Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Cancer Cell International
Published in: Cancer Cell International 1/2020

Open Access 01-12-2020 | Oral Cancer | Review

Cancer stem cells and oral cancer: insights into molecular mechanisms and therapeutic approaches

Authors: Ghazaleh Baniebrahimi, Fatemeh Mir, Razieh Khanmohammadi

Published in: Cancer Cell International | Issue 1/2020

Login to get access

Abstract

Cancer stem cells (CSCs) have been identified as a little population of cancer cells, which have features as the same as the cells normal stem cells. There is enough knowledge of the CSCs responsibility for metastasis, medicine resistance, and cancer outbreak. Therefore, CSCs control possibly provides an efficient treatment intervention inhibiting tumor growth and invasion. In spite of the significance of targeting CSCs in treating cancer, few study comprehensively explored the nature of oral CSCs. It has been showed that oral CSCs are able to contribute to oral cancer progression though activation/inhibition a sequences of cellular and molecular pathways (microRNA network, histone modifications and calcium regulation). Hence, more understanding about the properties of oral cancers and their behaviors will help us to develop new therapeutic platforms. Head and neck CSCs remain a viable and intriguing option for targeted therapy. Multiple investigations suggested the major contribution of the CSCs to the metastasis, tumorigenesis, and resistance to the new therapeutic regimes. Therefore, experts in the field are examining the encouraging targeted therapeutic choices. In spite of the advancements, there are not enough information in this area and thus a magic bullet for targeting and eliminating the CSCs deviated us. Hence, additional investigations on the combined therapies against the head and neck CSCs could offer considerable achievements. The present research is a review of the recent information on oral CSCs, and focused on current advancements in new signaling pathways contributed to their stemness regulation. Moreover, we highlighted various therapeutic approaches against oral CSCs.
Literature
1.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRefPubMed
2.
Siegel RL, Miller KD. Cancer statistics. CA Cancer J Clin. 2020;2020(70):7–30.CrossRef
3.
Gatta G, Botta L, Sanchez MJ, Anderson LA, Pierannunzio D, Licitra L. Prognoses and improvement for head and neck cancers diagnosed in Europe in early 2000s: The EUROCARE-5 population-based study. Eur J Cancer. 2015;51:2130–43.PubMedCrossRef
4.
Beynon RA, Lang S, Schimansky S, Penfold CM, Waylen A, Thomas SJ, Pawlita M, Waterboer T, Martin RM, May M, Ness AR. Tobacco smoking and alcohol drinking at diagnosis of head and neck cancer and all-cause mortality: results from head and neck 5000, a prospective observational cohort of people with head and neck cancer. Int J Cancer. 2018;143:1114–27.PubMedPubMedCentralCrossRef
5.
Marziliano A, Teckie S, Diefenbach MA. Alcohol-related head and neck cancer: summary of the literature. Head Neck. 2019.
6.
Paver EC, Currie AM, Gupta R, Dahlstrom JE. Human papilloma virus related squamous cell carcinomas of the head and neck: diagnosis, clinical implications and detection of HPV. Pathology. 2020;52:179–91.PubMedCrossRef
7.
Ramesh PS, Devegowda D, Singh A, Thimmulappa RK. NRF2, p53, and p16: predictive biomarkers to stratify human papillomavirus associated head and neck cancer patients for de-escalation of cancer therapy. Crit Rev Oncol Hematol. 2020;148:102885.PubMedCrossRef
8.
Berglund BA, Boring DL, Howlett AC. Investigation of structural analogs of prostaglandin amides for binding to and activation of CB1 and CB2 cannabinoid receptors in rat brain and human tonsils. Adv Exp Med Biol. 1999;469:527–33.PubMedCrossRef
9.
Zhu LX, Sharma S, Stolina M, Gardner B, Roth MD, Tashkin DP, Dubinett SM. Delta-9-tetrahydrocannabinol inhibits antitumor immunity by a CB2 receptor-mediated, cytokine-dependent pathway. J Immunol. 2000;165:373–80.PubMedCrossRef
10.
McKallip RJ, Nagarkatti M, Nagarkatti PS. Delta-9-tetrahydrocannabinol enhances breast cancer growth and metastasis by suppression of the antitumor immune response. J Immunol. 2005;174:3281–9.PubMedCrossRef
11.
Gillison ML, D’Souza G, Westra W, Sugar E, Xiao W, Begum S, Viscidi R. Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16-negative head and neck cancers. J Natl Cancer Inst. 2008;100:407–20.PubMedCrossRef
12.
Warnakulasuriya S, Reibel J, Bouquot J, Dabelsteen E. Oral epithelial dysplasia classification systems: predictive value, utility, weaknesses and scope for improvement. J Oral Pathol Med. 2008;37:127–33.PubMedCrossRef
13.
Brennan M, Migliorati CA, Lockhart PB, Wray D, Al-Hashimi I, Axéll T, Bruce AJ, Carpenter W, Eisenberg E, Epstein JB. Management of oral epithelial dysplasia: a review. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 2007;103:S19e11–2.
14.
Mohammadi M, Jaafari MR, Mirzaei HR, Mirzaei H. Mesenchymal stem cell: a new horizon in cancer gene therapy. Cancer Gene Ther. 2016;23:285–6.PubMedCrossRef
15.
Mirzaei H, Sahebkar A, Sichani LS, Moridikia A, Nazari S, Sadri Nahand J, Salehi H, Stenvang J, Masoudifar A, Mirzaei HR, Jaafari MR. Therapeutic application of multipotent stem cells. J Cell Physiol. 2018;233:2815–23.PubMedCrossRef
16.
Mirzaei H, Sahebkar A, Avan A, Jaafari MR, Salehi R, Salehi H, Baharvand H, Rezaei A, Hadjati J, Pawelek JM, Mirzaei HR. Application of mesenchymal stem cells in melanoma: a potential therapeutic strategy for delivery of targeted agents. Curr Med Chem. 2016;23:455–63.PubMedCrossRef
17.
Mirzaei HR, Sahebkar A, Salehi R, Nahand JS, Karimi E, Jaafari MR, Mirzaei H. Boron neutron capture therapy: moving toward targeted cancer therapy. J Cancer Res Ther. 2016;12:520–5.PubMedCrossRef
18.
Hashemi Goradel N, Ghiyami-Hour F, Jahangiri S, Negahdari B, Sahebkar A, Masoudifar A, Mirzaei H. Nanoparticles as new tools for inhibition of cancer angiogenesis. 2018;233:2902–10.
19.
Stoopler ET, Sollecito TP. Oral Cancer. Dent Clin North Am. 2018;62:9–10.CrossRef
20.
Mirzaei H, Sahebkar A, Jaafari MR, Hadjati J, Javanmard SH, Mirzaei HR, Salehi R. PiggyBac as a novel vector in cancer gene therapy: current perspective. Cancer Gene Ther. 2016;23:45–7.PubMedCrossRef
21.
