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  1. AU="Jordan P. Metcalf"
  2. AU=Peri?i? Nanut Milica AU=Peri?i? Nanut Milica
  3. AU="Pramod, Ganapathiraju"
  4. AU="Fu, Chu-Jun"
  5. AU="Nejad, Harry G."
  6. AU="Zhang, Q E"
  7. AU="Oppenheim, Madeline"

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  1. Artikel ; Online: The Role of Type I IFNs in Influenza

    Wenxin Wu / Jordan P. Metcalf

    Journal of Innate Immunity, Pp 1-

    Antiviral Superheroes or Immunopathogenic Villains?

    2020  Band 11

    Abstract: The important role of interferons (IFNs) in antiviral innate immune defense is well established. Although recombinant IFN-α was approved for cancer and chronic viral infection treatment by regulatory agencies in many countries starting in 1986, no IFNs ... ...

    Abstract The important role of interferons (IFNs) in antiviral innate immune defense is well established. Although recombinant IFN-α was approved for cancer and chronic viral infection treatment by regulatory agencies in many countries starting in 1986, no IFNs are approved for treatment of influenza A virus (IAV) infection. This is partially due to the complex effects of IFNs in acute influenza infection. IAV attacks the human respiratory system and causes significant morbidity and mortality globally. During influenza infection, depending on the strain of IAV and the individual host, type I IFNs can have protective antiviral effects or can contribute to immunopathology. In the context of virus infection, the immune system has complicated mechanisms regulating the expression and effects of type I IFN to maximize the antiviral response by both activating and enhancing beneficial innate cell function, while limiting immunopathological responses that lead to exaggerated tissue damage. In this review, we summarize the complicated, but important, role of type I IFNs in influenza infections. This includes both protective and harmful effects of these important cytokines during infection.
    Schlagwörter interferon ; influenza ; viral infection ; innate immunity ; cytokines ; Medicine ; R ; Internal medicine ; RC31-1245
    Thema/Rubrik (Code) 570
    Sprache Englisch
    Erscheinungsdatum 2020-06-01T00:00:00Z
    Verlag Karger Publishers
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  2. Artikel ; Online: Anthrax Edema and Lethal Toxins Differentially Target Human Lung and Blood Phagocytes

    Vineet I. Patel / J. Leland Booth / Mikhail Dozmorov / Brent R. Brown / Jordan P. Metcalf

    Toxins, Vol 12, Iss 464, p

    2020  Band 464

    Abstract: Bacillus anthracis , the causative agent of inhalation anthrax, is a serious concern as a bioterrorism weapon. The vegetative form produces two exotoxins: Lethal toxin (LT) and edema toxin (ET). We recently characterized and compared six human airway and ...

    Abstract Bacillus anthracis , the causative agent of inhalation anthrax, is a serious concern as a bioterrorism weapon. The vegetative form produces two exotoxins: Lethal toxin (LT) and edema toxin (ET). We recently characterized and compared six human airway and alveolar-resident phagocyte (AARP) subsets at the transcriptional and functional levels. In this study, we examined the effects of LT and ET on these subsets and human leukocytes. AARPs and leukocytes do not express high levels of the toxin receptors, tumor endothelium marker-8 (TEM8) and capillary morphogenesis protein-2 (CMG2). Less than 20% expressed surface TEM8, while less than 15% expressed CMG2. All cell types bound or internalized protective antigen, the common component of the two toxins, in a dose-dependent manner. Most protective antigen was likely internalized via macropinocytosis. Cells were not sensitive to LT-induced apoptosis or necrosis at concentrations up to 1000 ng/mL. However, toxin exposure inhibited B. anthracis spore internalization. This inhibition was driven primarily by ET in AARPs and LT in leukocytes. These results support a model of inhalation anthrax in which spores germinate and produce toxins. ET inhibits pathogen phagocytosis by AARPs, allowing alveolar escape. In late-stage disease, LT inhibits phagocytosis by leukocytes, allowing bacterial replication in the bloodstream.
    Schlagwörter anthrax ; lethal toxin ; edema toxin ; spores ; pathogenesis ; human lung ; Medicine ; R
    Thema/Rubrik (Code) 610
    Sprache Englisch
    Erscheinungsdatum 2020-07-01T00:00:00Z
    Verlag MDPI AG
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  3. Artikel ; Online: Early IFN-β administration protects cigarette smoke exposed mice against lethal influenza virus infection without increasing lung inflammation

