Skip to main content
Top
Published in: Cancer Cell International 1/2019

Open Access 01-12-2019 | Metastasis | Primary research

MiR-566 mediates cell migration and invasion in colon cancer cells by direct targeting of PSKH1

Authors: Ying Zhang, Siqi Zhang, Jian Yin, Ruisi Xu

Published in: Cancer Cell International | Issue 1/2019

Login to get access

Abstract

Background

Colorectal cancer (CRC), a common malignancy worldwide, and microRNAs (miRs) have been suggested to play roles in the disease. MiR-566 expression has been shown to be reduced in CRC, but its functions and mechanisms are still unclear.

Methods

Cell viability was assessed by using the CellTiter 96 AQueous One Solution Cell Proliferation kit. Cell proliferation was measured with MTT assay. Cell metastasis were measured by transwell assay. Luciferase reporter assays was used to confirm the target of MiR-566. PSKH1 expression was measured by RT-PCR and western blot.

Results

In the present study, we first observed that miR-566 was expressed in several CRC cell lines (SW480, SW620, LoVo, HT29 and Caco-2) at low levels compared to control colon epithelial cell lines (FHC). Further study showed that miR-566 overexpression suppressed cell survival and impeded cell proliferation, whereas inhibition of its expression enhanced cell survival and proliferation. Transwell assays showed that cell invasion and migration were reduced in cells overexpressing miR-566 and increased in those with inhibition of miR-566. Further analysis confirmed that PSKH1 is a target of miR-566. MiR-566 overexpression significantly inhibited PSKH1 expression and reintroduction of PSKH1 partially reversed the effects of miR-566 on CRC cell growth and metastasis in SW480 and Caco-2 cells.

