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

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Gastric Cancer
Published in: Gastric Cancer 1/2014

01-01-2014 | Review Article

Gastric cancer stem cells: therapeutic targets

Authors: Slavica Stojnev, Miljan Krstic, Ana Ristic-Petrovic, Vladisav Stefanovic, Takanori Hattori

Published in: Gastric Cancer | Issue 1/2014

Login to get access

Abstract

During the past decade, a growing body of evidence has implied that cancer stem cells (CSCs) play an important role in the development of gastric cancer (GC). The notion that CSCs give rise to GC and may be responsible for invasion, metastasis, and resistance to treatment has profound implications for anti-cancer therapy. Recent major advances in the rapidly evolving field of CSCs have opened novel exciting opportunities for developing CSC-targeted therapies. Discovery of specific markers and signaling pathways in gastric CSCs (GCSCs), with the perfecting of technologies for identification, isolation, and validation of CSCs, may provide the basis for a revolutionary cancer treatment approach based on the eradication of GCSCs. Emerging therapeutic tools based on specific properties and functions of CSCs, including activation of self-renewal signaling pathways, differences in gene expression profiles, and increased activity of telomerase or chemoresistance mechanisms, are developing in parallel with advances in nanotechnology and bioengineering. The addition of GCSC-targeted therapies to current oncological protocols and their complementary application may be the key to successfully fighting GC.
Literature
1.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRef
2.
3.
Katoh M. Dysregulation of stem cell signaling network due to germline mutation, SNP, Helicobacter pylori infection, epigenetic change and genetic alteration in gastric cancer. Cancer Biol Ther. 2007;6:832–9.PubMedCrossRef
4.
Hagiwara T, Mukaisho K, Nakayama T, Sugihara H, Hattori T. Long-term proton pump inhibitor administration worsens atrophic corpus gastritis and promotes adenocarcinoma development in Mongolian gerbils infected with Helicobacter pylori. Gut. 2011;60:624–30.PubMedCrossRef
5.
6.
Saikawa Y, Fukuda K, Takahashi T, Nakamura R, Takeuchi H, Kitagawa Y. Gastric carcinogenesis and the cancer stem cell hypothesis. Gastric Cancer. 2010;13:11–24.PubMedCrossRef
7.
Kakinoki R, Kushima R, Matsubara A, Saito Y, Okabe H, Fujiyama Y, et al. Re-evaluation of histogenesis of gastric carcinomas: a comparative histopathological study between Helicobacter pylori-negative and H. pylori-positive cases. Dig Dis Sci. 2009;54:614–20.PubMedCrossRef
8.
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;66:9339–44.PubMedCrossRef
9.
10.
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003;100:3983–8.PubMedCrossRef
11.
Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science. 2007;317:337.PubMedCrossRef
12.
Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature (Lond). 2001;414:105–11.CrossRef
13.
Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature (Lond). 2008;456:593–8.CrossRef
14.
Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell. 2010;18:510–23.PubMedCentralPubMedCrossRef
15.
16.
O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature (Lond). 2007;445:106–10.CrossRef
17.
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.PubMedCrossRef
18.
Barker N, Clevers H. Leucine-rich repeat-containing G-protein coupled receptors as markers of adult stem cells. Gastroenterology. 2010;138:1681–96.PubMedCrossRef
19.
Barker 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 (Lond). 2009;457:608–11.CrossRef
20.
21.
Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009;27:1006–20.PubMedCentralPubMedCrossRef
22.
23.
