Skip to main content

Advertisement

SpringerLink
Log in

MiR-382 Functions on the Regulation of Melanogenesis via Targeting dct in Rainbow Trout (Oncorhynchus mykiss)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are a class of endogenous small noncoding RNAs that are involved in a diverse collection of biological processes as important post-transcriptional regulators. However, little is known about the molecular regulatory mechanism of miRNAs in fish skin pigmentation. In this study, we first confirmed that dopachrome tautomerase (dct), a key gene of melanogenesis, is a target of miR-382 in rainbow trout (Oncorhynchus mykiss) using luciferase reporter assay. The analysis of different developmental stages and tissue expression patterns between wild-type and yellow mutant rainbow trout suggested that miR-382 is a potential regulator during the process of skin pigmentation. In vitro, miR-382 mimics in rainbow trout primary liver cells significantly downregulated dct expression and resulted in decreased expression of key melanogenic genes including tyrosine-related protein 1 (tyrp1) and premelanosome protein (pmel), whereas the expression level of dct was markedly increased after transfected with miR-382 inhibitor. In vivo, overexpression of miR-382 by injection of miR-382 agomir significantly depressed the expression of dct in dorsal skin, tail fin, and liver and then reduced the expression levels of tyrp1 and pmel. Furthermore, transfection of miR-382 mimics inhibited cell proliferation and induced apoptosis. Taken together, our results identified a functional role of miR-382 in rainbow trout skin pigmentation through targeting dct, which facilitate understanding the regulatory mechanism of rainbow trout skin color at the post-transcriptional level and provide a theoretical basis for molecular breeding with skin color as the target trait.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aksu-Menges E, Akkaya-Ulum YZ, Dayangac-Erden D, Balci-Peynircioglu B, Yuzbasioglu A, Topaloglu H, Talim B, Balci-Hayta B (2020) The common miRNA signatures associated with mitochondrial dysfunction in different muscular dystrophies. Am J Pathol 190:2136–2145

    Article  CAS  PubMed  Google Scholar 

  • Béjar J, Hong Y, Schartl M (2003) Mitf expression is sufficient to direct differentiation of medaka blastula derived stem cells to melanocytes. Development 130:6545–6553

    Article  PubMed  CAS  Google Scholar 

  • Boonanuntanasarn S, Yoshizaki G, Iwai K, Takeuchi T (2004) Molecular cloning, gene expression in albino mutants and gene knockdown studies of tyrosinase mRNA in rainbow trout. Pigment Cell Res 17:413–421

    Article  CAS  PubMed  Google Scholar 

  • Braasch I, Schartl M, Volff JN (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 7:74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bian C, Li R, Wen Z, Ge W, Shi Q (2021) Phylogenetic analysis of core melanin synthesis genes provides novel insights into the molecular basis of albinism in fish. Front Genet 12:707228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornell RA, Yemm E, Bonde G, Li W, d’Alençon C, Wegman L, Eisen J, Zahs A (2004) Touchtone promotes survival of embryonic melanophores in zebrafish. Mech Dev 121:1365–1376

    Article  CAS  PubMed  Google Scholar 

  • Costin GE, Valencia JC, Wakamatsu K, Ito S, Solano F, Milac AL, Vieira WD, Yamaguchi Y, Rouzaud F, Petrescu AJ, Lamoreux ML, Hearing VJ (2005) Mutations in dopachrome tautomerase (Dct) affect eumelanin/pheomelanin synthesis, but do not affect intracellular trafficking of the mutant protein. Biochem J 391:249–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao T, Zhen XC (2018) Dysregulation of miRNA and its potential therapeutic application in schizophrenia. CNS Neurosci Ther 24:586–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Jiang C, Sun R, Yang D, Liu Q (2020) Circular noncoding RNA NR3C1 acts as a miR-382-5p sponge to protect RPE functions via regulating PTEN/AKT/mTOR signaling pathway. Mol Ther 28:929–945

    Article  CAS  PubMed  PubMed Central  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 

