Mycoplasma synoviae induces upregulation of apoptotic genes, secretion of nitric oxide and appearance of an apoptotic phenotype in infected chicken chondrocytes

Veterinary Research

Volumn 43, Issue 1, 2012, Pages

  Dusanic, Daliborka ^a   Bencina, Dusan ^a   Oven, Irena ^a   Cizelj, Ivanka ^a   Bencina, Mojca ^b   Narat, Mojca ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); GALLUS GALLUS; MYCOPLASMA; MYCOPLASMA SYNOVIAE; MYCOPLASMATALES;

2,3 BIS(2 METHOXY 4 NITRO 5 SULFOPHENYL) 5 ((PHENYLAMINO)CARBONYL) 2H TETRAZOLIUM HYDROXIDE; 2,3-BIS(2-METHOXY-4-NITRO-5-SULFOPHENYL)-5-((PHENYLAMINO)CARBONYL)-2H-TETRAZOLIUM HYDROXIDE; NITRIC OXIDE; TETRAZOLIUM;

ANIMAL; ANIMAL DISEASE; APOPTOSIS; ARTICLE; BIRD DISEASE; CARTILAGE CELL; CELL CULTURE; CHICKEN; CONFOCAL MICROSCOPY; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; JURKAT CELL LINE; METABOLISM; MICROBIOLOGY; MYCOPLASMA SYNOVIAE; MYCOPLASMOSIS; PHASE CONTRAST MICROSCOPY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TIME;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CHICKENS; CHONDROCYTES; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROSCOPY, PHASE-CONTRAST; MYCOPLASMA INFECTIONS; MYCOPLASMA SYNOVIAE; NITRIC OXIDE; POULTRY DISEASES; REAL-TIME POLYMERASE CHAIN REACTION; TETRAZOLIUM SALTS; TIME FACTORS;

EID: 84858145677     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/1297-9716-43-7     Document Type: Article

References (58)