Hesari A, Azizian M, Sheikhi A, Nesaei A, Sanaei S, Mahinparvar N, Derakhshani M, Hedayt P, Ghasemi F, Mirzaei H. Chemopreventive and therapeutic potential of curcumin in esophageal cancer: current and future status. 2019;144:1215–26.
22.
Keshavarzi M, Darijani M. Molecular imaging and oral cancer diagnosis and therapy. J Cell Biochem. 2017;118:3055–60.PubMedCrossRef
23.
Marcial VA, Pajak TF, Mohiuddin M, Cooper JS, Al Sarraf M, Mowry PA, Curran W, Crissman J, Rodríguez M, Vélez-Garca E. Concomitant cisplatin chemotherapy and radiotherapy in advanced mucosal squamous cell carcinoma of the head and neck. Long-term results of the Radiation Therapy Oncology Group study 81–17. Cancer. 1990;66:1861–8.PubMedCrossRef
24.
25.
Nassar D, Blanpain C. Cancer stem cells: basic concepts and therapeutic implications. Annu Rev Pathol. 2016;11:47–76.PubMedCrossRef
26.
Chiou S-H, Yu C-C, Huang C-Y, Lin S-C, Liu C-J, Tsai T-H, Chou S-H, Chien C-S, Ku H-H, Lo J-F. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res. 2008;14:4085–95.PubMedCrossRef
27.
Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.PubMedPubMedCentralCrossRef
28.
Grimm M, Krimmel M, Polligkeit J, Alexander D, Munz A, Kluba S, Keutel C, Hoffmann J, Reinert S, Hoefert S. ABCB5 expression and cancer stem cell hypothesis in oral squamous cell carcinoma. Eur J Cancer. 2012;48:3186–97.PubMedCrossRef
29.
Hayashi S, Tanaka J, Okada S, Isobe T, Yamamoto G, Yasuhara R, Irie T, Akiyama C, Kohno Y, Tachikawa T. Lin28a is a putative factor in regulating cancer stem cell-like properties in side population cells of oral squamous cell carcinoma. Exp Cell Res. 2013;319:1220–8.PubMedCrossRef
30.
Richard V, Sebastian P, Nair MG, Nair SN, Malieckal TT, Kumar TS, Pillai MR. Multiple drug resistant, tumorigenic stem-like cells in oral cancer. Cancer Lett. 2013;338:300–16.PubMedCrossRef
31.
Zhang Q, Shi S, Yen Y, Brown J, Ta JQ, Le AD. A subpopulation of CD133+ cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to chemotherapy. Cancer Lett. 2010;289:151–60.PubMedCrossRef
32.
Felthaus O, Ettl T, Gosau M, Driemel O, Brockhoff G, Reck A, Zeitler K, Hautmann M, Reichert T, Schmalz G. Cancer stem cell-like cells from a single cell of oral squamous carcinoma cell lines. Biochem Biophys Res Commun. 2011;407:28–33.PubMedCrossRef
33.
Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730.CrossRefPubMed
34.
Prince M, Sivanandan R, Kaczorowski A, Wolf G, Kaplan M, Dalerba P, Weissman I, Clarke M, Ailles L. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci. 2007;104:973–8.PubMedCrossRefPubMedCentral
35.
Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–8.PubMed
36.
Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly J, Chandra D, Zhou J, Claypool K. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene. 2006;25:1696.PubMedCrossRef
37.
Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.PubMedCrossRef
38.
Mackenzie IC. Growth of malignant oral epithelial stem cells after seeding into organotypical cultures of normal mucosa. J Oral Pathol Med. 2004;33:71–8.PubMedCrossRef
39.
Todoroki K, Ogasawara S, Akiba J, Nakayama M, Naito Y, Seki N, Kusukawa J, Yano H. CD44v3+/CD24-cells possess cancer stem cell-like properties in human oral squamous cell carcinoma. Int J Oncol. 2016;48:99–109.PubMedCrossRef
40.
Ghuwalewala S, Ghatak D, Das P, Dey S, Sarkar S, Alam N, Panda CK, Roychoudhury S. CD44highCD24low molecular signature determines the cancer stem cell and EMT phenotype in oral squamous cell carcinoma. Stem Cell Res. 2016;16:405–17.PubMedCrossRef
41.
Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell. 2011;8:486–98.PubMedPubMedCentralCrossRef
42.
Shrivastava S, Steele R, Sowadski M, Crawford SE, Varvares M, Ray RB. Identification of molecular signature of head and neck cancer stem-like cells. Sci Rep. 2015;5:7819.PubMedPubMedCentralCrossRef
43.
Zhang Z, Sant’Ana Filho M, Nör JE. The biology of head and neck cancer stem cells. Oral Oncol. 2012;48:1–9.PubMedCrossRef
44.
45.
46.
Yan Y, Zuo X, Wei D. Concise review: emerging role of CD44 in cancer stem cells: a promising biomarker and therapeutic target. Stem Cells Transl Med. 2015;4:1033–43.PubMedPubMedCentralCrossRef
47.
Wang L, Zuo X, Xie K, Wei D. The role of CD44 and cancer stem cells. cancer stem cells. Berlin: Springer; 2018. p. 31–42.CrossRef
48.
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci. 2003;100:3983–8.PubMedCrossRefPubMedCentral
49.
50.
Ota N, Ohno J, Seno K, Taniguchi K, Ozeki S. In vitro and in vivo expression of aldehyde dehydrogenase 1 in oral squamous cell carcinoma. Int J Oncol. 2014;44:435–42.PubMedCrossRef
51.
Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, Wolf GT, Wicha MS, Prince ME. Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck. 2010;32:1195–201.PubMedPubMedCentralCrossRef
52.
53.
Neumeister V, Agarwal S, Bordeaux J, Camp RL, Rimm DL. In situ identification of putative cancer stem cells by multiplexing ALDH1, CD44, and cytokeratin identifies breast cancer patients with poor prognosis. Am J Pathol. 2010;176:2131–8.PubMedPubMedCentralCrossRef
54.
Chen Y-C, Chen Y-W, Hsu H-S, Tseng L-M, Huang P-I, Lu K-H, Chen D-T, Tai L-K, Yung M-C, Chang S-C. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun. 2009;385:307–13.PubMedCrossRef
55.
Prince ME, Zhou L, Moyer JS, Tao H, Lu L, Owen J, Egenti M, Zheng F, Chang AE, Xia J. Evaluation of the immunogenicity of ALDHhigh human head and neck squamous cell carcinoma cancer stem cells in vitro. Oral Oncol. 2016;59:30–42.PubMedPubMedCentralCrossRef
56.
Rae C, Tesson M, Babich JW, Boyd M, Sorensen A, Mairs RJ. The role of copper in disulfiram-induced toxicity and radiosensitization of cancer cells. J Nucl Med. 2013;54:953–60.PubMedCrossRef
57.
Keymoosi H, Gheytanchi E, Asgari M, Shariftabrizi A, Madjd Z. ALDH1 in combination with CD44 as putative cancer stem cell markers are correlated with poor prognosis in urothelial carcinoma of the urinary bladder. Asian Pac J Cancer Prev. 2014;15:2013–20.PubMedCrossRef
58.
Bourguignon LY, Wong G, Earle C, Chen L. Hyaluronan-CD44v3 interaction with Oct4-Sox2-Nanog promotes miR-302 expression leading to self-renewal, clonal formation, and cisplatin resistance in cancer stem cells from head and neck squamous cell carcinoma. J Biol Chem. 2012;287:32800–24.PubMedPubMedCentralCrossRef
