دورية أكاديمية

Cholesterol depletion induces mesenchymal properties in oral squamous cell carcinoma cell line.

التفاصيل البيبلوغرافية
العنوان: Cholesterol depletion induces mesenchymal properties in oral squamous cell carcinoma cell line.
المؤلفون: do Nascimento RB; Postgraduate Program in Dentistry and Health, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil., Cerqueira PSG; Postgraduate Program in Dentistry and Health, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil., Silva JC; Postgraduate Program in Dentistry and Health, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil., Fontes EK; Postgraduate Program in Dentistry and Health, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil., Dos Santos EA; Postgraduate Program in Dentistry and Health, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil., Dos Santos JN; Laboratory of Oral and Maxillofacial Pathology, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil., Nunes FD; Department of Oral Pathology, School of Dentistry, University of São Paulo, São Paulo, Brazil., Rodrigues MFSD; Postgraduate Program in Biophotonics Applied to Health Sciences, Nove De Julho University (UNINOVE), São Paulo, São Paulo, Brazil., Paiva KBS; Laboratory of Extracellular Matrix Biology and Cellular Interaction, Department of Anatomy, Institute of Biomedical Sciences, University of São Paulo, São Paulo, São Paulo, Brazil., Xavier FCA; Laboratory of Oral and Maxillofacial Pathology, School of Dentistry, Federal University of Bahia, Salvador, Bahia, Brazil.
المصدر: Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology [J Oral Pathol Med] 2024 Apr; Vol. 53 (4), pp. 246-257. Date of Electronic Publication: 2024 Mar 19.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Wiley-Blackwell Country of Publication: Denmark NLM ID: 8911934 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1600-0714 (Electronic) Linking ISSN: 09042512 NLM ISO Abbreviation: J Oral Pathol Med Subsets: MEDLINE
أسماء مطبوعة: Publication: Oxford, UK : Wiley-Blackwell
Original Publication: Copenhagen : Munksgaard, c1989-
مواضيع طبية MeSH: Carcinoma, Squamous Cell*/pathology , Mouth Neoplasms*/pathology , Head and Neck Neoplasms*, Humans ; Squamous Cell Carcinoma of Head and Neck ; Cell Line, Tumor ; Cell Proliferation ; Cholesterol ; Epithelial-Mesenchymal Transition/genetics ; Cell Movement
مستخلص: Background: Cholesterol in cell membranes is crucial for cell signaling, adhesion, and migration. Membranes feature cholesterol-rich caveolae with caveolin proteins, playing roles in epithelial-mesenchymal transition and cancer progression. Despite elevated cholesterol levels in tumors, its precise function and the effects of its depletion in oral squamous cell carcinoma remain unclear. The aim of this study was to evaluate the influence of cholesterol depletion in oral squamous cell carcinoma cell line and epithelial-mesenchymal transition process.
Methods: Cholesterol depletion was induced on SCC-9 cells by methyl-β-cyclodextrin and cell viability, proliferation, apoptosis, and colony formation capacities were evaluated. Gene and protein expressions were evaluated by reverse transcription polymerase chain reaction (RT-qPCR) and Western Blot, respectively, and cell sublocalization was assessed by immunofluorescence.
Results: Cholesterol depletion resulted in alteration of oral squamous cell carcinoma cell morphology at different concentrations of methyl-β-cyclodextrin, as well as decreased cell proliferation and viability rates. Analysis of CAV1 transcript expression revealed increased gene expression in the treated SCC-9 during the 24 h period, at different concentrations of methyl-β-cyclodextrin: 5 , 7.5, 10, and 15 mM, in relation to parental SCC-9. CAV1 protein expression was increased, with subsequent dose-dependent decrease. A statistically significant difference was observed in samples treated with 5 mM of methyl-β-cyclodextrin (p = 0.02, Kruskal-Wallis test). The immunofluorescence assay showed lower cytoplasmic and membrane labeling intensity in the treated samples for CAV1.
Conclusion: These findings indicate the modulation of cholesterol as a possible mechanism underlying the regulation of these molecules and activation of epithelial-mesenchymal transition in oral squamous cell carcinoma.
(© 2024 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.)
References: Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17‐48. doi:10.3322/caac.21763.