1. Pathogenicity of Mycoplasma synoviae in broiler chickens. Lockaby SB, Hoerr FJ, Lauerman LH, Kleven SH, Vet Pathol 1998 35 178 190 10.1177/030098589803500303 9598581 (Pubitemid 129548054)
2. Factors associated with virulence of Mycoplasma synoviae. Lockaby SB, Hoerr FJ, Lauerman LH, Smith BF, Samoylov AM, Tolvio-Kinnucan MA, Kleven SH, Avian Dis 1999 43 251 261 10.2307/1592615 10396638 (Pubitemid 29303304)
3. Virulence of Mycoplasma strains in experimentally infected broiler chickens. Hinz KH, Blome C, Ryll M, Berl Munch Tierartzl Wochenschr 2003 116 59 66 (Pubitemid 36144664)
4. Mycoplasma synoviae infection. Kleven SH, Diseases of Poultry Ames: Iowa State University Press, Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR, Swayne DE, 11 2003 756 766
5. The hemagglutination-positive phenotype of Mycoplasma synoviae induces experimental infectious synovitis in chickens more frequently than does the hemagglutination-negative phenotype. Narat M, Benina D, Kleven SH, Habe F, Infect Immun 1998 66 6004 6009 9826385 (Pubitemid 28531865)
6. Localisation of Mycoplasma pulmonis in cartilage. Kohn DF, Magill LS, Chinookoswong N, Infect Immun 1982 35 730 733 7056583
7. Experimental arthritis in rats produced by Mycoplasma arthritidis. Hill A, Dagnal GJR, J Comp Pathol 1975 85 45 52 10.1016/0021-9975(75)90083-3 1092737
8. Mycoplasma synoviae invades non-phagocytic chicken cells in vitro. Duani D, Beri RL, Cizelj I, Salmi S, Narat M, Benina D, Vet Microbiol 2009 138 114 119 10.1016/j.vetmic.2009.02.014 19321273
9. Nitric oxide causes anoikis through attenuation of E-cadherin and activation of caspase-3 in human gastric carcinoma AZ-521 cells infected with Mycoplasma hyorhinis. Obara H, Harasawa R, J Vet Med Sci 2010 72 869 874 10.1292/jvms.09-0573 20179380
10. Invasion of bovine peripheral-blood mononuclear cells and erythrocytes by Mycoplasma bovis. Van der Merwe J, Prysliak T, Perez-Casal J, Infect Immun 2010 78 4570 4578 10.1128/IAI.00707-10 20713619
11. Mycoplasma bovis induces apoptosis of bovine lymphocytes. Vanden Bush TJ, Rosenbusch RF, FEMS Immunol Med Microbiol 2002 32 97 103 10.1111/j.1574-695X. 2002.tb00540.x 11821230 (Pubitemid 34124107)
12. Mycoplasma fermentans inhibits tumor necrosis factor -induced apoptosis in the myelomonocytic U937 cell line. Gerlic M, Horowitz J, Horowitz S, Cell Death Differ 2004 11 1204 1212 10.1038/sj.cdd.4401482 15286682 (Pubitemid 39529963)
13. Mycoplasma fermentans infection promotes immortalization of human peripheral blood mononuclear cells in culture. Zhang S, Tsai S, Wu TT, Li B, Shih JW, Lo SC, Blood 2004 104 4252 4259 10.1182/blood-2004-04-1245 15331449 (Pubitemid 39620180)
14. Effect of Mycoplasmas on apoptosis of 32D cells is species.dependent. Zhang S, Lo SC, Curr Microbiol 2007 54 388 395 10.1007/s00284-006-0491-x 17486403 (Pubitemid 46733875)
15. Mycoplasma fermentans glycolipid-antigen as a pathogen in rheumatoid arthritis. Kawahito Y, Ichinose S, Sano H, Tsubouchi Y, Kohno M, Yoshikawa T, Tokunaga D, Hojo T, Harasawa R, Nakano T, Matsuda K, Biochem Biophys Res Commun 2008 369 561 566 10.1016/j.bbrc.2008.02.079 18307980
16. Role of sialidase in Mycoplasma alligatoris-induced pulmonary fibroblast apoptosis. Hunt ME, Brown DR, Vet Microbiol 2007 121 73 82 10.1016/j.vetmic. 2006.10.009 17276629
17. OppA, the ecto-ATPase of Mycoplasma hominis induces ATP release and cell death in HeLa cells. Hopfe M, Henrich B, BMC Microbiol 2008 8 55 10.1186/1471-2180-8-55 18394151 (Pubitemid 351551359)
18. Apoptosis induced by lipid-associated membrane proteins from Mycoplasma penetrans is mediated by nuclear factor B activation in mouse macrophage. Zeng Y, Wu Y, Deng Z, You X, Zhu C, Yu M, Wan Y, Can J Microbiol 2008 54 150 158 10.1139/W07-125 18388985 (Pubitemid 351302684)
19. Mycoplasma infection with M. arginini results in NF-B constitutive activation and inhibition of apoptosis in cells expressing Toll-like receptors TLR2/6. Shcheblyakov DV, Logunov DY, Zubkova OV, Shmarov MM, Rakovskaya IV, Naroditskii BS, Gintsburg AL, Gudkov AV, Mol Gen Mikrobiol Virusol 2008 23 163 167
20. Mycoplasma infection supresses p53, activates NF-B and cooperates with oncogenic Ras in rodent fibroblast transformation. Logunov DY, Scheblyakov DV, Zubkova OV, Shmarov MM, Rakovskaya IV, Gurova KV, Tararova ND, Burdelya LG, Naroditsky BS, Ginzburg AL, Gudkov AV, Oncogene 2008 27 4521 4531 10.1038/onc.2008.103 18408766
