Extract of the mycelium of T. matsutake inhibits elastase activity and TPA-induced MMP-1 expression in human fibroblasts

Kim,So  Young; Go,Kyung  Chan; Song,Yi  Seop; Jeong,Yeon  Su; Kim,Eun  Joo; Kim,Beom  Joon

doi:10.3892/ijmm.2014.1969

Extract of the mycelium of T. matsutake inhibits elastase activity and TPA-induced MMP-1 expression in human fibroblasts

Authors:
- So Young Kim
- Kyung Chan Go
- Yi Seop Song
- Yeon Su Jeong
- Eun Joo Kim
- Beom Joon Kim
View Affiliations

Affiliations: Major in Biomedical Science, Department of Medicine, Graduate School, Chung-Ang University, Seoul, Republic of Korea, Department of Dermatology, Chung-Ang University College of Medicine, Seoul, Republic of Korea
Published online on: October 14, 2014 https://doi.org/10.3892/ijmm.2014.1969
Pages: 1613-1621

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Skin aging is induced through complex biological processes in human skin caused by proteolysis of collagen and elastin, two structural proteins of the dermal extracellular matrix (ECM). Collagen and elastin degradation can induce the expression of matrix metalloproteinases (MMPs), as well as that of a family of zinc-dependent endopeptidases that play critical roles in skin aging. Moreover, elastase is a metalloproteinase which acts on the degradation of elastin in skin aging, and is also involved in the inhibition or the repair of wrinkle formation. Extract of the mycelium of Tricholoma matsutake (T. matsutake), or pine mushroom, is widely distributed in Asian countries. The extract is from the natural biomaterial of the mushroom which is rich in polysaccharides, including β-glucan. This extract has shown potent bioactive antioxidant, immunomodulatory and antitumoral properties. In the present study, we investigated whether the extract of the mycelium of T. matsutake has effects on elastase activity, as well as on the expression of tissue inhibitor of matrix metalloproteinases-1 (TIMP-1) and MMP-1 under basal conditions. Our results revealed that the extract of the mycelium of T. matsutake significantly decreased elastase activity in a dose-dependent manner and reduced the levels of MMP-1 and MMP-3. On the other hand, the expression of TIMP-1 and tropoelastin was increased in fibroblasts treated with the extract of the mycelium of T. matsutake. However, collagent expression was not affected. In addition, our results demonstrated that the extract of the mycelium of T. matsutake inhibited the 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced MMP-1 expression and suppressed TPA-induced p38 activity. Therefore, the inhibitory effects of the extract of the mycelium of T. matsutake on MMP-1 induction are mediated by the inhibition of p38 in human fibroblasts. Our data suggest that the extract of the mycelium of T. matsutake may prove to be an effective biomaterial for anti-wrinkle treatment, as it can obstruct the degradation of the dermal ECM.

