Invasion and persistence of Mycoplasma bovis in embryonic calf turbinate cells

Bürki, Sibylle; Gaschen, Véronique; Stoffel, Michael; Stojiljković, Ana; Frey, Joachim; Kuehni-Boghenbor, Kathrin; Pilo, Paola

doi:10.1186/s13567-015-0194-z

Cited by 47 publications

(69 citation statements)

References 63 publications

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“…Pathogenic bacteria are known to interact with these cytoskeletal proteins during infection 95,101,102 . Although mycoplasma have long been considered to be cell surface-associated parasitic bacteria, this dogma has been challenged with numerous reports citing phylogenetically-divergent mycoplasmas residing within eukaryote cells and possessing the molecular machinery for selective uptake into, survival within, and release from phagosomes [103][104][105][106][107][108][109] .…”

Section: Discussionmentioning

confidence: 99%

Cell surface processing of the P1 adhesin of Mycoplasma pneumoniae identifies novel domains that bind host molecules

Widjaja

Berry

Jarocki

et al. 2020

Sci Rep

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Mycoplasma pneumoniae is a genome reduced pathogen and causative agent of community acquired pneumonia. The major cellular adhesin, P1, localises to the tip of the attachment organelle forming a complex with P40 and P90, two cleavage fragments derived by processing Mpn142, and other molecules with adhesive and mobility functions. LC-MS/MS analysis of M. pneumoniae M129 proteins derived from whole cell lysates and eluents from affinity matrices coupled with chemically diverse host molecules identified 22 proteoforms of P1. Terminomics was used to characterise 17 cleavage events many of which were independently verified by the identification of semitryptic peptides in our proteome studies and by immunoblotting. One cleavage event released 1597 tSAAKpGApRppVppKpGApKppVQppKKpA 1627 from the C-terminus of P1 and this peptide was shown to bind to a range of host molecules. A smaller synthetic peptide comprising the C-terminal 15 amino acids, 1613 pGApKppVQppKKpA 1627 , selectively bound cytoskeletal intermediate filament proteins cytokeratin 7, cytokeratin 8, cytokeratin 18, and vimentin from a native A549 cell lysate. Collectively, our data suggests that ectodomain shedding occurs on the surface of M. pneumoniae where it may alter the functional diversity of P1, Mpn142 and other surface proteins such as elongation factor Tu via a mechanism similar to that described in Mycoplasma hyopneumoniae. The attachment organelle is a structurally and functionally sophisticated component of the M. pneumoniae cell that is responsible for the assembly of proteins essential for motility and adherence 1-8. An extensive list of host molecules including fibronectin 9-13 , fibrinogen 10-14 , plasminogen 11-13,15-17 , lactoferrin 10-12 , laminin 10-12 , and vitronectin 10-13 interact with surface accessible adhesins in M. pneumoniae. Other less well-defined host molecules include sialylated molecules 18 , oligosaccharides 19 , glycolipids 20 , and glycoproteins 21. The gene mpn141 encoding the major adhesin P1 is located in the same operon along with mpn140 and mpn142 and these three genes constitute a polycistronic transcriptional unit 22,23. mpn140 encodes for a 28 kDa putative phosphoesterase 24 and while it has been shown to degrade nanoRNA and dephosphorylate 3′-phosphoadenosine 5′-phosphate to AMP 25 , no role in adherence has been assigned for this protein. mpn142 generates a 130 kDa product (Mpn142) that is cleaved into two fragments of 40 kDa (P40) and 90 kDa (P90) immediately after or concurrent with translation 26,27. The cleavage event in Mpn142, first described over 25 years ago, was the first in what is now known to be a highly processed molecule on the surface of M. pneumoniae 28. P1 is a remarkably versatile molecule and the subject of numerous studies over the past 30 years. The only cleavage event that has been accurately assigned to P1 is the removal of the N-terminal 59 amino acids as a leader peptide 29. Molecular cross-linking and immunogold-labelling studies indicated that P1 forms a complex with P30, P40, and P90 ...

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Section: Discussionmentioning

confidence: 99%

Cell surface processing of the P1 adhesin of Mycoplasma pneumoniae identifies novel domains that bind host molecules

Widjaja

Berry

Jarocki

et al. 2020

Sci Rep

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“…The invasion of circulating immune cells and erythrocytes should not only play an important role in pathogenicity, potentially protecting the pathogen from the host immune response and administered antimicrobials, but could also promote persistence and further dissemination of the pathogen between organ systems. M. bovis antigens have also been visualized in hepatocytes and epithelial cells (Maeda et al., ), and invasion followed by intracellular replication has been demonstrated in primary embryonic calf turbinate cells (Bürki, Gaschen et al., ), as well as in bovine embryonic tracheal epithelial cells (Suleman et al., ). Although much awaits to be discerned about the pathways for entry and survival in these privileged niches, recent advances in molecular tools and imaging techniques should expedite our understanding of these processes.…”

Section: The Causative Organismmentioning

confidence: 99%

“…A major unknown is why and how M. bovis can cause so many different clinical signs and why in some cases it manifests as pneumonia, arthritis, mastitis, otitis media, keratoconjunctivitis or genital infections, infertility or abortion. It is not known how the organism circulates in the host and it has only relatively recently been shown to be able to persist intracellularly in vitro (Bürki, Gaschen et al., ; van der Merwe et al., ). It is thought that the animal's immune response contributes to lesion development, at least at the chronic stage, but this is not fully understood (Kauf, Rosenbusch, Paape, & Bannermann, ).…”

Section: Gap Analysismentioning

confidence: 99%

Gap analysis ofMycoplasma bovisdisease, diagnosis and control: An aid to identify future development requirements

Calcutt

Lysnyansky

Sachse

et al. 2018

Transbound Emerg Dis

103

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There is a worldwide problem of disease caused by Mycoplasma (M.) bovis in cattle; it has a significant detrimental economic and animal welfare impact on cattle rearing. Infection can manifest as a plethora of clinical signs including mastitis, pneumonia, arthritis, keratoconjunctivitis, otitis media and genital disorders that may result in infertility and abortion. Current diagnosis and control information are reviewed and analysed to identify gaps in knowledge of the causative organism in respect of the disease pathology, diagnosis and control methods. The main considerations are as follows: no vaccines are commercially available; antimicrobial resistance is increasing; diagnostic and antimicrobial sensitivity testing needs to be improved; and a pen-side test would facilitate more rapid diagnosis and implementation of treatment with antimicrobials. More data on host susceptibility, stress factors, immune response and infectious dose levels are required. The impact of asymptomatic carriers, M. bovis survival in the environment and the role of wildlife in transmitting the disease also needs investigation. To facilitate development of vaccines, further analysis of more M. bovis genomes, its pathogenic mechanisms, including variable surface proteins, is required, along with reproducible disease models.

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“…Activation of CD4+, CD8+ and c/d T-cells has been observed in response to heat-killed M. bovis [11], but not to live bacterial cells [13][14][15][16][17]. Although M. bovis is predominantly an extracellular pathogen, there is in vivo and in vitro evidence that suggests the potential for the bacterium to enter host cells [18][19][20][21][22]. Intracellular M. bovis can survive inside cells [13,20,21]; modulate cytokine expression [13,[23][24][25][26] and apoptosis [13,20,27]; or directly play a role in pathogenesis [28].…”

Section: The Challengesmentioning

confidence: 99%