The mysterious human epidermal cell cycle, or an oncogene-induced differentiation checkpoint

Cell Cycle

Volumn 11, Issue 24, 2012, Pages 4507-4516

  Gandarillas, Alberto ^a,b  

^a HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^b INSERM   (France)

Author keywords

Cancer; Cell cycle; Differentiation; DNA damage; Epidermis; Leukemia; MYC; OID; Replication stress; Stem cells

Indexed keywords

CYCLIN A; CYCLIN B; CYCLIN D; CYCLIN E; GREEN FLUORESCENT PROTEIN; MYC PROTEIN; PROTEIN P53;

APOPTOSIS; CELL AGING; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CELL FATE; CELL GROWTH; CELL PROLIFERATION; DNA DAMAGE; DNA REPLICATION; ENDOREDUPLICATION; EPIDERMIS CELL; HUMAN; KERATINOCYTE; MITOSIS; NONHUMAN; PROTEIN EXPRESSION; REVIEW;

EID: 84871480959     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.22529     Document Type: Review

References (84)

1. Meyer N, Penn LZ. Reflecting on 25 years with MYC. Nat Rev Cancer 2008; 8:976-90; PMID:19029958; http://dx.doi.org/10.1038/nrc2231.
2. Eilers M, Eisenman RN. Myc's broad reach. Genes Dev 2008; 22:2755-66; PMID:18923074; http://dx.doi.org/10.1101/gad.1712408.
3. Blagosklonny MV, Pardee AB. The restriction point of the cell cycle. Cell Cycle 2002; 1:103-10; PMID:12429916; http://dx.doi.org/10.4161/cc.1.2.108.
4. Askew DS, Ashmun RA, Simmons BC, Cleveland JL. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 1991; 6:1915-22; PMID:1923514.
5. Shi Y, Glynn JM, Guilbert LJ, Cotter TG, Bissonnette RP, Green DR. Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas. Science 1992; 257:212-4; PMID:1378649; http://dx.doi.org/10.1126/science. 1378649.
6. Evan GI, Littlewood TD. The role of c-myc in cell growth. Curr Opin Genet Dev 1993; 3:44-9; PMID:8453273; http://dx.doi.org/10.1016/S0959-437X(05)80339- 9.
7. León J, Ferrandiz N, Acosta JC, Delgado MD. Inhibition of cell differentiation: a critical mechanism for MYC-mediated carcinogenesis? Cell Cycle 2009; 8:1148-57; PMID:19282668; http://dx.doi.org/10.4161/cc.8.8.8126.
8. Smith KN, Lim JM, Wells L, Dalton S. Myc orchestrates a regulatory network required for the establishment and maintenance of pluripotency. Cell Cycle 2011; 10:592-7; PMID:21293186; http://dx.doi.org/10.4161/cc.10.4.14792.
9. Waikel RL, Kawachi Y, Waikel PA, Wang XJ, Roop DR. Deregulated expression of c-Myc depletes epidermal stem cells. Nat Genet 2001; 28:165-8; PMID:11381265; http://dx.doi.org/10.1038/88889.
10. Gandarillas A, Watt FM. c-Myc promotes differentiation of human epidermal stem cells. Genes Dev 1997; 11:2869-82; PMID:9353256; http://dx.doi.org/10. 1101/gad.11.21.2869.
11. Arnold I, Watt FM. c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr Biol 2001; 11:558-68; PMID:11369200; http://dx.doi.org/10.1016/S0960-9822(01)00154-3.
12. Böni R, Schuster C, Nehrhoff B, Burg G. Epidemiology of skin cancer. Neuro Endocrinol Lett 2002; 23(Suppl 2):48-51; PMID:12163848.
13. Brash DE, Ziegler A, Jonason AS, Simon JA, Kunala S, Leffell DJ. Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J Investig Dermatol Symp Proc 1996; 1:136-42; PMID:9627707.
