Skip to main content

Advertisement

SpringerLink
Log in

Differential expression and miRNA regulation of the GSTP1 gene in the regenerating liver of Chiloscyllium plagiosum

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Liver regeneration is a complicated process, and understanding the regulatory mechanism will be helpful in the treatment of diseases associated with liver. In this study, the one-third liver resection model was established in Chiloscyllium plagiosum, and the whole transcriptome of the C. plagiosum was generated using the Illumina–Solexa sequencing platform. Differentially expressed genes were analyzed using bioinformatics methods and verified using quantitative real-time PCR (qRT-PCR). Using miRanda and TargetScan, we screened the microRNA library for miRNAs that target the glutathione S-transferase P1(GSTP1) gene. Dual-luciferase reporter assays were used to confirm binding between the miRNA and GSTP1. Finally, we used western blotting analysis to determine expression of the GSTP1 protein. As a result, 65,356 unigenes were obtained in normal and damaged liver tissues, with mean length of 955 bp. A total of 359 differentially expressed genes were acquired; 217 of which were upregulated, and 142 were downregulated, including the GSTP1 gene, following liver resection. The presence of the GSTP1 protein in C. plagiosum was shown for the first time. Luciferase reporter assay revealed that GSTP1 messenger RNA was targeted by ipu-miR-143. The discovery and differential expression analysis of GSTP1 in C. plagiosum will be a valuable resource to explain the molecular mechanism of GSTP1 regulation of liver repair.

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
Fig. 7

References

  • Bhatnagar I, Kim SK (2010) Marine antitumor drugs: status, shortfalls and strategies. Marine drugs 8:2702–2720. doi:10.3390/md8102702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen QL, Luo Z, Huang C, Pan YX, Wu K (2016) De novo characterization of the liver transcriptome of javelin goby Synechogobius hasta and analysis of its transcriptomic profile following waterborne copper exposure. Fish Physiol Biochem 42:979–994. doi:10.1007/s10695-015-0190-2

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Jiao JW, Sun KX, Zong ZH, Zhao Y (2015) MicroRNA-133b targets glutathione S-transferase pi expression to increase ovarian cancer cell sensitivity to chemotherapy drugs. Drug design, development and therapy 9:5225–5235. doi:10.2147/DDDT.S87526

    PubMed  PubMed Central  Google Scholar 

  • Costa M et al (2014) Exploring bioactive properties of marine cyanobacteria isolated from the Portuguese coast: high potential as a source of anticancer compounds. Marine drugs 12:98–114. doi:10.3390/md12010098

    Article  Google Scholar 

  • Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. doi:10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hazon N, Wells A, Pillans RD, Good JP, Gary Anderson W, Franklin CE (2003) Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity comparative biochemistry and physiology Part B. Biochemistry & molecular biology 136:685–700

    Article  Google Scholar 

  • Jelski W, Zalewski B, Szmitkowski M (2008) The activity of class I, II, III, and IV alcohol dehydrogenase (ADH) isoenzymes and aldehyde dehydrogenase (ALDH) in liver cancer. Dig Dis Sci 53:2550–2555. doi:10.1007/s10620-007-0153-2

    Article  CAS  PubMed  Google Scholar 

  • Jin W, Li N, Zhang B, Wu F, Li W, Guo A, Deng Z (2008) Identification and verification of microRNA in wheat (Triticum aestivum). J Plant Res 121:351–355. doi:10.1007/s10265-007-0139-3

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109–D114. doi:10.1093/nar/gkr988

    Article  CAS  PubMed  Google Scholar 

  • Krupenko NI, Dubard ME, Strickland KC, Moxley KM, Oleinik NV, Krupenko SA (2010) ALDH1L2 is the mitochondrial homolog of 10-formyltetrahydrofolate dehydrogenase. J Biol Chem 285:23056–23063. doi:10.1074/jbc.M110.128843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X et al (2015) Ras association domain family member 10 suppresses gastric cancer growth by cooperating with GSTP1 to regulate JNK/c-Jun/AP-1 pathway. Oncogene. doi:10.1038/onc.2015.300

    Google Scholar 

  • Liu X, An BH, Kim MJ, Park JH, Kang YS, Chang M (2014) Human glutathione S-transferase P1-1 functions as an estrogen receptor alpha signaling modulator. Biochem Biophys Res Commun 452:840–844. doi:10.1016/j.bbrc.2014.09.017

    Article  CAS  PubMed  Google Scholar 

  • Liu Y et al (2013) A shark liver gene-derived active peptide expressed in the silkworm. Bombyx mori: preliminary studies for oral administration of the recombinant protein marine drugs 11:1492–1505. doi:10.3390/md11051492

  • Lu C et al (2013) Study of microRNAs related to the liver regeneration of the whitespotted bamboo shark Chiloscyllium plagiosum. BioMed research international 2013:795676. doi:10.1155/2013/795676

    PubMed  PubMed Central  Google Scholar 

  • Lv Z, Ou Y, Li Q, Zhang W, Ye B, Wu W (2009) Expression, purification and bioactivities analysis of recombinant active peptide from shark liver. Marine drugs 7:258–267. doi:10.3390/md7020258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Q, Su YQ, Wang J, Zhuang ZM, Tang QS (2013) Molecular cloning and expression analysis of major histocompatibility complex class IIB gene of the whitespotted bambooshark (Chiloscyllium plagiosum). Fish Physiol Biochem 39:131–142. doi:10.1007/s10695-012-9685-2

