Loss of Grainy head-like 1 is associated with disruption of the epidermal barrier and squamous cell carcinoma of the skin

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Mlacki, Michal ^a   Darido, Charbel ^b   Jane, Stephen M ^b,c   Wilanowski, Tomasz ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b MONASH UNIVERSITY   (Australia)

^c ALFRED HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DESMOGLEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TRANSCRIPTION FACTOR GRHL1; UNCLASSIFIED DRUG; 7,12 DIMETHYLBENZ[A]ANTHRACENE; CARCINOGEN; GRHL1 PROTEIN, MOUSE; MESSENGER RNA; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL INFILTRATION; CHROMOSOME NUMBER; CHROMOSOME STRUCTURE; CONTROLLED STUDY; ENZYME REGULATION; EPIDERMIS; IMMUNOCOMPETENT CELL; KERATINOCYTE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPILLOMA; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SKIN CANCER; SQUAMOUS CELL CARCINOMA; ANIMAL; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CHEMICALLY INDUCED; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; KNOCKOUT MOUSE; MAST CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN TUMOR; TOXICITY; TUMOR CELL CULTURE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; EPIDERMIS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOENZYME TECHNIQUES; MAST CELLS; MICE; MICE, KNOCKOUT; PAPILLOMA; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SKIN NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 84895887786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089247     Document Type: Article

References (70)

1. Dusek RL, Attardi LD (2011) Desmosomes: new perpetrators in tumour suppression. Nature reviews Cancer 11: 317-323.
2. Getsios S, Simpson CL, Kojima S, Harmon R, Sheu LJ, et al. (2009) Desmoglein 1-dependent suppression of EGFR signaling promotes epidermal differentiation and morphogenesis. The Journal of cell biology 185: 1243-1258.
3. Cui T, Chen Y, Yang L, Knosel T, Huber O, et al. (2012) The p53 target gene desmocollin 3 acts as a novel tumor suppressor through inhibiting EGFR/ERK pathway in human lung cancer. Carcinogenesis 33: 2326-2333.
4. Yang L, Chen Y, Cui T, Knosel T, Zhang Q, et al. (2012) Desmoplakin acts as a tumor suppressor by inhibition of the Wnt/beta-catenin signaling pathway in human lung cancer. Carcinogenesis 33: 1863-1870.
5. Franzen CA, Todorovic V, Desai BV, Mirzoeva S, Yang XJ, et al. (2012) The desmosomal armadillo protein plakoglobin regulates prostate cancer cell adhesion and motility through vitronectin-dependent Src signaling. PLoS One 7: e42132.
6. Ting SB, Wilanowski T, Cerruti L, Zhao LL, Cunningham JM, et al. (2003) The identification and characterization of human Sister-of-Mammalian Grainyhead (SOM) expands the grainyhead-like family of developmental transcription factors. The Biochemical journal 370: 953-962. (Pubitemid 36399088)
7. Wilanowski T, Tuckfield A, Cerruti L, O'Connell S, Saint R, et al. (2002) A highly conserved novel family of mammalian developmental transcription factors related to Drosophila grainyhead. Mechanisms of development 114: 37-50. (Pubitemid 34462951)
8. Darido C, Georgy SR, Wilanowski T, Dworkin S, Auden A, et al. (2011) Targeting of the Tumor Suppressor GRHL3 by a miR-21-Dependent Proto- Oncogenic Network Results in PTEN Loss and Tumorigenesis. Cancer Cell 20: 635-648.
9. Wilanowski T, Caddy J, Ting SB, Hislop NR, Cerruti L, et al. (2008) Perturbed desmosomal cadherin expression in grainy head-like 1-null mice. The EMBO journal 27: 886-897. (Pubitemid 351417170)
10. Kitamura Y, Go S, Hatanaka K (1978) Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 52: 447-452. (Pubitemid 8395558)
11. Nibbs RJ, Gilchrist DS, King V, Ferra A, Forrow S, et al. (2007) The atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors. The Journal of clinical investigation 117: 1884-1892. (Pubitemid 47036322)
12. Segre JA (2006) Epidermal barrier formation and recovery in skin disorders. The Journal of clinical investigation 116: 1150-1158.
13. Demehri S, Liu Z, Lee J, Lin MH, Crosby SD, et al. (2008) Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS biology 6: e123.
