CD147 self-regulates matrix metalloproteinase-2 release in gingival fibroblasts after coculturing with U937 monocytic cells.
CD147
U937 cells
antigens
fibroblasts
matrix metalloproteinase 2
monocytes
Journal
Journal of periodontology
ISSN: 1943-3670
Titre abrégé: J Periodontol
Pays: United States
ID NLM: 8000345
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
06
05
2019
revised:
11
08
2019
accepted:
26
08
2019
pubmed:
27
9
2019
medline:
15
9
2020
entrez:
27
9
2019
Statut:
ppublish
Résumé
Cluster of differentiation 147 (CD147) is a multifunctional glycoprotein that functions as an inducer of matrix metalloproteinase (MMP) expression in fibroblasts. Synergistically enhanced MMP-2 expression was recently observed in the coculture of human gingival fibroblasts (HGFs) and U937 human monocytic cells; however, the responsible mechanisms have not yet been fully established. The aim of this study was to evaluate the release of soluble CD147 in HGFs after coculturing with U937 cells and its functional effect on the enhancement of MMP-2 expression in HGFs. Enzyme-linked immunosorbent assay was used to determine the amount of CD147 protein in media, whereas real-time polymerase chain reaction was performed to evaluate the mRNA levels of CD147 and MMP-2 in HGFs and U937 cells. The enzyme activities of MMP-2 released from cells were examined by zymography. Transwell coculturing and conditioned media treatments were selected to rule out the effect of direct contact of HGFs and U937 cells. The protein and mRNA expression of CD147 in HGFs were enhanced after transwell coculturing with U937 cells and exposure to U937-conditioned medium. MMP-2 enzyme activities in HGFs were also significantly increased by the coculturing methods. Administration of exogenous CD147 enhanced MMP-2 expression in HGFs, whereas treatment with cyclosporine-A, which inhibited CD147 expression, reduced U937-enhanced MMP-2 expression in HGFs. CD147 can interact with fibroblasts to stimulate the expression of MMPs associated with periodontal extracellular matrix degradation. This study has demonstrated that CD147 released from fibroblasts might play a role in monocyte-enhanced MMP-2 expression in HGFs.
Sections du résumé
BACKGROUND
Cluster of differentiation 147 (CD147) is a multifunctional glycoprotein that functions as an inducer of matrix metalloproteinase (MMP) expression in fibroblasts. Synergistically enhanced MMP-2 expression was recently observed in the coculture of human gingival fibroblasts (HGFs) and U937 human monocytic cells; however, the responsible mechanisms have not yet been fully established. The aim of this study was to evaluate the release of soluble CD147 in HGFs after coculturing with U937 cells and its functional effect on the enhancement of MMP-2 expression in HGFs.
METHODS
Enzyme-linked immunosorbent assay was used to determine the amount of CD147 protein in media, whereas real-time polymerase chain reaction was performed to evaluate the mRNA levels of CD147 and MMP-2 in HGFs and U937 cells. The enzyme activities of MMP-2 released from cells were examined by zymography. Transwell coculturing and conditioned media treatments were selected to rule out the effect of direct contact of HGFs and U937 cells.
RESULTS
The protein and mRNA expression of CD147 in HGFs were enhanced after transwell coculturing with U937 cells and exposure to U937-conditioned medium. MMP-2 enzyme activities in HGFs were also significantly increased by the coculturing methods. Administration of exogenous CD147 enhanced MMP-2 expression in HGFs, whereas treatment with cyclosporine-A, which inhibited CD147 expression, reduced U937-enhanced MMP-2 expression in HGFs.
CONCLUSIONS
CD147 can interact with fibroblasts to stimulate the expression of MMPs associated with periodontal extracellular matrix degradation. This study has demonstrated that CD147 released from fibroblasts might play a role in monocyte-enhanced MMP-2 expression in HGFs.
Identifiants
pubmed: 31557319
doi: 10.1002/JPER.19-0278
doi:
Substances chimiques
BSG protein, human
0
Basigin
136894-56-9
MMP2 protein, human
EC 3.4.24.24
Matrix Metalloproteinase 2
EC 3.4.24.24
Matrix Metalloproteinase 1
EC 3.4.24.7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
651-660Informations de copyright
© 2019 American Academy of Periodontology.
Références
Listgarten MA. The role of dental plaque in gingivitis and periodontitis. J Clin Periodontol. 1988;15:485-487.
Cochran DL. Inflammation and bone loss in periodontal disease. J Periodontol. 2008;79:1569-1576.
Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 2000. 2014;64:57-80.
