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J. Biol. Chem., Vol. 279, Issue 3, 1676-1683, January 16, 2004

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Ultraviolet A-induced Production of Matrix Metalloproteinase-1 Is Mediated by Macrophage Migration Inhibitory Factor (MIF) in Human Dermal Fibroblasts^*

Hirokazu Watanabe, Tadamichi Shimizu, Jun Nishihira, Riichiro Abe, Toshinori Nakayama¶||, Masaru Taniguchi||**, Hisataka Sabe, Teruo Ishibashi, and Hiroshi Shimizu

From the Departments of Dermatology and Molecular Biochemistry, Hokkaido University Graduate School of Medicine, Kita-ku, Sapporo 060-8638, Japan, the ^¶Department of Medical Immunology and ^||Department of Molecular Immunology, Graduate School of Medicine, Chiba University, 1-8-1 Inohana Chuo-ku, Chiba 260-8670, Japan, the ^**Laboratory for Immune Regulation, RIKEN Research Center for Allergy and Immunology, Yokohama, 230-0045, Japan, and the Department of Molecular Biology, Osaka Bioscience Institute, Osaka 565-0874, Japan

Matrix metalloproteinases (MMPs) are thought to be responsible for dermal photoaging in human skin. In the present study, we evaluated the involvement of macrophage migration inhibitory factor (MIF) in MMP-1 expression under ultraviolet A (UVA) irradiation in cultured human dermal fibroblasts. UVA (20 J/cm²) up-regulates MIF production, and UVA-induced MMP-1 mRNA production is inhibited by an anti-MIF antibody. MIF (100 ng/ml) was shown to induce MMP-1 in cultured human dermal fibroblasts. We found that MIF (100 ng/ml) enhanced MMP-1 activity in cultured fibroblasts assessed by zymography. Moreover, we observed that fibroblasts obtained from MIF-deficient mice were much less sensitive to UVA regarding MMP-13 expression than those from wild-type BALB/c mice. Furthermore, after UVA irradiation (10 J/cm²), dermal fibroblasts of MIF-deficient mice produced significantly decreased levels of MMP-13 compared with fibroblasts of wild-type mice. Next we investigated the signal transduction pathway of MIF. The up-regulation of MMP-1 mRNA by MIF stimulation was found to be inhibited by a PKC inhibitor (GF109203X), a Src-family tyrosine kinase inhibitor (herbimycin A), a tyrosine kinase inhibitor (genistein), a PKA inhibitor (H89), a MEK inhibitor (PD98089), and a JNK inhibitor (SP600125). In contrast, the p38 inhibitor (SB203580) was found to have little effect on expression of MMP-1 mRNA. We found that PKC-pan, PKC/II, PKC (Thr505), PKC (Ser⁶⁴³), Raf, and MAPK were phosphorylated by MIF. Moreover, we demonstrated that phosphorylation of PKC/II and MAPK in response to MIF was suppressed by genistein, and herbimycin A as well as by transfection of the plasmid of C-terminal Src kinase. The DNA binding activity of AP-1 was significantly up-regulated 2 h after MIF stimulation. Taken together, these results suggest that MIF is involved in the up-regulation of UVA-induced MMP-1 in dermal fibroblasts through PKC-, PKA-, Src family tyrosine kinase-, MAPK-, c-Jun-, and AP-1-dependent pathways.

Received for publication, April 8, 2003 , and in revised form, October 10, 2003.

^* This work was supported in part by Grants-in-aid for research (No. 11670813 and 13357008) from the Ministry of Education, Science, and Culture of Japan, and the Shiseido Foundation for Skin Aging Research. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. of Dermatology, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan. Fax: 81-11-706-7820; E-mail: shimizu{at}med.hokudai.ac.jp.

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