Decrement of Transcriptome Level in Epithelial Tight Junction Claudin and Occludin as an Epithelial-Mesenchymal Transition Signature for Colorectal Cancer Biomarker

  • Maryam Ghoojaei Department of Biology, University of Central Florida, Florida, United States
  • Reza Shirkoohi Cancer Biology Research Center, Cancer Research Institute, Imam Khomeini Hospital Complex, Tehran University of Medical Sciences, Tehran, Iran
  • Mojtaba Saffari Department of Genetics, Faculty of Medicine, Tehran University of Medical Sciences, Tehran, Iran
  • Amirnader Emamirazavi Iran National Tumor Bank, Cancer Institute of Iran, Tehran University of Medical Sciences, Tehran, Iran
  • Mehrdad Hashemi Department of Genetics, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran; Farhikhtegan Medical Convergence Sciences Research Center, Farhikhtegan Hospital Tehran Medical sciences, Islamic Azad University, Tehran, Iran
Keywords: Colorectal Cancer, Metastasis, Gene Expression, Claudins, Occludin

Abstract

Background: Colorectal cancer is a common and fatal disease worldwide with increasing diagnosed cases yearly. Moreover, about 90% of deaths associated with cancers occur due to metastasis, which overcomes tight junction proteins such as claudin and occludin. The present study aimed to evaluate the significance of claudin and occludin expression change in human colorectal cancer. Materials and Methods: In this case-control study, 38 colorectal cancer patients were compared with normal samples regarding the expression levels of claudin and occludin genes by polymerase chain reaction. Results: The expression levels of claudin and occludin significantly decreased in tumor samples compared to normal samples. Conclusion: The change in the expression level of the claudin and occludin genes could be considered an influential factor in turning normal healthy tissues into cancerous cells.

References

Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74-108.

https://doi.org/10.3322/canjclin.55.2.74

PMid:15761078

Stewart BW, Wild CP. Lyon: International Agency for Research on Cancer. World Cancer Report; 2014.

Vega P, Valentín F, Cubiella J. Colorectal cancer diagnosis: Pitfalls and opportunities. World J Gastrointest Oncol. 2015;7(12):422.

https://doi.org/10.4251/wjgo.v7.i12.422

PMid:26690833 PMCid:PMC4678389

NCI. Adult Treatment Editorial Board. 2022 [Accessed 2016 June 8]. Available from: https://www.cancer.gov/types/colorectal/patient/rectal-treatment-pdq.

Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002;2(3):161-74.

https://doi.org/10.1038/nrc745

PMid:11990853

Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1(1):27-30.

https://doi.org/10.1038/nm0195-27

PMid:7584949

Radisky DC. Epithelial-mesenchymal transition. J Cell Sci. 2005;118(19):

https://doi.org/10.1242/jcs.02552

PMid:16179603

-6.

Craene BD, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer. 2013;13(2):97-110.

https://doi.org/10.1038/nrc3447

PMid:23344542

Chakrabarti R, Hwang J, Andres Blanco M, Wei Y, Lukačišin M, Romano RA, et al. Elf5 inhibits the epithelial-mesenchymal transition in mammary gland development and breast cancer metastasis by transcriptionally repressing Snail2. Nat Cell Biol. 2012;14(11):1212-22.

https://doi.org/10.1038/ncb2607

PMid:23086238 PMCid:PMC3500637

Denker BM, Nigam SK. Molecular structure and assembly of the tight junction. Am J Physiol Renal Physiol. 1998;274(1):F1-9.

https://doi.org/10.1152/ajprenal.1998.274.1.F1

PMid:9458817

Hou J, Konrad M. Claudins and Renal Magnesium Handling. Curr Top Membr. 2010;65:151-76.

https://doi.org/10.1016/S1063-5823(10)65007-7

Furuse M. Introduction: claudins, tight junctions, and the paracellular barrier. In Current Topics in Membranes. Boston: Elsevier; 2010. p. 1-19.

https://doi.org/10.1016/S1063-5823(10)65001-6

Zhu L, Han J, Li L, Wang Y, Li Y, Zhang S. Claudin family participates in the pathogenesis of inflammatory bowel diseases and colitis-associated colorectal cancer. Front Immunol. 2019;10:1441.

https://doi.org/10.3389/fimmu.2019.01441

PMid:31316506 PMCid:PMC6610251

Wang X, Tully O, Ngo B, Zitin M, Mullin JM. Epithelial tight junctional changes in colorectal cancer tissues. Sci World J. 2011;11:826-41.

https://doi.org/10.1100/tsw.2011.86

PMid:21479352 PMCid:PMC5720014

Martin TA, Mansel RE, Jiang WG. Loss of occludin leads to the progression of human breast cancer. Int J Mol Med. 2010;26(5):723-34.

https://doi.org/10.3892/ijmm_00000519

PMid:20878095

Orbán E, Szabó E, Lotz G, Kupcsulik P, Páska C, Schaff Z, et al. Different expression of occludin and ZO-1 in primary and metastatic liver tumors. Pathol Oncol Res. 2008;14(3):299-306.

https://doi.org/10.1007/s12253-008-9031-2

PMid:18386163

Huo Q, Kinugasa T, Wang L, Huang J, Zhao J, Shibaguchi H, Kuroki M, Tanaka T, Yamashita Y, Nabeshima K, Iwasaki H. Claudin-1 protein is a major factor involved in the tumorigenesis of colorectal cancer. Anticancer Res. 2009;29(3):851-7.

