Cancer stem cells in esophageal squamous cell cancer (Review)
- Authors:
- Qian Wu
- Zhe Wu
- Cuiyu Bao
- Wenjing Li
- Hui He
- Yanling Sun
- Zimin Chen
- Hao Zhang
- Zhifeng Ning
-
Affiliations: Basic Medical School, Hubei University of Science and Technology, Xianning, Hubei 437100, P.R. China, Nurse School, Hubei University of Science and Technology, Xianning, Hubei 437100, P.R. China, Basic Medical School, Ji'nan University Medical School, Guangzhou, Guangdong 510632, P.R. China - Published online on: September 20, 2019 https://doi.org/10.3892/ol.2019.10900
- Pages: 5022-5032
-
Copyright: © Wu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ and He J: Cancer statistics in China 2015. Ca Cancer J Clin. 66:115–132. 2016. View Article : Google Scholar : PubMed/NCBI | |
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2018. CA Cancer J Clin. 68:7–30. 2018. View Article : Google Scholar : PubMed/NCBI | |
Huang Y, Qu S, Zhu G, Wang F, Liu R, Shen X, Viola D, Elisei R, Puxeddu E, Fugazzola L, et al: BRAF V600E mutation-assisted risk stratification of solitary intrathyroidal papillary thyroid cancer for precision treatment. J Natl Cancer Inst. 110:362–370. 2018. View Article : Google Scholar : PubMed/NCBI | |
Leonard KL and Wazer DE: Genomic assays and individualized treatment of ductal carcinoma in situ in the era of value-based cancer care. J Clin Oncol. 34:3953–2955. 2016. View Article : Google Scholar : PubMed/NCBI | |
Dos Santos M, Brachet PE, Chevreau C and Joly F: Impact of targeted therapies in metastatic renal cell carcinoma on patient-reported outcomes: Methodology of clinical trials and clinical benefit. Cancer Treat Rev. 53:53–60. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen DS and Mellman I: Elements of cancer immunity and the cancer-immune set point. Nature. 541:321–330. 2017. View Article : Google Scholar : PubMed/NCBI | |
Başaran GA, Twelves C, Diéras V, Cortés J and Awada A: Ongoing unmet needs in treating estrogen receptor-positive/HER2-negative metastatic breast cancer. Cancer Treat Rev. 63:144–155. 2018. View Article : Google Scholar : PubMed/NCBI | |
Bourke L, Kirkbride P, Hooper R, Rosario AJ, Chico TJ and Rosario DJ: Endocrine therapy in prostate cancer: Time for reappraisal of risks, benefits and cost-effectiveness? Br J Cancer. 108:9–13. 2013. View Article : Google Scholar : PubMed/NCBI | |
Han SH, Kim JW, Kim M, Kim JH, Lee KW, Kim BH, Oh HK, Kim DW, Kang SB, Kim H and Shin E: Prognostic implication of ABC transporters and cancer stem cell markers in patients with stage III colon cancer receiving adjuvant FOLFOX-4 chemotherapy. Oncol Lett. 17:5572–5580. 2019.PubMed/NCBI | |
Xu PP, Fu D, Li JY, Hu JD, Wang X, Zhou JF, Yu H, Zhao X, Huang YH, Jiang L, et al: Anthracycline dose optimisation in patients with diffuse large B-cell lymphoma: A multicentre, phase 3, randomised, controlled trial. Lancet Haematol. 6:e328–e337. 2019. View Article : Google Scholar : PubMed/NCBI | |
Rous P: The relations of embryonic tissue and tumor in mixed grafts. J Exp Med. 13:239–247. 1911. View Article : Google Scholar : PubMed/NCBI | |
Bonnet D and Dick JE: Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 3:730–737. 1997. View Article : Google Scholar : PubMed/NCBI | |
Dick JE and Tsvee L: Biology of normal and acute myeloid leukemia stem cells. Int J Hematol. 82:389–396. 2005. View Article : Google Scholar : PubMed/NCBI | |
Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV and Lyuba V: Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res. 10:R102008. View Article : Google Scholar : PubMed/NCBI | |
Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD and Dirks PB: Identification of human brain tumour initiating cells. Nature. 432:396–401. 2004. View Article : Google Scholar : PubMed/NCBI | |
Collins AT, Berry PA, Hyde C, Stower MJ and Maitland NJ: Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65:10946–10951. 2005. View Article : Google Scholar : PubMed/NCBI | |
Odoux C, Fohrer H, Hoppo T, Guzik L, Stolz DB, Lewis DW, Gollin SM, Gamblin TC, Geller DA and Lagasse E: A stochastic model for cancer stem cell origin in metastatic colon cancer. Cancer Research. 68:6932–6941. 2008. View Article : Google Scholar : PubMed/NCBI | |
Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, Richel DJ, Stassi G and Medema JP: Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA. 105:13427–13432. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zhang H, Hao C, Wang H, Shang H and Li Z: Carboxypeptidase A4 promotes proliferation and stem cell characteristics of hepatocellular carcinoma. Int J Exp Pathol. 100:133–138. 2019. View Article : Google Scholar : PubMed/NCBI | |
Li X, Zhang Y, Ding J, Wang M, Li N, Yang H, Wang K, Wang D, Lin PP, Li M, et al: Clinical significance of detecting CSF-derived tumor cells in breast cancer patients with leptomeningeal metastasis. Oncotarget. 9:2705–2714. 2017.PubMed/NCBI | |
Lin Y, Totsuka Y, He Y, Kikuchi S, Qiao Y, Ueda J, Wei W, Inoue M and Tanaka H: Epidemiology of esophageal cancer in Japan and China. J Epidemiol. 23:233–242. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 136:E359–E386. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lao-Sirieix P and Fitzgerald RC: Screening for oesophageal cancer. Nat Rev Clin Oncol. 9:278–287. 2012. View Article : Google Scholar : PubMed/NCBI | |
Pennathur A, Gibson MK, Jobe BA and Luketich JD: Oesophageal carcinoma. Lancet. 381:400–412. 2013. View Article : Google Scholar : PubMed/NCBI | |
Chen M, Liu P, Chen Y, Chen Z, Shen M, Liu X, Li X, Lin Y, Yang R, Ni W, et al: Primary tumor regression patterns in esophageal squamous cell cancer treated with definitive chemoradiotherapy and implications for surveillance schemes. Cancer Manag Res. 11:3361–3369. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vira D, Basak SK, Veena MS, Wang MB, Batra RK and Srivatsan ES: Cancer stem cells, microRNAs, and therapeutic strategies including natural products. Cancer Metastasis Rev. 31:733–751. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fu W, Lei C, Yu Y, Liu S, Li T, Lin F, Fan X, Shen Y, Ding M, Tang Y, et al: EGFR/Notch antagonists enhance the response to inhibitors of the PI3K-Akt pathway by decreasing tumour-initiating cell frequency. Clin Cancer Res. 25:2835–2847. 2019. View Article : Google Scholar : PubMed/NCBI | |
Jia ZF, Wu YH, Cao DH, Cao XY, Jiang J and Zhou BS: Polymorphisms of cancer stem cell marker gene CD133 are associated with susceptibility and prognosis of gastric cancer. Future Oncol. 13:979–989. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kalantari E, Asgari M, Nikpanah S, Salarieh N, Lari MH and Madjd Z: Co-expression of putative cancer stem cell markers CD44 and CD133 in prostate carcinomas. Pathol Oncol Res. 23:793–802. 2017. View Article : Google Scholar : PubMed/NCBI | |
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 100:3983–3988. 2003. View Article : Google Scholar : PubMed/NCBI | |
Yan Y, Zuo X and Wei D: Concise review: Emerging role of CD44 in cancer stem cells: A promising biomarker and therapeutic target. Stem Cells Transl Med. 4:1033–1043. 2015. View Article : Google Scholar : PubMed/NCBI | |
Liou GY: CD133 as a regulator of cancer metastasis through the cancer stem cells. Int J Biochem Cell Biol. 106:1–7. 2019. View Article : Google Scholar : PubMed/NCBI | |
Tang KH, Dai YD, Tong M, Chan YP, Kwan PS, Fu L, Qin YR, Tsao SW, Lung HL, Lung ML, et al: A CD90(+) tumor-initiating cell population with an aggressive signature and metastatic capacity in esophageal cancer. Cancer Res. 73:2322–2332. 2013. View Article : Google Scholar : PubMed/NCBI | |
Moreira MP, da Conceição Braga L and Silva LM: STAT3 as a promising chemoresistance biomarker associated with the CD44+/high/CD24-/low/ALDH+ BCSCs-like subset of the triple-negative breast cancer (TNBC) cell line. Exp Cell Res. 363:283–290. 2018. View Article : Google Scholar : PubMed/NCBI | |
Nguyen PH, Giraud J, Staedel C, Chambonnier L, Dubus P, Chevret E, Bœuf H, Gauthereau X, Rousseau B, Fevre M, et al: All-trans retinoic acid targets gastric cancer stem cells and inhibits patient-derived gastric carcinoma tumor growth. Oncogene. 35:5619–5628. 2016. View Article : Google Scholar : PubMed/NCBI | |
