Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Letters
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-1074 Online ISSN: 1792-1082
Journal Cover
September-2023 Volume 26 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
September-2023 Volume 26 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML

  • Supplementary Files
    • Supplementary_Data1.pdf
    • Supplementary_Data2.pdf
Article Open Access

Silencing of GRHL2 induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth

  • Authors:
    • Nozomi Kawabe
    • Kohei Matsuoka
    • Kazuki Komeda
    • Nao Muraki
    • Miho Takaba
    • Yasuha Togami
    • Yumeno Ito
    • Mizuki Yamada
    • Noriaki Sunaga
    • Luc Girard
    • John D. Minna
    • Ling Cai
    • Yang Xie
    • Ichidai Tanaka
    • Masahiro Morise
    • Mitsuo Sato
  • View Affiliations / Copyright

    Affiliations: Division of Host Defense Sciences, Department of Integrated Health Sciences, Nagoya University Graduate School of Medicine, Nagoya, Aichi 461‑8673, Japan, Department of Respiratory Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma 371‑8511, Japan, Hamon Center for Therapeutic Oncology Research, Simmons Comprehensive Cancer Center, UT Southwestern Medical Center, Dallas, TX 75230‑8593, USA, Quantitative Biomedical Research Center, Peter O’Donnell School of Public Health, UT Southwestern Medical Center, Dallas, TX 75230‑8593, USA, Department of Respiratory Medicine, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466‑8550, Japan
    Copyright: © Kawabe et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 391
    |
    Published online on: July 25, 2023
       https://doi.org/10.3892/ol.2023.13977
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Grainyhead‑like 2 (GRHL2) is a transcription factor that suppresses epithelial‑to‑mesenchymal transition (EMT). It has been previously shown that GRHL2 can confer both oncogenic and tumor‑suppressive roles in human cancers, including breast, pancreatic and colorectal cancers. However, its role in lung cancer remains elusive. In the present study, a meta‑analysis of multiple gene expression datasets with clinical data revealed that GRHL2 expression was increased in lung cancer compared with that in the normal tissues. Copy number analysis of GRHL2, performed using datasets of whole exome sequencing involving 151 lung cancer cell lines, revealed frequent amplifications, suggesting that the increased GRHL2 expression may have resulted from gene amplification. A survival meta‑analysis of GRHL2 using The Cancer Genome Atlas (TCGA) dataset showed no association of GRHL2 expression with overall survival. GRHL2 expression was found to be associated with EMT status in lung cancer in TCGA dataset and lung cancer cell lines. GRHL2 knockdown induced partial EMT in the hTERT/Cdk4‑immortalized normal lung epithelial cell line HBEC4KT without affecting proliferation measured by CCK‑8 assays. In addition, GRHL2 silencing caused three lung cancer cell lines, H1975, H2009 and H441, to undergo partial EMT. However, the proliferative effects differed significantly. GRHL2 silencing promoted proliferation but not colony formation in H1975 cells whilst suppressing colony formation without affecting proliferation in H2009 cells, but it did not affect proliferation in H441 cells. These results suggest cell type‑dependent effects of GRHL2 knockdown. Downstream, GRHL2 silencing enhanced the phosphorylation of AKT and ERK, assessed by western blotting with phospho‑specific antibodies, in HBEC4KT, H1975 and H2009 cell lines but not in the H441 cell line. By contrast, transient GRHL2 overexpression did not affect A549 cell proliferation, which lack detectable endogenous expression of the GRHL2 protein. However, GRHL2 overexpression did suppress E‑cadherin expression in A549 cells. These results suggested that GRHL2 does not only function as a tumor suppressor of EMT but can also behave as an oncogene depending on the lung cancer cell‑type context.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

View References

1 

Hay ED: An overview of epithelio-mesenchymal transformation. Acta Anat (Basel). 154:8–20. 1995. View Article : Google Scholar : PubMed/NCBI

2 

Lim J and Thiery JP: Epithelial-mesenchymal transitions: Insights from development. Development. 139:3471–3486. 2012. View Article : Google Scholar : PubMed/NCBI

