Gsdma3 mutation causes bulge stem cell depletion and alopecia mediated by skin inflammation

American Journal of Pathology

Volumn 180, Issue 2, 2012, Pages 763-774

  Zhou, Yue ^a   Jiang, Xuan ^a   Gu, Pengyu ^a   Chen, Weiqian ^a   Zeng, Xuesi ^b   Gao, Xiang ^a,c  

^a NANJING UNIVERSITY   (China)

^b PEKING UNION MEDICAL COLLEGE   (China)

^c WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIBODY; CYCLOSPORIN A; CYTOKERATIN 15; ETHYLNITROSOUREA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN GASDERMIN A3; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALOPECIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DESTRUCTION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GENE MUTATION; HAIR FOLLICLE; HAIR LOSS; HISTOPATHOLOGY; HYPERKERATOSIS; MACROPHAGE; MALE; MOUSE; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN INFLAMMATION; STEM CELL;

ALOPECIA; ANIMALS; CYCLOSPORINE; DERMATITIS; DERMATOLOGIC AGENTS; GENOTYPE; HAIR FOLLICLE; MICE; MICE, INBRED STRAINS; POINT MUTATION; PROTEINS; STEM CELLS;

EID: 84862916670     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.10.034     Document Type: Article

References (55)

1. K.A. Moore, I.R. Lemischka Stem cells and their niches Science 311 2006 1880 1885
2. A.A. Panteleyev, C.A. Jahoda, A.M. Christiano Hair follicle predetermination J Cell Sci 114 2001 3419 3431
3. G. Cotsarelis, T.T. Sun, R.M. Lavker Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis Cell 61 1990 1329 1337
4. Y. Liu, S. Lyle, Z. Yang, G. Cotsarelis Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge J Invest Dermatol 121 2003 963 968
5. G. Taylor, M.S. Lehrer, P.J. Jensen, T.T. Sun, R.M. Lavker Involvement of follicular stem cells in forming not only the follicle but also the epidermis Cell 102 2000 451 461
6. H. Oshima, A. Rochat, C. Kedzia, K. Kobayashi, Y. Barrandon Morphogenesis and renewal of hair follicles from adult multipotent stem cells Cell 104 2001 233 245
7. M. Ito, Y. Liu, Z. Yang, J. Nguyen, F. Liang, R.J. Morris, G. Cotsarelis Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis Nat Med 11 2005 1351 1354
8. E.K. Ross, E. Tan, J. Shapiro Update on primary cicatricial alopecias J Am Acad Dermatol 53 2005 1 37 quiz 3840
9. N. Somani, W.F. Bergfeld Cicatricial alopecia: classification and histopathology Dermatol Ther 21 2008 221 237
10. M.J. Harries, R.D. Sinclair, S. Macdonald-Hull, D.A. Whiting, C.E. Griffiths, R. Paus Management of primary cicatricial alopecias: options for treatment Br J Dermatol 159 2008 1 22
11. M.J. Harries, R.M. Trueb, A. Tosti, A.G. Messenger, I. Chaudhry, D.A. Whiting, R. Sinclair, C.E. Griffiths, R. Paus How not to get scar(r) ed: pointers to the correct diagnosis in patients with suspected primary cicatricial alopecia Br J Dermatol 160 2009 482 501
12. K.J. McElwee Etiology of cicatricial alopecias: a basic science point of view Dermatol Ther 21 2008 212 220
13. M.J. Harries, K.C. Meyer, R. Paus Hair loss as a result of cutaneous autoimmunity: frontiers in the immunopathogenesis of primary cicatricial alopecia Autoimmun Rev 8 2009 478 483
14. K. Al-Refu, M. Goodfield Hair follicle stem cells in the pathogenesis of the scarring process in cutaneous lupus erythematosus Autoimmun Rev 8 2009 474 477
15. M.J. Harries, R. Paus The pathogenesis of primary cicatricial alopecias Am J Pathol 177 2010 2152 2162
16. O. Pozdnyakova, M. Mahalingam Involvement of the bulge region in primary scarring alopecia J Cutan Pathol 35 2008 922 925
17. N. Mobini, S. Tam, H. Kamino Possible role of the bulge region in the pathogenesis of inflammatory scarring alopecia: lichen planopilaris as the prototype J Cutan Pathol 32 2005 675 679
18. K. Al-Refu, S. Edward, E. Ingham, M. Goodfield Expression of hair follicle stem cells detected by cytokeratin 15 stain: implications for pathogenesis of the scarring process in cutaneous lupus erythematosus Br J Dermatol 160 2009 1188 1196