Conclusions

Taken together, the data show that CRC cell growth and metastasis can be significantly suppressed by miR-566 through targeting PSKH1.
Literature
1.
go back to reference Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, MacIntyre M, Allen C, Hansen G, Woodbrook R, Wolfe C, et al. The global burden of cancer 2013. JAMA Oncol. 2015;1(4):505–27.CrossRef Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, MacIntyre M, Allen C, Hansen G, Woodbrook R, Wolfe C, et al. The global burden of cancer 2013. JAMA Oncol. 2015;1(4):505–27.CrossRef
2.
go back to reference Fitzmaurice C, Allen C, Barber R, Barregard L, Bhutta Z, Brenner H, Dicker D, Chimed-Orchir O, Dandona R, Dandona L, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: a systematic analysis for the global burden of disease study. JAMA Oncol. 2017;3(4):524–48.CrossRef Fitzmaurice C, Allen C, Barber R, Barregard L, Bhutta Z, Brenner H, Dicker D, Chimed-Orchir O, Dandona R, Dandona L, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: a systematic analysis for the global burden of disease study. JAMA Oncol. 2017;3(4):524–48.CrossRef
3.
go back to reference Li Z, Li N, Wu M, Li X, Luo Z, Wang X. Expression of miR-126 suppresses migration and invasion of colon cancer cells by targeting CXCR4. Mol Cell Biochem. 2013;381(1–2):233–42.CrossRef Li Z, Li N, Wu M, Li X, Luo Z, Wang X. Expression of miR-126 suppresses migration and invasion of colon cancer cells by targeting CXCR4. Mol Cell Biochem. 2013;381(1–2):233–42.CrossRef
4.
go back to reference Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell. 2009;15(3):195–206.CrossRef Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell. 2009;15(3):195–206.CrossRef
5.
go back to reference Soreide K, Berg M, Skudal B, Nedreboe B. Advances in the understanding and treatment of colorectal cancer. Discov Med. 2011;12(66):393–404.PubMed Soreide K, Berg M, Skudal B, Nedreboe B. Advances in the understanding and treatment of colorectal cancer. Discov Med. 2011;12(66):393–404.PubMed
6.
go back to reference Wang J, Wang X, Liu F, Fu Y. microRNA-335 inhibits colorectal cancer HCT116 cells growth and epithelial–mesenchymal transition (EMT) process by targeting Twist1. Pharmazie. 2017;72(8):475–81.PubMed Wang J, Wang X, Liu F, Fu Y. microRNA-335 inhibits colorectal cancer HCT116 cells growth and epithelial–mesenchymal transition (EMT) process by targeting Twist1. Pharmazie. 2017;72(8):475–81.PubMed
7.
go back to reference Yao G, Zhang Y, Chen P, Ren X. MicroRNA-544 promotes colorectal cancer progression by targeting forkhead box O1. Oncol Lett. 2018;15(1):991–7.PubMed Yao G, Zhang Y, Chen P, Ren X. MicroRNA-544 promotes colorectal cancer progression by targeting forkhead box O1. Oncol Lett. 2018;15(1):991–7.PubMed
8.
go back to reference Cellura D, Pickard K, Quaratino S, Parker H, Strefford J, Thomas G, Mitter R, Mirnezami A, Peake N. miR-19-mediated inhibition of transglutaminase-2 leads to enhanced invasion and metastasis in colorectal cancer. Mol Cancer Res. 2015;13(7):1095–105.CrossRef Cellura D, Pickard K, Quaratino S, Parker H, Strefford J, Thomas G, Mitter R, Mirnezami A, Peake N. miR-19-mediated inhibition of transglutaminase-2 leads to enhanced invasion and metastasis in colorectal cancer. Mol Cancer Res. 2015;13(7):1095–105.CrossRef
9.
go back to reference Hu W, Coller J. What comes first: translational repression or mRNA degradation? The deepening mystery of microRNA function. Cell Res. 2012;22(9):1322–4.CrossRef Hu W, Coller J. What comes first: translational repression or mRNA degradation? The deepening mystery of microRNA function. Cell Res. 2012;22(9):1322–4.CrossRef
10.