Sapna G, Gokul S, Bagri-Manjrekar K. Matrix metalloproteinases and periodontal diseases. Oral Dis. 2014;20:538-550.
Bode W, Gomis-Ruth FX, Stockler W. Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the ‘metzincins’. FEBS Lett. 1993;331:134-140.
Stocker W, Grams F, Baumann U, et al. The metzincins-topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci. 1995;4:823-840.
Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol. 2003;200:448-464.
Mauviel A. Cytokine regulation of metalloproteinase gene expression. J Cell Biochem. 1993;53:288-295.
Roberts LM, Visser JA, Ingraham HA. Involvement of a matrix metalloproteinase in MIS-induced cell death during urogenital development. Development. 2002;129:1487-1496.
Soell M, Elkaim R, Tenenbaum H. Cathepsin C, matrix metalloproteinases, and their tissue inhibitors in gingiva and gingival crevicular fluid from periodontitis-affected patients. J Dent Res. 2002;81:174-178.
Goncalves LD, Oliveira G, Hurtado PA, et al. Expression of metalloproteinases and their tissue inhibitors in inflamed gingival biopsies. J Periodontal Res. 2008;43:570-577.
Dong W, Xiang J, Li C, Cao Z, Huang Z. Increased expression of extracellular matrix metalloproteinase inducer is associated with matrix metalloproteinase-1 and -2 in gingival tissues from patients with periodontitis. J Periodontal Res. 2009;44:125-132.
Maeso G, Bravo M, Bascones A. Levels of metalloproteinase-2 and -9 and tissue inhibitor of matrix metalloproteinase-1 in gingival crevicular fluid of patients with periodontitis, gingivitis, and healthy gingiva. Quintessence Int. 2007;38:247-252.
Biswas C, Zhang Y, DeCastro R, et al. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res. 1995;55:434-439.
Grass GD, Toole BP. How, with whom and when: an overview of CD147-mediated regulatory networks influencing matrix metalloproteinase activity. Biosci Rep. 2015;36:e00283.
Guo H, Zucker S, Gordon MK, Toole BP, Biswas C. Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected Chinese hamster ovary cells. J Biol Chem. 1997;272:24-27.
Foda HD, Rollo EE, Drews M, et al. Ventilator-induced lung injury upregulates and activates gelatinases and EMMPRIN: attenuation by the synthetic matrix metalloproteinase inhibitor, Prinomastat (AG3340). Am J Respir Cell Mol Biol. 2001;25:717-724.
Gabison EE, Hoang-Xuan T, Mauviel A, Menashi S. EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair. Biochimie. 2005;87:361-368.
Wang J, Yang D, Li C, Shang S, Xiang J. Expression of extracellular matrix metalloproteinase inducer glycosylation and caveolin-1 in healthy and inflamed human gingiva. J Periodontal Res. 2014;49:197-204.
Emingil G, Tervahartiala T, Mantyla P, Maatta M, Sorsa T, Atilla G. Gingival crevicular fluid matrix metalloproteinase (MMP)-7, extracellular MMP inducer, and tissue inhibitor of MMP-1 levels in periodontal disease. J Periodontol. 2006;77:2040-2050.
Lo YJ, Liu CM, Wong MY, Hou LT, Chang WK. Interleukin 1beta-secreting cells in inflamed gingival tissue of adult periodontitis patients. Cytokine. 1999;11:626-633.
Kuo PJ, Tu HP, Chin YT, et al. Cyclosporine-A inhibits MMP-2 and -9 activities in the presence of Porphyromonas gingivalis lipopolysaccharide: an experiment in human gingival fibroblast and U937 macrophage co-culture. J Periodontal Res. 2012;47:431-438.
Tu HP, Chen YT, Shieh YS, et al. Cyclosporin-induced downregulation of the expression of E-cadherin during proliferation of edentulous gingival epithelium in rats. J Periodontol. 2006;77:832-839.
Kuo PJ, Lin HL, Lin CY, et al. Crosstalk between human monocytic U937 cells and gingival fibroblasts in coculturally enhanced matrix metalloproteinase-2 expression. J Periodontol. 2016;87:1228-1237.
Steffensen B, Wallon UM, Overall CM. Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affinity binding to native type I collagen but not native type IV collagen. J Biol Chem. 1995;270:11555-11566.
Bordador LC, Li X, Toole B, et al. Expression of emmprin by oral squamous cell carcinoma. Int J Cancer. 2000;85:347-352.
Kanekura T, Chen X, Kanzaki T. Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metalloproteinases by fibroblasts. Int J Cancer. 2002;99:520-528.
Zucker S, Hymowitz M, Rollo EE, et al. Tumorigenic potential of extracellular matrix metalloproteinase inducer. Am J Pathol. 2001;158:1921-1928.
