Novel skin phenotypes revealed by a genome-wide mouse reverse genetic screen

Nature Communications

Volumn 5, Issue , 2014, Pages

  Liakath Ali, Kifayathullah ^a,b   Vancollie, Valerie E ^c   Heath, Emma ^a   Smedley, Damian P ^c   Estabel, Jeanne ^c   Sunter, David ^c   Ditommaso, Tia ^d,f   White, Jacqueline K ^c   Ramirez Solis, Ramiro ^c   Smyth, Ian ^d   Steel, Karen P ^c,e   Watt, Fiona M ^a  

^a GUY S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d MONASH UNIVERSITY   (Australia)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; HAIR; MUTATION; PHENOTYPE; RODENT; SKIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONGENITAL SKIN DISEASE; CONTROLLED STUDY; DIET; EPIDERMIS; FEMALE; GENE DELETION; GENE EXPRESSION; GENETIC SCREENING; GENOME; GRISCELLI SYNDROME; HAIR FOLLICLE; MOUSE; MUTANT; NONHUMAN; ONTOLOGY; PHENOTYPE; REVERSE GENETICS; SEBACEOUS GLAND; SKIN; TAIL; VALIDATION PROCESS; ANIMAL; GENETIC DATABASE; HUMAN; KNOCKOUT MOUSE; MALE; MUTATION; PROCEDURES;

ANIMALS; DATABASES, GENETIC; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MUTATION; PHENOTYPE; REVERSE GENETICS; SKIN;

EID: 84898669669     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4540     Document Type: Article

References (62)

