Solar Ultraviolet Irradiation Induces Decorin Degradation in Human Skin Likely via Neutrophil Elastase

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Li, Yong ^a   Xia, Wei ^a   Liu, Ying ^a   Remmer, Henriette A ^b   Voorhees, John ^a   Fisher, Gary J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; DECORIN; INTERSTITIAL COLLAGENASE; LEUKOCYTE ELASTASE; LEUKOCYTE ELASTASE INHIBITOR; PROTEINASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR WEIGHT; NEUTROPHIL CHEMOTAXIS; POLYMORPHONUCLEAR CELL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; RADIATION EXPOSURE; SKIN; SOLAR RADIATION; ULTRAVIOLET IRRADIATION;

ADULT; DECORIN; FEMALE; FIBRILLAR COLLAGENS; HUMANS; LEUKOCYTE ELASTASE; LEUKOCYTES, MONONUCLEAR; MALE; MATRIX METALLOPROTEINASE 1; PROTEIN BINDING; PROTEOLYSIS; SKIN; ULTRAVIOLET RAYS; YOUNG ADULT;

EID: 84883433902     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072563     Document Type: Article

References (46)

1. Fisher GJ (2005) The pathophysiology of photoaging of the skin. Cutis 75: 5-8; discussion 8-9.
2. Fisher GJ, Kang S, Varani J, Bata-Csorgo Z, Wan Y, et al. (2002) Mechanisms of photoaging and chronological skin aging. Arch Dermatol 138: 1462-1470.
3. Lauer-Fields JL, Juska D, Fields GB, (2002) Matrix metalloproteinases and collagen catabolism. Biopolymers 66: 19-32.
4. Quan T, Qin Z, Xia W, Shao Y, Voorhees JJ, et al. (2009) Matrix-degrading metalloproteinases in photoaging. J Investig Dermatol Symp Proc 14: 20-24.
5. Fisher GJ, Choi HC, Bata-Csorgo Z, Shao Y, Datta S, et al. (2001) Ultraviolet irradiation increases matrix metalloproteinase-8 protein in human skin in vivo. J Invest Dermatol 117: 219-226.
6. Kubes P, Smith R, Grisham MD, Granger DN, (1993) Neutrophil-mediated proteolysis. Differential roles for cathepsin G and elastase. Inflammation 17: 321-332.
7. Schornagel IJ, Sigurdsson V, Nijhuis EH, Bruijnzeel-Koomen CA, Knol EF, (2004) Decreased neutrophil skin infiltration after UVB exposure in patients with polymorphous light eruption. J Invest Dermatol 123: 202-206.
8. Janoff A, (1985) Elastase in tissue injury. Annu Rev Med 36: 207-216.
9. Carrino DA, Calabro A, Darr AB, Dours-Zimmermann MT, Sandy JD, et al. (2011) Age-related differences in human skin proteoglycans. Glycobiology 21: 257-268.
10. Gilchrest BA, (1982) Age-associated changes in the skin. J Am Geriatr Soc 30: 139-143.
11. Reed CC, Iozzo RV, (2002) The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconj J 19: 249-255.
12. Iozzo RV, Schaefer L, (2010) Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J 277: 3864-3875.
13. Neill T, Schaefer L, Iozzo RV, (2012) Decorin: a guardian from the matrix. Am J Pathol 181: 380-387.
14. Fleischmajer R, Fisher LW, MacDonald ED, Jacobs L Jr, Perlish JS, et al. (1991) Decorin interacts with fibrillar collagen of embryonic and adult human skin. J Struct Biol 106: 82-90.
15. Scott JE, (1992) Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J 6: 2639-2645.
16. Scott JE, (1996) Proteodermatan and proteokeratan sulfate (decorin, lumican/fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry 35: 8795-8799.
17. Beavan LA, Quentin-Hoffmann E, Schonherr E, Snigula F, Leroy JG, et al. (1993) Deficient expression of decorin in infantile progeroid patients. J Biol Chem 268: 9856-9862.
18. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, et al. (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743.
19. Geng Y, McQuillan D, Roughley PJ, (2006) SLRP interaction can protect collagen fibrils from cleavage by collagenases. Matrix Biol 25: 484-491.
20. Orgel JP, Eid A, Antipova O, Bella J, Scott JE, (2009) Decorin core protein (decoron) shape complements collagen fibril surface structure and mediates its binding. PLoS One 4: e7028.
21. Stuart K, Paderi J, Snyder PW, Freeman L, Panitch A, (2011) Collagen-binding peptidoglycans inhibit MMP mediated collagen degradation and reduce dermal scarring. PLoS One 6: e22139.
22. Carrino DA, Sorrell JM, Caplan AI, (2000) Age-related changes in the proteoglycans of human skin. Arch Biochem Biophys 373: 91-101.
23. Iozzo RV, (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67: 609-652.
24. Lochner K, Gaemlich A, Sudel KM, Venzke K, Moll I, et al. (2007) Expression of decorin and collagens I and III in different layers of human skin in vivo: a laser capture microdissection study. Biogerontology 8: 269-282.
