Differentiation pathways in carcinogenesis and in chemo- and radioresistance

Neoplasma

Volumn 59, Issue 1, 2012, Pages 6-17

  Janikova, M ^a   Skarda, J ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Chemoresistance; Hedgehog pathway; Notch pathway; Radioresistance; Stem cell; Wnt pathway

Indexed keywords

ACETYLSALICYLIC ACID; BETA CATENIN; BREAST CANCER RESISTANCE PROTEIN; CYCLIN D1; CYCLOOXYGENASE 2; FRIZZLED PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; IMATINIB; INDOMETACIN; INDUCIBLE NITRIC OXIDE SYNTHASE; JAGGED1; MATRIX METALLOPROTEINASE; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 4; NOTCH1 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; RETINOID; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR SOX2; VASCULOTROPIN; VITAMIN D; NOTCH RECEPTOR; TUMOR PROTEIN; WNT PROTEIN;

APOPTOSIS; BREAST CANCER; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CHEMORESISTANCE; EMBRYONIC STEM CELL; HUMAN; NONHUMAN; PHYSICAL SENSITIVITY; RADIOSENSITIVITY; REVIEW; WNT SIGNALING PATHWAY; ANIMAL; CELL TRANSFORMATION; CYTOLOGY; DRUG EFFECT; DRUG RESISTANCE; GENE EXPRESSION REGULATION; PHYSIOLOGY; PLURIPOTENT STEM CELL; RADIATION DOSE; RADIATION EXPOSURE;

ANIMALS; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; DRUG RESISTANCE, NEOPLASM; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HUMANS; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; PLURIPOTENT STEM CELLS; RADIATION TOLERANCE; RECEPTORS, NOTCH; WNT PROTEINS;

EID: 84863748077     PISSN: 00282685     EISSN: 13384317     Source Type: Journal    
DOI: 10.4149/neo_2012_002     Document Type: Review

References (130)

1. LEE CJ, DOSCH J, SIMEONE DM Pancreatic Cancer Stem Cells. J Clin Oncol 2008; 26: 2806-2812. http://dx.doi. org/10.1200/JCO.2008.16.6702
2. MASSARD C, DEUTSCH E, SORIA JC Tumour stem cell-targeted treatment: elimination or differentiation. Ann Oncol 2006; 17: 1620-1624. http://dx.doi.org/10.1093/annonc/mdl074
3. PAN G, LI J, ZHOU Y, ZHENG H, PEI D A negative feedback loop of transcription factors that controls stem cell pluripotency and self-renewal. FASEB J 2006; 20: 1730-1732. http://dx.doi.org/10.1096/fj.05-5543fje
4. VIEYRA D, ROSEN A, GOODELL M Identification and Characterization of SP Cells in ESC Cultures. Stem Cells Dev 2009; 18: 1155-1166. http://dx.doi.org/10.1089/scd.2008.0391
5. AL-HAJJ M, WICHA MS, BENITO-HERNANDEZ A, MORRISON SJ, CLARKE MF Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988. http://dx.doi.org/10.1073/pnas.0530291100
6. MARTIN GR Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by tera tocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78: 7634-7638. http://dx.doi.org/10.1073/pnas.78.12.7634
7. THOMSON JA, ITSKOVITZ-ELDOR J, SHAPIRO SS, WAKNITZ MA, SWIERGIEL JJ et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282: 1145-1147. http://dx.doi.org/10.1126/science.282.5391.1145
8. WU XZ Origin of cancer stem cells: the role of self-renewal and differentiation. Ann Surg Oncol 2008; 15: 407-414. http://dx.doi.org/10.1245/s10434-007-9695-y
9. DELLATORE SM, GARCIA AS, MILLER WM Mimicking stem cell niches to increase stem cell expansion. Curr Opin Biotechnol 2008; 19: 534-540. http://dx.doi.org/10.1016/j.copbio.2008.07.010
