Early detection of tumor cells in bone marrow and peripheral blood in a fast‑progressing gastric cancer model
- Authors:
- Prerna Bali
- Ivonne Lozano‑Pope
- Collin Pachow
- Marygorret Obonyo
-
Affiliations: Department of Medicine, School of Medicine, University of California, San Diego, La Jolla, CA 92093‑0640, USA - Published online on: January 12, 2021 https://doi.org/10.3892/ijo.2021.5171
- Pages: 388-396
This article is mentioned in:
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|
Torre LA, Siegel RL, Ward EM and Jemal A: Global cancer incidence and mortality rates and trends-an update. Cancer Epidemiol Biomarkers Prev. 25:16–27. 2016. View Article : Google Scholar | |
|
Bessede E, Dubus P, Megraud F and Varon C: Helicobacter pylori infection and stem cells at the origin of gastric cancer. Oncogene. 34:2547–2555. 2015. View Article : Google Scholar | |
|
Bessède E, Staedel C, Acuña Amador LA, Nguyen PH, Chambonnier L, Hatakeyama M, Belleannée G, Mégraud F and Varon C: Helicobacter pylori generates cells with cancer stem cell properties via epithelial-mesenchymal transition-like changes. Oncogene. 33:4123–4131. 2014. View Article : Google Scholar | |
|
Herrero R, Park JY and Forman D: The fight against gastric cancer-the IARC Working Group report. Best Pract Res Clin Gastroenterol. 28:1107–1114. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wang H, Stoecklein NH, Lin PP and Gires O: Circulating and disseminated tumor cells: Diagnostic tools and therapeutic targets in motion. Oncotarget. 8:1884–1912. 2017. View Article : Google Scholar : | |
|
Alix-Panabieres C, Riethdorf S and Pantel K: Circulating tumor cells and bone marrow micrometastasis. Clin Cancer Res. 14:5013–5021. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Joosse SA, Gorges TM and Pantel K: Biology, detection, and clinical implications of circulating tumor cells. EMBO Mol Med. 7:1–11. 2015. View Article : Google Scholar : | |
|
Lin H, Balic M, Zheng S, Datar R and Cote RJ: Disseminated and circulating tumor cells: Role in effective cancer management. Crit Rev Oncol Hematol. 77:1–11. 2011. View Article : Google Scholar | |
|
Riethdorf S, Wikman H and Pantel K: Review: Biological relevance of disseminated tumor cells in cancer patients. Int J Cancer. 123:1991–2006. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Messaritakis I, Politaki E, Kotsakis A, Dermitzaki EK, Koinis F, Lagoudaki E, Koutsopoulos A, Kallergi G, Souglakos J and Georgoulias V: Phenotypic characterization of circulating tumor cells in the peripheral blood of patients with small cell lung cancer. PLoS One. 12:e01812112017. View Article : Google Scholar : PubMed/NCBI | |
|
Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW and Hayes DF: Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 351:781–791. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Tinhofer I, Saki M, Niehr F, Keilholz U and Budach V: Cancer stem cell characteristics of circulating tumor cells. Int J Radiat Biol. 90:622–627. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wülfing P, Borchard J, Buerger H, Heidl S, Zänker KS, Kiesel L and Brandt B: HER2-positive circulating tumor cells indicate poor clinical outcome in stage I to III breast cancer patients. Clin Cancer Res. 12:1715–1720. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Dong Y, Skelley AM, Merdek KD, Sprott KM, Jiang C, Pierceall WE, Lin J, Stocum M, Carney WP and Smirnov DA: Microfluidics and circulating tumor cells. J Mol Diagn. 15:149–157. 2013. View Article : Google Scholar | |
|
Cohen SJ, Punt CJ, Iannotti N, Saidman BH, Sabbath KD, Gabrail NY, Picus J, Morse M, Mitchell E, Miller MC, et al: Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol. 26:3213–3221. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Miller MC, Doyle GV and Terstappen LW: Significance of circulating tumor cells detected by the cellsearch system in patients with metastatic breast colorectal and prostate cancer. J Oncol. 2010:6174212010. View Article : Google Scholar | |
|
