Influenza A Virus Neuraminidase Enhances Meningococcal Adhesion to Epithelial Cells through Interaction with Sialic Acid-Containing Meningococcal Capsules

Rameix‐Welti, Marie‐Anne; Zarantonelli, Leticia; Giorgini, Dario; Ruckly, Corinne; Marasescu, Monica; Werf, Sylvie van der; Alonso, Jean-Michel; Naffakh, Nadia; Taha, Muhamed‐Kheir

doi:10.1128/iai.00155-09

Cited by 52 publications

(50 citation statements)

References 48 publications

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“…During the colder seasons, the nasopharyngeal temperature is likely even lower than 33°C, as observed by Keck et al at 25°C ambient temperature, possibly enhancing the effects on N. meningitidis adhesion phenotypes. In winter months, the rate of meningococcal disease cases rises quickly, and this has been linked to the pattern of seasonal flu (54). In light of our findings, it seems plausible that acquisition of N. meningitidis during winter, when ambient and nasopharyngeal temperatures are low and when N. meningitidis is therefore best equipped for host colonization based on its expressional profile, might be more efficient.…”

Section: Discussionmentioning

confidence: 80%

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

et al. 2016

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bNeisseria meningitidis, the meningococcus, bears the potential to cause life-threatening invasive diseases, but it usually colonizes the nasopharynx without causing any symptoms. Within the nasopharynx, Neisseria meningitidis must face temperature changes depending on the ambient air temperature. Indeed, the nasopharyngeal temperature can be substantially lower than 37°C, the temperature commonly used in experimental settings. Here, we compared the levels of meningococcal biofilm formation, autoaggregation, and cellular adherence at 32°C and 37°C and found a clear increase in all these phenotypes at 32°C suggestive of a stronger in vivo colonization capability at this temperature. A comparative proteome analysis approach revealed differential protein expression levels between 32°C and 37°C, predominantly affecting the bacterial envelope. A total of 375 proteins were detected. Use of database annotation or the PSORTb algorithm predicted 49 of those proteins to be localized in the outer membrane, 21 in either the inner or outer membrane, 35 in the periplasm, 56 in the inner membrane, and 208 in the cytosol; for 6 proteins, no annotation or prediction was available. Temperature-dependent regulation of protein expression was seen particularly in the periplasm as well as in the outer and inner membranes. Neisserial heparin binding antigen (NHBA), NMB1030, and adhesin complex protein (ACP) showed the strongest upregulation at 32°C and were partially responsible for the observed temperature-dependent phenotypes. Screening of different global regulators of Neisseria meningitidis suggested that the extracytoplasmic sigma factor E might be involved in temperature-dependent biofilm formation. In conclusion, subtle temperature changes trigger adaptation events promoting mucosal colonization by meningococci. Microorganisms constantly adapt to changing environmental conditions. These changes include oxygen and nutrient availability, osmotic conditions, and temperature. The physiology of bacterial adaptation, including the underlying regulatory mechanisms that operate in response to radical temperature changes such as classical heat shock or cold shock, has been studied intensely (1-3). The heat shock response occurs during a transient upshift of growth temperature from 37°C to approximately 50°C (4). The heat shock response is controlled by the alternative sigma factor 32 , which regulates the expression of heat shock proteins mainly involved in protein folding or processing (4). In Escherichia coli, the cold shock response is triggered by a transient downshift from 37°C to 10°C that leads to generally slower transcriptional and translational responses except for about 26 upregulated proteins (5). The functions of these so-called cold shock proteins are less well understood than those of heat shock proteins, but they are likely involved in securing proper transcription, translation, and protein folding (5). Surprisingly little is known about the influence on bacterial physiology of slight temperature differences within mamma...

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Section: Discussionmentioning

confidence: 80%

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

et al. 2016

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“…3, solid black bars) (P Ͻ 0.05). This increase was dependent on the viral NA sialidase activity, since it was not observed when the DF1 cells expressed the mutant MZ-NA-Y406F or MZdelNA-Y406F proteins with no detectable sialidase activity (54) (Fig. 3, solid black bars) or in the presence of 1 M of zanamivir (Fig.…”

Section: Resultsmentioning

confidence: 99%

A Genetically Engineered Waterfowl Influenza Virus with a Deletion in the Stalk of the Neuraminidase Has Increased Virulence for Chickens

Munier

Larcher

Cormier-Aline

et al. 2010

J Virol

132

126

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A deletion of about 20 amino acids in the stalk of the neuraminidase (NA) is frequently detected upon transmission of influenza A viruses from waterfowl to domestic poultry. Using reverse genetics, a recombinant virus derived from a wild duck influenza virus isolate, A/Mallard/Marquenterre/Z237/83 (MZ), and an NA stalk deletion variant (MZ-delNA) were produced. Compared to the wild type, the MZ-delNA virus showed a moderate growth advantage on avian cultured cells. In 4-week-old chickens inoculated intratracheally with the MZ-delNA virus, viral replication in the lungs, liver, and kidneys was enhanced and interstitial pneumonia lesions were more severe than with the wild-type virus. The MZ-delNA-inoculated chickens showed significantly increased levels of mRNAs encoding interleukin-6 (IL-6), transforming growth factor-␤4 (TGF-␤4), and CCL5 in the lungs and a higher frequency of apoptotic cells in the liver than did their MZ-inoculated counterparts. Molecular mechanisms possibly underlying the growth advantage of the MZ-delNA virus were explored. The measured enzymatic activities toward a small substrate were similar for the wild-type and deleted NA, but the MZ-delNA virus eluted from chicken erythrocytes at reduced rates. Pseudoviral particles expressing the MZ hemagglutinin in combination with the MZ-NA or MZ-delNA protein were produced from avian cultured cells with similar efficiencies, suggesting that the deletion in the NA stalk does not enhance the release of progeny virions and probably affects an earlier step of the viral cycle. Overall, our data indicate that a shortened NA stalk is a strong determinant of adaptation and virulence of waterfowl influenza viruses in chickens.

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“…Other studies found no association between meningococcal disease and other respiratory viruses, such as adenovirus, parainfluenza virus, respiratory syncytial virus, or rhinovirus [11,12], which suggests that a specific pathophysiological process would be in play for influenza virus-meningococcus interactions. In a study of epithelial cell cultures, RameixWelti et al [13] found that a direct interaction between the influenza A virus neuraminidase and the N. meningitidis capsule enhanced bacterial adhesion to respiratory epithelial cells. This effect may promote N. meningitidis dissemination via the bloodstream [14].…”

Section: Case Discussionmentioning

confidence: 98%

Favorable outcome after life-threatening meningococcal disease complicating influenza A(H1N1) infection

et al. 2011

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Influenza A Virus Neuraminidase Enhances Meningococcal Adhesion to Epithelial Cells through Interaction with Sialic Acid-Containing Meningococcal Capsules

Abstract: The underlying mechanisms of the epidemiological association between influenza virus infections and

Cited by 52 publications

References 48 publications

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

A Genetically Engineered Waterfowl Influenza Virus with a Deletion in the Stalk of the Neuraminidase Has Increased Virulence for Chickens

Favorable outcome after life-threatening meningococcal disease complicating influenza A(H1N1) infection

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