Skip to main content
Hauptrubriken
CME Facharzt-Training Webinare Zeitschriften Bücher e.Medpedia Podcast
Service
Jobbörse Info & Hilfe
Fachgebiete
Anästhesiologie Allgemeinmedizin Arbeitsmedizin Augenheilkunde Chirurgie Dermatologie Gynäkologie und Geburtshilfe HNO Innere Medizin Kardiologie Neurologie Onkologie und Hämatologie Orthopädie und Unfallchirurgie Pädiatrie Pathologie Psychiatrie Radiologie Rechtsmedizin Urologie Zahnmedizin
Themen
Klimawandel und Gesundheit Neues aus dem Markt COVID-19 Praxis und Beruf Seltene Erkrankungen GOÄ & EBM Panorama
Sammlungen
Kasuistiken Algorithmen & Infografiken Blickdiagnosen Arthropedia FlapFinder (für Dermatochirurgen) Videos Kongressberichterstattung Medizin für Apothekerinnen und Apotheker Für Ärztinnen und Ärzte in Weiterbildung Für Medizinstudierende
Erweiterte Suche
Anmelden
nach oben
Surgery Today
Erschienen in: Surgery Today 12/2020

05.02.2020 | Review Article

Clinical implications of cancer stem cells in digestive cancers: acquisition of stemness and prognostic impact

verfasst von: Ryouichi Tsunedomi, Kiyoshi Yoshimura, Nobuaki Suzuki, Shoichi Hazama, Hiroaki Nagano