10. MALANCHI I, HUELSKEN J Cancer stem cells: never Wnt away from the niche. Curr Opin Oncol 2009; 21: 41-46. http://dx.doi.org/10.1097/CCO.0b013e32831d1faf
11. GOODELL MA, BROSE K, PARADIS G, CONNER AS, MULLIGAN RC Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183: 1797-1806. http://dx.doi.org/10.1084/jem.183.4.1797
12. PATRAWALA L, CALHOUN T, SCHNEIDER-BROUSSARD R, ZHOU J, CLAYPOOL K et al. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2-cancer cells are similarly tumorigenic. Cancer Res 2005; 65: 6207-6219. http://dx.doi.org/10.1158/0008-5472. CAN-05-0592
13. LEVINA V, MARRANGONI AM, DEMARCO R, GORELIK E, LOKHSIN AE Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS ONE 2008; 3: e3077. http://dx.doi.org/10.1371/journal. pone.0003077
14. RAMALHO-SANTOS M, YOON S, MATSUZAKI Y, MULLIGAN RC, MELTON DA "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002; 298: 597-600. http://dx.doi.org/10.1126/science.1072530
15. CROKER AK, ALLAN AL Cancer stem cells: implications for the progression and treatment of metastatic disease. J Cell Mol Med 2008; 12: 374-390. http://dx.doi.org/10.1111/j.1582-4934.2007.00211.x
16. PARK CY, TSENG D, WEISSMAN IL Cancer stem cell-directed therapies: recent data from the laboratory and clinic. Mol Ther 2009; 17: 219-230. http://dx.doi.org/10.1038/mt.2008.254
17. GARCIA-BARROS M, PARIS F, CORDON-CARDO C, LYDEN D, RAFII S et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003; 300: 1155-1159. http://dx.doi.org/10.1126/science.1082504
18. PARIS F, FUKS Z, KANG A, CAPODIECI P, JUAN G et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 2001; 293: 293-297. http://dx.doi.org/10.1126/science.1060191
19. LORUSSO G, RUEGG C The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochem Cell Biol 2008; 130: 1091-1103. http://dx.doi. org/10.1007/s00418-008-0530-8
20. MOELLER BJ, DREHER MR, RABBANI ZN, SCHROEDER T, CAO Y et al. Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell 2005; 8: 99-110. http://dx.doi. org/10.1016/j.ccr.2005.06.016
21. CALABRESE C, POPPLETON H, KOCAK M, HOGG TL, FULLER C et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11: 69-82. http://dx.doi.org/10.1016/j.ccr.2006.11.020
22. CHEN YC, HSU HS, CHEN YW, TSAI TH, HOW CK et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS ONE 2008; 3: e2637. http://dx.doi.org/10.1371/journal.pone.0002637
23. WANG ZX, TEH CH, KUEH JL, LUFKIN T, ROBSON P et al. Oct4 and Sox2 directly regulate expression of another pluripotency transcription factor, Zfp206, in embryonic stem cells. J Biol Chem 2007; 282: 12822-12830. http://dx.doi. org/10.1074/jbc.M611814200
24. LIM LS, LOH YH, ZHANG W, LI Y, CHEN X et al. Zic3 is required for maintenance of pluripotency in embryonic stem cells. Mol Biol Cell 2007; 18: 1348-1358. http://dx.doi. org/10.1091/mbc.E06-07-0624
25. WESTERN P, MALDONADO-SALDIVIA J, VAN DEN BERGEN, HAJKOVA P, SAITOU M et al. Analysis of Esg1 expression in pluripotent cells and the germline reveals similarities with Oct4 and Sox2 and differences between human pluripotent cell lines. Stem Cells 2005; 23: 1436-1442. http://dx.doi.org/10.1634/stemcells.2005-0146
26. WOODWARD WA, CHEN MS, BEHBOD F, ROSEN JM On mammary stem cells. J Cell Sci 2005; 118: 3585-3594. http://dx.doi.org/10.1242/jcs.02532
