Cancer stem cells, cancer cell plasticity and radiation therapy

Seminars in Cancer Biology

Volumn 31, Issue , 2015, Pages 28-35

  Vlashi, Erina ^a,b   Pajonk, Frank ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer stem cells; Radiation therapy; Reprogramming

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD133 ANTIGEN; CD24 ANTIGEN; CELL MARKER; HERMES ANTIGEN; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2; TUMOR MARKER;

CANCER CELL PLASTICITY; CANCER MODEL; CANCER RADIOTHERAPY; CANCER STEM CELL; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CLONAL EVOLUTION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; IONIZING RADIATION; NONHUMAN; NUCLEAR REPROGRAMMING; ONCOLOGICAL PARAMETERS; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SOLID TUMOR; TUMOR MICROENVIRONMENT; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASMS; PATHOLOGY; PROCEDURES; RADIATION RESPONSE; TUMOR VOLUME;

BIOMARKERS, TUMOR; CELL DIFFERENTIATION; CELL SURVIVAL; CLONAL EVOLUTION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; RADIOTHERAPY; TUMOR BURDEN;

EID: 84923218677     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.07.001     Document Type: Review

References (115)

1. Marjanovic N.D., Weinberg R.A., Chaffer C.L. Cell plasticity and heterogeneity in cancer. Clin Chem 2013, 59(1):168-179.
2. Greaves M., Maley C.C. Clonal evolution in cancer. Nature 2012, 481(7381):306-313.
3. Virchow R. Cellular-pathologie. Arch Pathol Anat Physiol Klin Med 1855, 8(1):3-39.
4. Cohneim J. Congenitales, quergestreiftes Muskelsarkom der Nieren. Virch Arch Pathol Anat Physiol Klin Med 1875, 65(1):64-69.
5. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889, 1:571-573.
6. Pierce G.B., Speers W.C. Tumors as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res 1988, 48(8):1996-2004.
7. 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(6464):645-648.
8. Hemmati H.D., Nakano I., Lazareff J.A., Masterman-Smith M., Geschwind D.H., Bronner-Fraser M., et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 2003, 100(25):15178-15183.
9. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., et al. Identification of human brain tumour initiating cells. Nature 2004, 432(7015):396-401.
10. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414(6859):105-111.
11. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003, 63(18):5821-5828.
12. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988.
13. Schatton T., Murphy G.F., Frank N.Y., Yamaura K., Waaga-Gasser A.M., Gasser M., et al. Identification of cells initiating human melanomas. Nature 2008, 451(7176):345-349.
14. 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(7222):593-598.
15. Boiko A.D., Razorenova O.V., van de Rijn M., Swetter S.M., Johnson D.L., Ly D.P., et al. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 2010, 466(7302):133-137.
16. Ishizawa K., Rasheed Z.A., Karisch R., Wang Q., Kowalski J., Susky E., et al. Tumor-initiating cells are rare in many human tumors. Cell Stem Cell 2010, 7(3):279-282.
17. Nowell P.C. The clonal evolution of tumor cell populations. Science 1976, 194(4260):23-28.
18. Burrell R.A., McGranahan N., Bartek J., Swanton C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 2013, 501(7467):338-345.
19. Cahill D.P., Kinzler K.W., Vogelstein B., Lengauer C. Genetic instability and Darwinian selection in tumours. Trends Cell Biol 1999, 9(12):M57-M60.
20. Cairns J. Mutation selection and the natural history of cancer. Nature 1975, 255(5505):197-200.
21. Shackleton M., Quintana E., Fearon E.R., Morrison S.J. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009, 138(5):822-829.
22. Penney K.L., Stampfer M.J., Jahn J.L., Sinnott J.A., Flavin R., Rider J.R., et al. Gleason grade progression is uncommon. Cancer Res 2013, 73(16):5163-5168.
23. Bidlingmaier S., Zhu X., Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med 2008, 86(9):1025-1032.