Riethdorf S, Fritsche H, Müller V, Rau T, Schindlbeck C, Rack B, Janni W, Coith C, Beck K, Jänicke F, et al: Significance of circulating tumor cells detected by the cellsearch system in patients with metastatic breast colorectal and prostate cancer. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: A validation study of the CellSearch system. Clin Cancer Res. 13:920–928. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Yang C, Zou K, Yuan Z, Guo T and Xiong B: Prognostic value of circulating tumor cells detected with the CellSearch system in patients with gastric cancer: Evidence from a meta-analysis. Onco Targets Ther. 11:1013–1023. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Soltani S, Mokarian F and Panjehpour M: The expression of CK-19 gene in circulating tumor cells of blood samples of metastatic breast cancer women. Res Pharm Sci. 10:485–496. 2015. | |
|
Andergassen U, Kolbl AC, Hutter S, Friese K and Jeschke U: Detection of circulating tumour cells from blood of breast cancer patients via RT-qPCR. Cancers (Basel). 5:1212–1220. 2013. View Article : Google Scholar | |
|
Zhao S, Yang H, Zhang M, Zhang D, Liu Y, Liu Y, Song Y, Zhang X, Li H, Ma W and Zhang Q: Circulating tumor cells (CTCs) detected by triple-marker EpCAM, CK19, and hMAM RT-PCR and their relation to clinical outcome in metastatic breast cancer patients. Cell Biochem Biophys. 65:263–273. 2013. View Article : Google Scholar | |
|
Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R and Kasimir-Bauer S: Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 11:R462009. View Article : Google Scholar : PubMed/NCBI | |
|
Grover PK, Cummins AG, Price TJ, Roberts-Thomson IC and Hardingham JE: Circulating tumour cells: The evolving concept and the inadequacy of their enrichment by EpCAM-based meth-odology for basic and clinical cancer research. Ann Oncol. 25:1506–1516. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Iinuma H, Watanabe T, Mimori K, Adachi M, Hayashi N, Tamura J, Matsuda K, Fukushima R, Okinaga K, Sasako M and Mori M: Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes' stage B and C colorectal cancer. J Clin Oncol. 29:1547–1555. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Kasimir-Bauer S, Hoffmann O, Wallwiener D, Kimmig R and Fehm T: Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res. 14:R152012. View Article : Google Scholar : PubMed/NCBI | |
|
Sun YF, Xu Y, Yang XR, Guo W, Zhang X, Qiu SJ, Shi RY, Hu B, Zhou J and Fan J: Circulating stem cell-like epithelial cell adhesion molecule-positive tumor cells indicate poor prognosis of hepatocellular carcinoma after curative resection. Hepatology. 57:1458–1468. 2013. View Article : Google Scholar | |
|
Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, et al: Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 339:580–584. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Moreno-Bueno G, Portillo F and Cano A: Transcriptional regulation of cell polarity in EMT and cancer. Oncogene. 27:6958–6969. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest. 119:1420–1428. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Singhal A, Deymier-Black AC, Almer JD and Dunand DC: Effect of high-energy X-ray doses on bone elastic properties and residual strains. J Mech Behav Biomed Mater. 4:1774–1786. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Eckert MA, Lwin TM, Chang AT, Kim J, Danis E, Ohno-Machado L and Yang J: Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell. 19:372–386. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Christie MJ, Bridge S, James LB and Beart PM: Excitotoxin lesions suggest an aspartatergic projection from rat medial prefrontal cortex to ventral tegmental area. Brain Res. 333:169–172. 1985. View Article : Google Scholar : PubMed/NCBI | |
|
Valcourt U, Carthy J, Okita Y, Alcaraz L, Kato M, Thuault S, Bartholin L and Moustakas A: Analysis of epithelial-mesenchymal transition induced by transforming growth factor β. Methods Mol Biol. 1344:147–181. 2016. View Article : Google Scholar | |
|