Erschienen in: Surgery Today | Ausgabe 12/2020

Einloggen, um Zugang zu erhalten

Abstract

Digestive system cancers are the most frequent cancers worldwide and often associated with poor prognosis because of their invasive and metastatic characteristics. Recent studies have found that the plasticity of cancer cells can impart cancer stem-like properties via the epithelial–mesenchymal transition (EMT). Cancer stem-like properties such as tumor initiation are integral to the formation of metastasis, which is the main cause of poor prognosis. Numerous markers of cancer stem cells (CSCs) have been identified in many types of cancer. Therefore, CSCs, via their stem cell-like functions, may play an important role in prognosis after surgery. While several reports have described prognostic analysis using CSC markers, few reviews have summarized CSCs and their association with prognosis. Herein, we review the prognostic potential of eight CSC markers, CD133, CD44, CD90, ALDH1A1, EPCAM, SOX2, SOX9, and LGR5, in digestive cancers including those of the pancreas, colon, liver, gastric, and esophagus.
Literatur
1.
Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67:177–93.PubMed
2.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.PubMed
3.
4.
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.PubMed
5.
El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557–766.PubMed
6.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMed
7.
Lamarca A, Asselin MC, Manoharan P, McNamara MG, Trigonis I, Hubner R, et al. 18F-FLT PET imaging of cellular proliferation in pancreatic cancer. Crit Rev Oncol Hematol. 2016;99:158–69.PubMed
8.
Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38:200–7.PubMed
9.
Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet. 2003;362:1907–17.PubMed
10.
Shimozawa N, Hanazaki K. Longterm prognosis after hepatic resection for small hepatocellular carcinoma. J Am Coll Surg. 2004;198:356–65.PubMed
11.
Lai EC, Lau WY. The continuing challenge of hepatic cancer in Asia. Surgeon. 2005;3:210–5.PubMed
12.
Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med. 2008;359:1995–2004.PubMedPubMedCentral
13.
Bruix J, Llovet JM. Major achievements in hepatocellular carcinoma. Lancet. 2009;373:614–6.PubMed
14.
Wu JC, Huang YH, Chau GY, Su CW, Lai CR, Lee PC, et al. Risk factors for early and late recurrence in hepatitis B-related hepatocellular carcinoma. J Hepatol. 2009;51:890–7.PubMed
15.
Chun JM, Kwon HJ, Sohn J, Kim SG, Park JY, Bae HI, et al. Prognostic factors after early recurrence in patients who underwent curative resection for hepatocellular carcinoma. J Surg Oncol. 2011;103:148–51.PubMed
16.
Tsunedomi R, Iizuka N, Tamesa T, Sakamoto K, Hamaguchi T, Somura H, et al. Decreased ID2 promotes metastatic potentials of hepatocellular carcinoma by altering secretion of vascular endothelial growth factor. Clin Cancer Res. 2008;14:1025–31.PubMed
17.
Bertuccio O, Chatenoud L, Levi F, Praud D, Ferlay J, Negri E, et al. Recent patterns in gastric cancer: a global overview. Int J Cancer. 2009;125:666–73.PubMed
18.
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386386.PubMed
19.
Weigelt B, Peterse JL, van’t Veer LJ. Breast cancer metastasis markers and models. Nat Rev Cancer. 2005;5:591–602.PubMed
20.
Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer. 2006;6:449–58.PubMed
21.
Zhang HX, Jin GF, Shen HB. Epidemiologic differences in esophageal cancer between Asian and Western populations. Chin J Cancer. 2012;31:281–6.PubMedPubMedCentral
22.
Tachimor Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y, et al. Supraclavicular node metastasis from thoracic esophageal carcinoma: A surgical series from a Japanese multi-institutional nationwide registry of esophageal cancer. J Thorac Cardiovasc Surg. 2014;148:1224–9.
23.
Yang D, Sun Y, Hu L, Zheng H, Ji P, Pecot CV, et al. Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell. 2013;23:186–99.PubMedPubMedCentral
24.
Mitra R, Chen X, Greenawalt EJ, Maulik U, Jiang W, Zhao Z, et al. Decoding critical long non-coding RNA in ovarian cancer epithelial-to-mesenchymal transition. Nat Commun. 2017;8:1604.PubMedPubMedCentral
25.
Mimori K, Saito T, Niida A, Miyano S. Cancer evolution and heterogeneity. Ann Gastroenterol Surg. 2018;2:332–8.PubMedPubMedCentral
26.
Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial–mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 2012;22:725–36.PubMedPubMedCentral
27.
28.
Bae YK, Choi JE, Kang SH, Lee SJ. Epithelial–mesenchymal transition phenotype is associated with clinicopathological factors that indicate aggressive biological behavior and poor clinical outcomes in invasive breast cancer. J Breast Cancer. 2015;18:256–63.PubMedPubMedCentral
29.
Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9:265–73.PubMed
30.
Taneyhill LA, Coles EG, Bronner-Fraser M. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development. 2007;134:1481–90.PubMed
31.
Deep G, Jain AK, Ramteke A, Ting H, Vijendra KC, Gangar SC, et al. SNAI1 is critical for the aggressiveness of prostate cancer cells with low E-cadherin. Mol Cancer. 2014;13:37.PubMedPubMedCentral
32.
Campbell K, Whissell G, Franch-Marro X, Batlle E, Casanova J. Specific GATA factors act as conserved inducers of an endodermal-EMT. Dev Cell. 2011;21:1051–61.PubMed
33.
Song K, Li Q, Jiang ZZ, Guo CW, Li P. Heparan sulfate D-glucosaminyl 3-O-sulfotransferase-3B1, a novel epithelial–mesenchymal transition inducer in pancreatic cancer. Cancer Biol Ther. 2011;12:388–98.PubMed
34.
Radisky ES, Radisky DC. Matrix metalloproteinase-induced epithelial–mesenchymal transition in breast cancer. J Mammary Gland Biol Neoplasia. 2010;1:201–12.
35.
Ke P, Wu ZD, Wen HS, Ying MX, Long HC, Qing LG. Current evidence on associations between the MMP-7 (-181A%3eG) polymorphism and digestive system cancer risk. Asian Pac J Cancer Rev. 2013;14:2269–72.
36.
Brabletz T, Jung A, Hermann K, Günther K, Hohenberger W, Kirchner T. Nuclear overexpression of the oncoprotein β-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol Res Pract. 1998;194:701–4.PubMed
37.
Williams ED, Gao D, Redfern A, Thompson EW. Controversies around epithelial–mesenchymal plasticity in cancer metastasis. Nat Rev Cancer. 2019;19:716–32.PubMedPubMedCentral
38.
Lu W, Kang Y. Epithelial–mesenchymal plasticity in cancer progression and metastasis. Dev Cell. 2019;49:361–74.PubMedPubMedCentral
39.
Gener P, Seras-Franzoso J, Callejo PG, Andrade F, Rafael D, Martínez F, et al. Dynamism, sensitivity, and consequences of mesenchymal and stem-like phenotype of cancer cells. Stem Cells Int. 2018;2018:4516454.PubMedPubMedCentral
40.
Chin VL, Lim CL. Epithelial–mesenchymal plasticity—engaging stemness in an interplay of phenotypes. Stem Cell Investig. 2019;6:25.PubMedPubMedCentral
41.
Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339:580–4.PubMedPubMedCentral
42.
Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–15.PubMedPubMedCentral
43.