27. XIAO L, YUAN X, SHARKIS SJ Activin A maintains selfrenewal and regulates fibroblast growth factor, Wnt, and bone morphogenic protein pathways in human embryonic stem cells. Stem Cells 2006; 24: 1476-1486. http://dx.doi. org/10.1634/stemcells.2005-0299
28. OKOYE UC, MALBON CC, WANG HY Wnt and Frizzled RNA expression in human mesenchymal and embryonic (H7) stem cells. J Mol Signal 2008; 3: 16. http://dx.doi. org/10.1186/1750-2187-3-16
29. WALSH J, ANDREWS PW Expression of Wnt and Notch pathway genes in a pluripotent human embryonal carcinoma cell line and embryonic stem cell. APMIS 2003; 111: 197-210. http://dx.doi.org/10.1034/j.1600-0463.2003.1110124.x
30. PINSON KI, BRENNAN J, MONKLEY S, AVERY BJ, SKARNES WC An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 2000; 407: 535-538. http://dx.doi.org/10.1038/35035124
31. LIU S, DONTU G, WICHA MS Mammary stem cells, selfrenewal pathways, and carcinogenesis. Breast Cancer Res 2005; 7: 86-95. http://dx.doi.org/10.1186/bcr1021
32. BARKER N: The canonical Wnt/beta-catenin signalling pathway. Methods Mol Biol 2008; 468: 5-15. http://dx.doi. org/10.1007/978-1-59745-249-6_1
33. DIHLMANN S, VON KNEBEL DOEBERITZ M Wnt/betacatenin-pathway as a molecular target for future anti-cancer therapeutics. Int J Cancer 2005; 113: 515-524. http://dx.doi. org/10.1002/ijc.20609
34. DU Q, PARK KS, GUO Z, HE P, NAGASHIMA M et al. Regulation of human nitric oxide synthase 2 expression by Wnt beta-catenin signaling. Cancer Res 2006; 66: 7024-7031. http://dx.doi.org/10.1158/0008-5472.CAN-05-4110
35. Katoh M, KATOH M Notch ligand, JAG1, is evolutionarily conserved target of canonical WNT signaling pathway in progenitor cells. Int J Mol Med 2006; 17: 681-685.
36. KATOH M, KATOH M CER1 is a common target of WNT and NODAL signaling pathways in human embryonic stem cells. Int J Mol Med 2006; 17: 795-799.
37. KATOH M, KATOH M WNT signaling pathway and stem cell signaling network. Clin Cancer Res 2007; 13: 4042-4045. http://dx.doi.org/10.1158/1078-0432.CCR-06-2316
38. THOMPSON MC, FULLER C, HOGG TL, DALTON J, FINKELSTEIN D et al. Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J Clin Oncol 2006; 24: 1924-1931. http://dx.doi.org/10.1200/JCO.2005.04.4974
39. Chiba T, ZHENG YW, KITA K, YOKOSUKA O, SAISHO H et al. Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology 2007; 133: 937-950. http://dx.doi.org/10.1053/j.gastro.2007.06.016
40. YOOK JI, LI XY, OTA I, FEARON ER, WEISS SJ Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 2005; 280: 11740-11748. http://dx.doi.org/10.1074/jbc. M413878200
41. SCHLANGE T, MATSUDA Y, LIEMHARD S, HUBER A, HYNES NE Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonical WNT pathway and EGFR transactivation. Breast Cancer Res 2007; 9: R63. http://dx.doi.org/10.1186/bcr1769
42. KAWANO Y, KYPTA R Secreted antagonists of the Wnt signalling pathway. J Cell Sci 2003; 116: 2627-2634. http://dx.doi. org/10.1242/jcs.00623
43. SELL S Stem cell origin of cancer and differentiation therapy. Crit Rev Oncol Hematol 2004; 51: 1-28. http://dx.doi.org/10.1016/j.critrevonc.2004.04.007
44. WANG S, SHEN Y, YUAN X, CHEN K, GUO X et al. Dissecting signaling pathways that govern self-renewal of rabbit embryonic stem cells. J Biol Chem 2008; 283: 35929-35940. http://dx.doi.org/10.1074/jbc.M804091200
