Asymmetric distribution of epidermal growth factor receptor directs the fate of normal and cancer keratinocytes in vitro

Stem Cells and Development

Volumn 19, Issue 2, 2010, Pages 209-220

  Le Roy, Hélène ^a   Zuliani, Thomas ^a   Wolowczuk, Isabelle ^b   Faivre, Nathan ^a   Jouy, Nathalie ^c   Masselot, Bernadette ^a,d   Kerkaert, Jean Pierre ^a,c,e   Formstecher, Pierre ^a,d,f   Polakowska, Renata ^a,d  

^a JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^b INSTITUT PASTEUR DE LILLE   (France)

^c Institut Pour la Recherche sur le Cancer de Lille (IRCL)   (France)

^d UNIV LILLE   (France)

^e IMPRT IFR114   (France)

^f LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; EPIDERMAL GROWTH FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL CYCLE; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL SELECTION; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIUM CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; MITOCHONDRION; MITOSIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEM CELL;

EID: 77649127139     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0150     Document Type: Article

References (85)

1. Slack JM. (2008). Origin of stem cells in organogenesis. Science 322:1498-1501.
2. Visvader JE and GJ Lindeman. (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8:755-768.
3. Kim CF and PB Dirks. (2008). Cancer and stem cell biology: how tightly intertwined? Cell Stem Cell 3:147-150.
4. Wang Y and SA Armstrong. (2008). Cancer: inappropriate expression of stem cell programs? Cell Stem Cell 2:297-299.
5. Dick JE. (2008). Stem cell concepts renew cancer research. Blood 112:4793-4807.
6. Knoblich JA. (2008). Mechanisms of asymmetric stem cell division. Cell 132:583-597.
7. Giebel B and I Bruns. (2008). Self-renewal versus differentiation in hematopoietic stem and progenitor cells: a focus on asymmetric cell divisions. Curr Stem Cell Res Ther 3:9-16.
8. Sun Y, SK Goderie and S Temple. (2005). Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45:873-886.
9. Normanno N, A De Luca, C Bianco, L Strizzi, M Mancino, MR Maiello, A Carotenuto, G De Feo, F Caponigro and DS Salomon. (2006). Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366:2-16.
10. Singh AB and RC Harris. (2005). Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 17:1183-1193.
11. Schneider MR, S Werner, R Paus and E Wolf. (2008). Beyond wavy hairs: the epidermal growth factor receptor and its ligands in skin biology and pathology. Am J Pathol 173:14-24.
12. de Giorgi V, S Sestini, D Massi, I Ghersetich and T Lotti. (2007). Keratinocyte growth factor receptors. Dermatol Clin 25:477-85, vii.
13. Jost M, C Kari and U Rodeck. (2000). The EGF receptor - an essential regulator of multiple epidermal functions. Eur J Dermatol 10:505-510.
14. Fortunel NO, JA Hatzfeld, PA Rosemary, C Ferraris, MN Monier, V Haydont, J Longuet, B Brethon, B Lim, I Castiel, R Schmidt and A Hatzfeld. (2003). Long-term expansion of human functional epidermal precursor cells: promotion of extensive amplification by low TGF-beta1 concentrations. J Cell Sci 116(Pt19):4043-4052.
15. Lacouture ME. (2006). Mechanisms of cutaneous toxicities to EGFR inhibitors. Nat Rev Cancer 6:803-812.
16. Reya T, SJ Morrison, MF Clarke and IL Weissman. (2001). Stem cells, cancer, and cancer stem cells. Nature 414:105-111.
17. Tysnes BB and R Bjerkvig. (2007). Cancer initiation and progression: involvement of stem cells and the microenvironment. Biochim Biophys Acta 1775:283-297.