Nishiyama M, Tsunedomi R, Yoshimura K, Hashimoto N, Matsukuma S, Ogihara H, et al. Metastatic ability and the epithelial–mesenchymal transition in induced cancer stem-like hepatoma cells. Cancer Sci. 2018;109:1101–9.PubMedPubMedCentral
44.
Grosse-Wilde A, Fouquier d'Hérouël A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, et al. Stemness of the hybrid epithelial/mesenchymal state in breast cancer and its association with poor survival. PLoS ONE. 2015;10:e0126522.PubMedPubMedCentral
45.
Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, Onodera M, et al. Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology. 2007;133:937–50.PubMed
46.
Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.PubMed
47.
Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells—perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66:9339–444.PubMed
48.
Szakács G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov. 2006;5:219–34.PubMed
49.
Sukowati CHC, Rosso N, Crocè LS, Tiribelli C. Hepatic cancer stem cells and drug resistance: relevance in targeted therapies for hepatocellular carcinoma. World J Hepatol. 2010;2:114–26.PubMedPubMedCentral
50.
Gillet JP, Gottesman MM. Advances in the molecular detection of ABC transporters involved in multidrug resistance in cancer. Curr Pharm Biotechnol. 2011;12:686–92.PubMedPubMedCentral
51.
Hashimoto N, Tsunedomi R, Yoshimura K, Watanabe Y, Hazama S, Oka M. Cancer stem-like sphere cells induced from de-differentiated hepatocellular carcinoma-derived cell lines possess the resistance to anti-cancer drugs. BMC Cancer. 2014;14:722.PubMedPubMedCentral
52.
Gottesman MM. Mechanisms of cancer drug resistance. Annu Rev Med. 2002;53:615–27.PubMed
53.
Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell. 2012;10:717–28.PubMed
54.
Gilbertson RJ, Rich JN. Making a tumour’s bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer. 2007;7:733–6.PubMed
55.
Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.PubMed
56.
Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917–20.PubMed
57.
Palk IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451:141–6.
58.
Plaks V, Koopman CD, Werb Z. Cancer. Circulating tumor cells. Science. 2013;341:1186–8.PubMed
59.
Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell. 2014;14:275–91.PubMed
60.
Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, et al. Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update. Nat Rev Clin Oncol. 2015;12:445–64.PubMedPubMedCentral
61.
Zhou L, Yu L, Zhu B, Wu S, Song W, Gong X, et al. Metastasis-associated in colon cancer-1 and aldehyde dehydrogenase 1 are metastatic and prognostic biomarker for non-small cell lung cancer. BMC Cancer. 2016;16:876.PubMedPubMedCentral
62.
Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005;65:5506–11.PubMed
63.
Cho RW, Clarke MF. Recent advances in cancer stem cells. Curr Opin Genet Dev. 2008;18:48–53.PubMed
64.
Polytarchou C, Iliopoulos D, Struhl K. An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. PNAS USA. 2012;109:14470–5.PubMedPubMedCentral
65.
Shan J, Shen J, Liu L, Xia F, Xu C, Duan G, Xu Y, et al. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology. 2012;56:1004–14.PubMed
66.
Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J. NF-κB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nat commun. 2013;4:2299.PubMed
67.
Infanger DW, Cho Y, Lopez BS, Mohanan S, Liu SC, Gursel D, et al. perivascular niche. Cancer Res. 2013;73:7079–89.PubMed
68.
Lawson DA, Bhakta NR, Kessenbrock K, Prummel KD, Yu Y, Takai K, et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature. 2015;526:131–5.PubMedPubMedCentral
69.
Matsukuma S, Yoshimura K, Ueno T, Oga A, Inoue M, Watanabe Y, et al. Calreticulin is highly expressed in pancreatic cancer stem-like cells. Cancer Sci. 2016;107:1599–609.PubMedPubMedCentral
70.
Yang L, Ping YF, Yu X, Qian F, Guo ZJ, Qian C, et al. Gastric cancer stem-like cells possess higher capability of invasion and metastasis in association with a mesenchymal transition phenotype. Cancer Lett. 2011;310:46–52.PubMed
71.
Yu SC, Bian XW. Enrichment of cancer stem cells based on heterogeneity of invasiveness. Stem Cell Rev. 2009;5:66–71.
72.
Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L, et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway. J Immunol. 2012;189:444–53.PubMed
73.
Watanabe Y, Yoshimura K, Yoshikawa K, Tsunedomi R, Shindo Y, Matsukuma S, et al. A stem cell medium containing neural stimulating factor induces a pancreatic cancer stem-like cell-enriched population. Int J Oncol. 2014;45:1857–66.PubMedPubMedCentral
74.
Horst D, Kriegl L, Engel J, Kirchner T, Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer. 2008;99:1285–9.PubMedPubMedCentral
75.
Horst D, Kriegl L, Engel J, Kirchner T, Jung A. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009;27:844–50.PubMed
76.
Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L, et al. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer. 2010;103:382–90.PubMedPubMedCentral
77.
Voglar T, Kriegl L, Horst D, Engel J, Sagebiel S, Schäffauer AJ, et al. The expression pattern of aldehyde dehydrogenase 1 (ALDH1) is an independent prognostic marker for low survival in colorectal tumors. Exp Mol Pathol. 2012;92:111–7.
78.
Saito S, Okabe H, Watanabe M, Ishimoto T, Iwatsuki M, Baba Y, et al. CD44v6 expression is related to mesenchymal phenotype and poor prognosis in patients with colorectal cancer. Oncol Rep. 2013;29:1570–8.PubMed
79.
Goossens-Beumer IJ, Zeestraten EC, Benard A, Christen T, Reimers MS, Keijzer R, et al. Clinical prognostic value of combined analysis of Aldh1, Survivin, and EpCAM expression in colorectal cancer. Br J Cancer. 2014;110:2935–44.PubMedPubMedCentral
80.
Ong CE, Chong PY, McArt DG, Chan JY, Tan HT, Kumar AP, et al. The prognostic value of the stem-like group in colorectal cancer using a panel of immunohistochemistry markers. Oncotarget. 2015;6:12763–73.PubMedPubMedCentral
81.
Yin Ah, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 1997;90:5002–12.PubMed
82.
Weigman A, Corbeil D, Hellwig A, Huttner WB. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA. 1997;94:12425–300.
83.
Bidlingmaier S, Zhu X, Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med. 2008;86:1025–32.PubMed
84.
Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.PubMed
85.
Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–8.PubMed
86.
Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–51.PubMed
87.
Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus MC, Cantino D, et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol. 2005;166:545–55.PubMedPubMedCentral
88.
Florek M, Haase M, Marzesco AM, Freund D, Ehninger G, Huttner WB, et al. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res. 2005;319:15–26.PubMed
89.
Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006;351:820–4.PubMed
90.
Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–55.PubMed
91.
O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–10.PubMed
