Selective Ablation of Ctip2/Bcl11b in Epidermal Keratinocytes Triggers Atopic Dermatitis-Like Skin Inflammatory Responses in Adult Mice

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Wang, Zhixing ^a   Zhang, Ling juan ^a   Guha, Gunjan ^a   Li, Shan ^a   Kyrylkova, Kateryna ^a   Kioussi, Chrissa ^a   Leid, Mark ^a   Ganguli Indra, Gitali ^a   Indra, Arup K ^a,b  

^a OREGON STATE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR INTERACTING PROTEIN 2; HELPER FACTOR; THYMIC STROMAL LYMPHOPOIETIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ALOPECIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOPIC DERMATITIS; CELL ASSAY; CELL INFILTRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CUTANEOUS PARAMETERS; DERMATITIS; EOSINOPHIL; EPIDERMIS CELL; GENE DELETION; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOCHEMISTRY; IMMUNOCOMPETENT CELL; KERATINOCYTE; KNOCKOUT MOUSE; MAST CELL; MOUSE; NONHUMAN; PROTEIN ABLATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; PRURITUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; SKIN SCALING; SKIN WATER LOSS; T LYMPHOCYTE; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; DERMATITIS, ATOPIC; EPIDERMIS; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; KERATINOCYTES; MICE; PERMEABILITY; REPRESSOR PROTEINS; TH2 CELLS; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 84871430284     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051262     Document Type: Article

References (63)

1. Fuchs E, Raghavan S, (2002) Getting under the skin of epidermal morphogenesis. Nat Rev Genet 3: 199-209.
2. Proksch E, Brandner JM, Jensen JM, (2008) The skin: an indispensable barrier. Exp Dermatol 17 (12):: 1063-1072 Available: http://www.ncbi.nlm.nih.gov/pubmed/19043850. Accessed 2012 Nov 23.
3. Tokura Y, (2010) Extrinsic and intrinsic types of atopic dermatitis. Journal of Dermatological Science 58: 1-7 doi:10.1016/j.jdermsci.2010.02.008.
4. Leung DY, Bieber T, (2003) Atopic dermatitis. The Lancet 361: 151-160 doi:10.1016/S0140-6736(03)12193-9.
5. Scharschmidt TC, Segre JA, (2008) Modeling atopic dermatitis with increasingly complex mouse models. J Invest Dermatol 128: 1061-1064 doi:10.1038/sj.jid.5701201.
6. Cork MJ, Danby SG, Vasilopoulos Y, Hadgraft J, Lane ME, et al. (2009) Epidermal Barrier Dysfunction in Atopic Dermatitis. Journal of Investigative Dermatology 129: 1892-1908 doi:10.1038/jid.2009.133.
7. B. Brandt E, Sivaprasad U, (2011) Th2 Cytokines and Atopic Dermatitis. Journal of Clinical & Cellular Immunology 02 Available:http://www.omicsonline.org/2155-9899/2155-9899-2-110.digital/2155-9899-2-110.html. Accessed 2012 Mar 9.
8. Biedermann T, Röcken M, Carballido JM, (2004) TH1 and TH2 lymphocyte development and regulation of TH cell-mediated immune responses of the skin. J Investig Dermatol Symp Proc 9: 5-14 doi:10.1111/j.1087-0024.2004.00829.x.
9. Comeau MR, Ziegler SF, (2010) The influence of TSLP on the allergic response. Mucosal Immunol 3: 138-147 doi:10.1038/mi.2009.134.
10. Ziegler SF, (2010) The role of thymic stromal lymphopoietin (TSLP) in allergic disorders. Current Opinion in Immunology 22: 795-799 doi:10.1016/j.coi.2010.10.020.
11. Kashyap M, Rochman Y, Spolski R, Samsel L, Leonard WJ, (2011) Thymic stromal lymphopoietin is produced by dendritic cells. J Immunol 187: 1207-1211 doi:10.4049/jimmunol.1100355.
12. Demehri S, Liu Z, Lee J, Lin M-H, 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 doi:10.1371/journal.pbio.0060123.
13. Li M, (2005) Retinoid X receptor ablation in adult mouse keratinocytes generates an atopic dermatitis triggered by thymic stromal lymphopoietin. Proceedings of the National Academy of Sciences 102: 14795-14800 doi:10.1073/pnas.0507385102.