Eljabo N, Nikolic N, Carkic J, et al. Genetic and epigenetic alterations in the tumour, tumour margins, and normal buccal mucosa of patients with oral cancer. Int J Oral Maxillofac Surg. 2018;47(8):976‐982. doi:10.1016/j.ijom.2018.01.020.
Smith A, Teknos TN, Pan Q. Epithelial to mesenchymal transition in head and neck squamous cell carcinoma. Oral Oncol. 2013;49(4):287‐292. doi:10.1016/j.oraloncology.2012.10.009.
De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer. 2013;13(2):97‐110. doi:10.1038/nrc3447.
Aiello NM, Maddipati R, Norgard RJ, et al. EMT subtype influences epithelial plasticity and mode of cell migration. Dev Cell. 2018;45(6):681‐695.e4. doi:10.1016/j.devcel.2018.05.027.
Suarez‐Martinez E, Suazo‐Sanchez I, Celis‐Romero M, Carnero A. 3D and organoid culture in research: physiology, hereditary genetic diseases and cancer. Cell Biosci. 2022;12(1):1‐19. doi:10.1186/s13578‐022‐00775‐w.
Rolim LSA, Mafra RP, de Pontes Santos HB, Souza LB, Pinto LP. Role of twist and podoplanin in partial epithelial–mesenchymal transition in oral squamous cell carcinoma. Braz Dent J. 2020;31(6):623‐633. doi:10.1590/0103‐6440202003542.
Vona R, Iessi E, Matarrese P. Role of cholesterol and lipid rafts in cancer signaling: a promising therapeutic opportunity? Front Cell Dev Biol. 2021;9:9. doi:10.3389/fcell.2021.622908.
Nascimento RB, Risteli M, Paiva KBS, et al. Cholesterol depletion affects caveolin‐1 expression, migration and invasion of oral tongue squamous cell carcinoma cell lines. Arch Oral Biol. 2023;150:105675. doi:10.1016/j.archoralbio.2023.105675.
Lee S, Kwon H, Jeong K, Pak Y. Regulation of cancer cell proliferation by caveolin‐2 down‐regulation and re‐expression. Int J Oncol. 2011;38(5):1395‐1402. doi:10.3892/ijo.2011.958.
Martinez‐Outschoorn UE, Sotgia F, Lisanti MP. Caveolae and signalling in cancer. Nat Rev Cancer. 2015;15(4):225‐237. doi:10.1038/nrc3915.
Auzair LBM, Vincent‐Chong VK, Ghani WMN, et al. Caveolin 1 (Cav‐1) and actin‐related protein 2/3 complex, subunit 1B (ARPC1B) expressions as prognostic indicators for oral squamous cell carcinoma (OSCC). Eur Arch Otorhinolaryngol. 2016;273(7):1885‐1893. doi:10.1007/s00405‐015‐3703‐9.
Nakatani K, Wada T, Nakamura M, Uzawa K, Tanzawa H, Fujita S. Expression of caveolin‐1 and its correlation with cisplatin sensitivity in oral squamous cell carcinoma. J Cancer Res Clin Oncol. 2005;131(7):445‐452. doi:10.1007/s00432‐004‐0662‐8.
Nascimento RB, Paiva KBS, Risteli M, et al. Loss of caveolin‐1 expression in tumor cells is associated with increased aggressiveness and cell invasion in oral squamous cell carcinoma. Head Neck Pathol. 2023;17(3):618‐630. doi:10.1007/s12105‐023‐01562‐w.
Liang W, Hao Z, Han J‐L, Zhu D‐J, Jin Z‐F, Xie W‐L. CAV‐1 contributes to bladder cancer progression by inducing epithelial‐to‐mesenchymal transition. Urol Oncol Semin Orig Investig. 2014;32(6):855‐863. doi:10.1016/j.urolonc.2014.01.005.
Masuelli L, Budillon A, Marzocchella L, et al. Caveolin‐1 overexpression is associated with simultaneous abnormal expression of the E‐cadherin/α‐β catenins complex and multiple ErbB receptors and with lymph nodes metastasis in head and neck squamous cell carcinomas. J Cell Physiol. 2012;227(9):3344‐3353. doi:10.1002/jcp.24034.
Setúbal MF, Rodrigues D, Gammon L, et al. Oncotarget. Effects of cetuximab and erlotinib on the behaviour of cancer stem cells in head and neck squamous cell carcinoma. 2018;9(17):13488‐13500. doi:10.18632/oncotarget.24416.