Cristescu R, Lee J, Nebozhyn M, Kim KM, Ting JC, Wong SS, Liu J, Yue YG, Wang J, Yu K, et al: Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat Med. 21:449–456. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Liu AN, Zhu ZH, Chang SJ and Hang XS: Twist expression associated with the epithelial-mesenchymal transition in gastric cancer. Mol Cell Biochem. 367:195–203. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Shioiri M, Shida T, Koda K, Oda K, Seike K, Nishimura M, Takano S and Miyazaki M: Slug expression is an independent prognostic parameter for poor survival in colorectal carcinoma patients. Br J Cancer. 94:1816–1822. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Uchikado Y, Natsugoe S, Okumura H, Setoyama T, Matsumoto M, Ishigami S and Aikou T: Slug Expression in the E-cadherin preserved tumors is related to prognosis in patients with esophageal squamous cell carcinoma. Clin Cancer Res. 11:1174–1180. 2005.PubMed/NCBI | |
|
Castro Alves C, Rosivatz E, Schott C, Hollweck R, Becker I, Sarbia M, Carneiro F and Becker KF: Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the down-regulation of E-cadherin. J Pathol. 211:507–515. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kim MA, Lee HS, Lee HE, Kim JH, Yang HK and Kim WH: Prognostic importance of epithelial-mesenchymal transition-related protein expression in gastric carcinoma. Histopathology. 54:442–451. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Yu Z, Pestell TG, Lisanti MP and Pestell RG: Cancer stem cells. Int J Biochem Cell Biol. 44:2144–2151. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Banerjee A, Thamphiwatana S, Carmona EM, Rickman B, Doran KS and Obonyo M: Deficiency of the myeloid differentiation primary response molecule MyD88 leads to an early and rapid development of Helicobacter-induced gastric malignancy. Infect Immun. 82:356–363. 2014. View Article : Google Scholar : | |
|
Lozano-Pope I, Sharma A, Matthias M, Doran KS and Obonyo M: Effect of myeloid differentiation primary response gene 88 on expression profiles of genes during the development and progression of Helicobacter-induced gastric cancer. BMC Cancer. 17:1332017. View Article : Google Scholar : PubMed/NCBI | |
|
Obonyo M, Rickman B and Guiney DG: Effects of myeloid differentiation primary response gene 88 (MyD88) activation on Helicobacter infection in vivo and induction of a Th17 response. Helicobacter. 16:398–404. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Obonyo M, Sabet M, Cole SP, Ebmeyer J, Uematsu S, Akira S and Guiney DG: Deficiencies of myeloid differentiation factor 88, Toll-like receptor 2 (TLR2), or TLR4 produce specific defects in macrophage cytokine secretion induced by Helicobacter pylori. Infect Immun. 75:2408–2414. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Obonyo M, Cole SP, Datta SK and Guiney DG: Evidence for interleukin-1-independent stimulation of interleukin-12 and down-regulation by interleukin-10 in Helicobacter pylori-infected murine dendritic cells deficient in the interleukin-1 receptor. FEMS Immunol Med Microbiol. 47:414–419. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Thamphiwatana S, Gao W, Obonyo M and Zhang L: In vivo treatment of Helicobacter pylori infection with liposomal lino-lenic acid reduces colonization and ameliorates inflammation. Proc Natl Acad Sci USA. 111:17600–17605. 2014. View Article : Google Scholar | |
|
Edling CE and Hallberg B: c-Kit-a hematopoietic cell essential receptor tyrosine kinase. Int J Biochem Cell Biol. 39:1995–1998. 2007. View Article : Google Scholar | |
|
Escribano L, Ocqueteau M, Almeida J, Orfao A and San Miguel JF: Expression of the c-kit (CD117) molecule in normal and malignant hematopoiesis. Leuk Lymphoma. 30:459–466. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Wang B, Chen Q, Cao Y, Ma X, Yin C, Jia Y, Zang A and Fan W: LGR5 is a gastric cancer stem cell marker associated with stemness and the EMT signature genes NANOG, NANOGP8, PRRX1, TWIST1, and BMI1. PLoS One. 11:e01689042016. View Article : Google Scholar : PubMed/NCBI | |
|