View Figures

View References

1	Naylor EC, Watson RE and Sherratt MJ: Molecular aspects of skin ageing. Maturitas. 69:249–256. 2011. View Article : Google Scholar
2	Jenkins G: Molecular mechanisms of skin ageing. Mech Ageing Dev. 123:801–810. 2002. View Article : Google Scholar
3	Iida I and Noro K: An analysis of the reduction of elasticity on the ageing of human skin and the recovering effect of a facial massage. Ergonomics. 38:1921–1931. 1995. View Article : Google Scholar : PubMed/NCBI
4	Seite S, Zucchi H, Septier D, Igondjo-Tchen S, Senni K and Godeau G: Elastin changes during chronological and photo-ageing: the important role of lysozyme. J Eur Acad Dermatol Venereol. 20:980–987. 2006.PubMed/NCBI
5	Mukherjee PK, Maity N, Nema NK and Sarkar BK: Bioactive compounds from natural resources against skin aging. Phytomedicine. 19:64–73. 2011.PubMed/NCBI
6	Imokawa G, Takema Y, Yorimoto Y, Tsukahara K, Kawai M and Imayama S: Degree of ultraviolet-induced tortuosity of elastic fibers in rat skin is age dependent. J Invest Dermatol. 105:254–258. 1995. View Article : Google Scholar : PubMed/NCBI
7	Teti A: Regulation of cellular functions by extracellular matrix. J Am Soc Nephrol. 2:S83–S87. 1992.PubMed/NCBI
8	Werner S, Krieg T and Smola H: Keratinocyte-fibroblast interactions in wound healing. J Invest Dermatol. 127:998–1008. 2007. View Article : Google Scholar : PubMed/NCBI
9	Enjoji M, Kotoh K, Iwamoto H, Nakamuta M and Nawata H: Self-regulation of type I collagen degradation by collagen-induced production of matrix metalloproteinase-1 on cholangiocarcinoma and hepatocellular carcinoma cells. In Vitro Cell Dev Biol Anim. 36:71–73. 2000. View Article : Google Scholar : PubMed/NCBI
10	Philips N and Devaney J: Beneficial regulation of type I collagen and matrixmetalloproteinase-1 expression by estrogen, progesterone, and its combination in skin fibroblasts. J Am Aging Assoc. 26:59–62. 2003.PubMed/NCBI
11	Fisher GJ, Datta SC, Talwar HS, et al: Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature. 379:335–339. 1996. View Article : Google Scholar : PubMed/NCBI
12	Rittie L and Fisher GJ: UV-light-induced signal cascades and skin aging. Ageing Res Rev. 1:705–720. 2002. View Article : Google Scholar : PubMed/NCBI
13	Brew K and Nagase H: The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta. 1803:55–71. 2010. View Article : Google Scholar : PubMed/NCBI
14	Shapiro SD, Endicott SK, Province MA, Pierce JA and Campbell EJ: Marked longevity of human lung parenchymal elastic fibers deduced from prevalence of D-aspartate and nuclear weapons-related radiocarbon. J Clin Invest. 87:1828–1834. 1991. View Article : Google Scholar : PubMed/NCBI
15	Mecham RP, Broekelmann TJ, Fliszar CJ, Shapiro SD, Welgus HG and Senior RM: Elastin degradation by matrix metalloproteinases. Cleavage site specificity and mechanisms of elastolysis. J Biol Chem. 272:18071–18076. 1997. View Article : Google Scholar : PubMed/NCBI
16	Kim JY, Byeon SE, Lee YG, et al: Immunostimulatory activities of polysaccharides from liquid culture of pine-mushroom Tricholoma matsutake. J Microbiol Biotechnol. 18:95–103. 2008.PubMed/NCBI
17	Ebina T: Activation of antitumor immunity by intratumor injection of biological preparations. Gan To Kagaku Ryoho. 30:1555–1558. 2003.(In Japanese).
18	Hoshi H, Yagi Y, Iijima H, Matsunaga K, Ishihara Y and Yasuhara T: Isolation and characterization of a novel immunomodulatory alpha-glucan-protein complex from the mycelium of Tricholoma matsutake in basidiomycetes. J Agric Food Chem. 53:8948–8956. 2005. View Article : Google Scholar : PubMed/NCBI
19	Choi JJ, Jin M, Lee JK, et al: Control of cytokine gene expression by PG101, a water-soluble extract prepared from Lentinus lepideus. Biochem Biophys Res Commun. 339:880–887. 2006. View Article : Google Scholar : PubMed/NCBI
20	Wasser SP: Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl Microbiol Biotechnol. 60:258–274. 2002.PubMed/NCBI
21	Rheinwald JG and Green H: Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell. 6:331–343. 1975. View Article : Google Scholar
22	Tsuji N, Moriwaki S, Suzuki Y, Takema Y and Imokawa G: The role of elastases secreted by fibroblasts in wrinkle formation: implication through selective inhibition of elastase activity. Photochem Photobiol. 74:283–290. 2001. View Article : Google Scholar : PubMed/NCBI
23	Bonnaure-Mallet M, Godeau G, Tixier JM, et al: Elastin derived peptides protect elastic fibres degradation by human neutrophil elastase: in vitro and in vivo studies using a mechanically induced rat gingival inflammatory model. J Periodontal Res. 30:58–65. 1995. View Article : Google Scholar
24	Westermarck J, Holmstrom T, Ahonen M, Eriksson JE and Kahari VM: Enhancement of fibroblast collagenase-1 (MMP-1) gene expression by tumor promoter okadaic acid is mediated by stress-activated protein kinases Jun N-terminal kinase and p38. Matrix Biol. 17:547–557. 1998. View Article : Google Scholar : PubMed/NCBI
25	Reunanen N, Westermarck J, Hakkinen L, et al: Enhancement of fibroblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stress-activated protein kinase pathways. J Biol Chem. 273:5137–5145. 1998. View Article : Google Scholar