92.
Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer. 2007;120:1444–500.PubMed
93.
Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007;132:2542–56.PubMed
94.
Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJ, Tahan SR. Increased expression of stem cell markers in malignant melanoma. Mod Pathol. 2007;20:102–7.PubMed
95.
Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer. 2007;43:935–46.PubMed
96.
Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res. 2008;14:123–9.PubMed
97.
Mizrak D, Brittan M, Alison M. CD133: molecule of the moment. J Pathol. 2008;214:3–9.PubMed
98.
Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer. 2008;18:506–14.PubMed
99.
Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008;15:504–14.PubMed
100.
Zhang J, Guo X, Chang DY, Rosen DG, Mercado-Uribe I, Liu J. CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol. 2012;25:456–64.PubMed
101.
Li CY, Li BX, Liang Y, Peng RQ, Ding Y, Xu DZ, et al. Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med. 2009;7:56.PubMedPubMedCentral
102.
Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009;457:603–7.PubMed
103.
Tirino V, Camerlingo R, Franco R, Malanga D, La Rocca A, Viglietto G, et al. The role of CD133 in the identification and characterisation of tumour-initiating cells in non-small-cell lung cancer. Eur J Cardiothorac Surg. 2009;36:446–53.PubMed
104.
Zhang DG, Jiang AG, Lu HY, Zhang LX, Gao XY. Isolation, cultivation and identification of human lung adenocarcinoma stem cells. Oncol Lett. 2015;9:47–544.PubMed
105.
Mia-Jan K, Jung SY, Kim IY, Oh SS, Choi E, Chang SJ, et al. CD133 expression is not an independent prognostic factor in stage II and III colorectal cancer but may predict the better outcome in patients with adjuvant therapy. BMC Cancer. 2013;13:166.PubMedPubMedCentral
106.
Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313–23.PubMed
107.
Iseki Y, Shibutani M, Maeda K, Nagahara H, Ikeya T, Hirakawa K. Significance of E-cadherin and CD44 expression in patients with unresectable metastatic colorectal cancer. Oncol Lett. 2017;14:1025–34.PubMedPubMedCentral
108.
Wu Q, Yang Y, Wu S, Li W, Zhang N, Dong X, et al. Evaluation of the correlation of KAI1/CD82, CD44, MMP7 and β-catenin in the prediction of prognosis and metastasis in colorectal carcinoma. Diagn Pathol. 2015;10:176.PubMedPubMedCentral
109.
Fang C, Fan C, Wang C, Huang Q, Meng W, Yu Y, et al. CD133+CD54+CD44+ circulating tumor cells as a biomarker of treatment selection and liver metastasis in patients with colorectal cancer. Oncotarget. 2016;7:77389–403.PubMedPubMedCentral
110.
Choi SL, Kim SY, Lee JH, Kim JY, Cho EW, Kim IG. Osteopontin production by TM4SF4 signaling drives a positive feedback autocrine loop with the STAT3 pathway to maintain cancer stem cell-like properties in lung cancer cells. Oncotarget. 2017;8:101284–97.PubMedPubMedCentral
111.
Wang HH, Liao CC, Chow NH, Huang LL, Chuang JI, Wei KC, et al. Whether CD44 is an applicable marker for glioma stem cells. Am J Transl Res. 2017;9:4785–806.PubMedPubMedCentral
112.
Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci. 2007;104:10158–63.PubMedPubMedCentral
113.
Ishimot T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell. 2011;19:387–400.
114.
Nagano O, Okazaki S, Saya H. Redox regulation in stem-like cancer cells by CD44 variant isoforms. Oncogene. 2013;32:5191–8.PubMed
115.
Günthert U, Hofmann M, Rudy W, Reber S, Zöller M, Haussmann I, et al. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell. 1991;65:13–24.PubMed
116.
Yu Q, Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 1999;13:35–48.PubMedPubMedCentral
117.
Uchino M, Kojima H, Wada K, Imada M, Onoda F, Satofuka H, et al. Nuclear beta-catenin and CD44 upregulation characterize invasive cell populations in non-aggressive MCF-7 breast cancer cells. BMC Cancer. 2010;10:414.PubMedPubMedCentral
118.
Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, et al. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial–mesenchymal transition and breast cancer progression. J Clin Invest. 2011;121:1064–74.PubMedPubMedCentral
119.
Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–7.PubMed
120.
Rege TA, Hagood JS. Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J. 2006;20:1045–54.PubMed
121.
Dan YY, Riehle KJ, Lazaro C, Teoh N, Haque J, Campbell JS, et al. Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc Natl Acad Sci USA. 2006;103:9912–7.PubMedPubMedCentral
122.
Masson NM, Currie IS, Terrace JD, Garden OJ, Parks RW, Ross JA. Hepatic progenitor cells in human fetal liver express the oval cell marker Thy-1. Am J Physiol Gastrointest Liver Physiol. 2006;291:G45–54.PubMed
123.
Yang ZF, Ngai P, Ho DW, Yu WC, Ng MN, Lau CK, et al. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology. 2008;47:919–28.PubMed
124.
Cheng BQ, Jiang Y, Li DL, Fan JJ, Ma M. Up-regulation of thy-1 promotes invasion and metastasis of hepatocarcinomas. Asian Pac J Cancer Prev. 2012;13:1349–53.PubMed
125.
Yamaoka R, Ishii T, Kawai T, Yasuchika K, Miyauchi Y, Kojima H, et al. CD90 expression in human intrahepatic cholangiocarcinoma is associated with lymph node metastasis and poor prognosis. J Surg Oncol. 2018;118:664–74.PubMed
126.
Balzar M, Briaire-de Bruijn IH, Rees-Bakker HA, Prins FA, Helfrich W, de Leij L, et al. Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions. Mol Cell Biol. 2001;21:2570–80.PubMedPubMedCentral
127.
128.
Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol. 2009;11:162–71.PubMed
129.
Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC. Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol. 2007;171:386–95.PubMedPubMedCentral
130.
Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology. 2009;136:1012–4.PubMed
131.
Moreb J, Schweder M, Suresh A, Zucali JR. Overexpression of the human aldehyde dehydrogenase class I results in increased resistance to 4-hydroperoxycyclophosphamide. Cancer Gene Ther. 1996;3:24–30.PubMed
132.
Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM, et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl ACad Sci USA. 1999;96:9118–233.PubMedPubMedCentral
133.
Balicki D. Moving forward in human mammary stem cell biology and breast cancer prognostication using ALDH1. Cell Stem Cell. 2007;1:485–7.PubMed
134.
Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. 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.PubMedPubMedCentral
135.
Corti S, Locatelli F, Papadimitriou D, Donadoni C, Salani S, Del Bo R, et al. Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cell. 2006;24:975–85.
136.
Armstrong L, Stojkovic M, Dimmick I, Ahmad S, Stojkovic P, Hole N, et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells. 2004;22:1142–51.PubMed
137.
Hess DA, Wirthlin L, Craft TP, Herrbrich PE, Hohm SA, Lahey R, et al. Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells. Blood. 2006;107:2162–9.PubMedPubMedCentral
138.
