Topical calcineurin inhibitors compromise stratum corneum integrity, epidermal permeability and antimicrobial barrier function

Experimental Dermatology

Volumn 19, Issue 6, 2010, Pages 501-510

  Kim, Minjeong ^a   Jung, Minyoung ^a   Hong, Seung Phil ^b   Jeon, Hyerin ^a   Kim, Min Jung ^a   Cho, Mee Yon ^a   Lee, Seung Hun ^c   Man, Mao Qiang ^d   Elias, Peter M ^d   Choi, Eung Ho ^a  

^a Yonsei University Wonju College of Medicine   (South Korea)

^b Konyang University College of Medicine   (South Korea)

^c Yonsei University College of Medicine   (South Korea)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antimicrobial peptides; Epidermal permeability barrier; Physiologic lipid mixture; Pimecrolimus; Tacrolimus

Indexed keywords

BETA DEFENSIN 3; CALCINEURIN INHIBITOR; CATHELIN RELATED ANTIMICROBIAL PEPTIDE; CERAMIDE DERIVATIVE; CHOLESTEROL; FATTY ACID; FATTY ACID SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INTERLEUKIN 1ALPHA; LIPID; PEPTIDE; PHYSIOLOGIC LIPID MIXTURE; PIMECROLIMUS; SERINE PALMITOYLTRANSFERASE; TACROLIMUS; TRICERAM; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EPIDERMIS; FEMALE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; LIPOGENESIS; MALE; MOUSE; NONHUMAN; PERMEABILITY BARRIER; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SKIN FUNCTION; SKIN PERMEABILITY; SKIN WATER LOSS; STRATUM CORNEUM;

ADULT; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BETA-DEFENSINS; CALCINEURIN; CATHELICIDINS; CYTOPLASMIC GRANULES; DESMOSOMES; ELECTRIC IMPEDANCE; ENZYME INHIBITORS; EPIDERMIS; FATTY ACID SYNTHETASE COMPLEX; FEMALE; GENE EXPRESSION; HOMEOSTASIS; HUMANS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; INTERLEUKIN-1ALPHA; LIPID METABOLISM; LIPIDS; MALE; MICE; MICE, HAIRLESS; PERMEABILITY; PROLIFERATING CELL NUCLEAR ANTIGEN; SERINE C-PALMITOYLTRANSFERASE; SKIN; TACROLIMUS; YOUNG ADULT;

EID: 77954071532     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2009.00941.x     Document Type: Article

References (49)

