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
July-2021 Volume 22 Issue 1

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
July-2021 Volume 22 Issue 1

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
Article Open Access

SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients

  • Authors:
    • Erik Lizárraga-Verdugo
    • Tatiana Galicia Carmona
    • Rosalío Ramos-Payan
    • Mariana Avendaño-Félix
    • Mercedes Bermúdez
    • Maryelv Parra-Niebla
    • César López-Camarillo
    • Edith Fernandez-Figueroa
    • Leonardo Lino-Silva
    • Herminia Arvelo Saavedra
    • Itzel Vela-Sarmiento
    • Roberto Cárdenas Ovando
    • Erika Ruíz-García
    • Maribel Aguilar-Medina
  • View Affiliations / Copyright

    Affiliations: Faculty of Chemical and Biological Sciences, Autonomous University of Sinaloa, 80010 Culiacán, Sinaloa, Mexico, Department of Translational Medicine, National Cancer Institute, 14080 Mexico City, Mexico, Oncogenomics Laboratory, Autonomous University of Mexico City, 06720 Mexico City, Mexico, Department of Computational Genomics Laboratories, National Cancer Institute, 14080 Mexico City, Mexico, Department of Pathology, National Cancer Institute, 14080 Mexico City, Mexico, Department of Gastrointestinal Tumors, National Cancer Institute, 14080 Mexico City, Mexico, School of Engineering and Sciences, Monterrreys' Technologic, 14380 Mexico City, Mexico
    Copyright: © Lizárraga-Verdugo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 497
    |
    Published online on: April 27, 2021
       https://doi.org/10.3892/ol.2021.12758
  • 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

Colorectal cancer (CRC) is one of the most common malignancies worldwide and includes colon cancer (CC) and rectal cancer (RC). Regarding CC, the development of novel molecular biomarkers for the accurate diagnosis and prognosis, as well as the identification of novel targets for therapeutic intervention, are urgently needed. SRY‑related high‑mobility group box 9 (SOX9), a transcription factor, is involved in development, and has been associated with the progression of human cancer. However, its underlying clinical and functional effects in CRC have not been fully understood. Therefore, the present study aimed to evaluate the clinical and functional relevance of SOX9 expression in CC. The expression of SOX9 in tumor tissues was evaluated in 97 biopsies from Mexican patients with CC with early‑stage I and II disease by immunohistochemistry (IHC). In addition, SOX9 silencing in the HCT116 cell line was performed using specific small interfering RNAs, while downregulation efficiency was verified by reverse transcription‑quantitative PCR and immunofluorescence. Spheroid‑formation assay was carried out using ultra‑low attachment plates. The IHC results showed that SOX9 was upregulated in patients with stage II (91%) and advanced T3 stage (67%) CC. Interestingly, higher SOX9 expression was associated with clinical stage, tumor size and tumor location. Furthermore, increased SOX9 expression was found in relapsed cases with local tumors; however, it was not associated with increased survival probability. Additionally, functional analysis indicated that SOX9 silencing significantly attenuated the sphere‑formation capability of HCT116 cells. The present study was the first to evaluate the expression levels of SOX9 in Mexican patients diagnosed with early‑stage CC. The aforementioned findings indicated that high SOX9 expression could play an important role in tumorigenesis and be associated with advanced T‑stages of clinical‑stage II patients, but not with relapse‑free survival.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Figure 7

View References

1 

Rawla P, Sunkara T and Barsouk A: Epidemiology of colorectal cancer: Incidence, mortality, survival, and risk factors. Prz Gastroenterol. 14:89–103. 2019.PubMed/NCBI

2 

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI

3 

Hawkes N: Cancer survival data emphasise importance of early diagnosis. BMJ. 364:l4082019. View Article : Google Scholar : PubMed/NCBI

4 

Rojas-Puente L, de la Garza-Salazar JG, Calderillo-Ruiz G, Lino-Silva LS, Millan SV, Noveron NR, Meneses-Garcia A, de la Vega HA and Ruiz Garcia EB: Increased incidence of colorectal cancer in young people (less than 40 years old) over the last ten years. J Cancerology. 1:16–22. 2014.

