The matricellular protein periostin contributes to proper collagen function and is downregulated during skin aging

Journal of Dermatological Science

Volumn 73, Issue 1, 2014, Pages 40-48

  Egbert, M ^a   Ruetze, M ^a,b   Sattler, M ^a   Wenck, H ^a   Gallinat, S ^a   Lucius, R ^b   Weise, J M ^a  

^a BEIERSDORF AG   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

Collagen; Matricellular protein; Periostin; Skin aging

Indexed keywords

COLLAGEN; TRANSCRIPTION FACTOR RUNX2;

ADULT; AGED; ARTICLE; COLLAGEN DEGRADATION; COLLAGEN METABOLISM; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CROSS LINKING; CUTANEOUS PARAMETERS; DERMIS; DOWN REGULATION; ELECTRON MICROSCOPY; FEMALE; FIBER; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; NORMAL HUMAN; PHOTOAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SKIN BIOPSY; SKIN PROTECTION; SKIN STRUCTURE; ULTRAVIOLET IRRADIATION; YOUNG ADULT;

AA2P; BAPN; COLLAGEN; CT; CYCLE THRESHOLD; DHLNL; DIHYDROXYLYSINONORLEUCINE; ECM; EXTRACELLULAR MATRIX; HDF; HHMD; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTIDINOHYDROXYMERODESMOSINE; HLNL; HP; HPLC; HUMAN DERMAL FIBROBLASTS; HYDROXYLYSINONORLEUCINE; HYDROXYLYSYLPYRIDINOLINE; L-ASCORBIC ACID 2-PHOSPHATE SESQUIMAGNESIUM SALT HYDRATE; LOX; LYSYLOXIDASE; MATRICELLULAR PROTEIN; MATRIX METALLOPROTEINASE; MMP; PERIOSTIN; QRT-PCR; QUANTITATIVE REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT HUMAN; RH; SKIN AGING; SKIN DERIVED PRECURSOR; SKP; SOLAR SIMULATED RADIATION; SSR; TEM; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET; UV; Β-AMINOPROPIONITRILE-FUMARATE;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; CELL ADHESION MOLECULES; CELLS, CULTURED; COLLAGEN TYPE I; DOWN-REGULATION; FEMALE; FIBROBLASTS; HOMEOSTASIS; HUMANS; MALE; MIDDLE AGED; RNA INTERFERENCE; SKIN; SKIN AGING; SUNLIGHT; TIME FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1; YOUNG ADULT;

EID: 84890122149     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2013.08.010     Document Type: Article

References (45)

