Mycoplasma hyopneumoniae variability: Current trends and proposed terminology for genomic classification.
Mycoplasma hyopneumoniae
Variable Number Tandem Repeats
genomic classification
terminology
variability
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Sep 2019
Sep 2019
Historique:
received:
25
03
2019
revised:
04
05
2019
accepted:
13
05
2019
pubmed:
18
5
2019
medline:
18
12
2019
entrez:
18
5
2019
Statut:
ppublish
Résumé
Mycoplasma hyopneumoniae (M. hyopneumoniae) is the aetiologic agent of enzootic pneumonia in swine, a prevalent chronic respiratory disease worldwide. Mycoplasma hyopneumoniae is a small, self-replicating microorganism that possesses several characteristics allowing for limited biosynthetic abilities, resulting in the fastidious, host-specific growth and unique pathogenic properties of this microorganism. Variation across several isolates of M. hyopneumoniae has been described at antigenic, proteomic, transcriptomic, pathogenic and genomic levels. The microorganism possesses a minimal number of genes that regulate the transcription process. Post-translational modifications (PTM) occur frequently in a wide range of functional proteins. The PTM by which M. hyopneumoniae regulates its surface topography could play key roles in cell adhesion, evasion and/or modulation of the host immune system. The clinical outcome of M. hyopneumoniae infections is determined by different factors, such as housing conditions, management practices, co-infections and also by virulence differences among M. hyopneumoniae isolates. Factors contributing to adherence and colonization as well as the capacity to modulate inflammatory and immune responses might be crucial. Different components of the cell membrane (i.e. proteins, glycoproteins and lipoproteins) may serve as adhesins and/or be toxic for the respiratory tract cells. Mechanisms leading to virulence are complex and more research is needed to identify markers for virulence. The utilization of typing methods and complete or partial-gene sequencing for M. hyopneumoniae characterization has increased in diagnostic laboratories as control and elimination strategies for this microorganism are attempted worldwide. A commonly employed molecular typing method for M. hyopneumoniae is Multiple-Locus Variable number tandem repeat Analysis (MLVA). The agreement of a shared terminology and classification for the various techniques, specifically MLVA, has not been described, which makes inferences across the literature unsuitable. Therefore, molecular trends for M. hyopneumoniae have been outlined and a common terminology and classification based on Variable Number Tandem Repeats (VNTR) types has been proposed.
Substances chimiques
Adhesins, Bacterial
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1840-1854Informations de copyright
© 2019 Blackwell Verlag GmbH.
Références
Ameri, M., Zhou, E. M., & Hsu, W. H. (2006). Western blot immunoassay as a confirmatory test for the presence of anti-Mycoplasma hyopneumoniae antibodies in swine serum. Journal of Veterinary Diagnostic Investigation, 18, 198-201. https://doi.org/10.1177/104063870601800210
Artiushin, S., & Minion, F. (1996). Arbitrarily primed PCR analysis of Mycoplasma hyopneumoniae field isolates demonstrates genetic heterogeneity. International Journal of Systemic Bacteriology, 46(1), 324-328. https://doi.org/10.1099/00207713-46-1-324
Assunção, P., De la Fe, C., Ramírez, A. S., González Llamazares, O., & Poveda, J. B. (2005). Protein and antigenic variability among Mycoplasma hyopneumoniae strains by SDS-PAGE and immunoblot. Veterinary Research Communications, 29, 563-574. https://doi.org/10.1007/s11259-005-3083-5
Bereiter, M., Young, T. F., Joo, H. S., & Ross, R. F. (1990). Evaluation of the ELISA, and comparison to the complement fixation test and radial immunodiffusion enzyme assay for detection of antibodies against Mycoplasma hyopneumoniae in swine serum. Veterinary Microbiology, 25, 177-192. https://doi.org/10.1016/0378-1135(90)90075-7
Bogema, D. R., Deutscher, A. T., Woolley, L. K., Seymour, L. M., Raymond, B. B. A., Tacchi, J. L., … Djordjevic, S. P. (2012). Characterization of cleavage events in the multifunctional cilium adhesin Mhp684 (P146) reveals a mechanism by which Mycoplasma hyopneumoniae regulates surface topography. MBio, 3(2), e00282-311. https://doi.org/10.1128/mBio.00282-11