go back to reference Wu N, Fesler A, Liu H, Ju J. Development of novel miR-129 mimics with enhanced efficacy to eliminate chemoresistant colon cancer stem cells. Oncotarget. 2018;9(10):8887–97.CrossRef Wu N, Fesler A, Liu H, Ju J. Development of novel miR-129 mimics with enhanced efficacy to eliminate chemoresistant colon cancer stem cells. Oncotarget. 2018;9(10):8887–97.CrossRef
11.
go back to reference Li J, Mao X, Wang X, Miao G. miR-433 reduces cell viability and promotes cell apoptosis by regulating MACC1 in colorectal cancer. Oncol Lett. 2017;13(1):81–8.CrossRef Li J, Mao X, Wang X, Miao G. miR-433 reduces cell viability and promotes cell apoptosis by regulating MACC1 in colorectal cancer. Oncol Lett. 2017;13(1):81–8.CrossRef
12.
go back to reference Qin Y, Huo Z, Song X, Chen X, Tian X, Wang X. mir-106a regulates cell proliferation and apoptosis of colon cancer cells through targeting the PTEN/PI3K/AKT signaling pathway. Oncol Lett. 2018;15(3):3197–201.PubMed Qin Y, Huo Z, Song X, Chen X, Tian X, Wang X. mir-106a regulates cell proliferation and apoptosis of colon cancer cells through targeting the PTEN/PI3K/AKT signaling pathway. Oncol Lett. 2018;15(3):3197–201.PubMed
13.
go back to reference Chen Z, Han S, Huang W, Wu J, Liu Y, Cai S, He Y, Wu S, Song W. MicroRNA-215 suppresses cell proliferation, migration and invasion of colon cancer by repressing Yin-Yang 1. Biochem Biophys Res Commun. 2016;479(3):482–8.CrossRef Chen Z, Han S, Huang W, Wu J, Liu Y, Cai S, He Y, Wu S, Song W. MicroRNA-215 suppresses cell proliferation, migration and invasion of colon cancer by repressing Yin-Yang 1. Biochem Biophys Res Commun. 2016;479(3):482–8.CrossRef
14.
go back to reference Sun J, Zhou J, Dong M, Sheng W. Dysregulation of MicroRNA-543 expression in colorectal cancer promotes tumor migration and invasion. Mol Carcinog. 2017;56(1):250–7.CrossRef Sun J, Zhou J, Dong M, Sheng W. Dysregulation of MicroRNA-543 expression in colorectal cancer promotes tumor migration and invasion. Mol Carcinog. 2017;56(1):250–7.CrossRef
15.
go back to reference Drusco A, Nuovo G, Zanesi N, Di Leva G, Pichiorri F, Volinia S, Fernandez C, Antenucci A, Costinean S, Bottoni A, et al. MicroRNA profiles discriminate among colon cancer metastasis. PLoS ONE. 2014;9(6):e96670.CrossRef Drusco A, Nuovo G, Zanesi N, Di Leva G, Pichiorri F, Volinia S, Fernandez C, Antenucci A, Costinean S, Bottoni A, et al. MicroRNA profiles discriminate among colon cancer metastasis. PLoS ONE. 2014;9(6):e96670.CrossRef
16.
go back to reference Kim S, Ahn T, Lee E, Do I, Lee S, Park S, Park J, Park Y, Lim H, Kang W, et al. Exploratory biomarker analysis for treatment response in KRAS wild type metastatic colorectal cancer patients who received cetuximab plus irinotecan. BMC Cancer. 2015;15:747.CrossRef Kim S, Ahn T, Lee E, Do I, Lee S, Park S, Park J, Park Y, Lim H, Kang W, et al. Exploratory biomarker analysis for treatment response in KRAS wild type metastatic colorectal cancer patients who received cetuximab plus irinotecan. BMC Cancer. 2015;15:747.CrossRef
17.
go back to reference Brede G, Solheim J, Tröen G, Prydz H. Characterization of PSKH1, a novel human protein serine kinase with centrosomal, golgi, and nuclear localization. Genomics. 2000;70(1):82–92.CrossRef Brede G, Solheim J, Tröen G, Prydz H. Characterization of PSKH1, a novel human protein serine kinase with centrosomal, golgi, and nuclear localization. Genomics. 2000;70(1):82–92.CrossRef
18.
go back to reference Brede G, Solheim J, Prydz H. PSKH1, a novel splice factor compartment-associated serine kinase. Nucleic Acids Res. 2002;30(23):5301–9.CrossRef Brede G, Solheim J, Prydz H. PSKH1, a novel splice factor compartment-associated serine kinase. Nucleic Acids Res. 2002;30(23):5301–9.CrossRef
