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Title: Bacillus anthracis spores germinate extracellularly at air-liquid interface in an in vitro lung model under serum-free conditions

Abstract

Aims: To better understand the parameters that govern spore dissemination after lung exposure using in vitro cell systems. Methods and Results: We evaluated the kinetics of uptake, germination and proliferation of B. anthracis Sterne spores in association with human primary lung epithelial cells, Calu-3, and A549 cell lines. We also analyzed the influence of various cell culture media formulations related to spore germination. Conclusions: We found negligible spore uptake by epithelial cells, but germination and proliferation of spores in the extracellular environment was evident, and was appreciably higher in A549 and Calu-3 cultures than in primary epithelial cells. Additionally, our results revealed spores in association with primary cells submerged in cell culture media germinated 1 h

Authors:
 [1];  [1];  [1];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Chemical and Biological Signature Sciences Group
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1222891
Report Number(s):
PNNL-SA-109060
400904120
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Applied Microbiology, 119(3):711-723
Additional Journal Information:
Journal Name: Journal of Applied Microbiology, 119(3):711-723
Country of Publication:
United States
Language:
English

Citation Formats

Powell, Joshua D., Hutchison, Janine R., Hess, Becky M., and Straub, Tim M. Bacillus anthracis spores germinate extracellularly at air-liquid interface in an in vitro lung model under serum-free conditions. United States: N. p., 2015. Web. doi:10.1111/jam.12872.
Powell, Joshua D., Hutchison, Janine R., Hess, Becky M., & Straub, Tim M. Bacillus anthracis spores germinate extracellularly at air-liquid interface in an in vitro lung model under serum-free conditions. United States. https://doi.org/10.1111/jam.12872
Powell, Joshua D., Hutchison, Janine R., Hess, Becky M., and Straub, Tim M. Thu . "Bacillus anthracis spores germinate extracellularly at air-liquid interface in an in vitro lung model under serum-free conditions". United States. https://doi.org/10.1111/jam.12872. https://www.osti.gov/servlets/purl/1222891.
@article{osti_1222891,
title = {Bacillus anthracis spores germinate extracellularly at air-liquid interface in an in vitro lung model under serum-free conditions},
author = {Powell, Joshua D. and Hutchison, Janine R. and Hess, Becky M. and Straub, Tim M.},
abstractNote = {Aims: To better understand the parameters that govern spore dissemination after lung exposure using in vitro cell systems. Methods and Results: We evaluated the kinetics of uptake, germination and proliferation of B. anthracis Sterne spores in association with human primary lung epithelial cells, Calu-3, and A549 cell lines. We also analyzed the influence of various cell culture media formulations related to spore germination. Conclusions: We found negligible spore uptake by epithelial cells, but germination and proliferation of spores in the extracellular environment was evident, and was appreciably higher in A549 and Calu-3 cultures than in primary epithelial cells. Additionally, our results revealed spores in association with primary cells submerged in cell culture media germinated 1 h},
doi = {10.1111/jam.12872},
journal = {Journal of Applied Microbiology, 119(3):711-723},
number = ,
volume = ,
place = {United States},
year = {Thu Jul 30 00:00:00 EDT 2015},
month = {Thu Jul 30 00:00:00 EDT 2015}
}

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Works referenced in this record:

Glutamine breakdown in rapidly dividing cells: waste or investment?
journal, January 2004


Effect of animal sera on Bacillus anthracis Sterne spore germination and vegetative cell growth: Sera effect on B. anthracis
journal, May 2012


Dendritic Cells Endocytose Bacillus anthracis Spores: Implications for Anthrax Pathogenesis
journal, April 2005

  • Brittingham, Katherine C.; Ruthel, Gordon; Panchal, Rekha G.
  • The Journal of Immunology, Vol. 174, Issue 9
  • DOI: 10.4049/jimmunol.174.9.5545

Analysis of broth-cultured Bacillus atrophaeus and Bacillus cereus spores
journal, November 2008


Lung Dendritic Cells Rapidly Mediate Anthrax Spore Entry through the Pulmonary Route
journal, June 2007

  • Cleret, Aurélie; Quesnel-Hellmann, Anne; Vallon-Eberhard, Alexandra
  • The Journal of Immunology, Vol. 178, Issue 12
  • DOI: 10.4049/jimmunol.178.12.7994

Nutrition Needs of Mammalian Cells in Tissue Culture
journal, September 1955


Characterization of the A549 Cell Line as a Type II Pulmonary Epithelial Cell Model for Drug Metabolism
journal, September 1998

