Cancer stem cells: Targeting the roots of cancer, seeds of metastasis, and sources of therapy resistance

Cancer Research

Volumn 75, Issue 6, 2015, Pages 924-929

  Adorno Cruz, Valery ^a   Kibria, Golam ^a   Liu, Xia ^a   Doherty, Mary ^a   Junk, Damian J ^a   Guan, Dongyin ^a   Hubert, Chris ^b   Venere, Monica ^b   Mulkearns Hubert, Erin ^b   Sinyuk, Maksim ^b   Alvarado, Alvaro ^b   Caplan, Arnold I ^a   Rich, Jeremy ^a,b,c   Gerson, Stanton L ^a,c   Lathia, Justin ^a,b,c   Liu, Huiping ^a,c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; ANTINEOPLASTIC AGENT; BRONTICTUZUMAB; CD47 ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DECITABINE; DEMCIZUMAB; EPHRIN RECEPTOR A2; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GUADECITABINE; LITHIUM; NAPABUCASIN; PACLITAXEL; RETINOIC ACID; TRANSCRIPTION FACTOR; TRASTUZUMAB; VANTICTUMAB; VISMODEGIB;

ACUTE MYELOBLASTIC LEUKEMIA; BREAST TUMOR; CANCER RESISTANCE; CANCER STEM CELL; CELL RENEWAL; CIRCULATING TUMOR CELL; COLON CANCER; CONFERENCE PAPER; CYTOKINE RELEASE; DNA METHYLATION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM TUMOR; GLIOBLASTOMA; GLIOMA STEM CELL; HUMAN; IMMUNE EVASION; LEUKEMIA REMISSION; LEUKEMOGENESIS; METASTASIS; METASTASIS POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SELF RENEWAL; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; DRUG EFFECTS; DRUG RESISTANCE; GENETIC EPIGENESIS; PHYSIOLOGY;

DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; HUMANS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; TUMOR MICROENVIRONMENT;

EID: 84933283091     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3225     Document Type: Conference Paper

References (65)