Bogema, D., Scott, N., Padula, M., Tacchi, J., Raymond, B., Jenkins, C., & Djordjevic, S. (2011). Sequence TTKF ↓ QE defines the site of proteolytic cleavage in Mhp683 protein, a novel glycosaminoglycan and cilium adhesin of Mycoplasma hyopneumoniae. Journal of Biological Chemistry, 286(48), 41217-41229. https://doi.org/10.1074/jbc.M111.226084
Calus, D., Baele, M., Meyns, T., de Kruif, A., Butaye, P., Decostere, A., … Maes, D. (2007). Protein variability among Mycoplasma hyopneumoniae isolates. Veterinary Microbiology, 120, 284-291. https://doi.org/10.1016/j.vetmic.2006.10.040
Calus, D., Maes, D., Vranckx, K., Villarreal, I., Pasmans, F., & Haesebrouck, F. (2010). Validation of ATP luminometry for rapid and accurate titration of Mycoplasma hyopneumoniae in Friis medium and a comparison with the color changing units assay. Journal of Microbiological Methods, 83, 335-340. https://doi.org/10.1016/j.mimet.2010.09.001
Charlebois, A., Marois-Créhan, C., Hélie, P., Gagnon, C. A., Gottschalk, M., & Archambault, M. (2014). Genetic diversity of Mycoplasma hyopneumoniae isolates of abattoir pigs. Veterinary Microbiology, 168, 348-356. https://doi.org/10.1016/j.vetmic.2013.11.006
Chen, J. W., Zhang, L., Song, J., Hwang, F., Dong, Q., Liu, J., & Qian, Y. (1992). Comparative analysis of glycoprotein and glycolipid composition of virulent and avirulent strain membranes of Mycoplasma hyopneumoniae. Current Microbiology, 24, 189-192. https://doi.org/10.1007/BF01579280
de Castro, L. A., Pedroso, T. R., Kuchiishi, S. S., Ramenzoni, M., Kich, J. D., Zaha, A., … Ferreira, H. B. (2006). Variable number of tandem aminoacid repeats in adhesion-related CDS products in Mycoplasma hyopneumoniae strains. Veterinary Microbiology, 116, 258-269. https://doi.org/10.1016/j.vetmic.2006.04.022
Debey, M. C., Jacobson, C. D., & Ross, R. F. (1992). Histochemical and morphologic changes of porcine airway epithelial cells in response to infection with Mycoplasma hyopneumoniae. American Journal of Veterinary Research, 53(9), 1705-1710.
DeBey, M., & Ross, R. (1994). Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ cultures. Infection and Immunity, 62, 5312-5318.
Degrange, S., Cazanave, C., Charron, A., Renaudin, H., Bebear, C., & Bebear, C. M. (2009). Development of multiple-locus variable-number tandem-repeat analysis for molecular typing of Mycoplasma pneumoniae. Journal of Clinical Microbiology, 47(4), 914-923. https://doi.org/10.1128/JCM.01935-08
Deutscher, A. T., Jenkins, C., Minion, F. C., Seymour, L. M., Padula, M. P., Dixon, N. E., … Djordjevic, S. P. (2010). Repeat regions R1 and R2 in the P97 paralogue Mhp271 of Mycoplasma hyopneumoniae bind heparin, fibronectin and porcine cilia. Molecular Microbiology, 78, 444-458. https://doi.org/10.1111/j.1365-2958.2010.07345.x
Deutscher, A., Tacchi, J., Minion, F., Padula, M., Crossett, B., Bogema, D., & Djordjevic, S. (2012). Mycoplasma hyopneumoniae Surface proteins Mhp385 and Mhp384 bind host cilia and glycosaminoglycans and are endoproteolytically processed by proteases that recognize different cleavage motifs. Journal of Proteome Research, 11, 1924-1936. https://doi.org/10.1021/pr201115v
Diaz, M. H., & Winchell, J. M. (2016). The evolution of advanced molecular diagnostics for the detection and characterization of Mycoplasma pneumoniae. Frontiers in Microbiology, 7, 232. https://doi.org/10.3389/fmicb.2016.00232
Djordjevic, S., Cordwell, S., Djordjevic, M., Wilton, J., & Minion, F. C. (2004). Proteolytic processing of the Mycoplasma hyopneumoniae cilium adhesin. Infection and Immunity, 72, 2791-2802. https://doi.org/10.1128/IAI.72.5.2791-2802.2004
Dos Santos, L. F., Sreevatsan, S., Torremorell, M., Moreira, M. A. S., Sibila, M., & Pieters, M. (2015). Genotype distribution of Mycoplasma hyopneumoniae in swine herds from different geographical regions. Veterinary Microbiology, 175, 374-381. https://doi.org/10.1016/j.vetmic.2014.11.018
Dumke, R., Catrein, I., Pirkil, E., Herrmann, R., & Jacobs, E. (2003). Subtyping of Mycoplasma pneumoniae isolates based on extended genome sequencing and on expression profiles. International Journal of Medical Microbiology, 292, 513-525. https://doi.org/10.1078/1438-4221-00231.