    Wenxin Wu / Lili Tian / Wei Zhang / J. Leland Booth / Jerry William Ritchey / Shuhua Wu / Chao Xu / Brent R. Brown / Jordan P. Metcalf

    Scientific Reports, Vol 12, Iss 1, Pp 1-

    2022  Band 12

    Abstract: Abstract During influenza A virus (IAV) infection, it is unclear whether type I interferons (IFNs) have defensive antiviral effects or contribute to immunopathology in smokers. We treated nonsmoking (NS) and cigarette smoke (CS)-exposed mice intranasally ...

    Abstract Abstract During influenza A virus (IAV) infection, it is unclear whether type I interferons (IFNs) have defensive antiviral effects or contribute to immunopathology in smokers. We treated nonsmoking (NS) and cigarette smoke (CS)-exposed mice intranasally with early (prophylactic) or late (therapeutic) IFN-β. We compared the mortality and innate immune responses of the treated mice following challenge with IAV. In NS mice, both early and late IFN-β administration decreased the survival rate in mice infected with IAV, with late IFN-β administration having the greatest effect on survival. In contrast, in CS-exposed mice, early IFN-β administration significantly increased survival during IAV infection while late IFN-β administration did not alter mortality. With regards to inflammation, in NS mice, IFN-β administration, especially late administration, significantly increased IAV-induced inflammation and lung injury. Early IFN-β administration to CS-exposed mice did not increase IAV-induced inflammation and lung injury as occurred in NS mice. Our results demonstrate, although IFN-β administration worsens the susceptibility of NS mice to influenza infection with increased immunopathology, early IFN-β administration to CS-exposed mice, which have suppression of the intrinsic IFN response, improved outcomes during influenza infection.
    Schlagwörter Medicine ; R ; Science ; Q
    Sprache Englisch
    Erscheinungsdatum 2022-03-01T00:00:00Z
    Verlag Nature Portfolio
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  4. Artikel ; Online: The NOTCH3 Downstream Target HEYL Is Required for Efficient Human Airway Basal Cell Differentiation

    Manish Bodas / Bharathiraja Subramaniyan / Andrew R. Moore / Jordan P. Metcalf / Sarah R. Ocañas / Willard M. Freeman / Constantin Georgescu / Jonathan D. Wren / Matthew S. Walters

    Cells, Vol 10, Iss 3215, p

    2021  Band 3215

    Abstract: Basal cells (BCs) are stem/progenitor cells of the mucociliary airway epithelium, and their differentiation is orchestrated by the NOTCH signaling pathway. NOTCH3 receptor signaling regulates BC to club cell differentiation; however, the downstream ... ...

    Abstract Basal cells (BCs) are stem/progenitor cells of the mucociliary airway epithelium, and their differentiation is orchestrated by the NOTCH signaling pathway. NOTCH3 receptor signaling regulates BC to club cell differentiation; however, the downstream responses that regulate this process are unknown. Overexpression of the active NOTCH3 intracellular domain (NICD3) in primary human bronchial epithelial cells (HBECs) on in vitro air–liquid interface culture promoted club cell differentiation. Bulk RNA-seq analysis identified 692 NICD3-responsive genes, including the classical NOTCH target HEYL, which increased in response to NICD3 and positively correlated with SCGB1A1 (club cell marker) expression. siRNA knockdown of HEYL decreased tight junction formation and cell proliferation. Further, HEYL knockdown reduced club, goblet and ciliated cell differentiation. In addition, we observed decreased expression of HEYL in HBECs from donors with chronic obstructive pulmonary disease (COPD) vs. normal donors which correlates with the impaired differentiation capacity of COPD cells. Finally, overexpression of HEYL in COPD HBECs promoted differentiation into club, goblet and ciliated cells, suggesting the impaired capacity of COPD cells to generate a normal airway epithelium is a reversible phenotype that can be regulated by HEYL. Overall, our data identify the NOTCH3 downstream target HEYL as a key regulator of airway epithelial differentiation.
    Schlagwörter NOTCH3 signaling ; HEYL ; proliferation ; differentiation ; airway epithelium ; basal stem/progenitor cells ; Biology (General) ; QH301-705.5
    Thema/Rubrik (Code) 571
    Sprache Englisch
    Erscheinungsdatum 2021-11-01T00:00:00Z
    Verlag MDPI AG
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  5. Artikel ; Online: Neither Lys- and DAP-type peptidoglycans stimulate mouse or human innate immune cells via Toll-like receptor 2.