18. Giard DJ, SA Aaronson, GJ Todaro, P Arnstein, JH Kersey, H Dosik and WP Parks. (1973). In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 51:1417-1423.
19. Brysk MM, CH Santschi, T Bell, RF Wagner Jr, SK Tyring and S Rajaraman. (1992). Culture of basal cell carcinoma. J Invest Dermatol 98:45-49.
20. Allombert-Blaise C, S Tamiji, L Mortier, H Fauvel, M Tual, E Delaporte, F Piette, EM DeLassale, P Formstecher, P Marchetti and R Polakowska. (2003). Terminal differentiation of human epidermal keratinocytes involves mitochondria- and caspase-dependent cell death pathway. Cell Death Differ 10:850-852.
21. Tamiji S, JC Beauvillain, L Mortier, N Jouy, M Tual, E Delaporte, P Formstecher, P Marchetti and R Polakowska. (2005). Induction of apoptosis-like mitochondrial impairment triggers antioxidant and Bcl-2-dependent keratinocyte differentiation. J Invest Dermatol 125:647-658.
22. Redvers RP, A Li and P Kaur. (2006). Side population in adult murine epidermis exhibits phenotypic and functional characteristics of keratinocyte stem cells. Proc Natl Acad Sci USA 103:13168-13173.
23. Bertoncello I and B Williams. (2004). Hematopoietic stem cell characterization by Hoechst 33342 and rhodamine 123 staining. Methods Mol Biol 263:181-200.
24. McKenzie JL, K Takenaka, OI Gan, M Doedens and JE Dick. (2007). Low rhodamine 123 retention identifies long-term human hematopoietic stem cells within the Lin-CD34+CD38-population. Blood 109:543-545.
25. Donnenberg VS, EM Meyer and AD Donnenberg. (2009). Measurement of multiple drug resistance transporter activity in putative cancer stem/progenitor cells. Methods Mol Biol 568:261-279.
26. Challen GA and MH Little. (2006). A side order of stem cells: the SP phenotype. Stem Cells 24:3-12.
27. Mackenzie IC. (2006). Stem cell properties and epithelial malignancies. Eur J Cancer 42:1204-1212.
28. Prince ME, R Sivanandan, A Kaczorowski, GT Wolf, MJ Kaplan, P Dalerba, IL Weissman, MF Clarke and LE Ailles. (2007). Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 104:973-978.
29. Thorburn A. (2004). Death receptor-induced cell killing. Cell Signal 16:139-144.
30. Besson A, SF Dowdy and JM Roberts. (2008). CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14:159-169.
31. Nasmyth K. (2001). A prize for proliferation. Cell 107:689-701.
32. Horsley V, AO Aliprantis, L Polak, LH Glimcher and E Fuchs. (2008). NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132:299-310.
33. Janzen V and DT Scadden. (2006). Stem cells: good, bad and reformable. Nature 441:418-419.
34. Orford KW and DT Scadden. (2008). Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9:115-128.
35. Rexer BN, JA Engelman and CL Arteaga. (2009). Overcoming resistance to tyrosine kinase inhibitors: Lessons learned from cancer cells treated with EGFR antagonists. Cell Cycle 8:18-22.
36. Buss JE, JE Kudlow, CS Lazar and GN Gill. (1982). Altered epidermal growth factor (EGF)-stimulated protein kinase activity in variant A431 cells with altered growth responses to EGF. Proc Natl Acad Sci USA 79:2574-2578.
37. Barrandon Y and H Green. (1987). Three clonal types of keratinocyte with different capacities for multiplication. Proc Natl Acad Sci USA 84:2302-2306.
38. Pellegrini G, O Golisano, P Paterna, A Lambiase, S Bonini, P Rama and M De Luca. (1999). Location and clonal analysis of stem cells and their differentiated progeny in the human ocular surface. J Cell Biol 145:769-782.
39. Reynolds BA and RL Rietze. (2005). Neural stem cells and neurospheres - re-evaluating the relationship. Nat Methods 2:333-336.
