Biological mechanisms underlying the ultraviolet radiation-induced formation of skin wrinkling and sagging I: Reduced skin elasticity, highly associated with enhanced dermal elastase activity, triggers wrinkling and sagging

International Journal of Molecular Sciences

Volumn 16, Issue 4, 2015, Pages 7753-7775

  Imokawa, Genji ^a   Ishida, Koichi ^b  

^a CHUBU UNIVERSITY   (Japan)

^b KAO CORPORATION   (Japan)

Author keywords

Elastase; Elastin fiber network; Skin elasticity; Ultraviolet A; Ultraviolet B

Indexed keywords

ELASTASE; ELASTATINAL; GELATINASE A; GELATINASE B; LEUPEPTIN; MATRIX METALLOPROTEINASE; PEPSTATIN; PHOSPHORAMIDON; PROTEINASE; PANCREATIC ELASTASE;

AGE; CONTROLLED CLINICAL TRIAL (TOPIC); CUTANEOUS PARAMETERS; DERMIS; ELASTIC FIBER; ELASTOLYSIS; ENZYME ACTIVITY; GINGER; HUMAN; NONHUMAN; OVARIECTOMY; REVIEW; SAGGING; SCANNING ELECTRON MICROSCOPY; SKIN ELASTICITY; SKINFOLD THICKNESS; ULTRAVIOLET IRRADIATION; ULTRAVIOLET RADIATION; WRINKLE; ADVERSE EFFECTS; ANIMAL; ELASTICITY; FIBROBLAST; METABOLISM; PATHOLOGY; PHYSIOLOGY; RADIATION RESPONSE;

ANIMALIA; RATTUS;

ANIMALS; DERMIS; ELASTICITY; FIBROBLASTS; HUMANS; PANCREATIC ELASTASE; SKIN AGING; ULTRAVIOLET RAYS;

EID: 84927596917     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16047753     Document Type: Review

References (56)