Hoffmann W: Current status on stem cells and cancers of the gastric epithelium. Int J Mol Sci. 16:19153–19169. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, Gordon SA, Shimada Y and Wang TC: Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 27:1006–1020. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Braun S and Naume B: Circulating and disseminated tumor cells. J Clin Oncol. 23:1623–1626. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Dardaei L, Shahsavani R, Ghavamzadeh A, Behmanesh M, Aslankoohi E, Alimoghaddam K and Ghaffari SH: The detection of disseminated tumor cells in bone marrow and peripheral blood of gastric cancer patients by multimarker (CEA, CK20, TFF1 and MUC2) quantitative real-time PCR. Clin Biochem. 44:325–330. 2011. View Article : Google Scholar | |
|
Moll R, Divo M and Langbein L: The human keratins: Biology and pathology. Histochem Cell Biol. 129:705–733. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Tuffaha MSA, Guski H and Kristiansen G: Immunohistochemistry in Tumor Diagnostics. Springer; Cham, New York, NY: pp. 49–58. 2018, View Article : Google Scholar | |
|
Guang W, Czinn SJ, Blanchard TG, Kim KC and Lillehoj EP: Genetic regulation of MUC1 expression by Helicobacter pylori in gastric cancer cells. Biochem Biophys Res Commun. 445:145–150. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ng GZ, Menheniott TR, Every AL, Stent A, Judd LM, Chionh YT, Dhar P, Komen JC, Giraud AS, Wang TC, et al: The MUC1 mucin protects against Helicobacter pylori pathogenesis in mice by regulation of the NLRP3 inflammasome. Gut. 65:1087–1099. 2016. View Article : Google Scholar | |
|
Linden SK, Sheng YH, Every AL, Miles KM, Skoog EC, Florin TH, Sutton P and McGuckin MA: MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog. 5:e10006172009. View Article : Google Scholar : PubMed/NCBI | |
|
McGuckin MA, Every AL, Skene CD, Linden SK, Chionh YT, Swierczak A, McAuley J, Harbour S, Kaparakis M, Ferrero R and Sutton P: Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis. Gastroenterology. 133:1210–1218. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kharbanda A, Rajabi H, Jin C, Tchaicha J, Kikuchi E, Wong KK and Kufe D: Targeting the oncogenic MUC1-C protein inhibits mutant EGFR-mediated signaling and survival in non-small cell lung cancer cells. Clin Cancer Res. 20:5423–5434. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ross JS and Slodkowska EA: Circulating and disseminated tumor cells in the management of breast cancer. Am J Clin Pathol. 132:237–245. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Kodack DP, Farago AF, Dastur A, Held MA, Dardaei L, Friboulet L, von Flotow F, Damon LJ, Lee D, Parks M, et al: Primary patient-derived cancer cells and their potential for personalized cancer patient care. Cell Rep. 21:3298–3309. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Lee HS, Lee HK, Kim HS, Yang HK, Kim YI and Kim WH: MUC1, MUC2, MUC5AC, and MUC6 expressions in gastric carcinomas: Their roles as prognostic indicators. Cancer. 92:1427–1434. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang HK, Zhang QM, Zhao TH, Li YY and Yi YF: Expression of mucins and E-cadherin in gastric carcinoma and their clinical significance. World J Gastroenterol. 10:3044–3047. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
von Mensdorff-Pouilly S, Snijdewint FG, Verstraeten AA, Verheijen RH and Kenemans P: Human MUC1 mucin: A multi-faceted glycoprotein. Int J Biol Markers. 15:343–356. 2000. View Article : Google Scholar | |
|
Deng M, Qin Y, Chen X, Wang Q and Wang J: MiR-206 inhibits proliferation, migration, and invasion of gastric cancer cells by targeting the MUC1 gene. Onco Targets Ther. 12:849–859. 2019. View Article : Google Scholar : | |
|
Gnemmi V, Bouillez A, Gaudelot K, Hémon B, Ringot B, Pottier N, Glowacki F, Villers A, Vindrieux D, Cauffiez C, et al: MUC1 drives epithelial-mesenchymal transition in renal carcinoma through Wnt/β-catenin pathway and interaction with SNAIL promoter. Cancer Lett. 346:225–236. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Nieto MA, Huang RY, Jackson RA and Thiery JP: EMT: 2016. Cell. 166:21–45. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Lamouille S, Xu J and Derynck R: Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 15:178–196. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Jung H, Kim B, Moon BI and Oh ES: Cytokeratin 18 is necessary for initiation of TGF-β1-induced epithelial-mesenchymal transition in breast epithelial cells. Mol Cell Biochem. 423:21–28. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Okabe H, Ishimoto T, Mima K, Nakagawa S, Hayashi H, Kuroki H, Imai K, Nitta H, Saito S, Hashimoto D, et al: CD44s signals the acquisition of the mesenchymal phenotype required for anchorage-independent cell survival in hepatocellular carcinoma. Br J Cancer. 110:958–966. 2014. View Article : Google Scholar : | |
