C-MYC-Induced Sebaceous Gland Differentiation Is Controlled by an Androgen Receptor/p53 Axis

Cell Reports

Volumn 3, Issue 2, 2013, Pages 427-441

  Cottle, Denny L ^a   Kretzschmar, Kai ^a,e   Schweiger, Pawel J ^d   Quist, Sven R ^b,d   Gollnick, Harald P ^b   Natsuga, Ken ^c,d   Aoyagi, Satoru ^c   Watt, Fiona M ^a,d,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c HOKKAIDO UNIVERSITY   (Japan)

^d CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; MYC PROTEIN; PROTEIN P53; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEBACEOUS GLAND; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, ANDROGEN; RNA, MESSENGER; SEBACEOUS GLAND NEOPLASMS; SEBACEOUS GLANDS; SIGNAL TRANSDUCTION; TAMOXIFEN; TESTOSTERONE; TUMOR SUPPRESSOR PROTEIN P53;

MURINAE; MUS;

EID: 84874236131     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.01.013     Document Type: Article

References (65)

1. Akamatsu H., Zouboulis C.C., Orfanos C.E. Control of human sebocyte proliferation in vitro by testosterone and 5-alpha-dihydrotestosterone is dependent on the localization of the sebaceous glands. J. Invest. Dermatol. 1992, 99:509-511.
2. Alimirah F., Panchanathan R., Chen J., Zhang X., Ho S.M., Choubey D. Expression of androgen receptor is negatively regulated by p53. Neoplasia 2007, 9:1152-1159.
3. Arnold I., Watt F.M. c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr. Biol. 2001, 11:558-568.
4. Azzi L., El-Alfy M., Labrie F. Gender differences and effects of sex steroids and dehydroepiandrosterone on androgen and oestrogen alpha receptors in mouse sebaceous glands. Br. J. Dermatol. 2006, 154:21-27.
5. Bayer-Garner I.B., Givens V., Smoller B. Immunohistochemical staining for androgen receptors: a sensitive marker of sebaceous differentiation. Am. J. Dermatopathol. 1999, 21:426-431.
6. Bernard D., Pourtier-Manzanedo A., Gil J., Beach D.H. Myc confers androgen-independent prostate cancer cell growth. J. Clin. Invest. 2003, 112:1724-1731.
7. Berta M.A., Baker C.M., Cottle D.L., Watt F.M. Dose and context dependent effects of Myc on epidermal stem cell proliferation and differentiation. EMBO Mol. Med. 2010, 2:16-25.
8. Buitrago W., Joseph A.K. Sebaceous carcinoma: the great masquerader: emgerging concepts in diagnosis and treatment. Dermatol. Ther. 2008, 21:459-466.
9. Ceballos E., Delgado M.D., Gutierrez P., Richard C., Müller D., Eilers M., Ehinger M., Gullberg U., León J. c-Myc antagonizes the effect of p53 on apoptosis and p21WAF1 transactivation in K562 leukemia cells. Oncogene 2000, 19:2194-2204.
10. Chang D.H., Cattoretti G., Calame K.L. The dynamic expression pattern of B lymphocyte induced maturation protein-1 (Blimp-1) during mouse embryonic development. Mech. Dev. 2002, 117:305-309.
11. Chen W., Tsai S.J., Liao C.Y., Tsai R.Y., Chen Y.J., Pan B.J., Hung C.L., Zouboulis C.C. Higher levels of steroidogenic acute regulatory protein and type I 3beta-hydroxysteroid dehydrogenase in the scalp of men with androgenetic alopecia. J. Invest. Dermatol. 2006, 126:2332-2335.
12. Chen W., Tsai S.J., Sheu H.M., Tsai J.C., Zouboulis C.C. Testosterone synthesized in cultured human SZ95 sebocytes derives mainly from dehydroepiandrosterone. Exp. Dermatol. 2010, 19:470-472.
13. Cui C.Y., Durmowicz M., Ottolenghi C., Hashimoto T., Griggs B., Srivastava A.K., Schlessinger D. Inducible mEDA-A1 transgene mediates sebaceous gland hyperplasia and differential formation of two types of mouse hair follicles. Hum. Mol. Genet. 2003, 12:2931-2940.