26	Lim M, Martinez T, Jablons D, et al: Tumor-derived EMMPRIN (extracellular matrix metalloproteinase inducer) stimulates collagenase transcription through MAPK p38. FEBS Lett. 441:88–92. 1998. View Article : Google Scholar
27	Kim GY, Lee JY, Lee JO, et al: Partial characterization and immunostimulatory effect of a novel polysaccharide-protein complex extracted from Phellinus linteus. Biosci Biotechnol Biochem. 70:1218–1226. 2006. View Article : Google Scholar : PubMed/NCBI
28	Hou Y, Ding X, Hou W, et al: Anti-microorganism, anti-tumor, and immune activities of a novel polysaccharide isolated from Tricholoma matsutake. Pharmacogn Mag. 9:244–249. 2013. View Article : Google Scholar : PubMed/NCBI
29	Amalinei C, Caruntu ID and Balan RA: Biology of metalloproteinases. Rom J Morphol Embryol. 48:323–334. 2007.PubMed/NCBI
30	Nagase H, Visse R and Murphy G: Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 69:562–573. 2006. View Article : Google Scholar : PubMed/NCBI
31	Tsukahara K, Moriwaki S, Hotta M, et al: The effect of sunscreen on skin elastase activity induced by ultraviolet-A irradiation. Biol Pharm Bull. 28:2302–2307. 2005. View Article : Google Scholar : PubMed/NCBI
32	Volman JJ, Helsper JP, Wei S, et al: Effects of mushroom-derived beta-glucan-rich polysaccharide extracts on nitric oxide production by bone marrow-derived macrophages and nuclear factor-kappaB transactivation in Caco-2 reporter cells: can effects be explained by structure? Mol Nutr Food Res. 54:268–276. 2010. View Article : Google Scholar
33	Tong H, Liu X, Tian D and Sun X: Purification, chemical characterization and radical scavenging activities of alkali-extracted polysaccharide fractions isolated from the fruit bodies of Tricholoma matsutake. World J Microbiol Biotechnol. 29:775–780. 2013. View Article : Google Scholar
34	Godeau G and Hornebeck W: Morphometric analysis of the degradation of human skin elastic fibres by human leukocyte elastase (EC 3-4-21-37) and human skin fibroblast elastase (EC 3-4-24). Pathol Biol (Paris). 36:1133–1138. 1988.PubMed/NCBI
35	Thorsett ED, Harris EE, Peterson ER, et al: Phosphorus-containing inhibitors of angiotensin-converting enzyme. Proc Natl Acad Sci USA. 79:2176–2180. 1982. View Article : Google Scholar : PubMed/NCBI
36	Tsukahara K, Takema Y, Moriwaki S, et al: Selective inhibition of skin fibroblast elastase elicits a concentration-dependent prevention of ultraviolet B-induced wrinkle formation. J Invest Dermatol. 117:671–677. 2001. View Article : Google Scholar : PubMed/NCBI
37	Jimenez F, Mitts TF, Liu K, Wang Y and Hinek A: Ellagic and tannic acids protect newly synthesized elastic fibers from premature enzymatic degradation in dermal fibroblast cultures. J Invest Dermatol. 126:1272–1280. 2006. View Article : Google Scholar : PubMed/NCBI
38	Philips N, Auler S, Hugo R and Gonzalez S: Beneficial regulation of matrix metalloproteinases for skin health. Enzyme Res. 2011:4272852011. View Article : Google Scholar : PubMed/NCBI
39	Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S and Voorhees JJ: Pathophysiology of premature skin aging induced by ultraviolet light. N Engl J Med. 337:1419–1428. 1997. View Article : Google Scholar : PubMed/NCBI
40	Garrington TP and Johnson GL: Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr Opin Cell Biol. 11:211–218. 1999. View Article : Google Scholar : PubMed/NCBI
41	Verma AK, Pong RC and Erickson D: Involvement of protein kinase C activation in ornithine decarboxylase gene expression in primary culture of newborn mouse epidermal cells and in skin tumor promotion by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res. 46:6149–6155. 1986.
42	Fagot D, Asselineau D and Bernerd F: Direct role of human dermal fibroblasts and indirect participation of epidermal keratinocytes in MMP-1 production after UV-B irradiation. Arch Dermatol Res. 293:576–583. 2002. View Article : Google Scholar : PubMed/NCBI
43	Huang TS, Duyster J and Wang JY: Biological response to phorbol ester determined by alternative G1 pathways. Proc Natl Acad Sci USA. 92:4793–4797. 1995. View Article : Google Scholar : PubMed/NCBI
44	Simon C, Simon M, Vucelic G, et al: The p38 SAPK pathway regulates the expression of the MMP-9 collagenase via AP-1-dependent promoter activation. Exp Cell Res. 271:344–355. 2001. View Article : Google Scholar : PubMed/NCBI
45	Westermarck J, Li SP, Kallunki T, Han J and Kahari VM: p38 mitogen-activated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase 1 (MMP-1) gene expression. Mol Cell Biol. 21:2373–2383. 2001. View Article : Google Scholar : PubMed/NCBI
46	Westermarck J, Seth A and Kahari VM: Differential regulation of interstitial collagenase (MMP-1) gene expression by ETS transcription factors. Oncogene. 14:2651–2660. 1997. View Article : Google Scholar : PubMed/NCBI
47	Millward TA, Zolnierowicz S and Hemmings BA: Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem Sci. 24:186–191. 1999. View Article : Google Scholar : PubMed/NCBI