59.
Wang Y, Yu Y, Tsuyada A, Ren X, Wu X, Stubblefield K, Rankin-Gee EK, Wang SE. Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene. 2011;30:1470.PubMedCrossRef
60.
Lee SH, Rigas NK, Lee C-R, Bang A, Srikanth S, Gwack Y, Kang MK, Kim RH, Park N-H, Shin K-H. Orai1 promotes tumor progression by enhancing cancer stemness via NFAT signaling in oral/oropharyngeal squamous cell carcinoma. Oncotarget. 2016;7:43239.PubMedPubMedCentralCrossRef
61.
Lee C-R, Lee SH, Rigas NK, Kim RH, Kang MK, Park N-H, Shin K-H. Elevated expression of JMJD6 is associated with oral carcinogenesis and maintains cancer stemness properties. Carcinogenesis. 2015;37:119–28.PubMedPubMedCentralCrossRef
62.
Lee SH, Hong HS, Liu ZX, Kim RH, Kang MK, Park N-H, Shin K-H. TNFα enhances cancer stem cell-like phenotype via Notch-Hes1 activation in oral squamous cell carcinoma cells. Biochem Biophys Res Commun. 2012;424:58–64.PubMedPubMedCentralCrossRef
63.
Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, Li J, Zhang Y, Chen L, Qian H. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 2011;11:71.PubMedPubMedCentralCrossRef
64.
Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN, Steindler DA. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia. 2005;7:967–76.PubMedPubMedCentralCrossRef
65.
Fujii H, Honoki K, Tsujiuchi T, Kido A, Yoshitani K, Takakura Y. Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int J Oncol. 2009;34:1381–6.PubMed
66.
Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, Chiapero-Stanke L, Taylor-Papadimitriou J, Burchell JM. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res. 2008;10:R52.PubMedPubMedCentralCrossRef
67.
Morata-Tarifa C, Jiménez G, García MA, Entrena JM, Griñán-Lisón C, Aguilera M, Picon-Ruiz M, Marchal JA. Low adherent cancer cell subpopulations are enriched in tumorigenic and metastatic epithelial-to-mesenchymal transition-induced cancer stem-like cells. Sci Rep. 2016;6:18772.PubMedPubMedCentralCrossRef
68.
Reynolds DS, Tevis KM, Blessing WA, Colson YL, Zaman MH, Grinstaff MW. Breast cancer spheroids reveal a differential cancer stem cell response to chemotherapeutic treatment. Sci Rep. 2017;7:10382.PubMedPubMedCentralCrossRef
69.
Liu J, Ma L, Xu J, Liu C, Zhang J, Liu J, Chen R, Zhou Y. Spheroid body-forming cells in the human gastric cancer cell line MKN-45 possess cancer stem cell properties. Int J Oncol. 2013;42:453–9.PubMedCrossRef
70.
Misuno K, Liu X, Feng S, Hu S. Quantitative proteomic analysis of sphere-forming stem-like oral cancer cells. Stem Cell Res Therapy. 2013;4:156.CrossRef
71.
Saleem S, Jamshed A, Faisal S, Hussain R, Tahseen M, Loya A, Sutton C. Patterns of cancer cell sphere formation in primary cultures of human oral tongue squamous cell carcinoma and neck nodes. Cancer Cell Int. 2014;14:542.PubMedPubMedCentralCrossRef
72.
Chen Y-K, Huang AH-C, Lin L-M. Sphere-forming-like cells (squamospheres) with cancer stem-like cell traits from VX2 rabbit buccal squamous cell carcinoma. Int J Oral Sci. 2014;6:212.PubMedPubMedCentralCrossRef
73.
Chen C, Wei Y, Hummel M, Hoffmann TK, Gross M, Kaufmann AM, Albers AE. Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLoS ONE. 2011;6:e16466.PubMedPubMedCentralCrossRef
74.
Vlashi E, Chen AM, Boyrie S, Yu G, Nguyen A, Brower PA, Hess CB, Pajonk F. Radiation-induced dedifferentiation of head and neck cancer cells into cancer stem cells depends on human papillomavirus status. Int J Radiat Oncol Biol Phys. 2016;94:1198–206.PubMedPubMedCentralCrossRef
75.
Dittmar T, Nagler C, Schwitalla S, Reith G, Niggemann B, Zänker KS. Recurrence cancer stem cells–made by cell fusion? Med Hypotheses. 2009;73:542–7.PubMedCrossRef
76.
Wang J, Guo LP, Chen LZ, Zeng YX, Lu SH. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res. 2007;67:3716–24.PubMedCrossRef
77.
Huang CX, Zhu Y, Duan GL, Yao JF, Li ZY, Li D, Wang QQ. Screening for MiRNAs related to laryngeal squamous carcinoma stem cell radiation. Asian Pac J Cancer Prev. 2013;14:4533–7.PubMedCrossRef
78.
Choi SH, Cho KJ, Nam SY, Lee SW, Kang J, Kim SY. Clinical significance of beta1 integrin expression as a prediction marker for radiotherapy in early glottic carcinoma. Laryngoscope. 2006;116:1228–31.PubMedCrossRef
79.
Bertrand G, Maalouf M, Boivin A, Battiston-Montagne P, Beuve M, Levy A, Jalade P, Fournier C, Ardail D, Magne N, et al. Targeting head and neck cancer stem cells to overcome resistance to photon and carbon ion radiation. Stem Cell Rev Rep. 2014;10:114–26.PubMedCrossRef
80.
Mishra L, Shetty K, Tang Y, Stuart A, Byers SW. The role of TGF-β and Wnt signaling in gastrointestinal stem cells and cancer. Oncogene. 2005;24:5775.PubMedCrossRef
81.
82.
Siddique HR, Saleem M. Role of BMI1, a stem cell factor, in cancer recurrence and chemoresistance: preclinical and clinical evidences. Stem Cells. 2012;30:372–8.PubMedCrossRef
83.
84.
O’Brien CA, Kreso A, Jamieson CH. Cancer stem cells and self-renewal. Clin Cancer Res. 2010;16:3113–20.PubMedCrossRef
85.
Giles RH, Es JH, Clevers H. Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta Rev Cancer. 2003;1653:1–24.CrossRef
86.
Liu S, Dontu G, Mantle ID, Patel S, Ahn N-S, Jackson KW, Suri P, Wicha MS. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66:6063–71.PubMedPubMedCentralCrossRef
87.
Leong KG, Karsan A. Recent insights into the role of notch signaling in tumorigenesis. Blood. 2006;107:2223–33.PubMedCrossRef
88.
Horikiri Y, Shimo T, Kurio N, Okui T, Matsumoto K, Iwamoto M, Sasaki A. Sonic hedgehog regulates osteoblast function by focal adhesion kinase signaling in the process of fracture healing. PLoS ONE. 2013;8:e76785.PubMedPubMedCentralCrossRef
89.
90.
Cavallaro U, Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer. 2004;4:118.PubMedCrossRef
91.
92.
Fan F, Samuel S, Evans KW, Lu J, Xia L, Zhou Y, Sceusi E, Tozzi F, Ye XC, Mani SA. Overexpression of Snail induces epithelial–mesenchymal transition and a cancer stem cell-like phenotype in human colorectal cancer cells. Cancer Med. 2012;1:5–16.PubMedPubMedCentralCrossRef
93.
Dieter SM, Ball CR, Hoffmann CM, Nowrouzi A, Herbst F, Zavidij O, Abel U, Arens A, Weichert W, Brand K. Distinct types of tumor-initiating cells form human colon cancer tumors and metastases. Cell Stem Cell. 2011;9:357–65.PubMedCrossRef
94.