14. Kulms D, Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 2000; 16:195-201; PMID:11068857; http://dx.doi.org/10.1034/j.1600-0781.2000.160501.x.
15. Banks-Schlegel S, Green H. Involucrin synthesis and tissue assembly by keratinocytes in natural and cultured human epithelia. J Cell Biol 1981; 90:732-7; PMID:6895225; http://dx.doi.org/10.1083/jcb.90.3.732.
16. Flores I, Murphy DJ, Swigart LB, Knies U, Evan GI. Defining the temporal requirements for Myc in the progression and maintenance of skin neoplasia. Oncogene 2004; 23:5923-30; PMID:15208685; http://dx.doi.org/10.1038/sj.onc. 1207796.
17. Frye M, Gardner C, Li ER, Arnold I, Watt FM. Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development 2003; 130:2793-808; PMID:12736221; http://dx.doi.org/10.1242/dev.00462.
18. Gebhardt A, Frye M, Herold S, Benitah SA, Braun K, Samans B, et al. Myc regulates keratinocyte adhesion and differentiation via complex formation with Miz1. J Cell Biol 2006; 172:139-49; PMID:16391002; http://dx.doi.org/10.1083/ jcb.200506057.
19. Gandarillas A, Davies D, Blanchard JM. Normal and c-Myc-promoted human keratinocyte differentiation both occur via a novel cell cycle involving cellular growth and endoreplication. Oncogene 2000; 19:3278-89; PMID:10918584; http://dx.doi.org/10.1038/sj.onc.1203630.
20. Edgar BA, Orr-Weaver TL. Endoreplication cell cycles: more for less. Cell 2001; 105:297-306; PMID:11348589; http://dx.doi.org/10.1016/S0092-8674(01) 00334-8.
21. De Veylder L, Larkin JC, Schnittger A. Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 2011; 16:624-34; PMID:21889902; http://dx.doi.org/10.1016/j.tplants.2011.07.001.
22. Ramirez A, Page A, Gandarillas A, Zanet J, Pibre S, Vidal M, et al. A keratin K5Cre transgenic line appropriate for tissue-specific or generalized Cre-mediated recombination. Genesis 2004; 39:52-7; PMID:15124227; http://dx.doi.org/10.1002/gene.20025.
23. Zanet J, Pibre S, Jacquet C, Ramirez A, de Alborán IM, Gandarillas A. Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification. J Cell Sci 2005; 118:1693-704; PMID:15797928; http://dx.doi.org/10.1242/jcs.02298.
24. Levens D. Disentangling the MYC web. Proc Natl Acad Sci USA 2002; 99:5757-9; PMID:11983876; http://dx.doi.org/10.1073/pnas.102173199.
25. Gomez-Roman N, Grandori C, Eisenman RN, White RJ. Direct activation of RNA polymerase III transcription by c-Myc. Nature 2003; 421:290-4; PMID:12529648; http://dx.doi.org/10.1038/nature01327.
26. Oskarsson T, Essers MA, Dubois N, Offner S, Dubey C, Roger C, et al. Skin epidermis lacking the c-Myc gene is resistant to Ras-driven tumorigenesis but can reacquire sensitivity upon additional loss of the p21Cip1 gene. Genes Dev 2006; 20:2024-9; PMID:16882980; http://dx.doi.org/10.1101/gad.381206.
27. Baena E, Gandarillas A, Vallespinós M, Zanet J, Bachs O, Redondo C, et al. c-Myc regulates cell size and ploidy but is not essential for postnatal proliferation in liver. Proc Natl Acad Sci USA 2005; 102:7286-91; PMID:15857952; http://dx.doi.org/10.1073/pnas.0409260102.
28. Moumen M, Chiche A, Deugnier MA, Petit V, Gandarillas A, Glukhova MA, et al. The proto-oncogene Myc is essential for mammary stem cell function. Stem Cells 2012; 30:1246-54; PMID:22438054; http://dx.doi.org/10.1002/stem.1090.
