The complex interplay between Mycoplasma synoviae and chicken chondrocytes (CCH), which come into direct contact during infectious synovitis, has been examined at the level of gene expression. Our previous studies demonstrated a significant influence of M. synoviae on the level of CCH gene expression. Here, we show for the first time that in vitro co-cultivation of M. synoviae and CCH also induces upregulation of gene expression in this mycoplasma. We observed significantly increased expression of genes important for M. synoviae pathogenicity, including cysteine protease cysP, neuraminidase nanH, haemagglutinin vlhA, and the putative nuclease MS53_0284. Moreover, the pattern of gene expression was dependent on the infection environment. In CCH, significant changes in the expression of genes encoding catabolic enzymes of the cartilage extracellular matrix (cathepsins B, K and L, aggrecanase ADAM10, and matrix metalloproteinase MMP2) were demonstrated. Infection of CCH with M. synoviae also elevated the expression of the gene encoding peptidyl arginine deiminase, type III (PADI3), which is responsible for the post-translational citrullination of proteins.
Bartok, B. and Firestein, G. S. (2010): Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol. Rev. 233, 233–255.
Bercic, R. L., Cizelj, I., Dušanic, D., Narat, M., Zorman-Rojs, O., Dovc, P. and Bencina, D. (2011): Neuraminidase of Mycoplasma synoviae desialylates heavy chain of the chicken immunoglobulin G and glycoproteins of chicken tracheal mucus. Avian Pathol. 40, 299–308.
Cecchini, K. R., Gorton, T. S. and Geary, S. J. (2007): Transcriptional responses of Mycoplasma gallisepticum strain R in association with eukaryotic cells. J. Bacteriol. 189, 5803–5807.
Cizelj, I., Bercic, R. L., Dušanic, D., Narat, M., Kos, J., Dovc, P. and Bencina, D. (2011): Mycoplasma gallisepticum and Mycoplasma synoviae express a cysteine protease CysP, which can cleave chicken IgG into Fab and Fc. Microbiology 157, 362–372.
Dušanic, D., Bencina, D., Oven, I., Cizelj, I., Bencina, M. and Narat, M. (2012): Mycoplasma synoviae induces upregulation of apoptotic genes, secretion of nitric oxide and appearance of an apoptotic phenotype in infected chicken chondrocytes. Vet. Res. 43, 7.
Dušanic, D., Bercic, R. L., Cizelj, I., Salmic, S., Narat, M. and Bencina, D. (2009): Mycoplasma synoviae invades non-phagocytic chicken cells in vitro. Vet. Microbiol. 138, 114–119.
Goldring, M. B. and Marcu, K. B. (2009): Cartilage homeostasis in health and rheumatic diseases. Arthritis Res. Ther. 11, 224.
Hallamaa, K. M., Tang, S. L., Ficorilli, N. and Browning, G. F. (2008): Differential expression of lipoprotein genes in Mycoplasma pneumoniae after contact with human lung epithelial cells, and under oxidative and acidic stress. BMC Microbiol. 8, 124.
Kerr, K. M. and Olson, N. O. (1970): Pathology of chickens inoculated experimentally or contactinfected with Mycoplasma synoviae. Avian Dis. 14, 290–320.
Lockaby, S. B., Hoerr, F. J., Lauerman, L. H. and Kleven, S. H. (1998): Pathogenicity of Mycoplasma synoviae in broiler chickens. Vet. Pathol. 35, 178–190.
Morrow, C. J., Whithear, K. G. and Kleven, S. H. (1990): Restriction endonuclease analysis of Mycoplasma synoviae strains. Avian Dis. 34, 611–616.
Narat, M., Bencina, D., Kleven, S. H. and Habe, F. (1998): The hemagglutination-positive phenotype of Mycoplasma synoviae induces experimental infectious synovitis in chickens more frequently than does the hemagglutination-negative phenotype. Infect. Immun. 66, 6004–6009.
Noormohammadi, A. H., Markham, P. F., Whithear, K. G., Walker, I. D., Gurevich, V. A., Ley, D. H. and Browning, G. F. (1997): Mycoplasma synoviae has two distinct phase-variable major membrane antigens, one of which is a putative hemagglutinin. Infect. Immun. 65, 2542–2547.
Novak, J. F., Hayes, J. D. and McMaster, J. H. (1995): Mycoplasma-mediated bone resorption in bone organ cultures. Microbios 81, 241–260.
Pfaffl, M. W. (2001): A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
Razin, S., Yogev, D. and Naot, Y. (1998): Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62, 1094–1156.
Rodwell, A. W. and Whitcomb, R. F. (1983): Methods for direct and indirect measurement of mycoplasma growth. In: Tully, J. G. and Razin, S. (eds) Methods in Mycoplasmology. Academic Press, New York–London. pp. 185–196.
Uysal, H., Nandakumar, K. S., Kessel, C., Haag, S., Carlsen, S., Burkhardt, H. and Holmdahl, R. (2010): Antibodies to citrullinated proteins: molecular interactions and arthritogenicity. Immunol. Rev. 233, 9–33.
Vasconcelos, A. T., Ferreira, H. B., Bizarro, C. V., Bonatto, S. L., Carvalho, M. O., Pinto, P. M., Almeida, D. F., Almeida, L. G., Almeida, R., Alves-Filho, L., Assuncao, E. N., Azevedo, V. A., Bogo, M. R., Brigido, M. M., Brocchi, M., Burity, H. A., Camargo, A. A., Camargo, S. S., Carepo, M. S., Carraro, D. M., de Mattos Cascardo, J. C., Castro, L. A., Cavalcanti, G., Chemale, G., Collevatti, R. G., Cunha, C. W., Dallagiovanna, B., Dambros, B. P., Dellagostin, O. A., Falcao, C., Fantinatti-Garboggini, F., Felipe, M. S., Fiorentin, L., Franco, G. R., Freitas, N. S., Frias, D., Grangeiro, T. B., Grisard, E. C., Guimaraes, C. T., Hungria, M., Jardim, S. N., Krieger, M. A., Laurino, J. P., Lima, L. F., Lopes, M. I., Loreto, E. L., Madeira, H. M., Manfio, G. P., Maranhao, A. Q., Martinkovics, C. T., Medeiros, S. R., Moreira, M. A., Neiva, M., Ramalho-Neto, C. E., Nicolas, M. F., Oliveira, S. C., Paixao, R. F., Pedrosa, F. O., Pena, S. D., Pereira, M., Pereira-Ferrari, L., Piffer, I., Pinto, L. S., Potrich, D. P., Salim, A. C., Santos, F. R., Schmitt, R., Schneider, M. P., Schrank, A., Schrank, I. S., Schuck, A. F., Seuanez, H. N., Silva, D. W., Silva, R., Silva, S. C., Soares, C. M., Souza, K. R., Souza, R. C., Staats, C. C., Steffens, M. B., Teixeira, S. M., Urmenyi, T. P., Vainstein, M. H., Zuccherato, L. W., Simpson, A. J. and Zaha, A. (2005): Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J. Bacteriol. 187, 5568–5577.
Vossenaar, E. R., Radstake, T. R., van der Heijden, A., van Mansum, M. A., Dieteren, C., de Rooij, D. J., Barrera, P., Zendman, A. J. and van Venrooij, W. J. (2004): Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages. Ann. Rheum. Dis. 63, 373–381.
Yamada, R. (2005): Peptidylarginine deiminase type 4, anticitrullinated peptide antibodies, and rheumatoid arthritis. Autoimmun. Rev. 4, 201–206.