The evolving cancer stem cell paradigm: Implications in veterinary oncology

Veterinary Journal

Volumn 205, Issue 2, 2015, Pages 154-160

  Pang, Lisa Y ^a   Argyle, David J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cancer cell plasticity; Cancer stem cells; Cellular reprogramming; Lineage tracing; Stemness; Tumour heterogeneity

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2;

ACUTE MYELOBLASTIC LEUKEMIA; ANGIOSARCOMA; APC GENE; APOPTOSIS; BRAIN CANCER; BREAST CANCER; BREAST CARCINOMA; CANCER CELL; CANCER GROWTH; CANCER PROGNOSIS; CANCER STEM CELL; CELL DIFFERENTIATION; CELL RENEWAL; CELL SUBPOPULATION; CELL SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; DNA REPAIR; GENE MUTATION; GENETIC HETEROGENEITY; GLIOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; IMMUNOPHENOTYPING; KIDNEY CARCINOMA; LIVER CANCER; LUNG CANCER; MELANOMA; NONHUMAN; NUCLEAR REPROGRAMMING; ONCOGENE; OSTEOSARCOMA; PANCREAS ADENOCARCINOMA; PROSTATE CANCER; PROSTATE CARCINOMA; RETINOBLASTOMA; REVIEW; TUMOR DIFFERENTIATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; CELL PLASTICITY; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; NEOPLASM; PHYSIOLOGY; VETERINARY;

ANIMALS; CELL PLASTICITY; CELL TRANSFORMATION, NEOPLASTIC; CELLULAR REPROGRAMMING; GENE EXPRESSION REGULATION, NEOPLASTIC; NEOPLASMS; NEOPLASTIC STEM CELLS;

EID: 84937523179     PISSN: 10900233     EISSN: 15322971     Source Type: Journal    
DOI: 10.1016/j.tvjl.2014.12.029     Document Type: Review

References (94)

1. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:3983-3988.
2. Anderson K., Lutz C., van Delft F.W., Bateman C.M., Guo Y., Colman S.M., Kempski H., Moorman A.V., Titley I., Swansbury J., et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 2011, 469:356-361.
3. Atlasi Y., Mowla S.J., Ziaee S.A., Bahrami A.R. OCT-4, an embryonic stem cell marker, is highly expressed in bladder cancer. International Journal of Cancer 2007, 120:1598-1602.
4. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
5. Bass A.J., Watanabe H., Mermel C.H., Yu S., Perner S., Verhaak R.G., Kim S.Y., Wardwell L., Tamayo P., Gat-Viks I., et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nature Genetics 2009, 41:1238-1242.
6. Bergkvist G.T., Argyle D.J., Pang L.Y., Muirhead R., Yool D.A. Studies on the inhibition of feline EGFR in squamous cell carcinoma: Enhancement of radiosensitivity and rescue of resistance to small molecule inhibitors. Cancer Biology and Therapy 2011, 11:927-937.
7. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Medicine 1997, 3:730-737.
8. Bradshaw T.J., Bowen S.R., Jallow N., Forrest L.J., Jeraj R. Heterogeneity in intratumor correlations of 18F-FDG, 18F-FLT, and 61Cu-ATSM PET in canine sinonasal tumors. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 2013, 54:1931-1937.
9. Campbell P.J., Yachida S., Mudie L.J., Stephens P.J., Pleasance E.D., Stebbings L.A., Morsberger L.A., Latimer C., McLaren S., Lin M.L., et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010, 467:1109-1113.
10. Chappell J., Dalton S. Roles for MYC in the establishment and maintenance of pluripotency. Cold Spring Harbor Perspectives in Medicine 2013, 3:a014381.
11. Charles N., Ozawa T., Squatrito M., Bleau A.M., Brennan C.W., Hambardzumyan D., Holland E.C. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010, 6:141-152.
12. Chen J., Li Y., Yu T.S., McKay R.M., Burns D.K., Kernie S.G., Parada L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488:522-526.
13. Chiu P.P., Jiang H., Dick J.E. Leukemia-initiating cells in human T-lymphoblastic leukemia exhibit glucocorticoid resistance. Blood 2010, 116:5268-5279.
14. de The H., Chen Z. Acute promyelocytic leukaemia: Novel insights into the mechanisms of cure. Nature Reviews. Cancer 2010, 10:775-783.
15. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., Qian D., Lam J.S., Ailles L.E., Wong M., et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783.
16. Ding L., Ley T.J., Larson D.E., Miller C.A., Koboldt D.C., Welch J.S., Ritchey J.K., Young M.A., Lamprecht T., McLellan M.D., et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012, 481:506-510.
17. Driessens G., Beck B., Caauwe A., Simons B.D., Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature 2012, 488:527-530.
18. Dylla S.J., Beviglia L., Park I.K., Chartier C., Raval J., Ngan L., Pickell K., Aguilar J., Lazetic S., Smith-Berdan S., et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE 2008, 3:e2428.
19. 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. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Research 2005, 65:9328-9337.
20. Friedmann-Morvinski D., Verma I.M. Dedifferentiation and reprogramming: Origins of cancer stem cells. EMBO Reports 2014, 15:244-253.
21. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. The New England Journal of Medicine 2012, 366:883-892.
22. Gibbs C.P., Kukekov V.G., Reith J.D., Tchigrinova O., Suslov O.N., Scott E.W., Ghivizzani S.C., Ignatova T.N., Steindler D.A. Stem-like cells in bone sarcomas: Implications for tumorigenesis. Neoplasia (New York, N.Y.) 2005, 7:967-976.
23. Gidekel S., Pizov G., Bergman Y., Pikarsky E. Oct-3/4 is a dose-dependent oncogenic fate determinant. Cancer Cell 2003, 4:361-370.
24. Greaves M., Maley C.C. Clonal evolution in cancer. Nature 2012, 481:306-313.
25. Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., Lander E.S. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
26. Gutova M., Najbauer J., Gevorgyan A., Metz M.Z., Weng Y., Shih C.C., Aboody K.S. Identification of uPAR-positive chemoresistant cells in small cell lung cancer. PLoS ONE 2007, 2:e243.
27. Hamburger A., Salmon S.E. Primary bioassay of human myeloma stem cells. The Journal of Clinical Investigation 1977, 60:846-854.
28. Hamburger A.W., Salmon S.E. Primary bioassay of human tumor stem cells. Science 1977, 197:461-463.
29. Hanahan D., Weinberg R.A. Hallmarks of cancer: The next generation. Cell 2011, 144:646-674.
30. Hanna J.H., Saha K., Jaenisch R. Pluripotency and cellular reprogramming: Facts, hypotheses, unresolved issues. Cell 2010, 143:508-525.
31. Hedan B., Thomas R., Motsinger-Reif A., Abadie J., Andre C., Cullen J., Breen M. Molecular cytogenetic characterization of canine histiocytic sarcoma: A spontaneous model for human histiocytic cancer identifies deletion of tumor suppressor genes and highlights influence of genetic background on tumor behavior. BMC Cancer 2011, 11:201.
32. Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
33. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., Okita K., Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460:1132-1135.
34. Huangfu D., Maehr R., Guo W., Eijkelenboom A., Snitow M., Chen A.E., Melton D.A. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nature Biotechnology 2008, 26:795-797.