1. Furth J, Kahn MC. The transmission of leukemia of mice with a single cell. Cancer Res 1937:276-82.
2. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997;3:730-7.
3. 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.
4. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100:3983-8.
5. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444:756-60.
6. Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature 2013;501:328-37.
7. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012;488:522-6.
8. Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell 2014;14:275-91.
9. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
10. Jan M, Snyder TM, Corces-Zimmerman MR, Vyas P, Weissman IL, Quake SR, et al. Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci Transl Med 2012;4:149ra18.
11. Chao MP, Weissman IL, Majeti R. The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications. Curr Opin Immunol 2012;24:225-32.
12. Adorno M, Sikandar S, Mitra SS, Kuo A, Nicolis Di Robilant B, Haro-Acosta V, et al. Usp16 contributes to somatic stem-cell defects in Down's syndrome. Nature 2013;501:380-4.
13. Chen J, McKay RM, Parada LF. Malignant glioma: lessons from genomics, mouse models, and stem cells. Cell 2012;149:36-47.
14. Wang ZA, Toivanen R, Bergren SK, Chambon P, Shen MM. Luminal cells are favored as the cell of origin for prostate cancer. Cell Rep 2014;8:1339-46.
15. Salz HK. Sex, stem cells and tumors in the Drosophila ovary. Fly 2013;7:3-7.
16. Zhang X, Guo A, Yu J, Possemato A, Chen Y, Zheng W, et al. Identification of STAT3 as a substrate of receptor protein tyrosine phosphatase T. Proc Natl Acad Sci U S A 2007;104:4060-4.
17. Singh D, Chan JM, Zoppoli P, Niola F, Sullivan R, Castano A, et al. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 2012;337:1231-5.
18. Liu Y, Gilbert MR, Kyprianou N, Rangnekar VM, Horbinski C. The tumor suppressor prostate apoptosis response-4 (Par-4) is regulated by mutant IDH1 and kills glioma stem cells. Acta Neuropathol 2014;128:723-32.
19. Suva ML, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H, Rabkin SD, et al. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 2014;157:580-94.
20. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014;344:1396-401.
21. Jiang Q, Crews LA, Barrett CL, Chun HJ, Court AC, Isquith JM, et al. ADAR1 promotes malignant progenitor reprogramming in chronic myeloid leukemia. Proc Natl Acad Sci U S A 2013;110:1041-6.
22. Mack SC, Witt H, Piro RM, Gu L, Zuyderduyn S, Stutz AM, et al. Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 2014;506:445-50.
23. Kim E, Kim M, Woo DH, Shin Y, Shin J, Chang N, et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell 2013;23:839-52.
24. Lotti F, Jarrar AM, Pai RK, Hitomi M, Lathia J, Mace A, et al. Chemotherapy activates cancer-associated fibroblasts to maintain colorectal cancer-initiating cells by IL-17A. J Exp Med 2013;210:2851-72.
25. Caplan AI. All MSCs are pericytes? Cell Stem Cell 2008;3:229-30.
26. Correa D, Lin P, Somoza R, Schiemann WP, Caplan AI. Bone marrow mesenchymal stem cells (BM-MSCs) regulate melanoma cancer cell extravasation at their perivascular niche. (Submitted) 2015.
27. Xiao H, Lasser C, Shelke G, Wang J, Radinger M, Lunavat T, et al. Mast cell exosomes promote lung adenocarcinoma cell proliferation inverted question mark role of KIT-stem cell factor signaling. Cell Commun Signal 2014;12:64.
28. Li B, Qiu B, Lee DS, Walton ZE, Ochocki JD, Mathew LK, et al. Fructose-1,6-bisphosphatase opposes renal carcinoma progression. Nature 2014;513:251-5.
29. Mathew LK, Skuli N, Mucaj V, Lee SS, Zinn PO, Sathyan P, et al. miR-218 opposes a critical RTK-HIF pathway in mesenchymal glioblastoma. Proc Natl Acad Sci U S A 2014;111:291-6.
30. Fack F, Espedal H, Keunen O, Golebiewska A, Obad N, Harter PN, et al. Bevacizumab treatment induces metabolic adaptation toward anaerobic metabolism in glioblastomas. Acta Neuropathol 2015;129:115-31.
31. Sakariassen PO, Prestegarden L, Wang J, Skaftnesmo KO, Mahesparan R, Molthoff C, et al. Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc Natl Acad Sci U S A 2006;103:16466-71.
32. Zheng Q, Banaszak L, Fracci S, Basali D, Dunlap SM, Hursting SD, et al. Leptin receptor maintains cancer stem-like properties in triple negative breast cancer cells. Endocr Relat Cancer 2013;20:797-808.
33. Chen S, Huang EH. The colon cancer stem cell microenvironment holds keys to future cancer therapy. J Gastrointest Surg 2014;18:1040-8.
34. Yang H, Liu Y, Bai F, Zhang JY, Ma SH, Liu J, et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene 2013;32:663-9.
35. Myers JT, Barkauskas DS, Huang AY. Dynamic imaging of marrow-resident granulocytes interacting with human mesenchymal stem cells upon systemic lipopolysaccharide challenge. Stem Cells Int 2013;2013:656839.
36. Sinkevicius KW, Kriegel C, Bellaria KJ, Lee J, Lau AN, Leeman KT, et al. Neurotrophin receptor TrkB promotes lung adenocarcinoma metastasis. Proc Natl Acad Sci U S A 2014;111:10299-304.