1. Brenner, S. Sequences and consequences. Phil. Trans. R Soc. B 365, 207-212 (2010).
2. Lander, E. S. Initial impact of the sequencing of the human genome. Nature 470, 187-197 (2011).
3. Tang, T. et al. A mouse knockout library for secreted and transmembrane proteins. Nat. Biotechnol. 28, 749-755 (2010).
4. Kumar, V. et al. Second-generation high-throughput forward genetic screen in mice to isolate subtle behavioral mutants. Proc. Natl Acad. Sci. USA 108(Suppl 3): 15557-15564 (2011).
5. Arwert, E. N., Hoste, E. & Watt, F. M. Epithelial stem cells, wound healing and cancer. Nat. Rev. Cancer 12, 170-180 (2012).
6. Fuchs, E. Scratching the surface of skin development. Nature 445, 834-842 (2007).
7. Benavides, F., Oberyszyn, T.M., VanBuskirk, A. M., Reeve, V. E. & Kusewitt, D. F. The hairless mouse in skin research. J. Dermatol. Sci. 53, 10-18 (2009).
8. Mulder, K. W. et al. Diverse epigenetic strategies interact to control epidermal differentiation. Nat. Cell Biol. 14, 753-763 (2012).
9. Beronja, S. et al. RNAi screens in mice identify physiological regulators of oncogenic growth. Nature 501, 185-190 (2013).
10. Braun, K. M. et al. Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130, 5241-5255 (2003). (Pubitemid 37369682)
11. Kretzschmar, K. W. & Watt, F. M. Markers of epidermal stem cell subpopulations in adult mammalian skin. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a013631 (2014).
12. Skarnes, W. C. et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342 (2011).
13. White, J. K. et al. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 154, 452-464 (2013).
14. Eppig, J. T. Algorithms for mutant sorting: the need for phenotype vocabularies. Mamm Genome 11, 584-589 (2000). (Pubitemid 30602228)
15. Smith, C. L., Goldsmith, C. A. & Eppig, J. T. The Mammalian Phenotype Ontology as a tool for annotating, analyzing and comparing phenotypic information. Genome Biol. 6, R7 (2005).
16. Gomez, C. et al. The interfollicular epidermis of adult mouse tail comprises two distinct cell lineages that are differentially regulated by Wnt, Edaradd, and Lrig1. Stem Cell Rep. 1, 19-27 (2013).
17. Jensen, K. B. et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4, 427-439 (2009).
18. Blanco, S. et al. The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet. 7, e1002403 (2011).
19. Frances, D. & Niemann, C. Stem cell dynamics in sebaceous gland morphogenesis in mouse skin. Dev. Biol. 363, 138-146 (2012).
20. Kellermayer, R. et al. Bigenic connexin mutations in a patient with hidrotic ectodermal dysplasia. Eur. J. Dermatol. 15, 75-79 (2005). (Pubitemid 40434629)
21. Tang, S., Han, H. & Bajic, V. B. ERGDB: estrogen responsive genes database. Nucleic Acids Res. 32, D533-D536 (2004). (Pubitemid 38081715)
22. Robinson, P. N. et al. The human phenotype ontology: a tool for annotating and analyzing human hereditary disease. Am. J. Hum. Genet. 83, 610-615 (2008).
23. Lopez-Pajares, V., Yan, K., Zarnegar, B. J., Jameson, K. L. & Khavari, P. A. Genetic pathways in disorders of epidermal differentiation. Trends Genet. 29, 31-40 (2013).
24. Doma, E., Rupp, C. & Baccarini, M. EGFR-ras-raf signaling in epidermal stem cells: roles in hair follicle development, regeneration, tissue remodeling and epidermal cancers. Int. J. Mol. Sci. 14, 19361-19384 (2013).
25. Ambatipudi, S. et al. Downregulation of keratin 76 expression during oral carcinogenesis of human, hamster and mouse. PloS One 8, e70688 (2013).
26. Pastural, E. et al. Griscelli disease maps to chromosome 15q21 and is associated with mutations in the myosin-Va gene. Nat. Genet. 16, 289-292 (1997). (Pubitemid 27280214)
27. Alsultan, A., Shamseldin, H. E., Osman, M. E., Aljabri, M. & Alkuraya, F. S. MYSM1 is mutated in a family with transient transfusion- dependent anemia, mild thrombocytopenia, and low NK-and B-cell counts. Blood 122, 3844-3845 (2013).
28. Wang, T. et al. The control of hematopoietic stem cell maintenance, selfrenewal, and differentiation by Mysm1-mediated epigenetic regulation. Blood 122, 2812-2822 (2013).
29. Gu, L. H. & Coulombe, P. A. Keratin function in skin epithelia: a broadening palette with surprising shades. Curr. Opin. Cell Biol. 19, 13-23 (2007). (Pubitemid 46123973)
30. Watt, F. M. & Collins, C. A. Role of beta-catenin in epidermal stem cell expansion, lineage selection, and cancer. Cold Spring Harb. Symp. Quant. Biol. 73, 503-512 (2008).
31. Franceschini, A. et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815 (2013).
32. Gutierrez, J. A. et al. A novel non-sense mutation in keratin 10 causes a familial case of recessive epidermolytic ichthyosis. Mol. Genet. Genomic Med. 1, 108-112 (2013).
33. Mercer, J. A., Seperack, P. K., Strobel, M. C., Copeland, N. G. & Jenkins, N. A. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349, 709-713 (1991). (Pubitemid 21912144)
