Defective maintenance of pH of stratum corneum is correlated with preferential emergence and exacerbation of atopic-dermatitis-like dermatitis in flaky-tail mice

Journal of Dermatological Science

Volumn 74, Issue 3, 2014, Pages 222-228

  Sakai, Takashi ^a   Hatano, Yutaka ^a   Zhang, Wei ^a   Fujiwara, Sakuhei ^a  

^a OITA UNIVERSITY   (Japan)

Author keywords

AD; Atopic dermatitis; Filaggrin; Flaky tail mice; FTM; NHE1; NMFs; SC; SPase; SPLA2; Stratum corneum pH; TARC; TEWL; TMG; TSLP; WT

Indexed keywords

1,1,3,3 TETRAMETHYLGUANIDINE; FILAGGRIN; IMMUNOGLOBULIN E; METHYLGUANIDINE; SERINE PROTEINASE; SODIUM PROTON EXCHANGE PROTEIN 1; THYMIC STROMAL LYMPHOPOIETIN; UNCLASSIFIED DRUG; 1,1,3,3-TETRAMETHYLGUANIDINE; CATION TRANSPORT PROTEIN; CYTOKINE; GUANIDINE DERIVATIVE; SLC9A1 PROTEIN, MOUSE; SODIUM PROTON EXCHANGE PROTEIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ACIDITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOPIC DERMATITIS; ATOPIC DERMATITIS LIKE DERMATITIS; C57BL 6 MOUSE; DISEASE ASSOCIATION; DISEASE EXACERBATION; ENZYME ACTIVATION; ENZYME ACTIVITY; EXPERIMENTAL MOUSE; FEMALE; FLAKY TAIL MOUSE; IMMUNOPATHOGENESIS; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROGNOSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SERODIAGNOSIS; STRATUM CORNEUM; THYMUS; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; DERMATITIS, ATOPIC; EPIDERMIS; METABOLISM;

ANIMALS; CATION TRANSPORT PROTEINS; CHEMOKINE CCL17; CYTOKINES; DERMATITIS, ATOPIC; EPIDERMIS; FEMALE; GUANIDINES; HYDROGEN-ION CONCENTRATION; IMMUNOGLOBULIN E; MICE, INBRED C57BL; SERINE PROTEASES; SODIUM-HYDROGEN ANTIPORTER;

EID: 84899955293     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2014.01.012     Document Type: Article

References (39)