Hess DA, Craft TP, Wirthlin L, Hohm S, Zhou P, Eades WC, et al. Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity. Stem Cell. 2008;26:611–20.
139.
Fleischman AG. ALDH marks leukemia stem cell. Blood. 2012;119:3376–7.PubMed
140.
Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, et al. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res. 2009;15:4234–41.PubMed
141.
Nishikawa S, Konno M, Hamabe A, Hasegawa S, Kano Y, Ohta K, et al. Aldehyde dehydrogenase high gastric cancer stem cells are resistant to chemotherapy. Int J Oncol. 2013;42:1437–42.PubMed
142.
Huang CP, Tsai MF, Chang TH, Tang WC, Chen SY, Lai HH, et al. ALDH-positive lung cancer stem cells confer resistance to epidermal growth factor receptor tyrosine kinase inhibitors. Cancer Lett. 2013;328:144–51.PubMed
143.
Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Cell. 2009;7:330–8.
144.
Zhang G, Ma L, Xie YK, Miao XB, Jin C. Esophageal cancer tumorspheres involve cancer stem-like populations with elevated aldehyde dehydrogenase enzymatic activity. Mol Med Rep. 2012;6:519–24.PubMed
145.
Fujiwara D, Kato K, Nohara S, Iwanuma Y, 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. 2013;434:773–8.PubMed
146.
Yang L, Ren Y, Yu X, Qian F, Bian BS, Xiao HL, et al. ALDH1A1 defines invasive cancer stem-like cells and predicts poor prognosis in patients with esophageal squamous cell carcinoma. Mod Pathol. 2014;27:775–83.PubMed
147.
Sarkar A, Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell. 2013;12:15–30.PubMedPubMedCentral
148.
Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003;17:126–40.PubMedPubMedCentral
149.
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMed
150.
Li XL, Eishi Y, Bai YQ, Sakai H, Akiyama Y, Tani M, et al. Expression of the SRY-related HMG box protein SOX2 in human gastric carcinoma. Int J Oncol. 2004;24:257–63.PubMed
151.
Sanada Y, Yoshida K, Ohara M, Oeda M, Konishi K, Tsutani Y. Histopathologic evaluation of stepwise progression of pancreatic carcinoma with immunohistochemical analysis of gastric epithelial transcription factor SOX2: comparison of expression patterns between invasive components and cancerous or nonneoplastic intraductal components. Pancreas. 2006;32:164–70.PubMed
152.
Forghanifard MM, Ardalan Khales S, Javdani-Mallak A, Rad A, Farshchian M, Abbaszadegan MR. Stemness state regulators SALL4 and SOX2 are involved in progression and invasiveness of esophageal squamous cell carcinoma. Med Oncol. 2014;31:922.PubMed
153.
154.
Han X, Fang X, Lou X, Hua D, Ding W, Foltz G, et al. Silencing SOX2 induced mesenchymal–epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients. PLoS ONE. 2012;7:e41335.PubMedPubMedCentral
155.
Basu-Roy U, Seo E, Ramanathapuram L, Rapp TB, Perry JA, Orkin SH, et al. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene. 2012;31:2270–82.PubMed
156.
Lundberg IV, Edin S, Eklöf V, Öberg Å, Palmqvist R, Wikberg ML. SOX2 expression is associated with a cancer stem cell state and down-regulation of CDX2 in colorectal cancer. BMC Cancer. 2016;16:471.PubMedPubMedCentral
157.
Liu L, Liu C, Zhang Q, Shen J, Zhang H, Shan J, et al. SIRT1-mediated transcriptional regulation of SOX2 is important for self-renewal of liver cancer stem cells. Hepatology. 2016;64:814–27.PubMed
158.
Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39:2195–214.PubMedPubMedCentral
159.
Kadaja M, Keyes BE, Lin M, Pasolli HA, Genander M, Polak L, et al. SOX9: a stem cell transcriptional regulator of secreted niche signaling factors. Genes Dev. 2014;28:328–41.PubMedPubMedCentral
160.
Bengochea A, de Souza MM, Lefrançois L, Le Roux E, Galy O, Chemin I, et al. Common dysregulation of Wnt/Frizzled receptor elements in human hepatocellular carcinoma. Br J Cancer. 2008;99:143–50.PubMedPubMedCentral
161.
Merle P, Kim M, Herrmann M, Gupte A, Lefrançois L, Califano S, et al. Oncogenic role of the frizzled-7/beta-catenin pathway in hepatocellular carcinoma. J Hepatol. 2005;43:854–62.PubMed
162.
Higashihara T, Yoshitomi H, Nakata Y, Kagawa S, Takano S, Shimizu H, et al. Sex determining region y box 9 induces chemoresistance in pancreatic cancer cells by induction of putative cancer stem cell characteristics and its high expression predicts poor prognosis. Pancreas. 2017;46:1296–304.PubMed
163.
Guo X, Xiong L, Sun T, Peng R, Zou L, Zhu H, et al. Expression features of SOX9 associate with tumor progression and poor prognosis of hepatocellular carcinoma. Diagn Pathol. 2012;7:44.PubMedPubMedCentral
164.
Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012;148:1015–28.PubMedPubMedCentral
165.
Santos JC, Carrasco-Garcia E, Garcia-Puga M, Aldaz P, Montes M, Fernandez-Reyes M, et al. SOX9 elevation acts with canonical WNT signaling to drive gastric cancer progression. Cancer Res. 2016;76:6735–46.PubMed
166.
Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–7.PubMed
167.
Brrker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 2009;457:608–11.
168.
Su S, Hong F, Liang Y, Zhou J, Liang Y, Chen K, et al. Lgr5 methylation in cancer stem cell differentiation and prognosis-prediction in colorectal cancer. PLoS ONE. 2015;10:e0143513.PubMedPubMedCentral
169.
Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells. 2005;23:879–94.PubMed
170.
Maeda S, Shinchi H, Kurahara H, Mataki Y, Maemura K, Sato M, et al. CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer. Br J Cancer. 2008;98:1389–97.PubMedPubMedCentral
171.
Li X, Zhao H, Gu J, Zheng L. Prognostic value of cancer stem cell marker CD133 expression in pancreatic ductal adenocarcinoma (PDAC): a systematic review and meta-analysis. Int J Clin Exp Pathol. 2015;8:12084–92.PubMedPubMedCentral
172.
Huang R, Mo D, Wu J, Ai H, Lu Y. CD133 expression correlates with clinicopathologic features and poor prognosis of colorectal cancer patients: an updated meta-analysis of 37 studies. Medicine. 2018;97:e10446.PubMedPubMedCentral
173.
Nagata T, Sakakura C, Komiyama S, Miyashita A, Nishio M, Murayama Y, et al. Expression of cancer stem cell markers CD133 and CD44 in locoregional recurrence of rectal cancer. Anticancer Res. 2011;31:495–500.PubMed
174.
Zhong C, Wu JD, Fang MM, Pu LY. Clinicopathological significance and prognostic value of the expression of the cancer stem cell marker CD133 in hepatocellular carcinoma: a meta-analysis. Tumour Biol. 2015;36:7623–30.PubMed
175.
Zhao Q, Zhou H, Liu Q, Cao Y, Wang G, Hu A, et al. Prognostic value of the expression of cancer stem cell-related markers CD133 and CD44 in hepatocellular carcinoma: From patients to patient-derived tumor xenograft models. Oncotarget. 2016;7:47431–43.PubMedPubMedCentral
176.
Chen YL, Lin PY, Ming YZ, Huang WC, Chen RF, Chen PM, et al. The effects of the location of cancer stem cell marker CD133 on the prognosis of hepatocellular carcinoma patients. BMC Cancer. 2017;17:474.PubMedPubMedCentral
177.
Wen L, Chen XZ, Yang K, Chen ZX, Zhang B, Chen JP, et al. Prognostic value of cancer stem cell marker CD133 expression in gastric cancer: a systematic review. PLoS ONE. 2013;8:e59154.PubMedPubMedCentral