40. Coles-Takabe BL, I Brain, KA Purpura, P Karpowicz, PW Zandstra, CM Morshead and D van der Kooy. (2008). Don't look: growing clonal versus nonclonal neural stem cell colonies. Stem Cells 26:2938-2944.
41. Harper LJ, K Piper, J Common, F Fortune and IC Mackenzie. (2007). Stem cell patterns in cell lines derived from head and neck squamous cell carcinoma. J Oral Pathol Med 36:594-603.
42. Filipowicz E, P Adegboyega, RL Sanchez and Z Gatalica. (2002). Expression of CD95 (Fas) in sun-exposed human skin and cutaneous carcinomas. Cancer 94:814-819.
43. Yasuda M, Y Tanaka, K Fujii and K Yasumoto. (2001). CD44 stimulation down-regulates Fas expression and Fas-mediated apoptosis of lung cancer cells. Int Immunol 13:1309-1319.
44. Kim Y, YS Lee, J Choe, H Lee, YM Kim and D Jeoung. (2008). CD44-epidermal growth factor receptor interaction mediates hyaluronic acid-promoted cell motility by activating protein kinase C signaling involving Akt, Rac1, Phox, reactive oxygen species, focal adhesion kinase, and MMP-2. J Biol Chem 283:22513-22528.
45. Reinehr R and D Häussinger. (2007). Hyperosmotic activation of the CD95 system. Meth Enzymol 428:145-160.
46. Lo HW and MC Hung. (2006). Nuclear EGFR signalling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway and patient survival. Br J Cancer 94:184-188.
47. Webb A, A Li and P Kaur. (2004). Location and phenotype of human adult keratinocyte stem cells of the skin. Differentiation 72:387-395.
48. Ito M, Y Liu, Z Yang, J Nguyen, F Liang, RJ Morris and G Cotsarelis. (2005). Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 11:1351-1354.
49. Fuchs E and H Green. (1980). Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell 19:1033-1042.
50. Benitah SA, M Frye, M Glogauer and FM Watt. (2005). Stem cell depletion through epidermal deletion of Rac1. Science 309:933-935.
51. Mammucari C, A Tommasi di Vignano, AA Sharov, J Neilson, MC Havrda, DR Roop, VA Botchkarev, GR Crabtree and GP Dotto. (2005). Integration of Notch 1 and calcineurin/NFAT signaling pathways in keratinocyte growth and differentiation control. Dev Cell 8:665-676.
52. Watt FM, S Estrach and CA Ambler. (2008). Epidermal Notch signalling: differentiation, cancer and adhesion. Curr Opin Cell Biol 20:171-179.
53. Scarpulla RC. (2008). Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann N Y Acad Sci 1147:321-334.
54. Vasioukhin V, L Degenstein, B Wise and E Fuchs. (1999). The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci USA 96:8551-8556.
55. Sibilia M and EF Wagner. (1995). Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269:234-238.
56. Murillas R, F Larcher, CJ Conti, M Santos, A Ullrich and JL Jorcano. (1995). Expression of a dominant negative mutant of epidermal growth factor receptor in the epidermis of transgenic mice elicits striking alterations in hair follicle development and skin structure. EMBO J 14:5216-5223.
57. Ciardiello F and G Tortora. (2008). EGFR antagonists in cancer treatment. N Engl J Med 358:1160-1174.
58. Sibilia M, R Kroismayr, BM Lichtenberger, A Natarajan, M Hecking and M Holcmann. (2007). The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75:770-787.
59. Schneider TE, C Barland, AM Alex, ML Mancianti, Y Lu, JE Cleaver, HJ Lawrence and R Ghadially. (2003). Measuring stem cell frequency in epidermis: a quantitative in vivo functional assay for long-term repopulating cells. Proc Natl Acad Sci USA 100:11412-11417.
60. Wilson A, E Laurenti, G Oser, RC van der Wath, W Blanco-Bose, M Jaworski, S Offner, CF Dunant, L Eshkind, E Bockamp, P Liá, HR Macdonald and A Trumpp. (2008). Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135:1118-1129.