Taylor PM, Woodfield RJ, Hodgkin MN, et al. Breast cancer cell-derived EMMPRIN stimulates fibroblast MMP2 release through a phospholipase A(2) and 5-lipoxygenase catalyzed pathway. Oncogene. 2002;21:5765-5772.
Nabeshima K, Iwasaki H, Koga K, Hojo H, Suzumiya J, Kikuchi M. Emmprin (basigin/CD147): matrix metalloproteinase modulator and multifunctional cell recognition molecule that plays a critical role in cancer progression. Pathol Int. 2006;56:359-367.
Si AI, Huang L, Xu J, Kumta SM, Wood D, Zheng MH. Expression and localization of extracellular matrix metalloproteinase inducer in giant cell tumor of bone. J Cell Biochem. 2003;89:1154-1163.
Cui HY, Guo T, Wang SJ, et al. Dimerization is essential for HAb18G/CD147 promoting tumor invasion via MAPK pathway. Biochem Biophys Res Commun. 2012;419:517-522.
Yan L, Zucker S, Toole BP. Roles of the multifunctional glycoprotein, emmprin (basigin; CD147), in tumour progression. Thromb Haemost. 2005;93:199-204.
Holt DJ, Chamberlain LM, Grainger DW. Cell-cell signaling in co-cultures of macrophages and fibroblasts. Biomaterials. 2010;31:9382-9394.
Zhang DW, Zhao YX, Wei D, et al. HAb18G/CD147 promotes activation of hepatic stellate cells and is a target for antibody therapy of liver fibrosis. J Hepatol. 2012;57:1283-1291.
Yurchenko V, Pushkarsky T, Li JH, Dai WW, Sherry B, Bukrinsky M. Regulation of CD147 cell surface expression: involvement of the proline residue in the CD147 transmembrane domain. J Biol Chem. 2005;280:17013-17019.
Arora K, Gwinn WM, Bower MA, et al. Extracellular cyclophilins contribute to the regulation of inflammatory responses. J Immunol. 2005;175:517-522.
Malesevic M, Gutknecht D, Prell E, et al. Anti-inflammatory effects of extracellular cyclosporins are exclusively mediated by CD147. J Med Chem. 2013;56:7302-7311.
Seizer P, Schonberger T, Schott M, et al. EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation. Atherosclerosis. 2010;209:51-57.
Dahan M, Nawrocki B, Elkaim R, et al. Expression of matrix metalloproteinases in healthy and diseased human gingiva. J Clin Periodontol. 2001;28:128-136.
Liu L, Li C, Cai X, Xiang J, Cao Z, Dong W. The temporal expression and localization of extracellular matrix metalloproteinase inducer (EMMPRIN) during the development of periodontitis in an animal model. J Periodontal Res. 2010;45:541-549.
Burger D, Rezzonico R, Li JM, et al. Imbalance between interstitial collagenase and tissue inhibitor of metalloproteinases 1 in synoviocytes and fibroblasts upon direct contact with stimulated T lymphocytes: involvement of membrane-associated cytokines. Arthritis Rheum. 1998;41:1748-1759.
Hojo Y, Ikeda U, Takahashi M, et al. Matrix metalloproteinase-1 expression by interaction between monocytes and vascular endothelial cells. J Mol Cell Cardiol. 2000;32:1459-1468.
Zhu Y, Liu X, Skold CM, et al. Collaborative interactions between neutrophil elastase and metalloproteinases in extracellular matrix degradation in three-dimensional collagen gels. Respir Res. 2001;2:300-305.
Konopka L, Pietrzak A, Brzezinska-Blaszczyk E. Effect of scaling and root planing on interleukin-1β, interleukin-8 and MMP-8 levels in gingival crevicular fluid from chronic periodontitis patients. J Periodontal Res. 2012;47:681-688.
McKleroy W, Lee TH, Atabai K. Always cleave up your mess: targeting collagen degradation to treat tissue fibrosis. Am J Physiol Lung Cell Mol Physiol. 2013;304:L709-L721.
Song F, Wisithphrom K, Zhou J, Windsor LJ. Matrix metalloproteinase dependent and independent collagen degradation. Front Biosci. 2006;11:3100-3120.
Makela M, Salo T, Uitto VJ, Larjava H. Matrix metalloproteinases (MMP-2 and MMP-9) of the oral cavity: cellular origin and relationship to periodontal status. J Dent Res. 1994;73:1397-1406.
Preshaw PM. Host modulation therapy with anti-inflammatory agents. Periodontol 2000. 2018;76:131-149.