25. Werth BB, Bashir M, Chang L, Werth VP, (2011) Ultraviolet irradiation induces the accumulation of chondroitin sulfate, but not other glycosaminoglycans, in human skin. PLoS One 6: e14830.
26. Korkmaz B, Moreau T, Gauthier F, (2008) Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions. Biochimie 90: 227-242.
27. Kapui Z, Varga M, Urban-Szabo K, Mikus E, Szabo T, et al. (2003) Biochemical and pharmacological characterization of 2-(9-(2-piperidinoethoxy)-4-oxo-4H-pyrido[1,2-a]pyrimidin-2-yloxymethyl)-4-(1-methylethyl)-6-methoxy-1,2-benzisothiazol-3(2H)-one-1,1-dioxide (SSR69071), a novel, orally active elastase inhibitor. J Pharmacol Exp Ther 305: 451-459.
28. Cabello-Verrugio C, Santander C, Cofre C, Acuna MJ, Melo F, et al. (2012) The internal region leucine-rich repeat 6 of decorin interacts with low density lipoprotein receptor-related protein-1, modulates transforming growth factor (TGF)-beta-dependent signaling, and inhibits TGF-beta-dependent fibrotic response in skeletal muscles. J Biol Chem 287: 6773-6787.
29. Honardoust D, Ding J, Varkey M, Shankowsky HA, Tredget EE, (2012) Deep dermal fibroblasts refractory to migration and decorin-induced apoptosis contribute to hypertrophic scarring. J Burn Care Res 33: 668-677.
30. Marchica CL, Pinelli V, Borges M, Zummer J, Narayanan V, et al. (2011) A role for decorin in a murine model of allergen-induced asthma. Am J Physiol Lung Cell Mol Physiol 300: L863-873.
31. Mohan RR, Tovey JC, Gupta R, Sharma A, Tandon A, (2011) Decorin biology, expression, function and therapy in the cornea. Curr Mol Med 11: 110-128.
32. Moreth K, Iozzo RV, Schaefer L, (2012) Small leucine-rich proteoglycans orchestrate receptor crosstalk during inflammation. Cell Cycle 11: 2084-2091.
33. Zhang C, Tan CK, McFarlane C, Sharma M, Tan NS, et al. (2012) Myostatin-null mice exhibit delayed skin wound healing through the blockade of transforming growth factor-beta signaling by decorin. Am J Physiol Cell Physiol 302: C1213-1225.
34. Boivin WA, Shackleford M, Vanden Hoek A, Zhao H, Hackett TL, et al. (2012) Granzyme B cleaves decorin, biglycan and soluble betaglycan, releasing active transforming growth factor-beta1. PLoS One 7: e33163.
35. Hiebert PR, Boivin WA, Abraham T, Pazooki S, Zhao H, et al. (2011) Granzyme B contributes to extracellular matrix remodeling and skin aging in apolipoprotein E knockout mice. Exp Gerontol 46: 489-499.
36. Imai K, Hiramatsu A, Fukushima D, Pierschbacher MD, Okada Y, (1997) Degradation of decorin by matrix metalloproteinases: identification of the cleavage sites, kinetic analyses and transforming growth factor-beta1 release. Biochem J 322 (Pt 3): 809-814.
37. Winchester B, (2005) Lysosomal metabolism of glycoproteins. Glycobiology 15: 1R-15R.
38. Flannery CR, (2006) Usurped SLRPs: novel arthritis biomarkers exposed by catabolism of small leucine-rich proteoglycans? Arthritis Res Ther 8: 106.
39. Melrose J, Fuller ES, Roughley PJ, Smith MM, Kerr B, et al. (2008) Fragmentation of decorin, biglycan, lumican and keratocan is elevated in degenerate human meniscus, knee and hip articular cartilages compared with age-matched macroscopically normal and control tissues. Arthritis Res Ther 10: R79.
40. Waddington RJ, Embery G, Smith AJ, (1998) Immunochemical detection of the proteoglycans decorin and biglycan in human gingival crevicular fluid from sites of advanced periodontitis. Arch Oral Biol 43: 287-295.
41. Codriansky KA, Quintanilla-Dieck MJ, Gan S, Keady M, Bhawan J, et al. (2009) Intracellular degradation of elastin by cathepsin K in skin fibroblasts-a possible role in photoaging. Photochem Photobiol 85: 1356-1363.
42. Li Y, Liu Y, Xu Y, Voorhees JJ, Fisher GJ, (2010) UV irradiation induces Snail expression by AP-1 dependent mechanism in human skin keratinocytes. J Dermatol Sci 60: 105-113.
43. Clark RA, Nauseef WM (2001) Isolation and functional analysis of neutrophils. Curr Protoc Immunol Chapter 7: Unit 7 23.
44. Fisher GJ, Quan T, Purohit T, Shao Y, Cho MK, et al. (2009) Collagen fragmentation promotes oxidative stress and elevates matrix metalloproteinase-1 in fibroblasts in aged human skin. Am J Pathol 174: 101-114.
45. Kuwaba K, Kobayashi M, Nomura Y, Irie S, Koyama Y, (2001) Elongated dermatan sulphate in post-inflammatory healing skin distributes among collagen fibrils separated by enlarged interfibrillar gaps. Biochem J 358: 157-163.
46. Scott JE, (1991) Proteoglycan: collagen interactions in connective tissues. Ultrastructural, biochemical, functional and evolutionary aspects. Int J Biol Macromol 13: 157-161.