45. DRAVID G, YE Z, HAMMOND H, CHEN G, PYLE A et al. Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 2005; 23: 1489-1501. http://dx.doi.org/10.1634/stemcells.2005-0034
46. NAITO AT, SHIOJIMA I, AKAZAWA H, HIDAKA K, MORISAKI T et al. Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci U S A 2006; 103: 19812-19817. http://dx.doi.org/10.1073/pnas.0605768103
47. SUMI T, TSUNEYOSHI N, NAKATSUJI N, SUEMORI H Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 2008; 135: 2969-2979. http://dx.doi.org/10.1242/dev.021121
48. JAMES D, LEVINE AJ, BESSER D, HEMMATI-BRIVANLOU A TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 2005; 132: 1273-1282. http://dx.doi.org/10.1242/dev.01706
49. ALMEIDA M, HAN L, BELLIDO T, MANOLAGAS SC, KOUSTENI S Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and-independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem 2005; 280: 41342-41351. http://dx.doi.org/10.1074/jbc.M502168200
50. VALLIER L, ALEXANDER M, PEDERSEN RA Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 2005; 118: 4495-4509. http://dx.doi.org/10.1242/jcs.02553
51. MULHOLLAND DJ, DEDHAR S, COETZEE GA, NELSON CC Interaction of nuclear receptors with the Wnt/beta-catenin/Tcf signaling axis: Wnt you like to know? Endocr Rev 2005; 26: 898-915. http://dx.doi.org/10.1210/er.2003-0034
52. SHAH S, HECHT A, PESTELL R, BYERS SW Trans-repression of beta-catenin activity by nuclear receptors. J Biol Chem 2003; 278: 48137-48145. http://dx.doi.org/10.1074/jbc.M307154200
53. IDOGAWA M, MASUTANI M, SHITASHIGE M, HONDA K, TOKINO T et al. Ku70 and poly(ADP-ribose) polymerase-1 competitively regulate beta-catenin and T-cell factor-4-mediated gene transactivation: possible linkage of DNA damage recognition and Wnt signaling. Cancer Res 2007; 67: 911-918. http://dx.doi.org/10.1158/0008-5472.CAN-06-2360
54. YUAN D, LIU L, GU D Transcriptional regulation of livin by beta-catenin/TCF signaling in human lung cancer cell lines. Mol Cell Biochem 2007; 306: 171-178. http://dx.doi. org/10.1007/s11010-007-9567-6
55. HADJIHANNAS MV, BRUCKNER M, JERCHOW B, BIRCHMEIER W, DIETMAIER W et al. Aberrant Wnt/beta-catenin signaling can induce chromosomal instability in colon cancer. Proc Natl Acad Sci U S A 2006; 103: 10747-10752. http://dx.doi.org/10.1073/pnas.0604206103
56. CHEN MS, WOODWARD WA, BEHBOD F, PEDDIBHOTLA S, ALFARO MP et al. Wnt/beta-catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line. J Cell Sci 2007; 120: 468-477. http://dx.doi. org/10.1242/jcs.03348
57. REID G, WIELINGA P, ZELCER N, DE HAAS M, VAN DEEMTER L et al. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 2003; 63: 1094-1103. http://dx.doi.org/10.1124/mol.63.5.1094
58. TENG Y, WANG X, WANG Y, MA D Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Commun 2010; 392: 373-379. http://dx.doi.org/10.1016/j.bbrc.2010.01.028
59. VERMEULEN L, DE SOUSA E, MELO F, VAN DER HEIJDEN M, CAMERON K et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010; 12: 468-476. http://dx.doi.org/10.1038/ncb2048
60. KATOH M, KATOH M STAT3-induced WNT5A signaling loop in embryonic stem cells, adult normal tissues, chronic persistent inflammation, rheumatoid arthritis and cancer (Review). Int J Mol Med 2007; 19: 273-278.