24. Clement V., Dutoit V., Marino D., Dietrich P.Y., Radovanovic I. Limits of CD133 as a marker of glioma self-renewing cells. Int J Cancer 2009, 125(1):244-248.
25. Griguer C.E., Oliva C.R., Gobin E., Marcorelles P., Benos D.J., Lancaster J.R., et al. CD133 is a marker of bioenergetic stress in human glioma. PLoS ONE 2008, 3(11):e3655.
26. Wang J., Sakariassen P.O., Tsinkalovsky O., Immervoll H., Boe S.O., Svendsen A., et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer 2007, 122(4):761-768.
27. Jaksch M., Munera J., Bajpai R., Terskikh A., Oshima R.G. Cell cycle-dependent variation of a CD133 epitope in human embryonic stem cell, colon cancer, and melanoma cell lines. Cancer Res 2008, 68(19):7882-7886.
28. Bao S. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
29. Pallini R., Ricci-Vitiani L., Banna G.L., Signore M., Lombardi D., Todaro M., et al. Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin Cancer Res 2008, 14(24):8205-8212.
30. Zeppernick F., Ahmadi R., Campos B., Dictus C., Helmke B.M., Becker N., et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 2008, 14(1):123-129.
31. Suetsugu A., Nagaki M., Aoki H., Motohashi T., Kunisada T., Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 2006, 351(4):820-824.
32. Miki J., Furusato B., Li H., Gu Y., Takahashi H., Egawa S., et al. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res 2007, 67(7):3153-3161.
33. Phillips T.M., McBride W.H., Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 98(24):1777-1785.
34. Fillmore C.M., Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008, 10(2):R25.
35. Prince M.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007, 104:973-978.
36. Jaggupilli A., Elkord E. Significance of CD44 and CD24 as cancer stem cell markers: an enduring ambiguity. Clin Develop Immunol 2012, 2012:708036.
37. Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nat Rev Cancer 2011, 11(4):254-267.
38. Kastan M.B., Schlaffer E., Russo J.E., Colvin O.M., Civin C.I., Hilton J. Direct demonstration of elevated aldehyde dehydrogenase in human hematopoietic progenitor cells. Blood 1990, 75(10):1947-1950.
39. Ginestier C., Hur M.H., 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(5):555-567.
40. Resetkova E., Reis-Filho J.S., Jain R.K., Mehta R., Thorat M.A., Nakshatri H., et al. Prognostic impact of ALDH1 in breast cancer: a story of stem cells and tumor microenvironment. Breast Cancer Res Treat 2010, 123(1):97-108.
41. Marcato P., Dean C.A., Pan D., Araslanova R., Gillis M., Joshi M., et al. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cells 2011, 29(1):32-45.
42. Bhaijee F., Pepper D.J., Pitman K.T., Bell D. Cancer stem cells in head and neck squamous cell carcinoma: a review of current knowledge and future applications. Head Neck 2012, 34(6):894-899.
43. Huang E.H., Hynes M.J., Zhang T., Ginestier C., Dontu G., Appelman H., et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009, 69(8):3382-3389.
44. Okudela K., Woo T., Mitsui H., Tajiri M., Masuda M., Ohashi K. Expression of the potential cancer stem cell markers, CD133, CD44, ALDH1, and beta-catenin, in primary lung adenocarcinoma-their prognostic significance. Pathol Int 2012, 62(12):792-801.
45. Goldstein A.S., Huang J., Guo C., Garraway I.P., Witte O.N. Identification of a cell of origin for human prostate cancer. Science 2010, 329(5991):568-571.
46. Vlashi E., Kim K., Lagadec C., Donna L.D., McDonald J.T., Eghbali M., et al. In vivo imaging, tracking, and targeting of cancer stem cells. J Natl Cancer Inst 2009, 101(5):350-359.
47. Lagadec C., Vlashi E., Bhuta S., Lai C., Mischel P., Werner M., et al. Tumor cells with low proteasome subunit expression predict overall survival in head and neck cancer patients. BMC Cancer 2014, 14(1):152.
48. Lagadec C., Vlashi E., Frohnen P., Alhiyari Y., Chan M., Pajonk F. The RNA-binding protein Musashi-1 regulates proteasome subunit expression in breast cancer- and glioma-initiating cells. Stem Cells 2014, 32(1):135-144.