3 

Nieto MA, Huang RY, Jackson RA and Thiery JP: EMT: 2016. Cell. 166:21–45. 2016. View Article : Google Scholar : PubMed/NCBI

4 

Puisieux A, Brabletz T and Caramel J: Oncogenic roles of EMT-inducing transcription factors. Nat Cell Biol. 16:488–494. 2014. View Article : Google Scholar : PubMed/NCBI

5 

Frisch SM, Farris JC and Pifer PM: Roles of grainyhead-like transcription factors in cancer. Oncogene. 36:6067–6073. 2017. View Article : Google Scholar : PubMed/NCBI

6 

He J, Feng C, Zhu H, Wu S, Jin P and Xu T: Grainyhead-like 2 as a double-edged sword in development and cancer. Am J Transl Res. 12:310–331. 2020.PubMed/NCBI

7 

Chung VY, Tan TZ, Tan M, Wong MK, Kuay KT, Yang Z, Ye J, Muller J, Koh CM, Guccione E, et al: GRHL2-miR-200-ZEB1 maintains the epithelial status of ovarian cancer through transcriptional regulation and histone modification. Sci Rep. 6:199432016. View Article : Google Scholar : PubMed/NCBI

8 

Cieply B, Farris J, Denvir J, Ford HL and Frisch SM: Epithelial-mesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and grainyhead-like-2. Cancer Res. 73:6299–6309. 2013. View Article : Google Scholar : PubMed/NCBI

9 

Cieply B, Riley P IV, Pifer PM, Widmeyer J, Addison JB, Ivanov AV, Denvir J and Frisch SM: Suppression of the epithelial-mesenchymal transition by grainyhead-like-2. Cancer Res. 72:2440–2453. 2012. View Article : Google Scholar : PubMed/NCBI

10 

Farris JC, Pifer PM, Zheng L, Gottlieb E, Denvir J and Frisch SM: Grainyhead-like 2 reverses the metabolic changes induced by the oncogenic epithelial-mesenchymal transition: Effects on anoikis. Mol Cancer Res. 14:528–538. 2016. View Article : Google Scholar : PubMed/NCBI

11 

Nishino H, Takano S, Yoshitomi H, Suzuki K, Kagawa S, Shimazaki R, Shimizu H, Furukawa K, Miyazaki M and Ohtsuka M: Grainyhead-like 2 (GRHL2) regulates epithelial plasticity in pancreatic cancer progression. Cancer Med. 6:2686–2696. 2017. View Article : Google Scholar : PubMed/NCBI

12 

Pan X, Zhang R, Xie C, Gan M, Yao S, Yao Y, Jin J, Han T, Huang Y, Gong Y, et al: GRHL2 suppresses tumor metastasis via regulation of transcriptional activity of RhoG in non-small cell lung cancer. Am J Transl Res. 9:4217–4226. 2017.PubMed/NCBI

13 

Shen J, Lv X and Zhang L: GRHL2 acts as an anti-oncogene in bladder cancer by regulating ZEB1 in epithelial-mesenchymal transition (EMT) process. Onco Targets Ther. 13:2511–2522. 2020. View Article : Google Scholar : PubMed/NCBI

14 

Werner S, Frey S, Riethdorf S, Schulze C, Alawi M, Kling L, Vafaizadeh V, Sauter G, Terracciano L, Schumacher U, et al: Dual roles of the transcription factor grainyhead-like 2 (GRHL2) in breast cancer. J Biol Chem. 288:22993–23008. 2013. View Article : Google Scholar : PubMed/NCBI

15 

Xiang J, Fu X, Ran W and Wang Z: Grhl2 reduces invasion and migration through inhibition of TGFβ-induced EMT in gastric cancer. Oncogenesis. 6:e2842017. View Article : Google Scholar : PubMed/NCBI

16 

Xiang X, Deng Z, Zhuang X, Ju S, Mu J, Jiang H, Zhang L, Yan J, Miller D and Zhang HG: Grhl2 determines the epithelial phenotype of breast cancers and promotes tumor progression. PLoS One. 7:e507812012. View Article : Google Scholar : PubMed/NCBI