5 

Ahnen DJ, Wade SW, Jones WF, Sifri R, Mendoza Silveiras J, Greenamyer J, Guiffre S, Axilbund J, Spiegel A and You YN: The increasing incidence of young-onset colorectal cancer: A call to action. Mayo Clin Proc. 89:216–224. 2014. View Article : Google Scholar : PubMed/NCBI

6 

Mishra DK, Veena U, Kaliki S, Kethiri AR, Sangwan VS, Ali MH, Naik MN and Singh V: Differential expression of stem cell markers in ocular surface squamous neoplasia. PLoS One. 11:e01618002016. View Article : Google Scholar : PubMed/NCBI

7 

Brenner H, Kloor M and Pox CP: Colorectal cancer. Lancet. 383:1490–1502. 2014. View Article : Google Scholar : PubMed/NCBI

8 

Li W, Zhang G, Wang HL and Wang L: Analysis of expression of cyclin E, p27kip1 and Ki67 protein in colorectal cancer tissues and its value for diagnosis, treatment and prognosis of disease. Eur Rev Med Pharmacol Sci. 20:4874–4879. 2016.PubMed/NCBI

9 

Krausova M and Korinek V: Wnt signaling in adult intestinal stem cells and cancer. Cell Signal. 26:570–579. 2014. View Article : Google Scholar : PubMed/NCBI

10 

Gassler N: Paneth cells in intestinal physiology and pathophysiology. World J Gastrointest Pathophysiol. 8:150–160. 2017. View Article : Google Scholar : PubMed/NCBI

11 

Sailaja BS, He XC and Li L: The regulatory niche of intestinal stem cells. J Physiol. 594:4827–4836. 2016. View Article : Google Scholar : PubMed/NCBI

12 

Jo A, Denduluri S, Zhang B, Wang Z, Yin L, Yan Z, Kang R, Shi LL, Mok J, Lee MJ, et al: The versatile functions of Sox9 in development, stem cells, and human diseases. Genes Dis. 1:149–161. 2014. View Article : Google Scholar : PubMed/NCBI

13 

Bastide P, Darido C, Pannequin J, Kist R, Robine S, Marty-Double C, Bibeau F, Scherer G, Joubert D, Hollande F, et al: Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J Cell Biol. 178:635–648. 2007. View Article : Google Scholar : PubMed/NCBI

14 

Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B and Kinzler KW: Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science. 275:1787–1790. 1997. View Article : Google Scholar : PubMed/NCBI

15 

Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B and Clevers H: Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 275:1784–1787. 1997. View Article : Google Scholar : PubMed/NCBI

16 

Javier BM, Yaeger R, Wang L, Sanchez-Vega F, Zehir A, Middha S, Sadowska J, Vakiani E, Shia J, Klimstra D, et al: Recurrent, truncating SOX9 mutations are associated with SOX9 overexpression, KRAS mutation, and TP53 wild type status in colorectal carcinoma. Oncotarget. 7:50875–50882. 2016. View Article : Google Scholar : PubMed/NCBI

17 

Aguilar-Medina M, Avendaño-Félix M, Lizárraga-Verdugo E, Bermúdez M, Romero-Quintana JG, Ramos-Payan R, Ruíz-García E and López-Camarillo C: SOX9 stem-cell factor: Clinical and functional relevance in cancer. J Oncol. 2019:67540402019. View Article : Google Scholar : PubMed/NCBI

18 

Blache P, van de Wetering M, Duluc I, Domon C, Berta P, Freund JN, Clevers H and Jay P: SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol. 166:37–47. 2004. View Article : Google Scholar : PubMed/NCBI

19 

Lü B, Fang Y, Xu J, Wang L, Xu F, Xu E, Huang Q and Lai M: Analysis of SOX9 expression in colorectal cancer. Am J Clin Pathol. 130:897–904. 2008. View Article : Google Scholar

