Heterogeneity and targeting of pancreatic cancer stem cells

Clinical Cancer Research

Volumn 18, Issue 16, 2012, Pages 4277-4284

  Penchev, Vesselin R ^a   Rasheed, Zeshaan A ^a   Maitra, Anirban ^a   Matsui, William ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXY 1 METHYLTETRALIN; 4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ALDEHYDE DEHYDROGENASE; CABOZANTINIB; CD131 ANTIGEN; CD133 ANTIGEN; CD24 ANTIGEN; CD34 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CYCLOPHOSPHAMIDE; DEATH RECEPTOR 5; GEMCITABINE; GSI 18; HERMES ANTIGEN; HLA DR5 ANTIGEN; NOTCH RECEPTOR; PROTEIN NODAL; SALINOMYCIN; SARIDEGIB; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SONIC HEDGEHOG PROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER INVASION; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL ISOLATION; CELL MIGRATION; COLONY FORMATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE IDENTIFICATION; GENE MUTATION; HUMAN; METASTASIS POTENTIAL; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, PANCREATIC DUCTAL; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS;

EID: 84865087341     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-3112     Document Type: Review

References (58)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29.
2. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
3. 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.
4. 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.
5. 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.
6. 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.
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. Kern SE, Shibata D. The fuzzy math of solid tumor stem cells: a perspective. Cancer Res 2007;67:8985-8.
9. Adams JM, Strasser A. Is tumor growth sustained by rare cancer stem cells or dominant clones? Cancer Res 2008;68:4018-21.
10. Tomasson MH. Cancer stem cells: a guide for skeptics. J Cell Biochem 2009;106:745-9.
11. Jimeno A, Feldmann G, Suárez-Gauthier A, Rasheed Z, Solomon A, Zou G-M, et al. A direct pancreatic cancer xenograft model as a platform for cancer stem cell therapeutic development. Mol Cancer Ther 2009;8:310-4.
12. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CHM, 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.
13. Brennan S, Matsui W. Cancer stem cells: controversies in multiple myeloma. J Mol Med 2009;87:1079-85.
14. Lapidot T, Fajerman Y, Kollet O. Immune-deficient SCID and NOD/SCID mice models as functional assays for studying normal and malignant human hematopoiesis. J Mol Med 1997;75:664-73.
15. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401.
16. 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.
17. Matsui W, Wang Q, Barber JP, Brennan S, Smith BD, Borrello I, et al. Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res 2008;68:190-7.
18. 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.
19. Jones RJ, Gocke CD, Kasamon YL, Miller CB, Perkins B, Barber JP, et al. Circulating clonotypic B cells in classic Hodgkin lymphoma. Blood 2009;113:5920-6.
20. 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.
21. Dalerba P, Dylla SJ, Park I-K, 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.
22. Li C, Wu JÄ, Hynes M, Dosch J, Sarkar B, Welling TH, et al. c-Met Is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 2011;141:2218-27.e5.
23. Emadi A, Jones RJ, Brodsky RA. Cyclophosphamide and cancer: golden anniversary. Nat Rev Clin Oncol 2009;6:638-47.
24. Rovira M, Scott S-G, Liss AS, Jensen J, Thayer SP, Leach SD. Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas. Proc Natl Acad Sci U S A 2010;107:75-80.
25. 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.
26. Li Y, Li A, Glas M, Lal B, Ying M, Sang Y, et al. c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Natl Acad Sci U S A 2011;108:9951-6.
27. 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.
28. Rasheed ZA, Kowalski J, Smith BD, Matsui W. Concise review: emerging concepts in clinical targeting of cancer stem cells. Stem Cells 2011;29:883-7.
29. Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clin Cancer Res 2012;18:4266-76.
30. Bar EE, Lin A, Mahairaki V, Matsui W, Eberhart CG. Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 2010;177:1491-502.