McDonald SA, Greaves LC, Gutierrez-Gonzalez L, Rodriguez-Justo M, Deheragoda M, Leedham SJ, et al. Mechanisms of field cancerization in the human stomach: the expansion and spread of mutated gastric stem cells. Gastroenterology. 2008;134:500–10.PubMedCrossRef
24.
Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, Li H, et al. Gastric cancer originating from bone marrow-derived cells. Science. 2004;306:1568–71.PubMedCrossRef
25.
Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature (Lond). 2002;418:41–9.CrossRef
26.
27.
28.
Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J, Terzis AJ. Opinion: The origin of the cancer stem cell: current controversies and new insights. Nat Rev Cancer. 2005;5:899–904.PubMedCrossRef
29.
Johansson CB, Youssef S, Koleckar K, Holbrook C, Doyonnas R, Corbel SY, et al. Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat Cell Biol. 2008;10:575–83.PubMedCrossRef
30.
Nygren JM, Liuba K, Breitbach M, Stott S, Thorén L, Roell W, et al. Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat Cell Biol. 2008;10:584–92.PubMedCrossRef
31.
Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med. 2009;15:1010–2.PubMedCrossRef
32.
Hayashida T, Jinno H, Kitagawa Y, Kitajima M. Cooperation of cancer stem cell properties and epithelial–mesenchymal transition in the establishment of breast cancer metastasis. J Oncol. 2011;2011:591427.PubMedCentralPubMed
33.
Alison MR, Lim SM, Nicholson LJ. Cancer stem cells: problems for therapy? J Pathol. 2011;223:147–61.PubMed
34.
Fuxe J, Vincent T, Garcia de Herreros A. Transcriptional crosstalk between TGF-β and stem cell pathways in tumor cell invasion: role of EMT promoting Smad complexes. Cell Cycle. 2010;9:2363–74.PubMedCrossRef
35.
36.
Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S, et al. Epithelial–mesenchymal transition in cancer development and its clinical significance. Cancer Sci. 2010;101:293–9.PubMedCrossRef
37.
Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5:744–9.PubMedCrossRef
38.
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.PubMedCentralPubMedCrossRef
39.
Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY, et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells. 2009;27:2059–68.PubMedCrossRef
40.
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
41.
Ryu HS, Park DJ, Kim HH, Kim WH, Lee HS. Combination of epithelial–mesenchymal transition and cancer stem cell-like phenotypes has independent prognostic value in gastric cancer. Hum Pathol. 2012;43:520–8.PubMedCrossRef
42.
Chen T, Yang K, Yu J, Meng W, Yuan D, Bi F, et al. Identification and expansion of cancer stem cells in tumor tissues and peripheral blood derived from gastric adenocarcinoma patients. Cell Res. 2012;22:248–58.PubMedCrossRef
43.
Han ME, Jeon TY, Hwang SH, Lee YS, Kim HJ, Shim HE, et al. Cancer spheres from gastric cancer patients provide an ideal model system for cancer stem cell research. Cell Mol Life Sci. 2011;68:3589–605.PubMedCrossRef
44.
Dhingra S, Feng W, Brown RE, Zhou Z, Khoury T, Zhang R, et al. Clinicopathologic significance of putative stem cell markers, CD44 and nestin, in gastric adenocarcinoma. Int J Clin Exp Pathol. 2011;4:733–41.PubMedCentralPubMed
45.
Smith LM, Nesterova A, Ryan MC, Duniho S, Jonas M, Anderson M, et al. CD133/prominin-1 is a potential therapeutic target for antibody–drug conjugates in hepatocellular and gastric cancers. Br J Cancer. 2008;99:100–9.PubMedCentralPubMedCrossRef
46.
Wang T, Ong CW, Shi J, Srivastava S, Yan B, Cheng CL, et al. Sequential expression of putative stem cell markers in gastric carcinogenesis. Br J Cancer. 2011;105:658–65.PubMedCentralPubMedCrossRef
47.
Jiang J, Zhang Y, Chuai S, Wang Z, Zheng D, Xu F, et al. Trastuzumab (herceptin) targets gastric cancer stem cells characterized by CD90 phenotype. Oncogene. 2012;31:671–82.PubMedCrossRef
48.
Zhang C, Li C, He F, Cai Y, Yang H. Identification of CD44+CD24+ gastric cancer stem cells. J Cancer Res Clin Oncol. 2011;137:1679–86.PubMedCrossRef
