Local burn injury impairs epithelial permeability and antimicrobial peptide barrier function in distal unburned skin

Critical Care Medicine

Volumn 42, Issue 6, 2014, Pages

  Plichta, Jennifer K ^a   Droho, Steve ^a   Curtis, Brenda J ^a   Patel, Parita ^a   Gamelli, Richard L ^a   Radek, Katherine A ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Antimicrobial peptides; burn injury; donor skin; lipids; permeability barrier

Indexed keywords

ADENOSINE PHOSPHATE; ENZYME; LIPID SYNTHESIS ENZYME; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEINASE; SKIN LIPID; SODIUM CHLORIDE; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; BURN; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEHYDRATION; DISTAL UNBURNED SKIN; ENZYME ACTIVITY; EPITHELIAL BARRIER FUNCTION; LIPOGENESIS; LUNG; MALE; MICROBIAL GROWTH; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCALD; SECONDARY INFECTION; SKIN; SKIN EPITHELIUM; SKIN FUNCTION; SKIN PERMEABILITY; SKIN WATER LOSS; TRAUMATIC BURN INJURY; WATER LOSS; WOUND HEALING;

ANALYSIS OF VARIANCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL INFECTIONS; BURNS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DEHYDRATION; EPIDERMIS; MALE; MEMBRANE LIPIDS; MICE; MICE, INBRED C57BL; PEPTIDE HYDROLASES; PERMEABILITY; POLYMERASE CHAIN REACTION; SKIN; WOUND HEALING;

EID: 84901488936     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0000000000000309     Document Type: Article

References (58)

