Skip to main content

Advertisement

SpringerLink
Log in

SNHG14 promotes the tumorigenesis and metastasis of colorectal cancer through miR-32-5p/SKIL axis

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

Colorectal cancer (CRC) is regarded as one of the top ten malignant cancers, which has caused millions of mortalities all over the world. Although advanced therapeutic methods have been employed to treat CRC, the prognosis of CRC patients remains unsatisfactory. Many researchers claimed long noncoding RNAs (lncRNAs) frequently participate in the development of cancers. Small nucleolar RNA host gene 14 (SNHG14) was proved to play roles in various cancers. Nevertheless, neither biological function nor regulatory mechanism of SNHG14 has been explored in CRC. This investigation is aimed at exploring the role of SNHG14 in CRC. The expression of genes including SNHG14, miR-32-5p, and ski-oncogene-like (SKIL) was measured by RT-qPCR assay. 5-Ethynyl-2′-deoxyuridine (EdU) assay was employed to measure cell proliferation. Cell migration and invasion were evaluated by transwell assay. Western blot assay was performed to test the protein expression. The binding capacity between miR-32-5p and SNHG14 (or SKIL) was explored by luciferase reporter and RNA immunoprecipitation (RIP) assays. SNHG14 expression is upregulated in CRC cells. Moreover, SNHG14 suppression inhibited the proliferation, metastasis, and epithelial-mesenchymal transition (EMT) process in CRC cells. miR-32-5p presented lower expression, which was negatively regulated by SNHG14. SKIL could combine with miR-32-5p. The mRNA and protein expression of SKIL was downregulated by SNHG14 knockdown or miR-32-5p overexpression. At last, the inhibitory effect of SNHG14 suppression on proliferation, metastasis, and EMT process was rescued by SKIL overexpression. SNHG14 regulates CRC progression via miR-32-5p/SKIL axis, providing a novel point in treatment of CRC patients.

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

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.

Similar content being viewed by others

References

  • Ballester V, Rashtak S, Boardman L (2016) Clinical and molecular features of young-onset colorectal cancer. World J Gastroenterol 22:1736–1744

    Article  CAS  Google Scholar 

  • Bundela S, Sharma A, Bisen PS (2014) Potential therapeutic targets for oral cancer: ADM, TP53, EGFR, LYN, CTLA4, SKIL, CTGF, CD70. PLoS One 9:e102610

    Article  Google Scholar 

  • Cai C, Huo Q, Wang X, Chen B, Yang Q (2017) SNHG16 contributes to breast cancer cell migration by competitively binding miR-98 with E2F5. Biochem Biophys Res Commun 485:272–278

    Article  CAS  Google Scholar 

  • Chen Y, Yu X, Xu Y, Shen H (2017) Identification of dysregulated lncRNAs profiling and metastasis-associated lncRNAs in colorectal cancer by genome-wide analysis. Cancer Med 6:2321–2330

    Article  CAS  Google Scholar 

  • Dong H, Wang W, Chen R, Zhang Y, Zou K, Ye M, He X, Zhang F, Han J (2018a) Exosome-mediated transfer of lncRNASNHG14 promotes trastuzumab chemoresistance in breast cancer. Int J Oncol 53:1013–1026

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong H, Wang W, Mo S, Liu Q, Chen X, Chen R, Zhang Y, Zou K, Ye M, He X, Zhang F, Han J, Hu J (2018b) Long non-coding RNA SNHG14 induces trastuzumab resistance of breast cancer via regulating PABPC1 expression through H3K27 acetylation. J Cell Mol Med 22:4935–4947

    Article  CAS  Google Scholar 

  • Iguchi T, Uchi R, Nambara S, Saito T, Komatsu H, Hirata H, Ueda M, Sakimura S, Takano Y, Kurashige J, Shinden Y, Eguchi H, Sugimachi K, Maehara Y, Mimori K (2015) A long noncoding RNA, lncRNA-ATB, is involved in the progression and prognosis of colorectal cancer. Anticancer Res 35:1385–1388