1. Lavker R.M. Structural alterations in exposed and unexposed aged skin. J Invest Dermatol 1979, 73:59-66.
2. Fisher G.J., Kang S., Varani J., Bata-Csorgo Z., Wan Y., Datta S., et al. Mechanisms of photoaging and chronological skin aging. Arch Dermatol 2002, 138:1462-1470.
3. Tang S., Lucius R., Wenck H., Gallinat S., Weise J.M. UV-mediated downregulation of the endocytic collagen receptor, Endo180, contributes to accumulation of extracellular collagen fragments in photoaged skin. J Dermatol Sci 2013, 70:42-48.
4. Bornstein P. Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 1995, 130:503-506.
5. Bornstein P. Matricellular proteins: an overview. J Cell Commun Signal 2009, 3:163-165.
6. Hamilton D.W. Functional role of periostin in development and wound repair: implications for connective tissue disease. J Cell Commun Signal 2008, 2:9-17.
7. Shimazaki M., Nakamura K., Kii I., Kashima T., Amizuka N., Li M., et al. Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 2008, 205:295-303.
8. Oka T., Xu J., Kaiser R.A., Melendez J., Hambleton M., Sargent M.A., et al. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 2007, 101:313-321.
9. Kii I., Nishiyama T., Li M., Matsumoto K., Saito M., Amizuka N., et al. Incorporation of tenascin-C into the extracellular matrix by periostin underlies an extracellular meshwork architecture. J Biol Chem 2010, 285:2028-2039.
10. Rios H., Koushik S.V., Wang H., Wang J., Zhou H.M., Lindsley A., et al. periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 2005, 25:11131-11144.
11. Zhou H.M., Wang J., Elliott C., Wen W., Hamilton D.W., Conway S.J. Spatiotemporal expression of periostin during skin development and incisional wound healing: lessons for human fibrotic scar formation. J Cell Commun Signal 2010, 4:99-107.
12. Nishiyama T., Kii I., Kashima T.G., Kikuchi Y., Ohazama A., Shimazaki M., et al. Delayed re-epithelialization in periostin-deficient mice during cutaneous wound healing. PLoS One 2011, 6:e18410.
13. Norris R.A., Damon B., Mironov V., Kasyanov V., Ramamurthi A., Moreno-Rodriguez R., et al. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 2007, 101:695-711.
14. Takayama G., Arima K., Kanaji T., Toda S., Tanaka H., Shoji S., et al. Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 2006, 118:98-104.
15. Kii I., Amizuka N., Minqi L., Kitajima S., Saga Y., Kudo A. Periostin is an extracellular matrix protein required for eruption of incisors in mice. Biochem Biophys Res Commun 2006, 342:766-772.
16. Li G., Jin R., Norris R.A., Zhang L., Yu S., Wu F., et al. Periostin mediates vascular smooth muscle cell migration through the integrins alphavbeta3 and alphavbeta5 and focal adhesion kinase (FAK) pathway. Atherosclerosis 2010, 208:358-365.
17. Maruhashi T., Kii I., Saito M., Kudo A. Interaction between periostin and BMP-1 promotes proteolytic activation of lysyl oxidase. J Biol Chem 2010, 285:13294-13303.
18. Byers P.H., Siegel R.C., Holbrook K.A., Narayanan A.S., Bornstein P., Hall J.G. X-linked cutis laxa: defective cross-link formation in collagen due to decreased lysyl oxidase activity. N Engl J Med 1980, 303:61-65.
19. Yamauchi M., Prisayanh P., Haque Z., Woodley D.T. Collagen cross-linking in sun-exposed and unexposed sites of aged human skin. J Invest Dermatol 1991, 97:938-941.
20. Norris R.A., Moreno-Rodriguez R., Hoffman S., Markwald R.R. The many facets of the matricelluar protein periostin during cardiac development, remodeling, and pathophysiology. J Cell Commun Signal 2009, 3:275-286.
21. Stab F., Wolber R., Blatt T., Keyhani R., Sauermann G. Topically applied antioxidants in skin protection. Methods Enzymol 2000, 319:465-478.
22. Ruetze M., Knauer T., Gallinat S., Wenck H., Achterberg V., Maerz A., et al. A novel niche for skin derived precursors in non-follicular skin. J Dermatol Sci 2013, 69:132-139.
23. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
24. Tang S., Lucius R., Wenck H., Gallinat S., Weise J.M. UV-mediated downregulation of the endocytic collagen receptor. Endo180, contributes to accumulation of extracellular collagen fragments in photoaged skin. J Dermatol Sci 2013, 70:42-48.