1. Molina PE: Neurobiology of the stress response: Contribution of the sympathetic nervous system to the neuroimmune axis in traumatic injury. Shock 2005; 24:3-10
2. Baxter CR: Fluid volume and electrolyte changes of the early postburn period. Clin Plast Surg 1974; 1:693-703
3. Loebl EC, Baxter CR, Curreri PW: The mechanism of erythrocyte destruction in the early post-burn period. Ann Surg 1973; 178:681-686
4. Alexander JW, MacMillan BG, Law E, et al: Treatment of severe burns with widely meshed skin autograft and meshed skin allograft overlay. J Trauma 1981; 21:433-438
5. Phillips TJ, Gilchrest BA: Clinical applications of cultured epithelium. Epithelial Cell Biol 1992; 1:39-46
6. Proksch E, Brandner JM, Jensen JM: The skin: An indispensable barrier. Exp Dermatol 2008; 17:1063-1072
7. Feingold KR, Schmuth M, Elias PM: The regulation of permeability barrier homeostasis. J Invest Dermatol 2007; 127:1574-1576
8. Proksch E, Holleran WM, Menon GK, et al: Barrier function regulates epidermal lipid and DNA synthesis. Br J Dermatol 1993; 128:473-482
9. Hachem JP, Crumrine D, Fluhr J, et al: pH directly regulates epidermal permeability barrier h omeostasis, and stratum corneum integrity/cohesion. J Invest Dermatol 2003; 121:345-353
10. Elias PM: Stratum corneum defensive functions: An integrated view. J Invest Dermatol 2005; 125:183-200
11. Ekanayake-Mudiyanselage S, Aschauer H, Schmook FP, et al: Expression of epidermal keratins and the cornified envelope protein involucrin is influenced by permeability barrier disruption. J Invest De rmatol 1998; 111:517-523
12. Elias PM: The skin barrier as an innate immune element. Semin Immunopathol 2007; 29:3-14
13. Aberg KM, Man MQ, Gallo RL, et al: Co-regulation and interdependence of the mammalian epidermal permeability and antimicrobial barriers. J Invest Dermatol 2008; 128:917-925
14. Caubet C, Jonca N, Brattsand M, et al: Degradat ion of corneodesmosome proteins by two serine proteases of the kallikrein family, SCTE/KLK5/hK5 and SCCE/KLK7/hK7. J Invest Dermatol 2004; 122:1235-1244
15. Yamasaki K, Schauber J, Coda A, et al: Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J 2006; 20:2068-2080
16. Ahrens K, Schunck M, Podda GF, et al: Mechanical and metabolic injury to the skin barrier leads to increased expression of murine beta-defensin-1,-3, and-14. J Invest Dermatol 2011; 131:443-452
17. Dorschner RA, Pestonjamasp VK, Tamakuwala S, et al: Cutaneous inj ury induces the release of cathelicidin anti-microbial peptides active against group A Streptococcus. J Invest Dermatol 2001; 117:91-97
18. Nizet V, Ohtake T, Lauth X, et al: Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 2001; 414:454-457
19. Schauber J, Dorschner RA, Coda AB, et al: Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J Clin Invest 2007; 117:803-811
20. Verga Falzacappa MV, Muckenthaler MU: Hepcidin: Iron-hormone and anti-microbial peptide. Gene 2005; 364:37-44
21. Glä ser R, Harder J, Lange H, et al: Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 2005; 6:57-64
22. Milner SM, Ortega MR: Reduced antimicrobial peptide expression in human burn wounds. Burns 1999; 25:411-413
23. Ortega MR, Ganz T, Milner SM: Human beta defensin is absent in burn blister fluid. Burns 2000; 26:724-726
24. Poindexter BJ, Bhat S, Buja LM, et al: Localization of antimicrobial peptides in normal and burned skin. Burns 2006; 32:402-407
25. Martin-Ezquerra G, Man MQ, Hupe M, et al: Psychological stress regulates antimicrobial peptide expression by both glucocorticoid and betaadrenergic mechanisms. Eur J Dermatol 2011; 21(Suppl 2):48-51
26. Radek KA: Antimicro bial anxiety: The impact of stress on antimicrobial immunity. J Leukoc Biol 2010; 88:263-277
27. Lopez NE, Krzyzaniak M, Costantini TW, et al: Vagal nerve stimulation blocks peritoneal macrophag e inflammatory responsiveness after severe burn injury. Shock 2012; 38:294-300
28. Brattsand M, Stefansson K, Lundh C, et al: A proteolytic cascade of kallikreins in the stratum corneum. J Invest Dermatol 2005; 124:198-203
29. Ganio MS, Gagnon D, Stapleton J, et al: Effect of human skin grafts on whole-body heat loss during exercise heat stress: A case report. J Burn Care Res 2013; 34:e263-e270
30. Harris IR, Farrell AM, Holleran WM, et al: Parallel regulation of sterol regulatory element binding protein-2 and the enzymes of cholesterol and fatty acid synthesis but not ceramid e synthesis in cultured human keratinocytes and murine epidermis. J Lipid Res 1998; 39:412-422
31. Denda M, Fuziwara S, Inoue K: Influx of calcium and chloride ions into epidermal keratinocytes regul ates exocytosis of epidermal lamellar bodies and skin permeability barrier homeostasis. J Invest Dermatol 2003; 121:362-367
