Cancer stem cell marker phenotypes are reversible and functionally homogeneous in a preclinical model of pancreatic cancer

Cancer Research

Volumn 75, Issue 21, 2015, Pages 4582-4592

  Dosch, Joseph S ^a,b   Ziemke, Elizabeth K ^a,b   Shettigar, Amrith ^a,b   Rehemtulla, Alnawaz ^b   Sebolt Leopold, Judith S ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; GEMCITABINE; SALINOMYCIN; ANTINEOPLASTIC ANTIMETABOLITE; CD133 ANTIGEN; CD24 ANTIGEN; CD24A PROTEIN, MOUSE; DEOXYCYTIDINE; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; LUCIFERASE; LY ANTIGEN; LY6A PROTEIN, MOUSE; MEMBRANE PROTEIN; PEPTIDE; PROM1 PROTEIN, HUMAN; PROM1 PROTEIN, MOUSE; PROTEIN P21; PROTEIN P53; PYRAN DERIVATIVE; TUMOR MARKER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; CANCER STEM CELL; CARCINOGENICITY; CELL HETEROGENEITY; CELL ISOLATION; CELL SUBPOPULATION; CHEMOSENSITIVITY; CHEMOTHERAPY; CLONOGENIC ASSAY; CONTROLLED STUDY; FLOW CYTOMETRY; HISTOLOGY; IN VIVO STUDY; MONOLAYER CULTURE; MOUSE; NONHUMAN; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PHENOTYPE; PRIORITY JOURNAL; TUMOR SPHEROID; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL TRANSFORMATION; DISEASE MODEL; EXPERIMENTAL NEOPLASM; GENETICS; METABOLISM; MULTICELLULAR SPHEROID; PANCREAS; PANCREAS TUMOR; PATHOLOGY; STAINING; TRANSGENIC MOUSE; TUMOR CELL CULTURE;

AC133 ANTIGEN; ANIMALS; ANTIGENS, CD; ANTIGENS, CD24; ANTIGENS, LY; ANTIMETABOLITES, ANTINEOPLASTIC; BIOMARKERS, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DEOXYCYTIDINE; DISEASE MODELS, ANIMAL; GLYCOPROTEINS; LUCIFERASES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; NEOPLASTIC STEM CELLS; PANCREAS; PANCREATIC NEOPLASMS; PEPTIDES; PHENOTYPE; PROTO-ONCOGENE PROTEINS P21(RAS); PYRANS; SPHEROIDS, CELLULAR; STAINING AND LABELING; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84946542139     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2793     Document Type: Article

References (46)