Sharma A, Bandyopadhayaya S, Chowdhury K, et al. Metformin exhibited anticancer activity by lowering cellular cholesterol content in breast cancer cells. PLoS One. 2019;1(14):1‐17.
Sohn J, Lin H, Fritch MR, Tuan RS. Influence of cholesterol/caveolin‐1/caveolae homeostasis on membrane properties and substrate adhesion characteristics of adult human mesenchymal stem cells. Stem Cell Res Ther. 2018;9(1):86. doi:10.1186/s13287‐018‐0830‐4.
Park E, Park MJ, Lee S, et al. Cholesterol depletion induces anoikis‐like apoptosis via FAK down‐regulation and caveolae internalization. J Pathol. 2009;218(3):337‐349. doi:10.1002/path.2531.
Lawrence MS, Sougnez C, Lichtenstein L, et al. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. 2015;517(7536):576‐582. doi:10.1038/nature14129.
Kakurina GV, Kondakova IV, Spirina LV, et al. Expression of genes encoding cell motility proteins during progression of head and neck squamous cell carcinoma. Bull Exp Biol Med. 2018;166(2):250‐252. doi:10.1007/s10517‐018‐4325‐1.
Li YC, Park MJ, Ye S‐K, Kim C‐W, Kim Y‐N. Elevated levels of cholesterol‐rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol‐depleting agents. Am J Pathol. 2006;168(4):1107‐1118. doi:10.2353/ajpath.2006.050959.
Onodera R, Motoyama K, Okamatsu A, et al. Involvement of cholesterol depletion from lipid rafts in apoptosis induced by methyl‐β‐cyclodextrin. Int J Pharm. 2013;452(1–2):116‐123. doi:10.1016/j.ijpharm.2013.04.071.
Lee SY, Ko S‐H, Shim J‐S, Kim D‐D, Cho H‐J. Tumor targeting and lipid rafts disrupting hyaluronic acid‐cyclodextrin‐based nanoassembled structure for cancer therapy. ACS Appl Mater Interfaces. 2018;10(43):36628‐36640. doi:10.1021/acsami.8b08243.
Yamaguchi R, Perkins G, Hirota K. Targeting cholesterol with β‐cyclodextrin sensitizes cancer cells for apoptosis. FEBS Lett. 2015;589(24 Part B):4097‐4105. doi:10.1016/j.febslet.2015.11.009.
Puram SV, Tirosh I, Parikh AS, et al. Single‐cell transcriptomic analysis of primary and metastatic tumor ecosystems in head and neck cancer. Cell. 2017;171(7):1611‐1624.e24. doi:10.1016/j.cell.2017.10.044.
Qi Z, Barrett T, Parikh AS, Tirosh I, Puram SV. Single‐cell sequencing and its applications in head and neck cancer. Oral Oncol. 2019;99:104441. doi:10.1016/j.oraloncology.2019.104441.
Stemmler MP, Eccles RL, Brabletz S, Brabletz T. Non‐redundant functions of EMT transcription factors. Nat Cell Biol. 2019;21(1):102‐112. doi:10.1038/s41556‐018‐0196‐y.
Hung K‐F, Lin S‐C, Liu C‐J, Chang C‐S, Chang K‐W, Kao S‐Y. The biphasic differential expression of the cellular membrane protein, caveolin‐1, in oral carcinogenesis. J Oral Pathol Med. 2003;32(8):461‐467. doi:10.1034/j.1600‐0714.2003.00185.x.
معلومات مُعتمدة: 017/2013 Fundação de Amparo à Pesquisa do Estado da Bahia; MCTI/CNPq-14/2014 Conselho Nacional de Desenvolvimento Científico e Tecnológico
فهرسة مساهمة: Keywords: caveolin; cell adhesion; cholesterol depletion; epithelial–mesenchymal transition; oral squamous cell carcinoma
المشرفين على المادة: 97C5T2UQ7J (Cholesterol)
تواريخ الأحداث: Date Created: 20240320 Date Completed: 20240418 Latest Revision: 20240418
رمز التحديث: 20240418
DOI: 10.1111/jop.13524
PMID: 38503722
قاعدة البيانات: MEDLINE
الوصف
تدمد:1600-0714
DOI:10.1111/jop.13524