49.
Xue Z, Yan H, Li J, Liang S, Cai X, Chen X, et al. Identification of cancer stem cells in vincristine preconditioned SGC7901 gastric cancer cell line. J Cell Biochem. 2012;113:302–12.PubMedCrossRef
50.
Hadnagy A, Gaboury L, Beaulieu R, Balicki D. SP analysis may be used to identify cancer stem cell populations. Exp Cell Res. 2006;312:3701–10.PubMedCrossRef
51.
Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood. 2002;99:507–12.PubMedCrossRef
52.
Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 2001;7:1028–34.PubMedCrossRef
53.
Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF, et al. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells. 2006;24:506–13.PubMedCrossRef
54.
Alison MR, Poulsom R, Brittan M, Schier S, Burkert J, Wright NA. Isolation of gut SP cells does not automatically enrich for stem cells. Gastroenterology. 2006;130:1012–4.PubMedCrossRef
55.
Fukuda K, Saikawa Y, Ohashi M, Kumagai K, Kitajima M, Okano H, et al. Tumor initiating potential of side population cells in human gastric cancer. Int J Oncol. 2009;34:1201–7.PubMed
56.
Schmuck R, Warneke V, Behrens HM, Simon E, Weichert W, Röcken C. Genotypic and phenotypic characterization of side population of gastric cancer cell lines. Am J Pathol. 2011;178:1792–804.PubMedCrossRef
57.
Nishii T, Yashiro M, Shinto O, Sawada T, Ohira M, Hirakawa K. Cancer stem cell-like SP cells have a high adhesion ability to the peritoneum in gastric carcinoma. Cancer Sci. 2009;100:1397–402.PubMedCrossRef
58.
Gil J, Stembalska A, Pesz KA, Sasiadek MM. Cancer stem cells: the theory and perspectives in cancer therapy. J Appl Genet. 2008;49:193–9.PubMedCrossRef
59.
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.PubMedCrossRef
60.
Platet N, Liu SY, Atifi ME, Oliver L, Vallette FM, Berger F, et al. Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett. 2007;258:286–90.PubMedCrossRef
61.
62.
63.
Saini V, Shoemaker RH. Potential for therapeutic targeting of tumor stem cells. Cancer Sci. 2010;101:16–21.PubMedCrossRef
64.
Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One. 2008;3:e2428.PubMedCentralPubMedCrossRef
65.
Johannessen TC, Bjerkvig R, Tysnes BB. DNA repair and cancer stem-like cells: potential partners in glioma drug resistance? Cancer Treat Rev. 2008;34:558–67.PubMedCrossRef
66.
Correia M, Machado JC, Ristimäki A. Basic aspects of gastric cancer. Helicobacter. 2009;14(s1):36–40.PubMedCrossRef
67.
Al-Hajj M. Cancer stem cells and oncology therapeutics. Curr Opin Oncol. 2007;19:61–4.PubMed
68.
Massard C, Deutsch E, Soria JC. Tumour stem cell-targeted treatment: elimination or differentiation. Ann Oncol. 2006;17:1620–4.PubMedCrossRef
69.
Cruz FD, Matushansky I. Solid tumor differentiation therapy—is it possible? Oncotarget. 2012;3:559–67.PubMed
70.
Ohno R, Asou N, Ohnishi K. Treatment of acute promyelocytic leukemia: strategy toward further increase of cure rate. Leukemia. 2003;17:1454–63.PubMedCrossRef
71.
Ginestier C, Wicinski J, Cervera N, Monville F, Finetti P, Bertucci F, et al. Retinoid signaling regulates breast cancer stem cell differentiation. Cell Cycle. 2009;8:3297–302.PubMedCentralPubMedCrossRef
72.
Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature (Lond). 2006;444:761–5.CrossRef
73.
Stojnev S, Pejcic M, Dolicanin Z, Velickovic LJ, Dimov I, Stefanovic V. Challenges of genomics and proteomics in nephrology. Ren Fail. 2009;31:765–72.PubMedCrossRef
74.
Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol. 2007;2:751–60.PubMedCrossRef
75.
Shigdar S, Lin J, Yu Y, Pastuovic M, Wei M, Duan W. RNA aptamer against a cancer stem cell marker epithelial cell adhesion molecule. Cancer Sci. 2011;102:991–8.PubMedCrossRef
76.
Lambert JM. Drug-conjugated monoclonal antibodies for the treatment of cancer. Curr Opin Pharmacol. 2005;5:543–9.PubMedCrossRef
77.
Chari RV. Targeted cancer therapy: conferring specificity to cytotoxic drugs. ACC Chem Res. 2008;41:98–107.PubMedCrossRef