25. Lutz V., Sattler M., Gallinat S., Wenck H., Poertner R., Fischer F. Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence. Skin Res Technol 2012, 18:168-179.
26. Avery N.C., Sims T.J., Bailey A.J. quantitative determination of collagen cross-links. Methods Mol Biol 2009, 522:103-121.
27. Rios H.F., Ma D., Xie Y., Giannobile W.V., Bonewald L.F., Conway S.J., et al. Periostin is essential for the integrity and function of the periodontal ligament during occlusal loading in mice. J Periodontol 2008, 79:1480-1490.
28. Marionnet C., Pierrard C., Vioux-Chagnoleau C., Sok J., Asselineau D., Bernerd F. Interactions between fibroblasts and keratinocytes in morphogenesis of dermal epidermal junction in a model of reconstructed skin. J Invest Dermatol 2006, 126:971-979.
29. Canty E.G., Kadler K.E. Procollagen trafficking processing and fibrillogenesis. J Cell Sci 2005, 118:1341-1353.
30. Canty E.G., Kadler K.E. Collagen fibril biosynthesis in tendon: a review and recent insights. Comp Biochem Physiol A Mol Integr Physiol 2002, 133:979-985.
31. Crawford S.E., Stellmach V., Murphy-Ullrich J.E., Ribeiro S.M., Lawler J., Hynes R.O., et al. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 1998, 93:1159-1170.
32. Kyriakides T.R., Zhu Y.H., Smith L.T., Bain S.D., Yang Z., Lin M.T., et al. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol 1998, 140:419-430.
33. Bradshaw A.D., Puolakkainen P., Dasgupta J., Davidson J.M., Wight T.N., Helene Sage E. SPARC-null mice display abnormalities in the dermis characterized by decreased collagen fibril diameter and reduced tensile strength. J Invest Dermatol 2003, 120:949-955.
34. Sullivan M.M., Barker T.H., Funk S.E., Karchin A., Seo N.S., Hook M., et al. Matricellular hevin regulates decorin production and collagen assembly. J Biol Chem 2006, 281:27621-27632.
35. Mao J.R., Taylor G., Dean W.B., Wagner D.R., Afzal V., Lotz J.C., et al. Tenascin-X deficiency mimics Ehlers-Danlos syndrome in mice through alteration of collagen deposition. Nat Genet 2002, 30:421-425.
36. Quan T., He T., Shao Y., Lin L., Kang S., Voorhees J.J., et al. Elevated cysteine-rich 61 mediates aberrant collagen homeostasis in chronologically aged and photoaged human skin. Am J Pathol 2006, 169:482-490.
37. Mo F.E., Muntean A.G., Chen C.C., Stolz D.B., Watkins S.C., Lau L.F. CYR61 (CCN1) is essential for placental development and vascular integrity. Mol Cell Biol 2002, 22:8709-8720.
38. Duncan M.R., Frazier K.S., Abramson S., Williams S., Klapper H., Huang X., et al. Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: down-regulation by cAMP. FASEB J 1999, 13:1774-1786.
39. Ivkovic S., Yoon B.S., Popoff S.N., Safadi F.F., Libuda D.E., Stephenson R.C., et al. Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 2003, 130:2779-2791.
40. Yang L., Serada S., Fujimoto M., Terao M., Kotobuki Y., Kitaba S., et al. Periostin facilitates skin sclerosis via PI3K/Akt dependent mechanism in a mouse model of scleroderma. PLoS One 2012, 7(7):e41994.
41. Pischon N., Babakhanlou-Chase H., Darbois L., Ho W.B., Brenner M.C., Kessler E., et al. A procollagen C-proteinase inhibitor diminishes collagen and lysyl oxidase processing but not collagen cross-linking in osteoblastic cultures. J Cell Physiol 2005, 203:111-117.
42. Kadler K.E., Hill A., Canty-Laird E.G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 2008, 20:495-501.
43. Sun M., Chen S., Adams S.M., Florer J.B., Liu H., Kao W.W., et al. Collagen V is a dominant regulator of collagen fibrillogenesis: dysfunctional regulation of structure and function in a corneal-stroma-specific Col5a1-null mouse model. J Cell Sci 2011, 124:4096-4105.
44. Tan K., Lawler J. The interaction of thrombospondins with extracellular matrix proteins. J Cell Commun Signal 2009, 3:177-187.
45. Danielson K.G., Baribault H., Holmes D.F., Graham H., Kadler K.E., Iozzo R.V. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 1997, 136:729-743.