19. M. Tamura, S. Tanaka, T. Fujii, A. Aoki, H. Komiyama, K. Ezawa, K. Sumiyama, T. Sagai, T. Shiroishi Members of a novel gene family, Gsdm, are expressed exclusively in the epithelium of the skin and gastrointestinal tract in a highly tissue-specific manner Genomics 89 2007 618 629
20. N. Saeki, Y. Kuwahara, H. Sasaki, H. Satoh, T. Shiroishi Gasdermin (Gsdm) localizing to mouse chromosome 11 is predominantly expressed in upper gastrointestinal tract but significantly suppressed in human gastric cancer cells Mamm Genome 11 2000 718 724
21. N. Saeki, D.H. Kim, T. Usui, K. Aoyagi, T. Tatsuta, K. Aoki, K. Yanagihara, M. Tamura, H. Mizushima, H. Sakamoto, K. Ogawa, M. Ohki, T. Shiroishi, T. Yoshida, H. Sasaki GASDERMIN, suppressed frequently in gastric cancer, is a target of LMO1 in TGF-beta-dependent apoptotic signalling Oncogene 26 2007 6488 6498
22. F. Runkel, A. Marquardt, C. Stoeger, E. Kochmann, D. Simon, B. Kohnke, D. Korthaus, F. Wattler, H. Fuchs, M. Hrab de Angelis, G. Stumm, M. Nehls, S. Wattler, T. Franz, M. Augustin The dominant alopecia phenotypes Bareskin, Rex-denuded, and Reduced Coat 2 are caused by mutations in gasdermin 3 Genomics 84 2004 824 835
23. D.P. Lunny, E. Weed, P.M. Nolan, A. Marquardt, M. Augustin, R.M. Porter Mutations in gasdermin 3 cause aberrant differentiation of the hair follicle and sebaceous gland J Invest Dermatol 124 2005 615 621
24. R.M. Porter, C.A. Jahoda, D.P. Lunny, G. Henderson, J. Ross, W.H. McLean, N.V. Whittock, N.J. Wilson, J. Reichelt, T.M. Magin, E.B. Lane Defolliculated (dfl): a dominant mouse mutation leading to poor sebaceous gland differentiation and total elimination of pelage follicles J Invest Dermatol 119 2002 32 37
25. S. Tanaka, M. Tamura, A. Aoki, T. Fujii, H. Komiyama, T. Sagai, T. Shiroishi A new Gsdma3 mutation affecting anagen phase of first hair cycle Biochem Biophys Res Commun 359 2007 902 907
26. J. Li, Y. Zhou, T. Yang, N. Wang, X. Lian, L. Yang Gsdma3 is required for hair follicle differentiation in mice Biochem Biophys Res Commun 403 2010 18 23
27. M. Lei, X. Gao, L. Yang, T. Yang, X. Lian Gsdma3 gene is needed for the induction of apoptosis-driven catagen during mouse hair follicle cycle Histochem Cell Biol 136 2011 335 343
28. F. Ruge, A. Glavini, A.M. Gallimore, H.E. Richards, C.P. Thomas, V.B. O'Donnell, M.P. Philpott, R.M. Porter Delineating immune-mediated mechanisms underlying hair follicle destruction in the mouse mutant defolliculated J Invest Dermatol 131 2011 572 579
29. F. He, Z. Wang, J. Zhao, J. Bao, J. Ding, H. Ruan, Q. Xie, Z. Zhang, X. Gao Large-scale screening of disease model through ENU mutagenesis in mice Chin Sci Bull 48 2003 2665 2671
30. E.D. Green Genome Analysis: A Laboratory Manual: Mapping Genomes 1997 Cold Spring Harbor Laboratory Press Plainview 71 134
31. J. Ding, Y. Gao, J. Zhao, H. Yan, S.Y. Guo, Q.X. Zhang, L.S. Li, X. Gao Pax6 haploinsufficiency causes abnormal metabolic homeostasis by down-regulating glucagon-like peptide 1 in mice Endocrinology 150 2009 2136 2144
32. K.M. Braun, C. Niemann, U.B. Jensen, J.P. Sundberg, V. Silva-Vargas, F.M. Watt Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis Development 130 2003 5241 5255
33. C.S. Trempus, R.J. Morris, C.D. Bortner, G. Cotsarelis, R.S. Faircloth, J.M. Reece, R.W. Tennant Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34 J Invest Dermatol 120 2003 501 511
34. T. Tumbar, G. Guasch, V. Greco, C. Blanpain, W.E. Lowry, M. Rendl, E. Fuchs Defining the epithelial stem cell niche in skin Science 303 2004 359 363
35. R.J. Morris, Y. Liu, L. Marles, Z. Yang, C. Trempus, S. Li, J.S. Lin, J.A. Sawicki, G. Cotsarelis Capturing and profiling adult hair follicle stem cells Nature Biotechnol 22 2004 411 417
36. V.P. Vidal, M.C. Chaboissier, S. Lutzkendorf, G. Cotsarelis, P. Mill, C.C. Hui, N. Ortonne, J.P. Ortonne, A. Schedl Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment Curr Biol 15 2005 1340 1351