1. Nghiem P, Pearson G, Langley R G. Tacrolimus and pimecrolimus: from clever prokaryotes to inhibiting calcineurin and treating atopic dermatitis. J Am Acad Dermatol 2002, 46:228-241.
2. Paul C, Cork M, Rossi A B, Papp K A, Barbier N, de Prost Y. Safety and tolerability of 1% pimecrolimus cream among infants: experience with 1133 patients treated for up to 2 years. Pediatrics 2006, 117:e118-128.
3. Remitz A, Harper J, Rustin M. Long-term safety and efficacy of tacrolimus ointment for the treatment of atopic dermatitis in children. Acta Derm Venereol 2007, 87:54-61.
4. Hengge U R, Ruzicka T, Schwartz R A, Cork M J. Adverse effects of topical glucocorticosteroids. J Am Acad Dermatol 2006, 54:1-15. quiz 16-18
5. Kao J S, Fluhr J W, Man M Q. Short-term glucocorticoid treatment compromises both permeability barrier homeostasis and stratum corneum integrity: inhibition of epidermal lipid synthesis accounts for functional abnormalities. J Invest Dermatol 2003, 120:456-464.
6. Lubbe J, Pournaras C C, Saurat J H. Eczema herpeticum during treatment of atopic dermatitis with 0.1% tacrolimus ointment. Dermatology 2000, 201:249-251.
7. Lerbaek A, Agner T. Facial eruption of molluscum contagiosum during topical treatment of atopic dermatitis with tacrolimus. Br J Dermatol 2004, 150:1210-1211.
8. Goksugur N, Ozbostanci B, Goksugur S B. Molluscum contagiosum infection associated with pimecrolimus use in pityriasis alba. Pediatr Dermatol 2007, 24:E63-65.
9. Rodriguez-Orozco A R, Ruiz-Reyes H, Marin-Hernandez D. Safety of topical tacrolimus and pimecrolimus in children with atopic dermatitis. Rev Alerg Mex 2005, 52:171-176.
10. Lubbe J. Topical tacrolimus for atopic dermatitis: euphoria and vigilance. Dermatology 2001, 203:1-2.
11. Menon G K, Feingold K R, Elias P M. Lamellar body secretory response to barrier disruption. J Invest Dermatol 1992, 98:279-289.
12. Lee S H, Elias P M, Proksch E, Menon G K, Mao-Quiang M, Feingold K R. Calcium and potassium are important regulators of barrier homeostasis in murine epidermis. J Clin Invest 1992, 89:530-538.
13. Feingold K R. Thematic review series: skin lipids. The role of epidermal lipids in cutaneous permeability barrier homeostasis. J Lipid Res 2007, 48:2531-2546.
14. Proksch E, Brandner J M, Jensen J M. The skin: an indispensable barrier. Exp Dermatol 2008, 17:1063-1072.
15. Harris I R, Farrell A M, Grunfeld C, Holleran W M, Elias P M, Feingold K R. Permeability barrier disruption coordinately regulates mRNA levels for key enzymes of cholesterol, fatty acid, and ceramide synthesis in the epidermis. J Invest Dermatol 1997, 109:783-787.
16. Oren A, Ganz T, Liu L, Meerloo T. In human epidermis, beta-defensin 2 is packaged in lamellar bodies. Exp Mol Pathol 2003, 74:180-182.
17. Braff M H, Di Nardo A, Gallo R L. Keratinocytes store the antimicrobial peptide cathelicidin in lamellar bodies. J Invest Dermatol 2005, 124:394-400.
18. Aberg K M, Radek K A, Choi E H. Psychological stress downregulates epidermal antimicrobial peptide expression and increases severity of cutaneous infections in mice. J Clin Invest 2007, 117:3339-3349.
19. Elias P M, Steinhoff M. " Outside-to-inside" (and now back to " outside" ) pathogenic mechanisms in atopic dermatitis. J Invest Dermatol 2008, 128:1067-1070.
20. Elias P M, Choi E H. Interactions among stratum corneum defensive functions. Exp Dermatol 2005, 14:719-726.
21. Aberg K M, Man M Q, Gallo R L. Co-regulation and interdependence of the mammalian epidermal permeability and antimicrobial barriers. J Invest Dermatol 2008, 128:917-925.
22. Hong S P, Kim M J, Jung M Y. Biopositive effects of low-dose UVB on epidermis: coordinate upregulation of antimicrobial peptides and permeability barrier reinforcement. J Invest Dermatol 2008, 128:2880-2887.
23. Sheu H M, Lee J Y, Chai C Y, Kuo K W. Depletion of stratum corneum intercellular lipid lamellae and barrier function abnormalities after long-term topical corticosteroids. Br J Dermatol 1997, 136:884-890.
24. Park H Y, Youm J K, Kwon M J, Park B D, Lee S H, Choi E H. K6PC-5, a novel sphingosine kinase activator, improves long-term ultraviolet light-exposed aged murine skin. Exp Dermatol 2008, 17:829-836.
25. Greenspan P, Gutman R L. Detection by nile red of agarose gel electrophoresed native and modified low density lipoprotein. Electrophoresis 1993, 14:65-68.