32. Elias PM, Nau P, Hanley K, et al: Formation of the epidermal calciu m gradient coincides with key milestones of barrier ontogenesis in the rodent. J Invest Dermatol 1998; 110:399-404
33. Faunce DE, Gregory MS, Kovacs EJ: Effects of acute ethanol exposure on cellular immune responses in a murine model of thermal injury. J Leukoc Biol 1997; 62:733-740
34. Wood LC, Jackson SM, Elias PM, et al: Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 1992; 90:482-487
35. Curtis BJ, Plichta JK, Blatt H, et al: Nicotinic acetylcholine receptor stimulation impairs epidermal permeability barrier function and recovery and modulates cornified envelope proteins. Life Sci 2012; 9 1:1070-1076
36. Radek KA, Elias PM, Taupenot L, et al: Neuroendocrine nicotinic receptor activation increases susceptibility to bacterial infections by suppressing antimicrobial peptide production. Cell H ost Microbe 2010; 7:277-289
37. Peschel A, Jack RW, Otto M, et al: Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based o n modification of membrane lipids with l-lysine. J Exp Med 2001; 193:1067-1076
38. Fowler SD,Greenspan P, Application of Nile red, a fluorescent hydrophobic probe, for the detection of neutral lipid dep osits in tissue sections: Comparison with oil red O, J Histochem Cytochem,1985,33, 833-836
39. Greenspan P, Mayer EP, Fowler SD: Nile red: A selective fluorescent stain for intracellular lipid droplets. J Cell Biol 1985; 100:965-973
40. Menges DA, Ternullo DL, Tan-Wilson AL, et al: Continuous assay of proteases using a microtiter plate fluorescence reader. Anal Biochem 1997; 254:144-147
41. Baroni A, Buommino E, De Gregorio V, et al: Structure and function of the epidermis related to barrier properties. Clin Dermatol 2012; 30:257-262
42. Holleran WM, Man MQ, Gao WN, et al: Sphingolipids are required for mammalian epidermal barrier function. Inhibition of sphingolipid synthesis delays barrier recovery after acute perturbation. J Clin Invest 1991; 88:13 38-1345
43. Harris IR, Farrell AM, Grunfeld C, et al: Permeability barrier disruption coordinately regulates mRNA levels for key enzymes of cholesterol, fatty acid, and ceramide synthesis in the epidermis. J Inve st Dermatol 1997; 109:783-787
44. Jackson SM, Williams ML, Feingold KR, et al: Pathobiology of the stratum corneum. West J Med 1993; 158:279-285
45. Brattsa nd M, Egelrud T: Purification, molecular cloning, and expression of a human stratum corneum trypsin-like serine protease with possible function in desquamation. J Biol Chem 1999; 274:30033-30040
46. Doss M, White MR, Tecle T, et al: Human defensins and LL-37 in mucosal immunity. J Leukoc Biol 2010; 87:79-92
47. Parameswaran GI, Sethi S, Murphy TF: Effects of bacterial infection on airway antimicrobial peptides and proteins in COPD. Chest 2011; 140:611-617
48. Tsai PW, Yang CY, Chang HT, et al: Human antimicrobial peptide LL-37 inhibits adhesion of Candida albicans by inte racting with yeast cell-wall carbohydrates. PLoS One 2011; 6:e17755
49. Lavelle JP, Apodaca G, Meyers SA, et al: Disruption of guinea pig urinary bladder permeability barrier in noninfectious cystitis. Am J Physiol 1998; 274:F205-F214
50. Maestrin i E, Monaco AP, McGrath JA, et al: A molecular defect in loricrin, the major component of the cornified cell envelope, underlies Vohwinkel?s syndrome. Nat Genet 1996; 13:70-77
51. Ishida-Yamamoto A, McGrath JA, Lam H, et al: The molecular pathology of progressive symmetric erythrokeratoderma: A frameshift mutation in the loricrin gene and perturbations in the cornified cell envelope. Am J Hum Genet 1997; 61:5 81-589
52. Jensen JM, Fö lster-Holst R, Baranowsky A, et al: Impaired sphingomyelinase activity and epidermal differentiation in atopic dermatitis. J Invest Dermatol 2004; 122:1423-1431
53. Kim BE, Howell MD, Guttman-Yassky E, et al: TNF-alpha downregulates filaggrin and loricrin through c-Jun N-terminal kinase: Role for TNF-alpha antagonists to improve skin barrier. J Invest Dermatol 2011; 131: 1272-1279
54. Irvine AD, McLean WH, Leung DY: Filaggrin mutations associated with skin and allergic diseases. N Engl J Med 2011; 365:1315-1327
55. Gruber R, Elias P M, Crumrine D, et al: Filaggrin genotype in ichthyosis vulgaris predicts abnormalities in epidermal structure and function. Am J Pathol 2011; 178:2252-2263
56. Kurzen H, Henrich C, Booken D, et al: Functional characterization of the epidermal cholinergic system in vitro. J Invest Dermatol 2006; 126:2458-2472
57. American Burn Association: 2012 National Burn Repository: Report of Data from 2002-2012. Chicago, IL, American Burn Association, 2012
58. Hachem JP, Houben E, Crumrine D, et al: Serine protease signaling of epidermal permeability barrier homeostasis. J Invest Dermatol 2006; 126:2074-2086