14. Li M, (2006) Topical vitamin D3 and low-calcemic analogs induce thymic stromal lymphopoietin in mouse keratinocytes and trigger an atopic dermatitis. Proceedings of the National Academy of Sciences 103: 11736-11741 doi:10.1073/pnas.0604575103.
15. Avram D, Fields A, Pretty On Top K, Nevrivy DJ, Ishmael JE, et al. (2000) Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J Biol Chem 275: 10315-10322.
16. Topark-Ngarm A, Golonzhka O, Peterson VJ, Barrett B, Martinez B, et al. (2006) CTIP2 associates with the NuRD complex on the promoter of p57KIP2, a newly identified CTIP2 target gene. J Biol Chem 281: 32272-32283.
17. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, et al. (2005) Neuronal Subtype-Specific Genes that Control Corticospinal Motor Neuron Development In Vivo. Neuron 45: 207-221 doi:10.1016/j.neuron.2004.12.036.
18. Kastner P, Chan S, Vogel WK, Zhang L-J, Topark-Ngarm A, et al. (2010) Bcl11b represses a mature T-cell gene expression program in immature CD4(+)CD8(+) thymocytes. Eur J Immunol 40: 2143-2154 doi:10.1002/eji.200940258.
19. Cismasiu VB, Adamo K, Gecewicz J, Duque J, Lin Q, et al. (2005) BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter. Oncogene 24: 6753-6764 doi:10.1038/sj.onc.1208904.
20. Senawong T, Peterson VJ, Avram D, Shepherd DM, Frye RA, et al. (2003) Involvement of the histone deacetylase SIRT1 in chicken ovalbumin upstream promoter transcription factor (COUP-TF)-interacting protein 2-mediated transcriptional repression. J Biol Chem 278: 43041-43050 doi:10.1074/jbc.M307477200.
21. Kastner P, Chan S, Vogel WK, Zhang L-J, Topark-Ngarm A, et al. (2010) Bcl11b represses a mature T-cell gene expression program in immature CD4(+)CD8(+) thymocytes. Eur J Immunol 40: 2143-2154 doi:10.1002/eji.200940258.
22. Zhang L-J, Vogel WK, Liu X, Topark-Ngarm A, Arbogast BL, et al. (2012) Coordinated Regulation of Transcription Factor Bcl11b Activity in Thymocytes by the Mitogen-activated Protein Kinase (MAPK) Pathways and Protein Sumoylation. J Biol Chem 287: 26971-26988 doi:10.1074/jbc.M112.344176.
23. Golonzhka O, Leid M, Indra G, Indra AK, (2007) Expression of COUP-TF-interacting protein 2 (CTIP2) in mouse skin during development and in adulthood. Gene Expr Patterns 7: 754-760.
24. Ganguli-Indra G, Liang X, Hyter S, Leid M, Hanifin J, et al. (2009) Expression of COUP-TF-interacting protein 2 (CTIP2) in human atopic dermatitis and allergic contact dermatitis skin. Experimental Dermatology 18: 994-996 doi:10.1111/j.1600-0625.2009.00876.x.
25. Golonzhka O, Liang X, Messaddeq N, Bornert J-M, Campbell AL, et al. (2008) Dual Role of COUP-TF-Interacting Protein 2 in Epidermal Homeostasis and Permeability Barrier Formation. J Investig Dermatol 129: 1459-1470 doi:10.1038/jid.2008.392.
26. Zhang L-J, Bhattacharya S, Leid M, Ganguli-Indra G, Indra AK, (2012) Ctip2 is a dynamic regulator of epidermal proliferation and differentiation by integrating EGFR and Notch signaling. J Cell Sci doi:10.1242/jcs.108969.
27. Dassule HR, Lewis P, Bei M, Maas R, McMahon AP, (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127: 4775-4785.
28. Indra AK, Warot X, Brocard J, Bornert JM, Xiao JH, et al. (1999) Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 27: 4324-4327.
29. Grewe M, Bruijnzeel-Koomen CA, Schöpf E, Thepen T, Langeveld-Wildschut AG, et al. (1998) A role for Th1 and Th2 cells in the immunopathogenesis of atopic dermatitis. Immunol Today 19: 359-361.