14. Aberg KM, Man MQ, Gallo RL, Ganz T, Crumrine D, et al. (2008) Coregulation and interdependence of the mammalian epidermal permeability and antimicrobial barriers. The Journal of investigative dermatology 128: 917-925. (Pubitemid 351374295)
15. Bangert C, Brunner PM, Stingl G (2011) Immune functions of the skin. Clinics in dermatology 29: 360-376.
16. Demehri S, Turkoz A, Kopan R (2009) Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 16: 55-66.
17. Sundberg JP, Sundberg BA, Beamer WG (1997) Comparison of chemical carcinogen skin tumor induction efficacy in inbred, mutant, and hybrid strains of mice: morphologic variations of induced tumors and absence of a papillomavirus cocarcinogen. Molecular carcinogenesis 20: 19-32. (Pubitemid 27461535)
18. Balmain A, Pragnell IB (1983) Mouse skin carcinomas induced in vivo by chemical carcinogens have a transforming Harvey-ras oncogene. Nature 303: 72-74. (Pubitemid 13125077)
19. Rickman L, Simrak D, Stevens HP, Hunt DM, King IA, et al. (1999) N-terminal deletion in a desmosomal cadherin causes the autosomal dominant skin disease striate palmoplantar keratoderma. Hum Mol Genet 8: 971-976. (Pubitemid 29250884)
20. Hunt DM, Rickman L, Whittock NV, Eady RA, Simrak D, et al. (2001) Spectrum of dominant mutations in the desmosomal cadherin desmoglein 1, causing the skin disease striate palmoplantar keratoderma. Eur J Hum Genet 9: 197-203. (Pubitemid 32237053)
21. Kottke MD, Delva E, Kowalczyk AP (2006) The desmosome: cell science lessons from human diseases. J Cell Sci 119: 797-806.
22. Patel S, Kartasova T, Segre JA (2003) Mouse Sprr locus: a tandem array of coordinately regulated genes. Mammalian genome : official journal of the International Mammalian Genome Society 14: 140-148.
23. Mischke D, Korge BP, Marenholz I, Volz A, Ziegler A (1996) Genes encoding structural proteins of epidermal cornification and S100 calcium-binding proteins form a gene complex ("epidermal differentiation complex") on human chromosome 1q21. The Journal of investigative dermatology 106: 989-992.
24. Lukanidin E, Sleeman JP (2012) Building the niche: the role of the S100 proteins in metastatic growth. Seminars in cancer biology 22: 216-225.
25. Koch PJ, de Viragh PA, Scharer E, Bundman D, Longley MA, et al. (2000) Lessons from loricrin-deficient mice: compensatory mechanisms maintaining skin barrier function in the absence of a major cornified envelope protein. The Journal of cell biology 151: 389-400.
26. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, et al. (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes & development 13: 1382-1397. (Pubitemid 29270244)
27. Kemp CJ, Donehower LA, Bradley A, Balmain A (1993) Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 74: 813-822. (Pubitemid 23270601)
28. Hainaut P, Wiman KG (2009) 30 years and a long way into p53 research. Lancet Oncol 10: 913-919.
29. Greenhalgh DA, Wang XJ, Donehower LA, Roop DR (1996) 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 56: 4413-4423. (Pubitemid 26330449)
30. Bailleul B, Surani MA, White S, Barton SC, Brown K, et al. (1990) Skin hyperkeratosis and papilloma formation in transgenic mice expressing a ras oncogene from a suprabasal keratin promoter. Cell 62: 697-708.
31. Brown K, Strathdee D, Bryson S, Lambie W, Balmain A (1998) The malignant capacity of skin tumours induced by expression of a mutant H-ras transgene depends on the cell type targeted. Current biology : CB 8: 516-524.
32. Frame S, Balmain A (2000) Integration of positive and negative growth signals during ras pathway activation in vivo. Current opinion in genetics & development 10: 106-113. (Pubitemid 30113713)
33. Blanpain C (2013) Tracing the cellular origin of cancer. Nat Cell Biol 15: 126-134.
34. Auden A, Caddy J, Wilanowski T, Ting SB, Cunningham JM, et al. (2006) Spatial and temporal expression of the Grainyhead-like transcription factor family during murine development. Gene Expr Patterns 6: 964-970. (Pubitemid 44309447)
35. Boglev Y, Wilanowski T, Caddy J, Parekh V, Auden A, et al. (2011) The unique and cooperative roles of the Grainy head-like transcription factors in epidermal development reflect unexpected target gene specificity. Developmental biology 349: 512-522.