78.
Baldus SE, Mönig SP, Zirbes TK, Thakran J, Köthe D, Köppel M, et al. Lewis (y) antigen (CD174) and apoptosis in gastric and colorectal carcinomas: correlations with clinical and prognostic parameters. Histol Histopathol. 2006;21:503–10.PubMed
79.
Boghaert ER, Sridharan L, Armellino DC, Khandke KM, DiJoseph JF, Kunz A, et al. Antibody-targeted chemotherapy with the calicheamicin conjugate hu3S193-N-acetyl gamma calicheamicin dimethyl hydrazide targets Lewis y and eliminates Lewis y-positive human carcinoma cells and xenografts. Clin Cancer Res. 2004;10:4538–49.PubMedCrossRef
80.
Scott AM, Tebbutt N, Lee FT, Cavicchiolo T, Liu Z, Gill S, et al. A phase I biodistribution and pharmacokinetic trial of humanized monoclonal antibody Hu3s193 in patients with advanced epithelial cancers that express the Lewis-Y antigen. Clin Cancer Res. 2007;13:3286–92.PubMedCrossRef
81.
Clavio M, Vignolo L, Albarello A, Varaldo R, Pierri I, Catania G, et al. Adding low-dose gemtuzumab ozogamicin to fludarabine, Ara-C and idarubicin (MY-FLAI) may improve disease-free and overall survival in elderly patients with non-M3 acute myeloid leukaemia: results of a prospective, pilot, multi-centre trial and comparison with a historical cohort of patients. Br J Haematol. 2007;138:186–95.PubMedCrossRef
82.
Katoh M. Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev. 2007;3:30–8.PubMedCrossRef
83.
Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.PubMedCrossRef
84.
Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature (Lond). 2004;432:324–31.CrossRef
85.
Kang DH, Han ME, Song MH, Lee YS, Kim EH, Kim HJ, et al. The role of hedgehog signaling during gastric regeneration. J Gastroenterol. 2009;44:372–9.PubMedCrossRef
86.
87.
Mutoh H, Hayakawa H, Sashikawa M, Sakamoto H, Sugano K. Direct repression of Sonic Hedgehog expression in the stomach by Cdx2 leads to intestinal transformation. Biochem J. 2010;427:423–34.PubMedCrossRef
88.
Sherman AE, Zavros Y. Role of Sonic Hedgehog signaling during progression from inflammation to cancer in the stomach. World J Gastrointest Pathophysiol. 2011;2:103–8.PubMedCentralPubMedCrossRef
89.
Zavros Y, Waghray M, Tessier A, Bai L, Todisco A, L Gumucio D, et al. Reduced pepsin A processing of sonic hedgehog in parietal cells precedes gastric atrophy and transformation. J Biol Chem. 2007;282:33265–332.PubMedCrossRef
90.
Xiao C, Ogle SA, Schumacher MA, Orr-Asman MA, Miller ML, Lertkowit N, et al. Loss of parietal cell expression of Sonic hedgehog induces hypergastrinemia and hyperproliferation of surface mucous cells. Gastroenterology. 2010;138:550–61.PubMedCrossRef
91.
Berman DM, Karhadkar SS, Maitra A, Montes De Oca R, Gerstenblith MR, Briggs K, et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature (Lond). 2003;425:846–51.CrossRef
92.
Lee KM, Lee JS, Jung HS, Park DK, Park HS, Hahm KB. Late reactivation of sonic hedgehog by Helicobacter pylori results in population of gastric epithelial cells that are resistant to apoptosis: implication for gastric carcinogenesis. Cancer Lett. 2010;287:44–53.PubMedCrossRef
93.
Li H, Fan X, Kovi RC, Jo Y, Moquin B, Konz R, et al. Spontaneous expression of embryonic factors and p53 point mutations in aged mesenchymal stem cells: a model of age related tumorigenesis in mice. Cancer Res. 2007;67:10889–98.PubMedCrossRef
94.
Martin J, Donnelly JM, Houghton J, Zavros Y. The role of sonic hedgehog reemergence during gastric cancer. Dig Dis Sci. 2010;55:1516–24.PubMedCrossRef
95.
Xu X, Zhang X, Wang S, Qian H, Zhu W, Cao H, et al. Isolation and comparison of mesenchymal stem-like cells from human gastric cancer and adjacent non-cancerous tissues. J Cancer Res Clin Oncol. 2011;137:495–504.PubMedCrossRef
96.
Fukaya M, Isohata N, Ohta H, Aoyagi K, Ochiya T, Saeki N, et al. Hedgehog signal activation in gastric pit cell and in diffuse type gastric cancer. Gastroenterology. 2006;131:14–29.PubMedCrossRef