30. Ziegler SF, Artis D, (2010) Sensing the outside world: TSLP regulates barrier immunity. Nature Immunology 11: 289-293 doi:10.1038/ni.1852.
31. Liu Y-J, (2006) Thymic stromal lymphopoietin: master switch for allergic inflammation. J Exp Med 203: 269-273 doi:10.1084/jem.20051745.
32. Dumortier A, Durham A-D, Di Piazza M, Vauclair S, Koch U, et al. (2010) Atopic Dermatitis-Like Disease and Associated Lethal Myeloproliferative Disorder Arise from Loss of Notch Signaling in the Murine Skin. PLoS ONE 5: e9258 doi:10.1371/journal.pone.0009258.
33. Boguniewicz M, Leung DYM, (2011) Atopic dermatitis: a disease of altered skin barrier and immune dysregulation. Immunol Rev 242: 233-246 doi:10.1111/j.1600-065X.2011.01027.x.
34. Dubrac S, Schmuth M, Ebner S, (2010) Atopic dermatitis: the role of Langerhans cells in disease pathogenesis. Immunology and Cell Biology 88: 400-409 doi:10.1038/icb.2010.33.
35. Novak N, Leung DY, (2011) Advances in atopic dermatitis. Current Opinion in Immunology 23: 778-783 doi:10.1016/j.coi.2011.09.007.
36. Spergel J, (2003) Atopic dermatitis and the atopic march. Journal of Allergy and Clinical Immunology 112: S118-S127 doi:10.1016/j.jaci.2003.09.033.
37. Proksch E, Feingold KR, Man MQ, Elias PM, (1991) Barrier function regulates epidermal DNA synthesis. Journal of Clinical Investigation 87: 1668-1673 doi:10.1172/JCI115183.
38. Segre JA, Bauer C, Fuchs E, (1999) Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat Genet 22: 356-360 doi:10.1038/11926.
39. Matsuki M, Yamashita F, Ishida-Yamamoto A, Yamada K, Kinoshita C, et al. (1998) Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1 (keratinocyte transglutaminase). Proc Natl Acad Sci USA 95: 1044-1049.
40. de Guzman Strong C, Wertz PW, Wang C, Yang F, Meltzer PS, et al. (2006) Lipid defect underlies selective skin barrier impairment of an epidermal-specific deletion of Gata-3. J Cell Biol 175: 661-670.
41. Barnes KC, (2010) An update on the genetics of atopic dermatitis: Scratching the surface in 2009. Journal of Allergy and Clinical Immunology 125: 16-29.e11 doi:10.1016/j.jaci.2009.11.008.
42. Palmer CNA, Irvine AD, Terron-Kwiatkowski A, Zhao Y, Liao H, et al. (2006) Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet 38: 441-446 doi:10.1038/ng1767.
43. Jakasa I, Koster ES, Calkoen F, McLean WHI, Campbell LE, et al. (2010) Skin Barrier Function in Healthy Subjects and Patients with Atopic Dermatitis in Relation to Filaggrin Loss-of-Function Mutations. Journal of Investigative Dermatology 131: 540-542 doi:10.1038/jid.2010.307.
44. Wong CK, Hu S, Cheung PFY, Lam CWK, (2010) Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: implications in allergic inflammation. Am J Respir Cell Mol Biol 43: 305-315 doi:10.1165/rcmb.2009-0168OC.
45. Reche PA, Soumelis V, Gorman DM, Clifford T, Liu Mr, et al. (2001) Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol 167: 336-343.
46. Quentmeier H, Drexler HG, Fleckenstein D, Zaborski M, Armstrong A, et al. (2001) Cloning of human thymic stromal lymphopoietin (TSLP) and signaling mechanisms leading to proliferation. Leukemia 15: 1286-1292.
47. Sebastian K, Borowski A, Kuepper M, Friedrich K, (2008) Signal transduction around thymic stromal lymphopoietin (TSLP) in atopic asthma. Cell Commun Signal 6: 5 doi:10.1186/1478-811X-6-5.