Erb HHH, Guggenberger F, Santer FR and Culig Z: Interleukin-4 induces a CD44high/CD49bhigh PC3 subpopulation with tumor-initiating characteristics. J Cell Biochem. 119:4103–4112. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ogawa T, Hirohashi Y, Murai A, Nishidate T, Okita K, Wang L, Ikehara Y, Satoyoshi T, Usui A, Kubo T, et al: ST6GALNAC1 plays important roles in enhancing cancer stem phenotypes of colorectal cancer via the Akt pathway. Oncotarget. 8:112550–112564. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang HH, Liao CC, Chow NH, Huang LL, Chuang JI, Wei KC and Shin JW: Whether CD44 is an applicable marker for glioma stem cells. Am J Transl Res. 9:4785–4806. 2017.PubMed/NCBI | |
Zhao JS, Li WJ, Ge D, Zhang PJ, Li JJ, Lu CL, Ji XD, Guan DX, Gao H, Xu LY, et al: Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One. 6:e214192011. View Article : Google Scholar : PubMed/NCBI | |
Matsuya Y: A serum-free culture medium for the minor inoculum of L line cells. Tohoku J Exp Med. 86:1–8. 1965. View Article : Google Scholar : PubMed/NCBI | |
Haylock DN, To LB, Dowse TL, Juttner CA and Simmons PJ: Ex vivo expansion and maturation of peripheral blood CD34+ cells into the myeloid lineage. Blood. 80:1405–1412. 1992.PubMed/NCBI | |
Petzer AL, Zandstra PW, Piret JM and Eaves CJ: Differential cytokine effects on primitive (CD34+CD38-) human hematopoietic cells: Novel responses to Flt3-ligand and thrombopoietin. J Exp Med. 183:2551–2558. 1996. View Article : Google Scholar : PubMed/NCBI | |
Möbest D, Goan SR, Junghahn I, Winkler J, Fichtner I, Hermann M, Becker M, de Lima-Hahn E and Henschler R: Differential kinetics of primitive hematopoietic cells assayed in vitro and in vivo during serum-free suspension culture of CD34+ blood progenitor cells. Stem Cells. 17:152–161. 1999. View Article : Google Scholar : PubMed/NCBI | |
Jimenez-Pascual A, Hale JS, Kordowski A, Pugh J, Silver DJ, Bayik D, Roversi G, Alban TJ, Rao S, Chen R, et al: ADAMDEC1 maintains a growth factor signaling loop in cancer stem cells. Cancer Discov. (pii): CD-18-1308. 2019.PubMed/NCBI | |
Abbaszadegan MR, Bagheri V, Razavi MS, Momtazi AA, Sahebkar A and Gholamin M: Isolation, identification and characterization of cancer stem cells: A review. J Cell Physiol. 232:2008–2018. 2017. View Article : Google Scholar : PubMed/NCBI | |
Xiao G, Li X, Li G, Zhang B, Xu C, Qin S, Du N, Wang J, Tang SC, Zhang J, et al: MiR-129 blocks estrogen induction of NOTCH signaling activity in breast cancer stem-like cells. Oncotarget. 8:103261–103273. 2017. View Article : Google Scholar : PubMed/NCBI | |
Trisciuoglio D, Tupone MG, Desideri M, Di Martile M, Gabellini C, Buglioni S, Pallocca M, Alessandrini G, D'Aguanno S and Del Bufalo D: BCL-XL overexpression promotes tumor progression-associated properties. Cell Death Dis. 8:32162017. View Article : Google Scholar : PubMed/NCBI | |
Wang JL, Yu JP, Sun ZQ and Sun SP: Radiobiological characteristics of cancer stem cells from esophageal cancer cell lines. World J Gastroenterol. 20:18296–18305. 2014. View Article : Google Scholar : PubMed/NCBI | |
Goodell MA, Rosenzweig M, Kim H, Marks DF, DeMaria M, Paradis G, Grupp SA, Sieff CA, Mulligan RC and Johnson RP: Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med. 3:1337–1345. 1997. View Article : Google Scholar : PubMed/NCBI | |
Parmar K, Sauk-Schubert C, Burdick D, Handley M and Mauch P: Sca+CD34- murine side population cells are highly enriched for primitive stem cells. Exp Hematol. 31:244–250. 2003. View Article : Google Scholar : PubMed/NCBI | |
Alvi AJ, Clayton H, Joshi C, Enver T, Ashworth A, Vivanco Md, Dale TC and Smalley MJ: Functional and molecular characterisation of mammary side population cells. Breast Cancer Research. 5:R1–R8. 2002. View Article : Google Scholar : PubMed/NCBI | |
Gross E, L'Faqihiolive FE, Ysebaert L, Brassac M, Struski S, Kheirallah S, Fournié JJ, Laurent G and Quillet-Mary A: B-chronic lymphocytic leukemia chemoresistance involves innate and acquired leukemic side population cells. Leukemia. 24:1885–1892. 2010. View Article : Google Scholar : PubMed/NCBI | |
Du J, Liu S, He J, Liu X, Qu Y, Yan W, Fan J, Li R, Xi H, Fu W, et al: MicroRNA-451 regulates stemness of side population cells via PI3K/Akt/mTOR signaling pathway in multiple myeloma. Oncotarget. 6:14993–15007. 2015. View Article : Google Scholar : PubMed/NCBI | |
Britton KM, Kirby JA, Lennard TW and Meeson AP: Cancer stem cells and side population cells in breast cancer and metastasis. Cancers. 3:2106–2130. 2011. View Article : Google Scholar : PubMed/NCBI | |