35. Huangfu D., Osafune K., Maehr R., Guo W., Eijkelenboom A., Chen S., Muhlestein W., Melton D.A. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nature Biotechnology 2008, 26:1269-1275.
36. Ishikawa K., Sasaki A., Haraguchi N., Yoshikawa Y., Mori M. A case of an alpha-fetoprotein-producing intrahepatic cholangiocarcinoma suggests probable cancer stem cell origin. The Oncologist 2007, 12:320-324.
37. Ishizawa K., Rasheed Z.A., Karisch R., Wang Q., Kowalski J., Susky E., Pereira K., Karamboulas C., Moghal N., Rajeshkumar N.V., et al. Tumor-initiating cells are rare in many human tumors. Cell Stem Cell 2010, 7:279-282.
38. Jones S., Zhang X., Parsons D.W., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Kamiyama H., Jimeno A., et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806.
39. Kreso A., O'Brien C.A., van Galen P., Gan O.I., Notta F., Brown A.M., Ng K., Ma J., Wienholds E., Dunant C., et al. Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 2013, 339:543-548.
40. Lamerato-Kozicki A.R., Helm K.M., Jubala C.M., Cutter G.C., Modiano J.F. Canine hemangiosarcoma originates from hematopoietic precursors with potential for endothelial differentiation. Experimental Hematology 2006, 34:870-878.
41. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M.A., Dick J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
42. Magalhaes G.M., Terra E.M., de Oliveira Vasconcelos R., de Barros Bandarra M., Moreira P.R., Rosolem M.C., Alessi A.C. Immunodetection of cells with a CD44+/CD24- phenotype in canine mammary neoplasms. BMC Veterinary Research 2013, 9:205.
43. 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., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
44. Marusyk A., Almendro V., Polyak K. Intra-tumour heterogeneity: A looking glass for cancer?. Nature Reviews. Cancer 2012, 12:323-334.
45. Mezencev R., Wang L., McDonald J.F. Identification of inhibitors of ovarian cancer stem-like cells by high-throughput screening. Journal of Ovarian Research 2012, 5:30.
46. Michishita M., Ezaki S., Ogihara K., Naya Y., Azakami D., Nakagawa T., Sasaki N., Arai T., Shida T., Takahashi K. Identification of tumor-initiating cells in a canine hepatocellular carcinoma cell line. Research in Veterinary Science 2014, 96:315-322.
47. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008, 3:e2888.
48. Moulay M., Liu W., Willenbrock S., Sterenczak K.A., Carlson R., Ngezahayo A., Murua Escobar H., Nolte I. Evaluation of stem cell marker gene expression in canine prostate carcinoma- and prostate cyst-derived cell lines. Anticancer Research 2013, 33:5421-5431.
49. Nakagawa M., Koyanagi M., Tanabe K., Takahashi K., Ichisaka T., Aoi T., Okita K., Mochiduki Y., Takizawa N., Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nature Biotechnology 2008, 26:101-106.
50. Nakanishi Y., Seno H., Fukuoka A., Ueo T., Yamaga Y., Maruno T., Nakanishi N., Kanda K., Komekado H., Kawada M., et al. Dclk1 distinguishes between tumor and normal stem cells in the intestine. Nature Genetics 2013, 45:98-103.
51. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., Cook K., Stepansky A., Levy D., Esposito D., et al. Identification of cancer stem cells derived from a canine lung adenocarcinoma cell line. Veterinary Pathology 2011, 48:1029-1034.
52. Nemoto Y., Maruo T., Sato T., Deguchi T., Ito T., Sugiyama H., Ishikawa T., Madarame H., Watanabe T., Shida Y., et al. Identification of cancer stem cells derived from a canine lung adenocarcinoma cell line. Veterinary Pathology 2011, 48:1029-1033.
53. Nik-Zainal S., Van Loo P., Wedge D.C., Alexandrov L.B., Greenman C.D., Lau K.W., Raine K., Jones D., Marshall J., Ramakrishna M., et al. The life history of 21 breast cancers. Cell 2012, 149:994-1007.
54. Notta F., Mullighan C.G., Wang J.C., Poeppl A., Doulatov S., Phillips L.A., Ma J., Minden M.D., Downing J.R., Dick J.E. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 2011, 469:362-367.
55. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
56. Orkin S.H., Hochedlinger K. Chromatin connections to pluripotency and cellular reprogramming. Cell 2011, 145:835-850.
57. Pang L.Y., Argyle D. Cancer stem cells and telomerase as potential biomarkers in veterinary oncology. The Veterinary Journal 2010, 185:15-22.
58. Pang L.Y., Cervantes-Arias A., Else R.W., Argyle D.J. Canine mammary cancer stem cells are radio- and chemo-resistant and exhibit an epithelial-mesenchymal transition phenotype. Cancers 2011, 3:1744-1762.
59. Pang L.Y., Bergkvist G.T., Cervantes-Arias A., Yool D.A., Muirhead R., Argyle D.J. Identification of tumour initiating cells in feline head and neck squamous cell carcinoma and evidence for gefitinib induced epithelial to mesenchymal transition. The Veterinary Journal 2012, 193:46-52.
60. Pang L.Y., Blacking T.M., Else R.W., Sherman A., Sang H.M., Whitelaw B.A., Hupp T.R., Argyle D.J. Feline mammary carcinoma stem cells are tumorigenic, radioresistant, chemoresistant and defective in activation of the ATM/p53 DNA damage pathway. The Veterinary Journal 2013, 196:414-423.
61. Pang L.Y., Gatenby E.L., Kamida A., Whitelaw B.A., Hupp T.R., Argyle D.J. Global gene expression analysis of canine osteosarcoma stem cells reveals a novel role for COX-2 in tumour initiation. PLoS ONE 2014, 9:e83144.
62. Piccirillo S.G., Reynolds B.A., Zanetti N., Lamorte G., Binda E., Broggi G., Brem H., Olivi A., Dimeco F., Vescovi A.L. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006, 444:761-765.