29. Zanet J, Freije A, Ruiz M, Coulon V, Sanz JR, Chiesa J, et al. A mitosis block links active cell cycle with human epidermal differentiation and results in endoreplication. PLoS One 2010; 5:e15701; PMID:21187932; http://dx.doi.org/ 10.1371/journal.pone.0015701.
30. Harvat BL, Wang A, Seth P, Jetten AM. Up-regulation of p27Kip1, p21WAF1/Cip1 and p16Ink4a is associated with, but not sufficient for, induction of squamous differentiation. J Cell Sci 1998; 111:1185-96; PMID:9547295.
31. Di Cunto F, Topley G, Calautti E, Hsiao J, Ong L, Seth PK, et al. Inhibitory function of p21Cip1/WAF1 in differentiation of primary mouse keratinocytes independent of cell cycle control. Science 1998; 280:1069-72; PMID:9582119; http://dx.doi.org/10.1126/science.280.5366.1069.
32. Hauser PJ, Agrawal D, Pledger WJ. Primary keratinocytes have an adhesion dependent S phase checkpoint that is absent in immortalized cell lines. Oncogene 1998; 17:3083-92; PMID:9872324; http://dx.doi.org/10.1038/sj.onc.1202235.
33. Pierce AM, Gimenez-Conti IB, Schneider-Broussard R, Martinez LA, Conti CJ, Johnson DG. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc Natl Acad Sci USA 1998; 95:8858-63; PMID:9671769; http://dx.doi.org/10.1073/pnas.95.15.8858.
34. Robles AI, Larcher F, Whalin RB, Murillas R, Richie E, Gimenez-Conti IB, et al. Expression of Cyclin D1 in epithelial tissues of transgenic mice results in epidermal hyperproliferation and severe thymic hyperplasia. Proc Natl Acad Sci USA 1996; 93:7634-8; PMID:8755527; http://dx.doi.org/10.1073/pnas.93.15. 7634.
35. Rodriguez-Puebla ML, LaCava M, Miliani De Marval PL, Jorcano JL, Richie ER, Conti CJ. Cyclin D2 overexpression in transgenic mice induces thymic and epidermal hyperplasia whereas Cyclin D3 expression results only in epidermal hyperplasia. Am J Pathol 2000; 157:1039-50; PMID:10980142; http://dx.doi.org/10. 1016/S0002-9440(10)64616-0.
36. Alkhalaf M, Ganguli G, Messaddeq N, Le Meur M, Wasylyk B. MDM2 overexpression generates a skin phenotype in both wild type and p53 null mice. Oncogene 1999; 18:1419-34; PMID:10050879; http://dx.doi.org/10.1038/sj.onc. 1202448.
37. Miliani de Marval PL, Gimenez-Conti IB, LaCava M, Martinez LA, Conti CJ, Rodriguez-Puebla ML. Transgenic expression of Cyclin-dependent kinase 4 results in epidermal hyperplasia, hypertrophy, and severe dermal fibrosis. Am J Pathol 2001; 159:369-79; PMID:11438484; http://dx.doi.org/10.1016/S0002-9440(10)61703- 8.
38. Macias E, Miliani de Marval PL, Senderowicz A, Cullen J, Rodriguez-Puebla ML. Expression of CDK4 or CDK2 in mouse oral cavity is retained in adult pituitary with distinct effects on tumorigenesis. Cancer Res 2008; 68:162-71; PMID:18172308; http://dx.doi.org/10.1158/0008-5472.CAN-07-2461.
39. Régnier M, Vaigot P, Darmon M, Pruniéras M. Onset of epidermal differentiation in rapidly proliferating basal keratinocytes. J Invest Dermatol 1986; 87:472-6; PMID:2428884; http://dx.doi.org/10.1111/1523-1747. ep12455517.
40. Watt FM, Lo Celso C, Silva-Vargas V. Epidermal stem cells: an update. Curr Opin Genet Dev 2006; 16:518-24; PMID:16919447; http://dx.doi.org/10.1016/j. gde.2006.08.006.