36. Augustin I, Gross J, Baumann D, Korn C, Kerr G, et al. (2013) Loss of epidermal Evi/Wls results in a phenotype resembling psoriasiform dermatitis. J Exp Med 210: 1761-1777.
37. Beaudry VG, Jiang D, Dusek RL, Park EJ, Knezevich S, et al. (2010) Loss of the p53/p63 regulated desmosomal protein Perp promotes tumorigenesis. PLoS Genet 6: e1001168.
38. He D, Li H, Yusuf N, Elmets CA, Athar M, et al. (2012) IL-17 mediated inflammation promotes tumor growth and progression in the skin. PLoS One 7: e32126.
39. Kawanishi H, Matsui Y, Ito M, Watanabe J, Takahashi T, et al. (2008) Secreted CXCL1 is a potential mediator and marker of the tumor invasion of bladder cancer. Clinical cancer research : an official journal of the American Association for Cancer Research 14: 2579-2587.
40. Bolitho C, Hahn MA, Baxter RC, Marsh DJ (2010) The chemokine CXCL1 induces proliferation in epithelial ovarian cancer cells by transactivation of the epidermal growth factor receptor. Endocrine-related cancer 17: 929-940.
41. Walser TC, Ma X, Kundu N, Dorsey R, Goloubeva O, et al. (2007) Immunemediated modulation of breast cancer growth and metastasis by the chemokine Mig (CXCL9) in a murine model. Journal of immunotherapy 30: 490-498. (Pubitemid 46988082)
42. Ohtani H, Jin Z, Takegawa S, Nakayama T, Yoshie O (2009) Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3+ T cells in lymphocyte-rich gastric carcinoma. The Journal of pathology 217: 21-31.
43. Oh ST, Schramme A, Tilgen W, Gutwein P, Reichrath J (2009) Overexpression of CXCL16 in lesional psoriatic skin. Dermato-endocrinology 1: 114-118.
44. Darash-Yahana M, Gillespie JW, Hewitt SM, Chen YY, Maeda S, et al. (2009) The chemokine CXCL16 and its receptor, CXCR6, as markers and promoters of inflammation-associated cancers. PLoS One 4: e6695.
45. Deng L, Chen N, Li Y, Zheng H, Lei Q (2010) CXCR6/CXCL16 functions as a regulator in metastasis and progression of cancer. Biochimica et biophysica acta 1806: 42-49.
46. Aldhous MC, Noble CL, Satsangi J (2009) Dysregulation of human beta-defensin-2 protein in inflammatory bowel disease. PLoS One 4: e6285.
47. Hollox EJ, Huffmeier U, Zeeuwen PL, Palla R, Lascorz J, et al. (2008) Psoriasis is associated with increased beta-defensin genomic copy number. Nature genetics 40: 23-25.
48. Hardman MJ, Waite A, Zeef L, Burow M, Nakayama T, et al. (2005) Macrophage migration inhibitory factor: a central regulator of wound healing. The American journal of pathology 167: 1561-1574. (Pubitemid 41713310)
49. Rohrl J, Huber B, Koehl GE, Geissler EK, Hehlgans T (2012) Mouse beta-defensin 14 (Defb14) promotes tumor growth by inducing angiogenesis in a CCR6-dependent manner. Journal of immunology 188: 4931-4939.
50. Christophi GP, Isackson PJ, Blaber S, Blaber M, Rodriguez M, et al. (2004) Distinct promoters regulate tissue-specific and differential expression of kallikrein 6 in CNS demyelinating disease. Journal of neurochemistry 91: 1439-1449. (Pubitemid 39658570)
51. Iwata A, Maruyama M, Akagi T, Hashikawa T, Kanazawa I, et al. (2003) Alpha-synuclein degradation by serine protease neurosin: implication for pathogenesis of synucleinopathies. Human molecular genetics 12: 2625-2635. (Pubitemid 37304685)
52. Breitenbach U, Tuckermann JP, Gebhardt C, Richter KH, Furstenberger G, et al. (2001) Keratinocyte-specific onset of serine protease BSSP expression in experimental carcinogenesis. The Journal of investigative dermatology 117: 634-640. (Pubitemid 32955591)
53. Borgono CA, Diamandis EP (2004) The emerging roles of human tissue kallikreins in cancer. Nature reviews Cancer 4: 876-890. (Pubitemid 39472954)
54. Yasuda S, Morokawa N, Wong GW, Rossi A, Madhusudhan MS, et al. (2005) Urokinase-type plasminogen activator is a preferred substrate of the human epithelium serine protease tryptase epsilon/PRSS22. Blood 105: 3893-3901. (Pubitemid 40656134)
55. Sallenave JM (2000) The role of secretory leukocyte proteinase inhibitor and elafin (elastase-specific inhibitor/skin-derived antileukoprotease) as alarm antiproteinases in inflammatory lung disease. Respiratory research 1: 87-92.