61. DIHLMANN S, SIERMANN A, VON KNEBEL DOEBERITZ M The nonsteroidal anti-inflammatory drugs aspirin and indomethacin attenuate beta-catenin/TCF-4 signaling. Oncogene 2001; 20: 645-653. http://dx.doi.org/10.1038/sj.onc.1204123
62. SHAH S, PISHVAIAN MJ, EASWARAN V, BROWN PH, BYERS SW The role of cadherin, beta-catenin, and AP-1 in retinoid-regulated carcinoma cell differentiation and proliferation. J Biol Chem 2002; 277: 25313-25322. http://dx.doi. org/10.1074/jbc.M203158200
63. PALMER HG, GONZALEZ-SANCHO JM, ESPADA J, BERCIANO MT, PUIG I et al. Vitamin D(3) promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition signaling. J Cell Biol 2001; 154: 369-387. http://dx.doi.org/10.1083/jcb.200102028
64. RAO AS, KREMENEVSKAJA N, VON WASIELEWSKI R, JAKUBCAKOVA V, KANT S et al. Wnt/beta-catenin signaling mediates antineoplastic effects of imatinib mesylate (gleevec) in anaplastic thyroid cancer. J Clin Endocrinol Metab 2006; 91: 159-168. http://dx.doi.org/10.1210/jc.2005-1381
65. TAKAHASHI-YANAGA F, SASAGURI T: The Wnt/betacatenin signaling pathway as a target in drug discovery. J Pharmacol Sci 2007; 104: 293-302. http://dx.doi.org/10.1254/jphs.CR0070024
66. ZHANG Q, MAJOR MB, TAKANASHI S, CAMP ND, NISHIYA N et al. Small-molecule synergist of the Wnt/betacatenin signaling pathway. Proc Natl Acad Sci U S A 2007; 104: 7444-7448. http://dx.doi.org/10.1073/pnas.0702136104
67. MIYABAYASHI T, TEO JL, YAMAMOTO M, MCMILLAN M, NGUYEN C et al. Wnt/beta-catenin/CBP signaling maintains long-term murine embryonic stem cell pluripotency. Proc Natl Acad Sci U S A 2007; 104: 5668-5673. http://dx.doi. org/10.1073/pnas.0701331104
68. BOLOS V, BLANCO M, MEDINA V, APARICIO G, DIAZPRADO S et al. Notch signalling in cancer stem cells. Clin Transl Oncol 2009; 11: 11-19. http://dx.doi.org/10.1007/s12094-009-0305-2
69. FIUZA UM, ARIAS AM Cell and molecular biology of Notch. J Endocrinol 2007; 194: 459-474. http://dx.doi.org/10.1677/JOE-07-0242
70. KLEIN T, BRENNAN K, ARIAS AM An intrinsic dominant negative activity of serrate that is modulated during wing development in Drosophila. Dev Biol 1997; 189: 123-134. http://dx.doi.org/10.1006/dbio.1997.8564
71. LOWELL S, JONES P, LE ROUX I, DUNNE J, WATT FM Stimulation of human epidermal differentiation by deltanotch signalling at the boundaries of stem-cell clusters. Curr Biol 2000; 10: 491-500. http://dx.doi.org/10.1016/S0960-9822(00)00451-6
72. WU Y, ZHOU BP New insights of epithelial-mesenchymal transition in cancer metastasis. Acta Biochim Biophys Sin (Shanghai) 2008; 40: 643-650. http://dx.doi.org/10.1111/j.1745-7270.2008.00443.x
73. AULEHLA A, WEHRLE C, BRAND-SABERI B, KEMLER R, GOSSLER A et al. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 2003; 4: 395-406. http://dx.doi.org/10.1016/S1534-5807(03)00055-8
74. CONLON RA, REAUME AG, ROSSANT J Notch1 is required for the coordinate segmentation of somites. Development 1995; 121: 1533-1545.