Macpherson H, Keir P, Webb S, Samuel K, Boyle S, Bickmore W, Forrester L and Dorin J: Bone marrow-derived SP cells can contribute to the respiratory tract of mice in vivo. J Cell Sci. 118:2441–2450. 2005. View Article : Google Scholar : PubMed/NCBI | |
Shimoda M, Ota M and Okada Y: Isolation of cancer stem cells by side population method. Methods Mol Biol. 1692:49–59. 2018. View Article : Google Scholar : PubMed/NCBI | |
Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K and Tang DG: Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2-cancer cells are similarly tumorigenic. Cancer Res. 65:6207–6019. 2005. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Komaki R, Wang L, Fang B and Chang JY: Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus. Clin Cancer Res. 14:2813–2823. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zhang G, Ma L, Xie YK, Miao XB and Jin C: Esophageal cancer tumorspheres involve cancer stem-like populations with elevated aldehyde dehydrogenase enzymatic activity. Mol Med Rep. 6:519–524. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yue Z, Qi B, Bettina S, Zhao L, Mysliwietz J, Ellwart J, Renner A, Hirner H, Niess H, Camaj P, et al: Stem cell-like side populations in esophageal cancer: A source of chemotherapy resistance and metastases. Stem Cells Dev. 23:180–192. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Xia Q, Jiang B, Chang W, Yuan W, Ma Z, Liu Z and Shu X: Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: A systematic review and meta-analysis. PLoS One. 10:e01451642015. View Article : Google Scholar : PubMed/NCBI | |
Zhou Y, Wang Y, Ju X, Lan J, Zou H, Li S, Qi Y, Jia W, Hu J, Liang W, et al: Clinicopathological significance of ALDH1A1 in lung, colorectal, and breast cancers: A meta-analysis. Biomark Med. 9:777–790. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ferrell CM, Dorsam ST, Ohta H, Humphries RK, Derynck MK, Haqq C, Largman C and Lawrence HJ: Activation of stem-cell specific genes by HOXA9 and HOXA10 homeodomain proteins in CD34+ human cord blood cells. Stem Cells. 23:644–655. 2010. View Article : Google Scholar | |
Seigel GM, Campbell LM, Narayan M and Gonzalez-Fernandez F: Cancer stem cell characteristics in retinoblastoma. Mol Vis. 11:729–737. 2005.PubMed/NCBI | |
Macdonagh L, Gallagher MF, Ffrench B, Gasch C, Breen E, Gray SG, Nicholson S, Leonard N, Ryan R, Young V, et al: Targeting the cancer stem cell marker, aldehyde dehydrogenase 1, to circumvent cisplatin resistance in NSCLC. Oncotarget. 8:72544–72563. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fu Z, Chen C, Zhou Q, Wang Y, Zhao Y, Zhao X, Li W, Zheng S, Ye H, Wang L, et al: LncRNA HOTTIP modulates cancer stem cell properties in human pancreatic cancer by regulating HOXA9. Cancer Lett. 410:68–81. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ji Y, Li X, Li Y, Zhong Y, Cao J, Xu R, Wang J, Zhou F, Li X, Yu D, et al: Aldehyde dehydrogenase-1 expression predicts unfavorable outcomes in patients with esophageal squamous cell carcinoma. Anticancer Res. 36:343–349. 2016.PubMed/NCBI | |
Song S, Ajani JA, Honjo S, Maru DM, Chen Q, Scott AW, Heallen TR, Xiao L, Hofstetter WL, Weston B, et al: Hippo coactivator YAP1 upregulates SOX9 and endows esophageal cancer cells with stem-like properties. Cancer Res. 74:4170–4182. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen MF, Chen PT, Lu MS and Chen WC: Role of ALDH1 in the prognosis of esophageal cancer and its relationship with tumor microenvironment. Mol Carcinog. 57:78–88. 2018. View Article : Google Scholar : PubMed/NCBI | |
Akbarzadeh M, Maroufi NF, Tazehkand AP, Akbarzadeh M, Bastani S, Safdari R, Farzane A, Fattahi A, Nejabati HR, Nouri M and Samadi N: Current approaches in identification and isolation of cancer stem cells. J Cell Physiol. Feb 11–2019.doi: 10.1002/jcp.28271 (Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Yang Z, Ni W, Cui C, Qi W, Piao L and Xuan Y: Identification of LETM1 as a marker of cancer stem-like cells and predictor of poor prognosis in esophageal squamous cell carcinoma. Hum Pathol. 81:148–156. 2018. View Article : Google Scholar : PubMed/NCBI | |