1. Bieber T. Atopic dermatitis. N Engl J Med 2008, 358:1483-1494.
2. McAleer M.A., Irvine A.D. The multifunctional role of filaggrin in allergic skin disease. J Allergy Clin Immunol 2013, 131:280-291.
3. 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 2008, 121:1337-1343.
4. Fluhr J.W., Kao J., Jain M., Ahn S.K., Feingold K.R., Elias P.M. Generation of free fatty acids from phospholipids regulates stratum corneum acidification and integrity. J Invest Dermatol 2001, 117:44-51.
5. Hachem J.P., Crumrine D., Fluhr J., Brown B.E., Feingold K.R., Elias P.M. pH directly regulates epidermal permeability barrier homeostasis, and stratum corneum integrity/cohesion. J Invest Dermatol 2003, 121:345-353.
6. Mauro T., Holleran W.M., Grayson S., Gao W.N., Man M.Q., Kriehuber E., et al. Barrier recovery is impeded at neutral pH, independent of ionic effects: implications for extracellular lipid processing. Arch Dermatol Res 1998, 290:215-222.
7. Elias P.M. The skin barrier as an innate immune element. Semin Immunopathol 2007, 29:3-14.
8. Hachem J.P., Man M.Q., Crumrine D., Uchida Y., Brown B.E., Rogiers V., et al. Sustained serine proteases activity by prolonged increase in pH leads to degradation of lipid processing enzymes and profound alterations of barrier function and stratum corneum integrity. J Invest Dermatol 2005, 125:510-520.
9. Kouzaki H., O'Grady S.M., Lawrence C.B., Kita H. Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J Immunol 2009, 183:1427-1434.
10. Hatano Y., Man M.Q., Uchida Y., Crumrine D., Scharschmidt T.C., Kim E.G., et al. Maintenance of an acidic stratum corneum prevents emergence of murine atopic dermatitis. J Invest Dermatol 2009, 129:1824-1835.
11. Hachem J.P., Behne M., Aronchik I., Demerjian M., Feingold K.R., Elias P.M., et al. Extracellular pH controls NHE1 expression in epidermis and keratinocytes: implications for barrier repair. J Invest Dermatol 2005, 125:790-797.
12. Chikakane K., Takahashi H. Measurement of skin pH and its significance in cutaneous diseases. Clin Dermatol 1995, 13:299-306.
13. Hachem J.P., Roelandt T., Schürer N., Pu X., Fluhr J., Giddelo C., et al. Acute acidification of stratum corneum membrane domains using polyhydroxyl acids improves lipid processing and inhibits degradation of corneodesmosomes. J Invest Dermatol 2010, 130:500-510.
14. Bibel D.J., Miller S.J., Brown B.E., Pandey B.B., Elias P.M., Shinefield H.R., et al. Antimicrobial activity of stratum corneum lipids from normal and essential fatty acid-deficient mice. J Invest Dermatol 1989, 92:632-638.
15. Di Marzio L., Cinque B., De Simone C., Cifone M.G. Effect of the lactic acid bacterium Streptococcus thermophilus on ceramide levels in human keratinocytes in vitro and stratum corneum in vivo. J Invest Dermatol 1999, 113:98-106.
16. Ament W., Huizenga J.R., Mook G.A., Gips C.H., Verkerke G.J. Lactate and ammonia concentration in blood and sweat during incremental cycle ergometer exercise. Int J Sports Med 1997, 18:35-39.
17. Thueson D.O., Chan E.K., Oechsli L.M., Hahn G.S. The roles of pH and concentration in lactic acid-induced stimulation of epidermal turnover. Dermatol Surg 1998, 24:641-645.
18. Behne M.J., Meyer J.W., Hanson K.M., Barry N.P., Murata S., Crumrine D., et al. NHE1 regulates the stratum corneum permeability barrier homeostasis. Microenvironment acidification assessed with fluorescence lifetime imaging. J Biol Chem 2002, 277:47399-47406.
19. Fluhr J.W., Behne M.J., Brown B.E., Moskowitz D.G., Selden C., Mao-Qiang M., et al. Stratum corneum acidification in neonatal skin: secretory phospholipase A2 and the sodium/hydrogen antiporter-1 acidify neonatal rat stratum corneum. J Invest Dermatol 2004, 122:320-329.
20. Fluhr J.W., Elias P.M., Man M.Q., Hupe M., Selden C., Sundberg J.P., et al. Is the filaggrin-histidine-urocanic acid pathway essential for stratum corneum acidification. J Invest Dermatol 2010, 130:2141-2144.