1. Slominski, A.T.; Zmijewski, M.A.; Skobowiat, C.; Zbytek, B.; Slominski, R.M.; Steketee, J.D. Sensing the environment: Regulation of local and global homeostasis by the skin's neuroendocrine system. Adv. Anat. Embryol. Cell Biol. 2012, 212, 1-115.
2. Slominski, A.T.; Zmijewski, M.A.; Zbytek, B.; Tobin, D.J.; Theoharides, T.C.; Rivier, J. Key role of CRF in the skin stress response system. Endocr. Rev. 2013, 34, 827-884.
3. Skobowiat, C.; Dowdy, J.C.; Sayre, R.M.; Tuckey, R.C.; Slominski, A. Cutaneous hypothalamic-pituitary-adrenal axis homolog: Regulation by ultraviolet radiation. Am. J. Physiol. Endocrinol. Metab. 2011, 301, E484-E493.
4. Skobowiat, C.; Sayre, R.M.; Dowdy, J.C.; Slominski, A.T. Ultraviolet radiation regulates cortisol activity in a waveband-dependent manner in human skin ex vivo. Br. J. Dermatol. 2013, 168, 595-601.
5. Slominski, A.T.; Kleszczyński, K.; Semak, I.; Janjetovic, Z.; Zmijewski, M.A.; Kim, T.K.; Slominski, R.M.; Reiter, R.J.; Fischer, T.W. Local melatoninergic system as the protector of skin integrity. Int. J. Mol. Sci. 2014, 15, 17705-17732.
6. Takema, Y.; Sakaino, Y.; Imokawa, G. Age-related changes in the mechanical properties and thickness of human facial skin. Br. J. Dermatol. 1994, 131, 641-648.
7. Takema, Y.; Yorimoto, Y.; Kawai, M. The relationship between age-related changes in the physical properties and development of wrinkles in human facial skin. J. Soc. Cosmet. Chem. 1995, 46, 163-173.
8. Tsukahara, K.; Takema, Y.; Kazama, H.; Yorimoto, Y.; Fujimura, T.; Moriwaki, S.; Kitahara, T.; Kawai, M.; Imokawa, G. A photographic scale for the assessment of human facial wrinkles. J. Cosmet. Sci. 2000, 51, 127-139.
9. Akazaki, S.; Imokawa, G. Mechanical methods for evaluating skin surface architecture in relation to wrinkling. J. Dermatol. Sci. 2001, 27, S5-S10.
10. Akasaki, S.; Nakagawa, H.; Kazama, H.; Osanai, O.; Kawai, M.; Takema, Y.; Imokawa, G. Age-related changes in skin wrinkles assessed by a novel three-dimensional morphometric analysis. Br. J. Dermatol. 2002, 147, 689-695.
11. Takema, Y.; Fujimura, T.; Ohsu, H.; Imokawa, G. Unusual wrinkle formation after temporary skin fixation followed by UVB irradiation in hairless mouse skin. Exp. Dermatol. 1996, 5, 145-149.
12. Takema, Y.; Imokawa, G. The effects of UV-A and UV-B irradiation on the viscoelastic properties of hairless mouse skin in vivo. Dermatology 1998, 196, 397-400.
13. Tsukahara, K.; Nakagawa, H.; Moriwaki, S.; Shingo, K.; Ohuchi, A.; Takema, Y.; Imokawa, G. Ovariectomy is sufficient to accelerate spontaneous skin ageing and to stimulate ultraviolet irradiation-induced photoageing of murine skin. Br. J. Dermatol. 2004, 151, 984-994.
14. Imayama, S.; Nakamura, K.; Takeuchi, M.; Hori, Y.; Takema, Y.; Sakaino, Y.; Imokawa, G. Ultraviolet-B irradiation deforms the configuration of elastic fibers during the induction of actinic elastosis in rats. J. Dermatol. Sci. 1994, 7, 32-38.
15. Imokawa, G.; Takema, Y.; Yorimoto, Y.; Tsukahara, K.; Kawai, M.; Imayama, S. Degree of ultraviolet-induced tortuosity of elastic fibers in rat skin is age-dependent. J. Investig. Dermatol. 1995, 105, 254-258.
16. Tsukahara, K.; Takema, Y.; Moriwaki, S.; Tsuji, N.; Suzuki, Y.; Fujimura, T.; Imokawa, G. Selective inhibition of skin fibroblast elastase elicits a dose-dependent prevention of UVB-induced wrinkle formation. J. Investig. Dermatol. 2001, 117, 671-677.
17. Smith, J.G., Jr.; Davidson, E.S.; Sams, W.M., Jr.; Clark, R.D. Alteration in human dermal connective tissue with age and chronic sun damage. J. Investig. Dermatol. 1962, 39, 347-350.
18. Mitchell, R.E. Chronic solar elastosis: An electron microscopic study of the dermis. J. Investig. Dermatol. 1967, 48, 203-220.