Liu Z-H, Dai X-M, Du B. Hes1: a key role in stemness, metastasis and multidrug resistance. Cancer Biol Therapy. 2015;16(3):353–9.CrossRef
95.
Chu P-Y, Hu F-W, Yu C-C, Tsai L-L, Yu C-H, Wu B-C, Chen Y-W, Huang P-I, Lo W-L. Epithelial–mesenchymal transition transcription factor ZEB1/ZEB2 co-expression predicts poor prognosis and maintains tumor-initiating properties in head and neck cancer. Oral Oncol. 2013;49:34–41.PubMedCrossRef
96.
Kathawala RJ, Gupta P, Ashby CR Jr, Chen Z-S. The modulation of ABC transporter-mediated multidrug resistance in cancer: a review of the past decade. Drug Resist Updates. 2015;18:1–17.CrossRef
97.
Braunholz D, Saki M, Niehr F, Öztürk M, Puertolas BB, Konschak R, Budach V, Tinhofer I. Spheroid culture of head and neck cancer cells reveals an important role of EGFR signalling in anchorage independent survival. PLoS ONE. 2016;11:e0163149.PubMedPubMedCentralCrossRef
98.
99.
Cui H, Zhang JA, Chen Chen, Liu JJ. ABC transporter inhibitors in reversing multidrug resistance to chemotherapy. Curr Drug Targets. 2015;16:1356–71.PubMedCrossRef
100.
Song J, Chang I, Chen Z, Kang M, Wang C-Y. Characterization of side populations in HNSCC: highly invasive, chemoresistant and abnormal Wnt signaling. PLoS ONE. 2010;5:e11456.PubMedPubMedCentralCrossRef
101.
Golebiewska A, Brons NH, Bjerkvig R, Niclou SP. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell. 2011;8:136–47.PubMedCrossRef
102.
Zhang P, Zhang Y, Mao L, Zhang Z, Chen W. Side population in oral squamous cell carcinoma possesses tumor stem cell phenotypes. Cancer Lett. 2009;277:227–34.PubMedCrossRef
103.
Yanamoto S, Kawasaki G, Yamada S-I, Yoshitomi I, Kawano T, Yonezawa H, Rokutanda S, Naruse T, Umeda M. Isolation and characterization of cancer stem-like side population cells in human oral cancer cells. Oral oncology. 2011;47:855–60.PubMedCrossRef
104.
Rinkenbaugh AL, Baldwin AS: The NF-kappaB pathway and cancer stem cells. Cells. 2016;5.
105.
Garner JM, Fan M, Yang CH, Du Z, Sims M, Davidoff AM, Pfeffer LM. Constitutive activation of signal transducer and activator of transcription 3 (STAT3) and nuclear factor kappaB signaling in glioblastoma cancer stem cells regulates the Notch pathway. J Biol Chem. 2013;288:26167–76.PubMedPubMedCentralCrossRef
106.
Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T, Sherlock G, Lewicki J, Shedden K, Clarke MF. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med. 2007;356:217–26.PubMedCrossRef
107.
Murohashi M, Hinohara K, Kuroda M, Isagawa T, Tsuji S, Kobayashi S, Umezawa K, Tojo A, Aburatani H, Gotoh N. Gene set enrichment analysis provides insight into novel signalling pathways in breast cancer stem cells. Br J Cancer. 2010;102:206–12.PubMedCrossRef
108.
Bano N, Yadav M, Mohania D, Das BC. The role of NF-kappaB and miRNA in oral cancer and cancer stem cells with or without HPV16 infection. PLoS One. 2018;13:e0205518.PubMedPubMedCentralCrossRef
109.
Lee SH, Lee C-R, Rigas NK, Kim RH, Kang MK, Park N-H, Shin K-H. Human papillomavirus 16 (HPV16) enhances tumor growth and cancer stemness of HPV-negative oral/oropharyngeal squamous cell carcinoma cells via miR-181 regulation. Papillomavirus Res. 2015;1:116–25.PubMedPubMedCentralCrossRef
110.
Song SJ, Poliseno L, Song MS, Ala U, Webster K, Ng C, Beringer G, Brikbak NJ, Yuan X, Cantley LC. MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling. Cell. 2013;154:311–24.PubMedPubMedCentralCrossRef
111.
Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011;17:211.PubMedPubMedCentralCrossRef
112.
Mirzaei H, Yazdi F, Salehi R, Mirzaei HR. SiRNA and epigenetic aberrations in ovarian cancer. J Cancer Res Ther. 2016;12:498–508.PubMedCrossRef
113.
Khani P, Nasri F, Khani Chamani F, Saeidi F, Sadri Nahand J, Tabibkhooei A, Mirzaei H. Genetic and epigenetic contribution to astrocytic gliomas pathogenesis. J Neurochem. 2019;148:188–203.PubMedCrossRef
114.
Moridikia A, Mirzaei H. MicroRNAs: potential candidates for diagnosis and treatment of colorectal cancer. J Cell Physiol. 2018;233:901–13.PubMedCrossRef
115.
Saadatpour L, Fadaee E, Fadaei S, Nassiri Mansour R, Mohammadi M, Mousavi SM, Goodarzi M, Verdi J, Mirzaei H. Glioblastoma: exosome and microRNA as novel diagnosis biomarkers. Cancer Gene Ther. 2016;23:415–8.PubMedCrossRef
116.
Nahand JS, Taghizadeh-Boroujeni S, Karimzadeh M, Borran S, Pourhanifeh MH, Moghoofei M, Bokharaei-Salim F, Karampoor S, Jafari A, Asemi Z, et al. microRNAs: new prognostic, diagnostic, and therapeutic biomarkers in cervical cancer. J Cell Physiol. 2019;234:17064–99.PubMedCrossRef
117.
Naeli P, Yousefi F, Ghasemi Y, Savardashtaki A, Mirzaei H. The role of microRNAs in lung cancer: implications for diagnosis and therapy. Curr Mol Med. 2020;20:90–101.PubMedCrossRef
118.
Aghdam AM, Amiri A, Salarinia R, Masoudifar A, Ghasemi F, Mirzaei H. MicroRNAs as diagnostic, prognostic, and therapeutic biomarkers in prostate cancer. Crit Rev Eukaryot Gene Exp. 2019;29:127–39.CrossRef
119.
Kooistra SM, Helin K. Molecular mechanisms and potential functions of histone demethylases. Nat Rev Mol Cell Biol. 2012;13:297.PubMedCrossRef
120.
Ye L, Fan Z, Yu B, Chang J, Al Hezaimi K, Zhou X, Park N-H, Wang C-Y. Histone demethylases KDM4B and KDM6B promotes osteogenic differentiation of human MSCs. Cell Stem Cell. 2012;11:50–61.PubMedPubMedCentralCrossRef
121.
Hsia DA, Tepper CG, Pochampalli MR, Hsia EY, Izumiya C, Huerta SB, Wright ME, Chen H-W, Kung H-J, Izumiya Y. KDM8, a H3K36me2 histone demethylase that acts in the cyclin A1 coding region to regulate cancer cell proliferation. Proc Natl Acad Sci. 2010;107:9671–6.PubMedCrossRefPubMedCentral
122.
Agger K, Cloos PA, Rudkjær L, Williams K, Andersen G, Christensen J, Helin K. The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A–ARF locus in response to oncogene-and stress-induced senescence. Genes Dev. 2009;23:1171–6.PubMedPubMedCentralCrossRef
123.
124.
Li J, Yu B, Deng P, Cheng Y, Yu Y, Kevork K, Ramadoss S, Ding X, Li X, Wang C-Y. KDM3 epigenetically controls tumorigenic potentials of human colorectal cancer stem cells through Wnt/β-catenin signalling. Nat Commun. 2017;8:15146.PubMedPubMedCentralCrossRef
125.
Sherry-Lynes MM, Sengupta S, Kulkarni S, Cochran BH. Regulation of the JMJD3 (KDM6B) histone demethylase in glioblastoma stem cells by STAT3. PLoS ONE. 2017;12:e0174775.PubMedPubMedCentralCrossRef