19.
go back to reference Pan X, Quan J, Li Z, Zhao L, Zhou L, Jinling X, Weijie X, Guan X, Li H, Yang S, et al. miR-566 functions as an oncogene and a potential biomarker for prognosis in renal cell carcinoma. Biomed Pharmacother. 2018;102:718–27.CrossRef Pan X, Quan J, Li Z, Zhao L, Zhou L, Jinling X, Weijie X, Guan X, Li H, Yang S, et al. miR-566 functions as an oncogene and a potential biomarker for prognosis in renal cell carcinoma. Biomed Pharmacother. 2018;102:718–27.CrossRef
20.
go back to reference Zhou W, Li X, Liu F, Xiao Z, He M, Shen S, Liu S. MiR-135a promotes growth and invasion of colorectal cancer via metastasis suppressor 1 in vitro. Acta Biochim Biophys Sin. 2012;44(10):838–46.CrossRef Zhou W, Li X, Liu F, Xiao Z, He M, Shen S, Liu S. MiR-135a promotes growth and invasion of colorectal cancer via metastasis suppressor 1 in vitro. Acta Biochim Biophys Sin. 2012;44(10):838–46.CrossRef
21.
go back to reference Wang B, Sun F, Dong N, Sun Z, Diao Y, Zheng C, Sun J, Yang Y, Jiang D. MicroRNA-7 directly targets insulin-like growth factor 1 receptor to inhibit cellular growth and glucose metabolism in gliomas. Diagn Pathol. 2014;9:211.CrossRef Wang B, Sun F, Dong N, Sun Z, Diao Y, Zheng C, Sun J, Yang Y, Jiang D. MicroRNA-7 directly targets insulin-like growth factor 1 receptor to inhibit cellular growth and glucose metabolism in gliomas. Diagn Pathol. 2014;9:211.CrossRef
22.
go back to reference Berg KCG, Eide PW, Eilertsen IA, Johannessen B, Bruun J, Danielsen SA, Bjornslett M, Meza-Zepeda LA, Eknaes M, Lind GE, et al. Multi-omics of 34 colorectal cancer cell lines—a resource for biomedical studies. Mol Cancer. 2017;16(1):116.CrossRef Berg KCG, Eide PW, Eilertsen IA, Johannessen B, Bruun J, Danielsen SA, Bjornslett M, Meza-Zepeda LA, Eknaes M, Lind GE, et al. Multi-omics of 34 colorectal cancer cell lines—a resource for biomedical studies. Mol Cancer. 2017;16(1):116.CrossRef
23.
go back to reference Marikar F, Jin G, Sheng W, Ma D, Hua Z. Metallothionein 2A an interactive protein linking phosphorylated FADD to NF-κB pathway leads to colorectal cancer formation. Chin Clin Oncol. 2016;5(6):76.CrossRef Marikar F, Jin G, Sheng W, Ma D, Hua Z. Metallothionein 2A an interactive protein linking phosphorylated FADD to NF-κB pathway leads to colorectal cancer formation. Chin Clin Oncol. 2016;5(6):76.CrossRef
24.
go back to reference Catto J, Alcaraz A, Bjartell A, De Vere White R, Evans C, Fussel S, Hamdy F, Kallioniemi O, Mengual L, Schlomm T, et al. MicroRNA in prostate, bladder, and kidney cancer: a systematic review. Eur Urol. 2011;59(5):671–81.CrossRef Catto J, Alcaraz A, Bjartell A, De Vere White R, Evans C, Fussel S, Hamdy F, Kallioniemi O, Mengual L, Schlomm T, et al. MicroRNA in prostate, bladder, and kidney cancer: a systematic review. Eur Urol. 2011;59(5):671–81.CrossRef
25.
go back to reference Yang J, Ma D, Fesler A, Zhai H, Leamniramit A, Li W, Wu S, Ju J. Expression analysis of microRNA as prognostic biomarkers in colorectal cancer. Oncotarget. 2017;8(32):52403–12.CrossRef Yang J, Ma D, Fesler A, Zhai H, Leamniramit A, Li W, Wu S, Ju J. Expression analysis of microRNA as prognostic biomarkers in colorectal cancer. Oncotarget. 2017;8(32):52403–12.CrossRef
26.
go back to reference Manne U, Jadhav T, Putcha B, Samuel T, Soni S, Shanmugam C, Suswam E. Molecular biomarkers of colorectal cancer and cancer disparities: current status and perspective. Curr Colorectal Cancer Rep. 2016;12(6):332–44.CrossRef Manne U, Jadhav T, Putcha B, Samuel T, Soni S, Shanmugam C, Suswam E. Molecular biomarkers of colorectal cancer and cancer disparities: current status and perspective. Curr Colorectal Cancer Rep. 2016;12(6):332–44.CrossRef