    Marybeth Langer / Alanson W Girton / Narcis I Popescu / Tarea Burgett / Jordan P Metcalf / K Mark Coggeshall

    PLoS ONE, Vol 13, Iss 2, p e

    2018  Band 0193207

    Abstract: Peptidoglycan (PGN), a major component of bacterial cell walls, is a pathogen-associated molecular pattern (PAMP) that causes innate immune cells to produce inflammatory cytokines that escalate the host response during infection. In order to better ... ...

    Abstract Peptidoglycan (PGN), a major component of bacterial cell walls, is a pathogen-associated molecular pattern (PAMP) that causes innate immune cells to produce inflammatory cytokines that escalate the host response during infection. In order to better understand the role of PGN in infection, we wanted to gain insight into the cellular receptor for PGN. Although the receptor was initially identified as Toll-like receptor 2 (TLR2), this receptor has remained controversial and other PGN receptors have been reported. We produced PGN from live cultures of Bacillus anthracis and Staphylococcus aureus and tested samples of PGN isolated during the purification process to determine at what point TLR2 activity was removed, if at all. Our results indicate that although live B. anthracis and S. aureus express abundant TLR2 ligands, highly-purified PGN from either bacterial source is not recognized by TLR2.
    Schlagwörter Medicine ; R ; Science ; Q
    Thema/Rubrik (Code) 616
    Sprache Englisch
    Erscheinungsdatum 2018-01-01T00:00:00Z
    Verlag Public Library of Science (PLoS)
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  6. Artikel ; Online: Regulation of influenza virus replication by Wnt/β-catenin signaling.

    Sunil More / Xiaoyun Yang / Zhengyu Zhu / Gayan Bamunuarachchi / Yujie Guo / Chaoqun Huang / Keith Bailey / Jordan P Metcalf / Lin Liu

    PLoS ONE, Vol 13, Iss 1, p e

    2018  Band 0191010

    Abstract: Wnt/β-catenin signaling is an essential pathway in cell cycle control. Dysregulation of the Wnt/β-catenin signaling pathway during viral infection has been reported. In this study, we examined the effect of modulating Wnt/β-catenin signaling during ... ...

    Abstract Wnt/β-catenin signaling is an essential pathway in cell cycle control. Dysregulation of the Wnt/β-catenin signaling pathway during viral infection has been reported. In this study, we examined the effect of modulating Wnt/β-catenin signaling during influenza virus infection. The activation of the Wnt/β-catenin pathway by Wnt3a increased influenza virus mRNA and virus production in in vitro in mouse lung epithelial E10 cells and mRNA expresson of influenza virus genes in vivo in the lungs of mice infected with influenza virus A/Puerto Rico/8/34. However, the inhibition of Wnt/β-catenin signaling by iCRT14 reduced virus titer and viral gene expression in human lung epithelial A549 cells and viral replication in primary mouse alveolar epithelial cells infected with different influenza virus strains. Knockdown of β-catenin also reduced viral protein expression and virus production. iCRT14 acts at the early stage of virus replication. Treatment with iCRT14 inhibited the expression of the viral genes (vRNA, cRNA and mRNA) evaluated in this study. The intraperitoneal administration of iCRT14 reduced viral load, improved clinical signs, and partially protected mice from influenza virus infection.
    Schlagwörter Medicine ; R ; Science ; Q
    Thema/Rubrik (Code) 570
    Sprache Englisch
    Erscheinungsdatum 2018-01-01T00:00:00Z
    Verlag Public Library of Science (PLoS)
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  7. Artikel ; Online: Influenza A(H1N1)pdm09 virus suppresses RIG-I initiated innate antiviral responses in the human lung.