Felde, O., Kreizinger, Z., Sulyok, K. M., Hrivnak, V., Kiss, K., Jerzsele, A., … Gyuranecz, M. (2018). Antibiotic susceptibility testing of Mycoplasma hyopneumoniae field isolates from Central Europe for fifteen antibiotics by microbroth dilution method. PLoS ONE, 13(12), 1-13. https://doi.org/10.1371/journal.pone.0209030
Felde, O., Kreizinger, Z., Sulyok, K. M., Marton, S., Banyai, K., Korbuly, K., … Gyuranecz, M. (2018). Genotyping Mycoplasma hyopneumoniae isolates based on multi-locus sequence typing, multiple-locus variable-number tandem repeat analysis and analyzing gene p146. Veterinary Microbiology, 222, 85-90. https://doi.org/10.1016/j.vetmic.2018.07.004
Ferrarini, M. G., Mucha, S., Parrot, D., Meiffrein, G., Ruggiero, B. J., Comte, G., … Sagot, M. F. (2018). Hydrogen peroxide production and myo-inositol metabolism as important traits for virulence of Mycoplasma hyopneumoniae. Molecular Microbiology, 108(6), 683-696. https://doi.org/10.1111/mmi.13957
Ferrarini, M. G., Siqueira, F. M., Mucha, S., Palama, T., Jobard, E., Elena-Herrmann, B., … Sagot, M. F. (2016). Insights on the virulence of swine respiratory tract mycoplasmas through genome-scale metabolic modeling. BMC Genomics, 17, 353. https://doi.org/10.1186/s12864-016-2644-z
Frey, J., Haldimann, A., & Nicolet, J. (1992). Chromosomal heterogeneity of various Mycoplasma hyopneumoniae field strains. International Journal of Systemic Bacteriology, 42(2), 275-280. https://doi.org/10.1099/00207713-42-2-275
Garza-Moreno, L., Segalés, J., Aragόn, V., Correa-Fiz, F., Pieters, M., Caromona, M., … Sibila, M. (2019). Characterization of Mycoplasma hyopneumoniae strains in vaccinated and non-vaccinated pigs from Spanish slaughterhouses. Veterinary Microbiology, 231, 18-23. https://doi.org/10.1016/j.vetmic.2019.02.023
Garza-Moreno, L., Segalés, J., Pieters, M., Romagosa, A., & Sibila, M. (2018). Acclimation strategies in gilts to control Mycoplasma hyopneumoniae infection. Veterinary Microbiology, 219, 23-29. https://doi.org/10.1016/j.vetmic.2018.04.005
Gautier-Bourchardon, A. V. (2018). Antimicrobial resistance in Mycoplasma spp. Microbiology Spectrum, 6(4), 1-21. https://doi.org/10.1128/microbiolspec.ARBA-0030-2018
Goodwin, R. F., Pomeroy, A. P., & Whittlestone, P. (1965). Production of enzootic pneumonia in pigs with mycoplasma. Veterinary Record, 77, 1247-1249.
Goodwin, R. F. W., Pomeroy, A. P., & Whittlestone, P. (1967). Characterization of Mycoplasma suipneumoniae: A mycoplasma causing enzootic pneumonia of pigs. Journal of Hygiene (Cambridge), 65, 85-96. https://doi.org/10.1017/S0022172400045563
Haldimann, A., Nicolet, J., & Frey, J. (1993). DNA sequence determination and biochemical analysis of the immunogenic p36, the lactate dehydrogenase (LDH) of Mycoplasma hyopneumoniae. Journal of General Microbiology, 139, 317-323. https://doi.org/10.1099/00221287-139-2-317
Han, J., Park, B., Shin, D., Song, S., Jeong, Y., & Lee, N. (2017). Complete genome sequence of Mycoplasma hyopneumoniae strain KM014, a clinical isolate from South Korea. Genome Announcements, 5(38), e01012-17. https://doi.org/10.1128/genomeA.01012-17.
Hsu, T., & Minion, F. C. (1998). Identification of the cilium binding epitope of the Mycoplasma hyopneumoniae P97 adhesin. Infection and Immunity, 66(10), 4762-4766.
Jiang, G. R., Nikolova, S., & Clarck, D. P. (2001). Regulation of the ldhA gene, enconding the fermentative lactate dehydrogenase of Escherichia coli. Microbiology, 147, 2437-2446.
Kannan, T. R., Provenzano, D., Wright, J. R., & Baseman, J. B. (2005). Identification and characterization of human surfactant protein A binding protein of Mycoplasma pneumoniae. Infection and Immunity, 75, 2828-2834. https://doi.org/10.1128/IAI.73.5.2828-2834.2005
Klein, U., de Jong, A., Moyaert, H., El Garch, F., Leon, R., Richard-Mazet, A., … Ayling, R. (2017). Antimicrobial susceptibility monitoring of Mycoplasma hyopneumoniae and Mycoplasma bovis isolated in Europe. Veterinary Microbiology, 204, 188-193. https://doi.org/10.1016/j.vetmic.2017.04.012
Kokotovic, B., Friis, N. F., Jensen, J. S., & Ahrens, P. (1999). Amplified-fragment length polymorphism fingerprinting of Mycoplasma species. Journal of Clinical Microbiology, 37(10), 3300-3307.
Le Carrou, J., Laurentie, M., Kobisch, M., & Gautier-Bouchardon, A. V. (2006). Persistence of Mycoplasma hyopneumoniae in experimentally infected pigs after marbofloxacin treatment and detection of mutations in the parC gene. Antimicrobial Agents and Chemotherapy, 50, 1959-1966. https://doi.org/10.1128/AAC.01527-05
Leal Zimmer, F. M. D. A., Paludo, G. P., Moura, H., Barr, J. R., & Ferreira, H. B. (2018). Differential secretome profiling of a swine tracheal cell line infected with mycoplasmas of the swine respiratory tract. Journal of Proteomics, 10(192), 147-159. https://doi.org/10.1016/j.jprot.2018.08.018
Li, Y. Z., Ho, Y. P., Chen, S. T., Chiou, T. W., Li, Z. S., & Shiuan, D. (2009). Proteomic comparative analysis of pathogenic strain 232 and avirulent strain J of Mycoplasma hyopneumoniae. Biochemistry (Mosc), 74(2), 215-220. https://doi.org/10.1134/S0006297909020138
Liu, W., Feng, Z., Fang, L., Zhou, Z., Li, Q., Sha, L., … Xiao, S. (2011). Complete genome sequence of Mycoplasma hyopneumoniae strain 168. Journal of Bacteriology, 193(4), 1016-1017. https://doi.org/10.1128/JB.01305-10.