48. Tasian SK, Doral MY, Borowitz MJ, Wood BL, Chen I-M, et al. (2012) Aberrant STAT5 and PI3K/mTOR pathway signaling occurs in human CRLF2-rearranged B-precursor acute lymphoblastic leukemia. Blood 120: 833-842 doi:10.1182/blood-2011-12-389932.
49. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, et al. (2002) Human epithelial cells trigger dendritic cell-mediated allergic inflammation by producing TSLP. Nature Immunology Available:http://www.nature.com/doifinder/10.1038/ni805. Accessed 2012 Mar 27.
50. Yoo J, (2005) Spontaneous atopic dermatitis in mice expressing an inducible thymic stromal lymphopoietin transgene specifically in the skin. Journal of Experimental Medicine 202: 541-549 doi:10.1084/jem.20041503.
51. Liu Y (2009) Chapter 1 TSLP in Epithelial Cell and Dendritic Cell Cross Talk. Advances in Immunology. Elsevier, Vol. 101. pp. 1-25. Available:http://linkinghub.elsevier.com/retrieve/pii/S0065277608010018. Accessed 2012 Apr 30.
52. Lee H-C, Ziegler SF, (2007) Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NF B. Proceedings of the National Academy of Sciences 104: 914-919 doi:10.1073/pnas.0607305104.
53. Takai T, (2012) TSLP expression: cellular sources, triggers, and regulatory mechanisms. Allergol Int 61: 3-17 doi:10.2332/allergolint.11-RAI-0395.
54. Lee H-C, Headley MB, Iseki M, Ikuta K, Ziegler SF, (2008) Cutting edge: Inhibition of NF-kappaB-mediated TSLP expression by retinoid X receptor. J Immunol 181: 5189-5193.
55. Abbas AK, Murphy KM, Sher A, (1996) Functional diversity of helper T lymphocytes. Nature 383: 787-793 doi:10.1038/383787a0.
56. van Vliet E, Uhrberg M, Stein C, Gleichmann E, (1993) MHC control of IL-4-dependent enhancement of B cell Ia expression and Ig class switching in mice treated with mercuric chloride. Int Arch Allergy Immunol 101: 392-401.
57. Nakayama T, Hieshima K, Nagakubo D, Sato E, Nakayama M, et al. (2004) Selective induction of Th2-attracting chemokines CCL17 and CCL22 in human B cells by latent membrane protein 1 of Epstein-Barr virus. J Virol 78: 1665-1674.
58. Wang Z, Coleman DJ, Bajaj G, Liang X, Ganguli-Indra G, et al. (2011) RXRα ablation in epidermal keratinocytes enhances UVR-induced DNA damage, apoptosis, and proliferation of keratinocytes and melanocytes. J Invest Dermatol 131: 177-187 doi:10.1038/jid.2010.290.
59. Liang X, Bhattacharya S, Bajaj G, Guha G, Wang Z, et al. (2012) Delayed Cutaneous Wound Healing and Aberrant Expression of Hair Follicle Stem Cell Markers in Mice Selectively Lacking Ctip2 in Epidermis. PLoS ONE 7: e29999 doi:10.1371/journal.pone.0029999.
60. Indra AK, Mohan WS, Frontini M, Scheer E, Messaddeq N, et al. (2005) TAF10 is required for the establishment of skin barrier function in foetal, but not in adult mouse epidermis. Dev Biol 285: 28-37.
61. Indra AK, Dupe V, Bornert JM, Messaddeq N, Yaniv M, et al. (2005) Temporally controlled targeted somatic mutagenesis in embryonic surface ectoderm and fetal epidermal keratinocytes unveils two distinct developmental functions of BRG1 in limb morphogenesis and skin barrier formation. Development 132: 4533-4544.
62. Argmann CA, Auwerx J, (2006) Collection of blood and plasma from the mouse. Curr Protoc Mol Biol Chapter 29: Unit 29A.3 doi:10.1002/0471142727.mb29a03s75.
63. Hyter S, Bajaj G, Liang X, Barbacid M, Ganguli-Indra G, et al. (2010) Loss of nuclear receptor RXRα in epidermal keratinocytes promotes the formation of Cdk4-activated invasive melanomas. Pigment Cell Melanoma Res 23: 635-648 doi:10.1111/j.1755-148X.2010.00732.x.