34. Fukuda, M. & Kuroda, T. S. Missense mutations in the globular tail of myosin-Va in dilute mice partially impair binding of Slac2-a/melanophilin. J. Cell Sci. 117, 583-591 (2004). (Pubitemid 38240199)
35. Hume, A. N., Ushakov, D. S., Tarafder, A. K., Ferenczi, M. A. & Seabra, M. C. Rab27a and MyoVa are the primary Mlph interactors regulating melanosome transport in melanocytes. J. Cell Sci. 120, 3111-3122 (2007). (Pubitemid 47517093)
36. Klomp, A. E., Teofilo, K., Legacki, E. & Williams, D. S. Analysis of the linkage of MYRIP and MYO7A to melanosomes by RAB27A in retinal pigment epithelial cells. Cell Motil. Cytoskeleton 64, 474-487 (2007). (Pubitemid 46801579)
37. Gibbs, D. et al. Function of MYO7A in the human RPE and the validity of shaker1 mice as a model for Usher syndrome 1B. Invest. Ophthalmol. Vis. Sci. 51, 1130-1135 (2010).
38. Clague, M. J., Coulson, J. M. & Urbe, S. Deciphering histone 2A deubiquitination. Genome Biol. 9, 202 (2008).
39. Zhu, P. et al. A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol. Cell 27, 609-621 (2007). (Pubitemid 47238636)
40. Nguyen, H. et al. Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat. Genet. 41, 1068-1075 (2009).
41. Lindsay, C. R. et al. P-Rex1 is required for efficient melanoblast migration and melanoma metastasis. Nat. Commun. 2, 555 (2011).
42. Li, A. et al. Rac1 drives melanoblast organization during mouse development by orchestrating pseudopod-driven motility and cell-cycle progression. Dev. Cell 21, 722-734 (2011).
43. Trantow, C. M., Cuffy, T. L., Fingert, J. H., Kuehn, M. H. & Anderson, M. G. Microarray analysis of iris gene expression in mice with mutations influencing pigmentation. Invest. Ophthalmol. Vis. Sci. 52, 237-248 (2011).
44. Ando, H., Ichihashi, M. & Hearing, V. J. Role of the ubiquitin proteasome system in regulating skin pigmentation. Int. J. Mol. Sci. 10, 4428-4434 (2009).
45. Bucan, M., Eppig, J. T. & Brown, S. Mouse genomics programs and resources. Mamm. Genome 23, 479-489 (2012).
46. Driskell, R. R. et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504, 277-281 (2013).
47. Bassett, J. H. et al. Rapid-throughput skeletal phenotyping of 100 knockout mice identifies 9 new genes that determine bone strength. PLoS Genet. 8, e1002858 (2012).
48. Schmidt, F. et al. The role of conserved PEX3 regions in PEX19-binding and peroxisome biogenesis. Traffic 13, 1244-1260 (2012).
49. Karnik, P. et al. Hair follicle stem cell-specific PPARgamma deletion causes scarring alopecia. J. Invest. Dermatol. 129, 1243-1257 (2009).
50. Cheung, C., Davies, N. G., Hoog, J. O., Hotchkiss, S. A. & Smith Pease, C. K. Species variations in cutaneous alcohol dehydrogenases and aldehyde dehydrogenases may impact on toxicological assessments of alcohols and aldehydes. Toxicology 184, 97-112 (2003). (Pubitemid 36009292)
51. Muzio, G., Maggiora, M., Paiuzzi, E., Oraldi, M. & Canuto, R. A. Aldehyde dehydrogenases and cell proliferation. Free Radic. Biol. Med. 52, 735-746 (2012).
52. Petiot, A. et al. A crucial role for Fgfr2-IIIb signalling in epidermal development and hair follicle patterning. Development 130, 5493-5501 (2003). (Pubitemid 37484016)
53. Schlake, T. & Sick, S. Canonical WNT signalling controls hair follicle spacing. Cell Adh. Migr. 1, 149-151 (2007).
54. Van Loo, P. L., Van Zutphen, L. F. & Baumans, V. Male management: coping with aggression problems in male laboratory mice. Lab. Anim. 37, 300-313 (2003). (Pubitemid 37297041)
55. Azzi, L., El-Alfy, M., Martel, C. & Labrie, F. Gender differences in mouse skin morphology and specific effects of sex steroids and dehydroepiandrosterone. J. Invest. Dermatol. 124, 22-27 (2005). (Pubitemid 40100944)
56. Jensen, K. B. & Watt, F. M. Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc. Natl. Acad. Sci. USA 103, 11958-11963 (2006). (Pubitemid 44215793)
57. Valenzuela, D. M. et al. High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat. Biotechnol. 21, 652-659 (2003). (Pubitemid 36638092)
58. Goldenberger, D., Perschil, I., Ritzler, M. & Altwegg, M. A simple 'universal' DNA extraction procedure using SDS and proteinase K is compatible with direct PCR amplification. PCR Methods Appl. 4, 368-370 (1995).
59. Boyle, E. I. et al. GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics 20, 3710-3715 (2004). (Pubitemid 40136825)
60. Supek, F., Bosnjak, M., Skunca, N. & Smuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PloS One 6, e21800 (2011).
61. Croft, D. et al. Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res. 39, D691-D697 (2011).
62. Chen, J., Bardes, E. E., Aronow, B. J. & Jegga, A. G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 37, W305-W311 (2009).