Liu, W., Xiao, S., Li, M., Guo, S., Li, S., Luo, R., … Fang, L. (2013). Comparative genomic analyses of Mycoplasma hyopneumoniae pathogenic 168 strain and its high-passaged attenuated strain. BMC Genomics, 14, 80. https://doi.org/10.1186/1471-2164-14-80.
Madsen, M. L., Nettleton, D., Thacker, E. L., Edwards, R., & Minion, F. C. (2006). Transcriptional profiling of Mycoplasma hyopneumoniae during heat shock using microarrays. Infection and Immunity, 74(1), 160-166. https://doi.org/10.1128/IAI.74.1.160-166.2006
Madsen, M. L., Nettleton, D., Thacker, E. L., & Minion, F. C. (2006). Transcriptional profiling of Mycoplasma hyopneumoniae during iron depletion using microarrays. Microbiology, 152, 937-944. https://doi.org/10.1099/mic.0.28674-0
Madsen, M. L., Oneal, M. J., Gardner, S. W., Strait, E. L., Nettleton, D., Thacker, E. L., & Minion, F. C. (2007). Array-based genomic comparative hybridization analysis of field strains of Mycoplasma hyopneumoniae. Journal of Bacteriology, 189(22), 7977-7982. https://doi.org/10.1128/JB.01068-07
Maes, D., Sibila, M., Kuhnert, P., Segales, J., Haesebrouck, F., & Pieters, M. (2018). Update on Mycoplasma hyopneumoniae infections in pigs: Knowledge gaps for improved disease control. Transboundary and Emerging Diseases, 65, 110-124. https://doi.org/10.1111/tbed.12677
Maniloff, J. (1983). Evolution of wall-less prokaryotes. Annual Review of Microbiology, 37, 477-499. https://doi.org/10.1146/annurev.mi.37.100183.002401
Marchioro, S., Del Pozo Sacristan, R., Michiels, A., Haesebrouck, F., Conceição, F., Dellagostin, O., & Maes, D. (2014). Immune responses of a chimeric protein vaccine containing Mycoplasma hyopneumoniae antigens and LTB against experimental M. hyopneumoniae infection in pigs. Vaccine, 32, 4689-4694. https://doi.org/10.1016/j.vaccine.2014.05.072
Maré, C. J., & Switzer, W. P. (1965). New species: Mycoplasma hyopneumoniae: A causative agent of virus pig pneumonia. Veterinary Medicine Small Animal Clinics, 60, 841-846.
Marois, C., Le Carrou, J., Kobisch, M., & Gautier-Bouchardon, A. V. (2007). Isolation of Mycoplasma hyopneumoniae from different sampling sites in experimentally infected and contact SPF piglets. Veterinary Microbiology, 120, 96-104. https://doi.org/10.1016/j.vetmic.2006.10.015
Mayor, D., Jores, J., Korczak, B. M., & Kuhnert, P. (2008). Multilocus sequence typing (MLST) of Mycoplasma hyopneumoniae: A diverse pathogen with limited clonality. Veterinary Microbiology, 127, 63-72. https://doi.org/10.1016/j.vetmic.2007.08.010
Mayor, D., Zeeh, F., Frey, J., & Kuhnert, P. (2007). Diversity of Mycoplasma hyopneumoniae in pig farms revealed by direct molecular typing of clinical material. Veterinary Research, 38, 391-398. https://doi.org/10.1051/vetres:2007006
Medina, J. L., Coalson, J. J., Brooks, E. G., Winter, V. T., Chaparro, A., Principe, M. F. R., … Dube, P. H. (2012). Mycoplasma pneumoniae CARDS toxin induces pulmonary eosinophilic and lymphocytic inflammation. American Journal of Respiratory Cell and Molecular Biology, 46(6), 815-822. https://doi.org/10.1165/rcmb.2011-0135OC
Meyns, T., Maes, D., Calus, D., Ribbens, S., Dewulf, J., Chiers, K., … Haesebrouck, F. (2007). Interactions of highly and low virulent Mycoplasma hyopneumoniae isolates with the respiratory tract of pigs. Veterinary Microbiology, 120, 87-95. https://doi.org/10.1016/j.vetmic.2006.10.010
Meyns, T., Maes, D., Dewulf, J., Vicca, J., Haesebrouck, F., & de Kruif, A. (2004). Quantification of the spread of Mycoplasma hyopneumoniae in nursery pigs using transmission experiments. Preventative Veterinary Medicine Journal, 66(1-4), 265-275. https://doi.org/10.1016/j.prevetmed.2004.10.001.