  • Foster, Kimberly A.; Oster, Christine G.; Mayer, Mary M.
  • Experimental Cell Research, Vol. 243, Issue 2
  • DOI: 10.1006/excr.1998.4172

Bacillus anthracis spore interactions with mammalian cells: Relationship between germination state and the outcome of in vitro
journal, January 2011

  • Gut, Ian M.; Tamilselvam, Batcha; Prouty, Angela M.
  • BMC Microbiology, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2180-11-46

Inhalational anthrax (Ames aerosol) in naïve and vaccinated New Zealand rabbits: characterizing the spread of bacteria from lung deposition to bacteremia
journal, January 2012

  • Gutting, Bradford W.; Nichols, Tonya L.; Channel, Stephen R.
  • Frontiers in Cellular and Infection Microbiology, Vol. 2
  • DOI: 10.3389/fcimb.2012.00087

A proposed role for glutamine in cancer cell growth through acid resistance
journal, January 2013

  • Huang, Weijiao; Choi, Wooyoung; Chen, Yuling
  • Cell Research, Vol. 23, Issue 5
  • DOI: 10.1038/cr.2013.15

Early events ofBacillus anthracis germination identified by time-course quantitative proteomics
journal, October 2006

  • Jagtap, Pratik; Michailidis, George; Zielke, Ryszard
  • PROTEOMICS, Vol. 6, Issue 19
  • DOI: 10.1002/pmic.200600314

Investigation of Bioterrorism-Related Anthrax, United States, 2001: Epidemiologic Findings
journal, October 2002

  • Jernigan, Daniel B.; Raghunathan, Pratima L.; Bell, Beth P.
  • Emerging Infectious Diseases, Vol. 8, Issue 10
  • DOI: 10.3201/eid0810.020353

Metabolism of amino-acids
journal, August 1935


Spore germination
journal, March 2002

  • Moir, A.; Corfe, B. M.; Behravan, J.
  • Cellular and Molecular Life Sciences (CMLS), Vol. 59, Issue 3
  • DOI: 10.1007/s00018-002-8432-8

In Vivo Demonstration and Quantification of Intracellular Bacillus anthracis in Lung Epithelial Cells
journal, July 2008

  • Russell, B. H.; Liu, Q.; Jenkins, S. A.
  • Infection and Immunity, Vol. 76, Issue 9
  • DOI: 10.1128/IAI.00282-08

Potential dissemination of Bacillus anthracis utilizing human lung epithelial cells
journal, April 2008


Transport of Bacillus anthracis from the lungs to the draining lymph nodes is a rapid process facilitated by CD11c+ cells
journal, July 2010

  • Shetron-Rama, Lynne M.; Herring-Palmer, Amy C.; Huffnagle, Gary B.
  • Microbial Pathogenesis, Vol. 49, Issue 1-2
  • DOI: 10.1016/j.micpath.2010.02.004

Inactivation of Bacillus anthracis Spores
journal, June 2003

  • Whitney, Ellen A. Spotts; Beatty, Mark E.; Taylor, Thomas H.
  • Emerging Infectious Diseases, Vol. 9, Issue 6
  • DOI: 10.3201/eid0906.020377

Anthrax Infection
journal, December 2011

  • Sweeney, Daniel A.; Hicks, Caitlin W.; Cui, Xizhong
  • American Journal of Respiratory and Critical Care Medicine, Vol. 184, Issue 12
  • DOI: 10.1164/rccm.201102-0209CI

What Is the Relevance of Lung Epithelial Cells during the Dissemination of Spores in Inhalational Anthrax?
journal, December 2008

  • Tournier, J. -N.; Cleret, A.; Quesnel-Hellmann, A.
  • Infection and Immunity, Vol. 77, Issue 1
  • DOI: 10.1128/IAI.01160-08

Pathology of Inhalational Anthrax Animal Models
journal, July 2010


Bacillus anthracis Spore Entry into Epithelial Cells Is an Actin-Dependent Process Requiring c-Src and PI3K
journal, July 2010


Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells
journal, July 2007

  • Yuneva, Mariia; Zamboni, Nicola; Oefner, Peter
  • The Journal of Cell Biology, Vol. 178, Issue 1
  • DOI: 10.1083/jcb.200703099

Glutamine breakdown in rapidly dividing cells: waste or investment?
journal, January 2004


Early events ofBacillus anthracis germination identified by time-course quantitative proteomics
journal, October 2006

  • Jagtap, Pratik; Michailidis, George; Zielke, Ryszard
  • PROTEOMICS, Vol. 6, Issue 19
  • DOI: 10.1002/pmic.200600314