14. Deplewski D., Rosenfield R.L. Growth hormone and insulin-like growth factors have different effects on sebaceous cell growth and differentiation. Endocrinology 1999, 140:4089-4094.
15. Driskell I., Oda H., Blanco S., Nascimento E., Humphreys P., Frye M. The histone methyltransferase Setd8 acts in concert with c-Myc and is required to maintain skin. EMBO J. 2011, 31:616-629.
16. Gaspar M.L., Meo T., Bourgarel P., Guenet J.L., Tosi M. A single base deletion in the Tfm androgen receptor gene creates a short-lived messenger RNA that directs internal translation initiation. Proc. Natl. Acad. Sci. USA 1991, 88:8606-8610.
17. Greenhalgh D.A., Wang X.J., Donehower L.A., Roop D.R. Paradoxical tumor inhibitory effect of p53 loss in transgenic mice expressing epidermal-targeted v-rasHa, v-fos, or human transforming growth factor alpha. Cancer Res. 1996, 56:4413-4423.
18. Hallenborg P., Feddersen S., Madsen L., Kristiansen K. The tumor suppressors pRB and p53 as regulators of adipocyte differentiation and function. Expert Opin. Ther. Targets 2009, 13:235-246.
19. Hasebe T., Mukai K., Yamaguchi N., Ishihara K., Kaneko A., Takasaki Y., Shimosato Y. Prognostic value of immunohistochemical staining for proliferating cell nuclear antigen, p53, and c-erbB-2 in sebaceous gland carcinoma and sweat gland carcinoma: comparison with histopathological parameter. Mod. Pathol. 1994, 7:37-43.
20. Hayashi N., Furihata M., Ohtsuki Y., Ueno H. Search for accumulation of p53 protein and detection of human papillomavirus genomes in sebaceous gland carcinoma of the eyelid. Virchows Arch. 1994, 424:503-509.
21. Hayward W.S., Neel B.G., Astrin S.M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 1981, 290:475-480.
22. Honeycutt K.A., Roop D.R. c-Myc and epidermal stem cell fate determination. J. Dermatol. 2004, 31:368-375.
23. Hong S., Pusapati R.V., Powers J.T., Johnson D.G. Oncogenes and the DNA damage response: Myc and E2F1 engage the ATM signaling pathway to activate p53 and induce apoptosis. Cell Cycle 2006, 5:801-803.
24. Horsley V., O'Carroll D., Tooze R., Ohinata Y., Saitou M., Obukhanych T., Nussenzweig M., Tarakhovsky A., Fuchs E. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 2006, 126:597-609.
25. Imperato-McGinley J., Gautier T., Cai L.Q., Yee B., Epstein J., Pochi P. The androgen control of sebum production. Studies of subjects with dihydrotestosterone deficiency and complete androgen insensitivity. J. Clin. Endocrinol. Metab. 1993, 76:524-528.
26. Izumi M., Mukai K., Nagai T., Matsubayashi J., Iwaya K., Chiu C.S., Goto H. Sebaceous carcinoma of the eyelids: thirty cases from Japan. Pathol. Int. 2008, 58:483-488.
27. Jensen K.B., Collins C.A., Nascimento E., Tan D.W., Frye M., Itami S., Watt F.M. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 2009, 4:427-439.
28. Ju Q., Fimmel S., Hinz N., Stahlmann R., Xia L., Zouboulis C.C. 2,3,7,8-Tetrachlorodibenzo-p-dioxin alters sebaceous gland cell differentiation in vitro. Exp. Dermatol. 2011, 20:320-325.
29. Kiyosaki K., Nakada C., Hijiya N., Tsukamoto Y., Matsuura K., Nakatsuka K., Daa T., Yokoyama S., Imaizumi M., Moriyama M. Analysis of p53 mutations and the expression of p53 and p21WAF1/CIP1 protein in 15 cases of sebaceous carcinoma of the eyelid. Invest. Ophthalmol. Vis. Sci. 2010, 51:7-11.