126.
Yan Q, Zhang S-M, Meeth K, Micevic G, Bosenberg M. Histone demethylase KDM5B is critical for PI3K-AKT-mTOR signaling and stemness of melanoma. FASEB J. 2017;31:468.CrossRef
127.
Yamamoto S, Tateishi K, Kudo Y, Yamamoto K, Isagawa T, Nagae G, Nakatsuka T, Asaoka Y, Ijichi H, Hirata Y. Histone demethylase KDM4C regulates sphere formation by mediating the cross talk between Wnt and Notch pathways in colonic cancer cells. Carcinogenesis. 2013;34:2380–8.PubMedCrossRef
128.
Metzger E, Stepputtis SS, Strietz J, Preca B-T, Urban S, Willmann D, Allen A, Zenk F, Iovino N, Bronsert P. KDM4 inhibition targets breast cancer stem–like cells. Cancer Res. 2017;77:5900–12.PubMedCrossRef
129.
130.
Amente S, Lania L, Majello B. The histone LSD1 demethylase in stemness and cancer transcription programs. Bioch Biophys Acta Gene Regul Mech. 2013;1829:981–6.CrossRef
131.
Chang B, Chen Y, Zhao Y, Bruick RK. JMJD6 is a histone arginine demethylase. Science. 2007;318:444–7.CrossRefPubMed
132.
Webby CJ, Wolf A, Gromak N, Dreger M, Kramer H, Kessler B, Nielsen ML, Schmitz C, Butler DS, Yates JR. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science. 2009;325:90–3.CrossRefPubMed
133.
Lee YF, Miller LD, Chan XB, Black MA, Pang B, Ong CW, Salto-Tellez M, Liu ET, Desai KV. JMJD6 is a driver of cellular proliferation and motility and a marker of poor prognosis in breast cancer. Breast Cancer Res. 2012;14:3001.CrossRef
134.
Boeckel J-N, Guarani V, Koyanagi M, Roexe T, Lengeling A, Schermuly RT, Gellert P, Braun T, Zeiher A, Dimmeler S. Jumonji domain-containing protein 6 (Jmjd6) is required for angiogenic sprouting and regulates splicing of VEGF-receptor 1. Proc Natl Acad Sci. 2011;108:3276–81.PubMedCrossRefPubMedCentral
135.
Hao J, Zhang Y, Deng M, Ye R, Zhao S, Wang Y, Li J, Zhao Z. MicroRNA control of epithelial-mesenchymal transition in cancer stem cells. Int J Cancer. 2014;135:1019–27.PubMedCrossRef
136.
137.
Vafadar A, Shabaninejad Z, Movahedpour A, Mohammadi S, Fathullahzadeh S, Mirzaei HR, Namdar A, Savardashtaki A, Mirzaei H. Long non-coding RNAs as epigenetic regulators in cancer. Curr Pharm Des. 2019;25:3563–77.PubMedCrossRef
138.
Shabaninejad Z, Vafadar A, Movahedpour A, Ghasemi Y, Namdar A, Fathizadeh H, Pourhanifeh MH, Savardashtaki A, Mirzaei H. Circular RNAs in cancer: new insights into functions and implications in ovarian cancer. J Ovarian Res. 2019;12:84.PubMedPubMedCentralCrossRef
139.
Saeedi Borujeni MJ, Esfandiary E, Baradaran A, Valiani A, Ghanadian M, Codoner-Franch P, Basirat R, Alonso-Iglesias E, Mirzaei H. Molecular aspects of pancreatic beta-cell dysfunction: Oxidative stress, microRNA, and long noncoding RNA. J Cell Physiol. 2019;234:8411–25.PubMedCrossRef
140.
141.
Naeli P, Pourhanifeh MH, Karimzadeh MR, Shabaninejad Z, Movahedpour A, Tarrahimofrad H, Mirzaei HR, Bafrani HH, Savardashtaki A, Mirzaei H, Hamblin MR. Circular RNAs and gastrointestinal cancers: epigenetic regulators with a prognostic and therapeutic role. Crit Rev Oncol Hematol. 2020;145:102854.PubMedCrossRef
142.
Mirzaei H, Momeni F, Saadatpour L, Sahebkar A, Goodarzi M, Masoudifar A, Kouhpayeh S, Salehi H, Mirzaei HR, Jaafari MR. MicroRNA: relevance to stroke diagnosis, prognosis, and therapy. J Cell Physiol. 2018;233:856–65.PubMedCrossRef
143.
Gholamin S, Mirzaei H. GD2-targeted immunotherapy and potential value of circulating microRNAs in neuroblastoma. J Cell Physiol. 2018;233:866–79.PubMedCrossRef
144.
Jamali L, Tofigh R, Tutunchi S, Panahi G, Borhani F, Akhavan S, Nourmohammadi P, Ghaderian SMH, Rasouli M, Mirzaei H. Circulating microRNAs as diagnostic and therapeutic biomarkers in gastric and esophageal cancers. J Cell Physiol. 2018;233:8538–50.PubMedCrossRef
145.
Masoudi MS, Mehrabian E, Mirzaei H. MiR-21: a key player in glioblastoma pathogenesis. J Cell Biochem. 2018;119:1285–90.PubMedCrossRef
146.
Simonian M, Mosallayi M, Mirzaei H. Circulating miR-21 as novel biomarker in gastric cancer: diagnostic and prognostic biomarker. J Cancer Res Ther. 2018;14:475.PubMed
147.
Fathullahzadeh S, Mirzaei H, Honardoost MA, Sahebkar A, Salehi M. Circulating microRNA-192 as a diagnostic biomarker in human chronic lymphocytic leukemia. Cancer Gene Ther. 2016;23:327–32.PubMedCrossRef
148.
Mashreghi M, Azarpara H, Bazaz MR, Jafari A, Masoudifar A, Mirzaei H. Angiogenesis biomarkers and their targeting ligands as potential targets for tumor angiogenesis. J Cell Physiol. 2018;233:2949–65.PubMedCrossRef
149.
Taghavipour M, Sadoughi F, Mirzaei H, Yousefi B, Moazzami B, Chaichian S, Mansournia MA, Asemi Z. Apoptotic functions of microRNAs in pathogenesis, diagnosis, and treatment of endometriosis. Cell Biosci. 2020;10:12.PubMedPubMedCentralCrossRef
150.
Sadri Nahand J, Moghoofei M, Salmaninejad A, Bahmanpour Z, Karimzadeh M, Nasiri M, Mirzaei HR, Pourhanifeh MH, Bokharaei-Salim F, Mirzaei H. Pathogenic role of exosomes and microRNAs in HPV-mediated inflammation and cervical cancer: a review. Int J Cancer. 2020;146:305–20.PubMedCrossRef
151.
Mohammadi M, Goodarzi M, Jaafari MR, Mirzaei HR, Mirzaei H. Circulating microRNA: a new candidate for diagnostic biomarker in neuroblastoma. Cancer Gene Ther. 2016;23:371–2.PubMedCrossRef
152.
Golabchi K, Soleimani-Jelodar R, Aghadoost N, Momeni F, Moridikia A, Nahand JS, Masoudifar A, Razmjoo H, Mirzaei H. MicroRNAs in retinoblastoma: potential diagnostic and therapeutic biomarkers. J Cell Physiol. 2018;233:3016–23.PubMedCrossRef
153.
Nahand JS, Karimzadeh MR, Nezamnia M, Fatemipour M, Khatami A, Jamshidi S, Moghoofei M, Taghizadieh M, Hajighadimi S, Shafiee A, et al. The role of miR-146a in viral infection. IUBMB Life. 2020;72:343–60.PubMedCrossRef
154.
155.
Sadri Nahand J, Bokharaei-Salim F, Karimzadeh M, Moghoofei M, Karampoor S, Mirzaei HR, Tabibzadeh A, Jafari A, Ghaderi A, Asemi Z, et al. MicroRNAs and exosomes: key players in HIV pathogenesis. HIV Med. 2019;21(4):246–278.PubMedCrossRef
156.
Pakshir K, Badali H. Interactions between immune response to fungal infection and microRNAs: the pioneer tuners. Mycoses. 2020;63:4–20.PubMedCrossRef
157.
Shabaninejad Z, Yousefi F, Movahedpour A, Ghasemi Y, Dokanehiifard S, Rezaei S, Aryan R, Savardashtaki A, Mirzaei H. Electrochemical-based biosensors for microRNA detection: nanotechnology comes into view. Anal Biochem. 2019;581:113349.PubMedCrossRef