Characterization of the A549 Cell Line as a Type II Pulmonary Epithelial Cell Model for Drug Metabolism
journal, September 1998

  • Foster, Kimberly A.; Oster, Christine G.; Mayer, Mary M.
  • Experimental Cell Research, Vol. 243, Issue 2
  • DOI: 10.1006/excr.1998.4172

Spore germination
journal, March 2002

  • Moir, A.; Corfe, B. M.; Behravan, J.
  • Cellular and Molecular Life Sciences (CMLS), Vol. 59, Issue 3
  • DOI: 10.1007/s00018-002-8432-8

The alveolar macrophage: the Trojan horse of Bacillus anthracis
journal, September 2002


A proposed role for glutamine in cancer cell growth through acid resistance
journal, January 2013

  • Huang, Weijiao; Choi, Wooyoung; Chen, Yuling
  • Cell Research, Vol. 23, Issue 5
  • DOI: 10.1038/cr.2013.15

Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells
journal, July 2007

  • Yuneva, Mariia; Zamboni, Nicola; Oefner, Peter
  • The Journal of Cell Biology, Vol. 178, Issue 1
  • DOI: 10.1083/jcb.200703099

Analysis of broth-cultured Bacillus atrophaeus and Bacillus cereus spores
journal, November 2008


Potential dissemination of Bacillus anthracis utilizing human lung epithelial cells
journal, April 2008


Nutrition Needs of Mammalian Cells in Tissue Culture
journal, September 1955


Inhibition of Bacillus anthracis Spore Outgrowth by Nisin
journal, September 2008

  • Gut, I. M.; Prouty, A. M.; Ballard, J. D.
  • Antimicrobial Agents and Chemotherapy, Vol. 52, Issue 12
  • DOI: 10.1128/aac.00625-08

Updating Perspectives on the Initiation of Bacillus anthracis Growth and Dissemination through Its Host
journal, February 2012

  • Weiner, Zachary P.; Glomski, Ian J.
  • Infection and Immunity, Vol. 80, Issue 5
  • DOI: 10.1128/iai.06061-11

Cooperativity and Interference of Germination Pathways in Bacillus anthracis Spores
journal, June 2011

  • Luu, H.; Akoachere, M.; Patra, M.
  • Journal of Bacteriology, Vol. 193, Issue 16
  • DOI: 10.1128/jb.05126-11

Formation and Composition of the Bacillus anthracis Endospore
journal, December 2003


Bacillus anthracis spore interactions with mammalian cells: Relationship between germination state and the outcome of in vitro
journal, January 2011

  • Gut, Ian M.; Tamilselvam, Batcha; Prouty, Angela M.
  • BMC Microbiology, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2180-11-46

Investigation of Bioterrorism-Related Anthrax, United States, 2001: Epidemiologic Findings
journal, October 2002

  • Jernigan, Daniel B.; Raghunathan, Pratima L.; Bell, Beth P.
  • Emerging Infectious Diseases, Vol. 8, Issue 10
  • DOI: 10.3201/eid0810.020353

Inhalational anthrax (Ames aerosol) in naïve and vaccinated New Zealand rabbits: characterizing the spread of bacteria from lung deposition to bacteremia
journal, January 2012

  • Gutting, Bradford W.; Nichols, Tonya L.; Channel, Stephen R.
  • Frontiers in Cellular and Infection Microbiology, Vol. 2
  • DOI: 10.3389/fcimb.2012.00087

Establishing a Liquid-covered Culture of Polarized Human Airway Epithelial Calu-3 Cells to Study Host Cell Response to Respiratory Pathogens In vitro
journal, February 2013

  • Harcourt, Jennifer L.; Haynes, Lia M.
  • Journal of Visualized Experiments, Issue 72
  • DOI: 10.3791/50157

Dendritic Cells Endocytose Bacillus anthracis Spores: Implications for Anthrax Pathogenesis
journal, April 2005

  • Brittingham, Katherine C.; Ruthel, Gordon; Panchal, Rekha G.
  • The Journal of Immunology, Vol. 174, Issue 9
  • DOI: 10.4049/jimmunol.174.9.5545

Thermal Resistance of Spores from Virulent Strains of Bacillus anthracis and Potential Surrogates
journal, November 2005


Works referencing / citing this record:

Evolutionary conservation of the antimicrobial function of mucus: a first defence against infection
journal, July 2018

  • Bakshani, Cassie R.; Morales-Garcia, Ana L.; Althaus, Mike
  • npj Biofilms and Microbiomes, Vol. 4, Issue 1
  • DOI: 10.1038/s41522-018-0057-2