97.
Song Z, Yue W, Wei B, Wang N, Li T, Guan L, et al. Sonic hedgehog pathway is essential for maintenance of cancer stem-like cells in human gastric cancer. PLoS One. 2011;6:e17687.PubMedCentralPubMedCrossRef
98.
99.
Scales SJ, de Sauvage FJ. Mechanisms of Hedgehog pathway activation in cancer and implications for therapy. Trends Pharmacol Sci. 2009;30:303–12.PubMedCrossRef
100.
Stanton BZ, Peng LF, Maloof N, Nakai K, Wang X, Duffner JL, et al. A small molecule that binds Hedgehog and blocks its signaling in human cells. Nat Chem Biol. 2009;5:154–6.PubMedCentralPubMedCrossRef
101.
Lauth M, Bergstrom A, Shimokawa T, Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small molecule antagonists. Proc Natl Acad Sci USA. 2007;104:8455–60.PubMedCrossRef
102.
Katoh M, Katoh M. Notch signaling in gastrointestinal tract. Int J Oncol. 2007;30:247–51.PubMed
103.
Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, et al. Notch signaling regulates stem cell numbers in vitro and in vivo. Nature (Lond). 2006;442:823–6.CrossRef
104.
Dang TP, Gazdar AF, Virmani AK, Sepetavec T, Hande KR, Minna JD, et al. Chromosome 19 translocation, overexpression of Notch3, and human lung cancer. J Natl Cancer Inst. 2000;92:1355–7.PubMedCrossRef
105.
Reedijk M, Odorcic S, Chang L, Zhang H, Miller N, McCready DR, et al. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res. 2005;65:8530–7.PubMedCrossRef
106.
Park JT, Li M, Nakayama K, Mao TL, Davidson B, Zhang Z, et al. Notch3 gene amplification in ovarian cancer. Cancer Res. 2006;66:6312–8.PubMedCrossRef
107.
Sekine A, Akiyama Y, Yanagihara K, Yuasa Y. Hath1 up-regulates gastric mucin gene expression in gastric cells. Biochem Biophys Res Commun. 2006;344:1166–71.PubMedCrossRef
108.
Piazzi G, Fini L, Selgrad M, Garcia M, Daoud Y, Wex T, et al. Epigenetic regulation of Delta-Like1 controls Notch1 activation in gastric cancer. Oncotarget. 2011;2:1291–301.PubMed
109.
Sun Y, Gao X, Liu J, Kong QY, Wang XW, Chen XY, et al. Differential Notch1 and Notch2 expression and frequent activation of Notch signaling in gastric cancers. Arch Pathol Lab Med. 2011;135:451–8.PubMed
110.
Sarmento LM, Barata JT. Therapeutic potential of Notch inhibition in T-cell acute lymphoblastic leukemia: rationale, caveats and promises. Expert Rev Anticancer Ther. 2011;11:1403–15.PubMedCrossRef
111.
112.
113.
Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, et al. PTEN dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature (Lond). 2006;441:475–82.CrossRef
114.
Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 2006;66:7445–52.PubMedCrossRef
115.
Lu D, Choi MY, Yu J, Castro JE, Kipps TJ, Carson DA. Salinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cells. Proc Natl Acad Sci USA. 2011;108:13253–7.PubMedCrossRef
116.
Clements WM, Wang J, Sarnaik A, Kim OJ, MacDonald J, Fenoglio-Preiser C, et al. Catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer. Cancer Res. 2002;62:3503–6.PubMed
117.
Katoh M, Katoh M. WNT signaling pathway and stem cell signaling network. Clin Cancer Res. 2007;13:4042–5.PubMedCrossRef
118.
Katoh M, Katoh M. Cross-talk of WNT and FGF signaling pathways at GSK3h to regulate h-catenin and SNAIL signaling cascade. Cancer Biol Ther. 2006;5:1059–64.PubMedCrossRef
119.
Cai C, Zhu X. The Wnt/β-catenin pathway regulates self-renewal of cancer stem-like cells in human gastric cancer. Mol Med Rep. 2012;5:1191–6.PubMed
120.
Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645–59.PubMedCrossRef
121.
Zhi QM, Chen XH, Ji J, Zhang JN, Li JF, Cai Q, et al. Salinomycin can effectively kill ALDH(high) stem-like cells on gastric cancer. Biomed Pharmacother. 2011;65:509–15.PubMedCrossRef
122.
123.
124.
125.
Zhang H, Yang MH, Zhao JJ, Chen L, Yu ST, Tang XD, et al. Inhibition of tankyrase 1 in human gastric cancer cells enhances telomere shortening by telomerase inhibitors. Oncol Rep. 2010;24:1059–65.PubMed