158.
Mirzaei H, Ferns GA, Avan A, Mobarhan MG. Cytokines and microRNA in coronary artery disease. Adv Clin Chem. 2017;82:47–70.PubMedCrossRef
159.
Jafari SH, Saadatpour Z, Salmaninejad A, Momeni F, Mokhtari M, Nahand JS, Rahmati M, Mirzaei H. Breast cancer diagnosis: Imaging techniques and biochemical markers. J Cell Physiol. 2018;233:5200–13.PubMedCrossRef
160.
Saeedi Borujeni MJ, Esfandiary E, Taheripak G, Codoner-Franch P, Alonso-Iglesias E, Mirzaei H. Molecular aspects of diabetes mellitus: resistin, microRNA, and exosome. J Cell Biochem. 2018;119:1257–72.PubMedCrossRef
161.
Mirzaei H. Stroke in women: risk factors and clinical biomarkers. J Cell Biochem. 2017;118:4191–202.PubMedCrossRef
162.
Tavakolizadeh J, Roshanaei K, Salmaninejad A, Yari R, Nahand JS, Sarkarizi HK, Mousavi SM, Salarinia R, Rahmati M, Mousavi SF, et al. MicroRNAs and exosomes in depression: potential diagnostic biomarkers. J Cell Biochem. 2018;119:3783–97.PubMedCrossRef
163.
Rashidi B, Hoseini Z, Sahebkar A, Mirzaei H. Anti-atherosclerotic effects of vitamins d and e in suppression of atherogenesis. J Cell Physiol. 2017;232:2968–76.PubMedCrossRef
164.
Kim T, Veronese A, Pichiorri F, Lee TJ, Jeon YJ, Volinia S, Pineau P, Marchio A, Palatini J, Suh SS, et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J Exp Med. 2011;208:875–83.PubMedPubMedCentralCrossRef
165.
Ku TK, Nguyen DC, Karaman M, Gill P, Hacia JG, Crowe DL. Loss of p53 expression correlates with metastatic phenotype and transcriptional profile in a new mouse model of head and neck cancer. Mol Cancer Res. 2007;5:351–62.PubMedCrossRef
166.
Hollstein M, Rice K, Greenblatt MS, Soussi T, Fuchs R, Sorlie T, Hovig E, Smith-Sorensen B, Montesano R, Harris CC. Database of p53 gene somatic mutations in human tumors and cell lines. Nucleic Acids Res. 1994;22:3551–5.PubMedPubMedCentral
167.
Yu CC, Tsai LL, Wang ML, Yu CH, Lo WL, Chang YC, Chiou GY, Chou MY, Chiou SH. miR145 targets the SOX9/ADAM17 axis to inhibit tumor-initiating cells and IL-6-mediated paracrine effects in head and neck cancer. Cancer Res. 2013;73:3425–40.PubMedCrossRef
168.
Shabaninejad Z, Pourhanifeh MH, Movahedpour A, Mottaghi R, Nickdasti A, Mortezapour E, Shafiee A, Hajighadimi S, Moradizarmehri S, Sadeghian M, et al. Therapeutic potentials of curcumin in the treatment of glioblstoma. Eur J Med Chem. 2020;188:112040.PubMedCrossRef
169.
Ahmed S, Khan H, Mirzaei H. Mechanics insights of curcumin in myocardial ischemia: where are we standing? Eur J Med Chem. 2019;183:111658.PubMedCrossRef
170.
Ghasemi F, Shafiee M, Banikazemi Z, Pourhanifeh MH, Khanbabaei H, Shamshirian A, Amiri Moghadam S, ArefNezhad R, Sahebkar A, Avan A, Mirzaei H. Curcumin inhibits NF-kB and Wnt/beta-catenin pathways in cervical cancer cells. Pathol Res Pract. 2019;215:152556.PubMedCrossRef
171.
Shafabakhsh R, Pourhanifeh MH, Mirzaei HR, Sahebkar A, Asemi Z, Mirzaei H. Targeting regulatory T cells by curcumin: a potential for cancer immunotherapy. Pharmacol Res. 2019;147:104353.PubMedCrossRef
172.
Banikazemi Z, Haji HA, Mohammadi M, Taheripak G, Iranifar E, Poursadeghiyan M, Moridikia A, Rashidi B, Taghizadeh M, Mirzaei H. Diet and cancer prevention: dietary compounds, dietary MicroRNAs, and dietary exosomes. J Cell Biochem. 2018;119:185–96.PubMedCrossRef
173.
Mirzaei H, Masoudifar A, Sahebkar A, Zare N, Sadri Nahand J, Rashidi B, Mehrabian E, Mohammadi M, Mirzaei HR, Jaafari MR. MicroRNA: a novel target of curcumin in cancer therapy. J Cell Physiol. 2018;233:3004–15.PubMedCrossRef
174.
Mirzaei H, Khoi MJ, Azizi M, Goodarzi M. Can curcumin and its analogs be a new treatment option in cancer therapy? Cancer Gene Ther. 2016;23:410.PubMedCrossRef
175.
Mirzaei H, Naseri G, Rezaee R, Mohammadi M, Banikazemi Z, Mirzaei HR, Salehi H, Peyvandi M, Pawelek JM, Sahebkar A. Curcumin: a new candidate for melanoma therapy? Int J Cancer. 2016;139:1683–95.PubMedCrossRef
176.
Sun J, Lu F, He H, Shen J, Messina J, Mathew R, Wang D, Sarnaik AA, Chang W-C, Kim M. STIM1-and Orai1-mediated Ca2+ oscillation orchestrates invadopodium formation and melanoma invasion. J Cell Biol. 2014;207:535–48.PubMedPubMedCentralCrossRef
177.
Zhu H, Zhang H, Jin F, Fang M, Huang M, Yang CS, Chen T, Fu L, Pan Z. Elevated Orai1 expression mediates tumor-promoting intracellular Ca2+ oscillations in human esophageal squamous cell carcinoma. Oncotarget. 2014;5:3455.PubMedPubMedCentralCrossRef
178.
Zhao W, Wang L, Han H, Jin K, Lin N, Guo T, Chen Y, Cheng H, Lu F, Fang W. 1B50-1, a mAb raised against recurrent tumor cells, targets liver tumor-initiating cells by binding to the calcium channel α2δ1 subunit. Cancer Cell. 2013;23:541–56.PubMedCrossRef
179.
Prevarskaya N, Skryma R, Shuba Y. Calcium in tumour metastasis: new roles for known actors. Nat Rev Cancer. 2011;11:609.PubMedCrossRef
180.
Roderick HL, Cook SJ. Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat Rev Cancer. 2008;8:361.PubMedCrossRef
181.
Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ. Calcium and cancer: targeting Ca2+ transport. Nat Rev Cancer. 2007;7:519.PubMedCrossRef
182.
Berridge MJ, Bootman MD, Roderick HL. Calcium: calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4:517.PubMedCrossRef
183.
Srikanth S, Gwack Y. Molecular regulation of the pore component of CRAC channels, Orai1. In: Current topics in membranes. 71. Amsterdam: Elsevier; 2013. p. 181–207.
184.
Gwack Y, Srikanth S, Feske S, Cruz-Guilloty F, Oh-hora M, Neems DS, Hogan PG, Rao A. Biochemical and functional characterization of Orai proteins. J Biol Chem. 2007;282:16232–43.PubMedCrossRef
185.
Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. Orai1 is an essential pore subunit of the CRAC channel. Nature. 2006;443:230.PubMedCrossRef
186.
Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel S-H, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 2006;441:179.PubMedCrossRef
187.
188.
Parekh AB. Functional consequences of activating store-operated CRAC channels. Cell Calcium. 2007;42:111–21.PubMedCrossRef
189.
190.
Zhan Z-Y, Zhong L-X, Feng M, Wang J-F, Liu D-B, Xiong J-P. Over-expression of Orai1 mediates cell proliferation and associates with poor prognosis in human non-small cell lung carcinoma. Int J Clin Exp Pathol. 2015;8:5080.PubMedPubMedCentral
191.