19. Stevanovic, D.V. Elastotic degeneration (a light and electron microscopic study). Br. J. Dermatol. 1976, 94, 23-29.
20. Montagna, W.; Carlisle, K. Structural changes in aging human skin. J. Investig. Dermatol. 1979, 73, 47-53.
21. Imayama, S.; Bravermann, I.M. A hypothetical explanation of the aging of skin. Chronological alteration of the three dimensional arrangement of collagen and elastic fibers in connective tissue. Am. J. Pathol. 1989, 134, 1019-1025.
22. Gibson, T.; Kenedi, R.M. The structural components of the dermis and their mechanical characteristics, in Advances in Biology of Skin. In The Dermis; Montagna, W., Bentley, J.P., Dobson, R.L., Eds.; Appleton-Century Crofts: New York, NY, USA, 1970; pp. 19-38.
23. Cua, A.B.; Wilhelm, K.P.; Maibach, H.I. Elastic properties of human skin: Relation to age, sex and anatomical region. Arch. Dermatol. Res. 1990, 282, 283-288.
24. Fujimura, T.; Takema, Y.; Moriwaki, S.; Tsukahara, K.; Imokawa, G.; Yamada, A.; Imayama, S. Analytical method to examine the effects of carbon dioxide lasers on skin: A study using wrinkles induced in hairless mice. Lasers Surg. Med. 2001, 28, 348-354.
25. Tsukahara, K.; Takema, Y.; Moriwaki, S.; Fujimura, T.; Imayama, S.; Imokawa, G. Carbon dioxide laser treatment promotes repair of the three-dimensional network of elastic fibers in rat skin. Br. J. Dermatol. 2001, 144, 452-458.
26. Tsukahara, K.; Takema, Y.; Fujimura, T.; Moriwaki, S.; Kitahara, T.; Imayama, S.; Imokawa, G. All-trans retinoic acid promotes the repair of tortuosity of elastic fibers in rat skin. Br. J. Dermatol. 1999, 140, 1048-1053.
27. Tsukahara, K.; Moriwaki, S.; Ohuchi, A.; Takema, Y. Ovariectomy accelerates photoaging of rat skin. Photochem. Photobiol. 2001, 73, 525-531.
28. Calleja-Agius, J.; Brincat, M.; Borg, M. Skin connective tissue and ageing. Best. Pract. Res. Clin. Obstet. Gynaecol. 2013, 27, 727-740.
29. Morisaki, N.; Moriwaki, S.; Sugiyama-Nakagiri, Y.; Haketa, K.; Takema, Y.; Imokawa, G. Neprilysin is identical to skin fibroblast elastase-Its role in skin ageing and UV responses. J. Biol. Chem. 2010, 285, 39819-39827.
30. Labat-Robert, J.; Kern, P.; Robert, L. Biomarkers of connective tissue aging: Biosynthesis of fibronectin, collagen type III and elastase. Ann. N. Y. Acad. Sci. 1992, 673, 16-22.
31. Bolognia, J.L. Aging skin. Am. J. Med. 1995, 98, 99S-103S.
32. Creidi, P.; Faivre, B.; Agache, P.; Richard, E.; Haudiquet, V.; Sauvanet, J.P. Effect of a conjugated oestrogen cream on ageing facial skin. A comparative study with a placebo cream. Maturitas 1994, 19, 211-223.
33. Pieraed-Franchimont, C.; Letawe, C.; Goffin, V.; Pierard, G.E. Skin water-holding capacity and transdermal estrogen therapy for menopause: A pilot study. Maturitas 1995, 22, 151-154.
34. Dunn, L.B.; Damesyn, M.; Moore, A.A.; Reuben, D.B.; Greendale, G.A. Does estrogen prevent skin aging? Results from the First National Health and and Nutrition Examination Survey. Arch. Dermatol. 1997, 133, 339-342.
35. Shah, M.G.; Maibach, H.I. Estrogen and skin. An overview. Am. J. Clin. Dermatol. 2001, 2, 143-150.
36. Sumino, H.; Ichikawa, S.; Abe, M.; Endo, Y.; Nakajima, Y.; Minegishi, T.; Ishikawa, O.; Kurabayashi, M. Effects of aging and postmenopausal hypoestrogenism on skin elasticity and bone mineral density in Japanese women. Endo J. 2004, 51, 159-164.
37. Sumino, H.; Ichikawa, S.; Abe, M.; Endo, Y.; Ishikawa, O.; Kurabayashi, M. Effects of aging, menopause, and hormone replacement therapy on forearm skin elasticity in women. J. Am. Geriatr. Soc. 2004, 52, 945-949.
38. Agache, P.G.; Monneur, C.; Leveque, J.L.; de Rigal, J. Mechanical properties and Young's modulus of human skin in vivo. Arch. Dermatol. Res. 1980, 269, 221-232.