    Article  CAS  PubMed  Google Scholar 

  • Mori M, Ishizaki M, Onda M (1995) Immunohistochemical investigation of hepatocellular pi class glutathione S-transferase in normal and regenerating rat liver. Nihon Ika Daigaku zasshi 62:447–455

    Article  CAS  PubMed  Google Scholar 

  • Mutallip M et al (2011) Glutathione S-transferase P1 (GSTP1) suppresses cell apoptosis and its regulation by miR-133alpha in head and neck squamous cell carcinoma (HNSCC). Int J Mol Med 27:345–352. doi:10.3892/ijmm.2010.589

    CAS  PubMed  Google Scholar 

  • Pajaud J et al (2015) Glutathione transferases P1/P2 regulate the timing of signaling pathway activations and cell cycle progression during mouse liver regeneration. Cell Death Dis 6:e1598. doi:10.1038/cddis.2014.562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. The Biochemical journal 360:1–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A et al (2016) Human glutathione S-transferase enzyme gene polymorphisms and their association with neurocysticercosis. Mol Neurobiol. doi:10.1007/s12035-016-9779-4

    Google Scholar 

  • Singh S, Shukla GC, Gupta S (2015) MicroRNA regulating glutathione S-transferase P1 in prostate cancer. Current pharmacology reports 1:79–88. doi:10.1007/s40495-014-0009-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su F, Hu X, Jia W, Gong C, Song E, Hamar P (2003) Glutathion S transferase pi indicates chemotherapy resistance in breast cancer. J Surg Res 113:102–108

    Article  CAS  PubMed  Google Scholar 

  • Uchida Y et al (2013) MiR-133a induces apoptosis through direct regulation of GSTP1 in bladder cancer cell lines. Urol Oncol 31:115–123. doi:10.1016/j.urolonc.2010.09.017

    Article  CAS  PubMed  Google Scholar 

  • Wilce MC, Parker MW (1994) Structure and function of glutathione S-transferases. Biochim Biophys Acta 1205:1–18

    Article  CAS  PubMed  Google Scholar 

  • Yamada Y, Kirillova I, Peschon JJ, Fausto N (1997) Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor Proceedings of the National Academy of Sciences of the United States of America. 94:1441–1446

  • Yang L et al (2012) Expression analysis of miRNAs in BmN cells. Gene 505:240–245. doi:10.1016/j.gene.2012.06.018

    Article  CAS  PubMed  Google Scholar 

  • Zhang J et al (2013) The identification of microRNAs in the whitespotted bamboo shark (Chiloscyllium plagiosum) liver by Illumina sequencing. Gene 527:259–265. doi:10.1016/j.gene.2013.06.012

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhu J, Xing R, Tie Y, Fu H, Zheng X, Yu B (2012) miR-513a-3p sensitizes human lung adenocarcinoma cells to chemotherapy by targeting GSTP1. Lung Cancer 77:488–494. doi:10.1016/j.lungcan.2012.05.107

    Article  PubMed  Google Scholar 

  • Zheng Q et al (2014) MicroRNA-452 promotes tumorigenesis in hepatocellular carcinoma by targeting cyclin-dependent kinase inhibitor 1B. Mol Cell Biochem 389:187–195. doi:10.1007/s11010-013-1940-z

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by financial grants from the National High Technology Research and Development Program (No. 2012ZX09102301-009 and 2011AA100603) and from the Foundation from Zhejiang Provincial Top Discipline of Biology. The authors thank NPG Language Editing for editing the language of this manuscript.

Author information

Authors and Affiliations

  1. College of Life Sciences, Zhejiang Sci-Tech University, Hangzhou, 310018, China

    Yinghua Ge, Jiewen Zhang, Xinyi Shi, Conger Lu, Lingrong Yang, Yuanyuan Li, Yanna Chen, Dandan Cheng, Jing Bai, Zhengbing Lv & Lili Liu

  2. Zhejiang Provincial Key Laboratory of Silkworm Bioreactor and Biomedicine, Hangzhou, 310018, China

    Yinghua Ge, Jiewen Zhang, Xinyi Shi, Conger Lu, Lingrong Yang, Yuanyuan Li, Yanna Chen, Dandan Cheng, Jing Bai, Zhengbing Lv & Lili Liu

Authors
  1. Yinghua Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiewen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinyi Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Conger Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lingrong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuanyuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanna Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dandan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jing Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhengbing Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lili Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhengbing Lv or Lili Liu.

Ethics declarations

All procedures performed in studies involving animals were in accordance with the ethical standards of Animal Ethics Committee of Zhejiang Sci-Tech University (2015–034). Informed consent was obtained from all individual participants included in the study.

ᅟ

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Yinghua Ge and Jiewen Zhang contributed equally to this work.

Electronic supplementary material

ESM 1

(DOCX 78 kb.)

ESM 2

(DOCX 158 kb.)

ESM 3

(DOCX 133 kb.)

ESM 4

(DOCX 13 kb.)

ESM 5

(DOCX 13 kb.)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ge, Y., Zhang, J., Shi, X. et al. Differential expression and miRNA regulation of the GSTP1 gene in the regenerating liver of Chiloscyllium plagiosum . Fish Physiol Biochem 43, 791–802 (2017). https://doi.org/10.1007/s10695-016-0332-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0332-1

Keywords

Search

Navigation