Michiels, A., Vranchx, K., Piepers, S., Del Pozo Sacristan, R., Arsenakis, I., Boyen, F., … Maes, D. (2017). Impact of diversity of Mycoplasma hyopneumoniae strains on lung lesions in slaughter pigs. Veterinary Research, 48(1), 2. https://doi.org/10.1186/s13567-016-0408-z
Minion, F. C., Adams, C., & Hsu, T. (2000). R1 region of P97 mediates adherence of Mycoplasma hyopneumoniae to swine cilia. Infection and Immunity, 68(5), 3056-3060. https://doi.org/10.1128/IAI.68.5.3056-3060.2000
Minion, F. C., Lefkowitz, E. L., Madsen, M. L., Cleary, B. L., Swartzell, S. M., & Mahairas, G. G. (2004). The genome sequence of Mycoplasma hyopneumoniae strain 232, the agent of swine mycoplasmosis. Journal of Bacteriology, 186(21), 7123-7133. https://doi.org/10.1128/JB.186.21.7123-7133.2004
Nathues, H., Grosse Beilage, E., Kreienbrock, L., Rosengarten, R., & Spergser, J. (2011). RAPD and VNTR analysis demonstrate genotypic heterogeneity of Mycoplasma hyopneumoniae isolates from pigs housed in a region with high pig density. Veterinary Microbiology, 152, 338-345. https://doi.org/10.1016/j.vetmic.2011.05.029
Okada, M., Asai, T., Futo, S., Mori, Y., Mukai, T., Yazawa, S., … Sato, S. (2005). Serological diagnosis of enzootic pneumonia of swine by a double-sandwich enzyme-linked immunosorbent assay using a monoclonal antibody and recombinant antigen (P46) of Mycoplasma hyopneumoniae. Veterinary Microbiology, 105, 251-259. https://doi.org/10.1016/j.vetmic.2004.11.006
Oneal, M. J., Schafer, E. R., Madsen, M. L., & Minion, F. C. (2008). Global transcriptional analysis of Mycoplasma hyopneumoniae following exposure to norepinephrine. Microbiology, 154, 2581-2588. https://doi.org/10.1099/mic.0.2008/020230-0
Paes, J. A., Lorenzatto, K. R., de Moraes, S. N., Moura, H., Barr, J. R., & Ferreira, H. B. (2017). Secretomes of Mycoplasma hyopneumoniae and Mycoplasma flocculare reveal differences associated to pathogenesis. Journal of Proteomics, 154, 69-77. https://doi.org/10.1016/j.jprot.2016.12.002
Pantoja, L. G., Pettit, K., Dos Santos, L. F., Tubbs, R., & Pieters, M. (2016). Mycoplasma hyopneumoniae genetic variability within a swine operation. Journal of Veterinary Diagnostic Investigation, 28(2), 175-179. https://doi.org/10.1177/1040638716630767
Park, S. C., Yibchok-Anun, S., Cheng, H., Young, T. F., Thacker, E. L., Minion, F. C., … Hsu, W. H. (2002). Mycoplasma hyopneumoniae increases intracellular calcium release in porcine ciliated tracheal cells. Infection and Immunity, 70, 2502-2506. https://doi.org/10.1128/IAI.70.5.2502-2506.2002
Petersen, A. C., Oneal, D. C., Seibel, J. R., Poel, K., Daum, C. L., Djordjevic, S. P., & Minion, F. C. (2016). Cross reactivity among the swine mycoplasmas as identified by protein microarray. Veterinary Microbiology, 192, 204-212. https://doi.org/10.1016/j.vetmic.2016.07.023
Pieters, M., & Fano, E. (2016). Mycoplasma hyopneumoniae management in gilts. Veterinary Record, 178(5), 122-123. https://doi.org/10.1136/vr.i481
Pinto, P. M., Chemale, G., de Castro, L. A., Costa, A. P., Kich, J. D., Vainstein, M. H., … Ferreira, H. B. (2007). Proteomic survey of the pathogenic Mycoplasma hyopneumoniae strain 7448 and identification of novel post-translationally modified and antigenic proteins. Veterinary Microbiology, 121, 83-93. https://doi.org/10.1016/j.vetmic.2006.11.018
Pinto, P. M., Klein, C. S., Zaha, A., & Ferreira, H. B. (2009). Comparative proteomic analysis of pathogenic and non-pathogenic strains from the swine pathogen Mycoplasma hyopneumoniae. Proteome Science, 7, 45. https://doi.org/10.1186/1477-5956-7-45
Pinto, P., Oliveira de Carvalho, M., Alves-Junior, L., Brocchi, M., & Silveira Schrank, I. (2007). Molecular analysis of an integrative conjugative element, ICEH, present in the chromosome of different strains of Mycoplasma hyopneumoniae. Genetics and Molecular Biology, 30, 256-263. https://doi.org/10.1590/S1415-47572007000200014
Pointon, A. M., Byrt, D., & Heap, P. (1985). Effect of enzootic pneumonia of pigs on growth performance. Australian Veterinary Journal, 62(1), 13-18. https://doi.org/10.1111/j.1751-0813.1985.tb06032.x
Raymond, B. B. A., Jenkins, C., Seymour, L. M., Tacchi, J. L., Widjaja, M., Jarocki, V. M., … Djordjevic, S. P. (2015). Proteolytic processing of the cilium adhesin MHJ_0194 (P123J) in Mycoplasma hyopneumoniae generates a functionally diverse array of cleavage fragments that bind multiple host molecules. Cellular Microbiology, 17(3), 425-444. https://doi.org/10.1111/cmi.12377