75. PARKS AL, HUPPERT SS, MUSKAVITCH MAT The dynamic of neuronic signalling underlying bristle development in Drosophila melanogaster. Mech Dev 1997; 63: 61-74. http://dx.doi. org/10.1016/S0925-4773(97)00675-8
76. KIERNAN AE, CORDES R, KOPAN R, GOSSLER A, GRIDLEY T The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 2005; 132: 4353-4362. http://dx.doi.org/10.1242/dev.02002
77. CHIBA S Notch signaling in stem cell systems. Stem Cells 2006; 24: 2437-2447. http://dx.doi.org/10.1634/stemcells.2005-0661
78. KITA A, IMAYOSHI I, HOJO M, KITAGAWA M, KOKUBU H et al. Hes1 and Hes5 Control the Progenitor Pool, Intermediate Lobe Specification, and Posterior Lobe Formation in the Pituitary Development. Mol Endocrinol 2007; 21: 1458-1466. http://dx.doi.org/10.1210/me.2007-0039
79. LEE CS, KAESTNER KH Clinical endocrinology and metabolism. Development of gut endocrine cells. Best Pract Res Clin Endocrinol Metab 2004; 18: 453-462. http://dx.doi. org/10.1016/j.beem.2004.08.008
80. NOGGLE SA, WEILER D, CONDIE BG Notch signaling is inactive but inducible in human embryonic stem cells. Stem Cells 2006; 24: 1646-1653. http://dx.doi.org/10.1634/stemcells.2005-0314
81. MOLOFSKY AV, PARDAL R, MORRISON SJ Diverse mechanisms regulate stem cell self-renewal. Curr Opin Cell Biol 2004; 16: 700-707. http://dx.doi.org/10.1016/j.ceb.2004.09.004
82. SCHMITT TM, DE POOTER RF, GRONSKI MA et al. Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiatied in vitro. Nat Immunol 2004; 5: 410-417. http://dx.doi.org/10.1038/ni1055
83. LUTOLF S, RADTKE F, AGUET M, SUTER U, TAYLOR V Notch1 is required for neuronal and glial differentiation in the cerebellum. Development 2002; 129: 373-385.
84. OHTSUKA T, SAKAMOTO M, GUILLEMOT F, KAGEYAMA R Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J Biol Chem 2001; 276: 30467-30474. http://dx.doi.org/10.1074/jbc. M102420200
85. RAMASAMY SK, LENKA N Notch exhibits ligand bias and maneuvers stage-specific steering of neural differentiation in embryonic stem cells. Mol Cell Biol 2010; 30: 1946-1957. http://dx.doi.org/10.1128/MCB.01419-09
86. CRAWFORD TQ, ROELINK H The notch response inhibitor DAPT enhances neuronal differentiation in embryonic stem cell-derived embryoid bodies independently of sonic hedgehog signaling. Dev Dyn 2007; 236: 886-892. http://dx.doi. org/10.1002/dvdy.21083
87. DONTU G, JACKSON KW, MCNICHOLAS E, KAWAMURA MJ, ABDALLAH WM et al. Role of Notch signaling in cellfate determination of human mammary stem/progenitor cells. Breast Cancer Res 2004; 6: R605-615. http://dx.doi. org/10.1186/bcr920
88. DEVGAN V, MAMMUCARI C, MILLAR SE, BRISKEN C, DOTTO GP p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 2005; 19: 1485-1495. http://dx.doi.org/10.1101/gad.341405
89. NOSEDA M, CHANG L, MCLEAN G, GRIM JE, CLURMAN BE et al. Notch activation induces endothelial cell cycle arrest and participates in contact inhibition: role of p21Cip1 repression. Mol Cell Biol 2004; 24: 8813-8822. http://dx.doi. org/10.1128/MCB.24.20.8813-8822.2004
90. LIU ZJ, XIAO M, BALINT K, SOMA A, PINNIX CC et al. Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. FASEB J 2006; 20: 1009-1011. http://dx.doi. org/10.1096/fj.05-4880fje
91. KANG DE, YOON IS, REPETTO E, BUSSE T, YERMIAN N et al. Presenilins mediate phosphatidylinositol 3-kinase/AKT and ERK activation via select signaling receptors. Selectivity of PS2 in platelet-derived growth factor signaling. J Biol Chem 2005; 280: 31537-31547. http://dx.doi.org/10.1074/jbc. M500833200
92. MUNGAMURI SK, YANG X, THOR AD, SOMASUNDARAM K Survival signaling by Notch1: mammalian target of rapamycin (mTOR)-dependent inhibition of p53. Cancer Res 2006; 66: 4715-4724. http://dx.doi.org/10.1158/0008-5472. CAN-05-3830
93. GUPTA-ROSSI N, SIX E, LEBAIL O, LOGEAT F, CHASTAGNER P et al. Monoubiquitination and endocytosis direct gamma-secretase cleavage of activated Notch receptor. J Cell Biol 2004; 166: 73-83. http://dx.doi.org/10.1083/jcb.200310098
94. SEUGNET L, SIMPSON P, HAENLIN M Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev Biol 1997; 192: 585-598. http://dx.doi. org/10.1006/dbio.1997.8723
95. WILKIN MB, CARBERY AM, FOSTIER M, ASLAM H, MAZALEYRAT SL et al. Regulation of notch endosomal sorting and signaling by Drosophila Nedd4 family proteins. Curr Biol 2004; 14: 2237-2244. http://dx.doi.org/10.1016/j.cub.2004.11.030