126.
Han MH, Kim GY, Moon SK, Kim WJ, Nam TJ, Choi YH. Apoptosis induction by glycoprotein isolated from Laminaria japonica is associated with down-regulation of telomerase activity and prostaglandin E2 synthesis in AGS human gastric cancer cells. Int J Oncol. 2011;38:577–84.PubMed
127.
Yao XX, Yin L, Sun ZC. The expression of hTERT mRNA and cellular immunity in gastric cancer and precancerosis. World J Gastroenterol. 2002;8:586–90.PubMed
128.
Lou H, Dean M. Targeted therapy for cancer stem cells: the patched pathway and ABC transporters. Oncogene. 2007;26:1357–60.PubMedCrossRef
129.
Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, et al. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res. 2005;65:4320–33.PubMedCrossRef
130.
131.
132.
Bissell MJ, Labarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell. 2005;7:17–23.PubMedCentralPubMed
133.
134.
Yang ZJ, Wechsler-Reya RJ. Hit ’em where they live: targeting the cancer stem cell niche. Cancer Cell. 2007;11:3–5.PubMedCrossRef
135.
Hombach-Klonisch S, Paranjothy T, Wiechec E, Pocar P, Mustafa T, Seifert A, et al. Cancer stem cells as targets for cancer therapy: selected cancers as examples. Arch Immunol Ther Exp. 2008;56:165–80.CrossRef
136.
Cao H, Xu W, Qian H, Zhu W, Yan Y, Zhou H, et al. Mesenchymal stem cell-like cells derived from human gastric cancer tissues. Cancer Lett. 2009;274:61–71.PubMedCrossRef
137.
Mishra PJ, Mishra PJ, Humeniuk R, Medina DJ, Alexe G, Mesirov JP, et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res. 2008;68:4331–9.PubMedCentralPubMedCrossRef
138.
Guo X, Oshima H, Kitmura T, Taketo MM, Oshima M. Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem. 2008;283:19864–71.PubMedCrossRef
139.
Hummel R, Hussey DJ, Haier J. MicroRNAs: predictors and modifiers of chemo- and radiotherapy in different tumour types. Eur J Cancer. 2010;46:298–311.PubMedCrossRef
140.
141.
Olmeda D, Jorda M, Peinado H, Fabra A, Cano A. Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene. 2010;26:1862–74.CrossRef
142.
Kim SU, Jeung EB, Kim YB, Cho MH, Choi KC. Potential tumor-tropic effect of genetically engineered stem cells expressing suicide enzymes to selectively target invasive cancer in animal models. Anticancer Res. 2011;31:1249–58.PubMed
143.
Kim KY, Yi BR, Lee HR, Kang NH, Jeung EB, Kim SU, et al. Stem cells with fused gene expression of cytosine deaminase and interferon-β migrate to human gastric cancer cells and result in synergistic growth inhibition for potential therapeutic use. Int J Oncol. 2012;40:1097–104.PubMed
Metadata
Title
Gastric cancer stem cells: therapeutic targets
Authors
Slavica Stojnev
Miljan Krstic
Ana Ristic-Petrovic
Vladisav Stefanovic
Takanori Hattori
Publication date
01-01-2014
Publisher
Springer Japan
Published in
Gastric Cancer / Issue 1/2014
Print ISSN: 1436-3291
Electronic ISSN: 1436-3305
DOI
https://doi.org/10.1007/s10120-013-0254-x

Other articles of this Issue 1/2014

Gastric Cancer 1/2014 Go to the issue

Original Article

Enhancement of 5-fluorouracil-induced cytotoxicity by leucovorin in 5-fluorouracil-resistant gastric cancer cells with upregulated expression of thymidylate synthase

Original Article

Comparison of advanced adenocarcinomas of esophagogastric junction and distal stomach in Japanese patients

Original Article

Treatment results of curative gastric resection from a specialist Australian unit: low volume with satisfactory outcomes

Original Article

Evaluation of HER2-based biology in 1,006 cases of gastric cancer in a Japanese population

Original Article

Long-term outcomes of patients who underwent limited proximal gastrectomy

Original Article

Feasibility of laparoscopy-assisted total gastrectomy in patients with clinical stage I gastric cancer

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits