Early-life regional and temporal variation in filaggrin-derived natural moisturizing factor, filaggrin-processing enzyme activity, corneocyte phenotypes and plasmin activity: implications for atopic dermatitis

British Journal of Dermatology

Volumn 179, Issue 2, 2018, Pages 431-441

  McAleer, M A ^a   Jakasa, I ^b   Raj, N ^c   O'Donnell, C P F ^d   Lane, M E ^c   Rawlings, A V ^c   Voegeli, R ^e   McLean, W H I ^f   Kezic, S ^g   Irvine, A D ^a,h  

^a OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^b UNIVERSITY OF ZAGREB   (Croatia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d NATIONAL MATERNITY HOSPITAL   (Ireland)

^e DSM NUTRITIONAL PRODUCTS LTD   (Switzerland)

^f UNIVERSITY OF DUNDEE   (United Kingdom)

^g Amsterdam Public Health research institute   (Netherlands)

^h TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN HYDROLASE; CALPAIN 1; FILAGGRIN; HISTIDINE; PLASMIN; PROTEINASE; UROCANIC ACID; CALPAIN; CAPN1 PROTEIN, HUMAN; CYSTEINE PROTEINASE; INTERMEDIATE FILAMENT PROTEIN;

ARTICLE; ATOPIC DERMATITIS; CHEEK; CHILD; CROSS-SECTIONAL STUDY; ELBOW; ENZYME ACTIVITY; FEMALE; GENOTYPE; HUMAN; HUMAN TISSUE; HUMIDIFIER; INFANT; MAJOR CLINICAL STUDY; MALE; MATURITY; NEWBORN; NOSE; OBSERVATIONAL STUDY; PHENOTYPE; PRESCHOOL CHILD; PRIORITY JOURNAL; SKIN CELL; STRATUM CORNEUM; AGE; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; MUTATION; PATHOLOGY; SKIN;

AGE FACTORS; CALPAIN; CHEEK; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; CYSTEINE ENDOPEPTIDASES; DERMATITIS, ATOPIC; ELBOW; FEMALE; FIBRINOLYSIN; HUMANS; INFANT; INFANT, NEWBORN; INTERMEDIATE FILAMENT PROTEINS; MALE; MUTATION; SKIN;

EID: 85052224602     PISSN: 00070963     EISSN: 13652133     Source Type: Journal    
DOI: 10.1111/bjd.16691     Document Type: Article

References (50)