30. Kulikov R., Letienne J., Kaur M., Grossman S.R., Arts J., Blattner C. Mdm2 facilitates the association of p53 with the proteasome. Proc. Natl. Acad. Sci. USA 2010, 107:10038-10043.
31. Latham J.A., Redfern C.P., Thody A.J., De Kretser T.A. Immunohistochemical markers of human sebaceous gland differentiation. Cytochem. 1989, 37:729-734.
32. Laurent S.J., Mednieks M.I., Rosenfield R.L. Growth of sebaceous cells in monolayer culture. In Vitro Cell. Dev. Biol. 1992, 28A:83-89.
33. Lin H.K., Wang L., Hu Y.C., Altuwaijri S., Chang C. Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase. EMBO J. 2002, 21:4037-4048.
34. Lo Celso C., Berta M.A., Braun K.M., Frye M., Lyle S., Zouboulis C.C., Watt F.M. Characterization of bipotential epidermal progenitors derived from human sebaceous gland: contrasting roles of c-Myc and beta-catenin. Stem Cells 2008, 26:1241-1252.
35. Magnúsdóttir E., Kalachikov S., Mizukoshi K., Savitsky D., Ishida-Yamamoto A., Panteleyev A.A., Calame K. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl. Acad. Sci. USA 2007, 104:14988-14993.
36. Markova M.S., Zeskand J., McEntee B., Rothstein J., Jimenez S.A., Siracusa L.D. A role for the androgen receptor in collagen content of the skin. J. Invest. Dermatol. 2004, 123:1052-1056.
37. McCulley J.P., Shine W.E. The lipid layer of tears: dependent on meibomian gland function. Exp. Eye Res. 2004, 78:361-365.
38. Montagna W., Ellis R.A., Silver A.F. Advances in Biology of Skin. The Sebaceous Glands 1963, Volume 4. Oxford, Pergamon.
39. Murphy D.J., Junttila M.R., Pouyet L., Karnezis A., Shchors K., Bui D.A., Brown-Swigart L., Johnson L., Evan G.I. Distinct thresholds govern Myc's biological output in vivo. Cancer Cell 2008, 14:447-457.
40. Nadiminty N., Tummala R., Lou W., Zhu Y., Zhang J., Chen X., eVere White R.W., Kung H.J., Evans C.P., Gao A.C. MicroRNA let-7c suppresses androgen receptor expression and activity via regulation of Myc expression in prostate cancer cells. J. Biol. Chem. 2012, 287:1527-1537.
41. Nantermet P.V., Xu J., Yu Y., Hodor P., Holder D., Adamski S., Gentile M.A., Kimmel D.B., Harada S., Gerhold D., et al. Identification of genetic pathways activated by the androgen receptor during the induction of proliferation in the ventral prostate gland. J. Biol. Chem. 2004, 279:1310-1322.
42. Nascimento E.M., Cox C.L., MacArthur S., Hussain S., Trotter M., Blanco S., Suraj M., Nichols J., Kübler B., Benitah S.A., et al. The opposing transcriptional functions of Sin3a and c-Myc are required to maintain tissue homeostasis. Nat. Cell Biol. 2011, 13:1395-1405.
43. Nesslinger N.J., Shi X.B., deVere White R.W. Androgen-independent growth of LNCaP prostate cancer cells is mediated by gain-of-function mutant p53. Cancer Res. 2003, 63:2228-2233.
44. Petersson M., Brylka H., Kraus A., John S., Rappl G., Schettina P., Niemann C. TCF/Lef1 activity controls establishment of diverse stem and progenitor cell compartments in mouse epidermis. EMBO J. 2011, 30:3004-3018.
45. Pusapati R.V., Rounbehler R.J., Hong S., Powers J.T., Yan M., Kiguchi K., McArthur M.J., Wong P.K., Johnson D.G. ATM promotes apoptosis and suppresses tumorigenesis in response to Myc. Proc. Natl. Acad. Sci. USA 2006, 103:1446-1451.
46. Rahl P.B., Lin C.Y., Seila A.C., Flynn R.A., McCuine S., Burge C.B., Sharp P.A., Young R.A. c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
47. Reichelt J., Breiden B., Sandhoff K., Magin T.M. Loss of keratin 10 is accompanied by increased sebocyte proliferation and differentiation. Eur. J. Cell Biol. 2004, 83:747-759.