  • Dmitriev P, Stankevicins L, Ansseau E, Petrov A, Barat A, Dessen P, Robert T, Turki A, Lazar V, Labourer E, Belayew A, Carnac G, Laoudj-Chenivesse D, Lipinski M, Vassetzky YS (2013) Defective regulation of microRNA target genes in myoblasts from facioscapulohumeral dystrophy patients. J Biol Chem 288:34989–35002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du J, Bai F, Zhao P, Li X, Li X, Gao L, Ma C, Liang X (2018) Hepatitis B core protein promotes liver cancer metastasis through miR-382-5p/DLC-1 axis. Biochim Biophys Acta Mol Cell Res 1865:1–11

    Article  CAS  PubMed  Google Scholar 

  • Du J, Chen X, Wang J, Chen H, Yue W, Lu G, Wang C (2019) Comparative skin transcriptome of two Oujiang color common carp (Cyprinus carpio var. color) varieties. Fish Physiol Biochem 45:177–185

    Article  CAS  PubMed  Google Scholar 

  • Djurdjevič I, Furmanek T, Miyazawa S, Sušnik Bajec S (2019) Comparative transcriptome analysis of trout skin pigment cells. BMC Genomics 20:359

    Article  PubMed  PubMed Central  Google Scholar 

  • Daemen S, Kersten S, Auwerx J, Wang X, Jörgensen JA, Moullan N, Daemen S, Kersten S, Auwerx J, Hoeks J (2019) MicroRNA-382 silencing induces a mitonuclear protein imbalance and activates the mitochondrial unfolded protein response in muscle cells. J Cell Physiol 234:6601–6610

    Article  PubMed  CAS  Google Scholar 

  • Dong Z, Luo M, Wang L, Yin H, Zhu W, Fu J (2020) MicroRNA-206 regulation of skin pigmentation in koi carp (Cyprinus carpio L.). Front Genet 11:47

  • Guyonneau L, Murisier F, Rossier A, Moulin A, Beermann F (2004) Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Mol Cell Bio 24:3396–3403

    Article  CAS  Google Scholar 

  • Ho JY, Hsu RJ, Liu JM, Chen SC, Liao GS (2017) MicroRNA-382-5p aggravates breast cancer progression by regulating the RERG/Ras/ERK signaling axis. Oncotarget 8:22443–22459

    Article  PubMed  Google Scholar 

  • He Q, Zhao L, Liu X, Zheng J, Liu Y, Liu L, Ma J, Cai H, Li Z, Xue Y (2019) MOV10 binding circ-DICER1 regulates the angiogenesis of glioma via miR-103a-3p/miR-382-5p mediated ZIC4 expression change. J Exp Clin Cancer Res 38:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Hattori RS, Yoshinaga TT, Butzge AJ, Hattori-Ihara S, Tsukamoto RY, Takahashi NS, Tabata YA (2020) Generation of a white-albino phenotype from cobalt blue and yellow-albino rainbow trout (Oncorhynchus mykiss): inheritance pattern and chromatophores analysis. PLoS ONE 15:e0214034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu S, Dai Y, Bai S, Zhao B, Wu X, Chen Y (2021a) GNAI2 promotes proliferation and decreases apoptosis in rabbit melanocytes. Genes 12:1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu S, Bai S, Dai Y, Yang N, Li J, Zhang X, Wang F, Zhao B, Bao G, Chen Y, Wu X (2021b) Deubiquitination of MITF-M regulates melanocytes proliferation and apoptosis. Front Mol Biosci 8:692724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito S, Wakamatsu K (2003) Quantitative analysis of eumelanin and pheomelanin in humans, mice, and other animals: a comparative review. Pigment Cell Res 16:523–531

    Article  PubMed  Google Scholar 

  • Jiao Z, Zhang ZG, Hornyak TJ, Hozeska A, Zhang RL, Wang Y, Wang L, Roberts C, Strickland FM, Chopp M (2006) Dopachrome tautomerase (Dct) regulates neural progenitor cell proliferation. Dev Biol 296:396–408