17 

Yang Z, Wu D, Chen Y, Min Z and Quan Y: GRHL2 inhibits colorectal cancer progression and metastasis via oppressing epithelial-mesenchymal transition. Cancer Biol Ther. 20:1195–1205. 2019. View Article : Google Scholar : PubMed/NCBI

18 

Chen W, Kang KL, Alshaikh A, Varma S, Lin YL, Shin KH, Kim R, Wang CY, Park NH, Walentin K, et al: Grainyhead-like 2 (GRHL2) knockout abolishes oral cancer development through reciprocal regulation of the MAP kinase and TGF-β signaling pathways. Oncogenesis. 7:382018. View Article : Google Scholar : PubMed/NCBI

19 

Faddaoui A, Sheta R, Bachvarova M, Plante M, Gregoire J, Renaud MC, Sebastianelli A, Gobeil S, Morin C, Ghani K and Bachvarov D: Suppression of the grainyhead transcription factor 2 gene (GRHL2) inhibits the proliferation, migration, invasion and mediates cell cycle arrest of ovarian cancer cells. Cell Cycle. 16:693–706. 2017. View Article : Google Scholar : PubMed/NCBI

20 

Hu F, He Z, Sun C and Rong D: Knockdown of GRHL2 inhibited proliferation and induced apoptosis of colorectal cancer by suppressing the PI3K/Akt pathway. Gene. 700:96–104. 2019. View Article : Google Scholar : PubMed/NCBI

21 

Quan Y, Jin R, Huang A, Zhao H, Feng B, Zang L and Zheng M: Downregulation of GRHL2 inhibits the proliferation of colorectal cancer cells by targeting ZEB1. Cancer Biol Ther. 15:878–887. 2014. View Article : Google Scholar : PubMed/NCBI

22 

Jolly MK, Tripathi SC, Jia D, Mooney SM, Celiktas M, Hanash SM, Mani SA, Pienta KJ, Ben-Jacob E and Levine H: Stability of the hybrid epithelial/mesenchymal phenotype. Oncotarget. 7:27067–27084. 2016. View Article : Google Scholar : PubMed/NCBI

23 

Cai L, Lin S, Girard L, Zhou Y, Yang L, Ci B, Zhou Q, Luo D, Yao B, Tang H, et al: LCE: An open web portal to explore gene expression and clinical associations in lung cancer. Oncogene. 38:2551–2564. 2019. View Article : Google Scholar : PubMed/NCBI

24 

Sato M, Shames DS and Hasegawa Y: Emerging evidence of epithelial-to-mesenchymal transition in lung carcinogenesis. Respirology. 17:1048–1059. 2012. View Article : Google Scholar : PubMed/NCBI

25 

Sato M, Shay JW and Minna JD: Immortalized normal human lung epithelial cell models for studying lung cancer biology. Respir Investig. 58:344–354. 2020. View Article : Google Scholar : PubMed/NCBI

26 

Sato M, Vaughan MB, Girard L, Peyton M, Lee W, Shames DS, Ramirez RD, Sunaga N, Gazdar AF, Shay JW and Minna JD: Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res. 66:2116–2128. 2006. View Article : Google Scholar : PubMed/NCBI

27 

Phelps RM, Johnson BE, Ihde DC, Gazdar AF, Carbone DP, McClintock PR, Linnoila RI, Matthews MJ, Bunn PA Jr, Carney D, et al: NCI-navy medical oncology branch cell line data base. J Cell Biochem Suppl. 24:32–91. 1996. View Article : Google Scholar : PubMed/NCBI

28 

Ramirez RD, Sheridan S, Girard L, Sato M, Kim Y, Pollack J, Peyton M, Zou Y, Kurie JM, Dimaio JM, et al: Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 64:9027–9034. 2004. View Article : Google Scholar : PubMed/NCBI

29 

van Kuppeveld FJ, Johansson KE, Galama JM, Kissing J, Bölske G, van der Logt JT and Melchers WJ: Detection of mycoplasma contamination in cell cultures by a mycoplasma group-specific PCR. Appl Environ Microbiol. 60:149–152. 1994. View Article : Google Scholar : PubMed/NCBI