    Wenxin Wu / Wei Zhang / J Leland Booth / Jordan P Metcalf

    PLoS ONE, Vol 7, Iss 11, p e

    2012  Band 49856

    Abstract: Influenza infection is a major cause of morbidity and mortality. Retinoic acid-inducible gene I (RIG-I) is believed to play an important role in the recognition of, and response to, influenza virus and other RNA viruses. Our study focuses on the ... ...

    Abstract Influenza infection is a major cause of morbidity and mortality. Retinoic acid-inducible gene I (RIG-I) is believed to play an important role in the recognition of, and response to, influenza virus and other RNA viruses. Our study focuses on the hypothesis that pandemic H1N1/09 influenza virus alters the influenza-induced proinflammatory response and suppresses host antiviral activity. We first compared the innate response to a clinical isolate of influenza A(H1N1)pdm09 virus, OK/09, a clinical isolate of seasonal H3N2 virus, OK/06, and to a laboratory adapted seasonal H1N1 virus, PR8, using a unique human lung organ culture model. Exposure of human lung tissue to either pandemic or seasonal influenza virus resulted in infection and replication in alveolar epithelial cells. Pandemic virus induces a diminished RIG-I mRNA and antiviral cytokine response than seasonal virus in human lung. The suppression of antiviral response and RIG-I mRNA expression was confirmed at the protein level by ELISA and western blot. We performed a time course of RIG-I and interferon-β (IFN-β) mRNA induction by the two viruses. RIG-I and IFN-β induction by OK/09 was of lower amplitude and shorter duration than that caused by PR8. In contrast, the pandemic virus OK/09 caused similar induction of proinflammatory cytokines, IL-8 and IL-6, at both the transcriptional and translational level as PR8 in human lung. Differential antiviral responses did not appear to be due to a difference in cellular infectivity as immunohistochemistry showed that both viruses infected alveolar macrophages and epithelial cells. These findings show that influenza A(H1N1)pdm09 virus suppresses anti-viral immune responses in infected human lung through inhibition of viral-mediated induction of the pattern recognition receptor, RIG-I, though proinflammatory cytokine induction was unaltered. This immunosuppression of the host antiviral response by pandemic virus may have contributed to the more serious lung infections that occurred in the H1N1 pandemic of 2009.
    Schlagwörter Medicine ; R ; Science ; Q
    Thema/Rubrik (Code) 570 ; 610
    Sprache Englisch
    Erscheinungsdatum 2012-01-01T00:00:00Z
    Verlag Public Library of Science (PLoS)
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  8. Artikel ; Online: Features of acute COVID-19 associated with post-acute sequelae of SARS-CoV-2 phenotypes

    Al Ozonoff / Naresh Doni Jayavelu / Shanshan Liu / Esther Melamed / Carly E. Milliren / Jingjing Qi / Linda N. Geng / Grace A. McComsey / Charles B. Cairns / Lindsey R. Baden / Joanna Schaenman / Albert C. Shaw / Hady Samaha / Vicki Seyfert-Margolis / Florian Krammer / Lindsey B. Rosen / Hanno Steen / Caitlin Syphurs / Ravi Dandekar /
    Casey P. Shannon / Rafick P. Sekaly / Lauren I. R. Ehrlich / David B. Corry / Farrah Kheradmand / Mark A. Atkinson / Scott C. Brakenridge / Nelson I. Agudelo Higuita / Jordan P. Metcalf / Catherine L. Hough / William B. Messer / Bali Pulendran / Kari C. Nadeau / Mark M. Davis / Ana Fernandez Sesma / Viviana Simon / Harm van Bakel / Seunghee Kim-Schulze / David A. Hafler / Ofer Levy / Monica Kraft / Chris Bime / Elias K. Haddad / Carolyn S. Calfee / David J. Erle / Charles R. Langelier / Walter Eckalbar / Steven E. Bosinger / IMPACC Network / Bjoern Peters / Steven H. Kleinstein / Elaine F. Reed / Alison D. Augustine / Joann Diray-Arce / Holden T. Maecker / Matthew C. Altman / Ruth R. Montgomery / Patrice M. Becker / Nadine Rouphael

    Nature Communications, Vol 15, Iss 1, Pp 1-

    results from the IMPACC study

    2024  Band 17

    Abstract: Abstract Post-acute sequelae of SARS-CoV-2 (PASC) is a significant public health concern. We describe Patient Reported Outcomes (PROs) on 590 participants prospectively assessed from hospital admission for COVID-19 through one year after discharge. ... ...

    Abstract Abstract Post-acute sequelae of SARS-CoV-2 (PASC) is a significant public health concern. We describe Patient Reported Outcomes (PROs) on 590 participants prospectively assessed from hospital admission for COVID-19 through one year after discharge. Modeling identified 4 PRO clusters based on reported deficits (minimal, physical, mental/cognitive, and multidomain), supporting heterogenous clinical presentations in PASC, with sub-phenotypes associated with female sex and distinctive comorbidities. During the acute phase of disease, a higher respiratory SARS-CoV-2 viral burden and lower Receptor Binding Domain and Spike antibody titers were associated with both the physical predominant and the multidomain deficit clusters. A lower frequency of circulating B lymphocytes by mass cytometry (CyTOF) was observed in the multidomain deficit cluster. Circulating fibroblast growth factor 21 (FGF21) was significantly elevated in the mental/cognitive predominant and the multidomain clusters. Future efforts to link PASC to acute anti-viral host responses may help to better target treatment and prevention of PASC.
    Schlagwörter Science ; Q
    Sprache Englisch
    Erscheinungsdatum 2024-01-01T00:00:00Z
    Verlag Nature Portfolio
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  9. Artikel ; Online: Phenotypes of disease severity in a cohort of hospitalized COVID-19 patients

    Al Ozonoff / Joanna Schaenman / Naresh Doni Jayavelu / Carly E. Milliren / Carolyn S. Calfee / Charles B. Cairns / Monica Kraft / Lindsey R. Baden / Albert C. Shaw / Florian Krammer / Harm van Bakel / Denise A. Esserman / Shanshan Liu / Ana Fernandez Sesma / Viviana Simon / David A. Hafler / Ruth R. Montgomery / Steven H. Kleinstein / Ofer Levy /
    Christian Bime / Elias K. Haddad / David J. Erle / Bali Pulendran / Kari C. Nadeau / Mark M. Davis / Catherine L. Hough / William B. Messer / Nelson I. Agudelo Higuita / Jordan P. Metcalf / Mark A. Atkinson / Scott C. Brakenridge / David Corry / Farrah Kheradmand / Lauren I.R. Ehrlich / Esther Melamed / Grace A. McComsey / Rafick Sekaly / Joann Diray-Arce / Bjoern Peters / Alison D. Augustine / Elaine F. Reed / Matthew C. Altman / Patrice M. Becker / Nadine Rouphael

    EBioMedicine, Vol 83, Iss , Pp 104208- (2022)

    Results from the IMPACC study

    2022  

    Abstract: Summary: Background: Better understanding of the association between characteristics of patients hospitalized with coronavirus disease 2019 (COVID-19) and outcome is needed to further improve upon patient management. Methods: Immunophenotyping Assessment ...