41. Kartasova T, Roop DR, Yuspa SH. Relationship between the expression of differentiation-specific keratins 1 and 10 and cell proliferation in epidermal tumors. Mol Carcinog 1992; 6:18-25; PMID:1380247; http://dx.doi.org/10.1002/mc. 2940060105.
42. Paramio JM, Casanova ML, Segrelles C, Mittnacht S, Lane EB, Jorcano JL. Modulation of cell proliferation by cytokeratins K10 and K16. Mol Cell Biol 1999; 19:3086-94; PMID:10082575.
43. Santos M, Bravo A, López C, Paramio JM, Jorcano JL. Severe abnormalities in the oral mucosa induced by suprabasal expression of epidermal keratin K10 in transgenic mice. J Biol Chem 2002; 277:35371-7; PMID:12119299; http://dx.doi.org/10.1074/jbc.M205143200.
44. Rosa-Garrido M, Ceballos L, Alonso-Lecue P, Abraira C, Delgado MD, Gandarillas A. A cell cycle role for the epigenetic factor CTCF-L/BORIS. PLoS One 2012; 7:e39371; PMID:22724006; http://dx.doi.org/10.1371/journal.pone. 0039371.
45. Lilly MA, Duronio RJ. New insights into cell cycle control from the Drosophila endocycle. Oncogene 2005; 24:2765-75; PMID:15838513; http://dx.doi.org/10.1038/sj.onc.1208610.
46. Freije A, Ceballos L, Coisy M, Barnes L, Rosa M, De Diego E, et al. Cyclin E drives human keratinocyte growth into differentiation. Oncogene 2012; PMID:22349815; http://dx.doi.org/10.1038/onc.2012.22.
47. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319:1352-5; PMID:18323444; http://dx.doi.org/10.1126/science.1140735.
48. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444:638-42; PMID:17136094; http://dx.doi.org/10. 1038/nature05327.
49. Osborn AJ, Elledge SJ, Zou L. Checking on the fork: the DNA-replication stress-response pathway. Trends Cell Biol 2002; 12:509-16; PMID:12446112; http://dx.doi.org/10.1016/S0962-8924(02)02380-2.
50. Bester AC, Roniger M, Oren YS, Im MM, Sarni D, Chaoat M, et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011; 145:435-46; PMID:21529715; http://dx.doi.org/10.1016/j. cell.2011.03.044.
51. Dazard JE, Piette J, Basset-Seguin N, Blanchard JM, Gandarillas A. Switch from p53 to MDM2 as differentiating human keratinocytes lose their proliferative potential and increase in cellular size. Oncogene 2000; 19:3693-705; PMID:10949923; http://dx.doi.org/10.1038/sj.onc.1203695.
52. Jones PH, Harper S, Watt FM. Stem cell patterning and fate in human epidermis. Cell 1995; 80:83-93; PMID:7813021; http://dx.doi.org/10.1016/0092- 8674(95)90453-0.
53. Meyers J, Craig J, Odde DJ. Potential for control of signaling pathways via cell size and shape. Curr Biol 2006; 16:1685-93; PMID:16950104; http://dx.doi.org/10.1016/j.cub.2006.07.056.
54. Moseley JB, Mayeux A, Paoletti A, Nurse P. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 2009; 459:857-60; PMID:19474789; http://dx.doi.org/10.1038/nature08074.
55. Lechler T, Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005; 437:275-80; PMID:16094321; http://dx.doi.org/10.1038/nature03922.
56. Hauser P, Ma L, Agrawal D, Haura E, Cress WD, Pledger WJ. Efficient down-regulation of Cyclin A-associated activity and expression in suspended primary keratinocytes requires p21(Cip1). Mol Cancer Res 2004; 2:96-104; PMID:14985466.