1. Irvine AD, McLean WH, Leung DY. Filaggrin mutations associated with skin and allergic diseases. N Engl J Med 2011; 365:1315–27
2. Weidinger S, Novak N. Atopic dermatitis. Lancet 2016; 387:1109–22
3. Halkjaer LB, Loland L, Buchvald FF et al. Development of atopic dermatitis during the first 3 years of life: the Copenhagen prospective study on asthma in childhood cohort study in high-risk children. Arch Dermatol 2006; 142:561–6
4. Yamamoto K. Studies on autosensitization dermatitis. Keio J Med 1961; 10:59–78
5. Ludriksone L, Garcia Bartels N, Kanti V et al. Skin barrier function in infancy: a systematic review. Arch Dermatol Res 2014; 306:591–9
6. Stamatas GN, Nikolovski J, Mack MC, Kollias N. Infant skin physiology and development during the first years of life: a review of recent findings based on in vivo studies. Int J Cosmet Sci 2011; 33:17–24
7. Stamatas GN, Nikolovski J, Luedtke MA et al. Infant skin microstructure assessed in vivo differs from adult skin in organization and at the cellular level. Pediatr Dermatol 2010; 27:125–31
8. Hoath SB, Pickens WL, Scarborogh TE et al. Characterisation of vernix caseosa: relevance to stratum corneum biology. In: Stratum Corneum, the Vital Structure (Marks MP, Deveque JL, eds), Cardiff: The Stratum Corneum Group, 2005
9. Kelleher MM, O'Carroll M, Gallagher A et al. Newborn transepidermal water loss values: a reference dataset. Pediatr Dermatol 2013; 30:712–16
10. Sandilands A, Sutherland C, Irvine AD, McLean WH. Filaggrin in the frontline: role in skin barrier function and disease. J Cell Sci 2009; 122:1285–94
11. McAleer MA, Irvine AD. The multifunctional role of filaggrin in allergic skin disease. J Allergy Clin Immunol 2013; 131:280–91
12. Carson CG, Rasmussen MA, Thyssen JP et al. Clinical presentation of atopic dermatitis by filaggrin gene mutation status during the first 7 years of life in a prospective cohort study. PLOS ONE 2012; 7:e48678
13. Kamata Y, Itoh Y, Kajiya A et al. Quantification of neutral cysteine protease bleomycin hydrolase and its localization in rat tissues. J Biochem 2007; 141:69–76
14. Kamata Y, Taniguchi A, Yamamoto M et al. Neutral cysteine protease bleomycin hydrolase is essential for the breakdown of deiminated filaggrin into amino acids. J Biol Chem 2009; 284:12829–36
15. Yamazaki M, Ishidoh K, Suga Y et al. Cytoplasmic processing of human profilaggrin by active mu-calpain. Biochem Biophys Res Commun 1997; 235:652–6
16. Hsu CY, Henry J, Raymond AA et al. Deimination of human filaggrin-2 promotes its proteolysis by calpain 1. J Biol Chem 2011; 286:23222–33
17. Takahashi M, Tezuka T. The content of free amino acids in the stratum corneum is increased in senile xerosis. Arch Dermatol Res 2004; 295:448–52
18. Barrett JG, Scott IR. Pyrrolidone carboxylic acid synthesis in guinea pig epidermis. J Invest Dermatol 1983; 81:122–4
19. DeLapp NW, Dieckman DK. Gamma glutamyl peptidase: a novel enzyme from hairless mouse epidermis. J Invest Dermatol 1988; 90:490–4
20. Rawlings AV. Molecular basis for stratum corneum maturation and moisturization. Br J Dermatol 2014; 171(Suppl. 3):19–28
21. Dapic I, Jakasa I, Yau NLH et al. Evaluation of an HPLC method for the determination of natural moisturizing factors in the human stratum corneum. Anal Lett 2013; 46:2133–44
22. Clements JA, Willemsen NM, Myers SA, Dong Y. The tissue kallikrein family of serine proteases: functional roles in human disease and potential as clinical biomarkers. Crit Rev Clin Lab Sci 2004; 41:265–312
23. Voegeli R, Rawlings AV, Doppler S et al. Profiling of serine protease activities in human stratum corneum and detection of a stratum corneum tryptase-like enzyme. Int J Cosmet Sci 2007; 29:191–200
24. Breternitz M, Flach M, Prässler J et al. Acute barrier disruption by adhesive tapes is influenced by pressure, time and anatomical location: integrity and cohesion assessed by sequential tape stripping. A randomized, controlled study. Br J Dermatol 2007; 156:231–40
25. Sandilands A, Smith FJ, Irvine AD, McLean WH. Filaggrin's fuller figure: a glimpse into the genetic architecture of atopic dermatitis. J Invest Dermatol 2007; 127:1282–4
26. Mohammed D, Matts PJ, Hadgraft J, Lane ME. Variation of stratum corneum biophysical and molecular properties with anatomic site. AAPS J 2012; 14:806–12
27. Voegeli R, Rawlings AV, Doppler S, Schreier T. Increased basal transepidermal water loss leads to elevation of some but not all stratum corneum serine proteases. Int J Cosmet Sci 2008; 30:435–42