27.
go back to reference Tutar L, Tutar E, Tutar Y. MicroRNAs and cancer; an overview. Curr Pharm Biotechnol. 2014;15(5):430–7.CrossRef Tutar L, Tutar E, Tutar Y. MicroRNAs and cancer; an overview. Curr Pharm Biotechnol. 2014;15(5):430–7.CrossRef
28.
go back to reference Tan W, Liu B, Qu S, Liang G, Luo W, Gong C. MicroRNAs and cancer: key paradigms in molecular therapy. Oncol Lett. 2018;15(3):2735–42.PubMed Tan W, Liu B, Qu S, Liang G, Luo W, Gong C. MicroRNAs and cancer: key paradigms in molecular therapy. Oncol Lett. 2018;15(3):2735–42.PubMed
29.
go back to reference Bhome R, Goh R, Bullock M, Pillar N, Thirdborough S, Mellone M, Mirnezami R, Galea D, Veselkov K, Gu Q, et al. Exosomal microRNAs derived from colorectal cancer-associated fibroblasts: role in driving cancer progression. Aging. 2017;9(12):2666–94.CrossRef Bhome R, Goh R, Bullock M, Pillar N, Thirdborough S, Mellone M, Mirnezami R, Galea D, Veselkov K, Gu Q, et al. Exosomal microRNAs derived from colorectal cancer-associated fibroblasts: role in driving cancer progression. Aging. 2017;9(12):2666–94.CrossRef
30.
go back to reference Rani S, Gately K, Crown J, O’Byrne K, O’Driscoll L. Global analysis of serum microRNAs as potential biomarkers for lung adenocarcinoma. Cancer Biol Ther. 2013;14(12):1104–12.CrossRef Rani S, Gately K, Crown J, O’Byrne K, O’Driscoll L. Global analysis of serum microRNAs as potential biomarkers for lung adenocarcinoma. Cancer Biol Ther. 2013;14(12):1104–12.CrossRef
31.
go back to reference Zhang K, Zhou X, Han L, Chen L, Chen L, Shi Z, Yang M, Ren Y, Yang J, Frank T, et al. MicroRNA-566 activates EGFR signaling and its inhibition sensitizes glioblastoma cells to nimotuzumab. Mol Cancer. 2014;13:63.CrossRef Zhang K, Zhou X, Han L, Chen L, Chen L, Shi Z, Yang M, Ren Y, Yang J, Frank T, et al. MicroRNA-566 activates EGFR signaling and its inhibition sensitizes glioblastoma cells to nimotuzumab. Mol Cancer. 2014;13:63.CrossRef
32.
go back to reference Xiao B, Zhou X, Ye M, Lv S, Wu M, Liao C, Han L, Kang C, Zhu X. MicroRNA-566 modulates vascular endothelial growth factor by targeting Von Hippel-Landau in human glioblastoma in vitro and in vivo. Mol Med Rep. 2016;13(1):379–85.CrossRef Xiao B, Zhou X, Ye M, Lv S, Wu M, Liao C, Han L, Kang C, Zhu X. MicroRNA-566 modulates vascular endothelial growth factor by targeting Von Hippel-Landau in human glioblastoma in vitro and in vivo. Mol Med Rep. 2016;13(1):379–85.CrossRef
33.
go back to reference Manning G, Whyte D, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science. 2002;298(5600):1912–34.CrossRef Manning G, Whyte D, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science. 2002;298(5600):1912–34.CrossRef
34.
go back to reference Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature. 2001;411(6835):355–65.CrossRef Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature. 2001;411(6835):355–65.CrossRef
35.
go back to reference Brede G, Solheim J, Stang E, Prydz H. Mutants of the protein serine kinase PSKH1 disassemble the Golgi apparatus. Exp Cell Res. 2003;291(2):299–312.CrossRef Brede G, Solheim J, Stang E, Prydz H. Mutants of the protein serine kinase PSKH1 disassemble the Golgi apparatus. Exp Cell Res. 2003;291(2):299–312.CrossRef
Metadata
Title
MiR-566 mediates cell migration and invasion in colon cancer cells by direct targeting of PSKH1
Authors
Ying Zhang
Siqi Zhang
Jian Yin
Ruisi Xu
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2019
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-019-1053-1

Other articles of this Issue 1/2019

Cancer Cell International 1/2019 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine