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Identification of cancer stem cells: from leukemia to solid cancers |
Yinghui HUANG1( ), Xiaoxue QIU2, Ji-Long CHEN2( ) |
1. China-Japan Union Hospital of Jilin University, Changchun 130033, China; 2. CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences (CAS), Beijing 100101, China |
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Abstract Cancer stem cells (CSCs) are widely considered to be a small cell population in leukemia and many solid cancers with the properties including self-renewal and differentiation to non-tumorigenic cancer cells. Identification and isolation of CSCs significantly depend on the special surface markers of CSCs. Aberrant gene expression and signal transduction contribute to malignancies of CSCs, which result in cancer initiation, progression and recurrence. The inefficient therapy of cancers is mainly attributed to the failure of elimination of the malignant CSCs. However, CSCs have not been detected in all cancers and hierarchical organization of tumors might challenge cancer stem cell models. Additionally, opinions about the validity of the CSC hypothesis, the biological properties of CSCs, and the relevance of CSCs to cancer therapy differ widely. In this review, we discuss the debate of cancer stem cell model, the parameters by which CSCs can or cannot be defined, and the advances in the therapy of CSCs.
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Keywords
Cancer stem cell
leukemia
solid tumor
signal transduction
therapy
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Corresponding Author(s):
HUANG Yinghui,Email:yhuang@jlu.edu.cn; CHEN Ji-Long,Email:chenjl@im.ac.cn
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Issue Date: 01 October 2010
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1 |
Abraham B K, Fritz P, McClellan M, Hauptvogel P, Athelogou M, Brauch H (2005). Prevalence of CD44+/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin Cancer Res , 11(3): 1154–1159
|
2 |
Al-Hajj M, Wicha M S, Benito-Hernandez A, Morrison S J, Clarke M F (2003). Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A , 100(7): 3983–3988 doi: 10.1073/pnas.0530291100
|
3 |
Bissell M J, Labarge M A (2005). Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell , 7(1): 17–23
|
4 |
Blair A, Hogge D E, Ailles L E, Lansdorp P M, Sutherland H J (1997). Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood , 89(9): 3104–3112
|
5 |
Bonnet D, Dick J E (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med , 3(7): 730–737 doi: 10.1038/nm0797-730
|
6 |
Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005). Opinion: migrating cancer stem cells- an integrated concept of malignant tumour progression. Nat Rev Cancer , 5(9): 744–749 doi: 10.1038/nrc1694
|
7 |
Bruce W R, Van Der Gaag H (1963). A Quantitative Assay for the Number of Murine Lymphoma Cells Capable of Proliferation in Vivo. Nature , 199: 79–80 doi: 10.1038/199079a0
|
8 |
Bui M R, Hodson V, King T, Leopold D, Dai S, Fiolkoski V, Oakes S, Duke R, Apelian D, Franzusoff A, DeGregori J (2010). Mutation-specific control of BCR-ABL T315I positive leukemia with a recombinant yeast-based therapeutic vaccine in a murine model. Vaccine , 28(37): 6028–6035 doi: 10.1016/j.vaccine.2010.06.085
|
9 |
Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T (2008). A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep , 9(6): 582–589 doi: 10.1038/embor.2008.74
|
10 |
Campbell L L, Polyak K (2007). Breast tumor heterogeneity: cancer stem cells or clonal evolution? Cell Cycle , 6(19): 2332–2338 doi: 10.4161/cc.6.19.4914
|
11 |
Carpten J D, Faber A L, Horn C, Donoho G P, Briggs S L, Robbins C M, Hostetter G, Boguslawski S, Moses T Y, Savage S, Uhlik M, Lin A, Du J, Qian Y W, Zeckner D J, Tucker-Kellogg G, Touchman J, Patel K, Mousses S, Bittner M, Schevitz R, Lai M H, Blanchard K L, Thomas J E (2007). A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature , 448(7152): 439–444 doi: 10.1038/nature05933
|
12 |
Chen J L, Limnander A, Rothman P B (2008). Pim-1 and Pim-2 kinases are required for efficient pre-B-cell transformation by v-Abl oncogene. Blood , 111(3): 1677–1685 doi: 10.1182/blood-2007-04-083808
|
13 |
Clarke M F, Dick J E, Dirks P B, Eaves C J, Jamieson C H, Jones D L, Visvader J, Weissman I L, Wahl G M (2006). Cancer stem cells–perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res , 66, 9339–9344 doi: 10.1158/0008-5472.CAN-06-3126
|
14 |
Collins A T, Berry P A, Hyde C, Stower M J, Maitland N J (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res , 65(23): 10946–10951 doi: 10.1158/0008-5472.CAN-05-2018
|
15 |
Deininger M W, Goldman J M, Melo J V (2000). The molecular biology of chronic myeloid leukemia. Blood , 96(10): 3343–3356
|
16 |
Druker B J, Talpaz M, Resta D J, Peng B, Buchdunger E, Ford J M, Lydon N B, Kantarjian H, Capdeville R, Ohno-Jones S, Sawyers C L (2001). Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med , 344(14): 1031–1037 doi: 10.1056/NEJM200104053441401
|
17 |
Fang D, Nguyen T K, Leishear K, Finko R, Kulp A N, Hotz S, Van Belle P A, Xu X, Elder D E, Herlyn M (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res , 65(20): 9328–9337 doi: 10.1158/0008-5472.CAN-05-1343
|
18 |
Ginestier C, Hur M H, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer C G, Liu S, Schott A, Hayes D, Birnbaum D, Wicha M S, Dontu G (2007). ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell , 1(5): 555–567 doi: 10.1016/j.stem.2007.08.014
|
19 |
Gregory M A, Phang T L, Neviani P, Alvarez-Calderon F, Eide C A, O’Hare T, Zaberezhnyy V, Williams R T, Druker B J, Perrotti D, Degregori J (2010). Wnt/Ca2+/NFAT signaling maintains survival of Ph+ leukemia cells upon inhibition of Bcr-Abl. Cancer Cell , 18(1): 74–87 doi: 10.1016/j.ccr.2010.04.025
|
20 |
Gregory P A, Bracken C P, Bert A G, Goodall G J (2008). MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle , 7(20): 3112–3118
|
21 |
Guo G, Qiu X, Wang S, Chen Y, Rothman P B, Wang Z, Chen Y, Wang G, Chen J L (2010). Oncogenic E17K mutation in the pleckstrin homology domain of AKT1 promotes v-Abl-mediated pre-B-cell transformation and survival of Pim-deficient cells. Oncogene , 29(26): 3845–3853 doi: 10.1038/onc.2010.149
|
22 |
Gutierrez A, Sanda T, Grebliunaite R, Carracedo A, Salmena L, Ahn Y, Dahlberg S, Neuberg D, Moreau L A, Winter S S, Larson R, Zhang J, Protopopov A, Chin L, Pandolfi P P, Silverman L B, Hunger S P, Sallan S E, Look A T (2009). High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Blood , 114(3): 647–650 doi: 10.1182/blood-2009-02-206722
|
23 |
Guzman M L, Jordan C T (2004). Considerations for targeting malignant stem cells in leukemia. Cancer Control , 11(2): 97–104
|
24 |
Haan S, Wüller S, Kaczor J, Rolvering C, N?cker T, Behrmann I, Haan C (2009). SOCS-mediated downregulation of mutant Jak2 (V617F, T875N and K539L) counteracts cytokine-independent signaling. Oncogene , 28(34): 3069–3080 doi: 10.1038/onc.2009.155
|
25 |
Hemmati H D, Nakano I, Lazareff J A, Masterman-Smith M, Geschwind D H, Bronner-Fraser M, Kornblum H I (2003). Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A , 100(25): 15178–15183 doi: 10.1073/pnas.2036535100
|
26 |
Herman S E, Gordon A L, Wagner A J, Heerema N A, Zhao W, Flynn J M, Jones J, Andritsos L, Puri K D, Lannutti B J, Giese N A, Zhang X, Wei L, Byrd J C, Johnson A J (2010). The phosphatidylinositol 3-kinase-{delta} inhibitor CAL-101 demonstrates promising pre-clinical activity in chronic lymphocytic leukemia by antagonizing intrinsic and extrinsic cellular survival signals. Blood , 2010(Jun): 3 (Epub ahead of print)
|
27 |
Hermann P C, Huber S L, Herrler T, Aicher A, Ellwart J W, Guba M, Bruns C J, Heeschen C (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell , 1(3): 313–323 doi: 10.1016/j.stem.2007.06.002
|
28 |
Hu Z, Pan X F, Wu F Q, Ma L Y, Liu D P, Liu Y, Feng T T, Meng F Y, Liu X L, Jiang Q L, Chen X Q, Liu J L, Liu P, Chen Z, Chen S J, Zhou G B (2009). Synergy between proteasome inhibitors and imatinib mesylate in chronic myeloid leukemia. PLoS One , 4(7): e6257 doi: 10.1371/journal.pone.0006257
|
29 |
Ito K, Bernardi R, Morotti A, Matsuoka S, Saglio G, Ikeda Y, Rosenblatt J, Avigan D E, Teruya-Feldstein J, Pandolfi P P (2008). PML targeting eradicates quiescent leukaemia-initiating cells. Nature , 453(7198): 1072–1078 doi: 10.1038/nature07016
|
30 |
Jabbour E, Cortes J, Kantarjian H (2010). Nilotinib for the treatment of chronic myeloid leukemia: An evidence-based review. Core Evid , 4: 207–213
|
31 |
Jamieson C H, Ailles L E, Dylla S J, Muijtjens M, Jones C, Zehnder J L, Gotlib J, Li K, Manz M G, Keating A, Sawyers C L, Weissman I L (2004). Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med , 351(7): 657–667 doi: 10.1056/NEJMoa040258
|
32 |
Jiang X, Forrest D, Nicolini F, Turhan A, Guilhot J, Yip C, Holyoake T, Jorgensen H, Lambie K, Saw K M, Pang E, Vukovic R, Lehn P, Ringrose A, Yu M, Brinkman R R, Smith C, Eaves A, Eaves C (2010). Properties of CD34+ CML stem/progenitor cells that correlate with different clinical responses to imatinib mesylate. Blood , 116(12): 2112–2121 doi: 10.1182/blood-2009-05-222471
|
33 |
Jordan C T, Upchurch D, Szilvassy S J, Guzman M L, Howard D S, Pettigrew A L, Meyerrose T, Rossi R, Grimes B, Rizzieri D A, Luger S M, Phillips G L (2000). The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia , 14(10): 1777–1784 doi: 10.1038/sj.leu.2401903
|
34 |
J?rgensen H G, Holyoake T L (2007). Characterization of cancer stem cells in chronic myeloid leukaemia. Biochem Soc Trans , 35(Pt 5): 1347–1351
|
35 |
Karnoub A E, Dash A B, Vo A P, Sullivan A, Brooks M W, Bell G W, Richardson A L, Polyak K, Tubo R, Weinberg R A (2007). Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature , 449(7162): 557–563 doi: 10.1038/nature06188
|
36 |
Kelly P N, Dakic A, Adams J M, Nutt S L, Strasser A (2007). Tumor growth need not be driven by rare cancer stem cells. Science , 317(5836): 337 doi: 10.1126/science.1142596
|
37 |
Kharas M G, Okabe R, Ganis J J, Gozo M, Khandan T, Paktinat M, Gilliland D G, Gritsman K (2010). Constitutively active AKT depletes hematopoietic stem cells and induces leukemia in mice. Blood , 115(7): 1406–1415 doi: 10.1182/blood-2009-06-229443
|
38 |
Kim C F, Jackson E L, Woolfenden A E, Lawrence S, Babar I, Vogel S, Crowley D, Bronson R T, Jacks T (2005). Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell , 121(6): 823–835
|
39 |
