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
May-2024 Volume 27 Issue 5

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
May-2024 Volume 27 Issue 5

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_Data.pdf
Article Open Access

The expression of trefoil factor family member 2 in increased at an acidic pH

  • Authors:
    • Yui Masumoto
    • Suzuka Matsuo
    • Natsuno Kinjou
    • Yuka Narieda
    • Morimasa Wada
    • Kyoko Fujimoto
  • View Affiliations / Copyright

    Affiliations: Division of Biochemistry, Department of Pharmacy, Nagasaki International University, Sasebo, Nagasaki 859 3298, Japan, Division of Molecular Biology, Department of Pharmacy, Nagasaki International University, Sasebo, Nagasaki 859 3298, Japan
    Copyright: © Masumoto et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 212
    |
    Published online on: March 15, 2024
       https://doi.org/10.3892/ol.2024.14345
  • 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

Trefoil factor family member 2 (Tff2) is significantly involved in intestinal tumor growth in ApcMin/+ mice, which can be used as a human colon cancer model. TFF2, which encodes TFF2 (spasmolytic protein 1) is highly expressed in human cancer tissues, including the pancreas, colon and bile ducts, as well as in normal gastric and duodenum tissues. By contrast, TFF2 exhibits low expression levels in other normal tissues, including the small and large intestine. Furthermore, TFF2 expression has not been detected in DLD‑1 cells, a cell line derived from human colon cancer. What induces TFF2 expression in normal and tumor cells is still unknown. Highly malignant tumor tissues are characterized by higher temperatures and lower pH (6.2‑6.9) than in normal tissues, where normal pH ranges from 7.2 to 7.4. This microenvironment exacerbates malignancy by promoting the acquisition of cell death resistance, drug resistance and immune escape. Therefore, the present study examined how TFF2 expression is affected in cultured cells that imitate the tumor tissue microenvironment. The incubation temperature was increased from 37 to 40˚C, but no expression of TFF2 was induced. Subsequently, a culture solution with an acidic pH was prepared to simulate the Warburg effect in tumors. TFF2 expression was increased by 42.8‑ and 5.8‑fold in cells cultured in acidic medium at pH 6.5 and 6.8 compared with at pH 7.4, respectively, as determined using the relative quantification method following quantitative polymerase chain reaction. The present study also analyzed fluctuations in the expression levels of genes other than TFF2, under acidic conditions. Acidic conditions upregulated the expression of genes related to cell membranes and glycoproteins, based on the Database for Annotation, Visualization, and Integrated Discovery. In conclusion, TFF2 was highly expressed under acidic conditions, implying that it may have an important function in protecting the plasma membrane from acidic environments in both normal and cancer cells. These findings warrant further investigation of TFF2 as a target of cancer therapy and diagnosis.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

View References

1 

Fujimoto K, Fujii G, Taguchi K, Yasuda K, Matsuo Y, Hashiyama A, Mutoh M, Tanaka H and Wada M: Involvement of trefoil factor family 2 in the enlargement of intestinal tumors in Apc(Min/+) mice. Biochem Biophys Res Commun. 463:859–863. 2015. View Article : Google Scholar : PubMed/NCBI

2 

Ma X, Yuan W and Ma J: Expression level of miR-199b in human colorectal cancer tissues and its correlation with clinicopathological features and prognosis of patients. Zhonghua Zhong Liu Za Zhi. 45:330–334. 2023.(In Chinese). PubMed/NCBI

3 

Qu Y, Yang Y, Ma D and Xiao W: Increased trefoil factor 3 levels in the serum of patients with three major histological subtypes of lung cancer. Oncol Rep. 27:1277–1283. 2012. View Article : Google Scholar : PubMed/NCBI

4 

Minegishi K, Dobashi Y, Koyama T, Ishibashi Y, Furuya M, Tsubochi H, Ohmoto Y, Yasuda T and Nomura S: Diagnostic utility of trefoil factor families for the early detection of lung cancer and their correlation with tissue expression. Oncol Lett. 25:1392023. View Article : Google Scholar : PubMed/NCBI

5 

Aihara E, Engevik KA and Montrose MH: Trefoil factor peptides and gastrointestinal function. Annu Rev Physiol. 79:357–380. 2017. View Article : Google Scholar : PubMed/NCBI

6 

Guo M, Wang R, Geng J, Li Z and Liu M, Lu X, Wei J and Liu M: Human TFF2-Fc fusion protein alleviates DSS-induced ulcerative colitis in C57BL/6 mice by promoting intestinal epithelial cells repair and inhibiting macrophage inflammation. Inflammopharmacology. 3:1387–1404. 2023. View Article : Google Scholar : PubMed/NCBI