    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 

  • Lv M, Chen H, Shao Y, Li C, Zhang W, Zhao X, Jin C, Xiong J (2017) MiR-92a regulates coelomocytes apoptosis in sea cucumber Apostichopus japonicus via targeting Aj14-3-3ζ in vivo. Fish Shellfish Immunol 69:211–217

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Zhong L, Yuan Z, Yao J, Zhong P, Liu J, Yao S, Zhao Y, Liu L, Chen M, Li L, Liu B (2019) MiR-382-5p modulates the ATRA-induced differentiation of acute promyelocytic leukemia by targeting tumor suppressor PTEN. Cell Signal 54:1–9

    Article  PubMed  CAS  Google Scholar 

  • Luo MK, Lu GQ, Yin HR (2021) Fish pigmentation and coloration: molecular mechanisms and aquaculture perspectives. Aquaculture 13:2392–2412

    Google Scholar 

  • Parichy DM (2006) Evolution of danio pigment pattern development. Heredity 97:200–210

    Article  CAS  PubMed  Google Scholar 

  • Popa IL, Milac AL, Sima LE, Alexandru PR, Pastrama F, Munteanu C, Negroiu G (2016) Cross-talk between dopachrome tautomerase and caveolin-1 is melanoma cell phenotype-specific and potentially involved in tumor progression. J Biol Chem 291:12481–12500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan J, Kang Y, Luo Z, Zhao G, Li L, Liu Z (2021) Integrated analysis of the responses of a circRNA-miRNA-mRNA ceRNA network to heat stress in rainbow trout (Oncorhynchus mykiss) liver. BMC Genomics 22:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugimoto M, Yuki M, Miyakoshi T, Maruko K (2005) The influence of long-term chromatic adaptation on pigment cells and striped pigment patterns in the skin of the zebrafish, Danio rerio. J Exp Zool A Comp Exp Biol 303:430–440

    Article  PubMed  Google Scholar 

  • Sugumaran M (2016) Reactivities of quinone methides versus o-quinones in catecholamine metabolism and eumelanin biosynthesis. Int J Mol Sci 17:1576

    Article  PubMed Central  CAS  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 

  • 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 19:1209

    Article  PubMed Central  CAS  Google Scholar 

  • Wang J, Chen C, Yan X, Wang P (2019) The role of miR-382-5p in glioma cell proliferation, migration and invasion. Onco Targets Ther 12:4993–5002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S, Huang J, Li Y, Zhao L, Liu Z, Kang Y, Wang J (2021a) Integrative mRNA-miRNA interaction analysis reveals the molecular mechanism of skin color variation between wild-type and yellow mutant rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol Part D Genomics Proteomics 40:100914

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Lu B, Li T, Liang G, Xu M, Liu X, Tao W, Zhou L, Kocher TD, Wang D (2021) Nile tilapia: a model for studying teleost color patterns. J Hered 112:469–484

    Article  CAS  PubMed  Google Scholar 

  • Wu SJ, Huang JQ, Li YJ (2021b) Cloning, sequence analysis, and expression of tyrp1a and tyrp2 genes related to body colour in different developmental stages and tissues of rainbow trout Oncorhynchus mykiss. Aquacult Int 29:941–961

    Article  CAS  Google Scholar 

  • Xu X, Jiang H, Li X, Wu P, Liu J, Wang T, Zhou X, Xiong J, Li W (2017) Bioinformatics analysis on the differentiation of bone mesenchymal stem cells into osteoblasts and adipocytes. Mol Med Rep 15:1571–1576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu TJ, Qiu P, Zhang YB, Yu SY, Xu GM, Yang W (2019) MiR-148a inhibits the proliferation and migration of glioblastoma by targeting ITGA9. Hum Cell 32:548–556