178.
Yiming L, Yunshan G, Bo M, Yu Z, Tao W, Gengfang L, et al. CD133 overexpression correlates with clinicopathological features of gastric cancer patients and its impact on survival: a systematic review and meta-analysis. Oncotarget. 2015;6:42019–27.PubMedPubMedCentral
179.
Wang JH, Huang ST, Zhang L, Liu ZG, Liang RX, Jiang SW, et al. Combined prognostic value of the cancer stem cell markers CD47 and CD133 in esophageal squamous cell carcinoma. Cancer Med. 2019;8:1315–25.PubMedPubMedCentral
180.
Leni A, Giuffrè G, Adamo V, Tuccari G. Prognostic impact of CD133 immunoexpression in node-negative invasive breast carcinomas. Anticancer Res. 2011;31:1315–20.
181.
Herpel E, Jensen K, Muley T, Warth A, Schnabel PA, Meister M, et al. The cancer stem cell antigens CD133, BCRP1/ABCG2 and CD117/c-KIT are not associated with prognosis in resected early-stage non-small cell lung cancer. Anticancer Res. 2011;31:4491–500.PubMed
182.
Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J, Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer. 2010;126:950–8.PubMed
183.
Salnikov AV, Kusumawidjaja G, Rausch V, Bruns H, Gross W, Khamidjanov A, et al. Cancer stem cell marker expression in hepatocellular carcinoma and liver metastases is not sufficient as single prognostic parameter. Cancer Lett. 2009;275:185–93.PubMed
184.
Guo Z, Li LQ, Jiang JH, Ou C, Zeng LX, Xiang BD, et al. Cancer stem cell markers correlate with early recurrence and survival in hepatocellular carcinoma. World J Gastroenterol. 2014;20:2098–106.PubMedPubMedCentral
185.
Lu C, Xu F, Gu J, Yuan Y, Zhao G, Yu X, et al. Clinical and biological significance of stem-like CD133+ CXCR4+ cells in esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2015;150:386–95.PubMed
186.
Immervoll H, Hoem D, Sakariassen PØ, Steffensen OJ, Molven A. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer. 2008;8:48.PubMedPubMedCentral
187.
Okamoto H, Fujishima F, Nakamura Y, Zuguchi M, Ozawa Y, Takahashi Y, et al. Significance of CD133 expression in esophageal squamous cell carcinoma. World J Surg Oncol. 2013;11:51.PubMedPubMedCentral
188.
Fan L, He F, Liu H, Zhu J, Liu Y, Yin Z, et al. CD133: a potential indicator for differentiation and prognosis of human cholangiocarcinoma. BMC Cancer. 2011;11:320.PubMedPubMedCentral
189.
Nakajima TE, Yoshida H, Okamoto N, Nagashima K, Taniguchi H, Yamada Y, et al. Nucleostemin and TWIST as predictive markers for recurrence after neoadjuvant chemotherapy for esophageal carcinoma. Cancer Sci. 2012;103:233–8.PubMed
190.
Hang D, Dong HC, Ning T, Dong B, Hou DL, Xu WG. Prognostic value of the stem cell markers CD133 and ABCG2 expression in esophageal squamous cell carcinoma. Dis Esophagus. 2012;25:638–44.PubMed
191.
Gotoda T, Matsumura Y, Kondo H, Saitoh D, Shimada Y, Kosuge T, et al. Expression of CD44 variants and its association with survival in pancreatic cancer. Jpn J Cancer Res. 1998;89:1033–40.PubMedPubMedCentral
192.
Li XP, Zhang XW, Zheng LZ, Guo WJ. Expression of CD44 in pancreatic cancer and its significance. Int J Clin Exp Pathol. 2015;8:6724–31.PubMedPubMedCentral
193.
Liu Y, Wu T, Lu D, Zhen J, Zhang L. CD44 overexpression related to lymph node metastasis and poor prognosis of pancreatic cancer. Int J Biol Markers. 2018;33:308–13.PubMed
194.
Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, et al. CD44s regulates the TGF-β-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res. 2012;72:3414–23.PubMed
195.
Kodama H, Murata S, Ishida M, Yamamoto H, Yamaguchi T, Kaida S, et al. Prognostic impact of CD44-positive cancer stem-like cells at the invasive front of gastric cancer. Br J Cancer. 2017;116:186–94.PubMed
196.
Hu B, Luo W, Hu RT, Zhou Y, Qin SY, Jiang HX. Meta-analysis of prognostic and clinical significance of CD44v6 in esophageal cancer. Medicine. 2015;94:e1238.PubMedPubMedCentral
197.
Fang M, Wu J, Lai X, Ai H, Tao Y, Zhu B, et al. CD44 and CD44v6 are correlated with gastric cancer progression and poor patient prognosis: evidence from 42 studies. Cell Physiol Biochem. 2016;40:567–78.PubMed
198.
Luo Y, Tan Y. Prognostic value of CD44 expression in patients with hepatocellular carcinoma: meta-analysis. Cancer Cell Int. 2016;16:47.PubMedPubMedCentral
199.
Wang Z, Tang Y, Xie L, Huang A, Xue C, Gu Z, et al. The prognostic and clinical value of CD44 in colorectal cancer: a meta-analysis. Front Oncol. 2019;9:309.PubMedPubMedCentral
200.
Taniguchi D, Saeki H, Nakashima Y, Kudou K, Nakanishi R, Kubo N, et al. CD44v9 is associated with epithelial–mesenchymal transition and poor outcomes in esophageal squamous cell carcinoma. Cancer Med. 2018;7:6258–68.PubMedPubMedCentral
201.
Songun I, Litvinov SV, van de Velde CJ, Pals ST, Hermans J, van Krieken JH. Loss of Ep-CAM (CO17-1A) expression predicts survival in patients with gastric cancer. Br J Cancer. 2005;92:1767–72.PubMedPubMedCentral
202.
Jing F, Kim HJ, Kim CH, Kim YJ, Lee JH, Kim HR. Colon cancer stem cell markers CD44 and CD133 in patients with colorectal cancer and synchronous hepatic metastases. Int J Oncol. 2015;46:1582–8.PubMed
203.
Horikawa M, Iinuma H, Inoue T, Ogawa E, Fukushima R. Clinical significance of intraperitoneal CD44 mRNA levels of magnetically separated CD45-negative EpCAM-positive cells for peritoneal recurrence and prognosis in stage II and III gastric cancer patients. Oncol Rep. 2011;25:1413–20.PubMed
204.
Zhao RC, Zhou J, Chen KF, Gong J, Liu J, He JY, et al. The prognostic value of combination of CD90 and OCT4 for hepatocellular carcinoma after curative resection. Neoplasma. 2016;63:288–98.PubMed
205.
Zhou L, Zhu Y. The EpCAM overexpression is associated with clinicopathological significance and prognosis in hepatocellular carcinoma patients: a systematic review and meta-analysis. Int J Surg. 2018;56:274–80.PubMed
206.
Spizzo G, Went P, Dirnhofer S, Obrist P, Simon R, Spichtin H, et al. High Ep-CAM expression is associated with poor prognosis in node-positive breast cancer. Breast Cancer Res Treat. 2004;86:207–13.PubMed
207.
Eichelberg C, Chun FK, Bedke J, Heuer R, Adam M, Moch H, et al. Epithelial cell adhesion molecule is an independent prognostic marker in clear cell renal carcinoma. Int J Cancer. 2013;132:2948–55.PubMed
208.
Spizzo G, Went P, Dirnhofer S, Obrist P, Moch H, Baeuerle PA, et al. Overexpression of epithelial cell adhesion molecule (Ep-CAM) is an independent prognostic marker for reduced survival of patients with epithelial ovarian cancer. Gynecol Oncol. 2006;103:483–8.PubMed
209.
Prince S, Zeidman A, Dekel Y, Ram E, Koren R. Expression of epithelial cell adhesion molecule in gallbladder carcinoma and its correlation with clinicopathologic variables. Am J Clin Pathol. 2008;129:424–9.PubMed
210.
Chen XL, Chen XZ, Wang YG, He D, Lu ZH, Liu K, et al. Clinical significance of putative markers of cancer stem cells in gastric cancer: A retrospective cohort study. Oncotarget. 2016;7:62049–69.PubMedPubMedCentral
211.