Deng W, Wang J, Zhang J, Cai J, Bai Z, Zhang Z. Orai1, a direct target of microRNA-519, promotes progression of colorectal cancer via Akt/GSK3β signaling pathway. Dig Dis Sci. 2016;61:1553–60.PubMedCrossRef
192.
Xia J, Wang H, Huang H, Sun L, Dong S, Huang N, Shi M, Bin J, Liao Y, Liao W. Elevated Orai1 and STIM1 expressions upregulate MACC1 expression to promote tumor cell proliferation, metabolism, migration, and invasion in human gastric cancer. Cancer Lett. 2016;381:31–40.PubMedCrossRef
193.
Wang L, Hao J, Zhang Y, Yang Z, Cao Y, Lu W, Shu Y, Jiang L, Hu Y, Lv W. Orai1 mediates tumor-promoting store-operated Ca2+ entry in human gastrointestinal stromal tumors via c-KIT and the extracellular signal-regulated kinase pathway. Tumor Biol. 2017;39:1010428317691426.
194.
Kim J-H, Lkhagvadorj S, Lee M-R, Hwang K-H, Chung HC, Jung JH, Cha S-K, Eom M. Orai1 and STIM1 are critical for cell migration and proliferation of clear cell renal cell carcinoma. Biochem Biophys Res Commun. 2014;448:76–82.PubMedCrossRef
195.
Liu H, Hughes JD, Rollins S, Chen B, Perkins E. Calcium entry via ORAI1 regulates glioblastoma cell proliferation and apoptosis. Exp Mol Pathol. 2011;91:753–60.PubMedCrossRef
196.
Yang S, Zhang JJ, Huang X-Y. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell. 2009;15:124–34.PubMedCrossRef
197.
Flourakis M, Lehen’kyi V, Beck B, Raphael M, Vandenberghe M, Abeele FV, Roudbaraki M, Lepage G, Mauroy B, Romanin C. Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis. 2010;1:e75.PubMedPubMedCentralCrossRef
198.
Maul-Pavicic A, Chiang SC, Rensing-Ehl A, Jessen B, Fauriat C, Wood SM, Sjöqvist S, Hufnagel M, Schulze I, Bass T. ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc Natl Acad Sci. 2011;108:3324–9.PubMedCrossRefPubMedCentral
199.
Gwack Y, Feske S, Srikanth S, Hogan PG, Rao A. Signalling to transcription: store-operated Ca2+ entry and NFAT activation in lymphocytes. Cell Calcium. 2007;42:145–56.PubMedCrossRef
200.
Xiao Z-J, Liu J, Wang S-Q, Zhu Y, Gao X-Y, Tin VP-C, Qin J, Wang J-W, Mong MP. NFATc2 enhances tumor-initiating phenotypes through the NFATc2/SOX2/ALDH axis in lung adenocarcinoma. Elife. 2017;6:e26733.PubMedPubMedCentralCrossRef
201.
Hessmann E, Zhang J-S, Chen N-M, Hasselluhn M, Liou G-Y, Storz P, Ellenrieder V, Billadeau DD, Koenig A. NFATc4 regulates Sox9 gene expression in acinar cell plasticity and pancreatic cancer initiation. Stem Cells Int. 2016;2016:5272498.PubMedCrossRef
202.
Perotti V, Baldassari P, Molla A, Vegetti C, Bersani I, Maurichi A, Santinami M, Anichini A, Mortarini R. NFATc2 is an intrinsic regulator of melanoma dedifferentiation. Oncogene. 2016;35:2862.PubMedCrossRef
203.
Gerlach K, Daniel C, Lehr HA, Nikolaev A, Gerlach T, Atreya R, Rose-John S, Neurath MF, Weigmann B. Transcription factor NFATc2 controls the emergence of colon cancer associated with IL-6-dependent colitis. Cancer Res. 2012;72:4340–50.PubMedCrossRef
204.
Yoshida R, Nagata M, Nakayama H, Niimori-Kita K, Hassan W, Tanaka T, Shinohara M, Ito T. The pathological significance of Notch1 in oral squamous cell carcinoma. Lab Invest. 2013;93:1068.PubMedCrossRef
205.
Kageyama R, Ohtsuka T, Tomita K. The bHLH gene Hes1 regulates differentiation of multiple cell types. Mol Cells. 2000;10:1–7.PubMedCrossRef
206.
207.
Kim RH, Kang MK, Shin K-H, Oo ZM, Han T, Baluda MA, Park N-H. Bmi-1 cooperates with human papillomavirus type 16 E6 to immortalize normal human oral keratinocytes. Exp Cell Res. 2007;313:462–72.PubMedCrossRef
208.
Wang Q, Li Z, Wu Y, Huang R, Zhu Y, Zhang W, Wang Y, Cheng J. Pharmacological inhibition of Bmi1 by PTC-209 impaired tumor growth in head neck squamous cell carcinoma. Cancer Cell Int. 2017;17:107.PubMedPubMedCentralCrossRef
209.
Chen D, Wu M, Li Y, Chang I, Yuan Q, Ekimyan-Salvo M, Deng P, Yu B, Yu Y, Dong J. Targeting BMI1 + cancer stem cells overcomes chemoresistance and inhibits metastases in squamous cell carcinoma. Cell Stem Cell. 2017;20(621–634):e626.
210.
Salarinia R, Sahebkar A, Peyvandi M, Mirzaei HR, Jaafari MR, Riahi MM, Ebrahimnejad H, Nahand JS, Hadjati J, Asrami MO, et al. Epi-drugs and Epi-miRs: moving beyond current cancer therapies. Curr Cancer Drug Targets. 2016;16:773–88.PubMedCrossRef
211.
212.
Saadatpour Z, Rezaei A, Ebrahimnejad H, Baghaei B, Bjorklund G, Chartrand M, Sahebkar A, Morovati H, Mirzaei HR, Mirzaei H. Imaging techniques: new avenues in cancer gene and cell therapy. Cancer Gene Ther. 2017;24:1–5.PubMedCrossRef
213.
Mirzaei H, Shakeri A, Rashidi B, Jalili A, Banikazemi Z, Sahebkar A. Phytosomal curcumin: a review of pharmacokinetic, experimental and clinical studies. Biomed Pharmacother. 2017;85:102–12.PubMedCrossRef
214.
Mirzaei HR, Mirzaei H, Lee SY, Hadjati J, Till BG. Prospects for chimeric antigen receptor (CAR) gammadelta T cells: a potential game changer for adoptive T cell cancer immunotherapy. Cancer Lett. 2016;380:413–23.PubMedPubMedCentralCrossRef
215.
Mirzaei HR, Pourghadamyari H, Rahmati M, Mohammadi A, Nahand JS, Rezaei A, Mirzaei H, Hadjati J. Gene-knocked out chimeric antigen receptor (CAR) T cells: tuning up for the next generation cancer immunotherapy. Cancer Lett. 2018;423:95–104.PubMedCrossRef
216.
Vakili-Ghartavol R, Mombeiny R, Salmaninejad A, Sorkhabadi SMR, Faridi-Majidi R, Jaafari MR, Mirzaei H. Tumor-associated macrophages and epithelial-mesenchymal transition in cancer: nanotechnology comes into view. J Cell Physiol. 2018;233:9223–36.PubMedCrossRef
217.
218.
Sadeghi S, Davoodvandi A, Pourhanifeh MH, Sharifi N, ArefNezhad R, Sahebnasagh R, Moghadam SA, Sahebkar A, Mirzaei H. Anti-cancer effects of cinnamon: insights into its apoptosis effects. Eur J Med Chem. 2019;178:131–40.PubMedCrossRef
219.
Davoodvandi A, Sahebnasagh R, Mardanshah O, Asemi Z, Nejati M, Shahrzad MK, Mirzaei HR, Mirzaei H. Medicinal plants as natural polarizers of macrophages: phytochemicals and pharmacological effects. Curr Pharm Des. 2019;25:3225–38.PubMedCrossRef
220.
221.
Damek-Poprawa M, Volgina A, Korostoff J, Sollecito TP, Brose MS, O’Malley BW Jr, Akintoye SO, DiRienzo JM. Targeted inhibition of CD133+ cells in oral cancer cell lines. J Dent Res. 2011;90:638–45.PubMedPubMedCentralCrossRef
222.