21. Krien P.M., Kermici M. Evidence for the existence of a self-regulated enzymatic process within the human stratum corneum - an unexpected role for urocanic acid. J Invest Dermatol 2000, 115:414-420.
22. Scharschmidt T.C., Man M.Q., Hatano Y., Crumrine D., Gunathilake R., Sundberg J.P., et al. Filaggrin deficiency confers a paracellular barrier abnormality that reduces inflammatory thresholds to irritants and haptens. J Allergy Clin Immunol 2009, 124:496-506.
23. Moniaga C.S., Egawa G., Kawasaki H., Hara-Chikuma M., Honda T., Tanizaki H., et al. Flaky tail mouse denotes human atopic dermatitis in the steady state and by topical application with Dermatophagoides pteronyssinus extract. Am J Pathol 2010, 176:2385-2393.
24. Vávrová K., Henkes D., Strüver K., Sochorová M., Skolová B., Witting M.Y., et al. Filaggrin Deficiency Leads to Impaired Lipid Profile and Altered Acidification Pathways in a 3D Skin Construct. J Invest Dermatol 2014, 134:746-753.
25. Hatano Y., Elias P.M., Crumrine D., Feingold K.R., Katagiri K., Fujiwara S. Efficacy of combined peroxisome proliferator-activated receptor-α ligand and glucocorticoid therapy in a murine model of atopic dermatitis. J Invest Dermatol 2011, 131:1845-1852.
26. Hatano Y., Man M.Q., Uchida Y., Crumrine D., Mauro T.M., Feingold K.R., et al. Murine atopic dermatitis responds to peroxisome proliferator-activated receptors alpha and beta/delta (but not gamma) and liver X receptor activators. J Allergy Clin Immunol 2010, 125:160-169.
27. Hatano Y., Adachi Y., Elias P.M., Crumrine D., Sakai T., Kurahashi R., et al. The Th2 cytokine, interleukin-4, abrogates the cohesion of normal stratum corneum in mice: implications for pathogenesis of atopic dermatitis. Exp Dermatol 2013, 22:30-35.
28. Taneda K., Tominaga M., Negi O., Tengara S., Kamo A., Ogawa H., et al. Evaluation of epidermal nerve density and opioid receptor levels in psoriatic itch. Br J Dermatol 2011, 165:277-284.
29. Fallon P.G., Sasaki T., Sandilands A., Campbell L.E., Saunders S.P., Mangan N.E., et al. A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming. Nat Genet 2009, 41:602-608.
30. Oyoshi M.K., Murphy G.F., Geha R.S. Filaggrin-deficient mice exhibit TH17-dominated skin inflammation and permissiveness to epicutaneous sensitization with protein antigen. J Allergy Clin Immunol 2009, 124:485-493.
31. Kawasaki H., Nagao K., Kubo A., Hata T., Shimizu A., Mizuno H., et al. Altered stratum corneum barrier and enhanced percutaneous immune responses in filaggrin-null mice. J Allergy Clin Immunol 2012, 129:1538-1546.
32. Kabashima K. New concept of the pathogenesis of atopic dermatitis: interplay among the barrier, allergy, and pruritus as a trinity. J Dermatol Sci 2013, 70:3-11.
33. Moniaga C.S., Jeong S.K., Egawa G., Nakajima S., Hara-Chikuma M., Jeon J.E., et al. Protease activity enhances production of thymic stromal lymphopoietin and basophil accumulation in flaky tail mice. Am J Pathol 2013, 182:841-851.
34. Bieber T., Cork M., Reitamo S. Atopic dermatitis: a candidate for disease-modifying strategy. Allergy 2012, 67:969-975.
35. Kakinuma T., Nakamura K., Wakugawa M., Mitsui H., Tada Y., Saeki H., et al. Thymus and activation-regulated chemokine in atopic dermatitis: serum thymus and activation-regulated chemokine level is closely related with disease activity. J Allergy Clin Immunol 2001, 107:535-541.
36. Kubo A., Nagao K., Amagai M. Epidermal barrier dysfunction and cutaneous sensitization in atopic diseases. J Clin Invest 2012, 122:440-447.
37. Kabashima-Kubo R., Nakamura M., Sakabe J., Sugita K., Hino R., Mori T., et al. A group of atopic dermatitis without IgE elevation or barrier impairment shows a high Th1 frequency: possible immunological state of the intrinsic type. J Dermatol Sci 2012, 67:37-43.
38. Schäfer L., Kragballe K. Abnormalities in epidermal lipid metabolism in patients with atopic dermatitis. J Invest Dermatol 1991, 96:10-15.
39. Tarroux R., Assalit M.F., Licu D., Périé J.J., Redoulès D. Variability of enzyme markers during clinical regression of atopic dermatitis. Skin Pharmacol Appl Skin Physiol 2002, 15:55-62.