31. Le A, Rajeshkumar NV, Maitra A, Dang CV. Conceptual framework for cutting the pancreatic cancer fuel supply. Clin Cancer Res 2012;18:4285-90.
32. 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.
33. Mani S, Evans K, Hollier B, Guo W, Weinberg R. Generation of stem-like cells via EMT: a new twist in cancer initiation and progression. AACR Education Book; 2009:173.
34. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009;11: 1487-95.
35. Maitra A, Adsay NV, Argani P, Iacobuzio-Donahue C, De MA, Cameron JL, et al. Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol 2003;16:902-12.
36. Hruban RH, van Mansfeld AD, Offerhaus GJ, van Weering DH, Allison DC, Goodman SN, et al. K-ras oncogene activation in adenocarcinoma of the human pancreas. A study of 82 carcinomas using a combination of mutant-enriched polymerase chain reaction analysis and allele-specific oligonucleotide hybridization. Am J Pathol 1993;143:545-54.
37. Redston MS, Caldas C, Seymour AB, Hruban RH, da Costa L, Yeo CJ, et al. p53 Mutations in pancreatic carcinoma and evidence of common involvement of homocopolymer tracts in DNA microdeletions. Cancer Res 1994;54:3025-33.
38. Hahn SA, Schutte M, Hoque ATMS, Moskaluk CA, da Costa LT, Rozenblum E, et al. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 1996;271:350-3.
39. Jones S, Zhang X, Parsons DW, Lin JC-H, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321:1801-6.
40. Tuveson DA, Hingorani SR. Ductal pancreatic cancer in humans and mice. Cold Spring Harbor Symp Quant Biol 2005;70:65-72.
41. Anderson K, Lutz C, van Delft FW, Bateman CM, Guo Y, Colman SM, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 2011;469:356-61.
42. Notta F, Mullighan CG, Wang JCY, Poeppl A, Doulatov S, Phillips LA, et al. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 2011;469:362-7.
43. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010;467:1114-7.
44. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. New Engl J Med 2012;366:883-92.
45. Maitra A, Kern SE, Hruban RH. Molecular pathogenesis of pancreatic cancer. Best Pract Res Clin Gastroenterol 2006;20:211-26.
46. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012;481:306-13.
47. Iacobuzio-Donahue CA, Velculescu VE, Wolfgang CL, Hruban RH. Genetic basis of pancreas cancer development and progression: insights from whole-exome and whole-genome sequencing. Clin Cancer Res 2012;18:4257-65.
48. Cioffi M, Dorado J, Baeuerle PA, Heeschen C. EpCAM/CD3-bispecific T-cell engaging antibody MT110 eliminates primary human pancreatic cancer stem cells. Clin Cancer Res 2012;18:465-74.
49. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med 2007;58:267-84.
50. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006;12:1167-74.
51. Rajeshkumar NV, Rasheed ZA, Garcia-Garcia E, Lopez-Rios F, Fujiwara K, Matsui WH, et al. A combination of DR5 agonistic monoclonal antibody with gemcitabine targets pancreatic cancer stem cells and results in long-term disease control in human pancreatic cancer model. Mol Cancer Ther 2010;9:2582-92.
52. Lonardo E, Hermann PC, Mueller M-T, Huber S, Balic A, Miranda-Lorenzo I, et al. Nodal/Activin signaling drives self-renewal and tumor-igenicity of pancreatic cancer stem cells and provides a target for combined drug therapy. Cell Stem Cell 2011;9:433-46.
53. Feldmann G, Fendrich V, McGovern K, Bedja D, Bisht S, Alvarez H, et al. An orally bioavailable small-molecule inhibitor of Hedgehog signaling inhibits tumor initiation and metastasis in pancreatic cancer. Mol Cancer Ther 2008;7:2725-35.
54. Feldmann G, Dhara S, Fendrich V, Bedja D, Beaty R, Mullendore M, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res 2007;67:2187-96.
55. 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.
56. Infinity stops phase 2 trials of saridegib in chondrosarcoma and myelofibrosis. [cited 2012 May 17]. Available from: http://www.reuters.com/ article/2012/06/18/idUS87102+18-Jun-2012+BW20120618.
57. Mullendore ME, Koorstra J-B, Li Y-M, Offerhaus GJ, Fan X, Henderson CM, et al. Ligand-dependent Notch signaling is involved in tumor initiation and tumor maintenance in pancreatic cancer. Clin Cancer Res 2009;15:2291-301.
58. Zhang G-N, Liang Y, Zhou L-J, Chen S-P, Chen G, Zhang T-P, et al. Combination of salinomycin and gemcitabine eliminates pancreatic cancer cells. Cancer Lett 2011;313:137-44.