Kim K Y, Kim S U, Leung P C, Jeung E B, Choi K C (2010). Influence of the prodrugs 5-fluorocytosine and CPT-11 on ovarian cancer cells using genetically engineered stem cells: tumor-tropic potential and inhibition of ovarian cancer cell growth. Cancer Sci , 101(4): 955–962 doi: 10.1111/j.1349-7006.2009.01485.x
|
40 |
Krause D S, Lazarides K, von Andrian U H, Van Etten R A (2006). Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells. Nat Med , 12(10): 1175–1180 doi: 10.1038/nm1489
|
41 |
Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, Huelsken J (2008). Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature , 452(7187): 650–653 doi: 10.1038/nature06835
|
42 |
Mani S A, Guo W, Liao M J, Eaton E N, Ayyanan A, Zhou A Y, Brooks M, Reinhard F, Zhang C C, Shipitsin M, Campbell L L, Polyak K, Brisken C, Yang J, Weinberg R A (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell , 133(4): 704–715
|
43 |
Mantovani A (2009). Cancer: Inflaming metastasis. Nature , 457(7225): 36–37 doi: 10.1038/457036b
|
44 |
Moshaver B, van Rhenen A, Kelder A, van der Pol M, Terwijn M, Bachas C, Westra A H, Ossenkoppele G J, Zweegman S, Schuurhuis G J (2008). Identification of a small subpopulation of candidate leukemia initiating cells in the side population (sp) of patients with acute myeloid leukemia. Stem Cells .
|
45 |
Murray P J (2007). The JAK-STAT signaling pathway: input and output integration. J Immunol , 178(5): 2623–2629
|
46 |
Nasr R, Guillemin M C, Ferhi O, Soilihi H, Peres L, Berthier C, Rousselot P, Robledo-Sarmiento M, Lallemand-Breitenbach V, Gourmel B, Vitoux D, Pandolfi P P, Rochette-Egly C, Zhu J, de Thé H (2008). Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat Med , 14(12): 1333–1342 doi: 10.1038/nm.1891
|
47 |
Nusse R (2003). Wnts and Hedgehogs: lipid-modified proteins and similarities in signaling mechanisms at the cell surface. Development , 130(22): 5297–5305 doi: 10.1242/dev.00821
|
48 |
O’Brien C A, Pollett A, Gallinger S, Dick J E (2007). A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature , 445(7123): 106–110 doi: 10.1038/nature05372
|
49 |
Peng C, Chen Y, Yang Z, Zhang H, Osterby L, Rosmarin A G, Li S (2010). PTEN is a tumor suppressor in CML stem cells and BCR-ABL-induced leukemias in mice. Blood , 115(3): 626–635 doi: 10.1182/blood-2009-06-228130
|
50 |
Piccirillo S G, Reynolds B A, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F, Vescovi A L (2006). Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature , 444(7120): 761–765 doi: 10.1038/nature05349
|
51 |
Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti M A, Daidone M G (2005). Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res , 65(13): 5506–5511 doi: 10.1158/0008-5472.CAN-05-0626
|
52 |
Pradhan A, Lambert Q T, Reuther G W (2007). Transformation of hematopoietic cells and activation of JAK2-V617F by IL-27R, a component of a heterodimeric type I cytokine receptor. Proc Natl Acad Sci U S A , 104(47): 18502–18507 doi: 10.1073/pnas.0702388104
|
53 |
Quintana E, Shackleton M, Sabel M S, Fullen D R, Johnson T M, Morrison S J (2008). Efficient tumour formation by single human melanoma cells. Nature , 456(7222): 593–598 doi: 10.1038/nature07567
|
54 |
Reya T, Duncan A W, Ailles L, Domen J, Scherer D C, Willert K, Hintz L, Nusse R, Weissman I L (2003). A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature , 423(6938): 409–414 doi: 10.1038/nature01593
|
55 |
Reya T, Morrison S J, Clarke M F, Weissman I L (2001). Stem cells, cancer, and cancer stem cells. Nature , 414(6859): 105–111 doi: 10.1038/35102167
|
56 |