48. Rokhlin O.W., Taghiyev A.F., Guseva N.V., Glover R.A., Chumakov P.M., Kravchenko J.E., Cohen M.B. Androgen regulates apoptosis induced by TNFR family ligands via multiple signaling pathways in LNCaP. Oncogene 2005, 24:6773-6784.
49. Rosenfield R.L. Relationship of sebaceous cell stage to growth in culture. J. Invest. Dermatol. 1989, 92:751-754.
50. Rosenfield R.L., Deplewski D., Kentsis A., Ciletti N. Mechanisms of androgen induction of sebocyte differentiation. Dermatology (Basel) 1998, 196:43-46.
51. Rosenfield R.L., Kentsis A., Deplewski D., Ciletti N. Rat preputial sebocyte differentiation involves peroxisome proliferator-activated receptors. J. Invest. Dermatol. 1999, 112:226-232.
52. Rudolf E., Rudolf K., Cervinka M. Camptothecin induces p53-dependent and -independent apoptogenic signaling in melanoma cells. Apoptosis 2011, 16:1165-1176.
53. Schirra F., Suzuki T., Richards S.M., Jensen R.V., Liu M., Lombardi M.J., Rowley P., Treister N.S., Sullivan D.A. Androgen control of gene expression in the mouse meibomian gland. Invest. Ophthalmol. Vis. Sci. 2005, 46:3666-3675.
54. Schirra F., Richards S.M., Liu M., Suzuki T., Yamagami H., Sullivan D.A. Androgen regulation of lipogenic pathways in the mouse meibomian gland. Exp. Eye Res. 2006, 83:291-296.
55. Schneider M.R., Paus R. Sebocytes, multifaceted epithelial cells: lipid production and holocrine secretion. Int. J. Biochem. Cell Biol. 2010, 42:181-185.
56. Sellheyer K., Krahl D. Blimp-1: a marker of terminal differentiation but not of sebocytic progenitor cells. J. Cutan. Pathol. 2010, 37:362-370.
57. Shah N.M., Pisapia D.J., Maniatis S., Mendelsohn M.M., Nemes A., Axel R. Visualizing sexual dimorphism in the brain. Neuron 2004, 43:313-319.
58. Sheiness D.K., Hughes S.H., Varmus H.E., Stubblefield E., Bishop J.M. The vertebrate homolog of the putative transforming gene of avian myelocytomatosis virus: characteristics of the DNA locus and its RNA transcript. Virology 1980, 105:415-424.
59. Shenk J.L., Fisher C.J., Chen S.Y., Zhou X.F., Tillman K., Shemshedini L. p53 represses androgen-induced transactivation of prostate-specific antigen by disrupting hAR amino- to carboxyl-terminal interaction. J. Biol. Chem. 2001, 276:38472-38479.
60. Snippert H.J., Haegebarth A., Kasper M., Jaks V., van Es J.H., Barker N., van de Wetering M., van den Born M., Begthel H., Vries R.G., et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010, 327:1385-1389.
61. Sundberg J.P., Boggess D., Sundberg B.A., Eilertsen K., Parimoo S., Filippi M., Stenn K. Asebia-2J (Scd1(ab2J)): a new allele and a model for scarring alopecia. Am. J. Pathol. 2000, 156:2067-2075.
62. Watt F.M., Frye M., Benitah S.A. MYC in mammalian epidermis: how can an oncogene stimulate differentiation?. Nat. Rev. Cancer 2008, 8:234-242.
63. Zouboulis C.C. [The sebaceous gland]. Hautarzt 2010, 61:467-468. 4704, 476-477.
64. Zouboulis C.C., Xia L., Akamatsu H., Seltmann H., Fritsch M., Hornemann S., Rühl R., Chen W., Nau H., Orfanos C.E. The human sebocyte culture model provides new insights into development and management of seborrhoea and acne. Dermatology (Basel) 1998, 196:21-31.
65. Zouboulis C.C., Seltmann H., Neitzel H., Orfanos C.E. Establishment and characterization of an immortalized human sebaceous gland cell line (SZ95). J. Invest. Dermatol. 1999, 113:1011-1020.