Han S, Zong S, Shi Q, Li H, Liu S, Yang W, et al. Is Ep-CAM expression a diagnostic and prognostic biomarker for colorectal cancer? A Systematic Meta-Analysis. EBioMedicine. 2017;20:61–9.PubMedPubMedCentral
212.
Stoecklein NH, Siegmund A, Scheunemann P, Luebke AM, Erbersdobler A, Verde PE, et al. Ep-CAM expression in squamous cell carcinoma of the esophagus: a potential therapeutic target and prognostic marker. BMC Cancer. 2006;6:165.PubMedPubMedCentral
213.
Kimura H, Kato H, Faried A, Sohda M, Nakajima M, Fukai Y, et al. Prognostic significance of EpCAM expression in human esophageal cancer. Int J Oncol. 2007;30:171–9.PubMed
214.
Chen J, Xia Q, Jiang B, Chang W, Yuan W, Ma Z, et al. Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: a systematic review and meta-analysis. PLoS ONE. 2015;10:e0145164.PubMedPubMedCentral
215.
Chen MF, Chen PT, Lu MS, Chen WC. Role of ALDH1 in the prognosis of esophageal cancer and its relationship with tumor microenvironment. Mol Carcinog. 2018;57:78–88.PubMed
216.
Miller TJ, McCoy MJ, Hemmings C, Bulsara MK, Iacopetta B, Platell CF. The prognostic value of cancer stem-like cell markers SOX2 and CD133 in stage III colon cancer is modified by expression of the immune-related markers FoxP3, PD-L1 and CD3. Pathology. 2017;49:721–30.PubMed
217.
Takeda K, Mizushima T, Yokoyama Y, Hirose H, Wu X, Qian Y, et al. Sox2 is associated with cancer stem-like properties in colorectal cancer. Sci Rep. 2018;8:17639.PubMedPubMedCentral
218.
219.
Lundberg IV, Löfgren Burström A, Edin S, Eklöf V, Öberg Å, Stenling R, et al. SOX2 expression is regulated by BRAF and contributes to poor patient prognosis in colorectal cancer. PLoS ONE. 2014;9:e101957.PubMedPubMedCentral
220.
Luanpitpong S, Li J, Manke A, Brundage K, Ellis E, McLaughlin SL, et al. SLUG is required for SOX9 stabilization and functions to promote cancer stem cells and metastasis in human lung carcinoma. Oncogene. 2016;35:2824–33.PubMed
221.
Richtig G, Aigelsreiter A, Schwarzenbacher D, Ress AL, Adiprasito JB, Stiegelbauer V, et al. SOX9 is a proliferation and stem cell factor in hepatocellular carcinoma and possess widespread prognostic significance in different cancer types. PLoS ONE. 2017;12:e0187814.PubMedPubMedCentral
222.
Raspaglio G, Petrillo M, Martinelli E, Li Puma DD, Mariani M, De Donato M, et al. Sox9 and Hif-2α regulate TUBB3 gene expression and affect ovarian cancer aggressiveness. Gene. 2014;542:173–81.PubMed
223.
Liu Z, Ren YA, Pangas SA, Adams J, Zhou W, Castrillon DH, et al. FOXO1/3 and PTEN depletion in granulosa cells promotes ovarian granulosa cell tumor development. Mol Endocrinol. 2015;29:1006–244.PubMedPubMedCentral
224.
Kawai T, Yasuchika K, Ishii T, Miyauchi Y, Kojima H, Yamaoka R, et al. SOX9 is a novel cancer stem cell marker surrogated by osteopontin in human hepatocellular carcinoma. Sci Rep. 2016;6:30489.PubMedPubMedCentral
225.
Xue TC, Zhang L, Ren ZG, Chen RX, Cui JF, Ge NL, et al. Sex-determination gene SRY potentially associates with poor prognosis but not sex bias in hepatocellular carcinoma. Dig Dis Sci. 2015;60:427–35.PubMed
226.
Lü B, Fang Y, Xu J, Wang L, Xu F, Xu E, et al. Analysis of SOX9 expression in colorectal cancer. Am J Clin Pathol. 2008;130:897–904.PubMed
227.
Bruun J, Kolberg M, Nesland JM, Svindland A, Nesbakken A, Lothe RA. Prognostic Significance of β-Catenin, E-Cadherin, and SOX9 in colorectal cancer: results from a large population-representative series. Front Oncol. 2014;4:118.PubMedPubMedCentral
228.
Mesquita P, Freire AF, Lopes N, Gomes R, Azevedo D, Barros R, et al. Expression and clinical relevance of SOX9 in gastric cancer. Dis Markers. 2019;2019:8267021.PubMedPubMedCentral
229.
Choi YJ, Song JH, Yoon JH, Choi WS, Nam SW, Lee JY, et al. Aberrant expression of SOX9 is associated with gastrokine 1 inactivation in gastric cancers. Gastric Cancer. 2014;17:247–54.PubMed
230.
McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, Black S, et al. Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer Biol Ther. 2006;5:419–26.PubMed
231.
Valladares-Ayerbes M, Blanco-Calvo M, Reboredo M, Lorenzo-Patiño MJ, Iglesias-Díaz P, Haz M, et al. Evaluation of the adenocarcinoma-associated gene AGR2 and the intestinal stem cell marker LGR5 as biomarkers in colorectal cancer. Int J Mol Sci. 2012;13:4367–87.PubMedPubMedCentral
232.
Liu Z, Dai W, Jiang L, Cheng Y. Over-expression of LGR5 correlates with poor survival of colon cancer in mice as well as in patients. Neoplasma. 2014;61:177–85.PubMed
233.
Chen Q, Zhang X, Li WM, Ji YQ, Cao HZ, Zheng P. Prognostic value of LGR5 in colorectal cancer: a meta-analysis. PLoS ONE. 2014;9:e107013.PubMedPubMedCentral
234.
Jiang Y, Li W, He X, Zhang H, Jiang F, Chen Z. Lgr5 expression is a valuable prognostic factor for colorectal cancer: evidence from a meta-analysis. BMC Cancer. 2016;16:12.PubMedPubMedCentral
235.
Becker L, Huang Q, Mashimo H. Lgr5, an intestinal stem cell marker, is abnormally expressed in Barrett's esophagus and esophageal adenocarcinoma. Dis Esophagus. 2010;23:168–74.PubMed
236.
von Rahden BH, Kircher S, Lazariotou M, Reiber C, Stuermer L, Otto C, et al. LgR5 expression and cancer stem cell hypothesis: clue to define the true origin of esophageal adenocarcinomas with and without Barrett's esophagus? J Exp Clin Cancer Res. 2011;30:23.
237.
Huang T, Qiu X, Xiao J, Wang Q, Wang Y, Zhang Y, et al. The prognostic role of Leucine-rich repeat-containing G-protein-coupled receptor 5 in gastric cancer: a systematic review with meta-analysis. Clin Res Hepatol Gastroenterol. 2016;40:246–53.PubMed
238.
Jang BG, Lee BL, Kim WH. Prognostic significance of leucine-rich-repeat-containing G-protein-coupled receptor 5, an intestinal stem cell marker, in gastric carcinomas. Gastric Cancer. 2016;19:767–77.PubMed
239.
Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer. 2009;9:274–84.PubMed
240.
Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559–644.PubMed
241.
Bahnassy AA, Zekri AR, El-Bastawisy A, Fawzy A, Shetta M, Hussein N, et al. Circulating tumor and cancer stem cells in hepatitis C virus-associated liver disease. World J Gastroenterol. 2014;20:18240–8.PubMedPubMedCentral
242.
Fang C, Fan C, Wang C, Huang Q, Meng W, Yu Y, et al. Prognostic value of CD133+ CD54+ CD44+ circulating tumor cells in colorectal cancer with liver metastasis. Cancer Med. 2017;6:2850–7.PubMedPubMedCentral
243.
Tanaka S. Precision medicine based on surgical oncology in the era of genome-scale analysis and genome editing technology. Ann Gastroenterol Surg. 2018;2:106–15.PubMedPubMedCentral
Metadaten
Titel
Clinical implications of cancer stem cells in digestive cancers: acquisition of stemness and prognostic impact
verfasst von
Ryouichi Tsunedomi
Kiyoshi Yoshimura
Nobuaki Suzuki
Shoichi Hazama
Hiroaki Nagano
Publikationsdatum
05.02.2020
Verlag
Springer Singapore
Erschienen in
Surgery Today / Ausgabe 12/2020
Print ISSN: 0941-1291
Elektronische ISSN: 1436-2813
DOI
https://doi.org/10.1007/s00595-020-01968-x