28. Mohammed D, Matts PJ, Hadgraft J, Lane ME. Depth profiling of stratum corneum biophysical and molecular properties. Br J Dermatol 2011; 164:957–65
29. Raj N, Voegeli R, Rawlings AV et al. Variation in the activities of late stage filaggrin processing enzymes, calpain-1 and bleomycin hydrolase, together with pyrrolidone carboxylic acid levels, corneocyte phenotypes and plasmin activities in non-sun exposed and sun-exposed facial stratum corneum of different ethnicities. Int J Cosmet Sci 2016; 38:567–75
30. Visscher MO, Utturkar R, Pickens WL et al. Neonatal skin maturation–vernix caseosa and free amino acids. Pediatr Dermatol 2011; 28:122–32
31. Chittock J, Cooke A, Lavender T et al. Development of stratum corneum chymotrypsin-like protease activity and natural moisturizing factors from birth to 4 weeks of age compared with adults. Br J Dermatol 2016; 175:173–20
32. Scott IR, Harding CR. Filaggrin breakdown to water binding compounds during development of the rat stratum corneum is controlled by the water activity of the environment. Dev Biol 1986; 115:84–92
33. Kennedy EA, Connolly J, Hourihane JO et al. Skin microbiome before development of atopic dermatitis: Early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J Allergy Clin Immunol 2017; 139:166–72
34. Gibbs NK, Norval M. Urocanic acid in the skin: a mixed blessing? J Invest Dermatol 2011; 131:14–17
35. Kuroda Y, Ito M, Ogawa T et al. A new sensitive method for assay of histidase in human skin and detection of heterozygotes for histidinemia. Clin Chim Acta 1979; 96:139–44
36. Fluhr JW, Darlenski R, Lachmann N et al. Infant epidermal skin physiology: adaptation after birth. Br J Dermatol 2012; 166:483–90
37. Takeda A, Higuchi D, Yamamoto T et al. Purification and characterization of bleomycin hydrolase, which represents a new family of cysteine proteases, from rat skin. J Biochem 1996; 119:29–36
38. Takeda A, Nonaka M, Ishikawa A, Higuchi D. Immunohistochemical localization of the neutral cysteine protease bleomycin hydrolase in human skin. Arch Dermatol Res 1999; 291:238–40
39. Schwartz DR, Homanics GE, Hoyt DG et al. The neutral cysteine protease bleomycin hydrolase is essential for epidermal integrity and bleomycin resistance. Proc Natl Acad Sci USA 1999; 96:4680–5
40. Raj N, Voegeli R, Rawlings AV et al. Variation in stratum corneum protein content as a function of anatomical site and ethnic group. Int J Cosmet Sci 2016; 38:224–31
41. Kashibuchi N, Hirai Y, O'Goshi K, Tagami H. Three-dimensional analyses of individual corneocytes with atomic force microscope: morphological changes related to age, location and to the pathologic skin conditions. Skin Res Technol 2002; 8:203–11
42. Tagami H. Location-related differences in structure and function of the stratum corneum with special emphasis on those of the facial skin. Int J Cosmet Sci 2008; 30:413–34
43. Strid J, Hourihane J, Kimber I et al. Disruption of the stratum corneum allows potent epicutaneous immunization with protein antigens resulting in a dominant systemic Th2 response. Eur J Immunol 2004; 34:2100–9
44. Strid J, Hourihane J, Kimber I et al. Epicutaneous exposure to peanut protein prevents oral tolerance and enhances allergic sensitization. Clin Exp Allergy 2005; 35:757–66
45. Bartnikas LM, Gurish MF, Burton OT et al. Epicutaneous sensitization results in IgE-dependent intestinal mast cell expansion and food-induced anaphylaxis. J Allergy Clin Immunol 2013; 131:e1–6
46. Brough HA, Simpson A, Makinson K et al. Peanut allergy: effect of environmental peanut exposure in children with filaggrin loss-of-function mutations. J Allergy Clin Immunol 2014; 134:e1
47. Fallon PG, Sasaki T, Sandilands A et al. A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming. Nat Genet 2009; 41:602–8
48. Horimukai K, Morita K, Narita M et al. Application of moisturizer to neonates prevents development of atopic dermatitis. J Allergy Clin Immunol 2014; 134:e6
49. Simpson EL, Chalmers JR, Hanifin JM et al. Emollient enhancement of the skin barrier from birth offers effective atopic dermatitis prevention. J Allergy Clin Immunol 2014; 134:818–23
50. Brown SJ, Kroboth K, Sandilands A et al. Intragenic copy number variation within filaggrin contributes to the risk of atopic dermatitis with a dose-dependent effect. J Invest Dermatol 2012; 132:98–104