    Abstract Summary: Background: Better understanding of the association between characteristics of patients hospitalized with coronavirus disease 2019 (COVID-19) and outcome is needed to further improve upon patient management. Methods: Immunophenotyping Assessment in a COVID-19 Cohort (IMPACC) is a prospective, observational study of 1164 patients from 20 hospitals across the United States. Disease severity was assessed using a 7-point ordinal scale based on degree of respiratory illness. Patients were prospectively surveyed for 1 year after discharge for post-acute sequalae of COVID-19 (PASC) through quarterly surveys. Demographics, comorbidities, radiographic findings, clinical laboratory values, SARS-CoV-2 PCR and serology were captured over a 28-day period. Multivariable logistic regression was performed. Findings: The median age was 59 years (interquartile range [IQR] 20); 711 (61%) were men; overall mortality was 14%, and 228 (20%) required invasive mechanical ventilation. Unsupervised clustering of ordinal score over time revealed distinct disease course trajectories. Risk factors associated with prolonged hospitalization or death by day 28 included age ≥ 65 years (odds ratio [OR], 2.01; 95% CI 1.28–3.17), Hispanic ethnicity (OR, 1.71; 95% CI 1.13–2.57), elevated baseline creatinine (OR 2.80; 95% CI 1.63– 4.80) or troponin (OR 1.89; 95% 1.03–3.47), baseline lymphopenia (OR 2.19; 95% CI 1.61–2.97), presence of infiltrate by chest imaging (OR 3.16; 95% CI 1.96–5.10), and high SARS-CoV2 viral load (OR 1.53; 95% CI 1.17–2.00). Fatal cases had the lowest ratio of SARS-CoV-2 antibody to viral load levels compared to other trajectories over time (p=0.001). 589 survivors (51%) completed at least one survey at follow-up with 305 (52%) having at least one symptom consistent with PASC, most commonly dyspnea (56% among symptomatic patients). Female sex was the only associated risk factor for PASC. Interpretation: Integration of PCR cycle threshold, and antibody values with demographics, comorbidities, and ...
    Schlagwörter COVID-19 ; SARS-CoV-2 ; Viral load ; Antibody ; Medicine ; R ; Medicine (General) ; R5-920
    Thema/Rubrik (Code) 610
    Sprache Englisch
    Erscheinungsdatum 2022-09-01T00:00:00Z
    Verlag Elsevier
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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  10. Artikel ; Online: Bacillus anthracis peptidoglycan stimulates an inflammatory response in monocytes through the p38 mitogen-activated protein kinase pathway.

    Marybeth Langer / Alexander Malykhin / Kenichiro Maeda / Kaushik Chakrabarty / Kelly S Williamson / Christa L Feasley / Christopher M West / Jordan P Metcalf / K Mark Coggeshall

    PLoS ONE, Vol 3, Iss 11, p e

    2008  Band 3706

    Abstract: We hypothesized that the peptidoglycan component of B. anthracis may play a critical role in morbidity and mortality associated with inhalation anthrax. To explore this issue, we purified the peptidoglycan component of the bacterial cell wall and studied ...

    Abstract We hypothesized that the peptidoglycan component of B. anthracis may play a critical role in morbidity and mortality associated with inhalation anthrax. To explore this issue, we purified the peptidoglycan component of the bacterial cell wall and studied the response of human peripheral blood cells. The purified B. anthracis peptidoglycan was free of non-covalently bound protein but contained a complex set of amino acids probably arising from the stem peptide. The peptidoglycan contained a polysaccharide that was removed by mild acid treatment, and the biological activity remained with the peptidoglycan and not the polysaccharide. The biological activity of the peptidoglycan was sensitive to lysozyme but not other hydrolytic enzymes, showing that the activity resides in the peptidoglycan component and not bacterial DNA, RNA or protein. B. anthracis peptidoglycan stimulated monocytes to produce primarily TNFalpha; neutrophils and lymphocytes did not respond. Peptidoglycan stimulated monocyte p38 mitogen-activated protein kinase and p38 activity was required for TNFalpha production by the cells. We conclude that peptidoglycan in B. anthracis is biologically active, that it stimulates a proinflammatory response in monocytes, and uses the p38 kinase signal transduction pathway to do so. Given the high bacterial burden in pulmonary anthrax, these findings suggest that the inflammatory events associated with peptidoglycan may play an important role in anthrax pathogenesis.
    Schlagwörter Medicine ; R ; Science ; Q
    Thema/Rubrik (Code) 571
    Sprache Englisch
    Erscheinungsdatum 2008-01-01T00:00:00Z
    Verlag Public Library of Science (PLoS)
    Dokumenttyp Artikel ; Online
    Datenquelle BASE - Bielefeld Academic Search Engine (Lebenswissenschaftliche Auswahl)

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