20 

Shen Z, Deng H, Fang Y, Zhu X, Ye GT, Yan L, Liu H and Li G: Identification of the interplay between SOX9 and S100P in the metastasis and invasion of colon carcinoma. Oncotarget. 6:20672–20684. 2015. View Article : Google Scholar : PubMed/NCBI

21 

Choi BJ, Park SA, Lee SY, Cha YN and Surh YJ: Hypoxia induces epithelial-mesenchymal transition in colorectal cancer cells through ubiquitin-specific protease 47-mediated stabilization of Snail: A potential role of Sox9. Sci Rep. 7:159182017. View Article : Google Scholar : PubMed/NCBI

22 

Zhang S, Che D, Yang F, Chi C, Meng H, Shen J, Qi L, Liu F, Lv L, Li Y, et al: Tumor-associated macrophages promote tumor metastasis via the TGF-β/SOX9 axis in non-small cell lung cancer. Oncotarget. 8:99801–99815. 2017. View Article : Google Scholar : PubMed/NCBI

23 

Carrasco-Garcia E, Lopez L, Aldaz P, Arevalo S, Aldaregia J, Egaña L, Bujanda L, Cheung M, Sampron N, Garcia I, et al: SOX9-regulated cell plasticity in colorectal metastasis is attenuated by rapamycin. Sci Rep. 6:323502016. View Article : Google Scholar : PubMed/NCBI

24 

Matheu A, Collado M, Wise C, Manterola L, Cekaite L, Tye AJ, Canamero M, Bujanda L, Schedl A, Cheah KS, et al: Oncogenicity of the developmental transcription factor Sox9. Cancer Res. 72:1301–1315. 2012. View Article : Google Scholar : PubMed/NCBI

25 

Jay P, Berta P and Blache P: Expression of the carcinoembryonic antigen gene is inhibited by SOX9 in human colon carcinoma cells. Cancer Res. 65:2193–2198. 2005. View Article : Google Scholar : PubMed/NCBI

26 

Zalzali H, Naudin C, Bastide P, Quittau-Prévostel C, Yaghi C, Poulat F, Jay P and Blache P: CEACAM1, a SOX9 direct transcriptional target identified in the colon epithelium. Oncogene. 27:7131–7138. 2008. View Article : Google Scholar : PubMed/NCBI

27 

Marcker Espersen ML, Linnemann D, Christensen IJ, Alamili M, Troelsen JT and Høgdall E: SOX9 expression predicts relapse of stage II colon cancer patients. Hum Pathol. 52:38–46. 2016. View Article : Google Scholar : PubMed/NCBI

28 

Lai CC, You JF, Yeh CY, Chen JS, Tang R, Wang JY and Chin CC: Low preoperative serum albumin in colon cancer: A risk factor for poor outcome. Int J Colorectal Dis. 26:473–481. 2011. View Article : Google Scholar : PubMed/NCBI

29 

Boonpipattanapong T and Chewatanakornkul S: Preoperative carcinoembryonic antigen and albumin in predicting survival in patients with colon and rectal carcinomas. J Clin Gastroenterol. 40:592–595. 2006. View Article : Google Scholar : PubMed/NCBI

30 

Dimitriou N, Arandjelović O, Harrison DJ and Caie PD: A principled machine learning framework improves accuracy of stage II colorectal cancer prognosis. NPJ Digit Med. 1:522018. View Article : Google Scholar : PubMed/NCBI

31 

Vera R, Aparicio J, Carballo F, Esteva M, González-Flores E, Santianes J, Santolaya F and Fernández-Cebrián JM: Recommendations for follow-up of colorectal cancer survivors. Clin Transl Oncol. 21:1302–1311. 2019. View Article : Google Scholar : PubMed/NCBI

32 

van Diest PJ, van Dam P, Henzen-Logmans SC, Berns E, van der Burg ME, Green J and Vergote I; European Organization for Research and Treatment of Cancer-Gynaecological Cancer Cooperative Group, : A scoring system for immunohistochemical staining: Consensus report of the task force for basic research of the EORTC-GCCG. J Clin Pathol. 50:801–804. 1997. View Article : Google Scholar : PubMed/NCBI