    CAS  PubMed  Google Scholar 

  • Ji N, Wang Y, Bao G, Yan J, Ji S (2019) LncRNA SNHG14 promotes the progression of cervical cancer by regulating miR-206/YWHAZ. Pathol Res Pract 215:668–675

    Article  CAS  Google Scholar 

  • Li Z, Hou P, Fan D, Dong M, Ma M, Li H, Yao R, Li Y, Wang G, Geng P, Mihretab A, Liu D, Zhang Y, Huang B, Lu J (2017) The degradation of EZH2 mediated by lncRNA ANCR attenuated the invasion and metastasis of breast cancer. Cell Death Differ 24:59–71

    Article  Google Scholar 

  • Liu G, Ye Z, Zhao X, Ji Z (2017) SP1-induced up-regulation of lncRNA SNHG14 as a ceRNA promotes migration and invasion of clear cell renal cell carcinoma by regulating N-WASP. Am J Cancer Res 7:2515–2525

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Li C, Xu J, Wu H (2018) A patient-oriented clinical decision support system for CRC risk assessment and preventative care. BMC Med Inform Decis Mak 18:118

    Article  Google Scholar 

  • Liu YJ, Zhou HG, Chen LH, Qu DC, Wang CJ, Xia ZY, Zheng JH (2019) MiR-32-5p regulates the proliferation and metastasis of cervical cancer cells by targeting HOXB8. Eur Rev Med Pharmacol Sci 23:87–95

    PubMed  Google Scholar 

  • Mao Z, Li H, Du B, Cui K, Xing Y, Zhao X, Zai S (2017) LncRNA DANCR promotes migration and invasion through suppression of lncRNA-LET in gastric cancer cells. Biosci Rep 37:BSR20171070

    Article  CAS  Google Scholar 

  • Mo Y, He L, Lai Z, Wan Z, Chen Q, Pan S, Li L, Li D, Huang J, Xue F, Che S (2018) LINC01287/miR-298/STAT3 feedback loop regulates growth and the epithelial-to-mesenchymal transition phenotype in hepatocellular carcinoma cells. J Exp Clin Cancer Res 37:149

    Article  Google Scholar 

  • Mohr AM, Mott JL (2015) Overview of microRNA biology. Semin Liver Dis 35:3–11

    Article  CAS  Google Scholar 

  • Qi X, Shao M, Sun H, Shen Y, Meng D, Huo W (2017) Long non-coding RNA SNHG14 promotes microglia activation by regulating miR-145-5p/PLA2G4A in cerebral infarction. Neuroscience 348:98–106

    Article  CAS  Google Scholar 

  • Shinozuka E, Miyashita M, Mizuguchi Y, Akagi I, Kikuchi K, Makino H, Matsutani T, Hagiwara N, Nomura T, Uchida E, Takizawa T (2013) SnoN/SKIL modulates proliferation through control of hsa-miR-720 transcription in esophageal cancer cells. Biochem Biophys Res Commun 430:101–106

    Article  CAS  Google Scholar 

  • Tutar Y (2014) miRNA and cancer; computational and experimental approaches. Curr Pharm Biotechnol 15:429

    Article  CAS  Google Scholar 

  • Wang J, Cao L, Wu J, Wang Q (2018a) Long non-coding RNA SNHG1 regulates NOB1 expression by sponging miR-326 and promotes tumorigenesis in osteosarcoma. Int J Oncol 52:77–88

    CAS  PubMed  Google Scholar 

  • Wang J, Lu Y, Ding H, Gu T, Gong C, Sun J, Zhang Z, Zhao Y, Ma C (2018b) The miR-875-5p inhibits SATB2 to promote the invasion of lung cancer cells. Gene 644:13–19

    Article  CAS  Google Scholar 

  • Wu Y, Hu L, Liang Y, Li J, Wang K, Chen X, Meng H, Guan X, Yang K, Bai Y (2017) Up-regulation of lncRNA CASC9 promotes esophageal squamous cell carcinoma growth by negatively regulating PDCD4 expression through EZH2. Mol Cancer 16:150

    Article  Google Scholar 

  • Xie SD, Qin C, Jin LD, Wang QC, Shen J, Zhou JC, Chen YX, Huang AH, Zhao WH, Wang LB (2019) Long noncoding RNA SNHG14 promotes breast cancer cell proliferation and invasion via sponging miR-193a-3p. Eur Rev Med Pharmacol Sci 23:2461–2468

