Protein Palmitoylation by ZDHHC13 Protects Skin against Microbial-Driven Dermatitis

Journal of Investigative Dermatology

Volumn 137, Issue 4, 2017, Pages 894-904

  Chen, Li Ying ^a,b   Yang Yen, Hsin Fang ^c   Tsai, Chun Chou ^a   Thio, Christina Li Ping ^a,b   Chuang, Hsiao Li ^d   Yang, Liang Tung ^e   Shen, Li Fen ^a   Song, I Wen ^a   Liu, Kai Ming ^a   Huang, Yen Te ^d   Liu, Fu Tong ^a   Chang, Ya Jen ^a   Chen, Yuan Tsong ^a   Yen, Jeffrey J Y ^a,b  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b ACADEMIA SINICA   (Taiwan)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^d NATIONAL APPLIED RESEARCH LABORATORIES   (Taiwan)

^e NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; FILAGGRIN; INTERLEUKIN 33; TUMOR NECROSIS FACTOR; ACYLTRANSFERASE; BIOLOGICAL MARKER; CYTOKINE; ZDHHC13 PROTEIN, MOUSE;

ALOPECIA; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; ATOPIC DERMATITIS; CELL INFILTRATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE; GENE MUTATION; GENETIC PREDISPOSITION; IMMUNOHISTOCHEMISTRY; LACZ GENE; LYMPHOID CELL; MOUSE; MUTAGENESIS; NONHUMAN; PALMITOYLATION; PROTEIN METABOLISM; RADIOIMMUNOPRECIPITATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN DEFECT; SKIN PERMEABILITY; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ZDHHC13 GENE; ANIMAL; DERMATITIS; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LIPOYLATION; METABOLISM; MICROBIOLOGY; MUTANT MOUSE STRAIN; NEEDLE BIOPSY; PATHOLOGY; RANDOMIZATION;

ACYLTRANSFERASES; ANIMALS; BIOMARKERS; BIOPSY, NEEDLE; CYTOKINES; DERMATITIS; DERMATITIS, ATOPIC; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; LIPOYLATION; MICE; MICE, MUTANT STRAINS; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 85015946198     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1016/j.jid.2016.12.011     Document Type: Article

References (42)