63. Prince M.E., Sivanandan R., Kaczorowski A., Wolf G.T., Kaplan M.J., Dalerba P., Weissman I.L., Clarke M.F., Ailles L.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:973-978.
64. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456:593-598.
65. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
66. Riggi N., Suva M.L., De Vito C., Provero P., Stehle J.C., Baumer K., Cironi L., Janiszewska M., Petricevic T., Suva D., et al. EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes and Development 2010, 24:916-932.
67. Rizzo S., Attard G., Hudson D.L. Prostate epithelial stem cells. Cell Proliferation 2005, 38:363-374.
68. Roesch A., Fukunaga-Kalabis M., Schmidt E.C., Zabierowski S.E., Brafford P.A., Vultur A., Basu D., Gimotty P., Vogt T., Herlyn M. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010, 141:583-594.
69. Rowland B.D., Peeper D.S. KLF4, p21 and context-dependent opposing forces in cancer. Nature Reviews. Cancer 2006, 6:11-23.
70. Rudin C.M., Durinck S., Stawiski E.W., Poirier J.T., Modrusan Z., Shames D.S., Bergbower E.A., Guan Y., Shin J., Guillory J., et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nature Genetics 2012, 44:1111-1116.
71. Sachlos E., Risueno R.M., Laronde S., Shapovalova Z., Lee J.H., Russell J., Malig M., McNicol J.D., Fiebig-Comyn A., Graham M., et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 2012, 149:1284-1297.
72. Sarkar A., Hochedlinger K. The sox family of transcription factors: Versatile regulators of stem and progenitor cell fate. Cell Stem Cell 2013, 12:15-30.
73. Schappa J.T., Frantz A.M., Gorden B.H., Dickerson E.B., Vallera D.A., Modiano J.F. Hemangiosarcoma and its cancer stem cell subpopulation are effectively killed by a toxin targeted through epidermal growth factor and urokinase receptors. International Journal of Cancer. Journal International du Cancer 2013, 133:1936-1944.
74. Schepers A.G., Snippert H.J., Stange D.E., van den Born M., van Es J.H., van de Wetering M., Clevers H. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012, 337:730-735.
75. Schuh A., Becq J., Humphray S., Alexa A., Burns A., Clifford R., Feller S.M., Grocock R., Henderson S., Khrebtukova I., et al. Monitoring chronic lymphocytic leukemia progression by whole genome sequencing reveals heterogeneous clonal evolution patterns. Blood 2012, 120:4191-4196.
76. Seigel G.M., Campbell L.M., Narayan M., Gonzalez-Fernandez F. Cancer stem cell characteristics in retinoblastoma. Molecular Vision 2005, 11:729-737.
77. Shah S.P., Roth A., Goya R., Oloumi A., Ha G., Zhao Y., Turashvili G., Ding J., Tse K., Haffari G., et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012, 486:395-399.
78. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
79. Stoica G., Lungu G., Martini-Stoica H., Waghela S., Levine J., Smith R. Identification of cancer stem cells in dog glioblastoma. Veterinary Pathology 2009, 46:391-406.
80. Suva M.L., Riggi N., Bernstein B.E. Epigenetic reprogramming in cancer. Science 2013, 339:1567-1570.
81. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
82. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
83. Taussig D.C., Miraki-Moud F., Anjos-Afonso F., Pearce D.J., Allen K., Ridler C., Lillington D., Oakervee H., Cavenagh J., Agrawal S.G., et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 2008, 112:568-575.
84. Thomas R., Borst L., Rotroff D., Motsinger-Reif A., Lindblad-Toh K., Modiano J.F., Breen M. Genomic profiling reveals extensive heterogeneity in somatic DNA copy number aberrations of canine hemangiosarcoma. Chromosome Research 2014, 22:305-319.
85. van Es J.H., Sato T., van de Wetering M., Lyubimova A., Nee A.N., Gregorieff A., Sasaki N., Zeinstra L., van den Born M., Korving J., et al. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nature Cell Biology 2012, 14:1099-1104.
86. Vicente-Duenas C., Romero-Camarero I., Cobaleda C., Sanchez-Garcia I. Function of oncogenes in cancer development: A changing paradigm. The EMBO Journal 2013, 32:1502-1513.
87. Visnyei K., Onodera H., Damoiseaux R., Saigusa K., Petrosyan S., De Vries D., Ferrari D., Saxe J., Panosyan E.H., Masterman-Smith M., et al. A molecular screening approach to identify and characterize inhibitors of glioblastoma stem cells. Molecular Cancer Therapeutics 2011, 10:1818-1828.
88. Visvader J.E. Cells of origin in cancer. Nature 2011, 469:314-322.
89. Visvader J.E., Lindeman G.J. Cancer stem cells: Current status and evolving complexities. Cell Stem Cell 2012, 10:717-728.
90. Walter M.J., Shen D., Ding L., Shao J., Koboldt D.C., Chen K., Larson D.E., McLellan M.D., Dooling D., Abbott R., et al. Clonal architecture of secondary acute myeloid leukemia. The New England Journal of Medicine 2012, 366:1090-1098.
91. Wilson H., Huelsmeyer M., Chun R., Young K.M., Friedrichs K., Argyle D.J. Isolation and characterisation of cancer stem cells from canine osteosarcoma. The Veterinary Journal 2008, 175:69-75.
92. Xu X., Hou Y., Yin X., Bao L., Tang A., Song L., Li F., Tsang S., Wu K., Wu H., et al. Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell 2012, 148:886-895.
93. Yachida S., Jones S., Bozic I., Antal T., Leary R., Fu B., Kamiyama M., Hruban R.H., Eshleman J.R., Nowak M.A., et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
94. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.