37. Lee JH, Bhang DH, Beede ang TL, Stripp BR, Bloch KD, et al. Lung stem cell differentiation in mice directed by endothelial cells via a BMP4-NFATc1-thrombospondin-1 axis. Cell 2014;156:440-55.
38. Kreso A, van Galen P, Pedley NM, Lima-Fernandes E, Frelin C, Davis T, et al. Self-renewal as a therapeutic target in human colorectal cancer. Nat Med 2014;20:29-36.
39. Bernardo GM, Keri RA. FOXA1: a transcription factor with parallel functions in development and cancer. Biosci Rep 2012;32:113-30.
40. Sizemore ST, Keri RA. The forkhead box transcription factor FOXC1 promotes breast cancer invasion by inducing matrix metalloprotease 7 (MMP7) expression. J Biol Chem 2012;287:24631-40.
41. Patsialou A, Bravo-Cordero JJ, Wang Y, Entenberg D, Liu H, Clarke M, et al. Intravital multiphoton imaging reveals multicellular streaming as a crucial component of in vivo cell migration in human breast tumors. Intravital 2013;2:e25294.
42. Gligorijevic B, Bergman A, Condeelis J. Multiparametric classification links tumor microenvironments with tumor cell phenotype. PLoS Biol 2014;12:e1001995.
43. Bockhorn J, Dalton R, Nwachukwu C, Huang S, Prat A, Yee K, et al. MicroRNA-30c inhibits human breast tumour chemotherapy resistance by regulating TWF1 and IL-11. Nat Commun 2013;4:1393.
44. Bockhorn J, Prat A, Chang Y-F, Liu X, Huang S, Shang M, et al. Differentiation and loss of malignant character of spontaneous pulmonary metastases in patient-derived breast cancer models. Cancer Res 2014;74:7406-17.
45. Fiori ME, Barbini C, Haas TL, Marroncelli N, Patrizii M, Biffoni M, et al. Antitumor effect of miR-197 targeting in p53 wild-type lung cancer. Cell Death Differ 2014;21:774-82.
46. Todaro M, Gaggianesi M, Catalano V, Benfante A, Iovino F, Biffoni M, et al. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell 2014;14:342-56.
47. Wan L, Lu X, Yuan S, Wei Y, Guo F, Shen M, et al. MTDH-SND1 interaction is crucial for expansion and activity of tumor-initiating cells in diverse oncogene- and carcinogen-induced mammary tumors. Cancer Cell 2014;26:92-105.
48. Bu P, Chen KY, Chen JH, Wang L, Walters J, Shin YJ, et al. A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells. Cell Stem Cell 2013;12:602-15.
49. Yu M, Bardia A, Aceto N, Bersani F, Madden MW, Donaldson MC, et al. Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 2014;345:216-20.
50. Dago AE, Stepansky A, Carlsson A, Luttgen M, Kendall J, Baslan T, et al. Rapid phenotypic and genomic change in response to therapeutic pressure in prostate cancer inferred by high content analysis of single circulating tumor cells. PLoS ONE 2014;9:e101777.
51. Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, et al. The PSA(-/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell 2012;10:556-69.
52. Lerner RG, Petritsch C. A microRNA-operated switch of asymmetric-to-symmetric cancer stem cell divisions. Nat Cell Biol 2014;16:212-4.
53. Ito T, Kwon HY, Zimdahl B, Congdon KL, Blum J, Lento WE, et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 2010;466:765-8.
54. Carruthers R, Ahmed SU, Strathdee K, Gomez-Roman N, Amoah-Buahin E, Watts C, et al. Abrogation of radioresistance in glioblastoma stem-like cells by inhibition of ATM kinase. Mol Oncol 2015;9:192-203.
55. Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A 2013;110:4009-14.
56. Mao P, Joshi K, Li J, Kim SH, Li P, Santana-Santos L, et al. Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3. Proc Natl Acad Sci U S A 2013;110:8644-9.
57. Scott JG, Hjelmeland AB, Chinnaiyan P, Anderson AR, Basanta D. Microenvironmental variables must influence intrinsic phenotypic parameters of cancer stem cells to affect tumourigenicity. PLoS Comput Biol 2014;10:e1003433.
58. Shi Y, Chen C, Zhang X, Liu Q, Xu JL, Zhang HR, et al. Primate-specific miR-663 functions as a tumor suppressor by targeting PIK3CD and predicts the prognosis of human glioblastoma. Clin Cancer Res 2014;20:1803-13.
59. Miao H, Gale NW, Guo H, Qian J, Petty A, Kaspar J, et al. EphA2 promotes infiltrative invasion of glioma stem cells in vivo through cross-talk with Akt and regulates stem cell properties. Oncogene 2015;34:558-67.
60. Li Z, Chen J. In vitro functional study of miR-126 in leukemia. Methods Mol Biol 2011;676:185-95.
61. Gupta K, Gulen F, Sun L, Aguilera R, Chakrabarti A, Kiselar J, et al. GSK3 is a regulator of RAR-mediated differentiation. Leukemia 2012;26:1277-85.
62. Gu X, Hu Z, Ebrahem Q, Crabb JS, Mahfouz RZ, Radivoyevitch T, et al. Runx1 regulation of Pu.1 corepressor/coactivator exchange identifies specific molecular targets for leukemia differentiation therapy. J Biol Chem 2014;289:14881-95.
63. Saunthararajah Y, Boccuni P, Nucifora G. Combinatorial action of RUNX1 and PU.1 in the regulation of hematopoiesis. Crit Rev Eukaryot Gene Expr 2006;16:183-92.
64. Wang Y, Cardenas H, Fang F, Condello S, Taverna P, Segar M, et al. Epigenetic targeting of ovarian cancer stem cells. Cancer Res 2014;74:4922-36.
65. Gurney A, Axelrod F, Bond CJ, Cain J, Chartier C, Donigan L, et al. Wnt pathway inhibition via the targeting of Frizzled receptors results in decreased growth and tumorigenicity of human tumors. Proc Natl Acad Sci U S A 2012;109:11717-22.