    PubMed  Google Scholar 

  • Xu Q, Zhu Q, Zhou Z, Wang Y, Liu X, Yin G, Tong X, Tu K (2018) MicroRNA-876-5p inhibits epithelial-mesenchymal transition and metastasis of hepatocellular carcinoma by targeting BCL6 corepressor like 1. Biomed Pharmacother 103:645–652

    Article  CAS  Google Scholar 

  • Yu B, Shan G (2016) Functions of long noncoding RNAs in the nucleus. Nucleus 7:155–166

    Article  CAS  Google Scholar 

  • Zhang CL, Zhu KP, Ma XL (2017a) Antisense lncRNA FOXC2-AS1 promotes doxorubicin resistance in osteosarcoma by increasing the expression of FOXC2. Cancer Lett 396:66–75

    Article  CAS  Google Scholar 

  • Zhang L, Li X, Chao Y, He R, Liu J, Yuan Y, Zhao W, Han C, Song X (2018) KLF4, a miR-32-5p targeted gene, promotes cisplatin-induced apoptosis by upregulating BIK expression in prostate cancer. Cell Commun Sign 16:53

  • Zhang W, Yuan W, Song J, Wang S, Gu X (2017b) LncRna CPS1-IT1 suppresses cell proliferation, invasion and metastasis in colorectal cancer. Cell Physiol Biochem 44:567–580

    Article  Google Scholar 

  • Zhang Z, Wang Y, Zhang W, Li J, Liu W, Lu W (2019) Long non-coding RNA SNHG14 exerts oncogenic functions in non-small cell lung cancer through acting as an miR-340 sponge. Biosci Rep 39

Download references

Acknowledgments

We appreciate the support of Regional Science Fund Project of the National Natural Science Foundation of China (Nos. 81760814, 81860819), High-level Innovative Talent Training Plan of Guizhou (100 levels) (the Qian family matches the talented person [2016] No. 4032), TCM Tumor Inheritance and Scientific And Technological Innovation Talent Base of Guizhou Province (Guizhou people lead [2018] No. 3), Doctor Foundation of the First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine (GYZYYFY-BS-2018[10]) and Research Project of Traditional Chinese Medicine and Ethnic Medicine Science and Technology of Guizhou Provincial Administration of Traditional Chinese Medicine (No. QZYY-2019-18).

Author information

Author notes

  1. Tao Ye and Ning Zhang contributed equally to this work.

Authors and Affiliations

  1. Oncology Department, The First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, No. 71 North Baoshan Road, Yunyan District, Guiyang, 550001, Guizhou, China

    Tao Ye, Wenyu Wu, Jinghui Wang & Wenqi Huang

  2. Pharmacy Department, The First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, 550001, Guizhou, China

    Ning Zhang

  3. Research Laboratory, The First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, 550001, Guizhou, China

    Bing Yang

  4. Department of Science and Education, The First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, No. 71 North Baoshan Road, Yunyan District, Guiyang, 550001, Guizhou, China

    Dongxin Tang

Authors
  1. Tao Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ning Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenyu Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bing Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinghui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenqi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dongxin Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dongxin Tang.

Ethics declarations

The present investigation was approved by the committee of the First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine

Conflict of interest

The authors declare that there are no competing interests.

Additional information

Editor: Tetsuji Okamoto

Electronic supplementary material

Fig S1

(A-B) The expression of proteins related to TGF-β and Wnt/β-catenin signaling pathway was examined by western blot assay. (C) The expression of SNHG14 was tested by RT-qPCR. *P < 0.05, **P < 0.01. (PNG 297 kb)

High Resolution Image (TIF 13877 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, T., Zhang, N., Wu, W. et al. SNHG14 promotes the tumorigenesis and metastasis of colorectal cancer through miR-32-5p/SKIL axis. In Vitro Cell.Dev.Biol.-Animal 55, 812–820 (2019). https://doi.org/10.1007/s11626-019-00398-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-019-00398-5

Keywords

Search

Navigation