96. HORI K, FOSTIER M, ITO M, FUWA TJ, GO MJ et al. Drosophila deltex mediates suppressor of Hairless-independent and late-endosomal activation of Notch signaling. Development 2004; 131: 5527-5537. http://dx.doi.org/10.1242/dev.01448
97. LE BORGNE R Regulation of Notch signalling by endocytosis and endosomal sorting. Curr Opin Cell Biol 2006; 18: 213-222. http://dx.doi.org/10.1016/j.ceb.2006.02.011
98. LE BORGNE R, BARDIN A, SCHWEISGUTH F The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 2005; 132: 1751-1762. http://dx.doi.org/10.1242/dev.01789
99. BRENNAN K, TATESON R, LIEBER T, COUSO JP, ZECCHINI V et al. The abruptex mutations of notch disrupt the establishment of proneural clusters in Drosophila. Dev Biol 1999; 216: 230-242. http://dx.doi.org/10.1006/dbio.1999.9501
100. LAWRENCE N, KLEIN T, BRENNAN K, MARTINEZ ARIAS A Structural requirements for notch signalling with delta and serrate during the development and patterning of the wing disc of Drosophila. Development 2000; 127: 3185-3195.
101. NICOLAS M, WOLFER A, RAJ K, KUMMER JA, MILL P et al. Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 2003; 33: 416-421. http://dx.doi.org/10.1038/ng1099
102. WEIJZEN S, RIZZO P, BRAID M, VAISHNAV R, JONKHEER SM et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat Med 2002; 8: 979-986. http://dx.doi.org/10.1038/nm754
103. PHILLIPS TM, MCBRIDE WH, PAJONK F The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006; 98: 1777-1785. http://dx.doi. org/10.1093/jnci/djj495
104. ZHENG Q, QIN H, ZHANG H, LI J, HOU L et al. Notch signaling inhibits growth of the human lung adenocarcinoma cell line A549. Oncol Rep 2007; 17: 847-852.
105. SRIURANPONG V, BORGES MW, RAVI RK, ARNOLD DR, NELKIN BD et al. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res 2001; 61: 3200-3205.
106. KALIRAI H, CLARKE RB Human breast epithelial stem cells and their regulation. J Pathol 2006; 208: 7-16. http://dx.doi. org/10.1002/path.1881
107. ECHELARD Y, EPSTEIN DJ, ST-JACQUES B, SHEN L, MOHLER J et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 1993; 75: 1417-1430. http://dx.doi. org/10.1016/0092-8674(93)90627-3
108. BALORDI F, FISHELL G Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wildtype stem cells have a limited capacity for self-renewal. J Neurosci 2007; 27: 14248-14259. http://dx.doi.org/10.1523/JNEUROSCI.4531-07.2007
109. KAWAHIRA H, MA NH, TZANAKAKIS ES, MCMAHON AP, CHUANG PT et al. Combined activities of hedgehog signaling inhibitors regulate pancreas development. Development 2003; 130: 4871-4879. http://dx.doi.org/10.1242/dev.00653
110. LIU S, DONTU G, MANTLE ID, PATEL S, AHN NS et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 2006; 66: 6063-6071. http://dx.doi.org/10.1158/0008-5472. CAN-06-0054
111. HUTCHIN ME, KARIAPPER MS, GRACHTCHOUK M, WANG A, WEI L et al. Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: conditional skin tumorigenesis recapitulates the hair growth cycle. Genes Dev 2005; 19: 214-223. http://dx.doi.org/10.1101/gad.1258705
112. HATSELL S, FROST AR Hedgehog signaling in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia 2007; 12: 163-173. http://dx.doi.org/10.1007/s10911-007-9048-2
113. MFOPOU JK, BOUWENS L Hedgehog signals in pancreatic differentiation from embryonic stem cells: revisiting the neglected. Differentiation 2008; 76: 107-117. http://dx.doi. org/10.1111/j.1432-0436.2007.00191.x
114. VAN TUYL M, POST M From fruitflies to mammals: mechanisms of signalling via the Sonic hedgehog pathway in lung development. Respir Res 2000; 1: 30-35. http://dx.doi. org/10.1186/rr9
115. ELLIS T, SMYTH I, RILEY E, BOWLES J, ADOLPHE C et al. Overexpression of Sonic Hedgehog suppresses embryonic hair follicle morphogenesis. Dev Biol 2003; 263: 203-215. http://dx.doi.org/10.1016/S0012-1606(03)00394-4
116. CAI C, THORNE J, GRABEL L Hedgehog serves as a mitogen and survival factor during embryonic stem cell neurogenesis. Stem Cells 2008; 26: 1097-1108. http://dx.doi.org/10.1634/stemcells.2007-0684
117. RHO JY, YU K, HAN JS, CHAE JI, KOO DB et al. Transcriptional profiling of the developmentally important signalling pathways in human embryonic stem cells. Hum Reprod 2006; 21: 405-412.