57. rd, Chen X, Smeets M, Hengst L, Prives C, Reed SI. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol 1998; 18:629-43; PMID:9418909.
58. Medema RH, Klompmaker R, Smits VA, Rijksen G. p21waf1 can block cells at two points in the cell cycle, but does not interfere with processive DNA-replication or stress-activated kinases. Oncogene 1998; 16:431-41; PMID:9484832; http://dx.doi.org/10.1038/sj.onc.1201558.
59. Ullah Z, Lee CY, Depamphilis ML. Cip/Kip Cyclin-dependent protein kinase inhibitors and the road to polyploidy. Cell Div 2009; 4:10; PMID:19490616; http://dx.doi.org/10.1186/1747-1028-4-10.
60. Muñoz-Alonso MJ, Acosta JC, Richard C, Delgado MD, Sedivy J, León J. p21Cip1 and p27Kip1 induce distinct cell cycle effects and differentiation programs in myeloid leukemia cells. J Biol Chem 2005; 280:18120-9; PMID:15746092; http://dx.doi.org/10.1074/jbc.M500758200.
61. Muñoz-Alonso MJ, Ceballos L, Bretones G, Frade P, León J, Gandarillas A. MYC accelerates p21CIP-induced megakaryocytic differentiation involving early mitosis arrest in leukemia cells. J Cell Physiol 2012; 227:2069-78; PMID:21769863; http://dx.doi.org/10.1002/jcp.22935.
62. García P, Frampton J, Ballester A, Calés C. Ectopic expression of Cyclin E allows non-endomitotic megakaryoblastic K562 cells to establish re-replication cycles. Oncogene 2000; 19:1820-33; PMID:10777216; http://dx.doi.org/10.1038/sj.onc.1203494.
63. Johnston LA, Prober DA, Edgar BA, Eisenman RN, Gallant P. Drosophila myc regulates cellular growth during development. Cell 1999; 98:779-90; PMID:10499795; http://dx.doi.org/10.1016/S0092-8674(00)81512-3.
64. Polakowska RR, Piacentini M, Bartlett R, Goldsmith LA, Haake AR. Apoptosis in human skin development: morphogenesis, periderm, and stem cells. Dev Dyn 1994; 199:176-88; PMID:7517223; http://dx.doi.org/10.1002/aja. 1001990303.
65. Gandarillas A. Epidermal differentiation, apoptosis, and senescence: common pathways? Exp Gerontol 2000; 35:53-62; PMID:10705039; http://dx.doi.org/10.1016/S0531-5565(99)00088-1.
66. Beer S, Zetterberg A, Ihrie RA, McTaggart RA, Yang Q, Bradon N, et al. Developmental context determines latency of MYC-induced tumorigenesis. PLoS Biol 2004; 2:e332; PMID:15455033; http://dx.doi.org/10.1371/journal.pbio.0020332.
67. Conacci-Sorrell M, Ngouenet C, Eisenman RN. Myc-nick: a cytoplasmic cleavage product of Myc that promotes alpha-tubulin acetylation and cell differentiation. Cell 2010; 142:480-93; PMID:20691906; http://dx.doi.org/10. 1016/j.cell.2010.06.037.
68. Uribesalgo I, Benitah SA, Di Croce L. From oncogene to tumor suppressor: the dual role of Myc in leukemia. Cell Cycle 2012; 11:1757-64; PMID:22510570; http://dx.doi.org/10.4161/cc.19883.
69. Wang X, Kua HY, Hu Y, Guo K, Zeng Q, Wu Q, et al. p53 functions as a negative regulator of osteoblastogenesis, osteoblast-dependent osteoclastogenesis, and bone remodeling. J Cell Biol 2006; 172:115-25; PMID:16380437; http://dx.doi.org/10.1083/jcb.200507106.
70. Jiang D, Lenardo MJ, Zúñiga-Pflücker JC. p53 prevents maturation to the CD4+CD8+ stage of thymocyte differentiation in the absence of T cell receptor rearrangement. J Exp Med 1996; 183:1923-8; PMID:8666950; http://dx.doi.org/10.1084/jem.183.4.1923.