Savona M, Talpaz M (2008). Getting to the stem of chronic myeloid leukaemia. Nat Rev Cancer , 8(5): 341–350 doi: 10.1038/nrc2368
|
57 |
Singh S K, Hawkins C, Clarke I D, Squire J A, Bayani J, Hide T, Henkelman R M, Cusimano M D, Dirks P B (2004). Identification of human brain tumour initiating cells. Nature , 432(7015): 396–401 doi: 10.1038/nature03128
|
58 |
Szotek P P, Pieretti-Vanmarcke R, Masiakos P T, Dinulescu D M, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin D T, Donahoe P K (2006). Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci U S A , 103(30): 11154–11159 doi: 10.1073/pnas.0603672103
|
59 |
Thiery J P (2002). Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer , 2(6): 442–454 doi: 10.1038/nrc822
|
60 |
Tian E, Zhan F, Walker R, Rasmussen E, Ma Y, Barlogie B, Shaughnessy J D Jr (2003). The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N Engl J Med , 349(26): 2483–2494 doi: 10.1056/NEJMoa030847
|
61 |
van der Pol M A, Feller N, Roseboom M, Moshaver B, Westra G, Broxterman H J, Ossenkoppele G J, Schuurhuis G J (2003). Assessment of the normal or leukemic nature of CD34+ cells in acute myeloid leukemia with low percentages of CD34 cells. Haematologica , 88(9): 983–993
|
62 |
van Noort M, Meeldijk J, van der Zee R, Destree O, Clevers H (2002). Wnt signaling controls the phosphorylation status of beta-catenin. J Biol Chem , 277(20): 17901–17905 doi: 10.1074/jbc.M111635200
|
63 |
Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler M U, Ganser A, Eder M, Scherr M (2007). Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood , 109(10): 4399–4405 doi: 10.1182/blood-2006-09-045104
|
64 |
Viswanathan S R, Daley G Q, Gregory R I (2008). Selective blockade of microRNA processing by Lin28. Science , 320(5872): 97–100 doi: 10.1126/science.1154040
|
65 |
Wang J C, Dick J E (2005). Cancer stem cells: lessons from leukemia. Trends Cell Biol , 15(9): 494–501 doi: 10.1016/j.tcb.2005.07.004
|
66 |
Wang Y, Krivtsov A V, Sinha A U, North T E, Goessling W, Feng Z, Zon L I, Armstrong S A (2010). The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science , 327(5973): 1650–1653 doi: 10.1126/science.1186624
|
67 |
Williams R T, den Besten W, Sherr C J (2007). Cytokine-dependent imatinib resistance in mouse BCR-ABL+, Arf-null lymphoblastic leukemia. Genes Dev , 21(18): 2283–2287 doi: 10.1101/gad.1588607
|
68 |
Wong D J, Liu H, Ridky T W, Cassarino D, Segal E, Chang H Y (2008). Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell , 2(4): 333–344 doi: 10.1016/j.stem.2008.02.009
|
69 |
Wuchter C, Ratei R, Spahn G, Schoch C, Harbott J, Schnittger S, Haferlach T, Creutzig U, Sperling C, Karawajew L, Ludwig W D (2001). Impact of CD133 (AC133) and CD90 expression analysis for acute leukemia immunophenotyping. Haematologica , 86(2): 154–161
|
70 |
Yang Y M, Chang J W (2008). Current status and issues in cancer stem cell study. Cancer Invest , 26(7): 741–755 doi: 10.1080/07357900801901856
|
71 |
Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E (2007). let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell , 131(6): 1109–1123
|
72 |
Zhang B, Strauss A C, Chu S, Li M, Ho Y, Shiang K D, Snyder D S, Huettner C S, Shultz L, Holyoake T, Bhatia R (2010). Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell , 17(5): 427–442 doi: 10.1016/j.ccr.2010.03.011
|
73 |
Zhao C, Blum J, Chen A, Kwon H Y, Jung S H, Cook J M, Lagoo A, Reya T (2007). Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell , 12(6): 528–541 doi: 10.1016/j.ccr.2007.11.003
|
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