33 

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

34 

Lizárraga-Verdugo E, Ruiz-García E, López-Camarillo C, Bermúdez M, Avendaño-Félix M, Ramos-Payán R, Romero-Quintana G, Ayala-Ham A, Villegas-Mercado C, Pérez-Plasencia C, et al: Cell curvival is regulated via SOX9/BCL2L1 axis in HCT-116 colorectal cancer cell line. J Oncol. 2020:57015272020. View Article : Google Scholar

35 

Wang L, He S, Yuan J, Mao X, Cao Y, Zong J, Tu Y and Zhang Y: Oncogenic role of SOX9 expression in human malignant glioma. Med Oncol. 29:3484–3490. 2012. View Article : Google Scholar : PubMed/NCBI

36 

Mauri G, Sartore-Bianchi A, Russo AG, Marsoni S, Bardelli A and Siena S: Early-onset colorectal cancer in young individuals. Mol Oncol. 13:109–131. 2019. View Article : Google Scholar : PubMed/NCBI

37 

Xicola RM, Manojlovic Z, Augustus GJ, Kupfer SS, Emmadi R, Alagiozian-Angelova V, Triche T Jr, Salhia B, Carpten J, Llor X, et al: Lack of APC somatic mutation is associated with early-onset colorectal cancer in African Americans. Carcinogenesis. 39:1331–1341. 2018. View Article : Google Scholar : PubMed/NCBI

38 

Wan YP, Xi M, He HC, Wan S, Hua W, Zen ZC, Liu YL, Zhou YL, Mo RJ, Zhuo YJ, et al: Expression and clinical significance of SOX9 in renal cell carcinoma, bladder cancer and penile cancer. Oncol Res Treat. 40:15–20. 2017. View Article : Google Scholar : PubMed/NCBI

39 

Mesquita P, Freire AF, Lopes N, Gomes R, Azevedo D, Barros R, Pereira B, Cavadas B, Pópulo H, Boaventura P, et al: Expression and clinical relevance of SOX9 in gastric cancer. Dis Markers. 2019:82670212019. View Article : Google Scholar : PubMed/NCBI

40 

Prévostel C and Blache P: The dose-dependent effect of SOX9 and its incidence in colorectal cancer. Eur J Cancer. 86:150–157. 2017. View Article : Google Scholar

41 

Lytle NK, Barber AG and Reya T: Stem cell fate in cancer growth, progression and therapy resistance. Nat Rev Cancer. 18:669–680. 2018. View Article : Google Scholar : PubMed/NCBI

42 

Beck B and Blanpain C: Unravelling cancer stem cell potential. Nat Rev Cancer. 13:727–738. 2013. View Article : Google Scholar : PubMed/NCBI

43 

Kuşoğlu A and Biray Avcı Ç: Cancer stem cells: A brief review of the current status. Gene. 681:80–85. 2019. View Article : Google Scholar

44 

Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, Meltzer SJ, Rodriguez-Bigas MA, Fodde R, Ranzani GN, et al: A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: Development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res. 58:5248–5257. 1998.PubMed/NCBI

45 

Boland CR and Goel A: Microsatellite instability in colorectal cancer. Gastroenterology. 138:2073–2087.e3. 2010. View Article : Google Scholar : PubMed/NCBI

46 

Santos JC, Carrasco-Garcia E, Garcia-Puga M, Aldaz P, Montes M, Fernandez-Reyes M, de Oliveira CC, Lawrie CH, Araúzo-Bravo MJ, Ribeiro ML, et al: SOX9 Elevation Acts with Canonical WNT Signaling to Drive Gastric Cancer Progression. Cancer Res. 76:6735–6746. 2016. View Article : Google Scholar : PubMed/NCBI

47 

Wang J, Xue X, Hong H, Qin M, Zhou J, Sun Q, Liang H and Gao L: Upregulation of microRNA-524-5p enhances the cisplatin sensitivity of gastric cancer cells by modulating proliferation and metastasis via targeting SOX9. Oncotarget. 8:574–582. 2017. View Article : Google Scholar : PubMed/NCBI

48 

Higashihara T, Yoshitomi H, Nakata Y, Kagawa S, Takano S, Shimizu H, Kato A, Furukawa K, Ohtsuka M and Miyazaki M: Sex determining region Y box 9 induces chemoresistance in pancreatic cancer cells by induction of putative cancer stem cell characteristics and its high expression predicts poor prognosis. Pancreas. 46:1296–1304. 2017. View Article : Google Scholar : PubMed/NCBI

49 

Aguilar-Medina M, Avendaño-Félix M, Lizárraga-Verdugo E, Bermúdez M, Romero-Quintana JG, Ramos-Payan R, Ruíz-García E and López-Camarillo C: SOX9 stem-cell factor: Clinical and functional relevance in cancer. J Oncol. 2019:67540402019. View Article : Google Scholar : PubMed/NCBI

50 

Liu C, Liu L, Chen X, Cheng J, Zhang H, Shen J, Shan J, Xu Y, Yang Z, Lai M, et al: Sox9 regulates self-renewal and tumorigenicity by promoting symmetrical cell division of cancer stem cells in hepatocellular carcinoma. Hepatology. 64:117–129. 2016. View Article : Google Scholar : PubMed/NCBI

51 

Network TCGA; Cancer Genome Atlas Network, : Comprehensive molecular characterization of human colon and rectal cancer. Nature. 487:330–337. 2012. View Article : Google Scholar : PubMed/NCBI

52 

Bahmad HF, Cheaito K, Chalhoub RM, Hadadeh O, Monzer A, Ballout F, El-Hajj A, Mukherji D, Liu YN, Daoud G, et al: Sphere-formation assay: Three-dimensional in vitro culturing of prostate cancer stem/progenitor sphere-forming cells. Front Oncol. 8:3472018. View Article : Google Scholar : PubMed/NCBI

53 

Shaheen S, Ahmed M, Lorenzi F and Nateri AS: Spheroid-Formation (Colonosphere) Assay for in vitro assessment and expansion of stem cells in colon cancer. Stem Cell Rev Rep. 12:492–499. 2016. View Article : Google Scholar : PubMed/NCBI

54 

Terasaki M, Matsumoto N, Hashimoto R, Endo T, Maeda H, Hamada J, Osada K, Miyashita K and Mutoh M: Fucoxanthin administration delays occurrence of tumors in xenograft mice by colonospheres, with an anti-tumor predictor of glycine. J Clin Biochem Nutr. 64:52–58. 2019. View Article : Google Scholar : PubMed/NCBI

55 

Rennebeck G, Martelli M and Kyprianou N: Anoikis and survival connections in the tumor microenvironment: Is there a role in prostate cancer metastasis? Cancer Res. 65:11230–11235. 2005. View Article : Google Scholar : PubMed/NCBI

56 

Stratton MR: Exploring the genomes of cancer cells: Progress and promise. Science. 331:1553–1558. 2011. View Article : Google Scholar : PubMed/NCBI

57 

Jinesh GG, Choi W, Shah JB, Lee EK, Willis DL and Kamat AM: Blebbishields, the emergency program for cancer stem cells: Sphere formation and tumorigenesis after apoptosis. Cell Death Differ. 20:382–395. 2013. View Article : Google Scholar : PubMed/NCBI

58 

Larsimont J-C, Youssef KK, Sánchez-Danés A, Sukumaran V, Defrance M, Delatte B, Liagre M, Baatsen P, Marine JC, Lippens S, et al: Sox9 controls self-renewal of oncogene targeted cells and links tumor initiation and invasion. Cell Stem Cell. 17:60–73. 2015. View Article : Google Scholar : PubMed/NCBI

59 

Prévostel C, Rammah-Bouazza C, Trauchessec H, Canterel-Thouennon L, Busson M, Ychou M and Blache P: SOX9 is an atypical intestinal tumor suppressor controlling the oncogenic Wnt/β-catenin signaling. Oncotarget. 7:82228–82243. 2016. View Article : Google Scholar

60 

Ma XL, Hu B, Tang WG, Xie S-H, Ren N, Guo L and Lu RQ: CD73 sustained cancer-stem-cell traits by promoting SOX9 expression and stability in hepatocellular carcinoma. J Hematol Oncol. 13:112020. View Article : Google Scholar : PubMed/NCBI

61 

Richtig G, Aigelsreiter A, Schwarzenbacher D, Ress AL, Adiprasito JB, Stiegelbauer V, Hoefler G, Schauer S, Kiesslich T, Kornprat P, et al: SOX9 is a proliferation and stem cell factor in hepatocellular carcinoma and possess widespread prognostic significance in different cancer types. PLoS One. 12:e01878142017. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Lizárraga-Verdugo E, Carmona TG, Ramos-Payan R, Avendaño-Félix M, Bermúdez M, Parra-Niebla M, López-Camarillo C, Fernandez-Figueroa E, Lino-Silva L, Saavedra HA, Saavedra HA, et al: SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients. Oncol Lett 22: 497, 2021.
APA
Lizárraga-Verdugo, E., Carmona, T.G., Ramos-Payan, R., Avendaño-Félix, M., Bermúdez, M., Parra-Niebla, M. ... Aguilar-Medina, M. (2021). SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients. Oncology Letters, 22, 497. https://doi.org/10.3892/ol.2021.12758
MLA
Lizárraga-Verdugo, E., Carmona, T. G., Ramos-Payan, R., Avendaño-Félix, M., Bermúdez, M., Parra-Niebla, M., López-Camarillo, C., Fernandez-Figueroa, E., Lino-Silva, L., Saavedra, H. A., Vela-Sarmiento, I., Ovando, R. C., Ruíz-García, E., Aguilar-Medina, M."SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients". Oncology Letters 22.1 (2021): 497.
Chicago
Lizárraga-Verdugo, E., Carmona, T. G., Ramos-Payan, R., Avendaño-Félix, M., Bermúdez, M., Parra-Niebla, M., López-Camarillo, C., Fernandez-Figueroa, E., Lino-Silva, L., Saavedra, H. A., Vela-Sarmiento, I., Ovando, R. C., Ruíz-García, E., Aguilar-Medina, M."SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients". Oncology Letters 22, no. 1 (2021): 497. https://doi.org/10.3892/ol.2021.12758
Copy and paste a formatted citation
x
Spandidos Publications style
Lizárraga-Verdugo E, Carmona TG, Ramos-Payan R, Avendaño-Félix M, Bermúdez M, Parra-Niebla M, López-Camarillo C, Fernandez-Figueroa E, Lino-Silva L, Saavedra HA, Saavedra HA, et al: SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients. Oncol Lett 22: 497, 2021.
APA
Lizárraga-Verdugo, E., Carmona, T.G., Ramos-Payan, R., Avendaño-Félix, M., Bermúdez, M., Parra-Niebla, M. ... Aguilar-Medina, M. (2021). SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients. Oncology Letters, 22, 497. https://doi.org/10.3892/ol.2021.12758
MLA
Lizárraga-Verdugo, E., Carmona, T. G., Ramos-Payan, R., Avendaño-Félix, M., Bermúdez, M., Parra-Niebla, M., López-Camarillo, C., Fernandez-Figueroa, E., Lino-Silva, L., Saavedra, H. A., Vela-Sarmiento, I., Ovando, R. C., Ruíz-García, E., Aguilar-Medina, M."SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients". Oncology Letters 22.1 (2021): 497.
Chicago
Lizárraga-Verdugo, E., Carmona, T. G., Ramos-Payan, R., Avendaño-Félix, M., Bermúdez, M., Parra-Niebla, M., López-Camarillo, C., Fernandez-Figueroa, E., Lino-Silva, L., Saavedra, H. A., Vela-Sarmiento, I., Ovando, R. C., Ruíz-García, E., Aguilar-Medina, M."SOX9 is associated with advanced T-stages of clinical stage II colon cancer in young Mexican patients". Oncology Letters 22, no. 1 (2021): 497. https://doi.org/10.3892/ol.2021.12758
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