Liu Q, Cui X, Yu X, Bian BS, Qian F, Hu XG, Ji CD, Yang L, Ren Y, Cui W, et al: Cripto-1 acts as a functional marker of cancer stem-like cells and predicts prognosis of the patients in esophageal squamous cell carcinoma. Mol Cancer. 16:812017. View Article : Google Scholar : PubMed/NCBI | |
Cabrera MC, Hollingsworth RE and Hurt EM: Cancer stem cell plasticity and tumor hierarchy. World J Stem Cells. 7:27–36. 2015. View Article : Google Scholar : PubMed/NCBI | |
Almanaa TN, Geusz ME and Jamasbi RJ: A new method for identifying stem-like cells in esophageal cancer cell lines. J Cancer. 4:536–548. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ajani JA, Wang X, Song S, Suzuki A, Taketa T, Sudo K, Wadhwa R, Hofstetter WL, Komaki R, Maru DM, et al: ALDH-1 expression levels predict response or resistance to preoperative chemoradiation in resectable esophageal cancer patients. Mol Oncol. 8:142–149. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chang L, Graham P, Hao J, Ni J, Deng J, Bucci J, Malouf D, Gillatt D and Li Y: Cancer stem cells and signaling pathways in radioresistance. Oncotarget. 7:11002–11017. 2016.PubMed/NCBI | |
Lynam-Lennon N, Heavey S, Sommerville G, Bibby BA, Ffrench B, Quinn J, Gasch C, O'Leary JJ, Gallagher MF, Reynolds JV and Maher SG: MicroRNA-17 is downregulated in esophageal adenocarcinoma cancer stem-like cells and promotes a radioresistant phenotype. Oncotarget. 8:11400–11413. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen KH, Guo Y, Li L, Qu S, Zhao W, Lu QT, Mo QY, Yu BB, Zhou L, Lin GX, et al: Cancer stem cell-like characteristics and telomerase activity of the nasopharyngeal carcinoma radioresistant cell line CNE-2R. Cancer Med. 7:4755–4764. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Jiang T, Mao A and Xu J: Esophageal cancer stem cells express PLGF to increase cancer invasion through MMP9 activation. Tumour Biol. 35:12749–12755. 2014. View Article : Google Scholar : PubMed/NCBI | |
Tsai ST, Wang PJ, Liou NJ, Lin PS, Chen CH and Chang WC: ICAM1 is a potential cancer stem cell marker of esophageal squamous cell carcinoma. PLoS One. 10:e01428342015. View Article : Google Scholar : PubMed/NCBI | |
Sauzay C, Voutetakis K, Chatziioannou A, Chevet E and Avril T: CD90/Thy-1, a cancer-associated cell surface signaling molecule. Front Cell Dev Biol. 7:662019. View Article : Google Scholar : PubMed/NCBI | |
Ji N, Yu JW, Ni XC, Wu JG, Wang SL and Jiang BJ: Bone marrow-derived mesenchymal stem cells increase drug resistance in CD133-expressing gastric cancer cells by regulating the PI3K/AKT pathway. Tumor Biol. 37:14637–14651. 2016. View Article : Google Scholar | |
Fan H and Lu S: Fusion of human bone hemopoietic stem cell with esophageal carcinoma cells didn't generate esophageal cancer stem cell. Neoplasma. 61:540–545. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mo JS, Park HW and Guan KL: The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep. 15:642–656. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sharon N, Vanderhooft J, Straubhaar J, Mueller J, Chawla R, Zhou Q, Engquist EN, Trapnell C, Gifford DK and Melton DA: Wnt signaling separates the progenitor and endocrine compartments during pancreas development. Cell Rep. 27:2281–2291.e5. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ma L, Wang Y, Hui Y, Du Y, Chen Z, Feng H, Zhang S, Li N, Song J, Fang Y, et al: WNT/NOTCH pathway is essential for the maintenance and expansion of human MGE progenitors. Stem Cell Reports. 12:934–949. 2019. View Article : Google Scholar : PubMed/NCBI | |
Huynh DL, Koh H, Chandimali N, Zhang JJ, Kim N, Kang TY, Ghosh M, Gera M, Park YH, Kwon T and Jeong DK: BRM270 inhibits the proliferation of CD44 positive pancreatic ductal adenocarcinoma cells via downregulation of sonic hedgehog signaling. Evid Based Complement Alternat Med. 2019:86204692019. View Article : Google Scholar : PubMed/NCBI | |
Che SM, Zhang XZ, Liu XL, Chen X and Hou L: The radiosensitization effect of NS398 on esophageal cancer stem cell-like radioresistant cells. Dis Esophagus. 24:265–273. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yue D, Zhang Z, Li J, Chen X, Ping Y, Liu S, Shi X, Li L, Wang L, Huang L, et al: Transforming growth factor-beta1 promotes the migration and invasion of sphere-forming stem-like cell subpopulations in esophageal cancer. Exp Cell Res. 336:141–149. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ding W, Mouzaki M, You H, Laird JC, Mato J, Lu SC and Rountree CB: CD133+ liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-beta-induced apoptosis. Hepatology. 49:1277–1286. 2009. View Article : Google Scholar : PubMed/NCBI | |
Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, Watanabe M, Beppu T, Tamada M, Nagano O, et al: CD44s regulates the TGF-β-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res. 72:3414–3423. 2012. View Article : Google Scholar : PubMed/NCBI | |
Mitra M, Kandalam M, Harilal A, Verma RS, Krishnan UM, Swaminathan S and Krishnakumar S: EpCAM is a putative stem marker in retinoblastoma and an effective target for T-cell-mediated immunotherapy. Mol Vis. 18:290–308. 2012.PubMed/NCBI | |
Zhang M, Tan S, Yu D, Zhao Z, Zhang B, Zhang P, Lv C, Zhou Q and Cao Z: Triptonide inhibits lung cancer cell tumorigenicity by selectively attenuating the Shh-Gli1 signaling pathway. Toxicol Appl Pharmacol. 365:1–8. 2019. View Article : Google Scholar : PubMed/NCBI | |
Arai MA, Ochi F, Makita Y, Chiba T, Higashi K, Suganami A, Tamura Y, Toida T, Iwama A, Sadhu SK, et al: GLI1 inhibitors identified by target protein oriented natural products isolation (TPO-NAPI) with hedgehog inhibition. ACS Chem Biol. 13:2551–2559. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yang Z, Cui Y, Ni W, Kim S and Xuan Y: Gli1, a potential regulator of esophageal cancer stem cell, is identified as an independent adverse prognostic factor in esophageal squamous cell carcinoma. J Cancer Res Clin Oncol. 143:243–254. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fujiwara D, Kato K, Nohara S, Iwanuma Y and Kajiyama Y: The usefulness of three-dimensional cell culture in induction of cancer stem cells from esophageal squamous cell carcinoma cell lines. Biochem Biophys Res Commun. 434:773–778. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kanamoto A, Ninomiya I, Harada S, Tsukada T, Okamoto K, Nakanuma S, Sakai S, Makino I, Kinoshita J, Hayashi H, et al: Valproic acid inhibits irradiation-induced epithelial-mesenchymal transition and stem cell-like characteristics in esophageal squamous cell carcinoma. Int J Oncol. 49:1859–1869. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang JX, Chen ZH, Xu Y, Chen JW, Weng HW, Yun M, Zheng ZS, Chen C, Wu BL, Li EM, et al: Downregulation of MicroRNA-644a promotes esophageal squamous cell carcinoma aggressiveness and stem-cell-like phenotype via dysregulation of PITX2. Clin Cancer Res. 23:298–310. 2017. View Article : Google Scholar : PubMed/NCBI | |
De Luca M, Aiuti A, Cossu G, Parmar M, Pellegrini G and Robey PG: Advances in stem cell research and therapeutic development. Nat Cell Biol. 21:801–811. 2019. View Article : Google Scholar : PubMed/NCBI | |
Reya T, Morrison SJ, Clarke MF and Weissman IL: Stem cells, cancer, and cancer stem cells. Nature. 414:105–111. 2001. View Article : Google Scholar : PubMed/NCBI | |
de Sousa EM, Vermeulen L, Richel D and Medema JP: Targeting Wnt signaling in colon cancer stem cells. Clin Cancer Res. 17:647–653. 2011. View Article : Google Scholar : PubMed/NCBI | |
Merchant AA and William M: Targeting Hedgehog-a cancer stem cell pathway. Clin Cancer Res. 16:3130–3140. 2010. View Article : Google Scholar : PubMed/NCBI | |
Galoczova M, Coates P and Vojtesek B: STAT3, stem cells, cancer stem cells and p63. Cell Mol Biol Lett. 23:122018. View Article : Google Scholar : PubMed/NCBI | |
Fu J and Wang H: Precision diagnosis and treatment of liver cancer in China. Cancer Lett. 412:283–288. 2017. View Article : Google Scholar : PubMed/NCBI | |
Irwin CR, Hitt MM and Evans DH: Targeting nucleotide biosynthesis: A strategy for improving the oncolytic potential of DNA viruses. Front Oncol. 7:2292017. View Article : Google Scholar : PubMed/NCBI | |