118. CHARAFE-JAUFFRET E, MONVILLE F, GINESTIER C, DONTU G, BIRNBAUM D et al. Cancer stem cells in breast: current opinion and future challenges. Pathobiology 2008; 75: 75-84. http://dx.doi.org/10.1159/000123845
119. HEISER PW, LAU J, TAKETO MM, HERRERA PL, HEBROK M Stabilization of beta-catenin impacts pancreas growth. Development 2006; 133: 2023-2032. http://dx.doi.org/10.1242/dev.02366
120. RIOBO NA, LU K, AI X, HAINES GM, EMERSON CP JR Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc Natl Acad Sci U S A 2006; 103: 4505-4510. http://dx.doi.org/10.1073/pnas.0504337103
121. LEE CJ, DOSCH J, SIMEONE DM Pancreatic Cancer Stem Cells. J Clin Oncol 2008; 26: 2806-2812. http://dx.doi. org/10.1200/JCO.2008.16.6702
122. KARHADKAR SS, BOVA GS, ABDALLAH N, DHARA S, GARDNER D et al. Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 2004; 431: 707-712. http://dx.doi.org/10.1038/nature02962
123. MEDINA V, CALVO MB, DIAZ-PRADO S, ESPADA J Hedgehog signalling as a target in cancer stem cells. Clin Transl Oncol 2009; 11: 199-207. http://dx.doi.org/10.1007/s12094-009-0341-y
124. VARNAT F, DUQUET A, MALERBA M, ZBINDEN M, MAS C et al. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med 2009; 1: 338-351. http://dx.doi. org/10.1002/emmm.200900039
125. GULINO A, FERRETTI E, DE SMAELE E Hedgehog signalling in colon cancer and stem cells. EMBO Mol Med 2009; 1: 300-302. http://dx.doi.org/10.1002/emmm.200900042
126. DEAN M, FOJO T, BATES S Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284. http://dx.doi. org/10.1038/nrc1590
127. MASSARD C, DEUTSCH E, SORIA JC Tumour stem cell-targeted treatment: elimination or differentiation. Ann Oncol 2006; 17: 1620-1624. http://dx.doi.org/10.1093/annonc/mdl074
128. MUELLER MT, HERMANN PC, WITTHAUER J, RUBIO-VIQUEIRA B, LEICHT SF et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009; 137: 1102-1113. http://dx.doi.org/10.1053/j.gastro.2009.05.053
129. SHINDO N, SAKAI A, ARAI D, MATSUOKA O, YAMASAKI Y et al. The ESC-E(Z) complex participates in the hedgehog signaling pathway. Biochem Biophys Res Commun 2005; 327: 1179-1187. http://dx.doi.org/10.1016/j.bbrc.2004.12.125
130. CHEN YL, CHEN HC, CHAN HY, CHUANG CK, CHANG YH et al. Co-conjugating chondroitin-6-sulfate/dermatan sulfate to chitosan scaffold alters chondrocyte gene expression and signaling profiles. Biotechnol Bioeng 2008; 101: 821-830. http://dx.doi.org/10.1002/bit.21953