30 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI

31 

Sato M, Girard L, Sekine I, Sunaga N, Ramirez RD, Kamibayashi C and Minna JD: Increased expression and no mutation of the Flap endonuclease (FEN1) gene in human lung cancer. Oncogene. 22:7243–7246. 2003. View Article : Google Scholar : PubMed/NCBI

32 

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al: Fiji: An open-source platform for biological-image analysis. Nat Methods. 9:676–682. 2012. View Article : Google Scholar : PubMed/NCBI

33 

Schneider CA, Rasband WS and Eliceiri KW: NIH image to imageJ: 25 Years of image analysis. Nat Methods. 9:671–675. 2012. View Article : Google Scholar : PubMed/NCBI

34 

McMillan EA, Ryu MJ, Diep CH, Mendiratta S, Clemenceau JR, Vaden RM, Kim JH, Motoyaji T, Covington KR, Peyton M, et al: Chemistry-first approach for nomination of personalized treatment in lung cancer. Cell. 173:864–878.e29. 2018. View Article : Google Scholar : PubMed/NCBI

35 

Kanda Y: Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 48:452–458. 2013. View Article : Google Scholar : PubMed/NCBI

36 

Saitoh M: Involvement of partial EMT in cancer progression. J Biochem. 164:257–264. 2018. View Article : Google Scholar : PubMed/NCBI

37 

Das AK, Sato M, Story MD, Peyton M, Graves R, Redpath S, Girard L, Gazdar AF, Shay JW, Minna JD and Nirodi CS: Non-small-cell lung cancers with kinase domain mutations in the epidermal growth factor receptor are sensitive to ionizing radiation. Cancer Res. 66:9601–9608. 2006. View Article : Google Scholar : PubMed/NCBI

38 

Sunaga N, Imai H, Shimizu K, Shames DS, Kakegawa S, Girard L, Sato M, Kaira K, Ishizuka T, Gazdar AF, et al: Oncogenic KRAS-induced interleukin-8 overexpression promotes cell growth and migration and contributes to aggressive phenotypes of non-small cell lung cancer. Int J Cancer. 130:1733–1744. 2012. View Article : Google Scholar : PubMed/NCBI

39 

Chen L, Liu H, Ji Y, Ma Z, Shen K, Shangguan X, Qian H, Zhao Y, Pan CW and Xue W: Downregulation of SHMT2 promotes the prostate cancer proliferation and metastasis by inducing epithelial-mesenchymal transition. Exp Cell Res. 415:1131382022. View Article : Google Scholar : PubMed/NCBI

40 

He F, Feng G, Ma N, Midorikawa K, Oikawa S, Kobayashi H, Zhang Z, Huang G, Takeuchi K and Murata M: GDF10 inhibits cell proliferation and epithelial-mesenchymal transition in nasopharyngeal carcinoma by the transforming growth factor-β/Smad and NF-κB pathways. Carcinogenesis. 43:94–103. 2022. View Article : Google Scholar : PubMed/NCBI

41 

Huang W, Huang H, Xiao Y, Wang L, Zhang T, Fang X and Xia X: UBE2T is upregulated, predicts poor prognosis, and promotes cell proliferation and invasion by promoting epithelial-mesenchymal transition via inhibiting autophagy in an AKT/mTOR dependent manner in ovarian cancer. Cell Cycle. 21:780–791. 2022. View Article : Google Scholar : PubMed/NCBI

42 

Ding C, Luo J, Li L, Li S, Yang L, Pan H, Liu Q, Qin H, Chen C and Feng J: Gab2 facilitates epithelial-to-mesenchymal transition via the MEK/ERK/MMP signaling in colorectal cancer. J Exp Clin Cancer Res. 35:52016. View Article : Google Scholar : PubMed/NCBI

43 

Karimi Roshan M, Soltani A, Soleimani A, Rezaie Kahkhaie K, Afshari AR and Soukhtanloo M: Role of AKT and mTOR signaling pathways in the induction of epithelial-mesenchymal transition (EMT) process. Biochimie. 165:229–234. 2019. View Article : Google Scholar : PubMed/NCBI

44 

Xu M, Cao FL, Li N, Gao X, Su X and Jiang X: Leptin induces epithelial-to-mesenchymal transition via activation of the ERK signaling pathway in lung cancer cells. Oncol Lett. 16:4782–4788. 2018.PubMed/NCBI