Pandey S and Robertson ES: Oncogenic Epstein-Barr virus recruits Nm23-H1 to regulate chromatin modifiers. Lab Invest. 98:258–268. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lin TA, Garden AS, Elhalawani H, Elgohari B, Jethanandani A, Ng SP, Mohamed AS, Frank SJ, Glisson BS, Debnam JM, et al: Radiographic retropharyngeal lymph node involvement in human papillomavirus-associated oropharyngeal carcinoma: Patterns of involvement and impact on patient outcomes. Cancer. 125:1536–1546. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wang D, Plukker JTM and Coppes RP: Cancer stem cells with increased metastatic potential as a therapeutic target for esophageal cancer. Semin Cancer Biol. 44:60–66. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hirai M, Kelsey LS, Vaillancourt M, Maneval DC, Watanabe T and Talmadge JE: Purging of human breast cancer cells from stem cell products with an adenovirus containing p53. Cancer Gene Ther. 7:197–206. 2000. View Article : Google Scholar : PubMed/NCBI | |
Eriksson M, Guse K, Bauerschmitz G, Virkkunen P, Tarkkanen M, Tanner M, Hakkarainen T, Kanerva A, Desmond RA, Pesonen S and Hemminki A: Oncolytic adenoviruses kill breast cancer initiating CD44+CD24-/low cells. Mol Ther. 15:2088–2093. 2007. View Article : Google Scholar : PubMed/NCBI | |
Cho RW, Wang X, Diehn M, Shedden K, Chen GY, Sherlock G, Gurney A, Lewicki J and Clarke MF: Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells. 26:364–371. 2010. View Article : Google Scholar | |
Mui UN, Haley CT and Tyring SK: Viral oncology: Molecular biology and pathogenesis. J Clin Med. 6(pii): 1112017. View Article : Google Scholar | |
Ali SM, Ross JS and Wang K: Reply to Genomic profiles of nasopharyngeal carcinoma: The importance of histological subtyping and Epstein-Barr virus in situ assays. Cancer. 124:435–436. 2018. View Article : Google Scholar : PubMed/NCBI | |
Satoru K, Naohiro W, Masamichi M, Zen Y, Endo K, Murono S, Sugimoto H, Yamaoka S, Pagano JS and Yoshizaki T: Epstein-Barr virus latent membrane protein 1 induces cancer stem/progenitor-like cells in nasopharyngeal epithelial cell lines. J Virol. 85:11255–11264. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chris C, Figueroa JA, Leonardo M, Colombo M, Summers G, Figueroa A, Aulakh A, Konala V, Verma R, Riaz J, et al: The role of human papilloma virus (HPV) infection in non-anogenital cancer and the promise of immunotherapy: A review. Int Rev Immunol. 33:383–401. 2014. View Article : Google Scholar : PubMed/NCBI | |
Swanson MS, Kokot N and Sinha UK: The role of HPV in head and neck cancer stem cell formation and tumorigenesis. Cancers (Basel). 8(pii): E242016. View Article : Google Scholar : PubMed/NCBI | |
Ortiz-Sánchez E, Santiago-López L, Cruz-Domínguez VB, Toledo-Guzmán ME, Hernández-Cueto D, Muñiz-Hernández S, Garrido E, Cantú De León D and García-Carrancá A: Characterization of cervical cancer stem cell-like cells: Phenotyping, stemness, and human papilloma virus co-receptor expression. Oncotarget. 7:31943–31954. 2016. View Article : Google Scholar : PubMed/NCBI | |
Lanfredini S, Olivero C, Borgogna C, Calati F, Powell K, Davies KJ, De Andrea M, Harries S, Tang HKC, Pfister H, et al: HPV8 field cancerization in a transgenic mouse model is due to Lrig1+ keratinocyte stem cell expansion. J Invest Dermatol. 137:2208–2216. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang M, Kumar B, Piao L, Xie X, Schmitt A, Arradaza N, Cippola M, Old M, Agrawal A, Ozer E, et al: Elevated intrinsic cancer stem cell population in human papillomavirus-associated head and neck squamous cell carcinoma. Cancer. 120:992–1001. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zhang M, Zhuang G, Sun X, Shen Y, Wang W, Li Q and Di W: TP53 mutation-mediated genomic instability induces the evolution of chemoresistance and recurrence in epithelial ovarian cancer. Diagn Pathol. 12:162017. View Article : Google Scholar : PubMed/NCBI | |
Chiche A, Moumen M, Romagnoli M, Petit V, Lasla H, Jézéquel P, de la Grange P, Jonkers J, Deugnier MA, Glukhova MA and Faraldo MM: p53 deficiency induces cancer stem cell pool expansion in a mouse model of triple-negative breast tumors. Oncogene. 36:2355–2365. 2016. View Article : Google Scholar : PubMed/NCBI | |
Shetzer Y, Molchadsky A and Rotter V: Oncogenic mutant p53 gain of function nourishes the vicious cycle of tumor development and cancer stem-cell formation. Cold Spring Harb Perspect Med. 6(pii): a0262032016. View Article : Google Scholar : PubMed/NCBI | |
