were treated according to animal care and use guidelines for scientific purposes established by the Institutional Animal Care and Use Committee of Shanghai Ocean University, Shanghai, China.

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Chen, X., Bai, Z. & Li, J. The Mantle Exosome and MicroRNAs of Hyriopsis cumingii Involved in Nacre Color Formation. Mar Biotechnol 21, 634–642 (2019). https://doi.org/10.1007/s10126-019-09908-8

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