|
Satelli A, Brownlee Z, Mitra A, Meng QH and Li S: Circulating tumor cell enumeration with a combination of epithelial cell adhesion molecule- and cell-surface vimentin-based methods for monitoring breast cancer therapeutic response. Clin Chem. 61:259–266. 2015. View Article : Google Scholar | |
|
Dvorak HF: Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med. 315:1650–1659. 1986. View Article : Google Scholar : PubMed/NCBI | |
|
Kletukhina S, Neustroeva O, James V, Rizvanov A and Gomzikova M: Role of mesenchymal stem cell-derived extracellular vesicles in epithelial-mesenchymal transition. Int J Mol Sci. 20:48132019. View Article : Google Scholar | |
|
Rattigan Y, Hsu JM, Mishra PJ, Glod J and Banerjee D: Interleukin 6 mediated recruitment of mesenchymal stem cells to the hypoxic tumor milieu. Exp Cell Res. 316:3417–3424. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Whiteside TL: The tumor microenvironment and its role in promoting tumor growth. Oncogene. 27:5904–5912. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Mittal V: Epithelial mesenchymal transition in tumor metastasis. Annu Rev Pathol. 13:395–412. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A and Weinberg RA: Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 117:927–939. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Shi J, Chai K, Ying X and Zhou BP: The role of snail in EMT and tumorigenesis. Curr Cancer Drug Targets. 13:963–972. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Soen B, Vandamme N, Berx G, Schwaller J and Vlierberghe PV: ZEB proteins in leukemia: Friends, Foes, or Friendly Foes? HemeSphere. 2:e432018. View Article : Google Scholar | |
|
Pantel K and Alix-Panabieres C: Circulating tumour cells in cancer patients: Challenges and perspectives. Trends Mol Med. 16:398–406. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang ZY and Ge HY: Micrometastasis in gastric cancer. Cancer Lett. 336:34–45. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Bock C, Rack B, Huober J, Andergassen U, Jeschke U and Doisneau-Sixou S: Distinct expression of cytokeratin, N-cadherin and CD133 in circulating tumor cells of metastatic breast cancer patients. Future Oncol. 10:1751–1765. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Q, Cao HZ and Zheng PS: LGR5 promotes the proliferation and tumor formation of cervical cancer cells through the Wnt/β-catenin signaling pathway. Oncotarget. 5:9092–9105. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, Baba H, Saya H and Nagano O: CD44+ slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and pros-taglandin E2 in gastric tumorigenesis. Cancer Sci. 101:673–678. 2010. View Article : Google Scholar | |
|
Ponta H, Sherman L and Herrlich PA: CD44: From adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol. 4:33–45. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 133:704–715. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Brabletz T, Jung A, Spaderna S, Hlubek F and Kirchner T: Opinion: Migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer. 5:744–749. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Hollier BG, Evans K and Mani SA: The epithelial-to-mesenchymal transition and cancer stem cells: A coalition against cancer therapies. J Mammary Gland Biol Neoplasia. 14:29–43. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Jeter CR, Yang T, Wang J, Chao HP and Tang DG: Concise review: NANOG in cancer stem cells and tumor development: An update and outstanding questions. Stem Cells. 33:2381–2390. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Torres-Padilla ME and Chambers I: Transcription factor heterogeneity in pluripotent stem cells: A stochastic advantage. Development. 141:2173–2181. 2014. View Article : Google Scholar : PubMed/NCBI |