Raymond, B. B. A., Jenkins, C., Turnbull, L., Whitchurch, C. B., & Djordjevic, S. P. (2018). Extracellular DNA release from the genome-reduced pathogen Mycoplasma hyopneumoniae is essential for biofilm formation on abiotic surfaces. Scientific Reports, 8(1), 10373. https://doi.org/10.1038/s41598-018-28678-2
Raymond, B. B. A., Tacchi, J. L., Jarocki, V. M., Minion, F. C., Padula, M. P., & Djordjevic, S. P. (2013). P159 from Mycoplasma hyopneumoniae binds porcine cilia and heparin and is cleaved in a manner akin to ectodomain shedding. Journal of Proteome Research, 12(12), 5891-5903. https://doi.org/10.1021/pr400903s
Raymond, B. B. A., Turnbull, L., Jenkins, C., Madhkoor, R., Schleicher, I., Uphoff, C. C., … Djordjevic, S. P. (2018). Mycoplasma hyopneumoniae resides intracellularly within porcine epithelial cells. Scientific Reports, 8(1), 17697. https://doi.org/10.1038/s41598-018-36054-3
Razin, S. (1985). Molecular biology and genetics of mycoplasmas (Mollicutes). Microbiology and Molecular Biology Reviews, 49(4), 419-455.
Razin, S., Yogev, D., & Naot, Y. (1998). Molecular biology and pathogenicity of mycoplasmas. Microbiology and Molecular Biology Reviews, 62, 1094-1156.
Rebaque, F., Camacho, P., Parada, J., Lucchesi, P., Ambrogi, A., & Tamiozzo, P. (2018). Persistence of the same genetic type of Mycoplasma hyopneumoniae in a closed herd for at least two years. Revista Argentina De Microbiologia, 50(2), 147-150. https://doi.org/10.1016/j.ram.2017.05.002
Ro, L., & Ross, R. (1983). Comparison of Mycoplasma hyopneumoniae strains by serologic methods. American Journal of Veterinary Research, 44, 2087-2094.
Rocha, E. P., & Blanchard, A. (2002). Genomic repeats, genome plasticity and the dynamics of Mycoplasma evolution. Nucleic Acids Research, 30(9), 2031-2042. https://doi.org/10.1093/nar/30.9.2031
Rodriguez, F., Ramirez, G. A., Sarradell, J., Andrada, M., & Lorenzo, H. (2004). Immunohistochemical labelling of cytokines in lung lesions of pigs naturally infected with Mycoplasma hyopneumoniae. Journal of Comparative Pathology, 130(4), 306-312. https://doi.org/10.1016/j.jcpa.2003.12.008
Rosengarten, R., Citti, C., Glew, M., Lischewski, A., DroeBe, M., Much, P., … Spergser, J. (2000). Host-pathogen interactions in mycoplasma pathogenesis: Virulence and survival strategies of minimalist prokaryotes. International Journal of Medical Microbiology, 290(1), 15-25.
Rosengarten, R., & Yogev, D. (1996). Variant colony surface antigenic phenotypes within Mycoplasma strain populations: Implications for species identification and strain identification. Journal of Clinical Microbiology, 34, 149-158.
Ross, R. F. (1999). Mycoplasmal diseases. In B. E. Straw, S. D'Allaire, W. L. Mengeling, & D. J. Taylor (Eds.), Diseases of swine (8th ed., pp. 495-505). Ames, IA: Iowa State University Press.
Scarman, A. L., Chin, J. C., Eamens, G. J., Delaney, S. F., & Djordjevic, S. P. (1997). Identification of novel species-specific antigens of Mycoplasma hyopneumoniae by preparative SDS-PAGE ELISA profiling. Microbiology, 143, 663-673. https://doi.org/10.1099/00221287-143-2-663
Schafer, E., Oneal, M., Madsen, M., & Minion, F. C. (2007). Global transcriptional analysis of Mycoplasma hyopneumoniae following exposure to hydrogen peroxide. Microbiology, 153, 3785-3790. https://doi.org/10.1099/mic.0.2007/011387-0
Seymour, L. M., Jenkins, C., Deutscher, A. T., Raymond, B. B. A., Padula, M. P., Tacchi, J. L., … Djordjevic, S. P. (2012). Mhp182 (P102) binds fibronectin and contributes to the recruitment of plasmin(ogen) to the Mycoplasma hyopneumoniae cell surface. Cellular Microbiology, 14, 81-94. https://doi.org/10.1111/j.1462-5822.2011.01702.x
Sibila, M., Pieters, M., Molitor, T., Maes, D., Haesebrouck, F., & Segalés, J. (2009). Current perspectives on the diagnosis and epidemiology of Mycoplasma hyopneumoniae infection. Veterinary Journal, 181, 221-231. https://doi.org/10.1016/j.tvjl.2008.02.020
Siqueira, F. M., Thompson, C. E., Virginio, V. G., Gonchoroski, T., Reolon, L., Almeida, L. G., … Zaha, A. (2013). New insights on the biology of swine respiratory tract mycoplasmas from a comparative genome analysis. BMC Genomics, 14, 175. https://doi.org/10.1186/1471-2164-14-175.