49. Xu H., Fu J., Ha S.W., Ju D., Zheng J., Li L., et al. The CCAAT box-binding transcription factor NF-Y regulates basal expression of human proteasome genes. Biochim Biophys Acta 2012, 1823(4):818-825.
50. Pan J., Zhang Q., Wang Y., You M. 26S proteasome activity is down-regulated in lung cancer stem-like cells propagated in vitro. PLoS ONE 2010, 5(10):e13298.
51. Adikrisna R., Tanaka S., Muramatsu S., Aihara A., Ban D., Ochiai T., et al. Identification of pancreatic cancer stem cells and selective toxicity of chemotherapeutic agents. Gastroenterology 2012, 143(1):234-245. e237.
52. Muramatsu S., Tanaka S., Mogushi K., Adikrisna R., Aihara A., Ban D., et al. Visualization of stem cell features in human hepatocellular carcinoma reveals in vivo significance of tumor-host interaction and clinical course. Hepatology 2013, 58(1):218-228.
53. Lagadec C., Vlashi E., Della Donna L., Dekmezian C., Pajonk F. Radiation-induced reprogramming of breast cancer cells. Stem Cells 2012, 30(5):833-844.
54. Vlashi E., Lagadec C., Vergnes L., Matsutani T., Masui K., Poulou M., et al. Metabolic state of glioma stem cells and nontumorigenic cells. Proc Natl Acad Sci U S A 2011, 108(38):16062-16067.
55. Elfadl D., Hodgkinson V.C., Long E.D., Scaife L., Drew P.J., Lind M.J., et al. A pilot study to investigate the role of the 26S proteasome in radiotherapy resistance and loco-regional recurrence following breast conserving therapy for early breast cancer. Breast 2011, 20(4):334-337.
56. Yamanaka S., Blau H.M. Nuclear reprogramming to a pluripotent state by three approaches. Nature 2010, 465(7299):704-712.
57. Greenow K., Clarke A.R. Controlling the stem cell compartment and regeneration in vivo: the role of pluripotency pathways. Physiol Rev 2012, 92(1):75-99.
58. Xu H., Wang W., Li C., Yu H., Yang A., Wang B., et al. WWP2 promotes degradation of transcription factor OCT4 in human embryonic stem cells. Cell Res 2009, 19(5):561-573.
59. Baltus G.A., Kowalski M.P., Zhai H., Tutter A.V., Quinn D., Wall D., et al. Acetylation of sox2 induces its nuclear export in embryonic stem cells. Stem Cells 2009, 27(9):2175-2184.
60. Chen Z.Y., Wang X., Zhou Y., Offner G., Tseng C.C. Destabilization of Kruppel-like factor 4 protein in response to serum stimulation involves the ubiquitin-proteasome pathway. Cancer Res 2005, 65(22):10394-10400.
61. Farrell A.S., Sears R.C. MYC degradation. Cold Spring Harbor Perspect Med 2014, 4(3).
62. Moretto-Zita M., Jin H., Shen Z., Zhao T., Briggs S.P., Xu Y. Phosphorylation stabilizes Nanog by promoting its interaction with Pin1. Proc Natl Acad Sci U S A 2010, 107(30):13312-13317.
63. Nichols J., Zevnik B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95(3):379-391.
64. Levasseur D.N., Wang J., Dorschner M.O., Stamatoyannopoulos J.A., Orkin S.H. Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. Genes Dev 2008, 22(5):575-580.
65. Liedtke S., Enczmann J., Waclawczyk S., Wernet P., Kogler G. Oct4 and its pseudogenes confuse stem cell research. Cell Stem Cell 2007, 1(4):364-366.
66. Liedtke S., Stephan M., Kogler G. Oct4 expression revisited: potential pitfalls for data misinterpretation in stem cell research. Biol. Chem. 2008, 389(7):845-850.
67. de Resende M.F., Chinen L.T., Vieira S., Jampietro J., da Fonseca F.P., Vassallo J., et al. Prognostication of OCT4 isoform expression in prostate cancer. Tumour Biol 2013, 34(5):2665-2673.
68. Koukourakis M.I., Giatromanolaki A., Tsakmaki V., Danielidis V., Sivridis E. Cancer stem cell phenotype relates to radio-chemotherapy outcome in locally advanced squamous cell head-neck cancer. Br J Cancer 2012, 106(5):846-853.
69. Zhang X., Han B., Huang J., Zheng B., Geng Q., Aziz F., et al. Prognostic significance of OCT4 expression in adenocarcinoma of the lung. Jpn J Clin Oncol 2010, 40(10):961-966.
70. Saigusa S., Tanaka K., Toiyama Y., Yokoe T., Okugawa Y., Ioue Y., et al. Correlation of CD133, OCT4, and SOX2 in rectal cancer and their association with distant recurrence after chemoradiotherapy. Ann Surg Oncol 2009, 16(12):3488-3498.
71. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122(6):947-956.
72. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126(4):663-676.
73. Arnold K., Sarkar A., Yram M.A., Polo J.M., Bronson R., Sengupta S., et al. Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 2011, 9(4):317-329.
74. Park D., Xiang A.P., Mao F.F., Zhang L., Di C.G., Liu X.M., et al. Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 2010, 28(12):2162-2171.
75. Tsukamoto T., Mizoshita T., Mihara M., Tanaka H., Takenaka Y., Yamamura Y., et al. Sox2 expression in human stomach adenocarcinomas with gastric and gastric-and-intestinal-mixed phenotypes. Histopathology 2005, 46(6):649-658.
76. Li X.L., Eishi Y., Bai Y.Q., Sakai H., Akiyama Y., Tani M., et al. Expression of the SRY-related HMG box protein SOX2 in human gastric carcinoma. Int J Oncol 2004, 24(2):257-263.
77. Rodriguez-Pinilla S.M., Sarrio D., Moreno-Bueno G., Rodriguez-Gil Y., Martinez M.A., Hernandez L., et al. Sox2: a possible driver of the basal-like phenotype in sporadic breast cancer. Modern Pathol 2007, 20(4):474-481.
78. Sanada Y., Yoshida K., Ohara M., Oeda M., Konishi K., Tsutani Y. Histopathologic evaluation of stepwise progression of pancreatic carcinoma with immunohistochemical analysis of gastric epithelial transcription factor SOX2: comparison of expression patterns between invasive components and cancerous or nonneoplastic intraductal components. Pancreas 2006, 32(2):164-170.
79. Alonso M.M., Diez-Valle R., Manterola L., Rubio A., Liu D., Cortes-Santiago N., et al. Genetic and epigenetic modifications of Sox2 contribute to the invasive phenotype of malignant gliomas. PLoS ONE 2011, 6(11):e26740.
80. Chou Y.T., Lee C.C., Hsiao S.H., Lin S.E., Lin S.C., Chung C.H., et al. The emerging role of SOX2 in cell proliferation and survival and its crosstalk with oncogenic signaling in lung cancer. Stem Cells 2013, 31(12):2607-2619.
81. Zhao W., Hisamuddin I.M., Nandan M.O., Babbin B.A., Lamb N.E., Yang V.W. Identification of Kruppel-like factor 4 as a potential tumor suppressor gene in colorectal cancer. Oncogene 2004, 23(2):395-402.
82. Lagadinou E.D., Sach A., Callahan K., Rossi R.M., Neering S.J., Minhajuddin M., et al. BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells. Cell Stem Cell 2013, 12(3):329-341.
83. Wei D., Gong W., Kanai M., Schlunk C., Wang L., Yao J.C., et al. Drastic down-regulation of Kruppel-like factor 4 expression is critical in human gastric cancer development and progression. Cancer Res 2005, 65(7):2746-2754.
84. Pandya A.Y., Talley L.I., Frost A.R., Fitzgerald T.J., Trivedi V., Chakravarthy M., et al. Nuclear localization of KLF4 is associated with an aggressive phenotype in early-stage breast cancer. Clin Cancer Res 2004, 10(8):2709-2719.
85. Hirsch H.A., Iliopoulos D., Tsichlis P.N., Struhl K. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Res 2009, 69(19):7507-7511.
86. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318(5858):1917-1920.
87. Chen X., Whitney E.M., Gao S.Y., Yang V.W. Transcriptional profiling of Kruppel-like factor 4 reveals a function in cell cycle regulation and epithelial differentiation. J Mol Biol 2003, 326(3):665-677.
88. Chen X., Johns D.C., Geiman D.E., Marban E., Dang D.T., Hamlin G., et al. Kruppel-like factor 4 (gut-enriched Kruppel-like factor) inhibits cell proliferation by blocking G1/S progression of the cell cycle. J Biol Chem 2001, 276(32):30423-30428.
89. Shields J.M., Christy R.J., Yang V.W. Identification and characterization of a gene encoding a gut-enriched Kruppel-like factor expressed during growth arrest. J Biol Chem 1996, 271(33):20009-20017.
90. Eramo A., Ricci-Vitiani L., Zeuner A., Pallini R., Lotti F., Sette G., et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 2006, 13(7):1238-1241.
91. Woodward W.A., Chen M.S., Behbod F., Alfaro M.P., Buchholz T.A., Rosen J.M. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci U S A 2007, 104(2):618-623.
