Porphyromonas gingivalis lipopolysaccharide and gingival fibroblast augment MMP-9 expression of monocytic U937 cells through cyclophilin A.
U937 cells
cyclophilin A
fibroblasts
gingiva
matrix metalloproteinase 9
Journal
Journal of periodontology
ISSN: 1943-3670
Titre abrégé: J Periodontol
Pays: United States
ID NLM: 8000345
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
revised:
06
07
2020
received:
09
02
2020
accepted:
10
07
2020
pubmed:
18
5
2021
medline:
3
5
2022
entrez:
17
5
2021
Statut:
ppublish
Résumé
Intercellular cross-talking was suggested in matrix metalloproteinase (MMP)-9 expression with unknown mechanisms. Studies showed cyclophilin A (CypA) playing an important role in regulating MMP-9 expression in varied diseases. The aim of the study was to examine the CyPA on the MMP-9 augmentation in monocytic U937 cells after Porphyromonas gingivalis (Pg) lipopolysaccharide (LPS) treatment and human gingival fibroblast (hGF) co-culture. In independent culture or co-culture of hGF and U937 cell, quantitative real-time polymerase chain reaction (qPCR) and zymography were selected to examine the mRNA and protein activity of MMP-9, respectively. The CyPA expression was determined by qPCR. LPS could enhance MMP-9 mRNA expression and enzyme activity in U937 cell. However, the enhancements were not observed in hGF. Similarly, LPS enhanced CyPA mRNA in U937, but not in hGF. After co-cultured with hGF, however, MMP-9 and CyPA in U937 increased regardless of the presence/absence of LPS. In U937 cells, the extra-supplied CyPA increased MMP-9 mRNA and enzyme activity, whereas the CyPA inhibitor, cyclosporine A, suppressed the LPS- and co-culture-enhanced MMP-9. Moreover, the inhibitors for MAP kinase, including PD98059 (ERK) and SP600125 (JNK), suppressed the CyPA-enhanced MMP-9 in U937. Through the CyPA pathway, the LPS and the hGF could augment the MMP-9 expression in the U937 cells.
Sections du résumé
BACKGROUND
Intercellular cross-talking was suggested in matrix metalloproteinase (MMP)-9 expression with unknown mechanisms. Studies showed cyclophilin A (CypA) playing an important role in regulating MMP-9 expression in varied diseases. The aim of the study was to examine the CyPA on the MMP-9 augmentation in monocytic U937 cells after Porphyromonas gingivalis (Pg) lipopolysaccharide (LPS) treatment and human gingival fibroblast (hGF) co-culture.
METHODS
In independent culture or co-culture of hGF and U937 cell, quantitative real-time polymerase chain reaction (qPCR) and zymography were selected to examine the mRNA and protein activity of MMP-9, respectively. The CyPA expression was determined by qPCR.
RESULTS
LPS could enhance MMP-9 mRNA expression and enzyme activity in U937 cell. However, the enhancements were not observed in hGF. Similarly, LPS enhanced CyPA mRNA in U937, but not in hGF. After co-cultured with hGF, however, MMP-9 and CyPA in U937 increased regardless of the presence/absence of LPS. In U937 cells, the extra-supplied CyPA increased MMP-9 mRNA and enzyme activity, whereas the CyPA inhibitor, cyclosporine A, suppressed the LPS- and co-culture-enhanced MMP-9. Moreover, the inhibitors for MAP kinase, including PD98059 (ERK) and SP600125 (JNK), suppressed the CyPA-enhanced MMP-9 in U937.
CONCLUSION
Through the CyPA pathway, the LPS and the hGF could augment the MMP-9 expression in the U937 cells.
Identifiants
pubmed: 33999413
doi: 10.1002/JPER.19-0740
doi:
Substances chimiques
Lipopolysaccharides
0
RNA, Messenger
0
Matrix Metalloproteinase 2
EC 3.4.24.24
Matrix Metalloproteinase 9
EC 3.4.24.35
Cyclophilin A
EC 5.2.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
449-457Informations de copyright
© 2021 American Academy of Periodontology.