56. Meyer-Hoffert U (2009) Reddish, scaly, and itchy: how proteases and their inhibitors contribute to inflammatory skin diseases. Archivum immunologiae et therapiae experimentalis 57: 345-354.
57. Devoogdt N, Revets H, Ghassabeh GH, De Baetselier P (2004) Secretory leukocyte protease inhibitor in cancer development. Annals of the New York Academy of Sciences 1028: 380-389. (Pubitemid 40361839)
58. Jarvinen M, Rinne A, Hopsu-Havu VK (1987) Human cystatins in normal and diseased tissues-a review. Acta histochemica 82: 5-18. (Pubitemid 18081108)
59. Kos J, Krasovec M, Cimerman N, Nielsen HJ, Christensen IJ, et al. (2000) Cysteine proteinase inhibitors stefin A, stefin B, and cystatin C in sera from patients with colorectal cancer: relation to prognosis. Clinical cancer research : an official journal of the American Association for Cancer Research 6: 505-511.
60. Dang H, Trempus C, Malarkey DE, Wei SJ, Humble M, et al. (2006) Identification of genes and gene ontology processes critical to skin papilloma development in Tg.AC transgenic mice. Molecular carcinogenesis 45: 126-140. (Pubitemid 43202586)
61. Hoffjan S, Stemmler S (2007) On the role of the epidermal differentiation complex in ichthyosis vulgaris, atopic dermatitis and psoriasis. The British journal of dermatology 157: 441-449. (Pubitemid 47256114)
62. Booth DR, Booth SE, Gillmore JD, Hawkins PN, Pepys MB (1998) SAA1 alleles as risk factors in reactive systemic AA amyloidosis. Amyloid : the international journal of experimental and clinical investigation : the official journal of the International Society of Amyloidosis 5: 262-265.
63. Moshkovskii SA, Vlasova MA, Pyatnitskiy MA, Tikhonova OV, Safarova MR, et al. (2007) Acute phase serum amyloid A in ovarian cancer as an important component of proteome diagnostic profiling. Proteomics Clinical applications 1: 107-117.
64. Milan E, Lazzari C, Anand S, Floriani I, Torri V, et al. (2012) SAA1 is overexpressed in plasma of non small cell lung cancer patients with poor outcome after treatment with epidermal growth factor receptor tyrosine-kinase inhibitors. Journal of proteomics 76 Spec No.: 91-101.
65. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, et al. (2008) The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nature cell biology 10: 1349-1355.
66. Hayes KR, Vollrath AL, Zastrow GM, McMillan BJ, Craven M, et al. (2005) EDGE: a centralized resource for the comparison, analysis, and distribution of toxicogenomic information. Molecular pharmacology 67: 1360-1368. (Pubitemid 40410437)
67. Pappas P, Sotiropoulou M, Karamanakos P, Kostoula A, Levidiotou S, et al. (2003) Acute-phase response to benzo[a]pyrene and induction of rat ALDH3A1. Chemico-biological interactions 143-144: 55-62. (Pubitemid 36258339)
68. Kushner I (1988) The acute phase response: an overview. Methods in enzymology 163: 373-383.
69. Karashima S, Kataoka H, Itoh H, Maruyama R, Koono M (1990) Prognostic significance of alpha-1-antitrypsin in early stage of colorectal carcinomas. International journal of cancer Journal international du cancer 45: 244-250.
70. Arlt A, Schafer H (2011) Role of the immediate early response 3 (IER3) gene in cellular stress response, inflammation and tumorigenesis. European journal of cell biology 90: 545-552.