61. Ratajczak MZ. (2008). Phenotypic and functional characterization of hematopoietic stem cells. Curr Opin Hematol 15:293-300.
62. Venezia TA, AA Merchant, CA Ramos, NL Whitehouse, AS Young, CA Shaw and MA Goodell. (2004). Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol 2:e301.
63. Glauche I, K Moore, L Thielecke, K Horn, M Loeffler and I Roeder. (2009). Stem cell proliferation and quiescence - two sides of the same coin. PLoS Comput Biol 5:e1000447.
64. Morrison SJ and AC Spradling. (2008). Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598-611.
65. Rosen JM and CT Jordan. (2009). The increasing complexity of the cancer stem cell paradigm. Science 324:1670-1673.
66. Discher DE, DJ Mooney and PW Zandstra. (2009). Growth factors, matrices, and forces combine and control stem cells. Science 324:1673-1677.
67. Croft DR and MF Olson. (2006). The Rho GTPase effector ROCK regulates cyclin A, cyclin D1, and p27Kip1 levels by distinct mechanisms. Mol Cell Biol 26:4612-4627.
68. O'Hagan KA, S Cocchiglia, AV Zhdanov, MM Tambuwala, MM Tambawala, EP Cummins, M Monfared, TA Agbor, JF Garvey, DB Papkovsky, CT Taylor and BB Allan. (2009). PGC-1alpha is coupled to HIF-1alpha-dependent gene expression by increasing mitochondrial oxygen consumption in skeletal muscle cells. Proc Natl Acad Sci USA 106:2188-2193.
69. Chen C, Y Liu, R Liu, T Ikenoue, KL Guan, Y Liu and P Zheng. (2008). TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 205:2397-2408.
70. Finkel T. (2006). Cell biology: a clean energy programme. Nature 444:151-152.
71. Zhang H, P Gao, R Fukuda, G Kumar, B Krishnamachary, KI Zeller, CV Dang and GL Semenza. (2007). HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11:407-420.
72. Jang YY and SJ Sharkis. (2007). A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110:3056-3063.
73. Koshiji M, Y Kageyama, EA Pete, I Horikawa, JC Barrett and LE Huang. (2004). HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23:1949-1956.
74. Dang CV, JW Kim, P Gao and J Yustein. (2008). The interplay between MYC and HIF in cancer. Nat Rev Cancer 8:51-56.
75. Lonergan T, B Bavister and C Brenner. (2007). Mitochondria in stem cells. Mitochondrion 7:289-296.
76. Cunningham JJ and MF Roussel. (2001). Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ 12:387-396.
77. Essers MA, S Offner, WE Blanco-Bose, Z Waibler, U Kalinke, MA Duchosal and A Trumpp. (2009). IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458:904-908.
78. Malhotra S and PW Kincade. (2009). Wnt-related molecules and signaling pathway equilibrium in hematopoiesis. Cell Stem Cell 4:27-36.
79. Zon LI. (2008). Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 453:306-313.
80. Iwasaki H and T Suda. (2009). Cancer stem cells and their niche. Cancer Sci 100:1166-1172.
81. Setoguchi T, T Taga and T Kondo. (2004). Cancer stem cells persist in many cancer cell lines. Cell Cycle 3:414-415.
82. Pollard SM, K Yoshikawa, ID Clarke, D Danovi, S Stricker, R Russell, J Bayani, R Head, M Lee, M Bernstein, JA Squire, A Smith and P Dirks. (2009). Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4: 568-580.
83. Fillmore CM and C Kuperwasser. (2008). Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10:R25.
84. van Staveren WC, DY Solís, A Hébrant, V Detours, JE Dumont and C Maenhaut. (2009). Human cancer cell lines: Experimental models for cancer cells in situ? For cancer stem cells? Biochim Biophys Acta 1795:92-103.
85. Rossi DJ, CH Jamieson and IL Weissman. (2008). Stems cells and the pathways to aging and cancer. Cell 132:681-696.