1. Dick JE. Stem cell concepts renew cancer research. Blood 2008;112: 4793-807.
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. 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.
4. 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 U S A 2007;104:10158-63.
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. 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.
7. 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.
8. Liu H, Patel MR, Prescher JA, Patsialou A, Qian D, Lin J, et al. Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models. Proc Natl Acad Sci U S A 2010;107:18115-20.
9. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009;458:780-3.
10. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO, et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci U S A 2011;108:7950-5.
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.
12. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature 2008;456:593-8.
13. Held MA, Curley DP, Dankort D, McMahon M, Muthusamy V, Bosenberg MW. Characterization of melanoma cells capable of propagating tumors from a single cell. Cancer Res 2010;70:388-97.
14. Buchstaller J, McKeever PE, Morrison SJ. Tumorigenic cells are common in mouse MPNSTs but their frequency depends upon tumor genotype and assay conditions. Cancer Cell 2012;21:240-52.
15. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009; 324:1457-61.
16. Tseng WW, Winer D, Kenkel JA, Choi O, Shain AH, Pollack JR, et al. Development of an orthotopic model of invasive pancreatic cancer in an immunocompetent murine host. Clin Cancer Res 2010;16: 3684-95.
17. Gu G, Brown JR, Melton DA. Direct lineage tracing reveals the ontogeny of pancreatic cell fates during mouse embryogenesis. Mech Dev 2003;120: 35-43.
18. Ishizawa K, Rasheed ZA, Karisch R, Wang Q, Kowalski J, Susky E, et al. Tumor-initiating cells are rare in many human tumors. Cell Stem Cell 2010;7:279-82.
19. Li C, Wu JJ, Hynes M, Dosch J, Sarkar B, Welling TH, et al. c-Met is amarker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 2011;141:2218-27 e5.
20. Kim MP, Fleming JB, Wang H, Abbruzzese JL, Choi W, Kopetz S, et al.ALDH activity selectively defines an enhanced tumor-initiating cell population relative to CD133 expression in human pancreatic adenocarcinoma. PLoS One 2011;6:e20636.
21. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, et al.EMT and dissemination precede pancreatic tumor formation. Cell 2012; 148:349-61.
22. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005;7:469-83.
23. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003;4:437-50.
24. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001;15:3243-8.
25. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, et al.Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004;119:847-60.
26. Safran M, Kim WY, Kung AL, Horner JW, DePinho RA, Kaelin WG Jr. Mouse reporter strain for noninvasive bioluminescent imaging of cells that have undergone Cre-mediated recombination. Mol Imaging 2003; 2:297-302.
27. Hu Y, Smyth GK. ELDA: Extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 2009;347:70-8.
28. Collins MA, Bednar F, Zhang Y, Brisset JC, Galban S, Galban CJ, et al. Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest 2012;122:639-53.
29. Ischenko I, Zhi J, Moll UM, Nemajerova A, Petrenko O. Direct reprogramming by oncogenic Ras and Myc. Proc Natl Acad Sci U S A 2013;110:3937-42.
30. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, Murter C, et al. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 2010;102:340-51.
31. Banerjee S, Nomura A, Sangwan V, Chugh R, Dudeja V, Vickers S, et al. CD133 tumor initiating cells (TIC) in a syngenic murine model of pancreatic cancer respond to Minnelide. Clin Cancer Res 2014;20:2388-99.
32. Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sanchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature 2014;514:628-32.
33. Ischenko I, Petrenko O, Hayman MJ. Analysis of the tumor-initiating and metastatic capacity of PDX1-positive cells from the adult pancreas. Proc Natl Acad Sci U S A 2014;111:3466-71.
34. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253-70.
35. 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.
36. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. JNatl Cancer Inst 2008;100:672-9.
37. 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.
38. Zhang GN, Liang Y, Zhou LJ, Chen SP, Chen G, Zhang TP, et al. Combination of salinomycin and gemcitabine eliminates pancreatic cancer cells. Cancer Lett 2011;313:137-44.
39. Frese KK, Neesse A, Cook N, Bapiro TE, Lolkema MP, Jodrell DI, et al. nab-Paclitaxel potentiates gemcitabine activity by reducing cytidine deaminase levels in a mouse model of pancreatic cancer. Cancer Discov 2012;2:260-9.
40. Sastra SA, Olive KP. Quantification of murine pancreatic tumors by highresolution ultrasound. Methods Mol Biol 2013;980:249-66.
41. Iacobuzio-Donahue CA. Genetic evolution of pancreatic cancer: lessons learnt from the pancreatic cancer genome sequencing project.Gut 2012;61: 1085-94.
42. Hruban RH, Goggins M, Parsons J, Kern SE. Progression model for pancreatic cancer. Clin Cancer Res 2000;6:2969-72.
43. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321:1801-6.
44. Kim MS, Zhong Y, Yachida S, Rajeshkumar NV, Abel ML, Marimuthu A, et al. Heterogeneity of pancreatic cancer metastases in a single patient revealed by quantitative proteomics. Mol Cell Proteomics 2014;13: 2803-11.
45. Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: A critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 2011; 8:486-98.
46. Olive KP, Tuveson DA. The use of targeted mouse models for preclinical testing of novel cancer therapeutics. Clin Cancer Res 2006;12: 5277-87.