92. Lagadec C., Vlashi E., Della Donna L., Meng Y., Dekmezian C., Kim K., et al. Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 2010, 12(1):R13.
93. Salmina K., Jankevics E., Huna A., Perminov D., Radovica I., Klymenko T., et al. Up-regulation of the embryonic self-renewal network through reversible polyploidy in irradiated p53-mutant tumour cells. Exp Cell Res 2010, 316(13):2099-2112.
94. Ghisolfi L., Keates A.C., Hu X., Lee D.K., Li C.J. Ionizing radiation induces stemness in cancer cells. PLoS ONE 2012, 7(8):e43628.
95. Jopling C., Boue S., Izpisua Belmonte J.C. Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat Rev Mol Cell Biol 2011, 12(2):79-89.
96. Chaffer C.L., Brueckmann I., Scheel C., Kaestli A.J., Wiggins P.A., Rodrigues L.O., et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci U S A 2011, 108(19):7950-7955.
97. Tata P.R., Mou H., Pardo-Saganta A., Zhao R., Prabhu M., Law B.M., et al. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 2013, 503(7475):218-223.
98. Shaykhiev R., Wang R., Zwick R.K., Hackett N.R., Leung R., Moore M.A., et al. Airway basal cells of healthy smokers express an embryonic stem cell signature relevant to lung cancer. Stem Cells 2013, 31(9):1992-2002.
99. Balkwill F.R., Capasso M., Hagemann T. The tumor microenvironment at a glance. J Cell Sci 2012, 125(Pt 23):5591-5596.
100. Gilbertson R.J., Rich J.N. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 2007, 7(10):733-736.
101. Salcedo R., Oppenheim J.J. Role of chemokines in angiogenesis: CXCL12/SDF-1 and CXCR4 interaction, a key regulator of endothelial cell responses. Microcirculation 2003, 10(3-4):359-370.
102. Shawber C.J., Das I., Francisco E., Kitajewski J. Notch signaling in primary endothelial cells. Ann N Y Acad Sci 2003, 995:162-170.
103. Fan X., Khaki L., Zhu T.S., Soules M.E., Talsma C.E., Gul N., et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010, 28(1):5-16.
104. Heddleston J.M., Li Z., McLendon R.E., Hjelmeland A.B., Rich J.N. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009, 8(20):3274-3284.
105. Hjelmeland A.B., Wu Q., Heddleston J.M., Choudhary G.S., MacSwords J., Lathia J.D., et al. Acidic stress promotes a glioma stem cell phenotype. Cell Death Differ 2011, 18(5):829-840.
106. Vermeulen L., De Sousa E.M.F., van der Heijden M., Cameron K., de Jong J.H., Borovski T., et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nature cell biology 2010, 12(5):468-476.
107. Giannoni E., Bianchini F., Masieri L., Serni S., Torre E., Calorini L., et al. Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness. Cancer Res 2010, 70(17):6945-6956.
108. Iliopoulos D., Hirsch H.A., Wang G., Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci U S A 2011, 108(4):1397-1402.
109. Ohanna M., Cheli Y., Bonet C., Bonazzi V.F., Allegra M., Giuliano S., et al. Secretome from senescent melanoma engages the STAT3 pathway to favor reprogramming of naive melanoma towards a tumor-initiating cell phenotype. Oncotarget 2013, 4(12):2212-2224.
110. Papadopoulou A., Kletsas D. Human lung fibroblasts prematurely senescent after exposure to ionizing radiation enhance the growth of malignant lung epithelial cells in vitro and in vivo. Int J Oncol 2011, 39(4):989-999.
111. Hawsawi N.M., Ghebeh H., Hendrayani S.F., Tulbah A., Al-Eid M., Al-Tweigeri T., et al. Breast carcinoma-associated fibroblasts and their counterparts display neoplastic-specific changes. Cancer Res 2008, 68(8):2717-2725.
112. Chiang C-S., Hong J.-H., Stalder A., Sun J.-R.H., Withers H.R., McBride.W.H. Late-delayed molecular responses to brain irradiation. Int J Rad Biol 1999.
113. Chiang C.S., Hong J.H., Stalder A., Sun J.R., Withers H.R., McBride W.H. Delayed molecular responses to brain irradiation. Int J Radiat Biol 1997, 72(1):45-53.
114. Cartwright P., McLean C., Sheppard A., Rivett D., Jones K., Dalton S. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 2005, 132(5):885-896.
115. Liu S., Cong Y., Wang D., Sun Y., Deng L., Liu Y., et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports 2014, 2(1):78-91.