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Li C, Wan H, Liu Y (2020) LINC00265 targets miR-382-5p to regulate SAT1, VAV3 and angiogenesis in osteosarcoma. Aging 12:20212–20225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XQ, Zhang B, Guo L, Liu Y, Meng FZ, Wang X, Hu WH, Khan AI, Ho WZ (2021) Exosomes transport anti-human immunodeficiency virus factors from human cervical epithelial cells to macrophages. J Innate Immun 13:269–279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan B, Liu B, Zhu CD, Li KL, Yue LJ, Zhao JL, Gong XL, Wang CH (2013) microRNA regulation of skin pigmentation in fish. J Cell Sci 126:3401–3408

    CAS  PubMed  Google Scholar 

  • Ye K, Wei Q, Gong Z, Huang Y, Liu H, Li Y, Peng X (2017) Effect of norcantharidin on the proliferation, apoptosis, and cell cycle of human mesangial cells. Ren Fail 39:458–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Liu J, Peng L, Ren L, Zhang H, Zou L, Liu W, Xiao Y (2017) Comparative transcriptome analysis of molecular mechanism underlying gray-to-red body color formation in red crucian carp (Carassius auratus, red var.). Fish Physiol Biochem 43:1387–1398

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Chu Q, Liu X, Xu T (2020a) MicroRNA-21 negatively regulates NF-κB signaling pathway via targeting IL1R1 in miiuy croaker. Dev Comp Immunol 105:103578

    Article  CAS  PubMed  Google Scholar 

  • Zhang WJ, Chen FF, Wang YQ, Yu W, Dong FL, Zhuang HX (2020b) MiR-150 inhibits proliferation of mantle-cell lymphoma cells via regulation of MET. Eur Rev Med Pharmacol Sci 24:12063–12072

    PubMed  Google Scholar 

  • Zheng Y, Zhou J, Li X, Xu G, Jin M, Shen R, Su R, Zhan S, Ding B, Jia M, Cui Y, Yu X (2018) Mir-382 promotes differentiation of rat liver progenitor cell WB-F344 by targeting Ezh2. Cell Physiol Biochem 48:2389–2398

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Tang J, Yang D, Tang C, Chen J (2020) Staphylococcal enterotoxin M induced inflammation and impairment of bovine mammary epithelial cells. J Dairy Sci 103:8350–8359

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Zhao H, Zhang L, Liu C, Feng S, Ma J, Li Q, Ke H (2019) Integrated analysis of RNA-seq and microRNA-seq depicts miRNA-mRNA networks involved in stripe patterns of Botia superciliaris skin. Funct Integr Genomics 19:827–838

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, He J, Jia X, Jiang J, Bai R, Yu X, Lv L, Fan R, He X, Geng J, You R, Dong Y (2010) MicroRNA-25 functions in regulation of pigmentation by targeting the transcription factor MITF in alpaca (Lama pacos) skin melanocytes. Domest Anim Endocrinol 38:200–209

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was funded by the National Natural Science Foundation of China (Grant No. 31760755), the Fuxi Youth Talent Training Program of Gansu Agricultural University (Grant No. Gaufx-02Y08), and the Outstanding Graduate Student “Innovation Star” Program of Gansu Province (2022CXZX-626).

Author information

Authors and Affiliations

  1. College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, 730070, China

    Shenji Wu, Jinqiang Huang, Zhe Liu & Lu Zhao

  2. College of Science, Gansu Agricultural University, Lanzhou, 730070, China

    Yongjuan Li

Authors
  1. Shenji Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jinqiang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yongjuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhe Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lu Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Shenji Wu wrote the manuscript. Jinqiang Huang designed the study. Yongjuan Li and Zhe Liu analyzed the data. Shenji Wu and Lu Zhao carried out experiments.

Corresponding author

Correspondence to Jinqiang Huang.

Ethics declarations

Consent for Publication

All authors declare that this paper has not been submitted to any other journal for publication. All authors have read and agree to the contents of the manuscript and consent to its publication.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, S., Huang, J., Li, Y. et al. MiR-382 Functions on the Regulation of Melanogenesis via Targeting dct in Rainbow Trout (Oncorhynchus mykiss). Mar Biotechnol 24, 776–787 (2022). https://doi.org/10.1007/s10126-022-10143-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-022-10143-x

Keywords

Search

Navigation