Weitere Artikel der Ausgabe 12/2020

Surgery Today 12/2020 Zur Ausgabe

How To Do It

Oncoplastic breast surgery combining partial mastectomy with a triangular skin resection and re-centralization of the nipple-areola

Original Article

Where do you insert a drain tube during breast reconstruction?

Review Article

Neuroendocrine tumors of the lung: clinicopathological and molecular features

Short Communication

Implantation of human adipose-derived stromal cells for the functional recovery of a murine heat-damaged muscle model

Original Article

Independent predictors of secondary invasive pancreatic remnant tumors after initial resection of an intraductal papillary mucinous neoplasm: a nationwide large-scale survey in Japan

Original Article

Prognostic nutritional index and postoperative outcomes in patients with colon cancer after laparoscopic surgery

Neu im Fachgebiet Chirurgie

23.04.2024 | Ablationstherapie | Nachrichten

Wie erfolgreich ist eine Re-Ablation nach Rezidiv?

23.04.2024 | Appendizitis | Nachrichten

Hinter dieser Appendizitis steckte ein Erreger

23.04.2024 | Operationsvorbereitung | Nachrichten

Mehr Schaden als Nutzen durch präoperatives Aussetzen von GLP-1-Agonisten?

19.04.2024 | EAU 2024 | Kongressbericht | Nachrichten

Ureterstriktur: Innovative OP-Technik bewährt sich
weitere anzeigen

Update Chirurgie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Aktuelle BDC Leitlinien-Webinare

S3-Leitlinie „Diagnostik und Therapie des Karpaltunnelsyndroms“

Karpaltunnelsyndrom BDC Leitlinien Webinare
CME: 2 Punkte

Das Karpaltunnelsyndrom ist die häufigste Kompressionsneuropathie peripherer Nerven. Obwohl die Anamnese mit dem nächtlichen Einschlafen der Hand (Brachialgia parästhetica nocturna) sehr typisch ist, ist eine klinisch-neurologische Untersuchung und Elektroneurografie in manchen Fällen auch eine Neurosonografie erforderlich. Im Anfangsstadium sind konservative Maßnahmen (Handgelenksschiene, Ergotherapie) empfehlenswert. Bei nicht Ansprechen der konservativen Therapie oder Auftreten von neurologischen Ausfällen ist eine Dekompression des N. medianus am Karpaltunnel indiziert.

Prof. Dr. med. Gregor Antoniadis
Berufsverband der Deutschen Chirurgie e.V.

S2e-Leitlinie „Distale Radiusfraktur“

Radiusfraktur BDC Leitlinien Webinare
CME: 2 Punkte

Das Webinar beschäftigt sich mit Fragen und Antworten zu Diagnostik und Klassifikation sowie Möglichkeiten des Ausschlusses von Zusatzverletzungen. Die Referenten erläutern, welche Frakturen konservativ behandelt werden können und wie. Das Webinar beantwortet die Frage nach aktuellen operativen Therapiekonzepten: Welcher Zugang, welches Osteosynthesematerial? Auf was muss bei der Nachbehandlung der distalen Radiusfraktur geachtet werden?

PD Dr. med. Oliver Pieske
Dr. med. Benjamin Meyknecht
Berufsverband der Deutschen Chirurgie e.V.

S1-Leitlinie „Empfehlungen zur Therapie der akuten Appendizitis bei Erwachsenen“

Appendizitis BDC Leitlinien Webinare
CME: 2 Punkte

Inhalte des Webinars zur S1-Leitlinie „Empfehlungen zur Therapie der akuten Appendizitis bei Erwachsenen“ sind die Darstellung des Projektes und des Erstellungswegs zur S1-Leitlinie, die Erläuterung der klinischen Relevanz der Klassifikation EAES 2015, die wissenschaftliche Begründung der wichtigsten Empfehlungen und die Darstellung stadiengerechter Therapieoptionen.

Dr. med. Mihailo Andric
Berufsverband der Deutschen Chirurgie e.V.