45 

Cook SJ, Stuart K, Gilley R and Sale MJ: Control of cell death and mitochondrial fission by ERK1/2 MAP kinase signalling. FEBS J. 284:4177–4195. 2017. View Article : Google Scholar : PubMed/NCBI

46 

Brix N, Samaga D, Belka C, Zitzelsberger H and Lauber K: Analysis of clonogenic growth in vitro. Nat Protoc. 16:4963–4991. 2021. View Article : Google Scholar : PubMed/NCBI

47 

Franken NAP, Rodermond HM, Stap J, Haveman J and van Bree C: Clonogenic assay of cells in vitro. Nat Protoc. 1:2315–2319. 2006. View Article : Google Scholar : PubMed/NCBI

48 

Chen AF, Liu AJ, Krishnakumar R, Freimer JW, DeVeale B and Blelloch R: GRHL2-Dependent enhancer switching maintains a pluripotent stem cell transcriptional subnetwork after exit from naive pluripotency. Cell Stem Cell. 23:226–238.e4. 2018. View Article : Google Scholar : PubMed/NCBI

49 

Gao X, Bali AS, Randell SH and Hogan BL: GRHL2 coordinates regeneration of a polarized mucociliary epithelium from basal stem cells. J Cell Biol. 211:669–682. 2015. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Kawabe N, Matsuoka K, Komeda K, Muraki N, Takaba M, Togami Y, Ito Y, Yamada M, Sunaga N, Girard L, Girard L, et al: Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth. Oncol Lett 26: 391, 2023.
APA
Kawabe, N., Matsuoka, K., Komeda, K., Muraki, N., Takaba, M., Togami, Y. ... Sato, M. (2023). Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth. Oncology Letters, 26, 391. https://doi.org/10.3892/ol.2023.13977
MLA
Kawabe, N., Matsuoka, K., Komeda, K., Muraki, N., Takaba, M., Togami, Y., Ito, Y., Yamada, M., Sunaga, N., Girard, L., Minna, J. D., Cai, L., Xie, Y., Tanaka, I., Morise, M., Sato, M."Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth". Oncology Letters 26.3 (2023): 391.
Chicago
Kawabe, N., Matsuoka, K., Komeda, K., Muraki, N., Takaba, M., Togami, Y., Ito, Y., Yamada, M., Sunaga, N., Girard, L., Minna, J. D., Cai, L., Xie, Y., Tanaka, I., Morise, M., Sato, M."Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth". Oncology Letters 26, no. 3 (2023): 391. https://doi.org/10.3892/ol.2023.13977
Copy and paste a formatted citation
x
Spandidos Publications style
Kawabe N, Matsuoka K, Komeda K, Muraki N, Takaba M, Togami Y, Ito Y, Yamada M, Sunaga N, Girard L, Girard L, et al: Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth. Oncol Lett 26: 391, 2023.
APA
Kawabe, N., Matsuoka, K., Komeda, K., Muraki, N., Takaba, M., Togami, Y. ... Sato, M. (2023). Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth. Oncology Letters, 26, 391. https://doi.org/10.3892/ol.2023.13977
MLA
Kawabe, N., Matsuoka, K., Komeda, K., Muraki, N., Takaba, M., Togami, Y., Ito, Y., Yamada, M., Sunaga, N., Girard, L., Minna, J. D., Cai, L., Xie, Y., Tanaka, I., Morise, M., Sato, M."Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth". Oncology Letters 26.3 (2023): 391.
Chicago
Kawabe, N., Matsuoka, K., Komeda, K., Muraki, N., Takaba, M., Togami, Y., Ito, Y., Yamada, M., Sunaga, N., Girard, L., Minna, J. D., Cai, L., Xie, Y., Tanaka, I., Morise, M., Sato, M."Silencing of <em>GRHL2</em> induces epithelial‑to‑mesenchymal transition in lung cancer cell lines with different effects on proliferation and clonogenic growth". Oncology Letters 26, no. 3 (2023): 391. https://doi.org/10.3892/ol.2023.13977
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team