71. Sulic S, Panic L, Barkic M, Mercep M, Uzelac M, Volarevic S. Inactivation of S6 ribosomal protein gene in T lymphocytes activates a p53-dependent checkpoint response. Genes Dev 2005; 19:3070-82; PMID:16357222; http://dx.doi.org/10.1101/gad.359305.
72. Feinstein E, Gale RP, Reed J, Canaani E. Expression of the normal p53 gene induces differentiation of K562 cells. Oncogene 1992; 7:1853-7; PMID:1501893.
73. Demidenko ZN, Korotchkina LG, Gudkov AV, Blagosklonny MV. Paradoxical suppression of cellular senescence by p53. Proc Natl Acad Sci USA 2010; 107:9660-4; PMID:20457898; http://dx.doi.org/10.1073/pnas.1002298107.
74. Galluzzi L, Kepp O, Kroemer G. TP53 and MTOR crosstalk to regulate cellular senescence. Aging (Albany NY) 2010; 2:535-7; PMID:20876940.
75. Ren Z, Ponten F, Nister M, Ponten J. Reconstruction of the two-dimensional distribution of p53 positive staining patches in sun-exposed morphologically normal skin. Int J Oncol 1997; 11:111-5; PMID:21528187.
76. Wang J, Sun Q, Morita Y, Jiang H, Gross A, Lechel A, et al. A differentiation checkpoint limits hematopoietic stem cell self-renewal in response to DNA damage. Cell 2012; 148:1001-14; PMID:22385964; http://dx.doi.org/10.1016/j.cell.2012.01.040.
77. Ullah Z, de Renty C, DePamphilis ML. Checkpoint kinase 1 prevents cell cycle exit linked to terminal cell differentiation. Mol Cell Biol 2011; 31:4129-43; PMID:21791608; http://dx.doi.org/10.1128/MCB.05723-11.
78. Puri PL, Bhakta K, Wood LD, Costanzo A, Zhu J, Wang JY. A myogenic differentiation checkpoint activated by genotoxic stress. Nat Genet 2002; 32:585-93; PMID:12415271; http://dx.doi.org/10.1038/ng1023.
79. Simonatto M, Giordani L, Marullo F, Minetti GC, Puri PL, Latella L. Coordination of cell cycle, DNA repair and muscle gene expression in myoblasts exposed to genotoxic stress. Cell Cycle 2011; 10:2355-63; PMID:21685725; http://dx.doi.org/10.4161/cc.10.14.15948.
80. Bar-Sagi D, Feramisco JR. Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 1985; 42:841-8; PMID:2996779; http://dx.doi.org/10.1016/0092-8674(85)90280-6.
81. Bagli DJ, D'Emilia JC, Summerhayes IC, Steele GD, Barlozzari T. c-Ha-ras-I oncogene-induced differentiation and natural killer cell resistance in a human colorectal carcinoma cell line. Cancer Res 1990; 50:2518-23; PMID:2180571.
82. Celano P, Berchtold CM, Mabry M, Carroll M, Sidransky D, Casero RA Jr., et al. Induction of markers of normal differentiation in human colon carcinoma cells by the v-rasH oncogene. Cell Growth Differ 1993; 4:341-7; PMID:8494794.
83. Feng Y, Bommer GT, Zhao J, Green M, Sands E, Zhai Y, et al. Mutant KRAS promotes hyperplasia and alters differentiation in the colon epithelium but does not expand the presumptive stem cell pool. Gastroenterology 2011; 141:1003-13, e1-10; PMID:21699772; http://dx.doi.org/10.1053/j.gastro.2011.05.007.
84. Boukamp P. Non-melanoma skin cancer: what drives tumor development and progression? Carcinogenesis 2005; 26:1657-67; PMID:15905207; http://dx.doi.org/10.1093/carcin/bgi123.