Stakenborg, T., Vicca, J., Butaye, P., Maes, D., Minion, F. C., Peeters, J., … Haesebrouck, F. (2005). Characterization of in vivo acquired resistance of Mycoplasma hyopneumoniae to macrolides and lincosamides. Microbial Drug Resistance, 11, 290-294. https://doi.org/10.1089/mdr.2005.11.290
Stakenborg, T., Vicca, J., Maes, D., Peeters, J., de Kruif, A., Haesebrouck, F., & Butaye, P. (2006). Comparison of molecular techniques for the typing of Mycoplasma hyopneumoniae isolates. Journal of Microbiological Methods, 66(2), 263-275. https://doi.org/10.1016/j.mimet.2005.12.002
Stipkovits, L., Nicolet, J., Haldimann, A., & Frey, J. (1991). Use of antibodies against the P36 protein of Mycoplasma hyopneumoniae for the identification of M. hyopneumoniae strains. Molecular and Cellular Probes, 5, 451-457. https://doi.org/10.1016/S0890-8508(05)80017-9
Strait, E., Madsed, M. L., Minion, F. C., & Thacker, E. L. (2003). Analysis of Mycoplasma hyopneumoniae field isolates. Conference for Research Workers in Animal Diseases, Chicago, IL.
Straw, B. E., Shin, S. J., & Yeager, A. E. (1990). Effect of pneumonia on growth rate and feed efficiency of minimal disease pigs exposed to Actinobacillus pleuropneumoniae and Mycoplasma hyopneumoniae. Preventive Veterinary Medicine, 9, 287-294. https://doi.org/10.1016/0167-5877(90)90074-R
Tacchi, J., Raymond, B., Haynes, P., Berry, I., Widjaja, M., Bogema, D., & Djordjevic, S. (2016). Post-translational processing targets functionally diverse proteins in Mycoplasma hyopneumoniae. Open Biology, 6, 150210. https://doi.org/10.1098/rsob.150210
Tacchi, J., Raymond, B., Jarocki, V., Berry, I., Padula, M., & Djordjevic, S. (2014). Cilium adhesin P216 (MHJ_0493) is a target of ectodomain shedding and aminopeptidase activity on the surface of Mycoplasma hyopneumoniae. Journal of Proteome Research, 13(6), 2920-2930. https://doi.org/10.1021/pr500087c
Takeuti, K. L., de Barcellos, D. E. S. N., de Andrade, C. P., de Almeida, L. L., & Pieters, M. (2017). Infection dynamics and genetic variability of Mycoplasma hyopneumoniae in self-replacement gilts. Veterinary Microbiology, 208, 18-24. https://doi.org/10.1016/j.vetmic.2017.07.007
Tamiozzo, P., Zamora, R., Lucchesi, P. M., Estanguet, A., Parada, J., Carranza, A., … Ambrogi, A. (2015). MLVA typing of Mycoplasma hyopneumoniae bacterins and field strains. Veterinary Record Open, 2(2), e000117. https://doi.org/10.1136/vetreco-2015-000117
Tavio, M., Poveda, C., Assunção, P., Ramírez, A., & Poveda, J. (2014). In vitro activity of tylvalosin against Spanish field strains of Mycoplasma hyopneumoniae. Veterinary Record, 175, 539. https://doi.org/10.1136/vr.102458
Thacker, E. L., & Minion, F. C. (2012). Mycoplasmosis. In J. J. Zimmerman, L. A. Karriker, A. Ramirez, K. J. Schwartz, & G. W. Stevenson (Eds.). Diseases of swine (10th ed., pp. 779-797). Chichester, UK: John Wiley & Sons, Inc.
Thacker, E. L., Thacker, B. J., Kuhn, M., Hawkins, P. A., & Waters, W. R. (2000). Evaluation of local and systemic immune responses induced by intramuscular injection of a Mycoplasma hyopneumoniae bacterin to pigs. American Journal of Veterinary Research, 61(11), 1384-1389. https://doi.org/10.2460/ajvr.2000.61.1384
Thongkamkoon, P., Narongsak, W., Kobayashi, H., Pathanasophon, P., Kishima, M., & Yamamoto, K. (2013). In vitro susceptibility of Mycoplasma hyopneumoniae field isolates and occurrence of fluoroquinolone, macrolides, and lincomycin resistance. Journal of Veterinary Medical Sciences, 75(8), 1067-1070. https://doi.org/10.1292/jvms.12-0520.
Tsungda, H., & Minion, F. C. (1998). Identification of the cilium binding epitope of the Mycoplasma hyopneumoniae P97 adhesin. Infection and Immunity, 66(10), 4762-4766.