21. Mycoplasma genitalium lipoproteins induce human monocytic cell expression of proinflammatory cytokines and apoptosis by activating nuclear factor B. Wu Y, Qiu H, Zeng Y, You X, Deng Z, Yu M, Zhu C, Mediators Inflamm 2008 2008 195427 18464921
22. Mycoplasmal infections prevent apoptosis and induce malignant transformation of interleukin-3-dependent 32D hematopoietic cells. Feng SH, Tsai S, Rodriguez J, Lo SC, Mol Cel Biol 1999 19 7995 8002 (Pubitemid 30413994)
23. An induced proximity model for caspase-8 activation. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM, J Biol Chem 1998 273 2926 2930 10.1074/jbc.273.5.2926 9446604 (Pubitemid 28133943)
24. The CASBAH: a searchable database of caspase substrates. Lüthi AU, Martin SJ, Cell Death Differ 2007 14 641 650 10.1038/sj.cdd.4402103 17273173 (Pubitemid 46444502)
25. Apoptosis: controlled demolition at the cellular level. Taylor RC, Cullen SP, Martin SJ, Nat Rev Mol Cell Biol 2008 9 231 241 18073771 (Pubitemid 351301823)
26. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. Arnoult D, Gaume B, Karbowski M, Sharpe J, Cecconi F, Youle RJ, EMBO J 2003 22 4385 4399 10.1093/emboj/cdg423 12941691 (Pubitemid 37087193)
27. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. Bossy-Wetzel E, Newmeyer DD, Green DR, EMBO J 1998 17 37 49 10.1093/emboj/17.1.37 9427739 (Pubitemid 28041046)
28. Lduring apoptosis. Hsu YT, Wolter KG, Youle RJ, Proc Natl Acad Sci USA 1997 94 3668 3672 10.1073/pnas.94.8.3668 9108035 (Pubitemid 27180430)
29. Chondrocyte apoptosis induced by nitric oxide. Blanco FJ, Ochs RL, Schwartz H, Lotz M, Am J Pathol 1995 146 75 85 7856740
30. Synovial fluid and peripheral blood immune complexes of patients with rheumatoid arthritis induce apoptosis in cytokine-activated chondrocytes. Schuerwegh AJ, Dombrecht EJ, Stevens WJ, Van Offel JF, Kockx MM, Bridts CH, De Clerck LS, Rheumatol Int 2007 27 901 909 10.1007/s00296-007-0336-3 17404735 (Pubitemid 47084244)
31. The role of nitric oxide in articular cartilage damage. Lotz M, Rheum Dis Clin North Am 1999 25 269 282 10.1016/S0889-857X(05)70067-3 10356417 (Pubitemid 29267883)
32. Nitric oxide: an important articular free radical. Murel GA, Doland MM, Jang D, Szabo C, Warren RF, Hannafin JA, J Bone Joint Surg Am 1996 78 265 274 8609118 (Pubitemid 26058799)
33. Chondrocyte apoptosis in experimental osteoarthritis is mediated by MEK 1/2 and p38 pathways: role of cyclooxygenase-2 and inducible nitric oxide synthase. Pelletier JP, Fernandes JC, Jovanovic DV, Reboul P, Martel-Pelletier J, J Rheumatol 2001 28 2509 2519 11708426 (Pubitemid 33031984)
34. ERK-1/2 and p38 kinase oppositely regulate nitric oxide-induced apoptosis of chondrocytes in association with p53, caspase-3 and differentiation status. Kim SJ, Ju JW, Oh CD, Yoon YM, Song WK, Kim JH, Yoo YJ, Bang OS, Kang SS, Chun JS, J Biol Chem 2002 277 1332 1339 10.1074/jbc.M107231200 11689560 (Pubitemid 34968887)
35. CD95-induced osteoarthritic chondrocyte apoptosis and necrosis: dependency on p38 mitogen-activated protein kinase. Wei L, Sun XJ, Wang Z, Chen Q, Arthritis Res Ther 2006 8 37 10.1186/ar1891 16469115
36. Methods for direct and indirect measurement of mycoplasma growth Methods in Mycoplasmology. Rodwell AW, Whitcomb RF, Academic Press, Razin S, Tully JG, 1983 1 185 196
37. CD44 is the physiological trigger of Fas up-regulation on rheumatoid synovial cells. Fuji K, Fuji Y, Hubscher S, Tanaka Y, J Immunol 2001 167 1198 1203 11466334 (Pubitemid 32703113)
38. National Center for Biotechnology Information/Primer-BLAST. http://www.ncbi.nlm.nih.gov/tools/primer-blast/index.cgi?LINK-LOC=BlastHome
39. Gene expression profiling of avian macrophage activation. Bliss T, Dohms JE, Emara MG, Keeler CL Jr, Vet Immunol Immunopathol 2005 105 289 299 10.1016/j.vetimm.2005.02.013 15808307 (Pubitemid 40460952)
40. Selection of reliable reference genes for qPCR studies on chondroprotective action. Toegel S, Huang W, Piana C, Unger FM, Wirth M, Goldring MB, Gabor F, Viernstein H, BMC Mol Biol 2007 8 13 10.1186/1471-2199-8- 13 17324259 (Pubitemid 46416840)