26. Choi E H, Brown B E, Crumrine D. Mechanisms by which psychologic stress alters cutaneous permeability barrier homeostasis and stratum corneum integrity. J Invest Dermatol 2005, 124:587-595.
27. Elias P M, Crumrine D, Rassner U. Basis for abnormal desquamation and permeability barrier dysfunction in RXLI. J Invest Dermatol 2004, 122:314-319.
28. Levi K, Baxter J, Meldrum H, Misra M, Pashkovski E, Dauskardt R H. Effect of corneodesmosome degradation on the intercellular delamination of human stratum corneum. J Invest Dermatol 2008, 128:2345-2347.
29. Wood L C, Jackson S M, Elias P M, Grunfeld C, Feingold K R. Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 1992, 90:482-487.
30. Nickoloff B J, Naidu Y. Perturbation of epidermal barrier function correlates with initiation of cytokine cascade in human skin. J Am Acad Dermatol 1994, 30:535-546.
31. Ye J, Garg A, Calhoun C, Feingold K R, Elias P M, Ghadially R. Alterations in cytokine regulation in aged epidermis: implications for permeability barrier homeostasis and inflammation. I. IL-1 gene family. Exp Dermatol 2002, 11:209-216.
32. Barland C O, Zettersten E, Brown B S, Ye J, Elias P M, Ghadially R. Imiquimod-induced interleukin-1 alpha stimulation improves barrier homeostasis in aged murine epidermis. J Invest Dermatol 2004, 122:330-336.
33. Paller A, Eichenfield L F, Leung D Y, Stewart D, Appell M. A 12-week study of tacrolimus ointment for the treatment of atopic dermatitis in pediatric patients. J Am Acad Dermatol 2001, 44:S47-57.
34. Pournaras C C, Lubbe J, Saurat J H. Staphylococcal colonization in atopic dermatitis treatment with topical tacrolimus (Fk506). J Invest Dermatol 2001, 116:480-481.
35. Ashcroft D M, Dimmock P, Garside R, Stein K, Williams H C. Efficacy and tolerability of topical pimecrolimus and tacrolimus in the treatment of atopic dermatitis: meta-analysis of randomised controlled trials. BMJ 2005, 330:516.
36. Proksch E, Folster-Holst R, Jensen J M. Skin barrier function, epidermal proliferation and differentiation in eczema. J Dermatol Sci 2006, 43:159-169.
37. Goldfeld A E, Tsai E, Kincaid R. Calcineurin mediates human tumor necrosis factor alpha gene induction in stimulated T and B cells. J Exp Med 1994, 180:763-768.
38. Rao A, Luo C, Hogan P G. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 1997, 15:707-747.
39. Vigil S V, de Liz R, Medeiros Y S, Frode T S. Efficacy of tacrolimus in inhibiting inflammation caused by carrageenan in a murine model of air pouch. Transpl Immunol 2008, 19:25-29.
40. Wood L C, Feingold K R, Sequeira-Martin S M, Elias P M, Grunfeld C. Barrier function coordinately regulates epidermal IL-1 and IL-1 receptor antagonist mRNA levels. Exp Dermatol 1994, 3:56-60.
41. Elias P M, Ansel J C, Woods L D, Feingold K R. Signaling networks in barrier homeostasis. The mystery widens. Arch Dermatol 1996, 132:1505-1506.
42. Jensen J M, Schutze S, Forl M, Kronke M, Proksch E. Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier. J Clin Invest 1999, 104:1761-1770.
43. Harris I R, Farrell A M, Holleran W M. Parallel regulation of sterol regulatory element binding protein-2 and the enzymes of cholesterol and fatty acid synthesis but not ceramide synthesis in cultured human keratinocytes and murine epidermis. J Lipid Res 1998, 39:412-422.
44. Gierens H, Nauck M, Roth M. Interleukin-6 stimulates LDL receptor gene expression via activation of sterol-responsive and Sp1 binding elements. Arterioscler Thromb Vasc Biol 2000, 20:1777-1783.
45. Liu A Y, Destoumieux D, Wong A V. Human beta-defensin-2 production in keratinocytes is regulated by interleukin-1, bacteria, and the state of differentiation. J Invest Dermatol 2002, 118:275-281.
46. Man M M, Feingold K R, Thornfeldt C R, Elias P M. Optimization of physiological lipid mixtures for barrier repair. J Invest Dermatol 1996, 106:1096-1101.
47. Yang L, Mao-Qiang M, Taljebini M, Elias P M, Feingold K R. Topical stratum corneum lipids accelerate barrier repair after tape stripping, solvent treatment and some but not all types of detergent treatment. Br J Dermatol 1995, 133:679-685.
48. Stuetz A, Grassberger M, Meingassner J G. Pimecrolimus (Elidel, SDZ ASM 981)--preclinical pharmacologic profile and skin selectivity. Semin Cutan Med Surg 2001, 20:233-241.
49. Simon G A, Maibach H I. Relevance of hairless mouse as an experimental model of percutaneous penetration in man. Skin Pharmacol Appl Skin Physiol 1998, 11:80-86.