Vasconcelos, A. T. R., Ferreira, H. B., Bizarro, C. V., Bonatto, S. L., Carvalho, M. O., Pinto, P. M., … Zaha, A. (2005). Swine and poultry pathogens: The complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. Journal of Bacteriology, 187, 5568-5577. https://doi.org/10.1128/JB.187.16.5568-5577.2005
Vicca, J., Maes, D., Stakenborg, T., Butaye, P., Minion, C., Peeters, J., … Haesebrouck, F. (2007). Resistance mechanism against fluoroquinolones in Mycoplasma hyopneumoniae field isolates. Microbial Drug Resistance, 13, 166-170. https://doi.org/10.1089/mdr.2007.716
Vicca, J., Maes, D., Thermote, L., Peeters, J., Haesebrouck, F., & de Kruif, A. (2002). Patterns of Mycoplasma hyopneumoniae Infections in Belgian farrow-to-finish pig herds with diverging disease-course. Journal of Veterinary Medicine, 49, 349-353. https://doi.org/10.1046/j.1439-0450.2002.00579.x
Vicca, J., Stakenborg, T., Maes, D., Butaye, P., Peeters, J., de Kruif, A., & Haesebrouck, F. (2003). Evaluation of virulence of Mycoplasma hyopneumoniae field isolates. Veterinary Microbiology, 97, 177-190. https://doi.org/10.1016/j.vetmic.2003.08.008
Vicca, J., Stakenborg, T., Maes, D., Butaye, P., Peeters, J., de Kruif, A., & Haesebrouck, F. (2004). In vitro susceptibilities of Mycoplasma hyopneumoniae field isolates. Antimicrobial Agents and Chemotherapy, 48, 4470-4472. https://doi.org/10.1128/AAC.48.11.4470-4472.2004
Villarreal, I., Maes, D., Meyns, T., Gebruers, F., Calus, D., Pasmans, F., & Haesebrouck, F. (2009). Infection with a low virulent Mycoplasma hyopneumoniae isolate does not protect piglets against subsequent infection with a highly virulent M. hyopneumoniae isolate. Vaccine, 27, 1875-1879. https://doi.org/10.1016/j.vaccine.2008.12.005
Villarreal, I., Maes, D., Vranckx, K., Calus, D., Pasmans, F., & Haesebrouck, F. (2011). Effect of vaccination of pigs against experimental infection with high and low virulence Mycoplasma hyopneumoniae strains. Vaccine, 29, 1731-1735. https://doi.org/10.1016/j.vaccine.2011.01.002
Villarreal, I., Vranckx, K., Calus, D., Pasmans, F., Haesebrouck, F., & Maes, D. (2012). Effect of challenge of pigs previously immunised with inactivated vaccines containing homologous and heterologous Mycoplasma hyopneumoniae strains. BMC Veterinary Research, 8, 2. https://doi.org/10.1186/1746-6148-8-2
Vranckx, K., Maes, D., Calus, D., Villarreal, I., Pasmans, F., & Haesebrouck, F. (2011). Multiple-locus variable-number tandem-repeat analysis is a suitable tool for differentiation of Mycoplasma hyopneumoniae strains without cultivation. Journal of Clinical Microbiology, 49(5), 2020-2023. https://doi.org/10.1128/JCM.00125-11
Wilton, J., Jenkins, C., Cordwell, S., Falconer, L., Minion, F. C., Oneal, D., & Djordjevic, S. (2009). Mhp493 (P216) is a proteolytically processed, cilium and heparin binding protein of Mycoplasma hyopneumoniae. Molecular Microbiology, 71, 566-582. https://doi.org/10.1111/j.1365-2958.2008.06546.x
Wilton, J. L., Scarman, A. L., Walker, M. J., & Djordjevic, S. P. (1998). Reiterated repeat region variability in the ciliary adhesion gene of Mycoplasma hyopneumoniae. Microbiology, 144, 1931-1943.
Wise, K. S. (1993). Adaptive surface variation in mycoplasmas. Trends in Microbiology, 1(2), 59-63.
Wise, K., & Kim, M. (1987a). Major membrane surface proteins of Mycoplasma hyopneumoniae selectively modified by covalently bound lipid. Journal of Bacteriology, 169, 5546-5555. https://doi.org/10.1128/jb.169.12.5546-5555.1987
Wise, K., & Kim, M. (1987b). Identification of intrinsic and extrinsic membrane proteins bearing surface epitopes of Mycoplasma hyopneumoniae. Israel Journal of Medical Sciences, 23, 469-473.
Woolley, L. K., Fell, F., Gonsalves, J. R., Walker, M. J., Djordjevic, S. P., Jenkins, C., & Eamens, G. J. (2012). Evaluation of clinical, histological and immunological changes and qPCR detection of Mycoplasma hyopneumoniae in tissues during the early stages of mycoplasmal pneumonia in pigs after experimental challenge with two field isolates. Veterinary Microbiology, 161, 186-195. https://doi.org/10.1016/j.vetmic.2012.07.025
Zhang, Q., Young, T. F., Ross, R. F., Zhang, Q., & Young, T. F. (1995). Identification and characterization of a Mycoplasma hyopneumoniae adhesin. Infection and Immunity, 63, 1013-1019.
Zielinski, G., & Ross, R. (1993). Adherence of Mycoplasma hyopneumoniae to porcine ciliated respiratory tract cells. American Journal of Veterinary Research, 54, 1262-1269.