37. H. Wang, T. Peters, D. Kess, A. Sindrilaru, T. Oreshkova, N. Van Rooijen, A. Stratis, A.C. Renkl, C. Sunderkotter, M. Wlaschek, I. Haase, K. Scharffetter-Kochanek Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation J Clin Invest 116 2006 2105 2114
38. P. Assouly, P. Reygagne Lichen planopilaris: update on diagnosis and treatment Semin Cutan Med Surg 28 2009 3 10
39. P. Karnik, Z. Tekeste, T.S. McCormick, A.C. Gilliam, V.H. Price, K.D. Cooper, P. Mirmirani Hair follicle stem cell-specific PPARgamma deletion causes scarring alopecia J Invest Dermatol 129 2009 1243 1257
40. T. Ito Hair follicle is a target of stress hormone and autoimmune reactions J Dermatol Sci 60 2010 67 73
41. K.C. Meyer, J.E. Klatte, H.V. Dinh, M.J. Harries, K. Reithmayer, W. Meyer, R. Sinclair, R. Paus Evidence that the bulge region is a site of relative immune privilege in human hair follicles Br J Dermatol 159 2008 1077 1085
42. M.J. Harries, K.C. Meyer, I.H. Chaudhry, C.E. Griffiths, R. Paus Does collapse of immune privilege in the hair-follicle bulge play a role in the pathogenesis of primary cicatricial alopecia? Clin Exp Dermatol 35 2009 637 644
43. V. Horsley, A.O. Aliprantis, L. Polak, L.H. Glimcher, E. Fuchs NFATc1 balances quiescence and proliferation of skin stem cells Cell 132 2008 299 310
44. P.M. Nolan, J. Peters, M. Strivens, D. Rogers, J. Hagan, N. Spurr, I.C. Gray, L. Vizor, D. Brooker, E. Whitehill, R. Washbourne, T. Hough, S. Greenaway, M. Hewitt, X. Liu, S. McCormack, K. Pickford, R. Selley, C. Wells, Z. Tymowska-Lalanne, P. Roby, P. Glenister, C. Thornton, C. Thaung, J.A. Stevenson, R. Arkell, P. Mburu, R. Hardisty, A. Kiernan, A. Erven, K.P. Steel, S. Voegeling, J.L. Guenet, C. Nickols, R. Sadri, M. Nasse, A. Isaacs, K. Davies, M. Browne, E.M. Fisher, J. Martin, S. Rastan, S.D. Brown, J. Hunter A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse Nat Genet 25 2000 440 443
45. M.F. Lyon, P.H. Glenister Bareskin (Bsk) Mouse News Lett 71 1984 26
46. H. Sato, T. Koide, H. Masuya, S. Wakana, T. Sagai, A. Umezawa, S. Ishiguro, M. Tamai, T. Shiroishi A new mutation Rim3 resembling Re(den) is mapped close to retinoic acid receptor alpha (Rara) gene on mouse chromosome 11 Mamm Genome 9 1998 20 25
47. M.F. Lyon, J.F. Zenthon Close linkage of bareskin (Bsk) and rex (Re) Mouse News Lett 74 1986 96
48. L. Ma, J. Liu, T. Wu, M. Plikus, T.X. Jiang, Q. Bi, Y.H. Liu, S. Muller-Rover, H. Peters, J.P. Sundberg, R. Maxson, R.L. Maas, C.M. Chuong "Cyclic alopecia" in Msx2 mutants: defects in hair cycling and hair shaft differentiation Development 130 2003 379 389
49. S. Eichmuller, C. van der Veen, I. Moll, B. Hermes, U. Hofmann, S. Muller-Rover, R. Paus Clusters of perifollicular macrophages in normal murine skin: physiological degeneration of selected hair follicles by programmed organ deletion J Histochem Cytochem 46 1998 361 370
50. R. Gillitzer, K. Wolff, D. Tong, C. Muller, T. Yoshimura, A.A. Hartmann, G. Stingl, R. Berger MCP-1 mRNA expression in basal keratinocytes of psoriatic lesions J Invest Dermatol 101 1993 127 131
51. B. Lu, B.J. Rutledge, L. Gu, J. Fiorillo, N.W. Lukacs, S.L. Kunkel, R. North, C. Gerard, B.J. Rollins Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice J Exp Med 187 1998 601 608
52. J. Xaus, M. Comalada, A.F. Valledor, J. Lloberas, F. Lopez-Soriano, J.M. Argiles, C. Bogdan, A. Celada LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-alpha Blood 95 2000 3823 3831
53. M.J. Harries, R. Paus Scarring alopecia and the PPAR-gamma connection J Invest Dermatol 129 2009 1066 1070
54. G. Cotsarelis Epithelial stem cells: a folliculocentric view J Invest Dermatol 126 2006 1459 1468
55. S. Muller-Rover, S. Bulfone-Paus, B. Handjiski, P. Welker, J.P. Sundberg, I.A. McKay, V.A. Botchkarev, R. Paus Intercellular adhesion molecule-1 and hair follicle regression J Histochem Cytochem 48 2000 557 568