Références
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.
Yucel-Lindberg T, Bage T. Inflammatory mediators in the pathogenesis of periodontitis. Exp Rev Mol Med. 2013;15:e7.
Ryan ME, Golub LM. Modulation of matrix metalloproteinase activities in periodontitis as a treatment strategy. Periodontol 2000. 2000;24:226-238.
Listgarten MA. Nature of periodontal diseases: pathogenic mechanisms. J Periodontal Res. 1987;22:172-178.
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.
Reynolds JJ. Collagenases and tissue inhibitors of metalloproteinases: a functional balance in tissue degradation. Oral Dis. 1996;2:70-76.
Woessner JF Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. Faseb J. 1991;5:2145-2154.
Sorsa T, Tjaderhane L, Konttinen YT, et al. Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Ann Med. 2006;38:306-321.
Van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9. Crit Rev Biochem Mol Biol. 2002;37:375-536.
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.
Fischer G, Bang H, Berger E, Schellenberger A. Conformational specificity of chymotrypsin toward proline-containing substrates. Biochim Et Biophys Acta. 1984;791:87-97.
Kaufman G, Whitescarver RA, Nunes L, Palmer XL, Skrtic D, Tutak W. Effects of protein-coated nanofibers on conformation of gingival fibroblast spheroids: potential utility for connective tissue regeneration. Biomed Mater. 2018;13:025006.
Graves DT, Oskoui M, Volejnikova S, et al. Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J Dent Res. 2001;80:1875-1879.
Jian CX, Li MZ, Zheng WY, et al. Tormentic acid inhibits LPS-induced inflammatory response in human gingival fibroblasts via inhibition of TLR4-mediated NF-kappaB and MAPK signalling pathway. Arch Oral Biol. 2015;60:1327-1332.
Scheres N, Crielaard W. Gingival fibroblast responsiveness is differentially affected by Porphyromonas gingivalis: implications for the pathogenesis of periodontitis. Mol Oral Microbiol. 2013;28:204-218.
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.
Morin MP, Grenier D. Regulation of matrix metalloproteinase secretion by green tea catechins in a three-dimensional co-culture model of macrophages and gingival fibroblasts. Arch Oral Biol. 2017;75:89-99.
Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 1991;66:807-815.
Fruman DA, Burakoff SJ, Bierer BE. Immunophilins in protein folding and immunosuppression. Faseb J. 1994;8:391-400.
Colgan J, Asmal M, Neagu M, et al. Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity. 2004;21:189-201.
Brazin KN, Mallis RJ, Fulton DB, Andreotti AH. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. PNAS. 2002;99:1899-1904.
Kim SH, Lessner SM, Sakurai Y, Galis ZS. Cyclophilin A as a novel biphasic mediator of endothelial activation and dysfunction. Am J Pathol. 2004;164:1567-1574.
Suzuki J, Jin ZG, Meoli DF, Matoba T, Berk BC. Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells. Circ Res. 2006;98:811-817.
Dawar FU, Wu J, Zhao L, Khattak MN, Mei J, Lin L. Updates in understanding the role of cyclophilin A in leukocyte chemotaxis. J Leukocyte Biol. 2017;101:823-826.
Halliday MR, Rege SV, Ma Q, et al. Accelerated pericyte degeneration and blood-brain barrier breakdown in apolipoprotein E4 carriers with Alzheimer's disease. J Cerebral Blood Flow Metab. 2016;36:216-227.
Yang Y, Lu N, Zhou J, Chen ZN, Zhu P. Cyclophilin A up-regulates MMP-9 expression and adhesion of monocytes/macrophages via CD147 signalling pathway in rheumatoid arthritis. Rheumatology. 2008;47:1299-1310.
Melchior A, Denys A, Deligny A, Mazurier J, Allain F. Cyclophilin B induces integrin-mediated cell adhesion by a mechanism involving CD98-dependent activation of protein kinase C-delta and p44/42 mitogen-activated protein kinases. Exp Cell Res. 2008;314:616-628.