De Oliveira SS, De Oliveira IM, De Souza W, Morgado-Díaz JA. Claudins upregulation in human colorectal cancer. FEBS Lett. 2005;579(27):6179-85.

https://doi.org/10.1016/j.febslet.2005.09.091

PMid:16253248

Mandle HB, Jahan FA, Bostick RM, Baron JA, Barry EL, Yacoub R, et al. Effects of supplemental calcium and vitamin D on tight‐junction proteins and mucin‐12 expression in the normal rectal mucosa of colorectal adenoma patients. Mol Carcinog. 2019;58(7):1279-90.

https://doi.org/10.1002/mc.23010

PMid:30938860 PMCid:PMC6548635

Adiseshaiah PP, Patel NL, Ileva LV, Kalen JD, Haines DC, McNeil SE. Longitudinal imaging of cancer cell metastases in two preclinical models: A correlation of noninvasive imaging to histopathology. Int J Mol Imaging. 2014;2014:102702.

https://doi.org/10.1155/2014/102702

PMid:24724022 PMCid:PMC3958723

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3-new capabilities and interfaces. Nucleic Acids Res. 2012;40(15):e115.

https://doi.org/10.1093/nar/gks596

PMid:22730293 PMCid:PMC3424584

Wong ML, Medrano JF. Real-time PCR for mRNA quantitation. Biotechniques. 2005;39(1):75-85.

https://doi.org/10.2144/05391RV01

PMid:16060372

Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30(9):e36.

https://doi.org/10.1093/nar/30.9.e36

PMid:11972351 PMCid:PMC113859

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001;25(4):402-8.

https://doi.org/10.1006/meth.2001.1262

PMid:11846609

Studio R. RStudio: Integrated development environment for R Version 0.98. 501. Newnes Boston, MA: 2012.

Gonzalez-Mariscal L, Betanzos A, Nava P, Jaramillo BE. Tight junction proteins. Prog Biophys Mol Biol. 2003;81(1):1-44.

https://doi.org/10.1016/S0079-6107(02)00037-8

PMid:12475568

Ganjzadeh F, Shirkoohi R. Association between occludin gene expression and clinical morphological characteristics in breast cancer. Tehran Univ Med J. 2015;73(1):18-23.

Park MW, Kim CH, Cheong JH, Bak KH, Kim JM, Oh SJ. Occludin expression in brain tumors and its relevance to peritumoral edema and survival. Cancer Res Treat. 2006;38(3):139-43.

https://doi.org/10.4143/crt.2006.38.3.139

PMid:19771274 PMCid:PMC2741679

Salehi P, Tafvizi F, Hesari KK. Low Expression of Occludin in the Melanoma Patient. Iran J Pathol. 2019;14(4):272.

https://doi.org/10.30699/IJP.2019.85213.1801

PMid:31754355 PMCid:PMC6824771

Phattarataratip E, Sappayatosok K. Expression of claudin-5, claudin-7 and occludin in oral squamous cell carcinoma and their clinico-pathological significance. J Clin Exp Dent. 2016;8(3):e299.

https://doi.org/10.4317/jced.52801

PMid:27398181 PMCid:PMC4930640

Hoellen F, Waldmann A, Banz Jansen C, Holtrich U, Karn T, Oberländer M, et al. Claudin 1 expression in cervical cancer. Mol Clin Oncol. 2017;7(5):880-4.

https://doi.org/10.3892/mco.2017.1391

PMid:29181184 PMCid:PMC5700277

Ye X, Zhao L, Kang J. Expression and significance of PTEN and Claudin 3 in prostate cancer. Oncol lett. 2019;17(6):5628-34.

https://doi.org/10.3892/ol.2019.10212

PMid:31186785 PMCid:PMC6507465

Ahmad A, Befekadu R, Askari S, Strömberg VH. Decreased Expression of Claudin 1, 3, 4, 5 and 7: A New Prognostic Marker in Colon Carcinoma. J Gastrointest Cancer Stromal Tumors. 2016;1:105.

Niknami Z, Eslamifar A, Emamirazavi A, Ebrahimi A, Shirkoohi R. The association of vimentin and fibronectin gene expression with epithelial-mesenchymal transition and tumor malignancy in colorectal carcinoma. EXCLI J. 2017;16:1009.

Osanai M, Murata M, Nishikiori N, Chiba H, Kojima T, Sawada N. Epigenetic silencing of occludin promotes tumorigenic and metastatic properties of cancer cells via modulations of unique sets of apoptosis-associated genes. Cancer Res. 2006;66(18):9125-33.

https://doi.org/10.1158/0008-5472.CAN-06-1864

PMid:16982755

Holczbauer Á, Gyöngyösi B, Lotz G, Szijártó A, Kupcsulik P, Schaff Z, et al. Distinct claudin expression profiles of hepatocellular carcinoma ad metastatic colorectal and pancreatic carcinomas. J Histochem Cytochem. 2013;61(4):294-305.

https://doi.org/10.1369/0022155413479123

PMid:23385421 PMCid:PMC3636686

Published
2022-12-31
How to Cite
Ghoojaei, M., Shirkoohi, R., Saffari , M., Emamirazavi, A., & Hashemi , M. (2022). Decrement of Transcriptome Level in Epithelial Tight Junction Claudin and Occludin as an Epithelial-Mesenchymal Transition Signature for Colorectal Cancer Biomarker . Galen Medical Journal, 11, e2350. https://doi.org/10.31661/gmj.v11i.2350
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Original Article