7 

Kosriwong K, Menheniott TR, Giraud AS, Jearanaikoon P, Sripa B and Limpaiboon T: Trefoil factors: Tumor progression markers and mitogens via EGFR/MAPK activation in cholangiocarcinoma. World J Gastroenterol. 17:1631–1641. 2011. View Article : Google Scholar : PubMed/NCBI

8 

Jahan R, Ganguly K, Smith LM, Atri P, Carmicheal J, Sheinin Y, Rachagani S, Natarajan G, Brand RE, Macha MA, et al: Trefoil factor(s) and CA19.9: A promising panel for early detection of pancreatic cancer. EBioMedicene. 42:375–385. 2019. View Article : Google Scholar

9 

Asaka S, Nakajima T, Momose M, Miyamoto T, Uehara T and Ota H: Trefoil factor family 2 protein: A potential immunohistochemical marker for aiding diagnosis of lobular endocervical glandular hyperplasia and gastric-type adenocarcinoma of the uterine cervix. Virchows Arch. 474:79–86. 2019. View Article : Google Scholar : PubMed/NCBI

10 

Jahan R, Shah A, Kisling SG, Macha MA, Thayer S, Batra SK and Kaur S: Odyssey of trefoil factors in cancer: Diagnostic and therapeutic implications. Biochim Biophys Acta Rev Cancer. 1873:1883622020. View Article : Google Scholar : PubMed/NCBI

11 

Zhang Y, Liu Y, Wang L and Song H: The expression and role of trefoil factors in human tumors. Transl Cancer Res. 8:1609–1617. 2019. View Article : Google Scholar : PubMed/NCBI

12 

So JY, Ohm J, Lipkowitz S and Yang L: Triple negative breast cancer (TNBC): Non-genetic tumor heterogeneity and immune microenvironment: Emerging treatment options. Pharmacol Ther. 237:1082532022. View Article : Google Scholar : PubMed/NCBI

13 

Funato Y, Yoshida A, Hirata Y, Hashizume O, Yamazaki D and Miki H: The oncogenic PRL protein causes acid addiction of cells by stimulating lysosomal exocytosis. Dev Cell. 55:387–397.e8. 2020. View Article : Google Scholar : PubMed/NCBI

14 

Pentheroudakis G, Kotoula V, Fountzilas E, Kouvatseas G, Basdanis G, Xanthakis I, Makatsoris T, Charalambous E, Papamichael D, Samantas E, et al: A study of gene expression markers for predictive significance for bevacizumab benefit in patients with metastatic colon cancer: A translational research study of the Hellenic Cooperative Oncology Group (HeCOG). BMC Cancer. 14:1112014. View Article : Google Scholar : PubMed/NCBI

15 

Otsuka K, Yamamoto Y and Ochiya T: Uncovering temperature-dependent extracellular vesicle secretion in breast cancer. J Extracell Vesicles. 10:e120492020. View Article : Google Scholar : PubMed/NCBI

16 

Pitt MA: Increased temperature and entropy production in cancer: The role of anti-inflammatory drugs. Inflammopharmacology. 23:17–20. 2015. View Article : Google Scholar : PubMed/NCBI

17 

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

18 

Miyahara E, Nishikawa T, Takeuchi T, Yasuda K, Okamoto Y, Kawano Y and Horiuchi M: Effect of myeloperoxidase inhibition on gene expression profiles in HL-60 cells exposed to 1,2,4-benzenetriol. Toxicology. 317:50–57. 2014. View Article : Google Scholar : PubMed/NCBI

19 

Landry J, Bernier D, Chrétien P, Nicole LM, Tanguay RM and Marceau N: Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res. 42:2457–2461. 1982.PubMed/NCBI

20 

Pettersen IKN, Tusubira D, Ashrafi H, Dyrstad SE, Hansen L, Liu XZ, Nilsson LIH, Løvsletten NG, Berge K, Wergedahl H, et al: Upregulated PDK4 expression is a sensitive marker of increased fatty acid oxidation. Mitochondrion. 49:97–110. 2019. View Article : Google Scholar : PubMed/NCBI

21 

Hoffmann W: Trefoil factor family (TFF) peptides and their diverse molecular functions in mucus barrier protection and more: Changing the paradigm. Int J Mol Sci. 21:45352020. View Article : Google Scholar : PubMed/NCBI