Santiago-Gomez A, Barrasa JI, Olmo N, et al. 4F2hc-silencing impairs tumorigenicity of HeLa cells via modulation of galectin-3 and beta-catenin signaling, and MMP-2 expression. Biochim Biophys Acta. 2013;1833:2045-2056.
Kuo PJ, Tu HP, Chin YT, et al. Cyclosporine-A inhibits MMP-2 and -9 activities in the presence ofPorphyromonas gingivalis lipopolysaccharide: an experiment in human gingival fibroblast and U937 macrophage co-culture. J Periodontal Res. 2012;47:431-438.
Sundstrom C, Nilsson K. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer. 1976;17:565-577.
Lehmann MH. Recombinant human granulocyte-macrophage colony-stimulating factor triggers interleukin-10 expression in the monocytic cell line U937. Mol Immunol. 1998;35:479-485.
Liu L, Li C, Cai C, Xiang J, Cao Z. Cyclophilin A (CypA) is associated with the inflammatory infiltration and alveolar bone destruction in an experimental periodontitis. Biochem Biophys Res Commun. 2010;391:1000-1006.
Liu L, Li C, Xiang J, Dong W, Cao Z. Over-expression and potential role of cyclophilin A in human periodontitis. J Periodontal Res. 2013;48:615-622.
Xue L, Su L, Zhao L, Li J, Du Y, Yu X. Cyclophilin a increases CD68(+) cell infiltration in rat experimental periodontitis. J Mol Histol. 2018;49:157-164.
Herath TD, Darveau RP, Seneviratne CJ, Wang CY, Wang Y, Jin L. Heterogeneous Porphyromonas gingivalis LPS modulates immuno-inflammatory response, antioxidant defense and cytoskeletal dynamics in human gingival fibroblasts. Sci Rep. 2016;6:29829.
Piehler AP, Grimholt RM, Ovstebo R, Berg JP. Gene expression results in lipopolysaccharide-stimulated monocytes depend significantly on the choice of reference genes. BMC Immunol. 2010;11:21.
Sherry B, Yarlett N, Strupp A, Cerami A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. PNAS. 1992;89:3511-3515.
Tanabe SI, Grenier D. Macrophage tolerance response to Aggregatibacter actinomycetemcomitans lipopolysaccharide induces differential regulation of tumor necrosis factor-alpha, interleukin-1 beta and matrix metalloproteinase 9 secretion. J Periodontal Res. 2008;43:372-377.
Spottl T, Hausmann M, Kreutz M, et al. Monocyte differentiation in intestine-like macrophage phenotype induced by epithelial cells. J Leukocyte Biol. 2001;70:241-251.
Zhu Y, Skold CM, Liu X, et al. Fibroblasts and monocyte macrophages contract and degrade three-dimensional collagen gels in extended co-culture. Respir Res. 2001;2:295-299.
Tegeder I, Schumacher A, John S, et al. Elevated serum cyclophilin levels in patients with severe sepsis. J Clin Immunol. 1997;17:380-386.
Wang L, Wang CH, Jia JF, et al. Contribution of cyclophilin A to the regulation of inflammatory processes in rheumatoid arthritis. J Clin Immunol. 2010;30:24-33.
Jin ZG, Melaragno MG, Liao DF, et al. Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ Res. 2000;87:789-796.
Coppinger JA, Cagney G, Toomey S, et al. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood. 2004;103:2096-2104.
Xue C, Sowden MP, Berk BC. Extracellular and intracellular cyclophilin a, native and post-translationally modified, show diverse and specific pathological roles in diseases. Arterioscler Thromb Vasc Biol. 2018;38:986-993.
Ke H, Huai Q. Crystal structures of cyclophilin and its partners. Front Biosci. 2004;9:2285-2296.
Rots NY, Iavarone A, Bromleigh V, Freedman LP. Induced differentiation of U937 cells by 1,25-dihydroxyvitamin D3 involves cell cycle arrest in G1 that is preceded by a transient proliferative burst and an increase in cyclin expression. Blood. 1999;93:2721-2729.