1. Amarasekara, D.S., Yu, J., Rho, J., Bone loss triggered by the cytokine network in inflammatory autoimmune diseases. J Immunol Res, 2015, 2015, 832127.
2. Barnes, K.C., An update on the genetics of atopic dermatitis: scratching the surface in 2009. J Allergy Clin Immunol 125 (2010), 16–29.
3. Brandt, E.B., Sivaprasad, U., Th2 cytokines and atopic dermatitis. J Clin Cell Immunol, 2, 2011, 110.
4. Chuang, H.L., Huang, Y.T., Chiu, C.C., Liao, C.D., Hsu, F.L., Huang, C.C., et al. Metabolomics characterization of energy metabolism reveals glycogen accumulation in gut-microbiota-lacking mice. J Nutr Biochem 23 (2012), 752–758.
5. Cork, M.J., Robinson, D.A., Vasilopoulos, Y., Ferguson, A., Moustafa, M., MacGowan, A., et al. New perspectives on epidermal barrier dysfunction in atopic dermatitis: gene-environment interactions. J Allergy Clin Immunol 118 (2006), 3–21.
6. DaVeiga, S.P., Epidemiology of atopic dermatitis: a review. Allergy Asthma Proc 33 (2012), 227–234.
7. Elias, P.M., Hatano, Y., Williams, M.L., Basis for the barrier abnormality in atopic dermatitis: outside-inside-outside pathogenic mechanisms. J Allergy Clin Immunol 121 (2008), 1337–1343.
8. Feil, R., Brocard, J., Mascrez, B., LeMeur, M., Metzger, D., Chambon, P., Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA 93 (1996), 10887–10890.
9. Fukata, Y., Fukata, M., Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci 11 (2010), 161–175.
10. Greaves, J., Chamberlain, L.H., Palmitoylation-dependent protein sorting. J Cell Biol 176 (2007), 249–254.
11. Greaves, J., Prescott, G.R., Gorleku, O.A., Chamberlain, L.H., The fat controller: roles of palmitoylation in intracellular protein trafficking and targeting to membrane microdomains. Mol Membr Biol 26 (2009), 67–79.
12. Haeck, I.M., Hamdy, N.A., Timmer-de Mik, L., Lentjes, E.G., Verhaar, H.J., Knol, M.J., et al. Low bone mineral density in adult patients with moderate to severe atopic dermatitis. Br J Dermatol 161 (2009), 1248–1254.
13. Haenuki, Y., Matsushita, K., Futatsugi-Yumikura, S., Ishii, K.J., Kawagoe, T., Imoto, Y., et al. A critical role of IL-33 in experimental allergic rhinitis. J Allergy Clin Immunol 130 (2012), 184–194.e11.
14. Hardman, M.J., Sisi, P., Banbury, D.N., Byrne, C., Patterned acquisition of skin barrier function during development. Development 125 (1998), 1541–1552.
15. Hou, S.Y., Mitra, A.K., White, S.H., Menon, G.K., Ghadially, R., Elias, P.M., Membrane structures in normal and essential fatty acid-deficient stratum corneum: characterization by ruthenium tetroxide staining and x-ray diffraction. J Invest Dermatol 96 (1991), 215–223.
16. Jakasa, I., Verberk, M.M., Esposito, M., Bos, J.D., Kezic, S., Altered penetration of polyethylene glycols into uninvolved skin of atopic dermatitis patients. J Invest Dermatol 127 (2007), 129–134.
17. Kelleher, M.M., O'Carroll, M., Gallagher, A., Murray, D.M., Dunn Galvin, A., Irvine, A.D., et al. Newborn transepidermal water loss values: a reference dataset. Pediatr Dermatol 30 (2013), 712–716.
18. Kim, B.S., Siracusa, M.C., Saenz, S.A., Noti, M., Monticelli, L.A., Sonnenberg, G.F., et al. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med, 5, 2013, 170ra16.
19. Kondo, Y., Yoshimoto, T., Yasuda, K., Futatsugi-Yumikura, S., Morimoto, M., Hayashi, N., et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol 20 (2008), 791–800.
20. Liang, C.C., You, L.R., Chang, J.L., Tsai, T.F., Chen, C.M., Transgenic mice exhibiting inducible and spontaneous Cre activities driven by a bovine keratin 5 promoter that can be used for the conditional analysis of basal epithelial cells in multiple organs. J Biomed Sci, 16, 2009, 2.
21. Linder, M.E., Deschenes, R.J., Model organisms lead the way to protein palmitoyltransferases. J Cell Sci 117 (2004), 521–526.
22. Linder, M.E., Deschenes, R.J., Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 8 (2007), 74–84.
23. Liu, K.M., Chen, Y.J., Shen, L.F., Haddad, A.N., Song, I.W., Chen, L.Y., et al. Cyclic alopecia and abnormal epidermal cornification in Zdhhc13-deficient mice reveal the importance of palmitoylation in hair and skin differentiation. J Invest Dermatol 135 (2015), 2603–2610.
24. Madison, K.C., Swartzendruber, D.C., Wertz, P.W., Downing, D.T., Lamellar granule extrusion and stratum corneum intercellular lamellae in murine keratinocyte cultures. J Invest Dermatol 90 (1988), 110–116.
25. Miller, A.M., Role of IL-33 in inflammation and disease. J Inflamm (Lond), 8, 2011, 22.
26. Nagy, A., Gertsenstein, M., Vintersten, K., Behringer, R., Staining whole mouse embryos for {beta}-galactosidase (lacZ) activity. CSH Protoc, 2007, 2007, prot4725.
27. O'Regan, G.M., Sandilands, A., McLean, W.H., Irvine, A.D., Filaggrin in atopic dermatitis. J Allergy Clin Immunol 124 (2009), R2–R6.
28. Palmer, C.N., Irvine, A.D., Terron-Kwiatkowski, A., Zhao, Y., Liao, H., Lee, S.P., et al. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet 38 (2006), 441–446.
29. Peterson, J.D., Chan, L.S., A comprehensive management guide for atopic dermatitis. Dermatol Nurs 18 (2006), 531–542.
30. Resh, M.D., Trafficking and signaling by fatty-acylated and prenylated proteins. Nat Chem Biol 2 (2006), 584–590.
31. Roediger, B., Kyle, R., Yip, K.H., Sumaria, N., Guy, T.V., Kim, B.S., et al. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat Immunol 14 (2013), 564–573.
32. Saleem, A.N., Chen, Y.H., Baek, H.J., Hsiao, Y.W., Huang, H.W., Kao, H.J., et al. Mice with alopecia, osteoporosis, and systemic amyloidosis due to mutation in Zdhhc13, a gene coding for palmitoyl acyltransferase. PLoS Genet, 6, 2010, e1000985.
33. Salimi, M., Barlow, J.L., Saunders, S.P., Xue, L., Gutowska-Owsiak, D., Wang, X., et al. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J Exp Med 210 (2013), 2939–2950.
34. Sandilands, A., Sutherland, C., Irvine, A.D., McLean, W.H., Filaggrin in the frontline: role in skin barrier function and disease. J Cell Sci 122 (2009), 1285–1294.
35. Saunders, S.P., Moran, T., Floudas, A., Wurlod, F., Kaszlikowska, A., Salimi, M., et al. Spontaneous atopic dermatitis is mediated by innate immunity, with the secondary lung inflammation of the atopic march requiring adaptive immunity. J Allergy Clin Immunol 137 (2015), 482–491.
36. Schmitz, A., Lazic, E., Koumaki, D., Kuonen, F., Verykiou, S., Rubsam, M., Assessing the in vivo epidermal barrier in mice: dye penetration assays. J Invest Dermatol, 135, 2015, e29.
37. Song, I.W., Li, W.R., Chen, L.Y., Shen, L.F., Liu, K.M., Yen, J.J., et al. Palmitoyl acyltransferase, Zdhhc13, facilitates bone mass acquisition by regulating postnatal epiphyseal development and endochondral ossification: a mouse model. PLoS One, 9, 2014, e92194.
38. Spergel, J.M., Paller, A.S., Atopic dermatitis and the atopic march. J Allergy Clin Immunol 112:Suppl (2003), S118–S127.
39. Sutton, L.M., Sanders, S.S., Butland, S.L., Singaraja, R.R., Franciosi, S., Southwell, A.L., et al. Hip14l-deficient mice develop neuropathological and behavioural features of Huntington disease. Hum Mol Genet 22 (2013), 452–465.
40. Tokura, Y., Extrinsic and intrinsic types of atopic dermatitis. J Dermatol Sci 58 (2010), 1–7.
41. Watson, W., Kapur, S., Atopic dermatitis. Allergy Asthma Clin Immunol, 7(Suppl 1), 2011, S4.
42. Williams, H., Robertson, C., Stewart, A., Ait-Khaled, N., Anabwani, G., Anderson, R., et al. Worldwide variations in the prevalence of symptoms of atopic eczema in the International Study of Asthma and Allergies in Childhood. J Allergy Clin Immunol 103 (1999), 125–138.