Tan MJ, White EA, Sowa ME, Harper JW, Aster JC and Howley PM: Cutaneous β-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling. Proc Natl Acad Sci USA. 109:E1473–E1480. 2012. View Article : Google Scholar : PubMed/NCBI | |
Shamir ER, Devine WP, Pekmezci M, Umetsu SE, Krings G, Federman S, Cho SJ, Saunders TA, Jen KY, Bergsland E, et al: Identification of high-risk human papillomavirus and Rb/E2F pathway genomic alterations in mutually exclusive subsets of colorectal neuroendocrine carcinoma. Mod Pathol. 32:290–305. 2019. View Article : Google Scholar : PubMed/NCBI | |
Dyson N, Howley PM, Münger K and Harlow E: The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science. 243:934–937. 1989. View Article : Google Scholar : PubMed/NCBI | |
Shanmugarajah R, Bin W, Snow ET, Sharma P, Pavey D, Merrett N, Ball MJ, Brain T, Fernando R and Robertson IK: Transcriptionally active human papillomavirus is strongly associated with Barrett's dysplasia and esophageal adenocarcinoma. Am J Gastroenterol. 108:1082–1093. 2013. View Article : Google Scholar : PubMed/NCBI | |
Anders M, Rösch T, Küster K, Becker I, Höfler H, Stein HJ, Meining A, Wiedenmann B and Sarbia M: Expression and function of the coxsackie and adenovirus receptor in Barrett's esophagus and associated neoplasia. Cancer Gene Ther. 16:508–515. 2009. View Article : Google Scholar : PubMed/NCBI | |
Chang F, Syrjänen S, Wang L and Syrjänen K: Infectious agents in the etiology of esophageal cancer. Gastroenterology. 103:1336–1348. 1992. View Article : Google Scholar : PubMed/NCBI | |
Chang F, Syrjänen S, Shen Q, Ji HX and Syrjänen K: Human papillomavirus (HPV) DNA in esophageal precancer lesions and squamous cell carcinomas from China. Int J Cancer. 45:21–25. 1990. View Article : Google Scholar : PubMed/NCBI | |
He Z, Xu Z, Hang D, Guo F, Abliz A, Weiss NS, Xi L, Liu F, Ning T, Pan Y, et al: Anti-HPV-E7 seropositivity and risk of esophageal squamous cell carcinoma in a high-risk population in China. Carcinogenesis. 35:816–821. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang L, Li J, Hou J, Li M, Cui X, Li S, Yu X, Zhang Z, Liang W, Jiang J, et al: p53 expression but not p16(INK4A) correlates with human papillomavirus-associated esophageal squamous cell carcinoma in Kazakh population. Infect Agent Cancer. 11:192016. View Article : Google Scholar : PubMed/NCBI | |
Ludmir EB, Stephens SJ, Palta M, Willett CG and Czito BG: Human papillomavirus tumor infection in esophageal squamous cell carcinoma. J Gastrointest Oncol. 6:287–295. 2015.PubMed/NCBI | |
Xi R, Pan S, Chen X, Hui B, Zhang L, Fu S, Li X, Zhang X, Gong T, Guo J, et al: HPV16 E6-E7 induces cancer stem-like cells phenotypes in esophageal squamous cell carcinoma through the activation of PI3K/Akt signaling pathway in vitro and in vivo. Oncotarget. 7:57050–57065. 2016. View Article : Google Scholar : PubMed/NCBI | |
Syrjänen KJ: HPV infections and oesophageal cancer. J Clin Pathol. 55:721–728. 2002. View Article : Google Scholar : PubMed/NCBI | |
Halec G, Schmitt M, Egger S, Abnet CC, Babb C, Dawsey SM, Flechtenmacher C, Gheit T, Hale M, Holzinger D, et al: Mucosal alpha-papillomaviruses are not associated with esophageal squamous cell carcinomas: Lack of mechanistic evidence from South Africa, China and Iran and from a world-wide meta-analysis. Int J Cancer. 139:85–98. 2016. View Article : Google Scholar : PubMed/NCBI | |
Yang L, Ji Y, Chen L, Li M, Wu F, Hu J, Jiang J, Cui X, Chen Y, Pang L, et al: Genetic variability in LMP2 and LMP7 is associated with the risk of esophageal squamous cell carcinoma in the Kazakh population but is not associated with HPV infection. PLoS One. 12:e01863192017. View Article : Google Scholar : PubMed/NCBI | |
da Costa AM, Fregnani JHTG, Pastrez PRA, Mariano VS, Silva EM, Neto CS, Guimarães DP, Villa LL, Sichero L, Syrjanen KJ and Longatto-Filho A: HPV infection and p53 and p16 expression in esophageal cancer: are they prognostic factors? Infect Agent Cancer. 12:542017. View Article : Google Scholar : PubMed/NCBI | |
Kayamba V, Bateman AC, Asombang AW, Shibemba A, Zyambo K, Banda T, Soko R and Kelly P: S HIV infection and domestic smoke exposure, but not human papilloma virus, are risk factors for oesophageal squamous cell carcinoma in Zambia: A case-control study. Cancer Med. 4:588–595. 2015. View Article : Google Scholar : PubMed/NCBI |