39. Labat-Robert, J.; Fourtanier, A.; Boyer-Lafargur, B.; Robert, L. Age-dependent increase of elastase type protease activity in mouse skin. Effect of UV irradiation. J. Photochem. Photobiol. B 2000, 57, 113-118.
40. Tsuji, N.; Moriwaki, S.; Suzuki, Y.; Takema, Y.; Imokawa, G. The role of elastases secreted by fibroblasts in wrinkle formation: Implication through selective inhibition of elastase activity. Photochem. Photobiol. 2001, 74, 283-290.
41. Szendri, M.; Meimon, G.; Bakala, H.; Frances, C.; Robert, L.; Godeau, G.; Hornebeck, W. On the presence of a metalloproteinase in human skin fibroblasts that degrades the human skin elastic fiber system. J. Investig. Dermatol. 1984, 83, 224-229.
42. Schwartz, D.E.; Paller, A.S.; Lizak, P.P.; Person, R.W. Elastase and neutral cathepsin production by human fibroblasts: Effect of culture conditions on synthesis and secretion. J. Investig. Dermatol. 1986, 86, 63-68.
43. Schwartz, E.; Cruickshank, F.A.; Lebwohl, M.G. Elastase-like protease and elastolytic activities expressed in cultured dermal fibroblasts derived from lesional skin of patients with pseudoxanthoma elasticum, actinic elastosis, and cutis laxa. Clin. Chim. Acta 1998, 176, 219-224.
44. Nakagawa, K.; Tsuji, T.; Kadoya, A.; Hamada, T. Elastase-like enzyme activity in cultured human fibroblast. Skin Res. 1987, 29, 793-797.
45. Godeau, G.; Hornebeck, W. Morphometric analysis of the degradation of human skin elastic fibers by human leukocyte elastase (EC 3-4-21-37) and human skin fibroblast elastase (EC 3-4-24). Pathol. Biol. 1988, 36, 1133-1138.
46. Homsy, R.; Pelletier-Lebon, P.; Tixier, J.M.; Godeau, G.; Robert, L.; Hornebeck, W. Characterization of human skin fibroblast elastase activity. J. Investig. Dermatol. 1998, 91, 472-477.
47. Croute, F.; Delaporte, E.; Bonnefoy, J.Y.; Fertin, C.; Thivolet, J.; Nicolas, J.F. Interleukin-1β stimulates fibroblast elastase activity. Br. J. Dermatol. 1991, 124, 538-541.
48. Mecham, R.P.; Broekelmann, T.J.; Fliszar, C.J.; Shapiro, S.D.; Welgus, H.G.; Senior, R.M. Elastin degradation by matrix metalloproteinases. J. Biol. Chem. 1997, 272, 18071-18076.
49. Fimiani, M.; Mazzatenta, C.; Alessandrini, C.; Paola, M.; Paola, C.; Andreassi, L. Middermal elastolysis: An ultrastructural and biochemical study. Arch. Dermatol. Res. 1995, 287, 152-157.
50. Imokawa, G. Mechanism of UVB-induced wrinkling of the skin: Paracrine cytokine linkage between keratinocytes and fibroblasts leading to the stimulation of elastase. J. Investig. Dermatol. Symp. Proc. 2009, 14, 36-43.
51. Tsukahara, K.; Nakagawa, H.; Moriwaki, S.; Takema, Y.; Fujimura, T.; Imokawa, G. Inhibition of ultraviolet-B-induced wrinkle formation by an elastase-inhibiting herbal extract: Implication for the mechanism underlying elastase-associated wrinkles. Int. J. Dermatol. 2006, 45, 460-468.
52. Imokawa, G. Recent advances in characterizing biological mechanisms underlying UV-induced wrinkles: A pivotal role of fibroblast-derived elastase. Arch. Dermatol. Res. 2008, 300, S7-S20.
53. Tsukahara, K.; Nakagawa, H.; Ohtuki, M.; Moriwaki, S.; Fujimura, T.; Takema, Y.; Imokawa, G. A clinical effect of Zingiber officinale (L.) Rose on facial wrinkles and skin elasticity. Jichi Med. School J. 2004, 27, 19-27.
54. Lorkowski, G.; Zijderhand-Bleekemolen, J.E.; Erdös, E.G.; von Figura, K.; Hasilik, A. Neutral endopeptidase-24.11 (enkephalinase). Biosynthesis and localization in human fibroblasts. Biochem. J. 1987, 248, 345-350.
55. Nadel, J.A. Neutral endopeptidase modulates neurogenic inflammation. Eur. Respir. J. 1991, 4, 745-754.
56. Misery, L. [Neuro-immuno-cutaneous system (NICS)]. Pathol. Biol. 1996, 44, 867-874.