22 

Ishibashi Y, Ohtsu H, Ikemura M, Kikuchi Y, Niwa T, Nishioka K, Uchida Y, Miura H, Aikou S, Gunji T, et al: Serum TFF1 and TFF3 but not TFF2 are higher in women with breast cancer in women without breast cancer. Sci Rep. 7:48462017. View Article : Google Scholar : PubMed/NCBI

23 

Nogueira-Librelotto DR, Scheeren LE, Macedo LB, Vinardell MP and Rolim CMB: pH-sensitive chitosan-tripolyphoshate nanoparticles increase doxorubicin-induced growth inhibition of cervical HeLa tumor cells by apoptosis and cell cycle modulation. Colloids Surf B Biointerfaces. 190:1108972020. View Article : Google Scholar : PubMed/NCBI

24 

Szlase W, Zendran I, Zalesińska A, Tarek M and Kulbacka J: Lipid composition of the cancer cell membrane. J Bioenerg Biomembr. 52:321–342. 2020. View Article : Google Scholar : PubMed/NCBI

25 

Yu G, Jiang P, Xiang Y and Zhang Y, Zhu Z, Zhang C, Lee S, Lee W and Zhang Y: Increased expression of protease-activated receptor 4 and trefoil factor 2 in human colorectal cancer. PLoS One. 10:e01226782015. View Article : Google Scholar : PubMed/NCBI

26 

Gala MK, Austin T, Ogino S and Chan AT: TFF2-CXCR4 axis is associated with BRAF V600E colon cancer. Cancer Prev Res. 8:614–619. 2015. View Article : Google Scholar : PubMed/NCBI

27 

Hoffmann W: Trefoil factor family (TFF) peptides and their different roles in the mucosal innate immune defense and more: An update. Curr Med Chem. 28:7387–7399. 2021. View Article : Google Scholar : PubMed/NCBI

28 

Järvå MA, Lingford JP, John A, Soler NM, Scott NE and Goddard-Borger ED: Trefoil factors share a lectin activity that defines their role in mucus. Nat Commun. 11:22652020. View Article : Google Scholar : PubMed/NCBI

29 

Wu C, Zhang J, Wang M, Du G and Chen J: Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol. 39:1031–1039. 2012. View Article : Google Scholar : PubMed/NCBI

30 

Guan N and Liu L: Microbial response to acid stress: Mechanisms and applications. Appl Microbiol Biotechnol. 104:51–65. 2020. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Masumoto Y, Matsuo S, Kinjou N, Narieda Y, Wada M and Fujimoto K: The expression of trefoil factor family member 2 in increased at an acidic pH. Oncol Lett 27: 212, 2024.
APA
Masumoto, Y., Matsuo, S., Kinjou, N., Narieda, Y., Wada, M., & Fujimoto, K. (2024). The expression of trefoil factor family member 2 in increased at an acidic pH. Oncology Letters, 27, 212. https://doi.org/10.3892/ol.2024.14345
MLA
Masumoto, Y., Matsuo, S., Kinjou, N., Narieda, Y., Wada, M., Fujimoto, K."The expression of trefoil factor family member 2 in increased at an acidic pH". Oncology Letters 27.5 (2024): 212.
Chicago
Masumoto, Y., Matsuo, S., Kinjou, N., Narieda, Y., Wada, M., Fujimoto, K."The expression of trefoil factor family member 2 in increased at an acidic pH". Oncology Letters 27, no. 5 (2024): 212. https://doi.org/10.3892/ol.2024.14345
Copy and paste a formatted citation
x
Spandidos Publications style
Masumoto Y, Matsuo S, Kinjou N, Narieda Y, Wada M and Fujimoto K: The expression of trefoil factor family member 2 in increased at an acidic pH. Oncol Lett 27: 212, 2024.
APA
Masumoto, Y., Matsuo, S., Kinjou, N., Narieda, Y., Wada, M., & Fujimoto, K. (2024). The expression of trefoil factor family member 2 in increased at an acidic pH. Oncology Letters, 27, 212. https://doi.org/10.3892/ol.2024.14345
MLA
Masumoto, Y., Matsuo, S., Kinjou, N., Narieda, Y., Wada, M., Fujimoto, K."The expression of trefoil factor family member 2 in increased at an acidic pH". Oncology Letters 27.5 (2024): 212.
Chicago
Masumoto, Y., Matsuo, S., Kinjou, N., Narieda, Y., Wada, M., Fujimoto, K."The expression of trefoil factor family member 2 in increased at an acidic pH". Oncology Letters 27, no. 5 (2024): 212. https://doi.org/10.3892/ol.2024.14345
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