Waldron NN, Kaufman DS, Oh S, Inde Z, Hexum MK, Ohlfest JR, Vallera DA. Targeting tumor-initiating cancer cells with dCD133KDEL shows impressive tumor reductions in a xenotransplant model of human head and neck cancer. Mol Cancer Ther. 2011;10:1829–38.PubMedPubMedCentralCrossRef
223.
Murillo-Sauca O, Chung MK, Shin JH, Karamboulas C, Kwok S, Jung YH, Oakley R, Tysome JR, Farnebo LO, Kaplan MJ, et al. CD271 is a functional and targetable marker of tumor-initiating cells in head and neck squamous cell carcinoma. Oncotarget. 2014;5:6854–66.PubMedPubMedCentralCrossRef
224.
Kuo SZ, Blair KJ, Rahimy E, Kiang A, Abhold E, Fan JB, Wang-Rodriguez J, Altuna X, Ongkeko WM. Salinomycin induces cell death and differentiation in head and neck squamous cell carcinoma stem cells despite activation of epithelial-mesenchymal transition and Akt. BMC Cancer. 2012;12:556.PubMedPubMedCentralCrossRef
225.
Chiu CC, Lee LY, Li YC, Chen YJ, Lu YC, Li YL, Wang HM, Chang JT, Cheng AJ. Grp78 as a therapeutic target for refractory head-neck cancer with CD24(-)CD44(+) stemness phenotype. Cancer Gene Ther. 2013;20:606–15.PubMedCrossRef
226.
Huang CE, Yu CC, Hu FW, Chou MY, Tsai LL. Enhanced chemosensitivity by targeting Nanog in head and neck squamous cell carcinomas. Int J Mol Sci. 2014;15:14935–48.PubMedPubMedCentralCrossRef
227.
Chang CW, Chen YS, Chou SH, Han CL, Chen YJ, Yang CC, Huang CY, Lo JF. Distinct subpopulations of head and neck cancer cells with different levels of intracellular reactive oxygen species exhibit diverse stemness, proliferation, and chemosensitivity. Cancer Res. 2014;74:6291–305.PubMedCrossRef
228.
Ma L, Zhang G, Miao XB, Deng XB, Wu Y, Liu Y, Jin ZR, Li XQ, Liu QZ, Sun DX, et al. Cancer stem-like cell properties are regulated by EGFR/AKT/beta-catenin signaling and preferentially inhibited by gefitinib in nasopharyngeal carcinoma. FEBS J. 2013;280:2027–41.PubMedCrossRef
229.
Wan G, Zhou L, Xie M, Chen H, Tian J. Characterization of side population cells from laryngeal cancer cell lines. Head Neck. 2010;32:1302–9.PubMedCrossRef
230.
Katayama R, Koike S, Sato S, Sugimoto Y, Tsuruo T, Fujita N. Dofequidar fumarate sensitizes cancer stem-like side population cells to chemotherapeutic drugs by inhibiting ABCG2/BCRP-mediated drug export. Cancer Sci. 2009;100:2060–8.PubMedCrossRef
231.
Gan GN, Eagles J, Keysar SB, Wang G, Glogowska MJ, Altunbas C, Anderson RT, Le PN, Morton JJ, Frederick B, et al. Hedgehog signaling drives radioresistance and stroma-driven tumor repopulation in head and neck squamous cancers. Cancer Res. 2014;74:7024–36.PubMedPubMedCentralCrossRef
232.
Pai S, Bamodu OA. CD47-SIRPalpha signaling induces epithelial-mesenchymal transition and cancer stemness and links to a poor prognosis in patients with oral squamous cell carcinoma. 2019;8.
233.
Keysar SB, Gomes N. Inhibiting translation elongation with SVC112 suppresses cancer stem cells and inhibits growth in head and neck squamous carcinoma. Cancer Res. 2020;80(5):1183–98.PubMedCrossRefPubMedCentral
234.
Han Z, Li Q, Wang Y, Wang L, Li X, Ge N, Wang Y, Guo C. Niclosamide induces cell cycle arrest in G1 phase in head and neck squamous cell carcinoma through Let-7d/CDC34 axis. Front Pharmacol. 2018;9:1544.PubMedCrossRef
235.
Kerk SA, Finkel KA, Pearson AT, Warner KA, Zhang Z, Nor F, Wagner VP, Vargas PA, Wicha MS, Hurt EM, et al. 5T4-targeted therapy ablates cancer stem cells and prevents recurrence of head and neck squamous cell carcinoma. Clin Cancer Res. 2017;23:2516–27.PubMedCrossRef
236.
Sun S, Liu S, Duan SZ, Zhang L, Zhou H, Hu Y, Zhou X, Shi C, Zhou R, Zhang Z. Targeting the c-Met/FZD8 signaling axis eliminates patient-derived cancer stem-like cells in head and neck squamous carcinomas. Cancer Res. 2014;74:7546–59.PubMedCrossRef
237.
Odenthal J, Rijpkema M, Bos D, Wagena E, Croes H, Grenman R, Boerman O, Takes R, Friedl P. Targeting CD44v6 for fluorescence-guided surgery in head and neck squamous cell carcinoma. Sci Rep. 2018;8:10467.PubMedPubMedCentralCrossRef
238.
Colnot DR, Quak JJ, Roos JC, van Lingen A, Wilhelm AJ, van Kamp GJ, Huijgens PC, Snow GB, van Dongen GA. Phase I therapy study of 186Re-labeled chimeric monoclonal antibody U36 in patients with squamous cell carcinoma of the head and neck. J Nucl Med. 2000;41:1999–2010.PubMed
239.
Kim J, Shin JH, Chen CH, Cruz L, Farnebo L, Yang J, Borges P, Kang G, Mochly-Rosen D, Sunwoo JB. Targeting aldehyde dehydrogenase activity in head and neck squamous cell carcinoma with a novel small molecule inhibitor. Oncotarget. 2017;8:52345–56.PubMedPubMedCentralCrossRef
240.
Liu J, Pan S, Hsieh MH, Ng N, Sun F, Wang T, Kasibhatla S, Schuller AG, Li AG, Cheng D, et al. Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974. Proc Natl Acad Sci USA. 2013;110:20224–9.PubMedCrossRefPubMedCentral
241.
McDermott SC, Rodriguez-Ramirez C, McDermott SP, Wicha MS, Nor JE. FGFR signaling regulates resistance of head and neck cancer stem cells to cisplatin. Oncotarget. 2018;9:25148–65.PubMedPubMedCentralCrossRef
Metadata
Title
Cancer stem cells and oral cancer: insights into molecular mechanisms and therapeutic approaches
Authors
Ghazaleh Baniebrahimi
Fatemeh Mir
Razieh Khanmohammadi
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2020
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-020-01192-0

Other articles of this Issue 1/2020

Cancer Cell International 1/2020 Go to the issue

Primary research

Identification of a potentially functional circRNA–miRNA–mRNA regulatory network for investigating pathogenesis and providing possible biomarkers of bladder cancer

Primary research

Synergy between hemagglutinin 2 (HA2) subunit of influenza fusogenic membrane glycoprotein and oncolytic Newcastle disease virus suppressed tumor growth and further enhanced by Immune checkpoint PD-1 blockade

Primary research

NF-κB and pSTAT3 synergistically drive G6PD overexpression and facilitate sensitivity to G6PD inhibition in ccRCC

Correction

Correction to: Identification of prognosis-related genes and construction of multi-regulatory networks in pancreatic cancer microenvironment by bioinformatics analysis

Primary research

Up-regulation of circ_LARP4 suppresses cell proliferation and migration in ovarian cancer by regulating miR-513b-5p/LARP4 axis

Primary research

MCM3AP-AS1/miR-876-5p/WNT5A axis regulates the proliferation of prostate cancer cells
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine
Image Credits