41. A new mathematical model for relative quantification in real-time RT-PCR. Pfaffl MW, Nucleic acids Res 2001 29 45 10.1093/nar/29.9.e45 11328886
42. Standardization of real-time PCR gene expression data from independent biological replicates. Willems E, Leyns L, Vandesompele J, Anal Biochem 2008 379 127 129 10.1016/j.ab.2008.04.036 18485881
43. Apoptotic chondrocyte death in rheumatoid arthritis. Kim HA, Song YW, Arthritis Rheum 1999 42 1528 1537 10.1002/1529-0131(199907)42:7<1528::AID- ANR28>3.0.CO;2-9 10403282 (Pubitemid 30265612)
44. Induced apoptosis of chondrocytes by Porphyromonas gingivalis as a possible pathway for cartilage loss in rheumatoid arthritis. Röhner E, Detert J, Kolar P, Hocke A, N'Guessan P, Matziolis G, Kanitz V, Bernimoulin JP, Kielbassa A, Burmester GR, Buttgereit F, Pischon N, Calcif Tissue Int 2010 87 333 340 10.1007/s00223-010-9389-5 20582408
45. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Wegner N, Lundbreg K, Kinloch A, Ficher B, Malmström V, Feldman M, Venables PJ, Immunol Rev 2010 233 34 54 10.1111/j.0105-2896.2009.00850.x 20192991
46. Presence of bacterial DNA and bacterial peptydoglycans in joints of patients with rheumatoid arthritis and other arthritidies. Van Der Heijden IM, Wilbrink B, Tchetverikov I, Schrijver A, Schouls LM, Hazenberg MP, Breedveld FC, Tak PP, Arthritis Rheum 2000 43 593 598 10.1002/1529-0131(200003)43:3<593:: AID-ANR16>3.0.CO;2-1 10728753 (Pubitemid 30394951)
47. Regulatory natural autoantibodies to apoptotic cells: pallbearers and protectors. Silverman G, Arthritis Rheum 2011 63 597 602 21360488
48. Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis. Hashimoto S, Ochs RL, Komiya S, Lotz M, Arthritis Rheum 1998 41 1632 1638 10.1002/1529-0131(199809)41:9<1632::AID-ART14>3.0.CO;2-A 9751096 (Pubitemid 28459922)
49. Detection of mycoplasmal infections in blood of patients with rheumatoid arthritis. Haier J, Nasralla M, Franco AR, Nicolson GL, Rheumatology 1999 38 504 509 10.1093/rheumatology/38.6.504 10402069 (Pubitemid 29504834)
50. Systematic detection of mycoplasmas by culture and polimerase chain reaction (PCR) procedures in 209 synovial fluid samples. Schaeverbeke T, Renaudin H, Clerc M, Lequen L, Vernhes JP, De Barbeyrac B, Bannwarth B, Bèbèar C, Dehais J, Br J Rheumatol 1997 36 310 314 10.1093/rheumatology/36.3.310 9133961
51. Mycoplasma fermentans in rheumatoid arthritis and other inflammatory arthritidies. Horowitz S, Evinson B, Borer A, Horowitz J, J Rheumatol 2000 12 2747 2753
52. The prevalence of Mycoplasma fermentans in patients with inflammatory arthritidies. Gilroy CB, Keat A, Taylor-Robinson D, Rheumatology 2001 40 1355 1358 10.1093/rheumatology/40.12.1355 11752504
53. Relationship between rheumatoid arthritis and Mycoplasma pneumoniae: a case-control study. Ramírez AS, Rosas A, Hernández-Beriain JA, Orengo JC, Saavedra P, de la Fe C, Fernández A, Poveda JB, Rheumatology 2005 44 912 914 10.1093/rheumatology/keh630 15814575 (Pubitemid 41511188)
54. Distribution of Mycoplasma pneumoniae and Mycoplasma salivarium in the synovial fluids of arthritis patients. Johnson SM, Bruckner F, Collins D, J Clin Microbiol 2007 45 953 957 10.1128/JCM.01973-06 17122006 (Pubitemid 46427717)
55. Pathology of chickens inoculated experimentally or contact-infected with Mycoplasma synoviae. Kerr KM, Olson O, Avian Dis 1970 14 290 320 5427236
56. Neuraminidase of Mycoplasma synoviae desialylates heavy chain of the chicken immunoglobulin G and glycoproteins of chicken tracheal mucus. Beri RL, Cizelj I, Duani D, Narat M, Zorman-Rojs O, Dov P, Benina D, Avian Pathol 2011 40 299 308 10.1080/03079457.2011.565311 21711189
57. Mycoplasma synoviae lipoprotein MSPB, the N-terminal part of VlhA haemagglutinin, induces secretion of nitric oxide, IL-6 and IN1beta in chicken macrophages. Lavri M, Benina D, Kothlow S, Kaspers B, Narat M, Vet Microbiol 2007 121 278 287 10.1016/j.vetmic.2006.12.005 17254721 (Pubitemid 46413609)
58. 5-fluorouracil induces Fas upregulation associated with apoptosis in liver metastases of colorectal cancer patients. Backus HHJ, Dukers DF, van Groeningen CJ, Vos W, Bloemena E, Wouters D, van Riel JMGH, Smid K, Giaccone G, Pinedo HM, Peters GJ, Ann Oncol 2001 12 209 216 10.1023/A:1008331525368 11300326 (Pubitemid 32223870)